{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:12:34Z","timestamp":1790831554062,"version":"4.1.0"},"reference-count":43,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"5420","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Science"],"published-print":{"date-parts":[[1999,6,4]]},"abstract":"<jats:p>\n            A controversial hypothesis has proposed that lizards are subject to a speed-dependent axial constraint that prevents effective lung ventilation during moderate- and high-speed locomotion. This hypothesis has been challenged by results demonstrating that monitor lizards (genus\n            <jats:italic>Varanus<\/jats:italic>\n            ) experience no axial constraint. Evidence presented here shows that, during locomotion, varanids use a positive pressure gular pump to assist lung ventilation. Disabling the gular pump reveals that the axial constraint is present in varanids but it is masked by gular pumping under normal conditions. These findings support the prediction that the axial constraint may be found in other tetrapods that breathe by costal aspiration and locomote with a lateral undulatory gait.\n          <\/jats:p>","DOI":"10.1126\/science.284.5420.1661","type":"journal-article","created":{"date-parts":[[2002,7,27]],"date-time":"2002-07-27T09:42:20Z","timestamp":1027762940000},"page":"1661-1663","source":"Crossref","is-referenced-by-count":107,"title":["Contribution of Gular Pumping to Lung Ventilation in Monitor Lizards"],"prefix":"10.1126","volume":"284","author":[{"given":"Tomasz","family":"Owerkowicz","sequence":"first","affiliation":[{"name":"Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Colleen G.","family":"Farmer","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James W.","family":"Hicks","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth L.","family":"Brainerd","sequence":"additional","affiliation":[{"name":"Department of Biology and Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"221","reference":[{"key":"e_1_3_1_2_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0094837300008903"},{"key":"e_1_3_1_2_3","unstructured":"; Exp. Biol. 47 33 (1987)."},{"key":"e_1_3_1_3_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.152.1.453"},{"key":"e_1_3_1_3_3","doi-asserted-by":"crossref","unstructured":"; Am. Zool. 31 644 (1991).","DOI":"10.1093\/icb\/31.4.644"},{"key":"e_1_3_1_4_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.199.11.2499"},{"key":"e_1_3_1_5_2","first-page":"R174","volume":"239","author":"Gleeson T. T.","year":"1980","unstructured":"Gleeson T. T., Mitchell G. S., Bennett A. F., Am. J. Physiol. 239, R174 (1980);","journal-title":"Am. J. Physiol."},{"key":"e_1_3_1_5_3","doi-asserted-by":"publisher","DOI":"10.1016\/0034-5687(81)90116-X"},{"key":"e_1_3_1_5_4","unstructured":"; A. F. Bennett in Biology of the Reptilia C. Gans and F. H. Pough Eds. (Academic Press London 1982) vol. 13 pp. 153\u2013199."},{"key":"e_1_3_1_6_2","unstructured":"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\u2013138."},{"key":"e_1_3_1_7_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.200.20.2629"},{"key":"e_1_3_1_8_2","unstructured":"We recorded x-ray videos of three juvenile I. iguana (70 to 100 g) and six V. exanthematicus (two adults 1500 and 2000 g and four juveniles 120 to 200 g) while they were locomoting at speeds of 1 to 3 km hour \u22121 on a motorized treadmill at 32\u00b0 to 35\u00b0C. 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."},{"key":"e_1_3_1_9_2","unstructured":"The number of gular pumps per breath was measured from recordings of air flow through the nares and mouth (10). Gular pumps appear on flow traces as a series of small inspirations between much larger expirations. When locomoting at 1 km hour \u22121 savannah monitors used a mean of 2.82 \u00b1 0.85 gular pumps per breath and at 2 km hour \u22121 they used a mean of 3.04 \u00b1 0.65 pumps per breath (means \u00b1 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)."},{"key":"e_1_3_1_10_2","unstructured":"Polyethylene cannulas (PE 160; 1.6-mm outer diameter O.D.) were surgically implanted into the gular cavity and one lung of four juvenile V. exanthematicus (100 to 200 g) and connected to Omega PX-138 pressure transducers sutured to the skin above the pectoral and pelvic girdles. Pressures were recorded during locomotion at treadmill speeds between 1 and 3 km hour \u22121 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)."},{"key":"e_1_3_1_11_2","unstructured":"Six savannah monitor lizards (body mass 305 to 480 g) were trained to locomote on a motorized treadmill in an environmental chamber at 36\u00b0C. During gular compression in varanids the mouth is closed and the internal nares are sealed by ridges of tissue (sublingual plicae) that lie lateral to the tongue (T. Owerkowicz unpublished data). We disrupted the oral seal by propping the mouth open with a retainer made from polyethylene tubing. A lightweight plastic mask was then epoxy glued around the snout to enclose the mouth and nostrils. For the control condition the same individuals were tested with just the plastic mask and no retainer. A bias flow of humidified air (1200 ml min \u22121 ) was drawn through the mask and a pneumotachograph (H. Rudolph 8421 series 0-5 LPM) connected to a differential pressure transducer (Validyne MP 45-1-871) measured air flow. Oxygen and CO 2 analyzers (Applied Electrochemistry S-3A and CD-3A) monitored the gas composition. Instruments were calibrated by injection of known volumes of mixed gases before data collection each day. Expired gas volume ( V\u0307 E ) and rate of oxygen consumption ( V\u0307 O 2 ) were measured during the last minute of locomotion and first minute of recovery at each speed. Four out of six of the animals tested would not locomote steadily in control and experimental conditions above 2 km hour \u22121 ; two locomoted steadily up to 3 km hour \u22121 ."},{"key":"e_1_3_1_12_2","unstructured":"The maximum running speeds measured for these lizards on a trackway in the lab are 15 km hour \u22121 for I. iguana and 6.6 km hour \u22121 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)."},{"key":"e_1_3_1_13_2","unstructured":"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\u2013281."},{"key":"e_1_3_1_14_2","doi-asserted-by":"publisher","DOI":"10.1071\/ZO9940185"},{"key":"e_1_3_1_15_2","unstructured":"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\u2013483;"},{"key":"e_1_3_1_15_3","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.198.8.1783"},{"key":"e_1_3_1_15_4","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-642-68964-2_1"},{"key":"e_1_3_1_15_5","first-page":"R89","volume":"233","author":"Wood S. C.","year":"1977","unstructured":"Wood S. C., Johansen K., Gatz R. N., Am. J. Physiol. 233, R89 (1977);","journal-title":"Am. J. Physiol."},{"key":"e_1_3_1_15_6","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051340306"},{"key":"e_1_3_1_16_2","doi-asserted-by":"publisher","DOI":"10.2307\/1564991"},{"key":"e_1_3_1_16_3","unstructured":"; 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 Gainesville FL 1981)."},{"key":"e_1_3_1_17_2","unstructured":"For example defense and threat display behavior ["},{"key":"e_1_3_1_17_3","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7998.1995.tb01787.x"},{"key":"e_1_3_1_17_4","unstructured":"; S. M. Deban J. C. O'Reilly"},{"key":"e_1_3_1_17_5","doi-asserted-by":"publisher","DOI":"10.1002\/jez.1402700506"},{"key":"e_1_3_1_17_6","unstructured":"] olfaction [T. S. Parsons in Biology of the Reptilia C. Gans and T. S. Parsons Eds. (Academic Press London 1970) vol. 2 pp. 99\u2013192;"},{"key":"e_1_3_1_17_7","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-010X(19961215)276:6<415::AID-JEZ5>3.0.CO;2-Q"},{"key":"e_1_3_1_17_8","unstructured":"] and thermoregulation ["},{"key":"e_1_3_1_17_9","doi-asserted-by":"publisher","DOI":"10.1086\/physzool.37.4.30152753"},{"key":"e_1_3_1_17_10","unstructured":"]. One abstract has been published in which Uromastyx was found to inflate its lungs with a gular pump while anaesthetized ["},{"key":"e_1_3_1_17_11","first-page":"6P","volume":"483","author":"Al-Ghamdi M. S.","year":"1995","unstructured":"Al-Ghamdi M. S., Jones J. F. X., Taylor E. W., J. Physiol. 483, 6P (1995)].","journal-title":"J. Physiol."},{"key":"e_1_3_1_18_2","unstructured":"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."},{"key":"e_1_3_1_19_2","first-page":"61","volume":"3","author":"Gans C.","year":"1970","unstructured":"Gans C., Forma Functio 3, 61 (1970);","journal-title":"Forma Functio"},{"key":"e_1_3_1_19_3","doi-asserted-by":"crossref","unstructured":"; Evolution 24 723 (1970).","DOI":"10.2307\/2406552"},{"key":"e_1_3_1_20_2","doi-asserted-by":"crossref","unstructured":"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\u2013209;","DOI":"10.4159\/harvard.9780674184404.c11"},{"key":"e_1_3_1_20_3","doi-asserted-by":"publisher","DOI":"10.1093\/icb\/34.2.289"},{"key":"e_1_3_1_21_2","unstructured":"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"},{"key":"e_1_3_1_21_3","first-page":"R342","volume":"241","author":"John-Alder H. B.","year":"1981","unstructured":"John-Alder H. B., Bennett A. F., Am. J. Physiol. 241, R342 (1981);","journal-title":"Am. J. Physiol."},{"key":"e_1_3_1_21_4","unstructured":"]. 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."},{"key":"e_1_3_1_22_2","unstructured":"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 IBN-9875245 and IBN-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."}],"container-title":["Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/science.284.5420.1661","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,13]],"date-time":"2024-01-13T09:09:27Z","timestamp":1705136967000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/science.284.5420.1661"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1999,6,4]]},"references-count":43,"journal-issue":{"issue":"5420","published-print":{"date-parts":[[1999,6,4]]}},"alternative-id":["10.1126\/science.284.5420.1661"],"URL":"https:\/\/doi.org\/10.1126\/science.284.5420.1661","relation":{},"ISSN":["0036-8075","1095-9203"],"issn-type":[{"value":"0036-8075","type":"print"},{"value":"1095-9203","type":"electronic"}],"subject":[],"published":{"date-parts":[[1999,6,4]]}}}