Behavioral Ecology and Sociobiology

, Volume 68, Issue 5, pp 861–870 | Cite as

The scent of sun worship: basking experience alters scent mark composition in male lizards

  • Robert J. P. Heathcote
  • Emily Bell
  • Patrizia d’Ettorre
  • Geoffrey M. While
  • Tobias Uller
Original Paper

Abstract

Signals used in female choice should honestly advertise the benefits that males can provide, with direct benefits often argued as being more important than indirect benefits. However, the nature of direct benefits in species without paternal care or nuptial gifts is poorly understood. Previous studies on lizards suggest that females decide where to settle and assumedly who to mate with based on information contained in scent marks from territorial males. Access to high-quality thermal resources is crucial for female reproductive success. Females may therefore be able to detect and exploit thermal-induced variation in the chemical composition of male scent marks when assessing the quality of his territory. We show that the amount of time male wall lizards (Podarcis muralis) are allowed to bask significantly alters the chemical composition of their femoral secretions used in scent marking. The direction of the change is consistent with adaptive plasticity to maintain signalling efficacy under warm conditions that increase evaporation of femoral secretions. The compounds affected by basking experience included those previously associated with male quality or shown to mediate male–male competition in lizards. However, whilst female lizards could discriminate between scent marks of males that had experienced different basking conditions, they did not preferentially associate with the scent from males from high-quality thermal conditions. These results highlight the potential importance of a previously neglected environmental effect on chemical signalling. We suggest thermal effects may have significant consequences for scent-mark composition in variable environments, with potential repercussions on olfactory communication in lizards.

Keywords

Chemical signalling Thermal plasticity Podarcis muralis Scent mark Female choice 

Supplementary material

265_2014_1700_MOESM1_ESM.docx (64 kb)
ESM 1(DOCX 63 kb)

References

  1. Aitchison J (1986) The statistical analysis of compositional data. Chapman & Hall, LondonCrossRefGoogle Scholar
  2. Alberts AC (1992) Constraints on the design of chemical communication systems in terrestrial vertebrates. Am Nat 139:S62–S89CrossRefGoogle Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. Avery RA (1971) Estimates of food consumption by the lizard Lacerta vivipara Jacquin. J Anim Ecol 40:351–365CrossRefGoogle Scholar
  5. Avery RA (1978) Activity patterns, thermoregulation and food consumption in two sympatric lizard species (Podarcis muralis and P. sicula) from central Italy. J Anim Ecol 47:143–158CrossRefGoogle Scholar
  6. Barbosa D, Font E, Desfilis E, Carretero M (2006) Chemically mediated species recognition in closely related Podarcis wall lizards. J Chem Ecol 32:1587–1598PubMedCrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classesGoogle Scholar
  8. Bushmann P, Atema J (2000) Chemically mediated mate location and evaluation in the lobster, Homarus americanus. J Chem Ecol 26:883–899CrossRefGoogle Scholar
  9. Calsbeek R, Sinervo B (2002) Uncoupling direct and indirect components of female choice in the wild. Proc Natl Acad Sci U S A 99:14897–14902PubMedCentralPubMedCrossRefGoogle Scholar
  10. Calsbeek R, Sinervo B (2007) Correlational selection on lay date and life-history traits: experimental manipulations of territory and nest site quality. Evolution 61:1071–1083PubMedCrossRefGoogle Scholar
  11. Candolin U (2000) Male-male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus). Behav Ecol Sociobiol 49:57–61CrossRefGoogle Scholar
  12. Carazo P, Font E, Desfilis E (2007) Chemosensory assessment of rival competitive ability and scent-mark function in a lizard, Podarcis hispanica. Anim Behav 74:895–902CrossRefGoogle Scholar
  13. Carazo P, Font E, Desfilis E (2008) Beyond ‘nasty neighbours’ and ‘dear enemies’? Individual recognition by scent marks in a lizard (Podarcis hispanica). Anim Behav 76:1953–1963CrossRefGoogle Scholar
  14. Carazo P, Font E, Desfilis E (2011) The role of scent marks in female choice of territories and refuges in a lizard Podarcis hispanica. J Comp Psychol 125:362–365PubMedCrossRefGoogle Scholar
  15. Clutton-Brock TH, Harvey PH (1978) Mammals, resources and reproductive strategies. Nature 273:191–195PubMedCrossRefGoogle Scholar
  16. Cooper W (1994) Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. J Chem Ecol 20:439–487PubMedCrossRefGoogle Scholar
  17. Cooper WE Jr, Trauth SE (1992) Discrimination of conspecific male and female cloacal chemical stimuli by males and possession of a probable pheromone gland by females in a cordylid lizard, Gerrhosaurus nigrolineatus. Herpetologica 48:229–236Google Scholar
  18. Damme RV, Bauwens D, Verheyen RF (1987) Thermoregulatory responses to environmental seasonality by the lizard Lacerta vivipara. Herpetologica 43:405–415Google Scholar
  19. Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci U S A 100:10341–10346PubMedCentralPubMedCrossRefGoogle Scholar
  20. Dussourd DE, Harvis CA, Meinwald J, Eisner T (1991) Pheromonal advertisement of a nuptial gift by a male moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A 88:9224–9227PubMedCentralPubMedCrossRefGoogle Scholar
  21. Edsman L (1990) Territoriality and competition in wall lizards. Dissertation, University of StockholmGoogle Scholar
  22. Eisner T, Smedley SR, Young DK, Eisner M, Roach B, Meinwald J (1996) Chemical basis of courtship in a beetle (Neopyrochroa flabellata): cantharidin as precopulatory “enticing” agent. Proc Natl Acad Sci U S A 93:6494–6498PubMedCentralPubMedCrossRefGoogle Scholar
  23. Emlen S, Oring L (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223PubMedCrossRefGoogle Scholar
  24. Escobar CM, Escobar CA, Labra A, Niemeyer HM (2003) Chemical composition of precloacal secretions of two Liolaemus fabiani populations: are they different? J Chem Ecol 29:629–638PubMedCrossRefGoogle Scholar
  25. Falls JB (1982) Individual recognition by sound in birds. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds. Academic, New York, pp 237–278Google Scholar
  26. Font E, Barbosa D, Sampedro C, Carazo P (2012) Social behavior, chemical communication, and adult neurogenesis: studies of scent mark function in Podarcis wall lizards. Gen Comp Endocrinol 177:9–17PubMedCrossRefGoogle Scholar
  27. Fox SF, Rose E, Myers R (1981) Dominance and the acquisition of superior home ranges in the lizard Uta Stansburiana. Ecology 62:888–893CrossRefGoogle Scholar
  28. Frazer JFD (1964) Introduced species of amphibians and reptiles in mainland Britain. Br J Herpetol 3:145–150Google Scholar
  29. Gabirot M, Castilla AM, López P, Martín J (2010a) Differences in chemical signals may explain species recognition between an island lizard, Podarcis atrata, and related mainland lizards, P. hispanica. Biochem Syst Ecol 38:521–528CrossRefGoogle Scholar
  30. Gabirot M, Castilla AM, López P, Martín J (2010b) Chemosensory species recognition may reduce the frequency of hybridization between native and introduced lizards. Can J Zool 88:73–80CrossRefGoogle Scholar
  31. Gosling LM, Atkinson NW, Collins SA, Roberts RJ, Walters RL (1996) Avoidance of scent-marked areas depends on the intruder’s body size. Behaviour 133:491–502CrossRefGoogle Scholar
  32. Haenel GJ, Smith LC, John-Alder HB, Guyer C (2003) Home-range analysis in Sceloporus undulatus (eastern fence lizard). I. Spacing patterns and the context of territorial behavior. Copeia 2003:99–112CrossRefGoogle Scholar
  33. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339CrossRefGoogle Scholar
  34. Hoi-Leitner M, Nechtelberger H, Hoi H (1995) Song rate as a signal for nest site quality in blackcaps (Sylvia atricapilla). Behav Ecol Sociobiol 37:399–405CrossRefGoogle Scholar
  35. Houck LD (2009) Pheromone communication in amphibians and reptiles. Annu Rev Physiol 71:161–176PubMedCrossRefGoogle Scholar
  36. Huey RB, Peterson CR, Arnold SJ, Porter WP (1989) Hot rocks and not-so-hot rocks: retreat-site selection by garter snakes and its thermal consequences. Ecology 70:931–944CrossRefGoogle Scholar
  37. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289PubMedCrossRefGoogle Scholar
  38. Kirkpatrick M (1996) Good genes and direct selection in the evolution of mating preferences. Evolution 50:2125–2140CrossRefGoogle Scholar
  39. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  40. Kopena R, Martín J, López P, Herczeg G (2011) Vitamin E supplementation increases the attractiveness of males’ scent for female European green lizards. PLoS ONE 6:e19410PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kwiat GA, Gist DH (1987) Annual reproductive cycle of an introduced population of European wall lizards (Podarcis muralis) in Ohio. J Herpetol 21:205–209CrossRefGoogle Scholar
  42. Labra A (2011) Chemical stimuli and species recognition in Liolaemus lizards. J Zool 285:215–221CrossRefGoogle Scholar
  43. Landolt PJ, Phillips TW (1997) Host plant influences on sex pheromone behavior of phytophagous insects. Annu Rev Entomol 42:371–391PubMedCrossRefGoogle Scholar
  44. Lever C (1977) The naturalized animals of the British Isles. Hutchinson, LondonGoogle Scholar
  45. López P, Martín J (2005) Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol Lett 1:404–406PubMedCentralPubMedCrossRefGoogle Scholar
  46. 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
  47. Martín J, López P (2000) Chemoreception, symmetry and mate choice in lizards. Proc R Soc Lond B 267:1265–1269Google Scholar
  48. Martín J, López P (2006a) Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex. Chemoecology 16:31–38CrossRefGoogle Scholar
  49. Martín J, López P (2006b) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Philos Trans R Soc Lond B 273:2619–2624Google Scholar
  50. Martín J, López P (2007) Scent may signal fighting ability in male Iberian rock lizards. Biol Lett 3:125–127PubMedCentralPubMedCrossRefGoogle Scholar
  51. Martín J, López P (2012) Supplementation of male pheromone on rock substrates attracts female rock lizards to the territories of males: a field experiment. PLoS ONE 7:e30108PubMedCentralPubMedCrossRefGoogle Scholar
  52. Martín J, López P (2013) Effects of global warming on sensory ecology of rock lizards: increased temperatures alter the efficacy of sexual chemical signals. Funct Ecol 27:1332–1340CrossRefGoogle Scholar
  53. Martin J, Moreira PL, López P (2007) Status-signalling chemical badges in male Iberian rock lizards. Funct Ecol 21:568–576CrossRefGoogle Scholar
  54. Martín J, Amo L, López P (2008) Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis. Naturwissenschaften 95:293–300PubMedCrossRefGoogle Scholar
  55. Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the reptilia: hormones, brain and behavior. University of Chicago Press, Chicago, pp 114–228Google Scholar
  56. Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol A 196:729–749CrossRefGoogle Scholar
  57. McGregor PK (1993) Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Philos Trans R Soc Lond B 340:237–244CrossRefGoogle Scholar
  58. Michaelides S, While GM, Bell C, Uller T (2013) Human introductions create opportunities for intra-specific hybridization in an alien lizard. Biol Invasions 15:1101–1112CrossRefGoogle Scholar
  59. Moreira P, López P, Martín J (2006) Femoral secretions and copulatory plugs convey chemical information about male identity and dominance status in Iberian rock lizards (Lacerta monticola). Behav Ecol Sociobiol 60:166–174CrossRefGoogle Scholar
  60. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045CrossRefGoogle Scholar
  61. Öckinger E, Schweiger O, Crist TO, Debinski DM, Krauss J et al (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13:969–979PubMedGoogle Scholar
  62. Olsson M, Madsen T (1996) Costs of mating with infertile males selects for late emergence in female sand lizards (Lacerta agilis L.). Copeia 1996:462–464Google Scholar
  63. Olsson M, Wapstra E, Schwartz T, Madsen T, Ujvari B, Uller T (2011) In hot pursuit: fluctuating mating system and sexual selection in sand lizards. Evolution 65:574–583PubMedCrossRefGoogle Scholar
  64. Pérez i de Lanuza G, Font E, Carazo P (2013) Color-assortative mating in a color-polymorphic lacertid lizard. Behav Ecol 24:273–279CrossRefGoogle Scholar
  65. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
  66. Rouault J-D, Marican C, Wicker-Thomas C, Jallon J-M (2004) Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D. melanogaster and D. simulans. Genetica 120:195–212PubMedCrossRefGoogle Scholar
  67. Runemark A, Gabirot M, Svensson EI (2011) Population divergence in chemical signals and the potential for premating isolation between islet- and mainland populations of the Skyros wall lizard (Podarcis gaigeae). J Evol Biol 24:795–809PubMedCrossRefGoogle Scholar
  68. Salvi D, Harris DJ, Kaliontzopoulou A, Carretero MA, Pinho C (2013) Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard. BMC Evol Biol 13:147PubMedCentralPubMedCrossRefGoogle Scholar
  69. Schulte U, Hochkirch A, Lötters S, Rödder D, Schweiger S, Weimann T, Veith M (2012) Cryptic niche conservatism among evolutionary lineages of an invasive lizard. Glob Ecol Biogeogr 21:198–211CrossRefGoogle Scholar
  70. Shine R, Reed RN, Shetty S, Lemaster M, Mason RT (2002) Reproductive isolating mechanisms between two sympatric sibling species of sea snakes. Evolution 56:1655–1662PubMedGoogle Scholar
  71. Tallamy D, Gorski P, Burzon J (2000) Fate of male-derived cucurbitacins in spotted cucumber beetle females. J Chem Ecol 26:413–427CrossRefGoogle Scholar
  72. Tokarz RR (1985) Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Anim Behav 33:746–753CrossRefGoogle Scholar
  73. Trumbo ST, Eggert A-K (1994) Beyond monogamy: territory quality influences sexual advertisement in male burying beetles. Anim Behav 48:1043–1047CrossRefGoogle Scholar
  74. Vahed K (1998) The function of nuptial feeding in insects: a review of empirical studies. Biol Rev 73:43–78CrossRefGoogle Scholar
  75. Valdar W, Solberg LC, Gauguier D, Cookson WO, Rawlins JNP, Mott R, Flint J (2006) Genetic and environmental effects on complex traits in mice. Genetics 174:275–281CrossRefGoogle Scholar
  76. Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, CambridgeCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Robert J. P. Heathcote
    • 1
  • Emily Bell
    • 1
  • Patrizia d’Ettorre
    • 2
  • Geoffrey M. While
    • 1
    • 3
  • Tobias Uller
    • 1
    • 4
  1. 1.Edward Grey Institute, Department of ZoologyUniversity of OxfordOxfordUK
  2. 2.Laboratory of Experimental and Comparative EthologyUniversity of Paris 13, Sorbonne Paris CitéVilletaneuseFrance
  3. 3.School of ZoologyUniversity of TasmaniaSandy BayAustralia
  4. 4.Department of BiologyLund UniversityLundSweden

Personalised recommendations