Skip to main content
Log in

Spatial variation in abiotic and biotic factors in a floodplain determine anuran body size and growth rate at metamorphosis

  • Population ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Body size at metamorphosis is a critical trait in the life history of amphibians. Despite the wide-spread use of amphibians as experimental model organisms, there is a limited understanding of how multiple abiotic and biotic factors affect the variation in metamorphic traits under natural conditions. The aim of our study was to quantify the effects of abiotic and biotic factors on spatial variation in the body size of tadpoles and size at metamorphosis of the European common toad (Bufo b. spinosus). Our study population was distributed over the riverbed (active tract) and the fringing riparian forest of a natural floodplain. The riverbed had warm ponds with variable hydroperiod and few predators, whereas the forest had ponds with the opposite characteristics. Spatial variation in body size at metamorphosis was governed by the interactive effects of abiotic and biotic factors. The particular form of the interaction between water temperature and intraspecific tadpole density suggests that abiotic factors laid the foundation for biotic factors: intraspecific density decreased growth only at high temperature. Predation and intraspecific density jointly reduced metamorphic size. Interspecific density had a negligible affect on body size at metamorphosis, suggesting weak inter-anuran interactions in the larval stage. Population density at metamorphosis was about one to two orders of magnitudes higher in the riverbed ponds than in the forest ponds, mainly because of lower tadpole mortality. Based on our results, we conclude that ponds in the riverbed appear to play a pivotal role for the population because tadpole growth and survival is best in this habitat.

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

Similar content being viewed by others

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with image J. Biophotonics Int 11:36–42

    Google Scholar 

  • Alford RA (1999) Ecology: resource use, competition, and predation. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. The University of Chicago Press, Chicago, pp 240–278

    Google Scholar 

  • Alford RA, Harris RN (1988) Effects of larval growth history on anuran metamorphosis. Am Nat 131:91–106

    Article  Google Scholar 

  • Allan JD (1976) Life history patterns in zooplankton. Am Nat 110:165–180

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Amézquita A, Lüddecke H (1999) Correlates of intrapopulational variation in size at metamorphosis of the high-Andean frog Hyla labialis. Herpetologica 55:295–303

    Google Scholar 

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

    Article  Google Scholar 

  • Angilletta MJ, Niewarowski PH, Dunham AE, Leache AD, Porter WP (2004b) Bergman’s clines in ectotherms: illustrating a life-history perspective with sceloporine lizards. Am Nat 164:E168–E183

    Article  Google Scholar 

  • Anholt BR, Werner EE, Skelly DK (2000) Effect of food and predators on the activity of four larval ranid frogs. Ecology 81:3509–3521

    Article  Google Scholar 

  • Arscott DB, Tockner K, van der Nat D, Ward JV (2002) Aquatic habitat dynamics along a braided alpine river ecosystem (Tagliamento River, northeast Italy). Ecosystems 5:802–814

    Google Scholar 

  • Berrigan D, Charnov EL (1994) Reaction norms for age and size at maturity in response to temperature: a puzzle for life historians. Oikos 70:474–478

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Biek R, Funk WC, Maxell BA, Mills LS (2002) What is missing in amphibian decline research: insights from ecological sensitivity analysis. Conserv Biol 16:728–734

    Article  Google Scholar 

  • Bradshaw WE, Johnson K (1995) Initiation of metamorphosis in the pitcher-plant mosquito: effects of larval growth history. Ecology 76:2055–2065

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Charnov EL, Gillooly JF (2004) Size and temperature in the evolution of fish life histories. Integr Comp Biol 44:494–497

    Article  Google Scholar 

  • Denton JS, Beebee TJC (1997) Effects of predator interactions, prey palatability and habitat structure on survival of natterjack toad Bufo calamita larvae in replicated semi-natural ponds. Ecography 20:166–174

    Article  Google Scholar 

  • Dunson WA, Travis J (1991) The role of abiotic factors in community organization. Am Nat 138:1067–1091

    Article  Google Scholar 

  • Giacoma C, Castellano S (2006) Bufo bufo. In: Sindaco R, Doria G, Razzetti E, Bernini F (eds) Atlante degli anfibi e dei rettili d’Italia/Atlas of Italian amphibians and reptiles. Societas Herpetologica Italica/Edizione Polistampa, Florence, pp 302–305

    Google Scholar 

  • Goater CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75:2264–2274

    Article  Google Scholar 

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

    Google Scholar 

  • Gray MJ, Smith LM (2005) Influence of land use on postmetamorphic body size of playa lake amphibians. J Wildl Manage 69:515–524

    Article  Google Scholar 

  • Indermaur L, Schaub M, Jokela J, Tockner K, Schmidt BR (2010) Differential response to abiotic conditions and predation risk, rather than competition avoidance, determine breeding site selection by anurans. Ecography. doi: 10.1111/j.1600-0587.2010.06150.x (in press)

  • Kuhn J (2001) Biologie der Erdkröte (Bufo bufo) in einer Wildflusslandschaft (obere Isar, Bayern). Z Feldherpetol 8:31–42

    Google Scholar 

  • Lampo M, De Leo GA (1998) The invasion ecology of the toad Bufo marinus: from South America to Australia. Ecol Appl 8:388–396

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Laurila A (1998) Breeding habitat selection and larval performance of two anurans in freshwater rock-pools. Ecography 21:484–494

    Article  Google Scholar 

  • Loehle C (2006) Species abundance distributions result from body size–energetics relationships. Ecology 87:2221–2226

    Article  PubMed  Google Scholar 

  • Loman J (2001) Intraspecific competition in tadpoles of Rana arvalis: does it matter in nature? A field experiment. Popul Ecol 43:253–263

    Article  Google Scholar 

  • Loman J (2002) Rana temporaria metamorph production and population dynamics in the field: effects of tadpole density, predation and pond drying. J Nat Conserv 10:95–107

    Article  Google Scholar 

  • McPeek MA, Peckarsky BL (1998) Life histories and the strengths of species interactions: combining mortality, growth, and fecundity effects. Ecology 79:867–879

    Article  Google Scholar 

  • Mitchell-Olds T (1987) Analysis of local variation in plant size. Ecology 68:82–87

    Article  Google Scholar 

  • Moehrlin GS, Juliano SA (1998) Plasticity of insect reproduction: testing models of flexible and fixed development in response to different growth rates. Oecologia 115:492–500

    Article  Google Scholar 

  • Newman RA (1988) Adaptive plasticity in development of Scaphiopus couchii tadpoles in desert ponds. Evolution 42:774–783

    Article  Google Scholar 

  • Petranka JW (1984) Sources of interpopulational variation in growth-responses of larval salamanders. Ecology 65:1857–1865

    Article  Google Scholar 

  • Petranka JW, Sih A (1986) Environmental instability, competition, and density-dependent growth and survivorship of a stream-dwelling salamander. Ecology 67:729–736

    Article  Google Scholar 

  • Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661

    Article  Google Scholar 

  • Reading CJ, Clarke RT (1999) Impacts of climate and density on the duration of the tadpole stage of the common toad Bufo bufo. Oecologia 121:310–315

    Article  Google Scholar 

  • Rohr JR, Sager T, Sesterhenn TM, Palmer BD (2006) Exposure, postexposure, and density-mediated effects of atrazine on amphibians: breaking down net effects into their parts. Environ Health Perspect 114:46–50

    Article  CAS  PubMed  Google Scholar 

  • Runge JP, Runge MC, Nichols JD (2006) The role of local populations within a landscape context: defining and classifying sources and sinks. Am Nat 167:925–938

    Article  Google Scholar 

  • Savage VM, Gillooly JF, Brown JH, West GB, Charnov EL (2004) Effects of body size and temperature on population growth. Am Nat 163:429–441

    Article  PubMed  Google Scholar 

  • Semlitsch RD, Scott DE, Pechmann JHK, Gibbons CA (1996) Structure and dynamics of an amphibian community. Evidence from a 16-year study of a natural pond. In: Cody ML, Smallwood LA (eds) Long-term studies of vertebrate communities. Academic Press, San Diego, pp 217–248

    Chapter  Google Scholar 

  • Skelly DK (2002) Experimental venue and estimation of interaction strength. Ecology 83:2097–2101

    Article  Google Scholar 

  • Skelly DK, Kiesecker JM (2001) Venue and outcome in ecological experiments: manipulations of larval anurans. Oikos 94:198–208

    Article  Google Scholar 

  • Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322

    Article  Google Scholar 

  • Skelly DK, Freidenburg LK, Kiesecker JM (2002) Forest canopy and the performance of larval amphibians. Ecology 83:983–992

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Tockner K, Klaus I, Baumgartner C, Ward JV (2006) Amphibian diversity and nestedness in a dynamic floodplain river (Tagliamento, NE-Italy). Hydrobiologia 565:121–133

    Article  Google Scholar 

  • Travis J, Keen WH, Juilianna J (1985) The role of relative body size in a predatory–prey relationship between dragonfly naiads and larval anurans. Oikos 45:59–65

    Article  Google Scholar 

  • Twombly S (1996) Timing of metamorphosis in a freshwater crustacean: comparison with anuran models. Ecology 77:1855–1866

    Article  Google Scholar 

  • Van Buskirk J (2005) Local and landscape influence on amphibian occurrence and abundance. Ecology 86:1936–1947

    Article  Google Scholar 

  • Van Buskirk J (2009) Natural variation in morphology of larval amphibians: phenotypic plasticity in nature? Ecol Monogr 79:681–705

    Article  Google Scholar 

  • Viertel B (1980) Überlebensraten und Mortalität bei Erdkrötenlarven (Bufo bufo L.) im Freiland. Salamandra 16:19–37

    Google Scholar 

  • Ward JV et al (1999) A reference river system for the Alps: the “Fiume Tagliamento”. Regul Rivers Res Manage 15:63–75

    Article  Google Scholar 

  • Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363

    Article  Google Scholar 

  • Werner EE (1998) Ecological experiments and research program in community ecology. In: Resetarits WJ, Bernardo J (eds) Ecological experiments: issues and perspectives. Oxford University Press, New York, pp 3–26

    Google Scholar 

  • Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93

    Article  Google Scholar 

  • Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Academic Press, San Diego

    Google Scholar 

Download references

Acknowledgments

We are grateful to Simone Blaser, Pascal Meuwly and Ursina von Planta for field data collection. The comments of Ross Alford, two anonymous referees and Sandra Hangartner improved the manuscript, as did the editing by Christopher Robinson and Sarah Poynton. All methods applied conform to the ethical and animal care guidelines issued by national (Ministerio dell’Ambiente e della Tutela del Territorio, Direzione per la Protezione della Natura, Roma) and regional (Direzione Centrale Risorse Agricole, Forestali e Naturali, Regione Friuli Venezia Giulia, Udine) authorities in Italy that kindly provided permits. The project was funded by the MAVA Foundation (Switzerland).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lukas Indermaur.

Additional information

Communicated by Ross Alford.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 648 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Indermaur, L., Schmidt, B.R., Tockner, K. et al. Spatial variation in abiotic and biotic factors in a floodplain determine anuran body size and growth rate at metamorphosis. Oecologia 163, 637–649 (2010). https://doi.org/10.1007/s00442-010-1586-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1586-4

Keywords

Navigation