Skip to main content
Log in

Altitudinal variation in body size in Bufo minshanicus supports Bergmann’s rule

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

According to Bergmann’s rule, in endothermic species, body sizes of individuals tend to be larger in colder climates compared to those in warmer climates. Some ectotherms, including amphibians, have also been found to conform to this rule. However, the validity of this rule is disputed, as it is uncertain whether Bergmann’s clines are generally applicable to all anuran species. Here we studied altitudinal variation in mean body size, egg size, age, and growth rate in Bufo minshanicus across six altitudes in the eastern Tibetan Plateau. Our results showed that mean body size increased with increasing altitude, which is consistent with Bergmann’s rule. Toads from higher altitudes also tended to have faster growth rates and older mean ages of reproductively mature adults, but did not have larger egg sizes. We suggest that, as growth rate is positively correlated with altitude, and it contributes to body size variation more than mean age does, then this explains why this species follows Bergmann’s rule.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams DC, Church JO (2008) Amphibians do not follow Bergmann’s rule. Evolution 62:413–420

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Angilletta MJ, Niewiarowski PH, Dunham AE et al (2004) Bergmann’s clines in ectotherms: illustrating a life-history perspective with sceloporine lizards. Am Nat 164:168–183

    Article  Google Scholar 

  • Ashton KG (2002a) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Glob Ecol Biogeogr 11:505–523

    Article  Google Scholar 

  • Ashton KG (2002b) Do amphibians follow Bergmann’s rule? Can J Zool 80:708–716

    Article  Google Scholar 

  • Ashton KG, Feldman CR (2003) Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151–1163

    Article  PubMed  Google Scholar 

  • Badyaev AV, Ghalambor CK (2001) Evolution of life histories along elevational gradients: trade-off between parental care and fecundity. Ecology 82:2948–2960

    Article  Google Scholar 

  • Beck E, Kottke I, Bendix J, Makeschin F, Mosandl R (2008) Gradients in a tropical mountain ecosystem—asynthesis. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of ecuador. Ecological studies, vol 198. Springer, Berlin, Heidelberg, pp 451–463

    Chapter  Google Scholar 

  • Belk MC, Houston DD (2002) Bergmann’s rule in ectotherms: a test using freshwater fishes. Am Nat 160:803–808

    Article  PubMed  Google Scholar 

  • Bergmann C (1847) Über die verhältnisse der warmeökonomie der thiere zuihrer grosse. Gott Stud 1:595–708

    Google Scholar 

  • Berven KA (1982) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution 36:962–983

    PubMed  Google Scholar 

  • Blackburn TM, Hawkins BA (2004) Bergmann’s rule and the mammal fauna of North America. Ecography 27:715–724

    Article  Google Scholar 

  • Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: consequences of an energetic definition of fitness. Am Nat 142:573–584

    Article  CAS  PubMed  Google Scholar 

  • Conover DO, Present TMC (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83:316–324

    Article  PubMed  Google Scholar 

  • de Queiroz A, Ashton KG (2004) The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann’s rule in tetrapods. Evolution 58:1674–1684

    Article  PubMed  Google Scholar 

  • Dziminski MA, Robert JD (2006) Fitness consequences of variable maternal provisioning in quacking frogs (Crinia georgiana). J Evol Biol 19:144–155

    Article  CAS  PubMed  Google Scholar 

  • Fei L, Ye CY (2001) The colour handbook of amphibians of Sichuan. China Forestry Publishing House, Beijing

    Google Scholar 

  • Halliday TR, Verrell PA (1988) Body size and age in amphibians and reptiles. J Herpet 22:253–265

    Article  Google Scholar 

  • Jin L, Chen C, Liao WB (2017) Altitudinal variation in body size and age in male spot-legged treefrog (Polypedates megacephalus). Russ J Ecol 48:476–481

    Article  Google Scholar 

  • Kaplan RH, King EG (1997) Egg size is a developmentally plastic trait: evidence from long term studies in the frog Bombina orientalis. Herpetologica 53:149–165

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Laugen AT, Laurila A, Jönsson KI et al (2005) Do common frogs (Rana temporaria) follow Bergmann’s rule? Evol Ecol Res 7:717–731

    Google Scholar 

  • Levinton JS (1983) The latitudinal compensation hypothesis: growth data and a model of latitudinal growth differentiation based upon energy budgets. I. Interspecific comparison of Ophryotrocha (Polychaeta: Dorvilleidae). Biol Bull-us 165:686–698

    Article  Google Scholar 

  • Levinton JS, Monahan RK (1983) The latitudinal compensation hypothesis: growth data and a model of latitudinal growth differentiation based upon energy budgets. II. Intraspecific comparisons between subspecies of Ophryotrocha puerilis. Biol Bull 165:699–707

    Article  PubMed  Google Scholar 

  • Li ST, Wu X, Li DY, Lou SL, Mi ZP, Liao WB (2013) Body size variation of Odorous Frog (Odorrana grahami) across altitudinal gradients. Herpetol J 23:187–192

    Google Scholar 

  • Liao WB (2011) A skeletochronlogical estimate of age in a population of the Siberian Wood Frog, Rana amurensis, from northeastern China. Acta Herpetol 6:237–245

    Google Scholar 

  • Liao WB, Lu X (2011) Variation in body size, age and growth in a subtropical treefrog (Rhacophorus omeimontis) along an altitudinal gradient in western China. Ethol Ecol Evol 23:248–261

    Article  Google Scholar 

  • Liao WB, Lu X (2012) Adult body size = f(initial size + growth rate × age): explaining the proximate cause of Bergmann’s cline in a toad along altitudinal gradients. Evol Ecol 26:579–590

    Article  Google Scholar 

  • Liao WB, Zhou CQ, Yang ZS et al (2010a) Age, size and growth in two populations of the dark-spotted frog Rana nigromaculata at different altitudes in southwestern China. Herpetol J 20:77–82

    Google Scholar 

  • Liao WB, Zhou CQ, Yang ZS, Hu JC, Lu X (2010b) Age, size and growth in two populations of the dark-spotted frog Rana nigromaculata at different altitudes in southwestern China. Herpetol J 20:77–82

    Google Scholar 

  • Liao WB, Lu X, Shen YW, Hu JC (2011) Age structure and body size of two populations of the rice frog Rana limnocharis from different altitudes. Ital J Zool 78:215–221

    Article  Google Scholar 

  • Liao WB, Lu X, Jehle R (2014) Altitudinal variation in reproductive investment and trade-off between egg size and clutch size in the Andrew’s Toad (Bufo andrewsi). J Zool 293:84–91

    Article  Google Scholar 

  • Liao WB, Luo Y, Lou SL, Lu D, Jehle R (2016) Geographic variation in life-history traits: growth season affects age structure, egg size and clutch size in Andrew’s toad (Bufo andrewsi). Front Zool 13:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Feng H, Jin L, Mi ZP, Zhou ZM, Liao WB (2018) Latitudinal variation in body size in Fejervarya limnocharis supports the inverse of Bergmann’s rule. Anim Biol 68:113–128

    Article  Google Scholar 

  • Lu X, Li B, Liang JJ (2006) Comparative demography of a temperate anuran, Rana chensinensis, along a relatively fine elevational gradient. Can J Zool 84:1789–1795

    Article  Google Scholar 

  • Ma XY, Lu X, Merilä J (2009) Altitudinal decline of body size in a Tibetan frog Nanorana parkeri. J Zool 279:364–371

    Article  Google Scholar 

  • Marangoni F, Tejedo M (2008) Variation in body size and metamorphic traits of Iberian spadefoot toads over a short geographic distance. J Zool 275:97–105

    Article  Google Scholar 

  • Matthews KR, Miaud C (2007) A skeletochronological study of the age structure, growth, and longevity of a mountain yellow-legged frog, Rana muscosa, in the Sierra Nevada, California. Copeia 2007:986–993

    Article  Google Scholar 

  • Mayr E (1956) Geographical character gradients and climatic adaptation. Evolution 10:105–108

    Article  Google Scholar 

  • McCarthy MA, Parris KM (2004) Clarifying the effect of toe clipping on frogs with Bayesian statistics. J Appl Ecol 41:780–786

    Article  Google Scholar 

  • Miaud C, Guyetant R, Elmberg J (1999) Variations in life-history traits in the common frog Rana temporaria (Amphibia: Anura): a literature review and new data from the French Alps. J Zool 249:61–73

    Article  Google Scholar 

  • Morrison C, Hero JM (2003) Geographic variation in life-history characteristics of amphibians: a review. J Anim Ecol 72:270–279

    Article  Google Scholar 

  • Oromi N, Sanuy D, Sinsch U (2012) Altitudinal variation of demographic life-history traits does not mimic latitudinal variation in natterjack toads (Bufo calamita). Zoology 115:30–37

    Article  PubMed  Google Scholar 

  • Ryser J (1996) Comparative life histories of a low- and a high-elevation population of the common frog Rana temporaria. Amphibia-Reptilia 17:183–195

    Article  Google Scholar 

  • Sinsch U, Marangoni F, Oromi N et al (2010) Proximate mechanisms determining size variability in natterjack toads. J Zool Lond 281:272–281

    Google Scholar 

  • Smirina EM (1994) Age determination and longevity in amphibians. Gerontology 40:133–146

    Article  CAS  PubMed  Google Scholar 

  • Walters RJ, Hassall M (2006) The temperature-size rule in ectotherms: may a general explanation exist after all? Am Nat 167:510–523

    Article  PubMed  Google Scholar 

  • Yamahira K, Conover DO (2002) Intra- vs. interspecific latitudinal variation in growth: adaptation to temperature or seasonality? Ecology 83:1252–1262

    Article  Google Scholar 

  • Yu T, Lu X (2013) Body size variation of four latitudinally-separated populations of a toad species: age and growth rate as the proximate determinants. Integr Zool 8:315–323

    Article  PubMed  Google Scholar 

  • Yu TL, Busam M, Wang DL, Chen K (2016) Plasticity of metamorphic traits in a high-altitude toad: interactive effects of food level and temperature. Amphibia-Reptilia 37:33–43

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are very grateful to Wen-hua Qi, Yan-Liang Han and Ji-zu Ning for their assistance in the field. We especially thank the parents and uncle of TLY for helping during all phases of the data collection. All animals were collected under the guidelines for animal care in China. Handling and processing of frogs followed approved protocols from Animal Scientific Procedures Act 1988 by the State Department of China. The Gahai-Zecha National Nature Reserve Management Bureau approved this project (approval number GHZCRMB/03-212014), and gave permission for fieldwork. The study was funded by Emergency Management Program of National Natural Science Foundation of China (Grant no. 31741019), Natural Science Foundation of Henan Province of China (Grant no. 182300410019), Foundation for University Key Teacher of Henan province (Grant no. 2016GGJS-098) and Program for Innovative Research Team (in Science and Technology) in universities of Henan Province (Grant no. 17IRTSTHN019). The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tong Lei Yu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Supplementary material 2 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, T.L., Wang, D.L., Busam, M. et al. Altitudinal variation in body size in Bufo minshanicus supports Bergmann’s rule. Evol Ecol 33, 449–460 (2019). https://doi.org/10.1007/s10682-019-09984-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-019-09984-1

Keywords

Navigation