Does host diet govern the structure and diversity of tapeworm assemblages in sharks? Insights from the literature and a model shark species; Cephaloscyllium isabellum _______________________________________________________________________________________ Trent Rasmussen (ID: 6737930) A thesis submitted for the degree of Masters of Science in Ecology University of Otago, Dunedin, New Zealand Supervisors: Haseeb Randhawa and Steve Wing i Abstract Previous research has shed some light on what phylogenetic and ecological factors may be important determinants of tapeworm parasite diversity in elasmobranchs (sharks, skates and rays). However, several potentially key factors for tapeworm transmission, including the breadth and composition of host’s diets, have been recognised as crucial gaps in our understanding. The main objective of this research was to investigate the relative importance of sharks’ diets for the structure and diversity of their tapeworm assemblages. First, the literature was searched for information on tapeworms and host features for a large subset of different shark species, and aspects of shark’s diets (including their diet breadth, diet composition and trophic level) were assessed for their relative importance as predictors of tapeworm diversity. Second, literature records were used to conduct a comprehensive analysis of the relationship between shark’s diet compositions and tapeworm compositions. Finally, the importance of host diet was examined as a potential encounter filter for restricting tapeworm diversity in a model shark species, Cephaloscyllium isabellum. The results of this study revealed diet breadth to be a key predictor of tapeworm richness in sharks, indicating that sharks with broader diets generally harbour more tapeworm species. The composition of tapeworms infecting a shark species was found to be related to its diet composition, and moreover, certain tapeworm taxa were found to be useful indicators of the host species' ecology and evolutionary history. The research on C. isabellum here offered only limited insights into the potential importance of diet as an encounter filter for the shark, but provided some new important data on both the diet and parasites of this species. Ultimately, the observational studies carried out within this research emphasise that aspects of sharks’ diets can have important implications for their tapeworm parasite assemblages. Further exploration of these patterns with experimental research may be able to validate the influence of these patterns in nature. ii Acknowledgements I would firstly like to thank the University for selecting me as a candidate for an MSc Research Year Scholarship, which supported me throughout this project. To my supervisors Haseeb Randhawa and Steve Wing, I cannot thank you enough for providing me with your critical support and feedback. Overall, I could not have hoped for better mentors. Thanks to Haseeb for his constant guidance and advice all the way from the inception of ideas for this research to the analyses and final stages of writing. Thanks to Steve for his advice and ideas, especially on the scientific methods for data collection, and for his support in overseeing the logistics for conducting this research. I would like to say a big thank you to the staff in the Marine Science and Botany departments for helping me to setup and carry out the practical parts of this research. Thanks to Doug Mackie, Daryl Coup and Sean Heseltine for their help in organising shark prey collections, and to Peter Batson and Adelle O'Neill for their assistance in collection trips and setup of my laboratory workspace. In addition, thanks to Gavin Heineman (Echo F/V) for his help in collections of sharks and some invertebrates. I am grateful for Vickey Tomlinson of the Botany department, for helping to provide me with the needed workspace and resources for some of the practical work, and for Michelle McKinlay (Botany) and Christoph Matthaei (Zoology) for their guidance on the logistics of completing and submitting this project. Thank you to my colleagues and professors who got involved with this research throughout various stages. I would like to thank Keith Probert for his advice regarding some of the identifications of collected invertebrate species and my fellow students Thibaut Anglade, Steph Bennington and Zuri Burns who helped me with some of the practical work. I would also like to extend my thanks to Robert Poulin and various members of the Evolutionary and Ecological Parasitology Group for their valuable discussions and insights regarding some of the ideas and methods used in this project. Finally, I would like to thank my partner Ashley, and my friends and family for being there for me during each stage of this project. My long and arduous journey towards completing this thesis was made possible thanks to their continued support and encouragement. iii Table of Contents Abstract .......................................................................................................................... i Acknowledgements ..................................................................................................... ii List of figures ................................................................................................................ v List of tables................................................................................................................. vi Chapter 1: Introduction .............................................................................................. 1 1.1. General introduction ........................................................................................... 2 1.2. Host specificity and barriers to parasite establishment ....................................... 4 1.3. The influence of host diet on parasite diversity .................................................. 7 1.4. Life cycles of shark tapeworms .......................................................................... 8 1.5. Biology of the model species: Cephaloscyllium isabellum .............................. 10 1.6. Study location ................................................................................................... 11 1.7. Aims, objectives and hypotheses ...................................................................... 12 1.8. Overview of thesis chapters .............................................................................. 13 Chapter 2: Host diet as a determinant of tapeworm diversity in sharks .............. 15 2.1. Introduction ....................................................................................................... 16 2.1.1. Objectives of chapter 2 ............................................................................... 18 2.2. Methods............................................................................................................. 19 2.2.1. Tapeworm data collection .......................................................................... 19 2.2.2. Host features data collection ....................................................................... 21 2.2.3. Data analysis ............................................................................................... 23 2.3. Results ............................................................................................................... 26 2.3.1. Determinants of tapeworm richness ........................................................... 28 2.3.2. Determinants of tapeworm TD ................................................................... 31 2.4. Discussion ......................................................................................................... 35 2.4.1. Conclusions ................................................................................................ 41 Chapter 3: Linking the diet composition of sharks to their tapeworm compositions and use of prey as intermediate hosts ............................................... 43 3.1. Introduction ....................................................................................................... 44 3.1.1. Objectives of chapter 3 ............................................................................... 46 3.2. Methods............................................................................................................. 47 3.2.1. Data collection of shark diets and tapeworms ............................................ 47 3.2.2. Analysis of diet vs. tapeworm composition ................................................ 50 3.2.3. Data collection on intermediate host families ............................................ 51 3.2.4. Analysis of intermediate host importance .................................................. 51 3.3. Results ............................................................................................................... 52 iv 3.3.1. The influence of sharks’ diets on their tapeworm compositions ................ 52 3.3.2. Linking trypanorhynch intermediate hosts with shark diet composition ... 59 3.4. Discussion ......................................................................................................... 63 3.4.1. The influence of sharks’ diets on their tapeworm compositions ................ 65 3.4.2. Linking trypanorhynch intermediate hosts with shark diet composition ... 69 3.4.3. Conclusions ................................................................................................ 71 Chapter 4: Analysing host diet and parasites in a model species; the draughtsboard shark Cephaloscyllium