Abstract
We have recorded long calls of free ranging groups of six Callithrix species, looking for species-specific parameters in the physical structure of the vocalizations. This comparative study is the first time a behavioral character (vocalization) has been incorporated in a study on Callithrix taxonomy. The long calls were analyzed in a digital sonograph and statistical comparisons performed, using analysis of variance. The data show that each of the six analyzed taxa can be distinguished on the basis of its call structure, mainly using the first long call note or syllable. In agreement with analyses based on morphological and genetic data, the vocalizations support the division of Callithrix into two groups: a jacchus-group and an aurita-group. The first group encompasses C. jacchus, C. geoffroyi, C. penicillata, and C. kuhlii, and the second, C. aurita, and C. flaviceps. Vocal parameters are able to distinguish all the taxa within each group, even C. flaviceps and C. kuhlii, whose specific status has been questioned. Differences between the four taxa of the jacchus-group suggested by vocalization data are not identical to those inferred on the basis of some morphological data. It is possible that vocalization differences are also influenced by historical secondary contact between populations and could have evolved as mechanisms of specific recognition and reproductive isolation. The results indicate that vocalization is a behavioral character that can be used to supplement other taxonomic data to study the phylogeny of the Callitrichidae and to improve our understanding of the evolution of the reproductive isolation of natural populations.
Resumen
Se grabaron vocalizaciones de canto de largo alcance de seis especies de Callithrix con la finalidad de comparar los patrones vocales de seis especies, para buscar caracteres capaces de diferenciarlos. Las vocalizaciones fueron analizadas en fonógrafo digital y tratadas estadísticamiente por medio de análisis de discrepancia. Los análisis demostraron que cada una de las seis especies pueden ser diferenciadas con base a la estructura de los cantos, principalmiente si se utiliza la primera nota o sílaba. De acuerdo con los análisis basados en datos morfológicos y genéticos, las vocalizaciones apoyan la división de Callithrix en dos grupos: grupo jacchus y el grupo aurita. El primero comprende C. jacchus, C. geoffroyi, C. penicillata y C. kuhlii, y el segundo incluye C. aurita y C. flaviceps. Los parámetros vocales pueden distinguir todas las especies dentro de cada grupo, incluyendo a C. flaviceps y a C. kuhlii, cuyos estados específicos han sido cuestionados. Las diferencias entre las cuatro especies del grupo Jacchus sugeridas por los datos de vocalización no son idénticas con las inferidas en base a los datos morfológicos. Es posible que dichas diferencias también están influenciadas por la historia de contacto secundario entre dichas poblaciones, y pueden haber evolucionado como mecanismos de reconocimiento poblacional y aislamiento reproductivo. Los resultados indican que la vocalización es un carácter del comportamiento que puede ser utilizado para complementar otros datos taxonómicos para estudiar la filogenia de los Callithrichidae y para mejorar nuestro entendimiento sobre la evolución del aislamiento reproductivo en poblaciones naturales.
Resumo
Foram gravadas vocalizações de longo alcance (canto) de Callithrix de vida livre, com a finalidade de comparar os padrões vocais de seis taxa, em busca de caracteres capazes de diferenciá-los. As vocalizações foram analisadas em sonógrafo digital e tratadas estatisticamente através de análises de variância. As análises sonoras demonstraram que cada um dos seis taxa pode ser diferenciado com base na estrutura dos seus cantos, principalmente utilizando-se a primeira nota, ou sílaba. Coerente com os dados morfológicos e genéticos, as vocalizações apoiam a divisão de Callithrix em dois grupos: jacchus e aurita. O primeiro compreende C. jacchus, C. geoffroyi, C. pencillata e C. kuhlii, e o segundo C. aurita e C. flaviceps. Dentro de cada grupo há parâmetros relacionados à duração e freqüência das notas capazes de diferenciar todos os taxa, inclusive C. flaviceps e C. kuhlii, cujos status taxonômicos tem sido questionados. As diferenças nos parâmetros acústicos entre os quatro taxa de Callithrix do grupo jacchus não estão claramente relacionadas às supostas distâncias filogenéticas inferidas com base em dados morfológicos. É possível que essas diferenças também tenham relação com a história das zonas de contato secundário entre esses taxa, sendo reforçadas como mecanismos de reconhecimento populacional e isolamento reprodutivo. Os resultados deste estudo indicam que a vocalização é um caráter comportamental que pode ser usado para suplementar outras técnicas de taxonomia de Callithrichidae e no entendimento da evolução do isolamento reprodutivo em populações naturais.
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Altmann SA (1967) The structure of primate communication. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 325–362
Ambrose L (2003) Three acoustic forms of Allen’s galagos (Primates; Galagonidae) in the Central African region. Primates 44:25–39
Barroso CML, Schneider H, Schneider MP, Sampaio I, Harada ML, Czelusniak J, Goodman M (1997) Update on the phylogenetic of New World monkeys: further DNA evidence for placing the pygmy marmoset (Cebuella) within the genus Callithrix. Int J Primatol 18(4):651–674
Brockelman WY, Schilling D (1984) Inheritance of stereotyped gibbon calls. Nature 312:634–636
Canavez FC, Moreira MAM, Simon F, Parham P, Seuanez HN (1999) Phylogenetic relationships of the Callitrichinae (Platyrrhini, Primates) based on β2-microglobulin DNA sequences. Am J Primatol 48:225–236
Chen HC, Geissmann T, Chen PC (2004) A survey of the taxonomic status of captive gibbons in Taiwan. Raffles Bull Zool 52(1):265–269
Coimbra-Filho AF (1986a) Sagui-da-serra, Callithrix aurita (Thomas, 1903). Informativo FBCN 10(1):3
Coimbra-Filho AF (1986b) Sagui-da-serra-escuro, Callithrix aurita (E. Geoffroy, 1812). Informativo FBCN 10(2):3
Coimbra-Filho AF (1990) Sistemática, distribuição geográfica e situação atual dos símios brasileiros (Platyrrhini-Primates). Rev Bras Biol 50(4):1063–1079
Coimbra-Filho AF, Pissinati A, Silva RR, Rylands AB (1993) Experimental multiple hybridism and natural hybrids among Callithrix species from eastern Brazil. In: Rylands AB (ed) Marmosets and tamarins: systematics, ecology and behaviour. Oxford University Press, Oxford, pp 95–120
Courtenay DO, Bearder SK (1989) The taxonomic status and distribution of bushbabies in Malawi with emphasis on the significance of vocalizations. Int J Primatol 10(1):17–34
Epple G (1968) Comparative studies on vocalization in marmoset monkeys (Hapalidae). Folia Primatol 8:1–40
Gautier JP (1978) Répertoire sonore de Cercopithecus cephus. Z Tierpsychol 46:113–169
Haimoff EH, Chivers DJ, Gittins SP, Whitten T (1982) A phylogeny of gibbons (Hylobates spp.) based on morphological and behavioural characters. Folia Primatol 39:213–237
Hershkovitz P (1977) Living New World monkeys (Platyrrhini), vol 1. University of Chicago Press, Chicago
Hodun A, Snowdon CT, Soini P (1981) Subspecific variation in the long calls of the tamarin, Saguinus fuscicollis. Z Tierpsychol 57:97–110
Hohmann G (1989) Comparative study of vocal communication in two Asian leaf monkeys, Presbytis johnii and Presbytis entellus. Folia Primatol 52:27–57
Jones BS, Harris DHR, Catchpole CK (1993) The stability of vocal signature in phee call of the common marmoset, Callithrix jacchus. Am J Primatol 31:67–75
Maeda T, Masataka N (1987) Locale specific vocal behaviour of the tamarin (Saguinus l. labiatus). Ethology 75:25–30
Marler P (1955) Characteristics of some animal calls. Nature 176:6–8
Marroig G, Cropp S, Cheverud JM (2004) Systematics and evolution of the jacchus group of marmosets (Platyrrhini). Am J Phys Anthropol 123:11–22
Marshall JT, Marshall ER (1976) Gibbons and their territorial songs. Science 193:235–237
Masters JC (1991) Loud calls of Galago crassicaudatus and G. garnettii and their relation to habitat structure. Primates 32:153–167
Meireles CMM, Sampaio MIC, Schneider MPC (1992) Protein variation, taxonomy and differentiation in five species of marmosets (genus Callithrix Erxleben, 1777). Primates 33:227–238
Mendes SL (1997a) Hybridization in free ranging Callithrix flaviceps and the taxonomy of the Atlantic forest marmosets. Neotrop Primates 5(1):6–8
Mendes SL (1997a) Padrões Biogeográficos e Vocais em Callithrix do grupo jacchus (Primates, Callitrichidae). Ph.D Thesis, Universidade Estadual de Campinas, Campinas, Brazil
Mittermeier RA, Coimbra-Filho AF (1981) Systematics: species and subspecies. In: Coimbra-Filho AF, Mittermeier RA (eds) Ecology and behavior of neotropical primates, vol 1. Academia Brasileira de Ciencias, Belo Horizonte, pp 29–111
Moreira MAM, Seuanez HN (1999) Mitochondrial pseudogenes and phyletic relationships of Cebuella and Callithrix (Platyrrhini, Primates). Primates 40(2):353–364
Natori M (1986) Interspecific relationships of Callithrix based on the dental characters. Primates 27(3):321–336
Natori M (1990) Numerical analysis of systematic status of Callithrix kuhli based on measurements of the postcanine dentition. Primates 31(4):555–562
Natori M (1994) Craniometrical variation among eastern Brazilian marmosets and their systematic relationships. Primates 35(2):167–176
Norcross JL, Newman JD (1993) Context and gender-specific differences in the acoustic structure of common marmoset (Callithrix jacchus) phee calls. Am J Primatol 30:37–54
Quris R (1980) Emission vocale de forte intensité chez Cercocebus galeritus agilis: structure, caractéristiques spécifiques e individuelles, modes d’émission. Mammalia 44(1):35–50
Rosenberger AL (1981) Systematics: the higher taxa. In: Coimbra-Filho AF, Mittermeier RA (eds) Ecology and behavior of neotropical primates, vol 1. Academia Brasileira de Ciencias, Belo Horizonte, pp 9–27
Rylands AB, Faria DS (1993) Habitats, feeding ecology, and home range size in the genus Callithrix. In: Rylands AB (ed) Marmosets and tamarins: systematics, ecology and behaviour. Oxford University Press, Oxford, pp 262–272
Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodriguez-Luna E (2000) An assessment of the diversity of New World Primates. Neotrop Primates 8(2):61–93
Rylands AB, Mittermeier RA, Coimbra-Filho AF (this volume) The systematics and distribution of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and Callimico (Callimico) (Callitrichidae, Primates). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: the marmoset/callimico radiation. Springer, New York pp 25–61
Sampaio IS, Schneider MP, Barroso CML, Schneider H (1996) Polymorphism of phosphogluconate dehydrogenase (PGD) in New World monkeys: taxonomic significance. Rev Bras Genét 19(1):87–92
Schneider H, Sampaio I, Harada ML, Barroso CML, Schneider MPC, Czelusniak J, Goodman M (1996) Molecular phylogeny of the New World monkeys (Platyrhini, Primates) based on two unlinked nuclear genes: IRBP Intron 1 and epsilon-globin sequences. Am J Phys Anthropol 100:153–179
Sena L, Vallinoto M, Sampaio I, Schneider H, Ferrari SF, Scneider MPC (2002) Mitochondrial COII gene sequences provide new insights into the phylogeny of marmoset species groups (Callitrichidae, Primates). Folia Primatol 73(5):240–251
Singer SS, Schmitz J, Schwiegk C, Zischler H (2003) Molecular cladistic markers in New World monkey phylogeny (Platyrrhini, Primates). Mol Phylogenet Evol 26:490–501
Snedecor GW, Cochran WG (1989) Statistical methods, 8ath edn. Iowa State University Press, Iowa
Snowdon CT (1993) A vocal taxonomy of the callitrichids. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, Oxford, pp 78–94
Snowdon CT, Hodun A, Rosenberger AL, Coimbra-Filho AF (1986) Long-call structure and its relation to taxonomy in lion tamarins. Am J Primatol 11:253–261
Struhsaker TT (1970) Phylogenetic implications of some vocalizations of Cercopithecus monkeys. In: Napier JR, Napier PH (eds) Old World monkeys: evolution, systematics, and behavior. Academic, New York, pp 365–444
Tagliaro CH, Schneider MPC, Schneider H, Sampaio IC, Stanhope MJ (1997) Marmoset phylogenetics, conservation perspectives, and evolution of the mtDNA control region. Mol Biol Evol 14(6):674–684
Vivo M (1991) Taxonomia de Callithrix Erxleben, 1777 (Callitrichidae, Primates). Fundação Biodiversitas, Belo Horizonte
Waser PM (1982) The evolution of male loud calls among mangabeys and baboons. In: Snowdon CT, Brown CH, Petersen MR (eds) Primate communication. Cambridge University Press, Cambridge, pp 117–143
Wied M zu (1826) Beiträge zur Naturgeschichte von Brasilien. II Band. Landes-Industrie-Comptoirs, Weimar, Germany
Zimmermann E, Bearder SK, Doyle GA, Andersson AB (1988) Variations in vocal patterns in Senegal and South African lesser bushbabies and their implications for taxonomic relationships. Folia Primatol 51:87–105
Acknowledgements
We acknowledge the collaboration of Dwain Santee, Braz Cosenza, Fabiano R. Melo, Vânia Diego, Bernardo F. A. Brito, Karen B. Strier, and Anthony B. Rylands, and the support of Unicamp, Museu de Biologia Prof. Mello Leitão, Reserva Natural da CVRD, Parque Estadual de Pedra Azul, Estação Biológica de Caratinga, Parque Ecológico de Americana, Reserva Biológica Augusto Ruschi, Reserva Biológica de Duas Bocas, Estação Experimental Lemos Maia, and Estação Ecológica de Tapacurá. We are also indebted to Susan Ford, who made very helpful suggestions on the manuscript.
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Mendes, S.L., Vielliard, J.M.E., De Marco, P. (2009). The Vocal Identity of the Callithrix Species (Primates, Callitrichidae). In: Ford, S., Porter, L., Davis, L. (eds) The Smallest Anthropoids. Developments in Primatology: Progress and Prospects. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-0293-1_3
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