Behavioral correlates of migration in bats – do migration strategies predict responses to a novel environment?

Abstract

Migration is a life-history trait that shapes individual-by-environment interactions, affecting fitness. Currently, many species are changing their migration strategies, stressing the need to identify and better understand the behavioral correlates of migration. As a partial migrant, the noctule bat, Nyctalus noctula, allows for rare intra-specific investigations of the potential behavioral causes (or consequences) of variation in migration. Here, we combined in-situ behavioral assays with stable isotope analyses to investigate whether spatial and acoustic responses to a roost-like novel environment correlate with migration strategy (local or distant). Given a migrant’s more frequent exposure to novel environments, we predicted migrants would enter a novel environment more quickly and show stronger spatial and acoustic exploration activity. However, individuals of local and distant origin did not differ in acoustic exploration (call activity per unit space), nor, contrasting to several bird studies, in spatial activity (number of chambers visited). Surprisingly, local individuals were more likely than migrants to enter the novel environment. Our findings suggest that small-scale exploration does not vary with migration, potentially because of similar selection pressures across migration strategies on small-scale exploration (e.g., exploration of roosts) as opposed to large-scale. Yet, our findings on the likelihood of entering a novel environment suggest that locals may be more risk-taking. Repeated measures would be necessary to determine if personality differences are underlying these responses. Our unique approach, combining behavioral assays with isotopic geolocation, gave us novel insight into an elusive taxon, highlighting the importance of studying behavioral correlates of migration across various taxa.

Full text

ORIGINAL ARTICLE
Behavioral Ecology and Sociobiology (2024) 78:68
https://doi.org/10.1007/s00265-024-03483-2
Communicated by G. S Wilkinson.
Extended author information available on the last page of the article
Abstract
Migration is a life-history trait that shapes individual-by-environment interactions, aecting tness. Currently, many spe-
cies are changing their migration strategies, stressing the need to identify and better understand the behavioral correlates
of migration. As a partial migrant, the noctule bat, Nyctalus noctula, allows for rare intra-specic investigations of the
potential behavioral causes (or consequences) of variation in migration. Here, we combined in-situ behavioral assays with
stable isotope analyses to investigate whether spatial and acoustic responses to a roost-like novel environment correlate
with migration strategy (local or distant). Given a migrant’s more frequent exposure to novel environments, we predicted
migrants would enter a novel environment more quickly and show stronger spatial and acoustic exploration activity.
However, individuals of local and distant origin did not dier in acoustic exploration (call activity per unit space), nor,
contrasting to several bird studies, in spatial activity (number of chambers visited). Surprisingly, local individuals were
more likely than migrants to enter the novel environment. Our ndings suggest that small-scale exploration does not vary
with migration, potentially because of similar selection pressures across migration strategies on small-scale exploration
(e.g., exploration of roosts) as opposed to large-scale. Yet, our ndings on the likelihood of entering a novel environment
suggest that locals may be more risk-taking. Repeated measures would be necessary to determine if personality dier-
ences are underlying these responses. Our unique approach, combining behavioral assays with isotopic geolocation, gave
us novel insight into an elusive taxon, highlighting the importance of studying behavioral correlates of migration across
various taxa.
Signicance Statement
The decision to migrate impacts both individual tness and ecosystem connectivity, yet we know very little about the
behavioral correlates of migration strategies. Studying such correlates is the rst step to identifying the behavioral causes
and consequences of migration. Here, we took advantage of a partially migratory species, the common noctule bat,
and a unique measure of acoustic exploration, to test potential correlations between migration strategy and small-scale
emergence and exploration. We found local individuals more likely to enter a novel environment than migrants and that
migration strategy did not predict acoustic exploration. This is the rst study examining novel environment responses
and migration in bats and reveals contrasting behavioral correlates of migration compared to other taxa. Our research,
therefore, highlights the importance of including more non-model species in the study of the causes and consequences of
animal migration.
Keywords Animal migration · Bats · Behavioral assay · Echolocation · Exploration behavior · Stable isotope analysis
Received: 18 October 2023 / Revised: 17 May 2024 / Accepted: 29 May 2024 / Published online: 5 June 2024
© The Author(s) 2024
Behavioral correlates of migration in bats – do migration strategies
predict responses to a novel environment?
TheresaSchabacker1,2 · SoaRizzi3,4 · TobiasTeige5· UweHomeister6· Christian C.Voigt2·
LysanneSnijders2,7
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Behavioral Ecology and Sociobiology (2024) 78:68
Introduction
Whether animals decide to migrate aects ecosystem func-
tioning and has consequences on the individual (e.g., physi-
ological), population (e.g., demography), and species level
(e.g., covarying life-history traits) (Cresswell et al. 2011;
Hobson et al. 2019). It is, therefore, crucial to better under-
stand variation in migratory behavior.
Populations of partial migratory species can oer impor-
tant insights into the behavioral correlates of migration.
Partial migratory populations are composed of individuals
that remain local throughout the year and individuals that
migrate over long distances. Partial migration is ubiqui-
tous in various taxa, including insects (Menz et al. 2019),
amphibians (Grayson et al. 2011), sh (Espinoza et al.
2016), birds (Arnekleiv et al. 2022), and mammals (Pur-
don et al. 2018). Individuals of partially migratory popu-
lations respond with dierent migration strategies to the
same environmental cues. It can, therefore, be expected
that individuals of such species show corresponding varia-
tion in behavioral responses to challenges in other contexts
as well. Such behavioral correlates may indicate underly-
ing behavioral syndromes as drivers of migration strategies
(e.g., Found and St. Clair 2016). Indeed, roaches (Rutilus
rutilus) with a shorter latency to emerge into a novel envi-
ronment were more likely to migrate from a lake (Chapman
et al. 2011), and migrating blue tits (Cyanistes caeruleus)
showed a shorter latency to approach a novel object than
residents (Nilsson et al. 2010). Yet, as far as we are aware,
no study investigated if long-distance migrants and locals of
the same species and population dier in how they explore,
i.e., examine and investigate, a novel environment, a behav-
ior which is likely crucial for detecting novel resources
in unfamiliar and changing habitats. Interestingly, echo-
locating bats, although understudied in this context, would
allow detailed quantitative investigation, not only of how
individuals move but also how they sample environmental
information during exploration.
Despite their species richness and pivotal role in eco-
system functioning (Kunz and Fenton 2005; Ghanem and
Voigt 2012), little is known about migration in bats (Popa-
Lisseanu and Voigt 2009). However, novel tools have now
become available to study their migration strategies. Using
non-invasive isotopic geolocation (Popa-Lisseanu et al.
2012), we can estimate the breeding origins of European
bats. Isotopic geolocation uses naturally occurring dier-
ences in stable isotope ratios, for example, stable hydrogen
isotope ratios in precipitation water (δ2HP), which are gov-
erned by global-scale hydrologic processes. The isotopic
dierences in precipitation are seasonally and spatially pre-
dictable by latitude and elevation and allow the reconstruc-
tion of so-called isotopic landscapes, i.e., isoscapes, which
assign an isotopic signature to specic locations (Hobson
1999, 2008; Bowen et al. 2005; Courtiol et al. 2018). This
regionally specic isotopic signature is incorporated into
consumer tissue via diet and drinking water. Analyzing
stable hydrogen isotope ratio of keratinous material (δ2HK;
e.g., fur), which is metabolically inert, provides a direct
reection of the location of fur growth and thereby allows
for the tracking of animal movements (Hobson and Was-
senaar 1996; Popa-Lisseanu et al. 2012; Sullivan et al. 2012;
Baerwald et al. 2014; Voigt et al. 2015; Hobson 2018). By
analyzing stable hydrogen isotopes in bat fur, Lehnert et al.
(2018) conrmed high variability in the migratory behavior
of common noctule bats (Nyctalus noctula) across Europe.
Additionally, they observed a high degree of consistency in
migratory behavior within individuals.
To investigate whether migration strategy and exploratory
behavior correlate, we estimated the migration strategies
and quantied the emergence and subsequent exploration
behavior for wild female noctule bats. We took advantage
of a well-monitored colony in Brandenburg, Northeastern
Germany, where the population comprises local, year-round
present individuals and individuals on migration using this
area as a stopover or wintering site. We combined isotopic
geolocation, based on hydrogen, with an in situ maze-like
novel environment assay. This novel environment assay
was recently established to quantify exploratory behavior
in another tree-dwelling bat species, the Nathusius’ bat
(Pipistrellus nathusii), and revealed individually consistent
dierences in spatial activity and ‘acoustic exploration’,
i.e., the level of environmental cue sampling per unit space
(Schabacker et al. 2021). Given that migrants frequently
encounter dierent and novel habitats, we predicted long-
distance migrants to emerge quicker into a novel envi-
ronment and to exhibit more exploratory behaviors (i.e.,
increased spatial and acoustic exploration activity) in the
test arena than local noctule bats of the same population.
Methods
Study species
Noctule bats are distributed throughout Europe. They are
insectivorous and typically roost in tree holes or crevices
or anthropogenic structures like attics or bat boxes. Com-
mon noctules migrate in early autumn and spring (Sluiter
et al. 1966; Hutterer et al. 2005). Albeit much of noctule
bat migration is still cryptic, banding eorts revealed that
the general migration pattern unfolds along a Northeastern–
Southwestern axis (Steens et al. 2004; Hutterer et al. 2005;
Lehnert et al. 2018; Lindecke et al. 2022), and some indi-
viduals were shown to cover more than 1600 km between
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Behavioral Ecology and Sociobiology (2024) 78:68
breeding and hibernating sites (Dietz et al. 2009). Copula-
tion occurs while bats migrate through dierent habitats.
This ensures the mixing of spatially segregated populations
and increases genetic diversity (Petit and Mayer 2000).
Pups are born in early summer (June/July).
General study approach
Between April 11th and 25th, and October 3rd and 28th of
2019, we sampled a total of 89 adult females from a wild
colony of Noctule bats near the village of Prieros, Branden-
burg, Germany (52°13’24"N, 13°45’16"E). We collected
adult female bats in the early evening (April) or late after-
noon (October) from roost boxes located 4–5 m above the
ground. To minimize disturbance in the population, we prior-
itized roost boxes based on the presence of previously tested
bats (identied by passive integrated transponders (PIT)
tags, see Supplementary Information) or based on group size
(as assessed from outside the box). Following removal from
roost boxes, we determined sex, body mass (digital pocket
scale, 0.01-gram scale, and spring balance, 0.1-gram scale,
+/- 0.1 g), and forearm length (analog vernier dial caliper,
0.1 mm scale). We excluded juveniles (when clearly distin-
guishable based on morphological characteristics (Brunet-
Rossinni and Wilkinson 2009; Kravchenko et al. 2020)) and
males from further study due to evidence of female-biased
migration in this species (Lehnert et al. 2018).
Female bats (mean ± standard deviation: weight:
29.3 ± 4.1 g, forearm length: 54.2 ± 1.2 mm) were kept
together in roosting groups in a dark environment (dark-
ened plastic boxes, approximately 30 × 20 × 15 cm) until
they were subjected to the behavioral assay (two hours later,
on average). The boxes were equipped with cloth and heat
packs to stimulate normothermia. Subsequently, we removed
females from these boxes and conducted the behavioral
assays primarily after sunset (or briey before (N = 4; 35 to
9 min before sunset)), a time during which noctule bats are
naturally active. Assays took place in a tent within 200 m of
the place of capture, providing a standardized environment
to ensure minimal external inuences. Ambient tempera-
tures were comparable between the months, with a mean of
10.9 ºC (range: 5.6–17.6 °C) in April and 10.4 °C (range:
6.0–18.0 °C) in October. After the behavioral assay, we took
a dorsal fur sample from just above the uropatagium for
isotopic geolocation (Voigt et al. 2015). The samples were
stored dry at ambient temperature until further analysis.
Observers were blind to the migratory strategy of the sub-
jects since the stable isotope results were only known after
the quantication of the behavioral responses.
Stable isotope analyses
Similar to other migratory bats, common noctule bats molt in
summer before autumn migration (Ilyin 1990; Kravchenko
et al. 2020). Accordingly, collected fur samples indicate the
location where an individual spent the previous summer
(2018 for April samples and 2019 for October samples). Fur
samples of juveniles represent the location where they were
born. Since Lehnert et al. (2018) provided evidence for high
individual repeatability of noctule bat migration strategies,
we here assume that bats did not change their migration
strategy between 2018 and 2019.
All stable hydrogen isotopes from bat fur samples were
analyzed at the stable isotope lab at the Leibniz Institute for
Zoo and Wildlife Research (Berlin, Germany). To prepare
the samples for analysis, we cleaned o all external contam-
inants and oils with a chloroform:methanol (2:1) solution.
The samples were placed in the cleaning solution for 24 h on
a shaking platform (Phoenix GmbH). The fur samples were
then dried for ten days in a drying oven (Heraeus Func-
tion Line, ThermoFischer Scientic, Bremen, Germany) at
50 °C.
We analyzed samples in sequence with keratin refer-
ence materials with known stable isotope ratios for the non-
exchangeable portion of hydrogen. We used four in-house
standards: sheep wool from Sweden (-167.9 ± 1‰), sheep
wool from Spain (-108.3 ± 1‰), goat wool from Tanzania,
Africa (-66.3 ± 0.9‰), and USGS42 standard (-74 ± 0.5‰)
from Tibetan human hair. A detailed description of the
preparation of the standards is reported in Popa-Lisseanu
et al. (2012). We weighed samples and standards using a
microbalance (Sartorius ME5, Göttingen, Germany) to
0.274 ± 0.01 mg and placed them into 3.3 mm × 5 mm
silver-foil capsules (IVA Analysetechnik e.K. Meerbusch,
Germany). We folded capsules into small packages and
stored them in a 96-well microtiter plate. After preparation
of the plate, we left it in a drying oven at 50 °C for 24 h
to remove extra moisture. Subsequently, we transferred
samples and standards into the carrousel of a Zero Blank
autosampler (Costech Analytical Technologies Inc., Italy)
of the high-temperature elemental analyzer (HTO Elemen-
taranalysator HEKAtech GmbH, Wegberg, Germany). The
samples were ushed for one hour with chemically pure
helium (Linde, Leuna, Germany) as a carrier gas at a ow
rate of 100 ml/min, eliminating remaining moisture and thus
suppressing the inux of ambient H2O. The foil packages
were then pyrolyzed in the element analyzer at 1450 °C.
The gas chromatograph separates H2, N2, and CO at 80 °C
and introduces the resolving H2 through the Cono III inter-
face (ThermoFischer Scientic, Bremen, Germany) into the
isotope ratio mass spectrometer (Delta V Advantage IRMS,
ThermoFischer Scientic, Bremen, Germany). We used
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Behavioral Ecology and Sociobiology (2024) 78:68
night vision camera (Sony Digital Camcorder, DCR-SR72E,
Sony, Tokyo, Japan) on a tripod equipped with a horizontal
arm positioned 1.5 m above the maze. Light was provided
by an infra-red ashlight (T38, Evolva Future Technology,
Shenzhen, China), shining at an angle from a xed posi-
tion. We captured vocalizations through a directional USG
Electret Ultrasound microphone (polar pattern 180°, Avisoft
Bioacoustics/Knowles FG, Berlin, Germany) connected to
an ultrasound recorder (UltraSoundGate 116Hb, Avisoft
Bioacoustics, Berlin, Germany), which was placed within
the larger box pointing to the center of the maze.
At the start of an assay, we placed the bat in the opaque
start tube (10 × 3 cm), while vertical and horizontal barriers
in the form of a small wooden dowel still obstructed the
exit. After an acclimatization period of 20 s, we removed
the barrier and gave a maximum of three minutes for the
bat to emerge from the start tube. We recorded the bats’
emergence times, i.e., the time it took for an individual to
emerge completely from the start tube: (1) latency to head
emergence (s), (2) latency to full body emergence (s), and
(3) duration of emergence (s) (i.e., the dierence between
(1) and (2)). If a bat did not emerge within three minutes,
we terminated the test since forcing it into the maze would
likely lead to a dierent type of behavioral response than
what we were interested in. After a successful emergence,
bats were allowed to explore the maze for two minutes, and
we recorded an individual’s exploratory behavior as (4) the
number of unique chambers discovered, (5) the total num-
ber of chambers visited, and (6) the number of times a bat
poked its head in an adjacent chamber. These response mea-
sures are congruent with those reported in Schabacker et al.
(2021) and were later quantied in detail using the open-
source event logging software BORIS (Friard and Gamba
2016; version 7.9.1). After each test, we removed potential
only those samples for further analysis where the amplitude
peak of the δ2H sample did not exceed 6500 mV. This is
based on repeated measures of in-house keratin standards
better than 3‰ (which is equivalent to one standard devia-
tion). Consequently, we had to exclude seven samples. The
robustness of this single isotope approach was conrmed
using a triple isotope approach on a subset of the data (See
Supplementary Information).
Behavioral assay and analysis
Prior to the behavioral assay in the experimental arena, we
conrmed a bat’s normothermia by measuring skin tem-
perature with a thermocouple (Peakmeter, PM6501; Ther-
mocouple, Sensor SSP-1-150, Peakmeter, Shenzhen, China,
+/- 2.2 °C). Skin temperature (> 30 °C) is a non-invasive
measurement that accurately reects rectal temperature
(Barclay et al. 1996). The experimental arena in which the
bats were subsequently placed mimicked a potential novel
roost, and we thus regarded its exploration as relevant for a
tree-dwelling bat species. The maze-like arena (Fig. 1 and
40 × 40 × 5 cm) consisted of nine separate chambers con-
nected through small gates (3 × 2.5 cm) on the upper half
of the walls. A rubber non-slip mat overlaid the oor to pro-
vide a good texture for crawling, a behavior intuitive to tree-
dwelling bats. A layer of insect screen overlaid the entire
maze, preventing a bat’s escape and oering another climb-
ing opportunity. The entrance to the maze was an opaque start
tube (10 × 3 cm) attached to the maze but blocked by a small
wooden dowel, which was removed at the start of an assay.
The entire maze was placed horizontally – to stimulate natu-
ral exploration behavior in all directions – in a larger box
(70 × 45 × 8 cm) with a transparent lid. We monitored the
bat’s movement from an aerial perspective by mounting a
Fig. 1 Schematic drawing of the
maze used during behavioral
assay. (A) Opaque start tube
(10 × 3 cm) where bats were
placed at the start of each assay.
(B) Wooden dowel obstructing the
entrance to the maze (only the ver-
tical dowel was used for common
noctules). (C) Gates connecting
single rooms. (D) Position of the
microphone. ©Rebecca Scheibke
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Behavioral Ecology and Sociobiology (2024) 78:68
Network of Isotopes in Precipitation (GNIP) database,
which is a publicly available database of global isotope
data. We tted a geostatistical mixed model to predict the
spatial distribution of δ2HP roughly covering Europe (longi-
tude range: -30° East to 60° West, latitude range: 30 North°
to 70° North; Supplementary Fig. S1). Subsequently, we
used the transfer function provided by Lehnert et al. (2018)
to relate δ2Hf values as a linear function to δ2HP values. This
transfer function uses a combination of δ2H values of local,
non-migrating insectivorous bat species and those of noct-
ule bats sampled during their non-migratory period across
Central and Eastern Europe (Voigt et al. 2014; Lehnert et al.
2018; Voigt and Lehnert 2018). We opted for this multispe-
cies-informed transfer function rather than a single-species
function, as only a relatively small sample size-informed
transfer function would have been available for noctule
bats, which might not cover the full range of variation in
the δ2H tissue values. The multispecies function, however,
results in a lower spatial resolution but generally ensures
a more comprehensive and reliable assignment (Voigt and
Lehnert 2018). By applying this function, we were able to
directly map the assignment samples onto the isoscape. We
used the isond function to test the probability of a sample
originating from the candidate location Prieros, Branden-
burg, Germany, under the null hypothesis that the unknown
location of origin is identical to the candidate location.
For assignments where the P-value fell below α = 0.05, we
rejected the null hypothesis and concluded a migratory sta-
tus for the respective individual. Finally, assignments were
visualized highlighting areas with the most probable place
of origin (Fig. 2).
Emergence, spatial activity, and acoustic
exploration behavior
Following Schabacker et al. (2021), we focused on three rel-
evant and independent response measures: full body emer-
gence (yes/no), the total number of chambers visited, and
acoustic exploration.
To test if the response to a novel environment varies
with migration strategy, three (generalized) linear models
were constructed, with body emergence (yes/no, binomial),
the total number of chambers visited (Poisson), or acoustic
exploration (normal) as the dependent variable and migra-
tion strategy (local/migrant) as the independent variable of
interest. Control variables included the season the sample
was taken (April or October) and the body condition of
the subject as weight (g) divided by forearm length (mm).
We conducted backward stepwise model selection, always
keeping the independent variable of interest (i.e., migration
strategy) in the model. Control variables with P ≥ 0.1 were
removed from the model. Qualitative conclusions regarding
olfactory cues by sterilizing the maze with a mild, unscented
detergent. Halfway through the night, we rotated the setup
to control for potential orientation biases. There was no sig-
nicant correlation between the likelihood to emerge and
the orientation of the setup (P > 0.30). Afterward, bats were
released on the same night and within 100 m of the original
capture location.
Audio analysis
We recorded echolocation activity during the exploration of
the novel environment and assessed the number of echoloca-
tion calls in Avisoft SASLab Pro (Avisoft Bioacoustics, Ver-
sion 5.2). Preceding the analysis, we converted the sampling
frequency from 250 kHz to 150 kHz. Spectrogram computa-
tion was accomplished via Fast Fourier Transformation 256,
parameters set to Hamming window (bandwidth 1270 Hz,
resolution 977 Hz) and volume normalized to 75%. Vocal
start and stop commands given by the observer allowed the
synchronization of video and audio recordings. We identi-
ed distinct echolocation calls via Avisoft’s call detection
and template-based spectrogram comparison feature, which
we veried and corrected via visual inspection. This enabled
us to count (7) the total number of echolocation calls after
full-body emergence. We quantied (8) ‘acoustic explora-
tion’ as a response measure, representing acoustic sampling
of the environment using echolocation while accounting for
spatial activity (number of chambers visited). Following
Schabacker et al. (2021), this was calculated as the residuals
of (7) the total number of echolocation calls emitted over
(5) the total number of chambers visited during the assay.
These residuals represent the variance that is not explained
by the tted regression line (see Results and Supplementary
Information). Lastly, we quantied the number of emitted
air pus (see Supplementary Information).
Statistical analysis
All analyses were conducted using the statistical software
R, version 4.2.1 (R Core Team 2022).
Isotopic geographic assignments
To delineate the origin of captured noctule bats in Bran-
denburg, we performed isotopic geolocation based on the
R package “IsoriX” and tightly followed the workow
described in Courtiol et al. (2018). Briey, the workow
is divided into three main components: generation of the
isoscape, tting the calibration model, and geographically
assigning unknown samples to the most probable place of
origin. We built the isoscape based on hydrogen isotope
ratios in precipitation water (δ2HP) obtained from the Global
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Behavioral Ecology and Sociobiology (2024) 78:68
strategy could not be reliably determined, and not all bats
emerged into the arena, resulting in dierent sample sizes
per analysis (Table 1).
the eect of migration did not dier between the starting
and nal models. Model assumptions were veried using
the packages ‘dHARMA’ (Hartig and Hartig 2017) and
‘performance’ (Lüdecke et al. 2021), using the functions:
check_collinearity(), simulateResiduals() and plot(). Due to
detected underdispersion in the Poisson model, we also con-
ducted a generalized Poisson regression using the ‘VGAM’
package, but this did not lead to qualitatively dierent con-
clusions. The data and code underlying the analyses can be
accessed through the Open Science Framework (Snijders
and Schabacker 2022).
Our initial intention was to also investigate individual
repeatability. However, due to the low number of repeated
assays (See Supplementary Information), we decided to
focus our analysis on the behavioral responses during the
rst assay only. Moreover, for several assays, the migration
Table 1 Sample size overview
Analysis category NMigrants/Locals
Total assays 98 -
Total unique bats assayed 89 -
Total unique stable hydrogen isotope
samples
82 49/33
Total unique bats that emerged into the
arena
45 -
Total unique bats with a stable hydrogen
isotope sample that emerged into the arena
41 19/22
Fig. 2 Geographic probability
distribution of the most probable
place of origin of an assigned
migrant (upper panel) and an
assigned local bat (lower panel).
The color scale indicates the level
of certainty of correct assign-
ment (expressed as P-value). Bats
for which a local status could
be excluded using an α = 5%
threshold were assigned a migrant
status. Bats for which a local
origin could not be excluded
were assigned a local status, i.e.,
originating from the sampling
location Prieros, Brandenburg,
Germany (~ 40 km Southeast of
Berlin, indicated on the maps by
the blue star). Isoclines (regions
of similar δ2HP values) follow
latitude closely and thus resolve
animal movements from East to
West poorly. However, there is
substantial evidence for migra-
tion happening along an axis from
Northeast to Southwest, making
it unlikely that bats carrying the
”local” isotopic ngerprint are
actually migrants stemming from
more Eastern regions on the same
latitude (e.g., as suggested in the
lower panel)
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Behavioral Ecology and Sociobiology (2024) 78:68
Discussion
Little is known about the behavioral correlates of migration
in partial migrants and, specically, whether migratory indi-
viduals may be characterized by more exploratory responses
to a novel environment. Here, we conducted one of the rst
novel environment tests in a partially migratory population.
In contrast to our expectations, we found that local individu-
als were more likely to emerge into the novel environment
than long-distance migrants, which may be explained by
local bats being more risk-taking. Furthermore, we found
no correlation between spatial exploration activity, acoustic
exploration (i.e., environmental cue sampling), and migra-
tion strategy, suggesting that explorative behavior is equally
important for migratory and local noctule bats.
Local individuals are more likely to enter the novel
environment
We observed a correlation between emergence behavior
and migration strategy, but in the opposite direction than
expected. As migrants are more often confronted with novel
environments, we expected migrants to be more likely to
emerge into the novel environment. Yet the long-distance
migrants were less likely to emerge than the local individu-
als. This also appears to contrast with related movement
ecology studies in other taxa. For example, roaches (Rutilus
rutilus) that emerged quicker from a refuge migrated more
often from a lake (Chapman et al. 2011). In bank voles
(Myodes glareolus), individuals with shorter latencies to
emerge and investigate an unknown area occupied larger
home ranges (Schirmer et al. 2019). Lastly, in two warbler
Results
Based on the stable hydrogen isotope analyses, 60% of the
bats were classied as long-distance migrants (Supplemen-
tary Table S1, Supplementary Fig. S2) and migrants were
as likely to be previously handled (banded) as local conspe-
cics (Fisher Exact Test: OR (95% CI) = 0.57 (0.20–1.54),
N = 89, P = 0.26). Only 51% of the bats emerged into the
novel environment arena, and these were most likely to be
locals (P = 0.01, Supplementary Table S2, Fig. 3a).
Individuals that emerged into the novel environment var-
ied considerably in their behavioral exploration responses
(Supplementary Fig. S3a-e), e.g., the total number of
chambers visited ranged from four to 28, and the number
of calls emitted after emergence ranged from 474 to 1443.
As expected, the number of calls was strongly correlated to
the total number of chambers visited (both variables square
root transformed; r = 0.42, N = 45, P = 0.004, Supplemen-
tary Fig. S4a). Despite this strong correlation, there was
substantial variation in how thoroughly bats acoustically
explored the novel environment (Supplementary Fig. S4b).
The variation in exploration responses was, however, not
driven by migration strategy since migrants did not show
higher spatial exploration activity (the number of chambers
visited, P = 0.70, Supplementary Tables S3, S4, Fig. 3b)
nor stronger acoustic exploration than locals in the novel
environment (P = 0.37, Supplementary Table S5, Fig. 3c).
Lastly, there were no notable correlations between any of
the quantied behavioral responses (i.e., emergence latency,
number of chambers visited, acoustic exploration, number
of air pus and number of head pokes into adjacent cham-
bers; Supplementary Table S6).
Fig. 3 Noctule bats’ behavioral
responses to the novel environ-
ment assay as a function of
their migration strategy. Local
individuals were (a) more
likely to emerge into the novel
environment (maze) (Ntotal =
82), yet local individuals and
long-distance migrants did not
dier in (b) their spatial explora-
tion activity (total number of
chambers visited) or (c) their
acoustic exploration (residuals
of the number of echolocation
calls emitted over the number of
chambers visited) (Ntotal = 41).
Box plots in panels (b) and (c)
depict the median as the central
line and interquartile range with
whiskers of 1.5 interquartile
distances
1 3
Page 7 of 11 68
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Behavioral Ecology and Sociobiology (2024) 78:68
the general level of acoustic exploration and spatial explora-
tion activity exhibited by migrants.
Unfortunately, due to a low recapture rate, we were not
able to collect enough repeated measures to test the individ-
ual repeatability of the behavioral responses. We can thus
not conclude whether the variation in the recorded behav-
ioral responses is indicative of personality. We do see some
interesting parallels with Nathusius’ bats, for which we pre-
viously demonstrated repeatability of the same behavioral
responses (Schabacker et al. 2021). Similar to noctule bats,
these migratory Nathusius’ bats showed substantial levels
of variation in spatial and acoustic traits and a strong cor-
relation between spatial exploration activity and echoloca-
tion activity. In contrast, acoustic exploration in noctule bats
did not vary with other exploratory behaviors, such as the
number of head pokes into adjacent chambers, as we found
in Nathusius’ bats. We hope to instigate future research
focusing on the repeated examination of novel environment
responses, and especially acoustic exploration, in echolo-
cating bats to gain further insight into the behavioural syn-
dromes that may underly the observed behavioral variation.
This could be achieved by housing bats temporarily (e.g.,
24 h) on-site, rather than depending on recapture, and con-
ducting repeated tests the following night, prior to release.
Potential implications for the conservation of
migrants
Animal migration is under pressure, and a better understand-
ing of the underlying mechanism that may make migrants
more vulnerable to changing environments would allow for
more targeted conservation plans (Wilcove and Wikelski
2008). We found long-distance migrants to be less eager
to enter a novel environment, meaning that migratory bats
may be more aected by novelty-associated stress. Expo-
sure to novelty increases eects associated with physiologi-
cal stress (Pster 1979), yet not all individuals are aected
equally. Studies with free-ranging sparrows showed that
when confronted with novelty, inquisitive birds exhibited
the lowest stress response, measured as stress-induced corti-
costerone (Lendvai et al. 2011). This has important implica-
tions since energy attributed to stress responses will not be
available for other energetically demanding activities, such
as migration. Given the rapidly changing world, especially
for migratory bats, which are continuously confronted with
anthropogenically changed roosts and stopover sites (Voigt
and Kingston 2016), future research should investigate if
migrants and locals indeed dier in their endocrinological
stress responses towards novelty. Furthermore, we did not
nd evidence that migrants and locals dier in their ability
to detect changes in the environment. So, migrants should
not have more diculty locating suitable novel roosting
species (Sylvia sp.), more individuals from the migra-
tory species entered a novel environment than individuals
from the closely related local species, and they did so more
quickly (Mettke-Hofmann and Greenberg 2005; Mettke-
Hofmann et al. 2009).
Fast emergence into a novel environment from a secure
place may be interpreted as a form of risk-taking (Carter et
al. 2013). As local individuals spend extended periods in the
same location, they likely have more complete information
about their current local environment simply because they
had more opportunities to sample (Dall et al. 2015). These
individuals could then be expected to be very well informed
about predation risks throughout the year and thus might
behave more condently, i.e., risk-prone (Error management
theory: Johnson et al. 2013; Feyten et al. 2019). In contrast,
migrants might benet from behaving warily and vigilantly
because they do not have extended knowledge about pre-
dation danger in their current environment (Dangerous
niche hypothesis: Greenberg and Mettke-Homann 2001;
Mettke-Hofmann et al. 2013). A more risk-averse behavior
in migrants could thus compensate for the increased risks
associated with migration behavior, especially in prey spe-
cies (Found and St. Clair 2016). It is important to note that
local bats were not more likely to emerge because they were
more habituated to human handling since local bats were
not more likely to be previously banded (and thus handled)
than long-distance migrants.
No dierence in spatial activity and acoustic
exploration between intra-specic migration
strategies
Bats actively manipulate the level of echolocation pulses
they emit and thus individually control incoming informa-
tion from the environment. We expected migrants to be
characterized by more acoustic exploration as they could
benet more from continuously updating their informa-
tion when moving through novel environments. However,
despite substantial variation in spatial exploration activity
and acoustic exploration, we found that neither of these
measures varied with migration strategy. Our results thus
suggest that spatial activity and environmental cue sampling
are equally used by locals and migrants, possibly because
spatial and acoustic exploration is crucial also outside the
migration context, such as during foraging and orientation
inside the roost (Kunz 1982; Schnitzler et al. 2003). In our
assays, we let bats choose whether they entered the novel
environment since forcing non-emerging bats into the novel
environment would likely result in fear-related behavioral
responses rather than exploration. We, however, acknowl-
edge that with only 50% of the bats emerging, it is possible
that the migrants that did emerge were not representative of
1 3
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use, you will need to obtain permission directly from the copyright
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org/licenses/by/4.0/.
References
Arnekleiv Ø, Eldegard K, Moa PF, Eriksen LF, Nilsen EB (2022) Driv-
ers and consequences of partial migration in an alpine bird spe-
cies. Ecol Evol 12:e8690. https://doi.org/10.1002/ece3.8690
Baerwald EF, Patterson WP, Barclay RMR (2014) Origins and migra-
tory patterns of bats killed by wind turbines in southern Alberta:
evidence from stable isotopes. Ecosphere 5:1–17. https://doi.
org/10.1890/ES13-00380.1
Barclay RMR, Kalcounis MC, Crampton LH, Stefan C, Vonhof MJ,
Wilkinson L, Brigham RM (1996) Can external radiotransmitters
be used to assess body temperature and torpor in bats? J Mammal
77:1102–1106. https://doi.org/10.2307/1382791
Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of
stable hydrogen and oxygen isotopes to wildlife forensics. Oeco-
logia 143:337–348. https://doi.org/10.1007/S00442-004-1813-Y
Brunet-Rossinni AK, Wilkinson GS (2009) Methods for age estima-
tion and the study of senescence in bats. In: Kunz T, Parsons S
(eds) Ecological and behavioral methods for the study of bats,
2nd edn. Johns Hopkins University, Baltimore, pp 315–325
Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R
(2013) Animal personality: what are behavioural ecologists mea-
suring? Biol Rev 88:465–475. https://doi.org/10.1111/BRV.12007
Chapman BB, Hulthén K, Blomqvist DR, Hansson LA, Nils-
son JÅ, Brodersen J, Anders Nilsson P, Skov C, Brönmark C
(2011) To boldly go: individual dierences in boldness inu-
ence migratory tendency. Ecol Lett 14:871–876. https://doi.
org/10.1111/J.1461-0248.2011.01648.X
R Core Team (2022) R: a language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna, Aus-
tria, https://www.r-project.org/
Courtiol A, Rousset F, Rohwäder MS, Soto DX, Lehnert LS, Voigt
CC, Hobson KA, Wassenaar LI, Kramer-Schadt S (2018)
Isoscape computation and inference of spatial origins with mixed
models using the R package IsoriX. In: Hobson A, Wassenaar
LI (eds) Tracking Animal Migration with stable isotopes, 2nd
edn. Academic, London, pp 207–236. https://doi.org/10.1016/
B978-0-12-814723-8.00009-X
Cresswell KA, Satterthwaite WH, Sword GA (2011) Understanding the
evolution of migration through empirical examples. In: Milner-
Gulland EJ, Fryxell JM, Sinclair ARE (eds) Animal Migration: A
Synthesis, online edn. Oxford Academic Press, Oxford, pp 7–17.
https://doi.org/10.1093/acprof:oso/9780199568994.003.0002
Dall SRX, Giraldeau LA, Olsson O, McNamara JM, Stephens DW
(2015) Information and its use by animals in evolutionary ecol-
ogy. Trends Ecol Evol 20:187–193. https://doi.org/10.1016/j.
tree.2005.01.010
Dietz C, von Helversen O, Nill D, Lina PH, Hutson AM (2009) Bats
of Britain, Europe and Northwest Africa. A & C Black, London
Espinoza M, Heupel MR, Tobin AJ, Simpfendorfer CA (2016) Evidence
of partial migration in a large coastal predator: opportunistic for-
aging and reproduction as key drivers? PLoS ONE 11:e0147608.
https://doi.org/10.1371/JOURNAL.PONE.0147608
spots or avoiding fatal collisions with novel anthropogenic
objects (e.g., wind turbines: Voigt et al. 2012; Lehnert et al.
2014) than locals. This is relevant since noctule bats are a
common victim of wind turbines (Lehnert et al. 2014).
Conclusion
Our unique approach, combining behavioral assays with iso-
topic geolocation in an elusive and vulnerable taxon, gave
us novel insight into the behavioral correlates of migration.
In contrast to our hypotheses, we found no relationship
between spatial or acoustic exploration activity and migra-
tion strategy and found local individuals more likely to enter
an unfamiliar environment than long-distance migrants.
This does not allign with related movement ecology stud-
ies in other taxa. Revealing such species-specic relation-
ships will be essential for a better and more comprehensive
understanding of the potential behavioral causes and conse-
quences of migration.
Supplementary Information The online version contains
supplementary material available at https://doi.org/10.1007/s00265-
024-03483-2.
Acknowledgements We thank Kseniia Kravchenko for assistance in
the isotope analysis, Anja Luckner for conducting the laboratory anal-
yses, and Ana Paul for support during eldwork. We thank Rebecca
Scheibke for her illustration of the novel environment assay. We also
wish to thank the two anonymous reviewers and the editor for their
constructive feedback that helped to substantially improve this manu-
script.
Funding LS was funded by a Humboldt Research Fellowship for Post-
doctoral Researchers (Ref 3.3 – NLD – 1192631 - HFST-P) awarded
by the Alexander von Humboldt-Stiftung.
Data availability The datasets and code generated and analyzed during
the current study are available through the Open Science Framework
(OSF): https://doi.org/10.17605/OSF.IO/KXTJ5. A key to the vari-
ables in the OSF is available on the nal pages of the Supplementary
Information and the OSF Wiki page.
Declarations
Ethics approval The use of animals adheres to the guidelines of the
Animal Behavior Society/Association for the Study of Animal Be-
haviour. All eldwork and associated procedures were conducted in
agreement with the authorities and in accordance with German law
under a German animal welfare permit (number 2347-25-2018) and
conservation permit (number LFU-N1-4743/128 + 25#314731/2018).
Conict of interest The authors have no relevant nancial or non--
nancial interests to disclose.
Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in any medium or format,
as long as you give appropriate credit to the original author(s) and the
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Page 9 of 11 68
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Behavioral Ecology and Sociobiology (2024) 78:68
Lehnert LS, Kramer-Schadt S, Schönborn S, Lindecke O, Niermann
I, Voigt CC (2014) Wind farm facilities in Germany kill noct-
ule bats from near and far. PLoS ONE 9:e103106. https://doi.
org/10.1371/journal.pone.0103106
Lehnert LS, Kramer-Schadt S, Teige T et al (2018) Variability and
repeatability of noctule bat migration in Central Europe: evidence
for partial and dierential migration. Proc R Soc B 285:20182174.
https://doi.org/10.1098/rspb.2018.2174
Lendvai ÁZ, Bókony V, Chastel O (2011) Coping with novelty and
stress in free-living house sparrows. J Exp Biol 214:821–828.
https://doi.org/10.1242/JEB.047712
Lindecke O, Currie SE, Fasel NJ, Fritze M, Kravchenko K, Kruszyn-
ski de Assis C, Lehnert LS, Röleke M, Voigt-Heucke SL,
Voigt CC (2022) Common Noctule Nyctalus noctula (Schre-
ber, 1774). In: Hackländer K, Zachos FE (eds) Handbook of
the mammals of Europe. Springer, Cham, pp 1–25. https://doi.
org/10.1007/978-3-319-65038-8_63-2
Lüdecke D, Ben-Shachar M, Patil I, Waggoner P, Makowski D (2021)
Performance: an R Package for Assessment, comparison and test-
ing of statistical models. J Open Source Softw 6:3139. https://doi.
org/10.21105/JOSS.03139
Menz MHM, Reynolds DR, Gao B, Hu G, Chapman JW, Wotton
KR (2019) Mechanisms and consequences of partial migra-
tion in insects. Front Ecol Evol 7:403. https://doi.org/10.3389/
fevo.2019.00403
Mettke-Hofmann C, Greenberg R (2005) Cognitive adaptations to
long distance migration. In: Greenberg R, Mara P (eds) Birds of
two worlds: the ecology and evolution of migration. Johns Hop-
kins University, Baltimore, pp 114–123
Mettke-Hofmann C, Lorentzen S, Schlicht E, Schneider J, Werner F
(2009) Spatial neophilia and spatial neophobia in resident and
migratory warblers (Sylvia). Ethology 115:482–492. https://doi.
org/10.1111/j.1439-0310.2009.01632.x
Mettke-Hofmann C, Winkler H, Hamel PB, Greenberg R (2013)
Migratory New World blackbirds (Icterids) are more neopho-
bic than closely related resident Icterids. PLoS ONE 8:e57565.
https://doi.org/10.1371/journal.pone.0057565
Nilsson ALK, Nilsson JÅ, Alerstam T, Bäckman J (2010) Migratory
and resident blue tits Cyanistes caeruleus dier in their reaction
to a novel object. Naturwissenschaften 97:981–985. https://doi.
org/10.1007/s00114-010-0714-7
Petit E, Mayer F (2000) A population genetic analysis of migration: the
case of the noctule bat (Nyctalus noctula). Mol Ecol 9:683–690.
https://doi.org/10.1046/J.1365-294X.2000.00896.X
Pster HP (1979) The glucocorticosterone response to novelty as a
psychological stressor. Physiol Behav 23:649–652. https://doi.
org/10.1016/0031-9384(79)90154-9
Popa-Lisseanu AG, Voigt CC (2009) Bats on the move. J Mammal
90:1283–1289. https://doi.org/10.1644/09-MAMM-S-130R2.1
Popa-Lisseanu AG, Sörgel K, Luckner A et al (2012) A triple-isotope
approach to predict the breeding origins of European bats. PLoS
ONE 7:e30388. https://doi.org/10.1371/journal.pone.0030388
Purdon A, Mole MA, Chase MJ, van Aarde RJ (2018) Partial
migration in savanna elephant populations distributed across
southern Africa. Sci Rep 8:11331. https://doi.org/10.1038/
s41598-018-29724-9
Schabacker T, Lindecke O, Rizzi S, Marggraf L, Pētersons G, Voigt
CC, Snijders L (2021) In situ novel environment assay reveals
acoustic exploration as a repeatable behavioral response in
migratory bats. Sci Rep 11:8174. https://doi.org/10.1038/
s41598-021-87588-y
Schirmer A, Herde A, Eccard JA, Dammhahn M (2019) Individuals
in space: personality-dependent space use, movement and micro-
habitat use facilitate individual spatial niche specialization. Oeco-
logia 189:647–660. https://doi.org/10.1007/s00442-019-04365-5
Feyten LEA, Demers EEM, Ramnarine IW, Brown GE, Zhang JX
(2019) Predation risk assessment based on uncertain informa-
tion: interacting eects of known and unknown cues. Curr Zool
65:75–76. https://doi.org/10.1093/cz/zoy083
Found R, Clair CS (2016) Behavioural syndromes predict loss of
migration in wild elk. Anim Behav 115:35–46. https://doi.
org/10.1016/j.anbehav.2016.02.007
Friard O, Gamba M (2016) BORIS: a free, versatile open-source
event-logging software for video/audio coding and live
observations. Methods Ecol Evol 7:1325–1330. https://doi.
org/10.1111/2041-210X.12584
Ghanem SJ, Voigt CC (2012) Increasing awareness of ecosystem ser-
vices provided by bats. Adv Stud Behav 44:279–302. https://doi.
org/10.1016/B978-0-12-394288-3.00007-1
Grayson KL, Bailey LL, Wilbur HM (2011) Life history benets of
residency in a partially migrating pond-breeding amphibian.
Ecology 92:1236–1246. https://doi.org/10.1890/11-0133.1
Greenberg R, Mettke-Hofmann C (2001) Ecological aspects of neo-
phobia and neophilia in birds. In: Nolan V, Thompson CF (eds)
Current ornithology, 16th edn. Springer, Boston, pp 119–178.
https://doi.org/10.1007/978-1-4615-1211-0_3
Hartig F, Hartig FM (2017) DHARMa - Residual Diagnostics for
HierArchical (Multi-level / Mixed) Regression Models. R Devel-
opment Core Team, Vienna, Austria, https://cran.microsoft.
com/snapshot/2017-03-04/web/packages/DHARMa/vignettes/
DHARMa.html
Hobson KA (1999) Tracing origins and migration of wildlife using
stable isotopes: a review. Oecologia 120:314–326. https://doi.
org/10.1007/S004420050865
Hobson KA (2008) Applying isotopic methods to tracking ani-
mal movements. Terr Ecol 2:45–78. https://doi.org/10.1016/
S1936-7961(07)00003-6
Hobson KA (2018) Application of isotopic methods to tracking animal
movements. In: Hobson KA, Wassenaar LI (eds) Tracking Animal
Migration with stable isotopes, 2nd edn. Academic, London, pp
85–115. https://doi.org/10.1016/B978-0-12-814723-8.00004-0
Hobson KA, Wassenaar LI (1996) Linking breeding and wintering
grounds of neotropical migrant songbirds using stable hydrogen
isotopic analysis of feathers. Oecologia 109:142–148. https://doi.
org/10.1007/S004420050068
Hobson KA, Kardynal KJ, Norris DR, Yohannes E (2019) Animal
migration: a context for using new techniques and approaches. In:
Hobson KA, Wassenaar LI (eds) Tracking Animal Migration with
stable isotopes, 2nd edn. Academic, London, pp 1–23. https://doi.
org/10.1016/B978-0-12-814723-8.00001-5
Hutterer R, Ivanova T, Meyer-Cords C, Rodrigues L (2005) Bat migra-
tions in Europe: a review of banding data and literature. Federal
Agency for Nature Conservation, Bonn, Germany
Ilyin VY (1990) The seasonal shedding of Pipistrellus nathusii and
Nyctalus noctula. In: Ilyn VY, Strelkov PP, Rodionov VA (eds)
Materials of the Fifth All-Union Conference on Bats. Penza State
Educational Institute, Penza, pp 86–89
Johnson DDP, Blumstein DT, Fowler JH, Haselton MG (2013) The
evolution of error: error management, cognitive constraints, and
adaptive decision-making biases. Trends Ecol Evol 28:474–481.
https://doi.org/10.1016/J.TREE.2013.05.014
Kravchenko KA, Vlaschenko AS, Lehnert LS, Courtiol A, Voigt CC
(2020) Generational shift in the migratory common noctule bat:
rst-year males lead the way to hibernacula at higher latitudes.
Biol Lett 16:20200351
Kunz TH (1982) Roosting ecology of bats. In: Kunz TH (ed)
Ecology of bats. Springer, Boston, pp 1–55. https://doi.
org/10.1007/978-1-4613-3421-7_1
Kunz T, Fenton M (2005) Preface. In: Kunz TH, Fenton MB (eds) Bat
ecology. University of Chicago Press, Chicago, pp xii-xix
1 3
68 Page 10 of 11
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Behavioral Ecology and Sociobiology (2024) 78:68
LI (eds) Tracking animal migration with stable isotopes, 2nd
edn. Academic, London, pp 117–135. https://doi.org/10.1016/
B978-0-12-814723-8.00005-2
Voigt CC, Popa-Lisseanu AG, Niermann I, Kramer-Schadt S (2012)
The catchment area of wind farms for European bats: a plea for
international regulations. Biol Conserv 153:80–86. https://doi.
org/10.1016/J.BIOCON.2012.04.027
Voigt CC, Lehnert SL, Popa-Lisseanu AG et al (2014) The trans-
boundary importance of articial bat hibernacula in managed
European forests. Biodivers Conserv 23:617–631. https://doi.
org/10.1007/s10531-014-0620-y
Voigt CC, Lehmann D, Greif S (2015) Stable isotope ratios
of hydrogen separate mammals of aquatic and terrestrial
food webs. Methods Ecol Evol 6:1332–1340. https://doi.
org/10.1111/2041-210X.12414
Wilcove DS, Wikelski M (2008) Going, going, gone: is animal
migration disappearing? PLoS Biol 6:1361–1364. https://doi.
org/10.1371/JOURNAL.PBIO.0060188
Publisher’s Note Springer Nature remains neutral with regard to juris-
dictional claims in published maps and institutional aliations.
Schnitzler HU, Moss CF, Denzinger A (2003) From spatial orienta-
tion to food acquisition in echolocating bats. Trends Ecol Evol
18:386–394. https://doi.org/10.1016/S0169-5347(03)00185-X
Snijders L, Schabacker T (2022) Data from: behavioural correlates of
migration in bats. Open Sci Framew. https://doi.org/10.17605/
OSF.IO/KXTJ5
Sullivan AR, Bump JK, Kruger LA, Peterson RO (2012) Bat-cave
catchment areas: using stable isotopes (δD) to determine the
probable origins of hibernating bats. Ecol Appl 22:1428–1434.
https://doi.org/10.1890/11-1438.1
Sluiter JW, van Heerdt PF (1966) Seasonal habits of the noctule bat
(Nyctalus noctula). Arch Neerl Zool 16:423–439. https://doi.org/
10.1163/036551666X00011
Steens R, Zöphel U, Brockmann D (2004) 40 Jahre Fledermausmar-
kierungszentrale Dresden: methodische Hinweise und Ergeb-
nisübersicht. Sächsisches Landesamt für Umwelt und Geologie,
Dresden
Voigt CC, Kingston T (2016) Bats in the Anthropocene. In: Voigt
CC, Kingston T (eds) Bats in the Anthropocene: conservation of
bats in a changing world. Springer, Cham, pp 1–9. https://doi.
org/10.1007/978-3-319-25220-9_1
Voigt CC, Lehnert LS (2018) Tracking of movements of terrestrial
mammals using stable isotopes. In: Hobson KA, Wassenaar
Authors and Aliations
TheresaSchabacker1,2 · SoaRizzi3,4 · TobiasTeige5· UweHomeister6· Christian C.Voigt2·
LysanneSnijders2,7
Lysanne Snijders
lysanne.snijders@wur.nl
1 Museum für Naturkunde, Leibniz-Institute for Evolution and
Biodiversity Science, Berlin, Germany
2 Department of Evolutionary Ecology, Leibniz Institute for
Zoo and Wildlife Research, Berlin, Germany
3 Applied Zoology and Nature Conservation, Zoological
Institute and Museum, University of Greifswald, Greifswald,
Germany
4 Faculty of Life Sciences, Humboldt Universitӓt zu Berlin,
Berlin, Germany
5 Büro für faunistisch-ökologische Fachgutachten, Berlin,
Germany
6 Natura – Büro für zoologische und botanische
Fachgutachten, Stuttgart, Germany
7 Behavioural Ecology Group, Wageningen University &
Research, Wageningen, Netherlands
1 3
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