Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warming
- 2.7k Downloads
Early life stages of many marine organisms are being challenged by climate change, but little is known about their capacity to tolerate future ocean conditions. Here we investigated a comprehensive set of biological responses of larvae of two commercially important teleost fishes, Sparus aurata (gilthead seabream) and Argyrosomus regius (meagre), after exposure to future predictions of ocean warming (+4 °C) and acidification (ΔpH = 0.5). The combined effect of warming and hypercapnia elicited a decrease in the hatching success (by 26.4 and 14.3 % for S. aurata and A. regius, respectively) and larval survival (by half) in both species. The length for newly-hatched larvae was not significantly affected, but a significant effect of hypercapnia was found on larval growth. However, while S. aurata growth was reduced (24.8–36.4 % lower), A. regius growth slightly increased (3.2–12.9 % higher) under such condition. Under acidification, larvae of both species spent less time swimming, and displayed reduced attack and capture rates of prey. The impact of warming on these behavioural traits was opposite but less evident. While not studied in A. regius, the incidence of body malformations in S. aurata larvae increased significantly (more than tripled) under warmer and hypercapnic conditions. These morphological impairments and behavioural changes are expected to affect larval performance and recruitment success, and further influence the abundance of fish stocks and the population structure of these commercially important fish species. However, given the pace of ocean climate change, it is important not to forget that species may have the opportunity to acclimate and adapt.
KeywordsOcean Acidification Early Life Stage Hatching Success Ocean Warming Elevated pCO2
We thank Maresa and CRIPSul for supplying fish eggs, and LusoReef, Oceanário de Lisboa and Aquário Vasco da Gama for supplying rotifers and microalgae.
Compliance with ethical standards
R.R. and M.S.P. designed the experiment; M.S.P. and G.D. performed the experiments; M.S.P., F.F., T.M., R.B., G.D., J.M., P.P.F. and R.R. analysed the data; M.S.P., F.F., T.M., R.B., G.D., A.M.F., J.M., M.P., H.P., E.J.G. and R.R. wrote the main paper. All authors discussed the results and their implications, and commented on the manuscript at all stages.
The Portuguese Foundation for Science and Technology (FCT) supported this study through doctoral grants to M.S.P. and G.D. (SFRH/BD/81928/2011 and SFRH/BD/73205/2010, respectively), a post-doc grant to F.F. (SFRH/BPD/79038/2011), and project grants to P.P.F. (AQUACOR-PROMAR31-03-05FEP-003) and R.R. (PTDC/MAR/0908066/2008 and PTDC/AAGGLO/3342/2012).
- Ahnelt H, Schade FM, Wegner M (2015) Ocean acidification leads to deformations of caudal vein angio‐architecture in juvenile threespine stickleback, Gasterosteus aculeatus Linnaeus. J. Fish DisGoogle Scholar
- Anderson JT (1988) A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J Northwest Atl Fish Sci 8:55–66Google Scholar
- Arias A (1980) Crecimiento, regimen alimentario y reproducción de la dorada (Sparus aurata L.) y del robalo (Dicentrarchus labrax L.) en los esteros de Cadiz. Investig Pesq 44:59–83Google Scholar
- Bromhead D, Scholey V, Nicol S, Margulies D, Wexler J, Stein M, Hoyle S, Lennert-Cody C, Williamson J, Havenhand J, Ilyina T, Lehodey P (2015) The potential impact of ocean acidification upon eggs and larvae of yellowfin tuna (Thunnus albacares). Deep Sea Res Part II 113:268–279CrossRefGoogle Scholar
- Collins M, Knutti R, Arblaster J, Dufresne J-L et al (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner G-K, Tignor M et al (eds) Climate Change 2013: The Physical Science Basis. Cambridge University Press, CambridgeGoogle Scholar
- Fernández I, Hontoria F, Ortiz-Delgado JB, Kotzamanis Y, Estévez A, Zambonino-Infante JL, Gisbert E (2008) Larval performance and skeletal deformities in farmed gilthead sea bream (Sparus aurata) fed with graded levels of Vitamin A enriched rotifers (Brachionus plicatilis). Aquaculture 283:10–115CrossRefGoogle Scholar
- Lewis E, Wallace DWR (1998) CO2SYS-Program developed for the CO2 system calculations. Carbon Dioxide Inf Anal Center, Report ORNL/CDIAC-105Google Scholar
- Maneja RH, Frommel AY, Browman HI, Clemmesen C, Geffen AJ, Folkvord A, Piatkowski U, Durif CMF, Bjelland R, Skiftesvik AB (2013a) The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2. Mar. BiolGoogle Scholar
- Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MCO, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. Proc Natl Acad Sci U S A 107:12930–12934Google Scholar
- Pousão-Ferreira P, Castanho S, Ribeiro L, Coutinho J, Bandarra NM, Mendes AC Larval rearing protocols for meagre Agyrosomus regius in LARVI’13 - Fish & shellfish larviculture symposium, Commun. Agric Appl Biol Sci, Laboratory of Aquaculture & Artemia Reference Center, Ghent University, Belgium. pp 378–381Google Scholar
- Quéro JC, Vayne JJ (1987) Le maigre, Argyrosomus regius (Asso, 1801) (Pisces, perciformes, sciaenidae) du golfe de Gascogne et des eaux plus septentrionales. Rev Trav Inst Pêches Marit 19(1985):35–66Google Scholar
- R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
- Ronnegard L, Shen X, Alam M (2010) hglm: a package for fitting hierarchical generalized linear models. R J 2:20–28Google Scholar
- Sanatamaría JA, Andrades JA, Herráez P, Fernández-Llebrez P, Becerra J (2005) Perinotochordal connective sheet of gilthead sea bream larvae (Sparus aurata, L.) affected by axial malformations: An histochemical and immunocytochemical study. Dev Biol 240:248–254Google Scholar
- Stanley RRE (2009) A biophysical study of connectivity in the early life history of coastal Newfoundland fishes. Memorial University of Newfoundland, St. John’sGoogle Scholar