An integrated approach to assess pupping areas and natal origins in a Conservation Dependent shark, Galeorhinus galeus Matthew N. McMillan Presented for the degree of Doctor of Philosophy School of Biological Sciences The University of Adelaide September 2018 i For Grandad. ii Declaration I, Matthew McMillan, certify that this work contains no material which has been accepted for the award of any other degree or diploma in my name, in any university or other tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference has been made in the text. In addition, I certify that no part of this work will, in the future, be used in a submission in my name, for any other degree or diploma in any university or other tertiary institution without the prior approval of the University of Adelaide and where applicable, any partner institution responsible for the joint- award of this degree. I acknowledge that copyright of published works contained within this thesis resides with the copyright holder(s) of those works. I also give permission for the digital version of my thesis to be made available on the web, via the University’s digital research repository, the Library Search and also through web search engines, unless permission has been granted by the University to restrict access for a period of time. I acknowledge the support I have received for my research through the provision of an Australian Government Research Training Program Scholarship. Matthew N. McMillan 25 September 2018 Cover image: A pregnant school shark Galeorhinus galeus with a PSAT tag prior to release by the author, South Australia. iii Table of Contents Declaration.................................................................................................................................... iii Abstract ......................................................................................................................................... vi Acknowledgements .................................................................................................................... viii CHAPTER 1: General introduction............................................................................................ 9 Thesis aims and scope ............................................................................................................... 18 References ................................................................................................................................. 22 CHAPTER 2: Elements and elasmobranchs: Hypotheses, assumptions, and limitations of elemental analysis........................................................................................................................ 25 Statement of Authorship............................................................................................................ 26 Appendix II.A: Supplementary material ................................................................................... 65 Part I. Consistency of elemental signals and bleaching effects on vertebrae ........................ 65 Part II. Exploratory comparisons of elasmobranch vertebrae and otoliths ............................ 71 References ................................................................................................................................. 72 CHAPTER 3: Natural tags reveal populations of Conservation Dependent school shark use different pupping areas .............................................................................................................. 73 Statement of Authorship............................................................................................................ 74 Appendix III.A: Supplementary material .................................................................................. 87 CHAPTER 4: When to leave home? Constraints on shark pup dispersal from pupping areas ............................................................................................................................................. 89 Statement of Authorship............................................................................................................ 90 Abstract ..................................................................................................................................... 93 Introduction ............................................................................................................................... 94 Materials and methods .............................................................................................................. 96 Results ..................................................................................................................................... 100 iv Discussion ............................................................................................................................... 107 References ............................................................................................................................... 112 CHAPTER 5: Stay warm, travel cool: Partial female migration and cool-water migration pathways in an overfished shark ............................................................................................. 117 Statement of Authorship.......................................................................................................... 118 Appendix V.A: Supplementary material ................................................................................. 131 CHAPTER 6: General discussion ........................................................................................... 137 Future directions for research .................................................................................................. 148 Conservation implications ....................................................................................................... 149 Conclusions ............................................................................................................................. 151 References ............................................................................................................................... 152 v Abstract Knowledge around reproductive movements and habitat use can be central to understanding the life histories of animal populations. Such knowledge can be especially important for managing recovery of populations depleted by human over-exploitation and habitat degradation. In marine environments, clarifying animal movements and habitat use can be difficult given the practical and logistical constraints of studying them. For my research I therefore integrate diverse techniques to cast light on reproductive movements and habitat use of the Conservation Dependent school shark Galeorhinus galeus, where conventional methodologies have left important knowledge gaps unanswered. A national rebuilding plan for the species highlighted a lack of knowledge around whether all female G. galeus migrate to historically identified pupping areas around Tasmania and Bass Strait in the south-eastern range of the species as current management assumes. Alternatively, reproductive movements and habitats may be more varied in extent and location, including pupping areas in South Australia to the northwest where aggregations of pregnant females occur. My overarching aim was to assess the spatial distribution of G. galeus pupping areas in southern Australia and the extent of shared natal origins among populations. I use: (1) element signatures in calcified shark vertebrae that derive from water chemistry and diet in birth areas as natural tags to test whether sharks from different populations recruit from common or different pupping areas, (2) energetic analyses to assess constraints on pup dispersal from pupping areas and whether pups caught in South Australia could feasibly have dispersed from known pupping areas around Tasmania and Bass Strait, and (3) satellite archival tags to track movements of pregnant G. galeus tagged in South Australia to assess pupping movements and the spatial distribution of likely pupping areas. My findings increase our knowledge of the extent and plasticity of reproductive movements and areas used by G. galeus and address several assumptions, on which current management is based, that conventional techniques such as mark-recapture studies and genetic investigations had left open to speculation. A review of elasmobranch vertebral chemistry analysis and ground-truthing laboratory experiments establish the utility of shark vertebrae as sources for natural tags. Element signatures were consistent among related time-resolved portions of the same and adjacent vertebrae, while vi commonly used bleach preparation did not affect element signatures for a range of elements, validating use of elasmobranch vertebrae as biogenic archives for microchemistry analyses. Post-natal element signatures from three cohorts of juvenile and sub-adult G. galeus were compared between populations in South Australia and Bass Strait. Signatures differed among populations, indicating use of different pupping areas and not supporting the previous assumption of uniform female migrations to common pupping areas. Bioenergetic analyses established an energy budget and assessed constraints on dispersal of G. galeus pups from pupping areas. High energetic costs of growth, small energy reserves, and low concentrations of energy storage lipids relative to adults indicated a trade-off