Evolutionary Ecology

, Volume 28, Issue 1, pp 69–88 | Cite as

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

  • Regina Vega-Trejo
  • J. Jaime Zúñiga-Vega
  • R. Brian Langerhans
Original Paper


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.


Geometric morphometrics Mark-recapture Survival Predation Body shape 



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.


  1. 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 267–281Google Scholar
  2. Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882PubMedGoogle Scholar
  3. Alvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195CrossRefGoogle Scholar
  4. 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 17:328–334CrossRefGoogle Scholar
  5. Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59:1014–1022CrossRefGoogle Scholar
  6. 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 14:32–38CrossRefGoogle Scholar
  7. Bookstein FL (1991) Morphometric tools for landmark data. Cambridge University Press, New YorkGoogle Scholar
  8. Brönmark C, Miner JG (1992) Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348–1350PubMedCrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  10. 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:e70121Google Scholar
  11. Capellán E, Nicieza AG (2007) Trade-offs across life stages: does predator-induced hatching plasticity reduce anuran post-metamorphic performance? Evol Ecol 21:445–458CrossRefGoogle Scholar
  12. Ceballos G, Oliva G (2005) Los mamíferos silvestres de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Fondo de Cultura Económica, MéxicoGoogle Scholar
  13. 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 251:309–322PubMedCrossRefGoogle Scholar
  14. 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 33:630–640CrossRefGoogle Scholar
  15. Choi I, Shim JH, Lee YS, Ricklefs RE (2000) Scaling of jumping performance in anuran amphibians. J Herpetol 34:222–227CrossRefGoogle Scholar
  16. Choi I, Shim JH, Ricklefs RE (2003) Morphometric relationships of take-off speed in anuran amphibians. J Exp Zool 299A:99–102CrossRefGoogle Scholar
  17. Cohen MP, Alford RA (1993) Growth, survival and activity patterns of recently metamorphosed Bufo marinus. Wildl Res 20:1–13CrossRefGoogle Scholar
  18. 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 81:1233–1243PubMedCrossRefGoogle Scholar
  19. Dayton GH, Saenz D, Baum KA, Langerhans RB, DeWitt TJ (2005) Body shape, burst speed, and escape behavior of larval anurans. Oikos 111:582–591CrossRefGoogle Scholar
  20. del Hoyo J, Elliot A, Sargarat J (1992) Handbook of the birds of the world. Vol. 1. Ostrich to ducks, vol 1. Lynx Edicions, BarcelonaGoogle Scholar
  21. del Hoyo J, Elliot A, Sargarat J (1996) Handbook of the birds of the world. Vol. 3. Hoatzin to auks. Lynx Edicions, BarcelonaGoogle Scholar
  22. del Hoyo J, Elliot A, Sargarat J (2001) Handbook of the birds of the world. Vol. 6. Mousebirds to Hornbills. Lynx Edicions, BarcelonaGoogle Scholar
  23. DeWitt TJ, Langerhans RB (2003) Multiple prey traits, multiple predators: keys to understanding complex community dynamics. J Sea Res 49:143–155CrossRefGoogle Scholar
  24. 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 1–9Google Scholar
  25. Duellman WE, Trueb L (1996) Musculoskeletal system. In: Duellman WE, Trueb L (eds) Biology of amphibians. Johns Hopkins University Press, Baltimore, pp 289–365Google Scholar
  26. Eklöv P, Svanbäck R (2006) Predation risk influences adaptive morphological variation in fish populations. Am Nat 167:440–452PubMedCrossRefGoogle Scholar
  27. Emerson SB (1978) Allometry and jumping in frogs: helping the twain to meet. Evolution 32:551–564CrossRefGoogle Scholar
  28. 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–S76Google Scholar
  29. Ficetola GF, De Bernardi F (2006) Trade-off between larval development rate and post-metamorphic traits in the frog Rana latastei. Evol Ecol 20:143–158CrossRefGoogle Scholar
  30. 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 27:816–829CrossRefGoogle Scholar
  31. Freeland WJ, Kerin SH (1991) Ontogenetic alteration of activity and habitat selection by Bufo marinus. Wildl Res 18:431–443CrossRefGoogle Scholar
  32. 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, MéxicoGoogle Scholar
  33. Goater CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75:2264–2274Google Scholar
  34. Gosner KL (1960) A simplified table for staging anuran embryos and larvae. Herpetologica 16:183–190Google Scholar
  35. Gray MJ, Smith LM (2005) Influence of land use on postmetamorphic body size of Playa Lake amphibians. J Wildl Manage 69:515–524CrossRefGoogle Scholar
  36. 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 3:1305–1316PubMedCentralPubMedCrossRefGoogle Scholar
  37. Hawley TJ (2009) The ecological significance and incidence of intraguild predation and cannibalism among anurans in ephemeral tropical pools. Copeia 4:748–757CrossRefGoogle Scholar
  38. Höglund J, Säterberg L (1989) Sexual selection in common toads: correlates with age and body size. J Evol Biol 2:367–372CrossRefGoogle Scholar
  39. 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 17:100–108CrossRefGoogle Scholar
  40. 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:e11680PubMedCentralPubMedCrossRefGoogle Scholar
  41. Johnson JB, Belk MC (2001) Predation environment predicts divergent life-history phenotypes among populations of the livebearing fish Brachyrhaphis rhabdophora. Oecologia 126:142–149CrossRefGoogle Scholar
  42. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108PubMedCrossRefGoogle Scholar
  43. Johnson JB, Zúñiga-Vega JJ (2009) Differential mortality drives life-history evolution and population dynamics in the fish Brachyrhaphis rhabdophora. Ecology 90:2243–2252PubMedCrossRefGoogle Scholar
  44. Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope’s rule of phyletic size increase. Evolution 58:1608–1612PubMedGoogle Scholar
  45. 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 177–220Google Scholar
  46. Langerhans RB (2009) Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis. J Evol Biol 22:1057–1075PubMedCrossRefGoogle Scholar
  47. Langerhans RB (2010) Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish. Integr Comp Biol 50:1167–1184PubMedCrossRefGoogle Scholar
  48. Langerhans RB, DeWitt TJ (2004) Shared and unique features of evolutionary diversification. Am Midl Nat 164:335–349Google Scholar
  49. Langerhans RB, Gifford ME (2009) Divergent selection, not life-history plasticity via food limitation, drives morphological divergence between predator regimes in Gambusia hubbsi. Evolution 63:561–567PubMedCrossRefGoogle Scholar
  50. Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318PubMedGoogle Scholar
  51. 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 62:67–118CrossRefGoogle Scholar
  52. Lever C (2001) The cane toad. The history and ecology of a successful colonist. Westbury Academic Publishing, Otley, West YorkshireGoogle Scholar
  53. Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956CrossRefGoogle Scholar
  54. 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, MéxicoGoogle Scholar
  55. Martof BS (1953) Territoriality in the green frog Rana clamitans. Ecology 34:165–174CrossRefGoogle Scholar
  56. McCollum SA, Van Buskirk J (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583–593CrossRefGoogle Scholar
  57. 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 3:68–81CrossRefGoogle Scholar
  58. Miller RR, Minckley WL, Norris SM (2005) Freshwater fishes of México. The University of Chicago Press, USAGoogle Scholar
  59. Mobley KB, Lussetti D, Johansson F, Englund G, Bokma F (2011) Morphological and genetic divergence in Swedish postglacial stickleback (Pungitius pungitius) populations. Evol Biol 11:287Google Scholar
  60. Nakazawa T, Ohba S, Ushio M (2013) Predator–prey body size relationships when predators can consume prey larger than themselves. Biol Lett 9:20121193PubMedCrossRefGoogle Scholar
  61. Newman RA, Dunham AE (1994) Size at metamorphosis and water loss in a desert anuran (Scaphiopus couchii). Copeia 2:372–381CrossRefGoogle Scholar
  62. Ortiz-Santaliestra ME, Fernández-Benéiteza MJ, Marcob A (2012) Density effects on ammonium nitrate toxicity on amphibians. Survival, growth and cannibalism. Aquat Toxicol 110–111:170–176PubMedCrossRefGoogle Scholar
  63. Pizzatto L, Shine R (2008) The behavioral ecology of cannibalism in cane toads (Bufo marinus). Behav Ecol Sociobiol 63:123–133CrossRefGoogle Scholar
  64. Putman RJ, Wratten SD (1984) Principles of ecology. University of California Press, BerkeleyGoogle Scholar
  65. Relyea RA (2001) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82:1947–1955CrossRefGoogle Scholar
  66. Relyea RA, Hoverman JT (2003) The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134:596–604PubMedGoogle Scholar
  67. 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 66:2903–2915PubMedCrossRefGoogle Scholar
  68. 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 203–232Google Scholar
  69. Rohlf FJ (2006) TpsDig. Department of Ecology and Evolution, State University of New York, Stony Brook, New YorkGoogle Scholar
  70. Rohlf FJ (2007) TpsRelw. Department of Ecology and Evolution, State University of New York, Stony Brook, New YorkGoogle Scholar
  71. Rouse DJ, Bishop CA, Struger J (1999) Nitrogen pollution: an assessment of its threat to amphibian survival. Environ Health Perspect 107:799–803PubMedCentralPubMedCrossRefGoogle Scholar
  72. Scoville AG, Pfrender ME (2010) Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc Nat Acad Sci 9:4260–4263CrossRefGoogle Scholar
  73. 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. Nov 2010
  74. Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, OxfordGoogle Scholar
  75. Steiner UK (2007) Investment in defense and cost of predator-induced defense along a resource gradient. Oecologia 152:201–210PubMedCrossRefGoogle Scholar
  76. 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 74:708–715CrossRefGoogle Scholar
  77. Tejedo M, Semlitsch RD, Hotz H (2000) Covariation of morphology and jumping performance in newly metamorphosed water frogs: effects of larval growth history. Copeia 2:448–458CrossRefGoogle Scholar
  78. 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 43:31–39CrossRefGoogle Scholar
  79. 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 18:180–190PubMedCrossRefGoogle Scholar
  80. Tingley R, Greenlees MJ, Shine R (2012) Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121:1959–1965CrossRefGoogle Scholar
  81. Toledo LF (2003) Predation on seven South American anuran species by water bugs (Belostomatidae). Phyllomedusa 2:105–108CrossRefGoogle Scholar
  82. Toledo LF (2005) Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetol Rev 36:395–400Google Scholar
  83. Toledo LF, Haddad CFB (2009) Colors and some morphological traits as defensive mechanisms in anurans. Int J Zool 2009:1–12CrossRefGoogle Scholar
  84. Toledo LF, Ribeiro RS, Haddad CFB (2007) Anurans as prey: an exploratory analysis and size relationships between predators and their prey. J Zool 27:170–177CrossRefGoogle Scholar
  85. 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 2013Google Scholar
  86. 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 38:476–483CrossRefGoogle Scholar
  87. Uller T, Olsson M (2010) Offspring size and timing of hatching determine survival and reproductive output in a lizard. Oecologia 162:663–671PubMedCrossRefGoogle Scholar
  88. Vamosi SM (2003) The presence of other fish species affects speciation in three spine sticklebacks. Evol Ecol Res 5:717–730Google Scholar
  89. Vincent SE, Moon BR, Shine R, Herrel A (2006) The functional meaning of ‘‘prey size’’ in water snakes (Nerodia fasciata, Colubridae). Oecologia 147:204–211PubMedCrossRefGoogle Scholar
  90. 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 45:256–262PubMedCrossRefGoogle Scholar
  91. 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 12:1–13Google Scholar
  92. 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 99:738–751CrossRefGoogle Scholar
  93. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S138CrossRefGoogle Scholar
  94. Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a primer. Elsevier Academic Press, LondonGoogle Scholar
  95. Zug GR (1972) Anuran locomotion: structure and function. 1. Preliminary observations on the relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia 1972:613–624CrossRefGoogle Scholar
  96. Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resume of native populations. Smithson Contrib Zool 284:1–58Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Regina Vega-Trejo
    • 1
  • J. Jaime Zúñiga-Vega
    • 1
  • R. Brian Langerhans
    • 2
  1. 1.Departamento de Ecología y Recursos Naturales, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMexico D.F.Mexico
  2. 2.Department of Biological Sciences, W.M. Keck Center for Behavioral BiologyNorth Carolina State UniversityRaleighUSA

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