food habits of european badgers ( meles meles ) along an altitudinal gradient of mediterranean...

Food habits of European badgers (Meles meles)along an altitudinal gradient of Mediterraneanenvironments: a field test of the earthwormspecialization 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 Mediter-ranean areas indicate small importance of earthworms (Lumbricus spp.) in badger diet and support the idea that badg-ers are generalist predators. Nevertheless, only dry areas have been sampled so far. We studied badger diet in six areasalong an elevation gradient with different rainfall and habitat conditions, which influenced earthworm availability. Weevaluated the influence of earthworm availability on badger diet along this environmental gradient. Badgers used awide 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 thediet was high in elevated and wet habitats and in spring and autumn–winter. Earthworm consumption was nonlinearlyrelated to availability, indicating high intake compared with availability in wet areas. Moreover, in summer, availabilitywas virtually zero in all habitats, whereas consumption averaged 15% volume of the diet. We tentatively suggest thatbadgers compensate for variations in earthworm availability by changing their foraging tactics. This suggests that badg-ers 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. Desdonnées 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 alimen-taire des blaireaux à six sites sur un gradient d’altitude qui présente différentes conditions de pluviosité et d’habitat quiinfluencent la disponibilité des vers de terre. Cela nous a permis de déterminer l’effet de la disponibilité des vers deterre sur le régime alimentaire des blaireaux le long de ce gradient environnemental. Les blaireaux utilizent une gammeétendue de proies dans les différents habitats échantillonnés et au cours des saisons de l’étude. Contrairement àd’autres études faites dans la région méditerranéenne, les vers de terre contribuent substantiellement (27 % du volumeestimé) au régime alimentaire des blaireaux. La fréquence des vers de terre dans le régime alimentaire est forte dansles habitats en altitude et les habitats humides, ainsi qu’au printemps et en automne–hiver. La relation entre la consom-mation de vers de terre et leur disponibilité n’est pas linéaire, ce qui indique une forte ingestion en fonction de la dis-ponibilité dans les endroits humides. De plus, bien que la disponibilité des vers de terre soit virtuellement nulle en étédans tous les habitats, ils représentent en moyenne 15 % du volume du régime alimentaire. Nous avançons l’hypothèseprovisoire que les blaireaux compensent les variations dans la disponibilité des vers de terre en changeant leurs tacti-ques de recherche de nourriture. Les blaireaux peuvent donc être considérés comme des prédateurs spécialisés des versde terre dans certains environnements de la région méditerranéenne.

[Traduit par la Rédaction] Virgós et al. 51

Can. J. Zool. 82: 41–51 (2004) doi: 10.1139/Z03-205 © 2004 NRC Canada

41

Received 9 May 2003. Accepted 11 November 2003. Published on the NRC Research Press Web site at http://cjz.nrc.ca on19 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), Facultadde Biología, Universidad Complutense, E-28040 Madrid, Spain.J.A. Blanco-Aguiar. Instituto de Investigación en Recursos Cinegéticos (IREC), Universidad de Castilla – La Mancha, Junta deComunidades de Castilla – La Mancha, Consejo Superior de Investigaciones Científicas, Ronda de Toledo s/n, E-13005 CiudadReal, Spain.G. Garrote, N. Almagro, and R.P. Viso. Departamento de Biología Animal I (Invertebrados), Facultad de Biología, UniversidadComplutense, E-28040 Madrid, Spain.

1Corresponding author (e-mail: [email protected]).

J:\cjz\Cjz8201\Z03-205.vpFebruary 13, 2004 7:56:17 AM

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Introduction

European badger (Meles meles) feeding ecology has beenextensively studied throughout most of the species’ range innorthwestern and central Europe (reviewed in Roper 1994;Goszczynski et al. 2000). Nevertheless, fewer studies deal-ing with this topic have been carried out in other regionssuch as the Mediterranean or Asia (but see Pigozzi 1991;Martín et al. 1995; Roper and Mickevicius 1995; Revilla andPalomares 2002a). Most studies undertaken in Britain andother parts of northwestern Europe indicated that badgersmay be considered specialized consumers of earthworms,Lumbricus spp. (Andersen 1954; Henry 1983; Kruuk 1989).However, this “earthworm specialization” hypothesis hasbeen challenged or refuted by several researchers based oninformation from other regions, especially the Mediterraneanand Russia, but also from some parts of Britain (Skinner andSkinner 1988; Shepherdson et al. 1990; Roper 1994; Roperand Mickevicius 1995; Revilla and Palomares 2002a). In arecent review, Goszczynski et al. (2000) indicated that mostRussian works cited by Roper and Mickevicius (1995) assupport of the generalist character of badger used a macro-scopic determination of prey remains, which is clearly inap-propriate for earthworm detection. These authors suggestedthat the specialization and generalization hypotheses may bereconciled and they advocated further studies to determinethe feeding adaptations of badgers to different habitats andenvironmental conditions.

To date, the studies conducted in the Mediterranean havebeen mainly carried out in the south where environmentalconditions are too dry and hot to permit an abundance ofearthworms (Edwards and Lofty 1977). Badgers thereforeneed to adapt their diets to other food resources such asfruits, insects, or rabbits (Oryctolagus cuniculus) (Kruuk andde Kock 1981; Ciampalini and Lovari 1985; Pigozzi 1991;Rodríguez and Delibes 1992; Martín et al. 1995; Revilla andPalomares 2002a). Although some authors indicated thatsome Mediterranean badger populations showed local spe-cializations in other abundant, predictable, and profitablefood resources such as rabbits (Martín et al. 1995; Fedrianiet al. 1998), Revilla and Palomares (2002a) refuted the pres-ence of local specializations towards rabbits among badgersin southwestern Spain and indicated that badgers behave astypical generalist species which take advantage of availableresources.

Nevertheless, “earthworm specialization” or alternative“local specialization” hypotheses need to be more rigorouslytested by means of simultaneous estimations of food intakeand food availability, the two main criteria for defining spe-cialization in an ecological sense (Stephens and Krebs 1986;Futuyma and Moreno 1988). Although Mediterranean envi-ronments are considered “bad” habitats for earthworms (Ed-wards and Lofty 1977; Kruuk 1989; Pigozzi 1991; Martín etal. 1995), some studies in wet locations in the Mediterraneanmountains of northern Spain (Ibáñez and Ibáñez 1980) indi-cated that some Mediterranean badger populations may bespecialized in earthworms. The large diversity of environ-ments, climates, habitats, and types of land use in Mediterra-nean mountains may be good places to test the earthwormspecialization hypothesis because we found dramaticchanges in rainfall and landscape types within a same area,

which could promote changes, both spatially and seasonally,in earthworm availability.

We studied three contrasting Mediterranean habitats toevaluate the influence of earthworm availability on badgerdiets. In particular, we tested whether badgers behave asearthworm specialists that prey upon earthworms regardlessof their availability or whether they are generalists thatchange their diets according to the availability of key foodresources in the field. Even when a species consumes preyaccording to availability, a certain trophic specialism couldbe hypothesized if consumption of a prey continues even atlocations or in season where the values of availability arenear zero. We tested this hypothesis both spatially (i.e., dif-ferent habitats) and seasonally (i.e., wet and dry season) ineach habitat studied.

Materials and methods

Study areasWe investigated six different areas (2 km × 2 km) located

at least 5 km apart in the mountains of Madrid Province incentral Spain over 2 years (1998 and 1999) (see Fig. 1). Ac-cording to spatial use of Mediterranean badgers, the distancebetween sampling areas preclude the possibility of simulta-neous use by the same badgers of different areas (Rodríguezet al. 1996; Revilla and Palomares 2002b).

Several badger setts (one to four in each area) or latrinesites (two to seven in each area) were sampled in each area,although we were unable to ascertain the exact number ofdifferent groups or individuals sampled in each case; in allareas, we obtained samples scattered throughout the 2 km ×2 km area, which allowed us to be confident about the reli-ability of our diet data in each area. Based on previousworks on badger feeding behaviour and spatial organization,we assumed that latrines located in a particular 2 km × 2 kmarea were associated with badgers feeding in this area (re-viewed in Kruuk 1989).

All sampled areas were situated within the Mediterraneanbioclimatic region (following Ozenda 1982). However, thepresence of mountains produces important changes in clima-

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42 Can. J. Zool. Vol. 82, 2004

Fig. 1. Location of Madrid Province in Spain and the six sam-pled areas within the Madrid province. Triangles represent supra-Mediterranean habitats, squares represent mixed habitats, and cir-cles represent meso-Mediterranean habitats.



tic conditions and gives rise to several different bioclimaticstages with differing vegetation formations, physiognomy,and climate (Rivas-Martínez et al. 1987). This fact led us tosample areas located in three different bioclimatic stages ofthe Mediterranean climate region. Areas 1 and 2 (hereinafterMontejo and Miraflores, respectively) are typical supra-Mediterranean stages located at 1200 m a.s.l. (Montejo) and1250 m a.s.l. (Miraflores) that resemble typical badger habi-tats in northwestern Europe but with, in addition, a notablesummer drought (15 vs. 250 mm in spring). Mean tempera-tures are hot in summer (18.5 °C) and relatively cold in win-ter (4 °C). Deciduous broad-leaved forests of Pyrenean oak(Quercus pyrenaica) cover the landscape with some standsof Scots pine (Pinus sylvestris), with large areas of pasturein Montejo but a more closed structure in Miraflores (Ta-ble 1).

Areas 3 and 4 (hereinafter Madarcos and Manzanares,respectively) were located in the middle between thesupra-Mediterranean stage and low-lying habitats (meso-Mediterranean bioclimatic stage) at 950–1050 m a.s.l. Theypossess mixed climatic and landscape structures, somewherebetween both habitat types, and will be referred to hereinaf-ter as mixed habitats. Rainfall is very low in summer (15 mm)and relatively abundant in spring (80 mm) and temperaturesare higher than in Montejo and Miraflores (20 °C in summerand 5 °C in winter). The landscape is covered mainly by typ-ical Mediterranean vegetation consisting of holm oak (Quercusilex) and different shrubs (gum cistus, Cistus ladanifer, andbroom, Cytisus scoparius), with the presence of Pyreneanoak and narrow-leaved ash (Fraxinus angustifolia) indicatingwetter conditions than in areas 5 and 6. In addition, the land-scape is moderately open in Madarcos and very open (abun-dant 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 typi-cally Mediterranean and are similar to those in areas alreadystudied in the Mediterranean (Ciampalini and Lovari 1985;Pigozzi 1991; Revilla and Palomares 2002a). Rainfall isvery scarce all year round (10 mm in summer and 40 mm inspring) and temperatures are very hot in summer (24 °C) andmoderate in winter (7 °C) and spring (15 °C). The landscapeis covered by holm oak forests and typical Mediterraneanscrubland 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 rear-ing predominating in Montejo, Miraflores, Madarcos, andManzanares, big-game hunting in Hoyo (red deer, Cervus

elaphus, and wild boar, Sus scrofa), and small-game hunting(mainly rabbits) and recreational activities and sheep grazingin Venturada.

Scat collectionIn all areas, the latrines were cleared on the first visit. La-

trines were visited at least once every 2 months, and inspring and summer, visits were made once a month. A totalof 364 scats were collected (sample size for each habitattype and season is given in Table 2). We considered eachclearly identified dropping located in each latrine pit to bean independent scat sample. In most cases, pits containedonly one scat, although sometimes more than one scat wasfound in bigger pits, in which case, we considered scats tobe different when it was clearly and objectively possible todefine the different units (by colour, texture, or form). Oth-erwise, we considered the entire pit content to be just onescat. Each scat was stored in a paper bag and then deep-frozen at –20 °C prior to subsequent analysis in the labora-tory.

Laboratory proceduresWe followed the protocols used by Kruuk and Parish

(1981). In brief, each scat was washed through a sieve with1.3-mm gauze, the water used for rinsing and particles pass-ing through the sieve being retained in a large beaker. Thesolid and visible remains were separated and examinedunder a 20× binocular microscope. Three subsamples of1.5 mL of the rinsing water were taken from the bottom ofthe beaker and washed into a petri dish, stained with picricacid, and then examined under a 40× binocular microscopefor evidence of the presence of earthworm chaetae. In each1.5-mL subsample, we assessed the volume of earthwormsingested by counting the number of chaetae in ten 1-cm2 ar-eas in the petri dish and then calculated the mean value. Foreach scat sample, we obtained the mean value of the numberof chaetae from the three subsamples. The mean value wasscored as described in Kruuk and Parish (1981) and we usedtheir proposed correlation equation to estimate the numberof earthworm gizzards from the chaetae score.

The food remains retained in the sieve were thoroughlyrinsed and then examined under water in a large shallowwhite dish. Identification was made with the help of keysand reference collections. We used the following categories:coleopteran (dung beetles from the family Scarabaeidae),larvae, myriapoda, amphibians, other vertebrates (reptilesand birds), mammals, fruits, and fungi.

For each scat, the total number of each kind of prey wascounted or extrapolated from the remains. The bulk of eachprey in the scat sample was assessed visually, using the same

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Virgós et al. 43

Treecover

Shrubcover

Pasturecover

Other (bareground, rocks)

Montejo 42.5 3.9 42.8 2.4Miraflores 69.2 9.3 16.6 2.5Madarcos 17.6 8.7 59.4 8.4Manzanares 22.2 36.2 41.2 0Hoyo 15.5 45.3 9.7 22.5Venturada 28.7 16.3 42.8 3.4

Table 1. Microhabitat composition (%) in the different sampledareas.

Sample size (number of scats)

Habitat type Spring Summer Autumn–winter Total

Supra-Mediterranean 70 47 41 158Mixed 77 53 14 144Meso-Mediterranean 24 24 14 62Total 171 124 69 364

Table 2. Number of European badger (Meles meles) scats col-lected in the different habitat types (bioclimatic stages) and sea-sons during the 2 years of study.



assumptions as Kruuk and Parish (1981), and their relativevolume in the diet in accordance with the seven-point scaleproposed by these authors was estimated. In addition, thefrequency of occurrence of each prey item in the differentseasons and habitats is presented.

Food availabilityIn all six areas, several potentially important food re-

sources for badgers (e.g., see Kruuk 1989; Roper 1994;Martín et al. 1995) were sampled: rabbits, earthworms, anddung beetles (the main coleopteran prey in badger diet;Kruuk 1989; Pigozzi 1991). The availability of these re-sources was estimated in spring and summer, since theseseasons present the highest climatic contrasts in centralSpain (Rivas-Martínez et al. 1987). This fact may lead tosignificant differences in the availability of food items,mainly earthworms, the availability of which has beenshown to differ markedly depending on rainfall and tempera-ture regimes (Edwards and Lofty 1977, Kruuk and Parish1981; Satchell 1983). Average values for spring and summerin both years were used as the availability measure.

Earthworm abundance was estimated using the formalinmethod (Raw 1959; Kruuk et al. 1979; Kruuk and Parish1981). In each area, we stratified the sampling by differenti-ating three microhabitats: tree canopy, shrub canopy, andpasture. In each one, seven randomly distributed plots of50 cm × 50 cm were placed on the ground after all groundcover had been removed. In Montejo, shrub estimation wasonly performed during the spring of the first year; in subse-quent seasons and years, this microhabitat was not sampledbecause of logistical difficulties and its low availability. Ineach plot, 2 L of 0.6% formalin was applied to stimulate theemergence of earthworms. Earthworms were counted for15 min in each plot; all plots were studied in the early morn-ing and for a period of no more than 3 h to mitigate the po-tentially confusing effects of the time of day. For each areaand microhabitat, we used the mean number of earthwormsrecorded as a measure of the indirect abundance in this stra-tum and area. Several factors such as soil type or time fromthe last rainfall might affect percolation of formalin and sub-sequent estimates of earthworm availability. Nevertheless,we consider that differences in formalin percolation maysimulate differences in water percolation during rainfall. Ad-ditionally, we sampled our areas in 1 week to sample undersimilar rainfall conditions.

In each area, the microhabitat availability for earthworms(following the abovementioned classification) was estimatedin spring, the season when earthworm density was assumedto be highest. Microhabitat availability was estimated by aseries of transects randomly distributed in each area. Tenkilometres was sampled, divided into three transects of3.3 km, each one 300 m from another. Each 10 m, we re-corded the microhabitat located at the stopping point. Thesedata were used to obtain a combined measurement of earth-worm availability in each area by using the product avail-ability of each microhabitat × mean number of earthwormsin this microhabitat.

Dung beetle availability was estimated by counting thenumber of cow scats in each area and then by visual inspec-tion for larvae and adult beetle in a sample of these scats.

We only estimated the number of dung beetles and theirlarvae because they represented the bulk of the beetles con-sumed by badgers elsewhere, but it is possible that othersources of beetles were present in the environment. There-fore, our availability index needs to be considered with somecaution. Because our work is delineated to test the earth-worm specialization hypothesis rather to test beetle special-ization, we assumed that the index could be a crudesurrogate of the true availability of coleopterans. Scat countswere performed in a 2 km long and 1 m wide linear transectrandomly selected in the area. During the scat survey, a sam-ple of 20 scats was inspected for 1 min and the number ofbeetles seen within the dung was counted. To mitigate thepotential effects of the time since dung deposition on theabundance of beetles, we sampled only fresh dung as deter-mined by aspect and a preliminary examination. The avail-ability value was obtained by multiplying the number ofcow scat samples by the mean number of dung beetles in thefresh scats in the surveyed area.

Rabbit abundance was indirectly estimated through thecounting of latrines (for a similar procedure see Palma et al.1999) in the same linear transects used to estimate cow scatabundance.

Statistical analysesTo analyse differences in badger diet between environ-

ments, we considered the three bioclimatic stages (supra-Mediterranean, mixed, and meso-Mediterranean) as differenthabitat types. In addition, scats were collected in three dif-ferent seasons: spring (mid-March to mid-June), summer(mid-June to mid-September), and autumn–winter (mid-September to mid-March). Habitat type and seasonal differ-ences in the relative volume of main prey items were ana-lysed by a two-way ANOVA with the relative volume ofeach prey item as a response variable and habitat type andseason as fixed factors. In all analyses, prior to testing sea-sonal and habitat effects, we tested for potential differencesamong sampling areas within habitat type through a hierar-chically nested mixed ANOVA with areas as random factorsnested within habitat types (fixed factor).

We compared the differences in the availability of earth-worms and coleopterans between seasons, habitat types, andmicrohabitats by using a three-way ANOVA with the earth-worm and coleopteran data as a response variable and sea-son, microhabitat, and habitat type as fixed factors.

The relationship between the availability of each prey re-source considered and their relative volume in the badger’sdiet was analysed using a linear regression analysis, and totest for potential nonlinear trends, we searched for the bestfit of each pair of regressions using CURVEEXPERT ver-sion 1.3 (Hyams 1997).

Finally, the relationship between diet diversity (measuredby the Shannon–Weaver index; Magurran 1988) and the rel-ative volume of earthworms in the diet was analysed usinglinear regression for each habitat type and season consid-ered.

All variables were checked for normality, and when vari-ables were not normal, we tested for positive kurtosis(Underwood 1996) to control any increase in the type I errorrate of variables with negative kurtosis. Nonvariables showed

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no significant deviation from normality or positive kurtosis.All statistical analyses were carried out using STATISTICAversion 6 (Statsoft Inc. 2001).

Results

Overall characteristics of badger dietBadgers 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) domi-nated badger diet, although earthworms also made an impor-tant contribution to badger diet (65% occurrence and 27% ofestimated volume). Remaining prey items generally consti-

tuted 27% of the estimated volume, but any one particularprey item could have reached values above 10% of the esti-mated volume in the overall diet. However, some of the preyitems reached higher values in some seasons or areas (Ta-ble 3).

Effects of habitat type and season on dietFirst, we tested if badger diet varied among areas within

habitat types. Only for amphibians and other vertebrates wasthe difference within habitats significant and higher than be-tween habitats. This is due to the large differences betweenManzanares and Madarcos in the case of amphibians(10.72% vs. 0.45%, respectively). With other vertebrates, the

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Virgós et al. 45

Prey item and diet diversity Spring Summer Autumn–winter Overall

EarthwormsSupra-Mediterranean 48.8 (84.3) 13.6 (48.9) 52.6 (75) 39.3 (71.5)Mixed 21.5 (67.5) 16.2 (47.2) 23.5 (41.7) 19.7 (61.8)Meso-Mediterranean 18.0 (75) 10.1 (41.7) 7.1 (50.0) 12.5 (56.4)

ColeopteransSupra-Mediterranean 20.1 (82.9) 24.5 (89.4) 12.1 (63.4) 18.7 (79.7)Mixed 34.4 (94.8) 42.8 (92.4) 22.5 (85.7) 36.4 (93.1)Meso-Mediterranean 12.2 (100) 26.1 (95.8) 9.1 (85.7) 16.8 (95.2)

MyriapodaSupra-Mediterranean 0.3 (4.3) 0.5 (6.4) 0.2 (2.4) 0.4 (4.4)Mixed 0.04 (1.3) 0.1 (1.9) 0.6 (7.1) 0.1 (2.1)Meso-Mediterranean 1.4 (12.5) 7.1 (29.2) 4.7 (28.6) 4.3 (22.6)

LarvaeSupra-Mediterranean 3.4 (25.7) 10.5 (44.7) 2.4 (29.3) 5.3 (32.3)Mixed 3.8 (36.4) 10.2 (64.1) 7.2 (50.0) 6.5 (47.9)Meso-Mediterranean 3.4 (50.0) 18.6 (66.7) 34.6 (92.9) 16.3 (66.1)

FungiSupra-Mediterranean 0.6 (10.0) 9.8 (34.0) 21.7 (4.9) 3.3 (15.8)Mixed 5.00 (23.4) 2.4 (17.0) 4.7 (21.4) 4.00 (20.8)Meso-Mediterranean 21.7 (66.7) 4.7 (20.8) 13.9 (57.1) 13.3 (46.8)

FruitsSupra-Mediterranean 1.1 (4.3) 7.5 (36.2) 14.9 (41.5) 6.6 (23.4)Mixed 1.9 (19.5) 7.9 (18.9) 5.9 (42.9) 4.5 (21.5)Meso-Mediterranean 2.3 (37.5) 3.1 (16.7) 0.6 (21.4) 2.2 (25.8)

AmphibiansSupra-Mediterranean 0 (0) 1.0 (10.6) 0.05 (2.4) 0.3 (3.8)Mixed 7.3 (26.0) 3.8 (11.3) 14.6 (50.0) 6.7 (22.9)Meso-Mediterranean 1 (12.5) 3.6 (12.5) 14.1 (28.6) 5.0 (16.1)

MammalsSupra-Mediterranean 1 (5.7) 9.4 (19.1) 5.8 (14.6) 4.7 (12.0)Mixed 0.5 (3.9) 1.6 (5.7) 0 (0) 0.9 (4.2)Meso-Mediterranean 3.6 (8.3) 2.7 (16.7) 0.9 (21.4) 2.6 (14.5)

Other vertebratesSupra-Mediterranean 0.3 (2.9) 2.4 (12.8) 2.7 (4.9) 0.9 (6.3)Mixed 1.2 (10.4) 1.6 (7.6) 0 (0) 1.2 (8.3)Meso-Mediterranean 2.7 (12.5) 10.2 (33.3) 10.1 (28.6) 7.3 (24.2)

Diet diversitySupra-Mediterranean 0.91 1.56 1.38 1.28Mixed 1.32 1.44 1.60 1.45Meso-Mediterranean 1.37 1.78 1.77 1.64

Table 3. Estimated ingested volume (%) and frequency of occurrence (in parentheses, %) for each dif-ferent prey category considered in each habitat type and season and diet diversity for each habitat typeand season.



difference was mainly due to the comparison between Hoyoand Venturada within the meso-Mediterranean habitat (8.98%vs. 0.92%, respectively). For the remainder of prey items, dietamong areas did not show significant variations (see Table 4).

Consumption of earthworms showed a statisticallysignificant interaction between habitat and season andsignificant results for the two factors when consideredseparately (Table 5). Earthworm occurrence was higher insupra-Mediterranean habitats than in mixed and meso-Mediterranean habitats (Duncan’s test, p < 0.001), andmixed habitats showed higher ingested volumes than meso-Mediterranean ones (Duncan’s test, p = 0.03) (see Fig. 2).Moreover, earthworm consumption was higher in spring andautumn–winter than in summer (Duncan’s test, both differ-ences p < 0.001) (Fig. 2). The interaction is a result of thelow occurrence of earthworms in autumn–winter in meso-Mediterranean habitats and the low value for supra-Mediterranean habitats in summer. In this season, badgers inall habitat types showed a very similar level of earthwormconsumption (see Fig. 2).

There were differences in coleopteran consumption bothbetween habitats and between seasons, although the interac-tion was not significant (Table 5). Coleopterans were con-sumed significantly less in autumn–winter than in spring andsummer (Duncan’s test, p < 0.001). In relation to habitattypes, coleopterans showed significantly higher frequency ofoccurrence in mixed habitats than in supra-Mediterraneanand meso-Mediterranean ones (Duncan’s test, p = 0.02 andp < 0.001, respectively) (see also Table 3). Badgers in supra-Mediterranean areas consumed more coleopterans than thosein meso-Mediterranean habitats (Duncan’s test, p = 0.03).

Among myriapods, interactions and fixed factors showedsignificant differences. However, the examination of the in-teraction indicated that seasonal differences were a result ofthe large consumption of myriapods in summer and autumn–winter in meso-Mediterranean habitats but not in the other

two habitats (Table 5). In addition, badgers in meso-Mediterranean habitats consumed significantly larger pro-portions 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 signifi-cant. However, we focussed on the interaction term (Ta-ble 5). Larvae were mainly consumed in summer andautumn–winter, although the pattern was not identical in allof the different habitat types. In meso-Mediterranean habi-tats, the highest frequency was observed in autumn–winter,

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Prey item Effect df F p

Earthworms Habitat 2 12.9 0.03Area 3 1.8 0.14

Coleopterans Habitat 2 12.3 0.03Area 3 1.4 0.23

Myriapoda Habitat 2 5.6 0.08Area 3 1.4 0.23

Larvae Habitat 2 5.6 0.08Area 3 1.2 0.29

Fungi Habitat 2 8.7 0.04Area 3 1.0 0.38

Fruits Habitat 2 0.5 0.65Area 3 1.5 0.21

Amphibians Habitat 2 1.0 0.47Area 3 10.4 <0.001

Mammals Habitat 2 3.1 0.17Area 3 1.3 0.29

Other vertebrates Habitat 2 1.1 0.43Area 3 2.6 0.05

Table 4. Results of the hierarchically mixed nested ANOVA withareas as random nested factor and habitat type as fixed factor forall the categories of prey items considered.

Volume ingested Effect df F p

Earthworms Season 2 10.7 <0.001Habitat 2 23.1 <0.001Season × habitat 4 6.6 <0.001

Coleopterans Season 2 7.3 <0.001Habitat 2 11.5 <0.001Season × habitat 4 0.6 0.66

Myriapoda Season 2 5.3 <0.01Habitat 2 16.7 <0.001Season × habitat 4 3.4 <0.01

Larvae Season 2 19.8 <0.001Habitat 2 20.6 <0.001Season × habitat 4 9.5 <0.001

Fungi Season 2 2.6 0.08Habitat 2 14.6 <0.001Season × habitat 4 10.6 <0.001

Fruits Season 2 3.6 0.03Habitat 2 3.3 0.04Season × habitat 4 2.2 0.07

Mammals Season 2 1.8 0.16Habitat 2 4.6 0.01Season × habitat 4 2.1 0.07

Table 5. Results of the two-way ANOVA with season and habi-tat type as fixed factors and the ingested volume of the differentprey items as the dependent variable.

Fig. 2. Interaction between habitat type and season for earth-worm volume in the diet. Whiskers represent the standard errorof the mean values, which are indicated by different symbols(see legend on the figure).



while in supra-Mediterranean and mixed habitats, larvaewere mainly consumed in summer (Table 3). This prey itemwas most important in the diet of meso-Mediterranean badg-ers (Duncan’s test, both p < 0.001).

Consumption of fungi did not show any seasonal differ-ences, although habitat and the interaction showed signifi-cant differences (Table 5). The interaction indicated that theseasonal pattern of fungi importance in badgers’ diet differsgreatly between habitats. In supra-Mediterranean habitats,summer is the season of greatest importance of fungi,whereas in meso-Mediterranean areas, spring is the most im-portant season (Table 3). Fungi consumption was higher inmeso-Mediterranean habitats than in mixed or supra-Mediterranean habitats (Duncan’s test, both p < 0.001).

For fruit consumption, there were seasonal and habitat dif-ferences even though the interaction was not significant(Table 5). More fruit was consumed by badgers in supra-Mediterranean habitats than those in meso-Mediterranean ar-eas (Duncan’s test, p = 0.008) even though no differenceswere 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 withautumn–winter).

Finally, for mammals, we only observed differences amonghabitat types (Table 5). The highest volume was recorded inbadgers in supra-Mediterranean habitats even though therewere no statistical differences compared with badgers inmeso-Mediterranean areas. Badgers in mixed habitatsconsumed lower volumes than those found in supra-Mediterranean habitats (Duncan’s test, p = 0.006) (Table 3).No rabbits were found in any sample and all mammals wereidentified as rodents even though no species identificationwas performed.

Seasonal and habitat differences in food availabilityWe tested for differences among areas in a determined

habitat type before the examination of habitat or seasonaldifferences. The nested mixed ANOVA indicated that areas

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 interac-tions were significant. Earthworms were statistically moreabundant in supra-Mediterranean and mixed habitats than inmeso-Mediterranean ones (Duncan’s test, both p < 0.001).However, availability was very low and similar in all areas insummer, with higher values in spring. It is interesting to notethat earthworm availability in supra-Mediterranean andmixed areas during summer was very similar to availabilityall year round in meso-Mediterranean habitats (and nearzero) (see Fig. 3a). Among microhabitats, a more compli-cated pattern arises, with the highest abundance of earth-worms below trees in supra-Mediterranean habitats and inpastures in mixed habitats (both in spring). Earthworm avail-

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Virgós et al. 47

Prey availability Effect df F p

Earthworms Season 1 32.2 <0.001Habitat 2 7.5 <0.001Microhabitat 2 10.0 <0.001Season × habitat 2 6.8 <0.001Season × microhabitat 2 10.5 <0.001Habitat × microhabitat 4 4.2 <0.01Season × habitat ×

microhabitat4 4.7 <0.001

Cow scats Season 1 5.5 0.03Habitat 2 13.4 <0.001Season × habitat 2 1.6 0.2Season 1 9.5 <0.01

Coleopterans Habitat 1 1.5 0.2Season × habitat 1 0.2 0.7

Table 6. Results of the three-way ANOVA with the mean num-ber of earthworms, cow scats, and coleopterans in cow scatscounted in the field as dependent variables and season, habitattype, and microhabitat as fixed factors.

Fig. 3. Earthworm availability (mean number of individualscounted in a 50 cm × 50 cm plot by formalin method) in thedifferent seasons (a) and microhabitats (b) for the different habi-tat types studied. Whiskers represent the standard error of themean values, which are indicated by different symbols (see leg-end on the figure).



ability was very low below shrubs in all habitats and seasons(see Fig. 3b).

The number of cow scat samples showed significant dif-ferences between seasons and habitats, although the interac-tion was not significant (Table 6). Cow scats were moreabundant in mixed and supra-Mediterranean habitats than inmeso-Mediterranean ones (Duncan’s test, both p < 0.001)(Fig. 4). Moreover, availability in spring was significantlyhigher than in summer (Duncan’s test, p = 0.03) (Fig. 4).

The number of coleopterans within cow scats was exam-ined in supra-Mediterranean and mixed habitats. In meso-Mediterranean habitats, counting was not carried out be-cause of the very low availability of cow scats (less than 20in all cases, see above). The results indicated significant dif-ferences for season but not for habitat (Table 6). A highernumber of coleopterans were recorded in summer than inspring (Duncan’s test, p = 0.003) (Fig. 4).

Finally, for rabbits, we found no significant differencesbetween seasons or habitats (all p > 0.20). Rabbit abundance(number of latrines per kilometre) was very low in all of theareas sampled.

Prey availability and badger foodEarthworm consumption is better described by a nonlinear

rationale model (r = 0.99, p < 0.001) than by a linear regres-sion model (r = 0.93). The nonlinear model indicated higherconsumption at high availabilities and relatively high con-sumption at low availabilities (Fig. 5). Coleopteran con-sumption is related to food availability (r = 0.85, p = 0.03,n = 6). Rabbit availability was very low and badgers in ourstudy areas did not consume them. In addition, it is interest-ing to note that the consumption of earthworms was rela-tively high in summer in all habitat types (between 10% and20% of overall volume) despite the low availability in thefield (absent in most of the habitats and microhabitats sam-pled with the formalin method). For example, earthwormavailability was zero in the summer of 1999 in all habitatand microhabitats sampled; however, earthworm consump-tion during this summer was 11.07% and 6.05% in badgersin supra-Mediterranean and mixed habitats, respectively.These values were clearly higher in the summer of 1998 (be-tween 12% and 22% of the estimated volume) despite thevery low availability values (including zero availability inmixed habitats but with a volume estimated at almost 22%).

Diet diversity and main prey itemsDiet diversity fluctuated between 0.9 for the diet of badg-

ers in supra-Mediterranean habitats in spring and 1.78 forthat 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 butslightly higher values in summer and autumn–winter (seeTable 3). Diet diversity was very negatively correlated withearthworm volume in the diet (r = –0.74, p = 0.02, n = 9),and no association was found between diversity andcoleopteran volume in the diet (r = –0.08, p = 0.84, n = 9).In general, other food resources of minor importance werecorrelated with diversity: larvae volume and other vertebrate

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48 Can. J. Zool. Vol. 82, 2004

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, whichare indicated by different symbols (see legend on the figure).

Fig. 5. Best nonlinear model (rationale model) describing the re-lationship between earthworm consumption (% volume) andearthworm availability (average number of earthworms in 100formalin plots). Data were log transformed.



volume were positively correlated with the diversity index,but fruit volume was negatively correlated with diversity.

Discussion

Badgers showed contrasting food habits among habitats inthe mountains of central Spain, despite the proximity of thelocations sampled. The available food supply for badgers inthe Mediterranean habitats varies greatly and badgers re-spond by shifting their diets towards different prey items.Thus, it is impossible to define a key resource for badgersacross the different habitat types sampled, with earthwormsonly dominating badgers’ diets in the supra-Mediterraneanstage. In mixed and meso-Mediterranean habitats, badgersshowed a broad-ranging diet dominated, especially in sum-mer, by coleopterans. On a broad scale, badgers thereforefeed on different resources in different areas as suggested byRoper (1994).

Seasonal variations in diet indicate variability in the im-portance of a resource from season to season. For example,earthworms are the key resource in spring in supra-Mediterranean areas and are very important in mixed habi-tats. On the other hand, beetles are the most important re-source in both of these habitat types in summer. Thesedifferences accord with the availability of food resources inthe field. Earthworms are only available in the rainy andmild conditions of spring and autumn–winter (Edwards andLoftfy 1977; Kruuk and Parish 1981), good weather condi-tions for earthworm emergence, and this is the case forsupra-Mediterranean and mixed habitats. In meso-Mediterranean habitats, earthworms are relatively less avail-able in spring but are still consumed in moderation and inproportion to availability. In meso-Mediterranean habitatsand during dry seasons in mixed and supra-Mediterraneanones, badgers replaced earthworms with dung beetles andother coleopterans, which are predictable and abundant re-sources. They are consumed more in summer when avail-ability is higher. It is interesting to note that meso-Mediterranean habitats showed a low availability of dung, sothe presence of coleopterans in the diet must indicate a highproportion of other environmental sources of beetles or, al-ternatively, higher search effort.

However, earthworm consumption is not linearly relatedto field availability, a key prediction of models of diet spe-cialization (Stephens and Krebs 1986; Futuyma and Moreno1988). 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 insupra-Mediterranean habitats in spring and autumn–winter(48.8% and 52.53% of the relative volume, respectively) isvery large in relation to availability, whereas the rest of thedata are relatively constant, despite large differences inavailability. For example, in the mixed habitats in spring,availability was high (average 331 worms by 100 formalinplots, see Materials and methods) and food consumption wasmoderate (21.4% of diet volume), whereas in summer for allhabitat types and in meso-Mediterranean habitats also inspring, consumption was between 10% and 18% and avail-ability fluctuated between 0 and 0.5 worms by 100 formalinplots (more than 10 times lower than in mixed habitats in

spring). Thus, two points suggest a specialism on earth-worms in these badger populations: (1) badgers feed onearthworms in a similar way despite very contrasting valuesof availability and continue to consume earthworms in rela-tively high amounts even under very low values of availabil-ity (also for a similar result in Belarus see Sidorovich 1997)and (2) consumption is higher compared with availability inseasons or areas of high earthworm availability. Kruuk andParish (1981) indicated in their pioneering work that earth-worm consumption is high and very similar in areas withlarge differences in availability. It is possible that our avail-ability measure was not well suited to test the specializationhypothesis, but our sample size was similar to those of pre-vious studies and our methodology was the same. In addi-tion, we sampled the most common habitat types for 2 yearsand in three contrasting microhabitats. It is difficult to ap-preciate how earthworms may constitute up to 18% of badg-ers’ diets in summer in mixed habitats when, in this habitatin summer, we were unable to find any earthworms in 2years 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 avail-ability by changing their foraging tactics and probably for-aging effort. Thus, badgers may be viewed as facultativespecialists that search preferentially for earthworms butprobably take other food resources during their foragingbouts (beetles, fruits, and fungi). It is likely that badgerssearch selectively and know where earthworms are most eas-ily found in summer but that the relatively low availabilityprobably does not provide for a good energetic balance.Therefore, badgers need to catch more beetles or search foralternative food sources.

Therefore, are badgers specialists or generalists? We agreewith Goszczynski et al. (2000) who suggest that a definitiveanswer to this question is not possible. Overall, badgers aregeneralist species with the capacity to survive on differentresources (Roper 1994; Neal and Cheeseman 1996; Revillaand Palomares 2002a). However, we suggest that our dataand those of others (reviewed in Kruuk 1989) indicate thatunder some circumstances, badgers are earthworm special-ists or, rather, at least they search intensively for earth-worms. Interestingly, this hypothesis was ruled out fornorthwestern Europe (Kruuk 1989; Woodroffe and Mac-donald 1993), some central and northeastern countries(Sidorovich 1997; Goszczynski et al. 2000), and some Medi-terranean areas, regions that are an important part of the dis-tribution of the species (Neal and Cheeseman 1996). Theseareas have in common a relatively wet climate for at least alarge part of the year (only in summer is rainfall very low inMediterranean mountains) and a relatively large proportionof the broad-leaved forests and pastures that are the pre-ferred habitats of earthworms (Kruuk et al. 1979; Brown1981; da Silva et al. 1993). It is possible to hypothesize thatbadgers are a good example of facultative strategists (Glas-ser 1982, 1984). Badgers behave more like specialists andless like facultative strategists in “good earthworm habitat”(more “constant” habitats in the original sense of Glasser1984), but they adopt a facultative generalist behaviour inmore variable environments, for example in summer in theMediterranean mountains or in very dry regions with a foodsupply that varies throughout the year. Facultative specialists

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Virgós et al. 49



and generalists are not easily classified as strict specialists orgeneralists and this may explain the cases of species that ex-hibit both specialist and generalist populations across theirdistribution, as appears to occur in badgers.

The facultative specialist strategy might be facilitated bythe good payoffs in terms of foraging decisions that earth-worms give badgers. Earthworms are easily caught and han-dled (Kruuk et al. 1979; Kruuk 1989), two important elementsin foraging decisions (Stephens and Krebs 1986). In addi-tion, earthworms are a very good energetic resource with aprotein content in their tissues similar to that in muscles invertebrates (Bolton and Phillipson 1976), and it has beenproved that there is a good relationship between earthwormconsumption and some important fitness correlates such asbody 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 ourthree habitat types even though the abundance of badgers isclearly higher in supra-Mediterranean and mixed habitatsthan in meso-Mediterranean habitats (Virgós and Casanovas1999). If the badgers that live in good earthworm habitatsare more abundant and present more complex social lifestyles and better reproductive success, then it is possible toconsider earthworm consumption as good for individual fit-ness, and specialization on earthworms could be viewed asan adaptive strategy in good earthworm habitats. We suggesta new formulation of specialization characterization thatincludes parameters linked to fitness and the life history ofindividuals, as well as population parameters such as the in-trinsic rate of growth. In this sense, areas such as the Medi-terranean mountains where environmental conditions forbadgers change dramatically in the space of a few kilometresmay be key places for testing the relationship between foodspecialization and fitness correlates.

Acknowledgements

Jorge G. Casanovas, Jorge Lozano, Sara Cabezas, TeresaRomero, Daniel López-Huertas, and Estrella Dávila helpedus with the field sampling. We also thank the Department ofAnimal Biology I (Invertebrates) for the use of laboratoryinstallations and especially Dr. Ignacio García, Dr. CarmenRoldán, and Dr. Marta Aro.

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