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The relative influence of forest loss and fragmentation on insectivorous bats: does the type of matrix matter?

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Abstract

Context Disentangling the relative effects of forest loss versus fragmentation on species distribution and abundance is crucial for adopting efficient biodiversity conservation actions, which could change with the nature of the landscape matrix. Objectives We tested the moderating effect of landscape matrix on insectivorous bats response to forest loss and fragmentation. Methods We conducted acoustic surveys at forest patches surrounded by either an agricultural-dominated matrix or a pine-dominated matrix. We related bat activity to forest amount and the number of forest patches at multiple spatial scales, and compared their effects between landscape matrices. Results Bat activity was associated with both predictors, however their effects varied with the matrix type. In agricultural landscapes, as the amount of forest increased, the activity of Histiotus montanus, Lasiurus cinereus and Tadarida brasiliensis increased, while activity of Myotis chiloensis decreased. Similarly, as fragmentation increased, the activity of Lasiurus varius and M. chiloensis increased, while activity of H. montanus decreased. In production-forest landscapes, only H. montanus decreased its activity with increasing forest amount. In contrast, activity of L. cinereus, M. chiloensis and T. brasiliensis increased with increasing fragmentation. Forest amount was a stronger predictor for agricultural landscapes than for production-forest landscapes, suggesting that low contrast matrices can mitigate the effects of forest loss. Conclusions Fragmented landscapes with native forest patches surrounded by a low contrast matrix may support a higher activity of insectivorous bats. Management efforts in fragmented landscapes should aim to decrease the patch-matrix contrast, which will mitigate the effects of forest loss on bats.
RESEARCH ARTICLE
The relative influence of forest loss and fragmentation
on insectivorous bats: does the type of matrix matter?
Annia Rodrı
´guez-San Pedro .Javier A. Simonetti
Received: 19 August 2014 / Accepted: 9 May 2015
ÓSpringer Science+Business Media Dordrecht 2015
Abstract
Context Disentangling the relative effects of forest
loss versus fragmentation on species distribution and
abundance is crucial for adopting efficient biodiversity
conservation actions, which could change with the
nature of the landscape matrix.
Objectives We tested the moderating effect of land-
scape matrix on insectivorous bats response to forest
loss and fragmentation.
Methods We conducted acoustic surveys at forest
patches surrounded by either an agricultural-dominat-
ed matrix or a pine-dominated matrix. We related bat
activity to forest amount and the number of forest
patches at multiple spatial scales, and compared their
effects between landscape matrices.
Results Bat activity was associated with both pre-
dictors, however their effects varied with the matrix
type. In agricultural landscapes, as the amount of
forest increased, the activity of Histiotus montanus,
Lasiurus cinereus and Tadarida brasiliensis in-
creased, while activity of Myotis chiloensis decreased.
Similarly, as fragmentation increased, the activity of
Lasiurus varius and M. chiloensis increased, while
activity of H. montanus decreased. In production-
forest landscapes, only H. montanus decreased its
activity with increasing forest amount. In contrast,
activity of L. cinereus,M. chiloensis and T. brasilien-
sis increased with increasing fragmentation. Forest
amount was a stronger predictor for agricultural
landscapes than for production-forest landscapes,
suggesting that low contrast matrices can mitigate
the effects of forest loss.
Conclusions Fragmented landscapes with native
forest patches surrounded by a low contrast matrix
may support a higher activity of insectivorous bats.
Management efforts in fragmented landscapes should
aim to decrease the patch-matrix contrast, which will
mitigate the effects of forest loss on bats.
Keywords Habitat fragmentation Habitat loss
Landscape matrix Insectivorous bats
Scale-dependent responses
Introduction
Landscape change is one of the most important
processes causing elevated rates of species extinction
and loss of biological diversity (Hooper et al. 2012). This
process involves both habitat loss and fragmentation,
two highly correlated processes that have different
effects on biodiversity (Haila 2002; Fahrig 2003).
When the effects of habitat loss and fragmentation are
Electronic supplementary material The online version of
this article (doi:10.1007/s10980-015-0213-5) contains supple-
mentary material, which is available to authorized users.
A. Rodrı
´guez-San Pedro (&)J. A. Simonetti
Departamento de Ciencias Ecolo
´gicas, Facultad
de Ciencias, Universidad de Chile, Casilla 653,
Santiago, Chile
e-mail: ar.sanpedro@gmail.com; sanpedro@ug.uchile.cl
123
Landscape Ecol
DOI 10.1007/s10980-015-0213-5
addressed independently, habitat loss has a greater
impact on biodiversity compared to the effects of
fragmentation by reducing species richness of many taxa
including insects, amphibians, birds, and small mam-
mals (Trzcinski et al. 1999; Nupp and Swihart 2000;
Cushman 2006; Ritchie et al. 2009;Cerezoetal.2010).
The effects of fragmentation, meanwhile, are usually
much weaker and abundance and species richness can
either increase or decrease in fragmented landscapes
(Fahrig 2003).
The direction and magnitude of the effects of
habitat loss and fragmentation on biodiversity might
also be mitigated by the structure of the landscape
matrix (Debinski 2006; Kupfer et al. 2006; Prevedello
and Vieira 2009). The matrix may compensate for
habitat loss providing additional resources for many
species or otherwise act as an ecological trap (With
2002; Vergara and Simonetti 2003; Ewers and Didham
2006; Harvey et al. 2006). In addition, matrix structure
can influence dispersal of fragment-dwelling biota
across the landscape (Ricketts 2001; Baum et al.
2004). Landscapes with structural similarity between
matrix and patches of original habitat would allow
greater faunal movement, while a contrasting struc-
tural matrix would impede movement (Gascon et al.
1999). As a type of forested habitat, plantation forests
may make up a higher quality matrix for embedded
native forest remnants compared with an agricultural
matrix, as they might provide suitable habitats for
many forest-dependent species (Lindenmayer and
Hobbs 2004; Fischer et al. 2006). In addition, plan-
tations may increase species richness and abundance
by improving connectivity between forest remnants
(Gascon et al. 1999; Lindenmayer et al. 1999; Ferreras
2001; Renjifo 2001), enhancing survival in human-
modified landscapes (Gascon et al. 1999; Kupfer et al.
2006; Rodrı
´guez-San Pedro and Simonetti 2013a).
Therefore, the effects of habitat loss and fragmentation
in agricultural dominated landscapes might differ
from those in production-forest landscapes.
Forests are a key habitat for bats throughout the
world. Many species depend on forest attributes such as
foliage and cavities of mature trees for roosting, that are
reduced in fragmented forest (Lacki et al. 2007). In
addition to roosting sites, bats also require suitable sites
for foraging with some species forage within forested
habitats, in forest gaps or along edges, roads or internal
trails in forests (Crome and Richards 1988;Morrisetal.
2010;Rodrı
´guez-San Pedro and Simonetti 2013a). In
Chile, most bat species are associated with forested
habitats (Galaz and Ya
´n
˜ez 2006). Lasiurus cinereus and
Lasiurus varius roost exclusively in the foliage of trees,
while Histiotus macrotus,Histiotus montanus and
Myotis chiloensis may utilize forests occasionally for
roosting (Galaz and Ya
´n
˜ez 2006). Thus, we would
expect a greater bat activity in landscapes with higher
forests cover compared to non-forest landscapes.
Likewise, landscape configurations with high spatial
complementarity between roosting and foraging sites
should support a higher bat activity.
Recent work by Ethier and Fahrig (2011) provided
the first evidence of a positive effect of forest
fragmentation, independent of forest amount, on bat
activity, highlighting the importance of both processes
when assessing bat response to habitat modifications.
However, this study was conducted in fragmented
agricultural landscapes, without considering whether
their results might be applied in landscapes with low
patch-matrix contrast. Rigorously comparing the
effects of habitat loss and fragmentation for patches
surrounded by a low contrast matrix compared to
patches with high contrast matrix will provide impor-
tant guidance in the context of landscape management
for the conservation of biodiversity.
In this paper, we examined how the relative
influence of forest amount and fragmentation on bat
activity vary among landscapes dominated by agri-
cultural lands (high-contrast system) and forestry
plantations-dominated landscapes (low-contrast sys-
tem). If low contrast matrices mitigate the effects of
forest loss and fragmentation on bat activity compared
to high contrast matrices then, bat activity would be
significantly associated with forest loss and fragmen-
tation in agricultural-dominated landscapes but not in
forest-dominated landscapes. To evaluate the relative
effects of forest amount and fragmentation on bat
activity, we used the same methodology followed by
Ethier and Fahrig (2011) in order to make our study
comparable.
Methods
Study area and site selection
The study was conducted in rural areas of central Chile
(Fig. 1). During the last decades, the temperate forest
of central Chile has been deforested and fragmented
Landscape Ecol
123
due to agriculture and forestry plantations (Echeverria
et al. 2006). Currently, the landscape consists of native
forest patches embedded in a matrix of commercial
pine (Pinus radiata) plantations, pastures and agricul-
tural lands (Echeverria et al. 2006). The estimated
cover of native forests decreased from 119,994 ha in
1975 to 39,002 ha in 2000. In 2000, 69 % of the total
area of native forest occurred in patches of less than
100 ha and only 3 % had a size greater than 1000 ha.
We selected 36 non-overlapping native forest
patches (focal patches) that ranged in size from 4.0 to
25.0 ha, focused on landscapes where the dominant
non-forest land cover was either exotic pine plantations
(18 focal patches) or agriculture (18 focal patches)
(Fig. 1). Landscapes were selected to represent a large
variation in forest amount and forest fragmentation and
to minimize, as far as possible, the expected correlation
between these two variables. To minimize the correla-
tion between forest amount and fragmentation, land-
scapes were chosen such that the proportion of native
forest and the number of forest patches represents a
gradient containing not only the common combinations
of high forest amount with low fragmentation and low
forest amount with high fragmentation, but also the
poorly represented combinations of low forest amount
with low fragmentation and high forest amount with
high fragmentation (Ethier and Fahrig 2011). Unfortu-
nately, this was not possible in our agricultural-
dominated landscapes, where forest amount and frag-
mentation were highly correlated at some spatial scales
(see Supporting Information).
We used ArcGIS 9.3 (ESRI 2006) to calculate the
proportion of native forest in the landscape within
each buffer distance, as a measure of forest loss, and
the number of forest patches as a measure of
fragmentation. To account for the possibility that
different bat species respond to the landscape at
different scales, we measured forest loss and frag-
mentation using several buffer sizes at radii of 1.0, 1.5,
2.0, 2.5, 3.0, 4.0 and 5.0 km from the center of each
focal patch. Unfortunately, little is known about the
home range size of Chilean bats. We chose these seven
landscapes buffer distances based on distances trav-
elled between roosting and foraging sites by similar
small and medium-sized aerial insectivorous bats
elsewhere (Elmore et al. 2005; Sparks et al. 2005;
Walters et al. 2007; Henderson and Broders 2008;
Kniowski and Gehrt 2014). Landscapes buffer dis-
tances greater than a 5-km radius were not examined
because those areas would overlap substantially,
Fig. 1 Map of south-
central Chile showing the
location of the 36 surveyed
focal patches
Landscape Ecol
123
producing spatial autocorrelation. Moreover, the se-
lected focal scales facilitate comparison with previous
research on scale-dependent associations of bats with
forest amount and fragmentation (Ethier and Fahrig
2011). Forest amount ranged from 1.1 to 60.2 % in
agricultural landscapes and from 6.5 to 66.8 % in
forested landscapes, meanwhile the number of forest
patches ranged from 3 to 15 in agricultural landscapes
and from 4 to 15 in forestry landscapes. The correla-
tion (Pearson’s r) between forest amount and frag-
mentation ranged from 0.16 to 0.81 in agricultural
landscapes and from 0.025 to 0.35 in forestry
landscapes (see supporting information). All land-
scape variables were based on land cover data from the
Catastro Nacional de Bosque Nativo from Corpo-
racio
´n Nacional Forestal, Chile (http://sit.conaf.cl/).
Bat surveys
We conducted bat surveys for each of the 36 focal
patches for one night each. At each focal patch,
surveys began at dusk and lasted for 4 h to coincide
with peak foraging periods of aerial insectivorous bats
(Kuenzi and Morrison 2003). Surveys were restricted
to the austral summer season (from February to mid-
March 2012 and January 2013), the peak season in bat
activity in temperate zones. Bats were surveyed using
two ultrasound bat-detectors model D240X (Pet-
tersson Elektronik AB, Uppsala, Sweden) per focal
patch coupled to a digital recorder MicroTrack II
(M-Audio) and operated in time-expanded modes.
Time-expanded mode records the full-spectrum
echolocation calls with a high-resolution sonogram
of each bat vocalization. These full-spectrum echolo-
cation calls were used to classify bat activity to species.
We placed the first bat detector at the edge of each
focal patch and the second detector 50 m into the focal
patch within a partial clearing with the microphone
pointing in the same direction as the first one. Calls
were displayed and analyzed using BatSound 2.1
(Pettersson Elektronik AB, Uppsala, Sweden). Bat
activity was quantified by counting the number of bat
passes per night at each point within each local patch
and used as a measure of bat relative abundance
(Walsh et al. 2004). We defined a ‘‘bat pass’’ as a
succession of more than two echolocation pulses
emitted by a bat flying by the detector (Law et al.
1999). Since most passes were recorded along forest
edges (74.7 and 66.4 % in agricultural and forestry
landscape, respectively), we combined the number of
bat passes recorded using both bat detectors (forest
edge and interior) to quantify bat activity per site. We
used bat activity as a comparative index amongst sites
as bat detectors do not allow for individuals to be
differentiated and thus an abundance estimate to be
determined. Surveys were not conducted on nights
with rain or fog to avoid reduced bat activity (Pye
1971; Erickson and West 2002).
For each focal patch, we also measured local habitat
variables such as patch size, temperature, wind speed
and mean density of trees across six 10 910 m
quadrats (Table 1), which has been shown to influence
insectivorous bats use of forested areas (Brigham and
Grindal 1997; Sleep and Brigham 2003). To control
for possible effects of prey availability on bat activity,
we used two light traps per site placed at least 50 m
from the nearest bat detector to capture nocturnal
flying insects simultaneously with the bat surveys. We
used the dry weight (biomass) of insects as a measure
of prey availability at each site.
Bat species identification
Passes of free-flying bats were classified to species
using quadratic discriminant function analysis (DFA).
This analysis was used because several variables
departed from normal distribution and the within-
group variance–covariance matrices were not homo-
geneous (Quinn and Keough 2002). Classification
functions were computed using a library of validated
reference calls which consisted of 264 full-spectrum
recordings from hand-released bats (H. montanus,L.
varius,M. chiloensis and T. brasiliensis) at the
location of study (Rodrı
´guez-San Pedro and Simonetti
2013b). Variables used in the analysis were call
duration, final frequency, slope frequency modulation,
peak frequency, minimal and maximal frequency. If
there was uncertainty or inconsistency in the classi-
fication, that recording was considered unidentifiable
and labeled as ‘‘unknown’’.
Statistical analysis
Data were first checked for normality using Shapiro–
Wilk test. Only when normality was not achieved even
after transformation, non-parametric tests were used.
Because our agricultural and forestry landscapes were
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123
distributed in three different regions which differed in
terms of their topography (Andes, Intermediate de-
pression and Coastal range), we conducted a pre-
liminary analysis using a non-parametric statistic,
Kruskal–Wallis test, to explore for differences in bat
activity for each species among regions. No regional
difference on bat activity was detected (Hfrom 0.307
to 5.282, P[0.05).
We fitted generalized linear models (GLMs)
separately for each matrix type (agricultural and
forestry) to assess the relationship between bat activity
for each species and the landscape structure (forest
amount and the number of forest patches) at each
spatial scale. We used a negative binomial with log-
link function across all GLM models, since count data
for bat activity were not normally distributed and
showed evidence of over-dispersion (Quinn and
Keough 2002). We built GLM models by first
determining local variables (patch size, temperature,
wind speed, tree density and insect biomass) that were
associated with bat activity for each species. To
identify which local variables significantly affected
bat activity, we ran separate regressions using the
number of bat passes per species at a site (bat activity)
as the response variable and included as predictor each
local variables. Variables with a significant effect on
bat activity (P\0.05) were retained and included in
the landscape models (Table 1).
To examine the relative effects of forest amount and
fragmentation on bat activity we included in each
landscape model the amount of native forest and the
number of forest patches as our landscape predictors of
interest as wellas any local variable that was significant
in previous separate regressions analyses. We estimated
the relative effect of forest loss and fragmentation by
comparing the partial regression coefficient, as well as
the number of species that responded significantly to
forest amount and fragmentation. We chose standard-
ized partial regression coefficient because this is a
robust method for estimating the relative importance of
forest amount and fragmentation, even when both
predictors are highly correlated (Smith et al. 2009),
which was our case at some spatial scales (see
supporting information). The inclusion of correlated
predictors in a regression model increases type II errors
by raising the standard error of partial coefficients
(Neter et al. 1990). However, removing highly corre-
lated predictors can lead to biased coefficient estimates
and poor model fit (Smith et al. 2009). We included
correlated predictors, forest amount and number of
forest patches, because they represent distinct eco-
logical mechanism that potentially influence bat ac-
tivity and removing one of them would lead to biased
estimates of the relative importance for the remaining
predictors (Smith et al. 2009). Before analysis, we
standardized the scales of all predictors to a mean of
zero and a standard deviation of one, so that equal
coefficients implied equal effect-strength and to sim-
plify expected variance partitions for each predictor
(Quinn and Keough 2002). In all GLMs, we assessed
Table 1 Results of
generalized linear models
(GLM) examining the
effects of patch local
variables (insect biomass,
tree density, temperature
and wind speed) on bat
activity per species
Missing data indicates no
significant effects of local
variables on bat activity.
Degrees of freedom are 1
for all models
Species Patch local variables bP
Agricultural landscapes
Histiotus montanus ––
Lasiurus cinereus ––
Lasiurus varius Tree density 0.17 0.005
Wind speed -0.18 \0.001
Myotis chiloensis Wind speed -0.24 0.048
Tadarida brasiliensis Tree density -0.14 0.015
Forestry landscapes
Histiotus montanus Temperature 0.23 0.009
Wind speed -0.17 0.019
Lasiurus cinereus Insect biomass 0.21 0.003
Temperature 0.54 \0.001
Lasiurus varius ––
Myotis chiloensis Wind speed -0.07 0.028
Tadarida brasiliensis Insect biomass 0.17 0.006
Landscape Ecol
123
statistical significance using Wald v
2
tests. We checked
for autocorrelation of the model residuals using the
Moran’s I.
We tested our hypothesis about the effects of
landscape matrix on the relationship between bat
activity and forest amount or fragmentation through an
analysis of covariance (ANCOVA) using GLMs with
negative binomial and log-link function, because
assumptions of normality and homogeneity of vari-
ance were not met (Quinn and Keough 2002). We
explored if the effect of forest amount or fragmenta-
tion on bat activity was similar between matrices
comparing the homogeneity of slopes by introducing
the interaction term (matrix type 9forest amount, and
matrix type 9number of forest patches) in each GLM
model (Quinn and Keough 2002). Significantly dif-
ferent slopes (PB0.05) indicate that the relationship
between bat activity and forest amount or fragmenta-
tion differs between matrix types.
Results
Across the 36 nights and 144 survey hours, we recorded
2134 echolocation passes, 1950 of which (91 %) could
be identified and attributed to five of the six species
expected to occur in the study area: H. montanus (55
passes), L. varius (470 passes), M. chiloensis (463
passes), L. cinereus (145 passes) and T. brasiliensis
(817 passes). Passes of L. cinereus were identified by
comparing call parameters with reference calls report-
ed for this species in other regions (O’Farrell et al.
2000). Nine percent of the echolocation passes could
not be analyzed due to the low intensity of the recorded
calls and were classified as ‘‘unknown’’. These passes,
therefore, were not included in the analyses at a species
level but were considered for overall activity analysis.
The most commonly encountered bat species across all
landscapes were L. varius and T. brasiliensis (present
at 35/36 sites) followed by M. chiloensis (28/36), L.
cinereus (21/36) and H. montanus (16/36). Bat activity
residuals were not significantly spatially autocorrelat-
ed for any of the species (Moran’s Ifrom -0.045 to
0.009, P[0.05).
In agricultural landscapes, four species responded
significantly to forest amount while three species
responded significantly to forest fragmentation
(Fig. 2). The relationship between forest amount and
bat activity was significantly positive in H. montanus at
all spatial scales, L. cinereus and T. brasiliensis at
intermediate (1.5–2.5 km) and large scales
(4.0–5.0 km) and negative in M. chiloensis (at 4.0 km)
(Fig. 2). Activity of L. varius was not strongly associ-
ated with forest amount (Fig. 2). Species responses to
forest fragmentation also varied in both direction and
magnitude (Fig. 2). The activity of L. varius and M.
chiloensis significantly increased with increasing frag-
mentation (at intermediate and large scales, respective-
ly), while activity levels significantly decreased for H.
montanus both at small (1.0–1.5 km) and larger scales
(2.5–4.0 km) (Fig. 2). Activity of L. cinereus and T.
brasiliensis were not strongly associated with forest
fragmentation (Fig. 2).
In forest-dominated landscapes, only one species
(H. montanus) responded significantly to forest
amount, but in an opposite way to agricultural
landscapes, with bat activity decreasing with increas-
ing forest amount at small and intermediate scales
(Fig. 3). In contrast, three species (L. cinereus,M.
chiloensis and T. brasiliensis) responded significantly
to forest fragmentation (Fig. 3), and in all cases, bat
activity increased with increasing fragmentation at
small and intermediate scales (Fig. 3). Activity of L.
varius was not significantly associated with either
forest amount or fragmentation (Fig. 3).
The analysis of homogeneity of slopes showed a
significant interaction between matrix type and both
forest amount and the number of forest patches,
suggesting that the effects of forest amount and
fragmentation on bat activity were different for agricul-
tural and forest-dominated landscapes (Table 2). These
effects tended to be stronger for agricultural than for
production-forest landscapes (Figs. 2,3).
Discussion
Bats respond differentially to forest loss, fragmenta-
tion and the nature of the intervening matrix. The
prediction that forest loss and fragmentation have
independent effects on biodiversity has been shown in
experimental studies that controlled for their relation-
ship (McGarigal and McComb 1995; Trzcinski et al.
1999; Villard et al. 1999; Ethier and Fahrig 2011).
These studies focused attention on the independent
effects of forest loss and fragmentation on species, but
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123
did not examine how these effects are modulated by
the structure of the landscape matrix (Debinski 2006).
Similar to Ethier and Fahrig (2011), we found that
the effects of forest amount varied among species. In
addition to forest amount, they found that when there
was evidence for an effect of forest fragmentation,
independent of forest amount, on bat activity, the
effect was positive for most species. These authors
Fig. 2 Scatter plots with error bars of standardized regression
coefficients from GLM examining the effects of forest amount
(square symbols) and fragmentation (circular symbols) on bat
activity in agricultural landscapes at multiple spatial scales. The
black symbols indicate statistical significant at P\0.05 and
unfilled symbols indicate no effect. Degrees of freedom are 1 and
15 for H. montanus and L. cinereus; 1 and 13 for L. varius; 1 and
14 for M. chiloensis and T. brasiliensis
Landscape Ecol
123
suggested that the mechanism driving a positive
response of bats to fragmentation might be a higher
complementation between (or access to) foraging and
roosting habitats in more fragmented landscapes or a
positive response to forest edges. Bats use forest edges
for commuting and foraging (Grindal and Brigham
1999; Morris et al. 2010; Rodrı
´guez-San Pedro and
Simonetti 2013a) and the high number of bat passes
Fig. 3 Scatter plots with error bars of standardized regression
coefficients from GLM examining the effects of forest amount
(square symbols) and fragmentation (circular symbols) on bat
activity in forestry landscapes at multiple spatial scales. The
black symbols indicate statistical significant at P\0.05 and
unfilled symbols indicate no effect. Degrees of freedom are 1 and
13 for H. montanus,L. cinereus and T. brasiliensis; 1 and 15 for
L. varius; 1 and 14 for M. chiloensis
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123
recorded along forest edges in our study (74.7 and
66.4 % in agricultural and forestry landscape, respec-
tively) seems to support this hypothesis. However, an
analysis of the relationship between bat activity and
forest edge density confirmed these assumptions only
for L. varius in agricultural landscapes, where we
found a significant positive effect of forest edge, but
not for the other four species. Therefore, we suggest
that our results of fragmentation effects on bat activity
are consistence with both the landscape complemen-
tation and the positive edge response hypotheses.
Future research should focus on the mechanism behind
individual bats species’ responses to fragmentation.
As forest amount increased, the activity of M.
chiloensis decreased in agricultural landscapes, a
surprising result for an assumed forest-dependent bat
species. M. chiloensis can either forage inside the
forest, close to vegetation, or in edge and gaps created
by natural or anthropogenic disturbance in central
Chile (Galaz and Ya
´n
˜ez 2006; Rodrı
´guez-San Pedro
and Simonetti 2013a). Individuals of this species are
able to use artificial structures, such as farmhouses, for
roosting in rural landscapes where a considerable
amount of forest has been removed (Galaz and Ya
´n
˜ez
2006). It is therefore possible that the availability of
forest edges and open areas for foraging and
Table 2 Summary statistics of the analysis of covariance (ANCOVA) to examine the effects of landscape matrix on the relationship
between bat activity and forest amount or fragmentation (covariates) at each spatial scale
Radius
(km)
Main effects Histiotus
montanus
Lasiurus
cinereus
Lasiurus varius Myotis
chiloensis
Tadarida
brasiliensis
Wald v
2
P Wald v
2
P Wald v
2
P Wald v
2
P Wald v
2
P
1.0 Matrix 4.06 0.044 1.28 0.259 1.14 0.285 6.58 0.010 0.15 0.704
Matrix 9forest amount 14.57 <0.001 1.46 0.227 0.18 0.669 0.05 0.829 0.06 0.800
Matrix 9number of
forest patches
2.96 0.085 2.86 0.091 2.19 0.139 0.09 0.764 0.41 0.524
1.5 Matrix 3.43 0.064 2.41 0.120 1.47 0.226 5.25 0.022 0.59 0.444
Matrix 9forest amount 6.93 0.008 0.23 0.630 2.24 0.134 0.23 0.629 0.59 0.441
Matrix 9number of
forest patches
0.72 0.397 0.19 0.667 3.41 0.065 1.45 0.228 0.25 0.614
2.0 Matrix 3.05 0.080 2.12 0.145 1.29 0.256 6.47 0.011 0.64 0.425
Matrix 9forest amount 6.24 0.012 0.36 0.551 1.62 0.203 1.63 0.202 1.28 0.257
Matrix 9number of
forest patches
0.15 0.701 0.22 0.636 2.33 0.127 0.00 0.974 1.72 0.189
2.5 Matrix 4.06 0.044 1.66 0.197 1.20 0.273 6.59 0.010 0.31 0.580
Matrix 9forest amount 6.19 0.013 0.74 0.391 2.02 0.155 2.55 0.110 0.09 0.765
Matrix 9number of
forest patches
2.22 0.137 3.34 0.068 5.18 0.023 0.23 0.632 11.82 0.001
3.0 Matrix 4.89 0.027 1.67 0.196 1.37 0.242 7.35 0.007 0.08 0.774
Matrix 9forest amount 3.94 0.047 1.06 0.302 1.02 0.313 2.77 0.096 0.58 0.445
Matrix 9number of
forest patches
4.71 0.030 4.82 0.028 7.62 0.006 0.53 0.467 7.89 0.005
4.0 Matrix 4.04 0.044 2.42 0.120 1.17 0.280 7.08 0.008 0.31 0.576
Matrix 9forest amount 3.12 0.078 0.91 0.340 3.14 0.076 5.14 0.023 0.23 0.631
Matrix 9number of
forest patches
2.61 0.106 2.61 0.107 13.25 <0.001 0.00 0.968 4.99 0.025
5.0 Matrix 3.44 0.063 2.30 0.129 1.03 0.310 7.17 0.007 0.35 0.553
Matrix 9forest amount 1.18 0.277 1.49 0.222 6.07 0.014 3.82 0.051 0.72 0.397
Matrix 9number of
forest patches
1.48 0.224 1.19 0.274 5.21 0.022 0.08 0.778 4.28 0.039
Significant results in bold
Landscape Ecol
123
anthropogenic structures for roosting may be driving
the observed negative relationship of M. chiloensis
with forest amount in agricultural landscapes. Sur-
prisingly, the activity of L. varius was unaffected by
forest amount, even though this species has been
associated with forested habitats (Galaz and Ya
´n
˜ez
2006; Rodrı
´guez-San Pedro and Simonetti 2013a),
suggesting that even species exhibiting a definitive
association with a particular habitat type at the patch
level have a great deal of variation in activity among
landscapes that could not be explained by forest
amount alone. It is not surprising that activity of
T.brasiliensis and L. cinereus were not affected by
fragmentation. This is probably because high wing
loading and high wing aspect ratio, features charac-
teristic of species foraging in open space (Norberg and
Rayner 1987), confer high speeds that make visiting
isolated patches energetically cheap. On the other
hand, some forest bat species, such as H. montanus,
are adapted to slower and more maneuverable flights
because of their lower wing loading and lower aspect
ratio. Thus, this and similar species may not be able to
afford prolonged commuting flights over an inhos-
pitable matrix like an agricultural landscape to isolated
forest patches because such flights would be ener-
getically costly for them (Norberg and Rayner 1987).
Bat activity in our study was associated with forest
amount and fragmentation, however their effects
varied between agricultural and forestry dominated
landscapes. In accordance with other studies, forest
amount was a significant predictor of activity of most
species in agricultural landscapes (McGarigal and
McComb 1995; Villard et al. 1999; Klingbeil and
Willig 2009; Ethier and Fahrig 2011), but not in those
dominated by forest plantations where only one
species responded significantly to forest amount.
Forest plantations might represent a ‘‘soft’’ matrix
for the biota inhabiting native forest patches, as
exemplified by the willingness of some taxa to move
through tree plantations particularly when it has a
well-developed understory (Estades et al. 2012;
Simonetti et al. 2013). For example, in landscapes
where native forests have been replaced by exotic
forestry plantations, bats are able to use such lands for
commuting, foraging and roosting (Borkin and Par-
sons 2010a,b,2011). The exotic pine plantations,
might provide habitat for some species of forest-
dwelling bats such as H. montanus,L. cinereus,L.
varius and M. chiloesnis in central Chile (Rodrı
´guez-
San Pedro and Simonetti 2013a), and thus could
compensate for habitat loss.
Like bats in temperate forests of Canada and
tropical forests of Peru and subtropical Atlantic forest
of Paraguay (Gorresen and Willig 2004; Klingbeil and
Willig 2009; Ethier and Fahrig 2011), bat species in
Chile displayed scale-dependent responses to forest
amount and fragmentation. In agricultural landscapes,
bat activity for most species was strongly determined
by both forest amount and fragmentation at large
spatial scales. Although limited information is avail-
able on the movements and home range size of Chilean
bat species, these scales are larger than the average
maximum distance traveled by similar small and
medium-sized aerial insectivorous bats during forag-
ing activity elsewhere (Elmore et al. 2005; Sparks
et al. 2005; Walters et al. 2007; Henderson and
Broders 2008; Kniowski and Gehrt 2014). The fact
that bat activity was associated with forest amount and
fragmentation at scales larger than the home range of
individual bats suggests that local bat activity reflects a
number of factors operating at different scales
probably depending on species-specific behavioral or
life-history characteristics.
In contrast to agricultural landscapes, bat activity was
associated significantly with forest amount and/or
fragmentation at the smallest spatial scales in forested
landscapes suggesting that the type of matrix could
affect not only the direction and magnitude of forest
amount and fragmentation on bat activity, but also the
spatial scale at which their effects operate on species.
Landscapes dominated by an agricultural matrix, with
smaller and more distant suitable habitat patches, are
likely associated with bats needing long commuting
flights. Whereas bats associated with forested land-
scapes have shorter home ranges and, consequently,
may respond to shorter scales in a modified landscape
(Chaverri et al. 2007;Saı
¨detal.2009;Kniowskiand
Gehrt 2014). For example, the Indiana bat (Myotis
sodalis) home ranges within a highly agricultural
landscape are larger compared to other studies in
forested and rural–urban landscapes (Kniowski and
Gehrt 2014). Our results suggest that multiple-scale
assessment are necessary to adequately quantify the
effects of forest amount and fragmentation on mobile
species that inhabit complex landscapes where habitat
patches are difficult to define and thus, may be critical to
the success of management and conservation strategies
in human modified landscapes.
Landscape Ecol
123
This study reinforces that of Ethier and Fahrig
(2011), adding the role of matrix complexity to the
analysis of the independent role of habitat loss and
fragmentation and providing evidence that low contrast
matrices can mitigate the effects of forest loss. Our
results indicate that fragmented landscapes with many
embedded native forest patches surrounded by a low
contrast matrix such as pine plantation (albeit species
depauperate) may support a higher activity of insec-
tivorous bats than fragmented landscapes with an
agricultural matrix. The fact that landscapes with small
forest patches embedded in such production-forests can
mitigate the effects of forest loss, enhances the capacity
of many taxa, including bats, to persist in landscapes
modified by humans. Forestry plantations are an
important component of these landscapes. We recom-
mend that effective conservation efforts and manage-
ment strategies in anthropogenically altered landscapes
should aim to reduce the degree of patch-matrix contrast
in order to mitigate the impact of forest loss and improve
biodiversity conservation.
Acknowledgments We are grateful to L.F. Aguirre (PCMB)
for the loan of bat detectors. Special thanks to R. Zu
´n
˜iga and Y.
Cerda for their invaluable help with the fieldwork and D. Rojas
for his help with statistical analysis. We are also grateful to the
Coordinating Editor and two anonymous reviewers for valuable
comments that improved a previous version of the manuscript.
This research has been partially supported by FONDECYT
1095046 and Programa Domeyko-Biodiversidad (IT3),
Universidad de Chile. A. Rodrı
´guez-San Pedro was supported
by a doctoral fellowship from Comisio
´n Nacional de
Investigacio
´n Cientı
´fica y Tecnolo
´gica (CONICYT), Chile.
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... Indeed, aerial insectivorous bats, corresponding to 30-50% of local bat species assemblages , are known to exert key top-down control of many insect populations, including agricultural pests (Cleveland et al. 2006;Jones et al. 2009;Kalka et al. 2008;Kunz et al. 2011). Despite their pivotal functional role in tropical systems and their great vulnerability to habitat loss (Alroy 2017), our understanding of bat assemblage responses to landscape-scale changes is still largely limited to temperate regions (Ethier and Fahrig, 2011;Frey-Ehrenbold et al. 2013;Jantzen and Fenton 2013;Rodríguez-San Pedro and Simonetti 2015). In the Neotropics, most of the studies focus on leaf-nosed bats (Phyllostomidae), as they are readily captured by mist nets (Chambers et al. 2016;Gorresen et al. 2005;Klingbeil and Willig 2009;Muylaert et al. 2016;Pinto and Keitt 2008). ...
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Moonlight intensity influences the activity patterns of bats. Some bat species reduce their activity levels during brighter nights, a phenomenon known as “lunar phobia.” While lunar phobia of bats has been extensively studied in tropical regions, the same is not the case of bats in temperate regions. By using acoustic detectors, we examined differences in the activity of insectivorous bats on nights with different moonlight intensity in an agricultural landscape of central Chile. We also examined the hourly activity patterns throughout the night and how these varied between full and new moon nights. All bat species modified their activity based on the moonlight intensity; however, their effects were species-specific. The activity of Lasiurus varius, L. villosissimus, Myotis chiloensis, and Histiotus montanus was lower during bright nights, while Tadarida brasiliensis was the only species whose activity was higher during bright nights. Hourly activity throughout the night differed between full moon nights and new moon nights in most bat species. During full moon, bats concentrated their activities in the early hours of the nights; a more homogeneous activity pattern was exhibited during new moon night. Our study demonstrates that moonlight affects the activity of bats in Chile, a factor that should be considered when studying bats.
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Segunda Edición actualizada de los Murciélagos de Chile
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To assess habitat use by foraging bats in southern British Columbia, Canada, we used narrow band bat detectors and estimated insect availability with light-suction traps. We measured bat activity and insect availability in harvested forests at three spatial scales: habitat type (existing cutblocks, cutblock/forest edges, and undisturbed forest), stand age-class (four classes ranging between 80 and 250 years), and elevational zone (three zones ranging between 540 and 1800 m). In cutblock and edge habitat types, foraging activity paralleled insect availability, being greatest along edges. However, in the forest where insect availability was high we detected virtually no bat foraging activity. High foraging rates (foraging attempts/commuting passes) along edges indicated that bats foraged most efficiently in this habitat type. These results suggest that the spatial complexity of a habitat, in combination with insect availability, influences habitat use by foraging bats. There were no statistically significant differences in bat foraging activity or insect availability among the stand age-classes, but foraging activity by bats and insect availability decreased with increasing elevational zone. Our results suggest that the impact of forest harvesting on habitat use by foraging bats varies with spatial scale. Although edge habitat appears to be an important foraging habitat for some bats, the effects of forest fragmentation on bat populations or communities is currently unknown. Thus, the creation of edge habitat through forest harvesting cannot be considered a reasonable technique for managing bat populations.
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Full-text available
To assess habitat use by foraging bats in southern British Columbia, Canada, we used narrow band bat detectors and estimated insect availability with light-suction traps. We measured bat activity and insect availability in harvested forests at three spatial scales: habitat type (existing cutblocks, cutblock/forest edges, and undisturbed forest), stand age-class (four classes ranging between 80 and 250 years), and elevational zone (three zones ranging between 540 and 1800 m). In cutblock and edge habitat types, foraging activity paralleled insect availability, being greatest along edges. However, in the forest where insect availability was high we detected virtually no bat foraging activity. High foraging rates (foraging attempts/commuting passes) along edges indicated that bats foraged most efficiently in this habitat type. These results suggest that the spatial complexity of a habitat, in combination with insect availability, influences habitat use by foraging bats. There were no statistically significant differences in bat foraging activity or insect availability among the stand age-classes, but foraging activity by bats and insect availability decreased with increasing elevational zone. Our results suggest that the impact of forest harvesting on habitat use by foraging bats varies with spatial scale. Although edge habitat appears to be an important foraging habitat for some bats, the effects of forest fragmentation on bat populations or communities is currently unknown. Thus, the creation of edge habitat through forest harvesting cannot be considered a reasonable technique for managing bat populations.
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Although bats are often thought of as cave dwellers, many species depend on forests for all or part of the year. Of the 45 species of bats in North America, more than half depend on forests, using the bark of trees, tree cavities, or canopy foliage as roosting sites. Over the past two decades it has become increasingly clear that bat conservation and management are strongly linked to the health of forests within their range. Initially driven by concern for endangered species-the Indiana bat, for example-forest ecologists, timber managers, government agencies, and conservation organizations have been altering management plans and silvicultural practices to better accommodate bat species. Bats in Forests presents the work of a variety of experts who address many aspects of the ecology and conservation of bats. The chapter authors describe bat behavior, including the selection of roosts, foraging patterns, and seasonal migration as they relate to forests. They also discuss forest management and its influence on bat habitat. Both public lands and privately owned forests are considered, as well as techniques for monitoring bat populations and activity. The important role bats play in the ecology of forests-from control of insects to nutrient recycling-is revealed by a number of authors. Bat ecologists, bat conservationists, forest ecologists, and forest managers will find in this book an indispensable synthesis of the topics that concern them. © 2007 by The Johns Hopkins University Press. All rights reserved.
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Use of bat detectors to perform inventories, determine activity, and assess differential use of habitats has become a generally accepted method. However, there has been vigorous disagreement as to the level of efficacy, primarily relating to the ability to distinguish certain species and groups of species. The primary explanation suggested for the inability to identify certain species is due to the magnitude of intraspecific variation resulting in overlap among species, presumably compounded by geographic variation. Lasiurus cinereus has been identified as exhibiting the greatest degree of geographic variation including recent findings of distinct variation between populations in Hawaii and Manitoba. We find that claims of geographic variation have not been proven because of small sample size and lack of adequate description of method, including the behavior of the bat and the context during which bats were recorded. Previous geographical comparisons of species have relied on standard statistical methods that do not allow a comprehensive examination of the range in variation of diagnostic call parameters. We present data from a broad range of sites throughout mainland United States and Hawaii, and compare a multivariate statistical approach with repertoire plots of characteristic frequency versus call duration. Although we demonstrated a statistical finding of geographic variation in L. cinereus, small sample size, context, and behavior could not be discounted as the proximal cause of observed variation. The perceived variation across the geographic range that we sampled did not affect our ability to identify the species by call structure. We suggest methods for future studies of geographic variation.