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ANIMAL BEHAVIOUR, 2008, 76, 709e715doi:10.1016/j.anbehav.2008.03.017

Are you strong enough to carry that seed? Seed size/body

size ratios influence seed choices by rodents

ALBERTO MUNOZ & RAUL BONAL

Departamento de Ciencias Ambientales, Facultad de Ciencias del Medio Ambiente,

Universidad de CastillaeLa Mancha

(Received 1 October 2007; initial acceptance 17 January 2008;

final acceptance 26 March 2008; published online 18 June 2008; MS. number: 9529R1)

Granivorous rodents prefer large seeds because they offer a higher nutrient content, but such preferencesmay be counterbalanced by the higher costs of handling and transporting larger seeds. We hypothesizedthat this compromise underlying foraging decisions depends simultaneously on the size of both seeds androdents. A given seed offers a fixed amount of resources, but the costs of handling and transporting thatseed could increase as the rodent size decreases. We designed a laboratory experiment to assess explicitlywhether seed choices depend on the size of both seeds and rodents. As a model, we used two different-sizedspecies, the Algerian mouse Mus spretus (8e15 g) and the wood mouse Apodemus sylvaticus (18e40 g), thatface the decision of choosing Holm oak (Quercus ilex) acorns from 0.5 to 15 g under natural conditions. Theprobability of seed removal decreased as the ratio of seed size to rodent size increased in both rodent spe-cies. Seeds heavier than 60% of the rodent’s mass led to substantial decreases in acorn removal and seedsheavier than 70% of the rodent’s mass were in no case removed. This critical value limited the choice of thelargest seeds by the smaller species, but not by the larger one. Therefore, the larger species selected largeracorns and with a wider variance in size than the smaller species. Our results show the importance of con-sidering jointly the sizes of seeds and rodents in the study of foraging decisions and seed dispersal behav-iour by granivorous rodents.

� 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: Algerian mouse; Apodemus sylvaticus; body size; ha

Correspoetal, InsE-28006is now aEcologıaReal 130

0003e3

ndling costs; Mus spretus; seed dispersal; seed size; wood mouse

Most small rodents are granivorous, and some species moveand cache seeds for later consumption, thus acting asimportant seed dispersers (Vander Wall 1990; Jansen et al.2002; Roth & Vander Wall 2005; Steele et al. 2006; Munoz& Bonal 2007). Many plant species depend on small rodentsfor seed dispersal (Vander Wall 1990; Herrera 2002), and theseed-size preferences of these animals can shape the evolu-tion of seed size. In fact, the larger seed size of plants dis-persed by granivores (Leishman et al. 1995; Hammondet al. 1996) is often explained by the preferences of graniv-orous species for larger seeds, which offer higher nutritional

ndence: A. Munoz, Departamento de Fisiologıa y Ecologıa Veg-tituto de Recursos Naturales, CCMA, CSIC. c/Serrano 115,Madrid, Spain (email: alberto.munoz@ccma.csic.es). R. Bonalt the Grupo de la Biodiversidad Genetica y Cultural �Area de, IREC (CSICeUCLMeJCCM), Ronda de Toledo s/n, Ciudad71, Spain.

709472/08/$34.00/0 � 2008 The Association for the Stu

rewards than smaller seeds (Smith & Reichman 1984; Jan-sen et al. 2002; Vander Wall 2003).

It is assumed that scatter-hoarding rodents should spacecaches to maximize cache recovery rate (e.g. to minimizeloss to pilferers) relative to the costs of transporting seeds(Stapanian & Smith 1978, 1984; Moore et al. 2007). In thiscontext, most field studies have shown that rodents preferlarge over small seeds (e.g. Vander Wall 1994; Garb et al.2000; Brewer 2001), and that large seeds are preferentiallydispersed and cached (Vander Wall 1995, 2003; Jansenet al. 2002; Xiao et al. 2004), even though they involvehigher transporting costs. Such preferences have obviousfitness consequences for the plant and for seed-size evolu-tion, as by being dispersed the seeds avoid the predationrisk under the mother plant and may be carried to safe mi-crosites for germination and seedling growth (Herrera2002; Pulido & Dıaz 2005; Munoz & Bonal 2007).

In most studies on seed preference by rodents, seeds ofdifferent plant species that differ in more traits than just

dy of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

ANIMAL BEHAVIOUR, 76, 3710

their size, such as morphology, nutrient content orchemical defences (Janzen 1969; Jensen 1985; Kollmanet al. 1998), were offered (reviewed in Moles et al. 2003),which may confound the effects attributed to seed-sizevariability (see Dıaz 1996; Blate et al. 1998). In onlya few cases have the seed choices of rodents facing differ-ent-sized seeds of the same plant species been tested (seeJansen et al. 2004 for a summary), although intraspecificseed-size variation is considerable in many plant species(Manasse 1990; Brewer 2001; Jansen et al. 2002; Xiaoet al. 2004; Bonal et al. 2007). Such studies evidencethat the trend towards a preference for large seeds is farfrom being a general rule. For instance, Brewer (2001)found that larger seeds of Astrocaryum mexicanum wereremoved faster, dispersed at shorter distances and eatenby predators at higher rates in caches than smaller ones.Conversely, Jansen et al. (2002) found that large seeds ofCarapa procera were removed at similar rates, dispersed atlonger distances and eaten by predators at lower rates incaches than small ones.

Preferences for large seeds are easy to interpret becausethey offer a higher nutrient content to rodents (Kerley &Erasmus 1991). However, the costs of handling and trans-porting seeds are also positively related to seed size, andthese costs may impose upper limits to the seed sizes pre-ferred by rodents (Jacobs 1992). In this scenario, rodentforaging decisions may be determined by the nutrientcontent of seeds and their handling/transport costs,both related positively with seed size. Here, we hypothe-size that this compromise depends critically on the sizeof the rodent, in such a way that the costs of handlingand transporting a given seed would decrease as the ro-dent size increases. Then, seed choices may be influencedby the ratio of seed size to rodent size. The striking incon-sistencies among various studies on seed-size preferencesmight thus be explained by relative differences in size be-tween seed and rodent species.

We designed a laboratory experiment to test the effectsof the ratio seed size/rodent size in seed choices. Asa model we used two different-sized rodents, the Algerianmouse (Mus spretus) and the wood mouse (Apodemus sylva-ticus), which are the most prominent rodent dispersers ofHolm oak (Quercus ilex) acorns on the Iberian Peninsula(Munoz & Bonal 2007). We predicted that the costs ofhandling and transporting a given acorn would decreaseas the rodent size increased, and thus, we expected thatthe larger species would choose larger acorns and witha wider variance in size than the smaller species. We alsodetermined explicitly the upper limits of acorn size con-straining rodent choices by testing the effects of acornsize/rodent size ratios on seed choices. Our results high-light the importance of considering not only the size ofthe seeds, but also the size of the rodents, in the studyof seed choices and seed dispersal behaviour.

METHODS

Study Species

The Algerian mouse (M. spretus) and the wood mouse(A. sylvaticus) are sympatric rodents in the Iberian

Peninsula (Blanco 1998). A. sylvaticus is larger (22e45 g)than M. spretus (8e18 g), and acorns are the bulk of theirdiet during the autumn (Pulido & Dıaz 2005). There isa considerable amount of literature evidencing that A. syl-vaticus scatter hoards acorns (den Ouden et al. 2005);none the less, we have recently shown that M. spretus isa prominent scatter hoarder too. This species dispersesthe acorns 1.5e2 m from the source tree and caches themsingly at a depth of 1.5e2 cm under the ground or underlitter, recovering 90.1% of the caches in the short term(Munoz & Bonal 2007). Thus, both species are importantscatter hoarders and are considered keystone dispersersfor the recruitment of Holm oaks (Pulido & Dıaz 2005),one of the most widespread trees in the Mediterraneanareas (Blanco et al. 1997). The size of Holm oak acorns is ex-tremely variable, ranging from 0.5 to 15 g; most of this var-iation is between trees, because acorn size is a fixed trait atthe intraindividual level (Bonal et al. 2007; Bonal & Munoz2008). Acorns are removed from the ground mainly bysmall rodents and ungulates (Pulido & Dıaz 2005; Bonal& Munoz 2007; Munoz & Bonal 2007).

Rodent Capture and Maintenance

We captured 20 adult M. spretus (body mass,X� SE ¼ 15:8� 0:6 g, range 11.0e21.5; 10 males þ 10 fe-males) and 20 adult A. sylvaticus (body mass,X� SE ¼ 27:5� 1:4 g, range 17.9e42.5 g; 10 males þ 10females) in several Holm oak forests in central Spain usingstandard Sherman live-traps. A. sylvaticus were signifi-cantly heavier than M. spretus (F1,38 ¼ 59.60, P < 0.001).We baited the Sherman traps with a piece of apple, andwe also added a piece of waterproof cotton to protect cap-tured rodents from cold and rain. We set the traps at 2000hours GMT and checked them the next morning at 0700hours GMT. Once trapped, rodents made a nest with thecotton provided and they consumed some of the apple.We captured the rodents during the acorn fall season(November) to ensure that they had foraging experiencewith acorns, given that learning can strongly affect theirseed-size preferences (Munoz & Bonal 2008). We carriedthe captured rodents to the University of CastillaeLaMancha facilities in their provisional nests made insidethe traps and housed them individually indoors in terraria(60 � 32 � 30 cm) filled with a layer of sand 5 cm deepand provided with a piece of waterproof cotton for useas nesting material. We provided food for hamsters, fruitand water ad libitum and kept each mouse in its home ter-rarium with a light:dark cycle of 12:12 h for at least 10days prior to the trials to ensure that they became familiar-ized with the novel environment (Munoz & Bonal 2008).The temperature of the experimental room was kept at15e17 �C. We performed experiments from 3 to 30December 2003 and kept each rodent at the university 15days on average (habituation þ trial). We trapped the ro-dents and maintained them in the laboratory with licensefrom the Junta de Comunidades de CastillaeLa Manchaand the University of CastillaeLa Mancha. All rodentswere healthy during the trials, and once experimentsended we released them at the exact sites where theyhad been captured.

MUNOZ & BONAL: SEED CHOICES BY GRANIVOROUS RODENTS 711

Experimental Set-up

We conducted trials indoors in 2 � 2 m arenas in whicheach rodent was offered 40 Holm oak acorns collected pre-viously in the forests where it had been trapped. Acornscollected included all categories of size within the naturalvariation at the study area (X� SE ¼ 4:14� 0:06 g,N ¼ 1600 acorns, range 0.20e12.71 g). We performed 40trials with the 40 rodents captured. Each rodent wentthrough a trial individually and only once. Before eachtrial, we selected the 40 acorns, weighed them with a digi-tal balance (to the nearest 0.01 g) and marked each witha small number written with an odourless pencil. Weavoided weevil-infested acorns (see Bonal & Munoz2007, 2008) as they are frequently rejected by rodents(Munoz & Bonal 2008). To ensure that each rodent was of-fered the full range of sizes, the 40 acorns of each trial in-cluded 10 acorns smaller than 3 g, 10 acorns between 3and 6 g, 10 acorns between 6 and 9 g and 10 acorns largerthan 9 g. We handled the acorns using fresh gloves toavoid human odour effects on seed preferences (Wenny2002). We also weighed the rodent under experimentationwith a digital balance (to the nearest 0.01 g). Then, weplaced the 40 acorns at the centre of the arena and thehome terrarium with the experimental rodent in one cor-ner. We also placed two metal cages (23 � 9 � 8 cm) pro-vided with a small piece of cotton in two sides of thearena, simulating sheltered sites to stimulate the experi-mental rodent to move and hoard the acorns (Fig. 1).The trial started at 2000 hours GMT, when we turned offthe light in the experimental room and turned on a softred light (both species are nocturnal). We daily monitoredthe fate of each acorn during the 4 subsequent days at0800 hours GMT when the light was turned on. At theend of the trial we classified each acorn as (1) eaten atthe point of encounter, (2) removed and eaten, or (3)removed and not eaten (dispersed). After each trial, wecarefully cleaned the arenas with odourless soap and waterto eliminate site-specific odour cues (Daly et al. 1980).

2 m

2 m

Home-terrarium

Cage

Cage

40Acorns

Figure 1. Diagram of the arenas used in the trials showing the posi-

tion of the home terrarium of the rodent under experimentation, theinitial position of the 40 seeds, and the two cages to stimulate the

rodent to hoard the seeds.

Data Analyses

We used ANCOVA models along with regression ap-proaches to investigate the relationships between acornmass and the proportion of acorns removed, eaten anddispersed (removed and not eaten). In the two-tailedANCOVAs, the proportion of acorns removed, eaten anddispersed was the dependent variable (square-root trans-formed); the rodent species was included as categoricalfactor and the intervals of 1 g of acorn mass as covariate.Using this procedure, an effect of species would indicatethat the intercepts differ, and an interaction term would in-dicate that the effect of acorn mass on each of the responsevariables depended on the species of rodent. When theseinteractions were significant, we performed a regressionapproach separately for each rodent species to assess the re-lationships between the proportion of acorns removed,eaten and dispersed and the acorn mass. To test for the ef-fects of the ratio acorn size/rodent size on acorn removalwe also performed an ANCOVA with the proportion ofacorns removed as dependent variable (square-root trans-formed), the rodent species as categorical factor and the ra-tio acorn size/rodent size as covariate. We tested thedifferences in size of the acorns removed, eaten and dis-persed between species using factorial ANOVAs with themean size of the acorns used by each individual as depen-dent variable and the species of rodent as categorical factor.In addition to the mean of acorn size, we also calculatedthe variance in size of seeds removed, eaten and dispersedby each individual and then we compared whether suchvariances differed between rodent species. In a first explor-atory stage we included the sex of individuals as a factor inthe analyses. However, we found no differences in seedchoices between males and females, and thus we removedthe variable ‘sex’ from the analyses.

RESULTS

Seed Removal

Acorns were preferentially moved to the home terrarium(40.3%) and the two metal cages (37.5%). The remainingacorns removed were moved to the corners of the arena.The ANCOVA with rodent species as factor and acorn size ascovariate showed that the relationship between the pro-portions of acorns removed and acorn size was different ineach rodent species (Table 1). The proportion of acorns re-moved by M. spretus was negatively related to acorn size(b � SE ¼ �0.73 � 0.22, t9 ¼ �3.27, P < 0.01), but no rela-tionship was found in A. sylvaticus (b � SE ¼ �0.11 � 0.33,t9 ¼ �0.33, P ¼ 0.75; Fig. 2a). We found a strong effect ofthe ratio acorn size/rodent size in the proportion of acornsremoved (ANCOVA: F1,23 ¼ 12.20, P ¼ 0.001). This rela-tionship was not affected by rodent species, although theinteraction ratio*rodent species was marginally significant(F1,23 ¼ 3.66, P ¼ 0.064). Thus, we tested the relationshipbetween the ratios and the proportion of acorns removedin each rodent species separately. In both species the pro-portion of acorns removed decreased as the ratio acornsize/rodent size increased, but this effect was much moremarked in M. spretus (b � SE ¼ �0.81 � 0.15, t15 ¼ �5.44,

Table 1. Results of the ANCOVA testing for the effects of rodent species and acorn size on the proportion of acorns removed, eaten andhoarded by experimental rodents

Removal Predation Hoarding

F1,17 P F1,17 P F1,16 P

Rodent species 13.84 <0.01 3.52 0.077 1.77 0.20Acorn size (covariate) 17.34 <0.001 21.24 <0.001 25.63 <0.001Rodent species*acorn size 14.38 0.001 2.54 0.129 5.59 0.03

ANIMAL BEHAVIOUR, 76, 3712

P < 0.0001) than in A. sylvaticus (b � SE ¼ �0.68 � 0.26,t8 ¼ �2.65, P ¼ 0.03). Ratios reaching 0.6 (i.e. seeds repre-senting 60% of rodent body mass) led to appreciable de-creases in acorn removal rates, and acorns 70% or more of

0

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Figure 2. Relationship between the percentage of acorns (a) moved,(b) eaten and (c) dispersed and the acorn size in M. spretus (white

circles, dotted line) and A. sylvaticus (black circles, solid line).

rodent body mass were in no case removed (Fig. 3). Thiscritical ratio of 0.7 sharply constrained acorn removal bythe smaller species, M. spretus, as the range of acorn sizesof Holm oaks was in all cases below 50% of the body massof A. sylvaticus, whereas approximately 5% of acorns wereabove 60% of the body mass of M. spretus. As a result, seedsremoved by A. sylvaticus were larger on average(F1,38 ¼ 64.67, P < 0.0001) and showed a higher variancein size (F1,38 ¼ 19.17, P < 0.0001; Fig. 4) than those re-moved by M. spretus.

Seed Predation and Dispersion

We found a strong effect of acorn size on the proportionof acorns eaten (Table 1). The proportion of acorns eaten de-creased sharply as the acorn size increased in both M. spretus(b � SE ¼ �0.72 � 0.20, t9 ¼ �3.84, P < 0.01) and A. sylvati-cus (b � SE ¼ �0.71 � 0.23, t9 ¼ �3.04, P ¼ 0.014, Fig. 2b).Acorns eaten by A. sylvaticus were larger on average(F1,38 ¼ 64.68, P < 0.0001) and more variable in size(F1,38 ¼ 24.17, P < 0.0001) than those eaten by M. spretus(Fig. 4). More than 95% of seeds eaten by both rodentspecies had been previously removed to the cages or thehome terrarium. Thus as rodents ate the small seeds thatthey had removed, the proportion of acorns removed andnot eaten (i.e. dispersed) increased with acorn size (Table 1)for M. spretus (b � SE ¼ 0.81 � 0.22, t7 ¼ 3.69, P ¼ 0.007)and A. sylvaticus (b � SE ¼ 0.71 � 0.23, t9 ¼ �3.03,P ¼ 0.014, Fig. 2c).

00.

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Figure 3. Relationship between the percentage of acorns removed

and the acorn size/rodent size ratio in M. spretus (white) and A. syl-vaticus (black).

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Figure 4. Comparisons of the (a) mean acorn mass and (b) mass var-

iance of acorns removed (white bars), eaten (black bars) and dis-

persed (i.e. removed and not eaten; grey bars) by mice. Lines on

bars show SE.

MUNOZ & BONAL: SEED CHOICES BY GRANIVOROUS RODENTS 713

DISCUSSION

Previous studies have found that rodents preferentiallyremove relatively large compared to small seeds (VanderWall 1994; Garb et al. 2000; Brewer 2001), a fact that isusually interpreted under optimal foraging theories giventhat the larger seeds offer higher nutritional rewards (Ker-ley & Erasmus 1991). However, in addition to the nutri-tional rewards animals also balance the costs associatedwith foraging (Stephens & Krebs 1986; Emlen 1996). Inthis context, larger seeds require longer times of handlingand transporting (Jacobs 1992), which may increase pre-dation risk of small rodents while foraging. These foragingcosts may counterbalance the preferences of rodents forlarge, more nutritious, seeds. We had hypothesized thatthe relationship between seed size and rodent size maybe critical in determining seed choices, because the costsof transporting a given seed would increase as the rodentsize decreases. Accordingly, we found a decrease in acornremoval as the acorn size increased in the small rodent(M. spretus) but not in the large one (A. sylvaticus), suggest-ing that transport costs impose upper limits to the seedsizes that the small species can remove profitably. The

main goal of this study was to assess explicitly the extentto which these costs depend on the rodent’s own size. Wefound that seeds representing 60% of rodent body massled to appreciable decreases in acorn removal rates, andseeds heavier than 70% of rodent body mass were in nocase removed. This critical ratio of 0.7 sharply constrainsthe range of Holm oak acorns suitable for M. spretus be-cause of its small size, but not for A. sylvaticus. For the lat-ter, the value of 0.7 would have constrained the removalof acorns heavier than 20 g, which are out of the rangeof acorn sizes produced by the Holm oak. Thus, the largestacorns of Q. ilex probably do not impose serious transportcosts to A. sylvaticus, and random removal may minimizethe time spent while selecting an acorn at the point of en-counter. As a consequence, A. sylvaticus removed a widerrange of variation in seed masses than M. spretus, whichagrees with studies on birds documenting that the rangeof seed sizes exploited increases with bird size (Wheel-wright 1985; Dıaz 1994).

We show that seed choices may result from balancinga variety of costs and benefits that are mediated by theratio of seed size to rodent size. These behaviouralcompromises have not been considered explicitly so farin the study of seed choices and seed dispersal by rodents.Rather, researchers have focused on the preferences forlarge or small seeds in different study systems and havenot considered the different ratios of seed size to rodentsize as a source of variability in the results obtained. Forinstance, Jansen et al. (2002) found that the larger seeds ofC. procera are cached farther than the smaller ones by My-oprocta exilis. In this system, the largest seeds were alwaysbelow 7% of the rodent body mass (ratio < 0.07) and thuscould be cached farther because of their lower transportcosts. By contrast, Brewer (2001) found that the smallerseeds of As. mexicanum are cached farther than the largerones by Heteromys desmarestianus. In Brewer’s study sys-tem, the largest seeds represented more than 25% of therodent body mass (ratio > 0.25) and thus may constrainseed caching at longer distances. Hence, it seems conve-nient to consider not only the size of seeds, but also therelative size of the rodents in the context of dispersal, atleast in the case of nut-like seeds like those of the Fagaceae(oaks, chestnuts, hazelnut etc.), which are among themost widespread trees in the temperate forests of theNorthern Hemisphere.

Our laboratory trials do not reproduce spatially ortemporally the environment where acorn dispersal takesplace, but this kind of experiment is useful to test specifichypotheses that are difficult to examine under naturalconditions (see Jenkins et al. 1995; Shimada 2001). We havedetermined in the laboratory that seed choices are influ-enced by the ratio seed size/rodent size, and further fieldstudies will help to strengthen our results and will godeep into the specific consequences of the dispersal behav-iour. However, our results put forward some direct implica-tions. Rodent size and seed size influence seed choices, andthus both may jointly affect the dispersal behaviour ofgranivorous rodents. In our study model, the larger species,A. sylvaticus, removed larger acorns and with a wider vari-ance in size than the smaller species, M. spretus, as the com-paratively higher ratios of seed size/rodent size in the latter

ANIMAL BEHAVIOUR, 76, 3714

limited their choice of the largest acorns. Thus, althoughboth species may enhance the dispersal of the largestacorns removed, as they ate preferentially the smaller seedsthat they had removed (see Steele et al. 1996; Jansen et al.2002), the critical ratio of 0.7 reduced significantly the re-moval (i.e. dispersal) of the largest seeds by the smallerrodent. This is evidenced by the lower size of acorns re-moved and not eaten by M. spretus in the experiments.Thus, the wide range of acorn size/rodent size ratios cov-ered by our study system may contribute to maintainingthe high variability of acorn size among Holm oaks (Bonalet al. 2007), as the two rodent species do not disperse pref-erentially the same optimum acorn size. In general, theseed size/rodent size ratios may help us to understand theseed dispersal patterns and seed size evolution in plantegranivore assemblages, provided that the community of ro-dents that disperse a given plant frequently encompassesdifferent-sized species (see Jensen 1985; Kollman et al.1998; Vander Wall 2003; Xiao et al. 2004; Tamura et al.2005). In such multispecific scenarios the seed size/rodentsize ratios are of particular relevance considering the grow-ing view that interactions between plants and animals needto be viewed from a more community-based perspectiverather than as simple pairwise comparisons (Strauss & Irwin2004).

Acknowledgments

We thank B. Nicolau and L. Arroyo for their assistance inthe experiments. M. Dıaz and P. A. Jansen providedhelpful comments that improved the manuscript. Micewere captured and maintained in the laboratory underlicense from the Consejerıa de Medio Ambiente (JCCM).This study was supported by the projects REN2003-07048/GLO (MEC), PAC-02-008 (JCCM) and 096/2002, 003/2007(MMA). A.M. and R.B. were supported by fellowships fromthe Junta de Comunidades de CastillaeLa Mancha. Ro-dent trappings and experiments were performed withlicense from the Junta de Comunidades de CastillaeLaMancha and the University of CastillaeLa Mancha.

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