Journal of Chemical Ecology

, Volume 20, Issue 2, pp 439–487 | Cite as

Chemical discrimination by tongue-flicking in lizards: A review with hypotheses on its origin and its ecological and phylogenetic relationships

  • William E. Cooper


Tongue-flicking is a synapomorphy of squamate reptiles functioning to sample chemicals for vomerolfactory analysis, which became possible in primitive squamates when ducts opened from the vomeronasal organs to the roof of the mouth. Extant iguanian lizards in families that do not use the tongue to sample chemical prey cues prior to attack partially protrude it in two feeding contexts: during capture by lingual prehension and after oral contact with prey. These lizards do not exhibit strike-induced chemosensory searching. Lingual prey prehension is present in iguanian lizards and inSphenodon, the sister taxon of Squamata. During attempts to capture prey, the tongues of primitive squamates inevitably made incidental contact with environmental substrates bearing chemicals deposited by prey, conspecifics, and predators. Such contact presumably induced selection for tongue-flicking and ability to identify biologically important chemicals. Most iguanian lizards are ambush foragers that use immobility as a major antipredatory defense. Because tongue-flicking at an ambush post would not allow chemical search beyond the vicinity of the head and would render them easier for predators and prey to detect, typical iguanians tongue-flick neither while foraging nor to identify predators. They do detect pheromones by tongue-flicking. Scleroglossan lizards are typically active foragers that rely on speed to escape. Being freer to move the tongue, they have evolved lingual sampling allowing detection of chemical cues of conspecifics, predators, and prey, as well as strike-induced chemosensory searching, some can follow pheromone trails by tongue-flicking. Some families have lingual morphology and behavior specialized for chemosensory sampling. In varanids and snakes, the taxa showing the greatest lingual specialization, additional prey-related chemosensory behaviors have evolved. In iguanian and scleroglossan families that have secondarily adopted the foraging mode typical of the other taxon, prey chemical discrimination involving tongue-flicking and strike-induced chemosensory searching are typical for the foraging mode rather than the taxon. Because foraging mode and state of prey chemical discrimination are stable within squamate families and to a large extent in higher taxa, both features have been retained from the ancestral condition in most families. However, in three cases in which foraging mode has changed from its ancestral state, the state of prey chemical discrimination has also changed, indicating that prey chemical discrimination is adaptively adjusted to foraging mode. Indeed, acquisition of lingually mediated prey chemical discrimination may have made feasible the evolution of active foraging, which in turn appears to have profoundly influenced the further evolution of squamate chemosensory structures and behavior, placing a selective premium on features enhancing the tongue's efficiency as a chemical sampling device. The advent of tongue-flicking to sample prey chemicals and thus detect hidden prey may have allowed generalist (cruise) or ambush foragers, if early squamates were such, to become specialists in active foraging. Alternatively, if the common ancestors of squamates were active foragers, the adoption of ambush foraging would have selected against participation of the tongue in locating prey. Acting jointly, tongue-flicking and active foraging have had momentous consequences for squamate diversification. Specialization for active foraging would appear to have had ramifying effects on antipredatory defenses, body form, territoriality, mating systems, and reproductive physiology.

Key Words

Tongue-flicking vomerolfaction squamata Scleroglossa Iguania lizards snakes iguanas geckos predatory-prey interaction olfaction active foraging ambush foraging poststrike elevation in tongue-flicking strike-induced comosensory searching 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alberts, A.C. 1989. Ultraviolet visual sensitivity in desert iguanas: Implications for pheromone detection.Anim. Behav. 38:129–137.Google Scholar
  2. Alberts, A.C. 1992. Pheromonal self-recognition in desert iguanas.Copeia 1992:229–232.Google Scholar
  3. Anderson, R.A. 1993. Analysis of foraging in a lizard,Cnemidophorus tigris: Salient features and environmental effects, pp. 83–116,in J.W. Wright and L.J. Vitt (eds.). Biology of Whiptail Lizards (GenusCnemidophorus). Oklahoma Museum of Natural History, Norman, Oklahoma.Google Scholar
  4. Anderson, R.A., andKarasov, W.H. 1981. Contrasts in energy intake and expenditure in sit-and-wait and widely foraging lizards.Oecologia 49:67–72.Google Scholar
  5. Anderson, R.A., andKarasov, W.H. 1988. Energetics of the lizardCnemidophorus tigris and life history consequences of food-acquisition mode.Ecol. Monogr. 58:79–110.Google Scholar
  6. Andrews, R.M. 1979. The lizardCorytophanes cristatus: An extreme “sit-and-wait” predator.Biotropica 11:136–139.Google Scholar
  7. Arnold, E.N. 1984. Ecology of lowland lizards in the eastern United Arab Emirates.J. Zool. 204:329–354.Google Scholar
  8. Arnold, E.N. 1990. Why do morphological phylogenies vary in quality? An investigation based on the comparative history of lizard clades.Proc. R. Soc. London B 240:135–172.Google Scholar
  9. Arnold, E.N., andBurton, J.A. 1978. A Field Guide to the Reptiles and Amphibians of Britain and Europe. Collins, London.Google Scholar
  10. Arnold, S.J. 1981. Behavioral variation in natural populations. I. Phenotypic, genetic, and environmental correlations between chemoreceptive responses to prey in the garter snake,Thamnophis elegans.Evolution 35:489–509.Google Scholar
  11. Auffenberg, W. 1981. The Behavioral Ecology of the Komodo Monitor. University Presses of Florida, Gainesville.Google Scholar
  12. Auffenberg, W. 1984. Notes on the feeding behaviour ofVaranus bengalensis (Sauria: Varanidae).J. Bombay Nat. Hist. Soc. 80:286–302.Google Scholar
  13. Baird, I.L. 1970. The anatomy of the reptilian ear, pp. 193–275,in C. Gans and T.S. Parsons (eds.). Biology of the Reptilia, Vol. 2, Morphology B. Academic Press, London.Google Scholar
  14. Beck, D.D. 1990. Ecology and behavior of the gila monster in southwestern Utah.J. Herpetol. 24:54–68.Google Scholar
  15. Beck, D.D., andLowe, C.H. 1991. Ecology of the beaded iizard,Heloderma horridum, in a tropical dry rain forest in Jalisco, Mexico.J. Herpetol. 25:395–406.Google Scholar
  16. Bennett, A.F. 1973. Ventilation in two species of lizards during rest and activity.Comp. Biochem. Physiol. 46A:653–671.Google Scholar
  17. Bertmar, G. 1981. Evolution of vomeronasal organs in vertebrates.Evolution 35:359–366.Google Scholar
  18. Bickler, P.E., andAnderson, R.A. 1986. Ventilation, gas exchange, and aerobic scope in a small monitor lizard,Varanus gilleni.Physiol. Zool. 59:76–83.Google Scholar
  19. Bissinger, B.E., andSimon, C.E. 1979. Comparison of tongue extrusion in representatives of six families of lizards.J. Herpetol. 13:133–139.Google Scholar
  20. Bogert, G.M. 1941. Sensory cues used by rattlesnakes in their recognition of ophidian enemies.Ann. N.Y. Acad. Sci. 41:329–344.Google Scholar
  21. Bogert, G.M., andDel Campo, R.M. 1956. The gila monster and its allies: The relationships, habits, and behavior of the lizards of the family Helodermatidae.Bull. Am. Mus. Nat. Hist. 109:1–238.Google Scholar
  22. Branch, B. 1988. Field Guide to the Snakes and other Reptiles of Southern Africa. Ralph Curtis, Sanibel Island, Florida.Google Scholar
  23. Brillet, C. 1990. Role des informations olfactives et visuelles dans la discrimination du sexe chez deux espèces de geckos nocturnesEublepharis macularius etParoedura pictus.Biol. Behav. 15:1–22.Google Scholar
  24. Brillet, C. 1991. Comparative analysis of the structure of the sexual behavior of two species of nocturnal geckos:Eublepharis macularius andParoedura pictus (Sauria, Gekkonidae).Behaviour 117:117–143.Google Scholar
  25. Broadley, D.G. 1978. A revision of the genusPlatysaurus A. Smith (Sauria: Cordylidae).Occ. Pap. Natl. Mus. Rhod., B., Nat. Sci. 6:129–185.Google Scholar
  26. Brown, W.S., andMacLean, F.M. 1983. Conspecific scent-trailing by newborn timber rattlesnakes,Crotalus horridus.Herpetologica 39:430–436.Google Scholar
  27. Burghardt, G.M. 1967. Chemical-cue preferences of inexperienced snakes: Comparative aspects.Science 157:718–721.PubMedGoogle Scholar
  28. Burghardt, G.M. 1970a. Chemical perception in reptiles, pp. 241–308,in J.W. Johnston, D.G. Moulton, and A. Turk (eds.). Advances in Chemoreception, Vol. I. Communication by Chemical Signals. Appleton-Century-Crofts, New York.Google Scholar
  29. Burghardt, G.M. 1970b. Intraspecific geographical variation in chemical food cue preferences of newborn garter snakes (Thamnophis sirtalis).Behaviour 36:246–257.Google Scholar
  30. Burghardt, G.M. 1973. Chemical release of prey attack: Extension to naive newly hatched lizards,Eumeces laticeps.Copeia 1973:178–181.Google Scholar
  31. Burghardt, G.M., Goss, S.E., andSchell, F.M. 1988. Comparison of earthworm- and fish-derived chemicals eliciting prey attack by garter snakes (Thamnophis).J. Chem. Ecol. 14:855–881.Google Scholar
  32. Camp, C. 1923. Classification of the Lizards.Bull. Am. Mus. Nat. Hist. 48:289–481.Google Scholar
  33. Chiszar, D., andScudder, K.M. 1980. Chemosensory searching by rattlesnakes during predatory episodes, pp. 125–139,in D. Müller-Schwarze and R.M. Silverstein (eds.). Chemical Signals in Vertebrates and Aquatic Invertebrates. Plenum Press, New York.Google Scholar
  34. Chiszar, D., Radcliffe, C.W., Scudder, K.M., andDuvall, D. 1983. Strike-induced chemosensory by rattlesnakes: The role of envenomation-related cues in the post-strike environment, pp. 1–24,in D. Müller-Schwarze and R.M. Silverstein (eds.). Chemical Signals in Vertebrates III. Plenum Press, New York.Google Scholar
  35. Chiszar, D., Radcliffe, C.W., Overstreet, R., Poole, T., andByers, T. 1985. Duration of strike-induced chemosensory searching in cottonmouths (Agkistrodon piscovorus) and a test of the hypothesis that striking prey creates a specific search image.Can. J. Zool. 63:1057–1061.Google Scholar
  36. Chiszar, D., Radcliffe, C.W., Boyd, R., Radcliffe, A., Yun, H., Smith, H.M., Boyer, T., Atkins, B., andFeiler, F. 1986a. Trailing behavior in cottonmouths (Agkistrodon piscivorus).J. Herpetol. 20:269–272.Google Scholar
  37. Chiszar, D., Radcliffe, C.W., andFeiler, F. 1986b. Trailing behavior in banded rock rattlesnakes (Crotalus lepidus klauberi) and prairie rattlesnakes (C. viridis viridis).J. Comp. Psychol. 100:368–371.Google Scholar
  38. Cooper, W.E., Jr. 1989a. Absence of prey odor discrimination by iguanid and agamid lizards in applicator tests.Copeia 1989:472–478.Google Scholar
  39. Cooper, W.E., Jr. 1989b. Prey odor discrimination in the varanoid lizardsHeloderma suspectum andVaranus exanthematicus.Ethology 81:250–258.Google Scholar
  40. Cooper, W.E., Jr. 1989c. Strike-induced chemosensory searching occurs in lizards.J. Chem. Ecol. 15:1311–1320.Google Scholar
  41. Cooper, W.E., Jr. 1990a. Prey odour discrimination by lizards and snakes, pp. 533–538,in D.W. MacDonald, D. Müller-Schwarze, and S.E. Natynczuk (eds.). Chemical Signals in Vertebrates 5. Oxford University Press, Oxford.Google Scholar
  42. Cooper, W.E., Jr. 1990b. Prey odor detection by teiid and lacertid lizards and the relationship of prey odor detection to foraging mode in lizard families.Copeia 1990:237–242.Google Scholar
  43. Cooper, W.E., Jr. 1990c. Chemical detection of predators by a lizard, the broad-headed skink (Eumeces laticeps).J. Exp. Zool. 256:162–167.Google Scholar
  44. Cooper, W.E., Jr. 1990d. Prey odor discrimination by anguid lizards.Herpetologica 46:183–190.Google Scholar
  45. Cooper, W.E., Jr. 1991a. Responses to prey chemicals by a lacertid lizard,Podarcis muralis: Prey chemical discrimination and poststrike elevation in tongue-flick rate.J. Chem. Ecol. 17:849–863.Google Scholar
  46. Cooper, W.E., Jr. 1991b. Discrimination of integumentary prey chemicals and strike-induced chemosensory searching in the ball python,Python regius.J. Ethol. 9:9–23.Google Scholar
  47. Cooper, W.E., Jr. 1992a. Prey odor discrimination and post-strike elevation in tongue flicking by a cordylid lizard,Gerrhosaurus nigrolineatus.Copeia 1992:146–154.Google Scholar
  48. Cooper, W.E., Jr. 1992b. Elevation in tongue-flick rate after biting prey in the broad-headed skink,Eumeces laticeps.J. Chem. Ecol. 18:455–467.Google Scholar
  49. Cooper, W.E., Jr. 1993. Duration of poststrike elevation in tongue-flicking rate in the savannah monitor lizard.Ethol. Ecol. Evol. 5:1–18.Google Scholar
  50. Cooper, W.E., Jr. 1994a. Lingual and searching responses to prey chemicals by three iguanian lizard species.Anim. Behav. In press.Google Scholar
  51. Cooper, W.E., Jr. 1994b. Prey chemical discrimination and foraging mode in gekkonoid lizards.Herpetol. Monogr. In press.Google Scholar
  52. Cooper, W.E., Jr. 1994c. Prey chemical discrimination, foraging mode, and phylogeny, pp. E.R. Pianka and L.J. Vitt (eds.). Lizard Ecology: The Third Generation. Princeton University Press, Princeton, New Jersey. In press.Google Scholar
  53. Cooper, W.E., Jr., andAlberts, A.C. 1990. Responses to chemical food stimuli by an herbivorous actively foraging lizard,Dipsosaurus dorsalis.Herpetologica 46:259–266.Google Scholar
  54. Cooper, W.E., Jr., andAlberts, A.C. 1991. Tongue-flicking and biting in response to chemical food stimuli by an iguanid lizard (Dipsosaurus dorsalis) having sealed vomeronasal ducts: Vomerolfaction may mediate these behavioral responses.J. Chem. Ecol. 17:135–146.Google Scholar
  55. Cooper, W.E., Jr. andAlberts, A.C. 1993. Post-bite elevation in tongue-flicking rate by an iguanian lizard,Dipsosaurus dorsalis. J. Chem. Ecol. In press.Google Scholar
  56. Cooper, W.E., Jr., andBurghardt, G.M. 1990a. Vomerolfaction and vomodor.J. Chem. Ecol. 16:103–105.Google Scholar
  57. Cooper, W.E., Jr., andBurghardt, G.M. 1990b. A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles.J. Chem. Ecol. 16:45–65.Google Scholar
  58. Cooper, W.E., Jr., andGarstka, W.R. 1987a. Discrimination of male conspecific from male heterospecific odors by male scincid lizards (Eumeces laticeps).J. Exp. Zool. 241:253–256.Google Scholar
  59. Cooper, W.E., Jr., andGarstka, W.R. 1987b. Lingual responses to chemical fractions of urodaeal glandular pheromone of the skinkEumeces laticeps.J. Exp. Zool. 242:249–253.Google Scholar
  60. Cooper, W.E., Jr., andTrauth, S.E. 1992. Discrimination of conspecific male and female cloacal chemical stimuli by males and possession of a probable pheromone gland by females in a cordylid lizard,Gerrhosaurus nigrolineatus.Herpetologica 48:229–236.Google Scholar
  61. Cooper, W.E., Jr., andVitt, L.J. 1984a. Conspecific odor detection by the male broad-headed skink,Eumeces laticeps: Effects of sex and site of odor source and of male reproductive condition.J. Exp. Zool. 230:199–209.PubMedGoogle Scholar
  62. Cooper, W.E., Jr., andVitt, L.J. 1984b. Detection of conspecific odors by the female broad-headed skink,Eumeces laticeps.J. Exp. Zool. 229:49–54.Google Scholar
  63. Cooper, W.E., Jr., andVitt, L.J. 1986a. Tracking o female conspecific odor trails by male broad-headed skinks (Eumeces laticeps).Ethology 71:242–248.Google Scholar
  64. Cooper, W.E., Jr., andVitt, L.J. 1986b. Lizard pheromones: Behavioral responses and adaptive significance in skinks of the genusEumeces, pp. 323–340,in D. Duvall, D. Müller-Schwarze, and R.M. Silverstein (eds.). Chemical Signals in Vertebrates 4: Ecology, Evolution, and Comparative Biology. Plenum Press, New York.Google Scholar
  65. Cooper, W.E., Jr., andVitt, L.J. 1986c. Interspecific odour discrimination by a lizard (Eumeces laticeps).Anim. Behav. 34:367–376.Google Scholar
  66. Cooper, W.E., Jr., andVitt, L.J. 1987a. Ethological isolation, sexual behavior and pheromones in the fasciatus species group of the lizard genusEumeces.Ethology 75:328–326.Google Scholar
  67. Cooper, W.E., Jr., andVitt, L.J. 1987b. Intraspecific and interspecific aggression in lizards of the scincid genusEumeces: Chemical detection of conspecific sexual competitors.Herpetologica 43:7–14.Google Scholar
  68. Cooper, W.E., Jr., andVitt, L.J. 1989. Prey odor discrimination by the broad-headed skink (Eumeces laticeps).J. Exp. Zool. 249:11–16.Google Scholar
  69. Cooper, W.E., Jr., Garstka, W.R., andVitt, L.J. 1986. Female sex pheromone in the lizardEumeces laticeps.Herpetologica 42:361–366.Google Scholar
  70. Cooper, W.E., Jr., McDowell, S.G., andRuffer, J. 1989. Strike-induced chemosensory searching in the colubrid snakesElaphe g. guttata andThamnophis sirtalis.Ethology 81:19–28.Google Scholar
  71. Cooper, W.E., Jr., Vitt, L.J., andCaldwell, J.P. 1994a. Movement and substrate tongue-flicks in phrynosomatic lizards.Copeia In press.Google Scholar
  72. Cooper, W.E., Jr., Lopez, P., andSalvador, A. 1994b. Pheromone detection by an amphisbaenian. In press.Google Scholar
  73. Cowles, R.B., andPhelan, R.L. 1958. Olfaction in rattlesnakes.Copeia 1958:77–83.Google Scholar
  74. Curio, V.E., andMöbius, H. 1978. Versuche zum Nachweis eines Riechvermögens vonAnolis l. lineatopus (Rept., Iguanidae).Z. Tierpsychol. 47:281–292.Google Scholar
  75. Dial, B.E. 1978. Aspects of the behavioral ecology of two Chihuahuan desert geckos (Reptilia, Lacertilia, Gekkonidae).J. Herpetol. 12:209–216.Google Scholar
  76. Dial, B.E. 1990. Predator-prey signals: Chemosensory identification of snake predators by eublepharid lizards and its ecological consequences, pp. 555–565,in D.W. MacDonald, D. Müller-Schwarze, and S.E. Natynczuk (eds.). Chemical Signals in Vertebrates 5. Oxford University Press, Oxford.Google Scholar
  77. Dial, B.E., Weldon, P.J., andCurtis, B. 1989. Chemosensory identification of snake predators (Phyllorhynchus decurtatus) by banded geckos (Coleonyx variegatus).Herpetol. 23:224–229.Google Scholar
  78. Díaz, J.A., andCarrascal, L.M. 1990. Prey size and food selection ofPsammodromus algirus (Lacertidae) in central Spain.J. Herpetol. 24:342–347.Google Scholar
  79. Dunham, A.E., Miles, D.B., andReznick, D.N. 1988. Life history patterns in squamate reptiles, pp. 441–522,in C. Gans and R.B. Huey (eds.). Biology of the Reptilia, Vol. 16, Ecology B: Defense and Life History. Alan R. Liss, New York.Google Scholar
  80. Dussault, M.H., andKrekorian, C.O. 1991. Conspecific discrimination by chemoreception in the desert iguana,Dipsosaurus dorsalis.Herpetologica 47:82–88.Google Scholar
  81. Duvall, D. 1979. Western fence lizard (Sceloporus occidentalis) chemical signals. I. Conspecific discriminations and release of a species-typical visual display.J. Exp. Zool. 210:321–326.Google Scholar
  82. Duvall, D. 1981. Western fence lizard (Sceloporus occidentalis) chemical signals. II. A replication with naturally breeding adults and a test of the Cowles and Phelan hypothesis of rattlesnake olfaction.J. Exp. Zool. 218:351–362.PubMedGoogle Scholar
  83. Duvall, D. 1982. Western fence lizard (Sceloporus occidentalis) chemical signals. III. An experimental ethogram of conspecific body licking.J. Exp. Zool. 221:23–26.Google Scholar
  84. Duvall, D., Müller-Schwarze, D., andSilverstein, R.M. 1986. Chemical Signals in Vertebrates 4: Ecology, Evolution, and Comparative Biology. Plenum Press, New York.Google Scholar
  85. Duvall, D., Chiszar, D., Hayes, W.K., Leonhardt, J.K., andGoode, M.J. 1990. Chemical and behavioral ecology of foraging in prairie rattlesnakes (Crotalus viridis viridis).J. Chem. Ecol. 16:87–101.Google Scholar
  86. Edroma, E.L., andSsali, W. 1983. Observations on the Nile monitor lizard (Varanus niloticus, L.) in Queen Elizabeth National Park, Uganda.Afr. J. Ecol. 21:197–201.Google Scholar
  87. Estes, R., De Queiroz, K., andGauthier, J. 1988. Phylogenetic relationships within Squamata, pp. 119–281,in R. Estes and G. Pregill (eds.). Phylogenetic Relationships of the Lizard Families. Stanford University Press, Stanford, California.Google Scholar
  88. Evans, L.T. 1961. Structure as related to behavior in the organization of populations of reptiles, pp. 148–178,in W.F. Blair (ed.). Vertebrate Speciation. University of Texas Press, Houston, Texas.Google Scholar
  89. Fellers, G.M., andDrost, C.A. 1991. Ecology of the island night lizard,Xantusia riversiana, on Santa Barbara Island.Herpetol. Monogr. 5:28–78.Google Scholar
  90. Ford, N.B. 1986. The role of pheromone trails in the sociobiology of snakes, pp. 261–278,in D. Duvall, D. Müller-Schwarze, and R.M. Silverstein (eds.). Chemical Signals in Vertebrates 4: Ecology, Evolution, and Comparative Biology. Plenum Press, New York.Google Scholar
  91. Fitch, H.S. 1935. Natural history of the alligator lizards.Trans. Acad. Sci. St. Louis 29:1–38.Google Scholar
  92. Fitch, H.S. 1954. Life history and ecology of the five-lined skink,Eumeces fasciatus.Univ. Kans. Publ. Mus. Nat. Hist. 8:1–156.Google Scholar
  93. Fitch, H.S. 1989. A field study of the slender glass lizard,Ophisaurus attenuatus, in northeastern Kansas.Occas. Pap. Mus. Nat. Hist. Univ. Kans. 125:1–50.Google Scholar
  94. Frost, D.R., andEtheridge, R. 1989. A phylogenetic analysis and taxonomy of iguanian lizards (Reptilia: Squamata).Misc. Publ. Univ. Kans. Mus. Nat. Hist. 81:1–65.Google Scholar
  95. Gabe, M., andSaint Girons, H. 1976. Contribution a la morphologie comparée des fosses nasales et de leurs annexes chez les lepidosauriens.Mem. Mus. Natl. Hist. Nat., Nouv. Ser. A 98:1–87 + 49 figs, 10 pl.Google Scholar
  96. Gauthier, J., Estes, R., andDe Queiroz, K. 1988. A phylogenetic analysis of Lepidosauromorpha, pp. 15–98,in R. Estes and G. Pregill (eds.). Phylogenetic Relationships of the Lizard Families. Stanford University Press, Stanford, California.Google Scholar
  97. Gillingham, J.C., andClark, D.L. 1981. Snake tongue-flicking: Transfer mechanics to Jacobson's organ.Can. J. Zool. 59:1651–1657.Google Scholar
  98. Gleeson, T.T. 1979. Foraging and transport costs in the Galapagos marine iguanas,Amblyrhynchus cristatus.Physiol. Zool. 52:549–557.Google Scholar
  99. Gleeson, T.T. 1981. Preferred body temperature, aerobic scope, and activity capacity in the monitor lizard,Varanus salvator.Physiol. Zool. 54:423–429.Google Scholar
  100. Goin, O.B. 1957. An observation of mating in the broad-headed skink,Eumeces laticeps.Herpetologica 13:155–156.Google Scholar
  101. Gomez, A., Font, E., andDesfilis, E. 1993. Chemoreception in the Lacertidae: exploration and conspecific discrimination in the Spanish wall lizard,Podarcis hispanica. Proceedings of First International Congress on Mediterranean Lacertids. In press.Google Scholar
  102. Gorniak, G.C., Rosenberg, H.I., andGans, C. 1982. Mastication in the tuatara,Sphenodon punctatus (Reptilia: Rhynchocephalia): Structure and activity of the motor system.J. Morphol. 171:321–353.Google Scholar
  103. Goosse, V., andBels, V.L. 1990. Analyse comportementale et fonctionelle des touchers linguaux lors de l'exploration et de la prise de nourriture chez le lézard vert (Lacerta viridis, Laurenti 1768).Bull. Soc. Herpetol. Fr. 53:31–39.Google Scholar
  104. Gove, D. 1979. A comparative study of snake and lizard tongue-flicking, with an evolutionary hypothesis.Z. Tierpsychol. 51:58–76.Google Scholar
  105. Gravelle, K., andSimon, C.A. 1980. Field observations on the use of the tongue-jacobson's organ system in two iguanid lizards,Sceloporus jarrovi andAnolis trinitatus.Copeia 1980:356–359.Google Scholar
  106. Graves, B.M., andHalpern, M. 1989. Chemical access to the vomeronasal organs of the lizardChalcides ocellatus.J. Exp. Zool. 249:150–157.PubMedGoogle Scholar
  107. Graves, B.M., andHalpern, M. 1990. Roles of vomeronasal chemoreception in tongue flicking, exploratory and feeding behaviour of the lizard,Chalcides ocellatus.Anim. Behav. 39:692–698.Google Scholar
  108. Graves, B.M., andHalpern, M. 1991. Discrimination of self from conspecific chemical cues inTiliqua Scincoides (Sauria: Scincidae).J. Herpetol. 25:125–126.Google Scholar
  109. Greenberg, B. 1943. Social behavior of the western banded gecko,Coleonyx variegatus Baird.Physiol. Zool. 16:110–122.Google Scholar
  110. Greenberg, N. 1985. Exploratory behavior and stress in the lizard,Anolis carolinensis.Z. Tierpsychol. 70:89–102.Google Scholar
  111. Halpern, M. 1992. Nasal chemical senses in reptiles: structure and function, pp. 423–523,in Biology of the Reptilia, Vol. 18, Brain, Hormones, and Behavior. C. Gans and D. Crews (eds.). University of Chicago Press, Chicago, Illinois.Google Scholar
  112. Halpern, M., andFrumin, N. 1979. Roles of the vomeronasal and olfactory systems in prey attack and feeding in adult garter snakes.Physiol. Behav. 22:1183–1189.PubMedGoogle Scholar
  113. Halpern, M., andKubie, J.L. 1980. Chemical access to the vomeronasal organs of garter snakes.Physiol. Behav. 24:367–371.PubMedGoogle Scholar
  114. Halpern, M., andKubie, J.L. 1983. Snake tongue flicking behavior: clues to vomeronasal system functions, pp. 45–72,in R.M. Silverstein and D. Müller-Schwarze (eds.). Chemical Signals in Vertebrates III. Plenum Press, New York.Google Scholar
  115. Heatwole, H. 1970. Thermal ecology of the desert dragonAmphibolurus inermis.Ecol. Monogr. 40:425–457.Google Scholar
  116. Henle, K. 1990. Population ecology and life history of three terrestrial geckos in arid Australia.Copeia 1990:759–781.Google Scholar
  117. Henle, K. 1991. Life history patterns in lizards of the arid and semiarid zone of Australia.Oecologia 88:347–358.Google Scholar
  118. Heterington, T.E. 1989. Use of vibratory cues for detection of insect prey by the sandswimming lizardScincus.Anim. Behav. 37:290–297.Google Scholar
  119. Hirth, H.F. 1963. The ecology of two lizards on a tropical beach.Ecol. Monogr. 33:83–112.Google Scholar
  120. Huey, R.B., andBennett, A.F. 1986. A comparative approach to field and laboratory studies in evolutionary biology, pp. 82–98,in M.E. Feder and G.V. Lauder (eds.). Predator-Prey Relationships: Perspectives and Approaches from the Study of Lower Vertebrates. University of Chicago Press, Chicago, Illinois.Google Scholar
  121. Huey, R.B., andPianka, E.R. 1981. Ecological consequences of foraging mode.Ecology 62:991–999.Google Scholar
  122. Iverson, J.B. 1979. Behavior and ecology of the rock iguanaCyclura carinata.Bull. Fla. State Mus. Biol. Sci. 24:175–358.Google Scholar
  123. James, C.D. 1991. Temporal variation in diets and trophic partitioning by coexisting lizards (Ctenotus: Scincidae) in central Australia.Oecologia 85:553–561.Google Scholar
  124. Jones, K.B. 1983. Movement patterns and foraging ecology of gila monsters (Heloderma suspectum Cope) in northwestern Arizona.Herpetologica 39:247–253.Google Scholar
  125. Kahmann, H. 1939. Uber das Jacobsonsche Organ der Echsen.Z. Vergl. Physiol. 26:669–695.Google Scholar
  126. Karges, J.P., andWright, J.W. 1987. A new species ofBarisia (Sauria, Anguidae) from Oaxaca, Mexico.Contrib. Sci. Nat. Hist. Mus. Los Angeles County 381:1–11.Google Scholar
  127. Kingsbury, B.A. 1989. Factors influencing activity inColeonyx variegatus.J. Herpetol. 23:399–404.Google Scholar
  128. Kluge, A.G. 1987. Cladistic relationships among the Gekkonoidea.Misc. Publ. Mus. Zool. Univ. Mich. 173:1–54.Google Scholar
  129. Krekorian, C.O. 1989. Field and laboratory observations on chemoreception in the desert iguana,Dipsosaurus dorsalis.J. Herpetol. 23:267–273.Google Scholar
  130. Lang, M. 1991. Generic relationships within the Cordyliformes (Reptilia: Squamata).Bull. Inst. R. Sci. Nat. Belg. Biol. 61:121–188.Google Scholar
  131. Lazell, J.D., Jr. 1973. The lizard genusIguana in the Lesser Antilles.Bull. Mus. Comp. Zool. 145:1–28.Google Scholar
  132. Loop, M.S., andScoville, S.A. 1972. Response of newbornEumeces inexpectatus to prey-object extracts.Herpetologica 28:254–256.Google Scholar
  133. Lopez, P., andSalvador, A. 1992. The role of chemosensory cues in discrimination of prey odors by the amphisbaenianBlanus cinereus.J. Chem. Ecol. 18:87–93.Google Scholar
  134. Magnusson, W.E., Paiva, L.J., Rocha, R.M., Franke, C.R., Kasper, L.A., andLima, A.P. 1985. The correlates of foraging mode in a community of Brazilian lizards.Herpetologica 41:324–332.Google Scholar
  135. Malan, M. 1946. Contributions to the comparative anatomy of the nasal capsule and the organ of Jacobson of the Lacertilia.Ann. Univ. Stellenbosch 24:69–137.Google Scholar
  136. Marchisin, A. 1980. Predator-prey interactions between snake-eating snakes and pit vipers. PhD dissertation. Rutgers University, Newark, University Microfilms number ADG80-20143.Google Scholar
  137. Mason, R.T. 1992. Reptilian pheromones, pp. 114–228,in C. Gans and D. Crews (eds.). Biology of the Reptilia, Vol. 18, Brain, Hormones, and Behavior. University of Chicago Press, Chicago, Illinois.Google Scholar
  138. Mason, R.T., andGutzke, W.H.N. 1990. Sex recognition in leopard gecko,Eublepharis macularius (Sauria: Gekkonidae): Possible mediation by skin-derived semiochemicals.J. Chem. Ecol. 16:27–36.Google Scholar
  139. Mautz, W.J., andNagy, K.A. 1987. Ontogenetic changes in diet, field metabolic rate, and water flux in the herbivorous lizardDipsosaurus dorsalis.Physiol. Zool. 60:640–658.Google Scholar
  140. McDowell, S.B. 1972. The evolution of the tongue of snakes, and its bearing on snake origins, pp. 191–273,in T. Dobzhansky, M.K. Hecht, and W.C. Steere (eds.). Evolutionary Biology, Vol. 6. Appleton-Century-Crofts, New York.Google Scholar
  141. McGovern, G.M., Mitchell, J.C., andKnisley, C.B. 1984. Field experiments on prey selection by the whiptail lizard,Cnemidophorus inornatus, in Arizona.J. Herpetol. 18:347–349.Google Scholar
  142. McLaughlin, R.L. 1989. Search modes of birds and lizards: Evidence for alternative movement patterns.Am. Nat. 133:654–670.Google Scholar
  143. Melcer, T., andChiszar, D. 1989. Striking prey creates a specific chemical search image in rattlesnakes.Anim. Behav. 37:477–486.Google Scholar
  144. Minnich, J.E., andShoemaker, V.H. 1970. Diet, behavior and water turnover in the desert iguana,Dipsosaurus dorsalis.Am. Midl. Nat. 84:496–509.Google Scholar
  145. Mitchell, D., Seely, M.K., Roberts, C.S., Pietruszka, R.D., McClain, E., Griffin, M., andYeaton, R.I. 1987. On the biology of the lizardAngolosaurus skoogi in the Namib Desert.Madoqua 15:201–216.Google Scholar
  146. Moermond, T.C. 1979. The influence of habitat structure onAnolis foraging behavior.Behaviour 70:147–167.Google Scholar
  147. Murray, G.W., andSchramm, D. 1987. A comparative study of the diet of the wedge-snouted sand lizard,Meroles cuneirostris (Strauch), and the sand diving lizard,Aporasaura anchietae (Bocage), (Lacertidae), in the Namib Desert.Madoqua 15:55–61.Google Scholar
  148. Murray, B.A., Bradshaw, S.D., andEdward, D.H. 1991. Feeding behavior and the occurrence of caudal luring in Burton's pygopodidLialis burtoni (Sauria: Pygopodidae.Copeia 1991:509–516.Google Scholar
  149. Nagy, K.A. 1973. Behavior, diet and reproduction in a desert lizard,Sauromalus obesus.Copeia 1973:93–102.Google Scholar
  150. O'Connell, B., Greenlee, R., andBacon, J. 1985. Strike-induced chemosensory searching in elapid snakes (cobras, taipans, tiger snakes, and death adders) at San Diego Zoo.Psychol. Rec. 35:431–436.Google Scholar
  151. Odendaal, F.J. 1979. Notes on the adaptive ecology and behaviour of four species ofRhotropus (Gekkonidae) from the Namib Desert with a special reference to a thermoregulatory mechanism employed byRhotropus afer.Madoqua 11:255–260.Google Scholar
  152. Paulissen, M.A. 1987. Optimal foraging and intraspecific diet differences in the lizardCnemidophorus sexlineatus.Oecologia 71:439–446.Google Scholar
  153. Perry, G., Lampl, I., Lerner, A., Rothenstein, D., Shani, E., Sivan, N., andWerner, Y.L. 1990. Foraging mode in lacertid lizards: variation and correlates.Amphibia-Reptilia 11:373–384.Google Scholar
  154. Peterson, C.C. 1990. Paradoxically low metabolic rate of the diurnal geckoRhotropus afer.Copeia 1990:233–237.Google Scholar
  155. Peterson, D.K., andWhitford, W.G. 1987. Foraging behavior ofUta stansburiana andCnemidophorus tigris in two different habitats.Southwest Nat. 32:427–433.Google Scholar
  156. Phillips, J.A., andAlberts, A.C. 1992. Naive ophiophagous lizards recognize and avoid venomous snakes using chemical cues.J. Chem. Ecol. 18:1775–1783.Google Scholar
  157. Pianka, E.R. 1968. Notes on the biology ofVaranus eremius.West. Austr. Nat. 11:39–44.Google Scholar
  158. Pianka, E.R. 1971. Notes on the biology ofVaranus tristis.West. Austr. Nat. 11:180–183.Google Scholar
  159. Pietruszka, R.D. 1986. Search tactics of desert lizards: how polarized are they?Anim. Behav. 34:1742–1758.Google Scholar
  160. Radcliffe, C.W., Chiszar, D., andO'Connell, B. 1980. Effects of prey size on poststrike behavior in rattlesnakesCrotalus durissus, C. enyo, andC. viridis.Bull. Psychon. Sci. 16:449–450.Google Scholar
  161. Regal, P.J. 1978. Behavioral differences between reptiles and mammals: an analysis of activity and mental capabilities, pp. 183–202,in B. Greenberg and P.D. MacLean (eds.). Behavior and Neurology of Lizards. United States Department of Health, Education, and Welfare, Washington, D.C.Google Scholar
  162. Regal, P.J. 1983. The adaptive zone and behavior of lizards, pp. 105–118,in R.B. Huey, E.R. Pianka, and T.W. Schoener (eds.). Lizard Ecology: Studies of a Model Organism. Harvard University Press, Cambridge, Massachusetts.Google Scholar
  163. Rica, J.P.M. 1982. Primeros datos sobre la población de lagart negro (Gallotia simonyi Steind.) de la Isla de Hierro.Amphibia-Reptilia 2:369–380.Google Scholar
  164. Schwenk, K. 1985. Occurrence, distribution, and functional significance of taste buds in lizards.Copeia 1985:91–101.Google Scholar
  165. Schwenk, K. 1986. Morphology of the tongue in the tuatara,Sphenodon punctatus (Reptilia, Lepidosauria), with comments on function and phylogeny.J. Morphol. 188:129–156.Google Scholar
  166. Schwenk, K. 1988. Comparative morphology of the lepidosaur tongue and its relevance to squamate phylogeny, pp. 569–598,in R. Estes and G. Pregill (eds.). Phylogenetic Relationships of the Lizard Families. Stanford University Press, Stanford, California.Google Scholar
  167. Schwenk, K. 1993. The evolution of chemoreception in squamate reptiles: A phylogenetic approach.Brain Behav. Evol. 41:124–137.PubMedGoogle Scholar
  168. Schwenk, K., andThrockmorton, G.S. 1989. Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics.J. Zool. (London) 219:153–175.Google Scholar
  169. Shenbrot, G.I., Rogovin, K.A., andSurov, A.V. 1991. Comparative analysis of spatial organization of desert lizard communities in middle Asia and Mexico.Oikos 61:157–168.Google Scholar
  170. Shine, R. 1986. Food habits, habitats and reproductive biology of four sympatric species of varanid lizards in tropicalAustralia.Herpetologica 42:346–360.Google Scholar
  171. Shine, R., andLambeck, R. 1989. Ecology of frillneck lizards,Chlamydosaurus kingii (Agamidae), in tropical Australia.Aust. Wildl. Res. 16:491–500.Google Scholar
  172. Shoji, T., andKurihara, K. 1991. Sensitivity and transduction mechanisms of responses to general odorants in turtle vomeronasal system.J. Gen. Physiol. 98:909–919.PubMedGoogle Scholar
  173. Siegel, S. 1956. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York.Google Scholar
  174. Simon, C.A., Gravelle, K., Bissinger, B.E., Eiss, I., andRuibal, R. 1981. The role of chemoreception in the iguanid lizardSceloporus jarrovi.Anim. Behav. 29:46–54.Google Scholar
  175. Stamps, J.A. 1977 Social behavior and spacing patterns in lizards, pp. 265–334,in C. Gans and D.W. Tinkle (eds.). Biology of the Reptilia, Vol. 7, Ecology and Behaviour A. Academic Press, London.Google Scholar
  176. Stamps, J.A. 1983. Sexual selection, sexual dimorphism, and territoriality, pp. 169–204,in R.B. Huey, E.R. Pianka, and T.W. Schoener (eds.). Lizard Ecology: Studies of a Model Organism. Harvard University Press, Cambridge, Massachusetts.Google Scholar
  177. Stamps, J.A. 1987. Conspecifics as cues to territory quality: A preference of juvenile lizards (Anolis aeneus) for previously used territories.Am. Nat. 129:629–642.Google Scholar
  178. Stebbins, R.C., andBarwick, R.E. 1968. Radiotelemetric study of thermoregulation in a lace monitor.Copeia 1968:541–547.Google Scholar
  179. Stoddart, D.M. 1980. Olfaction in Mammals. Academic Press, New York.Google Scholar
  180. Sylber, C.K. 1988. Feeding habits of the lizardsSauromalus varius andS. hispidus in the Gulf of California.J. Herpetol. 22:413–424.Google Scholar
  181. Thoen, C., Bauwens, R., andVerheyen, R. 1986. Chemoreceptive and behavioural responses of the common lizardLacerta vivipara to snake chemical deposits.Anim. Behav. 34:1805–1813.Google Scholar
  182. Tinkle, D.W. 1967. The life and demography of the side-blotched Lizard,Uta stansburiana.Misc. Publ. Mus. Zool., Univ. Mich. 132:1–182.Google Scholar
  183. Trillmich, K.G.K., andTrillmich, F. 1986. Foraging strategies of the marine iguana,Amblyrhynchus cristatus Behav. Ecol. Sociobiol. 18:259–266.Google Scholar
  184. Underwood, G. 1970. The eye, pp. 1–97,in C. Gans and T.S. Parsons (eds.). Biology of the Reptilia, Vol. 2, Morphology B. Academic Press, London.Google Scholar
  185. Van Damme, R., Bauwens, D., Vanderstighelen, D., andVerheyen, R.F. 1990a. Responses of the lizardLacerta vivipara to predator chemical cues: The effects of temperature.Anim. Behav. 40:298–305.Google Scholar
  186. Van Damme, R., Bauwens, D., Castilla, A.M., andVerheyen, R.F. 1990b. Comparative thermal ecology of the sympatric lizardsPodarcis tiliguerta andPodarcis sicula.Acta Oecol. 11:503–512.Google Scholar
  187. Van Damme, R., Bauwens, D., andVerheyen, R.F. 1991. The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizardLacerta vivipara Jacquin.Funct. Ecol. 5:507–517.Google Scholar
  188. Van Devender, R.W. 1982. Growth ecology of spiny-tailed and green iguanas in Costa Rica, with comments on the evolution of herbivory and large body size, pp. 162–183,in G.M. Burghardt and A.S. Rand (eds.). Iguanas of the World: Their Behavior, Ecology, and Conservation. Noyes, Park Ridge, New Jersey.Google Scholar
  189. Vernet, R.C., Grenot, C., andNouira, S. 1988. Flux hydriques et métabolisme énergétiques dans un peuplement de lacertidés des îles Kerkennah (Tunisie).Can. J. Zool. 66:555–561.Google Scholar
  190. Vitt, L.J. 1990. The influence of foraging mode and phylogeny on seasonality of tropical lizard reproduction.Pap. Avulsos Zool. Mus. Zool. Univ. Sao Paulo 37:107–123.Google Scholar
  191. Vitt, L.J. 1991. Ecology and life history of the scansorial arboreal lizardPlica plica (Iguanidae) in Amazonian Brazil.Can. J. Zool. 69:504–511.Google Scholar
  192. Vitt, L.J., andCongdon, J.D. 1978. Body shape, reproductive effort, and relative clutch mass in lizards.Am. Nat. 112:595–608.Google Scholar
  193. Vitt, L.J., andCooper, W.E., Jr. 1986. Foraging and diet of a diurnal predator (Eumeces laticeps) feeding on hidden prey.J. Herpetol. 20:408–415.Google Scholar
  194. Vitt, L.J., andPrice, H. 1982. Ecological and evolutionary determinants of relative clutch mass in lizards.Herpetologica 38:237–255.Google Scholar
  195. Vogel, P. 1979. Zur biologie des bindenwarans (Varanus salvator) im Westjavanischen naturschutzdebiet Ujung Kulon. PhD dissertation. University of Basel, Basel, Switzerland.Google Scholar
  196. Walls, G.Y. 1981. Feeding ecology of the tuatara (Sphenodon punctatus) on Stephens Island, Cook Strait.N. Zl. J. Ecol. 4:89–97.Google Scholar
  197. Walls, G.Y. 1983. Activity of the tuatara and its relationships to weather conditions on Stephens Island, Cook Strait, with observations on geckos and invertebrates.N. Zl. J. Zool. 10:309–318.Google Scholar
  198. Webb, J.K., andShine, R. 1992. To find an ant: trail-following in Australian blindsnakes (Typhlopidae).Anim. Behav. 43:941–948.Google Scholar
  199. Weldon, P.J. 1982. Responses to ophiophagous snakes by snakes of the genusThamnophis.Copeia 1982:788–794.Google Scholar
  200. Werner, D.I., Baker, E.M., Gonzales, E.C., andSosa, I.R. 1987. Kinship recognition and grouping in hatchling green iguanas.Behav. Ecol. Sociobiol. 21:83–89.Google Scholar
  201. Young, B.A. 1990. Is there a direct link between the ophidian tongue and Jacobson's organ?Amphibia-Reptilia 11:263–276.Google Scholar

Copyright information

© Plenum Publishing Corporation 1994

Authors and Affiliations

  • William E. Cooper
    • 1
  1. 1.Department of BiologyIndiana University-Purdue University at Fort WayneFort Wayne

Personalised recommendations