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doi:10.1016/j.ba

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Basic and Applied Ecology 10 (2009) 151–160 www.elsevier.de/baae

Ungulates, rodents, shrubs: interactions in a diverse

Mediterranean ecosystem

Alberto Munoz�, Raul Bonal1, Mario Dıaz2

Departamento de Ciencias Ambientales, Facultad de Ciencias del Medio Ambiente, Universidad de Castilla-La Mancha,

Avda. Carlos III s/n, E-45071 Toledo, Spain

Received 6 November 2006; accepted 28 January 2008

Abstract

Ungulate abundance has increased dramatically worldwide, having strong impacts on ecosystem functioning. Highungulate densities can reduce the abundance, diversity and/or body condition of small mammals, which has beenattributed to reductions in cover shelter and food availability by ungulates. The densities of wild ungulates haveincreased recently in high-diversity Mediterranean oak ecosystems, where acorn-dispersing small rodents are keystonespecies. We analysed experimentally ungulate effects on seed-dispersing rodents in two types of oak woodland: a forestwith dense shrub layer and in dehesas lacking shrubs. Ungulates had no significant effects on vegetation structure orrodent body mass, but they reduced dramatically rodent abundance in the lacking-shrub dehesas. In the forest,ungulates modified the spatial distribution and space use of rodents, which were more concentrated under shrubs in thepresence than in the absence of ungulates. Our results point to the importance of shrubs in mediating ungulate–rodentinteractions in Mediterranean areas, suggesting that shrubs serve as shelter for rodents against ungulate physicaldisturbances such as soil compaction, trampling or rooting. Holm oak seedling density was reduced by ungulates indehesa plots, but not in forests. Acorn consumption by ungulates may reduce oak recruitment to a great extent.Additionally, we suggest that ungulates may have a negative effect on oak regeneration processes by reducing theabundance of acorn-dispersing rodents. Given that shrubs seem to mediate ungulate effects on acorn dispersers,controlled shrub encroachment could be an effective alternative to ungulate population control or ungulate exclusionfor the sustainability of the high-diversity Mediterranean oak ecosystems.r 2008 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Zusammenfassung

Die Haufigkeit von Huftieren hat weltweit dramatisch zugenommen und starke Auswirkungen auf dasFunktionieren von Okosystemen. Hohe Huftierdichten konnen die Haufigkeit, die Diversitat und/oder die korperlicheVerfassung von kleineren Saugetieren verringern. Dies wird auf die Reduktion der schutzenden Deckung und derNahrungsverfugbarkeit zuruckgefuhrt. Die Dichten wilder Huftiere haben in jungster Zeit in hochdiversenmediterranen Eichenokosystemen zugenommen, in denen kleine Nagetiere, welche die Eicheln verbreiten,Schlusselarten darstellen. Wir untersuchten experimentell die Effekte, die Huftiere auf samenverbreitende Nagetiere

e front matter r 2008 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

ae.2008.01.003

ing author. Tel.: +34925 268800; fax: +34 925 268840.

ess: alberto.mmmunoz@uclm.es (A. Munoz).

Investigacion en Recursos Cinegeticos (CSIC-UCLM-JCCM) Ronda de Toledo s/n, 13071 Ciudad Real, Spain.

ess: Instituto de Recursos Naturales (IRN-CCMA-CSIC), c/Serrano 115 bis, 28006 Madrid, Spain.

ARTICLE IN PRESSA. Munoz et al. / Basic and Applied Ecology 10 (2009) 151–160152

haben, in zwei Typen von Eichenwaldern: in einem Wald mit einer dichten Strauchschicht und in Dehesas, die uberkeine Strauchschicht verfugen. Die Huftiere hatten keinerlei Effekte auf die Vegetationsstruktur oder auf dieKorpermasse der Nagetiere, reduzierten aber in dramatischem Ausmaß die Haufigkeit der Nagetiere in dengebuschlosen Dehesas. In den Waldern veranderten die Huftiere die raumliche Verteilung und die Raumnutzung derNagetiere, die bei Anwesenheit von Huftieren mehr unter den Gebuschen konzentriert waren als in ihrer Abwesenheit.Unsere Ergebnisse deuten auf die Wichtigkeit von Gebuschen bei der Vermittlung der Huftier-Nagetier-Beziehung inmediterranen Gebieten hin und lassen vermuten, dass Gebusche den Nagetieren als Schutz vor physischenAuswirkungen der Huftiere, wie Bodenverdichtung, Vertritt oder Entwurzlung, dienen. Die Keimlingsdichte derSteineiche war in den Probeflachen der Dehesas, aber nicht in denen der Walder, durch die Huftiere reduziert. DerEichelfraß durch Huftiere konnte den Eichennachwuchs in großerem Maße reduzieren. Zusatzlich vermuten wir, dassdie Huftiere einen negativen Effekt auf den Eichennachwuchs haben konnten, indem sie die Haufigkeiten der Nagetierereduzieren, die Eicheln verbreiten. Unter der Voraussetzung, dass die Gebusche die Auswirkungen der Huftiere auf dieEichelverbreiter beeinflussen, konnte fur die Nachhaltigkeit der hochdiversen mediterranen Eichenokosysteme einkontrolliertes Vordringen von Gebuschen eine effektive Alternative zu einer Kontrolle der Huftierpopulation odereinem Ausschluss von Huftieren sein.r 2008 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Keywords: Mediterranean; Oak regeneration; Rodents; Seed dispersal; Vegetation cover; Ungulate impacts

Introduction

The abundance of ungulates has increased sharplyworldwide in recent decades. Ungulate impacts onecosystem function could be dramatic, although theyhave been poorly quantified (Cote, Rooney, Tremblay,Dussault, & Waller, 2004). A number of studies haverecently documented negative effects of high densities ofungulates, both wild and domestic, on the abundance,diversity and body mass of small mammals (Caro, 2002;Keesing, 1998; Moser & Witmer, 2000; Schmidt, Olsen,Bildsøe, Sluydts, & Leirs, 2005; Smit et al., 2001; Torreet al., 2007). These negative effects have been argued tobe mediated by an impoverishment of habitat quality. Inthe first place, ungulates can decrease shrub cover, thusincreasing the exposure of small mammals to predators(Moser & Witmer, 2000; Smit et al., 2001). Second,ungulates can reduce food availability for small mam-mals (Caro, 2002; Keesing, 1998; Schmidt et al., 2005),leading to reduced body mass (Keesing, 1998).

Ungulate densities have increased sharply in Medi-terranean ecosystems in recent decades, due to thegrowing demand for big game hunting (Dıaz, Campos,& Pulido, 1997). The Mediterranean ecosystems aredominated by oaks, which depend to a great extent onacorn-dispersing rodents for regeneration (Goheen &Swihart, 2003; Jensen & Nielsen, 1986; Pulido & Dıaz,2005). Thus, acorn-dispersing rodents are consideredkeystone species in the functioning of Mediterraneanoak ecosystems (Dıaz, Pulido, & Maranon, 2003; Pulido& Dıaz, 2005). However, the effects of wild ungulates onacorn-dispersing rodents have not been studied so far.This kind of study is needed since these habitats are ofmain conservation interest and are among the 25biodiversity hotspots of the world (Myers, Mittermeier,Mittermeier, da Fonseca, & Kent, 2000).

In this study, we analyse the effects of wild ungulateson small rodent populations in representative Mediter-ranean ecosystems of the Iberian Peninsula. The studywas carried out in two typical Mediterranean woodlandtypes: (1) oak forests, with a well developed shrub layer,and (2) dehesas, human-made, savannah-like woodlandsconsisting of scattered oaks within a grassland matrixand with very few shrubs (Dıaz et al., 1997; Pulido &Dıaz, 2005). We explored the importance of shrubs(Moser & Witmer, 2000; Smit et al., 2001) and a shared-food source, acorns (Caro, 2002; Keesing, 1998; Schmidtet al., 2005), in mediating ungulate–rodent interactions.If shrub cover were important, we would expect lowerungulate impacts on rodents in shrubby habitats (i.e.forests as compared to dehesas). Thus, we tested theeffects of ungulates on vegetation structure and rodentpopulations both in forests and dehesas. On the otherside, if food were important, we would expect areduction of rodent body mass where ungulates arepresent (Keesing, 1998) and also that changes in theavailability of acorns would modify the impact ofungulates on rodent abundance. Hence, we testedungulate effects on rodent abundance and body massduring the acorn drop season, when acorns constitutethe bulk of the diet for both ungulates and rodents(Dıaz, Gonzalez, Munoz-Pulido, & Naveso, 1993;Focardi, Capizzi, & Monetti, 2000; Leiva & Fernan-dez-Ales, 2003; Munoz & Bonal, 2007, 2008; Pulido &Dıaz, 2005), and in spring, when there are no acorns atall because they have already been eaten or germinated(Bonal & Munoz, 2007; Munoz & Bonal, 2008). Finally,we analysed the effects of ungulates on oak recruitmentin both types of woodland, and discussed whether thedirect effects of ungulates on acorn-dispersing rodentsmay also lead to indirect effects in oak recruitment inthe Mediterranean oak woodlands.

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Materials and methods

Study area and study species

The study was conducted in the Cabaneros NationalPark (Ciudad Real province, Central Spain, 391240N,31350W), a natural reserve representative of Mediterra-nean oak forests and dehesas. In this area, forests aredominated by Holm oaks (Quercus ilex), with a meantree density of 30 trees ha�1 and a 60% shrub cover ofCistus ladanifer, Phyllirea angustifolia, Rosmarinus

officinalis and Erica arborea. Dehesas are savannah-likelandscapes, with a tree density of 14 trees ha�1, alsodominated by Holm oaks, and a shrub cover below 1%(see Pulido, Dıaz, & Hidalgo, 2001, for a comparativedescription of forests and dehesas). In the study area,dehesas were cleared from former forests in the 1960sand then used to keep a herd of some 1200 cows.Livestock rearing was abandoned afterwards in favourof big game hunting by the 1970s. Currently, nolivestock grazes inside the National Park and huntingis not allowed. The densities of red deer (Cervus elaphus)are high both in forests and dehesas (0.14 deer ha�1;Jimenez, 2004). Wild boars (Sus scrofa) and roe deer(Capreolus capreolus) can be also found in the NationalPark, but at lower densities. Two species of acorn-dispersing rodents inhabit the study area, the Algerianmouse (Mus spretus) and the wood mouse (Apodemus

sylvaticus). Both are prominent predators and dispersersof acorns during the acorn fall season (Munoz & Bonal,2007, 2008; Pulido & Dıaz, 2005).

Experimental design and rodent samplings

In 1995, ungulate exclosures were established withfences 2m tall and a 32 cm� 16 cmmesh width by theNational Park staff. The fences allow the passage ofrodent predators (red foxes Vulpes vulpes, genetsGenetta genetta, stone martens Martes foina, and wildcats Felis sylvestris mainly; Dıaz, Bonal, & Munoz,2004) as confirmed by the presence of scats at both sidesof fences (Munoz & Bonal, 2007). In the dehesa, only alarge exclosure of 30 ha was available in which weestablished eight sampling plots. In the forest, we alsoestablished eight sampling plots, but distributed in thefour small (5–7 ha) exclosures available (two samplingplots per exclosure). Forest and dehesa plots werelocated 1 km away. Each sampling plot consisted of twotrapping stations, one placed outside the ungulateexclosure and the other paired inside, both located atleast 50m away from the fence. Each trapping stationconsisted of 10 Sherman live-traps laid out in twoparallel lines of five traps with 10m between traps.Within each woodland type sampling plots wereseparated by at least 150m to ensure that each one

was an independent replicate of rodent responses toungulates, as rodent home-ranges of radio-trackedrodents were only 30–40m in diameter (unpublisheddata).

Sampling plots were permanently marked and trap-ping sessions were performed in September 2001 (only12 out of the 16 final plots), April 2003, November 2003and April 2004. Each session consisted of two con-secutive three-night trappings. In the first three-nighttrapping, we sampled half of the plots just before thenew moon. Then, we changed the traps to sample theother half of plots during three-night trapping just afterthe new moon. Hence, the traps of each sampling plotwere revised during three consecutive nights around thenew moon in order to avoid any confounding effect ofmoonlight on rodent activity and trappability (Dıaz,1992). Traps were set between 12:00 and 16:00GMTand checked between 7:00 and 9:00GMT. Each trap wasbaited with a piece of apple and a paste made of tuna inoil and flour. A piece of waterproof cotton was alsoadded to protect captured rodents from cold and rain.Rodents were identified to species, sexed, weighed usinga 100-g spring balance at checking, marked by cutting asmall piece of hair from their head, and released (seeTorre et al., 2007).

Measures of vegetation structure

In each trapping session, we measured the vegetationstructure at each trapping station in circles of 3m2

(1m radius) around each of the 10 Sherman traps. Wewere interested in analysing differences in vegetationstructure between areas with and without ungulates,not between woodland types. Thus, we used slightlydifferent methods for estimating vegetation structure ineach woodland type because of the obvious differencesbetween them (see Pulido & Dıaz, 2005; Pulido et al.,2001, for similar approaches). In the forest plots, wevisually estimated the percent cover of shrubs and herbstaller and smaller than 30 cm, adult trees, bare groundand litter. Bare ground was considered as the proportionof the sampled area which was not covered by herbs,shrubs or trees. Two observers independently estimatedcovers at several trapping stations; similar values wereobtained. In the dehesa plots, vegetation structure wasmeasured by placing a calibrated stick (to the nearest1 cm) vertically on the ground at five positions aroundtraps: one close to the trap, and four 1m away from thetrap in the four cardinal directions. We noted if the stickcontacted bare ground, herbs taller and/or smaller than30 cm and oak resprouts taller and/or smaller than30 cm, as well as whether or not the stick was under treecover. The maximum herb height was measured bynoting the highest contact on the stick (see Torre et al.,2007, for a similar procedure). Mean cover values for

ARTICLE IN PRESSA. Munoz et al. / Basic and Applied Ecology 10 (2009) 151–160154

each trapping station were computed as the percentagesof contacts with each vegetation layer out of the 50measures made (5 measures per trap� 10 traps pertrapping station), whereas maximum herb height wasaveraged from the 50 height measurements.

Seedling density

Ungulate effects on Holm oak recruitment were testedby comparing the density of current-year seedlings in thesampling plots in November 2004. We counted current-year seedlings in autumn (germination takes place inearly spring) because measures at this stage are morereliable for assessing recruitment in Mediterraneanareas. This is because in autumn the remaining seedlingshave already gone through the major bottleneck, whichis the mortality due to desiccation during the critical firstsummer drought (Pulido & Dıaz, 2005). Seedlings differclearly from resprouts, as they show clearly the marks ofthe insertion of the cotyledons, which last for at least 4years after emergence (Dıaz et al., 1997; Pulido & Dıaz,2005). In dehesa plots, we counted the number ofseedlings emerged under tree canopies and in a radialarea extending 4m beyond the tree canopy border,which is the area where rodents usually cache the acorns(Munoz, 2005). Counts were made on 20 oaks chosenrandomly from the eight dehesa plots (10 inside and 10outside the exclosures). In forest plots, we counted theseedlings in transects of 4� 12m, as trees show aclumped distribution and thus the method used indehesas would have given non-independent estimates ofseedling density. In the forest, 20 transects wererandomly placed at eight plots (10 inside and 10 outsidethe exclosures). Comparisons were made betweenexclosure and control plots within each woodland type,but not between woodland types because of the differentmethods used to estimate seedling densities.

Data analyses

Effects of woodland type and trapping session onrodent abundance (number of rodents captured, exclu-ding recaptures) and body mass were tested with factorialANOVAs. Ungulate effects on rodents were tested with arepeated-measures ANOVA with exclosure as within-subjects factor (exclosure plots and their controls werepaired by design) and woodland type and season asbetween-subject factors. Season could not be included asa within-subject factor because (a) traps were not exactlyin the same locations during all trapping sessions and (b)several plots were not sampled in the first trappingsession (see Torre et al., 2007, for a similar approach). Inall cases, post-hoc comparisons were made with LSDtests. Pregnant females and juveniles (the latter easilyrecognisable by their grey fur and small size) were

removed from the analyses of rodent body mass, and sexwas included as a fixed factor to account for sexualdimorphism. In order to reduce the number of vegeta-tion structure variables we performed Principal Com-ponent Analyses (PCA), which were computedseparately for forest and dehesa plots. We then usedthe factor scores of each sampling plot obtained fromthe gradients as response variables in ANOVAs toanalyse the effects of ungulates on vegetation structure.The effects of vegetation structure on rodent abundancewere tested with Spearman rank correlations betweenthe factor scores and the abundance of rodents pertrapping station. Also, we tested whether the slopesdefined by these correlations differed between ungulatetreatments with tests of parallelism. Shrub cover (sum ofthe cover of shrubs smaller and taller then 30 cm) wasincluded in the PCA, but was also considered indepen-dently due to its reported strong influence on rodentdistribution and activity (Dıaz, 1992; Lagos, Contreras,Meserve, Gutierrez, & Jaksic, 1995; Torre & Dıaz,2004). To test whether rodent captures were associatedwith shrubs we used logistic regressions at the trap level,using as dependent variable whether mice were capturedor not, and as independent variable the cover of shrubs.At the level of the trapping station we correlatedmean shrub cover and number of mice captured usingSpearman rank correlations. Finally, we analysedwhether the probability of mice capture dependedon tree cover in the dehesa plots by comparing theproportions of mice caught under tree cover withthe random proportion expected on the basis of theobserved cover of trees (w2 test).

Results

Rodent abundance

Overall, we captured 125 rodents from a totalsampling effort of 3600 trap nights. The Algerian mouse(M. spretus) was the most prevalent species (109),whereas the wood mouse (A. sylvaticus) was much rarer(16). Both total rodent abundance and the abundanceof M. spretus did not change significantly betweenSeptember 2001, April 2003 and November 2003 eitherin forest or dehesa plots (P40.5), but a strong declineoccurred in both woodland types between November2003 and April 2004 (Po0.001, Table 1; Fig. 1; seeAppendix A: Fig. 1). The wood mouse was only foundin April 2003, and it was more common in forest than indehesa plots (Po0.001, Table 1).

The effects of ungulates on the abundance of allrodents and M. spretus only were conditioned by thewoodland type (Table 2). Ungulates reduced dramati-cally the abundance of M. spretus alone and rodents as a

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Table 1. Results of factorial ANOVAs testing for the effects of woodland type and trapping session on rodent abundance

Factors d.f. All rodents M. spretus A. sylvaticus

F P F P F P

Trapping session 3,112 8.50 o0.001 10.80 o0.001 4.95 o0.01

Woodland type 1,112 0.12 0.79 0.08 0.78 3.46 0.06

Trapping�woodland 3,112 0.30 0.83 0.75 0.52 3.67 0.01

No

rode

nts

/ tra

ppin

g st

atio

n

Trapping session

Sept 2001April 2003

Nov 2003April 2004

-0.5

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

Trapping session

Sept 2001April 2003

Nov 2003April 2004

Holm oak forest Dehesa

Fig. 1. Rodents captured in 30 trap nights in ungulate-grazed

(solid circles) and exclosure (open circles) plots in Holm oak

forests (left panel) and dehesa sites (right panel). Lines indicate

standard errors.

Table 2. Results of the repeated-measures ANOVA testing

for the effects of ungulates on rodent abundance in different

woodland types and seasons

Source of variation All rodents Mus spretus

F1,40 P F1,40 P

Ungulates 27.41 o0.001 26.38 o0.001

Ungulates� habitat 11.79 o0.001 14.89 o0.001

Ungulates� season 1.21 0.28 0.55 0.46

Ungulates� habitat� season 1.41 0.24 2.16 0.15

A. Munoz et al. / Basic and Applied Ecology 10 (2009) 151–160 155

whole in dehesa plots (Po0.001 in both cases), but notin forest plots (P40.2 in both cases, Table 2; Fig. 1; seeAppendix A: Fig. 1). This result did not change amongtrapping sessions or seasonally (Table 2).

Vegetation structure and space use of rodents

In the forest plots, the PCA aggregated the variablesof vegetation in three main factors (eigenvalues41)explaining 74.9% of variance. The first factor segregatedareas under and outside tree cover, the second factorsegregated bare ground from vegetation cover, and thethird factor areas under shrubs smaller than 30 cm from

the rest (Table 3; see Appendix A: Fig. 2). Vegetationvariables measured in dehesa plots were also sum-marised by three main factors (eigenvalues41), whichexplained 82.1% of variance. The first factor segregatedareas under and outside tree cover, the second factorareas covered by herbs from areas with bare ground,and the third seemed to define a gradient of herb height(Table 3; see Appendix A: Fig. 3).

In forest plots, the presence or absence of ungulateshad no effects either on the vegetation structurevariables arising from the PCA (ANOVA with thefactor scores as response variable P40.6 in all cases), oron shrub cover when considered independently(F1,52 ¼ 1.19, P ¼ 0.28). At dehesa plots, similar resultswere found for the first and second factors (ANOVAP40.7 in all cases). However, the factor which defined agradient of herb height showed significant variationamong trapping sessions and exclosure treatments(Trapping session� exclosure F3,52 ¼ 4.5, Po0.01).Herbs were significantly taller in the absence (mean7S.E.: 20.472.7 cm) than in the presence (mean7S.E.:9.670.7 cm; LSD test Po0.01) of ungulates in April2003, and also in November 2003 (19.773.9 cm vs.13.171.4 cm; LSD test Po0.01). However, herb heightdid not differ between grazed plots (36.773.8 cm) andexclosures (38.272.6 cm) in September 2001 (LSD testP ¼ 0.88) or April 2004 (20.273.9 cm vs. 18.870.8 cm;LSD test P ¼ 0.2). The strong temporal variation inherb height precluded detecting consistent spatial effectsdue to ungulate activity, as herbs grazed in seasons witha high herb height were taller than herbs not grazed inseasons with a short herb height.

The abundance of M. spretus was not correlated withthe vegetation gradients defined by the PCA either inforests or dehesas (Spearman rank correlations, p40.3in all cases), and also the slopes from these correlationswere not affected by ungulate exclosure (ANCOVA,Test of Parallelism P40.7 in all cases). In dehesa plots,no significant correlation was found between herb heightand M. spretus abundance (rs ¼ �0.06; n ¼ 22 P ¼

0.79), but a significant association was found betweenabundance of M. spretus and tree cover, as the numberof rodents captured in traps placed under trees wassignificantly higher than the expected number at random(September 2001, w21 ¼ 14:8, Po0.01; April 2003,w21 ¼ 5:19, P ¼ 0.02; November 2003, w21 ¼ 4:49,

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Table 3. Results of the PCA analyses obtained from the variables of vegetation measured in forest and dehesa plots

Woodland PCA factors Significant correlations (40.7) Variance explained (%)

+ �

Forest plots F1 Herbs4ando30 Tree, litter 32.6

F2 Bare ground Herbs4ando30 27.4

F3 30oShrubs None 14.9

Dehesa plots F1 Tree/sprouts None 35.2

F2 Bare ground Herbs4ando30 28.7

F3 Herbso30 Herbs430 18.2

A. Munoz et al. / Basic and Applied Ecology 10 (2009) 151–160156

P ¼ 0.03). In forest plots, the probability of M. spretus

being captured in a trap was significantly and positivelycorrelated with shrub cover in the presence of ungulates(Wald’s statistic ¼ 3.75, P ¼ 0.03) but not in forestexclosures (Wald’s statistic ¼ 0.53, P ¼ 0.46; Fig. 2A).At the trapping station level, the abundance of M.

spretus correlated positively with shrub cover in thepresence (rs ¼ 0.40, n ¼ 22, P ¼ 0.05) but not in theabsence of ungulates (rs ¼ �0.18, n ¼ 22, P ¼ 0.31;Fig. 2B). The slopes defined by these correlations weresignificantly different between ungulate treatments(ANCOVA, Test of Parallelism: F1,84 ¼ 9.25, Po0.01;Fig. 2B). Thus, although ungulates have no effect on thetotal abundance of M. spretus in forest plots, theymodified the local abundance and space use of thisspecies, so that rodents were more associated withshrubs in presence of ungulates.

Rodent body mass

The body mass of M. spretus was unaffected bywoodland type during the study period except inNovember 2003, when it was higher in forest (mean7S.E.: 16.8870.67 g) than in dehesa plots (11.8570.56 g;LSD, Po0.001). Ungulate effects on rodent body masscould not be tested for the dehesa plots because of thelow number of mice captured in presence of ungulates(Fig. 1B). Rodent body mass was unaffected by un-gulates in the forest plots, for both M. spretus (presenceof ungulates: 13.5470.50 g; absence of ungulates:10.270.79 g, ANOVA P40.5 in all trapping sessions),and A. sylvaticus in April 2003 (presence of ungulates:25.2471.30 g; absence of ungulates: 25.2071.24 g,ANOVA F1,12 ¼ 1.84, P ¼ 0.2).

Oak seedling density

Ungulate effects on the density of holm oak seedlingsdiffered between woodland types (ungulate presen-ce�woodland interaction: F1,36 ¼ 4.89, P ¼ 0.03). Inforest plots, the density of seedlings per m2 was similarin the presence of ungulates (mean7S.E.: 0.0270.01)

than in exclosures (0.0470.01; P ¼ 0.59). By contrast,in dehesa plots seedling density was significantly higherin exclosures (0.1470.04) than in the presence ofungulates (0.0270.01; Po0.001).

Discussion

Ungulate effects on rodents

Wild ungulates had significant impacts on rodentabundance, and their effects were influenced by thewoodland type. They reduced rodent abundance by80% in the dehesa, where shrubs are very scarce. In theforest, ungulates altered the spatial distribution ofrodents, which were more closely associated with shrubsoutside the ungulate exclosures. Thus, our results pointto the importance of shrubs in mediating ungulate–ro-dent relationships in the Mediterranean oak woodlands.

Ungulates can have negative effects on small mam-mals by reducing shrub cover, which is essential forsmall mammals as shelter against predators (Jensen,Gray, & Hurst, 2003; Lagos et al., 1995; Torre & Dıaz,2004). In North America, Moser and Witmer (2000)found that elk and cattle foraging reduced shrub layer,and both the abundance and species richness of smallmammals. In the Netherlands, Smit et al. (2001) showedthat ungulate grazing reduced small mammal densitiesdue to a decrease in the structural complexity of thevegetation. However, in our study area the exclusion ofungulates had no significant effects on vegetationstructure. Ungulate exclosure increased herb height onlyin dehesa plots in several trapping sessions, but thestrong temporal variation in herb height precludedthe detection of spatial effects due to ungulates. Also,the effects of ungulates on rodents did not changeduring the study period, and rodent abundance was notcorrelated with herb height. Thus, it is unlikely that theeffects of ungulates on rodent abundance and space usewere driven by their effects on vegetation structure.

Ungulates can also affect negatively small mammalsby reducing food availability. In East African savannas,

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% Shrub cover

No

M. s

pret

us /

trap

0 15 30 45 60 75 90 105-0.1

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

0 15 30 45 60 75 90 105

No

M. s

pret

us /

trapp

ing

stat

ion

Ungulates15 25 35 45 55 65 75 85

-0.5

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

15 25 35 45 55 65 75 85No ungulates

(A) (A)

(B) (B)

Fig. 2. Relationship between the abundance of Mus spretus and shrub cover (A) at the trap level, and (B) at the trapping station

level both in presence (left graph) and absence (right graph) of ungulates in Holm oak forests during the study period. Lines indicate

standard errors.

A. Munoz et al. / Basic and Applied Ecology 10 (2009) 151–160 157

Keesing (1998) reported reductions in the body mass ofsmall mammals due to presence of large herbivores,which reduced the quality of the food available. In ouroak woodlands, acorns are the main food resource forrodents and ungulates in autumn (Bonal & Munoz,2007; Munoz & Bonal, 2007). However, ungulates hadno effects on rodent body mass, their impact on rodentabundance was significant only in the dehesa and therewere no differences in ungulate effects between seedingand no-seeding seasons. All these suggest that competi-

tion for acorns is not the main reason explaining theimpact of ungulates on rodents in the Mediterraneanoak woodlands.

In summary, our results do not suggest any main effectof ungulates on rodents mediated by alterations ofvegetation cover or competition for acorns. However,we found that the effects of ungulates on rodentabundance were more pronounced in the dehesa than inthe forest. This outcome may be explained by ourfindings on how rodent space use and local abundance

ARTICLE IN PRESSA. Munoz et al. / Basic and Applied Ecology 10 (2009) 151–160158

were affected by ungulates in the forest, where rodentswere captured more frequently under shrubs outside theexclosures. This effect may be a response of rodents toungulate direct disturbances on habitat, such as soilcompaction (Daniel, Potter, Altom, Aljoe, & Stevens,2002; Donkor et al., 2002; Torre et al., 2007), directtrampling, and wild boar rooting (Focardi et al., 2000).Keesing (1998) expected that this kind of disturbancesmay affect the space use of small mammals when theprobability of encounter with ungulates is high and theabundance of shelter for small mammals is low (Keesing,1998). Our results suggest that this phenomenon may alsobe taking place in Mediterranean ecosystems.

Soil compaction by ungulates can reduce the func-tionality of underground burrows (Jegou et al., 2002),and animals like earthworms tend to avoid compactedsoils (Stovold, Whalley, Harris, & White, 2004). Smallrodents like M. spretus and A. sylvaticus depend onunderground burrows (Khidas & Hansell, 1995), and ithas been recently shown that soil compaction by cattleaffects negatively the abundance of burrowing mammalsin Mediterranean grasslands (Torre et al., 2007).Rooting by wild boars can also damage burrow systems,and wild boars can also predate incidentally rodentswhile rooting, although plant material constitutes thebulk of their diet (Schley & Roper, 2003). Under thissituation, shrubs may shelter burrows from ungulatetrampling, soil compaction or rooting (own data), whatmay explain the association of rodents with shrubs ingrazed forest plots and the decrease of rodent abun-dance in grazed dehesa plots. The association betweenrodents and oaks in the savannah-like dehesas probablyintensifies the impact of ungulates on rodents, as thescattered trees are frequently visited by ungulates asfood source and cover (personal observation).

Implications for the sustainability of Mediterranean

ecosystems

Mediterranean ecosystems are among the 25 biodiver-sity hotspots of the world (Myers et al., 2000). TheMediterranean dehesas are preserved under the EUHabitats Directive because they maintain high levels ofplant and animal diversity, even higher than theMediterranean oak forests from which they originated(Dıaz et al., 2003). However, the conservation of dehesasis not sustainable in the long-term due to the chronicabsence of oak regeneration (Dıaz et al., 1997; Plieninger,Pulido, & Konold, 2003; Plieninger, Pulido, & Schaich,2004; Pulido & Dıaz, 2002; Pulido et al., 2001). Lowshrub layer in dehesas seems to impede oak regenerationlimiting the amount of acorns dispersed by rodents tosafe sites (i.e. shrubs) for establishment (Pulido & Dıaz,2005; Smit, den Ouden, & Dıaz, 2008). Here, we foundthat ungulates can lead to 80% decreases in the

abundance of seed-dispersing rodents when shrub coveris scarce. Thus, besides the direct negative effects ofungulates on oak regeneration as acorn predators (Pulido& Dıaz, 2005; Bonal & Munoz, 2007), they may haveindirect negative effects by reducing the abundance ofacorn-dispersing rodents, and consequently acorn dis-persal rates. These indirect heterospecific interactionsbetween acorn predators and dispersers have been foundbefore in oak woodlands (Munoz & Bonal, 2007).Nonetheless, our results should be taken with cautiondue to the limited spatial replication of our samplingdesign. We were able to test the effects of ungulates onindependent populations of small rodents, but replicatedstudies carried out in other woodlands, and with differentungulate densities, will help to increase our knowledge onthe interactions between rodents, ungulates and shrubs inother relevant scenarios.

The efforts to control ungulates have been focussed oneither reducing ungulate densities in large areas or onprotecting small areas of high conservation value, with nosuccessful outcomes in most cases (Cote et al., 2004). Inthe Mediterranean ecosystems shrubs seem to mediateungulate–rodent interactions, because they may serve asrefuges for keystone rodents against ungulate distur-bances. Hence, controlled shrub encroachment could bean effective alternative to ungulate population controland exclusion in the conservation of high-diversityMediterranean ecosystems (Ramırez & Dıaz, 2008).

Acknowledgements

J.M. Aparicio, K. Hovemeyer and three anonymousreviewers provided helpful comments on a previousversion of the manuscript. We thank the many studentswho helped during field work. This study was supportedby the Projects REN2003-07048/GLO and CGL2006-06647/BOS, PAC-02-008, 096/2002 (MMA) and 003/2007 (MMA). AM and RB were supported by fellow-ships from the JCCM. The Consejerıa de MedioAmbiente (JCCM) and the Cabaneros National Parkprovided the permits for rodent trapping.

Appendix A. Supplementary materials

Supplementary data associated with this article can befound in the online version at doi:10.1016/j.baae.2008.01.003.

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