The Role of Behavioral Research in the Conservation of Chimpanzees and Gorillas

Chimpanzees and gorillas are among man's closest living relatives, sharing most of the human genetic code and having many similarities to humans in anatomy, physiology, and behavior. Like humans, these apes make and use tools and have strong family bonds. Chimpanzees even show population-specific behaviors similar to those of human cultures. However, chimpanzee and gorilla populations are in dramatic decline due to bushmeat hunting, habitat loss, and the varied risks of small, isolated populations. The first step in conserving the world's ape populations in the wild is to recognize and understand the complexities of these threats. Mitigating the risks takes a deeper understanding of ape behavior. This article provides examples of how gorilla and chimpanzee behavioral studies intersect with, and are critical to, conservation efforts.     

Comparative studies on an antigenicity of plasma proteins from humans and apes by ELISA: a close relationship of chimpanzee and human

1. Antigenic differences between human and ape plasma proteins were quantitatively investigated by enzyme-linked immunosorbent assay (ELISA) using antisera against human and chimpanzee plasmas. 2. With anti-human plasma serum, both the chimpanzee and gorilla were very close to the human, although the chimpanzee was slightly closer to the human than to the gorilla; relative immunological distance (relative ID) of the chimpanzee was 71, while that of the gorilla was 74. 3. With anti-chimpanzee plasma serum, the chimpanzee was found to be closely related to the human; relative ID of the chimpanzee was 58, while that of the gorilla was 75. 4. From these a molecular phylogeny for humans and apes was deduced; among living apes, the chimpanzee is the most closely related species to the human.     

Evolution of subterminal satellite (StSat) repeats in hominids

Subterminal satellite (StSat) repeats, consisting of 32-bp-long AT-rich units (GATATTTCCATGTT(T/C)ATACAGATAGCGGTGTA), were first found in chimpanzee and gorilla (African great apes) as one of the major components of heterochromatic regions located proximal to telomeres of chromosomes. StSat repeats have not been found in orangutan (Asian great ape) or human. This patchy distribution among species suggested that the StSat repeats were present in the common ancestor of African great apes and subsequently lost in the lineage leading to human. An alternative explanation is that the StSat repeats in chimpanzee and gorilla have different origins and the repeats did not occur in human. The purpose of the present study was quantitative evaluation of the above alternative possibilities by analyzing the nucleotide variation contained in the repeats. We collected large numbers of sequences of repeat units from genome sequence databases of chimpanzee and gorilla, and also bonobo (an African great ape phylogenetically closer to chimpanzee). We then compared the base composition of the repeat units among the 3 species, and found statistically significant similarities in the base composition. These results support the view that the StSat repeats had already formed multiple arrays in the common ancestor of African great apes. It is thus suggested that humans lost StSat repeats which had once grown to multiple arrays.     

Variation in behavioral traits of two frugivorous mammals may lead to differential responses to human disturbance

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

Evolution of the Hominoid Semenogelin Genes,the Major Proteins of Ejaculated Semen

The hominoid primates (apes and humans) exhibit remarkable diversity in their social and sexual behavioral systems. This is reflected in many ways in their anatomy and physiology. For example, the testes and seminal vesicles are relatively large in species with high sperm competition like the chimpanzee and small in species with low or no sperm competition like the gorilla. Additionally, the chimpanzee is the only hominoid primate known to produce a firm copulatory plug, which presumably functions in sperm competition by blocking insemination of subsequent males. Here we examine the molecular evolution of the semenogelin genes (SEMG1 and SEMG2), which code for the predominant structural proteins in human semen. High molecular weight complexes of these proteins are responsible for the viscous gelatinous consistency of human semen; their rodent homologs are responsible for the formation of a firm copulatory plug. Chimpanzees have an expanded SEMG1 gene caused by duplications of tandem repeats, each encoding 60 amino acids, resulting in a protein nearly twice as long as that of humans. In contrast, at both SEMG1 and SEMG2 we observed several gorilla haplotypes that contain at least one premature stop codon. We suggest that these structural changes in the semenogelin proteins that have arisen since the human–chimpanzee–gorilla split may be responsible for the physiological differences between these species ejaculated semen that correlate with their sociosexual behavior. Present address: (Jensen-Seaman) Human and Molecular Genetics Center, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226, USA     

Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo

With the exception of humans, chimpanzees show the most diverse and complex tool-using repertoires of all extant species. Specific tool repertoires differ between wild chimpanzee populations, but no apparent genetic or environmental factors have emerged as definitive forces shaping variation between populations. However, identification of such patterns has likely been hindered by a lack of information from chimpanzee taxa residing in central Africa. We report our observations of the technological system of chimpanzees in the Goualougo Triangle, located in the Republic of Congo, which is the first study to compile a complete tool repertoire from the Lower Guinean subspecies of chimpanzee (Pan troglodytes troglodytes). Between 1999 and 2006, we documented the tool use of chimpanzees by direct observations, remote video monitoring, and collections of tool assemblages. We observed 22 different types of tool behavior, almost half of which were habitual (shown repeatedly by several individuals) or customary (shown by most members of at least one age-sex class). Several behaviors considered universals among chimpanzees were confirmed in this population, but we also report the first observations of known individuals using tools to perforate termite nests, puncture termite nests, pound for honey, and use leafy twigs for rain cover. Tool behavior in this chimpanzee population ranged from simple tasks to hierarchical sequences. We report three different tool sets and a high degree of tool-material selectivity for particular tasks, which are otherwise rare in wild chimpanzees. Chimpanzees in the Goualougo Triangle are shown to have one of the largest and most complex tool repertoires reported in wild chimpanzee populations. We highlight new insights from this chimpanzee population to our understanding of ape technological systems and evolutionary models of tool-using behavior.     

The Role of the Antiviral APOBEC3 Gene Family in Protecting Chimpanzees against Lentiviruses from Monkeys

Cross-species transmissions of viruses from animals to humans are at the origin of major human pathogenic viruses. While the role of ecological and epidemiological factors in the emergence of new pathogens is well documented, the importance of host factors is often unknown. Chimpanzees are the closest relatives of humans and the animal reservoir at the origin of the human AIDS pandemic. However, despite being regularly exposed to monkey lentiviruses through hunting, chimpanzees are naturally infected by only a single simian immunodeficiency virus, SIVcpz. Here, we asked why chimpanzees appear to be protected against the successful emergence of other SIVs. In particular, we investigated the role of the chimpanzee APOBEC3 genes in providing a barrier to infection by most monkey lentiviruses. We found that most SIV Vifs, including Vif from SIVwrc infecting western-red colobus, the chimpanzee’s main monkey prey in West Africa, could not antagonize chimpanzee APOBEC3G. Moreover, chimpanzee APOBEC3D, as well as APOBEC3F and APOBEC3H, provided additional protection against SIV Vif antagonism. Consequently, lentiviral replication in primary chimpanzee CD4⁺ T cells was dependent on the presence of a lentiviral vif gene that could antagonize chimpanzee APOBEC3s. Finally, by identifying and functionally characterizing several APOBEC3 gene polymorphisms in both common chimpanzees and bonobos, we found that these ape populations encode APOBEC3 proteins that are uniformly resistant to antagonism by monkey lentiviruses.     

A comprehensive atlas of white matter tracts in the chimpanzee

Chimpanzees (Pan troglodytes) are, along with bonobos, humans’ closest living relatives. The advent of diffusion MRI tractography in recent years has allowed a resurgence of comparative neuroanatomical studies in humans and other primate species. Here we offer, in comparative perspective, the first chimpanzee white matter atlas, constructed from in vivo chimpanzee diffusion-weighted scans. Comparative white matter atlases provide a useful tool for identifying neuroanatomical differences and similarities between humans and other primate species. Until now, comprehensive fascicular atlases have been created for humans (Homo sapiens), rhesus macaques (Macaca mulatta), and several other nonhuman primate species, but never in a nonhuman ape. Information on chimpanzee neuroanatomy is essential for understanding the anatomical specializations of white matter organization that are unique to the human lineage.

Diffusion MRI tractography reveals the first complete atlas of white matter of the chimpanzee, with the potential to help understand differences between the organization of human and chimpanzee brains.     

Detection and genetic characterization of enteroviruses circulating among wild populations of chimpanzees in Cameroon: relationship with human and simian enteroviruses

Enteroviruses (EVs), members of the family Picornaviridae, are a genetically and antigenically diverse range of viruses causing acute infections in humans and several Old World monkey (OWM) species. Despite their known wide distribution in primates, nothing is currently known about the occurrence, frequency, and genetic diversity of enteroviruses infecting apes. To investigate this, 27 chimpanzee and 27 gorilla fecal samples collected from undisturbed jungle areas with minimal human contact in Cameroon were screened for EVs. Four chimpanzee samples were positive, but none of the gorilla samples were positive. Genetic characterization of the VP1, VP4, and partial VP2 genes, the 5' untranslated region, and partial 3Dpol sequences enabled chimpanzee-derived EVs to be identified as (i) the species A type, EV76, (ii) a new species D type assigned as EV111, along with a human isolate from the Democratic Republic of Congo previously described by the International Committee on the Taxonomy of Viruses, and (iii) a new species B type (assigned as EV110) most closely related to, although a distinct type from, the SA5 isolate recovered from a vervet monkey. The identification of EVs infecting chimpanzees related to those circulating in human and OWM populations provides evidence for cross-species transmission of EVs between primates. However, the direction of transfer and the existence of primate sources of zoonotic enterovirus infections in humans require further investigation of population exposure and more extensive characterization of EVs circulating in wild ape populations.     

Evolution of X-Degenerate Y Chromosome Genes in Greater Apes: Conservation of Gene Content in Human and Gorilla,But Not Chimpanzee

Compared with the X chromosome, the mammalian Y chromosome is considerably diminished in size and has lost most of its ancestral genes during evolution. Interestingly, for the X-degenerate region on the Y chromosome, human has retained all 16 genes, while chimpanzee has lost 4 of the 16 genes since the divergence of the two species. To uncover the evolutionary forces governing ape Y chromosome degeneration, we determined the complete sequences of the coding exons and splice sites for 16 gorilla Y chromosome genes of the X-degenerate region. We discovered that all studied reading frames and splice sites were intact, and thus, this genomic region experienced no gene loss in the gorilla lineage. Higher nucleotide divergence was observed in the chimpanzee than the human lineage, particularly for genes with disruptive mutations, suggesting a lack of functional constraints for these genes in chimpanzee. Surprisingly, our results indicate that the human and gorilla orthologues of the genes disrupted in chimpanzee evolve under relaxed functional constraints and might not be essential. Taking mating patterns and effective population sizes of ape species into account, we conclude that genetic hitchhiking associated with positive selection due to sperm competition might explain the rapid decline in the Y chromosome gene number in chimpanzee. As we found no evidence of positive selection acting on the X-degenerate genes, such selection likely targets other genes on the chimpanzee Y chromosome. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Human-specific amino acid changes found in 103 protein-coding genes

We humans have many characteristics that are different from those of the great apes. These human-specific characters must have arisen through mutations accumulated in the genome of our direct ancestor after the divergence of the last common ancestor with chimpanzee. Gene trees of human and great apes are necessary for extracting these human-specific genetic changes. We conducted a systematic analysis of 103 protein-coding genes for human, chimpanzee, gorilla, and orangutan. Nucleotide sequences for 18 genes were newly determined for this study, and those for the remaining genes were retrieved from the DDBJ/EMBL/GenBank database. The total number of amino acid changes in the human lineage was 147 for 26,199 codons (0.56%). The total number of amino acid changes in the human genome was, thus, estimated to be about 80,000. We applied the acceleration index test and Fisher's synonymous/nonsynonymous exact test for each gene tree to detect any human-specific enhancement of amino acid changes compared with ape branches. Six and two genes were shown to have significantly higher nonsynonymous changes at the human lineage from the acceleration index and exact tests, respectively. We also compared the distribution of the differences of the nonsynonymous substitutions on the human lineage and those on the great ape lineage. Two genes were more conserved in the ape lineage, whereas one gene was more conserved in the human lineage. These results suggest that a small proportion of protein-coding genes started to evolve differently in the human lineage after it diverged from the ape lineage.     

Quantitative study of chimpanzee and gorilla counterparts of the human D antigen

The reactivities of three human anti-D monoclonal antibodies (mAbs) with human, chimpanzee, and gorilla red blood cells (RBCs) were compared by quantitative radioimmunology and indirect immunofluorescence methods. The number of antigenic sites varies widely in gorillas (from 48,000-283,000), while in chimpanzees this number is very close to that observed in human R₁R₂ RBCs. The affinity of the anti-D antibodies was slightly lower with ape RBCs than with D-positive human RBCs. In chimpanzee, the D-like epitopes recognition is enhanced by papain while the gorilla D-like epitopes are destroyed by enzyme treatment.     

The Influence of Body Mass Index,Age and Sex on Inflammatory Disease Risk in Semi-Captive Chimpanzees

Obesity and ageing are emerging issues in the management of captive primates, including Chimpanzees, Pan troglodytes. Studies on humans show that obesity and old age can independently increase the risk of inflammatory-associated diseases indicated by elevated levels of pro-inflammatory cells and proteins in the blood of older or obese compared to levels in younger or non-obese individuals. In humans, sex can influence the outcomes of these risks. Health management of these problems in chimpanzee populations requires an understanding of similarities and differences of factors influencing inflammatory disease risks in humans and in chimpanzees. We examined the relationship between age, sex and Body Mass Index (BMI) with hematological biomarkers of inflammatory disease risk established for humans which include the neutrophil to lymphocyte ratio (NLR), and neutrophil, white blood cell (WBC), platelet microparticle and platelet counts. We found that higher values of NLR, neutrophil count and platelet microparticle count were associated with higher BMI values and older age indicating increased inflammation risk in these groups; a similar pattern to humans. There was a strong sex by age interaction on inflammation risk, with older males more at risk than older females. In contrast to human studies, total WBC count was not influenced by BMI, but like humans, WBC and platelet counts were lower in older individuals compared to younger individuals. Our findings are similar to those of humans and suggest that further insight on managing chimpanzees can be gained from extensive studies of ageing and obesity in humans. We suggest that managing BMI should be an integral part of health management in captive chimpanzee populations in order to partially reduce the risk of diseases associated with inflammation. These results also highlight parallels in inflammation risk between humans and chimpanzees and have implications for understanding the evolution of inflammation related diseases in apes.     

Rh gene evolution in primates: study of intron sequences

By amplification and sequencing of RH gene intron 4 of various primates we demonstrate that an Alu-Sx-like element has been inserted in the RH gene of the common ancestor of humans, apes, Old World monkeys, and New World monkeys. The study of mouse and lemur intron 4 sequences allowed us to precisely define the insertion point of the Alu-Sx element in intron 4 of the RH gene ancestor common to Anthropoidea. Like humans, chimpanzees and gorillas possess two types of RH intron 4, characterized by the presence (human RHCE and ape RHCE-like genes) or absence (human RHD and ape RHD-like genes) of the Alu-Sx element. This led us to conclude that in the RH common ancestor of humans, chimpanzees, and gorillas, a duplication of the common ancestor gene gave rise to two genes, one differing from the other by a 654-bp deletion encompassing an Alu-Sx element. Moreover, most of chimpanzees and some gorillas posses two types of RHD-like intron 4. The introns 4 of type 1 have a length similar to that of human RHD intron 4, whereas introns 4 of type 2 display an insertion of 12 bp. The latest insertion was not found in the human genome (72 individuals tested). The study of RH intron 3 length polymorphism confirmed that, like humans, chimpanzees and gorillas possess two types of intron 3, with the RHD-type intron 3 being 289 bases shorter than the RHCE intron 3. By amplification and sequencing of regions encompassing introns 3 and 4, we demonstrated that chimpanzee and gorilla RH-like genes displayed associations of introns 3 and 4 distinct to those found in man. Altogether, the results demonstrate that, as in humans, chimpanzee and gorilla RH genes experienced intergenic exchanges.     

The Influence of Transect Use by Local People and Reuse of Transects for Repeated Surveys on Nesting in Western Lowland Gorillas (Gorilla gorilla gorilla) and Central Chimpanzees (Pan troglodytes troglodytes) in Southeast Cameroon

Monitoring populations of endangered species over time is necessary to guide and evaluate conservation efforts. This is particularly important for nonprotected areas that ensure connectivity between protected populations but are prone to uncontrolled hunting pressure. We investigated whether use of transects by local people and transect reuse for repeated surveys influence great ape nesting and bias results. We conducted simultaneous marked nest count surveys over 12 mo on established and newly opened transects in a nonprotected area subject to traditional heavy use by local people and recorded forest composition and signs of human activity. Chimpanzee and gorilla density estimates and encounter rates per kilometer were lower on established transects than on new ones. A generalized linear model indicated that hunting activity, distance to a regularly used forest trail, and transect type (old or new) predicted chimpanzee nest abundance, and distance to the trail and transect type predicted gorilla nest abundance, with no effect of habitat type (percentage suitable habitat) for either species. We, therefore, suggest that the difference in great ape nesting is a result of high levels of hunting by local people on established transects and forest trails. Our results support the use of repeated line transect surveys for monitoring great ape populations in many circumstances, although we advocate taking precautions in nonprotected areas, to avoid the bias imposed by use of established transects for hunting.     

Mapping suitable great ape habitat in and around the Lobéké National Park,South‐East Cameroon

As a result of extensive data collection efforts over the last 20–30 years, there is quite a good understanding of the large‐scale geographic distribution and range limits of African great apes. However, as human activities increasingly fragment great ape spatial distribution, a better understanding of what constitutes suitable great ape habitat is needed to inform conservation and resource extraction management. Chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) inhabit the Lobéké National Park and its surrounding forest management units (FMUs) in South‐East Cameroon. Both park and neighboring forestry concessions require reliable evidence on key factors driving great ape distribution for their management plans, yet this information is largely missing and incomplete. This study aimed at mapping great ape habitat suitability in the area and at identifying the most influential predictors among three predictor categories, including landscape predictors (dense forest, swampy forest, distance to water bodies, and topography), human disturbance predictors (hunting, deforestation, distance to roads, and population density), and bioclimatic predictor (annual precipitation). We found that about 63% of highly to moderately suitable chimpanzee habitat occurred within the Lobéké National Park, while only 8.4% of similar habitat conditions occurred within FMUs. For gorillas, highly and moderately suitable habitats occurred within the Lobéké National Park and its surrounding FMUs (82.6% and 65.5%, respectively). Key determinants of suitable chimpanzee habitat were hunting pressure and dense forest, with species occurrence probability optimal at relatively lower hunting rates and at relatively high‐dense forest areas. Key determinants of suitable gorilla habitat were hunting pressure, dense forests, swampy forests, and slope, with species occurrence probability optimal at relatively high‐dense and swampy forest areas and at areas with mild slopes. Our findings show differential response of the two ape species to forestry activities in the study area, thus aligning with previous studies.     

Conservation of intronic minisatellite polymorphisms in the SCK1/SHC2 gene of Hominidae

The neuronally expressed Shc adaptor homolog SCK1/SHC2 gene contains an unusually high number of minisatellites. In humans, twelve different minisatellite sequences are located in introns of SCK1/SHC2 and ten of them are highly polymorphic. Here we used primers developed for humans to screen ten intronic loci of SCK1/SHC2 in chimpanzee and gorilla, and undertook a comprehensive analysis of the genomic sequence to address the evolutionary events driving these variable repeats. All ten loci amplified in chimpanzee and gorilla contained hypervariable and low-variability minisatellites. The human polymorphic locus TR1 was monomorphic in chimpanzee and gorilla, but we detected polymorphic alleles in these apes for the human monomorphic TR7 locus. When we examined the repeat size among these hominoids, there was no consistent variation by length from humans to great apes. In spite of the inconsistent evolutionary dynamics in repeat length variation, exon 16 was highly conserved between humans and great apes. These results suggest that non-coding intronic minisatellites do not show a consistent evolutionary paradigm but evolved with different patterns among each minisatellite locus. These findings provide important insight for minisatellite conservation during hominoid evolution.     

Molecular epidemiology of hepatitis B virus variants in nonhuman primates

We characterized hepatitis B virus (HBV) isolates from sera of 21 hepatitis B virus surface antigen-positive apes, members of the families Pongidae and Hylobatidae (19 gibbon spp., 1 chimpanzee, and 1 gorilla). Sera originate from German, French, Thai, and Vietnamese primate-keeping institutions. To estimate the phylogenetic relationships, we sequenced two genomic regions, one located within the pre-S1/pre-S2 region and one including parts of the polymerase and the X protein open reading frames. By comparison with published human and ape HBV isolates, the sequences could be classified into six genomic groups. Four of these represented new genomic groups of gibbon HBV variants. The gorilla HBV isolate was distantly related to the chimpanzee isolate described previously. To confirm these findings, the complete HBV genome from representatives of each genomic group was sequenced. The HBV isolates from gibbons living in different regions of Thailand and Vietnam could be classified into four different phylogenetically distinct genomic groups. The same genomic groups were found in animals from European zoos. Therefore, the HBV infections of these apes might have been introduced into European primate-keeping facilities by direct import of already infected animals from different regions in Thailand. Taken together, our data suggest that HBV infections are indigenous in the different apes. One event involving transmission between human and nonhuman primates in the Old World of a common ancestor of human HBV genotypes A to E and the ape HBV variants might have occurred.     

Mother-infant separation and reunion in the great apes

One mother-infant dyad of each species of great ape, orang-utan, chimpanzee and gorilla, with an additional conspecific cagemate, were studied for the effects of maternal separation and reunion. High levels of agitation were observed in all infants immediately upon separation, followed by a longer period of behavioral depression with continuing, intermittent agitation. A compatible cagemate seemed to attenuate, to some degree, the behavioral depression reaction. Initial detachment following reunion with the mother occurred for all the great ape infants studied. Subsequent intensification of mother-infant attachment occurred during reunion for all three species. The findings of intermittent agitation during separation and the initial detachment upon reunion with the mother are not generally reported for monkeys, but are reported for human children. These data suggest that certain responses to maternal separation and reunion occur, to some degree, among all primates that have been studied, whereas other responses seen among apes and humans are not generally reported for monkeys.