Molecular, physiological, and organismal-level effects of thermal stress in corkscrew sea anemones Bartholomea annulata

Abstract

Changing ocean dynamics in the form of increasing seawater temperature are having drastic effects on the symbiotic relationships of coral reef cnidarians, causing them to bleach and die at increasing frequencies. Most research on thermotolerance in cnidarians revolves around the reef-building stony corals; much less information is available on the physiological effects of non-calcifying reef cnidarians such as the soft-bodied sea anemones. Despite the central ecological role of reef-building corals, it is important also to determine potential future effects of thermal stress on reef anemones, as these cnidarians may have major effects on tropical marine communities. On Caribbean coral reefs, corkscrew anemones Bartholomea annulata serve as hosts for Pederson’s cleaner shrimp, and provide visual cues for client fishes who approach them as cleaning stations to have their ectoparasites removed. This study aims to address gaps in our knowledge concerning whole-organismal processes, physiological functions, and molecular enzyme kinetics of corkscrew anemones in response to seawater temperature variability. The responses of this anemone species to temperature stress are described both under field conditions in the Florida Keys, and under laboratory conditions in aquarium cultures. In the field, the body size and microalgal characteristics of B. annulata varied with temperature, in that they were maximized at moderate temperatures, and exhibited reduced values indicating sublethal effects at extreme temperatures. Surface seawater temperature varied widely between winter (14°C) and summer (34°C) over 2 years in all 3 regions of the Keys examined. Chlorophyll concentration and microalgal abundance in anemone tentacles were significantly lower during summer in the Lower Keys than winter in the Middle and Upper Keys, indicating bleaching during the warmest season at the southernmost sites. Laboratory experiments revealed that anemone survival, body size, and microalgal abundance all decreased significantly at extreme temperatures, but increased within the optimal range of 22 - 25°C. Some individuals exposed to sublethal temperatures (18 or 32°C) later recovered after return to optimum, but those at < 14 or > 34°C all bleached and died. The effect of acclimation temperature was also studied at the physiological level and revealed that anemone respiration rate increases nearly linearly with temperature up to 32°C, while photosynthetic rate of symbiotic algae is maximal at only 22°C. This difference leads to a lower P:R ratio at higher temperatures, indicating a net loss of energy when compared to photosynthetic output. Temperature also significantly affected the potential metabolic activity measured via electron transport system activity, indicating that anemones at moderate reef temperatures are already operating at near maximal cellular levels. I conclude that these sea anemones experience seasonal thermal stress especially in the Lower Florida Keys during summer, when temperatures approach their upper lethal limit. Unbalanced energy budgets due to respiratory rate outpacing photosynthetic output at high temperatures may induce bleaching and subsequent loss of additional mutualistic benefits, leaving the anemone completely reliant on heterotrophic food sources. Florida Keys populations of B. annulata likely will decline under climate change, with consequences for reef fish health due to concurrent loss of their associated cleaner shrimp. Coral reef managers should focus on identifying at risk populations based on annual temperature regime and limit commercial harvest of this species during physiologically stressful summer months.