The greater nutritional value (e.g., in terms of nitrogen content) of seeds, in comparison to other plant structures, makes them a highly profitable resource for the vertebrates and invertebrates that prey upon them (22). As a consequence, intense seed predation (frequently greater than 50% and sometimes affecting the individual's entire seed crop) occurs over a wide range of plant species and habitats (7; 19). Seed predation has the capacity to strongly impact plant population dynamics by affecting plant regeneration, colonization ability, and spatial distribution (30; 18; 35). Ultimately, seed predators have the potential to act as agents of natural selection that influence seed traits (20). 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. Examples of such traits include thick, spiny fruits, hard seed coats, or defensive, toxic chemical compounds in the seed's endosperm (21; 37; 14). Defense mechanisms involving any trait that reduces consumption of plant tissue and/or negatively affects herbivore performance are referred to as resistance traits (42). However, given the abundance, diversity, and efficiency 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 (43). Plant tolerance traits have been studied much less than resistance traits, particularly in seed–predator interactions (38; 45). 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 (31; 9; 43; 45). Tolerance traits, such as the capacity to germinate after some degree of damage (i.e., mass loss) or the ability to resprout 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 proximate trait that reduces the impacts of predation and has been assumed to be, at least in part, an adaptive response to intense seed attack (9).

Tolerance has been studied by comparing the patterns of germination of intact seeds (and the growth of the seedlings they produce) against the response of seeds naturally infested by insects or of seeds in which contrasting levels of damage have been experimentally simulated by removing a portion of endosperm (10; 15; 9; 12; 3; 11; 28; 43). However, with very few exceptions, seed tolerance to damage caused by vertebrates has not been evaluated under naturally varying levels of damage (but see 41), despite the fact that vertebrates (e.g., rodents) cause major losses to individual seeds or plant seed crops (7; 19). Evidence of seed tolerance comes from studies carried out with a small subset of species, predominantly from tropical forests (e.g., 23; 15; 9; 43). The scant information from temperate zones comes largely from studies performed with species of the genus Quercus (41; 32; 12; 3; 45). Therefore, studies evaluating mechanisms of seed resistance/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 effects of seed predators. Likewise, a more realistic understanding of the degree of seed tolerance/resistance may be gained by using natural levels of damage (as opposed to artificial 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 Mediterranean ecosystem in California. This species is particularly interesting because its seeds contain compounds that are toxic to a variety of animals, including vertebrates (33; 27), 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 (45).

We assess the nature of antipredation mechanisms by specifically examining the impact that variation in natural levels of seed damage has on (1) seed germination, (2) seedling sprouting, 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 field; moreover, if damage were present, germination, sprouting, and seedling 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 heavily damaged seeds should still be able to germinate and produce seedlings that perform well. Finally, (3) if we find that intact seeds as well as seeds with a wide range in levels of damage in the field, and even heavily damaged seeds, are able to germinate, sprout, and produce seedlings, then the toxic seeds of A. californica might be using a combination of resistance and tolerance traits to deal with the attack by predators.