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Journal of Arid Environments

Journal of Arid Environments 72 (2008) 1698– 1708

0140-19

doi:10.1

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(A. Escu

journal homepage: www.elsevier.com/locate/jaridenv

Habitat use by large and small herbivores in a fluctuatingMediterranean ecosystem: Implications of seasonal changes

M. Rueda a,�, S. Rebollo a, L. Galvez-Bravo a, A. Escudero b

a Departamento de Ecologıa, Edificio de Ciencias, Universidad de Alcala, E-28871 Alcala de Henares, Madrid, Spainb Area de Biodiversidad y Conservacion, ESCET, Universidad Rey Juan Carlos, E-28933 Mostoles, Madrid, Spain

a r t i c l e i n f o

Article history:

Received 18 October 2007

Received in revised form

22 February 2008

Accepted 12 March 2008Available online 2 May 2008

Keywords:

Different-sized herbivores

Foraging habitat use

Oryctolagus cuniculus

Savannah-like ecosystem

Seasonality

Structural equation modelling

63/$ - see front matter & 2008 Elsevier Ltd.

016/j.jaridenv.2008.03.006

responding author. Tel.: +34 918856407; fax

ail addresses: marta.rueda@uah.es (M. Rueda

dero).

a b s t r a c t

Different-sized herbivores differ in several aspects from their relationship with food to

predation risk whilst foraging. Consequently, the spatial distribution of food, food quality

and refuge availability can determine differences in habitat selection by large and small

herbivores. In regions under Mediterranean climate, food and water availability are

subjected to spatial and temporal variations and habitat selection needs to be interpreted

within a seasonal context. To assess the influence of seasonality on foraging habitat use by

large and small herbivores, we developed a priori models taking into account direct

factors influencing habitat use (food, refuge and water), and indirect soil factors

(moisture, fertility and stoniness). Models were tested for free-ranging sheep and wild

rabbits in spring, summer and winter using structural equation modelling. The

importance of direct factors varied with body size and season. Sheep were highly

influenced by food abundance throughout the seasons. Rabbits were mainly influenced by

refuge availability in spring and winter, when food was not a limiting resource. However,

in summer, the relevance of refuge disappeared and food quality became an important

factor. Seasonality can modify the relative importance of known predictors for habitat use

by large and small herbivores inhabiting Mediterranean environments.

& 2008 Elsevier Ltd. All rights reserved.

1. Introduction

The spatial pattern and abundance of resources determines foraging habitat selection by herbivores (Cougenhour, 1991;Gross et al., 1995). In this context, herbivore body size is considered a critical parameter that exerts an important influenceon habitat choices, since different-sized herbivores can differ in aspects such as metabolic rates and digestive capacity(Demment and Van Soest, 1985), foraging parameters (Belovsky, 1997; Peters, 1983; Wilmshurst et al., 2000) or behaviour(Peters, 1983). Larger species, with a lower per mass metabolic rate, need large amounts of food but can cope withrelatively low food quality; whereas smaller species, with higher per mass metabolic rates, can cope with lower amounts offood but require a relatively high food quality (Belovsky, 1997; Olff et al., 2002; Wilmshurst et al., 2000). Different-sizedherbivores also differ in their predation risk whilst foraging (Olff and Ritchie, 1998). In general, large mammals usuallysuffer low predation because they assume active defence or are simply too large to be captured or disturbed by predators(Owen-Smith, 1988). However, small herbivores are limited by a higher predation risk (Krebs et al., 1999) and oftenrestricted to foraging in the proximity of cover and burrows (Kotler et al., 1991). At the landscape scale, food quantity,

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), salvador.rebollo@uah.es (S. Rebollo), lucia.galvez@uah.es (L. Galvez-Bravo), adrian.escudero@urjc.es

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quality or even refuge availability are factors spatially affected by water and/or nutrient dynamics, i.e., by topography(Mysterud et al., 2001) and temporally by seasonal changes.

The marked seasonality of the Mediterranean climate with hot, dry summers and cool, erratically moist winters,sustains a distinctive array of semi-arid grasslands and evergreen sclerophyllous scrub and forest. In such environments,where food and water flows are subjected to strong temporal variations, herbivore foraging habitat selection needs to beinterpreted within a seasonal context, since it is essential to understand habitat requirements during the period whenresources are limiting (Sinclair, 1975). Furthermore, potential seasonal shifts in foraging habitat use should also be studiedtaking into account herbivore body size, as temporal changes in resource availability may induce different herbivoreresponses depending on body size.

In this investigation, we evaluated the foraging habitat use of a small and a large herbivore in three seasons (spring,summer and winter) in a savannah-like ecosystem (dehesa). Dehesas are one of the ecosystems of the Iberian Peninsulawith greatest ecological and economic interest (Jofree et al., 1999). The undulating topography of dehesa ecosystems resultsin alternating gentle slopes and valleys. This conditions the distribution of soil fertility and productivity, which controlgrassland species composition and structure. Slope soils are poor with low content in nitrogen and organic matter content(Figueroa and Davy, 1991), while lowland soils are richer in nutrients and water, resulting in relatively high qualityherbaceous communities (Perez Corona et al., 1998; Vazquez de Aldana et al., 2000). As a consequence, pasturecommunities are particularly complex and diverse, both with respect to species diversity (Figueroa and Davy, 1991) and intheir dynamics and phenology (San Miguel, 2001), representing an excellent opportunity to study changes in herbivorehabitat use. We selected two herbivores of contrasting size: European rabbits (Oryctolagus cuniculus L.) and free-rangingsheep. Sheep are ruminant and have been classified as generalist herbivores (Schwartz and Ellis, 1981), whereas rabbits arehindgut-fermentors and have been classified as selective herbivores (Bhadresa, 1977). Rabbits also practice caecotrophy,i.e., the reingestion of soft faeces containing concentrated proteins and minerals (Hirakawa, 2001). Taking into accountknown direct factors influencing herbivore habitat use (food quantity and quality, refuge and water availability), andindirect soil factors, influenced by topography (moisture, fertility and stoniness), we developed a priori models for eachherbivore and season which were tested by means of structural equation modelling (SEM). We addressed the followingquestions: (1) how does the influence of the main factors affecting herbivore foraging habitat use change between seasons?(2) What are the implications of temporal and spatial segregation of resources for different herbivores living in a markedseasonal environment?

2. Methods

2.1. Study area

Research was conducted in a 330 ha dehesa located in Central Spain (401230N, 41120W). Mean elevation is 690 m. Climate issemi-arid continental-Mediterranean. Mean annual temperature and precipitation are 12.6 1C and 432.6 mm, with largeinterannual fluctuations and a drought period in summer. Soil is sandy to sandy-loam. Vegetation is typical of a dehesa, withsmall woodland patches and sparsely punctuated holm oak trees (Quercus ilex) in a pasture matrix. There are also extensiveareas of Mediterranean scrub dominated by Lavandula stoechas L. and Retama sphaerocarpa Boiss. The herbaceous layer is verydiverse and mainly composed of winter annual grasses, legumes and forbs which die at the beginning of summer. The dehesais managed for small game hunting (rabbits) as well as livestock grazing. The main wild herbivore is a dense population ofEuropean rabbits, with approximately 8.27 rabbit warrens/ha, which is considered a high density in Mediterranean habitats(Gea-Izquierdo et al., 2005). The area is also grazed by a transhumant flock of 600 free-ranging sheep (about 2 sheep/ha), fromDecember until the end of June. In summer, when most herbaceous vegetation is dry, sheep are removed from the dehesa, anddriven, as part of the human-managed system, to nearby mountain pastures where grasslands remain green.

The study area can be classified into five distinct classes regarding topography and vegetation: highlands, slopes, flatareas in mid-slope, lowlands and wet lowlands. They represent a gradient from highlands to wet lowlands of increasingherbaceous cover and height, primary productivity, perennial herbaceous cover and decreasing woody vegetation. Thesheepfold is located in a flat area in mid-slope. As consequence of the intense livestock use, high concentrations of dungand urine increase soil fertility in its vicinity. Wet lowlands are located close to a temporal bed stream bed (normally dry insummer) and lowlands are dominated by open, highly productive grasslands which, in favourable years, are mowed at theend of spring, when grasses have flowered. The approximate percentage of the study area occupied by each class was:highlands: 8%; slopes: 42%; flat areas in mid-slope: 7%; lowlands: 22%; wet lowlands: 21%.

2.2. The proposed models

SEM is an advanced statistical method that provides an insight into complex theoretical issues and has been typicallyused to support or discard an a priori hypothesised model (see Mitchell, 1992 for ecological applications). The specificationof the model consists of the translation of verbal hypotheses (based upon a priori knowledge) into a series of equationspreviously represented in the form of a path diagram which shows the causal relationships among all variables in thesystem.

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Food quality

Soil moisture

Soil fertility

Rabbit abundance

Food abundance

Water distance

Woody vegetation cover

Warren entrances

Soil stoniness

Soil fertility

Sheep abundance

Food abundance

Food quality

Water distance Soil moisture

Woody vegetation cover

Sheep fold distance

Soil stoniness

Fig. 1. Path diagram of the hypothetical factors affecting foraging habitat use for (a) rabbits and (b) sheep. One-headed arrows show causal effects of one

factor on another. Two-headed arrows show a correlation between two factors.

M. Rueda et al. / Journal of Arid Environments 72 (2008) 1698–17081700

The relationships illustrated in our path diagrams arise primarily from knowledge based on previous studies and fieldexperience. The a priori models (Fig. 1) propose that soil fertility, moisture and stoniness are indirectly influencingherbivore foraging habitat use (measured as herbivore abundance), mainly through their effect on food abundance, foodquality and refuge (warrens and woody vegetation for rabbits, sheepfold for sheep). We hypothesized that places withhigher values of soil fertility and soil moisture would have more food and of better quality, as previously observed indehesas (Perez Corona et al., 1998; Vazquez de Aldana et al., 2000). We also hypothesized that places with higher soilstoniness would have less food. This is based on previous studies carried out in the study area, where a negative linearrelationship between soil stoniness and green herbaceous cover was found (N ¼ 206, R2

¼ 0.30, po0.001) (M. Rueda,unpublished data). We hypothesized that food abundance and food quality would influence rabbit and sheep abundances.However, due to differences in body size and foraging strategy (Belovsky, 1997; Demment and Van Soest, 1985; Olff et al.,2002; Wilmshurst et al., 2000), we expected that food abundance would have a greater influence on sheep, and foodquality would mainly influence rabbit abundances. Since in seasonal environments herbivore distribution is stronglyassociated with distance to water (Traill, 2004), we hypothesized that herbivore abundances would be higher in the vicinityof drinking water sources. We also expected a correlation between soil moisture and distance to drinking water sourcessince both variables are conceptually related.

Perceived risk of predation affects the distance that an animal travel from cover to forage (Banks et al., 1999; Holmes,1991). As a small herbivore, rabbits are often restricted to foraging in pasture patches near areas of dense scrub or burrows,where they avoid predators more efficiently than in open areas (Palomares and Delibes, 1997). Thus, we hypothesised thatrabbit abundance would be higher close to areas with high woody vegetation cover and high warren abundance. Also, weexpected a stronger influence of woody vegetation cover on rabbit habitat use in summer, since rabbits consume moreholm oak sprouts, leaves and acorns when herbaceous biomass is low (Martins et al., 2002). Warrens are important forbreeding, refuge and shelter for climatic extremes (Kolb, 1991; Wheeler et al., 1981). Consequently, we included knownfactors affecting warren spatial distribution in the model, as they would indirectly affect rabbit habitat use. In dehesaecosystems, warrens are often located under holm oaks, which can provide shade during the summer and their root systemprovides structural support for burrow tunnels (Gea-Izquierdo et al., 2005). Also, warrens built under trees and shrubs havea lower flooding risk (Palomares, 2003). In dehesas, warren flooding events are influenced by topography, since openhabitats are associated to valleys with damp soils, whereas scrub areas are associated to dry slopes and highlands.Therefore, we hypothesized that warren density would be higher in areas with more woody vegetation cover and lowvalues of soil moisture. We also hypothesized a higher abundance of warrens in areas with low soil stoniness becauserabbits need soils suitable for excavation to build warrens (Parer and Libke, 1985).

Sheep also browse on holm oak (Bartolome et al., 1998), and use trees as shade (pers. obs.). Additionally, sheep behaveas central place foragers, the sheepfold being the central point of their home range (Lynch et al., 1992). Thus, wehypothesized that sheep would be influenced by woody vegetation but constrained by sheepfold distance. We expectedthat the further away from the sheepfold, the fewer sheep.

2.3. Sampling design and data collection

We randomly selected 220 points from a total of 350 intersections of a 50 m regular grid placed on an aerial photographof the study area. Each of the 220 points was regularly surveyed for herbivore abundance and different habitat variables inspring 2002 (April–June), summer 2002 (July–September) and winter 2003 (January–March).

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Sheep and rabbit abundances were described on the basis of pellet counts in permanent clearance plots. Pellet countinghas been widely used to estimate the abundance of lagomorphs and ungulates (Bailey and Putman, 1981; Palomares, 2001).Two rabbit dung plots of 0.5�0.5 m and one sheep dung plot of 0.5�5 m were randomly laid out in the vicinity of eachpoint, avoiding dense woody vegetation, since herbaceous food is scarce under woody vegetation cover, and rabbit latrines.In each season, all pellets were cleared from the dung plots when first established and revisited 6 weeks later, whenaccumulated pellets were removed and counted. Pellet persistence can differ between habitats and seasons (Iborra andLumaret, 1997). Thus, we estimated ‘‘pellet decay rates’’ in the three seasons and in lowland and highland zones in order toensure that the period between pellet clearance and count was adequate.

To quantify seasonal food abundance, we measured visual basal green cover in two permanent 0.5�0.5 m quadratsplaced in the vicinity of each point. We used green cover as a surrogate of food abundance since grazing species activelyselect green parts of plants from a relatively dry sward during the dry season (summer in our study) (Jarman and Sinclair,1979). To ensure that this variable was an appropriate measure of food availability, we tested the relationship betweengreen cover and plant biomass collected at 70 sampling points (r ¼ 0.84, po0.05).

Given the methodological constrains of obtaining a direct measure of food quality in our study, we used plantcomposition as a surrogate of food quality. Several studies have shown that the forage quality of semi-arid grasslands indehesa ecosystems varies with topographical relief and grass, legume and forb composition (Vazquez de Aldana et al.,2000). Upland and slope pastures mature earlier than those at the lower zones and are of lower quality, i.e., lower proteinand dry matter digestibility contents (Perez Corona et al., 1998). Following this criteria, we visually estimated the cover ofeach plant species in two 0.2�0.2 m quadrats in spring (May) at each of the 220 points. Afterwards, we obtained acompositional metric represented by the first axis of a detrended correspondence analysis (DCA) performed on speciescover data recorded at all points. This synthetic variable was highly correlated with three topographical position (highland,slope and lowland) (r ¼ 0.78, po0.05) and the three main functional groups (grasses, legumes and forbs) (r ¼ 0.95,po0.05) of our study site.

Water distance was considered as the shortest distance to surface water (small temporary ponds and seasonal streams)from every sampling point. Woody vegetation cover was assessed as percentage cover in a 10 m radius circular plot aroundeach point (after Morrison et al., 1998). Number of rabbit warren entrances was recorded as the number of entrances in a50 m radius around each point, since the feeding range of rabbits is restricted to about 100 m from warrens (Chapuis, 1990).Sheepfold distance was measured as distance to the sheepfold from each sampling point.

To estimate soil parameters (fertility, moisture and stoniness), four 10-cm deep soil samples were randomly collected ateach of the 220 points. Soil samples were mixed, air-dried and sieved before analyses. By definition, particles 42 mm wereclassified as stones. We used the weight of stones as a measure of soil stoniness. To obtain a variable representing soilfertility we developed a bioassay experiment. Barley seeds were sown on sieved soil samples, maintained undergreenhouse conditions and kept at constant humidity. Barley seedlings were harvested when maximum growth had beenachieved. Shoots were oven-dried at 70 1C and weighed. Barley biomass was used as a surrogate of soil fertility (see Moroet al., 1997 for methodology). Finally, we collected four additional soil samples at each point in spring, summer and winter,at least a week after a rainfall event, not during a dry period. Samples were oven-dried at 100 1C and weighed before andafter drying. The difference in weight was considered a measure of soil moisture.

Herbivore pellet abundance, green cover, distance to water and soil moisture were measured once in each season,whereas sheepfold distance, woody vegetation cover, warren entrances, soil stoniness and fertility were measured only inspring, since they remain relatively unchanged throughout the seasons.

2.4. Topography

Given that topography directly influences soil properties (fertility, moisture and stoniness), which in turn influenceherbivore habitat use, we assessed the influence of topography on herbivore habitat use and soil variables. For this, we usedthe topographical classification described in the study area section (highlands, slopes, flat areas in mid-slope, lowlands andwet lowlands). We also estimated the number of warrens and warren entrances in the five topography classes using ageographical information system (GIS).

2.5. Statistical analysis

2.5.1. Model estimation

The maximum likelihood method was used to estimate standardised path coefficients, which are equivalent tostandardised partial regression coefficients, i.e., show the relative effect of one variable upon another. The model wasevaluated separately for each herbivore and in each season. Food abundance, woody vegetation cover, number of warrenentrances, soil fertility and sheep abundance were log transformed to meet the assumption of multivariate normality. Thestatistical process of assessing whether or not the model fits the data is accomplished by a goodness-of-fit test, in which thecovariance in the observed data is compared with that expected if the model were true. The test statistic is asymptoticallydistributed as a chi-squared under the assumption of multivariate normality (Mitchell, 1992). However, a chi-squared testto evaluate the goodness-of-fit of a SEM requires a multinormal distribution and, under standard field data, usually

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produces error failures. Discrepancies between this test and other goodness of fit indexes are relatively usual. In these casesdiscarding the chi-squared test is recommended and more accurate tests, such as the normed fit index (NFI) and thegoodness-of-fit index (GFI) (Iriondo et al., 2003) should be considered. GFI and NFI range between 0 and 1, with values40.90 indicating a good fit (Bentler, 1989). We used multivariate Wald tests to assess the significance of individual pathcoefficients. This test locates the set of path coefficients that can be considered zero without worsening the fit(i.e., significantly increasing the w2) of the model (Bentler, 1989). SEM analysis was performed with the CALIS procedure ofthe SAS statistical software package (SAS Institute, 1990).

2.5.2. Topography

Differences in soil properties and rabbit and sheep abundances between topography classes were assessed with one-way ANOVA and repeated measures ANOVAs for variables recorded seasonally. Type III sums of squares was used since thedesign was unbalanced. All variables were tested for normality and homogeneity of variances. Log or square-roottransformations were performed when necessary. Post-hoc tests (Tukey-test, po0.05) were used to test which groupsdiffered significantly.

3. Results

Fluctuations in both green cover and distance to water throughout the year illustrate the marked seasonality in resourceavailability of our study area. Green cover varied between 1 and 97% (mean7SE; 33.971.9, n ¼ 220) in spring, between 0%and 39% (mean7SE; 2.3370.34, n ¼ 220) in summer and between 3% and 98% (mean7SE; 46.971.7, n ¼ 220) in winter(F ¼ 246.24, po0.001). The average distance of each sampling point to water varied between 0 and 99 m (mean7SE;81.372.0, n ¼ 220) in spring, between 3 and 135 m (mean7SE; 109.472.7, n ¼ 220) in summer and between 0 and 96 m(mean7SE; 53.272.4, n ¼ 220) in winter (F ¼ 131.94, po0.001).

3.1. Path analysis

3.1.1. Model fit

GFI and NFI suggested a good adjustment for rabbit and sheep models in spring and winter, as these indices weregreater than 0.90, indicating a good fit compared to a null model that assumes independence between variables. Insummer, the rabbit model had relatively poor GFIs and NFIs but close to 0.90, suggesting a reasonable adjustment (Table 1).

3.1.2. Common links for rabbit and sheep models

Soil fertility, soil moisture and soil stoniness presented a similar pattern within the three seasons as, for everyrelationship, the path coefficients always had the same sign and in most cases, a similar value (Fig. 2). In all models, foodabundance and food quality were strongly predicted by soil moisture. Soil fertility was a good predictor of food quality inthe three seasons and a good predictor of food abundance in spring. Soil stoniness only predicted food abundance in winterand with negative sign. The correlation between soil moisture and water distance resulted negative, since a greaterdistance from a water source means lower soil moisture content.

3.1.3. Rabbit models

The best predictors for rabbit abundance changed seasonally (Fig. 2). In spring, food quality, with a negative sign, anddensity of warren entrances were the only significant predictors of rabbit abundance. In summer, they changed to foodabundance, food quality, now positive, and woody vegetation cover. In winter, food abundance, food quality, again withnegative sign, and density of warren entrances were the significant predictors. Note that the spring and winter models weresimilar with the exception of food abundance, that had stronger effects on rabbit abundance in winter. As hypothesized, soilmoisture and soil stoniness inversely predicted density of warren entrances, but contrary to our expectations, woodyvegetation cover had no effect on warrens. Distance to drinking water did not affect rabbit abundance in any season.

3.1.4. Sheep models

Food abundance, food quality and sheepfold distance were the main significant predictors of sheep abundance in spring(Fig. 2). Of these, food abundance was the strongest predictor, whereas food quality and sheepfold distance had a negativeinfluence on sheep abundance. In winter, food abundance and sheepfold distance, both with a similar path coefficient, werethe only significant predictors of sheep abundance. Note that food abundance in the sheep model was a much strongerpredictor than in the rabbit model. Woody vegetation cover had no effects, and as in the rabbit model, distance to drinkingwater did not affect sheep abundance.

3.2. Topography

Soil Fertility varied strongly between the five topographic areas (F ¼ 29.35, po0.001), reaching the highest values in flatareas in mid-slope and wet lowlands (Fig. 3a). Soil moisture fluctuated seasonally in the five topographic areas (season:

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Table 1Model fit parameters: normed fit index (NFI), goodness of fit index (GFI)

GFI NFI

Rabbit spring 0.93 0.93

Rabbit summer 0.89 0.85

Rabbit winter 0.92 0.91

Sheep spring 0.93 0.93

Sheep winter 0.90 0.91

M. Rueda et al. / Journal of Arid Environments 72 (2008) 1698–1708 1703

F ¼ 448.68, po0.001; topography: F ¼ 107.185, po0.001; season� topography: F ¼ 43.31, po0.001), being highest in wetlowlands in the three seasons (Fig. 3b). Soil stoniness was rather similar in the five topographic areas except in wetlowlands where it had the lowest value (F ¼ 25.09, po0.001) (Fig. 3c).

In spring and winter, rabbits were significantly less abundant in wet lowlands (Fig. 4). In summer, rabbits were moreabundant in flat areas in mid-slope, and wet lowlands than in highlands and slopes (season: F ¼ 40.04, po0.001;topography: F ¼ 3.61, p ¼ 0.007; season� topography: F ¼ 5.95, po0.001). Sheep were significantly less abundant inuplands and slopes in spring, whereas in winter sheep also avoided wet lowlands (season: F ¼ 5.82, p ¼ 0.017; topography:F ¼ 17.11, po0.000; season� topography: F ¼ 1.08, p ¼ 0.364) (Fig. 4).

Slopes were the areas with the most warrens and warren entrances (8.88 and 83.43 warren entrances/ha), followed byuplands and lowlands, with a similar number of warrens (around 5.70 warrens/ha) but a different number of warrenentrances (57.33/ha in uplands, and 34.50/ha in lowlands). Flat areas in mid-slope and wet lowlands had the lowestnumber of warrens and warren entrances (around 2.50 and 12.50 warren entrances/ha).

4. Discussion

By using a broad scale approach, we have shown that herbivore habitat use is highly influenced by seasonal variations inresources, and that different herbivores respond to seasonal changes in different ways. The great importance that soilmoisture had as a predictor of food abundance and quality highlights the significance of water dynamics and topographyfor primary productivity in these semi-arid ecosystems, and consequently for the availability of food resources forherbivores. In this sense, results showed that in Mediterranean ecosystems the summer period and topography representthe main determinants of the largest temporal and spatial variations in the habitat selection of large and small herbivores.Note that only rabbit habitat use was analysed in summer, as sheep are traditionally translocated as consequence of thedepletion in herbaceous vegetation caused by the summer drought. With regard to SEM, the multiplicity of effects and therelationships between factors imply that herbivore habitat use is better understood using integrated approaches ratherthan considering factors separately. As a result, we obtained a global picture of the factors affecting the process under studyand clarified their relative importance.

4.1. Factors affecting small herbivore habitat use

For rabbits, the selection of foraging areas was driven by predation risk minimisation, food abundance and foodquality, but the importance of these factors changed seasonally. In spring and winter, rabbits foraged close to warrens.Throughout the system, slopes were the areas where we found more and larger warrens. This means that warren location,usually in drier sites with low food quality, should generate a conflict between the need for high quality foraging groundsand a good breeding and protective environment. This conflict can be solved in spring and winter when most vegetationaround warrens is green and relatively abundant, but not in summer. Warren location also explains why rabbits do not useproductive wet lowland areas, as these are relatively far away from warrens and are more frequently inundated,particularly in winter and early spring. The negative link between food quality and rabbit abundances in spring and winterconfirms this fact, since lowlands are the areas with the highest values of food quality (Perez Corona et al., 1998; Vazquezde Aldana et al., 2000). Rabbits also tend to avoid dense and high standing pastures, selecting foraging areas with shorterand sparser vegetation cover (Iason et al., 2002). The predictive power of food abundance in winter can be related to theneed for extra food to cope with increased metabolic demands at the start of the breeding season which, in Mediterraneantype climates, commences after the first autumn rains (Gonc-alvez et al., 2002).

In summer, lack of water constrains environmental suitability; most of the vegetation is dry and food becomes a limitingand extremely scarce resource. In addition, competition for food increases, as the rabbit population has grown rapidly as aconsequence of reproduction. This results in a change in habitat selection. First, the link between food abundance/qualityand rabbit abundance acquires a positive significance. Second, the relationship with warrens disappears, and a relationshipwith woody vegetation appears, i.e., now rabbits prefer to forage close to woody vegetation and/or on the woody vegetationitself. In the absence of water, rabbits need to consume green food to survive (Hayward, 1961). Therefore, they are forced to

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0.56

Rabbit abundance

Food abundance

Food quality

Water distance Soil moisture

Woodyvegetationcover

Warrenentrances

Soil fertility

Soil stoniness

U

U

U

U

- 0.24*

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0.03

0.31***

0.15**

0.13**0.65***

- 0.21**

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0.80***

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0.07

0.10

0.61

0.44

0.94

Food abundance

Food quality

Soil moisture

Woody vegetation cover

Warren entrances

Soil stoniness

-

-

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Sheep abundance

Food abundance

Food quality

Water distance Soil moisture

Woody vegetation cover

Sheepfold distance

Soil fertility

Soil stoniness

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0.71 ***0.51

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Food abundance

Food quality

Water distance

Woody vegetation cover

Sheepfold distance

Soil stoniness

Rabbit abundance

Food abundance

Food quality

Waterdistance Soil moisture

Woody vegetation cover

Warrenentrances

Soil fertility

Soil stoniness

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Food abundance

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Food abundance

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Woody vegetation cover

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Food abundance

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Water distance Soil moisture

Woody vegetation cover

Sheepfold distance

Soil stoniness

Fig. 2. Path model representations for factors that determine seasonal rabbit and sheep abundances: (a) rabbit abundance in spring, (b) rabbit abundance

in summer, (c) rabbit abundance in winter, (d) sheep abundance in spring, (e) sheep abundance in winter. Model for sheep abundances in summer was not

tested because sheep were not present in the system. One-headed arrows represent causal relationships while two-headed arrows represent correlations.

Positive effects are indicated by solid lines and negative effects by broken lines. Arrow widths are proportional to path coefficient magnitude.

Standardised path coefficients significantly different from 0 are marked with asterisks (*po0.05, **po0.01, ***po0.001). U represents the unexplained

variance of dependent variables.

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venture further away from warrens, toward flat areas and lowlands, where some perennial vegetation remains green.Traditional mowing of wet lowland areas at the beginning of the summer leads to the reduction of vegetation height,facilitating the use of these zones by this small herbivore. Use of open wet lowlands in summer may imply a higherperceived predation risk but nutritional needs seem to be shifting the perceived predation risk/foraging balance during this

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Fig. 3. Differences in indirect soil factors between the five topographic classes (1 ¼ highlands; 2 ¼ slopes; 3 ¼ flat areas in mid-slope; 4 ¼ lowland;

5 ¼ wet lowlands) in spring, summer and winter. (a) Mean (7SE) soil fertility (g barley), (b) mean (7SE) soil moisture (%), (c) mean (7SE) soil stoniness

(%). Different letters indicate statistical differences (Tukey-test, po0.05).

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Fig. 4. Differences in rabbit and sheep pellet densities (mean no. pellets m�2 month�17SE) between the five topographic classes (1 ¼ highlands,

2 ¼ slopes, 3 ¼ flat areas in mid-slope, 4 ¼ lowland, 5 ¼ wet lowlands) in spring (a), summer (b) and winter (c) for rabbits and spring (d) and winter (e)

for sheep. Summer is not represented in the sheep figure since they were absent from the system in this season. Different letters indicate statistical

differences (Tukey-test, po0.05).

M. Rueda et al. / Journal of Arid Environments 72 (2008) 1698–1708 1705

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resource-limited period. The abundance of green perennial species in summer does not seem enough to support the highrabbit densities found in our study area, especially taking into account that pastures usually become dry long before thefirst autumn rains. Consequently, rabbits resort to consuming woody twigs and bark which may be moist enough to meettheir water requirements, but contain insufficient digestive energy for maintenance (Cooke, 1982). This apparent drawbackmay be overcome by rabbits through caecotrophy, which becomes a valuable selective trait under Mediterranean semi-aridconditions.

4.2. Factors affecting large herbivore habitat use

Selection of foraging areas for sheep was mainly influenced by food abundance. However, sheep did not preferentiallyselect highly productive wet lowland areas to forage, and they even avoided these areas in winter. In our study, thesheepfold acted both as nocturnal refuge and as the main water source. Free-standing water is the principal focus aroundwhich most of the larger domestic ungulates orientate their foraging strategies (Coleman et al., 1989) and grazing intensityis reduced with longer distances to water points (Stuth, 1991). Although wet lowlands may be suitable for grazing, they arefurther away from the sheepfold (mean: 840 m) than other areas, and grazing pressure is significantly reduced at distancesgreater than 500 m from the sheepfold (Rebollo, 1996). Also, it is probable that sheep avoid foraging in the most productiveareas because grazing becomes less efficient when vegetation reaches its highest standing crop (Van de Koppel et al., 1996).Sheep are driven away (transhumance) from dehesa pastures with the arrival of summer, so it is impossible to know theresponse of our large herbivore to summer shortages in pasture availability.

Our study shows how seasonal changes modify the relative importance of the main documented predictions for largeand small herbivores in relation to food quantity, quality and predation risk perception, and it sheds new light on this facetof herbivore foraging ecology. For instance, food quality, which is recognised as an important factor influencing habitatselection for small herbivores (Belovsky, 1997; Demment and Van Soest, 1985; Olff et al., 2002), was only significant insummer. Moreover, perceived predation risk strongly constrains small herbivore habitat use (Krebs et al., 1999) but ourresults show that this happens only when food is not a limiting resource, i.e., in spring and winter. The interaction of bodysize and digestive system can complicate matters further. Compared with ruminants (sheep), hindgut-fermenters (rabbit)faster throughput is an advantage which outweighs their lower digestive efficiency, particularly on poor quality foods,provided that food resources are not limiting (Illius and Gordon, 1987). Consequently, when food is more abundant (springand winter), our small herbivore behaves as a more opportunistic forager whereas when food is limited (summer) itprobably becomes more selective. Several studies have found seasonal changes in the diet of wild rabbits (Gary et al., 2007;Martins et al., 2002). In addition, as the sheepfold is located in flat areas in mid-slope, high concentrations of livestock dungand urine could be increasing soil fertility. This suggests that preferential use by sheep for these areas in spring and wintercan facilitate its use by rabbits in summer. During spring and winter, our small and large herbivores overlapped in twoareas (flat areas in mid-slope and dry lowlands) where they could be competing for the same foraging resources. This isrelevant because rabbits, considered a keystone species in the Iberian Peninsula, have declined massively in the lastdecades (e.g. Virgos et al., 2007) and consequently livestock management and rabbit conservation strategies could be inconflict if both herbivores compete for the same food. Since the predictors influencing rabbit and sheep foraging habitat useare different, herbivore competition does not seem a problem. Also, differences in body size, digestive system and theinfluence of dental arcade morphology on feeding efficiency (Demment and Van Soest 1985; Illius and Gordon, 1987) areadaptations that may lead rabbits and sheep to use different food resources although foraging in similar areas. However,diet selection studies in our study site are necessary to confirm this.

The high patchiness and species richness characteristic of dehesas may favour a variety of vertebrate herbivores,generalists and specialists, independent of each other (Cromsigt and Olff, 2006), i.e., anatomical differences would allowspecies coexistence if ecosystems are highly heterogeneous. One of the drivers of dehesa heterogeneity is the promotion oflow intensity traditional land uses. Traditional management practices, including moderate livestock grazing, are essentialto sustain a mosaic of pastures and scrub, preferred rabbit habitats, and allow them to adapt to seasonal changes inresources. For instance, mowing in the early summer enables rabbit use of lowland areas at the time of lowest foodavailability. Habitat diversity may greatly improve the viability of herbivore populations living under the unpredictableclimatic conditions of the Mediterranean region. Thus, we agree with other authors (Beaufoy, 1998; Dıaz et al., 1997) thatmaintaining traditional management in dehesas seems to be crucial for the preservation of their wildlife.

Acknowledgments

We are grateful to G. Garcıa, F. Saura and D. Polanco for their help during field work; L. Perez for advice with soil sampleprocessing; J.M. de Miguel for help with the topographical classification of the dehesa; to the management of ‘Dehesa SantoAngel de la Guarda’ for providing access to the property; and to the CICYT Projects REN2000-0789 and REN2003-05553which funded this study. Thanks are owed to A.L. Pintor and O. Godoy for helpful comments and suggestions. Dr.D. Eldridge and two anonymous referees helped improve an earlier version of this manuscript. During this research M.R.was supported by a predoctoral FPI studentship of the Spanish MEC and from University of Alcala. L.G.B was supported by apredoctoral FPI studentship from the Madrid Autonomous Region authority.

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References

Bailey, R.E., Putman, R.J., 1981. Estimation of fallow deer (Dama dama) populations from faecal accumulation. Journal of Applied Ecology 18, 697–702.Banks, P.B., Hume, I.D., Crowe, O., 1999. Behavioural, morphological and dietary response of rabbits to predation risk from foxes. Oikos 85, 247–256.Bartolome, J., Franch, J., Plaixats, J., Seligman, N.G., 1998. Diet selection by sheep and goats on Mediterranean heath-woodland range. Journal of Range

Management 51, 383–391.Beaufoy, G., 1998. The EU Habitats Directive in Spain: can it contribute effectively to the conservation of extensive agro-ecosystems? Journal of Applied

Ecology 35, 974–978.Belovsky, G.E., 1997. Optimal foraging and community structure: the allometry of herbivore food selection and competition. Evolutionary Ecology 11,

641–672.Bentler, P.M., 1989. EQS structural equations program manual. BMDP Statistical Software.Bhadresa, R., 1977. Food preferences of rabbits Oryctolagus cuniculus L. at Holkham sand dunes, Norfolk. Journal of Applied Ecology 14, 287–291.Chapuis, J.L., 1990. Comparation of the diets of two sympatric lagomorphs, Lepus europaeus (Pallas) and Oryctolagus cuniculus (L.) in an agroecosystem of

the Ile-de-France. Mammalian Biology 55, 176–185.Coleman, S.W., Forbes, T.D.A., Stuth, J.W., 1989. Measurements of the plant-animal interface in grazing research. In: Martin, G.C. (Ed.), Grazing Research

Methods. American Society of Agronomy, pp. 37–52.Cooke, B.D., 1982. A shortage of water in natural pastures as a factor limiting a population of rabbits, Oryctolagus cuniculus (L.), in arid, north-eastern south

Australia. Wildlife Research 9, 465–476.Cougenhour, M.B., 1991. Spatial components of plant-herbivore interactions in pastoral ranching and native ungulate ecosystems. Journal of Range

Management 44, 530–542.Cromsigt, J.P.G.M., Olff, H., 2006. Resource partitioning among savanna grazers mediated by local heterogeneity: an experimental approach. Ecology 87,

1532–1541.Demment, M.W., Van Soest, P.J., 1985. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. American Naturalist 125,

541–672.Dıaz, M., Campos, P., Pulido, F.J., 1997. The Spanish dehesas: a diversity of land-use and wildlife. In: Pain, D., Pienkowsky, M. (Eds.), Farming and Birds in

Europe: The Common Agricultural Policy and its Implications for Bird Conservation. Academic Press, New York, pp. 178–209.Figueroa, M.E., Davy, A.J., 1991. Response of Mediterranean grassland species to changing rainfall. Journal of Ecology 79, 925–941.Gary, R.M., Twigg, L.E., Zampichelli, L., 2007. Seasonal changes in the diet of the European rabbit (Oryctolagus cuniculus) from the three different

Mediterranean habitats in south-western Australia. Wildlife Research 34, 25–42.Gea-Izquierdo, G., Munoz-Igualada, J., San Miguel-Ayanz, A., 2005. Rabbit warren distribution in relation to pasture communities in Mediterranean

habitats: consequences for management of rabbit populations. Wildlife Research 32, 723–731.Gonc-alvez, H., Alves, P.C., Rocha, A., 2002. Seasonal variation in the reproductive activity of the wild rabbit (Oryctolagus cuniculus algirus) in a

Mediterranean ecosystem. Wildlife Research 29, 165–173.Gross, J.E., Zank, C., Hobbs, N.T., Spalinger, D.E., 1995. Movement rules for herbivores in spatially heterogeneous environments: responses to small scale

pattern. Landscape Ecology 10, 209–218.Hayward, J.S., 1961. The ability of the wild rabbit to survive conditions of water restriction. Wildlife Research 6, 160–175.Hirakawa, H., 2001. Coprophagy in leporids and other mammalian herbivores. Mammal Review 31, 61–80.Holmes, W.G., 1991. Predation risk affects foraging behaviour of pikas: observational and experimental evidence. Animal Behaviour 42, 111–119.Iason, G.R., Manso, T., Sim, D.A., Hartley, F.G., 2002. The functional response does not predict the local distribution of European Rabbits (Oryctolagus

cuniculus) on grass swards: experimental evidence. Functional Ecology 16, 394–402.Iborra, O., Lumaret, J.P., 1997. Validity limits of the pellet group counts in wild rabbit (Oryctolagus cuniculus). Mammalia 61, 205–218.Illius, A.W., Gordon, I.J., 1987. The allometry of food intake in grazing ruminants. Journal of Animal Ecology 56, 989–999.Iriondo, J.M., Albert, M.J., Escudero, A., 2003. Structural equation modelling. An alternative for assessing causal relationships in threatened plant

populations. Biological Conservation 113, 367–377.Jarman, P.J., Sinclair, A.R.E., 1979. Feeding strategy and the pattern of resource partitioning in African ungulates. In: Sinclair, A.R.E., Norton-Griffiths, M.

(Eds.), Serengeti: Dynamics of an Ecosystem. University of Chicago Press, pp. 130–164.Jofree, R., Rambal, S., Ratte, J.P., 1999. The dehesa of Southern Spain and Portugal as a natural ecosystem mimic. Agroforestry System 45, 57–59.Kolb, H.H., 1991. Use of burrows and movements by wild rabbits (Oryctolagus cuniculus) in an area of hill grazing and forestry. Journal of Applied Ecology

28, 892–905.Kotler, B.P., Brown, J.S., Hasson, O., 1991. Factors affecting gerbil foraging behaviour and rates of owl predation. Ecology 72, 2249–2260.Krebs, C.J., Sinclair, A.R.E., Boonstra, R., Boutin, S., Martin, K., Smith, J.N.M., 1999. Community dynamics of vertebrate herbivores: how can we untangle the

web? In: Olff, H., Brown, V.K., Drent, R.H. (Eds.), Herbivores: Between Plants and Predator. Blackwell Science, Oxford, pp. 447–473.Lynch, J.J., Hinch, G.N., Adams, D.B., 1992. The behavior of sheep. Biological principles and implications for production. CAB International.Martins, H., Milne, J.A., Rego, F., 2002. Seasonal and spatial variation in the diet of the wild rabbit (Oryctolagus cuniculus L.) in Portugal. Journal of Zoology

258, 395–404.Mitchell, R.J., 1992. Testing evolutionary and ecological hypothesis using path analysis and structural equation modelling. Functional Ecology 6,

123–129.Moro, M.J., Pugnaire, F.I., Haase, P., Puigdefebregas, J., 1997. Effects of the canopy of Retama sphaerocarpa on its understory in a semiarid environment.

Functional Ecology 11, 425–431.Morrison, M.L., Marcot, B.G., Mannan, R.W., 1998. Wildlife-habitat relationships. Concepts and applications. In: Morrison, M.L., Marcot, B.G., Mannan,

R.W. (Eds.), Measurement of Wildlife Habitat: What to Measure and How to Measure. University of Wisconsin Press, pp. 139–167.Mysterud, A., Langvatn, R., Yoccoz, N.G., Stenseth, N.Chr., 2001. Plant phenology, migration and geographical variation on body weight of a large herbivore:

the effect of a variable topography. Journal of Animal Ecology 70, 915–923.Olff, H., Ritchie, M.E., 1998. Effects of herbivores on grassland plant diversity. Trends in Ecology and Evolution 13, 261–265.Olff, H., Ritchie, M.E., Prins, H.H.T., 2002. Global environmental controls of diversity in large herbivores. Nature 415, 901–904.Owen-Smith, R.N., 1988. Megaherbivores: The Influence of Very Large Body Size on Ecology. Cambridge University Press, Cambridge.Palomares, F., 2001. Comparison of three methods to estimate rabbit abundance in a Mediterranean environment. Wildlife Society Bulletin 29, 578–585.Palomares, F., 2003. The negative impact of heavy rains on the abundance of a Mediterranean population of European rabbits. Mammalian Biology 68,

224–234.Palomares, F., Delibes, M., 1997. Predation upon European rabbits and their use of open and closed patches in Mediterranean habitats. Oikos 80, 407–410.Parer, I., Libke, J.A., 1985. Distribution of rabbit, Oryctolagus cuniculus, warrens in relation to soil type. Wildlife Research 12, 387–405.Perez Corona, M.E., Vazquez de Aldana, B.R., Garcıa Criado, B., Garcıa Ciudad, A., 1998. Variations in nutritional quality and biomass production of semiarid

grasslands. Journal of Range Management 51, 570–576.Peters, R.H., 1983. The Ecological Implications of Body Size. Cambridge University Press, Cambridge.Rebollo, S., 1996. Analisis de la estrategia de pastoreo de pequenos rumiantes domesticos considerando distintas escalas espaciales. Ph.D. Thesis,

Universidad de Leon.San Miguel, A., 2001. Pastos Naturales Espanoles. Mundi-Prensa, Madrid.SAS Institute, 1990. SAS/STAT user’s guide. Release 6.04. SAS Institute.

ARTICLE IN PRESS

M. Rueda et al. / Journal of Arid Environments 72 (2008) 1698–17081708

Schwartz, C.C., Ellis, J.E., 1981. Feeding ecology and niche separation in some native and domestic ungulates on the shortgrass prairie. Journal of AppliedEcology 18, 343–353.

Sinclair, A.R.E., 1975. The resource limitation of trophic levels in tropical grassland ecosystems. Journal of Animal Ecology 44, 497–520.Stuth, J.W., 1991. Foraging behaviour. In: Heitschmidt, R.K., Stuth, J.W. (Eds.), Grazing Management: An Ecological Perspective. Timber Press, pp. 65–83.Traill, L.W., 2004. Seasonal utilization of habitat by large grazing herbivores in semi-arid Zimbabwe. South African Journal of Wildlife Research 34, 13–24.Van de Koppel, J., Huisman, J., Van der Wal, R., Olff, H., 1996. Patterns of herbivory along a gradient of primary productivity: an empirical and theoretical

investigation. Ecology 77, 736–745.Vazquez de Aldana, B.R., Garcıa-Ciudad, A., Perez-Corona, M.E., Garcıa-Criado, B., 2000. Nutritional quality of semi-arid grassland in western Spain over a

10-year period: changes in chemical composition of grasses, legumes and forbs. Grass Forage Science 55, 209–220.Virgos, E., Cabezas-Dıaz, S., Lozano, J., 2007. Is the wild rabbit (Oryctolagus cuniculus) a threatened species in Spain? Sociological constrains in the

conservation of species. Biodiversity and Conservation 16, 3489–3504.Wheeler, S.H., King, D.R., Robinson, M.H., 1981. Habitat and warren utilization by the European rabbit, Oryctolagus cuniculus (L.), as determined by radio-

tracking. Wildlife Research 8, 581–588.Wilmshurst, J.F., Fryxell, J.M., Bergman, C.M., 2000. The allometry of patch selection in ruminants. Proceedings of the Royal Society B—Biological Sciences

267, 345–349.