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Review Integrating food web diversity, structure and stability Neil Rooney1,2 and Kevin S. McCann3 1 School of Environmental Sciences, University of Guelph, Guelph, ON, N1G 2W1, Canada Saugeen Ojibway Nation, R. R. #5, Wiarton, ON, N0H 2T0, Canada 3 Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada 2 Given the unprecedented rate of species extinctions facing the planet, understanding the causes and consequences of species diversity in ecosystems is of paramount importance. Ecologists have investigated both the influence of environmental variables on species diversity and the influence of species diversity on ecosystem function and stability. These investigations have largely been carried out without taking into account the overarching stabilizing structures of food webs that arise from evolutionary and successional processes and that are maintained through species interactions. Here, we argue that the same large-scale structures that have been purported to convey stability to food webs can also help to understand both the distribution of species diversity in nature and the relationship between species diversity and food web stability. Specifically, the allocation of species diversity to slow energy channels within food webs results in the skewed distribution of interactions strengths that has been shown to confer stability to complex food webs. We end by discussing the processes that might generate and maintain the structured, stable and diverse food webs observed in nature. The triad of food web ecology Of the many characteristics that can be used to describe food webs, species diversity, structure and stability (see Glossary) are three that have driven much recent ecological research. These three domains are fascinating unto themselves, but some of the most groundbreaking ecology occurs at the intersection of these realms (Figure 1). As we outline below, ecologists have long been fascinated by the link between species diversity and food web stability (the diversity–stability domain). Results from empirical, experimental and theoretical studies regarding this link have been inconsistent, leaving the direct role of species diversity in the stability of food webs elusive. Early efforts to address this conundrum focused on using empirical data from qualitative food web networks to explore the relationship between food web complexity and stability (the structure– stability domain). An excellent review of these efforts was published by Dunne in 2006 [1]. More recently, ecologists have begun to explore the intersection between quantitative food web structures that do take into account the interaction strengths among species and the stability of whole food webs. Similarly, early research on the relationship between Corresponding author: Rooney, N. ([email protected]) 40 food web structure and diversity (the structure–diversity domain) focused on the relationship between qualitative food web structure and diversity. In this article, through a synthesis of theory and data, we make a case for linking species diversity to food web stability through the examination of weighted food web structures, where interaction strengths have a key role in defining that relationship. Below, we briefly synthesize progress that has been made within each of the domains identified in Figure 1, and then present a general integrated framework for diversity, stability and structure in food webs that reintegrates diversity directly into the stability of food webs through the lens of weighted food web structures. Finally, we present a synthesis of research that has focused on how diversity is generated and maintained in both space and time, and demonstrate how our framework fits within this larger ecological context. The diversity–stability debate The study of the relationship between diversity and food web stability has a long and storied history in ecology. Both intuition and observation led many ecologists to hold confidence in a causal link between diversity and stability. In his groundbreaking early work, Elton [2] noted that ‘simple communities are. . .more easily upset. . .than richer ones, that is, more subject to destructive oscillations in Glossary Energy channel: a food web structure that comprises a set of highly interacting, lower trophic-level species that derive their energy largely from the same basal resource. These energy channels tend to be coupled by higher order, mobile predators. Interaction strength: the interaction strength (ai,j) of species j on species i, is generally defined as the per capita measure of the instantaneous rate of population change of species i owing to changes in species j. This can be thought of in the classical sense as the terms of the elements of the community matrix (sensu Robert May [7]), or more directly as the rates of biomass flux between species j and i (e.g. the interaction strength, in terms of biomass flux, of predator j on prey species i is the per capita functional response). Qualitative food web: a representation of feeding interactions within an ecosystem that simply illustrates who eats whom, with no information about the strength of the feeding interactions. Quantitative food web: a representation of feeding interactions within an ecosystem that illustrates both the presence and strength of feeding interactions within that ecosystem. Stability: here, we generally define stability as any continuous metric that attempts to measure the likelihood of the persistence of some set of interacting species. Thus, different metrics (e.g. CV, maximum real eigenvalue or minimum population density) can be used to measure how stable the system is (e.g. a system with a high coefficient of variation is less likely to persist and so is less stable; a system with a lower minimum population density is less likely to persist and so is less stable, etc.). 0169-5347/$ – see front matter . Crown Copyright ß 2011 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.09.001 Trends in Ecology and Evolution, January 2012, Vol. 27, No. 1 Review populations and more vulnerable to invasions’. This inference is not surprising, given that homogenized systems (e.g. agricultural systems) are more prone to wild fluctuations in population densities (as characterized by pest outbreaks) compared with their more diverse counterparts [3,4]. Following Elton’s lead, MacArthur [5] noted that, among food webs, ‘Stability increases as the number of links increases. If the number of prey species for each species remains constant, an increase in the number of species in the community will increase the stability’. Although MacArthur put forth some plausible explanations for the relationship between diversity and stability in nature, he never rigorously tested them. This entire diversity–stability supposition, however, was challenged by both Gardner and Ashby [6] and May [7], who used theoretical approaches to test the relationship between diversity and stability in complex systems. May’s use of random community matrices importantly stripped the communities (i.e. food webs) of any structure, allowing for the direct test of the influence of diversity on the stability of the communities. In doing so, he demonstrated that diversity in fact tends to destabilize community dynamics in the absence of food web structure. More specifically, May posited a stability criterion, wherein food webs that are near equilibrium will tend towards stability when i(SC)1/2 <1 where i is the average interaction strength in the web, S is the number of species and C is the connectance of the web. Thus, a direct causal link between diversity and stability (in the absence of structure) was falsified, and May challenged ecologists to ‘...elucidate the devious strategies which make for stability in enduring natural systems.’ There have been many studies, both empirical and theoretical, that have attempted to elucidate the ‘devious strategies’ through which stability is attained in diverse ecosystems. Following on from May’s stability criterion, ecologists set out to investigate the relationship between connectance and species diversity, hypothesizing that stability could be gained in diverse communities as long as connectance decreased with increasing diversity [1,8,9]. Early explorations of qualitative food web data suggested that more diverse communities tend to have lower connectance, presenting a plausible mechanism through which more diverse communities could remain stable, given May’s stability criterion. In an important contribution, DeAngelis [10] showed that increased connectance could result in increased stability if: (i) consumers had low assimilation efficiencies (i.e. low interaction strengths) (ii) higher trophiclevel species had high levels of self regulation; or (iii) donor control had a large effect on the ecosystem in question. Tilman and colleagues [11–15] have effectively argued for several mechanisms by which the diversity of plant communities could beget temporal stability. However, these mechanisms are largely dependent on diversity occurring within the same trophic level (i.e. producers) and do little to explain the influence of multi trophic-level diversity. Most recent work on multi-trophic diversity has taken a theoretical approach and results often vary. Thebault and Loreau [16], for example, showed that, within multi-trophic food webs, increased diversity can lead to several outcomes, largely depending on the strengths of Trends in Ecology and Evolution January 2012, Vol. 27, No. 1 interactions among the species. Similarly, Duffy et al. [17] have shown that multi trophic-level food webs can result in a variety of diversity–function relationships. Results such as these demonstrate the importance of food web topology and the distribution of interaction strengths in nature in determining the relationship, or the lack thereof, between diversity and stability in food webs. Food web structure and stability Insight into the importance of structure in nature was highlighted in the diversity–stability debate by Yodzis [18]. Yodzis followed May’s mathematical scheme but this time created community matrices that instead contained real food web topologies and plausible estimates of interaction strength. Suddenly, these diverse natural food webs were more stable than the randomly assembled communities in May’s mathematical universe. Yodzis [18] confirmed that diversity in nature was not random; however, it still remained unclear what the underlying structure was that produced stability in these real food webs. One approach to tackling the problem of how food webs are structured to confer stability has been to identify stabilizing modules (or motifs) in food webs, whose stabilizing properties are hypothesized to cascade throughout the larger network of interactions [19,20]. Laboratory analysis of simplified microcosm food webs has demonstrated the stabilizing properties of weak interactions [21,22]. In soil food webs, Neutel et al. [23] have shown that, over the course of ecosystem succession, food webs generate omnivorous loop structures that are hypothesized to stabilize what would otherwise be a destabilizing increase in species diversity. Bascompte and colleagues [24] have similarly shown that the arrangement of interactions in marine food webs makes for relatively stable systems. Specifically, the occurrence of two consecutive strong interactions in food webs is less frequent than would be expected by chance, pointing to the destabilizing properties of strong interactions. Further, when two consecutive strong interactions do occur, they tend to be accompanied by omnivory. Interestingly, it has been shown that a strongly interacting and unstable food chain is often greatly stabilized by weak to moderate strengths of omnivory [16]. The common thread in these results is that they can be viewed within the light of the arrangement of interaction strengths in food webs, particularly weak interactions. McCann et al. [25] showed that weak interactions, which are overrepresented in real food webs [26], have the potential to be powerfully stabilizing. Recent work [27–29] has scaled this weak interaction effect up to the food web scale, documenting the stabilizing properties of fast and slow (i.e. weak and strong) energy channels in food webs. Within this structure, fast energy channels tend to have smaller, faster growing populations that have higher biomass turnover rates compared with the slow energy channels. The ‘food web structure’ domain in Figure 1 shows this overarching architecture, where the left side of the graph represents a slow energy channel wherein biomass turnover rates of taxonomic groups and the interaction strengths between consumers and resources are relatively low when compared with the fast energy channel illustrated on the right side of the graph. Importantly, these energy channels are 41 (Figure_1)TD$IG][ Review Trends in Ecology and Evolution January 2012, Vol. 27, No. 1 Food web structure Trophic position 5 4 3 2 1 40 0 20 60 80 100 Phytoplankton-derived carbon (%) Diversity Non-equilibrium stability Stability 3 2 1 0 0.0 0.5 1.0 1.5 2.0 2.5 Structural asymmetry 3.0 TRENDS in Ecology & Evolution Figure 1. The relationships among diversity, food web structure and stability. Food webs are structured such that top predators couple fast and slow energy channels. This is represented here by the Cantabrian Sea Shelf system [17], wherein top predators, such as tuna, hake and anglerfish, derive energy from both phytoplankton (fast) and detrital (slow) sources. This structural asymmetry in energy flow was shown to have stabilizing properties through the generation of asynchronous dynamics between consumers within each energy channel. The figure embedded in the ‘stability’ domain shows how structural asymmetry increased the non-equilibrium stability of a model system [14]. The relationships between diversity and stability, as well as between diversity and structure, are still unclear. However, we argue that a closer look at food web structure reveals that they are structured such that increasing diversity within slow channels has the potential to stabilize them. coupled by the foraging behavior of mobile top predators that derive energy from each energy channel. There are several reasons why this food web structure is stabilizing. When these systems are perturbed, populations in the fast channel respond quickly, allowing for the rapid recovery of predator populations. The lagged response of the populations in the slow energy channel sets up a scenario in which prey populations in the fast and slow energy channels are behaving in an asynchronous fashion. Such asynchronous resource dynamics produce a less variable resource base for predators, allowing for a rapid but damped return to equilibrium. The weak chain also competes with the strong chain, muting some of the energy flow that would go up the strong channel in the absence of the weak channel. This muting also enhances stability. The relationship between diversity and structure in food webs Here, we argue that we have an opportunity to re-examine the relationship between diversity and stability through 42 the lens of overarching food web architecture. Within offshore marine food webs, the flow of energy through the food web originates either from phytoplankton production (the fast channel) or detritus (the slow channel). Figure 2a shows data from the Cantabrian Sea Shelf ecosystem [30], and demonstrates not only that the diversity of taxa within the slow detrital energy channel (defined as any taxonomic group that ultimately derives more than 50% of its energy from detritus) is higher overall compared with the phytoplankton channel, but this pattern also holds within each trophic level examined. This pattern stands in contrast to the patterns for energy flow within each channel (Figure 2b). Here, even with lower diversity, the fast phytoplankton channel is more productive than the detrital channel. There are several potential proximate explanations for this observed pattern of increased diversity within the slower detrital energy channel (Figure 2a). One first prospective reason is that the benthos is more structurally complex compared with the pelagic zone [31]. Such (Figure_2)TD$IG][ Review (a) Trends in Ecology and Evolution January 2012, Vol. 27, No. 1 (b) 600 30 –1 y ) –2 20 Production (g C m Taxonomic diversity 25 15 10 5 400 200 0 0 2+ 3+ 4+ 2+ 3+ Trophic position (c) Trophic position (d) 25 2000 20 Percent frequency 1500 Number of chains 4+ 1000 500 15 10 5 0 0 Phytoplankton Detritus 3 4 5 6 7 8 9 10 11 12 13 14 15 Number of links TRENDS in Ecology & Evolution Figure 2. Diversity, production and network properties of energy channels within food webs. Comparing properties between energy channels in the Cantabrian Sea Shelf ecosystem reveals that: (a) the majority of diversity within the food web occurs within the slow channel, a property that is repeated at all trophic levels; and (b) productivity is far higher within the fast channel. Given the increased diversity, (c) the slow channel exhibits a higher degree of reticulation, as exhibited by the increased number of realized energy pathways from basal resource (detritus) to top predator compared with the fast energy channel; and (d) the detritus-based slow channel also shows an increase in the average number of links between basal resource and top predator (mean length = 9.2) compared with the fast channel (mean length = 8.6). Key: filled black bars, detritus; open bars, phytoplankton. complexity is expected to harbor more diverse communities than those found in structurally simple habitats, as both competitive and predatory refuges are found more often in complex habitats [32,33]. A second but not exclusive, plausible explanation for increased diversity in the benthos is that the basal resource (detritus) is less labile compared with phytoplankton, and this increases diversity as there is an ontogenetic decomposition process that requires more functional groups to break down the basal resource into usable energy [34]. Both of these factors point towards an increased number of niches within the benthos. By contrast, the pelagic zone is more spatially homogeneous, and the basal resource is far more labile compared with the recalcitrant detritus. Therefore, this energy channel is hypothesized to be a far more competitive environment wherein a singular strategy of growing fast and reproducing quickly is the most successful. Under these conditions, competitive exclusion could have a role in decreasing the diversity of the energy channel. There are empirical arguments to suggest that the above results might be widespread. We note that the architecture of the coupled energy channels in the Cantabrian Sea Shelf system that results in the observed differences in both diversity and interaction strengths has analogies in other ecosystems. The general structure proposed is that of macrohabitats (energy channels) that differ in their structure and are coupled by the feeding behavior of consumers. Similarly, lakes have benthic and pelagic habitats that are coupled by predatory action, and there is evidence that both zooplankton and fish communities are more diverse in the benthic compared with the pelagic habitat [19,35]. There are other food webs where 43 Review Reintegrating diversity back into food web stability Above and beyond the aforementioned putative causes of the patterns in diversity are the possible consequences of this pattern. Specifically, the resulting pattern holds interesting possibilities for a more direct relationship between diversity and stability in nature. For example, the network characteristics within the slow channel differ to those of the fast channel, with the possible number of pathways from basal resource to top predator being far higher in the detritus-based slow energy channel compared with the phytoplankton-based fast channel (Figure 2c). This pattern reflects back to MacArthur’s hypothesis that the amount of choice there is in following the pathways up through the food web is a measure of the stability of the community. Furthermore, the mean number of links between the basal resource and top predator within the detritus-based slow channel is higher compared with the fast channel (Figure 2d), representing a less efficient pathway from basal resource to top predator. It should be noted that this measure is not reflective of the mean trophic level of the top predator, but is instead a network attribute based on qualitative links, many of which are very weak. These observations are particularly fascinating when we revisit MacArthur [5], who stated that, ‘Efficiency enables individual animals to out compete others, but stability allows individual communities to out-survive less stable ones. From this, it seems reasonable that natural selection operates for maximum efficiency subject to certain necessary stability.’ Here, we propose that the observed coupled energy channel architecture of food webs provides efficiency (through the fast channel) and stability (through the slow channel) to larger food webs. One final but crucial pattern emerges from this analysis. As noted above, patterns of interaction strengths in nature have long been hypothesized to influence the stability of food webs. Specifically, it has been noted that the distribution of interaction strengths in nature is such that there are many weak and few strong interactions [26,35,39], and theoretical studies have shown this skewed distribution to be stabilizing [40]. We suggest here that this pattern can be explained by combining food web architecture and the distribution of diversity within food webs. One of the characteristics of feeding interactions within the slow channel is that they tend to be weaker than those in the fast channel [27]. Thus, we would predict that the majority of the weak interactions observed in nature would occur within these slow channels. This is supported in the analysis of the Cantabrian Sea Shelf ecosystem, where we determined the per-capita standardized measure of the strength of the interaction of predators on their prey (IS) as 44 calculated by Bascompte and others [24] as (Equation 1): IS ¼ ðQ=BÞ j DCi j Bi (1) where (Q/B)J is the number of times a population of predator j consumes its own weight per day, DCij is the proportion of prey i in the diet of predator j, and Bi is biomass of prey i. The well-documented pattern of interaction strengths in food webs being skewed towards many weak interactions holds true (Figure 3). This pattern, however, is primarily driven by the many weak interactions observed within the slow channel. Thus, we have a pattern in nature (the skewed distribution of interaction strengths) that has been purported to result in increased stability, and appears to be driven by the distribution of diversity within the food web. One factor that has been explored in determining food web structure and interaction strengths in nature has been body size. Body size ratios between predators and prey have been associated with trophic structure [41,42] and stability [43,44]. Our earlier work on macroecological relationships within and between energy channels showed clear differentiation in body size relationships between nested coupled energy channels [28], suggesting that the observed patterns of interactions strengths is repeated at different scales within food webs. These body size relationships were observed between coupled terrestrial and aquatic ecosystems, within aquatic ecosystems between benthic and pelagic energy channels, and finally within the pelagic energy channels between bacterioplankton and phytoplankton energy channels. It would follow that [(Figure_3)TD$IG]there would be differences in mean interaction strengths 50 45 40 35 30 Frequency coupling has been observed, but the distribution of diversity has not been documented. Such systems include canopy–understory predatory coupling in forest ecosystems [36], fungal and bacterial energy channel predatory coupling in soil ecosystems [37] and resource coupling by frugivorous birds in shrubland communities [38]. It will be fascinating to follow up the distribution of diversity within these systems to determine how general our observed pattern is in nature. Trends in Ecology and Evolution January 2012, Vol. 27, No. 1 25 20 15 10 5 0 –3.0 –2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 Log interaction strength Key: Detritus Phytoplankton TRENDS in Ecology & Evolution Figure 3. Distribution of integration strengths by energy channel. It has been established that the distribution of interaction strengths (defined here as the percapita, standardized measure of the strength of the interaction of predators on their prey [24]) is highly skewed towards many weak interactions and few strong interactions. Here, we show that this pattern is generated in the Cantabrian Sea Shelf ecosystem through the abundance of weak interactions found in the slow detrital channel. Key: filled black bars, detritus; open bars, phytoplankton. Review between these energy channels at all levels, reflecting the larger observations made in this paper. This pattern suggests that the stabilizing distribution of species and interaction strengths in food webs can be iterative and nested, conveying stability to food webs at many different spatial scales. Taken together, these patterns point towards a plausible resolution of the diversity–stability debate. Specifically, increased diversity can indeed lead to increased stability, if that diversity is in the right place within the food web architecture. Although May’s conclusion that diversity in the absence of structure begets instability was no doubt correct, our analysis suggests that food webs are indeed structured such that higher diversity in slow energy channels increases the relative proportion of weak interactions in food webs, leading to increased stability. We argue that, if this pattern holds, there are real insights that can be gained that will shed light on the causes and consequences of diversity in nature. Take, for example, tropical seagrass food webs. These ecosystems are both diverse and productive when not impacted by anthropogenic activities. However, increased human activities have been associated with decreased species diversity in seagrass beds. Tewfik et al. [38,45] examined the structure and diversity of seagrass food webs across a gradient of enrichment. As human density (and associated nutrient concentrations) increases, these ecosystems lose top predators, detritus, specialist consumers and edible seagrass. In effect, what is happening is that the fast phytoplankton energy channel begins to dominate the system, and the diversity associated with the benthic detrital energy channel is lost. As opportunistic consumers, sea urchins capitalize on this ready supply of energy and begin to dominate the systems. At extreme levels of nutrient enrichment, the systems are reduced to a homogenized system dominated by a single, relatively inedible seagrass and a predominance of sea urchins. Similar patterns of decreased diversity of ecosystems associated with homogenization and decreased stability have been observed in a variety of other ecosystems. Habitat fragmentation in tidal creeks reduces the structural complexity of the benthos, shifting food webs to becoming cyanobacterial based as opposed to seagrass and macroalgae based [4]. Algal bloom formation in lacustrine and oceanic ecosystems is largely associated with increased nutrient inputs and the resulting increased pelagic production [46]. Finally, agricultural ecosystems have the tendency to lose species that reside within the fungal energy channels in soil ecosystems [17,47]. Each of these processes represents a decrease in diversity that is targeted at the organisms that reside within slow energy channels, and result in decreased temporal stability of the remaining taxa. Temporal aspects of species diversity, structure and stability It is interesting to take one step back at this point to view our findings in a larger ecological context. As ecosystems mature, there are several characteristics that change in a rather predictable manner. Seminal work by Margalef [48] and Odum [49] highlighted several ecosystem characteristics that change over time that fit very well with Trends in Ecology and Evolution January 2012, Vol. 27, No. 1 our proposed framework for diversity, structure and stability. From an energetic point of view, more mature ecosystems (i.e. systems in later successional stages) have lower primary production per unit biomass (P:B ratio). Associated with this decreased P:B ratio is the increased importance of detritus as a basal resource for consumers. Furthermore, food webs tend to increase in complexity and diversity with time and are more resistant to external perturbations [23,34,40]. Thus, we propose that an increased importance of detritus in ecosystems results in an increase of species diversity in that channel. This increased diversity results in an increase in the number of weak interactions within food webs (Figure 3), conveying stability to the larger web. Furthermore, as these slow energy channels tend, on average, to have larger sized organisms compared with their fast counterparts, allometric relationships differ between the energy channels [28]. Along with this ecosystem development come changes in the behavior of the organisms that reside within. Recent research has brought the concept of connectance and food web stability back into the spotlight by highlighting the role of foraging biology in predicting food web complexity [50,51]. In these food webs, diet breadth based on body size determines food web connectance. It would be interesting, but beyond the scope of this paper, to examine how the energy channel differences in allometric relationships translate into diet breadth characteristics and the ensuing ramifications for differences in connectance between fast and slow energy channels. Concluding remarks In this paper, we have argued that the history of food web ecology has primarily been driven by two of the three domains identified in Figure 1: the diversity–stability domain and the structure–stability domain. A clear and natural area for research exists in studying the relationship between diversity and food web structure, which is the diversity–structure domain (Figure 1). Beyond pointing out this axis, we have identified where structure and diversity appear tightly linked, and propose proximate and ultimate explanations for this observed pattern. The developments that we have presented in this paper point to a novel way of viewing the causes and consequences of species diversity in food webs. In contrast to approaches that have looked for environmental variables that predict species diversity on the landscape scale, we suggest that understanding the distribution of species diversity can be greatly aided by viewing ecosystems through the lens of food web structure. We suggest that the very factors that result in differential energy flow though food web energy channels also result in different potential for species richness within these energy channels, where slow energy channels tend to be more species rich. These slow energy channels also exhibit, on average, more and weaker interactions among species, a putative causal mechanism for increased persistence and, hence, enduring diversity. 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