Journal of Tropical Ecology (2009) 25:551–554. Copyright © 2009 Cambridge University Press doi:10.1017/S0266467409990071 Printed in the United Kingdom SHORT COMMUNICATION Associational resistance to a tropical leaf-miner: does neighbour identity matter? Colin M. Orians∗,†,1 and Christer Bjorkman¨ † ∗ Department of Biology, Tufts University, Medford MA 02155, USA † Department of Ecology, Swedish University of Agricultural Sciences, SE-750 07 Uppsala, Sweden (Accepted 26 May 2009) Key Words: Acanthaceae, associational resistance, Corcovado National Park, enemy escape, insect density, insect dispersion, Piperaceae Associational resistance occurs when host plants long-distance attraction of specialist herbivores. The experience reduced attack when in the presence of other fact that host shifts by specialist herbivores are most plant species (Atsatt & O’Dowd 1976, Tahvanainen & common when congeneric species are present (Dalin Root 1972). The issue is most studied in agriculture and &Bjorkman¨ 2006) provides evidence that congeneric forestry because of the potential benefits to pest control species do attract specialists. Once in the habitat, the (Andow 1991, Brown & Ewel 1987, Tahvanainen & Root herbivore could use species-specific cues to locate their 1972), but recent research indicates that associational host plants. If neighbours are unrelated, however, visual resistance may be relatively common in natural systems and volatile cues may be absent or sufficiently low to as well (Hjalt¨ en´ et al. 1993, Karban 2007, Vehvilainen¨ limitlong-distanceattraction.Toexaminetheimportance et al. 2007, Wise et al. 2009; but see Osterg¨ ard˚ & of neighbour identity, we quantified the abundance and Ehrlen´ 2005, White & Whitham 2000), especially distribution of a specialist gracillariid leaf-miner when against specialist herbivores (Hamback¨ et al. 2000, 2003; their host plant, Piper reticulatum L, was imbedded in Stenberg et al. 2007). habitats dominated by conspecifics, by congenerics or by Although pest pressures are generally much higher in unrelated neighbours. the tropics (Ewel 1999), the importance of associational The sedentary nature of leaf-miners makes them ideal resistance in tropical systems is less clear. There are for the study of associational resistance. Larvae develop in examples of associational resistance from agricultural the leaf on which the adult females lay their eggs. Even if systems (Brown & Ewel 1987, Letourneau 1986, Risch larvae are parasitized or removed by predators, the mines et al. 1983), but its importance in natural tropical systems can still be counted. Historically, tests of associational remains unexplored. While host plant density is often resistance have focused on the effects of neighbours positively correlated with rates of herbivory in the tropics on herbivore density. We suggest that, for sedentary (Angulo-Sandoval & Aide 2000, Norghauer et al. 2006), species such as leaf-miners and galling insects, patterns of itisunknownwhetherspecificneighboursmightalterthis aggregation may also be important because of density- pattern. Here we examined the effect of neighbour identity dependent mortality (Vercher et al. 2008, Whitham on associational resistance. Moreover, because closely 1983). In leaf-miners, for example, both intraspecific related neighbours are chemically and morphologically competition (even cannibalism) and predation contribute more similar (Ehrlich & Raven 1964), we determined to density-dependent mortality (Bultman & Faeth 1986, whetherpatternsofassociationalresistancemightdepend Eber 2004, van Veen et al. 2002). Neighbour identity on the relatedness of neighbours. We expected that the is likely to affect patterns of aggregation, especially presence of congeneric plant species would facilitate of short-lived herbivores. If neighbours interfere with host location, short-lived females may be forced to oviposit several eggs on the same leaf or to oviposit 1 Corresponding author. Email: [email protected] on leaves already attacked by other mothers. Even 552 COLIN M. ORIANS AND CHRISTER BJORKMAN¨ under ideal conditions, leaf-miners are relatively short- lived (Facknath 2005, Hespenheide 1991). In addition, neighbours might further increase aggregation if few leaves are suitable in the habitat. In many leaf-miner systems this is the case (Liu et al. 2006, David Wagner pers. comm.). While it can be difficult to isolate the role that neighbours play in associational resistance in the most diverse forests of the tropics, the understorey of undisturbed forests are often dominated by a few species (Griffiths et al. 2007, Rasingam & Parthasarathy Piper Piper Aphelandra 2009, Richards 1996, Tsvuura et al. 2007). Species reticulatum hispidum golfodulcensis within Acanthaceae and Asteraceae, for example, are well known to dominate many tropical and subtropical understorey plant communities (Rasingam & Parthasarathy 2009, Richards 1996, Tsvuura et al. 2007). The tropical wet rain forest at Sirena Biological Station in the Pacific lowlands of Costa Rica (8◦30N83◦30W, Corcovado National Park, Osa Peninsula) is well suited for a study of associational resistance. While the tree species composition of the canopy is diverse, areas of the understorey community are often dominated by specificplantspecies:Aechmeamagdalenae(Bromeliaceae), Piper Piper Aphelandra Aphelandra golfodulcensis (Acanthaceae), several species reticulatum hispidum golfodulcensis of Piper (Piperaceae) and various understorey palms (Arecaceae) (Griffiths et al. 2007, pers. obs.). Our focal Figure 1. Effects of habitat type (neighbour identity) on the abundance species, Piper reticulatum, is a common understorey shrub of a gracillariid leaf-miner of Piper reticulatum; density (a) and per cent in Costa Rica and Panama and can be found in dense leaves with mines (b). Values are mean plus 1 SD. Bars with different stands with 50+ individuals, or may be interspersed letters are significantly different at P < 0.05. with other species, such as Piper hispidum Swartz and Aphelandra golfodulcensis McDade, that also form dense of mines/total number of leaves) or as proportion of leaves stands of 50+ individuals. Of the three plant species, only with mines (number of leaves with mines/total number Piper reticulatum is attacked by the specialist gracillariid of leaves). Differences in distribution were calculated leaf-miner.Thisprovidesauniqueopportunitytoexamine using a standard index of aggregation (variance/density). whether neighbour identity might alter the distribution High values indicate greater aggregation (contagious and abundance of a specialist herbivore. distribution). A one-way ANOVA was used to test for We expected that in a patch of conspecifics, high host significance of habitat type on leaf-miner density and density should increase the number of ovipositing females aggregation. Significance of differences among habitat and lead to high mine densities and high dispersion types was determined using Fisher’s LSD. (low aggregation) because of the abundance of suitable Mine density did not differ among habitats (F2,32 = 1.5, leaves. In contrast, we predicted that in the presence of P=0.24,Figure1a)withameandensityofapproximately heterospecifics, especially unrelated neighbours, densities 0.8 mines per leaf for all treatments. The proportion of will be lower and herbivores will be more aggregated. leaves with mines did, however, differ among habitats and To test these ideas, the abundance and distribution of was greater in the P. reticulatum habitat (F2,32 = 4.6, P = leaf-miners were quantified on P. reticulatum sampled 0.02, Figure 1b). Nearly 50% of the leaves had mines in from habitats dominated by conspecific P. reticulatum the P. reticulatum habitat as compared to 35% in the other (n = 15 individuals), congeneric P. hispidum (n = 10 habitat types. Dispersion was significantly influenced by individuals) or the unrelated A. golfodulcensis (n = 10 neighbour identity. The index of aggregation was highest individuals). All plants, non-reproductive and 1–2 m tall, in the A. golfodulcensis habitat, intermediate in the P. were at least 30 m from other sampled individuals. To hispidum habitat and lowest in the P. reticulatum habitat determine the abundance and distribution of leaf-miners, (F2,32 = 4.85, P = 0.01, Figure 2). we examined every leaf and counted the number of mines Although densities were slightly higher in the P. on each leaf on each P. reticulatum individual. Mine reticulatum habitat, there was no significant difference abundance was calculated as mine density (total number in density of leaf mines among the habitats. This result Associational resistance to a tropical leaf-miner 553 that if predation and parasitism pressures are higher in aggregated populations, it could lead to higher plant performance in heterospecific stands. Given the importance of aggregation in tritrophic interactions (Gripenberg & Roslin 2008, Whitham 1983), these results suggest that future work should examine if and how herbivore dispersion contributes to associational resistance in this and other systems. Piper Piper Aphelandra reticulatum hispidum golfodulcensis ACKNOWLEDGEMENTS Without the help of Andres Vega this research could Figure 2. Effects of habitat type (neighbour identity) on the extent of not have been completed. CMO thanks SLU for support aggregation of a gracillariid leaf-miner of Piper reticulatum. High values indicate greater aggregation. Values are mean plus 1 SD. Bars with during his sabbatical and both authors are grateful for the different letters