2022-06-03, Harel, Roi, Alavi, Shauhin, Ashbury, Alison M., Davis, Grace, Kalbitzer, Urs, Nunez, Chase L., Vining, Alexander Q., Walton, Zea, Havmøller, Rasmus Worsøe, Crofoot, Margaret C.

The complex, interconnected, and non-contiguous nature of canopy environments present unique cognitive, locomotor, and sensory challenges to their animal inhabitants. Animal movement through forest canopies is constrained; unlike most aquatic or aerial habitats, the three-dimensional space of a forest canopy is not fully realized or available to the animals within it. Determining how the unique constraints of arboreal habitats shape the ecology and evolution of canopy-dwelling animals is key to fully understanding forest ecosystems. With emerging technologies, there is now the opportunity to quantify and map tree connectivity, and to embed the fine-scale horizontal and vertical position of moving animals into these networks of branching pathways. Integrating detailed multi-dimensional habitat structure and animal movement data will enable us to see the world from the perspective of an arboreal animal. This synthesis will shed light on fundamental aspects of arboreal animals’ cognition and ecology, including how they navigate landscapes of risk and reward and weigh energetic trade-offs, as well as how their environment shapes their spatial cognition and their social dynamics.

2019-09, Samson, David R., Vining, Alexander Q., Nunn, Charles L.

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.

2016, Vining, Alexander Q., Nunn, Charles L.

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.

2022-01-05, Alavi, Shauhin, Vining, Alexander Q., Caillaud, Damien, Hirsch, Ben T., Havmøller, Rasmus Worsøe, Havmøller, Linnea W., Kays, Roland, Crofoot, Margaret C.

Animal movement along repeatedly used, “habitual” routes could emerge from a variety of cognitive mechanisms, as well as in response to a diverse set of environmental features. Because of the high conservation value of identifying wildlife movement corridors, there has been extensive work focusing on environmental factors that contribute to the emergence of habitual routes between protected habitats. In parallel, significant work has focused on disentangling the cognitive mechanisms underlying animal route use, as such movement patterns are of fundamental interest to the study of decision making and navigation. We reviewed the types of processes that can generate routine patterns of animal movement, suggested a new methodological workflow for classifying one of these patterns—high fidelity path reuse—in animal tracking data, and compared the prevalence of this pattern across four sympatric species of frugivorous mammals in Panama. We found the highest prevalence of route-use in kinkajous, the only nocturnal species in our study, and propose that further development of this method could help to distinguish the processes underlying the presence of specific routes in animal movement data.

2019-05, Teichroeb, Julie A., Vining, Alexander Q.

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.

2015-08, Marsh, Heidi L., Vining, Alexander Q., Levendoski, Emma K., Judge, Peter G.

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.

2021, Vining, Alexander Q., Nunn, Charles L., Samson, David R.

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.

2019, Kappeler, Peter M., Nunn, Charles L., Vining, Alexander Q., Goodman, Steven M.

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.

2015-05, Vining, Alexander Q., Marsh, Heidi L.

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.