The effect of low- and high-fiber diets on the population of entodiniomorphid ciliates Troglodytella abrassarti in captive chimpanzees (Pan troglodytes)

Troglodytella abrassarti is an intestinal entodiniomorphid ciliate commonly diagnosed in the feces of wild and captive chimpanzees (Pan troglodytes). Entodiniomorphids could be considered to have a mutualistic relationship with the great apes, in that the ciliates benefit from the intestinal ecosystem of the host, while also contributing to the fiber fermentation process. We examined the effect of diet on the infection intensities of T. abrassarti in two captive chimpanzees in the Liberec Zoo, Czech Republic. The chimpanzees were fed a low-fiber diet (LFD) with 14% neutral detergent fiber (NDF) and a high-fiber diet (HFD; 26% NDF) for 10 days with one transition, and two 10-day adaptation periods. Fecal samples were examined coproscopically with the merthiolate-iodine-formaldehyde concentration (MIFC) technique, in order to quantify the number of ciliates per gram of feces. A significant trend of increasing T. abrassarti numbers was observed when the animals were fed the LFD, compared to when they were fed the HFD. Our results suggest, however, that infection intensities of T. abrassarti in captive chimpanzees are not influenced primarily by the amount of fiber in the diet, but rather by the dietary starch concentration (HFD: 1%; LFD: 8%).     

The ciliate, Troglodytella abrassarti, contributes to polysaccharide hydrolytic activities in the chimpanzee colon

Entodiniomorphid ciliates are intestinal protists inhabiting the colons of African great apes. The participation of intestinal entodiniomorphid ciliates in ape hindgut digestion has been proposed, but little data have been available to support the hypothesis. We measured the specific activities of carboxymethyl cellulase, xylanase, inulinase, and α-amylase against different polysaccharides in the feces of captive chimpanzees and evaluated the participation of the entodiniomorphid ciliate, Troglodytella abrassarti, in these activities. T. abrassarti contributed to the total fecal hydrolytic activities of CM-cellulase by 16.2%, α-amylase by 5.95%, and xylanase by 0.66%. Inulinase activity in T. abrassarti samples was not measurable at reaction conditions used. The ciliates, T. abrassarti, actively participate in the chimpanzee hindgut fermentation of fiber and starch.     

The Intestinal Entodiniomorph Ciliates of Wild Lowland Gorillas (Gorilla gorilla gorilla) in Gabon,West Africa

Examination of 109 fecal samples from wild lowland gorillas revealed the presence of five species of entodiniomorph ciliates: Troglodytella ahrassarti, Troglodytella gorillae, and three unclassified species. These latter three species were also found in the feces of a captive gorilla in Gabon and are considered to be intestinal parasites or commensals.     

Codetection of Respiratory Syncytial Virus in Habituated Wild Western Lowland Gorillas and Humans During a Respiratory Disease Outbreak

Pneumoviruses have been identified as causative agents in several respiratory disease outbreaks in habituated wild great apes. Based on phylogenetic evidence, transmission from humans is likely. However, the pathogens have never been detected in the local human population prior to or at the same time as an outbreak. Here, we report the first simultaneous detection of a human respiratory syncytial virus (HRSV) infection in western lowland gorillas (Gorilla gorilla gorilla) and in the local human population at a field program in the Central African Republic. A total of 15 gorilla and 15 human fecal samples and 80 human throat swabs were tested for HRSV, human metapneumovirus, and other respiratory viruses. We were able to obtain identical sequences for HRSV A from four gorillas and four humans. In contrast, we did not detect HRSV or any other classic human respiratory virus in gorilla fecal samples in two other outbreaks in the same field program. Enterovirus sequences were detected but the implication of these viruses in the etiology of these outbreaks remains speculative. Our findings of HRSV in wild but human-habituated gorillas underline, once again, the risk of interspecies transmission from humans to endangered great apes.     

Evaluation of different storage methods to characterize the fecal bacterial communities of captive western lowland gorillas (Gorilla gorilla gorilla)

Freezing is considered to be the best method for long-term storage of bacterial DNA from feces; however this method cannot be usually applied for samples of wild primates collected in the challenging conditions of the tropical forest. In order to find an alternative conservation method of fecal samples from wild great apes, we compared freezing with other fixation methods. Fecal samples from 11 captive gorillas (Gorilla gorilla gorilla) from three Czech Zoos were stored using freezing, RNA Stabilization Reagent (RNAlater), and 96% ethanol. Subsequently, the samples were examined using culture-independent methods (PCR-DGGE, and Real-time PCR) to qualitatively and quantitatively assess fecal microbiota composition and to compare differences among the storage methods. Noticeably, freezing samples resulted in the highest recoveries of DNA. No significant differences in DNA recovery were found between freezing and using RNAlater; however, significantly lower DNA concentrations were recovered from samples stored in 96% ethanol. Using PCR-DGGE we found that either 96% ethanol, RNAlater or freezing were suitable for preserving bacterial DNA; however fingerprints obtained from RNAlater storage were more similar to those obtained from the frozen method; in comparison to the patterns resulting from storing samples in ethanol. Using qPCR, frozen samples yielded the highest values of bacterial counts, with the exception of Enterobacteriaceae, which showed the highest numbers using samples stored in ethanol. Sequences of amplicons obtained from PCR-DGGE belonged to the families Clostridiaceae, Lactobacillaceae, Staphylococcaceae, and Lachnospiraceae, phylum Firmicutes; however most amplicons showed sequence similarity to previously uncultured microorganisms. Bacteria belonging to the phylum Firmicutes were the most frequently identified species in the fecal bacterial communities of captive western gorillas. The study showed that RNAlater is an optimal storage method when freezing is not possible.     

Non‐invasive fecal hormone analysis and behavioral observations for monitoring stress responses in captive western lowland gorillas (Gorilla gorilla gorilla)

Non‐invasive techniques for monitoring the stress response in captive western lowland gorillas (Gorilla gorilla gorilla) were investigated. Fecal samples for cortisol measurement and concurrent behavioral data were collected from six individuals in a socially housed gorilla group (one adult male, three adult females and their three offspring) over a 7‐month period. Despite inter‐individual variation in the dynamics of fecal cortisol concentrations over time, several major secretory peaks coincided across individuals. High cortisol concentrations in feces were correlated with induced stressors or behavioral observations indicating high social tension, with a 1–2 day lag period. Entry progression order of the gorillas into a den complex and a supplant‐based dominance index were suitable indicators of overall dominance hierarchies, and fluctuations over time reflected periods of instability. Diurnal variation in fecal cortisol was not apparent when comparing afternoon and morning samples, however the sample collection interval was relatively short (3–5 hr). These results demonstrate the feasibility of monitoring stress responses based on the dynamics of both fecal cortisol excretion and behavior. This non‐invasive approach may be used for gauging responses to changes in husbandry, environment and group structure of captive gorillas. Zoo Biol 0:1–15, 2005. © 2005 Wiley‐Liss, Inc.     

Species association of hepatitis B virus (HBV) in non-human apes; evidence for recombination between gorilla and chimpanzee variants

Hepatitis B virus (HBV) infections are widely distributed in humans, infecting approximately one third of the world's population. HBV variants have also been detected and genetically characterised from Old World apes; Gorilla gorilla (gorilla), Pan troglodytes (chimpanzee), Pongo pygmaeus (orang-utan), Nomascus nastusus and Hylobates pileatus (gibbons) and from the New World monkey, Lagothrix lagotricha (woolly monkey). To investigate species-specificity and potential for cross species transmission of HBV between sympatric species of apes (such as gorillas and chimpanzees in Central Africa) or between humans and chimpanzees or gorillas, variants of HBV infecting captive wild-born non-human primates were genetically characterised. 9 of 62 chimpanzees (11.3%) and two from 11 gorillas (18%) were HBV-infected (15% combined frequency), while other Old world monkey species were negative. Complete genome sequences were obtained from six of the infected chimpanzee and both gorillas; those from P. t .ellioti grouped with previously characterised variants from this subspecies. However, variants recovered from P. t. troglodytes HBV variants also grouped within this clade, indicative of transmission between sub-species, forming a paraphyletic clade. The two gorilla viruses were phylogenetically distinct from chimpanzee and human variants although one showed evidence for a recombination event with a P.t.e.-derived HBV variant in the partial X and core gene region. Both of these observations provide evidence for circulation of HBV between different species and sub-species of non-human primates, a conclusion that differs from the hypothesis if of strict host specificity of HBV genotypes.     

Molecular diversity of entodiniomorphid ciliate Troglodytella abrassarti and its coevolution with chimpanzees

The entodiniomorphid ciliate Troglodytella abrassarti is a colonic mutualist of great apes. Its host specificity makes it a suitable model for studies of primate evolution. We explored molecular diversity of T. abrassarti with regard to large geographical distribution and taxonomic diversity of its most common host, the chimpanzee. We found a very low diversification of T. abrassarti in chimpanzees across Africa. Distribution of two types of T. abrassarti supports evolutionary separation of the Western chimpanzee, P. t. verus, from populations in Central and East Africa. Type I T. abrassarti is probably a derived form, which corresponds with the Central African origin of chimpanzees and a founder event leading to P. t. verus. Exclusivity of the respective types of T. abrassarti to Western and Central/Eastern chimpanzees corroborates the difference found between an introduced population of presumed Western chimpanzees on Rubondo Island and an autochthonous population in mainland Tanzania. The identity of T. abrassarti from Nigerian P. t. ellioti and Central African chimpanzees suggests their close evolutionary relationship. Although this contrasts with published mtDNA data, it corroborates current opinion on the exclusive position of P. t. verus within the chimpanzee phylogeny. The type of T. abrassarti occurring in Central and East African common chimpanzee was confirmed also in bonobos. This may point to the presence of an ancestral Type II found throughout the Lower Guinean rainforest dating back to the common Pan ancestor. Alternatively, the molecular uniformity of T. abrassarti may imply a historical overlap of the species' distribution ranges.     

Use of buckets as tools by Western lowland gorillas

While all great apes have been documented to use tools, gorillas are arguably the least proficient tool users. In 2009, a Western lowland gorilla (Gorilla gorilla gorilla) at the Buffalo Zoo was observed using a bucket, which had been provided as part of normal enrichment, as a tool to collect water. We conducted a brief, ad libitum investigation to confirm the validity of the initial observation. We then carried out a systematic investigation of the behavior in 2010. We collected 72 hr of videotaped data and tested the null hypothesis that the gorillas did not differ in their prevalence of engaging in bucket-use behaviors. We documented that all four adult gorillas in the group used buckets as drinking tools; however, there was significant individual variation in frequency and type of use of buckets. Four of the eight behaviors showed significant variation among individuals. The silverback male and the youngest adult female contacted and held the bucket significantly more than the remaining two adult females. The young female carried and drank from the bucket significantly more than any other individual. Furthermore, she was observed to fill the bucket with water four of the six times during which this behavior was observed. These data provide evidence of the ability of gorillas to utilize tools, given the appropriate environmental conditions. We continue to explore the abilities of gorillas to recognize the functionality of buckets as tools.     

Variability in the developmental life history of the genus Gorilla

Life history is influenced by factors both intrinsic (e.g., body and relative brain size) and extrinsic (e.g., diet, environmental instability) to organisms. In this study, we examine the prediction that energetic risk influences the life history of gorillas. Recent comparisons suggest that the more frugivorous western lowland gorilla shows increased infant dependence, and thus a slower life history, than the primarily folivorous mountain gorilla to buffer against the risk of starvation during periods of food unpredictability. We further tested this hypothesis by incorporating additional life history data from wild western lowland gorillas and captive western lowland gorillas with the assumption that the latter live under ecological conditions of energetic risk that more closely resemble those of mountain gorillas and thus should show faster life histories than wild members of the species. Overall, we found captive western lowland and wild mountain gorillas to have faster developmental life histories than wild western lowland gorillas, weaning their infants approximately a year earlier and thus reducing interbirth intervals by a year. These results provide support that energetic risk plays an important role in determining gorilla life history. Unlike previous assertions, gorillas do not have substantially faster life histories, at least at the genus level, than other great apes. This calls for a re‐evaluation of theories concerning comparative ape life history and evolution and highlights the need for data from additional populations that vary in energetic risk. Am J Phys Anthropol 152:165–172, 2013. © 2013 Wiley Periodicals, Inc.     

Discrepancies in the occurrence of Balantidium coli between wild and captive African great apes

Balantidium coli is a ciliate reported in many mammalian species, including African great apes. In the former, asymptomatic infections as well as clinical balantidiasis have been reported in captivity. We carried out a cross-sectional study of B. coli in African great apes (chimpanzees, bonobos, and both species of gorillas) and examined 1,161 fecal samples from 28 captive facilities in Europe, plus 2 sanctuaries and 11 wild sites in Africa. Samples were analyzed with the use of Sheather's flotation and merthiolate-iodine-formaldehyde (MIFC) sedimentation. MIFC sedimentation was the more sensitive technique for diagnostics of B. coli in apes. Although not detected in any wild-ape populations, B. coli was diagnosed in 52.6% of captive individuals. Surprisingly, in the apes' feces, trophozoites of B. coli were commonly detected, in contrast with other animals, e.g., Old World monkeys, pigs, etc. Most likely reservoirs for B. coli in captive apes include synantropic rats. High starch diets in captive apes are likely to exacerbate the occurrence of balantidiasis in captive apes.     

Endoparasites of western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic

A coprologic study of free-ranging western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Dzangha-Ndoki National Park, Central African Republic (2 degrees 51'34'N, 16 degrees 28'03'E) was conducted from October 1999 to November 2000. All 75 fecal samples examined were positive for endoparasites, and each contained at least two species. Parasites present included two genera of amoebae, entodiniomorph ciliates, including Prototapirella gorillae, Troglodytella spp., and Gorillophilus thoracatus, a Balantidium-like organism, strongyle/trichostrongyle eggs (including a presumptive Mammomonogamus sp. and several other genera), Strongyloides sp., Probstmayria sp., a spirurid, a trichuroid, and several unidentified trematodes. Flagellates and cestodes were not found. Despite the presence of a variety of parasite genera, in general, levels of parasitism were low. These data provide baseline parasitologic data for this population as part of a comprehensive health-monitoring program. With the advent of ecotourism in this study area, continued monitoring is indicated for insuring the health of both gorillas and humans in the Bai Hokou study area.     

A preliminary behavioral comparison of two captive all-male gorilla groups

Gorillas live in polygamous harem groups, generally composed of one male, several adult females, and their offspring. With an equal numbers of male and female gorillas born in captivity, however, housing gorillas in social breeding units inevitably means that some males will not have access to female social partners. Thus, the future of the captive gorilla population depends on the collective ability of zoos to house equal numbers of males and females. This study examined the behavioral profiles of two all-male groups of captive lowland gorillas (Gorilla gorilla gorilla) to provide information on this type of housing situation. One group consisted of three subadult individuals, while the other consisted of two subadults and a silverback. Data were collected during two 6-month intervals, for a total of 284 hr. The behavioral profiles of the animals were stable over the course of the study but proximity patterns changed. Differences in feeding, solitary play, and object-directed behavior were found between groups, while no significant differences were observed in affiliative or agonistic social behavior. At both institutions, group cohesion appeared to be high, particularly between subadults; these individuals spent approximately 10% of their time engaging in social behavior and 25-50% of their time in close proximity (within 5 m). However, the Zoo Atlanta males spent significantly more time within 1 m and 5 m of each other than the Santa Barbara males, which may reflect a higher level of cohesiveness among members of the Zoo Atlanta group. The behavioral profiles of the animals in this study were similar to those found in bachelor groups of wild mountain gorillas. One notable exception was the absence of homosexual behavior between the silverback and subadults in Santa Barbara and the low frequency of this behavior between subadults in both groups. Although more longitudinal data are needed, these data suggest that all-male groups can be a feasible housing strategy for males at certain periods of their life span. Zoo Biol 20:27-40, 2001. Copyright 2001 Wiley-Liss, Inc.     

Influence of social and environmental factors on nesting behaviour in captive gorillas (Gorilla gorilla gorilla)

Field studies on gorilla sleeping sites usually emphasize environmental influences on nest site selection, as individual nesting behaviours are usually not observed directly. In captivity, nesting behaviour and influencing factors are often overlooked. In the present study, the sleeping sites of members of a captive group of 16-21 gorillas were analysed, based on 152 nights over a 5-year period. Subadults tended to sleep apart from adults but clustered around the oldest blackback male. Full siblings and mothers with offspring were often nearest neighbours. Some sleeping dyads notably endured. Neither age of offspring nor rank of adult females influenced neighbour choice or distances; an interadult distance of 1.5-3 m was typical. Group dynamics were reflected in nesting arrangements. We suggest that possibilities for co-nesting and choice of sleeping sites should be provided to improve the welfare of captive gorillas and other great apes.     

Infant cradling in a captive mother gorilla

The purpose of the study presented here was to investigate the handedness and cradling preferences of a mother gorilla (Gorilla gorilla) from the Metro Toronto Zoo. The study also examined preferences for handedness for each member of the captive group. Observational data were collected using scan sampling at 60‐sec intervals. Handedness was determined with a coordinated bimanual tube test using peanut butter spread on the interior of a PVC tube. Our findings were largely consistent with the literature on laterality in African apes by documenting a left‐side cradling bias for one apparently ambidextrous captive gorilla mother. This bias was associated with a left head positioning preference by her infant. Although based on a single mother/infant pairing, this study indicates that cradling bias is not always determined by maternal handedness. Zoo Biol 27:420–426, 2008. © 2008 Wiley‐Liss, Inc.     

Paternity determination in captive lowland gorillas and orangutans and wild mountain gorillas by microsatellite analysis

Paternity exclusion studies provide useful information for testing certain theories of behavioral ecology and for the management and conservation of both wild and captive populations of endangered species. This study used eight human nuclear microsatellite loci, in the absence of species-specific PCR primers, to genetically identify the sires of 12 captive lowland gorillas (Gorilla gorilla gorilla) and 2 captive orangutans (Pongo pygmaeus pygmaeus andPongo p. abelii). Parentage assignments were confirmed by excluding all except a single potential sire for each offspring with the least two loci. Sire-offspring relationships were verified in 12 of the 14 cases, and reassigned in the case of two gorilla offspring. The orangutan paternity typing was supplemented by DNA fingerprinting. Additionally, five of the eight microsatellite loci, in conjunction with behavioral data, were used for a non-exhaustive set of paternity exclusions for five wild mountain gorillas (Gorilla g. beringei). The eight loci described in this study should be useful additions to the tools available for the study of genetics in the great apes.     

Population Density of Chimpanzees and Gorillas in the Petit Loango Reserve,Gabon: Employing a New Method to Distinguish Between Nests of the Two Species

We studied the vegetation and population density of chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in the Petit Loango Reserve, Gabon. The study site consists mainly of primary and secondary forest, and it also includes patches of savanna, inundated forest, and coastal scrub. The density of herbaceous plants of Marantaceae and Zingiberaceae, which serve as important foods for great apes at other study sites, is extremely low. It was very difficult to distinguish between the nests of chimpanzees and gorillas because most gorilla nests were made in trees. We developed a new method to identify the builder of nests via a combination of field observation of nests and fecal samples, and examination of hair samples under a scanning electron microscope. Nests of chimpanzees were mainly in primary forest, and the estimated density (0.78 individual per km ² ) is higher than the average density in Gabon and comparable to the nest density in the Lopé Reserve, Gabon. Nests of gorillas were mainly in secondary forest, and their estimated density (0.21) is similar to the average next density in Gabon but lower than the gorilla nest density in the Lopé Reserve. The low density of herbaceous foods seemed to influence the density of gorillas but not the density of chimpanzees.     

No evidence for transmission of antibiotic-resistant Escherichia coli strains from humans to wild western lowland gorillas in Lopé National Park, Gabon

The intensification of human activities within the habitats of wild animals is increasing the risk of interspecies disease transmission. This risk is particularly important for great apes, given their close phylogenetic relationship with humans. Areas of high human density or intense research and ecotourism activities expose apes to a high risk of disease spillover from humans. Is this risk lower in areas of low human density? We determined the prevalence of Escherichia coli antibiotic-resistant isolates in a population of the critically endangered western lowland gorilla (Gorilla gorilla gorilla) and other wild mammals in Lopé National Park (LNP), Gabon, and we tested whether the observed pattern could be explained by bacterial transmission from humans and domestic animals into wildlife populations. Our results show a high prevalence of antibiotic-resistant bacterial isolates in humans and low levels in gorillas and other wildlife. The significant differences in the genetic background of the resistant bacteria isolated from humans and gorillas suggest that transmission is low or does not occur between these two species. These findings indicate that the presence of antibiotic-resistant strains in wildlife do not imply direct bacteria transmission from humans. Thus, in areas of low human density, human-wildlife E. coli transmission seems to be low. The presence of antibiotic-resistant isolates in gorillas may be better explained by other mechanisms for resistance acquisition, such as horizontal gene exchange among bacteria or naturally acquired resistance.     

Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda

Numerous intestinal parasites identified in populations of wild nonhuman primates can be pathogenic to humans. Furthermore, nonhuman primates are susceptible to a variety of human pathogens. Because of increasing human encroachment into previously nonimpacted forests, and the potential for disease transmission between human and nonhuman primate populations, further detailed investigations of primate ecological parasitology are warranted. For meaningful comparisons to be made, it is important for methods to be standardized across study sites. One aspect of methodological standardization is providing reliable estimates of parasite prevalence and knowing how many samples are needed to adequately estimate an individual's parasite prevalence. In this study the parasitic fauna of 37 adult, adolescent, and juvenile male chimpanzees from the Ngogo group, Kibale National Park, Uganda, were assessed from 121 fecal samples collected over a 3-month period. Twelve taxa of intestinal species (five helminth and seven protozoan) were recovered from the samples. The four most prevalent species were Troglodytella abrassarti (97.3%), Oesophagostomum sp. (81.1%), Strongyloides sp. (83.8%), and Entamoeba chattoni (70.3%). No one species was found in all samples from any one animal, and Troglodytella abrassarti, the most common intestinal organism, was found in all of the serial samples of only 69.4% of the chimpanzees. The cumulative species richness for individuals significantly increased for every sequential sample (up to three to four samples) taken per animal during this study. The results indicate that to accurately diagnose total intestinal infection and evaluate group prevalence, three to four sequential samples from each individual must be collected on nonconsecutive days. This conclusion applies only to short study periods in which possible seasonal effects are not taken into consideration. Validation of these results at different study sites in different regions with different climatic patterns is needed.     

Sexual behavior and hormonal estrus cycles in captive aged lowland gorillas (Gorilla gorilla)

To evaluate whether observed cycles in proceptive behavior in aging lowland gorilla females (age 40+) at Brookfield Zoo were driven by ovarian activity, we compared monthly behavioral data to estradiol and progestogen cycles based on fecal hormone assessments. Progestogen peaks showed regularity and close coincidence with monthly sexual behaviors. Estradiol was more variable. Progestogen peaks varied between 22+/-5 days for the control female (29 years old), to 24+/-2.5 and 29+/-8 for the two aged subjects. In the first aged female, which was housed with other females and a silverback, the high degree of cyclicity in sexual behavior, regularity of progestogen cycles, and close concordance between hormonal cycling and sexual behavior strongly compared to patterns found (in this and other studies) in gorilla females <35 years old. Cyclical progestogen peaks were longer and more variable in the second aged female-perhaps because she lacked the social mediation of other females or a male. For husbandry reasons she is not housed with the gorilla group, behavioral data were not collected from her. The value of our longitudinal study is in obtaining reproductive profiles of primate females that are approaching maximum lifespan. This pilot study is part of a larger research project on reproductive senescence that will include other captive females >35 years old, a population that is rapidly increasing in North American zoos as gorillas continue to age.