Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Effects of size and temperature on developmental time

Abstract

Body size and temperature are the two most important variables affecting nearly all biological rates and times1,2,3,4,5,6,7. The relationship of size and temperature to development is of particular interest, because during ontogeny size changes and temperature often varies8,9,10,11,12. Here we derive a general model, based on first principles of allometry and biochemical kinetics, that predicts the time of ontogenetic development as a function of body mass and temperature. The model fits embryonic development times spanning a wide range of egg sizes and incubation temperatures for birds and aquatic ectotherms (fish, amphibians, aquatic insects and zooplankton). The model also describes nearly 75% of the variation in post-embryonic development among a diverse sample of zooplankton. The remaining variation is partially explained by stoichiometry, specifically the whole-body carbon to phosphorus ratio. Development in other animals at other life stages is also described by this model. These results suggest a general definition of biological time that is approximately invariant and common to all organisms.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The effect of incubation temperature on mass-corrected embryonic development time for amphibians (a), fish (b), multivoltine aquatic insects (c) and zooplankton (d) incubated at different constant temperature.
Figure 2: Plot as Fig. 1 but for marine fishes in the field (see Methods).
Figure 3: Plot as Fig. 1 but for aquatic ectotherms (data from Fig. 1a–d) and birds.
Figure 4: Plot as Fig. 1 but for post-embryonic (hatching to adult) development time for zooplankton (rotifers, copepods and cladocerans) incubated at different constant temperatures ranging from 5 to 30 °C.
Figure 5: The relationship between deviations for the fitted line in Fig. 4 (that is, Tc/(1 + (Tc/273)) versus t/m1/4) and whole-body carbon to phosphorus ratios (C:P) for adults of these species.

Similar content being viewed by others

References

  1. Schmidt-Nielsen, K. Scaling: Why is Animal Size So Important? (Cambridge Univ. Press, Cambridge, 1983).

    Google Scholar 

  2. Calder, W. A. III Size, Function, and Life History (Harvard Univ. Press, Cambridge, Massachusetts, 1984).

    Google Scholar 

  3. Peters, R. H. The Ecological Implications of Body Size (Cambridge Univ. Press, Cambridge, 1983).

    Book  Google Scholar 

  4. Calder, W. A. III in Avian Energetics (ed. Paynter, R. A.) 86–151 (Nutall Ornithology Club 15, Cambridge, 1974).

    Google Scholar 

  5. Lindstedt, S. L. & Calder, W. A. III Body size, physiological time, and longevity of homeothermic animals. Q. Rev. Biol. 56, 1–16 (1981).

    Article  Google Scholar 

  6. Somero, G. S. in Handbook of Physiology Vol. 13 (ed. Dantzler, W. H.) 1391–1444 (Oxford Univ. Press, New York, 1997).

    Google Scholar 

  7. Cossins, A H. & Bowler, K. Temperature Biology of Animals (Chapman and Hall, London, 1987).

    Book  Google Scholar 

  8. Gillooly, J. F. & Dodson, S. I. The relationship of neonate mass and incubation temperature to embryonic development time in a range of animal taxa. J. Zool. 251, 369–375 (2000).

    Article  Google Scholar 

  9. Gillooly, J. F. & Dodson, S I. The relationship of egg size and incubation temperature to embryonic development time in univoltine and multivoltine aquatic insects. Freshwat. Biol. 44, 595–604 (2000).

    Article  Google Scholar 

  10. Pauly, D. & Pullin, R. S. V. Hatching time in spherical, pelagic, marine fish eggs in response to temperature and egg size. Eviron. Biol. Fishes 22, 261–271 (1988).

    Article  Google Scholar 

  11. Heinroth, O. Die beziehungen swischen vogelgewicht, eigewicht, gelegewicht und brutdauer. J. Ornithol. 70, 172–285 (1912).

    Article  Google Scholar 

  12. Gillooly, J. F. Effect of body size and temperature on generation time in zooplankton. J. Plankt. Res. 22, 241–251 (2000).

    Article  Google Scholar 

  13. West, G. B., Brown, J. H. & Enquist, B. J. A general model for the origin of allometric scaling laws in biology. Science 276, 122–126 (1997).

    Article  CAS  Google Scholar 

  14. West, G. B., Brown, J. H. & Enquist, B. J. A general model for ontogenetic growth. Nature 413, 628–631 (2001).

    Article  ADS  CAS  Google Scholar 

  15. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).

    Article  ADS  CAS  Google Scholar 

  16. Scott, W. B. & Scott, M. G. Atlantic fishes of Canada. Can. Bull. Fish. Aquat. Sci. 219 (1988).

  17. Vetter, R. A. H. Ecophysiological studies on citrate-synthase: I: Enzyme regulation of selected crustaceans with regard to temperature adaptation. J. Comp. Physiol. B 165, 46–55 (1995).

    Article  CAS  Google Scholar 

  18. Raven, J. A. & Geider, R. J. Temperature and algal growth. New Phytol. 110, 441–461 (1988).

    Article  CAS  Google Scholar 

  19. McLeese, J. M. & Eales, J. G. 3,5,3′ Triiodo-L-thyroxine and L-thyroxine uptake into red blood cells of rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 102, 47–55 (1965).

    Article  Google Scholar 

  20. Elser, J. J., Dobberfuhl, D., MacKay, N. A. & Schampel, J. H. Organism size, life history and N:P stoichiometry: toward a unified view of cellular and ecosystem processes. Bioscience 46, 674–684 (1996).

    Article  Google Scholar 

  21. Hessen, D. O. & Lyche, A. Inter- and intraspecific variations in zooplankton element composition. Arch. Hydrobiol. 121, 343–353 (1991).

    Google Scholar 

  22. Main, T. M., Dobberfuhl, D. R. & Elser, J. J. N:P stoichiometry and ontogeny of crustacean zooplankton: A test of the growth rate hypothesis. Limnol. Oceanogr. 42, 1474–1478 (1997).

    Article  ADS  CAS  Google Scholar 

  23. Foran, J. A. A comparison of the life-history features of a temperate and a subtropical Daphnia species. Oikos 46, 185–193 (1986).

    Article  Google Scholar 

  24. Hanazato, T. & Yasuno, M. Effect of temperature in the laboratory studies on growth, egg development and first parturition of five species of cladocera. Jpn. J. Limnol. 46, 185–191 (1985).

    Article  Google Scholar 

  25. Andersen, D. H. & Benke, A. C. Growth and reproduction of the cladoceran Ceriodaphnia dubia from a forested floodplain swamp. Limnol. Oceanogr. 39, 1517–1527 (1994).

    Article  ADS  Google Scholar 

  26. Kankaala, P. & Wulff, F. Experimental studies on temperature-dependent embryonic and postembryonic developmental rates of Bosmina longispina maritime (Cladocera) in the Baltic. Oikos 36, 137–146 (1981).

    Article  Google Scholar 

  27. Maier, G. The effect of temperature on the development, reproduction, and longevity of two common cyclopoid copepods, Eucyclops serrulatus (Fischer) and Cyclops strennus (Fischer). Hydrobiologia 203, 165–175 (1990).

    Article  Google Scholar 

  28. Munro, I. G. The effect of temperature on the development of egg, naupliar and copepodite stages of two species of copepods, Cyclops vicinus (Uljanin) and Eudiaptomus gracilis (Sars). Oecologia 16, 355–367 (1974).

    Article  ADS  CAS  Google Scholar 

  29. Geiling, W. T. & Campbell, R. S. The effect of temperature on the development rate of the major life stages of Diaptomus pallidus (Herrick). Limnol. Oceanogr. 17, 304–307 (1972).

    Article  ADS  Google Scholar 

  30. Andersen, T. & Hessen, D. O. Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol. Oceanogr. 36, 807–814 (1991).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank S. Dodson, M. Ernest, C. M. Del Rio, E. Toolson, T. Turner and B. Wolf for comments or discussions that improved this manuscript. J.F.G. thanks J. S. Gillooly for support and encouragement. J.F.G., G.B.W. and J.H.B. are grateful for the support of the Thaw Charitable Trust and a Packard Interdisciplinary Science Grant; V.M.S., G.B.W. and J.H.B. for the support of the National Science Foundation; and E.L.C. for the support received as a MacArthur Fellow. G.B.W. also thanks the Theoretical Physics Department at Oxford Unviersity for its hospitality, and the EPSRC for support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James. F. Gillooly.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gillooly, J., Charnov, E., West, G. et al. Effects of size and temperature on developmental time. Nature 417, 70–73 (2002). https://doi.org/10.1038/417070a

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/417070a

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing