Wiesław Bogdanowicz

Pan-European Distribution of White-Nose Syndrome Fungus (Geomyces destructans) Not Associated with Mass Mortality

Background The dramatic mass mortalities amongst hibernating bats in Northeastern America caused by “white nose-syndrome” (WNS) continue to threaten populations of different bat species. The cold-loving fungus, Geomyces destructans, is the most likely causative agent leading to extensive destruction of the skin, particularly the wing membranes. Recent investigations in Europe confirmed the presence of the fungus G. destructans without associated mass mortality in hibernating bats in six countries but its distribution remains poorly known. Methodology/Principal Findings We collected data on the presence of bats with white fungal growth in 12 countries in Europe between 2003 and 2010 and conducted morphological and genetic analysis to confirm the identity of the fungus as Geomyces destructans. Our results demonstrate the presence of the fungus in eight countries spanning over 2000 km from West to East and provide compelling photographic evidence for its presence in another four countries including Romania, and Turkey. Furthermore, matching prevalence data of a hibernaculum monitored over two consecutive years with data from across Europe show that the temporal occurrence of the fungus, which first becomes visible around February, peaks in March but can still be seen in some torpid bats in May or June, is strikingly similar throughout Europe. Finally, we isolated and cultured G. destructans from a cave wall adjacent to a bat with fungal growth. Conclusions/Significance G. destructans is widely found over large areas of the European continent without associated mass mortalities in bats, suggesting that the fungus is native to Europe. The characterisation of the temporal variation in G. destructans growth on bats provides reference data for studying the spatio-temporal dynamic of the fungus. Finally, the presence of G. destructans spores on cave walls suggests that hibernacula could act as passive vectors and/or reservoirs for G. destructans and therefore, might play an important role in the transmission process.

ROOST CAVITY SELECTION BY NYCTALUS NOCTULA AND N. LEISLERI (VESPERTILIONIDAE, CHIROPTERA) IN BIAŁOWIEŻA PRIMEVAL FOREST, EASTERN POLAND

Abstract The selection of roost cavities by Nyctalus noctula and N. leisleri, 2 widespread species of mainly Eurasian distribution, was examined in Białowieża Primeval Forest in eastern Poland from May to August in 1998–2002. Because N. noctula is one of the most common forest-dwelling bats in Europe, whereas the smaller N. leisleri is relatively rare across its range (except in Ireland) and more limited to ancient forests, we hypothesized that these 2 taxa may differ significantly in their tree-cavity selection. Twenty-five N. noctula and 26 N. leisleri were radiotracked to 52 and 50 roost trees, respectively. For each accessible cavity roost occupied by N. noctula (n = 28) and N. leisleri (n = 39), 16 features were measured and compared with potentially available cavities (n = 72). Both species were selective in roost choice, and preferred cavities located higher (averaging 19 m above the ground), in more open surroundings, with smaller entrances, and with greater safety distance (from martens) than available cavities. Nearly all roosts occupied by bats were dry inside. Both species slightly more frequently settled in cavities with entrances facing NE and SW, but the differences were not statistically significant. Compared to the pool of available cavities, N. noctula was statistically more frequently found in cavities with wider inside cross section and with 1 entrance, unlike N. leisleri, which often used cavities with more than 1 entrance (range 1–6 entrances). One of the most noticeable differences between the 2 species was roost origin. N. leisleri used natural cavities (90%) more often than woodpecker cavities (10%), whereas N. noctula showed the opposite tendency (woodpecker-made cavities accounted for just over half of roosts chosen by this species). The safety distance also was significantly larger in N. leisleri than in N. noctula. A logistic regression model for N. noctula incorporating 4 cavity variables (safety distance from martens, height above ground, cavity origin, and mean distance to nearest vegetation) classified roost and available cavities correctly 85% and 94% of the time, respectively. For N. leisleri, the use of 2 variables only (i.e., height above ground and marten distance) resulted in correct assignment of 85% of roosts and 88% of available cavities. These differences suggest that the 2 species use different antipredator strategies that may have important consequences for their different survival rates in younger forests. In general, roosts in Białowieża Primeval Forest are selected under pressures of predation and climate, and there bats tend to use safe and warm shelters.

New Species in the Old World: Europe as a Frontier in Biodiversity Exploration, a Test Bed for 21st Century Taxonomy

The number of described species on the planet is about 1.9 million, with ca. 17,000 new species described annually, mostly from the tropics. However, taxonomy is usually described as a science in crisis, lacking manpower and funding, a politically acknowledged problem known as the Taxonomic Impediment. Using data from the Fauna Europaea database and the Zoological Record, we show that contrary to general belief, developed and heavily-studied parts of the world are important reservoirs of unknown species. In Europe, new species of multicellular terrestrial and freshwater animals are being discovered and named at an unprecedented rate: since the 1950s, more than 770 new species are on average described each year from Europe, which add to the 125,000 terrestrial and freshwater multicellular species already known in this region. There is no sign of having reached a plateau that would allow for the assessment of the magnitude of European biodiversity. More remarkably, over 60% of these new species are described by non-professional taxonomists. Amateurs are recognized as an essential part of the workforce in ecology and astronomy, but the magnitude of non-professional taxonomist contributions to alpha-taxonomy has not been fully realized until now. Our results stress the importance of developing a system that better supports and guides this formidable workforce, as we seek to overcome the Taxonomic Impediment and speed up the process of describing the planetary biodiversity before it is too late.

Summer Roost Selection by Tree-dwelling Bats Nyctalus noctula and N. leisleri: A Multiscale Analysis

Abstract Nyctalus noctula is one of the most common bats in the western Palearctic, whereas N. leisleri is relatively rare (except in Ireland, where N. noctula does not occur) and more limited to ancient forests. We radiotracked 26 N. noctula and 25 N. leisleri to 52 and 50 roost trees, respectively, from May to August in 1998–2002 in the Białowieża Primeval Forest in eastern Poland to test the hypothesis that N. leiseri has more specific tree-roosting requirements than N. noctula. Both species selected roosts at the microscale (cavity level), mesoscale (tree level), and megascale (plot level). N. noctula significantly preferred oaks, and avoided hornbeams and alders. N. leisleri roosted more often in oaks and ashes, and avoided hornbeams and alders. Roost trees occupied by both species were thicker and taller, with higher crowns than available trees. N. noctula and N. leisleri used oaks more frequently than ashes when average ambient temperatures were lower. Pregnant and lactating females of both species most often used oaks, whereas after the young could fly most roosts were in other tree species, mainly ashes. Reproductive status influenced the choice of roosts used by N. noctula, whereas both the reproductive status and ambient temperature were influential for N. leisleri. Both taxa preferred dying trees and avoided healthy ones, although N. noctula used hollows in healthy trees significantly more often than N. leisleri. In our opinion, more frequent use of healthy trees by N. noctula suggests a better ability to exploit younger, managed forests. However, differences in roost selection between these species were small.

Genetic identification of putative remains of the famous astronomer Nicolaus Copernicus

We report the results of mitochondrial and nuclear DNA analyses of skeletal remains exhumed in 2005 at Frombork Cathedral in Poland, that are thought to be those of Nicolaus Copernicus (1473–1543). The analyzed bone remains were found close to the altar Nicolaus Copernicus was responsible for during his tenure as priest. The mitochondrial DNA (mtDNA) profiles from 3 upper molars and the femurs were identical, suggesting that the remains originate from the same individual. Identical mtDNA profiles were also determined in 2 hairs discovered in a calendar now exhibited at Museum Gustavianum in Uppsala, Sweden. This calendar was the property of Nicolaus Copernicus for much of his life. These findings, together with anthropological data, support the identification of the human remains found in Frombork Cathedral as those of Nicolaus Copernicus. Up-to-now the particular mtDNA haplotype has been observed only 3 times in Germany and once in Denmark. Moreover, Y-chromosomal and autosomal short tandem repeat markers were analyzed in one of the tooth samples, that was much better preserved than other parts of the skeleton. Molecular sex determination revealed that the skeleton is from a male individual, and this result is consistent with morphological investigations. The minimal Y-chromosomal haplotype determined in the putative remains of Nicolaus Copernicus has been observed previously in many countries, including Austria, Germany, Poland, and the Czech Republic. Finally, an analysis of the SNP located in the HERC2 gene revealed the C/C genotype that is predominant in blue-eyed humans, suggesting that Copernicus may have had a light iris color.

Ancient and Contemporary DNA Sheds Light on the History of Mouse-Eared Bats in Europe and the Caucasus

Nietoperzowa Cave in southern Poland has more than 30 subfossils of mouse-eared bats of known age (820 ± 25 years BP). IfDNA has been preserved in a useable fashion in these fossils, they will provide unique opportunities for studying historic population genetics of these animals. We sequenced the entire cytochrome b gene (1,140 bp) from seven subfossil and 56 contemporary individuals of mouse-eared bats from Europe and the Caucasus Mts. Our phylogenetic estimates, combined with a low level of genetic differentiation (2.7%) suggest that M. myotis and M. oxygnathus recently diverged and are distinct at the subspecies level. We also included a fragment of mitochondrial hypervariable region (292 bp) from contemporary mouse-eared bats in our analyses, and noted that among eight haplogroups recorded in Europe and the Caucasian Mts., haplogroup D (recognized as oxygnathus) probably arose in the Crimean refugium and evolved in a steppe landscape. The Balkan stock (haplogroup F) was also successful and dispersed over extended areas. Individuals possessing this haplogroup can be found from the northern part of Apennine Peninsula to southern Poland. On the other hand, during the last ice age, individuals with haplogroup A (described as myotis) most likely found refugia in Iberia. As the glaciers retreated north, these individuals migrated north of the Alps to central Europe (and then to the Balkans). As this group has much stronger affinities with forests than mouse-eared bats from southern parts of Europe, the dispersal of these individuals would have followed the northern migration of deciduous trees in this area. The Carpathian Basin is an area of mixing for several haplogroups from different refugia, including those in Iberia, Apennine Peninsula, Balkans, and the Crimea. Nuclear RAG2 sequence data revealed reciprocal hybridization events of both historic and recent origins. Our results document for the first time that both taxa were present north of the Carpathian Mts. for at least the past 800 years (ca. 400 generations). These are the first subfossil bats from which DNA has been extracted and sequenced, opening new possibilities for future research. Finally, these data highlight the importance of large phylogeographic surveys even among very common taxa.

Swarming of bats at different elevations in the Carpathian Mountains

Swarming bat activity was monitored at three caves at elevations ranging from 880 m to 1,907 m above sea level in the Carpathian Mountains, using an infrared light barrier with data-logger, a video camera with a night-scope system, and subsequently by mist netting. A total of 6,175 bats of 19 species was captured, and over 70,000 passes through cave openings were registered. Caves differed in bat species richness, sex ratio, abundance of particular species and species composition. Peak species richness was observed in the mid-elevation cave. Bat activity was high in all caves, but declined with increasing altitude. Swarming activity occurred earlier at high elevation than at lower elevations. Activity of boreal-alpine species, such as Eptesicus nilssonii, peaked at the start of the swarming period, that of species typical of lower elevations, such as Myotis emarginatus, peaked in the middle of the swarming season. In a few species, males showed a significant preference for higher altitude caves, in contrast to females. A similar pattern was observed in the proportion of adults to juveniles, which increased with increasing elevation. Our results also suggest that M. brandtii and M. alcathoe were more often encountered at lower elevations, M. mystacinus (sensu stricto) at higher ones.

Skull Morphology of Two Cryptic Bat Species: Pipistrellus pipistrellus and P. pygmaeus — A 3D Geometric Morphometrics Approach with Landmark Reconstruction

Differences in skull morphology between two cryptic species of bat, Pipistrellus pipistrellus (n = 14) and P. pygmaeus (n = 15), originating from Great Britain, were investigated. Four different data sets were analysed: (1) 23 landmarks and (2) 26 landmarks on the dorsal and ventral sides of the cranium, respectively, (3) 49 landmarks on the upper jaw, and (4) 34 landmarks on the labial side of the mandible. For almost all data sets, when compared within sex groups, P. pipistrellus were significantly larger than P. pygmaeus; the biggest difference being observed in the mandible size. Interspecific differences in shape, analysed by Principal Component Analysis and Discriminant Function Analysis (DFA) of the Procrustes superimposed landmarks, were also mostly visible in the mandible, and were related to dietary differences between the species. For example, the longer and more upright canines of P. pipistrellus allow them to pierce harder prey, the bigger molars ease its processing, and the shortened body of the mandible and the more developed coronoid process presumably generate a stronger bite. The shape and size of the mandible proved to be a good characteristic for distinguishing both cryptic taxa. A procedure for estimating missing landmarks for 3D geometric morphometric purposes was created. Our procedure of finding the missing landmarks had no effect on the within-group loss of variation. DFA of data sets with reconstructed versus orginal (but reduced) landmarks yielded similar results (three versus two misclassified specimens in leave-one-out cross-validation).

Complete mitochondrial genome database and standardized classification system for Canis lupus familiaris

To contribute to the complete mitogenome database of the species Canis lupus familiaris and shed more light on its origin, we have sequenced mitochondrial genomes of 120 modern dogs from worldwide populations. Together with all the previously published mitogenome sequences of acceptable quality, we have reconstructed a global phylogenetic tree of 555 C. l. familiaris mitogenomes and standardized haplogroup nomenclature. The phylogenetic tree presented here and available online at http://clf.mtdna.tree.cm.umk.pl/ could be further used by forensic and evolutionary geneticists as well cynologists, for data quality control and unambiguous haplogroup classification. Our in-depth phylogeographic analysis of all C. l. familiaris mitogenomes confirmed that domestic dogs may have originated in East Asia during the Mesolithic and Upper Paleolithic time periods and started to expand to other parts of the world during Neolithic times.

Hybridization Hotspots at Bat Swarming Sites

During late summer and early autumn in temperate zones of the Northern Hemisphere, thousands of bats gather at caves, mainly for the purpose of mating. We demonstrated that this swarming behavior most probably leads not only to breeding among bats of the same species but also interbreeding between different species. Using 14 nuclear microsatellites and three different methods (the Bayesian assignment approaches of STRUCTURE and NEWHYBRIDS and a principal coordinate analysis of pairwise genetic distances), we analyzed 375 individuals belonging to three species of whiskered bats (genus Myotis) at swarming sites across their sympatric range in southern Poland. The overall hybridization rate varied from 3.2 to 7.2%. At the species level, depending on the method used, these values ranged from 2.1–4.6% in M. mystacinus and 3.0–3.7% in M. brandtii to 6.5–30.4% in M. alcathoe. Hybrids occurred in about half of the caves we studied. In all three species, the sex ratio of hybrids was biased towards males but the observed differences did not differ statistically from those noted at the population level. In our opinion, factors leading to the formation of these admixed individuals and their relatively high frequency are: i) swarming behaviour at swarming sites, where high numbers of bats belonging to several species meet; ii) male-biased sex ratio during the swarming period; iii) the fact that all these bats are generally polygynous. The highly different population sizes of different species at swarming sites may also play some role. Swarming sites may represent unique hybrid hotspots, which, as there are at least 2,000 caves in the Polish Carpathians alone, may occur on a massive scale not previously observed for any group of mammal species in the wild. Evidently, these sites should be treated as focal points for the conservation of biodiversity and evolutionary processes.