Many snakes are able to use their chemosensory system to detect scent of conspecifics, which is important in many social contexts. Age discrimination based on chemical cues may be especially important to ensure access to sexually mature potential partners. In this study, we used 24 individual Boa constrictor snakes (12 adults mature and 12 non-mature individuals) that had been captured in different areas of Ecuador, and were maintained in captivity at the Vivarium of Quito. We used tongue-flick experiments to examine whether these snakes were able to discriminate between scents from mature and non-mature individuals. Results showed that B. constrictor snakes used chemical cues to recognize conspecifics and that the scent of individuals of different ages elicited chemosensory responses of different magnitudes. The scents from adult conspecifics elicited the quickest and highest chemosensory responses (i.e., short latency times and high tongue-flick rates), although we did not find differential responses to scent of males and females. The magnitude of the responses was lower to scent of sub adult individuals, and then even lower to scent of juvenile snakes, but in all cases the scent of snakes was discriminated from a blank control. We discuss the potential chemical mechanisms that may allow age recognition and its implications for social and sexual behavior of this snake species.
Key words: age recognition, Boa constrictor, chemoreception, Ecuador, snakes.
Resumen
Muchas serpientes son capaces de usar su sistema quimiosensorial para detectar el olor de individuos coespecíficos, lo que es importante en muchos contextos sociales. La discriminación de la edad basada en señales químicas puede ser especialmente importante para asegurar el acceso a parejas potenciales que sean sexualmente maduras. En este estudio, usamos 24 individuos de una especie de boa (Boa constrictor) (12 individuos adultos y 12 inmaduros) que habían sido capturados en diferentes partes de Ecuador y eran mantenidos en cautividad el Vivarium de Quito. Usamos experimentos de protusiones linguales para examinar si esta serpiente es capaz de discriminar entre el olor de individuos maduros y no maduros. Los resultados mostraron que B. constrictor usa señales químicas para reconocer co-específicos y que el olor de individuos de distinta edad provoca respuestas quimiosensoriales de diferente magnitud. El olor de individuos adultos provocó las respuestas más rápidas y elevadas (esto es, tiempos de latencia más cortos y tasas más altas de protusiones linguales), aunque no encontramos diferencias en las respuestas a olores de machos y hembras. La magnitud de las respuestas fue más baja a olores de sub adultos, e incluso más baja a olor de juveniles, pero en todos los casos el olor de una serpiente era discriminado de un control no oloroso. Discutimos los posibles mecanismos químicos que pueden permitir esta discriminación de la edad y sus implicaciones para el comportamiento social y sexual de esta serpiente.
Palabras clave:Boa constrictor, Ecuador, quimio recepción, reconocimiento de la edad, serpientes.
Most snakes have the chemosensory ability to discriminate substrate deposited scent trails of ]]>
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Among the many potential chemosensory abilities, age discrimination based on chemical cues may be determinant in several circumstances. For example during the mating season; to ensure access to potential partners, animals should be able to discriminate sexually mature from non mature individuals (O’Donnell et al. 2004). Also, in many cases females should prefer to mate with older males because viability selection leads to older males of higher genotypic quality than younger ]]>
There are many studies of chemical communication in European and North American snakes (e.g., Andren 1982, Mason 1993, LeMaster & Mason 2001, Mason & Parker 2010). However, the ecology and biology of Neotropical snakes is poorly ]]>
Epicrates cenchria, both sexes can detect and discriminate chemical cues of conspecifcs from other boid species (Briguera et al. 1994, 1998). Other study showed that male and female Boa constrictor occidentalis detect conspecifics odors and discriminate between sexes based on chemical cues from the skin and the cloacal glands (Chiaraviglio & Briguera 2001). These chemosensory abilities may help males to follow scent ]]>
Waglerophis merremii can discriminate sex of conspecifics (Chiaraviglio & Gutiérrez 1994).
In this study, we examined whether a boa snake species (Boa constrictor) ]]>
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Materials and Methods
Study species: We studied a snake species, B. constrictor (L., 1758), member of the family Boidae. This is a boa species mainly found in Central and South America and some ]]>
In this study, we ]]>
B. constrictor snakes that had been captured in different areas of Ecuador, and were maintained in captivity at the Vivarium of Quito, Fundación Herpetológica Gustavo Orcés (Av. Amazonas N.º 3008 y Rumipamba, Quito, Ecuador). All individuals were maintained separately in their own terraria, with the adequate temperature (24-26°C) and humidity conditions (58-78%). Snakes were fed weekly chicken or mice (the type and number of prey items depended on the size of each snake). We considered adult mature individuals ]]>
Scent recognition experiments: Snakes have been shown to react to a variety of chemical stimuli with ]]>
B. constrictor snakes of different ages in response to chemical stimuli arising from cotton swab applicators impregnated with scents of conspecific adult males or females, sub adults, juveniles, or with deionized water (odorless control). Water was used to gauge ]]>
Corallus hortulanus) (Mehrtens 1987, Valencia et al. 2008). These snakes were also maintained in the Vivarium of Quito. We obtained snake scents from the cloacal area and the skin surrounding it of males or females, because these body parts produce chemicals that are deposited on substrate trails, and can be explored by other snakes (Mason & Parker 2010). ]]>
Trials were conducted during October-November 2008. Prior to the tests, snakes were gently taken from their terraria and kept ]]>
B. constrictor snake (n=24) was exposed to each scent stimulus and order of presentation was randomized. One trial per each animal was conducted each day. ]]>
To begin a trial, the experimenter slowly approached the cage and slowly moved the cotton swab to a position 1cm anterior to the snake`s snout. Snakes usually did not flee from the swab, but explored it repeatedly by tongueflicking or ignored it after the firsts TFs. The numbers of TFs directed to the swab were recorded for 60s beginning with the first TF. Latency to the first TF was computed as the number of seconds elapsed between presentations of the cotton swab to the first TF directed to the swab.
To examine differences in latency times and number of directed TFs (both log-transformed) among scent stimuli presented, we used three-way repeated measures analyses of variance (ANOVAs) with scent stimuli as a within factor, and with the sex (male vs. female) and age (adult vs. non-mature) of the responding snake as between factors. Pairwise post-hoc comparisons were planned using Tukey’s honestly significant ]]>
Results
Latency time: There were significant differences in latencies to the first TF between scent ]]>
B. constrictor snakes of different ages and sexes responded in a similar way to the different stimuli (i.e., the interactions were not significant) (Table 1, Fig. 1). Latencies to water were significantly longer than to any other stimuli (Tukey’s tests, p<0.02 in all cases). Latencies to scent of adult male and female B. constrictor were not significantly ]]>
B. constrictor snakes (p<0.01 in all cases), which did not significantly differ (p=0.86). Latencies to scent of male and female C. hortulanus did not significantly differ from latencies to scents of B. constrictor snakes of any sex or age (p>0.25 in all cases) (Fig. 1). ]]>
Tongue flicks directed to the swab: The numbers of TFs directed to the swab by B. constrictor snakes were significantly different depending on the scent stimuli, and female snakes had a significantly higher overall TF rate than males. However, snakes of all sexes and ages responded in a similar way to the ]]>
Table 1, Fig. 2).
Tongue flick rate to water was significantly lower than to any other stimuli (Tukey’s tests, p<0.001 in all cases). Responses to adult male and female B. ]]>
were not significantly different (p=0.99), both were significantly higher than to scent from subadult and juvenile B. constrictor snakes (p=0.00012 in all cases), and TF rates to scent of sub adults were significantly higher than to scent of juveniles (p=0.02). Responses to scent of adult male and female C. hortulanus were not significantly different (p=0.99). Both were significantly greater than to scent of juveniles ]]>
B. constrictor (p=0.00014 in all cases) (Fig. 2).
Discussion ]]>
Our results showed that B. constrictor snakes used chemical cues to recognize conspecifics and that the scent of individuals of different ages elicited chemosensory responses of different magnitude. The chemosensory tests first showed that individuals of any sex or age responded quicker with tongue-flicks and had higher responses to cotton swabs impregnated with any snakes’ scents than to cotton swabs with water alone. This confirms previous ]]>
Further, results of this study showed that the scents from adult conspecifics elicited the quickest and highest chemosensory responses although we did not find ]]>
B. constrictor show higher TF responses to female scent than to male scent (Chiaraviglio & Briguera 2001). Something similar occurs in other Boidae species, E. cenchria (Briguera et al. 1994, 1997). The apparent lack of sex discrimination in our study might be explained because chemosensory responses of snakes to conspecific scents may depend on their reproductive state (Chiaraviglio & Gutiérrez 1994).
In our study, the magnitude of the chemosensory responses was lower to scent of sub adult individuals, and even lower to scent of juvenile snakes. Nevertheless, as indicated above, all of these scents were detected by snakes. Interestingly, the scent of adults of a heterospecific snake was quickly detected but later elicited low TF responses that did not ]]>
B. constrictor and to scent of adult C. hortulanus indicated that there is species recognition. These results could suggest that although all these scents could be detected, after being identified, some of them were not further considered for more detailed chemosensory exploration, resulting in lower TF rates.
These differences in the magnitude of the responses are probably related to the different importance that finding individuals of different ages may have in social and sexual behavior of this snake. For example, in male Boiga irregularis snakes, adult female skin lipid pheromones induce courtship behavior, while adult male skin lipid pheromones induce combat behaviors (Greene & Mason 1998, 2000). Nonmature individuals are not involved in sexual ]]>
B. constrictor snakes we require further experiments.
Mature and ]]>
B. constrictor snakes responded in a similar way to the different scent stimuli, with high responses to scent of adult individuals and low responses to scent of juveniles. Although when finding a scent the “motivation” and posterior behavioral responses should vary with the age of the responding snake, it is likely that the same chemical stimuli induced similar tongue-flick responses in the vomeronasal system of any conspecific snake (Halpern 1992). Nevertheless, female snakes had higher overall TF rates to most stimuli than males, which ]]>
The chemosensory age discrimination may simply respond to differences in the amount of chemical secretions that individuals of different age produce, with juvenile snakes producing the lowest amounts of secretions. The production of ]]>
Thamnophis sirtalis, the methyl ketone pheromone blend found in the scent of the skin becomes dominated by the longest chain, unsaturated methyl ketones with increasing ]]>
In summary, in this study we show that B. constrictor snakes are able to use chemical cues of conspecifics in intraspecific recognition and age ]]>
Acknowledgments
We thank three anonymous reviewers for helpful comments, and K. Garzón and M.E. Barragán, from the Vivarium de Quito, Fundación Herpetológica Gustavo Orcés, for access and facilities to work with the snakes. Financial support was ]]>
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*Correspondencia: Marianne Gabirot: Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain; marianne.gabirot@cefe.cnrs.fr . Department Ecologie Comportementale, (U.M.R. 5175), CEFE-CNRS, 1919 Route de Mende, F34293 Montpellier, Cedex 5, France. Pablo Picerno: Fundacion Herpetológica Gustavo Orces, Vivarium de Quito, Av. Amazonas 3008 y Rumipamba, Quito, Ecuador; pablopicerno@yahoo.com Jorge Valencia: Fundacion Herpetológica Gustavo Orces, Vivarium de Quito, Av. Amazonas 3008 y Rumipamba, Quito, Ecuador; jvalencia@fhgo.org.ec . Pontificia Universidad Católica del Ecuador, Escuela de Biología, Museo de Zoología. Avenida 12 de Octubre y Roca, Apartado 17-01-2184. Quito, Ecuador. Pilar Lopez: Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain; pilar.lopez@mncn.csic.es José Martin: Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain; jose.nartin@mncn.csic.es 1. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain; jose.nartin@mncn.csic.es, pilar.lopez@mncn.csic.es 2. Department Ecologie Comportementale, (U.M.R. 5175), CEFE-CNRS, 1919 Route de Mende, F34293 Montpellier, Cedex 5, France; marianne.gabirot@cefe.cnrs.fr 3. Fundacion Herpetológica Gustavo Orces, Vivarium de Quito, Av. Amazonas 3008 y Rumipamba, Quito, Ecuador; pablopicerno@yahoo.com 4. Pontificia Universidad Católica del Ecuador, Escuela de Biología, Museo de Zoología. Avenida 12 de Octubre y Roca, Apartado 17-01-2184. Quito, Ecuador; jvalencia@fhgo.org.ec
Received 01-XI-2011.Corrected 04-V-2012.Accepted 05-VI-2012.