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An Isotope Approach Determining Cetacean – Cephalopod Trophic Interactions – An Isotope Approach By Christine Heather Jackson Bachelor of Arts, James Cook University Graduate Diploma (Health Promotion), Curtin University of Technology Master of Science, University of Tasmania Submitted in fulfilment of the requirements for the degree Doctor of Philosophy University of Tasmania (October 2016) ii DECLARATION This thesis contains no material which has been accepted for a degree or diploma by the University or any other institution, except by way of background information and duly acknowledged in the thesis, and to the best of my knowledge and belief no material previously published or written by another person except where due acknowledgement is made in the text of the thesis, nor does the thesis contain any material that infringes copyright Signed; _________________________________ Christine H. Jackson iii AUTHORITY OF ACCESS This thesis may be made available for loan and limited copying and communication in accordance with the Copyright Act 1968. Signed; _________________________________ Christine H. Jackson iv ABSTRACT Determining the biotic and abiotic influences on the distribution and abundance of marine mammals is essential for understanding the dynamics of the food chain. The predator-prey relationship can be deterministic in shaping both the community structure and function of marine ecosystems. This is especially pertinent to recovering toothed whale populations given their large size and high prey consumption rates. A greater knowledge of the trophic linkages between toothed whales and their prey will facilitate assessments of their combined impact on the ecosystem since marine food webs are a fusion of bottom-up and top-down energy and nutrient flow. This is of particular interest for regions that have recovering whale populations and varying climactic changes, such as Australia. Whales and dolphins strand in all Australian coastal areas. However, it is the southern states, of which Tasmania is a particular hotspot, that experience frequent strandings. In the previous two decades there has been in excess of 70 mass strandings. Two of the most common species to strand are long-finned pilot whales Globicephala melas edwardii and sperm whales Physeter macrocephalus. Until 2010, there had been 3974 of these two species that had stranded around Tasmania, 87% of which were long finned pilot whales and 13% were sperm whales (parks.tas.gov.au). Despite the frequent stranding of these toothed whales there is a paucity of trophic information for these species from the Tasmanian region. Similarly, comparatively little is known of the trophic dynamics of oceanic cephalopods which are considered a major prey of many toothed whales in this part of the world. This study used stable isotope analysis to quantify the diet and trophic relationship between toothed whales and cephalopods in regions surrounding Tasmania. Carbon (δ13C) and nitrogen (δ15N) isotopic analysis was conducted on cephalopods that were captured incidentally by commercial fisherman to provide a baseline with which to compare isotopic values of cephalopod prey from predator’s stomachs. Isotopic values indicated that the cephalopod community was inclusive of 3 distinct trophic levels (6.7 ± 1.1 ‰ (Moroteuthis v ingens) to 12.0 ± 0.5 ‰ (Idioteuthis cordiformis), ranging from lower trophic crustacean feeders to higher trophic fish feeders. Some cephalopod species provided evidence of resource partitioning while other species indicated a dietary shift from lower to higher trophic levels as they matured. Furthermore, cephalopods occupy a range of trophic levels and are therefore important vectors in transferring energy up the food chain, particularly to toothed whales. Intrinsic factors such as age, sex or lactation status exhibited little variation on skin δ13C and δ15N values of long-finned pilot whales from 3 stranding events off the coast of Tasmania. Nevertheless, small variations due to stranding events were evident. The δ13C and δ15N values suggested that some adult pilot whales may have a more demersal or shelf foraging habitat while most reflect a pelagic oceanic foraging habitat. Whales showed little trophic enrichment compared to beaks from their stomachs suggesting supplementation of their predominantly teuthophageous diet with other organisms. Long-finned pilot whales also had one of the lowest δ15N values (12.2 ± 0.4 ‰) for pelagic marine mammals in the region. Isotopic analysis defined sperm whales as an apex predator in this region. However, based on skin δ13C and δ15N values, sperm whales showed low variation in foraging based on strandings. Sperm whales are largely teuthophageous feeding on oceanic squid from the meso- and bathy-pelagic zone. δ13C and δ15N values of squid beaks from their stomach contents confirmed that the whales had been foraging in an analagous isotopic region to that of subtropical waters around Tasmania. The isotopic signature of sperm whales was likely a result of a mixture of both low and high trophic level cephalopod prey, with the δ15N value of some prey (e.g. M. hamiltoni 16.8 ± 0.7 ‰) exceeding that of the δ15N value of the predator (e.g. 14.7 ± 0.8 ‰). Smaller-sized beaked whales had lower δ15N values (range 11.0 ‰, Cuviers cavirostris calf to 13.2 ‰, Tasmacetus shepherdi) and assumed lower trophic position than some other odontocetes from the region. There was evidence of niche separation between species. Furthermore, isotopic values of stomach contents of a Cuvier’s beaked whale suggested it might not be predominantly vi teuthophageous. The beak δ15N values of all cephalopods from the stomach contents exceeded the δ15N values for the predator itself. Comparisons between different whale tissues of the same animal highlighted the importance of species- specific isotopic discrimination values to accurately evaluate foraging strategies. Toothed whales are good biological samplers for describing unknown cephalopod assemblages from meso- and bathypelagic water masses. Combined isotopic analysis of stomach contents with that of the predator highlighted whether oceanic cephalopods were likely to be a dominant prey item in their diet. Moreover, the importance of cephalopods as mid and higher order predators in the region and their role in transferring energy up the food chain was confirmed. However, evidence suggested that the toothed whales themselves were more generalist rather than specialist foragers. vii ACKNOWLEDGEMENTS I owe my sincere gratitude to many colleagues, friends and family for their support and help throughout the course of this study. Firstly I’d like to thank my amazing research supervisory team. Thanks especially to Dr Rosemary Gales who was very supportive throughout my study, providing assistance and samples to make this project possible. I’m very appreciative of the long hours in the field she spent to obtain the many samples. I’m also grateful to Dr Peter Nichols who was always supportive and ready to answer any questions (of which there were many). I’m also grateful to him for allowing me to use the lipid lab at CSIRO. My deepest thanks go to Dr Yves Cherel who guided and instructed me in the use of stable isotopes. I greatly appreciate his constructive criticism. I appreciate his willingness to help at all times and for helping with cephalopod beak identification. Last but not least I would like to thank Dr Patti Virtue who always encouraged and supported me throughout the project in whatever way possible. She was always there assuring me that it was possible, often going above and beyond that of a supervisor. I owe her my sincerest gratitude. The ANZ Holdsworth Wildlife Research Endowment and Winifred Violet Scott Charitable Trust funded this project and to which I am most grateful. I am also grateful to all the staff from the DPIPWE Princess Melikoff Marine Mammal Conservation Program who assisted throughout the project. This project was made possible by all your hard work and dedication. I’d like to give thanks to Isabel Beasley for her assistance with beak ID and measurements. A big thank you to Andrew Irvine and Rupert Davies for assistance in obtaining subsamples from the Taroona freezer. Thanks also to Steve O’Shea for assistance with beak identification. Special thanks must also go to captain (Brian Cooksley) and crew of the Adriatic Pearl who were extremely helpful and always went out of their way to collect squid specimens for the project. This project would not have been helpful without their assistance. A special thank you also to the captain and crew of the RV Tangoroa and Aurora Australis. Dr. Alan Williams identified the myctophids and I’m thankful for his time and effort in doing this. Graeme Ewing and Simon Willcox arranged and obtained some fish specimens for which I am most grateful. Over the years there have been many volunteers in sample viii collection, dissections and with whale strandings, a heartfelt thank you to all of you for the unselfish giving of your time. Your assistance greatly enhanced this project. Dr. Shapna Mazumder ran the stable isotope mass spectrometer at the University of Victoria, British Columbia. Thank you for your assistance and helpfulness. The use of the lab at Vancouver Island University was most appreciated. I am extremely grateful to Nicole Hellessey who did a wonderful job of making the maps for me, especially under time constraints. I would like to give a big thank you for the heartfelt love and support of my family. My children, Talisa, Adam and Levi have always
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