Acoustic parameters of courtship and human-directed friendly vocalisations in seven species of Neotropical deer in captivity
Patricia Black-Décima A D , Alejandra M. Hurtado A , J. M. Barbanti Duarte B and Mirta Santana C
+ Author Affiliations
- Author Affiliations
A Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, Miguel Lillo 205, 4000 Tucumán, Argentina.
B Núcleo de Pesquisa e Conservacão de Cervídeos (NUPECCE), Universidade Estadual Paulista (Unesp), Faculdade de Ciências Agrárias e Veterinárias, Via de Acesso Paulo Donato Castellane, s/n, Jaboticabal, CEP 14884-900, Brazil.
C Facultad de Medicina, Universidad Nacional de Tucumán, Ayacucho 491, 4000 Tucumán, Argentina.
D Corresponding author. Email: blackpatricia@gmail.com
Animal Production Science 60(10) 1283-1291 https://doi.org/10.1071/AN19377
Submitted: 1 July 2019 Accepted: 29 November 2019 Published: 8 May 2020
Abstract
Context: Polygynous deer rut vocalisations have been found to be highly conspicuous, typical of the species and important in sexual selection. Information about vocalisations is not available for Neotropical species (subfamily Odocoileinae).
Aims: The objective was to record courtship vocalisations from all Neotropical deer available, looking for differences among species useful for taxonomic identification, characterise the vocalisations according to acoustic parameters and to try to determine functions.
Methods: Four species of brocket deer (red, Mazama americana (n = 9); grey, M. gouazoubira (n = 7); Amazonian brown, M. nemorivaga (n = 3); Brazilian dwarf, M. nana (n = 1)), and one individual each of marsh (Blastocerus dichotomus), white-tailed (Odocoileus virginianus) and taruca (Hippocamellus antisensis) deer were recorded in captivity at two institutions, in conditions of courtship or human interaction. The acoustic analysis was performed with Praat. Data from the first three species of Mazama were analysed statistically with a multilevel model with two layers.
Key results: In the context of courting either females or humans, male deer produced low-intensity, short-duration (0.1–0.3 s) bleats with fundamental frequencies (F0) between 100 and 400 Hz; calls were similar among species. The duration of these calls for Amazonian brown brocket males was significantly longer than for males of the other two species. Females of two species had longer-duration calls than did males, in friendly interactions with humans. F0 differences among species for both friendly and courtship calls were almost significant for males of M. gouazoubira. Individual differences were highly significant for both duration and mean F0. Mean F0 for courtship calls of adult males was not correlated with body size in six of the seven species, in contrast to the theory of acoustic allometry.
Conclusions: The production of male courtship bleats is probably a basic feature of Odocoiline deer and is probably important in sexual selection and female choice. The differences from one species to another are not sufficient for taxonomic use but may be incipient isolating mechanisms between grey and Amazonian brown brocket deer.
Implications: Studies of deer vocalisations have shown their importance in sexual selection and their incredible variety in closely related species and subspecies, but they have dealt mainly with Old World deer. This study fills a gap in our knowledge, as the first on Neotropical deer, which constitute six genera and 17 species and are widely distributed in the Americas. These data are important for future studies on the function and phylogeny of deer vocalisations.
Additional keywords: Cervidae, Odocoilinae, New World deer.
References
Abril VV, Carnelossi EAG, González S, Duarte JMB (2010) Elucidating the evolution of the red brocket deer Mazama americana complex (Artiodactyla; Cervidae). Cytogenetic and Genome Research 128, 177–187.| Elucidating the evolution of the red brocket deer Mazama americana complex (Artiodactyla; Cervidae).Crossref | GoogleScholarGoogle Scholar | 20407221PubMed |
Atkeson TD, Marchinton RL, Miller KV (1988) Vocalizations of white-tailed deer. American Midland Naturalist 120, 194–200.
| Vocalizations of white-tailed deer.Crossref | GoogleScholarGoogle Scholar |
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Black-Décima P (2000) Home range, social structure, and scent marking behaviour in brown brocket deer (Mazama gouazoubira) in a large enclosure. Mastozoologia Neotropical 7, 5–14.
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 |
Cap H, Deleporte P, Joachim J, Reby D (2008) Male vocal behavior and phylogeny in deer. Cladistics 24, 917–931.
| Male vocal behavior and phylogeny in deer.Crossref | GoogleScholarGoogle Scholar |
Carranza J, Roldán M, de Fátima Carvalho Peroni E, Duarte JMB (2017) Weak premating isolation between two parapatric brocket deer species. Mammalian Biology 87, 17–26.
| Weak premating isolation between two parapatric brocket deer species.Crossref | GoogleScholarGoogle Scholar |
Carranza J, Roldán M, Duarte JMB (2018) Lack of mate selectivity for genetic compatibility within the red brocket deer Mazama americana complex. Mammalian Biology 88, 168–175.
| Lack of mate selectivity for genetic compatibility within the red brocket deer Mazama americana complex.Crossref | GoogleScholarGoogle Scholar |
Charlton BD, Reby D, McComb K (2007) Female red deer prefer the roars of larger males. Biology Letters 3, 382–385.
| Female red deer prefer the roars of larger males.Crossref | GoogleScholarGoogle Scholar | 17550876PubMed |
Charlton BD, McComb K, Reby D (2008) Free-ranging red deer hinds show greater attentiveness to roars with formant frequencies typical of young males. Ethology 114, 1023–1031.
| Free-ranging red deer hinds show greater attentiveness to roars with formant frequencies typical of young males.Crossref | GoogleScholarGoogle Scholar |
Cursino MS, Salviano MB, Abril VV, Zanetti E dos S, Duarte JMB (2014) The role of chromosome variation in the speciation of the red brocket deer complex: the study of reproductive isolation in females. BMC Evolutionary Biology 14, 40
| The role of chromosome variation in the speciation of the red brocket deer complex: the study of reproductive isolation in females.Crossref | GoogleScholarGoogle Scholar | 24593190PubMed |
Danilkin AA, Alekse? A, Hewison AJM (1996) ‘Behavioural ecology of Siberian and European roe deer.’ (Chapman & Hall: London)
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 |
Duarte JMB, González S (2010) ‘Neotropical cervidology: biology and medicine of Latin American deer.’ (Funep: Jaboticabal, Brazil)
Duarte JMB, González S, Maldonado JE (2008) The surprising evolutionary history of South American deer. Molecular Phylogenetics and Evolution 49, 17–22.
| The surprising evolutionary history of South American deer.Crossref | GoogleScholarGoogle Scholar |
Fant G (1970) ‘Acoustic theory of speech production.’ (Walter de Gruyter: The Hague)
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 |
Fernández-García JL (2012) The endangered Dama dama mesopotamica Brooke, 1875: genetic variability, allelic loss and hybridization signals. Contributions to Zoology (Amsterdam, Netherlands) 81, 223–233.
| The endangered Dama dama mesopotamica Brooke, 1875: genetic variability, allelic loss and hybridization signals.Crossref | GoogleScholarGoogle Scholar |
Fitch WT (2000) Skull dimensions in relation to body size in nonhuman mammals: the causal bases for acoustic allometry. Zoology (Jena, Germany) 103, 40–58.
Fitch WT, Reby D (2001) The descended larynx is not uniquely human. Proceedings of the Royal Society of London. Series B, Biological Sciences 268, 1669–1675.
| The descended larynx is not uniquely human.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 | 22257361PubMed |
Garcia M, Wyman MT, Charlton BD, Fitch WT, Reby D (2014) Response of red deer stags (Cervus elaphus) to playback of harsh versus common roars. Naturwissenschaften 101, 851–854.
| Response of red deer stags (Cervus elaphus) to playback of harsh versus common roars.Crossref | GoogleScholarGoogle Scholar | 25119193PubMed |
Gilbert C, Ropiquet A, Hassanin A (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography. Molecular Phylogenetics and Evolution 40, 101–117.
| Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography.Crossref | GoogleScholarGoogle Scholar | 16584894PubMed |
Groves C (2006) The genus Cervus in eastern Eurasia. European Journal of Wildlife Research 52, 14–22.
| The genus Cervus in eastern Eurasia.Crossref | GoogleScholarGoogle Scholar |
Hassanin A, Delsuc F, Ropiquet A, Hammer C, Jansen van Vuuren B, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT, Couloux A (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. Comptes Rendus Biologies 335, 32–50.
| Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar | 22226162PubMed |
Hauser MD (1993) The evolution of nonhuman primate vocalizations: effects of phylogeny, body weight, and social context. American Naturalist 142, 528–542.
| The evolution of nonhuman primate vocalizations: effects of phylogeny, body weight, and social context.Crossref | GoogleScholarGoogle Scholar | 19425989PubMed |
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 |
Ludt CJ, Schroeder W, Rottmann O, Kuehn R (2004) Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Molecular Phylogenetics and Evolution 31, 1064–1083.
| Mitochondrial DNA phylogeography of red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 15120401PubMed |
Martins GS (2015) Avaliacao da existencia de isolamento reprodutivo entre duas espécies de veados cinza (Mazama gouazoubira e Mazama nemorivaga) por meio de machos hibridos. MSc Thesis, Faculdade de Ciencias Agrarias e Veterinarias, Universidade Estadual Paulista, Jaboticabal, Brazil.
McComb KE (1991) Female choice for high roaring rates in red deer, Cervus elephas. Animal Behaviour 41, 79–88.
McElligott AG, Birrer M, Vannoni E (2006) Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies. Journal of Zoology 270, 340–345.
| Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies.Crossref | GoogleScholarGoogle Scholar |
Minami M, Kawamichi T (1992) Vocal repertoires and classification of the sika deer Cervus nippon. Journal of the Mammalogical Society of Japan 17, 71–94.
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 | 23667678PubMed |
Pitcher BJ, Briefer EF, Vannoni E, McElligott AG (2014) Fallow bucks attend to vocal cues of motivation and fatigue. Behavioral Ecology 25, 392–401.
| Fallow bucks attend to vocal cues of motivation and fatigue.Crossref | GoogleScholarGoogle Scholar |
Pitcher BJ, Briefer EF, McElligott AG (2015) Intrasexual selection drives sensitivity to pitch, formants and duration in the competitive calls of fallow bucks. BMC Evolutionary Biology 15, 149
| Intrasexual selection drives sensitivity to pitch, formants and duration in the competitive calls of fallow bucks.Crossref | GoogleScholarGoogle Scholar | 26279584PubMed |
Pitra C, Fickel J, Meijaard E, Groves C (2004) Evolution and phylogeny of old world deer. Molecular Phylogenetics and Evolution 33, 880–895.
| Evolution and phylogeny of old world deer.Crossref | GoogleScholarGoogle Scholar | 15522810PubMed |
Polziehn RO, Strobeck C (2002) A phylogenetic comparison of red deer and wapiti using mitochondrial DNA. Molecular Phylogenetics and Evolution 22, 342–356.
| A phylogenetic comparison of red deer and wapiti using mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 11884159PubMed |
Reby D, McComb K (2003a) Vocal communication and reproduction in deer. Advances in the Study of Behavior 33, 231–264.
| Vocal communication and reproduction in deer.Crossref | GoogleScholarGoogle Scholar |
Reby D, McComb K (2003b) 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, McComb K, Cargnelutti B, Darwin C, Fitch WT, Clutton-Brock T (2005) Red deer stags use formants as assessment cues during intrasexual agonistic interactions. Proceedings. Biological Sciences 272, 941–947.
| Red deer stags use formants as assessment cues during intrasexual agonistic interactions.Crossref | GoogleScholarGoogle Scholar | 16024350PubMed |
Reby D, Charlton BD, Locatelli Y, McComb K (2010) Oestrous red deer hinds prefer male roars with higher fundamental frequencies. Proceedings. Biological Sciences 277, 2747–2753.
| Oestrous red deer hinds prefer male roars with higher fundamental frequencies.Crossref | GoogleScholarGoogle Scholar | 20427342PubMed |
Richardson LW, Jacobson HA, Muncy RJ, Perkins CJ (1983) Acoustics of white-tailed deer (Odocoileus virginianus). Journal of Mammalogy 64, 245–252.
| Acoustics of white-tailed deer (Odocoileus virginianus).Crossref | GoogleScholarGoogle Scholar |
Ruprecht R (2014) Acoustic allometry in mammals. MSc thesis, University of Vienna, Austria.
Stachowicz JB, Vannoni E, Pitcher BJ, Briefer EF, Geffen E, McElligott AG (2014) Acoustic divergence in the rut vocalizations of Persian and European fallow deer. Journal of Zoology 292, 1–9.
| Acoustic divergence in the rut vocalizations of Persian and European fallow deer.Crossref | GoogleScholarGoogle Scholar |
Taylor AM, Reby D (2010) The contribution of source–filter theory to mammal vocal communication research: advances in vocal communication research. Journal of Zoology 280, 221–236.
| The contribution of source–filter theory to mammal vocal communication research: advances in vocal communication research.Crossref | GoogleScholarGoogle Scholar |
Torriani MVG, Vannoni E, McElligott AG (2006) Mother–young recognition in an ungulate hider species: a unidirectional process. American Naturalist 168, 412–420.
| Mother–young recognition in an ungulate hider species: a unidirectional process.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 IA, Volodina EV, Sibiryakova OV, Naidenko SV, Hernandez-Blanco JA, Litvinov MN, Rozhnov VV (2015a) Vocal activity of the red deer and the acoustic structure of its rutting calls in the Russian Far East. Doklady Biological Sciences 462, 144–147.
| Vocal activity of the red deer and the acoustic structure of its rutting calls in the Russian Far East.Crossref | GoogleScholarGoogle Scholar | 26164336PubMed |
Volodin IA, Matrosova VA, Volodina EV, Garcia AJ, Gallego L, Márquez R, Llusia D, Beltrán JF, Landete-Castillejos T (2015b) 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, Nahlik A, Tari T, Frey R, Volodina E (2019) 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 elaphas). 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 elaphas).Crossref | GoogleScholarGoogle Scholar |
