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RESEARCH ARTICLE
Patterns of brown bear damages on apiaries
and management recommendations in the
Cantabrian Mountains, Spain
Javier NavesID
1
*, Andre
´s Ordiz
2
, Alberto Ferna
´ndez-Gil
1
, Vincenzo Penteriani
3,4
, Marı
´a
del Mar Delgado
3
, Jose
´Vicente Lo
´pez-Bao
3
, Eloy Revilla
1
, Miguel Delibes
1
1Department of Conservation Biology, Estacio
´n Biolo
´gica de Doñana, Seville, Spain, 2Faculty of
Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, Ås,
Norway, 3Research Unit of Biodiversity (UMIB, UO-CSIC-PA), Oviedo University—Campus Mieres, Mieres,
Spain, 4Pyrenean Institute of Ecology (IPE), CSIC, Zaragoza, Spain
*jnaves@ebd.csic.es
Abstract
Large carnivores are often persecuted due to conflict with human activities, making their
conservation in human-modified landscapes very challenging. Conflict-related scenarios
are increasing worldwide, due to the expansion of human activities or to the recovery of car-
nivore populations. In general, brown bears Ursus arctos avoid humans and their settle-
ments, but they may use some areas close to people or human infrastructures. Bear
damages in human-modified landscapes may be related to the availability of food resources
of human origin, such as beehives. However, the association of damage events with factors
that may predispose bears to cause damages has rarely been investigated. We investigated
bear damages to apiaries in the Cantabrian Mountains (Spain), an area with relatively high
density of bears. We included spatial, temporal and environmental factors and damage pre-
vention measures in our analyses, as factors that may influence the occurrence and inten-
sity of damages. In 2006–2008, we located 61 apiaries, which included 435 beehives
damaged in the study area (346 km
2
). The probability of an apiary being attacked was posi-
tively related to both the intensity of the damage suffered the year before and the distance to
the nearest damaged apiary, and negatively related to the number of prevention measures
employed as well as the intensity of the damage suffered by the nearest damage apiary.
The intensity of damage to apiaries was positively related to the size of the apiary and to
vegetation cover in the surroundings, and negatively related to the number of human settle-
ments. Minimizing the occurrence of bear damages to apiaries seems feasible by applying
and maintaining proper prevention measures, especially before an attack occurs and select-
ing appropriate locations for beehives (e.g. away from forest areas). This applies to areas
currently occupied by bears, and to neighbouring areas where dispersing individuals may
expand their range.
PLOS ONE | https://doi.org/10.1371/journal.pone.0206733 November 28, 2018 1 / 18
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OPEN ACCESS
Citation: Naves J, Ordiz A, Ferna
´ndez-Gil A,
Penteriani V, Delgado MdM, Lo
´pez-Bao JV, et al.
(2018) Patterns of brown bear damages on
apiaries and management recommendations in the
Cantabrian Mountains, Spain. PLoS ONE 13(11):
e0206733. https://doi.org/10.1371/journal.
pone.0206733
Editor: Carlo Meloro, Liverpool John Moores
University, UNITED KINGDOM
Received: October 18, 2017
Accepted: October 18, 2018
Published: November 28, 2018
Copyright: ©2018 Naves et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This work received support from Agencia
Estatal de Investigacio
´n from the Ministry of
Economy, Industry and Competitiveness, Spain.
Project CGL2017-83045-R AEI/FEDER EU, Dr Eloy
Revilla; Agencia Estatal de Investigacio
´n from the
Ministry of Economy, Industry and
Competitiveness, Spain. Project CGL2017-82782-P
Introduction
The trade-off between species conservation and the management of human-wildlife conflicts
is central to conservation biology [1,2]. Damages and risks caused by wildlife can be of emo-
tional and economic importance, thus generating conflict and persecution by people [3]. This
is especially true for large carnivores, whose conservation in human-dominated landscapes is
increasingly challenging [4,5,6].
The occurrence of large carnivores near human settlements and infrastructures is fre-
quently perceived as problematic because these animals can attack livestock and pets as well as
damage crops and, although attacks on humans are very rare, especially in Europe [7], people
can fear them [8]. Conflict-related scenarios are increasing particularly where large carnivore
populations are re-occupying areas and habitats lost during the last few centuries, as well as
where human activities are expanding [9,10,11]. In such scenarios, collecting baseline infor-
mation on human-wildlife interactions is an essential step to delineate effective conflict mitiga-
tion strategies [9,12,13,14].
Interactions between large carnivores and human activities are receiving increasing atten-
tion, and brown bears Ursus arctos are no exception. Bears generally avoid humans and their
settlements, but some individuals use areas closer to people or anthropogenic infrastructures
even if this behaviour is not always linked to food availability [15]. Nevertheless, the occur-
rence of bear damages in human-modified landscapes implies that anthropogenic food
resources, such as beehives or livestock, are available [9,16]. Yet, the association of damages
with factors that predispose bears to such predation events have been rarely investigated (e.g.
[17,18,19,20]).
Beehives have long been present throughout most of the brown bear range in Eurasia and
North America, and patterns of bear damages are heterogeneous [12,19,21,22,23,24]. There-
fore, understanding how different factors can influence predation patterns should help design
appropriate measures to prevent and mitigate bear damages.
Due to habitat encroachment or reduction of bear habitats and chronic bear damages to
human property, the isolated and critically endangered population of brown bears in the Can-
tabrian Mountains (Spain) provides the opportunity to investigate the factors related to bear-
human conflict in this study area and elsewhere in Europe (Fig 1; [25,26,27]). The conflict
scenario related to damages and the conservation of this bear population has been the subject
of recent analyses [28], and this brown bear population has showed the highest rate of apiary
(i.e., an aggregation of beehives spread over a given area) damages per bear in Europe [12].
Therefore, mitigating bear damages seems essential to promote bear-human coexistence and
bear recovery in this area.
Our aim was to identify spatial and temporal correlates of bear damages to apiaries. In addi-
tion, we tried to identify environmental factors and prevention measures that may explain the
occurrence and intensity of damages. We expected that the probability that a given apiary is
damaged may be higher near to a damaged apiary and if the damage intensity to the latter is
high. We therefore assumed that once a bear has obtained a positive reward (food), it may be
prone to search for other apiaries nearby. We also expected that damage intensity to apiaries
would vary over the years because of yearly co-occurrence of other factors such as the availabil-
ity of food resources, spatial distribution of bears, or their space use and differential habitat
selection. Furthermore, we expected that the probability that an apiary is damaged may depend
on whether it has been damaged the year before and the intensity of the damage during the
same year. We also considered a set of variables related to the characteristics (e.g., number of
beehives, presence of damage prevention measures, including electric and/or traditional stone-
walls, see Fig 2) and other local environmental correlates (such as vegetation cover, roads and
Brown bear damages on apiaries
PLOS ONE | https://doi.org/10.1371/journal.pone.0206733 November 28, 2018 2 / 18
AEI/FEDER EU, Dr Vincenzo Penteriani; Regional
Government of Asturias. 2007-2010 Project:
Demographic evolution of the brown bear
population, identification of corridors of
communication between subpopulations and
analysis of the damages caused by the species to
agriculture and livestock in Asturias Ref. Pres. PA
2007:, 18.07-443F-610.000, Dr Miguel Delibes;
Ramon & Cajal research contract, Agencia Estatal
de Investigacio
´n from the Ministry of Economy,
Industry and Competitiveness, Spain. RYC-2014-
16263, Dr Marı
´a del Mar Delgado; Ramon & Cajal
research contract, Agencia Estatal de Investigacio
´n
from the Ministry of Economy, Industry and
Competitiveness, Spain. RYC-2015-18932; project
CGL2017-87528-R AEI/FEDER EU, Dr Jose
´Vicente
Lo
´pez-Bao. The funders had no role in study
design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
human settlements) of the apiaries. We expected that apiaries with implemented preventive
measures would have a lower probability of been damaged than unprotected ones, whereas
denser vegetation cover in the proximity of apiaries would increase the probability of damages,
because approaching the apiary would be less risky for bears. Finally, we expected that human
Fig 1. Location of the study area (346 km
2
; in light grey) within the current distribution of the brown bear in the Cantabrian Mountains (dark grey;
according to Naves et al. 2003 [30]). Coordinates of centroid to the study area: 43
o
0.370’ N, 6
o
38.534’ W.
https://doi.org/10.1371/journal.pone.0206733.g001
Brown bear damages on apiaries
PLOS ONE | https://doi.org/10.1371/journal.pone.0206733 November 28, 2018 3 / 18
infrastructures around apiaries would deter bears from approaching and eventually using api-
aries, because risk exposure for bears may be directly related to human activities [15,29].
Methods
The study area and the Cantabrian brown bear population
The Cantabrian Mountains are parallel to the Atlantic coast (Cantabrian Sea) of NW Spain.
Mean tree species are beech Fagus sylvatica, oak Quercus spp., birch Betula alba and chestnut
Castanea sativa. Beech and birch dominate in north face slopes and higher altitudes, over 600–
700 m, whereas oak and chestnut are more abundant in south faces slopes and lower altitudes.
Forests are interspersed with pasturelands and shrubs of broom Cytisus spp., Genista spp.,
heather Erica spp., Calluna vulgaris, and bilberry Vaccinium myrtillus, the latter usually domi-
nating montane and subalpine levels (ca. 1,000–1,700 m a.s.l.; more details in [30,31]).
Brown bears are distributed in two connected subpopulations [32], occupying ca. 7000
km
2
, with above 200 individuals in the western subpopulation (CI95% = 168–260 individuals)
Fig 2. In the Cantabrian Mountains, apiaries have traditionally been protected by stonewalls called ‘cortines’ or ‘albarizas’ (a; picture: J. Naves). In recent times,
the use of this ancient and traditional prevention method to deter bears has been lost in many areas; although some apiaries still have rock walls, several of them only use
electric fences (b; picture: J. Naves) or combine both approaches (c; picture: A. Ordiz). Picture d (picture: A. Ramos, Principado de Asturias) shows the incursion of a
brown bear in an apiary in the study area.
https://doi.org/10.1371/journal.pone.0206733.g002
Brown bear damages on apiaries
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and 20 in the eastern subpopulation (CI95% = 12–40 individuals; [26]). In particular, we
focused our analyses on a 346 km
2
area located in the western Cantabrian Mountains (south-
western Asturias), including the municipalities of Cangas de Narcea, Ibias, and Degaña, with
an elevation range between 450 and 1850 m a.s.l. (Fig 1). This study area includes portions of
the Cantabrian Mountains with the highest bear densities, but also some peripheral areas (Fig
1). Among other economic activities such as livestock herding and mining, beekeeping in
fixed apiaries is an important traditional activity in this area.
Apiaries in the study area and environmental attributes
We used the official database of bear damage claims from the Regional Government of Astu-
rias. The database is annual and for each claim, it includes: personal data of the claimer and
the ranger that visited the place, county, record number, parish, village, Julian date, adminis-
trative situation and geographical coordinates, amount of money compensated, damaged spe-
cies, and number of beehives attacked. We selected all the claims of bear damages that
occurred in the study area between 2006 and 2008, and we visited all of the damaged beehives
in the field in June and July 2009 to characterize them, e.g., to determine if they had protective
measures and their type, and to collect environmental information on the surroundings of the
apiaries. Additionally, we actively searched for additional apiaries in the study area, through
direct observations and surveys. These apiaries were not included in the official dataset of bear
damages, thus we considered them as the reference dataset of non-damaged apiaries.
In each of the visited apiaries, we collected information on several parameters (Table 1). At
the apiary level, we recorded the number of beehives and the presence of damage prevention
methods: electric fences, wire mesh fence and/or with stone walls, known as ‘cortines’ or
‘albarizas’, which are traditional constructions used to prevent the access of bears to beehives
(Fig 2). We also compiled information on different environmental attributes that may influ-
ence the vulnerability of apiaries to bear attacks. Environmental attributes were recorded at
three different spatial scales, within a 30, 500 and 2000 m radius around the apiaries. At the 30
m scale, we visually estimated vegetation cover as both the percentage of scrubland (bushy veg-
etation mainly composed by heathers and brooms, over 1 m in height), percentage of forest,
and percentage cover of human infrastructures (buildings and paved and unpaved roads).
Finally, we extracted the vegetation cover, number of settlements, and length of paved and
unpaved roads within 500 and 2000 m radius plots around the central beehive of each apiary,
using GIS layers from Cartografı
´a Tema
´tica Ambiental of the Principado de Asturias (Hojas
del Mapa de Vegetacio
´n, Litologı
´a, Roquedos y Ha
´bitat del Oso. Escala 1:25000. Principado de
Asturias, Spain).
Data analysis
We built binomial or negative binomial Generalized Linear Mixed Models (GLMM) to test
how different environmental factors, apiary features and spatial and temporal (yearly) patterns
affect the probability of damage to an apiary and, in case of damage, the number of beehives
attacked (damage intensity). First, we tested for the effects of spatial proximity and intensity of
damage in the nearest neighbouring apiary on the probability of an apiary being damaged. For
this analysis, we used the data from 2006 to 2008. Second, we considered the variables retained
in the previous step, to test whether or not the apiary had been damaged the year before (tem-
poral factor) and the intensity of that damage. For this analysis, we used the data from 2007
and 2008. Third, we added the environmental variables and apiary features to analyse their
potential effect on the probability of an apiary being damaged and on the intensity of the
Brown bear damages on apiaries
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damage. Because the latter analyses also included temporal predictors, we used again the data
from the last two years of our study (2007–2008).
We considered the following characteristics of the apiary and its environment at different
spatial scales: number of beehives and presence and number of prevention measures; distance
to the nearest damaged apiary and its damage intensity; whether a given apiary had been dam-
aged or not the previous year and the number of damaged beehives; percentage cover of scrub-
land, forest and human settlements (including infrastructures) within a 30 m around the
apiary; forest cover, number of human settlements and length (in km) of infrastructures within
a 500 and 2000 m around the apiary (Table 1). We included apiary identification and year (in
the spatial model) as random factors. We tested for collinearity among variables and model
selection was based on Akaike Information Criterion corrected for small sample sizes (AICc;
[33]). We run all potential models with the potential combinations of explanatory variables in
each of the analyses, i.e., the spatial analysis, the spatial and temporal analyses and, finally, the
analyses including spatial, temporal and environmental and apiary-related factors. Model aver-
aging was carried out only for those models with ΔAICc <2 to calculate parameter coefficients
and the relative importance values (RIV) of each explanatory variable [33]. Parameter
Table 1. Variables recorded in the study of brown bear damages to apiaries in the Cantabrian Mountains, Spain.
Variables Description Values / Units
1. Response variables
Probability of bear damage Apiary damaged / not damaged by bears in a given year binomial (0,1)
Intensity of bear damage Number of damaged beehives (>0) in a damaged apiary in a given year count (1,2, . . .N)
2. Predictors
Effects of spatial closeness/damage intensity of neighbour apiaries on damaged apiaries
Distance nearest Distance to the nearest damaged apiary in a given year km
Intensity nearest Number of damaged beehives (>0) in the nearest damaged apiary in a given year count (1,2, . . .N)
Yearly patterns in damaged apiaries
Probability-1 Apiary damaged / not damaged the year before binomial (0,1)
Intensity-1 Number of damaged beehives the year before count (0,1,2, . . .N)
Year Specific year of the study period (2006, 2007 or 2008) categorical
Apiary features
Prevention Presence / absence of prevention measures (electric fences, wire mesh fence, stone walls) binomial (0,1)
N_prevention Combined number of apiary prevention measures count (0,1,2,3)
N_beehives Number of beehives in the apiary count (1,2, . . .N)
Landscape attributes surrounding the apiary
Forest_30 Percentage of forest cover within a 30 m radius area around the apiary %
Scrub_30 Percentage of scrub (vegetation >1 m in height) cover within a 30 m radius area around the apiary %
Human_30 Percentage of human settlements within a 30 m radius area around the apiary %
Forest_500 Forest cover within a 500 m radius area around the apiary ha
Forest_2000 Forest cover within a 2000 m radius area around the apiary ha
Infrastructures_500 Length of paved and unpaved roads within a 500 m radius area around the apiary km
Infrastructures_2000 Length of paved and unpaved roads within a 2000 m radius area around the apiary km
N_settlements_500 Number of inhabited human settlements within a 500 m radius area around the apiary count (1,2, . . .N)
N_settlements_2000 Number of inhabited human settlements within a 2000 m radius area around the apiary count (1,2, . . .N)
3. Random factors
ID Identification code of each apiary categorical
Year Specific year of the study period (2006, 2007 or 2008) categorical
https://doi.org/10.1371/journal.pone.0206733.t001
Brown bear damages on apiaries
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estimates from model averaging derives from weighted averages of these values across all of
the considered models [34]. The relative importance value (RIV) of each explanatory variable
was estimated by summing Akaike weights across all models that contain the variable [33]. All
statistical analyses were performed in R 3.0.2 [35] using lme4 [36] and MuMIn [37] packages.
This study did not require ethics permission under European and Spanish legislation. Per-
mission for fieldwork was granted by Resolution of the General Direction of Biodiversity and
Landscape (Department of Environment and Rural Development; Ref. Pres. PA 2007: 18.07-
443F-610.000). Apiaries were located in communal and public lands, with no specific require-
ment for visit permissions.
Results
Between 2006 and 2008, 2,269 beehives were damaged by brown bears in the western Can-
tabrian Mountains. A total of 489 damaged beehives included in 65 apiaries were reported
in our study area (346 km
2
), out of which we were able to identify the exact location of 435
beehives (88.9%) in 61 apiaries (Table 2,Fig 3). Four apiaries were not found during field-
work in the recorded geographic coordinates, suggesting that those apiaries were removed
from the locations where they were damaged before fieldwork was conducted. Full data
set in S1 Table.
The mean number of beehives damaged per apiary and year in these 61 apiaries was 5.1
(range 1–33; Fig 3; see annual intensity of bear damages in Table 2). During 2008, the last year
of our study, bears damaged an average of 26.8% (SD = 27.0) of the beehives that were inside
the studied apiaries. Forty-three out of the 61 apiaries (70.5%) were damaged only one year,
whereas 12 and 6 apiaries were damaged in two and three years, respectively.
Model averaging of the analysis including spatial factors retained the two variables initially
considered: the spatial proximity (distance) and the damage intensity on the nearest damaged
apiary on the probability of an apiary being damaged (Table 3). Likewise, the analysis adding
temporal factors retained the three included variables, i.e., the spatial predictors, the damage
intensity of the focal apiary the year before, and the year effect (Table 3). Finally, we added pre-
dictors describing environmental factors and apiary features to analyse the overall probability
of damage and damage intensity. The most comprehensive model (Table 4) indicated that the
probability of an apiary being damaged in a given year was positively related to the intensity of
the damage it suffered the year before, i.e., not only if it had been attacked, which suggests a
pattern of temporal (annual) autocorrelation in damage occurrence. Against our prediction,
the probability of damage was also positively related to the distance to the nearest damaged
apiary, i.e., the farther the neighbouring damaged apiary, the higher the probability of an api-
ary being damaged. The probability of damage was negatively related to the number of preven-
tion measures and the intensity of the damage suffered by the nearest damaged apiary (Fig 4).
Both the spatial and the temporal components were significant and showed high RIV values
(RIV = 0.83 and 0.78, respectively; Table 4).
Overall, forty-seven percent of apiaries had stonewalls, 37% had electric fences, and 16%
had a wire mesh fence or other prevention measure. The proportion of apiaries without pre-
vention measures, or with one, two and three measures was 23%, 44%, 27% and 6%, respec-
tively (Table 2). The number of prevention measures significantly reduced the probability of
the apiary being damaged (RIV = 0.94; Table 4). The number of human settlements within a
500 m radius area around the apiary was positively correlated with the probability of the apiary
to be damaged (RIV = 0.84; Table 4). However presence of human infrastructure (i.e., paved
and unpaved roads) within a 2,000 m radius area had a negative relation with the probability
of damage (RIV = 0.70; Table 4).
Brown bear damages on apiaries
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Finally, the intensity of bear damages to apiaries was positively related to the number of
beehives in the apiary and to forest cover in the 2000 m around the apiary. The intensity of
damage was negatively influenced by the presence of human settlements around the apiary
(RIV>0.70 for all of these variables; Table 4,Fig 4).
We were able to visit in the field 44 of the 61 damaged apiaries, plus 20 other apiaries not
damaged by bears in 2006–2008, according to the official dataset on bear damages. Environ-
mental attributes, measured at 500 and 2000 m radius around the apiaries, did not differ
between visited (n = 44) and not visited apiaries (n = 17) (U Mann-Whitney tests, all P>0.1).
Therefore, we assumed that the set of apiaries considered in this study was representative of
the apiaries damaged by bears in the area.
Table 2. Descriptive statistics of the main variables recorded in the study.
Variables Values for damaged
apiaries
Mean ±SD (range) (N)
Values for undamaged
apiaries
Mean ±SD (range) (N)
N total
Number / Intensity of bear damages
(year = 2006)
6.7 ±7.9 (1–33) (N = 26) - (N = 55) 81
Number / Intensity of bear damages
(year = 2007)
4.5 ±4.8 (1–25) (N = 33) - (N = 48) 81
Number / Intensity of bear damages
(year = 2008)
4.3 ±3.7 (1–13) (N = 26) - (N = 55) 81
Predictors
1. Effects of spatial closeness/damage intensity of neighbour apiaries on
damaged apiaries
Distance nearest (year = 2006; km) 1.0 ±1.3 (0.0–5.8) 1.6 ±1.3 (0.0–5.9) 81
Distance nearest (year = 2007; km) 1.0 ±1.3 (0.0–5.9) 1.0 ±1.0 (0.0–4.3) 81
Distance nearest (year = 2008; km) 1.1 ±1.2 (0.0–4.1) 1.5 ±1.6 (0.0–6.7) 81
Intensity nearest (year = 2006) 7.0 ±8.1 (1–33) 4.4 ±4.5 (1–26) 81
Intensity nearest (year = 2007) 4.9 ±4.8 (1–25) 5.7 ±5.2 (1–25) 81
Intensity nearest (year = 2008) 4.7 ±3.9 (1–13) 5.0 ±3.4 (1–13) 81
2. Effects of damage intensity the year before on damaged apiaries
N_apiaries damaged year before (year = 2007) 13 (N = 33) 13 (N = 48) 81
N_apiaries damaged year before (year = 2008) 11 (N = 26) 22 (N = 55) 81
Number / Intensity -1 (year = 2007) 3.58 ±7.72 (0–33) 1.17 ±2.55 (0–12) 81
Number / Intensity-1 (year = 2008) 2.19 ±3.74 (0–13) 1.67 ±3.83 (0–25) 81
3. Apiary features and landscape attributes surrounding the apiary
N_apiaries with prevention measures 33 (N = 44) 15 (N = 20) 64
N_prevention 1.1 ±0.8 (0–3) 1.4 ±0.9 (0–3) 64
N_beehives 20.3 ±16.9 (1–70) 18.7 ±23.8 (1–90) 64
Forest_30 (%) 29.5 ±25.1 (0.0–90.0) 34.8 ±24.3 (0.0–90.0) 64
Scrub_30 (%) 39.5 ±30.8 (5.0–100.0) 37.6 ±23.6 (5.0–90.0) 64
Human_30 (%) 6.8 ±15.6 (0.0–50.0) 4.5 ±11.6 (0.0–65.0) 64
Forest_500 (ha) 19.6 ±13.6 (3.9–46.4) 20.8 ±14.5 (1.4–56.4) 64
Forest_2000 (ha) 337.0 ±192.4 (110.0–
746.4)
420.0 ±214.2 (140.7–943.7) 64
Infrastructures_500 (km) 0.6 ±0.8 (0.0–3.0) 0.6 ±0.8 (0.0–3.0) 64
Infrastructures_2000 (km) 3.1 ±2.7 (0.0–12.0) 3.1 ±2.2 (0.0–8.0) 64
N_settlements_500 1.5 ±1.0 (0.0–4.2) 1.8 ±1.0 (0.0–4.5) 64
N_settlements_2000 15.3 ±6.4 (7.6–29.8) 17.8 ±6.0 (7.8–27.4) 64
https://doi.org/10.1371/journal.pone.0206733.t002
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Discussion
Our findings suggest that the patterns of bear depredation on apiaries in the Cantabrian
Mountains is modulated by complex relations among different factors, including the yearly
recurrence and spatial patterns of attacks, the influence of different characteristics of the
Fig 3. Locations of damaged and undamaged apiaries in the study area in 2006–2008. For damaged apiaries, the number of damaged beehives is also
shown.
https://doi.org/10.1371/journal.pone.0206733.g003
Table 3. Model-averaged coefficients and relative importance values (RIV) for the variables included in the selected models to analyze the probability of damage on
apiaries by brown bears, and the intensity of damage, in the Cantabrian Mountains, Spain. The selected models with ΔAICc<2 that we used for model averaging can
be seen in S2 Table. The first model only included spatial variables, and the second model included spatial and temporal variables. In the second model, analyses were
restricted to 2007 and 2008 to be able to include variables describing damages in the previous year.
Effects of spatial proximity and damage intensity of neighbouring apiaries on the probability that an apiary is damaged
(binomial function; ID and Year as random factor; n = 243)
explanatory variables βSE pRIV
(Intercept) -0.6659 0.1680 0.0001
Distance nearest -0.3622 0.1620 0.0253 1.00
Intensity nearest 0.0119 0.0277 0.6670 0.28
Effects of spatial proximity and damage intensity of neighbouring apiaries, and intensity of damages the year before, on the probability that an apiary is
damaged
(binomial function; ID as random factor; n = 162)
explanatory variables βSE pRIV
(Intercept) -0.5815 0.2636 0.0274
Intensity-1 0.0735 0.0394 0.0624 0.89
Year (2008) -0.3704 0.3357 0.2698 0.28
Intensity nearest -0.0432 0.0416 0.2984 0.28
Distance nearest 0.1784 0.1648 0.2790 0.17
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apiaries (e.g., the number of preventive measures and the number of beehives per apiary), and
the environmental characteristics around the apiaries. Different studies have evaluated how
different factors impact on the probability and intensity of depredations by large carnivores
(see [38,39] and references therein), but fewer of them have analysed the role of multiple fac-
tors of diverse nature [18], particularly for bears [24].
The probability of an apiary being damaged by brown bears in a given year was positively
related to the intensity of damages suffered by the same apiary the year before, yet the proba-
bility of damage was lower if the apiary was protected by multiple preventive measures (Fig 4).
Nevertheless, the effectiveness of protecting a previously attacked apiary is limited, especially
when the attack was intense (Fig 4A). For instance, an unfenced apiary where five beehives
were damaged the year before has an attack probability of 0.25 in a given year. However if the
attack the previous year damaged 25 beehives, the probability of damage in the focus year
increases to 0.69. The installation of a prevention measure decreases this probability to 0.58,
and three prevention measures would reduce that probability to 0.33. Our results indicate that
it is much more effective to protect the apiaries before an attack occurs, substantially reducing
later risks, and reinforce that using several preventive measures is important to prevent dam-
ages [40].
In our study area, as in many other places in Europe, there is no obligation to adopt preven-
tive measures, even for claiming compensations for bear damages on apiaries. Then, the ten-
dency of bears to prey on beehives, the difficulty of preventing attacks in some cases, and the
Table 4. Model-averaged coefficients and relative importance values (RIV) for the variables included in the selected models to analyze the probability of damage on
apiaries by brown bears, and the intensity of damage, in the Cantabrian Mountains, Spain. This model included spatial-, temporal-, environmental-, and apiary-related
factors. See S2 Table for further information on the different variables and the selected models with ΔAICc<2 that we used for model averaging). This analysis was
restricted to visited apiaries and to 2007 and 2008, to be able to include variables describing damages in the previous year.
Probability that an apiary is damaged
(binomial function; ID as random factor; N = 128)
explanatory variables βSE pRIV
(Intercept) -0.392 0.887 0.659
Intensity-1 0.097 0.048 0.042 1.00
N_prevention -0.512 0.257 0.046 0.94
N_settlements_500 0.716 0.362 0.048 0.84
Distance nearest 0.443 0.230 0.054 0.83
Intensity nearest -0.123 0.069 0.076 0.78
Infrastructures_2000 -0.476 0.251 0.059 0.70
Year [2008] -0.686 0.447 0.125 0.44
Human_30 0.030 0.019 0.127 0.42
Scrub_30 -0.013 0.010 0.203 0.18
Forest_2000 -0.345 0.273 0.206 0.09
Forest_500 0.176 0.238 0.459 0.03
Intensity of bear damage
(negative binomial function; ID as random factor; N = 49)
explanatory variables βSE pRIV
(Intercept) 1.099 0.339 0.001
N_beehives 0.212 0.074 0.004 1.00
Forest_2000 0.374 0.153 0.015 0.87
N_settlements_500 -0.391 0.182 0.031 0.77
Intensity-1 0.027 0.017 0.102 0.45
N_prevention -0.255 0.159 0.108 0.36
Forest_500 0.247 0.104 0.017 0.13
https://doi.org/10.1371/journal.pone.0206733.t004
Brown bear damages on apiaries
PLOS ONE | https://doi.org/10.1371/journal.pone.0206733 November 28, 2018 10 / 18
positive rewards following a bear intrusion into an apiary could help explain why the probabil-
ity of an apiary being damaged was positively related to the intensity of damage suffered the
year before. Previous results from this study area showed that most of the damages were caused
by male bears [41], whose relatively stable home ranges [42] may help explain why some apiar-
ies were repeatedly damaged over time.
The probability of damage was positively related with the number of settlements in a 500 m
radius and negatively with the density of roads in a 2000 m radius (Table 4), which likely
reflects that beehives are often close to remote and isolated inhabited human settlements, gen-
erally inclusive of just a few constructions. The probability of damage increased with distance
to the closest damaged beehive and was lower with higher intensity of damage in the closest
beehive, suggesting that an attacked beehive prevented damages to the neighbouring ones.
Likewise, a recent study [43] found that a reduction in the intensity of wolf (Canis lupus) dep-
redations in a given site, in response to lethal management, was related to an increase in the
surrounding area. Finally, the observed inter-annual variation in damage probability suggests
that yearly variation, e.g., in the availability of natural food resources [44] and/or variation in
habitat use by bears, with potential individual variation across bears and years, may have an
effect on the probability of bear damage in a given year [41,45,46].
Damage intensity was higher for larger apiaries and with more forest cover in the immedi-
ate proximity (within 500 and 2000 m radius), whereas it was lower if there were more settle-
ments in the surroundings (Table 4). However, the intensity of the damage was proportionally
greater in the smaller apiaries (Fig 4B). For example, apiaries of 60 and 30 beehives surrounded
by forest (400 ha in 2000 m radius) would suffer an intensity of attack that would affect,
approximately, 8 and 4 beehives respectively (13% of the total number of beehives). However,
an apiary of 10 beehives would have 3 beehives damaged, i.e., 30% of the total. This might be
due to a satiation effect of the bear visiting the apiary. Therefore, bears use beehives near
remote settlements, i.e., the probability of damage was positively affected by number of settle-
ments in the surroundings, but bears made a less intense use of damaged beehives in those
areas when these apiaries were surrounded by more settlements. Most intense damage
occurred in areas with higher vegetation cover and lower human presence. Human presence
influences the distribution and activity patterns of many carnivore species [47,48,49,50], and
the relationship between vegetation cover and bear damage occurrence reinforces the impor-
tance of protective cover for bears and other large carnivores in human-modified landscapes
[51,52]. Within their home ranges, brown bears use areas that minimize human-caused dis-
turbance, both in terms of movement patterns [29,53] and resting behaviour, i.e., selecting the
most concealed resting sites when bears are close to human settlements [51]. Vegetation cover
is indeed an important factor that favours large carnivore persistence, but it also favors dam-
ages by carnivores to human property in human-dominated landscapes. This finding applies
for several species of canids, felids, and bears in different continents (e.g. [18,24,54,55,56]).
Conservation and management implications
We documented that the use of damage prevention measures as traditional stonewalls and/or
electric fences (see Fig 2) was associated to low occurrences of damages, especially when differ-
ent prevention measures were used in combination (Table 4). The application of prevention
Fig 4. Relationship between (a) the probability of bear damage to an apiary and the number of damaged beehives in the apiary in the previous
year and, (b) the intensity of the attack, defined by the number of damaged beehives, and forest cover within a 2000 m radius. Plots are based on
the model-averaged parameters (Table 4) that explained the probability and intensity of damage to apiaries by brown bears in the Cantabrian
Mountains, Spain. Other variables not represented here were fixed to their mean values and for the year 2007.
https://doi.org/10.1371/journal.pone.0206733.g004
Brown bear damages on apiaries
PLOS ONE | https://doi.org/10.1371/journal.pone.0206733 November 28, 2018 12 / 18
measures reduced both the probability of bear damage and, to a lower extent, the intensity of
the damages (Table 4,Fig 4). Therefore, the implementation of damage preventions measures
is a straightforward recommendation to reduce bear damages, especially in the new apiaries,
before the bears have preyed on them and thus have a tendency to repeat the attack later, even
if preventive measures are used. Furthermore, remote forested sites should be avoided as loca-
tions for beehives, to minimize bear damages. We also showed that an attacked apiary pre-
vented damages to the closest ones. Then, according to other studies [43], it is possible that the
reduction of attacks in an apiary can increase attacks in a neighbour one.
Application of prevention measures to reduce the impact of carnivores on human property
is indeed a well-established, worldwide management recommendation (e.g. [1,18,56]). Elec-
trified fences have been suggested as effective tools to reduce bear damages to apiaries [17,19,
20,40,57,58]. These results and management implications can be extrapolated to the whole
Cantabrian area because, (a) our results agree with previous studies carried out in the Canta-
brian range [40] and, (b) the relatively large amount of apiaries visited in this study make it
representative. In the Department of Rural Development of the Regional Government of Astu-
rias, the official dataset of 2017 registered 90 apiaries in the study area. We located 81 of those
apiaries, and 4 that had not even been registered, which illustrates the representativeness of
our study.
Increasing available funding to subsidise the cost of installing electric fences around bee-
hives and to maintain them over time would reduce the number of bear depredations on apiar-
ies and the budgetary investment by authorities in damage compensations. Between 2006 and
2008, the Regional Government of Asturias spent ca. €120 000 per year to compensate for
damages by bears on apiaries. Protecting beehives in the most risky and new locations, i.e.,
close to patches of thick vegetation, should be particularly prioritized. Electric fences are rela-
tively easy to maintain and economical to build (a cost of 750 €in raw materials was required
to build a photovoltaic energized mesh fence and 450 €for the energized wire fence, 2013–
2015 prices [40]), but they require routine inspection and maintenance to ensure proper pro-
tection [40,57,58]. Similarly, we recommended the use of preventive measures after an attack
occurred, e.g., by conditioning future economic compensations to the implementation and
proper maintenance of preventive measures.
Human tolerance towards the presence of large carnivores can influence conservation and
management goals and decisions, especially in areas with dense human populations [11,59,
60]. People experiencing damages have more negative attitudes [61], and this would be
expected for apiarists experiencing brown bear damage. The attitude of apiarists can shift
towards intolerance when damages occur [19] but protecting both human property and large
carnivores is possible if we know the factors that trigger large carnivore damages. Brown bears
are slowly recovering in the Cantabrian Mountains [27], like other European large carnivore
populations [10]. Our management recommendations, build upon previous studies that pro-
motes the protection of human property, such as livestock or apiaries, as an essential tool to
prevent wildlife conflicts especially before they occur (e.g. [1,56,62,63]). The recommenda-
tions apply to present bear range and, importantly, to neighbouring areas where the bear pop-
ulation is likely to expand in the future and conflicts may arise. Continuous, long-term
monitoring of both bear populations and damage occurrence are also necessary to adjust man-
agement interventions in the future.
Supporting information
S1 Table. Full data set.
(XLSX)
Brown bear damages on apiaries
PLOS ONE | https://doi.org/10.1371/journal.pone.0206733 November 28, 2018 13 / 18
S2 Table. Set of top candidate models (ΔAICc <2) with combinations of the variables that
could influence the probability and the intensity of damage of apiaries by brown bears in
the Cantabrian Mountains, Spain. Variables include environmental factors, apiary features,
and spatial and temporal factors. Note that the variables Probability-1, Prevention,
Human_30, Infrastructures_500 and N_settlements_2000 were not included in the candidate
models after running collinearity analyses.
(DOCX)
Acknowledgments
We thank all field rangers, especially F. Somoano and A. Ramos (“Patrulla oso”) and environ-
mental keepers from the Regional Government of Asturias involved in monitoring brown bear
damage in the study area. The suggestions of three anonymous referees and the editor greatly
helped to improve the manuscript.
Author Contributions
Conceptualization: Javier Naves, Alberto Ferna
´ndez-Gil, Eloy Revilla, Miguel Delibes.
Data curation: Javier Naves, Alberto Ferna
´ndez-Gil.
Formal analysis: Javier Naves, Andre
´s Ordiz, Vincenzo Penteriani, Marı
´a del Mar Delgado,
Jose
´Vicente Lo
´pez-Bao, Eloy Revilla.
Funding acquisition: Miguel Delibes.
Investigation: Javier Naves, Andre
´s Ordiz, Alberto Ferna
´ndez-Gil, Miguel Delibes.
Methodology: Javier Naves, Andre
´s Ordiz, Alberto Ferna
´ndez-Gil, Eloy Revilla, Miguel
Delibes.
Project administration: Eloy Revilla, Miguel Delibes.
Supervision: Miguel Delibes.
Writing – original draft: Javier Naves, Vincenzo Penteriani.
Writing – review & editing: Andre
´s Ordiz, Alberto Ferna
´ndez-Gil, Marı
´a del Mar Delgado,
Jose
´Vicente Lo
´pez-Bao, Eloy Revilla, Miguel Delibes.
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