Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae

Abstract

Organisms normally grow at a sub-maximal rate. After experiencing a period of arrested growth, individuals often show compensatory growth responses by modifying their life-history, behaviour and physiology. However, the strength of compensatory responses may vary across broad geographic scales as populations differ in their exposition to varying time constraints. We examined differences in compensatory growth strategies in common frog (Rana temporaria) populations from southern and northern Sweden. Tadpoles from four populations were reared in the laboratory and exposed to low temperature to evaluate the patterns and mechanisms of compensatory growth responses. We determined tadpoles’ growth rate, food intake and growth efficiency during the compensation period. In the absence of arrested growth conditions, tadpoles from all the populations showed similar (size-corrected) growth rates, food intake and growth efficiency. After being exposed to low temperature for 1 week, only larvae from the northern populations increased growth rates by increasing both food intake and growth efficiency. These geographic differences in compensatory growth mechanisms suggest that the strategies for recovering after a period of growth deprivation may depend on the strength of time constraints faced by the populations. Due to the costs of fast growth, only populations exposed to the strong time constraints are prone to develop fast recovering strategies in order to metamorphose before conditions deteriorate. Understanding how organisms balance the cost and benefits of growth strategies may help in forecasting the impact of fluctuating environmental conditions on life-history strategies of populations likely to be exposed to increasing environmental variation in the future.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Abrams PA, Leimar O, Nylin S, Wiklund C (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am Nat 147:381–395

    Article  Google Scholar 

  2. Ali M, Nicieza A, Wotton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190

    Article  Google Scholar 

  3. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Book  Google Scholar 

  4. Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  6. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177

    Article  Google Scholar 

  7. Benavides AG, Cancino JM, Ojeda FP (1994) Ontogenetic changes in gut dimension and macroalgal digestibility in the marine herbivorous fish, Aplodactylus punctatus. Funct Ecol 8:46–51

    Article  Google Scholar 

  8. Beniston M, Stephenson DB, Christensen OB, Ferro CAT, Frei C, Goyette S, Halsnaes K, Holt T, Jylhä K, Koffi B, Palutikof J, Schöll R, Semmler T, Woth K (2007) Future extreme events in European climate: an exploration of regional climate model projections. Clim Change 81:71–95

    Article  Google Scholar 

  9. Berger D, Gotthard K (2008) Time stress, predation risk and diurnal-nocturnal foraging trade-offs in larval prey. Behav Ecol Sociobiol 62:1655–1663

    Article  Google Scholar 

  10. Dahl E, Orizaola G, Nicieza AG, Laurila A (2012) Time constraints and flexibility of growth strategies: geographic variation in catch-up growth responses in amphibian larvae. J Anim Ecol 81:1233–1243

    PubMed  Article  Google Scholar 

  11. De Block M, Stoks R (2008) Compensatory growth and oxidative stress in a damselfly. Proc R Soc Lond B 275:781–785

    Article  Google Scholar 

  12. De Block M, Slos S, Johansson F, Stoks R (2008) Integrating life history and physiology to understand latitudinal size variation in a damselfly. Ecography 31:115–123

    Article  Google Scholar 

  13. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    PubMed  Article  Google Scholar 

  14. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074

    CAS  PubMed  Article  Google Scholar 

  15. Finch CE, Kirkwood TBL (2000) Change, development, and ageing. Oxford University Press, Oxford

    Google Scholar 

  16. Fraker ME (2008) The effect of hunger on the strength and duration of the antipredator behavioral response of green frog (Rana clamitans) tadpoles. Behav Ecol Sociobiol 62:1201–1205

    Article  Google Scholar 

  17. Gasc JP (1997) Atlas of amphibians and reptiles in Europe. Societas Europaea Herpetologica and Muséum National d′Histoire Naturelle (IEGB/SPN), Paris

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

    Google Scholar 

  19. 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

    Article  Google Scholar 

  20. Hector KL, Nakagawa S (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol 81:583–593

    PubMed  Article  Google Scholar 

  21. Horat P, Semlitsch RD (1994) Effects of predation risk and hunger on the behavior of two species of tadpoles. Behav Ecol Sociobiol 34:393–401

    Article  Google Scholar 

  22. Jobling M (2010) Are compensatory growth and catch-up growth two sides of the same coin? Aquacult Int 18:501–510

    Article  Google Scholar 

  23. Johansson F, Stoks R, Rowe L, De Block M (2001) Life-history plasticity in a damselfly: effect of combined time and biotic constraints. Ecology 82:1857–1869

    Article  Google Scholar 

  24. Johansson MJ, Primmer CR, Merilä J (2006) History vs. current demography: explaining the genetic population structure of the common frog (Rana temporaria). Mol Ecol 15:975–983

    CAS  PubMed  Article  Google Scholar 

  25. Kapoor BC, Smith H, Verighina IA (1975) The alimentary canal and digestion in teleosts. Adv Mar Biol 13:109–239

    CAS  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  27. Laurila A, Lindgren B, Laugen AT (2008) Antipredator defenses along a latitudinal gradient in Rana temporaria. Ecology 89:1399–1413

    PubMed  Article  Google Scholar 

  28. Lee W-S, Monaghan P, Metcalfe N (2012) The patterns of early growth trajectories affects adult breeding performance. Ecology 93:902–912

    PubMed  Article  Google Scholar 

  29. Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. In: Moller AP, Milinski M, Slater P (eds) Advances in the study of behaviour, vol 27., Stress and behavior. Academic, London, pp 215–290

    Google Scholar 

  30. 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

    CAS  PubMed  Article  Google Scholar 

  31. Lindgren B, Laurila A (2009) Physiological variation along latitudinal gradients: standard metabolic rate in Rana temporaria tadpoles. Biol J Linn Soc 98:217–224

    Article  Google Scholar 

  32. Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:155–176

    Article  Google Scholar 

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

    Google Scholar 

  34. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    PubMed  Article  Google Scholar 

  35. Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940

    PubMed  Article  Google Scholar 

  36. Metcalfe NB, Bull CD, Mangel M (2002) Seasonal variation in catch-up growth reveals state-dependent somatic allocations in salmon. Evol Ecol Res 4:871–881

    Google Scholar 

  37. Orizaola G, Dahl E, Nicieza AG, Laurila A (2013) Larval life history and anti-predator strategies are affected by breeding phenology in an amphibian. Oecologia 171:873–881

    PubMed  Article  Google Scholar 

  38. Parmesan C (2006) Ecological and evolutionary responses of recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  39. Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Article  Google Scholar 

  40. Relyea RA, Auld JR (2004) Having the guts to compete: how intestinal plasticity explain costs of inducible defences. Ecol Lett 7:869–875

    Article  Google Scholar 

  41. Richter-Boix A, Teplitsky C, Rogell B, Laurila A (2010) Local selection modifies phenotypic divergence in Rana temporaria tadpoles in the presence of gene flow. Mol Ecol 19:716–731

    PubMed  Article  Google Scholar 

  42. Roark AM, Bjorndal KA, Bolten AB (2009) Compensatory responses to food restriction in juvenile green turtles (Chelonia mydas). Ecology 90:2524–2534

    PubMed  Article  Google Scholar 

  43. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427

    Article  Google Scholar 

  44. Schultz ET, Lankford TE, Conover DO (2002) The covariance of routine and compensatory juvenile growth rates over a seasonality gradient in a coastal fish. Oecologia 133:501–509

    Article  Google Scholar 

  45. Scott DE, Casey ED, Donovan MF, Lynch TK (2007) Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival. Oecologia 153:521–532

    PubMed  Article  Google Scholar 

  46. Skalski GT, Picha ME, Gilliam JF, Borski RJ (2005) Variable intake, compensatory growth, and increased growth efficiency in fish: models and mechanisms. Ecology 86:1452–1462

    Article  Google Scholar 

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

    Article  Google Scholar 

  48. Sogard SM, Olla BL (2002) Contrasts in the capacity and underlying mechanisms for compensatory growth in two pelagic marine fishes. Mar Ecol Prog Ser 243:165–177

    Article  Google Scholar 

  49. Steiner UK (2007) Linking antipredator behaviour, ingestion, gut evacuation and costs of predator-induced responses in tadpoles. Anim Behav 74:1473–1479

    Article  Google Scholar 

  50. Stevens DJ, Hansell MH, Monaghan P (2000) Developmental trade-offs and life histories: strategic allocation of resources in caddis flies. Proc R Soc Lond B 267:1511–1515

    CAS  Article  Google Scholar 

  51. Stoks R, De Block M, Slos S, Van Doorslaer W, Rolff J (2006) Time constraints mediate predator-induced plasticity in immune function, condition, and life history. Ecology 87:809–815

    PubMed  Article  Google Scholar 

  52. Stoks R, Swillen I, De Block M (2012) Behaviour and physiology shape the growth accelerations associated with predation risk, high temperatures and southern latitudes in Ischnura damselfly larvae. J Anim Ecol 81:1034–1040

    PubMed  Article  Google Scholar 

  53. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272

    CAS  PubMed  Article  Google Scholar 

  54. Yearsley JM, Kyriazakis I, Gordon IJ (2004) Delayed costs of growth and compensatory growth rates. Funct Ecol 18:563–570

    Article  Google Scholar 

Download references

Acknowledgments

We thank Frank Johansson and Alfredo Nicieza for comments on a previous draft of the manuscript. The animals were collected with the permissions from the county authorities and the experiment was approved by the Ethical Committee for Animal Experiments in Uppsala County (C70/8). Our research was supported by Fundación Caja Madrid, Fundación Ramón Areces, Helge Ax:son Johnsons Stiftelse and Stiftelsen Oscar och Lili Lamms Minne (G.O.), Stiftelsen för Zoologisk Forskning (E.D.), and the Swedish Research Council (A.L.).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Germán Orizaola.

Additional information

Communicated by Ross Andrew Alford.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 26 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Orizaola, G., Dahl, E. & Laurila, A. Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae. Oecologia 174, 131–137 (2014). https://doi.org/10.1007/s00442-013-2754-0

Download citation

Keywords

  • Adaptive plasticity
  • Climate change
  • Food intake
  • Growth efficiency
  • Growth rates
  • Time constraints