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Oecologia

, Volume 181, Issue 1, pp 87–96 | Cite as

Linking reproduction, locomotion, and habitat use in the Trinidadian guppy (Poecilia reticulata)

  • Amanda I. Banet
  • Jon C. Svendsen
  • Kevin J. Eng
  • David N. Reznick
Behavioral ecology –original research

Abstract

Pregnancy inhibits locomotion, increases predation risk and may translate into reduced survival. The extent to which animals modify behavior in the wild to compensate for the locomotor costs of pregnancy remains poorly understood. We have investigated how reproductive allocation (RA—the proportion of body mass devoted to reproduction) affects locomotor performance and habitat use in Trinidadian guppy (Poecilia reticulata) populations from low- and high-predation regimes. During steady swimming, females with high RA had increased tail beat amplitudes, indicating increased swimming costs. Females with high RA also exhibited slower escape velocities, which may result in an increased risk of predation. In low-predation localities, females with high RA used habitats with a lower water velocity, suggesting that females may be modifying behavior to offset the locomotor costs of pregnancy. Habitat use in high-predation localities was severely restricted to areas without predators, which had a relatively slower water velocity with little or no variation in current. These results provide a link between the performance-related costs of reproduction and behavior in a natural setting and show that animals may compensate for reproductive traits that constrain locomotor performance by modifying habitat use.

Keywords

Swimming performance Poecilia reticulata Predation Reproductive costs Reproductive allocation 

Notes

Acknowledgments

This research was funded by an NSF Doctoral Dissertation Improvement Grant to A.I.B (DEB-0710185), an NSF FIBR Grant to D.N.R. (DEB-0623632EF), and a Grant from the Foundation for Science and Technology (FCT) in Portugal to J.C.S. (SFRH/BPD/89473/2012). The Idella Foundation provided travel funding to J.C.S. We thank Karin Nilsson for assistance in the field and Roslyn Dakin for advice on mixed models in R. Joel Trexler, Eric Sokol, J. Matt Hoch, Joseph Parkos, Clifton Ruehl, Doug Altshuler, Paolo Segre, and anonymous reviewers provided valuable comments on earlier versions of the manuscript.

Author contribution statement

AIB, DNR, and JCS conceived and designed the experiments. AIB and JCS performed the experiments. AIB and KJE analyzed the data. AIB wrote the manuscript. JCS and DNR provided editorial advice.

Compliance with ethical standards

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

References

  1. Bauwens D, Thoen C (1981) Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. J Anim Ecol 50:733. doi: 10.2307/4133 CrossRefGoogle Scholar
  2. Berger J (1991) Pregnancy incentives, predation constraints and habitat shifts: experimental and field evidence for wild bighorn sheep. Anim Behav 41:61–77. doi: 10.1016/S0003-3472(05)80503-2 CrossRefGoogle Scholar
  3. Brodie ED III (1989) Behavioral modification as a means of reducing the cost of reproduction. Am Nat 134:225–238. doi: 10.1086/284977 CrossRefGoogle Scholar
  4. Claireaux G, Couturier C, Groison A-L (2006) Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). J Exp Biol 209:3420–3428. doi: 10.1242/jeb.02346 CrossRefPubMedGoogle Scholar
  5. Coleman RM, Kutty V (2001) The predator of guppies on Trinidad is the pike cichlid Crenicichla frenata, not Crenicichla alta: a caution about working with cichlids. J Aquaricult Aquat Sci 9:89–92Google Scholar
  6. Domenici P, Blake R (1997) The kinematics and performance of fish fast-start swimming. J Exp Biol 200:1165–1178PubMedGoogle Scholar
  7. Drucker E, Jensen J (1996) Pectoral fin locomotion in the striped surfperch. I. Kinematic effects of swimming speed and body size. J Exp Biol 199:2235–2242PubMedGoogle Scholar
  8. Endler JA (1978) A predator’s view of animal color patterns. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology. Plenum Press, New York, pp 319–364CrossRefGoogle Scholar
  9. Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 73(3):959–970. doi: 10.2307/1940172 CrossRefGoogle Scholar
  10. Ghalambor CK, Reznick DN, Walker JA (2004) Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). Am Nat 164:38–50. doi: 10.1086/421412 CrossRefPubMedGoogle Scholar
  11. Haynes JL (1995) Standardized classification of poeciliid development for life-history studies. Copeia 1995:147–154. doi: 10.2307/1446809 CrossRefGoogle Scholar
  12. Herskin J, Steffensen JF (1998) Energy savings in sea bass swimming in a school: measurements of tail beat frequency and oxygen consumption at different swimming speeds. J Fish Biol 53:366–376. doi: 10.1111/j.1095-8649.1998.tb00986.x CrossRefGoogle Scholar
  13. Huey RB, Pianka ER (1981) Ecological consequences of foraging mode. Ecology 62:991–999Google Scholar
  14. Husak JF (2006) Do female collared lizards change field use of maximal sprint speed capacity when gravid? Oecologia 150:339–343. doi: 10.1007/s00442-006-0513-1 CrossRefPubMedGoogle Scholar
  15. Kvarnemo C, Moore GI, Jones AG (2007) Sexually selected females in the monogamous Western Australian seahorse. Proc R Soc B 274:521–525. doi: 10.1098/rspb.2006.3753 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Langerhans RB, Reznick DN (2010) Ecology and evolution of swimming performance in fishes: predicting evolution with biomechanics. In: Domenici P, Kapoor BG (eds) Fish locomotion: an etho-ecological perspective. Science Publishers, Enfield, pp 200–248CrossRefGoogle Scholar
  17. Lyon JP, Ryan TJ, Scroggie MP (2008) Effects of temperature on the fast-start swimming performance of an Australian freshwater fish. Ecol Freshw Fish 17:184–188. doi: 10.1111/j.1600-0633.2007.00244.x CrossRefGoogle Scholar
  18. Magnusson WE, de Paiva LJ, da Rocha RM et al (1985) The correlates of foraging mode in a community of Brazilian lizards. Herpetologica 41:324–332Google Scholar
  19. Plaut I (2002) Does pregnancy affect swimming performance of female Mosquitofish, Gambusia affinis? Funct Ecol 16:290–295. doi: 10.1046/j.1365-2435.2002.00638.x CrossRefGoogle Scholar
  20. Reznick D, Callahan H, Llauredo R (1996a) Maternal effects on offspring quality in poeciliid fishes. Am Zool 36:147–156. doi: 10.1093/icb/36.2.147 CrossRefGoogle Scholar
  21. Reznick DN, Iv MJB, Rodd FH, Ross P (1996b) Life-history evolution in guppies (Poecilia reticulata) 6. Differential mortality as a mechanism for natural selection. Evolution 50:1651. doi: 10.2307/2410901 CrossRefGoogle Scholar
  22. Rodewald AD (1998) Effects of gravidity on habitat use and antipredator behaviour in three-spined sticklebacks. J Fish Biol 52:973–984. doi: 10.1111/j.1095-8649.1998.tb00597.x CrossRefGoogle Scholar
  23. Roff DA (1992) Evolution of life histories: theory and analysis. Springer, Berlin Heidelberg New YorkGoogle Scholar
  24. Seigel RA, Huggins MM, Ford NB (1987) Reduction in locomotor ability as a cost of reproduction in gravid snakes. Oecologia 73:481–485. doi: 10.1007/BF00379404 CrossRefGoogle Scholar
  25. Shine R (1980) “Costs” of reproduction in reptiles. Oecologia 46:92–100. doi: 10.1007/BF00346972 CrossRefGoogle Scholar
  26. Shine R (1983) Reptilian viviparity in cold climates: testing the assumptions of an evolutionary hypothesis. Oecologia 57:397–405. doi: 10.1007/BF00377186 CrossRefGoogle Scholar
  27. Shine R, Bull J (1979) The evolution of live-bearing in lizards and snakes. Am Nat 113:905–923CrossRefGoogle Scholar
  28. Svendsen JC, Skov J, Bildsoe M, Steffensen JF (2003) Intra-school positional preference and reduced tail beat frequency in trailing positions in schooling roach under experimental conditions. J Fish Biol 62:834–846. doi: 10.1046/j.1095-8649.2003.00068.x CrossRefGoogle Scholar
  29. Svendsen JC, Banet AI, Christensen RHB et al (2013) Effects of intraspecific variation in reproductive traits, pectoral fin use and burst swimming on metabolic rates and swimming performance in the Trinidadian guppy (Poecilia reticulata). J Exp Biol 216:3564–3574. doi: 10.1242/jeb.083089 CrossRefPubMedGoogle Scholar
  30. Videler JJ, Wardle CS (1991) Fish swimming stride by stride: speed limits and endurance. Rev Fish Biol Fish 1:23–40. doi: 10.1007/BF00042660 CrossRefGoogle Scholar
  31. Vitt LJ, Congdon JD (1978) Body shape, reproductive effort, and relative clutch mass in lizards: resolution of a paradox. Am Nat 112:595–607. doi: 10.1086/283300 CrossRefGoogle Scholar
  32. Vitt L, Price H (1982) Ecological and evolutionary determinants of relative clutch mass in lizards. Herpetologica 38:237–255Google Scholar
  33. Walker JA, Ghalambor CK, Griset OL et al (2005) Do faster starts increase the probability of evading predators? Funct Ecol 19:808–815. doi: 10.1111/j.1365-2435.2005.01033.x CrossRefGoogle Scholar
  34. Wu W, Meijer OG, Lamoth CJC et al (2004) Gait coordination in pregnancy: transverse pelvic and thoracic rotations and their relative phase. Clin Biomech (Bristol, Avon) 19:480–488. doi: 10.1016/j.clinbiomech.2004.02.003 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Amanda I. Banet
    • 1
    • 2
    • 3
  • Jon C. Svendsen
    • 4
    • 5
  • Kevin J. Eng
    • 3
  • David N. Reznick
    • 3
  1. 1.Department of Biological SciencesCalifornia State UniversityChicoUSA
  2. 2.Department of Forest and Conservation SciencesUniversity of British ColumbiaVancouverCanada
  3. 3.Department of BiologyUniversity of CaliforniaRiversideUSA
  4. 4.Interdisciplinary Centre of Marine and Environmental Research (CIIMAR)University of PortoPortoPortugal
  5. 5.National Institute of Aquatic ResourcesTechnical University of Denmark (DTU)CharlottenlundDenmark

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