The Evolution of Cognitive Control in Lemurs.

Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel's sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species' natural history to understand the origins of complex cognition.

Genetic variation at MHC class II loci influences both olfactory signals and scent discrimination in ring-tailed lemurs.

BACKGROUND: Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual's quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual's body odors may signal its MHC composition and influence partner identification or mate choice. Here, we investigated MHC-based signaling and recipient sensitivity by testing for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity in a strepsirrhine primate, the ring-tailed lemur (Lemur catta). METHODS: First, we coupled genotyping of the MHC class II gene, DRB, with gas chromatography-mass spectrometry of genital gland secretions to investigate if functional genetic diversity is signaled by the chemical diversity of lemur scent secretions. We also assessed if the chemical similarity between individuals correlated with their MHC-DRB similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics. RESULTS: We found that both sexes signaled overall MHC-DRB diversity and pairwise MHC-DRB similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, the sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, suggesting that lemur genital odors function to advertise genetic quality. CONCLUSIONS: In summary, genital odors of ring-tailed lemurs provide honest information about an individual's absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, we suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage.

Sleep influences cognitive performance in lemurs.

Primates spend almost half their lives asleep, yet little is known about how sleep influences their waking cognition. We hypothesized that diurnal and cathemeral lemurs differ in their need for consistent, non-segmented sleep for next-day cognitive function-including long-term memory consolidation, self-control, foraging efficiency, and sociality. Specifically, we expected that strictly diurnal Propithecus is more reliant on uninterrupted sleep for cognitive performance, as compared to four other lemur species that are more flexibly active (i.e., cathemeral). We experimentally inhibited sleep and tested next-day performance in 30 individuals of 5 lemur species over 960 total nights at the Duke Lemur Center in Durham, North Carolina. Each set of pair-housed lemurs experienced a sleep restriction and/or deprivation protocol and was subsequently tested in a variety of fitness-relevant cognitive tasks. Within-subject comparisons of performance on these tasks were made by switching the pair from the experimental sleep inhibited condition to a normal sleep environment, thus ensuring cognitive equivalency among individuals. We validated effectiveness of the protocol via actigraphy and infrared videography. Our results suggest that 'normal' non-disrupted sleep improved memory consolidation for all lemurs. Additionally, on nights of normal sleep, diurnal lemurs performed better in foraging efficiency tasks than cathemeral lemurs. Social behaviors changed in species-specific ways after exposure to experimental conditions, and self-control was not significantly linked with sleep condition. Based on these findings, the links between sleep, learning, and memory consolidation appear to be evolutionarily conserved in primates.

Navigation strategies in three nocturnal lemur species: diet predicts heuristic use and degree of exploratory behavior.

Humans generally solve multi-destination routes with simple rules-of-thumb. Animals may do the same, but strong evidence is limited to a few species. We examined whether strepsirrhines, who diverged from haplorhines more than 58 mya, would demonstrate the use of three heuristics used by humans and supported in vervets, the nearest neighbor rule, the convex hull, and a cluster strategy, when solving a multi-destination route. We hypothesized that the evolution of these strategies may depend on a species' dietary specialization. Three nocturnal lemur species were tested on an experimental array at the Duke Lemur Center. Frugivorous fat-tailed dwarf lemurs (Cheirogaleus medius) were expected to follow paths most consistent with distance-saving navigational heuristics because fruit trees are stationary targets. Gray mouse lemurs (Microcebus murinus) and aye-ayes (Daubentonia madagascariensis), which rely on more mobile and ephemeral foods, were expected to use fewer paths consistent with these heuristics and be more exploratory. Our data supported all of these hypotheses. Dwarf lemurs used paths consistent with all three heuristics, took the shortest paths, and were the least exploratory. Mouse lemurs were quite exploratory but sometimes used paths consistent with heuristics. Aye-ayes showed no evidence of heuristic use and were the most exploratory. Distinguishable patterns of inter- and intra-individual variation in ability to solve the route, speed, and behavior occurred in each species. This research suggests that these simple navigational heuristics are not part of a readily available set of cognitive tools inherited by all primates but instead evolve due to need in each lineage.

Profiling caregivers: Hormonal variation underlying allomaternal care in wild red-bellied lemurs, Eulemur rubriventer.

Neuroendocrine evidence suggests that paternal care is mediated by hormonal mechanisms, where hormonal changes in expectant and new fathers facilitate infant care. In species with obligate and extensive paternal care such as humans, androgen levels decline once males are paired and have offspring, and in direct response to offspring care. Facultative infant care is widespread in the Order Primates, but the underlying hormonal mechanisms are largely unknown. We found that wild, red-bellied lemurs living in family groups (two adults and their presumed offspring) varied in the amount of care they provided infants. The more fathers invested in helping infants (measured as a composite of carrying, holding, huddling, grooming, and playing), and specifically the more they huddled and groomed with infants, the higher their fecal androgen (fA) levels, contrary to expectations. Carrying was negatively related to fA levels. Helping by subadults and juveniles was not related to their own fA levels. Elevated fA levels during infant dependence have been observed in other vertebrate species, and are thought to reflect reinvestment in mating rather than investment in dependent offspring. However, red-bellied lemurs do not mate until after infants are weaned, and they have long-term pair-bonds, suggesting that elevated fA levels play a role in offspring care. These results support a growing body of research suggesting that elevated androgen levels do not inhibit protective infant care.

Knowledgeable Lemurs Become More Central in Social Networks.

Strong relationships exist between social connections and information transmission [1-9], where individuals' network position plays a key role in whether or not they acquire novel information [2, 3, 5, 6]. The relationships between social connections and information acquisition may be bidirectional if learning novel information, in addition to being influenced by it, influences network position. Individuals who acquire information quickly and use it frequently may receive more affiliative behaviors [10, 11] and may thus have a central network position. However, the potential influence of learning on network centrality has not been theoretically or empirically addressed. To bridge this epistemic gap, we investigated whether ring-tailed lemurs' (Lemur catta) centrality in affiliation networks changed after they learned how to solve a novel foraging task. Lemurs who had frequently initiated interactions and approached conspecifics before the learning experiment were more likely to observe and learn the task solution. Comparing social networks before and after the learning experiment revealed that the frequently observed lemurs received more affiliative behaviors than they did before-they became more central after the experiment. This change persisted even after the task was removed and was not caused by the observed lemurs initiating more affiliative behaviors. Consequently, quantifying received and initiated interactions separately provides unique insights into the relationships between learning and centrality. While the factors that influence network position are not fully understood, our results suggest that individual differences in learning and becoming successful can play a major role in social centrality, especially when learning from others is advantageous.

The influence of visitor interaction on the behavior of captive crowned lemurs (Eulemur coronatus) and implications for welfare.

Research suggests that zoo visitors can have positive, negative, and neutral impacts on captive primate welfare; however, research investigating the implications of visitor-animal feeding experiences is extremely limited. In the UK, a large proportion of BIAZA zoos that house lemur species offer visitor interaction experiences (16 out of 33). This study investigated the impact on the behavior of a family group of crowned lemurs (Eulemur coronatus) housed at Newquay Zoo, UK of visitors, accompanied by a keeper, entering the enclosure to feed the lemurs. Behavior was observed under four conditions: (i) during visitor feed; (ii) 30 min post-visitor feed; (iii) during a keeper feed; and (iv) 30 min post-keeper feed. Keeper feeds were conducted by keepers only, on the day after visitor feeds. The lemur group spent significantly less time performing aggressive behavior and was also significantly more interactive with keepers during visitor feeds compared with keeper-only feeds. There was no significant difference in behaviors performed immediately after interacting with visitors. Over the study period, there was a tendency for interactions with visitors to increase, and for interactions with keepers during visitor feeds to decrease. After a 28-day interval without visitor interaction, the lemurs' interaction with visitors had returned to the level recorded at the start of the study. In conclusion, visitor interaction did not compromise the welfare of the study subjects in either the short- or long-term, while an increase in visitor interactions over time has interesting implications for the enrichment properties of, or habituation to, unfamiliar humans. Zoo Biol. 35:222-227, 2016. © 2016 Wiley Periodicals, Inc.

Captive Conditions of Pet Lemurs in Madagascar.

Live extraction of wildlife is a threat to biodiversity and can compromise animal welfare standards. Studies of the captive environments and welfare of pet primates are known, but none has focused on Madagascar. We aimed to expand knowledge about the captive conditions of pet lemurs in Madagascar. We hypothesized that captive lemurs would often be kept in restrictive settings, including small cages, would be fed foods inconsistent with their natural diets and, as a result, would be in bad physical or psychological health. Data were collected via a web-based survey (n = 253 reports) and from the websites and social media pages of 25 hotels. Most lemurs seen by respondents were either kept on a rope/leash/chain or in a cage (67%), though some lemurs were habituated and were not restrained (28%). Most of the time (72%) cages were considered small, and lemurs were rarely kept in captivity together with other lemurs (81% of lemurs were caged alone). Pet lemurs were often fed foods inconsistent with their natural diets, and most (53%) were described as being in bad health. These findings point to a need to undertake outreach to pet lemur owners in Madagascar about the captivity requirements of primates.

Is wounding aggression in zoo-housed chimpanzees and ring-tailed lemurs related to zoo visitor numbers?

Chimpanzees in laboratory colonies experience more wounds on weekdays than on weekends, which has been attributed to the increased number of people present during the week; thus, the presence of more people was interpreted as stressful. If this were also true for primates in zoos, where high human presence is a regular feature, this would clearly be of concern. Here we examine wounding rates in two primate species (chimpanzees Pan troglodytes and ring-tailed lemurs Lemur catta) at three different zoos, to determine whether they correlate with mean number of visitors to the zoo. Wounding data were obtained from a zoo electronic record keeping system (ZIMS™). The pattern of wounds did not correlate with mean gate numbers for those days for either species in any group. We conclude that there is no evidence that high visitor numbers result in increased woundings in these two species when housed in zoos. Zoo Biol. 35:205-209, 2016. © 2016 Wiley Periodicals, Inc.

Implicit sequence learning in ring-tailed lemurs (Lemur catta).

Implicit learning involves picking up information from the environment without explicit instruction or conscious awareness of the learning process. In nonhuman animals, conscious awareness is impossible to assess, so we define implicit learning as occurring when animals acquire information beyond what is required for successful task performance. While implicit learning has been documented in some nonhuman species, it has not been explored in prosimian primates. Here we ask whether ring-tailed lemurs (Lemur catta) learn sequential information implicitly. We tested lemurs in a modified version of the serial reaction time task on a touch screen computer. Lemurs were required to respond to any picture within a 2 × 2 grid of pictures immediately after its surrounding border flickered. Over 20 training sessions, both the locations and the identities of the images remained constant and response times gradually decreased. Subsequently, the locations and/or the identities of the images were disrupted. Response times indicated that the lemurs had learned the physical location sequence required in original training but did not learn the identity of the images. Our results reveal that ring-tailed lemurs can implicitly learn spatial sequences, and raise questions about which scenarios and evolutionary pressures give rise to perceptual versus motor-implicit sequence learning.

Assessing the impacts of nonrandom seed dispersal by multiple frugivore partners on plant recruitment.

Directed dispersal is defined as enhanced dispersal of seeds into suitable microhabitats, resulting in higher recruitment than if seeds were dispersed randomly. While this constitutes one of the main explanations for the adaptive value of frugivore-mediated seed dispersal, the generality of this advantage has received little study, particularly when multiple dispersers are involved. We used probability recruitment models of a long-lived rainforest tree in Madagascar to compare recruitment success under dispersal by multiple frugivores, no dispersal, and random dispersal. Models were parameterized using a three-year recruitment experiment and observational data of dispersal events by three frugivorous lemur species that commonly disperse its seeds. Frugivore-mediated seed dispersal was nonrandom with respect to canopy cover and increased modeled per-seed sapling recruitment fourfold compared to no dispersal. Seeds dispersed by one frugivore, Eulemur rubriventer, had higher modeled recruitment probability than seeds dispersed randomly. However, as a group, our models suggest that seeds dispersed by lemurs would have lower recruitment than if dispersal were random. Results demonstrate the importance of evaluating the contribution of multiple frugivores to plant recruitment for understanding plant population dynamics and the ecological and evolutionary significance of seed dispersal.

Ring-tailed lemurs: a species re-imagined.

For over 50 years, ring-tailed lemurs have been studied continuously in the wild. As one of the most long-studied primate species, the length and breadth of their study is comparable to research on Japanese macaques, baboons and chimpanzees. They are also one of the most broadly observed of all primates, with comprehensive research conducted on their behaviour, biology, ecology, genetics, palaeobiology and life history. However, over the last decade, a new generation of lemur scholars, working in conjunction with researchers who have spent decades studying this species, have greatly enhanced our knowledge of ring-tailed lemurs. In addition, research on this species has expanded beyond traditional gallery forest habitats to now include high altitude, spiny thicket, rocky outcrop and anthropogenically disturbed coastal forest populations. The focus of this special volume is to 're-imagine' the 'flagship species of Madagascar', bringing together three generations of lemur scholars.

Genetic Evidence for Male and Female Dispersal in Wild Lemur catta.

Lemur catta has traditionally been considered a species with male-biased dispersal; however, occasional female dispersal occurs. Using molecular data, we evaluated dispersal patterns in 2 L. catta populations in southwestern Madagascar: Tsimanampesotse National Park (TNP) and Bezà Mahafaly Special Reserve (BMSR). We also investigated the genetic differentiation between the populations and dispersal partner relatedness. Results showed minor genetic differentiation between the populations (Ï´(ST) = 0.039), which may indicate gene flow historically occurring in this region, made possible by the presence of L. catta groups between the sites. Different patterns of sex-biased dispersal were found between the sites using corrected assignment indices: male-biased dispersal in TNP, and a lack of sex-biased dispersal in BMSR. Observational evidence of female dispersal in BMSR supports these results and may imply intense female resource competition in and around BMSR, because small groups of 2-3 females have been observed dispersing within BMSR and entering the reserve from outside. These dispersing groups largely consisted of mothers transferring with daughters, although we have an aunt-niece pair transferring together. Genetic data suggest that males also transfer with relatives. Our data demonstrate that dispersal partners consist of same-sexed kin for L. catta males and females, highlighting the importance of kin selection.

Cognition in ring-tailed lemurs.

In order to better understand the evolution of cognitive abilities in primates, information on cognitive traits of the most basal living primates can provide important comparative baseline data. Compared to haplorhine primates, lemurs have relatively smaller brains and reduced abilities to solve problems in the technical and social domain. However, recent studies have suggested that some cognitive abilities of lemurs are qualitatively equal to those of haplorhines. Here, we review studies investigating cognitive abilities in the technical and social domain of ring-tailed lemur cognition. In the physical domain, ring-tailed lemurs exhibit similar qualitative cognitive skills as other lemurs but also haplorhine primates. In the social domain, ring-tailed lemurs appear to be more skilled in visual perspective taking than other lemurs. Compared to other lemurs, they also have highly elaborated communicative skills. Moreover, within-group coalitions have been observed in female ring-tailed lemurs during rare events of female evictions but not in other lemur species. However, in several other aspects of social cognition, such as reconciliation and social learning, ring-tailed lemurs' cognitive abilities are equal to those of other lemurs. Thus, additional systematic comparative studies in physical and social cognition are required for a more comprehensive understanding of the processes of cognitive evolution among primates.

Ecological risk aversion and juvenile ring-tailed lemur feeding and foraging.

The extended primate juvenile period has been linked to interactions between feeding ecology and sociality. However, accumulating field data on juvenile primates suggest variation in the linkages between foraging efficiency, group foraging and social behaviour. In many non-human primates, juvenile ability (strength, coordination and motor skills) does not limit foraging success. If predicted limitations in feeding are not found in juvenile monkeys, it is possible that the gregarious strepsirrhines may show foraging patterns similar to those implicated in the evolution of a life history where long juvenile periods are advantageous. To test these behavioural predictions, I present a mixed longitudinal sample of observations on feeding and foraging behaviour from ring-tailed lemurs (Lemur catta) at the Bezà Mahafaly Special Reserve, Madagascar. Like several platyrrhine species, close proximity during foraging, low feeding efficiency and low dietary diversity are not typical of ring-tailed lemurs. The lack of ecological trade-offs in these species may indicate stronger common roles of sociality and social complexity in structuring the elongation of the primate juvenile period.

Innovation and behavioral flexibility in wild redfronted lemurs (Eulemur rufifrons).

Innovations and problem-solving abilities can provide animals with important ecological advantages as they allow individuals to deal with novel social and ecological challenges. Innovation is a solution to a novel problem or a novel solution to an old problem, with the latter being especially difficult. Finding a new solution to an old problem requires individuals to inhibit previously applied solutions to invent new strategies and to behave flexibly. We examined the role of experience on cognitive flexibility to innovate and to find new problem-solving solutions with an artificial feeding task in wild redfronted lemurs (Eulemur rufifrons). Four groups of lemurs were tested with feeding boxes, each offering three different techniques to extract food, with only one technique being available at a time. After the subjects learned a technique, this solution was no longer successful and subjects had to invent a new technique. For the first transition between task 1 and 2, subjects had to rely on their experience of the previous technique to solve task 2. For the second transition, subjects had to inhibit the previously learned technique to learn the new task 3. Tasks 1 and 2 were solved by most subjects, whereas task 3 was solved by only a few subjects. In this task, besides behavioral flexibility, especially persistence, i.e., constant trying, was important for individual success during innovation. Thus, wild strepsirrhine primates are able to innovate flexibly, suggesting a general ecological relevance of behavioral flexibility and persistence during innovation and problem solving across all primates.

Lemur behaviour informs the evolution of social monogamy.

Recent comparative analyses reached contradictory conclusions about the evolutionary origins of social monogamy in primates and other mammals, but they ignored variation in social bond quality between pair-partners. Recent field studies of Malagasy primates (lemurs) with variable intersexual bonds indicate independent evolutionary transitions to pair-living from solitary and group-living ancestors, respectively, as well as four cumulative steps in evolutionary transitions from a solitary life style to pair-living that resolve some contradictory results of previous studies.

Relaxed open mouth as a playful signal in wild ring-tailed lemurs.

Play signals are commonly used by animals to communicate their playful motivation and to limit the risk that rough acts are misunderstood by playmates. The relaxed open mouth is the most common facial expression performed during play in many mammals and represents the ritualized version of the movement anticipating a play bite. The signaling nature of this expression has been proven in many haplorrhine species but never demonstrated in strepsirrhines. Our purpose was assessing whether, also in strepsirrhines, the relaxed open mouth has an actual communicative function. We studied wild ring-tailed lemurs (Lemur catta), characterized by highly social habits including intense playful interactions. They largely use playful signals, mostly performed with the black and white tail. The signaling function of the tail (tail play) has been widely demonstrated. We analyzed both tail play and the relaxed open mouth to verify how their distribution is affected by different play variables (e.g., play session symmetry, number of play mates, previous use of the same pattern). Indeed, ring-tailed lemurs use the relaxed open mouth as a communicative signal during play. Relaxed open mouth was more frequent during unbalanced interactions showing the highest asymmetry in the patterns performed by the two players (offensive/neutral). Compared to tail play, relaxed open mouth was more frequent during dyadic than polyadic interactions and, as a highly directional signal, it was more frequently replicated by the play mate. Therefore, the relaxed open mouth needs to be performed face-to-face so that signal detection can be optimized. Similar to previous findings in monkeys and apes, the relaxed open mouth in lemurs seems to be a ritualized signal used to engage and, perhaps, sustain playful interaction.

The ecology of spatial memory in four lemur species.

Evolutionary theories suggest that ecology is a major factor shaping cognition in primates. However, there have been few systematic tests of spatial memory abilities involving multiple primate species. Here, we examine spatial memory skills in four strepsirrhine primates that vary in level of frugivory: ruffed lemurs (Varecia sp.), ring-tailed lemurs (Lemur catta), mongoose lemurs (Eulemur mongoz), and Coquerel's sifakas (Propithecus coquereli). We compare these species across three studies targeting different aspects of spatial memory: recall after a long-delay, learning mechanisms supporting memory and recall of multiple locations in a complex environment. We find that ruffed lemurs, the most frugivorous species, consistently showed more robust spatial memory than the other species across tasks-especially in comparison with sifakas, the most folivorous species. We discuss these results in terms of the importance of considering both ecological and social factors as complementary explanations for the evolution of primate cognitive skills.

Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear.

Studies suggest that haplorhine primates are sensitive to what others can see and hear. Using two experimental designs, we tested the hypothesis that ring-tailed lemurs (N = 16) are also sensitive to the visual and auditory perception of others. In the first task, we used a go/no-go design that required lemurs to exploit only auditory information. In the second task, we used a forced-choice design where lemurs competed against a human who would prevent them from obtaining food if their approaches were detected. Subjects were given the choice of obtaining food silently or noisily when the competitor's back was turned. They were also given the choice to obtain food when the competitor could either see them or not. Here, we replicate the findings of previous studies indicating that ring-tailed lemurs are sensitive to whether they can be seen; however, we found no evidence that subjects are sensitive to whether others can hear them. Our findings suggest that ring-tailed lemurs converge with haplorhine primates only in their sensitivity to the visual information of others. The results emphasize the importance of investigating social cognition across sensory domains in order to elucidate the cognitive mechanisms that underlie apparently complex social behavior. These findings also suggest that the social dynamics of haplorhine groups impose greater cognitive demands than lemur groups, despite similarities in total group size.