Socio-spatial cognition in vervet monkeys

Abstract Safety in numbers is thought to be the principal advantage of living in groups for many species. The group can only provide protection against predators, however, when group cohesion is maintained. Vocalisations are used to monitor inter-individual distances, especially under conditions of poor visibility, but should be avoided in the presence of predators. Mentally tracking the movements of silent and invisible group members would allow animals foraging in dense vegetation to stay close to their group members while reducing the use of vocal contact. We tested the socio-spatial cognitive abilities of wild vervet monkeys (Chlorocebus pygerythrus) by comparing their reactions to plausible and implausible displacements of group members simulated by sound playbacks. Our methods are comparable to those used in studies of ‘object permanence’ and ‘invisible displacements’ of inanimate objects. Our results show that vervets can track the whereabouts of invisibly and silently moving group members, at least over short periods of time.

[1]  Mary Poss,et al.  Social Organization and Parasite Risk in Mammals: Integrating Theory and Empirical Studies , 2003 .

[2]  N. Humphrey.  The Social Function of Intellect , 1976 .

[3]  Melinda A. Novak,et al.  Object permanence in rhesus monkeys (Macaca mulatta). , 1994 .

[4]  Peter M. Bennett,et al.  Evolutionary biology: Brain size, energetics, ecology and life history patterns , 1983, Nature.

[5]  Colin Campbell,et al.  Experimental set ups , 2008 .

[6]  T. Aubin,et al.  When to be a dear enemy: flexible acoustic relationships of neighbouring skylarks, Alauda arvensis , 2008, Animal Behaviour.

[7]  Andrew J. King,et al.  Where Next? Group Coordination and Collective Decision Making by Primates , 2011, International Journal of Primatology.

[8]  Sylvain Fiset,et al.  Duration of cats' (Felis catus) working memory for disappearing objects , 2005, Animal Cognition.

[9]  Robin I. M. Dunbar,et al.  Evolution of the Social Brain , 2003, Science.

[10]  E. Temeles.  The role of neighbours in territorial systems: when are they 'dear enemies'? , 1994, Animal Behaviour.

[11]  Drew Rendall,et al.  Social brains, simple minds: does social complexity really require cognitive complexity? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  C. Stanford.  Chimpanzee Hunting Behavior , 1995 .

[13]  Christopher N. Templeton,et al.  Good neighbour, bad neighbour: song sparrows retaliate against aggressive rivals , 2009, Animal Behaviour.

[14]  T. Sawaguchi.  The size of the neocortex in relation to ecology and social structure in monkeys and apes. , 1992, Folia primatologica; international journal of primatology.

[15]  P. Whitten,et al.  Why fight? Selective forces favoring between-group aggression in a variably pair-living primate, the white-faced saki (Pithecia pithecia) , 2012 .

[16]  O. Güntürkün,et al.  Development of object permanence in food-storing magpies (Pica pica). , 2000, Journal of comparative psychology.

[17]  R. Seyfarth,et al.  Social Awareness in Monkeys1 , 2000 .

[18]  JULIA FISCHER,et al.  Use of statistical programs for nonparametric tests of small samples often leads to incorrectPvalues: examples fromAnimal Behaviour , 1998, Animal Behaviour.

[19]  I. Pepperberg,et al.  Development of Piagetian Object Permanence in a Grey Parrot (Psittacus erithacus) , 1997 .

[20]  Howard Eichenbaum,et al.  Spatial memory performance of freely-moving squirrel monkeys , 2003, Behavioural Brain Research.

[21]  J. Gomez.  Species comparative studies and cognitive development , 2005, Trends in Cognitive Sciences.

[22]  V. Dasser,et al.  A social concept in Java monkeys , 1988, Animal Behaviour.

[23]  Carel P. van Schaik,et al.  The evolution of female social relationships in nonhuman primates , 1997, Behavioral Ecology and Sociobiology.

[24]  John G. Robinson.  Spatial structure in foraging groups of wedge-capped capuchin monkeys Cebus nigrivittatus , 1981, Animal Behaviour.

[25]  J. Dale,et al.  Individual recognition: it is good to be different. , 2007, Trends in ecology & evolution.

[26]  I. Tattersall,et al.  Handbook of paleoanthropology , 2007 .

[27]  Marc D. Hauser,et al.  A nonhuman primate's expectations about object motion and destination: The importance of self-propelled movement and animacy , 1998 .

[28]  R. Byrne,et al.  Why creative intelligence is hard to find , 1988, Behavioral and Brain Sciences.

[29]  N. Newton-Fisher.  14 Chimpanzee Hunting Behavior , 2007 .

[30]  R. Byrne,et al.  African elephants have expectations about the locations of out-of-sight family members , 2008, Biology Letters.

[31]  C. Menzel.  Cognitive aspects of foraging in Japanese monkeys , 1991, Animal Behaviour.

[32]  H. Meunier,et al.  Participation in group defence: proximate factors affecting male behaviour in wild white-faced capuchins , 2012, Animal Behaviour.

[33]  R. Seyfarth,et al.  Recognition of Individuals Within and Between Groups of Free-Ranging Vervet Monkeys1 , 1982 .

[34]  S. Shultz,et al.  Stepwise evolution of stable sociality in primates , 2011, Nature.

[35]  G. Knoblich,et al.  Action coordination in groups and individuals: learning anticipatory control. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[36]  S. Shettleworth.  Cognition, evolution, and behavior , 1998 .

[37]  Robert M. Seyfarth,et al.  Grooming, alliances and reciprocal altruism in vervet monkeys , 1984, Nature.

[38]  M. Novak,et al.  Object permanence in orangutans (Pongo pygmaeus) and squirrel monkeys (Saimiri sciureus). , 1998, Journal of comparative psychology.

[39]  R. Zenuto.  Dear enemy relationships in the subterranean rodent Ctenomys talarum: the role of memory of familiar odours , 2010, Animal Behaviour.

[40]  Robert M. Seyfarth,et al.  Hierarchical Classification by Rank and Kinship in Baboons , 2003, Science.

[41]  H. Sigg,et al.  Home range and daily march in a Hamadryas baboon troop. , 1981, Folia primatologica; international journal of primatology.

[42]  M. Itzkowitz,et al.  THE BENEFITS OF DEAR ENEMY RECOGNITION IN THREE-CONTENDER CONVICT CICHLID (CICHLASOMA NIGROFASCIATUM) CONTESTS , 1999 .

[43]  Jean Piaget,et al.  La psychologie de l'enfant , 1967 .

[44]  R. Seyfarth,et al.  Vocal recognition in free-ranging vervet monkeys , 1980, Animal Behaviour.

[45]  C. Dumas,et al.  Object permanence in cats (Felis catus): an ecological approach to the study of invisible displacements. , 1992, Journal of comparative psychology.

[46]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[47]  J. Beehner,et al.  Factors affecting individual participation in group-level aggression among non-human primates , 2007 .

[48]  C. Schaik.  Why Are Diurnal Primates Living in Groups , 1983 .

[49]  D A Washburn,et al.  Comparative assessment of psychomotor performance: target prediction by humans and macaques (Macaca mulatta). , 1992, Journal of experimental psychology. General.

[50]  J. Altmann,et al.  Observational study of behavior: sampling methods. , 1974, Behaviour.

[51]  Josep Call,et al.  Tracking the displacement of objects: a series of tasks with great apes (Pan troglodytes, Pan paniscus, Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapiens). , 2006, Journal of experimental psychology. Animal behavior processes.

[52]  R. Brooks,et al.  Individual recognition by song in white-throated sparrows. II. Effects of location , 1975 .

[53]  D. Washburn,et al.  Can monkeys (Macaca mulatta) represent invisible displacement? , 1996, Journal of comparative psychology.

[54]  Great apes track hidden objects after changes in the objects' position and in subject's orientation , 2010, American journal of primatology.

[55]  Paul H. Harvey,et al.  Primates, brains and ecology , 2009 .

[56]  E. Font,et al.  Beyond ‘nasty neighbours’ and ‘dear enemies’? Individual recognition by scent marks in a lizard (Podarcis hispanica) , 2008, Animal Behaviour.

[57]  K. Zuberbühler,et al.  Vocal greeting behaviour in wild chimpanzee females , 2010, Animal Behaviour.

[58]  Audrey E. Cramer,et al.  Vervet monkeys as travelling salesmen , 1997, Nature.

[59]  I. Pepperberg,et al.  Development of Piagetian object permanence in a grey parrot (Psittacus erithacus). , 1997, Journal of comparative psychology.

[60]  C. Schaik,et al.  On the Ultimate Causes of Primate Social Systems , 1983 .

[61]  Robin I. M. Dunbar.  Neocortex size as a constraint on group size in primates , 1992 .

[62]  R. Hinde,et al.  Growing Points in Ethology , 1976 .

[63]  Robert M. Seyfarth,et al.  How vervet monkeys perceive their grunts: Field playback experiments , 1982, Animal Behaviour.

[64]  Robin I. M. Dunbar,et al.  The evolution of the social brain: anthropoid primates contrast with other vertebrates , 2007, Proceedings of the Royal Society B: Biological Sciences.

[65]  Sylvain Fiset,et al.  Invisible displacement understanding in domestic dogs (Canis familiaris): the role of visual cues in search behavior , 2007, Animal Cognition.

[66]  C. Nunn,et al.  Emerging infectious diseases and animal social systems , 2008, Evolutionary Ecology.

[67]  K. Zuberbühler,et al.  Leopard predation and primate evolution. , 2002, Journal of human evolution.

[68]  J. Bruce Falls,et al.  Individual recognition by song in white-throated sparrows. I. Discrimination of songs of neighbors and strangers , 1975 .

[69]  Robin I. M. Dunbar.  Social Brain Hypothesis , 1998, Encyclopedia of Evolutionary Psychological Science.

[70]  R. Seyfarth,et al.  How Monkeys See the World , 1990 .

[71]  F. Range,et al.  Can simple rules account for the pattern of triadic interactions in juvenile and adult female sooty mangabeys? , 2005, Animal Behaviour.

[72]  C. Janson.  Social correlates of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella , 1990, Animal Behaviour.

[73]  Robin I. M. Dunbar,et al.  Psychology. Evolution of the social brain. , 2003, Science.

[74]  Thomas Suddendorf,et al.  Do dogs (Canis familiaris) understand invisible displacement? , 2004, Journal of comparative psychology.

[75]  H. de Vries,et al.  Male monkeys remember which group members have given alarm calls , 2006, Proceedings of the Royal Society B: Biological Sciences.

[76]  J. Bruce Falls,et al.  Individual recognition by song in white-throated sparrows. III. Song features used in individual recognition , 1975 .

[77]  P. Wright,et al.  Object permanence in lemurs , 2009, Animal Cognition.

[78]  A floristic description and utilisation of two home ranges by vervet monkeys in Loskop Dam Nature Reserve, South Africa , 2010 .

[79]  J. Neiworth,et al.  A test of object permanence in a new-world monkey species, cotton top tamarins (Saguinus oedipus) , 2003, Animal Cognition.

[80]  P. Garber,et al.  Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis , 1989, American journal of primatology.

[81]  J. Piaget.  La construction du réel chez l'enfant , 1973 .

[82]  Josep Call,et al.  Representing space and objects in monkeys and apes , 2000, Cogn. Sci..

[83]  Sylvain Gagnon,et al.  Search behavior of dogs (Canis familiaris) in invisible displacement problems , 1993 .

[84]  Vincent P Ferrera,et al.  Internally Generated Error Signals in Monkey Frontal Eye Field during an Inferred Motion Task , 2010, The Journal of Neuroscience.

[85]  O. Güntürkün,et al.  Development of object permanence in food-storing magpies (Pica pica) , 2000 .

[86]  Thomas Suddendorf,et al.  Do chimpanzees (Pan troglodytes) understand single invisible displacement? , 2005, Animal Cognition.

[87]  R. Seyfarth,et al.  The influence of intergroup competition on the survival and reproduction of female vervet monkeys , 1987, Behavioral Ecology and Sociobiology.

[88]  Marie Trone,et al.  What do dolphins (Tursiops truncatus) understand about hidden objects? , 2009, Animal Cognition.

[89]  E. Menzel.  Chimpanzee Spatial Memory Organization , 1973, Science.

[90]  Ludwig Huber,et al.  Object permanence in common marmosets (Callithrix jacchus). , 2004, Journal of comparative psychology.

[91]  C. Boesch,et al.  Mental map in wild chimpanzees: An analysis of hammer transports for nut cracking , 1984, Primates.

[92]  Julian Huxley,et al.  Evolution as a Process , 1958 .

[93]  Bernd Heinrich,et al.  The ontogeny of caching in ravens, Corvus corax , 2007, Animal Behaviour.

[94]  Francesco Antinucci,et al.  Stage 6 object concept in nonhuman primate cognition: A comparison between gorilla (Gorilla gorilla gorilla) and Japanese macaque (Macaca fuscata). , 1986 .

[95]  R. Seyfarth,et al.  Social Awareness in Monkeys , 2000 .

[96]  D. Rendall,et al.  The meaning and function of grunt variants in baboons , 1999, Animal Behaviour.