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Trophic Interactions of Marine Sponges

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Trophic Interactions of Marine Sponges Trophic Interactions of Marine Sponges Charlotte Lucy Mortimer A thesis submitted to the Victoria University of Wellington in fulfilment of the requirements for the degree of Doctor of Philosophy 2020 Thesis abstract Marine communities in the Anthropocene are changing rapidly with potentially severe consequences for ecosystem functioning. Recently, there has been increased interest in the ecological role of sponges, particularly on coral reefs, driven by evidence that sponges may be less affected by this period of environmental change than other benthic organisms. The Sampela reef system in the Wakatobi Marine National Park, Indonesia, is an example of a reef that has shifted to sponge dominance following a decline in hard corals and an increase in sponge density. Previous research suggests that the Sampela reef system may support a greater abundance of spongivorous fishes relative to surrounding reefs, however, uncertainties remain regarding spongivore identity and predated sponges. In addition, little is known about how shifts towards sponge dominance affect the trophic structure of reefs. The primary aim of my thesis was to investigate sponge trophic interactions to gain insight into the way sponge- dominated reefs of the future might function. This information is essential to predict the broader functional consequences of increasing sponge dominance on reefs in the Anthropocene. In my first data chapter, I measured the functional impact of spongivorous fishes by quantifying sponge biomass consumption on Wakatobi reefs. Video analysis identified 33 species from 10 families of reef fish grazing on Xestospongia spp., although 95% of bites were taken by only 11 species. Gut content analysis indicated that Pygoplites diacanthus and Pomacanthus imperator were obligate spongivores and Pomacanthus xanthometopon, Zanclus cornutus and Siganus punctatus regularly consumed sponges. In situ feeding observations revealed that sponges from the family Petrosiidae are preferred by P. diacanthus and Z. cornutus. Spongivores were estimated to consume 46.6 ± 18.3 g sponge 1000 m- 2 of reef day-1 and P. diacanthus had the greatest predatory impact on sponges. While estimates provided here are conservative and likely underestimate the true magnitude of spongivory on Indo- Pacific coral reefs, this chapter provides the first known estimate of reef wide sponge biomass consumption. Comparisons with published data estimating coral consumption by Chaetodontids in the Pacific suggests that biomass transferred through both pathways is similar in magnitude. Hence spongivory is an important, yet overlooked, trophic pathway on Indo-Pacific reefs. In my second data chapter, I developed genetic methods to identify sponges from the stomach contents of spongivorous angelfishes sampled in my first chapter. A range of primers and associated predator- blocking primers targeting the 18S rDNA gene were designed and tested on extracts of sponge and spongivore DNA. Sequences were successfully amplified from 14 sponges spanning 6 orders of Porifera, with the majority of samples identified belonging to the order Haplosclerida. This study is the first to successfully sequence sponges from the gut contents of spongivorous fishes. Sequence data indicated that Pygoplites diacanthus consumed sponges with considerable chemical defences and 3 exhibited significant dietary plasticity within the Porifera phylum, similar to observations of angelfishes in the Caribbean and the eastern Pacific. In my third data chapter, I used stable isotope analysis to investigate differences in consumer niche widths and trophic diversity on the sponge-dominated Sampela reef system in comparison to an adjacent, higher quality reef. I measured the stable isotope ratios of coral reef fish representing different functional feeding groups, prey items and basal carbon sources at both sites. I used isotope data to calculate the trophic position and isotopic niches of each species and performed interspecific and inter- site comparisons. The fish assemblage had a significantly lower mean trophic position at the sponge- dominated site and the majority of species had wider isotopic niches, in accordance with optimal foraging theory which supports expansion in niche widths when per capita prey is low. The fish assemblage sampled at the sponge-dominated site used a significantly lower range of resources, had lower trophic diversity and obtained more carbon from benthic production than fish from the higher quality reef site. Results indicate a simpler trophic structure at the sponge-dominated site characterised by fish with more similar diets. Whilst trophic niche expansion may facilitate population survival in the short term, it can be expected to lead to intensified competition for increasingly scarce resources. In my final data chapter, I investigated niche partitioning and organic matter contributions to co- occurring temperate sponges. I sampled the stable isotope ratios of five abundant sponge species at 10 m and 30 m at two sites at opposing ends of Doubtful Sound, Fiordland. I also used an ROV to opportunistically sample sponges at depths >50 m and measured stable isotope ratios of picoplankton (<2 µm size phytoplankton), the 2-200 µm fraction of the water column, macroalgae and terrestrial organic matter (TOM), and used isotope mixing models to estimate the contribution of carbon sources to sponge species. Sponges displayed a wide range of δ15N values spanning two trophic levels and spatial variation in sponge stable isotope ratios was not reflected by water column resources. There was a high degree of interspecific resource partitioning and comparisons of isotopic niche size suggested more diverse resource use at the Outer Fiord site for Axinella richardsoni, Cymbastela tricalyciformis and Raspailia topsenti. Surprisingly, isotopic mixing models indicated that picoplankton was not a significant carbon source for sponges, which could not be easily explained but may relate to the degradation of dissolved TOM by heterotrophic bacteria. This study found that differential use of the 2-200 µm fraction of the water column and macroalgal derived OM supports the majority of sponges in Fiordland. However, terrestrial production may support some sponges via microbial pathways where marine production is limited. In summary, species identity and angelfish foraging strategies in the Wakatobi Marine National Park were consistent with known global patterns of spongivory. Observations of feeding behaviour suggested that alternative trophic pathways involving sponge mucus or sponge detritus may also be important for 4 upper trophic levels. Low densities of spongivores at the Sampela reef system indicate that spongivores may not necessarily benefit from shifts to sponge-dominance that result in low diversity sponge assemblages dominated by one or two competitive species. Whilst sponge consumption may be an important and overlooked trophic pathway on Indo-Pacific reefs, observations from the Sampela reef system demonstrate that the range of trophic pathways originating from the base of the food web is important for maintaining trophic complexity. Hence, sponge-dominated reefs resulting from a decline in corals relative to sponges are less productive and ultimately less stable than coral-dominated reefs. 5 Acknowledgements I would like to thank my primary academic supervisor Professor James Bell for his guidance, for keeping me on track during challenging times and for putting up with me for a year longer than anticipated. Being one of James’ students has taken me to some wonderful places and I have treasured our research group field trips, which allowed me to learn new skills alongside some fantastic people. I would also like to thank my secondary academic supervisor Dr Matt Dunn for constructive feedback on my thesis and some great chats in the early stages of my PhD. Thanks also go to Sarah Bury for her invaluable technical expertise, emotional support and extensive and constructive feedback on my writing. I am very thankful for the Commonwealth Scholarship and the Victoria Doctoral Submission Scholarship which have funded me during my thesis. Thanks also go to the PADI Foundation for supporting the stable isotope research in Indonesia and to Prof. Jamal Jompa and Prof. Abdul Haris at Hasanuddin University for facilitating this research. Thanks to Operation Wallacea for their funding associated with my fieldwork in Indonesia, covering travel expenses, diving, food and accommodation. I would particularly like to thank Pippa and Ro for their hard work and effective management of the Hoga Island Research station, and to the Indonesian staff for being truly instrumental in the running of Hoga Island. I am indebted to the team at NIWA: Josette, Julie and Anna, who took me on as one of the team and spent their valuable time teaching me how to process stable isotope samples. Also, to the Department of Conservation team on the MV Southern Winds: Rich, Chris, Ross and Chloe, I cannot thank you enough for the diving, water sampling and the wonderful food that helped me to complete my final chapter. I owe a big debt of gratitude to Irina and Meg for their patience in teaching me molecular techniques and to Maren for helping me to troubleshoot PCR problems. To my sponge club compadres: Emily, Meg, Albi, Joe, Andy, Irina and Holly; some of the best memories I have from the past four years involve you. I could not have done it without your support, both in the field and in the pub. Finally, to my friends and family, without
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