The Role of Diet in Shaping the Chemical Signal Design of Lacertid Lizards

Abstract

Lizards communicate with others via chemical signals, the composition of which may vary among species. Although the selective pressures and constraints affecting chemical signal diversity at the species level remain poorly understood, the possible role of diet has been largely neglected. The chemical signals of many lizards originate from the femoral glands that exude a mixture of semiochemicals, and may be used in a variety of contexts. We analyzed the lipophilic fraction of the glandular secretions of 45 species of lacertid lizard species by gas chromatography/mass spectrometry. The proportions of nine major chemical classes (alcohols, aldehydes, fatty acids, furanones, ketones, steroids, terpenoids, tocopherols and waxy esters), the relative contributions of these different classes (‘chemical diversity’), and the total number of different lipophilic compounds (‘chemical richness’) varied greatly among species. We examined whether interspecific differences in these chemical variables could be coupled to interspecific variation in diet using data from the literature. In addition, we compared chemical signal composition among species that almost never, occasionally, or often eat plant material. We found little support for the hypothesis that the chemical profile of a given species’ secretion depends on the type of food consumed. Diet breadth did not correlate with chemical diversity or richness. The amount of plants or ants consumed did not affect the relative contribution of any of the nine major chemical classes to the secretion. Chemical diversity did not differ among lizards with different levels of plant consumption; however, chemical richness was low in species with an exclusive arthropod diet, suggesting that incorporating plants in the diet enables lizards to increase the number of compounds allocated to secretions, likely because a (partly) herbivorous diet allows them to include compounds of plant origin that are unavailable in animal prey. Still, overall, diet appears a relatively poor predictor of interspecific differences in the broad chemical profiles of secretions of lacertid lizards.

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References

  1. Alberts AC (1991) Phylogenetic and adaptive variation in lizard femoral gland secretions. Copeia 1991:69–79

    Article  Google Scholar 

  2. Alberts AC, Sharp TR, Werner DI, Weldon PJ (1992) Seasonal variation of lipids in femoral gland secretions of male green iguanas (Iguana iguana). J Chem Ecol 18:703–712

    CAS  Article  PubMed  Google Scholar 

  3. Aldrich JR, Chauhan K, Zhang Q (2016) Pharmacophagy in green lacewings (Neuroptera: Chrysopidae: Chrysopa spp)? PeerJ 4:e1564

    Article  PubMed  PubMed Central  Google Scholar 

  4. Apps PJ, Weldon PJ, Kramer M (2015) Chemical signals in terrestrial vertebrates: search for design features. Nat Prod Rep 32:1131–1153

    CAS  Article  PubMed  Google Scholar 

  5. Baeckens S, Edwards S, Huyghe K, Van Damme R (2015) Chemical signalling in lizards: an interspecific comparison of femoral pore number in Lacertidae. Biol J Linn Soc 114:44–57

    Article  Google Scholar 

  6. Baeckens S, Herrel A, Broeckhoven C, Vasilopoulou-Kampitsi M, Huyghe K, Goyens J, Van Damme R (2017a) Evolutionary morphology of the lizard chemosensory system. Sci Rep 7:10141

  7. Baeckens S, Huyghe K, Palme R, Van Damme R (2017b) Chemical communication in the lacertid lizard Podarcis muralis: the functional significance of testosterone. Acta Zool 98:94–103

    Article  Google Scholar 

  8. Baeckens S, Van Damme R, Cooper WE (2017c) How phylogeny and foraging ecology drive the level of chemosensory exploration in lizards and snakes. J Evol Biol 30:627–640

    CAS  Article  PubMed  Google Scholar 

  9. Barbehenn RV (2003) Antioxidants in grasshoppers: higher levels defend the midgut tissues of a polyphagous species than a graminivorous species. J Chem Ecol 29:683–702

    CAS  Article  PubMed  Google Scholar 

  10. Blair JA (1957) Pigments and pterins in the skin of the green mamba Dendroaspis viridis. Nature 180:1371

    CAS  Article  Google Scholar 

  11. Block E, Jang S, Matsunami H, Sekharan S, Dethier B, Ertem MZ et al (2015) Implausibility of the vibrational theory of olfaction. Proc Natl Acad Sci 112:201503054

    Google Scholar 

  12. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    Article  PubMed  Google Scholar 

  13. Bouam I, Necer A, Saoudi M, Tahar-Chaouch L, Khelfaoui F (2016) Diet and daily activity patterns of the lacertid lizard Psammodromus algirus (Sauria: Lacertidae) in a semi-arid Mediterranean region. Zool Ecol 26:244–252

    Article  Google Scholar 

  14. Brooker RM, Munday PL, Chivers DP, Jones GP (2015) You are what you eat: diet-induced chemical crypsis in a coral-feeding reef fish. Proc R Soc B Biol Sci 282:20141887. https://doi.org/10.1098/rspb.2014.1887

  15. Bryant BP, Atema J (1987) Diet manipulation affects social behavior of catfish: importance of body odor. J Chem Ecol 13:1645–1661

    CAS  Article  PubMed  Google Scholar 

  16. Carretero MA (2004) From set menu to a la carte: linking issues in trophic ecology of Mediterranean lacertids. Ital J Zool 71:121–133

    Article  Google Scholar 

  17. Conner WE, Roach B, Benedict E, Meinwald J, Eisner T (1990) Courtship pheromone production and body size as correlates of larval diet in males of the arctiid moth Utetheisa ornatrix. J Chem Ecol 16:543–552

    CAS  Article  PubMed  Google Scholar 

  18. Cooper WE Jr, Vitt LJ (2002) Distribution, extent, and evolution of plant consumption by lizards. J Zool 257:487–517

  19. Daly JW, Garraffo MH, Spande TF, Jaramillo C, Rand SA (1994) Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J Chem Ecol 20:943–955

  20. Daly JW, Garraffo MH, Spande TF, Snelling R, Jaramillo C (2000) Rand AS, Alkaloids common to microsympatric myrmicine ants and dendrobatid frogs Martin. J Chem Ecol 26:73–85

  21. Dumbacher JP, Beehler BM, Spande TF, Garraffo HM, Daly JW (1992) Homobatrachotoxin in the genus Pitohui: chemical defense in birds? Science 258:799–801

  22. Eisner T, Meinwald J (1995) The chemistry of sexual selection. Proc Natl Acad Sci U S A 92:50–55

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 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 29:629–638

    CAS  Article  PubMed  Google Scholar 

  24. Franco MI, Turin L, Mershin A, Skoulakis EMC (2011) Molecular vibration-sensing component in Drosophila melanogaster olfaction. Proc Natl Acad Sci 108:3797–3802

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    CAS  Article  PubMed  Google Scholar 

  26. Gabirot M, Castilla AM, López P, Martín J (2010) Chemosensory species recognition may reduce the frequency of hybridization between native and introduced lizards. Can J Zool 88:73–80

    CAS  Article  Google Scholar 

  27. Gabirot M, López P, Martín J (2012) Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards Podarcis hispanica mirrors population differences in chemical signals. Chemoecology 22:65–73

    CAS  Article  Google Scholar 

  28. Gabirot M, Raux L, Dell’Ariccia G, Bried J, Ramos R, Gonález-Solís J, Buatois B, Crochet PA, Bonadonna F (2016) Chemical labels differ between two closely related shearwater taxa. J Avian Biol 47:540–551

    Article  Google Scholar 

  29. Gane S, Georganakis D, Maniati K, Vamvakias M, Ragoussis N, Skoulakis EMC, Turin L (2013) Molecular vibration-sensing component in human olfaction. PLoS One 8:e55780

  30. Garamszegi LZ, Eens M, Erritzøe J, Møller AP (2005) Sexually size dimorphic brains and song complexity in passerine birds. Behav Ecol 16:335–345

    Article  Google Scholar 

  31. Goolsby EW (2016) Likelihood-based parameter estimation for high-dimensional phylogenetic comparative models: overcoming the limitations of “distance-based” methods. Syst Biol 65:852–870

    Article  PubMed  Google Scholar 

  32. Herrel A, Vanhooydonck B, Van Damme R (2004) Omnivory in lacertid lizards: adaptive evolution or constraint? J Evol Biol 17:974–984

  33. Hunt J, Snook RR, Mitchell C, Crudgington HS, Moore AJ (2012) Sexual selection and experimental evolution of chemical signals in Drosophila pseudoobscura. J Evol Biol 25:2232–2241

  34. 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:e19410

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Kopena R, López P, Martín J (2014) Relative contribution of dietary carotenoids and vitamin E to visual and chemical sexual signals of male Iberian green lizards: an experimental test. Behav Ecol Sociobiol 68:571–581

    Article  Google Scholar 

  36. Marconi S, Manzi P, Pizzoferrato L, Buscardo E, Cerda H, Hernandez DL, Paoletti MG (2002) Nutritional evaluation of terrestrial invertebrates as traditional food in Amazonia. Biotropica 34:273–280

    Article  Google Scholar 

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

    Article  Google Scholar 

  38. Martín J, López P (2010) 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

    Article  PubMed  Google Scholar 

  39. Martín J, Ortega J, López P (2015) Interpopulational variations in sexual chemical signals of Iberian wall lizards may allow maximizing signal efficiency under different climatic conditions. PLoS One 10:e0131492

    Article  PubMed  PubMed Central  Google Scholar 

  40. Martín J, López P, Garrido M, Pérez-Cembranos A, Pérez-Mellado V (2013) Inter-island variation in femoral secretions of the Balearic lizard, Podarcis lilfordi (Lacertidae). Biochem Syst Ecol 50:121–128

  41. Martín J, López P, Iraeta P, Díaz JA, Salvador A (2016) Differences in males’ chemical signals between genetic lineages of the lizard Psammodromus algirus promote male intrasexual recognition and aggression but not female mate preferences. Behav Ecol Sociobiol 70:1657–1668

    Article  Google Scholar 

  42. Mayerl C, Baeckens S, Van Damme R (2015) Evolution and role of the follicular epidermal gland system in non-ophidian squamates. Amphibia-Reptilia 36:185–206

    Article  Google Scholar 

  43. Maynard-Smith J, Harper D (2003) Animal signals. Oxford University Press, New York

    Google Scholar 

  44. Merkling T, Hamilton DG, Cser B, Svedin N, Pryke SR (2016) Proximate mechanisms of colour variation in the frillneck lizard: geographical differences in pigment contents of an ornament. Biol J Linn Soc 117:503–515

    Article  Google Scholar 

  45. Meyers JJ, Herrel A, Nishikawa KC (2006) Morphological correlates of ant eating in horned lizards (Phrynosoma). Biol J Linn Soc 89:13–24

    Article  Google Scholar 

  46. Ord TJ, Martins EP (2006) Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Anim Behav 71:1411–1429

    Article  Google Scholar 

  47. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2013) CAPER: comparative analyses of phylogenetics and evolution in R. R package version 052. Available at: http://R-Forge.R-project.org/projects/caper/. Accessed: June 2016

  48. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    CAS  Article  PubMed  Google Scholar 

  49. Pérez-Mellado V, Corti C (1993) Dietary adaptations and herbivory in lacertid lizards of the genus Podarcis from western Mediterranean islands (Reptilia: Sauria). Bonn Zool Beitr 44:193–220

    Google Scholar 

  50. Pérez-Cembranos A, León A, Pérez-Mellado V (2016) Omnivory of an insular lizard: sources of variation in the diet of Podarcis lilfordi (Squamata Lacertidae). PLoS One 11:e0148947

    Article  PubMed  PubMed Central  Google Scholar 

  51. Pureswaran DS, Hofstetter RW, Sullivan BT, Grady AM, Brownie C (2016) Western pine beetle populations in Arizona and California differ in the composition of their aggregation pheromones. J Chem Ecol 42:404–413

    CAS  Article  PubMed  Google Scholar 

  52. Redford KH, Dorea JG (1984) The nutritional value of invertebrates with emphasis on ants and termites as food for mammals. J Zool 203:385–395

  53. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  54. Revell LJ (2013) Two new graphical methods for mapping trait evolution on phylogenies. Methods Ecol Evol 4:754–759

    Article  Google Scholar 

  55. Rodríguez A, Nogales M, Rumeu B, Rodríguez B (2008) Temporal and spatial variation in the diet of the endemic lizard Gallotia galloti in an insular Mediterranean scrubland. J Herpetol 42:213–222

    Article  Google Scholar 

  56. Rollmann SM, Houck LD, Feldhoff RC (2000) Population variation in salamander courtship pheromones. J Chem Ecol 26:2713–2724

    CAS  Article  Google Scholar 

  57. Roughgarden J (1979) Theory of population genetics and evolutionary ecology: an introduction. Macmillan, New York

    Google Scholar 

  58. Rundle HD, Chenoweth SF, Doughty P, Blows MW (2005) Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol 3:1988–1995

    CAS  Article  Google Scholar 

  59. Saberi M, Seyed-allaei H (2016) Odorant receptors of Drosophila are sensitive to the molecular volume of odorants. Sci Rep 6:25103

  60. Santos JC, Coloma LA, Cannatella DC (2003) Multiple recurring origins of aposematism and diet specialization in poison frogs. Proc Natl Acad Sci U S A 100:12792–12797

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Scali S, Sacchi R, Mangiacotti M et al (2016) Does a polymorphic species have a “polymorphic” diet? A case study from a lacertid lizard. Biol J Linn Soc 117:492–502

    Article  Google Scholar 

  62. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423

    Article  Google Scholar 

  63. Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228

    Article  PubMed  Google Scholar 

  64. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones: an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29:481–514

    CAS  Article  PubMed  Google Scholar 

  65. Van Damme R (1999) Evolution of herbivory in lacertid lizards: effects of insularity and body size. J Herp 33:663–674

    Article  Google Scholar 

  66. Verwaijen D, Van Damme R, Herrel A (2002) Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct Ecol 16:842–850

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  68. Wyatt TD (2014) Pheromones and animal behaviour: chemical signals and signatures. Cambridge University Press, Cambridge

    Google Scholar 

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Acknowledgments

We thank Josie Meaney for linguistic advice, and three anonymous reviewers for significantly improving drafts of this manuscript. Financial support to JM and RGR was provided by the Spanish’s Ministerio de Economía y Competitividad projects MICIIN-CGL2011-24150/BOS and MINECO CGL2014-53523-P. This work was part of SB’s doctoral thesis at the University of Antwerp.

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Correspondence to Simon Baeckens.

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This work was conducted under permits for Croatia (UP/I-612-07/14-48/111 & UP/I-612-07/14-48/33), The Netherlands (FF/74A/2015/009), Israel (2014/40323), SA Free State Province (S54C-515022511060), SA Eastern Cape Province (CRO 45/15CR & 46/15CR), SA Western Cape Province (0056-AAA041-00093), SA Northern Cape Province (FAUNA 229/2015 & 230/2015) and SA Limpopo Province (0092-MKT001-00004), and was in accordance with University of Antwerp (Belgium) animal welfare standards and protocols (ECD 2014-32). Captures of lizards and sampling procedures were performed under different licenses for the Environmental Agencies of the different Regional Governments of Spain where lizards were studied. All Greek species were collected in accordance with the Hellenic National Legislation (Presidential Decree 67/81).

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Baeckens, S., García-Roa, R., Martín, J. et al. The Role of Diet in Shaping the Chemical Signal Design of Lacertid Lizards. J Chem Ecol 43, 902–910 (2017). https://doi.org/10.1007/s10886-017-0884-2

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Keywords

  • Chemical communication
  • Semiochemicals
  • Diet
  • Femoral gland secretions
  • Herbivory
  • Lacertidae
  • Lizards
  • Phylogenetic comparison