Oceanographic and Biological Aspects of the Red Sea PDF

This book includes invited contributions presenting the latest research on the oceanography and environment of the Red Sea. In addition to covering topics relevant to research in the region and providing insights into marine science for non-experts, it is also of interest to those involved in the management of coastal zones and encourages further research on the Red Sea

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Springer Oceanography

Najeeb M. A. Rasul Ian C. F. Stewart Editors

Oceanographic and Biological Aspects of the Red Sea

Springer Oceanography

The Springer Oceanography series seeks to publish a broad portfolio of scientiﬁc books, aiming at researchers, students, and everyone interested in marine sciences. The series includes peer-reviewed monographs, edited volumes, textbooks, and conference proceedings. It covers the entire area of oceanography including, but not limited to, Coastal Sciences, Biological/Chemical/Geological/Physical Oceanography, Paleoceanography, and related subjects.

More information about this series at http://www.springer.com/series/10175

Najeeb M. A. Rasul • Ian C. F. Stewart Editors

Oceanographic and Biological Aspects of the Red Sea

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Editors Najeeb M. A. Rasul Center for Marine Geology Saudi Geological Survey Jeddah, Saudi Arabia

Ian C. F. Stewart Stewart Geophysical Consultants Pty. Ltd. College Park, Adelaide, SA, Australia

ISSN 2365-7677 ISSN 2365-7685 (electronic) Springer Oceanography ISBN 978-3-319-99416-1 ISBN 978-3-319-99417-8 (eBook) https://doi.org/10.1007/978-3-319-99417-8 Library of Congress Control Number: 2018952595 © Springer Nature Switzerland AG 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, speciﬁcally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microﬁlms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a speciﬁc statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional afﬁliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

The Red Sea has a unique tectonic history, environment and biology. It is a young ocean basin that along its length has undergone or is undergoing the transition from a continental rift to true oceanic seafloor spreading, the nature of which is still open to vigorous debate. In addition, due to its semi-enclosed nature and location within an arid region, the environment is affected by high evaporation rates that, together with limited contact with the Indian Ocean, result in high temperatures and salinities. Lower sea levels in the past have also led to extensive evaporite deposition within its basin. All of this has had a far-reaching impact on the oceanography, marine and terrestrial life of the region. This is one of a pair of volumes that together follow “The Red Sea: The Formation, Morphology, Oceanography and Environment of a Young Ocean Basin” published in 2015 under our joint editorship. The amount of new information that has become available since then is testament to the range and vigour of research now being carried out in the region, much of it in Saudi Arabia under the sponsorship of the Saudi Geological Survey, and to the level of international interest. Indeed, so much new research has taken place that we have divided the material into two volumes, this one, which concentrates on aspects of the oceanography and biology of the Red Sea, and a second volume concerned with geological, palaeoenvironmental and archaeological issues. A wide range of topics is examined in this volume, and the chapters aim to present some of the current thinking and summaries of research in each ﬁeld of study, including useful reference lists for further study. As with the earlier volume referred to above, which was the outcome of a workshop held in Jeddah, Saudi Arabia, in 2013, most of the chapters in this volume were originally presented at a workshop held in Jeddah, from February 15 to February 17, 2016, under the auspices of the Saudi Geological Survey (SGS), and have been independently reviewed, revised and edited for publication. Dr. Peter Vine’s wide-ranging contributions to this volume deserve special mention. We are indebted to him for his knowledge of key topics of Red Sea ecology and in particular for assistance in preparing chapters on the Red Sea’s endemic ﬁsh and dugongs. We are pleased to include a personal perspective on some of his own studies which we hope will stimulate further research in the ﬁelds he discusses. We would also like to mention Dr. John E. Randall who is a Senior Ichthyologist Emeritus at the Bishop Museum, Honolulu, and is a co-author of the chapter on endemic ﬁshes of the Red Sea. He has been carrying out research in marine zoology since obtaining a B.A. in 1950 from UCLA and a Ph.D. in marine zoology in 1955 from the University of Hawai’i. He has received numerous awards for his work, served on the editorial board of several journals and remains as editor of the scientiﬁc series he founded, Indo-Paciﬁc Fishes. He has over 900 publications, including 13 guidebooks on ﬁshes. He has described 799 valid new species of marine ﬁshes. The support of the Survey in the preparation of this volume is greatly appreciated, and we would like to thank all those who have been involved in its production. We would especially like to thank Dr. Zohair A. Nawab, former President of SGS, and Dr. Abdullah M. Alattas, former Assistant Vice President, as well as Eng. Hussain M. Al Otaibi, President of SGS and v

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Preface

Mr. Salah A. AlSefry, Assistant Vice President for Technical Affairs. Colleagues at the SGS and the Center for Marine Geology are also thanked for making the workshop a success. Mr. Louiesito Abalos played a substantial part in the preparation of material for publication. Finally, we acknowledge the contributions of the technical referees to improving the contents of the chapters together with the assistance of Viju Falgon Jayabalan and Banu Dhayalan (Project Coordinator), Janet Sterritt-Brunner (Production Books Project Coordinator) and Dr. Nabil Khéliﬁ, (Senior Editor, of Springer Nature) in preparing this volume for publication. Jeddah, Saudi Arabia Adelaide, Australia

Najeeb M. A. Rasul Ian C. F. Stewart

Contents

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Introduction to Oceanographic and Biological Aspects of the Red Sea . . . . . . Najeeb M. A. Rasul, Ian C. F. Stewart, Peter Vine and Zohair A. Nawab

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The Tides of the Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . David T. Pugh, Yasser Abualnaja and Ewa Jarosz

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Physical and Chemical Properties of Seawater in the Gulf of Aqaba and Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Riyad Manasrah, Ahmad Abu-Hilal and Mohammad Rasheed

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Sources of Organic Tracers in Atmospheric Dust, Surface Seawater Particulate Matter and Sediment of the Red Sea . . . . . . . . . . . . . . . . . . . . . . . Ahmed I. Rushdi, Zanna Chase, Bernd R. T. Simoneit and Adina Paytan

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Nitrogen, Phosphorus and Organic Carbon in the Saudi Arabian Red Sea Coastal Waters: Behaviour and Human Impact . . . . . . . . . . . . . . . . . Radwan Al-Farawati, Mohamed Abdel Khalek El Sayed and Najeeb M. A. Rasul

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Automatic Detection of Coral Reef Induced Turbulent Boundary Flow in the Red Sea from Flock-1 Satellite Data . . . . . . . . . . . . . . . . . . . . . . . 105 Maged Marghany and Mohamed Hakami

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Red Sea Coastal Lagoons: Their Dynamics and Future Challenges . . . . . . . . 123 Alaa M. A. Albarakati and Fazal Ahmad

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Distribution and Sources of Hydrocarbon Compounds in Sediments from Obhur Lagoon: Red Sea Coast of Saudi Arabia . . . . . . . . . . . . . . . . . . . 133 Ahmed I. Rushdi, Najeeb M. A. Rasul, Abdulgader Bazeyad and Ramil Dumenden

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Metal Contamination Assessment in the Sediments of the Red Sea Coast of Saudi Arabia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 Manikandan Karuppasamy, Mohammad Ali B. Qurban and Periyadan K. Krishnakumar

10 Calcite and Aragonite Saturation Levels of the Red Sea Coastal Waters of Yemen During Early Winter and Expected pH Decrease (Acidiﬁcation) Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171 Ahmed I. Rushdi, Aarif H. El-Mubarak and Khalid F. Al-Mutlaq 11 Geochemistry and Life at the Interfaces of Brine-Filled Deeps in the Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185 André Antunes, Stein Kaartvedt and Mark Schmidt 12 Desalination of Red Sea and Gulf of Aden Seawater to Mitigate the Fresh Water Crisis in the Yemen Republic . . . . . . . . . . . . . . . . . . . . . . . . . 195 Angelo Minissale, Dornadula Chandrasekharam and Mohamed Fara Mohamed Al-Dubai vii

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13 Red Sea Research: A Personal Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215 Peter Vine 14 Endemic Fishes of the Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 Sergey V. Bogorodsky and John E. Randall 15 Red Sea Sharks—Biology, Fisheries and Conservation. . . . . . . . . . . . . . . . . . . 267 Julia L. Y. Spaet 16 Review of Cetaceans in the Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281 Marina Costa, Maddalena Fumagalli and Amina Cesario 17 Where Dolphins Sleep: Resting Areas in the Red Sea . . . . . . . . . . . . . . . . . . . 305 Maddalena Fumagalli, Amina Cesario and Marina Costa 18 Status of Red Sea Dugongs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 327 Dirar Nasr, Ahmed M. Shawky and Peter Vine 19 Spatial Patterns of Standing Stock and Diversity of Macrobenthic Communities in the Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 355 Thadickal V. Joydas, Mohammad Ali B. Qurban, Manikandan Karuppasamy, Lotﬁ Rabaoui and Periyadan K. Krishnakumar 20 Seagrass Distribution, Composition and Abundance Along the Saudi Arabian Coast of Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 367 Mohammad Ali B. Qurban, Manikandan Karuppasamy, Periyadan K. Krishnakumar, Neus Garcias-Bonet and Carlos M. Duarte 21 Current Knowledge of Coral Diseases Present Within the Red Sea. . . . . . . . . 387 Amin R. Mohamed and Michael Sweet 22 Physicochemical Dynamics, Microbial Community Patterns, and Reef Growth in Coral Reefs of the Central Red Sea . . . . . . . . . . . . . . . . . 401 Anna Roik, Maren Ziegler and Christian R. Voolstra 23 Meiofauna of the Red Sea Mangroves with Emphasis on Their Response to Habitat Degradation: Sudan’s Mangroves as a Case Study . . . . . . . . . . . . . 419 Ahmed S. M. Khalil 24 Morphology and Anatomy of the Pearl Oyster, Pinctada margaritifera in the Red Sea: A Case Study from Dungonab Bay, Sudan . . . . . . . . . . . . . . . 437 Dirar Nasr 25 Copepoda—Their Status and Ecology in the Red Sea . . . . . . . . . . . . . . . . . . . 453 Ali M. Al-Aidaroos, Mohsen M. El-Sherbiny and Gopikrishna Mantha 26 Zooplankton of the Red Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477 Maher A. Aziz Amer 27 Phytoplankton and Primary Production in the Red Sea . . . . . . . . . . . . . . . . . . 491 Mohammad Ali B. Qurban, Mohideen Wafar and Moritz Heinle 28 The Role of Citizen Science in Monitoring Megafauna of the Red Sea . . . . . . 507 Agnese Mancini and Islam M. Elsadek Authors’ Biography. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521 Reviewers’ List . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543

Contents

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Introduction to Oceanographic and Biological Aspects of the Red Sea Najeeb M. A. Rasul, Ian C. F. Stewart, Peter Vine and Zohair A. Nawab

Location, Bathymetry and Statistics This volume builds on the success of a previous publication, “The Red Sea: The Formation, Morphology, Oceanography and Environment of a Young Ocean Basin”, edited by Rasul and Stewart (2015), in which an extensive introduction (Rasul et al. 2015) outlined the main features of the Red Sea, including aspects of the oceanography and biology which will not be repeated here in detail. The Red Sea is a semi-enclosed, elongated body of relatively warm water, about 2000 km long with a maximum width of 355 km, a surface area of roughly 458,620 km2, and a volume of *250,000 km3 (Head 1987). The Red Sea is bounded by nine countries, with numerous coastal lagoons, a large number of islands of various dimensions and extensive groups of shoals; it is bifurcated by the Sinai Peninsula into the Gulf of Aqaba and the Gulf of Suez at its northern end (Fig. 1.1). The sea is connected to the Arabian Sea and Indian Ocean via the Gulf of Aden in the south through the narrow Strait of Bab el Mandab, which has a minimum width of only 30 km, where the main channel is about 310 m deep and 25 km wide at Perim Island (Morcos 1970). Although the Hanish Sill at 13°44′N has a maximum depth of only 137 m, it is likely that the Red Sea has remained connected to the Gulf of Aden for at least the past 400,000 years (Lambeck et al. 2011). However, during the N. M. A. Rasul (&) Center for Marine Geology, Saudi Geological Survey, Jeddah, Saudi Arabia e-mail: [email protected]; ; [email protected] I. C. F. Stewart Stewart Geophysical Consultants Pty. Ltd., Adelaide, SA, Australia P. Vine Earth and Ocean Sciences, School of Natural Sciences, NUI Galway, Galway, Ireland Z. A. Nawab Saudi Geological Survey, Jeddah, Saudi Arabia

Last Glacial Maximum (LGM), the water depth over the Hanish Sill is estimated to have fallen to only 25–33 m (Biton et al. 2008; Lambeck et al. 2011), with considerable effects on the Red Sea circulation and ecology (Trommer et al. 2011). The Red Sea has three distinct depth zones; shallow shelves less than 50 m in depth (about 25%), deep shelves with depths ranging between 500 and 1000 m, and the central axis with depths between 1000 and about 2900 m. The continental slope has an irregular proﬁle, with a series of steps down to about 500 m depth. The 15% of the Red Sea that forms the narrow axial trough is over 1000 m in depth and contains a number of bathymetric depressions or Deeps, some containing hot saline brines (e.g., Hovland et al. 2015) and metalliferous sediments that were formed by the spreading of the sea. Recent data along the axis (Augustin et al. 2014) suggest that the western Suakin Deep, with a depth of 2860 m at 19.6° N is the deepest part of the Red Sea Rift. The seismically active Gulf of Aqaba is 160–180 km long and 19–25 km wide, narrow in the north and widening to the south with maximum depths of 1850 m toward the east, where shelves and coastal plains are absent. The Gulf of Suez is a 300 km long, 25–60 km wide, shallow flat bedded basin with depths ranging between 50 and 75 m. Depths increase toward the south but remain under the 100 m mark at the confluence of the Red Sea and do not exceed 200 m. The Red Sea is one of the youngest oceanic zones on earth, and along most of its length it forms a rift through the Precambrian Arabian-Nubian shield. The southern end of the Red Sea joins the Gulf of Aden spreading centre and the northern end of the East African Rift Zone at a triple junction in the Afar region, an area with extensive volcanism. In the early stages of rifting, prior to a permanent connection to the Gulf of Aden, thick evaporite deposits accumulated in the Red Sea, and on the shelf and marginal areas these deposits are overlain by recent sediments. The sea only turned into an open marine environment when the Gulf of Suez in the north and Indian Ocean in the south became connected in the Pliocene.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_1

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Fig. 1.1 Geographic map of the Red Sea area, where darker colours indicate greater depths or higher elevations (after Rasul and Stewart 2015)

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Introduction to Oceanographic and Biological Aspects …

Chapters in this Volume This volume is arranged into two main sections, the ﬁrst dealing with the Red Sea’s oceanography and the second covering biological research. It has been built around a workshop (held in 2016) hosted by the Saudi Geological Survey and includes contributions from experts working in Saudi Arabia, Egypt, Sudan, India, the United Kingdom, Ireland, France, Russia, the United States, New Zealand, Hong Kong, Italy, and the Falkland Islands. Despite this eclectic mix of Red Sea related topics, reflecting divergent lines of active research, there are several overlapping themes, in particular the fact that there are more questions than answers in our present knowledge of Red Sea marine biology.

Oceanography Eleven chapters deal with various aspects of the Red Sea’s oceanography, including tidal movements, properties of sea water, organic tracers in sediments, nitrogen, phosphorus and carbon in coastal waters, satellite studies on coral reef induced turbulence, the dynamics of coastal lagoons, hydrocarbons in Obhur lagoon sediments, metal contaminants in Saudi Arabia’s coastal waters, calcite and aragonite saturation levels in Yemen’s coastal waters, the geochemistry of brine-ﬁlled deeps, and desalination in Yemen. The Red Sea’s tidal movements are relatively small with semi-diurnal spring tides reaching a vertical range of about metre at the northern and southern extremities and “a central amphidrome, zero tidal range, between Jeddah and Port Sudan”. David Pugh and his colleagues have created a new tidal model for the Red Sea. This is the ﬁrst publication of their data and the model they produced is: (i) depth integrated and two dimensional, (ii) driven by Indian Ocean tidal boundary levels and eight tidal constituents, (iii) has a much higher resolution than any previous models, (iv) was run for a year to give high resolution of tidal frequencies, and (v) has a depth-independent friction drag coefﬁcient of 0.003. They used the model to compare with actual readings inside and outside the Red Sea, and conclude that “future modelling, necessarily three-dimensional, may address and incorporate the impact of direct gravitational forcing, and reduce small but systematic differences for observations. Meanwhile, the results published here represent a major advance on any previously published tidal representations”. Red Sea waters are well known for their clarity, especially in the northern Gulf of Aqaba. Manasrah and his co-workers examine the physical and chemical properties of seawater in the Gulf and Red Sea and provide a comprehensive presentation on the forces at work in shaping these

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waters, from meteorology to physical and chemical oceanography. The importance of a thermocline in maintaining the oligotrophic nature of surface waters is mentioned repeatedly and often in the context of there being a a seasonal cycle of stratiﬁcation in spring, maintenance of a shallow thermocline in summer, and subsequent deepening of the thermocline to produce “deep mixed layers in winter”. Some of the facts presented demonstrate key characteristics of the Gulf of Aqaba where evaporation amounts to between 0.5 and 1.0 cm per day; the pH is fairly constant at around 8.3 due to the buffering effects of calcium carbonate deposited by corals, and higher salinity levels result in density gradients. Higher concentrations of nutrients, chlorophyll a, ammonium, nitrates, nitrite, phosphates, and silicates in the Gulf of Aqaba in winter—due to mixing of the water column—all contribute toward enhanced primary productivity, resulting in higher phytoplankton abundance and increased chlorophyll a concentrations. Meanwhile, the authors comment that oxygen levels in the Gulf show a regular pattern, inversely proportional to that of temperature, exhibiting a well-balanced proﬁle in terms of respiration and photosynthesis and a high level of ventilation (mostly 100%) “due to annual deep mixing”. Rushdi and colleagues present a study and analysis on the sources of externally derived organic matter in the Red Sea. In order to do so they sampled dust, surface sea water particulate matter and coastal sediments, examining the extractable organic matter (EOM). Their ﬁndings are based on key parameters and molecular marker analysis enabling them to deduce the likely source of the various inputs, many of which are from natural sources such as plant debris. Dust is a major carrier with six million tons deposited into the Red Sea each year. In fact, the regional dust belt associated with low-latitude African and Asian deserts is the largest source of dust on our planet. Dust storms, that can be common in summer along both coastlines, carry vast quantities of nutrients, impacting oligotrophic waters such as those of the northern Red Sea. Whilst storms are natural events, they may carry pollutants resulting from human activities. An assortment of chemical compounds associated with dust and surface sediments were used to identify the likely source of associated pollutants. The compounds are mainly n-alkanes from both natural and anthropogenic sources, n-alkanoic acids, n-alkanols, methyl n-alkanoates, steroids, hopanes, steranes and UCM (unresolved complex mixture of branched and cyclic hydrocarbons) from petroleum inputs, and plasticizers which are all from anthropogenic sources. The presence of n-alkanes indicated un-degraded crude oil, whilst petroleum products in general are indicated by the biomarkers hopane and sterane hydrocarbons. Plasticizers can be released to the environment due to bio- and photo-degradation and are present in the dust. Overall, the authors concluded that both natural and anthropogenic components contribute to organic

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inputs in the Red Sea. The latter are most important in sediments where, depending on the location and types of human activity, they can exceed 30%. The Red Sea is generally nutrient deﬁcient (oligotrophic) and depends on inflow from the Indian Ocean, via Bab al Mandab, for most of its nitrogen and phosphorus. Concentrations of these decline northward, with peaks near coastal cities such as Jeddah where the impact of effluent outflows and industrial activities can be observed. Al-Farawati and his colleagues present their ﬁndings regarding the distribution, sources, and biogeochemical processes that control levels of dissolved inorganic phosphorus, dissolved inorganic nitrogen (nitrates, nitrites, ammonium) and dissolved organic carbon (DOC). They also calculated the contribution to the total nitrogen-phosphorus budget from anthropogenic sources. There is a distinct seasonality in dissolved and particulate carbon levels (DOC and POC), connected to peaks in primary production, with higher values in late spring. Nitrogen levels were dominated by ammonium in autumn (60% of total inorganic nitrogen, TIN) and nitrates in spring (62% of TIN). Anthropogenic nitrogen and phosphorus, mostly associated with sewage discharges into Jeddah’s coastal waters, account for 0.9% and 9.9% respectively of the deﬁcit of the two elements through the Red Sea/Indian Ocean exchange process at the Strait of Bab al Mandab. These elements are directly linked to the capacity of the water-body to support phytoplankton which deplete dissolved levels of nitrogen and phosphorus—potentially limiting factors for primary production. Exhaustion of nitrogen or phosphorus stops development of phytoplankton whilst exhaustion of silicate stops development of diatoms. The authors point out the importance of correctly identifying the limiting nutrient in coastal waters since it can determine the type of sewage treatment most appropriate for each situation. In turn, this will help to minimise costs and reduce ecological impact of sewage effluent on coastal marine life. They do however point to various difﬁculties with determining which nutrients are limiting factors and urge caution in reaching conclusions in this regard. The use of optical remote sensing systems to map and monitor surface and shallow water topography is well established but has been limited by a number of factors, ranging from availability and access to suitable satellites, to regularity and resolution of the images produced, effects of weather (especially cloud cover), water clarity (impacted by plankton and turbulence), limitations of depth penetration, and the need for proven algorithms that deliver reliable detection of selected criteria. Marghany and Hakami tested the suitability of the relatively new Flock-1 satellite system, launched in 2014 (comprising 28 tiny satellites), to detect the locations and main characteristics of some Red Sea coral reefs. This was the ﬁrst time that Flock-1 had been used for oceanographic surveys. They subjected the data to a ‘multi

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objective evolutionary algorithm’ (MOEA) developed to automatically detect the patterns of water disturbance (‘turbulent boundary flow’) overlying coral reefs—mainly on the Al-Wajh bank and Farasan Islands, off Saudi Arabia. Their results underline the ‘added value’ that can be gained from Flock-1 with potential implications for maritime activities including shipping and ﬁshing together with sediment and pollution tracking. The authors examined two hypotheses; ﬁrstly, that low radiometric resolution data such as that produced by Flock-1 can be used for surface and benthic coral features detection, and secondly that such machine learning and intelligent algorithms are able to accurately detect dynamic interactions between sea surface movement and benthic features such as coral reefs. The Flock-1 satellites, each measuring 30 10 10 cm, are equipped with cameras capable of taking pictures with a ground resolution of 3–5 m and visible spectra of 400–660 nm and near infrared 700–900 nm. In order to ground truth their results, the team used maps of Saudi Arabian coral reefs published in the Khaled bin Sultan Living Oceans Foundation Atlas of Saudi Arabian Red Sea Marine Habitats. When it comes to automatically detecting the water movements created by the hugely varied forms of coral reefs there is no ‘one size ﬁts all solution’. Instead the authors developed an MOEA that preserved the diversity of the solution set. Overall, the authors present a compelling case for greater use of Flock-1 data in Red Sea reef studies, using an MOEA. Moving from offshore reefs and shoals to coastal indentations in the form of lagoons, the characteristics of coastal lagoons, both in general and with particular reference to the Saudi Arabian Red Sea, are described by Albarakati and Ahmad. They studied water column conditions of Rabigh lagoon and the flushing times of Shoaiba, Obhur, Ras Hatiba, Rabigh and Yanbu. In Rabigh they found that the water column remains mixed (rather than stratiﬁed) throughout most of the year, with the possible exception of September to October when a weak stratiﬁcation may appear. Flushing times of the various lagoons ranged from a few days to a month. Coastal lagoons can be among the most productive ecosystems in the biosphere. Turning to Saudi Arabia’s coastal lagoons, they emphasise the high levels of biological productivity in these increasingly threatened environments and call for more studies and constant monitoring in order to ameliorate the stresses caused by human activities. Coastal lagoons of the Red Sea receive waste from the increasing levels of anthropogenic activity and some are used as intakes for desalination plants. “They contain different types of vegetated habitats, such as sea grasses or mangroves, which should be preserved as natural grounds for productivity.” The present levels of stress will rise even higher as a result of climate change and global warming. The authors call for involvement of a “wide variety of institutes and administrative units as well as research in a range of scientiﬁc

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Introduction to Oceanographic and Biological Aspects …

disciplines in association with those involved with the lagoons.” Ahmed Rushdi and his colleagues analysed surface sediment samples from Obhur Lagoon on the Red Sea coast of Saudi Arabia to determine the levels, distribution and sources of hydrocarbon compounds, the main sources of which were anthropogenic petroleum products and plasticizers, with lesser amounts from biogenic sources, including natural waxes of terrestrial higher plants and marine microbial detritus. The anthropogenic inputs of the total lipid hydrocarbons for all sediments ranged from 14 to 98% for petroleum products and from 2 to 18% for plasticizers, and biogenic inputs ranged from 0 to 10.7% for terrestrial higher plant waxes and from 0 to 68.5% for marine microbial detritus. The petroleum residues and plasticizers in the sediments probably affect the marine ecosystems and associated species groups that use the lagoon as a coastal nursery and spawning area. Further offshore, Karuppasamy et al. analysed surﬁcial sediment samples from sixty stations between 23oN and 28oN latitudes in the northern Red Sea for 10 metals. Arsenic was the only element to exhibit exceedance with 88% of the stations above upper continental crust concentrations. A sediment contamination assessment was carried out using the geoaccumulation index (Igeo) and enrichment factor (EF), and the ecological hazard was assessed using the Adverse Effect Index (AEI), Potential ecological risk factor (ER) and Potential ecological index (RI). Using statistical analyses, the stations were grouped as “uncontaminated”, “minor enrichment”, “metallogenic enrichment” and “anthropogenic enrichment”. Seawater samples from different depths at eight stations along the Red Sea coast of Yemen were collected by Rushdi et al. during early winter for the determinations of the temperature, salinity, pH value and total alkalinity proﬁles. The results showed that the surface seawater layers were several-fold supersaturated with respect to both calcite and aragonite and suggest that low magnesian calcite and aragonite are likely the major carbonate solid phases formed under current saturation levels. Recent studies show that the present oceanic pH values may drop by 0.1 and 0.4 units in 50 and 200 years, respectively. This will affect the morphology and mineralogy of calcium carbon deposits as well as the distribution of calcifying organisms in the region. Further studies are warranted to investigate the occurrence, distribution and mineralogy of corals and the effects of physical and chemical parameters upon their growth in the region. Antunes et al. investigate the geochemistry and life at the interfaces of the brine-ﬁlled deeps in the Red Sea where the extreme environments form characteristically steep gradients across the brine-seawater interfaces. Due to their unusual nature and unique combination of physical-chemical

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conditions these interfaces provide an interesting source of new ﬁndings in the ﬁelds of geochemistry, geology, microbiology, biotechnology, virology, and general biology. Turning to onshore water matters, Minissale et al. examine the consumption and uses of water in Yemen, which has a declining water table with the Mesozoic-Cenozoic aquifer unable to support irrigation and the geothermal reservoir too will decline due to excessive withdrawal of water. A solution to this problem is to develop the geothermal resources around Damt and Dhamar to support desalination of the Red Sea and Gulf of Aden seawater to generate electricity and fresh water to contribute to the country’s food and energy security and reduce dependence on food imports.

Biology The biology section of this volume is a valuable contribution to our knowledge and understanding of this fascinating marine biosphere, with sixteen chapters throwing light on such divergent, yet interconnected, topics as Crown of Thorns starﬁsh, algal-coral and sponge-coral interfaces, the ecological impact of aggressive damsel ﬁsh, endemic ﬁshes, sharks, cetaceans, dugongs, macrobenthos, seagrasses, coral diseases, microbial activity, mangroves, pearl oysters, copepods, zooplankton, phytoplankton, turtles and, most appropriately, the growing role of ‘citizen science’. Studies of Crown of Thorns starﬁsh, aggressive damselﬁsh, pink coralline algae and the ‘turf wars’ that take place between corals, sponges and algae are all covered in a reflective chapter by Peter Vine that looks back at some early research in these ﬁelds and shows how our understanding of the dynamics of reef ecology has advanced. Perhaps of greatest importance in this chapter is the author’s highlighting of the important role played by crustose coralline algae, CCA, not just in binding the reef structure, but also in providing suitable settlement surfaces on reefs where voracious cnidarians pose a threat to most larval forms in search, excuse the anthropogenic assumption, of a ‘safe home’. The present number of ﬁshes recorded from the Red Sea is 1166 species from 159 families whose habitats range from shallow to deep waters; among these 165 species are exclusively endemic to the Red Sea. The authors of the chapter on endemic Red Sea ﬁshes are themselves record breakers: Dr. J.E. Randall, still contributing to scientiﬁc literature at the age of 94, and Sergey Bogorodsky, a much younger man with a passion for his subject that is complimented by an attention to taxonomic detail and a high level of photographic expertise. Randall’s statistics are noteworthy with 902 published papers, 48 of which are on Red Sea ﬁshes. He has described and named 799 new species of ﬁsh and has written 13 regional ﬁsh guides, including “Red Sea

6

N. M. A. Rasul et al.

Reef Fishes” that is a must-have book for Red Sea divers and marine scientists. Most of his work is accompanied by sharply focused and expertly lit photographs of fresh specimens with the ﬁns carefully pinned out to enable identiﬁcation. Several species of ﬁsh that are commonly found in the Red Sea are shown in Figs. 1.2, 1.3, 1.4 and 1.5. Julia Spaet calls for urgent regional efforts to assess the status of Red Sea sharks, and the development and implementation of “effective management plans to ensure socio-ecological sustainability”. The author notes the presence of 29 shark species in the Red Sea and summarises what is known of these species. She makes a strong case for further studies and conservation efforts before some of the most threatened species disappear from these waters. It is a similar story with cetaceans, of which at least 16 species are found in the Red Sea, and Marina Costa and colleagues point out that we still do not have a clear picture

Fig. 1.3 Juvenile of the Yellowbar Angelﬁsh, Pomacanthus maculosus, occurs in the Red Sea (type locality, Luhaiya, Yemen), east to the Gulf of Oman and Arabian Gulf, south to Mozambique and the Seychelles, and has even been reported from the Mediterranean Sea by Bariche (2010). It usually occurs on sheltered, often silty, coral reefs, at depths of 4–20 m. It is solitary and adults are easily approached. Feeds on sponges and algae. Photo © Hans Sjoeholm

Fig. 1.2 The blue masked butterflyﬁsh, Chaetodon semilarvatus, ranges from the Red Sea (type locality, Massawa) and Gulf of Aden to southern Oman. It inhabits reefs of rich coral growth from depths of about 1–20 m and is often seen in pairs, occasionally in small aggregations. It tends to be inactive most of the day, hovering beneath ledges or plates of Acropora corals, feeding on polyps of hard and soft corals late in the afternoon (pers.comm. JE Randall and S Bogorodsky). Photo © Hans Sjoeholm

of the Red Sea’s whales and dolphins, particularly in the central and southern areas. They say that there is an “urgent need for a more up-to-date appraisal of cetaceans, including the presence, abundance, distribution and behaviour of represented species throughout the Red Sea” and state that there is a “duty of care for governments, NGOs and academic institutions within the region to support and facilitate the research required to acquire a better understanding of the Red Sea’s whales and dolphins.” Meanwhile, Maddalena Fumagalli and colleagues throw more light on one of the erstwhile ‘unknowns’ of Red Sea dolphins: where and when do they sleep? They point out that disturbance by humans, in for example tourist dolphin watch boats, can lead to sleep deprivation, impacting individual physiology and cognitive abilities. This can have “long term detrimental consequences on wild dolphin populations”. In the Red Sea the authors state that scientiﬁc studies on the impacts on dolphins are still preliminary, but the Samadi

1

Introduction to Oceanographic and Biological Aspects …

Fig. 1.4 Harlequin ﬁleﬁsh Oxymonacanthus halli and Rueppell’s wrasse Thalassoma rueppellii over an outcrop of coral. The harlequin ﬁleﬁsh is endemic to the Red Sea; type locality, Sanaﬁr Island, Gulf of Aqaba. It occurs on reefs with luxuriant coral growth in lagoons, bays and sheltered seaward reefs from depths of 0.5–30 m; usually seen in pairs among branches of Acropora corals; feeds on coral polyps; also takes refuge in ﬁre coral (Millepora). Closely related to Oxymonacanthus longirostris (Bloch & Schneider), wide-ranging in the rest of the Indo-Paciﬁc region. Rueppell’s wrasse is also endemic to the Red Sea; type locality, El Quseir. It occurs on coral reefs and adjacent habitats from 0.5 to 20 m and is reported to feed mainly on benthic invertebrates, occasionally on small ﬁshes. It is unafraid of divers, apparently attracted to the disturbances they often make to the substratum (pers.comm. JE Randall and S Bogorodsky). Photo © Hans Sjoeholm

Reef protection zone in Egypt is setting an example of how to manage this issue. They highlight the importance of identifying and protecting well established dolphin resting areas. The chapter by Nasr et al. on dugongs highlights the extent to which we are still guessing at important issues such as population status of these herbivorous marine mammals in the Red Sea. It also demonstrates what can be achieved by the concentrated efforts of a few individuals over a relatively short period of time. Hopefully, the recent survey work carried out in Egypt will be extended to other countries bordering the Red Sea. The authors repeat the assertion of

7

Fig. 1.5 The Crown Butterflyﬁsh (Chaetodon paucifasciatus) is known only from the Red Sea (type locality, El Quseir, Egypt) and the Gulf of Aden where it is found on coral reefs and adjacent habitats at depths from 1 to 30 m, usually in pairs, sometimes in small groups. Omnivorous, feeding on polyps of hard and soft corals, algae, small crustaceans, and polychaete worms (pers.comm. JE Randall and S Bogorodsky). Photo © Hans Sjoeholm

previous expert studies that have described our overall knowledge of Red Sea dugongs as ‘Data Deﬁcient’—an admission that reflects disappointingly on the administration of research on dugongs in this region over the past few decades. Emphasis on gaps in our knowledge and calls for further studies in their particular ﬁelds were made by several other authors. Thadickal Joydas and co-authors remind us that despite their importance and the unique characteristics of their habitat (high temperature, high salinity, oligotrophic conditions) “benthic studies conducted in the deep-sea environments of the Red Sea are few”. Turning to shallow water habitats Mohammad Qurban and co-workers provide an overview of the presence and distribution of seagrasses in the Red Sea. They too point to the dearth of scientiﬁc literature in this ﬁeld, stating that “there is little information on seagrass diversity and distribution in the Saudi Arabian coast of the Red Sea”.

8

The theme is reiterated by Amin Mohamed and Michael Sweet who review current knowledge of coral diseases in the Red Sea. They write that “despite their reported signiﬁcance in reefs around the world, the aetiologies of the majority of diseases are still unknown and coral epidemiology remains poorly understood”. Initial triggers for coral diseases, frequently involving bacteria, viruses, fungi or protozoa, are abiotic factors such as temperature, UV exposure or pollution, and the impact of coral predation resulting in feeding scars. It seems that “diseases affecting corals throughout the Red Sea are one of the least well explored and documented.” Anna Roik and colleagues present a study that highlights the physical and chemical impact on microbial community patterns which, in turn, affect coral reef growth. Their observations of the surface coverage of bacteria and algae— the “epilithic bioﬁlm”—“crucial for the recruitment of reef-builders” shows how these are influenced by seasonally variable factors such as temperature, salinity, and dissolved oxygen. Bacteria from the genus Endozoicomonas are particularly prevalent in central Red Sea corals and are sensitive to anthropogenic disturbances, thus providing an early warning of the impact of humankind on the Red Sea’s reefs. Meanwhile, endosymbiotic dinoflagellates in central Red Sea corals, vital for driving the calciﬁcation (and reef growth) process, are dominated by Symbodinium. They note that reef growth slows during summer months, probably because sea temperatures approach the upper tolerance levels for their symbiotic algae (“as evidenced by repeated mass-bleaching events during recent years”). Such baseline studies provide valuable frameworks for understanding the influences at play in terms of the ebb and flow of coral development and “for quantiﬁcation of the impacts of environmental change in the region”. In addition to corals and sea-grasses, the Red Sea’s sheltered bays and shorelines are natural habitats for mangrove trees that play a vital role in creating organic rich habitats for juvenile ﬁsh and crustaceans. Unfortunately, coastal development projects have paid little heed to the environmental contribution that mangroves make to the marine ecosystem. Ahmed Khalil has studied the small benthic invertebrates (meiofauna) that live in association with Sudan’s mangroves, including species of copepods, nematodes, ostracods, mud-dragons (Kinorhyncha), worms (Oligochaeta), flatworms (Platyhelminthes), jaw worms (Gnathostomulida), hairybacks (Gastrotricha) and cnidarians. He looked in particular at what happens to this diverse meiofaunal community when mangrove trees are chopped down and partially or completely cleared. Deforested sites had higher densities of copepod/nauplii and decreased nematodes. An increase in abundance of many forms was noted in the partially deforested sites. Removing mangroves caused a “decline in the efﬁciency of the ecosystem function as a nursery ground for marine organisms, which represents

N. M. A. Rasul et al.

one of the vital services provided by the mangrove ecosystem.” Among the larger species that are sometimes found clinging to the roots of mangroves is the pearl oyster, Pinctada margaritifera, which has been the subject of several mariculture projects in Dungonab Bay on Sudan’s northern Red Sea coastline. Spat are collected on ropes suspended from rafts in July and August and are then transferred to nursery trays. They are held in these until they are ready for on-growing in larger trays near Dungonab village. Biological research on Sudan’s pearl oysters has been carried out over many years by the author of this chapter, Dirar Nasr, who presents the most recent observations on the species, based primarily on his own research. Heavy settlement of oyster spat in Dungonab Bay is a quite unusual feature, not seen elsewhere in the Red Sea and possibly unique in terms of the scale of larval settlement of P. margaritifera throughout its range. It contrasts quite sharply with the situation regarding plankton elsewhere in the Red Sea where oligotrophic conditions do not generally favour such impressive planktonic concentrations. Two chapters in this publication take a timely look at plankton of the Red Sea. Ali Al-Aidaroos and colleagues present their ﬁndings on that most important link in the food chain, Copepoda, and Maher Amer presents a more general review of the zooplankton. An important source of the Red Sea’s plankton is the Indian Ocean whose waters in areas adjacent to the southern entrance of the Red Sea are recipients, via upwelling, of nutrient rich colder water. Carried into the Red Sea on northward flowing waters, these oceanic zooplankters encounter increasingly hostile conditions in terms of raised salinity and temperatures, compounded by decreased nutrient levels. These distinctive environments tend to promote endemicity in those forms that are adapted to meet the environmental challenges of the central and northern Red Sea. The important role played by copepods in linking primary producers with secondary consumers can hardly be over-emphasised. They are an extremely diverse group found in almost every available habitat. Over 970 species of planktonic copepods occur in the Indian Ocean with 276 found, according to this recent study by Al-Aidaroos and colleagues, in the Red Sea. Indeed, “the epipelagic zone in the Red Sea is usually dominated by copepods”, particularly in the southern half of the Red Sea during winter months when mesozooplankton are at their peak. The authors show how copepods are vulnerable to Ultraviolet-B radiation and may symbiotically influence growth and development of the Red Sea’s coral reefs and their associated biota. Contrasting with most topics covered in this volume, the author of ‘Zooplankton of the Red Sea’, Maher Amer, is able to direct the reader’s attention to a signiﬁcant number of studies, dating back to the beginning of the 19th century,

1

Introduction to Oceanographic and Biological Aspects …

including a number of major oceanographic expeditions. He lists 111 references and presents results from his own plankton sampling in the northern Red Sea. It is generally agreed that there is a decline in neritic species from south to north, and also that demersal plankton are most abundant in close proximity to coral reef patches as opposed to open water. The abundance of plankton in shallow depths is also much greater at night time. Furthermore, in accordance with other studies, it was found that copepods were the most abundant group among demersal zooplankton, accounting for 58.7% of the total, highlighting their importance in the food chain. The few studies on phytoplankton and primary production in the Red Sea mostly cover only limited areas. Qurban et al. review previous studies and show that the levels of biomass and production in the Red Sea are relatively low, with a north-south gradient and a distribution that is influenced by anticyclonic eddies, in which biomass and production are twice as high as those elsewhere, suggesting that the notion that the Red Sea is oligotrophic needs to be revised. The phytoplankton diversity is quite high, and with additional records of 74 species from the samples in four cruises, the current inventory of phytoplankton stands at 463 species. The review also suggests prospective avenues of phytoplankton research in the Red Sea waters. The manner in which data for science is gathered has changed over the centuries. Increasingly, scientists are tapping into the time, knowledge, expertise, enthusiasm and opportunity that untrained or lightly supervised ‘amateurs’ can bring to various ﬁeld studies. In addition to increased use of monitoring tools such as audio-visual recording and aerial drone surveys, the introduction of ‘citizen scientists’ can create valuable data sets in some of the most remote or difﬁcult habitats. This theme is explored by Agnese Mancini and Islam Elsadek in their presentation on monitoring megafauna in the Red Sea. They point to the previously untapped resource of safari boats and diving operations that visit reef sites on a daily basis and whose operatives are likely to be interested in, and cooperative with, organised surveys. “Engaging with this sector and creating long lasting partnerships for data collection through simple protocols could be a winning approach to obtain important information from remote areas and/or on rare species.” They applied this approach (in ‘Turtle Watch Egypt’) to surveying turtle populations in the northern Red Sea, completing 2448 observation reports at 157 sites and recorded 1038 sightings of turtles belonging to four species: hawksbill, green, loggerhead, and olive ridley. The research provides a valuable

9

model for future surveys of megafauna in other areas where commercial activities, such as dive tourism, bring people out on the sea on a frequent basis. This volume offers a wide range of fascinating studies on Red Sea marine life. Together with the previous volume, it provides a valuable resource for future scientiﬁc investigations. It is also a poignant reminder that humankind is blessed by rich, diverse and intricately connected biotopes. If there is an overarching theme or message in these pages it is to appreciate the proliﬁcacy of nature, to better understand its complexity, and to protect the extraordinary environments and species that form our unique planet.

References Augustin N, Devey CW, van der Zwan FM, Feldens P, Tominaga M, Bantan RA, Kwasnitschka T (2014) The rifting to spreading transition in the Red Sea. Earth Planet Sci Lett 395:217–230. https:// doi.org/10.1016/j.epsl.2014.03.047 Bariche M (2010) First record of the angelﬁsh Pomacanthus maculosus (Teleostei: Pomacanthidae) in the Mediterranean. Aqua 16(1):31– 33 Biton E, Gildor H, Peltier WR (2008) Red Sea during the last glacial maximum: implications for sea level reconstruction. Paleooceanography 23, PA1214. https://doi.org/10.1029/2007pa001431 Head SM (1987) Red Sea ﬁsheries. In: Edwards AJ, Head SM (eds) Red Sea: key environments. Pergamon Press, Oxford, pp 363–382 Hovland M, Rueslåtten H, Johnsen HK (2015) Red Sea salt formations —a result of hydrothermal processes. In: Rasul NMA, Stewart ICF (eds) The Red Sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer Earth System Sciences, Berlin Heidelberg, pp 187–203. https://doi.org/10.1007/ 978-3-662-45201-1_11 Lambeck K, Purcell A, Flemming NC, Vita-Finzi C, Alsharekh AM, Bailey GN (2011) Sea level and shoreline reconstructions for the Red Sea: isostatic and tectonic considerations and implications for hominin migration out of Africa. Quatern Sci Rev 30:3542–3574 Morcos SA (1970) Physical and chemical oceanography of the Red Sea. Oceanogr Mar Biol Annu Rev 8:73–202 Rasul NMA, Stewart ICF (eds) (2015) The Red Sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer Earth System Sciences, Berlin Heidelberg, 633 pp, ISBN 978-3-662-45200-4, ISBN 978-3-662-45201-1 (eBook). https://doi.org/10.1007/978-3-662-45201-1_1 Rasul NMA, Stewart ICF, Nawab ZA (2015) Introduction to the Red Sea: its origin, structure and environment. In: Rasul NMA, Stewart ICF (eds) The Red Sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer Earth System Sciences, Berlin Heidelberg, pp 1–28. https://doi.org/ 10.1007/978-3-662-45201-1_1 Trommer G, Siccha M, Rohling EJ, Grant K, van der Meer MTJ, Schouten S, Baranowski U, Kucera M (2011) Sensitivity of Red Sea circulation to sea level and insolation forcing during the last interglacial. Clim Past 7:941–955. https://doi.org/10.5194/cp-7-941-2011

2

The Tides of the Red Sea David T. Pugh, Yasser Abualnaja and Ewa Jarosz

Abstract

This paper describes the present tidal regime in the Red Sea. Both the diurnal and the semidiurnal tidal amplitudes are small because of the constricted connection to the Gulf of Aden and the Indian Ocean, at the Bab el Mandeb Strait. Semidiurnal tides have a classic half-wave pattern, with a central amphidrome, zero tidal range, between Jeddah and Port Sudan. We present a high resolution numerical model output of several tidal constituents, and also model the amphidrome position in terms of ingoing and outgoing tidal Kelvin waves. We quantify the energy budgets for fluxes and dissipation.

Introduction The Red Sea is a semi-enclosed, narrow basin that extends between latitudes 12.5oN and 30oN, with an average width of 220 km, a mean depth of 524 m (Morcos 1970; Patzert 1974), and maximum recorded depths of about 3000 m. Toward the north, it ends in two narrow gulfs, the Gulf of Suez with an average depth of 40 m and the Gulf of Aqaba with depths over 1800 m (Fig. 2.1a, b). The only signiﬁcant opening to the Indian Ocean is at its southern end through the shallow and narrow Bab el Mandeb Strait (a sill depth of 160 m and a minimum width of about 25 km) where it communicates with the Gulf of Aden. D. T. Pugh (&) National Oceanography Centre, Joseph Proudman Building, 6 Brownlow Street, Liverpool, L3 5DA, UK e-mail: [email protected] Y. Abualnaja Red Sea Science and Engineering Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia E. Jarosz Naval Research Laboratory, Oceanography Division Stennis Space Center, Stennis Space Center, MS 39529, USA

Seas that are connected with the open ocean through narrow straits are generally characterized by small tidal ranges (Defant 1961). Because of the restricting Bab el Mandeb Strait, the Red Sea tides are relatively small compared with those of the open ocean, and with those generally experienced along coasts near continental shelves. The semidiurnal oscillations predominate with maximum ranges on spring tides of about one metre in the far north at Suez, and in the southern entrance near Perim Island. The length and depth of the Red Sea give near-resonant half-wavelength dynamics for the semidiurnal tide, which on a rotating Earth results in a wave progression around an amphidrome (a point with zero tidal amplitude) roughly located between Jeddah and Port Sudan, as shown in Fig. 2.2. The diurnal tides are only a few centimetres in range throughout the Red Sea, being most evident in the records from around Port Sudan, in comparison with the locally very small semidiurnal tidal ranges. In the north, where the Red Sea divides into the Gulf of Aqaba and the Gulf of Suez, the two marginal gulfs have very different tidal regimes. The Gulf of Suez is shallow and interspersed with small islands. It has a mean depth of 36 m, and a natural period of 6.7 h; there is a semidiurnal amphidrome in the Gulf of Suez, and the strong currents imply an area of high local tidal energy dissipation. The Gulf of Aqaba has a mean depth of 650 m and a natural oscillation period of about 0.9 h (Defant 1961). The Gulf of Aqaba tides oscillate in phase with the adjacent Red Sea with a 35 min lag from the entrance at the Strait of Tiran, to the head of the Gulf, typical of a standing wave (Monismith and Genin 2004). Tidal currents in the Gulf of Aqaba appear to be associated with internal wave generation; as tidal currents flow through the Strait of Tiran, they drive internal tidal waves on the internal density interface. Their strength varies considerably throughout the year, influenced by varying density stratiﬁcation. Despite the small tidal range, the semidiurnal tide of the Red Sea has been important in the development of general scientiﬁc ideas about the tides, as discussed by Defant

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_2

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12 Fig. 2.1 a Map of the Red Sea, Bab el Mandeb Strait, Gulf of Aden and northwestern Indian Ocean, Dahlak and Farasan Banks, and the open ocean boundary of the model (dotted line); depth contours are in metres; b Locations of the sea level stations from heritage data subsurface pressure gauges (G89, G108, G109) all black circles. Those marked in red are sites of new observations for this study

D. T. Pugh et al.

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The Tides of the Red Sea

13

Fig. 2.2 Outline map of the semidiurnal lunar tidal range (M2) in the Red Sea and locations of the recent measurements. The coordinate X–Y system is used for ﬁtting Kelvin waves in Sect. 6 (DHI 1963)

(1961). Harris (1898) was the ﬁrst to explain dynamically the tides in the Red Sea in terms of the superposition of a standing wave produced by the tide generating forces and a progressive wave entering through the Bab el Mandeb Strait. Because of its long narrow shape and deep sides, the Red Sea was used as an early application of numerical computations of tides, before modern computer power made tidal modelling routine (Grace 1930). Proudman (1953) by modeling the Red Sea as 39 transverse sections along the axis, derived the behaviour of Red Sea tides as seiches in a one-dimensional basin; he also studied the influence of direct gravitational forcing within the Sea, in both cases without Earth rotation. The relative importance of tidal forcing through the Bab el Mandeb Strait, compared with direct gravitational forcing within the Red Sea itself, remained unclear. Defant (1961) called these external and direct forcing the co-oscillating and independent tides respectively; he suggested they are equally important, but also recommended consideration of the frictional energy losses, for a fuller description of the tidal dynamics.

Further recent evidence to help understand the Red Sea tidal budgets and energy dissipation, comes from detailed surveys of levels and currents at the southern end of the Red Sea (Jarosz et al. 2005a, b; Jarosz and Blain 2010). These surveys show a complicated system of tides with an amphidrome for M2 between the Perim narrows and the Hanish Sill. Tides to the south, in the Perim Narrows are similar to those in the Gulf of Aden. Amplitudes become very small near Assab and then increase northward to the co-oscillating amplitudes shown in Fig. 2.2. The numerical model simulation developed for Jarosz and Blain (2010), which included the full Red Sea, is the one used here, but whereas in that paper the emphasis was on the details of the southern Perim Narrows tides, here we look at the results from the model for the more extensive Red Sea, and compare them with a series of new high quality Red Sea tidal analyses which were not available at that time. The very high resolution model of the Red Sea tides, with both external and direct gravitational forcing, is described in detail. The results are then used to investigate the detailed

14

location and movement of the central semidiurnal amphidrome; we interpret these movements in terms of a model of a standing wave consisting of two Kelvin waves, one travelling northward along the Saudi Arabian coast, and a reflected wave travelling south along the Egyptian and Sudanese coast. We also address the traditional tidal question for the Red Sea: The relative importance of direct gravitational tidal forcing, and the external forcing by tides at the Bab el Mandeb Strait (Defant 1961). A general overview of sea level variability in the Red Sea, including weather, climate and tectonic effects, was published in an earlier volume in this series (Pugh and Abualnaja 2015).

Data Collection Before discussing the details of the recent data collection programme, it is appropriate to outline the prior state of knowledge, and of sea level data availability. In short, apart from information published by Vercelli (1925, 1927, 1931) and by Defant (1961), and the secondary port data published in nautical tide tables, until recently there has been very little robust sea level data available for analysis. In many cases, much of the published values in these tide table volumes are based on only a few days of observational data. The longest periods of data were from Port Sudan. Scientiﬁc sea level research with these data includes (Sultan et al. 1995; Sultan and Elghribi 2003), Elfatih (2010), and Mohamad (2012) (see Pugh and Abualnaja (2015) for a full listing). Satellite altimetry data has provided an alternative perspective.

Coastal in Situ Data These earlier coastal data were systematically collected and tabulated as a preparation for the numerical model of Red Sea tides which we detail later (Jarosz and Blain 2010). This numerical model was developed at the United States Naval Research Laboratory, as part of a joint KAUST-Woods Hole Oceanographic Institution physical oceanography research programme. The results have not previously been published in open scientiﬁc literature. In Table 2.1, the tidal harmonic constituents actually in the Red Sea, collected for the Red Sea modelling project entitled “Observation and Modeling—an Integrated Study of the Transport through the Strait of Bab el Mandab” (the BAM project) (see also Murray and Johns 1997) are listed. These consist of data at 22 water level stations, including three subsurface pressure gauges. The three subsurface pressure gauges were deployed for the BAM study. The model also uses data from other sites outside the Red Sea. Data and geographical locations of the water level stations were obtained from the listings of the International

D. T. Pugh et al.

Hydrographic Organization (1979). It must be noted that all the observed tidal amplitudes and phases come from near-coastal areas, so there is no check directly of the tidal elevations in open waters, and that many values are based on only short periods of data. In addition, as explained above, at some water level stations only a few tidal constituents were available for the comparison; the common constituents for all stations were O1, K1, M2, and S2. These are the principal lunar diurnal term O1, the luni-solar diurnal term K1, the principal semidiurnal lunar tide M2 and the principal semidiurnal solar tide S2. The locations are plotted in Fig. 2.1b. The model was also compared with tidal information for seven sites outside the Red Sea, in the Gulf of Aden, but inside the model boundary shown in Fig. 2.1. The full set of tidal data used for model comparison, together with fuller details of the process and maps of four additional modelled smaller tidal terms (Q1, P1, N2 and K2) is available in the original technical report (Jarosz and Blain 2010). For the subsurface pressure measurements, G89, G108 and G109, additional caution is necessary when considering the S2 tidal constituent term. This is because subsurface pressures include changes in atmospheric pressures; it is appropriate to give some background information here. In addition to gravitational forcing, there is another type of tidal forcing related to the solar heating variations, generally called radiational forcing. Detailed harmonic tidal analyses of atmospheric pressures show a daily constituent of 24 h period S1. In addition, there is an S2 constituent. Generally, the S1 constituent, representing diurnal air pressure changes, is a global tropical phenomenon, sometimes enhanced by the local diurnal land/sea winds; the radiational S2 constituent is driven by the twelve-hour oscillation of air pressure in the tropics. These air pressure tidal variations are included in subsurface pressure measurements, and must be corrected for. They are also, of course, potentially drivers of the measured marine tides. Figure 2.3 shows the variations of air pressure over 5 days at KAUST, with both diurnal and semidiurnal components. By the usual inverted barometer arguments, the atmospheric S2 low atmospheric pressures which occur globally at approximately 04:00 and 16:00 local time, are equivalent to a maximum sea level increase of 12.5 mm at the equator. In the Red Sea, the S2 atmospheric tide has an amplitude in the range 0.9–1.1 mbar (9–11 mm), decreasing with increasing latitude. The phase increases from east to west from 210 to 240 degrees relative to Greenwich, giving maximum pressures between 10:00 and 11:00 local time, and another pressure maximum between 22:00 and 23:00 local time (Ray and Ponte 2003). However, the problem in making this correction in a speciﬁc region is that we cannot know the extent of the local

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The Tides of the Red Sea

15

Table 2.1 Summary of earlier Red Sea tidal information, used for calibrating the numerical model. Amplitudes (H) in centimetres, phases (G) in UT. The ﬁnal two columns show the amplitude ratio for the two principal semidiurnal tides, 0.46 in the Equilibrium Tide forcing; and the phase differences which are also the age of the tide, the number of hours after new and full moon that the maximum (spring) tides occur. Consistency of these parameters within sets of analyses is an indication of robust processes Location

Latitude (N)

Longitude (E)

O1

K1

M2

S2

H

G

H

G

H

G

H

G

H (S2/M2)

G (S2-M2)

0.61

21

1

Perim

12.63

43.40

18.0

351

35.0

350

37.0

136

17.0

159

2

G89

12.73

43.13

15.0

345

30.0

340

23.0

121

14.0

142

3

G109

12.73

43.47

15.0

345

30.0

340

29.0

125

16.0

144

0.55

19

4

Assab

13.00

42.73

8.5

344

18.0

335

6.9

259

4.0

170

0.58

−89

5

Mocha

13.32

43.23

6.1

352

7.0

335

8.0

244

4.5

188

0.56

−56

6

G108

13.68

42.18

2.0

335

6.0

321

24.0

286

5.0

299

0.21

13

7

Hudaida

14.83

40.83

1.0

92

1.0

340

30.0

305

6.0

351

0.20

46

8

Ras Khathib

14.92

42.90

1.0

82

4.0

69

26.0

294

7.0

332

0.27

38

9

Kamaran

15.33

42.60

1.0

140

2.0

34

33.0

300

9.0

334

0.27

34

10

Massawa

15.62

39.47

2.0

184

2.3

16

33.4

328

12.4

332

0.37

4

11

Harmil Island

16.48

40.18

1.0

180

2.0

166

13.0

318

3.0

334

0.23

16

12

Port Sudan

19.60

37.23

2.0

170

2.0

168

1.0

204

1.0

256

1.00

52

13

Muhammad

20.90

37.17

2.0

175

3.0

166

6.0

132

1.0

185

0.17

53

14

Jeddah

21.52

39.13

1.0

161

2.8

156

6.0

109

1.0

132

0.17

23

15

Rabegh

22.73

38.97

4.0

162

4.0

156

11.0

124

2.0

165

0.18

41

16

Quseir

26.10

34.27

2.0

192

2.0

158

22.0

112

5.0

139

0.23

27

17

Shaker Island

27.45

24.03

1.0

178

2.0

167

25.0

117

4.0

144

0.16

27

18

Ashraﬁ Islands

27.78

33.72

1.0

153

2.0

167

25.0

118

4.0

145

0.16

27

19

Tor

28.23

33.62

2.0

159

4.0

164

8.0

205

1.0

230

0.13

25

20

Ras Ghan’d

28.35

33.12

2.0

157

2.0

160

18.0

274

7.0

302

0.39

28

21

Zafarana

29.12

32.67

1.0

199

3.0

165

42.0

280

12.7

301

0.30

21

22

Aqaba

29.52

35.00

1.0

146

2.0

158

28.0

128

8.0

155

0.29

27

23

Suez

29.93

32.55

1.3

170

4.5

158

56.0

278

14.0

306

0.25

28

0.33

19.3

4.0

Fig. 2.3 Air pressures from the KAUST offshore buoy showing regular daily cycles

7.4

22.2

6.9

16

D. T. Pugh et al.

inverse barometer effect on sea levels. If the sea levels make a full and immediate inverted barometer response, then the subsurface pressures will be a measure of the gravitational tide. But if there is only partial compensation for the air pressure forcing the measured subsurface pressures will be both gravitational and partly radiational. For these reasons caution is necessary in analyses and hydrodynamic interpretation of the S2 tide and to a lesser extent the K1 tide, especially where the gravitational tides are small, for example near amphidromes. To improve the availability of tidal constituents in the Red Sea, we have beneﬁted from the recent long-period measurements, as given in Table 2.2. These fall into four groups: • Subsea pressure measurements at four sites in Sudan, concentrated around the semidiurnal amphidrome; these were made with assistance from Elfatih Bakry Ahmed Eltaib, researcher in physical oceanography at the Institute of Marine Research, Red Sea University, Port Sudan;

• Three subsurface pressure measurements in Saudi Arabia, also near the amphidrome, as part of the KAUST Red Sea observing programme; • Sea level data from seven sites, established since 2012 as part of the Saudi General Commission for Survey new sea level network. The seven General Commission for Survey permanent gauges along the whole length of the Saudi Arabia coast are high quality Aquatrak acoustic measurements of water levels; • Current and air pressure measurements at the KAUST buoy mooring (Fig. 2.1b); the current components convention is: X positive along the Red Sea to the north, and Y positive across the Red Sea to the east. The values of tidal amplitudes and phases for the major terms are summarised in Table 2.3. The ﬁnal two columns in Table 2.3 show the ratio of the S2/M2 amplitudes, and the S2 minus M2 phase differences in the tidal constituents. These values are a useful check on the consistency of the analyses among themselves, in the region. The one exception to the

Table 2.2 Locations of new sea level measurements and sources. Red Sea University IMR is located in Port Sudan; GCS is the Saudi General Commission for Survey. Gauge manufacturers are accessible on the Web Location

Latitude (N)

Longitude (E)

Gauge

Parameter

Measuring authority

Months

Period

Swakin

19.12

37.34

RBR 420-TG

SSP

Red Sea University IMR

7.5

25 Feb 2013 to 7 Sept 2013

Port Sudan

19.63

37.22

RBR 420-TG

SSP

Red Sea University IMR

7.5

25 Feb 2013 to 7 Sept 2013

Sanganeeb

19.73

37.43

RBR 420-TG

SSP

Red Sea University IMR

6

14 May 2015 to 18 Oct 2015

Arkalai

20.23

37.20

RBR 420-TG

SSP

Red Sea University IMR

7.5

25 Feb 2013 to 7 Sept 2013

Al Lith

20.15

40.26

SBE Seagauge

SSP

KAUST

12

26 June 2013 to 15 June 2014

KAUST

22.31

39.11

RBR 420-TG

SSP

KAUST

6

6 Mar 2013 to 7 Sept 2013

Ar Rayis

23.52

38.61

SBE Seagauge

SSP

KAUST

12

5 June 2014 to 28 May 2015

Gizan

16.93

42.58

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

Al Qunfuda

19.12

41.07

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

Jeddah

21.54

39.15

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

Yanbau

24.11

38.07

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

Al Wajh

26.24

36.52

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

Duba

27.33

35.73

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

Magana

28.46

34.77

Aquatrak 5000

Level

GCS

12

1 April 2014 to 31 March 2015

2

The Tides of the Red Sea

17

Table 2.3 Principal tidal constituents from the new measurements listed in Table 2.2. See Table 2.1 for details of the ﬁnal two columns. Note the increased consistency among the analyses for this new data. Data from the KAUST buoy are for air pressures and current measurements (see text) Location

Latitude (N)

Longitude (E)

Swakin

19.12

37.34

O1

K1

M2

S2

H

G

H

G

H

G

H

G

2.1

159

3.4

168

1.0

176

1.3

245

H(S2/M2)

G(S2-M2)

1.30

69

Port Sudan

19.63

37.22

2.0

159

3.2

166

1.7

142

1.3

230

0.76

88

Sanganeeb

19.73

37.43

1.6

144

2.5

163

1.7

140

1.3

230

0.76

91

Arkalai

20.23

37.20

1.8

160

3.1

170

2.7

131

1.3

214

0.48

83

Al Lith

20.15

40.26

1.8

159

2.8

159

2.5

329

0.9

277

0.36

−52

KAUST

22.31

39.11

1.6

166

2.8

222

11.0

115

3.2

158

0.29

43

Ar Rayis

23.52

38.61

1.5

169

2.8

164

14.6

115

4.5

153

0.31

38

Gizan

16.93

42.58

1.7

136

2.1

132

32.0

295

10.4

326

0.33

31

Al Qunfuda

19.12

41.07

1.7

131

2.6

148

8.3

294

3.2

326

0.39

32

Jeddah

21.54

39.15

1.7

154

3.4

155

7.1

97

1.6

122

0.23

25

Yanbau

24.11

38.07

1.4

158

2.8

156

16.4

101

4.5

124

0.27

23

Al Wajh

26.24

36.52

1.1

159

3.4

146

23.3

103

6.9

124

0.30

21

Duba

27.33

35.73

1.1

161

2.6

157

24.9

103

7.1

125

0.29

22

1.0

169

2.4

152

27.5

110

8.0

135

0.29

25

Magana

28.46

34.77

KAUST Buoy

22.30

38.09 Air pressure (mb)

0.05

91

0.47

61

0.07

21

1.05

194

X currents (cm/s)

0.49

213

0.62

340

0.79

31

0.32

96

Y currents (cm/s)

0.67

135

0.88

217

1.87

59

0.92

52

deg/hour

speed

13.94

general internally consistent pattern, is the phase difference et al. Lith, which is minus 520. Elsewhere the differences are always positive and locally consistent. This difference is a measure of the age of the tide, the time between new or full moon and maximum semidiurnal spring tidal ranges (see Pugh and Woodworth 2014, p. 76). For all the sea level measurements made by the Saudi General Commission for Survey, the age of the tide is from 21 to 32 h; for the subsurface pressure measurements around Port Sudan the age is consistently around 70–90 h. This is probably due to the effects of the separate M2 and S2 amphidromes differing slightly as the M2 tidal wavelength is slightly longer (lower frequency). Similarly, the negative age et al. Lith can occur near an amphidrome. Also, the ages of the tides as measured on the pressure instruments may be affected by the air pressure and because of inexact adjustments for the S2 inverted barometer response discussed above. For tides near the central semidiurnal amphidrome where the tidal signal is small and comparable with meteorological “noise”, it is reasonable to ask whether repeated analyses can produce stable tidal constituents. Table 2.4 shows the results for four long-term KAUST measurements et al. Lith. The periods analysed are either a year, or in the ﬁrst case six-months. For example, M2 has amplitudes which range

15.04

28.98

30

between 2.4 and 2.5 cm, with phases between 3270 and 3310, a span equivalent to only eight minutes. This agreement from year to year is remarkably good even down to the one-millimetre level, and even applies to some very small gravitational terms such as the thrice-daily M3 term. This clearly shows that the actual observed tides are very stable at a ﬁxed location even very close to the amphidrome.

Altimetry Data The various long-term satellite altimetry missions have allowed tidal mapping from space using altimeter measurements of sea levels, generally with an accuracy of about 0.02 m. The sampling intervals, both in time and space call for very different analysis techniques from the traditional processing of regular measurements at ﬁxed coastal sites. Figure 2.4 shows the co-tidal chart for the M2 tidal constituent for the Red Sea based on Topex/Poseidon measurements and inverse dynamic modelling techniques developed by Egbert and Erofeeva (2002). By solving in frequency space, otherwise considerable computational effort is much reduced. The web site for the Oregon State University offers tools for generating tidal maps for several

18

D. T. Pugh et al.

Table 2.4 Al Lith tidal constituents, showing the remarkable stability of the principal tidal constituents, from four different long periods of sub-surface pressure measurements, even at the millimetre level Constituent

Speed

Amplitude (cm)

Phases (degrees)

Deg/h

2011

2012

2013–14

2014–15

Mean

Range

2011

2012

2013– 14

2014– 15

Mean

Range

O1

13.943

1.723

1.791

1.723

1.791

1.757

0.1

160

161

158

157

159

4

K1

15.0411

2.274

2.756

2.756

2.825

2.653

0.7

155

159

160

160

159

5

N2

28.4397

0.965

0.896

0.896

0.896

0.913

0.1

332

329

326

328

329

6

M2

28.9841

2.412

2.412

2.549

2.480

2.463

0.2

331

327

329

329

329

4

S2

30

0.896

0.896

0.965

0.896

0.913

0.1

278

277

276

277

277

3

K2

30.0821

0.276

0.345

0.276

0.276

0.293

0.1

317

326

320

320

321

9

M3

43.4761

0.345

0.276

0.276

0.207

0.276

0.1

283

282

301

312

295

29

Standard Dev (m) before analysis

0.15

0.18

0.20

0.20

Data Blocks

2011 May to November 2012

Standard Dev (m) after analysis

0.08

0.09

0.10

0.11

2012 is November 2011 to December 2012

Tidal variance %

33

25

24

27

2014 is June 2014 to May 2015

Non-tidal variance %

67

75

76

73

regions including the Red Sea, where the resolution is 1/600. The Oregon State University package, called OTIS (OregonSU Tidal Inversion Software) captures ninety percent of the Red Sea sea-level variability in this map of the M2 constituent (http://volkov.oce.orst.edu/tides/region.html). Agreement with the coastal observations is good, with all the general features reproduced. Local coastal differences from the general patterns, for example et al. Wajh, are not always captured.

resolved them into north and east components. Data were from 7 December 2014 to 28 February 2015. There was considerable vertical current shear and variability, but the averaged values as summarised in Table 2.5 were consistent. Note that the tidal currents are only about 10% of the observed current variance, or kinetic energy at this site.

Theoretical Background Standing Waves

Currents The two key factors in understanding the Red Sea tides are: The only available systematic measurements of currents are from the KAUST buoy system. The KAUST buoy is a long-term installation measuring currents with an acoustic current meter at several depths, air pressures, but not bottom pressures. The location is 22.300N, 38.090E, some 50 km off the Saudi coast, which at this latitude trends mainly south to north, rather than the overall Red Sea alignment of 23.5 degrees west of north. The water depth at the site is around 700 m. The currents at the KAUST buoy were measured by an acoustic Doppler current meter, in 4 m depth levels. We averaged currents in the bands from 15 to 91 m depths, and

• Due to the length and depth of the Red Sea, a natural period of seiche is very close to that for half a semidiurnal tidal wavelength, and a quarter of a diurnal wavelength. • The tidal amplitudes are small because of attenuation of external Indian Ocean forcing by the narrow Bab el Mandeb Strait in the south. The resonant effect is explained as follows. For gravity oscillations of water in an enclosed basin the natural period is given by Merian’s Formula:

2

The Tides of the Red Sea

19

For the Red Sea length of about 1600 km and a representative depth of 500 m the natural period is 12.6 h, close to semidiurnal resonance.

A Two-Wave Model We can model the central Red Sea semidiurnal tide as two oppositely travelling Kelvin waves, because of the standing wave system. A brief theoretical description follows. The forces that describe the motion of ocean currents in a rotating-Earth system cause a deflection of the currents toward the right of the direction of motion in the northern hemisphere and conversely in the southern hemisphere. The wave motion on this rotating system can be written as a Kelvin wave (Taylor 1920, 1922; Pugh and Woodworth 2014): fy x Hðx; y; tÞ ¼ H0 exp cos xt ð2Þ c c

Fig. 2.4 Co-tidal M2 chart of the Red Sea based on altimetry data (Egbert and Erofeeva 2002). The lines running northwest and southeast along the Red Sea axis are 5 h and 11 h phase lag on UT, respectively

2 sea length 2L Natural period ¼ pﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃ ¼ pﬃﬃﬃﬃﬃﬃ gD g water depth

ð1Þ

using a coordinate system as shown in Fig. 2.2. H is the pﬃﬃﬃﬃﬃﬃ water level, c is the wave speed gD, and f is the Coriolis parameter. x is the wave angular speed, t is the time variable and H0 is the amplitude at y = 0. Kelvin waves have the characteristic that rotation influences the way in which the wave amplitude decreases across the channel away from the value H0 at the y = 0 boundary as shown in Fig. 2.5a (in the northern hemisphere). The wave heights and currents have amplitudes: fy HðyÞ ¼ H0 exp c ð3Þ g 12 UðyÞ ¼ HðyÞ D

Table 2.5 Comparison of observed and modelled currents at the KAUST buoy. Here X and Y directions are geographic east and north, not as in Fig. 2.2 and later amphidrome analyses Observations O1

K1

M2

S2

Tidal

Residual

Major axis

H

G

H

G

H

G

H

G

Variance

Current

X (east)

0.49

213

0.66

340

0.79

31

0.32

96

20%

−12

cm/sec

Y (north)

0.67

135

0.88

217

1.88

59

0.92

52

8%

−8

cm/sec

X (east)

0.005

299

0.01

290

0.06

239

0.03

265

Y (north)

0.15

67

0.33

66

1.34

36

0.57

64

Alignment

For M2

17 degrees

East of north

3 degrees

East of north

Model

20

D. T. Pugh et al.

Fig. 2.5 K wave dynamics (after Pugh and Woodworth 2014): a A three-dimensional illustration of the elevations and currents for a Kelvin wave running parallel to a coast on its right-hand side (northern hemisphere). The normal dynamics of wave propagation are altered by the effects of the Earth’s rotation which act at right angles to the

direction of wave travel; b A two-dimensional section across the Kelvin wave at high tide, showing how the tidal amplitude falls away exponentially from the coast; at one Rossby radius the amplitude falls to 0.37 of the coastal amplitude. The wave is travelling into the paper

The exponential amplitude decay law has a scale length of c/f, which is called the barotropic Rossby radius of deformation. At a distance y = c/f from y = 0 the amplitude has fallen to 0.37 H0. The wave speed is the same as for a non-rotating case, and the currents are always parallel to the direction of wave propagation. Figure 2.5b shows the proﬁle across a Kelvin wave. Note that Kelvin waves can only move along a coast in one direction; this is with the coast on the right in the northern hemisphere. Figure 2.6 shows the co-tidal (equal phase) and co-amplitude (equal amplitudes and ranges) lines for a Kelvin wave reflected without energy loss at the head of a rectangular channel (Taylor 1922). The sense of rotation of the wave around the amphidrome is anticlockwise in the northern hemisphere and clockwise in the southern hemisphere. The co-tidal lines all radiate outward from the amphidrome and the co-amplitude lines form a set of nearly concentric circles with the centre at the amphidrome at which the amplitude is zero. The amplitude is greatest around the boundary of the basin. Figure 2.7 shows this displacement increasing as the reflected Kelvin wave is made weaker (Pugh 1981). For a reflected Kelvin wave, the ﬁrst amphidrome, where the incident and reflected waves cancel, is located at a position:

approximately a standing wave in an almost enclosed narrow basin on the rotating Earth. A standing tidal wave is represented by two Kelvin waves, travelling in opposite directions. The tidal progression rotates about the nodal point, which is a central tidal amphidrome. The incoming wave travels northward with a maximum amplitude along the coast of Saudi Arabia. At the northern end, the shallow water of the Gulf of Suez is a locally important area of energy loss due to the strong tidal currents, and bottom friction. Because of the energy loss, the tidal wave is not perfectly reflected. The reflected southward, slightly weaker, wave has a maximum amplitude along the coast of Egypt, Sudan and Eritrea. Because the reflected Kelvin wave is weaker than the incident Kelvin wave, the amphidrome is displaced from the centre of the channel to the left of the direction of the incident wave; hence the central semidiurnal amphidrome is displaced toward the Sudan coast. In a narrow channel, an amphidromic point may move outside the left-hand boundary, and in this case, although the full amphidromic system shown in Fig. 2.6 is not present, the co-tidal lines will still focus on an inland point. This is called a virtual or degenerate amphidrome. The tides of the Gulf of Suez have this degenerate amphidrome characteristic. The expressions in Eq. 4a for the amphidrome location in x and y have the advantage in separating the effects of the two physically variable quantities, the angular speed x, and the amplitude attenuation coefﬁcient of the reflected wave, a. The effects of each on the amphidromic position and movement are orthogonal to each other and so may be considered independently in the section below on locating the amphidrome.

pc 2x

ð4aÞ

c ln a 2f

ð4bÞ

x¼ y¼

Here a is the amplitude ratio of the reflected wave to the incident wave. In the Red Sea, the semidiurnal tides are

2

The Tides of the Red Sea

21

Fig. 2.6 Amphidrome dynamics: A three-dimensional drawing exaggerated to illustrate how a tidal wave progresses around an amphidrome in a basin in the Northern Hemisphere. The red numbers are hours in the semidiurnal cycle (after Pugh and Woodworth 2014)

Consider ﬁrst the effect of changing angular speed x on the x position. Although for a single tidal constituent the frequency and period are ﬁxed, on a daily basis the frequency of the semidiurnal tides is slightly modulated, notably through a spring-neap 14 day cycle. This is because the speeds of M2 and S2, being 28.980/h and 300/h respectively, when combined have frequencies that vary in the range:

Fig. 2.7 Amphidrome dynamics: The effects of the Earth’s rotation on a standing wave in a basin which is slightly longer than a quarter-wave length. With no rotation, there is a line of zero tidal amplitude. Because of the Earth’s rotation, the tidal wave rotates around a point of zero

HM2 xM2 þ HS2 xS2 H M2 þ H S2

and

HM2 xM2 þ HS2 xS2 HM2 þ HS2

ð5Þ

As we show in the section on locating the amphidrome, this range is from 29.290/h to 28.180/h for the Red Sea M2 and S2 amplitudes (Lamb 1932).

amplitude, called an amphidromic point. In the third case, because the reflected wave has lost energy through tidal friction, the amphidrome is displaced from the centre line. (after Pugh and Woodworth (2014)

22

Numerical Modelling Modelling Details Yang et al. (2013) developed a two-dimensional ﬁnite element model of tides in the Red Sea and the Gulf of Aden. Their model boundary is in the Indian Ocean at 560E; at this boundary, the model is driven by predicted tides based on ﬁve constituents, O1, P1, K1, M2 and S2. There are 21836 triangular area sectors. The outputs from their model include co-tidal charts for the Gulf of Aden, and some small plots of O1, K1, M2 and S2 tides in the Red Sea, but there is little detail available. Abohadima and Rakha (2013) developed a depth-integrated ﬁnite element model for the Red Sea to predict the tidal currents and tidal water level variations. The open boundary for their model is located at the Bab el Mandeb Strait, and the driver is the predicted levels at the Strait. The model had an element size varying from 15 km to less than 1 km. The output is only in terms of time variations of tidal levels and no attempt is made to look at individual tidal constituents in the elevations. The maximum tidal currents at springs are mapped, and show speeds of up to 20 cm/s. There is no direct gravitational forcing. Madah et al. (2015) present a numerical model study of the Red Sea tides, with external forcing in the Gulf of Aden, 63434 grid cells, and 5 km grid spacing. They also reproduce the general tidal features, but check these against only limited observational data. The numerical model results presented in this chapter are from Jarosz and Blain (2010), where fuller details are available. The model domain, shown in Fig. 2.1a, includes the Red Sea, Bab el Mandeb Strait, Gulf of Aden and the northwestern part of the Indian Ocean. The model area was chosen primarily to reproduce tidal waves propagating from the Indian Ocean, which is a signiﬁcant forcing of tidal motion in the Red Sea as discussed by Defant (1961); having a more remote external model boundary avoids having a boundary in the locality of the complicated Bab el Mandeb Strait tidal dynamics. Depth information for the model was obtained from two sources: The Naval Oceanographic Ofﬁce Digital Bathymetric Data Base-Variable Resolution (DBDB-V) (NAVOCEANO 1997) and charts published by the Defense Mapping Agency in 2006. The ﬁnite element grid used in these computations is displayed in Fig. 2.8. It consists of 84,717 nodes and 163,854 elements. Nodal spacing for this mesh varies throughout the modelled region and ranges between 0.2 and 56 km with the highest reﬁnement present in the Bab el Mandeb Strait and the Red Sea where the minimum and

D. T. Pugh et al.

maximum nodal spacings are 0.2 and 5.5 km, respectively. The coarsest resolution is located in deep waters of the Gulf of Aden and Indian Ocean. The two-dimensional form of the model is based on vertically integrated equations of motion and continuity, which, in a spherical coordinate system, are deﬁned as follows (Gill 1982): @U U @U V @U UVsinu þ þ fV @t Rcosu @k R @u Rcosu g @ sbk ðf agÞ ¼ Rcosu @k q0 H @V U @V V @V UVsinu þ þ þ fU þ @t Rcosu @k R @u Rcosu g @ sbu ðf agÞ ¼ R @u q0 H @f 1 @ðUHÞ 1 @ðVHcosuÞ þ þ ¼0 @t Rcosu @k Rcosu @u

ð6aÞ

ð6bÞ ð6cÞ

where t represents time, k, u denote degrees of longitude and latitude, R is Earth radius, f is the free surface elevation, U and V are the depth-averaged horizontal east-and north-directed velocities, respectively, H = f + h is the total water column depth, h is the bathymetric depth relative to the geoid, f = 2Xsinu is the Coriolis parameter, X is the angular speed of the Earth, qo is a reference density, g is the acceleration due to gravity, a is the Earth elasticity Love Number factor approximated as 0.69 for all tidal constituents as used by other investigators including Schwiderski (1980) and Hendershott (1981) (the slight frequency dependency (Wahr 1981) is not important here), η is the Newtonian Equilibrium tidal potential, and sbk, sbu are the bottom stresses taken as: pﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃ pﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃ sbk ¼ q0 Cd U U 2 þ V 2 ; sbu ¼ q0 Cd V U 2 þ V 2 ð7Þ where Cd denotes the bottom drag coefﬁcient. The Equilibrium tidal potential is expressed as (Reid 1990): gðk; u; tÞ ¼

X

Cjn f jn ðt0 ÞLj ðuÞ cos 2pðt t0 Þ=Tjn þ jk þ tjn ðt0 Þ

n;j

ð8Þ where t is time relative to to, which is the reference time, Cjn is a constant characterizing the amplitude of tidal constituent n of species j, fjn is the time-dependent nodal factor, tjn is the time-dependent astronomical argument, j = 0, 1, 2 are the tidal species (j = 0 declinational; j = 1 diurnal, j = 2 semidiurnal), Lo = 3sin2u−1, L1 = sin(2u), L2 = cos2u,

2

The Tides of the Red Sea

23

Fig. 2.8 Model ﬁnite element grid (84717 nodes and 163,854 elements) and an example of the model grid resolution within the central amphidrome area

and Tjn is the period of constituent n for species j. See Pugh and Woodworth (2014, Chap. 3) for a development of this expression involving tidal species, and for time dependence. Although direct gravitational tidal forcing is in the model, with elastic-earth corrections, the secondary effects of elastic earth tidal loading, and gravitational self-attraction are not included in the equations. Prior to being discretised, the continuity and momentum equations are combined into a Generalized Wave Continuity Equation (GWCE), which has been shown to have superior numerical properties to a primitive continuity equation when a ﬁnite element method is used in space (Lynch and Gray 1979). The ﬁnal forms of the GWCE and momentum equations, which are solved by the model, are given in Blain

and Rogers (1998), while numerical discretization of these equations is described in detail by Luettich et al. (1992) and Kolar et al. (1994). Additional model constraints at the land boundaries are: • no flow across. • friction-free tangential slip. At the open ocean boundary, the tidal elevation is generated by synthesising four diurnal (K1, O1, P1, Q1) and four semidiurnal (M2, S2, N2, K2) constituents. The tidal harmonic constants used to generate the elevation along the open boundary are linearly interpolated onto the boundary nodes using data from the World Ocean Tide Model

24

database FES99 (Lefevre et al. 2002). In addition, an equilibrium tidal potential forcing within the domain is applied for the same eight constituents. A time step of 15 s was used to ensure model stability based on the Courant number criterion. The parameter so, which weights the primitive and GWCE form of the continuity equation, was estimated from a formula given by Westerink et al. (1994) and set equal to 0.001. Finally, the minimum depth was assigned to be 3 m to eliminate any potential drying of computational nodes since the wetting and drying option was not included in these simulations. The model simulations were carried out for one year to generate a sufﬁciently long time series that allows the separation of the P1 constituent from the K1 constituent; resolution of the S2 constituent from the K2 constituent was also possible. Boundary conditions are already adjusted for nodal effects. The amplitudes and phases of the tidal constituents were obtained through harmonic analysis programmes (Foreman 1977, 1978). Note that the analyses of the actual observations in Tables 2.3 and 2.4 were done using the UK National Oceanography Centre TASK software, but the two processes are entirely compatible for the constituents discussed here. However, for full analyses and comparisons there are signiﬁcant differences, for example in deﬁning the phases of the annual Sa constituent. Several different model setups were utilized to simulate tides as close to those observed in the Red Sea as possible. The best ﬁt to the observations was obtained when the model was driven only by external forcing, that is, the tidal elevations applied along the open boundary located in the Indian Ocean. For this model run, a depth-independent constant value of 0.003 for the bottom drag coefﬁcient was used throughout the domain. When both external and direct gravitational (tidal potential) forcing mechanisms with the bottom friction coefﬁcient of 0.003 were applied, the modelling results, mostly for the semidiurnal tides, differed signiﬁcantly from the observations. For the principal semidiurnal constituents (M2, S2, N2, K2), these simulations produced degenerated amphidromic systems with virtual amphidromes located in Saudi Arabia. Contrary to the observations, these results also indicated that the semidiurnal outgoing (reflected) waves were larger than the ingoing waves. When the model was driven by both external and direct forcing a use of either larger constant bottom drag coefﬁcients (0.005 or larger) or depth-dependent bottom friction coefﬁcients (the Manning type friction law with the break depth of 30 m or less as deﬁned in http://adcirc.org/) did not improve modelling results and model-observation comparisons. The bottom friction terms (7) are a sole sink of energy of the barotropic tides in the version of the ADCIRC model used here. Thus, one of the efforts was focused on increasing the energy loss of the outgoing semidiurnal waves by applying the bottom friction coefﬁcient of 0.01 at the

D. T. Pugh et al.

model nodes between the African coast and the major axis of the Red Sea, while 0.003 was used at the remaining grid nodes. This effort also did not generate more realistic results for the semidiurnal tides. At the same time, simulations from the different model setups produced almost identical results for the diurnal tides in the Red Sea. In summary, the model that produced the results presented here is: • Depth integrated, two dimensional. • Driven by Indian Ocean tidal boundary levels; eight tidal constituents. • Has a much higher resolution than any previous models. • Was run for a year to give high resolution of tidal frequencies. • Has a depth-independent friction drag coefﬁcient of 0.003.

Model Validation There are many ways of comparing the model performance with actual observations. The overall comparison with, for example, the co-tidal chart in Figs. 2.2 and 2.4, is that the essential details are well reproduced. Results also agree generally with the basic mapping of Yang et al. (2013), and Madah et al. (2015). Before proceeding to detailed descriptions based on the model, it is appropriate to make direct comparisons with the observations of tidal constituents in Tables 2.1 and 2.3. For these comparisons, we look at the O1 constituent as representative of the diurnal constituents, and the M2 constituent as representative of the semidiurnal constituents. The K1 and S2 constituents are less suitable for comparisons because of the air pressure effects noted above. The ﬁrst comparison, shown in Table 2.6a, for O1, bearing in mind that the older observations in many cases are of limited quality, is of the ratio between the computed and observed constituent amplitudes (Hc/Ho), and the differences between the observed and computed phases (Gc-Go) in the third and second columns from the right. All the phase differences have been adjusted to fall in the range −1800 to +1800 for easier comparison. The amplitude ratio for O1 is close to the ideal 1.0 for the southern locations, varies in the central region, and is higher than 3.0 in the northern parts of the Red Sea where the model is giving amplitudes bigger than observed. Note however, that the observed maximum amplitudes are very small except in the south, and are typically only one or two centimetres. The O1 phases are generally in good agreement between observations and the model computations, with the model phases 15 degrees ahead of the observations, which is equivalent to one hour

2

The Tides of the Red Sea

25

Table 2.6 (a) Comparison of observed and modelled amplitudes and phases of the O1 constituent for heritage data (Table 2.1); (b) comparison of observed and modelled amplitudes and phases of the M2 constituent for heritage data (Table 2.1) 6a Location

Latitude (N)

Longitude (E)

O1

Observed

O1

Computed

H

G

H

G

Perim

12.63

43.40

18.0

351

19.1

352

1.06

1

1.1

G89

12.73

43.13

15.0

345

15.6

349

1.04

4

1.2

G109

12.73

43.47

15.0

345

16.5

353

1.10

8

2.7

Assab

13.00

42.73

8.5

344

9

344

1.06

0

0.5

Mocha

13.32

43.23

6.1

352

9.9

354

1.62

2

3.8

G108

13.68

42.18

2.0

335

4

331

2.00

−4

2.0

Hudaida

14.83

40.83

1.0

92

2.2

356

2.20

−96

2.5

Ras Khathib

14.92

42.90

1.0

82

2.1

355

2.10

−87

2.3

Kamaran

15.33

42.60

1.0

140

1.5

1

1.50

−139

2.3

Massawa

15.62

39.47

2.0

184

0.4

212

0.20

28

1.7

Harmil Island

16.48

40.18

1.0

180

0.5

180

0.50

0

0.5

Port Sudan

19.60

37.23

2.0

170

1.6

163

0.80

−7

0.5

Muhammad

20.90

37.17

2.0

175

1.7

163

0.85

−12

0.5

Jeddah

21.52

39.13

1.0

161

1.7

156

1.70

−5

0.7

Rabegh

22.73

38.97

4.0

162

1.9

156

0.48

−6

2.1

Quseir

26.10

34.27

2.0

192

2.3

160

1.15

−32

1.2

Shaker Island

27.45

24.03

1.0

178

2.3

160

2.30

−18

1.4

Ashraﬁ Islands

27.78

33.72

1.0

153

2.5

165

2.50

12

1.5

Tor

28.23

33.62

2.0

159

3

164

1.50

5

1.0

Ras Ghan’d

28.35

33.12

2.0

157

3.3

171

1.65

14

1.4

Zafarana

29.12

32.67

1.0

199

3.9

172

3.90

−27

3.0

Aqaba

29.52

35.00

1.0

146

2.4

160

2.40

14

1.5

Suez

29.93

32.55

1.3

170

4.1

172

3.15

2

2.8

Average

1.60

−15

1.7

StDev

0.89

40

0.9

6b Location

Latitude (N)

Longitude (E)

O1

Observed

O1

Computed

H

G

H

G

Perim

12.63

43.40

18.0

351

19.1

352

1.06

1

1.1

G89

12.73

43.13

15.0

345

15.6

349

1.04

4

1.2

G109

12.73

43.47

15.0

345

16.5

353

1.10

8

2.7

Assab

13.00

42.73

8.5

344

9

344

1.06

0

0.5

Mocha

13.32

43.23

6.1

352

9.9

354

1.62

2

3.8

G108

13.68

42.18

2.0

335

4

331

2.00

−4

2.0

Hudaida

14.83

40.83

1.0

92

2.2

356

2.20

−96

2.5

Ras Khathib

14.92

42.90

1.0

82

2.1

355

2.10

−87

2.3

Kamaran

15.33

42.60

1.0

140

1.5

1

1.50

−139

2.3

Massawa

15.62

39.47

2.0

184

0.4

212

0.20

28

1.7

Harmil Island

16.48

40.18

1.0

180

0.5

180

0.50

0

0.5

Port Sudan

19.60

37.23

2.0

170

1.6

163

0.80

−7

0.5

Muhammad

20.90

37.17

2.0

175

1.7

163

0.85

−12 0.5 (continued)

26

D. T. Pugh et al.

Table 2.6 (continued) 6b Location

Latitude (N)

Longitude (E)

Jeddah

21.52

39.13

O1

Observed

O1

Computed

H

G

H

G

161

1.7

156

1.0

1.70

−5

0.7

Rabegh

22.73

38.97

4.0

162

1.9

156

0.48

−6

2.1

Quseir

26.10

34.27

2.0

192

2.3

160

1.15

−32

1.2

Shaker Island

27.45

24.03

1.0

178

2.3

160

2.30

−18

1.4

Ashraﬁ Islands

27.78

33.72

1.0

153

2.5

165

2.50

12

1.5

Tor

28.23

33.62

2.0

159

3

164

1.50

5

1.0

Ras Ghan’d

28.35

33.12

2.0

157

3.3

171

1.65

14

1.4

Zafarana

29.12

32.67

1.0

199

3.9

172

3.90

−27

3.0

Aqaba

29.52

35.00

1.0

146

2.4

160

2.40

14

1.5

Suez

29.93

32.55

1.3

170

4.1

172

for diurnal constituents. The comparisons in Table 2.7a, for O1 with the much better observational data are encouragingly better, with the average modelled amplitudes 40% higher than observed. The phases are now 4.1 degrees behind the observations, equivalent to only 17 min time difference over the whole Red Sea area. Turning to the semidiurnal M2 tide, again the ratio between the computed and observed constituent amplitudes (Hc/Ho), and the differences between the observed and computed phases (Gc-Go) are again in the third and second columns from the right. (Hc/Ho) is 0.93, with modelled results slightly less than the observed. The timings show very good agreement except at Assab and Mocha in the south; overall the modelled timings lag the observations by four minutes (2 degrees for semidiurnal terms) but there is a large scatter with a standard deviation of just over an hour. Here all the phase differences have again been adjusted to fall in the range 00 to +3600 for easier comparison. The semidiurnal tides are much larger than the diurnal tides except for the amphidrome region in the central Red Sea. The comparisons in Table 2.7b, with the much better new observational data are better in some critical respects, but because many of the new long-term observations are deliberately in the vicinity of the central amphidrome, where the phases change very rapidly along the coasts, the phase differences are inevitably much more critically dependent on exact model locations so there is more error due to our localised sampling. Overall the model phases lag the new data by 320, equivalent to one hour. Note however, that on the Saudi Arabian coast the model amplitude shortfall is generally around 60%, and the phases of the M2 tide lag observations by close to an hour in a consistent pattern. On

3.15

2

2.8

1.60

−15

1.7

0.89

40

0.9

the opposite Sudan coast near Port Sudan the lag is about 2.5 h. Small shifts of the modelled amphidrome location can easily account for this. Overall the agreement is very good given the small amplitudes of the tidal waves, and the frictional uncertainties discussed above. Another test of the model viability, which weights comparison toward areas of bigger tidal amplitude, is the amplitude H of the vector difference between observed and predicted tidal amplitude/phase vectors. This is explained in the polar plot of Fig. 2.9. This parameter is computed by Cartesian algebra, for each location and each constituent, from the following expression (Davies et al. 1997): h i12 H ¼ ðAobs cos gobs Acom gcom Þ2 þ ðAobs sin gobs Acom sin gcom Þ2

ð9Þ A and g are amplitudes and phases, respectively, and sufﬁxes “com” and “obs” denote the computed and observed harmonic constants. For O1 Table 2.6a shows an average vector difference of 1.7 ± 0.9 cm with the greatest discrepancies in the far north of the Red Sea. Table 2.7a shows even better agreement with a difference vector of only 0.7 ± 0.4 cm. For the semidiurnal constituents exempliﬁed by M2, the amplitudes of the difference vector average 14.5 ± 9.0 cm for the older data in Table 2.6b. However, the agreement is much improved by comparisons with the new reliable data set, with difference vector amplitudes of 6.8 ± 5.0 cm. In part, this improvement is due to the concentration of the new measurements where the M2 amplitudes are small, but overall the model results prove to be robust when tested against the better, new observations.

2

The Tides of the Red Sea

27

Table 2.7 (a) Comparison of observed and modelled amplitudes and phases of the O1 constituent for new data (Table 2.2); (b) Comparison of observed and modelled amplitudes and phases of the M2 constituent for new data (Table 2.2). Amplitude ratios and phase differences are also tabulated. The vector amplitudes are the differences in vector space as shown in Fig. 2.9 Location

Latitude (N)

Longitude (E)

O1

Observed

O1

Computed

H

G

H

G

Swakin

19.12

37.34

2.1

159

1.5

163

0.73

4

0.6

Port Sudan

19.63

37.22

2.0

159

1.6

163

0.78

4

0.5

Sanganeeb

19.73

37.43

1.6

144

1.6

163

0.96

18

0.5

Arkalai

20.23

37.20

1.8

160

1.6

163

0.89

3

0.2

Al Lith

20.15

40.26

1.8

159

1.5

153

0.81

−6

0.4

KAUST

22.31

39.11

1.6

166

1.9

156

1.16

−10

0.4

Ar Rayis

23.52

38.61

1.5

169

2.0

157

1.31

−12

0.6

Gizan

16.93

42.58

1.7

136

0.5

74

0.28

−62

1.5

Al Qunfuda

19.12

41.07

1.7

131

1.2

149

0.72

17

0.6

Jeddah

21.54

39.15

1.7

154

1.7

156

1.01

2

0.1

Yanbau

24.11

38.07

1.4

158

2.0

157

1.44

−1

0.6

Al Wajh

26.24

36.52

1.1

159

2.2

158

2.04

−1

1.1

Duba

27.33

35.73

1.1

161

2.3

159

2.09

−2

1.2

Magana

28.46

34.77

1.0

169

2.4

157

2.36

−12

1.4

Location

Latitude (N)

Longitude (E)

Swakin

19.12

37.34

82

1.2

speed

13.94

28.98

M2

Observed

M2

Computed

H

G

H

G

1.0

176

0.8

258

0.76

Port Sudan

19.63

37.22

1.7

142

0.5

226

0.31

84

1.7

Sanganeeb

19.73

37.43

1.7

140

0.5

210

0.28

71

1.6

Arkalai

20.23

37.20

2.7

131

0.9

160

0.33

29

2.0

Al Lith

20.15

40.26

2.5

329

3.1

346

1.23

17

1.0

KAUST

22.31

39.11

11.0

115

5.3

116

0.48

1

5.7

Ar Rayis

23.52

38.61

14.6

115

7.2

119

0.49

4

7.5

Gizan

16.93

42.58

32.0

295

22.6

313

0.71

18

12.7

Al Qunfuda

19.12

41.07

8.3

294

11.8

334

1.42

40

7.6

Jeddah

21.54

39.15

7.1

97

3.1

108

0.43

11

4.1

Yanbau

24.11

38.07

16.4

101

8.2

121

0.50

20

9.1

Al Wajh

26.24

36.52

23.3

103

12.6

126

0.54

23

12.7

Duba

27.33

35.73

24.9

103

13.5

127

0.54

24

13.7

Magana

28.46

34.77

27.5

110

14.8

128

The currents at the KAUST buoy agree in general with the model, but there are some signiﬁcant differences. For both observations and currents, the semi-major axes align slightly east of north, consistent with the alignment of the nearest Saudi coastline at this latitude, but several degrees clockwise from the general 23 degree west of north alignment of the Red Sea. Note that the maximum north-going currents in the observations are some 2.5 h ahead of high

0.54

18

14.2

Average

0.61

32

6.8

StDev

0.33

28

5.0

water levels in the northern Red Sea, consistent with standing Kelvin Wave dynamics. Figure 2.10 plots the two ellipses for M2 currents, showing the observed currents are larger than the modelled currents, but the amplitudes are comparable and small. The modelled current ellipse is almost rectilinear. Note the same vertical (Y, north) scales but very different horizontal (X, east) scales, in Fig. 2.10.

28

D. T. Pugh et al.

• However, diurnal amplitudes are everywhere only about 1.5 cm. • Semidiurnal amplitudes are around 40 cm at the Bab el Mandeb Strait, then fall to near zero in the central Red Sea, then increase to 30 cm at Suez. • These semidiurnal amplitudes are on average 15% low in the Red Sea but within this average there are clear regional patterns: – In the south, model semidiurnal amplitudes are about 200% high. – North of the central amphidrome the model results for amplitude are systematically too low, at about 60% of the observed amplitudes. • Observed currents at the KAUST buoy are larger than the modelled currents and the ellipse is broader. Fig. 2.9 Diagram explaining the difference vector (green) in harmonic constituent comparisons of model (red) and observed (blue) tidal constituent amplitudes and phases plotted in a polar phase coordinate system

With these speciﬁc comparisons between observations and the model in mind, we can now look at the regional tidal dynamics, as shown by the model, to discuss the Red Sea tides in detail.

In summary, the model agrees well with the better new observations, which means that the modelling of the complexities in the southern Bab el Mandeb Strait entrance are good, as any error there will propagate through the Red Sea. However, there are systematic differences:

Tidal Elevations and Currents

• The modelled diurnal phases in levels are generally correct to within thirty minutes throughout the Red Sea. • Diurnal amplitudes are modelled high by about 20% in the central Red Sea, and about 80% high in the north.

Fig. 2.10 Observed and modelled M2 current ellipses. Units are cm/s. Note that the vertical (Y) scales are the same, but the X-scale for modelled data is expanded by 10. Y is geographic north positive, and X is geographic east positive. The semi-major axis is 170 east of north, while the modelled semi-major axis is 30 east of north

Here we discuss the Red Sea tides, based on the observations and model results. It is useful to compare the tides inside and outside the Red Sea as separated by the Bab el Mandeb Strait. To deﬁne external tides, we have done new detailed analyses. Table 2.8a shows the results of a year of sea level tidal analyses for Djibouti, Aden, and Salalah in Oman, three locations in the Arabian Sea, the ﬁrst two being approximately 100 and 150 km respectively outside the Bab el Mandeb Strait (see Fig. 2.1a). The analyses, all for the year 2015, are of data extracted from the University of Hawaii Sea Level Center database. There are extensive gaps in the data for Aden and Salalah, but the constituent amplitudes and phases are robust and internally consistent. Using the average values from Table 2.1 as representative of the Red Sea tides the bottom line in Table 2.8a shows that the age of the semidiurnal tide, inside and outside the Red Sea, is the same within an hour (20 ± 1). The Form factor (the ratio of the amplitudes (O1 + K1)/(M2 + S2) which indicates the relative importance of the diurnal to the semidiurnal tides, is 0.83 for Aden and Djibouti, whereas it is 0.39 inside the Red Sea. Outside, the tides are mixed, whereas inside they are dominated by the semidiurnal constituents. This semidiurnal enhancement is due to the effect of semidiurnal resonance in the Red Sea. Although both semidiurnal and diurnal tides are reduced by passage through the southern Bab el Mandeb Strait entrance, the semidiurnal tides are less attenuated due to this compensating internal resonance.

2

The Tides of the Red Sea

29

Table 2.8 (a) Comparison of tides in the Gulf of Aden and the Red Sea. Amplitude ratios are normalised to K1 and M2; (b) Comparison of Equilibrium Tide and modelled tidal ratios 8a Djibouti

Amplitude ratio

Aden

Amplitude ratio

Salalah

Amplitude ratio

H

G

H

G

H

G

Q1

4.2

354

0.11

4.0

357

0.10

4.6

353

0.13

O1

19.3

353

0.49

20.0

351

0.52

17.9

348

0.51

P1

11.9

347

0.30

13.0

1

0.34

10.4

340

0.30

K1

39.3

350

1.00

38.2

357

1.00

35.1

344

1.00

N2

13.1

130

0.27

13.3

130

0.27

8.1

134

0.26

M2

48.2

135

1.00

49.0

136

1.00

30.6

143

1.00

S2

21.6

155

0.45

21.7

155

0.44

11.8

166

0.39

K2

6.2

150

0.13

5.9

150

0.12

3.6

170

0.12

std Obs

49.8

50.7

Red Sea Table 2.1

37.3

Std residuals

5.3

3.3

6.7

Hours analysed

8753

4639.0

5958

Age

20

hours

19

hours

23

hours

19

hours

Type

0.84

mixed

0.82

mixed

1.25

mixed

0.33

semidiurnal

8b Red Sea

Arabian Gulf See above

Model

Equilibrium tide

Diurnal tides Q1

0.11

0.11

0.14

O1

0.51

0.51

0.71

P1

0.32

0.31

0.33

K1

1.00

1.00

1.00

0.27

0.27

0.19

M2

1.00

1.00

1.00

S2

0.44

0.43

0.47

K2

0.10

0.12

0.13

Semidiurnal N2

Table 2.8b compares the amplitudes of the major diurnal and semidiurnal constituents in the Red Sea from the model, and outside the Red Sea from the values in Table 2.8a. The agreement between outside and inside ratios (normalised to K1 and M2 amplitudes) is good at the 0.01 level, showing the validity of the model’s boundary conditions and also of its hydrodynamic processing. The third column in Table 2.8b compares these ratios with those in the direct gravitational global tide, the Equilibrium Tidal forcing. Compared with the Equilibrium Tide, in the Red Sea the Q1 and O1 tides are 40 percent weaker relative to K1; and the semidiurnal N2 is enhanced by some 50% relative to M2,

while the S2 solar semidiurnal term, is just a few percent less. We now give an overall description of the Red Sea tides based on observations and essentially on the patterns deﬁned by the model outputs. Figures 2.11, 2.12, 2.13 and 2.14 display the tidal charts, the computed co-amplitudes (in cm) and co-phases (in hours, relative to UTC (GMT)) of the tidal elevations for the O1, K1, M2 and S2 constituents. For very similar charts for additional tidal constituents Q1, P1, N2 and K2, see Jarosz and Blain (2010). As discussed above (Table 2.8a), due to semidiurnal resonance, except for the Bab el Mandeb Strait and the

30

D. T. Pugh et al.

Fig. 2.11 Model coamplitudes (in cm; red lines) and cophases (hours, GMT; black lines) for the O1 constituent

Fig. 2.12 Model coamplitudes (in cm; red lines) and cophases (hours, GMT; black lines) for the K1 constituent

central semidiurnal nodal region, the tides in the Red Sea are mainly semidiurnal. The tides in the Bab el Mandeb Strait are mixed, mainly semidiurnal (Jarosz et al. 2005a). The tidal regime is diurnal in the amphidromic systems east of Port Sudan and in the southern Gulf of Suez where the semidiurnal tides are weak in the vicinity of amphidromes. The amplitudes of the diurnal tidal components (Figs. 2.11 and 2.12) show very similar behaviour in the Red Sea, with little variability in the cross-sea direction. The largest values are found near and in the Bab el Mandeb Strait. In the Red Sea proper, the diurnal amplitudes are less than 5 cm. The major diurnal constituents have well-developed anticlockwise amphidromic systems in the Red Sea (K1 at approximately 16030′N; O1 at approximately 160N). The O1 wavelength is slightly longer than K1, as the period is longer, so the O1 amphidrome is displaced farther south from the reflecting node at the north end of the Red Sea. The amplitudes and phases of the major semidiurnal constituents also have similar distributions to each other. However, they show more complex behaviour than the diurnal constituents (Figs. 2.13 and 2.14). The semidiurnal

amplitudes show large variability in the along-sea direction. They also show some variations in the cross-sea direction between latitudes 150N and 170N (Dahlak and Farasan Banks). The largest constituent amplitudes are found in the Bab el Mandeb Strait, the Gulf of Suez, and around Dahlak Bank. Moreover, the amplitude and phase distributions indicate that the semidiurnal waves have three amphidrome locations, the main one in the centre between Jeddah and Port Sudan. Only the central amphidrome is fully developed as a counter-clockwise system with an amphidromic point located near 200N. The two other areas of Kelvin wave cancelling are examples of degenerate amphidromes: One is located at the northern end of the Bab el Mandeb Strait and another is in the southern part of the Gulf of Suez. Vercelli (1925) and Defant (1961), based on the limited data, postulated the amphidromic point of the M2 tide in the Bab el Mandeb Strait, located near Assab, southwest of that suggested by the model results. The location of the Suez nodal system is well replicated by the model simulation; it is due to slow wave progression and corresponding short tidal wavelengths, in the relatively shallow waters of the Gulf of Suez.

2

The Tides of the Red Sea

31

Fig. 2.13 Model coamplitudes (in cm; red lines) and cophases (hours, GMT; black lines) for the M2 constituent

Fig. 2.14 Model coamplitudes (in cm; red lines) and cophases (hours, GMT; black lines) for the S2 constituent

The model also gives tidal currents. These are generally very weak. The amplitudes and inclination of the semi-major axis for M2, are shown in Fig. 2.15 (the inclination angles were re-interpolated on a coarser grid for clarity). For all principal tidal components, distributions of the semi-major axis amplitudes show ampliﬁcation of tidal currents as they flow into the Bab el Mandeb Strait from the Gulf of Aden. The strongest diurnal currents are generated by the K1 constituent (semi-major axis current amplitudes of the O1, P1, and Q1 are, on average, 47%, 32%, and 9%, respectively, of those associated with K1) and the M2 constituent (semi-major axis amplitudes of the S2, N2, and K2 are, on average, 44%, 27%, and 10%, respectively, of those associated with M2). These current ratios are consistent with the wave amplitude ratios discussed above. Furthermore, the most energetic flow is present in the narrowest southern part of the Bab el Mandeb Strait with the maximum modelled amplitudes found near Perim where, for instance, the speeds of the K1 and M2 currents may reach over 40 cm/s. Farther north, the diurnal currents are below 5 cm/s, except for the K1 current amplitudes in the southern part of the Gulf of Suez, where they can reach 10 cm/s. The

direction of the maximum flow is generally aligned with the major axis of the Sea; however, there is some variability in inclination angles on the shallows, near the islands and coast. Semi-minor axis amplitudes are everywhere much less that the semi-major axis, so diurnal tidal currents are always nearly rectilinear in the Red Sea. In addition, the phase difference between the tidal elevation and maximum tidal velocity is usually approximately 900 for all diurnal constituents. The semi-major axes of the semidiurnal constituent ellipses, as for the diurnal ones, are the largest in the Bab el Mandeb Strait, just north of it, and in the Gulf of Suez; however, their amplitudes are also enhanced on the Farasan and Dahlak Banks and nearby. The direction of the maximum flow is aligned with the along-sea direction, except for regions such as the Farasan and Dahlak Banks (areas of shallow water less than 50 m in depth) where it can be locally quite variable. As for amplitudes, in general, the semidiurnal tidal currents are much stronger in the central and northern Red Sea than those generated by the diurnal tides. Semidiurnal tidal currents are everywhere, except locally near shallow coastal waters, nearly rectilinear, and

32

D. T. Pugh et al.

the residual tidal flow contributes little to the mean circulation observed in the Red Sea, though it may be more important in the Gulf of Suez shallow region.

Locating the Amphidrome

Fig. 2.15 Currents: the major axis (colourbar, in cm/s) and direction of the major axis of the M2 constituents

typically around 4 cm/s amplitude. The phase distributions for the semidiurnal constituents display more variability in the Red Sea than those of the diurnal tidal currents. Rapid phase changes are found in the southern part of the Sea, near the islands and coast. Additionally, for the N2 phase the model shows more variability in the deep waters, while the S2 phase is quite variable in the Gulf of Suez. Moreover, the tidal elevations and the maximum tidal currents for all semidiurnal constituents are such that maximum currents occur at mid-tidal levels, (phase differences of 2700 or 900) as is typical for the dynamics of basin seiche resonances; see Pugh and Woodworth (2014) for further illustrations. Details of spring-neap modulations in elevations and currents are given in Jarosz and Blain (2010). In general, the tidal residuals are very weak. The highest residual speeds are in the Bab el Mandeb Strait but they do not exceed 0.6 cm/s. The strongest residual flow is generally found in the narrow southern part of the Strait. In the Red Sea, the residual currents are even weaker and do not exceed 0.1 cm/s. Hence,

We now consider the observed locations and movement of the central Red Sea semidiurnal amphidrome. The daily location of the amphidrome can be determined with the help of a numerical model, either continuously, or for an individual tidal constituent. It can also be directly located from the tidal values at the sites surrounding it. This location can be determined for individual tidal constituents, and there is also the possibility of ﬁxing the location on a day-by-day basis (Pugh 1981). We used the hourly values of sea levels and sub-surface pressures at the three Sudan sites, Akurari, Port Sudan and Swakin, and the two Saudi Arabian sites of Al Lith and KAUST. First, we remove the weather effects by preparing a set of tidal predictions using a full set of constituents for each site. A least-squares daily harmonic analysis was then made of 25 hourly values from midnight to midnight to determine the amplitude (H) and phase (G) of the semidiurnal tide, conveniently called D2, and the diurnal tide, for all ﬁve stations. Figure 2.16 shows the semidiurnal D2 amplitudes. The KAUST amplitudes are signiﬁcantly greater than the amplitudes at the other four sites, nearer to the amphidrome. There are strong systematic patterns, with spring-neap and other periods, among the tidal syntheses for each station. The G values (not plotted) are related to midnight on each day and so advance on average by 24o per day. The daily values of H and G at the ﬁve stations form a set from which the amphidrome position on each day can be estimated. This was done by ﬁtting least-squares planes to the surfaces Hsin(G) and Hcos(G), which themselves represent the sea levels at a quarter of a tidal period separation. The subsurface pressure values were corrected for the daily air pressure cycle. For each plane, there is a line where it intersects the zero sea level plane, and along which the amplitudes are zero at that time. The second plane, ﬁtted three hours later will have another line of zero sea levels. An intersection of these two lines is the location where there are no semidiurnal sea level changes at any time, and this is the amphidrome location. The amphidrome location changes daily as indicated by the blue diamonds in Fig. 2.17. This distribution also shows a clear pattern, with locations concentrated along line orthogonal to the Red Sea axis. Fitting two planes can be justiﬁed by the small (millimetre) values

2

The Tides of the Red Sea

33

Fig. 2.16 The D2 semidiurnal tidal constituent amplitude determined on a daily basis. KAUST is signiﬁcantly north of the amphidrome. At Swakin the tide is sometimes near zero. Note that all D2 determinations are independent of eachother, and that the pattern is consistent

of the residuals; we are dealing with very small tidal amplitudes in this area so millimetre differences are probably in the noise level. The position of the M2 amphidrome using all ﬁve locations is 38.1090E, 19.6990N. Using only three locations, Al Lith, Akurari and Swakin, the position is 38.1520E, 19.6920N. The difference is only 5 km. Figure 2.17 also conﬁrms the robustness of the amphidrome positions. M2 amphidrome positions omitting KAUST, Arkali, Port Sudan and Swakin in turn shows differences of only a few kilometres. However, the inclusion of Al Lith, close to the amphidrome on the Saudi Arabian coast, proved necessary

Fig. 2.17 The daily semidiurnal tidal amphidrome positions as a function of latitude and longitude. The M2 amphidrome position determined over the full six –month period (ﬁve stations) is the big red triangle. The black dashed line shows the approximate location of the Sudan and Saudi Arabia coastlines. To test the stability of the solutions, the corresponding positions omitting in turn Arkali (dark blue diamond), Kaust (black square), Swakin (green diamond) and Port Sudan (hidden behing the black square) are shown. Omitting Al Lith produced unstable solutions. The positions for S2 and N2 are also shown

for a viable position. The positions of the N2 and S2 amphidromes are also plotted; the S2 is located away from the line of normal daily positions, probably due to the distorting atmospheric pressure effects on the subsurface pressures, but N2 is displaced as expected for amphidrome movement away from the central axis for bigger tidal amplitudes (N2 and M2 combined) (Pugh 1981). The alignment of the blue diamonds in Fig. 2.17 along a line which is at right angles to the central Red Sea axis conﬁrms the validity of our two-Kelvin-wave model. Figure 2.18 shows the daily positions with the axis rotated 230 anticlockwise from north, the best ﬁt to the along-Red Sea axis. The X-axis scale is compressed here, showing that even the more extreme daily positions are close to the theoretical line. The actual position of a central axis for Kelvin wave dynamics is not easily estimated because of coastal curvature and the wide distribution of coral reefs. However, by plotting on a Red Sea Admiralty chart (number 158) the displacement of the amphidrome at 38.1090E and 19.6990N from an estimated geographical central axis is between 45 and 60 km. The dashed blue line in Fig. 2.18 covers the estimated position of the central line where the two wave amplitudes would be equal, and the width of the line represents the uncertainty in estimating its position. We can compare movement with the theoretical expressions in Eqs. 4 and 5. For the northern end of the Red Sea, in the Gulf of Suez, and the S2/M2 ratio of 0.25 (Table 2.1), the frequency has maximum and minimum values of 29.290/h and 28.180/h, above and below the average of 28.980/h (see Lamb 1932, Sect. 224; Pugh 1981). If the amphidrome is on average (i.e., for M2) 800 km from the wave reflection at the northern end of the Red Sea, then at spring tides the amphidrome will move 10 km north, nearer to the reflecting point, and at neap tides the amphidrome will be 6 km farther south, away from the reflecting point.

34

D. T. Pugh et al.

Fig. 2.18 The amphidrome positions in kilometres, with the Y-coordinate rotated 230 anticlockwise from north, along an axis closely aligned to the Red Sea axis. The dashed vertical line is the estimated central axis Y = 0

The cross-sea y-axis amphidrome displacements will depend on the relative incident and reflected wave amplitudes, a, or more speciﬁcally as the natural logarithm of a, ln a (Eq. 4b). More energy is lost at spring tides than at neaps because of the stronger currents, and so it is expected that the reflected wave will be relatively weaker during spring tides, and that at these times the amphidrome can be displaced farther toward the Sudan coast. As Eq. (4b) shows, the displacement also depends on the latitude and the water depth. For the Red Sea at 200N, the Fig. 2.19 The relationship between the amplitude ratio of the ingoing and outgoing waves, and the amphidrome displacement

displacement from the centre is plotted in Fig. 2.19 as a function of a, the incident/reflected Kelvin wave amplitude ratio. The approximate Red Sea coastal boundaries are plotted as vertical dashed red lines. The amphidrome would be degenerate for a values less than 0.85. Figure 2.20 shows the amphidrome displacement from the northern reflection as a function of the daily semidiurnal tidal range, as represented by the range at KAUST. The coordinates are again as in Fig. 2.2. There is some scatter, but the overall trend is consistent with the movement

2

The Tides of the Red Sea

35

Fig. 2.20 The relationship between daily D2 semidiurnal amplitudes at KAUST, and the X-displacement of the amphidrome from its mean position, with coordinates aligned along and orthogonal to the Red Sea axis. This is related to the changes of the wave period from spring to neap tides. The red lines show spring and neap ranges at KAUST. The black line is the theoretical displacement from Eq. 4a

Fig. 2.21 The relationship between daily D2 semidiurnal amplitudes at KAUST, and the Y-displacement of the amphidrome from its mean position, with coordinates aligned along and orthogonal to the Red Sea axis (Fig. 2.2). This is related to the ratio of incident and reflected Kelvin wave amplitudes

southward at neap tides and northward at springs. The dashed black line shows the theoretical relationship as in Eq. 4a. Figure 2.21 shows the displacement from the central axis also using the coordinates as in Fig. 2.2. The blue line is the estimated central axis. Almost all values are showing a weaker reflected Kelvin wave, though there are some cases of a larger outgoing wave with positions to the right. The displacements mostly cluster about the mean, with no systematic increase as tidal ranges increase, though it is worth

noting that there is a tendency for the larger displacements to occur on the larger tidal ranges in the upper left quadrant.

Energy Budget Tidal Energy It is interesting to estimate tidal energy losses in the Red Sea and to relate them to the total global tidal energy budget.

36 Table 2.9 Energy fluxes into the Red Sea through the Hanish Sill transect (from Jarosz et al. 2005a, 2005b)

D. T. Pugh et al. Values are in Gigawatts Flux

O1

K1

N2

0.005

0.018

0.016

Global dissipation

M2

S2

Spring

Neaps

0.187

0.016

0.726

0.055

2500 0.01

Tidal energy is dissipated by friction in shelf seas, and also by losses to internal tides in the deep ocean Munk (1997). About 1 TW of energy is lost in the deep ocean, generally near areas of rough seabed topography. This energy is thought to be lost through internal tide generation and dissipation, a process which substantially contributes to the energy needed to maintain the large-scale thermohaline circulation of the ocean. Our two-dimensional Red Sea model cannot capture this internal energy sink process. The dissipation in shallow water due to bottom friction is concentrated in areas of resonance and large tides. The ﬁrst ﬁve areas are: Hudson Bay/Labrador (260 GW), European Shelf (210 GW), Yellow Sea (150 GW), NW Australian Shelf (150 GW) and the Patagonian Shelf (110 GW). Together, they account for more than half the estimated 1.6 TW of M2 total shelf dissipation. The total diurnal and semidiurnal shallow water dissipation is 2.5 TW. The total dissipation in the deep ocean due to internal tides, and in the shallow water areas due to bottom friction is estimated as 3.5 TW (see Pugh and Woodworth (2014) for a more detailed global discussion). The dissipation in the Red Sea is very small by comparison, but is worth evaluating as there are many such marginal seas that can contribute to the energy budget. First, we review the two methods available to us for computing energy fluxes and dissipation.

Fluxes Across Boundaries The tidal energy transmitted across a boundary may be calculated by integrating the energy fluxes that are computed from observed currents and elevations, or currents and elevations computed by numerical models. Clearly, if numerical models represent the currents and elevations over an area correctly, they must include the correct distribution of the areas of frictional energy dissipation. The instantaneous flux of energy per unit of cross section, in the direction of current U is: 1 2 Flux ¼ ðH þ fÞq jU j þ gf U ð10aÞ 2

Per cent

where q is the water density, g is gravitational acceleration, H is the water depth and f is the sea level difference from the mean sea level. This expression includes both the kinetic and potential energy fluxes. Fluxes are computed in the X and Y directions for each iteration and averaged over the period of each constituent for O1, K1, N2, M2 and S2. The results for the flow across a section at the Hanish Sill are given in Table 2.9. For a unit width of section over a tidal cycle, the fluxes can also be computed directly from the harmonic constituents: average energy flux =

1 qgDH0 U0 cos gf0 gU0 ð10bÞ 2

where H0 ; gf0 and ðU0 ; gU0 Þ are the amplitudes and phases of the elevations and currents for a particular constituent (see Pugh and Woodworth 2014, Appendix D). For a progressive wave, the currents and elevations are in phase and the currents are at a maximum at the same time as high water. As a result, there is maximum energy flux in the direction of the wave propagation. For a standing wave, there is no net energy flux because the currents and elevations are 900 out of phase, with maximum currents coinciding with the mid-tidal level. In the real world, a perfect standing wave cannot develop because there must be some energy lost at the reflection, and this energy must be supplied by a progressive wave component. Calculation of the total energy flux due to combinations of all the tidal harmonic constituents is very easy; they may be independently added arithmetically in the same way as the variance at several frequencies in a time series may be added. In general terms, the energy flux is proportional to the square of the constituent amplitudes, so that for the Red Sea the S2 energy flux is only about 10% of the M2 flux, and the energy flux due to other constituents is negligible.

Frictional Dissipation Energy losses in shallow seas result in a systematic adjustment of the tidal patterns and amphidrome locations as described earlier (Pugh 1981).

2

The Tides of the Red Sea

Frictional energy losses are related to the cube of the current speed, which means that much more energy is absorbed from the Kelvin wave at spring tides than at neap tides. It also means that dissipation is a localised phenomenon, in our case especially at the northern end in the Gulf of Suez. As a result, the reflection coefﬁcient a for the wave is much less at spring tides, and so the amphidrome displacement from the centre is greater. We might expect to see some spring-neap effects in the Y-displacement of the Red Sea central amphidrome, though this is not evident in Fig. 2.21. Over a spring-neap cycle the average value of dissipation (Jeffreys 1976) is: 9 2 9 4 3 UM c c 1 þ þ ð11Þ 2 4 64 where c is the ratio of the S2 and the M2 current constituent amplitudes. For the Equilibrium Tide the ratio c = 0.46, which implies that the average energy dissipated over a spring-neap cycle is 1.48 times that dissipated by M2 alone. In the northern Red Sea, where c = 0.3 (Table 2.3) the average dissipation over a spring-neap cycle is 1.20 times the M2 dissipation.

Fig. 2.22 Tidal energy dissipation rate (W/m2) for spring tides. Also shows the Hanish Sill transect (Table 2.9)

37

Figure 2.22 shows the energy losses in watts per square metre, for spring tides. Almost all diurnal and semidiurnal tidal energy, which is advected to or/and generated in the Red Sea, is dissipated below 180N. There are also enhanced dissipation rates, especially for the energetic semidiurnal constituents, in the Gulf of Suez. Table 2.9 shows the flux into the Red Sea through a transect at the Hanish Sill (Fig. 2.22). The M2 fluxes are much higher than for any other constituent. Note that representing any internal tidal dissipation is not possible in our two-dimensional model. On this basis, the tidal energy actually lost in the Red Sea is less than 0.01% of that dissipated globally. Dissipation for M2 in the Bab el Mandeb Strait entrance may be 0.02% of the global total (Jarosz et al. 2005a).

Internal and External Forcing Proudman (1953), Defant (1961) and others have reflected on the importance of direct gravitational forcing on Red Sea tides. Although we found the best ﬁt to the observation was obtained when the model was driven only by external Gulf

Fig. 2.23 Co-tidal map for the direct forcing only, for O1

38

Fig. 2.24 Co-tidal map for the direct forcing only for M2

of Aden tides, we have also run the model driven only by direct forcing within the Red Sea. The results for both O1 and M2 are shown in Figs. 2.23 and 2.24. Tides were allowed to radiate energy out of the Bab el Mandeb Strait. Both charts have distinct amphidromes. The O1 diurnal tides are quite small, but the M2 semidiurnal tides have amplitudes of more than 10 cm on the Dahlak Bank.

Conclusions Although they have small ranges, the tides of the Red Sea have been of considerable historical scientiﬁc interest. This is because they can be modelled as classical quarter-(diurnal) and half-(semidiurnal) Kelvin wave resonance. The ﬁrst numerical model of tides was developed for the Red Sea. However, rigorous testing of the many published model outputs has been limited by the very limited supply of sea level data and tidal analyses for the region. In this chapter, we have presented important new data from several sources, and tested a hitherto unpublished 2-D hydrodynamic model against the solid observational base.

D. T. Pugh et al.

The resulting co-tidal maps represent the best published representation of the four principal tidal constituents, O1, K1, M2 and S2. A caution is necessary when interpreting the K1 and S2 maps, because subsurface pressure observations include effects of twelve-hour oscillations of air pressure on tides in the tropics in the atmospheric pressures. Our best-ﬁt maps using the model are driven by Gulf of Aden forcing only; it was not necessary to include forcing by direct gravitational effects. While a scientiﬁcally satisfying model output would include all forcing and ﬁt the observations exactly, this proved impossible despite several experimental model adjustments, mainly by locally adjusting friction coefﬁcients. Possible unmodelled effects may include lateral boundary friction in the extensive shallow coral reefs (we assumed a no-slip boundary condition), and energy losses to coastal lagoons and internal tides. One of the most important omissions may point to the limits of two-dimensional tidal modelling in semi-enclosed seas, because of the loss of energy due to internal tidal dissipation; in general, internal tidal dissipation increases as the square of the amplitudes, whereas frictional barotropic energy losses are related to the cube of the current speed (Green and Nycander 2013). A full three-dimensional model would be needed to include these effects. The central semidiurnal amphidrome is well reproduced in models, and we have located its position more exactly by using daily tidal analyses from the local coastal stations. The movements of this amphidrome through a spring-neap cycle due to small frequency changes were clearly seen in the daily positions, but orthogonal movement due to varying energy dissipation was less evident. Future modelling, necessarily three-dimensional, may address and incorporate the impact of direct gravitational forcing, and reduce small but systematic differences for observations. Meanwhile, the results published here represent a major advance on any previously published tidal representations. Acknowledgements Several colleagues have helped substantially in this work, particularly in the collection of data, sometimes in difﬁcult locations. Elfatih Bakry, Ahmed Eltaib, and the Institute of Marine Research, Red Sea University, Port Sudan, managed the measurements in the Sudan, often in environmentally difﬁcult conditions. The KAUST sea level and current observations were curated by Mohammedali Nellayaputhenpeedika. The excellent strategic series of sea level measurements along the Saudi Arabian coast were made available, courtesy of the President of the Saudi General Commission for Survey. Within the GCS, it is a pleasure to acknowledge several valuable discussions on Red Sea tides with inter alia, Mohammed Al Harbi, Dr. N. T. Manoj, and Salem Salman Salem Al-Ghzwani. In addition, the work has been encouraged and advised by Dr. Dirar Nasr, Dr. Ian Vassie and Dr. Philip Woodworth. We are grateful to Dr. Mattias Green for help with the section on altimetry data and Fig. 2.4, and for suggestions on the importance of internal tidal energy dissipation.

2

The Tides of the Red Sea

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39 Technical Report DRP-92-6, U.S. Army Engineers Waterways Experiment Station, Vicksburg, MS, 137 pp Lynch DR, Gray WG (1979) A wave equation model for ﬁnite element tidal computations. Comp Fluid 7:207–228 Madah F, Mayerle R, Bruss G, Bento J (2015) Characteristics of tides in the Red Sea region, a numerical model study. Open J Marine Sci 5:193–209. https://doi.org/10.4236/ojms.2015.52016 Mohamad KAIA (2012) Sea level variation in the Red Sea based on SODA data. Thesis, Geophysical Institute, University of Bergen, M. Sc Monismith SG, Genin A (2004) Tides and sea level in the Gulf of Aqaba (Eilat). J Geophys Res 109:C04015 Morcos SA (1970) Physical and chemical oceanography of the Red Sea. Oceanogr Mar Biol Ann Rev 8:73–202 Munk W (1997) Once again: once again—tidal friction. Prog Oceanog 40:7–35 Murray SP, Johns W (1997) Direct observations of seasonal exchange through the Bab el Mandeb Strait. Geophys Res Lett 24:2557–2560 Naval Oceanographic Ofﬁce (NAVOCEANO) (1997) Data base description for Digital Bathymetric Data Base-Variable Resolution (DBDB-V), Version 1.0. Internal Report, Naval Oceanographic Ofﬁce, Stennis Space Center, MS Patzert WC (1974) Wind-induced reversal in Red Sea circulation. Deep Sea Res 21:109–121 Proudman J (1953) Dynamical oceanography. Methuen, London, p 410 Pugh DT (1981) Tidal amphidrome movement and energy dissipation in the Irish Sea. Geophys J R Astron Soc 67:515–527 Pugh DT, Woodworth PL (2014) Sea-level science: understanding tides, surges, tsunamis and mean sea level changes. Cambridge University Press, 395 pp Pugh DT, Abualnaja Y (2015) Sea-Level changes. In: Rasul NMA, Stewart ICF (eds) the red sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer Earth System Sciences, Berlin Heidelberg, pp 317-328. https://doi. org/10.1007/978-3-662-45201-1_18 Ray RD, Ponte RM (2003) Barometric tides from ECMWF operational analyses. Ann Geophys 21:1897–1910 Reid RO (1990) Water level changes. In: Herbich J (ed) Handbook of coastal and ocean engineering. Gulf Publishing, Houston, TX Schwiderski EW (1980) On charting global ocean tides. Rev Geophys 18:243–268 Sultan SAR, Ahmad F, Elghribi NM (1995) Sea level variability in the central Red Sea. Oceanol Acta 18(6):607–615 Sultan SAR, Elghribi NM (2003) Sea level changes in the central part of the Red Sea. Indian J Marine Sci 32:114–122 Taylor GI (1920) Tidal friction in the Irish Sea. Phil Trans Roy Soc London A 220:1–33. https://doi.org/10.1098/rsta.1920.0001 Taylor GI (1922) Tidal oscillations in gulfs and rectangular basins. Proc London Math Soc S20:148–181. https://doi.org/10.1112/plms/s220.1.148 Vercelli F (1925) Richerche di oceanograﬁa ﬁsica eseguite della R. N. AMMIRAGILIO MAGNAGHI (1923–24), Part I. Correnti e mare. Annali Idrograﬁci 11:1–188 Vercelli F (1927) Richerche di oceanograﬁa ﬁsica eseguite della R. N. AMMIRAGILIO MAGNAGHI (1923–24), Part IV, La temperatura e la salinita. Annali Idrograﬁci 11:1–66 Vercelli F (1931) Nuove ricerche sullen correnti marine nel Mar Rosso. Annali Idrograﬁco 12:424–428 Wahr J (1981) Body tides on an elliptical, rotating, elastic and oceanless Earth. Geophys J R Astron Soc 64:677–703 Westerink JJ, Blain CA, Luettich RA, Scheffner NW (1994) ADCIRC: an advanced three-dimensional circulation model for shelves, coasts and estuaries. Report 2: Users manual for ADCIRC-2DDI.

40 Dredging Research Program Technical Report DRP-92-6, U.S. Army Engineers Waterways Experiment Station, Vicksburg, MS, 156 pp Yang Y, Zuo J, Li J, Jia Sun J, Wei Tan W (2013) Simulation of the tide in the Red Sea and the Gulf of Aden. Proceedings of the

D. T. Pugh et al. twenty-third (2013) International offshore and polar engineering anchorage, Alaska, USA, June 30–July 5, 2013. Published by the international society of offshore and polar engineers (ISOPE). ISBN 978-1-880653-99–9; ISSN 1098-6189

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Physical and Chemical Properties of Seawater in the Gulf of Aqaba and Red Sea Riyad Manasrah, Ahmad Abu-Hilal and Mohammad Rasheed

Abstract

The Gulf of Aqaba is located in the sub-tropical arid zone between 28o–29o30′N and 34o30′–35oE. It is a semi-enclosed basin that extends over a length of 180 km with a width between 5 and 25 km (average of 16 km). The deepest point in the Gulf reaches 1825 m with an average depth of 800 m. The Gulf is connected to the Red Sea by the Strait of Tiran, which has a sill depth of about 265 m. The Gulf exhibits a seasonal cycle of stratiﬁcation in spring, maintenance of a shallow thermocline in summer, and subsequent deepening of the thermocline to produce deep mixed layers in winter. Much of the seasonal stratiﬁcation variability is determined by exchanges with the rest of the Red Sea. Nonetheless, inter-annual variability in wintertime temperatures appears to set the depth of maximum mixing. Because of being generally warm (>21 ºC), and subject to dry winds much of the year, the Gulf is a site of high evaporation rates, estimated at 0.5–1.0 cm/day, with recent estimated values lower than earlier ones. Given a surface area of the Gulf of about 1.7 109 m2, this implies a net inflow to the Gulf of about 54 m3s−1. Because the densities of the Gulf are different from the rest of the Red Sea, there are strong density-driven flows. These exchange flows through the Strait of Tiran are substantially larger than the net flows through the Straits. About 3 104 m3s−1 enters the Gulf near the surface, and leaves at depth through the Strait. The exchange varies annually with a net annual mean of 1.8 104 m3s−1. Surface water temperature may approach 28 ºC during summer months and fall to just above 20 ºC in winter. R. Manasrah (&) Faculty of Marine Sciences, The University of Jordan, Aqaba, Jordan e-mail: [email protected] A. Abu-Hilal Faculty of Science, Yarmouk University, Irbid, Jordan M. Rasheed Chemistry Department, The University of Jordan, Amman, Jordan

The generally weak currents (10 cm s−1) in the northern Gulf of Aqaba are largely driven by the prevailing down-Gulf winds and by the semi-diurnal internal tides generated in the Strait of Tiran. The annual meteorological measurements demonstrate that the wind speed fluctuates within a range of 0–12 ms−1 (mean 4.5 ± 2.4 ms−1). Moreover, a harmonic change of wind speed appears during summer causing a diurnal cycle that is represented by strong winds during daytime and relatively weaker winds during the night. Meanwhile, northerly winds (NNW-NNE) dominate over the study area and represent about 85% of total measurements. Mean values of air temperature range between 32.2 ± 3.16 °C in summer and 17.6 ± 3.46 °C in winter. The minimum humidity recorded in summer is 13% compared to a maximum of 83% in winter. The maximum sea level range, with reference to Global Mean Sea Level (MSL), during the year 2013 was 154.3 cm. The highest value was 101.7 cm observed on December 12, and the lowest value was −52.6 cm recorded in April 23. The pH at coastal and offshore waters of the Jordanian Gulf of Aqaba fluctuates around 8.3 with very minor temporal and spatial variations. This is typical for all coral reef waters because these waters are always saturated with calcium carbonate, which acts as a buffer and resists change in the pH. Inorganic nutrients (ammonia, nitrate, nitrite, phosphate and silicate) are essential for marine phytoplankton productivity and growth. Higher concentrations of nutrients and chlorophyll a concentrations occur during winter that are attributed to deep water vertical mixing during winter. Cross-shore mixing (from shallow to offshore waters) due to density currents (gravity currents) has been recently documented. This process drives coastal water down slope offshore when it gets cooler at night. The increased nutrient concentrations in the euphotic zone enhance primary productivity, resulting in higher phytoplankton abundance and increased chlorophyll a concentrations. Water column stratiﬁcation and high irradiance during summer result in

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_3

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a depletion of the inorganic nutrients in the upper waters by enhanced primary productivity at the subsurface level (50–75 m). Ammonium concentration fluctuates irregularly around 0.4 lM with a tendency to higher concentrations during the winter months (January to March). Nitrate and nitrite concentrations during the last ﬁve years showed a regular shift from a summer low (0.10 and 0.01 µM) to relatively high early winter values (0.6 and 0.25 µM). Phosphate concentrations are generally low during summer (*0.02 µM) and high during winter (*0.10 µM). Silicate concentrations show the same trend with 1.0 µM during summer and *2.0 µM in the winter. Dissolved oxygen concentrations at the Gulf of Aqaba show a regular pattern, inversely proportional to that of temperature, with a range of 6.4 to 7.4 mgl−1, indicating that the effects of the other ecosystem variables are masked by temperature. Waters of the Gulf of Aqaba are very well balanced in terms of respiration and photosynthesis and well ventilated due to the annual deep mixing with a saturation of 100%.

Introduction The Red Sea (Fig. 3.1) is a young (about 25 million years) body of water (Bosworth et al. 2005), created by the pulling apart of Africa and Arabia. It extends NNW to SSE between 12°N, 43°E and 30°N, 32°E and has a surface area of about 458,000 km2. It is a narrow elongated body of water, connected at its northern end with the Mediterranean Sea through the man-made Suez Canal and at its southern end with the Indian Ocean through the Strait of Bab el Mandab. Near latitude 28°N, the Red Sea bifurcates into a Y-shape to form the Gulf of Suez and Gulf of Aqaba. The Red Sea proper (excluding the Gulfs) extends for about 2000 km. The shorelines of the sea are straight in the north but notably sinuous in its central and southern parts where they form vast bays. The distance between the eastern and western Red Sea coasts (width) is 180 km at its narrowest part and about 360 km at the widest part at Massawa (Coleman 1974), while its average width at Bab el Mandab is only 27 km. The northern limit of the Red Sea in the Gulf of Aqaba lies at latitude 29°32′48″N, while the northern limit in the Gulf of Suez at Suez Bay is at latitude 29°57′18″ N (Fouda and Gerges 1994). The Red Sea is typically bounded on the landward side by a more or less narrow coastal strip (40–60 km wide), backed by high hills or mountains, which can rise to 3,000 m in some regions. In the northern and central Red Sea this central trough reaches to depths of more than 2,000 m, with the greatest depth at 2,860 m. From this trough, the seabed rises sharply to a terrace at depths of between 1,000 m and 600 m. This

terrace rises again to a continental shelf with a maximum depth of 300–400 m, and is often much shallower at around 50 m deep (PERSGA 2006). The continental shelf of the Red Sea is 15–30 km wide in the north and about 120 km wide in the south. However, in the most southerly part of the sea, the Farasan and Dahlak banks are considered as parts of a shallow shelf extending to the centre of the sea. All these geomorphic features are framed by a strip of coral reefs. Coral reefs fringe the entire Red Sea coast except for local break-ups at the mouths of ephemeral streams (Fouda and Gerges 1994; PERSGA 2006). The Gulf of Aqaba extends for 180 km with widths varying from 25 km in its southern part to 16 km at the north. The Gulf proper is divided into three elongated deep basins striking northeast. The northern basin is the shallowest (900 m deep) and is characterized by its flat bottom, while the other two deeps have irregular bottom topography and much greater depths. The maximum water depth in the Gulf reaches up to 1850 m in the central basin (Friedman 1985). With the exception of the northernmost part of the Gulf, fringing coral reefs grow along the entire coastline, varying in width between 10 and 100 m, depending on the slope gradients at the shelf edge (Friedman 1985). The Dead Sea transform system extends from the spreading ridge of the Red Sea northward to a zone of continent-continent collision in the Alpine orogenic belt in southern Turkey (Fig. 3.2). The structure, topography, and history of the entire region are expressions of continental plates moving along a transform system. The transform zone is about 1000 km long and marks the boundary between the western edge of the Arabian plate and the northern part of the African plate. The main structure is the strike-slip fault zone, which involves several separate fault planes that slice through the entire lithosphere (Opulithe 2014; Christiansen and Hamblin 2015). These faults are not straight but have several angular bends. As a result, large, deep pull-apart basins have formed along the strike-slip fault zone (Fig. 3.3). The Gulf of Aqaba (Elat) segment is the widest and deepest. The floor of one of these basins is about 1850 m below sea level. Further north, the Dead Sea trough is another pull-apart basin; it is 400 m below sea level, with water depths exceeding 300 m in places. Sediment ﬁlling the Dead Sea trough is derived from erosion of the adjacent mountains. It is several kilometres thick and continues to pour into the graben, forming alluvial fans. In a more humid climate, the Dead Sea trough would be a freshwater lake extension of the Gulf of Aqaba. The structural features north and south of the Dead Sea are no less impressive. Note the direction of plate movement illustrated in Fig. 3.2. The Arabian plate is moving northward relative to the African plate. Two major bends in the strike-slip fault system occur, one to the north in Lebanon and Syria and the other south of the Dead Sea. As the plates move near these bends, slippage

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Fig. 3.1 Red Sea topographic maps, with elevations in metres. The locations of Gulf of Aqaba (GAQ), Gulf of Suez (GS), Gulf of Aden (GA), Mediterranean Sea (ME), Tokar Gap (TG), Strait of Bab el Mandeb (SBM) are shown (After Zhai and Bower 2013)

Fig. 3.2 The Dead Sea transform system connects the Red Sea spreading ridge with the Alpine convergent belt. The movement along the transform zone has produced the long, deep, narrow pull-apart basins of the Gulf of Aqaba and the Dead Sea as well as the contractional folds of the northern Sinai and the Palmyra Mountains of Lebanon and Syria. Small eruptions of basalt occurred near the pull-apart basins (Opulithe 2014; Christiansen and Hamblin 2015)

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Fig. 3.3 Pull-apart basins in the Gulf of Aqaba and the Dead Sea dominate this photograph Taken from the Space Shuttle. Such basins are caused by movement on strike-slip faults that have sharp bends and offsets of the major faults (inset). These form three deep basins along the floor of the Gulf of Aqaba and the Dead Sea basin that lies below sea level (Opulithe 2014; Christiansen and Hamblin 2015)

along the fault is inhibited and broad zones of transpression result. This formed compressional folds that branch off the strike-slip fault zone in the Palmyra Mountains to the north (Fig. 3.2) (Opulithe 2014; Christiansen and Hamblin 2015). The Gulf of Aqaba oriented NNE-SSW is the northernmost sea-flooded part of the Syrian-African rift system (Figs. 3.4 and 3.5). The Dead Sea transform plate boundary offers a unique opportunity to study crustal and upper mantle deformation associated with strike-slip motion because of the simple and well-exposed pretransform geology and the slow (60%) in the Red Sea, where anthropogenic (mainly petroleum) inputs are apparently only signiﬁcant in sediments (>30%). It also indicates that short- or long-range transport of ﬁne dust particles, and coastal human activities including oil production and transportation could be major sources of organic detritus and pollutants to the marine environment.

Conclusions The analyses of dust, surface seawater particulate matter and sediments from various locations of the Red Sea show that natural biogenic and anthropogenic sources are both contributors to their organic matter contents, but the relative contributions vary spatially. The organic compounds include n-alkanes, methyl n-alkanoates, n-alkanols, n-alkanoic acids, sterols, carbohydrates, hopane and sterane biomarkers, and UCM. The natural sources of organic compounds are mainly from terrestrial vegetation, marine primary production and microbial inputs. They are higher in atmospheric dust and surface seawater particulate matter compared to the sediments. Anthropogenic organic compounds are more important in sediments (>30%) and depend on the location and the types of human coastal activities.

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The results of this study indicate that both natural and anthropogenic components contribute to organic inputs in the Red Sea. Thus, to carefully construct any predictive model for short- or long-range transport of such components in dust aerosols, coastal natural and/or anthropogenic inputs, and to understand their impacts on the coastal environments and the biogeochemical cycles of carbon in the marine environment, reliable information and analytical data are needed. Such information and data should include the sources, characteristics, and composition of both organic and inorganic components delivered by these processes. In addition, chemical composition (i.e., organic and inorganic) and physical properties of the coastal shelf sediments of the Red Sea and of the ﬁne aerosol dust are lacking. Thus, national and international scientiﬁc collaborations and efforts must be initiated to study the impacts of these processes and sources on the biogeochemistry of the Red Sea. Acknowledgements The authors thank Dr. Najeeb M.A. Rasul for the invitation to participate in this book project.

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Sources of Organic Tracers in Atmospheric Dust …

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87 Gulf of Suez. Environ Geol 58:1675–1687. https://doi.org/10.1007/ s00254-008-1668-3 Rushdi AI, Al-Mutlaq KF, Simoneit BRT, Al-Azri A, DouAbul AAZ, Al-Zarban S, Al-Yamani F (2010) Characteristics of lipid tracers to the Arabian Gulf by runoff from rivers and atmospheric dust transport. Arab J Geosci 3(2):113–131 Rushdi AI, Oros DR, Al-Mutlaq KF, He D, Medeiros PM, Simoneit BR (2016a) Lipid, sterol and saccharide sources and dynamics in surface soils during an annual cycle in a temperate climate region. Appl Geoch 66:1–13 Rushdi AI, Al-Mutlaq KF, El-Mubarak AH, Al-Saleh MA, El-Otaibi MT, Ibrahim SM, Simoneit BRT (2016b) Occurrence and sources of natural and anthropogenic lipid tracers in surface soils from arid urban areas of Saudi Arabia. Environ Pollut 208:696–703 Saad MAH, Kandeel MM (1988) Distribution of copper, iron and manganese in the coastal Red Sea Waters in front of Al-Ghardaqa. Proc Indian Nat Sci Acad 54:642–652 Sanders MJ, Morgan GR (1989) Review of the Fisheries Resources of the Red Sea and Gulf of Aden. United Nations, Food Agriculture Org, Rome, Fisheries Technical Paper 304, 138 pp Savoie DL, Prospero JM, Nees RT (1987) Nitrate, non-sea-salt sulfate, and mineral aerosol over the northwestern Indian ocean. J Geophy Res 92:933–942 Schauer JJ, Kleeman MJ, Cass GR, Simoneit BRT (2002) Measurement of emissions from air pollution sources. 5. C1-C32 organic compounds from gasoline-powered motor vehicles. Environ Sci Technol 36(6):1169–1180 Simoneit BRT (1977) Organic matter in eolian dusts over the Atlantic Ocean. Mar Chem 5:443–464 Simoneit BRT (1978) The organic chemistry of marine sediments. In: Riley JP, Chester R (eds) Chemical oceanography, vol. 7, 2nd edn. Academic Press, New York, pp 233–319 Simoneit BRT (1984) Organic matter of the troposphere-III. Characterization and sources of petroleum and pyrogenic residues in aerosols over the Western United States. Atmos Environ 18:51–67 Simoneit BRT (1985) Application of molecular marker analysis to vehicular exhaust for source reconciliation. Int J Environ Anal Chem 22:203–233 Simoneit BRT (1989) Organic matter of troposphere—V: application of molecular marker analysis to biogenic emissions into the troposphere for source reconciliations. J Atmos Chem 8:251–275 Simoneit BRT (2002) Biomass burning—a review of organic tracers for smoke from incomplete combustion. Appl Geochem 17:129–162 Simoneit BRT (2006) Atmospheric transport of terrestrial organic matter to the sea. In: Volkman JK (ed) The Handbook of Environmental Chemistry, vol. 2. Part N. Marine organic matter, biomarkers, isotopes and DNA. Springer, Berlin, pp 165–208 Simoneit BRT, Mazurek MA (1982) Organic matter of the troposphere —II. Natural background of biogenic lipid matter in aerosols over the rural western United States. Atmos Environ 16:2139–2159 Simoneit BRT, Mazurek MA, Reed WE (1983) Characterization of organic matter in aerosols over rural sites: phytosterols. In: Bjorøy M et al (eds) Advances in organic geochemistry 1981. Wiley, Chichester, pp 355–361 Simoneit BRT, Sheng G, Chen X, Fu J, Zhang J, Xu Y (1991) Molecular marker study of extractable organic matter in aerosols from urban areas of China. Atmos Environ 25A:2111–2129 Simoneit BRT, Elias VO, Kobayashi M, Kawamura K, Rushdi AI, Medeiros PM, Rogge WF, Didyk BM (2004) Sugars—dominant water-soluble organic compounds in soils and characterization as tracers in atmospheric particulate matter. Environ Sci Technol 38:5939–5949 Stalling DL, Gehrke CW, Zumwalt RW (1968) A new silylation reagent for amino acids bis(trimethylsilyl) trifluoroacetamide (BSTFA). Biochem Biophys Res 31:616–622

88 Stein M, Almogi-Labin A, Goldstein SL, Hemleben C, Starinsky A (2007) Late Quaternary changes in desert dust inputs to the Red Sea and Gulf of Aden from 87 Sr/86 Sr ratios in deep-sea cores. Earth Planet Sci Lett 261:104–119 Stephanou EG, Stratigakis NE (1993) Determination of anthropogenic and biogenic organic compounds on airborne particles: flash chromatographic fractionation and capillary gas chromatographic analysis. J Chromatogr 644:141–151 Street JH, Anderson RS, Rosenbauer RJ, Paytan A (2013) n-Alkane evidence for the onset of wetter conditions in the Sierra Nevada, California (USA) at the mid-late Holocene transition, *3.0 ka. Quaternary Res 79(1):14–23 Tarasov PE, Müller S, Zech M, Andreeva D, Diekmann B, Leipe C (2013) Last glacial vegetation reconstructions in the extreme-continental eastern Asia: potentials of pollen and n-alkane biomarker analyses. Quaternary Int 290:253–263 Tegen I, Lacis AA, Fung I (1996) The influence of climate forcing on mineral aerosols from disturbed soils. Nature 380:419–422 Tindale NW, Pease PP (1999) Aerosols over the Arabian Sea: atmospheric transport pathways and concentrations of dust and sea-salt. Deep-Sea Res 46:1577–1595 Tratt DM, Frouin RJ, Westphal DL (2001) April 1998 Asian dust event: a southern California perspective. J Geophys Res Atmos 106 (D16):18371–18379

A. I. Rushdi et al. Uno I, Harada K, Satake S, Hara Y, Wang Z (2005) Meteorological characteristics and dust distribution of the Tarim Basin simulated by the nesting RAMS/CFORS dust model. J Meteor Soc Japan 83:219–239 Urban RC, Alves CA, Allen AG, Cardoso AA, Campos MLAM (2016) Organic aerosols in a Brazilian agro-industrial area: speciation and impact of biomass burning. Atmos Res 169:271–279 Volkman JK, Barrett SM, Blackburn SI, Mansour MP, Sikes EL, Gelin F (1998) Microalgal biomarkers: a review of recent research developments. Organic Geochem 29(5):1163–1179 Weisse T (1989) The microbial loop in the Red Sea: dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar Ecol Prog Ser 55(2):241–250 Wiesenberg GL, Schwark L (2006) Carboxylic acid distribution patterns of temperate C 3 and C 4 crops. Org Geochem 37 (12):1973–1982 Zech M, Zech R, Rozanski K, Gleixner G, Zech W (2015) Do n-alkane biomarkers in soils/sediments reflect the d 2H isotopic composition of precipitation? A case study from Mt. Kilimanjaro and implications for paleoaltimetry and paleoclimate research. Isot Environ Health Stud 51(4):508–524

5

Nitrogen, Phosphorus and Organic Carbon in the Saudi Arabian Red Sea Coastal Waters: Behaviour and Human Impact Radwan Al-Farawati, Mohamed Abdel Khalek El Sayed and Najeeb M. A. Rasul

Abstract

The Red Sea is an oligotrophic marginal sea where the main source of nitrogen and phosphorus is the Indian Ocean water flowing through the Bab al Mandeb entrance in the south. Therefore, the nitrogen and phosphorus concentrations are expected to decrease northward. External sources resulting from urban activities enhance the level of phosphorus, nitrogen and carbon in coastal waters around major cities along the Red Sea. We utilized the results of dissolved inorganic phosphorus (reactive phosphate), dissolved inorganic nitrogen (nitrate, nitrite and ammonium) and organic carbon (dissolved organic carbon (DOC) and particulate organic carbon (POC)) along the coast of Jeddah in the eastern Red Sea, in order to understand the distribution, sources, and biogeochemical processes that control their levels in sea water. Moreover, the results were used to calculate the anthropogenic flux and contribution to the total budget of the Red Sea. The spatial distribution patterns showed very high concentrations of nitrogen, phosphorus and organic carbon in the water at the southern coast of Jeddah in comparison to the northern coast. Most of the wastewater (>300,000 m3 per day) of the city is discharged at this part of the coast. The quantity is beyond the nominal treatment capacity of the existing wastewater treatment plants, resulting in poor treatment efﬁciency. Further evidence of the importance of sewage discharges was obtained using salinity variations. The salinity was remarkably low at these locations and the projections of R. Al-Farawati (&) Faculty of Marine Sciences, Marine Chemistry Department, King Abdulaziz University, Jeddah, Saudi Arabia e-mail: [email protected] M. A. K. El Sayed National Institute of Oceanography and Fisheries, Academy of Scientiﬁc Research and Technology, Alexandria, Egypt N. M. A. Rasul Center for Marine Geology, Saudi Geological Survey, Jeddah, Saudi Arabia

salinity against nitrogen, phosphorus and organic carbon revealed signiﬁcant negative correlations. The seasonal distribution of DOC and POC reflected the seasonality of the primary productivity, showing higher values in late spring. POC showed a substantial proportion, accounting for up to 29% of total organic carbon. Ammonium was the major component in autumn, representing about 60% of the total inorganic nitrogen (TIN), while in spring nitrate became the principal component, constituting approximately 62% of the TIN. The application of various techniques revealed that nitrogen was the potential limiting element. Direct measurements and calculations indicated that the daily production of total nitrogen and phosphorus associated with sewage discharges into Jeddah coastal waters is about 21261 and 3360 kg, respectively. The inorganic forms of nitrogen and phosphorus represent 43 and 45% of the total nitrogen and phosphorus introduced into the area. Anthropogenic nitrogen and phosphorus sources at this part of the Red Sea coast represent about 0.9 and 9.9% of the deﬁcit of the two elements through the Red Sea/Indian Ocean water exchange process at the Strait of Bab al Mandab.

Introduction The sea has gained importance in the economies of countries, particularly its supply of different resources, as well as its use for tourism and recreational activities in coastal zones. It is therefore not surprising to note the increasing population density in the coastal areas, which is estimated to represent up to 60% of the global population density (Pernetta and Milliman 1995; Hinrichsen 1998). As a consequence, increasing amounts of urban, agricultural and industrial wastes containing environmentally harmful substances are produced and introduced into the coastal waters. Sewage discharge into the sea is, until now, commonly observed as the main solution in handling and managing

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_5

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wastewater in many coastal cities around the world. However, dumping of sewage effluents has to meet international environmental standards in order to conserve and maintain the marine environment. During recent decades, Jeddah, a mega city on the eastern Red Sea coast, has witnessed a major economic and demographic expansion. Jeddah also hosts a wide variety of industrial activities, such as oil reﬁneries, petrochemicals, food conservation and canning facilities. Jeddah sea port is one of the most important ports along the Red Sea coast, and is under pressure because of the rapid growth in population (Fig. 5.1; Aljouﬁe and Tiwari 2015). Population growth is inevitably accompanied by an increase in potable water consumption, which implies the necessity of a suitable management of wastewater produced by urban activities (Fig. 5.2; Aljouﬁe and Tiwari 2015). Jeddah is at the boundary between the Mediterranean and a monsoon-type climate, giving it a distinct seasonal variation (Zahran and Gilbert 2010; Almazroui et al. 2012). The climate during some of the year is attractive to tourists which results in increasing the population of the city. This might have important economic spin-offs for the city but may also impact the “pollution potential” (Taylor and Ghazi 1995). The coastal waters of Jeddah extend along the eastern coast of Red Sea between latitude 21.25oN and 21.75oN. In general, the Jeddah coast is divided into two main areas, the Northern Corniche and Southern Corniche (Fig. 5.3). There are several sewage discharge points that dump treated, partially treated or untreated sewage along the coast. Most of the discharged effluent comes from three major sewage treatment plants (STP), the Al-Kumra, Al-Balad and Al-Ruwais STPs (Fig. 5.3). The Al-Kumra STP delivers 250,000 m3 day−1 of sewage effluent to the Southern Corniche (http://www.hutahegerfeld.com/completed-alkhumra.

Fig. 5.1 Population growth in Jeddah (Aljouﬁe and Tiwari 2015). Data after year 2013 is estimated based on growth rate

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Fig. 5.2 Wastewater production in Jeddah (Aljouﬁe and Tiwari 2015). Data after the year 2013 is projection based on the current and previous data

php), which corresponds to its nominal treatment capacity; however, the real volume may be about 300,000 m3 day−1 (El Sayed 2002a). Al-Balad (68,000 m3 day−1) and Al-Ruwais STP (38,000 m3 day−1) discharge sewage into the Al-Arbaeen and Reayat Al-Shabab Lagoons, respectively (El-Rayis and Moammar 1998). The high nutrient input to the two lagoons is accompanied by a reduced water renewal, due to their particular morphological features, and results in massive algal blooms accompanied by the creation of durable anoxic conditions (El Sayed 2002b; El Sayed et al. 2011, 2015). Several studies have demonstrated the presence of organic contaminants (petroleum hydrocarbons) and inorganic contaminants (trace elements) in sediments and water at areas of sewage disposal along the Jeddah coast (Basaham 1998; Turki et al. 2002; Turki 2006; Al-Farawati et al. 2008a, 2011; Al-Farawati 2010; El-Maradny et al. 2016). Sewage discharge is believed to be a major source of nitrogen, phosphorus and carbon to the marine coastal environment (Aminot et al. 1990a; El Sayed 2002c; Burford et al. 2012; Cravo et al. 2015; Boehm et al. 2016; Rada et al. 2016; Markogianni et al. 2017). The anthropogenic flux of dissolved carbon, nitrogen and phosphorus from land-based activities represents the same order of magnitude as that from the natural flux (Pernetta and Milliman 1995). In such an environment, the behaviour of nitrogen, phosphorus and carbon changes according to the magnitude of the quantities and flux. Ultimately, this modiﬁes the biogeochemical and ecological properties of the environment. This chapter is based on data collected during studies undertaken along the Jeddah coastal area between 1998 and 2010. The study areas represent different ecological environments, regular and exposed environments with a relatively short residence time and conﬁned coastal lagoon type environments with restricted water renewal. The study area

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Fig. 5.3 The coastal waters of Jeddah showing discharge points of three STPs: Al-Kumra, Al-Balad and Al-Ruwais

receives waste disposal from the STPs. We aim to address the distribution and behaviour of phosphorus, nitrogen, carbon, and their ecological implications, and to evaluate the magnitude of the contribution of wastewater disposal from the local STPs to the total phosphorus and nitrogen budget of the Red Sea. Information regarding cruises, methodology and data collection is detailed in the references cited in the text.

General Distribution of C, N and P and Interacting Processes The major common features of the distribution of carbon, nitrogen and phosphorus in the coastal waters of Jeddah in the eastern Red Sea are the presence of particularly elevated concentrations in the vicinity of wastewater effluents, remarkable seasonal concentration variation and regular

concentration decreases with increasing distance from the coast line seaward as well as from south to north. These features result from the interaction of the following factors in the dispersion of these elements in the coastal area: the presence of ﬁxed discharge points, mixing and dilution under the action of local eddies and large-scale dispersion due to the action of coastal currents and wind effects. Biological activity may be superimposed on these factors, not to modify the dispersion pattern but to increase or decrease the concentration of the different components (El Sayed and Niaz 1999; El Sayed 2002c; Basaham et al. 2009; Al-Farawati et al. 2010; Al-Farawati 2010). The distribution of DOC and POC (Fig. 5.4) shows clearly the impact of the sewage discharge of the Al-Khumra STP. The average concentrations of DOC and POC in spring, 1.10 ± 0.15 and 0.52 ± 0.31 mg l−1 respectively, are higher than their corresponding values in fall (0.94 ± 0.16 and 0.44 ± 0.36 mg l−1). Assuming a regular

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and constant sewage release into the area, enhanced spring biological activity may explain the seasonal concentration difference. Important seasonal variability has been reported in surface seawater and was related to phytoplankton development and decay (Maciejewska and Pempkowiak 2014; Szymczycha et al. 2017). In both seasons, while DOC comprises the major part of the organic carbon pool, its contribution is remarkably constant, representing about 68% of the total organic carbon. In open seawater, POC constitutes a minor fraction of the total organic carbon (TOC) pool (DOC + POC); however, in coastal water, due to enhanced biological activity and land based sources, POC participation may become more important, as has been observed in Chesapeake Bay (Fisher et al. 1998) and the Baltic Sea (Maciejewska and Pempkowiak 2014). The distribution of dissolved nutrients (nitrate, nitrite, ammonia and phosphate) is comparable to that of carbon; concentrations of these dissolved nutrients are relatively

Fig. 5.4 Surface distribution pattern of DOC and POC during autumn and spring in the coastal waters of Jeddah

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high at the southern extremity of the Jeddah coast and decrease northward. Obviously, sewage discharge from the Al-Kumra treatment plant enhances the levels of nutrients (Fig. 5.5). The distribution of nitrate and nitrite follow approximately the same conﬁguration. Concentrations decrease northward from the main sewage discharge point (Fig. 5.5). The average nitrate concentration in spring is 0.93 lM and is about three times higher than in the fall (0.35 lM). Factors such as organic matter degradation and regeneration from bottom sediments may add extra nitrate to the water column (Harrison 1992; Souza et al. 2014; Sommer et al. 2016). On the other hand, nitrate elimination is attributed to an increased rate of assimilation by phytoplankton (Karsh et al. 2014; Fawcett et al. 2015; Van Oostende et al. 2017). Nitrogen as nitrite has an intermediate oxidation state (+3) between nitrate (N = +5) and ammonium (N = −3). Therefore, it could be oxidized to nitrate or reduced to

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Fig. 5.5 Surface distribution pattern of NO3, NH4 and PO4 during autumn and spring in the coastal waters of Jeddah

ammonium, resulting in low nitrite levels in the ambient waters (Wada and Hattori 1991). In open seawater, ammonium is the ﬁrst product of the mineralization of organic nitrogen; it is rapidly assimilated by the primary producers

and its concentration is almost undetectable (Wada and Hattori 1991). In Jeddah coastal waters, ammonium concentration is as high as nitrate concentration; its average concentration varies between 0.45 lM in the fall and

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−1 Table 5.1 Range and average concentrations of NO2−, NO3−, NH4+, TIN, PO−3 4 (µM), and DOC and POC (mgl ) in Jeddah coastal waters. Values in brackets represent average concentrations

NO2−

NO3−

NH4+

TIN

PO−3 4

DOC

POC

Coastal waters of jeddah Autumn

0.002–0.058 (0.018)

0.03–1.28 (0.35)

0.00–0.93 (0.45)

0.02–1.61 (0.04)

0.67–1.23 (0.94)

0.19–1.78 (0.44)

Spring

0.004–0.088 (0.02)

0.21–2.93 (0.93)

0.17–4.37 (0.83)

0.10–2.07 (0.37)

0.98–1.69 (1.11)

0.29–1.73 (0.52)

Coastal lagoons Reayat Al-Shabab Lagoon 2009

1.58–4.95 (3.12)

1.38–6.30 (2.68)

34.2–107 (77)

37–118 (82)

3.98–16.53 (12.98)

11.8–17.0 (15)

–

2010

0.27–8.22 (5.56)

0.09–33.23 (12.42)

26.8–1099 (299)

35.3–1099 (317)

3.73–37.7 (17.74)

2.69–46–68 (8.55)

2.25–4.15 (3.19)

Al-Arbaeen Lagoon 2009

4.62–15.43 (8.52)

0.47–12.36 (3.74)

164–334 (232)

153–455 (244)

13.21–23.66 (16.0)

19.25–40.0 (26.25)

–

2010

3.23–41.63 (11.86)

6.03–81.59 (20.82)

127–604 (249)

141–647 (282)

10.58–26.89 (17.26)

2.16–28.05 (5.61)

1.76–28.83 (7.01)

0.03–0.2

–

–

0.05–0.10

–

–

Open waters (central Red Sea)a – a

Karbe and Lange (1981)

0.83 lM in spring (Fig. 5.5 and Table 5.1). Ammonium is one of the principal nitrogenous components in sewage water. Beside the impact of sewage discharge, in situ production of ammonium takes place through degradation of dissolved organic nitrogen by heterotrophic bacteria and nitrate reduction in oxygen deﬁcient aquatic environments. In coastal waters, elevated levels of phosphate are usually associated with the discharge of different types of domestic, agricultural and industrial waste (Burford et al. 2012; Cravo et al. 2015). Phosphate distribution during the period of the study follows the trend observed for the other elements. Concentrations are high in the effluent and sea port areas and then decrease away from them (Fig. 5.5). In the entire area, concentrations decrease from the coast seaward.

Behaviour of C, N and P in the Coastal Waters: Relationship with Salinity When land-based effluents of fresh or low salinity water are discharged into the coastal area, the seawater is diluted resulting in low salinity values. Since salinity is a conservative parameter, it is frequently used to describe the biogeochemical behaviour of any chemical component present in the effluent water (Chester and Jickells 2012). Components that correlate negatively with salinity are classiﬁed as conservative, which means that the physical water mixing process is the only major acting parameter affecting the

presence of the component in water; any other chemical, biological or geological process might be absent or is of minor importance. In contrast, deviation from the theoretical dilution line indicates a non-conservative behaviour and the component(s) of interest might suffer from major acting processes other than simple physical dilution (Chester and Jickells 2012). As nutrients pass along a salinity gradient, they may be subjected to a number of chemical, physical and biological processes including: sorption-desorption. precipitation-dissolution, flocculation-deflocculation and biological uptake and recycling (Eyre and Balls 1999). These processes govern the delivery of nutrients to coastal waters and also determine the type of ecological impact (Edmond et al. 1981; Kaul and Froelich 1984). Numerous studies have demonstrated the non-conservative behaviour of nutrients during fresh water-seawater mixing (Fisher et al. 1992; Mantoura and Woodward 1983; Sholkovitz 1976; Zvalinsky et al. 2005). On the other hand, conservative behaviour has also been documented in various natural environments (Aminot et al. 1990b; El-Sayed 1988). Dissolved organic carbon (DOC) plays an important role in the global carbon cycle (Hansell et al. 2002). The concentration of DOC in seawater is mainly controlled by anthropogenic input and biological activities (Hansell and Carlson 1998; Dittmar and Kattner 2003). Biological activities have been shown to affect the seasonal distribution of DOC in seawater (Hansell and Carlson 1998; Hansell et al. 2002; Maciejewska and Pempkowiak 2014, 2015;

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Fig. 5.6 Correlation of salinity with DOC and POC in autumn and spring along the coastal waters of Jeddah

Szymczycha et al. 2017). Seasonal variability indicates in situ production of DOC during spring and consumption during winter (Bøsrheim and Myklestad 1997). Despite a limited salinity gradient of about 0.4 units, the relationship of salinity with DOC and POC exhibits a clear negative linear pattern (Fig. 5.6). At the effluent discharge point, the concentrations are clearly above the dilution line, suggesting exogenic DOC input (Aminot et al. 1990b). DOC from anthropogenic sources is superimposed on natural background DOC, probably resulting from primary productivity. A large proportion of this natural DOC reservoir is probably of a refractory nature showing conservative behaviour after dilution with sewage effluents. Additional fresh DOC from the effluent contributes to the total DOC, reflecting a positive anomaly (Fig. 5.6). At zero salinity, estimation of DOC concentration in sewage effluent gives a value of 35 mg l−1, which lies in the range of DOC concentrations for tertiary treated sewage used for the irrigation

of green areas in Jeddah (10 and 67 mg l−1; Al-Farawati et al. 2008b). POC usually constitutes a minor amount of total organic carbon in oceanic waters (Chester and Jickells 2012). However, the fractions of POC increase signiﬁcantly in coastal waters as a result of urban activities. At the sewage discharge point, POC represents more than 50% of the TOC. The POC contribution to the organic carbon reservoir would drop to less than 30% if the direct contribution from the effluent were eliminated. In case the value at the sewage discharge point is eliminated, these percentages would drop to 27 and 29% respectively. Moreover, the ratio of DOC/POC remains constant throughout the area. A plot of POC against salinity exhibits a moderately negative correlation, conﬁrming direct and probably indirect inputs from sewage effluent (Fig. 5.6). A high input of nutrients due to sewage discharge is utilized by marine phytoplankton through the photosynthesis process to produce living tissues.

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This living fraction is the most important indirect source of POC to the surface waters of open ocean water (Chester and Jickells 2012). It is worth mentioning that the direct daily load of total organic carbon from Al-Khumra STP effluent is about 3435 kg. The potential production of total organic carbon that could be produced assuming a complete assimilation of the nutrient load of the effluent is estimated at 9000 kg, three times the value of the direct load. Nitrogen components exhibit variable relationships with salinity. The detection of clear relationships of chemical variables within a restricted salinity gradient is relatively hard. During autumn, only nitrite appears to have a traceable relation with salinity, showing the dilution effect on the distribution of this nitrogen component (Fig. 5.7). During spring, concentrations of all the chemical constituents are signiﬁcantly higher and the character of the relationships with salinity is distinct. Nitrate and nitrite appear to have a non-conservative behaviour (Fig. 5.8). In the vicinity of the effluent discharge point, the salinity gradient extends between approximately 38.75 and 38.9, and the dilution line is very steep; nitrate loses more than 2 lM and nitrite loses about 0.06 lM. In the rest of the area, the slope of the dilution is much smoother; for approximately 0.35 salinity unit, nitrate concentration varies by only 0.25 lM and nitrite varies by less than 0.03 lM. Ammonium and phosphate have a common behaviour that is distinctly different from that of nitrite and nitrate. The plot of the two chemical variables against salinity (Fig. 5.9) shows that both vary independently from salinity. Away from the effluent station, relatively low concentrations are maintained, while ammonium shows greater dispersion. This may arise from the regular and simultaneous autotrophic consumption of the two nutrients. Ammonium, the ﬁrst product of the mineralization of organic nitrogen (Chester and Jickells 2012), is known to be readily consumed in open

Fig. 5.7 Correlation of salinity with NO2 in autumn along the coastal waters of Jeddah

R. Al-Farawati et al.

Fig. 5.8 Correlation of salinity with NO2 and NO3 in spring along the coastal waters of Jeddah

seawater. Nitrogen is the only nutritive element present at different oxidation states. It is known that nitrogen in ammonium (oxidation state = -3) is preferentially used by the algae due to its low energetic cost (Aminot and Kérouel 2004). The good agreement between ammonium and phosphate (Fig. 5.10) supports their common fate. Variation of the concentration of TIN is automatically accompanied by a modiﬁcation of the ratios of the different nitrogen components to TIN (Table 5.2). Nitrite does not vary signiﬁcantly; its contribution is limited to 2%. Meanwhile, ammonium and nitrate replace one another on the scale of the importance of their contribution to the total inorganic nitrogen pool. Ammonium is the major constituent in autumn, representing about 60% of the TIN, while in spring nitrate becomes the principal component, having approximately 62% of the TIN. Nitrate is the major and dominant ﬁxed nitrogen component in an oxidizing aquatic environment (Valiela 2005); other components, such as ammonium, are unstable or readily consumed. However, in coastal waters the situation is totally different. Contributions from land based sources,

5

Nitrogen, Phosphorus and Organic Carbon …

97

Fig. 5.10 Correlation of NH4 with PO4 in spring along the coastal waters of Jeddah

Fig. 5.9 Correlation of salinity with NH4 and PO4 in spring along the coastal waters of Jeddah

particularly sewage effluents, largely contribute to the disturbance of this order. This may arise from the direct input of ammonium nitrogen from the effluents. Results show that, in the surface waters close to sewage discharge point, ammonium contributes between 54 and 96% of the TIN (Table 5.2). Analyses of the effluent water (El Sayed 2002a) have shown that ammonium represents 93% of the TIN and that the effluent carries 1763 kg day−1 of ammonium Table 5.2 Average percentage of NO2−, NO3−, and NH4+ and average of N/P in autumn and spring in the coastal waters of Jeddah

Nitrogen component

nitrogen. The increase of the ammonium nitrogen contribution to the TIN pool may also result from the enhanced production of organic matter; its degradation may alter the environmental conditions (e.g., dissolved oxygen and pH) resulting in the accumulation of ammonium (NH4+ + NH3). Mineralization of organic matter is carried out by heterotrophic bacteria that use the organic substrate partly for energetic demand and partly for the synthesis of new organic matter (Martin and Meybeck 1979). At the same time, heterotrophic bacteria will assimilate the mineralized nitrogen and phosphorus to constitute a biomass of the average composition C45N8P (Goldman et al. 1987; Fenchel et al. 2012). Therefore, only the excess mineralized nitrogen is liberated as ammonium in the environment. The production of ammonium from the mineralization of the organic matter will depend on the nature of the substrate and the assimilation coefﬁcient of the heterotrophic bacteria community (Aminot and Kérouel 2004). Ammonium may also be produced through nitrate denitriﬁcation; however, dissolved oxygen data indicate that surface waters as well as waters up to 10 m depth are almost saturated with dissolved oxygen.

Autumn Average excluding value at sewage discharge point

Spring Average at sewage discharge point

Average excluding value at sewage discharge point

Average at sewage discharge point

NO2−

2

0.5

2

1

NO3−

38

3.5

62

45

NH4+

60

96

36

54

N/P

25

9

7

4

98

N/P Ratio and the Limiting Nutrient For their growth, the phytoplankton population consumes nutrient elements and progressively lowers their concentrations to the level where it becomes difﬁcult for the cells to ﬁnd their needs and their growth is slowed down. In this sense, nutrients are the limiting factor to the algal production. In turbid coastal water, light could be the limiting factor for planktonic production. The exhaustion of nitrogen or phosphorus stops the development of phytoplankton while the exhaustion of silicate stops the development of diatoms. The notion of limitation should be seen as depending on the nature of the nutrient element and the planktonic species. The determination of the limiting nutrient in coastal waters receiving sewage dumping is of great economic and ecological importance. Determination of whether phosphorus or nitrogen is the limiting element for the algal production would represent valuable information because it will determine the type of sewage treatment; the limiting element would be the one that must be eliminated during the treatment process. This will result in the reduction of the treatment cost and its ecological impact would be the reduction of excessive algal production that may damage the ecosystem and may also have adverse economic and touristic consequences. Both nitrogen and phosphorus have been shown to limit phytoplankton productivity in different marine environments. Phosphorus limits production in the Bay de Seine at the mouth of the Seine River and nitrogen become limiting in the open water (Videau 1995; Cugier 1999). The western basin of the Mediterranean Sea may be nitrate-limited (Owen et al. 1989), while parts of the eastern basin may be phosphate limited (Krom et al. 1991). Falkowski (1997) and Codispoti (1997) suggested that nitrogen is the limiting nutrient for primary production on a geological time scale. On the other hand, Tyrrell (1999) and Toggweiler (1999) considered that, in the long term, phosphorus must be the nutrient controlling phytoplankton productivity because the N/P ratio could principally be adjusted to phytoplankton demands by nitrogen ﬁxation. There is an extensive list of publications in which nutrient concentrations together with their molar ratios have been used to infer nutrient limitation as well as changes in the phytoplankton community assemblage (Krom et al. 1991; Dortch and Whitledge 1992; Justić et al. 1995; Béthoux et al. 2002; Moutin and Raimbault 2002; Nedwell et al. 2002; Wang et al. 2003; Dafner et al. 2003; Lane et al. 2004; Li et al. 2013; Mohamed and Amil 2015; Yadav et al. 2016; Zhou et al. 2017). The established N/P atomic ratio of the phytoplankton biomass is 16/1 (Redﬁeld et al. 1963). The comparison of this ratio with that measured in ambient water has usually

R. Al-Farawati et al.

been used to detect the limiting element. Deviations from this molar ratio have been used to infer which of the nutrient elements could be potentially limiting (Howarth 1988). An N/P ratio higher than 16/1 indicates an excess of nitrogen which means that phosphorus is the limiting element; a ratio lower than 16/1 indicates nitrogen limitation (Aminot and Kérouel 2004). Intensive surveys in the southern Red Sea yielded an N/P ratio of 20, which is higher than normal (Grasshoff 1969; Morcos 1970). According to the results of these studies, nitrogen is the limiting nutritive element in the Red Sea. This high N/P ratio was ascribed to nitrogen ﬁxation. In a more recent study, Hase et al. (2006) gave lower N/P ratios in the northern Red Sea and the Gulf of Aqaba (13:1 and 11:3 respectively) and concluded that nitrogen is the proximate and phosphorus is the ultimate limiting nutrient. In Jeddah coastal waters, N/P molar ratios varied widely in space and time. In autumn, off the effluent discharge point the ratio averaged 25 (Table 5.2). During spring, the N/P ratio is distinctly lower than that of autumn and has an average of 7 (Table 5.2). At the effluent station, the same trend is observed; the ratio is higher in autumn (9) and lower in spring (4) (Table 5.2). Evidently, these ratios are far from the widely-accepted values measured in open seawater. The explanation is that the ratio of Redﬁeld (1934) is the product of the mineralization of the phytoplankton biomass without any impact from any land sources that may directly introduce nitrogen and phosphorus in different proportions or may introduce organic matter of composition different from that of the natural algal biomass. Moreover, a series of processes, such as adsorption-desorption or nitriﬁcation-denitriﬁcation, which are particularly active in coastal waters, may interfere to modify drastically the N/P molar ratio. Previous studies on the chemical composition of effluent water have shown that the N/P ratio averaged about 16 (El Sayed 2002a); however, the same ratio in the dilution basin of the effluent averaged 3. This dramatic lowering of the ratio was attributed to the behaviour of the individual components of the inorganic nitrogen and phosphorus. El Sayed (2002a) showed that the inorganic nitrogen suffered an important loss that was ascribed to consumption and probably to denitriﬁcation at the sediment surface, while phosphorus was added to the water as a result of desorption from sediments and particulate matter. The same process was stated by Hase et al. (2006) as being responsible for the lower N/P ratios in the northern Red Sea compared to the Gulf of Aqaba. If, under these conditions, we accept the use of the N/P molar ratio as an indicator of the limiting nutrient in the area of study, it appears that phosphorus deﬁciency suggests phosphorus limitation in autumn while nitrogen deﬁciency in spring suggests nitrogen limitation.

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Nitrogen, Phosphorus and Organic Carbon …

Another method to identify the limiting element is the plot of phosphorus versus nitrogen; the element which is exhausted ﬁrst is taken to be the limiting one. The plot of the data of autumn and spring is not convincing and points are very scattered; however, when we introduce into the data sets the measurements in the vicinity of the effluent discharge point, we observe, at zero phosphorus concentration, an excess of TIN of 0.43 and 0.68 lM in autumn and spring respectively (Fig. 5.11). This does not fully agree with the previous estimate based on the N/P ratio. The use of the N/P ratio and the graphic representation appear to have some limitations in their use for detecting the limiting element. A more recent approach was proposed by Neill (2005) to detect which nutrient is limiting for plant growth in estuarine water at any salinity. The method is based on the N/P ratio in water and utilizes overlaid graphs for nutrient versus salinity. Graphs are prepared for (i) TIN versus salinity and (ii) phosphate versus salinity, with the scales for TIN and phosphate on the vertical axes set at a ratio of N:P = 16:1. When these graphs are overlaid, then the lowermost trend line denotes the limiting nutrient for plant growth at any salinity. Furthermore, if there is a transition from P to N limitation somewhere along the salinity gradient then this occurs at the salinity where the trend lines intersect. Application of this method to our results (Fig. 5.12) reveals that nitrogen is the limiting element in the coastal water of Jeddah. However, since it has been shown that the behaviour of TIN and reactive phosphate are not conservative, the applicability of the method in this case becomes very problematic. It is evident that the determination of the limiting nutrient is not very easy and should be treated with great caution. Our study has shown that the limiting element may vary in time and space and that it might be linked to the species

99

Fig. 5.12 Correlation of salinity with TIN and PO4 in autumn and spring along the coastal waters of Jeddah

composition of the phytoplankton population. This ecological aspect deserves a particular programme extending at least over a whole year with monthly sample collection in the three oceanographic disciplines, chemistry, biology and physics.

Pollution Load from Land-Based Sources

Fig. 5.11 Correlation of TIN with PO4 in autumn and spring along the coastal waters of Jeddah

The load of various organic and inorganic pollutants from point and non-point sources has to be evaluated to understand their fate and impact on marine organisms and humans at the end of the food chain. Excessive input of nitrogen and phosphorus and their consequent uptake by marine phytoplankton may cause the production of great quantities of algal biomass. Under extreme conditions this process evolves to eutrophication, hypoxia and anoxia (Gray et al. 2002). Pollution load can directly be obtained using the hydraulic flow and the average concentration of pollutant in the effluent. In case the average concentration in the effluent is unknown, then indirect determination can be undertaken using the projection of the concentration of the potential

100 Table 5.3 Daily pollution load (Kg) of nitrogen, phosphorus and carbon in Jeddah coastal waters, Al-Arbaeen and Reayat Al-Shabab Lagoons

R. Al-Farawati et al. Period

TIN

TN

PO4–P

TP

DOC

Jeddah coastal waters

2002

5709 (33.2%)

17220

819 (35.2%)

2334

–

Al-Arbaeen Lagoon

2009

2106

–

177

–

1920

2010

1167 (43.0%)

2711

89 (59.7%)

149

–

2009

638

–

112

–

1440

2010

697 (52.4%)

1330

50 (44.6%)

112

–

21261

1033

2595

3360

Average Reayat Al-Shabab Lagoon

1636

Average

668

Total

8013

133

81

Values in brackets represent percentage of inorganic forms of nitrogen and phosphorus

pollutant against salinity. Then it is possible to calculate the concentration at zero salinity as the pollutant value in the effluent. This type of estimation is applied when the behaviour of the considered element or component is conservative. Estimation of the pollution load in the Southern Corniche area can be directly reached using data obtained from the Al-Kumra STP, where the average concentrations of total phosphorus and total nitrogen are 251 and 1359 uM, respectively. These values correspond to 2334 and 17220 kg day−1 of total phosphorus and nitrogen, respectively (Table 5.3). The magnitude of the daily fluxes of TIN and PO4 account for 35.2 and 33.2% of the total nitrogen and phosphorus fluxes, respectively. Data on the composition and concentrations of nitrogen and phosphorus in sewage effluents of the other two major STPs that discharge to the Al-Arbaeen and Reayat Al-Shabab Lagoons are scarce. Therefore, indirect estimations based on the projection of salinity against nitrogen and phosphorus are suitable tools to evaluate the flux. Data for the two lagoons is available for dissolved components of nitrogen and phosphorus in 2009 and 2010. The relationship of salinity to both nitrogen and phosphorus is almost linear, indicating a conservative behaviour during their residence in the lagoons. Concentrations obtained by extrapolation at zero salinity are given in Table 5.3. The flux of TIN from the Al-Arbaeen Lagoon in 2009 (2106 kg day−1) is almost double its flux in 2010 (1167 kg day−1), whereas the flux values in 2009 and 2010 are nearly identical for the Reayat Al-Shabab Lagoon (Table 5.3). In general, the flux of nitrogen and phosphorus into the Al-Arbaeen Lagoon is higher than their flux to the Reayat Al-Shabab Lagoon; this in agreement with the magnitude of the hydraulic flow of sewage effluent into the two lagoons. The cumulative input of nitrogen and phosphorus into the coastal waters of Jeddah from the three major STPs is approximately 21000 and

3400 kg day−1. Signiﬁcant quantities of nitrogen and phosphorus are dumped into Jeddah coastal water which might have a signiﬁcant impact on marine life. A nutrient indicator algae (NIA) is the fleshy seaweed that was evaluated by the Regional Organization for the Conservation of the Environment of the Red Sea and Gulf of Aden (PERSGA) to measure the impact of nutrient discharge on the coral reefs of the Red Sea due to urban activities. The average value of NIA in the coral reefs has shown a pronounced increase from 4.8 to 7.4% between 2002 and 2008 (PERSGA 2010). Apparently, there has been a progressive increase in the concentration of nutrients in the coastal waters of Jeddah in the last few decades which may deteriorate the coral reef environment.

Potential Production of Organic Matter In coastal waters, organic matter (OM) may have different sources. One is the in situ biological production of organic matter (Kaiser et al. 2017) and the second is the organic matter directly introduced via different types of discharges such as rivers and streams, land based sources, particularly sewage effluents (Alonso-Hernández et al. 2017), and atmospheric transport (Mai-Thi et al. 2017). Another source of organic matter may come from the assimilation of the nutrient elements present in the effluents by the primary producers. Since the assimilation is more or less achieved depending on a variety of environmental variables, this organic matter is named potential organic matter (POM). OM is a master environmental variable; the transfer of the marine environment from oxic to suboxic and ﬁnally to anoxic conditions depends entirely on the amount of organic matter and the mixing of the water column. In this term, high quantities of organic matter and limited water circulation promote the development of suboxic and anoxic conditions

5

Nitrogen, Phosphorus and Organic Carbon …

101

(Chester and Jickells 2012). Based on the data of phosphorus, water transparency and algal biomass, inferred from chlorophyll data, and using the trophic state index (TSI) (Carlson 1977; Carlson and Simpson 1996), the Reayat Al-Shabab and Al-Arbaeen Lagoons can be classiﬁed as hypereutrophic lagoons (El Sayed et al. 2015). The atomic carbon: nitrogen: phosphorus ratio in marine phytoplankton is close to 106:16:1 (Redﬁeld 1934, 1958). Therefore, depending on this ratio and having the concentration of dissolved inorganic nitrogen and phosphorus, we are able to estimate the mass of organic carbon that may be produced upon the entire assimilation of the two elements, and as organic carbon represents about 50% of the weight of organic matter (Aminot and Kérouel 2004; Libes 2009), the weight of the POM becomes available. Based on that, the consumption of 1 g of dissolved inorganic nitrogen produces 11.4 g of algal organic matter and 1 g of phosphorus produces 82 g of algal organic matter. Based on concentrations measured in the Al-Khumra effluent, assimilation of dissolved phosphorus and TIN would generate 67.2 ton day−1 or 65.7 ton day−1 of organic matter, depending on which is the limiting element. The agreement with the calculated quantity of organic matter, produced by the utilization of inorganic forms of phosphorus, is expected since their ratio in the effluent from the Al-Kumra STP is 16:1. Under phosphorus limitation, the complete algal consumption of the phosphate load will generate each day about 4 and 7 tons of organic matter in the Reayat Al-Shabab and Al-Arbaeen Lagoons, respectively. If nitrogen were considered the limiting nutrient element, the potential organic matter that may be generated each day by the complete consumption of the TIN load is about 8 tons in Reayat Al-Shabab and 13 tons in Al-Arbaeen Lagoon.

phosphorus budgets which was estimated to be 64 109 mol year−1 for nitrogen and 0.4 109 mol year−1 for phosphorus (Béthoux 1988). Using the daily load of TN (21261 kg) and TP (3360 kg), the annual contribution from the coastal waters of Jeddah would represent about 0.9 and 9.9% of the nitrogen and phosphorus deﬁciency, respectively.

Budget of Nitrogen and Phosphorus in the Red Sea: Contribution of the Coastal Waters of Jeddah

References

Subsurface inflow of nutrient-rich waters from the Indian Ocean through the Gulf of Aden is the major source of nitrogen and phosphorus to the oligotrophic waters of the Red Sea (Morcos 1970). On the other hand, the Red Sea loses nitrogen and phosphorus due to deep water outflow to the Gulf of Aden (Grasshoff 1969; Naqvi et al. 1986; Béthoux 1988). It was argued that the outflow of nitrogen and phosphorus from the Red Sea is balanced by the inflow of subsurface water from the Gulf of Aden (Poisson et al. 1984; Papaud and Poisson 1986). However, investigations by other workers have shown that the concentrations of nutrients in the out flowing bottom water are higher than their concentrations in the inflowing water (Grasshoff 1969; Morcos 1970). This leads to an imbalance and deﬁciency in nitrogen and

Conclusions The current work utilized data collected along the Jeddah coastal area between 1998 and 2010 in order to investigate the behaviour and distribution of carbon, nitrogen and phosphorus, their flux from anthropogenic sources and their contribution to the total budget of nitrogen and phosphorus in the Red Sea. The spatial distribution reveals hot spots in the vicinity of sewage discharge points as indicated by lower salinity and negative correlation of salinity with carbon, nitrogen and phosphorus. The temporal distribution of DOC and POC indicates higher values in spring that can be attributed to higher activities of marine phytoplankton. Ammonium constitutes the majority of TIN in autumn while nitrate is the principal form of inorganic nitrogen in spring. Nitrogen is likely the potential limiting element as inferred using various techniques. Flux calculations indicate that the coastal waters of Jeddah contribute signiﬁcant fractions of nitrogen and phosphorus to the annual deﬁciency of the budgets of the two elements. Acknowledgements The authors would like to thank the Deanship of Scientiﬁc Research, King Abdulaziz University for ﬁnancial support through many projects which has allowed us to present the current work. The authors also greatly appreciate considerable logistical support from the Saudi Geological Survey.

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Goldman JC, Caron DA, Dennett MR (1987) Regulation of gross growth efﬁciency and ammonium regeneration in bacteria by substrate C: N ratio. Limnol Oceanogr 32:1239–1252. https://doi. org/10.4319/lo.1987.32.6.1239 Grasshoff K (1969) Chemical observations in the Red Sea and the inner Gulf of Aden during the International Indian Ocean Expedition 1964/65. Suppl. to Grasshoff K, Zur Chemie des Roten Meeres und des Inneren Golfs von Aden nach Beobachtungen von F.S. “Meteor” während der Indischen Ozean Expedition 1964/65. Meteor Forschungsergebnisse, Dtsch. Forschungsgemeinschaft, Deutsche Forschungsgemeinschaft, Reihe A Allgemeines, Physik und Chemie des Meeres, Gebrüder Bornträger, Berlin, Stuttgart, A6, pp 1–76. https://doi.org/10.1594/pangaea.603890 Gray JS, Wu RS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment. Mar Ecol Prog Ser 238:249–279 Hansell DA, Carlson CA (1998) Net community production of dissolved organic carbon. Global Biogeochem Cycles 12:443– 453. https://doi.org/10.1029/98GB01928 Hansell DA, Carlson CA, Amon RMW (2002) Biogeochemistry of marine dissolved organic matter. Academic Press, New York Harrison WG (1992) Regeneration of nutrients. In: Falkowski PG, Woodhead AD, Vivirito K (eds) Primary productivity and biogeochemical cycles in the sea. Springer, US, Boston, MA, pp 385–407 Hase C, Al-Qutob M, Dubinsky Z, Ibrahim EA, Lazar B, Stambler N, Tilzer MM (2006) A system in balance?—implications of deep vertical mixing for the nitrogen budget in the northern Red Sea, including the Gulf of Aqaba (Eilat). Biogeosci Discuss 3:383–408 Hinrichsen D (1998) Coastal waters of the world: Trends, threats, and strategies. Island Press, Washington, DC, p 275 Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Ann Rev Ecol Syst 19:89–110. https://doi.org/ 10.1146/annurev.es.19.110188.000513 Justić D, Rabalais NN, Turner RE, Dortch Q (1995) Changes in nutrient structure of river-dominated coastal waters: Stoichiometric nutrient balance and its consequences. Estuar Coast Shelf Sci 40:339–356. https://doi.org/10.1016/S0272-7714(05)80014-9 Kaiser D, Konovalov S, Schulz-Bull DE, Waniek JJ (2017) Organic matter along longitudinal and vertical gradients in the Black Sea. Deep Res Part I Oceanogr Res Pap. https://doi.org/10.1016/j.dsr. 2017.09.006 Karbe L, Lange J (1981) The chemical environment. In: Karbe L, Theil H, Weikert H, Mill AJB (eds) Mining metalliferous sediments from the Atlantic II Deep, Red Sea: pre-mining environmental conditions and evaluation of the risk to the environment. Environmental impact study presented to Saudi-Sudanese Red Sea Joint Commission, Hamburg, pp 75–99 Karsh KL, Trull TW, Sigman DM, Thompson PA, Granger J (2014) The contributions of nitrate uptake and efflux to isotope fractionation during algal nitrate assimilation. Geochim Cosmochim Acta 132:391–412. https://doi.org/10.1016/j.gca.2013.09.030 Kaul LW, Froelich PN (1984) Modeling estuarine nutrient geochemistry in a simple system. Geochim Cosmochim Acta 48:1417–1433. https://doi.org/10.1016/0016-7037(84)90399-5 Krom MD, Kress N, Brenner S, Gordon LI (1991) Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol Oceanogr 36:424–432. https://doi.org/10.4319/lo.1991.36. 3.0424 Lane RR, Day JW, Justic D, Reyes E, Marx B, Day JN, Hyﬁeld E (2004) Changes in stoichiometric Si, N and P ratios of Mississippi River water diverted through coastal wetlands to the Gulf of Mexico. Estuar Coast Shelf Sci 60:1–10. https://doi.org/10.1016/j. ecss.2003.11.015 Li R, Liu S, Zhang G, Ren J (2013) Biogeochemistry of nutrients in an estuary affected by human activities: the Wanquan River estuary,

103 eastern Hainan Island, China. Cont Shelf Res 57:18–31. https://doi. org/10.1016/j.csr.2012.02.013 Libes SM (2009) Introduction to marine biogeochemistry, 2nd edn. Academic Press, Amsterdam, p 928 Maciejewska A, Pempkowiak J (2014) DOC and POC in the water column of the southern Baltic. Part I. Evaluation of factors influencing sources, distribution and concentration dynamics of organic matter. Oceanologia 56(3):523–548. https://doi.org/10. 5697/oc.55-3.523 Maciejewska A, Pempkowiak J (2015) DOC and POC in the southern Baltic Sea. Part II—Evaluation of factors affecting organic matter concentrations using multivariate statistical methods. Oceanologia 57:168–176. https://doi.org/10.1016/j.oceano.2014.11.003 Mai-Thi N-N, St-Onge G, Tremblay L (2017) Contrasting fates of organic matter in locations having different organic matter inputs and bottom water O2 concentrations. Estuar Coast Shelf Sci 198:63–72. https://doi.org/10.1016/j.ecss.2017.08.044 Mantoura RFC, Woodward EMS (1983) Conservative behaviour of riverine dissolved organic carbon in the Severn Estuary: Chemical and geochemical implications. Geochim Cosmochim Acta 47:1293–1309. https://doi.org/10.1016/0016-7037(83)90069-8 Markogianni V, Varkitzi I, Pagou K, Dimitriou E (2017) Nutrient flows and related impacts between a Mediterranean river and the associated coastal area. Cont Shelf Res 134:1–14. https://doi.org/ 10.1016/j.csr.2016.12.014 Martin J-M, Meybeck M (1979) Elemental mass-balance of material carried by major world rivers. Mar Chem 7:173–206. https://doi. org/10.1016/0304-4203(79)90039-2 Mohamed KN, Amil R (2015) Nutrients enrichment experiment on seawater samples at Pulau Perhentian, Terengganu. Procedia Environ Sci 30:262–267. https://doi.org/10.1016/j.proenv.2015.10. 047 Morcos SA (1970) Physical and chemical oceanography of the Red Sea. Oceanogr Mar Biol Ann Rev 8:73–202 Moutin T, Raimbault P (2002) Primary production, carbon export and nutrients availability in western and eastern Mediterranean Sea in early summer 1996 (MINOS cruise). J Mar Syst 33:273–288. https://doi.org/10.1016/S0924-7963(02)00062-3 Naqvi SWA, Hansen HP, Kureishy TW (1986) Nutrient uptake and regeneration ratios in the Red Sea with reference to the nutrient budgets. Oceanol Acta 9:271–275 Nedwell DB, Dong LF, Sage A, Underwood GJC (2002) Variations of the nutrients loads to the mainland U.K. estuaries: Correlation with catchment areas, urbanization and coastal eutrophication. Estuar Coast Shelf Sci 54:951–970. https://doi.org/10.1006/ecss.2001. 0867 Neill M (2005) A method to determine which nutrient is limiting for plant growth in estuarine waters—at any salinity. Mar Pollut Bull 50:945–955. https://doi.org/10.1016/j.marpolbul.2005.04.002 Owen NJP, Rees AP, Woodward EMS, Mantoura RFC (1989) Owens, 1989 size-fractionated primary production and nitrogen assimilation in the northwest Mediterranean Sea during January 1989. Water Pollut Res Bull 13:126–135 Papaud A, Poisson A (1986) Distribution of dissolved CO2 in the Red Sea and correlations with other geochemical tracers. J Mar Res 44:385–402. https://doi.org/10.1357/002224086788405347 Pernetta JC, Milliman JD (1995) Land-ocean interactions in the coastal zone: implementation plan. International Geosphere-Biosphere Programme: A Study of Global Change of the International Council of Scientiﬁc Unions (ICSU), Stockholm, 215 pp PERSGA (2010) The status of coral reefs in the Red Sea and Gulf of Aden: 2009. PERSGA Technical Series Number 16, PERSGA, Jeddah, 105 pp Poisson A, Morcos S, Souvermezoglou E, Papaud A, Ivanoff A (1984) Some aspects of biogeochemical cycles in the Red Sea with special

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Automatic Detection of Coral Reef Induced Turbulent Boundary Flow in the Red Sea from Flock-1 Satellite Data Maged Marghany and Mohamed Hakami

Abstract

The novelty of this study is the use of a multi-objective evolutionary algorithm for the automatic detection of hydrodynamic turbulent boundaries overlying coral reefs. The procedure is implemented using sequences of Flock-1 satellite data acquired in the Red Sea. The study demonstrates that implementing Pareto-optimal solutions allows for the generation of accurate coral reef-water interface patterns. This is validated by a Pareto-optimal front and the receiver-operating characteristic (ROC) curve. The Pareto-optimal front indicates a signiﬁcant relationship between hydrodynamic turbulent boundaries, macroalgae, and coral reefs. The ROC curves conﬁrm the ﬁnding of the Pareto-optimal front that hydrodynamic turbulent boundary layers and macroalgae are caused by coral reefs. The performance accuracy is identiﬁed with an under-curve area of 90%. In conclusion, the multi-objective evolutionary algorithm has the applicability for the automatic detection of hydrodynamic turbulent boundary layers to coral reef studies.

Introduction Until now, no study has implemented Flock-1 satellite data in oceanography applications (Marghany 2015). The Flock-1 satellite was launched on 9 January 2014, and the data holds great promise for a wide variety of Earth observations because of its high spatial and temporal resolutions (Boshuizen et al. 2014). Consequently, this study is the extension of the ﬁrst work of Marghany (2015) to utilize Flock-1 data for turbulent hydrodynamic detection overlying coral reefs. M. Marghany (&) School of Humanities, Geography Section, University Sains Malaysia (USM), 11800 USM Penang, Malaysia e-mail: [email protected] M. Hakami Remote Sensing Department, Saudi Geological Survey, Jeddah, Saudi Arabia

Turbulent boundary flow requires a short revisit satellite cycle and high-resolution data to provide precise information regarding turbulent hydrodynamic flow that is important for ship navigation, ﬁshing, pollution and sediment transport (Meshal et al. 1984; Stocking et al. 2016). Remote sensing techniques are powerful tools for ocean feature mapping and monitoring (Goodman et al. 2013; Hedley et al. 2016). The measurement of the ocean from space is a function of the electromagnetic signal reflected from the sea that carries information on the primary observable quantities, including the colour, the radiant temperature, the roughness, and the height of the sea. Visible waveband radiometers of 399 nm–740 nm depend on reflected sunlight at approximately 57°–90°, which is a function of the local time of day. The thermal fluctuations of the sea surface are measured in the thermal infrared and microwave parts of the radiation spectrum. Hence infrared and microwave radiometers are used to measure the radiation temperature of the sea surface, and the emissivity is used to approximate the physical temperature of the ocean (Bruckner et al. 2012). Therefore, there is the possibility for this effect to be used in the discrimination of types of reef bottom; (1) the characteristic 570 nm feature in reflectance of brown hermatypic coral is at the cusp of increasing attenuation, and (2) the attenuation feature tends to produce a strong shoulder in reflectance in this wavelength region for all water transparencies and all bottom structures. Clouds are the most challenging aspect of visible and infrared remote sensing (Corbane et al. 2008), by partially hiding pixel information and corrupting a dataset with false values, thus introducing a bias. As a result, passive sensors are based on the visible wave band, and multispectral imaging spectrometer scanners are predominantly used (Hedley et al. 2016) to investigate ocean colour, chlorophyll suspended particulates and bathymetry. Infrared sensors are used principally for sea surface temperature (SST), while passive microwave sensors such as scanning microwave radiometers are used to determine sea surface salinity, sea roughness, internal waves, surface winds, and surface slicks.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_6

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Infrared radiometers measure the skin SST, whereas microwave radiometers, penetrating deeper, measure sub-skin SST. Nevertheless, the study of ocean turbulence is still at an early stage, and ocean turbulence studies are lost in other studies, for instance geostrophic currents, wave-current interactions, or sea surface temperature fluctuations (Rowlands et al. 2008). In the words of Stocking et al. (2016), turbulent flow is a kind of fluid flow in which the fluid experiences asymmetrical instabilities, or mixing. In turbulent flow, the fluid’s velocity at a point is continuously experiencing fluctuations in both magnitude and direction. In shallow waters, the coral reef cover induces a turbulent flow, since the permanent coral boundary interrelates through friction with the superimposed water column. Under these conditions, a layer of shear flow is formed that then creates a turbulent wall or boundary layer, and the hydrodynamics of the turbulent bottom boundary layer next to the coral surface governs the vertical transport of mass between the coral surface and the water column (Reidenbach et al. 2007; Stocking et al. 2016). The presence of an algal canopy increases turbulent kinetic energy within the roughness sublayer by *2.5 times in contrast with healthy corals while simultaneously decreasing bottom shear stress by an order of magnitude (Stocking et al. 2016). The turbulent hydrodynamics of coral reefs and algal flow are well understood (Reidenbach et al. 2007; Marghany 2015; Stocking et al. 2016) and have wide applicability. Previous studies in the Red Sea concerned coral reef mapping and monitoring using in situ measurements and remote sensing technologies (Benayahu and Loya 1981; Bailey et al. 2007; Benﬁeld et al. 2007; Bruckner et al. 2012). However, there is no study using integration of in situ measurements and remote sensing technology to explain how turbulent boundary flow can be generated by coral reefs. In addition, studies of Red Sea physical oceanography parameters must be instigated to investigate the turbulent boundary flow overlying coral reefs. In fact, variations in water column temperature, salinity and density as function of wind and tidal cycles can induce turbulent boundary flow. The geomorphology of the sea bed which involves, for instance, varieties of coral reef can modulate and enhance the pattern of turbulent boundary flow due to friction. In these regards, the following sections explain the generation of turbulent boundary flow along the Red Sea.

M. Marghany and M. Hakami

Perim Island (12°39′24″N, 43°24′54″E) is approximately 300 m deep (Rasul et al. 2015). The Red Sea has a length of 1930 km and a mean width of 270 km between l2°N and 28°N, with a long and narrow trench and is surrounded by mountains and deserts (Rushdi 2015). In particular, north of 28°N, the basin is bordered by the shallow Gulf of Suez to the north-west and the deep Gulf of Aqaba on the north-east (Fig. 6.1). The water depth varies throughout the Red Sea; the shallow continental shelf is less than 50 m deep in the south, and the deepest water is in the central trough, the width of which is roughly 50 km with a maximum depth of about 2700 m (Werner and Lange 1975). An interesting geological feature is the shallow sill of 137 m depth which is located in the north of the Hanish Archipelago at 13°44′N. The Red Sea rift has a different morphology compared to other mid-ocean ridges because of the presence and movement of giant submarine salt flows, which blanket large portions of the rift valley and thereby the oceanic crust (Augustin et al. 2016). Furthermore, the Red Sea involves large-scale geomorphological structures, including a deep rift valley, steep faults, highly tectonized terrain, rifted volcanoes, bent volcanic ridges with overlapping spreading centres and second order non-transform offsets that are typical for slow- and ultraslow spreading ridges. North of about 19.5N, oceanic crust occurs in wide isolated

Red Sea Topography and Sea Floor Geomorphology The Red Sea is an irregular semi closed basin connected through the narrow Strait of Bab al Mandab with the Gulf of Aden and the Indian Ocean, where the channel west of

Fig. 6.1 Red Sea topography

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Automatic Detection of Coral Reef Induced Turbulent Boundary …

bathymetric troughs and basins, the so-called “Deeps”, which are separated by shallower ‘Inter-Trough Zones’ where salt flows blanket the axial valley. Several seafloor depressions along the axis of the Red Sea contain highly saline brine pools which vary in temperature from about 22 ° C (Swallow and Crease 1965), and the brine-ﬁlled Deeps are associated with metalliferous sediments and hydrothermal settings (Gurvich 2006).

Turbulent Boundary Flow in the Red Sea The Red Sea dynamic turbulent boundary flow is a function of the monsoon wind regimes, and density-gradient currents due to low precipitation and high evaporation. The Red Sea is surrounded by arid areas, and is one of the saltiest of the world’s oceans. Thus, the deep waters are dominated by extremely salty water masses (Meshal et al. 1984; Meshal and Morcos 1984). In winter, the southern sea surface temperature is cooler than the northern one with 25 °C (Fig. 6.2a). In summer, conversely, the sea surface temperature increases from the north to the south, and the southern

Fig. 6.2 Wind effects on coastal circulation, salinity and temperature during a winter and b summer

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Red Sea has the highest sea surface temperature of 31.72 °C (Fig. 6.2b) (Sheppard et al. 1992). The subsurface at 200 m has a cool temperature of 22 °C, and the temperature then decreases below 300 m depth to 21.62 °C (Rushdi 2015). However, the sea surface salinity increases from south to north, and in the north the salinity is 40.20 ppt. The salinity increases more rapidly with water depth in the south as compared to the north. Below 200 m, the salinities range from 40.57 to 40.59 ppt (Fig. 6.2). Overall, the average Red Sea temperature and salinity are 22 °C and 40 ppt, respectively (Meshal et al. 1984; Meshal and Morcos 1984; Sheppard et al. 1992; Rushdi 2015). The wind monsoon pattern, density-gradient and mixing processes affect the distributions of temperature and salinity along the Red Sea (Morcos 1970; Sheppard et al. 1992). The north-westerly winds drive the surface water layer at C30 present as the typically mature C-22 S/R pairs (homohopanes; Simoneit 1984; Simoneit et al. 1990). Petroleum and vehicle engine exhaust commonly show higher concentration distributions of the 22S hopane relative to the corresponding 22R epimer (Simoneit 1984, 1985). The ratios of 22S/(S+R) for C31 and C32 extended hopanes ranged from 0.41 to 0.80 (mean = 0.62 ± 0.09) and from 0.33 to 0.98 (mean 0.55 ± 0.11), respectively. The average values of these ratios are similar to those for mature crude oil and petroleum hydrocarbons (Kvenvolden et al. 1990; Rushdi and Simoneit 2002a, b). Accordingly, these

A. I. Rushdi et al.

values conﬁrm that the origins of the hopane compound series in these sediments are from petroleum residues. The presence of steranes in the environment is generally from direct emissions of petroleum and or lubricants in vehicular engines (Abas and Simoneit 1996). Other possible major sources of these biomarkers to the marine environment are municipal wastewaters, ship-washing discharges and reﬁnery activities (Laws 1993). Thus, the steranes are also valuable supporting biomarker tracers for oil-product contamination and pollution in coastal and urban environments (e.g., Albaiges and Cuberes 1980; Aboul-Kassim and Simoneit 1996; Rushdi et al. 2017). The steranes in these lagoon sediments ranged from C27 to C29 with primarily the 5a, 14b, 17b and minor 5a, 14a, 17a conﬁgurations and both occurring as 20S and 20R epimers. The sterane epimerization ratio at C-20, S/(S+R) for these samples, range from 0.34 to 0.86 (average = 0.45 ± 0.13) for C27 and from 0.07 to 0.55 (average = 0.39 ± 0.15), for C29. These ratio values indicate that the sources of these biomarkers are of petroleum origins (Simoneit 1984; Peters and Moldowan 1993).

Plasticizers The presence of plastic debris in the marine environment has been identiﬁed as a great concern to ecological and environmental health (Carpenter and Smith 1972; Colton et al. 1974; Andrady 2011; Rushdi et al. 2009, 2014; Eriksen et al. 2013; Vegter et al. 2014; Eerkes-Medrano et al. 2015; Perkins 2015). It is estimated that about 269,000 tons or 5.25 trillion plastic objects are floating in oceanic surface waters (Xanthos and Walker 2017) and they account for 60–95% of marine litter (Derraik 2002; Walker et al. 1997, 2006; Surhoff and Scholz-Bottcher 2016). Because plasticizers, which make up the bulk chemical composition of plastic products, are hazardous and very stable compounds in the environment they are considered harmful substances to marine life. In comparison, the plasticizer concentrations (4– 201 ng g−1 dw, average = 52 ± 49 ng g−1 dw) in the lagoon sediments are much lower than the concentration (36990 ± 53620 ng g−1 dw) measured in sediments from the north of the Arabian Gulf and relatively higher than the concentration (7.8 ± 0.7 ng g−1 dw) in sediments from the coast of Qatar (Rushdi et al. 2017).

Unresolved Complex Mixture (UCM) Frequently, the GC traces of solvent extractable hydrocarbon compounds of environmental samples will occasionally show the presence of the unresolved complex mixture (UCM) of branched and cyclic compounds above the

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Distribution and Sources of Hydrocarbon Compounds …

baseline with the resolved compounds superimposed (Fig. 8.2; Simoneit 1984, 1985; Killops and Al-Juboori 1990; Frysinger et al. 2003). The major sources of the UCM are fossil fuel utilization and oil spills. Usually, diesel shows a broader UCM and gasoline exhibits a narrow UCM, where both are derived from the reﬁning of crude oil (Simoneit 1984, 1985; Gough and Rowland 1990; Frysinger et al. 2003). Hydrocarbon compounds from biogenic sources such as terrestrial plants have no UCM (Simoneit and Mazurek 1982). Therefore, the ratio of UCM to resolved compounds (U:R ratio) is used to assess the contamination level from oil spills and input of petroleum related products. The concentrations of UCM and the U:R ratio values are reported in Table 8.1. The high value of the U:R ratio suggests contamination from biodegraded petroleum residues. The values of the U:R range from 0.0 to 3.5 with an average of 0.9 ± 1.05, where samples with values >1.0 are considered to be contaminated, and accordingly it is evident that the lagoon is not highly contaminated with petroleum residues. The fraction of petroleum hydrocarbon compounds (i.e., petroleum n-alkanes, hopanes, steranes and UCM) is relatively high (77.1 ± 23.1% of the total EOM) relative to other hydrocarbon compounds in the sediment samples of the lagoon. The plasticizer fraction (6.8 ± 4.6%) is relatively higher than other coastal regions (e.g., Gulf of Suez (3.3 ± 2.0%), and the Qatar coast (0.42 ± 0.72%)). The fraction of microbial hydrocarbons is higher (14.6 ± 19.2%) than the fraction from terrestrial plants (1.5 ± 2.2%). Accordingly, the main source of hydrocarbon compounds in the sediment samples from the Obhur Lagoon is of anthropogenic origins (83.9 ± 20.4%), whereas the natural source is comparatively low (16.1 ± 20.4%).

Ecological Effects The Red Sea is a nutrient poor marine ecosystem, especially in the north (Levanon-Spanier et al. 1979; Badran et al. 2005). Some productive coastal habitats along the Red Sea are very important in sustaining the renewable nutrient sources. They are known as critical habitats because they provide breeding, feeding, nursing or nesting places for marine organisms (Ray 1976; IUCN 1983; Dugan 1990). These coastal habitats include sandy beaches (nesting sites for turtles, nurseries for crustaceans), rocky shores (sites for fauna and flora), and mangrove stands (nurseries for shrimp). The coastal ecosystems including lagoons such as the Obhur Lagoon are important nutrient sources in the region (Por 2012). For example, production from benthic macroalgae is considerably greater than from both microalgae and phytoplankton (Valiela et al. 1997). Petroleum product inputs from oil reﬁneries, oil transfer docks, and municipal sewage treatment plants in the Red Sea

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region are expected to affect the marine ecosystems and associated species groups (Loya 1975; Rinkevich and Loya 1979; Dicks 1987). Direct ecological impacts of petroleum pollution on the lagoon ecosystems of the region are expected, especially on the most sensitive egg, larval, and juvenile stages of the marine species and largely benthic species that rely on lagoon ecosystems for reproduction, growth and protection. Therefore, the current effects of petroleum contamination and other marine pollution inputs to the Obhur Lagoon ecosystem will need further study. In the meantime, control and preventive efforts can and should be undertaken by industry and government to limit the input of petroleum, petroleum products, and other chemical pollutants to avoid further pollution and prevent harm to this delicate marine ecosystem.

Conclusion The EOM hydrocarbon compounds in sediments from the Obhur Lagoon of Saudi Arabia were analysed using the GC-MS method. Wax from vascular higher plants and petroleum residues are obviously the main organic chemical contents of these samples, with petroleum being the major source of hydrocarbons in most of the sediments sampled. The presence of n-alkanes with odd carbon number predominance >C25 and the n-alkanoic acids with even carbon number predominance >C20 support the source input from vascular higher plant wax, which is further supported by the strong carbon number preference indices of both homologous series >C22. The inputs from petroleum related operations or spills are obvious, as conﬁrmed by the high levels of UCM and minor amounts of the hopane and sterane biomarkers in most of the sediment samples analyzed. The anthropogenic inputs to the lagoon sediments ranged from 28 to 100% with an average of 84 ± 20% (i.e., total petroleum products ranged from 14 to 98% (average = 77 ± 23%) and plasticizers ranged from 2 to 18% (average = 16 ± 20%)). The natural or biotic inputs to the lagoon sediments ranged from 0 to 68% (average = 15 ± 2%) from microbial sources and from 0 to 11% (average = 1.5 ± 2.2%) from higher plant wax sources.

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Metal Contamination Assessment in the Sediments of the Red Sea Coast of Saudi Arabia Manikandan Karuppasamy, Mohammad Ali B. Qurban and Periyadan K. Krishnakumar

Abstract

Surﬁcial sediment samples were collected from sixty stations between 23°N and 28°N latitudes in the northern Red Sea and were analyzed for 10 metals, namely Co, Cr, Cu, Fe, Hg, Mn, Mo, Ni, V, Zn and a metalloid, As. Based on mean concentrations, the order of abundance of the metals (dry weight) was: Fe (6320.61 mg kg−1) > Mn (409.71 mg kg−1) > Zn (38.76 mg kg−1) > V (19.73 mg kg−1) > Ni (15.92 mg kg−1) > Cu (15.51 mg kg−1) > Cr (14.6 mg kg−1) > Co (6.53 mg kg−1) > As (5.21 mg kg−1) > Mo (1.06 mg kg−1) > Hg (0.03 mg kg−1). Arsenic was the only element to exhibit exceedance with 88% of the stations above upper continental crust concentrations (UCC) and 8% of the stations above threshold effect level (TEL). Sediment contamination assessment was carried out using the geoaccumulation index (Igeo) and enrichment factor (EF) and ecological hazard was assessed using the Adverse Effect Index (AEI), Potential ecological risk factor (ER) and Potential ecological index (RI). Hierarchical Cluster analysis (HAC), Principal Component Analysis (PCA) and Linear Discriminant Analysis (LDA) were used to group stations as “uncontaminated”, “minor enrichment”, “metallogenic enrichment” and “anthropogenic enrichment”.

Introduction The ultimate repositories of organic and inorganic contaminants that are found in any aquatic ecosystem are sediments. When compared with the overlying water, they act as a sink M. Karuppasamy (&) M. A. B. Qurban P. K. Krishnakumar Center for Environment and Water Research Institute, King Fahd University of Petroleum and Minerals, Dhahran, Saudi Arabia e-mail: [email protected]; ; [email protected] M. A. B. Qurban Geosciences Department, King Fahd University of Petroleum and Minerals, Dhahran, Saudi Arabia

for most contaminants and hence are more conservative and reliable when determining the concentration of contaminants spatially as well as temporally (Marchand et al. 2006; Sany et al. 2013). Due to their toxicity, ubiquitous and persistence nature, non-biodegradability and ability to bio-accumulate in food chains, metal contamination in sediments is a worldwide problem (El-Sikaily et al. 2004; Fernandes et al. 2008; Kucuksezgin et al. 2011; Yu et al. 2012). The metal-laden particulates settle and accumulate in the bottom sediments while the dissolved metal adsorbs to the ﬁne particles which eventually also settle to the bottom sediments (Singh et al. 2005). Metals from both natural and anthropogenic sources tend to accumulate in the sediments in the same manner and hence it is difﬁcult to distinguish the source solely by quantifying the concentration of a metal. In order to overcome this difﬁculty, sediment quality assessments with multiple approaches based on chemometric, ecological risk and multivariate statistical techniques are usually applied (Kharroubi et al. 2012; Varol 2011). The Red sea is unique among the seas of the world as it has no permanent streams flowing into it (Hanna 1992) and terrigenous input comes mainly through wind, occasional rains and wadis (valleys). Due to rapid industrialization and urbanization, the Red sea is environmentally affected due to anthropogenic activities such as urbanization and coastal development, industries including power and desalination plants and reﬁneries, recreation and tourism, waste water treatment facilities, coastal mining and quarrying activities, oil bunkering and habitat modiﬁcation (PERSGA 2006). Several studies have reported the concentration of metals in the surﬁcial sediments of the Red Sea (Al-Shiwaﬁ et al. 2005; Badr et al. 2009; El-Sorogy et al. 2016; El Nemr et al. 2016; Idris et al. 2007; Mansour et al. 2013; Pan et al. 2011; Usman et al. 2013). However, an exhaustive study spanning the entire Saudi Arabian waters of the northern Red Sea is lacking. The main objective of this study was to determine the degree of metal contamination using sediment contamination indices, assess potential environmental risks of these metals in the study area by comparison with sediment

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_9

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quality guidelines (SQGs), and distinguish the natural and/or anthropogenic sources of these metals and identify regional hotspots using multivariate statistical techniques.

Methodology Sampling Design The work presented here is based on the oceanic cruise conducted in the Red Sea on board the oceanographic

Fig. 9.1 Sampling stations in the Saudi Arabian waters of Red Sea

M. Karuppasamy et al.

research vessel R/V Aegeo, during November 2012 (Fig. 9.1). Surﬁcial sediment samples were collected from 60 stations between 23°N and 28°N latitudes along quasi-meridional transects spaced at 30-km intervals from the coast toward the offshore covering the territorial waters of Saudi Arabia. Samples collected using a box corer were transferred to pre-cleaned labeled acid-rinsed containers and stored at −20 °C until analyzed. Three replicate samples were collected from each station. In the laboratory, sediment samples were freeze dried, sieved through 500 µm using a nylon sieve and were homogenized using a pestle and mortar.

9

Metal Contamination Assessment in the Sediments …

They were analyzed for 13 metals, namely As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Mo, Ni, Pb, V and Zn. Stations (Fig. 9.1) were grouped into three categories, NS (stations near the coast), CA (stations near the central axis of the Red Sea), and mid (stations found between nearshore and offshore stations).

QA/QC The sample preparation, collection, storage and distribution was carried out using stringent quality assurance measures to maintain sample identity and integrity throughout the study. To prevent contamination, all the plastic vials (LDPE) and glassware were washed with 10% nitric acid solution and rinsed thoroughly with Milli-Q water and dried. All reagents were analytical grade or super pure quality. During sample collection and on-site preparation, special care was taken not to contaminate or cross-contaminate the samples and all sample collection and preparation details were documented. From each station, triplicate samples were collected and were analyzed separately. A barcode sticker was generated for each sample collected which contained the following: Date of sampling, Time of sampling, Sample matrix, Station No., Project No., Depth of sampling, Latitude and Longitude. The sticker was stuck on each sample and was scanned into a database.

Analyses of Metals The determination of total extractable metal content of the sediment was carried out following USEPA method 3050 B. Each freeze-dried sediment sample measuring 0.5 g was digested in 5 ml of ultrapure HNO3. After thorough mixing, the sample was covered with SC506 Disposable Reflux Caps. The sample was refluxed at 95° ± 5 °C for 15 min without boiling on a hot block. After cooling, 5 ml of concentrated HNO3 was added, and the sample was further refluxed for another 30 min. After cooling the sample, 2 ml of water and 3 ml of 30% H2O2 were added. Total recoverable metal concentrations of As, Cd, Cr, Cu, Fe, Hg, Mn, Ni, Pb, V, and Zn were determined in triplicate with a Perkin Elmer DV8000 Inductively Coupled Plasma Optical Emission Spectrometer (ICP-OES) following USEPA method 6010. Hg was analyzed in Cold Vapor Atomic Fluorescence (CVAF) in a Hydra AF Gold plus Hg analyzer. The quality of the instrument was assured by running Laboratory Reagent Blank (LRB), Initial Calibration Veriﬁcation (ICV) and Continuous Calibration Veriﬁcation (CCV) standards. Three reference materials were also prepared in the same way as the samples and the trace metal concentrations

149

were determined using standard solutions prepared in the same acid matrix. NIST CRM 1646 estuarine sediment, NIST CRM 2702 river sediment, and NIST CRM 2704 were used (N = 3) to ensure the validation of data and the accuracy and precision of the analytical methods. Results of triplicate analyses revealed good reproducibility of the equipment. The recoveries were 85–95% for all the metals. Moreover, sample duplicates (10%) and sample spike (5) and spike duplicates were also run over a batch of 20 samples. All reagents used were of analytical grade. Nitric and hydrochloric acid were redistilled at a Milestone DuoPur sub-boiling distillation assembly before use. The quality of the distilled acid was assessed by analyzing trace metal content of the distilled acids with Agilent 7500 ICP-MS and found to be less than 10 ng kg−1. All solutions were prepared with MilliQ water. All plastic, quartz, and glassware were soaked in HNO3 (5%) for at least 24 h and repeatedly rinsed with ultra-pure water.

Quantification of Contamination Sediment Quality Guidelines Numerical sediment quality guidelines (SQGs) are a starting point for the evaluation of biological risk caused by substances in sediments (Hübner et al. 2009). By comparing the sediment concentration with the two sets of guidelines, that is, threshold effect level (TEL) and probable effect level (PEL), the potential degree of sediment-associated adverse effects to marine organisms can be evaluated, thereby assisting in the interpretation of sediment quality (Long and MacDonald 1998). As metals occur in sediments as complex mixtures, the mean PEL quotient method (Zhuang and Gao 2014), a useful tool to reduce multiple indices to a single entity, has been applied and is calculated using the following equation: X mean PEL quotient ¼ ðCn =PELn Þ=N ð9:1Þ

where Cn is concentration of metal ‘n’ in the sediment sample, PELn is the sediment quality guideline (PEL) value of metal ‘n’ and N is the sum of all examined metals. For marine sediments, the mean PEL quotients of 2.3 indicate that the combined effects of contaminants have an 8%, 21%, 49% and 73% probability of being biologically toxic, respectively (Long et al. 1995). In addition, concentrations of metals were also compared with

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Table 9.1 Enrichment factor (EF) and Igeo classes in relation to sediment quality EF classes

Sediment quality

Igeo

Igeo class

Sediment quality

EF < 1

No enrichment

0–0

0

Unpolluted

EF < 3

Minor enrichment

0–1

1

Unpolluted to moderately polluted

EF 3–5

Moderate enrichment

1–2

2

Moderately polluted

EF 5–10

Moderately severe enrichment

2–3

3

Moderately to highly polluted

EF 10–25

Severe enrichment

3–4

4

Highly polluted

EF 25–50

Extremely severe enrichment

4–5

5

Highly to very highly polluted

average upper continental crust (UCC) values (Rudnick and Gao 2003; Taylor and McLennan 1995). The Geoaccumulation index (Igeo), determines the status of metal contamination through comparison between surﬁcial sediment metal concentrations and natural background concentrations. Igeo is the most commonly calculated index of geoaccumulation and has been widely used (Amin et al. 2009; El Nemr et al. 2016; Müller 1979). It is calculated using the following equation:

Ms and Mc are metal concentrations in the sediment sample and the UCC values, while Fes and Fec are Fe concentrations in the sediment sample and UCC values respectively. Results of Igeo and EF were interpreted using Table 9.1. The Contamination factor (Cf) was calculated (Hakanson 1980) using the following equation:

Igeo ¼ log2 ðCn =1:5Bn Þ

where Cm is the concentration of element in the sample and Cb is the background concentration. Similarly, the Contamination degree (Cd) was calculated using the following equation:

ð9:2Þ

Cn and Bn represent the sample and background concentration of the metal ‘n’ respectively, and 1.5 is a constant included due to possible variations in the background value produced by lithogenic effects. In this study, due to the unavailability of local background concentrations, average upper continental crust values were used (Rudnick and Gao 2003; Taylor and McLennan 1995). The Enrichment Factor (EF) is another useful contamination index. In this study, iron was used as the reference element for geochemical normalization (Cheriyan et al. 2015; El-Sorogy et al. 2016; Saher and Siddiqui 2016; Schiff and Weisberg 1999). It is calculated using the following equation: EF ¼

Table 9.2 Interpretation categories for potential ecological risk and ecological risk index

Ms Fes

Mc Fec

Cf ¼ ðCm =Cb Þ

Cd ¼

i¼n X

ð9:4Þ

ð9:5Þ

Cf

i¼1

where Cd is the sum of the Cf for each sample. By using the Threshold Effect Levels (TELs) developed by Long et al. (1995), Adverse Effect Index (AEI) values were calculated using the following equation: AEI ¼

ðMetÞ ðERLÞ

ð9:6Þ

ð9:3Þ

Potential ecological risk

Risk index

Value

Category

Value

Category

Eri \40

Low

RI 150

Low

40 Eri \80

Moderate

150 RI < 300

Moderate

80 Eri \160

Considerable

300 RI < 600

Considerable

160 Eri \320

High

600 RI

Very high

Eri

320

Very high

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Metal Contamination Assessment in the Sediments …

151

Fig. 9.2 Spatial distribution of: a arsenic, b chromium, c cobalt and copper in the study area

where Met is the metal concentration in the sediment and ERL is the Effects Range-Low as reported by Long et al. (1995). According to Muñoz-Barbosa et al. (2012), if AEI 1 the metal concentration in the sample is not high enough to produce adverse effects in biota; however, if AEI 1 the metal concentration in the sample could produce adverse effects. Potential ecological risk index (ER) determines the level of metal toxicity and ecological sensitivity to metal contamination (Hakanson 1980) and is calculated using the following equation: Eri ¼ Cfi Tfi

ð9:7Þ

where Cfi is the contamination factor and Tfi is the response coefﬁcient for the toxicity of the single metal. The

corresponding Tfi values used are: Hg = 40, As = 10, Cu = Pb = Ni = 5, Cr = 2, Zn = 1. Potential toxicity response index (RI), a single index combining all of the metals studied, is calculated using the following equation: X RI ¼ Efi ð9:8Þ

where RI is the sum of the Efi for each studied metal. The interpretation categories for RI are shown in Table 9.2. All analyses were performed in the statistical package R (R Core Team 2014). Base R was used for cluster analysis while for PCA and DA, functions of the FactoMineR package (Lê et al. 2008) and MASS packages were used. Data were standardized prior to analysis.

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Fig. 9.3 Spatial distribution of: a iron, b manganese, c mercury and d molybdenum in the study area

Results Metal Distribution in Sediments The spatial distribution of 11 metals, namely As, Co, Cr, Cu, Fe, Hg, Mn, Mo, Ni, V, Zn are shown in Figs. 9.2, 9.3 and 9.4 and are summarized in Table 9.3. As cadmium and lead concentrations were less than the method detection limits in more than 80% of the stations they were not used in the estimation of summary statistics. Based on mean concentrations, metals in the surface sediments of the northern Red Sea exhibited the following order: Fe (6320.61 mg kg−1) > Mn (409.71 mg kg−1) > Zn (38.76 mg kg−1) > V (19.73 mg kg−1) > Ni (15.92 mg kg−1) > Cu (15.51 mg kg−1) > Cr (14.6 mg kg−1) > Co (6.53 mg kg−1) > As

(5.21 mg kg−1) > Mo (1.06 mg kg−1) > Hg (0.03 mg kg−1). The mean concentrations of Co, Cu, Fe, Mn, Ni, V and Zn showed progressive increments from the nearshore locations to the central axis zone while Cr and Hg were highest in the nearshore stations.

Comparison with UCC and Sediment Quality Guidelines Table 9.4 shows the comparison of metal concentrations in the present study to that of the average upper continental crust concentrations (UCC), threshold effect concentration (TEL) and probable effect concentration (PEL). Except for arsenic, mean concentrations of all the metals were less than the UCC. Ignoring the arsenic concentrations that

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153

Fig. 9.4 Spatial distribution of: a nickel, b vanadium, c zinc and d ﬁne-grained sediments in the study area

were less than the method detection limits, 88% of the stations showed exceedance relative to UCC and 8% of the stations showed exceedance relative to the threshold effects level (TEL). The average concentration of nickel showed a slight exceedance relative to the TEL, with exceedance relative to the UCC and TEL in 13% and 50% of the stations respectively. Mercury showed a slight exceedance of UCC at station 49 (Fig. 9.1). Concentrations of copper in all the stations were less than the UCC, while 22% of the stations exhibited exceedance relative to TEL. The mean PEL Quotient, the combination of six studied metals, showed that stations 13, 30, 37, 41 and 45 have 8% probability of being biologically toxic while the remaining stations have a 21% probability (Fig. 9.5).

Assessment of Geoaccumulation Index (Igeo) The geoaccumulation index is used in evaluating the concentration of metal contamination compared to a reference value (average upper continental crust concentration). The results are shown in Table 9.3. The results showed that the surﬁcial sediments of the Red Sea were uncontaminated for all the investigated metals except for As. Based on Igeo values, all the sampled stations were uncontaminated (class 1) for arsenic, while 72% of the stations were moderately contaminated (class 2). The mean Igeo values were 1.18 (As), −0.95 (Ni), −1.33 (Hg), −1.34 (Cu), −1.52 (Zn), and −1.88 (Cr). According to the mean Igeo values, contamination levels of As were in the increasing order of CA > NS > MID.

−1

51.00

28.23

9.72

Max.

Avg.

sd.

−1.42

−2.00

0

Igeo avg.

Classiﬁcation

3.90

2.43

ME

EF max.

EF avg.

Classiﬁcation*

MDE

3.27

3.92

2.57

MDE

3.29

4.29

2.16

0

−1.34

−0.68

−1.68

10.54

43.18

66.61

33.18

MDE

4.31

6.71

2.83

0

−1.15

−0.42

−1.86

4.56

14.20

22.41

8.25

MDE

4.53

6.29

3.74

0

−0.94

−0.28

−2.03

3.76

16.08

24.76

7.33

MID

MDE

4.67

5.30

3.20

0

−0.83

−0.37

−1.14

2.53

17.07

23.17

13.64

RZ

ME-minor enrichment; MDE-moderate enrichment; SE-severe enrichment

*

1.50

EF min.

EF

−0.96

−1.06

0

−2.54

−2.76

Igeo min.

8.41

40.98

54.78

Igeo max

Igeo

15.78

Min.

18.26

Ni RZ

NS

MID

Zn

NS

Concentration (mg kg )

Metal/Station type

ME

2.98

4.56

2.06

0

−1.68

−0.86

−2.44

5.44

17.11

28.85

9.66

NS

Cr

ME

2.38

4.31

1.85

0

−1.89

−1.34

−2.41

2.66

14.40

20.68

9.89

MID

ME

2.03

2.29

1.12

0

−2.04

−1.84

−2.22

1.08

12.84

14.66

11.27

RZ

ME

2.73

4.92

1.66

0

−1.83

−0.89

−2.67

4.30

11.29

20.26

5.87

NS

Cu

MDE

3.63

4.69

2.71

0

−1.27

−0.78

−2.53

3.33

16.03

21.77

6.51

MID

MDE

3.94

4.52

3.15

0

−1.07

−0.73

−1.36

2.83

18.08

22.62

14.64

RZ

SE

24.21

56.39

11.56

2

1.20

1.68

0.83

0.86

5.22

7.23

4.00

NS

As

SE

19.48

40.65

13.12

2

1.12

1.82

0.83

0.96

4.97

7.95

4.00

MID

Table 9.3 Summary statistics of trace metal concentrations (mg kg−1), geoaccumulation index (Igeo) and enrichment factor (EF) for the study area

SE

20.84

26.25

16.69

2

1.33

1.88

1.14

0.97

5.72

8.26

4.94

RZ

Hg

MDE

4.94

12.86

1.68

0

−1.20

−0.36

−1.88

0.010

0.034

0.058

0.020

NS

MDE

3.82

11.81

1.38

0

−1.30

−0.61

−2.62

0.009

0.032

0.049

0.012

MID

ME

2.95

4.36

1.94

0

−1.51

−1.12

−1.93

0.004

0.027

0.035

0.020

RZ

154 M. Karuppasamy et al.

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Table 9.4 Comparison of mean metal concentrations to average upper continental crust values and sediment quality guidelines UCC and sediment quality guidelines

Zn

Ni

Cr

Cu

As

Hg

References

UCC

71

20

35

25

1.5

0.05*

Taylor and McLennan (1995)

TEL

124

15.9

52.3

18.7

7.2

0.13

Macdonald et al. (1996)

PEL

271

42.8

160

108

41.6

0.7

Macdonald et al. (1996)

Mean

38.77

15.92

14.6

15.51

5.17

0.031

This study

*

Rudnick and Gao (2003)

Fig. 9.5 Spatial distribution of mean PEL quotient values in surface sediments of the Red Sea. The 4 colored lines, green, blue, orange and red represent the 8, 21, 49 and 73% probability of being biologically toxic

Assessment of Enrichment Factor (EF) The enrichment factor is used to distinguish the metals from geogenic (crustal) and anthropogenic (non-crustal) sources (Feng et al. 2004). EF values between 0.5 and 1.5 indicate that the given metal is entirely derived from crustal materials or natural weathering processes, whereas EF values higher than 1.5 suggest that a signiﬁcant portion of the metal is delivered from non-crustal materials and the sources are

more likely to be anthropogenic (Zhuang and Gao 2014) The mean EF values were 20.84 (As), 4.52 (Ni), 3.84 (Hg), 3.51 (Cu), 3.09 (Zn), and 2.42 (Cr) (Table 9.3). The order of enrichment was As > Ni > Hg > Cu > Zn > Cr. Based on average EF values, As showed high enrichment, while Ni, Hg, Cu and Zn showed moderate enrichment and Cr showed minor enrichment. Figures 9.6 and 9.7 show the spatial distribution of the calculated EFs for each of the studied metals. Based on the averages obtained for the sampled

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Fig. 9.6 Spatial distribution of: a As and b Ni enrichments; c and d show the average EF values of As and Ni based on locations. Blue, orange, pink and red dashed lines represent the minor, moderate, moderately severe and severe enrichment guidelines

locations, As showed high enrichment, Ni showed moderate enrichment and Cr showed minor enrichment in the nearshore, mid and central axis zone respectively. On the other hand, Zn and Cu showed minor enrichment in the nearshore stations while Hg showed minor enrichment in the stations occupied in the central axis.

Assessment of Adverse Effect Index (AEI) AEI values of Zn, Cr, and Hg in all the sampled stations were less than 1 suggesting no adverse effects to the marine biota. However, around 50% of the stations exceeded 1 for Ni, 22% for Cu, and 5% for As. At station 40, the AEI value was higher than 1 for all the three metals, Ni, Cu and As. Stations 23, 31, 40, 43, 44, 51, 52, 53, 60, 62, 63 and 64 exceeded 1 for both Ni and Cu. The average values of the AEI were 1.00 (Ni), 0.83 (Cu), 0.72 (As), 0.31(Zn), 0.28

(Cr) and 0.24 (Hg) (Table 9.5). Based on average AEI values, the order of the adverse effect of metals was Ni > Cu > As > Zn > Cr > Hg. Overall, as the average AEI values were less than 1, no adverse effect of the studied metals is expected on the marine biota. Based on the averages obtained by location for the sampled stations (Fig. 9.8), the AEI was less than 1 for all metals, except Ni which was higher than 1 in stations occupied in the central axis. The average AEI value of Ni was also greater than 1 for depths greater than 1000 m (Fig. 9.9).

Assessment of Potential Ecological Risk Factor (ER) and Potential Ecological Index (RI) The ER values of Zn, Ni, Cr, and Cu in all the sampling stations were less than 40 and hence pose a low hazard. However, ER values of As were higher than 40 in 13% of

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Fig. 9.7 Spatial distribution of: a Cr, b Cu, c Hg and d Zn enrichments in the study area

the stations while for Hg it was higher only at station 49. In the case of As, stations which exceeded 40 are: 22, 40, 41, 44, 52, 53, 56 and 59. The average values of the ER were 34.76 (As), 24.75 (Hg), 3.98 (Ni), 3.1 (Cu), 0.83 (Cr) and 0.55 (Zn) (Table 9.5). Based on average ER values, the order of the potential adverse effect of metals were As > Hg > Ni > Cu > Cr > Zn. Average values based on location (Fig. 9.10) and depth (Fig. 9.11) also pose a low ecological risk ( MID > CA. Regression of Fe on Zn, Ni, Cr, Cu, As and Hg was performed. The scatter plots and their regression curves

(Figs. 9.12, 9.13 and 9.14) show that several points lie above the 95% conﬁdence limit of the metal to Fe regression lines suggesting anomalous enrichment of these metals. The order of anomalous enrichments were: Ni > Hg > Cu > As > Zn > Cr. Hierarchical cluster analysis (HAC), principal component analysis (PCA) and linear discriminant analysis (LDA) were used in the evaluation of the contamination status of sediments in the Saudi Arabian waters of the Red Sea.

Grouping of Stations Based on HAC Hierarchical agglomerative cluster analysis (Fig. 9.15) was performed on the normalized data set by means of Ward’s

0.41

0.23

NAE

Max.

Avg.

Classiﬁcation

NAE

0.33

0.44

0.15

MID

0.22

0.72

0.40

LR

Min.

Max.

Avg.

Classiﬁcation

LR

0.58

0.77

0.26

Potential ecological risk factor (ER)

0.13

Min.

Adverse effect index (AEI)

NS

Zn

LR

0.61

0.94

0.47

NAE

0.35

0.54

0.27

RZ

LR

3.55

5.60

2.06

NAE

0.89

1.41

0.52

NS

Ni

LR

4.02

6.19

1.83

AE

1.01

1.56

0.46

MID

LR

4.27

5.79

3.41

AE

1.07

1.46

0.86

RZ

LR

0.98

1.65

0.55

NAE

0.33

0.55

0.18

NS

Cr

LR

0.82

1.18

0.57

NAE

0.28

0.40

0.19

MID

LR

0.73

0.84

0.64

NAE

0.25

0.28

0.22

RZ

LR

2.26

4.05

1.17

NAE

0.60

1.08

0.31

NS

Cu

LR

3.21

4.35

1.30

NAE

0.86

1.16

0.35

MID

Table 9.5 Summary statistics of adverse effect index (AEI) and potential ecological risk (ER) for the study area

LR

3.62

4.52

2.93

NAE

0.97

1.21

0.78

RZ

LR

34.79

48.21

26.67

NAE

0.72

1.00

0.55

NS

As

LR

33.16

53.00

26.67

NAE

0.69

1.10

0.55

MID

LR

38.15

55.04

32.96

NAE

0.79

1.14

0.68

RZ

LR

27.08

46.59

16.35

NAE

0.26

0.45

0.16

NS

Hg

LR

25.40

39.20

9.76

NAE

0.24

0.38

0.09

MID

LR

21.35

27.66

15.79

NAE

0.21

0.27

0.15

RZ

158 M. Karuppasamy et al.

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Fig. 9.8 Distribution with location of AEI values for Zn, Ni, Cr, Cu, As and Hg in the surface sediments of the Red Sea. NS, MID and CA represent the nearshore, middle and central axis zone respectively. The horizontal dashed red line shows the AEI value of 1

method, using Euclidean distances as a measure of similarity. The results obtained are presented by a dendrogram (Fig. 9.15). Based on 60 stations, the dendrogram displays grouping of 4 distinct clusters that were identiﬁed as (NE) cluster 1, cluster 2 (ME), cluster 3 (MME) and cluster 4 (SE) respectively. Cluster 1 was characterized by most of the coastal stations showing the least or no enrichment (NE) and could be grouped as ‘uncontaminated’. Cluster 2 was characterized mostly by stations located between the coast and central rift, showing minor enrichment (ME). Cluster 3 included stations mostly from the central rift zone showing metallogenic minor enrichment (MME), probably due to

metallogenesis from intense hydrothermal activity in the axial deeps. Cluster 4 had stations with the highest mean concentrations of the analyzed metals showing severe enrichment (SE), characterized by stations adjacent to coastal cities, namely Al Wajh and Umluj, possibly due to anthropogenic inputs.

Grouping of Stations Based on PCA Principal component 1 describes 40.66% of the original information, principal component 2 describes 27.46% and

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Fig. 9.9 Distribution with depth of AEI values for Zn, Ni, Cr, Cu, As and Hg in the surface sediments of the Red Sea. L500, G500 and G1000 represent depths less than 500, greater than 500 and greater than 1000 m respectively. The horizontal dashed red line shows the AEI value of 1

principal component 3 describes 21.2% (Fig. 9.16). The cumulative percentage of principal components 1, 2 and 3 was 89.34%. Principal component analysis identiﬁed nickel, arsenic and mercury enrichments as the domains that loaded most robustly on the ﬁrst principal component (Table 9.6 and Fig. 9.17a). For the second principal component, the domains of depth, copper, chromium and zinc enrichments were the most robust (Table 9.6 and Fig. 9.17b). From Fig. 9.3, it is possible to observe that principal component 1 separates stations occupied in cluster 4 (SE) from those of other clusters. The biplot (Fig. 9.18) shows that copper and zinc enrichments were highly correlated with depth while

enrichments of As, Hg and Cr increase with increasing longitude (from offshore to nearshore).

Grouping of Stations Based on LDA Spatial variations were further evaluated through discriminant analysis (p < 0.01). The classiﬁcation of functions (DFs) and matrices (CMs) for LDA of spatial concentrations of metal enrichments in the Red Sea obtained from the standard modes are shown in Fig. 9.19 and Table 9.7. The ﬁrst linear discriminant explained 74% of the between-group

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Fig. 9.10 Distribution with location of ER values for Zn, Ni, Cr, Cu, As and Hg in the surface sediments of the Red Sea. NS, MID and CA represent the nearshore, middle and central axis zone respectively. The horizontal dashed red line shows the ER value of 40

variance while the second and third discriminant explained 26 and 5% respectively. According to the standard DA mode using all discriminant variables, the corresponding CMs assigned 100% of the cases correctly.

Discussion Table 9.8 shows the comparison of metal concentrations from the present study to those of similar studies conducted in the Red Sea. In this study, an assessment of metal

contamination of sediment samples collected from several stations covering the entire Saudi Arabian waters of Red Sea has been conducted. Regarding chromium, all the samples collected in this study were less than the ERM levels. The upper limits measured in the present study were less than the earlier observations in the Saudi waters of Red Sea (Badr et al. 2009) Chromium is primarily used in the manufacturing of steel and alloys, to preserve wood, tan leather, electroplating metals, in pigments, dyes, drilling muds, and in corrosion inhibitors (Lin et al. 2013). In aquatic systems, it exists in

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M. Karuppasamy et al.

Fig. 9.11 Distribution with depth of ER values for Zn, Ni, Cr, Cu, As and Hg in the surface sediments of the Red Sea. NS, MID and CA represent the nearshore, middle and central axis zone respectively. The horizontal dashed red line shows the ER value of 40

trivalent or hexavalent form; the toxicity of the latter is higher than the former due to its bioavailability in aquatic systems. Nickel is used primarily in the manufacturing of stainless steel, nickel plating and nickel alloys. Fossil fuel combustion, nickel ore smelting and reﬁning are the major anthropogenic sources (Saffran et al. 2001). Nickel concentrations in the present study ranged from 7.33 to 24.76 mg kg−1 with an average concentration of 15.92 mg kg−1. Nickel concentrations around 25% of the stations were above the TEL value (18 mg kg−1). However, nickel concentrations in all

the stations were less than the ERM levels. The upper limits of nickel concentrations in the present study were three times less than the concentrations obtained by previous studies in Jeddah, Rabigh and Yanbu (Badr et al. 2009). Generally, nickel concentrations were similar to the concentrations recorded from Egypt and Yemen (Al-Shiwaﬁ et al. 2005; El Nemr et al. 2016). Also, as the pH value in the marine environment is greater than 6.7, nickel will predominantly exist as Ni hydroxides and becomes incorporated into sediments (Sunderman and Oskarsson 1991).

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Fig. 9.12 Relationship of a As, and b Cr concentrations (mg kg−1) with that of Fe (mg kg−1) in the sediments from the study area. Red dots represent the anomalous stations

Copper is an abundant element in the Earth’s crust and is an essential nutrient for both aquatic plants and animals, but is toxic at higher concentrations. Major anthropogenic sources of copper include mining, smelting, reﬁning, sewage and sludge dumpsites, and antifouling paints (Badr et al. 2009; Saffran et al. 2001). In the present study, copper concentrations ranged from 5.87 to 22.61 mg kg−1 with an average concentration of 15.51 mg kg−1. All the samples collected in this study were less than the TEL and ERM

levels. Also, the upper limits of copper concentrations from the present study match the concentrations obtained in Jeddah, Rabigh and Yanbu (Badr et al. 2009) and were less than the concentrations obtained in Sudan and Egypt (Dar et al. 2016; Idris et al. 2007). Zinc ranks as the 24th most abundant element in the Earth’s crust. It is a common contaminant in agricultural and food wastes, manufacturing of pesticides as well as antifouling paints (Badr et al. 2009). Organisms can take up

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M. Karuppasamy et al.

Fig. 9.13 Relationship of a Cu, and b Hg concentrations (mg kg−1) with that of Fe (mg kg−1) in the sediments from the study area. Red dots represent the anomalous stations

zinc, which is reflected in the BCF but the concentrations in the tissues are of no toxicological signiﬁcance (Chapman et al. 1996). Zinc appears to have a protective effect against the toxicities of both cadmium and lead (Calabrese et al. 1985). In the present study, concentrations of Zn ranged from 15.77 to 66.60 mg kg−1 with an average concentration of 38.77 mg kg−1. Similarly to copper, all the samples collected in this study were less than the stipulated TEL and ERM levels. Mean zinc concentrations in the present study were comparable to similar studies conducted in Egypt and Yemen (Omar et al. 2016; Salem et al. 2014) and were less

than the concentrations recorded in the Farasan Islands (Usman et al. 2013) and different locations in Saudi Arabia (Badr et al. 2009). Mercury is one of the most harmful contaminants in the marine environment (Araujo et al. 1996) Due to global mercury cycling, mercury is found in appreciable concentrations even in regions with no mercury emissions (Fisher 2003). It is listed as a high priority environmental contaminant by the Convention for the Protection of the Marine Environment of the North East Atlantic (OSPAR Convention), the International European Union Water Framework Directive

9

Metal Contamination Assessment in the Sediments …

Fig. 9.14 Relationship of a Ni, and b Zn concentrations (mg kg−1) with that of Fe (mg kg−1) in the sediments from the study area. Red dots represent the anomalous stations

Fig. 9.15 Hierarchical cluster analysis of metal concentrations from the study area

165

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M. Karuppasamy et al.

Fig. 9.16 Results of principal component analysis of metal enrichments from the study area

Table 9.6 Explanation for the total variance of the PCA analysis

Variables

VF1

VF2

VF3

EF-Zn

0.714

0.566

−0.145

EF-Ni

0.935

0.06

−0.04

EF-Cr

0.558

−0.631

EF-Cu

0.683

0.695

−0.034

EF-As

0.796

−0.302

0.326

EF-Hg

0.793

−0.387

0.261

Latitude Longitude

−0.34 0.295

0.44

0.195

0.911

−0.453

−0.829

Depth

0.185

0.885

0.036

Eigen value

3.66

2.47

1.90

% Total variance

40.66

27.46

21.21

Cumulative % variance

40.66

68.12

89.33

(EUWFD) and the United States Environmental Protection Agency (Palma et al. 2009). Mercury concentrations in the present study ranged from 0.012 to 0.058 mg kg−1 with an average concentration of 0.031 mg kg−1. All the samples collected in this study were less than the stipulated TEL and ERM levels. Mercury concentration levels in the present study were comparable to the concentrations recorded in Egypt (El Nemr et al. 2016) but were slightly higher than the concentrations recorded in Rabigh (Usman et al. 2013). A battery of geochemical and ecological risk assessment methods was used in evaluating the contamination status of surﬁcial sediments from the Red Sea. The geoaccumulation index classiﬁes the contamination status of sediments into

seven levels from uncontaminated to very contaminated. Based on geoaccumulation indices, arsenic was the only metal to exhibit moderate contamination in 72% of the stations. This could be due to the enrichment of arsenic in sulﬁde-rich sediments especially found in the median valley of the Red Sea (Hendricks et al. 1969; Kaplan et al. 1969; Onishi and Sandell 1955). All of the stations from the central axis had Igeo values greater than 1 and hence were categorized as moderately contaminated. Even though the geoaccumulation index is commonly used, it tends to minimize the degree of contamination because of the artiﬁcial introduction of 1.5 as the numerical factor (Covelli and Fontolan 1997). Based on the EF, As was the only metal which showed

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Fig. 9.18 Biplot of enrichment factors and groups based on principal component analysis

Fig. 9.17 Contribution of metals and other factors to dimensions 1 and 2

extreme enrichments at stations 30, 37, 40, 41, 45 and 49 located between Al Wajh and Umluj. Of these, stations 37, 41 and 45 exhibited moderately high enrichments for Ni and Hg, and moderate enrichments for Cu and Cr. Based on the adverse effect index (AEI), values higher than 1 were observed in 50, 22 and 5% of the stations for Ni, Cu and As. As was found to be higher than 1 in stations 22, 40 and 59. Station 40 (Fig. 9.1) had AEI value higher than 1 for Ni, Cu and As. Threshold effects levels (TEL) represent the upper limit of the range of sediment contaminant concentrations below which harmful effects are unlikely to be observed and above which they may or may not be observed. Concentrations of As, Ni, Cu and Hg showed exceedance relative to the TEL in 8%, 50%, 22% and 2% of the stations, respectively. The potential ecological risk index (ER) is a comprehensive method that determines the level of single element toxicity and uses a toxic-response factor for a given

Table 9.7 Classiﬁcation matrix for DA of spatial variation in the metal enrichment levels

Regions assigned by CA

Fig. 9.19 Results of discriminant analysis of metal enrichments from the study area

element, and thus can be used to evaluate the combined contamination risk from all of the elements to an ecological system, given by the potential toxicity response index (RI). Based on the ER, arsenic in 8 of the 60 stations had values greater than 40 and hence was a moderate potential ecological risk. Mercury was another metal to show a value greater than 40, but only at station 49. On the other hand, the RI was less than 150 and hence the risk from all of the metals combined is low. The results of PCA, CA and DA clearly indicate anthropogenic enrichments of nickel, arsenic and mercury in the region between Al Wajh and Umluj. Hence, further investigations focusing on these hotspots are required in order to identify the source of metal contamination in these locations.

% correct

Regions assigned by DA NE

ME

MME

SE

NE

100

5

0

0

0

ME

100

0

17

0

0

MME

100

0

0

34

0

SE

100

0

0

0

4

Total

100

5

17

34

4

168

M. Karuppasamy et al.

Table 9.8 Concentrations of selected metals (mg kg−1) in the surﬁcial sediments based on current and previous studies from the Red Sea Location (Red Sea)

Cr

Ni

Cu

Zn

Hg

References

Saudi Arabian territorial waters

M = 14.6

M = 15.92

M = 15.51

M = 38.77

M = 0.031

Present study (2016)

Jeddah, Saudi Arabia

12.98–22.81

67.78– 85.50

17.47– 23.77

52.74–76.36

–

Badr et al. (2009)

Rabigh, Saudi Arabia

13.18–25.69

79.69– 80.49

17.43– 25.13

41.36–63.43

–

Yanbu, Saudi Arabia

22.37–35.36

79.20– 90.79

18.38– 25.76

54.78–93.86

–

Rabigh, Saudi Arabia

Mean = 20.62

Mean = 8.69

Mean = 16

Mean = 39.71

Mean = 0.01

Youssef and El-Sorogy (2016)

Farasan Islands, Saudi Arabia

M = 9.61

M = 8.48

M = 112

M = 57.2

–

Usman et al. (2013)

Sudan

–

M = 102

M = 68.8

M = 83.6

–

Idris et al. (2007)

Egypt

M = 18.46

M = 11.40

M = 1.93

M = 22.63

M = 0.02

Salem et al. (2014)

Egypt

–

M = 13.72

M = 0.62

M = 26.27

M = 0.03

El Nemr et al. (2016)

Egypt

–

–

17.33– 75.83

76.23– 215.71

–

Dar et al. (2016)

Egypt

–

–

21.43

51.4

–

Okbah et al. (2005)

Yemen

15.9–24.5

9.3–14.7

24.8–39.3

88.6–138

–

Al-Shiwaﬁ et al. (2005)

Yemen

–

–

37.4–80.3

9.4–30.3

–

Omar et al. (2016)

Conclusion In the present study, sediment contamination in the northern Red Sea was evaluated by comparison with sediment quality guidelines (SQGs) and by using several geochemical, ecological, and multivariate statistical tools. Arsenic was the only element that showed exceedance to SQGs. As arsenic could naturally enter the marine environment either by weathering and decomposition of rocks or in the form of dust storms (El-Sorogy et al. 2016; Nriagu and Pacyna 1988), it would be difﬁcult to distinguish the source of arsenic as natural or anthropogenic. Distribution of arsenic in the central Red Sea reveals a natural source while elevated arsenic concentrations near Al Wajh and Yanbu could be due to point and non-point sources of pollution from industrial discharges and harbour activities. The second element that showed exceedance to TEL in 50% of the sampled stations is nickel. Nickel, being an abundant metal in the Earth’s crust, is found at relatively high levels along the central axis of the Red Sea. Also, nickel is insoluble in alkaline waters typically found in marine environments and exists predominantly as Ni hydroxides that get incorporated into sediments (Sunderman and Oskarsson 1991). Similar to arsenic, nickel and chromium enrichments along the coastal regions of Al Wajh, Yanbu and Rabigh could be attributed to

discharges from the reﬁneries, shipping and port activities. Isolated higher concentrations of mercury at Umluj could probably be due to the enrichment from anthropogenic sources associated with sewage discharges and the activities of the ﬁshing harbour in this region. Overall, the northern Red Sea is relatively uncontaminated except for some isolated hotspots in the region between Al Wajh and Umluj where anthropogenic enrichments of nickel, arsenic and mercury are evident.

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Metal Contamination Assessment in the Sediments …

Chapman PM, Allen HE, Godtfredsen K, Z’Graggen MN (1996) Policy analysis, peer reviewed: evaluation of bioaccumulation factors in regulating metals. Environ Sci Technol 30:448A–452A Cheriyan E, Sreekanth A, Mrudulrag SK, Sujatha CH (2015) Evaluation of metal enrichment and trophic status on the basis of biogeochemical analysis of shelf sediments of the southeastern Arabian Sea, India. Cont Shelf Res 108:1–11 Covelli S, Fontolan G (1997) Application of a normalization procedure in determining regional geochemical baselines. Environ Geol 30:34–45 Dar MA, Fouda FA, El-Nagar AM, Nasr HM (2016) The effects of land-based activities on the near-shore environment of the Red Sea. Egypt Environ Earth Sci 75:1–17 El-Sikaily A, Khaled A, Nemr AE (2004) Heavy metals monitoring using bivalves from Mediterranean Sea and Red Sea. Environ Monit Assess 98:41–58 El-Sorogy AS, Youssef M, Al-Kahtany K, Al-Otaiby N (2016) Assessment of arsenic in coastal sediments, seawaters and molluscs in the Tarut Island, Arabian Gulf, Saudi Arabia. J Afr Earth Sci 113:65–72 El Nemr A, El-Said GF, Khaled A, Ragab S (2016) Distribution and ecological risk assessment of some heavy metals in coastal surface sediments along the Red Sea. Egypt Int J Sed Res 31:164–172 Feng H, Han X, Zhang W, Yu L (2004) A preliminary study of heavy metal contamination in Yangtze River intertidal zone due to urbanization. Mar Pollut Bull 49:910–915 Fernandes C, Fontaínhas-Fernandes A, Cabral D, Salgado MA (2008) Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz-Paramos lagoon, Portugal. Environ Monit Assess 136:267–275 Fisher JF (2003) Elemental mercury and inorganic mercury compounds: human health aspects. World Health Org, Geneva Hakanson L (1980) An ecological risk index for aquatic pollution control. A sedimentological approach. Water Res 14:975–1001 Hanna RG (1992) The level of heavy metals in the Red Sea after 50 years. Sci Total Environ 125:417–448 Hendricks RL, Reisbick FB, Mahaffey EJ, Roberts DB, Peterson MN (1969) Chemical composition of sediments and interstitial brines from the Atlantis II, Discovery and Chain Deeps. In: Degens ET, Ross DA (eds) Hot brines and recent heavy metal deposits in the Red Sea. Springer, New York, pp 407–440 Hübner R, Astin KB, Herbert RJ (2009) Comparison of sediment quality guidelines (SQGs) for the assessment of metal contamination in marine and estuarine environments. J Environ Monit 11:713–722 Idris AM, Eltayeb M, Potgieter-Vermaak SS, Van Grieken R, Potgieter J (2007) Assessment of heavy metals pollution in Sudanese harbours along the Red Sea Coast. Microchem J 87:104–112 Kaplan I, Sweeney R, Nissenbaum A (1969) Sulfur isotope studies on Red Sea geothermal brines and sediments. In: Degens ET, Ross DA (eds) Hot brines and recent heavy metal deposits in the Red Sea. Springer, New York, pp 474–498 Kharroubi A, Gargouri D, Baati H, Azri C (2012) Assessment of sediment quality in the Mediterranean Sea-Boughrara lagoon exchange areas (southeastern Tunisia): GIS approach-based chemometric methods. Environ Monit Assess 184:4001–4014 Kucuksezgin F, Aydin-Onen S, Gonul L, Pazi I, Kocak F (2011) Assessment of organotin (butyltin species) contamination in marine biota from the Eastern Aegean Sea, Turkey. Mar Pollut Bull 62:1984–1988 Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18 Lin YC, Chang-Chien GP, Chiang PC, Chen WH, Lin YC (2013) Multivariate analysis of heavy metal contaminations in seawater and

169 sediments from a heavily industrialized harbor in southern Taiwan. Mar Pollut Bull 76:266–275 Long E, MacDonald D (1998) Recommended uses of empirically derived, sediment quality guidelines for marine and estuarine ecosystems. Hum Ecol Risk Assess 4:1019–1039 Long ER, Macdonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manage 19:81–97 Macdonald DD, Carr RS, Calder FD, Long ER, Ingersoll CG (1996) Development and evaluation of sediment quality guidelines for Florida coastal waters. Ecotoxicology 5:253–278 Mansour AM, Askalany MS, Madkour HA, Assran BB (2013) Assessment and comparison of heavy-metal concentrations in marine sediments in view of tourism activities in Hurghada area, northern Red Sea, Egypt. Egypt J Aquatic Res 39:91–103 Marchand C, Lallier-Verges E, Baltzer F, Albéric P, Cossa D, Baillif P (2006) Heavy metals distribution in mangrove sediments along the mobile coastline of French Guiana. Mar Chem 98:1–17 Müller G (1979) Schwermetalle in den Sedimenten des Rheins-Veränderungen seit 1971. Umschau 79:778–783 Muñoz-Barbosa A, Gutiérrez-Galindo E, Daesslé L, Orozco-Borbón M, Segovia-Zavala J (2012) Relationship between metal enrichments and a biological adverse effects index in sediments from Todos Santos Bay, northwest coast of Baja California, México. Mar Pollut Bull 64:405–409 Nriagu JO, Pacyna JM (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333:134–139 Okbah M, Shata M, Shridah M (2005) Geochemical forms of trace metals in mangrove sediments—Red Sea (Egypt). Chem Ecol 21:23–36 Omar WA, Saleh YS, Marie M-AS (2016) The use of biotic and abiotic components of Red Sea coastal areas as indicators of ecosystem health. Ecotoxicology 25:253–266 Onishi H, Sandell E (1955) Geochemistry of arsenic. Geochim Cosmochim Acta 7:1–33 Palma C, Lillebø A, Valenca M, Pereira E, Abreu M, Duarte A (2009) Mercury in sediments of the Azores deep sea platform and on sea mounts south of the archipelago—assessment of background concentrations. Mar Pollut Bull 58:1583–1587 Pan K, Lee OO, Qian PY, Wang WX (2011) Sponges and sediments as monitoring tools of metal contamination in the eastern coast of the Red Sea, Saudi Arabia. Mar Pollut Bull 62:1140–1146 PERSGA (2006) The State of the Marine Environment, Report for the Red Sea and Gulf of Aden. PERSGA, Jeddah, 242 p R Core Team (2014) R: a language and environment for statistical computing (Version 3.0. 2). R Foundation for Statistical Computing, Vienna, Austria Rudnick RL, Gao S (2003) Composition of the continental crust. In: Rudnick RL (ed) Treatise on geochemistry, vol 3. Elsevier, pp 1–64 Saffran K, Cash K, Hallard K, Neary B, Wright R (2001) Canadian water quality guidelines for the protection of aquatic life. CCME Water Quality Index 1.0 Users’ Manual, 5 p Saher NU, Siddiqui AS (2016) Comparison of heavy metal contamination during the last decade along the coastal sediment of Pakistan: multiple pollution indices approach. Mar Pollut Bull 105:403–410 Salem DMA, Khaled A, El Nemr A, El-Sikaily A (2014) Comprehensive risk assessment of heavy metals in surface sediments along the Egyptian Red Sea coast. Egypt J Aquat Res 40:349–362 Sany SBT, Salleh A, Rezayi M, Saadati N, Narimany L, Tehrani GM (2013) Distribution and contamination of heavy metal in the coastal sediments of Port Klang, Selangor, Malaysia. Water Air Soil Pollut 224:1476

170 Schiff KC, Weisberg SB (1999) Iron as a reference element for determining trace metal enrichment in southern California coastal shelf sediments. Mar Environ Res 48:161–176 Singh KP, Malik A, Sinha S, Singh VK, Murthy RC (2005) Estimation of source of heavy metal contamination in sediments of Gomti River (India) using principal component analysis. Water Air Soil Pollut 166:321–341 Sunderman WF, Oskarsson A (1991) Nickel. In: Merian E (ed) Metals and their compounds in the environment. VCH, Weinheim, pp 1101–1126 Taylor SR, McLennan SM (1995) The geochemical evolution of the continental crust. Rev Geophys 33:241–265 Usman AR, Alkredaa RS, Al-Wabel M (2013) Heavy metal contamination in sediments and mangroves from the coast of Red Sea:

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Calcite and Aragonite Saturation Levels of the Red Sea Coastal Waters of Yemen During Early Winter and Expected pH Decrease (Acidification) Effects

10

Ahmed I. Rushdi, Aarif H. El-Mubarak and Khalid F. Al-Mutlaq

Abstract

Seawater samples from different depths of eight stations along the Red Sea coast of Yemen were collected during early winter for the determinations of the temperature, salinity, pH value and total alkalinity proﬁles. The seawater surface temperature at 100 m) it ranged from 21.7 to 22.1 °C. The salinities were found to range from 36.32 to 37.36‰ at surface seawaters and from 40.27 to 40.35‰ at >100 m depths. The pH ranged from 7.983 to 8.198 at surface seawater and from 7.960 to 8.052 at deeper layers. The total alkalinities were found to range from 2.3268 to 3.6159 meq kg−1 at surface layers and from 2.4082 to 2.9659 meq kg−1 in seawater layers deeper than 100 m. The results showed that the surface seawater layers were several-fold supersaturated with respect to both calcite and aragonite, where the percent degree of saturation values ranged from 511 to 852% with respect to calcite and from 340 to 567% with respect to aragonite. At >100 m depth the percent degree of saturation ranged from 327% to 396% and from 221% to 268% with respect to calcite and aragonite, respectively. The results suggest that low magnesian calcite and aragonite are likely the major carbonate solid phases formed under current saturation levels. Recent studies show that the present oceanic pH values may drop by 0.1 and 0.4 units in 50 and 200 years, respectively. Thus, a projected change of −0.1 pH unit decreases the saturation levels to 426–710% for calcite and 283–473% for aragonite in surface waters A. I. Rushdi (&) ETAL, 2951 SE Midvale Dr, Corvallis, OR 97333, USA e-mail: [email protected] A. I. Rushdi Faculty of Sciences, Department of Earth and Environmental Sciences, Sana’a University, Sana’a, Yemen A. H. El-Mubarak K. F. Al-Mutlaq Plant Protection Department, College of Food and Agriculture Sciences, King Saud University, Riyadh, Saudi Arabia

and to 286–327% for calcite and 196–221% for aragonite at >100 m depth. A drop of −0.4 pH unit decreases the calcite saturation levels of surface and deep waters to 243–406% and 155–189%, respectively, whereas the saturation levels for aragonite reduce by 184–210% for surface waters and 105–120% for deep waters. These drops will affect the morphology and mineralogy of calcium carbon deposits as well as the distribution of calcifying organisms in the region. Further studies are warranted to investigate the occurrence, distribution and mineralogy of corals and the effects of physical and chemical parameters upon their growth in the region.

Introduction The Red Sea is about 1932 km long and about 280 km in width (Morcos 1970). It lies between 30°N and 12°30′N with an estimated total surface area ranging from 438,000 to 541,000 km2 and volume between 215,000 and 251,000 km3 (Morcos 1970; Edwards and Head 1987; Rasul et al. 2015). The Red Sea is situated in an arid region where evaporation exceeds precipitation and is considered as the saltiest part of the world’s ocean (Morcos 1970; Meshal et al. 1983; Edwards and Head 1987; Soﬁanos et al. 2002). It is a comparatively shallow sea, where the shallow shelf is extensive in the south. Therefore, most of the Yemen coast, which is located in the southeast section of the Red Sea, occupies a very shallow shelf. The Red Sea shoreline of Yemen extends from Midi in the north to Dhubab near Bab el-Mandab. The narrow southern straits of Bab el-Mandab (29 km in width) are the boundary between the Red Sea and the Gulf of Aden. The degree of saturation of seawater with respect to calcium carbonate minerals controls the precipitation and dissolution rates of the calcium carbonate solid phase at different depths in the oceans (Heath and Culberson 1970; Morse and Berner 1972; Silter et al. 1975; Berner 1976; Chen et al. 2006). It also affects the presence, mineralogy and

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_10

171

172

morphology of calcium carbonates in seawater (Lowenstam and Epstein 1957; Takahashi 1975; Mackenzie and Pigott 1981; Mucci and Morse 1984; Given and Wilkinson 1985; Rushdi 1992, 1993, 1995; Rushdi et al. 1992; Loste et al. 2003; De Choudens-Sanchez and Gonzalez 2009). Calcium carbonate minerals are mainly formed by organisms in the marine environment and include mostly aragonite, pure calcite and calcite with various amounts of magnesium contents known as magnesian calcite (Berner 1975; Schlager and James 1978; Loste et al. 2003). Inorganic precipitation of calcium carbonate deposits may form in some special places such as the Bahamas Banks and the hot Arabian coasts (Broecker and Takahashi 1966; Broecker et al. 2001). Calcium carbonate deposits are mainly high magnesian calcite and aragonite with low fractions of low magnesian calcite and pure calcite (Friedman 1965; Gevirtz and Friedman 1966; Mansour and Madkour 2015). In seawater, the inorganic precipitation of calcium carbonate is inhibited by the presence of dissolved organic and inorganic chemicals (Simkiss 1964; Pytkowicz 1965, 1973; Suess 1973; Folk 1974; Berner 1975; Rushdi et al. 1992; Rushdi 1992, 1995; Sun et al. 2015). Aragonite is favoured to precipitate in a solution with a magnesium-to-calcium concentration ratio more than 4, such as in seawater (Kitano 1964; Given and Wilkinson 1985; Rushdi et al. 1992; Rushdi 1993).

Fig. 10.1 Map showing the station locations and sampling area

A. I. Rushdi et al.

The open ocean surface seawater is generally 200–400% supersaturated with respect to calcite and aragonite minerals (Cloud 1962; Pytkowicz and Flower 1967; Broecker et al. 1979; Feely et al. 1984, 1988; Langdon et al. 2000; Chen et al. 2006; Rushdi 2015; Tynan et al. 2016). Precipitation and overgrowth of calcium carbonate by marine organisms evidently depend on the saturation states of solutions (Smith and Roth 1979; Gattuso et al. 1999; Takagi 2002; Waldbusser et al. 2015). Studies show that regional and temporal saturation states of surface seawater control the biogenic calcium carbonate formation (Broecker and Takahashi 1966; Smith and Pesret 1974; Opdyke and Wilkinson 1993; Suzuki et al. 1995; Kleypas et al. 1999; Broecker et al. 2001; Gibbs et al. 2016). The main purposes of this study are to determine the degree of saturation levels of the Red Sea coastal waters of Yemen with respect to calcite and aragonite, their changes as a result of pH decrease (acidiﬁcation) due to excess CO2 in seawater, and the possible biogeochemical impacts of these changes.

Study Area The study area was along the Red Sea coast of Yemen extending from Kamaran Island in the north to Jabal Zuqar Island in the south (i.e., between about 14o04.17′ and

10

Calcite and Aragonite Saturation Levels of the Red Sea …

173

15o39.83′N latitude and 42o10.10′ and 42o59.75′E longitude), as shown in Fig. 10.1. The coastal zone of Yemen is characterized by various key coastal habitats, including coral reefs (patch and solitary corals and fringing reefs), mangrove stands, salt marshes and seagrasses (Rushdi et al. 1994). Despite the fact the distribution of coastal reefs is limited in Yemen, some areas such as the al-Salif area north of Hodiedah seaport are rich in coral reefs and carbonate deposits (IUCN 1987; El-Anbaawy et al. 1992; Al-Anbaawy 1993; Kotb 2004). Human and developmental activities along the coast of Yemen, such as bottom water ﬁshing for prawn and shrimps, oil-terminals for oil loading and tourism development may distress the coral reef habitats (Rushdi et al. 1994; Rushdi 2012, 2015).

Experimental Procedure Sampling and Analytical Methods The sample acquisition was performed on board the research vessel Ibn-Majid from September 18 to October 1, 1999. The shipboard sampling and hydrographic program were basic, and seawater samples were obtained using plastic (PVC) samplers. The order of the sampling during the cruise was oxygen, pH, salinity, total alkalinity and nutrients. Temperature, pH, total alkalinity and standard hydrographical parameters were determined on board. The precision (2r) of each analysis was calculated from replicates from the same sample. Salinity samples from the water sampler were stored in standard citrate of magnesia bottles and analyzed against Copenhagen standards following the titration method described by Grasshoff et al. (1982). The estimate of precision of the salinity was ±0.009‰. The pH and total alkalinity of each sample were measured immediately after sample collection. The combination electrode (EIL 1160200) was standardized with pH 4.01 and pH 7.00 buffers at 25 °C. The pH of the samples was calculated from the equation: pHsw ¼ 4:01

Esw E4 S

ð1Þ

where pHsw is the pH of the sample, Esw and E4 are respectively the measured potentials of the sample and 4.01 buffer, and S is the measured slope of the electrode obtained from S¼

E4 E7 2:99

ð2Þ

The electrode was standardized before and after running samples from each cast. The slope of the electrode response was constant over long periods and the measurements of the

7.00 buffer were made at the beginning and the end of each cast. All measurements of the pH and total alkalinity were made at 25.0 ± 0.10 °C, where the samples were placed in the water bath for 10–20 min before measurements. The pH-meter used was an Orion Model 801 digital pH/mv meter. The precision was tested in the laboratory during the preparation for the cruise, and the precision (2r) of the measurements was ±0.01 pH. Total alkalinity of each sample was determined by the single-acid addition procedure described by Anderson and Robinson (1946) and developed by Culberson et al. (1970). The equation used by Culberson et al. (1970) is: TA ¼

1000 1000 aH Va Na ðVsw þ Na Þ Vsw Vsw cH

ð3Þ

TA is total alkalinity in meq kg−1 at 25 °C, Vsw is the volume of the seawater in ml, Va and Na are the volume and the normality of the acid, respectively, and aH = 10–pH. The activity coefﬁcient of hydrogen, cH in the NBS scale is 0.741 at 25 °C for salinity between 30 and 41‰ (Culberson et al. 1970). The precision was ±0.009 meq kg−1 for total alkalinity and reasonably good compared to the well-known Gran titration method (Gran 1952), which was reported to be 0.006 meq kg−1 (Rushdi et al. 1998).

Data Manipulation The degrees of saturation, X, of seawater with respect to calcite and of aragonite are deﬁned as the ratios of the ionic products of the concentrations of calcium and carbonate at in situ temperature, salinity and pressure to the solubility products, Ksp, of calcite and of aragonite under the in situ conditions. Thus, the degree of saturation is: X¼

ðCa2 þ ÞðCO2 3 Þ Ksp

ð4Þ

When X > 1, seawater is supersaturated with respect to calcite or aragonite, and seawater is undersaturated with respect to calcite and aragonite when X < 1. Seawater is considered saturated with calcite and aragonite when X = 1. The calcium concentration (Ca2+) in seawater varies by less than 1.5%. Thus, the calcium-to-salinity ratio in seawater (Culkin and Cox 1966) was used to estimate the calcium concentration. The carbonate ion (CO−2 3 ) concentration in seawater is calculated from: ðCO2 3 Þ¼

=

CAK2

ð5Þ

=

ðH þ Þ þ 2K2

=

where CA is carbonate alkalinity in meq kg−1, and K2 is the second dissociation constant of carbonic acid in seawater

174

A. I. Rushdi et al.

estimated from the equation of Mehrbach et al. (1973). CA is calculated using the expression: þ CA ¼ TA ðBðOHÞ 4 Þ ðOH Þ þ ðH Þ

¼ TA

TBðH þ Þ = ðH þ Þ þ KB

Kw= þ ðH þ Þ ðH þ Þ

ð6aÞ ð6bÞ

where TB = (B(OH)3 + ðBðOHÞ 4 Þ = 0.237 x (Chlorinity) =

obtained from Culkin (1965), KB is the dissociation constant of borate and estimated from Lyman (1956) and Dickson (1990), and Kw= is the dissociation constant of seawater obtained from Culberson and Pytkowicz (1973). The apparent dissociation solubility products of calcite and aragonite are based on the work of Mucci (1983). Finally, the degree of saturation is calculated by Eq. (4).

Results and Discussion Levels, Profiles and Distributions of Salinity, TA, pH and Saturation States of Calcite and Aragonite The measured values of air and surface seawater temperatures, salinity, TA, pH and the calculated saturation states of seawater samples with respect to calcite and aragonite are shown in Table 10.1. The distribution proﬁles of the different measured parameters are shown in Fig. 10.2. The measured parameters, their proﬁles and their spatial variations are discussed below. The air temperatures were recorded to be generally similar to the seawater surface temperatures and ranged from 25.5 to 27.5 °C. The seawater surface temperatures at 37.10‰ in the north at the stations 1 and 2, as shown in Figs. 10.2b and 10.3b. The general trends of the temperature and salinity (Fig. 10.3) indicated that both surface and deep-water circulation systems influenced the temperature and salinity distribution pattern. The surface temperature and salinity distributions were likely affected by

the influx of the surface water current with salinity similar to that of the Gulf of Aden from the south, and the deeper water current from the north with a temperature (low) and salinity (high) similar to the sinking surface water near the Suez Canal in the north (Siedler 1969; Morcos 1970). The two types of water masses are illustrated in Fig. 10.4a, where the low salinity and high temperature surface, and high salinity and low temperature water masses are shown. The surface water temperature shows a positive relation with salinity (Fig. 10.4b), likely caused by water evaporation at relatively higher temperatures. The temperature of the deeper waters, on the other hand, shows a negative correlation with salinity (Fig. 10.4c) indicating that colder waters are more saline (heavier) forming bottom water masses. The pH values of the surface seawater varied from 7.983 to 8.198 and showed a slight increase from south to north for the shoreline seawaters (Table 10.1). They obviously decrease with depth to a minimum (8.052–7.960) at *100 m depth for offshore seawaters as shown in Figs. 10.2c and 10.3c. The highest pH values of surface seawaters are shown between stations 4, 5 and 6, similar to the temperature distribution pattern. The measured pH values showed a positive correlation with surface seawater temperatures (Fig. 10.5a). This was likely attributed to dissolution of highly soluble carbonate minerals such as high magnesian calcite (Rushdi et al. 1994) that decreased the CO2(l) in the solution according to the following reaction: Mgx Ca1x CO3ðsÞ þ CO2ðlÞ þ H2 O $ xMg þ ð1 xÞCa2 þ þ 2HCO 3

ð7Þ

Thus, the dissolution of calcium carbonate likely caused the increase in the pH values of the seawater solutions, while re-precipitation of pure calcite and low magnesian calcite caused the decrease in the pH values. The pH also showed a negative correlation with the measured salinity of seawater (Fig. 10.5b), indicating that the pH of seawater is a non-conservative parameter. The trends of pH changes with temperature and salinity values might indicate that mainly physical, chemical and biological processes influenced the distribution of pH during early winter in this area. Total alkalinities were found to range from 2.3268 to 3.6159 meq kg−1 in surface seawaters and slightly increased toward the north and offshore (Figs. 10.2d and 10.3d). Lower alkalinity was observed around the stations 4 and 6 (Fig. 10.3d), possibly as a result of high organic matter oxidization. For offshore stations, it slightly changed with depth as shown in Fig. 10.3d. Total alkalinity (as normalized total alkalinity, NTA) did not show any correlation with the increase of seawater temperature and salinity changes (Fig. 10.5c and d) supporting the non-conservative property of alkalinity.

10

Calcite and Aragonite Saturation Levels of the Red Sea …

Table 10.1 The hydrographic data and parameters measured along the Red Sea coast of Yemen

Station no. 1

2

3

4

5

6

7

8

175

Air temp

Depth

Water temp

(°C)

(m)

(°C)

0

27.0

37.36

10

27.0

25

26.9

30 0

26.50

27.00

27.00

25.50

25.50

27.50

27.50

25.00

Salinity

pH

TA

X

(meq kg−1)

Calcite

Aragonite

8.181

3.6159

8.52

5.67

37.41

8.164

2.8355

6.41

4.28

37.30

8.189

3.7826

8.96

6.00

27.0

37.34

8.168

2.7876

6.30

4.23

26.0

37.10

8.181

3.2471

7.43

4.92

10

26.0

36.98

8.181

2.6187

5.92

3.93

25

26.0

37.15

8.198

2.5685

5.96

3.98

50

25.9

37.18

8.189

2.7106

6.15

4.13

100

25.9

37.24

8.181

2.9659

6.57

4.48

0

26.7

37.07

8.113

2.3806

4.84

3.21

10

26.7

36.82

8.164

2.3489

5.20

3.46

25

26.6

37.06

8.181

2.3263

5.28

3.53

0

26.6

37.50

8.147

2.3806

5.16

3.43

10

26.6

37.48

8.151

2.3489

5.11

3.40

25

26.5

37.55

8.164

2.3461

5.19

3.47

30

26.3

37.50

8.131

2.3268

4.82

3.23

50

26.1

37.34

8.181

2.3370

5.23

3.52

75

25.4

37.50

7.989

2.3952

3.68

2.49

100

22.0

40.27

7.960

2.3806

3.27

2.21

150

21.8

40.34

7.985

2.4581

3.48

2.39

200

21.7

40.35

7.960

2.5402

3.38

2.35

0

26.4

36.32

8.155

2.3867

5.15

3.42

10

26.1

36.80

8.077

2.4376

4.55

3.02

25

26.0

37.49

7.983

2.3879

3.74

2.50

0

26.8

37.27

8.214

2.3669

5.77

3.84

10

26.8

37.38

8.180

2.3554

5.41

3.61

25

26.5

37.40

8.168

2.3330

5.19

3.47

50

26.5

37.50

8.207

2.3975

5.68

3.82

75

26.1

37.39

8.189

2.3450

5.28

3.58

100

22.1

40.28

8.052

2.4082

3.96

2.68

150

22.0

40.31

8.018

2.4186

3.67

2.52

0

25.7

36.40

8.168

2.4496

5.34

3.53

10

25.7

36.32

8.087

2.4208

4.53

3.01

25

25.7

36.32

8.155

2.3806

5.02

3.35

0

25.9

36.49

8.134

2.4453

5.04

3.34

10

25.9

36.55

8.172

2.3370

5.13

3.41

25

25.7

36.55

8.164

2.3915

5.14

3.43

The saturation levels of seawater surface layers ranged from 5.11 (511%) to 8.52 (852%) with respect to calcite and from 3.40 (340%) to 5.67 (567%) with respect to aragonite (Table 10.1). The levels of supersaturation with respect to both calcite and aragonite increased from south to north, where the highest degrees of supersaturation were

recorded near Kamaran Island and extended along the shore-line (Fig. 10.3). The supersaturation levels of both minerals decreased with depth and reached the minimum (3.27 for calcite and 2.21 for aragonite) at depths below 100 m. They showed slight increases with an increase of temperature and a decrease with the increase of salinity for

176

A. I. Rushdi et al.

Fig. 10.2 Plots showing the distribution proﬁles of a seawater temperature, b seawater salinity, c pH values, d total alkalinity, e calcite degree of saturation and f aragonite degree of saturation

(a)

(c)

Station 2

4

6

5

7

8

4

6

7

5

Z (m)

Z (m)

150 200

200

Ω (Calcite) 250

250

250

6

4

5

7

8

0

0

0

50

50

50

Z (m)

150

150

150

Z (m)

100

100

100

Z (m)

7.4

7.1

6.8

6.5

6.2

5.9

5.6

Station 2

8

5.3

5

7

200

200

200

TA (meq kg-1)

Salinity

Ω (Aragonite)

250

250

250

4.6

4.8

4

4.4

4.2

3.6

3.8

3

3.4

3.2

2.8

2.4

2.2

2.6

3

3.14

2.93

3.07

2.72

2.86

2.79

2.51

2.58

2.65

2.3

2.37

2.44

40

38.8

39.2

39.6

38

38.4

37.2

37.6

36

36.4

36.8

calcite, and decreases with both salinity and temperature for aragonite, as shown in Fig. 10.6. This might be due to dissolution of high magnesian calcite and re-precipitation of aragonite and low magnesium calcite as mentioned above. Recent studies show that the seawater degrees of saturation states with respect to carbonate minerals in tropical seas control the formation and distribution of biogenic and

4.7

5

4.4

6

4.1

4

3.8

3.2

(f)

Station

2

3.5

8.2

8.14

8.17

8.11

8.08

8.05

8.02

8

7.99

(d) 7

7.96

26.5

26

25.5

25

24.5

24

23

22.5

23.5

22

21.5

5

8

100

150

200

6

7

5

pH

Station 4

6

50

100

150

2

4

0

50

100

T (oC)

(b)

Station 2

8

0

50

Z (m)

(e)

Station 2

0

Fig. 10.3 Cross sections showing the spatial distribution pattern of a seawater temperature, b seawater salinity, c pH values, d total alkalinity, e calcite degree of saturation and f aragonite degree of saturation

inorganic calcium carbonate (Kleypas et al. 1999; Broecker et al. 2001). The decrease of the seawater supersaturation, as a result of the increase of atmospheric CO2, shows a decrease in calcium carbonate formation by calcifying organisms such as foraminifera, pteropods and planktonic larvae of echinoderms (Comeau et al. 2009; Clark et al. 2009; Lombard et al. 2010; Müller et al. 2010). Less is known about the types and distribution of calcifying

10

Calcite and Aragonite Saturation Levels of the Red Sea …

177

Fig. 10.4 Temperature/salinity plots showing the different types of water masses, for a surface and deep seawaters, b surface seawaters, and c deep seawaters

plankton in the southern part of the Red Sea. The types of reefs observed in the study area were patch reefs of small separated hill-like reefs and solitary corals that occurred at regular intervals (Rushdi et al. 1994; Kotb et al. 2004). Shallow water bottom reef and hard substrates were observed south of Kamaran Island. It was also noticed that coral fragments are washed on to the shore in most areas (Rushdi et al. 1994). Generally, the distributions of coral reefs (patch reefs and solitary corals) followed the high degree of saturation of aragonite and calcite, where the dense

patches of coral reefs were found around Kamaran Island and north of as-Salif Village (Rushdi 2012). In other words, the highest densities of coral reefs were found where a high degree of saturation occurs. Based on the experimental results obtained by Rushdi et al. (1992), high magnesian calcite (>12 mol% MgCO3) is expected to dissolve under the saturation levels recorded in this study. Low magnesian calcite (100 m, where the total alkalinity slightly decreased with depth. The surface seawaters were supersaturated with respect to calcite and aragonite and ranged from 511% to 852% and from 340% to 567% for calcite and aragonite, respectively. They decreased with depth for offshore seawaters and reached minima at >100 m depths.

A. I. Rushdi et al.

The projected effect of the pH decrease as a result of excess atmospheric CO2 emission is prominent and can affect the growth and distribution of coral reefs and associated ecosystems in the coastal region of Yemen. For scientiﬁc and economic reasons, further studies of the distribution, mineralogy and types of coral reefs as well as the physical and chemical parameters that affect their presence, distribution, and growths, including other calcifying organisms, are needed for the Red Sea coast of Yemen.

Supplementary Material The following reactions take place when carbon dioxide dissolves in seawater: H2 O

CO2ðgÞ $ CO2ðlÞ

ðMS1Þ

CO2ðlÞ $ H2 CO3

ðMS2Þ

H2 CO3 $ H þ þ HCO 3

ðMS3Þ

þ 2 HCO 3 $ H þ CO3

ðMS4Þ

In the presence of calcium carbonate (CaCO3(s)) mineral, the following reaction occurs: CaCO3ðsÞ ¼ Ca2 þ þ CO2 3

ðMS5Þ

Acknowledgements The authors thank Prof. C-T. A. Chen and anonymous reviewers for the suggestions and remarks that improved the quality of the chapter.

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A. I. Rushdi et al. Rushdi AI (2012) Calcite and aragonite saturation states of Kamaran Strait surface seawater, Yemen: summer time. Arabian J Geosci 5:1093–1102 Rushdi AI (2015) Calcite and aragonite saturation states of the Red Sea and biogeochemical impacts of excess carbon dioxide. In: Rasul NMA, Stewart ICF (eds) The Red Sea: the formation, morphology, oceanography and environment of a young ocean basin. Springer Earth System Sciences, Berlin, pp 267–280 Rushdi AI, Abubakr MM, Hebba HMA (1994) Marine habitats of the Red Sea at AlUrj-Alsalif and Dhubab-Yaktul areas: their ecology, environment and management recommendations preliminary investigations. Faculty Sci, Sana’a University, Yemen, p 117 Rushdi AI, Chen C-TA, Suess E (1998) The solubility of calcite in seawater solution of different magnesium concentrations at 25 °C and 1 atm total pressure: a laboratory re-examination. La Mer 36:9– 22 Rushdi AI, Pytkowicz RM, Suess E, Chen CT (1992) The effects of magnesium-to-calcium ratio, in artiﬁcial seawater at different ionic products, upon the induction time, and the mineralogy of calcium carbonate: a laboratory study. Geol Rundsch 81:571–578 Santana-Casiano JM, González-Dávila M, Rueda M-J, Llinás O, González-Dávila EF (2007) The interannual variability of oceanic CO2 parameters in the northeast Atlantic subtropical gyre at the ESTOC site. Glob Biogeochem Cycles 21:GB1015 Schlager W, James NP (1978) Low-magnesian calcite limestones forming at the deep-sea floor, tongue of the ocean, Bahamas. Sedimentology 25(5):675–702 Schneider K, Erez J (2006) The effect of carbonate chemistry on calciﬁcation and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293 Siedler G (1969) General circulation of water masses in the Red Sea. In: Degens ET, Ross DA (eds) Hot brines and recent heavy metal deposits in the Red Sea. Springer, Berlin, pp 131–137 Silverman J, Lazar B, Erez J (2007) Effect of aragonite saturation, temperature, and nutrients on the community calciﬁcation rate of a coral reef. J Geophys Res Oceans 112:C05004 Silter WV, Be AWH, Berger WH (1975) Dissolution of deep-sea carbonates. In: Special Publication no. 13. Cushman Foundation for Foraminiferal Research Simkiss K (1964) The inhibitory effects of some metabolites on the precipitation of CaCO3 from artiﬁcial and natural seawater. ICES J Mar Sci 29:6–18 Smith AD, Roth AA (1979) Effect of carbon dioxide concentration on calciﬁcation in the Red coralline alga Bossiella orbigniana. Mar Biol 52:217–225 Smith SV, Pesret F (1974) Processes of carbon dioxide flux in the Fanning Island Lagoon. Paciﬁc Sci 28:225–245 Soﬁanos SS, Johns W, Murray SP (2002) Heat and freshwater budgets in the Red Sea from direct observations at Bab el Mandab. Deep Sea Res II 49:1323–1340 Suess E (1973) Interaction of organic compounds with calcium carbonate. Geochim Cosmochim Acta 34:157–168 Sun W, Jayaraman S, Chen W, Persson KA, Ceder G (2015) Nucleation of metastable aragonite CaCO3 in seawater. Proc Natl Acad Sci 112(11):3199–3204 Suzuki A, Nakamori T, Kayanne H (1995) The mechanism of production enhancement in coral reef carbonate systems: model and empirical results. Sediment Geol 99:259–280 Takagi Y (2002) Otolith formation and endolymph chemistry: a strong correlation between the aragonite saturation state and pH in the endolymph of the trout otolith organ. Mar Ecol Prog Ser 231:237– 245 Takahashi T (1975) Carbonate chemistry of seawater and the calcite compensation depth in the ocean. In: Dissolution of deep-sea

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Geochemistry and Life at the Interfaces of Brine-Filled Deeps in the Red Sea

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André Antunes, Stein Kaartvedt and Mark Schmidt

Abstract

The deep-sea brines of the Red Sea are unusual extreme environments and form characteristically steep gradients across the brine-seawater interfaces. Due to their unusual nature and unique combination of physical-chemical conditions these interfaces provide an interesting source of new ﬁndings in the ﬁelds of geochemistry, geology, microbiology, biotechnology, virology, and general biology. The current chapter summarizes recent and new results in the study of geochemistry and life at the interfaces of brine-ﬁlled deeps of the Red Sea.

enrichment of regular seawater in salt, heavy metals, and temperature. These brines accumulate in the deeps due to their higher density and, as a result of their stability, form characteristically sharp transition zones with seawater. These brine-seawater interfaces provide an unusual variety of physical-chemical conditions, which has attracted considerable interest from geologists and geochemists. Likewise, they also provide a wide range of environmental niches, which contribute to an impressive diversity of exotic new microbes and potential applications.

The Red Sea Brines and Their Geochemistry Introduction Although sometimes perceived as a mere narrow inlet of the Indian Ocean, the Red Sea is a unique and unusual water body unlike any other on our planet. This landlocked marine ecosystem is one of the warmest and saltiest seas and provides an ideal setting to study several relevant geological and biological processes. Noteworthy among the several different sites within the Red Sea are its deep-sea brines, which are a unique type of environment, combining multiple extremes. These topographical depressions were formed as a direct result of the tectonic splitting of the Arabian and the African plates. The same process also exposed evaporite layers from the Miocene, which underlie the Red Sea basin, allowing for the A. Antunes (&) Department of Biology, Edge Hill University, St. Helens Road, Ormskirk, Lancashire, L39 4QP, UK e-mail: [email protected] S. Kaartvedt Department of Biosciences, University of Oslo, Blindern, 0316 Oslo, Norway M. Schmidt GEOMAR Helmholtz, Centre for Ocean Research Kiel, Wischhofstr. 1-3, 24148 Kiel, Germany

Part of the geochemical data presented in this section summarizes yet unpublished results from the brine-seawater interfaces of selected Red Sea deeps. Geochemical data were derived from the joint German-Saudi-Egyptian-Sudanese research projects conducted during the last 15 years (e.g., www.jeddah-transect.org). These geochemical and hydrographic data were obtained during research cruises M44/3 and M52/3 (Pätzold et al. 2000 and Pätzold et al. 2003, respectively), P408-2 (Schmidt et al. 2011), and 64PE350-1 (Schmidt et al. 2013). Hydrographic data (i.e., water depth, temperature, light transmission) were recorded using a Sea and Sun-CTD which was built and calibrated for ambient temperatures of up to 80 °C. Water and brine was sampled by using 10 L Niskin-Rosette Water Samplers and an Interface Water Sampler. For further sampling and analytical procedures refer to Schmidt et al. (2015).

Geochemistry of the Brine-Seawater Interface The brine-seawater interface can be found at different depth levels in brine-ﬁlled Red Sea deeps (e.g., Hartmann et al. 1998). However, temperature/density gradients and thus thickness of the interface can vary drastically (e.g., Schmidt et al. 2003).

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_11

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Fig. 11.1 Brine-seawater interfaces of a the Discovery Deep; b Port Sudan Deep; and c Atlantis II Deep indicated by temperature proﬁles (red) and light transmission (black) data in 2012. The variable

environmental niches are categorized as 10 °C temperature steps from warm (Red Sea bottom water temperature) to hot (hydrothermal) conditions

The lowest brine bodies are remarkably stable and homogenous, mixing sparingly with the overlying seawater, and can form very sharp transition zones of less than 30 cm to 2 m thickness of the brine-seawater interface (Pätzold et al. 2003). Most of the brine-ﬁlled Red Sea Deeps exhibit brine-seawater interfaces like the Port Sudan Deep, of 1–2 m thickness and where density (salt content) increases from 1.025 to 1.2 g cm−3 and temperature increases from about 22 °C to >23 °C (Fig. 11.1b; Schmidt et al. 2015). However, the brine-seawater interface of the Discovery Deep extends to several tens of metres (Fig. 11.1a). Overspill or lateral (porewater) migration is regarded as a possible reason for the

shape of the Discovery brine-seawater interface (e.g., Hartmann et al. 1998; Schmidt et al. 2003). The exchange of heat and salt between brine and seawater in Red Sea deeps is, in general, mainly controlled by diffusive transport (Anschutz et al. 1999). Moreover, heating from below creates brine layer systems like the Atlantis II Deep, which exhibits several brine layers separated by strong temperature and density steps (Fig. 11.1c). The main steps are modulated by small cm-sized staircases when looking at the microstructure of the brine-seawater interface, for example, of the Atlantis II Deep (Albarakati et al. 2016; Swift et al. 2012). The brine-seawater interface, which is a

Fig. 11.2 Physical and chemical proﬁles at the brine-seawater interface of brine-ﬁlled northern basin of the Shaban Deep

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strong physical density boundary, creates a kind of sedimentary trap within the water column. Particle aggregation at the respective water depths, either by sedimentation or due to biogeochemical cycles is indicated by a strong decrease of light transmission due to turbidity increase at the brine-seawater interfaces (Fig. 11.1 a–c). The turbidity increase may be attributed to (bio)geochemical redox cycles, for example, iron or manganese precipitation (e.g., Scholten et al. 2000; Anschutz 2015), particle sedimentation, that is, marine planktonic sedimentation (e.g., Seeberg-Elverfeldt et al. 2004), or microbial growth (e.g., Eder et al. 2001, 2002; Botz et al. 2007; Abdallah et al. 2014). Drastic changes in environmental conditions and the formation of steep physical and chemical gradients (e.g., density, temperature, Eh) along the brine-seawater interface are observed in all brine-ﬁlled deeps of the Red Sea (e.g., Schmidt et al. 2003, 2015). As an example, the sulfur and carbon species and potential electron acceptor proﬁles of the brine-seawater interface are shown for the northern basin of the Shaban Deep in Fig. 11.2. We should note that several biogeochemical studies point to a probable microbial input in the geochemistry of the brines, particularly associated with these local geochemical cycles occurring at the chemoclines of the brine-seawater interface (reviewed by Antunes et al. 2011b). Transport/reaction calculations demonstrated that mass transport across the brine-seawater interface is not only

Fig. 11.3 Redox-sensitive processes, i.e., Fe(III)-reduction and Mn(IV)-precipitation at the brine-seawater interface are indicated by the deviation of measured Mn(II)- and Fe(II)concentrations from theoretical brine/seawater mixing composition (Shaban Deep). In situ ﬁlter samples of upper (left) and lower (right) part of the brine-seawater interface from the northern basin of the Shaban Deep covered with less than 3% TOC and amorphous Mn(IV)and Fe(III)-(hydr)oxides (H. Wehner, pers. comm.) support this idea

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controlled by diffusion but is also influenced by secondary biogeochemical formation/degradation and inorganic redox-cycles (Schmidt et al. 2003). Methanotrophic aerobic bacteria are found at the brine-seawater interfaces (Abdallah et al. 2014); however, potential electron acceptors for methane oxidation are, for example, Mn(IV), Fe(III)-oxides, and sulfate when oxygen is depleted (Fig. 11.2). In situ ﬁltration experiments within the brine-seawater interface of the Shaban Deep showed that large amounts of total Fe and total Mn can be found as amorphous Mn(IV)- and Fe(III)-(hydr) oxides within the brine-seawater interface (Fig. 11.3). Manganese and iron reduction coupled to bacterial methane oxidation is already described for other environmental niches (Beal et al. 2009), and molar quantities of these electron acceptors exceed methane concentrations within the brine-seawater interfaces by several orders of magnitude (Fig. 11.2). This could enable metal-oxides as potential redox-partners for methane oxidation in the brine-seawater interface, even when standard reaction stoichiometry and thermodynamic energy gain are considered (Schmidt et al. 2003). The d13C-CH4 proﬁle reaches a d13CCH4-maximum of up to −7‰ within the brine-seawater interface of Shaban Deep (Fig. 11.2). Such 13CCH4 enrichment in residual methane may indicate microbial methane oxidation processes within the interface (e.g., Whiticar and Faber 1986). However, an increase of DIC (dissolved inorganic carbon) concentration and related negative shift of d13C-DIC in the

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brine-seawater interface (Fig. 11.2) cannot only be attributed to methane oxidation. Microbial organic matter degradation is probably the dominant source for the DIC increase, d13C-DIC decrease, and pH decrease in the brine-seawater interface of the Shaban Deep, where also admixture of magmatic CO2 cannot be ruled out (Botz et al. 2011).

Microbiology of the Brine-Seawater Interface The 1960s: Early Studies The detection of brines at the bottom of the Red Sea led to almost immediate extensive surveys, focusing on geological and geochemical analysis (e.g., Degens and Ross 1969; Antunes et al. 2011b). This is in stark contrast with studies on microbiology of these locations, which received very little attention for an extended period of time. The ﬁrst microbiological surveys focused on brine samples from Atlantis II and swiftly declared them sterile due to the harshness of local environmental conditions (Watson and Waterbury 1969). More encouraging results were obtained with samples from the brine-seawater interface of Atlantis II, with the reported isolation of a Desulfovibrio strain that, unfortunately, has never been fully characterized (Trüper 1969).

The 1990s–2000s: Molecular-Based Surveys After a signiﬁcant gap in microbial exploration of the brines, the 1990s brought the isolation and description of Flexistipes sinusarabici as well as the ﬁrst molecular-based studies. Flexistipes sinusarabici was isolated from the Atlantis II brine-seawater interface and is a moderate thermophile, probably thriving on organic matter that accumulates at the interface (Fiala et al. 1990). During this period, data from the ﬁrst molecular-based studies, originally focusing on brine-seawater interface samples, drastically shifted our perception of the brines and revealed that they were teeming with rich and very diverse microbial communities, which included several new sequence groups with no close relatives (Eder et al. 1999, 2001, 2002). Some of these new phylogenetic groups (e.g., the KB1 group) seemed to be particularly well adapted to these locations as they were consistently detected in multiple brine pools, including some similar environments in the Mediterranean (e.g., Antunes et al. 2011b; van der Wielen et al. 2005).

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including representatives from new higher ranked taxa, both from the brine-seawater interface (Antunes et al. 2003, 2007; Eder et al. 2001) and the brine-sediment interface (Antunes et al. 2008a, b) of several different deeps. Within the microbes described during this period, Salinisphaera shabanensis is one of the most interesting (Fig. 11.4). S. shabanensis was isolated from the brine-seawater interface of Shaban Deep and represented a new species, genus, family, and order within the class Gammaproteobacteria (Antunes et al. 2003, 2017a; Vetriani et al. 2014). This organism has a remarkable physiological flexibility with broad growth ranges for oxygen, temperature, NaCl, hydrostatic pressure and also, to a lesser degree, pH (Antunes et al. 2003). This was seen as an adaptation to life at the gradient-rich environment provided by the brine-seawater interface. Another microbe isolated from the same location was Marinobacter salsuginis, which represented a new species also within the class Gammaproteobacteria (Antunes et al. 2007). An interesting feature of this organism was its ability to oxidize ferrous iron, which would link it with the complex redox cycles occurring at the brine-seawater interface (e.g., Scholten et al. 2000; Anschutz 2015). Furthermore, Eder et al. (2001) succeeded in isolating two strains, representing new species within the genus Halanaerobium. The strains, isolated from the brine-seawater interface of Kebrit Deep, grew chemoorganotrophically and between 5 and 34% NaCl. Members of the Halanaerobiales were postulated to contribute signiﬁcantly to the anaerobic degradation of organic matter enriched at the interface of Kebrit Deep, particularly as they seemed to be one of the main groups of sequences found in these samples (Eder et al. 2001). Unfortunately, and despite the fact that we have signiﬁcant information on their general

The 2000s: Cultivation Success Additional sampling and cultivation-based efforts in the early 2000s succeeded in isolating several new microbes,

Fig. 11.4 Transmission electron micrograph of a dividing Salinisphaera shabanensis cell. Bar, 1 µm. Reprinted from Antunes et al. (2003), with permission from Springer

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characteristics, these two strains have never been fully described.

The 2010s: Wider Exploration and -Omics The 2010s provided wider exploration opportunities with several new expeditions and sampling opportunities (Antunes 2017). This period also coincided with further molecular-based studies, genomics, and metagenomics. Metagenomics of samples from the Red Sea brines offered some new insights into local microbial communities, and speciﬁc physiological groups. Bougouffa et al. (2013) studied Atlantis II and Discovery and reported on the vertical stratiﬁcation of microbial communities in these locations. This study also reported on similarity in dominant groups both in deep-sea water overlying the brine (dominated by Alphaproteobacteria and Marine Group I Thaumarchaeaota) and, unexpectedly, in the brine (dominated by Gammaproteobacteria and the Euryarchaea). Temperature and salinity were suggested as the main driving influences in shaping these communities, which displayed higher abundances but lower diversity in the interfaces than in the lower convective layers. Later studies revealed that the thaumarchaeal ammonium oxidizing genus Nitrosopumilus was a major player in the brine-seawater interface (Ngugi et al. 2015), as frequently observed in other deep-sea locations. However, the dominant phylotype (BSA3), which accounted for >98% of all sequences, was distinct from other bathypelagic thaumarchaea and revealed a series of speciﬁc adaptations mostly linked to osmo-adaptation (Ngugi et al. 2015). A recent study reported on another key player in the nitrogen cycle of the brine-seawater interface and described the Nitrospina-like Candidatus “Nitromaritima” (Ngugi et al. 2016). These bacteria can constitute up to one third of the bacterial 16S rRNA gene sequences at the brine-seawater interface of Atlantis II, values which are unexpectedly high, and pointed to these interfaces constituting potential “hotspots” for Nitrospinae (Ngugi et al. 2015, 2016). Additional molecular-based surveys have focused on speciﬁc physiological groups within the brine-seawater interfaces. Noteworthy examples include the studies on aerobic methanotrophic communities in Atlantis II, Discovery, and Kebrit (Abdallah et al. 2014), and on methanogens and sulfate reducers present in the same locations, as well as Erba and Nereus (Guan et al. 2015). The ﬁrst study showed a high diversity of aerobic methanotrophs, particularly pronounced at Atlantis II, while the latter study conﬁrmed low numbers but high diversity of methanogens and sulfate reducers in all studied locations, with a higher distinctiveness of samples from Kebrit. More recent studies have also signiﬁcantly improved our knowledge on the metabolism and characteristics of

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uncultivated groups that are typical of these deep-sea brines (e.g., the bacterial KB1 group and the euryarchaeal MSBL1 group; Yakimov et al. 2013; La Cono et al. 2015; Nigro et al. 2016; Mwirichia et al. 2016), namely by exploiting single-cell genomics. Members of the KB1 appear to be able to import glycine betaine for osmotic regulation, but might also use it as carbon and energy source (La Cono et al. 2015; Nigro et al. 2016). Rather than being methanogens (as originally proposed; van der Wielen et al. 2005) members of the MSBL1 group seem to be comprised of sugar-fermenting organisms capable of autotrophic growth (Mwirichia et al. 2016). During this period, some application-driven studies, and whole-genome sequencing projects have focused on additional isolates from the brine-seawater interface of Atlantis II, Erba, Discovery, Kebrit, and Nereus (Sagar et al. 2013a, b; Zhang et al. 2016a, b). Unfortunately, these new isolates, which include strains related to the genera Cromohalobacter, Halobacillus, Halomonas, Idiomarina, Marinobacter, Pseudoalteromonas, Sediminimonas, Sulﬁtobacter, Thiomicrospira, and Zunongwangia, have not yet been fully described.

Potential Biotechnological Applications The bio-prospection of microbes, particularly those living in extreme environments, has been receiving considerable attention, and is frequently lauded as the solution to society’s biggest challenges: Feeding, Fueling, and Healing the World (e.g., Antunes et al. 2017b; Yin et al. 2015). The unique combination of extreme environmental conditions found in each brine of the Red Sea, and their unique microbial communities makes them privileged targets for the discovery of new biomolecules. Fittingly, several microbes from the Red Sea brines have an interesting set of genes and physiological capabilities, which might be relevant for biotechnological applications. Salinisphaera shabanensis has been reported to accumulate very high-concentrations of ectoine and betaine (Antunes et al. 2003), degrade oil-derived compounds (Alam et al. 2013), detoxify metals (Antunes et al. 2011a), and produce poly-b-hydroxybutyrate. These capabilities suggest a wide range of potential applications as diverse as bioremediation and bioleaching, production of compatible solutes (used as stabilisers and stress-protective agents), and production of sustainable and eco-friendly bio-plastics. Marinobacter salsuginis, also isolated from the same location, oxidises ferrous iron and can degrade several oil-derived compounds, suggesting potential application in bioremediation (Antunes et al. 2007). More recently, Sagar et al. (2013a, b) surveyed the capability of several new isolates from the brine-seawater

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interface to produce cytotoxic and apoptotic molecules. Results from these studies have also shown some very promising results, particularly against cancer cell lines.

The Red Sea Brines and Their Viral Communities Exploration of data from metagenomics provided the ﬁrst insights into the viral communities living in the brines of the Red Sea (Antunes et al. 2015). This study showed that viral communities are diverse and distinct from each other, but generally dominated by dsDNA viruses (Caudovirales), with a high number of unclassiﬁed viruses in Atlantis II. Furthermore, and mirroring what has been observed for microbes, viral communities were shown to be stratiﬁed across the brine-seawater interface. As these authors pointed out, further studies focusing on the viruses of the brines, supported by proper, dedicated sampling for virology studies, are still lacking and should represent one of the main targets for future expeditions.

Macro-Fauna of the Brine-Seawater Interface The extreme environmental conditions present in the brines prevent metazoans from inhabiting these ecosystems. However, enhanced abundance of macrofauna may occur in areas immediately adjacent to the brines, with various organisms taking beneﬁt of the microbial production originating in the pools or from symbiotic bacteria fueled by the vent environment. Such examples comprise dense beds of mussels with symbiotic bacteria along brine shorelines in the Gulf of Mexico (e.g., Cordes et al. 2009, 2010). Assessment of effects of the Red Sea brines on adjacent fauna is in its infancy. Earlier reports on macrofauna close to Fig. 11.5 Sea floor images at the margins of the brine pool of Valdivia Deep taken by an ROV. Apachecorbula appears as black coloured bivalves in (a) and as small black objects arranged in a narrow band in (b). Reprinted from Oliver et al. (2015), with permission from Cambridge University Press

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mid axial brine pools in the Red Sea appear limited to observations of holes in the sediment indicating burrowing polychaetes (Young and Ross 1974; Monin et al. 1982). Recently, a few studies have addressed the pelagic fauna at the brine-seawater interface as well as the benthic macrofauna surrounding brines. The starting hypotheses in these cases have been that - on the one hand - the extreme environment of the brines may affect the adjacent waters by making them inhospitable to most macroscopic life forms. Alternatively, the fauna at the brine-seawater interface might be enriched from taking advantage of the increased microbial production, or trapping of organic matter, at the surface of the brine-seawater interface (as discussed in the previous sections of this chapter). With respect to the pelagic fauna, the alternative hypotheses of avoidance or enrichment have been addressed at the brine-seawater interfaces of two very different brines, the Atlantis II and the Kebrit Deeps. Using a variety of tools, Kaartvedt et al. (2016) found that waters just above the brine pool of Atlantis II Deep (2000 m depth) were depleted of both zooplankton and other macrofauna, like ﬁsh. The authors suggested that the harsh environment of Atlantis II has a repellent effect, at least at close range. On the other hand, the pelagic fauna appeared to be enriched at the Kebrit Deep brine-seawater interface (1465 m). Indeed, video footage evidenced plankton and ﬁsh at the brine-seawater interface and submerged echosounders documented individuals apparently exploring the brine pool surface. Samples from horizontal and vertical net tows showed that concentrations of zooplankton increased toward the brine pool, being one order of magnitude higher than in waters above. The detected abundance of juvenile stages at the interface suggested local reproduction. In conclusion, it appeared that the Atlantis II Deep has a repellent effect on the pelagic fauna, at least at close range, whereas the microbial production at Kebrit Deep contributes to fueling the fauna in the water just above.

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Fig. 11.6 Shells of Apachecorbula muriatica. a– d Holotype, NMWZ. 2013.058.1. e–h Variations in outline and tumidity. Reprinted from Oliver et al. (2015), with permission from Cambridge University Press

Like zooplankton, macrofauna appeared depleted along the shores of Atlantis II (own unpublished results). The Red Sea is generally regarded as extremely poor in benthos (Monin et al. 1982; Pfannkuche 1993), but macrofauna was repeatedly observed in video records made along the rims of Kebrit (Vestheim and Kaartvedt 2016). Inactive sulfur chimneys along the rim of the brine had associated epifauna of sea anemones, polychaetes, and hydroids (Vestheim and Kaartvedt 2016). Furthermore, chimneys brought to the surface held a relatively abundant infauna consisting of polychaetes, gastropods and top snails. The species found at Kebrit included groups known to rely on chemosynthetic microbial symbionts or grazing on bacteria for their nutrition (Vestheim and Kaartvedt 2016).

The strongest evidence of macrofauna being fueled by production in a Red Sea brine appears from a study carried out at the Valdivia brine (1525 m). The fauna along the rim was assessed using a Remote Operated Vehicle (ROV), equipped with video cameras and sampling devices. A narrow band (*20 cm) of small clams along the rim was clearly associated with the pool (Fig. 11.5; Oliver et al. 2015), likely fueled by the local microbiota. The clams were collected and fully described as a new genus and species (Oliver et al. 2015; pictured in Fig. 11.6). The anatomy of this species suggests that it feeds on the scarce, yet brine-enriched microbes that the bivalves can ﬁlter out of the water just adjacent to the brine. Other characteristics of the clams suggest that food availability is still low. The

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functional morphology suggests that it is non-selective, likely a response to low food availability, which is also indicated by very low body mass (Oliver et al. 2015). There is no indication that this bivalve harbours chemosymbiotic bacteria. Even though the evidence appears unequivocal that the microbial production in the Valdivia brine translates to, and is exploited by adjacent macrofauna, this enrichment is much less exuberant than at brine sites in the Gulf of Mexico (Cordes et al. 2009, 2010). Also, the setting is very different, in that Cordes et al. describe sessile animals that live in shallow layers of brine found at the outer edges of larger pools or along shallow channels where interstitial brines are seeping through seafloor sediments. Furthermore, in contrast to the Red Sea, the bivalves in the Gulf of Mexico host methanotrophic endosymbionts in their gills, which are nourished by high concentrations of methane dissolved in brine. In conclusion, of the 25 brine pools along the central axis of the Red Sea, only 3 have been investigated regarding their potential effect on the immediately adjacent fauna. The lesson learnt so far is that as the brines differ in depths and chemical constituents, the adjacent fauna varies accordingly, displaying both avoidance and stimulation. The 22 brines remaining to be studied represent a wide variety of environments (Antunes et al. 2011b), with likely corresponding variations in their impact on the adjacent fauna. Overall, these intriguing and extreme environments set a fascinating scene for fundamental science and biological treasure hunting in the depths of the Red Sea.

Concluding Remarks The brine-ﬁlled deeps of the Red Sea are remarkable locations combining multiple unique geochemical conditions, multiple environmental extremes, and thriving populations of extremophiles. Recent research efforts have provided us with important new insights into the Geochemistry and Life in the brine-seawater interface, and very promising new ﬁndings. However, additional research is necessary focusing on new, as yet unstudied brine pools, and underexplored aspects (e.g., isolation of new microbes, viral communities, macrofauna, geomicrobiology), as well as potential biotechnological applications. Acknowledgements Most of the geochemical sampling and analytical work associated with the new data presented here has been conducted within the Jeddah-Transect Project (www.jeddah-transect.org). The collaboration of the Jeddah Transect Project between King Abdulaziz University and Helmholtz-Center for Ocean Research GEOMAR Kiel was funded by King Abdulaziz University (KAU) Jeddah, Saudi Arabia, under grant No. T-065/430-DSR. Moreover, geochemical data is presented which is based on interface sampling during RV Meteor cruises (ME44/3 and 52/3). Analytical support by D. Garbe-Schönberg,

A. Antunes et al. H. Erlenkeuser, and M. Böttcher was highly welcome.Overall, the work presented in this chapter is the outcome of several years of research in this ﬁeld. The authors are particularly indebted to former colleagues at the University of Regensburg, and at the Red Sea Research Center, Computational Bioscience Research Center, and the Coastal and Marine Resource Core Laboratory of the King Abdullah University of Science and Technology (KAUST). Part of the research presented here has been funded by the FCT (Fundação para a Ciência e a Tecnologia, Portugal), DFG (Deutsche Forschungsgemeinschaft, Germany), and SEDCO (Saudi Economic and Development Company, Saudi Arabia).

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Desalination of Red Sea and Gulf of Aden Seawater to Mitigate the Fresh Water Crisis in the Yemen Republic

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Angelo Minissale, Dornadula Chandrasekharam and Mohamed Fara Mohamed Al-Dubai

Abstract

By the year 2025 Yemen’s per capita water availability will be around 89 m3/year and the country will be highly water stressed. As a consequence, economic status of the farmers involved in qat (also referred as khat) cultivation, a product that supports 25% of the country’s GDP, will fall below the poverty line. With declining water table, the Mesozoic–Cenozoic aquifer of Yemen will be unable to support irrigation and the geothermal reservoir too will decline due to excessive withdrawal of water. A solution to this problem is to develop the geothermal resources around Damt and Dhamar to support desalination of the Red Sea and Gulf of Aden seawater to generate fresh water to contribute to the country’s food and energy security. Damt and Dhamar silicic volcanic sites have the potential to generate more than 134 106 kW of electricity. Fresh water generated through desalination using geothermal sources and wastewater treatment plants (WWTPs) will give the country food and energy security and reduce dependence on food imports.

Introduction The Yemen Republic, bordering the Gulf of Aden and the Red Sea, has a population of about 28 million (WM 2017). The country has a long coastline extending from the Arabian

A. Minissale (&) CNR-Italian Council for Research, Institute of Geosciences and Earth Resources, Via La Pira 4, 50121 Florence, Italy e-mail: [email protected] D. Chandrasekharam Indian Institute of Technology, Hyderabad, Telangana, India M. F. M. Al-Dubai Department of Earth and Environmental Sciences, Sana’a University, Sana’a, Republic of Yemen

Sea to the Red Sea, with half of the coastline bordering the Red Sea. This landmass has evolved along with the western Arabian Shield during the breakup of the Arabian–Nubian Shield (ANS) and has experienced several episodes of tectonic–magmatic surges that have given rise to the present-day grabens, horsts, drainage pattern and linear mountain ranges. Although the geographic area of Yemen is about 528,000 km2 (excluding the islands in the Red Sea; FAO 2009), only about 7% of this land area is cultivable (i.e., 36,960 km2). A large part of this cultivable land (*10%) is used for water intensive qat (also referred as khat) cultivation (FAO 2009). More than 52,000 wells draw groundwater to support irrigated farming, including qat cultivation. This is causing drastic depletion of the groundwater levels that is threatening the basic economy of the rural population that depends heavily on cash crops like qat (Alderwish and Dotteridge 1995; FAO 2009). Being a “rural economy crop”, qat cultivation is given more importance than other crops such as wheat, oats, vegetables and fruits. This is forcing the country to adopt virtual water trade (VWT) and import large volumes of food commodities, thereby threatening the food security of the country. However, the country has an option to ensure food and water security through desalination of Red Sea water using its huge geothermal energy resource. This will help the country to provide food and water security to the growing population for the next few decades. The evolution of the geothermal systems of Yemen, located along the eastern margin of the Red Sea, are coeval to the break-up of the Arabian–Nubian Shield (ANS) and subsequent volcanic and tectonic activity that accompanied the activation of the Red Sea rift 31 million years ago. The Mesozoic and Cenozoic formations, formed prior to the opening of the Red Sea, are the main source of groundwater supporting agriculture in Yemen. These aquifers became “steam heated” geothermal reservoirs, subsequent to the volcanic episodes that accompanied rifting.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_12

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Evolution of the Geothermal Systems in Yemen The split of the ANS at around 31 Ma gave rise to landmasses with similar geological and hydrogeological characteristics on either side of the Red Sea. The eastern part of the ANS is represented by the landmass that includes Saudi Arabia and the Yemen Republic. The initial process of ANS rifting was caused by an anomalous thermal regime around the SW part of Yemen, below the African landmass, now represented by Ethiopia. This anomalous thermal regime, caused by an uprising mantle plume, triggered the initial Red Sea rift, causing extensive volcanic activity over Yemen (represented by the Yemen volcanics) and Saudi Arabia (the Harrats) (Fig. 12.1), that lasted for about 1.5 Ma (Camp and Roobol 1992; Al-Amri 1994; Hofmann et al. 1997; Coulié et al. 2003; Bosworth et al. 2005; Chandrasekharam et al. 2015, 2016). The extensional regime along the Red Sea axis gave rise to the Red Sea rift axis, which is one of the youngest spreading axes in the world, with a rotational pivot around Egypt. Yemen experienced and continues to experience tectonic activity with associated basic and silicic volcanism, as evident from the 1937 eruption of the Dhamar Volcano and the emergence of silicic volcanic cones during the Quaternary period near Al Lisi, Damt and Isbil (Fig. 12.2). The Cenozoic volcanics covering a large part of SW Yemen overlie the productive regional sandstone and limestone aquifers hosted by the Mesozoic formations. The regional aquifers represented by the Mesozoic formations Fig. 12.1 Position of mantle plume and the evolution of the Yemen Traps (adapted from Bosworth et al. 2005; Chandrasekharam et al. 2015, 2016)

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evolved during the closure of the Tethyan Sea, which was a part of the East Gondwana Land or the Mozambique Ocean that existed between the west and east Gondwana landmasses during 700–850 Ma (Dalziel and Grunow 1992; Stern 1994). The geothermal province of western Yemen is represented by fault controlled thermal springs, and associated fumaroles and boiling pools. The surface temperature of the thermal waters range from 42 to 96 °C. Boiling pools and fumaroles are common around the younger silicic volcanoes (Fara et al. 1999; Minissale et al. 2007; Chandrasekharam et al. 2016). Copious travertine deposits are common around the volcanic centres. The adjacent active Red Sea spreading ridge and associated volcanic regime resulted in high heat flow (154 mW/m2) and geothermal gradient (77 °C/km) in this region. In the absence of a well-deﬁned drainage system in Yemen, the geothermal reservoirs are recharged by the groundwater occurring in the Mesozoic formations. This is evident from the anion signatures of the thermal and groundwater shown in Fig. 12.3. The contribution by the magmatic fluids to the geothermal systems is indicated by high SO4 components in both thermal and groundwater. This is supported by high He3/He4ratios (3.2) and high d13C (−4 to −8‰) in the thermal gases (Dowgiallo 1986; Fara et al. 1999; Mattash et al. 2005; Minissale et al. 2007). The Na–K–Mg geothermometers of Giggenbach (1988) and the reported high heat flow and geothermal gradient, together with the presence of a shallow magma chamber, strongly support high-temperature geothermal systems in

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Desalination of Red Sea and Gulf of Aden Seawater …

Fig. 12.2 Geological and tectonic features and volcanic centres along the western part of Yemen Fig. 12.3 Cl–SO4–HCO3 diagram (Giggenbach 1988) showing the similarities between aquifer waters and geothermal fluids (adapted from Chandrasekharam et al. 2016)

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Fig. 12.4 Development of regional graben formations during syn and post EAO (adapted from Albaroot et al. 2016 and Stern and Johnson 2010)

this region. Although the development of a 1 MWe pilot power plant around the Damt volcanic center was ﬁnalized, with the support of the UNEP, the project has been stalled due to current political developments in the country (Chandrasekharam et al. 2016). Since the Mesozoic aquifers are the main source supporting the geothermal systems in this region, over exploitation of the aquifers, as is done at present to support qat cultivation and other cash crops, may result in the decline in the efﬁciency of the geothermal systems and hence the reservoir capacity to support prolonged electricity generation. Thus, management of the groundwater systems is essential to support geothermal systems. The future option for Yemen to support sustainable food and water security is to depend on desalination of Red Sea water using geothermal power in order to reduce the dependence on groundwater for irrigation.

Evolution of the Hydrological Basins in Western Yemen The evolution of the hydrogeological basin is related to the East African Orogeny that includes the Arabian Nubian Shield (ANS), which was active between 750 and 530 Ma during the collision of the west and east Gondwana landmasses. The regional tectonic activities during this period resulted in uplifts and sinks that resulted in the formation of horsts (anticlines) and grabens (synclines) nearly parallel to the present day Red Sea margin (Fig. 12.4). The Tethys Sea that was active between the Indian–Madagascar landmasses and the East European landmasses (Stern 1994; Meert 2003;

Stern and Johnson 2010; Albaroot et al. 2016) (Fig. 12.4) inundated these grabens. During the Mesozoic and Cenozoic periods, these grabens were ﬁlled with continental and marginal (fluvial) basin sediments comprising shale, sandstone, and limestone. The most prominent grabens that host the largest thickness of these sediments are the approximately N– S trending Wajid and Marib Al Jawf basins (Fig. 12.2). The formation of graben structures started during the Jurassic when the Arabian Shield started foundering. The Tethyan Sea started invading the graben structures (marine transgression) causing sedimentation both from continental and marine sources. These graben structures subsequently transformed into major sedimentary basins like the Wajid and Marib Al Jawf basins. Thus, the Wajid and the Marib Al Jawf (Saba’tayn) basins became loci of thick sediments of shale, sandstone and limestone (Fig. 12.5). Subsequently, several satellite basins emerged during the orogenic period (i.e. Marib Graben, Shabwah Basin, Say’un al Masilah Basin, Ad Dhali Basin, Tihama Basin; Davison et al. 1994). The sedimentation continued until about 31 Ma, when the rifting of the Red Sea was initiated. The thickness of the initial Jurassic–Cretaceous sedimentary pile reached nearly 5 km. The sedimentary basins are delimited from the outcrops of the crystalline basement by major fault systems; the SW–NE trending Sada graben system, the WNW–ESE trending Al Jawf fault and the east–west trending Wadi Mawr fault (Kruck et al. 1996; As Saruri et al. 2010; Fig. 12.2). A simpliﬁed general stratigraphic section along Saba’tayn is shown in Fig. 12.6. The sandstone of the Kohlan and Tawilah formations constitutes a major regional aquifer system in the entire

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Fig. 12.5 Major sedimentary basins in western Yemen (adapted from Wagner 2011)

western Yemen with estimated reserves of 3–5 billion m3, with an annual recharge of about 100 million m3 (UN ESCWA 2013), followed by the Amran and Tawilah limestones. The Wajid aquifer system, enclosed by the Wadi Najran Basin (also known as the Wajid Basin) that lies below the Kohlan in the northern part of Yemen consists of two permeable formations, the lower and an upper sandstone aquifer separated by a thin layer of shale (total thickness *900 m in Saudi Arabia and 100 m in Yemen). This is a trans-boundary aquifer, shared by Saudi Arabia and Yemen, and covers an area of 33,500 km2. A large part of

the aquifer is in Saudi Arabia (28,500 km2) and only 5,000 km2 falls within the northern territory of Yemen (UN ESCWA 2013). The Tawilah sandstone aquifer, part of the Wasia–Biyadh sandstone of Saudi Arabia, has a potential of 500 billion m3 with an area of about 157,000 km2 of which 52,000 km2 falls within Yemen. In Yemen, recharge into this aquifer is low and occurs only when the rainfall exceeds 350 mm/year. Next to the Wajid sandstone, the Tawilah sandstone is a major aquifer in western Yemen, where the aquifer is 400 m thick (Shahin 2007). The Mesozoic and Cenozoic basins

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Fig. 12.6 Typical simpliﬁed stratigraphy of western Yemen showing the sedimentary formations (adapted from Bosence 1997)

Fig. 12.7 Subsurface section along A–B line in Fig. 2, showing the Tertiary and Quaternary volcanic cover (red outline) over the sedimentary formations, western Yemen (adapted from UN ESCWA 2013)

have undergone intense tectonic activity since 31 Ma, the time of initiation of the Red Sea rift, due to the Afar plume activity (Bosworth et al. 2005; Chandrasekharam et al. 2015, 2016). The plume triggered Tertiary and Quaternary volcanic activity that covered entire sedimentary basins in western Yemen as shown in Fig. 12.7. The volcanism is still active in areas like Damt, Damar, Lisi and Isbil (Fig. 12.5). Occasionally the fractured basalts also form shallow aquifers providing a limited supply of groundwater. Because of the active volcanism along the western margin and prevailing high heat flow and geothermal gradient, these aquifers are transformed into high potential geothermal

reservoirs capable of generating power (Chandrasekharam et al. 2016).

Water Resources Management Yemen is one of the water-stressed countries around the Red Sea with an annual per-capita availability of only 100 m3, which is far below the Middle East average (1,250 m3/year) and the world average of 7,500 m3/year (Van der Gun and Ahmed 1995; WHO 2000). The country receives an annual rainfall varying from 50 to 800 mm/year, mostly from the

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Fig. 12.8 Annual rainfall distribution (mm/year) in Yemen

Table 12.1 Annual water budget in Yemen for the year 2007

Table 12.2 Present and future per capita water availability

Source and use

Millions m3

Renewable water

2,500

Surface water

1,500

Groundwater

1,000

Agricultural uses

3,250 (93%)

Domestic uses

200 (6%)

Industrial uses

50 (1%)

Total water uses

3,500

Water deﬁciency

1,000

Year

Expected population

Quantity (m3/year)

1996

1,59,14,000

157

2001

1,89,44,000

132

2006

2,26,73,000

110

2011

2,77,39,000

90

2016

3,22,69,000

77

2021

3,79,94,000

66

2026

4,42,13,000

57

2031

5,06,94,000

49

Indian monsoon, with an average of 200 mm/year and the western margin recording the highest rainfall (Fig. 12.8). Because of the topography, most of the water drains as surface run-off. Although the country has excellent Mesozoic and Cenozoic aquifers (Wajid and Tawilah), most are covered by Tertiary and Quaternary volcanic flows. The volcanic flows also act as hard rock aquifers due to inter-connected joint systems at shallower levels. Over 90%

of the available groundwater is being utilized for agriculture, growing cash crops like coffee, and 40% of it is exclusively reserved for qat cultivation. The estimated renewable water resource is over 2 billion m3/year, while the total withdrawal (for irrigation, industry and domestic use) is over 3 billion m3/year (Table 12.1). The per capita water availability, with the growing population, is expected to decrease drastically (Table 12.2) exerting extreme water stress on the population

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in another decade. In order to meet the deﬁcit, the country is producing 25 million m3/year (FAO 2002) of desalinated water in Taiz. The cultivable land in Yemen is about 36,200 km2, which is used for raising crops such as cereals (6,860 km2), qat (1,229 km2), and the remaining land is divided to grow other cash crops like coffee, wheat, vegetables, and fruits. Besides crops, water is also needed to support livestock to meet milk and milk products demand in the country. Out of a 28 million population, 45% are actively involved in agriculture. Agriculture supports about 10% of the country’s GDP which is 23 billion US$/y. Due to the water deﬁcit for agriculture, the country imports cereals (2.3 million tons), milk products (164,000 tons) and vegetables and fruits (77,000 tons) at a cost of US$ 744 million, which cannot be afforded by the country (UNDP 1992; FAO 2009). To meet agricultural and domestic demand, nearly 3.5 km3 (3.5 billion m3) of groundwater is being pumped by 100,000 dug/bore wells at the rate of about 50 L/s, drawing water from depths of up to 1000 m to support qat cultivation (in 2007). This amount is over one billion m3 above the annual renewable water resources (Table 12.1). The groundwater table is declining at the rate of 7 m annually due to over use and poor recharge, hence the decrease in per capita water availability (Table 12.2) (McCombe et al. 1994; YNWA 2000; MWEY 2005; Hall and Ebaid 2008; Brown 2011). As a result, the Sa’adh basin (part of the Wajid aquifer system) is becoming dry, uprooting cultivation in this region (FAO 2005). In the case of coastal aquifers (the Tihama plains along the Red Sea coast) that consist of Quaternary alluvial deposits, the recharge and discharge are very high due to the high hydraulic conductivity of the aquifers. For example, with an average annual rainfall of 138 mm/year, the recharge and discharge of the Tihama aquifers are 100–150 m3/year respectively (Al-Kebsi and Chandrasekharam 2000). However, due to indiscriminate abstraction, the quality of the coastal aquifers is deteriorating due to salt water intrusion (Al-Kebsi and Chandrasekharam 2000; Fara and Lloyd 2002). Thus, the imbalance between water availability and demand is posing a serious problem for agriculture, threatening the rural economy (Alderwish and Dotteridge 1995; Foster 2003; Gatter 2012). This situation is aggravated with 3% annual population growth forcing over 7 million people to fall below the poverty line (FAO 2009). In order to meet the growing water demand, Sana’a is planning to transport desalinated water from the Red Sea coast at a cost of US$ 6.60/m3. The country has already installed a desalination plant in 2002 in Taiz, with a capacity of 28 MCM/y to supply fresh water to the urban population.

A. Minissale et al.

Quality of Water in the Sedimentary Basins As the sedimentary sequence in the Mesozoic and Cenozoic basins (Fig. 12.6) was deposited in a marine and continental marginal basin province, the groundwater in the sandstone and limestone aquifers will apparently contain a large seawater component (paleowater). Surface water inﬁltration and glaciations during those periods might have diluted the salt concentration, while the shallow Quaternary aquifers, like the alluvial aquifers along the coast and volcanic aquifers, represent modern precipitation. The chemical characteristics of groundwater samples from shallow and deep wells (representing the Wajid sandstone, Amran limestone, Tawilah sandstone and Quaternary alluvial and volcanic aquifers) collected over a period of two decades are documented in Table 12.1. Groundwater quality has not been studied in detail in Yemen. In most of the studies, the quality of groundwater has been assessed in terms of suitability for irrigation or drinking (MOMRY 1995); this means that the main interest in Yemen is usually in the degree of mineralization of the water encountered. Many electrical conductivity measurements have been carried out for this purpose in almost all parts of the country (MOMRY 1995; Sporry 1991). In the present study, several sets of new data, both unpublished and published, collected mainly for geothermal purposes with international cooperation between Italy and Yemen have been used (Minissale et al. 2007, 2013). All the groundwater samples, from the bore and dug wells in three selected areas: (1) the Sana’a basin, (2) the Dhamar Governorate and (3) near Yafa’a in Abyan Governorate, plus a few samples from Taiz, Hajjah are reported in Table 12.3. These areas fall well within the Wajid and Marib Al Jawf basins (Fig. 12.6). The water samples can be classiﬁed into groups using a Langelier and Ludwig (1942) diagram shown in Fig. 12.9. Based on the position of the samples in Fig. 12.9, it is possible to make certain broad and logical inferences. From Fig. 12.9 it is apparent that the water samples can be classiﬁed into three broad groups: (1) Na–Cl, (2) Ca–SO4 and (3) Ca–HCO3 groups. The salinity variation clearly demonstrates the chemical characteristics of the aquifer, with Kohlan (Wajid) sandstone and Amran limestone aquifers (Fig. 12.10) exhibiting high salinity due to their environment of deposition (shallow marine to shelf provenance; Davison et al. 1994). These three main groups are clearly depicted in Fig. 12.10. The Yafa’a samples are the most saline (total dissolved solids, TDS generally >1000 mg/kg), the Dhamar ones are less saline (TDS often 1 US$/m3 (plant capacity 5,000 m3/day), while it is 20 US cents/kWh; IRENA 2012; Chandrasekharam et al. 2017). However, this is not so in the case of geothermal energy sourced desalination plants, as the unit cost is far less compared to solar pv (photovoltaic) and even to wind. The projected levelized cost of electricity generated through solar pv in 2020 will around 10 US cents, while that generated from geothermal sources is 3) 3He/4He ratios in the thermal waters and gases from these sites gives an indication of a shallow magma chamber in the crust (Minissale et al. 2007). In fact, the western geothermal province of Yemen is an extension of the geothermal region of the western Arabian shield and has a high potential to generate electricity. If the approved UNEP fund to execute a 1 MWe (8 million kWh) pilot power plant in Damt materializes (Fig. 12.5), Yemen will be in a position to partly reduce its food imports, and increase its irrigated farming. The characteristics of the Damt geothermal province are very similar to those of the Jizan geothermal site, along with the western Saudi Arabian shield, and a few hundred kilometres NW of Damt. Assuming that similar geothermal conditions prevail in Damt, this site has the potential to generate more than 134 106 kW of electricity (Chandrasekharam et al. 2016). Desalination cost estimates using different energy sources indicate that to generate one m3 of desalinated water from the Red Sea using conventional energy source, costs

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Desalination of Red Sea and Gulf of Aden Seawater …

about 3 US$, while using solar pv the cost is 9 US$, and with a geothermal source it is 1.61 US$ (Chandrasekharam et al. 2017). Besides cost savings, geothermal provides low carbon emissions. The CO2 emission from coal-based power plants (kg CO2/MWh) is 953 while for geothermal based power plants it is 67 (Chandrasekharam and Bundschuh 2008; Shrestha et al. 2011; EIA 2016; Chandrasekharam et al. 2017). An analysis indicates that the per capita water availability of Yemen in 2025 will be 89 m3/year (Miller 2003), which is going to put the country under a highly water stressed condition. However, the government should amend the policy to mitigate water and food security by developing its geothermal resources. Utilizing geothermal fluids for power generation will not deplete the geothermal aquifers (Mesozoic and Cenozoic sandstone and limestone aquifers) and will provide a constant supply of fresh water through desalination. The country thus will continue its qat cultivation and other food commodities and reduce dependence on imported food. Geothermal energy, besides supporting the desalination process, can also support wastewater treatment plants (WWTPs) to recycle the wastewater for purposes other than domestic. At present, there are now more than 20 wastewater treatment plants (WWTPs), either operating or under construction, in Yemen, with a total treatment capacity that in the future will reach about 200,000 m3/day (73 106 m3/ year; Hall and Ebaid 2008). The majority of WWTPs are waste stabilization pond systems, which is the most appropriate treatment for the local conditions and, if designed correctly, should produce high-quality effluent, suitable for unrestricted re-utilization (Abu-Madi and Al-Sa’ed 2010). Conventional treatment is provided in the cities of Sana’a and Ibb, by extended aeration, and in Hajjah by Imhoff tanks and associated percolating ﬁlters. This type of WWTP produces relatively poor-quality effluents, but in these cases, the lack of space precludes the use of pond treatment (Hall and Ebaid 2008). In the city of Taiz, in the south of Yemen, the Ministry of Water and Environment is preparing a feasibility study for a brackish groundwater desalination plant. If feasible, the planned 5 million L/day plant will help to alleviate the city’s water shortage problem, where daily production would in the future represent some 20–30% of the current water production for the city.

Conclusion In another few years from now, Yemen will be under a highly water stressed condition with per-capita water availability dropping to 89 m3/year. This situation may force the country to depend on other countries for food and energy supplies. However, as discussed here, utilizing geothermal energy to support desalination together with WWTPs will

211

safeguard the country’s food-energy security. The policy makers should adopt a drastic change in the food and energy policy and immediately implement plans to develop all the geothermal energy sources that have been lying untapped for several decades. This will provide the country with a sound economy by supporting the enhanced cultivation of qat and increasing its GDP, and will improve the country’s socio-economic status by providing employment to the rural population and lifting them above the poverty line. Acknowledgements This study was possible thanks to many organizations that have provided funds for travel in Yemen, including UNESCO and the Italian Ministry of Foreign Affairs. The Geological Survey of Yemen, namely its director Dr. Ismail Al Ghanad and Dr. Mohamed Mattash, are warmly thanked, especially the latter for all the work in the ﬁeld in 2001, 2002, 2007 and 2008. The University of Sana’a is also thanked for providing a grant to M. F. Al-Dubai for travel to Italy. We thank Dr. Najeeb Rasul for inviting us to write this chapter and his patience in extending the time of submission.

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Red Sea Research: A Personal Perspective

13

Peter Vine

Abstract

In this chapter the author reflects on ﬁve strands of marine biological research in which he was involved in the Red Sea and reviews subsequent progress in their respective ﬁelds. He presents his own ﬁndings and those of other biologists on: (1) Crown of Thorns starﬁsh (Acanthaster planci) outbreaks; (2) Corals-v-algae and the influence of herbivorous ﬁsh on the outcome; (3) Corals-v-sponges and the ecological impact of the battle for dominance; (4) General reef ecology and conservation; and ﬁnally, (5) Taxonomy of Red Sea marine life. There have been substantial scientiﬁc developments in all the ﬁelds covered. Whilst we know much more than we did in the 1960s and 1970s, when much of the coral-reef research effort in the Red Sea was in its early stages, there are many questions still unanswered. Research continues, taking advantage of modern technologies, revealing the rich complexity and dynamic nature of the Red Sea’s coral reefs.

Introduction The Red Sea is like a living laboratory for tropical marine research, offering a wide range of environments, from sheltered muddy inlets to vertiginous coral drop-offs. Its remarkably clear waters and rich assemblages of ﬁsh and invertebrates attracted attention of European scientists as far back as Danish naturalist Peter Forsskål (1732–1763), who died during the ‘Arabia Felix’ expedition in Yemen. His collection, or surviving remnants of it, eventually arrived in Copenhagen and formed the starting point for many subsequent studies (Vine and Schmid 1987).

P. Vine (&) Earth and Ocean Sciences, School of Natural Sciences, NUI Galway, Galway, Ireland e-mail: [email protected]

Arriving in Port Sudan in 1970 in order to join the Cambridge Coral Starﬁsh Research Group (CCSRG), the author had previously spent a year on Tarawa atoll in Kiribati (then known as the Gilbert and Ellice Islands) and a year based at James Cook University in Townsville, Australia. Tarawa provided a unique introduction to SCUBA diving among coral reefs that was consolidated during a Rotary Fellowship year (1969) on Australia’s Great Barrier Reef, together with the oceanic islands of Melanesia, Micronesia and Polynesia. Port Sudan’s marine life had already been popularised by the exploits of Dr. Hans Hass and his wife Lotte, together with Cmd. Jacques Cousteau and the crew of Calypso. The latter had built an underwater house on nearby Shaab Rumi (‘Roman Reef’) and their books and television ﬁlms had inspired a young generation of underwater explorers. CCSRG was a loose afﬁliation of young British biologists and diving enthusiasts that was led by its chairman, Dr. Christopher Roads and Scientiﬁc Director, Rupert Ormond. The present author fulﬁlled the role of deputy director for two years, prior to becoming director of a new marine laboratory established by Khartoum University at the ancient, deserted city of Suakin. What Sudan offered was easy access to some of the world’s most proliﬁc coral reefs: Sanganeb, Shaab Rumi, Wingate, Towartit and the islands of the Suakin Archipelago. CCSRG’s raison d’être was to investigate the ecological triggers resulting in large aggregations of Acanthaster planci (Crown of Thorns starﬁsh: COTS) that were being reported in ‘plague’ numbers on coral reefs right across the Indo-Paciﬁc. In order to understand the population dynamics of COTS it is necessary to gain an appreciation of coral reef ecology in general, especially the various forces at play governing the recruitment and survival of corals, crustose coralline algae (CCA), invertebrates such as COTS and their predators (at all stages of their life-cycle). In 1970, when I started my work in the Red Sea, there were huge gaps in our knowledge of these criteria and ‘scientiﬁc’ conclusions often took the form of unsubstantiated hypotheses rather than data-driven factual analysis.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_13

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During the course of my Red Sea research we raised COTS larvae from the eggs; studied the starﬁsh’s larval responses to a range of physical and chemical factors; studied ﬁsh predators of COTS; investigated the ecological impact of aggressive behaviour by damselﬁsh; demonstrated the ecological signiﬁcance of CCA; collected serpulid tube worms, naming a new genus and four new species (Vine 1972); studied competition between corals, sponges and algae; monitored growth rates of coral colonies on Cousteau’s garage at Shaab Rumi (Vine and Head 1977); and tested systems for raising Tilapia (Sarotherodon spiluris)— normally a freshwater ﬁsh—in the saline waters of the Red Sea. This research was facilitated by a number of supportive organisations including CCSRG (partially funded by the UK Government’s Overseas Development Administration— ODA); Khartoum University’s Suakin Marine Biology Laboratory and the joint Saudi-British Fisheries Development Project, based in Jeddah. There have been numerous advances in the various strands of research that I pursued almost 50 years ago and I welcome the opportunity to revisit some topics of my early research and show where they have led since that time. I believe that there are lessons to be learnt from such an initiative, particularly in connection with the ﬁrst topic of this chapter that deals with outbreaks of COTS, but also in relation to an appreciation of the physical and biological dynamics of a ‘balanced’ reef system. Little did I appreciate, when studying the aggressive behaviour of reef ‘farmers’ (such as Stegastes nigricans), that this would reveal how their activities impact on both the physical structure of shallow reefs (poorly cemented due to CCA exclusion) and their attractiveness (or lack of it) to larvae of both corals and COTS as settlement sites (owing to exclusion of CCA by ‘farmed’ ﬁlamentous algae).

Crown of Thorns Starfish (Acanthaster planci) Outbreaks The Crown of Thorns starﬁsh (Acanthaster planci) (COTS) (Fig. 13.1) was ﬁrst mentioned by Rumphius in 1705 and described by Plancus and Gualtieri in 1743. The name Acanthaster planci was created by Linnaeus in 1758. The species rose in notoriety in the late 1950s and early 1960s when large numbers were recorded at popular tourist destinations such as Green Island off Cairns, in 1959, and other reports soon followed, describing widely distributed outbreaks right across the Indo-Paciﬁc. Professor Thomas Goreau ﬁrst reported on Red Sea aggregations in 1963. Our familiarity with life on coral reefs (and particularly COTS) can be traced back to the introduction to the general public of SCUBA (self-contained-underwater-breathing-

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apparatus), starting in the mid-1950s when proponents could be counted in the hundreds rather than thousands or millions. Sixty years later, in 2016, there were approximately 6 million active SCUBA divers and 20 million snorkelers worldwide and marine watersports were among the fastest growing sectors of the leisure/tourism industry. There were several key events along the way with books and ﬁlms playing a major role. Hans Hass’s book Diving to Adventure was ﬁrst published in German (Drei Jäger auf dem Meeresgrund) in 1939 and republished in English (translated by Barrows Mussey) in 1952 (Hass 1952a). It described Hans Hass’s early adventures in the Caribbean and off Curaçao. In the same year his ﬁrst account of diving in the Red Sea was published in English (Hass 1952b). Hass played a big role in popularizing diving during its early stages of development. The British Sub Aqua Club was founded in 1953 and wetsuits ﬁrst became available to the public in 1956. In the United States, the National Association of Underwater Instructors (NAUI) was founded in 1959 whilst PADI (the Professional Association of Diving Instructors) was established in 1966. Cousteau’s Silent World ﬁlm, partially shot in the Red Sea, received an Academy Award for Best Documentary Feature and the Palme d’Or award at the Cannes Film Festival in 1957. Scubapro introduced the stabilization jacket (BC or BCD) in 1971, followed by the dive computer in 1972. Cousteau’s famous Conshelf 2 experiment in underwater living took place in 1963 at Shaab Rumi reef in the Sudanese Red Sea. By the early 1960s SCUBA diving was an integral part of the tourism offering from the Red Sea and Indian Ocean, right across the Paciﬁc and into the Caribbean. Humankind was enthusiastically exploring and discovering a new world full of colour, adventure and beauty—a world that had existed for millennia but which had been tantalizingly out of reach until SCUBA changed everything. Reports of aggregations of COTS not surprisingly mirrored this rapid increase of underwater observers. The mere ‘discovery’ of ‘new’ starﬁsh outbreaks (i.e., previously unreported aggregations) was offered as evidence that reefs were facing unprecedented threats of imminent destruction. There were few voices questioning this apparently simplistic analysis and vested interests, particularly in terms of research grant applications (Sapp 1999), appeared to obstruct a more balanced examination of the cause of the ominous starﬁsh aggregations that so alarmingly transformed once flourishing reefs to blanched desolate seascapes. The massive scale of COTS outbreaks on the Great Barrier Reef and other Indo-Paciﬁc reefs caught the attention of world media, the general public and a somewhat perplexed scientiﬁc community. The ‘noise’ around COTS during the early 1970s included claims that this was the beginning of the end for the world’s coral reefs! Theo Brown (Brown and Willey 1972)

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Fig. 13.1 The Crown of Thorns Starﬁsh Acanthaster planci adult in the Sudanese Red Sea (© Sjoeholm)

wrote as follows: “As the infestation is allowed to spread unchecked, I believe the ultimate survival of the reef is in doubt. …. I believe the starﬁsh plague is the ﬁrst of a series of major ecological disturbances that will have far reaching and devastating effects on mankind. Perhaps through the Crown of Thorns infestation, we are witnessing the beginning of the end.” Peter James authored a book on this subject (Requiem for the reef: The story of ofﬁcial distortion about the Crown-of-Thorns starﬁsh. James et al. 1976). A well-balanced analysis of the debate surrounding COTS is provided by Ian Sapp (1999) in What Is Natural? Coral Reef Crisis. Joining the Cambridge Coral Starﬁsh Research Group (CCSRG) (Fig. 13.2) in 1971, the author had been following with interest a public debate between Richard Chesher (Chesher 1969), Thomas Dana (Dana et al. 1972) and William Newman. Chesher favoured the view that, more often than not, Man had a direct hand in the population explosions being witnessed throughout the Indo-Paciﬁc and therefore the starﬁsh should be controlled. He suggested that starﬁsh larvae are heavily preyed upon by live coral polyps and that predatory pressures may have been reduced by mechanical damage to reefs, such as reef blasting. On the other hand, Newman and Dana held the view that they were primarily natural events in the long-term life of coral reefs (Dana et al. 1972). Thomas Dana published evidence of previous aggregations and proposed that a likely trigger for reef disturbance, leading to A. planci outbreaks, was storm damage caused by cyclones and wave surge that could also wreak havoc on shallow reefs, uprooting and killing many coral

colonies. In a letter to the present author, Dana emphasized that this could be one of several natural events that trigger the outbreaks. “…if we have a potentially unstable situation, a number of parameters need to be considered, and perhaps all will form part of the model. We think storms are involved —typhoon, rain and wave types, but this does not exclude the other involvements” (pers. comm.). The Scientiﬁc Director of the CCSRG, Dr. Rupert Ormond (Ormond and Campbell 1974), discussed the possible outbreak mechanisms for COTS and proposed a ‘Special Instability’ hypothesis that draws attention to a feedback mechanism whereby coral-eating starﬁsh also create habitats (bare feeding scars) that are potential sites for even greater numbers of settled larvae. It has since been shown that the COTS larvae most frequently settle on pink coralline algae (e.g., Porolithon or Hydrolithon) that tend to colonise newly exposed surfaces of dead coral, playing a crucial role in cementing the reef structure. The pivotal signiﬁcance of CCA on coral reefs is an integral part of the COTS story and is discussed in relation to several topics covered in this chapter. By the early 1970s COTS was a global media phenomenon heavily laden with unsubstantiated claims regarding causes and extent of outbreaks. Despite reports of widely scattered aggregations of COTS on Indo-Paciﬁc coral reefs, there was mounting evidence that many of these could be natural events and as such may well, in the medium to long term, be a contributor to reef development rather than reef destruction. The author’s views, as presented in a number of publications (Vine 1970, 1973), aligned in most respects

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Fig. 13.2 Cambridge Coral Starﬁsh Research Group (CCSRG) Platform (Head and Ormond 1978) on Harvey Reef provided a living laboratory to study life on the reef (© Vine)

with those of Ormond and Campbell, together with Newman and Dana, in acknowledging the likelihood that A. planci aggregations are fundamentally naturally occurring events that may also be triggered by reef disturbances attributable to Man. Our knowledge and understanding of COTS has been greatly advanced by the many studies that have taken place since the early spate of studies in the late 1960s and early 1970s. First of all, we now know that there are effectively four species of COTS in the Indo Paciﬁc, as demonstrated by mitochondrial clades, from the Red Sea, the Paciﬁc (Pac), the Northern (NIO) and the Southern Indian Ocean (SIO) that, taken together, form a species complex (Vogler et al. 2008). In a Letter to Nature published in 1978, Richard Moore set forth his view that A. planci outbreaks are naturally occurring events. “I believe that a more detailed consideration of the ecology of A. planci … suggests violent population fluctuations without the assistance of Man’s activities.” It was a theory that he developed over the next ten years, ﬁnding much evidence to corroborate his early observations (Moore 1978). In terms of effort, endurance, tenacity and scientiﬁc achievement, attention must be drawn to the impressive report by Moore of the Queen Mary College 1984 Red Sea Expedition to Dungonab Bay entitled ‘A Study of an Outbreak Area of the Crown of Thorns Starﬁsh’ (Moore 1985). After conquering a long list of logistical challenges that

included rescuing a heat-exhausted team member from the sea, being left to carry on alone, sailing off one of Sudan’s most remote and poorly charted coastlines, suffering a terminal breakdown of the expedition’s compressor, self-medicating for potentially crippling ‘coral ear’ and ﬁnding that his underwater camera had not produced a single usable picture, he modestly reports: “In spite of this catalogue of mishaps, far more research was implemented than on previous visits to Dungonab Bay, and the original objectives of the expedition were largely fulﬁlled. In all, perhaps 15 man-days of ﬁeld work were realized, including the surveys of reefs between Port Sudan and Dungonab” (Moore 1985). Rick Moore’s study of Dungonab conﬁrmed previous observations of the common occurrence of COTS in the bay and of the impact of food supply on their behaviour. Where live corals were scarce, the starﬁsh tended to remain exposed in daytime, feeding on a range of items, including soft corals. In areas with a healthier coverage of scleractinian corals, the starﬁsh remained hidden in daytime, emerging to feed at night. He showed that the nutrient-rich shallow waters of Dungonab Bay area, well known as a spat collection and nursery area for pearl oysters, were also a long-term source of A. planci larvae that could seed COTS outbreaks on an annual basis. He noted evidence for larval settlement close to the entrance of the bay and suggested that localized changes in temperature or salinity (that are quite marked in this area) could stimulate settlement of the

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brachiolaria larvae. As for those larvae that drift out of Dungonab Bay and enter the main body of the central Red Sea, Moore drew attention to a gyre that sweeps from outside Dungonab, across toward Jeddah, then down past the Farasan Bank and back to Sudan where it flows northward from Suakin and Port Sudan, completing the circle off the Mohammad Quol area. He pointed to the common occurrence of COTS on the Farasan Bank, suggesting that this population might have seeded an outbreak off Port Sudan in 1970. Given the special instability of their recruitment ﬁgures and the widespread occurrence of ‘plagues’, an increasing number of scientists felt it unlikely that dense aggregations of COTS had not occurred naturally, long before Man’s impact on coastal environments reached the levels we see today. Natural events such as previous climate change, sea level alteration, hurricane damage or volcanic activity might all be expected to disturb the ecological balance, impacting survival of reef ﬁshes and invertebrates, and from time to time triggering COTs outbreaks. Coral reefs have lived with this threat for a very long time! Anthropogenic impacts, perceived as potentially creating similar impacts to natural events, include pollution, run-off (caused by agriculture or coastal developments), ocean warming, acidiﬁcation, dive tourism, anchoring, dredging, reef blasting and over-ﬁshing—all of which exact their toll on healthy ‘natural’ coral reefs and may lead to COTS (Dulvy et al. 2004) outbreaks. The overriding question remains: by what mechanism does the normal ‘control’ on COTS populations break down, triggering the massive aggregations that can wipe out nearly all the live corals along wide sections of coral reef? Zann et al. (1987) studied juvenile Acanthaster on reefs in Fiji. They found juveniles ‘hiding’ among loose algal encrusted coral rocks on the reef front, on the bases of dead Acropora in more sheltered locations and among the interstices of the crevices on the reef crest. Recruitment was studied over a nine-year period and was shown to be normally very low, with 8 month-old juveniles recorded at 0.004 per m2 in the boulder zone. However, a massive recruitment occurred in 1984, resulting in densities of 7 month-old juveniles at 8.3 per m2 in the same zone. By measuring, over a two-year period, sizes of individuals in the ‘outbreak cohort’, they demonstrated a sigmoidal growth curve with maximum diameter increases of “2.6, 16.7 and 5.3 mm/month in the algal-feeding, early coral-feeding and adult phases, respectively”. At 13–15 months, the young starﬁsh switched from feeding on coralline algae to feeding on scleractinian corals but they continued in their cryptic behaviour, withdrawing into crevices in daytime and generally being more active at night. This ﬁnally changed at around 20 months when they formed aggregations and could be seen out on the reefs during daytime. By this stage they

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were almost ready to breed, becoming sexually mature at 23 months. Zann and colleagues concluded that recruitment is erratic and that an outbreak results from a “single massive settlement”. Scientists have proposed a number of possible causes of massive settlement and survival (Moran 1986). Run-off of nutrient rich waters associated with coastal flooding may boost growth rates and hence survival at planktonic and early settled phases. There is experimental evidence to suggest that COTS outbreaks are predominantly controlled by phytoplankton availability. Heavy rain causing run off to the sea of nutrient rich water may lead to COTS outbreaks since it is known that larval development and growth is directly affected by the concentration of the phytoplankton on which COTS larvae feed. It has been shown, for example, that doubling concentrations of large phytoplankton can create an almost 10-fold increase in larval development, growth and survival of COTS. Rising sea temperatures (Raitsos et al. 2011) shortening the time larvae spend in the plankton, or juveniles spend as vulnerable algal feeding bottom-dwellers, have also been proposed as potential population growth triggers (Uthicke et al. 2015). The latter showed that in a nutrition medium containing 5,000 cells per ml, “a 2 °C increase may shorten developmental time by 30% and may increase the probability of survival by 240%. The main contribution of temperature is to ‘push’ well-fed larvae faster to settlement.” They concluded that warmer sea temperatures connected to climate change are important co-factors promoting COTS outbreaks. However, there seems to be two schools of thought with regard to the possible impact on COTS of a 2 °C temperature rise. Whilst Uthicke et al. (2015) indicate that such a rise may speed larval development and survival, Kamya et al. (2014, 2016) draw attention to a negative impact of such heightened temperatures on late stage brachiolaria larvae. They (Kamya et al. 2014, 2016) have focused on predicting possible side-effects of ocean warming on COTS. Reporting on experiments to examine the effects of temperature and acidity on larvae of Acanthaster, they showed that whilst there was no impact on fertilization or early larval development of 30 °C and pH 7.6, there was a marked negative impact on later larval stages—a contrary ﬁnding to that of Uthicke et al. (2015). Conjecturing that such a 2 °C rise might lead to a reduction in COTS success on low latitude coral reefs (where sea temperatures are expected to reach these levels), they also suggest that the warmer seas may result in migration of the starﬁsh to higher latitude coral reefs where temperatures are closer to 28 °C. They also point out that Acanthaster has a higher tolerance to temperature rise than do most reef building corals. This work may be of particular relevance to the central and southern Red Sea where temperatures are

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already higher than at comparable latitudes of the open Indo-Paciﬁc Ocean and where a sudden 1 °C rise has recently been reported. Raitsos et al. (2011) reported an increase of 1 °C over the previous 15 years in the Red Sea, resulting in both bleaching and a 30% reduction in coral growth—a trend that threatens to halt coral growth in the central Red Sea by 2070, especially in proximity to cities such as Yanbu, Jeddah, Gizan, Aqaba, Eilat, and Port Sudan (Sawall and Al-Sofyani 2015). Where such changes result in algal dominance over reef-building corals, COTS may be expected to experience signiﬁcant recruitment fluctuations, accompanied by a probable decrease in coverage of live corals. In a further development of this work Kamya et al. (2017) pointed to another potential set-back for COTS in the form of increased acidity of ocean waters (OA). More acid waters are expected to negatively impact on the CCA on which many juvenile Acanthaster depend for food (and, incidentally, coral larvae depend for settlement). Meanwhile, the increased acidity may enhance feeding rates by COTS’s herbivorous juveniles (Uthicke et al. 2013). This team found that settlement of COTS larvae “was signiﬁcantly reduced on crustose coralline algae (known settlement inducers of COTS) that had been exposed to OA conditions for 85 days prior to settlement assays”. Reduced settlement may be the largest bottleneck for overall juvenile production and their results indicate that “reductions in fertilization and settlement success alone would reduce COTS population replenishment by over 50%”. They conclude however that it is “unlikely that this effect is sufﬁcient to provide respite for corals from other negative anthropogenic impacts and direct stress from OA and warming on corals”. A complicating factor in predicting the impact of such changes is that COTS’ ability to withstand or adapt to the environmental changes associated with projected climate change effects (raised sea temperature and lowered pH levels) has been shown to differ, depending on parental identity (Sparks et al. 2017). Given the dramatic impact of increasing phytoplankton cell concentration in seawater containing COTS larvae (see above), it is not surprising that the presence of heightened concentrations of nutrient-rich waters is a major suspect behind outbreaks of the starﬁsh. The impact of nutrient levels was also suggested by Birkeland (1982) as a key factor in boosting larval development and survival. A boost in nutrient levels caused by run off during the breeding season, especially around mainland associated islands rather than on offshore reefs, might lead to high larval survival, settlement and early growth. Resulting outbreaks of COTS might become obvious, in terms of recorded numbers of adults, one to two years after such heightened nutrient levels boosted larval survival. Wolfe et al. (2017) have however

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questioned this, showing that eutrophic levels are not required for outbreak conditions. COTS larvae have been successfully raised on a monoculture diet of phytoplankton such as Dunaliella primolecta (M. Barker, pers. comm. 1973; Yamaguchi 1973; Lucas 1982, 1984). They may remain in the plankton for as short as ten days or as long as 50 days, depending on a variety of environmental factors, including sea temperature and density of phytoplankton food. As many authors have asserted, it is hardly surprising that A. planci populations are known to undergo dramatic changes and they are not alone among echinoderms in this regard (Calderwood et al. 2016). The intrinsic nature of their reproductive biology plays a signiﬁcant role in their tendency to undergo sudden population explosions (Ormond and Campbell 1974). Ormond et al. (1973), noting the chemical attraction of other COTS to a feeding starﬁsh, considered the local mini-aggregations could result in greatly increased fertilization success in breeding individuals, otherwise widely spaced on the reef. A single individual may release over a million eggs during one spawning episode and up to 50 million in a single season. “Outbreaking populations (ca. 100000 starﬁsh per reef) will kill thousands of square metres of coral, equivalent to hundreds of kilograms’ dry weight of soft tissues per day” (Keesing 1990). Mass synchronized spawning guarantees very high rates of egg fertilization, over 80% in samples taken at the peak of a major spawning event and 50 to 20% in animals 30–60 m apart—much higher than recorded in other invertebrates (Babcock and Mundy 1992). These numbers speak for themselves. In order to replace two adults, 20 million eggs would undergo a survival rate of about 0.00000001% where the larvae recruit. A jump in survival rate to 0.1% (one in a thousand) of 20 million eggs would result in 20,000 adult starﬁsh where the larvae have recruited. Given the logic dictated by these ﬁgures it seems likely that survival rates of larvae and young juveniles are a crucial element in the tendency of A. planci to undergo population explosions. Cowan et al. (2016) reported on various planktivorous damselﬁshes’ appetite for Acanthaster larvae. They showed that some species have the capacity to buffer against population fluctuations and may contribute toward the stability of COTS populations. This suggests that removal of planktivores from reef shallows would raise the prospect of higher survival rates of Acanthaster larvae, potentially leading to peaks in settlement of their late brachiolaria larvae. When the late brachiolaria larvae are ready to settle, they commence probing the reef for suitable locations in terms of refuge from predators, such as puffer ﬁsh (Fig. 13.3), and availability of food. Based on studies to date, it is clear that, like a number of other echinoderms, they actively seek out their preferred habitat of CCA (Fig. 13.4) that is abundant on Red Sea reefs. This tends to flourish in moderately

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exposed sections of the reef crest and shallow reef-face where it is often found encrusting dead Acropora corals. The young starﬁsh’s bright pink colouration, merging with that of the encrusting alga, combined with their cryptic behavior, provide camouflage and refuge from potential predators. By two weeks old, their mouths are developed and they start feeding on the CCA, leaving small white feeding scars, much as the adults do on corals, but on a much smaller scale (Henderson and Lucas 1971; Lucas 1973; Hughes et al. 2014; Yokochi and Ogura 1987). Coralline algae are thus a key component in settlement and survival of young COTS on the reef and, as we shall see in the next section, their distribution on the shallow reef is affected by ﬁsh that ‘farm’ the reef, such as Stegastes nigricans, with little or no coralline algae growing in damselﬁsh protected ‘farms’ where algal turf predominates. COTS begin feeding on live coral at 6–15 months old (depending on growth rates), when they are fully developed young adults with an effective protection of toxic spines and well-developed stomachs that spread over the coral polyps in an impressive display of extra-oral digestion (Barnes et al. 1970). Coral feeding COTS attract other COTS to the same location, tending to form aggregations. Individuals that become associated with such aggregations may forsake their cryptic behaviour and expose themselves on coral reefs as they feed in daylight, unlike their younger stages that are usually hidden beneath coral heads or in crevices during daytime, only emerging to feed at night. As mentioned above, despite their adults’ capacity to lay bare huge tracts of live coral, larval and juvenile phases of

Fig. 13.3 The pufferﬁsh, Arothron hispidus was shown to be an opportunistic predator on Acanthaster adults (Ormond et al. 1973). We kept several in cages on the reef to study their behaviour (© Vine)

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the starﬁsh are themselves vulnerable to predation by both ﬁsh and corals. It has also been noted that COTS aggregations feeding on live coral (creating surfaces for coralline algae to flourish) may also positively impact on the available surfaces for their own larvae to settle—creating favourable conditions for secondary outbreaks, potentially larger than initial ones in a given area (Ormond and Campbell 1974). Notwithstanding the degree of impact of the feedback mechanism proposed by Ormond and Campbell (1974), the role played by coralline algae cannot be over emphasized. Space, food and protection from predation are critical factors influencing survival of settled starﬁsh (Hughes et al. 2014). As stated above, crustose coralline algae play a vital role in stabilizing reef structure and are a common feature of healthy coral reefs. Not only do they help to build the reef form, cementing dead coral rubble together, but they also provide larval settlement surfaces for many invertebrates (including corals and starﬁsh) and create crevices for starﬁsh to hide, as well as food for a range of invertebrates, including COTS. Development of these encrusting algae is, as we shall see below, dependent on the scraping and browsing activities of reef ﬁsh and other invertebrate herbivores such as young Acanthaster themselves or sea urchins (e.g., Diadema). Experiments have shown that once new, clean, surfaces appear on reefs in the Red Sea, the ﬁrst colonisers of such surfaces are crustose coralline algae. A series of experiments related to algal growth in pomacentrid territories (Vine 1974) (see below) undertaken on a Sudanese reef, poses a number of questions regarding the role of herbivorous and grazing ﬁsh on the shallow water

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Fig. 13.4 Crustose coralline alga (CCA)—prime settlement substrate for many invertebrates including corals’ and A. planci larvae (© Sjoeholm)

reef structure, including their influence over settlement and growth of coralline algae. The author demonstrated that these important calcareous algae are absent from damselﬁsh ‘farms’, limiting their growth to areas where reef herbivores are more active. Randall (1972) also proposed that ﬁsh play an important role in survival of recently settled COTS. “Plant and detritus feeding animals may be among the more important consumers of newly transformed starﬁsh. Many of these animals such as ﬁshes, echinoids and gastropods are not very discriminating as they graze. Small benthic animals, though ingested incidentally, may be eaten in great numbers”. In April 1996, Charles Birkeland re-visited areas in Palau that he had recorded as being severely impacted by COTS in 1977–78. Writing to Jan Sapp, author of the book What is Natural? Coral Reef Crisis (Sapp 1999), he stated: “These areas have not only failed to recover after nearly 20 years, but they have deteriorated further. I think it is over ﬁshing of herbivorous ﬁshes so the coral recruits cannot get a start. The areas are all covered with algae. This is in great contrast to the beautiful healthy reefs which COTS did not infest in the 1970s.” Pratchett et al. (2014) brought the state of our knowledge of Acanthaster research from 1990 to 2014 up to date. Evidence is mounting of a crucial relationship between the presence of herbivorous ﬁsh and the recruitment of COTS (Jessen et al. 2014), both in terms of the initial outbreaks and indeﬁnite recovery periods due to algae preventing the re-establishment of reef building corals. There is a globally recognized trend toward loss of coral cover and increase in algal cover on many tropical reefs. A study on the Great

Barrier Reef showed that a phase shift from coral dominance to algal dominance was associated with low diversity of herbivorous ﬁshes and low abundance of algal browsers such as rabbit ﬁsh (Siganidae), and of grazers/detritivores such as surgeonﬁsh (Acanthuridae) (Cheal et al. 2010, 2012). Other episodic intrusions such as run-off after torrential rainfall (as noted above, larval development, growth and survival increases almost ten-fold with doubled concentrations of large phytoplankton; Brodie et al. 2005), hurricanes (Brown 1997), smothering of shallow habitats by dredge tailings or eutrophication from sewage outflows could all trigger conditions for high recruitment ﬁgures and these could be natural or anthropogenic in nature. Regardless of the causes, outbreaks of COTS on coral reefs can have serious implications. In areas such as the Great Barrier Reef where a 17 year cyclical pattern of outbreaks has been postulated, efforts have been made to introduce effective management control strategies based on methods employed for control of invasive species (which A. planci is not). The options and challenges involved have been discussed by Jessica Hoey et al. (2016), and include use of a robotic submersible known as COTSbot that is designed to search out and inject a toxin into individual starﬁsh. The full story may be somewhat more complex than the linear nature of the various hypothetical cause and effect scenarios discussed above. Nevertheless, we are getting closer to understanding COTS biology than we were in the 1960s and 1970s. As we move forward it is important to recognize that coral reef ecosystems are dynamic regimes

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that respond in complex ways to different conditions and that multiple factors are likely to be involved. Mayer (2004) discusses the importance of a holistic approach in attributing ‘blame’ for COTS outbreaks. Notwithstanding the multiple cause and effect scenarios alluded to above, it remains clear that protection of reef ﬁshes, especially herbivores, is a vital step in reef conservation and in supporting healthy coral growth. This is a ﬁeld of research worthy of closer attention since it impacts directly on development of management strategies for coral reefs (Dulvy et al. 2004; Hughes et al. 2014).

Corals–V-Algae and the Influence of Herbivorous Fish on the Outcome Whilst working with the CCSRG off Port Sudan, the author was a regular visitor to the reef shallows of ‘Harvey Reef’ (part of the Towartit reef complex) where a research platform was situated. Dart (1972) studied echinoids on this reef and hypothesized that their grazing of ﬁlamentous algae could contribute to coral larval settlement. One of the author’s regular swims from the platform to a point along the reef edge took him close to a patch of reef characterized by loose algal-coated dead coral rubble, defended from intruders (both ﬁsh and Man) by pugnacious damselﬁsh (Fig. 13.5). The rubble mound was adjacent to an area of shallow sand where the author regularly photographed ﬁsh. In a paper published by Vine (1974), the author wrote: … one way of encouraging parrotﬁsh and surgeonﬁsh to feed in front of the camera was to remove loose pieces of algal covered rubble from the reef and to place them on sand. Each time this was done many ﬁsh (mainly Acanthuridae, Siganidae, Chaetodontidae and Balistidae) commenced browsing on the displaced rock and, within about 30 min, the green matting of Fig. 13.5 Stegastes nigricans (previously Pomacentrus lividus) ‘farming’ ﬁlamentous algae. The ﬁsh chases intruding individuals away, preventing herbivores from grazing on the algal turf. This sets in train a chain reaction that involves, among other effects: increased sedimentation, prevention of settlement and growth of crustose coralline algae, loss of favoured coral settlement sites and weakening of reef structure (© Sjoeholm)

223 ﬁlamentous algae previously covering the rock had been consumed by ﬁsh, leaving the rubble fragments to merge inconspicuously with the colour of the lagoon sand.The question arose: why do these herbivorous ﬁsh not eat the green alga growing on the rocks in situ? The intensity of their browsing on displaced rocks was so great as to suggest that the in situ rocks would not have such a thick matting of green ﬁlamentous algae if they were grazed by surgeon and parrotﬁshes.

Suspecting that the reef’s architecture was being influenced by aggressive pomacentrids that were protecting their occupied rubble patches from reef grazers, the author set up a series of experiments to probe deeper. Several other characteristics of the damselﬁsh territories were noted during the course of this work. Fragments of dead coral were often poorly cemented and therefore easy to remove as ‘bait’ for other reef ﬁsh. In addition, there was little live coral growing among algal covered rocks, whereas around the edges of their territories encrusting corals were associated with relatively high densities of the serpulid tubeworms, Spirobranchus sp. The study (Vine 1974) led to some unexpected ﬁndings that provided a deeper understanding of the processes at work in a balanced coral reef environment. The essence of the ﬁeld experiment was that bathroom tiles were screwed onto the reef in shallow water to act as settlement plates. Some were protected by wire netting cages, preventing access to herbivorous ﬁshes (thus mirroring the effect of aggressive damselﬁsh chasing away competitors or of over-ﬁshing), whilst other tiles were left unprotected, permitting all ﬁsh to graze on their surfaces. After periods of 2– 4 weeks the plates were lifted, weeds were removed, dried and weighed, and the surfaces examined for attached organisms. A photograph of two such settlement plates after one of the experiments is shown here (Fig. 13.6). It clearly illustrates the impact of reef grazing ﬁsh on reef structure.

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Fig. 13.6 Settlement plates after ﬁlamentous algae have been removed. The protected (left-hand) plate had signiﬁcantly more ‘algal turf’ but no settlement of crustose coralline algae (CCA). The right-hand plate that was exposed to reef grazers had signiﬁcantly less algal turf formed by ﬁlamentous algae (since this had been grazed) but dense settlement by CCA. The latter are preferred settlement surfaces for coral planula larvae, A. planci larvae and the main source of food for young COTS, before they begin feeding on corals. This work was ﬁrst described in Vine (1974)

The left-hand plate (that was protected by a wire netting cage) had a clean surface after removal of a thick mono-speciﬁc algal turf formed by a matting of green ﬁlamentous algae. In contrast, the right-hand plate, that had been left exposed on the reef, adjacent to the protected plate, had a high percentage covering of CCA that was clearly visible after removal of the much thinner covering of ﬁlamentous algae. The latter was due to the fact that browsing and grazing reef ﬁsh, constantly scraping at the unprotected plate, efﬁciently cropped the algal turf and created fresh surfaces for settlement and growth of coralline algae. The twin tiles in the photograph taken during the above experiments in 1973 tell a compelling tale, pointing to several impacts of ﬁsh on coral reef development. One of the ﬁrst conclusions was that green ﬁlamentous algae coating the protected tiles would cover much of the reef top if it were not for the grazing/browsing activities of a healthy population of herbivorous reef ﬁshes that are largely responsible for controlling the extent of its growth. It was also clear that the aggressive behaviour of damselﬁsh (Fig. 13.5) led to growth of green ﬁlamentous algae within their territories. Subsequent researchers have categorized such ﬁsh as ‘farmers’. The experiments also showed how the ﬁlamentous algae were so successful in blanketing hard surfaces that they inhibited the settlement and growth of encrusting CCA that are one of the main instruments of reef cementation (and main food of young A. planci—see above discussion). The author concluded that the reason that the damsel ﬁsh territories comprised loose rubble rather than ﬁrmly attached fragments was connected to the aggressive

behavior of the damselﬁsh that prevented other ﬁsh from cropping the ﬁlamentous algae. The settlement experiments also showed how small sessile invertebrates such as spirorbids were much less frequent among the cage protected weed-covered settlement plates than on those that had been exposed to reef grazers (Fig. 13.7).

Fig. 13.7 Impact of Stegastes nigricans (previously Pomacentrus lividus) on development of algal turf formed by ﬁlamentous algae. Continuous lines are plates protected by wire netting cages; broken lines are unprotected settlement plates. It is clear that within the Stegastes territory the cages have little or no impact because the pomacentrids are performing the same task of excluding herbivores as are the cages. Outside the damsel ﬁsh territories there is a marked difference between algal growth in protected (caged) plates and those accessible to reef herbivores

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Later studies on the impact of herbivory in damselﬁshes conﬁrmed the author’s observations (e.g. Jessen et al. 2014) and have thrown new light on the signiﬁcance of these ﬁsh in shaping reef form and invertebrate diversity (Lobel 1980, 1981; Schopmeyer and Lirman 2015; Gordon et al. 2015; Hiroki and Kato 2002). At the time of writing, over 240 research papers have cited the above research (Vine 1974) and, thanks to such studies, we now have a clearer understanding on the influential role that damselﬁsh can play in reef morphology and ecology. A paper by Lobel (1980) afﬁrms that scraping of the substrate by herbivores promotes the growth of corals and coralline algae by reducing the abundance of ﬁlamentous algae (Stephenson and Searles 1960; Dart 1972; Vine 1974; Wonders 1977). Competition between corals and algae on coral reefs has been investigated by McCook et al. (2001). Meanwhile, Rasher et al. (2012) are in no doubt that herbivorous ﬁsh are pivotal in reducing algal cover with its associated sedimentation whilst creating surfaces for settlement and growth of corals. They showed that removal of herbivores resulted in proliferation of macroalgal cover by 9–46 times, macroalgal biomass by 23–84 times and cyanobacteria cover by 0–27 times whilst decreasing cover of encrusting coralline algae by 46–100% and short turf algae by 14–39%. These results are in line with those recorded by the present author in his investigations on Harvey reef, Sudanese Red Sea (Vine 1974) and are reflected in the settlement plate image shown here. Meanwhile, Hata and Kato (2002) studied Stegastes nigricans on reefs in Japan where they found that its fastidious ‘gardening’ of its ‘algae farms’ resulted in a nearly monocultural mat of the erect ﬁlamentous rhodophyte, Womersleyella setacea. They found S. nigricans unusual in this regard with other herbivorous damselﬁsh maintaining more species rich ‘farms’. S. nigricans was observed to weed out the less digestible algae, leaving more space for the digestible W. setacea. Interestingly, Lobel points out that the pomacentrids he studied feed primarily on epiphytes rather than the alga itself since they lack cellulases or other enzymes capable of digesting plant cell walls. He also states that whilst the red algal mat may not constitute an actual food resource, it is important as a vital refuge for small invertebrates and its variation in size affects the area available for epiphytic growth. He also points to the fact that benthic invertebrates and demersal plankters live within the algal mat including juvenile crabs, snails, polychaetes, brittle-stars and others. Commenting on the author’s observations in the Red Sea (Vine 1974), Lobel stated “pomacentrids can be regarded as a detriment to the physical development of the reef framework” and “it is becoming increasingly clear that grazing ﬁshes (and other benthic rasping feeders) are important agents controlling spatial utilization and competitive

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outcomes among corals, algae and other benthic organisms”. Furthermore, Potts (1977) suggested that pomacentrids may be such decisive factors in reef ecology that they may be responsible for “exclusion of certain coral species from an otherwise favorable habitat”. Ceccarelli et al. (2005) studied three species of territorial damselﬁsh in a seasonally Sargassum dominated algal coastal zone at Magnetic Island in Queensland, Australia. They noted that these ﬁsh can play a signiﬁcant role in deﬁning reef dynamics on coral reefs because they frequently occupy a large proportion of the substratum— Pomacentrus tripunctatus, P. wardi and Stegastes apicalis occupied 60% of available surface in the area of their study. As with related species on Red Sea reefs, their presence promoted the abundance of algal food in their territories. They concluded that damselﬁsh “appear to readily co-exist with large unpalatable macroalgae as they can use them as a substratum for promoting the growth of palatable epiphytes.” It is clear that damselﬁsh and corals are uneasy bed partners and promotion of algal coverage (inhibiting coral settlement and growth) may not be the ﬁsh’s only impact on corals. Kaufman (1977) showed that Eupomacentrus planifrons from the Caribbean actively kills corals, thus expanding available areas for algal growth. In a zone where competition between corals and algae is intense, such damselﬁsh exert an “important influence on the outcome of competition between corals and algae”. Others reached similar conclusions on the impact on species diversity that pomacentrids can exert. Potts (1977) showed that corals became smothered by algae and sediment when placed in pomacentrid territories. Soft corals suffered a similar plight. On the other hand, Birkeland (1977) showed how grazing ﬁshes have an opposite effect, reducing ﬁlamentous algae, creating free spaces into which coralline algae and juvenile invertebrates such Acanthaster or corals can settle. Head (1987) re-emphasised the importance of balanced reef grazing on the recruitment and survival of reef corals: “The larvae [of corals] always require a hard algal-free substrate to settle, so it is important that new bare substrate be continually formed on reefs. In consequence there is a non-linear relationship between the rate of grazing by such animals as echinoids and the recruitment success of corals. Too little grazing and no bare substrate is available, too much and the newly settled spat are killed before they are properly established (Sammarco 1980)” (Fig. 13.8). It is becoming increasingly clear that grazing ﬁshes (and other benthic rasping feeders) are important agents controlling spatial utilization and competitive outcomes among corals, algae and other benthic organisms (Lobel 1980). A pomacentrid may be such a decisive factor as to be responsible for exclusion of certain coral species from an otherwise favorable habitat (Potts 1977).

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Fig. 13.8 A healthy coral reef where scleractinian corals and crustose coralline algae create a vibrant habitat for ﬁsh and invertebrates (© Sjoeholm)

It is now clear that turf algae (‘farmed’ by pomacentrids) promote sedimentation, negatively impacting larval settlement and early growth of coral recruits. The consequential impact on cover by corals and coralline algae has been well described by a number of researchers (e.g., Ceccarelli et al. 2006). Meanwhile, CCA—also obstructed by turf algae— are essential elements of healthy reefs, contributing to calciﬁcation and inducing larval settlement of many reef organisms such as corals, soft corals, echinoderms and gastropods. This is an area of coral reef research that can provide valuable insights into the processes at work on the reef, particularly with regard to the tendency for coral dominated reefs to shift toward algal domination (Figs. 13.9 and 13.10). Rasher et al. (2012) undertook ﬁeld experiments in adjacent areas where herbivorous ﬁsh were, on the one hand protected from ﬁshing, and on the other hand unprotected and scarce. They showed how corals developed much more successfully on the blocks that were exposed to grazing by the herbivores. The effects were not conﬁned to the algal turf created by ﬁlamentous forms. Their support for reef herbivores is unambiguous: “herbivores strongly suppress macroalgal colonization and growth, lessen damage to corals, and promote coral recruitment and growth”. Of particular interest from a management control viewpoint is that the presence of reef herbivores is of much greater signiﬁcance than moderately elevated levels of nutrients. Whilst lowering nutrient levels is unlikely to reverse a shift toward algal domination, increasing the density of herbivores on the reef is a possible tool to shift the balance in favour of corals, given time for their impact to be felt (Jessen et al. 2014). These effects are being recognized at more and more tropical sites around the globe and humans are frequently,

but not always, the culprits responsible, as a result of ignorance and/or lack of controls, for removing herbivores and bringing about the decline of reefs whose ‘health’ and diversity they depend on for food (Burke et al. 2011; Lewis 1986; Hughes 2010; Rasher et al. 2012; Burke et al. 2011). Lirman (2001) studied the impact that algae have on coral growth rates in the Caribbean, basically concluding that increased algae resulted in signiﬁcant slowing of coral growth. The mechanism by which algae suppress coral growth and survival seems to be that the algae release compounds that enhance microbial activity on live coral surfaces, causing mortality of corals and stimulation of further algal growth (Smith et al. 2006). An interesting study by Katie Barott and colleagues (Barott et al. 2009), utilizing hyperspectrometry, demonstrated that whilst the impact of fleshy algae on corals in the Line Islands creates a zone of hypoxia and altered pigmentation, the combination of corals and CCA is not accompanied by such a disturbance. This reflects the fact that such coralline algae are often present among reef building corals without any obvious negative impact on the corals, whereas the same cannot be said for the damage that turf or fleshy algae cause to reef building corals (Fig. 13.9). The above ﬁndings were conﬁrmed by Barott et al. (2011) who compared reactions of Montastraea annularis corals to the macro algae Dictyota bartayresiana and Halimeda opuntia, together with a mixed consortium of turf algae. They once again showed that contact between all of the above algae and the coral resulted in hypoxia on the adjacent coral tissue. However, CCA and M. annularis “did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of

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Fig. 13.9 Sargassum weed dominating on what was previously a coral dominated reef (© Sjoeholm)

Fig. 13.10 Sargassum weed often smothers reef building corals that are stressed by environmental factors (© Sjoeholm)

coral–CCA interactions was positively correlated with per cent coral cover”. In other words, a healthy reef can be expected to host extensive stands of CCA, subject to restrictions on farming ﬁsh such as Stegastes lividus which, as we have seen above, promotes development of algal turf and consequently discourages settlement of CCA. Barott and colleagues proposed “a model in which fleshy algae and some species of turf macroalgae alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy

algae a competitive advantage over corals when human activities, such as overﬁshing and eutrophication, remove controls on algal abundance.” prioritization of management approaches that protect critical processes, such as herbivory, that bolster coral reefs against phase-shifts to macroalgae should slow reef decline and facilitate coral recovery from the numerous stresses impacting present day reefs (Rasher et al. 2012).

What began for the author as an academic study of whether ﬁsh behaviour plays a signiﬁcant role in deﬁning

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reef structure has turned out to be a much more critical line of enquiry in terms of management and conservation of coral reefs and our ability to reverse what are increasingly frequent ‘phase shifts’ from coral dominated to algal dominated reefs.

Corals-V-Sponges and Ecological Impact of the Battle for Dominance A SCUBA diver’s view of Red Sea coral reefs inevitably reveals an intricate and varied, apparently haphazard, arrangement of surfaces created by a wide range of species. Among the predominant forms are corals, algae (including calcareous forms), Bryozoa and sponges. Pressed close to each other, they are in constant competition to occupy the available space, keeping their adversaries at bay, whether these be separate colonies of the same species or opposing taxa. Close study of the interface between these invertebrate rivals has always been a source of fascination to the author since there seemed to be little understood forces at play in both the manner of attack and defence. In his book, Red Sea Invertebrates (Vine 1986), the author describes observations of the coral-killing sponge, Terpios viridis (Figs. 13.11 and 13.12), in the Sudanese Red Sea. The species was originally described by Keller (1891) from specimens collected on corals in the Stylophora zone on reefs close to Suakin. During the author’s own survey of reefs in this region in 1975, he noted large tracts of a thin blue-grey slimy sponge literally blanketing sections of reefs. Closer inspection revealed that the sponge, identiﬁed as T. viridis, was extensively overgrowing corals and thus killing them. A series of photographs of the sponge coral interface, taken at regular intervals, demonstrated the alarming rate at which this was taking place. At one site the sponge extended its coverage to an area of 400 m2 during the summer months. This occurred at 15–20 m deep along a 40 m stretch of reef face on which virtually all the smothered corals were killed. Studies in Guam at that time, reported by Bryan (1973), described similar events with sponge growth rates on colonies of Porites coral at 2.3 cm per month. In the central Red Sea, maximum growth of Terpios occurred during summer months, from May to October (when coral growth was suppressed), with a distinct slowdown in winter when the affected corals seemed to have greater success in repelling the invasions. Galaxea coral appeared to have a greater ability to defend against Terpios, but no species was immune. Terpios was by no means the only sponge to threaten live corals—at least 15 encrusting species were recorded—including some other members of the family Suberitidae (to which Terpios belongs)—but it was the most proliﬁc. It was clear that damage to reef building corals caused by these aggressive sponges could be just as devastating to a

P. Vine

well-balanced reef as could an invasion of Acanthaster. Furthermore, both species may sometimes combine to the detriment of reef corals. Corals attacked by COTS could be more susceptible to sponge invasion than healthy corals that have an ability to ‘ﬁght back’. It is also worth noting that damage inflicted on live corals by Terpios viridis and related species is not conﬁned to the immediate impact of sponge-carpeted dead reefs. Once established, the sponge may persist for years and during this period resettlement of corals and possible reef recovery is delayed until more coral-conducive conditions return, accompanied by a breakdown of the sponge layer (Plucer-Rosario 1987). Whilst the macro view of corals and sponges ﬁghting it out on Red Sea reefs was engaging enough for this inquisitive biologist, it raised more questions than it answered. There was clearly a need to take a closer view of what was happening at the cellular level. Microscopic and biochemical studies on both corals and sponges, particularly at the leading edge of sponge encroachment, were undertaken by several researchers. Tang et al. (2011) examined this interface between the encrusting sponge Terpios and the corals that it killed. They suggested that the dominance of sponge over coral is established at the leading edge of the encrustation by extension of arm- or tube-like structures that create a ‘scaffold’ for subsequent sponge invasion. Whilst the invasion activity is concentrated at the interface, reaction in corals seems to be more general with the coral associated bacterial community undergoing changes depending on distance from the sponge-coral junction. The coral’s defence mechanisms are induced by those areas of coral in direct contact with the sponge where a high concentration of nematocysts was observed. The most lethal damage inflicted by Terpios sponges in their assault on corals may be the fact that they block out the light, preventing photosynthesis of the coral’s symbiotic algae. Rützler (2002) has reviewed the ecological impact of crustose clionid sponges on Caribbean reef corals, emphasizing that they can have a dramatic effect on coral coverage, particularly on stressed corals whilst virile colonies are mostly able to resist being overgrown by these sponges. Triggers for rapid sponge extension may come from temperature changes (warmer or colder), sedimentation, organic pollution and physical damage caused by ﬁsh, boat anchors or other means. These boring sponges excavate cavities below the coral surface, depriving colonies of their structural base, or simply overgrow dying colonies, blanketing out the light on which they depend. Non-boring sponges such as Terpios and Chondrilla may rapidly extend their growth over corals whose resistance has been weakened by pollution or by a range of other impacts, both natural and anthropogenic. Studies on reef associated sponges and soft corals have drawn the attention of the pharmaceutical industry. Vacelet

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Fig. 13.11 The invasive sponge, Terpios viridis attacks a coral colony. It is a battle that can be won by either side but corals under stress from other factors often fail to resist the sponge’s attack (© Sjoeholm)

Fig. 13.12 Chalinula saudiensis is a distinctive vivid blue sponge that has strong antiviral properties (© Sjoeholm)

et al. (2001) described Chalinula saudiensis (Fig. 13.12), a distinctive vivid blue sponge that has strong antiviral properties. Hassan et al. (2010) isolated compounds from the soft coral Cladiella pachyclados and evaluated them for their ability to inhibit growth, proliferation, invasion and migration of prostate cancer cells. They state that “some of the new metabolites exhibited signiﬁcant anti-invasive activity”. The impact of sponges on coral reefs remains an important topic for both ﬁeld and laboratory research, since sponges not only play a key role in the health of coral reefs, but they may also provide inspiration for life-saving

pharmaceutical medicines. The above observations are just a brief introduction, based on the author’s observations and interests.

General Reef Ecology and Conservation A ﬁeld study of 30 reef locations in the Sudanese Red Sea, conducted by the author over a four-year period (Vine and Vine 1980), emphasized the difﬁculty faced by biologists attempting to impose order over such a complex array of

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interconnected habitats. Notwithstanding the intricacies and pitfalls involved in comparing different habitats, a few features were regarded as suitable for data recording. These included biodiversity as displayed by distribution of reef ﬁshes, physical aspects of different reefs in vertical proﬁle, and growth rates of reef corals (Vine and Head 1977). In addition to these studies, the author also collected spirorbid tube worms as part of a taxonomic and zoogeographic survey of the group (Vine 1972). The main study was presented at the Symposium on Coastal and Marine Environment of the Red Sea, Gulf of Aden and Tropical Western Indian Ocean, whose results were published in the proceedings of that event (Vine and Vine 1980). Approximately 250 species of reef-associated ﬁsh were recorded during the work and their presence was noted at each transect. One hundred and ninety-two species were recorded in Suakin harbour alone. Forty settled fauna and flora types were recognised and logged on transect illustrations. Transects were made on reefs at Sanganeb (Fig. 13.13), Wingate, the Umbria wreck, Towartit and Suakin. Coral growth rates were measured for corals growing on the Conshelf 2 garage at Shaab Rumi reef (Fig. 13.14). Four reef types were present: fringing reefs, shallow patch reefs, barrier reefs and offshore reefs or atolls. Standard features of many offshore reefs were a shallow reef-top that drops steeply from close to the surface to about 8–10 m where it is followed by a gently inclined terrace sloping down to around 15 m, followed by a second steep reef face from about 15 m to 30 m. This is then followed by a second incline that culminates in a steeper slope extending into deep water beyond the reach of divers on normal mix compressed air. On south and north reef faces this pattern is often compressed into an almost vertical reef face reaching from close to the surface to 30 m with no intervening terrace. It is beside such steep, deep reef faces that the larger ocean pelagic species of ﬁsh were found, such as schools of scalloped hammerhead sharks and barracuda. A notable feature of the Sudanese Red Sea is Sanganeb atoll with its prominent lighthouse. The author’s description of its underwater habitats in the 1970s is one that still evokes a sense of wonder at how unspoiled the reefs were at that time. The sea around Sanganeb is always clear and the biotopes are varied and flourishing. Species range from typically oceanic ones such as large tuna, sailﬁsh, greater hammerhead sharks, and Carcharhinus longimanus to a wide range of reef dwelling species and lagoonal forms such as the delicately coloured Pseudochromis flavivertex and many invertebrates more typical of lagoons or harbours than of open-water coral reefs. There is a semi-resident school of dolphins, frequently sighted turtles and manta rays, schools of barracuda and a variety of migratory sharks and other large pelagic ﬁsh. In winter months, especially November to April, hammerhead sharks tend to form schools at

P. Vine the south-west and north-east points of the atoll. These may be observed at shallow depths, around 20 m, in the early morning (before 0900) or in the evening, immediately prior to sunset. During May and June, sailﬁsh are relatively common around the atoll and they enter the shallow water on top of the reef and in the lagoon. There is a peak of zooplankton during January and February when many of the planktivorous species appear to be most active…We have heard it described as one of the most magniﬁcent diving locations in the world (Figs. 13.15 and 13.16).

Monitoring the status of Red Sea reefs is a vital management task in terms of highlighting threats and mitigating their impact (Kotb et al. 2004; Götz et al. 2003). Klaus (2015) provides an interesting account of the less well-known reefs to the south, where conditions for coral growth are generally more challenging than in the central Red Sea areas of Sudan, Saudi Arabia, and some of the southern sections of Egypt and Jordan. Head (1980), Sheppard (1982), Sheppard and Sheppard (1991), and Sheppard et al. (1992) also provided valuable reviews of the diversity and zonation of reef building corals along the Red Sea’s coastlines, whilst a recent paper by Nasr (2015) concentrates on reefs in Sudanese waters and Bruckner and Dempsey (2015) summarise conditions for the Saudi Arabian reefs. Several authors have stated that the Red Sea offers ideal conditions for investigation of potential acclimatization or adaptation mechanisms in corals to some of the predicted scenarios implicit in climate change and ocean acidiﬁcation (Sawal and Al-Sofyani 2015). Cantin et al. (2010) studied the impact of surface sea temperature (SST) rise on coral growth, using Diploastrea heliopora. They demonstrated that growth rates were inversely proportional to SST and postulated that predicted sea temperature rise in the central Red Sea would impact severely on calciﬁcation rates of this and other Red Sea corals. Efforts to provide greater protection for Sudan’s coral reefs are taking place within the context of intensifying pressures and notable decline in certain areas. Reinicke et al. (2003) presented results of an eleven-year photographic study of selected transects at Sanganeb. They summarised the status of reef habitats in the Red Sea and the threats they faced: major local threats include land ﬁlls, dredging, sedimentation, sewage discharge and effluents from desalination plants, mostly around towns, cities and tourist development sites. There is local reef damage around major tourism areas, caused by people and boat anchors, along with other threats. Fish populations are declining in some areas, because of increased demand for and ﬁshing pressure on food and ornamental species. Destructive ﬁshing practices such as trawling in fragile habitats is increasing. There has been an influx of illegal ﬁshing vessels seeking to meet demands of the export market and more affluent and growing populations locally. The other major threats are from pollution and shipping accidents, and future bleaching. Monitoring these reefs is becoming increasingly important, as climate change and warmer waters near the limits for coral growth.

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Fig. 13.13 Sanganeb atoll reef with lighthouse (© Vine)

Fig. 13.14 Cousteau’s underwater garage is the remains of the Conshelf 2 project. It is an ideal structure for studying coral ecology (© Sjoeholm)

Meanwhile, Riegl et al. (2012) studied coral colony sizes over two decades and provided evidence that Red Sea reefs are already being affected by climate change. “Coral size, measured as corrected average intercept of corals in transects, had decreased from 1997 to 2009, after having remained constant from 1988 to 1997. Recruitment had remained stable (*12 juvenile corals per m2). Size distributions had not changed signiﬁcantly but large corals had declined over 20 years. Thus, data from a wide range of sites taken over two decades support claims by others that climate

change is indeed beginning to show clear effects on Red Sea reefs” (Riegl et al. 2012). Salam (2006) reviewed the state of affairs regarding Marine Protected Areas (MPAs) in the Red Sea in 2006. He stated that 12 MPAs were selected for a Regional Network of MPAs for the Red Sea and Gulf of Aden. These included two sites in Djibouti to the south, two sites in Egypt (Ras Mohammed National Park and Red Sea Islands), Aqaba Marine Park in Jordan, the Straits of Tiran bordered by both Saudi Arabia and Egypt, Al Wejh Bank and Farasan Marine

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Fig. 13.15 Manta ray ﬁlter feeding in the Red Sea (© Sjoeholm)

Fig. 13.16 Whale sharks are the world’s largest ﬁsh and are ﬁlter feeders (© Sjoeholm)

Protected Area in Saudi Arabia, Aibat and Saad ad-Din Islands in Somalia, Sanganeb National Park, Dungonab Bay and Mukkawar Island in Sudan together with sites in Yemen including Socotra Islands Group National Protected Area and the Bir Ali–Belhaf area. Some of these had already been established for some years whilst others were to be newly formed as protected areas. Approximately ten years later, on 17 July 2016, the World Heritage Committee declared eight new sites, including Sanganeb atoll and Dungonab Bay—Mukkawar Island Marine National Park. The committee noted that the designation applied to two separate areas: Sanganeb: “an isolated, coral reef structure in the central Red Sea and the only atoll, 25 km off the shoreline of Sudan. The second element of the property is made up of Dungonab Bay and Mukkawar Island, situated 125 km north of Port Sudan. It includes a highly diverse system of coral reefs, mangroves,

sea-grass beds, beaches and islets. The site provides a habitat for populations of seabirds, marine mammals, ﬁsh, sharks, turtles and manta rays. Dungonab Bay also has a globally signiﬁcant population of dugongs.” The move was widely welcomed by marine scientists who have long been aware of the unique fauna and flora of these areas. Up to date information on the park is available online at www.sudanmarineparks.info. It is clear however, that the mere designation of MPA status does not provide any guarantees that coral reefs will be protected from anthropogenic impact. All the author’s work to date, and the overriding conclusion of the present review, conﬁrms the interconnected nature of life on coral reefs. Remove reef grazers in the form of shallow reef ﬁsh such as parrotﬁsh or surgeonﬁsh (Fig. 13.17) and the consequences will soon be felt in terms of a phase shift from coral to algal dominated reefs. Along with that will come

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greater coverage by sponges, migration of coral eating ﬁsh and decline of predatory species—in other words, a whole chain of events that leads to a dramatic collapse in biodiversity on the reefs (Gladstone et al. 2003). Policy makers need to understand this and also to have faith in the positive impact that properly managed MPAs can initiate and sustain. Marine Parks in coral areas are only as good as the conservation that they achieve. They will only be successful in attracting visitors if they have extraordinary ‘coral gardens’ vibrating with colourful species. In order to achieve this, the priority is to establish programmes that arrest ecological decline and start to put the clock back in terms of biodiversity. It sounds like an impossible dream but it has already been achieved in some cases and there are signs that much more can be achieved in the coming years. The methodology and efﬁcacy of MPAs in promoting reef building corals rather than blanketing seaweeds is discussed in some detail by a number of authors (Burke et al. 2011; Carilli et al. 2009; Knowlton and Jackson 2008; Mumby and Harborne 2010; Selig and Bruno 2010 and Burke et al. 2011). Their ﬁndings all reiterate the important role played by herbivorous reef ﬁshes and unanimously recommend that protection of these species should be a ﬁrst line of defence in terms of MPA management. Given the inextricable connection between reef herbivores and reef health there is an inescapable requirement to protect the ﬁsh communities that keep reefs healthy and can start the ball rolling in terms of reef recovery (Burke et al. 2011). This means that ‘no take’ rules are at the top of the list of conservation priorities in MPAs set up within coral reef areas.

Fig. 13.17 Surgeon ﬁsh Acanthurus sohal are herbivores and detritivores constantly picking at the shallow reef surface, usually near the reef crest (© Sjoeholm)

233

Mora et al. (2006) reviewed the global situation with regard to Marine Protected Areas around the world and concluded that whilst some ‘worked’, overall there was an urgent need for reassessment and room for considerable improvement. They created a veriﬁed database containing 980 MPAs and 98,650 km2 (18.7%) of the world’s coral reef habitats. Based on levels of poaching “as an indirect measurement of management performance”, they found that only “88 coral reef MPAs covering 1.6% of the world’s coral reefs are managed in such a way as to prevent such activities.” This does not mean that MPAs are not effective management tools. It does, however, indicate that the vast majority of MPAs are not being effectively managed. Creation of no-take areas is never a popular measure until the beneﬁts of such measures trickle through to ﬁshermen who realize that the stocks on which they depend are slowly recovering, thanks to restrictions imposed by the marine park authorities. Establishment of effective marine parks requires vision, scientiﬁc support, regional coordination and community leadership together with government facilitation/legislation, ﬁnancial resources and multi-party commitment. Public awareness is an essential tool to achieve these goals. Selig and Bruno (2010) found that MPAs can be very effective in maintaining stable coral cover. “MPA beneﬁts may appear modest in the short term, but over several decades could lead to large and highly ecologically signiﬁcant increases in coral cover as the cumulative importance of small annual effects becomes more important and the

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number of years of MPA protection increases. However, it remains to be seen whether the observed beneﬁts of MPAs are sufﬁcient to offset coral losses from major disease outbreaks and bleaching events, both of which are predicted to increase in frequency with climate change. Given the time lag for maximizing MPA effectiveness, implementing new MPAs and increasing enforcement should help maximize the ability of MPAs to prevent future coral loss”.

Taxonomy of Red Sea Marine Life Much of the marine biological research in the Red Sea has had a taxonomic bias—collecting, recording, preserving, describing and naming new species of ﬁsh and invertebrates. Given the high degree of endemicity in the Red Sea, it has provided rich pickings for enthusiastic amateurs and dedicated professionals alike. Indeed, the dividing line between hobbyists and experts has frequently been blurred by the cooperation that takes place between amateur collectors and professional taxonomists. Among ﬁsh experts one particular ichthyologist deserves special mention: Dr. J. E. Randall. The author was fortunate enough to welcome Dr. Randall on his ﬁrst visit to Sudan and to dive with him on numerous occasions when he was building up his ﬁrst-hand knowledge of Red Sea reef ﬁshes. An illustrated summary for the general public was ﬁrst published by Randall (1983). Jack Randall, as he is best known, has described over 799 new ﬁshes and more coral-reef species than anyone else in history. He has authored over 906 publications in marine biology, nine of which are regional guides on the ﬁshes of the Caribbean Sea, Hawaiian Islands, Red Sea, Oman, and Great Barrier Reef of Australia. Since 1970 he has been senior ichthyologist at the Bishop Museum, Honolulu. The present author described four new species of serpulids (Polychaeta) from the Red Sea including a new genus and new subgenus. Within a small group of probably twenty or so active serpulid taxonomists spread across the globe, these were signiﬁcant discoveries, but beyond that highly specialized interest group there was no impact whatsoever. Those of us that have contributed to the task of identifying, classifying, describing and naming the seemingly inexhaustible array of species with which we share the planet are increasingly aware that taxonomy is entering a period of rapid change, becoming less subjective or intuitive and more formulaic in nature. DNA does not lie. Genetic analysis provides deﬁnitive evidence for the process of separation and speciation. This involves new skill sets that differ from those of traditional taxonomy. Meanwhile, fewer and fewer specialized taxonomists are engaged in this science and as these people retire, unique skills and knowledge are being lost.

P. Vine

The situation is further complicated by the relatively recent discovery of the phenomenon of cryptic-speciation (Bickford et al. 2006), whereby individuals previously assigned to a single species have sufﬁciently distinct genetic make-up for them to be regarded as different species. An example of this is provided by the grouper Cephalopholis hemisktos which occurs in the Red Sea/Gulf of Aden as well as the Gulf of Oman/Arabian Gulf. The two populations have been isolated from each other for more than 800,000 years and have developed differences in pectoral ﬁn size, pectoral ﬁn ray count, oblique scale rows and asymptotic size (Randall and Ben-Tuvia 1983; Priest et al. 2016). Given the high levels of endemicity in the Red Sea (14% in ﬁshes according to Randall 1994), a function of its Pleistocene exposure to dramatic shifts in sea levels and sea temperatures, together with restricted access via the Straits of Bab al Mandeb, we can expect to ﬁnd many cases of cryptic-speciation across a wide range of the marine fauna of the region. In an article published in Bioscience, Lisa Drew (Drew 2011) discussed the threatened ‘extinction of taxonomists’. The ﬁgures are astounding and daunting! Almost two million species have been identiﬁed. In 2008 the ﬁgure was actually 1,922,710. In that year alone researchers newly described and named 18,225 living species (2010 State of Observed Species Report, University of Arizona). The decade-long Census of Marine Life, which ended in 2010, estimates that the ocean holds more than one million marine species, excluding microbes. The task of recognizing, describing and preserving the holotypes and paratypes, depositing them in museums and publishing this work is overwhelming. It is also, on a broad scale, inadequately valued or funded. As a result of climate change and our impact on nature, threatened communities in the Red Sea may be destroyed before their unique species are even recognized (Hobbs et al. 2011). The question is, does this really matter? It is a debate that needs to take place among scientiﬁc organisations before it is too late to turn back the clock. Acknowledgements Since this chapter covers most of my marine biological research in the Red Sea there are many people to whom I wish to express my gratitude but space does not allow an exhaustive listing. Academic support and encouragement for my work with serpulids and Acanthaster planci was provided by Professor E.W. Knight-Jones and by Dr. Phyllis Knight-Jones. I am grateful to the International Rotary Foundation for a fellowship that enabled me to spend a year at James Cook University in Queensland Australia, and to Swansea University College (Wales) and University College Galway (Ireland) where I wrote up much of my research whilst initially studying for a Ph.D. and later working as a post-doctoral fellow. My introduction to, and exploration of the Red Sea was facilitated by the Cambridge Coral Starﬁsh Research Group led by Dr. Rupert Ormond. I later joined Khartoum University and Suakin Marine Laboratory and

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it is a pleasure to acknowledge the friendship and support of my Sudanese academic colleagues including Dr. Dirar Nasr and Dr. Yousef Abu Gideiri, together with a number of active contributors to the Sudanese marine ﬁeld, especially Captain Abdel Halim Hamid. I would also like to mention Sheikh Gazi Zainy and Immel Publishing for publishing four of my Red Sea books; Michael McKinnon for the opportunity to assist in production of both books and ﬁlms on the Red Sea; and Robin Lehman for introducing me to large format underwater ﬁlming in the Red Sea. This chapter owes its genesis to Dr. Najeeb Rasul and Dr. Dirar Nasr, both of whom persisted in asking me to summarise my Red Sea research for this publication. I would also like to acknowledge the photographic contribution of Hans Sjoeholm. Finally, I owe a huge debt of gratitude to my wife, Paula and daughters, Catriona, Sinead and Megan who have participated in, supported and encouraged my research and writing about the Red Sea and its marine life.

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Red Sea Research: A Personal Perspective

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237 Stephenson W, Searles RB (1960) Experimental studies on the ecology of intertidal environments at Heron Island. I. Exclusion of reef ﬁsh from beach rock. Australian J Marine Freshwater Res 2:241–267 Tang SL, Hong MJ, Liao MH, Wann-Neng J, Chiang PW, Chen CB, Chen CA (2011) Bacteria associated with an encrusting sponge (Terpios hoshinota) and the corals partially covered by the sponge. Environmental Microbiol 13(5):1179–1191 Uthicke S, Pecorino D, Albright R, Negri AP, Cantin N, Liddy M, Dworjanyn S, Kamya P, Byrne M, Lamare M (2013) Impacts of ocean acidiﬁcation on early life-history stages and settlement of the coral-eating Sea Star Acanthaster planci. PLoS ONE 8(12):e82938. https://doi.org/10.1371/annotation/b03dc5d7-0cfd-4182-b39dfb9299275d5c Uthicke S, Logan M, Liddy M, Francis D, Hardy N, Lamare M (2015) Climate change as an unexpected co-factor promoting coral eating seastar (Acanthaster planci) outbreaks. Sci Reports 5:8402. https:// doi.org/10.1038/srep08402 Vacelet J, Al Sofyani A, Al Lihaibi S, Kornprobst J-M (2001) A new haplosclerid sponge species from the Red Sea. J Marine Biol Assoc UK 81(6):943–948 Vine PJ (1970) Field and laboratory observations of the Crown of Thorns starﬁsh, Acanthaster planci. Nature 228:341–342 Vine PJ (1972) Spirorbinae (Polychaeta: Serpulidae) from the Red Sea, including descriptions of a new genus and four new species. Zool J Linnean Soc 51(2):177–201 Vine PJ (1973) Crown of Thorns (Acanthaster planci) plagues: The natural causes theory. Atoll Res Bull 166:1–10 Vine PJ (1974) Effects of algal grazing and aggressive behaviour of the ﬁshes Pomacentrus lividus and Acanthurus sohal on coral-reef ecology. Marine Biol 24(2):131–136 Vine PJ, Head SM (1977) Growth of corals on Commander Cousteau’s underwater garage at Shaab Rumi (Sudanese Red Sea). Jeddah Nature J, pp 6–17 Vine PJ, Vine MP (1980) Ecology of Sudanese coral reefs with particular reference to reef morphology and distribution of ﬁshes. Proc Symp on The Coastal and Marine Environment of the Red Sea, Gulf of Aden and Tropical Western Indian Ocean. Khartoum, 9–14 Jan, University of Khartoum Vine P (1986) Red Sea Invertebrates. Immel Publishing, 224 pp Vine P, Schmid H (1987) Red Sea Explorers. Immel Publishing, 206 pp Vogler C, Benzie J, Lessios H, Barber P, Wörheide G (2008) A threat to coral reefs multiplied? Four species of crown-of-thorns starﬁsh. Biology Lett 4(6):696–699 Wolfe K, Graba-Landry A, Dworjanyn SA, Byrne M (2017) Superstars: Assessing nutrient thresholds for enhanced larval success of Acanthaster planci, a review of the evidence. Marine Pollution Bull. https://doi.org/10.1016/j.marpolbul.2016.12.079 Wonders JBW (1977) The role of benthic algae in the shallow reef of Curaco (Netherlands Antilles). III. The signiﬁcance of grazing. Aquatic Botany 3:357–390 Yamaguchi M (1973) Recruitment of coral reef asteroids, with emphasis on Acanthaster planci (L). Micronesica 9(2):207–212 Yokochi H, Ogura M (1987) Spawning period and discovery of juvenile Acanthaster planci (L.) (Echinodermata: Asteroidea) at northwestern Iriomote-Jima, Ryukyu Islands. Bull Marine Sci 41(2):611–616 Zann L, Brodie J, Berryman C, Naqasima M (1987) Recruitment, ecology, growth behaviour of juvenile Acanthaster planci (L) (Echinodermata: Asteroidea). Bull Marine Sci 41(2):561–575

Endemic Fishes of the Red Sea

14

Sergey V. Bogorodsky and John E. Randall

Abstract

The Red Sea is characterised by a unique composition of species of ﬁshes which, based on unpublished data of the present authors, currently consists of 1166 species from 159 families whose habitats range from shallow waters to the deep sea. There is a total of 1120 species in coastal waters of the Red Sea recorded within an overall depth range 0–200 m; among them, 165 species are exclusively endemics to the Red Sea, whilst another 51 species are restricted to the Red Sea and Gulf of Aden only, and 22 species living at depths greater than 200 m are endemic. As the westernmost peripheral area of the Indo-West Paciﬁc region, the Red Sea is at the opposite end of the distributions of many widespread coral reef organisms that range to the easternmost regions, such as the Hawaiian Islands, Easter Island, and the Marquesas Islands. It is noted that these areas exhibit high percentages of endemism among coastal ﬁshes. The Hawaiian archipelago has 30.7% of its ﬁshes as endemic species; Easter Island has 21.7%, the Red Sea 14.7% (19.3% when combined with the Gulf of Aden), and the Marquesas Islands have 13.7% endemic ﬁshes. The Red Sea is 2250 km in length and it is very deep, with an average depth of 490 m, and a maximum depth of 3040 m. As expected, the ﬁsh fauna is far from homogeneous. The most divergent sector is the Gulf of Aqaba. We have noted that its entrance to the rest of the Red Sea is shallow. It has a maximum width of only 24 km, but a maximum depth of 1850 m. The shore drops off quickly to deep water. The prevailing cross wind creates upwelling, resulting in surface sea temperature at least S. V. Bogorodsky (&) Senckenberg Research Institute and Natural History Museum Frankfurt, Senckenberganlage 25, 60325 Frankfurt Am Main, Germany e-mail: [email protected] J. E. Randall Bishop Museum, 1525 Bernice St, Honolulu, HI 96817-2704, USA

as low as 21 °C. Twenty-two of 46 species of Red Sea ﬁshes living at depths greater than 200 m in the Red Sea are endemic (48% endemism). The Gulf of Aqaba has 22 endemic coastal species of ﬁshes and eight endemic deep-dwelling species. By contrast, the neighboring Gulf of Suez, with extensive sand flats and a maximum depth of 70 m, has only seven endemic species of ﬁshes. Of the 165 endemic Red Sea species of ﬁshes, only two are elasmobranchs. Twenty-three families of Red Sea ﬁshes have more than 20% of endemic species with the highest rates of endemism occurring among the Pseudochromidae, Schindleriidae (83.3% and 100% respectively) and the family Gobiidae with the greatest number of endemic species (36 of 139 recorded species). A brief summary of the history of scientiﬁc research on Red Sea ﬁshes is provided together with complete lists of endemic species for (i) the entire Red Sea (separately for coastal and deep-dwelling ﬁshes); (ii) the Red Sea combined with the Gulf of Aden; (iii) the Gulf of Aqaba and the Gulf of Suez; and (iv) Lessepsian migrants. Ongoing research is likely to reveal additional endemic species in the region.

Introduction The origin and composition of the ﬁsh fauna of the Red Sea is best understood with knowledge of the geologic history of the sea, beginning with the plate tectonics of the region. During the Eocene, 40 million years ago, the Arabian Plate (including what is now the Arabian Peninsula) began to drift to the east from the plate on the African side known as Nubia at the rate of 1–2 cm per year. This separation (termed a rift) continued to the north, through what is now the Gulf of Aqaba, and created the Dead Sea. It also ranged to the south, resulting in the Great Rift Valley and the formation of the Great Lakes of East Africa. The rift of what was to become the Red Sea remained dry until 20 million years ago in the Miocene when the sea poured in from the Mediterranean part

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_14

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of the Tethys Sea. The rift expansion continues today, and given enough time, the Red Sea will become an ocean (Rasul et al. 2015). Five million years ago during the Pliocene, the northern end of the Red Sea uplifted, and the southern subsided, resulting in the Red Sea becoming a part of the Indo-Paciﬁc region. Corals, other invertebrates, marine plants, and ﬁshes from the Indian Ocean then colonized the Red Sea. During the Pleistocene Ice Ages from two million years to 10,000 years ago, the sea level of the Red Sea was lowered as much as about 130 m. The maximum depth of the Red Sea is about 2900 m, and the average depth is 490 m, so a lowering of 130 m would seem insigniﬁcant. However, the Hanish Sill near the narrow southern entrance to the Red Sea called Bab-al-Mandab has a depth at present of only 137 m. Thus, Pleistocene falls in sea level created a barrier between the Red Sea and the Gulf of Aden whilst the narrow and relatively shallow Strait of Tiran restricted water exchange between the Gulf of Aqaba and the Red Sea proper. With each ice age, the cycle repeated, and with each cycle the opportunity arose for marine species in the Red Sea to evolve independently from the Indian Ocean stock from whence they came. The sea level has been stable for about the last 5000 years, but the present burning of fossil fuels and the destruction of forests have accelerated the melting of the polar ice caps, causing an alarming rise in sea level, especially to population centres barely above sea level (Lieske and Myers 2004). Mention should be made of the impact of the Suez Canal on the ichthyofauna of both the Red Sea and the Mediterranean Sea. With the opening of the canal in 1869, the opportunity was provided for marine life to move from south to north and vice versa. The greatest movement of ﬁshes has been the former, with 57 Red Sea species reported as established in the Mediterranean Sea (Golani et al. 2002). Currently that number has increased to 106 species, so-called Lessepsian migrants, that have thus far colonized the Mediterranean. By contrast, only 12 Mediterranean species have been discovered in the northern Red Sea (Dor 1984). We present here a brief historical review of the systematic research on ﬁshes of the Red Sea. The ﬁrst widely accepted classiﬁcation of the animal life of Planet Earth is the ﬁrst volume of the tenth edition of “Systema Naturae”, written by the Swedish naturalist Carl Linnaeus, and published in 1758. Linnaeus was mainly a botanist. The part on ﬁshes was written for him by his friend Peter Artedi; they had been students together at the University of Uppsala in Sweden. We have found only one ﬁsh species from “Mari rubro” in this tome, referred to as “Chaetodon nigricans”. The description includes a sharp spine on each side at the base of the caudal ﬁn and nine dorsal spines. These characters readily link the ﬁsh as the oldest name for the common Red Sea surgeonﬁsh Acanthurus gahhm (Forsskål 1775).

S. V. Bogorodsky and J. E. Randall

Acanthurus nigricans is itself distributed from the Andaman Sea in the eastern Indian Ocean to Tonga in the western Paciﬁc Ocean. Fifty-eight species of Red Sea ﬁshes were described in 1775 by Peter Forsskål from Finland. He led a six-man Danish scientiﬁc expedition to the Red Sea in 1762. Five of the men died during the expedition, including Forsskål who succumbed to malaria in Yemen. The survivor, Carsten Niebuhr, brought Forsskål’s notes back to Denmark and edited the manuscript for publication. Ninety-nine of the skins were deposited in the Zoological Museum of Copenhagen. Klausewitz and Nielsen (1965) published photographs and x-rays of the surviving 69 skins of the Forsskål ﬁsh collection. Fricke (2008) detailed the history, authorship and taxonomic identity of species described in Forsskål’s work. In 1822, Dr. Eduard Rüppell of the Senckenberg Museum in Frankfurt collected ﬁshes in the Red Sea. During the period 1828–1830, he published “Fishes des rothen Meeres” in his “Atlas zu der Reise im nordischen Afrika”. Of 161 species accounts of ﬁshes, 75 were new to science. After more ﬁeld work in the Red Sea in 1831, his “Fische des rothen Meeres in Neue Wirbelthiere zu der Fauna van Abyssinien Gehorig” was published in four parts (1835– 1838), describing 164 species, 100 of which were new. At the same time that Rüppell was in the Red Sea, two more Germans, CG Ehrenberg and FG Hemprich, were collecting ﬁshes. Hemprich died in Massawa, Eritrea; Ehrenberg brought back a large collection of plants and animals to Berlin. He made the ﬁshes available to the famous Baron Georges Cuvier and Achille Valenciennes for their monumental 22-volume “Histoire naturelles des poisons” (Cuvier & Valenciennes 1828–1847); they attributed the authorship of Ehrenberg’s specimens to him. They also described other species from outside the Red Sea that were later found to range into the sea. Beginning from 1864, the German physician Carl Klunzinger commenced a ﬁve-year study of Red Sea ﬁshes in Egypt, which culminated in 1870–1871 with his “Synopsis der Fische des Rothen Meeres”; it contained 520 species. Three more years of ﬁeld work in Egypt, commencing in 1872, and subsequent research on the specimens, resulted in the publication of the ﬁrst part of his “Die Fische des Rothen Meeres” (1884) that contained 261 species; the second part was not published. Since Klunzinger, many people have collected ﬁshes in the Red Sea, and numerous scientiﬁc papers have been published on Red Sea ﬁshes, including four checklists (Botros 1971; Dor 1984; Goren and Dor 1994; Golani and Bogorodsky 2010). Dor (1984) listed almost 1000 species. Ten years later, Goren and Dor (1994) updated this checklist, adding another 250 species. They failed, however, to verify published records and their list contained numerous errors, improved by Golani and Bogorodsky (2010) in their revised

14

Endemic Fishes of the Red Sea

241

Table 14.1 Authors who described Red Sea ﬁshes Dates

Author

Number of valid species described from the Red Sea

Number of Red Sea endemic, depth 0–200 m

Number of Red Sea deep-water species, depth below 200 m

1828–1837

Rüppell

97

30

–

1775

Forsskål

93

6

–

1972–2017

Randall

52

38

1

2010–2018

Bogorodsky

32

29

–

1870–1884

Klunzinger

32

10

4

1828–1840

Cuvier and Valenciennes

24

7

–

1984–2018

Golani

20

12

5

1959–2000

Klausewitz

20

6

6

1980–2018

Fricke

15

12

3

1978–1995

Goren

13

8

2

1971–1988

Springer

6

4

–

checklist, reducing the number of species to 1078, in 154 families, 25 orders, and two classes. Since their publication many species new for science and new for the Red Sea were reported from the Red Sea, raising the number of species to 1166 (Eschmeyer et al. 2018 and unpublished authors’ data). The second author wrote a book entitled “Red Sea Reef Fishes” that was published in 1983 by Immel Publishing, based in London. The book includes 325 species, illustrated with 446 colour illustrations. The book “Fishes of the Gulf of Aqaba” by Maroof A. Khalaf and Ahmad M. Disi, also well illustrated in colour, was published in 1997 by the Marine Science Station in Jordan (Khalaf and Disi 1997). It demonstrated that the ﬁsh fauna of the Gulf of Aqaba is not the same as the rest of the Red Sea. Like the Red Sea, it is very deep, despite being very narrow by comparison. However, it is shallow at its entrance in the Strait of Tiran. As mentioned above, when the sea level was low, as during the Pleistocene, the Gulf of Aqaba was isolated from the rest of the Red Sea. Helmut Debelius’s popular book “Red Sea Reef Guide” was published in Debelius (1998) and included about 500 species of ﬁshes and invertebrates. One of the most useful identiﬁcation guides to Red Sea marine life is “Coral Reef Guide Red Sea”, with a subtitle: “The deﬁnitive guide to over 1200 species of underwater life”. It was written by Ewald Lieske and Robert F. Myers and published in 2004 by Harper Collins, London. A surprising number of new species of ﬁshes has been described from the Red Sea in recent years. Most have been small ﬁshes, especially those of the family Gobiidae, and some are species from deep water. Table 14.1 provides a list of the ichthyologists who have described more than ﬁve valid new species of Red Sea ﬁshes. It should also be noted that among the current authors, John E. Randall described about 800 valid species from the Indo-West Paciﬁc, 63 of which occur in the Red Sea. Indeed, for 52 of Randall’s

species the holotype was designated from the Red Sea, whilst in seven cases the paratype was from the Red Sea, and the remaining four species were described outside the Red Sea. This account would be incomplete without mentioning the signiﬁcant contribution to our knowledge of Red Sea and Indo-Paciﬁc ﬁshes made by Dr. Pieter Bleeker, from 1847 to 1865, who described 1373 new species, of which 571 are considered as valid, 68 of them ranging to the Red Sea. Most of his new ﬁshes were described from specimens of wide-ranging species that he collected in the East Indies.

Discussion Based on recent unpublished data of the present authors there are 1166 ﬁsh species from 159 families recorded from shallow to deep waters in the Red Sea. In many respects, there are marked differences between species occurring in coastal waters (above 200 m depth) and those living deeper than 200 m. A total of 1120 Red Sea ﬁsh species in 143 families and 26 orders are known from depths above 200 m (Bogorodsky, Randall and Krupp unpublished). More than half of the families are represented by one to three species only. Families with the greatest number of species are: Gobiidae (139 spp.), Labridae (65 spp.), Apogonidae (60 spp.), Serranidae (41 spp.), Blenniidae (40 spp.), Carangidae (39 spp.), Muraenidae (38 spp.), Pomacentridae (34 spp.), and Syngnathidae (32 spp.). All other families have fewer than 30 species. Compared to other marine regions, the rate of endemism is extremely high (the third highest in the world, see Table 14.2); our latest revised percentage of endemic Red Sea ﬁshes is 14.7% (i.e. 165 species listed in Table 14.3). Examples of Red Sea endemics are shown in Figs. 14.1, 14.2, 14.3, 14.4, 14.5, 14.6, 14.7 and 14.8.

242

S. V. Bogorodsky and J. E. Randall

Table 14.2 Percentage of endemism in different areas of the world Locality

Number of coastal ﬁshes

Percentage of endemic species (%)

References

Hawaiian Islands

570

30.4

This paper

Easter Island

139

21.7

Randall and Cea (2011)

Red Sea

1120

14.6

This paper

Marquesas Islands

597

13.7

Delrieu-Trottin et al. (2017)

Galápagos Islands

550

13.6

McCosker and Rosenblatt (2010)

Ascension Island

82

11.0

Floeter et al. (2008)

East Indies1

2631

10.6

Allen and Erdmann (2012)

Cocos Is., Costa Rica

264

10.2

Garrison (2005)

New Caledonia

2320

4.6

Fricke et al. (2011)

Mascarene Islands

1022

3.5

Fricke (1999)

Marshall Islands

817

850 m. This behaviour might represent previously unreported daytime foraging events within and below deep scattering layers (Spaet et al. 2017). Both diving studies provide evidence that mesopelagic habitats might be more commonly used by Whale and Scalloped hammerhead sharks than previously suggested. Additional research aimed at resolving the ecological, physiological and behavioural mechanisms underpinning vertical movement patterns of sharks in the Red Sea is clearly warranted. In the Egyptian Red Sea, a long-term citizen-science project has been conducted since 2004 focussing on photo-identiﬁcation of Oceanic whitetip sharks (Carcharhinus longimanus). This project has led to the identiﬁcation of over 800 individuals and an average of 25% re-sightings by 2017 based on 35,000 images and videos, indicating strong site attachment of this species to particular Red Sea reefs (Bojanowski unpublished data). In 2010, image collection expanded to Grey reef and Silky sharks, resulting in close to 3000 Grey reef and 1200 Silky shark photographs collected over a period of six years (Bojanowski unpublished data). Additionally, a shark-monitoring programme was initiated in 2010, recording shark sightings on recreational dives conducted in the Egyptian Marine Parks and other drop-off reefs. Species most commonly encountered by divers in Marine Parks were Grey reef, Oceanic whitetip, Pelagic thresher (Alopias pelagicus), Whitetip reef, and Scalloped hammerhead sharks (often in schools of up to 30 individuals). Silky, Whale and Tiger sharks (Galeocerdo cuvier) were only rarely recorded (Bojanowski unpublished data).

Grey reef, Scalloped hammerhead, Silky, and Whitetip reef sharks were among the most commonly encountered species in the central Red Sea of Saudi Arabia and Sudan, based on Baited Remote Underwater Video systems (BRUVs) (Fig. 15.2) and longline surveys (Clarke et al. 2012; Spaet et al. 2016). Between 2011 and 2013, both survey methods were opportunistically employed at central and southern Saudi Arabian Red Sea reef systems with the aim of collecting distribution and abundance data on Red Sea sharks and rays (Spaet et al. 2016). In addition, BRUVs were deployed in the northern Saudi Arabian Red Sea and at selected reef systems in Sudan. The ﬁndings revealed shark Catch Per Unit Effort (CPUE) estimates one to nearly two orders of magnitude lower for both survey methods in the Saudi Arabian Red Sea compared to other reef systems around the world (Spaet et al. 2016). In contrast, BRUVs CPUE values from relatively undisturbed Sudanese reefs were within the range of estimates from other locations where sharks are considered common (Spaet et al. 2016). These results suggest that decades of heavy ﬁshing pressure have signiﬁcantly altered the community structure of many Red Sea reef systems, but also show that marine protected areas [e.g., Sanganeb Marine National Park (PERSGA 2006)], have the potential to harbour relatively healthy shark populations. Elsewhere, the deployment of pelagic drift BRUVs (Santana-Garcon et al. 2014) has resulted in sightings of pelagic species in relatively high numbers (Meekan and Cappo 2004; Santana-Garcon et al. 2014). In the central Red Sea, on the contrary, this approach did not result in any shark sightings (Spaet et al. 2016). The apparent lack of pelagic shark species in offshore reef areas of the central Red

15

Red Sea Sharks—Biology, Fisheries and Conservation

273

Fig. 15.2 Images of shark encounters from Baited Remote Underwater Video system (BRUVs) surveys conducted in the Saudi Arabian Red Sea (a) Nurse shark (Nebrius ferrugineus); (b) Zebra shark (Stegostoma fasciatum)

Sea, compared to the north-western basin, suggests an uneven distribution of those animals throughout the Red Sea, especially regarding the absence of Oceanic whitetip and Pelagic thresher sharks, which are commonly observed in Egypt. Based on IUCN Red List criteria, Oceanic whitetip and Pelagic thresher sharks are regionally listed as Critically Endangered and Endangered, respectively (Jabado et al. 2017). This further highlights the immense importance of Egyptian reefs to the conservation of these species. Differences in the spatial distribution of shark diversity may be related to the pronounced north-south gradients in environmental parameters and habitat structure characterizing this narrow ocean basin; for example, biophysical gradients have been shown to influence assemblage structure and population genetic patterns in coral reef ﬁshes (Roberts et al. 1992; Nanninga et al. 2014).

Population Genetics Many of the shark taxa in the Arabian region are genetically distinct from their closest relatives in neighbouring areas (Naylor et al. 2012; Henderson et al. 2016). Furthermore, a number of global and range-wide studies on several shark species, including samples from the Red Sea, demonstrated substantial genetic differentiation between the Red Sea and widely separated Indo-Paciﬁc locations in Blacktip reef sharks (Delser et al. unpublished data), as well as a strong separation between Indo-Paciﬁc and Atlantic clades for Blacktip reef (Vignaud et al. 2014b), Silky (Clarke et al. 2015), Spot-tail (Giles et al. 2014) and Whale sharks (Schmidt et al. 2009; Vignaud et al. 2014a). Despite the evident distinctiveness of this region, only one study to date has speciﬁcally focussed on the genetic population structure of sharks around the Arabian Peninsula. Spaet et al. (2015) investigated the genetic population structure of four commercially exploited shark species between the Red Sea, the Gulf of Aden, the Gulf of Oman and the Arabian Gulf. The four species studied, Blacktip (Carcharhinus limbatus), Milk (Rhizoprionodon acutus), Scalloped hammerhead and

Spot-tail shark, differ markedly in their ecological, morphological, life-history and distributional patterns. Yet, results indicate that there are no contemporary barriers to gene flow across the study region for any of the species (Spaet et al. 2015). The apparent similarity of connectivity patterns across species with vastly different biological characteristics indicates that populations of other shark species may also function as common stocks across all ocean basins surrounding the Arabian Peninsula. Given current harvesting levels, this is a concerning situation, as unregulated exploitation in one or several countries is likely to cause uniform depletion across the entire stock.

Fisheries There has been a long history of shark ﬁshing in the Red Sea (Ben-Yami 1964). Although there is no directed commercial shark-ﬁshery, local populations have been heavily exploited by artisanal ﬁshers since the mid-1970s (Bonﬁl 2003). No quantitative ﬁsheries resource surveys have been carried out in any of the Red Sea states, but minor surveys were irregularly conducted in the 1960s–1980s (see summary in Sanders and Morgan 1989). These surveys showed that catches, particularly by gillnets, were often dominated by sharks, particularly in Saudi Arabia, Somalia and Sudan. Yet, regional as well as international markets for sharks were still underdeveloped at that time, resulting in most sharks being discarded. Since then several Red Sea countries, including Djibouti, Saudi Arabia, Sudan and Yemen, have shown signs of depleted shark populations (Hariri et al. 2002; Bonﬁl 2003; Spaet et al. 2016). Potential over-exploitation of Red Sea shark resources was suggested by a multidisciplinary evaluation of the “health” and sustainability of artisanal Red Sea shark ﬁsheries (Tesfamichael and Pitcher 2006), which also indicated that those ﬁsheries were as proﬁtable as large scale industrial ﬁsheries (e.g., trawl, shrimp and longline ﬁsheries). While country-speciﬁc information on population declines is rare, local over-exploitation has recently been suggested for shark

274

J. L. Y. Spaet

Fig. 15.3 Landings of juvenile Spot-tail sharks (Carcharhinus sorrah) at a ﬁsh market in Jeddah, Saudi Arabia

populations along the Saudi Arabian Red Sea coast (Clarke et al. 2013; Spaet et al. 2016). Furthermore, an interview-based analysis of the highest CPUE ﬁshers recalled for sharks in Eritrea, where a directed ﬁshery for sharks was ﬁrst reported in the 1950s (Marshall 1996), revealed an average decline in CPUE of around 10% per year for the period of 1960–2007 (Tesfamichael et al. 2014). A very similar CPUE decline rate (11% per year) was obtained through a time-series catch data reconstruction based on catch and effort data for the same period (Tesfamichael 2012). Most sharks are taken as bycatch in reef and bottom-trawl ﬁsheries (Tesfamichael and Pitcher 2006; Spaet and Berumen 2015) and landed at various sites along the Red Sea coastline. Catches are rarely managed and are often misidentiﬁed or unrecorded, resulting in a lack of species-speciﬁc data. Most shark catches are marketed fresh; however, poor infrastructure in many rural areas, especially Sudan and Yemen, often results in lower quality and reduced earning potential (Bonﬁl 2003; Bonﬁglioli and Hariri 2004;

Tesfamichael and Pitcher 2006; Alabsi and Komatsu 2014). Shark landings are currently reported to FAO from all Red Sea countries with the exception of Sudan (although ‘sharks, rays, skates etc.’ were reported from 1998 to 2002). The remaining countries started reporting shark landings between 1950 (Yemen) and 2010 (Djibouti). Yet, most records are inconsistent, preventing the comparison of species-speciﬁc landing information across years or among countries. In addition, FAO catch statistics are separated by country, not by regional catchment, making them difﬁcult to interpret as most Red Sea countries also have coastlines along the Mediterranean Sea, the Arabian Gulf or the Indian Ocean. National ﬁsheries statistical yearbooks and reports are available for several Red Sea countries (e.g., Saudi Arabia MoA 2007), but numbers within and across reports are often outdated and inconsistent. Eight species dominate Red Sea shark landings; in decreasing order, these are: Spot-tail, Grey reef, Blacktip, Silky, Milk, Blacktip reef, Sliteye, and Scalloped hammerhead sharks (Bonﬁl 2003; Spaet and Berumen 2015).

15

Red Sea Sharks—Biology, Fisheries and Conservation

275

Fig. 15.4 Carcasses of Silky sharks (Carcharhinus falciformis), which had their ﬁns removed after being landed at a ﬁsh market in Jeddah, Saudi Arabia

Together these species comprised over 90% of shark landings recorded over a 24-month ﬁsh market survey in Jeddah, Saudi Arabia from 2011 to 2013 (Spaet and Berumen 2015). One decade earlier they constituted over 66% of landings recorded during a short-term survey (8-weeks total) in Egypt, Sudan and Saudi Arabia (Bonﬁl 2003). Targeted shark ﬁsheries usually employ longlines, handlines and gill nets. Targeting sharks in critical habitats like pupping and nursery grounds is common in the Red Sea (PERSGA 2006) and is particularly prevalent and detrimental in a few species, including Blacktip and Spot-tail sharks (Bonﬁl 2003). This is further supported by single-day landings of up to 600 neonatal Spot-tail sharks reported from Saudi Arabian ﬁsh markets (Spaet and Berumen 2015) (Fig. 15.3). In the past, large sharks were highly sought after for their livers with liver oil being used as preservative for traditional wooden boats. Owing to an increasing availability of alternative preservatives, today liver oil is only being extracted by a negligible number of ﬁshermen for personal use (Marshall 1996; Hariri et al. 2002). While there is demand for fresh meat from most small-bodied sharks (mostly sold in small cubes), regional consumption of shark ﬁns seems to be very limited, occuring only at select Chinese restaurants

(Jabado and Spaet 2017). Generally, shark ﬁns are destined for export and most larger sharks are ﬁnned following ﬁsh market auctions upon sale for consumption at retail stores (Spaet and Berumen 2015) (Fig. 15.4). Remains of sharks after processing for meat and ﬁns are generally discarded (Jabado and Spaet 2017). Retail prices of sharks and their various products differ by species, size, availability and demand (Bonﬁl 2003). Shark meat is generally cheaper than that of most other marketed species. The meat of highly valued species such as the Roving coral grouper (Plectropomus pessuliferus) may be 10–20 times more expensive than shark meat (Spaet and Berumen 2015). Based on my observations at a ﬁsh market in Jeddah, Saudi Arabia, large Sphyrnids (which have disproportionately large ﬁns compared to their body size) appear to be the most expensive species and there is an obvious correlation between price and ﬁn size. Specimens measuring 2–3 m in length were sold for US$200, while other shark species (e.g., Bignose and Silky sharks) of the same size were auctioned for up to 50% less. Smaller sharks, regardless of developmental stage, are mostly sold in bundles of up to seven individuals for less than US$5 per bundle.

276

J. L. Y. Spaet

Interviews with Red Sea Fishermen

Sea coast, Thuwal (n = 9), Jeddah (n = 16) and Farasan Kebir (n = 25). Each interview lasted between 0.5 and 3 h. Except for three retired ﬁshermen, all interviewees were still active in the traditional ﬁsheries sector. All ﬁshermen interviewed were involved in multi-species ﬁsheries and in general did not target sharks during their ﬁshing operations. Yet, about 50% emphasized that they would target nursery areas for Blacktip, Blacktip reef, Spot-tail and Scalloped hammerhead sharks during certain times of the year. Most of these shark catches were routinely brought to the nearest ﬁsh market for onward sale and only a small number of neonates were kept for personal consumption. Most interviewees (98%) were unaware of a royal decree, issued in 2008 (Table 15.3), prohibiting shark ﬁshing in Saudi Arabian waters. However, in the light of an observed decline in shark abundance over the past 20 years (Table 15.4), the majority (80%) considered it important to implement management strategies for shark ﬁsheries in the region. The root of this decline was attributed to (1) an increase in multi-species ﬁsheries, resulting in less prey availability for shark species and (2) improved ﬁshing gear resulting in higher shark catches (Table 15.4). In addition, ﬁshermen from Thuwal pointed out that in 2008, longline ﬁshing fleets were instructed by the Saudi Ministry of Agriculture to target

To obtain further insights into Red Sea shark ﬁsheries, I conducted 50 interviews with local Saudi Arabian ﬁshermen between June 2011 and January 2013, based on the methods of Lam and Sadovy de Mitcheson (2011). Questions were asked in Arabic, with the help of local translators who had no background in ﬁsheries. Interviews were intended to provide information on the interviewee’s career history, details of past and current shark ﬁsheries, targeted species, seasonality, catch location, gear and vessel types used, utilization of caught specimens and the personal appraisal of each ﬁsherman regarding the current exploitation level of, and possible future management strategies for sharks. The majority of ﬁshermen employed in Saudi Arabian ﬁsheries are non-Saudi nationals who are hired temporarily and do not have any historical knowledge of elasmobranch ﬁsheries in the region. Hence, only traditional Saudi Arabian ﬁshermen who had worked in the ﬁshing sector for a minimum of 30 years were consulted. These individuals were identiﬁed by fellow ﬁshermen who were asked to name colleagues they considered to have good knowledge on sharks and shark ﬁsheries (Berg 2004). Interviews were conducted at three major ﬁshing locations along the Saudi Arabian Red Table 15.3 International instruments speciﬁc to shark protection in Red Sea countries, indicating the year of entry into force and existing national legislations (adapted from Jabado and Spaet 2017)

Country

International agreements CMS

CITES

Sharks MoU

National legislations

Djibouti

2004

1982

–

No speciﬁc regulations pertaining to sharks

Egypt

1983

1978

2014

Decree 79 of 2004 prohibits displaying, ﬁshing, moving or trading in sharks Decree 448 of 2005 prohibits the ﬁshing and sale of sharks in the Red Sea Decree 119 of 2009 prohibits selling, ﬁshing or trading in live or dead whole sharks or parts of them in all Egyptian waters

Eritrea

2005

1995

–

No speciﬁc regulations pertaining to sharks.

Israel

1983

1980

–

Since 1980 all sharks are protected in Israeli waters (all shark ﬁshing and ﬁnning is illegal)

Jordan

2001

1979

2014

No speciﬁc regulations pertaining to sharks

Saudi Arabia

1991

1996

2017

Decree 57543 of 23/08/1439 (year 2008) prohibits the ﬁshing of all shark species with any gear. Any sharks captured alive must be released back into the wild

Sudan

–

1983

2014

Since 2008, any form of shark product or shark ﬁshing is banned and gear restrictions are in place Since February 15, 2015, ﬁshing and any form of trade (including transport, sale and possession) in sharks are prohibited

Yemen

2006

1997

2014

Decree 42 of 1991 prohibits the dumping of damaged and undesirable ﬁsh back at sea after their catch. This decree serves as a ban on ﬁnning

Acronyms: CMS = Convention on Migratory Species; CITES = Convention on the International Trade in Endangered Species of Wild Flora and Fauna; Sharks MoU = Convention on Migratory Species Sharks Memorandum of Understanding

15

Red Sea Sharks—Biology, Fisheries and Conservation

Table 15.4 Percentage of Saudi Arabian interview respondents (n = 50) to selected questions pertaining to Red Sea shark ﬁsheries

277

Question related to

Answers (in %)

(A) Awareness of royal decree prohibiting sharks as by-catch

Aware (2)

Unaware (98)

(B) Sharks targeted

All sizes (10)

Neonates only (25)

By-catch only (65)

(C) Perceived abundance of sharks compared to 20 years ago

Declined (72)

Same (8)

Increased (20)

(D) Probable reason for shark decline

Less prey availability (68)

Finning (1)

(E) Perceived importance of management strategies for sharks

High (80)

Medium (5)

sharks in the northern and central Saudi Arabian provinces between Yanbu and Rabigh. One particular dhow operated longlines over the period of one year targeting large semi-pelagic and reef sharks. This dhow was consistently blamed for the drastic decline of shark populations in the area (Table 15.4). Sharks caught during this operation were either sold in Jeddah or transported to the Dubai ﬁsh market, which serves as major hub in the shark ﬁn trade (Rose 1996; Jabado et al. 2015).

Management and Conservation of Red Sea Sharks Over the past decades, there has been a signiﬁcant increase in both a general awareness of global overﬁshing and a recognition of the importance of sharks to the marine environment in particular (Stevens et al. 2000; Dulvy et al. 2008; Ferretti et al. 2010; Heithaus et al. 2012). This change in public and political perception has triggered management actions, such as listing certain shark species on the Convention on Migratory Species (CMS) and/or the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). While all Red Sea countries are signatories to one or both of these conventions (Table 15.3), the associated ﬁsheries management requirements have rarely been implemented (Jabado and Spaet 2017). Egypt, Jordan, Saudi Arabia, Sudan and Yemen have adopted a Sharks Memorandum of Understanding (Sharks MoU) under the auspices of CMS (Table 15.3). Yet, not a single Red Sea country participates in the International Plan of Action for Conservation and Management of Sharks (IPOA-Sharks), as suggested for all countries involved in targeted or incidental shark ﬁsheries by the United Nations Food and Agriculture Organization (FAO 1999). National legislations to manage the catch and trade of sharks have been developed by a number of Red Sea countries, ranging from bans on ﬁnning (Yemen) to complete bans on all shark ﬁshing activities (Egypt, Israel, Saudi Arabia, Sudan) (Table 15.3). Most of

More ﬁshermen (19)

Longlining fleet of 2008 (12) Low (15)

these policies, however, remain unenforced (Table 15.1) (Jabado and Spaet 2017). Several attempts have been made to overhaul regional management systems since the 1970s. Efforts included training of local ﬁsheries observers (Bonﬁl 2003; Gladstone 2008), the identiﬁcation of high priority conservation areas (PERSGA 2006; Gladstone 2008) and the development of management plans to promote sustainable shark ﬁshing in the Red Sea (Bonﬁl 2003). These efforts have largely failed due to the lack of political commitment to implement existing protection legislation. The limited attention directed toward the management and conservation of shark resources is most likely attributed to the political and institutional instability that prevails throughout the Red Sea region. In combination with the paucity of available information on most aspects of Red Sea shark biology (Spaet et al. 2012), this results in heavy, unmanaged ﬁshing pressure on existing shark populations, which is reflected in a dearth of sharks observed by ﬁsheries-independent survey methods in both coastal and oceanic Red Sea ecosystems [e.g., in Saudi Arabia (Bruckner et al. 2011; Spaet et al. 2016)]. Altogether, the synthesized data and scientiﬁc evidence presented here call for immediate conservation measures with a strong focus on upgrading management and enforcement capacities of the Red Sea ﬁsheries sector. Moreover, there is a general need to increase public awareness in the region about environmental issues related to overﬁshing. Overall, we need to overcome the status quo to ensure the long-term sustainability of shark ﬁsheries in the Red Sea (Hariri et al. 2002; Bonﬁl 2003; Gladstone 2008; Spaet and Berumen 2015; Spaet et al. 2016).

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J. L. Y. Spaet Tesfamichael D, Pitcher TJ (2006) Multidisciplinary evaluation of the sustainability of Red Sea ﬁsheries using Rapﬁsh. Fish Res 78:227– 235 Vignaud TM, Maynard JA, Leblois R, Meekan MG, Vázquez-Juárez R, Ramírez-Macías D, Pierce SJ, Rowat D, Berumen ML, Beeravolu C, Baksay S, Planes S (2014a) Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Mol Ecol 23:2590–2601 Vignaud TM, Mourier J, Maynard JA, Leblois R, Spaet J, Clua E, Neglia V, Planes S (2014b) Blacktip reef sharks, Carcharhinus melanopterus, have high genetic structure and varying demographic histories in their Indo-Paciﬁc range. Mol Ecol 23:5193–5207 Weigmann S (2016) Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. J Fish Biol 88:837–1037 White WT (2007) Catch composition and reproductive biology of whaler sharks (Carcharhiniformes: Carcharhinidae) caught by ﬁsheries in Indonesia. J Fish Biol 71:1512–1540

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Marina Costa, Maddalena Fumagalli and Amina Cesario

Abstract

The number of cetacean species present in the Red Sea is unknown. Navigation and associated exploration of Red Sea waters dates back thousands of years, but despite relatively high levels of human activity in the basin, observations of cetaceans in the Red Sea remain sparse. However, the absence of a comprehensive record of these marine mammals in the Red Sea is not due to the absence of cetaceans. The ﬁrst published report of cetaceans in the Red Sea was made by Forskål at the end of the 18th century and information about encounters with both live and stranded dolphins and whales continued throughout the 19th century. During the ﬁrst 80 years of the 20th century a number of new sightings conﬁrmed previous observations, suggesting some additions to the list. Following establishment of the Indian Ocean Whale Sanctuary in 1979, a renewed interest arose about cetacean conservation and dedicated surveys ﬁnally commenced. Information from smaller-scale projects was then collected in the waters off Egypt, Saudi Arabia, Sudan, Eritrea, Yemen and Israel, further raising the tally of cetacean species recorded in the Red Sea. The timely review presented in this chapter notes that at least 17 species of cetaceans have been observed in the Red Sea, including: Balaenoptera edeni, B. musculus, B. omurai, Megaptera novaeangliae, Delphinus delphis cfr. tropicalis, Grampus griseus, Globicephala macrorhynchus, M. Costa (&) South Atlantic Environmental Research Institute (SAERI), Stanley Cottage, Stanley, Falkland Islands e-mail: [email protected] M. Costa M. Fumagalli A. Cesario Tethys Research Institute, Viale G.B. Gadio 2, 20121 Milan, Italy M. Fumagalli Department of Zoology, University of Otago, 340 Great King Street, 9054 Dunedin, New Zealand A. Cesario School of Biological Sciences, Swire Institute of Marine Science, University of Hong Kong, Pokfulam Road, Hong Kong Sar, China

Kogia sima, Orcinus orca, Pseudorca crassidens, Steno bredanensis, Stenella attenuata, S. coeruleoalba, S. longirostris, Sousa plumbea, Tursiops aduncus, and T. truncatus. Whilst the cetacean populations of the northern Red Sea have been recently assessed, it is a matter of concern that much less is known about the presence of cetaceans in the central and southern parts of the basin. Given the accelerating growth of human populations, together with the associated degradation of the marine environment, there is an urgent need for a more up-to-date appraisal of cetaceans, including the presence, abundance, distribution and behaviour of represented species throughout the Red Sea. The effectiveness of cetacean stock management and conservation depends on such information and there is a duty of care for governments, NGOs and academic institutions within the region to support and facilitate the research required to acquire a better understanding of the Red Sea’s whales and dolphins.

Introduction The word ‘cetacean’ derives from the Ancient Greek jῆso1 later Latinized as cetus and denotes a large ﬁsh, a whale, a shark, or a sea monster (Rice 1998). Today, it identiﬁes a group of aquatic mammals including whales, dolphins and porpoises (Cetacea). Cetaceans are currently considered an Infraorder of the Order Cetartiodactyla, which includes the even-toed ungulates such as cattle, sheep, goats, giraffes, hippos, antelopes, camels and pigs (Infraorder Artiodactyla) (Perrin 2017). Cetaceans are divided into two Superfamilies, Mysticeti or baleen whales, and Odontoceti or toothed whales. The anatomical dissimilarities between baleen and toothed whales are marked, but morphological and molecular studies have clearly conﬁrmed the monophyletic origin of cetaceans (Rice 1998). Most recent literature cites 92 living species, of

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_16

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which 15 are Mysticeti and 77 Odontoceti (Perrin 2017). One species, the baiji or Yangtze river dolphin (Lipotes vexillifer), is considered functionally extinct. Among the marine mammals (i.e., cetaceans, pinnipeds, sirenians, marine and sea otters and the polar bear), cetaceans possess the most specialized adaptations to the aquatic environment, living in the water for their entire life and surfacing only to breathe, rest and/or during aerial displays. Adaptations include body modiﬁcation for swimming, such as the loss of hair and hindlimbs, the development of large and muscular tails and modiﬁcations to sensory organs. Most notable of these is the hearing system, which has evolved to facilitate communication, the detection and localization of prey and predators, and navigation in the aquatic environment (Nummela 2009). Odontocetes are also capable of echolocation, a process that enables animals to use reflected sounds to map the environment, including the detection of prey (Au 2009). Echolocation is poorly understood in Mysticeti (Au 2009). Cetaceans are mainly marine with some species having secondarily invaded freshwater habitats such as Sotalia fluviatilis (tucuxi), Platanista gangetica (South Asian river dolphin), Lipotes vexillifer (Baiji) and Inia geoffrensis spp. (Amazon river dolphin subspecies) (Perrin et al. 2009). To date, a certain degree of uncertainty persists about cetacean phylogeny and the number of extant cetacean species (Perrin 2017). In the last decades, rapid advancements in the ﬁeld of marine mammal research, and in particular the introduction of molecular methods, have resulted in changes of cetacean taxonomy (Moura et al. 2013). Few new species and subspecies have been identiﬁed, such as the species Sousa sahulensis (Jefferson and Rosenbaum 2014), and the subspecies Cephalorhynchus commersonii kerguelensis (Robineau et al. 2007). Other accepted species have been invalidated such as the Delphinus capensis (Cunha et al. 2015; Gatesy et al. 2013). On the other hand, several paraphyletic groupings are still awaiting full resolution (Berta et al. 2005; Perrin et al. 2009). Cetacean diversity in the Red Sea is poorly known. This lack of knowledge is not due to the absence of cetaceans, as recent studies have shown (Smeenk et al. 1996; Gladstone and Fisher 2000; Feingold 2007; Shawky and Aﬁﬁ 2008; Notarbartolo di Sciara et al. 2009; Ziltener and Kreicker 2013; Costa 2015; Shawky et al. 2015; Cesario 2017; Fumagalli 2016); neither is it due to limited opportunities for observations, since navigation of the Red Sea waters began thousands of years ago (2500 BC) (Bradbury 1988; Sherratt and Sherratt 1993; Searight 2003), with scientiﬁc expeditions in the second half of the 18th century (Hansen 1962). Although the reasons for the lack of information on the cetacean community of the Red Sea basin are unclear, it is possible to speculate why. The rich biodiversity of coastal tropical species (such as ﬁsh and corals) most likely ﬁrst

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attracted researchers’ attentions, especially as small specimens were easier to access and preserve. The strong winds that characterize the basin, and a general inaccessibility to large areas of the coast due to the lack of infrastructure might have hampered attempts to encounter and observe cetaceans, which typically are further offshore, spread over vast areas and at a low densities (Hammond 2010). The Red Sea accounts for about 0.13% of the world’s ocean area (Sea Around Us Project, 2014) and extends over a distance of approximately 1,930 km from north (*30°N) to south (*12°30’N). The basin separates northeast Africa from the Arabian Peninsula, and has an average width of 280 km (Edwards and Head 1987; Rasul and Stewart 2015). The maximum depth is about 2,850 m, recorded in the central part of the basin, but the average depth is only 490 m, mainly due to a large continental platform in its southern part (Morcos 1970). The Strait of Bab al Mandab in the south connects the Red Sea to the Gulf of Aden and then the Arabian Sea. The northern end extends into the Gulf of Aqaba and the Gulf of Suez, the latter reaching the Mediterranean Sea via the artiﬁcial Suez Canal since 1869 (Fig. 16.1). The countries bordering the Red Sea are Egypt, Sudan, Eritrea, Djibouti, Yemen, Saudi Arabia, Jordan and Israel. The presence of vast deserts and the lack of permanent rivers make the Red Sea one of the hottest and saltiest water-bodies on Earth, with a net annual evaporation of 1– 2 m (Edwards and Head 1987). Only two seasons (winter and summer) are present and influenced by the Indian monsoon regime. During winter (from October to April) the humid monsoon winds generate a net northward drift of surface waters that forces Indian Ocean waters, rich in nutrients, into the southern Red Sea. During summer (May to September) winds flow from north to south and the net drift continues moving north under a superﬁcial drift moving south (Raitsos et al. 2013). The effect of the seasonal regime and the presence of a large continental shelf in the southern part divide the Red Sea into two sub-basins at approximately 18°–20°N latitude. The central/south is less oligotrophic than the north and is characterized by sandy shores, thick stands of mangroves, and coral formations found mainly offshore (around the Dahlak and Farasan Islands). The north, on the contrary, is characterized by an extraordinary network of coral reefs, both in the form of fringing reefs (growing along the coast) and barrier reefs (separated from the coast by a channel of deep water). This extremely diverse coral community supports a diverse assemblage of benthic invertebrates and coral ﬁsh; the latter is thought to be the richest ﬁsh assemblage west of Indonesia and the Philippines, which are acknowledged as the global centres of diversity for ﬁshes (Edwards and Head 1987). Despite the limited geological time that has passed since re-colonisation of the Red Sea with the waters

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Fig. 16.1 Map of the Red Sea. The black dashed line indicates the division used in the text between the northern and central/southern parts of the Red Sea

of the Indian Ocean, the level of endemism in the Red Sea appears to be high and is favoured by the semi-isolation of the basin (Edwards and Head 1987; Di Battista et al. 2013, 2016a, b). Geologically, the Red Sea is a young ocean and is part of the Red Sea–Gulf of Aden rift system. The rift has been separating the African continental plate and the Arabian plate since about 30 Ma (Bosworth et al. 2005). The connections of the Red Sea with the Mediterranean Sea and the Indian Ocean were discontinuous, opening and closing during time. The passage with the Mediterranean Sea was deﬁnitely interrupted following the Messinian Event about 6 Ma, to be artiﬁcially reopened in 1869 through the Suez Canal. The connection of the Red Sea with Indian Ocean

opened for the ﬁrst time around 5 Ma ago and almost closed during the glacial periods. During periods of isolation from the Indian Ocean, the Red Sea experienced hypersaline conditions similar to those that now occur in the Dead Sea, and was unlikely to have supported many forms of life, cetaceans included (Fenton et al. 2000). As a consequence, cetaceans may have re-populated the Red Sea from the Indian Ocean around 10,000 years ago, well after the end of the last glacial maximum when sea level rise re-established the connection with the Indian Ocean (Almogi-Labin et al. 2008). Cetaceans of the Red Sea and the Indian Ocean are in fact considered to be part of the same assemblage (Ballance and Pitman 1998). However, the high biodiversity of the latter (Keller et al. 1982; Small and Small 1991; Ballance

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and Pitman 1998; Anderson 2005; Kiszka et al. 2007, 2010) is presumably unrepresentative of the Red Sea (Notarbartolo di Sciara et al. 2017). A phenomenon called Lessepsian migration (from the French engineer Ferdinand Marie de Lesseps who planned and supervised the construction of the Suez Canal), whereby animals are exchanged between the Red Sea and the Mediterranean Sea through the Suez Canal has occurred many times since the opening of the Suez Canal in 1869. More than 300 marine species have been recorded migrating into the Mediterranean Sea (Bentur et al. 2008) while very few organisms seem to have accomplished the opposite migration even though current flow alternates in direction (Morcos 1970; Bentur et al. 2008). The migration of animals from the warm waters of the Red Sea to the relatively cold waters of the Mediterranean Sea might be due to the warming of the latter as a result of climate change (Lejeusne et al. 2010). Cetacean migrations through the Suez Canal appear to be rare; the only certain record relates to the northbound movement of Indo-Paciﬁc humpback dolphins, subsequently sighted in the eastern part of the Mediterranean Sea (Kerem et al. 2001; Notarbartolo di Sciara 2016). Although human activities in the region have been recorded for centuries, pressures upon the Red Sea shores have dramatically increased in the last 40–45 years due to extensive development of urban areas, resulting in the population of the countries along the basin growing from about 5 to 9 million (Edwards and Head 1987; Sheppard et al. 1992; CIA 2017). The major threats identiﬁed in the Strategic Action Plan developed by the “Regional Organization for the Conservation of the Red Sea and Gulf of Aden” (PERSGA) include: extensive habitat destruction; unsustainable use of living marine resources; navigation risks, oil production and transport; impacts of urban and industrial development; expansion of coastal tourism; and the curio trade (PERSGA 1998). PERSGA was established to implement the Jeddah Convention (formally the “Convention for the Conservation of the Red Sea and Gulf of Aden Environment”), the most important regional agreement for the protection and conservation of the Red Sea, signed in 1982 by Djibouti, Egypt, Jordan, Palestine, Saudi Arabia, Somalia, Sudan, and Yemen. The pressures identiﬁed for the region are likely to have important consequences for the Red Sea ecosystem due to its innate vulnerabilities. The Red Sea is a semi-enclosed basin, has a strong reliance on the oil industry, high navigation risks, a lack of marine resource information, poor coastal zone planning, and social and political instability (Edwards and Head 1987; Gladstone et al. 1999). Cetaceans are charismatic animals whose role is important for both conservation (as umbrella and flagship species) and in the structuring of the marine ecosystems (Katona and Whitehead 1988; Kontoleon and Swanson 2003; Ainley

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et al. 2010; Roman and McCarty 2010; Estes et al. 2011). Due to their long life span and low reproductive rate, cetaceans are also very vulnerable to human activities and scientiﬁc knowledge is essential to allow appropriate management actions to be taken. Information about cetacean presence, abundance and distribution is still scattered for many marine regions around the world. In areas where human population growth is rapid and where human nearshore activities have resulted in the overexploitation of marine resources, including cetacean populations, this lack of information is particular alarming (Leatherwood and Donovan 1991; Dolar et al. 1994; Dolar 1994; Aragones et al. 1997; Anderson 2013). Following the recommendations issued by PERSGA (1998, 2002, 2004), and due to an increased interest in Red Sea cetaceans, there has been a recent surge to ﬁll the gaps in our current understanding of cetacean species in the basin (Gladstone and Fisher 2000; Al-Mansi and Sambas 2006; Hagan 2006; Salam 2006; Feingold 2007; Abraha et al. 2008; Cesario 2008, 2017; Fumagalli 2008, 2016; Shawky and Aﬁﬁ 2008; Al-Mansi 2009; Notarbartolo di Sciara et al. 2009, 2017; Ziltener and Kreicker 2013; Costa 2015; Shawky et al. 2015; Röthig et al. 2016). This chapter collates present and historical information on cetacean species presence and distribution in the Red Sea including published and grey (unpublished) literature. This is an endeavour needed not only to advance our knowledge on the Red Sea species, but also to enable the formulation of science-based marine conservation initiatives at both national and regional levels. This chapter summarises and revisits information that the authors, in collaboration with a large team of experts, have presented in a recent review (Notarbartolo di Sciara et al. 2017). The information contained in this chapter nonetheless is essential to complete the comprehensive approach this book provides.

Cetacean Species in the Red Sea Seventeen species of cetacean have been reliably recorded in the Red Sea to date, including four species of rorqual whales (family: Balaenopteridae), the dwarf sperm whale (family: Kogiidae), and twelve species of delphinids (family: Delphinidae). The list of conﬁrmed species, reporting the scientiﬁc name in Latin, and the common name in English (Committee on Taxonomy 2017) and Arabic (when available, translation by Encyclopaedia of Life 2017), is as follows: • Balaenoptera edeni Anderson, 1879—Bryde’s whale — • Balaenoptera musculus (Linnaeus, 1758)—Blue whale

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• Balaenoptera omurai Wada, Oishi and Yamada, 2003— Omura’s whale • Megaptera novaeangliae (Borowski 1781)—Humpback whale— • Kogia sima (Owen 1866)—Dwarf sperm whale • Delphinus delphis tropicalis Van Bree, 1971— Indo-Paciﬁc common dolphin • Globicephala macrorhynchus (Gray 1846)—Short ﬁnned pilot whale • Grampus griseus (G. Cuvier 1812)—Risso’s dolphin — • Orcinus orca (L. 1758)—Killer whale— • Pseudorca crassidens (Owen 1866)—False killer whale — • Sousa plumbea (G. Cuvier 1829)—Indian Ocean humpback dolphin— • Stenella attenuata Gray, 1846—Pantropical spotted dolphin— • Stenella coeruleoalba (Meyen 1833)—Striped dolphin — • Stenella longirostris (Gray 1828)—Spinner dolphin — • Steno bredanensis (Lesson 1828)—Rough-toothed dolphin— • Tursiops aduncus (Ehrenberg 1833)—Indo-Paciﬁc bottlenose dolphin— • Tursiops truncatus (Montagu 1821)—Common bottlenose dolphin— The ﬁrst cetacean observations in the Red Sea were made in the second half of the 18th century by Forskål (1775) during the Danish Arabian Expedition (1761–1767) that aimed to explore the southern part of the western Arabian Peninsula (at that time referred to as Arabia Felix) (Hansen 1962). Forskål reported the presence of two cetacean taxa (Fig. 16.2; Table 16.2); a baleen whale (of about 18 m) observed in the northern part of the Red Sea, and several dolphins observed in the area of Jeddah. Forskål referred to these dolphins as ‘Abu salâme’ (‘Father of Peace’), the Arabic name used locally for the species T. aduncus (Rüppell 1842; Beadon 1991). Following the flowering of geographical societies in Europe in the 19th Century, there was an increase in the number of expeditions to the Arabian region (The Qatar Digital Library, 2nd October 2017). The ﬁrst records of several cetaceans were described during this period (Fig. 16.2; Table 16.2), including three ‘new’ dolphin species; a large rounded-nose dolphin ﬁtting the description of G. griseus, described by Rüppell 1842 [1845] and later conﬁrmed by Klunzinger (1878); a long, narrowed-nose dolphin reported by Rüppell as “Delphinus longirostris Dussimier” ﬁtting the description of S. longirostris; and a

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Fig. 16.2 Number and species of cetaceans described in the Red Sea from 1750 to 2017 in 50-year periods bins. Bsp: Balaenoptera sp.; Ta: Tursiops aduncus; Gg: Grampus griseus; Sl: Stenella longirostris; Sb: Steno bredanensis; Ssp: Sousa sp.; Sp: Sousa plumbea; Be: Balaenoptera edeni; Sa: Stenella attenuata; Mn: Megaptera novaeangliae; Oo: Orcinus orca; Pc: Pseudorca crassidens; Gm: Globicephala melas; Tt: Tursiops truncatus; Sc: Stenella coeruleoalba; Dsp: Delphinus sp.; Ks: Kogia sima; Bo: Balaenoptera omurai

specimen reported by Blyth (1846, 1863) as “Delphinorhynchus rostratus”, ﬁtting the description of Steno bredanensis. Although identiﬁcation is uncertain because specimens were not collected or are untraceable (Notarbartolo di Sciara et al. 2017), the occurrence in the Red Sea of these three species was later conﬁrmed by Beadon (1991), Robineau and Rose (1983), and Frazier et al. (1987), respectively. In the 19th century several authors have reported the presence of baleen whales in the Red Sea, suggesting different names for the species (Ehrenberg 1833; Heuglin 1851, 1877; Heuglin and Fitzinger 1866; Klunzinger 1871; Anderson 1902). De Winton (in Anderson 1902) was the ﬁrst to correctly describe a specimen as “Balaenoptera edeni” and when the specimen was donated to the British Museum (Natural History) it became the ﬁrst evidence that the Bryde’s whale occurs in the Red Sea. The proof of the

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presence of Tursiops aduncus was provided by Hemprich and Ehrenberg (Ehrenberg 1833). They collected a dolphin skull in 1825 on Belhosse Island (Dahlak Archipelago, Eritrea), and named the species “Delphinus aduncus”. Years later genetic analyses proved that the skull effectively belonged to a Tursiops aduncus and the specimen became the holotype of the species (Perrin et al. 2007). Notarbartolo di Sciara et al. (2017) identiﬁed a further two taxa that were described in the 19th century. Observations of dolphins reported as T. aduncus by Klunzinger (1878) and Burton (1823, in Flower 1932) were reassessed as specimens of S. attenuata and Sousa sp., respectively (Fig. 16.2; Table 16.2). No additional cetaceans were reported in the Red Sea during the ﬁrst half of the 20th century. Two observations of T. aduncus were reported in the northern part of the basin by Flower (1932) and B. edeni by Anonymous (1950) (Fig. 16.2; Table 16.2). At the end of the Second World War, human attitudes toward nature and cetaceans in particular began ﬁnally to change from exploitation to conservation (Reeves 2009) resulting in the creation of several international Conventions and their associated Institutions. These included the International Union for the Conservation of Nature—IUCN, in 1948; the International Whaling Commission—IWC, in 1951; the Convention on International Trade in Endangered Species of Wild Fauna and Flora—CITES, in 1973; the Convention on the Conservation of Migratory Species of Wild Animals—CMS, in 1979; and the establishment of a global moratorium on commercial whaling in 1986. The creation of the ﬁrst IWC Whale Sanctuary in the Indian Ocean in 1979 (Perrin et al. 2009) stimulated new exploration of the Red Sea, and seven ‘new’ species (Fig. 16.2; Table 16.2) were added to the seven previously described for the area. These included Megaptera novaeangliae (P. Vine, pers. comm. in Baldwin et al. 1999; Debelius 1998), Orcinus orca (Frazier et al. 1987), Pseudorca crassidens (Alling et al. 1982; Alling 1986; Beadon 1991; Frazier et al. 1987; Robineau and Rose 1984; Weitkowitz 1992), Globicephala sp. (see comment below) (Leatherwood et al. 1991), Tursiops truncatus (Alling et al. 1982; Alling 1986; Beadon 1991; Frazier et al. 1987; Marchessaux 1980; Miyazaki and Amano 1991; Robineau and Rose 1984; Weitkowitz 1992), Stenella coeruleoalba (Frazier et al. 1987; Wilson et al. 1987), and Delphinus sp. (see comment below) (Leatherwood 1986; Roghi and Baschieri 1956; Smeenk et al. 1996). Two species of pilot whale are currently recognised: Globicephala melas (Traill 1809) distributed with two subspecies in the North Atlantic (G. m. melas) and in the Southern Hemisphere from Antarctica to subtropical waters (G. m. edwardii); and G. macrorhynchus (Gray 1846), with

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a circumpolar distribution in tropical and warm-temperate waters. G. macrorhynchus is the species considered to be present in the Red Sea (Rice 1998; Wang et al. 2014; Jefferson et al. 2015). The taxonomy of the genus Delphinus is unresolved. In the Red Sea, Smeenk et al. (1996) described a form with a very long beak which they called Delphinus cf. tropicalis. The same form was observed off Oman by Ballance and Pitman (1998) and Jefferson and Van Waerebeek (2004). Finally, in recent years three species previously undescribed for the Red Sea were added to the list of the Red Sea cetaceans observed in the Red Sea. Notarbartolo di Sciara et al. (2017) report evidence of the presence of Kogia sima and Balaenoptera omurai. One individual of blue whale was ﬁlmed in May 2018 in the Gulf of Aqaba (Letzter 2018). Considering these species the total number of species occurred at least once in the Red Sea is 17 (Fig. 16.2; Table 16.2). In the literature, seven other species have been suggested as possibly present in the basin, including: • • • • • • •

Balaenoptera physalus—Fin whale— B. borealis—Sei whale— B. acutorostrata—Common Minke whale Peponocephala electra—Melon-headed whale Feresa attenuata—Pygmy killer whale Physeter macrocephalus—Sperm whale Neophocaena phocaenoides—Indo-Paciﬁc porpoise

ﬁnless

Although these species have been recorded in the waters of the Indian Ocean, Arabian (Persian) Gulf and Gulf of Aden (Pilleri and Ghir 1972, 1973–1974; Al-Robaae 1975; Alling et al. 1982; Robineau and Rose 1984; Alling 1986; Leatherwood 1986; Preen 1989; Gallagher 1991; Small and Small 1991; Sheppard et al. 1992; Weitkowitz 1992; Eyre 1995; Robineau and Fiquet 1994a, b, 1996; Smeenk et al. 1996; Baldwin et al. 1998, 1999; Ballance and Pitman 1998; Baldwin 2003; Braulik et al. 2010; Eyre and Frizell 2012), there is currently no evidence that they occur or ever occurred in the Red Sea. The only mention of B. physalus in the Red Sea is from Flower (1932) who refers to a specimen recovered along the coast of the Gulf of Suez in 1893 reported by Anderson (1902). However, in Anderson (1902) the stranded whale was named as B. edeni without mentioning the presence of a ﬁn whale. The presence of B. borealis was mentioned in connection to a stranding that occurred in 1950 near Suez with the animal reported as ‘probably a Sei whale’ (Anonymous 1950). However, pictures taken in situ clearly show that the specimen to be B. edeni.

16

Review of Cetaceans in the Red Sea

In 1969 a specimen of B. acutorostrata was reported stranded south of Jizan (Saudi Arabia) by Leatherwood (1986), later repeated by Frazier et al. (1987) and Baldwin et al. (1999). However, the record lacks conﬁrmatory evidence and the presence of the species in the Red Sea remains unconﬁrmed (Table 16.2). A black dolphin identiﬁed as either P. electra or F. attenuata was mentioned by Notarbartolo di Sciara et al. (2007), but also in this case there is no evidence that either species is present in the Red Sea (Table 16.2). P. macrocephalus was reported by Roghi and Baschieri (1956) in Eritrean waters; however, the description of the feeding activity observed is typical of baleen whales, suggesting that the observed species was misidentiﬁed (Table 16.2). Neophocaena phocaenoides, commonly present in the Arabian Gulf, is reported as present in the Red Sea in the map on page 165 of Baldwin et al. (1999); however, there is no further mention in the text or elsewhere and its occurrence in the Red Sea remains unconﬁrmed.

Cetacean Distribution in the Red Sea Cetacean distribution within the Red Sea is unclear. The majority of observational effort in the last 40 years has mainly concentrated on the northern part of the basin (Table 16.1). Four species (S. attenuata Figs. 16.3 and 16.5, S. longirostris Figs. 16.4 and 16.5, T. aduncus in Fig. 16.6 and T. truncatus in Fig. 16.7) appear to be regularly observed and widely distributed across the entire basin, with T. aduncus associated with coastal waters and offshore coral reefs but not too distant from the coast such as Daedalus reef and the Brothers Islands (Ziltener and Kreicker 2013; Costa 2015; Notarbartolo di Sciara et al. 2017) (Table 16.2). Three species (G. griseus in Fig. 16.8, P. crassidens in Fig. 16.9, and S. plumbea in Fig. 16.10) are known to be frequently present in some areas, but are not commonly found in the northern part of the Red Sea (Beadon 1991; Feingold 2007; Costa 2015; Notarbartolo di Sciara et al. 2017). In the south, the few recorded observations suggest that the distributions of G. griseus and P. crassidens are similar to those observed in the north (Weitkowitz 1992; Eyre 1995; Eyre and Frizell 2012; Notarbartolo di Sciara et al. 2017), while S. plumbea appears to be commonly found along coastal areas (Weitkowitz 1992; Robineau and Rose 1984; Al-Safadi et al. 1995; Newton 1995; Gladstone and Fisher 2000; Hagan 2006; Al-Mansi 2009; Notarbartolo di Sciara et al. 2017). B. edeni (Figs. 16.11 and 16.12) appears to be sighted regularly in the central and southern part of the Red Sea (Gladstone and Fisher 2000; Abraha et al. 2008; Notarbartolo di Sciara et al. 2017); in the northern part the species is

287

generally infrequent with few observations reported during summer, in particular off Shalatin (Egypt; Fig. 16.1). D. d. tropicalis does not occur in the northern and central parts of the Red Sea but seems to be commonly observed in the southern part (Roghi and Baschieri 1956; Smeenk et al. 1996; Al-Mansi and Sambas 2006; Hagan 2006; Salam 2006; Al-Mansi 2009; Notarbartolo di Sciara et al. 2017). Five species (G. macrorhynchus, K. sima, O. orca, S. coeruleoalba, and S. bredanensis) are reported only from the central/southern part of the Red Sea (Leatherwood 1986; Frazier et al. 1987; Gladstone and Fisher 2000; Johnson 2004a, b, c; Hagan 2006; Notarbartolo di Sciara et al. 2017). Information about the distribution of these species is lacking but it is likely they are rare in the Red Sea. Finally, three species (B. musculus, B. omurai, and M. novaeangliae, Figs. 16.13 and 16.14) are considered rare in the Red Sea. B. musculus was ﬁlmed for the ﬁrst time in the Gulf of Aquaba in May 2018. B. omurai was observed for the ﬁrst time very recently near Safaga (Egypt) (Notarbartolo di Sciara et al. 2017). The species was initially regarded as a pygmy form of Bryde’s whale but genetic analyses showed that it was not particularly closely related to it (Sasaki et al. 2006). B. omurai was only recently recognised, and a misidentiﬁcation with B. edeni might have occurred although B. edeni is ‘easily’ recognisable due to the three ridges on the head. Observations of M. novaeangliae have been reported since the late 1990s (Debelius 1998; Baldwin et al. 1999; Costa 2015; Notarbartolo di Sciara et al. 2017) but in very low numbers and often the sighting reported belonged to the same individual moving along the coast. With the exception of B. omurai, the same species observed in the northern part of the Red Sea are also reported for the Gulf of Aqaba (Robineau and Rose 1983, 1984; Beadon 1991; Goffman et al. 1996; Bantin 1998a, b; Goffman 1997, 2003, 2006a, b; Feingold 2007; Mizrahi et al. 2009; Notarbartolo di Sciara et al. 2017) (Table 16.1). In the Gulf of Suez and Suez Canal two species (T. aduncus and S. plumbea) are commonly sighted (Rüppell 1842; Flower 1932; Mörzer Bruyns 1960; Burton 1964; Robineau and Rose 1984; Beadon 1991; Baldwin et al. 2004; Notarbartolo di Sciara et al. 2017). Several historical strandings of B. edeni were also reported on the coasts of the Gulf of Suez (Forskål 1775; Heuglin and Fitzinger 1866; Anderson 1902; Anonymous 1950). No recent sightings have been reported and the species is considered rare in the Gulf. There are two records of P. crassidens in the Gulf of Suez (Beadon 1991; Weitkowitz 1992). However, the species is known to be regularly present in the waters off the Straits of Tiran and in the Gulf of Aqaba (Feingold 2007; Costa 2015; Notarbartolo di Sciara et al. 2017). The shallow waters of Gulf of Suez seem to represent a limit to the distribution of the species.

288 Table 16.1 Species occurrence in the Red Sea divided into northern and central/southern parts and Gulf of Suez, Suez Canal, and Gulf of Aqaba

M. Costa et al. Region

Species

Possible distribution

Suez Canal

S. plumbea

Unknown occurrence, likely regular

T. aduncus

Common

T. truncatus

Possible from Mediterranean Sea?

B. edeni

Rare

P. crassidens

Rare

S. plumbea

Unknown occurrence, likely regular

T. aduncus

Common, widespread

Gulf of Suez

Gulf of Aqaba

Northern part

Central and Southern part

T. truncatus

Unknown occurrence

B. edeni

Rare

B. musculus

Rare or vagrant

G. griseus

Common in some areas

M. novaeangliae

Rare or vagrant

P. crassidens

Common in some areas

S. attenuata

Common, widespread

S. longirostris

Common, widespread

S. plumbea

Rare

T. aduncus

Common in coastal areas, widespread

T. truncatus

Unknown occurrence, likely rare

B. edeni

Infrequent but regular (only in summer?)

B. omurai

Unknown occurrence, likely rare

G. griseus

Common in some areas

M. novaeangliae

Rare or vagrant

P. crassidens

Common in some areas

S. attenuata

Common, widespread

S. longirostris

Common, widespread

S. plumbea

Infrequent but regular in some coastal areas

T. aduncus

Common in coastal areas, widespread

T. truncatus

Common along the coast and offshore, widespread

B. edeni

Common

B. omurai

Unknown occurrence, likely rare

D. d. tropicalis

Unknown occurrence, likely common

G. griseus

Common in some areas

G. macrorhynchus

Unknown occurrence, likely rare

K. sima

Unknown occurrence, likely rare

M. novaeangliae

Rare or vagrant

O. orca

Unknown occurrence, likely rare

P. crassidens

Common in some areas

S. attenuata

Common, widespread

S. bredanensis

Unknown occurrence, likely rare

S. coeruleoalba

Unknown occurrence, likely rare

S. longirostris

Common, widespread

S. plumbea

Common in coastal areas

T. aduncus

Common in coastal areas, widespread

T. truncatus

Common along the coast and offshore, widespread

16

Review of Cetaceans in the Red Sea

289

Fig. 16.3 Three individuals of Stenella attenuata photographed off Marsa Alam (Egypt) in 2010. Credit to HEPCA/Marina Costa

Fig. 16.4 Individual of Stenella longirostris photographed near Ras Banas Peninsula (Egypt) in 2011. Credit to HEPCA/Zoe Sanchez

T. truncatus has been observed in the Gulf of Suez (A. Ziltener, pers. comm.) but its distribution is unknown. Tursiops spp. are regularly found in the Suez Canal in the proximity of Port Said, and often are observed in winter while hunting sardines (I. Mohammed, pers. comm.). Because of the spatial proximity to the Mediterranean, it is likely that these dolphins belong to a sub-population of T. truncatus inhabiting Mediterranean waters off Israel, a distinct and smaller form compared to the common bottlenose

dolphins found in the rest of the Mediterranean Sea (Sharir et al. 2011; Kerem et al. 2012). In the southern part of the Suez Canal from Suez to the Bitter Lakes, bottlenose dolphins have also been encountered but there is no clear indication if they belong to T. aduncus from the Red Sea or to the T. truncatus from the Mediterranean Sea. T. truncatus from the Red Sea (identiﬁable by its large size—4 m) has never been reported in the Suez Canal although misidentiﬁcation with the other Tursiops spp. is unlikely but possible.

290 Fig. 16.5 Individual of Stenella longirostris (above) and of Stenella attenuata (below) photographed off the southern Egyptian coast in 2011. Credit to HEPCA/Amina Cesario

Fig. 16.6 Individuals of Tursiops aduncus photographed underwater in Samadai reef lagoon (Egypt) in 2013. Credit to HEPCA/Amina Cesario

M. Costa et al.

16

Review of Cetaceans in the Red Sea

291

Fig. 16.7 Individual of Tursiops truncatus photographed south of Ras Banas Peninsula (Egypt) in 2010. Credit to HEPCA/Marina Costa

Table 16.2 List of published and unpublished sources (ordered by year of publication or observation) reporting the presence of cetacean species observed in the Red Sea. Code meaning: spp = undeﬁned species related to genus described in the previous row; Ba = Balaenoptera acutorostrata; Be = B. edeni; Bo = B. omurai; Mn = Megaptera novaeangliae; Dsp = Delphinus sp.; Gg = Grampus griseus; Gm = Globicephala macrorhynchus; Ks = Kogia sima.; Oo = Orcinus orca; Pc = Pseudorca crassidens; PF = Peponocephala electra and/or Feresa attenuata; Pm = Physeter macrocephalus; Sb = Steno bredanensis; Sa = Stenella attenuata; Sc = Stenella coeruleoalba; Sl = Stenella longirostris; Sp = Sousa plumbea; Ta = Tursiops aduncus; Tt = Tursiops truncatus. New observation reported by the author; Citation from other source;? Species identiﬁcation uncertain as suggested by the author or because species description does not match with the name of the species indicated; *reported only as genus Reference

spp

Ba

Balaenoptera Be Bm

Bo

Mn

Dsp

Ks

Gg

Gm

Oo

Pc

PF

Pm

Sb

ssp

Stenella Sa Sc

Sl

Sp

ssp

Tursiops Ta

Tt

Forskål (1775) 11

Burton 1823 (in Flower 1932) 1

Ehrenberg (1833)

10

Rüppel (1842) [1845]

? 12

Blyth (1846, 1863) 2

Heuglin (1851) Heuglin (1861) Heuglin and Fitzinger (1866)

3

Klunzinger (1871) Heuglin (1877)

4

Klunzinger (1878)

5

?

16

a

? *

Specimen MSNG 3781 (1882) True 1889) Sclater (1891) Anderson (1902) Klunzinger (1915) Mertens (1925) Flower (1932)

6

Anonymous (1950)

7

11

8

Roghi and Salvadori (1956)

?

18

*

Mörzer Bruyns (1960) Burton (1964) 9

Slijper et al. (1964) Specimen FM 105019

b

(1966)

19

(continued)

292

M. Costa et al.

Table 2.2 (continued) Reference

spp

Ba

Balaenoptera Be Bm

Bo

Mn

Dsp

Ks

Gg

Gm

Oo

Pc

PF

Pm

Sb

ssp

Stenella Sa Sc

Sl

Sp

ssp

Tursiops Ta

Tt

Mörzer Bruyns (1971)

*

Pilleri and Gihr (1972) Neve (1973) Ross (1977) Beadon 1991

c

sc

?

Marchessaux (1980) Robineau (1981)

*

Schröder and Schulze (1981) Alling et al. (1982) Robineau and Rose (1983)

* * *

Robineau and Rose (1984) Piller (1985) Alling (1986)

?

Leatherwood (1986)

?

17

?

sc

De Silva (1987)

?

Frazier et al.( 1987)

13

?

sc

?

14

17

Gilpatrick et al. (1987) Perrin et al. (1987)

?

Wilson et al.( 1987) Leatherwood et al. (1989) Kruse et al. (1991) Leatherwood and Donovan (1991) Leatherwood et al. (1991)

* *

Miyazaki and Amano (1991) Sheppard et al. (1992) Weitkowitz (1992) Perrin et al. (1994) Eyre (1995 )

*

Al-Safadi et al. (1995) Eyre and Frizell (2012) Newton (1995)

d

Ross et al. (1995)

Scott (1995)

Goffman et al. (1996)

?

Smeenk et al. (1996)

* * sc

Goffman (1997)

Baldwin et al. (1998)

sc

Bantin (1998a,b)

Rice (1998) Archer and Perrin (1999)

?

sc

sc

Goffman (1997) Gladstone (2000) Gladstone and Fisher (2000)

sc

Spanier et al. (2000)

*

Jefferson and Karczmarski (2001) Kerem et al. (2001) Jefferson and Van Waerebeek (2002) Baldwin (2003)

ca

sc

Maughan (2003)

*

Baldwin et al. (2004)

Johnson (2004a,b,c) Perrin et al. (2004) PERSGA (2004) Al-Mansi and Sambas (2006)

?

Goffman (2003) Hoath (2003)

Debelius (1998)

Baldwin et al. (1999)

de de

sc

(continued)

16

Review of Cetaceans in the Red Sea

293

Table 2.2 (continued) Reference

spp

Ba

Balaenoptera Be Bm

Bo

Mn

Dsp

Ks

Gg

Gm

Oo

Pc

PF

Pm

Sb

ssp

Stenella Sa Sc

Sl

Sp

ssp

Tursiops Ta

Tt

Goffman (2006a,b) Hagan (2006)

de

Salam (2006)

de

15

?

sc

?

? ?

Feingold (2007)

?

Notarbartolo et al. (2007)

sc

Perrin et al. (2007) Goitom et al. (2007) Abraha et al. (2008) Cesario (2008) Fumagalli (2008) Hammond et al. (2008) Shawky and Afifi (2008) Al-Mansi (2009)

de

sc

?

Mizrahi et al. (2009) Notarbartolo et al. (2009) Culik (2010)

*

Bruckner (2011) Mendez et al. (2013) Ziltener and Kreicker (2013) Kleinertz et al. (2014) Wang et al. (2014) Costa (2015) Shawky et al. (2015) Röthig et al. (2016) Fumagalli (2016) Cesario (2017) Notarbartolo et al. (2017) Letzter (2018)

a

The specimen MSNG 3781, located in the Natural History Museum of Genoa, is a skull of Sousa sp. collected near Assab, Eritrea, in 1882 (Notarbartolo di Sciara et al. 2017); bThe specimen FM 105019, located in the Field Museum of Natural History in Chicago, is a skull of S. attenuata collected near Marsa Alam in 1966 (Notarbartolo di Sciara et al. 2017); cSurvey carried out in 1980–1981; dSurvey carried put in 1995; 1 Recorded as whale “Bitān”; 2Recorded as “Balaenoptera”; 3Recorded as “Balaenoptera Forskåli”; 4Recorded as “Balaenoptera Bitan”; 5 Recorded as a “giant whale”; 6Citation from Anderson (1902) but reported as ﬁn whale, “B. physalus”; 7Recorded as a “Sei whale B. borealis” but pictures revealed it was a B. edeni; 8Reported as “pilot whales” but from pictures they were likely Pseudorca crassidens;. 9Recorded as “little piked whales”; 10Recorded as “Phocoena”; 11Recorded as bottlenose dolphin but analyses of the drawings suggested it was a Sousa sp. (Notarbartolo di Sciara et al. 2017); 12Reported as “Delphinorhynchus rostratus F. Cuv.”; 13Reported as “Steno rostratus”; 14Reported as “Tursiops truncatus/gilli”; 15Reported as “Delphinus delphis” but clearly Stenella coeruleoalba in the picture; 16Recorded as “Tursiop aduncus” but the description suggest is Stenella attenuata (Notarbartolo di Sciara et al. 2017); 17S. attenuata erroneously listed as S. longirostris; 18The description of the foraging activities reminds of a baleen whale.; 19Reported as Delphinidae and later identiﬁed as S. attenuata (Notarbartolo di Sciara et al. 2017); scReported as Sousa chinensis; caReported as Delphinus capensis; deReported as Delphinus delphis

Fig. 16.8 Individual of Grampus griseus photographed near Abu Fandira reef (Egypt) in 2012. Credit to HEPCA/Gemma Veneruso

294 Fig. 16.9 Individuals of Pseudorca crassidens photographed offshore near St John’s reefs (Egypt) in 2012. Credit to HEPCA/Marina Costa

Fig. 16.10 Individual of Sousa plumbea photographed near Hamata (Egypt) in 2010. Credit to HEPCA/Amina Cesario

M. Costa et al.

16

Review of Cetaceans in the Red Sea

Fig. 16.11 Individual of Balaenoptera edeni photographed near Abu Fandira reef (Egypt) in 2012. Credit to HEPCA/Maddalena Fumagalli

Fig. 16.12 Individual of Balaenoptera edeni photographed off Jeddah (Saudi Arabia) while feeding. Credit to Tomas Zurita

295

296 Fig. 16.13 Individual of Megaptera novaeangliae photographed off Hurghada (Egypt) in 2011. Credit to Spiritual World Diving Federation SWDF/Sandra Caramelle

Fig. 16.14 Individual of Megaptera novaeangliae photographed off Hurghada (Egypt) in 2011. Credit to Spiritual World Diving Federation SWDF/Sandra Caramelle

M. Costa et al.

16

Review of Cetaceans in the Red Sea

Conclusions The seventeen species of cetaceans presented in this chapter account for 18% of the 92 cetacean species recognised world-wide (Perrin 2017). This represents a substantial level of biodiversity, if we consider the relatively small size of the basin (0.13% of the total world ocean surface; Sea Around Us Project 2017), Of these species, nine appear to be regular, two are rare or vagrant, and for six their occurrence is unclear mainly due to the lack of research effort in the central/southern region of the basin (Table 16.1). Despite meagre effort, the southern Red Sea is characterized by a greater diversity than the north where only seven species are considered regular. It is unclear whether the higher diversity observed is driven by more favourable environmental conditions (i.e., temperature, salinity, nutrients) or by the proximity to the Indian Ocean, where 31–33 cetacean species are known to occur (Ballance and Pitman 1998; De Boer et al. 2002; Kiszka et al. 2010; Jefferson et al. 2015) and may possibly venture in the Red Sea waters. The cetacean community in the Gulf of Aqaba reflects that observed in the northern part of the Red Sea with the main difference that the occurrence of T. truncatus is unclear. The apparent scarcity of S. plumbea is likely related to a lack of suitable habitat (lack of shallow waters, bays and a system of coastal reefs and islands). The Gulf of Suez is different from the rest of the Red Sea and Gulf of Aqaba, being relatively shallow and cold, with sandy/silty bottom sediment, and high water turbidity. Two species appear to be regular (T. aduncus and S. plumbea), while the presence and occurrence of T. truncatus is unclear and need further investigation. The most puzzling aspect of cetacean occurrence is the distribution of dolphins in the Suez Canal. T. aduncus and S. plumbea have been observed moving from the Red Sea in the canal up to the Bitter lakes (Mörzer Bruyns 1960; Pilleri and Gihr 1972; Robineau and Rose 1984; Beadon 1991; Notarbartolo di Sciara et al. 2017). S. plumbea seems to move along the entire canal since it has been sporadically observed in the Mediterranean Sea (Kerem et al. 2001; Notarbartolo di Sciara 2016). T. aduncus has not been reported in the Mediterranean Sea. It is unclear if this is due to species misidentiﬁcation, since its colour pattern and size are very similar to those of T. truncatus inhabiting the Mediterranean Sea (Beadon 1991; Kerem et al. 2012), or due to genuine lack of movement into the basin. It is also unknown how far the Mediterranean T. truncatus moves southward in the canal. Individuals of T. truncatus have been regularly observed at the entrance of the Suez Canal near Port Said and several have been found stranded along the Mediterranean coast nearby (I. Mohammed, pers. comm.).

297

Finally, it is unclear if these bottlenose dolphin populations mix and interbreed. M. novaeangliae does not seem to occur regularly in the basin. Information is scarce for the southern part of the Red Sea, although the rare individuals spotted might derive from the Southern Hemisphere populations or from the Arabian Sea one (Baker et al. 1993; Medrano-González et al. 2001). B. omurai was only recently described (Wada et al. 2003) and its range is poorly known. Several cetacean species or taxonomic groups generally found in tropical waters (i.e., sperm whale, melon-headed whales, pygmy killer whales, Fraser’s dolphin, and beaked whales) were not observed in the Red Sea. It is not clear if available habitats are unsuitable or if there is an aspect of semi-enclosed basins (such as the Mediterranean Sea or the Black Sea) that limits their ability to host the same cetacean species as the larger body of water to which they are connected (Costa 2015). Notarbartolo di Sciara et al. (2017) suggested that shallow waters (less than 200 m) extending north from the Strait of Bab al Mandab for about 180 km might form a barrier for deep-diving species such as sperm whales and beaked whales. In recent years, a large effort has been made to better understand the status of the cetacean community in the Red Sea. In Egyptian waters in particular, a flourishing tourism industry (UNEP-PERSGA 1997; Cesar 2003; Hilmi et al. 2012) and the work of local non-governmental organizations (i.e., the Hurghada Environmental Protection and Conservation Association—HEPCA) have contributed to the improved collection of cetacean observations at sea that, together with systematic surveys, provided important information about species presence, abundance, distribution and habitat use (Costa 2015). In the central and southern region of the basin cetacean surveys have just began due to the intensiﬁcation of dive tourism and it is considered likely that the number of species occurring in the Red Sea will increase as effort intensiﬁes. In Sudan few scientiﬁc reports have been published (Salam 2006; Nasr et al. 2012), and several dive guides working on the small fleet of diving vessels operating in the winter months are recording encounters with marine megafauna (marine mammals, sea turtles, sharks) (Massimo Bicciato, Compagnia del Mar Rosso, pers. comm.). In Eritrea cetacean observations have been gathered by the Marine Resources Research Division of the Eritrean Ministry of Marine Resources (2006–2016), contributing to the description of a ‘new’ species for the Red Sea (K. sima) and the conﬁrmation of the presence of S. bredanensis (Abraha et al. 2008; Notarbartolo di Sciara 2017). In Saudi Arabia several surveys have been carried out in past years, collecting important information about cetacean presence and distribution (Scott 1995; Gladstone and Fisher

298

2000; Al-Mansi and Sambas 2006; Al-Mansi 2009) and the description of a ‘new’ species—S. coeruleoalba—for the Red Sea (Hagan 2006). The ﬁrst aerial survey ever made in the Red Sea was carried out in 1986/87 by the Saudi Arabian Government (Meteorology and Environmental Protection Administration) to understand the status of conservation of the dugong (Dugong dugon) along the Saudi coasts (Preen 1989). However, cetacean data collected during this work remain unpublished and attempts to contact the author failed. Finally, the Israel Marine Mammal Research and Assistance Center (IMMRAC) has been collecting information on cetacean movements in the Bay of Eilat since 1994. Although the Red Sea can still be considered as relatively pristine (Notarbartolo di Sciara et al. 2017), the rapid growth of human activities along its coast, the presence of a well-developed oil industry, and the effects of climate change are generating concerns about cetacean conservation (IWC 2010). The limited information available for a large part of the basin is hampering the effectiveness of the strategies developed for cetacean conservation (Fouda and Gerges 1994; PERSGA 1998, 2002, 2004). The authors recommend that in the future dedicated surveys should be carried out in the central/southern part of the Red Sea to ﬁll this gap in knowledge about cetacean presence and distribution. Acknowledgements The authors would like to thank the Italian Cooperation in Egypt, the Hurghada Environmental Protection and Conservation Association (HEPCA), the University of Otago, the University of Hong Kong, the University of St. Andrews, the Earthwatch Institute, the Rufford Small Grant Foundation, and Boomerang for Earth Conservation for their ﬁnancial, logistic and scientiﬁc support during the long years of research in Egypt. We acknowledge the important contribution of Giuseppe Notarbartolo di Sciara, Amr Ali, Mahmoud Hanafy, Dani Kerem, Chris Smeenk, Daphna Feingold, Peter Rudolf and Yohannes T. Mebrahtu in advancing our understanding of the scientiﬁc, economic and social implications of the Red Sea. We thank David S. Janiger for the library of Marine Mammals, and are pleased to acknowledge Angela Ziltener, Maha Khalil, Elke Bojanowski, Islam El-Sadek, Mahmoud Ismail and the Egyptian diving centres for sharing their knowledge with the authors. We are also grateful to the ﬁeld assistants and volunteers who supported the ﬁeld work. Comments by the editors and reviewers on earlier drafts greatly enhanced the quality of this work. This chapter is dedicated to Amr Ali (1971–2016), whose brilliant visions and passionate dediction revolutionised the ﬁeld of marine resources conservation in Egypt.

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M. Costa et al. the 1991 Gulf War oil spill. NCWCD, Riyadh and Senckenberg Institute, Frankfurt, pp 438–458 Robineau D, Rose J-M (1983) Note sur le Stenella longirostris (Cetacea, Delphinidae) du golfe d’Aden. Mammalia 47(2):237–246 Robineau D, Rose J-M (1984) Les Cétacés de Djibouti - Bilan des connaissances actuelles sur la faune cétologique de la mer Rouge et du golfe d’Aden. Bull Muséum National d’Histoire Naturelle. Section A, Zoologie, Biologie Écologie Animales 6(1):219–249 Roghi G, Baschieri F (1956) Dahlak. With the Italian National Underwater Expedition in the Red Sea. Translated from the Italian. Nicholas Kaye, London Roman J, McCarthy JJ (2010) The whale pump: Marine mammals enhance primary productivity in a coastal basin. PLoS ONE 5(10): e13255 Ross GJB (1977) The taxonomy of bottlenosed dolphins Tursiops species in South African waters, with notes on their biology. Ann Cape Prov Mus (Nat History), vol 11, pp 1–194 Ross GJB, Heinsohn GE, Cockcroft VG, Parsons ECM, Porter L, Preen A (1995) Review of the taxonomic status of humpback dolphins, genus Sousa. Report to the Workshop on the Biology and Conservation of Small Cetaceans and Dugongs of Southeast Asia, Dumaguete, Philippines, UNEP/SEA95/WP 19:1–20 Röthig T, Spaet JLY, Kattan A, Schulz IK, Roberts M, Roik A, Voolstra CR (2016) Repeated observations of cetaceans and carcharhiniformes associations in the Red Sea. Marine Biodivers 46(1):25–26 Rüppell E (1842) Beschreibung mehrerer neuer Säugethiere, in der zoologischen Sammlung der Senckenbergischen naturforschenden Gesellschaft beﬁndlich. Abhandlungen aus dem Gebiet der beschreibenden Naturgeschichte 3:91–196 Salam MYA (2006) Marine and coastal environment conservation in Sudan: The role of marine protected areas. Workshop on the post-conflict national plan for environmental management in Sudan, Khartoum, July 2006. 31 pp. http://bit.ly/1jAeXob Sasaki T, Nikaido M, Wada S, Yamada TK, Cao Y, Hasegawa M, Okada N (2006) Balaenoptera omurai is a newly discovered baleen whale that represents an ancient evolutionary lineage. Mol Phylogenetics Evol 41:40–52 Schröder H, Schulze G (1981) Tierbeobachtungen unterwegs. In: Schröder H (ed) ’Acropora 1976 und 1979’, zwei meeresbiologische Sammelreisen ins Rote Meer. Meer und Museum 2:60–64 Sclater WL (1891) Genus Steno. In: Catalogue of Mammalia in the Indian Museum, Calcutta. Part II. Rodentia, Ungulata, Proboscidea, Hyracoidea, Carnivora, Cetacea, Sirenia, Marsupialia, Monotremata. Trustees Indian Museum, Calcutta, pp 324–325 Scott DA (1995) A directory of Wetlands in the Middle East. IUCN, Gland, Switzerland and IWRB, Slimbridge, UK, pp 1–31 Sea Around Us Project (October 2017) Large marine Ecosystems. Retrieved from: www.seaarounds.org Searight S (2003) The charting of the Red Sea. History Today 53:1–2 Sharir Y, Kerem D, Gol’din P, Spanier E (2011) Small size in the common bottlenose dolphin (Tursiops truncatus) in the eastern Mediterranean: a possible case of Levantine nanism. Marine Ecology Prog Ser 438:241–251 Shawky AM, Aﬁﬁ A (2008) Behaviour of spinner Dolphin at Sha’ab Samadai, Marsa Alam, Red Sea, Egypt. Egypt J Biol 10:36–41 Shawky AM, Alwany MA, Zakaria S, El-Etreby SG (2015) Estimation of the abundance of the spinner dolphin Stenella longirostris using photo identiﬁcation technique in Samadai Reef, Red Sea, Egypt. Catrina Int J Environ Sci 10:61–73 Sheppard C, Price A, Roberts C (1992) Marine ecology of the Arabian region. Academic Press Sherratt S, Sherratt A (1993) The growth of the Mediterranean economy in the early ﬁrst millennium BC. World Archaeol 24:361–378

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Where Dolphins Sleep: Resting Areas in the Red Sea

17

Maddalena Fumagalli, Amina Cesario and Marina Costa

Abstract

Periods of physiological quiescence are ubiquitous in animals. Resting is a vital, vulnerable and delicate phase of reduced vigilance to external stimuli that, in all animals, includes sleep components. In dolphins, resting is characterised by low activity and mobility, and sleep is exclusively unihemispheric slow wave sleep (USWS), an arrangement compatible with the voluntary respiratory function. Physiological needs and ecological conditions affect the way individuals arrange their behaviour during the photoperiod in order to accommodate the desirable but incompatible resting, foraging, mating, travelling needs and opportunities, to optimise beneﬁts and minimise ﬁtness costs. The duration and quality of rest strictly depend on the surrounding environmental conditions and the phase is susceptible to interruptions and disruptions. If animals are chronically deprived of rest and sleep, the cumulative effects of the deprivation can impact individual physiology and cognitive abilities, to the extent that the viability of individuals and their populations may be compromised. Dolphin-based tourism operations affect resting and sleeping patterns in a number of species and can lead to short-term behavioural responses, as well as long-term detrimental consequences, on wild dolphin populations. Among the Red Sea species, the spinner and Indo-Paciﬁc bottlenose dolphins display M. Fumagalli (&) Department of Zoology, University of Otago, 340 Great King Street, 9054 Dunedin, New Zealand e-mail: [email protected]

diurnal resting patterns inside, or in proximity to, coastal reefs. This generates a situation of high conservation concern as these species become not only more accessible for the tourism industry, but also more heavily exposed to it during a critical phase. In these circumstances, a precautionary approach is required. The spinner dolphin resting behaviour is well described and provides an interesting and comprehensive case study on the management of human interactions on resting dolphins. The island-associated ecotype of the spinner dolphin (Stenella longirostris) feeds exclusively at night and retreats to bays and lagoons to rest during the daytime. Resting areas have been reported in Hawaii, Brazil, Fiji, and in the Red Sea off Egypt, Sudan and Saudi Arabia. The spatial-temporal constraints on resting and the scarce behavioural plasticity make the spinner dolphin particularly vulnerable to rest disruptions. Indeed, the long-established tourism industry was held responsible for population decline and changes in habitat use in the Hawaiian dolphin population. In the Red Sea, the scientiﬁc investigation of impacts is still preliminary, but the establishment and success of the Samadai Reef specially managed area in Egypt shows that science-informed, precautionary and pragmatic management of dolphin-based activities is possible even in data poor contexts. Rest being a vital life function and given the dependence of dolphins on speciﬁc selected sites, resting areas surge to a status of highly critical habitats. Adequate investigation of impacts and management of anthropogenic activities inside resting areas and in their proximity are therefore priorities and key actions for the conservation of wild dolphin populations.

M. Fumagalli A. Cesario M. Costa Tethys Research Institute, Viale G. B. Gadio 2, 20121 Milano, Italy A. Cesario Swire Institute of Marine Science, School of Biological Sciences, University of Hong Kong, Pokfulam Road, Hong Kong SAR, China M. Costa South Atlantic Environmental Research Institute (SAERI), Stanley Cottage, Stanley, Falkland Islands

Introduction Periods of physiological quiescence are ubiquitous in animals (Campbell and Tobler 1984; Cirelli and Tononi 2008). All animals, from unicellular organisms (Wijnen and Young 2006), to terrestrial and aquatic invertebrates (Hartse 1989)

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_17

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and vertebrates (reviewed in Siegel 2008) display circadian fluctuations in alertness. Quiescence is a time for recovery and regeneration, and is generally exhibited as a state of low activity, with reduced mobility and responsiveness (Siegel 2005, 2016; Zepelin et al. 2005; Cirelli and Tononi 2008). The occurrence, duration and quality of resting states have evolved in order to facilitate survival by minimizing risks for the resting individual (Siegel 2008), hence the characteristics of resting patterns are driven by a combination of individual and species-speciﬁc factors (e.g., age and sex, genetics, social system), and by the characteristics of the surrounding habitat during the photoperiod (Siegel 2005). In all mammals, rest includes a phase of sleep at least once per day (Zepelin et al. 2005). Sleep is deﬁned as a sustained quiescence in a species-speciﬁc posture, accompanied by reduced responsiveness to external stimuli, quick reversibility to the wakeful condition, and characteristic changes in the electroencephalogram (EEG) (Zepelin et al. 2005). The method of EEG spectral analysis is frequently used in mammalian studies (Campbell and Tobler 1984) as a primary deﬁning feature of sleep episodes. Electroencephalography, the study of electrical activity in the brain, is a sophisticated procedure requiring the placement of electrodes on the scalp of the subject and their connection to an electroencephalograph, which elaborates the brain’s electrical activity. The output of an EEG is a graphic representation of the type of neural oscillations, or brain waves, recorded in the subject. In sleeping subjects, patterns in wave amplitude and period can be used to characterise different phases of sleep (Dement and Kleitman 1957; Wolpert 1969; Dijk et al. 1997; Carskadon and Dement 2011). The investigation of sleep behaviour based on EEG proﬁles, however, has been forcibly restricted to species that can be successfully kept in laboratory facilities and equipped with the instrumentation needed (approximately 70 of the extant 5,000 + mammalian species, e.g., cats, rats, dogs, armadillos, dolphins; Siegel 2016). Sleep is associated with restorative and energy conservation processes (Zepelin et al. 2005), learning, memory processing, and brain development, and is therefore essential (Cirelli and Tononi 2008). It is co-regulated by a circadian process (Process C) and by a sleep-wake homeostatic process (Process S) (Borbély 1982). Process C, mediated by the circadian clock of the organism, coordinates internal processes and alertness levels with the light-dark cycle. Process C is independent of the preceding amount of sleep or wakefulness, while Process S generates a drive or pressure to sleep based on the accumulation of sleep-inducing substances in the brain, which is a function of the time elapsed since the last sleep episode (Borbély 1982). The vast majority of animals engage in multiple sleep periods during the day (polyphasic sleep, e.g., rodents, lemurs; Campbell and Tobler 1984), whereas modern humans are among the

M. Fumagalli et al.

mammalian species displaying one single consolidated daily sleep phase (monophasic sleep) (Zepelin et al. 2005). Although still needing to be fully resolved, the presence, quality, intensity and functions of sleep are thought to vary between species and across the lifespan (Siegel 2008). Research shows that animals experiencing extended periods of vigilance and wakefulness subsequently enter a condition termed vigilance decrement where alertness to predators, processing of information, communication, navigation, foraging, feeding, and other complex tasks are negatively affected (Dukas and Clark 1995). In humans, episodes of sleep loss have been correlated to negative immunological, endocrine, cardiovascular responses (Aldabal and Bahammam 2011), lower vigilance (Drummond et al. 2005; Van Dongen et al. 2003), and impaired decision making, information processing, communication, distraction, and cost-beneﬁt analysis (Harrison and Horne 2000). At a cellular level and in a number of animal species, sleep loss causes upregulation of genes involved in energy metabolism, synaptic potentiation, and response to cellular stress (Cirelli 2006). By impairing important functions and processes at cellular, systemic and organism levels, sleep loss can ultimately make individuals more vulnerable to threats (e.g., diseases, predation). Furthermore, the cumulative effect of sleep deprivation can displace or impact other behaviours that facilitate survival (Siegel 2005). In humans, sleep recovery is affected by the type of sleep loss (acute or chronic), the duration of recovery sleep, and the time allowed for recovery, with different aspects of performance and neurobehavioral function recovering at different rates (Banks et al. 2016). There is evidence that the deprivation procedure may also affect some aspects of sleep rebound (Siegel 2016). Occasional episodes of sleep deprivation can be compensated with lengthening and intensiﬁcation of subsequent sleep (Borbély and Tobler 1985) but, when the disruption persists, or the surrounding environment is not conducive to satisfactory rest and sleep recovery, the deprivation can accumulate and become chronic. In this case, the sleep loss may no longer be successfully compensated with opportunistic recovery sleep, and the organism be required to undertake major adjustments of the structural organisation of the normal sleep, including rearrangements in the distribution, duration, intensity and timing of sleep phases (Lima et al. 2005).

Rest and Sleep in Delphinids There are currently 92 species of whales, dolphins and porpoises (Perrin 2017) in the mammalian Infraorder Cetacea (or Cetartiodactyla, favoured by evolutionary mammalogists). Of these, 17 species (Costa et al. this volume) are known to occur in the Red Sea. This chapter speciﬁcally

17

Where Dolphins Sleep: Resting Areas in the Red Sea

focuses on toothed whales (suborder Odontocete) of the family Delphinidae, as the taxon includes best studied species (e.g., bottlenose dolphin, spinner dolphin) and is the most represented in the Red Sea cetacean fauna (Costa et al. this volume). Delphind species display a wide range of ecological and behavioural adaptations that make them fully adapted to life in the aquatic environment. These include exquisite anatomical, metabolic and behavioural adaptations to breath-holding and the crushing effects of pressure, which allow dolphin species to effectively span the water column and reach depths up to several hundred metres (Kooyman Table 17.1 Deﬁnition of resting state

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2009). Dolphins, like all cetaceans, need to regularly reach the surface to breathe via the blowhole, the nostrils of cetaceans, located above the eyes at the top of the head. Differently from terrestrial mammals, cetacean ventilation is a voluntary and deliberate act, which requires a level of consciousness in order to be executed. The occurrence of schools and individuals at the sea surface creates an opportunity to collect data and observations on behaviour, from which inferences on critical times and habitats associated with vital functions can be made (Norris and Dohl 1980; Hanson and Defran 1993; Perrin and Mesnick 2003; Lusseau and Higham 2004; Lusseau 2006;

Species

Deﬁnition

Reference

Common bottlenose dolphin

Dolphins engaged in slow movements as a tight group (i.e., less than one body length between individuals). Movements during rest were slower than those seen in slow travelling behaviour (approximately one knot) and the dolphins were occasionally stationary. Resting lacked the active components of the other behaviours described

Constantine et al. (2004), after Shane et al. (1986)

Common bottlenose dolphin

Resting dolphins moved slowly, usually did not maintain a speciﬁc direction of travel, and often floated at the surface for several seconds to over a minute

Heithaus and Dill (2002)

Indo-Paciﬁc bottlenose dolphin

Low activity level, dolphins moving slowly (speed 10 cm/day

White plague type II

WPII

Sphingomonas spp., Aurantimonas corallicida

*17 coral species but primarily affects Dichocoenia stokesi

Similar to WPI, but much faster rate of tissue loss (*2 cm/day)

WA

Richardson et al. (2001)

White plague type III

WPIII

Sphingomonas spp., Aurantimonas corallicida

Primarily affects Montastraea annularis and Colpophyllia natans

Similar to WPII but the rate of tissue desctruction is extremely high, leaving white skeleton with no turf algae development

WA

Richardson et al. (2001)

White pox

White Patch Disease, Patchy Necrosis

Serratia marcescens

Exclusively affects Acropora palmata

Irregular lesions from a few cm2 to 80 cm2 that can develop simultaneously on all surfaces of the colony

WA

Sutherland et al. (2010)

White syndrome

WS

Opportunistic bacteria (Vibrio sp. and Rhodobacteraceae for example) followed by ciliate hytohagy

Many coral species including Turbinaria, Acropora, Gonisatrea, Pocillopora, Porites, Pavona, Stylophora, Montipora, Faviidae

Diffuse areas of tissue loss exposing bare skeleton

IP, RS, A

Luna et al. (2010), Sussman et al. (2008), Sweet and Bythell (2012, 2015), Pollock et al. (2017)

Yellow band disease

Yellow Blotch Disease, YBD

Bacterial (Vibrio spp.)

Primarily Montastraeaspp.

Focal/multifocal blotches followed by a circular yellow to white margin

WA, IP

Cervino et al. (2008), Weil et al. (2009), Croquer et al. (2013)

disease (Glas et al. 2012). Recent studies have also looked more deeply into how the cyanobacterial mat is self-sustaining, and results show that it is the photosynthetic CO2-ﬁxation of the cyanobacterium which enhances productivity of organic matter within the lesion during disease development (see the conceptual model presented in Fig. 21.5 of Sato et al. 2016). As this chapter deals with diseases in the Red Sea it is ﬁtting to mention another study here which focused on describing the pathobiome associated with different ‘phases’ of BBD lesions affecting Favia corals in Eilat (Arotsker et al. 2016). They showed that the pathobiome varied signiﬁcantly with regard to these ‘phases’, that is, highly active, waning and non-active, and illustrated that speciﬁc groups of bacteria, Gamma/Epsilon proteobacteria, Bacteroidetes and Firmicutes altered relative abundance. Speciﬁcally, one particular cyanobacterial strain (BGP10_4ST) was consistently detected in all lesion samples regardless of the phase it was in, leading these authors to hypothesis the role of this bacterium in BBD at this location.

First Record in the Red Sea and Locations Identified to Date Cases of characteristic BBD signs have been reported throughout the Red Sea, in particular Egypt (Mohamed et al. 2012), Saudi Arabia (Green and Bruckner 2000) and in the Gulf of Aqaba near Jordan (Al-Moghrabi 2001). A study by Mohamed et al. (2012) reported that BBD was the most prevalent coral disease in Egypt and the coral Favia stelligera appeared to be the most susceptible species. This is consistent with other studies from the Great Barrier Reef that have shown other faviid corals to be highly susceptible (Willis et al. 2004). A particularly high prevalence of BBD was observed in reef sites closest to larger cities such as Dahab, Sharm El-Sheikh and Hurghada in Egypt (Mohamed et al. 2012). The earlier study by Antonius (1988) attributed the high occurrence of BBD around Jeddah, Saudi Arabia, to the high eutrophication resulting from sewage outfall and a similar scenario is likely to be occurring throughout the Red

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Fig. 21.1 In situ photographs of black band disease (BBD) infected different coral colonies (a–f) showing the poly-microbial BBD mat kills healthy tissue leaving behind dead tissue or bare skeleton

Sea, particularly in heavily industrialised or inhabited areas. Outbreaks of BBD have been reported in areas where anthropogenic stressors are greater, for example, where there are high levels of terrestrial runoff (Bruckner et al. 1997; Frias-Lopez et al. 2002), increases in eutrophication (Kutaand Richardson 2002) and pollution including human faecal contamination (Antonius 1985; Al-Moghrabi 2001; Frias-Lopez et al. 2002).

White Syndromes (WSs) Clinical Signs, Pathology and Epidemiology White syndrome is the collective term used to describe a coral disease that shows a distinct marked lesion interface between apparently healthy tissue and the denuded coral tissue/exposed coral skeleton (Fig. 21.2). In general, WS is usually reserved for coral diseases showing these signs in the Indo-Paciﬁc and other ‘white disease’ names are utilised in the Caribbean, such as white band disease (WBD) and white plague (WP), for example. However, this is by no means a steadfast rule and some studies report instances of white band disease in the Indo-Paciﬁc (Antonius 1985, 1988). Furthermore, disease terms more commonly used in aquaria, such as shut down reaction (SDR) and rapid tissue necrosis

(RTN), can also sometimes be found within the literature describing wild diseases identical to that of the more generic term WS (Antonius and Riegl 1998). Regardless of the name given to diseases with this sign (or more likely as a direct result of the difﬁculties associated with deﬁning speciﬁc individual diseases from this common characteristic), there are conflicting reports about the ‘causal agent’ of this ‘disease’. Some argue this is evidence enough to suggest that either: (1) there are multiple causes of WS (brought about by geographical location and host coral for example) and therefore they should be classed as different diseases, and/or (2) the disease is polymicrobial in nature (i.e., ‘dominant’ microbes can be identiﬁed but vary). The dominant ‘causal agent’ could vary depending on where the diseased coral is (depth, geographical location etc.), the time the lesion is sampled (time of day, season etc.), the method of sampling (drill, fragged etc.), the preservation method of the sample (ethanol, snap frozen etc.), and the type of analysis conducted to assess the microbiome (platform for next generation sequencing, primers utilised etc.) (see Sweet and Bythell 2015; Sweet and Bulling 2017; Pollock et al. 2017). Indeed, Pollock et al. (2017) concluded that although WS appears visually similar with regard to the ﬁeld signs, distinct etiologies could be found. We draw readers to the review by Bourne et al. (2015), in which the authors lay out the current understanding of WS in more detail. As stated

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Fig. 21.2 In situ photographs of white syndrome (WS) infected Acropora colonies (g–j) showing the disease lesion kills healthy tissue leaving behind dead tissue or bare skeleton

above, Bourne et al. (2015) highlight the need to retain the general term of WS for Indo-Paciﬁc corals showing signs of tissue loss lacking distinguishing macroscopic signs and with unknown aetiologies; however, they suggest the utilisation of more speciﬁc names once standardised criteria have been met. For example, the use of the Genera name of the coral preceding the term ‘white syndrome’ allows for differentiation between possible similar macroscopic disease signs affecting different hosts, that is, Acropora WS and Montipora. Furthermore the terms ‘acute’ and ‘chronic’ have also been used to separate out similar signs with varying speeds of progression (Aeby et al. 2010; Ushijima et al. 2012). Due to the above, we will not go into any detail over the proposed or highlighted causal agents of WS throughout the Indo-Paciﬁc (Table 21.1); however, current evidence suggests that the disease (singular or plural) appears to be caused by bacteria. Evidence for this stems from studies where antibacterial agents have been utilised to treat diseased colonies and where Koch’s postulates have been partially or fully fulﬁlled in certain cases (Sutherland and Ritchie 2004; Ben-Haim and Rosenberg 2002; Ushijima et al. 2012; Sweet and Bythell 2015). Numerous bacteria (including Serratia marcescens, Vibrio shiloi, V. coralliilyticus, V. owensii and V. tubiashii) have been identiﬁed and described as ‘primary’ causal agents, all of which exhibit near identical disease signs. More recently, Pollock et al. (2017) have identiﬁed another potential player in the WS

pathobiome, that of Rhodobacteraceae. This latter study went so far as to suggest that the presence of individual bacterium species or certain groups (Families, Class for example) might serve as one of the diagnostic tools of this disease. It should also be noted at this point, that although evidence does seem to strongly point to a bacterium or bacteria as the causal agent of WS, other microorganism groups should not be ignored. For example, the role protists play in this disease is evident and certain species of ciliates have been shown to be responsible for the characteristic disease sign, that is, the white band caused by denuded tissue and exposed coral skeleton adjacent to apparently healthy coral tissue (Sweet and Bythell 2015).

First Record in the Red Sea and Locations Identified to Date Antonius (1988) was the ﬁrst to report the occurrence of WS on corals from the eastern coast of the Red Sea. Later Antonius and Riegl (1997) reported WS on reefs off the Sinai Peninsula and more recently Mohamed et al. (2012) reported the presence of WS in Egypt. This latter study highlighted instances of WS at Hurghada and the Gulf of Aqaba and Favia stelligera and the plate coral Acropora hyacinthus appeared to be the most susceptible species. In the earlier study by Antonius and Riegl (1997) the decline of reef health (between Taba and Ras Mohamed in the Gulf

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of Aqaba) was linked to an increase in the observed frequency of WS (along with outbreaks of Drupella snails). Although no recent surveys have been conducted to highlight if this trend continues, it would come as no surprise if it has, as WS is linked to numerous stress events such as increased sea surface temperatures, pollution and sedimentation, for example (Selig et al. 2006; Redding et al. 2013; Pollock et al. 2016). Increases in prevalence throughout the Red Sea would therefore mirror reports throughout the rest of the Indo-Paciﬁc (Willis et al. 2004; Weil et al. 2012).

A. R. Mohamed and M. Sweet

(Antonius and Lipscomb 2001). Progression of the disease has also been reported to be slower than that of BBD, approximately 1 mm per week, compared to rates of >1 mm per day for BBD. SEB has now been shown to affect a wide range of coral species throughout the Indo-Paciﬁc, and the disease resembles that of its Caribbean equivalent (Caribbean Ciliate Infection—CCI) with the same ciliate H. Corallasia being present on both (Sweet and Séré 2015).

First Record in the Red Sea and Locations Identified to Date

Skeletal Eroding Band (SEB) Clinical Signs, Pathology and Epidemiology Skeletal eroding band (SEB) was the ﬁrst coral disease described from an Indo-Paciﬁc reef (Antonius 1999). SEB is thought to be caused by a ciliate infection (Halofolliculina corallasia), which erodes the coral skeleton and is characterised by the loricae or tests that speckle the skeleton in microscopic black marks (Antonius 1999) (Fig. 21.3k and l). Tissue damage occurs when the ciliates mechanically disrupt the tissue (through a process of physically spinning and chemical secretion) when embedding their loricae into the skeletal matrix. In some instances SEB can and probably often is misidentiﬁed as BBD (described above), however, the speckled appearance of the band associated with SEB should be used as a distinguishing feature between the two

Fig. 21.3 In situ photographs of diseased colonies of Pocillopora and Acropora infected with skeletal eroding band (SEB) (k, l), a Porites colony heavily infected with pink-line syndrome (PLS) (m) and Porites ulcerative white spots (PUWS) (n)

Winkler et al. (2004) were the ﬁrst to highlight the presence of SEB in the Red Sea and conducted surveys along the Jordanian coast of Aqaba, where prevalence was low and two genera, Acropora and Stylophora, were found to be affected. Later, Mohamed et al. (2012) reported a similar low prevalence of SEB off the coast of Egypt, but only at one site (Ras Za’farana, in the Gulf of Suez). Here, Stylophora and Pocillopora were shown to be affected.

Pink Line Syndrome (PLS) Clinical Signs, Pathology and Epidemiology Pink line syndrome (PLS) was ﬁrst reported in 1996 affecting the scleractinian corals Porites lutea at Kavaratti in

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the Lakshadweep Islands in the Arabian Sea (reviewed by Ravindran et al. 2015). PLS is characterized by the presence of a band of pink-pigmented tissue separating dead skeleton from apparently healthy tissue. This band may begin as a small ring and progress outward, horizontally, across a coral colony (Fig. 21.3m). As with other coral diseases, the zone of dead skeleton is white in appearance with no algal overgrowth, indicating a relatively rapid rate of disease progression (Ravindran and Raghukumar 2002). Two fungi (an unidentiﬁed non-sporulating fungus and a dark melanised fungus identiﬁed as Curvularia lunata), together with a cyanobacterium (Phormidium valderianum), have been isolated from PLS-affected corals and inoculated on healthy corals, successfully causing PLS-like infections (Ravindran et al. 2001). Histological examination of these infected corals showed atrophy of the epidermis and calcicodermis, along with the reduction in the number of zooxanthellae. However, some argue that the macroscopic evidence alone, that is, a band of pink pigmented tissue, is not always sufﬁcient to infer that a disease has manifested itself (Benzoni et al. 2010). Indeed, such signs (pink or purple colouration of the coral tissue) can occur due to any number of different mechanical disturbances and subsequent recovery (Schuhmacher 1992; van Woesik 1998; Benzoni et al. 2010) and care needs to be taken when describing such signs as PLS in ﬁeld surveys.

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more universal name (Woodley et al. 2015). However, similar issues may occur to that of WS discussed above. For example, a study by Arboleda and Reichardt (2010) stated (with evidence from an inoculation trial, fulﬁlling part of Koch’s postulates) that a Vibrio (sharing a close relationship to V. natriegens and V. parahaemolyticus) is the causal agent of PUWS. However, it should be noted that identiﬁcation of this Vibrio in this particular study relied on utilising the 16S rRNA gene and Vibrios (as a genera) are known to share signiﬁcant similarities to each other, particularly in the 16S region. The use of only one gene to identify Vibrios to species level is therefore not recommended (Séré et al. 2015) and so the pathogen is likely still unknown.

First Record in the Red Sea and Locations Identified to Date Ulcerative white spot disease (UWS) has been reported in reefs off Ras Umm Sid, Sharm El-Sheikh in the northern Red Sea (Mohamed 2011; Mohamed et al. 2012). Here, two families of coral, Faviidae and Poritidae appeared to be most susceptible. In particular, the prevalence of UWS was high in Goniastrea edwardsi and Porites lutea.

Brown Band Disease (BrB) and Growth Anomalies (GA) First Record in the Red Sea and Locations Identified to Date Only one study has shown evidence of PLS in the Red Sea to date (Mohamed et al. 2012). PLS was found to occur at low prevalence in Egypt and Porites lutea appeared to be the most susceptible coral, supporting previous studies by Ravindran et al. (2001) and Sutherland et al. (2004).

Porites Ulcerative White Spot (PUWS) Clinical Signs, Pathology and Epidemiology Porites ulcerative white spot disease (PUWS) was ﬁrst observed in the Philippines in 1996 and shown to affect, as the name suggests, massive corals from the genera Porites. The disease is characterised by discrete, bleached, round foci, 3–5 mm in diameter (Raymundo et al. 2003) (Fig. 21.3n). These foci either regress or progress to full tissue-thickness ulcerations that can coalesce resulting in mortality of the whole colony (Raymundo et al. 2003). Since its initial discovery, PUWS has been shown to affect a few other genera (Echinopora, Goniastrea, Heliopora, Favia and Montipora) and so the term UWS has been proposed as a

Two other diseases have been mentioned as present in the Red Sea, brown band disease (BrB) and growth anomalies (GA) (Bruckner and Dempsey 2015). Both these diseases have been reported in Sharm El-Sheikh, Egypt and Saudi Arabia; however, there is little further information to draw on at this time. BrB reflects signs of WS with the differentiation being a large brown band (giving the disease its name) that is comprised of a single ciliate species, Philaster guamensis (Willis et al. 2004; Sweet and Bythell 2012) (Fig. 21.4o). However, one study argues that microscopically speaking WS and BrB are indistinguishable (Sweet and Bythell 2012). Growth anomalies are a currently understudied coral disease and are likely to be common across all coral regions (Fig. 21.4p and q). Indeed, sometimes these are not included in regular disease surveys unless in obvious high abundance or prevalence. However, some studies have highlighted the signiﬁcant morbidity and decreased fecundity, which has been attributed to GA throughout the Indo-Paciﬁc (Aeby et al. 2011). Similar to WS, the genera names have also been proposed to precede the term GA, for example Acropora growth anomalies (AGA) and Porites growth anomalies (PGA) (Aeby et al. 2011). The same study also drew links in GAs with increases in human population levels. The etiology of GA remains unknown but is

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Fig. 21.4 In situ photographs of brown band (BrB) disease infecting Acropora, note the presence of the light brown band formed by the ciliate (o) and growth anomalies affected Acropora and Montipora colonies (p and q)

hypothesised to be caused by viruses, excessive UV radiation, a genetic predisposition, and environmental degradation (Worket al. 2015).

Physical Damage that Can Manifest as Disease Signs Some signs of compromised health are caused by physical damage and are often confused with diseases during coral health surveys. Here we briefly outline such signs in order to try to avoid such misidentiﬁcation. These include sediment damage, pigmentation response, predation-associated tissue loss and damage to the tissue due to competition.

Sediment Damage Sediment damage is manifested by the presence of diffuse areas of tissue loss associated with ﬁne sediment accumulating on the coral surface (Fabricius 2005). In the northern Red Sea in Egypt, Mohamed et al. (2012) reported tissue loss due to sediment damage at the Ras Zafarana reefs in the Gulf of Suez. The authors claimed that the increase in sedimentation might be a result of uncontrolled massive construction of recreational resorts and hotels in the vicinity of this reef in addition to the high weathering and high wind

speed, which are characteristic for this area (Edwards 1987). Land ﬁlling accompanied with increasing coastal construction activities and re-suspension of bottom sediments due to human trampling, SCUBA divers, tourist boat anchoring and destructive ﬁshing methods are the major sources of heavy sedimentation in coral reefs along the Red Sea coast of Egypt (Hawkins and Roberts 1997).

Pigmentation Response Pigmentation response has been described as a generalized stress response of the host coral to many varied agents (Willis et al. 2004). The response may vary in intensity and colour, and margins of pink, blue and yellow colours on different colonies or species might be observed (Fig. 21.5r and s). However, a distinctive feature of this response is the production of a bright pink material along a lesion border that may be accompanied by increased skeletalization of affected corallites. This causes a visible thickening of corallite walls (Raymundo et al. 2005). The massive coral Porites has been shown to be the genera most affected by this in areas of the northern Red Sea (Mohamed et al. 2012). In many instances, such pigmentation is likely to be misdiagnosed as one of the diseases described above, that of pink line syndrome, and great care should be taken in this regard.

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397

Fig. 21.5 In situ photographs of some compromised health signs. r, s show pigmentation response that might be a generalized response of the coral to stress, t shows tissue loss that might be due to predation from sea urchin and u shows competitive coral-coral interaction

Tissue Loss Due to Coral-Eating Invertebrates

Competition

There are numerous reef organisms that feed on coral tissue, either directly or indirectly (Stella et al. 2011). These include certain ﬁsh species (ﬁsh bites), sea urchins and snails, for example (Fig. 21.5t). Here we will only address predation by snails as this often manifests itself as WS. Corallivorous snails from the genus Drupella including D. cornus, for example, are likely to be found on any reef if you search hard enough. If care is not undertaken during disease surveys, Drupella predation often appears like WS signs, that is, the clear demarcation between apparently healthy tissue and the denuded coral skeleton. Often the snails hide during the day in crevices within the coral and so are not always obvious to the casual observer. As such, we suggest that searching for snails around any suspected WS lesion should be mandatory before assigning a ‘lesion’ into any given disease category. Interestingly, in a reef health survey conducted across 25 reefs in 1996 throughout the Gulf of Aqaba, there was only one reef (off Ras umm Sidd near Sharm el Sheikh) which was classiﬁed as in poor condition. The reef in question had suffered from a plague of D. cornus and a subsequent outbreak of WS after the event. It has previously been reported that at particularly high population densities, the snails’ scars are quickly colonized by ﬁlamentous algae and likely pathogenic bacteria resulting in the onset of diseases such as WS and BrB, for example (Boucher 1986). McClanahan (1994) suggested that reef management (i.e., no ﬁshing) is likely to play an important role in the intensity of the Drupella populations and resulting outbreaks.

Space and light are two of the most important limiting resources on a coral reef. Stony corals use two basic strategies to compete for space, indirect encounters (also referred to as ‘overtopping’) and direct interactions (i.e., aggression) (Genin and Karp 1994). A coral health survey in the Egyptian Red Sea reported various competition interactions between coral-coral, coral-sponge, and coral-algae (Mohamed 2011) (Fig. 21.5u). It is not our intention to go into great detail regarding competition here; however, it is important to note that in some instances evidence of competition is not always clear and some surveyors may mis-characterise this as a disease of sorts. For example, a ‘novel’ disease was reported in the southern Arabian Gulf by Korruble and Riegl (1998). This ‘disease’ was termed Arabian yellow band disease (AYBD); however, on closer inspection the disease looks more like competition from an (as yet undescribed) sponge species.

Conclusion Coral diseases affect coral reefs globally, however, the Red Sea is among the less explored regions in terms of coral diseases documentation. The few coral health surveys that have been conducted in the Red Sea do, however, show that the corals in this region are affected by the more common diseases and other compromised health signs prevalent

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throughout the rest of the Indo-Paciﬁc. It is likely that given increased survey effort more diseases will be described in this region. Red Sea coral reefs are renowned for their high species diversity and the ability to thrive in extreme environmental conditions, with high salinity and sea surface temperatures being the norm. Researching coral diseases in this area may allow scientists to unravel why some coral species are more susceptible to certain diseases than others. Comparable studies between regions (throughout the Indo-Paciﬁc, for example) are also needed and may highlight areas which could act as natural reserves or sanctuaries with regard to disease outbreaks in the changing ocean.

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399 metallothionein expression as a biomarker and histopathological study on liver and gills. World J Fish Mar Sci 2:174–185 Myers R, Lieske E (2004) Coral reef guide Red Sea. Collins Publishers, London, p 384 Nagelkerken IK, Buchan GW, Smith K, Bonair P, Bush J, Garzon-Ferreira L, Botero P, Gayle CD, Harvell CD, Heberer C, Kim K, Petrovic C, Pors L, Yoshioka P (1997) Widespread disease in Caribbean Sea fans: II. Patterns of infection and tissue loss. Mar Ecol Prog Ser 160:255–263 Pantos O, Cooney RP, Le Tisser MDA, Barer MR, O’Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the caribbean coral Montastrea annularis. Environ Microbiol 5(5):370–382 Peters EC (1983) The role of environmental-stress in the development of coral diseases and microparasite infestations. Am Zool 23:960 Peters EC, Halas JC, McCarty HB (1986) Calicoblastic neoplasms in Acropora palmata, with a review of reports on anomalies of growth and form in corals. J Natl Cancer Inst 76(5):895–912 Pollock FJ, Wada N, Torda G, Willis BL, Bourne DG (2017) White syndrome-affected corals have a distinct microbiome at disease lesion fronts. Appl Environ Microbiol 83:e02799-16 Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2016) Correction: sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS ONE 11(11):e0165541 Rasoulouniriana D, Siboni N, Ben-Dov E, Kramarsky-Winter E, Loya Y, Kushmaro A (2009) Pseudoscillatoria coralii gen. nov., sp nov., a cyanobacterium associated with coral black band disease (BBD). Dis Aquat Organ 87:91–96 Ravindran J, Raghukumar C, Raghukumar S (2001) Fungi in Porites lutea: association with healthy and diseased corals. Dis Aquat Org 47:219–228 Ravindran JC, Raghukumar C (2002) Pink line syndrome (PLS) in the scleractinian coral Porites lutea. Coral Reefs 21:252 Ravindran JC, Raghukumar C (2006) Histological observations on the scleractinian coral Porites lutea affected by pink-line syndrome. Curr Sci 90(5):720–724 Ravindran J, Raghukumar C, Manikandan B (2015) Pink line syndrome (PLS). In: Downs CA, Bruckner AW, Porter JW, Galloway SB, Woodley CM (eds) Diseases of coral. Wiley, Hoboken Raymundo LJ, Harvell CD, Reynolds T (2003) Porites ulcerative white spot disease: description, prevalence and host range of a new coral disease affecting Indo-Paciﬁc Reefs. Dis Aquat Organ 56:95–104 Raymundo LJ, Rosell KB, Reboton C, Kaczmarsky L (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis Aquat Organ 64:181–191 Raymundo LJ, Weil E (2015) Indo-Paciﬁc coloured-band diseases of corals. In: Downs CA, Bruckner AW, Porter JW, Galloway SB, Woodley CM (eds) Diseases of coral. Wiley, Hoboken Redding JE, Myers-Miller RL, Baker DM, Fogel M, Raymundo LJ, Kim K (2013) Link between sewage-derived nitrogen pollution and coral disease severity in Guam. Mar Poll Bull 73:57–63 Riegl B, Antonius A (2003) Halofolliculina skeleton eroding band (SEB): a coral disease with fossilization potential? Coral Reefs 22 (1):48 Richardson LL (1992) Red band disease: a new cyanobacterial infestation of corals. In: Cahoon LB (ed) Proceedings of the 10th American Academy of Underwater Sciences, 24–27 Sept 1992, Wilmington, NC. American Academy of Underwater Sciences, Costa Mesa, CA, pp 153–160 Richardson LL (2004) Black band disease. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Heidelberg, pp 325–336 Richardson L, Smith G, Ritchie K, Carlton R (2001) Integrating microbiological, microsensor, molecular and physiologic techniques

400 in the study of coral disease pathogenesis. Hydrobiologia 460:71– 89 Sato Y, Civiello M, Bell SC, Willis BL, Bourne DG (2016) Integrated approach to understanding the onset and pathogenesis of black band disease in corals. Environ Microbiol 18:752–765 Schuhmacher H (1992) Impact of some corallivorous snails on stony corals in the Red Sea. In: Proceedings of the 7th International Coral Reef Symposium, Guam, vol 2, pp 840–846 Selig ER, Harvell CD, Bruno JF, Willis BL, Page CA, Casey KS, Sweatman H (2006) Analysing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney J, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. American Geophysical Union, Washington, DC, pp 111–128 Séré MG, Schleyer MH, Quod JP, Chabanet P (2012) Porites white patch syndrome: an unreported coral disease on Western Indian Ocean reefs. Coral Reefs 31(3):739 Séré MG, Chabanet P, Turquet J, Quod JP, Schleyer MH (2015) Identiﬁcation and prevalence of coral diseases on three western Indian Ocean coral reefs. Dis Aquat Organ 114(3):249–261 Séré M, Wilkinson DA, Schleyer MH, Chabanet P, Quod JP, Tortosa P (2016) Characterisation of an atypical manifestation of black band disease on Porites lutea in the western Indian Ocean. PeerJ 4:e2073 Sheppard CRC (ed) (2000) The Red Sea: seas at the millennium—an environmental evaluation, vol 2. Elsevier Science, The Netherlands Smith GW, Ritchie KB (1995) Bacteriological studies on white-band disease of Acropora cervicornis. In: European Meeting of the International Society for Reef Studies, 5–9 Sept 1995 Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. UNEP World Conservation Monitoring Centre, University. California Press, Berkeley Stella JS, Pratchett MS, Hutchings PA, Johns GP (2011) Coral-associated invertebrates: Diversity, ecological importance, and vulnerability to disturbance. Oceanogr Mar Biol 49:43–104 Sussman M, Bourne DG, Willis BL (2006) A single cyanobacterial ribotype is associated with both red and black bands on diseased corals from Palau. DAO 69:111–118 Sussman M, Victor S, Willis BL, Bourne DG (2008) Coral pathogen identiﬁed for white syndrome (WS) epizootics in the Indo-Paciﬁc. PLoS ONE 3(6):e2393 Sutherland KP, Ritchie KB (2004) White pox disease of the Caribbean Elkhorn coral, Acropora palmata. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, pp 289–297 Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Paciﬁc zooxanthellate corals. Mar Ecol Prog Ser 266:273–302 Sutherland KP, Porter JW, Turner JW, Thomas BJ, Looney EE, Luna TP, Meyers MK, Futch JC, Lipp EK (2010) Human sewage identiﬁed as likely source of white pox disease of the threatened Caribbean elkhorn coral Acropora palmata. Environ Microbiol 12 (5):1122–1131

A. R. Mohamed and M. Sweet Sweet MJ, Jones R, Bythell JC (2011) Coral diseases in aquaria and in nature. J Mar Biol Assoc UK 92:791–801 Sweet M, Bythell J (2012) Ciliate and bacterial communities associated with white syndrome and brown band disease in reef-building corals. Environ Microbiol 14:2184–2199 Sweet M, Burn D, Croquer A, Leary P (2013) Characterisation of the bacterial and fungal communities associated with different lesion sizes of dark spot syndrome occurring in the coral Stephanocoenia intersepta. PLoS ONE 8(4):e62580 Sweet M, Croquer A, Bythell J (2014) Experimental antibiotic treatment identiﬁes potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis. Proc R Soc Lond B Biol Sci 281:20140094 Sweet MJ, Bythell J (2015) White syndrome in Acropora muricata: non speciﬁc bacterial infection and ciliate histophagy. Mol Ecol 24:1150–1159 Sweet JM, Séré GM (2015) Ciliate communities consistently associated with coral diseases. J Sea Res 113:119–131. https://doi.org/10. 1016/j.seares.2015.06.008 Sweet MJ, Bulling MT (2017) On the importance of the microbiome and pathobiome in coral health and disease. Front Mar Sci 4:9 Ushijima B, Smith A, Aeby GS, Callahan SM (2012) Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian Reef Coral Montipora capitata. PLoS ONE 7(10):e46717 van Woesik R (1998) Lesion healing on massive Porites spp. corals. Mar Ecol Prog Ser 164:213–222 Weil E (2004) Coral reef diseases in the wider Caribbean. In: Rosenberg E, Loya Y (eds) Coral health and diseases. Springer-Verlag, Berlin, pp 35–68 Weil E, Croquer A, Urreiztieta (2009) Yellow band disease compromises the reproductive output of the Caribbean reef-building coral Montastraea faveolata (Anthozoa, Scleractinia). Dis Aquat Organ 87:45–55 Weil E, Irikawa A, Casareto B, Suzuki Y (2012) Extended geographic distribution of several Indo-Paciﬁc coral reef diseases. Dis Aquat Organ 98:163–170 Willis BL, Page CA, Dinsdale LA (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 69–104 Winkler R, Antonius A, Renegar DA (2004) The skeleton eroding band disease on coral reefs of Aqaba Red Sea. PSZNI Mar Ecol 25 (2):129–144 Woodley CM, Downs CA, Bruckner AW, Porter JW, Galloway S (2015) Diseases of coral. Wiley, Hoboken Work TM, Aeby GS (2006) Systematically describing gross lesions in corals. Dis Aquat Organ 70:155–160 Work T, Meteyer C (2014) To understand coral disease, look at coral cells. Eco Health 11(4):610–618 Work TM, Kaczmarsky LTV, Peters EC (2015) Skeletal growth anomalies in corals. In: Downs CA, Bruckner AW, Porter JW, Galloway SB, Woodley CM (eds) Diseases of coral. Wiley, Hoboken

Physicochemical Dynamics, Microbial Community Patterns, and Reef Growth in Coral Reefs of the Central Red Sea

22

Anna Roik, Maren Ziegler and Christian R. Voolstra

Abstract

Coral reefs in the Red Sea belong to the most diverse and productive reef ecosystems worldwide, although they are exposed to strong seasonal variability, high temperature, and high salinity. These factors are considered stressful for coral reef biota and challenge reef growth in other oceans, but coral reefs in the Red Sea thrive despite these challenges. In the central Red Sea high temperatures, high salinities, and low dissolved oxygen on the one hand reflect conditions that are predicted for ‘future oceans’ under global warming. On the other hand, alkalinity and other carbonate chemistry parameters are considered favourable for coral growth. In coral reefs of the central Red Sea, temperature and salinity follow a seasonal cycle, while chlorophyll and inorganic nutrients mostly vary spatially, and dissolved oxygen and pH fluctuate on the scale of hours to days. Within these strong environmental gradients micro- and macroscopic reef communities are dynamic and demonstrate plasticity and acclimatisation potential. Epilithic bioﬁlm communities of bacteria and algae, crucial for the recruitment of reef-builders, undergo seasonal community shifts that are mainly driven by changes in temperature, salinity, and dissolved oxygen. These variables are predicted to change with the

A. Roik (&) Marine Microbiology, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany e-mail: [email protected]; ; [email protected] A. Roik M. Ziegler C. R. Voolstra Red Sea Research Center, Division of Biological and Environmental Science and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia M. Ziegler Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany

progression of global environmental change and suggest an immediate effect of climate change on the microbial community composition of bioﬁlms. Corals are so-called holobionts and associate with a variety of microbial organisms that fulﬁll important functions in coral health and productivity. For instance, coral-associated bacterial communities are more speciﬁc and less diverse than those of marine bioﬁlms, and in many coral species in the central Red Sea they are dominated by bacteria from the genus Endozoicomonas. Generally, coral microbiomes align with ecological differences between reef sites. They are similar at sites where these corals are abundant and successful. Coral microbiomes reveal a measurable footprint of anthropogenic influence at polluted sites. Coral-associated communities of endosymbiotic dinoflagellates in central Red Sea corals are dominated by Symbiodinium from clade C. Some corals harbour the same speciﬁc symbiont with a high physiological plasticity throughout their distribution range, while others maintain a more flexible association with varying symbionts of high physiological speciﬁcity over depths, seasons, or reef locations. The coral-Symbiodinium endosymbiosis drives calciﬁcation of the coral skeleton, which is a key process that provides maintenance and formation of the reef framework. Calciﬁcation rates and reef growth are not higher than in other coral reef regions, despite the beneﬁcial carbonate chemistry in the central Red Sea. This may be related to the comparatively high temperatures, as indicated by reduced summer calciﬁcation and long-term slowing of growth rates that correlate with ocean warming trends. Indeed, thermal limits of abundant coral species in the central Red Sea may have been exceeded, as evidenced by repeated mass bleaching events during previous years. Recent comprehensive baseline data from central Red Sea reefs allow for insight into coral reef functioning and for quantiﬁcation of the impacts of environmental change in the region.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_22

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Introduction Coral reef ecosystems maintain a high species diversity, comparable to that of tropical rainforests, and they provide important ecosystem services such as provision of food, a source of income, and coastal protection (Reaka-Kudla 1997; Moberg and Folke 1999). The ecological and economic importance of coral reefs depends on the coral reef framework, which is essential for reef ecosystem functioning, as it provides habitats for reef species and thereby a foundation for ecosystem productivity (Graham 2014). Coral reefs are constructed by symbiotic reef-building corals that critically rely on sunlight and are limited to the warm and oligotrophic conditions of equatorial oceans (Buddemeier 1997; Wood 1999). These reefs predominantly exist in comparably stable physicochemical environments (Achituv and Dubinsky 1990; Wood 1999). Generally, reef-building corals live close to their upper thermal limit and are critically threatened by ocean warming (Wilkinson 1999). For this reason, coral reefs are among the ecosystems that are most susceptible to the consequences of global climate change (Hughes et al. 2003). Besides global stressors such as ocean warming and acidiﬁcation, local stressors such as eutrophication, pollution, and overﬁshing also constitute a threat to coral reefs worldwide (Spalding and Brown 2015). Today, environmental limits of coral reefs, responses of reef biota to stressors, and their potential for acclimatisation, adaptation, and resilience under environmental change are arguably the most relevant topics in coral reef research (Kleypas et al. 1999; Gove et al. 2013; Palumbi et al. 2014; Mumby and van Woesik 2014; Ochsenkühn et al. 2017; Osman et al. 2017). In this chapter, we present and characterise coral reefs in the central Red Sea and associated environmental conditions. Until recently access to this region was limited. Therefore, these reefs were sparsely studied and information about physicochemical conditions was commonly derived from remote sensing or short-term sampling events. However, in recent years the number of studies collecting in situ data from reefs in the central Red Sea has been growing (Berumen et al. 2013). We report on the most recent studies that provide comprehensive datasets and a baseline for coral reef research in this region. We begin by introducing the Red Sea coral reef ecosystems and describe the environmental regimes of coral reef habitats in the central Red Sea that demonstrate remarkable physicochemical structuring over spatial and temporal scales (Fig. 22.1). We discuss these environments in a global context and in relation to climate change. Next, we introduce biotic aspects of coral reefs, which are considered pivotal to reef functioning. We do this by presenting data on microbial (bacterial) communities that live in epilithic bioﬁlms and that influence larvae recruitment of reef-building coral species. We also report on microbes that associate with

A. Roik et al.

reef-building corals and are assumed to contribute to coral health and ﬁtness. After that, we address biological reef growth processes, the basis of reef habitat formation, including biogenic calciﬁcation and erosion (i.e., carbonate budgets). We highlight the measurable dynamics in the biotic realm and describe potential abiotic drivers of microbial community dynamics and reef growth processes in these coral reefs. We conclude by providing an overview of essential coral reef research questions to be addressed in this region.

Coral Reef Functioning in Challenging Environments—The Red Sea as a Case Study The Red Sea is located in one of the warmest climate zones globally and is one of the most saline seas (Edwards and Head 1987; Sheppard et al. 1992). Due to its geographic location spanning latitudes that are considered high for coral reefs (up to 28°N), the Red Sea is exposed to seasonal changes of physicochemical conditions (Raitsos et al. 2013; Sawall et al. 2015; van Hoytema et al. 2016; Roik et al. 2016). It includes some of the warmest coral reef environments, yet harbours some of the most diverse reefs worldwide (Sebens 1994; DeVantier et al. 2000). The Red Sea features remarkable coral reef formations along its entire coastline (Edwards and Head 1987; Price et al. 1998), while the neighbouring region of the Persian/Arabian Gulf (PAG) hosts marginal coral reef communities that hardly support reef growth (Riegl 1999; Purkis and Riegl 2005). In the Red Sea, challenging conditions such as high salinity and high temperature are paired with a remarkably high total alkalinity and aragonite saturation state, which are considered beneﬁcial for calciﬁcation and reef growth (Kleypas et al. 1999; Allemand et al. 2011). In addition, little terrestrial run-off and high light penetration (Schlichter et al. 1986; Sultan et al. 2015) also favour coral reef accretion. Strong latitudinal gradients of temperature, salinity, and nutrients (Raitsos et al. 2013; Kürten et al. 2014) give rise to a variety of habitats which can in part be considered challenging for coral reefs, especially in the southern and central Red Sea, where average sea surface temperatures are highest. This unique combination of challenging and beneﬁcial environmental conditions, as well as spatial gradients and seasonality make the Red Sea a valuable region to study coral reef dynamics. Reef-building corals and other reef organisms from these regions are expected to reveal physiological mechanisms and adaptations that can substantially contribute to the understanding of coral reef responses under environmental conditions that are predicted by global climate change projections. In this regard it is interesting to note that the northern Red Sea has been identiﬁed as a coral refuge, as it harbours corals that live well below their thermal threshold (Fine et al. 2013; Osman et al. 2017). Coral reefs of

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Physicochemical Dynamics, Microbial Community Patterns …

403

Fig. 22.1 Central Red Sea coral reefs. The map shows the coastal region of the central Red Sea between Jeddah and Thuwal (near KAUST). Coral reefs in this area span environmental gradients, suitable for the study of coral reef functioning under various environmental conditions. The marked reef sites are located along two environmental gradients, a cross-shelf gradient (reefs 1–3, marked with squares; Roik et al. 2016) and an anthropogenic gradient (reefs 4–9, marked with circles; Ziegler et al. 2016) near the city of Jeddah (map prepared by Ute Langner, King Abdullah University of Science and Technology (KAUST))

the Red Sea are increasingly threatened by environmental change and anthropogenic impacts alike (Atkinson et al. 2001; Loya et al. 2004; Raitsos et al. 2011; Ziegler et al. 2016), while their ecosystem functioning and global signiﬁcance is not yet fully understood. In the following, knowledge from the coral reefs of the central Red Sea is discussed under the consideration of recently contributed insights into reef functioning in this still understudied region.

Physicochemical Conditions in Central Red Sea Coral Reefs: Challenging High Temperatures, Low Dissolved Oxygen, Beneficial Carbonate Chemistry Environmental conditions in the central Red Sea partially deviate from conditions experienced in the majority of tropical coral reefs (Couce et al. 2012). Temperatures reach maxima of 33 °C (Davis et al. 2011; Roik et al. 2016) and the

summer average exceeds the global mean temperature for coral reefs by 1.4 °C (Kleypas et al. 1999). At the same time, salinity is about 5 PSU higher than the global coral reef average of 34.3 PSU (Table 22.1). Slowing coral growth rates (Cantin et al. 2010), decreased summer calciﬁcation rates (Roik et al. 2015), and repeated coral bleaching events during recent years (Monroe et al. 2018; Furby et al. 2013) demonstrate that temperatures in the central Red Sea exceed the thermal limits of local reef-building corals. Together, challenging summer temperatures and high salinity levels in the reef habitats of the central Red Sea reflect future predictions of ocean warming (IPCC Working Group I 2013). Adding to this, dissolved oxygen on central Red Sea reefs occasionally decreases below concentrations of 2 mg L−1, which is commonly considered hypoxic and a stressor to marine life (Vaquer-Sunyer and Duarte 2008). Low dissolved oxygen levels reflect the trend of deoxygenation in marine habitats that is also predicted to take place with the progression of ocean warming (Keeling et al. 2010).

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A. Roik et al.

Table 22.1 In situ environmental regimes in coral reef habitats of the central Red Sea

Environmental variable Temperature °C Salinity PSU −1

24.0−33.0 [29.0]

a

21.0−29.5 [27.6]

38.4−39.8 [39.3]

a

23.3−40.0 [34.3]b

a

Dissolved oxygen mg L

0.1−8.9 [3.5]

Nitrate and nitrite lmol L−1

0.1−1.0 [0.5]a

Phosphate lmol L

Worldwide(b)/GBR(c,

Central Red Sea

−1

0−0.10 [0.05]

Chlorophyll-a fluorescence lg L−1

d)

b

2.1−10.8 [6.7/7.0]c 0−3.3 [0.3]b

a

0−0.54 [0.13]b *0−4.0 [0.2/0.6]d

0−3.4 [0.4]a

The table shows the annual minimum, maximum, and mean in brackets for the central Red Sea and for other coral reefs worldwide. GBR = Great Barrier Reef References abased on continuous year-long measurements on reefs across the shelf, Roik et al. (2016); brange of estimated global averages for coral reefs [mean], Kleypas et al. (1999); crange of measurements on reefs at Heron Island (GBR) [means from two sites] [2]; drange derived from time series plots [lowest and highest mean from different reefs in the GBR], Schaffelke et al. (2012). Source Roik (2016)

total alkalinity (AT) and aragonite saturation state (Ωa) (Kleypas et al. 1999; Steiner et al. 2014), which support high biogenic calciﬁcation rates. A high buffering capacity of Red Sea waters against ocean acidiﬁcation can be assumed. Therefore, coral reefs in the Red Sea grow under conditions that represent a sharp contrast compared to some marginal coral habitats, such as Bermuda, the eastern tropical Paciﬁc including Galapagos and upwelling sites off Panama, where due to naturally low AT and Ωa, calcifying organisms are critically threatened by ocean acidiﬁcation (Manzello et al. 2008; Yeakel et al. 2015) (Table 22.2). Coral reefs thrive in the most oligotrophic parts of the oceans and low inorganic nutrient levels are essential to maintain healthy coral reefs (D’Angelo and Wiedenmann 2014; Rädecker et al. 2015). Hence, the highly oligotrophic conditions in the central and northern parts of the Red Sea (Silverman et al. 2007; Kürten et al. 2014) beneﬁt coral reef health. Nutrient levels and chlorophyll-a in the central Red Sea are lower than in most other reef locations (Table 22.1), but concentrations increase to the south (Raitsos et al. 2013; Sawall et al. 2014). In particular, phosphate concentrations (*0.07 µM) were remarkably low in the central Red Sea compared to other coral reefs worldwide (*0.08–0.6 µM; Szmant 2002). During summer, phosphate levels are further

With a dissolved oxygen concentration of about 2–4 mg L in the central Red Sea, the dissolved oxygen level is 3– 4 mg L−1 below what is measured at reefs, such as the Great Barrier Reef (GBR; Table 22.1), and also at reefs in the Gulf of Aqaba/Eilat (GoA) in the northern Red Sea (Badran 2001; Manasrah et al. 2006; Niggl et al. 2010). These low concentrations represent another aspect contributing to the challenging conditions for reef communities in the central Red Sea. Notably, these concentrations are likely driven by the comparatively higher temperatures that decrease oxygen solubility. While temperature data are routinely available from in situ measurements and remote sensing platforms, much less is known about the dynamics of dissolved oxygen in coral reef environments. In particular, only a few studies on coral reefs collected continuous dissolved oxygen data at a resolution that exceeded one sampling time per day. Hence, more continuous data and in-depth analyses of diel and seasonal patterns are needed to better understand the variability of dissolved oxygen on coral reefs and to estimate its effect on coral reef biota. Despite some challenging conditions for coral reefs in the central Red Sea, other environmental factors are actually considered beneﬁcial for benthic calcifying organisms and hence for reef growth. The Red Sea basin maintains a high −1

Table 22.2 Carbonate chemistry of central Red Sea coral reefs and global comparison

AT (lmol kg−1)

Region (study) a

Ωa

Central Red Sea (Roik et al. 2016)

2.346–2.431

4.50–5.20

Global preindustrial values (Manzello et al. 2008)b

*2.315

*4.30

GBR (Uthicke et al. 2014)c

2.069–2.315

2.60–3.80

Puerto Rico, Caribbean (Gray et al. 2012)d

2.223–2.315

3.40–3.90

Bermuda (Yeakel et al. 2015)

2.300–2.400

2.70–3.60

Panama, upwelling sites (Manzello et al. 2008)b

1.870

2.96

2.299

2.49

e

Galapagos (Manzello et al. 2008)

b

lowest and highest means per reef site and season (aragonite saturation state Ωa calculations were based on total alkalinity and pH measured on the NBS scale); bestimated averages, for details see referenced study; c lowest and highest means from reef sites during wet and dry seasons; dlowest and highest seasonal means from one site; eminimum and maximum from time series plots. Source Roik (2016) a

22

Physicochemical Dynamics, Microbial Community Patterns …

depleted, while nitrate and nitrite levels remain almost unchanged (Roik 2016). Such a shift in the nitrogen:phosphorus (N:P) balance toward a higher ratio has been previously demonstrated to decrease the heat and light stress tolerance of symbiotic reef-building corals in aquarium experiments (Wiedenmann et al. 2013) and might prove particularly calamitous during the summer. Whether an increased N:P ratio also decreases coral stress tolerance in situ still requires veriﬁcation. The naturally occurring inorganic nutrient ratios on the central Red Sea reefs offer an ideal case study to explore their influence on stressresistance of coral communities in more detail. Environmental conditions in central Red Sea reefs undergo spatio-temporal variability. This variability in many aspects is stronger than for many other tropical reefs. For instance, the annual temperature range spans up to 9 °C, which is 2–4 times larger than in most equatorial reefs (typically experiencing a range of 2–4 °C; Hume et al. 2013). This temperature range compares better to that of extreme regions that support marginal coral habitats, such as the Gulf of Oman (7 °C annual range) and the PAG (12– 20 °C, Hume et al. 2013). While reef temperature and salinity fluctuate the most between seasons, dissolved oxygen and pH undergo strong diel fluctuations that reflect biotic feedback of respiration, photosynthesis, and calciﬁcation of coral reef biota (Bates et al. 2010; Drupp et al. 2011). Chlorophyll-a and sedimentation rates in the central Red Sea vary over the cross-shelf gradient (Roik et al. 2016). Reef habitats span a range from highly oligotrophic offshore sites to more productive nearshore waters (Fig. 22.1; Table 22.1). Given the dynamic physicochemical conditions in central Red Sea reefs, the region is ideal to study reef-building communities and individual reef organisms in response to seasonal change and their local acclimatisation to spatially separated and challenging environmental regimes.

The Role of Microbial Communities in Coral Reef Functioning Coral reef research has historically focused on community composition of macrobenthic organisms such as corals and sponges (Benayahu and Loya 1977; Luckhurst and Luckhurst 1978; Done 1982), but more recently the role of microbial communities has come to the attention of research on coral reef functioning. Microbial communities are ubiquitous in coral reefs; they inhabit epilithic coral reef bioﬁlms (Sawall et al. 2012; Witt et al. 2012), and they associate with key-organisms of the coral reef, such as corals and sponges (Rosenberg et al. 2007; Hentschel et al. 2012). Microbial communities that live in marine bioﬁlms play pivotal roles in coral reef functioning. These roles include

405

contributions to nutrient cycles and ecosystem productivity (Wilson et al. 2003; Battin et al. 2003). Moreover, bioﬁlms play a role in larval settlement and recruitment of reef-building corals (Heyward and Negri 1999; Webster et al. 2004). Bacterial communities vary depending on the presence of different algal exudates that select for speciﬁc and functionally differential bacterial taxa (Barott et al. 2011; Nelson et al. 2013; Haas et al. 2013). For instance, bacterial communities, which induce high settlement rates of coral larvae (Sneed et al. 2015), are typically sustained in epilithic assemblages in the presence of certain coralline algae species. In contrast, algal turfs and associated bacteria reduce the settlement of marine invertebrates and inhibit survival of coral recruits (Arnold et al. 2010; Barott and Rohwer 2012; Webster et al. 2015). As a result, coralline algae dominance is associated with sustainable coral recruitment and reef growth. Under unfavourable conditions (e.g., high nutrient levels or overﬁshing) this state can rapidly shift towards a community dominated by turf algae, which is then likely to further develop into (macro) algal-dominated states and lead to the degradation of the coral reef habitat (Littler and Littler 1984; Hughes et al. 2007). Corals associate with unicellular dinoflagellate endosymbionts from the genus Symbiodinium and assemblages of other microorganisms (i.e., fungi, bacteria, archaea, and viruses), which together comprise the coral holobiont (Rohwer et al. 2002). These associations of microbial communities with reef-building corals underpin their success in oligotrophic, light-flooded warm oceans. Photosynthetic energy from Symbiodinium contributes substantially to the metabolic requirements and drives productivity of the coral host (Muscatine and Porter 1977). Carbon and nutrient cycling in the holobiont are further linked to the metabolism of the associated bacterial community (Rädecker et al. 2015). Bacterial associates are also suggested to play a crucial role in coral health and disease, and to fulﬁll symbiotic roles within the coral host (Rosenberg et al. 2007). Importantly, physiological acclimatisation to different habitats and environmental conditions can be achieved through changes of the associated microbial communities in the coral holobiont (Buddemeier and Fautin 1993; Reshef et al. 2006). Because microbial communities, both in bioﬁlms and associated as symbionts in corals, have the potential to alter patterns and functioning of coral reefs, a better understanding of their environmental drivers and dynamics is of great relevance.

Insights from Community Dynamics of Epilithic Bacterial Biofilms Among various bacterial habitats, such as the water column or in association with benthic invertebrates, epilithic bioﬁlms stand out for their remarkable diversity of bacterial taxa (Table 22.3). Coral- and sponge-associated bacterial

406 Table 22.3 Coral reef associated bacterial communities in the central Red Sea based on Operational Taxonomic Unit (OTU) richness and diversity

A. Roik et al. Bacterial habitat

Region of 16S rRNA gene

OTU richness estimate (Chao 1)

OTU diversity estimate (Inversed Simpson‘s Index)

Bioﬁlm

16S V 3–4a

400–900d

6–160d

a

d

Seawater

16S V 3–4

Seawater

16S V 5–6b b

Coral

16S V 5–6

Sponge

16S V 5–6c

140–270

4–13d

160–590e

2.5–7.8e

e

80–300

1.3–5.9e

300–700f

1.0–1.3f

OTU = operation taxonomic units, clustered at a similarity cut-off of 97%; aKlindworth et al. (2012); b Andersson et al. (2008); cSimister et al. (2012); dminimum and maximum per sample from Roik et al. (2016), e minimum and maximum per sample from Röthig et al. (2016b); Ziegler et al. (2016), only data from undisturbed sites are shown, coral species: Acropora hemprichii, Pocillopora verrucosa, Pleuractis (Fungia ) granulosa;flowest and highest means from Moitinho-Silva et al. (2014), sponge species: Xestospongia testudinaria, Stylissacarteri. Source Roik (2016)

communities exhibit a lower diversity and typically display a highly structured composition often dominated by only a few bacterial families that reflect a selective bacterial habitat (Moitinho-Silva et al. 2014; Röthig et al. 2016b; Ziegler et al. 2016). In contrast, coral reef bioﬁlms in the central Red Sea are characterised by a considerably higher diversity and richness (with up to 900 distinct Operational Taxonomic Units (OTUs) according to Chao1 estimator for species richness). A total of 16 bacterial families were dominant during the timeframe of a full year in all studied reef habitats from near- to offshore (Fig. 22.2a; Roik et al. 2016). Amongst these families were Rhodobacteraceae (Proteobacteria) and Flavobacteriaceae (Bacteroidetes) of which some taxa represent rapid surface colonisers and might act in the formation and maintenance of the bioﬁlm (Dang et al. 2008). But, while some species of Rhodobacteraceae are also known to enhance coral recruitment (Sharp et al. 2015), others might act as pathogenic opportunists in coral disease (Sunagawa et al. 2010; Roder et al. 2014a, b). If bioﬁlms were considered a reservoir of bacterial diversity that may provide a source of new taxa to the microbiomes of benthic invertebrates (e.g., reef-building corals), they may play an important role in contributing to organism disease or health, for example, through transmission of pathogens (Rosenberg et al. 2007) or provision of new physiological functions to the host (Bourne et al. 2016). Overall, implications and the potential of the high bacterial diversity and functions of certain bacterial taxa in coral reef bioﬁlms are still unknown and warrant further study. In the respective full-year study, bacterial community data were collected simultaneously with abiotic information across spatial and temporal scales allowing for the investigation of abiotic-biotic interactions (Roik et al. 2016), an approach that has been proposed recently for studying ecosystem functioning under consideration of natural variability and synergistic effects of multiple environmental drivers (Boyd and Hutchins 2012; Helmuth et al. 2014). Benthic bacterial assemblages in the central Red Sea reefs

were dynamic along a cross-shelf gradient of reefs, but also between seasons. Their species (OTU) diversity increased during spring and summer when growth of epilithic algae on the reef surfaces was highest. This observation supports the notion of an interaction of algal and bacterial communities via the release of algal exudates that incite bacterial metabolism (Barott et al. 2011; Haas et al. 2013). Furthermore, the increase in algal cover and bacterial diversity coincides with the timing of coral reproduction in spring and early summer (Bouwmeester 2014) and deserves further speciﬁc investigation to understand the possible implications for coral recruitment in the central Red Sea. Terrestrial run-off and chlorophyll-a were the most influential drivers/predictors of coral reef bioﬁlm communities in the GBR (Witt et al. 2012). In comparison, in the central Red Sea a combination of multiple variables (i.e., temperature, salinity, dissolved oxygen, and chlorophyll-a; Fig. 22.2b) correlated best with community shifts, and hence, are likely to drive bacterial bioﬁlm dynamics. Notably, these factors are predicted to change with the progression of global climate change (Keeling et al. 2010; IPCC Working Group I 2013). As a consequence, a restructuring of the bacterial assemblages is to be expected, and considering the role of bioﬁlms in coral recruitment, benthic community structure is very likely to be affected from bottom-up (Heyward and Negri 1999; Marhaver et al. 2013; Jessen et al. 2014). The comparative evaluation of winterand summer-speciﬁc community shifts can be considered a ﬁrst step leading to a better understanding of the community dynamics that can be expected under ocean warming scenarios (Table 22.4). Bacterial OTUs that were signiﬁcantly increased or decreased in the warmer seasons (Roik et al. 2016) can be considered candidates for temperature-sensitive taxa that presumably shift in abundance, responding to changes in temperature. Along these lines, this extensive data set on bioﬁlms provides a basis and poses new research questions for future investigations.

22

Physicochemical Dynamics, Microbial Community Patterns …

Relative Abundances (%)

(a)

407

(b)

100

2D Stress: 0.21 DO

spring 75

summer fall

50

Salinity

winter nearshore

Chlorophyll

25

midshore offshore Temperature

hore offs

mid sho re

nea rsho re

re

re

offs hore

mid sho

nea rsho

offs hore

mid sho re

nea rsho re

hore offs

mid sho re

nea rsho re

0

others (less 500 read count, 1004 OTUs)

OCS155 (Actinobacter ia, 3 OTUs)

unclassified (Bacteroidetes ,162 OTUs)

Saprospiraceae (Bacteroidetes, 225 OTUs)

Phyllobacteriaceae(Proteobacteria 39 OTUs)

Gloeobacteraceae (Cyanobacteria, 6 OTUs)

Erythrobacteraceae(Proteobacteria,12 OTUs)

Cyanobacteria, 65 OTUs) . Pseudanabaenaceae(

Xenococcaceae(Cyanobacteria16 OTUs) unclassified (Cyanobacteria, 70 OTUs) Pirellulaceae (Planctom ycetes, 85 OTUs) Halomonadaceae (Proteobacteria, 20 OTUs)

Alteromonadaceae(Proteobacteria, 131 OTUs)

unclassified (Proteobacteria, 785 OTUs)

Rivular iaceae(Cyanobacteria, 15 OTUs)

Synechococcaceae(Cyanobacteria,13 OTUs)

(Proteobacteria, 15 OTUs)

Hyphomonadaceae(Proteobacteria, 50 OTUs)

Flavobacteriaceae(Bacteroidetes,182 OTUs)

Pelagibacteraceae(Proteobacteria, 12 OTUs )

Flammeovirgaceae (Bacteroidetes.,163 OTUs)

Rhodobacteraceae(Proteobacteria, 213 OTUs)

Verrucomicrobiaceae(Verrucomicrobia, 79 OTUs) Rhodospir illaceae(Proteobacteria, 53 OTUs)

Fig. 22.2 Community composition and abiotic drivers of bacterial bioﬁlms in the central Red Sea. Epilithic bioﬁlm bacteria can influence macro-scale dynamics in the benthic community structure through their effects on the recruitment of invertebrate (in particular coral) larvae. Next-generation sequencing data of the bacterial 16S rRNA marker gene of year-long collected bioﬁlm samples from the central Red Sea (a) reveal a dynamic community structure that is characterised by a remarkably

Insights from Community Dynamics of Coral-Associated Microbes Reef-building coral species have distinct habitat preferences under which they perform at their best. They are also characterised by varying capabilities to acclimatise to changing environmental conditions. Their associated microbial symbionts represent a central component that influences acclimatisation and adaptation potential of the coral holobiont. Different Symbiodinium clades and species have different physiological and biochemical attributes, representing adaptations to distinct environments. These attributes can lead to differences in the performance of the coral host. For example, Symbiodinium clade D may confer increased thermal tolerance to its host, but leads to decreased growth rates in juvenile (Little et al. 2004) and adult corals (Pettay et al. 2015). In the Red Sea, corals associate with a large diversity of symbionts from the genus Symbiodinium that encompass phylogenetic and physiological differentiated strategies. Typically, each coral specimen harbours one or two abundant Symbiodinium types and a few background types that occur at very low abundances (Ziegler et al. 2017a). In the Red Sea, the majority of endosymbiotic dinoflagellates in most coral species can be assigned to Symbiodinium clade C and to a lesser extend to clade D, while species-speciﬁc

)

high OTU diversity (Operational Taxonomic Units, 97% similarity). (b) In situ abiotic variables that were simultaneously assessed allow for the exploration of abiotic-biotic interactions. A non-Metric Multidimensional Scaling (nMDS) approach based on Bray-Curtis similarities and multivariate correlation analysis identiﬁes temperature, salinity, dissolved oxygen (DO), and chlorophyll concentrations as potential abiotic drivers of community dynamics. (Source Roik et al. 2016, CC 4.0)

associations with clade A symbionts in corals from the family Pocilloporidae persist (Ziegler et al. 2017a). More speciﬁcally, clade C symbionts represent the largest diversity of all recorded Symbiodinium types in Red Sea corals and, interestingly, the prevalent but seemingly endemic type C41 was present in most coral hosts (Ziegler et al. 2017a). The ITS2 sequence of Symbiodinium C41 is highly similar to that of C1, and suggests a diversiﬁcation event speciﬁc to the Red Sea that requires further investigation. In the similar environmental settings of the PAG, the prevalence of the locally adapted species Symbiodinium thermophilum confers a high thermal tolerance to its coral hosts (Hume et al. 2016). In the Red Sea, Symbiodinium C41 may represent a similar opportunity to explore adaptations of the coral symbiont to local conditions and its role in host adaptation. The flexibility of the host-symbiont association plays a role in niche acclimatisation and ecological niche width of the coral holobiont. For example, two common coral species in the central Red Sea (Pocillopora verrucosa and Porites lutea) employ different strategies for niche acclimatisation in relation to the speciﬁcity of the coral-algae symbiosis. These coral species acclimatise between seasons and along environmental gradients of depth and distance to shore, either by establishing a speciﬁc symbiosis with a Symbiodinium type with a large physiological plasticity (P. verrucosa), or by forming different flexible associations with symbionts best adapted to the given environmental conditions (P. lutea;

408 Table 22.4 Candidates for temperature-sensitive bacterial taxa in epilithic coral reef bioﬁlms in the central Red Sea

A. Roik et al. Increased abundances with lower temperatures (winter) Bacterial species, family (Phylum)

Previously identiﬁed in

Reference (GenBank Accession#)

BLAST identity

Loktanella sp., Rhodobacteraceae (P)

Marine seabed sediments from an industrial harbor (Leghorn, Italy)

Chiellini et al. (unpublished) submitted (2012) (HE804021.1)

0.99

unclassiﬁed Phycisphaeraceae (PM)

Initial bioﬁlm formation on electrochemical CaCO3 deposition (Red Sea, Eilat)

Siboni et al. submitted (2009) (FJ594871.1)

0.99

Fulvivirga sp., Flammeovirgaceae (B)

Coral reef bioﬁlm (GBR, Australia)

Witt et al. (2011) (JF261960.1)

0.99

Fulvivirga sp., Flammeovirgaceae (B)

Coral reef bioﬁlm (GBR, Australia)

Witt et al. (2012) (JQ727158.1)

0.99

Winogradskyella sp. (bootstrap 93%), Flavobacteriaceae (B)

Coral reef bioﬁlm/crustose coralline algae (both: GBR, Australia)

Witt et al. (2011) (JF261857.1)/Webster et al. (2011) (HM177620.1)

0.99/0.98

unclassiﬁed Alphaproteobacteria (P)

Marine biofouling communities in heat exchanger

Taracido et al. (unpublished) submitted (2011) (GQ274234.1)

0.94

Increased abundances with higher temperatures (summer and fall) Bacterial species, family (Phylum)

Previously identiﬁed in

Reference (GenBank Accession#)

BLAST identity

Gloeobacter sp., Gloeobacteraceae (C)

Initial bioﬁlm formation on electrochemical CaCO3 deposition (Red Sea, Eilat)

Siboni et al. (unpublished) submitted (2009) (FJ594839.1)

0.99

unclassiﬁed Cohaesibacteraceae (P)

Scleractinian coral Acropora cervicornis (Caribbean)

Sunagawa et al. (2010) (GU118008.1)

0.99

Halomicronema sp., Pseudanabaenaceae (C)

Coral reef sediments (GBR, Australia)

Werner (unpublished) submitted (2006) (AM177412.1)

0.99

A4b (Ch)

Intertidal thrombolites (Bahamas, Caribbean)

Myshrall et al. (2010) (GQ484118.1)

0.99

unclassiﬁed Cystobacterineae (P)

Coral mucus (Red Sea)

Lampert et al. (2008) (EF576995.1)

0.97a

Rhodovulum sp, Rhodobacteraceae (P)

Microbial mat in hypersaline evaporation pond (Guerrero Negro, Mexico)

Kirk Harris et al. (2013) (JN446096.1)

0.98

unclassiﬁed Cystobacterineae (P)

Coral mucus (Red Sea)

Lampert et al. (2008) (EF576995.1)

0.97

unclassiﬁed Deltaproteobacteria (order: Myxococcales) (P)

Scleratinian coral Acropora palmata (Caribbean)

Pantos and Bythell (2006) (AY323192.1)

0.98b

Bacterial taxa with signiﬁcantly differential abundance patterns between cold and warm seasons are listed, including information about previous occurrence of identical or highly similar bacteria. Best BLASTn hits with 100% sequence coverage are shown, except a= 95% and b= 97% sequence coverage. If not speciﬁed otherwise, species classiﬁcation has a bootstrap value of 100%; P = Proteobacteria, B = Bacteroidetes, PM = Planctomycetes, C = Cyanobacteria, Ch = Chloroflexi; source Roik et al. (2016)

Ziegler et al. 2015a). The wide photoacclimatory potential of Symbiodinium can aid physiologically less flexible coral hosts like P. verrucosa to a relatively wide physiological niche as evidenced by the widespread occurrence throughout the Red Sea in this otherwise susceptible coral (Ziegler et al. 2014).

Host-symbiont associations may further limit and deﬁne light niches of corals as was ﬁrst described for Paciﬁc P. verrucosa and Pavona gigantea that harbour distinct Symbiodinium types and have distinct depth distributions (Iglesias-Prieto et al. 2004). In many coral species and locations the Symbiodinium community undergoes

22

Physicochemical Dynamics, Microbial Community Patterns …

depth-dependent shifts and may thus increase the depth distribution of their coral host (Frade et al. 2008; Lesser et al. 2010; Cooper et al. 2011). In contrast, corals in the Red Sea from the genera Porites, Pachyseris, Podabacia, and Leptoseris each maintain stable Symbiodinium communities over a 60 m depth gradient (Ziegler et al. 2015b), similar to several species in the genus Agaricia in the Caribbean (Bongaerts et al. 2013). Data of the same Symbiodinium type associated with different coral hosts in the Red Sea further reveal an effect of the host on the physiology of the symbionts (Ziegler et al. 2015b), thus adding another level of complexity to how Symbiodinium community dynamics may contribute to niche acclimatisation in corals. In contrast to coral-associated Symbiodinium communities that usually consist of only a few genotypes, coral-associated bacterial communities can consist of hundreds of taxa from many different phyla (Table 22.5). These diverse bacterial communities potentially entail a large diversity of functions that may beneﬁt the host (Bourne et al. 2016). Thus, bacterial communities represent a signiﬁcant potential for acclimatisation and adaptation of the coral holobiont (Bordenstein and Theis 2015; Ziegler et al. 2017b). Similar to the dynamics of the Symbiodinium community in the Red Sea, spatial and seasonal dynamics are also demonstrated for coral-associated bacterial assemblages. For instance, bacterial diversity in Ctenactis echinata from different central Red Sea reefs aligns with ecological differences between the sites, and bacterial composition is similar between reefs where these corals are abundant and successful (Roder et al. 2015). Microbial communities of Acropora hemprichii and Pocillopora verrucosa are structured according to the degree of anthropogenic impact and show a measurable anthropogenic footprint at polluted sites close to Jeddah, a city of over 4 million on the coast of the central Red Sea (Fig. 22.1; Ziegler et al. 2016). In these corals, host species-speciﬁcity of the microbiome is decreased at the most polluted sites (Ziegler et al. 2016). A similar pattern has also been observed in a mixed coral assemblage in the same area of impact, where microbial communities of hard and soft corals cluster by

Table 22.5 Microbial taxon richness across corals from the central Red Sea based on metabarcoding of the ITS2 and 16S marker genes for Symbiodinium and bacteria, respectively

409

impact and not by host organism (Lee et al. 2012). This loss of species-speciﬁcity of the bacterial community has previously been reported in diseased corals across ocean scales (Roder et al. 2014b). One of the best-known candidates for a bacterial coral-symbiont is found in the genus Endozoicomonas from the family Endozoicomonaceae (Neave et al. 2016). Endozoicomonas was one of the ﬁrst bacterial associates to be localised in endodermal tissues of a scleractinian coral and was consequently proposed to be a signiﬁcant member of the coral microbiome (Bayer et al. 2013; Neave et al. 2017). Bacteria from the genus Endozoicomonas are found in association with many coral species in the central Red Sea. These bacteria even dominate the microbiome with up to 75–90% in some specimens of Pocillopora verrucosa and Stylophora pistillata, respectively (Neave et al. 2017). Interestingly, each coral host species from the central Red Sea is associated with a distinct Endozoicomonas genotype, but speciﬁcity within different host species varies on a global scale (Roder et al. 2015; Ziegler et al. 2016; Neave et al. 2017). For instance, P. verrucosa harbours the same Endozoicomonas genotype throughout its global distribution range, while S. pistillata associates with geographically distinct genotypes (Neave et al. 2017). These different patterns were hypothesised to relate to the host species’ reproductive strategy, with higher geographic differentiation in brooding S. pistillata that transmits symbionts vertically and lower speciﬁcity in spawning P. verrucosa (Neave et al. 2017). However, the spawning coral A. hemprichii harbours distinct Enodozoicomonas genotypes between the polluted reef area close to Jeddah (Ziegler et al. 2016) and the more pristine area off Thuwal, 100 km to the north (Jessen et al. 2013). This indicates that other factors, for example, environmental stressors such as pollutants may also play a role in host-bacterial symbiont speciﬁcity. Indeed, the relative abundance of Endozoicomonas in coral microbiomes could be linked to habitat suitability, as illustrated in decreasing abundance toward less preferred/optimal habitats (Roder et al. 2015; Ziegler et al. 2016).

Coral genus

N

Symbiodinium OTUsa

N

Bacterial OTUs

Acropora

47

1–4

18

76–486b

17

104–908c

42

14–145d

Ctenactis Pleuractis (Fungia) Pocillopora Stylophora

7

2–4

32

62–865e

35

1–4

18

69–201b

16

25–140f

32

58–527f

23

2–6

OTU = Operational Taxonomic Unit, determined at 97% similarity cut off a all data from Ziegler et al. (2017a); bZiegler et al. (2016); cJessen et al. (2013); dRoder et al. (2015); eRöthig et al. (2016b); fNeave et al. (2016)

A. Roik et al.

GBudget [kg CaCO3 m-2 yr-1]

410

(a)

(b)

(c)

10

5

0

-5

maximum minimum -10 mean

ida f Tr act nd.

.

5

d rein

prei

ds p

.

eind ) pr

n Isla

A (Go

Ree

Se a

gin . Vir

Flor

U.S

Red 201

96

) 19

A (Go

014

lago

Se a

ea 2

hipe Arc gos Cha 012 an 2 ibbe Car 996 ia 1 nes

Indo

Red

ed S

R tral

n ther Nor

Cen

Fig. 22.3 Ranges of modern-day and preindustrial coral reef carbonate budgets. Carbonate budgets are a promising tool to track the trajectories of historical, modern-day, and future reef growth. (a) Central Red Sea reef budgets exceed the highest budgets of a northern Red Sea fringing reef (Dullo et al. 1996) and of the marginal reefs in (b) the Eastern Paciﬁc (Eakin 1996). Yet, these budgets are below the maxima from several other (often remote and minor impacted) coral reefs worldwide (Indonesia, Edinger et al. 2000;

Caribbean, Perry et al. 2013; and Chagos Archipelago, Perry et al. 2015). (c) Preindustrial estimates are based on fossil reef core analysis or a modelling approach (Hubbard et al. 1990; Dullo et al. 1996; Enochs 2015). In particular within the Red Sea, comparisons of modern-day carbonate budgets with historical estimates remain elusive due to sparseness of data. GoA = Gulf of Aqaba; preind. = preindustrial; only means of preindustrial reef growth are reported from the Red Sea (GoA) (Dullo et al. 1996)

To date, the signiﬁcance and functions of bacterial associates of the coral holobiont are largely unknown, although their role in coral health and disease has long been discussed (Rohwer et al. 2002; Reshef et al. 2006; Rosenberg et al. 2007; Bordenstein and Theis 2015). Analyses of whole genome sequences of several Endozoicomonas species, including taxa from Red Sea corals, indicate roles in sugar transport and protein secretion that may contribute to carbon cycling within the coral holobiont (Neave et al. 2014). Furthermore, in situ data suggest that restructuring of the microbiome could mediate environmental tolerance of the coral Pleuractis (Fungia) granulosato increased salinity (Röthig et al. 2016b). The bacterium Pseudomonas veronii was identiﬁed as one of the main contributors to putative functional shifts in the microbiome under high salinities. The same bacterial taxon was further found to be highly abundant in mucus from Porites spp. colonies in the Red Sea and PAG (Hadaidi et al. 2017), both regions characterised by high salinity, and thus it represents a second symbiotic candidate taxon in Red Sea corals. It is not yet clear to what degree bacterial communities influence holobiont physiological performance (Bourne et al. 2016), or interact with the Symbiodinium-coral symbiosis (Röthig et al. 2016a). Only

recently, Pogoreutz et al. (2017a) identiﬁed a potential link between bacteria and coral bleaching and also showed that susceptibility of bleaching is associated with diazotroph (i.e., nitrogen-ﬁxing bacteria) abundance (Pogoreutz et al. 2017b). Although progress has been made in deciphering functional aspects of coral-associated microbial community dynamics, future research employing functional microbial ecology approaches to the coral holobiont framework are necessary to further improve our understanding.

Biological Reef Growth Processes: Calcification and Carbonate Accretion as a Measure of Coral Reef Persistence The coral reef framework provides a living space for a range of highly diverse and productive coral reef biota (Graham 2014; Rogers et al. 2014). Not only calciﬁcation, but also processes of carbonate removal, i.e., erosion and dissolution, simultaneously influence the formation and maintenance of the reef framework (Glynn 1997; Perry and Hepburn 2008). Calciﬁcation of benthic communities (corals and coralline algae) contributes to reef growth, while dissolution and

22

Physicochemical Dynamics, Microbial Community Patterns …

bioerosion by parrotﬁsh, sea urchins, and endolithic bioeroders decrease reef growth and can lead to degradation of reefs when erosion rates exceed accretion (Glynn and Manzello 2015). A positive carbonate budget ensures the persistence of reef habitats, and is the result of high abundances of reef-builders and high calciﬁcation rates, which surpass rates of erosion. The estimation of carbonate budgets (i.e., carbonate net-production states) has proven valuable in identifying the state of reef ecosystems and quantifying potential reef degradation (Alvarez-Filip et al. 2009; Perry et al. 2013; Kennedy et al. 2013). Many coral reefs worldwide are characterised by negative (net-erosive) carbonate budgets, that are often related to an increased frequency of extreme climatic events (Eakin 2001; Schuhmacher et al. 2005) or local human impacts, such as pollution and eutrophication (Edinger et al. 2000; Chazottes et al. 2002). Environmental factors that influence calciﬁcation and erosion processes drive carbonate budgets. Temperature and carbonate chemistry are the most influential factors for calciﬁcation, implying the susceptibility of calcifying organisms to ocean warming and acidiﬁcation (Clausen and Roth 1975; Schneider and Erez 2006; Anthony et al. 2008; McCoy and Kamenos 2015). On the other hand, erosion is usually higher in turbid and nutrient rich habitats, because these are the preferred habitats of endolithic bioeroders (e.g., boring sponges, clams, and worms) (Pari et al. 1998; Chazottes et al. 2002). Also, low pH and a reduced carbonate saturation state can increase erosion rates (Wisshak et al. 2012; Fang et al. 2013) while reducing the calciﬁcation capacity of reef-builders, that leads to an additive negative effect of ocean acidiﬁcation on overall reef growth.

Insights from Coral Reef Calcification in the Central Red Sea Calciﬁcation is a temperature sensitive process. Observations along latitudinal temperature gradients have demonstrated that increasing temperatures, which remain below a certain threshold, enhance calciﬁcation rates in reef-building corals (Lough and Barnes 2000; Carricart-Ganivet 2004). However, when a critical thermal limit is exceeded, calciﬁcation rates decline as a result of thermal stress (Marshall and Clode 2004). Consequently, ocean warming compromises calcifying organisms. Speciﬁcally in reef-building corals, thermal stress disturbs the coral-dinoflagellate symbiosis and thereby is interfering with an important energy supply needed to maintain high calciﬁcation rates (Weis 2008). The study of reef calciﬁcation in the Red Sea is of interest, on the one hand, because it is one of the warmest regions with signiﬁcant coral reef formations and has been affected by comparably high warming rates over the past

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decades (Belkin 2009), both aspects being considered challenging for calcifying marine organisms. On the other hand, the carbonate chemistry in the Red Sea is comparable to coral reef preindustrial estimates and is considered beneﬁcial for biogenic calciﬁcation (Gattuso et al. 1999). Pelagic carbonate precipitation rates in the Red Sea were estimated to be higher than in the Gulf of Aden or the Indian Ocean (Steiner et al. 2014). In spite of this, benthic calciﬁcation rates of corals and coralline algae from the central Red Sea were not higher than elsewhere. For instance, the annual average calciﬁcation rates for the major reef-building coral genera Porites, Acropora, and Pocillopora did not exceed rates measured in other parts of the world (Roik et al. 2015). Calciﬁcation in the reefs of the central Red Sea might be on a trajectory of decline. First, calciﬁcation rates of Diploastrea heliopora, a massive-growing reef-building coral species, have decreased in correlation with gradually increasing sea surface temperatures over the past few decades (Cantin et al. 2010). Furthermore, Porites, Acropora, and Pocillopora exhibit an unusual seasonal pattern of calciﬁcation maxima during the cooler seasons rather than during summer, which is when calciﬁcation maxima are observed in a majority of other coral reefs worldwide (Crossland 1984; Hibino and van Woesik 2000; Kuffner et al. 2013). One possible explanation is that high temperatures during summer exceed the optima for calcifying organisms and limit their capacity for calciﬁcation. Also, coral bleaching events in the central Red Sea during the last decade support the notion that the thermal limits of many coral species have already been reached and exceeded (Monroe et al. 2018; Furby et al. 2013). However, it remains unresolved whether other conditions that are characteristic for the summer, for example, reduced dissolved oxygen and phosphate depletion, may contribute to the decrease in calciﬁcation of corals during the warmest season. High summer temperatures challenge calcifying organisms in the central and southern Red Sea, but not in the northern region where growth rates in various coral species (Stylophora pistillata, Pocillopora damicornis, and Acropora granulosa) reach their peaks in summer (Kotb 2001; Mass et al. 2007). In line with this, calciﬁcation in the coral P. verrucosa has an inverse seasonal pattern along the latitudinal gradient of the Red Sea basin. Calciﬁcation maxima occur during summer in the northern Red Sea, and during winter in the south, indicating limited adaptation to local environmental conditions in the central and southern parts (Sawall et al. 2015). It remains unclear whether other important reef-building corals follow the same latitudinal pattern, unless further in situ data from the southern region will be acquired to complement the ﬁndings from the central Red Sea (Roik et al. 2015).

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Carbonate Budgets in the Central Red Sea Estimates of carbonate budgets, or reef net-production states, mainly rely on in situ measurements of calciﬁcation and erosion rates in combination with census-based data to approximate the cumulative contribution of all biotic drivers of reef growth. These encompass benthic calciﬁcation rates and erosion rates of endolithic organisms and surface grazers, such as sea urchins and most importantly parrotﬁsh (Glynn 1997; Perry et al. 2012). Very few carbonate budget data are available from the Red Sea (Jones et al. 2015). The ﬁrst comprehensive account of reef growth in the Red Sea is from the Gulf of Aqaba in the northern Red Sea and shows calciﬁcation rates of corals, bioerosion measurements, and fossil reef growth estimates on a fringing reef (Fig. 22.3a and c; Heiss 1995; Dullo et al. 1996). Recently, carbonate budgets have been studied on central Red Sea reefs demonstrating a wide range of carbonate net-production states (Roik 2016). Reefs are characterised by net-erosion states in nearshore areas, while midshore and offshore reefs are in net-accretion states (Fig. 22.3a). According to these estimates, offshore reefs currently grow at twice the rate that nearshore reefs erode. The overall reef net-production states from the Red Sea are within the range of carbonate budgets from a variety of coral reefs worldwide (Fig. 22.3a and b; Eakin 1996; Edinger et al. 2000; Perry et al. 2013), but distinctly below the highest recorded budgets from remote and mostly unimpacted tropical reefs in the Indian Ocean (Fig. 22.3; Chagos Archipelago; Perry et al. 2015). In the central Red Sea, biotic and abiotic variables shape reef growth. Carbonate budgets aligned with the abundance of parrotﬁsh and also with the abundance of calcifying organisms (Roik 2016). Interestingly, total alkalinity was positively correlated with reef growth in the central Red Sea along the cross-shelf gradient, but differences along this gradient were in a relatively small range (*20– 50 lmol kg−1) (Roik 2016). Multiple laboratory, mesocosm, and in situ studies in various coral reefs report the positive relationship of benthic calciﬁcation and abiotic carbonate system variables, such as total alkalinity or carbonate saturation state (Langdon et al. 2000; Schneider and Erez 2006; Bates et al. 2010). The decrease of these variables due to ocean acidiﬁcation in many reefs worldwide may compromise carbonate production in the future (Gattuso et al. 1999), but the beneﬁcial carbonate chemistry in the Red Sea may delay the arrival of critically low total alkalinity and carbonate saturation due to ocean acidiﬁcation in this region. Yet, the notable influence of total alkalinity on reef growth in the central Red Sea indicates that even minor shifts in carbonate chemistry may bear large consequences for reef growth.

A. Roik et al.

As has been discussed previously, ocean warming is one of the major threats to calcifying organisms in the central Red Sea. As calciﬁcation rates have slowed over the past decades and are generally decreased during the warm season (Cantin et al. 2010; Sawall et al. 2015; Roik et al. 2015), it is important to elucidate whether overall reef growth in the central Red Sea is already impaired compared to historical rates of reef growth. Here, we compare recent carbonate budget estimates from the Red Sea with estimates of fossil reef growth rates during the Holocene (Fig. 22.3c; Hubbard et al. 1990; Enochs 2015). The lack of historical data from the central Red Sea impedes a direct comparison of the present-day budgets (Roik 2016) with reef growth in the past. The remaining comparison with 1995 estimates from the northern Red Sea (Dullo et al. 1996) leads to the notion that reef growth in the Red Sea has not decreased over the past decades (Fig. 22.3c). However, the latitudinal gradient of temperature, salinity and nutrients between the northern and the central Red Sea likely hampers this direct comparison. In order to consolidate this assumption further study of historical and present-day reef growth is required. Carbonate budgets are a promising tool to track the trajectories of modern-day and future reef states (Perry et al. 2012; Enochs 2015). Such data will be particularly valuable when evaluating the impact of disturbances in central Red Sea reefs. For this, the most recent carbonate budget study from 2014 (Roik 2016) may also prove a useful reference point to evaluate the impacts of the third global bleaching event 2015/2016 on coral reefs in the Red Sea (Monroe et al. 2018).

Conclusions and Outlook The central Red Sea is as a highly interesting region for coral reef research because of its spatially and seasonally dynamic environment, challenging conditions, and highly productive reef ecosystems. The recent accumulation of in situ environmental data and insights from the microbial ecology of reef bioﬁlms and corals provide new avenues for research questions to be addressed for coral reefs of this region (Box 1). Seasonal variability, high temperatures, high salinity, and low dissolved oxygen make the central Red Sea a challenging environment for coral reef biota whose mechanisms of acclimatisation and adaptation to these conditions are yet to be understood. The speciﬁc environmental conditions in the Red Sea allow for the in situ study of the influence of shifting inorganic nutrient (N:P) ratios on coral stress resistance. This may lead to a better understanding of the nutrient equilibrium between the different compartments in the coral holobiont and their relation to thermal stress susceptibility.

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Coral reef bioﬁlms in the central Red Sea harbour bacterial communities, which undergo seasonal cycles linked to the environmental dynamics. Comparison between winter and summer bacterial communities of bioﬁlms have guided the identiﬁcation of temperature-sensitive taxa, whose effect on coral reef functioning is likely to change with projected warming trends under global climate change. Bioﬁlm communities are of remarkably high bacterial richness and diversity. Beyond their influence on processes such as recruitment of reef biota, the relation between diverse bacterial bioﬁlm communities and the microbiomes of benthic reef invertebrates is unexplored and warrants further investigation. For instance, the consequences of a putative transmission of bacterial taxa from bioﬁlms to corals and possible effects to coral host ﬁtness remain to be determined. Understanding the dynamics, interactions and functions of these microbial taxa will enable us to better predict the consequences of, for example, temperature-related shifts on the coral reef ecosystem. Future research should also aim toward understanding the functional aspects of coral-associated algal community dynamics in the central Red Sea. For instance, the locally prevalent Symbiodinium type C41 represents an opportunity to explore adaptations to local conditions in the Red Sea as previously described for S. thermophilum in the Persian/Arabian Gulf (PAG). Furthermore, although much progress has been made in understanding the role of the bacterial coral-associate Endozoicomonas, experimental investigation should focus on elucidating its putative functions in the coral holobiont. In this regard, targeted functional proﬁling of other candidate taxa, such as P. veronii, may also increase our understanding of coral holobiont functioning. Lastly, understanding the influence of stressors on species-speciﬁc associations between corals and bacteria, such as the decrease of Endozoicomonas under adverse environmental conditions, will be critical in determining and better understanding coral health states. Repeated bleaching events and decreases in coral growth rates testify to the direct impact of global warming on coral reefs in the central Red Sea. In addition to high temperatures, other factors such as high salinity and low dissolved oxygen concentrations may be aggravated with the progression of climate change in the region, and the cumulative effects of these changes on coral growth and stress susceptibility remain elusive. The baseline of abiotic and reef growth data allows for tracking of the effects of disturbances, such as coral bleaching events, on overall ecosystem health. In the face of the global coral bleaching event of 2015/2016, these data are valuable for assessing long-term impacts and to track the recovery processes, which will provide insight into the resilience of central Red Sea coral reefs.

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Box 1. Knowledge gaps in coral reef functioning of central Red Sea reefs • detailed understanding of acclimatisation and adaptation mechanisms in reef biota to variable and challenging environmental conditions • influence of shifting inorganic nutrient (N:P) ratios on coral stress resistance • role of temperature-sensitive bacterial taxa in coral reef bioﬁlms • potential transmission of bacterial taxa from bioﬁlms to corals and consequences for host ﬁtness • locally adapted Symbiodinium types (e.g., type C41) • role of Endozoicomonas in the coral holobiont • osmoregulation of the different compartments of the coral holobiont • relationship between loss of bacterial speciesspeciﬁcity and reduced host-ﬁtness • cumulative effects of warm summer temperatures and other stressors on coral calciﬁcation and stress resilience • comparison of recent and historical carbonate budgets, assessment of the impact of the third global bleaching event of 2015/2016 on coral reef growth

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Meiofauna of the Red Sea Mangroves with Emphasis on Their Response to Habitat Degradation: Sudan’s Mangroves as a Case Study

23

Ahmed S. M. Khalil

Abstract

This chapter provides an overview on the meiofauna of mangroves in the Red Sea coast of Sudan, with an emphasis on the meiofaunal response to mangrove degradation. Investigations of meiofaunal response were based on comparing sites subjected to human impacts resulting in complete clearance and partial clearance of mangrove cover with a non-cleared site with intact mangrove cover in the southern coast of the Sudanese Red Sea. At the degraded mangrove sites, sediment sorting, mean grain size, water and organic contents in sediments changed signiﬁcantly, and the variation between shoreward (high-and mid-intertidal) and seaward (low-intertidal, shallow subtidal) zones intensiﬁed. These changes were attributed to modiﬁcation of the sediment depositional and reworking processes at the deforested sites. Correlated signiﬁcant changes in the structure of meiofauna at higher taxonomic levels were indicated by ANOSIM, resulting from the different responses of the various meiofaunal groups to the deforestation impact. Changes in the meiofaunal community structure at higher taxonomic levels were mainly due to increased copepod/nauplii and decreased nematode abundances at the deforested sites. Among other groups, abundances of Ostracoda, Acari and Kinorhyncha were also reduced, but some others, for example, Oligochaetes, Platyhelminthes, Gnathostomulida, Gastrotrichs, and Cnidaria became more frequent and abundant at the partially-deforested sites. Similar changes occurred at lower taxonomic levels in the nematode community structure. While changes in the abundance of different nematode species have contributed to the community variation at the deforested sites, the decrease in the abundance of Terschellingia sp. A. S. M. Khalil (&) Living Marine Resources and Climate Change, The Regional Organization for the Conservation of the Environment of the Red Sea and Gulf of Aden (PERSGA), Jeddah, Saudi Arabia e-mail: [email protected]

was the most important. The nematode species Shannon-Wiener diversity became signiﬁcantly higher at the partially-deforested site and lower at the completely deforested site, in comparison with the natural non-cleared mangrove site. The increased richness and diversity at the partially-deforested site, which was also indicated by species k-dominance curves, were attributed to the habitat heterogeneity of the patchy mangrove vegetation. These observations were also considered in the context of Connell’s intermediate disturbance hypothesis “with peak meifauna diversity at intermediate level of disturbance”. On the other hand, the results also recorded increased variability in the meiofaunal and nematode communities within the deforested sites, which was considered indicative of community stress. Seasonal variations of meiofaunal communities were also exaggerated at the deforested sites, which could be attributed to the decline of their resilience to seasonal changes due to loss of mangroves from the habitat. Among the nematode species, the relative abundance of selective deposit feeders showed a noticeable response, decreasing sharply at the deforested sites. This was related to the decline in the availability of organic/microbial food resulting from mangrove degradation. Other feeding guilds, especially non-selective deposit feeders, displayed an opposite trend, increasing in relative abundance as their feeding strategy might prove to be more energetically favourable with the decline of organic detritus and microbial contents at the deforested sites. Thus, the functional properties of the community were modiﬁed at the deforested areas, although nematode diversity was enhanced at the partially-deforested site. The overall feature of the change at the deforested sites was a shifting of ecosystem properties with consequent changes in the meiofauna, which indicated decline in the efﬁciency of the ecosystem function as a nursery ground for marine organisms, which represents one of the vital services provided by the mangrove ecosystem.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_23

419

420

Introduction Ecologists working on marine ecosystems have increasingly focused on the role of the meiofauna. Numerous descriptive studies on the temporal and spatial distribution of the meiofauna have been conducted (e.g., Dye 1983; Hodda and Nicholas 1985, 1986; Alongi 1987a, 1990; Nicholas et al. 1991; Vanhove et al. 1992) along with studies on trophic relations, interaction with epibenthos (e.g., Krishnamurthy et al. 1984; Dye and Lasiak 1986; Dittmann 1993, 1996; Schrijvers et al. 1995, 1997), nutrient recycling (Hopper et al. 1973), and the effects of physical/chemical disturbances (e.g., Alongi 1987b; Alongi and Christofferson 1992). The signiﬁcant role of meiofauna in energy flow in marine ecosystems is well known and documented. They help breakdown organic material into detritus, which facilitates their subsequent mineralization (e.g., Mclntyre 1968; Fenchel 1969; Gerlach 1971). Meiofauna greatly enhance biochemical transformations and metabolism of the community (Lee et al. 1974; Gee 1989), and they are an important food for the juveniles of many ﬁsh species and benthic macrofauna (Olafsson and Moore 1990). Because of their intimate association and dependence on sedimentary environments, high abundance, relatively sessile life styles, and short generation times, meiofauna have been widely used to study the effects of perturbations in aquatic ecosystems (Coull and Chandler 1992; Schratzberger and Warwick 1998). Meiofauna can also be maintained in relatively small volumes of sediment, so that changes in community structure can be observed in short-term experiments (Warwick et al. 1988). There is a range of publications assessing the effects of disturbance by different kinds of pollutants on meiofauna (e.g., reviews by Coulland Chandler 1992; Austen et al. 1994) using a variety of approaches in the ﬁeld, laboratory and in meso- and microcosms. The wide range of feeding habits enables meiofauna to occupy several trophic levels, while their relatively high density greatly enhances the flow of energy in the detrital subsystem (Dye 1983). Studying the response of meiofaunal communities to perturbations could thus help understand changes in ecosystem functions as indicated by the changes in the structure of the communities. This could be particularly important for mangroves, which represent one of the key tropical ecosystems that have faced degradation worldwide (e.g., Sasekumar 1993; Mastaller 1996, 1997), including in the Red Sea (Khalil 1994, 2015; Khalil and Krupp 1994). Based on these considerations, Khalil (2001, 2003) investigated the response of meiofauna to mangrove degradation in the central

A. S. M. Khalil

Red Sea coast in Sudan. Afterwards, some other similar studies were conducted in the region, for example., in Gazi Bay, Kenya (Mutua 2009; Mutuaet al. 2013) and yet again in the Red Sea coast in Sudan (Sabeel and Vanreusel 2015). Relatively few studies have been conducted on meiofauna in the tropical seas, compared to temperate and subtropical seas. Few meiofaunal studies have taken place in the Red Sea, most of which have been taxonomic (Andrassy 1959; Gerlach 1958, 1964, 1967). There have been some meiofaunal studies of ecology and distribution (e.g., Thiel 1979; Hanafy et al. 2011; El-Serehy et al. 2016). Recently, the linkages between the diversity of meiofauna and the functioning of marine ecosystems were investigated on a broader tropical geographical level including the Red Sea. The Red Sea meiofauna and prokaryoticheterotrophic production across seagrass, mangrove and reef sediments were investigated and compared in the three tropical oceans of the Caribbean, the Red and Celebes seas (Pusceddu et al. 2014). This chapter provides an overview of meiofauna of mangroves in the central Red Sea (Sudanese coast) with an emphasis on their response to the impacts of habitat degradation. Background studies that mainly contributed to this overview were conducted by the author (Khalil 2000, 2001, 2003) in the Sudanese Red Sea coast. The southern parts of this coast support sporadic growths of Avicennia marina mangroves, which have been subjected to different levels of human impacts, depending on the degree of the mangrove accessibility, and susceptibility to wood cutting and camel grazing. Investigations of meiofauna in these studies were based on three mangrove sites representing a completely cleared mangrove at Antabeeb, a partially cleared mangrove at Haidoub, and an uncleared mangrove at Sheikh-Ibrahim areas. Figure 23.1 shows the location of the area and a schematic diagram of mangrove sites focused on by the background studies that mainly contributed to this chapter. Meiofauna were investigated from core samples (/ = 3.5 cm collected to a depth of 5 cm) at high-, mid-, low- intertidal and subtidal zones, following extraction through repeated shaking and decantation (Higgins and Thiel 1988; Dittmann 1996). Nematodes were identiﬁed and studied based on Higgins and Thiel (1988), Warwick et al. (1998), Gerlach and Riemann (1973/1974), Lorenzen (1981), and Platt and Warwick (1983, 1988). Degradation impacts and the response of meiofauna were tested using univariate and multivariate methods. PRIMER (Plymouth Routines in Multivariate Ecological Research) software was mainly used in applying multivariate tests and calculating diversity indices, as well as constructing k-dominance curves for nematode species (Clarke and Warwick 1994).

23

Meiofauna of the Red Sea Mangroves with Emphasis …

421

Fig. 23.1 Location of mangrove sites with schematic diagram for the meiofaunal sampling zones at cleared, partially-cleared and non-cleared mangrove, which were investigated in studies carried out by Khalil (2001, 2003). The three sites are located south of Suakin town between 18°55′06″N, 37°24′43″E and 19° 04′50″N, 37°21′51″E. Hs, Ls: seasonal high and low seawater level Source Khalil (2001)

Extreme Conditions as a Limiting Factor Mangroves of the Red Sea grow in extreme natural conditions, which result in a harsh habitat with poor animal associations (Fishelson 1971). This may explain why there are relatively lower meiofaunal densities found in Red Sea mangroves compared to other tropical areas. Reported average densities in Sudan ranged between 98 and 983 individuals (ind.) 10 cm−2 in summer and 280–1650 ind. 10 cm−2 in winter, with a highest density of 2663 ind. 10 cm−2 in the studied mangrove areas of Sudan (Table 23.1). Hanafy et al.

(2011) also found relatively low meiofuna densities ranging between 100 and 130 ind. 10 cm−2 in littoral habitats of the northern Red Sea in Egypt. In comparison, Olafsson (1995) reported an average meiofaunal density of 1493 ind. 10 cm−2 and highest densities of 5263 ind. 10 cm−2 in mangrove areas in eastern Africa (Zanzibar). Also, Vanhove et al. (1992) recorded an average meiofaunal density of 3442 ind. 10 cm−2 in the sediments of Avicennia marina mangroves at Gazi Bay (Kenya), and even higher average densities in the sediments ofBruguierasp. and Rhizophora sp. mangroves. However, the average meiofaunal densities found in the Sudanese Red Sea

422 Table 23.1 Densities of total meiofauna (ind. 10 cm−2) in summer and winter from tidal zonesat the cleared, the partially-cleared and the non-cleared mangrove sites. Values are average densities with highest and lowest densities given between brackets. N = 4 for each station in each season

A. S. M. Khalil Site Cleared site

Partially-cleared site

Non-cleared site

Zone

Total meiofauna (individuals/10 cm²) Summer

Winter

High intertidal

98(82–116)

912(416–1543)

Mid intertidal

107(69–174)

689(358–1009)

Low intertidal

190(108–286)

1001(486–1424)

Subtidal

338(254–457)

820(688–996)

High intertidal

226(141–395)

381(225–542)

Mid intertidal

133(75–193)

280(181–477)

Low intertidal

983(544–1314)

457(316–562)

Subtidal

245(194–284)

1650(1069–2663)

High intertidal

150(69–213)

524(222–826)

Mid intertidal

141(91–245)

509(262–927)

Low intertidal

193(152–219)

507(408–849)

Subtidal

557(337–748)

696(251–1213)

Source Khalil (2001)

mangroves may compare well with those reported by some other studies in tropical areas. For example, in an extensive study investigating the meiobenthos in ﬁve mangrove estuaries in Australia, Alongi (1987a) recorded meiofaunal averages in the range of 74–1660 ind. 10 cm−2 for summer and 217–2454 ind. 10 cm−2 for winter at the different intertidal levels. The extreme conditions in the Red Sea mangroves may also restrict the number of species among meiofaunal groups. A total of 35 nematode genera were identiﬁed from these mangroves (Table 23.2), which is below the ranges recorded in several studies on mangrove habitats elsewhere. For example, Olafsson (1995) listed 94 nematode genera from mangroves in Zanzibar, and Somerﬁeld et al. (1998) reported 87 genera from a Malaysian mangrove forest. However, low numbers comparable with those recorded in the Red Sea in Sudan were reported elsewhere by some studies, for example, Sasekumar (1994) reported 51 nematode species from Avicennia sp. and 29 species from Rhizophora sp. mangroves in Selangor (Malaysia). In the Red Sea mangroves, higher meiofaunal densities were generally reported at low intertidal and subtidal levels, compared to mid- and high intertidal levels (Table 23.1). This agrees with ﬁndings by several studies on meiofauna in mangrove areas of other parts of the world, which reported the highest densities at low intertidal stations (Hoddaand Nicholas 1985; Alongi 1987a, 1990; Nicholas et al. 1991; Olafsson 1995; Dittmann 2000), although Dye (1983) found meiofauna in highest numbers at mid-water level. Alongi (1987a, 1990) concluded that physical factors accounted for such observed differences. This influence is probably more prominent under the extreme conditions of the Red Sea mangroves, as the meiofaunal abundance correlated well with such factors (see Table 23.3).

Modification of Sediment Characteristics at Degraded Mangroves The role of salt marsh vegetation that can actively trap sediment and enhance deposition is well documented in coastal sediment dynamics (Dyer 1986), especially that of mangroves (Davis 1940; MacNae 1968). Saenger et al. (1996) reported compaction of the soil, and modiﬁcation of sediment characteristics, sedimentation patterns and hydrological regimes in the ecosystem as the most obvious effects of mangrove over-cutting and clearing. In the Red Sea, modiﬁcation of sedimentary patterns, probably caused by the mangrove degradation, was indicated by increased variability within the partially-cleared and cleared mangrove sites in several features, for example, sediment sorting, mean grain size, and mud, water and organic contents in the sediments (Fig. 23.2). Generally, poorly sorted sediments were reported at all three mangrove sites (Fig. 23.2), which is in fact typical for estuarine areas with high silt/clay content (Dye 1983). However, the presence of the intact mangrove appears to play a role in improving the sediment sorting, as values declined signiﬁcantly for the degraded mangroves at the cleared and partially cleared sites (Fig. 23.2). Actually, these diment-transport regime plays a critical role in a variety of benthic ecological processes as shown by experimentation both in the ﬁeld and laboratory flumes (Snelgrove and Butman 1994). The Red Sea mangroves receive seasonal rainwater influx through valleys. The mangroves with their dense aerial roots (pneumatophores) enhance sediment deposition. They also cause the sediment reworking by waves and tidal movement to occur under moderate energy conditions, unlike extremely high-energy conditions, which were reported to produce very poorly sorted sediment

23

Meiofauna of the Red Sea Mangroves with Emphasis …

423

Table 23.2 Average abundance (ind. 10 cm−2) of nematode species in summer and winter seasons from the cleared, the partially-cleared and the non-cleared mangrove sites. N = 12 samples for each site in each of the summer and winter seasons Family

Species

Abundance (10 cm−2) Cleared site Summer

Winter

Partially-cleared site

Non-cleared site

Summer

Summer

Winter

Winter

Total

Axonolaimidae

Pseudolella sp.

0

0

0

4

0

0

4

Chromadoridae

Actinonema sp.

0

0

5

0

0

0

5

Comesomatidae

Cyatholaimidae Desmodoridae

Prochromadorella sp.

0

0

0

1

0

0

1

Ptycholaimellus sp.

0

0

4

0

0

1

5

Actarjania sp.

0

0

0

1

0

0

1

Dorylaimopsis sp.

0

0

0

9

0

0

9

Laimella sp.

0

0

0

1

0

0

1

Paracomesoma sp.

0

0

3

2

14

2

21

Sabatieria sp.

0

0

4

43

3

9

59

Paracanthonchus sp.

0

0

2

0

0

0

2

Pomponema sp.

0

0

1

0

0

0

1

Desmodora sp.

4

3

10

11

2

2

32

Metachromadora sp. Spirinia sp. Ethmolaimidae

42

1

15

18

29

17

122

0

0

49

114

1

2

166

Ethmolaimus sp.

0

46

0

1

17

0

64

Gomphionema sp.

0

0

0

1

0

0

1

Haliplectidae

Haliplectus sp.

0

6

0

8

0

1

15

Leptolaimidae

Camacolaimus sp.

0

0

1

4

0

0

5

Linhomoeidae

Halaphanolaimus sp.

0

0

15

35

0

1

51

Leptolaimus sp.

0

0

4

22

2

1

29

Metalinhomoeus sp.

0

0

4

12

1

5

22

Terschellingia sp.

0

0

143

184

100

330

757

Microlaimidae

Microlaimu ssp.

0

5

3

15

1

1

25

Monhysteridae

Diplolaimella sp.

0

0

2

0

1

5

8

Oncholaimidae

Siphonolaimidae

Diplolaimelloides sp.

0

0

0

0

2

0

2

Monhystera sp.

4

4

0

1

0

0

9

Oncholaimellu sp.

1

0

12

30

0

13

56

Oncholaimus sp.

3

1

0

0

1

1

6

Viscosia sp.

1

0

4

3

0

0

8

Siphonolaimus sp.

0

0

0

1

2

1

4

Tripyloididae

Tripyloides sp.

0

1

1

10

0

0

12

Xyalidae

Daptonema sp.

25

319

21

137

10

222

734

Steineria sp.

0

0

0

1

0

0

1

Stylotheristus sp.

0

0

0

9

0

6

15

Source Khalil (2001)

Theristus sp.

13

21

0

17

0

8

59

Total

93

407

303

695

186

628

2312

424

A. S. M. Khalil

Table 23.3 Correlations (r-values) of the abundances of total meiofauna and meiofaunal groups, and the nematode/copepod (N/C) ratio with some physical variables at the sampling sites. The correlation data are based on a total of 96 samples from all sites regardless of zones Variables % Mud

Mean grain size (lm)

Sorting (lm)

% Water contents

% Organic contents

Salinity ppt

Air Temp (° C)

Sediment Temp (°C)

Total meiofauna

0.43**

−0.35**

−0.25**

0.45**

0.32**

−0.33**

−0.47**

−0.44**

0.05

Nematoda

38**

−0.19

−0.10

0.51**

0.35**

−0.27**

−0.38**

−0.35**

−0.08

Copepoda

0.15

−0.44**

−0.41**

−0.19

−0.29**

−0.27**

N/C ratio

0.14

0.13

0.15

0.45**

0.30**

−0.25**

−0.38**

−0.37**

Foraminifera

0.09

0.27**

0.34**

0.34**

0.24*

−0.03

0.07

0.08

Nauplii

0.35**

−0.35**

−0.26**

0.01

0.16

−0.06

−0.09

−0.10

−0.07

−0.09

pH

Eh (mv)

Dissolved O2 (mg/l)

0.24*

0.13

0.17

0.15

0.36**

0.17

−0.01

−0.49**

0.05

0.12

−0.59**

0.00

−0.02

0.30**

0.15

0.18 −0.04

Ostracoda

−0.04

0.15

0.12

−0.12

−0.12

−0.12

−0.45**

0.18

Turbellaria

−0.10

0.05

−0.01

−0.16

−0.08

−0.14

−0.20*

−0.20*

0.15

0.19*

Polychaeta

−0.13

0.06

−0.01

−0.05

−0.03

−0.14

−0.19*

−0.19*

−0.08

0.10

0.00

Polychaete larvae

−0.24*

0.09

0.00

−0.17

−0.07

−0.15

−0.12

−0.11

−0.03

0.09

−0.02

Acari

0.10

0.12

0.14

0.32**

0.23*

−0.10

−0.24*

−0.25**

−0.34**

0.05

0.17

Kinorhyncha

0.00

0.06

0.14

0.10

0.03

0.04

0.05

−0.22*

0.04

0.10

0.19*

0.22*

0.00

0.18

Source Khalil (2001) (*): signiﬁcant at P < 0.05, (**): signiﬁcant at P < 0.01

(Boggs 1987). In areas where mangroves were removed from the shore, most of the light mud particles in the sediment load transport to a further distance seaward. This was more obvious at the cleared site, where a huge difference in mud content was found between the low and high intertidal zones (Fig. 23.2). The sediment grain size greatly influences water and organic contents (Snelgrove and Butman 1994), which were generally reduced at the cleared and partially-cleared mangrove sites respectively.

Response of Meiofaunal Groups The different meiofaunal groups responded to the disturbance by mangrove deforestation in different patterns. As shown in Fig. 23.3, nematodes, copepods and Foraminifera occurred in all samples, but the percentage occurrence of Ostracoda, Acari and Kinorhyncha decreased at the two impacted sites, becoming lowest at the cleared mangrove site. Nauplii, Cladocera and Platyhelminthes showed an opposite trend. Some other groups became more frequent at the partially-cleared versus the non-cleared site, such as Oligochaeta, Cnidaria and Isopoda, which occurred at the partially-cleared site only (Fig. 23.3). In terms of densities, some groups, for example, Foraminifera showed a marked decrease, while copepods and nauplii increased in their abundances with the increasing impact. As the increase in the abundance of copepods and nauplii was considerably

more, the total meiofaunal abundance showed signiﬁcantly higher numbers at the partially-cleared site in summer, and the cleared site in the winter season (Fig. 23.4). Coull and Chandler (1992) reviewed pollution studies on meiofauna and concluded that there is no paradigm that evolves concerning meiofaunal densities and pollution. It appears that although the mangrove degradation induced reduction in densities of several meiofaunal groups at the impacted sites, a general increase in total meiofaunal density may occur, resulting from a disproportional increase in a certain few taxa. Considering the disturbance to the community structure, this would be considered as a shift rather than a promotion of the total density. Nematodes, the most dominant group at the three sites, showed little density variation in response to the deforestation impact, particularly in winter (Fig. 23.4). Indeed, in pollution studies, nematode density was generally held to be relatively insensitive to the impact (Heip 1980; Moore and Bett 1989). Therefore, the nematode abundance alone has not been a good indicator in impact assessment studies (Coull and Chandler 1992). However, Schratzberger and Warwick (1998) found that nematode abundance declined signiﬁcantly in response to food limitation in a microcosm experiment set to investigate physical disturbance. As shown in Fig. 23.4, nematode density here did not change signiﬁcantly at the impacted sites in the winter, but it decreased signiﬁcantly at the cleared site in summer. Given the reduced detritus food in the sediments (loss of the mangrove cover)

23

Meiofauna of the Red Sea Mangroves with Emphasis …

425

Fig. 23.2 Sediment characteristics in summer and winter seasons at sites with cleared, partially-cleared and non-cleared mangrove cover. A1, H1, S1 are high intertidal; A2, H2, S2 are mid-intertidal; A3, H3, S3 are low intertidal; A4, H4, S4 are subtidal stations at the different sites as shown. P values of ANOVA tests for variation between sites and zones (stations) are shown in small boxes inside the plots Source Khalil (2003)

and low water level during summer, less food amounts were available at the cleared site, which may contribute to the signiﬁcant decrease in the nematode density. Furthermore, strong positive correlations of the nematode abundance with the water and organic contents in sediments were reported (Table 23.3).

Copepods (the second dominant group) showed a consistent increase in abundance, with the increasing intensity of the impact (Fig. 23.4). In contrast to nematodes, copepods have been reported as being very sensitive to environmental impacts (Coulland Chandler 1992). In several studies, various factors were indicated that affect copepod abundance.

426

A. S. M. Khalil

Fig. 23.3 Occurrence (%) of meiofaunal groups in the samples collected from each of the cleared, the partially-cleared and the non-cleared mangrove sites in the Red Sea. N = 32 for each site Source Khalil (2000)

Hoffmann et al. (1984) and Dittmann (1993) proposed that predation by epibenthos may influence copepod numbers. Olafsson et al. (1993) found that competition for food with benthic bivalves was responsible for lowering copepod numbers in a microcosm experiment. Thus, the increased copepod abundance at the impacted mangrove sites could result from exclusion of the predatory epibenthos, while mangrove macrofauna were observed to be greatly reduced in numbers at the partially-cleared cleared sites. Furthermore, Fondo and Martens (1998) found higher densities of epifauna in a natural mangrove area than in deforested areas in Gazi Bay, Kenya. On the other hand, Netto et al. (1999) reported copepods as the dominant group at the windward stations of a topographically controlled front of Rocas Atoll (NE Brazil). Similarly, increased wind effects in shore areas with removed mangrove shelter may contribute to the copepod density increase. Copepods are usually reported as one of the most sensitive meiobenthic groups to decreased oxygen, and as such are generally restricted to toxic conditions (Coull and Chandler 1992). As shown by Fig. 23.3, several other groups had in general higher occurrence in the sediment samples from the partially-cleared site. This made the partially-cleared site appear to be richer in terms of numbers of taxonomic groups present than either the cleared or the non-cleared site. A better indication of a uniform change with increasing impact was shown by the nematode/copepod ratio (N/C). Influenced mainly by the increase in copepods, and slightly by the decrease in nematode abundance, the N/C ratio declined gradually at the partially-cleared and the cleared sites (Fig. 23.4). An increase in the N/C ratio was found to

be an indication of organic pollution in several studies (Parker 1975; Raffaelli and Mason 1981; Raffaelli 1987; Coulland Chandler 1992). Here, the decline in the N/C ratio correlates well with the decline in the sediment organic content, as a direct result of removing the mangrove cover from the habitat (Table 23.3). A strong negative correlation with the pH values may indicate that the N/C ratio is normally high in the mangrove sedimentary habitats not affected by the clearing disturbance.

Changes in the Meiofaunal Community Structure The contrasting responses of the different meiofaunal groups modiﬁed their relative abundance in the community at the degraded mangrove sites, as indicated by the Analysis of Similarities (ANOSIM) in Table 23.4. Changes observed at the two impacted mangrove sites from the non-cleared mangrove site were more pronounced for winter than for summer, as shown by classiﬁcation analyses based on the Bray Curtis Similarity of abundances of the meiofauna (Fig. 23.5). This may indicate that the communities at the impacted sites also became less resilient to the seasonal fluctuations. As shown by Table 23.4, both meiofaunal communities at higher taxonomic levels and nematode communities at species level varied signiﬁcantly among the sites and the zones (P = 0.001). The Global R for between sites tests and the R-values in the pairwise comparisons were higher for meiofaunal communities (part 1a of Table 23.4) than for

23

Meiofauna of the Red Sea Mangroves with Emphasis …

427

Fig. 23.4 Abundances of total meiofauna, major meiofaunal groups and nematode/copepod ratio (N/C) in sediment samples collected from cleared, partially-cleared and non-cleared mangrove sites. A1, H1, S1 are high intertidal; A2, H2, S2 are mid intertidal; A3, H3, S3 are low intertidal; A4, H4 and S4 are subtidal stations at the different sites. P values of ANOVA tests for variation between sites and zones (stations) are shown in small boxes inside the plots. Ns. = not signiﬁcant at P < 0.05 Source Khalil (2003)

nematode communities (part 2a of Table 23.4). These higher R-values were due to higher variability among sites for meiofaunal communities at the high- and the mid-intertidal levels. On the other hand, the Global R for between zones

tests was higher for nematode communities than for meiofaunal communities. Thus, the increased variability within the cleared and the partially-cleared sites was indicated more obviously by the nematode communities (part 2b of

PC versus CL

0.001

0.742

0.002

0.322 0.09 0.307 0.29

Low intertidal versus Subtidal

High- versus low intertidal

High intertidal versus Subtidal

Mid intertidal versus Subtidal

0.481

0.259

PC versus CL

0.459 0.415

High- versus low intertidal

High intertidal versus subtidal

Mid intertidal versus subtidal

Source Khalil (2001)

0.476 0.148

Low intertidal versus subtidal

0.002

0.002

0.143

0.004

0.271 0.784

0.054 −0.063

0.123

0.446

0.465

0.339

0.109

0.404

0.002

0.002

0.011

0.177

0.004

0.162

P

R

0.058

0.002

0.009

Partially-cleared site P

0.207

0.689

0.443

P

R

0.074

0.013

0.208

R

Mid intertidal

0.084

0.031

0.019

0.029

0.174

Non-cleared site

0.211

0.393

0.096

Mid- versus low-intertidal

0.001

0.001

0.001

P

High- versus mid-intertidal

(b) Within sites

0.275

R

NC versus CL

High intertidal

R

Between stations: Global R = 0.473, P = 0.001

Total site

NC versus PC

(a) Among sites

0.121

0.238

0.248

0.227

0.077

Between sites: Global R = 0.338, P = 0.001

0.007

0.002

0.134

0.006

0.574

−0.025

Mid- versus low-intertidal

P 0.409

R −0.001

0.451

(2) Nematode communities

0.001 0.041

R

P

0.574 0.17

P 0.044

Partially-cleared site

0.102

0.219

R

Mid intertidal

Non-cleared site

0.144

0.002

P

0.001

P 0.002

High- versus mid-intertidal

(b) Within sites

0.6

0.191

NC versus CL

0.375

R

0.001

R

0.302

High intertidal P

Between sites: Global R = 0.367, P = 0.001 Between stations: Global R = 0.372, P = 0.001

Total site

NC versus PC

(a) Among sites

(1) Meiofaunal communities

0.728

0.776

0.761

R

P

0.032

0.012

0.001

0.269

0.296

0.155

0.122

−0.035

0.05

R

0.322

0.383

0.381

0.109

0.356

0.422

R

Cleared site

0.002

0.002

0.002

P

Cleared site

Low intertidal

0.222

0.431

0.663

R

Low intertidal

0.659

0.841

0.331

R

Subtidal

0.555

0.888

0.421

R

Subtidal

P

0.039

0.015

0.013

0.173

0.013

0.004

P

0.009

0.008

0.063

0.097

0.574

0.25

0.002

0.002

0.022

P

0.002

0.001

0.001

P

Table 23.4 Results of ANOSIM tests (values of R statistics and signiﬁcance from permutation tests) for differences of: (1) meiofaunal community structure, and (2) nematode community structure between the non-cleared (NC), the partially-cleared (PC) and the cleared (CL) sites and their stations. The analysis was based on abundance data of meiofaunal groups (for meiofaunal communities) and nematode species (for nematode communities) in the samples. Data were square-root transformed prior to analysis

428 A. S. M. Khalil

23

Meiofauna of the Red Sea Mangroves with Emphasis …

429

Fig. 23.5 Cluster analysis based on similarities of the abundance of meiofaunal groups (above) and nematode species (below) in summer and winter from three mangrove sites. A1, A2, A3 and A4 are sampling stations at Site A (cleared mangrove) from high-, mid-, low intertidal and subtidal zones, respectively. Similarly, H1–H4 are sampling stations at Site H (partially cleared mangrove) and S1–S4 are sampling stations at Site S (non-cleared mangrove). For meiofaunal groups, each zone is represented by four samples in each of summer and winter denoted by a, b, c and d. For nematode species, each zone is represented by three samples in each of summer and winter denoted by a, b, and c. CL: Cleared, PC: Partially cleared, NC: Non-cleared site, Hint: High intertidal; Mint: Mid intertidal; Lint: Low intertidal; Subt: Subtidal

Table 23.4), which underwent more structurally signiﬁcant changes than the meiofaunal high taxon level along the intertidal-subtidal transect (part 1b of Table 23.4).

Response of the Nematode Species Investigations on nematode assemblages in mangrove sediments in different tropical areas tend to support the fact that there is no distinct nematode assemblage conﬁned to the mangrove areas, that is, no numerically dominant endemic species or any common dominant genera among mangrove forests (Decraemer and Coomans 1978; Hodda and Nicholas 1985, 1986; Alongi 1987b, c, 1990; Krishnamurthy et al.

1984; Nicholas et al. 1991; Olafsson 1995; Somerﬁeld et al. 1998). This was also true for nematodes found in the Red Sea mangroves of Sudan; however, the nematode species responded to the impact of mangrove degradation differently (Table 23.2). In pollution studies, reductions in species diversities are usually reported (see review by Coulland Chandler 1992). In a microcosm experiment, Schratzberger and Warwick (1998) demonstrated that the nematode diversity changed signiﬁcantly when subjected to a physical disturbance. Similarly, Austenet al. (1998) reported changes in nematode diversity caused by biological disturbance of macrofauna. In the Red Sea, signiﬁcant changes in the Shannon-Wiener diversity of nematode species as an effect of mangrove deforestation

430

A. S. M. Khalil

Fig. 23.6 Shannon-Wiener diversity (H´) index of nematode species in summer and winter samples. A1, H1, S1 are high intertidal; A2, H2, S2 are mid-intertidal; A3, H3, S3 are low intertidal; A4, H4, S4 are

subtidal stations at the different sites. ANOVA results testing variations between sites and stations are shown in boxes inside the plots Source Khalil (2001)

were indicated (Fig. 23.6). Changes in nematode species diversity were also indicated by the k-dominance curves for the three sites (Fig. 23.7). As shown by Table 23.4, using the meiofaunal higher taxal groups as an assessment tool proved to be also a good

indicator here. This may support the suggestion made by several authors (Heip et al. 1988; Herman and Heip 1988; Warwick 1988a, b; Moore and Bett 1989) that species data gave no greater reﬁnement in assessing pollution effects than did higher taxon-level diversity. However, investigation at nematode generic levels here offered better discrimination between sites, and they were more indicative for the increased variability within the impacted sites (Fig. 23.5 and Table 23.4). (i) Meiofaunal groups (ii) Nematode species

Fig. 23.7 k-dominance curves for nematode species abundance at the cleared, the partially-cleared and the non-cleared mangrove sites in summer and winter Source Khalil (2001)

Furthermore, the investigations at nematode species level provided a better discrimination to understand changes in composition of the trophic groups. As shown by Fig. 23.8, nematode assemblages at the non-cleared mangrove site were dominated by selective deposit feeders. This could be attributed to the muddier sediment of the mangroves. In general, there is a trend for the deposit feeders to dominate in ﬁner sediments (Wieser 1959; Hopper and Meyers 1967; Tietjen 1969). In Australian mangroves, deposit feeders usually outnumber other feeding guilds (e.g., Hodda and Nicholas 1986; Alongi 1987c). However, Olafsson (1995) and Schrijvers et al. (1997) found the epigrowth feeders to be the most frequent and abundant nematode genera in eastern African mangroves. This was attributed by Olafsson (1995) to the relatively sandier sediment found there, compared to that reported in Australian mangroves. This is also in accordance with the ﬁndings in the Red Sea mangroves, as the contribution of the epigrowth feeders relatively increased at higher intertidal levels where less mud contents in sediments were recorded. The selective deposit feeders, as a dominant group at the non-cleared site, were severely affected by mangrove deforestation. Their relative contribution was reduced at the partially-cleared site and they were almost excluded at the

23

Meiofauna of the Red Sea Mangroves with Emphasis …

431

Fig. 23.8 Distribution of nematode feeding types as a mean percentage of abundance in total samples for sites and their zones at cleared, partially-cleared and non-cleared mangrove sites at the Red Sea coast in Sudan Source Khalil (2001)

cleared site (Fig. 23.8). Looking into species composition of the selective deposit feeders, it is clear that their decline was mainly due to a decreasing abundance of Terschellingia sp. (Fig. 23.9). Relevant experimental studies reported similar trends for Terschellingia sp. Schratzberger and Warwick (1998) studied the effects of physical disturbance on nematodes in a mud microcosm and found that the main differences between control and treatments were due to decreases in the abundance of Terschellingia sp. In another microcosm study testing the effects of biological disturbance on nematodes, Austen et al. (1998) reported Terschellingiasp. as the only species with abundance decreasing in almost all treatments.

The high densities of selective deposit feeders or ‘microvores’ (Moens and Vincx 1997) at the non-cleared mangrove site could be attributed to rich microbial contents of the sediments enriched by the mangrove detritus. Their decrease at the impacted site is thus due to a decline in the food availability, resulting from the mangrove degradation. This may explain the graded response shown by selective deposit feeders that were influenced by the degree of mangrove degradation. On the other hand, the non-selective deposit feeders displayed an opposite trend (Fig. 23.8), increasing in relative abundance at the impacted site. This may indicate that the non-selective feeding on a wide range basis proved to be more energetically favourable where

432

A. S. M. Khalil

Fig. 23.9 Relative abundance (%) of nematode genera contributing to nematode feeding types at the cleared, the partially-cleared and the non-cleared sites. Abundance data is based on a total of 72 samples.

Others(1)* include Actarjania, Diplolaimella and Steineria; Others(2)* include Gomphionema, Paracanthonchus, Prochromadorella, Ethmolaimus and Laimella

mangroves were lost and organic contents became low in sediments. It has been explained by some studies that non-selective deposit feeders, such as Monhystera, exhibit

continuous pumping activity of the pharynx and the food intake is purely passive. In addition, the non-selective deposit feeders presumably feed on a wide spectrum of food,

23

Meiofauna of the Red Sea Mangroves with Emphasis …

which may include bacteria, non-living aggregates, small flagellates etc., although the particle size of the food is restricted (Heip et al. 1985). The selective deposit feeders follow another strategy. They presumably pick up small food particles, such as bacteria, selectively (Wieser 1953), and they have well-developed sense organs and pumping of the pharynx is not continuous (Heip et al. 1985). In conditions where less organic/detritus contents were available in sediments at the impacted mangrove sites, active predation is perhaps also a more efﬁcient feeding strategy. This may explain the increase in the proportion of predators/omnivores at the cleared site and the partially-cleared site. However, these changes did not have such clear patterns as that shown by the deposit feeders (Fig. 23.8). Although non-selective deposit feeders dominated the nematode assemblage at the cleared site (Fig. 23.8), they were represented there by relatively fewer species (Fig. 23.9). Thus, the increase in numbers was due to the increased abundances of certain species, mainly Daptonema sp. Indeed, the species composition and relative abundance within the different feeding types differed markedly among the sites. This may reflect the range of the food spectra or ecological niches available. At the partially-cleared site the patchy distribution of the mangrove vegetation had perhaps created a patchier habitat than the non-cleared site with more intact and uniform mangroves. Left with a barren mud flat, the cleared mangrove site would support less habitat heterogeneity than either of the partially-cleared or the non-cleared sites. Consequently, species richness within the different feeding types, and the nematode diversity in general were highest at the partially-cleared site, followed by the non-cleared and lowest at the cleared site (Figs. 23.6 and 23.7).

The Nature and Indications of the Meiofaunal Response The meiofaunal response to disturbance from mangrove deforestation suggests that it ﬁts the predictions of the intermediate disturbance hypothesis (Connell 1978; Death and Winterbourn 1995), with peak meiofaunal diversity at intermediate levels of disturbance. This is based on the assumption that meiofaunal communities at the partially-cleared site are subjected to an intermediate intensity of the stress by mangrove clearing. The peak nematode diversity occurred at this site as indicated by the diversity index and k-dominance curves (see Figs. 23.6 and 23.7). The meiofaunal composition at higher taxonomic levels was also relatively richer at the partially-cleared site (see Fig. 23.3).

433

Fitting the intermediate disturbance hypothesis here is not surprising. In other studies, such a pattern of the meiofaunal response was demonstrated experimentally with various kinds of disturbance. Austen et al. (1998) reported a similar trend for a nematode community in response to biological disturbance in a microcosm experiment. Schratzberger and Warwick (1998) found that the response of nematodes in a mud microcosm subjected to spasmodic physical disturbance followed a pattern which was commensurate with the intermediate disturbance hypothesis. There are many examples of this pattern occurring in nature as well (Huston 1994). However, this should not be taken as a positive impact. Austen et al. (1998) demonstrated that the presence of patches by disturbance may create a heterogeneous mosaic of communities with enhanced regional meiofaunal diversity; however, disturbances appear to affect species composition differentially and hence probably also the functional properties of the community. Indeed, variability in meiofaunal community structure between tidal zones within the impacted mangrove sites was generally increased (see Figs. 23.4, 23.5 and Table 23.4). Schratzberger and Warwick (1998) provided experimental evidence supporting the contention by Warwick and Clarke (1993) that this variability is a symptom of community stress. The clearance disturbance resulted in the measured changes in the community structure. These changes, which were linked with habitat modiﬁcation, indicated a gradual shifting from the typical mangrove meiofaunal composition. Using nematodes as an example, the main change was a dramatic decline in selective deposit feeders, which reflects the decline in the ready availability of the microbial and organic food in the rich undisturbed mangrove sediments. Thus, the functional properties of the community were modiﬁed at the deforested areas, although nematode diversity was enhanced at the partially-deforested site. The overall feature of the change at the deforested sites was a shifting of ecosystem propertieswith consequent changes in the meiofauna, indicating deterioration in the efﬁciency of the ecosystem function as a nursery ground for marine organisms, which represents one of the vital services provided by the mangrove ecosystem. This conclusion is based on the assumption that the species composition is representative of community function (Austen et al. 1998), which partly reflects the whole ecosystem function. Seasonal variability in sediment characteristics and meiofaunal communities were also shown to be exaggerated at the cleared and partially cleared mangrove sites, which indicated the role of the mangrove cover in strengthening resilience of both abiotic and biotic components of the ecosystem to withstand seasonal and long-term changes.

434

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Morphology and Anatomy of the Pearl Oyster, Pinctada margaritifera in the Red Sea: A Case Study from Dungonab Bay, Sudan

24

Dirar Nasr

Abstract

The black-lip-mother of pearl oyster Pinctada margaritifera has special economic value in Dungonab Bay (Sudan). It has been cultivated in the area for a long time as it has the advantage of having a deﬁnite spawning season starting at the end of June and continuing throughout July and August. Morphological and anatomical studies of this oyster are given in this piece of work including description of external feature of the shells and internal organs such as the mantle, the gills, digestive system, circulatory system, nervous system, excretory system and the reproductive organs. Morphological and anatomical differences between P. margaritifera on one hand and both the European oyster, Ostrea edulis, and the American oyster, Crassostrea gigas, are presented. These differences included the presence of a long hinge on one side of the umbo in P. margaritifera an its absence in both O. edulis and C. virginica; both valves in P. margaritifera are moderately convex and neither of them can be easily distinguished, unlike O. edulis, and C. gigas; the mantles have free edges in P. margaritifera and the omission of pedal ganglia in both C. gigas and O. edulis due to the absence of a foot in these two species. Keywords

Teaching

Research

Project management

Introduction The history of the pearl oyster, Pinctada margaritifera in Sudan goes back to 1904 when the late Dr. Cyril Crossland studied some of its biological aspects in Dungonab Bay (Red Sea) and proved that it could be cultivated on a commercial D. Nasr (&) Red Sea University, Port Sudan, Sudan e-mail: [email protected]

scale. The black lip mother-of-pearl oyster, Pinctada margaritifera (Linnaeus) is found almost everywhere in the Red Sea, but they are especially abundant in Dungonab Bay. Its spat used to be collected on large rafts known as “spat collectors” where they settle soon after the spawning season (July–August). These spats were kept for one year in nursery trays at Umm El Sheikh Island and then transferred to growing trays at the Dungonab village site. Various aspects of oyster biology have been described by several authors such as the description of morphology and anatomy of Ostrea edulis; the morphology, anatomy and physiology of Crassostrea virginica, in addition to general descriptions of pearl oysters. However, rather more detailed morphological and anatomical studies of Pinctada margaritifera are given in this piece of work. The majority of dissections for studying the internal organs of P. margaritifera were done by breaking the ligament and then cutting the adductor muscle; the nervous system, however, was traced by treating preserved specimens with potassium hydroxide, glacial acetic acid, glycerol, chloral hydrate and acid haematoxylin. Among the major ﬁndings of studying P. margaritifera, morphologically, are that the shell of this species was found to be obtuse and that the growth at either side of the umbo is asymmetrical resulting in a long hinge on one side of the umbo; a condition that plays an important role in orienting P. margaritifera. Both valves in this species are moderately convex and neither of them can be easily distinguished unlike Ostrea edulis, and Crassostrea gigas where the left valve is easily distinguishable being deeper and more convex while the right valve is flat in the former and less convex in the latter. Internally the adductor muscle in P. margaritifera is very large compared to that of O. edulis and C. gigas. Similarly, unlike the O. edulis and C. gigas, the mantles have free edges. The nervous system in P. margaritifera consists of a pair of visceral ganglia, and cerebral ganglia in addition to pedal ganglia; the latter ganglia are missing in both C. gigas and O. edulis due to the absence of a foot in these species.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_24

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The sexes are separate in P. margaritifera, but there are no external features that indicate the type of sex in this species. However, the male and female gonads can be distinguished by the appearance of a portion of the gonad dropped in seawater: the male gonad appears as a milky substance while the female one appears as white and very tiny granules suspended in the water. The spawning period of P. margaritifera in the Sudanese Red Sea starts at the end of June and continues throughout July and August. Such a deﬁnite spawning season is one of the advantages in cultivating P. margaritifera on a commercial scale.

D. Nasr

then injected with warm jelly stained with methylene blue (since other injection materials such as latex, for instance, were not available). The majority of dissections, however, were done without narcotization by breaking the ligament with a screwdriver and then cutting the adductor muscle joining the right valve. The nervous system was traced by treating preserved specimens with potassium hydroxide, glacial acetic acid, glycerol, chloral hydrate and acid haematoxylin as will be shown later.

Morphology and General Anatomy Materials and Methods

The Shell

Specimens for morphological, and anatomical studies were taken from the growing trays at the Dungonab village site (Fig. 24.1). Some of these were dissected as described by Galtsoff (1964), where they were cleaned from fouling and narcotized by magnesium sulphate (Espom salt) for 24 h. For visceral and blood vessel examination, the narcotized specimens were placed in 5% formalin solution for 24 h and

The shell of P. margaritifera is solid, with slightly brittle newly grown parts at its periphery which are known as growth processes (Fig. 24.2). The growth processes are always damaged by corrosion and handling. The shape of the shell is almost circular. In his description of pearl-shells, Hynd (1954) introduced the term “reference axis” which is an imaginary curved line following the growth processes in

Fig. 24.1 Map of Dungonab Bay (after PERSGA/GEF 2004)

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Morphology and Anatomy of the Pearl Oyster …

439

Fig. 24.2 External view of the right shell of P. margaritifera with a photograph of the shell

the mid portion on the external surface of the shell from the umbo (oldest part of the shell) to the ventral border. He used the magnitude of the angle between the tangent to this curve at its distal end and the hinge line to determine whether the shell is oblique, erect or obtuse. If the angle is about 90˚, the shell is erect, if it is less than 90 it is oblique and if it is greater than 90˚, it is obtuse. Accordingly, all examined P. margaritifera specimens in Dungonab Bay were found to be of obtuse shell. The colour of the shell is greenish grey, being ornamented with whitish radial lines that represent the base of the growth processes. It is circular with irregular rings showing growth increments (Fig. 24.2). The two valves are inequilateral, that is the growth at either side of the umbo is asymmetrical. This condition results in a long hinge on one side of the umbo (Fig. 24.2). The hinge plays an important role in orienting P. margaritifera; the hinge side of the oyster being the dorsal side and the opposite side being the ventral border. The part of the hinge away from the umbo represents the posterior region of the oyster and the opposite side being the anterior border. If the bivalve is held in such a way as to have the umbo facing you and the long hinge is kept on the right hand side then the upper valve is the right valve and the lower one is the left valve (Fig. 24.3). The hinge contains a tough, dark brown elastic cord, the ligament (Fig. 24.3). In P. margaritifera the ligament is internal (ventral to the hinge), but the older part of it can be

Fig. 24.3 Internal view of the right valve of P. margaritifera with a photograph of the shell

seen externally just behind the umbo, while the younger part is hidden between the two valves. In the European flat oysters, Ostrea edulis, and the Paciﬁc oyster, Crassostrea gigas, the left valve (on which the oyster rests) is easily distinguishable being deeper and more convex while the right valve is flat in the former and less convex in the latter. In P. margaritifera, both valves are moderately convex and neither of them can be easily distinguished. The inner side of the shell shows various features. The byssal groove lies on the right valve at the end of the hinge just in front of the umbo through which byssal threads, by which the oyster attaches itself to a substratum, protrude (Fig. 24.3). The triangular portion of the shell lying dorsal and anterior to the byssal groove is known as the anterior ear. It is well deﬁned in the right valve by the byssal notch but ill-deﬁned in the left valve. The posterior ear is absent altogether in this species. There are no interlocking teeth along the hinge line as found in many bivalves, but, instead, there are small pits in both valves which widen in the mid-hinge line just behind the umbo supporting the ligament (Fig. 24.3). The muscle scar or the impressions that mark the attachment of muscles are quite visible on the inner side of each valve. The most conspicuous is the single (posterior) adductor muscle situated in the third posterior region of the shell. It is ovoid in shape although the shell is almost rounded. Other scars are those of the retractor, anterior and posterior levator and the

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D. Nasr

Fig. 24.4 General anatomy of P. margaritifera on the removal of the right valve, right mantle and right gill

pallial muscles (Fig. 24.3). The adductor muscle has the function of closing the two valves, however, the valves do open by the elasticity of the ligament. In P. margaritifera the adductor muscle is very large compared to that of O. edulis and C. gigas (Fig. 24.3). It is comma-shaped with rounded portion lying in the centre of the valve and a narrow concave portion pointing dorsally adhering to the rectum. The adductor muscle with its two portions are surrounded by the pericardium, the visceral mass, and the inhalent and exhalent chambers. It represents the posterior adductor muscle; the anterior one—found in other bivalves—is lost during metamorphosis after settlement of larvae (Galtsoff 1964). As in other oysters, it is composed of two portions quite visible to the naked eye, a posterior narrow white portion and a larger thick anterior portion that is semi-translucent. In a cross-section the former is found to be darkly stained in comparison with the latter striated muscle. It is well known that bivalve shell is composed of the three main layers common in most molluscan shells, a thin outer layer (periostracum), a middle prismatic layer and an inner nacreous layer. In P. margaritifera, these layers are quite distinct when the shell is transversely sawed. The thickness of the horny periostracum and the lustrous nacreous layers decrease going dorsally, towards the umbo and increase ventrally away from it. The middle prismatic layer shows the opposite tendency.

adductor muscle. This was achieved by the use of a screwdriver, and by narcotizing the animal with Epsom salt as described earlier. (i) The Mantle: After removal of the right valve, the animal is covered by the mantle lobes except in the region of the adductor muscle which is inserted directly into the shell (Fig. 24.4). The right and left mantles enclose the mantle cavity which contains all body organs. Both mantles are fused together in the region lying along the hinge covering the mouth, but, unlike the European oyster, O. edulis and the Paciﬁc oyster C. gigas, the mantles have free edges which are clearly shown in preserved specimens. In the aquarium, however, the two mantles always adhere together at the ventral side gaping at the anterior and posterior borders, thus forming the inhalant and exhalent openings respectively (Fig. 24.5).

The Body To investigate the soft parts of the oyster, the upper right valve was removed by breaking the ligament and cutting the

Fig. 24.5 P. margaritifera pumping seawater in the aquarium; the two mantles are separated in the mid-posterior region forming the exhalent opening

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Morphology and Anatomy of the Pearl Oyster …

Both mantles are attached to the visceral mass, the labial palps, the pericardium and the adductor and retractor muscles. The attachment with the gills starts at the level of the retractor muscle and proceeds dorsally. Ventral to the retractor muscle there is no actual fusion with the bases of the gills as in O. edulis and C. gigas, although the gills always adhere to the mantles in a special depression along the gill bases. The free edge of the mantles varies in colour from light brown to black in the same species living in the same area. Parts of the mantle are highly muscular and very much thickened, but they become thinner as they approach the visceral mass in the dorsal side. The colour of the surface of the mantle is white or creamy in the region covering the visceral mass when the oyster is healthy and fatty, but in weak and lean specimens of P. margaritifera the colour of the mantle may be transparent at the region of the visceral mass with its radial muscles quite visible. These radial muscles play an important role in pulling in the entire mantle. As in other oysters, the mantle edge is composed of three folds (Fig. 24.6). The outer fold adhering to the surface of the shell is thin and whitish in colour; its function is the secretion of the outer horny layer of the shell—the periostracum. The process of secretion was experimentally observed when shell repair of P. marqaritifera was carried out in the labratory. The middle fold is thicker than the outer fold with tentacles that gradually dorsally decreas in size. These tentacles take the function of sense organs, being sensitive to changes in light intensity, touch, vibrations or chemical additions to the surrounding water. The reaction of the pearl oyster to these changes in environment was observed in the aquarium as well as out of the water when the oysters are gaping exposing the mantle edge. The innermost fold is the thickest of the three folds with heavy pigmentation and powerful muscles and tentacles. The tentacles of the two mantle lobes interlocking with each other forming the mantle cavity, thus controlling the water flow. This fold is mobile and in live oysters, it is curved inward making a right angle with the surface of the shell. Microscopic studies of the mantles show that they are covered with

Fig. 24.6 Transverse section of the edge of the mantle of P. margaritifera with a photomicrograph

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a layer of epithelial cells on both sides. The thin connective tissue contains some blood sinuses with the circum-pallial artery and circum-pallial nerve being quite visible. Longitudinal muscle ﬁbers run parallel to the outlines of the mantle edge (Fig. 24.6). (ii) The gills: The gills of P. margaritifera are light brown in colour and comparatively large, occupying two thirds of the mantle cavity. They extend from the labial palps at the mouth region in the anterior part of the body to the anus at the posterior region. Each gill has a gill axis from which hang up two plates or demibranchs. The demibranch consist of a number of gill ﬁlaments or lamellae attached to each other by lateral interlocking cilia which can be seen with the aid of a microscope (Fig. 24.7a). Each demibranch consists of an outer descending and an inner ascending lamella. Thus the lamellae of both demibranchs, as expressed by Yonge (1960) and Fougerouse et al. (2008), are arranged in the form of a W, with the gill axis found in the median apex of the W. This can be seen in a transverse section made perpendicular to the gill axis (Fig. 24.7b). The lamellae of the outer and inner demibranchs of each gill is joined together by septa or intercellular junctions forming the so-called water tubes (Fig. 24.7b). The free edge of each demibranch includes a ciliated groove running along the entire length of the gill known as the terminal groove. Food particles collected by the gill surface are entangled by mucus and pass along this groove and along the base of the gill to the labial palps and to the mouth (Orton 1937; Yonge 1960; Galtsoff 1964). In a transverse section across the gill lamellae the ﬁlaments are found to be arranged in series of folds or plicae (Fig. 24.7b). The ﬁlaments in each plica vary in size and structure; the largest, lying in the bottom of the groove between two adjacent folds, is known as the principal ﬁlament. It is triangular in shape, supported by chitinous rods and surrounded on each side by a transitional ﬁlament which has a size intermediate between that of the principal ﬁlament and that of ordinary ﬁlaments. The latter are united together at their base by interﬁlamentous junctions. The single ordinary ﬁlament shows the following features (Fig. 24.7b): the presence of short cilia at its tip known as

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Fig. 24.7 a Transverse section of the gill of P. margaritifera showing an ordinary ﬁlament at the bottom right corner of the diagram. A photomicrograph of the section is shown on the left. b The lamellae of a demibranch arranged in the form of a W

frontal cilia, and comparatively longer ones on both sides are known as lateral cilia. Mucus glands are found in the epithelium lining the frontal region of the ﬁlament. Attachment of the gills to other organs varies in different regions of the body. The outer demibranch on each side is fused with the mantle up to the level of the retractor muscle. In the region of the labial palps each gill is attached to the visceral mass at the bases of the palps. At the same time the

Fig. 24.8 Transverse section across the points A-A, B-B and C-C in P. margaritifera showing the chambers at the base of the gills

septum attaches the mantle to the visceral mass before its fusion with the latter. This situation results in two chambers above each gill known as epibranchial chambers (Fig. 24.8). At the level of the retractor muscle, the septum that attaches the mantle to the visceral mass is lost, but the attachment of the gill with the visceral mass and the retractor muscle on one side and with the mantle on the other side persists. This condition results in one epibranchial chamber above each

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Morphology and Anatomy of the Pearl Oyster …

gill (Fig. 24.8). Just ventral to the retractor muscle, the attachment of the gills to the surrounding organs is lost with the exception of the adductor muscle to which it is attached by means of the pyloric process (Fig. 24.8). In preserved specimens, the two inner demibranchs can be easily separated unlike those of O. edulis and C. gigas. However, in the aquarium when the two valves are forced apart, the two inner demibranchs adhere to each other in the same way the outer demibranchs adhere to mantles, thus forming the common epibranchial chamber (Fig. 24.9). This interesting and peculiar sort of adhesion was explained by Herdman (1904): the line along which both gills and mantle lobes adhere to each other is covered with short stiff cilia that interlock to form a very effective ciliated junction. (iii) The digestive system: The organs concerned with collection and digestion of food in oysters comprise the mouth, the gills, labial palps, oesophagus, stomach, intestine and rectum, besides the crystalline style and the digestive diverticula. The digestive tract was studied by injecting warm jelly stained with methylene blue as described earlier. It begins with the mouth which is hidden under two projecting lips on the dorsal side at the umbo and is surrounded by the right and left pairs of the labial palps (Fig. 24.9). Anterior to the mouth lies the mobile muscular foot which plays some role in removing foreign and non-desirable particles that might accumulate in the palps, gills or mouth. The labial palps which serve as a food sorting apparatus are triangular in shape, each pair having an outer smooth surface and an inner folded one. The latter encloses a groove that leads to the mouth. Food particles which are sorted out by the labial palps enter the mouth and pass through the dorso-ventrally compressed esophagus which is very short compared to that of O. edulis (Fig. 24.9). The oesophagus leads to the stomach which is an ovoid irregular sac with its long axis lying almost at an acute angle to the hinge line.

Fig. 24.9 Digestive system of P. margaritifera

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Several small projections arise externally from the stomach wall with a conspicuous constriction in the anterior third part (or section) of the stomach dividing it into a smaller anterior and a larger posterior pouch. On other hand, the internal of the stomach wall is covered by an irregular shaped structure at the entrance to the crystalline style sac and the intestine. It is formed of two portions connected together by a narrow middle piece known as the gastric shield. The stomach is surrounded by the dark green digestive diverticula; it does not occupy a central position as in O. edulis or C. gigas, but lies in the posterio-dorsal part of P. margaritifera (Fig. 24.9). The digestive diverticula communicate with the stomach through numerous ductules joining each other to form major ducts. Two of these ducts open in the stomach laterally from the anterior and posterior sides, while a third one opens in the stomach ventrally from the posterior side. The function of the digestive diverticula is assimilation and digestion which take place in their cells (Yonge 1926b). The stomach is connected to the style through a funnel-shaped opening in the postero-ventral side; the latter after leaving the stomach proceeds ventrally, but slightly to the posterior region of the animal, and passes between the two converging bundles of the retractor muscles. At this point, it bends anteriorly in an obtuse angle and ends at the antero-ventral corner of the visceral mass (Fig. 24.10). On dissecting the crystalline style sac of a fresh specimen, it is found to be ﬁlled with a clear gelatinous rod, the crystalline style, having a bulging head that projects into the stomach and a tapering end that extends to the distal part of the sac, but on dissection of many specimens after being removed for 2 h from the water the crystalline style was not found. Thus, during unfavourable conditions, the crystalline style disappears or dissolves and in actively feeding bivalves, however, it rotates by the ciliary action of sac epithelium (Nelson 1918; Yonge 1926a). The gastric shield provides a base for

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Fig. 24.10 Transverse section of the style sac and the descending intestine in P. margaritifera. A photomicrograph of the section is shown on the bottom

grinding of food by the rotating head of the crystalline style (Galtsoff 1964). The intestine leaves the stomach at the same opening of the crystalline style sac and follows the course of the latter along its entire length. They are connected with each other through a narrow slit except in a very small portion at the distal end where the two structures are completely separated. This slit is formed by the development of two longitudinal folds in the wall of the style sac, one from the anterior side and the other from the posterior side; the two folds make dividing lines between the larger cylindrical left chamber, the crystalline style sac, and the smaller irregular right chamber, the descending limb of the intestine (Fig. 24.10). The latter makes a U-shaped curve to the left at the antero-ventral corner of the visceral mass and proceeds as the ascending limb of the intestine. Both limbs of the intestine intersect at the posterior extremity of the ventral surface of the visceral mass. Just beyond the point of intersection, the ascending intestine turns sharply in a dorsal direction running parallel to the adjacent descending intestine. At the level of the stomach, it curves posteriorly passing dorsal to the heart and adheres to the adductor muscle on the posterior side; from this point it proceeds as the rectum. The rectum opens in the exhalent chamber through the anus; the latter is surrounded by a leaf-like organ known as the anal funnel (Fig. 24.9). One of the major anatomical differences between P. margaritifera, on one hand, and O. edulis and C. gigas, on the other hand, is that in the latter two species the comparatively long intestine does not lead directly to the rectum as in P. margaritifera, but it

makes a loop around the visceral mass before ending in the rectum. The folds of the inner surface of the labial palps consist of connective tissue covered on both sides by ciliated epithelial cells which differ in size within the same fold (Fig. 24.11). The folds themselves decrease in size as they approach the entrance of the mouth. Unlike the inner surfaces the smooth outer surface has a narrow layer of epithelial cells which are almost cubical in appearance with very short cilia. The epithelium lining the groove between the two folded surfaces of the labial palps continues to the mouth and oesophagus without change in appearance. In the stomach, however, the ciliated epithelial cells cover the entire inner wall except for the portion lying under the gastric shield which is not ciliated (Fig. 24.12). The ciliated cells are narrow and characterized by a well-developed border and comparatively longer cilia; partially digested food matter is quite abundant in the lumen. The digestive diverticula communicate with the stomach through tubules that unite to form large ducts. In cross-section, the tubule looks round with a characteristic cross-shaped lumen (Fig. 24.13). The cells surrounding the lumen have large nuclei. At the four corners of the “cross” there are patches of darkly stained protoplasm with compact nuclei. The ducts, on the other hand, have lumen of irregular shape, but unlike the tubules, they have ciliated cells lining their lumens (Fig. 24.13). (iv) The circulatory system: Like other bivalves, P. margaritifera has an open circulatory system where the

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Morphology and Anatomy of the Pearl Oyster …

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Fig. 24.11 Transverse section through the inner (folded) surface of the labial palps in P. margaritifera. A photomicrograph of the section is shown on the right

Fig. 24.12 Transverse section through the stomach wall showing the gastric shield in P. margaritifera

Fig. 24.13 Transverse section of a typical tubule (left) and a typical large duct (right) of digestive divertica in P. margaritifera

arteries are not connected to the veins due to the presence of blood sinuses which act as capillaries. The blood is colourless and contains two types of cells, hyaline cells and granular cells. Injection of the arterial system by stained warm jelly through the ventricle gave partial success; this was, however, followed by dissection and observation of

minor arteries with the aid of a magnifying lens. While, the injection of the venous system through the auricles was failed due to the fact that these vessels have very thin walls which cannot support an increase in pressure, the best way to trace the major veins was to cut off the posterior third of the gills in preserved specimens and to inject the visible afferent

446

and efferent veins with very dilute Jelly stained with neutral red. The injection was supported by gently rubbing the vein’s walls and following their courses under a magnifying lens. The heart: The most conspicuous part of the circulatory system in P. margaritifera is the heart which is enclosed within a thin-walled sac, the pericardium, and is surrounded interiorly by the visceral mass and posterior by the adductor muscle (Fig. 24.14a). On its dorsal side it is fused with the ventral part of the rectum and on its ventral side it is bounded by the renal organs with which it communicates through a pair of reno-pericardial canals as will be shown later. The wall of the pericardium consists of connective tissue and many blood sinuses; its epithelium surface is rich in mucus cells (Fig. 24.14b), and its cavity is always ﬁlled with a fluid that bathes the heart. When it is not pumping, the heart is seen lying in the anterior half of the pericardial cavity, being very close to the ascending intestine, while when it is pumping it almost ﬁlls the cavity. It consists of Fig. 24.14 a Diagram of the main arterial system of P. margaritifera. b Transverse section of the pericardium wall of P. margaritifera. A photomicrograph of the section is shown on the left

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three chambers, a dorsal dirty white spongy ventricle and two ventral delicate auricles which vary in colour from light brown to black in the same species. The right and left auricles join the respective common efferent veins on both sides, while the common base of the two auricles is connected ventrally to the pericardial wall and the internephridial passing by a thin and very tough connective tissue. Dorsally, both auricles communicate with the ventricle separately. The dorsal part of the latter is completely fused with the ventral part of the rectum (Fig. 24.14a). The walls of the auricles and that of the ventricle vary greatly in transverse section; the latter is muscular, the muscle ﬁbers crossing one another in various directions with blood cells scattered in the spaces between the ﬁbers. The auricles, on the other hand, are slightly muscular. The blood flowing from the auricles to the ventricle is controlled by the auriculo-ventricular valve seen in section as projecting muscle ﬁbers.

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Morphology and Anatomy of the Pearl Oyster …

The arteries: The ventricle pumps the blood into the anterior and posterior aortas. The former is comparatively larger and passes dorsally under the rectum to bend slightly towards the anterior side and proceeds parallel to the hinge line (Fig. 24.14a). It forms a large ventral branch, the visceral artery after crossing the rectum. This branch supplies blood to the organs of the visceral mass and gives a smaller branch, the reno-gonadial artery to the gonads and the kidneys, and anterior to the visceral artery three small branches, the gastric arteries, leave the anterior aorta and supply the blood to the digestive diverticula. The cephalic artery supplies the anterior part of the body with a small branch, the labial artery, reaching the labial palps. It was noticed that all these branches leave the anterior aorta on both sides except the visceral artery which is an unpaired artery. In the region of the mouth the anterior aorta branches into two; each branch runs along the periphery of each mantle. These are the circumpallial arteries supplying the mantles (Fig. 24.14a). The posterior aorta on the other hand runs parallel to the rectum, but before reaching the anus it changes its direction and penetrates the adductor muscle and bifurcate into two branches inside the adductor muscle; one branch goes to the right and the other to the left; before reaching the point of insertion of the muscle in the shells both branches bend posteriorly and emerge from the adductor muscle in the region of the anus; they run across the mantles to the point of attachment of the two mantles, together forming the exhalent chamber (Fig. 24.14a). At this point they join the circumpallial arteries of the right and left sides. The two arteries emerging from the adductor muscle are the right and left posterior pallial arteries. Thus the posterior aorta supplies blood to the rectum, to the adductor muscle and to the two mantles. The veins: The most conspicuous veins that could be traced successfully are the common efferent veins, the branchial efferent veins, and the efferent veins and the small

Fig. 24.15 Diagram showing the major veins in P. margaritifera

447

transverse branches joining the branchial efferent veins from the gill ﬁlaments (Fig. 24.15). Other branches that carry deoxygenated blood from sinuses in various organs of the body to the afferent veins could not be traced successfully. The afferent vein runs along the gill axis where the two descending lamellae are fused together (Fig. 24.15). It carries deoxygenated blood from the body organs to the gill ﬁlaments. The branchial efferent vein is comparatively large and also runs along the gill axis adjacent to the afferent vein and parallel to the branchial nerve (Fig. 24.15). Small branches join the branchial efferent vein from the gill ﬁlaments. In a transverse section perpendicular to the gill axis the above mentioned veins are seen as two openings one lying on top of the other in the gill axis (Fig. 24.15). The branchial efferent vein that carries oxygenated blood from the gills communicates with the common efferent vein which empties into the respective auricle. (v) Nervous system: The nervous system in P. margaritifera is comparatively simple and consists of a pair of visceral ganglia, and cerebral ganglia in addition to pedal ganglia; the latter ganglia are missing in Crassostrea and Ostrea genera due to the absence of a foot in them. Nerves spread from these ganglia to various organs of the body. Very large and lean specimens were chosen for the study of the nervous system in P. margaritifera. Large nerves were quite visible in specimens preserved in 5% formalin as they have a whitish colour in contrast to the grayish colour of the specimens. Some specimens, however, were immersed in 10% nitric acid for several days and then cleared in glycerol to show the light brown nerves stained by the acid. Some were preserved in 5% formalin and treated with an aqueous solution of calcium hydroxide, glacial acetic acid, glycerol, chloral hydrate and acid haematoxylin. The latter two methods were suggested by Galtsoff (1964). These methods

448

were supplemented by dissection and observation under a magnifying lens beside microscopic examination. The large and conspicuous ganglia are the visceral ganglia found attached to the antero-ventral side of the adductor muscle at the pyloric processes which join the gills to the former. The two ganglia are united by a single and comparatively thick transverse visceral commissure. Nerves arising from the left ganglion are shown in Fig. 24.16 in which the right mantle, gill, and part of the visceral mass have been removed to expose the nerves. The posterior pallial nerve emerges from the visceral ganglion and runs along the ventral side of the adductor muscle before penetrating the mantle at the level of the anus on the posterior side. The anterior pallial nerve branches immediately after leaving the adductor muscle; these branches innervate the anterior region of the mantle. The branchial nerve runs dorsally for a very short distance, bends sharply to the ventral direction and runs along the gill axis, being parallel to the efferent vein (Fig. 24.16). The adductor muscle nerve arises from the dorsal side of the ganglion and runs dorsally along the adductor muscle. The root of the cerebro-visceral connective is found between the branchial nerve and the adductor muscle nerve and could be traced until it disappears in the visceral mass where dissection becomes necessary. It is very long, connecting the visceral ganglion with the cerebral ganglion on both sides. The latter ganglion is found by the side of the oesophagus with a small nerve, the cerebral commissure, passing over the oesophagus and linking the cerebral ganglia of both sides together. The pedal ganglia are found at the base of the foot; the two ganglia are joined together and they look almost as one ganglion. The cerebral and pedal ganglia are linked by the cerebro-pedal connective on both sides. Nerves spread from the pedal ganglia to innervate the foot and the byssal gland where byssal threads emerge from the body (Fig. 24.16). The nerve found along the periphery of the mantle is the circumpallial nerve arising Fig. 24.16 Diagram showing the nervous system of P. margaritifera. The right mantle and the right gill are removed. The left gill is pulled dorsally to expose the nerves below

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from the cerebral ganglion; it could not be traced as it is a very thin nerve. (vi) Excretory system: The excretory organs in the pearl oyster P. margaritifera consists of a pair of nephridia found on the surface of the visceral mass on both sides. Both nephridia communicate with each other through a transverse canal, the internephridial passage, which passes along the ventral side of the common base of the two auricles (Fig. 24.17a). The two organs are triangular in shape; the anterior base of this triangle lies along the gill base from the level of the pyloric process to the point of junction of the gill to the labial palp and the visceral mass in the dorsal side of the animal. This part of the nephridium consists of a glandular convoluted tube having a faint brownish colour which is quite distinguishable on the surface epithelium. The tapering posterior part of each nephridium extends across the body and joins the other organ on the other side through the narrow internephridial passage (Fig. 24.17a). The central portion of the nephridium consists of a lumen forming a reservoir for the storage of urine. The pericardium communicates with the nephridium through the thin-walled reno-pericardial canal which is an extension of the pericardium itself (Fig. 24.17a). The glandular tube of the nephridium consists of spongy tissue; it branches along its course and the branches divide on their turn into ﬁnetubules. Under the microscope, the tube and its branches are seen as irregular cubical cells with distinct nuclei surrounding the lumens of the tube and its branches (Fig. 24.17b). A short renal duct leads to the external renal opening, situated in a slit-like apperture, the reno-gonadial vestibule, at the junction of the gill with the visceral mass (Fig. 24.17b). (vii) Reproductive organs: The sexes are separate in P. margaritifera, but there are no external features that indicate the type of sex in this species. On removing the right valve, the gonad appears as a creamy or yellowish

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Morphology and Anatomy of the Pearl Oyster …

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Fig. 24.17 a Diagram showing the excretory system of P. margaritifera viewed from the posterior side. b Section through the reno-pericardial canal showing the adjacent renal cells. A photomicrograph of the section is shown on the left

white substance under the epithelium surface covering the visceral mass on both sides. The male and female gonads can, however, be distinguished by taking a portion of the creamy gonad with a glass pipette and dropping it into a beaker containing sea-water; the former appears as a milky substance while the latter appears as white and very tiny granules suspended in the water. Both male and female gonads consist of ﬁne tubules that branch on the left and right surfaces of the digestive diverticula being covered by the surface epithelium. The tubules increase in diameter as they extend ventrally and join the gonoduct on both sides. Each gonoduct opens in the respective reno-gonadil vestibule situated at the level of fusion of the gill base with the visceral mass. At sexual maturity, the gonads increase in size and the ﬁne branches of the gonoduct can be seen on the surface of the visceral mass through the thin surface epithelium. The maximum development of gonads in P. margaritifera is attained in June, but it depends mostly on the availability of food, avoidance of overcrowding and absence of turbidity due to suspended sediment particles.

The thickness of gonads which indicates the degree of gonadal development in oysters could be measured by taking a transverse section passing on the ventral border of the labial palps across the stomach to the posterior end of the body (Galtsoff 1964). In wild P. margaritifera that were 4– 5 years old collected outside the cultivated area at a depth of 4 meters, the thickness of the gonad was found to be 5– 6 mm. In the cultivated pearl oysters that were 3 years old collected from trays 2 m deep, the thickness of the gonad ranged from 3 to 3.5 mm. The histology of the male gonad shows follicles each of which is surrounded by a germinal epithelial layer with spermatozoa scattered at the periphery of follicular lumen. The shape and size of spermary in the follicle vary according to the degree of gonadal development and the season of the year. In slightly ripe gonads, the germinal epithelium of the follicle is quite distinct; some spermatozoa are distinguishable with their rounded heads and long tails which are directed towards the lumen of the follicle while other spermatozoa are found at different stages of development (Fig. 24.18a). In complete ripe spermary, however, the

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Fig. 24.18 a Transverse section of mature spermary of P. margaritifera with a photomicrograph b Photomicrograph of a transverse section of a ripe ovary of P. margaritifera

spermatozoa are densely packed inside the follicle and the germinal epithelium can hardly be distinguished. In the female gonad, the lumen of the follicle is ﬁlled with ova at different stages of development. These ova are attached to the walls of the follicle by narrow short stalks or peduncles, but as they become detached from the wall, the peduncles and the eggs become spherical, elongate or pea-shaped structures with large round nuclei and distinct nucleoli (Fig. 24.18b). The spawning period of P. margaritifera starts at the end of June and continues throughout July and August. Such a

deﬁnite spawning season is one of the advantages in cultivating P. margaritifera on a commercial scale (Crossland 1957; Reed 1964). In sexually mature oysters with ripe gonads, spawning could be induced by a sudden rise in temperature of the sea-water in the aquarium containing the oyster. This was observed in an experiment made to show the effect of temperature on shell movement when the water was warmed from 26 to 34 °C. However, only 3 out of 5 oysters chosen for this experiment responded to temperature stimulation.

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Conclusion

References

Some morphological and anatomical differences were highlighted between Pinctada margaritifera on one hand and both Ostrea edulis and Crassostrea virginica on the other hand. These differences included the growth at either side of the umbo which is asymmetrical in P. margaritifera resulting in a long hinge on one side of the umbo, a condition that plays an important role in orienting P. margaritifera. This feature is not found in either Ostrea edulis or Crassostrea virginica. Both valves in P. margaritifera are moderately convex and neither of them can be easily distinguished, unlike O. edulis, and C. gigas. The adductor muscle in P. margaritifera is very large compared to that of O. edulis and C. gigas, and the mantles have free edges in P. margaritifera. The missing of pedal ganglia in both C. gigas and O. edulis due to the absence of a foot in these species. One of the advantages of cultivating P. margaritifera in the Sudanese Red Sea is that this species has a deﬁnite spawning season starting at the end of June and continuing throughout July and August.

Crossland C (1957) The cultivation of the mother-of-pearl oyster in the Red Sea. Aust J Mar Freshw Res 8:11–130 Fougerouse A, Rousseau M and Lucas S (2008) Soft tissue anatomy, shell structure and biomineralization. In: Sauthgate P, Lucas J (eds) The pearl oyster. Elsevier BV pp 76–102 Galtsoff PS (1964) The American oyster crassostrea virginica Gmelin, vol 64. U.S. Bureau Fisheries Bulletin, pp 1–480 Herdman WA (1904) The pearl oyster ﬁsheries of the Gulf of Manaar. Report to the Government of Ceylon, Part II. The Royal Society, London, pp 37–67 Hynd JS (1954) A revision on the Australian pearl shells, Genus Pinctada (Lamellibranchia). Aust J Mar Freshw Res 6(1):98–137 Nelson TC (1918) On the origin, nature and function of the crystalline style of lamellibranchs. J Morphol 31:53–111 Orton JH (1937) Oyster biology and oyster culture. Buckland lectures for 1935. Arnold, London PERSGA/GEF (2004). Survey of the proposed marine protected area at Dungonab Bay and Mukawwar Island, Sudan. Report for PERSGA. PERSGA Jeddah Reed W (1964) The pearl shell farm at Dongonab Bay. Sudan Notes Rec 45:158–163 Yonge CM (1926a) The digestive diverticula in the lamellibranchs. Trans Roy Soc Edinburgh 54:703–718 Yonge CM (1926b) Structure and physiology of the organs of feeding and digestion in Ostrea edulis. J Marine Biol Assoc U K 14:295– 386 Yonge CM (I960) Oysters. Willmer Brothers & Harman Ltd. London, 209 p

Acknowledgements I am most grateful to Dr. P. J. Vine for his continuous encouragement and thanks are due to the Fish Diseases Laboratory at Weymouth, U.K., for allowing a working space in their laboratory. This research work has been sponsored by the National Council for Research, Khartoum, Sudan, to whom I am grateful, for much support and encouragement.

Copepoda—Their Status and Ecology in the Red Sea

25

Ali M. Al-Aidaroos, Mohsen M. El-Sherbiny and Gopikrishna Mantha

Abstract

The subclass Copepoda is an important driving force in linking the lower trophic to higher trophic levels in aquatic ecosystems. Despite their ecological importance in marine waters, very little work has been done along the Red Sea since the early 19th century. Until now, about 276 species from 76 genera, 55 families, and 6 orders of copepods have been recorded in the Red Sea. This chapter discusses the diversity, distribution and ecology of the Red Sea copepods, which show an increasing gradient of species richness and biomass from north to south. Moreover, the standing stock of zooplankton in the southern Red Sea is higher than the central and northern parts. The majority of copepods recorded are during the winter season. The epipelagic zone in the Red Sea is usually dominated by small-sized genera, especially Acrocalanus, Calocalanus, Clausocalanus, Corycaeus, Ctenocalanus, Macrosetella, Oithona, Oncaea, Paracalanus, Paraoithona and Parvocalanus. With increasing depths, microcopepods belonging to the family Oncaeidae become numerically more important than the calanoid copepods. A special focus has been provided with reference to the effect of UV-B radiation on their biology, which shows that the maximum mortality rates of copepods under ambient solar radiation levels average a ﬁve-fold increase over the average mortality in the dark. The chapter also discusses the symbiotic and parasitic relationship of copepods with other organisms, such as corals and coral-reef ﬁshes. A preliminary report shows A. M. Al-Aidaroos (&) M. M. El-Sherbiny G. Mantha Faculty of Marine Science, Department of Marine Biology, King Abdulaziz University, Jeddah, Saudi Arabia e-mail: [email protected] M. M. El-Sherbiny Faculty of Science, Department of Marine Science, Suez Canal University, Ismailia, Egypt G. Mantha Marina Laboratories, 14 Kavya Gardens, N. T. Patel Road, Chennai, 600107, Tamilnadu, India

that symbiotic copepods attain a high diversity from scleractinian coral genera, such as Pocillopora sp., Acropora sp., Stylophora sp., Favia sp. and Fungia sp. This chapter provides a baseline introduction on copepods and possible research in different aspects of their biology, which may provide a new step in copepod research in the Red Sea.

Introduction The subclass Copepoda is a group of small-sized, but most numerous, omnipresent and highly diversiﬁed aquatic crustaceans, which forms an important connecting link in the ecological food web. Taxonomically they are categorized into nine major orders, Platycopioida, Calanoida, Cyclopoida, Harpacticoida, Gelyelloida, Mormonilloida, Misophrioida, Siphonostomatoida and Monstrilloida (Boxshall and Hasley 2004; Ahyong et al. 2011). They inhabit almost all aquatic habitats from freshwater to hypersaline waters, from subterranean caves to waters collected in bromeliad leaves or leaf litter, from streams, rivers, and lakes to the sediment layers, from the open surﬁcial epipelagic waters to the deepest known ocean trenches and from the cold polar ice-water interface to the hot active hydrothermal vents (Huys and Boxshall 1991; Boxshall and Hasley 2004). Their mode of living is either or a combination of free-living, symbiotic, or internal or external parasites, on almost every animal phyla known in the aquatic environment, except Protozoa (Huys and Boxshall 1991). Except for Gelyelloida, all other copepod orders have been reported from marine waters (Boxshall and Halsey 2004). Cyclopoida and Poecilostomatoida, although having taxonomic ambiguities (Kim and Kim 2000; Boxshall and Halsey 2004; Huys et al. 2012), were considered as different orders (Huys and Boxshall 1991), but after the discovery of the family Fratiidae Ho et al. (1998), Boxshall and Halsey (2004) grouped them into the order Cyclopoida.

© Springer Nature Switzerland AG 2019 N. M. A. Rasul and I. C. F. Stewart (eds.), Oceanographic and Biological Aspects of the Red Sea, Springer Oceanography, https://doi.org/10.1007/978-3-319-99417-8_25

453

454

The Red Sea, being oligotrophic in nature, is considered an unfavourable environment for plankton owing to its high salinity, lack of any freshwater inputs and high evaporation rates (Weikert 1987), although having its own endemic diversity (Halim 1984). Many of the planktonic organisms which immigrate from the Indian Ocean via the Gulf of Aden to the northern Red Sea do not thrive well in higher salinities and temperatures that prevail in the deeper waters of the Red Sea, and hence are not able to survive during migration toward the northern Red Sea, while the evolution of endemic species is favoured (Kimor 1973). The majority of the copepods in the Red Sea are recorded from the planktonic Calanoida and Cyclopoida, and to some extent Harpacticoida that form an important link in the aquatic food chain by linking primary producers with secondary consumers (Gorelova 1974; Sullivan 1980; Kimmerer 1984; Sommer and Stibor 2002). Copepods are the most numerous zooplanktonic group, which makes up more than about 75% in the northern Red Sea (Almeida Prado-Por 1983, 1985; Aamer et al. 2006; Cornils et al. 2007a; Dorgham et al. 2012; Khalil and Abd El-Rahman 1997; El-Serehy et al. 2013), accounts for up to 83% in the central Red Sea (Weikert 1982; Böttger 1987; Schneider et al. 1994), and more than 70% in the southern Red Sea (Beckmann 1984; Böttger-Schnack 1995; Al-Aidaroos et al. 2016a) of the total zooplankton composition. Red Sea copepods originate and/or are closely related to the Indo-Paciﬁc origin (Por 1978; Halim 1990; Sen Gupta and Desa 2001; El-Sherbiny and Ueda 2008b; El-Sherbiny 2009; El-Sherbiny and Al-Aidaroos 2014). Presently, about 977 species of planktonic copepods are recorded from the Indian Ocean (Razouls et al. 2005–2017), with about 276 recorded species in the Red Sea (present study). The epipelagic zone in the Red Sea is usually dominated by copepods, and most conspicuously the small-sized genera: Acrocalanus, Calocalanus, Clausocalanus, Corycaeus, Ctenocalanus, Macrosetella, Oithona, Oncaea, Paracalanus, Paraoithona, Parvocalanus and Sapphirina (e.g., Beckmann 1984; Schneider and Lenz 1991; Schneider et al. 1994; Böttger-Schnack 1990b, 1994; Böttger-Schnack et al. 2001; Farstey et al. 2002). Recently, the importance of Acartia species has been documented in the coastal waters of the Red Sea (El-Sherbiny and Al-Aidaroos 2014; Al-Aidaroos et al. 2016a). In general, the abundance of large and small mesozooplankton in the central Red Sea is higher during winter than in autumn (Weikert 1980b, 1988; Böttger 1987). A decrease of 30% in the total biomass and abundance of zooplankton between the central (21°N) and northern Red Sea (24°N) during autumn 1980 was observed by Böttger (1987), whereas Delalo (1966) and Gordeyeva (1970) reported a continuous decrease in zooplankton from the south to the north. Concerning seasonal distribution, Halim (1969) reported that about 92% of copepod species in the Red Sea recorded were during the winter compared to about 62% recorded in the summer-autumn.

A. M. Al-Aidaroos et al.

In this chapter, we will focus on the diversity and distribution of copepods, and try to highlight the importance of copepods along the coral reefs, as well as the vulnerability of zooplankton to Ultraviolet-B (UV-B) radiation and some preliminary aspects on the symbiotic copepod associates of coral reefs in the Red Sea region.

History Most studies carried out in the Red Sea were focused mainly on the oceanic waters through several expeditions, for example, the POLA Expeditions 1895–96, 1897–1898, John Murray Expedition 1933–34, Soviet Expedition 1963, Metalliferous Sediments Atlantis-II Deep (MESEDA program), RV Sonne 1977–1978, RV Valdivia 1979 and 1980–1981, RV Meteor-III 1987, RV Tyro 1992–1993, RV Meteor-44/2 cruise 1999 and RV Pelagia 2012. These works paid much attention to zooplankton, including copepods. The subclass Copepoda has been studied in the Red Sea since the early 20th century (Cleve 1900). Due to its exceptionally isolated condition, many researchers showed their interest in copepod fauna of the Red Sea, for example, studies carried out along the longitudinal axis of the Red Sea (Sewell 1948; Gordeyeva 1970; Böttger-Schnack et al. 1989, 2004; Böttger-Schnack and Schnack 1989; Böttger-Schnack 1990b, 1991, 1992, 1994, 1995; Kürten et al. 2015), Gulf of Aqaba (Fedorina and Kornilova 1970; Schmidt 1973; Almeida Prado-Por 1983, 1984; Echelman and Fishelson 1990; Khalil and Abd El-Rahman 1997; El-Sherif and Aboul Ezz 2000; Al-Najjar 2002, 2005; El-Serehy and Abd El-Rahman 2004; Al-Najjar and Rasheed 2005; Cornils et al. 2005, 2007a, b, c; Aamer et al. 2006; El-Sherbiny et al. 2007; Al-Najjar and El-Sherbiny 2008; Schnack-Schiel et al. 2008; Dorgham et al. 2012; El-Serehy et al. 2013), central Red Sea (Karbe 1980; Weikert 1980a, b, 1981, 1982; Beckmann 1984; Ferrari and Böttger 1986; Böttger 1987; Böttger-Schnack 1988, 1990a; Schneider et al. 1994), southern Red Sea (Delalo 1966; Weikert 1980a, 1982; Beckmann 1984; Schneider et al. 1994; Böttger-Schnack 1995; Couwelaar 1997; Al-Aidaroos et al. 2016a) and neritic waters (Nicholls 1944; Couwelaar 1997; Al-Aidaroos et al. 2016a). Most of these works demonstrated that the majority of the microcopepod fauna of the Red Sea are the oncaeid copepods, which were prominently dealt with by Böttger-Schnack (1990a, b, 1991, 1992) and Böttger-Schnack et al. (2001).

Abundance and Diversity In the Red Sea, the diversity of oceanic zooplankton is relatively low compared to adjacent seas as well as other subtropical seas (Halim 1969, 1984; Kimor 1973;

25

Copepoda—Their Status and Ecology in the Red Sea

Böttger-Schnack 1994). Most Red Sea copepods are known to be inhabitants of the Indo-Paciﬁc region, of which about 33% are not known from the Mediterranean Sea (Halim 1969). Their diversity and abundance decrease northward with increasing distance from the southern entrance (Bab el Mandab), where the primary production is mainly controlled by the inflow of nutrient-rich waters into the Red Sea from the Gulf of Aden (Wafar et al. 2016). The shallow sill at Bab el Mandab prevents the exchange of bathypelagic plankton between the Red Sea and the deep waters of the Gulf of Aden. These deep-waters are warmer and more saline, and with a combined oxygen minimum and phosphate maximum extending from 300–600 m results in the fluctuation of plankton diversity and biomass related to surface circulation governed by the winds (Morcos 1970; Beckmann 1984; Schneider et al. 1994; Böttger-Schnack 1995; Couwelaar 1997; Soﬁanos and Johns 2003; Morcos and AbdAllah 2012; Wafar et al. 2016). Abundance varies with sampling depth, and mesh size used under different seasons; for example, calanoids dominate in the larger mesh size of about 1000 µm size fraction (Al-Najjar 2005; Al-Najjar and Rasheed 2005). The mean total biomass of the southern Red Sea zooplankton showed a two-fold increase from the SW monsoon (14– 17.5 ml m−2) toward the NE monsoon (23.9–40.2 ml m−2) (Couwelaar 1997). A higher biomass, around a 10-fold increase, was evident from the use of a smaller 65 µm mesh size when compared with a 300 µm mesh sized net from the upper 100 m layer (Böttger 1987; Schneider et al. 1994). However, Al-Najjar and Rasheed (2005) observed a significant difference with depth, showing higher biomass in the surface to 50 m, compared with the surface to 25 m depth, which might be related to the disturbance of the sea surface layer by low air pressure causing vertical mixing (Tomosada and Odate 1995) and subsequent nutrient enrichment (Manasrah et al. 2004; Al-Najjar and El-Sherbiny 2008) (Table 25.2).

Distribution Zooplankton diversity studies using small nets ( 100 µm mesh size) have documented the dominance of smaller sized copepods in the oceanic waters of the Red Sea (Böttger 1987; Böttger-Schnack 1988, 1994; Böttger-Schnack et al. 1989; Schneider et al. 1994). In the epipelagic zone (upper 100 m) of the northern Red Sea, the most dominant copepod genera were small calanoids, like Paracalanus, Acrocalanus, Clausocalanus, Centropages, Acartia, and relatively large calanoid species, such as Nannocalanus minor, Euchaeta concinna, Paracandacia truncata, in addition to the cyclopoid genera, Oithona, Oncaea, Corycaeus and Lubbockia. In the greater depths, the calanoids, Candacia samassae, Eucaheta plana, Macandrewella chelipes,

456

A. M. Al-Aidaroos et al.

Table 25.1 Distribution, abundance (ind m−3) and biomass studies carried out in the Red Sea. RS = Red Sea proper; NRS = northern Red Sea; CRS = central Red Sea; SRS = southern Red Sea; GoAq = Gulf of Aqaba; GoAden = Gulf of Aden; # = total depth is considered (all the depths range were added together and total abundance and biomass for the total depth is considered here); *** = total zooplankton Place

Vertical/horizontal

Mesh size (lm)

Depth (m)

No. of species

Abundance# range (average)

Biomass# (mg m−3/ ml m−2)

References

GoAq, NRS

Horizontal

100

Surface

51

1,326–9,825 (6,710)

–

Aamer et al. (2006)

SRS

Horizontal

150

Surface

100

1,058–25,787 (5,230)

–

Al-Aidaroos et al. (2016a)

GoAq, NRS

Vertical

200

500

31

(76.3)

–

Almeida Prado-Por (1983)

NRS

Horizontal

100

Surface

–

–

18.40 mg. dry wt. m−3 (annual average)

Al-Najjar and El-Sherbiny (2008)

GoAq, NRS

Vertical

150

100

55

–

–

Al-Najjar (2002)

GoAq, NRS

Horizontal

150

Surface

–

NA

19.9 ± 3.39 mg m−3 (Autumn) 31.9 ± 4.257 mg m−3 (Spring) 10.6 ± 2.52 mg m−3 (Summer)

Al-Najjar (2005)

GoAq, NRS

Vertical

100

25 50

–

–

2.15–6.71 mg m−3 4.08–9.88 mg m−3

Al-Najjar and Rasheed (2005)

GoAden and CRS

Vertical

300

1050

79,000–83,000*** ind. m−2

20–24 gm m−2

Beckmann (1984)

CRS

Vertical

100

450

45

30– 39 103(34 103) ind. m−2

–

Bottger-Schnack (1988)

GoAq, NRS

Vertical

150

1300

–

93–431 103 (89.3%)

–

Cornils et al. (2005)

GoAq, NRS

Vertical

200

100

18 families 26 genera

58.19–92.39 (79%)

–

Cornils et al. (2007a)

CRS and GoAden, SRS

Vertical

320

1500

–

–

mean 14–17.5 ml m−2 (SW Monsoon) mean 23.9– 40.2 ml m−2 (NE monsoon)

Couwelaar (1997)

RS

Horizontal

300

100 100–200 200–500

–

–

Winter 47.7 mg m−3 (NRS) 81.1 mg m−3 (central) 104.8 mg m−3 (SRS) 9 mg m−3 (NRS) 14 mg m−3 (central) 38 mg m−3 (SRS) 10 mg m−3 (NRS) 17 mg m−3 (central) 19 mg m−3 (SRS)

Delalo (1966)

GoAq, NRS

Vertical

100

100

52

(2,112) 87.9% copepods

GoAq, NRS

Horizontal

500

Surface

30

155 (winter) 103 (summer)

12.2 g m−3 (winter) 8.5 g m−2 (summer)

Echelman and Fishelson (1990)

GoAq, NRS

Vertical

55

100

74

–

–

El-Serehy and Abd El-Rahman (2004)

NRS

Horizontal and vertical

90

Surface and 100

81

251–1,940

–

El-Serehy et al. (2013) (continued)

***

Dorgham et al. (2012)

25

Copepoda—Their Status and Ecology in the Red Sea

457

Table 25.1 (continued) Place

Vertical/horizontal

Mesh size (lm)

Depth (m)

No. of species

Abundance# range (average)

Biomass# (mg m−3/ ml m−2)

References

GoAq, NRS

Vertical

100

100

66

(1,840) 84.7% copepods

–

El-Sherbiny et al. (2007)

GoAq, NRS

Horizontal

50

Surface

44

–

–

El-Sherif and Aboul Ezz (2000)

NRS and CRS

Vertical

65 300

500

–

2,520

Summer 42 mg m−3 (north) 142 mg m−3 (CRS) 15.5 mg m−3 (NRS) 59 mg m−3 (CRS)

Gordeyeva (1970)

GoAq, NRS

Horizontal

55

Surface

27

(1,945)

–

Khalil and Abd El-Rahman (1997)

65 200 330

50

–

–

3.1–504.5 ml m−3 (Summer) *** 6.4–249.1 ml m−3 (winter) *** 3.5–392.9 ml m−3 (Summer) *** 3.1–144.8 ml m−3 (winter) *** 1.6–596.5 ml m−3 (Summer) *** 3.5–83 ml m−3 (winter)

Klinker et al. (1978)

Summer

Oceanographic and Biological Aspects of the Red Sea

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