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Tolley K.A.,South African National Biodiversity Institute | Tolley K.A.,Stellenbosch University | Tilbury C.R.,Stellenbosch University | Measey G.J.,South African National Biodiversity Institute | And 5 more authors.
Journal of Biogeography | Year: 2011

Aim East Africa is one of the most biologically diverse regions, especially in terms of endemism and species richness. Hypotheses put forward to explain this high diversity invoke a role for forest refugia through: (1) accumulation of new species due to radiation within refugial habitats, or (2) retention of older palaeoendemic species in stable refugia. We tested these alternative hypotheses using data for a diverse genus of East African forest chameleons, Kinyongia. Location East Africa. Methods We constructed a dated phylogeny for Kinyongia using one nuclear and two mitochondrial markers. We identified areas of high phylogenetic diversity (PD) and evolutionary diversity (ED), and mapped ancestral areas to ascertain whether lineage diversification could best be explained by vicariance or dispersal. Results Vicariance best explains the present biogeographic patterns, with divergence between three major Kinyongia clades (Albertine Rift, southern Eastern Arc, northern Eastern Arc) in the early Miocene/Oligocene (>20Ma). Lineage diversification within these clades pre-dates the Pliocene (>6Ma). These dates are much older than the Plio-Pleistocene climatic shifts associated with cladogenesis in other East African taxa (e.g. birds), and instead point to a scenario whereby palaeoendemics are retained in refugia, rather than more recent radiations within refugia. Estimates of PD show that diversity was highest in the Uluguru, Nguru and East Usambara Mountains and several lineages (from Mount Kenya, South Pare and the Uluguru Mountains) stand out as being evolutionarily distinct as a result of isolation in forest refugia. PD was lower than expected by chance, suggesting that the phylogenetic signal is influenced by an unusually low number of extant lineages with long branch lengths, which is probably due to the retention of palaeoendemic lineages. Main conclusions The biogeographic patterns associated with Kinyongia are the result of long evolutionary histories in isolation. The phylogeny is dominated by ancient lineages whose origins date back to the early Miocene/Oligocene as a result of continental wide forest fragmentation and contraction due to long term climatic changes in Africa. The maintenance of palaeoendemic lineages in refugia has contributed substantially to the remarkably high biodiversity of East Africa. © 2011 Blackwell Publishing Ltd.


Menegon M.,Tropical Biodiversity Section | Menegon M.,Manchester Metropolitan University | Loader S.P.,University of Basel | Marsden S.J.,Manchester Metropolitan University | And 3 more authors.
Molecular Phylogenetics and Evolution | Year: 2014

Past climatic and tectonic events are believed to have strongly influenced species diversity in the Eastern Afromontane Biodiversity Hotspot. We investigated the phylogenetic relationships and historical biogeography of the East African genus Atheris (Serpentes: Viperidae), and explored temporal and spatial relationships between Atheris species across Africa, and the impact of palaeoclimatic fluctuations and tectonic movements on cladogenesis of the genus. Using mitochondrial sequence data, the phylogeny of East African species of Atheris shows congruent temporal patterns that link diversification to major tectonic and aridification events within East Africa over the last 15. million years (my). Our results are consistent with a scenario of a delayed direct west-east colonisation of the Eastern Arc Mountains of Atheris by the formation of the western rift. Based on the phylogenetic patterns, this terrestrial, forest-associated genus has dispersed into East Africa across a divided route, on both west-southeasterly and west-northeasterly directions (a C-shaped route). Cladogenesis in the Eastern Arc Mountains and Southern Highlands of Tanzania corresponds to late Miocene and Plio-Pleistocene climatic shifts. Taxonomically, our data confirmed the monophyly of Atheris as currently defined, and reveal four major East African clades, three of which occur in discrete mountain ranges. Possible cryptic taxa are identified in the Atheris rungweensis and A. ceratophora clades. © 2014 Elsevier Inc.


Rovero F.,Tropical Biodiversity Section | Rovero F.,Udzungwa Ecological Monitoring Center | Mtui A.S.,Udzungwa Ecological Monitoring Center | Kitegile A.S.,Udzungwa Ecological Monitoring Center | And 2 more authors.
Biological Conservation | Year: 2012

Hunting and habitat degradation are universal threats to primates across the tropics, thus deciphering the relative impact of threats on population relative abundance is critical to predicting extinction risk and providing conservation recommendations. We studied diurnal primates over a period of nearly 6. years in the Udzungwa Mountains of Tanzania, a site of global importance for primate conservation. We assessed how population relative abundance of five species (of which two are endemic and IUCN-Endangered) differed between two forest blocks that are similar in size and habitat types but contrast strongly in protection level, and how abundance changed during 2004-2009. We also measured habitat and disturbance parameters and, in the unprotected forest, evaluated hunting practices. We found significant differences in primates' abundance between protected and unprotected forests, with the greater contrast being the lower abundance of colobine monkeys (Udzungwa red colobus and Angolan colobus) in the unprotected forest. At this site moreover, colobines declined to near-extinction over the study period. In contrast, two cercopithecines (Sanje mangabey and Sykes' monkey) showed slightly higher abundance in the unprotected forest and did not decline significantly. We argue that escalating hunting in the unprotected forest has specifically impacted the canopy-dwelling colobus monkeys, although habitat degradation may also have reduced their abundance. In contrast, cercopithecines did not seem affected by the current hunting, and their greater ecological adaptability may explain the relatively higher abundance in the unprotected forest. We provide recommendations towards the long-term protection of the area. © 2011 Elsevier Ltd.


Lawson L.P.,University of Chicago | Lawson L.P.,University of Cincinnati | Bates J.M.,University of Chicago | Menegon M.,Tropical Biodiversity Section | Loader S.P.,University of Basel
BMC Evolutionary Biology | Year: 2015

Background: Peripatric speciation and peripheral isolation have uncertain importance in species accumulation, and are largely overshadowed by assumed dominance of allopatric modes of speciation. Understanding the role of different speciation mechanisms within biodiversity hotspots is central to understanding the generation of biological diversity. Here, we use a phylogeographic analysis of the spiny-throated reed frogs and examine sister pairings with unbalanced current distributional ranges for characteristics of peripatric speciation. We further investigate whether forest/grassland mosaic adapted species are more likely created through peripatric speciation due to instability of this habitat type. Results: We reconstructed a multi-locus molecular phylogeny of spiny-throated reed frogs which we then combined with comparative morphologic data to delimit species and analyze historical demographic change; identifying three new species. Three potential peripatric speciation events were identified along with one case of allopatric speciation. Peripatric speciation is supported through uneven potential and realized distributions and uneven population size estimates based on field collections. An associated climate shift was observed in most potentially peripatric splits. Morphological variation was highest in sexually dimorphic traits such as body size and gular shape, but this variation was not limited to peripatric species pairs as hypothesized. The potentially allopatric species pair showed no niche shifts and equivalent effective population sizes, ruling out peripatry in that speciation event. Two major ecological niche shifts were recovered within this radiation, possibly as adaptations to occupy areas of grassland that became more prevalent in the last 5 million years. Restricted and fluctuating grassland mosaics within forests might promote peripatric speciation in the Eastern Arc Biodiversity Hotspot (EABH). Conclusions: In our case study, peripatric speciation appears to be an important driver of diversity within the EABH biodiversity hotspot, implying it could be a significant speciation mechanism in highly fragmented ecosystems. Extensive peripatric speciation in this montane archipelago may explain the abundance of discrete lineages within the limited area of the EABH, as inferred in remote island archipelagos. Future phylogenetic studies incorporating demographic and spatial analyses will clarify the role of peripatric speciation in creating biodiversity hotspots. © 2015 Lawson et al.


Rovero F.,Tropical Biodiversity Section | Rovero F.,Udzungwa Ecological Monitoring Center | Martin E.,Udzungwa Ecological Monitoring Center | Martin E.,Sokoine University of Agriculture | And 3 more authors.
PLoS ONE | Year: 2014

Medium-to-large mammals within tropical forests represent a rich and functionally diversified component of this biome; however, they continue to be threatened by hunting and habitat loss. Assessing these communities implies studying species' richness and composition, and determining a state variable of species abundance in order to infer changes in species distribution and habitat associations. The Tropical Ecology, Assessment and Monitoring (TEAM) network fills a chronic gap in standardized data collection by implementing a systematic monitoring framework of biodiversity, including mammal communities, across several sites. In this study, we used TEAM camera trap data collected in the Udzungwa Mountains of Tanzania, an area of exceptional importance for mammal diversity, to propose an example of a baseline assessment of species' occupancy. We used 60 camera trap locations and cumulated 1,818 camera days in 2009. Sampling yielded 10,647 images of 26 species of mammals. We estimated that a minimum of 32 species are in fact present, matching available knowledge from other sources. Estimated species richness at camera sites did not vary with a suite of habitat covariates derived from remote sensing, however the detection probability varied with functional guilds, with herbivores being more detectable than other guilds. Species-specific occupancy modelling revealed novel ecological knowledge for the 11 most detected species, highlighting patterns such as 'montane forest dwellers', e.g. the endemic Sanje mangabey (Cercocebus sanjei), and 'lowland forest dwellers', e.g. suni antelope (Neotragus moschatus). Our results show that the analysis of camera trap data with account for imperfect detection can provide a solid ecological assessment of mammal communities that can be systematically replicated across sites. © 2014 Rovero et al.


Loader S.P.,University of Basel | Lawson L.P.,University of Chicago | Lawson L.P.,University of Cincinnati | Portik D.M.,University of California at Berkeley | Menegon M.,Tropical Biodiversity Section
BMC Research Notes | Year: 2015

Background: The East African spiny-throated reed frog complex (Hyperolius spinigularis, H. tanneri, and H. minutissimus) is comprised of morphologically similar species with highly fragmented populations across the Eastern Afromontane Region. Recent genetic evidence has supported the distinctiveness of populations suggesting a number of cryptic species. We analyse newly collected morphological data and evaluate the taxonomic distinctiveness of populations. Results: We find three new distinct species on the basis of morphological and molecular evidence. The primary morphological traits distinguishing species within the Hyperolius spinigularis complex include the proportions and degree of spinosity of the gular flap in males and snout-urostyle length in females. Other features allow the three species to be distinguished from each other (genetics). We refine the understanding of H. minutissimus which can be found in both forest and grassland habitats of the Udzungwa Mountains, and provide more details on the call of this species. Further details on ecology are noted for all species where known. Conclusions: Three new species are described and we narrow the definition and distribution of Hyperolius spinigularis and H. minutissimus in East Africa. The spiny-throated reed frogs have highly restricted distributions across the fragmented mountains of the Eastern Afromontane region. Given the newly defined and substantially narrower distributions of these spiny-throated reed frog species, conservation concerns are outlined. © 2015 Loader et al.; licensee BioMed Central.


Muller H.,Friedrich - Schiller University of Jena | Liedtke H.C.,University of Basel | Menegon M.,Tropical Biodiversity Section | Beck J.,University of Basel | And 3 more authors.
Biology Letters | Year: 2013

Many amphibian lineages show terrestrialization of their reproductive strategy and breeding is partially or completely independent of water. A number of causal factors have been proposed for the evolution of terrestrialized breeding. While predation has received repeated attention as a potential factor, the influence of other factors such as habitat has never been tested using appropriate data or methods. Using a dataset that comprises 180 amphibian species from various East African habitats, we tested whether species occurring in different habitats show different patterns of terrestrialization in their breeding strategy. We recovered a significant association between terrestrialized breeding strategies and forest habitats. In general, forest seems to act as a facilitator, providing a permissive environment for the evolution of terrestrialized breeding strategies. However, while terrestrial oviposition is strongly correlated with lowland and montane forest habitat, complete terrestrial development is significantly correlated with montane forest only, indicating different selective pressures acting at different steps towards complete terrestrial development. © 2013 The Author(s) Published by the Royal Society.


PubMed | University of Trento, University of York, Tropical Biodiversity Section and Research and Innovation Center Fondazione Edmund Machinery
Type: Journal Article | Journal: Ecological applications : a publication of the Ecological Society of America | Year: 2017

Spatially explicit models of animal abundance are a critical tool to inform conservation planning and management. However, they require the availability of spatially diffuse environmental predictors of abundance, which may be challenging, especially in complex and heterogeneous habitats. This is particularly the case for tropical mammals, such as nonhuman primates, that depend on multi-layered and species-rich tree canopy coverage, which is usually measured through a limited sample of ground plots. We developed an approach that calibrates remote-sensing imagery to ground measurements of tree density to derive basal area, in turn used as a predictor of primate density based on published models. We applied generalized linear models (GLM) to relate 9.8-ha ground samples of tree basal area to various metrics extracted from Landsat 8 imagery. We tested the potential of this approach for spatial inference of animal density by comparing the density predictions for an endangered colobus monkey, to previous estimates from field transect counts, measured basal area, and other predictors of abundance. The best GLM had high accuracy and showed no significant difference between predicted and observed values of basal area. Our species distribution model yielded predicted primate densities that matched those based on field measurements. Results show the potential of using open-access and global remote-sensing data to derive an important predictor of animal abundance in tropical forests and in turn to make spatially explicit inference on animal density. This approach has important, inherent applications as it greatly magnifies the relevance of abundance modeling for informing conservation. This is especially true for threatened species living in heterogeneous habitats where spatial patterns of abundance, in relation to habitat and/or human disturbance factors, are often complex and, management decisions, such as improving forest protection, may need to be focused on priority areas.


PubMed | Leibniz Institute For Primatenforschung, Naturhistorisches Museum Bern, Federal University of Sergipe, University of Western Australia and 22 more.
Type: Journal Article | Journal: Science advances | Year: 2017

Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats-mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the worlds primates and the costs of their loss to ecosystem health and human society is imperative.


PubMed | Tropical Biodiversity Section and Kyoto University
Type: Journal Article | Journal: American journal of primatology | Year: 2017

Leaf swallowing behavior, known as a form of self-medication for the control of nematode and tapeworm infection, occurs widely in all the African great apes (Pan troglodytes schweinfurthii, P. t. troglodytes, P. t. verus, P. t. vellerosus, Pan paniscus, Gorilla gorilla graueri), except mountain gorillas. It is also reported to occur in a similar context across a wide array of other animal taxa including, domestic dogs, wolves, brown bears, and civets. Despite long-term research on Asian great and small apes, this is the first report of leaf swallowing in an Asian species, the white-handed gibbon (Hylobates lar) in Khao Yai National Park, central Thailand. We present the first evidence of leaf swallowing (Gironniera nervosa Planch CANNABACEA) behavior (N=5 cases) and parasite (Streptopharagus pigmentatus) expulsion (N=4 cases), recorded during 4,300hr of direct animal observations during two distinct research projects. We recovered 4-18 rough, hairy, and hispid surfaced leaves from each sample, undigested and folded, from the freshly evacuated feces of five different individuals (2 males, 3 females, 5 to 34+ years old) living in three different social groups, between the hours of 06:00 to 10:30. Based on close inspection of the leaves, as observed in chimpanzees, it was clear that they were taken into the mouth, one at a time, folded and detached from the stem with the teeth before swallowing them whole. All instances occurred during the rainy season, the time when nematode worms were also found in the feces, although they were not found together with leaves in the same feces. These striking similarities in the details of leaf swallowing between white-handed gibbons and African great apes, and other animal species, suggest a similar self-medicative function.

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