Mapping vocal interactions in space and time differentiates signal broadcast versus signal exchange in meerkat groups.

Animal vocal communication research traditionally focuses on acoustic and contextual features of calls, yet substantial information is also contained in response selectivity and timing during vocalization events. By examining the spatiotemporal structure of vocal interactions, we can distinguish between 'broadcast' and 'exchange' signalling modes, with the former potentially serving to transmit signallers' general state and the latter reflecting more interactive signalling behaviour. Here, we tracked the movements and vocalizations of wild meerkat (Suricata suricatta) groups simultaneously using collars to explore this distinction. We found evidence that close calls (used for maintaining group cohesion) are given as signal exchanges. They are typically given in temporally structured call-response sequences and are also strongly affected by the social environment, with individuals calling more when they have more neighbours and juveniles responding more to adults than the reverse. In contrast, short note calls appear mainly in sequences produced by single individuals and show little dependence on social surroundings, suggesting a broadcast signalling mode. Despite these differences, both call categories show similar clustering in space and time at a group level. Our results highlight how the fine-scale structure of vocal interactions can give important insights into the usage and function of signals in social groups. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics.'

Mild movement sequence repetition in five primate species and evidence for a taxonomic divide in cognitive mechanisms.

When animals forage, they face complex multi-destination routing problems. Traplining behaviour-the repeated use of the same route-can be used to study how spatial memory might evolve to cope with complex routing problems in ecologically distinct taxa. We analyzed experimental data from multi-destination foraging arrays for five species, two cercopithecine monkeys (vervets, Chlorocebus pygerythrus, and Japanese macaques, Macaca fuscata) and three strepsirrhines (fat-tailed dwarf lemurs, Cheirogaleus medius, grey mouse lemurs, Microcebus murinus, and aye-ayes, Daubentonia madagascariensis). These species all developed relatively efficient route formations within the arrays but appeared to rely on variable cognitive mechanisms. We found a strong reliance on heuristics in cercopithecoid species, with initial routes that began near optimal and did not improve with experience. In strepsirrhines, we found greater support for reinforcement learning of location-based decisions, such that routes improved with experience. Further, we found evidence of repeated sequences of site visitation in all species, supporting previous suggestions that primates form traplines. However, the recursive use of routes was weak, differing from the strategies seen in well-known traplining animals. Differences between strepsirrhine and cercopithecine strategies may be the result of either ecological or phylogenetic trends, and we discuss future possibilities for disentangling the two.

Enriched sleep environments lengthen lemur sleep duration.

Characteristics of the sleep-site are thought to influence the quality and duration of primate sleep, yet only a handful of studies have investigated these links experimentally. Using actigraphy and infrared videography, we quantified sleep in four lemur species (Eulemur coronatus, Lemur catta, Propithecus coquereli, and Varecia rubra) under two different experimental conditions at the Duke Lemur Center (DLC) in Durham, NC, USA. Individuals from each species underwent three weeks of simultaneous testing to investigate the hypothesis that comfort level of the sleep-site influences sleep. We obtained baseline data on normal sleep, and then, in a pair-wise study design, we compared the daily sleep times, inter-daily activity stability, and intra-daily activity variability of individuals in simultaneous experiments of sleep-site enrichment and sleep-site impoverishment. Over 164 24-hour periods from 8 individuals (2 of each species), we found evidence that enriched sleep-sites increased daily sleep times of lemurs, with an average increase of thirty-two minutes. The effect of sleep-site impoverishment was small and not statistically significant. Though our experimental manipulations altered inter-daily stability and intra-daily variability in activity patterns relative to baseline, the changes did not differ significantly between enriched and impoverished conditions. We conclude that properties of a sleep-site enhancing softness or insulation, more than the factors of surface area or stability, influence lemur sleep, with implications regarding the importance of nest building in primate evolution and the welfare and management of captive lemurs.

Effects of host extinction and vector preferences on vector-borne disease risk in phylogenetically structured host-hector communities.

Anthropogenic disturbance impacts the phylogenetic composition and diversity of ecological communities. While changes in diversity are known to dramatically change species interactions and alter disease dynamics, the effects of phylogenetic changes in host and vector communities on disease have been relatively poorly studied. Using a theoretical model, we investigated how phylogeny and extinction influence network structural characteristics relevant to disease transmission in disturbed environments. We modelled a multi-host, multi-vector community as a bipartite ecological network, where nodes represent host and vector species and edges represent connections among them through vector feeding, and we simulated vector preferences and threat status on host and parasite phylogenies. We then simulated loss of hosts, including phylogenetically clustered losses, to investigate how extinction influences network structure. We compared effects of phylogeny and extinction to those of host specificity, which we predicted to strongly increase network modularity and reduce disease prevalence. The simulations revealed that extinction often increased modularity, with higher modularity as species loss increased, although not as much as increasing host specificity did. These results suggest that extinction itself, all else being equal, may reduce disease prevalence in disturbed communities. However, in real communities, systematic patterns in species loss (e.g. favoring high competence species) or changes in abundance may counteract these effects. Unexpectedly, we found that effects of phylogenetic signal in host and vector traits were relatively weak, and only important when phylogenetic signal of host and vector traits were similar, or when these traits both varied.

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.

Evolutionary dynamics of sexual size dimorphism in non-volant mammals following their independent colonization of Madagascar.

As predicted by sexual selection theory, males are larger than females in most polygynous mammals, but recent studies found that ecology and life history traits also affect sexual size dimorphism (SSD) through evolutionary changes in either male size, female size, or both. The primates of Madagascar (Lemuriformes) represent the largest group of mammals without male-biased SSD. The eco-evo-devo hypothesis posited that adaptations to unusual climatic unpredictability on Madagascar have ultimately reduced SSD in lemurs after dispersing to Madagascar, but data have not been available for comparative tests of the corresponding predictions that SSD is also absent in other terrestrial Malagasy mammals and that patterns of SSD changed following the colonization of Madagascar. We used phylogenetic methods and new body mass data to test these predictions among the four endemic radiations of Malagasy primates, carnivorans, tenrecs, and rodents. In support of our prediction, we found that male-biased SSD is generally absent among all Malagasy mammals. Phylogenetic comparative analyses further indicated that after their independent colonization of Madagascar, SSD decreased in primates and tenrecs, but not in the other lineages or when analyzed across all species. We discuss several mechanisms that may have generated these patterns and conclude that neither the eco-evo-devo hypothesis, founder effects, the island rule nor sexual selection theory alone can provide a compelling explanation for the observed patterns of SSD in Malagasy mammals.

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.

Evolutionary change in physiological phenotypes along the human lineage.

BACKGROUND AND OBJECTIVES: Research in evolutionary medicine provides many examples of how evolution has shaped human susceptibility to disease. Traits undergoing rapid evolutionary change may result in associated costs or reduce the energy available to other traits. We hypothesize that humans have experienced more such changes than other primates as a result of major evolutionary change along the human lineage. We investigated 41 physiological traits across 50 primate species to identify traits that have undergone marked evolutionary change along the human lineage. METHODOLOGY: We analysed the data using two Bayesian phylogenetic comparative methods. One approach models trait covariation in non-human primates and predicts human phenotypes to identify whether humans are evolutionary outliers. The other approach models adaptive shifts under an Ornstein-Uhlenbeck model of evolution to assess whether inferred shifts are more common on the human branch than on other primate lineages. RESULTS: We identified four traits with strong evidence for an evolutionary increase on the human lineage (amylase, haematocrit, phosphorus and monocytes) and one trait with strong evidence for decrease (neutrophilic bands). Humans exhibited more cases of distinct evolutionary change than other primates. CONCLUSIONS AND IMPLICATIONS: Human physiology has undergone increased evolutionary change compared to other primates. Long distance running may have contributed to increases in haematocrit and mean corpuscular haemoglobin concentration, while dietary changes are likely related to increases in amylase. In accordance with the pathogen load hypothesis, human monocyte levels were increased, but many other immune-related measures were not. Determining the mechanisms underlying conspicuous evolutionary change in these traits may provide new insights into human disease.

Inference by exclusion in lion-tailed macaques (Macaca silenus), a hamadryas baboon (Papio hamadryas), capuchins (Sapajus apella), and squirrel monkeys (Saimiri sciureus).

Previous research has suggested that several primate species may be capable of reasoning by exclusion based on the finding that they can locate a hidden object when given information about where the object is not. The present research replicated and extended the literature by testing 2 Old World monkey species, lion-tailed macaques (Macaca silenus) and a hamadryas baboon (Papio hamadryas), and 2 New World species, capuchin monkeys (Sapajus apella) and squirrel monkeys (Saimiri sciureus). The New World monkeys were tested on the traditional 2-way object choice task, and all 4 species were also tested on a more complex 3-way object choice task. In addition, the squirrel monkeys were tested on a 2-way object choice task with auditory information. The results showed that, whereas the Old World species were able to infer by exclusion on the 3-object task, some of the capuchin monkeys had difficulty on each of the 2- and 3-cup tasks. All but 1 of the squirrel monkeys failed to infer successfully, and their strategies appeared to differ between the visual and auditory versions of the task. Taken together, this research suggests that the ability to succeed on this inference task may be present throughout Old World monkey species, but is fragile in the New World species tested thus far. (PsycINFO Database Record

Information seeking in capuchins (Cebus apella): a rudimentary form of metacognition?

In previous research, great apes and rhesus macaques have demonstrated multiple apparently metacognitive abilities, whereas capuchin monkeys have not. The present experiment investigated whether at least a rudimentary form of metacognition might be demonstrated in capuchins if a simplified metacognitive task was used. Capuchins (Cebus apella) were required to locate a food reward hidden beneath one of two inverted cups that sat on a Plexiglas tray. In some conditions, the capuchins were shown where the food was hidden, in others they could infer its location, and in yet others they were not given information about the location of the food. On all trials, capuchins could optionally seek information about the food's location by looking up through the Plexiglas beneath the cups. In general, capuchins did this less often when they were shown the food reward, but not when they could infer the reward's location. These data suggest that capuchins-if metacognitive-only metacognitively control their information seeking in some conditions, particularly those in which information is presented in the visual domain. This may represent a rudimentary version of metacognitive control, in comparison with that seen in great apes and humans.