Abstract
Although chemical interactions play an essential role in lizard social behavior, the chemical composition of the femoral gland secretions that many lizards use for communication is known for only a few species, mainly European Lacertids. The tegu lizard, Salvator merianae, is the only species of the Teiidae family for which there is available information on lipids in femoral secretions, but only for captive bred males from Argentina. Here, based on mass spectra obtained by GC-MS, we found 69 lipophilic compounds in femoral gland secretions of wild males S. merianae from Brazil, including cholesterol and high amounts of saturated fatty acids (mainly hexadecanoic and octadecanoic). We found contrasting differences between wild and captive-bred males, which lack cholesterol but present high amount of 9,12-octadecadienoic acid. These within-species differences between wild and captive lizards strongly suggest the important influence of different diets on the chemical composition of the femoral gland secretion and suggest caution when interpreting results from captive animals, even in the same species.
Funding source: Fundação de Amparo à Pesquisa do Estado de São Paulo
Award Identifier / Grant number: FAPESP 2015/12841-5
Funding source: Ministerio de Economía y Competitividad Project
Award Identifier / Grant number: MINECO CGL2014-53523-P
Funding source: Ministerio de Ciencia, Innovación y Universidades Project
Award Identifier / Grant number: PGC2018-093592-B-I00
Acknowledgments
We thank two anonymous reviewers for helpful comments. Financial support was provided by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2015/12841-5) and by the Ministerio de Economía y Competitividad Project MINECO CGL2014-53523-P and Ministerio de Ciencia, Innovación y Universidades Project PGC2018-093592-B-I00 (MCIU/AEI/FEDER, EU) to J. Martín.
Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: Financial support was provided by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2015/12841-5) and by the Ministerio de Economía y Competitividad Project MINECO CGL2014-53523-P and Ministerio de Ciencia, Innovación y Universidades Project PGC2018-093592-B-I00 (MCIU/AEI/FEDER).
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
1. Wyatt, TD. Pheromones and animal behavior: chemical signals and signature mixtures, 2nd ed. Cambridge: Cambridge University Press; 2014.10.1017/CBO9781139030748Search in Google Scholar
2. Mason, RT. Reptile pheromones. In: Gans, C, Crews, D, editors. Biology of the Reptilia. Chicago: University of Chicago Press; 1992, vol. 18.Search in Google Scholar
3. Cole, CJ. Femoral glands in lizards: a review. Herpetologica 1966;22:199–206.Search in Google Scholar
4. Aragón, P, López, P, Martín, J. Discrimination of femoral gland secretions from familiar and unfamiliar conspecifics by male Iberian rock-lizards, Lacerta monticola. J Herp 2001;35:346–50. http://doi.org/10.2307/1566131.10.2307/1566131Search in Google Scholar
5. Carazo, P, Font, E, Desfilis, E. Beyond “nasty neighbors” and “dear enemies”? Individual recognition by scent marks in a lizard (Podarcis hispanica). Anim Behav 2008;76:1953–63. https://doi.org/10.1016/j.anbehav.2008.08.018.Search in Google Scholar
6. Martín, J, Amo, L, López, P. Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis. Naturwissenschaften 2008;95:293–300. https://doi.org/10.1007/s00114-007-0328-x.Search in Google Scholar
7. Khannoon, ER, El-Gendy, A, Hardege, JD. Scent marking pheromones in lizards: cholesterol and long chain alcohols elicit avoidance and aggression in male Acanthodactylus boskianus. Chemoecology 2011;21:143–9. https://doi.org/10.1007/s00049-011-0076-4.Search in Google Scholar
8. Nisa, C, Rodríguez-Ruis, G, López, P, da Silva Junior, PI, Rodrigues, MT, Martín, J. Chemosensory discrimination of male age by female Psammodromus algirus lizards base don femoral secretions and feces. Ethology 2019;125;802–09. https://doi.org/10.1111/eth.12934.Search in Google Scholar
9. Martín, J, López, P. Scent may signal fighting ability in male Iberian rock lizards. Biol Lett 2007;3:125–27. https://dx.doi.org/10.1098/rsbl.2006.0589.10.1098/rsbl.2006.0589Search in Google Scholar PubMed PubMed Central
10. Weldon, PJ, Flachsbarth, B, Schulz, S. Natural products from the integument of nonavian reptiles. Nat Prod Rep 2008;25:738–56. http://doi.org/10.1039/B509854H.10.1039/b509854hSearch in Google Scholar PubMed
11. Baeckens, S, García-Roa, R, Martín, J, Van Damme, R. The role of diet in shaping the chemical signal design of lacertid lizards. J Chem Ecol 2017;43:902–10. https://doi.org/10.1007/s10886-017-0884-2.Search in Google Scholar
12. García-Roa, R, Sáiz, J, Gómara, B, López, P, Martín, J. Dietary constraints can preclude the expression of an honest chemical sexual signal. Sci Rep 2017;7:6073. https://doi.org/10.1038/s41598-017-06323-8.Search in Google Scholar
13. Martín, J, Ortega, J, López, P. Interpopulational variations in sexual chemical signals of Iberian wall lizards may allow maximizing signal efficiency under different climatic conditions. Plos One 2015;10:e0131492. http://doi.org/0.1371/journal.pone.0131492.10.1371/journal.pone.0131492Search in Google Scholar PubMed PubMed Central
14. Baeckens, S, Martín, J, García-Roa, R, Pafilis, P, Huyghe, K, Van Damme, R. Environmental conditions shape the chemical signal design of lizards. Funct Ecol 2018;32:566–80. https://doi.org/10.1111/1365-2435.12984.Search in Google Scholar
15. Zozaya, SM, Higgie, M, Moritz, C, Hoskin, CJ. Are pheromones key to unlocking cryptic lizard diversity? Am Nat 2019;194:68–182. https://doi.org/10.1086/704059.Search in Google Scholar
16. Escobar, CA, Labra, A, Niemeyer, HM. Chemical composition of precloacal secretions of Liolaemus lizards. J Chem Ecol 2001;27:1677–90. https://doi.org/10.1023/a:1010470611061.10.1023/A:1010470611061Search in Google Scholar
17. Escobar, CM, Escobar, CA, Labra, A, Niemeyer, HM. Chemical composition of precloacal secretions of two Liolaemus fabiani populations: are they diferente? J Chem Ecol 2003;29:629–38. https://doi.org/10.1023/a:1022858919037.10.1023/A:1022858919037Search in Google Scholar
18. García-Roa, R, Ferreira, S, López, P, Martín, J. Genders matters: sexual differences in chemical signals of Liolaemus wiegmannii lizards (Iguania, Liolaemidae). Biochem Syst Ecol 2016;69:108–14. https://doi.org/10.1016/j.bse.2016.08.011.Search in Google Scholar
19. Martín, J, Chamut, S, Manes, ME, López, P. Chemical constituents of femoral gland secretions of male Tegu lizards (Tupinambis merianae) (Family Teiidae). Z Naturforsch 2011;66c;434–40. https://doi.org/10.1515/znc-2011-7-817.Search in Google Scholar
20. Ávila-Pires, TCS. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zool Verh 1995;299:1–706.Search in Google Scholar
21. Abe, AS. Observations on dormancy in tegu lizard, Tupinambis teguixin (Reptilia, Teiidae). Naturalia 1983;8:135–39.Search in Google Scholar
22. Harvey, MB, Ugueto, GN, GutberletJr.RL. Review of Teiid morphology with a revised taxonomy and phylogeny of the Teiidae (Lepidosauria: Squamata). Zootaxa 2012;345:1–156.10.7934/P759Search in Google Scholar
23. Chamut, S, Valdez, VG, Manes, ME. Functional morphology of femoral glands in the tegu lizard, Tupinambis merianae. Zool Sci 2009;26:289–93. https://doi.org/10.2108/zsj.26.289.Search in Google Scholar
24. Sazima, I. Corpse bride irresistible: a dead female tegu lizard (Salvator merianae) courted by males for two days at an urban park in South-eastern Brazil. Herpetol 2015;8:15–18.Search in Google Scholar
25. Lopes, HR, Abe, AS. Biologia reprodutiva e comportamento do teiu, Tupinambis teguixin, em cativeiro (Reptilia, Teiidae). In: Fang, TG, Montenegro, OL, Bodmer, RE, editors. Manejo y conservación de fauna silvestre en América Latina. La Paz, 1999.Search in Google Scholar
26. Naretto, S, Cardozo, G, Blengini, CS, Chiaraviglio, M. Importance of reproductive biology of a harvest lizard, Tupinmabis merianae, for the management of commercial harvesting. Wildlife Res 2015;42:697–704. https://doi.org/10.1071/WR15056.Search in Google Scholar
27. MeshakaJr.WE, Mazzotti, FJ, Rochford, MR. Ecologia plasticity and the future of the Argentine giant Tegu (Salvator merianae Dumeril and Bibron, 1839) in the Southeastern US. Southeast Nat 2019;18:659–76. https://doi.org/10.1656/058.018.0417.Search in Google Scholar
28. García-Roa, R, Sáiz, J, Gómara, B, López, P, Martín, J. How to tackle chemical communication? Relative proportions versus. semi-quantitative determination of compounds in lizard chemical secretions. Ecol Evol 2018;8:2032–40. https://doi.org/10.1002/ece3.3825.Search in Google Scholar
29. López, P, Martín, J. Age-related differences in lipophilic compounds found in femoral gland secretions of male spiny-footed lizards, Acanthodactylus erythrurus. Z Naturforsch C 2005;60c:915–20. https://doi.org/10.1515/znc-2005-11-1215.Search in Google Scholar
30. López, P, Martín, J. Fighting rules and rival recognition reduce costs of aggression in male lizards, Podarcis hispanica. Behav Ecol Sociobiol 2001;49:111–16. https://doi.org/10.1007/s002650000288.Search in Google Scholar
31. Apps, PJ, Weldon, PJ, Kramer, M. Chemical signals in terrestrial vertebrates: search for design features. Nat Prod Rep 2015;32:1131–53. http://doi.org/10.1039/C5NP00029G.10.1039/C5NP00029GSearch in Google Scholar
32. Alberts, AC, Sharp, TR, Werner, DI, Weldon, P. Seasonal variation of lipids in femoral gland secretion of male green iguanas, Iguana iguana. J Chem Ecol 1992;18:703–12. https://doi.org/10.1007/bf00994608.Search in Google Scholar
33. Alberts, AC, Pratt, NC, Phillips, JA. Seasonal productivity of lizard femoral glands: relationship to social dominance and androgen levels. Physiol Behav 1992;51:729–33. https://doi.org/10.1016/0031-9384(92)90109-F.Search in Google Scholar
34. Henneken, J, Goodger, JOD, Jones, TM, Elgar, MA. Diet-mediated pheromones and signature mixtures can enforce signal reliability. Frontiers Ecol Evol 2017;4:145. https://doi.org/10.3389/fevo.2016.00145.Search in Google Scholar
35. Martín, J, López, P. Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc London Ser B 2006;273:2619–24. https://doi.org/10.1098/rspb.2006.3619.Search in Google Scholar
36. Martín, J, López, P. Condition-dependent pheromone signaling by male rock lizards: more oily scents are more attractive. Chem Sens 2010;35:253–62. https://doi.org/10.1093/chemse/bjq009.Search in Google Scholar
37. Kopena, R, Martín, J, López, P, Herczeg, G. Vitamin E supplementation increases the attractiveness of males’ scent for female European green lizards. Plos One 2011;6:e19410. https://doi.org/10.1371/journal.pone.0019410.Search in Google Scholar
38. Kopena, R, López, P, Martín, J. 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 2016;68:571–81, https://doi.org/10.1007/s00265-013-1672-9.Search in Google Scholar
39. Vanzolini, P, Ramos-Costa, AMM, Vitt, LJ. Répteis da Caatinga, 1st ed. Rio de Janeiro: Academia Brasileira de Ciências; 1980.10.5962/bhl.title.109659Search in Google Scholar
40. Williams, JD, Donadío, OE, Ré, I. Notas relativas a la dieta de Tupinambis ruscens (Reptilia: Sauria) del noroeste argentino. Neotrópica 1993;39:41–51.Search in Google Scholar
41. Vega Parry, HE, Manes, ME. Alimentación de lagartos overos Tupinambis merianae com subproductos avícolas. Rev Argentina Prod Anim 2000;20:135–43.Search in Google Scholar
42. Brigelius-Flohe, R, Traber, MG. Vitamin E: function and metabolism. FASEB J 1999;13:1145–55. https://doi.org/10.1096/fasebj.13.10.1145.Search in Google Scholar
43. Gabirot, M, López, P, Martín, J, de Fraipont, M, Heulin, B, Sinervo, B, et al. Chemical composition of femoral secretions of oviparous and viviparous types of male common lizards Lacerta vivipara. Biochem Syst Ecol 2008;36:539–44. https://doi.org/10.1016/j.bse.2008.03.006.Search in Google Scholar
44. Martín, J, Civantos, E, Amo, L, López, P. Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behav Ecol Sociobiol 2007;62:173–79. https://doi.org/10.1007/s00265-007-0451-x.Search in Google Scholar
45. Martín, J, Moreira, PL, López, P. Status-signalling badges in male Iberian rock lizards. Funct Ecol 2007;21:568–76. https://doi.org/10.1111/j.1365-2435.2007.01262.x.Search in Google Scholar
46. Burr, GO, Burr, MM, Miller, E. On the nature of the fatty acids essential in nutrition. J Biol Chem 1930;86:587–621.10.1016/S0021-9258(20)78929-5Search in Google Scholar
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