Fluctuations in density of an outbreak species drive diversity cascades in food webs

Abstract

Patterns in food-web structure have frequently been examined in static food webs, but few studies have attempted to delineate patterns that materialize in food webs under nonequilibrium conditions. Here, using one of nature's classical nonequilibrium systems as the food-web database, we test the major assumptions of recent advances in food-web theory. We show that a complex web of interactions between insect herbivores and their natural enemies displays significant architectural flexibility over a large fluctuation in the natural abundance of the major herbivore, the spruce budworm (Choristoneura fumiferana). Importantly, this flexibility operates precisely in the manner predicted by recent foraging-based food-web theories: higher-order mobile generalists respond rapidly in time and space by converging on areas of increasing prey abundance. This "birdfeeder effect" operates such that increasing budworm densities correspond to a cascade of increasing diversity and food-web complexity. Thus, by integrating foraging theory with food-web ecology and analyzing a long-term, natural data set coupled with manipulative field experiments, we are able to show that food-web structure varies in a predictable manner. Furthermore, both recent food-web theory and longstanding foraging theory suggest that this very same food-web flexibility ought to be a potent stabilizing mechanism. Interestingly, we find that this food-web flexibility tends to be greater in heterogeneous than in homogeneous forest plots. Because our results provide a plausible mechanism for boreal forest effects on populations of forest insect pests, they have implications for forest and pest management practices.

Fig. 1.

Structure of the balsam fir source food web. (A) Total food web from all samples collected throughout entire study in all plot-years (1983–1993) and in all field experiments. (B) Food web occurring at the peak budworm density using weekly samples in all plots, showing the presence of several hyperparasitoid species (data from Plot 1, 1985; Plot 2, 1986; Plot 3, 1991; see SI Fig. 6). (C) Food web occurring at a lower declining density using weekly samples in all plots, showing a much smaller assemblage of hyperparasitoids than in B, but a larger assemblage of primary parasitoids attacking non-budworm herbivores (data from Plot 1, 1989; Plot 2, 1989; Plot 3, 1993; see SI Fig. 6). Primary parasitoids are represented by squares, secondary parasitoids are represented by ovals, tertiary parasitoids are represented by octagons, and entomopathogens are represented by circles connected by red lines to hosts. The brackets and numbers on the far left identify trophic level. For clarity, those primary parasitoids (third trophic level) attacking budworm and other herbivore species are placed above the herbivore species, whereas those attacking only the non-budworm herbivore species are placed below the herbivore species. Omnivore species occur in more than one trophic level and are represented by a solid color (not white). [Identification codes are shown in SI Table 3. Primary parasitoids attacking unidentifiable herbivores (numbers 67–75) are not shown.]

Fig. 2.

Food-web diversity and budworm density. A–D are based on untransformed data, and A′–D′ are based on transformed data. Similar results were obtained by both methods. (A) Number of primary parasitoids attacking only budworm increases significantly with increasing budworm density. (B) Number of primary parasitoids attacking one or more non-budworm herbivores decreases significantly with increasing budworm density. (C) Total number of primary parasitoids attacking all herbivores does not change in response to increasing budworm density. (D) Total number of secondary and tertiary parasitoids increases significantly with increasing budworm density. Results in D′ are not significant. This is mainly because of an “outlier” (indicated by arrow) caused by a sharp increase in budworm (second-instar budworm) density in Plot 2 in 1990 (see SI Fig. 6). This increase was caused by an invasion of budworm adults (moths) into the plot in 1989 from an other location(s). These invading moths laid eggs, thereby augmenting the local egg populations, resulting in a much greater number of budworm (second-instar budworm) in the following spring (1990) than normally would have occurred that year. This “artificial” (positive) deviation from the local host population trend did not result in a corresponding positive response by the secondary and tertiary parasitoid complex (i.e., parasitoid numbers continued to decline as expected from the trend). Results were significant when “outlier” was removed (dashed line; note P and R² values in D′). (In A–D, n = 20; in A′–D′, n = 17). SecTert and SeTer, secondary and tertiary; Pr, primary; Den, density.

Fig. 3.

Generalism and budworm density. A–D are based on untransformed data, and A′–D′ are based on transformed data. Similar results were obtained by both methods. (A) Total number of generalist parasitoid species (i.e., species that attack more than one host species) increases with increasing budworm density. (B) Number of primary generalist species does not change with increasing budworm density. (C) Number of secondary and tertiary generalists increases significantly with increasing budworm density. (D) Mean trophic position increases significantly with increasing budworm density. Results in D′ are not significant for the reasons stated in Fig. 2D′ above. However, when “outlier” (indicated by arrow) was removed, results were significant (dashed line; note P′ and R′² values). (In A–D, n = 20; in A′–D′, n = 17.) SecTert, secondary and tertiary; Den, density; TotGen, total generalists; GenPrim, primary generalists; GenSeTe, secondary and tertiary generalists; TP, trophic position.

Fig. 4.

Food webs from manipulative field experiments. (A) Food web generated by implanting several thousand overwintering budworm (second-instar budworm) (mass implanting) on 10–20 balsam fir trees each year from 1990 to 1995, showing the presence of several hyperparasitoid species. (B) Food web generated by implanting individual budworm larvae/pupae (individual implanting) on 150–200 balsam fir trees each year from 1992 to 1995. In contrast to the former experiment, no hyperparasitoids were found. Results of both experiments differed significantly regardless of temporal sequences examined [i.e., 1990–1995 (mass implanting) vs. 1992–1995 (individual implanting) or 1992–1995 for both experiments]. Primary parasitoids enclosed in red squares in individual implanting experiment were found only at low budworm densities. (All codes and symbols are the same as those used in Fig. 1.)