Effects of elevated temperature and eutrophication on tropical lagoon sponges

Coastal lagoons are important, but fragile ecosystems, which host diverse biological assemblages. However, these ecosystems are becoming increasingly exposed to anthropogenic stressors such as ocean warming and eutrophication. Sponges are important suspension feeders and are often important components of coastal lagoon communities. However, the impacts of anthropogenic stressors on lagoon-inhabiting sponges are poorly understood. This thesis examines the effects of elevated temperature and eutrophication on the physiological responses and temporal dynamics of three lagoon-inhabiting sponges, Neopetrosia chaliniformis, Amphimedon navalis and Spheciospongia vagabunda from Mauritius (western Indian Ocean). The effects of elevated temperature on A. navalis proteome dynamics and on the bentho-pelagic interactions of S. vagabunda were also explored.

In the first data chapter, I conducted a multifactorial experiment to investigate the short-term physiological responses of N. chaliniformis, A. navalis and S. vagabunda exposed to nine combinations of temperature and nitrate treatments for 14 days. Temperature treatments for this experiment were chosen based on the IPCC Representative Concentration Pathways, i.e. RCP6.0 (+2 oC) and RCP8.5 (+4 oC) projected for the year 2100. Nitrate concentrations were increased to approximately two- and three-fold the actual nitrate concentrations in the lagoons where sponges were collected. After 14 days of exposure, the photosynthetic pigment concentrations, and effective quantum yield of the two photosynthetic species (N. chaliniformis and S. vagabunda), as well as the buoyant weight of all species declined significantly. The gross photosynthetic rates and P:R ratios of N. chaliniformis and S. vagabunda also declined significantly, but the respiration rates of all species were significantly higher. The results from this chapter demonstrated that while lagoon-inhabiting sponges are susceptible to short term exposure to elevated temperatures, they are generally tolerant to elevated nitrate concentrations.

For my second data chapter, I conducted a four-week thermal tolerance experiment to investigate the physiological tolerance of these three sponges to elevated temperature. I also explored the proteomic responses of A. navalis to elevated temperature. The results showed that the physiology of N. chaliniformis and A. navalis were impacted over time, where after one-week of thermal exposure, both species experienced significant loss in buoyant weight and increases in pumping and holobiont oxygen consumption rates, respectively. In contrast, the bioeroding sponge S. vagabunda experienced an increase in buoyant weight over time and after a thermal exposure of two weeks, the effective quantum yield, pumping and holobiont oxygen consumption rates of this species appeared to stabilize, indicating the possible acclimation of this species to longer thermal exposure. A. navalis proteomic analysis after four weeks revealed significant changes in the expression of 50 proteins, which were mainly involved in oxidative stress, protein transport and cytoskeletal organization. These results demonstrate that medium- or long-term thermal experiments are more indicative of possible species-specificity and acclimation potential in sponges. Moreover, this study also demonstrates that thermal stress responses are also reflected at the proteome level and that a combination of physiology and proteomics can further enhance our understanding of stress mechanisms in sponges.

In my third data chapter, I aimed to assess the temporal variability in local distribution area (LDA), abundance and percentage cover of N. chaliniformis, A. navalis and S. vagabunda, respectively over a six- to eight-year period. I also aimed to explore the possible relationship between sea surface temperature (SST) and chlorophyll a (Chl a) concentration (used as a proxy for eutrophication), and temporal variability of these sponges. I found that while the LDA and percentage cover of N. chaliniformis decreased by 40.2% and 14.6%, those of S. vagabunda increased by 135.1% and 23.3%, respectively. No significant changes were observed in A. navalis LDA and percentage cover. A significant decline was seen in the abundance of N. chaliniformis and A. navalis, whereas a significant increase was noted for S. vagabunda abundance. N. chaliniformis and A. navalis abundance declines were likely due to a reduction in lagoonal coral cover, which often act as anchoring substrate for these sponges. The abundance of all species was significantly correlated with SST and Chl a concentration, but the nature of these correlations was species-specific. These results showed that lagoon-inhabiting sponges demonstrate species-specific temporal dynamics, which are mostly driven by changes in seawater temperature.

For my final data chapter, I aimed to estimate the bacterial cell consumption, Chl a uptake, net dissolved organic carbon uptake and net inorganic nutrient release of S. vagabunda when exposed to elevated seawater temperature. The results from this chapter indicated that the bacterial cell consumption and S. vagabunda bentho-pelagic interactions with the water column are relatively low compared to other shallow coastal sponges for which data are available. However, under future ocean warming scenarios RCP6.0 (+2 oC) and RCP8.5 (+4 oC), S. vagabunda bacterial cell consumption, net dissolved organic carbon uptake and net inorganic nutrient release would likely increase by 115% and 142%, respectively. These results suggest that thermally tolerant lagoon-inhabiting sponges would likely have an enhanced bentho-pelagic role in future anthropogenically-impacted lagoons, although based on current abundance, S. vagabunda has limited bentho-pelagic interactions with the water column.

In summary, the results presented in this thesis demonstrate that the responses of lagoon-inhabiting sponges to elevated temperature are species-specific. While some species are thermally susceptible to elevated temperature, other species such as S. vagabunda may have a potential to acclimate to at least short-term thermal stress. Consequently, thermally-tolerant species could potentially have an increasing bentho-pelagic role in coastal lagoons under future climate change scenarios. The impacts of thermal stress in sponges can also occur at the proteome level, where cellular biological functions such as redox reactions, protein transport and cytoskeletal organization are significantly disrupted. Furthermore, elevated temperature can equally contribute to the temporal variability of some lagoon-inhabiting sponge species. In contrast, this study demonstrated that lagoon-inhabiting sponges are most likely tolerant to eutrophication. Given that sponges are important components of coastal lagoons, it is critically important to assess and incorporate their potential roles to the ecological functioning of anthropogenically-impacted coastal lagoons.