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Food habits of European badgers (Meles meles)
along an altitudinal gradient of Mediterranean
environments: a field test of the earthworm
specialization hypothesis
Emilio Virgós, Julián G. Mangas, José Antonio Blanco-Aguiar, Germán Garrote,
Nuria Almagro, and Raquel P. Viso
Abstract: Food specialization by European badgers (Meles meles) is a largely debated controversy. Data from Mediterranean areas indicate small importance of earthworms (Lumbricus spp.) in badger diet and support the idea that badgers are generalist predators. Nevertheless, only dry areas have been sampled so far. We studied badger diet in six areas
along an elevation gradient with different rainfall and habitat conditions, which influenced earthworm availability. We
evaluated the influence of earthworm availability on badger diet along this environmental gradient. Badgers used a
wide range of prey items in the different habitats and seasons sampled. In contrast with other Mediterranean studies,
earthworms made an important contribution to badger diet (27% of estimated volume). Earthworm occurrence in the
diet was high in elevated and wet habitats and in spring and autumn–winter. Earthworm consumption was nonlinearly
related to availability, indicating high intake compared with availability in wet areas. Moreover, in summer, availability
was virtually zero in all habitats, whereas consumption averaged 15% volume of the diet. We tentatively suggest that
badgers compensate for variations in earthworm availability by changing their foraging tactics. This suggests that badgers could be viewed as specialist foragers for earthworms in some Mediterranean environments.
Résumé : La spécialisation alimentaire du blaireau d’Europe (Meles meles) fait l’objet de nombreuses discussions. Des
données en provenance de la région méditerranéenne indiquent la faible importance des vers de terre (Lumbricus spp.)
dans le régime alimentaire du blaireau et appuient l’hypothèse qui veut que le blaireau soit un prédateur généraliste.
Néanmoins, seules les régions arides ont été échantillonnées jusqu’à maintenant. Nous avons étudié le régime alimentaire des blaireaux à six sites sur un gradient d’altitude qui présente différentes conditions de pluviosité et d’habitat qui
influencent la disponibilité des vers de terre. Cela nous a permis de déterminer l’effet de la disponibilité des vers de
terre sur le régime alimentaire des blaireaux le long de ce gradient environnemental. Les blaireaux utilizent une gamme
étendue de proies dans les différents habitats échantillonnés et au cours des saisons de l’étude. Contrairement à
d’autres études faites dans la région méditerranéenne, les vers de terre contribuent substantiellement (27 % du volume
estimé) au régime alimentaire des blaireaux. La fréquence des vers de terre dans le régime alimentaire est forte dans
les habitats en altitude et les habitats humides, ainsi qu’au printemps et en automne–hiver. La relation entre la consommation de vers de terre et leur disponibilité n’est pas linéaire, ce qui indique une forte ingestion en fonction de la disponibilité dans les endroits humides. De plus, bien que la disponibilité des vers de terre soit virtuellement nulle en été
dans tous les habitats, ils représentent en moyenne 15 % du volume du régime alimentaire. Nous avançons l’hypothèse
provisoire que les blaireaux compensent les variations dans la disponibilité des vers de terre en changeant leurs tactiques de recherche de nourriture. Les blaireaux peuvent donc être considérés comme des prédateurs spécialisés des vers
de terre dans certains environnements de la région méditerranéenne.
[Traduit par la Rédaction]
Virgós et al.
51
Received 9 May 2003. Accepted 11 November 2003. Published on the NRC Research Press Web site at http://cjz.nrc.ca on
19 February 2004.
E. Virgós.1 Área de Biodiversidad y Conservación, Departamento de Matemáticas, Física Aplicada y Ciencias la Naturaleza,
Universidad Rey Juan Carlos, E-28933 Móstoles (Madrid), Spain.
J.G. Mangas. Área de Biodiversidad y Conservación, Departamento de Matemáticas, Física Aplicada y Ciencias la Naturaleza,
Universidad Rey Juan Carlos, E-28933 Móstoles (Madrid), Spain, and Departamento de Biología Animal I (Invertebrados), Facultad
de Biología, Universidad Complutense, E-28040 Madrid, Spain.
J.A. Blanco-Aguiar. Instituto de Investigación en Recursos Cinegéticos (IREC), Universidad de Castilla – La Mancha, Junta de
Comunidades de Castilla – La Mancha, Consejo Superior de Investigaciones Científicas, Ronda de Toledo s/n, E-13005 Ciudad
Real, Spain.
G. Garrote, N. Almagro, and R.P. Viso. Departamento de Biología Animal I (Invertebrados), Facultad de Biología, Universidad
Complutense, E-28040 Madrid, Spain.
1
Corresponding author (e-mail: [email protected]).
Can. J. Zool. 82: 41–51 (2004)
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Introduction
European badger (Meles meles) feeding ecology has been
extensively studied throughout most of the species’ range in
northwestern and central Europe (reviewed in Roper 1994;
Goszczynski et al. 2000). Nevertheless, fewer studies dealing with this topic have been carried out in other regions
such as the Mediterranean or Asia (but see Pigozzi 1991;
Martín et al. 1995; Roper and Mickevicius 1995; Revilla and
Palomares 2002a). Most studies undertaken in Britain and
other parts of northwestern Europe indicated that badgers
may be considered specialized consumers of earthworms,
Lumbricus spp. (Andersen 1954; Henry 1983; Kruuk 1989).
However, this “earthworm specialization” hypothesis has
been challenged or refuted by several researchers based on
information from other regions, especially the Mediterranean
and Russia, but also from some parts of Britain (Skinner and
Skinner 1988; Shepherdson et al. 1990; Roper 1994; Roper
and Mickevicius 1995; Revilla and Palomares 2002a). In a
recent review, Goszczynski et al. (2000) indicated that most
Russian works cited by Roper and Mickevicius (1995) as
support of the generalist character of badger used a macroscopic determination of prey remains, which is clearly inappropriate for earthworm detection. These authors suggested
that the specialization and generalization hypotheses may be
reconciled and they advocated further studies to determine
the feeding adaptations of badgers to different habitats and
environmental conditions.
To date, the studies conducted in the Mediterranean have
been mainly carried out in the south where environmental
conditions are too dry and hot to permit an abundance of
earthworms (Edwards and Lofty 1977). Badgers therefore
need to adapt their diets to other food resources such as
fruits, insects, or rabbits (Oryctolagus cuniculus) (Kruuk and
de Kock 1981; Ciampalini and Lovari 1985; Pigozzi 1991;
Rodríguez and Delibes 1992; Martín et al. 1995; Revilla and
Palomares 2002a). Although some authors indicated that
some Mediterranean badger populations showed local specializations in other abundant, predictable, and profitable
food resources such as rabbits (Martín et al. 1995; Fedriani
et al. 1998), Revilla and Palomares (2002a) refuted the presence of local specializations towards rabbits among badgers
in southwestern Spain and indicated that badgers behave as
typical generalist species which take advantage of available
resources.
Nevertheless, “earthworm specialization” or alternative
“local specialization” hypotheses need to be more rigorously
tested by means of simultaneous estimations of food intake
and food availability, the two main criteria for defining specialization in an ecological sense (Stephens and Krebs 1986;
Futuyma and Moreno 1988). Although Mediterranean environments are considered “bad” habitats for earthworms (Edwards and Lofty 1977; Kruuk 1989; Pigozzi 1991; Martín et
al. 1995), some studies in wet locations in the Mediterranean
mountains of northern Spain (Ibáñez and Ibáñez 1980) indicated that some Mediterranean badger populations may be
specialized in earthworms. The large diversity of environments, climates, habitats, and types of land use in Mediterranean mountains may be good places to test the earthworm
specialization hypothesis because we found dramatic
changes in rainfall and landscape types within a same area,
Can. J. Zool. Vol. 82, 2004
Fig. 1. Location of Madrid Province in Spain and the six sampled areas within the Madrid province. Triangles represent supraMediterranean habitats, squares represent mixed habitats, and circles represent meso-Mediterranean habitats.
which could promote changes, both spatially and seasonally,
in earthworm availability.
We studied three contrasting Mediterranean habitats to
evaluate the influence of earthworm availability on badger
diets. In particular, we tested whether badgers behave as
earthworm specialists that prey upon earthworms regardless
of their availability or whether they are generalists that
change their diets according to the availability of key food
resources in the field. Even when a species consumes prey
according to availability, a certain trophic specialism could
be hypothesized if consumption of a prey continues even at
locations or in season where the values of availability are
near zero. We tested this hypothesis both spatially (i.e., different habitats) and seasonally (i.e., wet and dry season) in
each habitat studied.
Materials and methods
Study areas
We investigated six different areas (2 km × 2 km) located
at least 5 km apart in the mountains of Madrid Province in
central Spain over 2 years (1998 and 1999) (see Fig. 1). According to spatial use of Mediterranean badgers, the distance
between sampling areas preclude the possibility of simultaneous use by the same badgers of different areas (Rodríguez
et al. 1996; Revilla and Palomares 2002b).
Several badger setts (one to four in each area) or latrine
sites (two to seven in each area) were sampled in each area,
although we were unable to ascertain the exact number of
different groups or individuals sampled in each case; in all
areas, we obtained samples scattered throughout the 2 km ×
2 km area, which allowed us to be confident about the reliability of our diet data in each area. Based on previous
works on badger feeding behaviour and spatial organization,
we assumed that latrines located in a particular 2 km × 2 km
area were associated with badgers feeding in this area (reviewed in Kruuk 1989).
All sampled areas were situated within the Mediterranean
bioclimatic region (following Ozenda 1982). However, the
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Table 1. Microhabitat composition (%) in the different sampled
areas.
Tree
cover
Montejo
Miraflores
Madarcos
Manzanares
Hoyo
Venturada
42.5
69.2
17.6
22.2
15.5
28.7
Shrub
cover
3.9
9.3
8.7
36.2
45.3
16.3
Pasture
cover
42.8
16.6
59.4
41.2
9.7
42.8
Other (bare
ground, rocks)
2.4
2.5
8.4
0
22.5
3.4
tic conditions and gives rise to several different bioclimatic
stages with differing vegetation formations, physiognomy,
and climate (Rivas-Martínez et al. 1987). This fact led us to
sample areas located in three different bioclimatic stages of
the Mediterranean climate region. Areas 1 and 2 (hereinafter
Montejo and Miraflores, respectively) are typical supraMediterranean stages located at 1200 m a.s.l. (Montejo) and
1250 m a.s.l. (Miraflores) that resemble typical badger habitats in northwestern Europe but with, in addition, a notable
summer drought (15 vs. 250 mm in spring). Mean temperatures are hot in summer (18.5 °C) and relatively cold in winter (4 °C). Deciduous broad-leaved forests of Pyrenean oak
(Quercus pyrenaica) cover the landscape with some stands
of Scots pine (Pinus sylvestris), with large areas of pasture
in Montejo but a more closed structure in Miraflores (Table 1).
Areas 3 and 4 (hereinafter Madarcos and Manzanares,
respectively) were located in the middle between the
supra-Mediterranean stage and low-lying habitats (mesoMediterranean bioclimatic stage) at 950–1050 m a.s.l. They
possess mixed climatic and landscape structures, somewhere
between both habitat types, and will be referred to hereinafter as mixed habitats. Rainfall is very low in summer (15 mm)
and relatively abundant in spring (80 mm) and temperatures
are higher than in Montejo and Miraflores (20 °C in summer
and 5 °C in winter). The landscape is covered mainly by typical Mediterranean vegetation consisting of holm oak (Quercus
ilex) and different shrubs (gum cistus, Cistus ladanifer, and
broom, Cytisus scoparius), with the presence of Pyrenean
oak and narrow-leaved ash (Fraxinus angustifolia) indicating
wetter conditions than in areas 5 and 6. In addition, the landscape is moderately open in Madarcos and very open (abundant pastures) in Manzanares (Table 1).
Finally, areas 5 and 6 (hereinafter Venturada and Hoyo)
are situated in the meso-Mediterranean bioclimatic stage
(850–900 m a.s.l.) where the climatic conditions are typically Mediterranean and are similar to those in areas already
studied in the Mediterranean (Ciampalini and Lovari 1985;
Pigozzi 1991; Revilla and Palomares 2002a). Rainfall is
very scarce all year round (10 mm in summer and 40 mm in
spring) and temperatures are very hot in summer (24 °C) and
moderate in winter (7 °C) and spring (15 °C). The landscape
is covered by holm oak forests and typical Mediterranean
scrubland consisting mainly of large tracts of C. ladanifer.
The structure of the landscape is very closed (Hoyo) or open
(Venturada) (Table 1).
Human land use differs from area to area, with stock rearing predominating in Montejo, Miraflores, Madarcos, and
Manzanares, big-game hunting in Hoyo (red deer, Cervus
Table 2. Number of European badger (Meles meles) scats collected in the different habitat types (bioclimatic stages) and seasons during the 2 years of study.
Sample size (number of scats)
Habitat type
Supra-Mediterranean
Mixed
Meso-Mediterranean
Total
Spring
70
77
24
171
Summer
47
53
24
124
Autumn–winter
Total
41
14
14
69
158
144
62
364
elaphus, and wild boar, Sus scrofa), and small-game hunting
(mainly rabbits) and recreational activities and sheep grazing
in Venturada.
Scat collection
In all areas, the latrines were cleared on the first visit. Latrines were visited at least once every 2 months, and in
spring and summer, visits were made once a month. A total
of 364 scats were collected (sample size for each habitat
type and season is given in Table 2). We considered each
clearly identified dropping located in each latrine pit to be
an independent scat sample. In most cases, pits contained
only one scat, although sometimes more than one scat was
found in bigger pits, in which case, we considered scats to
be different when it was clearly and objectively possible to
define the different units (by colour, texture, or form). Otherwise, we considered the entire pit content to be just one
scat. Each scat was stored in a paper bag and then deepfrozen at –20 °C prior to subsequent analysis in the laboratory.
Laboratory procedures
We followed the protocols used by Kruuk and Parish
(1981). In brief, each scat was washed through a sieve with
1.3-mm gauze, the water used for rinsing and particles passing through the sieve being retained in a large beaker. The
solid and visible remains were separated and examined
under a 20× binocular microscope. Three subsamples of
1.5 mL of the rinsing water were taken from the bottom of
the beaker and washed into a petri dish, stained with picric
acid, and then examined under a 40× binocular microscope
for evidence of the presence of earthworm chaetae. In each
1.5-mL subsample, we assessed the volume of earthworms
ingested by counting the number of chaetae in ten 1-cm2 areas in the petri dish and then calculated the mean value. For
each scat sample, we obtained the mean value of the number
of chaetae from the three subsamples. The mean value was
scored as described in Kruuk and Parish (1981) and we used
their proposed correlation equation to estimate the number
of earthworm gizzards from the chaetae score.
The food remains retained in the sieve were thoroughly
rinsed and then examined under water in a large shallow
white dish. Identification was made with the help of keys
and reference collections. We used the following categories:
coleopteran (dung beetles from the family Scarabaeidae),
larvae, myriapoda, amphibians, other vertebrates (reptiles
and birds), mammals, fruits, and fungi.
For each scat, the total number of each kind of prey was
counted or extrapolated from the remains. The bulk of each
prey in the scat sample was assessed visually, using the same
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assumptions as Kruuk and Parish (1981), and their relative
volume in the diet in accordance with the seven-point scale
proposed by these authors was estimated. In addition, the
frequency of occurrence of each prey item in the different
seasons and habitats is presented.
Food availability
In all six areas, several potentially important food resources for badgers (e.g., see Kruuk 1989; Roper 1994;
Martín et al. 1995) were sampled: rabbits, earthworms, and
dung beetles (the main coleopteran prey in badger diet;
Kruuk 1989; Pigozzi 1991). The availability of these resources was estimated in spring and summer, since these
seasons present the highest climatic contrasts in central
Spain (Rivas-Martínez et al. 1987). This fact may lead to
significant differences in the availability of food items,
mainly earthworms, the availability of which has been
shown to differ markedly depending on rainfall and temperature regimes (Edwards and Lofty 1977, Kruuk and Parish
1981; Satchell 1983). Average values for spring and summer
in both years were used as the availability measure.
Earthworm abundance was estimated using the formalin
method (Raw 1959; Kruuk et al. 1979; Kruuk and Parish
1981). In each area, we stratified the sampling by differentiating three microhabitats: tree canopy, shrub canopy, and
pasture. In each one, seven randomly distributed plots of
50 cm × 50 cm were placed on the ground after all ground
cover had been removed. In Montejo, shrub estimation was
only performed during the spring of the first year; in subsequent seasons and years, this microhabitat was not sampled
because of logistical difficulties and its low availability. In
each plot, 2 L of 0.6% formalin was applied to stimulate the
emergence of earthworms. Earthworms were counted for
15 min in each plot; all plots were studied in the early morning and for a period of no more than 3 h to mitigate the potentially confusing effects of the time of day. For each area
and microhabitat, we used the mean number of earthworms
recorded as a measure of the indirect abundance in this stratum and area. Several factors such as soil type or time from
the last rainfall might affect percolation of formalin and subsequent estimates of earthworm availability. Nevertheless,
we consider that differences in formalin percolation may
simulate differences in water percolation during rainfall. Additionally, we sampled our areas in 1 week to sample under
similar rainfall conditions.
In each area, the microhabitat availability for earthworms
(following the abovementioned classification) was estimated
in spring, the season when earthworm density was assumed
to be highest. Microhabitat availability was estimated by a
series of transects randomly distributed in each area. Ten
kilometres was sampled, divided into three transects of
3.3 km, each one 300 m from another. Each 10 m, we recorded the microhabitat located at the stopping point. These
data were used to obtain a combined measurement of earthworm availability in each area by using the product availability of each microhabitat × mean number of earthworms
in this microhabitat.
Dung beetle availability was estimated by counting the
number of cow scats in each area and then by visual inspection for larvae and adult beetle in a sample of these scats.
Can. J. Zool. Vol. 82, 2004
We only estimated the number of dung beetles and their
larvae because they represented the bulk of the beetles consumed by badgers elsewhere, but it is possible that other
sources of beetles were present in the environment. Therefore, our availability index needs to be considered with some
caution. Because our work is delineated to test the earthworm specialization hypothesis rather to test beetle specialization, we assumed that the index could be a crude
surrogate of the true availability of coleopterans. Scat counts
were performed in a 2 km long and 1 m wide linear transect
randomly selected in the area. During the scat survey, a sample of 20 scats was inspected for 1 min and the number of
beetles seen within the dung was counted. To mitigate the
potential effects of the time since dung deposition on the
abundance of beetles, we sampled only fresh dung as determined by aspect and a preliminary examination. The availability value was obtained by multiplying the number of
cow scat samples by the mean number of dung beetles in the
fresh scats in the surveyed area.
Rabbit abundance was indirectly estimated through the
counting of latrines (for a similar procedure see Palma et al.
1999) in the same linear transects used to estimate cow scat
abundance.
Statistical analyses
To analyse differences in badger diet between environments, we considered the three bioclimatic stages (supraMediterranean, mixed, and meso-Mediterranean) as different
habitat types. In addition, scats were collected in three different seasons: spring (mid-March to mid-June), summer
(mid-June to mid-September), and autumn–winter (midSeptember to mid-March). Habitat type and seasonal differences in the relative volume of main prey items were analysed by a two-way ANOVA with the relative volume of
each prey item as a response variable and habitat type and
season as fixed factors. In all analyses, prior to testing seasonal and habitat effects, we tested for potential differences
among sampling areas within habitat type through a hierarchically nested mixed ANOVA with areas as random factors
nested within habitat types (fixed factor).
We compared the differences in the availability of earthworms and coleopterans between seasons, habitat types, and
microhabitats by using a three-way ANOVA with the earthworm and coleopteran data as a response variable and season, microhabitat, and habitat type as fixed factors.
The relationship between the availability of each prey resource considered and their relative volume in the badger’s
diet was analysed using a linear regression analysis, and to
test for potential nonlinear trends, we searched for the best
fit of each pair of regressions using CURVEEXPERT version 1.3 (Hyams 1997).
Finally, the relationship between diet diversity (measured
by the Shannon–Weaver index; Magurran 1988) and the relative volume of earthworms in the diet was analysed using
linear regression for each habitat type and season considered.
All variables were checked for normality, and when variables were not normal, we tested for positive kurtosis
(Underwood 1996) to control any increase in the type I error
rate of variables with negative kurtosis. Nonvariables showed
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Table 3. Estimated ingested volume (%) and frequency of occurrence (in parentheses, %) for each different prey category considered in each habitat type and season and diet diversity for each habitat type
and season.
Prey item and diet diversity
Earthworms
Supra-Mediterranean
Mixed
Meso-Mediterranean
Coleopterans
Supra-Mediterranean
Mixed
Meso-Mediterranean
Myriapoda
Supra-Mediterranean
Mixed
Meso-Mediterranean
Larvae
Supra-Mediterranean
Mixed
Meso-Mediterranean
Fungi
Supra-Mediterranean
Mixed
Meso-Mediterranean
Fruits
Supra-Mediterranean
Mixed
Meso-Mediterranean
Amphibians
Supra-Mediterranean
Mixed
Meso-Mediterranean
Mammals
Supra-Mediterranean
Mixed
Meso-Mediterranean
Other vertebrates
Supra-Mediterranean
Mixed
Meso-Mediterranean
Diet diversity
Supra-Mediterranean
Mixed
Meso-Mediterranean
Spring
Summer
Autumn–winter
Overall
48.8 (84.3)
21.5 (67.5)
18.0 (75)
13.6 (48.9)
16.2 (47.2)
10.1 (41.7)
52.6 (75)
23.5 (41.7)
7.1 (50.0)
39.3 (71.5)
19.7 (61.8)
12.5 (56.4)
20.1 (82.9)
34.4 (94.8)
12.2 (100)
24.5 (89.4)
42.8 (92.4)
26.1 (95.8)
12.1 (63.4)
22.5 (85.7)
9.1 (85.7)
18.7 (79.7)
36.4 (93.1)
16.8 (95.2)
0.3 (4.3)
0.04 (1.3)
1.4 (12.5)
0.5 (6.4)
0.1 (1.9)
7.1 (29.2)
0.2 (2.4)
0.6 (7.1)
4.7 (28.6)
0.4 (4.4)
0.1 (2.1)
4.3 (22.6)
3.4 (25.7)
3.8 (36.4)
3.4 (50.0)
10.5 (44.7)
10.2 (64.1)
18.6 (66.7)
2.4 (29.3)
7.2 (50.0)
34.6 (92.9)
5.3 (32.3)
6.5 (47.9)
16.3 (66.1)
0.6 (10.0)
5.00 (23.4)
21.7 (66.7)
9.8 (34.0)
2.4 (17.0)
4.7 (20.8)
21.7 (4.9)
4.7 (21.4)
13.9 (57.1)
3.3 (15.8)
4.00 (20.8)
13.3 (46.8)
1.1 (4.3)
1.9 (19.5)
2.3 (37.5)
7.5 (36.2)
7.9 (18.9)
3.1 (16.7)
14.9 (41.5)
5.9 (42.9)
0.6 (21.4)
6.6 (23.4)
4.5 (21.5)
2.2 (25.8)
0 (0)
7.3 (26.0)
1 (12.5)
1.0 (10.6)
3.8 (11.3)
3.6 (12.5)
0.05 (2.4)
14.6 (50.0)
14.1 (28.6)
0.3 (3.8)
6.7 (22.9)
5.0 (16.1)
1 (5.7)
0.5 (3.9)
3.6 (8.3)
9.4 (19.1)
1.6 (5.7)
2.7 (16.7)
5.8 (14.6)
0 (0)
0.9 (21.4)
4.7 (12.0)
0.9 (4.2)
2.6 (14.5)
0.3 (2.9)
1.2 (10.4)
2.7 (12.5)
2.4 (12.8)
1.6 (7.6)
10.2 (33.3)
2.7 (4.9)
0 (0)
10.1 (28.6)
0.9 (6.3)
1.2 (8.3)
7.3 (24.2)
0.91
1.32
1.37
no significant deviation from normality or positive kurtosis.
All statistical analyses were carried out using STATISTICA
version 6 (Statsoft Inc. 2001).
Results
Overall characteristics of badger diet
Badgers used a wide range of prey items in the different
habitats, areas, and seasons sampled. Overall, coleopterans
(92% in occurrence and 36% of estimated volume) dominated badger diet, although earthworms also made an important contribution to badger diet (65% occurrence and 27% of
estimated volume). Remaining prey items generally consti-
1.56
1.44
1.78
1.38
1.60
1.77
1.28
1.45
1.64
tuted 27% of the estimated volume, but any one particular
prey item could have reached values above 10% of the estimated volume in the overall diet. However, some of the prey
items reached higher values in some seasons or areas (Table 3).
Effects of habitat type and season on diet
First, we tested if badger diet varied among areas within
habitat types. Only for amphibians and other vertebrates was
the difference within habitats significant and higher than between habitats. This is due to the large differences between
Manzanares and Madarcos in the case of amphibians
(10.72% vs. 0.45%, respectively). With other vertebrates, the
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Can. J. Zool. Vol. 82, 2004
Table 4. Results of the hierarchically mixed nested ANOVA with
areas as random nested factor and habitat type as fixed factor for
all the categories of prey items considered.
Table 5. Results of the two-way ANOVA with season and habitat type as fixed factors and the ingested volume of the different
prey items as the dependent variable.
Prey item
Effect
df
F
p
Volume ingested
Effect
df
F
p
Earthworms
Habitat
Area
Habitat
Area
Habitat
Area
Habitat
Area
Habitat
Area
Habitat
Area
Habitat
Area
Habitat
Area
Habitat
Area
2
3
2
3
2
3
2
3
2
3
2
3
2
3
2
3
2
3
12.9
1.8
12.3
1.4
5.6
1.4
5.6
1.2
8.7
1.0
0.5
1.5
1.0
10.4
3.1
1.3
1.1
2.6
0.03
0.14
0.03
0.23
0.08
0.23
0.08
0.29
0.04
0.38
0.65
0.21
0.47
<0.001
0.17
0.29
0.43
0.05
Earthworms
Season
Habitat
Season ×
Season
Habitat
Season ×
Season
Habitat
Season ×
Season
Habitat
Season ×
Season
Habitat
Season ×
Season
Habitat
Season ×
Season
Habitat
Season ×
2
2
4
2
2
4
2
2
4
2
2
4
2
2
4
2
2
4
2
2
4
10.7
23.1
6.6
7.3
11.5
0.6
5.3
16.7
3.4
19.8
20.6
9.5
2.6
14.6
10.6
3.6
3.3
2.2
1.8
4.6
2.1
<0.001
<0.001
<0.001
<0.001
<0.001
0.66
<0.01
<0.001
<0.01
<0.001
<0.001
<0.001
0.08
<0.001
<0.001
0.03
0.04
0.07
0.16
0.01
0.07
Coleopterans
Myriapoda
Larvae
Fungi
Fruits
Amphibians
Mammals
Other vertebrates
Coleopterans
Myriapoda
Larvae
Fungi
Fruits
Mammals
difference was mainly due to the comparison between Hoyo
and Venturada within the meso-Mediterranean habitat (8.98%
vs. 0.92%, respectively). For the remainder of prey items, diet
among areas did not show significant variations (see Table 4).
Consumption of earthworms showed a statistically
significant interaction between habitat and season and
significant results for the two factors when considered
separately (Table 5). Earthworm occurrence was higher in
supra-Mediterranean habitats than in mixed and mesoMediterranean habitats (Duncan’s test, p < 0.001), and
mixed habitats showed higher ingested volumes than mesoMediterranean ones (Duncan’s test, p = 0.03) (see Fig. 2).
Moreover, earthworm consumption was higher in spring and
autumn–winter than in summer (Duncan’s test, both differences p < 0.001) (Fig. 2). The interaction is a result of the
low occurrence of earthworms in autumn–winter in mesoMediterranean habitats and the low value for supraMediterranean habitats in summer. In this season, badgers in
all habitat types showed a very similar level of earthworm
consumption (see Fig. 2).
There were differences in coleopteran consumption both
between habitats and between seasons, although the interaction was not significant (Table 5). Coleopterans were consumed significantly less in autumn–winter than in spring and
summer (Duncan’s test, p < 0.001). In relation to habitat
types, coleopterans showed significantly higher frequency of
occurrence in mixed habitats than in supra-Mediterranean
and meso-Mediterranean ones (Duncan’s test, p = 0.02 and
p < 0.001, respectively) (see also Table 3). Badgers in supraMediterranean areas consumed more coleopterans than those
in meso-Mediterranean habitats (Duncan’s test, p = 0.03).
Among myriapods, interactions and fixed factors showed
significant differences. However, the examination of the interaction indicated that seasonal differences were a result of
the large consumption of myriapods in summer and autumn–
winter in meso-Mediterranean habitats but not in the other
habitat
habitat
habitat
habitat
habitat
habitat
habitat
Fig. 2. Interaction between habitat type and season for earthworm volume in the diet. Whiskers represent the standard error
of the mean values, which are indicated by different symbols
(see legend on the figure).
two habitats (Table 5). In addition, badgers in mesoMediterranean habitats consumed significantly larger proportions of myriapods than those in the other two habitats
(Duncan’s test, both p < 0.001) (also see Table 3).
For larvae, all effects and interactions were also significant. However, we focussed on the interaction term (Table 5). Larvae were mainly consumed in summer and
autumn–winter, although the pattern was not identical in all
of the different habitat types. In meso-Mediterranean habitats, the highest frequency was observed in autumn–winter,
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47
Table 6. Results of the three-way ANOVA with the mean number of earthworms, cow scats, and coleopterans in cow scats
counted in the field as dependent variables and season, habitat
type, and microhabitat as fixed factors.
Prey availability
Effect
df
F
p
Earthworms
Season
Habitat
Microhabitat
Season × habitat
Season × microhabitat
Habitat × microhabitat
Season × habitat ×
microhabitat
Season
Habitat
Season × habitat
Season
Habitat
Season × habitat
1
2
2
2
2
4
4
32.2
7.5
10.0
6.8
10.5
4.2
4.7
<0.001
<0.001
<0.001
<0.001
<0.001
<0.01
<0.001
1
2
2
1
1
1
5.5
13.4
1.6
9.5
1.5
0.2
0.03
<0.001
0.2
<0.01
0.2
0.7
Cow scats
Coleopterans
while in supra-Mediterranean and mixed habitats, larvae
were mainly consumed in summer (Table 3). This prey item
was most important in the diet of meso-Mediterranean badgers (Duncan’s test, both p < 0.001).
Consumption of fungi did not show any seasonal differences, although habitat and the interaction showed significant differences (Table 5). The interaction indicated that the
seasonal pattern of fungi importance in badgers’ diet differs
greatly between habitats. In supra-Mediterranean habitats,
summer is the season of greatest importance of fungi,
whereas in meso-Mediterranean areas, spring is the most important season (Table 3). Fungi consumption was higher in
meso-Mediterranean habitats than in mixed or supraMediterranean habitats (Duncan’s test, both p < 0.001).
For fruit consumption, there were seasonal and habitat differences even though the interaction was not significant
(Table 5). More fruit was consumed by badgers in supraMediterranean habitats than those in meso-Mediterranean areas (Duncan’s test, p = 0.008) even though no differences
were found among the remaining pairs of comparisons.
Fruits were mainly consumed in summer and autumn–
winter, with the lowest volume in the diet being in spring
(Duncan’s test, p = 0.03 with summer and p = 0.01 with
autumn–winter).
Finally, for mammals, we only observed differences among
habitat types (Table 5). The highest volume was recorded in
badgers in supra-Mediterranean habitats even though there
were no statistical differences compared with badgers in
meso-Mediterranean areas. Badgers in mixed habitats
consumed lower volumes than those found in supraMediterranean habitats (Duncan’s test, p = 0.006) (Table 3).
No rabbits were found in any sample and all mammals were
identified as rodents even though no species identification
was performed.
Seasonal and habitat differences in food availability
We tested for differences among areas in a determined
habitat type before the examination of habitat or seasonal
differences. The nested mixed ANOVA indicated that areas
Fig. 3. Earthworm availability (mean number of individuals
counted in a 50 cm × 50 cm plot by formalin method) in the
different seasons (a) and microhabitats (b) for the different habitat types studied. Whiskers represent the standard error of the
mean values, which are indicated by different symbols (see legend on the figure).
within a habitat showed the same earthworm availability
(random factor, F[3,442] = 0.58, p = 0.63).
Earthworm availability strongly changed between habitats,
seasons, and microhabitats (Table 6). All effects and interactions were significant. Earthworms were statistically more
abundant in supra-Mediterranean and mixed habitats than in
meso-Mediterranean ones (Duncan’s test, both p < 0.001).
However, availability was very low and similar in all areas in
summer, with higher values in spring. It is interesting to note
that earthworm availability in supra-Mediterranean and
mixed areas during summer was very similar to availability
all year round in meso-Mediterranean habitats (and near
zero) (see Fig. 3a). Among microhabitats, a more complicated pattern arises, with the highest abundance of earthworms below trees in supra-Mediterranean habitats and in
pastures in mixed habitats (both in spring). Earthworm avail© 2004 NRC Canada
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48
Fig. 4. Cow scat availability (a) and dung beetle availability
(b) in the different seasons for the different habitat types studied.
Whiskers represent the standard error of the mean values, which
are indicated by different symbols (see legend on the figure).
Can. J. Zool. Vol. 82, 2004
Fig. 5. Best nonlinear model (rationale model) describing the relationship between earthworm consumption (% volume) and
earthworm availability (average number of earthworms in 100
formalin plots). Data were log transformed.
Finally, for rabbits, we found no significant differences
between seasons or habitats (all p > 0.20). Rabbit abundance
(number of latrines per kilometre) was very low in all of the
areas sampled.
ability was very low below shrubs in all habitats and seasons
(see Fig. 3b).
The number of cow scat samples showed significant differences between seasons and habitats, although the interaction was not significant (Table 6). Cow scats were more
abundant in mixed and supra-Mediterranean habitats than in
meso-Mediterranean ones (Duncan’s test, both p < 0.001)
(Fig. 4). Moreover, availability in spring was significantly
higher than in summer (Duncan’s test, p = 0.03) (Fig. 4).
The number of coleopterans within cow scats was examined in supra-Mediterranean and mixed habitats. In mesoMediterranean habitats, counting was not carried out because of the very low availability of cow scats (less than 20
in all cases, see above). The results indicated significant differences for season but not for habitat (Table 6). A higher
number of coleopterans were recorded in summer than in
spring (Duncan’s test, p = 0.003) (Fig. 4).
Prey availability and badger food
Earthworm consumption is better described by a nonlinear
rationale model (r = 0.99, p < 0.001) than by a linear regression model (r = 0.93). The nonlinear model indicated higher
consumption at high availabilities and relatively high consumption at low availabilities (Fig. 5). Coleopteran consumption is related to food availability (r = 0.85, p = 0.03,
n = 6). Rabbit availability was very low and badgers in our
study areas did not consume them. In addition, it is interesting to note that the consumption of earthworms was relatively high in summer in all habitat types (between 10% and
20% of overall volume) despite the low availability in the
field (absent in most of the habitats and microhabitats sampled with the formalin method). For example, earthworm
availability was zero in the summer of 1999 in all habitat
and microhabitats sampled; however, earthworm consumption during this summer was 11.07% and 6.05% in badgers
in supra-Mediterranean and mixed habitats, respectively.
These values were clearly higher in the summer of 1998 (between 12% and 22% of the estimated volume) despite the
very low availability values (including zero availability in
mixed habitats but with a volume estimated at almost 22%).
Diet diversity and main prey items
Diet diversity fluctuated between 0.9 for the diet of badgers in supra-Mediterranean habitats in spring and 1.78 for
that of badgers in meso-Mediterranean habitats in summer.
The remaining values are located in a rather narrow interval,
with the lowest values recorded in spring and similar but
slightly higher values in summer and autumn–winter (see
Table 3). Diet diversity was very negatively correlated with
earthworm volume in the diet (r = –0.74, p = 0.02, n = 9),
and no association was found between diversity and
coleopteran volume in the diet (r = –0.08, p = 0.84, n = 9).
In general, other food resources of minor importance were
correlated with diversity: larvae volume and other vertebrate
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Virgós et al.
volume were positively correlated with the diversity index,
but fruit volume was negatively correlated with diversity.
Discussion
Badgers showed contrasting food habits among habitats in
the mountains of central Spain, despite the proximity of the
locations sampled. The available food supply for badgers in
the Mediterranean habitats varies greatly and badgers respond by shifting their diets towards different prey items.
Thus, it is impossible to define a key resource for badgers
across the different habitat types sampled, with earthworms
only dominating badgers’ diets in the supra-Mediterranean
stage. In mixed and meso-Mediterranean habitats, badgers
showed a broad-ranging diet dominated, especially in summer, by coleopterans. On a broad scale, badgers therefore
feed on different resources in different areas as suggested by
Roper (1994).
Seasonal variations in diet indicate variability in the importance of a resource from season to season. For example,
earthworms are the key resource in spring in supraMediterranean areas and are very important in mixed habitats. On the other hand, beetles are the most important resource in both of these habitat types in summer. These
differences accord with the availability of food resources in
the field. Earthworms are only available in the rainy and
mild conditions of spring and autumn–winter (Edwards and
Loftfy 1977; Kruuk and Parish 1981), good weather conditions for earthworm emergence, and this is the case for
supra-Mediterranean and mixed habitats. In mesoMediterranean habitats, earthworms are relatively less available in spring but are still consumed in moderation and in
proportion to availability. In meso-Mediterranean habitats
and during dry seasons in mixed and supra-Mediterranean
ones, badgers replaced earthworms with dung beetles and
other coleopterans, which are predictable and abundant resources. They are consumed more in summer when availability is higher. It is interesting to note that mesoMediterranean habitats showed a low availability of dung, so
the presence of coleopterans in the diet must indicate a high
proportion of other environmental sources of beetles or, alternatively, higher search effort.
However, earthworm consumption is not linearly related
to field availability, a key prediction of models of diet specialization (Stephens and Krebs 1986; Futuyma and Moreno
1988). Earthworm consumption is relatively high in summer
(more than 10% and near 20% in the mixed habitat),
whereas the availability, estimated by the formalin method,
in the field is virtually zero. In addition, consumption in
supra-Mediterranean habitats in spring and autumn–winter
(48.8% and 52.53% of the relative volume, respectively) is
very large in relation to availability, whereas the rest of the
data are relatively constant, despite large differences in
availability. For example, in the mixed habitats in spring,
availability was high (average 331 worms by 100 formalin
plots, see Materials and methods) and food consumption was
moderate (21.4% of diet volume), whereas in summer for all
habitat types and in meso-Mediterranean habitats also in
spring, consumption was between 10% and 18% and availability fluctuated between 0 and 0.5 worms by 100 formalin
plots (more than 10 times lower than in mixed habitats in
49
spring). Thus, two points suggest a specialism on earthworms in these badger populations: (1) badgers feed on
earthworms in a similar way despite very contrasting values
of availability and continue to consume earthworms in relatively high amounts even under very low values of availability (also for a similar result in Belarus see Sidorovich 1997)
and (2) consumption is higher compared with availability in
seasons or areas of high earthworm availability. Kruuk and
Parish (1981) indicated in their pioneering work that earthworm consumption is high and very similar in areas with
large differences in availability. It is possible that our availability measure was not well suited to test the specialization
hypothesis, but our sample size was similar to those of previous studies and our methodology was the same. In addition, we sampled the most common habitat types for 2 years
and in three contrasting microhabitats. It is difficult to appreciate how earthworms may constitute up to 18% of badgers’ diets in summer in mixed habitats when, in this habitat
in summer, we were unable to find any earthworms in 2
years of study in two different areas. We tentatively suggest,
in accordance with Kruuk and Parish (1981) and Kruuk
(1989), that badgers compensate for variations in food availability by changing their foraging tactics and probably foraging effort. Thus, badgers may be viewed as facultative
specialists that search preferentially for earthworms but
probably take other food resources during their foraging
bouts (beetles, fruits, and fungi). It is likely that badgers
search selectively and know where earthworms are most easily found in summer but that the relatively low availability
probably does not provide for a good energetic balance.
Therefore, badgers need to catch more beetles or search for
alternative food sources.
Therefore, are badgers specialists or generalists? We agree
with Goszczynski et al. (2000) who suggest that a definitive
answer to this question is not possible. Overall, badgers are
generalist species with the capacity to survive on different
resources (Roper 1994; Neal and Cheeseman 1996; Revilla
and Palomares 2002a). However, we suggest that our data
and those of others (reviewed in Kruuk 1989) indicate that
under some circumstances, badgers are earthworm specialists or, rather, at least they search intensively for earthworms. Interestingly, this hypothesis was ruled out for
northwestern Europe (Kruuk 1989; Woodroffe and Macdonald 1993), some central and northeastern countries
(Sidorovich 1997; Goszczynski et al. 2000), and some Mediterranean areas, regions that are an important part of the distribution of the species (Neal and Cheeseman 1996). These
areas have in common a relatively wet climate for at least a
large part of the year (only in summer is rainfall very low in
Mediterranean mountains) and a relatively large proportion
of the broad-leaved forests and pastures that are the preferred habitats of earthworms (Kruuk et al. 1979; Brown
1981; da Silva et al. 1993). It is possible to hypothesize that
badgers are a good example of facultative strategists (Glasser 1982, 1984). Badgers behave more like specialists and
less like facultative strategists in “good earthworm habitat”
(more “constant” habitats in the original sense of Glasser
1984), but they adopt a facultative generalist behaviour in
more variable environments, for example in summer in the
Mediterranean mountains or in very dry regions with a food
supply that varies throughout the year. Facultative specialists
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50
and generalists are not easily classified as strict specialists or
generalists and this may explain the cases of species that exhibit both specialist and generalist populations across their
distribution, as appears to occur in badgers.
The facultative specialist strategy might be facilitated by
the good payoffs in terms of foraging decisions that earthworms give badgers. Earthworms are easily caught and handled (Kruuk et al. 1979; Kruuk 1989), two important elements
in foraging decisions (Stephens and Krebs 1986). In addition, earthworms are a very good energetic resource with a
protein content in their tissues similar to that in muscles in
vertebrates (Bolton and Phillipson 1976), and it has been
proved that there is a good relationship between earthworm
consumption and some important fitness correlates such as
body mass (Kruuk and Parish 1983), reproductive output
(Hofer 1988), and social complexity (Johnson et al. 2002).
Unfortunately, we cannot obtain this type of data from our
three habitat types even though the abundance of badgers is
clearly higher in supra-Mediterranean and mixed habitats
than in meso-Mediterranean habitats (Virgós and Casanovas
1999). If the badgers that live in good earthworm habitats
are more abundant and present more complex social life
styles and better reproductive success, then it is possible to
consider earthworm consumption as good for individual fitness, and specialization on earthworms could be viewed as
an adaptive strategy in good earthworm habitats. We suggest
a new formulation of specialization characterization that
includes parameters linked to fitness and the life history of
individuals, as well as population parameters such as the intrinsic rate of growth. In this sense, areas such as the Mediterranean mountains where environmental conditions for
badgers change dramatically in the space of a few kilometres
may be key places for testing the relationship between food
specialization and fitness correlates.
Acknowledgements
Jorge G. Casanovas, Jorge Lozano, Sara Cabezas, Teresa
Romero, Daniel López-Huertas, and Estrella Dávila helped
us with the field sampling. We also thank the Department of
Animal Biology I (Invertebrates) for the use of laboratory
installations and especially Dr. Ignacio García, Dr. Carmen
Roldán, and Dr. Marta Aro.
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© 2004 NRC Canada
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February 13, 2004 7:56:18 AM