Abstract
The impact of temperature on photo-symbiotic relationships has been highly studied in the tropical reef-forming corals but overlooked in less charismatic groups such as solar-powered sacoglossan sea slugs. These organisms display one of the most puzzling symbiotic features observed in the animal kingdom, i.e., their mollusk-plastid association, which enables them to retain photosynthetic active chloroplasts (i.e., kleptoplasts) retrieved from their algae feed sources. Here we analyze the impact of thermal stress (+4°C) and high pCO2 conditions (ΔpH = 0.4) in survival, photophysiology (i.e., bleaching, photosynthetic efficiency, and metabolism) and stress defense mechanisms (i.e., heat shock and antioxidant response) of solar-powered sacoglossan sea slugs, from tropical (Elysia crispata) and temperate (E. viridis) environments. High temperature was the main factor affecting the survival of both species, while pH only affected the survival of the temperate model. The photobiology of E. viridis remained stable under the combined scenario, while photoinhibition was observed for E. crispata under high temperature and high pCO2. In fact, bleaching was observed within all tropical specimens exposed to warming (but not in the temperate ones), which constitutes the first report where the incidence of bleaching in tropical animals hosting photosynthetic symbionts, other than corals, occurs. Yet, the expulsion of kleptoplasts by the tropical sea slug, allied with metabolic depression, constituted a physiological response that did not imply signs of vulnerability (i.e., mortality) in the host itself. Although the temperate species revealed greater heat shock and antioxidant enzyme response to environmental stress, we argue that the tropical (stenotherm) sea slug species may display a greater scope for acclimatization than the temperate (eurytherm) sea slug. E. crispata may exhibit increased capacity for phenotypic plasticity by increasing fitness in a much narrower thermal niche (minimizing maintenance costs), which ultimately may allow to face severe environmental conditions more effectively than its temperate generalist counterpart (E. viridis).
Highlights
Kleptoplasty is an exciting research topic once it represents a unique naturally occurring biological condition, where chloroplasts can be found intra-cellularly within organisms phylogenetically distant from the algae host in which they evolved (Serôdio et al, 2014)
No significant differences were found between species (p = 0.152), FIGURE 1 | Effects of ocean warming and acidification on survival (%) of tropical E. crispata and temperate E. viridis species, under different climate change scenarios, i.e., control (18 and 26◦C, pH8.0); acidification (18 and 26◦C, pH7.6); warming (22 and 30◦C, pH8.0) and acidification + warming (22 and 30◦C, pH7.6) experimental treatments
In E. viridis, such increase was Certain habitats are subject to rapid fluctuations in physical characteristics across tidal cycles, where coastal sea slugs can be submitted to aerial emersion, FIGURE 4 | Effects of ocean warming and acidification on the tropical E. crispata and the temperate E. viridis species. (A) R – respiration and (B) NPP – net primary production under different climate change, i.e., control (18 and 26◦C, pH8.0); acidification (18 and 26◦C, pH7.6); warming (22 and 30◦C, pH8.0) and acidification + warming (22 and 30◦C, pH7.6) experimental treatments
Summary
Kleptoplasty is an exciting research topic once it represents a unique naturally occurring biological condition, where chloroplasts can be found intra-cellularly within organisms phylogenetically distant from the algae host in which they evolved (Serôdio et al, 2014). A decrease of 0.1 units in surface water pH was observed over the last decades, with projections indicating a further decrease between 0.14 and 0.42 units, by the end of the 21st century (Pörtner et al, 2014) Another result of the escalation of atmospheric partial pressure of carbon dioxide (pCO2) is the increase in global temperatures, with future projections estimating an increase of sea surface temperature (SST) of 3– 4◦C, by the end of the century (IPCC, 2013). Such future changes in ocean’s physical and chemical properties are expected to pose, to a more or less extent, biological restraints over marine biota (Kroeker et al, 2013). Tropical organisms are expected to be more vulnerable when faced upon future warming and acidification conditions, in comparison to all of those with temperate environments (Nilsson et al, 2009; Rosa et al, 2014)
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