Contribution of gular pumping to lung ventilation in monitor lizards

Science

Volumn 284, Issue 5420, 1999, Pages 1661-1663

  Owerkowicz, Tomasz ^a   Farmer, Colleen C ^b   Hicks, James W ^b   Brainerd, Elizabeth L ^c  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC CAPACITY; ANIMAL EXPERIMENT; ARTICLE; BREATHING MECHANICS; BREATHING MUSCLE; GAIT; HYPOTHESIS; LIZARD; LOCOMOTION; LUNG MINUTE VOLUME; LUNG VENTILATION; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; ZOOLOGY;

ANIMALS; ENERGY METABOLISM; GAIT; IGUANAS; LIZARDS; LOCOMOTION; OXYGEN CONSUMPTION; PHARYNX; PRESSURE; PULMONARY GAS EXCHANGE; PULMONARY VENTILATION;

EID: 0033522808     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.284.5420.1661     Document Type: Article

References (38)

1. D. R. Carrier, Paleobiology 13, 326 (1987); Exp. Biol. 47, 33 (1987).
2. D. R. Carrier, Paleobiology 13, 326 (1987); Exp. Biol. 47, 33 (1987).
3. _, J. Exp. Biol. 152, 453 (1990); Am. Zool. 31, 644 (1991).
4. _, J. Exp. Biol. 152, 453 (1990); Am. Zool. 31, 644 (1991).
5. D. Ritter, J. Exp. Biol. 199, 2499 (1996).
6. T. T. Gleeson, G. S. Mitchell, A. F. Bennett, Am. J. Physiol. 239, R174 (1980); G. S. Mitchell, T. T. Gleeson, A. F. Bennett, Respir. Physiol. 43, 365 (1981); A. F. Bennett, in Biology of the Reptilia, C. Gans and F. H. Pough, Eds. (Academic Press, London, 1982), vol. 13, pp. 153-199.
7. T. T. Gleeson, G. S. Mitchell, A. F. Bennett, Am. J. Physiol. 239, R174 (1980); G. S. Mitchell, T. T. Gleeson, A. F. Bennett, Respir. Physiol. 43, 365 (1981); A. F. Bennett, in Biology of the Reptilia, C. Gans and F. H. Pough, Eds. (Academic Press, London, 1982), vol. 13, pp. 153-199.
8. T. T. Gleeson, G. S. Mitchell, A. F. Bennett, Am. J. Physiol. 239, R174 (1980); G. S. Mitchell, T. T. Gleeson, A. F. Bennett, Respir. Physiol. 43, 365 (1981); A. F. Bennett, in Biology of the Reptilia, C. Gans and F. H. Pough, Eds. (Academic Press, London, 1982), vol. 13, pp. 153-199.
9. A. F. Bennett, in Advances in Veterinary Science and Comparative Medicine: Comparative Vertebrate Exercise Physiology, J. H. Jones, Ed. (Academic Press, San Diego, CA, 1994), vol. 38B, pp. 113-138.
10. T. Wang, D. R. Carrier, J. W. Hicks, J. Exp. Biol. 200, 2629 (1997).
11. -1 on a motorized treadmill at 32° to 35°C. Videos were recorded in lateral projection with a Siemens cineradiographic apparatus and a Sony DCR VX1000 Digital Camcorder at 30 frames per second and 1/250 s shutter speed. Each individual ran at the maximum speed that it would maintain steadily on the treadmill for between 1 and 3 min. Videos were reviewed frame by frame to look for evidence of gular pumping. Gular-pumping motions and associated lung inflations were obvious during locomotion and in a few breaths immediately after locomotion in all six V. exanthematicus (Fig. 2); no gular pumping was seen in the three I. iguana.
12. -1, they used a mean of 3.04 ± 0.65 pumps per breath (means ± SEM, n = 6; these means are not significantly different). Flow traces of breathing in I. iguana during locomotion show no evidence of gular pumping (C. Farmer, unpublished data).
13. -1 and synchronized with videoradiographs of the animals to correlate pressures with the gular and lung volume changes visible in the x-ray images (Fig. 2).
14. -1.
15. -1 for V. exanthematicus (1). Thus, the maximum treadmill speeds used in the metabolic studies represent only about 10% of the maximum speed of I. iguana and 30% of the maximum speed of V. exanthematicus (6).
16. R. Estes, K. de Queiroz, J. Gauthier, in Phylogenetic Relationships of the Lizard Families, R. Estes and G. Pregill, Eds. (Stanford Univ. Press, Stanford, CA, 1988), pp. 119-281.
17. K. A. Christian and K. E. Conley, Aust. J. Zool. 42, 185 (1994).
18. J. W. Hicks, in Biology of the Reptilia, C. Gans and A. S. Gaunt, Eds. (Society for the Study of Amphibians and Reptiles, Ithaca, NY, 1998), vol. 19, pp. 425-483; S. R. Hopkins, J. W. Hicks, T. K. Cooper, F. L. Powell, J. Exp. Biol. 198, 1783 (1995); S. F. Perry, Adv. Anat. Embryol. Cell Biol. 79, 1 (1983); S. C. Wood, K. Johansen, R. N. Gatz, Am. J. Physiol. 233, R89 (1977); G. J. W. Webb, H. Heatwole, J. de Bavay, J. Morphol. 134, 335 (1971).
19. J. W. Hicks, in Biology of the Reptilia, C. Gans and A. S. Gaunt, Eds. (Society for the Study of Amphibians and Reptiles, Ithaca, NY, 1998), vol. 19, pp. 425-483; S. R. Hopkins, J. W. Hicks, T. K. Cooper, F. L. Powell, J. Exp. Biol. 198, 1783 (1995); S. F. Perry, Adv. Anat. Embryol. Cell Biol. 79, 1 (1983); S. C. Wood, K. Johansen, R. N. Gatz, Am. J. Physiol. 233, R89 (1977); G. J. W. Webb, H. Heatwole, J. de Bavay, J. Morphol. 134, 335 (1971).
20. J. W. Hicks, in Biology of the Reptilia, C. Gans and A. S. Gaunt, Eds. (Society for the Study of Amphibians and Reptiles, Ithaca, NY, 1998), vol. 19, pp. 425-483; S. R. Hopkins, J. W. Hicks, T. K. Cooper, F. L. Powell, J. Exp. Biol. 198, 1783 (1995); S. F. Perry, Adv. Anat. Embryol. Cell Biol. 79, 1 (1983); S. C. Wood, K. Johansen, R. N. Gatz, Am. J. Physiol. 233, R89 (1977); G. J. W. Webb, H. Heatwole, J. de Bavay, J. Morphol. 134, 335 (1971).
21. J. W. Hicks, in Biology of the Reptilia, C. Gans and A. S. Gaunt, Eds. (Society for the Study of Amphibians and Reptiles, Ithaca, NY, 1998), vol. 19, pp. 425-483; S. R. Hopkins, J. W. Hicks, T. K. Cooper, F. L. Powell, J. Exp. Biol. 198, 1783 (1995); S. F. Perry, Adv. Anat. Embryol. Cell Biol. 79, 1 (1983); S. C. Wood, K. Johansen, R. N. Gatz, Am. J. Physiol. 233, R89 (1977); G. J. W. Webb, H. Heatwole, J. de Bavay, J. Morphol. 134, 335 (1971).
22. J. W. Hicks, in Biology of the Reptilia, C. Gans and A. S. Gaunt, Eds. (Society for the Study of Amphibians and Reptiles, Ithaca, NY, 1998), vol. 19, pp. 425-483; S. R. Hopkins, J. W. Hicks, T. K. Cooper, F. L. Powell, J. Exp. Biol. 198, 1783 (1995); S. F. Perry, Adv. Anat. Embryol. Cell Biol. 79, 1 (1983); S. C. Wood, K. Johansen, R. N. Gatz, Am. J. Physiol. 233, R89 (1977); G. J. W. Webb, H. Heatwole, J. de Bavay, J. Morphol. 134, 335 (1971).
23. A. J. Phillips, J. Herpetol. 29, 407 (1995); D. King and B. Green, Goanna: The Biology of Varanid Lizards (New South Wales University Press, Kensington, NSW, Australia, 1993); W. Auffenberg, The Behavioral Ecology of the Komodo Monitor (University Presses of Florida, Gainesvilie, FL, 1981).
24. A. J. Phillips, J. Herpetol. 29, 407 (1995); D. King and B. Green, Goanna: The Biology of Varanid Lizards (New South Wales University Press, Kensington, NSW, Australia, 1993); W. Auffenberg, The Behavioral Ecology of the Komodo Monitor (University Presses of Florida, Gainesvilie, FL, 1981).
25. A. J. Phillips, J. Herpetol. 29, 407 (1995); D. King and B. Green, Goanna: The Biology of Varanid Lizards (New South Wales University Press, Kensington, NSW, Australia, 1993); W. Auffenberg, The Behavioral Ecology of the Komodo Monitor (University Presses of Florida, Gainesvilie, FL, 1981).
26. For example, defense and threat display behavior [V. L. Bels, J.-P. Gasc, V. Goosse, S. Renous, R. Vernet, J. Zool. 235, 95 (1995); S. M. Deban, J. C. O'Reilly, T. Theimer, J. Exp. Zool. 270, 451 (1994)], olfaction [T. S. Parsons, in Biology of the Reptilia, C. Gans and T. S. Parsons, Eds. (Academic Press, London, 1970), vol. 2, pp. 99-192; B. E. Dial and K. Schwenk, J. Exp. Zool. 276, 415 (1996)], and thermoregulation [G. A. Bartholomew and V. A. Tucker, Physiol. Zool. 37, 341 (1964)]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized [M. S. Al-Ghamdi, J. F. X. Jones, E. W. Taylor, J. Physiol. 483, 6P (1995)].
27. For example, defense and threat display behavior [V. L. Bels, J.-P. Gasc, V. Goosse, S. Renous, R. Vernet, J. Zool. 235, 95 (1995); S. M. Deban, J. C. O'Reilly, T. Theimer, J. Exp. Zool. 270, 451 (1994)], olfaction [T. S. Parsons, in Biology of the Reptilia, C. Gans and T. S. Parsons, Eds. (Academic Press, London, 1970), vol. 2, pp. 99-192; B. E. Dial and K. Schwenk, J. Exp. Zool. 276, 415 (1996)], and thermoregulation [G. A. Bartholomew and V. A. Tucker, Physiol. Zool. 37, 341 (1964)]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized [M. S. Al-Ghamdi, J. F. X. Jones, E. W. Taylor, J. Physiol. 483, 6P (1995)].
28. For example, defense and threat display behavior [V. L. Bels, J.-P. Gasc, V. Goosse, S. Renous, R. Vernet, J. Zool. 235, 95 (1995); S. M. Deban, J. C. O'Reilly, T. Theimer, J. Exp. Zool. 270, 451 (1994)], olfaction [T. S. Parsons, in Biology of the Reptilia, C. Gans and T. S. Parsons, Eds. (Academic Press, London, 1970), vol. 2, pp. 99-192; B. E. Dial and K. Schwenk, J. Exp. Zool. 276, 415 (1996)], and thermoregulation [G. A. Bartholomew and V. A. Tucker, Physiol. Zool. 37, 341 (1964)]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized [M. S. Al-Ghamdi, J. F. X. Jones, E. W. Taylor, J. Physiol. 483, 6P (1995)].
29. For example, defense and threat display behavior [V. L. Bels, J.-P. Gasc, V. Goosse, S. Renous, R. Vernet, J. Zool. 235, 95 (1995); S. M. Deban, J. C. O'Reilly, T. Theimer, J. Exp. Zool. 270, 451 (1994)], olfaction [T. S. Parsons, in Biology of the Reptilia, C. Gans and T. S. Parsons, Eds. (Academic Press, London, 1970), vol. 2, pp. 99-192; B. E. Dial and K. Schwenk, J. Exp. Zool. 276, 415 (1996)], and thermoregulation [G. A. Bartholomew and V. A. Tucker, Physiol. Zool. 37, 341 (1964)]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized [M. S. Al-Ghamdi, J. F. X. Jones, E. W. Taylor, J. Physiol. 483, 6P (1995)].
30. For example, defense and threat display behavior [V. L. Bels, J.-P. Gasc, V. Goosse, S. Renous, R. Vernet, J. Zool. 235, 95 (1995); S. M. Deban, J. C. O'Reilly, T. Theimer, J. Exp. Zool. 270, 451 (1994)], olfaction [T. S. Parsons, in Biology of the Reptilia, C. Gans and T. S. Parsons, Eds. (Academic Press, London, 1970), vol. 2, pp. 99-192; B. E. Dial and K. Schwenk, J. Exp. Zool. 276, 415 (1996)], and thermoregulation [G. A. Bartholomew and V. A. Tucker, Physiol. Zool. 37, 341 (1964)]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized [M. S. Al-Ghamdi, J. F. X. Jones, E. W. Taylor, J. Physiol. 483, 6P (1995)].
31. For example, defense and threat display behavior [V. L. Bels, J.-P. Gasc, V. Goosse, S. Renous, R. Vernet, J. Zool. 235, 95 (1995); S. M. Deban, J. C. O'Reilly, T. Theimer, J. Exp. Zool. 270, 451 (1994)], olfaction [T. S. Parsons, in Biology of the Reptilia, C. Gans and T. S. Parsons, Eds. (Academic Press, London, 1970), vol. 2, pp. 99-192; B. E. Dial and K. Schwenk, J. Exp. Zool. 276, 415 (1996)], and thermoregulation [G. A. Bartholomew and V. A. Tucker, Physiol. Zool. 37, 341 (1964)]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized [M. S. Al-Ghamdi, J. F. X. Jones, E. W. Taylor, J. Physiol. 483, 6P (1995)].
32. Single individuals from each of six additional species were videoradiographed to look for gular pumping during and immediately after locomotion. Gular pumping was observed in Uromastyx maliensis, Eublepharis macularius, Tupinambis teguixin, and Heloderma suspectum. No gular pumping was observed in Chamaeleo jacksonii or Tiliqua scincoides.
33. C. Gans, Forma Functio 3, 61 (1970); Evolution 24, 723 (1970).
34. C. Gans, Forma Functio 3, 61 (1970); Evolution 24, 723 (1970).
35. K. F. Liem, in Functional Vertebrate Morphology, M. Hildebrand, D. M. Bramble, K. F. Liem, D. B. Wake, Eds. (Harvard Univ. Press, Cambridge, MA, 1985), pp. 185-209; E. L. Brainerd, Am. Zool. 34, 289 (1994).
36. K. F. Liem, in Functional Vertebrate Morphology, M. Hildebrand, D. M. Bramble, K. F. Liem, D. B. Wake, Eds. (Harvard Univ. Press, Cambridge, MA, 1985), pp. 185-209; E. L. Brainerd, Am. Zool. 34, 289 (1994).
37. To obtain an estimate of locomotor endurance, we timed six savannah monitor lizards (0.640 to 0.900 kg) (up to 15 min) while they were locomoting to exhaustion on a motorized treadmill once per day, over the course of a week. Exhaustion was assumed after an animal failed to respond to repetitive prodding and slid to the end of the treadmill (length = 2.5 m) [after H. B. John-Alder and A. F. Bennett, Am. J. Physiol. 241, R342 (1981)]. The procedure was repeated for each individual with the animal's gular region wrapped with 5-cm-wide Elastoplast tape to prevent gular pumping. The tape did not interfere directly with air flow in any way; the mouth was free to open, the cartilaginous rings of the trachea prevented tracheal compression, and the glottis in varanids is located in the front of the oral cavity below the internal nares, well cranial to the position of the tape. The animals used for these endurance tests were larger than those used for ventilation and oxygen consumption measurements (10); therefore, it is not unexpected that they were able to sustain locomotion at higher speeds than would be predicted from Fig. 4.
38. All animal experiments were conducted in accordance with institutional guidelines. We thank W. Bennett, D. Carrier, A. Crompton, T. Hiebert, N. Kley, T. Landberg, J. O'Reilly, R. Simons, and A. Summers for valuable comments on the manuscript We are very grateful to L Meszoly for the line drawings used in Fig. 2. This study was supported by NSF grants IBM-9875245 and IBM-9419892 and a University of Massachusetts Executive Area for Research grant to E.L.B., NSF grant IBN-9630807 to J.W.H., NIH grant 1F32-HL09796-01 to C.G.F., and a traveling fellowship (Company of Biologists Limited) and a Chapman Fellowship to T.O.