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Zoo and wildlife management faces a problem with bird sexing,as many bird taxa have indiscernible gender differences in size and coloration. Problematic groups are geese,cranes,rails,raptors,owls,parrots,doves,auks,shearwaters and some passerines. Commonly accepted invasive sexing techniques based on genetics,laparoscopy,morphometric and on cloacal inspection,are all needed in bird capturing and handling. Capturing and subsequent manipulations may be inapplicable for free-ranging birds,whereas distant voice-based sexing is relevant for many species. This review evaluates the potential for noninvasive sexing by separate calls or duet calls,for adult birds of 69 species from 16 orders and for chicks of 11 species from 7 orders. For adult birds of 25 species,a single call per individual was sufficient for 100 % reliable sexing by ear or using spectrographic analysis. For chicks,the potential for voice-based sexing seems to be very limited. For birds calling rarely or unpredictably,we propose a simple way of provoking vocalization using playbacks of species-specific calls that are available from sound libraries. We conclude that sexing by voice may represent a feasible alternative to the classical sexing techniques,both in the wild and in captivity.


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Gender identification using acoustic analysis in birds without external sexual dimorphism

Show Author's information Ilya A. Volodin1,2( )Elena V. Volodina2Anna V. Klenova1Vera A. Matrosova3Ilya A. Volodin1,2( )Elena V. Volodina2Anna V. Klenova1Vera A. Matrosova3
Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Vorobievy Gory, 12/1, Moscow 119991, Russia
Scientific Research Department, Moscow Zoo, B. Gruzinskaya, 1, Moscow 123242, Russia
Engelhardt Institute of Molecular Biology RAS, Moscow, Russia

Abstract

Zoo and wildlife management faces a problem with bird sexing,as many bird taxa have indiscernible gender differences in size and coloration. Problematic groups are geese,cranes,rails,raptors,owls,parrots,doves,auks,shearwaters and some passerines. Commonly accepted invasive sexing techniques based on genetics,laparoscopy,morphometric and on cloacal inspection,are all needed in bird capturing and handling. Capturing and subsequent manipulations may be inapplicable for free-ranging birds,whereas distant voice-based sexing is relevant for many species. This review evaluates the potential for noninvasive sexing by separate calls or duet calls,for adult birds of 69 species from 16 orders and for chicks of 11 species from 7 orders. For adult birds of 25 species,a single call per individual was sufficient for 100 % reliable sexing by ear or using spectrographic analysis. For chicks,the potential for voice-based sexing seems to be very limited. For birds calling rarely or unpredictably,we propose a simple way of provoking vocalization using playbacks of species-specific calls that are available from sound libraries. We conclude that sexing by voice may represent a feasible alternative to the classical sexing techniques,both in the wild and in captivity.

Keywords: Vocalization, Monomorphic birds, Call-based sexing, Sexing by sound

References(120)

Archibald GW. The unison call of cranes as a useful taxonomic tool. 1976. PhD thesis. Cornell University, Ithaca, p 167.
Aubin T, Mathevon N, Staszewski V, Boulinier T. Acoustic communication in the Kittiwake Rissa tridactyla: potential cues for sexual and individual signatures in long calls. Polar Biol. 2007;30:1027-33.https://doi.org/10.1007/s00300-007-0262-6
DOI

Balkiz O, Dano S, Barbraund C, Tekin S, Özesmi U, Dündar M, Béchet A. Sexing greater flamingo chicks from feather bulb DNA. Waterbirds. 2007;30:450-3.

Ballintijn MR, ten Cate C. Sex differences in the vocalizations and syrinx of the collared dove (Streptopelia decaocto). Auk. 1997;114:22-39.

Baptista LF, Gaunt SLL. Bioacoustics as a tool in conservation studies. In: Clemmons JR, Buchholtz R, editors. Behavioral approaches to conservation in the wild. Cambridge: Cambridge University Press; 1997. p. 212-42.

Barbraud C, Mariani A, Jouventin P. Variation in call properties of the snow petrel, Pagodroma nivea, in relation to sex and body size. Aust J Zool. 2000;48:421-30.

Bazzano G, Lèche A, Martella MB, Navarro JL. Efficiency of the cloacal sexing technique in greater rhea chicks (Rhea americana). Brit Poult Sci. 2012;53(3):394-6.

Beja-Pereira A, Oliveira R, Alves PC, Schwartz MK, Luikart G. Advancing ecological understandings through technological transformations in noninvasive genetics. Mol Ecol Res. 2009;9:1279-301.

Berkunsky I, Mahler B, Reboreda JC. Sexual dimorphism and determination of sex by morphometrics in blue-fronted amazons (Amazona aestiva). Emu. 2009;109:192-7.

Boersma PD, Davies EM. Sexing monomorphic birds by vent measurements. Auk. 1987;104:779-83.

Bourgeois K, Cure C, Legrand J, Gomez-Diaz E, Vidal E, Aubin T, Mathevon N. Morphological versus acoustic analysis: what is the most efficient method for sexing yelkouan shearwaters Puffinus yelkouan? J Ornithol. 2007;148: 261-9.https://doi.org/10.1007/s10336-007-0127-3
DOI
Boyd JH. Taxonomy in flux: version 2.52c. 2013. http://jboyd.net/Taxo/List1.html.

Bragina EV, Beme IR. The sexual and individual differences in the vocal repertoire of adult Siberian cranes (Grus leucogeranus, Gruidae). Zoologicheskii Zhurnal. 2007;86:1468-81.

Bragina EV, Beme IR. Siberian crane duet as an individual signature of a pair: comparison of visual and statistical classification techniques. Acta Ethol. 2010;13:39-48.

Bragina EV, Beme IR. Sexual and individual features in the long-range and short-range calls of the white-naped crane. Condor. 2013;115:501-7.

Bretagnolle V. Behavioural affinities of the blue petrel Halobaena caerulea. Ibis. 1990;132:102-23.

Bretagnolle V, Genevois F. Geographic variation in the call of the blue petrel: effects of sex and geographical scale. Condor. 1997;99:985-9.

Bretagnolle V, Lequette B. Structural variation in the call of the Cory's shearwater (Calonectris diomedea, Aves, Procellariidae). Ethology. 1990;85:313-23.

Bretagnolle V, Thibault JC. Method for sexing fledglings in Cory's shearwaters and comments on sex-ratio variation. Auk. 1995;112:785-90.

Bretagnolle V, Zotier R, Jouventin P. Comparative population biology of four prions (genus Pachyptila) from the Indian Ocean and consequences for their taxonomic status. Auk. 1990;107:305-16.

Brooke ML. Sexual differences in the voice and individual recognition in the Manx shearwater (Puffinus puffinus). Anim Behav. 1978;26:622-9.

Brooke ML. Sexual dimorphism in the voice of the greater shearwater. Wilson Bull. 1988;100:319-23.

Brown AW, Brown LM, Stevick PT. Sexing mute swans Cygnus olor by discriminant analysis. Ring Migrat. 2003;21:174-80.

Buchanan OM. Homosexual behavior in wild orange-fronted parakeets. Condor. 1966;68:399-400.

Calabuig CP, Greenb AJ, Ferrera M, Muriela R, Moreirac H. Sexual size dimorphism and sex determination by morphometric measurements in the coscoroba swan. Stud Neotrop Fauna E. 2011;46:177-84.

Carlson G, Trost CH. Sex determination of the whooping crane by analysis of vocalizations. Condor. 1992;94:532-6.

Cavanagh PM, Ritchison G. Variation in the bounce and whinny songs of the Eastern screech-owl. Wilson Bull. 1987;99:620-7.

Clapperton BK. Sexual differences in pukeko calls. Notornis. 1983;30:69-70.

Conover MR. Parental care by male-female and female-female pairs of ringbilled gulls. Colon Waterbird. 1989;12:148-52.

Conover MR, Hunt GL. Experimental evidence that female-female pairs in gull result from a shortage of breeding males. Condor. 1984;86:472-6.

Copestake PG, Croxall JP, Prince PA. Use of cloacal sexing techniques in mark-recapture estimates of breeding population size in Wilson's storm petrel Oceanites oceanites in South Georgia. Polar Biol. 1988;8:271-9.

Cosens SE. Development of vocalizations in the American coot. Can J Zool. 1981;59:1921-8.

Craig JL, McArdle BH, Wetin PD. Sex determination of the pukeko or swamphen. Notornis. 1980;27:287-91.

Cure C, Aubin T, Mathevon N. Acoustic convergence and divergence in two sympatric burrowing nocturnal seabirds. Biol J Linn Soc. 2009;96:115-34.

Cure C, Aubin T, Mathevon N. Intra-sex vocal interactions in two hybridizing seabird species (Puffinus sp.). Behav Ecol Sociobiol. 2010;64:1823-37.

Cure C, Aubin T, Mathevon N. Sex discrimination and mate recognition by voice in the yelkouan shearwater Puffinus yelkouan. Bioacoustics. 2011;20:235-50.

Delport W, Kemp AC, Ferguson WH. Vocal identification of individual African wood owls Strix woodfordii: a technique to monitor long-term adult turnover and residency. Ibis. 2002;144:30-9.

Digby A, Bell BD, Teal PD. Vocal cooperation between the sexes in little spotted kiwi Apteryx owenii. Ibis. 2013;155:229-45.

Eda-Fujiwara H, Yamamoto A, Sugita H, Takahashi Y, Kojima Y, Sakashita R, Ogawa H, Miyamoto T, Kimura T. Sexual dimorphism of acoustic signals in the oriental white stork: non-invasive identification of sex in birds. Zool Sci. 2004;8:817-21.

Elie JE, Mathevon N, Vignal C. Same-sex pair-bonds are equivalent to male-female bonds in a life-long socially monogamous songbird. Behav Ecol Sociobiol. 2011;65:2197-208.

Fabricius E. Homosexualitet hos gragashanar Anser anser. Var Fagelwärld. 1981;40:427-46.

Farquahar C. Individual and intersexual variation in alarm calls of the white-tailed hawk. Condor. 1993;95:234-9.

Genevois F, Bretagnolle V. Sexual dimorphism of voice and morphology in the thin-billed prion (Pachyptila bekheri). Notornis. 1995;42:1-10.

Genovart M, McMinn M, Bowler D. A discriminant function for predicting sex in the Balearic shearwater. Waterbirds. 2003;26:72-6.

Gill FB, Stokes FJ, Stokes CC. Observations on the horned screamer. Wilson Bull. 1974;86:43-50.

Goller F, Riede T. Integrative physiology of fundamental frequency control in birds. J Physiol Paris. 2013;107:230-42.

Goncharova MV, Klenova AV, Bragina EV. Development of cues to individuality and sex in calls of three crane species: when is it good to be recognizable? J Ethol. 2015;33:165-75.

Grava T, Mathevon N, Place E, Balluet P. Individual acoustic monitoring of the European eagle owl Bubo bubo. Ibis. 2008;150:279-87.

Grecian VD, Diamond AW, Chardine JW. Sexing razorbills Alca torda breeding at Machias seal island, New Brunswick, Canada, using discriminant function analysis. Atlantic Seabirds. 2003;5:73-80.

Green PT. Sexing birds by discriminant analysis: further considerations. Ibis. 1989;131:442-7.

Griffiths R, Double MC, Orr K, Dawson R. A DNA test to sex most birds. Mol Ecol. 1998;7:1071-5.

Guallar S, Quesada J, Gargallo G, Herrando S, Romero JM. Use of discriminant analysis in the sex determination of passerines breeding in the western Mediterranean. Revista Catalana d'Ornitologia. 2010;26:38-50.

Gullion GW. Voice differences between sexes in the American coot. Condor. 1950;52:272-3.

Hanson HC. Methods of determining age in Canada geese and other waterfowl. J Wildl Manage. 1949;13:177-83.

Hardouin LA, Thompson R, Stenning M, Reby D. Anatomical bases of sex- and size-related acoustic variation in herring gull alarm calls. J Avian Biol. 2013;44:1-10.

Herting BL, Belthoff JR. Bounce and double trill songs of male and female western screech-owls: characterization and usefulness for classification of sex. Auk. 2001;118:1095-101.

Huchzermeyer FW. Diseases of Ostrich and Other Ratites. Pretoria: Agricultural Research Council; 1998.

Hunt GL, Newman AL, Warner MH, Wingfield JC, Kaiwi J. Comparative behavior of male-female and female-female pairs among western gulls prior to egg-laying. Condor. 1984;86:157-62.

James PC, Robertson HA. The calls of male and female Madeiran storm-petrels (Oceanodroma castro). Auk. 1985a;102:391-3.

James PC, Robertson HA. Sexual dimorphism in the voice of the little shearwater Puffinus assimilis. Ibis. 1985b;127:388-90.

James PC, Robertson HA. The call of bulwer's petrel (Bulweria bulwerii), and the relationship between intersexual call divergence and aerial calling in the nocturnal Procellariiformes. Auk. 1985c;102:878-82.

Janicke T, Ritz MS, Hahn S, Peter H-U. Sex recognition in brown skuas: do acoustic signals matter? J Ornithol. 2007;148:565-9.

Jensen T, Pernasetti FM, Durrant B. Conditions for rapid sex determination in 47 avian species by PCR of genomic DNA from blood, shell-membrane blood vessels, and feathers. Zoo Biol. 2003;22:561-71.

Johnsgard PA. Tracheal anatomy of the Anatidae and its taxonomic significance. Wildfowl Trust Ann Rep. 1961;12:58-69.

Klenova AV, Goncharova MV, Bragina EV, Kashentseva TA. Vocal development and voice breaking in Demoiselle Cranes (Anthropoides virgo). Bioacoustics. 2014;23:247-65.

Klenova AV, Volodin IA, Volodina EV. Duet structure provides information about pair identity in the red-crowned crane (Grus japonensis). J Ethol. 2008;26:317-25.

Klenova AV, Volodin IA, Volodina EV, Postelnykh KA. Voice breaking in adolescent red-crowned cranes (Grus japonenis). Behaviour. 2010;147:505-24.

Klenova AV, Zubakin VA, Zubakina EV, Kolesnikova YA. Indicators of individuality and sex in advertising calls of two closely related auklet species (Charadriiformes, Alcidae): crested auklet and parakeet auklet (Aethia cristatella, Cyclorhynchus psittacula). Zool Zh. 2012;91:869-80.

Koshmyanova NV, Tikhonov AV, Kharitonov SP. Spectro-temporal structure of alarm calls and sex differences in chicks of the black-headed gull (Larus ridibundus L.). Rep High Sch Biol Sci. 1984;6:30-3.

Krechmar EA. Alarm duets of white-fronted geese, Anser albifrons. Zool Zh. 2003;82:1239-49.

Lessells CM, Rowe CL, McGregor PK. Individual and sex differences in the provisioning calls of European bee-eaters. Anim Behav. 1995;49:244-7.

Livezey BC. A phylogenetic analysis and classification of recent dabbling ducks (Tribe Anatini) based on comparative morphology. Auk. 1991;108:471-507.

Livezey BC. A phylogenetic analysis of the whistling and white-backed ducks (Anatidae, Dendrocygninae) using morphological characters. Ann Carnegie Mus. 1995;64:65-97.

Malagó W, Medaglia A, Matheucci E, Henrique-Silva F. New PCR multiplexes for sex typing of ostriches. Braz J Biol. 2005;65:743-5.

Martin K, Cooke E. Bi-parental care in willow ptarmigan—a luxury? Anim Behav. 1987;35:369-79.

Martin K, Horn AG, Hannon SJ. The calls and associated behavior of breeding willow ptarmigan in Canada. Wilson Bull. 1995;107:496-509.

Matrosova VA, Volodin IA, Volodina EV, Vasilieva NA. Stability of acoustic individuality in the alarm calls of wild yellow ground squirrels Spermophilus fulvus and contrasting calls from trapped and free-ranging callers. Naturwissenschaften. 2010;97:707-15.

Maurer G, Smith C, Süsser M, Magrath RD. Solo and duet calling in the pheasant coucal: sex and individual call differences in a nesting cuckoo with reversed size dimorphism. Aust J Zool. 2008;56:143-9.

Miller WJ, Wagner FH. Sexing mature Columbiformes by cloacal characters. Auk. 1955;72:279-85.

Mizuta T, Yamada H, Lin RS, Yodogawa Y, Okanoya K. Sexing white-rumped munias in Taiwan, using morphology, DNA and distance calls. Ornithol Sci. 2003;2:97-102.

Monk DS, Koenig RD. Individual, brood and sex variation in begging calls of western bluebirds. Wilson Bull. 1997;109:328-32.

Morinha F, Cabral JA, Bastos E. Molecular sexing of birds: a comparative review of polymerase chain reaction (PCR)-based methods. Theriogenology. 2012;78:703-14.

Mudrik EA, Kashentseva TA, Gamburg EA, Gavrikova EY, Politov DV. Non-invasive method of sex identification of crane chicks by the DNA from capillary vessels of allantois. Russian J Devel Biol. 2013;44:279-82.

Mulard H, Aubin T, White JF, Wagner RH, Danchin E. Voice variance may signify ongoing divergence among black-legged kittiwake populations. Biol J Linn Soc. 2009;97:289-97.

Niemeier MM. Structural and functional aspects of vocal ontogeny in Grus canadensis (Gruidae: Aves). 1979. PhD thesis. University of Nebraska, Lincoln, p 135.

Nuechterlein GL, Buitron D. Vocal advertising and sex recognition in eared grebes. Condor. 1992;94:937-43.

O'Dwyer TW, Priddel D, Carlile N, Bartle JA, Buttemer WA. An evaluation of three field techniques for sexing Gould's petrels (Pterodroma leucoptera) (Procellariidae). Emu. 2006;106:245-52.

Odom KJ, Mennill DJ. A quantitative description of the vocalizations and vocal activity of the barred owl. Condor. 2010;112:549-60.

O'Huallachain D, Dunne J. Analysis of biometric data to determine the sex of woodpigeons Columba palumbus. Ring Migrat. 2010;25:29-32.

Penhallurick J. World Bird Info. 2013. http://www.worldbirdinfo.net/.

Purchase HG. Raising geese. Farmers Bull. 1978;2251:1-14.

Radford AN. Voice breaking in males results in sexual dimorphism of green woodhoopoe calls. Behaviour. 2004;141:555-69.

Radesäter T. On the ontogeny of orienting movements in the triumph ceremony in two species of geese (Anser anser L. and Branta canadensis L.). Behaviour. 1974;50:1-15.

Regnaut S, Lucas FS, Fumagalli L. DNA degradation in avian faecal samples and feasibility of non-invasive genetic studies of threatened capercaillie populations. Conserv Gen. 2006;7:449-53.

Richner H. Avian laparoscopy as a field technique for sexing birds and an assessment of its effects on wild birds. J Field Ornithol. 1989;60:137-42.

Saino N, de Ayala RM, Boncoraglio G, Martinelli R. Sex difference in mouth coloration and begging calls of barn swallow nestlings. Anim Behav. 2008;75:1375-82.

Saino N, Galeotti P, Sacchi R, Boncoraglio G, Martinelli R, Molle A. Sex differences in begging vocalizations of nestling barn swallows, Hirundo rustica. Anim Behav. 2003;66:1003-10.

Schwing R, Parsons S, Nelson XJ. Vocal repertoire of the New Zealand kea parrot Nestor notabilis. Curr Zool. 2012;58:727-40.

Serventy DL. A method of sexing petrels in field observations. Emu. 1956;56:213-4.

Simons TR. Behavior and attendance patterns of the fork-tailed storm petrel. Auk. 1981;98:145-58.

Smith GC, Jones DN. Vocalizations of the marbled frogmouth I: descriptions and an analysis of sex differences. Emu. 1997;97:290-5.

Soley JT, Groenewals HB. Reproduction. In: Deeming DC, editor. The Ostrich, Biology, Production and Health. New York: CABI Publishing; 1999. p. 129-58.

Steyn P, Scott J. Notes on the breeding biology of the wood owl. Ostrich. 1972;44:118-25.

Swanson DA, Rappole JH. Determining the sex of adult white-winged doves by cloacal characteristics. North Am Bird Bander. 1992;17:137-9.

Swengel SR. Sex determination. In: Ellis D, Gee G, Mirande C, editors. Cranes: their biology, husbandry, and conservation. Baraboo: ICF; 1996. p. 223-9.

Taoka M, Okumura H. Sexual differences in flight calls and the cue for vocal sex recognition of swinhoe's storm-petrels. Condor. 1990;92:571-5.

Taoka M, Sato T, Kamada T, Okumura H. Sexual dimorphism of chatter-calls and vocal sex recognition in Leach's storm-petrels (Oceanodroma leucorhoa). Auk. 1989a;106:498-501.

Taoka M, Won P-O, Okumura H. Vocal behavior of swinhoe's storm-petrel (Oceanodroma monorhis). Auk. 1989b;106:471-4.

ten Thoren A, Bergmann H-H. Die Entwicklung der Lautausserungen bei der Graugans (Anser anser). J Ornithol. 1987;128:181-207.

Tikhonov AV. Acoustic signalization and ecology of birds. Moscow: Moscow University Press; 1986. p. 236.

Turner L. A rapid method of sexing Canada geese. J Wildl Manage. 1953;17:542-3.

Venuto V, Ferraiuolo V, Bottoni L, Massa R. Distress call in six species of African Poicephalus parrots. Ethol Ecol Evol. 2001;13:49-68.

Volodin IA. Behavior repertoire of Rufibrenta ruficollis (Anserini, Anseriformes). 1. Locomotory behaviour. Zool Zh. 1990a; 69(9):57-66.

Volodin IA. Behavior repertoire of Rufibrenta ruficollis. 2. Acoustic behaviour. Zool Zh. 1990b; 69(10):98-106.
Volodin IA. Setting-up and maintaining social relations within groups of red-breasted geese (Rufibrenta rificollis Pall.) in captivity. Bull Soc Nat Moscow Biol B. 1990c;95(3):42-50.
Volodin IA, Volodina EV, Klenova AV. Non-invasive sex recognition in the white-faced whistling duck. Int Zoo News. 2003;50(3):160-7.

Volodin IA, Volodina EV, Matrosova VA, Kholodova MV. Bioacoustical sexing with playback-evoked loud whistles in the Cuban whistling duck Dendrocygna arborea. Sci Res Zool. 2005a;18:105-12.

Volodin I, Kaiser M, Matrosova V, Volodina E, Klenova A, Filatova O, Kholodova M. The technique of noninvasive distant sexing for four monomorphic Dendrocygna whistling duck species by their loud whistles. Bioacoustics. 2009;18:277-90.

Volodin IA, Klenova AV, Volodina EV. Modelling bioacoustical monitoring through years with captive population of the red-breasted goose. Casarca Bull Goose Swan Duck Study Group North Eurasia. 2008;11(1):22-46.

Volodin IA, Volodina EV, Klenova AV, Filatova OA. Individual and sexual differences in the calls of the monomorphic white-faced whistling duck Dendrocygna viduata. Acta Ornithol. 2005b;40:43-52.

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Publication history

Received: 22 October 2014
Accepted: 03 November 2015
Published: 13 November 2015
Issue date: January 2015

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© 2015 Volodin et al.

Acknowledgements

Acknowledgements

The authors are sincerely grateful to the anonymous reviewers for their valuable comments provided to the manuscript. This study was supported by the Russian Foundation for Basic Research (grants 12-04-00260a to IV, EV and VM and 12-04-00414a to AK, for studying the acoustic-based, laparoscopy and gene-based methods of sexing of a few Anseriformes, Gruidae and Alcidae species included in this review), by the President RF Foundation (Grant MK-1781.2012.4 to AK, for studying Alcidae species, also included in this review) and by the Russian Scientific Foundation (Grant No 14-14-00237) to IV, EV, AK and VM for completing the review.

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