Socioecological factors influencing population structure of gorillas and chimpanzees

Differences in distribution and density between gorillas and chimpanzees are reconsidered with special reference to population structure. Both ecological and social factors influencing population structure are compared between species and between habitats within species. Gorillas and chimpanzees respond differently to a decline in food quality, such as fruit scarcity: gorillas change diet and decrease range, while chimpanzees do not change diet but may expand range. These responses result in different effects on their grouping patterns. For gorillas the dispersed distribution and reduction of range size decreases the rate of inter-unit encounters and female transfer. The concentration of social units increases the rate of aggressive contact between units and stimulates female transfer. Social units of gorillas may crowd or disperse in order to attain the optimal density. This tendency may result in similar densities of gorillas across habitats. By contrast, the distribution patterns or range size may not affect inter-unit relationships of chimpanzees. Within a single unit-group, various reproductive strategies are adopted by both sexes. Independent travel of females and flexible grouping patterns enable them to survive at very low density in extraordinary large ranges. Density and inter-unit relationships are good criteria for a healthy population of gorillas, while the size of unit-group and inter-individual relationships are good criteria for chimpanzees. Conservation planners should consider these differences for sympatric and allopatric survival in these species.     

Sex differences in the relative lengths of metacarpals and metatarsals in gorillas and chimpanzees

Sex differences other than the simple dimorphism in size were documented for the metapodials of two primate species. Lengths of metacarpals and metatarsals were obtained from the skeletons of 64 gorillas and 42 chimpanzees. Length ratios were constructed for all possible pairings of the five bones in each individual hand and foot. For both species, several of these length ratios exhibited substantial differences between the sexes. Body size was not the basis for these sex differences; when specimens of similar size were compared, the sex differences remained. In humans, length ratios for the fingers and toes also have previously been demonstrated to exhibit sex differences, and the length ratio for the index and ring fingers (the 2D:4D ratio) has been shown to correlate with various medical conditions. Various facts suggest that length ratios in human digits are associated with androgen exposure, probably during prenatal development. For gorillas, the metacarpal length ratio showing the largest sex difference was 4Mc:5Mc in both hands, and the metatarsal length ratio showing the largest sex difference was 1Mt:2Mt in the left foot. Sex differences in length ratios also existed for chimpanzees, but they were generally smaller than for gorillas. Apparently, both gorillas and chimpanzees are affected by developmental mechanisms, possibly androgenic mechanisms, similar to those in humans. Analyses of previous measurements [Susman, R.L., 1979 Comparative and functional morphology of hominoid fingers. Am. J. Phys. Anthropol. 50, 215-236] revealed that all components of the rays are not affected equally by whatever mechanisms are responsible for the sex differences in length ratios.     

Investigation of the human Rh blood group system in nonhuman primates and other species with serologic and Southern blot analysis

To investigate the evolution of the Rh blood-group system in anthropoid apes, New and Old World monkeys, and nonprimate animals, serologic typing of erythrocytes from these species with antibodies specific for the human Rh blood-group antigens was performed. In addition, genomic DNA from these animals was analyzed on Southern blots with a human Rh-specific cDNA.Consistent with earlier reports, serologic results showed that gorilla and chimpanzee erythrocytes had epitopes recognized by human Rh D and c antisera, and gibbon erythrocytes were recognized by the c antisera. Surprisingly, some Old and New World monkeys also expressed a Rh c epitope on their erythrocytes. No erythrocytes from the nonprimate animals reacted specifically with any of the human Rh antisera.Southern blot analysis with a human Rh-specific cDNA probe detected Rh-related sequences in anthropoid apes, all New and Old World monkeys, and in most nonprimate animals tested. Although some Rh-related restriction fragments were conserved across species lines in primates, the Rh locus was more polymorphic in chimpanzees and gorillas than in humans. In addition, restriction fragments segregating with the presence of the D antigen in humans were present in the primate species that expressed the D antigen.     

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

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

Demographic influences on the behavior of chimpanzees

Recent research has revealed substantial diversity in the behavior of wild chimpanzees. Understanding the sources of this variation has become a central focus of investigation. While genetic, ecological, and cultural factors are often invoked to explain behavioral variation in chimpanzees, the demographic context is sometimes overlooked as a contributing factor. Observations of chimpanzees at Ngogo, Kibale National Park, Uganda, reveal that the size and structure of the unit group or community can both facilitate and constrain the manifestation of behavior. With approximately 150 individuals, the Ngogo community is much larger than others that have been studied in the wild. We have taken advantage of the unusual demographic structure of this community to document new and intriguing patterns of chimpanzee behavior with respect to hunting, territoriality, and male social relationships. Chimpanzees at Ngogo hunt often and with a considerable degree of success. In addition, male chimpanzees there frequently patrol the boundary of their territory and engage in repeated bouts of lethal intergroup aggression. By forming two distinct subgroups, male chimpanzees at Ngogo also develop social bonds above the level of dyadic pairs. While the sheer number of chimpanzees contributes to differences in hunting, patrolling, mating, and subgrouping at Ngogo, the demographic situation may also constrain behavioral interactions. At Ngogo, male chimpanzees who are closely related genetically through the maternal line do not appear to affiliate or cooperate with each other. Demographic constraints may be responsible for this finding. In this paper, I use these examples to illustrate how the demographic context affects the possible range of behavioral options open to individuals and ultimately contributes to the explanation of behavioral diversity in chimpanzees.     

Gorilla RH-like genes and antigens

 It has been previously shown that most of the human IgG monoclonal D-specific antibodies define a polymorphism in the gorilla consisting of two phenotypes: D^gor-positive and D^gor-negative. By quantitative indirect immunofluorescence assay and quantitative immunoblotting it was evaluated that the number of D^gor antigenic sites per gorilla red cell varies from a level equivalent to that observed for human RhD-positive cells to a level eight times higher. By immunoblotting with a rabbit reagent specific for the carboxylic end of human Rh-polypeptides it was demonstrated that RBCs from all gorillas, whatever their D^gor phenotype, possess 33000 relative molecular mass Rh-like polypeptides. The expression of the D^gor antigen was shown to be associated with the presence of three polymorphic bands defined by Southern blot using a human exon 4 RHCE probe, and to a length polymorphism of gorilla intron 3 evidenced by polymerase chain reaction. By contrast, the expression of the D^gor antigen was not associated to the length polymorphism of gorilla intron 4 which is related to the presence or absence of an Alu-Sx element in intron 4, paralleling the situation observed in human. These results confirmed the presence in the gorilla genome of at least two RH-like genes, one of which being responsible for D^gor polymorphism. The phylogenesis of the human and gorilla RH genes is discussed in light of the comparison of intron 4 sequences. Received: 23 March 1998 / Revised: 18 June 1998     

Hierarchy and social status in Budongo chimpanzees

The status hierarchy is fundamental in the lives of male chimpanzees. This study describes the dominance interactions and social status among adult male chimpanzees of the Sonso community in the Budongo Forest Reserve, Uganda, during the period that they were first studied (1994 and 1995). Social dominance is typically measured using the behaviour of either the subordinate or the dominant individual, but a relationship is dependent on the behaviour of both parties and this study explicitly used both subordinate and dominant behaviours to investigate the status hierarchy. Among adult males of the Sonso community, agonistic interactions occurred at a low rate and pant-grunts were rare, but males could be ranked into separate hierarchies of agonistic dominance and pant-grunting (labelled respect) using ratios of behaviour performed/behaviour received. These hierarchies were combined to form a single hierarchy of social status that divided the males among five distinct status levels. The highest status level was held by an alliance between two males who replaced the previous alpha male during the first part of the study. Neither male in this alliance partnership pant-grunted to the other, although the reason for cooperative behaviour was unclear. Although the nominally beta male was treated as such by other adult males, he achieved surprisingly little mating success. Budongo Forest chimpanzees do not warrant the sometimes-expressed view that they are non-aggressive and peaceable and the broad pattern of their status interactions matches with that seen in other chimpanzee populations.     

Survey of gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>) and chimpanzees (<Emphasis Type="Italic">Pan troglodytes troglodytes</Emphasis>) in Southwestern Cameroon

A study on the distribution and population density of the western lowland gorilla (Gorilla g. gorilla) and the central chimpanzee (Pan t. troglodytes) was undertaken between December 1997 and August 2000 in the Campo and Maan Forests in southwestern Cameroon. The aim of this survey was to estimate the densities of the apes in different parts of the area, to assess the importance of the region for the conservation of these endangered species and to determine the influence of human activities such as logging and hunting. The survey was based on night nest counts on a total of 665.5 km of line transects. The overall density in the Campo Forest was estimated at 0.2 gorillas/km² and at 0.63–0.78 chimpanzees/km². The overall density of chimpanzees in the Maan Forest was estimated at 0.8–1 individuals/km². Gorilla density in this area was too low to allow an estimation. The highest gorilla nest density was found in secondary forest. The gorilla density in unlogged forest was significantly lower. Chimpanzees showed a clear preference for less disturbed areas. In unlogged forest, old secondary forests (logging more than 23 years ago) and areas of recent logging with large remaining patches of primary forest, significantly higher densities were calculated than inside the more heavily exploited logging concession. In areas with both logging and high hunting pressure both species were rare or even absent. The Campo Maan area is considered a very important area for the conservation of gorillas and chimpanzees. Conservation measures are urgently required to reduce the impact of logging and hunting. The creation of the Campo Maan National Park in January 2000 is an important measure to preserve the unique biodiversity in this so far hardly protected area.     

Seasonal change in the composition of the diet of eastern lowland gorillas

Details are presented of the composition of the diet of eastern lowland gorillas, derived mainly from a study of their fresh trails and fecal analysis, during the course of an entire year in the tropical lowland forests of the Itebero region, Zaire. Gorillas ate 194 plant foods from 121 species and 45 families. They consumed 48 species of fruits; and 89% of fecal samples contained fruit seeds, but fruits were a relatively small part (25%) of the total number of food items. The composition of their diet changed seasonally. When consumption of fruit decreased in the long rainy and the long dry seasons, the gorillas ate, in addition to Zingiberaceae and Marantaceae, many kinds of leaf and bark, which may be an important buffer against the shortage of fruits. Gorillas also fed regularly on ants (Ponerinae), and the frequency of consumption showed small seasonal variations. From a comparison of diet composition, eastern lowland gorillas appeared to be intermediate between the other two subspecies. The choice of food showed differences in preference of fruits and insects between subspecies and may reflect high similarities within subspecies in lowland and montane forests.     

The function of male aggressive displays towards females in mountain gorillas

In groups ofGorilla g. beringei, male aggression towards females regularly takes the form of male display. This paper examines male display towards females in two Karisoke study groups (Group 5 and Group BM) in 1989, a period when none of the females were new immigrants. Results are based on 259 hr of focal observations and 121 hr ofad libitum observations on male behaviors towards females. The goal is to see if the data are compatible with four non-mutually exclusive hypotheses to explain male displays towards females: (1) demonstration of male fighting abilities to influence female long term residence decision; (2) decrease potential competitive inequities between females; (3) provision to females of an occasion to confirm their subordinance to a male; and (4) short term influence on mating. First, male-female proximity was tested against proportion of male displays, to rule out the possibility that males display towards females simply because they happen to be close by. There was no association between proximity and male display. Dominant males were responsible for a higher proportion of displays than subordinate males. This is consistent with the idea that males display to demonstrate their fighting abilities, or their qualities as protector, since dominant males are the ones offering long term protection against infanticide and predators. Females that were in a position to transfer did not receive a higher proportion of male display, however. Long term resident dominant females received a higher proportion of displays from the dominant males, which is consistent with the idea that males attempt to decrease potential competitive inequities between females. There was an association between female appeasement reactions and male displays, which suggests that males display to create occasions for the females to confirm their subordinance to them. Estrous females did not receive a higher proportion of male displays, and there was no association between male display and copulation, suggesting that male displays are not a form of courtship aggression aimed at influencing mating in the short term.     

Environmental factors influencing the seasonality of estrus in chimpanzees

Although the energetics of the estrous cycle in primates is not well understood, evidence suggests that energy and nutrient acquisition influence ovulation and the timing of conception. Energy for estrus has to compete with energy allocated for cellular maintenance, thermoregulation, movement for food, and predation avoidance. While some chimpanzee (Pan troglodytes) populations do not have a seasonal birth period, evidence suggests that there is seasonality in the number of estrous females. Similarly, the onset of postpartum cycles has been reported to be seasonal. We used 33 months of data from the Taï National Park, Côte dIvoire, to examine how the number of estrous females in a given month was influenced by the abundance and distribution of food, diet, rainfall and temperature. In a second analysis, we examined if there was a seasonal effect on first estrous swellings in adolescent females and postpartum adult females. Results demonstrated that the number of females in estrous in a given month was positively related to food abundance and percent foraging time spent eating insects, and negatively related to mean rainfall in the two preceding months and the mean high temperature. The timing of first estrous swellings of postpartum females and prepartum young females was positively related to the food abundance, and negatively related to mean high temperature. These results showed that environmental conditions can seasonally limit the energetically demanding estrus cycle. The presence of estrous females increases gregariousness in chimpanzee communities, and this study identified environmental factors that affect estrus directly and hence social grouping indirectly.     

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.     

Conflict and post-conflict behavior in a small group of chimpanzees

Chimpanzee research plays a central role in the discussions of conflict negotiation. Reconciliation, or the attraction and affiliation of former opponents following conflict, has been proposed as a central element of conflict negotiation in chimpanzees and various other taxa. In an attempt to expand the database of chimpanzee conflict resolution, conflict and post-conflict behavior were recorded for a small group of socially housed chimpanzees at the Chimpanzee and Human Communication Institute, at Central Washington University. Data were collected over six 6-week periods between 1997 and 2000, for a total of 840 hours of observation, resulting in a substantial post-conflict (PC) and matched control (MC) data set. The data demonstrate this group’s tendencies to maintain visual contact and closer proximity after conflicts. Dyadic corrected conciliatory tendencies ranged between 0 – 37.5% and averaged 17.25% across all dyads. Individual corrected conciliatory tendencies ranged between 5.8 and 32%. The results of this study combined with recent publications on captive and free-ranging chimpanzee post-conflict behavior suggest that variation in post-conflict behavior may be important to our understanding of chimpanzee conflict negotiation, and may also have implications for the design and management of captive chimpanzee enclosures and social groups, respectively.     

A mobile element based phylogeny of Old World monkeys

SINEs (Short INterspersed Elements) are a class of non-autonomous mobile elements that are <500 bp in length and have no open reading frames. Individual SINE elements are essentially homoplasy free with known ancestral states, making them useful genetic systems for phylogenetic studies. Alu elements are the most successful SINE in primate genomes and have been utilized for resolving primate phylogenetic relationships and human population genetics. However, no Alu based phylogenetic analysis has yet been performed to resolve relationships among Old World monkeys. Using both a computational approach and polymerase chain reaction display methodology, we identified 285 new Alu insertions from sixteen Old World monkey taxa that were informative at various levels of catarrhine phylogeny. We have utilized these elements along with 12 previously reported loci to construct a phylogenetic tree of the selected taxa. Relationships among all major clades are in general agreement with other molecular and morphological data sets but have stronger statistical support.     

Genetic Peculiarity of the Yakut Population as Inferred from Autosomal Loci

The autosomal gene pool of Yakuts was analyzed with a panel of polymorphic Alu insertions. The observed allele frequencies were typical for other Asian ethnic groups. Genetic differentiation of three Yakut populations was relatively high, 2%. East Siberian ethnic groups were shown to have a common gene pool and to experience no intense gene flow from other populations. Development of the Yakut gene pool was assumed to involve no substantial genetic effect of neighboring populations. The results fit both autochthonous and southern origin hypotheses.     

Predation on mammals by chimpanzees in the montane forest of Kahuzi, Zaire

The rate of predation on mammals by chimpanzees was determined from carcasses and from fecal specimens found on fresh trails during a 16-month period in the montane forest of Kahuzi-Biega National Park, Zaire. A unit-group of semi-habituated chimpanzees, composed of 22 – 23 individuals including 8 adult or adolescent males, appeared to kill about 18 – 30 mammalian prey (16 – 28Cercopithecus monkeys) per year, if the multiple kills by chimpanzees were not considered. A juvenile l'Hoest's monkey was recorded for the first time as the prey of chimpanzees in this study. Predation occurred in the late dry and the early rainy seasons, when the diversity of ripe fruits was the highest during the year. The Kahuzi chimpanzees tended to kill mammals less frequently but to killCercopithecus monkeys more frequently than chimpanzees in other habitats. The absence of red colobus monkeys, which are the most frequent prey in Gombe, Mahale, and Tai, might be responsible for the low predation rate. However, the estimated rate of predation onCercopithecus monkeys is the highest record among various chimpanzee habitats. At least 11 – 18% of theCercopithecus population seemed to be lost annually as a result of being killed by chimpanzees. Chimpanzees may be the most important predators on these monkeys in the absence of leopards at Kahuzi. The examination of fecal samples and carcasses suggested that adult (probably male) or adolescent chimpanzees tended to eat juvenile or subadult monkeys most frequently, as is also seen for chimpanzees in Gombe, Mahale, and Tai.     

Skeletal evidence of trauma in African apes, with special reference to the gombe chimpanzees

Incidence of cranial and postcranial skeletal trauma was investigated in samples of chimpanzees (Pan troglodytes troglodytes, P. troglodytes schweinfurthii), lowland gorillas (Gorilla gorilla gorilla), and bonobos (P. paniscus). The larger (adult) samples of chimpanzees (N=127 crania, 92 postcrania) and gorillas (N=136 crania, 62 postcrania) are curated at the Powell-Cotton Museum, Birchington, U.K. The bonobo collection (N=71 crania, 15 postcrania) is housed the Musée Royal de l'Afrique Centrale in Tervuren, Belgium. In addition, data were collected on the small but extremely well-documented skeletal sample from Gombe National Park (N=14 crania, 13 postcrania — including adults and adolescents). Cranial injuries, including healed fractures and bite wounds, were fairly frequent in the museum collection of chimpanzees (5.5% of individuals), but were twice as frequent in gorillas (11.0%). In the Gombe sample an even higher incidence was observed (28.6% of individuals). Bonobos, however, showed the lowest incidence of cranial trauma found among any of the African ape samples (1.4% of individuals). Postcranial trauma, documented most clearly by healed fractures, was seen in 21.7% of the Powell-Cotton chimpanzees, 30.8% of Gombe chimpanzees, 17.7% of gorillas, and in 13.3% of bonobos. Most of these lesions were found in the upper appendage. Nevertheless, highly debilitating healed fractures of the femur were also noted, most frequently and severe in female gorillas. The pattern of injuries suggests serious risks of falling in all free-ranging African apes, but also (in chimpanzees and gorillas) considerable risk from interindividual aggression, especially for males.