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For most primates living in tropical forests, food resources occur in patchworks of different habitats that vary seasonally in quality and quantity. Efficient navigation (i.e., spatial memory-based orientation) towards profitable food patches should enhance their foraging success. The mechanisms underpinning primate navigating ability remain nonetheless mostly unknown. Using GPS long-term tracking (596 days) of one group of wild western lowland gorillas (Gorilla gorilla gorilla), we investigated their ability to navigate at long distances, and tested for how the sun was used to navigate at any scale by improving landmark visibility and/or by acting as a compass. Long episodic movements ending at a distant swamp, a unique place in the home range where gorillas could find mineral-rich aquatic plants, were straighter and faster than their everyday foraging movements relying on spatial memory. This suggests intentional targeting of the swamp based on long-distance navigation skills, which can thus be efficient over a couple of kilometres. Interestingly, for both long-distance movements towards the swamp and everyday foraging movements, gorillas moved straighter under sunlight conditions even under a dense vegetation cover. By contrast, movement straightness was not markedly different when the sun elevation was low (the sun azimuth then being potentially usable as a compass) or high (so providing no directional information) and the sky was clear or overcast. This suggests that gorillas navigate their home range by relying on visual place recognition but do not use the sun azimuth as a compass. Like humans, who rely heavily on vision to navigate, gorillas should benefit from better lighting to help them identify landmarks as they move through shady forests. This study uncovers a neglected aspect of primate navigation. Spatial memory and vision might have played an important role in the evolutionary success of diurnal primate lineages.

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Balantioides coli (=Balantidium coli), a large ciliated protozoan, is reported in multiple free-ranging and captive primate species, often in association with a clinical presentation that requires medical intervention. This report describes the clinical effectiveness of paromomycin sulfate against B.coli in zoo-kept mandrill monkeys (Mandrillus sphinx, at orally doses of 8-31 mg/kg, once daily (SID) for 7 days) and gorillas (Gorilla gorilla gorilla, at orally doses of 1.4-3.1 mg/kg, SID for 5 days).

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Although western lowland gorillas (Gorilla gorilla gorilla) are the most numerous and widespread gorilla subspecies, they have remained relatively unstudied. International tourism has been initiated at several sites in the Congo Basin, which necessitates habituation of gorillas to human presence. However, habituation has proven difficult due to several obstacles, including relatively low population densities, small group sizes, and thick understory vegetation. In this article, we propose refinements to current approaches to habituating western lowland gorillas that maximize safety and emphasize adaptive responses based on empirical evidence. In addition to reviewing published reports, our approach is informed by the recent habituation of the Mététélé group in the Djéké Triangle, an area that was recently included in the Nouabalé-Ndoki National Park in Republic of Congo. We evaluate progress in habituation according to time spent in the presence of the gorillas and their reactions to humans. The Mététélé group is composed of 14 individuals and has a home range that overlaps with two habituated gorilla groups. Early in the habituation process, we discovered that three of Mététélé's group members were individuals who had previously been habituated as members of other groups. The presence of these individuals expedited the habituation process. Familiarity with humans may have also reduced aggressive responses during the habituation process. The overall result is a refined step-by-step approach to the habituation of western lowland gorillas that includes procedures and assessments to meet best-practice guidelines and ensure the wellbeing of both gorillas and humans.

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We carried out a comparative analysis between the bacterial microbiota composition of zoo-housed western lowland gorillas and their wild counterparts through 16S rRNA gene amplicon sequencing. In addition, we characterised the carbohydrate-active and methanogenic potential of the zoo-housed gorilla (ZHG) microbiome through shotgun metagenomics and RNA sequencing. The ZHG microbiota showed increased alpha diversity in terms of bacterial species richness and a distinct composition from that of the wild gorilla microbiota, including a loss of abundant fibre-degrading and hydrogenic Chloroflexi. Metagenomic analysis of the CAZyome indicated predominant oligosaccharide-degrading activity, while RNA sequencing revealed diverse cellulase and hemi-cellulase activities in the ZHG gut, contributing to a total of 268 identified carbohydrate-active enzymes. Metatranscriptome analysis revealed a substantial contribution of 38% of the transcripts from anaerobic fungi and archaea to the gorilla microbiome. This activity originates from cellulose-degrading and hydrogenic fungal species belonging to the class Neocallimastigomycetes, as well as from methylotrophic and hydrogenotrophic methanogenic archaea belonging to the classes Thermoplasmata and Methanobacteria, respectively. Our study shows the added value of RNA sequencing in a multiomics approach and highlights the contribution of eukaryotic and archaeal activities to the gut microbiome of gorillas.

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In nonhuman animals, the phenomenon of rapid facial mimicry (RFM)-the automatic, involuntary, and rapid (<1 s) replication of others' facial expressions-has been mainly investigated in the playful domain. In immature lowland gorillas Gorilla gorilla gorilla both play face (PF) and full PF (FPF) are rapidly mimicked between the players. This makes the species suitable to test hypotheses on the factors influencing RFM during play. The observations on 3 captive groups of lowland gorillas (N = 27) revealed that contrary to expectations, the closeness of social bond negatively influenced the occurrence of RFM but it did not affect either RFM latency or its overlapping index (OVERLAP). RFM was affected by the degree of symmetry of play fighting: the more balanced the session, the higher the occurrence of RFM. Players of the same sex class responded faster than players of different sex. These findings suggest that RFM may help synchronizing behaviors of playmates matching in size (same-sex) and promote symmetric playful interactions. "Laughing together" (measured by the RFM OVERLAP) lasted longer when the responder perfectly mirrored the partner expression (PF→PF; FPF→FPF). If PF and FPF convey information on the different play roughness degree, through "laughing together" the players could coordinate their actions and share positive moods and playful intensity. If the perfect congruency in the motor resonance, also known as social sensitivity, can foster a possible emotional dialogue between gorillas remains to be investigated.

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Four female Japanese macaques (Macaca fuscata) from the same group as well as Wolf's guenon (Cercopithecus wolfi) and a Western lowland gorilla (Gorilla gorilla gorilla) from a second institution presented with vaginal foreign bodies in parallel with diseases of the urogenital tract or with endocrine disorders. These foreign bodies were associated with a mild to marked, diffuse vaginitis in all cases. Underlying pathological conditions consisted of a cavernous uterine hemangioma in a 20-year-old macaque, diffuse endometritis in a 21-year-old macaque, an in situ endometrial carcinoma in a 24-year-old macaque, endometritis and an ovarian cyst-like structure in the 27-year-old Western lowland gorilla, chronic cystitis and chronic renal disease in a 24-year-old macaque, and a history of hypothyroidism with irregular reproductive cycles in the 12-year-old Wolf's guenon. Vaginal foreign bodies have been reported in nonhuman primates used in biomedical research, but their concurrence with underlying conditions has not been explored. In women, vaginal foreign bodies have been linked to serious underlying medical conditions. This case series emphasizes the recommendation to investigate this abnormal behavior for underlying medical or adverse psychosocial conditions in primates under human care.

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Among African great apes, play is virtually absent between adult lowland gorillas (Gorilla gorilla gorilla). Here, we report an extremely rare case of adult-adult play observed in the lowland gorilla group housed at La Vallée de Singes (France). We recorded three playful interactions between the silverback and an adult lactating female. Given the diverse causal and functional nature of play, different factors may join in promoting this behaviour. In our group, contrary to what has been shown by previous studies in wild and captive gorillas, adult females spent more time in spatial proximity with the silverback than with other females. Hence, the probability of social interaction (including play) between silverback and adult females was enhanced. Moreover, the motivation of the lactating female to play might be an effect of oxytocin, a hormone that reaches high concentration levels during lactation and that promotes social affiliation. The fact that play invitations were always performed by the female might support this hypothesis. Certainly, we cannot exclude the possibility that the play event is a group idiosyncrasy or an artefact of captivity, even though the subjects never showed abnormal behaviour. Structurally, play sessions showed a suitable degree of pattern variability and switching frequency from one pattern to another. The proportion of offensive patterns was higher in the female during play and in the male during aggression, which conforms to the role reversal play phenomenon. In conclusion, this report confirms that the absence of evidence is not the evidence of absence. It is likely that under particular physiological or socio-ecological conditions, adult-adult play may be manifested as an "unconventional" part of gorilla social behaviour.

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A goal of the comparative approach is to test a variety of species on the same task. Here, we examined whether the factors that helped capuchin monkeys improve their performance in a dichotomous choice task would generalize to three other primate species: orangutans, gorillas, and drill monkeys. In this task, subjects have access to two options, each resulting in an identical food, but one (the ephemeral option) is only available if it is chosen first, whereas the other one (the permanent option) is always available. Therefore, the food-maximizing solution is to choose the ephemeral option first, followed by the permanent option for an additional reward. On the original version (plate task), the options were discriminated by the color and pattern of the plates holding the food, while on two subsequent versions we used altered cues that we predicted would improve performance: (1) the color of the foods themselves (color task), which we hypothesized was relevant to primates, who choose foods rather than substrates on which foods are found when foraging, and (2) patterned cups covering the foods (cup task), which we hypothesized would help primates avoid the prepotent response associated with visible food. Like capuchins, all three species initially failed to solve the plate task. However, while orangutans improved their performance from the plate to the color task, they did not for the cup task, and only a few gorillas and no drills succeeded in either task. Unfortunately, our ability to interpret these data was obscured by differences in the subjects' level of experience with cognitive testing and practical constraints that precluded the use of completely identical procedures across species. Nonetheless, we consider what these results can tell us, and discuss the value of conducting studies across multiple sites despite unavoidable differences.

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Primates, especially apes, are popular with the public, often attracting large crowds. These crowds could cause behavioral change in captive primates, whether positive, neutral, or negative. We examined the impact of visitors on the behavior of six western lowland gorillas (Gorilla gorilla gorilla), observing the troop over 6 weeks during high season (4.5 hr/day, 35 days, May-July 2016). We used focal scan sampling to determine activity budget and enclosure usage, and focal continuous sampling to identify bouts of anxiety-related behavior (visitor-directed vigilance, self-scratching, and aggression). Both daily zoo-entry numbers (VGATE ) and instantaneous crowds at the exhibit (VDENSITY ) were measured. Overall, VGATE had little effect across behaviors. However, consistent with the more acute time frame of measurement, VDENSITY was a better predictor of behavior; at high crowd volumes, we observed significant group-level changes in activity budget (increased inactivity, increased locomotion, and decreased environment-related behaviors), increase in some anxiety-related behaviors, and decreased enclosure usage. Although contributing similar effects, it could not be determined if crowd numbers, composition, or noise most affected the troop, nor any chronic effects of exposure to large crowds. Nevertheless, our findings suggest that measures to minimize the impacts of large crowds at the exhibit would be beneficial. Furthermore, we highlight potential discrepancies between common methods for measuring visitor numbers: VGATE is less sensitive to detecting visitor effects on behavioral indices than VDENSITY . Future studies should appropriately match the biological time frame of welfare indicators and visitor measures used to ensure the reliability of findings.

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Human activities can lead to a shift in wildlife species' spatial distribution. Understanding the specific effects of human activities on ranging behavior can improve conservation management of wildlife populations in human-dominated landscapes. This study evaluated the effects of forest use by humans on the spatial distribution of mammal species with different behavioral adaptations, using sympatric western lowland gorilla and central chimpanzee as focal species. We collected data on great ape nest locations, ecological and physical variables (habitat distribution, permanent rivers, and topographic data), and anthropogenic variables (distance to trails, villages, and a permanent research site). Here, we show that anthropogenic variables are important predictors of the distribution of wild animals. In the resource model, the distribution of gorilla nests was predicted by nesting habitat distribution, while chimpanzee nests were predicted first by elevation followed by nesting habitat distribution. In the anthropogenic model, the major predictors of gorilla nesting changed to human features, while the major predictors of chimpanzee nesting remained elevation and the availability of their preferred nesting habitats. Animal behavioral traits (body size, terrestrial/arboreal, level of specialization/generalization, and competitive inferiority/superiority) may influence the response of mammals to human activities. Our results suggest that chimpanzees may survive in human-encroached areas whenever the availability of their nesting habitat and preferred fruits can support their population, while a certain level of human activities may threaten gorillas. Consequently, the survival of gorillas in human-dominated landscapes is more at risk than that of chimpanzees. Replicating our research in other sites should permit a systematic evaluation of the influence of human activity on the distribution of mammal populations. As wild animals are increasingly exposed to human disturbance, understanding the resulting consequences of shifting species distributions due to human disturbance on animal population abundance and their long-term survival will be of growing conservation importance.

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The use of tools, long thought to be uniquely human, has now been observed in other animal taxa including several species of birds, non-primate mammals as well as some non-human primate species. Chimpanzees, one of humankind's closest living relatives, exceed all other non-human animal species as they have been reported to use an exceptionally large toolkit. However, relatively little is known about the tool-use skills of the other great ape species. While the majority of tools described are inanimate objects, the use of social tools has received relatively little attention. Here we provide the first evidence of naturally occurring spontaneous exploitative behaviour of a conspecific as a social tool for food acquisition in non-human animals. We observed gorillas in captivity utilising a conspecific as a ladder to gain access to unreachable food. We discuss our findings in the light of other studies on social tool use and suggest the need for more nuanced interpretations of gorillas' cognitive skills.

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The field of environmental enrichment for zoo animals, particularly great apes, has been revived by technological advancements such as touchscreen interfaces and motion sensors. However, direct animal-computer interaction (ACI) is impractical or undesirable for many zoos. We developed a modular cuboid puzzle maze for the troop of six Western lowland gorillas (Gorilla gorilla gorilla) at Bristol Zoo Gardens, United Kingdom. The gorillas could use their fingers or tools to interact with interconnected modules and remove food rewards. Twelve modules could be interchanged within the frame to create novel iterations with every trial. We took a screen-free approach to enrichment: substituting ACI for tactile, physically complex device components, in addition to hidden automatic sensors, and cameras to log device use. The current study evaluated the gorillas' behavioral responses to the device, and evaluated it as a form of "cognitive enrichment." Five out of six gorillas used the device, during monthly trials of 1 h duration, over a 6 month period. All users were female including two infants, and there were significant individual differences in duration of device use. The successful extraction of food rewards was only performed by the three tool-using gorillas. Device use did not diminish over time, and gorillas took turns to use the device alone or as one mother-infant dyad. Our results suggest that the device was a form of cognitive enrichment for the study troop because it allowed gorillas to solve novel challenges, and device use was not associated with behavioral indicators of stress or frustration. However, device exposure had no significant effects on gorilla activity budgets. The device has the potential to be a sustainable enrichment method in the long-term, tailored to individual gorilla skill levels and motivations. Our study represents a technological advancement for gorilla enrichment, an area which had been particularly overlooked until now. We wholly encourage the continued development of this physical maze system for other great apes under human care, with or without computer logging technology.

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Echinococcus multilocularis is the etiologic agent of alveolar echinococcosis (AE), a severe and potentially fatal larval cestode infection primarily affecting the liver. AE is known to occur in dead-end intermediate hosts, including humans and nonhuman primates. Between 1999 and 2016, AE was diagnosed in seven western lowland gorillas (Gorilla gorilla gorilla), all from a Swiss zoo. Six gorillas died of the disease. One individual is still alive, receives continuous albendazole medication, and shows no clinical signs. Most infected animals remained asymptomatic for years. Only one young gorilla showed early signs of acute discomfort and abdominal pain. In the final stage of the disease, affected animals died suddenly, or showed a short course of nonspecific but severe clinical signs, including lethargy, recumbency, abdominal enlargement, and anorexia. Postmortem examination confirmed hepatic AE complicated by peritonitis in most cases. Echinococcus multilocularis infection may remain undetected because of a very long incubation period. Hematological and biochemical parameters rarely showed abnormalities in this phase. Thus, inclusion of abdominal hepatic ultrasound examination and serology is recommended for early AE detection in routine examinations of gorillas in endemic areas or where food is potentially contaminated with E. multilocularis eggs. Ultrasound or computed tomography was useful to monitor progression and to estimate the volumetric extension of the hepatic lesions. Current medication with albendazole, which proved to be effective for human patients, was not able to stop progression of hepatic lesions in gorillas. Therefore, its therapeutic value remains questionable in gorillas. However, long-term oral albendazole treatment proved to be safe, and therapeutic plasma levels published for humans were achieved. Preventive measures such as thermo-treatment of food or vaccination of gorillas and other nonhuman primates should be considered in areas where E. multilocularis is present.

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In order to gain an understanding of the frequency of veterinary intervention during the periparturient period of western lowland gorillas (Gorilla gorilla gorilla) in captivity between 1996 and 2016, a survey was sent to institutions associated with the Association of Zoos and Aquariums' Gorilla Species Survival Plan®. A total of 193 births were reported during the survey period, from 51/53 institutions. There were six incidences of prolonged labor (longer than 6 hr; 3%), six cases of cesarean section (3%), and three incidences of veterinary intervention that did not involve a cesarean section (2%). Fifty-one gorilla neonates (26%) were assist-reared (required intervention lasting longer than 24 hr). Out of 51 attempts to reintroduce neonates to dams or surrogates, 42 were accepted (82%), while nine attempts (18%) were deemed failures. The age group with the highest rate of maternal or surrogate acceptance after reintroduction was between 6 and 12 mo of age. Compared to data from a 1981 survey, the percentage of assist-reared gorillas decreased from 64% to 26%. Results show that veterinary intervention in the periparturient period is low, and there is a high rate of acceptance of neonates by either the dam or a surrogate after intervention. Advances in captive husbandry and veterinary knowledge have led to a reduced risk of veterinary intervention during gorilla parturition; however, the long-term effects on behavioral development of the neonate should be considered before removal of the infant from the dam for any period of time.

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An onset of respiratory disease in a captive bachelor group (n = 3) of western lowland gorillas (Gorilla gorilla gorilla) was concomitant with peak attendance of visitors at the institution and with unwanted occurrences of food items being thrown in the gorillas' enclosure. While the condition of two individuals improved with supportive therapy and antibiotics, the third gorilla died three days following initiation of treatment. A fatal bacterial pneumonia, secondary to an infection by a human parainfluenza virus 2 (HIPV-2), was considered to be the cause of death based on histopathology, lung cultures, and reverse transcription PCR. HPIV-2 activity in the human population of the province was detected for that period, including the same viral strain. This report confirms a HPIV-2 respiratory illness and associated death in a gorilla. Clinical presentation and context suggest conspecifics were also affected and that contaminated food thrown by visitors may have been the source of infection.

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Corridors are intended to increase species survival by abating landscape fragmentation resulting from the conversion of natural habitats into human-dominated matrices. Conservation scientists often rely on 1 type of corridor model, typically the least-cost model or current-flow model, to construct a linkage design, and their choice is not usually based on theory or empirical evidence. We developed a method to empirically confirm whether corridors produced by these 2 models are used by target species under current landscape conditions. We applied this method in the Gamba landscape between 2 national parks in southwestern Gabon. We collected signs of presence of African forest elephant (Loxodonta cyclotis), forest buffalo (Syncerus caffer nanus), and 2 apes, western lowland gorilla (Gorilla gorilla gorilla) and central chimpanzee (Pan troglodytes troglodytes), on transects. We used patch-occupancy models to identify least-cost and current-flow corridors for these 4 species. On average, 28.7% of current-flow corridors overlapped with least-cost corridors, confirming that the choice of corridor model can affect the location of the resulting linkage design. We validated these corridors by monitoring signs and examining camera detections on new transects within and outside modeled corridors. Current-flow corridors performed better than least-cost corridors for elephants, whereas the opposite was found for buffalo and apes. Locations of the highest priority corridors for the 3 taxa did not overlap, and only 18.3% of their combined surface was common among 2 species. We used centrality metrics to calculate the average contribution of corridor pixels to landscape connectivity and derived an index that can be used to prioritize corridors. As a result, we recommend protecting at least 17.4% of the land surface area around Gamba town to preserve the preferred travel routes of the target species.

Selección Empírica entre Diseños de Menor Costo y de Flujo de Corriente para Establecer Corredores de Fauna en Gabón Resumen La intención de los corredores es incrementar la supervivencia de las especies abatiendo la fragmentación del paisaje que resulta de la conversión de los hábitats naturales en matrices dominadas por humanos. Los científicos de la conservación con frecuencia dependen de un tipo de modelo de corredor, comúnmente el modelo de menor costo o el de flujo de corriente para construir un diseño de conexiones y su elección no suele estar basada en evidencia teórica o empírica. Desarrollamos un método para confirmar empíricamente si los corredores producidos por estos dos modelos son usados por las especies diana bajo las condiciones actuales del paisaje. Aplicamos este método en el paisaje de Gamba entre dos parques nacionales al suroeste de Gabón. Recolectamos señales de la presencia del elefante de bosque africano (Loxodonta cyclotis), el búfalo de bosque (Syncerus caffer nanus), y dos primates: el gorila occidental de tierras bajas (Gorilla gorilla gorilla) y el chimpancé central (Pan troglodytes troglodytes) a lo largo de transectos en esta zona. Usamos modelos de ocupación de fragmentos para identificar los corredores de menor costo y los de flujo de corriente para estas cuatro especies. En promedio, el 28.7% de los corredores de flujo de corriente se traslaparon con los corredores de menor costo, lo que confirmó que la elección de modelo de corredor puede afectar la ubicación del diseño de conexiones resultante. Validamos estos corredores por medio del monitoreo de señales y la examinación de detecciones con cámaras en transectos nuevos dentro y fuera de los corredores modelados. Los corredores de flujo de corriente tuvieron un mejor desempeño que los corredores de menor costo para los elefantes, mientras que fue el caso contrario para los búfalos y los primates. La ubicación de los corredores con mayor prioridad para los tres taxones no se traslapó y sólo el 18.3% de las superficies combinadas fue común para dos especies. Usamos medidas de centralidad para calcular la contribución promedio de los pixeles del corredor hacia la conectividad del paisaje y derivamos un índice que puede usarse para priorizar los corredores. Como resultado de nuestro estudio recomendamos proteger al menos el 17.4% del área de superficie terrestre alrededor del poblado de Gamba para preservar las rutas de viaje de las especies diana.

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Cardiac disease is a leading cause of mortality in zoo-housed western lowland gorillas (Gorilla gorilla gorilla). The gut microbiome is associated with cardiac disease in humans and similarly the gut microbiome may be associated with cardiac diseases in close relatives of humans, such as gorillas. We assessed the relationship between cardiac disease and gut bacterial composition in eight zoo-housed male western lowland gorillas (N = 4 with and N = 4 without cardiac disease) utilizing 16S rRNA gene analysis on the Illumina MiSeq sequencing platform. We found bacterial composition differences between gorillas with and without cardiac disease. Bacterial operational taxonomic units from phyla Bacteroidetes, Spirochaetes, Proteobacteria and Firmicutes were significant indicators of cardiac disease. Our results suggest that further investigations between diet and cardiac disease could improve the management and health of zoo-housed populations of this endangered species.

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Serum 25-hydroxyvitamin D concentrations were assessed in subadult to adult captive lowland gorillas ( Gorilla gorilla gorilla) (n = 26) at two institutions with different husbandry and management practices. Serum 25-hydroxyvitamin D (25[OH]D) concentrations for gorillas managed predominantly indoors was low (14.2 ± 5.9 ng/ml), despite consuming commercial biscuits fortified with vitamin D3. Concentrations of 25(OH)D in gorillas with near daily outdoor access were significantly higher than gorillas managed indoors, although many individuals still had serum values below concentrations recommended for adult humans. Consideration should be given to assessing 25(OH)D concentrations in all captive gorillas and providing specific supplementation, particularly to juveniles without access to direct sunlight.

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Syngamid strongylids of the genus Mammomonogamus undoubtedly belong among the least known nematodes with apparent zoonotic potential and the real diversity of the genus remains hard to evaluate without extensive molecular data. Eggs of Mammomonogamus sp. are frequently found in feces of African forest elephants (Loxodonta cyclotis) and western lowland gorillas (Gorilla gorilla gorilla) in Dzanga-Sangha Protected Areas. Using sedimentation-based coproscopic techniques, we found the eggs of Mammomonogamus in 19·7% elephant and 54·1% gorilla fecal samples with 8-55 and 1-24 eggs per gram of fecal sediment for elephants and gorillas, respectively. We used a combination of light microscopy, scanning electron microscopy and analysis of cytochrome c oxidase subunit I (cox1) and a partial sequence of 18S rDNA isolated from single eggs to test the hypothesis of possible Mammomonogamus conspecificity in gorillas and elephants. Whereas 18S rDNA sequences were identical in both gorillas and elephants, we distinguished seven different haplotypes within the cox1. Two haplotypes were found in both gorillas and elephants suggesting sharing of Mammomonogamus. Assignment of the parasite to M. loxodontis is proposed. Provided sequences represent the first genomic data on Mammomonogamus spp.

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