An aggregation pheromone is a substance, emitted by an individual, that induces aggregative behaviour in conspecifics (Shorey, 1973). These pheromones have evolved several times in insects (Wertheim, 2001), which implies that under certain circumstances selection can favour individuals that seek out conspecifics. Although a number of advantages is apparent for individuals in large groups (see for example Pulliam & Caraco, 1984; Parrish & Edelstein-Keshet, 1999), the evolution of aggregative behaviour requires that even at low densities, advantages outweigh all associated costs. Such a situation could arise when survival or reproduction is hampered at low population densities, i.e. with an Allee effect.
The Allee effect was named after W. C. Allee, for his prominent role in construing adaptive value to grouping behaviour in animals (Allee et al., 1949; Courchamp et al., 1999). Recently, Stephens et al. (1999) provided a clear definition for the Allee effect: ‘A positive relationship between any component of individual fitness and either numbers or density of conspecifics’. This definition emphasises that the Allee effect is based on an advantage to the individual, and it accepts a wide range of mechanisms to achieve such benefits (for examples, see Courchamp et al., 1999; Stephens & Sutherland, 1999). Additionally, a distinction was made between component Allee effects, manifesting positive density dependence on a component of fitness, and demographic Allee effects, concerning total fitness. The latter mostly depict the hump-shaped relationship that is commonly associated with Allee effects, where at some densities the positive density dependence dominates, but at other densities costs outweigh the benefits. The component Allee effect reflects only the isolated mechanism that yields a benefit to aggregation, which might or might not be sufficient to compensate for the connected costs.
If it is expected for a specific species, that the evolution of an aggregation pheromone was driven by positive density dependence at low densities, a component Allee effect can be sought. In controlled experiments, the fitness consequences of isolated mechanisms can be measured, and may provide insight into the selective force that has promoted the use of aggregation pheromone.
The fruit fly Drosophila melanogaster Meigen uses an aggregation pheromone that is emitted by males and mated females (Bartelt et al., 1985; Wertheim, 2001). In a previous field study, potential costs and benefits to the use of an aggregation pheromone in this fly species were identified (Wertheim, 2001). The adult flies aggregate, feed, and breed on decaying fruits (Spieth, 1974). The pheromone induces aggregated oviposition in females (Wertheim, 2001). Consequently, the larvae also have an aggregated distribution across resource substrates. The larvae of D. melanogaster feed on yeasts that develop on a substrate (Brito Da Cunha et al., 1951; Cooper, 1959; Begon, 1986), but at low larval densities, fungi and moulds can overtake a substrate instead (Ashburner, 1989). In laboratory cultures on artificial substrates, larvae suffer high mortality at low larval density (Sang, 1956; Ashburner, 1989).
The aim of the work presented here was to identify a component Allee effect in resource exploitation by D. melanogaster larvae, which might explain the evolution of the use of aggregation pheromone in this species. It is hypothesised that an Allee effect in D. melanogaster larvae can arise from an increased efficiency of a group of larvae to temper fungal growth; however a recent study with larvae of D. subobscura feeding at a natural resource (rowan berries) showed no indication of any facilitation when feeding in groups (Hoffmeister & Rohlfs, 2001). It is possible that the type of substrate on which the larvae develop determines the need for aggregated distributions. In any case, larval density by itself might be insufficient to yield a benefit regarding resource exploitation. In fact, it is likely that adults contribute to the quality of the larval substrates, because a number of Drosophila species is known to inoculate substrates with different species of yeast (Gilbert, 1980; Fogleman & Foster, 1989; Morais et al., 1995).
To test for an Allee effect by larval densities, and a potential added role for adult flies, standard substrates were infested manually with specified numbers of larvae, or standard substrates were infested through oviposition by adult flies. The standard substrates consisted of mashed apple, which constitutes a fairly benign resource for larval development, or apple chunks, which are both more natural and more demanding for larvae to exploit (B. Wertheim, pers. obs.). The observations during the first experiment inspired a more thorough procedure for a second experiment. Before infesting the standard substrates manually with specified numbers of larvae, each standard substrate received a preliminary treatment, consisting of incubation with a specified number of adult flies of specified sex, or the addition of the synthetic aggregation pheromone or its solvent. The fungal growth on the substrates was recorded throughout the larval development. The survival, developmental time, and thorax length of the emerging flies were compared across larval densities and preliminary treatments.