Habitat selection of an endangered primate, the samango monkey (Cercopithecus albogularis schwarzi): Integrating scales to prioritize habitat for wildlife management.

AIM: As habitat loss continues to accelerate with global human population growth, identifying landscape characteristics that influence species occurrence is a key conservation priority in order to prevent global biodiversity loss. In South Africa, the arboreal samango monkey (Cercopithecus albogularis sp.) is threatened due to loss and fragmentation of the indigenous forests it inhabits. The aim of this study was to determine the habitat preferences of the samango monkey at different spatial scales, and to identify key conservation areas to inform management plans for this species. LOCATION: This study was carried out in the western Soutpansberg Mountains, which represents the northernmost population of samango monkeys within South Africa, and the only endangered subspecies (C. a. schwarzi). METHODS: We used sequentially collected GPS points from two samango monkey groups followed between 2012 and 2017 to quantify the used and available habitat for this species within the western Soutpansberg Mountains. We developed 2nd-order (selection of ranging area), 3rd-order (selection within range), and 4th-order (feeding site selection) resource selection functions (RSFs) to identify important habitat features at each scale. Through scale integration, we identified three key conservation areas for samango monkeys across Limpopo Province, South Africa. RESULTS: Habitat productivity was the most important landscape variable predicting probability of use at each order of selection, indicating the dependence of these arboreal primates on tall-canopy indigenous forests. Critical habitat across Limpopo was highly fragmented, meaning complete isolation between subpopulations is likely. MAIN CONCLUSIONS: Understanding the habitat characteristics that influence samango monkey distribution across South Africa is crucial for prioritizing critical habitat for this species. Our results indicated that large, contiguous patches of tall-canopy indigenous forest are fundamental to samango monkey persistence. As such, protected area expansion of large forest patches and creation of forest corridors are identified as key conservation interventions for this species.

Normalized difference vegetation index, temperature and age affect faecal thyroid hormone concentrations in free-ranging African elephants.

Conservation biologists can use hormone measurements to assess animals' welfare, reproductive state, susceptibility to stressors, as well as energy expenditure. Quantifying hormone concentrations from faecal samples is particularly advantageous as samples can be collected without disturbing animals' behaviour. In order for an endocrine marker to be useful for wildlife managers, we need to understand how extrinsic and intrinsic factors affect hormone concentrations in free-ranging animal populations. Thyroid hormones are linked to basal metabolic rate and energy expenditure. Previous research demonstrated that triiodothyronine (T3) can be measured successfully in faecal matter of African elephants, Loxodonta africana. However, to our knowledge, research into factors affecting changes in elephant T3 levels has only been carried out in captive elephants so far. Thus, we present the first study of faecal T3 metabolite (mT3) concentrations of a large population of free-ranging African elephants. Over 15 months, we collected faecal samples from identified (n = 43 samples) and unidentified (n = 145 samples) individuals in Madikwe Game Reserve, South Africa. We investigated whether vegetative productivity [normalized difference vegetation index (NDVI)] in interaction with mean monthly temperature, age and sex affected mT3 concentrations. We found a significant negative interaction effect of NDVI and temperature. Increasing NDVI was related to higher concentrations of mT3, but increasing temperature was related to a decrease in mT3 concentrations in individually identified and unidentified elephants. In unidentified individuals, juvenile elephants had significantly higher mT3 concentrations compared to adult elephants. Faecal T3 can successfully be quantified in samples from free-ranging elephant populations and thus provides insight into energy expenditure in large herbivores.

Influence of food availability, plant productivity, and indigenous forest use on ranging behavior of the endangered samango monkey (Cercopithecus albogularis schwarzi), in the Soutpansberg Mountains, South Africa.

Understanding the determinants of ranging patterns in species susceptible to habitat fragmentation is fundamental for assessing their long-term adaptability to an increasingly human-dominated landscape. The aim of this study was to determine and compare the influence of ground-based food availability, remotely sensed plant productivity, and indigenous forest use on the ranging patterns of the endangered samango monkey (Cercopithecus albogularis schwarzi). We collected monthly ranging data on two habituated samango monkey groups, from February 2012 to December 2016, from our field site in the Soutpansberg Mountains, South Africa. We used linear mixed models to explore how food availability, plant productivity, and indigenous forest use influenced monthly ranging patterns, while controlling for group size, number of sample days and day length. We found that as more areas of high plant productivity (derived from remotely sensed EVI) were incorporated into the ranging area, both total and core monthly ranging areas decreased. In addition, both total ranging area and mean monthly daily path length decreased as more indigenous forest was incorporated into the ranging area. However, we found no effect of either ground-based food availability or remotely sensed plant productivity on ranging patterns. Our findings demonstrate the behavioral flexibility in samango monkey ranging, as samangos can utilize matrix habitat during periods of low productivity but are ultimately dependent on access to indigenous forest patches. In addition, we highlight the potential of using remotely sensed areas of high plant productivity to predict ranging patterns in a small ranging, forest-dwelling guenon, over ground-based estimates of food availability.

Adapting Methodology Used on Captive Subjects for Estimating Gut Passage Time in Wild Monkeys.

Gut passage time of food has consequences for primate digestive strategies, which subsequently affect seed dispersal. Seed dispersal models are critical in understanding plant population and community dynamics through estimation of seed dispersal distances, combining movement data with gut passage times. Thus, developing methods to collect in situ data on gut passage time are of great importance. Here we present a first attempt to develop an in situ study of gut passage time in an arboreal forest guenon, the samango monkey (Cercopithecus albogularis schwarzi) in the Soutpansberg Mountains, South Africa. Cercopithecus spp. consume large proportions of fruit and are important seed dispersers. However, previous studies on gut passage times have been conducted only on captive Cercopithecusspp. subjects, where movement is restricted, and diets are generally dissimilar to those observed in the wild. Using artificial digestive markers, we targeted provisioning of a male and a female samango monkey 4 times over 3 and 4 days, respectively. We followed the focal subjects from dawn until dusk following each feeding event, collecting faecal samples and recording the date and time of deposition and the number of markers found in each faecal sample. We recovered 6.61 ± 4 and 13 ± 9% of markers from the male and the female, respectively, and were able to estimate a gut passage window of 16.63-25.12 h from 3 of the 8 trials. We discuss methodological issues to help future researchers to develop in situ studies on gut passage times.

Social network changes during space restriction in zoo chimpanzees.

Several studies across anthropoid species have demonstrated how primates respond to the increased risk of conflict during space restriction with various behavioral strategies. Three strategies have been proposed relating to tension regulation, conflict avoidance, and inhibition. Prior research supporting these strategies has focused on individual- and dyadic-level analyses, yet group-living animals live within a web of inter-individual connections. Here, for the first time, we used a network approach to investigate how social structure and individuals' connectedness change during space restriction. We collected grooming and aggression data during a 6-week control period and a 5-week period of space restriction in a large group of zoo chimpanzees. We compared network density and individual centrality measures (degree, eigenvector, and betweenness centrality) between these two periods using permutation tests. The density of the unidirectional grooming network was significantly lower during space restriction, indicating fewer grooming partners and a less cohesive network. This was mainly due to a reduction in females' grooming partners (degree) and an increase in females' betweenness centrality. We found no differences in the mutual grooming or aggression networks. Our findings are consistent with a conflict avoidance strategy and complement previous findings from the same dataset based on individual behavioral rates that supported a selective inhibition strategy. The results highlight the dynamic nature of social structure and its inherent flexibility to respond effectively to short-term changes in the environment.

Using Parasitic Load to Measure the Effect of Anthropogenic Disturbance on Vervet Monkeys.

Vervet monkeys, Chlorocebus pygerythrus, thrive in urban areas of KwaZulu-Natal, South Africa, and present a suitable model to assess parasitic load as a measure of anthropogenic disturbance, such as urbanization. We collected vervet monkey faecal samples from four study sites representing a gradient of land use and urbanization. We assessed faecal parasites using the faecal flotation method calculating eggs per gram and parasite richness. Overall, the more urban vervet monkey populations had a significantly higher parasite richness and abundance. Our study shows the applicability of using parasite load to measure the effect of urbanization on wildlife.

Durability and flexibility of chimpanzee grooming patterns during a period of dominance instability.

Growing evidence from studies on primates and other taxa has shown that the maintenance of long-term affiliative patterns influences fitness. Thus, understanding how individuals regulate social interactions in response to environmental and social factors contributes to our understanding of the evolutionary basis of sociality. We investigated the durability of affiliation patterns in chimpanzees across three 3-month periods of varying social uncertainty depending on the degree of stability in the male hierarchy, with a 2-year gap between each period. Periods were unstable (no clear alpha male), recently stable (new alpha male just established) and stable (alpha male in place for 2 years). We focused on three features of social exchange shared by human and non-human primates: consistency of exchanges across periods, durability of preferred partners, and degree of reciprocity in each period. We compared male-to-male, female-to-female, male-to-female, and female-to-male grooming patterns. Overall, more grooming was exchanged in the stable period. Grooming patterns were not consistent across the three periods, but were only consistent between the recently stable and stable periods for female-to-female and male-to-female dyads. As predicted from the opportunistic nature of male relationships, male-to-male grooming was least likely to be correlated across all periods and males had relatively fewer durable (i.e., preferred partners in all periods) same-sex partners than females. Our predictions that grooming reciprocity would be less likely during the unstable period and in male-male dyads were only partially supported. We found grooming reciprocity in all periods for female-female dyads but only in the stable period for male-male and female-male dyads. Although long-term affiliative patterns are well studied in primates, this is the first study to investigate the association between social uncertainty and durability of affiliative patterns. Our findings suggest social uncertainty influences social exchange and highlight the importance of considering group instability in studies of social relationships.

The Occurrence of Postconflict Skills in Captive Immature Chimpanzees (Pan troglodytes).

Conflict management strategies can reduce costs of aggressive competition in group-living animals. Postconflict behaviors such as reconciliation and third-party postconflict affiliation are widely accepted as social skills in primates and have been demonstrated in many species. Although immature primates possess a repertoire of species-specific behaviors, it is thought that they gradually develop appropriate social skills throughout prolonged juvenility to establish and maintain complex social relationships within their group. We examined the occurrence of postconflict skills in five immature chimpanzees (Pan troglodytes) over 15 mo, focusing on interactions that were not with the subject's mother. We observed reconciliation, with conciliatory tendencies comparable to adults, and provide the first evidence that captive immature chimpanzees commonly reconciled using social play. However, immatures were not more likely to reconcile valuable than nonvaluable relationships. We also observed third party postconflict affiliation although at a lower level than reported for adults. Our results provide evidence for postconflict skills in immature chimpanzees but the lack of higher conciliatory tendency with valuable partners and low occurrence of third-party affiliation indicates extended juvenility may be required refine these skills. Further work is needed to investigate whether these behaviors have the same function and effectiveness as those found in adults.

Happy hamsters? Enrichment induces positive judgement bias for mildly (but not truly) ambiguous cues to reward and punishment in Mesocricetus auratus.

Recent developments in the study of animal cognition and emotion have resulted in the 'judgement bias' model of animal welfare. Judgement biases describe the way in which changes in affective state are characterized by changes in information processing. In humans, anxiety and depression are characterized by increased expectation of negative events and negative interpretation of ambiguous information. Positive wellbeing is associated with enhanced expectation of positive outcomes and more positive interpretation of ambiguous information. Mood-congruent judgement biases for ambiguous information have been demonstrated in a range of animal species, with large variation in the way tests are administered and in the robustness of analyses. We highlight and address some issues using a laboratory species not previously tested: the Syrian hamster (Mesocricetus auratus). Hamsters were tested using a spatial judgement go/no-go task in enriched and unenriched housing. We included a number of controls and additional behavioural tests and applied a robust analytical approach using linear mixed effects models. Hamsters approached the ambiguous cues significantly more often when enriched than unenriched. There was no effect of enrichment on responses to the middle cue. We discuss these findings in light of mechanisms underlying processing cues to reward, punishment and true ambiguity, and the implications for the welfare of laboratory hamsters.

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support.

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.

Female sexual advertisement reflects resource availability in twentieth-century UK society.

Evolutionary theory suggests that men and women differ in the characteristics valued in potential mates. In humans, males show a preference for physical attractiveness, whereas females seek cues that relate to resources and future earning potential. If women pursue marriage as an economic strategy, female sexual advertisement should increase during periods of poor economic conditions when the number of high-quality male partners becomes a limited resource. To test this prediction, measures of skin display and clothing tightness were taken for clothes portrayed in UK Vogue magazine from 1916 to 1999. These estimates of sexual advertisement were analyzed in relation to an index of economic prosperity (GDP), while controlling for general increases in economic conditions and sexual display over the course of the past century. The results indicate that female sexual display increases as economic conditions decline, with the level of breast display and the tightness of clothing at the waist and hips the key factors underlying this increase. Breast size and symmetry and female body form are secondary sexual characteristics that play an important role in sexual attractiveness. Since advertisement of these features increases as levels of competition for high-quality partners increases, females appear to use marriage as an economic strategy. Patterns of female fashion appear to be underpinned by evolutionary considerations relating resource availability to female reproductive success.