SHORT COMMUNICATION Associational Resistance to a Tropical Leaf-Miner: Does Neighbour Identity Matter?

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 are significantly different at P < 0.05. financial support of SLU. We thank Johan Stenberg and two anonymous reviewers for comments on a previous version. is quite surprising given the importance of host plant density on herbivory (Angulo-Sandoval & Aide 2000, Norghauer et al. 2006). Although this result suggests that LITERATURE CITED P. reticulatum does not escape herbivory when associated with other plant species, we did find that more leaves were ANDOW, D. A. 1991. Vegetational diversity and arthropod population attacked (nearly 50% of all leaves) in conspecific stands, response. Annual Review of Entomology 36:561–586. indicating that developing leaves rarely escape attack ANGULO-SANDOVAL, P. & AIDE, T. M. 2000. Effect of plant density and by female leaf-miners when there is an abundance of light availability on leaf damage in Manilkara bidentata (Sapotaceae). conspecifichostplantsandaremorelikelytoescapeattack Journal of Tropical Ecology 16:447–464. in the presence of heterospecific species. This supports ATSATT, P. & O’DOWD, D. 1976. Plant defense guilds. Science 193:24– the indication that associational resistance to specialist 29. herbivores is quite common (Hamback¨ et al. 2000, 2003; BROWN, B. J. & EWEL, J. J. 1987. Herbivory in complex and simple Stenberg et al. 2007, Tahvanainen & Root 1972). tropical successional ecosystems. Ecology 68:108–116. Leaf-miner dispersion provides further evidence for BULTMAN, T. L. & FAETH, S. H. 1986. Leaf size selection by leaf-mining the possibility of associational resistance. Mines are insects on Quercus emoryi (Fagaceae). Oikos 46:311–316. more aggregated when P. reticulatum is associated with DALIN, P. & BJORKMAN,¨ C. 2006. Native insects colonizing introduced heterospecificneighbours,especiallyinthepresenceofthe tree species – patterns and potential risks. Pp. 63–77 in Paine, unrelated A. golfodulcensis. The greater aggregation in the T. D. (ed.). Invasive forest insects, introduced forest trees, and altered A. golfodulcensis habitat is expected to increase density- ecosystems. Springer, the Netherlands. dependent mortality due to competition or predation EBER, S. 2004. Bottom-up density regulation in the holly leaf-miner (Bultman & Faeth 1986, Eber 2004). Phytomyza ilicis. Journal of Animal Ecology 73:948–958. In conclusion, to our knowledge no previous studies EHRLICH, P. R. & RAVEN, P. H. 1964. Butterflies and plants: a study in have investigated associational resistance in tropical coevolution. Evolution 18:586–608. forests. This is somewhat surprising given the high EWEL, J. J. 1999. Natural systems as models for the design of sustainable number of interacting species, the high diversity of systems of land use. Agroforestry Systems 45:1–21. specialist herbivores, and the fact that areas of the FACKNATH, S. 2005. Leaf age and life history variables of a understorey are often dominated by specific plant species. leafminer: the case of Liriomyza trifolii on potato leaves. Entomologia All of these facts suggest that associational resistance may Experimentalis et Applicata 115:79–87. be quite common in understorey tropical communities. GRIFFITHS, M. E., MOHOMMAD, B. A. & VEGA, A. 2007. Dry Our study indicates that associational resistance may season distribution of land crabs, Gecarcinus quadratus (Crustacea: operate in these habitats. We found that heterospecific Gecarcinidae), in Corcovado National Park, Costa Rica. Revista de neighbours, especially unrelated ones, affect the per Biolog´ıa Tropical 55:219–224. cent leaves attacked and patterns of aggregation, but GRIPENBERG, S. & ROSLIN, T. 2008. Neither the devil nor the deep not the density of leaf mines. Since leaf-miners can blue sea: larval mortality factors fail to explain the abundance and have significant effects on plant fitness (Magalhaes˜ et al. distribution of Tischeria ekebladella. Ecological Entomology 33:346– 2008, Wagner et al. 2008) our findings suggest 356. 554 COLIN M. ORIANS AND CHRISTER BJORKMAN¨

◦ HAMBACK,¨ P. A., AGREN, J. & ERICSON, l. 2000. Associational RISCH, S. J., ANDOW, D. & ALTIERI, M. A. 1983. Agroecosystem resistance: insect damage to purple loosestrife reduced in thickets diversity and pest control: data, tentative conclusions and new of sweet gale. Ecology 81:1784–1794. research directions. Environmental Entomology 12:625–629. HAMBACK,¨ P. A., PETTERSSON, J. & ERICSON, L. 2003. Are STENBERG, J. A., HEIJARI, J., HOLOPEINEN, J. K. & ERICSON, L. 2007. associational refuges species specific? Functional Ecology 17: Presence of Lythrum salicaria enhances the bodyguard effects of the 87–93. parasitoidAsecodesmentoforFilipendulaulmaria.Oikos116:482–490. HESPENHEIDE, H. A. 1991. Bionomics of leaf-mining insects. Annual TAHVANAINEN, J. O. & ROOT, R. B. 1972. The influence of vegetational Review of Entomology 36:535–560. diversity on the population ecology of a specialized herbivore, HJALT¨ EN,´ J., DANNELL, K. & LUNDBERG, P. 1993. Herbivore avoidance Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321– by association: vole and hare utilization of woody plants. Oikos 346. 68:125–131. TSVUURA, Z., GRIFFITHS, M. E. & LAWES, M. J. 2007. The effect of KARBAN, R. 2007. Associational resistance for mule’s ears with herbaceous understory cover on fruit removal and seedling survival sagebrush neighbors. Plant Ecology 191:295–303. in coastal dune forest trees in South Africa. Biotropica 39:428–432. LETOURNEAU, D. K. 1986. Associational resistance in squash VANVEEN,F.J.F.,MULLER,¨ C. B., ADRIAANSE, I. C. T. & GODFRAY, monoculture and polyculture in tropical Mexico. Environmental H. C. J. 2002. Spatial heterogeneity in risk of secondary parasitism in Entomology 15:285–292. a natural population of an aphid parasitoid Journal of Animal Ecology LIU, Z. M., MEATS, A. & BEATTIE, G. A. C. 2006. Modification of host 71:463–469. findingandovipositionbehaviourofthecitrusleafminer,Phyllocnistis VEHVILAINEN,¨ H., KORICHEVA, J. & RUOHOMAKI,¨ K. 2007. Tree citrella, by horticultural mineral oil. Entomologia Experimentalis et species diversity influences herbivore abundance and damage: meta- Applicata 121:243–251. analysis of long-term forest experiments. Oecologia 152:287–298. MAGALHAES,˜ S. T. V., GUEDES, R. N. C., LIMA, E. R. & DEMUNER, VERCHER, R., FARIAS, A., MARZAL, C., SOTO, A., TENA, A. & A. J. 2008. Coffee leaf volatiles and egg laying by the coffee leafminer GARCIA-MARÍ,F.2008.Factorsinfluencingadultfemaleoviposition Leucoptera coffeella. Crop Protection 27:1038–1041. in the citrus leafminer Phyllocnistis citrella. Agricultural and Forest NORGHAUER, J. M., MALCOLM, J. R. & ZIMMERMAN, B. L. 2006. Entomology 10:45–51. Juvenile mortality and attacks by a specialist herbivore increase WAGNER, D., DEFOLIART, L., DOAK, P. & SCHNEIDERHEINZE, J. 2008. with conspecific adult basal area of Amazonian Swietenia macrophylla Impact of epidermal leaf mining by the aspen leaf miner (Phyllocnistis (Meliaceae). Journal of Tropical Ecology 22:451–460. populiella) on the growth, physiology, and leaf longevity of quaking ◦ OSTERG¨ ARD, H. & EHRLEN,´ J. 2005. Among population variation in aspen. Oecologia 157:259–267. specialist and generalist seed predation – the importance of host plant WHITE, J. A. & WHITHAM, T. G. 2000. Associational susceptibility of distribution, alternative hosts and environmental variation. Oikos cottonwood to a box elder herbivore. Ecology 81:1795–1803. 111:39–46. WHITHAM, T. G. 1983. Host manipulation of parasites: within-plant RASINGAM, L. & PARTHASARATHY, N. 2009. Diversity of understory variation as a defense against rapidly evolving pests. Pp. 15–41 in plants in undisturbed and disturbed tropical lowland forests of Denno, R. F. & Mcclure, M. S. (eds.). Variable plants and herbivores in Little Andaman Island, India. Biodiversity and Conservation 18:1045– natural and managed systems. Academic Press, New York. 1065. WISE, M. J., YI, C. G. & ABRAHAMSON, W. G. 2009. Associational RICHARDS, P. W. 1996. The tropical rain forest. (Second edition). resistance, gall-fly preferences, and a stem dimorphism in Solidago Cambridge University Press, Cambridge. 600 pp. altissima. Acta Oecologia 35:471–476.