Skip to main content
Log in

Morphological differentiation among populations of Rhinella marina (Amphibia: Anura) in western Mexico

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

Abstract

Conspecific populations inhabiting different environments may exhibit morphological differences, potentially reflecting differential local adaptation. In anuran amphibians, morphology of the pelvis and hindlimbs may often experience strong selection due to effects on locomotion. In this study, we used the cane toad Rhinella marina to test the hypothesis that populations experiencing a higher abundance of predators should suffer higher mortality rates and exhibit morphological traits associated with enhanced locomotor performance (narrower pelvis and head, longer pelvis and hindlimbs, shorter presacral vertebral column). We investigated inter-population variation in survival rate, abundance of predators, and body shape across five populations in rivers in western Mexico. We conducted (1) mark-recapture experiments to calculate survival rates, (2) linear transects with point counts to estimate abundance of predatory spiders, snakes, and birds, and (3) geometric morphometric analyses to investigate body shape variation. We found significant differences among populations in survival rates, abundance of predators, and body shape. However, these three variables were not necessarily inter-related. Increased predator abundance did not result in decreased survival rates, suggesting other causes of mortality affect these populations. While some morphological differences supported our predictions (trend for longer pelvis, shorter presacral vertebral column, and narrower head in sites with increased abundance of spiders and snakes), other aspects of morphology did not. We discuss alternative explanations for the lack of clear associations between predation, survival, and morphology.

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
Fig. 6

Similar content being viewed by others

References

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Academiai Kiado, Budapest, pp 267–281

    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 

  • Alvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195

    Article  Google Scholar 

  • Arendt JD (2003) Reduced burst speed is a cost of rapid growth in anuran tadpoles: problems of autocorrelation and inferences about growth rates. Funct Ecol 17:328–334

    Article  Google Scholar 

  • Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59:1014–1022

    Article  Google Scholar 

  • Beck CW, Congdon JD (2000) Effects of age and size at metamorphosis on performance and metabolic rates of southern toad, Bufo terrestris, metamorphs. Funct Ecol 14:32–38

    Article  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data. Cambridge University Press, New York

    Google Scholar 

  • Brönmark C, Miner JG (1992) Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348–1350

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Cabrera-Guzmán E, Crossland MR, Brown GP, Shine R (2013) Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina) PLoS One 8:e70121

    Google Scholar 

  • Capellán E, Nicieza AG (2007) Trade-offs across life stages: does predator-induced hatching plasticity reduce anuran post-metamorphic performance? Evol Ecol 21:445–458

    Article  Google Scholar 

  • Ceballos G, Oliva G (2005) Los mamíferos silvestres de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Fondo de Cultura Económica, México

    Google Scholar 

  • Chadwell BA, Hartwell HJ, Peters SE (2002) Comparison of isometric contractile properties in hindlimb extensor muscles of the frogs Rana pipiens and Bufo marinus: Functional correlations with differences in hopping performance. J Morphol 251:309–322

    Article  PubMed  Google Scholar 

  • Child T, Phillips BL, Brown GP, Shine R (2008) The spatial ecology of cane toads (Bufo marinus) in tropical Australia: why do metamorph toads stay near the water? Austral Ecol 33:630–640

    Article  Google Scholar 

  • Choi I, Shim JH, Lee YS, Ricklefs RE (2000) Scaling of jumping performance in anuran amphibians. J Herpetol 34:222–227

    Article  Google Scholar 

  • Choi I, Shim JH, Ricklefs RE (2003) Morphometric relationships of take-off speed in anuran amphibians. J Exp Zool 299A:99–102

    Article  Google Scholar 

  • Cohen MP, Alford RA (1993) Growth, survival and activity patterns of recently metamorphosed Bufo marinus. Wildl Res 20:1–13

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Dayton GH, Saenz D, Baum KA, Langerhans RB, DeWitt TJ (2005) Body shape, burst speed, and escape behavior of larval anurans. Oikos 111:582–591

    Article  Google Scholar 

  • del Hoyo J, Elliot A, Sargarat J (1992) Handbook of the birds of the world. Vol. 1. Ostrich to ducks, vol 1. Lynx Edicions, Barcelona

    Google Scholar 

  • del Hoyo J, Elliot A, Sargarat J (1996) Handbook of the birds of the world. Vol. 3. Hoatzin to auks. Lynx Edicions, Barcelona

    Google Scholar 

  • del Hoyo J, Elliot A, Sargarat J (2001) Handbook of the birds of the world. Vol. 6. Mousebirds to Hornbills. Lynx Edicions, Barcelona

    Google Scholar 

  • DeWitt TJ, Langerhans RB (2003) Multiple prey traits, multiple predators: keys to understanding complex community dynamics. J Sea Res 49:143–155

    Article  Google Scholar 

  • DeWitt TJ, Schneider SM (2004) Phenotypic variation from single genotypes. In: Dewitt TJ, Schneider SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University, New York, pp 1–9

    Google Scholar 

  • Duellman WE, Trueb L (1996) Musculoskeletal system. In: Duellman WE, Trueb L (eds) Biology of amphibians. Johns Hopkins University Press, Baltimore, pp 289–365

    Google Scholar 

  • Eklöv P, Svanbäck R (2006) Predation risk influences adaptive morphological variation in fish populations. Am Nat 167:440–452

    Article  PubMed  Google Scholar 

  • Emerson SB (1978) Allometry and jumping in frogs: helping the twain to meet. Evolution 32:551–564

    Article  Google Scholar 

  • Emerson SB (1985) Jumping and leaping. In: Hildebrand ME, Bramble DM, Rome KF (eds) Functional vertebrate morphology. 2002. The design of vertebrate muscular systems: comparative and integrative approaches. Clinical orthopaedics and related research. Philadelphia, vol 403, pp S59–S76

  • Ficetola GF, De Bernardi F (2006) Trade-off between larval development rate and post-metamorphic traits in the frog Rana latastei. Evol Ecol 20:143–158

    Article  Google Scholar 

  • Flores EE, Stevens M, Moore AJ, Blount JD (2013) Diet, development and the optimization of warning signals in post-metamorphic green and black poison frogs. Funct Ecol 27:816–829

    Article  Google Scholar 

  • Freeland WJ, Kerin SH (1991) Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildl Res 18:431–443

    Article  Google Scholar 

  • García A, Ceballos G (1994) Field guide to the reptiles and amphibians of the Jalisco Coast, Mexico. Fundación ecológica de Cuixmala, A.C. Instituto de Biología, UNAM, México

    Google Scholar 

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

    Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae. 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 

  • Harrison JF, Cease AJ, VandenBrooks JM, Albert T, Davidowitz G (2013) Caterpillars selected for large body size and short development time are more susceptible to oxygen-related stress. Ecol Evol 3:1305–1316

    Article  PubMed Central  PubMed  Google Scholar 

  • Hawley TJ (2009) The ecological significance and incidence of intraguild predation and cannibalism among anurans in ephemeral tropical pools. Copeia 4:748–757

    Article  Google Scholar 

  • Höglund J, Säterberg L (1989) Sexual selection in common toads: correlates with age and body size. J Evol Biol 2:367–372

    Article  Google Scholar 

  • Hossie TJ, Ferland-Raymond B, Burness G, Murray DL (2010) Morphological and behavioural responses of frog tadpoles to perceived predation risk: a possible role for corticosterone mediation? Ecoscience 17:100–108

    Article  Google Scholar 

  • Johansson F, Lederer B, Lind MI (2010) Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. PLoS One 5:e11680

    Article  PubMed Central  PubMed  Google Scholar 

  • Johnson JB, Belk MC (2001) Predation environment predicts divergent life-history phenotypes among populations of the livebearing fish Brachyrhaphis rhabdophora. Oecologia 126:142–149

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Johnson JB, Zúñiga-Vega JJ (2009) Differential mortality drives life-history evolution and population dynamics in the fish Brachyrhaphis rhabdophora. Ecology 90:2243–2252

    Article  PubMed  Google Scholar 

  • Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope’s rule of phyletic size increase. Evolution 58:1608–1612

    PubMed  Google Scholar 

  • Langerhans RB (2006) Evolutionary consequences of predation: avoidance, escape, reproduction, and diversification. In: Elewa AMT (ed) Predation in organisms: a distinct phenomenon. Springer, Heidelberg, pp 177–220

    Google Scholar 

  • Langerhans RB (2009) Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis. J Evol Biol 22:1057–1075

    Article  CAS  PubMed  Google Scholar 

  • Langerhans RB (2010) Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish. Integr Comp Biol 50:1167–1184

    Article  PubMed  Google Scholar 

  • Langerhans RB, DeWitt TJ (2004) Shared and unique features of evolutionary diversification. Am Midl Nat 164:335–349

    Google Scholar 

  • Langerhans RB, Gifford ME (2009) Divergent selection, not life-history plasticity via food limitation, drives morphological divergence between predator regimes in Gambusia hubbsi. Evolution 63:561–567

    Article  PubMed  Google Scholar 

  • Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318

    PubMed  Google Scholar 

  • Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypothesis using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

    Article  Google Scholar 

  • Lever C (2001) The cane toad. The history and ecology of a successful colonist. Westbury Academic Publishing, Otley, West Yorkshire

    Google Scholar 

  • Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956

    Article  Google Scholar 

  • López LO, Woolrich-Piña GA, Lemos-Espinal JA (2009) La familia Bufonidae en México. Universidad Nacional Autónoma de México, Comisión Nacional para el Conocimiento y el Uso de la Biodiversidad, México

    Google Scholar 

  • Martof BS (1953) Territoriality in the green frog Rana clamitans. Ecology 34:165–174

    Article  Google Scholar 

  • McCollum SA, Van Buskirk J (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583–593

    Article  Google Scholar 

  • Menin M, Waldez F, Lima AP (2008) Temporal variation in the abundance and number of species of frogs in 10,000 ha of a forest in Central Amazonia, Brazil. S Am J Herpetol 3:68–81

    Article  Google Scholar 

  • Miller RR, Minckley WL, Norris SM (2005) Freshwater fishes of México. The University of Chicago Press, USA

    Google Scholar 

  • Mobley KB, Lussetti D, Johansson F, Englund G, Bokma F (2011) Morphological and genetic divergence in Swedish postglacial stickleback (Pungitius pungitius) populations. Evol Biol 11:287

    Google Scholar 

  • Nakazawa T, Ohba S, Ushio M (2013) Predator–prey body size relationships when predators can consume prey larger than themselves. Biol Lett 9:20121193

    Article  PubMed  Google Scholar 

  • Newman RA, Dunham AE (1994) Size at metamorphosis and water loss in a desert anuran (Scaphiopus couchii). Copeia 2:372–381

    Article  Google Scholar 

  • Ortiz-Santaliestra ME, Fernández-Benéiteza MJ, Marcob A (2012) Density effects on ammonium nitrate toxicity on amphibians. Survival, growth and cannibalism. Aquat Toxicol 110–111:170–176

    Article  PubMed  Google Scholar 

  • Pizzatto L, Shine R (2008) The behavioral ecology of cannibalism in cane toads (Bufo marinus). Behav Ecol Sociobiol 63:123–133

    Article  Google Scholar 

  • Putman RJ, Wratten SD (1984) Principles of ecology. University of California Press, Berkeley

    Google Scholar 

  • Relyea RA (2001) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82:1947–1955

    Article  Google Scholar 

  • Relyea RA, Hoverman JT (2003) The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596–604

    PubMed  Google Scholar 

  • Reznick DN, Bassar RD, Travis J, Helen Rodd F (2012) Life-history evolution in guppies VIII: the demographics of density regulation in guppies (Poecilia reticulata). Evolution 66:2903–2915

    Article  PubMed  Google Scholar 

  • Rodríguez-Palafox A, Corona AM (2002) Lista de artrópodos de la región de Chamela, Jalisco, México. In: Noguera FA, Vega-Rivera JH, García-Aldrete AN, Quesada-Avendaño M (eds) Historia natural de Chamela. Instituto de Biología, UNAM, México, pp 203–232

    Google Scholar 

  • Rohlf FJ (2006) TpsDig. Department of Ecology and Evolution, State University of New York, Stony Brook, New York

    Google Scholar 

  • Rohlf FJ (2007) TpsRelw. Department of Ecology and Evolution, State University of New York, Stony Brook, New York

    Google Scholar 

  • Rouse DJ, Bishop CA, Struger J (1999) Nitrogen pollution: an assessment of its threat to amphibian survival. Environ Health Perspect 107:799–803

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scoville AG, Pfrender ME (2010) Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc Nat Acad Sci 9:4260–4263

    Article  Google Scholar 

  • Solís F, Ibáñez R, Hammerson G, Hedges B, Diesmos A, Matsui M, Hero JM, Richards S, Coloma L, Ron S, La Marca E, Hardy J, Powell R, Bolaños F, Chaves G, Ponce P (2009) Rhinella marina. In: IUCN 2010. IUCN red list of threatened species. Version 2010.4. www.iucnredlist.org. Nov 2010

  • Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Oxford

    Google Scholar 

  • Steiner UK (2007) Investment in defense and cost of predator-induced defense along a resource gradient. Oecologia 152:201–210

    Article  PubMed  Google Scholar 

  • Stoks R, De Block M, Van de Meutter F, Johansson F (2005) Predation cost of rapid growth: behavioural coupling and physiological decoupling. J Anim Ecol 74:708–715

    Article  Google Scholar 

  • Tejedo M, Semlitsch RD, Hotz H (2000) Covariation of morphology and jumping performance in newly metamorphosed water frogs: effects of larval growth history. Copeia 2:448–458

    Article  Google Scholar 

  • Tejedo M, Marangoni F, Pertoldi C, Richter-Boix A, Laurila A, Orizaola G, Nicieza AG, Álvarez D, Gomez-Mestre I (2010) Contrasting effects of environmental factors during larval stage on morphological plasticity in post-metamorphic frogs. Clim Res 43:31–39

    Article  Google Scholar 

  • Teplitsky C, Plenet S, Lena JP, Mermet N, Malet E, Joly P (2005) Escape behaviour and ultimate causes of specific induced defences in an anuran tadpole. J Evol Biol 18:180–190

    Article  CAS  PubMed  Google Scholar 

  • Tingley R, Greenlees MJ, Shine R (2012) Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121:1959–1965

    Article  Google Scholar 

  • Toledo LF (2003) Predation on seven South American anuran species by water bugs (Belostomatidae). Phyllomedusa 2:105–108

    Article  Google Scholar 

  • Toledo LF (2005) Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetol Rev 36:395–400

    Google Scholar 

  • Toledo LF, Haddad CFB (2009) Colors and some morphological traits as defensive mechanisms in anurans. Int J Zool 2009:1–12

    Article  Google Scholar 

  • Toledo LF, Ribeiro RS, Haddad CFB (2007) Anurans as prey: an exploratory analysis and size relationships between predators and their prey. J Zool 27:170–177

    Article  Google Scholar 

  • Touchon JC, Jiménez RR, Abinette SH, Vonesh JR, Warkentin KM (2013) Behavioral plasticity mitigates risk across environments and predators during anuran metamorphosis. Oecologia. Online publication date: 4 July 2013

  • Tracy CR, Christian KA, Burnip N, Austin BJ, Cornall A, Iglesias S, Reynolds SJ, Tixier T, Noëne CL (2013) Thermal and hydric implications of diurnal activity by a small tropical frog during the dry season. Austral Ecol 38:476–483

    Article  Google Scholar 

  • Uller T, Olsson M (2010) Offspring size and timing of hatching determine survival and reproductive output in a lizard. Oecologia 162:663–671

    Article  PubMed  Google Scholar 

  • Vamosi SM (2003) The presence of other fish species affects speciation in three spine sticklebacks. Evol Ecol Res 5:717–730

    Google Scholar 

  • Vincent SE, Moon BR, Shine R, Herrel A (2006) The functional meaning of ‘‘prey size’’ in water snakes (Nerodia fasciata, Colubridae). Oecologia 147:204–211

    Article  CAS  PubMed  Google Scholar 

  • Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD (2005) Many-to-one mapping of form to function: a general principle in organismal design? Integr Comp Biol 45:256–262

    Article  PubMed  Google Scholar 

  • Walsh MR, Reznick DN (2009) Phenotypic diversification across an environmental gradient: a role for predators and resource availability on the evolution of life histories. Evolution 12:1–13

    Google Scholar 

  • Ward-Fear G, Brown GP, Shine R (2010) Factors affecting the vulnerability of cane toads (Bufo marinus) to predation by ants. Biol J Linn Soc 99:738–751

    Article  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S138

    Article  Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a primer. Elsevier Academic Press, London

    Google Scholar 

  • Zug GR (1972) Anuran locomotion: structure and function. 1. Preliminary observations on the relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 1972:613–624

    Article  Google Scholar 

  • Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resume of native populations. Smithson Contrib Zool 284:1–58

    Google Scholar 

Download references

Acknowledgments

This research was funded by the Dirección General de Asuntos del Personal Académico-Universidad Nacional Autónoma de México (UNAM) through the project PAPIIT IN206309-3. Hugh Drummond and Zenón Cano-Sanatana provided helpful advice. Fieldwork was assisted by F. Reyes-Rodríguez, A. Hernández-Rosas, A. Molina-Moctezuma, E. García-Molina, A. Arellano, E. Romero-García, and I. González-Leyva. I. Castellanos provided help on the estimation on predator abundance. We thank the personnel of the Biosphere Reserva Chamela-Cuixmala: E.Ramírez-García, A. Miranda, E. Robles-Jiménez, J. M. Robles-Jiménez, D. Verduzco-Robles, I. Rubio-Crisoto, and N. Barocio. J. Zúñiga-Guitérrez provided logistic support. This paper constitutes a partial fulfillment of the Graduate Program in Biological Sciences of the Universidad Nacional Autónoma de México. R. Vega-Trejo acknowledges the scholarship and financial support provided by the Consejo Nacional de Ciencia y Tecnología and UNAM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Regina Vega-Trejo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vega-Trejo, R., Zúñiga-Vega, J.J. & Langerhans, R.B. Morphological differentiation among populations of Rhinella marina (Amphibia: Anura) in western Mexico. Evol Ecol 28, 69–88 (2014). https://doi.org/10.1007/s10682-013-9667-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-013-9667-6

Keywords

Navigation