Climate change and tropical sponges: The effect of elevated pCO₂ and temperature on the sponge holobiont

As atmospheric CO₂ concentrations rise, associated ocean warming (OW) and ocean acidification (OA) are predicted to cause declines in reef-building corals globally, shifting reefs from coral-dominated systems to those dominated by less sensitive species. Sponges are important structural and functional components of coral reef ecosystems, but despite increasing field-based evidence that sponges may be ‘winners’ in response to environmental degradation, our understanding of how they respond to the combined effects of OW and OA is limited. This PhD thesis explores the response of four abundant Great Barrier Reef species – the phototrophic Carteriospongia foliascens and Cymbastela coralliophila and the heterotrophic Stylissa flabelliformis and Rhopaloeides odorabile to OW and OA levels predicted for 2100, under two CO₂ Representative Concentration Pathways (RCPs). The overall aim of this research is to bridge gaps in our understanding of how these important coral reef organisms will respond to projected climate change, to begin to explore whether a sponge dominated state is a possible future trajectory for coral reefs.

To determine the tolerance of adult sponges to climate change, these four species were exposed to OW and OA in the Australian Institute of Marine Science’s (AIMS) National Sea Simulator (SeaSim) in a 3-month experimental study. The first data chapter explores the physiological responses of these sponges to OW and OA to gain a broad understanding of sponge holobiont survival and functioning under these conditions. In this chapter I also address the hypothesis that phototrophic and heterotrophic sponges will exhibit differential responses to climate change. In the second and third data chapters I explore the cellular lipid and fatty acid composition of sponges, and how these biochemical constituents vary with OW and OA. Lipids and fatty acids are not only vital energy stores, they form the major components of cell membranes, and the structure and composition of these biochemical constituents ultimately determines the integrity and physiological competency of a cell. Therefore through these analyses I aimed to determine how OW and OA affects the metabolic balance of sponges, and to understand mechanisms underpinning observed systemic sponge responses. Finally, to provide greater insight into the population level impacts of climate change on tropical sponges, in the last data chapter I explore the response of the phototrophic species Carteriospongia foliascens to OW/OA throughout its developmental stages.

I found that while sponges can generally tolerate climate change scenarios predicted under the RCP6.0 conditions for 2100 (30ºC/ pH 7.8), environmental projections for the end of this century under the RCP8.5 (31.5ºC/ pH 7.6) will have significant implications for their survival. Temperature effects were much stronger than OA effects for all species; however, phototrophic and heterotrophic species responded differently to OA. Elevated pCO₂ exacerbated temperature stress in heterotrophic sponges but somewhat ameliorated thermal stress in phototrophic species. Furthermore, sponges with siliceous spiculated skeletons resisted the RCP 8.5 conditions for longer than the aspiculate species. Biochemical analysis revealed that spiculated species also have greater cell membrane support features, which is likely to contribute to the observed stress tolerance. I also found that the additional energy available to phototrophic sponges under OA conditions may be used for investment into cell membrane support, providing protection against thermal stress. Finally, larval survival and settlement success of C. foliascens was unaffected by OW and OA treatments, and juvenile sponges exhibited greater tolerance than their adult counterparts, again with evidence that OA reduces OW stress for some of these life stages.

Based on the species studied here, this thesis confirms that sponges are better able to deal with OW and OA levels predicted for 2100 under RCP6.0, compared to many corals for which survival in a high CO₂ world requires OW to remain below 1.5°C. This suggests sponges may be future ‘winners’ on coral reefs under global climate change. However, if CO₂ atm concentrations reach levels predicted under RCP8.5, the prognosis for sponge survival by the end of this century changes as inter-species sponge tolerances to OW and OA differ. Under this projection it is likely we will also start to see a shift in sponge populations to those dominated by phototrophic sponges with siliceous spiculated skeletons. Overall, this thesis gives a holistic view of OW and OA impacts on tropical sponges and provides the basis from which to explore the potential for a sponge-coral regime shift in a high CO₂ world.

Bennett H., 2017. Climate change and tropical sponges: The effect of elevated pCO₂ and temperature on the sponge holobiont. PhD thesis, Victoria University of Wellington, 219 p. Thesis.

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