Testing the functionality of precloacal secretions from both sexes in the South American lizard, Liolaemus chiliensis

in Amphibia-Reptilia
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

The behavior of lizards can be highly influenced by chemical senses. The most studied pheromonal sources in lizards has been the femoral and precloacal gland secretions, although studies have been focused on male secretions, probably because these glands are usually only present in males or are poorly developed in females when they are present. Here, we aimed to study in Liolaemus chiliensis, one of the few Liolaemus species in which females have precloacal glands, if female precloacal secretions convey information. We recorded the response of both sexes to secretions from females and males, as well as to control (solvent). The lizards started to explore the secretions sooner than the control. Both sexes moved more when exposed to female secretions than to the control, and males, but not females, explored female secretions more than the other scents. These results suggest that volatile compounds of the secretions allow lizards to recognize the presence of conspecifics, and, at least for males, these trigger the exploration of non-volatile compounds of the secretions that may reveal the sex of the individual that deposited them. This is the first study that explores the response to female precloacal secretions in Liolaemus, and data indicate that the female secretions of L. chiliensis contain relevant information for social interactions.

Amphibia-Reptilia

Publication of the Societas Europaea Herpetologica

Sections

References

AbdalaC.S. (2007): Phylogeny of the boulengeri group (Iguania: Liolaemidae, Liolaemus) based on morphological and molecular characters. Zootaxa 1538: 1-84.

AlbertsA.C. (1990): Chemical properties of femoral gland secretions in the desert iguana, Dipsosaurus dorsalis. J. Chem. Ecol. 16: 13-25.

AlbertsA.C.WernerD.I. (1993): Chemical recognition of unfamiliar conspecifics by green iguanas: functional significance of different signals components. Anim. Behav. 46: 197-199.

AparicioJ.OcampoM. (2010): Liolaemus group montanus Etheridge, 1995 (Iguania-Liolaemidae). Cuad. Herpetol. 24: 133-135.

BaeckensS.EdwardsS.HuygheK.Van DammeR. (2015): Chemical signalling in lizards: an interspecific comparison of femoral pore numbers in Lacertidae. Biol. J. Linn. Soc. 114: 44-57.

BaeckensS.HuygheK.PalmeR.Van DammeR. (2017): Chemical communication in the lacertid lizard Podarcis muralis: the functional significance of testosterone. Acta Zool. 98: 94-103.

BairdT.A.McGeeA.A.YorkJ.R. (2015): Responses to femoral gland secretions by visually adept male and female collared lizards. Ethology 121: 513-519.

BozzoV. (2014): Interacciones sociales en el lagarto llorón (Liolaemus chiliensis). Thesis for the Degree of Veterinarian Physician. Facultad de Ciencias Silvoagropecuarias, Escuela Medicina Veterinaria, p. 35. Universidad Mayor, Santiago.

BreitmanM.F.MorandoM.AvilaL.J. (2013): Past and present taxonomy of the Liolaemus lineomaculatus section (Liolaemidae): is the morphological arrangement hypothesis valid? Zootaxa 168: 612-668.

CabreraA.L. (1994): Regiones Fitogeográficas Argentinas. Acme S.A.C.I., Buenos Aires.

CarazoP.FontE.DesfilisE. (2008): Beyond ‘nasty neighbours’ and ‘dear enemies’? Individual recognition by scent marks in a lizard (Podarcis hispanica). Anim. Behav. 76: 1953-1963.

CeiJ.M. (1986): Reptiles del Centro, Centro-Oeste y Sur de la Argentina. Herpetofauna de las Zonas Aridas y Semiaridas. Turin, Museo Regionale di Scienze Naturali Monografie.

CeiJ.M. (1993): Reptiles del Noroeste, Nordeste y Este de la Argentina. Herpetofauna de las Selvas Subtropicales, Puna y Pampa. Turin, Museo Regionale di Scienze Naturali Monografie.

ColeC.J. (1966): Femoral glands of the lizard, Crotaphytus collaris. J. Morph. 118: 119-135.

CooperW.E.J. (1998): Evaluation of swab and related tests as a bioassay for assessing responses by Squamate reptiles to chemical stimuli. J. Chem. Ecol. 24: 841-866.

CooperW.E.J.LópezP.SalvadorA. (1994): Pheromones detection in amphisbaenian. Anim. Behav. 47: 1401-1411.

CowlesR.B.PhelanR.L. (1958): Olfaction in rattlesnakes. Copeia 1958: 77-83.

Donoso BarrosR. (1966): Reptiles de Chile. Universidad de Chile, Santiago.

EscobarC.A.LabraA.NiemeyerH.M. (2001): Chemical composition of precloacal secretions of Liolaemus lizards. J. Chem. Ecol. 27: 1677-1690.

EscobarC.M.EscobarC.A.LabraA.NiemeyerH.M. (2003): Chemical composition of precloacal secretions of two Liolaemus fabiani populations: are they different? J. Chem. Ecol. 29: 629-638.

EtheridgeR. (1993): Lizards of the Liolaemus darwinii complex (Squamata: Iguania: Tropiduridae) in northern Argentina. Mus. Reg. Sci. Nat. Bull. 11: 137-199.

EtheridgeR. (1995): Redescription of Ctenoblepharys adspersa Tschudi, 1845, and the taxonomy of Liolaeminae (Reptilia: Squamata: Tropiduridae). Am. Mus. Novit. 3142: 1-34.

FrostD.R.EtheridgeR. (1989): A phylogenetic analysis and taxonomy of iguanian lizards (Reptilia: Squamata). U. Kansas Mus. Nat. Hist. Mis. Publ. 81: 1-65.

García-RoaR.CarreiraS.LópezP.MartínJ. (2016): Genders matters: sexual differences in chemical signals of Liolaemus wiegmannii lizards (Iguania, Liolaemidae). Biochem. Syst. Ecol. 69: 108-114.

ImparatoB.A.AntoniazziM.M.RodriguesM.T.JaredC. (2007): Morphology of the femoral glands in the lizard Ameiva ameiva (Teiidae) and their possible role in semiochemical dispersion. J. Morph. 268: 636-648.

KhannoonE.BreithauptT.El-GendyA.HardegeJ.D. (2010): Sexual differences in behavioural response to femoral gland pheromones of Acanthodactylus boskianus. Herpetol. J. 20: 225-229.

KhannoonE.R.R.DollahonN.R.BauerA.M. (2013): Comparative study of the pheromone-manufacturing femoral glands in two sympatric species of lacertid lizards (Acanthodactylus). Zool. Sci. 30: 110-117.

LabraA. (2006): Chemoreception and the assessment of fighting abilities in the lizard Liolaemus monticola. Ethology 112: 993-999.

LabraA. (2008): Multi-contextual use of chemosignals by Liolaemus lizards. In: Chemical Signals in Vertebrates 11, p.  357-365. HurstJ.BeynonR.RobertsS.WyattT., Eds, Springer, New York.

LabraA. (2011): Chemical stimuli and species recognition in Liolaemus lizards. J. Zool. 285: 215-221.

LabraA.NiemeyerH.M. (1999): Intraspecific chemical recognition in the lizard Liolaemus tenuis. J. Chem. Ecol. 25: 1799-1811.

LabraA.HoareM. (2014): Chemical recognition in a snake-lizard predator-prey system. Acta. Ethol. 18: 173-179.

LabraA.BeltránS.NiemeyerH.M. (2001): Chemical exploratory behavior in the lizard Liolaemus bellii. J. Herpetol. 35: 51-55.

LabraA.BrannJ.H.FadoolD.A. (2005): Heterogeneity of voltage- and chemosignal-activated response profiles in vomeronasal sensory neurons. J. Neurophysiol. 94: 2535-2548.

LabraA.PienaarJ.HansenT.F. (2009): Evolution of thermal physiology in Liolaemus lizards: adaptation, phylogenetic inertia, and niche tracking. Am. Nat. 174: 204-220.

LabraA.Reyes-OlivaresC.WeymannM. (2016): Asymmetric response to heterotypic distress calls in the lizard Liolaemus chiliensis. Ethology 122: 758-768.

LabraA.EscobarC.A.AguilarM.P.NiemeyerH.M. (2002): Sources of pheromones in the lizard Liolaemus tenuis. Rev. Chil. Hist. Nat. 75: 141-147.

LaurentR.F. (1986): Description of new Iguanidae of the genus Liolaemus. Acta Zool. Lilloana 38: 87-106.

LoboF. (2001): A phylogenetic analysis of lizards of the Liolaemus chiliensis group (Iguania: Tropiduridae). Herpetol. J. 11: 137-150.

LoboF.LaurentR.F. (1995): Un nouveau Liolaemus Andin (Tropiduridae). Rev. Fr. d’Aquariol.-Herpetol. 22: 107-116.

LópezP.AragónP.MartínJ. (2003): Responses of female lizards, Lacerta monticola, to males’ chemical cues reflect their mating preference for older males. Behav. Ecol. Sociobiol. 55: 73-79.

LouwS.BurgerB.V.Le RouxM.Van WykJ.H. (2007): Lizard epidermal gland secretions I: chemical characterization of the femoral gland secretion of the sungazer, Cordylus giganteus. J. Chem. Ecol. 33: 1806-1818.

MartínJ.LópezP. (2000): Chemoreception, symmetry and mate choice in lizards. Proc. R. Soc. Lond. B 267: 1265-1269.

MartínJ.LópezP. (2006): Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Funct. Ecol. 20: 1087-1096.

MartínJ.LópezP. (2013): Responses of female rock lizards to multiple scent marks of males: effects of male age, male density and scent over-marking. Behav. Process. 94: 109-114.

MartínJ.LópezP. (2014): Pheromones and chemical communication in lizards. In: Reproductive Biology and Phylogeny of Lizards and Tuatara, p.  43-77. RheubertustinJ.SiegelD.TrauthS., Eds, CRC Press, Boca Raton.

MartínJ.Martínez-SilvestreA.LópezP.IbáñezA.Rodríguez-DomínguezM.A.VerdaguerI. (2015): Lipophilic compounds in femoral secretions of males and females of the El Hierro giant lizard Gallotia simonyi (Lacertidae). Biochem. Syst. Ecol. 61: 286-292.

Martínez OliverI.LoboF. (2002): Una nueva especie de Liolaemus del grupo alticolor (Iguania: Liolaemidae) de la Puna salteña, Argentina. Cuad. Herpetol. 16: 47-64.

MayerlC.BaeckensS.Van DammeR. (2015): Evolution and role of the follicular epidermal gland system in non-ophidian squamates. Amphibia-Reptilia 36: 185-206.

MellaJ.E. (2005): Guía de Campo Reptiles de Chile: Zona Central. Centro de Ecología Aplicada Ltda, Santiago.

MoreiraP.L.LópezP.MartínJ. (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: 166-174.

Pincheira-DonosoD.HodgsonD.J.TregenzaT. (2008): Comparative evidence for strong phylogenetic inertia in precloacal signalling glands in a species-rich lizard clade. Evol. Ecol. Res. 10: 11-28.

UetzP.HošekJ. (2017): The reptile database. http://www.reptile-database.org.

ValdecantosS.MartínezV.LabraA. (2014): Comparative morphology of Liolaemus lizards precloacal glands. Acta Herpetol. 9: 147-158.

VicenteN.S.HalloyM. (2016): Chemical recognition of conspecifics in a Neotropical lizard, Liolaemus pacha (Iguania: Liolaemidae): relation to visual displays, season and sex. J. Ethol. 34: 329-335.

WyattT.D. (2014): Pheromones and Animal Behavior. Chemical Signals and Signature Mixes. Cambridge University Press, New York.

Figures

  • Ventral view of the cloacal area of an adult male (A) and a female (B) of Liolaemus chiliensis showing the precloacal pores (black arrow) with secretions. Note in (A) the thickening at the tail base where hemipenes are located. Pictures were taken in alive individuals in the lab.

    View in gallery
  • Mean (+SE) of three behaviors recorded in Liolaemus chiliensis, in three experimental conditions: precloacal secretions of males, females and a control. (A) Latency to the first tongue flick. (B) Number of tongue flicks to the stone. (C) Time in movement, standardized by the total time of the trial.

    View in gallery

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 8 8 2
Full Text Views 4 4 3
PDF Downloads 2 2 1
EPUB Downloads 0 0 0