Sociobiology 60(3): 242-251 (2013) DOI: 10.13102/Sociobiology.V60i3.242-251
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Portal de Periódicos Eletrônicos da Universidade Estadual de Feira de Santana (UEFS) Sociobiology 60(3): 242-251 (2013) DOI: 10.13102/sociobiology.v60i3.242-251 Sociobiology An international journal on social insects research ArticlE - ANtS Protection Mutualisms and the Community: Geographic Variation in an Ant-Plant Symbiosis and the Consequences for Herbivores EG Pringle1, DM Gordon2 1 - University of Michigan, Ann Arbor, Michigan, USA. 2 - Stanford University, Stanford, California, USA. Article History Abstract Edited by Protection mutualisms mediate trophic interactions in many systems, but their effects Kleber Del-Claro, UFU, Brazil on the surrounding community are rarely studied. Ant-plant symbioses are classic received 02 July 2013 Initial acceptance 31 July 2013 examples of protection mutualisms: myrmecophytic plants provide nesting space and Final acceptance 12 August 2013 food for symbiotic ants in exchange for ant defense. Ant defense should thus reduce the abundance of herbivores, but studies of ant-plant symbioses usually measure damage Key words to the plant without quantifying the herbivores themselves. In this study, we investiga- Ant-plant mutualism, Azteca, context ted whether geographic variation in the quality of ant defense in a symbiotic mutualism dependence, Cordia alliodora, Cordia alliodora Azteca seasonally dry tropical forest, between trees and ants was associated with the abundance trophic cascades and species richness of plant herbivore communities. In three tropical-dry-forest sites in Middle America, we found that the density of Azteca ants within trees was negatively Corresponding author associated with the levels of leaf herbivory. At sites where ants were effective tree Elizabeth G. Pringle defenders, tree herbivores were less abundant and herbivore assemblages on trees exhibi- University of Michigan ted lower species richness than at a site where ants were poor defenders. In addition, 830 N University St Ann Arbor, MI 48103, USA in a site where ants reduced herbivory, herbivore communities were less abundant and E-Mail: [email protected] diverse in the presence of ants than in their absence, where as in a site where ants did not reduce herbivory, there were no differences in herbivore abundance or richness between trees with or without ants. We conclude that geographic variation in the quality of ant defense drives variation in myrmecophytic-plant herbivore communities. Moreover, ant-plant protection mutualisms should have important but rarely considered effects on herbivore population dynamics and food-plant specialization. Introduction or unimportant, when in fact the studies so far suggest that protection tends to have strong effects on local diversity Mutualistic interactions between species can strongly and abundance. Interestingly, it has been suggested that the affect the structure of ecological communities (Stachowicz, overall effect of protection is to reduce local species 2001; Bruno et al. 2003; Hay et al., 2004). For example, animal diversity (Rudgers and Clay, 2008; Rudgers et al., 2010; seed dispersal can determine the composition of tropical-tree but see Jani et al., 2010), which contrasts with other well- communities (Terborgh et al., 2008), and pollinator preferen- known mutualisms that clearly enhance local diversity (e.g., ces can favor the spread of certain plant species (Chittka and fig trees, corals) (Terborgh, 1986; Stachowicz, 2001; Hay et Schürkens, 2001). Protection mutualisms, in which a mutua- al., 2004). Such community consequences have been so little list defends its partner against natural enemies, are frequently studied, however, that we do not know how general such local shown to affect the growth and fitness of individual orga- effects may be, or how these mutualisms affect systems on nisms, but very little is known about how these interactions larger spatial and temporal scales. structure the communities in which they are embedded. The In terrestrial communities, ant protection frequently paucity of such studies may give the false impression that determines the strength of trophic cascades (sensu Hunter the community effects of protection mutualisms are rare and Price, 1992). Ants both decrease herbivory as mutualists Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology ISSN: 0361-6525 Sociobiology 60(3): 242-251 (2013) 243 of plants by predating and harassing herbivores (Hölldobler abundances of the herbivores that eat the plant. Yet although and Wilson, 1990) and increase herbivory as mutualists of ants' capacity to reduce herbivory and increase plant fitness in honeydew-producing Hemiptera by protecting them from such systems is well documented (Chamberlain and Holland, other predators (Way, 1963; Del-Claro and Oliveira, 2000). 2009; Rosumek et al., 2009), and some studies have contras- In both mutualistic roles, ant protection can reduce the di- ted the effects on plants of different herbivore species (e.g., versity and abundance of other arthropods in a system, but Frederickson 2005; Palmer and Brody, 2013), very few stu- the strength of these effects varies among taxa and depends dies have investigated the community of herbivores associa- on environmental context (Fowler and Macgarvin, 1985; ted with a given myrmecophyte (but see, e.g., Janzen, 1967; Wimp and Whitham, 2001; Kaplan and Eubanks, 2005; Oli- Gaume et al., 1997; Itino and Itioka, 2001). This lacuna pro- veira and Del-Claro, 2005; Mooney, 2007; Rudgers et al., bably results in part from the difficulty of identifying insect 2010). Indeed, although ant-plant interactions tend to have larval forms, which often inflict most of the leaf damage in positive effects on individual plants (Styrsky and Eubanks, the diverse tropical forests where myrmecophytes are com- 2007; Chamberlain and Holland, 2009), which suggests that mon (Davidson and McKey, 1993). Surmounting this diffi- ants should reduce the abundance, if not also the diversity, of culty will be essential for understanding the community role untended herbivores on those plants, these effects are often played by these classic study systems. non-significant at both plant- and experimental-plot-scales The myrmecophytic tree Cordia alliodora (Ruiz & (Kaplan and Eubanks, 2005; Mooney, 2007; Rudgers et al., Pavón) Oken (Boraginaceae) hosts colonies of Azteca ants 2010). This is inconsistent with the evidence that ants reduce (Hymenoptera: Formicidae: Dolichoderinae) in Neotropical herbivory levels (Chamberlain and Holland, 2009; Styrsky, forests. Ants nest in hollow swellings, known as domatia, 2007) unless most herbivores collectively consume very little at stem nodes, and tend honeydew-producing scale insects and ants defend only against the few herbivores that inflict the (Hemiptera: Coccidae and Pseudococcidae) that feed on most damage. Whether or not such conditions are generally plant phloem from inside the domatia. Azteca ants can re- true, they raise interesting and mostly unanswered questions duce folivory on C. alliodora (Tillberg, 2004; Trager and about the relative abundances of herbivore species in these Bruna, 2006; Pringle et al., 2011), but the magnitude of these systems, and about the relative specialization of those species effects depends on the size of the ant colony, the size of the on ant-defended food plants. tree, and geographic location (Pringle et al., 2011; Pringle The strength of any given ant-plant interaction is et al., 2012a). There have been few studies of C. alliodora geographically variable. The identities and abundances of herbivores, but many of the lepidopteran larvae that eat the ants, herbivores, and even other predators vary over space tree's leaves in Middle America can be identified by compari- and affect how much ants benefit plants (Bronstein, 1994; son with a database of caterpillars and their food plants from Rudgers and Strauss, 2004; Mooney, 2007; Rosumek et al., northwestern Costa Rica (Janzen and Hallwachs, 2009). 2009). Geographic variation in the effectiveness of ant de- In this study, we investigated geographic variation in fense will also affect food availability for herbivores of a C. alliodora herbivore communities.We investigated varia- given plant, with potential cascading effects on herbivore tion in the density of ants within and among C. alliodora population sizes and even food-plant specialization (i.e., in a trees and in the effectiveness of ant defense in three sites geographic mosaic of coevolution, sensu Thompson, 2005). in Middle America. By conducting surveys of the herbivore In one of the few studies to examine the community assemblages on individual trees, we asked whether the abun- effects of a geographically variable ant-plant interaction, Rud- dance and species richness of known C. alliodora herbivores gers et al., (2010) reported that, in three Arizona populations were negatively associated with the density of ants and the of wild cotton, there was a positive relationship between how effectiveness of ant defense at a site. We then asked whether much ant presence within a site increased plant fitness and trees occupied by Azteca ants supported lower abundance and influenced arthropod community composition. Geographic richness of known herbivores than unoccupied trees within variation in the effects of ants in that system resulted from each of two sites that differed in the typical effectiveness of ant differences in total ant abundance and the relative abundance