Nocturnal chats of farmed animals: non-rutting vocalisations of male Iberian red deer, Cervus elaphus hispanicus
Ilya A. Volodin A B * , Svetlana S. Gogoleva C , Andrés J. Garcia D , Tomás Landete-Castillejos D and Elena V. Volodina BA Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Vorobievy Gory, 12/1, Moscow 119234, Russia.
B Department of Behaviour and Behavioural Ecology of Mammals, Severtsov Institute of Ecology and Evolution, Leninskii pr. 33, Moscow 119071, Russia.
C Department of Tropical Ecology of Mammals, Severtsov Institute of Ecology and Evolution, Leninskii pr. 33, Moscow 119071, Russia.
D Animal Science Tech. Applied to Wildlife Research Group. IREC (UCLM-CSIC-JCCM), and Sec. Rec. Cinegéticos, IDR, UCLM, Albacete 02071, Spain.
Animal Production Science 63(16) 1687-1696 https://doi.org/10.1071/AN22188
Submitted: 16 February 2022 Accepted: 14 January 2023 Published: 20 February 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Captive environment may inhibit the emission of some call types by non-domesticated farm and zoo animals; so, their complete vocal repertoires remain unknown. Automated acoustic recording might help fill this gap of knowledge.
Aim: The aim of this study was to describe vocalisations of farmed Iberian red deer, Cervus elaphus hispanicus, stags out of the autumnal rutting period (in summer and in winter) applying the manual and automated acoustic recording.
Methods: In this pilot study, automated audio recording of undisturbed animals followed with spectrographic analysis showed hidden parts of social acoustic communication in farmed male Iberian red deer in non-breeding period.
Key results: We detected three call types (roars, contact calls and bellows). Stag contact calls and bellows were described in the first time in red deer. Non-rutting roars were acoustically similar with rutting roars reported for wild-living Iberian red deer stags but of lower-frequency than were stag rutting roars recorded on the same farm in previous studies. Stag contact calls were reminiscent of hind contact calls recorded on the same farm in previous studies, but lower in frequency and shorter. Stag bellows were acoustically similar with bellows of male domestic cattle.
Conclusion: This study reveals previously unknown parts of male red deer vocal repertoire.
Implications: The lack of certain components of behavioural and vocal repertoire may indicate potential welfare problems in farmed and zoo animals.
Keywords: acoustic communication, animal behaviour, animal welfare, automated recordings, call types, non-rutting period, red deer, stag calls.
References
Ababaikeri B, Abduriyim S, Tohetahong Y, Mamat T, Ahmat A, Halik M (2020) Whole-genome sequencing of Tarim red deer (Cervus elaphus yarkandensis) reveals demographic history and adaptations to an arid-desert environment. Frontiers in Zoology 17, 31| Whole-genome sequencing of Tarim red deer (Cervus elaphus yarkandensis) reveals demographic history and adaptations to an arid-desert environment.Crossref | GoogleScholarGoogle Scholar |
Baotic A, Sicks F, Stoeger AS (2015) Nocturnal ‘humming’ vocalizations: adding a piece to the puzzle of giraffe vocal communication. BMC Research Notes 8, 425
| Nocturnal ‘humming’ vocalizations: adding a piece to the puzzle of giraffe vocal communication.Crossref | GoogleScholarGoogle Scholar |
Bishop JC, Falzon G, Trotter M, Kwan P, Meek PD (2019) Livestock vocalisation classification in farm soundscapes. Computers and Electronics in Agriculture 162, 531–542.
| Livestock vocalisation classification in farm soundscapes.Crossref | GoogleScholarGoogle Scholar |
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. Ethology Ecology and Evolution 25, 52–69.
| Determinants of the acoustic behaviour of red deer during breeding in a wild alpine population, and implications for species survey.Crossref | GoogleScholarGoogle Scholar |
Bowyer RT, Kitchen DW (1987) Sex and age-class differences in vocalizations of Roosevelt elk during rut. The American Midland Naturalist 118, 225–235.
| Sex and age-class differences in vocalizations of Roosevelt elk during rut.Crossref | GoogleScholarGoogle Scholar |
Briefer EF (2012) Vocal expression of emotions in mammals: mechanisms of production and evidence. Journal of Zoology 288, 1–20.
| Vocal expression of emotions in mammals: mechanisms of production and evidence.Crossref | GoogleScholarGoogle Scholar |
Charlton BD, Reby D (2011) Context-related acoustic variation in male fallow deer (Dama dama) groans. PLoS ONE 6, e21066
| Context-related acoustic variation in male fallow deer (Dama dama) groans.Crossref | GoogleScholarGoogle Scholar |
Clutton-Brock TH, Albon SD (1979) The roaring of red deer and the evolution of honest advertisement. Behaviour 69, 145–170.
| The roaring of red deer and the evolution of honest advertisement.Crossref | GoogleScholarGoogle Scholar |
Couchoux C, Aubert M, Garant D, Réale D (2015) Spying on small wildlife sounds using affordable collar-mounted miniature microphones: an innovative method to record individual daylong vocalisations in chipmunks. Scientific Reports 5, 10118
| Spying on small wildlife sounds using affordable collar-mounted miniature microphones: an innovative method to record individual daylong vocalisations in chipmunks.Crossref | GoogleScholarGoogle Scholar |
Della Libera M, Passilongo D, Reby D (2015) Acoustics of male rutting roars in the endangered population of Mesola red deer Cervus elaphus italicus. Mammalian Biology 80, 395–400.
| Acoustics of male rutting roars in the endangered population of Mesola red deer Cervus elaphus italicus.Crossref | GoogleScholarGoogle Scholar |
Dillon WR, Goldstein M (1984) ‘Multivariate analysis: methods and applications.’ (Wiley: New York, NY, USA)
Doan K, Niedziałkowska M, Stefaniak K, Sykut M, Jędrzejewska B, Ratajczak-Skrzatek U, Piotrowska N, Ridush B, Zachos FE, Popović D, Baca M, Mackiewicz P, Kosintsev P, Makowiecki D, Charniauski M, Boeskorov G, Bondarev AA, Danila G, Kusak J, Rannamae E, Saarma U, Arakelyan M, Manaseryan N, Krasnodębski D, Titov V, Hulva P, Bălăsescu A, Trantalidou K, Dimitrijević V, Shpansky A, Kovalchuk O, Klementiev AM, Foronova I, Malikov DG, Juras A, Nikolskiy P, Grigoriev SE, Cheprasov MY, Novgorodov GP, Sorokin AD, Wilczyński J, Protopopov AV, Lipecki G, Stanković A (2022) Phylogenetics and phylogeography of red deer mtDNA lineages during the last 50 000 years in Eurasia. Zoological Journal of the Linnean Society 194, 431–456.
| Phylogenetics and phylogeography of red deer mtDNA lineages during the last 50 000 years in Eurasia.Crossref | GoogleScholarGoogle Scholar |
Feighny JA, Williamson KE, Clarke JA (2006) North American elk bugle vocalizations: male and female bugle call structure and context. Journal of Mammalogy 87, 1072–1077.
| North American elk bugle vocalizations: male and female bugle call structure and context.Crossref | GoogleScholarGoogle Scholar |
Frey R, Volodin I, Volodina E, 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). Journal of Anatomy 220, 271–292.
| Vocal anatomy, tongue protrusion behaviour and the acoustics of rutting roars in free-ranging Iberian red deer stags (Cervus elaphus hispanicus).Crossref | GoogleScholarGoogle Scholar |
Geist V, Bayer M (1988) Sexual dimorphism in the Cervidae and its relation to habitat. Journal of Zoology 214, 45–53.
| Sexual dimorphism in the Cervidae and its relation to habitat.Crossref | GoogleScholarGoogle Scholar |
Gogoleva SS, Volodina EV, Volodin IA, Kharlamova AV, Trut LN (2010) The gradual vocal responses to human-provoked discomfort in farmed silver foxes. Acta Ethologica 13, 75–85.
| The gradual vocal responses to human-provoked discomfort in farmed silver foxes.Crossref | GoogleScholarGoogle Scholar |
Gogoleva SS, Volodin IA, Volodina EV, Kharlamova AV, Trut LN (2013) Effects of selection for behavior, human approach mode and sex on vocalization in silver fox. Journal of Ethology 31, 95–100.
| Effects of selection for behavior, human approach mode and sex on vocalization in silver fox.Crossref | GoogleScholarGoogle Scholar |
Golosova OS, Volodin IA, Isaeva IL, Volodina EV (2017) Effects of free-ranging, semi-captive and captive management on the acoustics of male rutting calls in Siberian wapiti Cervus elaphus sibiricus. Mammal Research 62, 387–396.
| Effects of free-ranging, semi-captive and captive management on the acoustics of male rutting calls in Siberian wapiti Cervus elaphus sibiricus.Crossref | GoogleScholarGoogle Scholar |
Golosova OS, Kholodova MV, Volodin IA, Volodina EV, Likhatsky EY, Náhlik A, Tari T (2021) Vocal phenotype of male rutting roars and genetic markers delineate East European red deer (Cervus elaphus) from Central and West European populations. The Science of Nature 108, 30
| Vocal phenotype of male rutting roars and genetic markers delineate East European red deer (Cervus elaphus) from Central and West European populations.Crossref | GoogleScholarGoogle Scholar |
Gunderson HL, Mahan BR (1980) Analysis of sonagrams of American Bison (Bison bison). Journal of Mammalogy 61, 379–381.
| Analysis of sonagrams of American Bison (Bison bison).Crossref | GoogleScholarGoogle Scholar |
Hall SJG, Vince MA, Shillito Walser E, Garson PJ (1988) Vocalisations of the Chillingham cattle. Behaviour 104, 78–104.
| Vocalisations of the Chillingham cattle.Crossref | GoogleScholarGoogle Scholar |
Hu P, Shao Y, Xu J, Wang T, Li Y, Liu H, Rong M, Su W, Chen B, Cui S, Cui X, Yang F, Tamate H, Xing X (2019) Genome-wide study on genetic diversity and phylogeny of five species in the genus Cervus. BMC Genomics 20, 384
| Genome-wide study on genetic diversity and phylogeny of five species in the genus Cervus.Crossref | GoogleScholarGoogle Scholar |
Hurtado AM, Smith-Flueck JM, Black-Decima P (2012) Comparison of vocalisations of introduced European red deer stags (Cervus elaphus) in north-western Patagonia (Argentina) with native European populations. Animal Production Science 52, 714–719.
| Comparison of vocalisations of introduced European red deer stags (Cervus elaphus) in north-western Patagonia (Argentina) with native European populations.Crossref | GoogleScholarGoogle Scholar |
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.
| Vocal behaviour in the endangered Corsican deer: description and phylogenetic implications.Crossref | GoogleScholarGoogle Scholar |
Landete-Castillejos T, García A, Gómez JÁ, Molina A, Gallego L (2003) Subspecies and body size allometry affect milk production and composition, and calf growth in red deer: comparison of Cervus elaphus hispanicus and Cervus elaphus scoticus. Physiological and Biochemical Zoology 76, 594–602.
| Subspecies and body size allometry affect milk production and composition, and calf growth in red deer: comparison of Cervus elaphus hispanicus and Cervus elaphus scoticus.Crossref | GoogleScholarGoogle Scholar |
Laurijs KA, Briefer EF, Reimert I, Webb LE (2021) Vocalisations in farm animals: a step towards positive welfare assessment. Applied Animal Behaviour Science 236, 105264
| Vocalisations in farm animals: a step towards positive welfare assessment.Crossref | GoogleScholarGoogle Scholar |
Long AM, Moore NP, Hayden TJ (1998) Vocalizations in red deer (Cervus elaphus), sika deer (Cervus nippon), and red × sika hybrids. Journal of Zoology 244, 123–134.
| Vocalizations in red deer (Cervus elaphus), sika deer (Cervus nippon), and red × sika hybrids.Crossref | GoogleScholarGoogle Scholar |
Manteuffel G, Puppe B, Schön PC (2004) Vocalization of farm animals as a measure of welfare. Applied Animal Behaviour Science 88, 163–182.
| Vocalization of farm animals as a measure of welfare.Crossref | GoogleScholarGoogle Scholar |
McComb KE (1988) Roaring and reproduction in red deer (Cervus elaphus). Doctoral thesis, University of Cambridge.
Mcloughlin MP, Stewart R, McElligott AG (2019) Automated bioacoustics: methods in ecology and conservation and their potential for animal welfare monitoring. Journal of The Royal Society Interface 16, 20190225
| Automated bioacoustics: methods in ecology and conservation and their potential for animal welfare monitoring.Crossref | GoogleScholarGoogle Scholar |
Meiri M, Kosintsev P, Conroy K, Meiri S, Barnes I, Lister A (2018) Subspecies dynamics in space and time: a study of the red deer complex using ancient and modern DNA and morphology. Journal of Biogeography 45, 367–380.
| Subspecies dynamics in space and time: a study of the red deer complex using ancient and modern DNA and morphology.Crossref | GoogleScholarGoogle Scholar |
Mota-Rojas D, Broom DM, Orihuela A, Velarde A, Napolitano F, Alonso-Spilsbury M (2020) Effects of human–animal relationship on animal productivity and welfare. Journal of Animal Behaviour and Biometeorology 8, 196–205.
| Effects of human–animal relationship on animal productivity and welfare.Crossref | GoogleScholarGoogle Scholar |
Murie OJ (1932) Elk calls. Journal of Mammalogy 13, 331–336.
| Elk calls.Crossref | GoogleScholarGoogle Scholar |
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. Applied Animal Behaviour Science 163, 58–68.
| Acoustic analysis of cattle (Bos taurus) mother–offspring contact calls from a source–filter theory perspective.Crossref | GoogleScholarGoogle Scholar |
Padilla de la Torre M, Briefer EF, Ochocki BM, McElligott AG, Reader T (2016) Mother–offspring recognition via contact calls in cattle, Bos taurus. Animal Behaviour 114, 147–154.
| Mother–offspring recognition via contact calls in cattle, Bos taurus.Crossref | GoogleScholarGoogle Scholar |
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, e63841
| Roaring high and low: composition and possible functions of the Iberian stag’s vocal repertoire.Crossref | GoogleScholarGoogle Scholar |
Reby D, McComb K (2003) Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Animal Behaviour 65, 519–530.
| Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags.Crossref | GoogleScholarGoogle Scholar |
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). Journal of Experimental Biology 219, 1224–1236.
| Evidence of biphonation and source–filter interactions in the bugles of male North American wapiti (Cervus canadensis).Crossref | GoogleScholarGoogle Scholar |
Riede T, Lingle S, Hunter EJ, Titze IR (2010) Cervids with different vocal behavior demonstrate different viscoelastic properties of their vocal folds. Journal of Morphology 271, 1–11.
| Cervids with different vocal behavior demonstrate different viscoelastic properties of their vocal folds.Crossref | GoogleScholarGoogle Scholar |
Rusin IY, Volodin IA, Sitnikova EF, Litvinov MN, Andronova RS, Volodina EV (2021) Roaring dynamics in rutting male red deer Cervus elaphus from five Russian populations. Russian Journal of Theriology 20, 44–58.
| Roaring dynamics in rutting male red deer Cervus elaphus from five Russian populations.Crossref | GoogleScholarGoogle Scholar |
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. Frontiers in Zoology 12, 2
| The power of oral and nasal calls to discriminate individual mothers and offspring in red deer, Cervus elaphus.Crossref | GoogleScholarGoogle Scholar |
Sibiryakova OV, Volodin IA, Volodina EV (2018) Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus. Ethology 124, 733–742.
| Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus.Crossref | GoogleScholarGoogle Scholar |
Solow AR (1990) A randomization test for misclassification probability in discriminant analysis. Ecology 71, 2379–2382.
| A randomization test for misclassification probability in discriminant analysis.Crossref | GoogleScholarGoogle Scholar |
Struhsaker TT (1967) Behavior of the elk (Cervus canadensis) during the rut. Zeitschrift für Tierpsychologie 24, 80–114.
| Behavior of the elk (Cervus canadensis) during the rut.Crossref | GoogleScholarGoogle Scholar |
Studd EK, Derbyshire RE, Menzies AK, Simms JF, Humphries MM, Murray DL, Boutin S (2021) The Purr-fect catch: using accelerometers and audio recorders to document kill rates and hunting behaviour of a small prey specialist. Methods in Ecology and Evolution 12, 1277–1287.
| The Purr-fect catch: using accelerometers and audio recorders to document kill rates and hunting behaviour of a small prey specialist.Crossref | GoogleScholarGoogle Scholar |
Vaňkova D, Málek J (1997) Characteristics of the vocalizations of red deer Cervus elaphus hinds and calves. Bioacoustics 7, 281–289.
| Characteristics of the vocalizations of red deer Cervus elaphus hinds and calves.Crossref | GoogleScholarGoogle Scholar |
Vaňková D, Bartoš L, Málek J (1997) The role of vocalization in the communication between red deer hinds and calves. Ethology 103, 795–808.
| The role of vocalization in the communication between red deer hinds and calves.Crossref | GoogleScholarGoogle Scholar |
Volodin I, Volodina E, Frey R, Carranza J, Torres-Porras J (2013a) Spectrographic analysis points to source-filter coupling in rutting roars of Iberian red deer. Acta Ethologica 16, 57–63.
| Spectrographic analysis points to source-filter coupling in rutting roars of Iberian red deer.Crossref | GoogleScholarGoogle Scholar |
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. Russian Journal of Theriology 12, 99–106.
| Vocal activity and acoustic structure of the rutting calls of Siberian wapiti (Cervus elaphus sibiricus) and their imitation with a hunting luring instrument.Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Matrosova VA, Volodina EV, Garcia AJ, Gallego L, Márquez R, Llusia D, Beltrán JF, Landete-Castillejos T (2015) Sex and age-class differences in calls of Iberian red deer during the rut: reversed sex dimorphism of pitch and contrasting roars from farmed and wild stags. Acta Ethologica 18, 19–29.
| Sex and age-class differences in calls of Iberian red deer during the rut: reversed sex dimorphism of pitch and contrasting roars from farmed and wild stags.Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Sibiryakova OV, Volodina EV (2016) Sex and age-class differences in calls of Siberian wapiti Cervus elaphus sibiricus. Mammalian Biology 81, 10–20.
| Sex and age-class differences in calls of Siberian wapiti Cervus elaphus sibiricus.Crossref | GoogleScholarGoogle Scholar |
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, 271–284.
| 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.Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Sibiryakova OV, Vasilieva NA, Volodina EV, Matrosova VA, Garcia AJ, Pérez-Barbería FJ, Gallego L, Landete-Castillejos T (2018a) Old and young female voices: effects of body weight, condition and social discomfort on the vocal aging in red deer hinds (Cervus elaphus). Behaviour 155, 915–939.
| Old and young female voices: effects of body weight, condition and social discomfort on the vocal aging in red deer hinds (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Sibiryakova OV, Vasilieva NA, Volodina EV, Matrosova VA, Garcia AJ, Pérez-Barbería FJ, Gallego L, Landete-Castillejos T (2018b) Between-year vocal aging in female red deer (Cervus elaphus). BMC Research Notes 11, 737
| Between-year vocal aging in female red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Matrosova VA, Frey R, Kozhevnikova JD, Isaeva IL, Volodina EV (2018c) Altai pika (Ochotona alpina) alarm calls: individual acoustic variation and the phenomenon of call-synchronous ear folding behavior. The Science of Nature 105, 40
| Altai pika (Ochotona alpina) alarm calls: individual acoustic variation and the phenomenon of call-synchronous ear folding behavior.Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Nahlik A, Tari T, Frey R, Volodina EV (2019a) Rutting roars in native Pannonian red deer of Southern Hungary and the evidence of acoustic divergence of male sexual vocalization between Eastern and Western European red deer (Cervus elaphus). Mammalian Biology 94, 54–65.
| Rutting roars in native Pannonian red deer of Southern Hungary and the evidence of acoustic divergence of male sexual vocalization between Eastern and Western European red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Sibiryakova OV, Soldatova NV, Volodina EV (2019b) Acoustically different contact calls of mother and young goitred gazelle are equally individualized: is this a common relationship in ruminants? Behaviour 156, 1185–1207.
| Acoustically different contact calls of mother and young goitred gazelle are equally individualized: is this a common relationship in ruminants?Crossref | GoogleScholarGoogle Scholar |
Volodin IA, Volodina EV, Rutovskaya MV (2022) Camel whistling vocalisations: male and female call structure and context in Camelus bactrianus and Camelus dromedarius. Bioacoustics 31, 132–147.
| Camel whistling vocalisations: male and female call structure and context in Camelus bactrianus and Camelus dromedarius.Crossref | GoogleScholarGoogle Scholar |
Volodina EV, Volodin IA, Chelysheva EV, Frey R (2018) Hiss and snort call types of wild-living giraffes Giraffa camelopardalis: acoustic structure and context. BMC Research Notes 11, 12
| Hiss and snort call types of wild-living giraffes Giraffa camelopardalis: acoustic structure and context.Crossref | GoogleScholarGoogle Scholar |
Watts JM, Stookey JM (1999) Effects of restraint and branding on rates and acoustic parameters of vocalization in beef cattle. Applied Animal Behaviour Science 62, 125–135.
| Effects of restraint and branding on rates and acoustic parameters of vocalization in beef cattle.Crossref | GoogleScholarGoogle Scholar |
Wilson MW, Ridlon AD, Gaynor KM, Gaines SD, Stier AC, Halpern BS (2020) Ecological impacts of human-induced animal behaviour change. Ecology Letters 23, 1522–1536.
| Ecological impacts of human-induced animal behaviour change.Crossref | GoogleScholarGoogle Scholar |
Zulkifli I (2013) Review of human-animal interactions and their impact on animal productivity and welfare. Journal of Animal Science and Biotechnology 4, 25
| Review of human-animal interactions and their impact on animal productivity and welfare.Crossref | GoogleScholarGoogle Scholar |