Eur J Wildl Res
DOI 10.1007/s10344-014-0862-8
ORIGINAL PAPER
Living above the treeline: roosting ecology of the alpine bat
Plecotus macrobullaris
Antton Alberdi & Joxerra Aihartza & Ostaizka Aizpurua &
Egoitz Salsamendi & R. Mark Brigham & Inazio Garin
Received: 11 June 2014 / Revised: 12 September 2014 / Accepted: 22 September 2014
# Springer-Verlag Berlin Heidelberg 2014
Abstract Little is known about the alpine bat community, but
recent studies suggest that the alpine long-eared bat, Plecotus
macrobullaris, commonly forages in alpine habitats, although
most of its known roosting records are from locations situated
below the treeline. Aiming to contribute to resolving this
seemingly contradictory pattern of ecological preferences of
P. macrobullaris, we carried out a radio-tracking study to (1)
identify its roosts and unveil its roosting habitat preferences,
(2) determine whether bats found foraging in alpine habitats
do actually roost and breed in such high-mountain environments, and (3) test if any elevation-related sexual segregation
occurs. We captured 117 alpine long-eared bats and radiotracked 37 individuals to 54 roosts located at elevations between 1,450 and 2,430 m, 46 of them above the treeline. Bats
used rock crevices (30 roosts), scree deposits (21) and buildings (3) for roosting, and most lactating and pregnant females
relied on crevices. Bats selected areas with high meadow
availability near the roost, while avoiding densely forested
areas. Foraging areas and roosting sites were located at the
same elevation, indicating that alpine long-eared bats use
alpine areas for both roosting and foraging in the Pyrenees.
Breeding females roosted at lower elevations than nulliparous
females and males, though they remained above the treeline.
Although being considerably different to the ecological preferences described so far in the Alps, the roosting behaviour we
observed was consistent with some ecological traits, namely
Communicated by C. Gortázar
A. Alberdi (*) : J. Aihartza : O. Aizpurua : E. Salsamendi : I. Garin
Department of Zoology and Animal Cell Biology, Faculty of Science
and Technology, University of The Basque Country UPV/EHU,
Leioa, The Basque Country, Spain
e-mail: [email protected]
R. M. Brigham
Department of Biology, University of Regina, Regina, Canada
foraging and trophic behaviour, of P. macrobullaris, as well as
its distribution pattern linked to mountain regions.
Keywords Alpine long-eared bat . Mountain long-eared bat .
Pyrenees . Radio-tracking . Sexual segregation . Scree
deposits . Thermoregulation
Introduction
The diversity and activity of chiropterans in alpine environments may have been underestimated thus far (Alberdi et al.
2013). Elevation-gradient diversity and abundance studies
have shown that chiropteran diversity and activity decreases
above mid-elevations (Holzhaider and Zahn 2001), which
may have led many elevation-related diversity studies to overlook the alpine belt (Holzhaider and Zahn 2001; Pavlinic and
Tvrtkovic 2004). However, some recent studies have shown
that bats do exploit alpine environments (Barataud 2005;
Alberdi et al. 2013). Although more than a dozen species have
been captured or detected above the treeline in Europe (Aellen
1962; Barataud 2005; Alberdi et al. 2013), there are few
known roosting records. The particular physiological requirements of bats most likely hamper them from roosting at high
elevation. For instance, pregnant and lactating females cannot
take advantage of deep torpor, presumably in order to speed
foetal and neonatal development (Dzal and Brigham 2012). It
appears that the majority of bats found in alpine environments
are primarily lowland species that occasionally commute to
higher elevations when conditions become favourable
(Michaelsen 2010) or use alpine environments as commuting
routes (Aellen 1962; Alberdi et al. 2012a). Nevertheless,
detailed information about the spatial and temporal dynamics
of bats in alpine habitats is still largely unknown.
The alpine long-eared bat, Plecotus macrobullaris
(Kuzjakin, 1965), stands out among the bat species reported
Eur J Wildl Res
in European alpine environments. More than two thirds of the
bats captured in European supraforestal habitats by Alberdi
et al. (2013) were P. macrobullaris. The study did not identify
the pattern of elevation-related sexual segregation reported for
many other species (Cryan et al. 2000; Russo 2002), and
instead, breeding females were captured up to 1,000 m above
the treeline (Garin et al. 2003). Additionally, molecular analysis of diet showed that P. macrobullaris forage in alpine
habitats rather than only using them for commuting (Alberdi
et al. 2012b). However, depending on the geographic area, the
elevation range of P. macrobullaris spans from sea level up to
2,800 m (Alberdi et al. 2013), and this species has been found
in habitats other than alpine grounds. Two studies carried out
in Switzerland identified a preference towards deciduous forest environments (Rutishauser et al. 2012; Ashrafi et al. 2013),
while a population studied in Italy was shown to avoid woodlands (Preatoni et al. 2011). The species has also been captured in semi-arid steppes and other scarcely vegetated areas
(Shehab et al. 2007; Benda et al. 2008).
Similarly, current understanding of the roosting ecology of
P. macrobullaris is still inconclusive. Most known roosting
locations are from the Alps, where the species is commonly
found in buildings below the treeline (Presetnik et al. 2009;
Mattei-Roesli 2010; Rutishauser et al. 2012), corresponding to
the reported use of woodlands as foraging grounds in these
areas. However, the species has also been captured in the
alpine belt of several mountain ranges in Europe, far from
woodlands and where buildings are very scarce (Alberdi et al.
2013). These observations suggest that P. macrobullaris
may use other types of roosting resources, similar to those
used by other alpine vertebrates. Several alpine birds rely
on boulders, crevices and ledges for nesting, and a small
number also take advantage of caves (Cramp et al. 1994).
Small terrestrial mammals usually shelter in rock or stone
stacks such as scree deposits (Luque-Larena et al. 2002),
whereas large mammals tend to shelter close to steep cliffs
(Villaret et al. 1997). Roosting at high elevations would
allow bats to be closer to their foraging grounds, but lower
temperatures may limit breeding females, which are
prevented from entering into deep and long torpor when
gestating or nursing their pups (Dzal and Brigham 2012).
Conversely, roosting at lower elevations would probably
offer females better climatic conditions, but they would
have to fly greater distances when commuting between
roosting and foraging sites.
Finally, an important factor that must be taken into account
is the substantially lower detectability of bats that roost in
natural rock crevices compared to animals sheltering in caves,
and even more so in buildings, which are commonly examined for research and conservation purposes. In fact, most
P. macrobullaris colonies sheltering in buildings have been
discovered as a result of extensive building monitoring
programmes (Mattei-Roesli 2010), which may have led to a
biased view of the actual roosting preferences of the species.
No study to date has focused on the roosting ecology of
P. macrobullaris, and therefore the relative frequency of different roost types remains unknown.
In order to elucidate the roosting ecology of alpine
P. macrobullaris during the breeding season, we identified
the roosting locations and determined the types of roosts used
by individual alpine long-eared bats using radio-tracking. We
tested whether (1) bats select any specific habitat for setting
their roosts, (2) if elevation differences exist between foraging
and roosting sites and (3) if any elevation-related sexual
segregation occurs in their roosting behaviour. This information will allow us to assess whether Pyrenean P. macrobullaris
exhibit a mid-elevation anthropophilic roosting pattern similar
to that depicted in the Alps, or conversely, if they behave in a
similar manner to alpine species that both forage and roost in
the alpine belt.
Methods
Fieldwork
This study was performed in July and August 2012, in eight
valleys scattered throughout the Pyrenees (Fig. 1). The Pyrenees mountain chain separates the Iberian Peninsula from
continental Europe with elevations ranging from 500 to
3,400 m amsl. Nets were set following the technique of
Alberdi et al. (2013) in 18 sparsely vegetated meadow locations with elevations ranging from 1,550 to 2,370 m, the range
at which 95 % of known records in the Pyrenees are found
(Alberdi et al. 2013).
Captured bats were identified in the field using morphological characteristics (Dietz and Helversen 2004). Bats
were sexed and aged by visual inspection, with lactating
females identified by the production of milk after gentle
pressure on the mammary glands. Bats weighing 8–12 g
were fitted with 0.35 g radio transmitters (PipII, Biotrack
Ltd., Dorset, UK) and released at the site of capture within
20 min of being caught. We tracked the tagged bats to
diurnal roosts for 8 days, except on the first day after
tagging, as often as accessibility made it feasible. Based
on the species’ reported foraging range (Arthur and
Lemaire 2009; Preatoni et al. 2011), a radius of at least
10 km from each capture location was surveyed, mainly on
foot in areas far from roads or vehicle tracks. We searched
for signals from bats in roosts at elevations ranging from
1,200 to 2,950 m, covering the montane (dense deciduous
and/or coniferous forest), subalpine (sparse trees) and alpine (meadows and sparsely vegetated areas) belts. Exact
roost locations were recorded using GPS devices (Oregon
550, Garmin, Kansas, USA).
Eur J Wildl Res
Fig. 1 Geographic location of the eight valleys where P. macrobullaris individuals were captured and tracked in the Pyrenees
Data analysis
Radio-tracked bats were grouped into three classes based on
sex and reproductive condition: breeding (lactating and pregnant) females, nulliparous females and males. Roost types
were classified into four categories: crevices, caves, scree
deposits and buildings. Rock fractures or fissures up to
20 cm wide, regardless of whether they occurred in large cliffs
or boulders, were classified as crevices. We defined scree
deposits as accumulations of rock fragments at the base of
cliffs, composed mainly of rocks about 10–80 cm in diameter.
Roosts in fissures of boulders within scree deposits were
considered as crevices. We characterised each roost using
the following variables: elevation, distance to the capture site
(capture distance) and elevation difference relative to the
treeline in each area (treeline difference). We tested whether
data were normally distributed with the Shapiro-Wilk test and
determined homogeneity of variances using Levene’s test.
Parameters that fulfilled both assumptions were analysed
using one-way ANOVA (α=0.05), and the Tukey method
was used for post hoc multiple test comparisons. For parameters that did not fulfil the assumption of normality, we used
the nonparametric Kruskal-Wallis test and Wilcoxon signed
rank test (for pairwise comparisons).
We analysed eight habitat variables to test for habitat selection and compared our results with the published literature. We
calculated the relative area of each habitat type in two
predefined radii around each roosting site: r=1,300 m to obtain
comparable results with that of Rutishauser et al. (2012), and
r=2,900 m, which is the average distance recorded between the
capture sites and roosting sites in this study. The studied variables were the relative area in percentages of (1) deciduous
forest, (2) mixed forest, (3) coniferous forest, (4) open forest,
(5) shrubbery, (6) orchards and (7) meadows. Following
(Rutishauser et al. 2012), we also calculated the landscape
diversity based on four landscape types (settlement, forest,
shrubbery and meadows). Correlation between variables was
assessed using Spearman’s rank correlation coefficient (ρ) and
ensured that all pairwise values were below 0.5 (Kutner et al.
2004). All roost locations were compared to a random set of
locations generated within the study area. We used a chi-square
goodness-of-fit analysis to test whether habitat composition
around roosts was significantly different from random. The
habitat selection analysis was developed using generalised
linear models (GLM) with a binomial error distribution and a
logit link function (logistic regression models). In order to
estimated the availability of different roost types, we calculated
the relative surface of rocky areas and counted the number of
buildings in the 10-km-radius area. Land cover data used for
obtaining the variables for the habitat selection analysis and the
relative rock cover were obtained from Corine Land Cover
2006 (http://sia.eionet.europa.eu/CLC2006), while the
cartography of buildings was obtained from the Territorial
Information System of Aragón SITAR (http://sitar.aragon.es/)
and the Cartographic Institute of Catalunya ICC (http://www.
icc.es/). Since availabilities of different roost types were not
comparable at the unit level—e.g. scree and rock walls vs.
buildings—their availability at different elevations was
assessed by probability density functions. We generated
kernel density estimations (KDE) of available buildings and
rocky areas across the elevation range using the density function available in R package STAT (Deng and Wickham 2011),
and plotted with the KDE of the employed roosts to obtain a
visual reference of roost availability with respect to elevation.
Roost fidelity (FR) was calculated using the following
equation:
FR ¼
n
X
Ri−1
Pi−1
i¼1
where Ri is the number of different roosts used by the bat i,
Pi is the number of records for the bat i, and n is the total
Eur J Wildl Res
number of bats in the sample. FR, therefore, ranges from 0 to 1
and reflects the probability of roost switching each day, with
the highest values indicating high lability (1=switches every
day) and low values indicating high fidelity (0=same roost
everyday). All spatial and statistical analyses were performed
using GIS software ArcView 3.2 and R 2.9.2 (http://cran.rproject.org/).
Results
We captured 147 bats at 16 netting sites, 117 of them (79 %)
being alpine long-eared bats (Table 1). We radio-tagged 51
animals and were able to identify the roosts of 37 (72 %): 8
breeding females, 12 nulliparous females and 17 males for an
average of 3.4±0.81 location points during the 8-day sampling period. The total radio-tracking effort amounted to 178
person-days.
Roost types
We identified 54 roosts, averaging 2.2±0.85 roost per bat
(several tracked bats shared the same roosts). P. macrobullaris
used three of the four defined roosts categories: crevices (n=
30), scree deposits (21) and buildings (3). Roosts were located
between 1,450 and 2,430 m amsl. The crevices used by bats
were located in various types of rock structures. Bats used
crevices on both sunny south faces and shaded north faces
with snowfields nearby (10–15 m). Males roosted in scree
deposits more often than females, yet five females were also
tracked to these locations, including a pregnant female found
roosting in a scree deposit for a single day. At these deposits,
bats were found alone under average-sized stones (Fig. 2c).
The three building roosts (5.5 % of all roosts) housed maternity colonies comprising 10–15 individuals. The buildings
were in relatively good condition, and the colonies were
located in narrow spaces between wall stones or in the rafters.
The three buildings were solitary structures surrounded by
natural habitats (Table 2).
Habitat selection and roost availability
The chi-square goodness-of-fit analysis showed that roosts
were not located randomly in relation to surrounding habitat
types (X2 =64.422, df=9, p<0.001). The logistic regression
models showed that roosting sites were located closer to
meadows and open forest, and further away from deciduous
forest and shrubbery (Table 3). The values of the remaining
variables were not statistically significant. The two analysed
ranges (r=1,300 m and r=2,900 m) showed consistent results,
though the effect of mixed forest was only significant in the
1,300-m radius. Roosts were located on average 1.91 ±
1.41 km away from the closest forest and 349±297 m above
the treeline. The area within the 10-km radius around roosting
sites consisted of a landscape where the relative extent of bare
rock areas was 27.6 % and the average building availability
was 1.67±1.35 building/km2. However, the availability of
both types of roosts varied with elevation (Fig. 3). Building
density peaked at 1,200 m amsl and tended to decrease with
increasing elevation, even though buildings occurred at up to
2,500 m. The peak in crevice and scree resources was at
2,500 m, though rocky areas were available in the elevation
range between 1,500 and 3,000 m.
Spatial organisation
We found no difference in the elevation of capture sites between
the three bat classes (Kruskal-Wallis: X2 =1.77, df=2, p=0.410),
but we did find differences in the elevation of roosting sites
(ANOVA: F=6.748, df=2, p=0.002). The average elevation of
roosts used by breeding bats was lower than the elevation of
nulliparous females (Tukey: p<0.01) and males (Tukey: p=
0.030) (Table 2). Despite the mean elevation of nulliparous
females being 147 m higher than that of males, differences were
not statistical significance (Tukey: p=0.141). The overall mean
elevation of roosts and capture sites was not statistically different
(Wilcoxon test: v=823.5, p=0.488), and neither were differences within breeding females (Wilcoxon test: v=38, p=
0.070), nulliparous females (Wilcoxon test: v=20, p=0.15)
and males (Wilcoxon test: v=327, p=0.410). Elevation differed
depending on the roost type used (ANOVA: F=4.716, df=2, p=
0.013), as roosts located at rock crevices (1,997±255 m) were at
a higher elevation than roosts in buildings (1,633±175 m,
Tukey: p=0.035). No elevation differences were observed between crevices and screes (Tukey: p=0.089), and screes and
buildings (Tukey: p=0.299). Crevice and scree roosts were
respectively 458±254 m and 254±287 m above the treeline,
while building roosts were 103±92 m below the treeline.
The overall index of roosting fidelity (FR) was 0.51, but
values differed considerably among bat classes and roost
categories. By class, pregnant and lactating females showed
the highest fidelity (FR =0.11), nulliparous females had intermediate values (FR =0.35), whereas males exhibited high
roosting lability (FR =0.88). By category, bats roosting in
buildings had the highest fidelity (FR =0), followed by bats
roosting in crevices (FR =0.21). Conversely, bats roosting in
scree deposits exhibited low fidelity, switching roosts every
day they were tracked (FR =1).
Discussion
This study shows that in the Pyrenees the use of alpine habitats
by P. macrobullaris is not limited to commuting and
Eur J Wildl Res
Table 1 General characteristics of capture locations and obtained samples. Numbers between parentheses indicate the number of radio-tracked
individuals
Valley
Place
Elevation (m)
Distance to forest (km)
Breeding females
Nulliparous females
Males
Ansó
Zuriza
Tachera
Plan d’Aniz
Cubilar de las Vacas
1,550
1,920
1,740
1,570
0.62
1.31
1.44
0.67
1 (1)
0
4 (2)
2
4
2 (2)
5
1
2 (2)
0
2 (2)
1 (1)
Izagra
La Ripera
Ibon de Piedrafita
Llana del Portillo
Cuello Bubalar
Pardina
Cuello Bizeto
Arrablo
Insolas
Barrosa
Biadós
Campirme
1,800
1,590
1,640
1,790
1,800
1,900
2,005
2,350
2,370
1,780
1,770
2,030
Average
1,850±244
2.74
1.3
1.23
3.7
0.32
1.72
2.49
3.86
2.77
1.87
0.27
0.12
1 (1)
2 (1)
0
0
0
0
0
5 (2)
0
1 (1)
5 (3)
2 (2)
Total
23 (13)
2 (2)
5 (1)
0
2 (2)
0
2 (1)
0
3 (1)
0
8 (1)
6 (3)
4 (4)
0
1 (1)
1
2 (1)
1 (1)
5 (2)
1 (1)
4 (1)
14 (3)
7 (3)
4 (2)
5 (1)
44 (17)
50 (21)
Hecho
Aisa
Tena
Ordesa-Añisclo
Bielsa
Plan
Pallars Sobirà
1.65±1.17
occasional foraging bouts but instead this species also roosts
and breeds in alpine environments. Eighty-five percent of the
roosts we found were located above the treeline, including
most of the breeding sites. The ecological pattern of roost use
by this species does not correspond to that of a lowland
species that occasionally commutes to higher elevations for
foraging. Instead, the majority of P. macrobullaris roosts
occur at the same elevations as foraging areas (Table 2),
suggesting that the population of alpine long-eared bats is
resident in the Pyrenean alpine habitat (Fig. 2). Free-ranging
individuals have also been captured at high elevations (above
1,800 m) in the Alps, the Pindos Mountains, the Caucasus and
the Zagros Mountains (Alberdi et al. 2013), suggesting that
the pattern we observed may be similar to that of other
populations.
Roost types
P. macrobullaris used various structures including natural and
artificial shelters for roosting, as is common among bats
(Rancourt et al. 2005; Lausen and Barclay 2006). Nevertheless, the observed roosting behaviour differed from that described in previous studies of this species (Benda et al. 2004;
Presetnik et al. 2009; Mattei-Roesli 2010; Rutishauser et al.
2012) and of Plecotus bats in general (Swift 1998). In our
study area, alpine long-eared bats roosted primarily in crevices. We found that both males and females (including five of
the nine pregnant and lactating bats) used crevices during the
active season. Crevices in cliffs are also typically used as
nesting places for alpine birds such as the alpine chough, the
wallcreeper and the white-winged snowfinch (Madge and
Burn 1994; Saniga 1995; Yan-Hua et al. 2002). These sites
likely provide protection from predators and harsh meteorological conditions.
Notably, roosting among the small stones of scree deposits
was common in alpine long-eared bats. Some bats, mainly
crevice-dwellers such as Myotis daubentonii and Myotis
nattereri, have occasionally been found in rocky debris on
the floor of caves and tunnels (Baagøe 2001). Furthermore,
there is a single observation of a northern bat (Eptesicus
nilsonii) roosting among stones in Norway (van der Kooij
1999). Myotis leibii and Myotis evotis are, to our knowledge,
the only species known to commonly roost in talus slopes
(Solick and Barclay 2006; Johnson et al. 2011). Recently,
Myotis lucifugus was recorded to roost in scree slopes in
Colorado, USA (D. Neubaum, personal communication). Talus slopes are typical roosting resources for several small
mammals closely linked to rocky environments, such as the
snow vole (Chionomys nivalis) and the North American pika
(Ochotona princeps) (Smith and Weston 1990), although
these mammals usually build a lair below or among stones.
Scree is abundant and easy to identify in craggy landscapes,
where it offers a variety of microclimatic conditions depending on composition, rock sizes, and deposit depth (Scapozza
et al. 2011). Thus, bats can potentially find the optimal conditions under scree deposits by moving through the deposit.
Only three breeding females out of the 37 tracked bats were
observed roosting in buildings. This contrasts with data from
Eur J Wildl Res
Fig. 2 Roost views, with icons
showing exact roost locations. a
General view of a roost area in
Añisclo Canyon; the area covered
by photos b and c is marked with
white insets. b Detail of the
limestone cliff with a horizontal
crevice (1,880 m) where two
breeding females roosted. c The
scree deposit (2,140 m) of five
roosting points belonging to two
male bats; the area shown by
photo d is marked with an inset. d
A male alpine long-eared bat
roosting in a scree deposit
sticking out its head after stones
had been removed
the Alps, where nearly all known roosts are exclusively located in buildings (Presetnik et al. 2009; Mattei-Roesli 2010;
Rutishauser et al. 2012). P. macrobullaris in the Alps and the
Pyrenees may indeed have completely different roosting behaviours; however, we cannot exclude the possibility that
studies in the Alps may have overemphasised the importance
of buildings. Almost all the records in the Alps come from
building surveys considered suitable a priori, which entails a
bias towards buildings. Similarly, the few roosts that were
previously known in the Pyrenees were also in buildings
(Dejean 2009, personal observations), but our radio-tracking
approach revealed an entirely different scenario. Because
P. macrobullaris has also been captured in supraforestal habitats in the Alps (Alberdi et al. 2013), a similar radio-tracking
Table 2 Summary statistics for roosting sites of breeding females, nulliparous females and males. The last three columns show the number of roost types
used by bats from each category
Breeding
females
Nulliparous
females
Males
Total
Capture elevation (m)
Roosting
elevation (m)
Treeline
difference (m)
Forest distance (km)
Capture distance (km)
Crevices
Screes
Buildings
1,887±225
1,705±208
123±280
0.78±1.02
2.86±2.17
5
1
3
1,921±118
2,071±212
510±255
2.74±1.22
3.51±2.39
8
4
0
1,930±291
1,850±244
1,924±234
1,921±249
345±285
349±297
1.89±1.37
1.91±1.41
2.66±2.13
2.88±2.18
17
30
16
21
0
3
Eur J Wildl Res
Table 3 Used and available habitat features and the coefficients of the GLM in the two analysed scales
1300 m radius
Deciduous forest (%)
Mixed forest (%)
Coniferous forest (%)
Open forest (%)
Shrubbery (%)
Orchards (%)
Meadows (%)
Richness (1–4)
2900 m radius
Used
Available
Coefficient
Used
Available
Coefficient
2.57±5.62
0.51±1.89
8.61±16.67
11.01±13.40
1.25±3.77
0
50.59±18.58
2.27±0.87
16.10±20.55
5.93±13.56
14.70±19.83
8.12±12.98
8.03±13.55
0.04±0.75
22.66±23.45
2.37±0.69
−0.087***
−0.125*
−0.014
0.033**
−0.124**
−9.461
0.023***
0.106
3.68±5.21
2.03±4.83
7.35±11.47
7.50±9.39
2.18±2.87
0
51.33±13.33
2.81±0.39
15.77±16.88
5.76±10.29
14.69±15.85
7.94±9.82
7.57±9.94
0.04±0.47
22.54±19.63
2.97±0.62
−0.092***
−0.023
−0.023
0.061***
−0.109**
−12.906
0.045***
−0.474
*p<0.05; **p<0.01; ***p<0.001 (significant)
study in the Alps would unambiguously determine whether
the observations we made in the Pyrenees can be extrapolated
to other areas.
Roost availability and habitat selection
0.0010
Density
0.0005
0.0000
Fig. 3 Density plot of the
elevational distribution of used
roosts and the availability of
different roosting resources across
the altitudinal gradient. The grey
area indicates the kernel density
estimation (KDE) of roosting
sites. The blue line indicates the
KDE of buildings. The red line
indicates the KDE of the rock
resources. The vertical dashed
line indicates the average treeline
elevation in the study area
0.0015
Results from the habitat selection analysis suggest that at least
in the Pyrenees P. macrobullaris is an open-space forager.
These results are in accordance with the molecular diet analysis, which showed that bats forage in alpine meadows
(Alberdi et al. 2012b). Additionally, no P. macrobullaris have
been captured so far in dense forest areas in the Pyrenees
(Alberdi et al. 2013). Roosting near foraging areas would
allow bats to save energy by minimising long displacement
flights, and the predominant use of crevices and scree deposits
is probably linked to that fact, since natural rock resources in
the alpine belt provide almost unlimited roosts near the
meadows used as foraging grounds. Rock roosts were located
on average at higher elevation than roost in buildings, corresponding to their relative availability across the elevational
gradient (Fig. 3). Most buildings are located below the treeline
while most rock areas can be found in the alpine belt. Bats
opted not to fly to lower elevations for roosting, and the radiotracking approach disclosed that more breeding females
roosted in crevices than in buildings, some of which were
located above the treeline. Additionally, all non-breeding bats
were found to use crevices in rocky structures. This suggests
that females may select artificial shelters either when suitable
rock resources in the surroundings of foraging grounds are
limited or when they provide more suitable, perhaps warmer
or drier, conditions for reproduction than rocks.
The pattern identified in this study largely contrasts with
the observations reported from the Alps, where roosting areas
of P. macrobullaris were linked to deciduous forest environments, while meadows were avoided (Rutishauser et al.
2012). It is important to note that another radio-tracking study
carried out in the Alps concluded that bats avoided woodlands
(Preatoni et al. 2011). Therefore, further studies are necessary
in order to obtain a clearer picture of the actual ecological
preferences of this species in the Alps.
500
1000
1500
2000
Elevation range
2500
3000
Eur J Wildl Res
Spatial organisation
References
We did not observe overall differences between the mean
elevation of capture sites (foraging areas) and roosting sites.
Nevertheless, although being captured at the same mean elevation as the rest of the classes, breeding females roosted lower
than the nulliparous females and males. Therefore, while no
altitudinal segregation was observed when capturing free-flying
bats, altitudinal segregation relating to breeding condition did
occur in regards to roosts selection. Breeding bats have different
thermal requirements than nulliparous females and males
(Cryan et al. 2000), which prevents them from lowering their
body temperature to the same extent as non-breeding bats (Dzal
and Brigham 2012). As a result, all bats exploit the same
elevation belt for foraging, but males and nulliparous females
are able to roost at higher elevation most likely because they are
not restricted in their ability to lower their body temperature,
which allows them to shelter in colder roosts closer to their
foraging areas. While breeding females showed higher roosting
fidelity and mostly relied on crevices, males used both scree
deposits and crevices evenly and used structures spread over a
wider elevational range. The solitary behaviour of males, their
ability to exploit structurally diverse natural roosts and their
frequent switching between sites contribute to a labile roosting
behaviour that potentially allows males to remain close to
temporally variable foraging patches. Even though the short
tracking time of each bat prevented us from studying the longterm spatiotemporal dynamics of the roosting behaviour of
P. macrobullaris, within the 40-day time span of the study, we
did not observe temporal variations in the behaviour of the bats.
Our research shows that P. macrobullaris uses a variety of
roosts, with rocky structures being used more often than
human-made buildings, most likely because rock resources
offer the necessary shelter and are closer to foraging habitats
than most buildings. Scree deposits deserve special mention
given that they are comparatively unknown in the roosting
spectrum of bats worldwide. Bats were found roosting up to
1,000 m above the treeline, suggesting that this species has
evolved some specific adaptations, whether physiological, behavioural or both, for coping with the demanding abiotic conditions of alpine environments. Comparative studies of the
torpor behaviour of different classes in other species may help
elucidate specific adaptations. Finally, the existence of a breeding population in an alpine area confirms the alpine long-eared
bat’s affinity towards high-mountain environments, which is in
accordance with the species’ trophic ecology (Alberdi et al.
2012b) and alpine distribution (Alberdi et al. 2013).
Aellen V (1962) Le baguement des chauves-souris au Col de Bretolet
(Valais). Arch des Sci 14:365–392, Genève
Alberdi A, Aihartza J, Albero JC et al (2012a) First records of the particoloured bat Vespertilio murinus (Chiroptera: Vespertilionidae) in
the Pyrenees. Mammalia 76:109–111
Alberdi A, Garin I, Aizpurua O, Aihartza J (2012b) The foraging ecology
of the mountain long-eared bat Plecotus macrobullaris revealed
with DNA mini-barcodes. PLoS ONE 7:e35692. doi:10.1371/
journal.pone.0035692.t001
Alberdi A, Garin I, Aizpurua O, Aihartza J (2013) Review on the
geographic and elevational distribution of the mountain long-eared
bat Plecotus macrobullaris, completed by utilising a specific mistnetting technique. Acta Chiropterol 15:451–461
Arthur L, Lemaire M (2009) Les chauves-souris de France, Belgique,
Luxembourg et Suisse. Biotope Editions, Meze
Ashrafi S, Rutishauser M, Ecker K et al (2013) Habitat selection of three
cryptic Plecotus bat species in the European Alps reveals contrasting
implications for conservation. Biodivers Conserv 22:2751–2766.
doi:10.1007/s10531-013-0551-z
Baagøe HJ (2001) Danish bats (Mammalia: Chiroptera): atlas and analysis of distribution, occurrence and abundance. Zoological
Museum, University of Copenhagen, Copenhagen
Barataud M (2005) Fréquentation des paysages sud-alpins par des
chiroptères en activités de chasse. Le Rhinolophe 17:11–22
Benda P, Kiefer A, Hanak V, Veith M (2004) Systematic status of African
populations of long-eared bats, genus Plecotus (Mammalia:
Chiroptera). Folia Zool 53:1–47
Benda P, Georgiakakis P, Dietz C (2008) Bats (Mammalia: Chiroptera) of
the Eastern Mediterranean and Middle East. Part 7. The bat fauna of
Crete, Greece. Acta Soc Zool Bohem 72:105–190
Cramp S, Perrins CM, Brooks DJ, Dunn E (1994) Handbook of the birds
of Europe the Middle East and Nort Africa. VIII—Crows to finches.
Oxford University Press, Oxford
Cryan P, Bogan M, Altenbach J (2000) Effect of elevation on distribution of
female bats in the Black Hills, South Dakota. J Mammal 81:719–725
Dejean S (2009) Capture du très peu connu Oreillard montagnard
(Plecotus macrobullaris). Taís 3:18–19
Deng H, Wickham H (2011) Density estimation in R. Electronic
publication
Dietz C, Helversen von O (2004) Illustrated identification key to the bats
of Europe. Electronic publication. Accessed 15 May 2010
Dzal YA, Brigham RM (2012) The tradeoff between torpor use and
reproduction in little brown bats (Myotis lucifugus). J Comp
Physiol B 183:279–288
Garin I, Garcia-Mudarra JL, Aihartza J et al (2003) Presence of Plecotus
macrobullaris (Chiroptera: Vespertilionidae) in the Pyrenees. Acta
Chiropterol 5:243–250
Holzhaider J, Zahn A (2001) Bats in the Bavarian Alps: species composition and utilization of higher altitudes in summer. Mamm Biol 66:
144–154
Johnson J, Kiser J, Watrous K, Peterson T (2011) Day-roosts of Myotis
leibii in the Appalachian Ridge and Valley of West Virginia.
Northeast Nat 18:95–106
Kutner M, Nachtsheim C, Neter J (2004) Applied linear regression
models. McGraw Hill/Irwin Series. Accessed 8 Sept 2014
Lausen CL, Barclay RMR (2006) Benefits of living in a building: big
brown bats (Eptesicus fuscus) in rocks versus buildings. J Mammal
87:362–370
Luque-Larena JJ, López P, Gosálbez J (2002) Microhabitat use by the
snow vole Chionomys nivalis in alpine environments reflects rockdwelling preferences. Can J Zool 80:36–41
Madge S, Burn H (1994) Crows and jays. Christopher Helm Publishers
Ltd, London
Acknowledgments The Basque Government supported this study
(project IT-301/10), and the Governments of Aragon and Catalonia
provided the necessary permits for performing it. We thank all the
students and forest rangers who participated in the demanding fieldwork.
Eur J Wildl Res
Mattei-Roesli M (2010) Situazione del genere Plecotus (Chiroptera) nel
Cantone Ticino (Svizzera). Boll Soc ticin Sci nat 98:31–34
Michaelsen T (2010) Steep altitudinal gradients can benefit lowland bats.
Folia Zool 59:203–205
Pavlinic I, Tvrtkovic N (2004) Altitudinal distribution of four Plecotus
species (Mammalia, Vespertilionidae) occurring in Croatia. Croatian
Nat Hist Museum 13:395–401
Preatoni D, Spada M, Wauters L et al (2011) Habitat use in the female
Alpine long-eared bat (Plecotus macrobullaris): does breeding
make the difference? Acta Chiropterol 13:355–364
Presetnik P, Koselj K, Zagmajster M (2009) Atlas netopirjev
(Chiroptera) Slovenije. Atlas of bats (Chiroptera) of Slovenia.
Miklavž na Dravskem polju : Center za kartografijo favne in
flore, Ljubiana
Rancourt SJ, Rule MI, O’Connell MA (2005) Maternity roost site
selection of long-eared myotis, Myotis evotis. J Mammal 86:
77–84
Russo D (2002) Elevation affects the distribution of the two sexes in
Daubenton’s bats Myotis daubentonii (Chiroptera: Vespertilionidae)
from Italy. Mammalia 66:543–551
Rutishauser MD, Bontadina F, Braunisch V et al (2012) The challenge
posed by newly discovered cryptic species: disentangling the environmental niches of long-eared bats. Divers Distrib 18:1107–1119
Saniga M (1995) Seasonal distribution, altitudinal and horizontal migration of the wallcreeper (Tichodroma muraria) in the Malá Fatra
Mountais, Slovak Carpathians. Folia Zool 44:237–246
Scapozza C, Lambiel C, Baron L et al (2011) Internal structure and
permafrost distribution in two alpine periglacial talus slopes,
Valais, Swiss Alps. Geomorphology 132:208–221. doi:10.1016/j.
geomorph.2011.05.010
Shehab A, Karatas A, Amr Z et al (2007) The distribution of bats
(Mammalia: Chiroptera) in Syria. Vertebrate Zool 57:103–132
Smith AT, Weston ML (1990) Ochotona princeps. Mamm Species 352:
1–8
Solick D, Barclay R (2006) Thermoregulation and roosting behaviour of
reproductive and nonreproductive female western long-eared bats
(Myotis evotis) in the Rocky Mountains of Alberta. Can J Zool 84:
589–599
Swift SM (1998) Long-eared bats. Poyser, London
van der Kooij J (1999) Nordflaggermus Eptesicus nilssonii funnet i
steinrøys. Fauna 52:208–211
Villaret JC, Bon R, Rivet A (1997) Sexual segregation of habitat by the
alpine ibex in the French Alps. J Mammal 78:1273–1281
Yan-Hua Q, Zuo-Hua Y, De Ritis SF (2002) Distribution patterns of snow
finches (genus Montifringilla) in the Tibetan Plateau of China.
Avocetta 26:11–18