Of Various Habitat Types in Moldova and the Danube Delta (Romania)

Home , Eptesicus, Vespertilionidae

Travaux du Muséum National d’Histoire Naturelle © 30 Juin Vol. LIV (1) pp. 223–242 «Grigore Antipa» 2011 DOI: 10.2478/v10191-011-0014-2

THE USE BY BATS (CHIROPTERA: VESPERTILIONIDAE) OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA (ROMANIA)

IRINA POCORA, VIOREL POCORA

Abstract. Our investigations were carried out in Moldova and the Danube Delta areas during summer periods of 2006-2010. The habitat types which were investigated were: 23 humid areas, 13 woodlands, 7 settlements – streetlamps, 25 car transects. Woodlands and humid areas are the most important habitat types to the majority of bat species, whereas the habitats along roads (mostly made in open areas) are less important. Pipistrellus kuhlii and Nyctalus noctula, also Eptesicus serotinus, Nyctalus leisleri and Vespertilio murinus proved generalists in using foraging habitats, these species being most frequently recorded. In the humid areas, Nyctalus noctula (25.2%), Myotis sp. (24%) and Pipistrellus nathusii/Pipistrellus kuhlii (22.3%) are the most abundant species. In the woodlands, Nyctalus noctula is the most abundant species (19.5%), followed by Pipistrellus nathusii/Pipistrellus kuhlii (17.6%) and Myotis sp. (11.2%). Along the roads, Nyctalus noctula (44%) and Eptesicus serotinus (13.2%) are the most abundant species. At the streetlamps, Nyctalus noctula (45.4%) and Nyctalus leisleri (12.8%) are the most abundant species. In the settlements, Pipistrellus kuhlii (26%) and Nyctalus noctula (23%) are the most abundant species. Résumé. Nos recherches ont été déroulées en Moldavie et dans le Delta du Danube durant la période de la saison chaude, de 2006 à 2010. Les types d’habitats qui ont été étudiés sont: 23 zones humides, 13 forêts, 7 localités - les pôles de lumière, 25 transects en voiture. Les forêts et les zones humides sont les plus importants habitats pour la plupart des espèces de chauves-souris, tandis que les habitats le long des routes (principalement représentées par des zones ouvertes) sont moins importants. Les espèces Pipistrellus kuhlii et Nyctalus noctula mais aussi Eptesicus serotinus, Nyctalus leisleri et Vespertilio murinus sont généralistes en utilisation des habitats d’alimentation, donc elles sont les espèces plus fréquemment signalées. Dans les zones humides Nyctalus noctula (25,2%), Myotis sp. (24%) et Pipistrellus nathusii/Pipistrellus kuhlii (22,3%) sont les espèces les plus abondantes. Dans les habitats forestiers, l’espèce la plus abondante est Nyctalus noctula (19,5%), suivie par Pipistrellus nathusii/Pipistrellus kuhlii (17,6%) et Myotis sp. (11,2%). Le long des routes, les espèces les plus abondantes sont Nyctalus noctula (44%) et Eptesicus serotinus (13,2%). Près des pôles de lumière Nyctalus noctula (45,4%) et Nyctalus leisleri (12,8%) sont les espèces les plus abondantes. Dans les localités, les espèces les plus abondantes sont Pipistrellus kuhlii (26%) et Nyctalus noctula (23%). Key words: bats, habitat use, summer period, echolocation, ecology.

INTRODUCTION It is essential to identify the habitat types and characteristics preferred by bat species to define appropriate conservation guidelines and to apply effective protection measures. Habitat selection is one of the principal components of the species ecology, which permits species to coexist (Rosenzweig, 1981). Little is known regarding the degree of habitat specialization in bats, but it is largely presumed that most insectivorous species are habitat generalists and feed opportunistically as prey are observed (Altringham, 1996). However there is some evidence suggesting preferences for some available types of habitat over others (Sherwin et al., 2000). Forests are the most important foraging habitats for bats (Cel’uch & Kropil, 2008). Forests and other woodland habitats positively affect 224 IRINA POCORA, VIOREL POCORA foraging activity and roost availability for many species of bats (Myotis sp.) (Jaberg & Guisan, 2001). The importance of riparian foraging habitats, observed by us confirms findings for other geographical areas (Vaughan et al., 1996; Mickevièiene & Mickevièinus, 2001; Jaberg & Guisan, 2001; Russo & Jones, 2003). Romania is an area of high bat species diversity, being identified 31 bat species so far. Such high number of species makes the acoustic identification of bats in flight an especially challenging task. 26 of the 31 bat species in Romania are considered critically endangered, endangered or vulnerable (Botnariuc & Tatole, 2005). Data concerning the bat populations present in Romania are few and they are referring especially to the bat populations from caves and less to those from buildings. Most of the forests from Romania were cut, regenerating forests probably will never resemble with those that have been cut, and old pieces that were left are small and isolated. Landscapes, in which these fragments of ancient forest remain, differ remarkable from the original conditions, that their value as habitat for many species of wild animals, including bats, is unknown. By the '70s, aquatic wetland areas in eastern Romania were part of a huge wetland consisting of lakes and estuary hook, whose rivers once regularly flooded them with melting snow. By the '70s, planning of the rivers of eastern Romania began in order to stop flooding and obtain new areas for intensive agriculture. Therefore many dam lakes have been built. Gravel beds have been studded by a network of drainage channels. All the meadow and riparian forests have been cleared and poplar and willow plantations were created, in areas between dam and river. Most lawns have been cleared (Ion, 2007). The fragmentation of the forests, reduction of humid area surfaces, agricultural intensification and other man made activities, the lack of connection elements (bushes, rows of trees, isolated trees) from the habitats preferred by bats, make the area of Moldova to be the area with the lowest diversity of chiropterofauna of the country. In our study, a large number of endangered or vulnerable species featured in riparian habitats and broadleaved woodlands, these habitats constituting an important target for conservation. The forested areas limited by humid areas and connection elements between habitats (rows of trees, bushes) are key habitats for bats. The aim of this study was to identify the exploitation of foraging habitats by bats in the Danube Delta and Moldova areas (Romania) as revealed by acoustic surveys. This is the first study on bat habitat use ever conducted in the region. From this study, it is obvious that key habitats play an important role for bat populations and that more information on habitat selection is needed to improve the conservation of bats.

MATERIAL AND METHODS Study sites The investigations have performed in fifty-five sites, situated in the Danube Delta and Moldova areas. We investigated the following 4 habitat types: 1) 23 humid areas (4 channels near Letea: Letea channel, Sulina-Letea channel, Magearu channel, Sulimanca channel – near Merhei lake; Sulina and Busurca channels; Gârla Turceascã/Serenea (Sfântu Gheorghe) channel and Rãdãcinoasele channel (Chilia Veche) – the Danube Delta; Brateº channel (GL), Danube River (GL), Prut (GL), THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 225 Bahlui (IS) and Siret (IS) rivers, Pruteþul Bãlãtãu (IS), Roºu (NT), Roºcani (VS) and Puºcaºi (VS) lakes, fish-breeding farms Larga Jijia (IS), Iezãr – Dorohoi (BT) and Cârja (VS) - Moldova), the width of water flows varied from 7 m to 150 m; 2) 13 woodlands (Letea Forest – the Danube Delta; woodland areas near the Danube river (GL), Prut (GL), Siret (GL and IS), Bãlãtãu (IS); Fãlciu (VS); Bicaz Gorges (NT), Vânãtori-Neamþ Natural Park (NT); Roºcani (IS), Lunca Mirceºti (IS) and Bãdeana (VS) forests, Bârlad’s park (VS), Botanical Garden of Iaºi (IS) - Moldova), if more than 50% of the territory surveyed with a detector was overgrown with trees; 3) 7 settlements – streetlamps (Letea and Chilia villages, Sulina town – the Danube Delta; Secu Monastery (NT), Iaºi town, Deleni, Crâng and Viiºoara (VS) villages - Moldova) and 4) 25 car surveys along roads (mostly in open habitat). The importance of habitat types to bats was estimated not only according to the differences of the frequency of each species within them but also according to the mean number of the passes of the detected species. Abbreviations County names: BT – Botoºani, GL – Galaþi, IS – Iaºi, NT – Neamþ, TL – Tulcea, VS – Vaslui. Sampling design and sound recording We conducted sampling from 2006 to 2010, from March to September. The records were made based on transects and in fixed points. In some habitats there were made only transects, in others before or after transect there were made records in fixed points. At the feeding places on the water bodies, at streetlamps, there were made records only from fixed points. Transects had the length of 1-2 km, and were made in semi-opened habitats (forest border, forest road) and opened habitats (glades, outside the forest, settlements, channels, rivers, lakes); excepting those made on the roads using a slowly going car (25 km/h), for one hour. In 6 sites (channels from Danube Delta and near Galaþi) transects were covered by boat. The medium speed of transects made on foot was of 3.8-4 km/h and of 4.5-5 km/h in those by the boat. Transects were started 30-40 min immediately after the sunset (or after 50-60 min at the feeding places). The records from fixed points and from transects were of about 20 min, excepting those along roads, of one hour. 64 hours of records were analyzed. The number of bat passes recorded in each site was used as an indication of bat activity. A bat pass is the continuous string of echolocation calls heard on a bat detector as a bat flies within range (Vaughan et al., 1996). When recording, we minimized the use of lights to avoid any interference with bat activity (Russo & Jones, 2003). Intensive population surveys of bats are difficult to conduct because of their nocturnal behavior, their wide home range and the problems related to species identification in flight (Jaberg & Guisan, 2001). Effective monitoring of echolocation calls is vital in many studies of the ecology and conservation of bats (Parsons & Jones, 2000). Bat activity may be successfully surveyed using ultrasound detectors. In temperate regions it is generally easier to accumulate large date sets using acoustical techniques than using traditional netting. The data were collected with the detector with time expansion (Tranquility); the ultrasounds of the bats that were passing near the detector microphone were recorded on a Sony (MZ-NH600 Silver). Afterwards, with the help of software (Batsound Pro version 3.31), sonograms were created, from which the bat species were identified. We used sample frequency of 44.1 kHz, 16 bits / sample and 512 226 IRINA POCORA, VIOREL POCORA FFT, with Hamming window for analysis. We obtained a resolution of 112 kHz for Spectrogram and power spectrum. To identify the sonograms belonging to a certain species, data from a series of authors were used (Tupinier, 1997; Ahlen & Baagøe, 1999; Russ, 1999; Jones et al., 2000; Parsons & Jones, 2000; Russo & Jones, 1999, 2002). The data on Myotis kind species were cumulated, in the case of the identification with the time expansion detector, because the sonograms of those species were alike, making the identification difficult (Tab. 2), excepting some calls on which we managed to identify some Myotis species (Tab. 1). Working material: Tranquility time expansion detector, Sony minidisk for recordings, headphones, GPS/PDA, frontal, thermo–hygrometer, heterodyne detector (Bat detector MKII – Magenta Electronics), boat, car.

RESULTS AND DISCUSSIONS Because most of the identifications were made with the time expansion detector based on ultrasounds analysis, recorded, the species identification with a question mark isn’t 100% sure, until the capture of bats. Because of that, the identification of some species of bats isn’t sure, so we used mark ? for these species. In this study, with the aid of time expansion detector, we examined distribution, abundance, species richness in 4 types of habitats: humid areas, woodlands, settlements – streetlamps and along roads. The importance of various habitat types to bats was assessed according to the mean numbers of passes of the registered species and according to the occurrence frequency of each bat species. In the habitats investigated by us, we identified 20 species of bats: Barbastella barbastellus, Eptesicus nilssonii, E. serotinus, Hypsugo savii, Myotis dasycneme, M. daubentonii, M. emarginatus?, M. nattereri, M. mystacinus/M. brandtii, M. myotis/M. oxygnathus, Nyctalus lasiopterus, N. leisleri, N. noctula, Pipistrellus kuhlii, P. nathusii, P. pygmaeus, P. pipistrellus, Pecotus sp., Vespertilio murinus, Tadarida teniotis?.

I. HABITAT SELECTION BY DIFFERENT SPECIES OF BATS 1. Until now, Barbastella barbastellus species was accidentally occurred in Moldova area and in the Danube Delta it wasn’t reported. In Europe, such species, with a limited distribution and high degree of behavioral specialization, is considered most vulnerable to extinction (Haupt, 2005). In the study area, in the investigated types of habitats, it’s a rare species (Tab. 3), being occurred inside old oak forests, with dead wood (Letea Forest – TL and Bãdeana Forest – IS), and while hunting, we met the species near waters (Prut River, Danube, Brateº channel – GL, Bahlui River – IS), in parks (Botanical Garden Iaºi – IS and Bârlad’s park – VS) and along the rural roads (Letea village – TL). In the records made with time expansion detector, Barbastella barbastellus can be sometimes mistaken with Pipistrellus nathusii/Pipistrellus kuhlii and Hypsugo savii, because it emits two kinds of signals, rarely both of them being recorded. When only one signal is recorded (at 37-40 kHz), the identification can be mistaken. 2. The present data suggest that, in the Balkans (Bulgaria, southern Romania, Croatia), the range of Eptesicus nilssonii is restricted to few islets of boreal forest habitats (Benda et al., 2003). Previous studies provided contrasting views upon THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 227 habitat use of Eptesicus nilssonii: whereas Jong (1994) emphasizes the outstanding importance of lakes and forest habitats for the species, in a Scandinavian region dominated by coniferous forest, other studies (Rydell & Racey, 1995) described the northern bat as a typical streetlamp bat. In the investigated habitats we found that Eptesicus nilssonii is a rare species (Tab. 3). We notice that the habitats important for sheltering are coniferous forests (Bicaz Gorges, Vânãtori-Neamþ Natural Park – NT), and for foraging streetlamps are important (Roºu Lake, Secu Monastery - NT), possibly humid areas as well (the Danube - GL, Siret - IS, Roºu Lake - NT). Sometimes, in the records, the species can be mistaken with Eptesicus serotinus, Myotis myotis/Myotis oxygnathus or Plecotus sp. 3. Eptesicus serotinus is an anthropophilous species. The abundance of the species is influenced by the presence of localities. In our study, the highest presence was recorded along the roads, because those are bounded by villages and opened areas that are crossed by the species. In the areas studied by us, we noticed that the habitats preferred by serotine, for sheltering, are human settlements (especially villages – 29.7%) (Tab. 2). As feeding areas, Eptesicus serotinus prefers the forest edges (broadleaved and mixed forests, the highest abundance being recorded in Lunca Mirceºti (IS) – 40%), streetlamps and, in a small proportion, humid areas (the highest percentage was recorded in Rãdãcinoasele channel, near Chilia Veche (TL ) – 37.3%) and parks. 4. Hypsugo savii is a rare species in the study area (Tab. 3). Until now the species hasn’t been identified in Moldova and in the Danube Delta. Russo & Jones (2003) specifies that in the Mediterranean region, rivers and lakes are the most important feeding habitats. In our study, it seems that the main habitats for the species are humid areas (rivers, channels and lakes – the highest presence of the species was recorded at Roºcani Lake (IS) – 13%) and localities near which there are humid areas (Sulina - TL). Hypsugo savii is hard to detect. The emission frequency is similar to those of Pipistrellus nathusii and Pipistrellus kuhlii, with which Hypsugo savii can be confused. 5. For the species of Myotis kind, wetlands and woodlands are the most important habitats (Tab. 2). Myotis species are occurred within all kinds of forestry areas in which we made recordings, excepting the parks, being more abundant in areas bordered by humid areas (Bicaz Gorges – NT, Siret River, near Mogoºeºti - IS, Letea Forest - TL). Myotis sp. were identified in all investigated humid areas (channels, rivers, lakes and ponds), excepting large lakes, large rivers and channels (the Danube and Sulina). Myotis sp. was prevalent in the records made in 11 of the 23 humid areas. 6. Nyctalus noctula is a prevalent species, and the most frequent in all types of studied habitats (Tabs 2, 3). The species occurs in all types of forests (broadleaved, mixed and coniferous), as well as in parks. The species belong to Nyctalus were met in all the investigated humid areas, and were the most abundant species in fish breeding farms (Larga Jijia - IS and Iezãr Dorohoi - BT), on Bahlui River - IS and Sulina channel - TL. Along the roads and at streetlamps, Nyctalus species pass 50% from the total of identified species. Nyctalus leisleri was often occurred feeding at streetlamps and along the roads. It seems that, for Nyctalus lasiopterus forested areas are the most important (for shelter: Letea Forest, Bârlad park) and streetlamps, for feeding (Letea village - TL, Roºu Lake, Secu Monastery - NT). Nyctalus lasiopterus hasn’t been identified by now in Moldova and the Danube Delta. 7. For Pipistrellus nathusii/Pipistrellus kuhlii species, riparian broadleaved forests and parks, all the investigated types of humid areas and human settlements 228 IRINA POCORA, VIOREL POCORA are the most important habitats. If in the urban areas, maybe Pipistrellus kuhlii is the most abundant species, in humid habitats and forests Pipistrellus nathusii is among the most abundant species. Pipistrellus kuhlii is considered to be anthropophilous species – house species – prefering the shelters offered by the buildings, hunts above waters and at streetlamps (Sachanowicz et al., 2006). Pipistrellus kuhlii is the prevalent species in the “Lunca Inferioarã a Prutului” Natural Park - GL (44%). In Sulina town, we met the species at streetlamps, representing 54.4% of total number of bats. Pipistrellus nathusii prefers wetlands, because of which, in the Danube Delta it is quite frequent but, for Romania is a rare species. We can’t say how much Pipistrellus nathusii represents in percentage in different habitats, basing on the time expansion detector recordings. 8. In Romania, Pipistrellus pipistrellus is quite spread, though there is few previous data from Moldova and Dobrogea (Decu et al., 2003). Pipistrellus pipistrellus is an anthropophilous species, being the most spread in Europe, especially in humid areas and forests. Although it’s an anthropophilous species, many nursing roosts are in forests, especially if there are near waters (Boye & Dietz, 2005). From our study it results that the woodlands (broadleaved, mixed and coniferous forests, as well as parks) and settlements (Tab. 2) are the most important habitats for the species. The species was prevalent in the Bicaz Gorges forested area where it represented 47% of bat species. Pipistrellus pipistrellus is a subdominant species, but constant in the studied habitats (Tab. 3). 9. Pipistrellus pygmaeus is common in northen and southern parts of Europe, in Central Europe mostly confined to the valleys of larger river systems (Dietz & Helversen, 2004). We noticed that the humid broadleaved forests are the most important habitats for the species. The species was also met in other types of forestry areas (broadleaved, mixed and coniferous, as well as parks), and humid habitats, but in small percentage. Inside localities, the high percentage was given by the abundance of the species in Letea village (Tab. 2). In the studied habitats, Pipistrellus pygmaeus is a subdominant species, but constant (Tab. 3). From the areas studied by us, the species was dominant in Letea Forest, which is a humid broadleaved forest, bordered by large humid areas. Thereby, Pipistrellus pygmaeus can be considered an indicatory species for this type of forest. Wetlands, which are not bordered by forests, are not visited by the species (Sulina and Sf. Gheorghe channels– TL, Bahlui River - IS) or are rarely visited (Prut River – GL, Pruteþul Bãlãtãu – IS, Rãdãcinoasele channel – Chilia, TL). 10. Vespertilio murinus was observed hunting above large areas of water (lakes and rivers), agricultural areas and forests, as well as at streetlamps (Safi et al., 2007). Because of this, in different researched habitats, with the help of the time expansion detector, we frequently identified the species (75.7%) (Tab. 3). Along the roads, which are mostly bounded by agricultural areas and localities, this bat was present in the highest percentage (Tab. 2). The following preferred habitats are forests and streetlamps (Tab. 2). The highest presence was recorded at the streetlamps from Secu Monastery (14%). The research based on the ultrasound emission of this species can be partly wrong, because it presents the same frequency and same pattern as Nyctalus species and Eptesicus serotinus. Figure 1 renders the degree of affinity between species recorded with time expansion detector, in different habitats from the study area, based on similarity index analysis, Bray-Curtis method. The tightest affinity is between cryptic and sympatric species Pipistrellus pipistrellus and Pipistrellus pygmaeus, both of them THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 229 being identified in all habitats, constant in the records, but subdominant (Tab. 3). In the habitats where Pipistrellus pipistrellus dominated, Pipistrellus pygmaeus is a rare species and the other way around, thereby they don’t compete, even if both species are met in the same habitat, they’re using different microhabitats for feeding. Pipistrellus pipistrellus is characteristic for anthropogenic habitats, while Pipistrellus pygmaeus is an indicatory species for humid natural broadleaved forests. Inter-specific overlap in habitat use is low and consequently foraging ranges are segregated spatially (Nicholls & Racey, 2006). Also, there’s high affinity between Nyctalus leisleri and Vespertilio murinus, given by the similar percentages, concerning the presence in certain types of habitats. Both species like the habitats along the roads and to forage at streetlamps. Nyctalus noctula and Pipistrellus kuhlii are generalist species, because of the plasticity in echolocation calls. This allows them to explore, for foraging, a variety of habitats structured differently and feed with diverse insects. These species don’t have preferences for a certain kind of habitat and for shelter selection, being the most abundant species in all the investigated habitats (Tabs 2, 3). Because of this, in the study area the species presents high affinity. Based on the affinity, the species are grouped in 2 clusters: common and rare species. Because Tadarida teniotis species was identified in only one site (Letea Forest), it is an accidental species. From the rare species, affinity is present between Nyctalus lasiopterus and Eptesicus nilssonii, both species presenting the same percentage and preferring, as foraging area, the streetlamps (Fig. 1). According to the frequency and dominance, in Moldova and Dobrogea, Nyctalus noctula and Pipistrellus nathusii/Pipistrellus kuhlii are very common, Nyctalus leisleri, Eptesicus serotinus, Myotis sp., Vespertilio murinus are common, Pipistrellus pipistrellus and Pipistrellus pygmaeus are subdominant while Plecotus sp., Eptesicus nilssonii, Nyctalus lasiopterus, Hypsugo savii and Barbastella barbastellus are considered rare bat species in the habitat types of the primary importance (Tab. 3).

Fig. 1 - The similarity dendogram between identified bat species, with the help of the time expansion detector, in different types of habitats. 230 IRINA POCORA, VIOREL POCORA

Table 1 The presence of bat species in different habitats from the Danube Delta and Moldova areas, their status in Romania (Botnariuc & Tatole, 2005). LR – Low Risk, VU – Vulnerable, EN – Endangered.

Habitat types Status in Wetlands Settlements Along Woodlands Species Romania roads B. barbastellus VU + + - + E. nilssonii EN + + + + E. serotinus VU + + + + H. savii VU + + + + M. dasycneme* EN + - - + M. daubentonii * EN + + - + M. emarginatus* EN + + - + M. nattereri* EN + - - + M. mystacinus/M. brandtii* EN + - + + M. myotis/M. oxygnathus* EN + - - + N. lasiopterus EN + + + + N. leisleri EN + + + + N. noctula LR + + + + P. kuhlii LR + + + + P. nathusii EN + + + + P. pygmaeus LR + + + + P. pipistrellus LR + + + + Plecotus sp. VU + + + + V. murinus EN + + + + T. teniotis --+-+ Total no of species 19 16 13 20 (* Based on some calls we managed to determine some Myotis species)

Table 2 The proportion of bat species that are representative for the studied habitat types.

Habitat types Wetlands Settlements Streetlamps Along Woodlands Species roads B. barbastellus < 0.5% < 0.5% - - 1.4% E. nilssonii < 0.5% - 3.3% 0.07% 1.5% E. serotinus 4.2% 10% 7.7% 13.2% 10.2% H. savii 1.5% 1.2% 1.1% 0.6% < 0.5% Myotis sp. 24% 1.6% - 0.7% 11.2% N. lasiopterus 0.7% < 0.5% 3.3% 1% 1.5% N. leisleri 3.4% 4% 12.8% 12.7% 6.1% N. noctula 25.2% 23.1% 45.4% 44% 19.5% P. nathusii/P. kuhlii 22.3% 26.3% 9.3% 12.3% 17.6% P. pygmaeus 9.6% 17.1% 4.4% 3% 9.8% P. pipistrellus 4.3% 10% 2% 1.2% 10.8% Plecotus sp. 0.8% < 0.5% 0.9% < 0.5% 3% V. murinus 3% 5.6% 9.9% 11.6% 6.9% (* The data about the species of Myotis kind were cumulated, in case of identifying with the time expansion detector, because the sonograms of those species are alike, making a difficult identification) THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 231

Table 3 Percentage value and class of ecological indices: dominance (D), frequency (F) and ecological significance index (W) (Varvara et al., 2001).

No. Species No of D% F% W% crt. passes 1. Barbastella barbastellus 12 0.3 D1 12.2 C1 0.04 W1 2. Eptesicus nilssonii 30 0.7 D1 10.8 C1 0.08 W1 3. Eptesicus serotinus 378 8.6 D4 83.8 C4 7.2 W4 4. Hypsugo savii 44 1 D1 25.3 C2 0.3 W2 5. Myotis sp. 484 11 D5 48.6 C2 5.3 W4 6. Nyctalus lasiopterus 51 1.2 D2 27 C2 0.3 W2 7. Nyctalus leisleri 341 7.8 D4 75.7 C4 5.9 W4 8. Nyctalus noctula 1430 33 D5 89.2 C4 29.4 W5 9. P. nathusii/P. kuhlii 757 17.2 D5 87.8 C4 15.1 W5 10. Pipistrellus pipistrellus 187 4.3 D3 58.1 C3 2.3 W3 11. Pipistrellus pygmaeus 325 7.4 D4 56.8 C3 4.2 W3 12. Plecotus sp. 38 0.9 D1 23 C1 0.2 W2 13. Vespertilio murinus 314 7.1 D4 75.7 C4 5.4 W4 14. Tadarida teniotis 1 - D1 1.4 C1 - W1

II. HABITAT TYPES WHICH AFFECT THE COMMUNITY COMPOSITION AND THE SPECIES DISTRIBUTION In Moldova and the Danube Delta, woodlands and humid areas are the most important habitat types to the majority of bat species, whereas the habitats along roads (mostly made in open areas) are less important. 1. Wetland habitats The so called ‘trawling bats’ from Europe (Myotis daubentonii, Myotis dasycneme and Myotis capaccinii) hunt almost exclusively in wetlands, where insects are caught on the water surface. Managing wetland habitats is crucial for these specialists. Specific micro-habitat features may affect food availability (insects) and determine the quality of wetlands. Such features are: width of the watercourse, the presence of trees (bushes) that confine the watercourse (riparian vegetation), water quality, vegetation at the water surface, and elements of connection between foraging areas and roosts, sensitivity to habitat alteration. The ‘trawling bats’ are predictors for humid quality habitats (Biscardi et al., 2007; Langton et al., 2009). The protection and correct management of water habitats are undoubtedly key points in planning bat conservation. Riverine habitats and fauna are threatened by many factors such as pollution, channelization, dredging damming, alteration and destruction of riparian vegetation. Degradation of riparian habitats influences their insect communities and consequently foraging bats (Vaughan et al., 1996; Russo & Jones, 2003). In this study, we recorded high levels of activity of Myotis bats (mainly of species Myotis daubentonii), Pipistrellus nathusii/Pipistrellus kuhlii, Nyctalus noctula and Pipistrellus pygmaeus over channels, rivers and lakes (see fig. 2). For Hypsugo savii lakes are important as foraging areas. The bat species composition differs a lot from an observation point to another. From the humid areas investigated, Prut river shows the largest diversity of species (14 species – 232 IRINA POCORA, VIOREL POCORA Pipistrellus kuhlii is a dominant species, with 43.5%) and Roºcani Lake (13 species – Nyctalus noctula with 41%), followed by 2 channels near Letea Forest (Pipistrellus pygmaeus with 45.2%), Bahlui River (Nyctalus noctula with 33.3%) and Siret Mogoºeºti (Myotis sp. – 61.5%) with 11 species. The fewest species were recorded on Busurca channel, near Sulina (2 species), on a channel near Sf. Gheorghe (2 species) (maybe because the recording was started early and the bat species haven’t arrived at the foraging area, yet), on Sulina channel - TL (4 species) (which is anthropogenic), also at Larga Jijia ferm - IS (3 species), probably because of eutrophization. In humid habitats from the studied areas, the tightest affinity is between Pipistrellus kuhlii/Pipistrellus nathusii, Myotis sp. and Nyctalus noctula species (Fig. 3). The affinity is given by the high abundance of the species. If Pipistrellus nathusii and Myotis daubentonii are indicators for water quality, Pipistrellus kuhlii is indicator for humid anthropogenic habitats. Because many of the investigated areas are limited by forested areas, the abundance of Nyctalus noctula can be explained, in such habitats.

Fig. 2 - Specific composition of bats from the investigated wetlands

Fig. 3 - The similarity dendogram between identified bat species from the investigated humid areas. THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 233 As regards the affinity between different sites of wetland habitats (Fig. 4), the tightest affinity is between Pruteþul Bãlãtãu (meander of Prut River) and Siret River, near Mogoºeºti - IS, affinity given by the approximate abundance of the same species (Nyctalus noctula, Pipistrellus kuhlii and Myotis daubentonii). Both humid areas are confined by forested areas, in which poplars plantation are prevalent and are partially anthropogenic. The affinity between Letea and Sulimanca channels is given by the fact that both are located near Letea Forest (TL), being foraging areas for about the same bat species, and the value of abundance of different species is similar. The affinity between Bahlui River (IS) and Prut River, near Cârja (VS) sites is given by the abundance of Pipistrellus kuhlii and Nyctalus noctula species, generated by the presence of villages from the surroundings. Both habitats are represented by rivers, but Bahlui River is not confined by trees, while Prut presents forested banks; the width of the water flow also differs.

humid areas

Fig. 4 - The similarity dendogram between humid sites investigated: 1 – Pruteþul Bãlãtãu (IS), 2 – Danube (GL), 3 – Brateº channel (GL), 4 – Prut River, near Vlãdeºti Lake (GL), 5 - Bahlui River (IS), 6 – Letea channel (TL), 7 – Sulina-Letea channel (TL), 8 – Magearu channel (TL), 9 – Sulimanca channel, near Merhei Lake (TL), 10 – Rãdãcinoasele channel, near Sf. Gheorghe (TL), 11 – Sulina channel (TL), 12 – Busurca channel, near Sulina (TL), 13 – Serenea channel, near Chilia Veche (TL), 14 – Roºu Lake (NT), 15 – Prut River, near Cârja (VS), 16 – Cârja Farm (VS), 17 – Larga Jijia Farm (IS), 18 – Siret River, near ªendreni (GL), 19 – Puºcaºi Lake (VS), 20 – Iezãr Dorohoi (BT), 21 – Siret River, near Mogoºeºti (IS), 22 – Siret River, near Mirceºti (IS), 23 – Roºcani Lake (IS).

The key humid areas for bats are water flows of 6 m wide, at least, limited by trees, bushes or reed (channels from the Danube Delta, streams and rivers) or forested (Prut River, Siret River), lakes and the presence of woods closer to wetlands (Roºu Lake – NT, Roºcani Lake –IS, Puºcaºi Lake – VS). The eutrophied lakes from fish breeding farms, large channels (Sulina) and anthropogenic rivers (the Danube), without riparian vegetation, are less visited by the bats. 2. Woodlands There are also important targets for bat conservation, because they are used by a considerable number of threatened species. The bats are avoiding the forest with a homogenous canopy, from which the dead wood is removed (Russo & Jones, 234 IRINA POCORA, VIOREL POCORA 2003; Ulrich et al., 2007). Forests fragmentation is an important process with impact on the bats fauna, and this process could be taken in consideration further as the main cause in species extinction (Reiter, 2004). The coverage with natural or semi- natural vegetation (dense forests, bushes, isolated trees, patches of forest and lawn) seem to affect the distribution of each bat species and the community composition (isolated trees affect the distribution of Eptesicus nilssonii). Few elements from habitats are used as flying ways, markers during migration for the species with short echolocation radius or as shelters against predators (bushes, isolated trees, small patches of trees) (Jaberg & Guisan, 2001). We recorded high levels of activity of Nyctalus noctula, Pipistrellus nathusii/Pipistrellus kuhlii, Myotis species, Pipistrellus pipistrellus, Eptesicus serotinus and Pipistrellus pygmaeus in the woodland areas that we investigated (Fig. 5).

Fig. 5 - Specific composition of bats from woodland areas from Moldova and the Danube Delta.

Letea Forest, old broadleaved woodland, favors abundant and diverse communities of forest bats (19 species). One of this species is Tadarida teniotis, few echolocation calls being identified. The species wasn’t reported before in Romania. We mentioned it in the study because no other species gives such a low frequency as this one: 13-15 kHz (Pocora & Pocora, 2007). The most abundant species in the study area is Pipistrellus pygmaeus (58.6%). In other woodland areas there were identified 10 species of bats: the forested area along Prut River – “Lunca Inferioarã a Prutului” Natural Park - GL (Pipistrellus kuhlii was the dominant species – 45.7%), Vânãtori-Neamþ Park - NT (Nyctalus noctula with 47.7%), Lunca Mirceºti Forest - IS (Eptesicus serotinus with 40%), Roºcani Forest – IS (Pipistrellus pipistrellus with 25%) and Bârlad Park - VS (Nyctalus noctula with 35.7%). The fewest species (4) and the lowest activity of bats were recorded in the forested area near the Danube (GL), where the poplars plantation was present. In figure 6, it’s observed that, based on the species similarity, a group was delimited, represented by the more abundant species: Eptesicus serotinus, Nyctalus leisleri, Vespertilio murinus, Nyctalus noctula, Pipistrellus pipistrellus, Plecotus sp., Myotis sp. and Pipistrellus pygmaeus, out of which Barbastella barbastellus species adds up as indicatory species of old forests. The affinity between Hypsugo savii and Tadarida teniotis species is given by the fact that both are accidental species in such habitats. Concerning the affinity between forestry habitats (Fig. 7), the tightest affinity is between the forested area along Prut River – “Lunca Inferioarã a Prutului” Natural THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 235

Fig. 6 - Dendrogram similarity between bat species found in the investigated forestry habitats.

woods 13 7 2 8 12 6 4 5 11 3 10 9 1 0.48 0.4 0.32 0.24 0.16 0.08 0

Fig. 7 - The dendogram similarity between investigated woodlands habitats: 1 – Pruteþul Bãlãtãu (IS), 2 – dam on Danube (GL), 3 – dam on Prut River (GL), 4 – Prut forestry area, near Fãlciu (VS), 5 – Letea Forest (TL), 6 – Botanical Garden of Iaºi (IS), 7 – Bicaz Gorges (NT), 8 –Vânãtori-Neamþ Natural Park, 9 – Siret forestry area, near Mogoºeºti (IS), 10 – Lunca Mirceºti (IS), 11 – Roºcani Forest (IS), 12 – Bârlad Park (VS), 13 – Bãdeana Forest (VS).

Park – GL (riparian forest) and Roºcani Forest – IS (oak forest); even if it doesn’t represent the same type of forest, the affinity is given by the fact that both forestry habitats present humid areas around (Prut River, respectively Roºcani Lake), and Pipistrellus kulhii and Pipistrellus pipistrellus are the most abundant species, generalist species characteristic to anthropogenic areas. Both areas present a high diversity, 10 species of bats. The affinity between the Botanical Garden Iaºi – IS and Bârlad Park – VS is given by the abundance of the same species: Nyctalus noctula and Pipistrellus nathusii/Pipistrellus kuhlii and the approximately presence of the same species. 236 IRINA POCORA, VIOREL POCORA The forests with the highest diversity and bat activity were the humid broadleaved ones (Letea Forest – TL), riparian (forested areas on the banks of Prut and Siret rivers) or forests of Quercus sp. which have humid areas in the surroundings (Roºcani Forest – IS). Also, the mixed (Vânãtori-Neamþ Natural Park) and coniferous (Bicaz Gorges) forests are important, especially if they present humid areas in the neighborhood, used by bats for foraging. 3. Settlements Also, the presence of urbanized areas might also influence species distributions, as some species regularly forage near artificial lights (Jaberg & Guisan, 2001; Russo & Jones, 2003). Some highly synanthropic bat species have adapted well to urban habitats. Towns and villages offer them not only plenty of diversified foraging areas, but also many suitable shelters (Bartonièka & Zukal, 2003). Localities are very important for the species: Pipistrellus kuhlii, Nyctalus noctula, Eptesicus serotinus and Pipistrellus pipistrellus (Fig. 8). The most abundant species from settlements, especially urban ones, from the east of the country is Pipistrellus kuhlii. Unlike the humid forestry habitats, in localities, the diversity and activity of the bats are lower. There were identified between 5 species (Chilia village and Viiºoara village) and 9 species (Letea village).

Fig. 8 - Specific composition of bats from settlements.

In the dendogram of similarity between the identified species (Fig. 9), the highest affinity is between the species Nyctalus noctula, Pipistrellus kuhlii and Pipistrellus pipistrellus. They are the most abundant species from the urban and rural settlements. All the species hunt at streetlamps. The high abundance of Pipistrellus pygmaeus species is given only by the high percentage that is recorded in Letea village (Tab. 2). In the dendogram that represents the similarities between studied localities (Fig. 10), it was observed that the highest affinity is between Chilia village (TL) and Iaºi city, given by the abundance of Pipistrellus kuhlii and Nyctalus noctula species and the presence of the same species. Pipistrellus kuhlii species is present because the transects were made near Chilia channel, respectively near Bahlui River. A high affinity is also between Crâng and Viiºoara villages (VS), given by the abundance of Nyctalus noctula and Eptesicus serotinus species. THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 237

settlements

0.48

Fig. 9 - Dendrogram similarity between species of bats found in localities.

settlements 5

0.48 0.4 0.32 0.24 0.16 0.08 0

Fig. 10 - The dendogram similarity between investigated settlements: 1 – Letea village (TL), 2 – Sulina town (TL), 3 – Chilia village (TL), 4 – Iaºi city, 5 – Deleni village (VS), 6 – Crâng village (VS), 7 – Viiºoara village (VS).

Artificial light sources attracts insects which sometimes form dense aggregations. Because of streetlamps bats frequently feed in villages and even in urban and suburban areas. In Sweden, it was observed that the species that hunt at streetlamps are: Nyctalus noctula, Vespertilio murinus, Eptesicus nilssonii and occasionally Pipistrellus pipistrellus (Rydell, 1992). In our area of study, we observed that the species that hunt at streetlamps are: Nyctalus noctula, N. lasiopterus, N. leisleri, Vespertilio murinus, Pipistrellus kuhlii, Eptesicus serotinus, E. nilssonii, occasionally Pipistrellus pygmaeus and P. pipistrellus. The most abundant species is Nyctalus noctula - 46% (Fig. 11). Based on the dendogram of similarities between the identified species, it was observed that the highest affinity is between the species that usually hunt at 238 IRINA POCORA, VIOREL POCORA

Fig. 11 - Specific composition of bat foraging at streetlamps. streetlamps (Fig. 12). Other two pairs of species that present affinity are Eptesicus nilssonii and Plecotus sp., Pipistrellus pipistrellus and Hypsugo savii, affinity given by the fact that the species were recorded in small percentages, only in one site. In Letea village, from fixed point, records were made at 4 streetlamps. Here there was the foraging area of 7 bat species, the most abundant being Nyctalus noctula (45.6%). In Sulina town, at streetlamps (4 species), Pipistrellus kuhlii was the most abundant species (66%). At Secu Monastery, at the streetlamps (8 species), Nyctalus noctula was the dominant species (47.8%). The negative impact of urbanization on bats might be counteracted by parks with old trees, humid areas (ponds, rivers), fostering trees and gardens. Rydell & Racey (1995) suggested that by attracting insects, mercury streetlamps provide local patches of food for some bat species and could be important during critical periods for their survival and reproduction. 4. Roads The presence of highroads leads to the fragmentation of the habitats. In Romania, many roads are cut of opened and semi-opened habitats, and are passing

streetlamps

Fig. 12 - Dendrogram similarity between species of bats found feeding at streetlamps. THE USE BY BATS OF VARIOUS HABITAT TYPES IN MOLDOVA AND THE DANUBE DELTA 239 through many localities. Along the roads there were recorded the fewest bat species (Tab. 1). Agricultural areas, completely opened, that not encourage the presence of bats are the main habitats that border the streets from Romania. Farmland practices should maximize landscape complexity, favor structural variation and connectivity, and limit the spread of pesticides which has harmful effects on bat populations (Russo & Jones, 2003). The most common species, along the roads from Moldova and Dobrogea are Nyctalus noctula, N. leisleri and Eptesicus serotinus, followed by Pipistrellus kuhlii and Vespertilio murinus, the species Pipistrellus pipistrellus and P. pygmaeus being present in a very low percentage (Fig. 13). Among the 25 transects made in such habitats, in transect from Vânãtori – Zaboloteni (IS) (27.08.2009) the most numerous bats, belonging to 6 species, were recorded (165), in the transect Vadu - Nãvodari (CT) (29.07.2006) only 11 bats of 4 species were recorded. The most numerous species (9) were identified in Iaºi – Poiana transect, on 01.09.2009.

Fig. 13 - Specific composition of bats along the roads.

car surveys

Fig. 14 - Dendrogram similarity between species of bats found along roads. 240 IRINA POCORA, VIOREL POCORA Based on dendogram of similarities between the identified species, it was observed that the highest affinity is between the most abundant species present along the roads: Eptesicus serotinus, Nyctalus leisleri, N. noctula, Vespertilio murinus and Pipistrellus kuhlii.

ACKNOWLEDGEMENTS This work was supported through the project CNCSIS-UEFISCSU project number PN II-RU PD – 326/2010, funded by the Romanian Education and Research Office. The authors are grateful to Farkas and Abigel Szodoray-Paradi from APLR (Bat Association from Romania) for the equipment and the support given. We thank to the coordinators of the Indicator bat project – Romania – Darwin Initiative - Bats and Roadside Mammals Survey (Kate Jones and Colin Catto) for the recording equipment. We thank also to Constantin Ion for the Batsound program.

GRADUL DE FOLOSIRE, DE CÃTRE LILIECI (CHIROPTERA: VESPERTILIONIDAE), AL DIFERITELOR TIPURI DE HABITATE DIN MOLDOVA ªI DELTA DUNÃRII (ROMÂNIA)

REZUMAT Investigaþiile noastre au fost defãºurate în Moldova ºi Delta Dunãrii, în perioada sezonului cald, din 2006 pânã în 2010. Tipurile de habitat care au fost investigate sunt: 23 zone umede, 13 pãduri, 7 localitãþi - stâlpi de luminã, 25 de transecte cu ajutorul maºinii. Pãdurile ºi zonele umede sunt cele mai importante tipuri de habitate pentru majoritatea speciilor de chiroptere, în timp ce habitatele de-a lungul ºoselelor (majoritatea reprezentate de zone deschise) sunt mai puþin importante. Speciile Pipistrellus kuhlii ºi Nyctalus noctula dar ºi Eptesicus serotinus, Nyctalus leisleri ºi Vespertilio murinus sunt generaliste în folosirea habitatelor de hrãnire, fiind speciile cele mai frecvent înregistrate. În zonele umede Nyctalus noctula (25,2%), Myotis sp. (24%) ºi Pipistrellus nathusii/Pipistrellus kuhlii (22,3%) sunt speciile cele mai abundente. În habitatele forestiere, cea mai abundentã specie este Nyctalus noctula (19,5%), urmatã de Pipistrellus nathusii/Pipistrellus kuhlii (17,6%) ºi Myotis sp. (11,2%). De-a lungul ºoselelor, cele mai abundente specii sunt Nytcalus noctula (44%) ºi Eptesicus serotinus (13,2%). La stâlpii de luminã Nyctalus noctula (45,4%) ºi Nyctalus leisleri (12,8%) sunt cele mai abundente specii. În localitãþi, speciile cele mai abundente sunt Pipistrellus kuhlii (26%) ºi Nyctalus noctula (23%).

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