Abstract
In male European red deer Cervus elaphus, rutting calls that are responsible for male reproductive success are higher in fundamental frequency in captivity than in the wild. This study compares the acoustics of stag rutting calls among wild-living, semi-captive and captive stags within an Asian subspecies of C. elaphus, the Siberian wapiti Cervus elaphus sibiricus. Male Siberian wapiti rutting calls (bugles) were collected using automated recording systems in three populations (wild-living, semi-captive and captive), all originated from the Altai/Khakasian region of Central Siberia (Russia). Selected 435 bugles (145 per population) were analysed spectrographically for 14 variables of the bugle high (>1 kHz) fundamental frequency (g0) and scored for shape of g0 contour: trapeze, descending or saddle. Among bugles, 74.3% had the trapeze contour, 23.7% had the descending contour and 2.1% had the saddle contour. The additional low (<0.2 kHz) fundamental frequency (f0) was found in 76.1% of bugles, whereas deterministic chaos was found in 16.8% of bugles. Bugles of captive stags were shortest and highest in frequency. The captive management selectively affected only bugles with the trapeze contour, whereas bugles with descending contour remained unaffected by variations of deer holding regime. Stag rutting bugles are subspecies-specific and may therefore serve as acoustic indicator of subspecies for the Siberian wapiti among other Asian and American subspecies of wapiti.
Similar content being viewed by others
References
Barelli C, Mundry R, Heistermann M, Hammerschmidt K (2013) Cues to androgens and quality in male gibbon songs. PLoS One 8(12):e82748. doi:10.1371/journal.pone.0082748
Bartoš L, Šustr P, Janovský P, Bertagnoli J (2003) Sika deer (Cervus nippon) lekking in a free-ranging population in northern Austria. Folia Zool 52:1–10
Bocci A, Telford M, Laiolo P (2013) Determinants of the acoustic behaviour of red deer during breeding in a wild alpine population, and implications for species survey. Ethol Ecol Evol 25:52–69
Boersma P, Weenink D (2013) Praat: doing phonetics by computer. Version 5.3.51. http://www.praat.org/
Bowyer TR, Kitchen DW (1987) Sex and age-class differences in vocalization of Roosevelt elk during rut. Am Midl Nat 118:225–235
Briefer EF (2012) Vocal expression of emotions in mammals: mechanisms of production and evidence. J Zool 288:1–20
Briefer EF, Tettamanti F, McElligott AG (2015) Emotions in goats: mapping physiological, behavioural and vocal profiles. Anim Behav 99:131–143
Catchpole EA, Fan Y, Morgan BJT, Clutton-Brock TH, Coulson T (2004) Sexual dimorphism, survival and dispersal in red deer. J Agr Biol Env Stat 9:1–26
Charlton BD, Reby D (2011) Context-related acoustic variation in male fallow deer (Dama dama) groans. PLoS One 6(6):e21066. doi:10.1371/journal.pone.0021066
Clutton-Brock TH, Albon SD (1979) The roaring of red deer and the evolution of honest advertising. Behaviour 69:145–170
Clutton-Brock TH, Major M, Albon SD, Guinness FE (1987) Early development and population dynamics in red deer. I. Density-dependent effects on juvenile survival. J Anim Ecol 56:53–67
Clutton-Brock TH, Coulson TN, Milner-Gulland EJ, Thomson D, Armstrong HM (2002) Sex differences in emigration and mortality affect optimal management of deer populations. Nature 415:633–637
Coulson TN, Albon SD, Guinness FE, Pemberton JP, Clutton-Brock TH (1997) Population sub-stucture, local density and calf winter survival in red deer (Cervus elaphus). Ecology 78:852–863
Coulson T, Guinness F, Pemberton J, Clutton-Brock T (2004) The demographic consequences of releasing a population of red deer from culling. Ecology 85:411–422
Della Libera M, Passilongo D, Reby D (2015) The acoustics of male rutting roars in the endangered population of Mesola red deer Cervus elaphus italicus. Mammal Biol 80:395–400
Fedosenko AK (1980) The maral (ecology, behaviour, management). Nauka, Alma-Ata [in Russian]
Feighny JA, Williamson KE, Clarke JA (2006) North American elk bugle vocalizations: male and female bugle call structure and context. J Mammal 87:1072–1077
Frey R, Riede T (2013) The anatomy of vocal divergence in North American elk and European red deer. J Morphol 274:307–319
Frey R, Volodin IA, Volodina EV, Carranza J, Torres-Porras J (2012) Vocal anatomy, tongue protrusion behaviour and the acoustics of rutting roars in free-ranging Iberian red deer stags (Cervus elaphus hispanicus). J Anat 220:271–292
Frey R, Volodin IA, Fritsch G, Volodina EV (2016) Potential sources of high frequency and biphonic vocalization in the dhole (Cuon alpinus). PLoS One 11(1):e0146330. doi:10.1371/journal.pone.0146330
Hall SJG, Vince MA, Walser ES, Garson PJ (1988) Vocalisations of the Chillingham cattle. Behaviour 104:78–104
Herbst CT (2014) Glottal efficiency of periodic and irregular in vitro red deer voice production. Acta Acustica united with Acustica 100:724–733
Kazakov AP (2012) Census of maral (Cervus elaphus sibiricus Severtzov, 1873) population in Republik of Khakasia. Curremt problems of nature management, game management and game animal breeding 1:533–534
Kidjo N, Cargnelutti B, Charlton BD, Wilson C, Reby D (2008) Vocal behaviour in the endangered Corsican deer: description and phylogenetic implications. Bioacoustics 18:159–181
Kim YH, Lee JW, Chae S, Moon SH, Do EJ, Oh SE, Zhang GJ, Lee MY (2015) Development of a PCR-based assay to differentiate Cervus elaphus sibiricus from Cervus antlers. J Korean Soc Appl Biol Chem 58:61–66
Kuznetsova MV, Danilkin AA, Kholodova MV (2012) Phylogeography of red deer (Cervus elaphus): analysis of mtDNA cytochrome b polymorphism. Biol Bull 39:323–330
Long AM, Moore NP, Hayden TJ (1998) Vocalizations in red deer (Cervus elaphus), sika deer (Cervus nippon), and red × sika hybrids. J Zool 224:123–134
Lunitsin VG, Borisov NP (2012) Deer management for velvet antlers production in Russia. VNIIPO, Barnaul [In Russian]
Manteuffel G, Puppe B, Schön PC (2004) Vocalization of farm animals as a measure of welfare. Appl Anim Behav Sci 88:163–182
McComb K (1987) Roaring by red deer stags advances the date of oestrus in hinds. Nature 330:648–649
Nikol'skii AA (1975) Basic patterns of male Bactrian red deer (Cervus elaphus bactrianus) rutting calls. Zool Zh 54:1897–1900 [in Russian]
Nikol'skii AA (2011) The effect of amplitude modulation on the spectrum structure of the red deer sound signal. Doklady Biol Sci 437:107–109
Nikol'skii AA, Pereladova OB, Rutovskaja MV, Formozov NA (1979) The geographical variability of rut calls in red deer males. Bull Moscow Soc Natur Biol 84(6):46–55 [in Russian]
Nussey DH, Pemberton J, Donald A, Kruuk LEB (2006) Genetic consequences of human management in an introduced island population of red deer (Cervus elaphus). Heredity 97:56–65
Padilla de la Torre M, Briefer EF, Reader T, McElligott AG (2015) Acoustic analysis of cattle (Bos taurus) mother–offspring contact calls from a source–filter theory perspective. Appl Anim Behav Sci 163:58–68
Passilongo D, Reby D, Carranza J, Apollonio M (2013) Roaring high and low: composition and possible functions of the Iberian stag’s vocal repertoire. PLoS One 8(5):e63841. doi:10.1371/journal.pone.0063841
Reby D, McComb K (2003) Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim Behav 65:519–530
Reby D, McComb K, Cargnelutti B, Darwin CJ, Fitch WT, Clutton-Brock TH (2005) Red deer stags use formants as assessment cues during intra-sexual agonistic interactions. Proc R Soc Lond B 272:941–947
Reby D, Wyman MT, Frey R, Passilongo D, Gilbert J, Locatelli Y, Charlton BD (2016) Evidence of biphonation and source–filter interactions in the bugles of male North American wapiti (Cervus canadensis). J Exp Biol 219:1224–1236
Riede T, Titze IR (2008) Vocal fold elasticity of the Rocky Mountain elk (Cervus elaphus nelsoni) - producing high fundamental frequency vocalization with a very long vocal fold. J Exp Biol 211:2144–2154
Riede T, Lingle S, Hunter E, Titze IR (2010) Cervids with different vocal behavior demonstrate different visco-elastic properties of their vocal folds. J Morphol 271:1–11
Robbins JA, von Keyserlingk MAG, Fraser D, Weary DM (2016) Farm size and animal welfare. J Anim Sci 94:5439–5455
Sibiryakova OV, Volodin IA, Matrosova VA, Volodina EV, Garcia AJ, Gallego L, Landete-Castillejos T (2015) The power of oral and nasal calls to discriminate individual mothers and offspring in red deer, Cervus elaphus. Front Zool 12:2. doi:10.1186/s12983-014-0094-5
Sibiryakova OV, Volodin IA, Frey R, Zuther S, Kisebaev TB, Salemgareev AR, Volodina EV (2017) Remarkable vocal identity in wild-living mother and neonate saiga antelopes: a specialization for breeding in huge aggregations? Sci Nat 104:11. doi:10.1007/s00114-017-1433-0
Stepanova VV (2010) Expansion of geographic range of red deer in Yakutia. Russ J Biol Invasions 1:30–36
Struhsaker TT (1968) The behavior of the elk (Cervus canadensis) during the rut. Z Tierpsychol 24:80–114
Titze IR, Riede T (2010) A cervid vocal fold model suggests greater glottal efficiency in calling at high frequencies. PLoS Comp Biol 6(8):e1000897. doi:10.1371/journal.pcbi.1000897
Volodin IA, Volodina EV (2002) Biphonation as a prominent feature of the dhole Cuon alpinus sounds. Bioacoustics 13:105–120
Volodin IA, Volodina EV, Frey R, Carranza J, Torres-Porras J (2013a) Spectrographic analysis points to source-filter coupling in rutting roars of Iberian red deer. Acta Ethol 16:57–63
Volodin IA, Volodina EV, Frey R, Maymanakova IL (2013b) Vocal activity and acoustic structure of the rutting calls of Siberian wapiti (Cervus elaphus sibiricus) and their imitation with a hunting luring instrument. Russ J Theriol 12:99–106
Volodin IA, Matrosova VA, Volodina EV, Garcia AJ, Gallego L, Márquez R, Llusia D, Beltrán JF, Landete-Castillejos T (2015a) Sex and age-class differences in calls of Iberian red deer during rut: reversed sex dimorphism of pitch and contrasting roars from farmed and wild stags. Acta Ethol 18:19–29
Volodin IA, Volodina EV, Sibiryakova OV, Naidenko SV, Hernandez-Blanco JA, Litvinov MN, Rozhnov VV (2015b) Vocal activity and the acoustic structure of rutting calls in red deer in the Russian Far East. Doklady Biol Sci 462:144–147
Volodin IA, Volodina EV, Golosova OS (2016a) Automated monitoring of vocal rutting activity in red deer (Cervus elaphus). Russ J Theriol 15:91–99
Volodin IA, Sibiryakova OV, Volodina EV (2016b) Sex and age-class differences in calls of Siberian wapiti Cervus elaphus sibiricus. Mammal Biol 81:10–20
Volodin IA, Volodina EV, Frey R (2017) Bull bellows and bugles: a remarkable convergence of low and high-frequency vocalizations between male domestic cattle Bos taurus and the rutting calls of Siberian and North American wapiti. Bioacoustics 26. doi:10.1080/09524622.2016.1275805
Watts JM, Stookey JM (1999) Effects of restraint and branding on rates and acoustic parameters of vocalization in beef cattle. Appl Anim Behav Sci 62:125–135
Wilden I, Herzel H, Peters G, Tembrock G (1998) Subharmonics, biphonation, and deterministic chaos in mammal vocalization. Bioacoustics 9:171–196
Acknowledgements
We thank the staff of Khakasskiy State Nature Reserve for help and support, and the owners of deer facilities for providing possibility to work in their farms. We thank the anonymous reviewer for the valuable comments to the manuscript. This study has been conducted in collaboration with the staff of Khakasskiy State Nature Reserve, in accordance to its Siberian wapiti research project and in accordance to ethical and animal welfare standards. In all deer facilities, animal disturbance was kept at minimum, as the recording has been conducted automatically in the absence of people. The study was supported by Russian Science Foundation, grant no. 14-14-00237 (for OSG, IAV and EVV).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Karol Zub
Electronic supplementary material
Supplementary Audio S1
Rutting bugles of male Siberian wapiti with trapeze contour, with descending contour and with saddle contour. (WAV 668 kb)
Rights and permissions
About this article
Cite this article
Golosova, O.S., Volodin, I.A., Isaeva, I.L. et al. Effects of free-ranging, semi-captive and captive management on the acoustics of male rutting calls in Siberian wapiti Cervus elaphus sibiricus . Mamm Res 62, 387–396 (2017). https://doi.org/10.1007/s13364-017-0322-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13364-017-0322-4