Exploring the function of red colouration in female spiny-footed lizards (Acanthodactylus erythrurus): patterns of seasonal colour change

In: Amphibia-Reptilia
View More View Less
  • 1 Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), Calle José Gutiérrez Abascal 2, E-28006 Madrid, Spain
  • 2 Departamento de Ecología, Edificio de Ciencias, Universidad de Alcalá, E-28871 Alcalá de Henares, Madrid, Spain

Login via Institution

Purchase instant access (PDF download and unlimited online access):

€25.00$30.00

In spiny-footed lizards (Acanthodactylus erythrurus), adult females (but not males) show conspicuous red colouration in the tail and hind legs. To investigate the function of this red colouring and proximal causes of seasonal colour change, we captured adult females before the reproductive season and kept them in captivity in one of the three following situations: with a male and fertilization possible, with a male and fertilization impossible, or with another female (fertilization also impossible). Colour was quantified using spectrophotometry. Red colouration increased shortly before the onset of reproduction, but faded during the breeding season and became whitish (light buff-gray) in all cases. Both fertilized and unfertilized females laid eggs or were gravid after two months of the experiment, but while fertilized females laid mostly fertile eggs, unfertilized females only laid infertile eggs. Both egg formation and colour change might be triggered by abiotic factors, although female characteristics also play a role, since heavier females changed colour and laid eggs earlier. Females interacting freely with a male were darker at the end of the breeding season than females separated from the male, indicating that fertilization or physical contact might also have an effect on colouration. Colour change patterns found in this study suggest that female red colouration might have a mating-related function, but do not support a courtship rejection function for the red colour. However, whitish colouration resulting from red fading might signal gravidity in this species. Future experimental manipulation of female colouration will be needed to test these hypotheses.

  • Amundsen T., Forsgren E. (2001): Male mate choice selects for female coloration in a fish. Proc. Natl. Acad. Sci. USA 98: 13155-13160.

  • Amundsen T., Forsgren E., Hansen L.T.T. (1997): On the function of female ornaments: male bluethroats prefer colourful females. Proc. R. Soc. B 264: 1579-1586.

    • Search Google Scholar
    • Export Citation
  • Andersson M. (1994): Sexual Selection. Princeton University Press, Princeton.

  • Baird T.A. (2004): Reproductive coloration in female collared lizards, Crotophytus collaris, stimulates courtship by males. Herpetologica 60: 337-348.

    • Search Google Scholar
    • Export Citation
  • Bauwens D., Verheyen R.F. (1987): Variation of reproductive traits in a population of the lizard Lacerta vivipara. Holarctic Ecol. 10: 120-127.

    • Search Google Scholar
    • Export Citation
  • Belliure J. (2009): Lagartija colirroja-Acanthodactylus erythrurus. In: Enciclopedia virtual de los vertebrados españoles. Salvador A., Marco A., Eds, Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org.

    • Search Google Scholar
    • Export Citation
  • Blasco M. (1975): Dimorfismo sexual en una población de Acanthodactylus erythrurus Schinz, procedente del litoral arenoso de Málaga. Cuadernos de Ciencias Biológicas 4: 5-10.

    • Search Google Scholar
    • Export Citation
  • Bleu J., Le Galliard J.F., Meylan S., Massot M., Fitze P.S. (2011): Mating does not influence reproductive investment, in a viviparous lizard. J. Exp. Zool. 315: 458-464.

    • Search Google Scholar
    • Export Citation
  • Burns K.J. (1998): A phylogenetic perspective on the evolution of sexual dichromatism in tanagers (Thraupidae): the role of female versus male plumage. Evolution 52: 1219-1224.

    • Search Google Scholar
    • Export Citation
  • Busack S.D., Jaksić F.M. (1982): Autoecological observations of Acanthodactylus erythrurus (Sauria: Lacertidae) in southern Spain. Amphibia-Reptilia 3: 237-255.

    • Search Google Scholar
    • Export Citation
  • Busack S.D., Klosterman L.L. (1987): Reproduction in a Spanish population of Acanthodactylus erythrurus (Reptilia: Lacertilia: Lacertidae). Ann. Carnegie Mus. 56: 97-102.

    • Search Google Scholar
    • Export Citation
  • Butcher G.S., Rohwer S.A. (1989): The evolution of conspicuous and distinctive coloration for communication in birds. Curr. Ornithol. 6: 51-108.

    • Search Google Scholar
    • Export Citation
  • Castilla A.M., Barbadillo L.J., Bauwens D. (1992): Annual variation in reproductive traits in the lizard Acanthodactylus erythrurus. Can. J. Zool. 70: 395-402.

    • Search Google Scholar
    • Export Citation
  • Chan R., Stuart-Fox D., Jessop T.S. (2009): Why are females ornamented? A test of the courtship stimulation and courtship rejection hypotheses. Behav. Ecol. 20: 1334-1342.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr. (1984): Female secondary sexual coloration and sex recognition in the keeled earless lizard, Holbrookia propinqua. Anim. Behav. 32: 1142-1150.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr. (1988): Aggressive behavior and courtship rejection in brightly and plainly colored female keeled earless lizards (Holbrookia propinqua). Ethology 77: 265-278.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr., Adams C.S., Dobie J.L. (1983): Female color change in the keeled earless lizard, Holbrookia propinqua: relationship to the reproductive cycle. Southwest. Nat. 28: 275-280.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr., Burns N.B. (1987): Social significance of ventrolateral colouration in the fence lizard (Sceloporus undulatus). Anim. Behav. 35: 526-532.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr., Crews D. (1988): Sexual coloration, plasma concentrations of sex steroid hormones, and responses to courtship in female keeled earless lizards (Holbrookia propinqua). Horm. Behav. 22: 12-25.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr., Greenberg N. (1992): Reptilian coloration and behavior. In: Biology of the Reptilia. Physiology E: Hormones, Brain and Behavior, Vol. 18, p.  298-422. Gans C., Crews D., Eds, University of Chicago Press, Chicago.

    • Search Google Scholar
    • Export Citation
  • Cooper W.E. Jr., McGuire J.A. (1993): Progesterone induces bright orange throat coloration in female Petrosaurus mearnsi. Amphibia-Reptilia 14: 213-221.

    • Search Google Scholar
    • Export Citation
  • Cuadrado M. (2000): Body colors indicate the reproductive status of female common chameleons: experimental evidence for the intersex communication function. Ethology 106: 79-91.

    • Search Google Scholar
    • Export Citation
  • Cuervo J.J., Shine R. (2007): Hues of a dragon’s belly: morphological correlates of ventral coloration in water dragons. J. Zool. 273: 298-304.

    • Search Google Scholar
    • Export Citation
  • Cuthill I.C., Bennett A.T.D., Partridge J.C., Maier E.J. (1999): Plumage reflectance and the objective assessment of avian sexual dichromatism. Am. Nat. 153: 183-200.

    • Search Google Scholar
    • Export Citation
  • Duvall D., Guillette L.J. Jr., Jones R.E. (1982): Environmental control of reptilian reproductive cycles. In: Biology of the Reptilia. Physiology D: Physiological Ecology, Vol. 13, p.  201-231. Gans C., Pough F.H., Eds, Academic Press, London.

    • Search Google Scholar
    • Export Citation
  • Endler J.A., Mielke P.W. (2005): Comparing entire colour patterns as birds see them. Biol. J. Linn. Soc. 86: 405-431.

  • Fitze P.S., Cote J., San-Jose L.M., Meylan S., Isaksson C., Andersson S., Rossi J.M., Clobert J. (2009): Carotenoid-based colours reflect the stress response in the common lizard. PLOS ONE 4: e5111.

    • Search Google Scholar
    • Export Citation
  • Galán P. (1996): Sexual maturity in a population of the lacertid lizard Podarcis bocagei. Herpetol. J. 6: 87-93.

  • Grill C.P., Rush V.N. (2000): Analysing spectral data: comparison and application of two techniques. Biol. J. Linn. Soc. 69: 121-138.

  • Hager S.B. (2001): The role of nuptial coloration in female Holbrookia maculata: evidence for a dual signaling system. J. Herpetol. 35: 624-632.

    • Search Google Scholar
    • Export Citation
  • Hawlena D. (2009): Colorful tails fade when lizards adopt less risky behaviors. Behav. Ecol. Sociobiol. 64: 205-213.

  • Heinsohn R., Legge S., Endler J.A. (2005): Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309: 617-619.

  • Laloi D., Richard M., Lecomte J., Massot M., Clobert J. (2004): Multiple paternity in clutches of common lizard Lacerta vivipara: data from microsatellite markers. Mol. Ecol. 13: 719-723.

    • Search Google Scholar
    • Export Citation
  • Lessells C.M., Boag P.T. (1987): Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.

  • López P., Martín J. (2005): Age related differences in lipophilic compounds found in femoral gland secretions of male spiny-footed lizards, Acanthodactylus erythrurus. Z. Naturforsch. C 60: 915-920.

    • Search Google Scholar
    • Export Citation
  • Matt K.S., Moore M.C., Knapp R., Moore I.T. (1997): Sympathetic mediation of stress and aggressive competition: plasma catecholamines in free-living male tree lizards. Physiol. Behav. 61: 639-647.

    • Search Google Scholar
    • Export Citation
  • McGraw K.J. (2007): Dietary mineral content influences the expression of melanin-based ornamental coloration. Behav. Ecol. 18: 137-142.

    • Search Google Scholar
    • Export Citation
  • Muma K.E., Weatherhead P.J. (1989): Male traits expressed in females: direct or indirect sexual selection? Behav. Ecol. Sociobiol. 25: 23-31.

    • Search Google Scholar
    • Export Citation
  • Nunn C.L. (1999): The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58: 229-246.

    • Search Google Scholar
    • Export Citation
  • Olsson M., Madsen T. (2001): Promiscuity in sand lizards (Lacerta agilis) and adder snakes (Vipera berus): causes and consequences. J. Hered. 92: 190-197.

    • Search Google Scholar
    • Export Citation
  • Olsson M., Shine R. (1997): Advantages of multiple matings to females: a test of the infertility hypothesis using lizards. Evolution 51: 1684-1688.

    • Search Google Scholar
    • Export Citation
  • Pérez-Mellado V. (1998): Acanthodactylus erythrurus (Schinz, 1834). In: Reptiles. Fauna ibérica, Vol. 10, p.  167-175. Salvador, A., Coord., Museo Nacional de Ciencias Naturales, Madrid.

    • Search Google Scholar
    • Export Citation
  • Ramírez-Sandoval E., Ramírez-Bautista A., Vitt L.J. (2006): Reproduction in the lizard Phyllodactylus lanei (Squamata: Gekkonidae) from the Pacific coast of Mexico. Copeia 2006: 1-9.

    • Search Google Scholar
    • Export Citation
  • Salica M.J., Halloy M. (2009): Nuptial coloration in female Liolaemus quilmes (Iguania: Liolaemidae): relation to reproductive state. Rev. Esp. Herpetol. 23: 141-149.

    • Search Google Scholar
    • Export Citation
  • Salvador A., Díaz J.A., Veiga J.P., Bloor P., Brown R.P. (2008): Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav. Ecol. 19: 169-176.

    • Search Google Scholar
    • Export Citation
  • Seva E. (1982): Taxocenosis de lacértidos en un arenal costero alicantino. Servicio de Publicaciones de la Universidad de Alicante, Alicante.

    • Search Google Scholar
    • Export Citation
  • Shine R. (2003): Locomotor speeds of gravid lizards: placing ‘costs of reproduction’ within an ecological context. Funct. Ecol. 17: 526-533.

    • Search Google Scholar
    • Export Citation
  • StatSoft, Inc. (2011): Statistica (data analysis software system), version 10. www.statsoft.com.

  • Uller T., Olsson M. (2005): Multiple copulations in natural populations of lizards: evidence for the fertility assurance hypothesis. Behaviour 142: 45-56.

    • Search Google Scholar
    • Export Citation
  • Vaughan G.L., Greenberg N. (1987): Propanolol, a beta-adrenergic antagonist, retards response to MSH in skin of Anolis carolinensis. Physiol. Behav. 40: 555-558.

    • Search Google Scholar
    • Export Citation
  • Warner D.A., Shine R. (2007): Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154: 65-73.

    • Search Google Scholar
    • Export Citation
  • Watkins G.G. (1997): Inter-sexual signalling and the functions of female coloration in the tropidurid lizard Microlophus occipitalis. Anim. Behav. 53: 843-852.

    • Search Google Scholar
    • Export Citation
  • Weiss S.L. (2002): Reproductive signals of female lizards: pattern of trait expression and male response. Ethology 108: 793-813.

  • Weiss S.L. (2006): Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav. Ecol. 17: 726-732.

    • Search Google Scholar
    • Export Citation
  • Weiss S.L., Kennedy E.A., Bernhard J.A. (2009): Female-specific ornamentation predicts offspring quality in the striped plateau lizard, Sceloporus virgatus. Behav. Ecol. 20: 1063-1071.

    • Search Google Scholar
    • Export Citation
  • Weiss S.L., Kennedy E.A., Safran R.J., McGraw K.J. (2011): Pterin-based ornamental coloration predicts yolk antioxidant levels in female striped plateau lizards (Sceloporus virgatus). J. Anim. Ecol. 80: 519-527.

    • Search Google Scholar
    • Export Citation
  • Whittier J.M., Tokarz R.R. (1992): Physiological regulation of sexual behavior in female reptiles. In: Biology of the Reptilia. Physiology E: Hormones, Brain and Behavior, Vol. 18, p.  24-69. Gans C., Crews D., Eds, University of Chicago Press, Chicago.

    • Search Google Scholar
    • Export Citation
  • Ziegler I. (1965): Pterine als Wirkstoffe und Pigmente. Ergeb. Physiol. 56: 1-66.

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 90 40 7
Full Text Views 59 3 0
PDF Downloads 8 1 0