Cognition in Ring-Tailed Lemurs

Understanding the evolution of cognition has been widely regarded as a major challenge in evolutionary research. Primates stand out in this context because they have larger brains compared to equally sized other mammals [Isler and van Schaik, 2009]. These effects also increase disproportionately within the primate order from strepsirrhines to haplorhines to hominins and humans [Dunbar, 1992; Isler et al., 2008]. Given that larger brains are energetically more expensive [Aiello and Wheeler, 1995], the most puzzling questions in this context are how and why primates, and especially humans, have evolved such powerful and distinctive cognitive abilities requiring so much costly neural tissue [Herrmann et al., 2007; Navarrete et al., 2011].

Research on cognitive abilities of strepsirrhine primates is of particular interest because after their split from other primates about 60 million years ago [Yoder et al., 1996; Yoder and Yang, 2004; but for palaeontological records, see Seiffert et al., 2003], they retained many ancestral primate traits, making them the best living models of early primates and the link between primates and other mammals [Martin, 1990; Fichtel and Kappeler, 2010]. However, cognitive abilities of strepsirrhine primates remain understudied, and the existing studies revealed conflicting results.

Alison Jolly [1966a] established the importance of comparative studies of lemur social intelligence in the early days of primatology. She concluded that ‘Lemur and Propithecus are both socially intelligent and socially dependent. They are, however, hopelessly stupid towards unknown inanimate objects. In this branch of the primates, the basic qualities of primate society have evolved without the formal inventive intelligence of true monkeys' [Jolly, 1966a, pp. 165-166]. Accordingly, these older studies suggested that lemur cognitive abilities in the physical domain are inferior to those of haplorhines [Maslow and Harlow, 1932; Jolly, 1964; Ehrlich et al., 1976], but more recent studies indicated that their cognitive abilities often match those of haplorhines [reviewed in Fichtel and Kappeler, 2010].

Here, we review the cognititive abilities of ring-tailed lemurs (Lemur catta), which live in multi-male, multi-female groups with one of the largest group sizes among lemurs and which exhibit clear dominance hierarchies [Sauther et al., 1999; Jolly et al., 2006]. These aspects of their social system allow evaluation of the influence of social complexity on cognition by comparing cognitive abilities of ring-tailed lemurs with those of other lemur species organized into smaller groups. These same features make them comparable to many haplorhines [Jolly, 1966a, b; Kappeler, 2012], opening a window of opportunities for comparative cognition research. Because many previous studies have been hampered by very small sample sizes, we only consider studies that have tested at least 4 ring-tailed lemurs in our review of physical and social cognition below.

Dealing effectively with objects and their spatial, numerical and causal relationships is critically important for everyday survival when searching for food, shelter or avoiding predators. Spatial cognition enables animals to identify their position, to remember what is located where, and to travel efficiently between sites [Gallistel, 1989]. A comparative study of spatial memory in 4 lemur species (table 1) revealed that frugivorous lemurs have more robust spatial memory than folivorous species, with ring-tailed lemurs exhibiting intermediate spatial cognitive abilities [Rosati et al., 2014]. However, solitary wild grey mouse lemurs with an omnivorous diet also learned the spatial location of feeding sites rapidly [Lührs et al., 2009].

Regarding numerical understanding, ring-tailed lemurs are able to form abstract numerical ascending rules and can apply them to novel sets of numerosities [Merritt et al., 2011]. Furthermore, ring-tailed lemurs are as good as brown, mongoose and ruffed lemurs in understanding the outcome of simple arithmetic operations of up to 3 items (table 1) [Santos et al., 2005a]. As in other primates, ring-tailed and mongoose lemurs' ability to discriminate between quantities depends on the ratio between choices being at least 1:3 or larger to successfully select the larger quantity in a spontaneous food choice task (table 1) [Jones and Brannon, 2012]. In addition, the precision of their approximate number system is comparable to that of rhesus monkeys (Macaca mulatta)[Jones et al., 2014].

Ring-tailed lemurs are also able to organize sequences in memory and to retrieve ordered sequences. Indeed, their accuracy and response times were similar to those of haplorhine monkeys [Merritt et al., 2007]. Moreover, ring-tailed as well as black lemurs were able to deal efficiently with large numbers of discriminative problems in visual discrimination learning sets (table 1) [Cooper, 1974; Ohta et al., 1984].

Tool use has not been reported for any strepsirrhine primate, perhaps because they have limited dexterity [Torigoe, 1985] due to the lack of a precision grip [Holtkötter, 1997]. They may therefore be physically unable to perform certain tasks requiring a high level of manual precision. However, recent research suggests that they nevertheless have some understanding of tool properties and functionality. Ring-tailed lemurs are able to choose between a functional and a non-functional tool to retrieve an inaccessible reward as quickly as capuchins, tamarins and vervet monkeys [Santos et al., 2005b]. They are, just as black, brown and red-fronted lemurs, also able to acquire a novel behaviour pattern to solve simple puzzle box problems (table 1) [Kappeler, 1987; Fornasieri et al., 1990; Anderson et al., 1992; Kendal et al., 2010; Schnoell and Fichtel, 2012].

Finally, a basic problem-solving skill that is essential for an effective interaction with the environment is inhibitory control, which is the ability to control ones' behaviour and impulsive reactions that would disrupt, for example, the efficient completion of a task leading to a potential food reward [Vlamings et al., 2010]. Ring-tailed lemurs are able to successfully use inhibitory control to acquire a reward but did not outperform other lemurs (table 1) [MacLean et al., 2013, 2014]. Thus, their abilities in the physical cognitive domain are qualitatively similar to those of other lemurs, but also to those of many haplorhine primates [Fichtel and Kappeler, 2010].

In contrast to haplorhine primates, brain size of lemurs does not correlate with group size [MacLean et al., 2009]. However, performance in a social cognitive task did correlate with the species-typical group size, but not with brain size, suggesting the potential for cognitive evolution without concomitant changes in brain size [MacLean et al., 2013]. In particular, ring-tailed lemurs exhibit some similarities in social organization and social structure with haplorhines [Kappeler, 1999], suggesting convergent sociocognitive evolution [Sandel et al., 2011]. Below, we will summarize the current knowledge of ring-tailed lemurs' social cognition, focusing on the structure of social relationships (competition, postconflict behaviour, coalitions), gaze following, social learning and innovations, as well as communication.

Ring-tailed lemurs live in multi-male, multi-female groups with some of the largest group sizes among lemurs [Kappeler, 2012]. Males and females exhibit separate linear dominance hierarchies [Jolly, 1966b], but rank is not inherited maternally as in many Old World primates [Kappeler, 1993a]. Ring-tailed lemurs are able to use transitive interference, a form of deductive reasoning that might be a cognitive mechanism by which animals can learn the relationships within their group's dominance hierarchy [MacLean et al., 2008]. Ring-tailed lemurs mastered transitive interference better than pair-living mongoose lemurs, suggesting that social complexity is an important selective force for the evolution of cognitive abilities relevant to transitive reasoning [MacLean et al., 2008].

One mechanism of social behaviour that is exhibited by many haplorhine primates is reconciliation after aggression, and some studies suggest that ring-tailed lemurs do reconcile after conflicts [Rolland and Roeder, 2000; Palagi et al., 2005], whereas other studies found no evidence for it [Kappeler, 1993b]. Reconciliation has also been documented in black, brown and red-fronted lemurs as well as in sifakas (table 1) [Kappeler, 1993b; Roeder et al., 2002; Palagi et al., 2008]. Third-party affiliation after aggression seems to be absent in this species [Kappeler, 1993b]. The formation of coalitions appears to be limited to specific contexts in ring-tailed lemurs. Although male ring-tailed as well as red-fronted lemurs tend to form partnerships during migration, they do not actively support each other in within-group conflicts [Gould, 1997a; Ostner and Kappeler, 2004]. Female ring-tailed lemurs experience high levels of competition over reproduction, resulting even in eviction of potential competitors [Vick and Pereira, 1989]. In contrast to males, related females occasionally form within-group coalitions during eviction of other females [Jolly, 1998]. However, female coalitions have not been documented in red-fronted lemurs during eviction of other females [Kappeler and Fichtel, 2012].

Another benefit of group-living is to gather information about the environment, for instance about what to feed on, what to avoid, or about appropriate sex-specific behaviours, by observing conspecifics [Gould, 1997b; O'Mara and Hickey, 2012]. Ring-tailed lemurs as well as black and brown lemurs use gaze following to track the attention of conspecifics [Shepherd and Platt, 2008; Ruiz et al., 2009]. In contrast to black, mongoose and red ruffed lemurs, brown and ring-tailed lemurs are also able to follow human gaze [Botting et al., 2011; Sandel et al., 2011]. Ring-tailed lemurs, just as many Eulemur species, red ruffed lemurs and aye-ayes are able to learn socially [Kappeler, 1987; Fornasieri et al., 1990; Anderson et al., 1992; Kendal et al., 2010; Schnoell and Fichtel, 2012]. However, studies on social learning in the wild indicate that, in contrast to red-fronted lemurs [Schnoell and Fichtel, 2012], the spread of information appears to be limited to subgroups of individuals that tolerate each other in close proximity [Kendal et al., 2010]. Although ring-tailed lemurs are able to learn socially, there is only one report of a potential behavioural tradition, which describes the innovation and spread of a novel way of drinking in a captive population [Hosey et al., 1997]. Behavioural traditions in the wild have also been found in Verreaux's and Coquerel's sifakas and potentially in red-fronted lemurs [Fichtel and van Schaik, 2006; Fichtel and Kappeler, 2011; Schnoell and Fichtel, 2013]. Finally, ring-tailed lemurs are more skilled in using social cues in comparison to brown, black, mongoose, black-and-white ruffed lemurs and Coquerel's sifakas in a food competition task in which the experimental subject was supposed to avoid food that an experimenter was facing [Sandel et al., 2011; MacLean et al., 2013].

Thus, in the realm of social intelligence, ring-tailed lemurs appear to be more skilled than other lemurs in using social cues during food competition tasks. Within-group coalitions appear to be rare and limited to rare events of female evictions. However, in several other aspects of social cognition, such as reconciliation and social learning, ring-tailed lemurs' performance is equal to those of other lemurs.

In the realm of communication, non-human primates have a limited repertoire of signals, but they can provide listeners with an open-ended, highly modifiable and cognitively rich set of meanings [Cheney and Seyfarth, 2010]. Among lemurs, ring-tailed lemurs have the largest vocal repertoire, produce the largest number of facial expressions and have elaborated olfactory communication [Fichtel, unpubl. data]. They produce functionally referential alarm calls in response to both aerial and terrestrial predators [Pereira and Macedonia, 1991], whereas sifakas and red-fronted lemurs produce functionally referential alarm calls only in response to aerial predators [Fichtel and Kappeler, 2002; Fichtel and van Schaik, 2006; Fichtel and Kappeler, 2011]. Red-tailed sportive lemurs and grey mouse lemurs, however, produce general alarm calls instead of predator-specific ones [Fichtel, 2007; Rahlfs and Fichtel, 2010]. Ring-tailed lemurs also produce more visual signals than red-fronted or ruffed lemurs [Pereira et al., 1988; Pereira and Kappeler, 1997]. They also use various scent marks to signal individuality as well as dominance and reproductive status [Kappeler, 1990; Drea, 2007; Charpentier et al., 2008; Crawford et al., 2011]. Ring-tailed lemurs are also able to recognize kin or choose mating partners by means of olfactory signals [Charpentier et al., 2010; Crawford et al., 2011]. Even cross-modal recognition of individuals by means of olfactory and vocal signals has been demonstrated in ring-tailed lemurs [Kuhlaci et al., 2014]. Thus, ring-tailed lemurs appear to have more elaborate communicative skills than many other lemurs.

In summary, although only limited data are available, this review indicates that ring-tailed lemurs exhibit similar qualitative cognitive skills in the physical domain as other lemurs and many haplorhine primates [Fichtel and Kappeler, 2010]. In the social domain, ring-tailed lemurs are better skilled in using social cues in food competition tasks than other lemurs. Coalitions have only been observed in female ring-tailed lemurs during rare events of female evictions. However, in several other aspects of social behaviour, such as reconciliation and social learning, ring-tailed lemurs' cognitive abilities are equal to those of other lemurs with the caveat that the social behaviour and cognitive abilities of other lemurs have not yet been studied in comparable detail. Thus, additional systematic comparative studies in physical and social cognition are required for a more comprehensive understanding of the processes of primate cognitive evolution.

We are very grateful to Michelle Sauther for inviting us to contribute to this species issue. We also thank Peter Kappeler for many discussions about lemur behaviour and for comments on the present paper. This paper is dedicated to Alison Jolly for establishing the importance of comparative studies in primate cognition.