Sequential Fragmentation of Pleistocene Forests in an East Africa Biodiversity Hotspot: Chameleons as a Model to Track Forest History

CITATION: Measey, G. J. & Tolley, K. A. 2011. Sequential fragmentation of Pleistocene forests in an East Africa biodiversity hotspot : chameleons as a model to track forest history. PLoS ONE, 6(10): e26606, doi:10.1371/journal.pone.0026606.The original publication is available at http://journals.plos.org/plosoneBackground The Eastern Arc Mountains (EAM) is an example of naturally fragmented tropical forests, which contain one of the highest known concentrations of endemic plants and vertebrates. Numerous paleo-climatic studies have not provided direct evidence for ancient presence of Pleistocene forests, particularly in the regions in which savannah presently occurs. Knowledge of the last period when forests connected EAM would provide a sound basis for hypothesis testing of vicariance and dispersal models of speciation. Dated phylogenies have revealed complex patterns throughout EAM, so we investigated divergence times of forest fauna on four montane isolates in close proximity to determine whether forest break-up was most likely to have been simultaneous or sequential, using population genetics of a forest restricted arboreal chameleon, Kinyongia boehmei. Methodology/Principal Findings We used mitochondrial and nuclear genetic sequence data and mutation rates from a fossil-calibrated phylogeny to estimate divergence times between montane isolates using a coalescent approach. We found that chameleons on all mountains are most likely to have diverged sequentially within the Pleistocene from 0.93–0.59 Ma (95% HPD 0.22–1.84 Ma). In addition, post-hoc tests on chameleons on the largest montane isolate suggest a population expansion ∼182 Ka. Conclusions/Significance Sequential divergence is most likely to have occurred after the last of three wet periods within the arid Plio-Pleistocene era, but was not correlated with inter-montane distance. We speculate that forest connection persisted due to riparian corridors regardless of proximity, highlighting their importance in the region's historic dispersal events. The population expansion coincides with nearby volcanic activity, which may also explain the relative paucity of the Taita's endemic fauna. Our study shows that forest chameleons are an apposite group to track forest fragmentation, with the inference that forest extended between some EAM during the Pleistocene 1.1–0.9 Ma.http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0026606Publisher's versio

Mind the gaps: investigating the cause of the current range disjunction in the Cape Platanna, Xenopus gilli (Anura: Pipidae)

Low-lying areas of the Cape at Africa’s south-westernmost tip have undergone dramatic marine-remodelling, with regular changes in sea-level following glacial cycles. Species for which marine barriers are impenetrable underwent concomitant radical distribution changes which may account for current range disjunctions. The Cape platanna, Xenopus gilli, is a frog distributed in only three disjunt areas within low-lying regions of the southwestern Cape. We determined the relationship between frogs from these three disjunct areas, by using a combination of morphometric analysis and mtDNA (ND2 and 16S fragments) sequences of 130 frogs from eight ponds. Coalescent analyses on molecular data dated the divergence in two major clades to around 4.6 Mya, a period during which major uplifting on the eastern side of the subcontinent caused climate changes throughout southern Africa. Principal components analysis showed significant morphometric differences between each clade on head and limb measurements. Consistent differences in ventral colouration and patterning were also observed. We report on increased levels of hybridisation with X. laevis throughout the range of X. gilli, which reaches at least 27% hybrids in some ponds. Urgent conservation actions are required to control habitat loss from alien invasive vegetation, and prevent introgression with the domestic-exotic, X. laevis

Patterns of geographic variation between mitochondrial and nuclear markers in Heaviside’s (Benguela) dolphins (Cephalorhynchus heavisidii)

The Heaviside's (or Benguela) dolphin (Cephalorhynchus heavisidii) is endemic to the west coast of southern Africa. The present study investigated the population genetic structure across a large portion of the species distribution using mitochondrial control region and nuclear (microsatellite) markers. A total of 395 biopsy skin samples were analyzed; they were collected from free‐ranging Heaviside's dolphins in 7 locations along 1650 km of coast between Table Bay, South Africa and Walvis Bay, Namibia. Both genetic markers rejected the hypothesis of 1 homogenous population but revealed contrasting results in the genetic structuring of putative populations. Mitochondrial DNA suggested either 2 populations or a fine‐scale division with 6 (sub) populations, while microsatellite markers were indicative of 2 widespread populations with measurable gene flow between them. Neutrality tests and mismatch distribution of the mitochondrial sequences indicated a departure from mutation–drift equilibrium due to a population expansion at the 2 extremes of the geographic range, but not towards the middle of the distribution. These results highlight the importance of evaluating multiple genetic markers to gain reliable insights into population processes and structure.Supplementary material: Table S1 Summary of genetic variation based on 16 microsatellite loci in the Heaviside's dolphin: Ta stands for annealing temperature, bp for allele sizes, and Na represents the number of alleles examined within each putative population where observed (HO) and expected (HE) heterozygosities were estimated; n indicates the number of individuals used in calculations; dash (−) indicates loci which were not polymorphic, PI stands for Probability of Identity per locus, and PIsibs indicates Probability of Identity for genetic similarity among siblings per locus. Locus SCA22 did not amplify and loci Dde09 and Dde059 were monomorphic Table S2 Genetic variability estimates in mtDNA control region sequences excluding singletons (n = 27) for haplotype diversity (h) and nucleotide diversity (π) Table S3 Summary of genetic variation based on 13 microsatellite loci in the Heaviside's dolphin: Na indicates the number of alleles examined per each sampling site where observed (HO) and expected (HE) heterozygosities were estimated, HWE stands for Hardy‐Weinberg equilibrium; n indicates the number of individuals used in calculations, § denotes loci out of HWE (≤0.05) and ∗ indicates evidence for null allele. Locus SCA22 did not amplify and loci Dde09 and Dde059 were monomorphic Table S4 Sex‐biased dispersal results for males and females with respect to FIS, FST, HO, HS, mean assignment and variance assignment Table S5 Haplotype frequencies per sampling location of 51 haplotypes identified in biopsy samples of Heaviside's dolphins obtained at seven locations off the southwest African coast Table S6 STRUCTURE clustering analysis: a. Proportion of Heaviside's dolphin individuals from each of the seven sampling locations assigned to each of the two clusters inferred from STRUCTURE analysis Figure S1 Median‐joining network of mtDNA control region haplotypes without singletons for Heaviside's dolphins found off the southwest coast of southern Africa. Figure S2 Average posterior probability (ln K) for each of the seven clusters (i.e., K 1 to 7) from 15 independent runs. Figure S3 Log‐likelihood values (Ln Pr(X/K)) from 15 independent runs, where the ad hoc statistic delta K (ΔK) shows the most probable number of genetic clusters (K). Figure S4 Bayesian assignment probabilities where K = 6 clusters were inferred from STRUCTURE analysis. Two sampling sites, Hondeklipbaai and Port Nolloth, are grouped together as in the AMOVA results using mtDNA control region data. Each individual is represented by a thin vertical line, which is portioned into K coloured segments that represent the individual's estimated membership fractions in K clusters. Black lines separate individuals of different populations. The six putative populations are labelled below the figure.The National Research Foundation (NRF) of South Africa, the Kate Sanderson Bequest Fund administered by the Internation-al Union for Conservation of Nature (IUCN), the South African National Biodiversity Institute-Threatened Spe-cies Programme, the Andrew W. Mellon Foundation and the Rufford Small Grants Foundation.https://onlinelibrary.wiley.com/journal/174948772020-09-01hj2020Mammal Research Institut

Phylogeny and phylogeography of chelonians from sub-Saharan Africa—A review of current knowledge in tribute to Margaretha D. Hofmeyr

Species-level phylogeny and especially phylogeography of African chelonians is a comparatively under-studied field of research. We review the current knowledge of phylogeny and phylogeography, highlight congruence of spatial phylogeographic patterns amongst chelonians and other taxa and suggest future research directions to address gaps in knowledge. Our review shows that phylogeographic and phylogenetic investigations have led to unexpected findings. For example, for Pelomedusa, a putatively wide-ranging monotypic terrapin genus, cryptic diversity was revealed, with more than ten species being uncovered. The formerly recognized tortoise genus Homopus sensu lato was found to be paraphyletic with respect to Chersina. To resolve this situation, Homopus was restricted to the four-toed species H. areolatus and H. femoralis and the genus Chersobius was resurrected for the five-toed species C. boulengeri, C. signatus, and C. solus. Three previously recognized taxa were shown to be invalid, viz. the putatively extinct terrapin species Pelusios seychellensis and the tortoise subspecies Chersobius signatus cafer and Stigmochelys pardalis babcocki. Together with taxonomy, the knowledge of phylogeographic structuring sets a solid foundation for conservation measures and allows the identification of Management and Conservation Units. However, the current legislation, in particular the enforcement of the Nagoya Protocol under the Convention of Biological Diversity (CBD), has largely halted research on widely distributed taxa and turned the well-intended concept of Access and Benefit Sharing into a major impediment for conservation and research. The current situation leads for many species to a continued usage of outdated and incorrect taxonomic classifications resulting in an error cascade of conservation decisions. This is counterproductive to the aims of the CBD, that is, the protection of biodiversity. Sequencing historical DNA from museum specimens using aDNA approaches could be a short-term approach to mitigate, but not solve, this impediment

Long-term feeding ecology and habitat use in harbour porpoises Phocoena phocoena from Scandinavian waters inferred from trace elements and stable isotopes

BACKGROUND: We investigated the feeding ecology and habitat use of 32 harbour porpoises by-caught in 4 localities along the Scandinavian coast from the North Sea to the Barents Sea using time-integrative markers: stable isotopes (δ(13)C, δ(15)N) and trace elements (Zn, Cu, Fe, Se, total Hg and Cd), in relation to habitat characteristics (bathymetry) and geographic position (latitude). RESULTS: Among the trace elements analysed, only Cd, with an oceanic specific food origin, was found to be useful as an ecological tracer. All other trace elements studied were not useful, most likely because of physiological regulation and/or few specific sources in the food web. The δ(13)C, δ(15)N signatures and Cd levels were highly correlated with each other, as well as with local bathymetry and geographic position (latitude). Variation in the isotopic ratios indicated a shift in harbour porpoise's feeding habits from pelagic prey species in deep northern waters to more coastal and/or demersal prey in the relatively shallow North Sea and Skagerrak waters. This result is consistent with stomach content analyses found in the literature. This shift was associated with a northward Cd-enrichment which provides further support to the Cd 'anomaly' previously reported in polar waters and suggests that porpoises in deep northern waters include Cd-contaminated prey in their diet, such as oceanic cephalopods. CONCLUSION: As stable isotopes and Cd provide information in the medium and the long term respectively, the spatial variation found, shows that harbour porpoises experience different ecological regimes during the year along the Scandinavian coasts, adapting their feeding habits to local oceanographic conditions, without performing extensive migration

Exploration into the hidden world of Mozambique’s sky island forests:new discoveries of reptiles and amphibians

We carried out a survey of reptiles and amphibians within Afromontane forest and woodland slopes of three inselbergs in northern Mozambique (Mount Mabu, Mount Namuli, and Mount Ribáuè). A total of 56 species (22 amphibians and 34 reptiles) were recorded during the current survey. Our findings substantially increase the number of herpetofaunal species recorded from these mountains (Mount Ribáuè 59%, Mount Mabu 37%, and Mount Namuli 11% of the total species), including one new country record and several putative new species. An updated checklist of the herpetofauna of these mountains is presented

Conservation status and threats for African reptiles

The assimilation of information on taxonomy, distribution, basic ecology and conservation status of Africa's reptiles lags far behind that for most other continents. Many regions of mainland Africa are rarely surveyed, resulting in severe knowledge gaps that currently limit effective conservation of African reptiles. Here, we provide a précis on the knowledge gaps and conservation status of mainland African reptiles, and quantify the main threats based on IUCN Red List of Threatened Species assessments using publicly available distribution data. Our results show that these data are insufficient to confidently identify areas of high biodiversity, with large gaps in knowledge in the Horn of Africa, central Africa and West Africa. There is a strong overall taxonomic bias in extinction risk with 45% of families more threatened than expected by chance. Furthermore, Amphisbaenidae, Chameleonidae, Gerrhosauridae, Testudinidae, Viperidae all have a high percentage of their constituent species at risk. Overall, land transformation for agriculture, particularly subsistence farming, constitutes the primary threat to African reptiles, and our derived Threat Index based on socio-economic traits of African countries show that risk is high in Burundi, Ethiopia, Liberia, Malawi, Rwanda and Sierra Leone. These findings highlight important challenges facing the conservation of African reptiles, and we suggest that conservation priorities in mainland Africa be focussed on areas where the potential for overall loss of biodiversity is high, particularly in regions where knowledge is inadequate

A multilocus phylogeny of the world Sycoecinae fig wasps (Chalcidoidea: Pteromalidae)

The Sycoecinae is one of five chalcid subfamilies of fig wasps that are mostly dependent on Ficus inflorescences for reproduction. Here, we analysed two mitochondrial ( COI , Cyt b ) and four nuclear genes (ITS2, EF-1α, RpL27a, mago nashi ) from a worldwide sample of 56 sycoecine species. Various alignment and partitioning strategies were used to test the stability of major clades. All topologies estimated using maximum likelihood and Bayesian methods were similar and well resolved but did not support the existing classification. A high degree of morphological convergence was highlighted and several species appeared best described as species complexes. We therefore proposed a new classification for the subfamily. Our analyses revealed several cases of probable speciation on the same host trees (up to 8 closely related species on one single tree of F. sumatrana ), which raises the question of how resource partitioning occurs to avoid competitive exclusion. Comparisons of our results with fig phylogenies showed that, despite sycoecines being internally ovipositing wasps host-switches are common incidents in their evolutionary history. Finally, by studying the evolutionary properties of the markers we used and profiling their phylogenetic informativeness, we predicted their utility for resolving phylogenetic relationships of Chalcidoidea at various taxonomic levels

Filling the gap: Noteworthy herpetological discoveries in North West Province, South Africa

The North West Province, South Africa, is centrally situated in southern Africa and is characterised by savannah with a mesic, temperate climate in the east and a hot, arid climate in the west. While the eastern region is fairly well-documented for herpetofauna, the arid central and western regions are poorly surveyed. Given that the Province has been targeted by the national government for development of infrastructure, the overall deficiency of biodiversity data could result in impact assessments that are not well-informed. We, therefore, carried out herpetofaunal surveys over two years (2019–2020) in the North West Province to improve knowledge on the distributions of reptiles and amphibians. Our surveys added a total of 578 new records to an earlier baseline of 1340 records. In addition, over 300 records were added to a citizen-science platform in connection with our surveys. As compared to the previous 100 years, our surveys increased the herpetofaunal dataset by 68% in just two years, increased geographic coverage by 20% and brought the total number of species with accurate records for the Province to 102 reptiles and 23 amphibians. We also recorded range extensions for five reptile species and confirmed the presence of Dendroaspis polylepis (Black Mamba) in the west where it had been last recorded in 1996. Our surveys resulted in a significant increase in biodiversity data for the Province and provided a better foundation for spatial planning that accounts for biodiversity and the maintenance of ecological function

A new species of Chameleon (Sauria: Chamaeleonidae: Kinyongia) highlights the biological affinities between the Southern Highlands and Eastern Arc Mountains of Tanzania

A new species of chameleon is described from the Livingstone and Udzungwa Mountains of Tanzania. The new species is morphologically most similar to Kinyongia vanheygeni. Furthermore, a single, short rostral appendage shows the species similarity to other Eastern Arc endemic Kinyongia species (e.g. K. uthmoelleri, K. oxyrhina, K. magomberae and K. tenuis). Females of all these species lack any rostral ornamentation and are all very similar morphologically. Males of the new species, on which the morphological diagnosis is based, can be distinguished from other Kinyongia by a shorter rostral appendage that bifurcates at the tip. They are easily distinguished from K. vanheygeni, otherwise the most similar species, by differences in head scalation and the length and shape of the rostral appendage. The new species is associated with montane rainforest and is known from only four forest fragments of which two are in the Udzungwa and two in the Livingstone Mountains. Phylogenetically, the new species is sister to K. tenuis and K. magomberae, which together, form a clade that also contains K. oxyrhina. The disjunct distribution of the new species, in the Livingstone and Udzungwa mountains, stretches across the ‘Makambako Gap’ which is a putative biogeographical barrier separating the distinct faunas of the Southern highlands and Eastern Arc Mountains. Evidence from this species however, points to potentially closer biological affinities between the Livingstone and Udzungwa mountains