Acta Oecologica 36 (2010) 227e233 Contents lists available at ScienceDirect Acta Oecologica journal homepage: www.elsevier.com/locate/actoec Original article The impact of specialist and generalist pre-dispersal seed predators on the reproductive output of a common and a rare Euphorbia species Mário Boieiro a,*, Carla Rego b, Artur R.M. Serrano a, Xavier Espadaler c a Centro de Biologia Ambiental/Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, 1749-016 Lisboa, Portugal b Grup de Biologia Evolutiva (GBE), Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain c CREAF and Unitat d'Ecología, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain article info abstract Article history: Pre-dispersal seed predators can have a severe impact on the reproductive output of their hosts, which Received 31 August 2009 can translate into negative effects on population dynamics. Here we compared the losses due to specialist Accepted 8 January 2010 and generalist insect seed predators in two Euphorbia species, a rare (Euphorbia welwitschii) and Published online 4 February 2010 a common one (Euphorbia characias). Pre-dispersal losses to specialist seed-wasps (Eurytoma jaltica) and generalist hemipterans (Cydnus aterrimus and Dicranocephalus agilis) were on average higher for the rare Keywords: E. welwitschii than for its widespread congener. In both Euphorbia species, the variation in losses to Seed predation specialist and generalist seed predators was not related with traits indicative of plant size, fecundity, or Seed-feeding insects Congeneric species isolation. Nevertheless, the temporal variation in losses to seed-wasps seemed to be intimately associ- Plant rarity ated with the magnitude of yearly variation in fruit production. The impact of seed-wasps and hemip- terans on the reproductive output of both Euphorbia species was additive, though there was evidence for infochemical-mediated interference at the fruit level. The moderate levels of seed predation in E. welwitschii, together with the results from the comparative analysis with its widespread congener, suggest that insect seed predation is not a causal effect of plant rarity. Ó 2010 Elsevier Masson SAS. All rights reserved. 1. Introduction usually feed directly upon the seeds or use them as oviposition sites, ensuring a rich food resource for the development of their From anthesis until seed germination the reproductive potential progeny. Many studies have reported that pre-dispersal seed of a plant species diminishes progressively as a consequence of the predation by insects could be extremely severe, frequently leading losses imposed by a variety of factors acting in conjunction or to losses greater than 50% of the total seed crop (Crawley, 2000; sequentially. Despite the plurality of causes governing the repro- Fenner and Thompson, 2005; Kolb et al., 2007). Even so, several ductive success of plant species, seed predation has frequently been authors (e.g., Janzen, 1971; Andersen, 1988) claim that estimations reported as a major form of seed mortality (Janzen, 1971; Crawley, of insect pre-dispersal seed predation are still conservative or even 2000) with seeds being consumed both before and after the misleading due to the inadequacy of the sampling methodology. dispersal phase. Although either form of seed predation may Therefore, the loss of seeds as a result of predation may be impose considerable reproductive losses (Hulme, 2002), pre- a potential threat for plant population growth or maintenance. dispersal seed predation has also the potential to negatively Various examples have highlighted how insect seed predation has influence seed dispersal mechanisms. For example, by damaging clearly the potential to affect the population dynamics of its host fruits pre-dispersal seed predators may render them unattractive to species by limiting plant recruitment (Louda, 1982a,b; Louda and frugivorous dispersers and even contribute to a lower number of Potvin, 1995; Kelly and Dyer, 2002; Münzbergová, 2005), which plantedisperser interactions (e.g., Jordano, 1987; Sallabanks and may ultimately lead to population decline. This was the case stated Courtney, 1992; Izhaki, 1998; Bas et al., 2005). Pre-dispersal seed by Hegazy and Eesa (1991) where extraordinarily heavy seed predators belong to a variety of animal groups, but many of them predation by bruchid beetles was considered a major threat to the are inconspicuous specialized insects that attack a particular plant existence of the narrow endemic Ebenus armitagei. According to species or a few closely related species (Hulme, 2002). These insects some authors, the impact of seed predators on the reproductive output of endemic plants may represent a mechanism that might help explain plant rarity (e.g., Lavergne et al., 2005; Münzbergová, fi * Corresponding author. Tel.: þ351 21 750 0000; fax: þ351 21 750 0028. 2005). Other studies, however, identi ed other factors that corre- E-mail address: [email protected] (M. Boieiro). late with commonerare differences and found no evidence for 1146-609X/$ e see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2010.01.001 228 M. Boieiro et al. / Acta Oecologica 36 (2010) 227e233 a key role of seed predation in determining plant rarity (Fiedler, number of individuals (less than 20 individuals) and the observa- 1987; Simon and Hay, 2003; Lavergne et al., 2004). tion of recruitment failure during consecutive years in several of Insect seed predators, particularly the host-specific ones, can them may be indicative of their susceptibility to the negative effects also act as important selective forces by exerting consistent selec- of small population size (M. Boieiro, unpubl. data). During the last tion on particular plant traits (Zimmerman, 1980; Brody and century, E. welwitschii suffered a considerable decline as a result of Mitchell, 1997; Caruso, 2001; Cariveau et al., 2004). Pre-dispersal habitat destruction, which is still considered the major threat to its seed predators may, together with pollinators and other flower existence. visitors, drive flowering synchrony, flowering phenology and In both Euphorbia species, the fruit is a trilocular green capsule influence inflorescence characteristics, flower size and flower enclosing one smooth carunculate seed per loculum. The fruits longevity (Brody, 1997; Fenner et al., 2002; Wright and Meagher, differ in external morphology since the capsules of E. characias are 2003; Strauss and Whittall, 2006). pubescent while those of E. welwitschii are glabrous and somewhat Some of the few studies comparing pre-dispersal seed predation thicker. During fruit maturation seed predators are regularly in co-occurring closely related plant species revealed how partic- observed puncturing or ovipositing in full-sized fruits. Two kinds of ular plant traits may correlate with levels of insect damage. Green insect predators are responsible for reproductive losses in both and Palmbad (1975) stated that differential predation on two Euphorbia species: a specialist seed-wasp, Eurytoma jaltica Zerova Astragalus species may be due to differences in fruit morphology (Eurytomidae) and generalist hemipterans, Cydnus aterrimus and biochemistry, fruit internal temperature, and seed energy (Forster) (Cydnidae) and Dicranocephalus agilis (Scopoli) (Sten- contents. They found that lower levels of seed predation were ocephalidae). The seed-wasp E. jaltica can be found mating and correlated with fruit and seed characteristics that impose severe ovipositing in the fruits of Euphorbia species in April and May. The constraints on insect oviposition and larvae development. In larvae of this species develop inside the seeds feeding on their another study, Greig (1993) evaluated the impact of pre-dispersal contents. They overwinter inside the seeds and the adults emerge seed predators in a set of Piper species that exhibited alternative in the following spring, when fruits are again available for ovipo- reproductive strategies (partitioning between seed size and seed sition. In Iberia, E. characias and E. welwitschii are the only known number). She recorded the highest levels of insect damage in the hosts of E. jaltica (M. Boieiro, unpubl. data). The hemipterans less fecund species, which were also the ones that produced the C. aterrimus and D. agilis are generalist species that feed upon larger seeds. These species are attractive to a wider array of pred- a variety of plant species from different genera (Stichel, 1955/1962; ators, particularly weevils that can develop on large-sized seeds, Moulet, 1995). These insects are frequently seen on the fruits of but are unable to do so in the small-sized seeds of their congeners. Euphorbia species puncturing the seeds during the fruiting period. This kind of comparison among groups of congeneric co-occurring They inject saliva into the seed where extra-oral digestion takes species is considered a powerful method for studying patterns and place and then suck back the resulting liquids leaving the seed processes in evolutionary ecology. This procedure is now being deprived of its contents. increasingly applied in plant conservation biology since the anal- ysis of the main causes of mortality in pairs of common-rare species 2.2. Study sites may lead to a clearer understanding of the underlying causes of rarity and provide valuable information for the management of The study was carried out from 2002 to 2004 at five sites