Genetic censusing identifies an unexpectedly sizeable population of an endangered large mammal in a fragmented forest landscape

Abstract

Background: As habitat degradation and fragmentation continue to impact wildlife populations around the world, it is critical to understand the behavioral flexibility of species in these environments. In Uganda, the mostly unprotected forest fragment landscape between the Budongo and Bugoma Forests is a potential corridor for chimpanzees, yet little is known about the status of chimpanzee populations in these fragments.

Results: From 2011 through 2013, we noninvasively collected 865 chimpanzee fecal samples across 633 km(2) and successfully genotyped 662 (77%) at up to 14 microsatellite loci. These genotypes corresponded to 182 chimpanzees, with a mean of 3.5 captures per individual. We obtained population size estimates of 256 (95% confidence interval 246-321) and 319 (288-357) chimpanzees using capture-with-replacement and spatially explicit capture-recapture models, respectively. The spatial clustering of associated genotypes suggests the presence of at least nine communities containing a minimum of 8-33 individuals each. Putative community distributions defined by the locations of associated genotypes correspond well with the distribution of 14 Y-chromosome haplotypes.

Conclusions: These census figures are more than three times greater than a previous estimate based on an extrapolation from small-scale nest count surveys that tend to underestimate population size. The distribution of genotype clusters and Y-chromosome haplotypes together indicate the presence of numerous male philopatric chimpanzee communities throughout the corridor habitat. Our findings demonstrate that, despite extensive habitat loss and fragmentation, chimpanzees remain widely distributed and exhibit distinct community home ranges. Our results further imply that elusive and rare species may adapt to degraded habitats more successfully than previously believed. Their long-term persistence is unlikely, however, if protection is not afforded to them and habitat loss continues unabated.

Figure 1

Map of the study area in Uganda. The inset map displays the landscape’s location within Uganda. Green indicates forest cover during the study period.

Figure 2

Map of search effort over the study area. One-km² grid cells are overlaid over the corridor region between the Budongo and Bugoma Forests. Gray shading indicates relative search effort in each cell, with the number of search occasions (days) binned. Search effort was not available in the Bulindi area, where samples were collected during concurrent long-term research.

Figure 3

Genotyped sample collection locations across the study area. Not all samples are visible due to map scaling. The black line indicates the region of integration used in the SECR model. Samples outside the region of integration were collected in Siiba Forest Reserve and were excluded from analysis.

Figure 4

Putative chimpanzee communities (a) and associated Y-chromosome haplotypes (b). a Minimum convex polygons (MCPs) for genotyped samples found in association. Names of putative chimpanzee communities correspond to nearest villages and are listed below the MCP, with Y-chromosome haplotypes found in that putative community listed in parentheses. Underlined names indicate researched communities with preexisting data on approximate community sizes and home range extents. Each community is represented by a unique color. b Median joining network for the 14 Y-chromosome haplotypes. The relative similarity of haplotypes is represented by the lengths of branches, and the relative frequency of occurrence of each haplotype is indicated by the sizes of circles. Colors in haplotype circles correspond to putative communities in (a) exhibiting that haplotype.