Western Lowland Research Articles

Discordance between skeletal and dental age at time of death in a western lowland gorilla (Gorilla gorilla gorilla)

A young adult male western lowland gorilla died of accidental causes at the St. Louis Zoo in 2010. Necropsy results indicate he was in good health with no injuries or illnesses. His skeleton was macerated and examination revealed developmental anomalies. Although his chronological age was ~9 years, partial fusion of the capitulum and trochlea to his left humerus and the olecranon process to his right ulna were the only instances of postcranial epiphyseal union, indicating a gorilla of Stage I. However, with mandibular M3 in full occlusion, maxillary M3 near occlusion, and canines still erupting, his dental age is Stage IV. We compare his skeletal dimensions to those published and find he is of average size. His behavior and appearance were similar to that of his conspecifics. Possible causes of delayed skeletal maturation include disorders increasing growth hormone, decreasing testosterone, or altering connective tissue composition. Although dental and skeletal maturation are usually correlated, they are able to proceed in a discordant fashion. This case‐study highlights: (1) the fact that the dentition and skeleton are under separate but related physiological and genetic controls and (2) the importance of relying on multiple lines of evidence when aging unknown individuals. We acknowledge the provision of skeletal material and life history records by Ingrid Porton and the veterinary staff of the St. Louis Zoo.

Survey of Ghodaghodi Lake Complex for Cotton Pygmy Goose Nettapus coromandelianus and Marsh Mugger Crocodylus palustris

Ghodaghodi lake complex is a Ramsar Site and also an important bird area. It forms an important wildlife corridor between terai and Siwaliks and between the two protected areas of the western lowland Nepal, Bardia National Park and Sukla Phanta Wildlife Reserve. A variety of wildlife has been recorded in the area including 140 species of birds, 34 species of mammals, 9 species of herpetofauna, 29 species of fish and several varieties of plant species. Past data shows that the site had 1% south Asian population of Cotton Pygmy Goose Nettapus coromandelianus and presence of Marsh Mugger Crocodylus palustris. Current survey targeted to these two indicator species has shown that Cotton Pygmy Goose has declined by 70% and Marsh Muggers with no clear trend of decline or increase. Hunting and disturbance, encroachment, habitat alteration are identified as major threats to the area. Recommendations are made for habitat management, education and awareness, scientific and participatory monitoring of lake biodiversity with birds and crocodiles as the indicator species, strengthening and capacity building of local CBOs, formation of district level coordination body and to provide a special category status for the GLA.

Dispatches

Dispatches

Extraversion predicts longer survival in gorillas: an 18-year longitudinal study.

Personality plays an important role in determining human health and risk of earlier death. However, the mechanisms underlying those associations remain unknown. We moved away from testing hypotheses rooted in the activities of modern humans, by testing whether these associations are ancestral and one side of a trade-off between fitness costs and benefits. We examined personality predictors of survival in 283 captive western lowland gorillas (Gorilla gorilla gorilla) followed for 18 years. We found that of four gorilla personality dimensions--dominance, extraversion, neuroticism and agreeableness--extraversion was associated with longer survival. This effect could not be explained by demographic information or husbandry practices. These findings suggest that understanding how extraversion and other personality domains influence longevity requires investigating the evolutionary bases of this association in nonhuman primates and other species.

Endowment effects in gorillas (Gorilla gorilla).

Reports of endowment effects in nonhuman primates have received considerable attention in the comparative literature in recent years. However, little is known about the mechanisms underlying these effects. Continuing to explore endowment effects across different species of primate may reveal subtle differences in behavior that can help formulate specific hypotheses about the relevant mechanisms and the social and ecological factors that have shaped them. In this study, we use a paradigm that has previously been used to test chimpanzees (Pan troglodytes) and orangutans (Pongo spp.) to explore whether western lowland gorillas (Gorilla gorilla) exhibit comparable endowment effects. We find that gorillas exhibit endowment effects when in possession of food, but not nonfood, items, and that they show a statistically stronger effect than chimpanzees but not orangutans. These findings are consistent with the hypothesis that mechanisms for endowment effects in primates may be related to inhibitory control or risk aversion.

The Neighbor Effect in Bachelor and Breeding Groups of Western Lowland Gorillas (Gorilla gorilla gorilla)

Behavioral monitoring is an essential tool for understanding how animal management decisions, including exhibit design choices, impact animal behavior and welfare. The purpose of this study was to use behavioral monitoring techniques to determine the interaction between 2 groups (bachelor and breeding groups) of western lowland gorillas that are housed in separate habitats that partially face one another. We performed simultaneous, 30-minute group observations on the breeding and bachelor groups and recorded all occurrences of agonistic and affiliative behavior, vocalizations, and visual monitoring of the adjacent group. At 5-minute intervals, we also recorded which gorillas in the observed group were potentially visible to the neighboring group. Our results indicated that there was considerable variation in the percentage of time each gorilla spent monitoring the neighboring group. We were also able to demonstrate that the visibility of individuals in the breeding group of gorillas was related to behavior of the gorillas in the bachelor group. Although non-contact aggression increased with the visual presence of the adult male of the breeding group, more severe aggression that could cause injury was not influenced by his presence. Results also showed an association between visual presence of a particular female in the breeding group and a decrease in contact aggression in the bachelor group. Since many zoological exhibits allow visual access to other animals, it is important to determine the impact that neighbors may have on each other. Our study investigating interactions between neighboring gorilla groups is an example of how behavioral monitoring can be used to assess the impact of a wide range of management decisions on animal behavior and welfare.

The effect of body orientation on judgments of human visual attention in western lowland gorillas (Gorilla gorilla gorilla).

The ability to appreciate the attentional states of others is an important element used in discerning the presence of Theory of Mind in an individual. Whether primates are able to recognize attention, and further, use such information to predict behavior, remains contentious. In this study, six western lowland gorillas (Gorilla gorilla gorilla) were tested under different conditions that aimed to investigate not only their understanding of what a human experimenter sees, but also what information they use to make these judgments. In all experiments the gorillas selected between two human experimenters, one who could see them and one who could not. In Experiment 1 the gorillas' performance was significantly above chance in conditions where they judged body orientation, head orientation, and eyes. Experiment 2 showed that the gorillas' initial judgments of attention may be based on body orientation rather than facial cues. Experiment 3 demonstrated that the gorillas were better able to utilize facial cues in some conditions, when these cues were paired with a more neutral body orientation. These findings suggest that the gorillas are using a hierarchical approach to determining visual attention, by making an immediate decision based on the most salient cue-body orientation. However, when body orientation is more ambiguous their ability to judge the less prominent cues of the face and eyes does improve.

Genetic diversity of North American captive‐born gorillas (Gorilla gorilla gorilla)

Western lowland gorillas (Gorilla gorilla gorilla) are designated as critically endangered and wild populations are dramatically declining as a result of habitat destruction, fragmentation, diseases (e.g., Ebola) and the illegal bushmeat trade. As wild populations continue to decline, the genetic management of the North American captive western lowland gorilla population will be an important component of the long-term conservation of the species. We genotyped 26 individuals from the North American captive gorilla collection at 11 autosomal microsatellite loci in order to compare levels of genetic diversity to wild populations, investigate genetic signatures of a population bottleneck and identify the genetic structure of the captive-born population. Captive gorillas had significantly higher levels of allelic diversity (t7 = 4.49, P = 0.002) and heterozygosity (t7 = 4.15, P = 0.004) than comparative wild populations, yet the population has lost significant allelic diversity while in captivity when compared to founders (t7 = 2.44, P = 0.04). Analyses suggested no genetic evidence for a population bottleneck of the captive population. Genetic structure results supported the management of North American captive gorillas as a single population. Our results highlight the utility of genetic management approaches for endangered nonhuman primate species.

COMPARISON OF LARYNGEAL MASK AIRWAY USE WITH ENDOTRACHEAL INTUBATION DURING ANESTHESIA OF WESTERN LOWLAND GORILLAS (GORILLA GORILLA GORILLA)

The laryngeal mask airway is an alternative to endotracheal intubation that achieves control of the airway by creating a seal around the larynx with an inflatable cuff. This study compared use of the laryngeal mask airway with endotracheal intubation in anesthetized western lowland gorillas (Gorilla gorilla gorilla). Eight adult gorillas were immobilized for routine and diagnostic purposes for a total of nine anesthetic events. During each anesthetic event, gorillas were either intubated (n = 4; group A) or fitted with a laryngeal mask airway (n= 5; group B). Time required to place each airway device, physiologic parameters, and arterial blood gas were measured and compared between the two groups. There were no significant differences between the two groups for time required to place airway device, heart rate, hemoglobin oxygen saturation, end-tidal carbon dioxide, arterial partial pressure of carbon dioxide, or arterial pH between the two groups. Mean arterial partial pressure of oxygen was significantly greater in group B, 15 (group A: 94 +/- 44 mm Hg; group B: 408 +/- 36 mm Hg; P= 0.0025) and 45 (group A: 104 +/- 21 mm Hg; group B: 407 +/- 77 mm Hg; P = 0.0026) min after airway device placement. Mean respiratory rate was significantly greater in group A at multiple time points. Mean arterial pressure (group A: 129 +/- 16 mm Hg; group B: 60 +/- 8 mm Hg) and diastolic blood pressure (group A: 115 +/- 21 mm Hg; group B: 36 +/- 10 mm Hg) were significantly greater in group A at the time of airway device placement. The laryngeal mask airway maintained oxygenation and ventilation effectively in all gorillas and is a useful alternative to endotracheal intubation in western lowland gorillas.

Non-invasive monitoring of physiological stress in the Western lowland gorilla (Gorilla gorilla gorilla): Validation of a fecal glucocorticoid assay and methods for practical application in the field

Enzymeimmunoassays (EIAs) allow researchers to monitor stress hormone output via measurement of fecal glucocorticoid metabolites (FGCMs) in many vertebrates. They can be powerful tools which allow the acquisition of otherwise unobtainable physiological information from both captive animals and wild animals in remote forest habitats, such as great apes. However, methods for hormone measurement, extraction and preservation need to be adapted and validated for field settings. In preparation for a field study of Western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic we used samples from captive gorillas collected around opportunistic stressful situations to test whether four different glucocorticoid EIAs reflected adrenocortical activity reliably and to establish the lag-time from the stressor to peak excretion. We also validated a field extraction technique and established a simple, non-freezer-reliant method to preserve FGCMs in extracts long-term. We determined the rate of FGCM change over 28days when samples cannot be extracted immediately and over 12h when feces cannot be preserved immediately in alcohol. Finally, we used repeat samples from identified individuals to test for diurnal variation in FGCM output. Two group-specific assays measuring major cortisol metabolites detected the predicted FGCM response to the stressor reliably, whereas more specific cortisol and corticosterone assays were distinctly less responsive and thus less useful. We detected a lag time of 2–3days from stressor to peak FGCM excretion. Our field extraction method performed as well as an established laboratory extraction method and FGCMs in dried extracts stored at ambient temperatures were as stable as those at −20°C over 1yr. Hormones in non-extracted feces in alcohol were stable up to 28days at ambient temperatures. FGCMs in un-fixed gorilla feces deteriorated to almost 50% of the original values within 6h under field conditions. We detected no diurnal variation in FGCMs in samples from wild gorillas. Our study highlights the importance of thorough biological and immunological validation of FGCM assays, and presents validated, practical methods for the application of non-invasive adrenocortical monitoring techniques to field conservation contexts where it is crucially needed.

Reye's or Reye's‐like syndrome in western lowland gorilla (Gorilla gorilla gorilla)

A 15-year-old western lowland gorilla (Gorilla gorilla gorilla) died shortly after transfer to the North Carolina Zoo. Complete blood count, serum biochemical analysis, and necropsy were performed. Combination of compatible clinical signs, biochemical and histopathological findings fulfilled all of the CDC definition criteria of Reye's or a Reye's like syndrome. This report describes a case of Reye's syndrome or Reye's-like syndrome in a non-human primate.

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.

Noninvasive Follow-Up of Simian Immunodeficiency Virus Infection in Wild-Living Nonhabituated Western Lowland Gorillas in Cameroon

Simian immunodeficiency viruses infecting western lowland gorillas (SIVgor) are closely related to HIV-1 and are most likely the ancestors of HIV-1 groups O and P. At present, limited data are available on genetic diversity, transmission, viral evolution, and pathogenicity of SIVgor in its natural host. Between 2004 and 2011, 961 putative gorilla fecal samples were collected at the Campo Ma'an National Park, Cameroon. Among them, 16% cross-reacted with HIV-1 antibodies, corresponding to at least 34 infected gorillas. Combining host genotyping and field data, we identified four social groups composed of 7 to 15 individuals each, with SIV rates ranging from 13% to 29%. Eleven SIVgor-infected gorillas were sampled multiple times; two most likely seroconverted during the study period, showing that SIVgor continues to spread. Phylogenetic analysis of partial env and pol sequences revealed cocirculation of closely related and divergent strains among gorillas from the same social group, indicating SIVgor transmissions within and between groups. Parental links could be inferred for some gorillas infected with closely related strains, suggesting vertical transmission, but horizontal transmission by sexual or aggressive behavior was also suspected. Intrahost molecular evolution in one gorilla over a 5-year period showed viral adaptations characteristic of escape mutants, i.e., V1V2 loop elongation and an increased number of glycosylation sites. Here we show for the first time the feasibility of noninvasive monitoring of nonhabituated gorillas to study SIVgor infection over time at both the individual and population levels. This approach can also be applied more generally to study other pathogens in wildlife.

Suspected macular degeneration in a captive western lowland gorilla (gorilla gorilla gorilla)

The case of a 31-year-old captive female Western lowland gorilla (Gorilla gorilla gorilla) with decreased near vision but good distance vision is presented. Examination of the fundus revealed drusen-like bodies in the macula presumably because of an age-related macular degeneration (AMD).

Brief communication: Hand preference for bimanual and unimanual feeding in captive gorillas: Extension in a second colony of apes

Right-hand dominance is widely considered to be a uniquely human trait. Whether nonhuman primates exhibit similar population-level hand preferences remains a topic of considerable debate. Despite extensive research focusing on laterality in nonhuman primates, our interpretation of these studies is limited due to methodological issues including the lack of a common measure of hand preference and the use of tasks that may not be reliable indicators of handedness. The use of consistent methods between studies is necessary to enable comparisons within and between species and allow for more general conclusions to be drawn from these results. The present study replicates methods used in recent research reporting population-level right-handedness in captive gorillas (Meguerditchian et al.,2010). Observational data were collected on hand preference for unimanual and bimanual feeding in 14 captive western lowland gorillas (Gorilla gorilla gorilla). Individual-level preferences were found, primarily for bimanual feeding; however, the data reveal no group-level directional bias (contra Meguerditchian et al.). Like the study by Meguerditchian et al. (2010), though, bimanual feeding revealed significantly stronger hand preferences than unimanual reaching, and age, sex, group membership, or rearing history had no effect on hand preference. Finally, variations in diet and corresponding grip type between studies suggest that hand preferences may vary across bimanual tasks depending on grip morphology. This study aims to contribute to our existing knowledge of primate laterality by increasing the number of individuals investigated using methods that allow for comparisons with similar research.

Recovery Potential of a Western Lowland Gorilla Population following a Major Ebola Outbreak: Results from a Ten Year Study

Investigating the recovery capacity of wildlife populations following demographic crashes is of great interest to ecologists and conservationists. Opportunities to study these aspects are rare due to the difficulty of monitoring populations both before and after a demographic crash. Ebola outbreaks in central Africa have killed up to 95% of the individuals in affected western lowland gorilla (Gorilla gorilla gorilla) populations. Assessing whether and how fast affected populations recover is essential for the conservation of this critically endangered taxon. The gorilla population visiting Lokoué forest clearing, Odzala-Kokoua National Park, Republic of the Congo, has been monitored before, two years after and six years after Ebola affected it in 2004. This allowed us to describe Ebola's short-term and long-term impacts on the structure of the population. The size of the population, which included around 380 gorillas before the Ebola outbreak, dropped to less than 40 individuals after the outbreak. It then remained stable for six years after the outbreak. However, the demographic structure of this small population has significantly changed. Although several solitary males have disappeared, the immigration of adult females, the formation of new breeding groups, and several birth events suggest that the population is showing potential to recover. During the outbreak, surviving adult and subadult females joined old solitary silverbacks. Those females were subsequently observed joining young silverbacks, forming new breeding groups where they later gave birth. Interestingly, some females were observed joining silverbacks that were unlikely to have sired their infant, but no infanticide was observed. The consequences of the Ebola outbreak on the population structure were different two years and six years after the outbreak. Therefore, our results could be used as demographic indicators to detect and date outbreaks that have happened in other, non-monitored gorilla populations.

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.

Gorilla gorilla gorilla

The gorilla genome reveals that genetic similarities among humans and the apes are more complex than expected, and allows a fresh assessment of the evolutionary mechanisms that led to the primate species seen today. See Article p.169 The genome of the gorilla has been sequenced, making it possible to compare the DNA of the four surviving hominid genera: human, chimpanzee, gorilla and orang-utan. The data — mainly from a female western lowland gorilla named Kamilah, but also from other gorillas representing both the western lowland and eastern lowland sub-species — imply that in almost one-third of its genome, the gorilla is closer to the human or chimpanzee than the human and chimp are to each other. Around 500 genes show accelerated evolution in gorilla, human and chimpanzee lineages, and there is evidence for parallel acceleration, particularly in genes associated with hearing. On the basis of genetic and fossil evidence, the authors suggest that the human–chimpanzee and human–chimpanzee–gorilla speciation events occurred at around 6 million and 10 million years ago respectively, whereas the two gorilla species diverged around 1.75 million years ago.

Extending across continents: Travel medicine and Latin America

Wildlife tourism is proliferating worldwide and has the potential to raise revenue for conservation as well as public awareness of conservation issues. However, concerns are growing about the potentially negative influence of such tourism on the wildlife involved. We investigate the effects of habituation, ecotourism and research activities on levels of faecal glucocorticoid metabolites (FGCMs), a proxy for physiological stress, in wild western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic. We compare FGCMs in three human-contacted groups with those in unhabituated gorillas. We also explore how human–gorilla contact influences FGCMs of a gorilla group undergoing habituation and investigate how measures of general human–gorilla contact, tourism and human proximity influence FGCMs in recently and long-term habituated groups. Two of the three human-contacted groups had higher levels of FGCMs than unhabituated gorillas. The group undergoing habituation had the highest FGCMs, which increased up to 21 days following contacts, suggesting a cumulative FGCM response, in line with descriptions of a hormonal adaptation response to a chronic intermittent stressor. FGCMs in habituated groups were significantly associated with increasing frequency of violation of the 7 m distance rule by observers and with a medical intervention but not with other measures of human pressure. Our findings provide critical information for the management of this, and other, species whose conservation depends on habituation for ecotourism.

Severe Idiopathic Hypocalcemia in a Juvenile Western Lowland Gorilla,Gorilla gorilla gorilla

A 6-mo-old, male western lowland gorilla (Gorilla gorilla gorilla) was evaluated because of tetany of both hands. The gorilla had alternating periods of constipation, diarrhea, and bloating since birth. A diagnosis of idiopathic hypocalcemia was based on severe hypocalcemia, a normal vitamin D level, response to oral calcium and vitamin D therapy, and eventual resolution. Idiopathic hypocalcemia, an uncommon disease in neonatal humans, should be considered in young gorillas with persistent gastrointestinal problems or acute tetany.