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Front. Physiol. | doi: 10.3389/fphys.2018.01675

Distinct bleaching resilience of photosynthetic plastid-bearing mollusks under thermal stress and high CO2 conditions

 Gisela Dionisio1, 2*, Filipa Faleiro2,  Regina Bispo3,  Ana Lopes2,  Sonia Cruz1, Tiago Repolho2, Ricardo Calado1 and  Rui Rosa2, 4*
  • 1Centre for Environmental and Marine Studies CESAM, University of Aveiro, Portugal
  • 2Centro de Ciências do Mar e do Ambiente (MARE), Portugal
  • 3Instituto Superior de Psicologia Aplicada (ISPA), Portugal
  • 4Universidade de Lisboa, Portugal

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 analyse the impact of thermal stress (+4ºC) and high pCO2 conditions (∆pH=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 (Elysia 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).

Keywords: Climate Change, Bleaching, kleptoplasty, mollusk-plastid association, Photobiology, Oxidative Stress

Received: 01 Aug 2018; Accepted: 08 Nov 2018.

Edited by:

Gionata De Vico, Università degli Studi di Napoli Federico II, Italy

Reviewed by:

Folco Giomi, Università degli Studi di Padova, Italy
Marco Iammarino, Istituto Zooprofilattico Sperimentale di Puglia e Basilicata (IZSPB), Italy  

Copyright: © 2018 Dionisio, Faleiro, Bispo, Lopes, Cruz, Repolho, Calado and Rosa. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Gisela Dionisio, Centre for Environmental and Marine Studies CESAM, University of Aveiro, Aveiro, Portugal, gisela.dionisio@gmail.com
Dr. Rui Rosa, Universidade de Lisboa, Lisbon, Portugal, rrosa@fc.ul.pt