Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Population divergence in growth rate and antipredator defences in Rana arvalis

  • 280 Accesses

  • 59 Citations

Abstract

Growth and development rates often differ among populations of the same species, yet the factors maintaining this differentiation are not well understood. We investigated the antipredator defences and their efficiency in two moor frog Rana arvalis populations differing in growth and development rates by raising tadpoles in outdoor containers in the nonlethal presence and absence of three different predators (newt, fish, dragonfly larva), and by estimating tadpole survival in the presence of free-ranging predators in a laboratory experiment. Young tadpoles in both populations reduced activity in the presence of predators and increased hiding behaviour in the presence of newt and fish. Older tadpoles from the slow-growing Gotland population (G) had stronger hiding behaviour and lower activity in all treatments than tadpoles from the fast-growing Uppland population (U). However, both populations showed a plastic behavioural response in terms of reduced activity. The populations differed in induced morphological defences especially in response to fish. G tadpoles responded with relatively long and deep body, short tail and shallow tail muscle, whereas the responses in U tadpoles were often the opposite and closer to the responses induced by the other predators. U tadpoles metamorphosed earlier, but at a similar size to G tadpoles. There was no evidence that growth rate was affected by predator treatments, but tadpoles metamorphosed later and at larger size in the predator treatments. G tadpoles survived better in the presence of free-ranging predators than U tadpoles. These results suggest that in these two populations, low growth rate was linked with low activity and increased hiding, whereas high growth rate was linked with high activity and less hiding. The differences in behaviour may explain the difference in survival between the populations, but other mechanisms (i.e. differences in swimming speed) may also be involved. There appears to be considerable differentiation in antipredator responses between these two R. arvalis populations, as well as with respect to different predators.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2.
Fig. 3
Fig. 4

References

  1. Allison PD (1999) Logistic regression using the SAS® system. Theory and application. SAS institute Inc, Cary

  2. Altwegg R (2002) Predator-induced life-history plasticity under time constraints in pool frogs. Ecology 83:2542–2551

  3. Altwegg R, Reyer H-U (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882

  4. Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240

  5. Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234

  6. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:150–177

  7. Arendt JD (2003) Reduced burst speed is a cost of rapid growth in anuran tadpoles: problems of autocorrelation and inferences about growth rates. Funct Ecol 17:328–334

  8. Arendt JD, Wilson DS (2000) Population differences in the onset of cranial ossification in pumpkinseed (Lepomis gibbosus), a potential cost of rapid growth. Can J Fish Aquat Sci 54:1796–1801

  9. Arnqvist G, Johansson F (1998) Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larvae. Ecology 79:1847–1858

  10. Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599–1608

  11. Berven KA, Gill DE (1983) Interpreting geographic variation in life history traits. Am Zool 23:85–97

  12. Billerbeck JM, Lankford TE Jr, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates I Trade-offs with swimming performance in Menidia menidia. Evolution 55:1863–1872

  13. Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407

  14. Bookstein FL (1991) Morphometric tools for landmark data. Cambridge University Press, Cambridge

  15. Brommer JE (2003) Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc R Soc Lond B 271:S110–S113

  16. Conover DO, Schultz TA (1995) Phenotypic similarity and the evolutionary significance of countergradient selection. Trends Ecol Evol 10:248–252

  17. De Meester L (1993) Genotype, fish-mediated chemicals and phototactic behavior in Daphnia magna. Ecology 71:1467–1474

  18. DeWitt TJ, Robinson BW, Wilson DS (2000) Functional diversity among predators of a freshwater snail imposes an adaptive tradeoff for shell morphology. Evol Ecol Res 2:129–148

  19. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton

  20. Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D, Grossenbacher K, Haffner P, Lescure J, Martens H, Martinéz Rica JP, Oliveira ME, Sofianidou TS, Veith M, Zuiderwijk A (1997) Atlas of amphibians and reptiles in Europe. Societas Europaea Herpetologica and Muséum National d’Histoire Naturelle (IEGB/SPN), Paris

  21. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

  22. Gotthard K (2000) Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J Anim Ecol 69:896–902

  23. Gotthard K, Nylin S, Wiklund C (1994) Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99:281–289

  24. Gregory TR, Wood CM (1998) Individual variation and the interrelationships between swimming performance, growth rate and feeding in juvenile rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 55:1583–1590

  25. Huntingford FA, Wright PJ, Tierney JF (1994) Adaptive variation in antipredator behaviour in threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 277–296

  26. James AC, Partridge L (1998) Geographic variation in competitive ability in Drosophila melanogaster. Am Nat 151:530–537

  27. Jones M, Laurila A, Peuhkuri N, Piironen J, Seppä T (2003) Timing an ontogenetic niche shift: responses of emerging alevins to chemical cues from predators and competitors. Oikos 102:155–163

  28. Kolok AS, Oris JT (1995) The relationship between specific growth rate and swimming performance in male fathead minnows (Pimephales promelas). Can J Zool 73:2165–2167

  29. Lankford TE Jr, Billerbeck JM, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates II Trade-offs in vulnerability to predation in Menidia menidia. Evolution 55:1873–1881

  30. Lardner B (1998) Plasticity or fixed adaptive traits? Strategies for predation avoidance in Rana arvalis tadpoles. Oecologia 117:119–126

  31. Laugen AT, Laurila A, Räsänen K, Merilä J (2003) Latitudinal countergradient variation in the common frog (Rana temporaria) development rates---evidence for local adaptation. J Evol Biol 16:996–1005

  32. Laurila A, Kujasalo J, Ranta E (1998) Predator-induced changes in life history in two anuran tadpoles: effects of predator diet. Oikos 83:307–317

  33. Laurila A, Pakkasmaa S, Crochet P-A, Merilä J (2002) Predator--induced plasticity in early life history and morphology in two anuran species. Oecologia 132:524–530

  34. Lima SL (1998a) Stress and decision-making under the risk of predation: recent developments from behavioural, reproductive and ecological perspectives. Adv Stud Behav 27:215–290

  35. Lima SL (1998b) Nonlethal effects in the ecology of predator-prey interactions. BioScience 48:25–34

  36. Lindgren B, Laurila A (2005) Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria. J Evol Biol 18:820–828

  37. Kishida O, Nishimura K (2004) Bulgy tadpoles: inducible defense morph. Oecologia 140:414–421

  38. Magurran AE (1998) Population differentiation without speciation. Philos Trans R Soc Lond B 353:275–286

  39. Mangel M, Stamps J (2001) Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res 3:583–593

  40. McCollum SA, Van Buskirk J (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583–593

  41. Morin PJ (1985) Predation intensity, prey survival and injury frequency in an amphibian predator--prey interaction. Copeia 1985:638–644

  42. Munch SB, Conover DO (2003) Rapid growth results in increased susceptibility to predation in Menidia menidia. Evolution 57:2119–2127

  43. Nylin S, Gotthard K, Wiklund C (1996) Reaction norms for age and size at maturity in Lasiommata butterflies: predictions and tests. Evolution 50:1351–1358

  44. Odin H, Eriksson B, Perttu K (1983) Temperature climate maps for Swedish forestry. Swedish University of Agricultural Sciences, Uppsala

  45. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540

  46. Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93

  47. Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839

  48. Relyea RA (2005) The heritability of predator-induced defenses: traits, trait plasticities and genetic correlations. J Evol Biol 18:856–866

  49. Riechert SE, Hedrick AV (1990) Levels of predation and genetically based anti-predator behaviour in the spider, Agelenopsis aperta. Anim Behav 40:679–687

  50. Schoeppner NM, Relyea RA (2005) Damage, digestion and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512

  51. Sih A (1987) Predators and prey lifestyles: an evolutionary and ecological overview. In: Kerfoot WC, Sih A (eds) Predation. Direct and indirect impacts on aquatic communities. University Press of New England, Hanover, pp 203–224

  52. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

  53. Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Anim Behav 47:465–468

  54. Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350

  55. Smoker WW (1986) Variation of embryo developmental rate, fry growth, and disease susceptibility in hatchery stocks of chum salmon. Aquaculture 57:219–226

  56. Spitze K (1992) Predator-mediated plasticity of prey life-history and morphology: Chaoborus americanus predation on Daphnia pulex. Am Nat 139:229–247

  57. Storfer A, Sih A (1998) Gene flow and ineffective antipredator behavior in a stream-breeding salamander. Evolution 52:558–565

  58. Teplitsky C, Plénet S, Joly P (2003) Tadpoles’ responses to risk of fish introduction. Oecologia 134:270–277

  59. Teplitsky C, Plénet S, Léna J-P, Mermet N, Malet E, Joly P (2005) Escape behaviour and ultimate causes of specific induced defences in an anuran tadpole. J Evol Biol 18:180–190

  60. Tollrian R, Dodson SI (1999) Inducible defenses in Cladocera: constraints, costs and multipredator environments. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 177–202

  61. Tollrian R, Harvell CD (eds) (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

  62. Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489

  63. Van Buskirk J (2002) Phenotypic lability and the evolution of predator-induced plasticity in tadpoles. Evolution 56:361–370

  64. Van Buskirk J, McCollum SA (2000) Influence of tail shape on tadpole swimming performance. J Exp Biol 203:2149–2158

  65. Van Buskirk J, Saxer G (2001) Delayed costs of an induced defense in tadpoles? Morphology, hopping, and development rate at metamorphosis. Evolution 55:821–829

  66. Wilkinson L (2000) SYSTAT® for Windows®. Chicago

Download references

Acknowledgments

We thank Pierre-André Crochet, Katja Enberg, Maria Järvi-Laturi, Beatrice Lindgren, Outi Pihlajamäki and Katja Räsänen for field and laboratory assistance, and Nina Peuhkuri, Miguel Tejedo, Celine Teplitsky and an anonymous reviewer for helpful comments on the manuscript. The study was performed with the permission C 72/1 from Uppsala county ethical committee for animal experiments. Our research was funded by the Swedish Research Council (AL) and the Academy of Finland (SP, JM).

Author information

Correspondence to Anssi Laurila.

Additional information

Communicated by Roland Brandl

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Laurila, A., Pakkasmaa, S. & Merilä, J. Population divergence in growth rate and antipredator defences in Rana arvalis . Oecologia 147, 585–595 (2006). https://doi.org/10.1007/s00442-005-0301-3

Download citation

Keywords

  • Growth rate
  • Inducible defences
  • Plasticity
  • Population differentiation
  • Predation