Hugo Rebelo

Unravelling biodiversity, evolution and threats to conservation in the Sahara‐Sahel

Deserts and arid regions are generally perceived as bare and rather homogeneous areas of low diversity. The Sahara is the largest warm desert in the world and together with the arid Sahel displays high topographical and climatic heterogeneity, and has experienced recent and strong climatic oscillations that have greatly shifted biodiversity distribution and community composition. The large size, remoteness and long‐term political instability of the Sahara‐Sahel, have limited knowledge on its biodiversity. However, over the last decade, there have been an increasing number of published scientific studies based on modern geomatic and molecular tools, and broad sampling of taxa of these regions. This review tracks trends in knowledge about biodiversity patterns, processes and threats across the Sahara‐Sahel, and anticipates needs for biodiversity research and conservation. Recent studies are changing completely the perception of regional biodiversity patterns. Instead of relatively low species diversity with distribution covering most of the region, studies now suggest a high rate of endemism and larger number of species, with much narrower and fragmented ranges, frequently limited to micro‐hotspots of biodiversity. Molecular‐based studies are also unravelling cryptic diversity associated with mountains, which together with recent distribution atlases, allows identifying integrative biogeographic patterns in biodiversity distribution. Mapping of multivariate environmental variation (at 1 km × 1 km resolution) of the region illustrates main biogeographical features of the Sahara‐Sahel and supports recently hypothesised dispersal corridors and refugia. Micro‐scale water‐features present mostly in mountains have been associated with local biodiversity hotspots. However, the distribution of available data on vertebrates highlights current knowledge gaps that still apply to a large proportion of the Sahara‐Sahel. Current research is providing insights into key evolutionary and ecological processes, including causes and timing of radiation and divergence for multiple taxa, and associating the onset of the Sahara with diversification processes for low‐mobility vertebrates. Examples of phylogeographic patterns are showing the importance of allopatric speciation in the Sahara‐Sahel, and this review presents a synthetic overview of the most commonly hypothesised diversification mechanisms. Studies are also stressing that biodiversity is threatened by increasing human activities in the region, including overhunting and natural resources prospection, and in the future by predicted global warming. A representation of areas of conflict, landmines, and natural resources extraction illustrates how human activities and regional insecurity are hampering biodiversity research and conservation. Although there are still numerous knowledge gaps for the optimised conservation of biodiversity in the region, a set of research priorities is provided to identify the framework data needed to support regional conservation planning.

The shaping of genetic variation in edge‐of‐range populations under past and future climate change

With rates of climate change exceeding the rate at which many species are able to shift their range or adapt, it is important to understand how future changes are likely to affect biodiversity at all levels of organisation. Understanding past responses and extent of niche conservatism in climatic tolerance can help predict future consequences. We use an integrated approach to determine the genetic consequences of past and future climate changes on a bat species, Plecotus austriacus. Glacial refugia predicted by palaeo-modelling match those identified from analyses of extant genetic diversity and model-based inference of demographic history. Former refugial populations currently contain disproportionately high genetic diversity, but niche conservatism, shifts in suitable areas and barriers to migration mean that these hotspots of genetic diversity are under threat from future climate change. Evidence of population decline despite recent northward migration highlights the need to conserve leading-edge populations for spearheading future range shifts.

Genetic variation among spiny-footed lizards in the Acanthodactylus pardalis group from North Africa

ABSTRACT The systematics of the genus Acanthodactylus was classically based on external morphological traits, osteological characters and morphology of the hemipenes. Although the identification of species complexes is relatively easy, the distinction within some groups is difficult due to a high variability of the external morphology. Partial mitochondrial (12S and 16S rRNA) sequences (371 and 499 base pairs, respectively) were analysed from 32 specimens of the A. pardalis group from northern Africa including the described species A. busacki, A. maculatus, A. mechriguensis and A. pardalis. Several highly distinct genetic units were resolved, but with little support for relationships between them. These units did not coincide with current taxonomic units, but showed geographic structuring. Although the A. pardalis group displays significant variation, the present taxonomy of the group must be considered unsatisfactory since it is not supported by genetic evidence. For some forms, such as A. mechriguensis there is no support and it is suggested that it should be synonymized with A. maculatus. More data are clearly needed for other forms. Complex microevolutionary patterns due to the recent contraction/expansion phases of the Sahara Desert probably are related with the phylogenetic patterns observed.

What Story Does Geographic Separation of Insular Bats Tell? A Case Study on Sardinian Rhinolophids

Competition may lead to changes in a species’ environmental niche in areas of sympatry and shifts in the niche of weaker competitors to occupy areas where stronger ones are rarer. Although mainland Mediterranean (Rhinolophus euryale) and Mehely’s (R. mehelyi) horseshoe bats mitigate competition by habitat partitioning, this may not be true on resource-limited systems such as islands. We hypothesize that Sardinian R. euryale (SAR) have a distinct ecological niche suited to persist in the south of Sardinia where R. mehelyi is rarer. Assuming that SAR originated from other Italian populations (PES) – mostly allopatric with R. mehelyi – once on Sardinia the former may have undergone niche displacement driven by R. mehelyi. Alternatively, its niche could have been inherited from a Maghrebian source population. We: a) generated Maxent Species Distribution Models (SDM) for Sardinian populations; b) calibrated a model with PES occurrences and projected it to Sardinia to see whether PES niche would increase R. euryale’s sympatry with R. mehelyi; and c) tested for niche similarity between R. mehelyi and PES, PES and SAR, and R. mehelyi and SAR. Finally we predicted R. euryale’s range in Northern Africa both in the present and during the Last Glacial Maximum (LGM) by calibrating SDMs respectively with SAR and PES occurrences and projecting them to the Maghreb. R. mehelyi and PES showed niche similarity potentially leading to competition. According to PES’ niche, R. euryale would show a larger sympatry with R. mehelyi on Sardinia than according to SAR niche. Such niches have null similarity. The current and LGM Maghrebian ranges of R. euryale were predicted to be wide according to SAR’s niche, negligible according to PES’ niche. SAR’s niche allows R. euryale to persist where R. mehelyi is rarer and competition probably mild. Possible explanations may be competition-driven niche displacement or Maghrebian origin.

Postglacial colonization of Europe by the barbastelle bat: agreement between molecular data and past predictive modelling

The barbastelle (Barbastella barbastellus) is a rare forest bat with a wide distribution in Europe. Here, we combine results from the analysis of two mtDNA fragments with species distribution modelling to determine glacial refugia and postglacial colonization routes. We also investigated whether niche conservatism occurs in this species. Glacial refugia were identified in the three southern European peninsulas: Iberia, Italy and the Balkans. These latter two refugia played a major role in the postglacial colonization process, with their populations expanding to England and central Europe, respectively. Palaeo‐distribution models predicted that suitable climatic conditions existed in the inferred refugia during the last glacial maximum (LGM). Nevertheless, the overlap between the current and the LGM distributions was almost inexistent in Italy and in the Balkans, meaning that B. barbastellus populations were forced to shift range between glacial and interglacial periods, a process that probably caused some local extinctions. In contrast, Iberian populations showed a ‘refugia within refugium’ pattern, with two unconnected areas containing stable populations (populations that subsisted during both glacial and interglacial phases). Moreover, the match between LGM models and the refugial areas determined by molecular analysis supported the hypothesis of niche conservatism in B. barbastellus. We argue that geographic patterns of genetic structuring, altogether with the modelling results, indicate the existence of four management units for conservation: Morocco, Iberia, Italy and UK, and Balkans and central Europe. In addition, all countries sampled possessed unique gene pools, thus stressing the need for the conservation of local populations.

Factors Influencing Bat Activity and Mortality at a Wind Farm in the Mediterranean Region

Our study aims to determine how different climatic variables influence bat activity and mortality at wind farms in Portugal. The study was conducted from March to October 2007 at a wind farm with 20 turbines located in Northern Portugal. Bat activity was determined by ground bounded acoustic sampling, while mortality was assessed through fatality searches around each turbine. Sampling occurred weekly and activity was measured the night before fatality search. The highest activity and mortality rates were from Nyctalus leisleri and Pipistrellus pipistrellus. The majority of activity and mortality (95% and 94% in that order) occurred from August to October and both were significantly correlated with wind speed, temperature and relative humidity; mortality also appeared to be influenced by wind direction. Our results show that it is possible to establish a relationship between ground bounded activity and mortality. Our results are relevant for the implementation of effective minimization measures and, therefore, for bat conservation in the Mediterranean region. Specifically, our results show that nearly all (94%) of bat mortality at wind farms happens from August to October, at temperatures higher than 13.O°C, and wind speeds lower than 5.0 m.s-1.

Designing Optimized Multi-Species Monitoring Networks to Detect Range Shifts Driven by Climate Change: A Case Study with Bats in the North of Portugal

Here we develop a framework to design multi-species monitoring networks using species distribution models and conservation planning tools to optimize the location of monitoring stations to detect potential range shifts driven by climate change. For this study, we focused on seven bat species in Northern Portugal (Western Europe). Maximum entropy modelling was used to predict the likely occurrence of those species under present and future climatic conditions. By comparing present and future predicted distributions, we identified areas where each species is likely to gain, lose or maintain suitable climatic space. We then used a decision support tool (the Marxan software) to design three optimized monitoring networks considering: a) changes in species likely occurrence, b) species conservation status, and c) level of volunteer commitment. For present climatic conditions, species distribution models revealed that areas suitable for most species occur in the north-eastern part of the region. However, areas predicted to become climatically suitable in the future shifted towards west. The three simulated monitoring networks, adaptable for an unpredictable volunteer commitment, included 28, 54 and 110 sampling locations respectively, distributed across the study area and covering the potential full range of conditions where species range shifts may occur. Our results show that our framework outperforms the traditional approach that only considers current species ranges, in allocating monitoring stations distributed across different categories of predicted shifts in species distributions. This study presents a straightforward framework to design monitoring schemes aimed specifically at testing hypotheses about where and when species ranges may shift with climatic changes, while also ensuring surveillance of general population trends.

Female dietary bias towards large migratory moths in the European free-tailed bat (Tadarida teniotis).

In bats, sexual segregation has been described in relation to differential use of roosting and foraging habitats. It is possible that variation may also exist between genders in the use of different prey types. However, until recently this idea was difficult to test owing to poorly resolved taxonomy of dietary studies. Here, we use high-throughput sequencing to describe gender-related variation in diet composition of the European free-tailed bat (Tadarida teniotis), while controlling for effects of age and season. We analysed guano pellets collected from 143 individuals mist-netted from April to October 2012 and 2013, in northeast Portugal. Moths (Lepidoptera; mainly Noctuidae and Geometridae) were by far the most frequently recorded prey, occurring in nearly all samples and accounting for 96 out of 115 prey taxa. There were significant dietary differences between males and females, irrespective of age and season. Compared to males, females tended to consume larger moths and more moths of migratory behaviour (e.g. Autographa gamma). Our study provides the first example of gender-related dietary variation in bats, illustrating the value of novel molecular tools for revealing intraspecific variation in food resource use in bats and other insectivores.

Responses of Bats to Climate Change: Learning from the Past and Predicting the Future

Climate change is widely regarded as being of major and growing importance for influencing the future distribution and abundance of organisms. However, the potential effect on bats has received little attention. Herein we provide some general background for climate change and its broader context to biodiversity. We use predicted climate-induced ‘universal responses’ by organisms and data from historical (Holocene) events to better predict how bats may respond. We also outline how climate change effects on bats will create challenges for populations in the future, how best to mitigate impacts and current research needs.

Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: Evidence from DNA metabarcoding

The interaction between agricultural production and wildlife can shape, and even condition, the functioning of both systems. In this study, we i) explored the degree to which a widespread European bat, namely the common bent‐wing bat Miniopterus schreibersii, consumes crop‐damaging insects at a continental scale, and ii) tested whether its dietary niche is shaped by the extension and type of agricultural fields. We employed a dual‐primer DNA metabarcoding approach to characterize arthropod 16S and COI DNA sequences within bat faecal pellets collected across 16 Southern European localities, to first characterize the bat species’ dietary niche, second measure the incidence of agricultural pests across their ranges and third assess whether geographical dietary variation responds to climatic, landscape diversity, agriculture type and vegetation productivity factors. We detected 12 arthropod orders, among which lepidopterans were predominant. We identified >200 species, 44 of which are known to cause agricultural damage. Pest species were detected at all but one sampling site and in 94% of the analysed samples. Furthermore, the dietary diversity of M. schreibersii exhibited a negative linear relation with the area of intensive agricultural fields, thus suggesting crops restrict the dietary niche of bats to prey taxa associated with agricultural production within their foraging range. Overall, our results imply that M. schreibersii might be a valuable asset for biological pest suppression in a variety of agricultural productions and highlight the dynamic interplay between wildlife and agricultural systems.