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10 - Prey capture and prey processing behavior and the evolution of lingual and sensory characteristics: divergences and convergences in lizard feeding biology

Published online by Cambridge University Press:  04 August 2010

Stephen M. Reilly
Affiliation:
Program in Ecology and Evolutionary Biology Department of Biological Sciences Ohio University
Lance D. McBrayer
Affiliation:
Department of Biology Georgia Southern University
Stephen M. Reilly
Affiliation:
Ohio University
Lance B. McBrayer
Affiliation:
Georgia Southern University
Donald B. Miles
Affiliation:
Ohio University
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Summary

Introduction

Prey location, capture, and subsequent processing are fundamentally important behaviors critical to the assimilation of food resources. All three of these behaviors involve movements of the tongue and jaws and it is well known that both tongue movements and tongue morphology vary widely among lizards (Schwenk, 2000). A central element of the sit-and-wait (ambush) vs. wide foraging paradigm involves the trade-off between prey capture function and chemosensory acuity. In general, ambush feeders are thought to use the tongue primarily to capture prey located visually, whereas wide foragers are thought to have traded tongue-based prey capture for tongue-flicking, which is critical to locating widely dispersed prey by using chemoreception (Pianka and Vitt, 2003; Cooper, 1997a). The switch to chemosensory tongue function among scleroglossan lizards is certainly linked to their wide-foraging strategy; in fact, this transition has enabled wide foragers to dominate lizard communities worldwide (Vitt et al., 2003). In this chapter we examine the trade-off between feeding behaviors (prey capture and subsequent prey processing) and chemosensory function in lizards with data available to date. First, we present new data and a review of kinematic patterns of “prey capture” behaviors. This analysis illustrates three basic prey capture modes used by lizards. Next, we review patterns of post-capture prey processing behavior that reveal three evolutionary transitions in lizard “chewing” behavior. Finally, we compare changes in lizard feeding behavior with quantified characteristics of the vomeronasal system, tongue morphology, prey discrimination ability, and foraging behavior from the literature to examine how changes in feeding function correlate with changes in chemosensory function.

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Lizard Ecology , pp. 302 - 333
Publisher: Cambridge University Press
Print publication year: 2007

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References

Archie, J. W. (1985). Methods for coding variable morphological features for numerical taxonomic analysis. Syst. Zool. 34, 326–45.CrossRefGoogle Scholar
Bels, V. L. (2003) Evaluating the complexity of the trophic system in Reptilia. In Vertebrate Biomechanics and Evolution, ed. Bels, V. L., Gasc, J. P and Casinos, A., pp. 185–202. Oxford: Bios Scientific Publishers.Google Scholar
Bels, V. L. and Goosse, V. (1990). Comparative kinematic analysis of prey capture in Anolis carolinensis (Iguania) and Oplurus cuvieri (Oplurinae). Belg. J. Zool. 122, 223–34.Google Scholar
Bels, V. L., Chardon, M. and Kardong, K. (1994). Biomechanics of the hyolingual system in Squamata. In Biomechanics of Feeding in Vertebrates, ed. Bels, V. L., Chardon, M. and Vandewalle, P. (Adv. Comp. Environ. Physiol., vol. 18.), pp. 197–240. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Bels, V. L., Davenport, J. and Renous, S. (1997). Kinematic analysis of the feeding behavior in the box turtle Terrepene carolina (Reptilia: Emydidae). J. Exp. Biol. 277, 198–212.Google Scholar
Cleuren, J. and De Vree, F. (2000). Feeding in Crocodilia. In Feeding, ed. Schwenk, K., pp. 337–58. New York: Academic Press.Google Scholar
Cooper, W. E. (1990). Prey odor discrimination by anguid lizards. Herpetologica 46, 183–90.Google Scholar
Cooper, W. E. (1994a). Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. J. Chem. Ecol. 20, 439–87.CrossRefGoogle Scholar
Cooper, W. E. (1994b). Prey chemical discrimination, foraging mode, and phylogeny. In Lizard Ecology, ed. Vitt, L. J. and Pianka, E. R., pp. 95–116. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Cooper, W. E. (1995a). Foraging mode, prey chemical discrimination, and phylogeny in lizards. Anim. Behav. 50, 973–85.CrossRefGoogle Scholar
Cooper, W. E. (1995b) Evolution and function of lingual shape in lizards, with emphasis on elongation, extensibility, and chemical sampling. J. Chem. Ecol. 21, 477–505.CrossRefGoogle Scholar
Cooper, W. E. (1995c). Prey chemical discrimination and foraging mode in gekkonid lizards. Herpetol. Monogr. 9, 120–9.CrossRefGoogle Scholar
Cooper, W. E. (1996). Variation and evolution of forked tongues in squamate reptiles. Herp. Nat. Hist. 4, 135–50.Google Scholar
Cooper, W. E. (1997a). Correlated evolution of prey chemical discrimination with foraging, lingual morphology and vomeronasal chemoreceptor abundance in lizards. Behav. Ecol. Sociobiol. 41, 257–65.CrossRefGoogle Scholar
Cooper, W. E. (1997b). Independent evolution of squamate olfaction and vomerolfaction and correlated evolution of vomerolfaction and lingual structure. Amph.-Rept. 18, 85–105.CrossRefGoogle Scholar
Cooper, W. E. and Wyck, J. H. (1994). Absence of prey chemical discrimination by tongue flicking in an ambush-foraging lizard having actively foraging ancestors. Ethology 97, 317–28.CrossRefGoogle Scholar
Cooper, W. E. and Habegger, J. J. (2000). Lingual and biting responses to food chemicals by some eublepharid and gekkonid geckos. J. Herpetol. 34, 360–8.CrossRefGoogle Scholar
Delheusy, V. G. and Bels, V. L. (1992). Kinematics of feeding behavior in Oplurus cuvieri (Reptilia: Iguanidae). J. Exp. Biol. 170, 155–86.Google Scholar
Delheusy, V. G. and Bels, V. L. (2000). Kinematics of feeding of Phelsuma madagascariensis (Reptilia: Gekkonidae). J. Exp. Biol. 202, 3715–30.Google Scholar
Delheusy, V., Brillet, C. and Bels, V. L. (1995). Etude cinématique de la prise de nourriture che Eublepharis macularis (Reptilia: Gekkota) et comparison au sien des geckos. Amph.-Rept. 15, 185–201.CrossRefGoogle Scholar
Delheusy, V., Toubeau, G. and Bels, V. L. (1994). Tongue structure and function in Oplurus cuvieri (Reptilia: Iguanidae). Anat. Rec. 238, 263–76.CrossRefGoogle Scholar
Dunham, A. E., Miles, D. B. and Reznick, D. N. (1988). Life history patterns in squamate reptiles. In Biology of the Reptilia, vol. 16, ed. Gans, C. and Huey, Ray, pp. 441–519 New York: A. R. Liss.Google Scholar
Elias, J. A., McBrayer, L. D. and Reilly, S. M. (2000). Prey transport kinematics in Tupinambis teguixin and Varanus exanthematicus: conservation of feeding behavior in ‘chemosensory-tongued’ lizards. J. Exp. Biol. 203, 791–801.Google ScholarPubMed
Estes, R., de Queiroz, K. and Gauthier, J. (1988). Phylogenetic relationships within Squamata. In Phylogenetic Relationships of the Lizard Families: Essays Commemorating Charles L. Camp, ed Estes, R. and Pregill, G., pp. 119–281. Stanford, CA: Stanford University Press.Google Scholar
Fellers, G. M. and Drost, C. A. (1991). Ecology of the island night lizard, Xantusia riversiana, on Santa Barbara Island, California. Herp. Monogr. 5, 28–78.CrossRefGoogle Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1–15.CrossRefGoogle Scholar
Gabe, M. and Girons, Saint H. (1976). Contribution à la morphologie comparée des fosses nasales et des leurs annexes chez les lépidosoriens. Mem. Natl. Mus. Nat. Hist. Paris A98, 1–87.Google Scholar
Gans, C. (1969). Comments on inertial feeding. Copeia 1969, 855–7.CrossRefGoogle Scholar
Gans, C., Vree, F. and Carrier, D. (1985). Usage pattern of the complex masticatory muscles in the shingleback lizard, Trachydosaurus rugosus: a model for muscle placement. Am. J. Anat. 173, 219–40.CrossRefGoogle ScholarPubMed
Gorniak, G. C., Rosenberg, H. I. and Gans, C. (1982). Mastication in the tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia): structure and activity of the motor system. J. Morphol. 171, 321–53.CrossRefGoogle Scholar
Goosse, V. and Bels, V. L. (1992). Kinematic and functional analysis of feeding behavior in Lacerta viridia (Reptilia: Lacertidae). Zool. Jb. Anat. 122, 187–202.Google Scholar
Gove, D. (1979). A comparative study of snake and lizard tongue flicking with an evolutionary hypothesis. Z. Tierpsychol. 51, 58–76.CrossRefGoogle Scholar
Herrel, A., Cleuren, J. and Vree, F. (1995). Prey capture in the lizard Agama stellio. J. Morphol. 224, 313–29.CrossRefGoogle Scholar
Herrel, A., Meyers, J. M., Aerts, P. and Nishikawa, K. C. (2001). Functional implications of supercontracting muscle in the chameleon tongue retractors. J. Exp. Biol. 204, 3621–37.Google ScholarPubMed
Herrel, A., Timmermans, J.-P. and Vree, F. (1998). Tongue flicking in agamid lizards: morphology, kinematics, and muscle activity patterns. Anat. Rec. 252, 102–16.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Herrel, A., Verstappen, M. and Vree, F. (1999). Modulatory complexity of the feeding repertoire in scincid lizards. J. Comp. Physiol. A184, 501–18.CrossRefGoogle Scholar
Hillenius, W. J. and Rehorek, S. J. (2001). Eyes to nose: the Harderian gland as part of the vomeronasal system. J. Morphol. 248, 240.Google Scholar
Kraklau, D. M. (1991). Kinematics of prey capture and chewing in the lizard Agama agama. J. Morphol. 210, 195–212.CrossRefGoogle Scholar
Lee, M. S. Y. (1998). Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships. Biol. J. Linn. Soc. 65, 369–453.CrossRefGoogle Scholar
Martins, E. P. and Hansen, T. F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into analysis of interspecific data. Am. Nat. 149, 646–67.CrossRefGoogle Scholar
McBrayer, L. D. (2004). The relationship between skull morphology, biting performance and foraging mode in Kalahari lacertid lizards. Zool. J. Linn. Soc. 140, 403–16.CrossRefGoogle Scholar
McBrayer, L. D. and Reilly, S. M. (2002). Prey processing in lizards: behavioral variation in sit-and-wait and widely foraging taxa. Can. J. Zool. 80, 882–92.CrossRefGoogle Scholar
McDowell, S. B. (1972). The evolution of the tongue of snakes, and its bearing on snake origins. In Evolutionary Ecology, vol. 6. ed. Dobzhansky, T., Hecht, M. K. and Steere, W. C., pp. 191–273. New York: Appleton-Century-Crofts.Google Scholar
Meyers, J. J., Herrel. A. and Birch, J. (2002). Scaling of morphology, bite force, and feeding kinematics in an iguanian and a scleroglossan lizard. In Topics in Functional and Ecological Vertebrate Morphology, ed. Aerts, P., D'Aout, K., Herrel, A. and Damme, R., pp. 47–62. New York: Shaker Publishing.Google Scholar
Nishikawa, K. C. (2000) Feeding in frogs. In Feeding, ed. Schwenk, K., pp. 117–47. New York: Academic Press.Google Scholar
O'Reilly, J. C. (2000). Feeding in caecilians. In Feeding, ed. Schwenk, K., pp. 149–66. New York: Academic Press.Google Scholar
Perry, G. (1999). The evolution of search modes: ecological versus phylogenetic perspectives. Am. Nat. 153, 98–109.CrossRefGoogle ScholarPubMed
Pianka, E. R. and Vitt, L. J. (2003). Lizards: Windows to the Evolution of Diversity. Berkeley, CA: University of California Press.Google Scholar
Rehorek, S. J., Hillenius, W. J., Quan, W. and Halpern, M. (1999). Keeping an eye on the nose: the Harderian gland is part of the VN system. Am. Zool. 39, 96A.Google Scholar
Rehorek, S. J., Hillenius, W. J., Quan, W. and Halpern, M. (2000). Passage of Harderian gland secretions to the vomeronasal organ of Thamnophis sirtalis (Serpentes: Colubridae). Can. J. Zool. 78, 1284–8.CrossRefGoogle Scholar
Reilly, S. M. and Lauder, G. V.. (1989). Kinetics of tongue projection in Ambystoma tigrinum: quantitative kinematics, muscle function, evolutionary hypotheses. J. Morphol. 199, 223–43.CrossRefGoogle Scholar
Reilly, S. M., McBrayer, L. D. and White, T. D. (2001). Prey processing in amniotes: biomechanical and behavioral patterns of food reduction. Comp. Biochem. Physiol. A128, 397–415.CrossRefGoogle Scholar
Schwenk, K. (1986). Morphology of the tongue in tuatara, Sphenodon punctatus (Reptilia: Lepidosauria), with comments on function and phylogeny. J. Morphol. 188, 129–56.CrossRefGoogle Scholar
Schwenk, K. (1988). Comparative morphology of the lepidosaur tongue and its relevance to squamate phylogeny. In Phylogenetic Relationships of the Lizard Families: Essays Commemorating Charles L. Camp, ed. Estes, R. and Pregill, G., pp. 569–97. Stanford, CA: Stanford University Press.Google Scholar
Schwenk, K. (1993) The evolution of chemoreception in squamate reptiles: a phylogenetic approach. Brain Behav. Evol. 41, 124–37.CrossRefGoogle ScholarPubMed
Schwenk, K. (1994). Why snakes have forked tongues. Science 263, 1573–7.CrossRefGoogle ScholarPubMed
Schwenk, K. (1995). Of tongues and noses: chemoreception in lizards and snakes. Trends Ecol. Evol. 10, 7–12.CrossRefGoogle ScholarPubMed
Schwenk, K. (2000). Feeding in lepidosaurs. In Feeding, ed. Schwenk, K., pp. 175–291. New York: Academic Press.Google Scholar
Schwenk, K. and Bell, D. A. (1988). Chameleon-like tongue protrusion in an agamid lizard. Experientia 44, 697–700.CrossRefGoogle Scholar
Schwenk, K. and Throckmorton, G. S. (1989). Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics. J. Zool. Lond. 219, 153–75.CrossRefGoogle Scholar
Schwenk, K. and Wagner, G. P. (2001). Function and the evolution of phenotypic stability: connecting pattern to process. Am. Zool. 41, 552–63.Google Scholar
Smith, K. K. (1984). The use of the tongue and hyoid apparatus during feeding in lizards (Ctenosaura similis and Tupinambis nigropunctatus). J. Zool. Lond. 202, 115–43.CrossRefGoogle Scholar
Smith, K. K. (1988). Form and function of the tongue in agamid lizards with comments on its significance. J. Morphol. 196, 157–71.CrossRefGoogle ScholarPubMed
Smith, K. K. and Kier, W. M. (1989). Trunks, tongues, and tentacles: moving with skeletons of muscle. Am. Sci. 77, 29–35.Google Scholar
Smith, T. L., Kardong, K. V. and Bels, V. L. (1999). Prey capture behavior in the blue-tongued skink, Tiliqua scincoides. J. Herpetol. 33, 362–9.CrossRefGoogle Scholar
Urbani, J.-M. and Bels, V. L. (1995). Feeding behaviour in two scleroglossan lizards: Lacerta viridis (Lacertidae) and Zonosaurus laticaudatus (Cordylidae). J. Zool. Lond. 236, 265–90.CrossRefGoogle Scholar
Vitt, L. J. and Pianka, E. R. (2005). Deep history impacts present day ecology and biodiversity. Proc. Nat. Acad Sci. USA 102, 7877–81.CrossRefGoogle ScholarPubMed
Vitt, L. J., Pianka, E. R., Cooper, W. E. and Schwenk, K. (2003). History and the global ecology of squamate reptiles. Am. Nat. 162, 44–60.CrossRefGoogle ScholarPubMed
Wagner, G. P. and Schwenk, K. (2000). Evolutionary stable configurations: functional integration and the evolution of phenotypic stability. Evol. Biol. 31, 155–217.Google Scholar
Walls, G. Y. (1981). Feeding ecology of the tuatara (Sphenodon punctatus) on Stephens Island, Cook Strait. New Zealand J. Ecol. 4, 89–97.Google Scholar

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