Colobus Research Articles

Genomic and transcriptomic evidence for descent from Plasmodium and loss of blood schizogony in Hepatocystis parasites from naturally infected red colobus monkeys.

Hepatocystis is a genus of single-celled parasites infecting, amongst other hosts, monkeys, bats and squirrels. Although thought to have descended from malaria parasites (Plasmodium spp.), Hepatocystis spp. are thought not to undergo replication in the blood-the part of the Plasmodium life cycle which causes the symptoms of malaria. Furthermore, Hepatocystis is transmitted by biting midges, not mosquitoes. Comparative genomics of Hepatocystis and Plasmodium species therefore presents an opportunity to better understand some of the most important aspects of malaria parasite biology. We were able to generate a draft genome for Hepatocystis sp. using DNA sequencing reads from the blood of a naturally infected red colobus monkey. We provide robust phylogenetic support for Hepatocystis sp. as a sister group to Plasmodium parasites infecting rodents. We show transcriptomic support for a lack of replication in the blood and genomic support for a complete loss of a family of genes involved in red blood cell invasion. Our analyses highlight the rapid evolution of genes involved in parasite vector stages, revealing genes that may be critical for interactions between malaria parasites and mosquitoes.

Selecting between iron-rich and clay-rich soils: a geophagy field experiment with black-and-white colobus monkeys in the Budongo Forest Reserve, Uganda.

Geophagy, the intentional consumption of soil, has been observed in humans and numerous other animal species. Geophagy has been posited to be adaptive, i.e., consumed soil protects against gastrointestinal distress and/or supplements micronutrients. We conducted a field experiment in the Budongo Forest, Uganda, to investigate geophagic behaviors, including soil preference, the quantity of soil eaten, and competition for access to preferred soils. We placed pairs of artificial tree stumps at two existing geophagy sites. One stump contained soil from the surrounding area, Sonso, that could supplement bioavailable iron. The other stump contained soil from a neighboring community, Waibira, that was richer in clay minerals, which could provide protection from plant secondary compounds. We monitored activity and engagement with the stumps for 10 days using camera traps. After 5 days, we reversed the type of soil that was in the stumps at both sites (i.e., a crossover design). Only Colobus guereza (black-and-white colobus monkeys) interacted with the stumps. These monkeys used visual and olfactory cues to select between the two soils and exclusively ate the clay-rich soil, consuming 9.67kg of soil over 4.33h. Our findings lend the greatest plausibility to the protection hypothesis.Additionally, monkeys competed for access to the stumps, and 13% of the videos captured aggression, including pushing, excluding, and chasing other individuals from the experimental stumps. Nine episodes of vigilance and flight behavior were also observed. Given that intentionally ingested soil is a valuable resource that may confer health benefits, geophagy sites should be conserved and protected.

Loss of protozoan and metazoan intestinal symbiont biodiversity in wild primates living in unprotected forests

In light of the current biodiversity crisis, investigating the human impact on non-human primate gut biology is important to understanding the ecological significance of gut community dynamics across changing habitats and its role in conservation. Using traditional coproscopic parasitological techniques, we compared the gastrointestinal protozoan and metazoan symbiont richness of two primates: the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species live sympatrically in both protected and unprotected forests within the Udzungwa Mountains of Tanzania with distinct ecological adaptations and diets. Our results showed that terrestrial and omnivorous yellow baboons had 2 (95% CI 1.47–2.73) and 3.78 (2.62–5.46) times higher gut symbiont richness (both including and excluding rare protozoans) compared to the arboreal and leaf-eating Udzungwa red colobus in unprotected and protected forest, respectively. We also found a consistent depletion of symbiont richness in red colobus living in the unprotected forest fragment compared to the continuous protected forests [the latter having 1.97 times (95% CI 1.33–2.92) higher richness], but not in yellow baboons. Richness reduction was particularly evident in the Udzungwa red colobus monkeys, confirming the pattern we reported previously for gut bacterial communities. This study demonstrates the impact of human activities even on the microbiodiversity of the intestinal tract of this species. Against the background of rapid global change and habitat degradation, and given the health benefits of intact gut communities, the decrease in natural gut symbionts reported here is worrying. Further study of these communities should form an essential part of the conservation framework.

Non-human primates in the Gambia harbour human-associated pathogenic Escherichia coli strains

Increasing contact between humans and non-human primates provides an opportunity for the transfer of potential pathogens or antimicrobial resistance between different host species. We have investigated genetic diversity and antimicrobial resistance in Escherichia coli isolates from a range of non-human primates dispersed across the Gambia: patas monkey (n=1), western colobus monkey (n=6), green monkey (n=14) and guinea baboon (n=22). From 43 stools, we recovered 99 isolates. We performed Illumina whole-genome shotgun sequencing on all isolates and nanopore long-read sequencing on isolates with antimicrobial resistance genes. We inferred the evolution of E. coli in this population using the EnteroBase software environment. We identified 43 sequence types (ten of them novel), spanning five of the eight known phylogroups of E. coli. Many of the observed sequence types and phylotypes from non-human primates have been associated with human extra-intestinal infection and carry virulence characteristics associated with disease in humans, particularly ST73, ST217 and ST681. However, we found a low prevalence of antimicrobial resistance genes in isolates from non-human primates. Hierarchical clustering showed that ST442 and ST349 from non-human primates are closely related to isolates from human infections, suggesting recent exchange of bacteria between humans and monkeys. Our results are of public health importance, considering the increasing contact between humans and wild primates.

Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes

The gut microbiome is structured by social groups in a variety of host taxa. Whether this pattern is driven by relatedness, similar diets or shared social environments is under debate because few studies have had access to the data necessary to disentangle these factors in wild populations. We investigated whether diet, relatedness or the 1 m proximity network best explains differences in the gut microbiome among 45 female colobus monkeys in eight social groups residing at Boabeng-Fiema, Ghana. We combined demographic and behavioural data collected during May – August 2007 and October 2008 – April 2009 with 16S rRNA sequencing of faecal samples collected during the latter part of each observation period. Depending on the beta diversity index, social group identity explained 19–28% of the variation in gut microbiome beta diversity. When comparing the predictive power of dietary dissimilarity, relatedness and connectedness in the 1 m proximity network, the models with social connectedness received the strongest support, even in our analyses that excluded within-group dyads. This novel finding indicates that microbes may be transmitted during intergroup encounters, which could occur either indirectly via shared environments or directly via social contact. Lastly, some of the gut microbial taxa that appear to be transmitted via 1 m proximity are associated with digestion of plant material. Further research is needed to investigate whether this type of gut microbe transmission yields health benefits, which could provide an incentive for the formation and maintenance of social bonds within and between social groups.

Anogenital distance as a measure of male competitive ability in Rwenzori Angolan colobus.

Anogenital distance (AGD) is positively correlated to fetal androgen exposure and developmental masculinization in mammals. Independent of overall body size, AGD shows a strong positive correlation with male fertility and in rodents, AGD is a good indicator of male competitive ability and is associated with female choice. We hypothesized that AGD will also predict male competitive ability in non-human primates. To test this, we measured AGD noninvasively with a parallel laser in a wild population of Angolan colobus monkeys (Colobus angolensis ruwenzorii) in Uganda and correlated to it to their social structure. C. angolensis ruwenzorii form a multilevel society with both one-male/multifemale units (OMUs) and multimale/multifemale units (MMUs). We compared AGD in males from five OMUs and six MMUs and related it to their fecal androgen metabolite concentrations, dominance rank and body size, and to the number of females in their unit. Males in OMUs had greater access to females, so were predicted to have longer AGDs, but this was not found. AGD also did not correlate overall with mean fecal androgen metabolites in MMUs. However, AGD was correlated with dominance rank in MMUs, demonstrating that higher-ranking males in these multimale units had longer AGDs. Body size did not show the same relationship with dominance rank, suggesting that male rank was not just a reflection of absolute male size. Our findings indicate that AGD predicts male competitive ability in this species and that it may be a useful correlate throughout the non-human primates. These results also support the idea that prenatal androgen exposure increases the likelihood of the expression of behaviors that maintain high dominance rank.

Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum.

Gastrointestinal parasites colonizing the mammalian gut influence the host immune system and health. Parasite infections, mainly helminths, have been studied intensively in both humans and non-human animals, but relatively rarely within a conservation framework. The Udzungwa red colobus monkey (Procolobus gordonorum) is an endangered endemic primate species living in the Udzungwa Mountains of Tanzania, a global biodiversity hotspot. Since this endemic primate species is highly sensitive to human disturbance, here we investigate whether habitat type (driven by natural and human-induced factors) is associated with helminth diversity. Using standard flotation and sedimentation techniques, we analyzed 251 fecal samples belonging to 25 social groups from four different forest blocks within the Udzungwa Mountains. Five parasitic helminth taxa were recovered from Udzungwa red colobus, including Trichuris sp., Strongyloides fulleborni, S. stercoralis, a strongylid nematode and Colobenterobius sp. We used Generalized Linear Mixed Models to explore the contribution of habitat type, altitude and fecal glucocorticoid levels (as biomarkers of stress) in predicting gut parasite variation. Although some parasites (e.g., Trichuris sp.) infected more than 50% of individuals, compared to others (e.g., Colobenterobius sp.) that infected less than 3%, both parasite richness and prevalence did not differ significantly across forests, even when controlling for seasonality. Stress hormone levels also did not predict variation in parasite richness, while altitude could explain it resulting in lower richness at lower altitudes. Because human activities causing disturbance are concentrated mainly at lower altitudes, we suggest that protection of primate forest habitat preserves natural diversity at both macro- and microscales, and that the importance of the latter should not be underestimated.

Reciprocity and rotating social advantage among females in egalitarian primate societies

Interfemale competition regimes in primate societies have been described as despotic or egalitarian based on female social behaviour. Hierarchies and nepotism are typical of despotic primates, where dominance rank and kinship are known to be strong drivers of who grooms whom and who fights with whom. However, a general theory for what structures female–female interactions in egalitarian societies remains underdeveloped. We present two nonmutually exclusive hypotheses that each propose a mechanism for levelling social advantages in a group by conferring social favour to all or most females over time: transitory states (age, residency status and reproductive state) bias social interactions and/or reciprocity governs social interactions. In this study, we (1) determined that a group of red colobus monkeys, Procolobus rufomitratus tephrosceles, in Kibale National Park, Uganda, are highly egalitarian; (2) tested our hypotheses for how egalitarianism may be maintained in this group; and (3) analysed findings across primate studies for support for either hypothesis. In red colobus, agonistic interactions were predicted by age – a transitory state – and transitory states and reciprocity predicted grooming interactions: avid groomers, older females and short-term resident females received more grooming. In addition, behavioural indicators of social status (aggression given and grooming received) were not associated with reproductive success in red colobus, as might be expected in an egalitarian group where variance in fitness should be low. Across primates, we found that transitory states commonly structure social interactions in egalitarian societies but not in despotic societies and that reciprocity is highly variable, especially among egalitarian societies. Rotating social advantage as females shift among transitory states and/or reciprocate grooming may lower interfemale skew in social benefits and potentially in lifetime reproductive success in egalitarian groups, setting them apart from despotic societies where dominance hierarchies and kinship maintain a more static and unequal distribution of social advantage.

Conservation Education, Alternative Livelihood and Habitat Restoration: The Best Strategies for Conservation of Magombera Forest Reserve

The Magombera forest is a home of endemic and endangered biological species such as Udzungwa red colobus monkey (Procolobus gordonorum) and the Magombera chameleon (Kinyongia magomberae). However, the forest is facing high threat of disappearing through resources extraction pressure from adjacent local communities. The project aimed at improving conservation of Magombera forest by involving the adjacent communities through provision of conservation education, restoration initiatives and bee keeping as alternative livelihoods. The study revealed that the concept of forest conservation is well supported. Nevertheless, people are extracting resources from the forest for their subsistence. The dependence of the people on the forest is due to lack of alternatives to the forest resources, inability of the people to produce alternatives source of income and little conservation education. The project resulted in a community having a positive attitude change towards conservation. The improved bee keeping was introduced to the community and successfully adopted. About 89% of indigenous trees planted for restoring the degraded area of the forest survived, only 11% of trees planted could not survive. There is a need to expand the scale of the project by involving many participants particularly youths that showed strong interest in the project.

Why Colobus Monkeys (Colobus guereza) are Attracted to Human Settlements, and Urinate When They Come Across Humans in Their Territory and in Predator Dominant Places? Observation from Bale Mountains National Park, in Ethiopia

Colobus guereza is among the native African primates characterized by a having mainly black, short-haired tails with a small amount of white at the tip. The current study was made on groups of C. guereza found in Bale Mountains National Park, in the east of Rift Valley in Ethiopia. It is commonly called Colobus guereza gallarum though the taxonomy of this group has not been well-resolved. The aim of this paper was to identify the reasons for high abundance of the species in human settlements and related behavioural responses to human appearance in their territory following the recent observation made in Bale Mountains National Park. These issues were addressed through exploration of similar studies in different organisms including primates and referring various journals. The study indicated the high abundance of the species in human settlement has been associated with the need of protection from predators as interactions with humans can buffer non-human primates against the negative impact of environmental factors. Similarly, the urination of C. guereza was found to be anti-predator strategy, which has been demonstrated in combination with alarm calls, running back and forth, etc in other primates. The close attraction of C. guereza to human settlements can affect their existence either positively or negatively. Those unable to adapt to altered habitats will be forced into marginal habitat patches. While those that adapt, are able to live with the changing ecology and survive in agricultural systems often come into direct competition with humans. Similarly, the greater human-primate contact can increase pathogen transmission. Urination which was observed in C. guereza plays key roles in animal territorial defense and in prey-predator interaction. This overlooked behavioural aspect of primates is crucial in conservation of species. Keywords : Attract, Colobus guereza , human settlements, territory, urination. DOI : 10.7176/ALST/75-02 Publication date :June 30 th 2019

Intergroup variation in oestrogenic plant consumption by black‐and‐white colobus monkeys

Intergroup variation in oestrogenic plant consumption by black‐and‐white colobus monkeys

Comparative morphology of the lingual papillae and their connective tissue cores in the tongue of the Abyssinian black-and-white colobus (Colobus guereza).

We observed the morphology of the lingual papillae (filiform, fungiform, foliate, and vallate) and their underlying connective tissue cores (CTCs) in Abyssinian black-and-white colobus monkeys using light and scanning electron microscopy. The tongues of both juvenile and senescent individuals were relatively short in the rostro-caudal direction, with a rounded apex. Lingual tori were absent. Numerous filiform papillae were distributed over the entire tongue, except at the lingual root. A pair of foliate papillae was present on both the lateral and caudal margins of the corpus. Three vallate papillae were distributed on the boundary between the caudal part of the body and the root in both juvenile and senescent individuals. Based on scanning electron microscopy observations, the morphologies of the filiform papillae differed between juvenile and senescent individuals. The epithelial surface of juvenile filiform papillae had a main process, but the associated processes were weak and the underlying CTCs displayed immature morphology. In contrast, the epithelial surface of senescent filiform papillae was associated with several accessory processes, and their underlying CTCs consisted of several auxiliary cores that nearly encircled the main core, forming a concavity in the papilla. CTCs of the filiform papillae showed variable morphology. Juvenile filiform CTCs exhibited a rather primitive morphology, resembling those of the hamster, mole, and Cape hyrax while, conversely, despite the basically folivorous diet of the Abyssinian black-and-white colobus, senescent filiform CTCs resembled those found in omnivorous primates, including members of the Callitrichinae and Homoidea, and also those in Carnivora (e.g., Canidae and Felidae).

Yersinia infection in two captive guereza colobus monkeys (Colobus guereza).

Two guereza colobus monkeys (Colobus guereza) reared in a zoological garden in Japan suddenly died of multifocal fibrinonecrotic gastroenteritis and septicemia associated with infection by Yersinia spp. It was necessary to microbiologically differentiate Yersinia frederiksenii and Y. enterocolitica. We described the pathological findings and discuss the causal agent to emphasize the need to revert to using a combination of multiple examinations for diagnosis.

Effects of Chimpanzee (Pan troglodytes) Hunting Seasonality and Red Colobus (Piliocolobus badius) Association on Diana Monkeys (Cercopithecus diana) in Taï National Park, Côte d’Ivoire

Polyspecific associations occur when species overlap in their environment by chance, converge at common resources, or in response to predation pressure. However, because larger groups may themselves attract the attention of predators, species forming associations must balance the costs and benefits of comingling. Experimental and observational research suggests red colobus (Piliocolobus badius) associate with Diana monkeys (Cercopithecus diana) in Tai National Park, Cote d’Ivoire in response to seasonally shifting predation pressure from chimpanzees (Pan troglodytes verus). Research on this system has focused on immediate behavioral effects of comingling by red colobus and Diana monkeys. We expand on these analyses and explore longer-term changes in Diana monkey behavior. We use scan samples (N = 7025) collected on three Diana monkey groups over 5 years (N = 380 days) to assess differences in diet, activity budget, and strata use in relation to associating with red colobus and chimpanzee hunting seasonality and test for interaction effects between these two variables. We found limited evidence showing Diana monkeys make more than ephemeral behavioral changes in response to comingling with red colobus during chimpanzees’ hunting season (September–November). Synergistic effects of association and hunting season include expanded use of the main canopy, decreased fruit consumption, and increased invertebrate consumption. We find little evidence indicating Diana monkeys minimize behaviors that increase risk of predation from chimpanzees while associated with red colobus during the season when chimpanzees hunt most often. We conclude that when there are few member costs to forming mixed groups, participating species may tolerate associations even without accruing any benefits.

Spatial configuration becomes more important with increasing habitat loss: a simulation study of environmentally-transmitted parasites

Landscape changes can be an important modifier of disease. Habitat fragmentation commonly results in reduced connectivity in host populations and increased use of the remaining habitat. For environmentally transmitted parasites, this presents a possible trade-off between transmission potential at the local and global level. We quantify the effects of fragmentation on the transmission of an environmentally transmitted parasite, teasing apart the relative effects of habitat composition and configuration on both host movement behaviour and subsequent infection patterns. We use a spatially-explicit epidemiological model to simulate the effects of habitat fragmentation, using, as an example, whipworm (Trichuris sp.) within a red colobus monkey population (Procolobus rufomitratus). We found that habitat fragmentation did not always lead to a trade-off between population connectivity and concentration of habitat use in host movement behaviour or in final population infection patterns. However, our simulation results suggest the spatial configuration of the remaining habitat became increasingly influential on behavioural and infection outcomes as habitat was removed. Additionally, we found common fragmentation metrics provided little ability to explain variation in propagation of infections. Our results suggest an interaction between habitat configuration and composition should be considered when assessing disease related impacts of habitat fragmentation on environmentally transmitted parasites, especially in cases where habitat loss is high (≥ 30%). We also propose that spatially-explicit simulations that capture a host’s response to fragmentation could aid in the development of novel landscape metrics targeted towards specific host-parasite-landscape systems.

Changes in the Protected Areas of Bayelsa State, Nigeria

Bayelsa state is one of the core states in the Niger Delta region that inhabits several species of biodiversity of global significance. Six major protected forest reserves (viz: Taylor creek, Apoi creek, Nun river, Edumanon, Ikibiri creek and Igbedi creek) with natural, ecological and cultural importance have been gazetted. This study reviews changes in the conserved area. The study found that developmental projects (construction works mainly due urbanization, industrialization, etc) and quest for food (through agricultural activities) as the main cause of decline in size of the protected areas. The study also found that Taylor creek, Nun river and Edumanon forest reserve have the highest level of shrinkage. Based on species diversity, individual species is under intense pressure with regard to abundance and distribution due to excessive loss of habitats (through logging, deforestation, bush burning and clearing for farming purposes) and hunting. As such, some vital species which are found in these forest reserves within the last 3-5 decades have gone on extinction in the area. Among the 6 forest reserves, Apoi creek is the only forest reserve in Ramsar-listed coastal and freshwater wetlands in Bayelsa state. The forest is also the major stronghold of the endemic Niger Delta Red Colobus monkey ( Procolobus epieni ). The study provided information on the protected areas in Bayelsa state as well as their challenges. Hence, there is the need for effective implementation and surveillance of legislation/law concerning biodiversity conservation within and around the protected areas.

Population Status, Distribution, and Threats of <i>Colobus guereza gallarum</i> in Bale Mountains National Park, Southeastern Ethiopia

Colobus guereza gallarum is the subspecies of Colobus monkey (Colobus guereza) restricted to the Ethiopian highlands to the east of the Rift Valley. This study was carried out from February to June 2016 to provide data on Population status, distribution, and threats of C. g. gallarum in Bale Mountains National Park. Line transects with 5 km distance were made in all survey areas to estimate the whole population in the area. Field visits and questionnaire distribution were made to assess community perception and threats to the species. The major population of C. g. gallarum was observed in Rira. A total of 116 and 113 individuals were observed in the wet and dry seasons, respectively. There was no significant difference between wet and dry seasons (F= 0.072, df=1, p=0.795) of the population size of C. g. gallarum. Out of 229 individuals of guereza counted in both dry and wet seasons, 44 were adult males, 58 adult females, 42 sub-adult males, 43 sub-adult females and the remaining 42 were young individuals. However, as t-test indicated, here was no significant difference between wet and dry seasons in a number of in this sex and age categories (P>0.70). The male to female ratio was 1.00:1.1, while, the age ratio of young to all other individuals was 1.00:4.45. Here also, the ratio of young to an adult female was 1.00:1.40 and 1.00:1.36 during dry and wet seasons, respectively. The response of communities indicated the presence of positive perception towards the species due to its main importance for tourism and cultural aspect of the communities. Moreover, habitat destruction due to logging, farmland expansion and settlement were main observed threats to species in the area.

Cascading competition: the seasonal strength of scramble influences between-group contest in a folivorous primate

Habitat-wide depletion of food leads to scramble feeding competition and animals can mitigate costs with behavioral adjustments in ranging and activity budgets. In seasonal environments, scramble feeding competition may be more intense in lean seasons leading to shifts in the ranges of neighboring groups and cascading changes for other types of competition. Here, we specifically investigated the interplay between within-group scramble (WGS) and between-group contest competition (BGC) using four groups of ursine colobus monkeys (Colobus vellerosus) at Boabeng-Fiema, Ghana. These groups were known to be impacted by WGS and our first goal was to assess whether this competition was occurring in both the abundant and lean seasons. Within-season, between-group comparisons showed WGS in both seasons but greater behavioral compensation in the lean season, especially for larger groups. We then focused on differences in ranging behavior within groups, between seasons to examine whether greater WGS in the lean season influenced the intensity of BGC (rates and “wins” of between-group encounters). The largest and the smallest groups entered more trees and ranged slightly further per day in the lean season suggesting stronger WGS. These two groups also faced more between-group encounters with the small uni-male group winning more often in the lean season. Both middle-sized multi-male groups shifted their ranging towards the edge of the fragment in the lean season. They also engaged in fewer between-group encounters, which they usually lost. This study demonstrates the interplay between different types of competition. It also confirms that male membership disproportionately influence group competitiveness in C. vellerosus. Animals face different forms of competition over limited resources every day but the ways that these competition types influence one another is rarely studied. We focused on within-group scramble competition (WGS) for food in four groups of ursine colobus monkeys and examined how seasonal changes in this type of competition influenced between-group contest competition (BGC). We found that the lean season for food availability showed greater WGS, and that animals compensated for this by using more of their home range. Some highly competitive groups were able to move into shared areas with other groups in the lean season, winning encounters with other groups, while groups with poor competitive ability were forced to range into lower quality areas and avoided other groups. Thus, WGS had cascading effects leading to changes in BGC, showing the importance of studying different types of competition collectively.

Low antibody prevalence against Bacillus cereus biovar anthracis in Taï National Park, Côte d'Ivoire, indicates high rate of lethal infections in wildlife.

Bacillus cereus biovar anthracis (Bcbva) is a member of the B. cereus group which carries both B. anthracis virulence plasmids, causes anthrax-like disease in various wildlife species and was described in several sub-Saharan African rainforests. Long-term monitoring of carcasses in Taï National Park, Côte d’Ivoire, revealed continuous wildlife mortality due to Bcbva in a broad range of mammalian species. While non-lethal anthrax infections in wildlife have been described for B. anthracis, nothing is known about the odds of survival following an anthrax infection caused by Bcbva. To address this gap, we present the results of a serological study of anthrax in five wildlife species known to succumb to Bcbva in this ecosystem. Specific antibodies were only detected in two out of 15 wild red colobus monkeys (Procolobus badius) and one out of 10 black-and-white colobus monkeys (Colobus polykomos), but in none of 16 sooty mangabeys (Cercocebus atys), 9 chimpanzees (Pan troglodytes verus) and 9 Maxwell’s duikers (Cephalophus maxwellii). The combination of high mortality and low antibody detection rates indicates high virulence of this disease across these different mammalian species.

Predation by female chimpanzees: Toward an understanding of sex differences in meat acquisition in the last common ancestor of Pan and Homo

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants). This difference has long been assumed to reflect human female reproductive constraints, particularly caring for and provisioning mates and offspring. Long-term studies of chimpanzees (Pan troglodytes) enable tests of hypotheses about the possible origins of human sex differences in hunting, prior to pair-bonding and regular provisioning. We studied two eastern chimpanzee communities (Kasekela, Mitumba) in Gombe, Tanzania and one (Kanyawara) in Kibale, Uganda. Relative to males, females had low hunting rates in all three communities, even where they encountered red colobus monkeys (the primary prey of chimpanzees) as often as males did. There was no evidence that clinging offspring hampered female hunting. Instead, consistent with the hypothesis that females should be more risk-averse than males, females at all three sites specialized in low-cost prey (terrestrial/sedentary prey at Gombe; black and white colobus monkeys at Kanyawara). Female dominance rank was positively correlated with red colobus hunting probability only at Kasekela, suggesting that those in good physical condition were less sensitive to the costs of possible failure. Finally, the potential for carcass appropriation by males deterred females at Kasekela (but not Kanyawara or Mitumba) from hunting in parties containing many adult males. Although chimpanzees are not direct analogs of the last common ancestor (LCA) of Pan and Homo, these results suggest that before the emergence of social obligations regarding sharing and provisioning, constraints on hunting by LCA females did not necessarily stem from maternal care. Instead, they suggest that a risk-averse foraging strategy and the potential for losing prey to males limited female predation on vertebrates. Sex differences in hunting behavior would likely have preceded the evolution of the sexual division of labor among modern humans.