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Barbastelle bats (Barbastella spp.) specialize in the predation of moths: implications for foraging tactics and conservation
Acta O~cologica, 1997, 18 (2), 91-106
Barbastelle bats (Barbastella spp.) specialize in the predation of moths: implications for foraging tactics and conservation Antoine Sierro (1) and Raphael Arlettaz (2, 3 , ) (2)
( x) Institute of Zoolog3, University of Neuchdtel, Switzerland. Institute of Zoology and Animal Ecology, University of Lausanne, Switzerland: (3) Present address and for correspondence: School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 lUG, UK. Phone~Fax: +44 117 927 69 94 E-mail: Raphael.A rlettaz@izea, uniL ch
Received: 7.11.95
Accepted: 21.I 1.96
Abstract The diet of barbastelle bats, Barbastella (b.) barbastellus and B. (b.) teucomelas, captured, respectively, in the Swiss Alps and in the Kirghiz Tien Shian and Pamir mountains (central Asia) was investigated through faecal analysis. Location of hunting habitats and data on foraging behaviour of Swiss barbastelle bats were obtained from radiotracking. In either area, ca. 99% of prey by volume consisted of Lepidoptera. The regular occurrence of one small arctiid species in the diet of Swiss barbastelles, as well as the predominance (84%) of tympanate moths among the Lepidoptera sampled at foraging sites suggest that B. barbastellus could prey to a large extent on smaller tympanate moths. Observations of foraging bats showed that, in the study area, barbastelles behaved as typical aerialhawking bat species, although they hunted exclusively just above the forest canopy. This aerial-hawking bat species has seemingly evolved a peculiar foraging technique to overcome the defence system of its probable tympanate prey. The diet of Barbastella appears one of the narrowest among Palaearctic bats. Such a specialization in foraging habits probably points to a higher vulnerability of this species, as compared to other more flexible aerial-hawking bats, to negative changes in the abundance of moth populations. This could explain its current rarity throughout most of Europe.
Keywords: Barbastella, Chiroptera, conservation, diet, echolocation, endangered species, evolutionary arms race, Lepidoptera, light trap, predator-prey relationship, trophic ecology.
R~sum~ Au moyen d'analyses f6cales, nous avons 6tudi6 le r6gime alimentaire des chauves-souris barbastelles, Barbastella (b.) barbasteUus et B. (b.) leucomelas, tant dans les Alpes valaisannes (Suisse) que dans les chaines des Tien Shian et Pamir Alaf (Kirghizstan, Asie Centrale). En Suisse, des donntes sur tes habitats de ehasse et le comportement de fourragement ont 6galement 6t6 obtenues par
* To whom reprint requests should be addressed.
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A. Sierro and R. Arlettaz
radiopistage. Dans les deux rtgions gtographiques, les 16pidopt~res constituaient environ 99 % du volume des proies consommtes. La prtsence rtguli~re d'une petite esp~ce d'Arctiidae dans les 6chantillons de crottes en provenance des Alpes, ainsi que la nette prtdominance (84 % en frtquence) des 16pidoptbres tympants dans les pitgeages lumineux effectuts au sein de la zone de chasse visitte p a r la population suivie par radiottltmttrie, sugg~rent que B. barbastellus est sptcialis6 dans la prtdation des petits 16pidopt~res nocturnes tympants. Les observations de radiopistage ont montr6 que les barbastelles se comportaient comme des chasseurs atriens typiques ; toutefois, elles concentraient leur effort de chasse dans une zone situte juste au-dessus de la canopte des boisements forestiers. Cette esp~ce a semble-t-il dtvelopp6 une strattgie de prtdation (syst~me sonar ?) tout-~-fait paxticuli~re pour dtjouer le systtme auditif de ses proies tympantes. La niche trophique de la barbastelle est l'une des plus 6troites et sptcialistes parmi les chauves-souris paltarctiques, ce qui sugg~re une vulntrabilit6 accrue de l'esp~ce, par rapport aux autres chauves-souris chassant 6galement des proies atriennes, tout changement ntgatif au sein des populations de 16pidopt~res nocturnes. Ceci expliquerait sa raret6 actuelle dans la majeure partie de l'Europe.
INTRODUCTION The barbastelle bat, Barbastella barbastellus, is currently considered as one of the most endangered bat species in western Europe (STEBBINCS & GRIFFrrrt, 1986; STEBBINOS, 1988). Over the past decades, severe population declines or even local extinctions have been reported by many bat workers, and the range of this species seems now very patchy, apparently mostly restricted to upland areas (e.g. R]CnARZ, 1989; BENZALetal. 1991; Zn~oc, 1994). On Col de Bretolet, at the French-Swiss border, for instance, B. barbastellus was the second most abundant bat species mistnetted by ornithologists in the late '50s and early '60s, but the frequency of capture of this species has dropped dramatically since then (fig. 1). In contrast with western
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FIG. 1. - Relative number of barbastelle bats (B. barbastellus in percent of all bat captures) mist-netted by ornithologists on Col de Bretolet (Valais, Switzerland, and Haute-Savoie, France) over 23 years (19581994; years with no netting activity or totalling < 30 bat captures have been excluded). Data presented here include 162 captures of 13. barbastellus for a total of 1676 bats caught. Source: database of the "Rdseau Chauves-souris Valais" (R. ARLETTAZ,A. LUC,ON & A. SXERRO,unpublished).
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Barbastelle bats prey on moths
Europe, there are still sizeable wintering colonies in central eastern Europe (URBANCZYK, 1991; UHR~q, 1994-95), suggesting that this species is less threatened or vulnerable there. Similarly, the eastem Asian form leucomelas, which is either considered a distinct valid species (CORBET, 1978; NOWAK, 1991; FROST & TtMM, 1992) or simply a subspecies of B. barbastellus (QuMslWIa, 1985), does not seem to be in such a critical situation (e.g. RYBINet al., 1989). The reasons for the decline of western European barbastelles have not been identified (SVEBBrNGS& GRIFFrrH, 1986). Indeed, only data on the diet of B. barbastellus are currently available (BECK, 1994-95; RYDELL et al., 1996); this situation impedes proposing any concrete conservation measures. Specialized predators relying on few prey types are generally more vulnerable than generalist, more flexible predators. The present study aims at testing the hypothesis that highly specialized foraging habits could account for the drastic decline recently faced by western barbastelle bats. We thus compare the diets of barbastelles occurring both in the western Palaearctic (form barbastellus) and in the eastern Palaearctic region (form leucomelas), and discuss dietary niches in the context of prey abundance (estimated by light-trapping), foraging tactics (as revealed by radiotracking and visual observation), and trophic specialization, drawing possible implications for the species conservation. METHODS
AND STUDY AREA
Droppings were collected from individuals mist-netted by the authors at underground entrances both in the Swiss Alps (Mont Chemin, Valais; n = 33) and in the Tien Shian and Pamir mountains of central Asia (Kirghizstan; n = 16); some additional captures were made by ornithologists in late summer and autumn on Col de Bretolet (Valais, Switzerland; n = 4) (table I). Bats were held in linen bags and faeces collected before releasing them at night.
TABLEI . - Localities where faecal samples of barbastelle bats have been collected: country, region (canton
for Switzerland; district for Kirghizstan), locality, coordinates, altitude, date of collection, number of bats that yielded faeces. Country Switzerland
Region Valais Valais
Kirghizstan
Kocbkorskyi Jetiogjuzskyi Aravanskyi Nookatskyi Nookatskyi Batkensykyi
Total
Vol. 18, n ~ 2 - 1997
Locality
Coordinates
Altitude
Date
n bats
1200 m
22 11 4
Mont Chemin (mine) Bretolet pass
46~
7~
46~
6~
1920 m
8.5.92-8.10.92 19.6.93-30.8.93 27.8.92-7.9.92
Cholpon (salt mine) Chong Jargylchak Dangi Tuja Mujun Aktala Ak Dzhilga Kanigut mine (Gherm)
42~176
2100 m
24.8.92
2
42~176 40~176 40~176 39~176 39~176
1950 m ll00m 1800m 2200 m 1570 m
1.9.92 16.9.92 24.9.92 25.9.92 30.9.92 2.10.92
1 1 2 5 5 53
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A. Sierro and R. Arlettaz
In the laboratory, faecal material was dissected under a binocular microscope (magnification up to 60x) and prey remains were identified referring to identification guides (e.g. MCANEYet aL, 1991), to the collection of the Museum of Natural History of Sion, and to insects gathered at the study site. For each dropping, the percentage of volume occupied by a given prey category was estimated to the nearest 5-10%. An overall percentage was then calculated for each individual sample, one sample consisting of all droppings collected from one individual (ARLEa~rAZ, 1995). The reliability of faecal analyses to quantify the composition of bat diets has been demonstrated several times: e.g. KtJNZ & WHITAKER(1983) and DICKMANN8Z HUANG(1988). At Mont Chemin, Switzerland, seasonal variation in food abundance was estimated by lighttrapping insects within the main foraging area of a small population of B. barbastellus whose home range was delimited by radiotracking (see below). Light-traps are generally considered as a relatively good tool to estimate the abundance of aerial, nocturnal insects (MUIRHEAD-THOMSON,1991), although serious biases are to be expected, particularly with insect species which do not present a positive phototactism (Kuyz, 1988). Insect trapping sessions were performed between April and October 1992 during seven nights (one night per month). Trapping was deliberately restricted to calm and dry nights with reduced or no moon light, i.e. on nights offering the most favorable sampling conditions. Insects were identified to the order or family level, except for Lepidoptera where determination to the species level was often possible. Identification guides (e.g. CHINERY, 1988) as well as the collections of the Museum of Natural History of Sion served as a reference basis. As regards moth systematics, we refen'ed to LERAUT(1980). Radiotracking sessions took place at Mont Chemin (Valais, Swiss Alps) from June through to October 1992, with complements in June 1993. Bats were mist-netted at the entrance of two abandoned mine gaieties, and fitted with small glue-on (cyanocrylate glue) radiotransmitters (BD2B; 0.65-0.68 g, Holohil Systems Ltd, Ontario, Canada). Because of strong topographic constraints, the standard tag was modified by the producer so as to maximize detection range (ca. 1.5 kin); this resulted in a reduced battery lifespan. A piece of reflector tape (ScotchliteTM) fixed on the upper side of the tag enabled location and identification of the tracked individual in the field through direct visual observation with the help of a night scope (Big III, Wild-Leitz, Leica SA, CH-1020 Renens, Switzerland) coupled with an infrared halogen lamp. Twelve radiotracking sessions were performed on 11 individuals (8 males and 3 females). Bright 8 • 56 binoculars (Habicht TM) were used in the twilight to watch the foraging behaviour of freshly emerged bats. An ultrasound detector (Mini bat II, Summit, Birmingham, B18 5NY, UK) was used to assess the identity of untagged individuals according to AHL~N (1990). This author states that ((using a good quality detector, the experienced observer can't miss this species>>. Bats were tracked on foot from dusk to dawn by one single observer equipped with a radio-receiver (Wagener, Herwarthstrasse 22, D-50000 K61n, Germany) and a H-antenna. Locations were obtained using the ((homing-in on the animab> method (WHITE & GARROTr, 1990). Field observations were recorded on a walkman tape-recorder. The habitat surrounding the Swiss mine (Mont Chemin), where most faeces were gathered and where radiotracking sessions took place, consists mostly of a mixture of xeric pine (Pinus sylvestris), oak (Quercus pubescens) and spruce (Picea abies) lbrests growing on stony outcrops and steep slopes; however, patches of traditional meadowland and a small village are also present on a nearby plateau. The typical vegetation around the alpine pass is characteristic of the upper edge of the subalpine forest, with Picea abies and Alnus viridis as dominant tree species. By contrast, the environment around sampled Kirghiz localities consisted mainly of xeric habitats including steppe and subdesert areas, and forests were totally absent.
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Barbastelle bats prey on moths
RESULTS
Diet composition A total of 53 (n = 37 for Switzerland, n = 16 for Kirghizstan) individual faecal samples comprising 246 droppings was analysed; one individual faecal sample thus consisted, on average, of 4.6 faeces. Only four insect orders were identified in faeces: Lepidoptera, Neuroptera, Trichoptera and Diptera; moreover, the last two categories appeared only in the Swiss material. In both study areas, and during all months, the diet consisted almost entirely of Lepidoptera (fig. 2); overall monthly means were
[]
Lepidoptera
[]
Neuroptera
[ ] Trichoptera
9
Diptera
I
Switzerland
10080-
6040A
20-
E "= 0O > Kirghizstan co 100-
4=,1
m.
8060-
4020. May
June
July
Aug
Sept
Oct
Month FIG. 2 . - Seasonal diet composition (percent volume) of individual Barbastella captured in Switzerland and Kirghizstan (for more details about locations, see table I). Sample size is given at column foot.
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A. Sierro and R. Arlettaz
98.9% and 99.4% by volume in Switzerland and Kirghizstan, respectively. As is the rule with Lepidoptera fragments in bat droppings (MeANEr et al., 1991; SHmL et aL, 1991; RVDELL& ARLEa'a'AZ,1994), it was not possible to establish which families were present; however, fragments were typical of moths (antennae; uncoloured scales except in July and August, see below; densely haired legs) and there was no evidence of the presence of diurnal Lepidoptera in the faeces. This observation is further supported by the predominance of bright yellow scales in the faeces of the Swiss barbastelles in July and August. As revealed by the insect trapping, the only Lepidoptera species in that area exhibiting such a bright colour is Eilema complana, a small arctiid of the subfamily Lithosiinae, which appeared abundantly in July and August in the light trap. Neuroptera (Hemerobiidae) fragments represented, overall, only 0.4% and 0.6% of Swiss and Kirghiz faecal samples, respectively. Among the 37 Swiss faecal sampies, minor portions of Hemerobiidae were present in only two samples from July (10 and 5% of the sample volume, respectively). Similarly, only two of the 16 Kirghiz samples comprised this prey category (5% each). Trichoptera and Diptera (Cecidomyiidae) were each recorded in only one Swiss sample. Only two leg fragments of moths provided information about the size of the eaten prey, by comparison with items of the reference collection; they both indicated a wingspan of ca. 25-30 nun. According to the moth species caught at the foraging site, this roughly corresponds to the body size of a small-sized moth, e.g. of the family Pyralidae.
Prey abundance at foraging grounds As revealed by light trapping, insect abundance within the main foraging area of the population of B. barbastellus at Mont Chemin (Switzerland) showed a large predominance of Diptera and Lepidoptera throughout the season (fig. 3). These two insect categories represented, respectively, as much as 52% and 36% of the total number of items recorded (n = 7404). However, ca. 90% of the Diptera items were very small (< 8 mm body length); only Limonidae and Tipulidae exhibited larger body sizes. Nocturnal Lepidoptera were by far the most abundant medium- and large-sized insect prey found in the trap. Among the moths, small specimens (wingspan < ca. 30 mm) were more abundant (69%) than larger ones (> ca. 30 mm wingspan; 31%) (table II and fig. 4). According to the species collected at the site, the small size class comprises all the families of the suborder Microlepidoptera but also some Macrolepidoptera, the Nolidae and the Lithosiinae (Arctiidae). Accordingly, the second class corresponds to the suborder Macrolepidoptera, minus the two above mentioned groups. Pyralidae were by far the most abundant Lepidoptera family (44%), followed by Geometridae and Noctuidae (14% and 16%, respectively). Moth families for which the existence of auditory organs - hereafter called "tympanate" although Sphingidae have palpal hearing organs (SCO~LE, 1992) - has been evidenced largely predominated from spring to autumn (table II, fig, 4); their overall proportion was as high as 84% of the total moth population (table II and fig. 4). Three taxa were particularly abundant, totalling 44.4% of trapped moths: Catoptria permutatella, Scoparia sp. (both Pyralidae) and the yellowcoloured Eilema complana (Arctiidae: Lithosiinae). Ac~(Eco~gwa
97
Barbastelle bats prey on moths
1500
1000
,,Q
500
~
r~A l'/~'rnetT~ C~
-'4Pr/7
a
/z Neuroptera /~at~ a , ,HOmo#tera Netero#tera TrichoPtera
Seasonal abundance (number of items) Of the main insect categories light-trapped within the foraging area of a small population of Barbasteila barbastellus in the Swiss Alps (Mont Chemin, V a l a i s ) .
FIG. 3. -
Hunting grounds and foraging behaviour The eleven radiotracked individuals carried transmitters for a total of 29 days. Because of complex topography, adverse weather conditions and, possibly, transmitter defect, only 8 :individuals provided information on foraging areas over 19 nights (average: 2.1 nights per successful radiotracking trial); one individual was radiotracked during two successive field seasons (table III). All the bats foraged on a steep slope covered by xeric forest vegetation, consisting mainly of Pinus sylvestris, between 900 and 1200 m altitude; human settlements and open habitats such as meadVol: 18, n ~ 2 -
1997
98
A. Sierro and R. Arlettaz
TABLE II. -- The different families and subfamilies of nocturnal Lepidoptera collected with light trap in the foraging area o f B. barbastellus at Mont Chemin (Valais, Switzerland) with respect to occurrence frequency (absolute and percentage; n total = 2658 items), to body size (L = large tara, i.e. wingspan > - 3 0 mm; s = small tara, i.e. wingspan < - 3 0 ram) and to the presence~absence of auditory organs according to literature (e.g. SCOeLe, 1992) (symbol "-"." no evidence of auditory organs).
Taxa Microlepidoptera Limacodidae Ethmidae
Gelechiidae Yponomeutidae Tortricidae Pyralidae Pterophoridae Macrolepidoptera Lasiocampidae Thyatiridae Geometlidae Sphingidae Notodontidae Lymantriidae Arctiidae Lithosiinae Arctiinae Callimorphinae Nolidae Noctuidae
n
1 1 120 8 223 1180 2 17 1 373 10 6 12 267
%
Body size
4.5 8.4 44.4
14
tympana
L L L L L L
10.1
s L L 16 421
Hearing organ
tympana
tympana palpal hearing system tympana tympana tympana tympana tympana
tympana
s 15.8
L
tympana
owland were avoided. The area of the minimum convex polygon drawn from the most external radio-locations of the radio-tagged population amounted to 56 ha, whereas the mean estimated individual home range was 8.8 ha (SD = 5.8 ha; n = 8). Given that bats were usually loyal to their feeding zones over successive nights, this high variance merely reflected the great seasonal and interindividual variation in the area prospected by individual bats. Some individual feeding grounds overlapped, but we could not assess the simultaneous presence of two or more foraging bats at the same hunting territory. Daily roosts consisted of rocky crevices situated in cliff walls located within the foraging area of the radio-tracked population. We succeeded to observe visually (with the night scope) radio-tagged barbastelle bats while foraging during only two short periods of less than two minutes each on only two nights, at a distance of 10-40 m. The main reason for the lack of direct observation of foraging bats carrying radiotransmitters was mostly the difficult local topography. Fortunately, additional observations with binoculars could be made at more accessible places in the same site on eight further occasions (totalling more than 25 minutes of direct visual contact), while untagged individuals were performing their first foraging bouts at dusk. Then, bat identification was achieved in the field by using an heterodyne bat detector tuned at 30-35 KHz, according to the criteria outlined by Ar~LEN (1981, 1990; see Methods). All foraging barbastelle bats we could watch were Acta (Ecologica
Barhastelle bats prey on moths
99
600
400
_~
" 200
fo,~//fOo
v ~- f ~ o ~ , 9~
J'e.,~ r
o cl
[ ] moths with auditory organs
z,9~
""
"~
~4'<.oe .,-Ooz,/_/~"
[ ] moths with no evidence of auditory organs
Seasonal comparison of the abundance (number of items) of small vs. large and tympanate vs. nontympanate moths within a foraging zone used by foraging barbastelle bats in the Swiss Alps (Mont Chemin, Valais).
FIG. 4 . -
flying just above the forest canopy, ca. 2-4 m above tree crowns. The flight was fairly adroit, and speed appeared slow to moderate. We could not observe barbastelle bats gleaning prey directly from the uppermost tree branches. DISCUSSION
Trophic niche Consisting almost exclusively of moths, the diet of Barbastella appears to be the narrowest yet found for Palaearctic bat species. This high diet specialization was Vol. 18, n ~ 2 - 1997
100
A. Sierro and R. Arlettaz
TABLEIII. -- Summary of the 12 radiotracking trials carried out in 1992-93 on 11 individual barbastelle bats
at Mont Chemin (Valais, Switzerland); from left to right: individual (ring number), sex, age, period with recorded signal emission, and number of nights with monitored foraging activity. Individual
Sex
Age
Period
N 134 N 141 K 724
male male male
adult subadult adult
M 139 N 143 N 144 K 592 N 145 N 133 N 148 N 201
male male female male female male female male
adult adult subadult adult subadult adult adult adult
16-17.06.92 22-23.06.92 03.07.92 08.06.93 31.07-05.08.92 04.08.92 11-13.08.92 10-13.08.92 06.09.92 14-16.09.92 08-09.10.92 27-30.06.93
Total
Number of nights with foraging activity recorded 1 1 0 0 4 0 2 3 1 3 2 2 19
already pointed out by BECK (1994-95) and RVDELLet al. (1996). However, the proportion of moths is even greater in our study than in the latter two. To some extent, this may reflect differences in sampling procedures. First, contrary to BECK(1994-95) and RVOELLet al. (1996), who analysed droppings gathered from underneath roosts, we collected faecal samples directly from mist-netted individuals. Given that variation of bat diet composition is chiefly due to inter-individual variation rather than to within individual variation (e.g. ARLE~AZ, 1995; p. 105), that discrepancy may be merely methodological. It cannot be excluded, however, that the guano investigated by BECI~ (1994-95) and RYDELLet al. (1996) had been contaminated by other bat species which could roost together with barbastelles from time to time; a guano contamination might also explain the presence of scarce debris of non-flying prey (e.g. Araneae) in the latter study. Since faecal samples in the present study were collected from quite different mountainous environments in the Swiss Alps (forest) and in the Kirghiz Tien Shian and Pamir Alai ranges of central Asia (steppe), the trophic specialization of barbastelle bats clearly does not stem from the use of similar habitat types in both areas, and therefore points to a highly species-specific diet selectivity and/or foraging constraint in Barbastella. Because of their slender skull morphology, as compared to other vespertilionid bats of similar body size (ScHOBER& GRt~ERGER, 1987), barbastelle bats are probably not able to capture larger insects (FREEMAN,1981) and should feed on more abundant, smaller moth prey items (e.g. Tortricidae, Pyralidae or Lithosiinae), most of which are tympanate (table !I). Although direct evidence about prey body size refers to only two leg fragments in this study, this view is also supported by the regular occurrence of scales of the small yellow-coloured arctiid moth species Eilema complana (ca. 30 mm wingspan; Lithosiinae, table II) in the faeces of Swiss barbastelles in July and August. Acta GEcologica
Barbastelle bats prey on moths
101
Among the other European bat species, only Tadarida teniotis (RYDELL8Z ARLETTAZ, 1994) and Plecotus austriacus (BECK, 1994-95) seem to feed, but to a lesser extent than Barbastella, on moths (< 90% by volume and frequency, respectively). Two North American bat species have also been reported to include mostly moths in their diets: Euderma maculatum and Plecotus townsendii (WAI-PING 8Z FENTON, 1989; SAMPLE(~ WHITMORE,'1993). Tadarida is a molossid bat, whereas Plecotus and Euderma are representatives of the long-eared bats of the tribe Plecotini (Vespertilionidae), which also includes the genus Barbastetla (see below). A singular foraging tactics?
As far as we know, bats seem to have evolved three different foraging strategies to overcome the defence mechanisms evolved by insects that possess auditory organs. Aerial-hawking bats may first emit very low intensity calls which are particularly undetectable to prey or, second, they may glean prey from substrates relying on passive acoustical cues (e.g. sounds generated by moving targets) instead of on echolocation. In the Holarctic zone, these two strategies seem widespread among the vespertilionids belonging to the genus Myotis and to the tribe of plecotine bats (Plecotus, Euderma, etc.; FAURE et al., 1990; ANDERSON& RACEY, 1991; FAURE & BARCLAY, 1994). Thirdly, bats may also use frequencies below or above the range of best auditory sensitivity of prey (the "allotonic frequency" hypothesis; NovIcK, 1977; FENTON & FLrLLARD,1979; FULLARD,1987; JONES, 1992). Of the three above-mentioned moth predators, Plecotus auritus and P. townsendii behave mostly like typical passive listeners while gleaning (e.g. ANDERSON& RACEr, 1991; SAMPLE & WH~TMORE, 1993), whereas Tadarida teniotis and Euderma maculatum are exclusive aerial foragers which both use very low frequency calls (ca. 1012 kHz) that are clearly audible to the human ear (LEONARD& FENTON, 1984; ZBINDEN & ZINGG' 1986). The available data on the echolocation of barbastelle bats denote a very singular detection system in these bats, probably unique among the Holarctic bat species. Firstly, JONES (1993) suspected very unusual sonograms, shaped like an inverted "J" in this species, a "convex" call design not reported for other European vespertilionid bat species which all exhibit "concave" calls. Secondly, field ultrasound recordings suggest that foraging Barbastella typically emit two different types of calls, either loud or weak pulses, at ca. 32 kHz and 42 kHz, respectively (AHLEN, 1981) 1. If barbastelle bats are actually preying mostly on tympanate moths, we may speculate that low frequency, high-intensity pulses could be used during the detection phase, whereas the low-intensity calls - particularly unconspicuous to tympanate prey could be restricted to the approach and capture phase; this could also explain why free-ranging foraging barbastelle bats typically emit either pure sequences of low frequency calls or alternate the two types of calls (AHLEN, 1981; P. ZINGG, in litt.). However, it cannot a priori be excluded that barbastelle bats might perhaps simply rely on a "passive-listening" strategy instead of echolocation, at least during the last phase of prey capture. Our visual observations of foraging B. barbastellus confirm that this species is primarily an aerial-hawking forager adept at foraging close to clutter since our bats 1. K. G. I-IELLERand E ZrNGO(unpublisheddata) havefoundsimilarcall patterns(pers. comm.). Vol. 18, n~2 - 1997
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A. Sierro and R. Arlettaz
were hunting just above the forest canopy (AHLI~N, 1990; NORBERG& RAYNER, 1987). In the present study, bats did apparently not glean prey from surfaces; indeed, there is no evidence as yet that barbastelle bats occasionally glean prey from substrates, as suggested by RYDELLet al. (1996). Besides, the arthropods which are captured by typical substrate-gleaning bat species (e.g. BECK, 1994-95) miss totally in barbastelle's diet. Unfortunately, we could not see the patrolling barbastelles "pausing, and rising a little with near-hovering flight" as described by AHLI~N(1990). Interestingly, these observations would be consistent with the hypothesis that Barbastella might actually rely on passive acoustic cues (the noise produced by fluttering moths?) to capture its flying prey. Additionally, KONSTANTINOV& MAKAROV(1981) have suggested that its unusual ear morphology provides Barbastella with a strongly enhanced hearing directionality, a character usually shared by passive listening bats (OBRISTet al., 1993).
Evolutionary context According to VOLLETH(1985) and FROST& T~M (1992), the short ears - at least relatively to other plecotine bats - of Barbastella are probably a synapomorphy of this genus, i.e. barbastelle bats have probably evolved reduced ear size from a Plecotuslike ancestor. Barbastelle bats may therefore have retained some basic features of the hunting behaviour of their ancestors as well (see COLES et al., 1989), although they have presumably switched to an aerial-foraging strategy. The use of low intensity calls or even of passive listening, both typical of most plecotine bats (ANoERSON& RACEr, 1991; WATERS& JONES, 1995), as well as the ability to perform flight pauses accompanied by almost hovering sequences (AnL~N, 1990), could be part of this legacy.
Prey selection and community organization Contrary to most European aerial-hawking vespertilionid bat species that are flexible predators including different insect categories in their diets (see the review by RYDELL et al., 1995), Barbastella is apparently very restricted in its food choice. A narrow diet usually reflects a trophic specialization. Moreover, RYDELLet al. (1995) have proposed that a bat subsistence based primarily on nocturnal moths should require a highly specialized predator because most of these prey exhibit auditory organs tuned to the main frequencies used by aerial-hawking bats. In Barbastella, however, such a specialization would not necessarily result from active prey selection. Indeed, passive selection sensu FAURE & BARCLAY (1992) may also be possible because: 1) moths appeared particularly abundant at the Swiss feeding habitats; 2) the singular morphology and echolocation system of Barbastella may imply particular foraging constraints. This view is furthermore consistent with the current opinion that active prey selection has so far not been conclusively established among insectivorous vespertilionid bats (e.g. ARLETTAZ& PERPaN, 1995). However, in the case of Barbastella, the question remains why these bats do not catch other types of prey which also occur at their feeding places, e.g. Hymenoptera, Coleoptera or large-sized Diptera (this study). It is hard to imagine that drastic design constraints could enable Barbastella to catch moths but not other flying prey of similar body size, unless 1) barbastelle bats use passive listening for prey capture and 2) moths are more noisy on the wing, other things being equal, than other flying insects, i.e. more conspicuous for a passive-listening predator. Competition with coexisting Acta CEcologica
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insectivorous bat species within the s a m e c o m m u n i t y could, o f course, force Barbastella to feed exclusively on moths. Their suspected r e m a r k a b l e capability to catch flying t y m p a n a t e moths, either through echolocation or passive listening, might be so advantageous, however, that the capture o f other prey types c o u l d eventually be neglected. I m p l i c a t i o n s for c o n s e r v a t i o n
On the other hand, a p r o b a b l e disadvantage o f the singular niche o f Barbastella is that this species c o u l d o n l y survive in areas which yield sufficient populations o f moths. This suggests a high vulnerability o f barbastelle bats to negative changes in the density o f their prey. T h e progressive destruction o f cultivated landscapes in western Europe, including the intensification o f farming practices and the use o f pesticides against m a n y m o t h species w h i c h are a m o n g the most detrimental pests in agriculture (e.g. Pyralidae, Tortricidae, Noctuidae), have r e d u c e d moth populations (HEvt)EMANN, 1980; BLAB & KUDRNA, 1982; SCHWARZ, 1983; GEIGER, 1987; CHARMILLOT et al., 1994). This m a y have affected Barbastella's s u r v i v a l and reproduction, either directly through the loss o f suitable foraging habitats and/or indirectly through poisoning. The g l o b a l impact o f street l a m p s on m o t h populations m a y also be questioned. If street l a m p s can locally provide advantages to individual foraging bats (e.g. RYDELL, 1991, 1992), severe crashes in moth populations have been reported within intensely illuminated areas (GEPP, 1981; GEIGER, 1987). The recent p h e n o m e n a l extension o f street lamps might thus have p l a y e d some role in the decrease o f barbastelle bats in western Europe. Are these the reasons why relict populations o f barbastelle bats subsist apparently n o w a d a y s m o s t l y in s o m e eastern E u r o p e a n countries and in remote, better preserved m o u n t a i n o u s areas o f western Europe?
ACKNOWLEDGMENTS We acknowledge Prof. W. MATTrmY,Prof. C. MERMODand J. M. WEBERwho supervised this study. We thank P. MOSnVtANNand E "rta~aAN who collected faeces on Col de Bretolet, as well as G. DANOLIr,,ER, E. KASWEKOV,J. M. PtLLET, S. RYBn~ and J. Z~A who took part in the trip to Kirghizstan. A. Coa'rv, J. C. ROBERT,N. VONROTENand C. StE~Er,~rnALERgave advice on the methods of insect trapping and identification. J. M. DAYER,C. LANDRYand J. C. PRAZand SmRRO'Sfamily provided technical assistance. D. CnEPaXand K. G, HELLERprovided literature on moths and streetlamps. Our best thanks also to K. G. HALER,G. JONES, P. RACEV,J. RVDELL,D. WATERSand P. ZIN~Gfor their thorough appraisal of the manuscript. Captures in the Swiss Alps were undertaken under licence from the Nature Conservancy Service of State Valais. AS was supported financially by the Rrseau Chauves-sourisValais and Fondation Mariftan; RA's expedition to Kirghizstan was funded by the Socirt6 Acadrmique Vaudoise, Fondation Marirtan, Basler Stiftung for zoologische Forschung, Acadrmie Suisse des Sciences Naturelles, Fondation Georgine Claraz, Fondation du 450e anniversairede l'Universit6 de Lausanne and Musre zoologique de Lausanne.
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ANDERSON E. & RACEY P. A., 1991. - Feeding behaviour of captive brown long-eared bats Plecotus auritus. Anita. Behav., 42, 489-493. ARLETTAZ R., 1995. - Ecology of the sibling mouse-eared bats (Myotis myotis and Myotis blythii): zoogeography, niche, competition, and foraging. PhD thesis, University of Lausanne, 223 p. ARLEqq'AZR. & PERRIN N., 1995. -- The trophic niches of sympatric sibling Myotis myotis and M. blythii: do mouse-eared bats select prey? Syrup. zool. Soc. Lond., 67, 361-376. BECK A., 1994-95. - Fecal analyses of European bat species. Myotis, 32-33, 109-119. BENZAL J., DE PAZ O. & GISBERT J., 1991. - Los murcielagos de la Peninsula Iberica y Baleares. Patrones biogeograficos de su distribucion. In: BENZALJ. & DE PAZ O., eds., Los murcielagos de Espaha y Portugal Ministerio de Agricultura, Pesca y Alimentacion, Madrid, 37-92. BLAB J. & KUDRNA C., 1982. - Hilfsprogramm fiir Schmetterlinge. Naturschutz aktue|l, Kilda-Verlag, Greven, 32 p. CHARMILLOTP. J., H.~CHLERM. • PASQU1ERO., 1994. - Noctuelles et arpenteuses nuisibles en arboriculture. Rev. suisse Vitic. Arboric., 26, 367-378. CHINERY M., 1988. - lnsectes d'Europe occidentale. Arthaud, Paris, 320 p. COLES R. B., GUPPYA., ANDERSONE. t~ SCHLEGELP., 1989. - Frequency sensitivity and directional hearing in the gleaning bat, Plecotus auritus (Linnaeus 1758). J. comp. Physiol. A , 165, 269-280. CORBET G. B., 1978. - The mammals of the Palaearctic region: a taxonomic review. British M u s e u m (Natural History), London. DICKMANNC. R. & HUANGC., 1988. - The reliability of fecal analysis as a method for determining the diet of insectivorous mammals. J. Mammal., 69, 108-113. FAURE P. A. & BARCLAYR. M. R., 1992. - The sensory basis of prey detection by the long-eared bat, Myotis evotis, and the consequences for prey selection. Anita. Behav., 44, 31-39. FAURE P. A. & BARCLAY R. M. R., 1994. - Substrate-gleaning versus aerial-hawking: plasticity in the foraging and echolocation behaviour of the long-eared bat, Myotis evotis. J. comp. Physiol. A, 174, 651-660. FAURE P. A., FULLARDJ. H. & BARCLAYR, M. R., 1990. - The response of tympanate moths to the echolocation calls of a substrate gleaning bat, Myotis evotis. J. comp. Physiol. A, 166, 843-849. FENTON M. B. 8z FULLARDJ. n . , 1979. - The influence of moth hearing on bat echolocation strategies. J. comp. Physiol. A, 132, 77-86. FREEMAN P., 1981. - Correspondance of food habits and morphology in insectivorous bats. J. Mammal.; 62, 164-166. FROST D. R. & TtMM R. M., 1992. - Phylogeny of Plecotine bats (Chiroptera: "Vespertilionidae"): summary of the evidence and proposal of a logically consistent taxonomy. Am. Mus. Novitates, No 3034, 16 p. FULLARDJ. H., 1987. - Sensory ecology and neuroethology of moths and bats: interactions in a global perspective. In: FENTONM. B., RACEYP. A. & RAYNERJ. M. V., eds., Recent advances in the study of bats. Cambridge University Press, 244-272. GEIGER W., 1987. - Les papillons de jour et leurs biotopes. Espkces, dangers qui les menacent, protection. Ligue Suisse Protection Nature, Bale. GEr,P J., 1981. - Programmrahmen fiir einen umfassenden Lepidopterenschutz, Beih. Vertiff. Naturschutz Landschaftspflege Bad.-Wtirt, 21. HEYDEMANNB., 1980. - Die Bedeutung von Tier- und Pflanzenarten in Okosystemen, ihre Geflihrdung und ihr Schutz. Jahrb. Naturschutz und Landschaftspflege Nr. 30, Kilda-Vedag, Greven. JONES G., 1992. - Bats vs. moths: studies on the diets of rhinolophid and hipposiderid bats support the aUotonic frequency hypothesis. In: HORACEK I. & VOHRALm V., eds., Prague studies in Mammalogy, Charles University Press, Prague, 87-92. JONES G., 1993. - Flight morphology, flight performance and echolocation in british bats. In: KAPTEYNK., ed., Proceedings of the 1st European bat detector workshop, Netherlands bat research foundation, Amsterdam, 59-78. KONSTANTINOVA. I. & MAKAROVA. K., 1981. - Bioacoustic characteristics of the echolocation system of the European wide-eared bat Barbastella barbastellus. Biophysica, 26, 1112-1118. KuNz T. H., 1988. - Methods of assessing the availability of prey to insectivorous bats. In: KuNz T. H., ed., Ecological and behavioral methods for the study of bats, Smithsonian Institution Press, Washington, 191-210.
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KUNZ f. H. & WH1TAKERJ. O. Jr., 1983. - An evaluation of feca analysis for determining food habits of insectivorous bats. Can. J. Zool., 61, 1317-1321. LEONARDM. L. & FENTONM. B., 1984. - Echolocation calls of Euderma maculatum (Vespertilionidae): use in orientation and communication. J. Mammal., 65, 122-126. LERAUTP., 1980. - Liste systdmatique et synonymique des l_Apidopt~res de France, Belgique et Corse. Revue des LEpidoptEristes fran~ais et Bulletin de la SociEtE entomologique de France. SupplEment. Paris, 334 p. McANEY C., SHIELC., SULLIVANC. ~s FAIRLEYJ., 1991. - The analysis of bat droppings. Occ. Publ. Mammal Society, London, 14, 48 p. MUIRHEAD-THoMSONR. C., 1 9 9 1 . - Trap responses of flying insects. The influence of trap design on capture efficiency. Academic Press, London, 287 p. NORBERG U. M. & RAVNER J. M. V., 1987. - Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Phil. Trans. R. Soc. London B, 316, 335-427. NovlcK A., 1977. - Acoustic orientation. In: Wr~SATr W. A., ed., Biology of bats, vol. 3. New York, Academic Press, 273-287. NOWAKR. M., 1991. - Walker's mammals of the worM. Fifth ed. The Johns Hopkins University Press, Baltimore, Maryland. OBRIST M., FENTON M. B., E~ER J. L. & SCrmECELP. A., 1993. - What ears do for bats: a comparative study of pinna sound pressure transformation in Chiroptera. J. exp. Biol., 180, 119-152. QUMSIVEHM. B., 1985. - The bats of Egypt. Spec. Publ. Mus. Texas Tech. University, 23. RICHARZ K., 1989. - Ein neuer Wochenstubennachweis der Mopsfledermaus Barbastella barbastellus (Schreber, 1774) in Bayern mit Bemerkungen zu Wochenstubenfunden in der BRD und DDR sowie zu Wintervorkommen und SchutzmEglichkeiten. Myotis, 27, 71-80. RYBIN S. N., HORACEKI. • CERVENYJ,. 1989. - Bats of Southern Kirghizia: distribution and faunal status. In: HANAKV., HORACEKI. 8= GAISLERJ., eds., European bat research 1987, Charles Univ. Press, Praha, 421-441. RYDELLJ., 1991. - Seasonal use of illuminated areas by foraging northern bats Eptesicus nilssonL Holarctic Ecology, 14, 203-207. RVDELL J., 1992. - Exploitation of insects around streetlamps by bats in Sweden. Functional Ecology, 6, 744-750. RYDELL J. & ARLETTAZR., 1994. - Low frequency echolocation enables the bat Tadarida teniotis to feed on tympanate insects. Proc. R. Soc. Lond. B, 257, 175-178. RVDELL J., JONES G. & WAVERS D., 1995. - Echolocating bats and hearing moths: who are the winners? Oikos, 73, 419-424. RYDELL J., NATUSCHKEG., THEILERA. & ZINGG P. E., 1996. - F o o d habits of the barbastelle bat Barbastella barbastellus. Ecogmphy, 19, 62-66. SAMPLE B. E. & WHiTMORE R. C., 1993. - Food habits of the endangered Virginia big-eared bat in West Virginia. s Mammal., 74, 428-435. SCHOBER W. & GRIMMBERGER E., 1987. - Die Fledermiiuse Europas: kennen, bestimmen, schiitzen. Franck'sche Vedagshandlung, Stuttgart, 222 p. SCnWARZU., 1983. - Der Naturgarten. Kriiger-Veflag, Frankfurt, 7th edition. SCOBLE M. J., 1 9 9 2 . - The Lepidoptera. Form, Function and Diversity. Oxford University Press, London. SHIEL C. B., MCANEY C. M. & FMRLEY J. S., 1991. - Analysis of the diet of Natterer's bat Myotis nattereri and the common long-eared bat Plecotus auritus in the West of Ireland. J. Zool. Lond., 223, 299-305. STEBBrNGS R., 1988. - Conservation of European bats. Christopher Helm, London. STEBBINGS R. & GRIFFITH E, 1986. - D i s t r i b u t i o n and status of bats in Europe. Institute of Terrestrial Ecology, Monks Wood Experimental Station, Huntingdon, Great Britain. UnRLN M., 1994-95. - The finding of a mass winter colony of Barbastella barbastellus a n d Pipistrellus pipistrellus (Chiroptera, Vespertilionidae) in Slovakia. Myotis, 32-33, 131-133. URBANCZYKZ., 1991. - Hibernation of Myotis daubentoni and Barbastella barbastellus in Nietoperek bat reserve. Myotis, 29, 115-120. VOLLETH M., 1985. - Chromosomal homologies of the genera Vespertilio, Plecotus and Barbastellus (Chiroptera). Genetica, 66, 231-236.
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WAI-P1NG V. & FENTON M. B., I989. - Ecology of spotted bats: roosting and foraging behaviour. s Mammal., 70, 617-622. WATERS D. • JONES G,, 1995. - Echolocation call structure and intensity in five species of insectivorous bats. J. Exp. Biol., 198, 475-489. WHITE G. C. t~z GARROTT R. A., 1990. - Analysis of wildlife radio-tracking data. Academic Press, San Diego. ZErNDEN K. & ZINGG E E., 1986. - Search and hunting signals of echolocating European flee-tailed bats, Tadarida teniotis, in southern Switzerland. Mammalia, 50, 9-25. ZmGG E E., 1994. - Neue Vorkommen der Mopsfledermaus (Barbastella barbastellus Schreber, 1774) im Berner Oberland. Mitt. Naturwissenschaftl. Ges. Thun, 1994, 121-132.
Acre (Ecologica
Barbastelle bats (Barbastella spp.) specialize in the predation of moths: implications for foraging tactics and conservation Antoine Sierro (1) and Raphael Arlettaz (2, 3 , ) (2)
( x) Institute of Zoolog3, University of Neuchdtel, Switzerland. Institute of Zoology and Animal Ecology, University of Lausanne, Switzerland: (3) Present address and for correspondence: School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 lUG, UK. Phone~Fax: +44 117 927 69 94 E-mail: Raphael.A rlettaz@izea, uniL ch
Received: 7.11.95
Accepted: 21.I 1.96
Abstract The diet of barbastelle bats, Barbastella (b.) barbastellus and B. (b.) teucomelas, captured, respectively, in the Swiss Alps and in the Kirghiz Tien Shian and Pamir mountains (central Asia) was investigated through faecal analysis. Location of hunting habitats and data on foraging behaviour of Swiss barbastelle bats were obtained from radiotracking. In either area, ca. 99% of prey by volume consisted of Lepidoptera. The regular occurrence of one small arctiid species in the diet of Swiss barbastelles, as well as the predominance (84%) of tympanate moths among the Lepidoptera sampled at foraging sites suggest that B. barbastellus could prey to a large extent on smaller tympanate moths. Observations of foraging bats showed that, in the study area, barbastelles behaved as typical aerialhawking bat species, although they hunted exclusively just above the forest canopy. This aerial-hawking bat species has seemingly evolved a peculiar foraging technique to overcome the defence system of its probable tympanate prey. The diet of Barbastella appears one of the narrowest among Palaearctic bats. Such a specialization in foraging habits probably points to a higher vulnerability of this species, as compared to other more flexible aerial-hawking bats, to negative changes in the abundance of moth populations. This could explain its current rarity throughout most of Europe.
Keywords: Barbastella, Chiroptera, conservation, diet, echolocation, endangered species, evolutionary arms race, Lepidoptera, light trap, predator-prey relationship, trophic ecology.
R~sum~ Au moyen d'analyses f6cales, nous avons 6tudi6 le r6gime alimentaire des chauves-souris barbastelles, Barbastella (b.) barbasteUus et B. (b.) leucomelas, tant dans les Alpes valaisannes (Suisse) que dans les chaines des Tien Shian et Pamir Alaf (Kirghizstan, Asie Centrale). En Suisse, des donntes sur tes habitats de ehasse et le comportement de fourragement ont 6galement 6t6 obtenues par
* To whom reprint requests should be addressed.
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radiopistage. Dans les deux rtgions gtographiques, les 16pidopt~res constituaient environ 99 % du volume des proies consommtes. La prtsence rtguli~re d'une petite esp~ce d'Arctiidae dans les 6chantillons de crottes en provenance des Alpes, ainsi que la nette prtdominance (84 % en frtquence) des 16pidoptbres tympants dans les pitgeages lumineux effectuts au sein de la zone de chasse visitte p a r la population suivie par radiottltmttrie, sugg~rent que B. barbastellus est sptcialis6 dans la prtdation des petits 16pidopt~res nocturnes tympants. Les observations de radiopistage ont montr6 que les barbastelles se comportaient comme des chasseurs atriens typiques ; toutefois, elles concentraient leur effort de chasse dans une zone situte juste au-dessus de la canopte des boisements forestiers. Cette esp~ce a semble-t-il dtvelopp6 une strattgie de prtdation (syst~me sonar ?) tout-~-fait paxticuli~re pour dtjouer le systtme auditif de ses proies tympantes. La niche trophique de la barbastelle est l'une des plus 6troites et sptcialistes parmi les chauves-souris paltarctiques, ce qui sugg~re une vulntrabilit6 accrue de l'esp~ce, par rapport aux autres chauves-souris chassant 6galement des proies atriennes, tout changement ntgatif au sein des populations de 16pidopt~res nocturnes. Ceci expliquerait sa raret6 actuelle dans la majeure partie de l'Europe.
INTRODUCTION The barbastelle bat, Barbastella barbastellus, is currently considered as one of the most endangered bat species in western Europe (STEBBINCS & GRIFFrrrt, 1986; STEBBINOS, 1988). Over the past decades, severe population declines or even local extinctions have been reported by many bat workers, and the range of this species seems now very patchy, apparently mostly restricted to upland areas (e.g. R]CnARZ, 1989; BENZALetal. 1991; Zn~oc, 1994). On Col de Bretolet, at the French-Swiss border, for instance, B. barbastellus was the second most abundant bat species mistnetted by ornithologists in the late '50s and early '60s, but the frequency of capture of this species has dropped dramatically since then (fig. 1). In contrast with western
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FIG. 1. - Relative number of barbastelle bats (B. barbastellus in percent of all bat captures) mist-netted by ornithologists on Col de Bretolet (Valais, Switzerland, and Haute-Savoie, France) over 23 years (19581994; years with no netting activity or totalling < 30 bat captures have been excluded). Data presented here include 162 captures of 13. barbastellus for a total of 1676 bats caught. Source: database of the "Rdseau Chauves-souris Valais" (R. ARLETTAZ,A. LUC,ON & A. SXERRO,unpublished).
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Barbastelle bats prey on moths
Europe, there are still sizeable wintering colonies in central eastern Europe (URBANCZYK, 1991; UHR~q, 1994-95), suggesting that this species is less threatened or vulnerable there. Similarly, the eastem Asian form leucomelas, which is either considered a distinct valid species (CORBET, 1978; NOWAK, 1991; FROST & TtMM, 1992) or simply a subspecies of B. barbastellus (QuMslWIa, 1985), does not seem to be in such a critical situation (e.g. RYBINet al., 1989). The reasons for the decline of western European barbastelles have not been identified (SVEBBrNGS& GRIFFrrH, 1986). Indeed, only data on the diet of B. barbastellus are currently available (BECK, 1994-95; RYDELL et al., 1996); this situation impedes proposing any concrete conservation measures. Specialized predators relying on few prey types are generally more vulnerable than generalist, more flexible predators. The present study aims at testing the hypothesis that highly specialized foraging habits could account for the drastic decline recently faced by western barbastelle bats. We thus compare the diets of barbastelles occurring both in the western Palaearctic (form barbastellus) and in the eastern Palaearctic region (form leucomelas), and discuss dietary niches in the context of prey abundance (estimated by light-trapping), foraging tactics (as revealed by radiotracking and visual observation), and trophic specialization, drawing possible implications for the species conservation. METHODS
AND STUDY AREA
Droppings were collected from individuals mist-netted by the authors at underground entrances both in the Swiss Alps (Mont Chemin, Valais; n = 33) and in the Tien Shian and Pamir mountains of central Asia (Kirghizstan; n = 16); some additional captures were made by ornithologists in late summer and autumn on Col de Bretolet (Valais, Switzerland; n = 4) (table I). Bats were held in linen bags and faeces collected before releasing them at night.
TABLEI . - Localities where faecal samples of barbastelle bats have been collected: country, region (canton
for Switzerland; district for Kirghizstan), locality, coordinates, altitude, date of collection, number of bats that yielded faeces. Country Switzerland
Region Valais Valais
Kirghizstan
Kocbkorskyi Jetiogjuzskyi Aravanskyi Nookatskyi Nookatskyi Batkensykyi
Total
Vol. 18, n ~ 2 - 1997
Locality
Coordinates
Altitude
Date
n bats
1200 m
22 11 4
Mont Chemin (mine) Bretolet pass
46~
7~
46~
6~
1920 m
8.5.92-8.10.92 19.6.93-30.8.93 27.8.92-7.9.92
Cholpon (salt mine) Chong Jargylchak Dangi Tuja Mujun Aktala Ak Dzhilga Kanigut mine (Gherm)
42~176
2100 m
24.8.92
2
42~176 40~176 40~176 39~176 39~176
1950 m ll00m 1800m 2200 m 1570 m
1.9.92 16.9.92 24.9.92 25.9.92 30.9.92 2.10.92
1 1 2 5 5 53
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In the laboratory, faecal material was dissected under a binocular microscope (magnification up to 60x) and prey remains were identified referring to identification guides (e.g. MCANEYet aL, 1991), to the collection of the Museum of Natural History of Sion, and to insects gathered at the study site. For each dropping, the percentage of volume occupied by a given prey category was estimated to the nearest 5-10%. An overall percentage was then calculated for each individual sample, one sample consisting of all droppings collected from one individual (ARLEa~rAZ, 1995). The reliability of faecal analyses to quantify the composition of bat diets has been demonstrated several times: e.g. KtJNZ & WHITAKER(1983) and DICKMANN8Z HUANG(1988). At Mont Chemin, Switzerland, seasonal variation in food abundance was estimated by lighttrapping insects within the main foraging area of a small population of B. barbastellus whose home range was delimited by radiotracking (see below). Light-traps are generally considered as a relatively good tool to estimate the abundance of aerial, nocturnal insects (MUIRHEAD-THOMSON,1991), although serious biases are to be expected, particularly with insect species which do not present a positive phototactism (Kuyz, 1988). Insect trapping sessions were performed between April and October 1992 during seven nights (one night per month). Trapping was deliberately restricted to calm and dry nights with reduced or no moon light, i.e. on nights offering the most favorable sampling conditions. Insects were identified to the order or family level, except for Lepidoptera where determination to the species level was often possible. Identification guides (e.g. CHINERY, 1988) as well as the collections of the Museum of Natural History of Sion served as a reference basis. As regards moth systematics, we refen'ed to LERAUT(1980). Radiotracking sessions took place at Mont Chemin (Valais, Swiss Alps) from June through to October 1992, with complements in June 1993. Bats were mist-netted at the entrance of two abandoned mine gaieties, and fitted with small glue-on (cyanocrylate glue) radiotransmitters (BD2B; 0.65-0.68 g, Holohil Systems Ltd, Ontario, Canada). Because of strong topographic constraints, the standard tag was modified by the producer so as to maximize detection range (ca. 1.5 kin); this resulted in a reduced battery lifespan. A piece of reflector tape (ScotchliteTM) fixed on the upper side of the tag enabled location and identification of the tracked individual in the field through direct visual observation with the help of a night scope (Big III, Wild-Leitz, Leica SA, CH-1020 Renens, Switzerland) coupled with an infrared halogen lamp. Twelve radiotracking sessions were performed on 11 individuals (8 males and 3 females). Bright 8 • 56 binoculars (Habicht TM) were used in the twilight to watch the foraging behaviour of freshly emerged bats. An ultrasound detector (Mini bat II, Summit, Birmingham, B18 5NY, UK) was used to assess the identity of untagged individuals according to AHL~N (1990). This author states that ((using a good quality detector, the experienced observer can't miss this species>>. Bats were tracked on foot from dusk to dawn by one single observer equipped with a radio-receiver (Wagener, Herwarthstrasse 22, D-50000 K61n, Germany) and a H-antenna. Locations were obtained using the ((homing-in on the animab> method (WHITE & GARROTr, 1990). Field observations were recorded on a walkman tape-recorder. The habitat surrounding the Swiss mine (Mont Chemin), where most faeces were gathered and where radiotracking sessions took place, consists mostly of a mixture of xeric pine (Pinus sylvestris), oak (Quercus pubescens) and spruce (Picea abies) lbrests growing on stony outcrops and steep slopes; however, patches of traditional meadowland and a small village are also present on a nearby plateau. The typical vegetation around the alpine pass is characteristic of the upper edge of the subalpine forest, with Picea abies and Alnus viridis as dominant tree species. By contrast, the environment around sampled Kirghiz localities consisted mainly of xeric habitats including steppe and subdesert areas, and forests were totally absent.
Acta (Ecologica
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Barbastelle bats prey on moths
RESULTS
Diet composition A total of 53 (n = 37 for Switzerland, n = 16 for Kirghizstan) individual faecal samples comprising 246 droppings was analysed; one individual faecal sample thus consisted, on average, of 4.6 faeces. Only four insect orders were identified in faeces: Lepidoptera, Neuroptera, Trichoptera and Diptera; moreover, the last two categories appeared only in the Swiss material. In both study areas, and during all months, the diet consisted almost entirely of Lepidoptera (fig. 2); overall monthly means were
[]
Lepidoptera
[]
Neuroptera
[ ] Trichoptera
9
Diptera
I
Switzerland
10080-
6040A
20-
E "= 0O > Kirghizstan co 100-
4=,1
m.
8060-
4020. May
June
July
Aug
Sept
Oct
Month FIG. 2 . - Seasonal diet composition (percent volume) of individual Barbastella captured in Switzerland and Kirghizstan (for more details about locations, see table I). Sample size is given at column foot.
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98.9% and 99.4% by volume in Switzerland and Kirghizstan, respectively. As is the rule with Lepidoptera fragments in bat droppings (MeANEr et al., 1991; SHmL et aL, 1991; RVDELL& ARLEa'a'AZ,1994), it was not possible to establish which families were present; however, fragments were typical of moths (antennae; uncoloured scales except in July and August, see below; densely haired legs) and there was no evidence of the presence of diurnal Lepidoptera in the faeces. This observation is further supported by the predominance of bright yellow scales in the faeces of the Swiss barbastelles in July and August. As revealed by the insect trapping, the only Lepidoptera species in that area exhibiting such a bright colour is Eilema complana, a small arctiid of the subfamily Lithosiinae, which appeared abundantly in July and August in the light trap. Neuroptera (Hemerobiidae) fragments represented, overall, only 0.4% and 0.6% of Swiss and Kirghiz faecal samples, respectively. Among the 37 Swiss faecal sampies, minor portions of Hemerobiidae were present in only two samples from July (10 and 5% of the sample volume, respectively). Similarly, only two of the 16 Kirghiz samples comprised this prey category (5% each). Trichoptera and Diptera (Cecidomyiidae) were each recorded in only one Swiss sample. Only two leg fragments of moths provided information about the size of the eaten prey, by comparison with items of the reference collection; they both indicated a wingspan of ca. 25-30 nun. According to the moth species caught at the foraging site, this roughly corresponds to the body size of a small-sized moth, e.g. of the family Pyralidae.
Prey abundance at foraging grounds As revealed by light trapping, insect abundance within the main foraging area of the population of B. barbastellus at Mont Chemin (Switzerland) showed a large predominance of Diptera and Lepidoptera throughout the season (fig. 3). These two insect categories represented, respectively, as much as 52% and 36% of the total number of items recorded (n = 7404). However, ca. 90% of the Diptera items were very small (< 8 mm body length); only Limonidae and Tipulidae exhibited larger body sizes. Nocturnal Lepidoptera were by far the most abundant medium- and large-sized insect prey found in the trap. Among the moths, small specimens (wingspan < ca. 30 mm) were more abundant (69%) than larger ones (> ca. 30 mm wingspan; 31%) (table II and fig. 4). According to the species collected at the site, the small size class comprises all the families of the suborder Microlepidoptera but also some Macrolepidoptera, the Nolidae and the Lithosiinae (Arctiidae). Accordingly, the second class corresponds to the suborder Macrolepidoptera, minus the two above mentioned groups. Pyralidae were by far the most abundant Lepidoptera family (44%), followed by Geometridae and Noctuidae (14% and 16%, respectively). Moth families for which the existence of auditory organs - hereafter called "tympanate" although Sphingidae have palpal hearing organs (SCO~LE, 1992) - has been evidenced largely predominated from spring to autumn (table II, fig, 4); their overall proportion was as high as 84% of the total moth population (table II and fig. 4). Three taxa were particularly abundant, totalling 44.4% of trapped moths: Catoptria permutatella, Scoparia sp. (both Pyralidae) and the yellowcoloured Eilema complana (Arctiidae: Lithosiinae). Ac~(Eco~gwa
97
Barbastelle bats prey on moths
1500
1000
,,Q
500
~
r~A l'/~'rnetT~ C~
-'4Pr/7
a
/z Neuroptera /~at~ a , ,HOmo#tera Netero#tera TrichoPtera
Seasonal abundance (number of items) Of the main insect categories light-trapped within the foraging area of a small population of Barbasteila barbastellus in the Swiss Alps (Mont Chemin, V a l a i s ) .
FIG. 3. -
Hunting grounds and foraging behaviour The eleven radiotracked individuals carried transmitters for a total of 29 days. Because of complex topography, adverse weather conditions and, possibly, transmitter defect, only 8 :individuals provided information on foraging areas over 19 nights (average: 2.1 nights per successful radiotracking trial); one individual was radiotracked during two successive field seasons (table III). All the bats foraged on a steep slope covered by xeric forest vegetation, consisting mainly of Pinus sylvestris, between 900 and 1200 m altitude; human settlements and open habitats such as meadVol: 18, n ~ 2 -
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A. Sierro and R. Arlettaz
TABLE II. -- The different families and subfamilies of nocturnal Lepidoptera collected with light trap in the foraging area o f B. barbastellus at Mont Chemin (Valais, Switzerland) with respect to occurrence frequency (absolute and percentage; n total = 2658 items), to body size (L = large tara, i.e. wingspan > - 3 0 mm; s = small tara, i.e. wingspan < - 3 0 ram) and to the presence~absence of auditory organs according to literature (e.g. SCOeLe, 1992) (symbol "-"." no evidence of auditory organs).
Taxa Microlepidoptera Limacodidae Ethmidae
Gelechiidae Yponomeutidae Tortricidae Pyralidae Pterophoridae Macrolepidoptera Lasiocampidae Thyatiridae Geometlidae Sphingidae Notodontidae Lymantriidae Arctiidae Lithosiinae Arctiinae Callimorphinae Nolidae Noctuidae
n
1 1 120 8 223 1180 2 17 1 373 10 6 12 267
%
Body size
4.5 8.4 44.4
14
tympana
L L L L L L
10.1
s L L 16 421
Hearing organ
tympana
tympana palpal hearing system tympana tympana tympana tympana tympana
tympana
s 15.8
L
tympana
owland were avoided. The area of the minimum convex polygon drawn from the most external radio-locations of the radio-tagged population amounted to 56 ha, whereas the mean estimated individual home range was 8.8 ha (SD = 5.8 ha; n = 8). Given that bats were usually loyal to their feeding zones over successive nights, this high variance merely reflected the great seasonal and interindividual variation in the area prospected by individual bats. Some individual feeding grounds overlapped, but we could not assess the simultaneous presence of two or more foraging bats at the same hunting territory. Daily roosts consisted of rocky crevices situated in cliff walls located within the foraging area of the radio-tracked population. We succeeded to observe visually (with the night scope) radio-tagged barbastelle bats while foraging during only two short periods of less than two minutes each on only two nights, at a distance of 10-40 m. The main reason for the lack of direct observation of foraging bats carrying radiotransmitters was mostly the difficult local topography. Fortunately, additional observations with binoculars could be made at more accessible places in the same site on eight further occasions (totalling more than 25 minutes of direct visual contact), while untagged individuals were performing their first foraging bouts at dusk. Then, bat identification was achieved in the field by using an heterodyne bat detector tuned at 30-35 KHz, according to the criteria outlined by Ar~LEN (1981, 1990; see Methods). All foraging barbastelle bats we could watch were Acta (Ecologica
Barhastelle bats prey on moths
99
600
400
_~
" 200
fo,~//fOo
v ~- f ~ o ~ , 9~
J'e.,~ r
o cl
[ ] moths with auditory organs
z,9~
""
"~
~4'<.oe .,-Ooz,/_/~"
[ ] moths with no evidence of auditory organs
Seasonal comparison of the abundance (number of items) of small vs. large and tympanate vs. nontympanate moths within a foraging zone used by foraging barbastelle bats in the Swiss Alps (Mont Chemin, Valais).
FIG. 4 . -
flying just above the forest canopy, ca. 2-4 m above tree crowns. The flight was fairly adroit, and speed appeared slow to moderate. We could not observe barbastelle bats gleaning prey directly from the uppermost tree branches. DISCUSSION
Trophic niche Consisting almost exclusively of moths, the diet of Barbastella appears to be the narrowest yet found for Palaearctic bat species. This high diet specialization was Vol. 18, n ~ 2 - 1997
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A. Sierro and R. Arlettaz
TABLEIII. -- Summary of the 12 radiotracking trials carried out in 1992-93 on 11 individual barbastelle bats
at Mont Chemin (Valais, Switzerland); from left to right: individual (ring number), sex, age, period with recorded signal emission, and number of nights with monitored foraging activity. Individual
Sex
Age
Period
N 134 N 141 K 724
male male male
adult subadult adult
M 139 N 143 N 144 K 592 N 145 N 133 N 148 N 201
male male female male female male female male
adult adult subadult adult subadult adult adult adult
16-17.06.92 22-23.06.92 03.07.92 08.06.93 31.07-05.08.92 04.08.92 11-13.08.92 10-13.08.92 06.09.92 14-16.09.92 08-09.10.92 27-30.06.93
Total
Number of nights with foraging activity recorded 1 1 0 0 4 0 2 3 1 3 2 2 19
already pointed out by BECK (1994-95) and RVDELLet al. (1996). However, the proportion of moths is even greater in our study than in the latter two. To some extent, this may reflect differences in sampling procedures. First, contrary to BECK(1994-95) and RVOELLet al. (1996), who analysed droppings gathered from underneath roosts, we collected faecal samples directly from mist-netted individuals. Given that variation of bat diet composition is chiefly due to inter-individual variation rather than to within individual variation (e.g. ARLE~AZ, 1995; p. 105), that discrepancy may be merely methodological. It cannot be excluded, however, that the guano investigated by BECI~ (1994-95) and RYDELLet al. (1996) had been contaminated by other bat species which could roost together with barbastelles from time to time; a guano contamination might also explain the presence of scarce debris of non-flying prey (e.g. Araneae) in the latter study. Since faecal samples in the present study were collected from quite different mountainous environments in the Swiss Alps (forest) and in the Kirghiz Tien Shian and Pamir Alai ranges of central Asia (steppe), the trophic specialization of barbastelle bats clearly does not stem from the use of similar habitat types in both areas, and therefore points to a highly species-specific diet selectivity and/or foraging constraint in Barbastella. Because of their slender skull morphology, as compared to other vespertilionid bats of similar body size (ScHOBER& GRt~ERGER, 1987), barbastelle bats are probably not able to capture larger insects (FREEMAN,1981) and should feed on more abundant, smaller moth prey items (e.g. Tortricidae, Pyralidae or Lithosiinae), most of which are tympanate (table !I). Although direct evidence about prey body size refers to only two leg fragments in this study, this view is also supported by the regular occurrence of scales of the small yellow-coloured arctiid moth species Eilema complana (ca. 30 mm wingspan; Lithosiinae, table II) in the faeces of Swiss barbastelles in July and August. Acta GEcologica
Barbastelle bats prey on moths
101
Among the other European bat species, only Tadarida teniotis (RYDELL8Z ARLETTAZ, 1994) and Plecotus austriacus (BECK, 1994-95) seem to feed, but to a lesser extent than Barbastella, on moths (< 90% by volume and frequency, respectively). Two North American bat species have also been reported to include mostly moths in their diets: Euderma maculatum and Plecotus townsendii (WAI-PING 8Z FENTON, 1989; SAMPLE(~ WHITMORE,'1993). Tadarida is a molossid bat, whereas Plecotus and Euderma are representatives of the long-eared bats of the tribe Plecotini (Vespertilionidae), which also includes the genus Barbastetla (see below). A singular foraging tactics?
As far as we know, bats seem to have evolved three different foraging strategies to overcome the defence mechanisms evolved by insects that possess auditory organs. Aerial-hawking bats may first emit very low intensity calls which are particularly undetectable to prey or, second, they may glean prey from substrates relying on passive acoustical cues (e.g. sounds generated by moving targets) instead of on echolocation. In the Holarctic zone, these two strategies seem widespread among the vespertilionids belonging to the genus Myotis and to the tribe of plecotine bats (Plecotus, Euderma, etc.; FAURE et al., 1990; ANDERSON& RACEY, 1991; FAURE & BARCLAY, 1994). Thirdly, bats may also use frequencies below or above the range of best auditory sensitivity of prey (the "allotonic frequency" hypothesis; NovIcK, 1977; FENTON & FLrLLARD,1979; FULLARD,1987; JONES, 1992). Of the three above-mentioned moth predators, Plecotus auritus and P. townsendii behave mostly like typical passive listeners while gleaning (e.g. ANDERSON& RACEr, 1991; SAMPLE & WH~TMORE, 1993), whereas Tadarida teniotis and Euderma maculatum are exclusive aerial foragers which both use very low frequency calls (ca. 1012 kHz) that are clearly audible to the human ear (LEONARD& FENTON, 1984; ZBINDEN & ZINGG' 1986). The available data on the echolocation of barbastelle bats denote a very singular detection system in these bats, probably unique among the Holarctic bat species. Firstly, JONES (1993) suspected very unusual sonograms, shaped like an inverted "J" in this species, a "convex" call design not reported for other European vespertilionid bat species which all exhibit "concave" calls. Secondly, field ultrasound recordings suggest that foraging Barbastella typically emit two different types of calls, either loud or weak pulses, at ca. 32 kHz and 42 kHz, respectively (AHLEN, 1981) 1. If barbastelle bats are actually preying mostly on tympanate moths, we may speculate that low frequency, high-intensity pulses could be used during the detection phase, whereas the low-intensity calls - particularly unconspicuous to tympanate prey could be restricted to the approach and capture phase; this could also explain why free-ranging foraging barbastelle bats typically emit either pure sequences of low frequency calls or alternate the two types of calls (AHLEN, 1981; P. ZINGG, in litt.). However, it cannot a priori be excluded that barbastelle bats might perhaps simply rely on a "passive-listening" strategy instead of echolocation, at least during the last phase of prey capture. Our visual observations of foraging B. barbastellus confirm that this species is primarily an aerial-hawking forager adept at foraging close to clutter since our bats 1. K. G. I-IELLERand E ZrNGO(unpublisheddata) havefoundsimilarcall patterns(pers. comm.). Vol. 18, n~2 - 1997
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were hunting just above the forest canopy (AHLI~N, 1990; NORBERG& RAYNER, 1987). In the present study, bats did apparently not glean prey from surfaces; indeed, there is no evidence as yet that barbastelle bats occasionally glean prey from substrates, as suggested by RYDELLet al. (1996). Besides, the arthropods which are captured by typical substrate-gleaning bat species (e.g. BECK, 1994-95) miss totally in barbastelle's diet. Unfortunately, we could not see the patrolling barbastelles "pausing, and rising a little with near-hovering flight" as described by AHLI~N(1990). Interestingly, these observations would be consistent with the hypothesis that Barbastella might actually rely on passive acoustic cues (the noise produced by fluttering moths?) to capture its flying prey. Additionally, KONSTANTINOV& MAKAROV(1981) have suggested that its unusual ear morphology provides Barbastella with a strongly enhanced hearing directionality, a character usually shared by passive listening bats (OBRISTet al., 1993).
Evolutionary context According to VOLLETH(1985) and FROST& T~M (1992), the short ears - at least relatively to other plecotine bats - of Barbastella are probably a synapomorphy of this genus, i.e. barbastelle bats have probably evolved reduced ear size from a Plecotuslike ancestor. Barbastelle bats may therefore have retained some basic features of the hunting behaviour of their ancestors as well (see COLES et al., 1989), although they have presumably switched to an aerial-foraging strategy. The use of low intensity calls or even of passive listening, both typical of most plecotine bats (ANoERSON& RACEr, 1991; WATERS& JONES, 1995), as well as the ability to perform flight pauses accompanied by almost hovering sequences (AnL~N, 1990), could be part of this legacy.
Prey selection and community organization Contrary to most European aerial-hawking vespertilionid bat species that are flexible predators including different insect categories in their diets (see the review by RYDELL et al., 1995), Barbastella is apparently very restricted in its food choice. A narrow diet usually reflects a trophic specialization. Moreover, RYDELLet al. (1995) have proposed that a bat subsistence based primarily on nocturnal moths should require a highly specialized predator because most of these prey exhibit auditory organs tuned to the main frequencies used by aerial-hawking bats. In Barbastella, however, such a specialization would not necessarily result from active prey selection. Indeed, passive selection sensu FAURE & BARCLAY (1992) may also be possible because: 1) moths appeared particularly abundant at the Swiss feeding habitats; 2) the singular morphology and echolocation system of Barbastella may imply particular foraging constraints. This view is furthermore consistent with the current opinion that active prey selection has so far not been conclusively established among insectivorous vespertilionid bats (e.g. ARLETTAZ& PERPaN, 1995). However, in the case of Barbastella, the question remains why these bats do not catch other types of prey which also occur at their feeding places, e.g. Hymenoptera, Coleoptera or large-sized Diptera (this study). It is hard to imagine that drastic design constraints could enable Barbastella to catch moths but not other flying prey of similar body size, unless 1) barbastelle bats use passive listening for prey capture and 2) moths are more noisy on the wing, other things being equal, than other flying insects, i.e. more conspicuous for a passive-listening predator. Competition with coexisting Acta CEcologica
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insectivorous bat species within the s a m e c o m m u n i t y could, o f course, force Barbastella to feed exclusively on moths. Their suspected r e m a r k a b l e capability to catch flying t y m p a n a t e moths, either through echolocation or passive listening, might be so advantageous, however, that the capture o f other prey types c o u l d eventually be neglected. I m p l i c a t i o n s for c o n s e r v a t i o n
On the other hand, a p r o b a b l e disadvantage o f the singular niche o f Barbastella is that this species c o u l d o n l y survive in areas which yield sufficient populations o f moths. This suggests a high vulnerability o f barbastelle bats to negative changes in the density o f their prey. T h e progressive destruction o f cultivated landscapes in western Europe, including the intensification o f farming practices and the use o f pesticides against m a n y m o t h species w h i c h are a m o n g the most detrimental pests in agriculture (e.g. Pyralidae, Tortricidae, Noctuidae), have r e d u c e d moth populations (HEvt)EMANN, 1980; BLAB & KUDRNA, 1982; SCHWARZ, 1983; GEIGER, 1987; CHARMILLOT et al., 1994). This m a y have affected Barbastella's s u r v i v a l and reproduction, either directly through the loss o f suitable foraging habitats and/or indirectly through poisoning. The g l o b a l impact o f street l a m p s on m o t h populations m a y also be questioned. If street l a m p s can locally provide advantages to individual foraging bats (e.g. RYDELL, 1991, 1992), severe crashes in moth populations have been reported within intensely illuminated areas (GEPP, 1981; GEIGER, 1987). The recent p h e n o m e n a l extension o f street lamps might thus have p l a y e d some role in the decrease o f barbastelle bats in western Europe. Are these the reasons why relict populations o f barbastelle bats subsist apparently n o w a d a y s m o s t l y in s o m e eastern E u r o p e a n countries and in remote, better preserved m o u n t a i n o u s areas o f western Europe?
ACKNOWLEDGMENTS We acknowledge Prof. W. MATTrmY,Prof. C. MERMODand J. M. WEBERwho supervised this study. We thank P. MOSnVtANNand E "rta~aAN who collected faeces on Col de Bretolet, as well as G. DANOLIr,,ER, E. KASWEKOV,J. M. PtLLET, S. RYBn~ and J. Z~A who took part in the trip to Kirghizstan. A. Coa'rv, J. C. ROBERT,N. VONROTENand C. StE~Er,~rnALERgave advice on the methods of insect trapping and identification. J. M. DAYER,C. LANDRYand J. C. PRAZand SmRRO'Sfamily provided technical assistance. D. CnEPaXand K. G, HELLERprovided literature on moths and streetlamps. Our best thanks also to K. G. HALER,G. JONES, P. RACEV,J. RVDELL,D. WATERSand P. ZIN~Gfor their thorough appraisal of the manuscript. Captures in the Swiss Alps were undertaken under licence from the Nature Conservancy Service of State Valais. AS was supported financially by the Rrseau Chauves-sourisValais and Fondation Mariftan; RA's expedition to Kirghizstan was funded by the Socirt6 Acadrmique Vaudoise, Fondation Marirtan, Basler Stiftung for zoologische Forschung, Acadrmie Suisse des Sciences Naturelles, Fondation Georgine Claraz, Fondation du 450e anniversairede l'Universit6 de Lausanne and Musre zoologique de Lausanne.
REFERENCES
AHLI~NI., 1981. -- Identification of Scandinavian bats by their sounds. The Swedish University of Agricultural Sciences, Department of Wildlife Ecology, Uppsala, Sweden. Report No. 6, 56 p. AHLENI., 1990. -- Identification of bats in flight. Swedish Society for Conservation of Nature and the Swedish Youth Association for Environmental Studies and Conservation, Stockholm, 53 p. Vol. 18, n~
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Acre (Ecologica