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Femoral secretions and copulatory plugs convey chemical information about male identity and dominance status in Iberian rock lizards (Lacerta monticola)

  • Pedro L. Moreira
  • Pilar López
  • José Martín
Original Article

Abstract

Socially dominant males often signal their status to rival males and/or females. We tested the hypotheses that Lacerta monticola femoral gland secretions and copulatory plugs convey chemical information about male identity and dominance status. We estimated male dominance status by staging male–male agonistic encounters in a neutral arena. We then conducted two experiments to compare male tongue-flick behavior toward chemical stimuli consisting of cotton swabs bearing (1) deionized water (control), the lizard’s own femoral secretions, and the femoral secretions of another male and (2) phosphate-buffered saline solution (control), the lizard’s own plug products, and the plug products of another male. Results indicate that males discriminated their own femoral secretions and plugs from those of other males. They also discriminated morphological attributes of other males that were associated with dominance status based on chemical cues arising from femoral secretions and discriminated the dominance status of other males based on chemical cues arising from the plugs. Femoral secretions that convey information about male identity and dominance status may be hypothesized to function in the establishment of L. monticola dominance hierarchies through scent-marking of territories. We suggest that copulatory plugs and femoral secretions may allow males to scent-mark the female body and postulate that this behavior may influence male and female reproductive decisions under selective pressures of sperm competition.

Keywords

Chemical signals Copulatory plugs Femoral gland secretions Social dominance Sperm competition 

Notes

Acknowledgements

We thank El Ventorrillo MNCN field station for use of their facilities. Research was supported by a postdoctoral fellowship from Fundação para a Ciência e a Tecnologia (SFRH/BPD/14939/2004) to PM, by the MEC project CGL2005-00391/BOSM, and conducted under license from Instituto da Conservação da Natureza—Parque Natural da Serra da Estrela, Portugal.

References

  1. Alberts AC (1989) Ultraviolet visual sensitivity in desert iguanas: implication for pheromone detection. Anim Behav 38:129–137CrossRefGoogle Scholar
  2. Alberts AC (1990) Chemical properties of femoral gland secretions in the desert iguana, Dipsosaurus dorsalis. J Chem Ecol 16:13–25CrossRefGoogle Scholar
  3. Alberts AC (1992a) Density dependent scent gland activity in desert iguanas. Anim Behav 44:774–776CrossRefGoogle Scholar
  4. Alberts AC (1992b) Pheromonal self-recognition in desert iguanas. Copeia 1992:229–232CrossRefGoogle Scholar
  5. Alberts AC (1993) Chemical and behavioral studies of femoral gland secretions in iguanid lizards. Brain Behav Evol 41:255–260PubMedCrossRefGoogle Scholar
  6. Alberts AC, Pratt NC, Phillipis JA (1992) Seasonal productivity of lizard femoral glands: relationship to social dominance and androgen levels. Physiol Behav 51:729–733PubMedCrossRefGoogle Scholar
  7. Alberts AC, Phillipis JA, Werner DI (1993) Sources of intraspecific variability in the protein composition of lizard femoral gland secretions. Copeia 1993:775–781CrossRefGoogle Scholar
  8. Alberts AC, Werner DI (1993) Chemical recognition of unfamiliar conspecifics by green iguanas: functional significance of different signal components. Anim Behav 46:197–199CrossRefGoogle Scholar
  9. Anderholm S, Olsson M, Wapstra E, Ryberg K (2004) Fit and fat from enlarged badges: a field experiment on male sand lizards. Proc R Soc Lond B 271:142–144CrossRefGoogle Scholar
  10. Andersson M (1994) Sexual selection. Princeton Univ. Press, PrincetonGoogle Scholar
  11. Aragón P, López P, Martín J (2001a) Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implications from field spatial relationships between males. Behav Ecol Sociobiol 50:128–133CrossRefGoogle Scholar
  12. Aragón P, López P, Martín J (2001b) Discrimination of femoral gland secretions from familiar and unfamiliar conspecifics by male Iberian rock-lizards, Lacerta monticola. J Herpetol 35:346–350CrossRefGoogle Scholar
  13. Aragón P, López P, Martín J (2001c) Effects of conspecific chemical cues on settlement and retreat-site selection of male lizards, Lacerta monticola. J Herpetol 35:681–684CrossRefGoogle Scholar
  14. Aragón P, López P, Martín J (2001d) Seasonal changes in activity and spatial and social relationships of the Iberian rock lizard, Lacerta monticola. Can J Zool 79:1965–1971CrossRefGoogle Scholar
  15. Aragón P, López P, Martín J (2003) Differential avoidance responses to chemical cues from familiar and unfamiliar conspecifics by male Iberian rock lizards (Lacerta monticola). J Herpetol 37:583–585CrossRefGoogle Scholar
  16. Aragón P, López P, Martín J (2004) The ontogeny of spatio-temporal tactics and social relationships of adult male Iberian rock lizards, Lacerta monticola. Ethology 110:1001–1019CrossRefGoogle Scholar
  17. Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399Google Scholar
  18. Birkhead TR, Møller AP (eds) (1998) Sperm competition and sexual selection. Academic, LondonGoogle Scholar
  19. Calsbeek R, Sinervo B (2002) Uncoupling direct and indirect components of female choice in the wild. Proc Natl Acad Sci U S A 99:14897–14902PubMedCrossRefGoogle Scholar
  20. Cooper WE Jr (1994) Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. J Chem Ecol 20:439–487CrossRefGoogle Scholar
  21. Devine MC (1975) Copulatory plugs in snakes: enforced chastity. Science 187:844–845PubMedCrossRefGoogle Scholar
  22. Devine MC (1977) Copulatory plugs, restricted mating opportunities and reproductive competition among male garter snakes. Nature 267:345–346PubMedCrossRefGoogle Scholar
  23. Devine MC (1984) Potential for sperm competition in reptiles: behavioral and physiological consequences. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 509–521Google Scholar
  24. Fox H (1977) The urogenital system of reptiles. In: Gans C, Parsons TS (eds) Morphology E. Biology of the reptilia, vol 6. Academic, New York, pp 1–157Google Scholar
  25. Glinski TH, Krekorian CO’N (1985) Individual recognition in free-living adult male desert iguanas, Dipsosaurus dorsalis. J Herpetol 19:541–544CrossRefGoogle Scholar
  26. Gosling LM (1990) Scent-marking by resource holders: alternative mechanisms for advertising the costs of competition. In: Duvall D, Muller-Schwarze D, Silverstein RM (eds) Chemical signals in vertebrates, vol 5. Oxford Univ. Press, Oxford, pp 315–328Google Scholar
  27. Gosling LM, Roberts SC (2001) Scent-marking by male mammals: cheat-proof signals to competitors and mates. Adv Stud Behav 30:169–217Google Scholar
  28. Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford Univ. Press, New YorkGoogle Scholar
  29. Halpern M (1992) Nasal chemical senses in reptiles: structure and function. In: Gans C, Crews D (eds) Brain, hormones, and behavior. Biology of the reptilia, vol 18. University of Chicago, Chicago, pp 423–522Google Scholar
  30. In den Bosch HAJ (1994) First record of mating plugs in lizards. Amphib-Reptil 15:89–93CrossRefGoogle Scholar
  31. Jaeger RG, Gillette JR, Cooper RC (2004) Sexual coercion in a territorial salamander: males punish socially polyandrous female partners. Anim Behav 63:871–877CrossRefGoogle Scholar
  32. Krohmer RW (2004) Variation in seasonal ultrastructure of sexual granules in the renal sex segment of the Northern Water Snake, Nerodia sipedon sipedon. J Morphol 261:70–80PubMedCrossRefGoogle Scholar
  33. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121Google Scholar
  34. López P, Martín J (2001) Fighting rules and rival recognition reduce the costs of aggression in male lizards, Podarcis hispanica. Behav Ecol Sociobiol 49:111–116CrossRefGoogle Scholar
  35. López P, Martín J (2005) Chemical compounds from femoral gland secretions of male Iberian rock lizards, Lacerta monticola cyreni. Z Naturforsch C 60:632–636PubMedGoogle Scholar
  36. López P, Muñoz A, Martín J (2002) Symmetry, male dominance and female mate preferences in the Iberian rock lizard, Lacerta monticola. Behav Ecol Sociobiol 52:342–347CrossRefGoogle Scholar
  37. Marler CA, Moore MC (1988) Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behav Ecol Sociobiol 23:21–26CrossRefGoogle Scholar
  38. Marler CA, Moore MC (1989) Time and energy costs of aggression in testosterone-implanted free-living male mountain spiny lizards. Physiol Zool 62:1334–1350Google Scholar
  39. Martín J, López P (2000) Chemoreception, symmetry and mate choice in lizards. Proc R Soc Lond B 267:1265–1269CrossRefGoogle Scholar
  40. Martín J, Salvador A (1993) Tail loss reduces mating success in the Iberian rock-lizard, Lacerta monticola. Behav Ecol Sociobiol 32:185–189CrossRefGoogle Scholar
  41. Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Brain, hormones, and behavior. Biology of the reptilia, vol 18. University of Chicago, Chicago, pp 114–228Google Scholar
  42. Mathis A (1990) Territorial salamanders assess sexual and competitive information using chemical signals. Anim Behav 40:953–962CrossRefGoogle Scholar
  43. Mayer W, Arribas O (2003) Phylogenetic relationships of the European lacertid genera Archaeolacerta and Iberolacerta and their relationships to some other ‘Archaeolacertae’ (sensu lato) from Near East, derived from mitochondrial DNA sequences. J Zoolog Syst Evol Res 41:157–161CrossRefGoogle Scholar
  44. Moore AJ, Gowaty PA, Wallin WG, Moore PJ (2001) Sexual conflict and the evolution of female mate choice and male social dominance. Proc R Soc Lond B 268:517–523CrossRefGoogle Scholar
  45. Moore AJ, Gowaty PA, Moore PJ (2003) Females avoid manipulative males and live longer. J Evol Biol 16:523–530PubMedCrossRefGoogle Scholar
  46. Moreira PL (2002) Sexual selection and sperm competition in the Iberian rock lizard (Lacerta monticola). Ph.D. thesis, University of SheffieldGoogle Scholar
  47. Moreira PL, Birkhead TR (2003) Copulatory plugs in the Iberian rock lizard do not prevent insemination by rival males. Funct Ecol 17:796–802CrossRefGoogle Scholar
  48. Moreira PL, Birkhead TR (2004) Copulatory plug displacement and prolonged copulation in the Iberian rock lizard (Lacerta monticola). Behav Ecol Sociobiol 56:290–297CrossRefGoogle Scholar
  49. Olsson M (1994a) Nuptial coloration in the sand lizard, Lacerta agilis: an intra-sexually selected cue to fighting ability. Anim Behav 48:607–613CrossRefGoogle Scholar
  50. Olsson M (1994b) Rival recognition affects male contest behavior in sand lizards (Lacerta agilis). Behav Ecol Sociobiol 35:249–252CrossRefGoogle Scholar
  51. Olsson M, Madsen T (1995) Female choice on male quantitative traits in lizards—why is it so rare? Behav Ecol Sociobiol 36:179–184CrossRefGoogle Scholar
  52. Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 503–577CrossRefGoogle Scholar
  53. Olsson M, Madsen T (2001) Promiscuity in sand lizard (Lacerta agilis) and adder snakes (Vipera berus): causes and consequences. J Hered 92:190–197PubMedCrossRefGoogle Scholar
  54. Olsson M, Shine R (2000) Ownership influences the outcome of male–male contests in the scincid lizard, Niveoscincus microlepidotus. Behav Ecol 11:587–590CrossRefGoogle Scholar
  55. Olsson M, Madsen T, Ujvari B, Wapstra E (2004) Fecundity and MHC affects ejaculation tactics and paternity bias in sand lizards. Evolution 58:906–909PubMedGoogle Scholar
  56. Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications. Kluwer, Netherlands, pp 335–364Google Scholar
  57. Parker TH (2003) Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus). Evolution 57:2157–2165PubMedGoogle Scholar
  58. Parker TH, Ligon JD (2002) Dominant male red junglefowl (Gallus gallus) test the dominance status of other males. Behav Ecol Sociobiol 53:20–24CrossRefGoogle Scholar
  59. Parker TH, Ligon JD (2003) Female mating preferences in red junglefowl: a meta-analysis. Ethol Ecol Evol 15:63–72Google Scholar
  60. Pizzari T, Froman DP, Birkhead TR (2002) Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus. Heredity 88:112–116PubMedCrossRefGoogle Scholar
  61. Pizzari T (2003) Food, vigilance, and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird. Behav Ecol 14:593–601CrossRefGoogle Scholar
  62. Qvarnström A, Forsgren E (1998) Should females prefer dominant males? Trends Ecol Evol 13:498–501CrossRefGoogle Scholar
  63. Ross P, Crews D (1977) Influence of the seminal plug on mating behaviour in the garter snake. Nature 267:344–345PubMedCrossRefGoogle Scholar
  64. Ross P, Crews D (1978) Stimuli influencing mating behavior in the garter snake, Thamnophis radix. Behav Ecol Sociobiol 4:133–142CrossRefGoogle Scholar
  65. Sever DM, Stevens RA, Ryan TJ, Hamlett WC (2002) Ultrastructure of the reproductive system of the Black Swamp Snake (Seminatrix pygaea). III. Sexual segment of the male kidney. J Morphol 252:238–254PubMedCrossRefGoogle Scholar
  66. Shine R, Olsson M, Mason RT (2000) Chastity belts in gartersnakes: the functional significance of mating plugs. Biol J Linn Soc 70:377–390CrossRefGoogle Scholar
  67. Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioural sciences, 2nd edn. McGraw-Hill, SingaporeGoogle Scholar
  68. Taylor GT, Haller J, Bartko G, Weiss J (1984) Conspecific urine marking in male–female pairs of laboratory rats. Physiol Behav 32:541–546PubMedCrossRefGoogle Scholar
  69. Tokarz RR (1995) Mate choice in lizards: a review. Herpetol Monogr 9:17–40CrossRefGoogle Scholar
  70. Verwaijen D, Van Damme R, Herrel A (2002) Relationship between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct Ecol 16:842–850CrossRefGoogle Scholar
  71. Weil MR, Aldridge RD (1984) Seasonal histochemistry of the renal sexual segment in the male Northern Water Snake (Nerodia sipedon). J Exp Zool 210:327–332CrossRefGoogle Scholar
  72. Wise SE, Verret FD, Jaeger RG (2004) Tail autotomy in territorial salamanders influences scent marking by residents and behavioral responses of intruders to resident chemical cues. Copeia 2004:165–172CrossRefGoogle Scholar
  73. Zucker N (1994) A dual status-signalling system: a matter of redundancy or differing roles? Anim Behav 47:15–22CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Pedro L. Moreira
    • 1
  • Pilar López
    • 2
  • José Martín
    • 2
  1. 1.Centro de Biologia AmbientalFaculdade de Ciências da Universidade de LisboaLisboaPortugal
  2. 2.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales, CSICMadridSpain

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