Behavioral Ecology and Sociobiology

, Volume 66, Issue 5, pp 653–667 | Cite as

The alarm call system of wild black-fronted titi monkeys, Callicebus nigrifrons

  • Cristiane Cäsar
  • Richard Byrne
  • Robert J. Young
  • Klaus Zuberbühler
Original Paper

Abstract

Upon encountering predators, many animals produce specific vocalisations that alert others and sometimes dissuade the predators from hunting. Callicebus monkeys are known for their large vocal repertoire, but little is known about the function and meaning of most call types. We recorded a large number of natural predator responses from five different groups of black-fronted titi monkeys in their Atlantic forest habitat in South Eastern Brazil. When detecting predatory threats, adult group members responded with call sequences that initially consisted of two brief, high-pitched calls with distinct frequency contours. Call A was mainly given to raptors but also to predatory capuchin monkeys and other threats within the canopy, while call B was given to predatory or non-predatory disturbances on the ground. In later parts of the sequences, we also recorded a high-pitched unmodulated call C and various low-pitched loud calls. Results therefore suggest that calls A and B provide listeners with rapid and reliable information about the general classes of danger experienced by the caller, while obtaining more specific information through other call types and combinations and behavioural responses. We discuss these findings in relation to current evolutionary theory of primate communication.

Keywords

Call sequences New Platyrrhini Semantic Predation Cognition 

References

  1. Arnold K, Zuberbühler K (2006a) The alarm-calling system of adult male putty-nosed monkeys, Cercopithecus nictitans martini. Anim Behav 72:643–653. doi:10.1016/j.anbehav.2005.11.017 CrossRefGoogle Scholar
  2. Arnold K, Zuberbühler K (2006b) Semantic combinations in primate calls. Nature 441:303–303. doi:10.1038/441303a CrossRefGoogle Scholar
  3. Arnold K, Zuberbühler K (2008) Meaningful call combinations in a non-human primate. Curr Biol 18:R202–R203. doi:10.1016/j.cub.2008.01.040 PubMedCrossRefGoogle Scholar
  4. Bezerra B, Barnett A, Souto A, Jones G (2009) Predation by the tayra on the common marmoset and the pale-throated three-toed sloth. J Ethol 27:91–96. doi:10.1007/s10164-008-0090-3 CrossRefGoogle Scholar
  5. Bianchi RDC, Mendes SL (2007) Ocelot (Leopardus pardalis) predation on primates in Caratinga Biological Station, Southeast Brazil. Am J Primatol 69:1173–1178. doi:10.1002/ajp.20415 CrossRefGoogle Scholar
  6. Bicca-Marques JC, Garber PA, Azevedo-Lopes MAO (2002) Evidence of three resident adult male group members in a species of monogamous primate, the red titi monkey (Callicebus cupreus). Mammalia 66:138–142Google Scholar
  7. Blumstein DT (1999) Alarm calling in three species of marmots. Behaviour 136:731–757CrossRefGoogle Scholar
  8. Boinski S, Chapman CA (1995) Predation on primates: where are we and what's next? Evol Anthropol 4:1–3. doi:10.1002/evan.1360040102 CrossRefGoogle Scholar
  9. Bossuyt F (2002) Natal dispersal of titi monkeys (Callicebus moloch) at Cocha Cashu, Manu National Park, Peru. Am J Phys Anthropol Supplement 34:47Google Scholar
  10. Campbell M, Snowdon C (2007) Vocal responses of captive-reared Saguinus oedipus during mobbing. Int J Primatol 28:257–270. doi:10.1007/s10764-007-9123-y CrossRefGoogle Scholar
  11. Caro TM (2005) Antipredator defense in birds and mammals. Univ Chicago Press, Chicago, Antipredator Defense in Birds and MammalsGoogle Scholar
  12. Cäsar C, Young RJ (2008) A case of adoption in a wild group of black-fronted titi monkeys (Callicebus nigrifrons). Primates 49:146–148. doi:10.1007/s10329-007-0066-x PubMedCrossRefGoogle Scholar
  13. Cäsar C, Franco ES, Soares GDN, Young RJ (2008) Observed case of maternal infanticide in a wild group of black-fronted titi monkeys (Callicebus nigrifrons). Primates 49:143–145. doi:10.1007/s10329-007-0067-9 PubMedCrossRefGoogle Scholar
  14. Cheney DL, Seyfarth RM (1990) How monkeys see the world: Inside the mind of another species. Chicago University Press, ChicagoGoogle Scholar
  15. Cisneros-Heredia DF, León-Reyes A, Seger S (2005) Boa constrictor Predation on a Titi monkey, Callicebus discolor. Neotrop Primates 13:11–12. doi:10.1896/1413-4705.13.3.11 CrossRefGoogle Scholar
  16. Clarke E, Reichard UH, Zuberbühler K (2006) The syntax and meaning of wild gibbon songs. PLoS One 1:e73PubMedCrossRefGoogle Scholar
  17. Coelho CM, De Melo LFB, Sábato MAL, Magni EMV, Hirsch A, Young RJ (2008) Habitat use by wild maned wolves (Chrysocyon brachyurus) in a transition zone environment. J Mammal 89:97–104. doi:10.1644/06-mamm-a-383.1 CrossRefGoogle Scholar
  18. 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 Primatol 81:86–95PubMedCrossRefGoogle Scholar
  19. Derby OA (1966) The Serra of Espinhaço, Brazil. J Geol 14:374–401CrossRefGoogle Scholar
  20. Digweed SM, Fedigan LM, Rendall D (2005) Variable specificity in the anti-predator vocalizations and behaviour of the white-faced capuchin, Cebus capucinus. Behaviour 142:997–1021CrossRefGoogle Scholar
  21. Eckardt W, Zuberbuhler K (2004) Cooperation and competition in two forest monkeys. Behav Ecol 15:400–411. doi:10.1093/beheco/arh032 CrossRefGoogle Scholar
  22. Ferrari SF (2009) Predation risk and antipredator strategies. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates. Developments in primatology. Progress and Prospects, Springer New York, pp 251–277. doi:10.1007/978-0-387-78705-3_10 CrossRefGoogle Scholar
  23. Fichtel C, Perry S, Gros-Louis J (2005) Alarm calls of white-faced capuchin monkeys: an acoustic analysis. Anim Behav 70:165–176. doi:10.1016/j.anbehav.2004.09.020 CrossRefGoogle Scholar
  24. Freese CH, Oppenheimer JR (1981) The capuchin monkeys, genus Cebus. In: Coimbra-Filho A, Mittermeier RA (eds) Ecology and behavior of neotropical primates, vol 1. Academia Brasileira de Ciências, Rio de Janeiro, pp 331–390Google Scholar
  25. Giulietti AM, Pirani JR (1988) Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a workshop on neotropical distribution. Academia Brasileira de Ciências, Rio de Janeiro, pp 39–69Google Scholar
  26. Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço Range region, Eastern Brazil. In: Davis SD, Heywood VH, Herrera-Macbryde O, Villa-Lobos J, Hamilton AC (eds) Centres of plant diversity, a guide and strategy for their conservation. Information Press, Oxford, pp 397–404Google Scholar
  27. Glantz SA, Slinker BK (2001) Primer of Applied Regression and Analysis of Variance. 2nd ed. McGraw-Hill, New York NYGoogle Scholar
  28. Hirsch A (2003) Habitat fragmentation and priority areas for primate conservation in the Rio Doce Basin, Minas Gerais. Neotrop Primates 11:195–196Google Scholar
  29. Kinzey WG (1981) The titi monkeys, genus Callicebus. In: Coimbra-Filho AF, Mittermeier RA (eds) Ecology and behavior of neotropical primates, vol 1. Academia Brasileira de Ciências, Rio de Janeiro, pp 241–296Google Scholar
  30. Kinzey W, Becker M (1983) Activity pattern of the masked titi monkey, Callicebus personatus. Primates 24:337–343. doi:10.1007/bf02381979 CrossRefGoogle Scholar
  31. Kinzey WG, Robinson JG (1983) Intergroup loud calls, range size, and spacing in Callicebus torquatus. Am J Phys Anthropol 60:539–544. doi:10.1002/ajpa.1330600416 PubMedCrossRefGoogle Scholar
  32. Kinzey W, Rosenberger A, Heisler P, Prowse D, Trilling J (1977) A preliminary field investigation of the yellow handed titi monkey, Callicebus torquatus torquatus, in Northern Peru. Primates 18:159–181. doi:10.1007/bf02382957 CrossRefGoogle Scholar
  33. Kirchhof J, Hammerschmidt K (2006) Functionally referential alarm calls in tamarins (Saguinus fuscicollis and Saguinus mystax)—evidence from playback experiments. Ethology 112:346–354. doi:10.1111/j.1439-0310.2006.01165.x CrossRefGoogle Scholar
  34. Klein BC, Harper LH, Bierregaard RO, Powell GVN (1988) The nesting and feeding behavior of the ornate hawk-eagle near Manaus, Brazil. Condor 90:239–245CrossRefGoogle Scholar
  35. Lawrence JM (2003) Preliminary report on the natural history of brown titi monkeys (Callicebus brunneus) at the Los Amigos Research Station, Madre de Dios, Peru. Am J Phys Anthropol Supplement 36:136Google Scholar
  36. Lemasson A, Ouattara K, Bouchet H, Zuberbühler K (2010) Speed of call delivery is related to context and caller identity in Campbell's monkey males. Naturwissenschaften 97:1023–1027. doi:10.1007/s00114-010-0715-6 PubMedCrossRefGoogle Scholar
  37. Ludwig G, Aguiar L, Miranda J, Teixeira G, Svoboda W, Malanski L, Shiozawa M, Hilst C, Navarro I, Passos F (2007) Cougar predation on black-and-gold howlers on Mutum Island, Southern Brazil. Int J Primatol 28:39–46. doi:10.1007/s10764-006-9103-7 CrossRefGoogle Scholar
  38. Macedonia JM, Evans CS (1993) Variation among mammalian alarm call systems and the problem of meaning in animal signals. Ethology 93:177–197. doi:10.1111/j.1439-0310.1993.tb00988.x CrossRefGoogle Scholar
  39. Manser MB (2001) The acoustic structure of suricates' alarm calls varies with predator type and the level of response urgency. Proc Roy Soc Lond B 268:2315–2324CrossRefGoogle Scholar
  40. Manser MB, Seyfarth RM, Cheney DL (2002) Suricate alarm calls signal predator class and urgency. Trends Cogn Sci 6:55–57PubMedCrossRefGoogle Scholar
  41. Marler P (1955) Characteristics of some animal calls. Nature 176:6–8CrossRefGoogle Scholar
  42. Martin P, Bateson P (2007) Measuring behaviour: an introductory guide, 3rd edn. Cambridge University Press, CambridgeGoogle Scholar
  43. Mendoza SP, Mason WA (1986) Parental division-of-labor and differentiation of attachments in a monogamous primate (Callicebus moloch). Anim Behav 34:1336–1347CrossRefGoogle Scholar
  44. Miller LE, Treves A (2007) Predation on primates: past studies, current challenges, and directions for the future. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 535–547Google Scholar
  45. Miranda J, Bernardi I, Moro-Rios R, Passos F (2006) Antipredator behavior of brown howlers attacked by black hawk-eagle in Southern Brazil. Int J Primatol 27:1097–1101. doi:10.1007/s10764-006-9062-z CrossRefGoogle Scholar
  46. Moynihan M (1966) Communication in the titi monkey, Callicebus. J Zool 150:77–127. doi:10.1111/j.1469-7998.1966.tb02999.x CrossRefGoogle Scholar
  47. Müller KH (1995) Ranging in masked titi monkeys (Callicebus personatus) in Brazil. Folia Primatol 65:224–228CrossRefGoogle Scholar
  48. Müller AE, Anzenberger G (2002) Duetting in the titi monkey Callicebus cupreus: structure, pair specificity and development of duets. Folia Primatol 73:104–115PubMedCrossRefGoogle Scholar
  49. Mundry R, Sommer C (2007) Discriminant function analysis with nonindependent data: consequences and an alternative. Anim Behav 74:965–976. doi:10.1016/j.anbehav.2006.12.028 CrossRefGoogle Scholar
  50. Ouattara K, Lemasson A, Zuberbühler K (2009) Campbell’s monkeys use affixation to alter call meaning. Plos One 4:e7808. doi:10.1371/journal.pone.0007808
  51. Oversluijs Vasquez MR, Heymann EW (2001) Crested eagle (Morphnus guianensis) predation on infant tamarins (Saguinus mystax and Saguinus fuscicollis, Callitrichinae). Folia Primatol 72:301–303PubMedCrossRefGoogle Scholar
  52. Owings DH, Virginia RA (1978) Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70CrossRefGoogle Scholar
  53. Rendall D, Owren MJ, Ryan MJ (2009) What do animal signals mean? Anim Behav 78:233–240. doi:10.1016/j.anbehav.2009.06.007 CrossRefGoogle Scholar
  54. Rendell LE, Matthews JN, Gill A, Gordon JCD, Macdonald DW (1999) Quantitative analysis of tonal calls from five odontocete species, examining interspecific and intraspecific variation. J Zool 249:403–410. doi:10.1111/j.1469-7998.1999.tb01209.x CrossRefGoogle Scholar
  55. Robinson JG (1979a) Analysis of the organization of vocal communication in the titi monkey Callicebus moloch. Z Tierpsychol 49:381–405PubMedCrossRefGoogle Scholar
  56. Robinson JG (1979b) Vocal regulation of use of space by groups of titi monkeys Callicebus moloch. Behav Ecol Sociobiol 5:1–15CrossRefGoogle Scholar
  57. Robinson JG (1981) Vocal regulation of inter- and intragroup spacing during boundary encounters in the titi monkey, Callicebus moloch. Primates 22:161–172. doi:10.1007/bf02382607 CrossRefGoogle Scholar
  58. Robinson SK (1994) Habitat selection and foraging ecology of raptors in Amazonian Peru. Biotropica 26:443–458CrossRefGoogle Scholar
  59. Robinson JG, Wright PC, Kinzey WG (1987) Monogamous cebids and their relatives: intergroup calls and spacing. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) In primate societies. University of Chicago Press, Chicago, pp 44–53Google Scholar
  60. Rowe N (1996) The pictorial guide to the living primates. Pogonias Press, East Hampton NYGoogle Scholar
  61. Sampaio DT, Ferrari SF (2005) Predation of an infant titi monkey (Callicebus moloch) by a tufted capuchin (Cebus apella). Folia Primatol 76:113–115. doi:10.1159/000073617 PubMedCrossRefGoogle Scholar
  62. Schel AM, Tranquilli S, Zuberbühler K (2009) The alarm call system of two species of black-and-white colobus monkeys (Colobus polykomos and Colobus guereza). J Comp Psychol 123:136–150. doi:10.1037/A0014280 PubMedCrossRefGoogle Scholar
  63. Seyfarth RM, Cheney DL (1980) The ontogeny of vervet monkey alarm calling behavior: a preliminary report. Z Tierpsychol 54:37–56CrossRefGoogle Scholar
  64. Seyfarth RM, Cheney DL, Marler P (1980a) Monkey responses to three different alarm calls—evidence of predator classification and semantic communication. Science 210:801–803PubMedCrossRefGoogle Scholar
  65. Seyfarth RM, Cheney DL, Marler P (1980b) Vervet monkey alarm calls—semantic communication in a free-ranging primate. Anim Behav 28:1070–1094CrossRefGoogle Scholar
  66. Sieving KE, Hetrick SA, Avery ML (2010) The versatility of graded acoustic measures in classification of predation threats by the tufted titmouse Baeolophus bicolor: exploring a mixed framework for threat communication. Oikos 119:264–276. doi:10.1111/j.1600-0706.2009.17682.x CrossRefGoogle Scholar
  67. Silva JA, Talamoni SA (2003) Diet adjustments of maned wolves, Chrysocyon brachyurus (Illiger) (Mammalia, Canidae), subjected to supplemental feeding in a private natural reserve, Southeastern Brazil. Revista Brasileira de Zoologia 20:339–345CrossRefGoogle Scholar
  68. Strier KB (2007) Primate behavioral ecology. Allyn and Bacon, BostonGoogle Scholar
  69. Tabachnick BG, Fidell LS (2001) Using multivariate statistics, 4th edn. Allyn & Bacon, BostonGoogle Scholar
  70. Templeton CN, Greene E, Davis K (2005) Allometry of alarm calls: black-capped chickadees encode information about predator size. Science 308:1934–1937. doi:10.1126/science.1108841 PubMedCrossRefGoogle Scholar
  71. Terborgh J (1983) Five New World primates: a study in comparative ecology. Princeton University Press, Princeton, N.JGoogle Scholar
  72. Valeggia CR, Mendoza SP, Fernandez-Duque E, Mason WA, Lasley B (1999) Reproductive biology of female titi monkeys (Callicebus moloch) in captivity. Am J Primatol 47:183–195PubMedCrossRefGoogle Scholar
  73. Vasconcelos MF (2001) Adições à avifauna da Serra do Caraça, Minas Gerais. Atualidades Ornitológicas. Atualidades Ornitológicas 104:3–4Google Scholar
  74. Vasconcelos MF, Melo Junior TA (2001) An ornithological survey of Serra do Caraça, Minas Gerais. Brazil Cotinga 15:21–31Google Scholar
  75. Wheeler B (2010) Production and perception of situationally variable alarm calls in wild tufted capuchin monkeys (Cebus apella nigritus). Behav Ecol Sociobiol 64:989–1000. doi:10.1007/s00265-010-0914-3 CrossRefGoogle Scholar
  76. Zuberbühler K (2000a) Causal knowledge of predators' behaviour in wild Diana monkeys. Anim Behav 59:209–220PubMedCrossRefGoogle Scholar
  77. Zuberbühler K (2000b) Referential labelling in Diana monkeys. Anim Behav 59:917–927PubMedCrossRefGoogle Scholar
  78. Zuberbühler K (2001) Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli. Behav Ecol Sociobiol 50:414–422CrossRefGoogle Scholar
  79. Zuberbühler K (2009) Survivor signals: the biology and psychology of animal alarm calling. Adv Stud Behav 40:277–322. doi:10.1016/S0065-3454(09)40008-1 CrossRefGoogle Scholar
  80. Zuberbühler K, Noë R, Seyfarth RM (1997) Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589–604CrossRefGoogle Scholar
  81. Zuberbühler K, Jenny D, Bshary R (1999) The predator deterrence function of primate alarm calls. Ethology 105:477–490CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Cristiane Cäsar
    • 1
    • 2
    • 3
  • Richard Byrne
    • 1
  • Robert J. Young
    • 2
  • Klaus Zuberbühler
    • 1
  1. 1.School of PsychologyUniversity of St AndrewsScotlandUnited Kingdom
  2. 2.Conservation, Ecology and Animal Behaviour Group, Department of Post-Graduate Studies in Zoology, Prédio 41Pontifícia Universidade Católica de Minas GeraisBelo HorizonteBrazil
  3. 3.Instituto Cultural InhotimBrumadinhoBrazil

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