Advertisement

Oecologia

, Volume 170, Issue 1, pp 47–55 | Cite as

Interactive influence of biotic and abiotic cues on the plasticity of preferred body temperatures in a predator–prey system

  • Radovan Smolinský
  • Lumír Gvoždík
Physiological ecology - Original research

Abstract

The ability to modify phenotypes in response to heterogeneity of the thermal environment represents an important component of an ectotherm’s non-genetic adaptive capacity. Despite considerable attention being dedicated to the study of thermally-induced developmental plasticity, whether or not interspecific interactions shape the plastic response in both a predator and its prey remains unknown. We tested several predictions about the joint influence of predator/prey scents and thermal conditions on the plasticity of preferred body temperatures (T p) in both actors of this interaction, using a dragonfly nymphs–newt larvae system. Dragonfly nymphs (Aeshna cyanea) and newt eggs (Ichthyosaura alpestris) were subjected to fluctuating cold and warm thermal regimes (7–12 and 12–22°C, respectively) and the presence/absence of a predator or prey chemical cues. Preferred body temperatures were measured in an aquatic thermal gradient (5–33°C) over a 24-h period. Newt T p increased with developmental temperature irrespective of the presence/absence of predator cues. In dragonflies, thermal reaction norms for T p were affected by the interaction between temperature and prey cues. Specifically, the presence of newt scents in cold regime lowered dragonfly T p. We concluded that predator–prey interactions influenced thermally-induced plasticity of T p but not in a reciprocal fashion. The occurrence of frequency-dependent thermal plasticity may have broad implications for predator–prey population dynamics, the evolution of thermal biology traits, and the consequences of sustaining climate change within ecological communities.

Keywords

Aeshna Biotic interactions Preferred temperature Reciprocal plasticity Thermal acclimation Triturus 

Notes

Acknowledgments

We thank to four anonymous reviewers for their valuable comments on the previous versions of this paper. This work was funded by a grant from the Czech Science Foundation (P506/10/2170) and the Czech Ministry of Education (LC06073). The Agency for Nature Conservation and Landscape Protection of the Czech Republic issued permission to capture the newts (1154/ZV/2008).

Supplementary material

442_2012_2283_MOESM1_ESM.pdf (16 kb)
Supplementary material 1 (PDF 16 kb)

References

  1. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326PubMedCrossRefGoogle Scholar
  2. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordGoogle Scholar
  3. Angilletta MJ, Bennett AF, Guderley H, Navas CA, Seebacher F, Wilson RS (2006) Coadaptation: a unifying principle in evolutionary thermal biology. Physiol Biochem Zool 79:282–294PubMedCrossRefGoogle Scholar
  4. Blois C (1985) The larval diet of three anisopteran (Odonata) species. Freshw Biol 15:505–514CrossRefGoogle Scholar
  5. Blumberg MS, Lewis SJ, Sokoloff G (2002) Incubation temperature modulates post-hatching thermoregulatory behavior in the Madagascar ground gecko, Paroedura pictus. J Exp Biol 205:2777–2784PubMedGoogle Scholar
  6. Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:e1000357. doi: 10.1371/journal.pbio.1000357 PubMedCrossRefGoogle Scholar
  7. Deere JA, Chown SL (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. Am Nat 168:630–644PubMedCrossRefGoogle Scholar
  8. Dijkstra KDB (2006) Field guide to the dragonflies of Britain and Europe. British Wildlife, DorsetGoogle Scholar
  9. Downes S (2001) Trading heat and food for safety: costs of predator avoidance in a lizard. Ecology 82:2870–2881CrossRefGoogle Scholar
  10. Downes S, Shine R (1998) Heat, safety or solitude? Using habitat selection experiments to identify a lizard’s priorities. Anim Behav 55:1387–1396PubMedCrossRefGoogle Scholar
  11. Dvořák J, Gvoždík L (2010) Adaptive accuracy of temperature oviposition preferences in newts. Evol Ecol 24:1115–1127CrossRefGoogle Scholar
  12. Feder ME, Pough FH (1975) Temperature selection by the red-backed salamander, Plethodon c. cinereus (Green) (Caudata: Plethodontidae). Comp Biochem Physiol A 50:91–98PubMedCrossRefGoogle Scholar
  13. Fry FEJ (1947) Effects of the environment on animal activity. Univ Toronto Stud Biol Ser 55:1–62Google Scholar
  14. Gabriel W, Lynch M (1992) The selective advantage of reaction norms for environmental tolerance. J Evol Biol 5:41–59CrossRefGoogle Scholar
  15. Ghalambor CK, Mckay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407CrossRefGoogle Scholar
  16. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331PubMedCrossRefGoogle Scholar
  17. Gliwicz MZ (1986) Predation and the evolution of vertical migration in zooplankton. Nature 320:746–748CrossRefGoogle Scholar
  18. Griffiths RA (1996) Newts and salamanders of Europe. Academic, LondonGoogle Scholar
  19. Gvoždík L (2003) Postprandial thermophily in the Danube crested newt, Triturus dobrogicus. J Therm Biol 28:545–550CrossRefGoogle Scholar
  20. Gvoždík L (2011) Plasticity of preferred body temperatures as means of coping with climate change? Biol Lett. doi: 1098/rsbl.2011.0960 PubMedGoogle Scholar
  21. Gvoždík L, Van Damme R (2008) The evolution of thermal performance curves in semi-aquatic newts: thermal specialists on land and thermal generalists in water? J Therm Biol 33:395–403CrossRefGoogle Scholar
  22. Gvoždík L, Puky M, Šugerková M (2007) Acclimation is beneficial at extreme test temperatures in the Danube crested newt, Triturus dobrogicus (Caudata, Salamandridae). Biol J Linn Soc 90:627–636CrossRefGoogle Scholar
  23. Hadamová M, Gvoždík L (2011) Seasonal acclimation of preferred body temperatures improves the opportunity for thermoregulation in newts. Physiol Biochem Zool 84:166–174PubMedCrossRefGoogle Scholar
  24. Herczeg G, Herrero A, Saarikivi J, Gonda A, Jantti M, Merilä J (2008) Experimental support for the cost-benefit model of lizard thermoregulation: the effects of predation risk and food supply. Oecologia 155:1–10PubMedCrossRefGoogle Scholar
  25. Hertz PE, Huey RB, Stevenson RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. Am Nat 142:796–818PubMedCrossRefGoogle Scholar
  26. Hirvonen H (1999) Shifts in foraging tactics of larval damselflies: effects of prey density. Oikos 86:443–452CrossRefGoogle Scholar
  27. Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12., Physiology C, Physiological ecology. Academic, London, pp 25–91Google Scholar
  28. Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137:S91–S115CrossRefGoogle Scholar
  29. Huey RB, Berrigan D, Gilchrist GW, Herron JC (1999) Testing the adaptive significance of acclimation: a strong inference approach. Am Zool 39:323–336Google Scholar
  30. Hutchison VH, Hill LG (1976) Thermal selection in the hellbender, Cryptobranchus alleganiensis, and the mudpuppy, Necturus maculosus. Herpetologica 32:327–331Google Scholar
  31. Iwami T, Kishida O, Nishimura K (2007) Direct and indirect induction of a compensatory phenotype that alleviates the costs of an inducible defense. PLoS ONE 2:e1084PubMedCrossRefGoogle Scholar
  32. Johnson TP, Bennett AF (1995) The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. J Exp Biol 198:2165–2175PubMedGoogle Scholar
  33. Kelsch SW, Neill WH (1990) Temperature preference versus acclimation in fishes—selection for changing metabolic optima. Trans Am Fish Soc 119:601–610CrossRefGoogle Scholar
  34. Kingsolver JG, Gomulkiewicz R (2003) Environmental variation and selection on performance curves. Integr Comp Biol 43:470–477PubMedCrossRefGoogle Scholar
  35. Kishida O, Mizuta Y, Nishimura K (2006) Reciprocal phenotypic plasticity in a predator–prey interaction between larval amphibians. Ecology 87:1599–1604PubMedCrossRefGoogle Scholar
  36. Kopp M, Gavrilets S (2006) Multilocus genetics and the coevolution of quantitative traits. Evolution 60:1321–1336PubMedGoogle Scholar
  37. Kopp M, Tollrian R (2003) Reciprocal phenotypic plasticity in a predator–prey system: inducible offences against inducible defences? Ecol Lett 6:742–748CrossRefGoogle Scholar
  38. Krstevska B, Hoffmann AA (1994) The effects of acclimation and rearing conditions on the response of tropical and temperate populations of Drosophila melanogaster and Drosophila simulans to a temperature gradient (Diptera, Drosophilidae). J Insect Behav 7:279–288CrossRefGoogle Scholar
  39. Kurdíková V, Smolinský R, Gvoždík L (2011) Mothers matter too. Benefits of temperature oviposition preferences in newts. PLoS ONE 6:e23842PubMedCrossRefGoogle Scholar
  40. Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446PubMedCrossRefGoogle Scholar
  41. Luttbeg B, Hammond JI, Sih A (2009) Dragonfly larvae and tadpole frog space use games in varied light conditions. Behav Ecol 20:13–21CrossRefGoogle Scholar
  42. Měráková E, Gvoždík L (2009) Thermal acclimation of swimming performance in newt larvae: the influence of diel temperature fluctuations during embryogenesis. Funct Ecol 23:989–995CrossRefGoogle Scholar
  43. Michimae H, Wakahara M (2002) A tadpole-induced polyphenism in the salamander Hynobius retardatus. Evolution 56:2029–2038PubMedGoogle Scholar
  44. Mitchell WA, Angilletta MJ (2009) Thermal games: frequency-dependent models of thermal adaptation. Funct Ecol 23:510–520CrossRefGoogle Scholar
  45. Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989CrossRefGoogle Scholar
  46. Orizaola G, Braña F (2004) Hatching responses of four newt species to predatory fish chemical cues. Ann Zool Fenn 41:635–645Google Scholar
  47. O’Steen S, Bennett AF (2003) Thermal acclimation effects differ between voluntary, maximum, and critical swimming velocities in two cyprinid fishes. Physiol Biochem Zool 76:484–496PubMedCrossRefGoogle Scholar
  48. Padilla DK, Adolph SC (1996) Plastic inducible morphologies are not always adaptive: The importance of time delays in a stochastic environment. Evol Ecol 10:105–117CrossRefGoogle Scholar
  49. Pfennig DW (1992) Polyphenism in spadefoot toad tadpoles as a locally adjusted evolutionarily stable strategy. Evolution 46:1408–1420CrossRefGoogle Scholar
  50. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540CrossRefGoogle Scholar
  51. Šamajová P, Gvoždík L (2009) The influence of temperature on diving behaviour in the alpine newt, Triturus alpestris. J Therm Biol 34:401–405Google Scholar
  52. Šamajová P, Gvoždík L (2010) Inaccurate or disparate temperature cues? Seasonal acclimation of terrestrial and aquatic locomotor capacity in newts. Funct Ecol 24:1023–1030CrossRefGoogle Scholar
  53. Schmidt BR, Van Buskirk J (2005) A comparative analysis of predator-induced plasticity in larval Triturus newts. J Evol Biol 18:415–425PubMedCrossRefGoogle Scholar
  54. Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512PubMedCrossRefGoogle Scholar
  55. Sih A (2005) Predator-prey space use as an emergent outcome of a behavioral response race. In: Barbosa P, Castellanos I (eds) Ecology of predator–prey interactions. Oxford University Press, New York, pp 240–255Google Scholar
  56. Smith LD, Palmer AR (1994) Effects of manipulated diet on size and performance of brachyuran crab claws. Science 264:710–712PubMedCrossRefGoogle Scholar
  57. Smolinský R, Gvoždík L (2009) The ontogenetic shift in thermoregulatory behaviour of newt larvae: testing the ‘enemy-free temperatures’ hypothesis. J Zool 279:180–186CrossRefGoogle Scholar
  58. Stevenson RD, Peterson CR, Tsuji JS (1985) The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiol Zool 58:46–57Google Scholar
  59. Stich HB, Lampert W (1981) Predator evasion as an explanation of diurnal vertical migration by zooplankton. Nature 293:396–398CrossRefGoogle Scholar
  60. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. http://www.R-project.org. R Foundation for Statistical Computing, Vienna
  61. Tollrian R (1995) Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76:1691–1705CrossRefGoogle Scholar
  62. Valladares F, Gianoli E, Gomez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763PubMedCrossRefGoogle Scholar
  63. Van Buskirk J (2002) Phenotypic lability and the evolution of predator-induced plasticity in tadpoles. Evolution 56:361–370PubMedGoogle Scholar
  64. Van Buskirk J (2011) Amphibian phenotypic variation along a gradient in canopy cover: species differences and plasticity. Oikos 120:906–914CrossRefGoogle Scholar
  65. Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585CrossRefGoogle Scholar
  66. Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028CrossRefGoogle Scholar
  67. Van Buskirk J, McCollum SA, Werner EE (1997) Natural selection for environmentally induced phenotypes in tadpoles. Evolution 51:1983–1992CrossRefGoogle Scholar
  68. Van Damme R, Bauwens D, Verheyen R (1991) The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizard Lacerta vivipara Jacquin. Funct Ecol 5:507–517CrossRefGoogle Scholar
  69. Watson S, Russell AP (2000) A posthatching developmental staging table for the long-toed salamander, Ambystoma macrodactylum krausei. Amphib Reptilia 21:143–154Google Scholar
  70. Wilhoft DC, Anderson JD (1960) Effect of acclimation on the preferred body temperature of the lizard, Sceloporus occidentalis. Science 131:610–611PubMedCrossRefGoogle Scholar
  71. Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6:e325. doi: 10.1371/journal.pbio.0060325 CrossRefGoogle Scholar
  72. Wilson RS, James RS, Johnston IA (2000) Thermal acclimation of locomotor performance in tadpoles and adults of the aquatic frog Xenopus laevis. J Comp Physiol B 170:117–124PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of Population BiologyInstitute of Vertebrate Biology AS CRKoněšínCzech Republic

Personalised recommendations