Male guppies compensate for lost time when mating in turbid water

  • Sean M. EhlmanEmail author
  • Daniel Martinez
  • Andrew Sih
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Turbidity (a measure of the cloudiness of water) decreases the visual range of organisms, altering interactions within and between species. For species that visually assess mates, turbidity may affect mating interactions and mate choice. A central question, then, is to what degree organisms plastically adjust mating behaviors to cope with visually altered environments. Here, we investigate the effect of turbidity on the mating behavior of guppies (Poecilia reticulata) in Trinidad, where some streams are increasingly turbid due to upstream rock quarrying. We collected fish from two highly turbid streams (with upstream rock quarries) and two pristine streams (no upstream quarries) in the same drainages. We then observed male mating behaviors with females from the same populations in both turbid and clear assays, recording displays and sneak copulation attempts. Males from turbid streams showed greater individual consistency in mating behaviors. But regardless of provenance, male guppies spent less time associating with females in turbid water overall. When males and females did interact, however, males greatly increased the rate of all mating behaviors in turbid as compared to clear water. Thus, even when lacking a long-term evolutionary history with high turbidity, guppies compensate for lost time when mating in a visually altered environment.

Significance statement

Given the global nature of increases in turbidity, understanding behavioral responses to this aquatic anthropogenic change is critical. Here, we investigate the degree to which Trinidadian guppy males in affected areas are able to plastically compensate in turbid water by adjusting mating behaviors. We also test the degree to which previous chronic exposure to turbidity alters this plasticity. In contrast to predictions, we did not find population differences in plasticity; across all populations, however, we found significant plasticity in the guppy mating system in response to anthropogenically increased turbidity. While males spent less time associating with females in turbid water overall, males increased mating effort during periods of association, compensating for lost time in turbid water. We discuss this plasticity and the implications for guppy sexual selection and secondary sexual characteristics such as coloration.


Environmental change Guppy Mating behavior Plasticity Turbidity 



We would like to thank the Sih lab for offering insights during the analysis phase. The manuscript was improved by helpful edits from A. Pilastro, K. Heubel, and an anonymous reviewer. We also gratefully acknowledge the Asa Wright Nature Centre, with special thanks to Ronnie Hernandez, for facilitating our work at the William Beebe Tropical Research Station. SME was supported by the UC Davis Center for Population Biology and by an NSF Graduate Research Fellowship.

Compliance with ethical standards

Ethical approval

Fish were collected under the approval of the Trinidad and Tobago Ministry of Food Production, Aquaculture Division. All procedures herein performed were approved in accordance with national and international ethics standards by the University of California Davis’ Institutional Animal Care and Use Committee.

Conflict of interest

The authors declare that they have no conflict of interest.

Data accessibility statement

The dataset collected and analyzed during the current study is available from the corresponding author on reasonable request.


  1. Abrahams M, Kattenfeld M (1997) The role of turbidity as a constraint on predator-prey interactions in aquatic environments. Behav Ecol Sociobiol 40:169–174. CrossRefGoogle Scholar
  2. Archard GA, Cuthill IC, Partridge JC (2009) Light environment and mating behavior in Trinidadian guppies (Poecilia reticulata). Behav Ecol Sociobiol 64:169–182. CrossRefGoogle Scholar
  3. Baerends GP, Brouwer R, Waterbolk HTJ (1955) Ethological studies on Lebistes reticulatus (Peters). Behav 8:249–332. CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  5. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer Associates, Inc., Sunderland, MAGoogle Scholar
  7. Bolker BM (2015) Linear and generalized linear mixed models. In: Fox GA, Negrete-Yankelevich S, Sosa VJ (eds) Ecological statistics: contemporary theory and application. Oxford University Press, Oxford, pp 309–333CrossRefGoogle Scholar
  8. Borner KK, Krause S, Mehner T, Uusi-Heikkilä S, Ramnarine IW, Krause J (2015) Turbidity affects social dynamics in Trinidadian guppies. Behav Ecol Sociobiol 69:645–651. CrossRefGoogle Scholar
  9. Candolin U, Heuschele J (2008) Is sexual selection beneficial during adaptation to environmental change? Trends Ecol Evol 23:446–452. CrossRefPubMedGoogle Scholar
  10. Castillo Cajas RF, Selz OM, Ripmeester EAP, Seehausen O, Maan ME (2012) Species-specific relationships between water transparency and male coloration within and between two closely related Lake Victoria cichlid species. Int J Evol Biol 2012:161306–161312. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chapman BB, Morrell LJ, Krause J (2009) Plasticity in male courtship behaviour as a function of light intensity in guppies. Behav Ecol Sociobiol 63:1757–1763. CrossRefGoogle Scholar
  12. Chapman BB, Morrell LJ, Tosh CR, Krause J (2010) Behavioural consequences of sensory plasticity in guppies. Proc R Soc Lond B 277:1395–1401. CrossRefGoogle Scholar
  13. Clark E, Aronson LR (1951) Sexual behavior in the guppy, Lebistes reticulatus. Zoologica 36:49–66Google Scholar
  14. Davies-Colley RJ, Smith DG (2001) Turbidity, suspended sediment, and water clarity: a review. J Am Water Resour As 37:1085–1101. CrossRefGoogle Scholar
  15. Dearing JA, Jones RT (2003) Coupling temporal and spatial dimensions of global sediment flux through lake and marine sediment records. Glob Planet Change 39:147–168. CrossRefGoogle Scholar
  16. Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89. CrossRefPubMedGoogle Scholar
  17. Ehlman SM, Sandkam BA, Breden F, Sih A (2015) Developmental plasticity in vision and behavior may help guppies overcome increased turbidity. J Comp Physiol A 201:1125–1135. CrossRefGoogle Scholar
  18. Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:1–20 CrossRefGoogle Scholar
  19. Endler JA (1987) Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim Behav 35:1376–1385. CrossRefGoogle Scholar
  20. Engström-Öst J, Candolin U (2007) Human-induced water turbidity alters selection on sexual displays in sticklebacks. Behav Ecol 18:393–398. CrossRefGoogle Scholar
  21. Evans JP, Kelley JL, Ramnarine IW, Pilastro A (2002) Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 52:496–502. CrossRefGoogle Scholar
  22. Gardner MB (1981) Effects of turbidity on feeding rates and selectivity of bluegills. Trans Am Fish Soc 110:446–450.<446:EOTOFR>2.0.CO;2 CrossRefGoogle Scholar
  23. Godin J-GJ, McDonough HE (2003) Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav Ecol 14:194–200. CrossRefGoogle Scholar
  24. Godin J-GJ (1995) Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229. CrossRefPubMedGoogle Scholar
  25. Gregory RS, Levings CD (1998) Turbidity reduces predation on migrating juvenile pacific salmon. Trans Am Fish Soc 127:275–285.<0275:TRPOMJ>2.0.CO;2 CrossRefGoogle Scholar
  26. Grether GF (2005) Environmental change, phenotypic plasticity, and genetic compensation. Am Nat 166:E115–E123.
  27. Heubel KU, Schlupp I (2006) Turbidity affects association behaviour in male Poecilia latipinna. J Fish Biol 68:555–568. CrossRefGoogle Scholar
  28. Heuschele J, Mannerla M, Gienapp P, Candolin U (2009) Environment-dependent use of mate choice cues in sticklebacks. Behav Ecol 20:1223–1227. CrossRefGoogle Scholar
  29. Hibler TL, Houde AE (2006) The effect of visual obstructions on the sexual behaviour of guppies: the importance of privacy. Anim Behav 72:959–964
  30. Horkel JD, Pearson WD (1976) Effects of turbidity on ventilation rates and oxygen consumption of green sunfish, Lepomis cyanellus. Trans Am Fish Soc 105:107–113.<107:EOTOVR>2.0.CO;2 CrossRefGoogle Scholar
  31. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, PrincetonGoogle Scholar
  32. Houde AE (1987) Mate choice based upon naturally occurring color-pattern variation in a guppy population. Evolution 41:1–10. CrossRefPubMedGoogle Scholar
  33. Järvenpää M, Lindström K (2004) Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proc R Soc Lond B 271:2361–2365. CrossRefGoogle Scholar
  34. Kimbell HS, Morrell LJ (2015) Turbidity influences individual and group level responses to predation in guppies, Poecilia reticulata. Anim Behav 103:179–185. CrossRefGoogle Scholar
  35. Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25:393–401. CrossRefGoogle Scholar
  36. Kolluru GR, Grether GF (2005) The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata). Behav Ecol 16:294–300. CrossRefGoogle Scholar
  37. Kolluru GR, Grether GF, Contreras H (2006) Environmental and genetic influences on mating strategies along a replicated food availability gradient in guppies (Poecilia reticulata). Behav Ecol Sociobiol 61:689–701. CrossRefGoogle Scholar
  38. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0–33,
  39. Leahy SM, McCormick MI, Mitchell MD, Ferrari MCO (2011) To fear or to feed: the effects of turbidity on perception of risk by a marine fish. Biol Lett 7:811–813. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lehtiniemi M, Engström-Öst J, Viitasalo M (2005) Turbidity decreases anti-predator behaviour in pike larvae, Esox lucius. Environ Biol Fish 73:1–8. CrossRefGoogle Scholar
  41. Lowe-McConnell RH (1987) Ecological studies in tropical fish communities. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  42. Luyten PH, Liley NR (1985) Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behav 95:164–179. CrossRefGoogle Scholar
  43. Luyten PH, Liley NR (1991) Sexual selection and competitive mating success of male guppies (Poecilia reticulata) from four Trinidad populations. Behav Ecol Sociobiol 28:329–336. CrossRefGoogle Scholar
  44. Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecol Lett 14:591–602. CrossRefPubMedGoogle Scholar
  45. Maan ME, Seehausen O, van Alphen JJM (2010) Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish. Biol J Linn Soc 99:398–406. CrossRefGoogle Scholar
  46. Magellan K, Magurran AE (2007) Behavioural profiles: individual consistency in male mating behaviour under varying sex ratios. Anim Behav 74:1545–1550. CrossRefGoogle Scholar
  47. Magurran AE (2005) Evolutionary Ecology: the Trinidadian Guppy. Oxford University Press, OxfordCrossRefGoogle Scholar
  48. Martínez Ruiz C, Knell RJ (2017) Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors. J Anim Ecol 86:117–127. CrossRefPubMedGoogle Scholar
  49. Milinski M, Bakker T (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333CrossRefGoogle Scholar
  50. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  51. Ranåker L, Jönsson M, Nilsson PA, Brönmark C (2012) Effects of brown and turbid water on piscivoreprey fish interactions along a visibility gradient. Freshw Biol 57:1761–1768. CrossRefGoogle Scholar
  52. Reznick DN, Rodd FH, Cardenas M (1996) Life-history evolution of guppies (Poecilia reticulata: Poecilidae). IV. Parallelism in life-history phenotypes. Am Nat 147:319–338. CrossRefGoogle Scholar
  53. Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937. CrossRefPubMedGoogle Scholar
  54. Ruell EW, Handelsman CA, Hawkins CL, Sofaer HR, Ghalambor CK, Angeloni L (2013) Fear, food and sexual ornamentation: plasticity of colour development in Trinidadian guppies. Proc Roy Soc B 280:20122019. CrossRefGoogle Scholar
  55. Seehausen O, van Alphen JJM (1998) The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behav Ecol Sociobiol 42:1–8. CrossRefGoogle Scholar
  56. Seehausen O, van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811. CrossRefGoogle Scholar
  57. Shenoy K, Crowley PH (2011) Endocrine disruption of male mating signals: ecological and evolutionary implications. Funct Ecol 25:433–448. CrossRefGoogle Scholar
  58. Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088. CrossRefGoogle Scholar
  59. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. CrossRefPubMedGoogle Scholar
  60. Stoffel MA, Nakagawa S, Schielzeth H, Goslee S (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639-1644.
  61. Sundin J, Berglund A, Rosenqvist G (2010) Turbidity hampers mate choice in a pipefish. Ethology 116:713–721Google Scholar
  62. Sundin J, Rosenqvist G, Myhren S, Berglund A (2016) Algal turbidity hampers ornament perception, but not expression, in a sex-role-reversed pipefish. Ethology 122:215–225. CrossRefGoogle Scholar
  63. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183. CrossRefGoogle Scholar
  64. Wilkinson CR (1999) Global and local threats to coral reef functioning and existence: review and predictions. Mar Freshw Res 50:867–878. CrossRefGoogle Scholar
  65. Wong BBM, Candolin U, Lindström K (2007) Environmental deterioration compromises socially enforced signals of male quality in three-spined sticklebacks. Am Nat 170:184–189. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environment Science and PolicyUniversity of California, DavisDavisUSA
  2. 2.Animal Behavior Graduate Group and Center for Population BiologyUniversity of California, DavisDavisUSA

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