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Amanda S. Kahn Ecophysiology of glass sponge reefs by Amanda S. Kahn A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in ECOLOGY Department of Biological Sciences University of Alberta © Amanda S. Kahn, 2016 Abstract Suspension feeders are an important component of carbon exchange between the water column and the seafloor, a process called pelagic-benthic coupling. Sponges (Phylum Porifera) are filter feeders that consume especially small particles. They eat bacteria, which are inaccessible to most other filter feeders but which make up 10-30% of primary productivity. Feeding by sponges in shallow waters may have considerable effects on energy flow through ecosystems, especially in food-poor environments. This dissertation focuses on the ecophysiology of glass sponge (Porifera, Hexactinellida) reefs, one of the densest aggregations of sponges known in deep water, to determine the flow of energy through reefs and its underlying physiological mechanisms from the scale of the cell up to the ecosystem. Combined, the results explore the ecosystem functions of an important habitat on the northeast Pacific continental shelf and lend insight into the ecology of hexactinellids elsewhere in the world and in past oceans including the ancient sponge reefs in the Tethys Sea. Paired water samples collected in situ before and after passing through a sponge showed that reef sponges remove bacterial carbon and release ammonium into the water column. Stable carbon and nitrogen isotope signatures of reef sponges indicate that bacterioplankton came from both terrestrial and oceanic sources to differing degrees at different reefs, and possibly from bacteria associated with sediments. Microscopical investigation showed that reef sponges also released fecal pellets – aggregates that were 100 to 1000 times larger than the particles they consumed – thereby moving microbial food energy to the benthos as well. Glass sponge reefs have the highest grazing rate of any benthic suspension feeding community measured to date because of the high volumes of water they filter, their efficient removal of bacteria, and their sheer density and size. 13C-labeled bacteria fed to the sponges remained in the tissue for at least two weeks, suggesting that sponges retain and sequester carbon as biomass as well. Repeat visits to the same reef sites and same individual sponges over three years showed that reef- forming glass sponges have similar growth rates, recovery after damage, and recruitment rates ii to those of shallower water demosponge species. Study of cell and tissue production however showed conservative processes for tissue maintenance. Pieces of the reef species Aphrocallistes vastus were collected and newly forming nuclei labelled with the cell proliferation marker EdU. Very little proliferation occurred in mature regions of the body; most labeling occurred in growing (tip) regions of the sponge. Cell turnover rates were similar to those found in non- growing, mature regions of three shallow temperate sponge species (Sycon coactum, Spongilla lacustris, and Haliclona mollis). In general, sponges were found to vary rates of cell turnover depending on season, taxon, and life history stage suggesting an ability to modify energetic investment in tissue maintenance depending on environmental conditions. Most importantly, for demosponges at least, mature choanocytes – the pumping and feeding cell of sponges – were replaced not by direct replication as in colonial flagellates, but by immigration and differentiation of stem cells as in other animals. Light and electron microscopy showed that tissue and skeletal growth was localized to the growing regions at the tips of the glass sponge Aphrocallistes vastus. Choanoblasts – founder cells for flagellated chambers – first divided to form clusters, then produced enucleate collar bodies that expanded the flagellated chambers to their full size. Combined, the results presented here contribute to an understanding of the flow of energy through glass sponge reefs and the energetic requirements of reef sponges. Glass sponge reefs transfer from microbial food energy to the water column and the benthos through pelagic- benthic coupling, with food sources that can sustain their intense feeding and can fuel comparable growth rates to those of shallower species in food-rich habitats. Other glass sponge communities throughout the deep sea may share similar roles of pelagic-benthic coupling and, in their food-poor environment, act as localized oases of food energy. The tissue structure and tissue maintenance of syncytial glass sponges reflects adaptations to a low-food environment, and could also reflect the conditions in which sponges and other early animals evolved. iii Preface Chapter 2 has been published as Kahn, A. S., G. Yahel, J. W. F. Chu, V. Tunnicliffe, and S. P. Leys. 2015. Benthic grazing and carbon sequestration by deep-water glass sponge reefs. Limnology and Oceanography 60:78-88. GY, VT, and SPL designed the experiment, collected, and analyzed the raw data. Data from JWFC contributed unpublished data for analysis. GY, VT, SPL, and I did data analysis and contributed to the writing of the manuscript. Chapter 3 has been published as Kahn, A. S., L. J. Vehring, R. R. Brown, and S. P. Leys. 2015. Dynamic change, recruitment, and resilience in reef-forming glass sponges. Journal of the Marine Biological Association of the United Kingdom. 96(2):429-436. I led this paper’s direction and analysis. LJV, RRB, and SPL contributed to data collection. SPL obtained ship time and led the ROV dives to take time-series photos. SPL and I contributed to the writing of the manuscript. Chapter 4 will be submitted as a coauthored publication with Sally P. Leys (SPL; University of Alberta). SPL and I designed the project’s direction and analysis. I developed protocols, laboratory experiments, and statistical analyses. SPL and I contributed to the writing of the manuscript. Chapter 5 is collaborative work involving A.R. Bramucci, R. Case, J.W.F. Chu, and S.P. Leys (University of Alberta). SPL and I designed the study. ARB, RC, JWFC, SPL, and I collected sponges and isotope samples. JWFC, TR, and I processed samples for isotope analysis. I did all statistical analyses. SPL and I contributed to the writing of the manuscript. Chapter 6 has been submitted to the journal Invertebrate Biology as a coauthored publication (short communication) with S.P. Leys (University of Alberta). SPL and I collected sponge samples. I did all laboratory experiments and sampling processes. SPL and I interpreted the morphology, and we both contributed to writing the manuscript. iv Acknowledgments A wise thesis committee member told me, “You can’t go it alone in science” and it is extremely true. This research would not have developed to fruition without the support of many. Especially, my supervisor Sally Leys dedicated so much of her expertise, knowledge, insight, time, and personal care into my progress that I feel she is one of the few others who are as proud of this final product as I am. Rolf Vinebrooke and Rebecca Case served as excellent advisors as my thesis committee; I appreciate the depth that your diverse expertise brought to my project. I also thoroughly enjoyed my candidacy exam, where Sally, Rolf, Rebecca, Warren Gallin (who even agreed to come back for a thesis defense), and Marianne Douglas grilled me about my knowledge and as a result helped me realize the bigger picture of my research. I also appreciate my external examiner Marta Ribes for agreeing to evaluate my thesis in the midst of moving and for being willing to teleconference all the way from Spain. I also could not go it alone financially. I was primarily supported by the NSERC Vanier Canada Graduate Student Scholarship but also received support from the Faculty of Graduate Studies and Research, Department of Biological Sciences, Bamfield Marine Sciences Centre, Donald M. Ross Scholarship, the BMO Graduate Student Scholarship, and awards from the Society for Integrative and Comparative Biology and the World Sponge Conference. Sally also supported me in the final months of my program – yet another example of her commitment to my success. I value the interactions I had with all of my labmates. Pam Windsor Reid stands out as a valued, inspiring labmate and grounded friend. The others helped me get through the highs and lows of graduate school: Nathan Farrar with his love for music from the 90’s and his dismal attitude toward the future of science careers (which was so fun to argue!); Danielle Pendlebury’s incredible work ethic and our naan-eating, row-boating adventures in Bamfield; Rachel Brown’s snarky comments and foodie ways; Jasmine Mah’s empathy and her willingness to roll down grassy hills. I also thank the newbies, Lauren Law and Curtis Dinn, for their entertainment and support. Kristen Kruper helped in so many ways, with long days in Bamfield, long nights of staining and sectioning, and always with a compassionate ear and encouraging words. Research support and mentoring ranged from technical to emotional support. In Bamfield, Eric Clelland hands-down made much of my field work possible. Arlene Oatway was a constant source of knowledge and positive energy in the Microscopy Unit. George Braybrook, De-ann Rollings, and Nathan Gerein in the EAS SEM lab made all of the beautiful SEM micrographs in this thesis possible. Allan Harms at NRAL was indispensable for the isotope analyses done in this work. Tom Hantos provided access to a lyophilizer. v Several supportive friends also helped me in the field and in the lab. Nicole Webster especially was a loyal friend and an adroit colleague. Suz Anthony, Kat Anderson, Anna Bramucci, Paul Kirchberger, Leen Labeeuw, and all of my new friends from November Project offered sanity breaks and oftentimes field help throughout the thesis process. Thank you to the following mentees over the years: Kristen Kruper, Laura Vehring, Matthew Weigel, Stephanie Yu, Afyqah Kamarul-Zaman, Laura Vehring, and Laura Hamonic.
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