Publications by category
Journal articles
Novella-Fernandez R, Juste J, Ibáñez C, Rebelo H, Russo D, Alberdi A, Kiefer A, Graham L, Paul H, Doncaster CP, et al (In Press). Broad-scale patterns of geographic avoidance between species emerge in the absence of fine-scale mechanisms of coexistence. Diversity and Distributions: a journal of conservation biogeography
Alberdi A, Razgour O, Aizpurua O, Novella-Fernandez R, Aihartza J, Budinski I, Garin I, Ibáñez C, Izagirre E, Rebelo H, et al (In Press). Diet diversification shapes broad-scale distribution patterns in European bats.
Abstract:
Diet diversification shapes broad-scale distribution patterns in European bats
AbstractLarge-scale species’ distributions have been traditionally attributed to physiological traits related to abiotic factors, while behavioural features linked to biotic interactions have received little attention. We tested the relationship between trophic and spatial niche breadths through combining species distribution modelling with dietary DNA metabarcoding of over 400 bats sampled across Europe belonging to seven species. Our results point to a causality cascade between hunting plasticity, trophic niche breadth and spatial niche breadth, and thus indicate that behavioral plasticity and dietary diversification can contribute to shaping broad-scale species distributions.
Abstract.
Razgour O (In Press). Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition.
Biological ReviewsAbstract:
Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition
Biodiversity underlies ecosystem resilience, ecosystem function, sustainable economies, and human well-being. Understanding how biodiversity sustains ecosystems under anthropogenic stressors and global environmental change will require new ways of deriving and applying biodiversity data. A major challenge is that biodiversity data and knowledge are scattered, biased, collected with numerous methods, and stored in inconsistent ways. The Group on Earth Observations Biodiversity Observation Network (GEO BON) has developed the Essential Biodiversity Variables (EBVs) as fundamental metrics to help aggregate, harmonize and interpret biodiversity observation data from diverse sources. Mapping and analysing EBVs can help to evaluate how aspects of biodiversity are distributed geographically and how they change over time. EBVs are also intended to serve as inputs and validation to forecast the status and trends of biodiversity, and to support policy and decision making. Here, we assess the feasibility of implementing Genetic Composition EBVs (Genetic EBVs), which are metrics of within-species genetic variation. We review and bring together numerous areas of the field of genetics and evaluate how each contributes to global and regional genetic biodiversity monitoring with respect to theory, sampling logistics, metadata, archiving, data aggregation, modelling, and technological advances. We propose four Genetic EBVs: (1) genetic diversity; (2) genetic differentiation; (3) inbreeding; and (4) effective population size (Ne). We rank Genetic EBVs according to their relevance, sensitivity to change, generalizability, scalability, feasibility and data availability. We outline the workflow for generating genetic data underlying the Genetic EBVs, and review advances and needs in archiving genetic composition data and metadata. We discuss how Genetic EBVs can be operationalized by visualizing EBVs in space and time across species and by forecasting Genetic EBVs beyond current observations using various modelling approaches. Our review then explores challenges of aggregation, standardization, and costs of operationalizing the Genetic EBVs, as well as future directions and opportunities to maximize their uptake globally in research and policy. The collection, annotation, and availability of genetic data has made major advances in the past decade, each of which contributes to the practical and standardized framework for large-scale genetic observation reporting. Rapid advances in DNA sequencing technology present new opportunities, but also challenges for operationalizing Genetic EBVs for biodiversity monitoring regionally and globally. With these advances, genetic composition monitoring is starting to be integrated into global conservation policy, which can help support the foundation of all biodiversity and species’ long-term persistence in the face of environmental change. We conclude with a summary of concrete steps for researchers and policy makers for advancing operationalization of Genetic EBVs. The technical and analytical foundations of Genetic EBVs are well developed, and conservation practitioners should anticipate their increasing application as efforts emerge to scale up genetic biodiversity monitoring regionally and globally.
Abstract.
Moraes B, Razgour O, Souza- Alves JP, Boubli J, Bezerra B (In Press). Habitat suitability for primate conservation in
north-east Brazil. Oryx: journal of fauna and flora international
Novella-Fernandez R, Ibañez C, Juste J, Clare EL, Doncaster CP, Razgour O (In Press). Trophic resource partitioning drives fine-scale coexistence in cryptic bat species. Ecology and Evolution
Festa F, Ancillotto L, Santini L, Pacifici M, Rocha R, Toshkova N, Amorim F, Benitez-Lopez A, Domer A, Hamidovic D, et al (2022). Bat responses to climate change: a systematic review.
BIOLOGICAL REVIEWS Author URL.
Horta P, Raposeira H, Baños A, Ibáñez C, Razgour O, Rebelo H, Juste J (2022). Counteracting forces of introgressive hybridization and interspecific competition shape the morphological traits of cryptic Iberian Eptesicus bats.
Scientific Reports,
12(1).
Abstract:
Counteracting forces of introgressive hybridization and interspecific competition shape the morphological traits of cryptic Iberian Eptesicus bats
AbstractCryptic species that coexist in sympatry are likely to simultaneously experience strong competition and hybridization. The first phenomenon would lead to character displacement, whereas the second can potentially promote morphological similarity through adaptive introgression. The main goal of this work was to investigate the effect of introgressive hybridization on the morphology of cryptic Iberian Eptesicus bats when facing counteracting evolutionary forces from interspecific competition. We found substantial overlap both in dentition and in wing morphology traits, though mainly in individuals in sympatry. The presence of hybrids contributes to a fifth of this overlap, with hybrids showing traits with intermediate morphometry. Thus, introgressive hybridization may contribute to species adaptation to trophic and ecological space responding directly to the macro-habitats characteristics of the sympatric zone and to local prey availability. On the other hand, fur shade tended to be browner and brighter in hybrids than parental species. Colour differences could result from partitioning of resources as an adaptation to environmental factors such as roost and microhabitats. We argue that a balance between adaptive introgression and niche partitioning shapes species interactions with the environment through affecting morphological traits under selection.
Abstract.
Novella-Fernandez R, Juste J, Ibañez C, Nogueras J, Osborne PE, Razgour O (2022). The role of forest structure and composition in driving the distribution of bats in Mediterranean regions.
Scientific Reports,
12(1).
Abstract:
The role of forest structure and composition in driving the distribution of bats in Mediterranean regions
AbstractForests are key native habitats in temperate environments. While their structure and composition contribute to shaping local-scale community assembly, their role in driving larger-scale species distributions is understudied. We used detailed forest inventory data, an extensive dataset of occurrence records, and species distribution models integrated with a functional approach, to disentangle mechanistically how species-forest dependency processes drive the regional-scale distributions of nine forest specialist bats in a Mediterranean region in the south of Spain. The regional distribution patterns of forest bats were driven primarily by forest composition and structure rather than by climate. Bat roosting ecology was a key trait explaining the strength of the bat-forest dependency relationships. Tree roosting bats were strongly associated with mature and heterogeneous forest with large trees (diameters > 425 mm). Conversely, and contrary to what local-scale studies show, our results did not support that flight-related traits (wing loading and aspect ratio) drive species distributional patterns. Mediterranean forests are expected to be severely impacted by climate change. This study highlights the utility of disentangling species-environment relationships mechanistically and stresses the need to account for species-forest dependency relationships when assessing the vulnerability of forest specialists towards climate change.
Abstract.
Riley J, Zeale MRK, Razgour O, Turpin J, Jones G (2021). Predicting the past, present and future distributions of an endangered marsupial in a semi‐arid environment. Animal Conservation, 24(5), 890-903.
Aizpurua O, Nyholm L, Morris E, Chaverri G, Herrera Montalvo LG, Flores-Martinez JJ, Lin A, Razgour O, Gilbert MTP, Alberdi A, et al (2021). The role of the gut microbiota in the dietary niche expansion of fishing bats.
Animal Microbiome,
3(1).
Abstract:
The role of the gut microbiota in the dietary niche expansion of fishing bats
Abstract
. Background
. Due to its central role in animal nutrition, the gut microbiota is likely a relevant factor shaping dietary niche shifts. We analysed both the impact and contribution of the gut microbiota to the dietary niche expansion of the only four bat species that have incorporated fish into their primarily arthropodophage diet.
.
. Results
. We first compared the taxonomic and functional features of the gut microbiota of the four piscivorous bats to that of 11 strictly arthropodophagous species using 16S rRNA targeted amplicon sequencing. Second, we increased the resolution of our analyses for one of the piscivorous bat species, namely Myotis capaccinii, and analysed multiple populations combining targeted approaches with shotgun sequencing. To better understand the origin of gut microorganisms, we also analysed the gut microbiota of their fish prey (Gambusia holbrooki). Our analyses showed that piscivorous bats carry a characteristic gut microbiota that differs from that of their strict arthropodophagous counterparts, in which the most relevant bacteria have been directly acquired from their fish prey. This characteristic microbiota exhibits enrichment of genes involved in vitamin biosynthesis, as well as complex carbohydrate and lipid metabolism, likely providing their hosts with an enhanced capacity to metabolise the glycosphingolipids and long-chain fatty acids that are particularly abundant in fish.
.
. Conclusions
. Our results depict the gut microbiota as a relevant element in facilitating the dietary transition from arthropodophagy to piscivory.
.
Abstract.
Rocha R, Aziz SA, Brook CE, Carvalho WD, Cooper‐Bohannon R, Frick WF, Huang JC, Kingston T, López‐Baucells A, Maas B, et al (2020). Bat conservation and zoonotic disease risk: a research agenda to prevent misguided persecution in the aftermath of COVID‐19. Animal Conservation, 24(3), 303-307.
Alberdi A, Razgour O, Aizpurua O, Novella-Fernandez R, Aihartza J, Budinski I, Garin I, Ibanez C, Izagirre E, Rebelo H, et al (2020). DNA metabarcoding and spatial modelling link diet diversification with distribution homogeneity in European bats. Nature Communications, 11
White R, Razgour O (2020). Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review, 50, 336-352.
Razgour O, Kasso M, Santos H, Juste J (2020). Up in the air: threats to Afromontane biodiversity from climate change and habitat loss revealed by genetic monitoring of the Ethiopian Highlands bat. Evolutionary Applications: evolutionary approaches to environmental, biomedical and socio-economic issues, 14, 794-806.
Centeno‐Cuadros A, Razgour O, García‐Mudarra JL, Mingo‐Casas P, Sandonís V, Redondo A, Ibáñez C, Paz O, Martinez‐Alós S, Pérez Suarez G, et al (2019). Comparative phylogeography and asymmetric hybridization between cryptic bat species. Journal of Zoological Systematics and Evolutionary Research, 57(4), 1004-1018.
Razgour O, Forester B, Taggart JB, Bekaert M, Juste J, Ibáñez C, Puechmaille SJ, Novella-Fernandez R, Alberdi A, Manel S, et al (2019). Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections.
Proceedings of the National Academy of Sciences,
116(21), 10418-10423.
Abstract:
Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections
Local adaptations can determine the potential of populations to respond to environmental changes, yet adaptive genetic variation is commonly ignored in models forecasting species vulnerability and biogeographical shifts under future climate change. Here we integrate genomic and ecological modeling approaches to identify genetic adaptations associated with climate in two cryptic forest bats. We then incorporate this information directly into forecasts of range changes under future climate change and assessment of population persistence through the spread of climate-adaptive genetic variation (evolutionary rescue potential). Considering climate-adaptive potential reduced range loss projections, suggesting that failure to account for intraspecific variability can result in overestimation of future losses. On the other hand, range overlap between species was projected to increase, indicating that interspecific competition is likely to play an important role in limiting species’ future ranges. We show that although evolutionary rescue is possible, it depends on a population’s adaptive capacity and connectivity. Hence, we stress the importance of incorporating genomic data and landscape connectivity in climate change vulnerability assessments and conservation management.
Abstract.
Amorim F, Razgour O, Mata VA, Lopes S, Godinho R, Ibáñez C, Juste J, Rossiter SJ, Beja P, Rebelo H, et al (2019). Evolutionary history of the European free‐tailed bat, a tropical affinity species spanning across the Mediterranean Basin. Journal of Zoological Systematics and Evolutionary Research, 58(1), 499-518.
Razgour O, Taggart JB, Manel S, Juste J, Ibáñez C, Rebelo H, Alberdi A, Jones G, Park K (2018). An integrated framework to identify wildlife populations under threat from climate change.
Mol Ecol Resour,
18(1), 18-31.
Abstract:
An integrated framework to identify wildlife populations under threat from climate change.
Climate change is a major threat to global biodiversity that will produce a range of new selection pressures. Understanding species responses to climate change requires an interdisciplinary perspective, combining ecological, molecular and environmental approaches. We propose an applied integrated framework to identify populations under threat from climate change based on their extent of exposure, inherent sensitivity due to adaptive and neutral genetic variation and range shift potential. We consider intraspecific vulnerability and population-level responses, an important but often neglected conservation research priority. We demonstrate how this framework can be applied to vertebrates with limited dispersal abilities using empirical data for the bat Plecotus austriacus. We use ecological niche modelling and environmental dissimilarity analysis to locate areas at high risk of exposure to future changes. Combining outlier tests with genotype-environment association analysis, we identify potential climate-adaptive SNPs in our genomic data set and differences in the frequency of adaptive and neutral variation between populations. We assess landscape connectivity and show that changing environmental suitability may limit the future movement of individuals, thus affecting both the ability of populations to shift their distribution to climatically suitable areas and the probability of evolutionary rescue through the spread of adaptive genetic variation among populations. Therefore, a better understanding of movement ecology and landscape connectivity is needed for predicting population persistence under climate change. Our study highlights the importance of incorporating genomic data to determine sensitivity, adaptive potential and range shift potential, instead of relying solely on exposure to guide species vulnerability assessments and conservation planning.
Abstract.
Author URL.
Vasconcelos R, Razgour O, Tarroso P, Fasola M, Carranza S, Alves PC (2018). Combining molecular and landscape tools for targeting evolutionary processes in reserve design: an approach for islands. PLOS ONE, 13(7), e0200830-e0200830.
Razgour O, Persey M, Shamir U, Korine C (2018). The role of climate, water and biotic interactions in shaping biodiversity patterns in arid environments across spatial scales. Diversity and Distributions, 24(10), 1440-1452.
Razgour O, Rebelo H, Di Febbraro M, Russo D (2016). Painting maps with bats: Species distribution modelling in bat research and conservation.
Hystrix,
27(1).
Abstract:
Painting maps with bats: Species distribution modelling in bat research and conservation
Species distribution models (SDMs) offer an effective tool for identifying species conservation requirements and forecasting how global environmental changes will affect species diversity and distribution. This approach is particularly relevant for bats because their nocturnal behaviour hinders detectability and identification in flight. Despite their important contribution to global biodiversity and wide geographical ranges, bats have been under-represented in early SDM studies, and only in the last few years has this approach become more widely used in bat research. We carried out a meta-analysis of the published literature to review the history of the use of SDMs in bat research and their application in conservation, climate change assessments and genetic studies. We focus on the geographical coverage, theme and modelling algorithm of published studies, and compare studies that are uniquely dedicated to bats to multi-taxa studies that include bats. We provide recommendations for good modelling practices through considering spatial scale and spatial biases, selecting ecologically relevant variables, following rigorous modelling protocols, and recognising the limitations of extrapolation across temporal scales. We suggest future developments that will further favour the use of SDMs to study bat ecology and biogeography, as well as inform conservation management. We conclude that despite an increase in bat SDM studies, their scope and application can be further enhanced through incorporating dispersal, landscape connectivity and biotic interactions between bats, their prey and their pathogens.
Abstract.
Jones M, Bertola LD, Razgour O (2016). Predicting the effect of interspecific competition on habitat suitability for the endangered african wild dog under future climate and land cover changes.
Hystrix,
27(1).
Abstract:
Predicting the effect of interspecific competition on habitat suitability for the endangered african wild dog under future climate and land cover changes
Apex predators play an important role in regulating ecological interactions, and therefore their loss can affect biodiversity across trophic levels. Large carnivores have experienced substantial population and range declines across Africa, and future climate change is likely to amplify these threats. Hence it is important to understand how future environmental changes will affect their long-term habitat suitability and population persistence. This study aims to identify the factors limiting the distribution of the endangered African wild dog, Lycaon pictus, and determine how biotic interactions and changing climate and land cover will affect future range suitability. We use Species Distribution Models (SDMs) to predict the current and future distribution of suitable conditions for L. pictus and its dominant competitor Panthera leo. We show that range suitability for L. pictus is limited by climatic and land cover variables, as well as high niche and range overlap with P. leo. Although both species are predicted to experience range contractions under future climate change, L. pictus may benefit from release from the effect of interspecific competition in eastern and central parts of its range. Our study highlights the importance of including land cover variables with corresponding future projections and incorporating the effects of competing species when predicting the future distribution of species whose ranges are not solely limited by climate. We conclude that SDMs can help identify priority areas for the long-term conservation of large carnivores, and therefore should be used to inform adaptive conservation management in face of future climate change.
Abstract.
Razgour O (2015). Beyond species distribution modeling: a landscape genetics approach to investigating range shifts under future climate change.
Ecological Informatics,
30, 250-256.
Abstract:
Beyond species distribution modeling: a landscape genetics approach to investigating range shifts under future climate change
Understanding how biodiversity will respond to future climate change is a major conservation and societal challenge. Climate change is predicted to force many species to shift their ranges in pursuit of suitable conditions. This study aims to use landscape genetics, the study of the effects of environmental heterogeneity on the spatial distribution of genetic variation, as a predictive tool to assess how species will shift their ranges to track climatic changes and inform conservation measures that will facilitate movement. The approach is based on three steps: 1) using species distribution models (SDMs) to predict suitable ranges under future climate change, 2) using the landscape genetics framework to identify landscape variables that impede or facilitate movement, and 3) extrapolating the effect of landscape connectivity on range shifts in response to future climate change. I show how this approach can be implemented using the publicly available genetic dataset of the grey long-eared bat, Plecotus austriacus, in the Iberian Peninsula. Forest cover gradient was the main landscape variable affecting genetic connectivity between colonies. Forest availability is likely to limit future range shifts in response to climate change, primarily over the central plateau, but important range shift pathways have been identified along the eastern and western coasts. I provide outputs that can be directly used by conservation managers and review the viability of the approach. Using landscape genetics as a predictive tool in combination with SDMs enables the identification of potential pathways, whose loss can affect the ability of species to shift their range into future climatically suitable areas, and the appropriate conservation management measures to increase landscape connectivity and facilitate movement.
Abstract.
Alberdi A, Gilbert MTP, Razgour O, Aizpurua O, Aihartza J, Garin I (2015). Contrasting population-level responses to Pleistocene climatic oscillations in an alpine bat revealed by complete mitochondrial genomes and evolutionary history inference.
Journal of Biogeography,
42(9), 1689-1700.
Abstract:
Contrasting population-level responses to Pleistocene climatic oscillations in an alpine bat revealed by complete mitochondrial genomes and evolutionary history inference
Aim: We used an integrative approach to reconstruct the evolutionary history of the alpine long-eared bat, Plecotus macrobullaris, to test whether the variable effects of Pleistocene climatic oscillations across geographical regions led to contrasting population-level demographic histories within a single species. Location: the Western Palaearctic. Methods: We sequenced the complete mitochondrial genomes of 57 individuals from across the distribution of the species. The analysis integrated ecological niche modelling (ENM), approximate Bayesian computation (ABC), measures of genetic diversity and Bayesian phylogenetic methods. Results: We identified two deep lineages: a western lineage, restricted to the Pyrenees and the Alps, and an eastern lineage, which expanded across the mountain ranges east of the Dinarides (Croatia). ENM projections of past conditions predicted that climatic suitability was reduced during cold stages in the areas inhabited by the western lineage, while the opposite trend was observed in the mountains inhabited by the eastern lineage. The palaeodemographic scenario that best fitted our data is consistent with the western lineage population size having shrunk repeatedly because of the extensive glaciation events that occurred in the Alps and Pyrenees during the Pleistocene. In contrast, the eastern lineage maintained a constant population size as is consistent with more limited glaciation in the mountains of south-eastern Europe and the Middle East. Main conclusions: This study shows that the demographic response of populations to Pleistocene climatic oscillations depended on their geographical location, offering an example of population-level variations in the effects and long-term consequences of climate change.
Abstract.
Razgour O, Salicini I, Ibáñez C, Randi E, Juste J (2015). Unravelling the evolutionary history and future prospects of endemic species restricted to former glacial refugia.
Molecular Ecology,
24(20), 5267-5283.
Abstract:
Unravelling the evolutionary history and future prospects of endemic species restricted to former glacial refugia
The contemporary distribution and genetic composition of biodiversity bear a signature of species' evolutionary histories and the effects of past climatic oscillations. For many European species, the Mediterranean peninsulas of Iberia, Italy and the Balkans acted as glacial refugia and the source of range recolonization, and as a result, they contain disproportionately high levels of diversity. As these areas are particularly threatened by future climate change, it is important to understand how past climatic changes affected their biodiversity. We use an integrated approach, combining markers with different evolutionary rates and combining phylogenetic analysis with approximate Bayesian computation and species distribution modelling across temporal scales. We relate phylogeographic processes to patterns of genetic variation in Myotis escalerai, a bat species endemic to the Iberian Peninsula. We found a distinct population structure at the mitochondrial level with a strong geographic signature, indicating lineage divergence into separate glacial refugia within the Iberian refugium. However, microsatellite markers suggest higher levels of gene flow resulting in more limited structure at recent time frames. The evolutionary history of M. escalerai was shaped by the effects of climatic oscillations and changes in forest cover and composition, while its future is threatened by climatically induced range contractions and the role of ecological barriers due to competition interactions in restricting its distribution. This study warns that Mediterranean peninsulas, which provided refuge for European biodiversity during past glaciation events, may become a trap for limited dispersal and ecologically limited endemic species under future climate change, resulting in loss of entire lineages.
Abstract.
Razgour O, Rebelo H, Puechmaille SJ, Juste J, Ibáñez C, Kiefer A, Burke T, Dawson DA, Jones G (2014). Scale-dependent effects of landscape variables on gene flow and population structure in bats.
Diversity and Distributions,
20(10), 1173-1185.
Abstract:
Scale-dependent effects of landscape variables on gene flow and population structure in bats
Aim: a common pattern in biogeography is the scale-dependent effect of environmental variables on the spatial distribution of species. We tested the role of climatic and land cover variables in structuring the distribution of genetic variation in the grey long-eared bat, Plecotus austriacus, across spatial scales. Although landscape genetics has been widely used to describe spatial patterns of gene flow in a variety of taxa, volant animals have generally been neglected because of their perceived high dispersal potential. Location: England and Europe. Methods: We used a multiscale integrated approach, combining population genetics with species distribution modelling and geographical information under a causal modelling framework, to identify landscape barriers to gene flow and their effect on population structure and conservation status. Genotyping involved 23 polymorphic microsatellites and 259 samples from across the species' range. Results: We identified distinct population structure shaped by geographical barriers and evidence of population fragmentation at the northern edge of the range. Habitat suitability (as captured by species distribution models, SDMs) was the most important landscape variable affecting genetic connectivity at the broad spatial scale, while at the fine scale, lowland unimproved grasslands, the main foraging habitat of P. austriacus, played a pivotal role in promoting genetic connectivity. Main conclusions: the importance of lowland unimproved grasslands in determining the biogeography and genetic connectivity in P. austriacus highlights the importance of their conservation as part of a wider landscape management for fragmented edge populations. This study illustrates the value of using SDMs in landscape genetics and highlights the need for multiscale approaches when studying genetic connectivity in volant animals or taxa with similar dispersal abilities.
Abstract.
Hope PR, Bohmann K, Gilbert MTP, Zepeda-Mendoza ML, Razgour O, Jones G (2014). Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera, Vespertilionidae) in winter.
Front Zool,
11Abstract:
Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera, Vespertilionidae) in winter.
BACKGROUND: Temperate winters produce extreme energetic challenges for small insectivorous mammals. Some bat species inhabiting locations with mild temperate winters forage during brief inter-torpor normothermic periods of activity. However, the winter diet of bats in mild temperate locations is studied infrequently. Although microscopic analyses of faeces have traditionally been used to characterise bat diet, recently the coupling of PCR with second generation sequencing has offered the potential to further advance our understanding of animal dietary composition and foraging behaviour by allowing identification of a much greater proportion of prey items often with increased taxonomic resolution. We used morphological analysis and Illumina-based second generation sequencing to study the winter diet of Natterer's bat (Myotis nattereri) and compared the results obtained from these two approaches. For the first time, we demonstrate the applicability of the Illumina MiSeq platform as a data generation source for bat dietary analyses. RESULTS: Faecal pellets collected from a hibernation site in southern England during two winters (December-March 2009-10 and 2010-11), indicated that M. nattereri forages throughout winter at least in a location with a mild winter climate. Through morphological analysis, arthropod fragments from seven taxonomic orders were identified. A high proportion of these was non-volant (67.9% of faecal pellets) and unexpectedly included many lepidopteran larvae. Molecular analysis identified 43 prey species from six taxonomic orders and confirmed the frequent presence of lepidopteran species that overwinter as larvae. CONCLUSIONS: the winter diet of M. nattereri is substantially different from other times of the year confirming that this species has a wide and adaptable dietary niche. Comparison of DNA derived from the prey to an extensive reference dataset of potential prey barcode sequences permitted fine scale taxonomic resolution of prey species. The high occurrence of non-volant prey suggests that gleaning allows prey capture at low ambient temperatures when the abundance of flying insects may be substantially reduced. Interesting questions arise as to how M. nattereri might successfully locate and capture some of the non-volant prey species encountered in its faeces. The consumption of lepidopteran larvae such as cutworms suggests that M. nattereri eats agricultural pest species.
Abstract.
Author URL.
Razgour O, Juste J, Ibáñez C, Kiefer A, Rebelo H, Puechmaille SJ, Arlettaz R, Burke T, Dawson DA, Beaumont M, et al (2013). The shaping of genetic variation in edge-of-range populations under past and future climate change.
Ecol Lett,
16(10), 1258-1266.
Abstract:
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.
Abstract.
Author URL.
Razgour O, Korine C, Saltz D (2011). Does interspecific competition drive patterns of habitat use in desert bat communities?.
Oecologia,
167(2), 493-502.
Abstract:
Does interspecific competition drive patterns of habitat use in desert bat communities?
Bodies of water are a key foraging habitat for insectivorous bats. Since water is a scarce and limiting resource in arid environments, bodies of open water may have a structuring effect on desert bat communities, resulting in temporal or spatial partitioning of bat activity. Using acoustic monitoring, we studied the spatial and temporal activity patterns of insectivorous bats over desert ponds, and hypothesised that sympatric bat species partition the foraging space above ponds based on interspecific competitive interactions. We used indirect measures of competition (niche overlap and competition coefficients from the regression method) and tested for differences in pond habitat selection and peak activity time over ponds. We examined the effect of changes in the activity of bat species on their potential competitors. We found that interspecific competition affects bat community structure and activity patterns. Competing species partitioned their use of ponds spatially, whereby each species was associated with different pond size and hydroperiod (the number of months a pond holds water) categories, as well as temporally, whereby their activity peaked at different hours of the night. The drying out of temporary ponds increased temporal partitioning over permanent ponds. Differences in the activity of species over ponds in response to the presence or absence of their competitors lend further support to the role of interspecific competition in structuring desert bat communities. We suggest that habitat use and night activity pattern of insectivorous bats in arid environments reflect the trade-offs between selection of preferred pond type or activity time and constraints posed by competitive interactions. © 2011 Springer-Verlag.
Abstract.
Razgour O, Clare EL, Zeale MRK, Hanmer J, Schnell IB, Rasmussen M, Gilbert TP, Jones G (2011). High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species.
Ecol Evol,
1(4), 556-570.
Abstract:
High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species.
Sympatric cryptic species, characterized by low morphological differentiation, pose a challenge to understanding the role of interspecific competition in structuring ecological communities. We used traditional (morphological) and novel molecular methods of diet analysis to study the diet of two cryptic bat species that are sympatric in southern England (Plecotus austriacus and P. auritus) (Fig. 1). Using Roche FLX 454 (Roche, Basel, CH) high-throughput sequencing (HTS) and uniquely tagged generic arthropod primers, we identified 142 prey Molecular Operational Taxonomic Units (MOTUs) in the diet of the cryptic bats, 60% of which were assigned to a likely species or genus. The findings from the molecular study supported the results of microscopic analyses in showing that the diets of both species were dominated by lepidopterans. However, HTS provided a sufficiently high resolution of prey identification to determine fine-scale differences in resource use. Although both bat species appeared to have a generalist diet, eared-moths from the family Noctuidae were the main prey consumed. Interspecific niche overlap was greater than expected by chance (O(jk) = 0.72, P < 0.001) due to overlap in the consumption of the more common prey species. Yet, habitat associations of nongeneralist prey species found in the diets corresponded to those of their respective bat predator (grasslands for P. austriacus, and woodland for P. auritus). Overlap in common dietary resource use combined with differential specialist prey habitat associations suggests that habitat partitioning is the primary mechanism of coexistence. The performance of HTS is discussed in relation to previous methods of molecular and morphological diet analysis. By enabling species-level identification of dietary components, the application of DNA sequencing to diet analysis allows a more comprehensive comparison of the diet of sympatric cryptic species, and therefore can be an important tool for determining fine-scale mechanisms of coexistence.
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Author URL.
Razgour O, Hanmer J, Jones G (2011). Using multi-scale modelling to predict habitat suitability for species of conservation concern: the grey long-eared bat as a case study. Biological Conservation, 144(12), 2922-2930.
Razgour O, Korine C, Saltz D (2010). Pond characteristics as determinants of species diversity and community composition in desert bats. Animal Conservation, 13(5), 505-513.
Chapters
Razgour O (2020). Plecotus austriacus Species Complex (P. austriacus, P. kolombatovici, P. gaisleri, P. teneriffae). In Hackländer K, Zachos F (Eds.)
Handbook of the Mammals of Europe, Springer.
Abstract:
Plecotus austriacus Species Complex (P. austriacus, P. kolombatovici, P. gaisleri, P. teneriffae)
Abstract.
Publications by year
In Press
Novella-Fernandez R, Juste J, Ibáñez C, Rebelo H, Russo D, Alberdi A, Kiefer A, Graham L, Paul H, Doncaster CP, et al (In Press). Broad-scale patterns of geographic avoidance between species emerge in the absence of fine-scale mechanisms of coexistence. Diversity and Distributions: a journal of conservation biogeography
Alberdi A, Razgour O, Aizpurua O, Novella-Fernandez R, Aihartza J, Budinski I, Garin I, Ibáñez C, Izagirre E, Rebelo H, et al (In Press). Diet diversification shapes broad-scale distribution patterns in European bats.
Abstract:
Diet diversification shapes broad-scale distribution patterns in European bats
AbstractLarge-scale species’ distributions have been traditionally attributed to physiological traits related to abiotic factors, while behavioural features linked to biotic interactions have received little attention. We tested the relationship between trophic and spatial niche breadths through combining species distribution modelling with dietary DNA metabarcoding of over 400 bats sampled across Europe belonging to seven species. Our results point to a causality cascade between hunting plasticity, trophic niche breadth and spatial niche breadth, and thus indicate that behavioral plasticity and dietary diversification can contribute to shaping broad-scale species distributions.
Abstract.
Razgour O (In Press). Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition.
Biological ReviewsAbstract:
Global genetic diversity status and trends: towards a suite of Essential Biodiversity Variables (EBVs) for genetic composition
Biodiversity underlies ecosystem resilience, ecosystem function, sustainable economies, and human well-being. Understanding how biodiversity sustains ecosystems under anthropogenic stressors and global environmental change will require new ways of deriving and applying biodiversity data. A major challenge is that biodiversity data and knowledge are scattered, biased, collected with numerous methods, and stored in inconsistent ways. The Group on Earth Observations Biodiversity Observation Network (GEO BON) has developed the Essential Biodiversity Variables (EBVs) as fundamental metrics to help aggregate, harmonize and interpret biodiversity observation data from diverse sources. Mapping and analysing EBVs can help to evaluate how aspects of biodiversity are distributed geographically and how they change over time. EBVs are also intended to serve as inputs and validation to forecast the status and trends of biodiversity, and to support policy and decision making. Here, we assess the feasibility of implementing Genetic Composition EBVs (Genetic EBVs), which are metrics of within-species genetic variation. We review and bring together numerous areas of the field of genetics and evaluate how each contributes to global and regional genetic biodiversity monitoring with respect to theory, sampling logistics, metadata, archiving, data aggregation, modelling, and technological advances. We propose four Genetic EBVs: (1) genetic diversity; (2) genetic differentiation; (3) inbreeding; and (4) effective population size (Ne). We rank Genetic EBVs according to their relevance, sensitivity to change, generalizability, scalability, feasibility and data availability. We outline the workflow for generating genetic data underlying the Genetic EBVs, and review advances and needs in archiving genetic composition data and metadata. We discuss how Genetic EBVs can be operationalized by visualizing EBVs in space and time across species and by forecasting Genetic EBVs beyond current observations using various modelling approaches. Our review then explores challenges of aggregation, standardization, and costs of operationalizing the Genetic EBVs, as well as future directions and opportunities to maximize their uptake globally in research and policy. The collection, annotation, and availability of genetic data has made major advances in the past decade, each of which contributes to the practical and standardized framework for large-scale genetic observation reporting. Rapid advances in DNA sequencing technology present new opportunities, but also challenges for operationalizing Genetic EBVs for biodiversity monitoring regionally and globally. With these advances, genetic composition monitoring is starting to be integrated into global conservation policy, which can help support the foundation of all biodiversity and species’ long-term persistence in the face of environmental change. We conclude with a summary of concrete steps for researchers and policy makers for advancing operationalization of Genetic EBVs. The technical and analytical foundations of Genetic EBVs are well developed, and conservation practitioners should anticipate their increasing application as efforts emerge to scale up genetic biodiversity monitoring regionally and globally.
Abstract.
Moraes B, Razgour O, Souza- Alves JP, Boubli J, Bezerra B (In Press). Habitat suitability for primate conservation in
north-east Brazil. Oryx: journal of fauna and flora international
Novella-Fernandez R, Ibañez C, Juste J, Clare EL, Doncaster CP, Razgour O (In Press). Trophic resource partitioning drives fine-scale coexistence in cryptic bat species. Ecology and Evolution
Horta P, Raposeira H, Vaz AS, António J, Juste J, Razgour O, Rebelo H (In Press). What about Adaptive Introgression? the Genomic Revolution is Shaping Scientific and Public Perception.
Abstract:
What about Adaptive Introgression? the Genomic Revolution is Shaping Scientific and Public Perception
Abstract
. Genetic miscegenation was historically perceived as a maladaptive process or even an imperfection of nature. However, through adaptive introgression, some species can share genes associated with well-adapted traits. Current scientific perceptions on the benefits of adaptive introgression can help to clarify how these paradoxes condition scientific progress and influence public beliefs and decision-making. We carried out a systematic review and bibliometric analysis using artificial intelligence on adaptive introgression evidence. The genomic revolution provided an exponential growing of evidence predominately interpreted as beneficial for species adaptation. We show that this remarkable increase on publications influences public perception in the medium-long term. Despite an initially emotional response, peoples’ final opinion tends to incorporate science-based evidence, although prejudices seem to influence peoples’ polarity opinion. We argue that developing the knowledge on adaptive introgression will allow to scientifically refute theories that promote genetic “purity”, used to justify racism and other forms of discrimination.
Abstract.
2022
Festa F, Ancillotto L, Santini L, Pacifici M, Rocha R, Toshkova N, Amorim F, Benitez-Lopez A, Domer A, Hamidovic D, et al (2022). Bat responses to climate change: a systematic review.
BIOLOGICAL REVIEWS Author URL.
Horta P, Raposeira H, Baños A, Ibáñez C, Razgour O, Rebelo H, Juste J (2022). Counteracting forces of introgressive hybridization and interspecific competition shape the morphological traits of cryptic Iberian Eptesicus bats.
Scientific Reports,
12(1).
Abstract:
Counteracting forces of introgressive hybridization and interspecific competition shape the morphological traits of cryptic Iberian Eptesicus bats
AbstractCryptic species that coexist in sympatry are likely to simultaneously experience strong competition and hybridization. The first phenomenon would lead to character displacement, whereas the second can potentially promote morphological similarity through adaptive introgression. The main goal of this work was to investigate the effect of introgressive hybridization on the morphology of cryptic Iberian Eptesicus bats when facing counteracting evolutionary forces from interspecific competition. We found substantial overlap both in dentition and in wing morphology traits, though mainly in individuals in sympatry. The presence of hybrids contributes to a fifth of this overlap, with hybrids showing traits with intermediate morphometry. Thus, introgressive hybridization may contribute to species adaptation to trophic and ecological space responding directly to the macro-habitats characteristics of the sympatric zone and to local prey availability. On the other hand, fur shade tended to be browner and brighter in hybrids than parental species. Colour differences could result from partitioning of resources as an adaptation to environmental factors such as roost and microhabitats. We argue that a balance between adaptive introgression and niche partitioning shapes species interactions with the environment through affecting morphological traits under selection.
Abstract.
Bhalla IS, Razgour O, Rigal F, Whittaker RJ (2022). Landscape features drive insectivorous bat activity in Indian rice fields.
Novella-Fernandez R, Juste J, Ibañez C, Nogueras J, Osborne PE, Razgour O (2022). The role of forest structure and composition in driving the distribution of bats in Mediterranean regions.
Scientific Reports,
12(1).
Abstract:
The role of forest structure and composition in driving the distribution of bats in Mediterranean regions
AbstractForests are key native habitats in temperate environments. While their structure and composition contribute to shaping local-scale community assembly, their role in driving larger-scale species distributions is understudied. We used detailed forest inventory data, an extensive dataset of occurrence records, and species distribution models integrated with a functional approach, to disentangle mechanistically how species-forest dependency processes drive the regional-scale distributions of nine forest specialist bats in a Mediterranean region in the south of Spain. The regional distribution patterns of forest bats were driven primarily by forest composition and structure rather than by climate. Bat roosting ecology was a key trait explaining the strength of the bat-forest dependency relationships. Tree roosting bats were strongly associated with mature and heterogeneous forest with large trees (diameters > 425 mm). Conversely, and contrary to what local-scale studies show, our results did not support that flight-related traits (wing loading and aspect ratio) drive species distributional patterns. Mediterranean forests are expected to be severely impacted by climate change. This study highlights the utility of disentangling species-environment relationships mechanistically and stresses the need to account for species-forest dependency relationships when assessing the vulnerability of forest specialists towards climate change.
Abstract.
2021
Horta P, Raposeira H, Baños A, Ibáñez C, Razgour O, Rebelo H, Juste J (2021). Counteracting Forces of Introgressive Hybridization and Interspecific Competition Shape the Morphological Traits of Cryptic Lberian Eptesicus Bats.
Riley J, Zeale MRK, Razgour O, Turpin J, Jones G (2021). Predicting the past, present and future distributions of an endangered marsupial in a semi‐arid environment. Animal Conservation, 24(5), 890-903.
Aizpurua O, Nyholm L, Morris E, Chaverri G, Montalvo LGH, Flores-Martinez JJ, Lin A, Razgour O, Gilbert MTP, Alberdi A, et al (2021). The role of the gut microbiota in the dietary niche expansion of fishing bats.
Aizpurua O, Nyholm L, Morris E, Chaverri G, Herrera Montalvo LG, Flores-Martinez JJ, Lin A, Razgour O, Gilbert MTP, Alberdi A, et al (2021). The role of the gut microbiota in the dietary niche expansion of fishing bats.
Animal Microbiome,
3(1).
Abstract:
The role of the gut microbiota in the dietary niche expansion of fishing bats
Abstract
. Background
. Due to its central role in animal nutrition, the gut microbiota is likely a relevant factor shaping dietary niche shifts. We analysed both the impact and contribution of the gut microbiota to the dietary niche expansion of the only four bat species that have incorporated fish into their primarily arthropodophage diet.
.
. Results
. We first compared the taxonomic and functional features of the gut microbiota of the four piscivorous bats to that of 11 strictly arthropodophagous species using 16S rRNA targeted amplicon sequencing. Second, we increased the resolution of our analyses for one of the piscivorous bat species, namely Myotis capaccinii, and analysed multiple populations combining targeted approaches with shotgun sequencing. To better understand the origin of gut microorganisms, we also analysed the gut microbiota of their fish prey (Gambusia holbrooki). Our analyses showed that piscivorous bats carry a characteristic gut microbiota that differs from that of their strict arthropodophagous counterparts, in which the most relevant bacteria have been directly acquired from their fish prey. This characteristic microbiota exhibits enrichment of genes involved in vitamin biosynthesis, as well as complex carbohydrate and lipid metabolism, likely providing their hosts with an enhanced capacity to metabolise the glycosphingolipids and long-chain fatty acids that are particularly abundant in fish.
.
. Conclusions
. Our results depict the gut microbiota as a relevant element in facilitating the dietary transition from arthropodophagy to piscivory.
.
Abstract.
2020
Rocha R, Aziz SA, Brook CE, Carvalho WD, Cooper‐Bohannon R, Frick WF, Huang JC, Kingston T, López‐Baucells A, Maas B, et al (2020). Bat conservation and zoonotic disease risk: a research agenda to prevent misguided persecution in the aftermath of COVID‐19. Animal Conservation, 24(3), 303-307.
Alberdi A, Razgour O, Aizpurua O, Novella-Fernandez R, Aihartza J, Budinski I, Garin I, Ibanez C, Izagirre E, Rebelo H, et al (2020). DNA metabarcoding and spatial modelling link diet diversification with distribution homogeneity in European bats. Nature Communications, 11
White R, Razgour O (2020). Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review, 50, 336-352.
Razgour O (2020). Plecotus austriacus Species Complex (P. austriacus, P. kolombatovici, P. gaisleri, P. teneriffae). In Hackländer K, Zachos F (Eds.)
Handbook of the Mammals of Europe, Springer.
Abstract:
Plecotus austriacus Species Complex (P. austriacus, P. kolombatovici, P. gaisleri, P. teneriffae)
Abstract.
Fernandez RN, ez CI, Juste J, Clare B, Doncaster CP, Razgour O (2020). Trophic resource partitioning drives fine-scale coexistence in cryptic bat species.
Razgour O, Kasso M, Santos H, Juste J (2020). Up in the air: threats to Afromontane biodiversity from climate change and habitat loss revealed by genetic monitoring of the Ethiopian Highlands bat. Evolutionary Applications: evolutionary approaches to environmental, biomedical and socio-economic issues, 14, 794-806.
Razgour O, Kasso M, Santos H, Juste J (2020). Up in the air: threats to Afromontane biodiversity from climate change and habitat loss revealed by modelling and landscape genetics of the Ethiopian Highlands long-eared bat.
2019
Centeno‐Cuadros A, Razgour O, García‐Mudarra JL, Mingo‐Casas P, Sandonís V, Redondo A, Ibáñez C, Paz O, Martinez‐Alós S, Pérez Suarez G, et al (2019). Comparative phylogeography and asymmetric hybridization between cryptic bat species. Journal of Zoological Systematics and Evolutionary Research, 57(4), 1004-1018.
Razgour O, Forester B, Taggart JB, Bekaert M, Juste J, Ibáñez C, Puechmaille SJ, Novella-Fernandez R, Alberdi A, Manel S, et al (2019). Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections.
Proceedings of the National Academy of Sciences,
116(21), 10418-10423.
Abstract:
Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections
Local adaptations can determine the potential of populations to respond to environmental changes, yet adaptive genetic variation is commonly ignored in models forecasting species vulnerability and biogeographical shifts under future climate change. Here we integrate genomic and ecological modeling approaches to identify genetic adaptations associated with climate in two cryptic forest bats. We then incorporate this information directly into forecasts of range changes under future climate change and assessment of population persistence through the spread of climate-adaptive genetic variation (evolutionary rescue potential). Considering climate-adaptive potential reduced range loss projections, suggesting that failure to account for intraspecific variability can result in overestimation of future losses. On the other hand, range overlap between species was projected to increase, indicating that interspecific competition is likely to play an important role in limiting species’ future ranges. We show that although evolutionary rescue is possible, it depends on a population’s adaptive capacity and connectivity. Hence, we stress the importance of incorporating genomic data and landscape connectivity in climate change vulnerability assessments and conservation management.
Abstract.
Amorim F, Razgour O, Mata VA, Lopes S, Godinho R, Ibáñez C, Juste J, Rossiter SJ, Beja P, Rebelo H, et al (2019). Evolutionary history of the European free‐tailed bat, a tropical affinity species spanning across the Mediterranean Basin. Journal of Zoological Systematics and Evolutionary Research, 58(1), 499-518.
2018
Razgour O, Taggart JB, Manel S, Juste J, Ibáñez C, Rebelo H, Alberdi A, Jones G, Park K (2018). An integrated framework to identify wildlife populations under threat from climate change.
Mol Ecol Resour,
18(1), 18-31.
Abstract:
An integrated framework to identify wildlife populations under threat from climate change.
Climate change is a major threat to global biodiversity that will produce a range of new selection pressures. Understanding species responses to climate change requires an interdisciplinary perspective, combining ecological, molecular and environmental approaches. We propose an applied integrated framework to identify populations under threat from climate change based on their extent of exposure, inherent sensitivity due to adaptive and neutral genetic variation and range shift potential. We consider intraspecific vulnerability and population-level responses, an important but often neglected conservation research priority. We demonstrate how this framework can be applied to vertebrates with limited dispersal abilities using empirical data for the bat Plecotus austriacus. We use ecological niche modelling and environmental dissimilarity analysis to locate areas at high risk of exposure to future changes. Combining outlier tests with genotype-environment association analysis, we identify potential climate-adaptive SNPs in our genomic data set and differences in the frequency of adaptive and neutral variation between populations. We assess landscape connectivity and show that changing environmental suitability may limit the future movement of individuals, thus affecting both the ability of populations to shift their distribution to climatically suitable areas and the probability of evolutionary rescue through the spread of adaptive genetic variation among populations. Therefore, a better understanding of movement ecology and landscape connectivity is needed for predicting population persistence under climate change. Our study highlights the importance of incorporating genomic data to determine sensitivity, adaptive potential and range shift potential, instead of relying solely on exposure to guide species vulnerability assessments and conservation planning.
Abstract.
Author URL.
Vasconcelos R, Razgour O, Tarroso P, Fasola M, Carranza S, Alves PC (2018). Combining molecular and landscape tools for targeting evolutionary processes in reserve design: an approach for islands. PLOS ONE, 13(7), e0200830-e0200830.
Razgour O, Persey M, Shamir U, Korine C (2018). The role of climate, water and biotic interactions in shaping biodiversity patterns in arid environments across spatial scales. Diversity and Distributions, 24(10), 1440-1452.
2016
Razgour O, Rebelo H, Di Febbraro M, Russo D (2016). Painting maps with bats: Species distribution modelling in bat research and conservation.
Hystrix,
27(1).
Abstract:
Painting maps with bats: Species distribution modelling in bat research and conservation
Species distribution models (SDMs) offer an effective tool for identifying species conservation requirements and forecasting how global environmental changes will affect species diversity and distribution. This approach is particularly relevant for bats because their nocturnal behaviour hinders detectability and identification in flight. Despite their important contribution to global biodiversity and wide geographical ranges, bats have been under-represented in early SDM studies, and only in the last few years has this approach become more widely used in bat research. We carried out a meta-analysis of the published literature to review the history of the use of SDMs in bat research and their application in conservation, climate change assessments and genetic studies. We focus on the geographical coverage, theme and modelling algorithm of published studies, and compare studies that are uniquely dedicated to bats to multi-taxa studies that include bats. We provide recommendations for good modelling practices through considering spatial scale and spatial biases, selecting ecologically relevant variables, following rigorous modelling protocols, and recognising the limitations of extrapolation across temporal scales. We suggest future developments that will further favour the use of SDMs to study bat ecology and biogeography, as well as inform conservation management. We conclude that despite an increase in bat SDM studies, their scope and application can be further enhanced through incorporating dispersal, landscape connectivity and biotic interactions between bats, their prey and their pathogens.
Abstract.
Jones M, Bertola LD, Razgour O (2016). Predicting the effect of interspecific competition on habitat suitability for the endangered african wild dog under future climate and land cover changes.
Hystrix,
27(1).
Abstract:
Predicting the effect of interspecific competition on habitat suitability for the endangered african wild dog under future climate and land cover changes
Apex predators play an important role in regulating ecological interactions, and therefore their loss can affect biodiversity across trophic levels. Large carnivores have experienced substantial population and range declines across Africa, and future climate change is likely to amplify these threats. Hence it is important to understand how future environmental changes will affect their long-term habitat suitability and population persistence. This study aims to identify the factors limiting the distribution of the endangered African wild dog, Lycaon pictus, and determine how biotic interactions and changing climate and land cover will affect future range suitability. We use Species Distribution Models (SDMs) to predict the current and future distribution of suitable conditions for L. pictus and its dominant competitor Panthera leo. We show that range suitability for L. pictus is limited by climatic and land cover variables, as well as high niche and range overlap with P. leo. Although both species are predicted to experience range contractions under future climate change, L. pictus may benefit from release from the effect of interspecific competition in eastern and central parts of its range. Our study highlights the importance of including land cover variables with corresponding future projections and incorporating the effects of competing species when predicting the future distribution of species whose ranges are not solely limited by climate. We conclude that SDMs can help identify priority areas for the long-term conservation of large carnivores, and therefore should be used to inform adaptive conservation management in face of future climate change.
Abstract.
2015
Razgour O (2015). Beyond species distribution modeling: a landscape genetics approach to investigating range shifts under future climate change.
Ecological Informatics,
30, 250-256.
Abstract:
Beyond species distribution modeling: a landscape genetics approach to investigating range shifts under future climate change
Understanding how biodiversity will respond to future climate change is a major conservation and societal challenge. Climate change is predicted to force many species to shift their ranges in pursuit of suitable conditions. This study aims to use landscape genetics, the study of the effects of environmental heterogeneity on the spatial distribution of genetic variation, as a predictive tool to assess how species will shift their ranges to track climatic changes and inform conservation measures that will facilitate movement. The approach is based on three steps: 1) using species distribution models (SDMs) to predict suitable ranges under future climate change, 2) using the landscape genetics framework to identify landscape variables that impede or facilitate movement, and 3) extrapolating the effect of landscape connectivity on range shifts in response to future climate change. I show how this approach can be implemented using the publicly available genetic dataset of the grey long-eared bat, Plecotus austriacus, in the Iberian Peninsula. Forest cover gradient was the main landscape variable affecting genetic connectivity between colonies. Forest availability is likely to limit future range shifts in response to climate change, primarily over the central plateau, but important range shift pathways have been identified along the eastern and western coasts. I provide outputs that can be directly used by conservation managers and review the viability of the approach. Using landscape genetics as a predictive tool in combination with SDMs enables the identification of potential pathways, whose loss can affect the ability of species to shift their range into future climatically suitable areas, and the appropriate conservation management measures to increase landscape connectivity and facilitate movement.
Abstract.
Alberdi A, Gilbert MTP, Razgour O, Aizpurua O, Aihartza J, Garin I (2015). Contrasting population-level responses to Pleistocene climatic oscillations in an alpine bat revealed by complete mitochondrial genomes and evolutionary history inference.
Journal of Biogeography,
42(9), 1689-1700.
Abstract:
Contrasting population-level responses to Pleistocene climatic oscillations in an alpine bat revealed by complete mitochondrial genomes and evolutionary history inference
Aim: We used an integrative approach to reconstruct the evolutionary history of the alpine long-eared bat, Plecotus macrobullaris, to test whether the variable effects of Pleistocene climatic oscillations across geographical regions led to contrasting population-level demographic histories within a single species. Location: the Western Palaearctic. Methods: We sequenced the complete mitochondrial genomes of 57 individuals from across the distribution of the species. The analysis integrated ecological niche modelling (ENM), approximate Bayesian computation (ABC), measures of genetic diversity and Bayesian phylogenetic methods. Results: We identified two deep lineages: a western lineage, restricted to the Pyrenees and the Alps, and an eastern lineage, which expanded across the mountain ranges east of the Dinarides (Croatia). ENM projections of past conditions predicted that climatic suitability was reduced during cold stages in the areas inhabited by the western lineage, while the opposite trend was observed in the mountains inhabited by the eastern lineage. The palaeodemographic scenario that best fitted our data is consistent with the western lineage population size having shrunk repeatedly because of the extensive glaciation events that occurred in the Alps and Pyrenees during the Pleistocene. In contrast, the eastern lineage maintained a constant population size as is consistent with more limited glaciation in the mountains of south-eastern Europe and the Middle East. Main conclusions: This study shows that the demographic response of populations to Pleistocene climatic oscillations depended on their geographical location, offering an example of population-level variations in the effects and long-term consequences of climate change.
Abstract.
Razgour O, Salicini I, Ibáñez C, Randi E, Juste J (2015). Unravelling the evolutionary history and future prospects of endemic species restricted to former glacial refugia.
Molecular Ecology,
24(20), 5267-5283.
Abstract:
Unravelling the evolutionary history and future prospects of endemic species restricted to former glacial refugia
The contemporary distribution and genetic composition of biodiversity bear a signature of species' evolutionary histories and the effects of past climatic oscillations. For many European species, the Mediterranean peninsulas of Iberia, Italy and the Balkans acted as glacial refugia and the source of range recolonization, and as a result, they contain disproportionately high levels of diversity. As these areas are particularly threatened by future climate change, it is important to understand how past climatic changes affected their biodiversity. We use an integrated approach, combining markers with different evolutionary rates and combining phylogenetic analysis with approximate Bayesian computation and species distribution modelling across temporal scales. We relate phylogeographic processes to patterns of genetic variation in Myotis escalerai, a bat species endemic to the Iberian Peninsula. We found a distinct population structure at the mitochondrial level with a strong geographic signature, indicating lineage divergence into separate glacial refugia within the Iberian refugium. However, microsatellite markers suggest higher levels of gene flow resulting in more limited structure at recent time frames. The evolutionary history of M. escalerai was shaped by the effects of climatic oscillations and changes in forest cover and composition, while its future is threatened by climatically induced range contractions and the role of ecological barriers due to competition interactions in restricting its distribution. This study warns that Mediterranean peninsulas, which provided refuge for European biodiversity during past glaciation events, may become a trap for limited dispersal and ecologically limited endemic species under future climate change, resulting in loss of entire lineages.
Abstract.
2014
Razgour O, Rebelo H, Puechmaille SJ, Juste J, Ibáñez C, Kiefer A, Burke T, Dawson DA, Jones G (2014). Scale-dependent effects of landscape variables on gene flow and population structure in bats.
Diversity and Distributions,
20(10), 1173-1185.
Abstract:
Scale-dependent effects of landscape variables on gene flow and population structure in bats
Aim: a common pattern in biogeography is the scale-dependent effect of environmental variables on the spatial distribution of species. We tested the role of climatic and land cover variables in structuring the distribution of genetic variation in the grey long-eared bat, Plecotus austriacus, across spatial scales. Although landscape genetics has been widely used to describe spatial patterns of gene flow in a variety of taxa, volant animals have generally been neglected because of their perceived high dispersal potential. Location: England and Europe. Methods: We used a multiscale integrated approach, combining population genetics with species distribution modelling and geographical information under a causal modelling framework, to identify landscape barriers to gene flow and their effect on population structure and conservation status. Genotyping involved 23 polymorphic microsatellites and 259 samples from across the species' range. Results: We identified distinct population structure shaped by geographical barriers and evidence of population fragmentation at the northern edge of the range. Habitat suitability (as captured by species distribution models, SDMs) was the most important landscape variable affecting genetic connectivity at the broad spatial scale, while at the fine scale, lowland unimproved grasslands, the main foraging habitat of P. austriacus, played a pivotal role in promoting genetic connectivity. Main conclusions: the importance of lowland unimproved grasslands in determining the biogeography and genetic connectivity in P. austriacus highlights the importance of their conservation as part of a wider landscape management for fragmented edge populations. This study illustrates the value of using SDMs in landscape genetics and highlights the need for multiscale approaches when studying genetic connectivity in volant animals or taxa with similar dispersal abilities.
Abstract.
Hope PR, Bohmann K, Gilbert MTP, Zepeda-Mendoza ML, Razgour O, Jones G (2014). Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera, Vespertilionidae) in winter.
Front Zool,
11Abstract:
Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera, Vespertilionidae) in winter.
BACKGROUND: Temperate winters produce extreme energetic challenges for small insectivorous mammals. Some bat species inhabiting locations with mild temperate winters forage during brief inter-torpor normothermic periods of activity. However, the winter diet of bats in mild temperate locations is studied infrequently. Although microscopic analyses of faeces have traditionally been used to characterise bat diet, recently the coupling of PCR with second generation sequencing has offered the potential to further advance our understanding of animal dietary composition and foraging behaviour by allowing identification of a much greater proportion of prey items often with increased taxonomic resolution. We used morphological analysis and Illumina-based second generation sequencing to study the winter diet of Natterer's bat (Myotis nattereri) and compared the results obtained from these two approaches. For the first time, we demonstrate the applicability of the Illumina MiSeq platform as a data generation source for bat dietary analyses. RESULTS: Faecal pellets collected from a hibernation site in southern England during two winters (December-March 2009-10 and 2010-11), indicated that M. nattereri forages throughout winter at least in a location with a mild winter climate. Through morphological analysis, arthropod fragments from seven taxonomic orders were identified. A high proportion of these was non-volant (67.9% of faecal pellets) and unexpectedly included many lepidopteran larvae. Molecular analysis identified 43 prey species from six taxonomic orders and confirmed the frequent presence of lepidopteran species that overwinter as larvae. CONCLUSIONS: the winter diet of M. nattereri is substantially different from other times of the year confirming that this species has a wide and adaptable dietary niche. Comparison of DNA derived from the prey to an extensive reference dataset of potential prey barcode sequences permitted fine scale taxonomic resolution of prey species. The high occurrence of non-volant prey suggests that gleaning allows prey capture at low ambient temperatures when the abundance of flying insects may be substantially reduced. Interesting questions arise as to how M. nattereri might successfully locate and capture some of the non-volant prey species encountered in its faeces. The consumption of lepidopteran larvae such as cutworms suggests that M. nattereri eats agricultural pest species.
Abstract.
Author URL.
2013
Razgour O, Juste J, Ibáñez C, Kiefer A, Rebelo H, Puechmaille SJ, Arlettaz R, Burke T, Dawson DA, Beaumont M, et al (2013). The shaping of genetic variation in edge-of-range populations under past and future climate change.
Ecol Lett,
16(10), 1258-1266.
Abstract:
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.
Abstract.
Author URL.
2011
Razgour O, Korine C, Saltz D (2011). Does interspecific competition drive patterns of habitat use in desert bat communities?.
Oecologia,
167(2), 493-502.
Abstract:
Does interspecific competition drive patterns of habitat use in desert bat communities?
Bodies of water are a key foraging habitat for insectivorous bats. Since water is a scarce and limiting resource in arid environments, bodies of open water may have a structuring effect on desert bat communities, resulting in temporal or spatial partitioning of bat activity. Using acoustic monitoring, we studied the spatial and temporal activity patterns of insectivorous bats over desert ponds, and hypothesised that sympatric bat species partition the foraging space above ponds based on interspecific competitive interactions. We used indirect measures of competition (niche overlap and competition coefficients from the regression method) and tested for differences in pond habitat selection and peak activity time over ponds. We examined the effect of changes in the activity of bat species on their potential competitors. We found that interspecific competition affects bat community structure and activity patterns. Competing species partitioned their use of ponds spatially, whereby each species was associated with different pond size and hydroperiod (the number of months a pond holds water) categories, as well as temporally, whereby their activity peaked at different hours of the night. The drying out of temporary ponds increased temporal partitioning over permanent ponds. Differences in the activity of species over ponds in response to the presence or absence of their competitors lend further support to the role of interspecific competition in structuring desert bat communities. We suggest that habitat use and night activity pattern of insectivorous bats in arid environments reflect the trade-offs between selection of preferred pond type or activity time and constraints posed by competitive interactions. © 2011 Springer-Verlag.
Abstract.
Razgour O, Clare EL, Zeale MRK, Hanmer J, Schnell IB, Rasmussen M, Gilbert TP, Jones G (2011). High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species.
Ecol Evol,
1(4), 556-570.
Abstract:
High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species.
Sympatric cryptic species, characterized by low morphological differentiation, pose a challenge to understanding the role of interspecific competition in structuring ecological communities. We used traditional (morphological) and novel molecular methods of diet analysis to study the diet of two cryptic bat species that are sympatric in southern England (Plecotus austriacus and P. auritus) (Fig. 1). Using Roche FLX 454 (Roche, Basel, CH) high-throughput sequencing (HTS) and uniquely tagged generic arthropod primers, we identified 142 prey Molecular Operational Taxonomic Units (MOTUs) in the diet of the cryptic bats, 60% of which were assigned to a likely species or genus. The findings from the molecular study supported the results of microscopic analyses in showing that the diets of both species were dominated by lepidopterans. However, HTS provided a sufficiently high resolution of prey identification to determine fine-scale differences in resource use. Although both bat species appeared to have a generalist diet, eared-moths from the family Noctuidae were the main prey consumed. Interspecific niche overlap was greater than expected by chance (O(jk) = 0.72, P < 0.001) due to overlap in the consumption of the more common prey species. Yet, habitat associations of nongeneralist prey species found in the diets corresponded to those of their respective bat predator (grasslands for P. austriacus, and woodland for P. auritus). Overlap in common dietary resource use combined with differential specialist prey habitat associations suggests that habitat partitioning is the primary mechanism of coexistence. The performance of HTS is discussed in relation to previous methods of molecular and morphological diet analysis. By enabling species-level identification of dietary components, the application of DNA sequencing to diet analysis allows a more comprehensive comparison of the diet of sympatric cryptic species, and therefore can be an important tool for determining fine-scale mechanisms of coexistence.
Abstract.
Author URL.
Razgour O, Hanmer J, Jones G (2011). Using multi-scale modelling to predict habitat suitability for species of conservation concern: the grey long-eared bat as a case study. Biological Conservation, 144(12), 2922-2930.
2010
Razgour O, Korine C, Saltz D (2010). Pond characteristics as determinants of species diversity and community composition in desert bats. Animal Conservation, 13(5), 505-513.
