{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T23:51:57Z","timestamp":1773186717572,"version":"3.50.1"},"reference-count":51,"publisher":"The Company of Biologists","issue":"15","license":[{"start":{"date-parts":[[2020,9,3]],"date-time":"2020-09-03T00:00:00Z","timestamp":1599091200000},"content-version":"vor","delay-in-days":1860,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,8,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n               <jats:p>Crocodilians are among the most vocal non-avian reptiles. Adults of both sexes produce loud vocalizations known as \u2018bellows\u2019 year round, with the highest rate during the mating season. Although the specific function of these vocalizations remains unclear, they may advertise the caller's body size, because relative size differences strongly affect courtship and territorial behaviour in crocodilians. In mammals and birds, a common mechanism for producing honest acoustic signals of body size is via formant frequencies (vocal tract resonances). To our knowledge, formants have to date never been documented in any non-avian reptile, and formants do not seem to play a role in the vocalizations of anurans. We tested for formants in crocodilian vocalizations by using playbacks to induce a female Chinese alligator (Alligator sinensis) to bellow in an airtight chamber. During vocalizations, the animal inhaled either normal air or a helium\/oxygen mixture (heliox) in which the velocity of sound is increased. Although heliox allows normal respiration, it alters the formant distribution of the sound spectrum. An acoustic analysis of the calls showed that the source signal components remained constant under both conditions, but an upward shift of high-energy frequency bands was observed in heliox. We conclude that these frequency bands represent formants. We suggest that crocodilian vocalizations could thus provide an acoustic indication of body size via formants. Because birds and crocodilians share a common ancestor with all dinosaurs, a better understanding of their vocal production systems may also provide insight into the communication of extinct Archosaurians.<\/jats:p>","DOI":"10.1242\/jeb.119552","type":"journal-article","created":{"date-parts":[[2015,8,5]],"date-time":"2015-08-05T22:06:08Z","timestamp":1438812368000},"page":"2442-2447","source":"Crossref","is-referenced-by-count":37,"title":["A Chinese alligator in heliox: formant frequencies in a crocodilian"],"prefix":"10.1242","volume":"218","author":[{"given":"Stephan A.","family":"Reber","sequence":"first","affiliation":[{"name":"Department of Cognitive Biology, University of Vienna, Vienna 1150, Austria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takeshi","family":"Nishimura","sequence":"additional","affiliation":[{"name":"Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Judith","family":"Janisch","sequence":"additional","affiliation":[{"name":"Department of Cognitive Biology, University of Vienna, Vienna 1150, Austria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark","family":"Robertson","sequence":"additional","affiliation":[{"name":"St Augustine Alligator Farm Zoological Park, St Augustine, FL 32080, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"W. Tecumseh","family":"Fitch","sequence":"additional","affiliation":[{"name":"Department of Cognitive Biology, University of Vienna, Vienna 1150, Austria"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","reference":[{"key":"2021042509031751200_JEB119552C1","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1121\/1.1928124","article-title":"Frequency analysis of vowels produced in a helium-rich atmosphere","volume":"34","author":"Beil","year":"1962","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C2","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1080\/08912963.2011.560723","article-title":"Crocodilian behaviour: a window to dinosaur behaviour?","volume":"23","author":"Brazaitis","year":"2011","journal-title":"Hist. Biol."},{"key":"2021042509031751200_JEB119552C3","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1121\/1.418121","article-title":"Mechanisms of vocal production in budgerigars (Melopsittacus undulatus)","volume":"101","author":"Brittan-Powell","year":"1997","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C4","first-page":"364","article-title":"Review and classification of call types of juvenile crocodilians, and factors affecting distress calls","volume-title":"Crocodilian Biology and Evolution","author":"Britton","year":"2001"},{"key":"2021042509031751200_JEB119552C5","doi-asserted-by":"publisher","first-page":"960","DOI":"10.1111\/eth.12141","article-title":"Formant frequencies are acoustic cues to caller discrimination and are a weak indicator of the body size of corncrake males","volume":"119","author":"Budka","year":"2013","journal-title":"Ethology"},{"key":"2021042509031751200_JEB119552C6","first-page":"1","article-title":"Observations on acoustic behavior of crocodilians","volume":"58","author":"Campbell","year":"1973","journal-title":"Zoologica"},{"key":"2021042509031751200_JEB119552C7","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1016\/j.anbehav.2006.09.021","article-title":"Female perception of size-related formant shifts in red deer, Cervus elaphus","volume":"74","author":"Charlton","year":"2007","journal-title":"Anim. Behav."},{"key":"2021042509031751200_JEB119552C8","doi-asserted-by":"publisher","first-page":"3414","DOI":"10.1242\/jeb.061358","article-title":"Cues to body size in the formant spacing of male koala (Phascolarctos cinereus) bellows: honesty in an exaggerated trait","volume":"214","author":"Charlton","year":"2011","journal-title":"J. Exp. Biol."},{"key":"2021042509031751200_JEB119552C9","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1007\/s10071-012-0527-5","article-title":"Perception of size-related formant information in male koalas (Phascolarctos cinereus)","volume":"15","author":"Charlton","year":"2012","journal-title":"Anim. Cogn."},{"key":"2021042509031751200_JEB119552C10","volume-title":"Acoustic Theory of Speech Production","author":"Fant","year":"1960"},{"key":"2021042509031751200_JEB119552C11","doi-asserted-by":"publisher","first-page":"1213","DOI":"10.1121\/1.421048","article-title":"Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques","volume":"102","author":"Fitch","year":"1997","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C12","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1111\/j.1469-7998.1999.tb01020.x","article-title":"Acoustic exaggeration of size in birds via tracheal elongation: comparative and theoretical analyses","volume":"248","author":"Fitch","year":"1999","journal-title":"J. Zool."},{"key":"2021042509031751200_JEB119552C13","first-page":"65","article-title":"Unpacking \u201cHonesty\u201d: Vertebrate vocal production and the evolution of acoustic signals","volume-title":"Acoustic Communication","author":"Fitch","year":"2002"},{"key":"2021042509031751200_JEB119552C14","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1046\/j.1439-0310.2000.00572.x","article-title":"Perception of vocal tract resonances by whooping cranes Grus americana","volume":"106","author":"Fitch","year":"2000","journal-title":"Ethology"},{"key":"2021042509031751200_JEB119552C15","doi-asserted-by":"publisher","first-page":"1669","DOI":"10.1098\/rspb.2001.1704","article-title":"The descended larynx is not uniquely human","volume":"268","author":"Fitch","year":"2001","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"2021042509031751200_JEB119552C16","first-page":"26","article-title":"Structure and pattern of the roars of Chinese alligators (Alligator sinensis)","volume":"31","author":"Garrick","year":"1975","journal-title":"Herpetologica"},{"key":"2021042509031751200_JEB119552C17","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1093\/icb\/17.1.225","article-title":"Social signals and behaviors of adult alligators and crocodiles","volume":"17","author":"Garrick","year":"1977","journal-title":"Am. Zool."},{"key":"2021042509031751200_JEB119552C18","first-page":"157","article-title":"Social signals of adult American alligators","volume":"160","author":"Garrick","year":"1978","journal-title":"Bull. Am. Museum Nat. Hist."},{"key":"2021042509031751200_JEB119552C19","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1007\/BF00609454","article-title":"The effects of tracheal coiling on the vocalizations of cranes (Aves: Gruidae)","volume":"161","author":"Gaunt","year":"1987","journal-title":"J. Comp. Physiol. A Neuroethol. Sens. Neural."},{"key":"2021042509031751200_JEB119552C20","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1086\/512136","article-title":"Communication of male quality in owl hoots","volume":"169","author":"Hardouin","year":"2007","journal-title":"Am. Nat."},{"key":"2021042509031751200_JEB119552C21","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1111\/j.1600-048X.2013.00144.x","article-title":"Anatomical bases of sex- and size-related acoustic variation in herring gull alarm calls","volume":"45","author":"Hardouin","year":"2014","journal-title":"J. Avian Biol."},{"key":"2021042509031751200_JEB119552C22","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1111\/j.1439-0310.2006.01247.x","article-title":"Black and White colobus monkey (Colobus guereza) roars as a source of both honest and exaggerated information about body mass","volume":"112","author":"Harris","year":"2006","journal-title":"Ethology"},{"key":"2021042509031751200_JEB119552C23","doi-asserted-by":"publisher","first-page":"1201","DOI":"10.1121\/1.396621","article-title":"The acoustics of the vocal tract in the horseshoe bat, Rhinolophus hildebrandti","volume":"84","author":"Hartley","year":"1988","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C24","unstructured":"Herrsch, G. L.\n           (1966). Bird voices and resonant tuning in helium air mixtures. PhD thesis, University of California, Berkeley."},{"key":"2021042509031751200_JEB119552C25","first-page":"294","article-title":"Vocalizations in juvenile crocodilians","volume":"44","author":"Herzog","year":"1977","journal-title":"Zeitschrift Fur Tierpsychologie-J. Comp. Ethol."},{"key":"2021042509031751200_JEB119552C26","doi-asserted-by":"publisher","first-page":"429","DOI":"10.2307\/2406936","article-title":"Tracheal dead space in the respiration of birds","volume":"25","author":"Hinds","year":"1971","journal-title":"Evolution"},{"key":"2021042509031751200_JEB119552C27","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1121\/1.1918935","article-title":"Helium speech","volume":"36","author":"Holywell","year":"1964","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C28","doi-asserted-by":"publisher","first-page":"1256","DOI":"10.1111\/jeb.12397","article-title":"Migrate small, sound big: functional constraints on body size promote tracheal elongation in cranes","volume":"27","author":"Jones","year":"2014","journal-title":"J. Evol. Biol."},{"key":"2021042509031751200_JEB119552C29","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1002\/ajpa.22124","article-title":"Soprano singing in gibbons","volume":"149","author":"Koda","year":"2012","journal-title":"Am. J. Phys. Anthropol."},{"key":"2021042509031751200_JEB119552C30","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1098\/rsbl.2011.0701","article-title":"Dolphin whistles: a functional misnomer revealed by heliox breathing","volume":"8","author":"Madsen","year":"2012","journal-title":"Biol. Lett."},{"key":"2021042509031751200_JEB119552C31","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1111\/j.1469-7998.2006.00144.x","article-title":"Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies","volume":"270","author":"McElligott","year":"2006","journal-title":"J. Zool."},{"key":"2021042509031751200_JEB119552C32","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1111\/j.0908-8857.2007.03695.x","article-title":"Allometry, bilateral asymmetry and sexual differences in the vocal tract of common eiders Somateria mollissima and king eiders S. spectabilis","volume":"38","author":"Miller","year":"2007","journal-title":"J. Avian Biol."},{"key":"2021042509031751200_JEB119552C33","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1038\/325053a0","article-title":"Vocal tract resonances in oscine bird sound production: evidence from birdsongs in a helium atmosphere","volume":"325","author":"Nowicki","year":"1987","journal-title":"Nature"},{"key":"2021042509031751200_JEB119552C34","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1086\/physzool.66.5.30163824","article-title":"Frogs in helium: the anuran vocal sac is not a cavity resonator","volume":"66","author":"Rand","year":"1993","journal-title":"Physiol. Zool."},{"key":"2021042509031751200_JEB119552C35","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1006\/anbe.2003.2078","article-title":"Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags","volume":"65","author":"Reby","year":"2003","journal-title":"Anim. Behav."},{"key":"2021042509031751200_JEB119552C36","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1098\/rspb.2004.2954","article-title":"Red deer stags use formants as assessment cues during intrasexual agonistic interactions","volume":"272","author":"Reby","year":"2005","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"2021042509031751200_JEB119552C37","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1002\/ar.1090920308","article-title":"The laryngeal region of Alligator mississippiensis","volume":"92","author":"Reese","year":"1945","journal-title":"Anat. Rec."},{"key":"2021042509031751200_JEB119552C38","doi-asserted-by":"crossref","first-page":"2859","DOI":"10.1242\/jeb.202.20.2859","article-title":"Vocal tract length and acoustics of vocalization in the domestic dog (Canis familiaris)","volume":"202","author":"Riede","year":"1999","journal-title":"J. Exp. Biol."},{"key":"2021042509031751200_JEB119552C39","first-page":"27","article-title":"Cavity resonances in the production of orientation cries","volume":"75","author":"Roberts","year":"1973","journal-title":"Periodicum Biologorum"},{"key":"2021042509031751200_JEB119552C40","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/0041-624X(75)90052-9","article-title":"Rodent ultrasound production mechanism","volume":"13","author":"Roberts","year":"1975","journal-title":"Ultrasonics"},{"key":"2021042509031751200_JEB119552C41","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1111\/j.1469-7998.2009.00661.x","article-title":"The contribution of source-filter theory to mammal vocal communication research","volume":"280","author":"Taylor","year":"2010","journal-title":"J. Zool."},{"key":"2021042509031751200_JEB119552C42","volume-title":"Principles of Voice Production","author":"Titze","year":"1994"},{"key":"2021042509031751200_JEB119552C43","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1007\/s002650050519","article-title":"Sex-biased dispersal in a long-lived polygynous reptile (Crocodylus johnstoni)","volume":"44","author":"Tucker","year":"1998","journal-title":"Behav. Ecol. Sociobiol."},{"key":"2021042509031751200_JEB119552C44","doi-asserted-by":"publisher","first-page":"e3113","DOI":"10.1371\/journal.pone.0003113","article-title":"Low frequency groans indicate larger and more dominant fallow deer (Dama dama) males","volume":"3","author":"Vannoni","year":"2008","journal-title":"PLoS ONE"},{"key":"2021042509031751200_JEB119552C45","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1111\/j.1469-185X.2009.00079.x","article-title":"Acoustic communication in crocodilians: from behaviour to brain","volume":"84","author":"Vergne","year":"2009","journal-title":"Biol. Rev."},{"key":"2021042509031751200_JEB119552C46","doi-asserted-by":"publisher","first-page":"1019","DOI":"10.1093\/icb\/29.3.1019","article-title":"Social displays of the American alligator (Alligator mississippiensis)","volume":"29","author":"Vliet","year":"1989","journal-title":"Amer. Zool."},{"key":"2021042509031751200_JEB119552C47","doi-asserted-by":"publisher","first-page":"2984","DOI":"10.1121\/1.2714910","article-title":"Acoustic signals of Chinese alligators (Alligator sinensis): social communication","volume":"121","author":"Wang","year":"2007","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C48","doi-asserted-by":"publisher","first-page":"832","DOI":"10.1111\/j.1439-0310.2009.01671.x","article-title":"Response specificity to advertisement vocalization in the Chinese alligator (Alligator sinensis)","volume":"115","author":"Wang","year":"2009","journal-title":"Ethology"},{"key":"2021042509031751200_JEB119552C49","doi-asserted-by":"publisher","first-page":"2082","DOI":"10.1121\/1.3203667","article-title":"Why do Chinese alligators (Alligator sinensis) form bellowing choruses: A playback approach","volume":"126","author":"Wang","year":"2009","journal-title":"J. Acoust. Soc. Am."},{"key":"2021042509031751200_JEB119552C50","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1071\/WR9830407","article-title":"Crocodylus johnstoni in the McKinlay River Area N. T, V.* Abnormalities and injuries","volume":"10","author":"Webb","year":"1983","journal-title":"Wildl. Res."},{"key":"2021042509031751200_JEB119552C51","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1017\/S0094837300004036","article-title":"Acoustic analyses of potential vocalization in Lambeosaurine dinosaurs (Reptilia, Ornithischia)","volume":"7","author":"Weishampel","year":"1981","journal-title":"Paleobiology"}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/218\/15\/2442\/1888653\/jeb119552.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/218\/15\/2442\/1888653\/jeb119552.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,25]],"date-time":"2021-04-25T10:28:53Z","timestamp":1619346533000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/218\/15\/2442\/14244\/A-Chinese-alligator-in-heliox-formant-frequencies"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,8,1]]},"references-count":51,"journal-issue":{"issue":"15","published-print":{"date-parts":[[2015,8,1]]}},"URL":"https:\/\/doi.org\/10.1242\/jeb.119552","relation":{},"ISSN":["1477-9145","0022-0949"],"issn-type":[{"value":"1477-9145","type":"electronic"},{"value":"0022-0949","type":"print"}],"subject":[],"published":{"date-parts":[[2015,8,1]]}}}