Abstract
One potential trade-off that bold individuals face is between increased predation risks and gains in resources. Individuals experiencing high predation and hungry individuals (or individuals with low body condition) are predicted to show increased boldness. We examined one behavioral trait previously reported to be associated with boldness (the time individual fish needed to emerge from shelter) in various populations of mollies (Poecilia spp.). Our study system included several southern Mexican surface streams with high piscine predation and high food availability, sulfidic surface streams with high avian predation, in which the inhabiting fish show reduced body condition, and a sulfidic cave, where predation and body condition are low. Our comparison revealed very short times to emerge from the start box in populations from non-sulfidic streams. In sulfidic habitats (whether surface or cave), it took individual Poecilia mexicana considerably longer to emerge from the start box, and the same difference was also found in an independent comparison between P. mexicana and the closely related, highly sulfide-adapted Poecilia sulphuraria. Fish reared under common garden conditions (in the absence of predators and hydrogen sulfide) showed intermediate boldness scores to the extremes observed in the field. Our data thus indicate that (a) boldness is shaped by environmental conditions/experiential effects, but is not heritable, (b) predation affects boldness in the predicted direction, but (c) low body condition leads to reduced boldness. Extremophile Poecilia spp. spend most of their time surfacing to survive under sulfidic and hypoxic conditions, which exposes them to increased levels of predations, but the fish forage on the bottom. Hence, in this system, increased boldness does not increase foraging success. We argue that energy limitation favors reducing energetically costly behaviors, and exploring novel environments may be just one of them.
Similar content being viewed by others
References
Alvarez del Villar J (1948) Descripción de una nueva especie de Mollienisia capturada en Baños del Azufre, Tabasco (Pisces, Poeciliidae). An Esc Nac Cienc Biol 5:275–281
Bakker TCM (1986) Aggressiveness in sticklebacks (Gasterosteus aculeatus)—a behavior-genetic study. Behaviour 98:1–144
Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473
Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of bishop, Brachyraphis episcopi. Anim Behav 68:1325–1329
Brown C, Jones F, Braithwaite VA (2005) In situ examination of boldness–shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav 70:1003–1009
Brown C, Burgess F, Braithwaite VA (2007a) Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62:237–243
Brown C, Jones F, Braithwaite VA (2007b) Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi. J Fish Biol 71:1590–1601
Carrico R, Blumberg W, Peisach J (1978) The reversible binding of oxygen to sulfhemoglobin. J Biol Chem 253:7212–7215
Chapman LJ, Chapman CA (1993) Desiccation, flooding, and the behavior of Poecilia gillii (Pisces: Poeciliidae). Ichthyol Explor Freshw 4:279–287
Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936
Dall SR, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739
Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184
Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847–852
Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138
Dingemanse NJ, Van der Plas F, Wright J, Réale D, Schrama M, Roff DA, Van der Zee E, Barber I (2009) Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc R Soc Lond B 276:1285–1293
Evans C (1967) The toxicity of hydrogen sulphide and other sulphides. Quart J Exp Physiol 52:231–248
Fraser DF, Gilliam JF, Daley MJ, Le AN, Skalski GT (2001) Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am Nat 158:124–135
Godin J-GJ, Dugatkin LA (1999) Female mating preference for bold males in the guppy, Poecilia reticulata. Proc Natl Acad Sci U S A 93:10262–10267
Gordon MS, Rosen DE (1962) A cavernicolous form of the Poeciliid fish Poecilia sphenops from Tabasco, México. Copeia 1962:360–368
Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86
Gosling SD, John OP (1999) Personality dimensions in non-human animals: a cross-species review. Curr Dir Psychol Sci 8:69–75
Ip YK, Kuah SSL, Chew SF (2004) Strategies adopted by the mudskipper Boleophthalmus boddaerti to survive sulfide exposure in normoxia or hypoxia. Physiol Biochem Zool 77:824–837
Johnsson JI, Sernland E, Blixt M (2001) Sex-specific aggression and antipredator behaviour in young brown trout. Ethology 107:587–599
Kilgour R (1975) Open-field test as an assessment of temperament of dairy cows. Anim Behav 23:615–624
Körner KE, Schlupp I, Plath M, Loew ER (2006) Spectral sensitivity of mollies: comparing surface- and cave-dwelling Atlantic mollies, Poecilia mexicana. J Fish Biol 69:54–65
Kramer DL (1983) The evolutionary ecology of respiratory modes in fishes: an analysis based on the costs of breathing. Environ Biol Fish 9:145–158
Kramer DL, Manley D, Bourgeois R (1983) The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes. Can J Zool 61:653–665
Lopez P, Hawlena D, Polo V, Amo L, Martin J (2006) Sources of individual shy–bold variations in antipredator behaviour of male Iberian rock lizards. Anim Behav 69:1–9
Magnhagen C (2007) Social influence on the correlation between behaviours in young-of-the-year perch. Behav Ecol Sociobiol 61:525–531
Magurran AE, Macías Garcia C (2000) Sex differences in behaviour as an indirect consequence of mating system. J Fish Biol 57:839–857
McCune S (1995) The impact of paternity and early socialization on the development of cats’ behaviour to people and novel objects. Appl Anim Behav Sci 45:109–124
Miller RR (1975) Five new species of Mexican poeciliid fishes of the genera Poecilia, Gambusia, and Poeciliopsis. Occ Pap Mus Zool Univ Mich 672:1–44
Miller RR (2005) Freshwater fishes of Mexico. University of Chicago Press, Chicago
National Research Council (1979) Hydrogen sulfide. University Park, Baltimore
Nicholls P (1975) The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts of the reduced alpha-peak. Biochem Biophys Acta 396:24–35
van Oers K, Drent PJ, de Goede P, van Nordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73
Park C, Nagel R, Blumberg W, Peisach J, Maliozzo R (1986) Sulfhemoglobin: properties of partially sulfurated tetramers. J Biol Chem 261:8805–8810
Parzefall J (1974) Rückbildung aggressiver Verhaltensweisen bei einer Höhlenform von Poecilia sphenops (Pisces, Poeciliidae). Z Tierpsychol 35:66–84
Parzefall J (1979) Zur Genetik und biologischen Bedeutung des Aggressionsverhaltens von Poecilia sphenops (Pisces, Poeciliidae). Z Tierpsychol 50:399–422
Parzefall J (1993) Schooling behaviour in population-hybrids of Astyanax fasciatus and Poecilia mexicana (Pisces, Characidae and Poeciliidae). In: Schröder H, Bauer J, Schartl M (eds) Trends in ichthyology: an international perspective. Blackwell Scientific, Oxford, pp 297–303
Peters N, Peters G, Parzefall J, Wilkens H (1973) Über degenerative und konstruktive Merkmale bei einer phylogenetisch jungen Höhlenform von Poecilia sphenops (Pisces, Poeciliidae). Int Rev Gesamten Hydrobiol 58:417–436
Plath M (2008) Male mating behavior and costs of sexual harassment for females in cavernicolous and extremophile populations of Atlantic mollies (Poecilia mexicana). Behaviour 145:73–98
Plath M, Schlupp I (2008) Parallel evolution leads to reduced shoaling behavior in two cave-dwelling populations of Atlantic mollies (Poecilia mexicana, Poeciliidae, Teleostei). Environ Biol Fish 82:289–297
Plath M, Strecker U (2008) Behavioral diversification in a young species flock of pupfish (Cyprinodon spp., Cyprinodontidae, Teleostei): shoaling and aggressive behavior. Behav Ecol Sociobiol 62:1727–1737
Plath M, Tobler M (2009) The evolutionary ecology of the cave molly (Poecilia mexicana) from the Cueva del Azufre system. In: Trajano E, Bichuette ME, Kapoor BG (eds) The biology of subterranean fishes (in press)
Plath M, Parzefall J, Schlupp I (2003) The role of sexual harassment in cave- and surface-dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 54:303–309
Plath M, Parzefall J, Körner KE, Schlupp I (2004) Sexual selection in darkness? Female mating preferences in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei). Behav Ecol Sociobiol 55:596–601
Plath M, Heubel KU, García de León FJ, Schlupp I (2005) Cave molly females (Poecilia mexicana, Poeciliidae, Teleostei) like well-fed males. Behav Ecol Sociobiol 58:144–151
Plath M, Hauswaldt JS, Moll K, Tobler M, García de León FJ, Schlupp I, Tiedemann R (2007a) Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, from a Mexican cave with toxic hydrogen sulfide. Mol Ecol 16:967–976
Plath M, Tobler M, Riesch RW, García de León FJ, Giere O, Schlupp I (2007b) Survival in an extreme habitat: the roles of behaviour and energy limitation. Naturwissenschaften 94:991–996
Plath M, Makowicz AM, Schlupp I, Tobler M (2007c) Sexual harassment in live-bearing fishes: comparing courting and non-courting species. Behav Ecol 18:680–688
Ptacek MB, Breden F (1998) Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J Fish Biol 53:64–81
Réale D, Festa-Bianchet M (2003) Predator-induced natural selection on temperament in bighorn ewes. Anim Behav 65:463–470
Réale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318
Reaney LT, Backwell PRY (2007) Risk-taking behavior predicts aggression and mating success in a fiddler crab. Behav Ecol 18:521–525
Riesch R, Tobler M, Schlupp I, Plath M (2009) Offspring number in a livebearing fish (Poecilia mexicana, Poeciliidae): reduced fecundity and reduced plasticity in a population of cave mollies. Environ Biol Fishes 84:89–94
Rochette R, Tetreault F, Himmelman JH (2001) Aggregation of whelks, Buccinium undatum, near feeding predators—the role of reproductive requirement. Anim Behav 61:31–41
Schartl M, Meyer MK, Wilde B (2006) Description of Priapella chamulae sp. n.—a new poeciliid fish from the upper Río Grijalva system, Tabasco, Mexico (Teleostei: Cyprinodontiformes: Poeciliidae). Zool Abh Dresden 55:59–67
Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Quart Rev Biol 79:241–277
Sinn DL, Apiolaza LA, Moltschaniwskyj NA (2006) Heritability and fitness-related consequences of squid personality traits. J Evol Biol 19:1437–1447
Stein MB, Chartier MJ, Lizak MV, Jang L (2001) Familial aggregation of anxiety-related quantitative traits in generalized social phobia—clues to understand “disorder” heritability? Am J Med Genet 105:79–83
Svartberg K, Tapper I, Temrin H, Radesater T, Thorman S (2005) Consistency of personality in dogs. Anim Behav 69:283–291
Tobler M (2008) Divergence in trophic ecology characterises colonisation of extreme habitats. Biol J Linn Soc 95:517–528
Tobler M, Schlupp I, Heubel KU, Riesch R, García de León FJ, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585
Tobler M, Schlupp I, Plath M (2007) Predation of a cavefish (Poecilia mexicana, Poeciliidae) by a giant water bug (Belostoma, Belostomatidae) in a Mexican sulfur cave. Ecol Entomol 32:492–495
Tobler M, DeWitt TJ, Schlupp I, García de León FJ, Herrmann R, Feulner PGD, Tiedemann R, Plath M (2008a) Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution 62:2643–2659
Tobler M, Riesch R, García de León FJ, Schlupp I, Plath M (2008b) Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei) as only survivors in a small sulphidic habitat. J Fish Biol 72:523–533
Tobler M, Franssen C, Plath M (2008c) Male-biased predation of a cave fish by a giant water bug. Naturwissenschaften 95:775–779
Yoshida M, Nagamine M, Uematsu K (2005) Comparison of behavioral responses to a novel environment between three teleosts, bluegill Lepomis macrochirus, crucian carp Carassius langsdorfii, and goldfish Carassius auratus. Fish Sci 71:314–319
Ward A, Thomas P, Hart P, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568
Weber JM, Kramer DL (1983) Effects of hypoxia and surface access on growth, mortality, and behavior of juvenile guppies, Poecilia reticulata. Can J Fish Aquat Sci 40:1583–1588
Webster MM, Ward AJW, Hart PJB (2009) Individual boldness affects interspecific interactions in sticklebacks. Behav Ecol Sociobiol 63:511–520
Wilson ADM, McLaughlin RL (2007) Behavioural syndromes in brook charr, Salvelinus fontinalis: prey-search in the field corresponds with space use in novel laboratory situations. Anim Behav 74:689–698
Wilson DS, Coleman K, Clark AB, Biederman L (1993) The shy–bold continuum in pumkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J Comp Psychol 107:250–260
Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446
Winemiller KO (1989) Development of dermal lip protuberances for aquatic surface respiration in South American characid fishes. Copeia 1989:382–390
Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin RK (2003) Inter- and intra-population variations in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften 90:374–377
Yerkes RM (1939) The life history and personality of the chimpanzee. Am Nat 73:97–112
Acknowledgments
We would like to thank A. Böttger, N. Bunzel (both University of Potsdam), and J. Horstkotte (University of Hamburg) for their help in the field. We thank G. Rosenthal for commenting on a previous manuscript draft. G. Rosenthal and J.B. Johnson kindly provided information about boldness in Xiphophorus spp. The Mexican Government (Permiso de Pesca de Fomento No. DGOPA.06192.240608.-1562), Semarnat (No. SGPA/DGVS/04148/08 and SGPA/DGVS/04751/08), as well as the Municipal of Tacotalpa (SM/1133/208) kindly provided permits for the work at the Cueva del Azufre and the Baños del Azufre areas. Financial support came from the DFG (PL 470/1-2, to M.P.) and from NSF (#105095200).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. Bakker
Rights and permissions
About this article
Cite this article
Riesch, R., Duwe, V., Herrmann, N. et al. Variation along the shy–bold continuum in extremophile fishes (Poecilia mexicana, Poecilia sulphuraria). Behav Ecol Sociobiol 63, 1515–1526 (2009). https://doi.org/10.1007/s00265-009-0780-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-009-0780-z