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

Sexual dimorphism in bite performance drives morphological variation in chameleons

Phenotypic performance in different environments is central to understanding the evolutionary and ecological processes that drive adaptive divergence and, ultimately, speciation. Because habitat structure can affect an animal's foraging behaviour, anti-predator defences, and communication behaviour, it can influence both natural and sexual selection pressures. These selective pressures, in turn, act upon morphological traits to maximize an animal's performance. For performance traits involved in both social and ecological activities, such as bite force, natural and sexual selection often interact in complex ways, providing an opportunity to understand the adaptive significance of morphological variation with respect to habitat. Dwarf chameleons within the Bradypodion melanocephalum-Bradypodion thamnobates species complex have multiple phenotypic forms, each with a specific head morphology that could reflect its use of either open-or closed-canopy habitats. To determine whether these morphological differences represent adaptations to their habitats, we tested for differences in both absolute and relative bite performance. Only absolute differences were found between forms, with the closed-canopy forms biting harder than their open-canopy counterparts. In contrast, sexual dimorphism was found for both absolute and relative bite force, but the relative differences were limited to the closed-canopy forms. These results indicate that both natural and sexual selection are acting within both habitat types, but to varying degrees. Sexual selection seems to be the predominant force within the closed-canopy habitats, which are more protected from aerial predators, enabling chameleons to invest more in ornamentation for communication. In contrast, natural selection is likely to be the predominant force in the open-canopy habitats, inhibiting the development of conspicuous secondary sexual characteristics and, ultimately, enforcing their overall diminutive body size and constraining performance

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

Counting chirps : acoustic monitoring of cryptic frogs

Funding for the frog survey was received from the National Geographic Society/Waitt Grants Program (No. W184-11). The EPSRC and NERC helped to fund this research through a PhD grant (No. EP/1000917/1) to D.L.B. R.A. and G.J.M. acknowledge initiative funding from the National Research Foundation of South Africa.1 .  Global amphibian declines have resulted in a vital need for monitoring programmes that follow population trends. Monitoring using advertisement calls is ideal as choruses are undisturbed during data collection. However, methods currently employed by managers frequently rely on trained observers, and/or do not provide density data on which to base trends. 2 .  This study explores the utility of monitoring using acoustic spatially explicit capture-recapture (aSECR) with time of arrival (ToA) and signal strength (SS) as a quantitative monitoring technique to measure call density of a threatened but visually cryptic anuran, the Cape peninsula moss frog Arthroleptella lightfooti. 3 .  The relationships between temporal and environmental variables (date, rainfall, temperature) and A. lightfooti call density at three study sites on the Cape peninsula, South Africa were examined. Acoustic data, collected from an array of six microphones over four months during the winter breeding season, provided a time series of call density estimates. 4 .  Model selection indicated that call density was primarily associated with seasonality fitted as a quadratic function. Call density peaked mid-breeding season. At the main study site, the lowest recorded mean call density (0·160 calls m-2 min-1) occurred in May and reached its peak mid-July (1·259 calls m-2 min-1). The sites differed in call density, but also the effective sampling area. 5 .  Synthesis and applications.The monitoring technique, acoustic spatially explicit capture–recapture (aSCR), quantitatively estimates call density without disturbing the calling animals or their environment, while time of arrival (ToA) and signal strength (SS) significantly add to the accuracy of call localisation, which in turn increases precision of call density estimates without the need for specialist field staff. This technique appears ideally suited to aid the monitoring of visually cryptic, acoustically active species.Publisher PDFPeer reviewe

A general framework for animal density estimation from acoustic detections across a fixed microphone array

Acoustic monitoring can be an efficient, cheap, non‐invasive alternative to physical trapping of individuals. Spatially explicit capture–recapture (SECR) methods have been proposed to estimate calling animal abundance and density from data collected by a fixed array of microphones. However, these methods make some assumptions that are unlikely to hold in many situations, and the consequences of violating these are yet to be investigated. We generalize existing acoustic SECR methodology, enabling these methods to be used in a much wider variety of situations. We incorporate time‐of‐arrival (TOA) data collected by the microphone array, increasing the precision of calling animal density estimates. We use our method to estimate calling male density of the Cape Peninsula Moss Frog Arthroleptella lightfooti. Our method gives rise to an estimator of calling animal density that has negligible bias, and 95% confidence intervals with appropriate coverage. We show that using TOA information can substantially improve estimate precision. Our analysis of the A. lightfooti data provides the first statistically rigorous estimate of calling male density for an anuran population using a microphone array. This method fills a methodological gap in the monitoring of frog populations and is applicable to acoustic monitoring of other species that call or vocalize

Frog eat frog: exploring variables influencing anurophagy

Background. Frogs are generalist predators of a wide range of typically small prey items. But descriptions of dietary items regularly include other anurans, such that frogs are considered to be among the most important of anuran predators. However, the only existing hypothesis for the inclusion of anurans in the diet of post-metamorphic frogs postulates that it happens more often in bigger frogs. Moreover, this hypothesis has yet to be tested

Mechanistic reconciliation of community and invasion ecology

CITATION: Latombe, G., et al. 2021. Mechanistic reconciliation of community and invasion ecology. Ecosphere, 12(2):e03359, doi:10.1002/ecs2.3359.The original publication is available at https://esajournals.onlinelibrary.wiley.comCommunity and invasion ecology have mostly grown independently. There is substantial overlap in the processes captured by different models in the two fields, and various frameworks have been developed to reduce this redundancy and synthesize information content. Despite broad recognition that community and invasion ecology are interconnected, a process‐based framework synthesizing models across these two fields is lacking. Here we review 65 representative community and invasion models and propose a common framework articulated around six processes (dispersal, drift, abiotic interactions, within‐guild interactions, cross‐guild interactions, and genetic changes). The framework is designed to synthesize the content of the two fields, provide a general perspective on their development, and enable their comparison. The application of this framework and of a novel method based on network theory reveals some lack of coherence between the two fields, despite some historical similarities. Community ecology models are characterized by combinations of multiple processes, likely reflecting the search for an overarching theory to explain community assembly and structure, drawing predominantly on interaction processes, but also accounting largely for the other processes. In contrast, most models in invasion ecology invoke fewer processes and focus more on interactions between introduced species and their novel biotic and abiotic environment. The historical dominance of interaction processes and their independent developments in the two fields is also reflected in the lower level of coherence for models involving interactions, compared to models involving dispersal, drift, and genetic changes. It appears that community ecology, with a longer history than invasion ecology, has transitioned from the search for single explanations for patterns observed in nature to investigate how processes may interact mechanistically, thereby generating and testing hypotheses. Our framework paves the way for a similar transition in invasion ecology, to better capture the dynamics of multiple alien species introduced in complex communities. Reciprocally, applying insights from invasion to community ecology will help us understand and predict the future of ecological communities in the Anthropocene, in which human activities are weakening species’ natural boundaries. Ultimately, the successful integration of the two fields could advance a predictive ecology that is urgently required in a rapidly changing world.https://esajournals.onlinelibrary.wiley.com/doi/full/10.1002/ecs2.3359Publisher's versio

Using the IUCN Environmental Impact Classification for Alien Taxa to inform decision-making

The Environmental Impact Classification for Alien Taxa (EICAT) is an important tool for biological invasion policy and management and has been adopted as an International Union for Conservation of Nature (IUCN) standard to measure the severity of environmental impacts caused by organisms living outside their native ranges. EICAT has already been incorporated into some national and local decision-making procedures, making it a particularly relevant resource for addressing the impact of non-native species. Recently, some of the underlying conceptual principles of EICAT, particularly those related to the use of the precautionary approach, have been challenged. Although still relatively new, guidelines for the application and interpretation of EICAT will be periodically revisited by the IUCN community, based on scientific evidence, to improve the process. Some of the criticisms recently raised are based on subjectively selected assumptions that cannot be generalized and may harm global efforts to manage biological invasions. EICAT adopts a precautionary principle by considering a species’ impact history elsewhere because some taxa have traits that can make them inherently more harmful. Furthermore, non-native species are often important drivers of biodiversity loss even in the presence of other pressures. Ignoring the precautionary principle when tackling the impacts of non-native species has led to devastating consequences for human well-being, biodiversity, and ecosystems, as well as poor management outcomes, and thus to significant economic costs. EICAT is a relevant tool because it supports prioritization and management of non-native species and meeting and monitoring progress toward the Kunming–Montreal Global Biodiversity Framework (GBF) Target 6

Using the IUCN Environmental Impact Classification for Alien Taxa to inform decision-making

The Environmental Impact Classification for Alien Taxa (EICAT) is an important tool for biological invasion policy and management and has been adopted as an International Union for Conservation of Nature (IUCN) standard to measure the severity of environmental impacts caused by organisms living outside their native ranges. EICAT has already been incorporated into some national and local decision-making procedures, making it a particularly relevant resource for addressing the impact of non-native species. Recently, some of the underlying conceptual principles of EICAT, particularly those related to the use of the precautionary approach, have been challenged. Although still relatively new, guidelines for the application and interpretation of EICAT will be periodically revisited by the IUCN community, based on scientific evidence, to improve the process. Some of the criticisms recently raised are based on subjectively selected assumptions that cannot be generalized and may harm global efforts to manage biological invasions. EICAT adopts a precautionary principle by considering a species’ impact history elsewhere because some taxa have traits that can make them inherently more harmful. Furthermore, non-native species are often important drivers of biodiversity loss even in the presence of other pressures. Ignoring the precautionary principle when tackling the impacts of non-native species has led to devastating consequences for human well-being, biodiversity, and ecosystems, as well as poor management outcomes, and thus to significant economic costs. EICAT is a relevant tool because it supports prioritization and management of non-native species and meeting and monitoring progress toward the Kunming–Montreal Global Biodiversity Framework (GBF) Target 6