American Journal of Botany 96(7): 1255–1261. 2009.
The greater nutritional value (e.g ., in terms of nitrogen con-
tent) of seeds, in comparison to other plant structures, makes
them a highly profi table resource for the vertebrates and inver-
tebrates that prey upon them ( Janzen, 1971 ). As a consequence,
intense seed predation (frequently greater than 50% and some-
times affecting the individual ’ s entire seed crop) occurs over a
wide range of plant species and habitats ( Crawley, 1992 ; Hulme,
1998 ). Seed predation has the capacity to strongly impact plant
population dynamics by affecting plant regeneration, coloniza-
tion ability, and spatial distribution ( Louda, 1982 ; Hulme, 1997 ;
Pic ó and Retana, 2000 ). Ultimately, seed predators have the po-
tential to act as agents of natural selection that infl uence seed
traits ( Hulme and Benkman, 2002 ). Accordingly, plants deploy
a variety of mechanisms to lessen the impact of predation on a
plant ’ s seed crop or on an individual seed.
Some plants prevent or reduce predation via traits in their
fruits and seeds that can function as predator deterrents. Ex-
amples of such traits include thick, spiny fruits, hard seed coats,
or defensive, toxic chemical compounds in the seed ’ s en-
dosperm ( Janzen, 1969 ; Rosenthal and Bell, 1979 ; Grubb et al.,
1998 ). Defense mechanisms involving any trait that reduces
consumption of plant tissue and/or negatively affects herbivore
performance are referred to as resistance traits ( Strauss and
Agrawal, 1999 ). However, given the abundance, diversity, and
effi ciency of predators, seeds are unlikely to be able to prevent
or deter attack by deploying only one or a few defensive traits.
An alternative set of antipredation mechanisms involves
traits that allow seeds to tolerate damage from predators ( Valle-
jo-Mar í n et al., 2006 ). Plant tolerance traits have been studied
much less than resistance traits, particularly in seed – predator
interactions ( Rosenthal and Kotanen, 1994 ; Xiao et al., 2007 ).
However, growing evidence suggests that tolerance traits in
seeds might play an important role in the likelihood of seeds
becoming seedlings in the face of predation ( Mack, 1998 ; Dal-
ling and Harms, 1999 ; Vallejo-Mar í n et al., 2006 ; Xiao et al.,
2007 ). Tolerance traits, such as the capacity to germinate after
some degree of damage (i.e., mass loss) or the ability to re-
sprout after extensive damage to the young seedling ’ s stem,
have been shown for seeds with relatively large reserve mass,
either in absolute terms or relative to the size of its predators. In
these species, an oversized package of reserves can be a proxi-
mate trait that reduces the impacts of predation and has been
assumed to be, at least in part, an adaptive response to intense
seed attack ( Dalling and Harms, 1999 ).
Tolerance has been studied by comparing the patterns of ger-
mination of intact seeds (and the growth of the seedlings they
produce) against the response of seeds naturally infested by in-
sects or of seeds in which contrasting levels of damage have
been experimentally simulated by removing a portion of en-
dosperm ( Dalling et al., 1997 ; Harms and Dalling, 1997 ;
Dalling and Harms, 1999 ; Fukumoto and Kajimura, 2000 ;
Branco et al., 2002 ; Edwards and Gadek, 2002 ; Leiva and
Fern á ndez-Al é s, 2005 ; Vallejo-Mar í n et al., 2006 ). However,
with very few exceptions, seed tolerance to damage caused by
vertebrates has not been evaluated under naturally varying lev-
els of damage (but see Steele et al., 1993 ), despite the fact that
vertebrates (e.g., rodents) cause major losses to individual seeds
or plant seed crops ( Crawley, 1992 ; Hulme, 1998 ). Evidence of
seed tolerance comes from studies carried out with a small sub-
set of species, predominantly from tropical forests (e.g., Janzen,
1976 ; Harms and Dalling, 1997 ; Dalling and Harms, 1999 ;
Vallejo-Mar í n et al., 2006 ). The scant information from temperate
1 Manuscript received 30 September 2008; revision accepted 6 March 2009.
The authors thank G. G ó mez, M. Rosenfi eld, and B. Ruiz-Guerra for
assistance in the fi eld and greenhouse. L. Lopes provided valuable help on
statistical analyses. R. Von Itter and D. Wilson provided logistical support
in the greenhouse. An earlier draft of this paper was greatly improved by
comments from N. Chiariello, D. Hansen, and two anonymous reviewers.
2 Author for correspondence (e-mail: firstname.lastname@example.org);
present address: Universidad Nacional Aut ó noma de M é xico, Centro de
Investigaciones en Ecosistemas, Antigua Carretera a P á tzcuaro 8701, Col.
Ex-Hacienda de San Jos é de la Huerta, CP 58190, Morelia, Michoac á n,
M é xico
SEED TOLERANCE TO PREDATION: EVIDENCE FROM
THE TOXIC SEEDS OF THE BUCKEYE TREE
( AESCULUS CALIFORNICA ; SAPINDACEAE) 1
EDUARDO MENDOZA 2 AND RODOLFO DIRZO
Department of Biology, Stanford University, Stanford, California 94305-5020 USA
Tolerance, the capacity of plants to withstand attack by animals, as opposed to resistance, has been poorly examined in the
context of seed predation. We investigated the role that the seed mass of the large-seeded endemic tree Aesculus californica plays
as a tolerance trait to rodent attack by comparing, under greenhouse conditions, patterns of germination, and subsequent seedling
growth, of seeds with a wide range of natural damage. Germination percentage was reduced by 50% and time to germination
by 64% in attacked compared to intact seeds, and germination probability was negatively correlated with damage. Seedlings that
emerged from intact seeds were taller and bore more leaves than those from damaged seeds. This species ’ large seed mass favors
tolerance to damage because heavily damaged seeds are able to germinate and produce seedlings. This fi nding is signifi cant given
that seeds of this species are known to contain chemical compounds toxic to vertebrates, a resistance trait. We posit that this com-
bination of tolerance and resistance traits might be a particularly effective antipredation strategy when seeds are exposed to a va-
riety of vertebrate predators.
Key words: Aesculus californicus ; California buckeye tree; Jasper Ridge; large-seeded plant; resistance traits; rodent seed
predation; Sapindaceae; tolerance traits.
AMERICAN JOURNAL OF BOTANY
like infl orescences. Fruits generally enclose one glossy brown seed 2 – 5 cm
long, with a fresh mass of about 50 g ( Hickman, 1993 ; Mooney and Bartho-
lomew, 1974 ). All parts of the plant are considered toxic to humans and live-
stock because of the presence of glycosidal compounds ( Kubo and Ying, 1992 ;
Callahan, 2005 ). Flowers are poisonous to honey bees, but native insects such
as the checkerspot ( Euphydryas chalcedona ) and the pale swallowtail ( Papilio
eurymedon ) butterfl ies consume its nectar with no apparent deleterious effects
( Murphy et al., 1984 ; Hickman, 1993 ; Callahan, 2005 ). Seeds of this species
were used by Native Americans to make fl our after removing the toxic com-
pounds in a lengthy leaching process, and preparations from seeds or bark were
used to treat several diseases and even to facilitate fi sh capture by forcing them
to swim toward the water surface ( Mooney and Bartholomew, 1974 ; Kubo and
Ying, 1992; Anderson and Roderick, 2006 ).
Seed collection — In December 2006, we collected 137 seeds: of these 89
were intact, and 48 were naturally attacked. To prevent a signifi cant removal of
resources from the ground at the Jasper Ridge Biological Preserve, we were
restricted to collecting nuts along trails running through woodland areas. Al-
though our sample included seeds from several maternal trees, our collection
protocol, coupled with the limited sample size, prevented us from analyzing our
results in terms of genetic family effects. Our results represent, therefore, a
random collection of several genetic families.
Collected seeds were weighed and measured (length). Rodent attack is read-
ily recognizable by incisor marks ( Fig. 1 ), and is caused mainly by tree squirrels
( Sciurus sp.) (E. Mendoza, personal observation). Percentage of seed mass lost
to rodent consumption was estimated visually by comparison with intact seeds
of similar size. In a greenhouse at 25 ° C at Stanford University, each seed was
placed on the surface of soil in pots (11.3 L) and watered daily. Seeds were
monitored for germination, sprouting, and, after establishment, for leaf produc-
tion and growth in height. We recorded the time to germination and the percent-
age of germination over time for intact and damaged seeds (regardless of the
magnitude of damage). We also assessed the probability of germination as a
function of the degree of seed damage. For these analyses, a seed was defi ned
as germinated when the root was clearly visible. We also quantifi ed the time
until sprouting (i.e., the number of days it took for germinated seeds to produce
a main stem with its fi rst leaf).
We compared the growth of seedlings that emerged from intact and attacked
seeds in terms of (1) the temporal pattern of leaf production measured since
sprouting and (2) the increment in height growth, measured as the distance from
the soil to the insertion point of the newest, fully developed leaf at a date that
roughly corresponded to day 40 since germination.
Statistical analysis — We evaluated the impact of damage on seed germina-
tion with a G -test of independence (using Williams ’ correction; Sokal and
Rohlf, 2003). The same analysis was used to examine differences in the number
of seeds that sprouted after germination. We compared time to germination and
to sprouting (once germination occurred) between intact and attacked seeds
with a Wilcoxon two-sample test and its associated U -statistic (with correction
for tied ranks and sample sizes > 20; Sokal and Rohlf, 2003). The impact of
degree of attack on the probability of germination was evaluated with a logistic
regression analysis, using percentage of mass lost to predation as the explana-
tory variable, and whether the seed germinated (1) or not (0) as the response
variable. Analyses were carried out using the program JMP version 4.0.2 (SAS
Institute, Cary, North Carolina, USA).
Using the lme function of the R programming language (R Development
Core Team, 2008), we fi tted a mixed-effects model to analyze leaf production
accounting for correlation of measurements within individuals ( Crawley, 2002 ).
The fi xed effect was seed condition (intact, attacked), the random effect was
time nested within individual seeds, and the response variable was number of
leaves per plant. The variables time and number of leaves were square-root
transformed to meet model assumptions of continuity and linearity. Residuals
of the model were inspected for any trend in a plot of fi tted values vs. standard-
ized residuals. We compared growth rates (height divided by the number of
days since sprouting) between seedlings from intact and attacked seeds with a
Wilcoxon two-sample test in the same way we compared time required to ger-
minate and sprout (Sokal and Rohlf, 2003).
We examined the relationship between mass of intact seeds and number of
leaves produced at three different times over the course of the experiment with
linear regression analysis using JMP version 4.0.2. Seed mass was the explana-
tory variable, and number of leaves was the response variable. We combined
seedling size data for the periods 6 – 8, 14 – 16, and 34 – 36 d. The number of
leaves was Box – Cox transformed to yield a continuous response variable and
meet assumptions of homoscedasticity and normality of residuals.
zones comes largely from studies performed with species of the
genus Quercus ( Steele et al., 1993 ; Meiners and Handel, 2000 ;
Fukumoto and Kajimura, 2000 ; Branco et al., 2002 ; Xiao et al.,
2007 ). Therefore, studies evaluating mechanisms of seed resis-
tance/tolerance in other temperate forest plants can further our
understanding of the relative importance of these strategies
among the suite of mechanisms plants deploy to lessen the ef-
fects of seed predators. Likewise, a more realistic understand-
ing of the degree of seed tolerance/resistance may be gained by
using natural levels of damage (as opposed to artifi cial damage)
caused by predators, particularly rodents, whose impact has
been rarely assessed in this context.
In this study, we experimentally examined the tolerance that
seeds of the endemic buckeye tree, Aesculus californica (Spach)
Nutt., may have to damage caused by rodents in a Mediterra-
nean ecosystem in California. This species is particularly inter-
esting because its seeds contain compounds that are toxic to a
variety of animals, including vertebrates ( Mooney and Bartho-
lomew, 1974 ; Kubo and Ying, 1992 ), and at the same time, it
produces very large seeds (with large reserve mass), which can
be attractive to vertebrate predators. Therefore, this species
seems to combine traits that can potentially operate as tolerance
(large mass) and resistance (toxic metabolites) mechanisms.
The way tolerance, resistance, and other traits interact to reduce
the impact of predators on plants is poorly understood ( Xiao et
al., 2007 ).
We assess the nature of antipredation mechanisms by specifi -
cally examining the impact that variation in natural levels of
seed damage has on (1) seed germination, (2) seedling sprout-
ing, and (3) seedling growth of the buckeye tree under controlled
experimental conditions. We hypothesized: (1) If resistance is
the primary mechanism that A. californica seeds deploy to deal
with the attack of vertebrate predators (as the reported presence
of defensive compounds suggests; discussed later) seeds would
have no damage or very low levels of damage in the fi eld; more-
over, if damage were present, germination, sprouting, and seed-
ling growth should be negatively and strongly impacted. In
contrast, (2) if A. californica seeds are using tolerance as a
mechanism to deal with predation, intact seeds should be rare,
while relatively high damage should be common and even heav-
ily damaged seeds should still be able to germinate and produce
seedlings that perform well. Finally, (3) if we fi nd that intact
seeds as well as seeds with a wide range in levels of damage in
the fi eld, and even heavily damaged seeds, are able to germi-
nate, sprout, and produce seedlings, then the toxic seeds of A.
californica might be using a combination of resistance and tol-
erance traits to deal with the attack by predators.
MATERIALS AND METHODS
Study species — Aesculus californica is a large shrub or tree (4 – 12 m) in the
family Sapindaceae. Its distribution is restricted to the coastal and Sierran foot-
hill regions of California with mediterranean-type climate, although some
populations have been reported in Oregon ( Mooney and Bartholomew, 1974 ;
Hickman, 1993 ; Callahan, 2005 ). Aesculus californica trees are associated with
mesic habitats such as those found near streams. In our study site, the Jasper
Ridge Biological Preserve of Stanford University, A. californica occurs pre-
dominantly in mesic microenvironments, but it can also be found in dryer mi-
croenvironments. It is one of the most common trees in our study site, with the
second highest value of importance, following oaks ( Quercus spp.) (R. Dirzo,
unpublished data). The leaves of this tree abscise and fall during the middle of
the summer drought, before fruit development from late summer to fall/early
winter (see Mooney and Bartholomew, 1974 ). Fruits of A. californica are
spherical or slightly three-lobed, leathery capsules, borne at the tip of panicle-
MENDOZA AND DIRZO — TOLERANCE TO SEED PREDATION IN BUCKEYE
unable to germinate ( Fig. 2B ), there was a signifi cant relation-
ship between percentage of seed mass loss and germination
probability. The logistic regression shows that germination
probability gradually decreased as the percentage of mass con-
sumed increased ( P = 0.0045, N = 51; Fig. 2B ).
Seedling growth — We found that the rates of growth, mea-
sured as height increment, were higher for seedlings that emerged
from intact seeds (median = 1.21 cm/day) than for seedlings
emerged from attacked seeds (median= 0.87 cm/day; U s = 853.5,
P = 0.012) ( Fig. 3A ). Likewise, we found a signifi cant effect of
seed condition (attacked or intact, P = 0.027), time ( P < 0.001),
and their interaction ( P < 0.001) on seedling growth (leaf pro-
duction). This result refl ects that, with time, the number of leaves
per plant increasingly differed between seedlings emerging from
the two types of seed ( Fig. 3B ). At the end of the experiment,
seedlings that emerged from intact seeds had four more leaves,
on average, than seedlings from attacked seeds.
Regression analyses to examine the relationship between
seed mass of intact seeds and size (number of leaves) of seed-
lings at three different times after germination ( Fig. 3C ) showed
that size of seedlings was not affected by seed mass at day 7 of
growth, because the slope of the relationship was statistically
indistinguishable from zero ( R 2 = 0.007, P = 0.4967, N = 69,
Fig. 3C ). In contrast, we found an increasingly signifi cant posi-
tive relationship between seed mass and seedling size with time
Seed characterization — Mean mass ( ± 1 SE) of intact seeds
( N = 137) was 58.1 ± 1.9 g ( Fig. 1 ), while seeds with evidence
of vertebrate attack ( N = 48) had a mean mass of 45.7 ± 3.2 g.
Although the typical estimated damage (mass loss) among at-
tacked seeds was relatively low (median = 28%), the range was
considerable, extending from 3% to a striking 90% ( Fig. 1 ).
Patterns of germination — Seed predation had a positive im-
pact on the speed of germination. The median time for germina-
tion of attacked seeds was almost one-third the median time for
germination of intact seeds ( U s = 1644.5, P < 0.001; Fig. 2A ).
In contrast, the germination potential of attacked seeds was re-
duced nearly by half: only 25 of 47 (53.2%) germinated, while
among intact seeds, 79 of 81 (97.5%) did so ( Fig. 2A ). This con-
trast in germination success was highly signifi cant ( G =39.18,
df = 1, P < 0.001). Moreover, while 91% of the intact seeds that
germinated were able to sprout, only 72% of the attacked and
germinated seeds sprouted ( G =17.57, df = 1, P < 0.001). In
contrast, there was no difference in the median time to sprout
between attacked and intact seeds that germinated (13 and 12 d,
respectively; U s = 787.5, t = 1.52, P = 0.13; data not shown).
Seeds that did not germinate had rotted by the end of the study.
Although there was considerable variation in damage levels
among seeds that germinated, as well as among seeds that were
Fig. 1. Damage to attacked seeds of Aesculus californica collected at the Jasper Ridge Preserve, California. Top, left to right, photographs of damage
categories: > 0 – 20, > 40 – 60, and > 80%. Bottom, frequency of seeds in categories of damage; broken line shows median (Me) damage.
AMERICAN JOURNAL OF BOTANY
( R 2 = 0.117, P = 0.0132, N = 52, at day 15; and R 2 = 0.120, P =
0.0110, N = 53, at day 35).
Effects of rodent attack on germination and sprouting pat-
terns — Attack by rodents had a clear impact on the performance
of seeds and seedlings of A. californica . On the one hand, attack
reduced germination success, sprouting, and growth of seedlings.
On the other hand, attack by rodents signifi cantly reduced the
time to germination. Among intact seeds, germination success
( > 97%), as well as subsequent sprouting (91%), were markedly
high. Intact seeds of the closely related species A. octandra are
also reported to have very high levels of germination success in
Fig. 2. Impact of damage to seeds of Aesculus californica on germina-
tion. (A) Germination of intact (black dots) and attacked (white dots) seeds
over time in the greenhouse. Me I = median number of days to germination
for intact seeds; Me A = median number of days to germination for attacked
seeds. (B) Relationship between seed damage and the probability of germi-
nation. Central panel shows the relationship as described by logistic re-
gression analysis. Upper and lower box-plots show the distribution of
damage for seeds that germinated and of those that failed to germinate,
respectively; lines of boxes indicate from left to right, 25th percentile, me-
dian, and 75th percentile; whiskers indicate 90th and 10th percentiles.
Fig. 3. Relationship between damage and seedling growth. (A)
Growth rates of seedlings that emerged from intact and attacked seeds,
measured from sprouting to approximately day 40 of development. Bot-
tom, central, and upper lines in boxes correspond respectively to the 25th
percentile, median, and 75th percentile. Whiskers indicate 10th and 90th
percentiles. (B) Number of leaves per plant, over time, of seedlings that
emerged from intact (black dots) and attacked (white dots) seeds. Each
data point corresponds to the mean of between 18 and 34 intact seeds and
between 8 and 14 attacked seeds. Error bars represent ± 1 SE. (C) Relation-
ship between the weight of intact seeds and the size (number of leaves) of
their corresponding seedlings at three different times during the experi-
ment. Diamonds correspond to day 7 ( R 2 = 0.007, P = 0.49), triangles to
day 15 ( R 2 = 0.117, P = 0.01), and stars to day 35 ( R 2 = 0.120, P = 0.01).
MENDOZA AND DIRZO — TOLERANCE TO SEED PREDATION IN BUCKEYE
In the case of A. californica , we posit that the consequences of
predation would depend on the timing of attack. For example,
because seed release of A. californica usually starts late in the
dry season, early attack leading to early germination might ex-
pose seeds to desiccation. On the contrary, if attack occurs after
the onset of the rainy season, early germination might allow
seedlings emerged from attacked seeds to have an earlier start
to take full advantage of the rainy season to grow. Elucidation
of the net effect of accelerated germination for the performance
of A. californica seedlings warrants further work.
The possible incidence of multiple events of attack on a sin-
gle seed might reduce the effectiveness of tolerance as a way to
deal with the effects of predation. However, observations from
an ongoing experiment in the fi eld suggest that the incidence of
repeated events of attack by vertebrates is low (E. Mendoza,
Because predators displace seeds upon attack (E. Mendoza,
unpublished data), the possibility arises of predation also operat-
ing as a means of secondary dispersal. An important role of sec-
ondary dispersal by rodents for seedling establishment has been
suggested in a closely related species, A. turbinata ( Hoshizaki
et al., 1997 ). It is known from other temperate, large-seeded spe-
cies that rodents such as squirrels scatter-hoard seeds for later
consumption and, in doing so, protect seeds from attack by other
vertebrate and invertebrate predators ( Vander Wall, 1990 ).
Moreover, when cached or scatter-hoarded seeds are not recov-
ered, germination and seedling establishment may be favored.
Likewise, it has been proposed that during the time seeds remain
cached and during germination, the concentration of chemical
compounds decreases, making seeds more accessible to consum-
ers ( Smallwood et al., 2001 ). Therefore, the infl uence seed mass
might have in plant performance does not conclude at the germi-
nation and early seedling growth stages, but includes the poten-
tial for seedlings to resprout or compensate for foliage loss
caused by folivores ( Dalling and Harms, 1999 ). Large seeds may
thus be an adaptation to enable plants to resprout once dispersed
by rodents, and not only an adaptation to grow faster. How patterns
of seed dispersal and attack relate to seed mass variation and
seedling establishment is an important next step to examine for
A. californica at our study site.
Effects of rodent attack on seedling performance — Attack
affected not only germination but also seedling growth. Seed-
lings that emerged from attacked seeds were shorter and had
fewer leaves than did seedlings that were the same age but
emerged from intact seeds. These results indicate that seedlings
that emerged from attacked seeds were able to only partially
compensate for the effect of seed damage.
The contrast in size between seedlings that emerged from in-
tact and attacked seeds and the fact that a relationship between
seed mass and seedling size became increasingly evident with
time suggest that seed reserves were used not only to subsidize
the initial growth of seedlings but also to support their longer-
term growth. These fi ndings are consistent with the fact that
seeds attached to the fully developed seedlings still had a no-
ticeable amount of endosperm, which was gradually exhausted
as seedlings grew, and with the report that seedling survival and
growth are affected by experimental cotyledon excision weeks
after germination in large-seeded species such as Q. rugosa
( Bonfi l, 1998 ) and Gustavia superba ( Dalling and Harms, 1999 ;
Kitajima, 2003 ).
Larger size can help seedlings escape from the many hazards
they face during their growth, including herbivory, competition,
the fi eld ( Levy, 1984 ). In comparison, only 53% of the attacked
seeds germinated, and 72% of these germinated seeds sprouted.
Therefore, in spite of the negative effects of attack on germina-
tion and sprouting, a relatively large proportion (38%) of the ini-
tial number of attacked seeds produced seedlings, compatible
with the hypothesis that seeds of A. californica are able to toler-
ate attack by vertebrate predators probably because of their large
mass. However, there was a large amount of variation in the per-
centage of mass loss among attacked seeds that successfully ger-
minated and also among those that failed to germinate. These
results suggest that, in contrast to what happens in some species
of oak, in which vertebrate consumption of the endosperm con-
taining the embryo is discouraged by the presence of tannins
( Steele et al., 1993 ), in the case of A. californica , rodents may on
occasion kill seeds (i.e., impede their germination).
Germination success of partially attacked seeds is usually re-
duced compared to the germination of intact seeds ( Janzen,
1976 ; Cipollini and Stiles, 1991 ; Koptur, 1998 ; Fukumoto and
Kajimura, 2000 ; Branco et al., 2002 ; Leiva and Fern á ndez-Al é s,
2005; Vallejo-Mar í n et al., 2006 ; Xiao et al., 2007 ), but damage
has also been shown not to have a signifi cant effect on ( Dalling
et al., 1997 ; Vallejo-Mar í n et al., 2006 ) or to even increase
( Karban and Lowenberg, 1992 ; Steele et al., 1993 ) germina-
tion. This variation in the response of seeds of different species
to damage seems to be a function of the level of attack they re-
ceive but also of their level of tolerance to damage ( Janzen,
1976 ; Koptur, 1998 ; Branco et al., 2002 ). For example, in some
species seed damage affecting just 10% of endosperm mass
leads to a complete failure to germinate ( Vallejo-Mar í n et al.,
2006 ), while other species such as Prioria copaifera are able
to fully compensate, because germination of seeds in which
mass losses are as high as 60% is similar to that of intact seeds
( Dalling et al., 1997 ). Results of this study indicate that A. cali-
fornica falls in the category of species with a great capacity to
tolerate seed damage because seeds with up to 75% of their
mass consumed are able to germinate.
Seeds of A. californica attacked by rodents germinated faster
than intact seeds, a response similar to that observed in acorns
of Quercus suber and Q. mongolica , seeds of the shrubs Sesba-
nia drummondii and Gossypium spp. infested by insects, and
some tropical rain forest species in which damage was artifi -
cially infl icted ( Karban and Lowenberg, 1992 ; Branco et al.,
2002 ; Ceballos et al., 2002 ; Vallejo-Mar í n et al., 2006 ; Yi and
Zhang, 2008 ). Observed reductions in the time to germination
as a consequence of insect infestation range from 17% in Q.
mongolica to 42% (high seed damage) in Q. suber ( Branco
et al., 2002 ; Yi and Zhang, 2008 ). Therefore, it seems that
within a certain range of variation, increased seed mass loss
caused by animal attack may lead to faster germination. Mecha-
nisms that may be involved in this effect include a release in the
physical constraint that the endosperm imposes on radical elon-
gation ( Branco et al., 2002 ), an increase in the activity of en-
zymes such as amylase that promote germination ( Yi and
Zhang, 2008 ), and scarifi cation of the seed coat ( Karban and
Lowenberg, 1992 ; Koptur, 1998 ). Yet, regardless of the spe-
cifi c underlying mechanism, the question remains as to what
consequences this change in germination time has on seedling
establishment. Increased speed of germination in attacked seeds
might be adaptive by allowing early seedling emergence before
intraspecifi c competition intensifi es, thus favoring chances of
establishment ( Karban and Lowenberg, 1992 ). However, the
consequences of increased speed of germination due to preda-
tion are context-dependent (see Karban and Lowenberg 1992 ).
AMERICAN JOURNAL OF BOTANY
FUKUMOTO , H. , AND H. KAJIMURA . 2000 . Effects of insect predation on
hypocotyl survival and germination success of mature Quercus vari-
abilis acorns. Journal of Forest Research 5 : 31 – 34 .
GREEN , P. T. , AND P. A. JUNIPER . 2004 . Seed mass, seedling herbivory and
the reserve effect in tropical rainforest seedlings. Functional Ecology
18 : 539 – 547 .
GRUBB , P. J. , D. J. METCALFE , E. A. A. GRUBB , AND G. D. JONES .
1998 . Nitrogen-richness and protection of seeds in Australian tropi-
cal rainforest: A test plant defence theory. Oikos 82 : 467 – 482 .
HARMS , K. E. , AND J. W. DALLING . 1997 . Damage and herbivory tolerance
through resprouting as an advantage of large seed size in tropical trees
and lianas. Journal of Tropical Ecology 13 : 617 – 621 .
HICKMAN , J. C. [ed.], 1993 . The Jepson manual, higher plants of California.
University of California Press, Berkeley, California, USA.
HOSHIZAKI , K. , W. SUZUKI , AND S. SASAKI . 1997 . Impacts of secondary
seed dispersal and herbivory on seedling survival in Aesculus tur-
binata. Journal of Vegetation Science 8 : 735 – 742 .
HULME , P. E. 1997 . Post-dispersal seed predation and the establishment of
vertebrate dispersed plants in Mediterranean scrublands. Oecologia
111 : 91 – 98 .
HULME , P. E. 1998 . Post-dispersal seed predation: Consequences for plant
demography and evolution. Perspectives in Plant Ecology, Evolution
and Systematics 1 : 32 – 46 .
HULME , P. E. , AND C. W. BENKMAN . 2002 . Granivory. In C. Herrera and O.
Pellmyr [eds.], Plant – animal interactions: An evolutionary approach,
132 – 154. Blackwell Scientifi c Publications, Oxford, UK.
JANZEN , D. H. 1969 . Seed-eaters versus seed size number, toxicity and dis-
persal. Evolution 23 : 1 – 27 .
JANZEN , D. H. 1971 . Seed predation by animals. Annual Review of Ecology
and Systematics 2 : 465 – 492 .
JANZEN , D. H. 1976 . Reduction of Mucuna andreana (Leguminosae) seed-
ling fi tness by artifi cial seed damage. Ecology 57 : 826 – 828 .
KARBAN , R. , AND G. LOWENBERG . 1992 . Feeding by seed bugs and wee-
vils enhances germination of wild Gossypium species. Oecologia 92 :
196 – 200 .
KITAJIMA , K. 2003 . Impact of cotyledon and leaf removal on seedling
survival in three tree species with contrasting cotyledon functions.
Biotropica 35 : 429 – 434 .
KOPTUR , S. 1998 . Effects of seed damage on germination in the common
vetch ( Vicia sativa l.) . American Midland Naturalist 140 : 393 – 396 .
KUBO , I. , AND B.-P. YING . 1992 . Phenolic constituents of California buck-
eye fruit. Phytochemistry 31 : 3793 – 3794 .
LEIVA , M. J. , AND R. FERN Á NDEZ-AL É S . 2005 . Holm-oak ( Quercus ilex
subsp. Ballota ) acorns infestation by insects in Mediterranean dehe-
sas and shrublands its effect on acorn germination and seedling emer-
gence. Forest Ecology and Management 212 : 221 – 229 .
LEVY , F. 1984 . The demography of sweet buckeye ( Aesculus octandra
Marsh.) seeds and seedlings. Bulletin of the Torrey Botanical Club
111 : 307 – 315 .
LOUDA , S. M. 1982 . Limitation of the recruitment of the shrub Haplopappus
squarrosus (Asteraceae) by fl ower- and seed-feeding insects. Journal
of Ecology 70 : 43 – 53 .
MACK , A. L. 1998 . An advantage of large seed size: Tolerating rather than
succumbing to seed predators. Biotropica 30 : 604 – 608 .
MEINERS , S. J. , AND S. N. HANDEL . 2000 . Additive and nonaddi-
tive effects of herbivory and competition on tree seedling mor-
tality, growth, and allocation. American Journal of Botany 87 :
1821 – 1826 .
MOONEY , H. A. , AND B. BARTHOLOMEW . 1974 . Comparative carbon bal-
ance and reproductive modes of two Californian Aesculus species.
Botanical Gazette 135 : 306 – 313 .
MURPHY , D. D. , M. S. MENNINGER , AND P. R. EHRLICH . 1984 . Nectar source
distribution as a determinant of oviposition host species in Euphydryas
chalcedona. Oecologia 62 : 269 – 271 .
PIC Ó , F. X. , AND J. RETANA . 2000 . Temporal variation in the female fi tness
components of reproductive success over the extended fl owering sea-
son of a Mediterranean perennial herb. Oikos 89 : 485 – 492 .
R DEVELOPMENT CORE TEAM . 2008 . R: A language and environment for
statistical computing. R Foundation for Statistical Computing, Vienna,
Austria. Website http://www.R-project.org .
or physical damage. In addition, seed size correlates with the
capacity to repetitively resprout after severe shoot damage
( Dalling et al., 1997 ; Dalling and Harms, 1999; Green and Juni-
per, 2004 ). Therefore, while the large reserves in the seeds of A.
californica seem to be a proximate trait providing tolerance to
the damage caused by rodent attack, it remains to be tested what
the impact of seed attack is on seedling growth and plant estab-
lishment in the fi eld, as compared to the performance of seed-
lings emerged from intact seeds. Moreover, the demographic
consequences of predation leading to seed or seedling death de-
pend on the critical number of plants that can be recruited into
the population ( Louda, 1982 ). If tolerance to damage allows the
buckeye tree to escape partial damage by predators, resulting in
later plant recruitment, large seed mass could be seen as an
adaptive trait for the species.
The seeds of A. californica seem to combine traits related to
resistance (presence of chemical compounds) as well as toler-
ance to predation. This combination of antipredation traits can
be a profi table strategy in ecological settings where mortality
hazards vary in time and space and seeds are exposed to a vari-
ety of predators ( Xiao et al., 2007 ). Moreover, because contacts
(probability of encountering) between seeds and predators are
more likely to result in plant death than contacts between estab-
lished plants and herbivores, the presence of a combination of
defense mechanisms might be particularly favored in seeds as a
strategy to reduce the impact of a coterie of omnipresent preda-
tors (in our case, potentially, deer, mice, squirrels, and inverte-
brates) and increase plant regeneration and population growth.
ANDERSON , K. , AND W. RODERICK . 2006 . California buckeye, Aesculus cali-
fornica (Spach) Nutt. Plant guides. USDA, NRCS National Plant Data
Center, Baton Rouge, Louisiana, USA. Website http://plants.usda.
gov/plantguide/pdf/cs_aeca.pdf [accessed 15 February 2008] .
BONFIL , C. 1998 . The effects of seed size, cotyledon reserves, and her-
bivory on seedling survival and growth in Quercus rugosa and Q.
laurina (Fagaceae). American Journal of Botany 85 : 79 – 87 .
BRANCO , M. , C. BRANCO , H. MEROUANI ,
2002 . Germination success, survival and seedling vigor of Quercus
suber acorns in relation to insect damage. Forest Ecology and
Management 166 : 159 – 164 .
CALLAHAN , F. 2005 . Plant of the year: California buckeye ( Aesculus cali-
fornica (Spach) Nutt.) . Kalmiopsis 12 : 9 – 15 .
CEBALLOS , L. , C. ANDARY , M. DELESCLUSE , M. GIBERNAU , D. MCKEY ,
AND M. HOSSAERT-MCKEY . 2002 . Effects of sublethal attack by a
sucking insect, Hyalymenus tarsatus , on Sesbania drummondii seeds:
Impact on some traits related to fi tness. Ecoscience 9 : 28 – 36 .
CIPOLLINI , M. L. , AND E. W. STILES . 1991 . Seed predation by the bean
weevil Acanthoscelides obtectus on Phaseolus species: Consequences
for seed size, early growth and reproduction. Oikos 60 : 205 – 214 .
CRAWLEY , M. J. 1992 . Seed predators and population dynamics. In M.
Fenner [ed.], Seeds: The ecology of regeneration in plant communi-
ties, 157 – 191. CAB International, Wallingford, UK.
CRAWLEY , M. J. 2002 . Stastical computing an introduction to data analy-
sis using S-Plus. John Wiley and Sons, New York, New York, USA.
DALLING , J. W. , AND K. E. HARMS . 1999 . Damage tolerance and cotyle-
donary resource use in the tropical tree Gustavia superba. Oikos 85 :
257 – 264 .
DALLING , J. W. , K. E. HARMS , AND R. AIZPR Ú A . 1997 . Seed damage toler-
ance and seedling resprouting ability of Prioria copaifera in Panam á .
Journal of Tropical Ecology 13 : 481 – 490 .
EDWARDS , W. , AND P. GADEK . 2002 . Multiple resprouting from diaspores
and single cotyledons in the Australian tropical tree species
Idiospermum australiense. Journal of Tropical Ecology 18 : 943 – 948 .
AND M. H. ALMEIDA .
MENDOZA AND DIRZO — TOLERANCE TO SEED PREDATION IN BUCKEYE
ROSENTHAL , G. A. , AND E. A. BELL . 1979 . Naturally occurring, toxic non-
protein amino acids. In G. A. Rosenthal and D. H. Janzen, [eds.],
Herbivores: Their interaction with secondary plant metabolites, 353 –
385. Academic Press, New York, USA.
ROSENTHAL , J. P. , AND P. M. KOTANEN . 1994 . Terrestrial plant tolerance
to herbivory. Trends in Ecology & Evolution 9 : 145 – 148 .
SMALLWOOD , P. D. , M. A. STEELE , AND S. H. FAETH . 2001 . The ultimate
basis of the caching preferences of rodents, and the oak-dispersal syn-
drome: Tannins, insects, and seed germination. American Zoologist
41 : 840 – 851 .
SOKAL , R. R. , AND F. J. ROHLF . 2003 . Biometry. W. H. Freeman, New
York, New York, USA.
STEELE , M. A. , T. KNOWLES , K. BRIDLE , AND E. L. SIMMS . 1993 . Tannins
and partial consumption of acorns: Implications for dispersal of oaks
by seed predators. American Midland Naturalist 130 : 229 – 238 .
STRAUSS , S. Y. , AND A. A. AGRAWAL . 1999 . The ecology and evolution
of plant tolerance to herbivory. Trends in Ecology & Evolution 14 :
179 – 185 .
VALLEJO-MAR Í N , M. , C. A. DOM Í NGUEZ , AND R. DIRZO . 2006 . Simulated
seed predation reveals a variety of germination responses of
neotropical rain forest species. American Journal of Botany 93 :
369 – 376 .
VANDER WALL , S. B. 1990 . Food hoarding in animals. University of
Chicago Press, Chicago, Illinois, USA.
XIAO , Z. , M. K. HARRIS , AND Z. ZHANG . 2007 . Acorn defenses to herbivory
from insects: Implications for the joint evolution of resistance, toler-
ance and escape. Forest Ecology and Management 238 : 302 – 308 .
YI , X. F. , AND Z. B. ZHANG . 2008 . Infl uence of insect-infested cotyledons on
early growth of Mongolian oak, Quercus mongolica. Photosynthetica
46 : 139 – 142 .