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Research Interests: Phylogenetics, Archives, Biology, Medicine, Chiroptera, and 14 moreBiological Sciences, Phylogeny, Population, Humans, Animals, Phylogenetic analysis, Feces, Phylogenetic Tree, Severe Acute Respiratory Syndrome (SARS), Coronavirus, Molecular Sequence Data, Betacoronavirus, Severe Acute Respiratory Syndrome, and Medical and Health Sciences
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Lifespan is a fundamental demographic parameter that we can seldom measure in animals with elusive behaviour like bats. Even more useful parameters for modelling the life history are survival or reproduction by age and sex. However, in... more
Lifespan is a fundamental demographic parameter that we can seldom measure in animals with elusive behaviour like bats. Even more useful parameters for modelling the life history are survival or reproduction by age and sex. However, in practice there are substantial obstacles to achieve information of that kind and, regretfully, we often rely on longevity records. This paper provides new records on long-lived Rhinolophus euryale individuals, including one female more than 25 years old. We also discuss the evidentiary support for the widely accepted age at first reproduction in that species.
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Research Interests: Zoology, Geography, Chiroptera, Mammalia, Pyrenees, and 6 moreBats, Pyrénées, Iberian Peninsula, Summer, Pirineus, and Vespertilio murinus
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Research Interests: Evolutionary Biology, Geography, Earth Sciences, Phylogeography, Biology, and 13 moreBiogeography, Inference, Ecological Niche Modelling, Chiroptera, Historical Biogeography, Pleistocene, Biological Sciences, Environmental Sciences, Mitochondrial DNA, Population, Approximate Bayesian Computation, Europe, and Bayesian Phylogenetics
Traditionally, researchers have assessed diet selection by comparing consumed versus available taxa. However, taxonomic assignment is probably irrelevant for predators, who likely base their selection on characteristics including prey... more
Traditionally, researchers have assessed diet selection by comparing consumed versus available taxa. However, taxonomic assignment is probably irrelevant for predators, who likely base their selection on characteristics including prey size, habitat, or behavior. Here, we use an aquatic insectivore, the threatened Pyrenean Desman (Galemys pyrenaicus), as a model species to assess whether biological traits help unravel the criteria driving food and habitat preferences. We reanalyzed data from a previous taxonomy-based study of prey selection in two contrasting streams, one with excellent conservation status and the other affected by diversion for hydropower and forestry. Available and consumed prey were characterized according to nine biological traits, and diet selection was estimated by comparing availability—measured from Surber net samples, and consumption—analyzed by metabarcoding desman feces. Traits offered a biologically coherent image of diet and almost identical selection pa...
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Myotis emarginatus seems fond of spiders and flies, a unique feeding style among European bats. The importance of each prey type varies among studies, so this paper aims to expand on the knowledge to unveil the trophic niche of M.... more
Myotis emarginatus seems fond of spiders and flies, a unique feeding style among European bats. The importance of each prey type varies among studies, so this paper aims to expand on the knowledge to unveil the trophic niche of M. emarginatus by studying its diet changes throughout the maternity season. We sampled five maternity colonies in the Basque Country every 2 weeks for the whole duration of the maternity season and studied their diet using DNA metabarcoding methods. We observed significant changes in diet diversity and composition. At the beginning of the season, M. emarginatus consumed a variety of prey orders, Diptera being the most abundant; but as the season progressed, the relative consumption of Araneae increased. By August, 80% of the weighted percentage of occurrences (wPOO) corresponded to the orb-web-building spider Araneus diadematus. Orb-web-building spiders need habitats of high vertical complexity to grow in abundance. Therefore, conserving them is essential to...
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It includes all the sequences we got after amplyfied and massively sequenced bats' faecal DNA, excluding those with less than 15 copies, and those which didn't occur in both amplification replicas
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Includes all the MOTUs (and their sequences) built after filtering and bioinformatic processing the originary sequences got from amplifying and massive sequencing of bats' faecal DN
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Molecular analysis of diet overcomes the considerable limitations of traditional techniques for identifying prey remains in bat faeces. We collected faeces from individual Mountain long-eared bats Plecotus macrobullaris trapped using mist... more
Molecular analysis of diet overcomes the considerable limitations of traditional techniques for identifying prey remains in bat faeces. We collected faeces from individual Mountain long-eared bats Plecotus macrobullaris trapped using mist nets during the summers of 2009 and 2010 in the Pyrenees. We analysed their diet using DNA mini-barcodes to identify prey species. In addition, we inferred some basic features of the bat’s foraging ecology that had not yet been addressed. P. macrobullaris fed almost exclusively on moths (97.8%). As prey we detected one dipteran genus (Tipulidae) and 29 moth taxa: 28 were identified at species level (23 Noctuidae, 1 Crambidae, 1 Geometridae, 1 Pyralidae, 1 Sphingidae, 1 Tortricidae), and one at genus level (Rhyacia sp., Noctuidae). Known ecological information about the prey species allowed us to determine that bats had foraged at elevations between 1,500 and 2,500 m amsl (above mean sea level), mostly in subalpine meadows, followed by other open habitats such as orophilous grasslands and alpine meadows. No forest prey species were identified in the diet. As 96.4% of identified prey species were tympanate moths and no evidence of gleaning behaviour was revealed, we suggest P. macrobullaris probably forages by aerial hawking using faint echolocation pulses to avoid detection by hearing moths. As we could identify 87.8% of the analysed sequences (64.1% of the MOTUs, Molecular Operational Taxonomic Units) at species level, we conclude that DNA mini-barcodes are a very useful tool to analyse the diet of moth-specialist bats
Molecular techniques allow non-invasive dietary studies from faeces, providing an invaluable tool to unveil ecological requirements of endangered or elusive species. They contribute to progress on important issues such as genomics,... more
Molecular techniques allow non-invasive dietary studies from faeces, providing an invaluable tool to unveil ecological requirements of endangered or elusive species. They contribute to progress on important issues such as genomics, population genetics, dietary studies or reproductive analyses, essential knowledge for conservation biology. Nevertheless, these techniques require general methods to be tailored to the specific research objectives, as well as to substrate- and species-specific constraints. In this pilot study we test a range of available primers to optimise diet analysis from metabarcoding of faeces of a generalist aquatic insectivore, the endangered Pyrenean desman (Galemys pyrenaicus, É. Geoffroy Saint-Hilaire, 1811, Talpidae), as a step to improve the knowledge of the conservation biology of this species. Twenty-four faeces were collected in the field, DNA was extracted from them, and fragments of the standard barcode region (COI) were PCR amplified by using five primer sets (Brandon-Mong, Gillet, Leray, Meusnier and Zeale). PCR outputs were sequenced on the Illumina MiSeq platform, sequences were processed, clustered into OTUs (Operational Taxonomic Units) using UPARSE algorithm and BLASTed against the NCBI database. Although all primer sets successfully amplified their target fragments, they differed considerably in the amounts of sequence reads, rough OTUs, and taxonomically assigned OTUs. Primer sets consistently identified a few abundant prey taxa, probably representing the staple food of the Pyrenean desman. However, they differed in the less common prey groups. Overall, the combination of Gillet and Zeale primer sets were most cost-effective to identify the widest taxonomic range of prey as well as the desman itself, which could be further improved stepwise by adding sequentially the outputs of Leray, Brandon-Mong and Meusnier primers. These results are relevant for the conservation biology of this endangered species as they allow a better characterization of its food and habitat requirements
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Representative sequences for each MOT
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Acknowledgements This work was funded by the EU project LIFE IREKIBAI (LIFE14 NAT/ES/000186) and the Basque Government. Amaiur Esnaola enjoyed a predoctoral grant by the Basque Government. Authors are very thankful for Arturo Elosegi and... more
Acknowledgements This work was funded by the EU project LIFE IREKIBAI (LIFE14 NAT/ES/000186) and the Basque Government. Amaiur Esnaola enjoyed a predoctoral grant by the Basque Government. Authors are very thankful for Arturo Elosegi and Aitor Arrizabalaga for their assistance in making this work possible, and also for technical and human support provided by Secuencing and Genotyping Unit – Genomic Facilities – SGIker (UPV/EHU/ERDF, EU). Abstract
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Recent research has confirmed the efficiency of insectivorous bats as pest suppressors, underlining the ecological services they offer in agroecosystems. Therefore, some efforts try to enhance bat foraging in agricultural landscapes by... more
Recent research has confirmed the efficiency of insectivorous bats as pest suppressors, underlining the ecological services they offer in agroecosystems. Therefore, some efforts try to enhance bat foraging in agricultural landscapes by acting upon environmental factors favouring them. In this study, we monitored a Miniopterus schreibersii colony, in the southern Iberian Peninsula. We intensively sampled their faeces and analysed them by metabarcoding to describe how the bent-winged bat diet would change with time, and to test whether their most-consumed prey would seasonally depend on different landscapes or habitats. Our results confirm that M. schreibersii are selective opportunist predators of moths, dipterans, mayflies, and other fluttering insects, shifting their diet to temporary peaks of prey availability in their foraging range, including both pest and non-pest insects. Supporting our hypothesis, throughout the year, M. schreibersii consume insects linked to diverse open hab...
Ó The Author(s) 2011. This article is published with open access at Springerlink.com Abstract Bat coronaviruses (CoV) are putative precursors of the severe acute respiratory syndrome (SARS) CoV and other CoV that crossed the species... more
Ó The Author(s) 2011. This article is published with open access at Springerlink.com Abstract Bat coronaviruses (CoV) are putative precursors of the severe acute respiratory syndrome (SARS) CoV and other CoV that crossed the species barrier from zoonotic reservoirs into the human population. To determine the presence and distribution of CoV in Iberian bats, 576 individuals of 26 different bat species were captured in 13 locations in Spain. We report for the first time the presence of 14 coronaviruses in 9 Iberian bat species. Phylogenetic analysis of a conserved CoV genome region (RdRp gene) shows a wide diversity and distribution of alpha and betacoronavirus in Spain. Interestingly, although some of these viruses are related to other European BatCoV, or to Asian CoV, some of the viruses found in Spain cluster in new groups of a and b CoV. GenBank accession numbers: Partial sequences of RdRp gene of bat coronaviruses obtained in this study were deposited in GenBank under the accessi...
ABSTRACTRoosts are vital for the survival of many species, and how individuals choose one site over another is affected by various ecological factors. Biomechanical constraints could also affect roost selection, particularly in volant... more
ABSTRACTRoosts are vital for the survival of many species, and how individuals choose one site over another is affected by various ecological factors. Biomechanical constraints could also affect roost selection, particularly in volant taxa that require sites with easy access, thereby reducing costs (i.e., predation, accidents). To date, no studies have established an association between landing performance and roost-site selection, as predicted by biomechanical constraints associated with flight. We aim to determine roost-site selection in disc-winged bats (Thyroptera tricolor), a species known to roost within developing tubular leaves. This study is coupled with various experiments that measure how a conspicuous apex affects landing tactics and performance. We show that T. tricolor prefers leaves with a longer apex, the space typically used for landing. Bats also approach and enter these leaves more consistently, increasing task performance while reducing the risk of injuries.Summa...
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Lifespan is a fundamental demographic parameter that we can seldom measure in animals with elusive behaviour like bats. Even more useful parameters for modelling the life history are survival or reproduction by age and sex. However, in... more
Lifespan is a fundamental demographic parameter that we can seldom measure in animals with elusive behaviour like bats. Even more useful parameters for modelling the life history are survival or reproduction by age and sex. However, in practice there are substantial obstacles to achieve information of that kind and, regretfully, we often rely on longevity records. This paper provides new records on long-lived Rhinolophus euryale individuals, including one female more than 25 years old. We also discuss the evidentiary support for the widely accepted age at first reproduction in that species.
Fasta file of the OTUs built from mini-COI sequences got from bat faeces with Zeale primer
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1. The degree of trophic specialization determines the ability of predators to cope with changing foraging conditions, but in predators that prey on hundreds of species it is challenging to assess, especially when prey identity varies... more
1. The degree of trophic specialization determines the ability of predators to cope with changing foraging conditions, but in predators that prey on hundreds of species it is challenging to assess, especially when prey identity varies among predator individuals and across space and time. 2. Here, we test the hypothesis that a bat species foraging on flying insects like moths will show ample flexibility in trophic niche, and this irrespective of phylogenetic relationships among moths, so as to cope with a high diversity of prey types that vary across seasons. We predict that individual bats will show functional dietary differences consistent with energetic requirements and hunting skills. 3. We used DNA metabarcoding to determine the diet of 126 Mediterranean horseshoe bats (Rhinolophus euryale) from two different sites during three seasons. Simultaneously, we measured moth availability and characterized the traits of 290 moth taxa. Next, we explored the relationship between phylogeny and traits of all consumed and available moth taxa. Finally, we assessed the relationship between individual traits of bats and traits related to prey profitability, for which we used the RLQ and fourth-corner statistical techniques. 4. Seasonality was the main factor explaining the functional dietary variation in adult bats, with moths consumed irrespective of their phylogenetic relationships. While adults consumed moths with a broad range in wing loading, body mass and echolocation detection ability, juveniles consumed slower, smaller and lighter moths, which suggests that young individuals may undergo some fitness gain and/or psychomotor learning process during which they would acquire more effective foraging skills. 5. Our approach revealed a degree of functional flexibility in the trophic niche previously unknown for an insectivorous bat. R. euryale consumed a wide variety of moth taxa differing in profitability throughout seasons and between ontogenetic stages. We showed the validity of trait-based approaches to gain new insights in the trophic specialization of predators consuming hundreds of species of prey
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ZOTU sequences obtained from DNA extracted from faeces of Rhinolophus hipposideros in a vineyard system
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Presence/absence data matrix of bat individuals x MOTU
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Myotis emarginatus is one of the few bats known to feed mostly on spiders. In order to study the importance of this type of prey, we analysed the species’ diet in five colonies across the Iberian Peninsula using amplicon metabarcoding in... more
Myotis emarginatus is one of the few bats known to feed mostly on spiders. In order to study the importance of this type of prey, we analysed the species’ diet in five colonies across the Iberian Peninsula using amplicon metabarcoding in order to describe its composition at the species level, and analyse its geographic variability within the peninsula. We identified 138 prey species, belonging to 11 different arthropod orders. Among them, 45 species of spiders were identified, mostly of the orb-web building guild, as consumed by 82 out of 106 studied bats, corresponding to every colony and season sampled. Besides, lepidopterans and dipterans were also consumed in every colony. Among the latter, the stable fly Stomoxys calcitrans was especially important in two of the colonies, showing thatM. emarginatus can also opportunistically exploit different resources or foraging grounds, such as cattle sheds, which affects the composition of its diet also at ordinal level of prey.
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Outbreaks of the processionary moth Thaumetopoea pityocampa (Denis & Schiffermüller, 1775), a forest pest from the Palearctic, are thought to induce a behavioral response of bats, but up to now the moth has been seldom identified as bats’... more
Outbreaks of the processionary moth Thaumetopoea pityocampa (Denis & Schiffermüller, 1775), a forest pest from the Palearctic, are thought to induce a behavioral response of bats, but up to now the moth has been seldom identified as bats’ prey. Studies on bat diets suggest moths with cyclical outbreaks attract a wide array of bat species from different foraging guilds. We test whether bats feed upon T. pityocampa in the Iberian Peninsula irrespective of the predator’s ecological and morphological features. We found that seven out of ten bat species belonging to different foraging guilds contained T. pityocampa DNA in their faeces and no difference was found in the foraging frequency among foraging guilds. A different size of the typical prey or the lack of fondness for moths can explain the absence of the pest in some bat species. Moreover, the intraspecific foraging frequency of T. pityocampa also changed with the sampling site likely representing differential availability of the m...
Research Interests: Quality, Biology, Diet, Ecology, Medicine, and 8 moreLepidoptera, Canada, Population, Predation, Service, Flight, Pheromone, and Pine Forest
Inferences of the interactions between species’ ecological niches and spatial distribution have been historically based on simple metrics such as low-resolution dietary breadth and range size, which might have impeded the identification... more
Inferences of the interactions between species’ ecological niches and spatial distribution have been historically based on simple metrics such as low-resolution dietary breadth and range size, which might have impeded the identification of meaningful links between niche features and spatial patterns. We analysed the relationship between dietary niche breadth and spatial distribution features of European bats, by combining continent-wide DNA metabarcoding of faecal samples with species distribution modelling. Our results show that while range size is not correlated with dietary features of bats, the homogeneity of the spatial distribution of species exhibits a strong correlation with dietary breadth. We also found that dietary breadth is correlated with bats’ hunting flexibility. However, these two patterns only stand when the phylogenetic relations between prey are accounted for when measuring dietary breadth. Our results suggest that the capacity to exploit different prey types ena...
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There is growing evidence about the role of insectivorous bats against agricultural pests in various crops. Nevertheless, little research addressed the aggregational and functional responses of bat assemblages to changes in pest... more
There is growing evidence about the role of insectivorous bats against agricultural pests in various crops. Nevertheless, little research addressed the aggregational and functional responses of bat assemblages to changes in pest availability across a spatio-temporal scale. Therefore, we examined the activity and diet habits of different bat species using DNA metabarcoding by simultaneously monitoring the relative abundance of two major pests (the European grapevine moth, Lobesia botrana, and the leaf rolling tortrix, Sparganothis pilleriana) through the grape growing season, in a vineyard region of the Iberian Peninsula. During pest major irruptions, we found the highest bat activity levels and frequencies of grape pests in the diet of bats, although not all bat species contributed equally to pest suppression. Bats of different foraging guilds positively responded to pest abundances, indicating distinct bat species may synergistically play a role at suppressing agricultural pests at...
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Large-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... more
Large-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.
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1.The degree of trophic specialization determines the ability of predators to cope with changing foraging conditions, but in predators that prey on hundreds of species it is challenging to assess, especially when prey identity varies... more
1.The degree of trophic specialization determines the ability of predators to cope with changing foraging conditions, but in predators that prey on hundreds of species it is challenging to assess, especially when prey identity varies among predator individuals and across space and time. 2.Here, we test the hypothesis that a bat species foraging on flying insects like moths will show ample flexibility in trophic niche, and this irrespective of phylogenetic relationships among moths, so as to cope with a high diversity of prey types that vary across seasons. We predict that individual bats will show functional dietary differences consistent with energetic requirements and hunting skills. 3.We used DNA metabarcoding to determine the diet of 126 Mediterranean horseshoe bats (Rhinolophus euryale) from two different sites during three seasons. Simultaneously, we measured moth availability and characterized the traits of 290 moth taxa. Next, we explored the relationship between phylogeny and traits of all consumed and available moth taxa. Finally, we assessed the relationship between individual traits of bats and traits related to prey profitability, for which we used the RLQ and fourth-corner statistical techniques. 4.Seasonality was the main factor explaining the functional dietary variation in adult bats, with moths consumed irrespective of their phylogenetic relationships. While adults consumed moths with a broad range in wing loading, body mass and echolocation detection ability, juveniles consumed slower, smaller and lighter moths, which suggests that young individuals may undergo some fitness gain and/or psychomotor learning process during which they would acquire more effective foraging skills. 5.Our approach revealed a degree of functional flexibility in the trophic niche previously unknown for an insectivorous bat. R. euryale consumed a wide variety of moth taxa differing in profitability throughout seasons and between ontogenetic stages. We showed the validity of trait-based approaches to gain new insights in the trophic specialization of predators consuming hundreds of species of prey. This article is protected by copyright. All rights reserved.