Monkeys and Prosimians: Social Learning D. M. Fragaszy and J. Crast, University of Georgia, Athens, GA, USA ã 2010 Elsevier Ltd. All rights reserved. Introduction Tarsiiformes (tarsiers of Southeast Asia). All prosimians live in tropical habitats in Africa and Asia and the vast In this chapter, we highlight examples of social influ- majority are arboreal and nocturnal. Prosimians are some- ences on learning observed in prosimians and monkeys times referred to as ‘living fossils’ because they appear to and consider the role of socially mediated learning in have some physical similarities to ancestral primates of the biology of these animals. Learning is always the approximately 50 Mya. In general, prosimians rely to a outcome of interacting physical, social, and individual greater extent than other primates on olfaction. Some are factors and takes place over time. Thus, we cannot parse solitary foragers; others travel and forage in groups ranging learning, either as a process or as an outcome, into from small family units to larger social groups of as many as portions that are socially influenced and portions that 27 individuals. Weknow less about the lifestyles and behav- are not. Instead, we can document how social processes ior of prosimians than of monkeys. affect behavior relevant to the learning process, and In comparison with prosimians, species in the suborder we can seek evidence for social contributions to learning Anthropoidea are characterized by a relatively larger outcomes. brain for their body mass, diurnal lifestyle, and a greater To begin, we provide some background on the taxo- reliance on vision than on olfaction. Anthropoid species nomic groups of interest in this chapter: monkeys and generally exhibit greater manual dexterity than prosi- prosimians. Primates are a remarkably diverse order. Body mians, and anthropoids are more likely to live in groups. size alone spans three orders of magnitude, from tiny pro- New World monkeys (infraorder Platyrrhini) are arboreal simians weighing a few hundred grams to massive apes and relatively small-bodied, ranging in size from approxi- weighing more than 100 kg. Diet, morphology, mating mately 100 g (the pygmy marmoset [Cebuella pygmaea]) up systems, locomotor style, life history, and every other to 10 kg (the muriqui [Brachyteles arachnoides] and spider aspect of the biology of these animals is as diverse as body monkey [Genus Ateles]). Many genera live in small family size, and this diversity is important when considering groups; others live in medium-to-large social groups the contributions of the social context to learning in par- (as many as 50–60 individuals). Within the New World ticular species. monkeys are the subfamilies Callitrichinae (marmosets and tamarins), Atelinae (muriquis, woolly, howler, and spider monkeys), Pitheciinae (titis, sakis, bearded sakis, Phylogeny of Prosimians and Monkeys and uakaris), Cebinae (squirrel monkeys and capuchins), and Aotinae (owl monkeys, the only nocturnal anthro- As Fleagle (1999) discusses in greater detail, the order poid). During the platyrrhine radiation in the Americas, Primates includes two suborders: Prosimii, prosimians, and the genera adapted to distinct niches, making a living in Anthropoidea, monkeys, apes, and humans (see Figure 1). different parts of the forest canopy and resulting in great The two suborders have evolved separately for at least diversity in social organization, reproductive strategy, 55 Million years. Two infraorders are classified within diet, and locomotor style. Anthropoidea: the platyrrhines (New World monkeys) Compared to New World monkeys, Old World monkeys and catarrhines (Old World monkeys, apes, and humans). (superfamily Cercopithecoidea) are mostly larger-bodied, New and Old World monkeys diverged approximately ranging from around 1 kg to approximately 30 kg, and some 40 Millions of years ago (Mya), and apes and hominids are terrestrial. Old World monkeys include subfamilies (hominids include modern humans and their ancestors; Cercopithecinae (baboons, mandrills, drills, macaques, superfamily Hominoidea) diverged from the Old World mangabeys, and guenons) and Colobinae (colobus monkeys monkeys (superfamily Cercopithecoidea) approximately and langurs), which differ particularly in their dietary adap- 20 Mya. Given their lengthy independent evolution, vari- tations (see Fleagle for details). Most cercopithecoid species ation in the life histories, body sizes, social organizations, live in large polygamous social groups with clear dominance etc., within each suborder, infraorder, and superfamily in hierarchies within and between matrilines (female kin the order Primates is to be expected. groups), and some form multilevel societies during parts The suborder Prosimii includes the infraorders Lemur- of the year. Of all primate superfamilies, cercopithecoids iformes (the lemurs of Madagascar), Lorisiformes (the have the widest geographic range, greatest number of spe- lorises of Africa and Asia and the galagos of Africa), and cies, and form some of the largest groups and biomass 468 Monkeys and Prosimians: Social Learning 469 Order Primates Suborder Prosimii* Anthropoidea (all prosimians: lemurs, (monkeys, apes, lorises, galagos, and tarsiers) and humans) Infraorder Lemuriformes Lorisiformes Tarsiiformes* Platyrrhini Catarrhini (all lemurs) (all lorises (the tarsiers) (all new world (all old world monkeys, and galagos) monkeys) apes, and humans) Superfamily Ceboidea Cercopithecoidea Hominoidea (all new world (all old world (apes and humans) monkeys) monkeys) + Family Callitrichidae Atelidae Cebidae Cercopithecidae Hylobatidae Pongidae Hominidae (marmosets and (howlers, spider (squirrel (all old world (gibbons and (the great apes) (humans) tamarins) monkeys, and monkeys, capuchins, monkeys) siamangs) muriquis) owl monkeys, etc.) Subfamily Cercopithecinae Colobinae (baboons, macaques, (colobus species, guenons, etc.) langurs) Genus Pongo Gorilla Pan Homo All primates All monkeys All anthropoids All apes All hominoids All hominids (including extinct Pygmaeus Gorilla Troglodytes Sapiens All prosimians forms and modern humans) (orangutans) (3 subspecies) (chimpanzees) Species (2 subspecies) (3 subspecies) paniscus (bonobos) *There is some disagreement among primatologists concerning where to place tarsiers. Many researchers +Fleagle (1999) and others have recently eliminated the family callitrichidae and included marmosets suggest that they more properly belong closer to the anthropoids and thus revise the primate classifications and tamarins in the family cebidae. to reflect this view. Here, for simplicity, we continue to use the traditional classifications. Figure 1 Primate taxonomic classification. This abbreviated taxonomy illustrates how primates are grouped into increasingly specific categories. Only the more general categories are shown, except for the great apes and humans. Reproduced from Turnbaugh WA, Nelson H, Jurmain R, and Kilgore L (2002) Understanding Physical Anthropology and Archaeology, 8th edn., with permission from Wadsworth. densities in the primate order. Despite this, Old World social partners in a way different from that of species that monkeys have less diversity in diet and social organization are highly reliant on vision. Third, motor patterns and than New World monkeys. action proclivities vary considerably across species. For example, leaf-eating monkeys are generally less likely to Phylogeny and Socially Mediated manipulate objects spontaneously than species that feed on Learning seeds and nuts. Finally, the variability in behavioral ecology across species means that individuals of different species are interested in different kinds of activities, locations, This brief review of primate phylogeny suggests some objects, and events. For example, leaf-eating monkeys reasons why we might expect socially mediated learning may be less likely to attend to sequences of actions during to vary across primate taxa. First, group demographics and feeding than are seed- or nut-eating species; omnivorous social dynamics within groups define the social context, species are less likely to attend to the odor of leaves eaten and thus influence socially mediated learning within a by another than are dietary specialists. Behavioral priorities group. The number of groupmates, their age and sex, and and proclivities of each species constrain what an individ- the nature of social relationships within the group vary ual is likely to learn in the first place, and thus the role of enormously across species, and may vary considerably social context in learning. within species as well. Groups of monkeys of the same species may live in smallish groups (4–7 individuals) or quite large groups (more than 40 individuals) depending on the local distribution of resources. Second, reliance on The Sources of Social Context various sensory modalities (vision, olfaction, audition, and Social Organization touch) in social interaction and in general activity varies across taxa. For example, species that are particularly atten- The social organization (i.e., the size, demographic com- tive to smell (such as many prosimians) will be affected by position, and spatiotemporal coordination of individuals 470 Monkeys and Prosimians: Social Learning within a group) and social relationships among individuals juveniles; adult males most slowly or not at all. If social in a group provide the boundaries of the social context in influences contributed to the spread of the behavior, it did which an individual