Use of Genetic Analysis to Determine Population Structure in the Cross River Gorilla

Many animals today, including some gorilla populations, live in patchy discontinuous habitats as a result of human alteration of the environment. When small populations become fragmented and migration between subpopulations decreases or stops, consequent increases in inbreeding and loss of genetic diversity can have serious negative effects on the long-term viability of population fragments and, by extension, the population as a whole. Determining which subpopulations are in migratory contact with each other can highlight important dispersal corridors as well as identify isolated areas, thereby suggesting priority areas for conservation.
We used genetic analysis of a large collection of non-invasively collected samples to assess patterns of population structure and migration in the Cross River gorilla (see Bergl & Vigilant 2007 for a full account). These gorillas are located at least 200 km northwest of other gorilla populations and are largely restricted to rugged highland areas straddling the Nigeria-Cameroon border. Recently revived as a distinct subspecies, Gorilla gorilla diehli (Sarmiento & Oates 2000; Groves 2001), the Cross River gorilla is one of Africa's most critically endangered primates (IUCN 2005). Recent surveys suggest that the total population numbers fewer than 300 individuals and is fragmented into as many as 10th separate localities with limited potential for reproductive contact and unknown population structure (Oates et al. 2003; Sunderland-Groves et al. 2003; Sunderland-Groves & Jaff 2004). Despite its distinctiveness and high degree of threat, little is known of the Cross River gorilla beyond cranial morphology, basic distribution and single-site studies of feeding ecology (Sarmiento & Oates 2000; Oates et al. 2003; Stumpf et al. 2003).
Between December 2002 and September 2004, fecal samples (N = 322) were collected from gorilla night nests and trails during intensive nest searches and reconnaissance walks at all but one of the known Cross River gorilla localities. Unfortunately, the small number and poor quality of samples from three other localities (Okwangwo-Takamanda, Takamada East and Takamanda North) resulted in these areas being unrepresented in the analysis. The remaining samples allowed us to conduct a range of genetic analyses to assess population structure and patterns of migration.

Population Structure
We were able to detect a previously unknown population structure in the Cross River gorilla. Our analysis suggests that three subpopulations are present: a large central subpopulation consisting of the majority of known Cross River gorilla localities, and two peripheral subpopulations represented by the gorillas of Afi (western subpopulation) and Kagwene Mountains (eastern subpopulation). This pattern of subdivision corresponds largely to patterns of habitat fragmentation. The constituent localities of the central subpopulation are all connected by continuous forested lowland habitat, with the exception of Mone North which is separated by a small road and scattered farm land. In contrast, Afi Mountain is almost totally isolated from other gorilla areas by farmland and a frequently travelled highway. Likewise, Kagwene Mountain, though connected to Upper Mbulu by a narrow forest corridor, is largely surrounded by substantial areas of montane grassland and farmland.

Migration
Prior research on this population suggested that migration between gorilla localities was likely rare (Bucknell & Groves 2002; Oates et al. 2003; Sunderland-Groves et al. 2003). Our genetic data show that some animals have migrated between localities within the current generation. We were able to identify as migrants four individuals (two male and two female) from four different localities. Two migrants (one male and one female) each moved from one of the two most isolated localities (Kagwene and Afi mountains) into the nearest neighbouring locality (Upper Mbulu and Mbe Mountains, respectively). However, neither of these two source localities appears to be a recipient of migrants as both are genetically quite homogenous (though one Afi individual apparently does have admixed ancestry).
In undisturbed gorilla populations, where there are relatively high densities of gorillas, animals that disperse from their natal group are likely to find other groups or individuals quite readily, whereas in areas such as Kagwene and Afi Mountains, where there appear to be only single social groups or very small communities of gorillas (Oates et al. 2003), opportunities for dispersing individuals to find new groups will be limited. Thus, dispersers will be under pressure to travel long distances or cross barriers such as roads and disturbed forest, potentially resulting in large dispersal distances. This may explain why individuals migrated from even relatively isolated areas like Afi and Kagwene.
The other two migrants detected were collected in Takamanda South and Mone North, but could not be definitively assigned to a source population. Likely source localities for these migrants, based on geographic proximity, are among the unsampled gorilla areas.
In addition to these migrants, several individuals of admixed ancestry were detected. This suggests that migrants are not only able to move between localities, but are also reproducing.

Conservation Implications
The genetic population structure we detected in Cross River gorillas has important implications for the conservation and management of this critically endangered primate. Overall, our analyses suggest that the situation facing this population is not quite as dire as had been assumed. We documented reproductive connectivity during the current generation between several localities, including the most peripheral population nuclei, and genetic similarity between most of the sampled localities. Using conservative criteria, approximately 11% (8 of 71) of individuals were inferred to be migrants or to have recent ancestry from more than one locality.
Conservation efforts must, therefore, focus on the maintenance, and if possible, expansion, of forest connectivity between gorilla localities. While such actions present a challenge for both conservation biologists and wildlife managers, the situation allows for some optimism given that substantial habitat remains between many of the areas. Only two of the gorilla localities are separated by habitat discontinuities (i.e., roads separating Afi Mountain and Mone North from the central portion of the gorillas' range), and, even in these cases, forested habitat abuts the discontinuity. In all other cases, at least narrow forest corridors (and in many cases large continuous areas of forest) connect the population nuclei.
Much of the forest which constitutes Cross River gorilla habitat is already legally protected, and several additional areas are currently being considered for protected area status. Yet key corridors, such as those between Kagwene Mountain and Upper Mbulu, and between Mone North and the other members of the central subpopulation, currently have no legal status. Revision of the status of these areas needs to be considered.
Besides habitat loss, other human activities, such as bushmeat hunting in particular, can also limit migration. Extensive hunting in lowland areas is likely the main cause of the gorillas' current distribution in the highlands. This pressure needs to be relaxed in order to allow migration through, and potentially recolonization of, lowland habitat. Control of hunting is particularly important in the center of the gorillas' range, which contains the largest concentration of gorillas and substantial areas (approximately 1,300 km²) of continuous forest.

Richard A. Bergl and Linda Vigilant

This article is largely excerpted from: Bergl & Vigilant (2007). Financial support for this project was provided by the National Geographic Society Conservation Trust, Conservation International, Lincoln Park Zoo, Primate Conservation Inc., and the Max Planck Society. We thank the National Parks Service (Nigeria), the Cross River State Forestry Commission (Nigeria), and the Ministry of Environment (Cameroon) for allowing R. Bergl to conduct fieldwork in areas under their management. We thank J. Oates for help in developing and implementing the project. We also thank J. Sunderland-Groves, M. Ashu, E. Nwufoh, A. Mbong, C. Ransom, N. Mkpe, M. Tabeh, P. Jenkins, L. Gadsby, the Wildlife Conservation Society and local assistants too numerous to mention for assistance in the field. Thanks to A. Abraham, M. Arandjelovic, B. Bradley, D. Lukas, K. Langergraber, H. Siedel and O. Thalmann for assistance with laboratory analyses and helpful discussion.

References
Bergl, R. A. & Vigilant, L. (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Molecular Ecology 16, 501-516
Bucknell, D. & Groves, J. L. (2002) Local Perception of the Population Size, Distribution and Ranging Behaviour of the Cross River Gorilla Within the Takamanda and Mone Forest Reserves and the Mbulu Forest, Cameroon. New York (Wildlife Conservation Society Report)
Groves C. P. (2001) Primate Taxonomy. Washington, DC (Smithsonian Institution Press)
IUCN (2005) 2005 IUCN Red List of Threatened Species. Gland (IUCN)
Oates, J. et al. (2003) The Cross River gorilla: Natural history and status of a neglected and critically endangered subspecies. In: Taylor, A. & Goldsmith, M. L. (eds.) Gorilla Biology. Cambridge (Cambridge University Press)
Sarmiento, E. E. & Oates, J. F. (2000) The Cross River gorilla: a distinct subspecies Gorilla gorilla diehli Matschie 1904. American Museum Novitates 3304, 1-55
Stumpf, R. et al. (2003) Patterns of diversity in gorilla cranial morphology. In: Taylor, A. & Goldsmith, M. L. (eds.) Gorilla Biology: A Multidisciplinary Perspective. Cambridge (Cambridge University Press)
Sunderland-Groves, J. L. & Jaff, B. (2004) Developing a Conservation Strategy for the Cross River Gorilla: Proceedings of the 2nd International Workshop and Conference on the Conservation of the Cross River Gorilla. New York (Wildlife Conservation Society)
Sunderland-Groves, J. L. et al. (2003) Surveys of the Cross River gorilla and chimpanzee populations in Takamanda Forest Reserve, Cameroon. In: Comiskey, J. A. et al. (eds.) Takamanda: The Biodiversity of an African Rainforest. Washington, DC (Smithsonian Institution)

Dr. Richard Bergl conducted his Ph.D. research on the Cross River gorilla population in Nigeria and Cameroon. He is currently Curator of Conservation and Research at the North Carolina Zoological Park.
Dr. Linda Vigilant directs research focused on genetic analysis of wild primate populations at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany.

Cross River overview

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