Wild Geladas Research Articles

Technical note: A biological anthropologist's guide for applying microbiome science to studies of human and non-human primates.

A central goal of biological anthropology is connecting environmental variation to differences in host physiology, biology, health, and evolution. The microbiome represents a valuable pathway for studying how variation in host environments impacts health outcomes. While there are many resources for learning about methods related to microbiome sample collection, laboratory analyses, and genetic sequencing, there are fewer dedicated to helping researchers navigate the dense portfolio of bioinformatics and statistical approaches for analyzing microbiome data. Those that do exist are rarely related to questions in biological anthropology and instead are often focused on human biomedicine. To address this gap, we expand on existing tutorials and provide a "road map" to aid biological anthropologists in understanding, selecting, and deploying the data analysis and visualization methods that are most appropriate for their specific research questions. Leveraging an existing dataset of fecal samples and survey data collected from wild geladas living in Simien Mountains National Park in Ethiopia (Baniel et al., 2021), this paper guides researchers toward answering three questions related to variation in the gut microbiome across host and environmental factors. By providing explanations, examples, and a reproducible workflow for different analytic methods, we move beyond the theoretical benefits of considering the microbiome within anthropological research and instead present researchers with a guide for applying microbiome science to their work. This paper makes microbiome science more accessible to biological anthropologists and paves the way for continued research into the microbiome's role in the ecology, evolution, and health of human and non-human primates.

Manual preference, performance, and dexterity for bimanual grass-feeding behavior in wild geladas (Theropithecus gelada).

We assessed whether wild geladas, highly specialized terrestrial grass eaters, are lateralized for bimanual grass-plucking behavior. According to the literature, we expected that complex motor movements in grass feeding would favor the emergence of a population-level hand bias in these primates. In addition, we described geladas' manual behavior based on systematic observations of several individuals. Our study group included 28 individuals belonging to a population of free-ranging geladas frequenting the Kundi plateau, Ethiopia. We filmed monkeys while feeding on grass, and hand preference and performance were coded. Geladas performed more plucking movements per second with their left hand (LH) compared to the right one and preferred their LH both to start and finish collection bouts. Also, the rhythmic movements of each hand had a significant tendency towardisochrony. Finally, geladas used forceful pad-to-pad precision grips, in-hand movements, and compound grips to pluck and collect grass blades, considered the most advanced manual skills in primate species. The LH's leading role suggests an advantage of the right hemisphere in regulating geladas' bimanual grass-feeding behavior. The tactile input from the hands and/or rhythmic hand movements might contribute to explaining this pattern of laterality. Our findings highlighted the importance of adopting multiple laterality measures to investigate manual laterality. Moreover, the need to speed up the execution time of manual foraging might be a further important factor in studying the evolution of manual laterality and dexterity in primates.

Urinary neopterin reflects immunological variation associated with age, helminth parasitism, and the microbiome in a wild primate.

Neopterin, a product of activated white blood cells, is a marker of nonspecific inflammation that can capture variation in immune investment or disease-related immune activity and can be collected noninvasively in urine. Mounting studies in wildlife point to lifetime patterns in neopterin related to immune development, aging, and certain diseases, but rarely are studies able to assess whether neopterin can capture multiple concurrent dimensions of health and disease in a single system. We assessed the relationship between urinary neopterin stored on filter paper and multiple metrics of health and disease in wild geladas (Theropithecus gelada), primates endemic to the Ethiopian highlands. We tested whether neopterin captures age-related variation in inflammation arising from developing immunity in infancy and chronic inflammation in old age, inflammation related to intramuscular tapeworm infection, helminth-induced anti-inflammatory immunomodulation, and perturbations in the gastrointestinal microbiome. We found that neopterin had a U-shaped relationship with age, no association with larval tapeworm infection, a negative relationship with metrics related to gastrointestinal helminth infection, and a negative relationship with microbial diversity. Together with growing research on neopterin and specific diseases, our results demonstrate that urinary neopterin can be a powerful tool for assessing multiple dimensions of health and disease in wildlife.

A novel statovirus identified in fecal samples from wild geladas in the Ethiopian highlands.

We present a novel statovirus in geladas (Theropithecus gelada), graminivorous primates endemic to the Ethiopian highlands. Using a high-throughput sequencing approach, we identified contiguous sequences in feces from two adult female geladas in the Simien Mountains National Park, Ethiopia, that share similarities to statoviruses. Our phylogenetic analysis of the whole genome, as well as the RNA-dependent RNA polymerase (RdRp) and capsid protein (CP) amino acid sequences, revealed that the gelada statoviruses cluster with those from other primates (laboratory populations of Macaca nemestrina and Macaca mulatta). As the first report of statovirus in wild primates, this finding contributes to our understanding of the phylogenetic and geographic distribution of statoviruses and their hosts.

Effects of climate variability on the demography of wild geladas.

Nonhuman primates are an essential part of tropical biodiversity and play key roles in many ecosystem functions, processes, and services. However, the impact of climate variability on nonhuman primates, whether anthropogenic or otherwise, remains poorly understood. In this study, we utilized age‐structured matrix population models to assess the population viability and demographic variability of a population of geladas (Theropithecus gelada) in the Simien Mountains, Ethiopia with the aim of revealing any underlying climatic influences. Using data from 2008 to 2019 we calculated annual, time‐averaged, and stochastic population growth rates (λ) and investigated relationships between vital rate variability and monthly cumulative rainfall and mean temperature. Our results showed that under the prevailing environmental conditions, the population will increase (λ s = 1.021). Significant effects from rainfall and/or temperature variability were widely detected across vital rates; only the first year of infant survival and the individual years of juvenile survival were definitively unaffected. Generally, the higher temperature in the hot‐dry season led to lower survival and higher fecundity, while higher rainfall in the hot‐dry season led to increased survival and fecundity. Overall, these results provide evidence of greater effects of climate variability across a wider range of vital rates than those found in previous primate demography studies. This highlights that although primates have often shown substantial resilience to the direct effects of climate change, their vulnerability may vary with habitat type and across populations.

The face never lies: facial expressions and mimicry modulate playful interactions in wild geladas

Play fighting, the most common form of social play in mammals, is a fertile field to investigate the use of visual signals in animals’ communication systems. Visual signals can be exclusively emitted during play (e.g. play faces, PF, context-dependent signals), or they can be released under several behavioural domains (e.g. lip-smacking, LS, context-independent signals). Rapid facial mimicry (RFM) is the involuntary rapid facial congruent response produced after perceiving others’ facial expressions. RFM leads to behavioural and emotional synchronisation that often translates into the most balanced and longest playful interactions. Here, we investigate the role of playful communicative signals in geladas (Theropithecus gelada). We analysed the role of PF and LS produced by wild immature geladas during play fighting. We found that PFs, but not LS, were particularly frequent during the riskiest interactions such as those including individuals from different groups. Furthermore, we found that RFM (PF→PF) was highest when playful offensive patterns were not biased towards one of the players and when the session was punctuated by LS. Under this perspective, the presence of context-independent signals such as LS may be useful in creating an affiliative mood that enhances communication and facilitates most cooperative interactions. Indeed, we found that sessions punctuated by the highest frequency of RFM and LS were also the longest ones. Whether the complementary use of PF and LS is strategically guided by the audience or is the result of the emotional arousal experienced by players remains to be investigated.Significance StatementFacial expressions and their rapid replication by an observer are fundamental communicative tools during social contacts in human and non-human animals. Play fighting is one of the most complex forms of social interactions that can easily lead to misunderstanding if not modulated through an accurate use of social signals. Wild immature geladas are able to manage their play sessions thus limiting the risk of aggressive escalation. While playing with unfamiliar subjects belonging to other groups, they make use of a high number of play faces. Moreover, geladas frequently replicate others’ play faces and emit facial expressions of positive intent (i.e. lip-smacking) when engaging in well-balanced long play sessions. In this perspective, this “playful facial chattering” creates an affiliative mood that enhances communication and facilitates most cooperative interactions.

Inter-sexual multimodal communication during mating in wild geladas: the leading role of females.

Female primates can emit vocalizations associated with mating that can function as honest signals of fertility. Here, we investigated the role of mating calls and visual signals in female geladas (Theropithecus gelada). Because females have a central role in the gelada society and seem to solicit sexual interactions, we answered whether they emit vocalizations in conjunction with gazing to increase mating success probability. Before and during copulations, females can emit pre-copulation calls and copulation calls. For the first time, we identified a new female vocalization emitted at the final stage of copulations (end-copulation call), possibly marking the occurrence of ejaculation. We found that longer pre-copulation call sequences were followed by both prolonged copulations and the presence of end-copulation calls, thus suggesting that females use pre-copulation calls to ensure successful copula completion. Moreover, we found that different combinations of female vocal types and gazing had different effects on male vocal behavior and motivation to complete the copula. The analysis of the vocal and visual signals revealed a complex inter-sexual multimodal chattering with the leading role of females in the signal exchange. Such chattering, led by females, modulates male sexual arousal, thus increasing the probability of the copula success.

Infant handling increases grooming towards mothers in wild geladas (Theropithecus gelada)

Infant handling – involving affiliative behavior from non-mothers to infants – is a phenomenon that is variably present in Old World monkeys and can be granted by mothers to obtain social services, such as grooming. Here we investigated for the first time whether infant handling could influence grooming exchange in wild geladas. We gathered data on the population of Kundi highland (Ethiopia) in 2019/2020. Via sampling on 15 focal mothers from eight different One-Male Units, we video-recorded 55 grooming sessions between focal mothers and non-focal females (mothers or non-mothers). We also recorded the possible occurrence of infant handling performed by non-focal females. We found that grooming sessions were longer between mother and non-mothers and in the presence than in the absence of infant handling. Hence, our results show that infant handling can influence the grooming exchange between wild gelada females. Because grooming is used to establish and reinforce social bonds in primates, infant handling may act as a ‘social bridge’ in a female bonded society. From an evolutionary perspective, infant handling strategies might represent the stepping stone to more complex forms of infant care, such as allomaternal care and cooperative breeding.

First evidence of yawn contagion in a wild monkey species

Yawn contagion occurs when individuals yawn in response to the yawn of others (triggers). This is the first account of yawn contagion in wild geladas (Theropithecus gelada), a monkey species that shows yawn contagion in captivity and is organized in core units (one-male/bachelor groups) forming multilevel associations. In a population of geladas from the Kundi plateau (Ethiopia) we found that the yawning response was highest when geladas could perceive a triggering yawn, which confirms that yawn contagion is present in the wild. Yawn duration, mouth-opening degree and presence/absence of vocalisation (possibly modulating yawn detectability) did not affect the likelihood of contagion. Males and females, known to be both implicated in movement initiation within groups, were similarly powerful as yawn triggers. Instead, group membership and responder sex had a significant role in shaping the phenomenon. Yawn contagion was highest between individuals belonging to different core units and males were most likely to respond to others’ yawns. Because males have a non-negligible role in inter-group coordination, our results suggest that yawn contagion may have a communicative function that goes beyond the basic unit level.

Looking into each other's eyes makes it better: eye-to-eye contact enhances sexual interactions in wild geladas

In human and nonhuman primates eye-to-eye contact (EEC), a face-to-face communication component, can promote emotional/attentional engagement and prolong affiliative interactions. Owing to its direct impact on fitness, the reproductive context is perhaps the most critical context for investigating EEC's importance. However, the presence of this phenomenon around mating and its functions in primates is still understudied. In this work, we investigated whether EEC was present during copulations and influenced the copula duration and postcopulation grooming occurrence in the wild gelada, Theropithecus gelada , an Old World monkey species. We found that the previous presence of the male ‘look-at’ triggered the female ‘look-at’. Moreover, copulations were most likely to last longer in the presence of EEC. In addition, the occurrence of postcopulation grooming between partners, most frequently initiated by females, increased when copulations included EEC. Females' engagement in EEC with the male may be a form of continuation of female precopulatory proceptivity and facilitate males' copulatory activity. By prolonging sexual contacts, EEC may also increase the chances of ejaculation. By grooming their partners after mating, female geladas may attempt to reduce male arousal and prolong the social interaction with them, possibly strengthening their social bond. These results provide the first quantitative evidence that EEC is an effective mechanism for prolonging mating interactions and enhancing postmating affiliation in a Papionini species. On a broader perspective, the presence of EEC in an Old World monkey species suggests that EEC may have been favoured by natural selection to promote reproductive advantages during human evolution. • Eye-to-eye contact is little studied in the mating context. • Gelada females can look at and establish eye contact with males during copulation. • Eye-to-eye contact increases copula duration and possibly reproduction success. • Eye-to-eye contact increases postmating grooming and possibly male-female cohesion. • Eye-to-eye contact strengthens social bonds between mates in monkeys.

Wild geladas (Theropithecus gelada) in crops\u2014more than in pasture areas\u2014reduce aggression and affiliation

Human–primate interfaces are expanding and, despite recent studies on primates from peri-urban environments, little research exists on the impact of agriculture and/or pasture areas on primate social behavior and health. We assessed how crop/pasture areas potentially alter social behavior and health of wild geladas (Theropithecus gelada) frequenting the unprotected area of Kundi (Ethiopia). We predicted that compared to pasture areas, crop areas (i) would be more challenging for geladas (prediction 1) and (ii) would have a greater impact on both aggressive and affiliative behavior, by reducing grooming time and enhancing competition (prediction 2). During January–May 2019 and December 2019–February 2020, we collected data (via scan, focal animal sampling, and video analyses) on direct human disturbance, external signs of pathologies and social behavior of 140 individuals from 14 one-male units and two all-male units. Animals experienced the highest level of human disturbance in crop areas (in line with prediction 1). Individuals from the groups preferentially frequenting crop areas showed the highest prevalence of external signs of pathologies consistent with chemical and biological contamination (alopecia/abnormally swollen parts). We collected 48 fecal samples. Samples from frequent crop users contained the highest rates of parasitic elements/gram (egg/larva/oocyst/cyst) from Entamoeba histolytica/dispar, a parasite common in human settlements of the Amhara region. In crop areas, subjects spent less time grooming but engaged in lower rates of intense aggression (in partial agreement with prediction 2). We speculate that the reduction in social behavior may be a tactic adopted by geladas to minimize the likelihood of detection and maximize food intake while foraging in crops.

Let’s unite in play! Play modality and group membership in wild geladas

Two of the main hypotheses put forth to explain the function of immature social play are the Social Skill Hypothesis and the Motor Training Hypothesis focussing on whether play can improve social competence to develop cooperative social networks or physical abilities to outcompete others, respectively. Here, we tested these hypotheses on a monkey species, the wild gelada (Theropithecus gelada) from the Kundi plateau, Ethiopia. This species is organized in bands divided in One-Male Units (OMUs), united only via social play. Immatures form ‘play units’ in which individuals from the same and different OMUs interact. We analysed the potential differences between inter- and intra-OMU play to verify which of the two hypotheses (Social Skill or Motor Training Hypothesis) best explains the function of play in geladas. We analysed 527 video-recorded social play sessions and found mixed support for both hypotheses. In agreement with the Social Skill Hypothesis, we found that play in geladas shows scarce social canalization being similarly distributed across age, sex and group membership. In line with the Motor Training Hypothesis, we detected higher levels of competition (shorter and more unbalanced sessions) in inter-OMU compared to intra-OMU play. Hence, in geladas play can be a tool for both the development of social relationships and the improvement of the physical skills necessary to cope with either future mates or competitors. In conclusion, neither hypothesis can be discarded and both hypotheses concur in explaining why immature geladas peculiarly form ‘play units’ embracing both ingroup and outgroup members.

Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas

BackgroundAdaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments.ResultsHere, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas (Theropithecus gelada). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods.ConclusionTogether, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa.1akjfNgEHq-cf4GgXinJf8Video abstract

Primate Reproduction: When Timing Is Everything

In species with intense male competition, reproducing at the wrong time can have dire consequences for females. A new study of wild gelada monkeys finds that females delay or accelerate puberty to moderate the risks of inbreeding and infanticide.

Male-Mediated Maturation in Wild Geladas

The timing of female maturation in wild mammals is often constrained by ecological variables that relate to food acquisition. However, maturational timing in female mammals can also respond to social variables. Specifically, the arrival of novel males can accelerate maturation while the presence of related males can inhibit it. Despite studies on more than two dozen mammalian taxa in captivity, evidence for male-mediated maturation has not been systematically demonstrated in any wild population. Here, we report the first evidence of male-mediated maturation in a wild primate, the gelada (Theropithecus gelada). After the arrival of a new breeding male in the group (a male takeover), young females were three times more likely to mature. We then examined these takeover-associated maturations in more detail: some were earlier than expected (a presumptive "Vandenbergh effect," or male-accelerated maturation), some were at the expected age for the average female gelada, and some were later than expected (a presumptive "inbreeding avoidance delay," or father-induced reproductive suppression). An examination of fecal estrogens, which rise just before visible signs of maturation in this species, revealed that male takeovers induced a surge in estrogens for immature females of all ages-even females that did not mature. These are the first data to demonstrate that specific males are associated with the onset of maturation in a wild primate and to provide a possible mechanism for this change. These results suggest that all male-mediated maturation (whether accelerated, on-time, or delayed) may be governed by similar neuroendocrine processes.

Ecology eclipses phylogeny as a major driver of nematode parasite community structure in a graminivorous primate.

Understanding the relative strength of ecology and phylogeny in shaping parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.We characterized the gastrointestinal (GI) parasite community of wild geladas (Theropithecus gelada), primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.Geladas exhibited very constrained GI parasite communities: only two genera (Oesophagostomum and Trichostrongylus) were identified across 303 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g., Bos taurus, Ovis aries) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to Oesophagostomum sp., seven to Trichostrongylus sp., and one to T. vitrinus.Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited ~4x higher ASV richness than geladas at a less disturbed location within the park.In this system, ecology was a stronger predictor of parasite community structure than phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.

The social functions of complex vocal sequences in wild geladas

Several studies show that highly social taxa produce relatively more complex vocalizations. Yet, very few of these cases have demonstrated the function that vocal complexity plays within a highly social setting. Here, we assess potential functions of vocal complexity in male geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. Geladas are known for both their diverse vocalizations (routinely produced in long sequences) and their complex social structure (extremely large groups and long-term male-female bonds). We tested whether sequence complexity (i.e., including elaborate “derived” calls that are unique to geladas and absent in closely related taxa) or size (i.e., number of calls) may function (1) to counteract the challenges of living in a large group (overcoming conspecific noise and crowding, maintaining cohesion), or (2) to maintain social bonds with females. We found that an increase in conspecific noise contributed to the use of longer and more complex sequences. However, behavioral contexts in which the risk of separation was highest (i.e., traveling) were associated with only longer (but not more complex) sequences. We also found that sequence complexity (but not size) was associated with male-female bonding as complex call sequences were produced primarily when males were in close proximity to and approached females, and they led to males being groomed by females. Together, these findings suggest that, while a noisy backdrop of conspecific vocalizations might contribute to vocal complexity, the potential driver of gelada vocal complexity is the need to maintain cross-sex bonds. Why do some animals make many diverse sounds while others make only a few simple sounds? Broad comparisons suggest that sociality may be important as more social species (e.g., those with large group size and social bonding) tend to make more types of sounds. Yet, it remains unclear why gregarious species need an expanded call repertoire. Here, we take advantage of previous work on a highly social primate (geladas) that identified several complex vocalizations that contribute to gelada’s expanded vocal repertoire. To better understand why geladas evolved an expanded set of calls, we focus on the context where complex calls are produced and the responses those calls elicit. We found that the potential driver of the use of more call types is the need to maintain cross-sex bonds, suggesting an important role for male-female bonds in the evolution of vocal complexity.

Dietary niches of terrestrial cercopithecines from the Plio-Pleistocene Shungura Formation, Ethiopia: evidence from Dental Microwear Texture Analysis

This study aims to explore the feeding ecology of two terrestrial papionins, Papio and Theropithecus from the Shungura Formation in Ethiopia, the most complete stratigraphic and paleontological record of the African Plio-Pleistocene. Two aspects were evaluated using Dental Microwear Texture Analysis: differences in diet between the extinct genera and their extant relatives, and any potential dietary fluctuations over time. Amongst more than 2,500 cercopithecid dental remains, 154 Theropithecus molars and 60 Papio molars were considered. Thirty-nine extant wild baboons and 20 wild geladas were also considered. The results show that diets of extinct monkeys from Member G already differed between genera as it is the case for their extant representatives. The shearing facets on the Theropithecus molars display significant variations in microwear textures, suggesting several dietary shifts over time. Two events point to higher intakes of herbaceous monocots (tougher than dicots foliages), at about 2.91 Ma (between members B and C) and at 2.32 Ma (between members E and F). These two events are separated by an inverse trend at about 2.53 Ma (between members C and D). Some of these variations, such as between members E and F are supported by the enamel carbon isotopic composition of herbivorous mammals and with paleovegetation evidence.

Graminivory and Fallback Foods: Annual Diet Profile of Geladas (Theropithecus gelada) Living in the Simien Mountains National Park, Ethiopia

All primates show some dietary flexibility, particularly during food shortages. Foods consumed during times of scarcity (i.e., fallback foods) strongly influence the ecology and evolution of a species. Geladas (Theropithecus gelada) eat primarily graminoid leaves (i.e., grasses and sedges), but also consume other diet items (e.g., underground storage organs), especially in the dry season. We investigated the feeding ecology of wild geladas in the Sankaber region of the Simien Mountains National Park, Ethiopia across 12 mo. We asked how the gelada diet in this region, which is disturbed by livestock and agriculture, correlated with food availability and whether underground foods are fallback foods. We quantified the monthly diets of adults from eight reproductive units using instantaneous scan sampling, and seasonal aboveground and underground food availability using point-intercept transects and soil core sampling. Geladas primarily consumed graminoid leaves year-round (76.3% of the annual diet, 36.2–93.2% of the monthly diet) but spent considerable time consuming underground foods in the dry season (14.0% of the annual diet, 11.1–49.7% of the diet across dry season months). Graminoid consumption increased with graminoid availability, and underground food consumption decreased with graminoid availability. Underground food availability did not vary significantly between the dry and wet season sampling months, supporting the hypothesis that underground foods are fallback foods for geladas. We then compiled data from gelada feeding studies and found that underground foods are an important dry season diet item across study sites, but geladas rely more heavily on underground foods in habitats more heavily influenced by humans. Understanding the range and effects of primate dietary flexibility in human-modified habitats will contribute to a better understanding of how changing environments shape primate ecology and evolution.

Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.