Aerobic and behavioral flexibility allow estuarine gastropods to flourish in rapidly changing and extreme pH conditions

Abstract

Despite efforts to understand marine organismal responses to ocean acidification (gradual change in pH/ $${p_{{\text{C}}{{\text{O}}_2}}}$$ over decades), there is a lack of information about the capabilities of coastal organisms to endure rapid and extreme pH change (often full units within hours). We predicted that gastropods faced with estuarine acidification avoid extreme pH exposure through isolation and/or escape behavior, and energetically compensate for feeding and energy uptake limitations by facultative metabolic depression (FMD). To test this, we studied behavioral (organism activity) and aerobic (cardiac performance) responses to acidification in two closely related tropical intertidal species, the estuarine Indothais gradata (two populations) and the open-shore Reishia bitubercularis. Snails were exposed in the laboratory to either acutely declining or stable low pH conditions, using two acidification modes (HNO3-acidification and CO2-aeration). Under acutely declining pH, aerobic performance was regulated to unexpectedly low pH levels (4.5), effectively extending the field pH range for activity. This pH performance threshold marked the onset of behavioral isolation and FMD (as opposed to respiratory stress) and was lower in Indothais than Reishia snails during mineral acidification. Behavioral (in isolated gastropods) and environmental hypercapnic acidosis complicates interpretation of lowered metabolic performance. Stable reduced pH exposures resulted in different behavioral and physiological responses by the Indothais populations, including more prominent escape from water in the seaward population. Overall, these results suggest that aerobic and behavioral flexibility are crucial to organismal fitness in widely fluctuating pH circumstances. They further warn against overgeneralizing marine acidification consequences across physiological dispositions, taxonomic levels, and ecological systems.