Brain organization of gorillas reflects species differences in ecology

Gorillas include separate eastern (Gorilla beringei) and western (Gorilla gorilla) African species that diverged from each other approximately 2 million years ago. Although anatomical, genetic, behavioral, and socioecological differences have been noted among gorilla populations, little is known about variation in their brain structure. This study examines neuroanatomical variation between gorilla species using structural neuroimaging. Postmortem magnetic resonance images were obtained of brains from 18 captive western lowland gorillas (Gorilla gorilla gorilla), 15 wild mountain gorillas (Gorilla beringei beringei), and 3 Grauer's gorillas (Gorilla beringei graueri) (both wild and captive). Stereologic methods were used to measure volumes of brain structures, including left and right frontal lobe gray and white matter, temporal lobe gray and white matter, parietal and occipital lobes gray and white matter, insular gray matter, hippocampus, striatum, thalamus, each hemisphere and the vermis of the cerebellum, and the external and extreme capsules together with the claustrum. Among the species differences, the volumes of the hippocampus and cerebellum were significantly larger in G. gorilla than G. beringei. These anatomical differences may relate to divergent ecological adaptations of the two species. Specifically, G. gorilla engages in more arboreal locomotion and thus may rely more on cerebellar circuits. In addition, they tend to eat more fruit and have larger home ranges and consequently might depend more on spatial mapping functions of the hippocampus. Am J Phys Anthropol 156:252–262, 2015. © 2014 Wiley Periodicals, Inc.     

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.     

Species and sex identification of western lowland gorillas (Gorilla gorilla gorilla), eastern lowland gorillas (Gorilla beringei graueri) and humans

Methods for the identification of the sex and species of individuals from samples non-invasively taken from humans and gorillas were established. Amplification of a segment of amelogenin (AMG), which is an X–Y homologous gene, using two pairs of primers from human AMG, revealed both X- and Y-specific bands. The possibility of sex identification was examined by typing the AMG gene using hair and fecal samples from captive western lowland gorillas (Gorilla gorilla gorilla) in Japan and hair samples from wild eastern lowland gorillas (Gorilla beringei graueri) in the Kahuzi-Biega National Park, Democratic Republic of Congo, which were sexed by direct observation. Species-specific bands of AMG in gorillas and humans were identified by restriction fragment length polymorphisms analysis. These tests could be used for sexing unidentified individuals of wild western and eastern lowland gorillas, and screening contamination of human DNA from non-invasively acquired samples.     

Hand preferences in captive gorillas,orang-utans and gibbons

Hand preference was assessed in 12 gorillas (Gorilla gorilla gorilla), 13 orang-utans (Pongo pygmaeus abelii), and 9 gibbons (Hylobates lar) by using a floor retrieval task and a mesh retrieval task. Hand preference was also assessed in 8 gorillas and 8 orang-utans by using a task involving the unfastening of a hasp. A bipedal requirement during testing (mesh retrieval task) facilitated detection of hand preferences. A significant left-hand preference was found for the gibbons with 6 of 6 gibbons preferring their left hand on the mesh retrieval task. Similarly, a significant right-hand preference was found for the gorillas with 10 of 12 gorillas preferring their right hand on the mesh retrieval task. The data for the orang-utan suggest a bimodal distribution on all tasks. Since the gibbon and gorilla in the wild engage in bipedal locomotion more frequently than the orangutan, one possible interpretation for these results correlates the degree of bipedal behavior of a species in its natural environment with its readiness to exhibit a unilateral population-level hand preference.     

Are gorillas right-handed or not?

Comparative data on laterality of function in primates are useful for elucidating its evolution, including its link to asymmetry of cerebral structure. Recently the gorilla (Gorilla gorilla, Pongidae) has been nominated as the other hominoid species closest toHomo sapiens in terms of handedness. This study aims to scrutinise the 22 accounts of gorillas' hand preferences. Numerous shortcomings exist in the published literature on the topic, so that a firm conclusion is not yet possible. It is not yet clear whether gorillas are right-preferent, left-preferent, or ambi-preferent, and additional data are needed.     

Hand-clapping as a communicative gesture by wild female swamp gorillas

Hand-clapping is a form of gestural communication commonly observed in captive great apes yet only isolated instances of this behaviour have been documented in the wild. Nearly 20 years ago Fay recorded the first observations of hand-clapping in western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic. Here we present observations of Likouala swamp gorillas using hand-clapping as a form of gestural communication in previously undocumented contexts in the wild. We observed hand-clapping on four different occasions in four different groups. The hand-clap was always exhibited by an adult female and always consisted of two consecutive claps conducted in front of the body. We suggest the functional significance of the behaviour was to maintain and enforce group cohesiveness during instances of alarm. These observations suggest western lowland gorillas have a means of communicating that is thus far absent in their eastern counterparts (Gorilla beringei ssp.). This could be a gestural culture found only in western lowland gorillas which should be investigated further to shed light on the evolution of communication among hominoids.     

‘Separating the wheat from the chaff’: A novel food processing technique in captive gorillas (Gorilla g. gorilla)

Observation of a novel food processing technique is reported for captive zoo gorillas (Gorilla g. gorilla). It is similar in function to that of Japanese macaques' wheat placer mining behaviour and consists of puffing/blowing air with the mouth onto a mixture of oat grains and chaff in order to separate out the oat grains. Three females in two of four groups regularly use this behaviour. Other individuals in these groups or individuals of the two other groups in the same zoo do not use it. However, a very similar behaviour has been observed in three other individuals in a gorilla group of another zoo. The existence of this technique in spatially separated groups implies that multiple individuals have invented it for themselves. The possible role of social transmission is still to be investigated.     

The subspecies concept in primatology: The case of mountain gorillas

The criteria for the application of subspecific units in living primate populations have received little attention relative to other vertebrate taxa, even though they have important implications for conservation strategies for many nonhuman primate populations. One of the most critically endangered primates is the mountain gorilla,Gorilla gorilla beringei, of which 600 animals exist in east-central Africa. FollowingSarmiento et al. (1996), taxonomists have proposed splitting these populations into two subspecies as part of a revised taxonomy of the genusGorilla. In this paper I review the application of the subspecies concept in primatology, using the gorillas of Bwindi Impenetrable National Park and the Virungas as case studies. An examination of genetic, morphological, biogeographic, ecological, and behavioral evidence indicates that reclassifying Bwindi gorillas as taxonomically distinct from those in the Virungas is not well supported and needs further study. Because taxonomy provides the basis of conservation management policies, a cautious and conservative approach to the subspecies question is warranted in the case of endangered primate populations.     

Dental and phylogeographic patterns of variation in gorillas

Gorilla patterns of variation have great relevance for studies of human evolution. In this study, molar morphometrics were used to evaluate patterns of geographic variation in gorillas. Dental specimens of 323 adult individuals, drawn from the current distribution of gorillas in equatorial Africa were divided into 14 populations. Discriminant analyses and Mahalanobis distances were used to study population structure.Results reveal that: 1) the West and East African gorillas form distinct clusters, 2) the Cross River gorillas are well separated from the rest of the western populations, 3) gorillas from the Virunga mountains and the Bwindi Forest can be differentiated from the lowland gorillas of Utu and Mwenga-Fizi, 4) the Tshiaberimu gorillas are distinct from other eastern gorillas, and the Kahuzi-Biega gorillas are affiliated with them. These findings provide support for a species distinction between Gorilla gorilla and Gorilla beringei, with subspecies G. g. diehli, G. g. gorilla, G. b. graueri, G. b. beringei, and possibly, G. b. rex-pygmaeorum. Clear correspondence between dental and other patterns of taxonomic diversity demonstrates that dental data reveal underlying genetic patterns of differentiation.Dental distances increased predictably with altitude but not with geographic distances, indicating that altitudinal segregation explains gorilla patterns of population divergence better than isolation-by-distance. The phylogeographic pattern of gorilla dental metric variation supports the idea that Plio-Pleistocene climatic fluctuations and local mountain building activity in Africa affected gorilla phylogeography. I propose that West Africa comprised the historic center of gorilla distribution and experienced drift-gene flow equilibrium, whereas Nigeria and East Africa were at the periphery, where climatic instability and altitudinal variation promoted drift and genetic differentiation. This understanding of gorilla population structure has implications for gorilla conservation, and for understanding the distribution of sympatric chimpanzees and Plio-Pleistocene hominins.     

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.     

The cryptic genetic structure of the North American captive gorilla population

Western lowland gorillas (Gorilla gorilla gorilla) were imported from across their geographical range to North American zoos from the late 1800s through 1974. The majority of these gorillas were imported with little or no information regarding their original provenance and no information on their genetic relatedness. Here, we analyze 32 microsatellite loci in 144 individuals using a Bayesian clustering method to delineate clusters of individuals among a sample of founders of the captive North American zoo gorilla collection. We infer that the majority of North American zoo founders sampled are distributed into two distinct clusters, and that some individuals are of admixed ancestry. This new information regarding the existence of ancestral genetic population structure in the North American zoo population lays the groundwork for enhanced efforts to conserve the evolutionary units of the western lowland gorilla gene pool. Our data also show that the genetic diversity estimates in the founder population were comparable to those in wild gorilla populations (Mondika and Cross River), and that pairwise relatedness among the founders is no different from that expected for a random mating population. However, the relatively high level of relatedness (R = 0.54) we discovered in a pair of known breeding pairs reveals the need for incorporating genetic relatedness estimates in the captive management of western lowland gorillas.     

Genetic identification of elusive animals: re-evaluating tracking and nesting data for wild western gorillas

Western gorillas Gorilla gorilla have been exceedingly difficult to habituate to the presence of human observers. Nevertheless, researchers have amassed a wealth of information on population densities and group structure for this ape species by locating and counting the sleeping nests of wild individuals. Such nest-count studies have suggested that western gorilla groups often have multiple silverbacks and these multimale groups occasionally divide into smaller subgroups. However, observational data from forest clearing sites and from a few recently habituated western gorilla groups show no evidence of multimale family groups or of subgrouping. This discrepancy underscores a long-standing question in ape research: How accurately do nesting sites reflect true group compositions? We evaluated these indirect measures of group composition by using DNA from faeces and hair to genetically identify individual gorillas at nesting sites. Samples were collected from unhabituated wild western gorillas ranging near Mondika Research Center in the Central African Republic and Republic of Congo. DNA extracted from these samples was genotyped at up to 10 microsatellite loci and one X–Y homologous locus for sex identification. Individuals were then identified at nesting sites by their unique multilocus genotypes, thus providing a 'molecular census' of individual gorillas. Results confirm that western gorillas often build more than one nest at a nesting site and, thus, nest counts can be highly inaccurate indicators of group size and composition. Indeed, we found that nest counts can overestimate group size by as much as 40%, indicating that true gorilla population numbers are probably lower than those reported from census surveys. This study demonstrates how genetic analysis can be a valuable tool for studying and conserving elusive, endangered animals.     

Preference for structural environmental features in captive lowland gorillas (Gorilla gorilla gorilla)

Increased interest in the behavioral effects of captive environments and advances in zoo design have resulted in a proliferation of “naturalistic” animal habitats. Although scientists have demonstrated that such exhibits have some positive effects on behavior, very little is known about the complex relationships between these specialized environments and behavior. This study sought to determine preferences for structural environmental features, such as slope and trees, exhibited by captive lowland gorillas (Gorilla gorilla gorilla). An average of 496 location scans were collected on each of 23 gorillas, housed in 6 groups. The results indicate that enclosure usage was significantly associated with the features of slope, nearness to holding facility, and presence of environmental components additional to substrate (e.g., tree or rock). In particular, areas with flat ground that were near the holding building and that included at least one component additional to substrate were preferred by all animals. © 1993 Wiley-Liss, Inc.     

An experimental study of nettle feeding in captive gorillas

Mountain gorillas (Gorilla beringei beringei) in Karisoke, Rwanda, feed on the stinging nettle Laportea alatipes by means of elaborate processing skills. Byrne [e.g. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 358:529–536, 2003] has claimed that individuals acquire these skills by means of the so‐called program‐level imitation, in which the overall sequence of problem‐solving steps (not the precise actions) is reproduced. In this study we present western lowland gorillas (Gorilla gorilla gorilla) with highly similar nettles. Twelve gorillas in three different groups (including also one nettle‐naïve gorilla) used the same program‐level technique as wild mountain gorillas (with differences mainly on the action level). Chimpanzees, orangutans, and bonobos did not show these program‐level patterns, nor did the gorillas when presented with a plant similar in structural design but lacking stinging defenses. We conclude that although certain aspects (i.e. single actions) of this complex skill may be owing to social learning, at the program level gorilla nettle feeding derives mostly from genetic predispositions and individual learning of plant affordances. Am. J. Primatol. 70:584–593, 2008. © 2008 Wiley‐Liss, Inc.     

Behavioral Ecology of Sympatric Chimpanzees and Gorillas in Bwindi Impenetrable National Park,Uganda: Diet

Via a field study of chimpanzees (Pan troglodytes schweinfurthii) and gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, we found that their diets are seasonally similar, but diverge during lean seasons. Bwindi chimpanzees fed heavily on fruits of Ficus sp., which were largely ignored by the gorillas. Bwindi gorilla diet was overall more folivorous than chimpanzee diet, but was markedly more frugivorous than that of gorillas in the nearby Virunga Volcanoes. During 4 mo of the year Bwindi gorilla diet included more food species than that of the chimpanzees. Three factors in particular—seasonal consumption of fibrous foods by gorillas, interspecific differences in preferred fruit species, and meat consumption by chimpanzees—contributed to dietary divergence between the two species. When feeding on fruits, gorillas ate Myrianthus holstii more frequently than chimpanzees did, while chimpanzees included more figs in their annual diet. Chimpanzee diet included meat of duikers and monkeys; gorilla frequently consumed decaying wood.     

No evidence for female kin association,indications for extragroup paternity,and sex‐biased dispersal patterns in wild western gorillas

Characterizing animal dispersal patterns and the rational behind individuals’ transfer choices is a long‐standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one‐male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher‐than‐expected within‐group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long‐term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R _ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.     

The role of taste in food selection by African apes: implications for niche separation and overlap in tropical forests

Ripe fruit eating shapes the behavior of most of the apes. Gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes) are very different sizes and, consequently, have been traditionally viewed as ecologically distinct, but few studies have explored the behavioral and physiological foundations of their diets. Debate continues on the extent that large-bodied gorillas may be less selective and more opportunistic fruit eaters than chimpanzees. Taste responses have been predicted to relate to body size and digestive strategies. This study employs laboratory research on taste perception and discrimination among captive zoo-housed chimpanzees and relates it to previous work on gorillas to better characterize diets and niche separation among these apes. During the captive trials, differences were recorded in consumption patterns of water and varying concentrations of dilute aqueous fructose (sweet) and tannic acid solutions (astringent), compounds commonly found in wild foods. The chimpanzees exhibited similar preference thresholds for fructose (50 mM) to other primates studied. They exhibited slightly lower inhibition thresholds for tannic acid solutions than gorillas, but higher than smaller primates studied to date. These preliminary findings suggest that tannin tolerance may well be mediated by body size, though possible species differences in salivary proteins or other sensory differences remain to be explored. This research furthers our efforts to understand the roles of body size and physiological adaptations in shaping diet and niche separation of chimpanzees and gorillas.     

Microsatellite DNA loci identify individuals and provide no evidence for multiple paternity in wild tuatara (Sphenodon: Reptilia)

Six new microsatellite DNA loci are isolated from a genomic library of the sphenodontid reptile tuatara (Sphenodon) and presented here as a tool for identifying individuals for future paternity and kinship studies. These loci, in combination with four previously published loci, are sufficient to discriminate between clutch-mate siblings from Stephens Island and Brothers Island populations. These populations represent high and low levels of genetic diversity in tuatara populations respectively. An estimate of minimum number of fathers of each clutch found no evidence for multiple paternity in any clutch. These newly isolated loci complete the development of an array of genetic tools for use in tuatara to enhance ongoing conservation and management of wild, translocated and captive populations.     

Newly Discovered Gorilla Population in the Ebo Forest,Littoral Province,Cameroon

We report on a new population of gorillas discovered in November 2002 in the Ebo Forest, Littoral Province, Cameroon. We observed A group of q7 gorillas directly for 83 min, and they were in auditory range for 155 min. Further evidence of gorilla presence included 8 nest groups totaling 38 nests, distinctive feeding signs accompanied by footprints, and a gorilla cranium collected from the nearby village of Iboti. This newly discovered gorilla population is geographically intermediate between the 2 extant populations of western gorillas: Gorilla gorilla gorilla, the most populous gorilla subspecies living in Gabon, Equatorial Guinea, Congo-Brazzaville, Central African Republic and Cameroon to the south of the Sanaga River, and G. g. diehli or the Cross River gorilla, a small population of ca. 250 individuals on the Cameroon-Nigeria border. It is not possible to assign the new gorilla population to either subspecies on the basis of measurements of the single male cranium. Genetic analyses of freshly shed hairs, collected from gorilla nests, may help to resolve the taxonomic status of the Ebo gorillas.     

Simian homologues of human herpesviruses and implications for novel viral introduction to free-living mountain gorillas

The endangered mountain gorilla (Gorilla beringei beringei) in Rwanda, Uganda, and the Democratic Republic of Congo is frequently in contact with humans through tourism, research activities, and illegal entry of people into protected gorilla habitat. Herpesviruses, which are ubiquitous in primates, have the potential to be shared in any setting where humans and gorillas share habitat. Based on serological findings and clinical observations of orofacial ulcerated lesions resembling herpetic lesions, an alpha-herpesvirus resembling human herpes simplex virus type 1 (HSV-1) has long been suspected to be present in human-habituated mountain gorillas in the wild. While the etiology of orofacial lesions in the wild has not been confirmed, HSV-1 has been suspected in captively-housed mountain gorillas and confirmed in a co-housed confiscated Grauer's gorilla (Gorilla beringei graueri). To better characterize herpesviruses infecting mountain gorillas and to determine the presence/absence of HSV-1 in the free-living population, we conducted a population-wide survey to test for the presence of orally shed herpesviruses. DNA was extracted from discarded chewed plants collected from 294 individuals from 26 groups, and samples were screened by polymerase chain reaction using pan-herpesvirus and HSV-1-specific assays. We found no evidence that human herpesviruses had infected free-ranging mountain gorillas. However, we found gorilla-specific homologs to human herpesviruses, including cytomegaloviruses (GbbCMV-1 and 2), a lymphocryptovirus (GbbLCV-1), and a new rhadinovirus (GbbRHV-1) with similar characteristics (i.e., timing of primary infection, shedding in multiple age groups, and potential modes of transmission) to their human counterparts, human cytomegalovirus, Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus, respectively.