Miniopterus schreibersii (Kuhl, 1817)

Don E. Wilson & Russell A. Mittermeier, 2019, Miniopteridae, Handbook of the Mammals of the World – Volume 9 Bats, Barcelona: Lynx Edicions, pp. 674-709 : 699-700

16.

Schreibers’s Long-fingered Bat

Miniopterus schreibersii

French: Minioptére de Schreibers / German: Eigentliche Langfligelfledermaus / Spanish: Murciélago de cueva

Other common names: Schreiber’s Bent-winged Bat

Taxonomy. Vespertilio schreibersii Natterer in Kuhl, 1817 ,

“sudostlichen Gebirge des Bannats: in der Columbézer Héhle [= southeastern mountains of Banat in the Columbazer Cave],” Banat, near Coronini, Romania.

Recent phylogenetic studies using DNA sequencing have restricted M. schreibersii to Europe, North Africa, and part of the Near East. Populations of Miniopterus of medium size from sub-Saharan Africa, East Asia, and Australia, which were until recently all included within this species, are now considered distinct species, not even closely related to M. schreibersii . The genetically closest species to M. schreibersii are M. pallidus from the Middle East and M. maghrebensis from north-western Africa. Monotypic.

Distribution. S Europe from Iberian Peninsula E to N & W Anatolia ( Turkey) and W Georgia, N to C France, Slovakia, and Romania, and S to Morocco, N Algeria, Tunisia, NW & NE Libya (Tripolitania and Cyrenaica), Syria, Lebanon, Israel, and possiblyJordan, also on most Mediterranean Is; historical records or occasionally in SW Germany, Switzerland, and Czech Republic. In the Maghreb,it shares habitat with the Maghrebian Long-fingered Bat ( M. maghrebensis ) and in Levant with the Pallid Long-fingered Bat ( M. pallidus ), but distributional limits in these areas are not well defined.

Descriptive notes. Head-body 51-59 mm, tail 52-63 mm, ear 10-12 mm, hindfoot 9-8-10-9 mm, forearm 43—-47-1 mm; weight 10-14 g. Pelage of Schreibers’s Long-fingered Bat is short, very dense, and silky. Dorsum is uniformly grayish, ashen, or more rarely grayish brown, with somewhat paler venter. Hairs are bicolored, with darker bases. Wing membranes and uropatagium are dark. Ears are small, and tragus (5-5-7 mm) is slender and slightly curved forward. Chromosomal complement has 2n = 46 and FN = 52-56 ( Italy, Switzerland, Greece, and Turkey). X-chromosomeis metacentric, and Y-chromosome is dot-like acrocentric.

Habitat. Wide variety of habitats including semi-desert steppes (Maghreb, Levant, or south-eastern Iberia), humid areas of deciduous forest in the north of the distribution, and Mediterranean scrub and forests, generally at elevations of 1000-1400 m. Breeding colonies of Schreibers’s Long-fingered Bat generally occur below 1000 m, although they can occur up to 1200 m. Non-breeding and hibernating colonies can occupy shelters up to ¢. 1400 m.

Food and Feeding. Schreibers’s Long-fingered Batis an aerial hawker, mostly hunting moths in open spaces, but it has sufficiently maneuverable flight to forage in forest edge, clearings, below forest canopies, and close to vegetation. In France near the northern limit of the distribution, they frequently use well-lit urban areas to forage, preferring areas lit by white streetlights. They also forage in orchards and parks. In contrast, dense pine forests and closed and homogeneous deciduous or mixed woodlands are avoided. For commuting, they mainly use woodland borders, hedgerows, and riverine forests. In Italy, they were most active over rivers and to a lesser extent in olives and chestnuts groves and Mediterranean and beech woodlands, and they were never recorded in Mediterranean maquis (shrubland) and agricultural lands. In Portugal, Schreibers’s Long-fingered Bat more actively forages activity near water, urban areas, and native forests. Diet mostly contains Lepidoptera , which generally accounts for more than 70% by volume of ingested prey. In a study conducted in Slovenia, Lepidoptera was the main prey: 79% of the annual diet by volume, maximum of more than 90% in summer, and minimum of 50% in autumn. With decreasing importance, other insects in the diet were Neuroptera (mostly Chrysopidae ) with average volume of 9-2% and maximum of 26% in late autumn, Diptera with average volume of 7:4% and maximum of 15-7% in spring and 21:6% in autumn, Trichoptera with average volume of 2:2% and 12:3% in autumn, and Coleoptera with average volume of 1:4% and maximum of ¢.10% at the end of spring. Diet was most diverse in late October. Schreibers’s Long-fingered Bat hunts small to medium-sized winged prey (wing length: 2-18 mm, average 13-2 mm). It can switch to other seasonally abundant prey. A recent study in which prey species were identified with DNA sequencing of remains of prey in feces and using metabarcoding techniques allowed more detailed understanding of dietary composition. Samples of 79 individuals from 16 different locations in seven European countries were analyzed. There were twelve arthropod orders, among which lepidopterans were predominant (they were present in more than 97% of the samples analyzed and accounted for 75% of the total operational taxonomy-assigned units (OTUs). Diptera (20 families) was the second most common order, appearing in more than 50% of the samples, and Neuroptera and Coleoptera occurred in 25% of the samples. Thirty-five families of Lepidoptera were represented in the samples, with Noctuidae the most frequent, occurring in 85% of samples and with more than 300 different OTUs, followed by Geometridae at 50%. As many as 44 insects consumed are considered agricultural pests, mostly moths that occurred in 92% of the samples; 22 of these pests are considered major pests and appeared in 73% of the samples. Dipterous families also occurred in samples; these families (e.g. Culicidae and Simuliidae ) can cause discomfort and transmit diseases to humans and domestic animals. Many prey species consumed by Schreibers’s Long-fingered Bats are tympanate insects (mainly moths in families Noctuidae and Geometridae and lacewings of the family Chrysopidae ), capable of hearing ultrasound calls of bats. Echolocation calls of Schreibers’s Long-fingered Bat have peak frequency of 54 kHz, whichis at the limit of the hearing capacity of tympanate moths.

Breeding. Schreibers’s Long-fingered Bat is seasonally monoestrous, with one young per pregnancy and delayed implantation in winter. Mating occurs in September and early October. Egg is fertilized immediately, but blastocyst does not implant in the uterus until end of hibernation, which in the French Pyrenees is in March or early April. Births occur in late June or earlyJuly in France and Spain and at the beginning ofJune in the more temperate areas of Portugal. Complete duration of the reproductive cycle from mating to birth is 8-9 months. Young begin to fly at ¢.40 days old and are fully developed at 60-70 days old. Females reach sexual maturity at c.1 year old and have their first young at c.2 years old.

Activity patterns. In France, pregnant Schreibers’s Long-fingered Bats emerged from roosts to feed c.1 hour after sunset in May and returned 2-5 hours before sunrise with a period of activity of 5-5 hours. Lactating females emerged c.42 minutes after sunset in June and returned c.2 hours before sunrise, with c.6 hours oftotal activity. During all nights, no female returned to the roost temporarily, even during lactation. In Slovenia, the first bat emerged ¢.20 minutes after sunset in a small colony of 100 individuals. Like most temperate species, Schreibers’s Long-fingered Bats enter daily torpor to save energy during short unfavorable periods and hibernate during the coldest months of winter. Duration of hibernation is variable depending on local weather, ranging from five months at most in northern France to two months in areas with milder winters in Portugal and Spain. Shelters selected for hibernation have temperatures of 5-10°C in Spain and 3-7-4-5°C in Croatia. Hibernation is not continuous but characterized by interruptions of activity with movement within and among roosts. In north-eastern Spain (Catalonia) and Croatia, hibernation occurs from the end of December to mid-February. Before hibernation in October to mid-November, body mass increases up to 31-5% in just 29 days. Schreibers’s Long-fingered Bats roost in caves and cave-like structures such as mines and tunnels. Some individuals or small groups occasionally occur in fissures of rocks or human structures. Echolocation calls have downward FM signals, with start frequencies of 59-3-113-5 kHz, end frequencies of 47-5-55-7 kHz, peak frequencies of 49-4-62-5 kHz, durations of 2—13-8 milliseconds, and intervals of 40-209-3 millisecondsin Italy and start frequencies of 104-8-118-3 kHz, end frequencies of 46-3-52 kHz, peak frequencies of 56-4—61-7 kHz, and durations of 2-8—4-6 milliseconds in Turkey.

Movements, Home range and Social organization. In France, radio-tracked female Schreibers’s Long-fingered Bats during periods shorter than a week had home ranges that corresponded to their foraging strategy of an open-air hunter with good flight abilities. Home ranges were significantly larger for lactating females (average 22,318 ha) than for pregnant females (10,837 ha). The entire colony’s home range, from all radio-tracking records, was smaller for pregnant females (89,359 ha) than for lactating females (162,997 ha). Each bat foraged every night in 1-9 small feeding areas. The longest distance recorded with precision from the roost to a foraging area was 29-7 km for a lactating female and 24-7 km for a pregnant female. In Portugal, females during reproduction do not move more than 15-5 km from their day roost, and 82% of feeding areas were found within a 10km radius of the day roost. Selection of feeding areas wasrelated to distance to the day roost and proximity of water. Populations of Schreibers’s Long-fingered Bat have a typical metapopulation structure. Each population occupies a large territory of several thousand square kilometers where it has a network of underground roosts with different environmental characteristics. Different subpopulations occupy different roosts within their territory throughout the annual cycle, depending on energy requirements of each period for each sex and age class. Throughout the year, each individual will have used a good number of these shelters. It was found that the main cause of seasonal movements in Portugal was to occupy caves with temperatures suitable for needs of each group at a particular time of the year. Nursery colonies are located in caves with temperatures of ¢.19°C, those used for hibernation have temperatures of ¢.11-5°C, and those used during transitions have intermediate temperatures that allow beneficial daytime torpor. A second cause of movement can be access to foraging areas with better ambient temperatures and better insect availability. After hibernation, female Schreibers’s Long-fingered Bats migrated to spring or equinoctial roosts and again to maternity roosts just before parturition. Soon after young were weaned, females migrated to equinoctial roosts where they spent autumn and sometimes winter. Pattern of migration of males was similar to that of females, but they left and arrived at hibernacula later and remained more mobile during the maternity season. Young remained in warm nurseries longer than their mothers, presumably because high temperatures of nurseries help increase growth. Maternity colonies spent the yearly cycle in well-defined home ranges (mean 19 km?) that overlapped greatly. Individuals were furthest from maternity sites during hibernation, but even then, 80% remained within 90 km of them. Each hibernaculum attracted individuals from multiple nurseries within 10-8 km? Females in Portugal were highly philopatric. This has an important impact on genetic structure of the populations such that nursery colonies have strong geographic structure. Females do not affect gene flow among colonies, but males do because during the mating season, individuals of both sexes from different colonies meet in certain refuges. Greater genetic diversity is found in these mating shelters and hibernacula. Displacement among roosts can exceed 300 km, but most are less than 100 km. Because of the seasonal nature of these movements and distances involved, Schreibers’s Long-fingered Bat is considered a regional migrant. In these migratory and commuting flights, individuals use rivers as landmarks for orientation and navigation. During these movements, individuals travel more than 50 km /h. Schreibers’s Long-fingered Batis very gregarious, and it, without a doubt, forms the largest colonies in Europe, although they are modest in size compared with other species of Miniopterus . In Bezanovo Parnicite Cave in northern Bulgaria, 65,000 individuals have been counted, and in Dyavolskoto Garlo Cave in the Rhodopes Mountains of southern Bulgaria, as many as 40,800 individuals were counted during hibernation. This cave supposedly hosts Schreibers’s Longfingered Bats from Bulgaria, Greece, and the Republic of North Macedonia. As many as 60,000 females and their young were counted in a nursery colony in Devetaskata Pestera Cave in Bulgaria. In Croatia, 35,000 individuals were found in a nursery colony, and more than 30,000 individuals in KusStrovka Cave and 27,000 in a hut of Visti¢ina were hibernating in Trbusnjak. These bats are probably part of the Pannonian—Dinaric metapopulation that includes populations from Austria, Slovakia, Hungary, Slovenia, and Croatia whose existence has been revealed through marking studies. In Portugal, the Cave of Marvao Island has a colony of¢.20,000 breeding and hibernating individuals. In Spain, the largest hibernation colony is 33,000 individuals and is located in an abandoned train tunnel. Longest longevity record for Schreibers’s Long-fingered Bat 1s 16 years.

Status and Conservation. Classified as Near Threatened on The IUCN Red List. Schreibers’s Long-fingered Bat has been extirpated in Germany and Ukraine and has declined to near extirpation in Switzerland since the 1960s. Similarly, a hibernating population in Austria has declined from 2500 to only 1-2 individuals, and all maternity colonies have been lost. It is included in Annex II (and IV) of the EU Habitats and Species Directive and hence requires special measures for conservation including designation of Special Areas for Conservation.

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Figures

1. Asian Long-fingered Bat (Miniopterus fuliginosus), 2. Large Long-fingered Bat (Miniopterus magnater), 3. Small Long-fingered Bat (Miniopterus pusillus), 4. Intermediate Long-fingered Bat (Miniopterus meduius), 5. Ryukyu Long-fingered Bat (Miniopterus fuscus), 6. Eschscholtz’s Long-fingered Bat (Miniopterus eschscholtzii), 7. Philippine Long-fingered Bat (Miniopterus paululus), 8. Great Long-fingered Bat (Miniopterus tristis), 9. Shortridge’s Long-fingered Bat (Miniopterus shortridgei), 10. Javanese Long-fingered Bat (Miniopterus blepotis), 11. Little Long-fingered Bat (Miniopterus australis), 12. Small Melanesian Long-fingered Bat (Miniopterus macrocneme), 13. Loyalty Long-fingered Bat (Miniopterus robustior), 14. Australian Long-fingered Bat (Miniopterus orianae), 15. Pallid Long-fingered Bat (Miniopterus pallidus), 16. Schreibers’s Long-fingered Bat (Miniopterus schreibersu), 17. Neghrohion Long-fingered Bat (Miniopterus maghrebensis)

Distribution. S Europe from Iberian Peninsula E to N & W Anatolia ( Turkey ) and W Georgia , N to C France , Slovakia , and Romania , and S to Morocco , N Algeria , Tunisia , NW & NE Libya (Tripolitania and Cyrenaica), Syria , Lebanon , Israel , and possiblyJordan, also on most Mediterranean Is; historical records or occasionally in SW Germany , Switzerland , and Czech Republic . In the Maghreb,it shares habitat with the Maghrebian Long-fingered Bat ( M. maghrebensis ) and in Levant with the Pallid Long-fingered Bat ( M. pallidus ), but distributional limits in these areas are not well defined.