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.connectance ͉ parasitism ͉ trophic ͉ predation ͉ trematode F ood webs trace the flow of energy through an ecosystem. In revealing how consumer-resource interactions lead to trophic cascades, apparent competition, and diversity-stability relationships, food webs provide a unifying theme for ecology (1). Ironically, the most common consumer strategy, parasitism (2), is usually left out of food webs because parasites are often more difficult to quantify by standard ecological methods (3). To fit the resulting parasite-free food webs, prominent theoretical concepts, such as the cascade (4) and niche (5) models, generally assume that consumers eat species smaller than themselves, suggesting that new theoretical models may be needed to accommodate parasites, which eat species larger than themselves. Before taking this step, however, it is expedient to consider how, if at all, parasites affect food webs.Insect parasitoids are the only type of parasite commonly included in food webs. This is because parasitoids are large relative to host size, are easy to sample, and can affect insect population dynamics. However, insights gained from adding parasitoids to food webs may not extend to other infectious agents that have very different life histories (6). In comparison with highly host-specific parasitoids, individual life stages of typical parasites (an adult tapeworm in a dog's gut) can have a broad host range (7). Furthermore, many typical parasites have complex multiple-host life cycles that are embedded in food webs (3). Calls for considering typical parasites in food webs (3,(8)(9)(10) have gained few responses. The initial efforts have shown little effect of including parasites in food webs beyond obvious increases in species richness, number of links, trophi...

Concomitant predation on parasites is highly variable but constrains the ways in which parasites contribute to food web structure

“…Parasites' unique life histories and ways of feeding suggest that they should interact with other species differently than free‐living species (Marcogliese & Cone 1997; Lafferty, Dobson & Kuris 2006; Lafferty et al . 2008; Warren et al .…”

“…The vast majority of food web studies, however, have focused on networks of predator–prey interactions between free‐living species (Combes 1996; Huxham, Beaney & Raffaelli 1996; Marcogliese & Cone 1997; Lafferty, Dobson & Kuris 2006), prompting calls for a broader and more comprehensive food web theory (Marcogliese & Cone 1997; Lafferty, Dobson & Kuris 2006; Fontaine et al . 2011; Kéfi et al .…”

“…2011; Kéfi et al . 2012), especially where parasites are concerned (Marcogliese & Cone 1997; Lafferty, Dobson & Kuris 2006; Dobson et al . 2008; Lafferty et al .…”

“…Huxham, Beaney & Raffaelli 1996). They participate in a large proportion of feeding links (henceforth ‘links’) (Lafferty, Dobson & Kuris 2006; Dunne et al . 2013a) and exhibit comparable diversity and biomass to free‐living species (Dobson et al .…”

“…2013a). The higher connectance of food webs including concomitant links may in turn drive other trends in food web structure, especially in properties such as mean food chain length which have been observed to increase when parasites are added to food webs (Lafferty, Dobson & Kuris 2006) and are known to positively correlate with connectance (Dunne, Williams & Martinez 2002b). In addition to changing connectance, the addition of concomitant predation altered the frequencies with which different configurations of interactions among species occurred.…”