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Animal Behaviour 84 (2012) 1435e1442

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Animal Behaviour

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

Responses of a scatter-hoarding rodent to seed morphology: links between seedchoices and seed variability

Alberto Muñoz a,b,*, Raúl Bonal b,c,d, Josep Maria Espelta b

aDepartamento de Didáctica de la Ciencias Experimentales, Facultad de Educación, Universidad Complutense de Madrid, Madrid, SpainbCREAF, Cerdanyola del Vallès, SpaincGrupo de la Biodiversidad Genética y Cultural, Departamento de Ecología, Instituto de Recursos Cinegéticos (CSIC-UCLM-JCCM), Ciudad Real, SpaindGrupo DITEG Instituto de Ciencias Ambientales (ICAM), Área de Zoología, Universidad de Castilla-La Mancha, Toledo, Spain

a r t i c l e i n f o

Article history:Received 23 May 2012Initial acceptance 21 June 2012Final acceptance 4 September 2012Available online 10 October 2012MS. number: 12-00390R

Keywords:acornAlgerian mouseanimaleplant interactionhandling costhoarding behaviourHolm oakMus spretusQuercus ilexseed cachingsmall rodent

* Correspondence: A. Muñoz, Departamento de Didimentales, Facultad de Educación, Universidad CompRoyo Villanova s/n Ciudad Universitaria, 28040 Madr

E-mail address: alberto.munoz.munoz@edu.ucm.e

0003-3472/$38.00 � 2012 The Association for the Stuhttp://dx.doi.org/10.1016/j.anbehav.2012.09.011

Seed preferences of scatter-hoarding granivores may influence the evolution of seed traits in plants.However, there is little evidence linking the granivores’ responses to specific seed traits to the variabilityof seeds in a single plant species. This information is essential for understanding how the decisions ofgranivores can shape plant life histories. We analysed how seed morphology (size and shape) of theHolm oak, Quercus ilex, influences seed choices of the seed-disperser, the Algerian mouse, Mus spretus.We studied the seed variability of the oak and whether the frequency of seed phenotypes matched theseed choices of the disperser. The probabilities of seed removal decreased as the seeds became larger andmore bullet-shaped, so that seeds that were simultaneously large and bullet-shaped had the lowestprobabilities of being dispersed. These seeds are probably refused by rodents because they impose higherhandling and transport costs. The size and shape of the Holm oak seeds were highly variable betweentrees, but extraordinarily consistent within a single tree over different years. However, the analysis ofseed variability revealed a disproportionately low frequency of large bullet-shaped phenotypes, whichare those barely removed by rodents. Seed preferences of dispersers of species with high seed variabilitybetween trees can lead to differences in the chances of seeds produced by different trees being dispersed.Those seed phenotypes preferred by dispersers could make a higher contribution to the next generation,which could influence the evolution and variability of seeds in a plant species.� 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Many plant species depend on the removal and dispersal of theirseeds by seed-caching animals for successful recruitment (VanderWall 1990; Jansen et al. 2002; den Ouden et al. 2005; Roth &Vander Wall 2005; Steele et al. 2006; Briggs et al. 2009; Xiaoet al. 2009; Muñoz & Bonal 2011). In these species, it is thoughtthat dispersers’ preferences for certain seed features may influencethe evolution of seed traits (Vander Wall 2010). This hypothesis ismainly supported by cross-species comparisons, so that the largerseed size of zoochorous species would be explained by dispersers’preferences for large, more nutritious seeds (e.g. Smith & Reichman1984; Leishman et al. 1995; Hammond et al. 1996; Vander Wall2003; Moles et al. 2003, 2005). However, differences betweenseed species may be caused by phylogenetic effects not linked toselection pressures imposed by dispersers. This makes it moredifficult to disentangle the seed traits potentially influenced by

áctica de las Ciencias Exper-lutense de Madrid, C/Rectorid, Spain.s (A. Muñoz).

dy of Animal Behaviour. Published

dispersers (Herrera 1992; Jordano 1995a). Intraspecific approachesare much less common, despite the fact that they provide bettermodels for analysing selection pressures of animals on specific seedtraits (Jordano 1995b; Jansen et al. 2004; Pollux et al. 2007; Muñoz& Bonal 2008a). At the intraspecific level, seed traits might influ-ence the preferences of seed-caching animals, and these traitscould be subjected to selection pressures if they are highly variablebetween individual plants, consistent within the same motherplant and over time, and heritable (see Jordano 1995b).

Seed shape has received much less attention than seed size inthe context of seed choices of animals. Dispersers prefer largerseeds because of their higher nutrient content (Jansen et al. 2004;Xiao et al. 2004; Muñoz & Bonal 2008a), but their choices may alsodepend on the costs of handling and transporting the seeds (Kerley& Erasmus 1991; Jacobs 1992; Emlen 1996). In this context, a largeseed size can impose higher transport costs on dispersers (Muñoz &Bonal 2008a), but seed shape may also affect their seed choices if itinfluences handling and transport costs. Thus, two seeds of thesame size but different shape can provide the same amount ofnutrients, yet entail different handling and transport costs. Hence,

by Elsevier Ltd. All rights reserved.

A. Muñoz et al. / Animal Behaviour 84 (2012) 1435e14421436

the combination of size and shape may be relevant for seed choicesof dispersers and could have further consequences for seed traitevolution. Similarly, fruit choices of avian frugivores could haveaffected the evolution of fruit morphology in endozoochorousplants, in which larger fruits are more bullet shaped to facilitateswallowing of the fruit (see Herrera 1992).

In this study, we analysed the intraspecific variability of seedmorphology (seed size and seed shape) between and withinmother trees in the Holm oak, Quercus ilex, over different years. Westudied how seed morphology influenced seed choices of the mainseed-dispersing rodent, the Algerian mouse, Mus spretus, andcompared the extent to which the natural distribution of seedphenotypes matched the preferences of dispersers. The acorn fallseason in the Holm oak lasts from September to December (Bonal &Muñoz 2007), and during this period the Algerian mouse removesand caches hundreds of acorns several metres away from thecanopies of the mother oaks (Leiva & Fernández-Alés 2003; Muñoz& Bonal 2008b, 2011). This rodent’s decision whether or not toremove Holm oak acorns from under the tree is critical to acorndispersal, given that acorns dropped beneath mother oaks sufferhigh predation pressure from various seed predators and thus havefewer chances of recruiting than those dispersed beyond motheroaks (Bonal & Muñoz 2007; Muñoz & Bonal 2011).

In the Holm oak, acorn size shows high variability, from 0.5 to15 g (Bonal et al. 2007; Bonal & Muñoz 2008), and also high vari-ation in shape (i.e. the ratio between seed length and transversaldiameter) from almost spherical acorns to very elongated, bullet-shaped ones (Fig. 1). Our specific objectives were to analyse (1)the effects of acorn size and acorn shape on seed choices ofM. spretus in the laboratory, (2) the natural variability and temporalconsistency of acorn shape and size between and within Holm oaksin the field, and (3) whether the frequency of the different acornphenotypes observed in the Holm oak matches the foraging pref-erences shown by seed-caching rodents.

Figure 1. Intraspecific variability of acorn shape and size in the Holm oak, Quercus ilex. In ta different mother tree.

METHODS

Study Area and Study Species

The study area was at the Cabañeros National Park (39�240N,3�350WCiudad Real, central Spain), a nature reserve representativeof Mediterranean oak forests where the Holm oak is the mostcommon tree species (details of the study area can be found inBonal et al. 2007; Muñoz et al. 2009). Holm oak crops can be verylarge, although with strong interannual variability (Bonal & Muñoz2007; Espelta et al. 2008). The Algerian mouse is a small species(8e23 g) that accounts for more than 95% of the rodent populationat the study area (Muñoz et al. 2009). The other species present isthe wood mouse, Apodemus sylvaticus. Algerian mice and Holmoaks often occur in the same area because both thrive in dryMediterranean environments. Other acorn predators at the studysite are wild boars, Sus scrofa, and red deer, Cervus elaphus. Jays,Garrulus glandarius, also feed on acorns but they are rarely seen,probably because the study area does not fulfil the habitatrequirements of this corvid.

Seed Choice Experiments

Seed choice experiments were performed in the laboratory,where we could control rodent body mass as an independentvariable in foraging choices. This is very important because the‘seed mass/rodent mass’ ratio determines the actual transport costsand thus conditions seed removal behaviour (Muñoz & Bonal2008a). We captured 20 adult M. spretus at the study area withstandard Sherman live-traps. Traps were set between 1200 and1600 hours GMT and checked daily between 0700 and 0900 hoursGMT on 3 consecutive days. Each trap was baited with a piece ofapple and a paste made of tuna in oil and flour. A piece of water-proof cotton was also added as bedding material and to protect the

his species, acorns range from almost spherical to bullet shaped. Each acorn belongs to

A. Muñoz et al. / Animal Behaviour 84 (2012) 1435e1442 1437

captured rodents from cold and rain (Muñoz et al. 2009). Oncetrapped, the rodents made a nest with the cotton provided andconsumed some of the apple. We captured one pregnant femaleand five juveniles, which were immediately released. No lactatingfemales were caught during our 3-day trapping.

We carried the adult nonbreeding rodents to the University ofCastilla-La Mancha facilities in their provisional nests made insidethe traps. The rodents were captured in the middle of the acorn fallseason (November) to ensure that they had already fed on acorns,because previous feeding experience can affect seed size prefer-ences (Muñoz & Bonal 2008b). Rodents were individually housedindoors in terraria (60 � 32 cm and 30 cm high) filled with a layerof sand 5 cm deep and provided with a piece of waterproof cottonfor use as nesting material. Hamster food, fruit and water wereprovided ad libitum. Each mouse was kept in its home terrariumwith a light:dark cycle of 12:12 h for 10 days prior to the trials, toensure that it became familiarized with the new environment.

Seed choice trials were conducted indoors in 2 � 2 m arenas inwhich each of the 20 rodents captured (10 male and 10 female) wasgiven 40 acorns collected at the study area. These acorns repre-sented the seed mass and shape variability (the ratio betweenacorn length and width) found at the study area (mass: mean -� SE ¼ 3.10 � 0.07 g, N ¼ 800, range 0.20e9.52 g; shape: mean -� SE ¼ 2.20 � 0.01, N ¼ 800, range 1.61e3.96; see Fig. 1). The 40acorns used on each experimental rodent were selected to matchthe variability of size and shape existing in the field. We checkedthat the variance in acorn mass and shape was the same betweenand within individual rodents to ensure that acorn samples werenot biased (acorn mass: F19,779 ¼ 1.24, P ¼ 0.22; acorn shape:F19,779 ¼ 1.12, P ¼ 0.33). Before each trial, 40 acorns were selectedand weighed with a digital balance (to the nearest 0.01 g),measured with a digital calliper (to the nearest 0.01 mm), andmarked with a small number written with an odourless pencil.Weevil-infested acorns were discarded as they are rejected by thisrodent species (Muñoz & Bonal 2008b). Researchers/technicianswore fresh gloves while handling seeds to minimize possiblehuman odour cues on seed preferences (Wenny 2002).

Each experimental rodent was weighed with a digital balance(to the nearest 0.01 g) immediately before the trial started (bodymass: mean � SE ¼ 15.8 � 0.6 g, range 11.0e21.5 g, N ¼ 20). Then,the 40 acorns were placed at the centre of the arena, and the hometerrarium with the rodent inside was placed in one corner. Twocages (23 � 9 cm and 8 cm high) equipped with a small piece ofcotton were also placed on two sides of the arena simulatingsheltered sites in order to stimulate the experimental rodent toremove and hoard the acorns. The trial started at 2000 hours GMT,when the simulated ‘daylight’ was turned off in the experimentalroom (this rodent species is nocturnal). We adjusted the duration ofthe experiments (4 days with a light:dark cycle of 12:12 h) and thenumber of seeds offered to each rodent (40) to ensure that therodents had enough time to select and remove some seeds so as toenable us to measure their seed preferences. After the 4 days ofeach experiment, we noted whether the 40 acorns had beenremoved or eaten. Over the 4 days of testing, eaten acorns were notreplenished and the only food source available to each experi-mental rodent was the 40 acorns. After each trial, the arena wascarefully cleaned with nonperfumed soap and water to eliminatesite-specific odour cues (Daly et al. 1980).

We kept each rodent at the university for 15 days on average(habituation þ trial). Rodent trapping and experimental proce-dures in the laboratory were licensed by the Consejería de MedioAmbiente (JCCM-2003), Ministry of Environment (RegionalGovernment of Castilla, La Mancha). All experimental rodents werehealthy during the trials and, once the experiments ended, theywere released at the sites where they had been captured. To ease

their return to field, the rodents were released on warm, sunnydays.

Seed Trait Variability in Holm Oaks

We selected and geopositioned 27 Holm oaks randomlydistributed throughout the study area. In these focal trees wemonitored for 4 consecutive years (2002e2005) acorn shape andmass. We set seed traps hung under the canopies that wereemptied every 15 days from the outset to the end of the acorn fallseason. Each year, weweighed (to the nearest 0.01 g) andmeasuredthe length and width (to the nearest 0.01 mm) of at least 15 soundacorns per tree (Bonal et al. 2007). We also measured and weighedmore than 5000 acorns collected from 100 additional oaks at thestudy area to analyse the relationship between acorn shape andacorn mass in the Holm oak population.

Data Analyses

In the analyses of acorn choice of rodents we considered theacorn mass/rodent mass ratio as an independent variable, since thetransport costs depend simultaneously both on the mass ofthe seed and that of the rodent (Muñoz & Bonal 2008a). Usinga generalized linear model with a forward stepwise procedure wetested whether acorn removal (a dependent variable with a bino-mial distribution) was influenced by the seed/rodent mass ratioand acorn shape (independent variables). With the data from theacorn choice experiments we developed a function to predict theprobabilities of acorn removal (P) based on acorn shape (S) andthe acorn mass/rodent mass ratio (R).

We used general linear models to analyse how acorn mass andshape varied between trees and over the years, and also regressionsto study the relationships between acorn size and shape in the focaltrees. To assess intraindividual repeatability in acorn mass andshape, we calculated the coefficients of variation (CVs) for theacorns of each tree. Then, we compared the CVs of mass and shapewith a repeated measures ANOVA in which the variable ‘tree’ wasthe within-subjects factor accounting for the association of bothtypes of CVs within the same tree. To check for any potentiallyconfounding effect of spatial autocorrelation on the acorn mass orshape in the focal trees, we also performed two Mantel tests. Wetested whether differences in acorn mass and shape between oakswere related to the geographical distance between them.

Finally, the relationships of acorn mass with acorn length andwidth were analysed using 5236 acorns that were collected,weighed and measured from 100 random trees to test whichfunction best fitted the data distribution. We used a chi-square testto assess whether the frequency of phenotypes of acorn shapes wasrandomly distributed within the range of acorn masses, that is,whether there was any tendency for larger or smaller acorns to bemore bullet shaped or round.

RESULTS

Seed Choice of Rodents

Rodents removedonaverage75.6%of acorns andate50.1%of them(partially or completely eaten). The generalized linear model showedthat acorn removal was first influenced by the acorn mass/rodentmass ratio (estimate� SE¼ 2.88� 0.58, Wald¼ 24.32, P< 0.0001),so that the probability of a given rodent removing an acorn decreasedas the acorn mass/rodent mass ratio increased. The model showedthat acorn shape also had a significant effect on the probability ofacorn removal (estimate� SE¼ 0.79� 0.28,Wald¼ 8.08, P¼ 0.004),which decreased as the acorn length/acorn width ratio increased.

A. Muñoz et al. / Animal Behaviour 84 (2012) 1435e14421438

Similarly, removed acorns were on average more spherical (shape:mean � SE¼ 2.17� 0.01, N¼ 604) than those not removed byrodents (shape: mean � SE¼ 2.27� 0.02, N¼ 195; F1, 794 ¼ 32.66,P< 0.0001). Thus, large and bullet-shaped acorns were less likely tobe removed by rodents, and the functionpredicting the probability ofacorn removal (Pr) on the basis of acorn shape (S) and the acornmass/rodent mass ratio (R) clearly showed that the probability of beingremovedwas lower for bullet-shaped acornswhen they had a higheracorn/rodent mass ratio (Pr ¼ 0.315þ 0.662� Se0.179� Re0.181� S2e0.425� R2e0.067� S� R (Rmodel ¼ 0.76); Fig. 2).

Seed Shape and Mass Variation in Holm Oaks

Both acorn shape and acorn size differed significantly betweenthe 27 focal trees (shape: F26, 347 ¼ 60.3, P < 0.0001; size: F26,333 ¼ 60.3, P < 0.0001; Fig. 3a), with no relationship between meanacorn size and mean acorn shape per tree (ß � SE ¼ �0.02 � 0.05,t25 ¼ �0.44, P ¼ 0.66, R2 ¼ 0.007) and no spatial autocorrelation ineither variable (Mantel tests: mass: R ¼ �0.09, P ¼ 0.97; shape:R ¼ 0.014, P ¼ 0.38). Acorn mass and acorn shape were highlyrepeatable within the same tree (CVs: mean � SE: shape:0.006 � 0.001; size: 0.094 � 0.011), but repeatability for shape wasstronger than for mass (repeatedmeasures ANOVA for comparisonsof CVs: F1, 26 ¼ 68.72, P < 0.0001). Moreover, the consistency overthe 4-year period (between year X and year Xþ1) was stronger foracorn shape (ß � SE ¼ 0.83 � 0.06, t64 ¼ 14.1, P < 0.001, R2 ¼ 0.75)than for acorn mass (ß � SE ¼ 0.61 � 0.09, t74 ¼ 7.14, P < 0.0001,R2 ¼ 0.40; comparison of correlation coefficients: P ¼ 0.002). In

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Figure 2. Relationship between probability of acorn removal by the Algerian mouse, Musbetween acorn mass and rodent mass.

fact, we found significant interannual changes in acorn mass (F3,101 ¼ 3.89, P ¼ 0.011), with trees producing heavier acorns in 2003than in other years (Tukey HSD: all P values < 0.05), whereas nosignificant interannual changes in acorn shape were recorded (F3,94 ¼ 1.59, P ¼ 0.20; Fig. 3b).

Using the sample of more than 5000 acorns collected from over100 Holm oaks, we found that acorn shape was biased within theacorn mass range (c2 ¼ 10413.4, P < 0.0001), and found a lowfrequency of large and bullet-shaped phenotypes in the population(Fig. 4a). Acorn width (W) and mass (M) showed a linear relation-ship (W ¼ 9.28 þ 1.18M; R2 ¼ 0.90, P < 0.0001), whereas the rela-tionship between acorn length (L) and mass best fitteda logarithmic function (L ¼ 19.87 þ 22.82log M; R2 ¼ 0.81,P < 0.0001; Fig. 4b). Hence, beyond a certain mass acorns growbasically in width and, accordingly, the masselength regressionslopes for acorns larger than 7, 8, 9 and 10 g decrease steadily (0.69,0.50, 0.14 and 0.11, respectively), explaining why large bullet-shaped acorns are rare.

DISCUSSION

We have found that variability in seed morphology withina single plant species can influence the foraging decisions of itsseed-dispersing rodent. Our seed choice experiments showed thatAlgerian mice avoided removing large and bullet-shaped seeds ofthe Holm oak. Seed traits in this species varied sharply betweendifferent trees, but showed high repeatability within the same treeand over time, so that Holm oaks producing large bullet-shaped

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Figure 3. (a) Variability in acorn size (open diamonds) and acorn shape (filled rectangles; the ratio between acorn length and acorn width) for the 27 focal Holm oaks, and (b)variation of mean acorn mass (black symbols) and shape (grey symbols) over the 4 years of study. Bars represent SE and whiskers represent SD

A. Muñoz et al. / Animal Behaviour 84 (2012) 1435e1442 1439

acorns may have fewer chances of dispersal by Algerian mice, thusdecreasing their recruitment contribution to the next generation.This might have changed the frequency of seed phenotypes in thepopulation of Holm oaks over evolutionary time, as the lack of largeand bullet-shaped phenotypes currently found in natural pop-ulations of the Holm oak would suggest.

Most research on the adaptive value of seed or fruit traits todispersers has been conducted at the interspecific level (Lomascolo

& Schaefer 2010; Lomascolo et al. 2010; Vander Wall 2010).Consequently, the theory that seed choices of animals have influ-enced seed trait evolution is mainly based on studies of interspe-cific seed size variation, which link the larger seed size of animal-dispersed plants to the dispersers’ preferences for large seeds(reviewed in Moles et al. 2003, 2005). The intraspecific seed traitvariability prevents potentially confusing effects concurrent withplant species identity and, hence, it offers a better scenario for

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Figure 4. Relationships between (a) acorn mass and acorn shape (the ratio between acorn length and acorn width), and (b) acorn length (circles) and acorn width (triangles) withacorn mass.

A. Muñoz et al. / Animal Behaviour 84 (2012) 1435e14421440

analysing selection pressures on specific seed traits. At the intra-specific level, seed traits could be subjected to selection pressures ifthey were variable between mother plants, repeatable at theintraindividual level and over time, heritable and relevant for seeddispersal likelihood. Other studies have failed to find links betweenforaging decisions of animals and variability of seed phenotypesbecause selection pressures are diffuse within the whole seeddispersal process (Pollux et al. 2007) or because intraspecific seedvariability is very high within the same mother plant (Jordano1995b). However, in our study system we found a high variationin the size and shape of seeds between different mother trees,a high consistency of these traits within the same mother tree, andclear seed trait preferences of scatter-hoarding rodents. Thisscenario provides a good model system for investigating howdisperser decisions can influence seed trait evolution.

Recently, Wang & Chen (2009) experimentally showed thatphysical traits of seeds, such as size, are more important for thedecisions of seed-caching rodents than other seed traits such aschemical composition. This is probably because physical traitsinfluence the costs of handling and transporting seeds for smallanimals (Jacobs 1992; Muñoz & Bonal 2008a). We recorded some ofthe experimental rodents and observed that they always trans-ported the acorns by gnawing the distal point and holding themwith the head up. Hence, for a given rodent, the higher the acorn

weight is, the higher the transport cost (Muñoz & Bonal 2008b). Inaddition, at equal acorn mass, acorns with a high ratio of length/width probably impose an added mechanical cost of transport,because rodents need to raise their heads up further than for morespherical acorns. This would explain why an acorn’s removalprobabilities diminished notably when it was both heavy and bulletshaped (Fig. 2). The greater difficulties of transporting large, bullet-shaped acornsmay represent a serious handicap for acorn dispersalthat could explain why there is a lack of large, bullet-shapedphenotypes in the population of Holm oaks studied. It is verylikely that trees producing large, bullet-shaped acorns may havefewer chances of dispersal, thus decreasing their recruitment andcontribution to the next generation. The removal of acorns byM. spretus from beneath mother canopies is critical for the naturalrecruitment of Holm oaks at the study area (Muñoz & Bonal 2007,2011), given the mortality of acorns not taken away from themother trees (Pulido & Díaz 2005; Bonal & Muñoz 2007; Muñoz &Bonal 2011).

The low intraindividual and temporal variability of acorn traitssuggests that they may have a genetic basis, as has been reportedfor other plant species (Cober et al. 1997; Salas et al. 2006; Robertet al. 2008). Also, the lack of spatial correlation in our study treesrules out any significant environmental effect on seedmorphology.

A. Muñoz et al. / Animal Behaviour 84 (2012) 1435e1442 1441

Although shape and mass were highly consistent over the years,seedmass variedmore than seed shape. This variationmay respondto annual changes in the availability of resources in temperate areas(rain, nutrients, etc.), which often lead to changes in seed size orseed numbers across years (Espelta et al. 2008, 2009; Koenig et al.2009). In fact, the larger seed size of Holm oaks documented in2003 could have been caused by the rainy autumn in that year atthe study area. The consistency of shape is maintained regardless ofchanges in the available resources, suggesting that the amount ofresources invested in each seed (i.e. seed mass) is independent ofthe way the resources are organized at the seed level (i.e. seedshape). This makes it possible for different trees to produce seeds ofthe same mass but different shape (Figs 1, 3a).

We have found a relationship between seed preferences ofa seed disperser and the frequency of seed variability of the plant itdisperses. Seed morphologies with a lower probability of dispersalwere represented less within the range of seed phenotypes ina natural population. However, we have no direct evidence that theAlgerianmouse has influenced the evolution of seedmorphology inthe Holm oak. On the one hand, it would be worthwhile to havedata on the heritability of seed traits, even though in long-livedspecies such as oaks a seedling takes several decades to becomean adult tree that produces seeds. On the other hand, there areother acorn predators that could also impose different selectionpressures on acorn traits, such as insects (Bonal et al. 2007; Espeltaet al. 2009), ungulates (Gómez 2004) or other rodents, larger thanM. spretus, such as A. sylvaticus (Muñoz & Bonal 2008a), which maycontribute to maintaining a greater seed trait variability dependingon their responses to seed traits. Recent studies have suggested thatin-depth investigation of the behavioural responses of animals toplant propagules is important for improving our understanding ofseed dispersal processes (Cousens et al. 2010;Muñoz & Bonal 2011).However, such behavioural approaches are still scarce in the liter-ature on animaleplant interactions, partly because it is difficult totrack the individual decisions of seed dispersers (Jordano & Schupp2000; Cousens et al. 2010). Thus, further studies on this topic willhelp to shed light on the role of granivores in the functionalsignificance of seed traits.

Acknowledgments

We thank B. Nicolau and L. Arroyo for their assistance in labo-ratory experiments and field work. This work was supported by theprojects REN2003-07048/GLO (MEC), 096/2002 (MMA), PII1C09-0256-9052 (JCCM) and Consolider e Ingenio MONTES (CSD 2008-00040) A.M. and R.B. were supported by JCCM fellowships and ‘Juande la Cierva’ contracts. S. Rutherford and two anonymous refereesprovided helpful comments that improved the manuscript.

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