Marine Joly

Touchscreen-based cognitive tasks reveal age-related impairment in a primate aging model, the grey mouse lemur (Microcebus murinus).

Mouse lemurs are suggested to represent promising novel non-human primate models for aging research. However, standardized and cross-taxa cognitive testing methods are still lacking. Touchscreen-based testing procedures have proven high stimulus control and reliability in humans and rodents. The aim of this study was to adapt these procedures to mouse lemurs, thereby exploring the effect of age. We measured appetitive learning and cognitive flexibility of two age groups by applying pairwise visual discrimination (PD) and reversal learning (PDR) tasks. On average, mouse lemurs needed 24 days of training before starting with the PD task. Individual performances in PD and PDR tasks correlate significantly, suggesting that individual learning performance is unrelated to the respective task. Compared to the young, aged mouse lemurs showed impairments in both PD and PDR tasks. They needed significantly more trials to reach the task criteria. A much higher inter-individual variation in old than in young adults was revealed. Furthermore, in the PDR task, we found a significantly higher perseverance in aged compared to young adults, indicating an age-related deficit in cognitive flexibility. This study presents the first touchscreen-based data on the cognitive skills and age-related dysfunction in mouse lemurs and provides a unique basis to study mechanisms of inter-individual variation. It furthermore opens exciting perspectives for comparative approaches in aging, personality, and evolutionary research.

Do solitary foraging nocturnal mammals plan their routes

Large-brained diurnal mammals with complex social systems are known to plan where and how to reach a resource, as shown by a systematic movement pattern analysis. We examined for the first time large-scale movement patterns of a solitary-ranging and small-brained mammal, the mouse lemur (Microcebus murinus), by using the change-point test and a heuristic random travel model to get insight into foraging strategies and potential route-planning abilities. Mouse lemurs are small nocturnal primates inhabiting the seasonal dry deciduous forest in Madagascar. During the lean season with limited food availability, these lemurs rely on few stationary food resources. We radio-tracked seven lemurs and analysed their foraging patterns. First change-points coincided with out-of-sight keystone food resources. Travel paths were more efficient in detecting these resources than a heuristic random travel model within limits of estimated detection distance. Findings suggest that even nocturnal, solitary-ranging mammals with small brains plan their route to an out-of-sight target. Thus, similar ecological pressures may lead to comparable spatial cognitive skills irrespective of the degree of sociality or relative brain size.

Posture Does Not Matter! Paw Usage and Grasping Paw Preference in a Small-Bodied Rooting Quadrupedal Mammal

Background Recent results in birds, marsupials, rodents and nonhuman primates suggest that phylogeny and ecological factors such as body size, diet and postural habit of a species influence limb usage and the direction and strength of limb laterality. To examine to which extent these findings can be generalised to small-bodied rooting quadrupedal mammals, we studied trees shrews (Tupaia belangeri). Methodology/Principal Findings We established a behavioural test battery for examining paw usage comparable to small-bodied primates and tested 36 Tupaia belangeri. We studied paw usage in a natural foraging situation (simple food grasping task) and measured the influence of varying postural demands (triped, biped, cling, sit) on paw preferences by applying a forced-food grasping task similar to other small-bodied primates. Our findings suggest that rooting tree shrews prefer mouth over paw usage to catch food in a natural foraging situation. Moreover, we demonstrated that despite differences in postural demand, tree shrews show a strong and consistent individual paw preference for grasping across different tasks, but no paw preference at a population level. Conclusions/Significance Tree shrews showed less paw usage than small-bodied quadrupedal and arboreal primates, but the same paw preference. Our results confirm that individual paw preferences remain constant irrespective of postural demand in some small-bodied quadrupedal non primate and primate mammals which do not require fine motoric control for manipulating food items. Our findings suggest that the lack of paw/hand preference for grasping food at a population level is a universal pattern among those species and that the influence of postural demand on manual lateralisation in quadrupeds may have evolved in large-bodied species specialised in fine manipulations of food items.

The role of acoustic signaling for spacing and group coordination in a nocturnal, pair-living primate, the western woolly lemur (Avahi occidentalis)

OBJECTIVES How social groups govern their distribution in time and space is a central question in socioecology. The aim of this study is to explore the role of acoustic signaling for spacing and cohesiveness in a nocturnal, cohesive, pair-living strepsirrhine. MATERIAL AND METHODS The study was conducted in northwestern Madagascar. Six pairs of Avahi occidentalis were radio-collared and home range usage, vocalizations and call-associated behavior recorded using GPS-based focal animal sampling. Home range size was analyzed using ArcView GIS 3.3. Calls were characterized by a multiparametric sound analysis. RESULTS Three frequently used, acoustically distinct call types were identified: the avahee call, the whistle call, and the growling call, the latter is a soft; the two others are loud calls. Call types are given by both sexes and convey individually-specific signatures. Call types are used primarily in the locomotion context in the non-core-area of home ranges. The least common avahee call is responded by the avahee call from farther away. The more common whistle call, given when partners become visually isolated, and the growling call emitted at close distances, were answered by the whistle and the growling call. Results suggest a spacing function for the avahee call and group coordination functions for the other call types. DISCUSSION Our study provides first empirical evidence for a nocturnal, cohesive pair-living strepsirrhine that vocal signaling represents an important mechanism for spacing, group coordination and decision making. Findings contribute to a better understanding of the evolutionary roots of primate vocal communication.

MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus).

Human and non-human primates exhibit facial movements or displays to communicate with one another. The evolution of form and function of those displays could be better understood through multispecies comparisons. Anatomically based coding systems (Facial Action Coding Systems: FACS) are developed to enable such comparisons because they are standardized and systematic and aid identification of homologous expressions underpinned by similar muscle contractions. To date, FACS has been developed for humans, and subsequently modified for chimpanzees, rhesus macaques, orangutans, hylobatids, dogs, and cats. Here, we wanted to test whether the MaqFACS system developed in rhesus macaques (Macaca mulatta) could be used to code facial movements in Barbary macaques (M. sylvanus), a species phylogenetically close to the rhesus macaques. The findings show that the facial movement capacity of Barbary macaques can be reliably coded using the MaqFACS. We found differences in use and form of some movements, most likely due to specializations in the communicative repertoire of each species, rather than morphological differences.

Seasonal Effects on Sleeping Site Ecology in a Nocturnal Pair-Living Lemur (Avahi occidentalis)

Seasonal changes may have a strong effect on the safety of sleeping sites in arboreal primates. For example, changes in vegetation thickness may impact predation risk and energy expenditure related to thermoregulation. We investigated how seasonality influenced sleeping site characteristics and usage pattern in an arboreal primate living in a highly seasonal environment. The western woolly lemur (Avahi occidentalis) lives in the dry deciduous forest of northwestern Madagascar, where leaf coverage greatly varies across the year. We examined the hypothesis that these lemurs change their sleeping site behavior dependent on season. We collected data on sleeping site height and location, and characterized usage patterns in six radiotagged pairs between May and December 2008. During the late dry season, pairs preferentially slept in the middle part of a tree. In contrast, there was no height preference during the early rainy season. The lemurs used more sleeping sites during the early rainy than during the late dry season and stayed more days at the same sleeping tree in the late dry season. Our findings support the hypothesis that season affects sleeping site selection in an arboreal primate species living in a highly seasonal environment. During the late dry season, western woolly lemurs are particularly conspicuous to hunters and we therefore suggest a better monitoring of the forest in this season to guarantee their future survival.

Intraocular pressure in the smallest primate aging model: the gray mouse lemur

OBJECTIVE The aim of this study was to assess the practicability of common tonometers used in veterinary medicine for rapid intraocular pressure (IOP) screening, to calibrate IOP values gained by the tonometers, and to define a reference IOP value for the healthy eye in a new primate model for aging research, the gray mouse lemur. STUDIED ANIMALS AND PROCEDURES TonoVet® and the TonoPen™ measurements were calibrated manometrically in healthy enucleated eyes of mouse lemurs euthanized for veterinary reasons. For comparison of the practicability of both tonometers as a rapid IOP assessment tool for living mouse lemurs, the IOP of 24 eyes of 12 animals held in the hand was measured. To define a standard reference value for IOP in mouse lemurs, 258 healthy animals were measured using the TonoVet® . RESULTS Intraocular pressure measurements for the TonoVet® can be corrected using the formula: y = 0.981 + (1.962*TonoVet® value), and those for the TonoPen™ using that of y = 5.38 + (1.426*TonoPen™ value). The calibrated IOP for a healthy mouse lemur eye was 20.3 ± 2.8 mmHg. The TonoVet® showed advantages in practicability, for example, small corneal contact area, short and painless corneal contact, shortened total time spent on investigation, as well as the more accurate measured values. IOP measurements of healthy mouse lemur eyes were not affected by age, sex, eye side, or colony. CONCLUSION Tonometry using TonoVet® is the more practicable assessment tool for IOP measurement of the tiny eyes of living mouse lemurs. Pathological deviations can be identified based on the described reference value.

Photoperiodic regime influences onset of lens opacities in a non-human primate

Background Opacities of the lens are typical age-related phenomena which have a high influence on photoreception and consequently circadian rhythm. In mouse lemurs, a small bodied non-human primate, a high incidence (more than 50% when >seven years) of cataracts has been previously described during aging. Previous studies showed that photoperiodically induced accelerated annual rhythms alter some of mouse lemurs’ life history traits. Whether a modification of photoperiod also affects the onset of age dependent lens opacities has not been investigated so far. The aim of this study was therefore to characterise the type of opacity and the mouse lemurs’ age at its onset in two colonies with different photoperiodic regimen. Methods Two of the largest mouse lemur colonies in Europe were investigated: Colony 1 having a natural annual photoperiodic regime and Colony 2 with an induced accelerated annual cycle. A slit-lamp was used to determine opacities in the lens. Furthermore, a subset of all animals which showed no opacities in the lens nucleus in the first examination but developed first changes in the following examination were further examined to estimate the age at onset of opacities. In total, 387 animals were examined and 57 represented the subset for age at onset estimation. Results The first and most commonly observable opacity in the lens was nuclear sclerosis. Mouse lemurs from Colony 1 showed a delayed onset of nuclear sclerosis compared to mouse lemurs from Colony 2 (4.35 ± 1.50 years vs. 2.75 ± 0.99 years). For colony 1, the chronological age was equivalent to the number of seasonal cycles experienced by the mouse lemurs. For colony 2, in which seasonal cycles were accelerated by a factor of 1.5, mouse lemurs had experienced 4.13 ± 1.50 seasonal cycles in 2.75 ± 0.99 chronological years. Discussion Our study showed clear differences in age at the onset of nuclear sclerosis formation between lemurs kept under different photoperiodic regimes. Instead of measuring the chronological age, the number of seasonal cycles (N = four) experienced by a mouse lemur can be used to estimate the risk of beginning nuclear sclerosis formation. Ophthalmological examinations should be taken into account when animals older than 5–6 seasonal cycles are used for experiments in which unrestricted visual ability has to be ensured. This study is the first to assess and demonstrate the influence of annual photoperiod regime on the incidence of lens opacities in a non-human primate.

First comparative approach to touchscreen-based visual object–location paired-associates learning in humans (Homo sapiens) and a nonhuman primate (Microcebus murinus).

A recent study suggests that a specific, touchscreen-based task on visual object–location paired-associates learning (PAL), the so-called Different PAL (dPAL) task, allows effective translation from animal models to humans. Here, we adapted the task to a nonhuman primate (NHP), the gray mouse lemur, and provide first evidence for the successful comparative application of the task to humans and NHPs. Young human adults reach the learning criterion after considerably less sessions (one order of magnitude) than young, adult NHPs, which is likely due to faster and voluntary rejection of ineffective learning strategies in humans and almost immediate rule generalization. At criterion, however, all human subjects solved the task by either applying a visuospatial rule or, more rarely, by memorizing all possible stimulus combinations and responding correctly based on global visual information. An error-profile analysis in humans and NHPs suggests that successful learning in NHPs is comparably based either on the formation of visuospatial associative links or on more reflexive, visually guided stimulus–response learning. The classification in the NHPs is further supported by an analysis of the individual response latencies, which are considerably higher in NHPs classified as spatial learners. Our results, therefore, support the high translational potential of the standardized, touchscreen-based dPAL task by providing first empirical and comparable evidence for two different cognitive processes underlying dPAL performance in primates.

Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance

Contemporary evolutionary theories propose that living in groups drives the selection of enhanced cognitive skills to face competition and facilitate cooperation between individuals. Being able to coordinate both in space and time with others and make strategic decisions are essential skills for cooperating within groups. Social tolerance and an egalitarian social structure have been proposed as one specific driver of cooperation. Therefore, social tolerance is predicted to be associated with enhanced cognitive skills that underpin communication and coordination. Social tolerance should also be associated with enhanced inhibition, which is crucial for suppressing automatic responses and permitting delayed gratification in cooperative contexts. We tested the performance of four closely related non-human primate species (genus Macaca) characterized by different degrees of social tolerance on a large battery of cognitive tasks covering physical and social cognition, and on an inhibitory control task. All species performed at a comparable level on the physical cognition tasks but the more tolerant species outperformed the less tolerant species at a social cognition task relevant to cooperation and in the inhibitory control task. These findings support the hypothesis that social tolerance is associated with the evolution of sophisticated cognitive skills relevant for cooperative social living.