A critical assessment of two species distribution models: a case study of the vervet monkey (Cercopithecus aethiops)

Aim Species distribution models are invaluable tools in biogeographical, ecological and applied biological research, but specific concerns have been raised in relation to different modelling techniques in terms of their validity. Here we compare two fundamentally different approaches to species distribution modelling, one based on simple occurrence data where the lack of an ecological framework has been criticized, and the other firmly based in socio‐ecological theory but requiring highly detailed behavioural information that is often limited in availability. Location (Sub‐Saharan) Africa. Methods We used two distinct techniques to predict the realized distribution of a model species, the vervet monkey (Cercopithecus aethiops Linnaeus, 1758). A maximum entropy model was produced taking 13 environmental variables and presence‐only data from 174 sites throughout Africa as input, with an additional 58 sites retained to test the model. A time‐budget model considering the same environmental variables was constructed from detailed behavioural data on 20 groups representing 14 populations, with presence‐only data from the remaining 218 sites reserved to test model predictions on vervet monkey occurrence. Both models were further validated against a reference species distribution map as drawn up by the African Mammals Databank. Results Both models performed well, with the time budget and maximum entropy algorithms correctly predicting vervet monkey presence at 78.4% and 91.4% of their respective test sites. Similarly, the time‐budget model correctly predicted presence and absence at 87.4% of map pixels against the reference distribution map, and the maximum entropy model achieved a success rate of 81.8%. Finally, there was a high level of agreement (81.6%) between the presence–absence maps produced by the two models, and the environmental variables identified as most strongly driving vervet monkey distribution were the same in both models. Main conclusions The time‐budget and maximum entropy models produced accurate and remarkably similar species distribution maps, despite fundamental differences in their conceptual and methodological approaches. Such strong convergence not only provides support for the credibility of current results, but also relieves concerns about the validity of the two modelling approaches.     

Composition and stability of the vervet monkey milk microbiome

The human milk microbiome is vertically transmitted to offspring during the postnatal period and has emerged as a critical driver of infant immune and metabolic development. Despite this importance in humans, the milk microbiome of nonhuman primates remains largely unexplored. This dearth of comparative work precludes our ability to understand how species‐specific differences in the milk microbiome may differentially drive maternal effects and limits how translational models can be used to understand the role of vertically transmitted milk microbes in human development. Here, we present the first culture‐independent data on the milk microbiome of a nonhuman primate. We collected milk and matched fecal microbiome samples at early and late lactation from a cohort of captive lactating vervet monkeys (N = 15). We found that, similar to humans, the vervet monkey milk microbiome comprises a shared community of taxa that are universally present across individuals. However, unlike in humans, this shared community is dominated by the genera Lactobacillus, Bacteroides, and Prevotella. We also found that, in contrast to previous culture‐dependent studies in humans, the vervet milk microbiome exhibits greater alpha‐diversity than the gut microbiome across lactation. Finally, we did not find support for the translocation of microbes from the gut to the mammary gland within females (i.e., “entero‐mammary pathway”). Taken together, our results show that the vervet monkey milk microbiome is taxonomically diverse, distinct from the gut microbiome, and largely stable. These findings demonstrate that the milk microbiome is a unique substrate that may selectively favor the establishment and persistence of particular microbes across lactation and highlights the need for future experimental studies on the origin of microbes in milk.     

Gut microbiota in wild and captive Guizhou snub‐nosed monkeys,Rhinopithecus brelichi

Many colobine species—including the endangered Guizhou snub‐nosed monkey (Rhinopithecus brelichi) are difficult to maintain in captivity and frequently exhibit gastrointestinal (GI) problems. GI problems are commonly linked to alterations in the gut microbiota, which lead us to examine the gut microbial communities of wild and captive R. brelichi. We used high‐throughput sequencing of the 16S rRNA gene to compare the gut microbiota of wild (N = 7) and captive (N = 8) R. brelichi. Wild monkeys exhibited increased gut microbial diversity based on the Chao1 but not Shannon diversity metric and greater relative abundances of bacteria in the Lachnospiraceae and Ruminococcaceae families. Microbes in these families digest complex plant materials and produce butyrate, a short chain fatty acid critical to colonocyte health. Captive monkeys had greater relative abundances of Prevotella and Bacteroides species, which degrade simple sugars and carbohydrates, like those present in fruits and cornmeal, two staples of the captive R. brelichi diet. Captive monkeys also had a greater abundance of Akkermansia species, a microbe that can thrive in the face of host malnutrition. Taken together, these findings suggest that poor health in captive R. brelichi may be linked to diet and an altered gut microbiota.     

Dopamine Gates Visual Signals in Monkey Prefrontal Cortex Neurons

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The Thatcher illusion in humans and monkeys

Primates possess the remarkable ability to differentiate faces of group members and to extract relevant information about the individual directly from the face. Recognition of conspecific faces is achieved by means of holistic processing, i.e. the processing of the face as an unparsed, perceptual whole, rather than as the collection of independent features (part-based processing). The most striking example of holistic processing is the Thatcher illusion. Local changes in facial features are hardly noticeable when the whole face is inverted (rotated 180°), but strikingly grotesque when the face is upright. This effect can be explained by a lack of processing capabilities for locally rotated facial features when the face is turned upside down. Recently, a Thatcher illusion was described in the macaque monkey analogous to that known from human investigations. Using a habituation paradigm combined with eye tracking, we address the critical follow-up questions raised in the aforementioned study to show the Thatcher illusion as a function of the observer''s species (humans and macaques), the stimulus'' species (humans and macaques) and the level of perceptual expertise (novice, expert).     

Food distribution,dominance, and aggressive behaviors in bonnet macaques

Resource availability or distribution may affect interindividual competition in species such as primates, which forage in social groups, and several field studies suggest that dominance status predicts access to restricted food sources. Increased competition due to restricted resources may result in the intensification of aggressive behaviors. The study reported here examines the impact of manipulation of the distribution of food resources in a laboratory-housed group of bonnet macaques to assess the impact of distribution on aggressive behaviors. Food was restricted to a space which allowed access to only one or two individuals at a time or was dispersed throughout the living enclosure to allow universal access in alternating periods. During periods of clumped distribution, the monkeys obtained access to the food in order of their dominance status in the group. In addition, overall levels of aggressive behaviors increased, submissive behavior increased, and play decreased during periods of clumped distribution of food. These results confirm the findings from field studies indicating increases in agonism with restriction of food resources. These findings also have implications for primate colony management, in terms of developing strategies for minimizing intragroup aggression in captive groups.     

Menopause in female rhesus monkeys

Fifteen female rhesus monkeys (Macaca mulatto), ranging in age from 8 to 34 years, were studied for one year to characterize the endocrine and menstrual changes associated with menopause in this species. Five monkeys were premenopausal; these younger monkeys, ages 8–11 years, menstruated and showed cyclic ovarian activity during the 12–month study period, as evidenced by menses and periodic elevations of serum estradiol (E₂) and luteinizing hormone (LH) concentrations. Four females, ages 24–26 years, were in transition to menopause. Two of these perimenopausal females menstruated and secreted E₂ and LH in a periodic fashion; the other two females showed elevated LH concentrations, consistently low E₂ levels, and no evidence of menstruation. Six females, ages 27–34 years, were clearly postmenopausal; LH concentrations were high, whereas E₂ concentrations were uniformly low. There was a significant inverse correlation between basal E₂ concentrations and age, and a significant positive correlation between age and LH concentrations across all 15 animals. Hormonal changes indicative of ovulation, when they occurred, were generally restricted to the winter and early spring months. Histological analysis of ovaries from four postmenopausal females revealed little or no evidence of active folliculogenesis. These data indicate that menopause in female rhesus monkeys does not occur until the second half of thethird decade of life. © 1995 Wiley-Liss, Inc.     

Seasonal variation in the positional behavior of red howling monkeys (Alouatta seniculus)

Recent studies on the positional behavior of primates reveal that significant seasonal variation occurs in both locomotion and postures that is related to changes in diet and foraging techniques. Howling monkeys (genusAlouatta), which also have a seasonally varied diet, are predicted to have correspondingly varied positional behaviors. Two groups of red howling monkeys were studied in a primary rain forest in French Guinana during the dry and wet seasons. During the dry season, when howler diet is based mainly on leaves, howlers traveled more frequently by quadrupedal walking on large supports, a mode of progression that is probably inexpensive energetically and relatively stable. During feeding, quadrupedal and tripedal stand contributed considerably, a posture probably associated with the equal distribution of leaves within a tree crown. In contrast, during the wet season, when fruit was abundant, howlers fed very frequently by sitting on large supports, probably because fruit consumption required more time for special manipulation. However, most seasonal changes in feeding postures, and in travel and feeding locomotion, were difficult to associate directly with dietary shifts. These behavioral changes may be more highly correlated with slight modifications in microhabitat use (horizontal and vertical daily ranges, similar and alternative arboreal pathways) that are not considered in this paper.