Tantalising tongues: male carpet pythons use chemoreception to differentiate among females
G. L. Bryant A C , P. W. Bateman A B and P. A. Fleming A
+ Author Affiliations
- Author Affiliations
A School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia.
B Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa.
C Corresponding author. Email: G.Bryant@murdoch.edu.au
Australian Journal of Zoology 59(1) 42-48 https://doi.org/10.1071/ZO11029
Submitted: 7 April 2011 Accepted: 30 May 2011 Published: 8 July 2011
Abstract
For animals sparsely distributed across a landscape, finding and identifying a receptive female during a short breeding period can be a challenge for males. Many snakes appear to rely on the production of sex-specific pheromones to synchronise the timing of reproductive behaviour. The rare Australian south-west carpet python (Morelia spilota imbricata) displays non-aggressive mating aggregations of up to six males around a receptive female, suggesting that males are responding to some chemical signal that enables multiple males simultaneously to identify and locate the female. We investigated chemoreceptive response (tongue-flicking) of 10 male pythons under laboratory conditions to 12 (randomly ordered) treatments each presented for three minutes. Cutaneous chemicals (dissolved in hexane solvent) were collected on cotton buds from the skin of six female pythons and male responses to these were compared with six control treatments. Male pythons produced a greater number of tongue flicks during the first minute of each trial, with fewer in minutes 2 and 3. Male chemoreceptive response in the third minute varied significantly between treatments and was only maintained for trials presenting cutaneous chemicals collected from the three relatively largest female pythons. This experiment suggests that male carpet pythons can use chemoreception to obtain information about their social environment, identifying pheromone cues from large, potentially fecund females. This ability would be adaptive for male mate-selection behaviour and is likely to also reduce costs of searching behaviour.
Additional keywords: mate searching, reproductive behaviour, snakes, tongue-flicking.
References
Bryant, G. L., Eden, P., de Tores, P. J., and Warren, K. S. (2010). Improved procedure for implanting radiotransmitters in the coelomic cavity of snakes. Australian Veterinary Journal 88, 443–448.| Improved procedure for implanting radiotransmitters in the coelomic cavity of snakes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbgs1WgtQ%3D%3D&md5=428887af5f1f50b8c55b0f37824a0f37CAS | 20958284PubMed |
Bryant, G. L., Dundas, S. J., and Fleming, P. A. (). Tree hollows are of conservation importance for a Near-Threatened python species. Journal of Zoology , .
Burger, J. (1989). Following of conspecific and avoidance of predator chemical cues by pine snakes (Pituophis melanoleucus). Journal of Chemical Ecology 15, 799–806.
| Following of conspecific and avoidance of predator chemical cues by pine snakes (Pituophis melanoleucus).Crossref | GoogleScholarGoogle Scholar |
Chiszar, D., Radcliffe, C., and Feiler, F. (1986). Trailing behavior in banded rock rattlesnakes (Crotalus lepidus klauberi) and prairie rattlesnakes (C. viridis viridis). Journal of Comparative Psychology 100, 368–371.
| Trailing behavior in banded rock rattlesnakes (Crotalus lepidus klauberi) and prairie rattlesnakes (C. viridis viridis).Crossref | GoogleScholarGoogle Scholar |
Clark, R. W. (2007). Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites. Behavioral Ecology 18, 487–490.
| Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites.Crossref | GoogleScholarGoogle Scholar |
Coupe, B. H. (2005). Mate-location behavior of timber (Crotalus horridus) and sidewinder (Crotalus cerastes) rattlesnakes. Ph.D. Thesis, Ohio State University, Ohio.
Downes, S. (1999). Prey odor influences retreat-site selection by naive broadheaded snakes (Hoplocephalus bungaroides). Journal of Herpetology 33, 156.
| Prey odor influences retreat-site selection by naive broadheaded snakes (Hoplocephalus bungaroides).Crossref | GoogleScholarGoogle Scholar |
Duvall, D., Schuett, G. W., and Arnold, S. J. (1993). Ecology and evolution of snake mating systems. In ‘Snakes: Ecology and Behavior’. (Eds R. A. Seigel and J. T. Collins.) pp. 165–200. (McGraw-Hill, Inc.: New York.)
Fitch, H. S. (1960). Autecology of the copperhead. University of Kansas Publications. Museum of Natural History 13, 85–288.
Ford, N. B. (1986). The role of pheromones trails in the sociobiology of snakes. In ‘Chemical Signals in Vertebrates. Vol. 4: Ecology, Evolution, and Comparative Biology.’ (Eds D. Duvall, D. Müller-Schwarze. and R. M. Silverstein.) pp. 261–278. (Plenum Press: New York.)
Greenbaum, E. (2004). The influence of prey-scent stimuli on predatory behavior of the North American copperhead Agkistrodon contortrix (Serpentes: Viperidae). Behavioral Ecology 15, 345–350.
| The influence of prey-scent stimuli on predatory behavior of the North American copperhead Agkistrodon contortrix (Serpentes: Viperidae).Crossref | GoogleScholarGoogle Scholar |
Heller, S., and Halpern, M. (1981). Laboratory observations on conspecific and congeneric scent trailing in garter snakes (Thamnophis). Behavioral and Neural Biology 33, 372–377.
| Laboratory observations on conspecific and congeneric scent trailing in garter snakes (Thamnophis).Crossref | GoogleScholarGoogle Scholar |
Kardong, K. V., and Smith, T. L. (2002). Proximate factors involved in rattlesnake predatory behavior: a review. In ‘Biology of the Vipers’. (Eds G. W. Schuett, M. Hoggren, M. E. Douglas and H. W. Greene.) pp. 253–266. (Eagle Mountain Publishing: Utah.)
Karlson, P., and Luscher, M. (1959). ‘Pheromones’: a new term for a class of biologically active substances. Nature 183, 55–56.
| ‘Pheromones’: a new term for a class of biologically active substances.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1M%2Flt1agsQ%3D%3D&md5=7aaf7aac50eca63398acef69d752674aCAS | 13622694PubMed |
King, R. B., and Turmo, J. R. (1997). The effects of ecdysis on feeding frequency and behavior of the common garter snake (Thamnophis sirtalis). Journal of Herpetology 31, 310–312.
| The effects of ecdysis on feeding frequency and behavior of the common garter snake (Thamnophis sirtalis).Crossref | GoogleScholarGoogle Scholar |
Le Master, M. P., and Mason, R. T. (2001). Evidence for a female sex pheromone mediating male trailing behavior in the red-sided garter snake, Thamnophis sirtalis parietalis. Chemoecology 11, 149–152.
| Evidence for a female sex pheromone mediating male trailing behavior in the red-sided garter snake, Thamnophis sirtalis parietalis.Crossref | GoogleScholarGoogle Scholar |
Le Master, M. P., and Mason, R. T. (2002). Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. Journal of Chemical Ecology 28, 1269–1285.
| Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvFWjsrg%3D&md5=b78788e9b1064f70b388299863009308CAS | 12184402PubMed |
Le Master, M. P., Moore, I. T., and Mason, R. T. (2001). Conspecific trailing behaviour of red-sided garter snakes, Thamnophis sirtalis parietalis, in the natural environment. Animal Behaviour 61, 827–833.
| Conspecific trailing behaviour of red-sided garter snakes, Thamnophis sirtalis parietalis, in the natural environment.Crossref | GoogleScholarGoogle Scholar |
Madsen, T., and Shine, R. (2002). Short and chubby or long and slim? Food intake, growth and body condition in free-ranging pythons. Austral Ecology 27, 672–680.
| Short and chubby or long and slim? Food intake, growth and body condition in free-ranging pythons.Crossref | GoogleScholarGoogle Scholar |
Mason, R. T. (1992). Reptilian pheromones. In ‘Biology of the Reptilia. Vol. 18. Hormones, Brains and Behavior’. (Eds C. Gans and D. Crews.) pp. 114–228. (University of Chicago Press: Chicago.)
Mason, R.T., Jones, T. H., Fales, H. M., Pannell, L. K., and Crews, D. (1990). Characterization, synthesis, and behavioral responses to sex attractiveness pheromones of red-sided garter snakes (Thamnophis sirtalis parietalis). Journal of Chemical Ecology 16, 2353–2369.
| Characterization, synthesis, and behavioral responses to sex attractiveness pheromones of red-sided garter snakes (Thamnophis sirtalis parietalis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVymur0%3D&md5=ad15bf51ebc5b461b4f9d355276edc02CAS |
Pearson, D. (2002). The ecology and conservation of the south-western Australian carpet python, Morelia spilota imbricata. Ph.D. Thesis Thesis, University of Sydney.
Pearson, D., Shine, R., and Williams, A. (2002). Geographic variation in sexual size dimorphism within a single snake species (Morelia spilota, Pythonidae). Oecologia 131, 418–426.
| Geographic variation in sexual size dimorphism within a single snake species (Morelia spilota, Pythonidae).Crossref | GoogleScholarGoogle Scholar |
Pernetta, A. P., Reading, C. J., and Allen, J. A. (2009). Chemoreception and kin discrimination by neonate smooth snakes, Coronella austriaca. Animal Behaviour 77, 363–368.
| Chemoreception and kin discrimination by neonate smooth snakes, Coronella austriaca.Crossref | GoogleScholarGoogle Scholar |
Rivas, J. A., and Burghardt, G. M. (2001). Understanding sexual size dimorphism in snakes: wearing the snake’s shoes. Animal Behaviour 62, F1–F6.
| Understanding sexual size dimorphism in snakes: wearing the snake’s shoes.Crossref | GoogleScholarGoogle Scholar |
Schwenk, K. (1995). Of tongues and noses: chemoreception in lizards and snakes. Trends in Ecology Evolution 10, 7–12.
| Of tongues and noses: chemoreception in lizards and snakes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFWlsQ%3D%3D&md5=9796b8ff262123b2a1b7394f29f44b97CAS | 21236937PubMed |
Seigel, R. A., and Ford, N. B. (1987). Reproductive ecology. In ‘Snakes: Ecology and Evolutionary Biology’. (Eds R. A. Seigel, J. T. Collins and S. S. Novak.) pp. 210–253. (McGraw-Hill, Inc.: New York.)
Shine, R. (2005). Life-history evolution in reptiles. Annual Review of Ecology, Evolution and Systematics 36, 23–46.
| Life-history evolution in reptiles.Crossref | GoogleScholarGoogle Scholar |
Shine, R., and Fitzgerald, M. (1995). Variation in mating systems and sexual size dimorphism between populations of the Australian python Morelia spilota (Serpentes: Pythonidae). Oceologia 103, 490–498.
| Variation in mating systems and sexual size dimorphism between populations of the Australian python Morelia spilota (Serpentes: Pythonidae).Crossref | GoogleScholarGoogle Scholar |
Shine, R., O’Connor, D., and Mason, R. T. (2000). Female mimicry in garter snakes: behavioural tactics of “she-males” and the males that court them. Canadian Journal of Zoology 78, 1391–1396.
| Female mimicry in garter snakes: behavioural tactics of “she-males” and the males that court them.Crossref | GoogleScholarGoogle Scholar |
Shine, R., Phillips, B., Waye, H., LeMaster, M. P., and Mason, R. T. (2003). The lexicon of love: what cues cause size-assortative courtship by male garter snakes? Behavioral Ecology and Sociobiology 53, 234–237.
| The lexicon of love: what cues cause size-assortative courtship by male garter snakes?Crossref | GoogleScholarGoogle Scholar |
Shine, R., O’Donnell, R. P., Langkilde, T., Wall, M. D., and Mason, R. T. (2005a). Snakes in search of sex: the relation between mate-locating ability and mating success in male garter snakes. Animal Behaviour 69, 1251–1258.
| Snakes in search of sex: the relation between mate-locating ability and mating success in male garter snakes.Crossref | GoogleScholarGoogle Scholar |
Shine, R., Webb, J. K., Lane, A., and Mason, R. T. (2005b). Mate location tactics in garter snakes: effects of rival males, interrupted trails and non-pheromonal cues. Functional Ecology 19, 1017–1024.
| Mate location tactics in garter snakes: effects of rival males, interrupted trails and non-pheromonal cues.Crossref | GoogleScholarGoogle Scholar |
Smith, C. F., Schwenk, K., Earley, R. L., and Schuett, G. W. (2008). Sexual size dimorphism of the tongue in a North American pitviper. Journal of Zoology 274, 367–374.
| Sexual size dimorphism of the tongue in a North American pitviper.Crossref | GoogleScholarGoogle Scholar |
Stark, P.C., Chiszar, D., Stiles, K. E., and Smith, H. M. (2002). A laboratory situation for studying the effects of chemical and visual cues on prey trailing in brown treesnakes (Boiga irrgularis). Journal of Herpetology 36, 57.
Webb, J. K., and Shine, R. (1992). To find an ant: trail-following in Australian blindsnakes (Typhlopidae). Animal Behaviour 43, 941–948.
| To find an ant: trail-following in Australian blindsnakes (Typhlopidae).Crossref | GoogleScholarGoogle Scholar |
