Publications by authors named "Alex K Piel"

26 Publications

  • Page 1 of 1

Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

mSystems 2021 Jun 22:e0126920. Epub 2021 Jun 22.

Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.
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http://dx.doi.org/10.1128/mSystems.01269-20DOI Listing
June 2021

CD4 receptor diversity represents an ancient protection mechanism against primate lentiviruses.

Proc Natl Acad Sci U S A 2021 Mar;118(13)

Lukuru Wildlife Research Foundation, Tshuapa-Lomami-Lualaba Project, BP 2012, Kinshasa, Democratic Republic of the Congo.

Infection with human and simian immunodeficiency viruses (HIV/SIV) requires binding of the viral envelope glycoprotein (Env) to the host protein CD4 on the surface of immune cells. Although invariant in humans, the Env binding domain of the chimpanzee CD4 is highly polymorphic, with nine coding variants circulating in wild populations. Here, we show that within-species CD4 diversity is not unique to chimpanzees but found in many African primate species. Characterizing the outermost (D1) domain of the CD4 protein in over 500 monkeys and apes, we found polymorphic residues in 24 of 29 primate species, with as many as 11 different coding variants identified within a single species. D1 domain amino acid replacements affected SIV Env-mediated cell entry in a single-round infection assay, restricting infection in a strain- and allele-specific fashion. Several identical CD4 polymorphisms, including the addition of -linked glycosylation sites, were found in primate species from different genera, providing striking examples of parallel evolution. Moreover, seven different guenons ( spp.) shared multiple distinct D1 domain variants, pointing to long-term trans-specific polymorphism. These data indicate that the HIV/SIV Env binding region of the primate CD4 protein is highly variable, both within and between species, and suggest that this diversity has been maintained by balancing selection for millions of years, at least in part to confer protection against primate lentiviruses. Although long-term SIV-infected species have evolved specific mechanisms to avoid disease progression, primate lentiviruses are intrinsically pathogenic and have left their mark on the host genome.
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http://dx.doi.org/10.1073/pnas.2025914118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8020793PMC
March 2021

Fermented food consumption in wild nonhuman primates and its ecological drivers.

Am J Phys Anthropol 2021 Mar 2. Epub 2021 Mar 2.

Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, Japan.

Objectives: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits.

Materials And Methods: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates.

Results: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures.

Discussion: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.
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http://dx.doi.org/10.1002/ajpa.24257DOI Listing
March 2021

Ecological correlates of chimpanzee (Pan troglodytes schweinfurthii) density in Mahale Mountains National Park, Tanzania.

PLoS One 2021 12;16(2):e0246628. Epub 2021 Feb 12.

Department of Anthropology, University College London, London, United Kingdom.

Understanding the ecological factors that drive animal density patterns in time and space is key to devising effective conservation strategies. In Tanzania, most chimpanzees (~75%) live outside national parks where human activities threaten their habitat's integrity and connectivity. Mahale Mountains National Park (MMNP), therefore, is a critical area for chimpanzees (Pan troglodytes schweinfurthii) in the region due to its location and protective status. Yet, despite its importance and long history of chimpanzee research (>50 years), a park-wide census of the species has never been conducted. The park is categorized as a savanna-woodland mosaic, interspersed with riparian forest, wooded grassland, and bamboo thicket. This heterogeneous landscape offers an excellent opportunity to assess the ecological characteristics associated with chimpanzee density, a topic still disputed, which could improve conservation plans that protect crucial chimpanzee habitat outside the park. We examined the influence of fine-scale vegetative characteristics and topographical features on chimpanzee nest density, modeling nest counts using hierarchical distance sampling. We counted 335 nests in forest and woodland habitats across 102 transects in 13 survey sites. Nests were disproportionately found more in or near evergreen forests, on steep slopes, and in feeding tree species. We calculated chimpanzee density in MMNP to be 0.23 ind/km2, although density varied substantially among sites (0.09-3.43 ind/km2). Density was associated with factors related to the availability of food and nesting trees, with topographic heterogeneity and the total basal area of feeding tree species identified as significant positive predictors. Species-rich habitats and floristic diversity likely play a principal role in shaping chimpanzee density within a predominately open landscape with low food abundance. Our results provide valuable baseline data for future monitoring efforts in MMNP and enhance our understanding of this endangered species' density and distribution across Tanzania.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0246628PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7880473PMC
February 2021

Red-tailed monkeys (Cercopithecus ascanius) prey upon and mob birds in the Issa Valley, western Tanzania.

Primates 2020 Jul 12;61(4):563-566. Epub 2020 Jun 12.

Greater Mahale Ecosystem Research and Conservation Project, Box 66, Kigoma, Tanzania.

Interactions between monkeys and birds are rarely observed and, consequently, rarely described in the scientific literature. We recorded two encounters between birds (Prionops plumatus and Strix woodfordii) and red-tailed monkeys (Cercopithecus ascanius) in a woodland-mosaic habitat in western Tanzania. We observed a male red-tailed monkey consume a small bird in its entirety. Although only a few feathers remained, we provisionally identified the bird as a white-crested helmetshrike. We also observed a group of red-tailed monkeys mobbing, but not killing, an African wood owl on the forest floor. This is the first reported observation of this kind. These encounters suggest that guenons may generalize large-bodied avians as threats and small-bodied avians as potential prey. Hetero-specific encounters such as these provide insights into primate diet and anti-predatory behavior.
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http://dx.doi.org/10.1007/s10329-020-00834-1DOI Listing
July 2020

The importance of nutrient hotspots for grazing ungulates in a Miombo ecosystem, Tanzania.

PLoS One 2020 30;15(3):e0230192. Epub 2020 Mar 30.

Department of Sustainable Agriculture, Biodiversity Conservation and Ecosystems Management, The Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania.

While movement patterns of grazing ungulates are strongly dependent on forage quality their use of nutrient hotspots such as termite mounds or grazing lawns has rarely been quantified, especially in savanna ecosystems where soil-nutrient quality is low. Additionally, few experiments have been conducted to determine the role of termite mound- and grazing lawn-derived soils in improving forage quality in the field. We studied wild ungulate grazing activities around ten termite mounds, six grazing lawns and their respective control sites in a Miombo system of Issa Valley, western Tanzania, in the same system. We used indirect observations (i.e., dung, tracks) to identify seasonal and spatial variations in habitat use of various wild mammalian grazers. Grazer visitation rates were nine and three times higher on termite mounds and grazing lawns, respectively, compared to control sites. During the rainy season, termite mounds were more frequently used than grazing lawns while the latter were used more often during the dry season. In an additional pot experiment with soils derived from different areas, we found that Cynodon dactylon in termite mound-derived soils had twice as high Nitrogen and Phosphorous contents and biomass compared to grasses planted in grazing lawn soils and control site soils. We highlight that both termite mounds and grazing lawns play a significant role in influencing seasonal nutrient dynamics, forage nutrient quality, habitat selectivity, and, hence, grazing activities and movement patterns of wild ungulate grazers in savannas. We conclude that termite mounds and grazing lawns are important for habitat heterogeneity in otherwise nutrient-poor savanna systems.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0230192PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7105114PMC
June 2020

Food abundance and weather influence habitat-specific ranging patterns in forest- and savanna mosaic-dwelling red-tailed monkeys (Cercopithecus ascanius).

Am J Phys Anthropol 2019 10 19;170(2):217-231. Epub 2019 Aug 19.

School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, United Kingdom.

Objectives: Primates that live in predominantly forested habitats and open, savanna mosaics should exhibit behavioral responses to differing food distributions and weather. We compared ecological constraints on red-tailed monkey ranging behavior in forest and savanna mosaic environments. Intraspecific variation in adaptations to these conditions may reflect similar pressures faced by hominins during the Plio-Pleistocene.

Methods: We followed six groups in moist evergreen forest at Ngogo (Uganda) and one group in a savanna-woodland mosaic at the Issa Valley (Tanzania). We used spatial analyses to compare home range sizes and daily travel distances (DTD) between sites. We used measures of vegetation density and phenology to interpolate spatially explicit indices of food (fruit, flower, and leaves) abundance. We modeled DTD and range use against food abundance. We modeled DTD and at Issa hourly travel distances (HTD), against temperature and rainfall.

Results: Compared to Issa, monkeys at Ngogo exhibited significantly smaller home ranges and less variation in DTD. DTD related negatively to fruit abundance, which had a stronger effect at Issa. DTD and HTD related negatively to temperature but not rainfall. This effect did not differ significantly between sites. Home range use did not relate to food abundance at either site.

Conclusions: Our results indicate food availability and thermoregulatory constraints influence red-tailed monkey ranging patterns. Intraspecific variation in home range sizes and DTD likely reflects different food distributions in closed and open habitats. We compare our results with hypotheses of evolved hominin behavior associated with the Plio-Pleistocene shift from similar closed to open environments.
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http://dx.doi.org/10.1002/ajpa.23920DOI Listing
October 2019

CD4 receptor diversity in chimpanzees protects against SIV infection.

Proc Natl Acad Sci U S A 2019 02 4;116(8):3229-3238. Epub 2019 Feb 4.

Sanaga-Yong Chimpanzee Rescue Center, In Defense of Animals-Africa, Portland, OR 97204.

Human and simian immunodeficiency viruses (HIV/SIVs) use CD4 as the primary receptor to enter target cells. Here, we show that the chimpanzee CD4 is highly polymorphic, with nine coding variants present in wild populations, and that this diversity interferes with SIV envelope (Env)-CD4 interactions. Testing the replication fitness of SIVcpz strains in CD4 T cells from captive chimpanzees, we found that certain viruses were unable to infect cells from certain hosts. These differences were recapitulated in CD4 transfection assays, which revealed a strong association between CD4 genotypes and SIVcpz infection phenotypes. The most striking differences were observed for three substitutions (Q25R, Q40R, and P68T), with P68T generating a second N-linked glycosylation site (N66) in addition to an invariant N32 encoded by all chimpanzee CD4 alleles. In silico modeling and site-directed mutagenesis identified charged residues at the CD4-Env interface and clashes between CD4- and Env-encoded glycans as mechanisms of inhibition. CD4 polymorphisms also reduced Env-mediated cell entry of monkey SIVs, which was dependent on at least one D1 domain glycan. CD4 allele frequencies varied among wild chimpanzees, with high diversity in all but the western subspecies, which appeared to have undergone a selective sweep. One allele was associated with lower SIVcpz prevalence rates in the wild. These results indicate that substitutions in the D1 domain of the chimpanzee CD4 can prevent SIV cell entry. Although some SIVcpz strains have adapted to utilize these variants, CD4 diversity is maintained, protecting chimpanzees against infection with SIVcpz and other SIVs to which they are exposed.
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http://dx.doi.org/10.1073/pnas.1821197116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6386711PMC
February 2019

Leopard (Panthera pardus) predation on a red-tailed monkey (Cercopithecus ascanius) in the Issa Valley, western Tanzania.

Primates 2019 Jan 17;60(1):15-19. Epub 2018 Nov 17.

School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool, L33AF, UK.

Predation is predicted to be an important selection pressure for primates. Evidence for this hypothesis is rare, however, due to the scarcity of direct observations of primate predation. We describe an observation of leopard (Panthera pardus) predation on a red-tailed monkey (Cercopithecus ascanius schmidti) at the Issa Valley, a savanna-woodland mosaic landscape in western Tanzania. We compare rates of evidence of leopard presence between Issa and other primate study sites in sub-Saharan Africa. An increase in direct observations of leopards at Issa in recent years suggests that leopards may be habituating to researcher presence.
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http://dx.doi.org/10.1007/s10329-018-0700-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6331503PMC
January 2019

PARV4 found in wild chimpanzee faeces: an alternate route of transmission?

Arch Virol 2019 Feb 20;164(2):573-578. Epub 2018 Oct 20.

CEITEC-VFU, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 612 42, Brno, Czech Republic.

Human parvovirus 4 (PARV4, family Parvoviridae, genus Tetraparvovirus) displays puzzling features, such as uncertain clinical importance/significance, unclear routes of transmission, and discontinuous geographical distribution. The origin, or the general reservoir, of human PARV4 infection is unknown. We aimed to detect and characterize PARV4 virus in faecal samples collected from two wild chimpanzee populations and 19 species of captive non-human primates. We aimed to investigate these species as a potential reservoir and alternate route of transmission on the African continent. From almost 500 samples screened, a single wild Pan troglodytes schweinfurthii sample tested positive. Full genome analysis, as well as single ORF phylogenies, confirmed species-specific PARV4 infection.
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http://dx.doi.org/10.1007/s00705-018-4073-6DOI Listing
February 2019

Temporal patterns of chimpanzee loud calls in the Issa Valley, Tanzania: Evidence of nocturnal acoustic behavior in wild chimpanzees.

Authors:
Alex K Piel

Am J Phys Anthropol 2018 07;166(3):530-540

School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, United Kingdom.

Objectives: Much is known about chimpanzee diurnal call patterns, but far less about night-time vocal behavior. I deployed a passive acoustic monitoring (PAM) system to assess 24-hr temporal acoustic activity of wild, unhabituated chimpanzees that live in a woodland mosaic habitat similar to hominin landscapes from the Plio-Pleistocene. A primary aim was to apply findings to our broader understanding to chimpanzee 24-hr activity patterns, and what implications this may have for reconstructing hominin adaptations to similarly hot, dry, and open landscapes. I also tested whether chimpanzees conform to the acoustic adaptation hypothesis, and produce loud calls during periods of optimal sound transmission.

Methods: Nine custom-made solar-powered acoustic transmission units (SPATUs) recorded continuously for 250 days over 11 months in the Issa Valley, western Tanzania. I complemented acoustic data with environmental data from weather stations as well as behavioral data collected on chimpanzee nest group sizes to assess the relationship between party size and calling.

Results: Chimpanzees called at all hours of the day and night in both wet and dry seasons, and night and day calls exhibited parallel rates/month, although twilight calls were produced significantly more in the dry, compared to the wet season. Calls were more likely during warmer temperatures and lower humidity. Call rate was positively associated with (nest) party size and counter-calls exhibited no temporal variation in their origins (similar vs. adjacent valleys).

Conclusions: Chimpanzees were acoustically active throughout the 24-hr cycle, although at low rates compared to diurnal activity, revealing night-time activity in an ape otherwise described as diurnal. Chimpanzee loud calls partially, and weakly, conformed to the acoustic adaptation hypothesis and likely responded to social, rather than environmental factors. Call rates accurately reflect grouping patterns and PAM is demonstrated to be an effective means of remotely assessing activity, especially at times and from places that are difficult to access for researchers.
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http://dx.doi.org/10.1002/ajpa.23609DOI Listing
July 2018

The diet of open-habitat chimpanzees (Pan troglodytes schweinfurthii) in the Issa valley, western Tanzania.

J Hum Evol 2017 11 3;112:57-69. Epub 2017 Oct 3.

School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, United Kingdom; Ugalla Primate Project, Box 108, Uvinza, Tanzania; Department of Archaeology and Anthropology, University of Cambridge, United Kingdom.

Comparative data on the diets of extant primates inform hypotheses about hominin resource use. Historically, data describing chimpanzee diets stem primarily from forest-dwelling communities, and we lack comparative data from chimpanzees that live in mosaic habitats that more closely resemble those reconstructed for Plio-Pleistocene hominins. We present data on the diet of a partially-habituated community of open habitat chimpanzees (Pan troglodytes schweinfurthii) from the Issa valley, western Tanzania, collected over a four-year period. Based mostly on macroscopic faecal analysis, Issa chimpanzees consumed a minimum of 69 plant species. There was no relationship between plant consumption and either fruit availability or feeding tree density; the most frequently consumed plant species were found in riverine forests, with woodland species consumed more frequently during the late dry season. We conclude by contextualising these findings with those of other open-habitat chimpanzee sites, and also by discussing how our results contribute towards reconstructions of early hominin exploitation of mosaic landscapes.
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http://dx.doi.org/10.1016/j.jhevol.2017.08.016DOI Listing
November 2017

Adenovirus infection in savanna chimpanzees (Pan troglodytes schweinfurthii) in the Issa Valley, Tanzania.

Arch Virol 2018 Jan 4;163(1):191-196. Epub 2017 Oct 4.

CEITEC-VFU, University of Veterinary and Pharmaceutical Sciences Brno, Palackého tř. 1946/1, 612 42, Brno, Czech Republic.

Adenoviruses are a widespread cause of diverse human infections with recently confirmed zoonotic roots in African great apes. We focused on savanna-dwelling chimpanzees in the Issa Valley (Tanzania), which differ from those from forested sites in many aspects of behavior and ecology. PCR targeting the DNA polymerase gene detected AdV in 36.7% (69/188) of fecal samples. We detected five groups of strains belonging to the species Human mastadenovirus E and two distinct groups within the species Human mastadenovirus C based on partial hexon sequence. All detected AdVs from the Issa Valley are related to those from nearby Mahale and Gombe National Parks, suggesting chimpanzee movements and pathogen transmission.
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http://dx.doi.org/10.1007/s00705-017-3576-xDOI Listing
January 2018

Raw material procurement for termite fishing tools by wild chimpanzees in the Issa valley, Western Tanzania.

Am J Phys Anthropol 2017 10 16;164(2):292-304. Epub 2017 Jun 16.

RLAHA, School of Archaeology, Leverhulme Trust Early Career Fellow, University of Oxford, Oxford, OX1 3QY, United Kingdom.

Objectives: Chimpanzee termite fishing has been studied for decades, yet the selective processes preceding the manufacture of fishing tools remain largely unexplored. We investigate raw material selection and potential evidence of forward planning in the chimpanzees of Issa valley, western Tanzania.

Materials And Methods: Using traditional archaeological methods, we surveyed the location of plants from where chimpanzees sourced raw material to manufacture termite fishing tools, relative to targeted mounds. We measured raw material abundance to test for availability and selection. Statistics included Chi-Squared, two-tailed Wilcoxon, and Kruskall-Wallace tests.

Results: Issa chimpanzees manufactured extraction tools only from bark, despite availability of other suitable materials (e.g., twigs), and selected particular plant species as raw material sources, which they often also exploit for food. Most plants were sourced 1-16 m away from the mound, with a maximum of 33 m. The line of sight from the targeted mound was obscured for a quarter of these plants.

Discussion: The exclusive use of bark tools despite availability of other suitable materials indicates a possible cultural preference. The fact that Issa chimpanzees select specific plant species and travel some distance to source them suggests some degree of selectivity and, potentially, forward planning. Our results have implications for the reconstruction of early hominin behaviors, particularly with regard to the use of perishable tools, which remain archaeologically invisible.
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http://dx.doi.org/10.1002/ajpa.23269DOI Listing
October 2017

A comparative molecular survey of malaria prevalence among Eastern chimpanzee populations in Issa Valley (Tanzania) and Kalinzu (Uganda).

Malar J 2016 08 19;15(1):423. Epub 2016 Aug 19.

Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences Brno, 612 42, Brno, Czech Republic.

Background: Habitat types can affect vector and pathogen distribution and transmission dynamics. The prevalence and genetic diversity of Plasmodium spp. in two eastern chimpanzee populations-Kalinzu Forest Reserve, Uganda and Issa Valley, Tanzania-inhabiting different habitat types was investigated. As a follow up study the effect of host sex and age on infections patterns in Kalinzu Forest Reserve chimpanzees was determined.

Methods: Molecular methods were employed to detect Plasmodium DNA from faecal samples collected from savanna-woodland (Issa Valley) and forest (Kalinzu Forest Reserve) chimpanzee populations.

Results: Based on a Cytochrome-b PCR assay, 32 out of 160 Kalinzu chimpanzee faecal samples were positive for Plasmodium DNA, whilst no positive sample was detected in 171 Issa Valley chimpanzee faecal samples. Sequence analysis revealed that previously known Laverania species (Plasmodium reichenowi, Plasmodium billbrayi and Plasmodium billcollinsi) are circulating in the Kalinzu chimpanzees. A significantly higher proportion of young individuals were tested positive for infections, and switching of Plasmodium spp. was reported in one individual. Amongst the positive individuals sampled more than once, the success of amplification of Plasmodium DNA from faeces varied over sampling time.

Conclusion: The study showed marked differences in the prevalence of malaria parasites among free ranging chimpanzee populations living in different habitats. In addition, a clear pattern of Plasmodium infections with respect to host age was found. The results presented in this study contribute to understanding the ecological aspects underlying the malaria infections in the wild. Nevertheless, integrative long-term studies on vector abundance, Plasmodium diversity during different seasons between sites would provide more insight on the occurrence, distribution and ecology of these pathogens.
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http://dx.doi.org/10.1186/s12936-016-1476-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992209PMC
August 2016

Passive acoustic monitoring reveals group ranging and territory use: a case study of wild chimpanzees (Pan troglodytes).

Front Zool 2016 8;13:34. Epub 2016 Aug 8.

Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany ; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany.

Background: Assessing the range and territories of wild mammals traditionally requires years of data collection and often involves directly following individuals or using tracking devices. Indirect and non-invasive methods of monitoring wildlife have therefore emerged as attractive alternatives due to their ability to collect data at large spatiotemporal scales using standardized remote sensing technologies. Here, we investigate the use of two novel passive acoustic monitoring (PAM) systems used to capture long-distance sounds produced by the same species, wild chimpanzees (Pan troglodytes), living in two different habitats: forest (Taï, Côte d'Ivoire) and savanna-woodland (Issa valley, Tanzania).

Results: Using data collected independently at two field sites, we show that detections of chimpanzee sounds on autonomous recording devices were predicted by direct and indirect indices of chimpanzee presence. At Taï, the number of chimpanzee buttress drums detected on recording devices was positively influenced by the number of hours chimpanzees were seen ranging within a 1 km radius of a device. We observed a similar but weaker relationship within a 500 m radius. At Issa, the number of indirect chimpanzee observations positively predicted detections of chimpanzee loud calls on a recording device within a 500 m but not a 1 km radius. Moreover, using just seven months of PAM data, we could locate two known chimpanzee communities in Taï and observed monthly spatial variation in the center of activity for each group.

Conclusions: Our work shows PAM is a promising new tool for gathering information about the ranging behavior and habitat use of chimpanzees and can be easily adopted for other large territorial mammals, provided they produce long-distance acoustic signals that can be captured by autonomous recording devices (e.g., lions and wolves). With this study we hope to promote more interdisciplinary research in PAM to help overcome its challenges, particularly in data processing, to improve its wider application.
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http://dx.doi.org/10.1186/s12983-016-0167-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4977853PMC
August 2016

Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii).

Parasitology 2016 05 3;143(6):741-8. Epub 2016 Mar 3.

Biology Centre,Institute of Parasitology,Academy of Sciences of the Czech Republic,Branišovská 31,370 05 České Budějovice,Czech Republic.

To address the molecular diversity and occurrence of pathogenic species of the genus Entamoeba spp. in wild non-human primates (NHP) we conducted molecular-phylogenetic analyses on Entamoeba from wild chimpanzees living in the Issa Valley, Tanzania. We compared the sensitivity of molecular [using a genus-specific polymerase chain reaction (PCR)] and coproscopic detection (merthiolate-iodine-formaldehyde concentration) of Entamoeba spp. We identified Entamoeba spp. in 72 chimpanzee fecal samples (79%) subjected to species-specific PCRs for six Entamoeba species/groups (Entamoeba histolytica, Entamoeba nuttalli, Entamoeba dispar, Entamoeba moshkovskii, Entamoeba coli and Entamoeba polecki ST2). We recorded three Entamoeba species: E. coli (47%), E. dispar (16%), Entamoeba hartmanni (51%). Coproscopically, we could only distinguish the cysts of complex E. histolytica/dispar/moshkovskii/nuttalli and E. coli. Molecular prevalence of entamoebas was higher than the prevalence based on the coproscopic examination. Our molecular phylogenies showed that sequences of E. dispar and E. coli from Issa chimpanzees are closely related to sequences from humans and other NHP from GenBank. The results showed that wild chimpanzees harbour Entamoeba species similar to those occurring in humans; however, no pathogenic species were detected. Molecular-phylogenetic methods are critical to improve diagnostics of entamoebas in wild NHP and for determining an accurate prevalence of Entamoeba species.
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http://dx.doi.org/10.1017/S0031182016000263DOI Listing
May 2016

The ecological determinants of baboon troop movements at local and continental scales.

Mov Ecol 2015 1;3(1):14. Epub 2015 Jul 1.

Department of Biosciences, College of Science, Swansea University, Swansea, UK.

Background: How an animal moves through its environment directly impacts its survival, reproduction, and thus biological fitness. A basic measure describing how an individual (or group) travels through its environment is Day Path Length (DPL), i.e., the distance travelled in a 24-hour period. Here, we investigate the ecological determinants of baboon (Papio spp.) troop DPL and movements at local and continental scales.

Results: At the continental scale we explore the ecological determinants of annual mean DPL for 47 baboon troops across 23 different populations, updating a classic study by Dunbar (Behav Ecol Sociobiol 31: 35-49, 1992). We find that variation in baboon DPLs is predicted by ecological dissimilarity across the genus range. Troops that experience higher average monthly rainfall and anthropogenic influences have significantly shorter DPL, whilst troops that live in areas with higher average annual temperatures have significantly longer DPL. We then explore DPLs and movement characteristics (the speed and distribution of turning angles) for yellow baboons (Papio cynocephalus) at a local scale, in the Issa Valley of western Tanzania. We show that our continental-scale model is a good predictor of DPL in Issa baboons, and that troops move significantly slower, and over shorter distances, on warmer days. We do not find any effect of season or the abundance of fruit resources on the movement characteristics or DPL of Issa baboons, but find that baboons moved less during periods of high fruit availability.

Conclusion: Overall, this study emphasises the ability of baboons to adapt their ranging behaviour to a range of ecological conditions and highlights how investigations of movement patterns at different spatial scales can provide a more thorough understanding of the ecological determinants of movement.
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http://dx.doi.org/10.1186/s40462-015-0040-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4487562PMC
July 2015

Population status of chimpanzees in the Masito-Ugalla Ecosystem, Tanzania.

Am J Primatol 2015 Oct 26;77(10):1027-35. Epub 2015 Jun 26.

Department of Archaeology and Anthropology, University of Cambridge, Cambridge CB2 3QG, United Kingdom.

More than 75 percent of Tanzania's chimpanzees live at low densities on land outside national parks. Chimpanzees are one of the key conservation targets in the region and long-term monitoring of these populations is essential for assessing the overall status of ecosystem health and the success of implemented conservation strategies. We aimed to assess change in chimpanzee density within the Masito-Ugalla Ecosystem (MUE) by comparing results of re-walking the same line transects in 2007 and 2014. We further used published remote sensing data derived from Landsat satellites to assess forest cover change within a 5 km buffer of these transects over that same period. We detected no statistically significant decline in chimpanzee density across the surveyed areas of MUE between 2007 and 2014, although the overall mean density of chimpanzees declined from 0.09 individuals/km(2) in 2007 to 0.05 individuals/km(2) in 2014. Whether this change is biologically meaningful cannot be determined due to small sample sizes and large, entirely overlapping error margins. It is therefore possible that the MUE chimpanzee population has been stable over this period and indeed in some areas (Issa Valley, Mkanga, Kamkulu) even showed an increase in chimpanzee density. Variation in chimpanzee habitat preference for ranging or nesting could explain variation in density at some of the survey sites between 2007 and 2014. We also found a relationship between increasing habitat loss and lower mean chimpanzee density. Future surveys will need to ensure a larger sample size, broader geographic effort, and random survey design, to more precisely determine trends in MUE chimpanzee density and population size over time.
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http://dx.doi.org/10.1002/ajp.22438DOI Listing
October 2015

African origin of the malaria parasite Plasmodium vivax.

Nat Commun 2014 ;5:3346

Division of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK.

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.
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http://dx.doi.org/10.1038/ncomms4346DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4089193PMC
November 2015

Termite fishing by wild chimpanzees: new data from Ugalla, western Tanzania.

Primates 2014 Jan 30;55(1):35-40. Epub 2013 May 30.

Division of Biological Anthropology, University of Cambridge, Pembroke Street, Cambridge, CB2 3QG, UK,

Chimpanzees manufacture flexible fishing probes to fish for termites in Issa, Ugalla, western Tanzania. These termite-fishing tools are similar in size and material to those used by long-studied communities of chimpanzees in western Tanzania (Pan troglodytes schweinfurthii) and in West Africa (P. t. verus), but not central African populations (P. t. troglodytes). This report adds to the patchwork of evidence of termite-fishing tool use behaviour by chimpanzees across Africa.
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http://dx.doi.org/10.1007/s10329-013-0362-6DOI Listing
January 2014

The malagarasi river does not form an absolute barrier to chimpanzee movement in Western Tanzania.

PLoS One 2013 11;8(3):e58965. Epub 2013 Mar 11.

Department of Anthropology, University of California San Diego, San Diego, California, United States of America.

The Malagarasi River has long been thought to be a barrier to chimpanzee movements in western Tanzania. This potential geographic boundary could affect chimpanzee ranging behavior, population connectivity and pathogen transmission, and thus has implications for conservation strategies and government policy. Indeed, based on mitochondrial DNA sequence comparisons it was recently argued that chimpanzees from communities to the north and to the south of the Malagarasi are surprisingly distantly related, suggesting that the river prevents gene flow. To investigate this, we conducted a survey along the Malagarasi River. We found a ford comprised of rocks that researchers could cross on foot. On a trail leading to this ford, we collected 13 fresh fecal samples containing chimpanzee DNA, two of which tested positive for SIVcpz. We also found chimpanzee feces within the riverbed. Taken together, this evidence suggests that the Malagarasi River is not an absolute barrier to chimpanzee movements and communities from the areas to the north and south should be considered a single population. These results have important consequences for our understanding of gene flow, disease dynamics and conservation management.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0058965PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3594223PMC
December 2013

Prevalence and climatic associated factors of Cryptosporidium sp. infections in savanna chimpanzees from Ugalla, Western Tanzania.

Parasitol Res 2013 Jan 11;112(1):393-9. Epub 2012 Oct 11.

Laboratory of Parasitology, Faculty of Pharmacy, University of Barcelona, Av. Joan XXIII s/n E-08028, Barcelona, Catalonia, Spain.

Studies about parasitization by Cryptosporidium in great apes have been scarce and mostly conducted in captivity. The present study reports the presence of Cryptosporidium sp. in wild chimpanzees (Pan troglodytes) from Ugalla, western Tanzania. Ugalla is one of the driest, most open, and seasonal habitats inhabited by chimpanzees. Cryptosporidium sp. was found in 8.9 % of the samples. The presence of the parasite was determined by preserving fecal samples in chemical conventional fixatives (MIF and alcohol absolute) staining them using a modified Zielh-Neelsen technique, and examining them with a light microscope. The number of fecal samples positive for Cryptosporidium was significantly higher during the rainy than during the dry season (p < 0.005). The results showed that feces collected in the rainy season were almost three times more likely to be positive for Cryptosporidium than those collected in the dry season (OR = 2.81). Cryptosporidium detection was significantly negatively affected by highest temperatures (>28.7 °C, p < 0.001). Cryptosporidiosis can cause serious health problems in humans and its potential effect on Ugalla chimpanzees is discussed.
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http://dx.doi.org/10.1007/s00436-012-3147-8DOI Listing
January 2013

High prevalence of simian immunodeficiency virus infection in a community of savanna chimpanzees.

J Virol 2011 Oct 20;85(19):9918-28. Epub 2011 Jul 20.

Department of Microbiology, University of Alabama, Birmingham, AL 35294, USA.

Simian immunodeficiency virus of chimpanzees (SIVcpz) has a significant negative impact on the health, reproduction, and life span of chimpanzees, yet the prevalence and distribution of this virus in wild-living populations are still only poorly understood. Here, we show that savanna chimpanzees, who live in ecologically marginal habitats at 10- to 50-fold lower population densities than forest chimpanzees, can be infected with SIVcpz at high prevalence rates. Fecal samples were collected from nonhabituated eastern chimpanzees (Pan troglodytes schweinfurthii) in the Issa Valley (n = 375) and Shangwa River (n = 6) areas of the Masito-Ugalla region in western Tanzania, genotyped to determine the number of sampled individuals, and tested for SIVcpz-specific antibodies and nucleic acids. None of 5 Shangwa River apes tested positive for SIVcpz; however, 21 of 67 Issa Valley chimpanzees were SIVcpz infected, indicating a prevalence rate of 31% (95% confidence interval, 21% to 44%). Two individuals became infected during the 14-month observation period, documenting continuing virus spread in this community. To characterize the newly identified SIVcpz strains, partial and full-length viral sequences were amplified from fecal RNA of 10 infected chimpanzees. Phylogenetic analyses showed that the Ugalla viruses formed a monophyletic lineage most closely related to viruses endemic in Gombe National Park, also located in Tanzania, indicating a connection between these now separated communities at some time in the past. These findings document that SIVcpz is more widespread in Tanzania than previously thought and that even very low-density chimpanzee populations can be infected with SIVcpz at high prevalence rates. Determining whether savanna chimpanzees, who face much more extreme environmental conditions than forest chimpanzees, are more susceptible to SIVcpz-associated morbidity and mortality will have important scientific and conservation implications.
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http://dx.doi.org/10.1128/JVI.05475-11DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3196395PMC
October 2011