Elsevier

Biological Conservation

Volume 194, February 2016, Pages 194-208
Biological Conservation

Genetic consequences of human forest exploitation in two colobus monkeys in Guinea Bissau

https://doi.org/10.1016/j.biocon.2015.12.019Get rights and content

Highlights

  • We compared the genetic patterns of two colobus monkeys in a human-impacted landscape.

  • We found fine-scale spatial genetic substructure for red colobus females.

  • We found strong bottleneck and low effective population sizes for both primates.

  • Bottlenecks were a consequence of human forest exploitation during the last centuries.

  • Genetic data indicates that red colobus is more sensitive to habitat disturbances.

Abstract

The ability of forest-dwelling species to adapt to changes in their habitat is being increasingly challenged by the rapid pace of human-induced forest degradation. Understanding the effect of such environmental changes on biodiversity requires comparative analyses across species living within the same habitats. We investigated the effect of forest exploitation on the genetic structure and demography of two sympatric arboreal primates showing differences in their socioecology: the Western black-and-white colobus (Colobus polykomos) and Temminck's red colobus (Procolobus badius temminckii). We conducted the study in a fragmented and human-impacted forest in Guinea Bissau. Using microsatellite data from six C. polykomos and eight P. b. temminckii social groups, we found that in C. polykomos the distribution of genetic diversity followed an isolation-by-distance pattern whereas for P. b. temminckii, the results suggested restriction in female dispersal. We detected a strong, recent bottleneck for both primates, which we inferred to have resulted from the anthropogenic exploitation of forest resources in the last centuries. The bottleneck signal was stronger for P. b. temminckii as a likely consequence of its larger estimated ancestral population size. Finally, we discussed the different analytical approaches used. Our results confirm that P. b. temminckii is more affected by habitat changes than C. polykomos, despite being phylogenetically close. Nonetheless, the low estimated effective population sizes and the known demographic changes indicate that both species are severely threatened by human forest exploitation, requiring urgent conservation action.

Introduction

Habitat loss and fragmentation are among the main current threats to biodiversity. Although natural processes can cause population fragmentation and affect population structure, expansion of human land use is occurring at such a pace that most natural populations are likely to be negatively affected (Craul et al., 2009, Epps et al., 2005, Fahrig, 2003, Gerlach and Musolf, 2000, Goossens et al., 2006). Besides reducing the total area of suitable habitat, the negative effects of landscape modification include habitat fragmentation, a process that divides populations into smaller, isolated units (Frankham et al., 2002, Frankham, 2006). As a result, a decrease of gene flow and genetic diversity is expected, reducing the evolutionary potential of the population or species and increasing its risk of extinction (e.g. Frankham et al., 2002, Johansson et al., 2007, Keller and Waller, 2002). Genetic data can provide insights into the past and current challenges faced by fragmented wild populations (Chikhi and Bruford, 2005, Dixon et al., 2007, Goossens et al., 2005, Mona et al., 2014, Quéméré et al., 2010, Zhu et al., 2010), and studying the spatial distribution of genetic variation potentially allows the identification of habitat discontinuities responsible for the disruptions of demographic structure (Chikhi and Bruford, 2005, Manel et al., 2003). Inferring demographic history also allows us to identify major factors (e.g. climatic, ecological, anthropogenic) that have impacted the population in the past and that are likely to influence its distribution in the future (Goossens et al., 2005, Olivieri et al., 2008, Quéméré et al., 2012, Sharma et al., 2012).

The extent to which habitat loss and fragmentation affect a species is highly dependent on its ability to disperse, the degree of habitat fragmentation and the matrix of unsuitable habitat between patches (Frankham et al., 2002, Frankham, 2006). Species that are capable of maintaining dispersal despite habitat fragmentation will be the least affected (Debinski and Holt, 2000, Kareiva, 1987, Villard, 2002). On the other hand, less mobile species or those highly dependent on habitat fragments are more likely to experience isolation (e.g. Goossens et al., 2006, Liu et al., 2009). Indeed, where biodiversity is concerned, fragmentation is not a simple property of the habitat but rather the result of complex interactions between changes in the habitat and the ability of species to cope with these changes. Comparative analyses across species living in the same habitats are thus necessary. African colobines are expected to be susceptible to habitat fragmentation since they are forest-dependent species. Moreover, and especially in West African forests, they are declining due to the loss of tropical rainforest, disease outbreaks and ongoing hunting (Minhós et al., 2013a, Oates et al., 2008a, Oates et al., 2008b, Struhsaker, 2005). It is true that major population declines, due to habitat loss and human activities, are affecting many West African species, which are under more intense threats when compared to species in other sub-Saharan countries (Brashares et al., 2001). For instance, the decline of large mammal populations is higher in West African protected areas than in protected areas from other African regions (Craigie et al., 2010). The great conservation challenges faced by West African species are most likely a consequence of various causes acting at various scales, including the lack of financial and personnel resources in protected areas combined with intense hunting for bushmeat consumption (Brashares et al., 2004) and habitat destruction. For example, the West African red colobus, Procolobus badius waldroni, was the first primate to be declared extinct in the 20th century (Oates et al., 2000). These authors claimed that colobus monkeys have been neglected in terms of conservation actions and stressed the urgency for conservation policies that protect the red colobus, otherwise extinction may extend to other subspecies of this primate as well.

The western black-and-white colobus (Colobus polykomos) and Temmink's red colobus (Procolobus badius temminckii) are the westernmost taxa within the African colobus monkeys. They share many ecological requirements having predominantly arboreal lifestyles within tropical woodlands and are often found in sympatry (Oates et al., 1994). However, they have contrasting social systems and differ in their socioecology, which make them interesting models to test the ability of arboreal species to adapt to habitat degradation. C. polykomos live in relatively small groups with either males or both sexes dispersing (Korstjens et al., 2002, Minhós et al., 2013b, Oates et al., 1994) and P. b. temminckii live in much larger groups with female-biased dispersal (Starin, 1994, Minhós et al., 2013b). A survey of the eastern black-and-white and red colobus (Colobus guereza and Procolobus pennantii ssp., respectively) in a highly fragmented habitat in Uganda revealed that red colobus were more sensitive to habitat fragmentation, as they were absent from most forest patches (Onderdonk and Chapman, 2000). The ability of black-and-white colobus to adapt their diet, home range and group size to shrinking forest patches was highlighted as a possible explanation for their higher resilience to such degraded forests. Similar flexibility has also been described for the same species in Ethiopia (Dunbar, 1987) and Kibale (Uganda; Struhsaker, 1997). In Guinea Bissau, C. polykomos and P. b. temminckii group home ranges often overlap (Gippoliti and Dell'Omo, 1996, Gippoliti and Dell'Omo, 2003). Both species are reported to have patchy but broad distributions in the country (Gippoliti and Dell'Omo, 2003), but the most recent census indicates that they are disappearing from most areas (Casanova and Sousa, 2007). Cantanhez National Park (CNP) in South-West Guinea Bissau is one of the last areas in the country where tropical forest—although highly fragmented—still persists and is home to the largest populations of these primates (Fig. 1; IBAP, 2007). Nevertheless, forests are being reduced at a rapid rate as a result of human activities and both primates are hunted for meat consumption and commerce (Costa et al., 2013a, Costa et al., 2013b, Hockings and Sousa, 2013, Minhós et al., 2013a).

Here, we tested the hypothesis that forest exploitation (e.g. forest fragmentation, habitat degradation, poaching) has a major negative impact on the persistence of these forest-dwelling primates. As arboreal species, we expected both primates to be affected by forest fragmentation and habitat degradation in Cantanhez. However, we predicted that P. b temminckii is more heavily affected due to female dispersal at shorter distances and its lager social groups when compared with C. polykomos. Hence, we investigated the demographic history and the interaction between genetic structure and habitat degradation in CNP for these two sympatric species, using non-invasive molecular techniques. First, we analysed population genetic structure and relatedness patterns at a fine spatial scale to infer discontinuities in dispersal. Second, we inferred and dated changes in effective population size. Finaly, we provide a brief but comprehensive discussion on the advantages and limitations of three different and complimentary methods that we have applied to investigate the demographic history of these species. This comparative study provides new data regarding the interaction between socioecology and a species' capacity to stably persist under anthropogenic habitat disturbance, while also informing upon the conservation priorities that are critical for these threatened populations.

Section snippets

Study site and social groups

Cantanhez National Park is located on a peninsula (total area: 1067 Km2), in south-western Guinea-Bissau (NE limit: 11°22′58″N, 14°46′12″E; SW limit: 11°2′18″S. 15°15′58″W). The forest is now fragmented into patches (ranging from 47.5 to 2500 ha; Simão, 1997) most of which are connected in some way (Fig. 1). Before being declared a National Park in 2008, Cantanhez forest areas were considered critical for biodiversity conservation in Guinea-Bissau, with some of the fragments being protected from

Faecal samples for genetic analyses

A total of eight C. polykomos and six P. b. temminckii social groups were sampled (Fig. 1). By sampling one social group of each taxon per forest fragment (Fig. 1), we collected 380 faecal samples. After removing the repeated individuals and the low quality DNA samples from the dataset we analysed 52 C. polykomos individuals (11–14 loci, 97.2% complete genotypes, mean quality index (Miquel et al., 2006) of 0.84) and 72 P. b. temminckii individuals (10–13 loci, 96,5% complete genotypes, mean

Absence of genetic structure at the scale of Cantanhez National Park

Overall, we found no strong signal of population structure in the two colobus monkeys in Cantanhez National Park. Both clustering approaches (spatial and non-spatial) were concordant. The only substantially discordant results that we found were obtained when we compared the ‘full’ with the ‘non-related’ datasets, which was particularly evident for P. b. temminckii. When the most related individuals were removed, both approaches agreed in identifying a single genetic cluster. The absence of

Data Accessibility

Microsatellite data deposited into Dryad.

Authors Contributions

T.M., M.W.B., C.S., L.V. and C.C. Research concept and design; T.M., M.F.S. and. Collection and/or assembly of data; T.M., L.C., M.F.S., R.H., M.W.B., Data analysis and interpretation; T.M. and R.H. Statistical analysis; T.M. Writing the article; T.M, L.C., C.S, M.F.S., R.H., C.C. M.W.B.; Critical revision of the article and T.M., L.C., C.S, L.V., M.F.S., R.H., C.C. and M.W.B. Final approval of the article.

Acknowledgements

We are deeply grateful to the Institute of Biodiversity and Protected Areas (IBAP) in Guinea Bissau for providing logistical support during all fieldwork. We thank Forestry and Fauna Department (DGFC) and Action for Development (AD) for field assistance and permits and National Institute for Studies and Research (INEP) and Gabinete de Planificação Costeira for providing us with the land cover maps. We are sincerely thankful to all CNP field guards that helped with the sample collection: Mutaro

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