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Biomechanics of the Hyolingual System in Squamata

  • V. L. Bels
  • M. Chardon
  • K. V. Kardong
Part of the Advances in Comparative and Environmental Physiology book series (COMPARATIVE, volume 18)

Abstract

The hyolingual system of Squamata is a highly versatile system used in different feeding, drinking, chemoreception, and social behaviors. In each of these activities, either the entire hyolingual system or one of its elements is used. For instance, in the majority of lizards, the tongue acts as the main element for liquid uptake, intraoral food and liquid transport, and in chemoreception, whereas the hyoid apparatus plays a major role during social interactions by acting on the ventral floor of the throat. In varanids, the hyoid apparatus is involved in both deglutition of foods and liquids, and during social displays.

Keywords

Prey Capture Buccal Cavity Tongue Protrusion Garter Snake Tongue Flick 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Altevogt R, Altevogt R (1954) Studien zur Kinematik der Chamäleonenzunge. Z Vergl Physiol 36: 66–77Google Scholar
  2. Auffenberg W (1972) Komodo dragons. Nat Hist 81: 52–59Google Scholar
  3. Auffenberg W (1978) Social and feeding behavior in Varanus komodoensis. In: Greenberg N, Mac Lean PD (eds) Behavior and neurology of lizards. Nimh, Bethesda, pp 301–331Google Scholar
  4. Auffenberg W (1981) The behavioral ecology of the Komodo monitor. University of Florida Press, GainesvilleGoogle Scholar
  5. Avery DF, Tanner WW (1971) Evolution of the iguanine lizards (Sauria, Iguandiae) as determined by osteological and myological characters. Brigham Young Univ Sci Bull 3: 1–71Google Scholar
  6. Avery DF, Tanner WW (1982) Buccal floor of reptiles, a summary. Great Basin Nat 42: 273–349Google Scholar
  7. Bell D (1984) Tongue use and prey capture in chameleons. Am Zool 24: 108AGoogle Scholar
  8. Bell D (1987) Identification of perikarya in the chameleon tongue. Proc Ord Gen Meet Soc Eur Herpetol Nijmegen 4: 63–66Google Scholar
  9. Bell D (1989) Functional anatomy of the chameleon tongue. Zool Jahrb Anat 119: 313–336Google Scholar
  10. Bell D (1990) Kinematics of prey capture in the chameleon. Zool Jahrb Physiol 94: 247–260Google Scholar
  11. Bell T (1826) Observation sur la structure du gosier du genre Anolis. Ann Sci Nat 7: 191–195Google Scholar
  12. Bels VL (1990a) Quantitative analysis of prey-capture kinematics in Anolis equestris (Reptilia: Iguanidae). Can J Zool 68: 2192–2198Google Scholar
  13. Bels VL (1990b) The mechanism of dewlap extension in Anolis carolinensis (Reptilia; Iguaniade) with histological analysis of the hyoid apparatus. J Morphol 206: 225–244Google Scholar
  14. Bels VL (1992) Functional analysis of the ritualized behaviuoral motor pattern in lizards: evolution of behavior and the concept of ritualization. Zool Jahrb 122: 2141–2159Google Scholar
  15. Bels VL, Baltus I (1987) First analysis of the feeding sequence of Chameleo dilepis. Proc Ord Gen Meet Soc Eur Herpetol Nijmegen 4: 67–70Google Scholar
  16. Bels VL, Baltus I (1989) First analysis of feeding in Anolis lizards. In: Splechtna H, Hilgers H (eds) Fortschritte der Zoologie/Progress in Zoology, Band/vol 35. Trends in vertebrate morphology. Fischer, Stuttgart, pp 141–145Google Scholar
  17. Bels VL, Goosse V (1989) A first report of relative movements within the hyoid apparatus during feeding in Anolis equestris (Reptilia: Iguanidae). Experientia 45: 1088–1091Google Scholar
  18. Bels VL, Goosse V (1990) Comparative kinematic analysis of prey capture in Anolis carolinensis 1 (Iguania) and Lacerta viridis (Scleroglossa). J Exp Zool 255: 120–124Google Scholar
  19. Bels VL, Goosse V, Kardong K (1992) Kinematic analysis of drinking by the lacertid lizard, Lacerta viridis (Squamates, Scleroglossa). J Zool Lond 229: 659–682Google Scholar
  20. Brücke E (1872) Über de Zunge des Chameleonen. Sitzungsber Math-Nat Kl Akad Wiss Wien 8: 62–70Google Scholar
  21. Burghardt GM (1970) Chemical perception in reptiles. In: Johnson JW, Moulton DG, Turk A (eds) Advances in chemoreeeption. Communication by chemical signals, vol 1. Appleton-Century-Cropts, New York, pp 241–308Google Scholar
  22. Burghardt GM (1990) Chemically mediated predation in vertebrates: diversity, ontogeny, and information. In: Macdonald DW, Müller-Schwarze D, Natynczuk S (eds) Chemical signals in vertebrates. Oxford University Press, New York, pp 475–499Google Scholar
  23. Camp CL (1923) Classification of the lizards. Bull Am Mus Nat Hist 48: 289–481Google Scholar
  24. Carpenter CC (1978) Ritualistic social behaviors in lizards. In: Greenberg N, Mac Lean (eds) Behavior and neurology of lizards. Nimh, Rockville, pp 253–267Google Scholar
  25. Carpenter CC, Ferguson GW (1977) Variation and evolution of stereotyped behavior in reptiles. In: Gans C, Tinkle DW (eds) Biology of Reptilia, vol 7. Ecology and behavior A. Academic Press, London, pp 335–554Google Scholar
  26. Chemin A (1899) L’appareil hyoïdien et son fonctionnement chez Calotes versicolor. Note pour servir à l’étude de l’anatomie comparée de l’os hyoïde. Bibl Anat 7: 114–123Google Scholar
  27. Chiszar D, Scudder K, Kinght L (1976) Rate of tongue flicking by garter snakes (Thamnophis radix haydeni) and rattlesnakes (Crotalus v. viridis, Sistrurus catenatus tergeminus, and Sistrurus catenatus edwardsi) during prolonged exposure to food odors. Behave Biol 18: 273–283Google Scholar
  28. Chiszar D, Radcliffe CW, Scudder KM (1977) Analysis of the behavioral sequence emitted by rattlesnakes during feeding episodes. I. Striking and chemosensory searching. Behav Biol 21: 418–425Google Scholar
  29. Chiszar D, Radcliffe DW, Scudder KM, Duvall D (1983) Strike-induced chemosensory searching by rattlesnakes: the role of envenomation-related chemical cues in the post-strike environment. In: Müller-Schwarze D, Silverstein RM (eds) Chemical signals III. Plenum Press, New York, pp 1–24Google Scholar
  30. Chiszar D, Melcer T, Lee R, Radcliffe CW, Duvale D (1990) Chemical cues used by prairie rattlesnakes (Crotalus viridis) as they follow the trail of rodent prey. J Chem Ecol 16: 79–86Google Scholar
  31. Cooper WE (1989) Strike-induced chemosensory searching occurs in lizards. J. Chem Ecol 15(4): 1311–1320Google Scholar
  32. Cooper WE (1990a) Prey odour discrimination by lizards and snakes. In: Macdonald DW, Müller-Schwarze D, Natynczuk SE (eds) Chemical signals in vertebrates. Oxford University Press, New York, pp 533–538Google Scholar
  33. Cooper WE (1990b) Prey odor detection by teiid and lacertid lizards and the relationship of prey odor detection to foraging mode in lizard families. Copeia 1990: 237–242Google Scholar
  34. Cooper WE, Burghardt GM (1990) Vomerolfaction and vomodor. J Chem Ecol 16: 103–105Google Scholar
  35. Cundall D (1987) Functional morphology. In: Seigel RA, Collins JT, Novak SS (eds) Snakesecology and evolutionary biology. Macmillan, New York, pp 106–142Google Scholar
  36. Cundall D, Gans C (1979) Feeding in water snakes: an electromyographic study. J Exp Zool 209: 189–208Google Scholar
  37. Delheusy V, Bels VL (1992) Kinematics of feeding behaviour in Opiums cuvieri (Reptilia: Iguanidae). J Exp Biol 170: 155–186Google Scholar
  38. Duvall D, Chiszar D (1990) Behavioural and chemical ecology of vernal migration and pre and post-strike predatory activity in prairie rattlesnakes: field and laboratory experiments. In: Macdonald DW, Müller-Schwarz D, Natynczuk SE (eds) Chemical signals in vertebrates 5. Oxford University Press, New York, pp 539–554Google Scholar
  39. Duvall D, Müller-Schwarze D, Silverstein RM (1986) Chemical signals in vertebrates 4: ecology, evolution and comparative biology. Plenum Press, New YorkGoogle Scholar
  40. Duvernoy GL (1836) Sur les mouvements du la langue de chameleon. C R Hebd Séanc Acad Sci Paris 2: 349–351Google Scholar
  41. El-Toubi MR (1947) Some observations on the osteology of Uromastix aegyptia (Forskai). Bull Fac Sci Cairo Fouas I Univ 25: 1–10Google Scholar
  42. Estes R, Pregill G (1988) Phylogenetic relationships of the lizard families. Stanford Univ Press, StanfordGoogle Scholar
  43. Font E, Kramer M (1989) A multivariate clustering approach to display repertoire analysis: head-bobbing in Anolis equestris (Sauria, Iguanidae). Amphib-Reptilia 10: 331–344Google Scholar
  44. Font E, Rome LC (1990) Functional morphology of dewlap extension in the lizard Anolis equestris (Iguanidae). J Morphol 206 (1990): 245–258PubMedGoogle Scholar
  45. Frazzetta TH (1966) Studies on the morphology and function of the skull in the Boidae (Serpentes). Part II. Morphology and function of the jaw apparatus in Python sebae and Python molurus. J Morphol 118: 217–296PubMedGoogle Scholar
  46. Gandolfi H (1908) Der Zunge der Agamidae und Iguanidae. Zool Anz 32: 56Google Scholar
  47. Gans C (1967) The chameleon. Nat Hist 76: 52–59Google Scholar
  48. Gillingham JC, Clark: DL (1981a) Snake tongue-flicking: transfer mechanism to Jacobson’s organ. Can J Zool 59: 1651–1657Google Scholar
  49. Gillingham JC, Clark DL (1981b) An analysis of prey-searching behavior in the western diamondback rattlesnake, Crotalus atrox. Behav Neural Biol 32: 235–240Google Scholar
  50. Gnanamuthu CP (1930a) The anatomy and mechanism of the tongue of Chamaeleon cararatus. Proc Zool Soc Lond Part II: 467–486Google Scholar
  51. Gnanamuthu CP (1930b) The mechanism of the throat-fan in a ground lizards, Sitana ponticeriana. Cuv Rec Ind Mus 32: 149–159Google Scholar
  52. Gnanamuthu CP (1937) Comparative study of the hyoid and tongue of some typical genera of reptiles. Proc Zool Soc B: 1–66Google Scholar
  53. Graves BM, Halpern M (1990) Roles of vomeronasal organ chemoreception in tongue flicking exploratory and feeding behaviour of the lizard, Chalcides ocellatus. Anim Behav 39: 692–698Google Scholar
  54. Goosse V, Bels VL (1990) Analyse comportementale et fonctionnelle des touchers linguaux lors de l’exploration et de la prise de nourriture chez le lézard vert (Lacerta viridis Laurenti 1768). Bull Soc Herp Fr 53: 31–33Google Scholar
  55. Goosse V, Bels VL (1992a) Kinematic and functional analysis of feeding behaviour in Lacerta viridis (Reptilia: Lacertidae). Zool Jahrb 122: 187–202Google Scholar
  56. Goosse V, Bels VL (1992b) Tongue movements during chemosensory behavior in the European green lizard Lacerta viridis. Can J Zool 70: 1886–1896Google Scholar
  57. Gorniak GC, Rosenberg HI, Gans C (1982) Mastication in the tuatara Sphenodon punctatus (Reptilia: Rhynchocephalia): structure and activity of the motor system. J Morphol 171: 321–353Google Scholar
  58. Gorman GC (1968) The relationships of Anolis of the roquet species group (Sauria: Iguanidae): Comparative study of display behavior. Breviora 284: 1–31Google Scholar
  59. Gove D (1979) A comparative study of snake and lizard tongue-flicking with an evolutionary hypothesis. Z Tierpsychol 51: 58–76Google Scholar
  60. Graves BM, Halpern M (1989) Chemical access to the vomeronasal organs of the lizard Chalcides ocellatus. J Exp Zool 249: 150–157PubMedGoogle Scholar
  61. Greenberg N (1977) A neuroethological study of the display behavior in the lizard Anolis carolinensis (Sauria Iguanidae). Am Zool 17: 191–201Google Scholar
  62. Greene HW (1982) Dietary and phenotypic diversity in lizards: why are some organisms specialized? In: Mossakowski D, Roth G (eds) Environmental adaptation and evolution. Fischer, New York, pp 107–128Google Scholar
  63. Greene HW (1983) Dietary correlates of the origin and radiation of snakes. Am Zool 23: 431–441Google Scholar
  64. Halpern M (1983) Nasal chemical senses in snakes. In: Ewert JP, Carpina RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 141–176Google Scholar
  65. Halpern M (1987) The organization and function of the vomeronasal system. Annu Rev Neurosci 10: 325–362PubMedGoogle Scholar
  66. Halpern M, Furmin N (1979) Roles of the vomeronasal and olfactory systems in prey attack and feeding in adult garter snakes. Physiol Behav 22: 1183–1189PubMedGoogle Scholar
  67. Halpern M, Kubie JL (1984) The role of the ophidian vomeronasal system in species-typical behavior. Trends Neurosci 7(12): 472–477Google Scholar
  68. Heidweiller J, Zweers GA (1990) Drinking mechanisms in the zebra finch and the Bengalese finch. Condor 92: 1–28Google Scholar
  69. Houston J (1828) On the structure and mechanism of the tongue of the chameleon. Trans R Ir Acad 15: 177–201Google Scholar
  70. Iverson JB (1982) Adaptations to herbivory in iguanine lizards. In: Burghardt GM, Rand AS (eds) Iguanas of the world; their behavior ecology and conservation. Noyes, Park Ridge, pp 60–76Google Scholar
  71. Iwasaki S (1990) Fine structure of the dorsal lingual epithelium of the lizard Gekko japonicus (Lacertilia Gekkonidae). Am J Anat 187: 12–20PubMedGoogle Scholar
  72. Kamal AM, Hammouda HG (1965a) The chondrocranium of the snake Eryx jaculus. Acta Zool 46: 167–208Google Scholar
  73. Kamal AM, Hammouda HG (1965b) The development of the skull of Psammophis sibilans. J Morphol 116: 197–246Google Scholar
  74. Kardong KV (1974) Kinesis of the jaw apparatus during the strike in the cottonmouth snake, Agkistrodon piscivorous. Forma Functio 7: 327–354Google Scholar
  75. Kardong KV (1977) Kinesis of the jaw apparatus during swallowing in the cottonmouth snake, Agkistrodon piscivorous. Copeia 1977: 338–348Google Scholar
  76. Kardong KV, Dullemeijer P, Fransen JAM (1986) Feeding mechanism in the rattlesnake Crotalus durissus. Amphib-Reptilia 7: 271–302Google Scholar
  77. Kardong KV, Haverly J (1993) Drinking by the common boa, C. Boa constrictor. Copeia 1993: 808–818Google Scholar
  78. Kathariner L (1894) Anatomie und Mechanismus der Zunge des Vermiliguer. Jena Z Naturwise 29: 247–270.Google Scholar
  79. Kent WS (1895) Observations on the frilled lizard Chlamydosaurus kingii. Proc Zool Soc Lond 46: 712–719Google Scholar
  80. Kestevelen HL (1944) The evolution of the skull and cephalic muscles: a comparative study of their development and adult morphology. Part III. The Sauria (Reptilia). Aust Mus Sid Mem VIII 3: 237–269Google Scholar
  81. Kier WM (1982) The functional morphology of the musculature of squid (Loliginidae) arms and tentacles. J Morphol 172: 179–192Google Scholar
  82. Kier WM, Smith KK (1985) Tongues, tentacles and trunks: the biomechanics of movement in muscular-hydrostats. Zool J Linn Soc 83: 307–324Google Scholar
  83. Kraklau DM (1991) Kinematics of prey capture and chewing in the lizard Agama agama. J Morphol 210: 195–212Google Scholar
  84. Kubie JL, Halpern M (1979) Chemical senses involved in garter-snake prey trailing. J Comp Physiol Psychol 93(4): 648–667Google Scholar
  85. Kubie JL, Vagvolgyi A, Halpern M (1978) The roles of the vomeronasal and olfactory systems in the courtship behavior of male garter snakes. J Comp Physiol Psychol 92: 627–641Google Scholar
  86. Langebartel DA (1968) The hyoid and its associated muscles in snakes. III Biol Monogr 38: 1–156Google Scholar
  87. List JC (1966) Comparative osteology of the snake families Typhlopidae and Leptopyphlopidae. III Biol Monogr 36: 1–112Google Scholar
  88. Losos J (1985) Male aggressive behavior in a pair of sympatric sibling species. Breviora 484: 1–30Google Scholar
  89. McDowell SB (1972) The evolution of the tongue of snakes and its bearing in snake origins. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology, vol 6. Meredith, New York, pp 192–273Google Scholar
  90. Meredith M, Burghardt GM (1978) Electrophysiological studies of the tongue and accessory olfactory bulb in garter snakes. Physiol Behav 21: 1001–1008PubMedGoogle Scholar
  91. Mivart SG (1870) On the myology of Chameleo parsonii. Proc Sci Meet Zool Soc Lond 57: 850–890Google Scholar
  92. Murphy JB, Mitchell LA (1974) Ritualized combat behavior of the pygmy monitor lizard Varanus gilleni (Sauria: Varanidae). Herpetologica 30: 90–97Google Scholar
  93. Oelrich TM (1956) The anatomy of the head of Ctenosaura pectinata. Misc Publ Mus Zool Univ Mich 94: 1–122Google Scholar
  94. Owasa G (1898) Beiträge zur Anatomie der Hatteria punctata. Arch Mikrosk Anat 51: 481–691Google Scholar
  95. Presch W (1974) A survey of the dentition of the macroteiid lizards (Teiidae: Lacertilia). Herpetologica 30: 344–349Google Scholar
  96. Rabinowitz T, Tandler B (1986) Papillary morphology of the tongue of the American chameleon: Anolis carolinensis. Anat Rec 216: 483–489PubMedGoogle Scholar
  97. Richter H (1933) Das Zungenbein und seine Muskulatur bei den Lacertilia vera. Jena Z Naturwiss 66: 395–480Google Scholar
  98. Rieppel O (1981) The hyobranchial skeleton in some little known lizards and snakes. J Herpetol 15: 433–440Google Scholar
  99. Rieppel O, Labhardt L (1979) Mandibular mechanics in Varanus niloticus (Reptilia: Lacertilia). Herpetologica 35: 158–163Google Scholar
  100. Romer AS (1956) Osteology of the reptiles. University Chicago Press, ChicagoGoogle Scholar
  101. Schwenk K (1982) Lizard tongue morphology: disparate functions and comprehensive designs. Am Zool 22: 923Google Scholar
  102. Schwenk K (1985) Occurrence, distribution and functional significance of taste buds in lizards. Copeia 1985: 91–101Google Scholar
  103. Schwenk K (1986) Morphology of the tongue in the Tuatara Sphenodon punctatus (Reptilia: Lepidosauria) with comments on function and phylogeny. J Morphol 188: 129–156Google Scholar
  104. Schwenk K (1987) Evolutionary determinants of cranial form and function in lizards. Am Zool 27: 105AGoogle Scholar
  105. Schwenk K (1988) Comparative morphology of the Lepidosaur tongue and its relevance to squamate phylogeny. In: Estes R, Pregill G (eds) Phylogenetic relationships of the lizard families, Essays commemorating C.L. Camp. Stanford Univ Press, Stanford, pp 569–598Google Scholar
  106. Schwenk K, Bell DA (1988) A cryptic intermediate in the evolution of chameleon tongue projection. Experientia 44: 697–700PubMedGoogle Scholar
  107. Schwenk K, Greene HW (1987) Water collection and drinking in Phrynocephalus helioscopus: a possible condensation mechanism. J Herpetol 21: 134–139Google Scholar
  108. Schwenk K, Throckmorton GS (1989) Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics. J Zool (Lond) 219: 153–176Google Scholar
  109. Shine R (1990) Function and evolution of the frill of the frillneck lizard Chlamydosaurus kingii (Sauria: Agamidae). Biol J Linn Soc 40: 11–20Google Scholar
  110. Smith KK (1984) The use of the tongue and hyoid apparatus during feeding in lizards (Ctenosaura similis and Tupinambis nigropunctatus). J Zool (Lond) 202: 115–143Google Scholar
  111. Smith KK (1986) Morphology and function of the tongue and hyoid apparatus in Varanus (Varanidae Lacertilia). J Morphol 187: 261–287PubMedGoogle Scholar
  112. Smith KK (1988) Form and function of the tongue in agamid lizards with comments on its phylogenetic significance. J Morphol 196: 157–171PubMedGoogle Scholar
  113. Smith KK, Kier WM (1989) Trunks, tongues and tentacles: moving with skeletons of muscle. Am Sci 77: 28–35Google Scholar
  114. Smith K, Mackay M (1990) The morphology of the intrinsic tongue musculature in snakes (Reptilia Ophidia): functional and phylogenetic implications. J Morphol 205: 307–324Google Scholar
  115. So KK, Wainwright PC, Bennett AF (1992) Kinematics of prey processing in Chamaelo jacksonii: conservation of function with morphological specialization. J Zool Lond 226: 47–64Google Scholar
  116. Sondhi KC (1958) The hyoid and associated structures in some Indian reptiles. Ann Zool 2: 157–227Google Scholar
  117. Throckmorton G, De Bavay SJ, Chaffey W, Merrotsy B, Noske BS, Noske R (1985) The mechanism of frill erection in the bearded dragon Amphibolurus barbatus with comments on the jacky lizard A. muricatus (Agamidae). J Morphol 183: 285–292Google Scholar
  118. Tilak R (1964) The hyoid apparatus of Uromastix hardwickii Gray. Sci Cult 30: 244–246Google Scholar
  119. Ulinski PS (1972) Tongue movements in the common boa (Constrictor constrictor). Anim Behav 20: 373–383PubMedGoogle Scholar
  120. Underwood G (1971) A modern appreciation of Camp’s “classification of the lizards”. Introduction to reprint by SSARGoogle Scholar
  121. Von Geldern CE (1919) Mechanism in the production of throat-fan in the chameleon Anolis carolinensis. Proc Calif Acad Sci 9: 313–329Google Scholar
  122. Wainwright PC, Bennett AF (1992a) The mechanism of tongue projection. I Electromyographic tests of functional hypotheses. J Exp Biol 168: 1–21Google Scholar
  123. Wainwright PC, Bennett AF (1992b) The mechanism of tongue projection. II. Role of shape in muscular hydrostat. J Exp Biol 168: 23–40Google Scholar
  124. Wainwright PC, Kraklau DM, Bennett AF (1991) Kinematics of tongue projection in Chamaeleo oustaleti. J Exp Biol 159: 109–133Google Scholar
  125. Willard WA (1915) The cranial nerves of Anolis carolinensis. Bull Mus Comp Zool 59: 1–134Google Scholar
  126. Young BA (1990) Is there a direct link between the ophidian tongue and Jacobson’s organ? Amphib-Reptilia 11: 263–276Google Scholar
  127. Zavattari E (1911) I muscoli ioidei dei sauri in rapporto con i muscoli ioidei degli altri vertebrati. Mem Acad Sci Torino 60: 351–392Google Scholar
  128. Zoond A (1933) The mechanism of projection of the chameleon’s tongue. J Exp Biol 10: 174–185Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1994

Authors and Affiliations

  • V. L. Bels
    • 1
  • M. Chardon
    • 2
  • K. V. Kardong
    • 3
  1. 1.Agronomic Centre of Applied ResearchesC.A.R.A.H.Belgium
  2. 2.Laboratory of Functional MorphologyUniversity of LiègeLiègeBelgium
  3. 3.Department of ZoologyWashington State UniversityPullmanUSA

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