Search

Studies on drawing often focused on spatial aspects of the finished products. Here, the drawing behavior was studied by analyzing its intermittent process, between drawing (i.e. marking a surface) and interruption (i.e. a pause in the marking gesture). To assess how this intermittence develops with age, we collected finger-drawings on a touchscreen by 185 individuals (children and adults). We measured the temporal structure of each drawing sequence to determine its complexity. To do this, we applied temporal fractal estimators to each drawing time series before combining them in a Principal Component Analysis procedure. The youngest children (3-year-old) drew in a more stereotypical way with long-range dependence detected in their alternations between states. Among older children and adults, the complexity of drawing sequences increased showing a less predictable behavior as their drawings become more detailed and figurative. This study improves our understanding of the temporal aspects of drawing behavior, and contributes to an objective understanding of its ontogeny.

Female primates represent the most important social partner for their developing offspring. However, mothers may strongly differ in the way they relate to their offspring (e.g., in terms of two different dimensions: protectiveness and rejection). In this study, we aimed to assess how dominance style predicts (i) changes in maternal behavior through offspring development, and (ii) the link between maternal behavior and offspring behavior. We conducted behavioral observations on 34 free-ranging immatures of two species of macaques with different dominance styles: less tolerant Japanese macaques (JM; Macaca fuscata) and more tolerant moor macaques (MM; Macaca maura). Our results showed that maternal behavior differed between JM and MM: maternal proximity and grooming decreased through offspring development more quickly in MM than in JM, whereas maternal rejection and aggression, which were generally more frequent in JM, decreased with offspring age similarly in both species. In contrast, maternal restraint of offspring decreased similarly with offspring age in both species. Furthermore, dominance style was differentially associated with the link between maternal and offspring behavior: in MM only, maternal grooming predicted an increase of the probability that offspring interacted with partners other than their mothers and engaged in solitary play, whereas maternal rejection predicted a decrease in the occurrence of solitary play. Overall, these results suggest interspecific variation in maternal behavior during offspring's first years of life, and point to the possibility that these differences may have an important role in shaping their behavioral development.

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere. Published version This study was financially supported by grants from Kyoto University, Japan through its Step-Up program (AM) and by the Japan Society for the Promotion of Science (#24770232 and #16H06181 to AM, and #15H04283 to MO). LF was supported by the Japan Ministry of Education, Culture, Sports, Science and Technology (MEXT) through a Monbukagakusho schol- arship (#140411), by the Japan Society for the Promotion of Science through a JSPS-DC2 fellowship and Grant-in-Aid (#446), and by the Leading Graduate Program in Primatology and Wildlife Science (PWS) of Kyoto University (JSPS-U04).

Identifying how infection modifies host behaviours that determine social contact networks is important for understanding heterogeneity in infectious disease dynamics. Here, we investigate whether group social behaviour is modified during bacterial infection in fruit flies ( Drosophila melanogaster ) according to pathogen species, infectious dose, host genetic background and sex. In one experiment, we find that systemic infection with four different bacterial species results in a reduction in the mean pairwise distance within infected female flies, and that the extent of this change depends on pathogen species. However, susceptible flies did not show any evidence of avoidance in the presence of infected flies. In a separate experiment, we observed genetic- and sex-based variation in social aggregation within infected, same-sex groups, with infected female flies aggregating more closely than infected males. In general, our results confirm that bacterial infection induces changes in fruit fly behaviour across a range of pathogen species, but also highlight that these effects vary between fly genetic backgrounds and can be sex-specific. We discuss possible explanations for sex differences in social aggregation and their consequences for individual variation in pathogen transmission.

Background Anaesthesia is often required in common marmosets undergoing various procedures. The aim of this study was to evaluate anaesthetic and cardiopulmonary effects of alfaxalone, alfaxalone-ketamine and alfaxalone-butorphanol-medetomidine in common marmosets. Methods The following treatments were repeatedly administered to seven female common marmosets: Treatment A, alfaxalone (12 mg kg-1 ) alone; treatment AK, alfaxalone (1 mg animal-1 ) plus ketamine (2.5 mg animal-1 ); treatment AMB, alfaxalone (4 mg kg-1 ), medetomidine (50 µg kg-1 ) plus butorphanol (0.3 mg kg-1 ); and treatment AMB-Ati, AMB with atipamezole at 45 minutes. Results and conclusions Marmosets became laterally recumbent and unresponsive for approximately 30 minutes in A and AK and for approximately 60 minutes in AMB. The animals showed rapid recovery following atipamezole injection in AMB-Ati. The decrease in heart rate and SpO2 was significantly greater in AMB compared to A and AK. Oxygen supplementation, anaesthetic monitors and atipamezole should be available especially when AMB is administered.

Changes in marine ecosystems are easier to detect in upper‐level predators, like seabirds, which integrate trophic interactions throughout the food web.Here, we examined whether diving parameters and complexity in the temporal organization of diving behavior of little penguins (Eudyptula minor) are influenced by sea surface temperature (SST), water stratification, and wind speed—three oceanographic features influencing prey abundance and distribution in the water column.Using fractal time series analysis, we found that foraging complexity, expressed as the degree of long‐range correlations or memory in the dive series, was associated with SST and water stratification throughout the breeding season, but not with wind speed. Little penguins foraging in warmer/more‐stratified waters exhibited greater determinism (memory) in foraging sequences, likely as a response to prey aggregations near the thermocline. They also showed higher foraging efficiency, performed more dives and dove to shallower depths than those foraging in colder/less‐stratified waters.Reductions in the long‐term memory of dive sequences, or in other words increases in behavioral stochasticity, may suggest different strategies concerning the exploration–exploitation trade‐off under contrasting environmental conditions., Little penguins foraging in warmer/more‐stratified waters exhibited less stochastic foraging sequences likely as a response to prey aggregations nearby the thermocline. Ultimately, they showed higher foraging efficiency and numbers of dives, and lower mean dive depths than those foraging in colder/less‐stratified waters.

Group living is beneficial for individuals, but also comes with costs. One such cost is the increased possibility of pathogen transmission because increased numbers or frequencies of social contacts are often associated with increased parasite abundance or diversity. The social structure of a group or population is paramount to patterns of infection and transmission. Yet, for various reasons, studies investigating the links between sociality and parasitism in animals, especially in primates, have only accounted for parts of the group (e.g., only adults), which is likely to impact the interpretation of results. Here, we investigated the relationship between social network centrality and an estimate of gastrointestinal helminth infection intensity in a whole group of Japanese macaques (Macaca fuscata). We then tested the impact of omitting parts of the group on this relationship. We aimed to test: (1) whether social network centrality – in terms of the number of partners (degree), frequency of interactions (strength), and level of social integration (eigenvector) – was linked to parasite infection intensity (estimated by eggs per gram of faeces, EPG); and, (2) to what extent excluding portions of individuals within the group might influence the observed relationship. We conducted social network analysis on data collected from one group of Japanese macaques over three months on Koshima Island, Japan. We then ran a series of knock-out simulations. General linear mixed models showed that, at the whole-group level, network centrality was positively associated with geohelminth infection intensity. However, in partial networks with only adult females, only juveniles, or random subsets of the group, the strength of this relationship - albeit still generally positive - lost statistical significance. Furthermore, knock-out simulations where individuals were removed but network metrics were retained from the original whole-group network showed that these changes are partly a power issue and partly an effect of sampling the incomplete network. Our study indicates that sampling bias can thus hamper our ability to detect real network effects involving social interaction and parasitism. In addition to supporting earlier results linking geohelminth infection to Japanese macaque social networks, this work introduces important methodological considerations for research into the dynamics of social transmission, with implications for infectious disease epidemiology, population management, and health interventions.

Studies on drawing often focused on spatial aspects of the finished products. Here, the drawing behaviour was studied by analysing its intermittent process, between drawing (i.e. marking a surface) and interruption (i.e. a pause in the marking gesture). To assess how this intermittence develops with age, we collected finger-drawings on a touchscreen by 185 individuals (children and adults). We measured the temporal structure of each drawing sequence to determine its complexity. To do this, we applied temporal fractal estimators to each drawing time series before combining them in a Principal Component Analysis procedure. The youngest children (3 years-old) drew in a more stereotypical way with long-range dependence detected in their alternations between states. Among older children and adults, the complexity of drawing sequences increased showing a less predictable behaviour as their drawings become more detailed and figurative. This study improves our understanding of the temporal aspects of drawing behaviour, and contributes to an objective understanding of its ontogeny.

Long-range signaling, such as acoustic communication, is best understood within the broader context of all potential receivers. Exactly what kind of information is transmitted or obtained is a matter of debate. To address this issue, we describe the communication network of a population of wild siamangs (Symphalangus syndactylus), small territorial apes that sing loud and complex duets. Based on calling data collected over >3400 observation hours on 7 groups of wild siamangs, we used linear mixed-effects models to evaluate the effect of changes in group composition on singing rates and social network analysis to study the effect of social change on the structure of this siamang communication network. Results show that, compared to stable groups, groups whose composition had recently changed elicited significantly more responses to their calls from neighboring groups. These results support the hypothesis that listening individuals can take advantage of public information to detect points of social instability in the community, e.g., adult males seeking opportunities to obtain their own territory. Our results help explain some sociobiological conundrums concerning hylobatids, e.g., by highlighting a potential strategic benefit for males living in the multimale, single female groups that are reported in some species, advance our understanding of the function of calling in hylobatids, and offer theoretical and methodological insights applicable to other taxa such as birds and cetaceans.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships. Publisher PDF

Lemuricola (Protenterobius) nycticebi is the only pinworm species known to infect strepsirrhine primates outside Africa, and the only pinworm species yet described in slow lorises. Here, we provided a detailed morphological comparison of female and male worms, and a first description of fourth-stage larvae collected from free-living slow lorises (Nycticebus menagensis) in Sabah, Malaysian Borneo. Using mitochondrial and nuclear markers, we also reconstructed the species' phylogenetic relationship with other pinworms infecting primates. Both morphological and molecular results indicated a distinct association between L. (P.) nycticebi and its host. However, while taxonomy identified this species as a member of the Lemuricola clade and grouped pinworms infecting lemurs and slow lorises together, phylogenetic reconstruction split them, placing L. (P.) nycticebi within the Enterobius clade. Our results suggest that L. (P.) nycticebi may represent a different taxon altogether, and that it is more closely related to pinworm species infecting Old World primates outside Madagascar. Pongobius pongoi (Foitová et al., 2008) n. comb. is also proposed., Graphical abstract Image 1, Highlights • Pinworms and their primate hosts have a long history of association. • L. (P.) nycticebi was recovered from slow lorises in the wild. • L. (P.) nycticebi was taxonomy classified within the Lemuricola clade. • However, molecular phylogenetics placed it within the Enterobius clade. • Taxonomic and molecular identifications should complement species descriptions.

Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates’ home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross‐species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum, the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.

Este artículo se encuentra disponible en la siguiente URL: https://www.nature.com/articles/s41598-021-84250-5.pdf Gaze sensitivity allows us to interpret the visual perspective of others, inferring their intentions and attentional states. In order to clarify the evolutionary history of this ability, we assessed the response of free-ranging Japanese macaques (Macaca fuscata) to human gaze in three contexts: threat (Experiment 1), cooperation (Experiment 2), and competition (Experiment 3). Subjects interpreted the direct gaze of an approaching human as a sign of threat, showing a greater flight initiation distance and more threats towards the human in this condition than when the human gazed in another direction. Subjects also adapted their behavior to the attentional cues of a human who gave them food, by for example moving into his visual field. However, the macaques did not seem to take the visual perspective of a human competing with them over food, as they failed to first retrieve the food that was not visible to the human (i.e., located behind an opaque barrier). Our results support the idea that Japanese macaques can respond to a human’s gaze flexibly depending on the context. Moreover, they highlight the importance of studying animal behavior across different species and contexts to better understand the selective pressures that might have led to its evolution.

Este artículo se encuentra disponible en la siguiente URL: https://www.nature.com/articles/s41598-021-82198-0.pdf En este artículo también participan: Risma Illa Maulany, Putu Oka Ngakan y Federica Amici. In several species, rank predicts access to food, and subordinates may need specific behavioural strategies to get a share of resources. This may be especially important in despotic species, where resources are strongly biased in favour of dominants and subordinates may more strongly rely on specific tactics to maximize food intake. Here, we compared three macaque species with an experimental set-up reproducing feeding competition contest. Following our predictions, more tolerant species mostly retrieved food in the presence of others and were less dependent on specific tactics. Contrarily, subordinates in more despotic species more likely collected food (1) when dominants could not see food or (2) were attacking others, (3) while “dissimulating”, or (4) “storing food”. Our study reveals that dominance styles reliably predict the probability of using specific food retrieval tactics and provides important insights on the social conditions that might have led to the emergence of tactical deception.

Metamorphosis is a widespread developmental process that involves considerable changes in morphology, habitat use, ecology and behaviour between early developmental (larval) stages and adult forms. Among amphibians, anuran larvae (tadpoles) undergo massive morphological and ecological changes during their development, with early stages characterized by somatic growth, whereas more conspicuous changes (i.e. metamorphosis) occur later during development. In this study, we examined how locomotor and behavioural traits covary with morphology (body size) and metamorphosis (hindlimb and forelimb development) across developmental stages in spined toad (Bufo spinosus) tadpoles. As expected, we found that locomotion and behaviour undergo significant changes during tadpole development. These changes are curvilinear across developmental stages, with a phase of increasing activity and locomotion followed by a phase of stasis and/or reduction in locomotion and behavioural complexity. All the metrics we investigated indicate that the peak of activity and associated behaviour is situated at a pivotal stage when somatic growth decreases and significant morphological changes occur (i.e. hindlimb growth). Future studies that aim to investigate determinants of locomotion should include developmental stages as covariates in order to assess whether the sensitivity of locomotion to environmental variables changes across developmental stages.

Este artículo se encuentra disponible en la siguiente URL: https://www.nature.com/articles/s41598-020-79246-6.pdf En este artículo también participan: Karimullah Karimullah, Risma Illa Maulany, Putu Oka Ngakan, Andi Siady Hamzah y Bonaventura Majolo. Primates live in complex social systems with social structures ranging from more to less despotic. In less despotic species, dominance might impose fewer constraints on social choices, tolerance is greater than in despotic species and subordinates may have little need to include novel food items in the diet (i.e. neophilia), as contest food competition is lower and resources more equally distributed across group members. Here, we used macaques as a model to assess whether different dominance styles predict differences in neophilia and social tolerance over food. We provided familiar and novel food to 4 groups of wild macaques (N = 131) with different dominance styles (Macaca fuscata, M. fascicularis, M. sylvanus, M. maura). Our study revealed inter- and intra-specific differences in individuals’ access to food, which only partially reflected the dominance styles of the study subjects. Contrary to our prediction, social tolerance over food was higher in more despotic species than in less despotic species. Individuals with a higher dominance rank and being better socially integrated (i.e. higher Eigenvector centrality) were more likely to retrieve food in all species, regardless of their dominance style. Partially in line with our predictions, less integrated individuals more likely overcame neophobia (as compared to more integrated ones), but only in species with more tolerance over food. Our study suggests that individual characteristics (e.g. social integration or personality) other than dominance rank may have a stronger effect on an individual’s access to resources.

Primate parasite study is an important subject in primate research, especially with the ongoing threats from anthropogenic disturbances such as land conversion and deforestation. This study is conducted to investigate the occurrence of Cryptosporidium and Giardia in primates of the Lower Kinabatangan Wildlife Sanctuary (LKWS), Sabah, Malaysia. Fecal samples collected were tested with immunochromatographic test kits to rapidly screen for Cryptosporidium spp. and Giardia spp. in samples from 45 long-tailed macaques and 40 proboscis monkeys. The overall rate of infection for Cryptosporidium spp. for both species is moderately high at approximately 44.71% (n = 38), with 17.64% (n = 14) individuals are positive with Giardia spp., while 38.82% of the individuals (n=33) tested are not infected with either Cryptosporidium spp. or Giardia spp. Parasite documentation is an integral aspect of primate research, as the information will provide insights on the health status and disease risk of non-human primate populations, thus helping scientists to make better conservation plans for wildlife.

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.

International audience; Social information and socially transmitted pathogens are governed by social structure, and also shape social interactions. However, information and infection are rarely investigated as interactive factors driving social evolution. We propose exactly such an integrative framework, drawing attention to mechanisms of social phenotypic plasticity for information spread and pathogen control.

SUMMARY: How interactions between individuals contribute to the emergence of complex societies is a major question in biology. Nonetheless, little remains known about how simple rules of social attraction (e.g. to information) and social avoidance (e.g. of disease) interact to shape sociality. We developed an individual-based model where individuals choose with whom to interact depending on the status of group mates (informed and/or infected). Statistical models indicate that the emergence of social structure depends on the cost/benefit trade-offs underlying the system. Critically, pressures that optimize social relationships – i.e. minimize risky connections while favouring those that maximize benefits – yield modular networks. The most modular networks emerged when few individuals monopolized values of pathogen whereas information was more equally distributed across the group. We argue that investigating the mechanisms of such social trade-offs, simultaneously accounting for both attractive and repulsive forces acting on individuals, will help us understand the complexity of individual relationships.

Soil-transmitted helminths (STH) remain neglected tropical parasites, despite infecting millions of people worldwide and being among the most common parasites regulating wildlife populations. Although typically reported in coproscopic surveys of nonhuman primates (NHP), little is known about factors regulating STH diversity and distribution, or how they might affect their hosts. Here, we investigate STH diversity (species richness) and distribution (infection prevalence) in NHP using an extensive database on primate–parasite associations coupled with sociodemographic and environmental data for each host species. We used principal components analysis (PCA) to reduce a large number of correlated explanatory variables to a smaller number of uncorrelated variables explaining their variance. We then applied a Bayesian phylogenetic mixed-effects modeling framework and provide evidence that environmental, including anthropogenic features, and host-related traits influence parasite diversity and distribution. STH diversity was negatively associated with latitude and human population density in each species’ geographic range, while STH prevalence was positively associated with both latitude and human population density, as well as primate group size. Understanding how anthropogenic change might alter the intimate ecological relationships formed by primates and their oft-neglected parasites should be a priority in the Anthropocene as human–nonhuman primate interfaces continue to expand at unprecedented rates.

International audience; Gastrointestinal nematodes are known to be one of the most economically important parasites in livestock production. In order to test whether fractal analysis of behaviour can be used as a diagnostic tool for detection of infected animals, we investigated fractal patterns in the behavioural activity of domestic sheep (Ovis aries) in relation to strongylid infection. Temporal dynamics in activity patterns of 20 sheep were recorded at high resolutions using tri-axial accelerometer loggers attached to the neck of naturally infected subjects. We measured fractal dynamics in the resultant acceleration time series, divided into periods of activity and inactivity, using several fractal methods and tested the prediction that temporal complexity in the activity patterns of infected control sheep and experimentally dewormed sheep should differ. Detrended fluctuation analysis (DFA) revealed that sheep behaviour sequences were characterized by long-range correlations, meaning that acceleration fluctuations are not random but depend on long-term activity events. Generalized linear mixed models built to test for the effect of deworming on fractal estimates showed that the temporal organization of sheep activity varies with the status of strongylid infection. Our results indicate that sheep treated with anthelmintics exhibited a higher complexity in their activity sequences than parasitized sheep, suggesting that organizational patterns of their behaviour change with gastrointestinal parasite infection. Thus, we provide evidence for the potential utility of fractal methods in behavioural welfare monitoring.

Within host communities, related species are more likely to share common parasitic agents, and as a result, morphological similarities have led researchers to conclude that parasites infecting closely related hosts within a community represent a single species. However, genetic diversity within parasite genera and host range remain poorly investigated in most systems. Strongyloides is a genus of soil-transmitted nematode that has been reported from several primate species in Africa and Asia, and has been estimated to infect hundreds of millions of people worldwide, although no precise estimates are available. Here we describe a case of infection with a cryptic species of Strongyloides in a Bornean (Philippine) slow loris (Nycticebus menagensis) living within a diverse community of several primate species in the Lower Kinabatangan Wildlife Sanctuary, Malaysian Borneo. Fresh fecal samples were collected from five primate species and nematode larvae cultured from these samples were selected for phylogenetic analyses. Sequences obtained for most larvae were identified as S. fuelleborni, grouping into three different clusters and showing no aggregation within specific hosts or geographic location. In contrast, a set of parasite sequences obtained from a slow loris clustered closely with S. stercoralis into a different group, being genetically distinct to sequences reported from other primate hosts, humans included. Our results suggest that although S. fuelleborni infects all haplorrhines sampled in this primate community, a different species might be infecting the slow loris, the only strepsirrhine in Borneo and one of the least studied primates in the region. Although more data are needed to support this conclusion, we propose that Strongyloides species in primates might be more diverse than previously thought, with potential implications for ecological and evolutionary host-parasite associations, as well as epidemiological dynamics. Keywords: Strongyloides, Nycticebus menagensis, Cryptic species, Host-parasite interactions, Malaysian Borneo

Global population expansion has increased interactions and conflicts between humans and nonhuman primates over shared ecological space and resources. Such ecological overlap, along with our shared evolutionary histories, makes human-nonhuman primate interfaces hot spots for the acquisition and transmission of parasites. In this chapter, we bring to light the importance of human-macaque interfaces in particular as hot spots for infectious disease ecological and epidemiological assessments. We first outline the significance and broader objectives behind research related to the subfield of primate infectious disease ecology and epidemiology. We then reveal how members of the genus Macaca, being among the most socioecologically flexible and invasive of all primate taxa, live under varying degrees of overlap with humans in anthropogenic landscapes. Thus, human-macaque interfaces may favor the bidirectional exchange of parasites. We then review studies that have isolated various types of parasites at human-macaque interfaces, using information from the Global Mammal Parasite Database (GMPD: http://www.mammalparasites.org/). Finally, we elaborate on avenues through which the implementation of both novel conceptual frameworks (e.g., Coupled Systems, One Health) and quantitative network-based approaches (e.g., social and bipartite networks, agent-based modeling) may potentially address some of the critical gaps in our current knowledge of infectious disease ecology at human-primate interfaces.

Objectively measuring the effects of parasitism on animal health is challenging, especially in the wild. Analyses of behavioural organization are increasingly used for this purpose, to identify animals in pathological or otherwise challenged states. Here, we investigated the possible impact of gastrointestinal helminth infection on the behaviour of wild chimpanzees, Pan troglodytes schweinfurthii, by applying fractal analysis to their feeding patterns. We predicted that higher intensity of strongylid infection should be associated with altered organizational complexity in temporal sequences of behaviour. We observed 15 habituated male chimpanzees in Kalinzu Reserve Forest, Uganda, and collected behavioural time series via focal animal sampling. We quantified the number of strongylid eggs per gram of faecal sediment using a modified simple sedimentation method to estimate the intensity of infection with strongylid nematodes. We used detrended fluctuation analysis (DFA) to explore long-range dependence in binary sequences of feeding behaviour as an index of organizational complexity along a stochastic-deterministic gradient. We then built several generalized linear mixed models to examine the relationship between behavioural organization and strongylid infection. Our results indicate that chimpanzee feeding sequences are long-range dependent and antipersistent, i.e. short bouts tended to be followed by long bouts and vice versa. Furthermore, the complexity of chimpanzee feeding sequences and the intensity of infection with strongylid nematodes were positively related: individuals with more intense infections exhibited more stochastic feeding sequences. In contrast, more conventional analyses did not reveal any relationship between parasitism and chimpanzee behaviour, nor did a survival analysis find variation in the probability of switching between behaviour states across chimpanzees with varying infection phenotypes. This work suggests that strongylid nematodes do pose a challenge for wild chimpanzees, manifest as altered organizational complexity in behaviour sequences, and provides further evidence that fractal analyses can have a valuable role in animal health monitoring.

International audience; Animals have evolved a wide range of behaviours that act as barriers to decrease the risk of parasite infection. Faecal avoidance may, for example, limit contact with orofaecally transmitted parasites, such as gastrointestinal nematodes. When present in faeces, however, nematode eggs need to mature before reaching their infective stage. If strategies have evolved in hosts to specifically avoid nematodes, old faeces with infective larvae should elicit stronger avoidance behaviour than fresh faeces that contain noninfective stages. Here, we carried out two experiments to test the hypothesis that mandrills, Mandrillus sphinx, an Old-World primate, exhibit specific behavioural strategies to avoid nematode infection. Our results show that individuals did not avoid faeces in a nonfeeding context but did avoid eating food items contaminated with faecal material, females more so than males. However, neither the presence of nematodes nor the age of faeces influenced the level of avoidance observed, suggesting that mandrills avoid faecal material in general rather than nematodes specifically when foraging.

Social structure can theoretically regulate disease risk by mediating exposure to pathogens via social proximity and contact. Investigating the role of central individuals within a network may help predict infectious agent transmission as well as implement disease control strategies, but little is known about such dynamics in real primate networks. We combined social network analysis and a modeling approach to better understand transmission of a theoretical infectious agent in wild Japanese macaques, highly social animals which form extended but highly differentiated social networks. We collected focal data from adult females living on the islands of Koshima and Yakushima, Japan. Individual identities as well as grooming networks were included in a Markov graph-based simulation. In this model, the probability that an individual will transmit an infectious agent depends on the strength of its relationships with other group members. Similarly, its probability of being infected depends on its relationships with already infected group members. We correlated: (i) the percentage of subjects infected during a latency-constrained epidemic; (ii) the mean latency to complete transmission; (iii) the probability that an individual is infected first among all group members; and (iv) each individual's mean rank in the chain of transmission with different individual network centralities (eigenvector, strength, betweenness). Our results support the hypothesis that more central individuals transmit infections in a shorter amount of time and to more subjects but also become infected more quickly than less central individuals. However, we also observed that the spread of infectious agents on the Yakushima network did not always differ from expectations of spread on random networks. Generalizations about the importance of observed social networks in pathogen flow should thus be made with caution, since individual characteristics in some real world networks appear less relevant than they are in others in predicting disease spread. Am. J. Primatol. 78:767-779, 2016. © 2016 Wiley Periodicals, Inc.

Ethnopharmacological relevance Primates forage on a variety of plant parts to balance their dietary intake to meet requirements of energy, nutrition and maintenance, however the reason(s) leading them to ingest some plants which have no nutritional value and/or contain bioactive or even toxic secondary metabolites is recently gaining closer attention. The growing literature suggests that primates consume plants for medicinal purposes (self-medication) as well, particularly when infected with parasites and pathogens (bacteria, viruses, microbes). Interestingly, some of the plants they consume are also used by humans for similar purposes or may have potential uses for humans. Materials and methods As part of a 16-month study of the parasite ecology of a sub-species of Japanese macaques (Macaca fuscata yakui) on the island of Yakushima, we surveyed their feeding habits and collected a subset of plants and plant parts observed being ingested by macaques. The ethnomedicinal value of these plants was surveyed and methanolic extracts of 45 plant parts were tested in vitro against important parasites of humans, including four protozoan parasites Plasmodium falciparum, Trypanosoma brucei rhodesiense, T. cruzi and Leishmania donovani, and the trematode flatworm Schistosoma mansoni. Potential toxicity of the extracts was also assessed on mammalian cells. Results A wide range of ethnomedicinal uses in Asia for these plants is noted, with 37% associated with the treatment of parasites, pathogens and related symptoms. Additionally, the 45 extracts tested showed broad and significant activity against our test organisms. All extracts were active against T. b. rhodesiense. The majority (over 80%) inhibited the growth of P. falciparum and L. donovani. Half of the extracts also displayed antiprotozoal potential against T. cruzi while only several extracts were active against both larval and adult stages of S. mansoni. Cytotoxicity was generally low, although several extracts lacked specific toxicity to test parasites. Conclusions Our results indicated a number of plants and their parts to have antiparasitic activity not previously reported in the ethnopharmacological literature. Enhanced understanding of the primate diets, particularly during periods of intensified parasite infection risk may help to further narrow down plants of interest for lead compound development. The study of animal self-medication is a complementary approach, with precedence, to drug discovery of new lead drug compounds against human parasitic diseases.

Background Biological information about captive Japanese macaques, including hematology and blood chemistry, is still lacking despite the fact that ethological and ecological data have accumulated during decades of field research. Methods Hematological (511 examinations of 280 Japanese macaques) and blood chemistry data (between 33 and 284 examinations from between 29 and 257 individual macaques) in clinically healthy, simian retrovirus-free Japanese macaques tested between 2009 and 2013 were reviewed. Results and conclusions Specific hematological and blood chemistry data for Japanese macaques without clinical signs of disease were provided in this study. Averages presented can be used as hematological parameters for Japanese macaques. Some differences between Japanese macaques and other closely related macaque species were found. Some parameters varied according to macaque age and sex, as well as regional origin. The data in this study will provide useful clinical indices for Japanese macaques in captive and similar conditions.

In myriad biological systems, multiple lines of evidence indicate that modularity, wherein parts of a network are organized into modules such as subgroups in animal networks, may affect social transmission processes. In animal societies, there is increased interest in understanding variation in the effects of modularity on transmission as it may provide important insight into a given network’s performance, in addition to the evolutionary consequences the structure of the network may have for individual fitness. Yet, to our knowledge, the degree to which network efficiency is modularity dependent has not yet been investigated in great detail in behavioral and evolutionary ecology. Here, we investigated to what degree network efficiency, as a proxy for social transmission, is modularity dependent. We created 2798 networks varying in group size and density, and tested whether network structure (density, Newman’s modularity, eigenvector centralization) and group size shape network efficiency. We also used published data from 41 primate social networks to test whether the predictions generated in our simulations were supported by empirical observations. Our results show a non-linear relationship between modularity and global efficiency, with the latter peaking at intermediate values of modularity in both theoretical and empirical networks. This phenomenon may have relevance for observed variation in social structure and its link with network performance. Our results may thus provide a basis from which to discuss the evolution of complex systems such as animal societies. Networks may maximize performance and minimize transmission costs, as demonstrated in neural networks, but to what degree network efficiency is modularity dependent has not yet been investigated in behavioral ecology. We provide evidence that modularity, such as subgrouping in animal networks, can have non-linear effects on transmission processes, with low values of modularity tending to positively influence social transmission and high values tending to negatively influence transmission. This pattern was consistent across small, medium, and large social groups from theoretical networks, and was corroborated by our empirical networks which were derived from 41 small- to medium-sized groups of 15 primate species. These results have potential implications for the understanding of social flexibility and its link with network performance, in addition informing many interdisciplinary fields, such as communication and computer science.

Threats from parasites and pathogens are ubiquitous, and many use pathways that exploit host trophic interactions for their transmission. As such, host organisms have evolved a behavioural immune system to facilitate contamination-risk assessment and avoidance of potential contaminants in various contexts, including feeding. Detecting pathogen threats can rely on different sensory modalities allowing animals to screen for a wide array of contaminants. Here, we present a series of experiments in which bonobos showed clear avoidance of contaminated food items, and were sensitive to risk along a contamination probability gradient. Across experiments, bonobos appeared to use multisensorial cues to inform their feeding decisions. In addition, bonobos showed reduced tactile, gustatory and tool use activities when in the presence of contaminant versus control odours in a challenging foraging context. Our experiments build on previous work conducted in Japanese macaques and chimpanzees aiming at a better understanding of the ways in which the behavioural immune system operates in primates.This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.

This study was financially supported by the following institutions: the WWF-UK through R. Downie, the Japanese Mombukagakusho and the Japanese Society for the Promotion of Science, the Zone Atelier Antarctique et Subantarctique –LTER France of the CNRS. The Southern Ocean is currently experiencing major environmental changes, including in sea‐ice cover. Such changes strongly influence ecosystem structure and functioning and affect the survival and reproduction of predators such as seabirds. These effects are likely mediated by reduced availability of food resources. As such, seabirds are reliable eco‐indicators of environmental conditions in the Antarctic region. Here, based on 9 years of sea‐ice data, we found that the breeding success of Adélie penguins (Pygoscelis adeliae) reaches a peak at intermediate sea‐ice cover (ca. 20%). We further examined the effects of sea‐ice conditions on the foraging activity of penguins, measured at multiple scales from individual dives to foraging trips. Analysis of temporal organisation of dives, including fractal and bout analyses, revealed an increasingly consistent behaviour during years with extensive sea‐ice cover. The relationship between several dive parameters and sea‐ice cover in the foraging area appears to be quadratic. In years of low and high sea‐ice cover, individuals adjusted their diving effort by generally diving deeper, more frequently and by resting at the surface between dives for shorter periods of time than in years with intermediate sea‐ice cover. Our study therefore suggests that sea‐ice cover is likely to affect the reproductive performance of Adélie penguins through its effects on foraging behaviour, as breeding success and most diving parameters share a common optimum. Some years, however, deviated from this general trend, suggesting that other factors (e.g. precipitation during the breeding season) might sometimes become preponderant over the sea‐ice effects on breeding and foraging performance. Our study highlights the value of monitoring fitness parameters and individual behaviour concomitantly over the long‐term to better characterize optimal environmental conditions and potential resilience of wildlife. Such an approach is crucial if we want to anticipate the effects of environmental change on Antarctic penguin populations. Postprint

International audience; Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher‐order aspects of female macaque (genus: Macaca ) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely‐related species. We use a social network approach to describe higher‐order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species‐typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex‐ratio, and current living condition (captive vs. free‐living). We assembled 34–38 datasets of female‐female dyadic aggression and allogrooming among captive and free‐living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate‐strong phylogenetic signals in dominance traits, but moderate‐weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely‐connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

International audience; Spatial scale-invariant Lévy walk (power-law) patterns seem common among animals that move continually during searching. Scaling laws also describe well the spontaneous patterns of waiting times of sit-and-wait ambush predators, which show random ‘burstiness’ that appears scale-invariant across a broad set of scales. The occurrence of these scaling laws has been attributed to stochastic decision-based queuing processes. Taken together these various studies suggest that stochastic decision-based queuing processes may apply more generally across taxa with divergent foraging strategies, ranging from highly mobile pursuit predators to the less mobile ambush predators. Here we provide support for this proposition by demonstrating that simple stochastic priority processes capture accurately the timings of dives made by little penguins, Eudyptula minor, in their natural habitat, whose use of space and time falls between that of sit-and-wait predators and Lévy walkers.

Bats that typically forage in the forest understorey can be difficult to capture using mist nets or harp traps alone. We assessed the effectiveness of an ultrasonic lure for increasing capture rates of vespertilionid bats in two forest zones in Japan. One sequence of stimuli was modelled on social calls of four species that typically forage in narrow-space; the other on those of four species that forage along edges and in forest gaps. The lure increased capture rates by 24.5 times in cool temperate deciduous forest in Hokkaido, and 9.75 times in warm temperate evergreen rain forest in Yakushima, compared with the control condition. Narrow-space foraging bats of the genus Murina dominated the catch at both sites and were caught most frequently when the trap was located in the cluttered environment of the forest understorey. There was no significant effect of call type on capture rate. The lure is an effective method for increasing capture rates of bats and particularly for narrow-space foraging s...