Evol Ecol DOI 10.1007/s10682-006-9107-y ORIGINAL PAPER Satiation of predispersal seed predators: the importance of considering both plant and seed levels Raul Bonal Æ Alberto Mun˜ oz Æ Mario Dı´az Received: 11 November 2005 / Accepted: 10 August 2006 Ó Springer Science+Business Media B.V. 2006 Abstract Plants can reduce the fitness costs of granivory by satiating seed pre- dators. The most common satiation mechanism is the production of large crops, which ensures that a proportion of the seeds survive predation. Nevertheless, satiation of small granivores at the seed level may also exist. Larger seeds would satiate more efficiently, enhancing the probability of seed survival after having been attacked. However, a larger seed size could compromise the efficiency of satiation by means of large crops if there were a negative relationship between seed size and the number of seeds produced by an individual plant. We analyze both types of satiation in the interaction between the holm oak Quercus ilex and the chestnut weevil Curculio elephas. Both crop size and acorn size differed strongly in a sample of 32 trees. Larger crop sizes satiated weevils, and higher proportions of the seeds were not attacked as crop size increased. Larger seeds also satiated weevil larvae, as a larger acorn size increased the likelihood of embryo survival. Seedling size was strongly related to acorn size and was reduced by weevil attack, but seedlings coming from large weeviled acorns were still larger. The number and the size of the acorns produced by individual trees were nega- tively related. Larger proportions of the crop were infested in oaks producing less numerous crops of larger acorns. However, contrary to expectations, these trees did not satiate more effectively at the seed level either. Effective satiation by larger acorns was precluded by larger multi-infestation rates associated to smaller seed crops, in such a way that the proportion of attacked seeds that survived did not vary among trees with different acorn sizes. These results highlight the need of considering satiation by means of large crops and large seeds in studies of predispersal seed predation. Long-term monitoring on individual oaks will help to assess whether there is a trade-off between the number and the size of the acorns R. Bonal Æ A. Mun˜ oz Æ M. Dı´az Departamento de Ciencias Ambientales, Facultad de Ciencias del Medio Ambiente, Universidad de Castilla-La Mancha, Toledo, Spain R. Bonal (&) Department of Entomology, Natural History Museum, Cromwell Road, SW7 5BD London, UK e-mail: [email protected] 123 Evol Ecol and, if it existed, how it could condition the fitness consequences of both types of satiation. Keywords Seed size Æ Seed number Æ Predispersal seed predation Æ Satiation Æ Multi-infestation Æ Granivorous insects Æ Curculio Æ Quercus Introduction Seed consumption (granivory) causes fitness costs to plants, as it reduces their reproductive output. Plants have evolved both resistance and satiation strategies to reduce these fitness costs. Resistance mechanisms preclude consumption and include physical barriers like hard seed coats, awns or characteristic shapes (Harper et al. 1970; Janzen 1971; Kelrick et al. 1986;Dı´az 1996; Hulme and Benkman 2002), or chemical defences such as toxic or deterrent compounds (Janzen 1971,Dı´az 1996, Hulme and Benkman 2002). Satiation does not prevent consumption but reduces its negative consequences (Stowe et al. 2000), and may be achieved by large seed crops (Crawley 1997). In the case of the strategies against granivory, resistance/satiation trade-offs are evident. The formation of physical barriers or the synthesis of chemical defences requires resources that cannot be employed elsewhere, so that large investments on the protection of individual seeds impair the capacity of producing large seed crops (Hulme and Benkman 2002). Satiation of granivores has been considered almost exclusively from the point of view of the mother plant. It has been estimated as the number of seeds saved depending on crop size, considering all the seeds consumed by granivores to be killed. However, many species of granivorous insects do not always consume seeds completely (see Oliver and Chapin 1984; Dalling et al. 1997; Mack 1998; Siscart et al. 1999; Branco et al. 2002; Sousa et al. 2003). Attacked seeds whose embryo is not predated and that retain enough reserves for seedling devel- opment after consumption may be viable (Oliver and Chapin 1984; Branco et al. 2002; Sousa et al. 2003). Both embryo survival and the amount of reserves left would increase with seed size (Dalling et al. 1997; Mack 1998; Sousa et al. 2003). Thus, besides the widely considered satiation at the plant level, satiation at the seed level should be taken into account. Plants could thus reduce the negative fitness consequences of granivorous insect attacks by both satiating with large crops and large seeds. However, several studies have found negative relationships between seed size and the number of seeds pro- duced (Eriksson and Jakobsson 1999; Parciak 2002; review in Sakai and Harada 2001). Such an inverse relationship might preclude the combination of both types of satiation by the same individual plant. Moreover, a smaller number of seeds at a plant level could increase the likelihood for a seed to suffer multi-infestation, as this risk could increase when the number of seeds available for the insects decreases (Desouhant et al. 2000). If large-seeded individuals also produce smaller seed crops, the increased effectiveness of satiation at the seed level could be impaired by an increased number of larvae per seed, as more seed tissue would be needed to satiate them. The physical and chemical protection of oak Quercus spp. seeds is usually weak, whereas satiation of oak seed predators by means of large crops is widespread (Crawley 1997; Hulme and Benkman 2002). Usually, satiation in oaks has been 123 Evol Ecol studied at the population level giving rise to the concept of ‘‘masting’’. Masting consists in large seed crops synchronized among trees and separated by a variable number of low crop seasons (reviews in Kelly (1994) and Kelly and Sork (2002)). The proportion of seeds (acorns) consumed or attacked by granivores, especially insects, is generally much lower in mast than in lean years (Crawley and Long 1995). On the other side, it is known that acorns are not always consumed completely by insects, so that infested acorns can germinate and produce viable seedlings (Oliver and Chapin 1984; Soria et al. 1996; Siscart et al. 1999; Branco et al. 2002). Larger acorns could have higher chances of satiating developing insect larvae before they reach the embryo (Siscart et al. 1999). However, it has not been explicitly addressed whether producing large acorns could be an effective satiation strategy, and whether satiation at this level could interact with satiation by means of large crops. The aim of the present study was to analyze both types of satiation at individual trees. We carried out a study with the holm oak Quercus ilex and its more prevalent predispersal seed consumer, the chestnut weevil Curculio elephas, a specialist insect whose larvae develops inside the acorns. We specifically tested (1) whether large seed crops could satiate weevils by comparing the proportion of acorns attacked among isolated trees differing in the number of acorns produced; (2) whether large acorns could satiate weevil larvae; (3) whether there is a negative relationship be- tween the number and the size of the acorns produced; and (4) whether the number of acorns produced by a tree influenced the likelihood of multi-infestation and the amount of cotyledon left uneaten in the infested acorns. On this basis, we will compare the relative contribution of both satiation strategies in terms of the final reproductive output of holm oaks. Material and methods Study area The study was carried out in the Caban˜ eros National Park (Ciudad Real province, central Spain; 39°24¢ N, 3°35¢ W). The vegetation of the Park is Mediterranean, being oaks (Quercus suber, Q. ilex, Q. faginea and Q. pyrenaica) the main tree species. Our study site was located in the flat lowlands of the Park, whose tree populations are dominated by holm oaks Quercus ilex. The original tall shrubland with scattered trees that occupied these lowlands (Jime´nez 1998) was cleared and ploughed long before the declaration of the National Park in 1995, as it happened in most part of the Iberian Peninsula from the Middle Ages onwards (Dı´az et al. 1997; Pulido et al. 2001; Pulido and Dı´az 2002). The resulting landscape is savannah-like, with holm oak trees scattered within a grassland matrix. The study site had a surface of 7 ha, with a mean tree density of 13.28 trees/ha. Study species The holm oak is the most widespread tree species of the Iberian Peninsula, extending over more than five million hectares (Blanco et al. 1997). It is a Medi- terranean evergreen oak whose crops can be very large (up to 38,000 acorns/tree), although with a strong inter-annual variability (Rupe´rez 1957; Herrera et al. 1998). Holm oak acorns are eaten by a large variety of animals, from insects to ungulates 123 Evol Ecol (Dı´az et al. 1993, 1995;Dı´az and Martı´n 1998; Leiva and Ferna´ndez-Ale´s 2003, 2005; Go´ mez 2004a; Pulido and Dı´az 2005). Acorn size is extremely variable, with values ranging between 1 and 14 g (Rupe´rez 1957; Pulido and Dı´az 2002,Go´ mez 2004b). The embryo is located at the pointed, distal end of the acorn. Most seed biomass is composed by the two large cotyledons, which constitute the reserves for seedling development. Mean acorn mass varies among populations (Rupe´rez 1957) and among individuals within populations (Soria et al.