Pitheciid vocal communication: what can we say about what they are saying?

Bruna Bezerra, Cristiane Casar, Leandro Jerusalinsky, Adrian Barnett, Monique Bastos, Antonio Souto, Gareth Jones

Abstract


The variation in ecological traits in pitheciids allows investigation of vocal communication over a range of social and acoustic circumstances. In this review paper we present a summary of the history of pitheciid vocal studies and review i) the status of our current knowledge of the vocal repertoire sizes of pitheciid primates, ii) how much do we understand about the context of different acoustic signals and iii) how can we potentially use our knowledge of vocalisations in animal welfare practices. We show trends across taxa and identify gaps in our knowledge. For instance, the repertoires described for Titi monkeys and Sakis have the expected sizes for these genera, considering their relatively small social group sizes. However, Uacari groups can contain over 100 individuals, and a larger vocal repertoire than the ones described would be expected, which could be a consequence of the fission-fusion social system where the large group divides into smaller subgroups. Nevertheless, vocal repertoires exist for only about 12% of the pitheciid species and nothing is known, for example, on call ontogeny. We hope that this review will serve as a reference point for researchers interested in investigating vocal behaviour in this primate group, thus, optimising both funding focus and, researcher’s time and effort. Also, we hope to help defining methodologies and strategies for the conservation and management of pitheciid monkeys.


Keywords


vocal repertoires; meaning attributed calls; alarm calls; conservation methods; playback survey; welfare practices

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References


Adams DB, Erhart EM (2009) Differential response to predators in the Gray's bald-faced saki monkey (Pithecia irrorata): A playback experiment. American Journal of Physical Anthropology 48:75

Aldrich BC, Molleson L, Nekaris KAI (2008) Vocalizations as a conservation tool: an auditory survey of the Andean titi monkey Callicebus oenanthe Thomas, 1924 (Mammalia: Primates: Pitheciidae) at Tarangue, Northern Peru. Contributions to Zoology 77:1-6

Arbid MA, Liebal K, Pika S (2008) Primate vocalization, gesture and the evolution of human language. Current Anthropology 49:1053-1076

Arnold K, Zuberbühler K (2006) Semantic combinations in primate calls. Nature 441:303

Barnett AA (2010) Diet, habitat use and conservation ecology of the golden-backed uacari, Cacajao melanocephalus ouakary, in Jaú National Park, Amazonian Brazil. PhD Thesis, Roehampton University, London, UK

Barnett AA, Castilho CV, Shapley RL, Anicácio A (2005) Diet, habitat selection and natural history of Cacajao melanocephalus ouakary in Jaú National Park, Brazil. International Journal of Primatology 26:949-969

Barnett AA, Schiel V, Deveny A, Valsko J, Spironello WR, Ross C (2011) Predation on Cacajao ouakary and Cebus albifrons (Primates: Platyrrhini) by harpy eagles. Mammalia 75:169-172

Barnett AA, Shaw P (2014) More food or fewer predators? The benefits to birds of associating with a Neotropical primate varies with their foraging strategy. Journal of Zoology 294:224-233

Bezerra BM (2010) Behaviour and vocal communication in golden-backed uakaris: Cacajao melanocephalus. PhD Thesis, University of Bristol, Bristol, UK

Bezerra BM, Barnett AA, Souto A, Jones G (2011) Ethogram and natural history of golden-backed uakaris (Cacajao melanocephalus). International Journal of Primatology 32:46-68

Bezerra BM, Souto AS, Jones G (2010a) Vocal repertoire of golden-backed uakaris (Cacajao melanocephalus): call structure and context. International Journal of Primatology 31:759-778

Bezerra BM, Souto AS, Jones G (2010b) Responses of golden-backed uakaris, Cacajao melanocephalus, to call playback: implications for surveys in the flooded igapó forest. Primates 51:327-336

Bezerra BM, Souto AS, Jones G (2011) Perspectives in primate bioacoustics. In: Potocki E, Krasiñski J (eds) Primatology: Theories, methods and research. Nova Science Publishers, Hauppauge, NewYork, pp. 1-28

Bezerra BM, Souto AS, Jones G (2012) Propagation of the loud “tchó” call of golden-backed uakaris, Cacajao melanocephalus, in the blackwater-swamp forests of the upper Amazon. Primates 53:317-325

Bezerra BM, Barnett A, Souto AS, Jones G (2013) Vocal communication in Cacajao, Chripotes and Pithecia: current knowledge and future directions. In: Veiga LM, Barnett AB, Ferrari SF, Norconk MA (eds) Evolutionary Biology and conservation of Titis, Sakis and Uakaris. Cambridge University Press, Cambridge, pp. 303-310

Bouchet H, Blois-Heulin C, Lemasson A (2013) Social complexity parallels vocal complexity: a comparison of three non-human primate species. Frontiers in Psychology doi: 10.3389/fpsyg.2013.00390

Bowler M, Knogge C, Heymann EW, Zinner D (2012) Multilevel societies in New World Primates? Flexibility may characterize the organization of Peruvian red uakaris (Cacajao calvus ucayalii). International Journal of Primatology 33:1110-1124

Bradbury JW, Vehrencamp SL (2011) Principles of animal communication. 2 ed. Sinauer Associates, Sunderland, MA

Buchanan DB, Mittermeier RA, van Roosmalen MGM (1981) The saki monkeys, genus Pithecia. In: Coimbra-Filho RA, Mittermeier RA (eds) Ecology and behaviour of Neotropical primates. Academia Brasileira de Ciências, Rio de Janeiro, pp. 391-417

Byrne H, Rylands AB, Carneiro JC, Alfaro JWL, Bertuol F, da Silva MN, Messias M, Groves CP, Mittermeier RA, Farias I, Hrbek T (2016) Phylogenetic relationships of the New World titi monkeys (Callicebus): first appraisal of taxonomy based on molecular evidence. Frontiers in Zoology 13:1-26

Cäsar C (2011) Anti-predator behaviour of black-fronted titi monkeys (Callicebus nigrifrons). PhD thesis, University of Saint Andrews, UK

Cäsar C, Zuberbühler K (2012) Referential alarm calling behaviour in New World primates. Current Zoology 58:680-697

Candiotti A, Zuberbühler K, Lemasson A (2012) Context-related call combinations in female Diana monkeys. Animal Cognition 15:327-339

Cäsar C, Zuberbuhler K, Young RJ, Byrne RW (2013) Titi monkey call sequences vary with predator location and type. Biology Letters 9:20130535-20130535

Cäsar C, Byrne R, Young RJ, Zuberbühler K (2012a) The alarm call system of wild black-fronted titi monkeys, Callicebus nigrifrons. Behavioral Ecology and Sociobiology 66:653-667

Cäsar C, Byrne R, Hoppitt W, Young RJ, Zuberbühler K (2012b) Evidence for semantic communication in titi monkey alarm calls. Animal Behaviour 84:405-411

Caselli CB, Mennill D, Bicca-Marques JC, Setz EZF (2014) Vocal Behavior of black-fronted titi monkeys (Callicebus nigrifrons): Acoustic properties and pehavioral contexts of loud calls. American Journal of Primatology 76:788–800

Chagas R, Ferrari SF (2010) Population parameters of the endangered titi monkey, Callicebus coimbrai Kobayashi and Langguth, 1999, in the fragmented landscape of southern Sergipe, Brazil. Brazilian Journal of Biology 71:569-575

Cisneros-Heredia DF, León-Reyes A, Seger S (2005) Boa constrictor predation on a titi monkey, Callicebus discolor. Neotropical Primates 13:11-12

Clarke E, Reichard UH, Zuberbühler K (2006) The syntax and meaning of wild gibbon songs. PLoS ONE 1:e73

Clay Z, Zuberbühler K (2009) Food-associated calling sequences in bonobos. Animal Behaviour 77:1387-1396.

Cleveland J, Snowdon CT (1982) The complex vocal repertoire of the adult cotton-top tamarin Saguinus oedipus oedipus. Zeitschrift für Tierpsychologie 58:231-270

Crockford C, Boesch C (2005) Call combinations in wild chimpanzees. Behaviour 142:397-421

Dacier A, de Luna AG, Fernandez-Duque E, Di Fiore A (2011) Estimating population density of Amazonian titi monkeys (Callicebus discolor) via playback point counts. Biotropica 43:135-140

Dalponte JC, Silva FE, Silva-Júnior JS (2014) New species of titi monkey, genus Callicebus Thomas, 1903 (Primates, Pitheciidae), from Southern Amazonia, Brazil. Papéis Avulsos de Zoologia 54:457-472

de Luna AG, Sanmiguel R, Di Fiore A, Fernandez-Duque E (2010) Predation and predation attempts on red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador. Folia Primatologica 81:86-95

Defler TR (2003) Primates de Colombia. Conservation International, Bogotá

Di Bitetti M (2003) Food-associated calls of tufted capuchin monkeys (Cebus apella nigritus) are functionally referential signals. Behaviour 140:565-592

Di Fiore A, Fernandez-Duque E, Hurst D (2007) Adult male replacement in socially monogamous equatorial saki monkeys (Pithecia aequatorialis). Folia Primatologica 78:88-98

Dixson A, Anderson M (2001) Sexual selection and the comparative anatomy of reproduction in monkeys, apes, and human beings. Annual Review of Sex Research 12:121-144

Dittus WPJ (1984). Toque macaque food calls: semantic communication concerning food distribution in the environment. Animal Behaviour 32:470-477

Ey E, Fischer F (2009) The “acoustic adaptation hypothesis” - a review of the evidence from birds, anurans and mammals. Bioacoustics 19:21-48

Fernandez-Duque E, Di Fiore A, de Luna AG (2013) Pair-mate relationships and parenting in ecuatorial saki monkeys (Pithecia aequatorialis) and red titi monkeys (Callicebus discolor) of Ecuador. In: Veiga LM, Barnett AB, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of titis, sakis and uacaris. Cambridge University Press, Cambridge, pp. 295-302

Ferrari SF, Guedes PG, Figueiredo W, Barnett AA (2014) Reconsidering the nomenclature of the black-faced uacaris (Cacajao melanocephalus group, sensu Hershkovitz, 1987) from the northern Amazon basin. Zootaxa 3866:353-370

Fontaine R (1981). The uakaris, Genus Cacajao. In: Coimbra-Filho A, Mittermeier RA (eds) Ecology and behavior of Neotropical Primates. Academia Brasileira de Ciências, Rio de Janeiro

Gouzoules S, Gouzoules H, Marler P (1984) Rhesus monkey (Macaca mulatta) screams: representational signalling in the recruitment of agonistic aid. Animal Behaviour 32:182-193

Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington

Groves C (2005) Order Primates. In: Wilson DE, Reeder DM (eds) Mammals of the world: a taxonomic and geographic reference. 3 ed. The Johns Hopkins University Press, Baltimore, pp. 111-184

Gros-Louis J (2004) The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller. Animal Behaviour 67:431-440

Henline WT (2007) Vocal repertoire of white-faced sakis (Pithecia pithecia). MSc dissertation, Eastern Kentucky University, Kentucky, USA

Hewson CJ (2004) Do vocalizations tell us anything about animal welfare? Canadian Veterinary Journal 45:621-624

IUCN (2017) The IUCN red list of threatened species. [http://www.iucnredlist.org.] Accessed 27 June 2017

Jerusalinsky L (2013) Distribuição geográfica e conservação de Callicebus coimbrai Kobayashi and Langguth, 1999 (Primates - Pitheciidae) na mata atlântica do nordeste Brasileiro. PhD Thesis, Universidade Federal da Paraíba, João Pessoa, Brazil

Jerusalinsky L, Oliveira MM, Pereira RF, Santana V, Bastos PCR, Ferrari SF (2006) Preliminary evaluation of the conservation status of Callicebus coimbrai Kobayashi & Langguth, 1999 in the Brazilian state of Sergipe. Primate Conservation 21:25-32

Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. International Journal of Primatology 23:707-740

Kershenbaum A (2014) Entropy rate as a measure of animal vocal complexity. Bioacoustics 23:195-208

Kinzey WG, Rosenberger AL, Heisler PS, Prowse DL, Trilling JS (1977) A preliminary field investigation of the yellow-handed titi monkeys, Callicebus torquatus torquatus, in northern Peru. Primates 18:159-181

Kirchhof J, Hammerschmidt K (2006) Functionally referential alarm calls in tamarins (Saguinus fuscicollis and Saguinus mystax) - Evidence from playback experiments. Ethology 112:346-354

Krams I, Krama T, Freeberg TM, Kullberg C, Lucas JR (2012) Linking social complexity and vocal complexity: a parid perspective. Philosophical Transactions of the Royal Society B 367:1879-1891

Kroodsma DE, Miller EH (1996) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca

Linhart P, Ratcliffe VF, Reby D, Spinka M. (2015). Expression of emotional arousal in two different piglet call types. PloS One 10:e0135414

Marler P, Evans C, Hauser MD (1992) Animal signals: reference, motivation or both? In: Papoucek H, Jürgens U, Papoucek M (eds) Nonverbal vocal communication: comparative and developmental approaches. Cambridge University Press, Cambridge, pp. 66-86

Marques ELN, Beltrão-Mendes R, Ferrari SF (2013) Primates, Pitheciidae, Callicebus barbarabrownae Hershkovitz, 1990: New localities for the critically endangered titi monkey in the São Francisco basin, state of Sergipe, Brazil. Check List 9:113-115

Marsh LK (2014) A taxonomic revision of the saki monkeys, Pithecia Desmarest, 1804. Neotropical Primates 21:1-65

Martins SS, Lima EM, Silva-Júnior JS (2005). Predation of a bearded saki (Chiropotes utahicki) by a harpy eagle (Harpia harpyja). Neotropical Primates 13:7-10

McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biology Letters 1:381-385

McCowan B, Rommeck I (2006) Bioacoustic monitoring of aggression in group-housed rhesus macaques. Journal of Applied Animal Welfare Science 9:261-26

Melo FR, Mendes SL (2000) Emissão de gritos longos por grupos de Callicebus nigrifrons e suas reações a playback. In: Alonso C, Langguth A (eds) A Primatologia do Brasil 7. Ed Universitária, Sociedade Brasileira de Primatologia, João Pessoa, pp. 215-222

Mitani JC, Marler P (1989) A phonological analysis of male gibbon singing behavior. Behaviour 109:20-45

Müller AE, Anzenberger G (2002) Duetting in the titi monkey Callicebus cupreus: structure, pair specificity and development of duets. Folia Primatologica 73:104-115

Norconk MA (2006) Long-term study of group dynamics and female reproduction in Venezuelan Pithecia pithecia. International Journal of Primatology 27:653-674

Norconk MA (2007) Sakis, uakaris, and titi monkeys. In: Campbell C, Fuentes A, MacKinnon KG, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp. 122-139

Ouattara K, Lemasson A, Zuberbühler K (2009) Campbell's monkeys concatenate vocalizations into context-specific call sequences. Proceedings of the National Academy of Sciences 106:22026-22031

Pinto LP (2008) Ecologia alimentar do cuxiu-de-nariz-vermelho Chiropotes albinasus (Primates: Pitheciidae) na Floresta Nacional do Tapajos, Pará. PhD Thesis, Universidade Estadual de Campinas, Brazil

Pinto LP, Barnett AA, Bezerra BM, Boubli JP, Bowler M, Cardoso NA, Caselli CB, Rodriguez JO, Santos RR, Setz EZF, Veiga LM (2013) Why we know so little: the challenges of fieldwork on the Pitheciids. In: Veiga LM, Barnett AB, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of titis, sakis and uacaris Cambridge University Press, Cambridge, pp. 145-150

Plumptre AJ, Sterling EJ, Buckland S (2013) Primate census and survey techniques. In: Sterling EJ, Bynum N, Blair ME (eds) Primate Ecology and Conservation: A handbook of techniques. Oxford University Press. Oxford, pp. 10-26

Printes RC, Rylands AB, Bicca-Marques JC (2011) Distribution and status of the Critically Endangered blond titi monkey Callicebus barbarabrownae of northeast Brazil. Oryx 45:439-443

Rettig NL (1978) Breeding behavior of the harpy eagle Harpia harpyja. Auk 95:629-643

Robinson JG (1979) An analysis of the organization of vocal communication in the titi monkey Callicebus moloch. Zeitschrift fur Tierpsychologie 49:381-405

Robinson JG (1981) Vocal Regulation of Inter- and intragroup spacing during boundary encounters in the titi monkey, Callicebus moloch. Primates 22:161-172.

Robinson JG (1984) Syntactic structures in the vocalizations of wedge-capped capuchin monkeys Cebus olivaceus. Behaviour 90:46-79

Schel AM, Zuberbühler K (2012) Predator and non-predator long-distance calls in Guereza colobus monkeys. Behavioural Processes 91:41-49

Semple S, Higham JP (2013) Primate signals: current issues and perspectives. American Journal of Primatology 75: 613-620

Seyfarth RM, Cheney DL, Marler P (1980) Vervet monkey alarm calls: semantic communication in a free-ranging primate. Animal Behaviour 28:1070-1094

Silva SSB, Ferrari SF (2009) Behavior patterns of southern bearded sakis (Chiropotes satanas) in the fragmented landscape of eastern Brazilian Amazonia. American Journal of Primatology 71:1-7

Silva-Junior JS, Figueiredo-Ready WMB, Ferrari SF (2013) Taxonomy and geographic distribution of the Pitheciidae. In: Veiga LM, Barnett AB, Ferrari SF, Norconk MA (eds) Evolutionary biology and conservation of titis, sakis and uacaris. Cambridge University Press, Cambridge, pp. 31-42

Souza-Alves JP, Ferrari SF (2010) Responses of wild titi monkeys, Callicebus coimbrai (Primates: Platyrrhini: Pitheciidae), to the habituation process. Zoologia 27:861-866

Skowronski MD, Fenton BM (2009) Detecting bat calls: an analysis of automated methods. Acta Chiropterologica 11:191-203

Slocombe KE, Zuberbühler K (2005) Agonistic screams in wild chimpanzees (Pan troglodytes schweinfurthii) vary as a function of social role. Journal of Comparative Psychology 119:67-77

van Roosmalen MGM, Mittermeier RA, Milton K (1981) The bearded sakis, Genus Chiropotes. In: Coimbra-Filho AF, Mittermeier RA (eds) Ecology and Behavior of Neotropical Primates. Academia Brasileira de Ciências, Rio de Janeiro, pp. 419-442

Veiga LM (2006) Ecologia e comportamento do cuxiú-preto (Chiropotes satanas) na paisagem fragmentada da Amazônia oriental. PhD Thesis, Universidade Federal do Pará, Brazil.

Veiga LM, Barnett AA, Ferrari SF, Norconk MA (2013) Evolutionary Biology and Conservation of Titis, Sakis and Uacaris. Cambridge University Press.

Wheeler BC (2010) Production and perception of situationally variable alarm calls in wild tufted capuchin monkeys (Cebus apella nigritus). Behavioral Ecology and Sociobiology 64:989-1000

Wheeler BC, Fischer J (2015) The blurred boundaries of functional reference: a response to Scarantino and Clay. Animal Behaviour 100:e9-e13

Zuberbühler K (2001) Predator-specific alarm calls in Campbell’s guenons. Behavioral Ecology and Sociobiology 50:414-422

Zuberbühler K (2002) A syntactic rule in forest monkey communication. Animal Behaviour 63:293-299

Zuberbühler K (2006) Language evolution: The origin of meaning in Primates. Current Biology 16:123-125

Zuberbühler K, Noe R, Seyfarth RM (1997) Diana monkey long-distance calls: messages for conspecifics and predators. Animal Behaviour 53:589-604


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