When warming hits harder: survival, cellular stress and thermal limits of Sparus aurata larvae under global change
- 438 Downloads
Understanding physiological and molecular compensation mechanisms that shape thermotolerance is crucial for estimating the effects of ocean warming on fish stocks, especially during early life stages, whose tolerance determines recruitment success and population viability. The aims of this study were to assess the sensitivity of fish larvae toward ocean warming and heat wave events in the commercial species, Sparus aurata, whose habitat is likely to be affected by rising water temperatures. We (1) estimated its critical thermal maximum (CTmax) and relative mortality upon warming, (2) quantified stress biomarkers: heat shock protein 70 kDa, total ubiquitin, antioxidant enzymes (superoxide dismutase, catalase, glutathione-S-transferase), lipid peroxidation and protein carbonylation, and (3) analyzed histopathological changes as a result of thermal stress. Larvae showed increasing levels of lethargy with increasing temperature, attaining a cumulative CTmax value of 30 °C. Relative mortality increased upon warming, reaching 80 % at 30 °C. Oxidative damage was higher at moderate temperatures and decreased at 24 °C probably due to a significant increase in superoxide dismutase’s (SODs) activity. Hsp70 chaperone levels also increased at 26 °C, but unfolding persisted at higher temperatures as shown by the increase in total ubiquitin at 26 and 28 °C, indicating protein damage. Skeletal muscle showed disorganization of muscle fibers from 24 °C onwards. Overall, protein denaturation seems to be the major cause of larval mortality, potentially compromising recruitment’s success from 22 °C onwards, since larvae migrate into nursery grounds by spring and summer (i.e., high temperatures), thus hindering the viability of local fish stocks. These data demonstrate that the biochemical homeostasis of fish can be disturbed within an ecologically realistic thermal range and emphasize the risks of rising global temperatures for larval fishes.
KeywordsHeat Wave Protein Carbonylation Coastal Lagoon Fish Stock Relative Mortality
The authors would like to thank Marta Martins, Ana Patrícia and Carolina Madeira for the help given in the maintenance of experimental systems and feeding of the organisms. Authors would like to thank MARESA for providing not only S. aurata larvae but also microalgae, rotifers and Artemia salina nauplii.
This study had the support of the Portuguese Fundação para a Ciência e a Tecnologia (FCT) (individual grants: senior researcher position to CV, SFRH/BPD/72564/2010 to PMC, SFRH/BD/80613/2011 to DM; Project Grants PTDC/MAR/119068/2010 and PTDC/MAR-EST/2141/2012; strategic Project Grants UID/Multi/04378/2013 and UID/MAR/04292/2013).
Compliance with ethical standards
Conflict of interest
We have no competing interests.
- Chícharo L, Teodósio MA (1991) Contribuição para o estudo do ictioplâncton do estuário do Guadiana. Rev Biol Univ Aveiro 4:277–286Google Scholar
- FAO (2015) Cultured Aquatic Species Information Programme. Sparus aurata. In: Colloca F, Cerasi S (eds) Fisheries and Aquaculture Department, Rome. http://www.fao.org/fishery/culturedspecies/Sparus_aurata/en. Accessed 6 Apr 2015
- Froese R, Pauly D (eds) (2006) Fish base. World Wide Web electronic publication. http://www.fishbase.org
- Fulda S, Gorman AM, Hori O, Samali A (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010:23. doi: 10.1155/2010/214074
- Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturicacid formation. J Biol Chem 246:7130–7139Google Scholar
- Houde ED (1989) Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87:471–495Google Scholar
- IPCC (2001) Third assessment report of the working group I. In: Houghton JT et al (eds) The science of climate change. Cambridge University Press, CambridgeGoogle Scholar
- IPCC (2007) Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, chap 3. Observations: surface and atmospheric climate change (section 3.8 Changes in extreme events). In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Cambridge University Press, CambridgeGoogle Scholar
- IPCC (2013) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Cambridge University Press, CambridgeGoogle Scholar
- IPCC (2014) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. In: Pachauri RK, Meyer LA (eds) Climate change 2014: synthesis report. IPCC, GenevaGoogle Scholar
- José R (2012) Sparus aurata larvae production in mesocosm: evaluation of abiotic and biotic parameters. Dissertation, University of Porto, PortugalGoogle Scholar
- Meyer E, Aglyamova GV, Matz MV (2011) Profiling gene expression responses of coral larvae (Acropora milepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol Ecol 20(17):3599–3616Google Scholar
- Miranda PMA, Coelho FES, Tomé AR, Valente MA, Carvalho A, Pires C, Pires HO, Pires VC, Ramalho C (2002) 20th century portuguese climate and climate scenarios, in climate change in Portugal. In: Santos FD, Forbes K, Moita R (eds) Scenarios, impacts and adaptation measures—SIAM project. Gradiva, Lisboa, pp 23–83Google Scholar
- Moretti A, Fernandez-Criado MP, Cittolin G, Guidastri R (1999) Manual on hatchery production of seabass and gilthead seabream, vol 1. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
- Peck MA, Huebert KB, Llopiz JK (2012) Intrinsic and extrinsic factors driving match–mismatch dynamics during the early life history of marine fishes. Adv Ecol Res 47:178–278Google Scholar
- Santos FD, Miranda P (eds) (2006) Climate change in Portugal: scenarios, impacts and adaptation measures—SIAM II project. Gradiva, LisboaGoogle Scholar
- Sola L, Moretti A, Crosetti D, Karaiskou N, Magoulas A, Rossi AR, Rye M, Triantafyllidis A, Tsigenopoulos CS (2007) Genetic effects of domestication, culture and breeding of fish and shellfish, and their impacts on wild populations: Gilthead seabream S. aurata. In: Svåsand T, Crosetti D, García-Vázquez E, Verspoor E (eds) Genetic impact of aquaculture activities on native populations, a European network (EU contract no. RICA-CT-2005-022802). Final scientific report, p 176. http://genimpact.imr.no/
- Suau P, Lopez J (1976) Contribution to knowledge of biology of Gilt-Head (S. aurata L.). Investig Pesq 40:169–199Google Scholar
- Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500Google Scholar
- Woodin SA, Hilbish TJ, Helmuth B, Jones SJ, Wethey DS (2013) Climate change, species distribution models, and physiological performance metrics: predicting when biogeographic models are likely to fail. Ecol Evol 3(10):3334–3346Google Scholar