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Reef Sharks: Recent Advances in Ecological Understanding to Inform Conservation

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Reef Sharks: Recent Advances in Ecological Understanding to Inform Conservation Chondrichthyan conservation in marine protected areas: Elucidating species associations in two chondrichthyan hotspots using non- invasive techniques by Geoffrey J. Osgood B.Sc., University of Calgary, 2014 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY in the Department of Biology © Geoffrey J. Osgood, 2020 University of Victoria All rights reserved. This dissertation may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. We acknowledge with respect the Lekwungen peoples on whose traditional territory the University stands and the Songhees, Esquimalt and WSÁNEĆ peoples whose historical relationships with the land continue to this day. ii Supervisory Committee Chondrichthyan conservation in marine protected areas: Elucidating species associations in two chondrichthyan hotspots using non- invasive techniques by Geoffrey J. Osgood B.Sc., University of Calgary, 2014 Supervisory Committee Dr. Julia Baum, Supervisor Department of Biology Dr. Francis Juanes, Member Department of Biology Dr. Verena Tunnicliffe, Member Department of Biology Dr. Joanna Mills Flemming, Outside Member Department of Mathematics and Statistics iii Abstract Chondrichthyans—sharks, rays, skates, and chimaeras—influence top down control of food webs and connect disparate ecosystems, yet populations of many species around the world have experienced sharp declines in abundance. Marine protected areas (MPAs) have a long history of conserving marine biodiversity, but their effectiveness to protect representative and critical habitat for threatened species on a global scale is controversial and hindered by a lack of biological and ecological data for the majority of chondrichthyan species. In this thesis, I use non-invasive baited remote underwater video (BRUV) and citizen science diver data to explore diverse chondrichthyan communities in two countries, South Africa and Costa Rica, with data- poor chondrichthyan fisheries and limit conservation funding, and the relationships of these chondrichthyans to biotic and abiotic factors in their habitats in and around MPAs. First, through a literature review, I find substantial taxonomic and geographic biases in understanding of reef shark biology, ecology, and conservation, which impair ability to implement effective conservation measures for these species. After identifying these research gaps, I used BRUVs to explore the diversity of a chondrichthyan hotspot in South Africa, finding many poorly understood endemic chondrichthyans. I discovered strong associations of the chondricthyan community to different habitat types (sand versus reef and kelp habitat), which resulted in poor diversity within one of the region’s larger MPAs—a whale sanctuary whose focus on large charismatic whales left mostly poorer quality sand habitat protected. However, a high occurrence of chondrichthyans within a neighbouring MPA suggested even small MPAs can conserve a high abundance of smaller species, especially if residency can be demonstrated. I then used the BRUV data to examine the relationships amongst these chondrichthyans and the community of other iv marine animals within the region, finding strong co-occurrence patterns that suggest chondrichthyans, particularly the endemic catsharks, could serve as effective ‘umbrella’ species for conservation in this region where little other information is available for conservation planning and monitoring. Finally, at Cocos Island, an MPA off Costa Rica, I discovered similarly strong, species-specific associations to another aspect of habitat: temperature. I found significant and species-specific responses to the El Niño–Southern Oscillation (ENSO). For example, the scalloped hammerhead Sphryna lewini counts declined by 224.7% during strong El Niño conditions and by 14.7% with just a 1°C rise in SST, while the benthic whitetip reef shark Triaenodon obesus had a weaker response, dropping by only 7.9% and 4.4%, respectively. In general, strong El Niño events reduced sightings within the MPA, providing some of the first indications of how a rising frequency and intensity of these events will impact the spatial distribution of both chondrichthyans and their habitat in the Eastern Tropical Pacific. Overall, this thesis provides insight into the factors influencing chondrichthyan abundance and diversity, demonstrating the importance of considering both biotic and abiotic factors during MPA design and the need to study these factors across diverse taxonomic groups and ecosystems. v Table of Contents Supervisory Committee ................................................................................................................ ii Abstract ......................................................................................................................................... iii Table of Contents .......................................................................................................................... v List of Tables ............................................................................................................................... vii List of Figures ............................................................................................................................. viii Acknowledgements ...................................................................................................................... xi Dedication ................................................................................................................................... xiv Chapter 1 – Introduction ............................................................................................................. 1 1.1 Marine protected areas as conservation tools .................................................................. 2 1.2 Chondrichthyans: marine predators in need of conservation ........................................ 6 1.3 Thesis overview ................................................................................................................... 9 Chapter 2 – Reef sharks: recent advances in ecological understanding to inform conservation ................................................................................................................................. 14 2.1 Abstract .............................................................................................................................. 15 2.2 Introduction ....................................................................................................................... 16 2.3 Methods .............................................................................................................................. 17 2.4 Reef shark diversity and overview of recent advances .................................................. 19 2.5 Habitats, movement, and home ranges ........................................................................... 24 2.6 Diets and trophic ecology ................................................................................................. 29 2.7 Genetics .............................................................................................................................. 31 2.8 Abundance ......................................................................................................................... 33 2.9 Threats ............................................................................................................................... 40 2.10 Conservation status ......................................................................................................... 41 2.11 Protecting reef sharks ..................................................................................................... 47 2.12 Future research needs..................................................................................................... 49 2.13 Conclusions ...................................................................................................................... 51 Chapter 3 – Using baited remote underwater videos (BRUVs) to characterize chondrichthyan communities in a global biodiversity hotspot ............................................... 53 3.1 Abstract .............................................................................................................................. 54 3.2 Introduction ....................................................................................................................... 55 3.3 Methods and materials ..................................................................................................... 59 3.3.1 Sampling design ........................................................................................................... 59 3.3.2 Baited remote underwater video (BRUV) design and analysis ................................... 62 3.3.3 Statistical analysis ........................................................................................................ 64 3.4 Results ................................................................................................................................ 66 3.4.1 Chondrichthyan frequency of occurrence and relative abundance .............................. 70 3.4.2 Chondrichthyan diversity ............................................................................................. 72 3.4.3 Chondrichthyan community composition .................................................................... 72 3.4.4 Overlap of habitat and protection
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