Skip to main content
SpringerLink
Log in

Cognitive consequences of cooperative breeding in primates?

  • Review
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Several hypotheses propose that cooperative breeding leads to increased cognitive performance, in both nonhuman and human primates, but systematic evidence for such a relationship is missing. A causal link might exist because motivational and cognitive processes necessary for the execution and coordination of helping behaviors could also favor cognitive performance in contexts not directly related to caregiving. In callitrichids, which among primates rely most strongly on cooperative breeding, these motivational and cognitive processes include attentional biases toward monitoring others, the ability to coordinate actions spatially and temporally, increased social tolerance, increased responsiveness to others’ signals, and spontaneous prosociality. These processes are likely to enhance performance particularly in socio-cognitive contexts. Therefore, cooperatively breeding primates are expected to outperform their independently breeding sister taxa in socio-cognitive tasks. We evaluate this prediction by reviewing the literature and comparing cognitive performance in callitrichids with that of their sister taxa, i.e. squirrel monkeys, which are independent breeders, and capuchin monkeys, which show an intermediate breeding system. Consistent with our prediction, this review reveals that callitrichids systematically and significantly outperform their sister taxa in the socio-cognitive, but not in the non-social domain. This comparison is complemented with more qualitative evaluations of prosociality and cognitive performance in non-primate cooperative breeders, which suggest that among mammals, cooperative breeding generally produces conditions conducive to socio-cognitive performance. In the hominid lineage, however, the adoption of extensive allomaternal care presumably resulted in more pervasive cognitive consequences, because the motivational consequences of cooperative breeding was added to an ape-level cognitive system already capable of understanding simple mental states, which enabled the emergence of shared intentionality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Notes

  1. Whether social influences on the acceptance of novel foods by adults (Visalberghi and Addessi 2000a, b, 2003; Addessi et al. 2007) also differ between callitrichids and their sister taxa cannot be decided conclusively on the basis of the data currently available. Addessi et al. (2007) found that in two species of cooperatively breeding primates, in marmosets (Callithrix jacchus) and in Goeldi's monkeys (Callimico goeldii), the acceptance of novel food was not increased by group mates eating either the same or different food, as compared to the mere presence of group mates not eating anything. In the same study, Goeldi's monkeys, but not marmosets, paid more visual attention if their group mates were eating the same novel food. However, different results might have been obtained if novelty levels had been adjusted more closely to species-typical affordances because the neophobic Goeldi's monkeys never tasted the new food in any condition, whereas common marmosets’ responsiveness was very high already in the presence condition, presumably resulting in a ceiling effect in the other conditions. Capuchin monkeys were tested in a similar setting (Visalberghi and Addessi 2000b), and the kind of food the group mates were consuming also did not affect the acceptance of novel foods. However, no comparison of the social influence alone is possible because the callitrichids, unlike the capuchins, were not tested in a control condition with novel food in the absence of group members. In addition, there is evidence that experimentally induced food aversions can be reversed through interaction with non-averse conspecifics in adult common marmosets (Queyras et al. 2000) and tamarins (Saguinus fuscicollis and Saguinus labiatus, Prescott et al. 2005), but comparative data from sister taxa are again lacking.

References

  • Achenbach GG, Snowdon CT (1999) Response to sibling birth in juvenile cotton-top tamarins (Saguinus oedipus). Behaviour 135:845–862

    Google Scholar 

  • Addessi E, Chiarotti F, Visalberghi E, Anzenberger AA (2007) Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi’s monkeys (Callimico goeldii). Am J Primatol 69:1210–1222

    PubMed  Google Scholar 

  • Addessi E, Crescimbene L, Visalberghi E (2008) Food and token quantity discrimination in capuchin monkeys (Cebus apella). Anim Cogn 11:275–282

    PubMed  Google Scholar 

  • Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim Behav 49:201–208

    Google Scholar 

  • Anderson JR, Awazu S, Fujita K (2000) Can squirrel monkeys (Saimiri sciureus) learn self-control? A study using food array selection tests and revers-reward contingency. J Exp Psychol Anim Behav Process 26:87–97

    CAS  PubMed  Google Scholar 

  • Anderson JR, Kuroshima H, Kuwahata H, Fujita K (2004) Do squirrel monkeys (Saimiri sciureus) and capuchin monkeys (Cebus apella) predict that looking leads to touching. Anim Cogn 7:185–192

    PubMed  Google Scholar 

  • Aureli F, Schaffner C (2006) Causes, consequences and mechanisms of reconciliation: the role of cooperation. In: Kappeler PM, van Schaik CP (eds) Cooperation in primates and humans. Mechanisms and evolution. Springer, Heidelberg

    Google Scholar 

  • Baker PJ, Harris S (2004) Red foxes. The behavioural ecology of red foxes in urban Bristol. In: Macdonald DW, Sillero-Zubiri C (eds) Biology and conservation of wild canids. Oxford University Press, Oxford, pp 207–216

    Google Scholar 

  • Baldovino MC, Bitetti MS (2008) Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier? Folia Primatol 79:79–92

    PubMed  Google Scholar 

  • Bales K, Dietz J, Baker A, Miller K, Tardif SD (2000) Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatol 71:27–38

    CAS  PubMed  Google Scholar 

  • Baron-Cohen S (1999) Evolution of a theory of mind? In: Corballis MC, Lea SEG (eds) The descent of mind: psychological perspectives on hominid evolution. University Press, Oxford

    Google Scholar 

  • Barrickman NL, Bastian ML, Isler K, van Schaik CP (2008) Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild. J Hum Evol 54:568–590

    PubMed  Google Scholar 

  • Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512

    CAS  PubMed  Google Scholar 

  • Boesch C (1991) Teaching among wild chimpanzees. Anim Behav 41:530–532

    Google Scholar 

  • Boesch C (1994) Cooperative hunting in wild chimpanzees. Anim Behav 48:653–667

    Google Scholar 

  • Boesch C (2002) Cooperative hunting roles among taï chimpanzees. Hum Nat 13:27–46

    Google Scholar 

  • Boinski S (1994) Affiliation patterns among male Costa Rican squirrel monkeys. Behaviour 130:191–209

    Google Scholar 

  • Boinski S, Fragaszy DM (1989) The ontogeny of foraging in squirrel monkeys, Saimiri oerstedi. Anim Behav 37:415–428

    Google Scholar 

  • Bräuer J, Call J, Tomasello M (2004) Visual perspective taking in dogs (Canis familiaris) in the presence of barriers. Appl Anim Behav Sci 88(3–4):299–317

    Google Scholar 

  • Bräuer J, Kaminski J, Riedel J, Call J, Tomasello M (2006) Making inferences about the location of hidden food: social dog, causal ape. J Comp Psychol 120:38–47

    PubMed  Google Scholar 

  • Bräuer J, Call J, Tomasello M (2007) Chimpanzees really know what others can see in a competitive situation. Anim Cogn 10:439–448

    PubMed  Google Scholar 

  • Brosnan SF, Freeman C, De Waal FBM (2006) Partner’s behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys. Am J Primatol 68:713–724

    PubMed  Google Scholar 

  • Brown GR, Almond REA, van Bergen Y (2004) Begging, stealing and offering: food transfer in non-human primates. Adv Stud Behav 34:265–295

    Google Scholar 

  • Brown GR, Almond REA, Bates NJ (2005) Adult-infant food transfer in common marmosets: an experimental study. Am J Primatol 65:301–312

    PubMed  Google Scholar 

  • Bruce AS (2000) Social structure and helping behavior in captive elephants. Zoo Biol 19(5):447–459

    Google Scholar 

  • Bugnyar T, Huber L (1997) Push or pull: an experimental study on imitation in marmosets. Anim Behav 53:1–14

    Google Scholar 

  • Burkart JM (2009) Socio-cognitive abilities and cooperative breeding. In: Röska-Hardy LS, Neumann-Held EM (eds) Learning from animals? Examining the nature of human uniqueness. Psychology Press, New York, pp 123–141

  • Burkart JM, Heschl A (2006) Geometrical gaze following in common marmosests (Callithrix jacchus). J Comp Psychol 120(2):120–130

    PubMed  Google Scholar 

  • Burkart JM, Heschl A (2007) Perspective taking or behaviour reading? Understanding of visual access in common marmosets (Calithrix jacchus). Anim Behav 73:457–469

    Google Scholar 

  • Burkart JM, Fehr E, Efferson C, van Schaik CP (2007) Other-regarding preferences in a non-human primate, the common marmoset (Callithrix jacchus). Proc Natl Acad Sci USA 104(50):19762–19766

    CAS  PubMed  Google Scholar 

  • Burkart JM, Strasser A, Foglia M (2009a) Trade-offs between social learning and innovativeness in common marmosets (Callithrix jacchus)? Anim Behav 77:1291–1301

    Google Scholar 

  • Burkart JM, Hrdy SB, van Schaik CP (2009b) Cooperative breeding and human cognitive evolution. Evol Anthropol (in press)

  • Caldwell C, Whiten A (2002) Evolutionary perspectives on imitation: is a comparative psychology of social learning possible? Anim Cogn 5:193–208

    PubMed  Google Scholar 

  • Caldwell C, Whiten A (2003) Scrounging facilitates social learning in common marmosets, Callithrix jacchus. Anim Behav 65:1085–1092

    Google Scholar 

  • Caldwell C, Whiten A (2004) Testing for social learning and imitation in common marmosets, Callithrix jacchus, using an artificial fruit. Anim Cogn 7:77–85

    PubMed  Google Scholar 

  • Call J (2007) Social knowledge in primates. In: Dunbar RIM, Barrett L (eds) Handbook of evolutionary psychology. Oxford University Press, New York, pp 71–81

    Google Scholar 

  • Call J, Carpenter M (2002) Three sources of information in social learning. In: Dautenhahn K, Nehaniv CL (eds) Imitation in animals and artifacts. MIT Press, Cambridge

    Google Scholar 

  • Call J, Agnetta B, Tomasello M (2000) Cues that chimpanzees do and do not use to find hidden objects. Anim Cogn 3:23–34

    Google Scholar 

  • Campbell CJ, Fuentes A, MacKinnon KC, Panger MA, Bearder SK (eds) (2007) Primates in perspective. Oxford University Press, New York

    Google Scholar 

  • Canavez F, Moreira M, Ladasky J, Pissinatti A, Parham P, Seuz H (1999) Molecular phylogeny of New World primates (Platyrrhini) based on sub>2-microglobulin DNA sequences. Molecular Phyologen Evol 12:74–82

    CAS  Google Scholar 

  • Caro TM, Hauser MD (1992) Is there teaching in nonhuman animals? Q Rev Biol 67:151–172

    CAS  PubMed  Google Scholar 

  • Cheney DL, Seyfarth RM (1990) Attending to behavior versus attending to knowledge: examining monkeys’ attribution of mental states. Anim Behav 40:742–753

    Google Scholar 

  • Cheney DL, Seyfarth RM (2007) Baboon metaphysics. University of Chicago Press, Chicago, p 348

    Google Scholar 

  • Chisholm JS (2003) Uncertainty, contingency, and attachment: a life history theory of theory of mind. In: Sterelny K, Fitness J (eds) From mating to mentality. Evaluating evolutionary psychology. Psychology Press, New York, pp 125–154

    Google Scholar 

  • Cools AKA, van Hout AJ-M, Melissen HJ (2008) Canine reconciliation and third-party-initiated postconflict affiliation: do peacemaking social mechanisms in dogs rival those of higher primates? Ethology 114:53–63

    Google Scholar 

  • Coussi-Korbel S, Fragaszy DM (1995) On the relation between social dynamics and social learning. Anim Behav 50:1441–1453

    Google Scholar 

  • Creel S, Creel NM (2002) The African wild dog. Behavior, ecology, and conservation. Princeton University Press, New Jersey, p 340

    Google Scholar 

  • Cronin KA, Snowdon CT (2008) The effects of unequal reward distributions on cooperative problem solving by cottontop tamarins, Saguinus oedipus. Anim Behav 75:245–257

    PubMed  Google Scholar 

  • Cronin KA, Kurian AV, Snowdon CT (2005) Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus). Anim Behav 69:133–142

    PubMed  Google Scholar 

  • Cronin KA, Schroeder KKE, Rothewell ES, Silk JB, Snowdon CT (2009) Cooperatively breeding cottontop tamarins (Saguinus oedipus) do not donate rewards to their long-term mates. J Comp Psychol (in press)

  • Csibra G (2007) Teachers in the wild. Trends Cogn Sci 11(3):95–96

    PubMed  Google Scholar 

  • Custance DM, Whiten A, Fredman T (1999) Social learning of an artificial fruit task in capuchin monkeys (Cebus apella). J Comp Psychol 113:13–23

    Google Scholar 

  • Custance DM, Whiten A, Fredman T (2002) Social learning and primate reintroduction. Int J Primatol 23(3):479–499

    Google Scholar 

  • Dautenhahn K, Nehaniv CL (2002) Imitation in animals and artifacts. MIT Press, Cambridge

    Google Scholar 

  • de Blois ST, Novak MA, Bond M (1998) Object permanence in orangutans (Pongo pygmaeus) and squirrel monkeys (Saimiri sciureus). J Comp Psychol 112:137–152

    PubMed  Google Scholar 

  • De la Torre S, Snowdon CT (2002) Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea. Anim Behav 63:847–856

    Google Scholar 

  • de Waal FBM (1997) Food transfers through mesh in brown capuchins. J Comp Psychol 111:370–378

    PubMed  Google Scholar 

  • de Waal FBM, Leimgruber K, Greenberg AR (2008) Giving is self-rewarding for monkeys. Proc Natl Acad Sci USA 105(36):13685–13689

    PubMed  Google Scholar 

  • Deaner RO, van Schaik CP, Johnson V (2006) Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evol Psychol 4:149–196

    Google Scholar 

  • Deaner RO, Isler K, Burkart JM, van Schaik CP (2007) Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav Evol 70(2):115–124

    PubMed  Google Scholar 

  • Dell’Mour V, Range F, Huber L (2009) Social learning and mother’s behavior in manipulative tasks in infant marmosets. Am J Primatol 71:1–7

    Google Scholar 

  • Digby LJ (1994) Social organization in a wild population of Callithrix jacchus: II. Intragroup social behavior. Primates 36(3):361–375

    Google Scholar 

  • Digby LJ, Ferrari SF, Saltzman W (2007) Callitrichines: the role of competition in cooperatively breeding species. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 85–105

    Google Scholar 

  • Doré FY, Fiset S, Goulet S, Dumas MC, Gagnon S (1996) Search behavior in cats and dogs: interspecific differences in working memory and spatial cognition. Anim Learn Behav 24:142–149

    Google Scholar 

  • Dumas C, Brunet C (1994) Object permanence in capuchin monkeys: a study of invisible displacements. Can J Exp Psychol 48:341–358

    Google Scholar 

  • Dumas C, Pagé DD (2006) Strategy planning in dogs (Canis familiaris) in a progressive elimination task. Behav Process 73:22–28

    Google Scholar 

  • Egnor SER, Hauser MD (2004) A paradox in the evolution of primate vocal learning. Trends Neurosci 27(11):649–654

    CAS  PubMed  Google Scholar 

  • Elowson AM, Snowdon CT (1994) Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Anim Behav 47(6):1267–1277

    Google Scholar 

  • Elowson AM, Sweet CS, Snowdon CT (1992) Ontogeny of trill and J-call vocalizations in the pygmy marmoset (Cebuella pygmaea). Anim Behav 42:703–715

    Google Scholar 

  • Elowson AM, Snowdon CT, Lazaro-Perea C (1998a) ‘Babbling’ and social context in infant monkeys: parallels to human infants. Trends Cogn Sci 2:31–37

    Google Scholar 

  • Elowson AM, Snowdon CT, Lazaro-Perea C (1998b) Infant ‘babbling’ in a nonhuman primate: complex sequences of vocal behavior. Behaviour 135:643–664

    Google Scholar 

  • Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24(6):581–604

    CAS  PubMed  Google Scholar 

  • Erdohegyi Á, Topál J, Virányi Z, Miklósi Á (2007) Dog-logic: inferential reasoning in a two-way choice task and its restricted use. Anim Behav 74(4):725–737

    Google Scholar 

  • Estes RD, Goddard J (1967) Prey selection and hunting behavior of the African hunting dog. J Wildl Manag 31:52–70

    Google Scholar 

  • Fedigan L, Carnegie SD, Jack KM (2008) Predictors of reproductive success in female white-faced capuchins (Cebus capucinus). Am J Physic Anthropol 137:82–90

    Google Scholar 

  • Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 423:785–791

    Google Scholar 

  • Feistner AT, Price EC (1990) Food-sharing in cotton-top tamarins (Saguinus oedipus). Folia Primatol 54:34–45

    CAS  PubMed  Google Scholar 

  • Feistner AT, Price EC (1991) Food offering in New World primates: two species added. Folia Primatol 57:165–168

    Google Scholar 

  • Feistner AT, Price EC (2000) Food sharing in black lion tamarins (Leontopithecus crysopygus). Am J Primatol 52(1):47–54

    CAS  PubMed  Google Scholar 

  • Ferrari SF (1987) Food transfer in a wild marmoset group. Folia Primatol 48(3–4):203–206

    CAS  PubMed  Google Scholar 

  • Fichtel C (2008) Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux’s sifakas (Propithecus verreauxi verreauxi). Am J Primatol 70:127–135

    PubMed  Google Scholar 

  • Flavell JH (1985) Cognitive development. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Fragaszy DM, Visalberghi E (1989) Social influences on the acquisition of tool-using behaviors in tufted capuchin monkeys (Cebus apella). J Comp Psychol 103(2):159–170

    CAS  PubMed  Google Scholar 

  • Fragaszy DM, Baer J, Adams-Curtis L (1991) Behavioural development and maternal care in tufted capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus) from birth through seven months. Dev Psychobiol 24:375–394

    CAS  PubMed  Google Scholar 

  • Fragaszy DM, Feuerstein JM, Mitra D (1997a) Transfers of food from adults to infants in tufted capuchins (Cebus apella). J Comp Psychol 111(2):194–200

    CAS  PubMed  Google Scholar 

  • Fragaszy DM, Visalberghi E, Galloway A (1997b) Infant capuchin monkey’s behaviour with novel foods: opportunism not selectivity. Anim Behav 53:1337–1343

    PubMed  Google Scholar 

  • Franks NR, Richerdson T (2006) Teaching in tandem-running ants. Nature 439:153

    CAS  PubMed  Google Scholar 

  • Fredman T, Whiten A (2008) Observational learning from tool using models by human-reared and mother-reared capuchin monkeys (Cebus apella). Anim Cogn 11:295–309

    PubMed  Google Scholar 

  • Garber PA, Moya L, Malaga C (1984) A preliminary field study of the moustached tamarin monkey (Saguinus mystax) in northeastern Peru: Questions concerned with the evolution of a communal breeding system. Folia Primatol 42:17–32

    Google Scholar 

  • Gaudio JL, Snowdon CT (2008) Spatial cues more salient than color cues in cotton-top tamarins (Saguinus oedipus) reversal learning. J Comp Psychol 122:441–444

    Google Scholar 

  • Genty E, Palmier C, Roeder J (2004) Learning to suppress responses to the larger of two rewards in two species of lemurs, Eulemur fulvus and E. macaco. Anim Behav 67:925–932

    Google Scholar 

  • Hammerschmidt K, Freudenstein T, Jürgens U (2001) Vocal development in squirrel monkeys. Behaviour 138:1179–1204

    Google Scholar 

  • Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9(9):439–444

    PubMed  Google Scholar 

  • Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785

    PubMed  Google Scholar 

  • Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–2636

    CAS  PubMed  Google Scholar 

  • Hare B, Addessi E, Call J, Tomasello M, Visalberghi E (2003) Do capuchin monkeys, Cebus apella, know what conspecifics do and do not see? Anim Behav 65:131–142

    Google Scholar 

  • Hare B, Plyusinina I, Ignacio N, Schepina O, Stepika A, Wrangham RW, Trut L (2005) Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol 2005:226–230

    Google Scholar 

  • Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephants fit in? Neurosci Biobehav Rev 32:86–98

    PubMed  Google Scholar 

  • Hauser MD (1989) Ontogenetic changes in the comprehension and production of vervet monkey (Cercopithecus aetiops) vocalizations. J Comp Psychol 103:149–158

    Google Scholar 

  • Hauser MD, Chen MK, Chen F, Chuang E (2003) Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc R Soc B 279:2363–2370

    Google Scholar 

  • Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104(9):3562–3567

    CAS  PubMed  Google Scholar 

  • Herrmann E, Call J, Hernandez-Lloreda MV, Hare B, Tomasello M (2007) Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science 317:1360–1366

    CAS  PubMed  Google Scholar 

  • Heyes C (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:702–731

    Google Scholar 

  • Holland B, Rice WR (1998) Chase-away sexual selection: antagonistic seduction vs resistance. Int J Org Evol 52(1):1–7

    Google Scholar 

  • Hrdy S (1999) Mother nature: a history of mothers, infants, and natural selection. Pantheon Books, New York

    Google Scholar 

  • Hrdy S (2005a) Comes the child before the man: how cooperative breeding and prolonged postweaning dependence shaped human potentials. In: Hewlett B, Lamb M (eds) Hunter gatherer childhood. Transactions, Piscataway

    Google Scholar 

  • Hrdy S (2005b) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Ahnert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis; from the 92nd Dahlem Workshop Report. MIT Press, Cambridge, pp 9–32

    Google Scholar 

  • Hrdy S (2009) Mothers and others. The evolutionary origins of mutual understanding. Harvard University Press, Cambridge

    Google Scholar 

  • Humle T, Snowdon CT (2008) Socially biased learning in the acquisition of a complex foraging task in juvenile cottontop tamarins (Saguinus oedipus). Anim Behav 75:267–277

    Google Scholar 

  • Isler K, van Schaik CP (2009) The expensive brain: a framework for explaining evolutionary changes in brain size. J Hum Evol (in press)

  • Itakura S, Anderson JR (1996) Learning to use experimenter-given cues during an object-choice task by a capuchin monkey. Curr Psychol Cogn 15:103–112

    Google Scholar 

  • Jack KM (2007) The cebines. Toward an explanation of variable social structure. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger MA, Bearder SK (eds) Primates in perspective. Oxford University Press, New York

    Google Scholar 

  • Janik VM, Slater PJB (2000) The different roles of social learning in vocal communication. Anim Behav 60(1):1–11

    PubMed  Google Scholar 

  • Jantschke B, Welker C, Klaiber-Schuh A (1998) Rearing without paternal help in the Bolivian owl monkey Aotus azarae boliviensis: a case study. Folia Primatol 69:115–120

    Google Scholar 

  • Jensen K, Hare B, Call J, Tomasello M (2006) What’s in it for me? Self-regard precludes altruism and spite in chimpanzees. Proc R Soc B 273:1013–1021

    PubMed  Google Scholar 

  • Joyce SM, Snowdon CT (2007) Developmental changes in food transfers in cotton-top tamarins (Saguinus oedipus). Am J Primatol 69:955–965

    PubMed  Google Scholar 

  • Kaminski J, Call J, Fischer J (2004) Word learning in a domestic dog: evidence for “fast mapping”. Science 304(5677):1682–1683

    CAS  PubMed  Google Scholar 

  • Karin-D’Arcy RM, Povinelli DJ (2002) Do chimpanzees know what each other see? A closer look. Int J Comp Psychol 15(1):853–865

    Google Scholar 

  • Kelley J (2004) Life history and cognitive evolution in the apes. In: Russel AE, Begun DR (eds) The evolution of thought. Cambridge University Press, Cambridge

    Google Scholar 

  • Koenig A, Rothe H (1991) Social relationships and individual contribution to cooperative behaviour in captive common marmosets (Callithrix jacchus). Primates 32(2):183–195

    Google Scholar 

  • König A (1995) Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus). Am J of Primatol 35(4):311–317

    Google Scholar 

  • Kostan KM, Snowdon CT (2002) Attachment and social preferences in cooperatively-reared cotton-top tamarins. Am J Primatol 57:131–139

    PubMed  Google Scholar 

  • Kralik J, Hauser MD, Zimlicki R (2002) The relationship between problem solving and inhibitory control: cotton-top tamarin (Saguinus oedipus) performance in a reversed contingency task. J Comp Psychol 116(1):39–50

    PubMed  Google Scholar 

  • Kramer KL (2005) Children’s help and the pace of reproduction: cooperative breeding in humans. Evol Anthropol 14(6):224–237

    Google Scholar 

  • Kumashiro M, Ishibashi H, Uchiyama Y, Itakura S, Murata A, Iriki A (2003) Natural imitation induced by joint attention in Japanese monkeys. Int J Psychophysiol 50:81–99

    PubMed  Google Scholar 

  • Lakshminarayanan VR, Santos LR (2008) Capuchin monkeys are sensitive to others’ welfare. Curr Biol 18(21):R999–R1000

    CAS  PubMed  Google Scholar 

  • Leadbeater E, Raine NE, Chittka L (2006) Social learning: ants and the meaning of teaching. Curr Biol 16(9):R323–R325

    CAS  PubMed  Google Scholar 

  • Lee PC, Moss CJ (1986) Early maternal investment in male and female elephant calves. Behav Ecol Sociobiol 18:35–361

    CAS  Google Scholar 

  • Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in brids and primates. Brain Behav Evol 63:233–246

    PubMed  Google Scholar 

  • Lieblich AK, Symmes D, Newman JD, Shapiro M (1980) Development of the isolation peep in laboratory-bred squirrel monkeys. Anim Behav 28:1–9

    Google Scholar 

  • Ligon JD, Burt DB (2004) Evolutionary origins. In: Koenig W, Dickinson J (eds) Ecology and evolution of cooperative breeding in birds. University Press, Cambridge, pp 5–34

    Google Scholar 

  • Lonsdorf E (2006) What is the role of mothers in the acquisition of termite-fishing behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? Anim Cogn 9(1):36–46

    PubMed  Google Scholar 

  • Macdonald DW (1979) “Helpers” in fox society. Nature 282(5734):69–71

    Google Scholar 

  • Macdonald DW (1987) Running with the fox. BBC Books, London

    Google Scholar 

  • Macdonald DW (2001) The new encyclopedia of mammals. Oxford University Press, New York

    Google Scholar 

  • Macdonald DW, Sillero-Zubiri C (2004a) Biology and conservation of wild canids. Oxford University Press, New York

    Google Scholar 

  • Macdonald DW, Sillero-Zubiri C (2004b) Dramatis personae. In: Macdonald DW, Sillero-Zubiri C (eds) Biology and conservation of wild canids. Oxford University Press, New York

    Google Scholar 

  • Malcolm JR, Marten K (1982) Natural selection and the communal rearing of pups in African wild dogs (Lycaon pictus). Behav Ecol Sociobiol 10(1):1–13

    Google Scholar 

  • Matsuzawa S, Biro D, Humle T, Inoue-Nakamura N, Tonooka R, Yamakoshi G (2001) Emergence of culture in wild chimpanzees: education by master-apprenticeship. In: Matsuzawa S (ed) Primate origins of human cognition and behavior. Springer, Tokyo

    Google Scholar 

  • McNutt JW (1996) Adoption in African wild dogs, Lycaon pictus. J Zool 240:163–173

    Google Scholar 

  • Mendes N, Huber L (2004) Object permanence in common marmosets (Callithrix jacchus). J Comp Psychol 118:103–112

    PubMed  Google Scholar 

  • Miklosi A, Csanyi V (2004) Comparative social cognition: what can dogs teach us? Anim Behav 67:995–1004

    Google Scholar 

  • Miklósi A, Polgardi R, Topal J, Csanyi V (1998) Use of experimenter-given cues in dogs. Anim Cogn 1:113–121

    Google Scholar 

  • Miklósi A, Polgardi R, Topal J, Csanyi V (2000) Intentional behaviour in dog-human communication: an experimental analysis of “showing” behaviour in the dog. Anim Cogn 3:159–166

    Google Scholar 

  • Mineka S, Cook M (1988) Social learning and the acquisition of snake fear in monkeys. In: Zentall TR, Galef BG (eds) Social learning: psychological and biological perspectives. Erlbaum, Hillsdale, pp 51–73

    Google Scholar 

  • Mitani JC, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40(4):213–220

    Google Scholar 

  • Mitani JC, Watts DP, Muller MN (2002) Recent developments in the study of wild chimpanzee behavior. Evol Anthropol 11:9–25

    Google Scholar 

  • Moscovice LR, Snowdon CT (2006) The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus. Anim Behav 71:933–943

    PubMed  Google Scholar 

  • Naderi S, Miklósi A, Doka A, Csanyi V (2001) Cooperative interactions between blind persons and their dog. Appl Anim Behav Sci 74:59–80

    Google Scholar 

  • Neiworth JJ, Burman MA, Basile BM, Lickteig MT (2002) Use of experimenter-given cues in visual co-orienting and in an object-choice task by a New World Monkey species, Cotton Top Tamarins (Saguinus oedipus). J Comp Psychol 116(1):3–11

    PubMed  Google Scholar 

  • Neiworth JJ, Steinmark E, Basile BM, Wonders R, Steely F, DeHart C (2003) A test of object permanence in a new-world monkey species, cotton top tamarins (Saguinus oedipus). Anim Cogn 6:27–37

    PubMed  Google Scholar 

  • Newman JD, Symmes D (1982) Inheritance and experience in the acquisition of primate acoustic behavior. In: Snowdon CT, Brown CH, Pertersen M (eds) Primate communication. Cambridge University Press, London

    Google Scholar 

  • Norcross JL, Newman JD (1993) Context and gender-specific differences in the acoustic structure of common marmosets (Callithrix jacchus). Am J Primatol 30:37–54

    Google Scholar 

  • O’Brien TG, Robinson J (1991) Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness. Behav 199:30–50

    Google Scholar 

  • Osthaus B, Slater AM, Lea SEG (2003) Can dogs defy gravity? A comparison with the human infant and a non-human primate. Dev Sci 6(5):489–497

    Google Scholar 

  • Perry S (1996) Female-female social relationships in wild white-faced capuchin monkeys, Cebus capucinus. Am J Primatol 40(2):167–182

    Google Scholar 

  • Pistorio AL, Vintch B, Wang X (2006) Acoustic analysis of vocal development in a New World primate, the common marmoset (Callithrix jacchus). J Acoust Soc Am 120(3):1655–1670

    PubMed  Google Scholar 

  • Poole JH, Moss CJ (2008) Elephant sociality and complexity: the scientific evidence. In: Wemmer C, Christen K (eds) Elephants and ethics: toward a morality of co-existence. Johns Hopkins University Press, Baltimore

  • Poole JH, Tyack PL, Stoeger-Howath AS, Watwood S (2005) Elephant capable of vocal learning. Nature 434:455–456

    CAS  PubMed  Google Scholar 

  • Premack D (2007) Human and animal cognition: continuity and discontinuity. Proc Natl Acad Sci USA 104(35):13861–13867

    CAS  PubMed  Google Scholar 

  • Prescott MJ, Buchanan-Smith HM, Smith AC (2005) Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus). Am J Primatol 65(4):313–326

    CAS  PubMed  Google Scholar 

  • Price E, Caldwell CA (2007) Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis. Behav Process 74(1):13–20

    Google Scholar 

  • Price E, Feistner AT (1993) Food sharing in lion tamarins: tests of three hypotheses. Am J Primatol 31(3):211–221

    Google Scholar 

  • Queyras A, Scolavino M, Puopolo M, Vitale A (2000) Social influence on induced food preference in common marmosets (Callithrix jacchus). Folia Primatol 71:367–374

    CAS  PubMed  Google Scholar 

  • Range F, Viranyi Z, Huber L (2007) Selective imitation in domestic dogs. Curr Biol 17:868–872

    CAS  PubMed  Google Scholar 

  • Rapaport LG (1999) Provisioning of young in golden lion tamarins (Callitrichidae, Leontopithecus rosalia): a test of the information hypothesis. Ethology 105(7):619–636

    Google Scholar 

  • Rapaport LG (2006) Parenting behaviour: babbling bird teachers? Curr Biol 16(17):R675–R677

    CAS  PubMed  Google Scholar 

  • Rapaport LG, Ruiz-Miranda CR (2002) Tutoring in wild golden lion tamarins. Int J Primatol 23(5):1063–1070

    Google Scholar 

  • Rapaport LG, Ruiz-Miranda C (2006) Ontogeny of provisioning in two populations of wild golden lion tamarins (Leontopithecus rosalia). Behav Ecol Sociobiol 60(5):724–735

    Google Scholar 

  • Ray DA, Xing JC, Hedges DJ, Hall MA, Laborde ME, Anders BA, White BR, Stoilova N, Fowlkes JD, Landry KE et al (2005) Alu insertion loci and platyrrhine primate phylogeny. Molecular Phyologen Evol 35:117–126

    CAS  Google Scholar 

  • Reader SM, Laland KN (2002) Social intelligence, innovation and enhanced brain size in primates. Proc Natl Acad Sci USA 99:4436–4441

    CAS  PubMed  Google Scholar 

  • Rosati AG, Stevens JR, Hare B, Hauser MD (2007) The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos, and human adults. Curr Biol 17:1–6

    Google Scholar 

  • Rose LM (1997) Vertebrate predation and food-sharing in Cebus and Pan. Int J Primatol 18:727–765

    Google Scholar 

  • Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71:93–113

    CAS  PubMed  Google Scholar 

  • Roush RS, Snowdown CT (2001) Food transfers and the development of feeding behavior and food-associated vocalizations in cotton-top tamarins. Ethology 107:415–429

    Google Scholar 

  • Rukstalis M, Fite JE, French JA (2003) Social change affects vocal structure in a callitrichid primate (Callithrix kuhlii). Ethology 109:327–340

    Google Scholar 

  • Russon AE (1997) Exploiting the expertise of others. In: Whiten A, Byrne RW (eds) Macchiavellian intelligence. II: Evaluations and extensions. Cambridge University Press, Cambridge, pp 174–206

    Google Scholar 

  • Santos LR, Hauser MD (1999) How monkeys see the eyes: cotton-top tamarins’ reaction to changes in visual attention and action. Anim Cogn 3:131–139

    Google Scholar 

  • Santos CV, French JA, Otta E (1997) Infant carrying behavior in callithrichid primates: Callithrix and Leontopithecus. Int J Primatol 18(6):889–907

    Google Scholar 

  • Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35(2):146–160

    CAS  PubMed  Google Scholar 

  • Schaffner CM, Caine NG (2000) The peacefulness of cooperatively breeding primates. In: Aureli F, De Waal FB (eds) Natural conflict resolution. University of California Press, Berkeley, pp 155–169

    Google Scholar 

  • Schino G, Spinozzi G, Berlinguer L (1990) Object concept and mental representation in Cebus apella and Macaca fascicularis. Primates 31:537–544

    Google Scholar 

  • Schrader L, Todt D (1993) Contact call parameters covary with social context in common marmosets, Callithrix jacchus. Anim Behav 46:1026–1028

    Google Scholar 

  • Schradin C, Anzenberger G (2003) Mothers, not fathers, determine the delayed onset of male carrying in Goeldi’s monkey (Calimico goeldii). J Hum Evol 45:389–399

    PubMed  Google Scholar 

  • Schulte BA (2000) Social structure and helping behavior in captive elephants. Zoo Biol 19(5):447–459

    Google Scholar 

  • Sear R, Mace R (2008) Who keeps children alive? A review of the effects of kin on child survival. Evol Hum Behav 29:1–18

    Google Scholar 

  • Seyfarth RM, Cheney DL (1986) Vocal development in vervet monkeys. Anim Behav 34:1640–1658

    Google Scholar 

  • Silk JB (2007) Empathy, sympathy and prosocial preferences in primates. In: Dunbar RIM, Barrett L (eds) Handbook of Evolutionary Psychology. Oxford University Press, New York, pp 115–126

  • Silk JB, Brosnan SF, Vonk J, Henrich J, Povinelli DJ, Richardson AS, Lambeth SP, Mascaro J, Schapiro SJ (2005) Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437:1357–1359

    CAS  PubMed  Google Scholar 

  • Snowdon CT (2001) Social processes in communication and cognition in callitrichid monkeys: a review. Anim Cogn 4:247–257

    Google Scholar 

  • Snowdon CT, Boe CY (2003) Social communication about unpalatable foods in tamarins (Saguinus oedipus). J Comp Psychol 117(2):142–148

    PubMed  Google Scholar 

  • Snowdon CT, Cronin KA (2007) Cooperative breeders do cooperate. Behav Process 76(2):138–141

    Google Scholar 

  • Snowdon CT, Elowson AM (1999) Pygmy marmosets modify call structure when paired. Ethology 105:893–908

    Google Scholar 

  • Snowdon CT, Elowson AM (2001) ‘Babbling’ in pygmy marmosets: development after infancy. Behaviour 138:1235–1248

    Google Scholar 

  • Snowdon CT, Pickhard JJ (1999) Family feuds: severe aggression among cooperatively breeding cotton-top tamarins. Int J Primatol 20(5):651–663

    Google Scholar 

  • Soltis J, Wegner FH, Newman JD (2003) Adult cortisol response to immature offspring play in captive squirrel monkeys. Physiol Behav 80:217–223

    CAS  PubMed  Google Scholar 

  • Steiper ME, Ruvolo M (2003) New World monkey phylogeny based on X-linked G6PD DNA sequences. Molecular Phylogen Evol 27:121–130

    CAS  Google Scholar 

  • Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two new world monkeys. Biol Lett 1:223–226

    PubMed  Google Scholar 

  • Stevens JR, Wood JN, Hauser MD (2007) When quantity trumps number: discrimination experiments in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus). Anim Cogn 10:429–437

    PubMed  Google Scholar 

  • Sutcliffe AG, Poole TB (1984) Intragroup agonistic behavior in captive groups of the common marmoset Callithrix jacchus jacchus. Int J Primatol 5(5):473–489

    Google Scholar 

  • Thornton A, McAuliffe K (2006) Teaching in wild meerkats. Science 313:227–229

    CAS  PubMed  Google Scholar 

  • Tomasello M (1996) Do apes ape? In: Heyes C, Galef BG (eds) Social learning in animals: the roots of culture. Academic Press, London, pp 319–346

    Google Scholar 

  • Tomasello M, Carpenter M (2007) Shared intentionality. Dev Sci 10(1):121–125

    PubMed  Google Scholar 

  • Tomasello M, Rakoczy H (2003) What makes human cognition unique? From individual to shared to collective intentionality. Mind Lang 18(2):121–147

    Google Scholar 

  • Tomasello M, Carpenter M, Call J, Behne T, Moll H (2005) Understanding and sharing intentions: the origins of cultural cognition. Behav Brain Sci 28:675–735

    PubMed  Google Scholar 

  • Topal J, Gacsi M, Miklosi A, Viranyi Z, Kubinyi E, Csanyi V (2005) Attachment to humans: a comparative study on hand-reared wolves and differently socialized dog puppies. Anim Behav 70:1367–1375

    Google Scholar 

  • Topal J, Edohegyi A, Manyik R, Miklosi A (2006) Mindreading in a dog: an adaptation of a primate “mental attribution” study. Int J Psychol Psychol Ther 6:365–380

    Google Scholar 

  • Topál J, Byrne RW, Miklósi A, Csányi V (2006) Reproducing human actions and action sequences: “Do as I Do!” in a dog. Anim Cogn 9(4):355–367

    PubMed  Google Scholar 

  • Trut L (1999) Early canid domestication: the farm-fox experiment. Am Sci 87:160–169

    Google Scholar 

  • Tsujimoto S, Sawaguchi T (2002) Working memory of action: a comparative study of ability to selecting response based on previous action in New World monkeys (Saimiri sciureus and Callithrix jacchus). Behav Process 58:149–155

    Google Scholar 

  • Udell MAR, Wynne CD (2008) A review of domestic dogs (Canis familiaris) human-like behaviors: or why behavior analysts should stop worrying and love their dogs. J Exp Anal Behav 89:247–261

    PubMed  Google Scholar 

  • Udell MAR, Dorey NR, Wynne CDL (2008a) Wolves outperform dogs in following human social cues. Anim Behav 76:1767–1773

    Google Scholar 

  • Udell MAR, Giglio RF, Wynne CD (2008b) Domestic dogs (Canis familiaris) use human gestures but not nonhuman tokens to find hidden food. J Comp Psychol 122:84–93

    PubMed  Google Scholar 

  • van Schaik CP (2004) Among orangutans: red apes and the rise of human culture. Harvard University Press (Belknap), Cambridge

    Google Scholar 

  • van Schaik CP, Burkart JM (2009a) Mind the gap: cooperative breeding and the evolution of our unique features. In: Kappeler PM, Silk J (eds) Mind the gap: tracing the origins of human universals (in press)

  • van Schaik CP, Burkart JM (2009b) Why culture makes smart: the cultural intelligence hypothesis. Ethology (in press)

  • van Schaik CP, Pradhan GR (2003) A model for tool-use traditions in primates: implications for the coevolution of culture and cognition. J Hum Evol 44:645–664

    PubMed  Google Scholar 

  • Vick SJ, Anderson JR (2000) Learning and limits of use of gaze by capuchin monkeys (Cebus apella) in an object-choice task. J Comp Psychol 114(2):200–207

    CAS  PubMed  Google Scholar 

  • Viranyi Z, Topal J, Gacsi M, Miklosi A, Csanyi V (2004) Dogs respond appropriately to cues of humans’ attentional focus. Behav Process 66:161–172

    Google Scholar 

  • Virányi Z, Gácsi M, Kubinyi E, Topál J, Belényi B, Ujfalussy D, Miklósi A (2008) Comprehension of human pointing gestures in young human-reared wolves (Canis lupus) and dogs (Canis familiaris). Anim Cogn 11:373–387

    PubMed  Google Scholar 

  • Visalberghi E (1994) Learning processes and feeding behavior in monkeys. In: Galef BG, Mainardi M, Valsecchi P (eds) Behavioural aspects of feeding: basic and applied research on mammals. Harwood Academic, Chur

    Google Scholar 

  • Visalberghi E, Addessi E (2000a) Response to changes in food palatability in tufted capuchin monkeys, Cebus apella. Anim Behav 59:231–238

    PubMed  Google Scholar 

  • Visalberghi E, Addessi E (2000b) Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys. Anim Behav 60:69–76

    PubMed  Google Scholar 

  • Visalberghi E, Addessi E (2003) Food for thought: social learning about food in capuchin monkeys. In: Fragaszy DM, Perry S (eds) Traditions in non-human animals: models and evidence. Cambridge University Press, Cambridge, pp 187–212

    Google Scholar 

  • Vitale A, Queyras A (1997) The response to novel foods in common marmosets (Callithrix jacchus): the effects of different social contexts. Ethology 103:395–403

    Article  Google Scholar 

  • Voelkl B, Huber L (2000) True imitation in marmosets. Anim Behav 60:195–202

    PubMed  Google Scholar 

  • Voelkl B, Huber L (2007) Imitation as faithful copying of a novel technique in marmoset monkeys. PLoS ONE 2(7):e611

    PubMed  Google Scholar 

  • Voelkl B, Schrauf C, Huber L (2006) Social contact influences the response of infant marmosets towards novel food. Anim Behav 72:365–372

    Google Scholar 

  • Vonk J, Brosnan SF, Silk JB, Henrich J, Richerdson AS, Lambeth SP, Schapiro SJ, Povinelli DJ (2008) Chimpanzees do not take advantage of very low cost opportunities to deliver food to unrelated group members. Anim Behav 75:1757–1770

    Google Scholar 

  • Ward C, Smuts B (2007) Quantity-based judgments in the domestic dog (Canis lupus familiaris). Anim Cogn 10:71–80

    Google Scholar 

  • Warneken F, Tomasello M (2006) Altruistic helping in human infants and young chimpanzees. Science 311:1301–1303

    CAS  PubMed  Google Scholar 

  • Warneken F, Hare B, Melis AP, Hanus D, Tomasello M (2007) Spontaneous altruism by chimpanzees and young children. Plos Biol 5(7):e184, 1–7

    Google Scholar 

  • Webb DM, Zhang J (2005) FoxP2 in song-learning birds and vocal-learning mammals. J Hered 96(3):212–216

    CAS  PubMed  Google Scholar 

  • Weiss DJ, Garibaldi BT, Hauser MD (2001) The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. J Comp Psychol 115(3):258–271

    CAS  PubMed  Google Scholar 

  • Werdenich D, Huber L (2002) Social factors determine cooperation in marmosets. Anim Behav 64:771–781

    Google Scholar 

  • Westergaard GC, Haynie MK, Lundquist AL, Suomi SJ (1999) Carrying, sharing, and hand preference in tufted capuchins (Cebus apella). Int J Primatol 20(1):153–162

    Google Scholar 

  • Whiten A, Byrne RW (1997) Macchiavellian intelligence. II: Extensions and evaluations. Cambridge University Press, New York

    Google Scholar 

  • Whiten A, Ham R (1992) On the nature and evolution of imitation in the animal kingdom: reappraisal of a century of research. Adv Stud Behav 21:239–283

    Google Scholar 

  • Whiten A, van Schaik CP (2007) The evolution of animal “cultures” and social intelligence. Philos Trans Roy Soc B 362(1480):603–620

    Google Scholar 

  • Whiten A, Horner V, Litchfield CA, Marshall-Pescini S (2004) How do apes ape? Learn Behav 32(1):36–52

    PubMed  Google Scholar 

  • Wilson EO (1975) Sociobiology. Harvard University Press, Cambridge

    Google Scholar 

  • Winter P, Handley P, Ploog D, Schott D (1973) Ontogeny of squirrel monkey calls under normal conditions and under acoustic isolation. Behaviour 47:230–239

    CAS  PubMed  Google Scholar 

  • Wynne DDL, Udell MAR, Lord KA (2008) Ontogeny’s impact on human–dog communication. Anim Behav 76:e1–e4

    Google Scholar 

  • Yamamoto ME (1993) From dependence to sexual maturity: the behavioural ontogeny of Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, ecology and behaviour. Oxford University Press, Oxford, pp 235–254

    Google Scholar 

  • Yamamoto ME, Lopes FdA (2004) Effect of removal from the family group on feeding behavior by captive Callithrix jacchus. Int J Primatol 25:489–500

    Google Scholar 

  • Zahed SR, Prudom SL, Snowdon CT, Ziegler TE (2007) Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus). Am J Primatol 70:84–92

    Google Scholar 

Download references

Acknowledgments

We thank Adrian Jaeggi, Marta Manser, Claudia Rudolf von Rohr, Carsten Schradin, Charles Snowdon, Andrea Strasser and two anonymous reviewers for their valuable comments. This study was supported by SNF grants 3100A0-111915 and SNF 105312-114107.

Author information

Authors and Affiliations

  1. Anthropological Institute, University of Zurich, Winterthurerstr. 190, 8057, Zurich, Switzerland

    Judith Maria Burkart & Carel P. van Schaik

Authors
  1. Judith Maria Burkart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carel P. van Schaik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Judith Maria Burkart.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burkart, J.M., van Schaik, C.P. Cognitive consequences of cooperative breeding in primates?. Anim Cogn 13, 1–19 (2010). https://doi.org/10.1007/s10071-009-0263-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-009-0263-7

Keywords

Search

Navigation