Oikos 118: 809Á818, 2009 doi: 10.1111/j.1600-0706.2008.17397.x, # 2009 The Authors. Journal compilation # 2009 Oikos Subject Editor: Frank Van Veen. Accepted 12 December 2008 Competition as a structuring force in leaf miner communities Ayco J. M. Tack, Otso Ovaskainen, Philip J. Harrison and Tomas Roslin A. J. M. Tack ([email protected]), O. Ovaskainen, P. J. Harrison and T. Roslin, Dept of Biological and Environmental Sciences, Div. of Population Biology, PO Box 65 (Viikinkaari 1), FI-00014 University of Helsinki, Finland. The role of competition in structuring communities of herbivorous insects is still debated. Despite this, few studies have simultaneously investigated the strength of various forms of competition and their effect on community composition. In this study, we examine the extent to which different types of competition will affect the presence and abundance of individual leaf miner species in local communities on oak trees Quercus robur. We first use a laboratory experiment to quantify the strength of intra- and interspecific competition. We then conduct a large-scale field experiment to determine whether competition occurring in one year extends to the next. Finally, we use observational field data to examine the extent to which mechanisms of competition uncovered in the two experiments actually reflect into patterns of co- occurrence in nature. In our experiment, we found direct competition at the leaf-level to be stronger among conspecific than among heterospecific individuals. Indirect competition among conspecifics lowered the survival and weight of larvae of T. ekebladella, both at the branch and the tree-level. In contrast, indirect competition among heterospecifics was only detected in one out of three species pairs examined. In the field experiment, the presence of a given moth species in one year affected the relative abundance of leaf miner species in the next year. Nevertheless, patterns of competition observed in these experiments did not translate into repulsion among free-ranging leaf miners: conspecific larvae of four leaf- mining species were aggregated on the same trees, shoots and leaves. In contrast, heterospecific larvae were only aggregated at the tree-level. We propose that despite the fact that leaf miners do compete and that such effects extend through time, the incidence and strength of competition is relatively small at realistic densities. Hence, competition will likely be of minor importance in shaping the distribution of leaf miners in a natural setting. Whether competition is an important structuring force in forms of competition. The larvae themselves will not be communities of folivorous insects has been the subject of able to alleviate competition by dispersing. As a likely hot debate (Hairston et al. 1960, Murdoch 1966, Janzen consequence, several studies have addressed patterns of 1973, Lawton and Strong 1981, Kaplan and Denno 2007). distribution in leaf miners (Bultman and Faeth 1985, Sato For decades, competition was assumed to be unimportant Á 1991, Cornelissen and Stiling 2008), or the strength and largely because insect densities in the field are typically prevalence of individual forms of competition among this much lower than those needed to consume the complete type of insects (Faeth 1992, Fisher et al. 2000). Never- host plant (Hairston et al. 1960, Lawton and Strong 1981, theless, few studies have attempted to relate the inferred Strong et al. 1984). Such a pattern would seem unexpected strength of competition to patterns of co-occurrence in a world governed by fierce competition, in which we realized in nature (but see Bultman and Faeth 1986). would expect herbivores to compete for consuming the very Even less is known about the temporal scales on which last host plant. Hence, direct interference competition will competition acts: whether the effects only extend for a few seem rare (but see Roslin and Roland 2005). Nevertheless, days or whether they also act on individuals in the next the role of intra- and interspecific competition has recently growing season (cf. Karban and Baldwin 1997). been resurrected as a factor to take account of (Denno et al. In this paper, we use leaf miners of the pedunculate oak 1995, Ohgushi 2005, Kaplan and Denno 2007). This Quercus robur as a model system to compare the role of revival has partly been due to an increased focus on a less different modes of competition in structuring herbivorous obvious form of competition. Even in a predominantly communities. We define direct competition as the perfor- green world, indirect competition may be mediated by the mance of a focal individual being lowered by other host plant (Ohgushi 2005, Kaplan and Denno 2007), or by individuals present on the same leaf, and indirect competi- shared natural enemies (Holt 1977, Morris et al. 2005). tion as performance being lowered by individuals present Leaf miners form interesting targets for studies of on other parts of the plant. In this context, we explicitly competition. Due to the sedentary feeding mode of their focus on indirect competition as mediated by the host plant, larval stage, spatial patterns in the behavior of ovipositing and exclude apparent competition through shared natural females will largely determine the potential for different enemies (sensu Holt 1977) by excluding all parasitoids from 809 our experimental treatments. We then use a three-step perspective of these species, the oak forms a taxonomically approach to quantify the importance of such interactions at well defined host. In the landscape of Finland, Q. robur is a different temporal scales: we first use a laboratory experi- relatively rare tree species, hence offering a patchy resource ment to quantify the strength of intra- and interspecific with a distinct spatial structure. In addition, the trees competition. We then conduct a large-scale field experi- themselves are structured into several hierarchical units: ment to determine whether competition occurring in one branches, shoots (i.e. twigs grown from a single bud in the year actually extends to the next. Finally, we use observa- current year) and leaves (see Fig. 1 in Roslin et al. 2006). tional field data on the distribution of four species to Among the more than twenty leaf miner species examine the extent to which mechanisms of competition occurring in southern Finland on Q. robur, three families uncovered in the two experiments actually reflect into are quantitatively dominant in terms of individual abun- patterns of co-occurrence in nature. More specifically, we dances. In the family Tischeriidae, two species (Tischeria ask 1) at what hierarchical levels (trees, branches and/or ekebladella and T. dodonaea) form shallow blotch mines on leaves) we can detect competition; 2) how the strength of the upper surface of the leaves. In the family Gracillariidae, different modes of competition compare to each other; 3) species Phyllonorycter harrisella and P. quercifoliella form whether competitive effects extend across years, as mediated tent-like mines on the lower surface of the leaf. These two by the host plant and 4) to what extent individual modes of congeneric species cannot be reliably distinguished on the competition are reflected in patterns of co-occurrence basis of external leaf-mine morphology, and will therefore among leaf miners in nature. be treated as a compound group in the observational parts of our data. In the family Nepticulidae, species Ectoedemia albifasciella, Stigmella ruficapitella, S. roborella, S. samiatella Material and methods and S. svenssoni form mines of varying morphology on the upper surface of the leaf. Of these, congeneric species of Study system Stigmella cannot be reliably identified, and their larvae are hence treated as a group in observational data. In Finland, Quercus robur is the only representative of a large While mining slightly different parts of the leaf blade, all genus of trees. This species forms the host of a diverse insect the above groups co-occur on leaves during major parts of community. Across Europe, more than 200 species of the summer, and might therefore compete with each other. Lepidoptera alone feed on oak leaves Á a figure higher The univoltine tischeriids occur on mature leaves in the late than for any other European tree species (Southwood 1961). summer, the bivoltine gracillarids occur both on fresh leaves The number of leaf miners is particularly high, most of in early summer and mature leaves in autumn. Of the which are host specific (Hering 1957). Hence, from the nepticulids the species E. albifasciella and S. svenssoni are Figure 1. Treatment types applied in the laboratory experiment: (a) control treatment, in which one moth-pair was introduced on a single branch on the tree; (b) direct intraspecific, in which two pairs of the same moth species were introduced on the same branch, resulting in a higher density of leaf mines; (c) indirect intraspecific, in which two pairs of the same moth species were introduced on different branches on the same tree; (d) direct interspecific, in which two moth pairs of different species were introduced on the same branch; (e) indirect interspecific, in which two moth pairs of different species were introduced on different branches on the same tree. Shown in the bottom- right are the leaf mines of Tischeria ekebladella and of Phyllonorycter spp. 810 univoltine, whereas S. ruficapitella, S. roborella and Competition over different time periods S. samiatella are bivoltine. Tischeriids hibernate as larvae, while gracillarids and nepticulids pupate in autumn. To examine the extent to which effects of competition may extend over time, we conducted a field experiment. Here, we transplanted moths of T. ekebladella onto 50 oak trees Direct versus indirect competition on the island of Wattkast, southwestern Finland (for a map, see Gripenberg and Roslin 2005). We selected naturally To examine the strength of intra- and interspecific growing oak trees varying in height between 1 and 3 m, so competition, we conducted an experiment at the Haapas- that every single leaf could be examined.