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Quantity discrimination in Port Jackson sharks incubated under elevated temperatures

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Abstract

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.

Significance statement

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.

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References

  • Agrillo C, Bisazza A (2014) Spontaneous versus trained numerical abilities. A comparison between the two main tools to study numerical competence in non-human animals. J Neurosci Methods 234:82–91

    Article  Google Scholar 

  • Agrillo C, Dadda M, Bisazza A (2007) Quantity discrimination in female mosquitofish. Anim Cogn 10:63–70

    Article  Google Scholar 

  • Agrillo C, Piffer L, Bisazza A (2011) Number versus continuous quantity in numerosity judgments by fish. Cognition 119:281–287

    Article  Google Scholar 

  • Agrillo C, Petrazzini MEM, Bisazza A (2014) At the root of math: numerical abilities in fish. In: Geary DC, Berch DB, Koepke KM (eds) Evolutionary origins and early development of number processing. Academic Press, London, pp 3–34

    Chapter  Google Scholar 

  • Amiel JJ, Shine R (2012) Hotter nests produce smarter young lizards. Biol Lett 8:372–374

    Article  Google Scholar 

  • Amiel JJ, Bao S, Shine R (2017) The effects of incubation temperature on the development of the cortical forebrain in a lizard. Anim Cogn 20:117–125

    Article  Google Scholar 

  • Bass NC, Mourier J, Knott NA, Day J, Guttridge T, Brown C (2016) Long-term migration patterns and bisexual philopatry in a benthic shark species. Mar Freshw Res 68:1414–1142. 1411

    Article  Google Scholar 

  • Boysen ST, Berntson GG, Mukobi KL (2001) Size matters: impact of item size and quantity on array choice by chimpanzees (Pan troglodytes). J Comp Psychol 115:106–110

    Article  CAS  Google Scholar 

  • Brown C (2012) Experience and learning in changing environments. In: Candolin U, Wong BB (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford, pp 46–62

    Chapter  Google Scholar 

  • Burt JM, Tinker MT, Okamoto DK, Demes KW, Holmes K, Salomon AK (2018) Sudden collapse of a mesopredator reveals its complementary role in mediating rocky reef regime shifts. Proc R Soc B 285(1883):20180553

    Article  Google Scholar 

  • Calosi P, Bilton DT, Spicer JI (2008) Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol Lett 4:99–102

    Article  Google Scholar 

  • Cano J, Nicieza A (2006) Temperature, metabolic rate, and constraints on locomotor performance in ectotherm vertebrates. Funct Ecol 20:464–470

    Article  Google Scholar 

  • Carazo P, Font E, Forteza-Behrendt E, Desfilis E (2009) Quantity discrimination in Tenebrio molitor: evidence of numerosity discrimination in an invertebrate? Anim Cogn 12:463–470

    Article  CAS  Google Scholar 

  • Chittka L, Geiger K (1995) Can honey bees count landmarks? Anim Behav 49:159–164

    Article  Google Scholar 

  • Clark BF, Amiel JJ, Shine R, Noble DWA, Whiting MJ (2014) Colour discrimination and associative learning in hatchling lizards incubated at ‘hot’ and ‘cold’ temperatures. Behav Ecol Sociobiol 68:239–247

    Article  Google Scholar 

  • 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 1029–1136

    Google Scholar 

  • Dayananda B, Webb JK (2017) Incubation under climate warming affects learning ability and survival in hatchling lizards. Biol Lett 13:20170002

    Article  Google Scholar 

  • Di Santo V (2016) Intraspecific variation in physiological performance of a benthic elasmobranch challenged by ocean acidification and warming. J Exp Biol 219:1725–1733

    Article  Google Scholar 

  • Di Santo V, Bennett WA (2011) Effect of rapid temperature change on resting routine metabolic rates of two benthic elasmobranchs. Fish Physiol Biochem 37:929–934

    Article  Google Scholar 

  • Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM (2010) Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243

    Article  Google 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 333:301–306

    Article  CAS  Google Scholar 

  • Fagan WF, Lewis MA, Auger-Méthé M, Avgar T, Benhamou S, Breed G, LaDage L, Schlägel UE, Tang WW, Papastamatiou YP, Forester J, Mueller T (2013) Spatial memory and animal movement. Ecol Lett 16:1316–1329

    Article  Google Scholar 

  • Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330

    Article  Google Scholar 

  • Geary DC, Berch DB, Koepke KM (2014) Evolutionary origins and early development of number processing. Academic Press, London

    Google Scholar 

  • Gervais C, Mourier J, Rummer J (2016) Developing in warm water: irregular colouration and patterns of a neonate elasmobranch. Mar Biodivers 46(4):743–744

    Article  Google Scholar 

  • Gervais C, Nay TJ, Renshaw G, Johansen JL, Steffensen JF, Rummer J (2018) Too hot to handle? Using movement to alleviate effects of elevated temperatures in a benthic elasmobranch, Hemiscyllium ocellatum. J Mar Biol 165:162

    Article  Google Scholar 

  • Hager MC, Helfman GS (1991) Safety in numbers: shoal size choice by minnows under predatory threat. Behav Ecol Sociobiol 29:271–276

    Article  Google Scholar 

  • Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210

    Article  Google Scholar 

  • Hunt S, Low J, Burns K (2008) Adaptive numerical competency in a food-hoarding songbird. Proc R Soc Lond B 275:2373–2379

    Article  Google Scholar 

  • Jones JC, Helliwell P, Beekman M, Maleszka R, Oldroyd BP (2005) The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. J Comp Physiol A 191:1121–1129

    Article  Google Scholar 

  • Jonson KM, Lyle JG, Edwards MJ, Penny RHC (1976) Effect of prenatal heat stress on brain growth and serial discrimination reversal learning in the guinea pig. Brain Res Bull 1:133–150

    Article  CAS  Google Scholar 

  • Krusche P, Uller C, Dicke U (2010) Quantity discrimination in salamanders. J Exp Biol 213:1822–1828

    Article  Google Scholar 

  • Last PR, Stevens JD (2009) Sharks and rays of Australia. CSIRO Publishing, Melbourne

    Google Scholar 

  • Laundré JW, Hernández L, Medina PL, Campanella A, López-Portillo J, González-Romero A, Grajales-Tam KM, Burke AM, Gronemeyer P, Browning DM (2014) The landscape of fear: the missing link to understand top-down and bottom-up controls of prey abundance? Ecology 95:1141–1152

    Article  Google Scholar 

  • Monteiro T, Vasconcelos M, Kacelnik A (2013) Starlings uphold principles of economic rationality for delay and probability of reward. Proc R Soc B 280:20122386

    Article  Google Scholar 

  • Munday PL, Kingsford MJ, O’Callaghan M, Donelson JM (2008) Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27:927–931

    Article  Google Scholar 

  • Nilsson GE, Crawley N, Lunde IG, Munday PL (2009) Elevated temperature reduces the respiratory scope of coral reef fishes. Glob Chang Biol 15:1405–1412

    Article  Google Scholar 

  • Nowicki JP, Miller GM, Munday PL (2012) Interactive effects of elevated temperature and CO2 on foraging behavior of juvenile coral reef fish. J Exp Mar Biol Ecol 412:46–51

    Article  Google Scholar 

  • Panteleeva S, Reznikova Z, Vygonyailova O (2013) Quantity judgments in the context of risk/reward decision making in striped field mice: first “count,” then hunt. Front Psychol 4:53

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Petrazzini MEM, Fraccaroli I, Gariboldi F, Agrillo C, Bisazza A, Bertolucci C, Foà A (2017) Quantitative abilities in a reptile (Podarcis sicula). Biol Lett 13:20160899

    Article  Google Scholar 

  • Pistevos JC, Nagelkerken I, Rossi T, Olmos M, Connell SD (2015) Ocean acidification and global warming impair shark hunting behaviour and growth. Sci Rep 5:16293

    Article  CAS  Google 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 411–484

    Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org

  • Rodda K, Seymour R (2008) Functional morphology of embryonic development in the Port Jackson shark Heterodontus portusjacksoni (Meyer). J Fish Biol 72:961–984

    Article  Google Scholar 

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    Article  CAS  Google Scholar 

  • Rosa R, Baptista M, Lopes VM, Pegado MR, Ricardo-Paula J, Trübenbach K, Leal MC, Calado R, Repolho T (2014) Early-life exposure to climate change impairs tropical shark survival. Proc R Soc B 281:20141738

    Article  Google Scholar 

  • Rosa R, Pimentel M, Galan JG, Baptista M, Lopes VM, Couto A, Guerreiro M, Sampaio E, Castro J, Santos C, Calado R, Repolho T (2016) Deficit in digestive capabilities of bamboo shark early stages under climate change. Mar Biol 163:60

    Article  Google Scholar 

  • Rugani R, Cavazzana A, Vallortigara G, Regolin L (2013) One, two, three, four, or is there something more? Numerical discrimination in day-old domestic chicks. Anim Cogn 16:557–564

    Article  Google Scholar 

  • Schluessel V (2015) Who would have thought that ‘jaws’ also has brains? Cognitive functions in elasmobranchs. Anim Cogn 18:19–37

    Article  CAS  Google 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

  • Szabo B, Noble DWA, Whiting MJ (2019) Context-specific response inhibition and differential impact of a learning bias in a lizard. Anim Cogn 22:317–329

    Article  Google Scholar 

  • Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633

    Article  Google Scholar 

  • 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 159–176

  • Vila Pouca C, Brown C (2018) Food approach conditioning and discrimination learning using sound cues in benthic sharks. Anim Cogn 21:481–492

    Article  Google Scholar 

  • Vila Pouca C, Brown C (2019) Lack of social preference between unfamiliar and familiar juvenile Port Jackson sharks Heterodontus portusjacksoni. J Fish Biol:1–7

  • Vila Pouca C, Gervais C, Reed J, Brown C (2018) Incubation under climate warming affects behavioral lateralisation in Port Jackson sharks. Symmetry 10:184

    Article  Google Scholar 

  • Wang X, Green DS, Roberts SP, de Belle JS (2007) Thermal disruption of mushroom body development and odor learning in Drosophila. PLoS One 2:e1125

    Article  Google Scholar 

  • Ward C, Smuts BB (2007) Quantity-based judgments in the domestic dog (Canis lupus familiaris). Anim Cogn 10:71–80

    Article  Google Scholar 

  • Wong B, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673

    Article  Google Scholar 

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Acknowledgments

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.

Funding

This research was funded by the Department of Biological Sciences at Macquarie University, and CVP was supported by an Endeavour Postgraduate (PhD) Scholarship.

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Authors and Affiliations

  1. Department of Biological Sciences, Macquarie University, Sydney, 2109, Australia

    Catarina Vila Pouca, Connor Gervais, Joshua Reed & Culum Brown

  2. AgroParisTech, 16 Rue Claude Bernard, F-75231, Paris, France

    Jade Michard

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  1. Catarina Vila Pouca
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Correspondence to Catarina Vila Pouca.

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The authors declare that they have no conflicts of interest.

Ethical approval

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.

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Communicated by S. D. Twiss

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Vila Pouca, C., Gervais, C., Reed, J. et al. Quantity discrimination in Port Jackson sharks incubated under elevated temperatures. Behav Ecol Sociobiol 73, 93 (2019). https://doi.org/10.1007/s00265-019-2706-8

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