Chemically mediated self-recognition in sibling juvenile common gartersnakes (Thamnophis sirtalis) reared on same or different diets: evidence for a chemical mirror?
In: BehaviourDepartment of Ecology & Evolutionary Biology, University of Tennessee, Knoxville, TN 37920, USA
Search for other papers by Gordon M. Burghardt in
Current site
Google Scholar
Search for other papers by Adam M. Partin in
Current site
Google Scholar
Search for other papers by Harry E. Pepper in
Current site
Google Scholar
Search for other papers by Jordan M. Steele in
Current site
Google Scholar
Search for other papers by Samuel M. Liske in
Current site
Google Scholar
Search for other papers by Allyson E. Stokes in
Current site
Google Scholar
Search for other papers by Ariel N. Lathan in
Current site
Google Scholar
Search for other papers by Cary M. Springer in
Current site
Google Scholar
Search for other papers by Matthew S. Jenkins in
Current site
Google Scholar
Abstract
Although self-recognition or self-awareness has been studied with the visually-based mirror test, passed by several species, primarily apes, the possibility of a chemically-based analogue is controversial. Prior studies suggested that chemical self-recognition may occur in some squamate reptiles. To evaluate this possibility, we studied 24 individually housed gartersnakes, Thamnophis sirtalis, raised from birth on either earthworm or fish diets and tested 12 male and 12 female snakes with cage liners that were either clean, their own, or from same-sex siblings fed their own or the opposite diet. Tongue flicking and activity were recorded in 30-minute video-recorded trials in a balanced design. After initial habituation to the stimuli, male, but not female, snakes discriminated between their own stimuli and those from littermates fed the same diet. Combined with other data and studies, the possibility that a chemical ‘mirror’ form of self-recognition exists in squamate reptiles is supported.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Aguilar, P.M., Labra, A. & Niemeyer, H.M. (2009). Chemical self-recognition in the lizard Liolaemus fistzgeraldi. — J. Ethol. 27: 181-184.
-
Alberts, A.A. (1989). Ultraviolet visual sensitivity in desert iguanas: implications for pheromone detection. — Anim. Behav. 38: 129-137.
-
Alberts, A.A. (1992). Pheromonal self-recognition in desert iguanas. — Copeia: 229-232.
-
Baeckens, S., Herrel, A., Broeckhoven, C., Vasilopoulou-Kampitis, M., Huyghe, K., Goyens, J. & Van Damme, R. (2017). Evolutionary morphology of the lizard chemosensory system. — Sci. Rep. 7: 10141.
-
Baragli, P., Scopa, C., Maglieri, V. & Palagi, E. (2021). If horses had toes: demonstrating mirror self recognition at group level in Equus caballus. — Anim. Cogn. 24: 1099-1108.
-
Burghardt, G.M. (1980). Behavioral and stimulus correlates of vomeronasal functioning in reptiles: feeding, grouping, sex, and tongue use. — In: Chemical signals in vertebrates and aquatic invertebrates (Müller-Schwarze, D. & Silverstein, R., eds). Plenum, New York, NY, p. 275-301.
-
Burghardt, G.M. (1983). Aggregation and species discrimination in newborn snakes. — Z. Tierpsychol. 61: 89-101.
-
Burghardt, G.M. & Schwartz, J.M. (1999). Geographic variations on methodological themes in comparative ethology: a natricine snake perspective. — In: Geographic variation in behavior: perspectives on evolutionary mechanisms (Foster, S.A. & Endler, J.A., eds). Oxford University Press, Oxford, p. 69-94.
-
Carazo, P., Font, E. & Desfilis, E. (2008). Beyond “nasty neighbours” and “dear enemies”? Individual recognition by scent marks in a lizard (Podarcis hispanica). — Anim. Behav. 76: 1953-1963.
-
Cazzolla Gatti, R. (2016). Self-consciousness: beyond the looking-glass and what dogs found there. — Ethol. Ecol. Evol. 28: 232-240.
-
Cazzolla Gatti, R., Velichevskaya, A., Gottesman, B. & Davis, K. (2021). Grey wolf may show signs of self-awareness with the sniff test of self-recognition. — Ethol. Ecol. Evol. 33: 444-467.
-
Chiszar, D., Smith, H.M., Bogert, C.M. & Vidaurri, J. (1991). A chemical sense of self in timber and prairie rattlesnakes. — Bull. Psychon. Soc. 29: 153-154.
-
Chiszar, D., Tomlinson, W.T., Smith, H.M., Murphy, J.B. & Radcliffe, C.W. (1995). Behavioural consequences of husbandry manipulations: indicators of arousal, quiescence and environmental awareness. — In: Health and welfare of captive reptiles (Warwick, C., Frye, F.L. & Murphy, J.B., eds). Chapman & Hall, London, p. 186-204.
-
Chiszar, D., Wellborn, S., Wand, W.A., Scudder, K.M. & Smith, H.M. (1980). Investigatory behavior in snakes, II: cage cleaning and induction of defecation in snakes. — Anim. Learn. Behav. 8: 505-510.
-
Conant, R. (1971). Reptile and amphibian management at Philadelphia Zoo. — Int. Zoo Yearb. 11: 224-230.
-
Cooper, W.E. Jr. & Burghardt, G.M. (1990). Vomerolfaction and vomodor. — J. Chem. Ecol. 16: 103-105.
-
de Waal, F. (2016). Are we smart enough to know how smart animals are? — W.W. Norton, New York, NY.
-
de Waal, F.B.M. (2019). Fish, mirrors, and a gradualist perspective on self-awareness. — PLoS Biol. 17: e3000112.
-
Doody, J.S., Burghardt, G.M. & Dinets, V. (2013). Breaking the social-nonsocial dichotomy: a role for reptiles in vertebrate social behaviour research? — Ethology 119: 95-103.
-
Dundee, H.A. & Miller, M.C. (1968). Aggregative behavior and habitat conditioning by the prairie ringneck snake, Diadophis punctatus arnyi. — Tulane Stud. Zool. Bot. 15: 41-58.
-
Duvall, D., Graves, B.M. & Carpenter, G.C. (1987). Visual and chemical composite signaling effects of Sceloporus lizard fecal boli. — Copeia: 1028-1031.
-
Fabbro, F., Agliotl, S.M., Bergamasco, M., Clarici, A. & Panksepp, J. (2015). Evolutionary aspects of self- and world consciousness in vertebrates. — Front. Human Neurosci. 9: 157. DOI:10.3389/fnhum.2015.00157.
-
Font, E., Burghardt, G.M. & Leal, M. (in press). Reptile brains, behavior, and cognition: multiple misconceptions. — In: Health and welfare of captive reptiles, 2nd edn. (Warwick, C., Arena, P. & Burghardt, G.M., eds). Springer Nature, Cham.
-
Gallup, G.G., Jr. & Anderson, J.R. (2018). The “olfactory mirror” and other recent attempts to demonstrate self-recognition in non-primate species. — Behav. Process. 148: 16-19.
-
Gallup, G.G., Jr. & Anderson, J.R. (2019). Self-recognition in animals: where do we stand 50 years later? Lessons from cleaner wrasse and other species. — Psychol. Consciousn.: Theor. Res. Pract. 7: 46-58.
-
Gallup, G.G., Jr., Anderson, J.R. & Shillito, D.J. (2002). The mirror test. — In: The cognitive animal: empirical and theoretical perspectives on animal cognition (Bekoff, M., Allen, C. & Burghardt, G.M., eds). MIT Press, Cambridge, MA, p. 325-333.
-
Gove, D. & Burghardt, G.M. (1983). Context-correlated parameters of snake and lizard tongue-flicking. — Anim. Behav. 31: 718-723. DOI:10.1016/S0003-3472(83)80227-9.
-
Graves, B.M. & Halpern, M. (1991). Discrimination of self from conspecific chemical cues in Tiliqua scincoides (Sauria: Scincidae). — J. Herp. 25: 125-126.
-
Halpin, Z.T. (1986). Individual odors among mammals: origins and functions. — Adv. Study Behav. 16: 39-70.
-
Halpin, Z.T. (1990). Responses of juvenile eastern garter snakes (Thamnophis sirtalis sirtalis) to own, conspecific and clean odors. — Copeia: 1157-1160.
-
Horowitz, A. (2017). Smelling themselves: dogs investigate their own odours longer when modified in an “olfactory mirror” test. — Behav. Process. 143: 17-24.
-
Hsiang, A., Field, D.J., Webster, T.H., Behlke, A.D.B., Davis, M.B., Raciot, R.A. & Gauthier, J.A. (2015). The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. — BMC Evol. Biol. 15: 87. DOI:10.1186/s12862-015-0358-5.
-
Khvatov, I.A., Sokolov, AY. & Kharitonov, A.N. (2019). Snakes Elaphe radiata may acquire awareness of their body limits when trying to hide in a shelter. — Behav. Sci. 9: 67. DOI:10.3390/bs9070067.
-
Labra, A. (2006). Chemoreception and the assessment of fighting abilities in the lizard Liolaemus monticola. — Ethology 112: 993-999.
-
Lyman-Henley, L. & Burghardt, G.M. (1994). Opposites attract: effects of social and dietary experience on snake aggregation behaviour. — Anim. Behav. 47: 980-982.
-
Mangiacotti, M., Gaggiani, S., Coladonato, A.J., Scali, S., Zuffi, M.A.L. & Sacchi, R. (2019). First experimental evidence that proteins from femoral glands convey identity related information in a lizard. — Acta Ethol. 22: 57-65.
-
Mangiacotti, M., Martin, J., López, P., Reyes-Olivares, C.V., Rodriguez-Ruiz, G., Coladonato, A.J., Scali, S., Zuffi, M.A.L. & Sacchi, R. (2020). Proteins from femoral gland secretions of male rock lizards Iberolacerta cyreni allow self — but not individual-recognition of unfamiliar males. — Behav. Ecol. Sociobiol. 74: 68. DOI:10.1007/s00265-020-02847-8.
-
Martín, J., García, E.R., Ortega, J. & López, P. (2020). How to maintain underground social relationships? Chemosensory sex, partner and self recognition in a fossorial amphisbaenian. — PLoS ONE 15: e0237188. DOI:10.1371/journal.pone.0237188.
-
Matteo, J.M. & Johnston, R.E. (2000). Kin recognition and the ‘armpit effect’: evidence of self-referent phenotypic matching. — Proc. Roy. Soc. Lond. B: Biol. Sci. 267: 695-700.
-
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.
-
Pernetta, A.P., Reading, C.J. & Allen, J.A. (2009). Chemoreception and kin discrimination by neonate smooth snakes, Coronella austrica. — Anim. Behav. 77: 363-368.
-
Petrulis, A., Alvarez, P. & Eichenbaum, H. (2005). Neural correlates of social odor recognition and the representation of individual social odors within entorhinal cortex and ventral subiculum. — Neuroscience 130: 259-274.
-
Placyk, J.S. & Burghardt, G.M. (2011). Evolutionary persistence of chemically elicited ophiophagus antipredator responses in gartersnakes, Thamnophis sirtalis. — J. Comp. Psychol. 125: 134-142.
-
Reichenbach, N.G. (1983). An aggregation of female garter snakes under corrugated metal sheets. — J. Herpetol. 17: 412-413.
-
Reiss, D. & Morrison, R. (2017). Reflecting on mirror self-recognition: a comparative view. — In: APA handbook of comparative psychology, vol. 2 (Call, J., Burghardt, G.M., Pepperberg, I.M., Snowdon, C.T. & Zentall, T., eds). American Psychological Association, Washington, DC, p. 745-763.
-
Schwenk, K. (1995). Of tongues and noses: chemoreception in lizards and snakes. — Trends Ecol. Evol. 10: 7-12.
-
Skinner, M. & Miller, N. (2020). Aggregation and social interaction in garter snakes (Thamnophis sirtalis sirtalis). — Behav. Ecol. Sociobiol. 74: 51. DOI:10.1007/s00265-020-2827-0.
-
Sommerville, B.A. & Broom, D.M. (1998). Olfactory awareness. — Appl. Anim. Behav. Sci. 57: 269-286.
-
Van Damme, R., Bauwens, D., Thoen, C., Vanderstighelen, D. & Verheyen, R.F. (1995). Responses of naïve lizards to predator chemical cues. — J. Herpetol. 33: 38-43.
-
Van Moorleghem, C., Huyghe, K. & Van Damme, R. (2020). Chemosensory deficiency may render island-dwelling lizards more vulnerable to invasive predators. — Biol. J. Linn. Soc. 129: 128-142.
-
Wellborn, S., Scudder, K.M., Smith, H.M., Stimac, K. & Chiszar, D. (1982). Investigatory behavior in snakes: III. Effects of familiar odors on investigation of clean cages. — Psychol. Rec. 32: 169-177.
-
Yeager, C. & Burghardt, G.M. (1991). The effect of food competition on aggregation: evidence for social recognition in the plains garter snake (Thamnophis radix). — J. Comp. Psychol. 105: 380-386.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2816 | 639 | 50 |
| Full Text Views | 229 | 29 | 2 |
| PDF Views & Downloads | 375 | 65 | 2 |
Chemically mediated self-recognition in sibling juvenile common gartersnakes (Thamnophis sirtalis) reared on same or different diets: evidence for a chemical mirror?
In: BehaviourDepartment of Ecology & Evolutionary Biology, University of Tennessee, Knoxville, TN 37920, USA
Search for other papers by Gordon M. Burghardt in
Current site
Google Scholar
PubMed
Search for other papers by Adam M. Partin in
Current site
Google Scholar
PubMed
Search for other papers by Harry E. Pepper in
Current site
Google Scholar
PubMed
Search for other papers by Jordan M. Steele in
Current site
Google Scholar
PubMed
Search for other papers by Samuel M. Liske in
Current site
Google Scholar
PubMed
Search for other papers by Allyson E. Stokes in
Current site
Google Scholar
PubMed
Search for other papers by Ariel N. Lathan in
Current site
Google Scholar
PubMed
Search for other papers by Cary M. Springer in
Current site
Google Scholar
PubMed
Search for other papers by Matthew S. Jenkins in
Current site
Google Scholar
PubMed
Abstract
Although self-recognition or self-awareness has been studied with the visually-based mirror test, passed by several species, primarily apes, the possibility of a chemically-based analogue is controversial. Prior studies suggested that chemical self-recognition may occur in some squamate reptiles. To evaluate this possibility, we studied 24 individually housed gartersnakes, Thamnophis sirtalis, raised from birth on either earthworm or fish diets and tested 12 male and 12 female snakes with cage liners that were either clean, their own, or from same-sex siblings fed their own or the opposite diet. Tongue flicking and activity were recorded in 30-minute video-recorded trials in a balanced design. After initial habituation to the stimuli, male, but not female, snakes discriminated between their own stimuli and those from littermates fed the same diet. Combined with other data and studies, the possibility that a chemical ‘mirror’ form of self-recognition exists in squamate reptiles is supported.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2816 | 639 | 50 |
| Full Text Views | 229 | 29 | 2 |
| PDF Views & Downloads | 375 | 65 | 2 |