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Ghosts of thermal past: reef fish exposed to historic high temperatures have heightened stress response to further stressors

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Abstract

Individual exposure to stressors can induce changes in physiological stress responses through modulation of the hypothalamic–pituitary–interrenal (HPI) axis. Despite theoretical predictions, little is known about how individuals will respond to unpredictable short-lived stressors, such as thermal events. We examine the primary neuroendocrine response of coral reef fish populations from the Îles Eparses rarely exposed to anthropogenic stress, but that experienced different thermal histories. Skunk anemonefish, Amphiprion akallopisos, showed different cortisol responses to a generic stressor between islands, but not along a latitudinal gradient. Those populations previously exposed to higher maximum temperatures showed greater responses of their HPI axis. Archive data reveal thermal stressor events occur every 1.92–6 yr, suggesting that modifications to the HPI axis could be adaptive. Our results highlight the potential for adaptation of the HPI axis in coral reef fish in response to a climate-induced thermal stressor.

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References

  • Angelier F, Wingfield JC (2013) Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. Gen Comp Endocrinol 190:118–128

    Article  CAS  PubMed  Google Scholar 

  • Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525

    Article  CAS  PubMed  Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26

    Article  Google Scholar 

  • Busch DS, Hayward LS (2009) Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv 142:2844–2853

    Article  Google Scholar 

  • Casey KS, Brandon TB, Cornillon P, Evans R (2010) The past, present and future of the AVHRR Pathfinder SST Program. In: Barale V, Gower JFR, Alberotanza L (eds) Oceanography from space, revisited. Springer, Dordrecht, pp 323–341

    Google Scholar 

  • Chabanet P, Bigot L, Naim O, Garnier R, Moyne-Picard M (2002) Coral reef monitoring at Reunion Island (Western Indian Ocean). Proc 9th Int Coral Reef Symp 2:873–878

    Google Scholar 

  • Conand C, Chabanet P, Quod JP, Bigot L (1998) Suivi de l’état de santé des récifs coralliens du S-O de l’Océan Indien. Manuel méthodologique Programme Régional Environnement COI 27

  • Donelson JM, Munday PL, McCormick MI, Nilsson GE (2011) Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish. Glob Chang Biol 17:1712–1719

    Article  Google Scholar 

  • Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32

    Article  Google Scholar 

  • English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Townsville, Australia

    Google Scholar 

  • Fricke HW (1975) Selektives feinderkennen bei dem anemonenfisch Amphiprion bicinctus (Rüppell). J Exp Mar Bio Ecol 19:1–7

    Article  Google Scholar 

  • Frisch AJ, Anderson TA (2000) The response of coral trout (Plectropomus leopardus) to capture, handling and transport and shallow water stress. Fish Physiol Biochem 23:23–34

    Article  CAS  Google Scholar 

  • Gardiner NM, Munday PL, Nilsson GE (2010) Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLoS One 5:e13299

    Article  PubMed Central  PubMed  Google Scholar 

  • Grenchik MK, Donelson JM, Munday PL (2013) Evidence for developmental thermal acclimation in the damselfish Pomacentrus moluccensis. Coral Reefs 32:85–90

    Article  Google Scholar 

  • Grutter AS, Pankhurst NW (2000) The effects of capture, handling, confinement and ectoparasite load on plasma levels on cortisol, glucose and lactate in the coral reef fish Hemigymnus melapterus. J Fish Biol 57:391–401

    Article  CAS  Google Scholar 

  • Love OP, McGowan PO, Sheriff MJ (2012) Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities. Funct Ecol 27:81–92

    Article  Google Scholar 

  • Lutjeharms JRE (2006) The Agulhas current. Springer, Berlin

    Google Scholar 

  • Mazeaud MM, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with a general review. Trans Am Fish Soc 106:201–212

    Article  CAS  Google Scholar 

  • McEwen BS, Sapolsky RM (1995) Stress and cognitive function. Curr Opin Neurobiol 5:205–216

    Article  CAS  PubMed  Google Scholar 

  • Mills SC, Mourier J, Galzin R (2010) Plasma cortisol and 11-ketotestosterone enzyme immunoassay (EIA) kit validation for three fish species: the orange clownfish Amphiprion percula, the orangefin anemonefish Amphiprion chrysopterus and the blacktip reef shark Carcharhinus melanopterus. J Fish Biol 77:769–777

    CAS  PubMed  Google Scholar 

  • Moyer JT (1980) Influence of temperate waters on the behavior of the tropical anemonefish Amphiprion clarkii at Miyake-Jima, Japan. Bull Mar Sci 30:261–277

    Google Scholar 

  • Mullner A, Linsenmair KE, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118:549–558

    Article  Google Scholar 

  • Naim O, Quod JP (1999) The coral reefs of French Indian ocean territories (FIOT). Reef Encounter 26:33–36

    Google Scholar 

  • Pankhurst NW (2001) Stress inhibition of reproductive endocrine processes in a natural population of the spiny damselfish Acanthochromis polycanthus. Mar Freshw Res 52:753–761

    Article  CAS  Google Scholar 

  • Pankhurst NW, Sharples DF (1992) Effects of capture and confinement on plasma cortisol concentrations in the snapper, Pagrus auratus. Aust J Mar Freshw Res 43:345–356

    Article  CAS  Google Scholar 

  • Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62:1015–1026

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Romero LM, Wikelski M (2002) Exposure to tourism reduces stress-induced corticosterone levels in Galapagos marine iguanas. Biol Conserv 108:371–374

    Article  Google Scholar 

  • Rummer JL, Couturier CS, Stecyk JAW, Gardiner NM, Kinch JP, Nilsson GE, Munday PL (2014) Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Glob Change Biol 20:1055–1066

    Article  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2010) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–2994

    Article  PubMed  Google Scholar 

  • Swart NC, Lutjeharms JRE, Ridderinkhof H, DeRuijter WPM (2010) Observed characteristics of Mozambique Channel eddies. J Geophys Res 115:CO9006

    Article  Google Scholar 

  • Sumpter JP (1991) The stress response and its consequences in cultured fish. Bull Inst Zool 16:229–236

    Google Scholar 

  • Sumpter JP (1997) The endocrinology of stress. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 95–118

    Google Scholar 

  • Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297

    Article  CAS  PubMed  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • Wingfield JC (2008) Comparative endocrinology, environment and global change. Gen Comp Endocrinol 157:207–216

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Kelley JP, Angelier F (2011) What are extreme environmental conditions and how do organisms cope with them? Curr Zool 57:363–374

    Google Scholar 

Download references

Acknowledgments

Financial support was provided from INEE-INSU-IRD-AAMP-FRB-TAAF-Îles Eparses (Clownfish), Agence National de Recherche (ANR-11-JSV7-012-01/Live and Let Die), LabEx “CORAIL” (Where do we go now?), and FCT (SFRH/BPD/26901/2006). We thank the BioReCIE team (Pierre Barroil, Christophe Cadet, Patrick Durville, Eric Hoarau, Jean-Benoît Nicet, Emmanuel Tessier, Thierry Mulochau) for field support; Jeff Maynard, S. Heron, and G. Ahmadia for analyzing SST data; Gaël Simon, Danielle Bergazin, and Nathalie Tolou for laboratory/administrative assistance. We thank Alastair Harborne, Sophie Nedelec, Jeff Maynard, and anonymous referees for their critical comments.

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Authors and Affiliations

  1. USR 3278 CRIOBE CNRS-EPHE-UPVD, BP 1013, 98729, Papetoai, Moorea, French Polynesia

    S. C. Mills & R. Beldade

  2. Laboratoire d’Excellence “CORAIL”, France

    S. C. Mills, R. Beldade, P. Chabanet & L. Bigot

  3. MARE – Marine and Environmental Sciences Centre, Faculdade de Ciências, Centro da Universidade de Lisboa, Campo Grande, 1749-016, Lisbon, Portugal

    R. Beldade

  4. UMR ENTROPIE, Institut de Recherche pour le Développement, CS 41095, 97495, Sainte Clotilde Cedex, La Réunion, France

    P. Chabanet & L. Bigot

  5. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, 95060, USA

    J. L. O’Donnell & G. Bernardi

  6. School of Marine and Environmental Affairs, University of Washington, Seattle, WA, 98105, USA

    J. L. O’Donnell

Authors
  1. S. C. Mills
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  2. R. Beldade
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  3. P. Chabanet
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  4. L. Bigot
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  5. J. L. O’Donnell
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  6. G. Bernardi
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Corresponding author

Correspondence to S. C. Mills.

Additional information

Communicated by Ecology Editor Dr Alastair Harborne

S. C. Mills and R. Beldade are joint first authors.

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Mills, S.C., Beldade, R., Chabanet, P. et al. Ghosts of thermal past: reef fish exposed to historic high temperatures have heightened stress response to further stressors. Coral Reefs 34, 1255–1260 (2015). https://doi.org/10.1007/s00338-015-1333-8

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  • DOI: https://doi.org/10.1007/s00338-015-1333-8

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