Biodiversity and community structure of free- living marine nematodes from intertidal areas in the Persian Gulf Narjes Sahraean Biodiversity and community structure of free- living marine nematodes from intertidal areas in the Persian Gulf Promoter: Prof. Dr. Tom Moens Thesis submitted in partial fulfilment of the requirements for the degree of Doctor in Science (Marine Sciences) Academic year 2016-2017 Members of reading and examination committee Prof. Dr. Ann Vanreusel (chair) Ghent University, Belgium Dr. Nele De Meester (secretary) Ghent University, Biology Dept, Marine Biology Prof. Dr. Koen Sabbe Ghent University, Biology Dept., Laboratory for Protistology & Aquatic Ecology Prof. Dr. Frederik Leliaert Botanical Garden Meise, Belgium & Ghent University, Biology Dept. Prof. Dr. Helena Adão University of Evora, Portugal Prof. Dr. Giovanni dos Santos Federal University of Pernambuco, Brazil Prof. Dr. Tom Moens (promoter) Ghent University, Belgium Dedicated to: Hadi, Parmida, Amirhossein, my parents and Marianne for all their love and supports Table of contents Table of contents ACKNOWLEDGMENTS I SUMMARY IV SAMENVATTING VIII CHAPTER 1 GENERAL INTRODUCTION 3 1. STUDY AREA: THE PERSIAN GULF 5 1.1 Geographical, physical and climatological features 5 1.2 Geo-political and industrial importance 11 1.3 Marine Ecosystems of the Persian Gulf 12 1.4 Environmental threats to the Persian Gulf marine environment 16 General information 16 Environmental stressors 17 2 INTERTIDAL AREAS AND SANDY BEACHES 23 2.1 Intertidal areas 23 2.2 Sandy beaches: Definition, characteristics and classification 24 3 BENTHIC COMMUNITIES OF BEACHES 28 3.1 Definition, classification and ecological significance 28 3.2 Intertidal meiobenthos: abundance and diversity 29 3.3 Marine nematodes 30 3.3.1 General characteristics 30 3.3.2 Nematode biodiversity 31 3.3.3 Temporal and spatial patterns in marine nematode assemblages 32 3.4 Zonation patterns of intertidal meiofauna/nematodes 36 3.4.1 Horizontal zonation patterns 36 3.4.2 Vertical patterns 39 3.5. Nematode feeding strategies 41 .3.6 Functional roles of nematodes in ecosystems 43 .3.6.1 Roles in benthic food chains 44 3.6.2. Roles in microbial decomposition and nutrient cycling 45 3.7. Marine nematode dispersal and population genetics 46 3.8. Nematodes as bio-indicators 48 3.9. Diversity measures to monitor impact 50 3.10. Benthic fauna of the PG 52 4. RESEARCH AIMS AND OBJECTIVES 53 CHAPTER 2 NEMATODE ASSEMBLAGE STRUCTURE AND DIVERSITY IN INTERTIDAL BEACHES OF THE NORTHERN PART OF THE STRAIT OF HORMUZ 59 1 INTRODUCTION 62 2 MATERIALS AND METHODS 64 2.1 Sampling sites and design 64 2.2 Sample collection, elutriation and analysis 65 2.3 Data analysis 67 3 RESULTS 69 3.1 Sediment granulometry and total element analysis 69 3.2 Nematode abundance and dominant genera 70 3.3 Nematode diversity 74 3.4 Nematode assemblage structure 77 4 DISCUSSION 82 4.2. Nematode diversity and abundance 83 4.3 Nematode assemblage composition 87 5 CONCLUSIONS 89 CHAPTER 3 YEAR-TO-YEAR VARIABILITY IN BEACH NEMATODE ASSEMBLAGE STRUCTURE AND BIODIVERSITY ALONG THE NORTHERN COAST OF THE STRAIT OF HORMUZ, PERSIAN GULF 99 1 INTRODUCTION 102 2 MATERIALS AND METHODS 104 3 RESULTS 107 3.1 Nematode abundance 107 3.2 Nematode diversity and dominant genera 110 3.3 Nematode assemblage structure 119 4 DISCUSSION 125 4.1 Sediment granulometry and inter-annual variation in nematode assemblages 125 4.2 Climatological effects on inter-annual variation in nematode assemblages 126 4.3 Nematode genus composition and biological interactions 128 4.4 Episodic extremes as a possible cause for inter-annual variability in nematode assemblages 130 4.5 Nematodes as environmental indicators in intertidal areas in the Strait of Hormuz 131 5 CONCLUSION 132 CHAPTER 4 LACK OF POPULATION GENETIC STRUCTURE IN THE MARINE NEMATODES PTYCHOLAIMELLUS PANDISPICULATUS AND TERSCHELLINGIA LONGICAUDATA IN BEACHES OF THE STRAIT OF HORMUZ, IRAN 141 1 INTRODUCTION 144 2 MATERIALS AND METHODS 147 2.1 Study area 147 2.2 Sampling 148 2.3 Morphological identification and vouchering of specimens 148 2.4 Choice of marker sequences 148 2.5 DNA extraction, PCR amplification and sequencing 149 2.6 Population genetic and phylogenetic analysis 150 3 RESULTS AND DISCUSSION 152 3.1 Population genetic structure of Ptycholaimellus pandispiculatus 153 3.2 Population genetic structure and cryptic diversity of Terschellingia longicaudata 157 4 CONCLUSIONS 160 CHAPTER 5 GENERAL DISCUSSION AND FUTURE PERSPECTIVES 171 5. GENERAL DISCUSSION 173 5.1. Marine biodiversity of the PG 173 5.2. Nematode diversity in the PG compared to other sites worldwide 174 5.3. Nematode assemblage composition in the context of environmental pollution 180 5.4. Population genetics 186 5.5. FUTURE PERSPECTIVES 189 REFERENCES 193 APPENDICES 226 i Acknowledgments First and foremost of all, I would like to praise the Almighty God, who has given me all the blessings I have. I would like to express my deepest gratitude to my promoter Prof. Dr. Tom Moens who accepted me as his student and for offering me a place in his working group to work on this topic and for all the supports he provided during my time in Ghent. From the beginning to the end of my PhD study, he was always patient with me, spent lots of time to look after my works, show me the way to go and correct my study. His guidance from the initial steps up to the final stages of this work enabled me to develop an understanding of the subject. On top of everything, Tom was not only a great promoter but also an understandable friend that sympathize and help me overcome difficulties in my life during stay in Belgium. I am really grateful for his excellent guidance throughout my doctoral study at Ghent University. It was a great honor to work with him and I am certainly looking forward for future cooperations. I am extremely grateful to the members of the reading and examination committee: prof. Dr. Ann Vanreusel, prof. Dr. Koen Sabbe, prof. Dr. Helena Adão, prof. Dr. Giovanni dos Santos, prof. Dr. Frederik Leliaert and Dr. Nele De Meester for their excellent comments and suggestions that significantly improved the thesis quality. I would like to express my sincere appreciation to Dr. Ruth Gingold of Sweep & More for a thorough proofreading and help with the structure of chapter 5. Many years in the Marine Biology Research Group, allowed me to meet many fascinating people. I would like to thank all former and present colleagues at this group for creating a friendly atmosphere. Special thanks to Jelle Van Campenhout, Frederik Leliaert, Nele De Meester and Sofie Derycke for their helps and technical expertise. Thank you for sharing your knowledge, good advice, always being open to discuss results and ideas. My sincere gratitude to Annelien Rigaux for her assistance in molecular experiments. I would like to extend my appreciation to An-Sofie D’Hondt for the Dutch summary translation. Many thanks to my office-mate, Joey Genevieve Martinez, for his honest friendship. Thanks to Jeroen De Caesemaeker for all of his computer technical helps. Thanks also to Bart Beuselinck, Niels Viaene and Isolde De Grem for their assistances. i My grateful thanks are also expressed to Mrs. Marianne Border and her husband Hans for lots of helps during our staying in Belgium. I will never forget your kindness. Without them, those past couple of years, would have been much more difficult. Marianne shared many of the joyful and most memorable moments with us. I am most grateful for her extremely friendly and helpful attitude. I wish you to thanks my all Iranian friends in Belgium. I consider myself very fortunate to share your friendship, thank you. I wish to thank Dr. Hossein Negarestan for his helps in the preliminary step of my PhD works. Dr. Keivan Ejlali Khanaghah (Persian Gulf and Oman Sea Ecology Research Center) is also acknowledged for his effective assistances through my PhD work. My sincere appreciations also go to my parents who have been pillar of strength and all of the things I have are from them. Thank to them for their prayers and great moral supports. Thanks to my sister Nasim and my two brothers Hamed and Sadegh for being always concerned about me and for turning the distance into a minor gap via their constant greetings through email and chat and phone calls. Without their attention life was difficult here. Finally, I would like to express my special appreciation and gratitude to my beloved husband, Hadi. Undoubtedly without his helps, love, guidance, spiritual support and encouragement, this thesis would not have been easily completed. He patiently spent some years of his life abroad and shared every moment and giving me the strength. He always kept me going and optimistic. I would like to thank him deeply for his unwavering love and all valuable supports and encouragements. Very special thanks to my lovely children, Parmida and Amirhossein, for creation of enjoyable moments and comfortable atmosphere to finish my thesis. Thank you for making me always smile and laugh, even during the hardest times. As always, it is difficult to mention everybody, I would like to thank all those who direct and indirect supported and helped me during the time being in Ghent and completing this dissertation. Narjes Sahraean March 2017 ii iii Summary The Persian Gulf is a semi-enclosed marginal sea, connected to the Gulf of Oman through the Strait of Hormuz. About one third of the world’s oil is produced in this region. It is an important military, economic and political region due to its oil and gas resources and it is one of the most important waterways in the world. Moreover, the Persian Gulf is located in a subtropical, hyper-arid region with often extreme air temperatures, a high evaporation rate and hence a high water salinity.