Parasites dominate food web links

Abstract

Parasitism is the most common animal lifestyle, yet food webs rarely include parasites. The few earlier studies have indicated that including parasites leads to obvious increases in species richness, number of links, and food chain length. A less obvious result was that adding parasites slightly reduced connectance, a key metric considered to affect food web stability. However, reported reductions in connectance after the addition of parasites resulted from an inappropriate calculation. Two alternative corrective approaches applied to four published studies yield an opposite result: parasites increase connectance, sometimes dramatically. In addition, we find that parasites can greatly affect other food web statistics, such as nestedness (asymmetry of interactions), chain length, and linkage density. Furthermore, whereas most food webs find that top trophic levels are least vulnerable to natural enemies, the inclusion of parasites revealed that mid-trophic levels, not low trophic levels, suffered the highest vulnerability to natural enemies. These results show that food webs are very incomplete without parasites. Most notably, recognition of parasite links may have important consequences for ecosystem stability because they can increase connectance and nestedness.

Fig. 1.

Vulnerability to natural enemies peaks at intermediate trophic levels in the Carpinteria Salt Marsh. Trophic level represents the maximum chain length of a species. Bars represent the average number of natural enemy species that attack consumers in different trophic levels. Vulnerability to predators (dark shading) decreases with trophic level (top predators have no predators themselves). Vulnerability to parasites (light shading), in contrast, increases with trophic level.

Fig. 2.

Comparison of directed connectance with and without parasite links in Carpinteria Salt Marsh. The first bar includes only predator–prey links. The middle bar adds observed parasite–host links but, as in the few previous webs that have incorporated typical parasites, does so inappropriately (see Introduction). The third and fourth bars provide two new methods for determining how parasites affect connectance. The third bar excludes parasite–parasite and predator–parasite links. The fourth bar includes predator–parasite and parasite–parasite links. Comparison of the third and fourth bars with the first bar indicates that parasites increase connectance in food webs. Error bars represent 95% confidence limits.

Fig. 3.

A food web for Carpinteria Salt Marsh divided into four subweb matrices (12). Each consumer species is represented as a column. Rows contain the same list of species, but as prey or hosts. A dot indicates a link in the web. The upper left quadrant is the six-trophic-level predator–prey subweb (or classic food web). The upper right quadrant is the parasite–host subweb. The lower left quadrant is the predator–parasite subweb. Here predators eat parasites in prey, and predators eat free-living stages of parasites. The lower right quadrant is the parasite–parasite subweb, e.g., intraguild predation among larval trematodes in molluscan first-intermediate hosts.