Non-invasive genetic monitoring of wild central chimpanzees

Abstract

Background: An assessment of population size and structure is an important first step in devising conservation and management plans for endangered species. Many threatened animals are elusive, rare and live in habitats that prohibit directly counting individuals. For example, a well-founded estimate of the number of great apes currently living in the wild is lacking. Developing methods to obtain accurate population estimates for these species is a priority for their conservation management. Genotyping non-invasively collected faecal samples is an effective way of evaluating a species' population size without disruption, and can also reveal details concerning population structure.

Methodology/principal findings: We opportunistically collected wild chimpanzee faecal samples for genetic capture-recapture analyses over a four-year period in a 132 km(2) area of Loango National Park, Gabon. Of the 444 samples, 46% yielded sufficient quantities of DNA for genotyping analysis and the consequent identification of 121 individuals. Using genetic capture-recapture, we estimate that 283 chimpanzees (range: 208-316) inhabited the research area between February 2005 and July 2008. Since chimpanzee males are patrilocal and territorial, we genotyped samples from males using variable Y-chromosome microsatellite markers and could infer that seven chimpanzee groups are present in the area. Genetic information, in combination with field data, also suggested the occurrence of repeated cases of intergroup violence and a probable group extinction.

Conclusions/significance: The poor amplification success rate resulted in a limited number of recaptures and hence only moderate precision (38%, measured as the entire width of the 95% confidence interval), but this was still similar to the best results obtained using intensive nest count surveys of apes (40% to 63%). Genetic capture-recapture methods applied to apes can provide a considerable amount of novel information on chimpanzee population size and structure with minimal disturbance to the animals and represent a powerful complement to traditional field-based methods.

Figure 1. Determination of chimpanzee group composition and minimum territory size.

Each letter represents an individual's genotype and its sampling location over the course of the entire study period. Females are denoted by ♀, males are denoted by ♂. Underlined samples were found at the same location on the same day. (i) Relative geographic locations of samples from individuals A through F (ii) Assuming that individuals found together belong to the same group, here male B links together samples A and C, thus A,B & C are all members of a single community. (iii) If males B, E & D all carry the same Y-haplotype we assume they belong to the same community and draw a minimum convex polygon (MCP) around these individuals. As chimpanzees are territorial, we assume that females found within this MCP belong to the males' community. Thus, individuals, A, B, C, D & E all belong to the same community. (iv) Because female C was found within the Y-haplotype defined MCP at one collection event, we can extend the MCP to include any other sampling events of female C. By doing so, female F now also falls within the MCP of the group so that individuals A, B, C, D, E & F all belong to the same group. See text for exceptions to these rules.

Figure 2. Map of Loango research site, geographic location of all faecal samples in study and the seven Loango chimpanzee groups.

Males are designated by their Y-chromosome haplotype (uppercase A-I). Females are designated by the lowercase letter(s) of the group in whose minimum convex polygon (MCP) they were found (a, bi, c, dg, e, f or h). Females that did not occur in any MCP or that were found in association with more than one group throughout the study are represented by black circles. In cases where females were found both within and outside of a given MCP, the MCP was enlarged to include the “exterior” geographic location of the female. MCPs represent minimum territory boundaries of each chimpanzee community. Area of MCPs stated in parentheses in legend. For group H (southern most points) only 2 individuals were identified and so no MCP could be drawn. Inset, map of Africa with Gabon highlighted in white, arrow indicates location of Loango field site.

Figure 3. Loango chimpanzee groups and composition over the 4-year study period.

ID is consensus name given to matching chimpanzee genotypes. In row “sex”, M = male, F = female. Y-hap refers to the Y-chromosome haplotype of the male individual. Y-hap MCP is the group membership identity of each individual based on their exclusive inclusion in any of the Y-haplotype defined MCPs. B?/A? means individual may belong or have belonged to either group B or A over the study period. A?/C? individual may belong or have belonged to either group C or A. “?” indicates females could not be attributed to any group. Grey boxes bound first and last instance when group members detected over the 4-year study period.

Figure 4. Frequency of detection of individual chimpanzee genotypes during the study period.