Here, we have synthesized a number of recent theoretical and empirical contributions to suggest that food webs have an adaptable underlying framework that plays a major role in maintaining the persistence of complex interacting assemblages in a naturally variable world. By using organismal traits that scale to body size, we have shown that food webs are constructed of a hump-shaped architecture such that spatially localized lower trophic levels are increasingly coupled by more mobile higher trophic-level organisms. This pattern implies that as we move up food webs, we are in fact increasingly coupling organisms in space (McCann et al. 2005
). Importantly, this hump-shaped architecture appears to be invariant, repeating itself at different resolutions within food webs (within habitats, between habitats and between ecosystems). Furthermore, metabolic theory predicts asymmetric energy flux between coupled energy channels at each level of resolution, as the body sizes of organisms occupying coupled energy channels consistently differ ().
This invariant hump-shaped trophic structure with adaptable apex consumers appears to have important consequences for food-web dynamics. We first looked at the role of stochastic resources on the simple food-web module (i.e. C
) that underlies the invariant hump-shaped trophic observation. In a purely stochastic resource model, we found that asynchronous resources in space and time are muted by an adaptable consumer reacting to this variability. More synchronized resources weaken and eventually remove this stabilizing effect because they reduce the ability for an organism to adapt and average over the environment. We then revisited deterministic food-web theory to show that slow (weak) pathways play not only a critical role in deflecting energy away from potentially fast (strong) unstable interactions (McCann et al. 1998
) but also the combination of fast–slow pathways readily generate resource asynchrony (McCann 2000
). This result is consistent with other fast–slow models containing higher numbers of species that found similar stabilizing results (Post et al. 2000
; Rooney et al. 2006
). This general theory resonates with MacArthur's suggestion that generalists play a critical buffering role in food webs (MacArthur 1955
). Both the theory discussed here and within MacArthur (1955)
do not account for the generalism that occurs due to resource switching by life stage. Here, the rapid behavioural mechanism that drives stability no longer necessarily holds. Further work is needed to understand how this different aspect of generalism plays out in whole food webs.
Our empirical work on aquatic food webs and terrestrial soil food webs revealed some strong consistencies across both environments in the food-web architecture. More empirical analysis, though, across a broader range of terrestrial ecosystems is required. Some important recent work has revealed that there are both fundamental similarities and differences between aquatic and terrestrial ecosystems (Cebrian 2004
; Cebrian & Latrigure 2004
; Shurin et al. 2006
). These differences are not inconsistent with our observations here but importantly point out that the magnitude of different pathways can vary considerably between aquatic and terrestrial webs (e.g. detrital). Nonetheless, differences noted in Shurin et al
; body size and growth rates) agree with our arguments above that terrestrial dynamics are probably a slow channel relative to aquatic flux rates.
While we primarily have focused on how this theory works, there are obvious exceptions and omissions that require reconciliation. The above theory does not make any attempt to embed the role of positive interactions in food webs. This is critical, and fortunately recent research has made significant progress in this area (e.g. Bascompte & Jordano 2007
). Integration across antagonistic and mutualistic work remains a challenge. Additionally, not all food webs are organized so strictly by size as suggested above (e.g. Lafferty et al. 2006
). Insect food webs seem to be an obvious exception to this rule with many higher trophic-level organisms, such as parasitoids, much smaller than their prey. There is clearly a demand for future theory to also more rigorously embed parasites in food webs (Lafferty et al. 2006
). Consistent with the general theory discussed here though, Eveleigh et al.'s (2007)
empirical example found that adaptability within a parasitoid food web occurred in the higher trophic levels. Another obvious exception comes in the form of large mobile herbivores on the terrestrial landscape. Ungulates, for example, often migrate enormous distances, potentially turning the hump-shaped trophic structure upside down. In a sense, the same pieces of the puzzle that confer stability remain. Here, the large herbivores move across the landscape decoupling themselves from their own resources before depleting them and simultaneously removing themselves from their localized predators before they overconsume the herbivores. Recent work has found that lions appear to employ switching behaviour based on the fluctuations in major herbivore prey, and so here top predators are also adaptively responding on the landscape (Owen-Smith & Mills 2008
). Similarly, deBruyn et al. (2004)
found that major predators in the St Lawrence River responded on rapid behavioural time scales to a sewage-enriched food web.
Food-web ecology has frequently adopted a static view of empirical food webs. In this paper, we have argued that the food-web change noted by some empiricists (Winemiller 1990
) may in fact be extremely important for understanding what sustains ecological networks. Unfortunately, gathering the long-term food-web data to test this prediction is an onerous and slow task. However, ecologists may be able to switch this temporal axis to a spatial axis to explore the influence of variability on food-web dynamics and afford us glimpses into the workings of these amazingly complex entities. To accomplish this, ecologists can examine food-web variability by empirically examining how specific ecosystems, with relatively consistent species assemblages, change across gradients in environmental conditions. These gradients can be natural (e.g. lake size, latitude) or human-driven (e.g. human density). Understanding variability across such gradients may also enable us to begin to predict the consequences of human modification on the structure and functioning of ecological systems (McCann 2007
It is worth considering the role of human modifications on the landscape within the context of the framework laid out here. The above theory argues that the variation in lower trophic-level species allows for an ecosystem to maintain a range of responses to a variable world while mobile organisms act to integrate across this landscape of species variability, and do so in such a way as to prevent any lower level organisms from monopolizing space and energy. The large organisms thus promote the balance and maintenance of a diverse and variable assemblage of organisms. Given this, it is of concern that much human activity frequently homogenizes resources in space (e.g. agriculture, silviculture) and also removes higher order consumers by harvesting and habitat fragmentation (Pauly et al. 1998
; Tylianakis et al. 2007
). The synchronization of resources and the removal of the flexible apex consumers therefore remove some of the potent stabilizing forces outlined here. Human modification may be attacking the very aspect of food-web structure that makes it so robust.
It may be that such human actions will be countered by the differential response of fast and slow pathways generating asynchronous variability in prey in space. Here too, though, the human influence frequently is strongly skewing the nature of such fast–slow pathways. As an example, nutrient loading often drives complete dominance by the planktonic web in the form of an algal bloom that shades out littoral production. The system is no longer a balance of littoral and pelagic production but becomes largely a fast pelagic channel process. In this case, the planktonic channel ultimately responds and tends to be relatively low in diversity and dominated by large, inedible blue-green algae. The usually fast pelagic channel is thus changed into a larger, slower, weakly consumed pathway dominated by lower trophic levels. The once persistent diverse pelagic habitat is then transformed into a monoculture of inedible algae, where the fate of primary production is detritus, resulting in increased bacterial decomposition rates. Thus, many aquatic ecosystems with high nutrient loading are now creating dead zones wherein massive bacterial respiration rates remove oxygen from large areas once hospitable to a diverse assemblage of organisms (Moffat 1998
). Other examples exist; agricultural systems effectively skew energy towards fast bacterial pathways and away from slower fungal pathways (Hendrix et al. 1986
), while Layman et al. (2007)
have documented niche width collapse in a top predator coinciding with the homogenization of energy flows following fragmentation. Human modifications may not be just homogenizing variability in space but also appear to be homogenizing production in many ecosystems and, in doing so, slowly decaying the upper trophic structure of ecosystems and their services (Dobson et al. 2006
It is possible that the much impacted ecosystems may ultimately be stabilized by similar mechanisms to those argued above. As an example, the enhancement of the fast pelagic pathway by nutrient run-off may in turn be stabilized by the development of primary production based on largely inedible, or weakly consumed, phytoplankton (i.e. the pelagic channel becomes composed of weak interactions in such a case). However, under such potentially stable conditions, many species will be held at greatly reduced densities. At this point, the question may turn away from stability and more to ecosystem function. In this particular case, the aquatic ecosystem probably experiences greatly reduced function along some fundamental axes (e.g. large anoxic areas, greatly reduced fish production, reduced zooplankton productivity). The stability we have discussed in this paper does not speak to which system is the most stable, but rather how food-web structure helps maintain nature's diverse assemblages. It is possible, although not examined here, that the repeatable hump-shaped structures discussed create a functional system redundancy that enhances the stability of a complex network over a simple network. If so, biological outcomes such as runaway blue-green algae and bacteria may be the final expression of a defeated ecosystem. Curiously, the fate of most aquatic microcosms, perhaps the ultimate homogenized ecosystem, is a similar detrital and bacterial takeover.