Predicting future climate change impacts on the potential distribution of the black howler monkey (Alouatta pigra): an endangered arboreal primate.

Climate change is one of the main factors affecting biodiversity worldwide at an alarming rate. In addition to increases in global extreme weather events, melting of polar ice caps, and subsequent sea level rise, climate change might shift the geographic distribution of species. In recent years, interest in understanding the effects of climate change on species distribution has increased, including species which depend greatly on forest cover for survival, such as strictly arboreal primates. Here, we generate a series of species distribution models (SDMs) to evaluate future projections under different climate change scenarios on the distribution of the black howler monkey (Alouatta pigra), an endemic endangered primate species. Using SDMs, we assessed current and future projections of their potential distribution for three Social Economic Paths (SSPs) for the years 2030, 2050, 2070, and 2090. Specifically, we found that precipitation seasonality (BIO15, 30.8%), isothermality (BIO3, 25.4%), and mean diurnal range (BIO2, 19.7.%) are the main factors affecting A. pigra distribution. The future climate change models suggested a decrease in the potential distribution of A. pigra by projected scenarios (from - 1.23 to - 12.66%). The highly suitable area was the most affected above all in the more pessimist scenario most likely related to habitat fragmentation. Our study provides new insights into the potential future distribution and suitable habitats of Alouatta pigra. Such information could be used by local communities, governments, and non-governmental organizations for conservation planning of this primate species.

Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.).

The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.

The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra).

Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free-ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health-related consequences from the parasite-microbiome interplay.

Natural diets promote retention of the native gut microbiota in captive rodents.

Wild animals entering captivity experience radical lifestyle changes resulting in microbiome alterations. However, little is known about the factors that drive microbial community shifts in captivity, and what actions could mitigate microbial changes. Using white-throated woodrats (Neotoma albigula), we tested whether offering natural diets in captivity facilitates retention of native microbial communities of captive animals. Wild-caught woodrats were brought to laboratory conditions. Woodrats received either a natural diet of Opuntia cactus or an artificial diet of commercial chow over three weeks. Microbial inventories from woodrat feces at the time of capture and in captivity were generated using Illumina 16S rRNA sequencing. We found that providing woodrats with wild-natural diets significantly mitigated alterations in their microbiota, promoting a 90% retention of native microbial communities across the experiment. In contrast, the artificial diet significantly impacted microbial structure to the extent that 38% of the natural microflora was lost. Core bacteria including Bifidobacterium and Allobaculum were lost, and abundances of microbes related to oxalate degradation decreased in individuals fed artificial but not natural diets. These results highlight the importance of supplementing captive diets with natural foods to maintain native microbiomes of animals kept in artificial conditions for scientific or conservation purposes.

The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra).

Parasitic infections in wildlife are shaped by host-related traits including individual reproductive condition. It has been argued that female primates are more susceptible to infectious diseases during pregnancy due to short-term changes in immune function that result in reduced ability to combat infections. Likewise, lactation, which is the most energetically expensive state, may affect immunity and infection risk due to tradeoffs between milk production and maintenance of immune function. Here, we examine the degree to which parasite prevalence and parasite richness are affected by female reproductive condition and stress levels in wild female black howler monkeys (Alouatta pigra). Over the course of one year, we collected fresh fecal samples from 15 adult females belonging to seven black howler groups living in Escárcega, Mexico. Fecal samples were used for parasitological analysis and for measuring fecal glucocorticoid metabolites (i.e., stress biomarker). We found that the prevalence of intestinal parasites and parasite richness did not differ among non-pregnant, pregnant, and lactating females. Fecal glucocorticoid metabolite levels increased significantly during pregnancy and during the first month of lactation, and positively predicted the probability of Controrchis biliophilus infection. Parasite prevalence and richness decreased during the months of increased rainfall. We conclude that reproductive physiology has limited consequences on intestinal parasitic infection risk in female black howler monkeys and that seasonal environmental fluctuations have greater effects.

Fluctuations in daily energy intake do not cause physiological stress in a Neotropical primate living in a seasonal forest.

Animals may face periods of nutritional stress due to short-term food shortage and/or low energy consumption associated with seasonal fluctuations in resource availability. We tested the hypothesis that periods of restricted macronutrient and energy intake result in energy deficits and physiological stress in wild black howler monkeys (Alouatta pigra) inhabiting seasonal tropical semi-deciduous forests. We conducted full-day follows of focal animals recording feeding rates, time spent feeding, and total amount of food ingested. We carried out nutritional analysis of foods collected from feeding trees and calculated the daily nutrient and energy intake of each focal individual. Fecal glucocorticoid metabolites (fGCM) of focal animals were used as an indicator of physiological stress. We found that fluctuations in daily energy intake across seasons did not have significant effects on fGCM of individuals. However, protein intake was negatively associated with fGCM, highlighting the interplay among macronutrients, metabolism, and the endocrine system. Fecal glucocorticoid metabolites were also positively related to fruit availability, but this relationship was most likely due to social stress associated with intergroup encounters and resource defense that occurred when preferred trees were fruiting. Behavioral strategies such as dietary shifts and nutrient mixing, and metabolic adaptations such as low energy expenditure allowed individuals to fulfill their minimum energy requirements even during periods of decreased resource availability and intake. The present study suggests that seasonal variations in food, macronutrient, and energy acquisition may have limited physiological costs for animals that exploit different types of plant resources such as howler monkeys.

Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species.

Recent studies suggest that variation in diet across time and space results in changes in the mammalian gut microbiota. This variation may ultimately impact host ecology by altering nutritional status and health. Wild animal populations provide an excellent opportunity for understanding these interactions. However, compared to clinical studies, microbial research targeting wild animals is currently limited, and many published studies focus only on a single population of a single host species. In this study we utilize fecal samples from two species of howler monkey (Alouatta pigra and A. palliata) collected at four sites to investigate factors influencing the gut microbiota at three scales: taxonomic (host species), ecosystemic (forest type), and local (habitat disturbance/season). The results demonstrate that the effect of host species on the gut microbiota is stronger than the effect of host forest type, which is stronger than the effect of habitat disturbance or seasonality. Nevertheless, within host species, gut microbiota composition differs in response to forest type, habitat disturbance, and season. Variations in the effect size of these factors are associated both with host species and environment. This information may be beneficial for understanding ecological and evolutionary questions associated with Mesoamerican howler monkeys, as well as determining conservation challenges facing each species. These mechanisms may also provide insight into the ecology of other species of howler monkeys, non-human primates, and mammals.

Sexual conflict in primates.

Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for delineating variation in primate behavior and morphology. The goals of this review are to highlight the rapidly rising field of sexual conflict and the ongoing shift in our understanding of interactions between the sexes. We discuss the evidence for sexual conflict within the Order Primates, and assess how studies of primates have illuminated and can continue to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest directions for future research.