Examining the dual hormone hypothesis in wild male mountain gorillas (Gorilla beringei beringei).

The Challenge Hypothesis is an influential framework for understanding how androgens are involved in the promotion of competitive behavior during mating-related challenges and has been tested extensively in studies across scientific disciplines. Mixed support in psychological research led scholars to develop the Dual Hormone Hypothesis as a potential path forward, which argues that glucocorticoids moderate the relationship between androgens and status-striving. In the current study, we examine the Challenge Hypothesis and the Dual Hormone Hypothesis in wild male mountain gorillas, representing the first time the latter hypothesis has been tested in a non-human primate. In a sample of 30 adult males comprising over 600 days of observation, we find some limited support for the Challenge Hypothesis. Greater daily rates of targeted aggression toward other adult males corresponded to higher fecal androgen metabolites 1-2 days following observations, though this pattern did not fully generalize to dominance rank or other competitive behaviors examined. However, we find no support for the Dual Hormone Hypothesis: neither dominance rank nor any category of competitive behavior was predicted by the interaction between androgens and glucocorticoids. We close by discussing how this initial investigation might be leveraged toward the development of an expanded Dual Hormone Hypothesis that draws on the large evidence base in primate behavioral ecology.

Primate and wildlife law outreach campaigns in the Republic of Congo: Assessing knowledge gain of school children in urban centers compared to rural villages.

Primate populations are declining throughout tropical Africa. Great apes are threatened from extinction despite the existence of wildlife laws that fully protect them in their range states. But, due to a lack of knowledge and understanding of these laws, they remain largely ineffective. There is, therefore, a crucial need to improve awareness of wildlife laws in Congo. We conducted an education campaign and tested the effectiveness of two communication tools (wildlife law flyer and gorilla/pet-trade comic book) in increasing school children's knowledge in rural and urban settings using evaluation questionnaires. We found extremely low precampaign knowledge of wildlife laws but detected a moderate increase of knowledge attributed to our communication tools. We discuss the usefulness of different communication tools and their relevance for knowledge increase with different audiences. Our study provides insights into the design of education campaigns, most notably the use of flyers and booklets, which can help to increase knowledge. Evaluations can help to improve the design of education campaigns, particularly message wording and identification of appropriate communication tools with the goal of improving compliance with wildlife laws.

An exploration of Menzerath's law in wild mountain gorilla vocal sequences.

Menzerath's law, traditionally framed as a negative relationship between the size of a structure and its constituent parts (e.g. sentences with more clauses have shorter clauses), is widespread across information-coding systems ranging from human language and the vocal and gestural sequences of primates and birds, to the building blocks of DNA, genes and proteins. Here, we analysed an extensive dataset of 'close-call' sequences produced by wild mountain gorillas (Gorilla beringei beringei, no. individuals = 10, no. sequences = 2189) to determine whether, in accordance with Menzerath's law, a negative relationship existed between the number of vocal units in a sequence and the duration of its constituent units. We initially found positive evidence for this but, on closer inspection, the negative relationship was driven entirely by the difference between single- and multi-unit (two to six unit) sequences. Once single-unit sequences were excluded from the analysis, we identified a relationship in the opposite direction, with longer sequences generally composed of longer units. The close-call sequences of mountain gorillas therefore represent an intriguing example of a non-human vocal system that only partially conforms to the predictions of Menzerath's law.

Using long-term ranging patterns to assess within-group and between-group competition in wild mountain gorillas.

BACKGROUND: Competition within and between social groups determines access to resources and can be inferred from space use parameters that reflect depletion of food resources and competitive abilities of groups. Using location data from 1998 to 2017, we investigated within- and between-group competition in 12 groups of wild mountain gorillas (Gorilla beringei beringei). As within-group feeding competition is expected to increase with group size, an increase in group size is predicted to lead to an increase in the size of annual home ranges and core areas, but to a decrease in fidelity (reuse of an area). Due to asymmetries in competitive abilities, larger groups are expected to have higher exclusivity (degree of non-shared space) of annual home ranges and core areas than smaller groups. RESULTS: We found evidence of within-group feeding competition based on a positive relationship between group size and both annual home range and core area size as well as a negative relationship between group size and core area fidelity. Additionally, fidelity of core areas was lower than of home ranges. Between-group competition was inferred from a trend for groups with more members and more males to have more exclusive home ranges and core areas. Lastly, annual core areas were largely mutually exclusive. CONCLUSIONS: Our study suggests that non-territorial, group-living animals can have highly dynamic, long-term avoidance-based spacing patterns, both temporally and spatially, to maintain annual core area exclusivity among groups while concurrently shifting these areas annually within overlapping home ranges to avoid resource depletion. Despite ranging in larger home ranges and core areas, larger groups were able to maintain more exclusive ranges than smaller groups, suggesting a competitive advantage for larger groups in between-group competition in a non-territorial species. Together, these findings contribute to understanding how social animals make behavioral adjustments to mitigate the effects of intraspecific competition.

Plasmodium ovale wallikeri in Western Lowland Gorillas and Humans, Central African Republic.

Human malaria parasites have rarely been reported from free-ranging great apes. Our study confirms the presence of the human malaria parasite Plasmodium ovale wallikeri in western lowland gorillas and humans in Dzanga Sangha Protected Areas, Central African Republic, and discusses implications for malaria epidemiology.

Spatial representation of magnitude in humans (Homo sapiens), Western lowland gorillas (Gorilla gorilla gorilla), and American black bears (Ursus americanus).

The spatial-numerical association of response codes (SNARC) effect is the tendency for humans to respond faster to relatively larger numbers on the left or right (or with the left or right hand) and faster to relatively smaller numbers on the other side. This effect seems to occur due to a spatial representation of magnitude either in occurrence with a number line (wherein participants respond to relatively larger numbers faster on the right), other representations such as clock faces (responses are reversed from number lines), or culturally specific reading directions, begging the question as to whether the effect may be limited to humans. Given that a SNARC effect has emerged via a quantity judgement task in Western lowland gorillas and orangutans (Gazes et al., Cog 168:312-319, 2017), we examined patterns of response on a quantity discrimination task in American black bears, Western lowland gorillas, and humans for evidence of a SNARC effect. We found limited evidence for SNARC effect in American black bears and Western lowland gorillas. Furthermore, humans were inconsistent in direction and strength of effects, emphasizing the importance of standardizing methodology and analyses when comparing SNARC effects between species. These data reveal the importance of collecting data with humans in analogous procedures when testing nonhumans for effects assumed to bepresent in humans.

Detection of novel RNA viruses from free-living gorillas, Republic of the Congo: genetic diversity of picobirnaviruses.

Most of the emerging infectious diseases reported so far originated in wildlife. Therefore, virological surveillance of animals and particularly great apes is of great interest to establish the repertory of viruses associated with healthy hosts. This will further help to identify the emergence of new viruses and predict the possibility of interspecies transmission. In this study, we performed shotgun viral metagenomics on stool samples collected from seventeen free-living wild gorillas from the Republic of the Congo. The analysis revealed the presence of novel RNA viruses (picobirnaviruses, partitivirus, and Picornavirales (posa-like and dicistrovirus-like viruses)). Among these, picobirnavirus-related sequences were abundantly covered in the stools. Based on genetic variations both in capsid and RdRp proteins of picobirnaviruses, at least 96 variants were identified and most of them were novel. Among the 96, 22 variants had a nearly complete genome or segment. A comprehensive sequence analysis identified a potential new genogroup/genetic cluster and the presence of a short linear amino acid motif (ExxRxNxxxE) in a hypothetical protein. The sequence analysis of posa-like virus and dicistrovirus showed that these two viruses were novel members in the respective viral families. In conclusion, the identification of novel RNA viruses and their genetic diversity increases our knowledge about viruses that are associated with stools of wild gorillas and contributes to the initiatives in the search for potential emerging zoonotic viruses.

Male-female interactions in multimale groups of mountain gorillas.

Male-female social interactions may vary according to female receptivity, female parity, and male dominance rank. Such variation may be less apparent in species with one-male mating systems than those with multimale mating systems, as within-group male-male competition and female mate choice are absent. Examining variation in male-female interactions in multimale groups in species with a predominantly one-male mating system may help to shed light on plasticity in behavioral patterns and the evolution of mating systems. In this study, we investigated the effect of female receptivity (i.e., days when mating occurred), female parity, and male dominance rank on the patterns of spatial proximity, grooming, following, and aggression among 34 male-female dyads in four multi-male groups of Virunga mountain gorillas. In addition, as a preliminary investigation of potential physiological costs incurred by females in a mating context (coercion), we tested whether female receptivity and female parity explained variation in immunoreactive glucocorticoid (iGC) levels of females. The amount of time male-female dyads spent in close proximity was significantly higher for parous versus nulliparous females and for high- versus low-ranking males. The rate of male aggression to females did not vary significantly with female parity, male rank, or female receptivity. However, post hoc analysis showed that both proximity and aggression increased for the males that participated in the matings on days that females were receptive. Grooming and following by males occurred infrequently. Neither female receptivity nor parity influenced iGC levels in females, a finding that is more consistent with courtship than coercion of females by males. Overall, our results suggest that males advertise their ability to provide protection to females and their offspring, and females seek out males that can do so.

Inference of gorilla demographic and selective history from whole-genome sequence data.

Although population-level genomic sequence data have been gathered extensively for humans, similar data from our closest living relatives are just beginning to emerge. Examination of genomic variation within great apes offers many opportunities to increase our understanding of the forces that have differentially shaped the evolutionary history of hominid taxa. Here, we expand upon the work of the Great Ape Genome Project by analyzing medium to high coverage whole-genome sequences from 14 western lowland gorillas (Gorilla gorilla gorilla), 2 eastern lowland gorillas (G. beringei graueri), and a single Cross River individual (G. gorilla diehli). We infer that the ancestors of western and eastern lowland gorillas diverged from a common ancestor approximately 261 ka, and that the ancestors of the Cross River population diverged from the western lowland gorilla lineage approximately 68 ka. Using a diffusion approximation approach to model the genome-wide site frequency spectrum, we infer a history of western lowland gorillas that includes an ancestral population expansion of 1.4-fold around 970 ka and a recent 5.6-fold contraction in population size 23 ka. The latter may correspond to a major reduction in African equatorial forests around the Last Glacial Maximum. We also analyze patterns of variation among western lowland gorillas to identify several genomic regions with strong signatures of recent selective sweeps. We find that processes related to taste, pancreatic and saliva secretion, sodium ion transmembrane transport, and cardiac muscle function are overrepresented in genomic regions predicted to have experienced recent positive selection.

Molecular epidemiological study of adenovirus infecting western lowland gorillas and humans in and around Moukalaba-Doudou National Park (Gabon).

Adenoviruses are widespread in human population as well as in great apes, although the data about the naturally occurring adenovirus infections remain rare. We conducted the surveillance of adenovirus infection in wild western lowland gorillas in Moukalaba-Doudou National Park (Gabon), in order to investigate naturally occurring adenovirus in target gorillas and tested specifically a possible zoonotic transmission with local people inhabiting the vicinity of the park. Fecal samples were collected from western lowland gorillas and humans, and analyzed by PCR. We detected adenoviral genes in samples from both gorillas and the local people living around the national park, respectively: the overall prevalence rates of adenovirus were 24.1 and 35.0 % in gorillas and humans, respectively. Sequencing revealed that the adenoviruses detected in the gorillas were members of Human mastadenovirus B (HAdV-B), HAdV-C, or HAdV-E, and those in the humans belonged to HAdV-C or HAdV-D. Although HAdV-C members were detected in both gorillas and humans, phylogenetic analysis revealed that the virus detected in gorillas are genetically distinct from those detected in humans. The HAdV-C constitutes a single host lineage which is compatible with the host-pathogen divergence. However, HAdV-B and HAdV-E are constituted by multiple host lineages. Moreover, there is no evidence of zoonotic transmission thus far. Since the gorilla-to-human transmission of adenovirus has been shown before, the current monitoring should be continued in a broader scale for getting more insights in the natural history of naturally occurring adenoviruses and for the safe management of gorillas' populations.

An investigation of the auditory perception of western lowland gorillas in an enrichment study.

Previous research has highlighted the varied effects of auditory enrichment on different captive animals. This study investigated how manipulating musical components can influence the behavior of a group of captive western lowland gorillas (Gorilla gorilla gorilla) at Bristol Zoo. The gorillas were observed during exposure to classical music, rock-and-roll music, and rainforest sounds. The two music conditions were modified to create five further conditions: unmanipulated, decreased pitch, increased pitch, decreased tempo, and increased tempo. We compared the prevalence of activity, anxiety, and social behaviors between the standard conditions. We also compared the prevalence of each of these behaviors across the manipulated conditions of each type of music independently and collectively. Control observations with no sound exposure were regularly scheduled between the observations of the 12 auditory conditions. The results suggest that naturalistic rainforest sounds had no influence on the anxiety of captive gorillas, contrary to past research. The tempo of music appears to be significantly associated with activity levels among this group, and social behavior may be affected by pitch. Low tempo music also may be effective at reducing anxiety behavior in captive gorillas. Regulated auditory enrichment may provide effective means of calming gorillas, or for facilitating active behavior. Zoo Biol. 35:398-408, 2016. © 2016 Wiley Periodicals, Inc.

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology.

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro-ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the host's external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga-Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context.

Profiling unauthorized natural resource users for better targeting of conservation interventions.

Unauthorized use of natural resources is a key threat to many protected areas. Approaches to reducing this threat include law enforcement and integrated conservation and development (ICD) projects, but for such ICDs to be targeted effectively, it is important to understand who is illegally using which natural resources and why. The nature of unauthorized behavior makes it difficult to ascertain this information through direct questioning. Bwindi Impenetrable National Park, Uganda, has many ICD projects, including authorizing some local people to use certain nontimber forest resources from the park. However, despite over 25 years of ICD, unauthorized resource use continues. We used household surveys, indirect questioning (unmatched count technique), and focus group discussions to generate profiles of authorized and unauthorized resource users and to explore motivations for unauthorized activity. Overall, unauthorized resource use was most common among people from poor households who lived closest to the park boundary and farthest from roads and trading centers. Other motivations for unauthorized resource use included crop raiding by wild animals, inequity of revenue sharing, and lack of employment, factors that created resentment among the poorest communities. In some communities, benefits obtained from ICD were reported to be the greatest deterrents against unauthorized activity, although law enforcement ranked highest overall. Despite the sensitive nature of exploring unauthorized resource use, management-relevant insights into the profiles and motivations of unauthorized resource users can be gained from a combination of survey techniques, as adopted here. To reduce unauthorized activity at Bwindi, we suggest ICD benefit the poorest people living in remote areas and near the park boundary by providing affordable alternative sources of forest products and addressing crop raiding. To prevent resentment from driving further unauthorized activity, ICDs should be managed transparently and equitably.

Admixture between historically isolated mitochondrial lineages in captive Western gorillas: recommendations for future management.

Although captive populations of western gorilla have been maintained in the United States for over a century, little is known about the geographic origins and genetic composition of the current zoo population. Furthermore, although previous mitochondrial analyses have shown that free-range gorilla populations exhibit substantial regional differentiation, nothing is known of the extent to which this variation has been preserved in captive populations. To address these questions, we combined 379 pedigree records with data from 52 mitochondrial sequences to infer individual haplogroup affiliations, geographical origin of wild founders and instances of inter-breeding between haplogroups in the United States captive gorilla population. We show that the current captive population contains all major mitochondrial lineages found within wild western lowland gorillas. Levels of haplotype diversity are also comparable to those found in wild populations. However, the majority of captive gorilla matings have occurred between individuals with different haplogroup affiliations. Although restricting crosses to individuals within the same haplogroup would preserve the phylogeographic structure present in the wild, careful management of captive populations is required to minimize the risk of drift and inbreeding. However, when captive animals are released back into the wild, we recommend that efforts should be made to preserve natural phylogeographic structure.

Gorillas with white sclera: A naturally occurring variation in a morphological trait linked to social cognitive functions.

Human eye morphology is considered unique among the primates in that humans possess larger width/height ratios (WHR), expose a greater amount of visible sclera (SSI; width of exposed eyeball/width of visible iris), and critically, have a white sclera due to a lack of pigmentation. White sclera in humans amplifies gaze direction, whereas the all-dark eyes of apes are hypothesized to conceal gaze from others. This study examines WHR and SSI in humans (N = 13) and gorillas (N = 85) engaged in direct and averted gazes and introduces a qualitative assessment of sclera color to evaluate variations in sclera pigmentation. The results confirm previous findings that humans possess a larger WHR than gorillas but indicate that humans and gorillas display similar amounts of visible sclera. Additionally, 72% (N = 124) of gorilla eyes in this sample deviated from the assumed all-dark eye condition. This questions whether gaze camouflage is the primary function of darkened sclera in non-human primates or whether other functional roles can be ascribed to the sclera, light or dark. We argue that white sclera evolved to amplify direct gazes in humans, which would have played a significant role in the development of ostensive communication, which is communication that both shows something and shows the intention to show something. We conclude that the horizontal elongation of the human eye, rather than sclera color, more reliably distinguishes human from great ape eyes, represented here by gorillas.

Modeling variation in early life mortality in the western lowland gorilla: Genetic, maternal and other effects.

Uncovering sources of variation in gorilla infant mortality informs conservation and life history research efforts. The international studbook for the western lowland gorilla provides information on a sample of captive gorillas large enough for which to analyze genetic, maternal, and various other effects on early life mortality in this critically endangered species. We assess the importance of variables such as sex, maternal parity, paternal age, and hand rearing with regard to infant survival. We also quantify the proportions of variation in mortality influenced by heritable variation and maternal effects from these pedigree and survival data using variance component estimation. Markov chain Monte Carlo simulations of generalized linear mixed models produce variance component distributions in an animal model framework that employs all pedigree information. Two models, one with a maternal identity component and one with both additive genetic and maternal identity components, estimate variance components for different age classes during the first 2 years of life. This is informative of the extent to which mortality risk factors change over time during gorilla infancy. Our results indicate that gorilla mortality is moderately heritable with the strongest genetic influence just after birth. Maternal effects are most important during the first 6 months of life. Interestingly, hand-reared infants have lower mortality for the first 6 months of life. Aside from hand rearing, we found other predictors commonly used in studies of primate infant mortality to have little influence in these gorilla data.

Western lowland gorilla (Gorilla gorilla gorilla) birth patterns and human presence in zoological settings.

There is some evidence to suggest that zoo visitors may have a disruptive impact on zoo-housed animals, especially primates. While some consider western lowland gorillas (Gorilla gorilla gorilla) to be particularly reactive to large crowds, the evidence of these effects is mixed, and is likely highly influenced by exhibit design, and group composition. While the majority of studies have focused on behavioral responses to human presence, there is the potential for physiological effects as well, including the possibility of affecting the timing of parturition. Such effects have been demonstrated in laboratory-housed callitrichids and chimpanzees, but unlike laboratory settings where human presence is lowest during the weekends, human presence might peak during weekends in public zoo settings. However, in a study of zoo-housed chimpanzees, there were no significant differences between the number of chimpanzee births that occurred on weekdays compared to weekends [Wagner and Ross, 2008], and we sought to test these questions with gorillas. We analyzed the timing of 336 live gorilla births and 48 stillbirths at 53 accredited North American zoos from 1985-2014, and similarly to chimpanzees, found no weekend or weekday effect on number of births (live births: G = 0.000, p = 1; stillbirths: G = 0.166, p < 0.684). These data add to our understanding of the potential influence of human presence on primate behavior and physiology, and add to evidence suggesting that the effects of zoo visitors on exhibited species may be less profound than previously assumed.

The effects of auditory enrichment on gorillas.

Several studies have demonstrated that auditory enrichment can reduce stereotypic behaviors in captive animals. The purpose of this study was to determine the relative effectiveness of three different types of auditory enrichment-naturalistic sounds, classical music, and rock music-in reducing stereotypic behavior displayed by Western lowland gorillas (Gorilla gorilla gorilla). Three gorillas (one adult male, two adult females) were observed at the Buffalo Zoo for a total of 24 hr per music trial. A control observation period, during which no sounds were presented, was also included. Each music trial consisted of a total of three weeks with a 1-week control period in between each music type. The results reveal a decrease in stereotypic behaviors from the control period to naturalistic sounds. The naturalistic sounds also affected patterns of several other behaviors including locomotion. In contrast, stereotypy increased in the presence of classical and rock music. These results suggest that auditory enrichment, which is not commonly used in zoos in a systematic way, can be easily utilized by keepers to help decrease stereotypic behavior, but the nature of the stimulus, as well as the differential responses of individual animals, need to be considered.

The birth of an infant decreases group spacing in a zoo-housed lowland gorilla group (Gorilla gorilla gorilla).

Changes in group composition can alter the behavior of social animals such as gorillas. Although gorilla births are presumed to affect group spacing patterns, there is relatively little data about how these events affect gorilla group cohesion. We investigated how members of a western lowland gorilla group (n = 6) at Lincoln Park Zoo (Chicago, IL, USA) spaced themselves prior to and after the birth of an infant, to investigate changes in group cohesion. Gorillas were housed in an indoor-outdoor enclosure in which access to the outdoors was permitted when temperatures exceeded 5°C. We recorded spatial locations of each group member using 30-min group scans on tablet computers with an electronic map interface, as well as noting their access to outdoor areas. Data from the 4 months following the birth was compared to a control period corresponding to early pregnancy. We measured distances between all possible group dyads for each scan and subsequently calculated a mean distance between all group members. An ANOVA revealed that access to the outdoors had no effect on group spacing (F(1,56) = 0.066, P = 0.799). However, the presence of an infant resulted in a significant reduction in inter-individual distance (F(1,56) = 23.988, P = 0.000), decreasing inter-individual spacing by 12.5%. This information helps characterize the behavioral impact of a new birth on captive gorilla social structure and could potentially inform future management of breeding gorilla groups.

Twelve-year proximity relationships in a captive group of western lowland gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park, California, USA.

Proximity data were collected in a captive breeding group of gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park (currently called the San Diego Zoo Safari Park) twice a year (spring and fall periods) for over 12 years, by using a convenient method in which individuals less than 5 m from each animal in the group were recorded by scan sampling, approximately once per hour. Immature females from infancy to young adulthood maintained relatively frequent proximity to both their mothers and the silverback male and spent little time alone (no animals within 10 m), with relatively large individual differences. On the other hand, immature males decreased the time spent near their mothers and the silverback male and increased the time spent alone with increasing age. Therefore, sex differences in proximity to mothers and the silverback male became apparent after late juvenility. Some adult females maintained increased frequency of proximity to the silverback male than that by other females over the 12-year period, indicating the presence of long-term, stable proximity relationships between the silverback male and the adult females. Such long-term, stable proximity relationships were also observed among adult females. Some association patterns reported in wild gorillas, such as frequent proximity between adult females with dependent offspring and the silverback male and close relationships between related females, were not observed in the present study. The idiosyncratic or individual factors influencing some association patterns were easily reflected in captive situations.