Insect herbivores are trapped between the low food quality of their host plants and the impact of their natural enemies (Lawton & McNeill 1979). The chemical composition of plants makes them poor food for herbivores: typically they are low in nitrogen but high in lignin and cellulose, and contain secondary metabolites that act as toxins, repellents and digestibility reducers (Hartley & Jones 1997). Meanwhile, predators, parasites and disease reduce herbivore abundance (Hairston, Smith & Slobodkin 1960). How plant quality and natural enemies interact to limit insect herbivore populations, that is the relative contributions of so-called top-down vs. bottom-up regulatory factors, is a contentious issue (Hunter & Price 1992; Gange & Brown 1997). Experimental tests of the relative strengths of top-down and bottom-up forces remain relatively rare in terrestrial systems (Walker & Jones 2001). Furthermore, most efforts to quantify these two factors measure herbivore abundances only over relatively local scales. This may be highly misleading, given that although most insect herbivores have relatively small geographical ranges compared to the more widespread species (Gaston 2003), in absolute terms many have moderate to large ranges, over which substantial variation in both plant quality and pressure from natural enemies can be expected. The levels of many plant secondary compounds are altered markedly by abiotic environmental factors such as soil type, light, temperature, ultraviolet radiation, ozone and rainfall, as well as being affected by plant growth rate (Herms & Mattson 1992; Jones & Hartley 1999). Thus, it seems highly likely that the quality of a particular food plant for a given species of insect herbivore will differ, perhaps substantially, between, for instance, widely separated parts of its geographical range. Similarly, the species and abundance composition of the assemblages of natural enemies that attack a particular species of insect herbivore changes in space, often also in part as a consequence of environmental factors, which may result in geographical variation in the mortality pressure that they exert (e.g. Schönrogge, Walker & Crawley 1998, 2000; Brewer & Gaston 2003; Gaston 2003).
Spatial variation in the food quality of host plants, in natural enemy pressure and in the interaction between the two seem likely to shape the spatial abundance structure of insect herbivores throughout their geographical ranges. Indeed, such variation probably contributes to the constraints on herbivore range limits, which almost invariably means that even host-specialists may only occupy a small proportion of the geographical ranges of their food plants (e.g. Strong, Lawton & Southwood 1984; Quinn, Gaston & Roy 1997, 1998; Cowley et al. 1999; Ungerer, Ayres & Lombardero 1999; for a review see Gaston 2003).
Exploring issues of geographical range structure and its determinants is complicated for most species by many practical considerations, including issues of the spatial extent of sampling required, and the difficulties of measuring resource use, abundances and vital rates. One study system that has proved to be of immense value in examining spatial variation in population processes for a herbivore, at a spectrum of spatial scales, is that of European (or English) holly Ilex aquifolium L. (Aquifoliaceae), the host-specialist holly leaf-miner Phytomyza ilicis Curtis (Diptera, Agromyzidae) and the suite of natural enemies that attack the leaf-miner (Heads & Lawton 1983; Valladares & Lawton 1991; McGeoch & Gaston 2000; Metcalfe, Marçal & Gaston 2000; Eber et al. 2001; Brewer & Gaston 2002, 2003; Klok, Chown & Gaston 2003). In this study, we used this system to test three hypotheses: (i) host-plant quality exhibits systematic patterns of spatial variation across its geographical range; (ii) the distribution and abundance of an insect herbivore is affected by this variation in plant quality; and (iii) the effects of top-down (bird and parasitism attack rates) and bottom-up factors (host-plant quality) on insect herbivore abundance and performance alter across the host plant's geographical range.
the study system
Holly is a relatively small, dioecious, evergreen tree. It has distinctive, dark green, glossy leaves that are usually spiny with a thick cuticle. Its natural range extends throughout northwestern, central and southern Europe (Peterken & Lloyd 1967; Hultén & Fries 1986). It can also be found less commonly in scattered localities in parts of North Africa and has been reported as having a narrow band of distribution extending into Asia Minor, although there is some doubt as to whether the latter is indeed so.
The holly leaf-miner is the most common insect herbivore of European holly. It is strictly monophagous, so its geographical range is ultimately limited by the availability of holly trees. The life histories of P. ilicis and its natural enemies have been described in detail by Cameron (1939), Lewis & Taylor (1967) and Ellis (2000). Put briefly, the holly leaf-miner exhibits a univoltine life cycle. In Britain, eggs are laid in June on new holly leaves (the tree has just one flush of new leaves per year) into the base of the underside of the midrib. When laying an egg, the adult female P. ilicis leaves a characteristic leaf scar due to the insertion of her ovipositor. The presence of these scars means that oviposition density for a local population may easily be censused. The vast majority of the life history of each individual is spent inhabiting a single holly leaf. After hatching, the larvae eat through the midrib and enter the outer parenchyma of the leaf lamina during the autumn, causing a blister-type mine. They feed throughout the following winter months and pupate in the mine in March, emerging from the leaf as adults in late May or June. The short life span of the adults and the tight synchronization between their emergence and the flush of new leaves severely restricts the possible influence of long-distance immigration and emigration on local population dynamics.
During the period spent within holly leaves, a leaf-miner population may be subject to a number of potential mortalities that are largely sequential, albeit with some overlap. They have been relatively well documented (Cameron 1939; Lewis & Taylor 1967; Heads & Lawton 1983) and include miscellaneous larval deaths, larval parasitism by the parasitoid Chrysocharis gemma Walker (Hymenoptera: Eulophidae), bird predation, pupal parasitism by at least eight species of hymenopteran parasitoids and miscellaneous pupal mortality. These causes of mortality can be identified by dissection of the mine at the end of the life cycle of the leaf-miner. In addition, larvae that successfully complete their development and emerge as adult flies can also be identified from the characteristic emergence holes on the leaf surface. Therefore, the holly leaf-miner has a life cycle that is more suitable than most for measuring a number of components of the basic demographic rates of a local population. The level of oviposition, a number of components of mortality and the rate of successful emergence for a local population in any one year can all be assessed by rapid censusing techniques and dissection of a representative sample of leaves from the holly trees at a site.
Previous studies of this system have shown that the holly leaf-miner (i) occurs predominantly in the more northerly parts of the geographical range of its host plant, where it tends to be ubiquitous; (ii) has an asymmetrical abundance structure to its geographical range, with high to moderate local densities predominantly running in a band across Europe from southwest to northeast, and declining away from this region; and (iii) experiences individual top-down mortality components that are largely independent of one another, and often exhibit different spatial patterns (Brewer & Gaston 2002, 2003). However, variation in bottom-up factors such as host-plant quality, and its interaction with top-down factors, has not been quantified previously. Here we assess spatial variation in both top-down and bottom-up factors across the range of this herbivore, reporting the findings of a new field study.