Evaluating the resilience of Antarctic echinoderms to Southern Ocean freshening: Short- and long-term responses

Climate change is impacting marine ecosystems worldwide, presenting a significant threat to biodiversity. In the Southern Ocean, organisms are facing increasing challenges due to warming, ocean acidification, reduced sea-ice cover, and freshening—the reduction in salinity caused by freshwater input. Salinity is a crucial environmental factor that affects the development, growth, reproduction, and survival of aquatic organisms. While the effects of warming, acidification and loss of sea ice cover on Antarctic marine life have been widely studied, the impact of low salinity has been under-researched. Understanding the physiological impact of environmental stressors, such as freshening, is crucial for identifying species particularly vulnerable to change. This may be particularly important for animals which are considered to have poor osmoregulatory abilities, such as echinoderms which are strictly marine with no known freshwater species. In Antarctica, echinoderms are highly abundant and conspicuous, making up around 10‰ of benthic fauna. Many are endemic to Antarctica, having adapted to the low, stable temperature environment over millions of years. Climate change will likely increase the rate and frequency of hyposalinity events in Antarctica, where vast amounts of freshwater from melting glaciers and liquid precipitation rapidly enters coastal waters, diluting seawater. Over the longer-term, climate change is also expected to cause widespread net freshening over the whole Southern Ocean. For a group of animals adapted to a thermally stable and predictable environment, and with limited abilities to function in low-salinity conditions, echinoderms are potentially vulnerable to climate-change-induced freshening in Antarctica. However, little is known about their ability to tolerate acute, short-term reductions in salinity, and even less is understood about their capacity to acclimate to sustained low-salinity conditions. This thesis set out to assess the physiological and behavioural responses of common Antarctic echinoderms to low salinity exposure over both short- and long-term timeframes, in order to evaluate their vulnerability to present and future climate-change-induced freshening. An initial global literature review of echinoderms revealed inconsistencies in experimental approaches and descriptions of short- and long-term low salinity tolerance, making comparisons between species and regional groups challenging. To address this, a methodology was developed using the temperate echinoid Echinus esculentus, which showed distinct short- and long-term metabolic responses to low salinity. Experimental data demonstrated that E. esculentus could acclimate to moderate salinity reductions, with thresholds identified between 21‰ and 26‰. This approach was then applied to Antarctic echinoderms. Acute tolerance experiments revealed species-specific responses, with unexpected variations across habitats and class. Despite this variability, phylum-wide similarities were observed in oxygen consumption, activity rates, and osmotic strategy responses. The brittle star Ophionotus victoriae showed the lowest tolerance to salinity reductions, highlighting its vulnerability to freshening, while holothurians demonstrated remarkable tolerance, in particular Echinopsolus charcoti and Cucumaria georgiana. Long-term exposure studies on the echinoid Sterechinus neumayeri and asteroid Odontaster validus indicated successful acclimation to a mid-range salinity level (29‰) within their short-term tolerance range. However, at lower salinity (24‰), although survival rates remained high, physiological and behavioural responses failed to stabilise. Significant reductions in animal mass suggested that high catabolic tissue breakdown was necessary to maintain core homeostatic functions, with prolonged exposure likely leading to mortality. To understand the mechanistic basis of low salinity acclimation, a metabolomic approach was applied to tissue samples of S. neumayeri and O. validus from the long-term experiments. These analyses provided insights into the micromolecular adaptations of cold-temperature-adapted echinoderms and their strategies for low salinity acclimation. In particular, the osmolyte profile in both species differs from temperate echinoderms and other marine invertebrates, with branched-chain amino acids (valine, leucine, and isoleucine) potentially acting as both compatible osmolytes, cryoprotectants and even an energy reserve. Overall, this thesis demonstrates that Antarctic echinoderms are capable of short-term resilience to moderate salinity reductions, with certain species showing remarkable tolerance and varying levels of acclimation capacity. This acclimation potential may provide partial resilience to predicted climate change-induced freshening. However, their long-term acclimation potential is limited, and species-specific vulnerabilities highlight the need for further research. The study also reveals that unique adaptations, such as specific osmolyte profiles, may influence their survival and ability to cope with future environmental changes. These insights highlight the need for ongoing research into Antarctic echinoderms and other marine organisms to understand their physiological limitations, which is crucial for developing targeted conservation strategies to mitigate the impacts of future freshening and environmental changes on their survival.

Natural Environment Research Council C-CLEAR PhD studentship (grant number NE/S007164/1).