Login | Register

Cross-population responses to conspecific chemical alarm cues in wild Trinidadian guppies, Poecilia reticulata: evidence for local conservation of cue production


Cross-population responses to conspecific chemical alarm cues in wild Trinidadian guppies, Poecilia reticulata: evidence for local conservation of cue production

Brown, Grant E. and Elvidge, Chris K. and Macnaughton, Camille J. and Ramnarine, Indar and Godin, Jean-Guy J. (2010) Cross-population responses to conspecific chemical alarm cues in wild Trinidadian guppies, Poecilia reticulata: evidence for local conservation of cue production. Canadian Journal of Zoology, 88 (2). pp. 139-147. ISSN 0008-4301

PDF - Published Version

Official URL: http://dx.doi.org/10.1139/Z09-127


Within freshwater fishes, closely related species produce alarm cues that are chemically similar, leading to conserved antipredator responses. Similar conservation trends are predicted for species with geographically isolated populations. Here, we tested this hypothesis with the guppy (Poecilia reticulata Peters, 1859) from two populations within the Aripo River, Trinidad. Free-ranging guppies in the Lower Aripo (high-predation population) exhibited more risk-aversive inspection behaviour towards a fish predator model paired with the alarm cues of guppies collected from the same population versus a river water control. In comparison, when paired with the alarm cues of guppies from the Upper Aripo (low-predation population), the response was intermediate. In the laboratory, we tested Upper and Lower Aripo guppies to the alarm cues of the same or different Aripo River donors, Quaré River guppies (a high-predation population from a different drainage), or a water control. Both Upper and Lower Aripo River guppies exhibited the highest intensity response to donors from the same population and the lowest intensity response to Quaré River donors, with the response to different Aripo donors being intermediate. Collectively, these results demonstrate a trend of intraspecific conservation of chemical alarm cue production, leading to population-specific responses to conspecific cues.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Article
Authors:Brown, Grant E. and Elvidge, Chris K. and Macnaughton, Camille J. and Ramnarine, Indar and Godin, Jean-Guy J.
Journal or Publication:Canadian Journal of Zoology
Date:February 2010
  • Concordia University
  • Natural Sciences and Engineering Research Council of Canada
ID Code:6713
Deposited On:09 Jun 2010 23:40
Last Modified:24 Aug 2016 21:26
Blumstein, D.T. 2006. The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology, 112(3): 209–217.

Botham, M.S., Hayward, R.K., Morrell, L.J., Croft, D.P., Ward, J.R., Ramnarine, I., and Krause, J. 2008. Risk-sensitive antipredator behavior in the Trinidadian guppy, Poecilia reticulata. Ecology, 89(11): 3174–3185.

Brown, G.E. 2003. Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish. 4(3): 227–234.

Brown, G.E., and Dreier, V.M. 2002. Predator inspection behaviour and attack cone avoidance in a characin fish: the effects of predator diet and prey experience. Anim. Behav. 63(6): 1175–1181.

Brown, G.E., and Godin, J.-G.J. 1997. Anti-predator responses to conspecific and heterospecific skin extracts by threespine sticklebacks: alarm pheromones revisited. Behaviour, 134(15–16): 1123–1134.

Brown, G.E., and Godin, J.-G.J. 1999a. Chemical alarm signals in wild Trinidadian guppies (Poecilia reticulata). Can. J. Zool. 77(4): 562–570.

Brown, G.E., and Godin, J.-G.J. 1999b. Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Anim. Behav. 57(2): 475–481.

Brown, G.E., Adrian, J.C., Jr., Erikson, J., Kaufman, I.H., and Gershaneck, D. 2001a. Responses to nitrogen oxides by Characiforme fishes suggest evolutionary conservation in ostariophysan alarm pheromones. In Chemical signals in vertebrates. Vol. 9. Edited by A. Marchlewska-Koj, J.J. Lepri, and D. Müller-Schwarze. Plenum Press, New York. pp. 305–312.

Brown, G.E., Golub, J.L., and Plata, D.L. 2001b. Attack cone avoidance during predator inspection visits by wild finescale dace (Phoxinus neogaeus): the effects of predator diet. J. Chem. Ecol. 27(8): 1657–1666.

Brown, G.E., Adrian, J.C., Jr., Naderi, N.T., Harvey, M.C., and Kelly, J.M. 2003. Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J. Chem. Ecol. 29(8): 1781–1796.

Brown, G.E., Foam, P.E., Cowell, H.E., Guevara-Fiore, P., and Chivers, D.P. 2004. Production of chemical alarm cues in convict cichlids: the effects of diet, body condition and ontogeny. Ann. Zool. Fenn. 41(3): 487–499.

Brown, G.E., Rive, A.C., Ferrari, M.C.O., and Chivers, D.P. 2006. The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. Behav. Ecol. Sociobiol. 61(1): 9–16.

Brown, C., Burgess, F., and Braithwaite, V.A. 2007. Heritable and experiential effects on boldness in a tropical poeciliid. Behav. Ecol. Sociobiol. 62(2): 237–243.

Brown, G.E., Macnaughton, C.J., Elvidge, C.K., Ramnarine, I., and Godin, J.-G.J. 2009. Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies. Behav. Ecol. Sociobiol. 63(5): 699–706.

Chivers, D.P., and Smith, R.J.F. 1998. Chemical alarm signaling in aquatic predator–prey systems: a review and prospectus. Ecoscience, 5: 338–352.

Chivers, D.P., Wisenden, B.D., Hindman, C.J., Michalak, T.A., Kusch, R.C., Kaminskyj, S.G., Jack, K.L., Ferrari, M.C., Pollock, R.J., Halbgewachs, C.F., Pollock, M.S., Alemadi, S., James, C.T., Savaloja, R.K., Goater, C.P., Corwin, A., Mirza, R.S., Kiesecker, J.M., Brown, G.E., Adrian, J.C., Jr., Krone, P.H., Blaustein, A.R., and Mathis, A. 2007. Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proc. R. Soc. Lond. B Biol. Sci. 274(1625): 2611–2619.

Crispo, E., Bentzen, P., Reznick, D.N., Kinnison, M.T., and Hendry, A.P. 2006. The relative influence of natural selection and geography on gene flow in guppies. Mol. Ecol. 15(1): 49–62.

Croft, D.P., Albanese, B., Arrowsmith, B.J., Botham, M., Webster, M., and Krause, J. 2003. Sex-biased movement in the guppy (Poecilia reticulata). Oecologia (Berl.), 137(1): 62–68.

Dugatkin, L.A., and Godin, J.G.-J. 1992. Predator inspection, shoaling and foraging under predation hazard in the Trinidadian guppy, Poecilia reticulata. Environ. Biol. Fishes, 34(3): 265–276.

Dussault, G.V., and Kramer, D.L. 1981. Food and feeding behaviour of the guppy, Poecilia reticulata (Pisces: Poeciliidae). Can. J. Zool. 59(4): 684–701.

Endler, J.A. 1995. Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol. Evol. 10(1): 22–29.

Endler, J.A., and Houde, A.E. 1995. Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution, 49(3): 456–468.

Fajen, A., and Breden, F. 1992. Mitochondrial DNA sequence variation among natural populations of the Trinidad guppy, Poecilia reticulata. Evolution, 46(5): 1457–1465.

Foster, S.A. 1999. The geography of behaviour: an evolutionary perspective. Trends Ecol. Evol. 14(5): 190–195.

Godin, J.-G.J. 1995. Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia (Berl.), 103(2): 224–229.

Herczeg, G., Gonda, A., and Merilä, J. 2009. Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J. Evol. Biol. 22(3): 544–552.

Kats, L.B., and Dill, L.M. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience, 5: 361–394.

Kelly, C.D., Godin, J.-G.J., and Wright, J.M. 1999. Geographic variation in multiple paternity within natural populations of the guppy (Poecilia reticulata). Proc. R. Soc. Lond. B Biol. Sci. 266(1436): 2403–2408.

Kelly, J.M., Adrian, J.C., Jr., and Brown, G.E. 2006. Can the ratio of aromatic skeletons explain cross-species responses within evolutionarily conserved Ostariophysan alarm cues?: testing the purine-ratio hypothesis. Chemoecology, 16(2): 93–96.

Leduc, A.O.H.C., Noseworthy, M.K., Adrian, J.C., Jr., and Brown, G.E. 2003. Detection of conspecific and heterospecific alarm signals by juvenile pumpkinseed under weak acidic conditions. J. Fish Biol. 63(5): 1331–1336.

Leduc, A.O.H.C., Roh, E., Breau, C., and Brown, G.E. 2007. Learned recognition of a novel odour by wild juvenile Atlantic salmon, Salmo salar, under fully natural conditions. Anim. Behav. 73(3): 471–477.

Leduc, A.O.H.C., Roh, E., and Brown, G.E. 2009. Effects of acid rainfall on juvenile Atlantic salmon (Salmo salar) antipredator behaviour: loss of chemical alarm function and potential survival consequences during predation. Mar. Freshw. Res. 60(12): 1223–1230.

Lima, S.L., and Dill, L.M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68(4): 619–640.

Lima, S.L., and Steury, T.D. 2005. Perception of predation risk: the foundation of nonlethal predator–prey interactions. In Ecology of predator–prey interactions. Edited by P. Barbosa and I. Castellanos. Oxford University Press, Oxford. pp 166–188.

Magurran, A.E. 1998. Population differentiation without speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353(1366): 275–286.

Magurran, A.E. 2005. Evolutionary ecology: the Trinidadian guppy. Oxford University Press, Oxford.

Magurran, A.E., and Seghers, B.H. 1990. Population differences in predator recognition and attack cone avoidance in the guppy Poecilia reticulata. Anim. Behav. 40(3): 443–452.

Magurran, A.E., and Seghers, B.H. 1994. Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour, 128(1–2): 121–134.

Magurran, A.E., Irving, P.W., and Henderson, P.A. 1996. Is there a fish alarm pheromone? A wild study and critique. Proc. R. Soc. Lond. B Biol. Sci. 263(1376): 1551–1556.

Mathis, A., and Smith, R.J.F. 1993. Chemcial alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). Behav. Ecol. 4(3): 260–265.

Mirza, R.S., and Chivers, D.P. 2001a. Are chemical alarm cues conserved within salmonid fishes? J. Chem. Ecol. 27(8): 1641–1655.

Mirza, R.S., and Chivers, D.P. 2001b. Chemical alarm signals enhance survival of brook charr (Salvelinus fontinalis) during encounters with predatory chain pickerel (Esox niger). Ethology, 107(11): 989–1005.

Mirza, R.S., Scott, J.J., and Chivers, D.P. 2001. Differential responses of male and female red swordtails to chemical alarm cues. J. Fish Biol. 59(3): 716–728.

Nordell, S.E. 1998. The response of female guppies, Poecilia reticulata, to chemical stimuli from injured conspecifics. Environ. Biol. Fishes, 51(3): 331–338.

Owings, D.H., Coss, R.G., McKernon, D., Rowe, M.P., and Arrowood, P.C. 2001. Snake-directed antipredator behaviour of rock squirrels (Spermophilus variegates): population differences and snake species discrimination. Behaviour, 138(5): 575–595.

Reznick, D., Butler, M.J., IV, Rodd, F.H., and Ross, P. 1996. Life-history evolution in guppies (Poecilia reticulata) 6. Differential mortality as a mechanism for natural selection. Evolution, 50(4): 1651–1660.

Reznick, D., Butler, M.J., IV, and Rodd, H. 2001. Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments. Am. Nat. 157(2): 126–140.

Schutz, F. 1956. Vergleichende Untersuchugen über die Schreckreaktion bei Fischen unde deren Verbreitung. Z. Vgl. Physiol. 38(1–2): 84–135.

Smith, R.J.F. 1997. Does one result trump all others? A response to Magurran, Irving and Henderson. Proc. R. Soc. Lond. B Biol. Sci. 264(1380): 445–450.

Smith, R.J.F. 1999. What good is smelly stuff in the skin? Cross-function and cross-taxa effects in fish ‘alarm substances’. In Advances in chemical signals in vertebrates. Edited by R.E. Johnston, D. Müller-Schwarze, and P.W. Kluwer Academic, New York. pp 475–488.

Sokal, R.R., and Rohlf, F.J. 1995. Biometry: the principles and practice of statistics in biological research. 3rd ed. W.H. Freeman and Co., New York.

van Oosterhout, C., Joyce, D.A., Cummings, S.M., Blais, J., Barson, N.J., Ramnarine, I.W., Mohammed, R.S., Persad, N., and Cable, J. 2006. Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution, 60(12): 2562–2574.

Wisenden, B.D., and Chivers, D.P. 2006. The role of public chemical information in antipredator behaviour. In Fish chemoreception. Edited by F. Ladich, S.P. Colins, P. Moller, and B.G. Kapoor. Science Publishers, Enfield, N.H. pp 259–278.

All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.

Repository Staff Only: item control page

Downloads per month over past year

Back to top Back to top