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Endangered Species in Small Habitat Patches Can Possess High Genetic Diversity: the Case of the Tana River Red Colobus and Mangabey

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Endangered Species in Small Habitat Patches Can Possess High Genetic Diversity: the Case of the Tana River Red Colobus and Mangabey Conserv Genet DOI 10.1007/s10592-010-0065-0 RESEARCH ARTICLE Endangered species in small habitat patches can possess high genetic diversity: the case of the Tana River red colobus and mangabey David N. M. Mbora • Mark A. McPeek Received: 29 April 2009 / Accepted: 8 February 2010 Ó Springer Science+Business Media B.V. 2010 Abstract We used mtDNA sequence data from the Tana variation in both primates was found within forest frag- River red colobus and mangabey to determine how their ments. Although both species showed strong inter-forest population genetic structure was influenced by dispersal patch genetic structure we found no correspondence and habitat fragmentation. The colobus and mangabey are between genetic and geographic distances for the two pri- critically endangered primates endemic to gallery forests in mates. We attributed the high genetic diversity to recent eastern Kenya. The forests are a Pliocene–Pleistocene high effective population size, and high sequence diver- refugium that has recently undergone significant habitat gence and strong genetic structures to long-term habitat loss and fragmentation due to human activities. We changes in the landscape. expected both primates to exhibit low levels of genetic diversity due to elevated genetic drift in their small pop- Keywords MtDNA Á Climate change Á Africa Á ulations, and to show a strong correspondence between Genetic diversity Á Conservation genetic and geographic distance due to disruption of gene flow between forests by habitat fragmentation. Addition- ally, because mangabey females are philopatric, we Introduction expected their mtDNA variation to be homogeneous within forest patches but to be heterogeneous between patches. In The current genetic diversity of any species has been contrast, colobus have a female-biased dispersal and so we influenced by many factors in the past. Past changes in expected their mtDNA variation to be homogeneous within climate are known to be a major influence on the distri- and between forest patches. We found high levels of hap- bution of populations and therefore their genetic structure lotype and nucleotide diversity as well as high levels of (Hewitt 2000). In Africa, climate change caused major sequence divergence between haplotype groups in both shifts in faunal assemblages during a time interval lasting species. The red colobus had significantly higher genetic 5.3 million years during the Pliocene–Pleistocene epochs variation than the mangabey did. Most of the genetic (deMenocal 2004; Bobe and Behrensmeyer 2004). The genetic imprint of these habitat changes is evident in sev- eral mammals in East Africa; buffalo (Heller et al. 2008), D. N. M. Mbora Á M. A. McPeek Department of Biological Sciences, Dartmouth College, elephant (Okello et al. 2008), hippopotamus (Okello et al. Hanover, NH 03755, USA 2005) and baboons (Storz et al. 2002a, b). During that e-mail: [email protected] interval, lower temperatures and increased aridity in East Africa reduced and fragmented tropical forests and left D. N. M. Mbora Tana River Primate National Reserve, P O Box 4, Hola, Kenya them as isolated patches along major rivers and on high elevation (Bobe and Behrensmeyer 2004). These forest D. N. M. Mbora (&) refugia have provided important habitat for forest depen- Department of Biology, Whittier College, PO Box 634, Whittier, dent non-human primates (Fleagle 1999). Thus, the current CA 90608, USA e-mail: [email protected]; [email protected]; population genetic structure of primates endemic to these [email protected] forests should reflect their histories in these refugia. 123 Conserv Genet Furthermore, primates endemic to these forests are now We analyzed the population structures of mtDNA vari- vulnerable to further loss of genetic diversity because of ation (NADH dehydrogenase subunit 4, ND4, gene) of the additional forest reduction and fragmentation caused by Tana River red colobus and mangabey to determine how human activities (Mace and Balmford 2000). they are influenced by the pattern of dispersal and habitat The Tana River forests of southeastern Kenya are an fragmentation. We expected both primates to exhibit low example of forest fragments whose origin dates back to the levels of genetic diversity due to genetic drift in their rel- increasing aridity of the Pliocene–Pleistocene interval in atively small populations, and for populations that were East Africa (Bobe and Behrensmeyer 2004). Botanical geographically close to one another to be more genetically surveys of the Tana River forests suggest that evergreen similar because of greater gene flow (Wright 1978; Kimura forests were once more continuous in Africa (Hamilton and Weiss 1964). Mangabey females are largely philopatric 1981). In particular, 12% of tree species in the Tana are (Kinnaird 1992), while red colobus females disperse on from the Guinea-Congolian region indicating an earlier attaining sexual maturity (Marsh 1979). Thus, we expected period of continuous rain forest across the African continent the mtDNA variation in the mangabey to be relatively (Medley 1992). The forests occupy the lower floodplain of homogeneous within forest patches but to be heterogeneous the Tana River and are of great conservation importance. between forest patches. Conversely, we expected the They are part of the east African coastal forests global mtDNA variation of the red colobus to be relatively biodiversity hotspot (Myers et al. 2000) and support a high homogeneous within and between forest patches due to diversity of rare plant and animal species (Andrews et al. female dispersal in this species (Marsh 1979). 1975). In particular, they provide the only known habitat of two endemic primates: the Tana River red colobus (Pro- colobus rufomitratus) and the Tana mangabey (Cercocebus Materials and methods galeritus). Both species are critically endangered (Hilton- Taylor 2000) and ranked among the IUCN’s top 25 most Study area and species endangered primates (Grubb et al. 2003; Mittermeier et al. 2007). It is estimated that the population of the colobus is The study area comprises approximately 26 km2 of gallery less than 1000 individuals and that of the mangabey does forest occurring in scattered patches of various sizes on not exceed 2000 individuals (Butynski and Mwangi 1994). both sides of the Tana River in eastern Kenya (Fig. 1; In addition to the natural forest fragmentation caused by Mbora and Meikle 2004). This area encompasses the entire the meandering of the river in its old stage, recent human distribution range of the Tana River red colobus and activities have further reduced and fragmented the forests mangabey. These forests exist in an arid environment with causing precipitous declines in the primate populations, and an annual total rainfall of less than 400 mm. Forest is extinctions in several of the fragments (Mbora and Meikle created and maintained by groundwater, and by periodic 2004). Thus, these forests offer a natural setting to study the flooding of the river (Hughes 1990). The depth of the water effects of forest loss and fragmentation on population table drops off rapidly from the edge of the river and limits genetic structure of endemic, endangered forest primates. the lateral extent of the forests to about 1 km on either side The population structure seen in mitochondrial DNA (Hughes 1990). The intervening matrix is mainly cultivated can be particularly useful in understanding the effects of land, riparian grassland and dry shrubs. forest loss and fragmentation on population genetic struc- We mapped the gallery forest using aerial photographs ture of forest primates. Mitochondrial DNA is maternally taken in 1994 and 1996, and selected 12 forest patches as inherited (Gyllensten et al. 1985), lacks recombination study sites. We chose forest patches so that approximately (Hayashi et al. 1985) and exhibits rapid sequence evolution equal forest area was sampled east and west of the Tana (Brown et al. 1979). Consequently, any mtDNA lineages River, and inside and outside the Tana River Primate that diverge in populations (e.g. in forest fragments) are National Reserve (TRPNR) to capture the range of habitat independent clones that rapidly accumulate divergent sets conditions within the floodplain (Fig. 1). We surveyed of mutations through time. Thus, in species where females each study forest to determine the number of resident are philopatric, there should exist little or no variation groups of colobus and mangabeys, and identified a subset within, and much variation between populations, e.g. in of groups within each forest for detailed studies of group many macaque species (Macaca spp.; Melnick and Hoelzer size, age and sex composition over time. We systemati- 1992) and vervet monkeys (Cercopithecus aethiops aethi- cally selected social groups that were easy to locate and ops; Shimada 2000). In contrast, female dispersal should to identify using ‘‘marker’’ animals. Since 2001, we have lead to much differentiation within and less differentiation periodically surveyed the forests and monitored all these between populations; e.g. in the hamadryas baboons (Papio study groups (Mbora and Meikle 2004; Mbora, unpub- hamadryas hamadryas; Hapke et al. 2001). lished data). 123 Conserv Genet Fig. 1 Study area indicating the location and distribution of study of the Tana River Primate National Reserve. The Roman numeral forests in southeastern Kenya for the colobus (a) and mangabey (b). codes identify study forests adjacent to them, and the major villages The frame on the top half of the map shows the approximate location are named The Tana colobus and mangabey are of similar body Collection of fecal samples and DNA extraction size but their behavioral ecologies and life history strate- gies are quite different (Kinnaird 1992; Marsh 1979). The In 2004 and 2005, from July to September, we collected red colobus is a specialist frugivore with limited vagility. It fecal samples from study groups of colobus and mangabeys is almost exclusively arboreal and lives in relatively small by following them, on separate days, from 0600 h to social groups that exhibit high site fidelity (Marsh 1981).
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