Gut microbiome is actively involved in multiple physiological processes of the animals, including accessing nutrients and maintaining health. Although knowledge on functional impact of gut microbiome has increased greatly in the past decades, our understanding of the mechanisms governing the ecology and evolution of gut microbiome remains obscure. The gut microbiome is potentially affected by factors relating to the hosts (e.g. digestive system, phylogeny) and the environment (e.g. season, habitat type, interactions with sympatric animals of the same and different species). Many previous studies have revealed that mammalian microbiome strongly correlates with host phylogenetic relationship and digestive system, indicating co-divergence of gut microbiome with the host specific characteristics. However, there has been debate about the influence of host phylogeny on gut microbiome comparing to the environmental factors. Since mammals must acquire gut microbes from the outside environment, differences in diet, local habitat and other environmental factors could substantially alter gut microbiome. One way to disentangle the effects of environmental factors on gut microbiome from the host-related factors is to compare gut microbiome of closely related species living sympatrically and allopatrically. Using 16S rRNA Illumina sequencing, we investigated the gut microbiome of 15 primate species living in Moukalaba-Doudou National Park, Gabon and Kibale National Park, Uganda. Utilizing matrix and topological comparisons, we assessed the relative role of host phylogeny, digestive system (colobus/non-colobus), substrate use (arboreal/ terrestrial) and sharing of habitats (geographic distance) in influencing microbiome composition of the nonhuman primates. In particular, weighted UniFrac was found correlated with host phylogeny, digestive system and geographic distance, whereas unweighted UniFrac was found unrelated with any of the factors tested. Overall, our result revealed that in addition to the host-related factors, habitat sharing also played a nonnegligible role in determining gut microbiome composition. This study contributes to a deeper understanding the underlying mechanism governing the ecology and evolution of gut microbiome.
Fecal particle size is a measurement of the result of chewing. It provides important information about the feeding and digestion of herbivores. Understanding the effects of the potential proximate determinants, such as age, sex, and dietary toughness, on fecal particle size helps us interpret this widely used measurement, but have not been extensively investigated, especially in primates. This study aims to clarify how these factors influence fecal particle size in omnivorous Yakushima Japanese macaques. We simultaneously documented their diet, food toughness, and fecal particle size in the lowland area of Yakushima in the period from March 2018 to April 2019. Fecal particle size showed limited differences across months and no difference among age-sex classes. Dietary toughness showed no effects on fecal particle size, while only the consumption of fruits showed a marginally significant negative effect. Our data indicate that food toughness did not limit food comminution in our study subjects, while no age-sex class showed a difference in chewing ability. The lack of variation might derive from a less tough diet compared to the gelada, in which an effect of toughness on fecal particle size was found. These results suggest that food comminution is less variable in frugivores and omnivores primates compare to highly specialized species (such as geladas). This study showed dietary toughness, age and sex differences not always result in fecal particle size variations in frugivores and omnivores species, while the physical structure of foods should be considered during interpreting relevant results.
Despite the contrasting niches during daytime and nighttime, few primates called cathemeral exhibit significant activity distributed over the 24-h. The main hypotheses suggested as the adaptive significance of cathemerality were thermoregulation strategy to avoid heat/cold stress, antipredator strategy to avoid diurnal raptor, feeding strategy to fill energy requirement by feeding fibrous food over 24-h during periods of fruits scarcity. Few studies tested together these hypotheses and found that feeding strategy appeared to be the strongest factors determinants of cathemerality in Eulemur (Donati et al 2011 Animal behav). However, this was a controversial hypothesis for cathemeral lemurs, Hapalemur, that could digest fiber (Eppley et al 2017 Behav Ecol Sociobiol). A study featuring Eulemur did not support also this hypothesis (Curtis et al. 1999 Amer J Primatol). We previously found that cathemerality in dry forest in Ankarafantsika is probably a strategy for maintaining water-balance on days of high ambient temperatures and dry condition (Razanaparany and Sato 2020 Folia Primatol). Therefore, we tested the hypotheses postulated as the adaptive significance of cathemerality in the brown lemurs in dry forest in northwestern Madagascar. We followed two groups of (Common brown lemur) Eulemur fulvus all-day and all-night, over 9 months, equality distributed two seasons. As brown lemurs were hypothesized to shift into nocturnal during defoliation periods to avoid diurnal raptors, we determined the canopy openness and use the data as a proxy of exposure to raptors. We assessed the fiber intake, water intake from food and metabolizable energy intake. We found that the diurnal activity level of the brown lemurs decreased on days of lower humidity, higher ambient temperatures, and closer canopy cover by leaves. Their nocturnal activity level increased with their energy intakes and during defoliation periods. Our results supported that cathemerality is probably thermoregulation to cope with the heat stress, an anti-predator strategy to avoid the diurnal raptors. As canopy cover and humidity are likely linked to the water availability, these results also suggest that cathemerality is probably a strategy to cope with dry/heat stresses in the daytime and ensuring the energy intake during the night. Water accessibility would explain the increase of their diurnal activity during hot daytime and the decrease of nocturnal activity level and nocturnal energy intake at night in the wet season.
Pathogen transmission is a key issue in both public health and wildlife conservation. Predicting pathogen transmission using social network analysis (SNA) has been trending upward following numerous studies of wildlife showing positive relationships between an individual’s social network centrality (a measurement of its importance in a network) and its probability or degree of infection; including in macaques. Based on this work, we aimed to test whether social network centrality can predict parasite infection in different macaque species and populations. We constructed 4 data sets based on behavioral observations and parasitological investigation using 2 groups each of rhesus macaques (Macaca mulatta) and Japanese macaques (Macaca fuscata). We modeled the relationship between social network centrality and intestinal parasite infection intensity in each group and compared the results among them. We also conducted simulations to control for the effect of sample size (i.e. number of fecal samples for parasitology) on the determined relationship. Generalized linear mixed models suggest a positive relationship between centrality and infection in only one macaque population (Japanese macaques of Koshima). Simulations show that small sample size was unlikely to have affected our results. Overall, our results suggest that social network centrality does not generally predict parasite infection across species and populations, which may relate more strongly to the various local ecologies of the studied groups. However, we cannot rule out the possible influence of seasonality in our study because our data were collected at each site in different seasonal conditions. Furthermore, human influences such as degree of provisioning and population management may also play a role. Ultimately, this work emphasizes the importance of understanding the mechanisms underlying transmission and how they might vary across populations and groups when attempting to relate social factors to infection.
Human receive information not only through direct experience but also through referential media such as videos. Human experience is largely expanded by the ability to utilize information which refer to particular events and objects that are out-ofsight. Such referential information can be conveyed through videos in human older than 4-year-old (DeLoache 1987). It is also known that the same age of children start to understand referential function of language and thus language acquisition may facilitate the understanding of referential function of media (Flavell et al 1990; Perner 1991). However, it is unclear whether and to what extent such referential competence is shared in nonlinguistic animals. To address this, we tested whether chimpanzees (Pan troglodytes) can garner video information about relevant events, which is not directly observed (here, food being hidden in the next room) and, if so, what factors may facilitate their usage of referential information process. Five chimpanzees first observed food-hiding in one room. A half banana was baited into one of the two cups (green/red) by an experimenter. Chimpanzee then moved to the next room received a choice test. Foodhiding was demonstrated either directly in front of them (Real condition) or through video (Video condition). Two individuals performed better than chance in both conditions suggests that chimpanzees may share the ability to acquire information based on referential media–referent association with humans. Conversely, the remaining three individuals failed in both conditions suggests that spatial dissociation and/or temporal delay between observation and choice test may be causes of failure. Future studies need to test if their understanding of referential function of video can be facilitated by improving task continuity in space and time.
Taste perception is fundamental in dietary selection for many animals. Bitter taste perception is important not only in dietary selection but also in preventing animals from ingesting potentially toxic compounds. Previous studies have revealed evolutionary divergence of the bitter taste receptor gene (TAS2R) repertoire in mammals, including primates, using publicly available whole genome sequence (WGS) data. Plant tissues contain more toxic compounds than animal tissues do. Herbivores could have less TAS2R genes because they are predicted to be more tolerant and less sensitive to bitter compounds to ingest poisons. On the other hand, herbivores could have more TAS2R genes because they are predicted to be in need of selecting and ingesting bitter plants which other animals avoid. Cercopithecid (African and Asian) monkeys are an excellent subject for studying adaptive evolution of bitter sensation because they have diverged into folivores (colobines) and omnivores (cercopithecines). However, only a few genera have been studied in this context. Dependence on WGS data is also potentially problematic due to its inherent incompleteness especially for multigene families such as TAS2Rs. In this study, we employed the target capture (TC) method specifically probing TAS2Rs followed by massive-parallel sequencing for nine cercopithecid species (seven cercopithecines: two Papio, two Macaca, one each of Cercopithecus, Chlorocebus and Erythrocebus species; two colobines: one each of Semnopithecus and Colobus species). We show that TC is far more effective than WGS in retrieving gene sequence and distinguishing intact and disrupted genes. We also find bitter taste gene composition differs among the species. Further studies are required to investigate whether difference of gene composition result in difference of receptor sensitivity and behavioral reactivity to bitter compounds.
The knowledge about how body parts are located and what they look like is important for species and individual discrimination in animals. In this study, we used eye-tracking to investigate whether chimpanzees have this body knowledge or not. We tested six chimpanzees and recorded their gaze behavior towards chimpanzee body stimuli. We focused on manipulations of arms or legs. For either arms or legs, there were four conditions. The first was normal bodies as a control. In the second condition, we misplaced one arm or a leg to a wrong position. In the third condition, we replaced an arm with a leg, or vice versa. In the fourth condition, we replaced an arm or a leg with a human arm or leg. The AOIs (areas of interest) were the strange body parts in the manipulated conditions or the corresponding ones in the control condition. We examined the number of trials in which chimpanzees had looked at the AOIs, the time to first fixation to AOIs, and the fixation duration of AOIs. Chimpanzees had more trials looking at the AOIs in the second and fourth conditions than control. Although there was no difference in the time to first fixation to AOIs across conditions, they had longer fixation durations in all manipulated conditions than control. The results showed that chimpanzees paid more attention to the strange body parts than control in general. This suggests that chimpanzees have the knowledge of the locations and appearances of body parts, as humans do, indicating that our common ancestor may have the knowledge about their body parts, too.