2025 Theses Doctoral

Hanging on in a forest fragment? The long and short-term effects of habitat loss on guenon monkeys with a focus on golden monkeys (Cecopithecus mitis kandti) in Rwanda

Johnston, Amanda

Habitat loss is one of the greatest threats to biodiversity and has a range of negative consequences that are both immediate and time delayed. Immediate effects, such as population decline and loss of resources, are easy to observe. However, the effects that are time-delayed, such as inbreeding depression, can be harder to identify. Often these effects interact. For example, large-scale population loss can, over time, lead to inbreeding depression.

The subsequent decrease in health can leave an individual at higher risk of infection with parasites or disease. These effects are also magnified in small, isolated populations, such as those in forest fragments. Identifying how habitat loss affects wildlife, particularly vulnerable populations, is not only important for conservation efforts, but to understand the mechanisms that can lead to population decline and extinction.The guenons are a tribe of largely forest-dwelling monkeys that are widely distributed across sub-Saharan Africa. Many guenons have experienced habitat loss, largely because of deforestation for economic development.

One such taxon is the golden monkey (Cercopithecus mitis kandti), a subspecies of mitis monkey with only two extant populations. The first and much larger population (> 4000) is spread across the Virunga Massif, with the Rwandan portion of the population residing in Volcanoes National Park (VNP). The second, smaller (~ 200) population is found in Gishwati Forest, Rwanda. Historically, the two populations were connected, but more than three decades of deforestation, beginning prior to the 1970s, separated and isolated them. While VNP lost around 25 percent of its total forest cover, deforestation in Gishwati Forest continued past the 1980s, and by 2006 less than 10 percent of the original forest (pre-1970s) remained. The golden monkey populations in both locations almost certainly declined in that period as well.

In this dissertation, I examined how habitat loss, both historic and recent, has affected guenon monkeys. I did this by first exploring how habitat change across four biogeographic periods affected genetic diversity in seven guenon species. Then, I examined how the recent and rapid habitat loss in Rwanda affected the genetic diversity and parasite infection in the two extant golden monkey populations.

In Chapter 1, I assessed the demographic history of seven guenon species with the pairwise sequential Markovian coalescence, using one high-quality genome per species. I then used MaxENT methods to model historic changes in habitat suitability for each species across four biogeographic periods. Finally, I compared the changes in effective population size (Ne) to variation in habitat suitability, and among species. I found that species that retained more suitable habitat across biogeographic periods showed declines in Ne that were less drastic than those of species that experienced a large reduction in suitable habitat. Additionally, species that occupied a geographically wider range like Chlorocebus sabaeus and Cercopithecus neglectus had more suitable habitat within each period than less widespread species and consequently also did not experience the same large declines in Ne.

To explore the effects of recent habitat loss on genetic diversity, in Chapter 2 I report research based on fecal DNA from seven golden monkey groups in VNP and Gishwati Forest. I sequenced targeted, putatively neutral regions and extracted single nucleotide polymorphisms with which I conducted several tests of genetic diversity, a test of genetic structure within the sample pool, and modeled golden monkey demographic history in fastsimcoal2 using the site frequency spectrum. The results of these tests (FST = 0.056; He = 0.248 ) indicate moderate levels of genetic diversity in both VNP and Gishwati populations. However, individual levels of genetic differentiation indicated historic population decline (mean FIS = -0.29), which was supported by heterozygosity excess tests. Results of the population structure analysis indicated the existence of two genetic clusters. One cluster was shared between VNP and Gishwati, while the other was found only in Gishwati monkeys. Additionally, the best fit demographic model showed that the populations split approximately fifteen generations ago, supporting the structure results.

Finally, in Chapter 3, I examined how location (VNP versus Gishwati) and human contact (low vs. high) affected several measures of parasite infection. Using records of parasites identified morphologically from the feces collected for Chapter 2, I calculated prevalence of infection, rate of multiple occurence, and richness. I tested the effect of human contact by quantifying it in two ways: monkeys’ involvement in crop foraging, and by measuring the distance between the sample location and forest edge. I assessed the effect of population or crop foraging and used a linear mixed model to explore if there was an interaction effect between population and human contact (using distance to forest edge). Both populations had the same richness. Overall, the VNP monkeys had higher prevalence of infection and higher rates of multiple infection (Fisher’s exact test: p < 0.001 for both tests) which is likely a result of the higher population density and greater amount of time spent on the forest floor. Groups that crop foraged had a higher prevalence of Capillaria infection (p < 0.001), likely because the crops they consume are often fertilized with manure. When I used distance to forest edge as a proxy for human contact, samples in Gishwati Forest found closer to the forest edge were more likely to be infected; furthermore, in both forests, samples collected nearer the edge were more likely to be infected with Capillaria. These results suggest that population density along with forest edge permeability and human presence outside the forest (in the form of agricultural activity) increase infection risk in golden monkeys.

This dissertation confirms that both long-term and immediate effects of habitat loss are evident in guenons, adding to the growing literature regarding how habitat loss affects wildlife populations. Not only did habitat loss lead to decreases in population size across guenons, but habitat change in Rwanda affected parasite infection in the golden monkeys. Golden monkeys seem to be at low risk of negative consequences from current levels of parasite infection or inbreeding. Future research should build on these results by 1) sequencing additional golden monkey DNA, ideally including individuals from groups in Uganda and the Democratic Republic of Congo, 2) sequencing a golden monkey reference genome, and 3) conducting a genetic study of all golden monkey parasites.