Oecologia (2004) 140: 654–661 DOI 10.1007/s00442-004-1629-9
COMMUNITY ECOLOGY
Marko Rohlfs . Thomas S. Hoffmeister
Spatial aggregation across ephemeral resource patches in insect communities: an adaptive response to natural enemies?
Received: 12 January 2004 / Accepted: 13 May 2004 / Published online: 1 July 2004 # Springer-Verlag 2004
Abstract Although an increase in competition is a common cost associated with intraspecific crowding, spatial aggregation across food-limited resource patches is a widespread phenomenon in many insect communities. Because intraspecific aggregation of competing insect larvae across, e.g. fruits, dung, mushrooms etc., is an important means by which many species can coexist (aggregation model of species coexistence), there is a strong need to explore the mechanisms that contribute to the maintenance of this kind of spatial resource exploitation. In the present study, by using Drosophila-parasitoid interactions as a model system, we tested the hypothesis whether intraspecific aggregation reflects an adaptive response to natural enemies. Most of the studies that have hitherto been carried out on Drosophila-parasitoid interactions used an almost two-dimensional artificial host environment, where host larvae could not escape from parasitoid attacks, and have demonstrated positive densitydependent parasitism risk. To test whether these studies captured the essence of such interactions, we used natural breeding substrates (decaying fruits). In a first step, we analysed the parasitism risk of Drosophila larvae on a three-dimensional substrate in natural fly communities in the field, and found that the risk of parasitism decreased with increasing host larval density (inverse density dependence). In a second step, we analysed the parasitism risk of Drosophila subobscura larvae on three breeding substrate types exposed to the larval parasitoids Asobara tabida and Leptopilina heterotoma. We found direct density-dependent parasitism on decaying sloes, inverse density dependence on plums, and a hump-shaped relationship between fly larval density and parasitism risk on crab apples. On crab apples and plums, fly larvae M. Rohlfs (*) . T. S. Hoffmeister Zoological Institute, Department of Animal Ecology, ChristianAlbrechts-University of Kiel, Am Botanischen Garten 1-9, 24098 Kiel, Germany e-mail:
[email protected] Tel.: +49-431-8804145 Fax: +49-431-8802403
benefited from a density-dependent refuge against the parasitoids. While the proportion of larvae feeding within the fruit tissues increased with larval density, larvae within the fruit tissues were increasingly less likely to become victims of parasitoids than those exposed at the fruit surface. This suggests a facilitating effect of group-feeding larvae on reaching the spatial refuge. We conclude that spatial aggregation in Drosophila communities can at least in part be explained as a predator avoidance strategy, whereby natural enemies act as selective agents maintaining spatial patterns of resource utilisation in their host communities. Keywords Density dependence . Drosophila . Hostparasitoid interaction . Predator avoidance . Top-down selection
Introduction A common cost associated with the gregarious exploitation of food-limited resource patches is an increase in intraspecific competition, and hence a reduction in individual fitness (Begon et al. 1996). Despite these costs, resource exploitation through insects is often characterised by a positive response of individuals to the presence of conspecifics, which raises the general question why is the formation of intraspecific aggregations so widespread in insect communities (Prokopy and Roitberg 2001)? One mechanism by which aggregation may provide a benefit is that individuals at high population densities can experience a diluted risk of attacks from natural enemies (Parrish and Edelstein-Keshet 1999; Stephens et al. 1999; Hunter 2000), or may profit from a density-dependent spatial refuge against predators (see Hawkins 1994; Zwölfer and Arnold-Rinehart 1994). Thus, behaviours leading to spatial aggregation of competitors have been interpreted as predator avoidance strategies (e.g. Krebs and Davies 1996). For host-parasitoid interactions, inverse density-dependent parasitism has frequently (approximately 30% of cases) been found (Lessels 1985;
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Stiling 1987); however, the mechanisms for inverse density dependence remain elusive for most of the cases (Walde and Murdoch 1988). If aggregation provides a selective advantage with respect to the risk of attacks from predators, natural enemies may have contributed to the evolution of spatial resource exploitation of the species affected. With this in mind, it is necessary to ask the question is intraspecific aggregation of competing insect larvae (a result of aggregated egg-laying behaviour) across ephemeral resource patches (e.g. fruits, mushrooms, dung, etc.) an adaptive response to their natural enemies (see also Hoffmeister and Rohlfs 2001; Wertheim 2001)? Given the fact that intraspecific aggregation is the key mechanism promoting high local species diversity in many insect communities (aggregation model of species coexistence, e.g. Shorrocks et al. 1984; Shorrocks and Sevenster 1995; Hartley and Shorrocks 2002), natural enemies might act as selective agents maintaining spatial patterns of resource utilisation, which in turn facilitate species coexistence in the prey communities. Drosophila communities are a prime example of intraspecific aggregation across fragmented resources (Atkinson and Shorrocks 1984), and its effect on the condition for local species coexistence has been demonstrated in detail (Sevenster and van Alphen 1996; Toda et al. 1999; Wertheim et al. 2000; Krijger and Sevenster 2001). Parasitoid wasps attacking the larval stages of these insects are important natural enemies in such ecological communities (Carton et al. 1986). Recent studies have demonstrated that parasitoids are able to acquire information from the host environment, which allows them to allocate foraging time to the availability of hosts in a patch (e.g. van Lenteren and Bakker 1978; Galis and van Alphen 1981; van Alphen and Galis 1983; Wertheim 2001; van Alphen et al. 2003). This plastic response of parasitoids to host densities accounted for a functional response of the wasps that led to positive density-dependent parasitism risk rather than a diluted risk of parasitism, and thus cannot explain the aggregation of hosts (Wertheim 2001). While the dilution of parasitism risk can be precluded as a
driving force for larval aggregations, spatial refuges have not yet been tested as an adaptive reason for aggregation, since most of these studies were carried out on an almost two-dimensional artificial host environment (thin layer of yeast suspension on Petri dishes) that does not allow the fly larvae to escape from parasitoid attacks. Thus, an important question is whether these studies capture the essence of such host-parasitoid interactions? We expect that this might not be the case, because drosophilids use an array of different and often three-dimensional breeding substrates (Shorrocks 1982). Unlike the situation in most laboratory studies, direct density-dependent parasitism may not be a persistent pattern when considering the variety of host habitats. For example, larval aggregation on natural breeding substrates might lead to density-dependent refuges for Drosophila larvae if they can escape from parasitism by feeding in regions of a substrate patch that a female parasitoid is unable to reach with her ovipositor (Zwölfer and Arnold-Rinehart 1994, for gall-forming insects). If such a spatial refuge expands with increasing density when host larvae feed gregariously in single patches, this would lead to inverse density-dependent parasitism at the patch scale (Zwölfer and Arnold-Rinehart 1994). To explore the risk of parasitism of single fly larvae within host aggregations the critical experiment is an analysis of the individual behaviour of the parasitoids that, together with host habitat variability, is the major determinant of such parasitism risk (Bernstein 2000; Casas 2000; Vet 2001). The present study compares the outcome of densitydependent Drosophila-parasitoid interactions on various fly larval feeding substrates. First, we start with a field survey aimed at assessing density-dependent parasitism in natural and clearly three-dimensional substrates of fruitbreeding Drosophila communities. Second, we tested Drosophila subobscura (Collin) (Diptera, Drosophilidae) at several larval densities on three different decaying fruit types and analysed individual patch time allocation and parasitisation success of her most important parasitoids Asobara tabida (Nees) (Hymenoptera, Braconidae) and Leptopilina heterotoma (Thomson) (Hymenoptera, Figiti-
Table 1 Density dependence of the proportion of emerged parasitoids as a function of host number. Results are shown from general linear models (GLM) analyses, with total number of hosts (Nt) as the explanatory variable for Np/Nt, where Nf=the number of emerged drosophilid flies, Np=the number of parasitoids (Asobara sp. and Leptopilina sp.) and Nt=Nf+Np. To each data set, we fitted a
model of the form Np/Nt=β0+β1ln(Nt+1), where β0 is a constant, and β1 estimates the linear component of the density-dependent parasitism. The sign of the estimator β1 as derived from the GLM depicts the type of density dependence [positive (+), negative (−)]. GFK Großkönigsförde, KIEL Kiel
Sample
KIEL01a KIEL02b KIEL03b KIEL04a GKF01a GKF02a GKF03a
Mean parasitism rate±SD
0.11±0.21 0.17±0.23 0.13±0.25 0.31±0.29 0.06±0.15 0.03±0.11 0.18±0.24
Complete record
Reduced record
F-statistic
P
β1
F-statistic
P
β1
F1,57=1.57 F1,88=3.32 F1,83=5.27 F1,59=0.54 F1,124=1.97 F1,161=0.84 F1,46=1.23
0.2153 0.0718 0.0242 0.4653 0.1629 0.3608 0.2732
−0.4777 +0.3917 −0.6340 −0.2030 +0.2370 −0.2163 −0.3031
F1,20=26.93 F1,45=6.63 F1,40=21.16 F1,42=2.27 F1,27=6.01 F1,16=18.82 F1,28=8.48
0 indicated a higher rate of parasitism in fly larvae from the surface fraction, and values
