Animal Behaviour xxx (2012) 1e8

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

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

choices and seed variability
Alberto Muñoz a, b, *, Raúl Bonal b, c, d, Josep Maria Espelta b
a
Departamento de Didáctica de la Ciencias Experimentales, Facultad de Educación, Universidad Complutense de Madrid, Madrid, Spain
b
CREAF, Cerdanyola del Vallès, Spain
c
Grupo de la Biodiversidad Genética y Cultural, Departamento de Ecología, Instituto de Recursos Cinegéticos (CSIC-UCLM-JCCM), Ciudad Real, Spain
d
Grupo 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
Seed preferences of scatter-hoarding granivores may influence the evolution of seed traits in plants.
Article history: However, there is little evidence linking the granivores’ responses to specific seed traits to the variability
Received 23 May 2012 of seeds in a single plant species. This information is essential for understanding how the decisions of
Initial acceptance 21 June 2012 granivores can shape plant life histories. We analysed how seed morphology (size and shape) of the
Final acceptance 4 September 2012 Holm oak, Quercus ilex, influences seed choices of the seed-disperser, the Algerian mouse, Mus spretus.
Available online xxx We studied the seed variability of the oak and whether the frequency of seed phenotypes matched the
MS. number: 12-00390R seed choices of the disperser. The probabilities of seed removal decreased as the seeds became larger and
more bullet-shaped, so that seeds that were simultaneously large and bullet-shaped had the lowest
Keywords: probabilities of being dispersed. These seeds are probably refused by rodents because they impose higher
acorn
handling and transport costs. The size and shape of the Holm oak seeds were highly variable between
Algerian mouse
trees, but extraordinarily consistent within a single tree over different years. However, the analysis of
animaleplant interaction
handling cost
seed variability revealed a disproportionately low frequency of large bullet-shaped phenotypes, which
hoarding behaviour are those barely removed by rodents. Seed preferences of dispersers of species with high seed variability
Holm oak between trees can lead to differences in the chances of seeds produced by different trees being dispersed.
Mus spretus Those seed phenotypes preferred by dispersers could make a higher contribution to the next generation,
Quercus ilex which could influence the evolution and variability of seeds in a plant species.
seed caching Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
small rodent

Many plant species depend on the removal and dispersal of their
seeds by seed-caching animals for successful recruitment (Vander
Wall 1990; Jansen et al. 2002; den Ouden et al. 2005; Roth &
Vander Wall 2005; Steele et al. 2006; Briggs et al. 2009; Xiao
et al. 2009; Muñoz & Bonal 2011). In these species, it is thought
that dispersers’ preferences for certain seed features may influence
the evolution of seed traits (Vander Wall 2010). This hypothesis is
mainly supported by cross-species comparisons, so that the larger
seed size of zoochorous species would be explained by dispersers’
preferences for large, more nutritious seeds (e.g. Smith & Reichman
1984; Leishman et al. 1995; Hammond et al. 1996; Vander Wall
2003; Moles et al. 2003, 2005). However, differences between
seed species may be caused by phylogenetic effects not linked to
selection pressures imposed by dispersers. This makes it more
difficult to disentangle the seed traits potentially influenced by
* Correspondence: A. Muñoz, Departamento de Didáctica de las Ciencias Exper-
imentales, Facultad de Educación, Universidad Complutense de Madrid, C/Rector
Royo Villanova s/n Ciudad Universitaria, 28040 Madrid, Spain.
E-mail address: alberto.munoz.munoz@edu.ucm.es (A. Muñoz).
dispersers (Herrera 1992; Jordano 1995a). Intraspecific approaches
are much less common, despite the fact that they provide better
models for analysing selection pressures of animals on specific seed
traits (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 traits
could be subjected to selection pressures if they are highly variable
between individual plants, consistent within the same mother
plant and over time, and heritable (see Jordano 1995b).
Seed shape has received much less attention than seed size in
the context of seed choices of animals. Dispersers prefer larger
seeds because of their higher nutrient content (Jansen et al. 2004;
Xiao et al. 2004; Muñoz & Bonal 2008a), but their choices may also
depend on the costs of handling and transporting the seeds (Kerley
& Erasmus 1991; Jacobs 1992; Emlen 1996). In this context, a large
seed size can impose higher transport costs on dispersers (Muñoz &
Bonal 2008a), but seed shape may also affect their seed choices if it
influences handling and transport costs. Thus, two seeds of the
same size but different shape can provide the same amount of
nutrients, yet entail different handling and transport costs. Hence,

0003-3472/$38.00 Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.anbehav.2012.09.011

Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011
2 A. Muñoz et al. / Animal Behaviour xxx (2012) 1e8

the combination of size and shape may be relevant for seed choices
of dispersers and could have further consequences for seed trait
evolution. Similarly, fruit choices of avian frugivores could have
affected the evolution of fruit morphology in endozoochorous
plants, in which larger fruits are more bullet shaped to facilitate
swallowing of the fruit (see Herrera 1992).
In this study, we analysed the intraspecific variability of seed
morphology (seed size and seed shape) between and within
mother trees in the Holm oak, Quercus ilex, over different years. We
studied how seed morphology influenced seed choices of the main
seed-dispersing rodent, the Algerian mouse, Mus spretus, and
compared the extent to which the natural distribution of seed
phenotypes matched the preferences of dispersers. The acorn fall
season in the Holm oak lasts from September to December (Bonal &
Muñoz 2007), and during this period the Algerian mouse removes
and caches hundreds of acorns several metres away from the
canopies of the mother oaks (Leiva & Fernández-Alés 2003; Muñoz
& Bonal 2008b, 2011). This rodent’s decision whether or not to
remove Holm oak acorns from under the tree is critical to acorn
dispersal, given that acorns dropped beneath mother oaks suffer
high predation pressure from various seed predators and thus have
fewer chances of recruiting than those dispersed beyond mother
oaks (Bonal & Muñoz 2007; Muñoz & Bonal 2011).
In the Holm oak, acorn size shows high variability, from 0.5 to
15 g (Bonal et al. 2007; Bonal & Muñoz 2008), and also high vari-
ation in shape (i.e. the ratio between seed length and transversal
diameter) 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 of
M. spretus in the laboratory, (2) the natural variability and temporal
consistency of acorn shape and size between and within Holm oaks
in the field, and (3) whether the frequency of the different acorn
phenotypes observed in the Holm oak matches the foraging pref-
erences shown by seed-caching rodents.
METHODS
Study Area and Study Species
The study area was at the Cabañeros National Park (39
240 N,
3
350 W Ciudad Real, central Spain), a nature reserve representative
of Mediterranean oak forests where the Holm oak is the most
common tree species (details of the study area can be found in
Bonal et al. 2007; Muñoz et al. 2009). Holm oak crops can be very
large, although with strong interannual variability (Bonal & Muñoz
2007; Espelta et al. 2008). The Algerian mouse is a small species
(8e23 g) that accounts for more than 95% of the rodent population
at the study area (Muñoz et al. 2009). The other species present is
the wood mouse, Apodemus sylvaticus. Algerian mice and Holm
oaks often occur in the same area because both thrive in dry
Mediterranean environments. Other acorn predators at the study
site 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 habitat
requirements of this corvid.
Seed Choice Experiments
Seed choice experiments were performed in the laboratory,
where we could control rodent body mass as an independent
variable in foraging choices. This is very important because the
‘seed mass/rodent mass’ ratio determines the actual transport costs
and thus conditions seed removal behaviour (Muñoz & Bonal
2008a). We captured 20 adult M. spretus at the study area with
standard Sherman live-traps. Traps were set between 1200 and
1600 hours GMT and checked daily between 0700 and 0900 hours
GMT on 3 consecutive days. Each trap was baited with a piece of
apple 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

Figure 1. Intraspecific variability of acorn shape and size in the Holm oak, Quercus ilex. In this species, acorns range from almost spherical to bullet shaped. Each acorn belongs to
a different mother tree.

Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011
 A. Muñoz et al. / Animal Behaviour xxx (2012) 1e8
captured rodents from cold and rain (Muñoz et al. 2009). Once
trapped, the rodents made a nest with the cotton provided and
consumed some of the apple. We captured one pregnant female
and five juveniles, which were immediately released. No lactating
females were caught during our 3-day trapping.
We carried the adult nonbreeding rodents to the University of
Castilla-La Mancha facilities in their provisional nests made inside
the traps. The rodents were captured in the middle of the acorn fall
season (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 housed
indoors in terraria (60  32 cm and 30 cm high) filled with a layer
of sand 5 cm deep and provided with a piece of waterproof cotton
for use as nesting material. Hamster food, fruit and water were
provided ad libitum. Each mouse was kept in its home terrarium
with a light:dark cycle of 12:12 h for 10 days prior to the trials, to
ensure that it became familiarized with the new environment.
Seed choice trials were conducted indoors in 2  2 m arenas in
which each of the 20 rodents captured (10 male and 10 female) was
given 40 acorns collected at the study area. These acorns repre-
sented the seed mass and shape variability (the ratio between
acorn 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 40
acorns used on each experimental rodent were selected to match
the variability of size and shape existing in the field. We checked
that the variance in acorn mass and shape was the same between
and within individual rodents to ensure that acorn samples were
not 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 selected
and weighed with a digital balance (to the nearest 0.01 g),
measured with a digital calliper (to the nearest 0.01 mm), and
marked with a small number written with an odourless pencil.
Weevil-infested acorns were discarded as they are rejected by this
rodent species (Muñoz & Bonal 2008b). Researchers/technicians
wore fresh gloves while handling seeds to minimize possible
human 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 (body
mass: 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 home
terrarium with the rodent inside was placed in one corner. Two
cages (23  9 cm and 8 cm high) equipped with a small piece of
cotton were also placed on two sides of the arena simulating
sheltered sites in order to stimulate the experimental rodent to
remove and hoard the acorns. The trial started at 2000 hours GMT,
when the simulated ‘daylight’ was turned off in the experimental
room (this rodent species is nocturnal). We adjusted the duration of
the experiments (4 days with a light:dark cycle of 12:12 h) and the
number of seeds offered to each rodent (40) to ensure that the
rodents had enough time to select and remove some seeds so as to
enable us to measure their seed preferences. After the 4 days of
each experiment, we noted whether the 40 acorns had been
removed or eaten. Over the 4 days of testing, eaten acorns were not
replenished and the only food source available to each experi-
mental rodent was the 40 acorns. After each trial, the arena was
carefully cleaned with nonperfumed soap and water to eliminate
site-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 Medio
Ambiente (JCCM-2003), Ministry of Environment (Regional
Government of Castilla, La Mancha). All experimental rodents were
healthy during the trials and, once the experiments ended, they
were released at the sites where they had been captured. To ease
Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011
3
their return to field, the rodents were released on warm, sunny
days.
Seed Trait Variability in Holm Oaks
We selected and geopositioned 27 Holm oaks randomly
distributed throughout the study area. In these focal trees we
monitored for 4 consecutive years (2002e2005) acorn shape and
mass. We set seed traps hung under the canopies that were
emptied every 15 days from the outset to the end of the acorn fall
season. Each year, we weighed (to the nearest 0.01 g) and measured
the length and width (to the nearest 0.01 mm) of at least 15 sound
acorns per tree (Bonal et al. 2007). We also measured and weighed
more than 5000 acorns collected from 100 additional oaks at the
study area to analyse the relationship between acorn shape and
acorn mass in the Holm oak population.
Data Analyses
In the analyses of acorn choice of rodents we considered the
acorn mass/rodent mass ratio as an independent variable, since the
transport costs depend simultaneously both on the mass of
the seed and that of the rodent (Muñoz & Bonal 2008a). Using
a generalized linear model with a forward stepwise procedure we
tested whether acorn removal (a dependent variable with a bino-
mial distribution) was influenced by the seed/rodent mass ratio
and acorn shape (independent variables). With the data from the
acorn choice experiments we developed a function to predict the
probabilities of acorn removal (P) based on acorn shape (S) and
the acorn mass/rodent mass ratio (R).
We used general linear models to analyse how acorn mass and
shape varied between trees and over the years, and also regressions
to study the relationships between acorn size and shape in the focal
trees. To assess intraindividual repeatability in acorn mass and
shape, we calculated the coefficients of variation (CVs) for the
acorns of each tree. Then, we compared the CVs of mass and shape
with a repeated measures ANOVA in which the variable ‘tree’ was
the within-subjects factor accounting for the association of both
types of CVs within the same tree. To check for any potentially
confounding effect of spatial autocorrelation on the acorn mass or
shape in the focal trees, we also performed two Mantel tests. We
tested whether differences in acorn mass and shape between oaks
were related to the geographical distance between them.
Finally, the relationships of acorn mass with acorn length and
width were analysed using 5236 acorns that were collected,
weighed and measured from 100 random trees to test which
function best fitted the data distribution. We used a chi-square test
to assess whether the frequency of phenotypes of acorn shapes was
randomly distributed within the range of acorn masses, that is,
whether there was any tendency for larger or smaller acorns to be
more bullet shaped or round.
RESULTS
Seed Choice of Rodents
Rodents removed on average 75.6% of acorns and ate 50.1% of them
(partially or completely eaten). The generalized linear model showed
that acorn removal was first influenced by the acorn mass/rodent
mass ratio (estimate  SE ¼ 2.88  0.58, Wald ¼ 24.32, P < 0.0001),
so that the probability of a given rodent removing an acorn decreased
as the acorn mass/rodent mass ratio increased. The model showed
that acorn shape also had a significant effect on the probability of
acorn removal (estimate  SE ¼ 0.79  0.28, Wald ¼ 8.08, P ¼ 0.004),
which decreased as the acorn length/acorn width ratio increased.
4 A. Muñoz et al. / Animal Behaviour xxx (2012) 1e8

Similarly, removed acorns were on average more spherical (shape:
mean  SE ¼ 2.17  0.01, N ¼ 604) than those not removed by
rodents (shape: mean  SE ¼ 2.27  0.02, N ¼ 195; F1, 794 ¼ 32.66,
P < 0.0001). Thus, large and bullet-shaped acorns were less likely to
be removed by rodents, and the function predicting the probability of
acorn removal (Pr) on the basis of acorn shape (S) and the acorn mass/
rodent mass ratio (R) clearly showed that the probability of being
removed was lower for bullet-shaped acorns when they had a higher
acorn/rodent mass ratio (Pr ¼ 0.315 þ 0.662  Se0.179  Re
0.181  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 between
the 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 mean
acorn 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 in
either 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 highly
repeatable within the same tree (CVs: mean  SE: shape:
0.006  0.001; size: 0.094  0.011), but repeatability for shape was
stronger than for mass (repeated measures ANOVA for comparisons
of CVs: F1, 26 ¼ 68.72, P < 0.0001). Moreover, the consistency over
the 4-year period (between year X and year Xþ1) was stronger for
acorn 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
fact, we found significant interannual changes in acorn mass (F3,
101 ¼ 3.89, P ¼ 0.011), with trees producing heavier acorns in 2003
than in other years (Tukey HSD: all P values < 0.05), whereas no
significant 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 over
100 Holm oaks, we found that acorn shape was biased within the
acorn mass range (c2 ¼ 10413.4, P < 0.0001), and found a low
frequency 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 fitted
a 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 grow
basically in width and, accordingly, the masselength regression
slopes 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 within
a single plant species can influence the foraging decisions of its
seed-dispersing rodent. Our seed choice experiments showed that
Algerian mice avoided removing large and bullet-shaped seeds of
the Holm oak. Seed traits in this species varied sharply between
different trees, but showed high repeatability within the same tree
and over time, so that Holm oaks producing large bullet-shaped

1
Probabillty of

0.8

0.6
acorn removal

0.4

0.2

0
0.
3.4 1
3.2 0.
3 2
0. e
2.8 3
siz
0. t
2.6 4 en
Ac 2.4 0. od
or
n 2.2
5
e/r
sh
ap 2 0.
6 siz
1.8 n
e 0. or
1.6
7 Ac
0.
1.4 8

Figure 2. Relationship between probability of acorn removal by the Algerian mouse, Mus spretus, acorn shape (the ratio between acorn length and acorn width), and the ratio
between acorn mass and rodent mass.

Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011
 A. Muñoz et al. / Animal Behaviour xxx (2012) 1e8 5

7
(a)

1
Acorn dry mass and shape

0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
Oak

5.5
(b)

4.5

3.5

2.5

1.5

1
2002 2003 2004 2005

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

acorns may have fewer chances of dispersal by Algerian mice, thus
decreasing their recruitment contribution to the next generation.
This might have changed the frequency of seed phenotypes in the
population of Holm oaks over evolutionary time, as the lack of large
and 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 to
dispersers 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 trait
variability prevents potentially confusing effects concurrent with
plant species identity and, hence, it offers a better scenario for

Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011
6 A. Muñoz et al. / Animal Behaviour xxx (2012) 1e8

4
3.8 (a)
3.6
3.4
3.2
Acorn shape 3
2.8
2.6
2.4
2.2
2
1.8
1.6
1.4
1.2
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
60
57
54 (b)
51
Length/width (mm)

48
45
42
39
36
33
30
27
24
21
18
15
12
9
6

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Acorn mass (g)

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) with
acorn mass.

analysing selection pressures on specific seed traits. At the intra-
specific level, seed traits could be subjected to selection pressures if
they were variable between mother plants, repeatable at the
intraindividual level and over time, heritable and relevant for seed
dispersal likelihood. Other studies have failed to find links between
foraging decisions of animals and variability of seed phenotypes
because selection pressures are diffuse within the whole seed
dispersal process (Pollux et al. 2007) or because intraspecific seed
variability is very high within the same mother plant (Jordano
1995b). However, in our study system we found a high variation
in the size and shape of seeds between different mother trees,
a high consistency of these traits within the same mother tree, and
clear seed trait preferences of scatter-hoarding rodents. This
scenario provides a good model system for investigating how
disperser decisions can influence seed trait evolution.
Recently, Wang & Chen (2009) experimentally showed that
physical traits of seeds, such as size, are more important for the
decisions of seed-caching rodents than other seed traits such as
chemical composition. This is probably because physical traits
influence the costs of handling and transporting seeds for small
animals (Jacobs 1992; Muñoz & Bonal 2008a). We recorded some of
the experimental rodents and observed that they always trans-
ported the acorns by gnawing the distal point and holding them
with the head up. Hence, for a given rodent, the higher the acorn
weight is, the higher the transport cost (Muñoz & Bonal 2008b). In
addition, 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 more
spherical acorns. This would explain why an acorn’s removal
probabilities diminished notably when it was both heavy and bullet
shaped (Fig. 2). The greater difficulties of transporting large, bullet-
shaped acorns may represent a serious handicap for acorn dispersal
that could explain why there is a lack of large, bullet-shaped
phenotypes in the population of Holm oaks studied. It is very
likely that trees producing large, bullet-shaped acorns may have
fewer chances of dispersal, thus decreasing their recruitment and
contribution to the next generation. The removal of acorns by
M. spretus from beneath mother canopies is critical for the natural
recruitment of Holm oaks at the study area (Muñoz & Bonal 2007,
2011), given the mortality of acorns not taken away from the
mother trees (Pulido & Díaz 2005; Bonal & Muñoz 2007; Muñoz &
Bonal 2011).
The low intraindividual and temporal variability of acorn traits
suggests that they may have a genetic basis, as has been reported
for other plant species (Cober et al. 1997; Salas et al. 2006; Robert
et al. 2008). Also, the lack of spatial correlation in our study trees
rules out any significant environmental effect on seed
morphology.

Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011
 A. Muñoz et al. / Animal Behaviour xxx (2012) 1e8
Although shape and mass were highly consistent over the years,
seed mass varied more than seed shape. This variation may respond
to annual changes in the availability of resources in temperate areas
(rain, nutrients, etc.), which often lead to changes in seed size or
seed numbers across years (Espelta et al. 2008, 2009; Koenig et al.
2009). In fact, the larger seed size of Holm oaks documented in
2003 could have been caused by the rainy autumn in that year at
the study area. The consistency of shape is maintained regardless of
changes in the available resources, suggesting that the amount of
resources invested in each seed (i.e. seed mass) is independent of
the way the resources are organized at the seed level (i.e. seed
shape). This makes it possible for different trees to produce seeds of
the same mass but different shape (Figs 1, 3a).
We have found a relationship between seed preferences of
a seed disperser and the frequency of seed variability of the plant it
disperses. Seed morphologies with a lower probability of dispersal
were represented less within the range of seed phenotypes in
a natural population. However, we have no direct evidence that the
Algerian mouse has influenced the evolution of seed morphology in
the Holm oak. On the one hand, it would be worthwhile to have
data on the heritability of seed traits, even though in long-lived
species such as oaks a seedling takes several decades to become
an adult tree that produces seeds. On the other hand, there are
other acorn predators that could also impose different selection
pressures on acorn traits, such as insects (Bonal et al. 2007; Espelta
et al. 2009), ungulates (Gómez 2004) or other rodents, larger than
M. spretus, such as A. sylvaticus (Muñoz & Bonal 2008a), which may
contribute to maintaining a greater seed trait variability depending
on their responses to seed traits. Recent studies have suggested that
in-depth investigation of the behavioural responses of animals to
plant propagules is important for improving our understanding of
seed 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 to
track the individual decisions of seed dispersers (Jordano & Schupp
2000; Cousens et al. 2010). Thus, further studies on this topic will
help to shed light on the role of granivores in the functional
significance 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 the
projects 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 ‘Juan
de la Cierva’ contracts. S. Rutherford and two anonymous referees
provided helpful comments that improved the manuscript.
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Please cite this article in press as: Muñoz, A., et al., Responses of a scatter-hoarding rodent to seed morphology: links between seed choices and
seed variability, Animal Behaviour (2012), http://dx.doi.org/10.1016/j.anbehav.2012.09.011