Cephalorhynchus Heavisidii and Tursiops Aduncus) Found Along the Coast of South Africa
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A GENETIC STUDY OF TWO INSHORE DOLPHIN SPECIES (CEPHALORHYNCHUS HEAVISIDII AND TURSIOPS ADUNCUS) FOUND ALONG THE COAST OF SOUTH AFRICA by Keshni Gopal Submitted in partial fulfilment of the requirements For the degree of Doctor of Philosophy (Zoology) In the Faculty of Natural & Agricultural Sciences University of Pretoria Pretoria (November 2013) i © University of Pretoria A GENETIC STUDY OF TWO INSHORE DOLPHIN SPECIES (CEPHALORHYNCHUS HEAVISIDII AND TURSIOPS ADUNCUS) FOUND ALONG THE COAST OF SOUTH AFRICA Student: Keshni Gopal (Student number: 29596892) Administrative Supervisor: Dr. P. J. Nico de Bruyn Mammal Research Institute University of Pretoria P. O. Box 61 Pretoria 8000 South Africa Academic Supervisors: Dr. Leszek Karczmarski The Swire Institute of Marine Science School of Biological Sciences The University of Hong Kong Cape d’Aguilar Shek O Hong Kong Dr. Krystal A. Tolley Applied Biodiversity Research South African National Biodiversity Institute Private Bag X7 Claremont 7735 South Africa ii © University of Pretoria Preface “It’s not the strongest of the species that survives, nor the most intelligent that survives. It is the one that is most adaptable to change.” ~ Charles Darwin iii © University of Pretoria Dedication I dedicate this thesis to my love, Pascal, for always being there for me and for being my pillar of strength! I further dedicate this thesis to my parents, for their continual support and love. iv © University of Pretoria Acknowledgements I am grateful to everyone who has contributed in the completion of this project. Firstly, I would like to acknowledge my supervisors: Nico de Bruyn, Krystal Tolley, and Leszek Karczmarski, for their support. This research has been possible thanks to the Andrew W. Mellon Foundation, National Research Foundation and IUCN for the financial support and running costs for majority of the project; the Threatened Species Programme for providing financial support so additional microsatellite loci could be analyzed; and the Rufford Small Grants Foundation for providing funds for extra sea work. Sincere thanks go out to the following principle collaborators: Dr. Stephanie Plön, a researcher associate, at the Nelson Mandela Metropolitan University; and Dr. Geremy Cliff from the KwaZulu Natal Sharks Board for providing Indo-Pacific bottlenose dolphin tissue samples. Special thanks go to Dr. Kim Andrews, from the University of Hawaii, for loaning her Hawaiian sling for my sample collection and to Dr. Simon Elwen, for collecting skin biopsies from Heaviside’s dolphins in Namibia for this study. Heartfelt thanks go to the Oceans and Coast Department: Michael Meyer, Toufiek Samaai, Steven McCue and Deon Kotze for providing the resources and assistance on most of my trips on the west coast. Without your support, obtaining biopsies samples from those areas would not have been possible. Many thanks to the following people that have assisted on my sea trips and for adding value to my data collection: Mammal Research Institute: Meredith Thornton and Caryn Behrmann on Balaena South African National Biodiversity Institute: Zoë Davids Two Oceans Aquarium: Vincent Cader, on Baggin Port Nolloth Outboard & Salvage: Cobus van Baalen on Slimvis An ethical clearance certificate was granted by SANBI to conduct research on Heaviside’s dolphins (001/2011). The following permits were issued by the Department of Environmental v © University of Pretoria Affairs for the duration of the sea work: RES2009/06, RES2010/24, RES2011/70, and RES2012/67. The Ministry of Environment and Tourism, Namibia, issued the following export permits for me to receive the biopsy samples Dr. Elwen collected for this project: 78438, 120586, and 138004. To my lab buddies at the Molecular Laboratory: Zoë Davids, Buyisile Makhubo, Shelley Edwards, Jessica Da Silva, Shandrè Dreyer and Ryan Daniels – thank you all for the general chit-chats, and especially the giggles which made the lab a better environment to be in. An extra special thank you to Zoë Davids, for sharing her working environment with me; for being a great colleague and for bearing with my every now and then “bizarre PhD student behaviour.” I also want to thank Rowena Siebritz for assisting with the administration and procurement side of my project. To my mentor, Colleen Seymour, thank you for coming on board during the last phase of my research. I appreciate the effort you have made by providing constructive comments on my drafts, and to Leslie Powrie, thank you for your assistance with creating a model for the Population Viability Analysis. Heartfelt gratitude goes to my family: Bapuji, Mummy, Jayesh, Hashika and Keshriebhabi; and friends: Nawaal, Darshana and Andrew for their moral support and the yummy home-made pizzas! To my furry four-legged best friend, Master Woofles - you have no idea how much you have kept me going. The happiness and love you have showered upon me every time I saw you gave me the strength to overcome anything, and even though you cannot speak, I know that you knew exactly what it was I was going through. Thank you for always being that great sphere of blissful energy! Lastly, to the love of my life, Pascal, there are not enough words that can describe the important role you have played throughout my PhD. Thank you for always being there for me through the good and tough times, and for being patient with me whilst undergoing this journey. Your constant words of wisdom, and most of all, for just being there by my side till the end, was always a comfort. I will forever be grateful for all that you have done. vi © University of Pretoria Abstract Genetic parameters such as genetic variability, gene flow, relatedness and migration were determined between two South African coastal delphinid species, Cephalorhynchus heavisidii (Heaviside’s dolphin) and Tursiops aduncus (Indo-Pacific Bottlenose dolphin), in order to contribute towards designing efficient conservation management strategies. The molecular markers used in this study include the mitochondrial DNA control region (mtDNA) and several microsatellite loci that were chosen from existing dolphin primer sets which also proved to cross- amplify on additional cetacean species. The population structure and gene flow investigated for Heaviside’s dolphins across seven sampling sites (n = 395) revealed contrasting results. Mitochondrial DNA suggested six populations within the range studied (ФST = 0.15611, P < 0.0001), whilst microsatellite data identified only two populations and differed with respect to the relative levels of specific pair- wise population differentiation comparisons. Neutrality tests of the mitochondrial sequences combined to the mismatch distribution analysis, pointed towards a population expansion at the two geographic extremes (Table Bay and Walvis Bay), whereas bottleneck tests suggest a bottleneck in the northern population (Lamberts Bay, Hondeklipbaai, Port Nolloth, Luderitz, and Walvis Bay). Genetic relatedness and population connectivity of the two known populations and amongst sampling localities confirmed that connectivity and relatedness exist among the sampling sites, and that the northern and southern meta-populations are less well connected. Table Bay area was revealed unique because of its high relatedness. The sampling sites are different from each other in terms of population connectivity and relatedness, suggesting spatial partitioning in relation to environmental and social factors within the population, with some level of connectivity displayed in certain localities. The establishment of shark nets along the KwaZulu-Natal coastline that protects beach goers has had a long-term detrimental effect on the bottlenose dolphin (Tursiops aduncus) populations that inhabit the area since they are incidentally caught in these nets. A comparative study was done by comparing recently collected data (2007 - 2011) to previous sampling (1994 - 2000; Natoli et al. 2008) using mitochondrial DNA control region sequences (583 bp) and fourteen nuclear microsatellite data. The mtDNA sequences suggest that the coastal/migratory population has vii © University of Pretoria undergone a relatively recent demographic change shown by the FST value (ФST = 0.1138, P < 0.0180) in conjunction with the strong expansion signal shown by the mismatch distribution. It is suggested that the two populations be managed independently with a strong focus on conserving the coastal resident population North of Ifafa. Population Viability Analysis revealed that the coastal resident population of T. aduncus would be more affected than the migratory population by the number of individuals being caught in the shark nets. With respect to C. heavisidii, sensitivity analysis revealed that as little as 15 individuals removed from a small population size (n = 10 000) will produce a trend that may affect the overall population size of this species. This study exemplifies the importance of gathering long term life history data, inclusive of the threats faced by both species, in order to implement the correct conservation measures for continual monitoring to take place and ensure the survivorship of both species. viii © University of Pretoria Declaration I, Keshni Gopal, declare that the thesis/dissertation, which I hereby submit for the degree of Doctor of Philosophy (Zoology) at the University of Pretoria, is my own work and has not previously been submitted by me for a degree at this or any other tertiary institution. SIGNATURE: DATE: ix © University of Pretoria Table of Contents PREFACE .................................................................................................................................................................