Long-term home range stability provides foraging benefits in western gorillas.

OBJECTIVES: Long-term home range stability presumably emerges because familiarity with an area improves fitness through increased foraging efficiency, reduced predation risk, or reduced costs of intergroup aggression. While the use of spatial memory by primates has been widely demonstrated, few studies have examined whether long-term space use creates opportunities for interannual reuse of spatial knowledge. Here we examine the ranging behavior of western gorillas (Gorilla gorilla) to assess the degree of long-term site fidelity and the foraging consequences of reuse of space. METHODS: We measured interannual home range overlap over a 10-year period for a single group of gorillas at the Mondika Research Center, using both grid-based and kernel density estimation. By plotting the total area used over time, we identified periods of home-range stability and expansion. We compared foraging and ranging behavior in familiar versus unfamiliar areas, considering fruit trees visited, dietary diversity, and daily path length, to determine whether the lack of spatial knowledge in unfamiliar areas was associated with foraging costs. RESULTS: Average interannual home range overlap by the group remained high throughout the study. During periods of home range expansion, daily path lengths increased but not the number of fruit trees visited, suggesting that reduced familiarity with the area led to decreased foraging efficiency because individuals lacked prior knowledge of where to find resources. DISCUSSION: Western gorillas at Mondika exhibit long-term home range stability, presumably reflecting a strategy that relies on the use of spatial memory to increase foraging efficiency that is favored by their reliance on ephemeral fruit resources.

Spatial cognition in western gorillas (Gorilla gorilla): an analysis of distance, linearity, and speed of travel routes.

Spatial memory allows animals to retain information regarding the location, distribution, and quality of feeding sites to optimize foraging decisions. Western gorillas inhabit a complex environment with spatiotemporal fluctuations of resource availability, prefer fruits when available, and travel long distances to reach them. Here, we examined movement patterns-such as linearity, distance, and speed of traveling-to assess whether gorillas optimize travel when reaching out-of-sight valued resources. Our results show that gorillas travel patterns are affected by the activity they perform next, the type of food they feed on, and their preference level to specific fruits, suggesting they are able to optimize foraging based on spatial knowledge of their resources. Additionally, gorillas left in the direction of the next resource as soon as they started traveling and decelerated before approaching food resources, as evidence that they have a representation of their exact locations. Moreover, home range familiarity did not influence gorillas' movement patterns, as travel linearity in the core and periphery did not differ, suggesting that they may not depend wholly on a network of paths to navigate their habitat. These results show some overlap with chimpanzees' spatial abilities. Differences between the two ape species exist, however, potentially reflecting more their differences in diet (degree of frugivory) rather than their cognitive abilities. Further studies should focus on determining whether gorillas are able to use shortcuts and/or approach the same goal from multiple directions to better identify the spatial abilities used by this species.

Exaggerated Sexual Swellings and the Probability of Conception in Wild Sanje Mangabeys (Cercocebus sanjei).

Females of several catarrhine primate species exhibit exaggerated sexual swellings that change in size and coloration during the menstrual cycle and, in some species, gestation. Although their function remains under debate, studies indicate that swellings may contain information males could use to discern ovulation and the probability that a cycle will be conceptive. Here we combine visual ratings of swellings with hormonal data for a group of Sanje mangabeys (18 adult, 3 adolescent females) to determine if their swellings provide reliable information on female fertility. In all cases where ovulation was detected (N = 7), it occurred during maximum tumescence, and in 83.3% during the first two days of the "shiny phase," a period during maximum tumescence when the swelling was brightest. There were no significant differences in maximum tumescence and shiny phase duration among cycles of different probability of conception, although there was a trend toward conceptive cycles exhibiting shorter shiny phases than nonconceptive ones. Only 25% (N = 4) of postconceptive swellings developed the shiny phase, and adolescents displayed the longest maximum tumescence and shiny phases. The conspicuous nature of the shiny phase and the frequent overlap between its onset and ovulation suggest that its presence serves as a general signal of ovulation and that the cycle has a high probability of being conceptive. It also suggests that swellings in some Sanje mangabeys are more accurate signals of fertility than in other primates.

The function of loud calls (Hoot Series) in wild western gorillas (Gorilla gorilla).

The use of loud vocal signals to reduce distance among separated social partners is well documented in many species; however, the underlying mechanisms by which the reduction of spacing occurs and how they differ across species remain unclear. Western gorillas (Gorilla gorilla) offer an opportunity to investigate these issues because their vocal repertoire includes a loud, long-distance call (i.e., hoot series) that is potentially used in within-group communication, whereas mountain gorillas use an identical call exclusively during intergroup encounters. First, we tested whether the hoot series functions as a contact/separation call. Second, we examined which individuals were more likely to reply and which party was more responsible for decreasing distance to identify the underlying mechanisms and cognitive implications of hoot series. We collected behavioral, spatial, and acoustic data on five adult gorillas over 15 months at the Mondika Research Center (Republic of Congo and CAR). Hoot series are individually distinct calls and given by both male and female gorillas when separated from each other. Following hooting, the distance between separated group members decreased significantly; thus we concluded that western gorillas use this call to reestablish group cohesion. The way in which proximity was achieved depended upon listeners replying or not to the caller. Replies may indicate a conflict between callers about intended travel direction, with vocal interchanges serving to negotiate a consensus. Although the acoustic features of vocal signals are highly constrained in closely related species, our results demonstrate that the function and usage of particular calls can be flexible.

Individual distinctiveness in call types of wild western female gorillas.

Individually distinct vocalizations play an important role in animal communication, allowing call recipients to respond differentially based on caller identity. However, which of the many calls in a species' repertoire should have more acoustic variability and be more recognizable is less apparent. One proposed hypothesis is that calls used over long distances should be more distinct because visual cues are not available to identify the caller. An alternative hypothesis proposes that close calls should be more recognizable because of their importance in social interactions. To examine which hypothesis garners more support, the acoustic variation and individual distinctiveness of eight call types of six wild western gorilla (Gorilla gorilla) females were investigated. Acoustic recordings of gorilla calls were collected at the Mondika Research Center (Republic of Congo). Acoustic variability was high in all gorilla calls. Similar high inter-individual variation and potential for identity coding (PIC) was found for all call types. Discriminant function analyses confirmed that all call types were individually distinct (although for call types with lowest sample size - hum, grumble and scream - this result cannot be generalized), suggesting that neither the distance at which communication occurs nor the call social function alone can explain the evolution of identity signaling in western gorilla communication.

Reproductive characteristics of wild Sanje mangabeys (Cercocebus sanjei).

An accurate description of reproductive characteristics and ovarian endocrinology is necessary to address questions about the reproductive strategies and life history of a species and for meaningful, cross species analyses. Here we used analysis of fecal estradiol (fE) and behavioral observations to determine for the first time the reproductive characteristics and endocrinology of a wild group (N = 18 adult and 3 adolescent females) of Sanje mangabeys (Cercocebus sanjei). The study was conducted in the Udzungwa Mountains National Park, Tanzania, from October 2008 through September 2010. Average cycle length (±SD) was 29.3 ± 3.2 days in adults and 51.4 ± 5.5 days in adolescents. Menses appeared within 5.1 ± 2.1 days in adults and 4.8 ± 0.3 days in adolescents after the end of maximum tumescence, and lasted 6.7 ± 3.1 and 10.3 ± 5.0 days, respectively. Infant death tended to reduce the number of cycles to conception (4.3 ± 1.5 cycles after a surviving infant vs. 2.6 ± 1.0 cycles after infant death). Adolescents cycled for at least 16 months without conceiving. Implantation bleeding began 17.5 ± 0.7 days from the onset of detumescence, and lasted 10.0 ± 1.4 days. Gestation length averaged 171.8 ± 3.4 days. Postpartum amenorrhea lasted 6.7 ± 2.3 months while females whose infants had died resumed cycling within 14.3 ± 5.9 days. The interbirth interval after a surviving infant averaged 20.0 ± 4.3 months. These reproductive characteristics of the Sanje mangabey resembled those of other mangabeys and related cercopithecines, with the exception of an earlier onset and longer duration of menstruation and implantation bleeding. Further information on the physiology of the Sanje mangabey is needed to clarify what factors may cause the unusual characteristics of both, their menses and implantation bleeding.

The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest.

To understand the evolutionary histories and conservation potential of wild animal species it is useful to assess whether taxa are genetically structured into different populations and identify the underlying factors responsible for any clustering. Landscape features such as rivers may influence genetic population structure, and analysis of structure by sex can further reveal effects of sex-specific dispersal. Using microsatellite genotypes obtained from noninvasively collected fecal samples we investigated the population structure of 261 western lowland gorillas (WLGs) (Gorilla gorilla gorilla) from seven locations spanning an approximately 37,000 km(2) region of mainly continuous rain forest within Central African Republic (CAR), Republic of Congo and Cameroon. We found our sample to consist of two or three significantly differentiated clusters. The boundaries of the clusters coincided with courses of major rivers. Moreover, geographic distance detoured around rivers better-explained variation in genetic distance than straight line distance. Together these results suggest that major rivers in our study area play an important role in directing WLG gene flow. The number of clusters did not change when males and females were analyzed separately, indicating a lack of greater philopatry in WLG females than males at this scale.

Seasonal mortality patterns in non-human primates: implications for variation in selection pressures across environments.

Examining seasonal mortality patterns can yield insights into the drivers of mortality and thus potential selection pressures acting on individuals in different environments. We compiled adult and juvenile mortality data from nine wild non-human primate taxa to investigate the role of seasonality in patterns of mortality and address the following questions: Is mortality highly seasonal across species? Does greater environmental seasonality lead to more seasonal mortality patterns? If mortality is seasonal, is it higher during wet seasons or during periods of food scarcity? and Do folivores show less seasonal mortality than frugivores? We found seasonal mortality patterns in five of nine taxa, and mortality was more often tied to wet seasons than food-scarce periods, a relationship that may be driven by disease. Controlling for phylogeny, we found a positive relationship between the degree of environmental seasonality and mortality, with folivores exhibiting more seasonal mortality than frugivores. These results suggest that mortality patterns are influenced both by diet and degree of environmental seasonality. Applied to a wider array of taxa, analyses of seasonal mortality patterns may aid understanding of life-history evolution and selection pressures acting across a broad spectrum of environments and spatial and temporal scales.

The strategic use of sex in wild female western gorillas.

Human females, unlike most mammals, are sexually active outside of fertile periods. This decoupling of sexual behavior from its conceptive function has had an enormous impact on human social relationships, and yet we know little about why there was selection for nonconceptive mating. Here we examine one form of nonconceptive mating, the mating that occurs during pregnancy or post-conceptive (PC) mating, in wild western gorillas (Gorilla gorilla). Using a near complete mating record for five females during gestation, we show that pregnant females varied in the timing and frequency of mating, and used PC mating conditionally, synchronizing copulations to occur on days when other females mated, and refraining from mating for lengthy periods when no other females mated. As pregnant females mated exclusively with the same male before and after conception, and mated in response to group female (and not male) behavior, we conclude that western gorillas used PC mating as a form of female competition, and not to confuse paternity or to obtain immediate benefits from the male, as suggested earlier. The male initiated copulations preferentially with females of high rank, rather than distinguishing between pregnant and cycling females. Therefore, PC mating appears to be a strategy by which high-ranking pregnant females attempt to minimize male interest in other females, while reinforcing their own status and potentially delaying conception in others. These findings indicate that female-mating competition is more important than considered earlier, and may be a factor in the evolution of nonconceptive mating in humans.

Potential for female kin associations in wild western gorillas despite female dispersal.

Female philopatry and male dispersal are the norm for most mammals, and females that remain in their natal region often derive foraging or social benefits from proximity to female kin. However, other factors, such as constraints on group size or a shortage of potential mates, may promote female dispersal even when female kin associations would be beneficial. In these cases, female kin associations might develop, not through female philopatry, but through female emigration to the same group. To date, little attention has been focused on the potential for kin-biased behaviour between females in female-dispersing species. Here we investigate the genetic relationships among adults in eight wild groups of unhabituated western gorillas (Gorilla gorilla) at the Mondika Research Center using microsatellite genotyping of DNA collected from hair and faeces. We found that almost half (40%) of adult females had an adult female relative in the same group and average within-group relatedness among females was significantly higher than that expected under a model of random dispersal. This provides the first genetic evidence that females can maintain social associations with female relatives in spite of routine natal and secondary dispersal. In addition, we show that females appear to avoid related silverback males when making dispersal decisions, suggesting that a strategy of non-random female dispersal may also function to avoid inbreeding.

Habituation of western gorillas: the process and factors that influence it.

Habituation of western gorillas to human presence is generally an expensive, lengthy and difficult process. Here we describe the habituation process for two groups of western gorillas at the Mondika Research Center, with the hope that the lessons we learned will facilitate future gorilla studies. We expand upon earlier studies by describing the process through complete habituation for both males and females, and for more than one group. The major obstacle to habituation was developing sufficient tracking skills to follow gorilla trail on a daily basis. Once this was achieved, the silverback became semi-habituated (i.e. ignoring human presence during half of contacts) within a year, although the majority of group females continued to avoid humans. As female presence at contacts increased, a period of male recidivism followed, requiring an additional year before his complete habituation was reached. Habituating the females took longer than the male, but we found, contrary to earlier studies, that it consisted of the same stages, including avoidance, aggression, and curiosity before habituation. We compare results between groups and across sites and discuss how factors such as tracking abilities, group size and cohesion, population density and home range overlap, and the manner of approaching gorillas during contacts influence the habituation process.

Potential for Ebola transmission between gorilla and chimpanzee social groups.

Over the past decade Ebola hemorrhagic fever has emerged repeatedly in Gabon and Congo, causing numerous human outbreaks and massive die-offs of gorillas and chimpanzees. Why Ebola has emerged so explosively remains poorly understood. Previous studies have tended to focus on exogenous factors such as habitat disturbance and climate change as drivers of Ebola emergence while downplaying the contribution of transmission between gorilla or chimpanzee social groups. Here we report recent observations on behaviors that pose a risk of transmission among gorilla groups and between gorillas and chimpanzees. These observations support a reassessment of ape-to-ape transmission as an amplifier of Ebola outbreaks.

Plant DNA sequences from feces: potential means for assessing diets of wild primates.

Analyses of plant DNA in feces provides a promising, yet largely unexplored, means of documenting the diets of elusive primates. Here we demonstrate the promise and pitfalls of this approach using DNA extracted from fecal samples of wild western gorillas (Gorilla gorilla) and black and white colobus monkeys (Colobus guereza). From these DNA extracts we amplified, cloned, and sequenced small segments of chloroplast DNA (part of the rbcL gene) and plant nuclear DNA (ITS-2). The obtained sequences were compared to sequences generated from known plant samples and to those in GenBank to identify plant taxa in the feces. With further optimization, this method could provide a basic evaluation of minimum primate dietary diversity even when knowledge of local flora is limited. This approach may find application in studies characterizing the diets of poorly-known, unhabituated primate species or assaying consumer-resource relationships in an ecosystem.

Locomotor behavior and long bone morphology in individual free-ranging chimpanzees.

We combine structural limb data and behavioral data for free-ranging chimpanzees from Taï (Ivory Coast) and Mahale National Parks (Tanzania) to begin to consider the relationship between individual variation in locomotor activity and morphology. Femoral and humeral cross sections of ten individuals were acquired via computed tomography. Locomotor profiles of seven individuals were constructed from 3387 instantaneous time-point observations (87.4 hours). Within the limited number of suitable chimpanzees, individual variation in locomotor profiles displayed neither clear nor consistent trends with diaphyseal cross-sectional shapes. The percentages of specific locomotor modes did not relate well to diaphyseal shapes since neither infrequent nor frequent locomotor modes varied consistently with shapes. The percentage of arboreal locomotion, rather than estimated body mass, apparently had comparatively greater biological relevance to variation in diaphyseal shape. The mechanical consequences of locomotor modes on femoral and humeral diaphyseal shapes (e.g., orientation of bending strains) may overlap between naturalistic modes more than currently is recognized. Alternatively, diaphyseal shape may be unresponsive to mechanical demands of these specific locomotor modes. More data are needed in order to discern between these possibilities. Increasing the sample to include additional free-ranging chimpanzees, or primates in general, as well as devoting more attention to the mechanics of a greater variety of naturalistic locomotor modes would be fruitful to understanding the behavioral basis of diaphyseal shapes.

Impact of ecological and social factors on ranging in western gorillas.

We examined the influence of ecological (diet, swamp use, and rainfall) and social (intergroup interaction rate) factors on ranging behavior in one group of western gorillas (Gorilla gorilla gorilla) during a 16-month study. Relative to mountain gorillas, western gorillas live in habitats with reduced herb densities, more readily available fruit (from seasonal and rare fruit trees), and, at some sites, localized large open clearings (swamps and "bais"). Ranging behavior reflects these ecological differences. The daily path length (DPL) of western gorillas was longer (mean=2,014 m) than that of mountain gorillas, and was largely related to fruit acquisition. Swamp use occurred frequently (27% of days) and incurred a 50% increase in DPL, and 77% of the variation in monthly frequency of swamp use was explained by ripe fruit availability within the swamp, and not by the absence of resources outside the swamp. The annual home-range size was 15.4 km2. The western gorilla group foraged in larger areas each month, and reused them more frequently and consistently through time compared to mountain gorillas. In contrast to mountain gorillas, intergroup encounters occurred at least four times more frequently, were usually calm rather than aggressive, and had no consistent effect on DPL or monthly range size for one group of western gorillas. High genetic relatedness among at least some neighboring males [Bradley et al., Current Biology, in press] may help to explain these results, and raises intriguing questions about western gorilla social relationships.

Behavioral ecology of western gorillas: new insights from the field.

The papers in this issue are from a conference held in May 2002 at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany. This conference brought together researchers from all current western gorilla sites for the first time with the aim of synthesizing the most current information available on western gorilla behavioral ecology. Our goal was to assess the degree of behavioral diversity in gorillas in light of our current understanding of social evolution. The articles include 1) synopses of the current information on western gorilla foraging strategy, social behavior, life history, and genetic variation; 2) more-detailed descriptions of home-range use and intergroup encounters across sites; and 3) the first description of the social behavior of western gorilla females.

Dispersed male networks in western gorillas.

Although kin-selection theory has been widely used to explain the tendency of individuals to bias beneficial behaviors towards relatives living within the same social group, less attention has focused on kin-biased interactions between groups. For animal societies in which females emigrate, as is the case for mountain gorillas (Gorilla beringei beringei), encounters between males in different groups often involve aggressive displays that can escalate to physical violence and fatal injuries. However, recent findings on the little-studied western gorilla (Gorilla gorilla) indicate that interactions between social groups occur more frequently than they do in mountain gorillas and are often, although not always, surprisingly nonaggressive. We investigated the pattern of genetic relationships between individuals of different groups and found evidence suggesting a previously unrecognized "dispersed male network" social structure in western gorillas in which the single males leading social groups were usually related to one or more nearby males. We propose that this provides a basis for extra-group, kin-biased behaviors and may explain the reported peaceful intergroup interactions. Furthermore, these results suggest that a patrilocal social structure, in which males remain in their natal region and potentially benefit from kin associations, is a feature unifying African apes and humans.