Mitigating the impact of Bats in historic churches: The response of Natterer's Bats Myotis nattereri to artificial roosts and deterrence

© 2016 Zeale et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Bats frequently roost in historic churches, and these colonies are of considerable conservation value. Inside churches, bat droppings and urine can cause damage to the historic fabric of the building and to items of cultural significance. In extreme cases, large quantities of droppings can restrict the use of a church for worship and/or other community functions. In the United Kingdom, bats and their roosts are protected by law, and striking a balance between conserving the natural and cultural heritage can be a significant challenge. We investigated mitigation strategies that could be employed in churches and other historic buildings to alleviate problems caused by bats without adversely affecting their welfare or conservation status. We used a combination of artificial roost provision and deterrence at churches in Norfolk, England, where significant maternity colonies of Natterer's bats Myotis nattereri damage church features. Radio-tracking data and population modelling showed that excluding M. nattereri from churches is likely to have a negative impact on their welfare and conservation status, but that judicious use of deterrents, especially high intensity ultrasound, can mitigate problems caused by bats. We show that deterrence can be used to move bats humanely from specific roosting sites within a church and limit the spread of droppings and urine so that problems to congregations and damage to cultural heritage can be much reduced. In addition, construction of bespoke roost spaces within churches can allow bats to continue to roost within the fabric of the building without flying in the church interior. We highlight that deterrence has the potential to cause serious harm toM. nattereri populations if not used judiciously, and so the effects of deterrents will need careful monitoring, and their use needs strict regulation

Integrated Operational Taxonomic Units (IOTUs) in Echolocating Bats: A Bridge between Molecular and Traditional Taxonomy

Background: Nowadays, molecular techniques are widespread tools for the identification of biological entities. However, until very few years ago, their application to taxonomy provoked intense debates between traditional and molecular taxonomists. To prevent every kind of disagreement, it is essential to standardize taxonomic definitions. Along these lines, we introduced the concept of Integrated Operational Taxonomic Unit (IOTU). IOTUs come from the concept of Operational Taxonomic Unit (OTU) and paralleled the Molecular Operational Taxonomic Unit (MOTU). The latter is largely used as a standard in many molecular-based works (even if not always explicitly formalized). However, while MOTUs are assigned solely on molecular variation criteria, IOTUs are identified from patterns of molecular variation that are supported by at least one more taxonomic characteristic. Methodology/Principal Findings: We tested the use of IOTUs on the widest DNA barcoding dataset of Italian echolocating bats species ever assembled (i.e. 31 species, 209 samples). We identified 31 molecular entities, 26 of which corresponded to the morphologically assigned species, two MOTUs and three IOTUs. Interestingly, we found three IOTUs in Myotis nattereri, one of which is a newly described lineage found only in central and southern Italy. In addition, we found a level of molecular variability within four vespertilionid species deserving further analyses. According to our scheme two of them (i.e. M. bechsteinii and Plecotus auritus) should be ranked as unconfirmed candidate species (UCS). Conclusions/Significance: From a systematic point of view, IOTUs are more informative than the general concept of OTUs and the more recent MOTUs. According to information content, IOTUs are closer to species, although it is important to underline that IOTUs are not species. Overall, the use of a more precise panel of taxonomic entities increases the clarity in the systematic field and has the potential to fill the gaps between modern and traditional taxonomy

Deep differentiation between and within Mediterranean glacial refugia in a flying mammal, the Myotis nattereri bat complex

Aim The role of glacial refugia in the biogeographical patterns in the Western Palaearctic region has been widely discussed, but many questions remain unre- solved. We examined the biogeography, genetic diversity, spatial distribution and evolutionary history of the Myotis nattereri bat species complex to investi- gate the presence of multiple refugia and the persistence of Quaternary differ- entiation between and within Mediterranean refugia in a flying mammal. Location Western Palaearctic region (central and southern Europe and north- western Maghreb). Methods We analysed three mitochondrial fragments (cytochrome b, NADH dehydrogenase subunit 1 and the control region; 1570 bp) from 136 individu- als of the M. nattereri complex sampled from 87 different localities using a range of phylogenetic techniques. Divergences among clades were also dated using a Bayesian coalescence approach. Results Phylogenetic analyses identified four main lineages, coincident with the four cryptic species recently described. Each species is further subdivided into well-supported lineages with evident geographical structure. Estimates of genetic diversity and polymorphism were very high for the majority of subclades, with the exception of M. nattereri s.s. Main conclusions The M. nattereri bat complex comprises four species whose distributions in the Western Palaearctic correspond to four main glacial refugia (Iberia, Italy, Balkans and Morocco). These species are the result of long-term isolation (remarkable in a flying mammal) over several glacial cycles. The Balkan species expanded into central Europe in a rapid recolonization pro- cess. Both the Iberian and Italian peninsulas show a clear pattern of refugia- within-refugia in their genetic structuring, with a deeply differentiated southern Italian clade. Morocco shows two markedly differentiated lineages, probably separated by the Atlas Mountains. The legacy of Pleistocene cycles is evident in both the speciation and the intraspecific diversification events.Peer reviewe

Multilocus phylogeny and species delimitation within the Natterer’s bat species complex in the Western Palearctic

Delimiting species is a crucial issue for many biological disciplines and is of primary importance for designing effective conservation plans. Traditional taxonomy based on morphological characters can be misled by the presence of phenotypic plesiomorphism or adaptative convergence. The use of multiple locus genetic data appears thus as a powerful tool for recognizing species boundaries. In this study, we used six nuclear introns and two mitochondrial markers to conduct a phylogenetic study of the Myotis nattereri species complex in the Western Palearctic. We combined tree-based and non-tree-based analyses, and also used concatenated phylogenetic methods of the separated nuclear and mitochondrial dataset as well as a recent coalescence-based multilocus approach. The strong concor- dance between the results of the analyses conducted confirms that M. nattereri is a paraphyletic group that is composed of four well-differentiated lineages in the study area. In the framework of the unified species concept, these four clades can be confidently considered as four valid species. This recognition of new cryptic species in the Western Mediterranean region shows that the biodiversity of this well- studied area is still not fully understoodPeer reviewe

Two new cryptic bat species within the Myotis nattereri species complex (Vespertilionidae, Chiroptera) from the western palaearctic

The Myotis nattereri species complex consists of an entangled group of Western Palaearctic bats characterized by fringing hairs along the rear edge of their uropatagium. Some members are relatively common while others are rare but all forms are morphologically very similar and their taxonomy is unresolved. Recent studies based on different molecular markers have shown that several major and unexpected lineages exist within this group of forest-dwelling bats. All the mitochondrial and nuclear markers tested to date have shown that these major lineages evolved as fully independent and coherent units and therefore each qualifies as distinct species. In the absence of proper morphological diagnosis, these lineages are informally referred to in the literature under different names. We explore here the external and craniodental variation of these lineages. Although all morphological measurements were overlapping between these lineages, we show that lineages can be completely discriminated in a multivariate morphometric space. Consistent with previous molecular reconstructions, these four major lineages represent two pairs of related species, each represented by a named species (Myotis nattereri s. str. and M. escalerai, respectively) and by unnamed forms (Myotis sp. A and Myotis sp. B, respectively). Herein we describe formally these two unnamed forms to clarify the taxonomy within this species complex. This new taxonomic view has important implication for the protection of these species, as three of the four taxa must now be considered as range-restricted species in need of conservation actions

Coronavirus and paramyxovirus in bats from Northwest Italy

Background: Bat-borne virus surveillance is necessary for determining inter-species transmission risks and is important due to the wide-range of bat species which may harbour potential pathogens. This study aimed to monitor coronaviruses (CoVs) and paramyxoviruses (PMVs) in bats roosting in northwest Italian regions. Our investigation was focused on CoVs and PMVs due to their proven ability to switch host and their zoonotic potential. Here we provide the phylogenetic characterization of the highly conserved polymerase gene fragments. Results: Family-wide PCR screenings were used to test 302 bats belonging to 19 different bat species. Thirty-eight animals from 12 locations were confirmed as PCR positive, with an overall detection rate of 12.6% [95% CI: 9.3–16.8]. CoV RNA was found in 36 bats belonging to eight species, while PMV RNA in three Pipistrellus spp. Phylogenetic characterization have been obtained for 15 alpha- CoVs, 5 beta-CoVs and three PMVs; moreover one P. pipistrellus resulted co-infected with both CoV and PMV. A divergent alpha-CoV clade from Myotis nattereri SpA is also described. The compact cluster of beta-CoVs from R. ferrumequinum roosts expands the current viral sequence database, specifically for this species in Europe. To our knowledge this is the first report of CoVs in Plecotus auritus and M. oxygnathus, and of PMVs in P. kuhlii. Conclusions: This study identified alpha and beta-CoVs in new bat species and in previously unsurveyed Italian regions. To our knowledge this represents the first and unique report of PMVs in Italy. The 23 new bat genetic sequences presented will expand the current molecular bat-borne virus databases. Considering the amount of novel bat-borne PMVs associated with the emergence of zoonotic infections in animals and humans in the last years, the definition of viral diversity within European bat species is needed. Performing surveillance studies within a specific geographic area can provide awareness of viral burden where bats roost in close proximity to spillover hosts, and form the basis for the appropriate control measures against potential threats for public health and optimal management of bats and their habitats