Assessment of in situ nest decay rate for chimpanzees (Pan troglodytes ellioti Matschie, 1914) in Mbam-Djerem National Park, Cameroon: implications for long-term monitoring.

Accurate assessment of great ape populations is a prerequisite for conservation planning. Indirect survey methods using nest and dung, and a set of conversion parameters related to nest decay rates, are increasingly used. Most surveys use the standing crop nest count (SCNC) method, whereby nests are counted along transects and the estimated nest density is converted into chimpanzee density using an often non-local nest decay rate. The use of non-local decay rate is thought to introduce substantial bias to ape population estimates given that nest decay rates vary with location, season, rainfall, nest shape, and tree species used. SCNC method has previously been applied in Mbam-Djerem National Park (MDNP) in Cameroon, for chimpanzee surveys using a non-local nest decay rate. This current study aimed to measure a local nest decay rate for MDNP and implications for chimpanzee population estimates in the MDNP. The mean nest decay rate estimated using a logistic regression analysis was 127 [95% CI (100-160)] days. Moreover, the results suggested that rainfall strongly influenced the nest decay rate over the early stage of the lifetime of the nests. The study confirms that estimates of chimpanzee density and abundance using non-local decay rates should be treated with caution. Our research emphasized the importance of using local nest decay rates and other survey methods which do not depend on decay rates to obtain more accurate estimates of chimpanzee densities in order to inform conservation strategies of these great apes in MDNP.

Habitat differentiation among three Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) populations.

Ecological niche models (ENMs) are often used to predict species distribution patterns from datasets that describe abiotic and biotic factors at coarse spatial scales. Ground-truthing ENMs provide important information about how these factors relate to species-specific requirements at a scale that is biologically relevant for the species. Chimpanzees are territorial and have a predominantly frugivorous diet. The spatial and temporal variation in fruit availability for different chimpanzee populations is thus crucial, but rarely depicted in ENMs. The genetic and geographic distinction within Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) populations represents a unique opportunity to understand fine scale species-relevant ecological variation in relation to ENMs. In Cameroon, P. t. ellioti is composed of two genetically distinct populations that occupy different niches: rainforests in western Cameroon and forest-woodland-savanna mosaic (ecotone) in central Cameroon. We investigated habitat variation at three representative sites using chimpanzee-relevant environmental variables, including fruit availability, to assess how these variables distinguish these niches from one another. Contrary to the assumption of most ENM studies that intact forest is essential for the survival of chimpanzees, we hypothesized that the ecotone and human-modified habitats in Cameroon have sufficient resources to sustain large chimpanzee populations. Rainfall, and the diversity, density, and size of trees were higher at the rainforest. The ecotone had a higher density of terrestrial herbs and lianas. Fruit availability was higher at Ganga (ecotone) than at Bekob and Njuma. Seasonal variation in fruit availability was highest at Ganga, and periods of fruit scarcity were longer than at the rainforest sites. Introduced and secondary forest species linked with anthropogenic modification were common at Bekob, which reduced seasonality in fruit availability. Our findings highlight the value of incorporating fine scale species-relevant ecological data to create more realistic models, which have implications for local conservation planning efforts.

The relationship between the abundance of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) and its habitat: a conservation concern in Mbam-Djerem National Park, Cameroon.

BACKGROUND: Understanding the relationship between great apes and their habitat is essential for the development of successful conservation strategies. The chimpanzee Pan troglodytes ellioti is endemic to Nigeria and Cameroon, and occupies an ecologically diverse range of habitats from forests to forest-savannah mosaic in Mbam-Djerem National Park (MDNP) in Cameroon. The habitat variation in chimpanzees is poorly understood in MDNP which provides an excellent opportunity to assess ecological factors that shape the abundance and distribution patterns of P. t. ellioti over a small geographic scale. RESULTS: We counted 249 nests along 132 km of transects in total. Of these, 119 nests along 68 km occurred in dense forest and 130 nests along 64 km in forest-savannah mosaic. Chimpanzee density was 0.88 [95% CI (0.55-1.41)] individuals/km2 in the dense forest and 0.59 [95% CI (0.19-1.76)] in the forest-savannah mosaic. Nest abundance varied with vegetation type and was higher in areas with dense canopy cover, steeper slopes and relatively higher altitudes. CONCLUSIONS: Our estimates of chimpanzee densities were lower than reported in other studied populations in the range of the Nigeria-Cameroon chimpanzee. However, we found that habitat features, slope and altitude likely play a role in shaping patterns of chimpanzee nesting ecology. Further studies need to be focused on nest decay rates and phenology of useful plants in order to model chimpanzee abundance and distribution in Mbam-Djerem National Park.

Climate warming causes declines in crop yields and lowers school attendance rates in Central Africa.

Although a number of recent studies suggest that climate associated shifts in agriculture are affecting social and economic systems, there have been relatively few studies of these effects in Africa. Such studies would be particularly useful in Central Africa, where the impacts of climate warming are predicted to be high but coincide with an area with low adaptive capacity. Focusing on plantain (Musa paradisiaca), we assess whether recent climate change has led to reduced yields. Analysis of annual temperature between 1950 and 2013 indicated a 0.8°C temperature increase over this 63-year period - a trend that is also observed in monthly temperatures in the last twenty years. From 1991 to 2011, there was a 43% decrease in plantain productivity in Central Africa, which was explained by shifts in temperature (R2=0.68). This decline may have reduced rural household wealth and decreased parental investment in education. Over the past two decades, there was a six month decrease in the duration of school attendance, and the decline was tightly linked to plantain yield (R2=0.82). By 2080, mean annual temperature is expected to increase at least 2°C in Central Africa, and our models predict a concomitant decrease of 39% in plantain yields and 51% in education outcomes, relative to the 1991 baseline. These predictions should be seen as a call-to-action for policy interventions such as farmer training programs to enhance the adaptive capacity of food production systems to mitigate impacts on rural income and education.

Conservation strategies for understanding and combating the primate bushmeat trade on Bioko Island, Equatorial Guinea.

Bioko Island, Equatorial Guinea is among the important places in Africa for the conservation of primates, but a cultural preference for bushmeat and a lack of effective law enforcement has encouraged commercial bushmeat hunting, threatening the survival of the remaining primate population. For over 13 years, we collected bushmeat market data in the Malabo market, recording over 35,000 primate carcasses, documenting "mardi gras" consumption patterns, seasonal carcass availability, and negative effects resulting from government intervention. We also conducted forest surveys throughout Bioko's two protected areas in order to localize and quantify primate populations and hunting pressure. Using these data, we were able to document the significant negative impact bushmeat hunting had on monkey populations, estimate which species are most vulnerable to hunting, and develop ecological niche models to approximate the distribution of each of Bioko's diurnal primate species. These results also have allowed for the identification of primate hotspots, such as the critically important southwest region of the Gran Caldera Scientific Reserve, and thus, priority areas for conservation on Bioko, leading to more comprehensive conservation recommendations. Current and future efforts now focus on bridging the gap between investigators and legislators in order to develop and effectively implement a management plan for Bioko's Gran Caldera Scientific Reserve and to develop a targeted educational campaign to reduce demand by changing consumer attitudes toward bushmeat. Using this multidisciplinary approach, informed by biological, socioeconomic, and cultural research, there may yet be a positive future for the primates of Bioko.

Why Are Nigeria-Cameroon Chimpanzees (Pan troglodytes ellioti) Free of SIVcpz Infection?

Simian immunodeficiency virus (SIV) naturally infects two subspecies of chimpanzee: Pan troglodytes troglodytes from Central Africa (SIVcpzPtt) and P. t. schweinfurtii from East Africa (SIVcpzPts), but is absent in P. t. verus from West Africa and appears to be absent in P. t. ellioti inhabiting Nigeria and western Cameroon. One explanation for this pattern is that P. t. troglodytes and P. t schweinfurthii may have acquired SIVcpz after their divergence from P. t. verus and P. t. ellioti. However, all of the subspecies, except P. t. verus, still occasionally exchange migrants making the absence of SIVcpz in P. t. ellioti puzzling. Sampling of P. t. ellioti has been minimal to date, particularly along the banks of the Sanaga River, where its range abuts that of P. t. troglodytes. This study had three objectives. First, we extended the sampling of SIVcpz across the range of chimpanzees north of the Sanaga River to address whether under-sampling might account for the absence of evidence for SIVcpz infection in P. t. ellioti. Second, we investigated how environmental variation is associated with the spread and prevalence of SIVcpz in the two chimpanzee subspecies inhabiting Cameroon since environmental variation has been shown to contribute to their divergence from one another. Finally, we compared the prevalence and distribution of SIVcpz with that of Simian Foamy Virus (SFV) to examine the role of ecology and behavior in shaping the distribution of diseases in wild host populations. The dataset includes previously published results on SIVcpz infection and SFVcpz as well as newly collected data, and represents over 1000 chimpanzee fecal samples from 41 locations across Cameroon. Results revealed that none of the 181 P. t. ellioti fecal samples collected across the range of P. t. ellioti tested positive for SIVcpz. In addition, species distribution models suggest that environmental variation contributes to differences in the distribution and prevalence of SIVcpz and SFVcpz. The ecological niches of these two viruses are largely non-overlapping, although stronger statistical support for this conclusion will require more sampling. Overall this study demonstrates that SIVcpz infection is absent or very rare in P. t. ellioti, despite multiple opportunities for transmission. The reasons for its absence remain unclear, but might be explained by one or more factors, including environmental variation, viral competition, and/or local adaptation-all of which should be explored in greater detail through continued surveillance of this region.

Long-Term Urban Market Dynamics Reveal Increased Bushmeat Carcass Volume despite Economic Growth and Proactive Environmental Legislation on Bioko Island, Equatorial Guinea.

Bushmeat hunting is extensive in west and central Africa as both a means for subsistence and for commercial gain. Commercial hunting represents one of the primary threats to wildlife in the region, and confounding factors have made it challenging to examine how external factors influence the commercial bushmeat trade. Bioko Island, Equatorial Guinea is a small island with large tracts of intact forest that support sizeable populations of commercially valuable vertebrates, especially endemic primates. The island also has a low human population and has experienced dramatic economic growth and rapid development since the mid-1990's. From October 1997 - September 2010, we monitored the largest bushmeat market on Bioko in Malabo, recording over 197,000 carcasses for sale. We used these data to analyze the dynamics of the market in relation to political events, environmental legislation, and rapid economic growth. Our findings suggest that bushmeat hunting and availability increased in parallel with the growth of Equatorial Guinea's GDP and disposable income of its citizens. During this 13-year study, the predominant mode of capture shifted from trapping to shotguns. Consequently, carcass volume and rates of taxa typically captured with shotguns increased significantly, most notably including intensified hunting of Bioko's unique and endangered monkey fauna. Attempts to limit bushmeat sales, including a 2007 ban on primate hunting and trade, were only transiently effective. The hunting ban was not enforced, and was quickly followed by a marked increase in bushmeat hunting compared to hunting rates prior to the ban. Our results emphasize the negative impact that rapid development and unenforced legislation have had on Bioko's wildlife, and demonstrate the need for strong governmental support if conservation strategies are to be successful at preventing extinctions of tropical wildlife.

Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot.

BACKGROUND: The mechanisms that underlie the diversification of tropical animals remain poorly understood, but new approaches that combine geo-spatial modeling with spatially explicit genetic data are providing fresh insights on this topic. Data about the diversification of tropical mammals remain particularly sparse, and vanishingly few opportunities exist to study endangered large mammals that increasingly exist only in isolated pockets. The chimpanzees of Cameroon represent a unique opportunity to examine the mechanisms that promote genetic differentiation in tropical mammals because the region is home to two chimpanzee subspecies: Pan troglodytes ellioti and P. t. trogolodytes. Their ranges converge in central Cameroon, which is a geographically, climatically and environmentally complex region that presents an unparalleled opportunity to examine the roles of rivers and/or environmental variation in influencing the evolution of chimpanzee populations. RESULTS: We analyzed microsatellite genotypes and mtDNA HVRI sequencing data from wild chimpanzees sampled at a fine geographic scale across Cameroon and eastern Nigeria using a spatially explicit approach based upon Generalized Dissimilarity Modeling. Both the Sanaga River and environmental variation were found to contribute to driving separation of the subspecies. The importance of environmental variation differed among subspecies. Gene-environment associations were weak in P. t. troglodytes, whereas environmental variation was found to play a much larger role in shaping patterns of genetic differentiation in P. t. ellioti. CONCLUSIONS: We found that both the Sanaga River and environmental variation likely play a role in shaping patterns of chimpanzee genetic diversity. Future studies using single nucleotide polymorphism (SNP) data are necessary to further understand how rivers and environmental variation contribute to shaping patterns of genetic variation in chimpanzees.

Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change.

BACKGROUND: The Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) is found in the Gulf of Guinea biodiversity hotspot located in western equatorial Africa. This subspecies is threatened by habitat fragmentation due to logging and agricultural development, hunting for the bushmeat trade, and possibly climate change. Although P. t. ellioti appears to be geographically separated from the neighboring central chimpanzee (P. t. troglodytes) by the Sanaga River, recent population genetics studies of chimpanzees from across this region suggest that additional factors may also be important in their separation. The main aims of this study were: 1) to model the distribution of suitable habitat for P. t. ellioti across Cameroon and Nigeria, and P. t. troglodytes in southern Cameroon, 2) to determine which environmental factors best predict their optimal habitats, and 3) to compare modeled niches and test for their levels of divergence from one another. A final aim of this study was to examine the ways that climate change might impact suitable chimpanzee habitat across the region under various scenarios. RESULTS: Ecological niche models (ENMs) were created using the software package Maxent for the three populations of chimpanzees that have been inferred to exist in Cameroon and eastern Nigeria: (i) P. t. troglodytes in southern Cameroon, (ii) P. t. ellioti in northwestern Cameroon, and (iii) P. t. ellioti in central Cameroon. ENMs for each population were compared using the niche comparison test in ENMtools, which revealed complete niche divergence with very little geographic overlap of suitable habitat between populations. CONCLUSIONS: These findings suggest that a positive relationship may exist between environmental variation and the partitioning of genetic variation found in chimpanzees across this region. ENMs for each population were also projected under three different climate change scenarios for years 2020, 2050, and 2080. Suitable habitat of P. t. ellioti in northwest Cameroon / eastern Nigeria is expected to remain largely unchanged through 2080 in all considered scenarios. In contrast, P. t. ellioti in central Cameroon, which represents half of the population of this subspecies, is expected to experience drastic reductions in its ecotone habitat over the coming century.

The population genetics of wild chimpanzees in Cameroon and Nigeria suggests a positive role for selection in the evolution of chimpanzee subspecies.

BACKGROUND: Chimpanzees (Pan troglodytes) can be divided into four subspecies. Substantial phylogenetic evidence suggests that these subspecies can be grouped into two distinct lineages: a western African group that includes P. t. verus and P. t. ellioti and a central/eastern African group that includes P. t. troglodytes and P. t. schweinfurthii. The geographic division of these two lineages occurs in Cameroon, where the rages of P. t. ellioti and P. t. troglodytes appear to converge at the Sanaga River. Remarkably, few population genetic studies have included wild chimpanzees from this region. RESULTS: We analyzed microsatellite genotypes of 187 wild, unrelated chimpanzees, and mitochondrial control region sequencing data from 604 chimpanzees. We found that chimpanzees in Cameroon and eastern Nigeria comprise at least two, and likely three populations. Both the mtDNA and microsatellite data suggest that there is a primary separation of P. t. troglodytes in southern Cameroon from P. t. ellioti north and west of the Sanaga River. These two populations split ~200-250 thousand years ago (kya), but have exchanged one migrant per generation since separating. In addition, P. t. ellioti consists of two populations that split from one another ~4 kya. One population is located in the rainforests of western Cameroon and eastern Nigeria, whereas the second population appears to be confined to a savannah-woodland mosaic in central Cameroon. CONCLUSIONS: Our findings suggest that there are as many as three genetically distinct populations of chimpanzees in Cameroon and eastern Nigeria. P. t. troglodytes in southern Cameroon comprises one population that is separated from two populations of P. t. ellioti in western and central Cameroon, respectively. P. t. ellioti and P. t. troglodytes appear to be characterized by a pattern of isolation-with-migration, and thus, we propose that neutral processes alone can not explain the differentiation of P. t. ellioti and P. t. troglodytes.

Sequence diversity of Pan troglodytes subspecies and the impact of WFDC6 selective constraints in reproductive immunity.

Recent efforts have attempted to describe the population structure of common chimpanzee, focusing on four subspecies: Pan troglodytes verus, P. t. ellioti, P. t. troglodytes, and P. t. schweinfurthii. However, few studies have pursued the effects of natural selection in shaping their response to pathogens and reproduction. Whey acidic protein (WAP) four-disulfide core domain (WFDC) genes and neighboring semenogelin (SEMG) genes encode proteins with combined roles in immunity and fertility. They display a strikingly high rate of amino acid replacement (dN/dS), indicative of adaptive pressures during primate evolution. In human populations, three signals of selection at the WFDC locus were described, possibly influencing the proteolytic profile and antimicrobial activities of the male reproductive tract. To evaluate the patterns of genomic variation and selection at the WFDC locus in chimpanzees, we sequenced 17 WFDC genes and 47 autosomal pseudogenes in 68 chimpanzees (15 P. t. troglodytes, 22 P. t. verus, and 31 P. t. ellioti). We found a clear differentiation of P. t. verus and estimated the divergence of P. t. troglodytes and P. t. ellioti subspecies in 0.173 Myr; further, at the WFDC locus we identified a signature of strong selective constraints common to the three subspecies in WFDC6-a recent paralog of the epididymal protease inhibitor EPPIN. Overall, chimpanzees and humans do not display similar footprints of selection across the WFDC locus, possibly due to different selective pressures between the two species related to immune response and reproductive biology.

Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations.

The history of the genus Pan is a topic of enduring interest. Chimpanzees (Pan troglodytes) are often divided into subspecies, but the population structure and genetic history of chimpanzees across Africa remain unclear. Some population genetics studies have led to speculation that, until recently, this species constituted a single population with ongoing gene flow across its range, which resulted in a continuous gradient of allele frequencies. Chimpanzees, designated here as P. t. ellioti, occupy the Gulf of Guinea region that spans southern Nigeria and western Cameroon at the center of the distribution of this species. Remarkably, few studies have included individuals from this region, hindering the examination of chimpanzee population structure across Africa. Here, we analyzed microsatellite genotypes of 94 chimpanzees, including 32 designated as P. t. ellioti. We find that chimpanzees fall into three major populations: (i) Upper Guinea in western Africa (P. t. verus); (ii) the Gulf of Guinea region (P. t. ellioti); and (iii) equatorial Africa (P. t. troglodytes and P. t. schweinfurthii). Importantly, the Gulf of Guinea population is significantly different genetically from the others, sharing a last common ancestor with the populations in Upper Guinea ~0.46 million years ago (mya) and equatorial Africa ~0.32 mya. Equatorial chimpanzees are subdivided into up to three populations occupying southern Cameroon, central Africa, and eastern Africa, which may have constituted a single population until ~0.10-0.11 mya. Finally, occasional hybridization may be occurring between the Gulf of Guinea and southern Cameroon populations.

History of click-speaking populations of Africa inferred from mtDNA and Y chromosome genetic variation.

Little is known about the history of click-speaking populations in Africa. Prior genetic studies revealed that the click-speaking Hadza of eastern Africa are as distantly related to click speakers of southern Africa as are most other African populations. The Sandawe, who currently live within 150 km of the Hadza, are the only other population in eastern Africa whose language has been classified as part of the Khoisan language family. Linguists disagree on whether there is any detectable relationship between the Hadza and Sandawe click languages. We characterized both mtDNA and Y chromosome variation of the Sandawe, Hadza, and neighboring Tanzanian populations. New genetic data show that the Sandawe and southern African click speakers share rare mtDNA and Y chromosome haplogroups; however, common ancestry of the 2 populations dates back >35,000 years. These data also indicate that common ancestry of the Hadza and Sandawe populations dates back >15,000 years. These findings suggest that at the time of the spread of agriculture and pastoralism, the click-speaking populations were already isolated from one another and are consistent with relatively deep linguistic divergence among the respective click languages.

Whole-mtDNA genome sequence analysis of ancient African lineages.

Studies of human mitochondrial (mt) DNA genomes demonstrate that the root of the human phylogenetic tree occurs in Africa. Although 2 mtDNA lineages with an African origin (haplogroups M and N) were the progenitors of all non-African haplogroups, macrohaplogroup L (including haplogroups L0-L6) is limited to sub-Saharan Africa. Several L haplogroup lineages occur most frequently in eastern Africa (e.g., L0a, L0f, L5, and L3g), but some are specific to certain ethnic groups, such as haplogroup lineages L0d and L0k that previously have been found nearly exclusively among southern African "click" speakers. Few studies have included multiple mtDNA genome samples belonging to haplogroups that occur in eastern and southern Africa but are rare or absent elsewhere. This lack of sampling in eastern Africa makes it difficult to infer relationships among mtDNA haplogroups or to examine events that occurred early in human history. We sequenced 62 complete mtDNA genomes of ethnically diverse Tanzanians, southern African Khoisan speakers, and Bakola Pygmies and compared them with a global pool of 226 mtDNA genomes. From these, we infer phylogenetic relationships amongst mtDNA haplogroups and estimate the time to most recent common ancestor (TMRCA) for haplogroup lineages. These data suggest that Tanzanians have high genetic diversity and possess ancient mtDNA haplogroups, some of which are either rare (L0d and L5) or absent (L0f) in other regions of Africa. We propose that a large and diverse human population has persisted in eastern Africa and that eastern Africa may have been an ancient source of dispersion of modern humans both within and outside of Africa.