Quantity discrimination in Port Jackson sharks incubated under elevated temperatures
Ocean warming can induce physiological and behavioural effects in marine predators that can cascade through ecosystems. A lack of understanding of the effects of elevated temperature on shark behaviour remains an impediment to forecasting ecosystem-wide impacts. Port Jackson shark eggs were incubated and reared at current and projected end-of-century temperatures (+ 3 °C). We tested juvenile’s learning ability with a quantity discrimination task. The mortality rate of sharks reared in warm water was 41.7% compared with no mortality in the present-day sharks. Contrary to expectations, our results suggest that surviving hatchlings from the elevated-temperature group took fewer days to reach learning criterion and had a higher proportion of correct choice compared with hatchlings reared under present conditions. Additionally, this is the first data suggesting that sharks can discriminate different quantities. Our results seem to indicate that learning and behaviour might play a role in allowing elasmobranchs to overcome some of the deleterious effects of climate warming, but further research is needed to fully comprehend these findings.
The world’s oceans are warming at an unprecedented rate, which will impair development and alter physiological and behavioural traits in marine predators. Learning may play a leading role in allowing apex and mesopredators to adapt to a rapidly changing environment; however, no studies have tested the impacts of ocean warming in their learning abilities. We incubated and reared Port Jackson shark eggs at current and projected end-of-century temperatures (+ 3 °C). Contrary to expectations, surviving juveniles from the elevated-temperature group showed better learning performance, potentially adding learning ability to a growing list of traits that incubation temperature can modify during early development in marine predators. Our results were not entirely negative; it is possible that increased learning performance might allow apex and mesopredators to increase foraging efficiency and match increased energetic demands caused by elevated temperature.
KeywordsOcean warming Elasmobranchs Mesopredator Numerical learning Animal cognition
We thank the members and interns of The Fish Lab and staff at SIMS, in particular, Andrew Niccum, for husbandry and aquarium maintenance assistance. We also thank the two anonymous reviewers and editors whose suggestions helped improve and clarify this manuscript.
This research was funded by the Department of Biological Sciences at Macquarie University, and CVP was supported by an Endeavour Postgraduate (PhD) Scholarship.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Egg collection occurred under NSW Fisheries permit P08/0010-4.2. The experiments were approved by the Macquarie University Animal Ethics Committee (ARA 2016-027). All animals were euthanised at the end of the experiment with a lethal dose of MS-222 (tricaine methane-sulfonate; 1.5 g/L seawater) for brain anatomy studies.
- Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G (2013) Long-term climate change: projections, commitments and irreversibility. In: IPCC (ed) Climate change 2013 - the phsyical science basis. Cambridge University Press, Cambridge, pp 1029–1136Google Scholar
- Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet earth. Science 333:301–306CrossRefGoogle Scholar
- Geary DC, Berch DB, Koepke KM (2014) Evolutionary origins and early development of number processing. Academic Press, LondonGoogle Scholar
- Last PR, Stevens JD (2009) Sharks and rays of Australia. CSIRO Publishing, MelbourneGoogle Scholar
- Pörtner H-O, Karl DM, Boyd PW et al (2014) Ocean systems. In: climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. In: Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 411–484Google Scholar
- R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.orgGoogle Scholar
- Spedicato GA, Kang TS, Yalamanchi SB, Yadav D (2016) The markovchain package: a package for easily handling Discrete Markov Chains in R. https://cran.r-project.org/web/packages/markovchain/markovchain.pdf
- Van Der Kraak G, Pankhurst NW (1997) Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 159–176Google Scholar
- Vila Pouca C, Brown C (2019) Lack of social preference between unfamiliar and familiar juvenile Port Jackson sharks Heterodontus portusjacksoni. J Fish Biol:1–7Google Scholar