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Beyond Sexual Dimorphism and Habitat Boundaries: Coloration Correlates with Morphology, Age, and Locomotor Performance in a Toad

  • Francisco Javier Zamora-Camacho
  • Mar Comas
Research Article

Abstract

Coloration is often key in animal communication, and is frequently subjected to strong natural and sexual selection, often with opposed directions: natural selection typically favors cryptic colorations whereas sexual selection may favor conspicuous colorations. Also, different coloration traits may convey different pieces of information. Plus, coloration may vary among habitats, mirroring local selective pressures. In this work, we test if color parameters (luminosity, chroma, and hue) of back and throat are related to different life-history and morphological traits in Epidalea calamita toads. Furthermore, we check possible variability of color parameters between agrosystem and natural habitat toads. Toad coloration was sexually dimorphic, which suggests a role of coloration in sexual communication. Moreover, coloration correlated with age, body size, hindlimb length, and sprint speed. These findings suggest communication based on coloration beyond sex recognition: coloration could act as a signal of overall quality of bearers, with a potential role in mate choice. Moreover, coloration differed between habitats. Greener backs in agrosystem toads could indicate greater intensity of predator pressure, while their higher saturation could indicate greater investment in mate attraction. This result is aligned with previous findings that agrosystem toads respond to reduced lifespan with greater reproductive investment.

Keywords

Amphibian Anuran Color traits Epidalea calamita Habitat differences Skeletochronology 

Notes

Acknowledgements

Toads were captured in accordance with permissions from Junta de Andalucía issued to the authors (reference AWG/MGD/MGM/CB). The authors assumed the expenses of the work. FJZ-C was partly supported by a Fundación Ramón Areces postdoctoral grant and a Juan de la Cierva-Formación contract by the Spanish Government, and MC was supported by a Severo Ochoa contract (ref: SVP-2014-068620). Comments by two anonymous reviewers improved the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Andersson, S., & Prager, M. (2006). Quantifying colors. In K. J. McGraw & G. E. Hill (Eds.), Bird coloration volume I: Mechanisms and measurements (pp. 41–89). Cambridge: Harvard University Press.Google Scholar
  2. Arai, E., Hasegawa, M., Makino, T., Hagino, A., Sakai, Y., Ohtsuki, H., et al. (2017). Physiological conditions and genetic controls of phaeomelanin pigmentation in nestling barn swallows. Behavioral Ecology, 28, 706–716.CrossRefGoogle Scholar
  3. Avilés, J. M., & Parejo, D. (2013). Colour also matters for nocturnal birds: Owlet bill coloration advertises quality and influences parental feeding behaviour in little owls. Oecologia, 173, 399–408.CrossRefPubMedGoogle Scholar
  4. Banks, B., Beebee, T. J. C., & Denton, J. S. (1993). Long-term management of a natterjack toad (Bufo calamita) population in southern Britain. Amphibia-Reptilia, 14, 155–168.CrossRefGoogle Scholar
  5. Bell, R. C., & Zamudio, K. R. (2012). Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity. Proceedings of the Royal Society B, 279, 4687–4693.CrossRefPubMedGoogle Scholar
  6. Boomsma, J. J., & Arntzen, J. W. (1985). Abundance, growth and feeding of natterjack toads (Bufo calamita) in a 4-year-old artificial habitat. Journal of Applied Ecology, 22, 395–405.CrossRefGoogle Scholar
  7. Bowcock, H., Brown, G. P., & Shine, R. (2009). Beastly bondage: The costs of amplexus in cane toads (Bufo marinus). Copeia, 2009, 29–36.Google Scholar
  8. Burtt, E. H. (1981). The adaptiveness of animal colors. BioScience, 31, 723–729.CrossRefGoogle Scholar
  9. Candolin, U. (2003). The use of multiple cues in mate choice. Biological Reviews, 78, 167–176.CrossRefGoogle Scholar
  10. Caro, T. (2005). The adaptive significance of coloration in mammals. BioScience, 55, 125–136.CrossRefGoogle Scholar
  11. Cloudsley-Thompson, J. L. (1999). Multiple factors in the evolution of animal coloration. Naturwissenschaften, 86, 123–132.CrossRefPubMedGoogle Scholar
  12. Clusella-Trullas, S., van Wyk, J. H., & Spotila, J. R. (2007). Thermal melanism in ectotherms. Journal of Thermal Biology, 32, 235–245.CrossRefGoogle Scholar
  13. Comas, M., Reguera, S., Zamora-Camacho, F. J., Salvadó, H., & Moreno-Rueda, G. (2016). Comparison of the effectiveness of phalanges vs. humeri and femurs to estimate lizard age with skeletochronology. Animal Biodiversity and Conservation, 39, 237–240.Google Scholar
  14. de Luna, A. G., Hödl, W., & Amézquita, A. (2010). Colour, size and movement as visual subcomponents in multimodal communication by the frog Allobates femoralis. Animal Behaviour, 79, 739–745.CrossRefGoogle Scholar
  15. Dey, C. J., Valcu, M., Kempenaers, B., & Dale, J. (2015). Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). Journal of Evolutionary Biology, 28, 250–258.CrossRefPubMedGoogle Scholar
  16. Endler, J. A. (1990). On the measurement and classification of colour in studies of animal colour patterns. Biological Journal of the Linnean Society, 41, 315–352.CrossRefGoogle Scholar
  17. Galeano, S. P., & Harms, K. E. (2016). Coloration in the polymorphic frog Oophaga pumilio associates with level of aggressiveness in intraspecific and interspecific behavioral interactions. Behavioral Ecology and Sociobiology, 70, 83–97.CrossRefGoogle Scholar
  18. Gilford, T. (1988). The evolution of conspicuous coloration. The American Naturalist, 131, S7–S21.CrossRefGoogle Scholar
  19. Giraudeau, M., Friesen, C. R., Sudykam, J., Rollings, N., Whittington, C. M., Wilson, M. R., et al. (2016). Ageing and the cost of maintaining coloration in the Australian painted dragon. Biology Letters, 12, 20160077.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gomez, D., Richardson, C., Lengagne, T., Derex, M., Plénet, S., Joly, P., et al. (2010). Support for a role of colour vision in mate choice in the nocturnal European treefrog (Hyla arborea). Behaviour, 147, 1753–1768.CrossRefGoogle Scholar
  21. Gomez, D., Richardson, C., Lengagne, T., Plénet, S., Joly, P., Léna, J. P., et al. (2009). The role of nocturnal vision in mate choice: Females prefer conspicuous males in the European tree frog (Hyla arborea). Proceedings of the Royal Society B, 276, 2351–2358.CrossRefPubMedGoogle Scholar
  22. Gomez, D., Richardson, C., Théry, M., Lengagne, T., Léna, J. P., Plénet, S., et al. (2011). Multimodal signals in male European treefrog (Hyla arborea) and the influence of population isolation on signal expression. Biological Journal of the Linnean Society, 103, 633–647.CrossRefGoogle Scholar
  23. Gómez-Mestre, I. (2014). Sapo corredor—Epidalea calamita (Laurenti, 1768). In A. Salvador & A. Marco (Eds.), Enciclopedia Virtual de los Vertebrados Españoles. Madrid: Museo Nacional de Ciencias Naturales. http://www.vertebradosibericos.org. See.
  24. Grafen, A. (1990). Biological signals as handicaps. Journal of Theoretical Biology, 144, 517–546.CrossRefPubMedGoogle Scholar
  25. Grether, G. F., Hudon, J., & Millie, D. F. (1999). Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proceedings of the Royal Society of London B, 266, 1317–1322.CrossRefGoogle Scholar
  26. Grether, G. F., Kolluru, G. R., & Nersissian, K. (2004). Individual colour patches as multicomponent signals. Biological Reviews of the Cambridge Philosophical Society, 79, 583–610.CrossRefPubMedGoogle Scholar
  27. Hettyey, A., Herczeg, G., Laurila, A., Crochet, P. A., & Merilä, J. (2009). Body temperature, size, nuptial colouration and mating success in male moor frogs (Rana arvalis). Amphibia-Reptilia, 30, 37–43.CrossRefGoogle Scholar
  28. Hill, G. E. (1996). Redness as a measure of the production cost of ornamental coloration. Ethology Ecology and Evolution, 8, 157–175.CrossRefGoogle Scholar
  29. Hill, G. E., & McGraw, K. J. (2006a). Bird coloration. Vol. 1. Mechanisms and measurement. Cambridge: Harvard University Press.Google Scholar
  30. Hill, G. E., & McGraw, K. J. (2006b). Bird coloration. Vol. 2. Function and evolution. Cambridge: Harvard University Press.Google Scholar
  31. Husak, J. F., Fox, S. F., Lovern, M. B., & van den Bussche, R. A. (2006b). Faster lizards sire more offspring: Sexual selection on whole-animal performance. Evolution, 60, 2122–2130.CrossRefPubMedGoogle Scholar
  32. Husak, J. F., Macedonia, J. M., Fox, S. F., & Sauceda, R. C. (2006a). Predation cost of conspicuous male coloration in collared lizards (Crotaphyllus collaris): An experimental test using clay-covered model lizards. Ethology, 112, 572–580.CrossRefGoogle Scholar
  33. Isaksson, C., Örnborg, J., Stephensen, E., & Andersson, S. (2005). Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits. EcoHealth, 2, 138–146.CrossRefGoogle Scholar
  34. Jacobs, L. E., Vega, A., Dudgeon, S., Kaiser, K., & Robertson, J. M. (2017). Local not vocal: Assortative female choice in divergent populations of red-eyed treefrogs, Agalychnis callidryas (Hylidae: Phylomedusinae). Biological Journal of the Linnean Society, 120, 171–178.Google Scholar
  35. Jongman, R. H. G., Braak, C. J. F., & Tongeren, O. F. R. (1995). Data analysis in community and landscape ecology. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  36. Kindermann, C., & Hero, J. M. (2016). Rapid dynamic colour change is an intrasexual signal in a lek breeding frog (Litoria wilcoxii). Behavioral Ecology and Sociobiology, 70, 1995–2003.CrossRefGoogle Scholar
  37. Krohn, A. R., & Rosenblum, E. B. (2016). Geographic color variation and physiological color change in eastern collared lizards (Crotaphyllus collaris) from southern New Mexico, USA. Herpetologica, 72, 318–323.CrossRefGoogle Scholar
  38. Maan, M. E., & Cummings, M. E. (2009). Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. PNAS, 106, 19072–19077.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Martín, J., & López, P. (2001). Risk of predation may explain the absence of nuptial coloration in the wall lizard, Podarcis muralis. Evolutionary Ecology Research, 3, 889–898.Google Scholar
  40. Martínez, F., & Montero, G. (2004). The Pinus pinea L. woodlands along the coast of South-western Spain: Data for a new geobotanical interpretation. Plant Ecology, 175, 1–18.CrossRefGoogle Scholar
  41. McGraw, K. J. (2005). The antioxidant function of many animal pigments: Are there consistent health benefits of sexually selected colourants? Animal Behaviour, 69, 757–764.CrossRefGoogle Scholar
  42. McGraw, K. J., Hill, G. E., Stradi, R., & Parker, R. S. (2001). The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and northern cardinals (Carduelis cardinalis). Physiological and Biochemical Zoology, 74, 843–852.CrossRefPubMedGoogle Scholar
  43. McLister, J. D. (2003). The metabolic cost of amplexus in the grey tree frog (Hyla versicolor): Assessing the energetics of male mating success. Canadian Journal of Zoology, 81, 388–394.CrossRefGoogle Scholar
  44. Merilaita, S., Lyytinen, A., & Mappes, J. (2001). Selection for cryptic coloration in a visually heterogeneous habitat. Proceedings of the Royal Society of London, 268, 1925–1929.CrossRefGoogle Scholar
  45. Miaud, C., Sanuy, D., & Avrillier, J. N. (2000). Terrestrial movements of the natterjack toad Bufo calamita (Amphibia, Anura) in a semi-arid, agricultural landscape. Amphibia-Reptilia, 21, 357–369.CrossRefGoogle Scholar
  46. Molnár, O., Bajer, K., Mészáros, B., Török, J., & Herczeg, G. (2013). Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton-Zuk hypothesis. Naturwissenschaften, 100, 551–558.CrossRefPubMedGoogle Scholar
  47. Montgomerie, R. (2006). Analyzing colors. In: G. E. Hill, K. J. McGraw (Eds), Bird coloration Volume I: mechanisims and measurements (pp 90–140). Cambridge, MA: Harvard University Press.Google Scholar
  48. Moore, M. P., & Martin, R. A. (2016). Intrasexual selection favours an immune-correlated colour ornament in a dragonfly. Journal of Evolutionary Biology, 29, 2256–2265.CrossRefPubMedGoogle Scholar
  49. Olsson, M. (1994). Nuptial coloration in the sand lizard, Lacerta agilis: And intra-sexually selected cue to fighting ability. Animal Behaviour, 48, 607–613.CrossRefGoogle Scholar
  50. Pärt, T., & Qvarnström, A. (1997). Badge size in collared flycatchers predicts outcome of male competition over territories. Animal Behaviour, 54, 893–899.CrossRefGoogle Scholar
  51. Pauers, M. J., McKinnon, J. S., & Ehlinger, T. J. (2004). Directional sexual selection on chroma and within-pattern colour contrast in Labeotropheus fuelleborni. Proceedings of the Royal Society of London B, 271, S444–S447.CrossRefGoogle Scholar
  52. Penteriani, V., Delgado, M. M., Alonso-Álvarez, C., Pina, V., Sergio, N., Bartolommei, F., P., et al (2007). The importance of visual cues for nocturnal species: Eagle owls fledglings signal with white mouth feathers. Ethology, 113, 934–943.CrossRefGoogle Scholar
  53. Pérez i de Lanuza, G., Carazo, P., & Font, E. (2014). Colours of quality: Structural (but not pigment) coloration informs about male quality in a polychromatic lizard. Animal Behaviour, 90, 73–81.CrossRefGoogle Scholar
  54. Polo-Cavia, N., Oliveira, J. M., Villa, R., Márquez, A. J., R (2016). Background colour matching in a wild population of Alytes obstetricans. Amphibia-Reptilia, 37, 253–260.CrossRefGoogle Scholar
  55. Preest, M. R., & Pough, F. H. (2003). Effects of body temperature and hydration state on organismal performance of toads, Bufo americanus. Physiological and Biochemical Zoology, 76, 229–239.CrossRefPubMedGoogle Scholar
  56. Promislow, D. E. L., Montgomerie, R., & Martin, T. E. (1992). Mortality costs of sexual dimorphism in birds. Proceedings of the Royal Society B, 250, 143–150.CrossRefGoogle Scholar
  57. Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for biologists. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  58. Reguera, S., Zamora-Camacho, F. J., & Moreno-Rueda, G. (2014). The lizard Psammodromus algirus (Squamata: Lacertidae) is darker at high altitudes. Biological Journal of the Linnean Society, 112, 132–141.CrossRefGoogle Scholar
  59. Richardson, C., Gomez, D., Durieux, R., Théry, M., Joly, P., Léna, J. P., et al. (2010). Hearing is not necessarily believing in nocturnal anurans. Biology Letters, 6, 633–635.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Robson, M. A., & Miles, D. B. (2000). Locomotor performance and dominance in male tree lizards, Urosaurus ornatus. Functional Ecology, 14, 338–344.CrossRefGoogle Scholar
  61. Rojas, B. (2017). Behavioural, ecological, and evolutionary aspects of diversity in frog colour patterns. Biological Reviews, 92, 1059–1080.CrossRefPubMedGoogle Scholar
  62. Schulte-Hostedde, A. I., & Schank, C. M. M. (2009). Secondary sexual traits and individual phenotype in male green frogs (Rana clamitans). Journal of Herpetology, 43, 89–95.CrossRefGoogle Scholar
  63. Sheldon, B. C., Arponen, H., Laurila, A., Crochet, P. A., & Merilä, J. (2003). Sire coloration influences offspring survival under predation risk in the moorfrog. Journal of Evolutionary Biology, 16, 1288–1295.CrossRefPubMedGoogle Scholar
  64. Shults, A. J., & Burns, K. J. (2017). The role of sexual and natural selection in shaping patterns of sexual dicromatism in the largest family of songbirds (Aves: Thraupidae). Evolution, 71, 1061–1074.CrossRefGoogle Scholar
  65. Siefferman, L., Hill, G. E., & Dobson, F. S. (2005). Ornamental plumage coloration and condition are dependent on age in eastern bluebirds Sialia sialis. Journal of Avian Ecology, 36, 428–435.Google Scholar
  66. Simons, M. J. P., Cohen, A. A., & Verhulst, S. (2012). What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds—A meta-analysis. PLoS ONE, 7, e43088.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sinsch, U. (1988). Temporal spacing of breeding activity in the natterjack toad, Bufo calamita. Oecologia, 76, 399–407.CrossRefPubMedGoogle Scholar
  68. Starnberger, I., Preininger, D., & Hoedl, W. (2014). The anuran vocal sac: A tool for multimodal signalling. Animal Behaviour, 97, 281–288.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Stearns, S. C. (2000). Life history evolution: Successes, limitations, and prospects. Naturwissenschaften, 87, 476–486.CrossRefPubMedGoogle Scholar
  70. Stevens, M., & Ruxton, G. D. (2012). Linking the evolution and form of warning coloration in nature. Proceedings of the Royal Society B, 279, 417–426.CrossRefPubMedGoogle Scholar
  71. Stuart, Y. E., Dappen, N., & Losin, N. (2012). Inferring predator behavior from attack rates on prey-replicas that differ in conspicuousness. PLoS ONE, 7, e48497.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Stuart-Fox, D. M., Moussalli, A., Johnston, G. R., & Owens, I. P. F. (2004). Evolution of color variation in dragon lizards: Quantitative tests of the role of crypsis and local adaptation. Evolution, 58, 1549–1559.CrossRefPubMedGoogle Scholar
  73. Stuart-Fox, D. M., & Ord, T. J. (2004). Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proceedings of the Royal Society of London B, 271, 2249–2255.CrossRefGoogle Scholar
  74. Sztatecsny, M., Preininger, D., Freudmann, A., Loretto, M. C., Maier, F., & Hödl, W. (2012). Don’t get the blues: Conspicuous nuptial colouration of male moor frogs (Rana arvalis) supports visual male recognition during scramble competition in large breeding aggregations. Behavioral Ecology and Sociobiology, 66, 1587–1593.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Sztatecsny, M., Strondl, C., Baierl, A., Ries, C., & Hödl, W. (2010). Chin up: Are the bright throats of male common frogs a condition-independent visual cue? Animal Behaviour, 79, 779–786.CrossRefGoogle Scholar
  76. Talloen, W., Van Dyck, H., & Lens, L. (2004). The cost of melanization: Butterfly wing coloration under environmental stress. Evolution, 58, 360–366.PubMedPubMedCentralGoogle Scholar
  77. Tejedo, M. (1992a). Effects of body size and timing of reproduction on reproductive success on female natterjack toad (Bufo calamita). Journal of Zoology, 228, 545–555.CrossRefGoogle Scholar
  78. Tejedo, M. (1992b). Large male mating advantage in natterjack toads, Bufo calamita: Sexual selection or energetic constraints? Animal Behavior, 44, 557–569.CrossRefGoogle Scholar
  79. Tejedo, M., & Reques, R. (1994). Plasticity in metamorphic traits of natterjack tadpoles: The interactive effects of density and pond duration. Oikos, 71, 295–304.CrossRefGoogle Scholar
  80. Umbers, K. D. L., Silla, A. J., Bailey, J. A., Shaw, A. K., & Byrne, P. G. (2016). Dietary carotenoids change the colour of Southern corroboree frogs. Biological Journal of the Linnean Society, 119, 436–444.CrossRefGoogle Scholar
  81. Vanhooydonck, B., Measey, J., Edwards, S., Makhubo, B., Tolley, K. A., & Herrel, A. (2015). The effects of substratum on locomotor performance in lacertid lizards. Biological Journal of the Linnean Society, 115, 869–881.CrossRefGoogle Scholar
  82. Vásquez, T., & Pfennig, K. S. (2007). Looking on the bright side: Females prefer coloration indicative of male size and condition in the sexually dichromatic spadefoot toad, Scaphiopus couchii. Behavioral Ecology and Sociobiology, 62, 127–135.CrossRefGoogle Scholar
  83. Yeomans, K. A., & Golder, P. A. (1982). The Guttman-Kaiser criterion as a predictor of the number of common factors. The Statistician, 31, 221–229.CrossRefGoogle Scholar
  84. Zahavi, A., & Zahavi, A. (1997). The handicap principle, a missing piece of Darwin’s puzzle. New York: Oxford University Press.Google Scholar
  85. Zambre, A. M., & Thaker, M. (2017). Flamboyant sexual signals: Multiple messages for multiple receivers. Animal Behaviour, 127, 197–203.CrossRefGoogle Scholar
  86. Zamora-Camacho, F. J. (2018a). Locomotor performance in a running toad: Roles of morphology, sex and agrosystem versus natural habitat. Biological Journal of the Linnean Society, 123, 411–421.CrossRefGoogle Scholar
  87. Zamora-Camacho, F. J. (2018b). Integrating time progression in ecoimmunology studies: Beyond immune response intensity. Current Zoology.  https://doi.org/10.1093/cz/zoy045.CrossRefPubMedPubMedCentralGoogle Scholar
  88. Zamora-Camacho, F. J., & Comas, M. (2017). Greater reproductive investment, but shorter lifespan, in agrosystem than in natural-habitat toads. PeerJ, 5, e3791.CrossRefPubMedPubMedCentralGoogle Scholar
  89. Zamora-Camacho, F. J., Reguera, S., Rubiño-Hispán, M. V., & Moreno-Rueda, G. (2014). Effects of limb length, body mass, gender, gravidity, and elevation on escape speed in the lizard Psammodromus algirus. Evolutionary Biology, 41, 509–517.CrossRefGoogle Scholar
  90. Zuk, M., & Kolluru, G. R. (1998). Exploitation of sexual signals by predators and parasitoids. The Quarterly Review of Biology, 73, 415–438.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA
  2. 2.Department of Biogeography and Global ChangeMuseo Nacional de Ciencias Naturales (MNCN), Spanish National Research Council (CSIC)MadridSpain
  3. 3.Estación Biológica de Doñana (EBD-CSIC)SevilleSpain

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