Fish Transgenerational adaptative Strategies to ocean acidification and warming
Oceanography
Final Report Abstract
Designed to address key shortcomings that existed in the research on ocean acidification and warming (OAW) nearly a decade ago, FITNESS was the first long-term study to keep a large, economically important fish species (European seabass, Dicentrarchus labrax) for the full course of several generations (8 years) under defined conditions of OAW. Crossfactorial OAW conditions included two fluctuating temperatures (ambient and ambient + 5°C) and 3 PCO2 levels (650 (ambient), 1200 and 1700 µatm CO2). FITNESS performed several long-term experiments that allowed measurements to be made on all life stages (embryos, larvae, juveniles and adults). Importantly, FITNESS was designed to compare OAW responses among the F0 and F1 generation of parental fish that had undergone exposure to OAW and offspring of natural (wild) broodstocks. The research conducted in FITNESS represented a more holistic assessment of acclimation and adaptation capacity to OAW to specifically address i) the integration of cellular, tissue and organismal responses, and ii) the transgenerational adaptive capacity (genetic, transgenerational effects) of organisms with complex (long) life cycles, particularly fish. This was an ambitious and ground breaking project that was made more challenging due to financial cut-backs. The project was originally submitted and reviewed as a joint DFG-ANR bilateral application. Additionally, a fire in the rearing facilities caused a delay in a long-term experiment and the F0 generation matured more slowly than anticipated, delaying planned experiments on the F1 generation. Nonetheless, the FITNESS team consisting of the two German PIs and their French colleagues (formerly formal project partners), two PhD students and several post doctoral fellows, Master and Bachelor students, managed to rear European seabass in several OAW conditions from 2 days post-hatch to adulthood, including several spawning events, amongst others producing an F1 generation with fully documented parental OAW history. Information obtained from these long-term experiments, performed on several generations on a relatively long-lived fish, advanced the field in several aspects. Various measures at the cellular, tissue and organismal levels indicated generally good acclimation capacities of juveniles and adults to OAW but a higher sensitivity of larvae, especially to the combination of the two drivers (warming and acidification). Interestingly, while F1 juveniles showed the best growth in the warm scenario and, thus, appeared to profit from increasing temperatures, F1 larvae appeared more sensitive to those same conditions, which may lead to further repercussions over successive generations. These results underscore the importance of including phenology and ontogeny in climate change studies to be able to identify long-term bottlenecks for the survival of a population. Finally, we were also able to show that nutrition and food availability is a central driver in setting climate change resilience - especially in the warm life condition scenarios, food availability defines the severity of the antagonistic effects of warming and acidification. The basis for this lies far beyond food availability alone, though, we found that the underlying digestive and metabolic capacities, as well as the metabolome as such, react towards OAW in the long run and lead to effects not discernible in short term studies. The results of FITNESS are not only of importance to the scientific community working on climate change effects, but also have a high value for application in aquaculture. Specifically the identification of physiological limits and life stage specific bottlenecks will be able to assist in making commercial fish farming resilient towards future climate change in European waters. FITNESS exemplifies the long-term commitment needed by the scientific community and funders of research programs to enable gathering information and providing the best possible advice to decision makers on the transgenerational adaptive capacity of long-lived fishes and other marine species to ongoing ocean acidification and warming.
Publications
- (2017) Effects of warming rate, acclimation temperature and ontogeny on the critical thermal maximum of temperate marine fish larvae. PLoS ONE
Moyano, M.; Candebat, C.; Ruhbaum, Y.; Álvarez-Fernández, S.; Claireaux, G.; Zambonino-Infante, J.-L. and Peck, M.A.
(See online at https://doi.org/10.1371/journal.pone.0179928) - (2019): Combined effects of ocean acidification and temperature on larval and juvenile growth, development and swimming performance of European sea bass (Dicentrarchus labrax). PLOS One, 14, e0221283
Cominassi, L.; Moyano, M.; Claireaux, G.; Howald, S.; Mark, F. C.; Zambonino-Infante, J. L.; Quazuguel, P.; Le Bayon, N. and Peck, M. A.
(See online at https://doi.org/10.1371/journal.pone.0221283) - (2019): Future ocean warming may prove beneficial for the northern population of European seabass, but ocean acidification does not. Journal of Experimental Biology 222, jeb213017
Howald, S.; Cominassi, L.; LeBayon, N.; Claireaux, G. and Mark, F.C.
(See online at https://doi.org/10.1242/jeb.213017) - (2020): Food availability modulates the combined effects of ocean acidification and warming on fish growth. Scientific Reports, 10, 2338
Cominassi, L.; Moyano, M.; Claireaux, G.; Howald, S.; Mark, F. C.; Zambonino-Infante, J. L. and Peck, M. A.
(See online at https://doi.org/10.1038/s41598-020-58846-2) - (2021) Effect of long-term intergenerational exposure to ocean acidification on ompa and ompb transcripts expression in European seabass (Dicentrarchus labrax). Mar Env Res, 170:105438
Mazurais, D., Neven, C., Servili, A., Madec, L., Collet, S., Zambonino-Infante, J., Mark, F.C.
(See online at https://doi.org/10.1016/j.marenvres.2021.105438) - (2022) Effects of ocean acidification over successive generations decrease resilience of larval European sea bass to ocean acidification and warming but juveniles could benefit from higher temperatures in the NE Atlantic. Journal of Experimental Biology 225(9), jeb243802
Howald, S.; Moyano, M.; Crespel, A.; Kuchenmüller, L.; Cominassi, L.; Claireaux, G.; Peck, M.A. and Mark, F.C.
(See online at https://doi.org/10.1242/jeb.243802) - (2022) The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance. BMC Genomics, 23: 448
Cohen-Rengifo, M.; Danion, M.; González, A.-A.; Begout, M.-L.; Cormier, A.; Noël, C.; Cabon, J.; Vitré, T.; Mark, F.C.; Mazurais, D.
(See online at https://doi.org/10.1186/s12864-022-08647-w)
