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Differential stress responses in fish from areas of high- and low-predation pressure

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Abstract

We subjected fish from regions of high and low levels of predation pressure in four independent streams to a mild stressor and recorded their opercular beat rates. Fish from low-predation areas showed higher maximum, minimum and mean opercular beat frequencies than fish from high-predation regions. The change in opercular beat frequency (scope) was also significantly greater in fish from low- than in fish from high-predation regions. Under normal activity levels, however, low predation fish showed a reduced opercular beat frequency, which may be indicative of reduced activity levels or metabolic rate. Opercular beat frequency was negatively correlated with standard length as one would expect based on higher metabolic rates in smaller fish. We suggest that these contrasting stress responses are most likely the result of differential exposure to predators in fish from high- and low-predation areas. We argue that reduced stress responses in high-predation areas evolved to prevent excessive energy expenditure by modulating the fright response.

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References

  • Barcellos LJG, Nicolaiewsky S, de Souza SMG, Lulhier F (1999) Plasmatic levels of cortisol in the response to acute stress in Nile tilapia, Oreochromis niloticus (L), previously exposed to chronic stress. Aquacult Res 30:437–444

    Article  Google Scholar 

  • Barreto RE, Volpato GL (2004) Caution for using ventilatory frequency as an indicator of stress in fish. Behav Processes 66:43–51

    PubMed  Google Scholar 

  • Barreto RE, Luchiari AC, Macondes AL (2003) Ventilatory frequency indicates visual recognition of an allopatric predator in naïve Nile tilapia. Behav Processes 60:235–239

    PubMed  Google Scholar 

  • Basu N, Nakano T, Grau EG, Iwama GK (2001) The effects of cortisol on heat shock protein 70 levels in two fish species. Gen Comp Endocrinol 124:97–105

    CAS  PubMed  Google Scholar 

  • Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of the poeciliid, Brachyraphis episcope. Anim Behav 68:1325–1329

    Article  Google Scholar 

  • Brown C, Braithwaite VA (2005) Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi. Behav Ecol 16:482–487. doi:10.1093/beheco/ari016

    Google Scholar 

  • Brown C, Gardner C, Braithwaite VA (2004) Population variation in lateralised eye use in the poeciliid Brachyraphis episcopi. Proc R Soc Lond Ser B (Suppl) 271:S455–S457

    Google Scholar 

  • Brown C, Jones FC, Braithwaite VA (2005) Environmental influences on boldness-shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav (in press)

  • Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ (2000) The effects of early rearing environment on the development of GABA A and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22:219–229

    CAS  PubMed  Google Scholar 

  • Claireaux G, Lagardère JP (1999) Influence of temperature, oxygen and salinity on the metabolism of European sea bass. J Sea Res 42:157–168

    CAS  Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905. doi:10.1046/j.1365–2656.1999.00337.x

    Google Scholar 

  • Clutton-Brock T (1989) A natural history of domesticated mammals. Cambridge University Press, Cambridge

    Google Scholar 

  • Cooke SJ, Steinmetz J, Degner JF, Grant EC, Philipp DP (2003) Metabolic fright responses of different-sized largemouth bass (Micropterus salmoides) to two avian predators show variations in nonlethal energetic costs. Can J Zool 81:699–709

    Article  Google Scholar 

  • DeKoning ABL, Picard DJ, Bond SR, Schulte PM (2004) Stress and interpopulation variation in glycolytic enzyme activity and expression in a teleost fish Fundulus heteroclitus. Physiol Biochem Zool 77:18–26

    CAS  PubMed  Google Scholar 

  • Dunlap KD, Wingfield JC (1995) External and internal influences on indexes of physiological stress 1 Seasonal and population variation in adrenocortical secretion of free-living lizards, Sceloporus occidentalis. J Exp Zool 271:36–46

    CAS  PubMed  Google Scholar 

  • Ellis T, James JD, Stewart C, Scott AP (2004) A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. J Fish Biol 65:1233–1252

    CAS  Google Scholar 

  • Endler JA (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29

    Article  Google Scholar 

  • Espmark Y, Langvatn R (1985) Development and habituation of cardiac and behavioral-responses in young red deer calves (Cervus elaphus) exposed to alarm stimuli. J Mammal 66:702–711

    Google Scholar 

  • Fevolden SE, Røed KH, Fjalestad K (2003) A combined salt and confinement stress enhances mortality in rainbow trout (Oncorhynchus mykiss) selected for high stress responsiveness. Aquaculture 216:67–76

    Article  Google Scholar 

  • Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion—Facultative suppression of growth and reproduction. Ecology 73: 959–970

    Google Scholar 

  • Grantner A, Taborsky M (1998) The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae). J Comp Physiol B 168:427–433

    Article  Google Scholar 

  • Haase E, Donham RS (1980) Hormones and domestication. In: Epple A (ed) Avian Endocrinology. Academic, Santiago, pp 549–561

    Google Scholar 

  • Haukenes AH, Barton BA (2004) Characterization of the cortisol response following an acute challenge with lipopolysaccharide in yellow perch and the influence of rearing density. J Fish Biol 64:851–862

    CAS  Google Scholar 

  • Höjesjö J, Johnsson JI, Axelsson M (1999) Behavioural and heart rate responses to food limitation and predation risk: an experimental study on rainbow trout. J Fish Biol 55:1009–1019

    Article  Google Scholar 

  • Hughes GM (1960) A comparative study of gill ventilation in marine teleosts. J Exp Biol 37:28–45

    Google Scholar 

  • Jennions MD, Telford SR (2002) Life-history phenotypes in populations of Brachyrhaphis episcopi (Poeciliidae) with different predator communities. Oecologia 132:44–50

    Article  Google Scholar 

  • Johnsson JI, Höjesjö J, Fleming IA (2001) Behavioural and heart rate responses to predation risk in wild and domesticated Atlantic salmon. Can J Fish Aquat Sci 58:788–794

    Article  Google Scholar 

  • Jones DR (1971) Theoretical analysis of factors which may limit the maximum oxygen uptake of fish: The oxygen cost of the cardiac and branchial pumps. J Theor Biol 32:341–349

    CAS  PubMed  Google Scholar 

  • Kunzl C, Sachser N (1999) The behavioural endocrinology of domestication: a comparison between the domestic Guinea pig (Gavia opera f porcellus) and its wild ancestor, the Cavy (Cavia apera). Horm Behav 35:28–37

    CAS  PubMed  Google Scholar 

  • Lepage O, Overli O, Petersson E, Jarvi T, Winberg S (2000) Differential stress coping in wild and domesticated sea trout. Brain Behav Evol 56:259–268

    CAS  PubMed  Google Scholar 

  • Lucas MC, Johnstone ADF, Priede IG (1993) Use of physiological telemetry as a method of estimating metabolism of fish in the natural environment. Trans Am Fish Soc 122:822–833

    Article  Google Scholar 

  • Majica CL (1998) Comparative ecology and historical biogeography of the genus Brachyraphis. Environ Biol Fishes 51:117–127

    Article  Google Scholar 

  • Metcalfe NB, Huntingford FA, Thorpe JE (1987) The influence of predation risk on the feeding motivation and foraging strategy of juvenile Atlantic salmon. Anim Behav 35:901–911

    Google Scholar 

  • Miller RB (1954) Comparative survival of wild and hatchery-reared cutthroat trout in a stream. Trans Am Fish Soc 83:120–130

    Google Scholar 

  • Olla BL, Davis MW, Schreck CB (1997) Effects of simulated trawling on sablefish and walleye pollock: The role of light intensity, net velocity and towing duration. J Fish Biol 50:1181–1194

    Article  Google Scholar 

  • Øverli O, Olsen RE, Lovik F, Ringo E (1999) Dominance hierarchies in Arctic charr, Salvelinus alpinus L: differential cortisol profiles of dominant and subordinate individuals after handling stress. Aquacult Res 30:259–264

    Article  Google Scholar 

  • Øverli O, Pottinger TG, Carrick TR, Overli E, Winberg S (2001) Brain monoaminergic activity in rainbow trout selected for high and low stress responsiveness. Brain Behav Evol 57:214–224

    PubMed  Google Scholar 

  • Pfeiffer W (1962) The fright reaction of fish. Biol Rev 37:495–511

    CAS  PubMed  Google Scholar 

  • Poole WR, Nolan DT, Wevers T, Dillane M, Cotter D, Tully O (2003) An ecophysiological comparison of wild and hatchery-raised Atlantic salmon (Salmo salar L) smolts from the Burrishoole system, western Ireland. Aquaculture 222:301–314

    Article  Google Scholar 

  • Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132

    CAS  PubMed  Google Scholar 

  • Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Fitness and adaptation in a novel environment: Effect of inbreeding, prior environment, and lineage. Evolution 57:1822–1828

    PubMed  Google Scholar 

  • Robb T, Abrahams MV (2003) Variation in tolerance to hypoxia in a predator and prey species: an ecological advantage of being small?. J Fish Biol 62:1067–1081

    Article  Google Scholar 

  • Romero LM (2004) Physiological stress in ecology: Lessons from biomedical research. Trends Ecol Evol 19:249–255

    Article  Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Sutterland AM (1969) Effects of exercise on cardiac and ventilation frequency in three species of freshwater teleosts. Physiol Zool 42:36–52

    Google Scholar 

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Acknowledgements

We thank the Smithsonian Tropical Research Institute for their continued support and Fiona Burgess for her aid with husbandry. Thanks also to Felicity Brown for her help collecting the fish. The fish were collected and exported under licence from the Panamanian authorities (ANAM permit# 31503). This work was funded by NERC grant no NER/A/S/01/00608.

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  1. Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, EH9 3JT, UK

    Culum Brown, Carolyn Gardner & Victoria A. Braithwaite

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  1. Culum Brown
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  2. Carolyn Gardner
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  3. Victoria A. Braithwaite
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Correspondence to Culum Brown.

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Communicated by G. Heldmaier

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Brown, C., Gardner, C. & Braithwaite, V.A. Differential stress responses in fish from areas of high- and low-predation pressure. J Comp Physiol B 175, 305–312 (2005). https://doi.org/10.1007/s00360-005-0486-0

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  • DOI: https://doi.org/10.1007/s00360-005-0486-0

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