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Simple Summary: Climate change has made bleaching events increasingly common in coral reefs. As such, scientists are rushing to better understand what will be the outcomes of bleaching on these tropical ecosystems. However, scientific focus is mostly being given to the direct impacts promoted by these events (e.g., mass mortality of corals, coral reef decay, community transitions), with indirect ones remaining largely overlooked (e.g., impacts on trophic interactions of highly specialized animals). Organisms directly affected by bleaching display a poorer nutritional value, but the effects this may have on their predators remain largely overlooked. To address this gap in scientific research, we advocate the use of the model predator–prey pair featuring the nudibranch sea slug Berghia stephanieae and its prey, the photosymbiotic glass anemone Exaiptasia diaphana. As the two species are already used as models in other research fields, one can build upon existing knowledge to determine if and how this highly specialized sea slug, that only preys upon glass anemones, is affected in terms of survival and reproductive fitness when only bleached prey are available. Moreover, this model pair will also allow investigating if such trophic effects cascade over consecutive generations, shaping populations and ultimately ruling species survival. 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. [ABSTRACT FROM AUTHOR]

Simple Summary: Some species of sacoglossan sea slugs are able to steal chloroplasts from the algae they feed on and maintain them functional for several months, a process termed "kleptoplasty". One of these photosynthetic slugs is Elysia crispata, found in coral reefs of the Gulf of Mexico. This sacoglossan inhabits different depths (0–25 m), being exposed to different food sources and contrasting light conditions. In this work, we characterized the pigment and fatty acid (FA) profiles, and quantified the total lipid, glycolipid and phospholipid contents of E. crispata from shallow (0–4 m) and deeper (8–12 m) waters, after a month of starvation to determine the longest and more stable retention of chloroplasts and its relation to habitat depth. Biochemical analyses allowed the identification of 12 photosynthetic pigments and 27 FAs. Heterogeneity in the composition of pigments confirmed the long-term retention of functional chloroplasts ingested from different algae. However, the differences found in pigment profile, total lipid content, and FA composition on individuals of E. crispata were not related to habitat depth. High amounts of glycolipids, exclusive chloroplast lipids, suggest a good condition of these photosynthetic organelles in animal cells. These results contribute baseline physiological data that may help explain evolutionary associations such as endosymbiosis. Long-term retention of functional chloroplasts in animal cells occurs only in sacoglossan sea slugs. Analysis of molecules related to the maintenance of these organelles can provide valuable information on this trait (kleptoplasty). The goal of our research was to characterize the pigment and fatty acid (FA) composition of the sea slug Elysia crispata and their associated chloroplasts that are kept functional for a long time, and to quantify total lipid, glycolipid and phospholipid contents, identifying differences between habitats: shallow (0–4 m) and deeper (8–12 m) waters. Specimens were sampled and analyzed after a month of food deprivation, through HPLC, GC-MS and colorimetric methods, to ensure an assessment of long-term kleptoplasty in relation to depth. Pigment signatures indicate that individuals retain chloroplasts from different macroalgal sources. FA classes, phospholipid and glycolipid contents displayed dissimilarities between depths. However, heterogeneities in pigment and FA profiles, as well as total lipid, glycolipid and phospholipid amounts in E. crispata were not related to habitat depth. The high content of chloroplast origin molecules, such as Chl a and glycolipids after a month of starvation, confirms that E. crispata retains chloroplasts in good biochemical condition. This characterization fills a knowledge gap of an animal model commonly employed to study kleptoplasty. [ABSTRACT FROM AUTHOR]

Simple Summary: Some sea slugs have evolved highly specialized feeding habits and solely prey upon a reduced number of species. This is the case of Berghia stephanieae, a sea slug that feeds exclusively on glass anemones, such as Exaiptasia diaphana. Glass anemones host photosynthetic microalgae that B. stephanieae ingest when preying upon E. diaphana. The association between these photosynthetic microalgae and sea slugs appears to be limited in time, particularly if B. stephanieae is deprived of prey hosting these microalgae. In the present study, we validate the use of a non-invasive and non-destructive approach that allows monitoring the persistence of this association in live sea slugs by measuring chlorophyll fluorescence. A complete loss of photosynthetic microalgae was observed within 8 days when animals were deprived of food or fed glass anemones with no microalgae (bleached anemones). As such, the association between B. stephanieae and photosynthetic microalgae acquired when preying glass anemones is not a true symbiosis. Future studies may use the technique here described to monitor the prevalence of the association between sea slugs and photosynthetic microalgae, particularly under bleaching events that will impair sea slugs to acquire microalgae by preying upon their invertebrate hosts. 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. [ABSTRACT FROM AUTHOR]