Living costs of ocean acidification and warming in herbivorous gastropods and their adaptations

Over the last century, atmospheric concentration of carbon dioxide (pCO₂) has been increasing at an unprecedented rate due to anthropogenic CO₂ emission. The elevated pCO₂ is predicted to cause substantial abiotic changes in future marine ecosystems, including ocean acidification and warming. In addition, extreme climatic events, such as heatwaves, will become more prevalent and persistent due to global warming. Thus, extensive studies have been conducted to determine how ocean acidification and warming affect marine organisms. It is generally considered that these climate change stressors will cause adverse effects on many marine organisms and hence disrupt ecosystem functioning in future. This prediction is, however, largely based on short-term experiments with simple experimental design that may have overestimated the impacts of climate change stressors. In fact, growing evidence shows that some marine organisms can acclimate to the predicted seawater conditions. Therefore, this thesis aims to examine the impacts of ocean acidification and warming on marine organisms and their potential adaptations. Herbivorous gastropods from intertidal to subtidal zones were chosen as the study animals in view of their substantial contribution to herbivory in their habitat. Ocean acidification and warming can raise the energy demand of marine organisms, impacting their energy budget and ultimately survival. After a prolonged exposure period, I found that ocean acidification has limited effect on the energy budget and survival of subtidal gastropods (Thalotia conica and Phasianella australis), suggesting that they are able to cope with the elevated energy demand under ocean acidification. This response can be mediated indirectly by the positive effect of CO₂ enrichment on the nutritional quality (energy content and C:N ratio) of primary producers, which in turn boosts the energy gain of gastropods. In contrast, I found that ocean warming reduces the energy budget, growth and survival of these subtidal gastropods at temperature below their thermal tolerance, implying that prolonged exposure to sublethal thermal stress (e.g. persistent heatwaves) can already threaten their populations.

While ocean acidification and warming enhanced the nutritional quality of primary producers, such indirect positive effect was shown to be outweighed by their combined direct negative effects on the energy budget of gastropods, culminating in energy depletion and mortality. Compared to subtidal gastropods, intertidal gastropods are considered to be more resistant to ocean acidification and warming in view of the large environmental fluctuations in their habitat, which make them have greater acclimation capacity through behavioural and physiological adaptations. Yet, their fitness and survival may still be challenged by the abrupt increase in temperature to an extreme level during heatwaves. I showed that intertidal gastropods (Nerita atramentosa, Austrocochlea concamerata and Austrocochlea constricta) are able to exhibit adaptive behaviour (e.g. hiding) during heatwaves so that their body temperature can be maintained within their survivable range. Furthermore, their molecular defence mechanisms (e.g. production of heat shock proteins and antioxidative enzymes) were found to be activated to alleviate the impacts of heatwaves so that they can resist (N. atramentosa) or recover (A. concamerata) from thermal stress. Since heatwaves are mostly transient, these adaptive behavioural and physiological responses probably allow intertidal gastropods to maintain their populations and ecological functions in their habitat. Calcification is predicted to be hindered by ocean acidification due to the reduced pH and carbonate saturation state of seawater, which can weaken shell mechanical strength. Contrary to this prediction, I found that ocean acidification has limited effect on the shell hardness of both intertidal (N. atramentosa and A. constricta) and subtidal gastropods (Austrocochlea odontis, Turbo undulatus, Bulla quoyii, T. conica and P. australis). Instead, ocean warming resulted in the production of softer shells in some subtidal gastropods (T. undulatus, B. quoyii and P. australis). Moreover, all the tested subtidal gastropods produced aragonite as the only carbonate mineral, which is more soluble than calcite. In contrast, a bimineralic intertidal gastropod (A. constricta) could reduce shell solubility by increasing precipitation of calcite under ocean acidification, which also minimizes the energy cost of calcification and allows faster shell growth. This finding suggests that calcification is primarily governed by energy budget rather than seawater carbonate chemistry. Overall, subtidal gastropods would be more vulnerable than intertidal gastropods to physical damage and shell dissolution in future marine ecosystems. In conclusion, I demonstrated both positive and negative responses of herbivorous gastropods to ocean acidification and warming, where warming could trigger detrimental effects on the energy budget, calcification and survival of subtidal gastropods. In contrast, intertidal gastropods appeared to be robust to ocean acidification and warming, probably attributed to their adaptive responses (e.g. behavioural and physiological adaptations). Based on the findings in this thesis, the populations of subtidal gastropods and their ecological contributions would be undermined by climate change stressors, possibly leading to serious repercussions on the future subtidal environment, such as disrupted trophic dynamics and modifications in habitat structures.

Leung J. Y. S., 2018. Living costs of ocean acidification and warming in herbivorous gastropods and their adaptations. PhD thesis, University of Adelaide. Thesis (restricted access).

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