Assessing the Trophic Impact of Bleaching: The Model Pair Berghia stephanieae/Exaiptasia diaphana.

Bleaching events associated with climate change are increasing worldwide, being a major threat to tropical coral reefs. Nonetheless, the indirect impacts promoted by the bleaching of organisms hosting photosynthetic endosymbionts, such as those impacting trophic interactions, have received considerably less attention by the scientific community. Bleaching significantly affects the nutritional quality of bleached organisms. The consequences promoted by such shifts remain largely overlooked, namely on specialized predators that have evolved to prey upon organisms hosting photosynthetic endosymbionts and benefit nutritionally, either directly or indirectly, from the available pool of photosynthates. In the present study, we advocate the use of the model predator-prey pair featuring the stenophagous nudibranch sea slug Berghia stephanieae that preys upon the photosymbiotic glass anemone Exaiptasia diaphana to study the impacts of bleaching on trophic interactions. These model organisms are already used in other research fields, and one may benefit from knowledge available on their physiology, omics, and culture protocols under controlled laboratory conditions. Moreover, B. stephanieae can thrive on either photosymbiotic or aposymbiotic (bleached) glass anemones, which can be easily maintained over long periods in the laboratory (unlike photosymbiotic corals). As such, one can investigate if and how nutritional shifts induced by bleaching impact highly specialized predators (stenophagous species), as well as if and how such effects cascade over consecutive generations. Overall, by using this model predator-prey pair one can start to truly unravel the trophic effects of bleaching events impacting coral reef communities, as well as their prevalence over time.

Prevalence and Photobiology of Photosynthetic Dinoflagellate Endosymbionts in the Nudibranch Berghia stephanieae.

Berghia stephanieae is a stenophagous sea slug that preys upon glass anemones, such as Exaiptasia diaphana. Glass anemones host photosynthetic dinoflagellate endosymbionts that sea slugs ingest when consuming E. diaphana. However, the prevalence of these photosynthetic dinoflagellate endosymbionts in sea slugs appears to be short-lived, particularly if B.stephanieae is deprived of prey that host these microalgae (e.g., during bleaching events impacting glass anemones). In the present study, we investigated this scenario, along with food deprivation, and validated the use of a non-invasive and non-destructive approach employing chlorophyll fluorescence as a proxy to monitor the persistence of the association between sea slugs and endosymbiotic photosynthetic dinoflagellates acquired through the consumption of glass anemones. Berghia stephanieae deprived of a trophic source hosting photosynthetic dinoflagellate endosymbionts (e.g., through food deprivation or by feeding on bleached E. diaphana) showed a rapid decrease in minimum fluorescence (Fo) and photosynthetic efficiency (Fv/Fm) when compared to sea slugs fed with symbiotic anemones. A complete loss of endosymbionts was observed within 8 days, confirming that no true symbiotic association was established. The present work opens a new window of opportunity to rapidly monitor in vivo and over time the prevalence of associations between sea slugs and photosynthetic dinoflagellate endosymbionts, particularly during bleaching events that prevent sea slugs from incorporating new microalgae through trophic interactions.