Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Plecotus macrobullaris (Chiroptera: Vespertilionidae)

Plecotus macrobullaris (Chiroptera: Vespertilionidae) Abstract Plecotus macrobullaris (Kuzjakin, 1965) is a medium-sized chiropteran commonly called the alpine long-eared bat, and 1 of the 11 Palearctic species recognized in the genus Plecotus. It has the characteristic long ears of plecotine bats, and externally its most conspicuous diagnostic characteristic is the inverted triangular-shaped pad most individuals exhibit in the chin. It is distributed across the mountain environments in the southwestern and central regions of the Palearctic. It is the most abundant bat species in European alpine environments, although it can be also found at lower elevations. It roosts on both natural (rock crevices, caves, and scree deposits) and artificial shelters (buildings), and it mainly feeds on moths. P. macrobullaris is currently listed as “Least Concern” by the International Union for Conservation of Nature and Natural Resources, although actual population sizes and demographic trends are unknown. Plecotus macrobullaris (Kuzjakin, 1965) Alpine Long-eared Bat Plecotus auritus macrobullarisKuzjakin, 1965:76. Type locality “near Vladikavikaz, North, Ossetia, Russ. Fed.” Plecotus alpinusKiefer and Veith, 2002:8. Type locality “Ristolas, Haute-Alpes, France.” Plecotus microdontusSpitzenberger et al., 2002:5. Type locality “Lienz, Eastern Tyrol, Austria.” Context and Content. Order Chiroptera, family Vespertilionidae, subfamily Vespertilioninae, tribe Plecotini. Plecotus macrobullaris is 1 of the 11 Palearctic species recognized in the genus Plecotus (Spitzenberger et al. 2006). Several authors have suggested the presence of 2 geographically separated subspecies of P. macrobullaris (Spitzenberger et al. 2003; Benda et al. 2004; Kiefer and von Helversen 2004): P. macrobullaris macrobullaris (Eastern group) and P. macrobullaris alpinus (Western group). This division is supported by the presence of 2 geographically separated mitochondrial lineages that probably diverged more than 1 million years ago (Alberdi et al. 2015b). The average mitochondrial dissimilarity between specimens of the 2 lineages is 3.4%. However, there is no information about the genomic structure of populations based on nuclear DNA, thus subspecific differentiation cannot be entirely confirmed. Additionally, the craniometric differentiation does not agree with the phylogenetic dissimilarity, as individuals from the Caucasus (Western lineage) and Alps (Eastern lineage) highly resemble each other, whereas individuals from the Balkans, Turkey, and Syria (Eastern lineage) occupy morphospaces of their own (Spitzenberger et al. 2006). Nomenclatural Notes.Plecotus macrobullaris was first described in the northern slope of the Greater Caucasus (North Ossetia) by Kuzjakin in 1965, as a subspecies of Plecotus auritus, namely P. auritus macrobullaris (Kuzjakin 1965). In 2001–2002, 2 research groups almost simultaneously reported the existence of a clade distinct from P. auritus and P. austriacus in the Austrian Alps (Spitzenberger et al. 2001; Kiefer et al. 2002). Subsequently, each research group described it as a new species (Kock 2002), assigning 2 different names: Plecotus alpinus (Kiefer and Veith 2002) and Plecotus microdontus (Spitzenberger et al. 2002). In 2003, molecular contrast between the newly described species and P. auritus macrobullaris described nearly 40 years earlier by Kuzjakin, indicated they belong to the same clade (Spitzenberger et al. 2003). Therefore, the original nomenclature was recognized as the valid name for the species, but upgraded to the species level. DIAGNOSIS Plecotus macrobullaris (Figs. 1 and 2) shares high morphological similarity with the other Plecotus species in areas where their distributions overlap, namely the brown long-eared bat P. auritus, the gray long-eared bat P. austriacus, and Kolombatovic’s long-eared bat P. kolombatovici. The most conspicuous diagnostic characteristic of P. macrobullaris is the inverted triangular-shaped chin pad that most individuals (e.g., 95% in the Swiss Alps—Ashrafi et al. 2010) exhibit below the lower lip (Spitzenberger et al. 2002). The chin pad of the other species tends to be rounded and is often darker in young individuals (Sachanowicz and Ciechanowski 2006). However, variation in color, size, and shape of the chin pad can lead to inconsistent identification. Male specimens can be identified with high reliability based on penis shape (Ashrafi et al. 2010). P. macrobullaris specimens exhibit a cylindrical penis, whereas the penis of P. austriacus and P. kolombatovici males is club-shaped and the penis of P. auritus narrows toward the end (Dietz and von Helversen 2004; Tvrtkovic et al. 2005). Although several authors have proposed other means of identification based on external qualitative characters such as the color of the ventral fur or the presence of hair on the hind feet (Kiefer and Veith 2002; Dietz and von Helversen 2004), most of them have not been validated across the entire geographic range of the species. Despite the large morphometric overlap between the 4 western Palearctic long-eared bats (Tvrtkovic et al. 2005; Ashrafi et al. 2010), a multilinear combination of 8 morphometric measurements yielded an identification success rate of 97.5% among Plecotus from Switzerland. In addition, several authors reported that the thumb length is a relatively good criterion to differentiate P. macrobullaris (> 6.2 mm) from P. austriacus and P. kolombatovici (< 6.6 mm) where these 3 species cohabit (Spitzenberger et al. 2002; Tvrtkovic et al. 2005). All the mentioned Plecotus species can be unambiguously discerned using short mitochondrial molecular markers, such as the cytochrome b or the control region (Juste et al. 2004; Spitzenberger et al. 2006), as well as the standardized COI barcode region (Agnarsson et al. 2011). Fig. 1. View largeDownload slide An adult female Plecotus macrobullaris from Aísa, Pyrenees, Spain. Photograph by A. Alberdi. Fig. 1. View largeDownload slide An adult female Plecotus macrobullaris from Aísa, Pyrenees, Spain. Photograph by A. Alberdi. Fig. 2. View largeDownload slide Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult male Plecotus macrobullaris (Natural History Museum in Belgrade 01/14) from Ćetanica plateau (Serbia), captured on 26 July 2013. Condylobasal length is 15.64 mm. Photograph by Ivana Budinski used with permission. Fig. 2. View largeDownload slide Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult male Plecotus macrobullaris (Natural History Museum in Belgrade 01/14) from Ćetanica plateau (Serbia), captured on 26 July 2013. Condylobasal length is 15.64 mm. Photograph by Ivana Budinski used with permission. GENERAL CHARACTERS Plecotus macrobullaris is a medium-sized (6–10 g, forearm length usually between 39 and 43 mm) Palearctic bat. It has the characteristic long ears of plecotine bats, which are fully erect and extended forward when echolocating and in flight, and folded and curled sideways when at rest. Ears and tragus are light brown, and eyes are fairly large and black. The face is dark brown, with a robust snout and a pinkish mandible where the inverted triangular-shaped pad usually stands out on the chin. The ventral fur is dense and usually looks whitish, often with pale yellowish highlights both sides of the neck and shoulders; the dorsal fur is typically pale gray. All hairs are bicolored in adult specimens, with a black base and lighter tips. There is no sexual dimorphism in fur coloration. The patagium is light brown and translucent, without fur. Coloration, morphometric measurements, and the length of the fur are subject to considerable geographical variation. Dental formula is i 2/3, c 1/1, p 2/3, m 3/3, total 36. Mean external biometric measurements (mm; with range and n) were: forearm length 41.2 (35.5–44.8, 195); length of hind foot 7.6 (6.6–9.0, 177); tragus length 17.2 (14.2–20.0, 166); tragus width 5.8 (5.0–7.0, 157); thumb length 6.9 (5.5–7.9, 192); and claw length 2.6 (0.9–3.6, 83—Kiefer and Veith 2002; Garin et al. 2003; Trizio et al. 2005; Tvrtkovic et al. 2005; Ashrafi et al. 2010). Females are usually larger than males (Tvrtkovic et al. 2005; Ashrafi et al. 2010). Mean craniometric measurements (mm; with range and n) were: greatest length of skull 17.0 (15.9–18.3, 82); condylocanine length 15.1 (14.1–16.1, 70); condylobasal length 15.8 (14.7–16.9, 80); height of braincase 7.6 (7.1–8.1, 80); breadth of braincase 8.5 (7.7–9.3, 75); breadth of interorbital constriction 3.5 (3.1–3.9, 81); maximum bulla diameter 4.6 (4.2–4.9, 57); anterior palatal breadth 3.8 (3.4–4.2, 75); maxillary breadth 6.3 (5.9–6.7, 81); length of upper toothrow from 1st incisor to 3rd molar 6.7 (6.3–7.2, n = 51); length of upper toothrow from canine to 3rd molar 5.6 (5.3–6.3, 87—Kiefer and Veith 2002; Spitzenberger et al. 2003; Benda et al. 2004). The cranial and dental structures are similar across the entire geographic distribution of P. macrobullaris, but the skull size and the auditory bullae tend to be smaller in the Western clade than in the Eastern clade (Spitzenberger et al. 2003). DISTRIBUTION Plecotus macrobullaris is the only bat species with a palealpine distribution (Fig. 3; i.e., widely distributed across the Palearctic, but limited to mountain environments—Alberdi et al. 2014). It is found in the main mountain ranges in the southwestern and central Palearctic, as well as the close surroundings (Alberdi et al. 2013). To date, P. macrobullaris has been found in the Pyrenees (France and Spain—Garin et al. 2003; Alberdi et al. 2013), Alps (Austria, France, Italy, Liechtenstein, Slovenia, Switzerland—Chirichella et al. 2003; Kiefer and von Helversen 2004; Trizio et al. 2005; Spitzenberger et al. 2006; Presetnik et al. 2009; Mattei-Roesli 2010; Rutishauser et al. 2012), Dinaric Alps (Albania, Bosnia-Herzegovina, Croatia, Macedonia, Montenegro, Serbia—Juste et al. 2004; Tvrtkovic et al. 2005; Sachanowicz and Ciechanowski 2006; Bekker and Boshamer 2007; Budinski et al. 2016), Pindos Mountains (Greece—Alberdi et al. 2013), several mountain ranges in Turkey (Kaçkar, Taurus, Guneydogu Toroslar—Karatas and Sozen 2006), Greater Caucasus (Georgia, Russia—Spitzenberger et al. 2006; Kiefer 2008; Alberdi et al. 2013), Lower Caucasus (Armenia, Azerbaijan—Kiefer 2008), Anti-Lebanon (Syria—Benda et al. 2006), and the Iranian Alborz and Zagros Mountains (Benda et al. 2012). P. macrobullaris has been also found on 2 Mediterranean islands: Corsica and Crete (Kiefer and von Helversen 2004; Benda et al. 2008). Fig. 3. View largeDownload slide Geographic distribution of Plecotus macrobullaris. The 2 matrilineal clades are: 1, Western clade (P. m. alpinus); 2, Eastern clade (P. m. macrobullaris). Fig. 3. View largeDownload slide Geographic distribution of Plecotus macrobullaris. The 2 matrilineal clades are: 1, Western clade (P. m. alpinus); 2, Eastern clade (P. m. macrobullaris). The elevational range of P. macrobullaris spans from sea level up to about 2,800 m, even though there are considerable differences between geographic areas. Almost all records in the Pyrenees and the Zagros mountains are above 1,500 m, but the species can be found at considerably lower elevations in very steep and mountainous regions. In such regions, P. macrobullaris shows an extremely wide elevational distribution (e.g., in the Alps it can be found between 200 and 2,200 m—Alberdi et al. 2013), and in Croatia from sea level up to mountain tops (Pavlinic and Tvrtkovic 2004). No fossils are known. FORM AND FUNCTION Echolocation calls are fairly similar to other Plecotus species. Plecotus macrobullaris emits multiharmonic, downward frequency-modulated signals consisting mostly of the 1st and the lower part of the 2nd harmonic (Dietrich et al. 2006; Barataud 2014). The 1st harmonic starts at about 46 kHz and ends around 23 kHz, with a peak frequency around 35 kHz. The 2nd harmonic starts around 67 kHz and does not overlap with the 1st harmonic. The pulse length varies considerably depending on the surrounding environment, emitting short signals (up to 0.8 ms) when flying close to the clutter, and long signals (up to 7.3 ms) when flying far from the clutter. The longer the signal the lower the frequency band and the peak frequency. Although P. macrobullaris is genetically more closely related to P. auritus, its signal structure is closer to that of P. austriacus. ECOLOGY Plectous macrobullaris females aggregate in small groups (5–25) to form breeding colonies (Ashrafi et al. 2010). These colonies may contain several nulliparous females, with an occasional presence of male bats (Alberdi et al. 2015a). Distribution records indicate that P. macrobullaris is ecologically linked to mountain environments (Kiefer and Veith 2002; Alberdi et al. 2013), although it is not restricted to high elevations (Pavlinic and Tvrtkovic 2004; Ashrafi et al. 2010). Using an ecological niche modeling approach, Alberdi et al. (2014) concluded that the broad-scale distribution of P. macrobullaris is mainly shaped by topographic factors, as it is found in areas with very steep topography but missing in flatlands. In contrast, the relative influence of climatic factors was much lower, as the distribution of P. macrobullaris covers a very broad climatic range, from the extremely cold and rainy Alps to the warm and dry mountains in the Middle East. Alberdi et al. (2014) suggested that its fondness for steep environments might be the result of increased availability of rocky and open-space areas that would provide appropriate foraging and roosting environments for P. macrobullaris. However, the study of roosting and foraging preferences of P. macrobullaris has yielded contrasting results. Most of the known roosting sites of P. macrobullaris are man-made buildings (Alberdi et al. 2013). In fact, it is one of the most common species found in church attics in the Alps (Rutishauser et al. 2012). Nevertheless, results of a radiotracking study performed in the Pyrenees depicted a very different behavior. Alberdi et al. (2015a) captured 51 free-flying P. macrobullaris, and radiotracked them to their roosting sites. Most bats sheltered in rock crevices, and many males and nulliparous females made systematic use of scree deposits as roosts. Many of those roosting sites were found in alpine environments (above the upper forest treeline). Only 3 of the 51 tracked bats, all of them breeding females, roosted in buildings. The authors considered 2 possible explanations for the contrasting results. Bats (mainly breeding females) might make use of buildings more often in the Alps than in the Pyrenees because the climatic conditions are colder (about 2°C at the same elevation). Conversely, almost all the records in the Alps come from surveys of building that were considered suitable a priori, which entails a systemic bias toward man-made buildings. Similarly, the few roosts that were known in the Pyrenees before the radiotracking study were also buildings (Alberdi et al. 2015a). Bats might also use natural roosting resources in the Alps, but the previously described approaches may not be suitable for revealing the entire roosting spectrum of P. macrobullaris. Plecotus macrobullaris has been also found in caves, mostly in the southeastern area of its distribution (Benda et al. 2008, 2012). Probably, it was originally linked to karstic areas with high availability of rock crevices, scree slopes, and caves. In fact, this preference to limestone environments can be still seen in the Pyrenees Mountains and Croatia (Tvrtkovic et al. 2005; Alberdi et al. 2013). However, P. macrobullaris has been able to take advantage of relatively new roosting resources such as man-made buildings. Finally, a male P. macrobullaris was documented using tree hole indicating that they might occasionally use alternate types of roosts. These results depict a flexible roosting behavior, and suggest that depending on the environmental conditions, as well as sexual and reproductive status, P. macrobullaris bats may exhibit different roosting preferences (Fig. 4). Fig. 4. View largeDownload slide Some of the most common roosting resources used by Plecotus macrobullaris. (A) Church in Kupljenik, Slovenia (632 m), where a small (5 adults) maternity colony was identified in 2012. (B) Crack (exact location indicated by the green arrow) in a large rock wall in Valle de Tena, Spain (2,250 m), where a maternity colony of > 10 individuals was located in 2013. A red circle indicates the presence of a researcher. (C) Talus slope in Valle de Aísa, Spain (1,450 m), where a nulliparous female was located for several days in 2013. (D) A female P. macrobullaris and its pup in a church attic in Laas, Italy, in July 2012 (920 m). (E) A male P. macrobullaris roosted in a crack in Currundué, Spain (1,740 m), in July 2013. (F) A male P. macrobullaris roosted in a scree deposit in Valle de Añisco, Spain (2,140 m), in July 2013. Fig. 4. View largeDownload slide Some of the most common roosting resources used by Plecotus macrobullaris. (A) Church in Kupljenik, Slovenia (632 m), where a small (5 adults) maternity colony was identified in 2012. (B) Crack (exact location indicated by the green arrow) in a large rock wall in Valle de Tena, Spain (2,250 m), where a maternity colony of > 10 individuals was located in 2013. A red circle indicates the presence of a researcher. (C) Talus slope in Valle de Aísa, Spain (1,450 m), where a nulliparous female was located for several days in 2013. (D) A female P. macrobullaris and its pup in a church attic in Laas, Italy, in July 2012 (920 m). (E) A male P. macrobullaris roosted in a crack in Currundué, Spain (1,740 m), in July 2013. (F) A male P. macrobullaris roosted in a scree deposit in Valle de Añisco, Spain (2,140 m), in July 2013. Roosting-site habitat selection has also produced contrasting results. Rutishauser et al. (2012) reported that P. macrobullaris chooses buildings surrounded by forest environments, although Alberdi et al. (2015a) found that most roosts were located closer to meadows and open forests, and further away from deciduous forest and shrubbery. These conflicting results might reflect a geographical trend (i.e., bats roost closer to forest in the Alps than in the Pyrenees), or it might be due to the differences in the employed approaches and the roosting resources that were examined. Rutishauser et al. (2012) studied the location of man-made buildings where P. macrobullaris was found roosting, but Alberdi et al. (2015a) analyzed the roosts spotted after radiotracking free-ranging bats, mainly natural rock cracks and scree deposits. Interestingly, the building roosts identified in the latter study were located close to or surrounded by forest (Alberdi et al. 2015a). Regarding foraging preferences, the abundant captures performed hundreds of meters above the upper forest limit (Alberdi et al. 2013), the roosts located far from forest environments (Alberdi et al. 2015a), and the open-space moth species identified in its diet (Alberdi et al. 2012) suggest that, at least in the Pyrenees, P. macrobullaris is an open-space forager. However, this pattern largely contrasts with the observations reported from the Swiss Alps, where Ashrafi et al. (2013) concluded that P. macrobullaris avoids grasslands and selects its foraging habitat according to the heterogeneity of vertical vegetation structures. Similarly, Pavlinic and Tvrtkovic (2004) reported that in Croatia the species appears linked to deciduous forests, but P. macrobullaris has never been observed in forests in the Pyrenees (Alberdi et al. 2013). To further blur the picture of foraging preferences of P. macrobullaris, another radiotracking study carried out in the Italian Alps concluded that P. macrobullaris avoids woodlands (Preatoni et al. 2011). Two radiotracking studies indicated that the foraging range of P. macrobullaris is usually below 4 km (Ashrafi 2010; Preatoni et al. 2011), although displacement of up to 7 km, and elevation differences of more than 1,000 m have been recorded in a single night (Alberdi et al. 2015a). The diet of P. macrobullaris is mainly composed of moths (Order Lepidoptera), although it also consumes coleopterans and dipterans (Ashrafi et al. 2011; Alberdi et al. 2012). Most moth species identified in its diet belong to the family Noctuidae, and 96% of prey species (Alberdi et al. 2012) identified using molecular methods were tympanate moths (i.e., species that can detect bats’ echolocation calls—Goerlitz et al. 2010). Multiple ecological and distribution data suggest the existence of competitive exclusion between P. macrobullaris and P. austriacus. Both species use similar open and semi-open areas for foraging, and their diets are basically composed of grassland moth species (Razgour et al. 2011; Alberdi et al. 2012). Conversely, the trophic niche of P. auritus is different, as it also includes nonflying arthropods and is basically composed of woodland prey (Ashrafi et al. 2011; Razgour et al. 2011). There are also large similarities in echolocation signals and flight behavior (Dietrich et al. 2006). All these ecological resemblances likely yield a parapatric distribution of P. austriacus and P. macrobullaris in many geographic areas. In Switzerland P. austriacus occupies the Northern lowland areas, while P. macrobullaris is restricted to the mountainous regions (Rutishauser et al. 2012). A similar geographical split is also observed in Croatia, where P. macrobullaris seems to be restricted to the karstic areas (Tvrtkovic et al. 2005). In the southern slopes of the Pyrenees Mountains, the parapatric distribution responds to an altitudinal pattern rather than to a geographical one. In that mountain range, P. macrobullaris occupies the highest open areas and P. austriacus is found in lower zones (Alberdi et al. 2013). There are also exceptions where both species can be found together, such as the Swiss city of Genève (Rutishauser et al. 2012), or several subalpine areas in the Pyrenees (Alberdi et al. 2013). As occurs with the other Plecotus species, P. macrobullaris emits very faint echolocation pulses (Dietrich et al. 2006). These pulses attenuate rapidly, making it almost impossible for most ultrasound detectors to record P. macrobullaris even from 5 m of distance. In addition, differentiation from other Plecotus species is also very challenging (Barataud 2014). Consequently, its presence and abundance can be overlooked or underestimated in biodiversity surveys solely based on echolocation detection. Additionally, Alberdi et al. (2013) reported a surprisingly meager capture success of P. macrobullaris individuals in water points, suggesting that other capture techniques such as setting long net-chains in open areas should be employed to increase capture efficiency and obtain a better picture of abundance of this species. BEHAVIOR When roosting in man-made buildings Plectous macrobullaris is usually found forming monospecific colonies, although it has been occasionally observed sharing attics with other Plecotus species; specifically P. kolombatovici and P. auritus (Tvrtkovic et al. 2005; Ashrafi et al. 2010). In caves it has been found along with species of Rhinolophus and Myotis (Benda et al. 2012). Roost fidelity varies according to the type of roosting resource used, as well as the sex and reproductive condition of the individual. Individuals roosting in man-made buildings show very high roost fidelity and bats roosting in natural rock crevices exhibit slightly less fidelity. The lowest fidelity is found in the use of scree deposits, as these bats change their roosting location almost every day (Alberdi et al. 2015a). Regarding sex and reproductive condition, breeding females barely change their roosting sites, nulliparous females show intermediate fidelity, although males exhibit a very labile behavior, switching their roosts almost every day (Alberdi et al. 2015a). There is no confirmed data about the hibernation behavior of P. macrobullaris. The only known information is based on 2 observations of Plecotus specimens hibernating in caves with ice formations above > 2,000 m in the Pyrenees Mountains and the Slovenian Alps (Kryštufek 1987; Aihartza 1992). As both observations are prior to the description of P. macrobullaris, they were not identified as such. However, the knowledge on the ecology of Plecotus bats suggests that those observations most probably belong to P. macrobullaris. GENETICS Despite the morphological and ecological similarity to Plectous austriacus (Ashrafi et al. 2011), P. macrobullaris belongs to the so-called “auritus group” (Juste et al. 2004; Spitzenberger et al. 2006). This group is divided into 2 main mitochondrial clades, between which 79.5% of the total genetic variation occurs (Alberdi et al. 2015b). The presence of these 2 matrilineal lineages was reported by the 1st molecular analyses of P. macrobullaris (Spitzenberger et al. 2003), and was later confirmed using complete mitochondrial genomes (Alberdi et al. 2015b). The 1st analyses based on short mitochondrial markers (e.g., control region) showed differences of about 2.5% between the 2 lineages (Spitzenberger et al. 2003), although the complete mitochondrial sequences exhibited larger overall differentiation, namely 3.4% (Alberdi et al. 2015b). All the individuals from the Pyrenees and the Alps belong to the Western clade (Alberdi et al. 2015b), while the individuals from the other mountain ranges belong to the Eastern clade. Hence, the current contact zone involving the 2 lineages is located between the Eastern Alps and the Dinaric Alps (Eastern Italy, Slovenia, and Northern Croatia). All molecularly characterized individuals from Eastern Italy and Slovenia but 1 belongs to the Western clade, while all individuals from Croatia belong to the Eastern clade (Spitzenberger et al. 2006; Alberdi et al. 2015b). Based on complete mitochondrial genomes, Alberdi et al. (2015b) reported that both lineages split more than 1 million year ago, before the beginning of the large Pleistocene climatic oscillations. Using paleoclimatic niche reconstructions the authors estimated that the Dinarides (Croatia) remained ecologically unsuitable for most of the time during the Pleistocene, which could have acted as a natural ecological barrier that prevented the interbreeding between the lineages. The genetic structure of both populations is rather different, reflecting different paleodemographic histories. The Eastern lineage conserves considerably larger genetic diversity than the Western lineage. The Eastern lineage began to diversify around 900,000 years ago and exhibits marked population structure. Conversely, the most recent common female ancestor of the Western lineage was estimated to live about 68,000 years ago, and diversification probably occurred after the last glaciation (Alberdi et al. 2015b). CONSERVATION Plectous macrobullaris is listed as “Least Concern” by the International Union for Conservation of Nature and Natural Resources (Hutson et al. 2016), but due to its recent discovery the actual conservation status of P. macrobullaris is still uncertain. However, the abundant captures performed in high-mountain environments (Alberdi et al. 2013), as well as the large number of roosts found in buildings in the Alps (Rutishauser et al. 2012) and the Dinarides (Pavlinic and Tvrtkovic 2004) suggest that it is currently a relatively abundant species in mountainous environments. Although in the Pyrenees Mountains the species has been mainly found in natural roosts (Alberdi et al. 2015a), most breeding colonies known in the Alps are in the attics of man-made structures, specifically churches (Rutishauser et al. 2012). Hence, the conservation and management of such buildings are important for the conservation of the species. Because the Alps are one of the coldest regions in the geographic distribution of P. macrobullaris, the availability of warm shelters suitable for breeding, such as church attics, might be essential for the conservation of P. macrobullaris in the region. Synonymy completed 2 November 2017 Version of Record, first published online May 9, 2018, with fixed content and layout in compliance with Art. 8.1.3.2 ICZN. Nomenclatural statement.—A life science identifier (LSID) number was obtained for this publication: urn:lsid:zoobank.org:pub:CBE7455F-57F2-4CA7-A126-D4EF8F8C6D24 LITERATURE CITED Agnarsson , I. , C. M. Zambrana-Torrelio , N. P. Flores-Saldana , and L. J. May-Collado . 2011 . A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia) . PLoS Currents 3 : RRN1212 . Google Scholar CrossRef Search ADS PubMed Aihartza , J . 1992 . Ipar-belarrihandia, bitxia bezain ezezaguna . Elhuyar 60 : 25 – 27 . Alberdi , A. , I. Garin , O. Aizpurua J. Aihartza . 2012 . The foraging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes . PLoS One 7 : e35692 . Google Scholar CrossRef Search ADS PubMed Alberdi , A. , I. Garin , O. Aizpurua J. Aihartza . 2013 . Review on the geographic and elevational distribution of the mountain long-eared bat Plecotus macrobullaris, completed by utilising a specific mist-netting technique . Acta Chiropterologica 15 : 451 – 461 . Google Scholar CrossRef Search ADS Alberdi , A. , O. Aizpurua , J. Aihartza I. Garin . 2014 . Unveiling the factors shaping the distribution of widely distributed alpine vertebrates, using multi-scale ecological niche modelling of the bat Plecotus macrobullaris . Frontiers in Zoology 11 : 77 . Google Scholar CrossRef Search ADS PubMed Alberdi , A. , J. Aihartza , O. Aizpurua , E. Salsamendi , M. Brigham I. Garin . 2015a . Living above the treeline: roosting ecology of the alpine bat Plecotus macrobullaris . European Journal of Wildlife Research 61 : 17 – 25 . Google Scholar CrossRef Search ADS Alberdi , A. , M. T. P. Gilbert , O. Razgour , O. Aizpurua , J. Aihartza I. Garin . 2015b . 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 : 1689 – 1700 . Google Scholar CrossRef Search ADS Ashrafi , S . 2010 . Resource partitioning in three cryptic, sympatric bat species (Plecotus spp.) with contrasting conservation status . Ph.D. dissertation , Universität Bern , Bern, Switzerland . Ashrafi , S. , A. Beck , M. Rutishauser , R. Arlettaz F. Bontadina . 2011 . Trophic niche partitioning of cryptic species of long-eared bats in Switzerland: implications for conservation . European Journal of Wildlife Research 57 : 843 – 849 . Google Scholar CrossRef Search ADS Ashrafi , S. , F. Bontadina , A. Kiefer , I. Pavlinic R. Arlettaz . 2010 . Multiple morphological characters needed for field identification of cryptic long-eared bat species around the Swiss Alps . Journal of Zoology 281 : 241 – 248 . Google Scholar CrossRef Search ADS Ashrafi , S. , M. Rutishauser , K. Ecker , M. K. Obrist , R. Arlettaz F. Bontadina . 2013 . Habitat selection of three cryptic Plecotus bat species in the European Alps reveals contrasting implications for conservation . Biodiversity and Conservation 22 : 2751 – 2766 . Google Scholar CrossRef Search ADS Barataud , M . 2014 . Écologie acoustique des chiroptères d’Europe . Biotope Éditions , Meze, France . Bekker , J. J. Boshamer . 2007 . First records of Plecotus auritus (Linnaeus, 1758) and Plecotus macrobullaris Kuzjakin, 1965 in the Republic of Macedonia . Lutra 50 : 43 – 48 . Benda , P. , et al. 2006 . Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 4. Bat fauna of Syria: distribution, systematics, ecology . Acta Societatis Zoologicae Bohemicae 70 : 1 – 329 . Benda , P. , et al. 2012 . Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 10. Bat fauna of Iran . Acta Societatis Zoologicae Bohemicae 76 : 163 – 582 . Benda , P. , P. Georgiakakis C. Dietz . 2008 . Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 7. The bat fauna of Crete, Greece . Acta Societatis Zoologicae Bohemicae 72 : 105 – 190 . Benda , P. , A. Kiefer , V. Hanak M. Veith . 2004 . Systematic status of African populations of long-eared bats, genus Plecotus (Mammalia: Chiroptera) . Folia Zoologica 53 : 1 – 47 . Budinski , I. , B. Karapandza , V. Josipovic , J. Jovanovic M. Paunovic . 2016 . The first record of alpine long-eared bat Plecotus macrobullaris in Serbia . Turkish Journal of Zoology 40 : 984 – 988 . Google Scholar CrossRef Search ADS Chirichella , R. , et al. 2003 . The Adamello-Brenta Natural Park bat community (Mammalia, Chiroptera): distribution and population status . Hystrix 14 : 29 – 45 . Dietrich , S. , D. P. Szameitat , A. Kiefer , H. U. Schnitzler A. Denzinger . 2006 . Echolocation signals of the plecotine bat, Plecotus macrobullaris Kuzyakin, 1965 . Acta Chiropterologica 8 : 465 – 475 . Google Scholar CrossRef Search ADS Dietz , C. O. von Helversen . 2004 . Illustrated identification key to the bats of Europe . Dietz & von Helversen, Electronic Publication. Garin , I. , J. L. Garcia-Mudarra , J. Aihartza , U. Goiti J. Juste . 2003 . Presence of Plecotus macrobullaris (Chiroptera: Vespertilionidae) in the Pyrenees . Acta Chiropterologica 5 : 243 – 250 . Google Scholar CrossRef Search ADS Goerlitz , H. R. , H. M. ter Hofstede , M. R. K. Zeale , G. Jones , and M. W. Holderied . 2010 . An aerial-hawking bat uses stealth echolocation to counter moth hearing . Current Biology 20 : 1568 – 1572 . Google Scholar CrossRef Search ADS PubMed Hutson , A. M. , S. Aulagnier , J. Juste , A. Karataş , J. Palmeirim M. Paunović . 2016 . Plecotus macrobullaris. The International Union for Conservation of Nature and Natural Resources red list of threatened species . http://www.iucnredlist.org/details/136229/0. Accessed 31 December 2017 . Juste , J. , et al. 2004 . Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands . Molecular Phylogenetics and Evolution 31 : 1114 – 1126 . Google Scholar CrossRef Search ADS PubMed Karatas , A. M. Sozen . 2006 . Bats of the middle and upper Kızılırmak regions, Central Anatolia, Turkey . Lynx 37 : 151 – 159 . Kiefer , A . 2008 . Phylogeny of Western Palaearctic long-eared bats (Mammalia, Chiroptera, Plecotus) – a molecular perspective . Johannes Gutenberg-Universität , Mainz, Germany . Kiefer , A. O. von Helversen . 2004 . Plecotus macrobullaris (Kuzjakin, 1965) - Alpenlangohr . Pp. 1051 – 1058 in Handbuch der Säugetiere Europas - Fledertiere II ( F. Krapp , ed.). AULA-Verlag , Wiebelsheim, Germany . Kiefer , A. M. Veith . 2002 . A new species of long-eared bat from Europe (Chiroptera: Vespertilionidae) . Myotis 39 : 5 – 16 . Kiefer , A. , F. Mayer , J. Kosuch , O. von Helversen M. Veith . 2002 . Conflicting molecular phylogenies of European long-eared bats (Plecotus) can be explained by cryptic diversity . Molecular Phylogenetics and Evolution 25 : 557 – 566 . Google Scholar CrossRef Search ADS PubMed Kock , D . 2002 . The publication dates of Plecotus alpinus Kiefer and Veith, 2002 and of Plecotus microdontus Spitzenberger, 2002 . Acta Chiropterologica 4 : 219 – 220 . Google Scholar CrossRef Search ADS Kryštufek , B . 1987 . Distribution of bats in Slovenia (Yugoslavia) . In European bat research 1987 ( V. Hanak , I. Horáček , and J. Gaisler , eds.). Charles University Press , Praha, Czech Republic 399 – 401 . Kuzjakin , A . 1965 . Otrjad Rukokrylyje. Ordo Chiroptera . In Opredelitel mljekopitayushtshikh SSSR ( N. Bobrinskij , B. Kuznetsov , and A. Kuzjakin , eds.). Isd. Prosveshtshenije Moscow 79 – 116 . Mattei-Roesli , M . 2010 . Situazione del genere Plecotus (Chiroptera) nel Cantone Ticino (Svizzera) . Bollettino della Società ticinese di Scienze naturali 98 : 31 – 34 . Pavlinic , I. N. Tvrtkovic . 2004 . Altitudinal distribution of four Plecotus species (Mammalia, Vespertilionidae) occurring in Croatia . Natura Croatica 13 : 395 – 401 . Preatoni , D. , M. Spada , L. Wauters , G. Tosi A. Martinoli . 2011 . Habitat use in the female Alpine long-eared bat (Plecotus macrobullaris): does breeding make the difference ? Acta Chiropterologica 13 : 355 – 364 . Google Scholar CrossRef Search ADS Presetnik , P. , K. Koselj M. Zagmajster . 2009 . Atlas netopirjev (Chiroptera) Slovenije. Atlas of bats (Chiroptera) of Slovenia . Miklavž na Dravskem polju: Center za kartografijo favne in flore , Ljubljana, Slovenia . Razgour , O. , et al. 2011 . High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species . Ecology and Evolution 1 : 556 – 570 . Google Scholar CrossRef Search ADS PubMed Rutishauser , M. D. , F. Bontadina , V. Braunisch , S. Ashrafi R. Arlettaz . 2012 . The challenge posed by newly discovered cryptic species: disentangling the environmental niches of long-eared bats . Diversity and Distributions 18 : 1107 – 1119 . Google Scholar CrossRef Search ADS Sachanowicz , K. M. Ciechanowski . 2006 . Plecotus macrobullaris – new bat species for Albanian fauna (Chiroptera: Vespertilionidae) . Lynx (Praha) 37 : 241 – 246 . Spitzenberger , F. , E. Haring N. Tvrtkovic . 2002 . Plecotus microdontus (Mammalia, Vespertilionidae), a new bat species from Austria . Natura Croatica 11 : 1 – 18 . Spitzenberger , F. , J. Pialek E. Haring . 2001 . Systematics of the genus Plecotus (Mammalia, Vespertilionidae) in Austria based on morphometric and molecular investigations . Folia Zoologica 50 : 161 – 172 . Spitzenberger , F. , P. Strelkov E. Haring . 2003 . Morphology and mitochondrial DNA sequences show that Plecotus alpinus Kiefer & Veith, 2002 and Plecotus microdontus Spitzenberger, 2002 are synonyms of Plecotus macrobullaris Kuzjakin, 1965 . Natura Croatica 12 : 39 – 53 . Spitzenberger , F. , P. Strelkov , H. Winkler E. Haring . 2006 . A preliminary revision of the genus Plecotus (Chiroptera, Vespertilionidae) based on genetic and morphological results . Zoologica Scripta 35 : 187 – 230 . Google Scholar CrossRef Search ADS Trizio , I. , et al. 2005 . First record of the alpine long-eared bat (Plecotus macrobullaris Kuzjakin, 1965) in Lombardy (Northern Italy) revealed by DNA analysis . Natura Bresciana 34 : 171 – 175 . Tvrtkovic , N. , I. Pavlinic E. Haring . 2005 . Four species of long-eared bats (Plecotus, Geoffroy, 1818; Mammalia, Vespertilionidae) in Croatia: field identification and distribution . Folia Zoologica 54 : 75 – 88 . © The Author(s) 2018. Published by Oxford University Press on behalf of American Society of Mammalogists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Mammalian Species Oxford University Press

Plecotus macrobullaris (Chiroptera: Vespertilionidae)

Alberdi, Antton; Aizpurua, Ostaizka
Mammalian Species , Volume Advance Article (958) – May 9, 2018
Download PDF
8 pages

Loading next page...
 
/lp/ou_press/plecotus-macrobullaris-chiroptera-vespertilionidae-dUXgwrhe1a
Publisher
Oxford University Press
Copyright
© The Author(s) 2018. Published by Oxford University Press on behalf of American Society of Mammalogists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
ISSN
0076-3519
eISSN
1545-1410
DOI
10.1093/mspecies/sey003
Publisher site
See Article on Publisher Site

Abstract

Abstract Plecotus macrobullaris (Kuzjakin, 1965) is a medium-sized chiropteran commonly called the alpine long-eared bat, and 1 of the 11 Palearctic species recognized in the genus Plecotus. It has the characteristic long ears of plecotine bats, and externally its most conspicuous diagnostic characteristic is the inverted triangular-shaped pad most individuals exhibit in the chin. It is distributed across the mountain environments in the southwestern and central regions of the Palearctic. It is the most abundant bat species in European alpine environments, although it can be also found at lower elevations. It roosts on both natural (rock crevices, caves, and scree deposits) and artificial shelters (buildings), and it mainly feeds on moths. P. macrobullaris is currently listed as “Least Concern” by the International Union for Conservation of Nature and Natural Resources, although actual population sizes and demographic trends are unknown. Plecotus macrobullaris (Kuzjakin, 1965) Alpine Long-eared Bat Plecotus auritus macrobullarisKuzjakin, 1965:76. Type locality “near Vladikavikaz, North, Ossetia, Russ. Fed.” Plecotus alpinusKiefer and Veith, 2002:8. Type locality “Ristolas, Haute-Alpes, France.” Plecotus microdontusSpitzenberger et al., 2002:5. Type locality “Lienz, Eastern Tyrol, Austria.” Context and Content. Order Chiroptera, family Vespertilionidae, subfamily Vespertilioninae, tribe Plecotini. Plecotus macrobullaris is 1 of the 11 Palearctic species recognized in the genus Plecotus (Spitzenberger et al. 2006). Several authors have suggested the presence of 2 geographically separated subspecies of P. macrobullaris (Spitzenberger et al. 2003; Benda et al. 2004; Kiefer and von Helversen 2004): P. macrobullaris macrobullaris (Eastern group) and P. macrobullaris alpinus (Western group). This division is supported by the presence of 2 geographically separated mitochondrial lineages that probably diverged more than 1 million years ago (Alberdi et al. 2015b). The average mitochondrial dissimilarity between specimens of the 2 lineages is 3.4%. However, there is no information about the genomic structure of populations based on nuclear DNA, thus subspecific differentiation cannot be entirely confirmed. Additionally, the craniometric differentiation does not agree with the phylogenetic dissimilarity, as individuals from the Caucasus (Western lineage) and Alps (Eastern lineage) highly resemble each other, whereas individuals from the Balkans, Turkey, and Syria (Eastern lineage) occupy morphospaces of their own (Spitzenberger et al. 2006). Nomenclatural Notes.Plecotus macrobullaris was first described in the northern slope of the Greater Caucasus (North Ossetia) by Kuzjakin in 1965, as a subspecies of Plecotus auritus, namely P. auritus macrobullaris (Kuzjakin 1965). In 2001–2002, 2 research groups almost simultaneously reported the existence of a clade distinct from P. auritus and P. austriacus in the Austrian Alps (Spitzenberger et al. 2001; Kiefer et al. 2002). Subsequently, each research group described it as a new species (Kock 2002), assigning 2 different names: Plecotus alpinus (Kiefer and Veith 2002) and Plecotus microdontus (Spitzenberger et al. 2002). In 2003, molecular contrast between the newly described species and P. auritus macrobullaris described nearly 40 years earlier by Kuzjakin, indicated they belong to the same clade (Spitzenberger et al. 2003). Therefore, the original nomenclature was recognized as the valid name for the species, but upgraded to the species level. DIAGNOSIS Plecotus macrobullaris (Figs. 1 and 2) shares high morphological similarity with the other Plecotus species in areas where their distributions overlap, namely the brown long-eared bat P. auritus, the gray long-eared bat P. austriacus, and Kolombatovic’s long-eared bat P. kolombatovici. The most conspicuous diagnostic characteristic of P. macrobullaris is the inverted triangular-shaped chin pad that most individuals (e.g., 95% in the Swiss Alps—Ashrafi et al. 2010) exhibit below the lower lip (Spitzenberger et al. 2002). The chin pad of the other species tends to be rounded and is often darker in young individuals (Sachanowicz and Ciechanowski 2006). However, variation in color, size, and shape of the chin pad can lead to inconsistent identification. Male specimens can be identified with high reliability based on penis shape (Ashrafi et al. 2010). P. macrobullaris specimens exhibit a cylindrical penis, whereas the penis of P. austriacus and P. kolombatovici males is club-shaped and the penis of P. auritus narrows toward the end (Dietz and von Helversen 2004; Tvrtkovic et al. 2005). Although several authors have proposed other means of identification based on external qualitative characters such as the color of the ventral fur or the presence of hair on the hind feet (Kiefer and Veith 2002; Dietz and von Helversen 2004), most of them have not been validated across the entire geographic range of the species. Despite the large morphometric overlap between the 4 western Palearctic long-eared bats (Tvrtkovic et al. 2005; Ashrafi et al. 2010), a multilinear combination of 8 morphometric measurements yielded an identification success rate of 97.5% among Plecotus from Switzerland. In addition, several authors reported that the thumb length is a relatively good criterion to differentiate P. macrobullaris (> 6.2 mm) from P. austriacus and P. kolombatovici (< 6.6 mm) where these 3 species cohabit (Spitzenberger et al. 2002; Tvrtkovic et al. 2005). All the mentioned Plecotus species can be unambiguously discerned using short mitochondrial molecular markers, such as the cytochrome b or the control region (Juste et al. 2004; Spitzenberger et al. 2006), as well as the standardized COI barcode region (Agnarsson et al. 2011). Fig. 1. View largeDownload slide An adult female Plecotus macrobullaris from Aísa, Pyrenees, Spain. Photograph by A. Alberdi. Fig. 1. View largeDownload slide An adult female Plecotus macrobullaris from Aísa, Pyrenees, Spain. Photograph by A. Alberdi. Fig. 2. View largeDownload slide Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult male Plecotus macrobullaris (Natural History Museum in Belgrade 01/14) from Ćetanica plateau (Serbia), captured on 26 July 2013. Condylobasal length is 15.64 mm. Photograph by Ivana Budinski used with permission. Fig. 2. View largeDownload slide Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult male Plecotus macrobullaris (Natural History Museum in Belgrade 01/14) from Ćetanica plateau (Serbia), captured on 26 July 2013. Condylobasal length is 15.64 mm. Photograph by Ivana Budinski used with permission. GENERAL CHARACTERS Plecotus macrobullaris is a medium-sized (6–10 g, forearm length usually between 39 and 43 mm) Palearctic bat. It has the characteristic long ears of plecotine bats, which are fully erect and extended forward when echolocating and in flight, and folded and curled sideways when at rest. Ears and tragus are light brown, and eyes are fairly large and black. The face is dark brown, with a robust snout and a pinkish mandible where the inverted triangular-shaped pad usually stands out on the chin. The ventral fur is dense and usually looks whitish, often with pale yellowish highlights both sides of the neck and shoulders; the dorsal fur is typically pale gray. All hairs are bicolored in adult specimens, with a black base and lighter tips. There is no sexual dimorphism in fur coloration. The patagium is light brown and translucent, without fur. Coloration, morphometric measurements, and the length of the fur are subject to considerable geographical variation. Dental formula is i 2/3, c 1/1, p 2/3, m 3/3, total 36. Mean external biometric measurements (mm; with range and n) were: forearm length 41.2 (35.5–44.8, 195); length of hind foot 7.6 (6.6–9.0, 177); tragus length 17.2 (14.2–20.0, 166); tragus width 5.8 (5.0–7.0, 157); thumb length 6.9 (5.5–7.9, 192); and claw length 2.6 (0.9–3.6, 83—Kiefer and Veith 2002; Garin et al. 2003; Trizio et al. 2005; Tvrtkovic et al. 2005; Ashrafi et al. 2010). Females are usually larger than males (Tvrtkovic et al. 2005; Ashrafi et al. 2010). Mean craniometric measurements (mm; with range and n) were: greatest length of skull 17.0 (15.9–18.3, 82); condylocanine length 15.1 (14.1–16.1, 70); condylobasal length 15.8 (14.7–16.9, 80); height of braincase 7.6 (7.1–8.1, 80); breadth of braincase 8.5 (7.7–9.3, 75); breadth of interorbital constriction 3.5 (3.1–3.9, 81); maximum bulla diameter 4.6 (4.2–4.9, 57); anterior palatal breadth 3.8 (3.4–4.2, 75); maxillary breadth 6.3 (5.9–6.7, 81); length of upper toothrow from 1st incisor to 3rd molar 6.7 (6.3–7.2, n = 51); length of upper toothrow from canine to 3rd molar 5.6 (5.3–6.3, 87—Kiefer and Veith 2002; Spitzenberger et al. 2003; Benda et al. 2004). The cranial and dental structures are similar across the entire geographic distribution of P. macrobullaris, but the skull size and the auditory bullae tend to be smaller in the Western clade than in the Eastern clade (Spitzenberger et al. 2003). DISTRIBUTION Plecotus macrobullaris is the only bat species with a palealpine distribution (Fig. 3; i.e., widely distributed across the Palearctic, but limited to mountain environments—Alberdi et al. 2014). It is found in the main mountain ranges in the southwestern and central Palearctic, as well as the close surroundings (Alberdi et al. 2013). To date, P. macrobullaris has been found in the Pyrenees (France and Spain—Garin et al. 2003; Alberdi et al. 2013), Alps (Austria, France, Italy, Liechtenstein, Slovenia, Switzerland—Chirichella et al. 2003; Kiefer and von Helversen 2004; Trizio et al. 2005; Spitzenberger et al. 2006; Presetnik et al. 2009; Mattei-Roesli 2010; Rutishauser et al. 2012), Dinaric Alps (Albania, Bosnia-Herzegovina, Croatia, Macedonia, Montenegro, Serbia—Juste et al. 2004; Tvrtkovic et al. 2005; Sachanowicz and Ciechanowski 2006; Bekker and Boshamer 2007; Budinski et al. 2016), Pindos Mountains (Greece—Alberdi et al. 2013), several mountain ranges in Turkey (Kaçkar, Taurus, Guneydogu Toroslar—Karatas and Sozen 2006), Greater Caucasus (Georgia, Russia—Spitzenberger et al. 2006; Kiefer 2008; Alberdi et al. 2013), Lower Caucasus (Armenia, Azerbaijan—Kiefer 2008), Anti-Lebanon (Syria—Benda et al. 2006), and the Iranian Alborz and Zagros Mountains (Benda et al. 2012). P. macrobullaris has been also found on 2 Mediterranean islands: Corsica and Crete (Kiefer and von Helversen 2004; Benda et al. 2008). Fig. 3. View largeDownload slide Geographic distribution of Plecotus macrobullaris. The 2 matrilineal clades are: 1, Western clade (P. m. alpinus); 2, Eastern clade (P. m. macrobullaris). Fig. 3. View largeDownload slide Geographic distribution of Plecotus macrobullaris. The 2 matrilineal clades are: 1, Western clade (P. m. alpinus); 2, Eastern clade (P. m. macrobullaris). The elevational range of P. macrobullaris spans from sea level up to about 2,800 m, even though there are considerable differences between geographic areas. Almost all records in the Pyrenees and the Zagros mountains are above 1,500 m, but the species can be found at considerably lower elevations in very steep and mountainous regions. In such regions, P. macrobullaris shows an extremely wide elevational distribution (e.g., in the Alps it can be found between 200 and 2,200 m—Alberdi et al. 2013), and in Croatia from sea level up to mountain tops (Pavlinic and Tvrtkovic 2004). No fossils are known. FORM AND FUNCTION Echolocation calls are fairly similar to other Plecotus species. Plecotus macrobullaris emits multiharmonic, downward frequency-modulated signals consisting mostly of the 1st and the lower part of the 2nd harmonic (Dietrich et al. 2006; Barataud 2014). The 1st harmonic starts at about 46 kHz and ends around 23 kHz, with a peak frequency around 35 kHz. The 2nd harmonic starts around 67 kHz and does not overlap with the 1st harmonic. The pulse length varies considerably depending on the surrounding environment, emitting short signals (up to 0.8 ms) when flying close to the clutter, and long signals (up to 7.3 ms) when flying far from the clutter. The longer the signal the lower the frequency band and the peak frequency. Although P. macrobullaris is genetically more closely related to P. auritus, its signal structure is closer to that of P. austriacus. ECOLOGY Plectous macrobullaris females aggregate in small groups (5–25) to form breeding colonies (Ashrafi et al. 2010). These colonies may contain several nulliparous females, with an occasional presence of male bats (Alberdi et al. 2015a). Distribution records indicate that P. macrobullaris is ecologically linked to mountain environments (Kiefer and Veith 2002; Alberdi et al. 2013), although it is not restricted to high elevations (Pavlinic and Tvrtkovic 2004; Ashrafi et al. 2010). Using an ecological niche modeling approach, Alberdi et al. (2014) concluded that the broad-scale distribution of P. macrobullaris is mainly shaped by topographic factors, as it is found in areas with very steep topography but missing in flatlands. In contrast, the relative influence of climatic factors was much lower, as the distribution of P. macrobullaris covers a very broad climatic range, from the extremely cold and rainy Alps to the warm and dry mountains in the Middle East. Alberdi et al. (2014) suggested that its fondness for steep environments might be the result of increased availability of rocky and open-space areas that would provide appropriate foraging and roosting environments for P. macrobullaris. However, the study of roosting and foraging preferences of P. macrobullaris has yielded contrasting results. Most of the known roosting sites of P. macrobullaris are man-made buildings (Alberdi et al. 2013). In fact, it is one of the most common species found in church attics in the Alps (Rutishauser et al. 2012). Nevertheless, results of a radiotracking study performed in the Pyrenees depicted a very different behavior. Alberdi et al. (2015a) captured 51 free-flying P. macrobullaris, and radiotracked them to their roosting sites. Most bats sheltered in rock crevices, and many males and nulliparous females made systematic use of scree deposits as roosts. Many of those roosting sites were found in alpine environments (above the upper forest treeline). Only 3 of the 51 tracked bats, all of them breeding females, roosted in buildings. The authors considered 2 possible explanations for the contrasting results. Bats (mainly breeding females) might make use of buildings more often in the Alps than in the Pyrenees because the climatic conditions are colder (about 2°C at the same elevation). Conversely, almost all the records in the Alps come from surveys of building that were considered suitable a priori, which entails a systemic bias toward man-made buildings. Similarly, the few roosts that were known in the Pyrenees before the radiotracking study were also buildings (Alberdi et al. 2015a). Bats might also use natural roosting resources in the Alps, but the previously described approaches may not be suitable for revealing the entire roosting spectrum of P. macrobullaris. Plecotus macrobullaris has been also found in caves, mostly in the southeastern area of its distribution (Benda et al. 2008, 2012). Probably, it was originally linked to karstic areas with high availability of rock crevices, scree slopes, and caves. In fact, this preference to limestone environments can be still seen in the Pyrenees Mountains and Croatia (Tvrtkovic et al. 2005; Alberdi et al. 2013). However, P. macrobullaris has been able to take advantage of relatively new roosting resources such as man-made buildings. Finally, a male P. macrobullaris was documented using tree hole indicating that they might occasionally use alternate types of roosts. These results depict a flexible roosting behavior, and suggest that depending on the environmental conditions, as well as sexual and reproductive status, P. macrobullaris bats may exhibit different roosting preferences (Fig. 4). Fig. 4. View largeDownload slide Some of the most common roosting resources used by Plecotus macrobullaris. (A) Church in Kupljenik, Slovenia (632 m), where a small (5 adults) maternity colony was identified in 2012. (B) Crack (exact location indicated by the green arrow) in a large rock wall in Valle de Tena, Spain (2,250 m), where a maternity colony of > 10 individuals was located in 2013. A red circle indicates the presence of a researcher. (C) Talus slope in Valle de Aísa, Spain (1,450 m), where a nulliparous female was located for several days in 2013. (D) A female P. macrobullaris and its pup in a church attic in Laas, Italy, in July 2012 (920 m). (E) A male P. macrobullaris roosted in a crack in Currundué, Spain (1,740 m), in July 2013. (F) A male P. macrobullaris roosted in a scree deposit in Valle de Añisco, Spain (2,140 m), in July 2013. Fig. 4. View largeDownload slide Some of the most common roosting resources used by Plecotus macrobullaris. (A) Church in Kupljenik, Slovenia (632 m), where a small (5 adults) maternity colony was identified in 2012. (B) Crack (exact location indicated by the green arrow) in a large rock wall in Valle de Tena, Spain (2,250 m), where a maternity colony of > 10 individuals was located in 2013. A red circle indicates the presence of a researcher. (C) Talus slope in Valle de Aísa, Spain (1,450 m), where a nulliparous female was located for several days in 2013. (D) A female P. macrobullaris and its pup in a church attic in Laas, Italy, in July 2012 (920 m). (E) A male P. macrobullaris roosted in a crack in Currundué, Spain (1,740 m), in July 2013. (F) A male P. macrobullaris roosted in a scree deposit in Valle de Añisco, Spain (2,140 m), in July 2013. Roosting-site habitat selection has also produced contrasting results. Rutishauser et al. (2012) reported that P. macrobullaris chooses buildings surrounded by forest environments, although Alberdi et al. (2015a) found that most roosts were located closer to meadows and open forests, and further away from deciduous forest and shrubbery. These conflicting results might reflect a geographical trend (i.e., bats roost closer to forest in the Alps than in the Pyrenees), or it might be due to the differences in the employed approaches and the roosting resources that were examined. Rutishauser et al. (2012) studied the location of man-made buildings where P. macrobullaris was found roosting, but Alberdi et al. (2015a) analyzed the roosts spotted after radiotracking free-ranging bats, mainly natural rock cracks and scree deposits. Interestingly, the building roosts identified in the latter study were located close to or surrounded by forest (Alberdi et al. 2015a). Regarding foraging preferences, the abundant captures performed hundreds of meters above the upper forest limit (Alberdi et al. 2013), the roosts located far from forest environments (Alberdi et al. 2015a), and the open-space moth species identified in its diet (Alberdi et al. 2012) suggest that, at least in the Pyrenees, P. macrobullaris is an open-space forager. However, this pattern largely contrasts with the observations reported from the Swiss Alps, where Ashrafi et al. (2013) concluded that P. macrobullaris avoids grasslands and selects its foraging habitat according to the heterogeneity of vertical vegetation structures. Similarly, Pavlinic and Tvrtkovic (2004) reported that in Croatia the species appears linked to deciduous forests, but P. macrobullaris has never been observed in forests in the Pyrenees (Alberdi et al. 2013). To further blur the picture of foraging preferences of P. macrobullaris, another radiotracking study carried out in the Italian Alps concluded that P. macrobullaris avoids woodlands (Preatoni et al. 2011). Two radiotracking studies indicated that the foraging range of P. macrobullaris is usually below 4 km (Ashrafi 2010; Preatoni et al. 2011), although displacement of up to 7 km, and elevation differences of more than 1,000 m have been recorded in a single night (Alberdi et al. 2015a). The diet of P. macrobullaris is mainly composed of moths (Order Lepidoptera), although it also consumes coleopterans and dipterans (Ashrafi et al. 2011; Alberdi et al. 2012). Most moth species identified in its diet belong to the family Noctuidae, and 96% of prey species (Alberdi et al. 2012) identified using molecular methods were tympanate moths (i.e., species that can detect bats’ echolocation calls—Goerlitz et al. 2010). Multiple ecological and distribution data suggest the existence of competitive exclusion between P. macrobullaris and P. austriacus. Both species use similar open and semi-open areas for foraging, and their diets are basically composed of grassland moth species (Razgour et al. 2011; Alberdi et al. 2012). Conversely, the trophic niche of P. auritus is different, as it also includes nonflying arthropods and is basically composed of woodland prey (Ashrafi et al. 2011; Razgour et al. 2011). There are also large similarities in echolocation signals and flight behavior (Dietrich et al. 2006). All these ecological resemblances likely yield a parapatric distribution of P. austriacus and P. macrobullaris in many geographic areas. In Switzerland P. austriacus occupies the Northern lowland areas, while P. macrobullaris is restricted to the mountainous regions (Rutishauser et al. 2012). A similar geographical split is also observed in Croatia, where P. macrobullaris seems to be restricted to the karstic areas (Tvrtkovic et al. 2005). In the southern slopes of the Pyrenees Mountains, the parapatric distribution responds to an altitudinal pattern rather than to a geographical one. In that mountain range, P. macrobullaris occupies the highest open areas and P. austriacus is found in lower zones (Alberdi et al. 2013). There are also exceptions where both species can be found together, such as the Swiss city of Genève (Rutishauser et al. 2012), or several subalpine areas in the Pyrenees (Alberdi et al. 2013). As occurs with the other Plecotus species, P. macrobullaris emits very faint echolocation pulses (Dietrich et al. 2006). These pulses attenuate rapidly, making it almost impossible for most ultrasound detectors to record P. macrobullaris even from 5 m of distance. In addition, differentiation from other Plecotus species is also very challenging (Barataud 2014). Consequently, its presence and abundance can be overlooked or underestimated in biodiversity surveys solely based on echolocation detection. Additionally, Alberdi et al. (2013) reported a surprisingly meager capture success of P. macrobullaris individuals in water points, suggesting that other capture techniques such as setting long net-chains in open areas should be employed to increase capture efficiency and obtain a better picture of abundance of this species. BEHAVIOR When roosting in man-made buildings Plectous macrobullaris is usually found forming monospecific colonies, although it has been occasionally observed sharing attics with other Plecotus species; specifically P. kolombatovici and P. auritus (Tvrtkovic et al. 2005; Ashrafi et al. 2010). In caves it has been found along with species of Rhinolophus and Myotis (Benda et al. 2012). Roost fidelity varies according to the type of roosting resource used, as well as the sex and reproductive condition of the individual. Individuals roosting in man-made buildings show very high roost fidelity and bats roosting in natural rock crevices exhibit slightly less fidelity. The lowest fidelity is found in the use of scree deposits, as these bats change their roosting location almost every day (Alberdi et al. 2015a). Regarding sex and reproductive condition, breeding females barely change their roosting sites, nulliparous females show intermediate fidelity, although males exhibit a very labile behavior, switching their roosts almost every day (Alberdi et al. 2015a). There is no confirmed data about the hibernation behavior of P. macrobullaris. The only known information is based on 2 observations of Plecotus specimens hibernating in caves with ice formations above > 2,000 m in the Pyrenees Mountains and the Slovenian Alps (Kryštufek 1987; Aihartza 1992). As both observations are prior to the description of P. macrobullaris, they were not identified as such. However, the knowledge on the ecology of Plecotus bats suggests that those observations most probably belong to P. macrobullaris. GENETICS Despite the morphological and ecological similarity to Plectous austriacus (Ashrafi et al. 2011), P. macrobullaris belongs to the so-called “auritus group” (Juste et al. 2004; Spitzenberger et al. 2006). This group is divided into 2 main mitochondrial clades, between which 79.5% of the total genetic variation occurs (Alberdi et al. 2015b). The presence of these 2 matrilineal lineages was reported by the 1st molecular analyses of P. macrobullaris (Spitzenberger et al. 2003), and was later confirmed using complete mitochondrial genomes (Alberdi et al. 2015b). The 1st analyses based on short mitochondrial markers (e.g., control region) showed differences of about 2.5% between the 2 lineages (Spitzenberger et al. 2003), although the complete mitochondrial sequences exhibited larger overall differentiation, namely 3.4% (Alberdi et al. 2015b). All the individuals from the Pyrenees and the Alps belong to the Western clade (Alberdi et al. 2015b), while the individuals from the other mountain ranges belong to the Eastern clade. Hence, the current contact zone involving the 2 lineages is located between the Eastern Alps and the Dinaric Alps (Eastern Italy, Slovenia, and Northern Croatia). All molecularly characterized individuals from Eastern Italy and Slovenia but 1 belongs to the Western clade, while all individuals from Croatia belong to the Eastern clade (Spitzenberger et al. 2006; Alberdi et al. 2015b). Based on complete mitochondrial genomes, Alberdi et al. (2015b) reported that both lineages split more than 1 million year ago, before the beginning of the large Pleistocene climatic oscillations. Using paleoclimatic niche reconstructions the authors estimated that the Dinarides (Croatia) remained ecologically unsuitable for most of the time during the Pleistocene, which could have acted as a natural ecological barrier that prevented the interbreeding between the lineages. The genetic structure of both populations is rather different, reflecting different paleodemographic histories. The Eastern lineage conserves considerably larger genetic diversity than the Western lineage. The Eastern lineage began to diversify around 900,000 years ago and exhibits marked population structure. Conversely, the most recent common female ancestor of the Western lineage was estimated to live about 68,000 years ago, and diversification probably occurred after the last glaciation (Alberdi et al. 2015b). CONSERVATION Plectous macrobullaris is listed as “Least Concern” by the International Union for Conservation of Nature and Natural Resources (Hutson et al. 2016), but due to its recent discovery the actual conservation status of P. macrobullaris is still uncertain. However, the abundant captures performed in high-mountain environments (Alberdi et al. 2013), as well as the large number of roosts found in buildings in the Alps (Rutishauser et al. 2012) and the Dinarides (Pavlinic and Tvrtkovic 2004) suggest that it is currently a relatively abundant species in mountainous environments. Although in the Pyrenees Mountains the species has been mainly found in natural roosts (Alberdi et al. 2015a), most breeding colonies known in the Alps are in the attics of man-made structures, specifically churches (Rutishauser et al. 2012). Hence, the conservation and management of such buildings are important for the conservation of the species. Because the Alps are one of the coldest regions in the geographic distribution of P. macrobullaris, the availability of warm shelters suitable for breeding, such as church attics, might be essential for the conservation of P. macrobullaris in the region. Synonymy completed 2 November 2017 Version of Record, first published online May 9, 2018, with fixed content and layout in compliance with Art. 8.1.3.2 ICZN. Nomenclatural statement.—A life science identifier (LSID) number was obtained for this publication: urn:lsid:zoobank.org:pub:CBE7455F-57F2-4CA7-A126-D4EF8F8C6D24 LITERATURE CITED Agnarsson , I. , C. M. Zambrana-Torrelio , N. P. Flores-Saldana , and L. J. May-Collado . 2011 . A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia) . PLoS Currents 3 : RRN1212 . Google Scholar CrossRef Search ADS PubMed Aihartza , J . 1992 . Ipar-belarrihandia, bitxia bezain ezezaguna . Elhuyar 60 : 25 – 27 . Alberdi , A. , I. Garin , O. Aizpurua J. Aihartza . 2012 . The foraging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes . PLoS One 7 : e35692 . Google Scholar CrossRef Search ADS PubMed Alberdi , A. , I. Garin , O. Aizpurua J. Aihartza . 2013 . Review on the geographic and elevational distribution of the mountain long-eared bat Plecotus macrobullaris, completed by utilising a specific mist-netting technique . Acta Chiropterologica 15 : 451 – 461 . Google Scholar CrossRef Search ADS Alberdi , A. , O. Aizpurua , J. Aihartza I. Garin . 2014 . Unveiling the factors shaping the distribution of widely distributed alpine vertebrates, using multi-scale ecological niche modelling of the bat Plecotus macrobullaris . Frontiers in Zoology 11 : 77 . Google Scholar CrossRef Search ADS PubMed Alberdi , A. , J. Aihartza , O. Aizpurua , E. Salsamendi , M. Brigham I. Garin . 2015a . Living above the treeline: roosting ecology of the alpine bat Plecotus macrobullaris . European Journal of Wildlife Research 61 : 17 – 25 . Google Scholar CrossRef Search ADS Alberdi , A. , M. T. P. Gilbert , O. Razgour , O. Aizpurua , J. Aihartza I. Garin . 2015b . 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 : 1689 – 1700 . Google Scholar CrossRef Search ADS Ashrafi , S . 2010 . Resource partitioning in three cryptic, sympatric bat species (Plecotus spp.) with contrasting conservation status . Ph.D. dissertation , Universität Bern , Bern, Switzerland . Ashrafi , S. , A. Beck , M. Rutishauser , R. Arlettaz F. Bontadina . 2011 . Trophic niche partitioning of cryptic species of long-eared bats in Switzerland: implications for conservation . European Journal of Wildlife Research 57 : 843 – 849 . Google Scholar CrossRef Search ADS Ashrafi , S. , F. Bontadina , A. Kiefer , I. Pavlinic R. Arlettaz . 2010 . Multiple morphological characters needed for field identification of cryptic long-eared bat species around the Swiss Alps . Journal of Zoology 281 : 241 – 248 . Google Scholar CrossRef Search ADS Ashrafi , S. , M. Rutishauser , K. Ecker , M. K. Obrist , R. Arlettaz F. Bontadina . 2013 . Habitat selection of three cryptic Plecotus bat species in the European Alps reveals contrasting implications for conservation . Biodiversity and Conservation 22 : 2751 – 2766 . Google Scholar CrossRef Search ADS Barataud , M . 2014 . Écologie acoustique des chiroptères d’Europe . Biotope Éditions , Meze, France . Bekker , J. J. Boshamer . 2007 . First records of Plecotus auritus (Linnaeus, 1758) and Plecotus macrobullaris Kuzjakin, 1965 in the Republic of Macedonia . Lutra 50 : 43 – 48 . Benda , P. , et al. 2006 . Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 4. Bat fauna of Syria: distribution, systematics, ecology . Acta Societatis Zoologicae Bohemicae 70 : 1 – 329 . Benda , P. , et al. 2012 . Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 10. Bat fauna of Iran . Acta Societatis Zoologicae Bohemicae 76 : 163 – 582 . Benda , P. , P. Georgiakakis C. Dietz . 2008 . Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 7. The bat fauna of Crete, Greece . Acta Societatis Zoologicae Bohemicae 72 : 105 – 190 . Benda , P. , A. Kiefer , V. Hanak M. Veith . 2004 . Systematic status of African populations of long-eared bats, genus Plecotus (Mammalia: Chiroptera) . Folia Zoologica 53 : 1 – 47 . Budinski , I. , B. Karapandza , V. Josipovic , J. Jovanovic M. Paunovic . 2016 . The first record of alpine long-eared bat Plecotus macrobullaris in Serbia . Turkish Journal of Zoology 40 : 984 – 988 . Google Scholar CrossRef Search ADS Chirichella , R. , et al. 2003 . The Adamello-Brenta Natural Park bat community (Mammalia, Chiroptera): distribution and population status . Hystrix 14 : 29 – 45 . Dietrich , S. , D. P. Szameitat , A. Kiefer , H. U. Schnitzler A. Denzinger . 2006 . Echolocation signals of the plecotine bat, Plecotus macrobullaris Kuzyakin, 1965 . Acta Chiropterologica 8 : 465 – 475 . Google Scholar CrossRef Search ADS Dietz , C. O. von Helversen . 2004 . Illustrated identification key to the bats of Europe . Dietz & von Helversen, Electronic Publication. Garin , I. , J. L. Garcia-Mudarra , J. Aihartza , U. Goiti J. Juste . 2003 . Presence of Plecotus macrobullaris (Chiroptera: Vespertilionidae) in the Pyrenees . Acta Chiropterologica 5 : 243 – 250 . Google Scholar CrossRef Search ADS Goerlitz , H. R. , H. M. ter Hofstede , M. R. K. Zeale , G. Jones , and M. W. Holderied . 2010 . An aerial-hawking bat uses stealth echolocation to counter moth hearing . Current Biology 20 : 1568 – 1572 . Google Scholar CrossRef Search ADS PubMed Hutson , A. M. , S. Aulagnier , J. Juste , A. Karataş , J. Palmeirim M. Paunović . 2016 . Plecotus macrobullaris. The International Union for Conservation of Nature and Natural Resources red list of threatened species . http://www.iucnredlist.org/details/136229/0. Accessed 31 December 2017 . Juste , J. , et al. 2004 . Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands . Molecular Phylogenetics and Evolution 31 : 1114 – 1126 . Google Scholar CrossRef Search ADS PubMed Karatas , A. M. Sozen . 2006 . Bats of the middle and upper Kızılırmak regions, Central Anatolia, Turkey . Lynx 37 : 151 – 159 . Kiefer , A . 2008 . Phylogeny of Western Palaearctic long-eared bats (Mammalia, Chiroptera, Plecotus) – a molecular perspective . Johannes Gutenberg-Universität , Mainz, Germany . Kiefer , A. O. von Helversen . 2004 . Plecotus macrobullaris (Kuzjakin, 1965) - Alpenlangohr . Pp. 1051 – 1058 in Handbuch der Säugetiere Europas - Fledertiere II ( F. Krapp , ed.). AULA-Verlag , Wiebelsheim, Germany . Kiefer , A. M. Veith . 2002 . A new species of long-eared bat from Europe (Chiroptera: Vespertilionidae) . Myotis 39 : 5 – 16 . Kiefer , A. , F. Mayer , J. Kosuch , O. von Helversen M. Veith . 2002 . Conflicting molecular phylogenies of European long-eared bats (Plecotus) can be explained by cryptic diversity . Molecular Phylogenetics and Evolution 25 : 557 – 566 . Google Scholar CrossRef Search ADS PubMed Kock , D . 2002 . The publication dates of Plecotus alpinus Kiefer and Veith, 2002 and of Plecotus microdontus Spitzenberger, 2002 . Acta Chiropterologica 4 : 219 – 220 . Google Scholar CrossRef Search ADS Kryštufek , B . 1987 . Distribution of bats in Slovenia (Yugoslavia) . In European bat research 1987 ( V. Hanak , I. Horáček , and J. Gaisler , eds.). Charles University Press , Praha, Czech Republic 399 – 401 . Kuzjakin , A . 1965 . Otrjad Rukokrylyje. Ordo Chiroptera . In Opredelitel mljekopitayushtshikh SSSR ( N. Bobrinskij , B. Kuznetsov , and A. Kuzjakin , eds.). Isd. Prosveshtshenije Moscow 79 – 116 . Mattei-Roesli , M . 2010 . Situazione del genere Plecotus (Chiroptera) nel Cantone Ticino (Svizzera) . Bollettino della Società ticinese di Scienze naturali 98 : 31 – 34 . Pavlinic , I. N. Tvrtkovic . 2004 . Altitudinal distribution of four Plecotus species (Mammalia, Vespertilionidae) occurring in Croatia . Natura Croatica 13 : 395 – 401 . Preatoni , D. , M. Spada , L. Wauters , G. Tosi A. Martinoli . 2011 . Habitat use in the female Alpine long-eared bat (Plecotus macrobullaris): does breeding make the difference ? Acta Chiropterologica 13 : 355 – 364 . Google Scholar CrossRef Search ADS Presetnik , P. , K. Koselj M. Zagmajster . 2009 . Atlas netopirjev (Chiroptera) Slovenije. Atlas of bats (Chiroptera) of Slovenia . Miklavž na Dravskem polju: Center za kartografijo favne in flore , Ljubljana, Slovenia . Razgour , O. , et al. 2011 . High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species . Ecology and Evolution 1 : 556 – 570 . Google Scholar CrossRef Search ADS PubMed Rutishauser , M. D. , F. Bontadina , V. Braunisch , S. Ashrafi R. Arlettaz . 2012 . The challenge posed by newly discovered cryptic species: disentangling the environmental niches of long-eared bats . Diversity and Distributions 18 : 1107 – 1119 . Google Scholar CrossRef Search ADS Sachanowicz , K. M. Ciechanowski . 2006 . Plecotus macrobullaris – new bat species for Albanian fauna (Chiroptera: Vespertilionidae) . Lynx (Praha) 37 : 241 – 246 . Spitzenberger , F. , E. Haring N. Tvrtkovic . 2002 . Plecotus microdontus (Mammalia, Vespertilionidae), a new bat species from Austria . Natura Croatica 11 : 1 – 18 . Spitzenberger , F. , J. Pialek E. Haring . 2001 . Systematics of the genus Plecotus (Mammalia, Vespertilionidae) in Austria based on morphometric and molecular investigations . Folia Zoologica 50 : 161 – 172 . Spitzenberger , F. , P. Strelkov E. Haring . 2003 . Morphology and mitochondrial DNA sequences show that Plecotus alpinus Kiefer & Veith, 2002 and Plecotus microdontus Spitzenberger, 2002 are synonyms of Plecotus macrobullaris Kuzjakin, 1965 . Natura Croatica 12 : 39 – 53 . Spitzenberger , F. , P. Strelkov , H. Winkler E. Haring . 2006 . A preliminary revision of the genus Plecotus (Chiroptera, Vespertilionidae) based on genetic and morphological results . Zoologica Scripta 35 : 187 – 230 . Google Scholar CrossRef Search ADS Trizio , I. , et al. 2005 . First record of the alpine long-eared bat (Plecotus macrobullaris Kuzjakin, 1965) in Lombardy (Northern Italy) revealed by DNA analysis . Natura Bresciana 34 : 171 – 175 . Tvrtkovic , N. , I. Pavlinic E. Haring . 2005 . Four species of long-eared bats (Plecotus, Geoffroy, 1818; Mammalia, Vespertilionidae) in Croatia: field identification and distribution . Folia Zoologica 54 : 75 – 88 . © The Author(s) 2018. Published by Oxford University Press on behalf of American Society of Mammalogists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

Mammalian Species – Oxford University Press

Published: May 9, 2018

References

  • A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia)
    Agnarsson
  • Ipar-belarrihandia, bitxia bezain ezezaguna
    Aihartza
  • The foraging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes
    Alberdi
  • Review on the geographic and elevational distribution of the mountain long-eared bat Plecotus macrobullaris, completed by utilising a specific mist-netting technique
    Alberdi
  • Unveiling the factors shaping the distribution of widely distributed alpine vertebrates, using multi-scale ecological niche modelling of the bat Plecotus macrobullaris
    Alberdi
  • Living above the treeline: roosting ecology of the alpine bat Plecotus macrobullaris
    Alberdi
  • Contrasting population-level responses to Pleistocene climatic oscillations in an alpine bat revealed by complete mitochondrial genomes and evolutionary history inference
    Alberdi