Skip to main content
Log in

Multimodal sexual signals in male ocellated lizards Lacerta lepida: vitamin E in scent and green coloration may signal male quality in different sensory channels

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

The mechanisms that confer honesty to multiple sexual signals of vertebrates remain less known. We suggest that vitamin E in the scent (femoral secretions) and carotenoids in coloration of Lacerta lepida lizards might advertise quality because they are relevant in metabolism as major antioxidants and have a dietary origin. Results showed that there may be similar trade-offs between immunity and both chemical and visual signaling, as males with more vitamin E in secretions and those with more greenish, darker, and saturated carotenoid-dependent colorations had a higher immune response. This suggests that only high-quality males can divert from metabolism and allocate enough vitamin E to secretions and enough carotenoids to coloration. Therefore, information provided by visual and chemical signals is congruent. The use of multiple sensory channels may allow signaling a male quality under different circumstances or reinforce the reliability of the signal when both signals are perceived simultaneously. However, we also found that characteristics of carotenoid-dependent coloration mirror the amounts of vitamin E in secretions. This might support that carotenoids, which are not true antioxidants in the organism, would just reflect and “inform” on the actual contents of metabolic antioxidant vitamin E, which is part of the true system that prevent oxidation. We suggest that the metabolic roles of vitamins might be the actual basis of honesty of many sexual displays, and that carotenoid-based signals might be just the visible part of the whole system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aitchison J (1986) The statistical analysis of compositional data: monographs in statistics and applied probability. Chapman and Hall, London

    Google Scholar 

  • Alberts AC (1992) Constraints on the design of chemical communication systems in terrestrial vertebrates. Am Nat 139:62–89

    Article  Google Scholar 

  • Alberts AC (1993) Chemical and behavioral studies of femoral gland secretions in iguanid lizards. Brain Behav Evol 41:255–260

    Article  CAS  PubMed  Google Scholar 

  • Aragón P, López P, Martín J (2001) Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implication of field spatial relationships between males. Behav Ecol Sociobiol 50:128–133

    Article  Google Scholar 

  • Arnold ED, Ovenden DW (2002) A field guide to the reptiles and amphibians of Britain and Europe. Collins, London

    Google Scholar 

  • Belliure J, Smith L, Sorci G (2004) Effect of testosterone on T cell-mediated immunity in two species of Mediterranean lacertid lizards. J Exp Zool 301A:411–418

    Article  CAS  Google Scholar 

  • Bender DA (2009) Nutritional biochemistry of the vitamins, 2nd edn. Cambridge Univ press, Cambridge

    Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  CAS  PubMed  Google Scholar 

  • Brigelius-Flohe R, Traber MG (1999) Vitamin E: function and metabolism. FASEB J 13:1145–1155

    CAS  PubMed  Google Scholar 

  • Burton GW, Traber MG (1990) Vitamin E: antioxidant activity, biokinetics, and bioavailability. Annu Rev Nutr 10:357–382

    Article  CAS  PubMed  Google Scholar 

  • Carazo P, Font E, Desfilis E (2007) Chemosensory assessment of rival competitive ability and scent mark function in a lizard (Podarcis hispanica). Anim Behav 74:895–902

    Article  Google Scholar 

  • Castilla A, Bauwens D (1992) Habitat selection by the lizard Lacerta lepida in a Mediterranean oak forest. Herpetol J 2:27–30

    Google Scholar 

  • Christen S, Woodall AA, Shigenaga MK, Southwell-Keely PT, Duncan MW, Ames BN (1997) γ-Tocopherol traps mutagenic electrophiles such as NOx and complements α-tocopherol: physiological implications. Proc Natl Acad Sci USA 94:3217–3222

    Article  CAS  PubMed  Google Scholar 

  • Cooper WE, Greenberg N (1992) Reptilian coloration and behavior. In: Gans C, Crews D (eds) Biology of the Reptilia, vol 18. University of Chicago Press, Chicago, pp 298–422

    Google Scholar 

  • 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 USA 100:10341–10346

    Article  CAS  PubMed  Google Scholar 

  • Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:125–153

    Article  Google Scholar 

  • Evans HM, Bishop KS (1922) On the existence of a hitherto unrecognized dietary factor essential for reproduction. Science 56:650–651

    Article  CAS  PubMed  Google Scholar 

  • Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a carotenoid-based secondary sexual trait. Science 300:103

    Article  CAS  PubMed  Google Scholar 

  • Fleishman LJ, Bowman M, Saunders D, Miller WE, Rury MJ, Loew ER (1997) The visual ecology of Puerto Rican anoline lizards: habitat light and spectral sensitivity. J Comp Physiol A 181:446–460

    Article  Google Scholar 

  • Font E, Pérez i de Lanuza G, Sampedro C (2009) Ultraviolet reflectance and cryptic sexual dichromatism in the ocellated lizard, Lacerta (Timon) lepida (Squamata: Lacertidae). Biol J Linn Soc 97:766–780

    Article  Google Scholar 

  • Fraser DR (1995) Vitamin D. Lancet 345:104–107

    Article  CAS  PubMed  Google Scholar 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    Article  CAS  PubMed  Google Scholar 

  • Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  • Hayes CE, Nashold FE, Spach KM, Pedersen LB (2003) The immunological functions of the vitamin D endocrine system. Cell Mol Biol 49:277–300

    CAS  PubMed  Google Scholar 

  • Kopena R, López P, Martín J (2009) Lipophilic compounds from the femoral gland secretions of male Hungarian green lizards, Lacerta viridis. Z Naturforsch C 64:434–440

    CAS  PubMed  Google Scholar 

  • Kotiaho JS (2001) Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol Rev 76:365–376

    Article  CAS  PubMed  Google Scholar 

  • Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510

    Google Scholar 

  • Loew ER, Fleishman LJ, Foster RG, Provencio I (2002) Visual pigments and oil droplets in diurnal lizards: a comparative study of Caribbean anoles. J Exp Biol 205:927–938

    PubMed  Google Scholar 

  • López P, Martín J (2005) Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol Lett 1:404–406

    Article  PubMed  Google Scholar 

  • López P, Martín J (2006) Lipids in the femoral gland secretions of male Schreiber's green lizards, Lacerta schreiberi. Z Naturforsch C 61:763–768

    PubMed  Google Scholar 

  • López P, Martín J, Cuadrado M (2002) Pheromone mediated intrasexual aggression in male lizards, Podarcis hispanicus. Aggress Behav 28:154–163

    Article  Google Scholar 

  • López P, Martín J, Cuadrado M (2003) Chemosensory cues allow male lizards Psammodromus algirus to override visual concealment of sexual identity by satellite males. Behav Ecol Sociobiol 54:218–224

    Article  Google Scholar 

  • López P, Amo L, Martín J (2006) Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. J Chem Ecol 32:473–488

    Article  PubMed  Google Scholar 

  • López P, Gabirot M, Martín J (2009a) Immune challenge affects sexual coloration of male Iberian wall lizards. J Exp Zool A Ecol Genet Physiol 311:96–104

    Article  PubMed  Google Scholar 

  • López P, Gabirot M, Martín J (2009b) Immune activation affects chemical sexual ornaments of male Iberian wall lizards. Naturwissenschaften 96:65–69

    Article  PubMed  Google Scholar 

  • Mardones P, Rigotti A (2004) Cellular mechanisms of vitamin E uptake: relevance in α-tocopherol metabolism and potential implications for disease. J Nutr Biochem 15:252–260

    Article  CAS  PubMed  Google Scholar 

  • Martín J, López P (2000) Chemoreception, symmetry and mate choice in lizards. Proc R Soc Lond B 267:1265–1269

    Article  Google Scholar 

  • Martín J, López P (2006a) Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Funct Ecol 20:1087–1096

    Article  Google Scholar 

  • Martín J, López P (2006b) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc Lond B 273:2619–2624

    Article  Google Scholar 

  • Martín J, López P (2009) Multiple color signals may reveal multiple messages in male Schreiber's green lizards, Lacerta schreiberi. Behav Ecol Sociobiol 63:1743–1765

    Article  Google Scholar 

  • Martín J, López P (in press) Pheromones and reproduction in Reptiles. In: Norris DO, Lopez KH (eds) Hormones and reproduction in Vertebrates. Reptiles. Academic Press, San Diego, California

  • Martín J, Moreira PL, López P (2007) Status-signalling chemical badges in male Iberian rock lizards. Funct Ecol 21:568–576

    Article  Google Scholar 

  • Martín J, Amo L, López P (2008) Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis. Naturwissenschaften 95:293–300

    Article  PubMed  Google Scholar 

  • Martínez A, Rodríguez-Girones MA, Barbosa A, Costas M (2008) Donator acceptor map for carotenoids, melatonin and vitamins. J Phys Chem A 112:9037–9042

    Article  PubMed  Google Scholar 

  • Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the Reptilia, vol 18. University of Chicago Press, Chicago, pp 114–228

    Google Scholar 

  • Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 1. Mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147

    Google Scholar 

  • Müller-Schwarze D (2006) Chemical ecology of vertebrates. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  Google Scholar 

  • Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B (Suppl) 270:254–256

    Article  Google Scholar 

  • Ortuño J, Esteban MA, Meseguer J (2000) High dietary intake of α-tocopherol acetate enhances the nonspecific immune response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 10:293–307

    Article  PubMed  Google Scholar 

  • Pérez-Mellado V (1998) Lacerta lepida (Daudin, 1802). In: Ramos MA (ed) Fauna Ibérica, vol 10, Museo Nacional de Ciencias Naturales. CSIC, Madrid, pp 198–207

    Google Scholar 

  • Ressel S, Schall JJ (1989) Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78:158–164

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defence and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Svensson E, Sinervo B, Comendant T (2001) Density-dependent competition and selection on immune function in genetic lizard morphs. Proc Natl Acad Sci USA 98:12561–12565

    Article  CAS  PubMed  Google Scholar 

  • Tella JL, Lemus JA, Carrete M, Blanco G (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. PloS ONE 3:e3295

    Article  PubMed  Google Scholar 

  • Václav R, Prokop P, Fekiac V (2007) Expression of breeding coloration in European green lizards (Lacerta viridis): variation with morphology and tick infestation. Can J Zool 85:1199–1206

    Article  Google Scholar 

  • Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169–174

    Article  Google Scholar 

  • Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones? Am Nat 143:936–938

    Article  Google Scholar 

  • Weldon PJ, Flachsbarth B, Schulz S (2008) Natural products from the integument of nonavian reptiles. Nat Prod Rep 25:738–756

    Article  CAS  PubMed  Google Scholar 

  • Westneat DF, Birkhead TR (1998) Alternative hypothesis linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065–1073

    Article  Google Scholar 

  • Whiting MJ, Webb JK, Keogh JS (2009) Flat lizard female mimics use sexual deception in visual but not chemical signals. Proc R Soc B 276:1585–1591

    Article  PubMed  Google Scholar 

  • Winklhofer-Roob BM, Rock E, Ribalta J, Shmerling DH, Roob JM (2003) Effects of vitamin E and carotenoid status on oxidative stress in health and disease. Evidence obtained from human intervention studies. Mol Aspects Med 24:391–402

    Article  CAS  PubMed  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, Cambridge

    Book  Google Scholar 

Download references

Acknowledgments

We thank two anonymous reviewers for their helpful comments and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the project MCI-CGL2008-02119/BOS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Martín.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martín, J., López, P. Multimodal sexual signals in male ocellated lizards Lacerta lepida: vitamin E in scent and green coloration may signal male quality in different sensory channels. Naturwissenschaften 97, 545–553 (2010). https://doi.org/10.1007/s00114-010-0669-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-010-0669-8

Keywords

Navigation