Are large complex ecosystems more unstable? A theoretical reassessment with predator switching

Multi-species Lotka-Volterra models exhibit greater instability with an increase in diversity and/or connectance. These model systems, however, lack the likely behavior that a predator will prey more heavily on some species if other prey species decline in relative abundance. We find that stability does not depend on diversity and/or connectance in multi-species Lotka-Volterra models with this 'predator switching'. This conclusion is more consistent with several empirical observations than the classic conclusion, suggesting that large complex ecosystems in nature may be more stable than previously supposed.     

Current food web models cannot explain the overall topological structure of observed food webs

Topological food webs illustrating “who eats whom” in different systems exhibit similar, non‐random, structures suggesting that general rules govern food web structure. Current food web models correctly predict many measures of food web topology from knowledge of species richness and connectance (fraction of possible predator–prey links that actually occur), together with assumptions about the ecological rules governing “who eats whom”. However, current measures are relatively insensitive to small changes in topology. Improvement of, and discrimination among, current models requires development of new measures of food web structure. Here I examine whether current food web models (cascade, niche, and nested hierarchy models, plus a random null model) can predict a new measure of food web structure, structural stability. Structural stability complements other measures of food web topology because it is sensitive to changes in topology that other measures often miss. The cascade and null models respectively over‐ and underpredict structural stability for a set of 17 high‐quality food webs. While the niche and nested hierarchy models provide unbiased predictions on average, their 95% confidence intervals frequently fail to include the observed data. Observed structural stabilities for all models are overdispersed compared to model predictions, and predicted and observed structural stabilities are uncorrelated, indicating that important sources of variation in structural stability are not captured by the models. Crucially, poor model performance arises because observed variation in structural stability is unrelated to variation in species richness and connectance. In contrast, almost all other measures of food web topology vary with species richness and connectance in natural webs. No model that takes species richness and connectance as the only input parameters can reproduce observed variation in structural stability. Further progress in predicting and explaining food web topology will require fundamentally new models based on different input parameters.     

Estimating morphologically determined connectance and structure for food webs of freshwater invertebrates

1. Connectance is a parameter of central importance in determining food-web structure, but the processes determining its value remain unclear. In evaluating possible explanations it is useful to know what patterns, and values, of connectance occur in food webs assembled at random from a set of species in a regional species pool; i.e. where the number of links is determined by the morphological features of the species present, not by the immediate effects of energetics or stability on the particular web. 2. This study examines, by means of laboratory experiments, the occurrence of potential feeding interactions among a set of freshwater invertebrate species randomly selected from different freshwater sites in a geographical region. The results from pairwise feeding trials are used to construct two ‘theoretical’ food webs, in which the patterns and values of connectance are examined. 3. Analyses of these webs indicate that their structure is consistent with the observed values in previously documented ‘real’ webs. Directed connectance values of 0.12–0.16 (or less) suggest that the assembled webs are no more connected than many freshwater webs from natural systems. The number of links per species increases curvilinearly with the number of species, during web assembly, consistent with recent hypotheses. 4. These results also indicate that quantifying, and understanding the determinants of, trophic generalism or specialism does have implications for understanding how connectance is constrained in real webs. Freshwater invertebrates seem to be relatively generalist, and freshwater food webs perhaps correspondingly highly connected. Such arguments have implications for interpreting other aspects of food-web structure in these systems, and for parameterizing models that are based on connectance.     

Food Web Topology in High Mountain Lakes

Although diversity and limnology of alpine lake systems are well studied, their food web structure and properties have rarely been addressed. Here, the topological food webs of three high mountain lakes in Central Spain were examined. We first addressed the pelagic networks of the lakes, and then we explored how food web topology changed when benthic biota was included to establish complete trophic networks. We conducted a literature search to compare our alpine lacustrine food webs and their structural metrics with those of 18 published lentic webs using a meta-analytic approach. The comparison revealed that the food webs in alpine lakes are relatively simple, in terms of structural network properties (linkage density and connectance), in comparison with lowland lakes, but no great differences were found among pelagic networks. The studied high mountain food webs were dominated by a high proportion of omnivores and species at intermediate trophic levels. Omnivores can exploit resources at multiple trophic levels, and this characteristic might reduce competition among interacting species. Accordingly, the trophic overlap, measured as trophic similarity, was very low in all three systems. Thus, these alpine networks are characterized by many omnivorous consumers with numerous prey species and few consumers with a single or few prey and with low competitive interactions among species. The present study emphasizes the ecological significance of omnivores in high mountain lakes as promoters of network stability and as central players in energy flow pathways via food partitioning and enabling energy mobility among trophic levels.     

Connectance indicates the robustness of food webs when subjected to species loss

Many ecologists are concerned that biodiversity loss from human impact on natural ecosystems could compromise ecosystem stability. A relationship between diversity and stability was proposed by MacArthur [MacArthur, R.H., 1955. Fluctuation of animal populations and a measure of community stability. Ecology 36, 533–536.]. Current thinking (for example, McCann, K., 2000. The diversity–stability debate. Nature 405, 228–233.) acknowledges that interaction pattern among species, rather than species richness per se, is one element of this relationship. Dunne et al. [Dunne, J.A., Williams, R.J., Martinez, N.D., 2002a. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5, 558–567.] showed that the robustness of 16 food webs is correlated with their connectance. Connectance is one measure of interaction pattern. Robustness relates to the maintenance of network integrity and so has consequences for stability; the loss of integrity must have ecosystem-wide implications. This paper tests the hypothesis that changes in a food web's connectance indicate changes in its robustness. It concludes that any change in connectance with species loss, but especially large, negative changes, constitutes a decrease in robustness. Estimation of the change in connectance could support interpretation of monitoring data on species composition, acting as an indicator of food web robustness and, indirectly, of ecosystem stability. It could assist managers to understand the implications of biodiversity loss caused by human intervention in ecosystems, and could assist either choice of intervention or amelioration of impacts.     

Seasonality,diaspore traits and the structure of plant-frugivore networks in Neotropical savanna forest

Complex frugivory networks are common in heterogeneous environments, but how the structure of those networks varies due to seasonality and other environmental factors remains unclear. For example, seasonal variation in rainfall can influence fruit production and diaspore characteristics, which could alter the quantity and quality of resources available to different animals in the network and, hence, network structure. We investigated how a frugivory network varied seasonally in Brazilian savanna (Cerrado), where there are well-defined dry and wet seasons and fructification mainly during the rainy season for most tree species. We recorded fruit consumption by animals during the dry and wet seasons in two different gallery forests and used these data to test the hypotheses that connectance, links per species and nestedness would be higher in the dry season than rainy season due to low available food in the former that would be consumed by various species of frugivores. Concomitantly, we also measured seed width and lipid content from diaspores of the fruiting trees to determine if these characteristics influenced interaction properties between fruiting trees and frugivores. Among the measured network parameters, connectance, links per species and specialization varied between seasons in one site but not in the other, indicating that seasonal variation in networks is not necessarily consistent over time or space. The number of tree species with small diaspores with high lipid content differed between seasons, and those characteristics were key factors increasing the interaction parameter of fruiting trees. We suggest that network stability between seasons may be related to local frugivore diversity, resource availability, and fruit quality.     

Transient dynamics and food-web complexity in the Lotka-Volterra cascade model

How does the long-term behaviour near equilibrium of model food webs correlate with their short-term transient dynamics? Here, simulations of the Lotka -Volterra cascade model of food webs provide the first evidence to answer this question. Transient behaviour is measured by resilience, reactivity, the maximum amplification of a perturbation and the time at which the maximum amplification occurs. Model food webs with a higher probability of local asymptotic stability may be less resilient and may have a larger transient growth of perturbations. Given a fixed connectance, the sizes and durations of transient responses to perturbations increase with the number of species. Given a fixed number of species, as connectance increases, the sizes and durations of transient responses to perturbations may increase or decrease depending on the type of link that is varied. Reactivity is more sensitive to changes in the number of donor-controlled links than to changes in the number of recipient-controlled links, while resilience is more sensitive to changes in the number of recipient-controlled links than to changes in the number of donor-controlled links. Transient behaviour is likely to be one of the important factors affecting the persistence of ecological communities.     

Global synthesis suggests that food web connectance correlates to invasion resistance

Biological invasions are a key component of global change, and understanding the drivers of global invasion patterns will aid in assessing and mitigating the impact of invasive species. While invasive species are most often studied in the context of one or two trophic levels, in reality species invade communities comprised of complex food webs. The complexity and integrity of the native food web may be a more important determinant of invasion success than the strength of interactions between a small subset of species within a larger food web. Previous efforts to understand the relationship between food web properties and species invasions have been primarily theoretical and have yielded mixed results. Here, we present a synthesis of empirical information on food web connectance and species invasion success gathered from different sources (estimates of food web connectance from the primary literature and estimates of invasion success from the Global Invasive Species Database as well as the primary literature). Our results suggest that higher‐connectance food webs tend to host fewer invaders and exert stronger biotic resistance compared to low‐connectance webs. We argue that while these correlations cannot be used to infer a causal link between food web connectance and habitat invasibility, the promising findings beg for further empirical research that deliberately tests for relationships between food web connectance and invasion.     

Intestine length in the fishes of a tropical stream: 2. Relationships to diet — the long and short of a convoluted issue

Synopsis We examined the relationship between the intestine length and the amount of plant material in the diet of 21 species of fish from forest streams in Panama. Alimentary tract analyses supplemented by literature reports showed that four loricariid catfish species and one poeciliid were specialized herbivores consuming almost exclusively periphyton and detritus. Four species, including one erythrinid, one characid, one trichomyctycterid and one eleotrid, were carnivores consuming almost entirely food of animal origin. Twelve species, including five characids, one lebiasinid, two pimelodelids, three cichlids and one poeciliid, were omnivores consuming food of both plant and animal origin, but the average proportion of food of plant origin (detritus and algae plus higher plant parts) varied from 4–60%. Most omnivores increased plant food consumption with increasing size. Because intestine length increases allometrically with body size and the pattern of increase differs considerably among species and is influenced by length:mass relationships, we compared species at the same size and took both length and mass into account. At a given size, intestine lengths of herbivores were longer than those of omnivores, and these were longer than those of carnivores. Differences in intestine length among the dietary categories were greater at larger body sizes and when the common size was defined by body mass than when it was defined by body length. There was no trend for the average proportion of plant material consumed to be related to intestine length among the omnivores, when confounding effects of body mass were taken into account. The slopes of the allometric equations relating log₁₀ intestine length to log₁₀ body size for herbivores tended to be higher than for omnivores and higher for omnivores than for carnivores, but both herbivores and omnivores showed extensive variation and overlap with the other dietary categories. Among the omnivores, there was no trend for slopes to be steeper for species consuming more plant material on average or for species showing larger ontogenetic increases in plant consumption. These results permit increased precision in describing diet-intestine length relationships, but indicate that the widely held belief that intestine length reflects diet in fishes should only be applied to broad dietary categories and not to finer divisions among omnivores.     

Community stability,complexity and species life history strategies

The essence of the contradiction between traditional ecological complexity-stability hypothesis and recent theoretical results is clarified. The distinction between resilience and resistance is stressed. The possibilities of field verification of May's model are discussed. No satisfactory method for estimation of connectance and mean interaction strength in plant communities has been found. Relation between these parameters and stability in real communities remains an open question. The relation between connectance and stability (resilience) in purely competitive model communities is more complicated than May's rule predicts. The certain value of connectance having been achieved, stability increases with increasing connectance. We assessed the positive relation between species diversity and resistance, and negative relation between species diversity and resilience in plant communities during old-field succession in xeric habitat. But there is no causal relationship between species diversity and both kinds of stability. Resistance and resilience of the plant communities studied were determined primarily by life history strategies of constituent species. The results are interpreted in terms of Grimes' life history strategies and imply the validity of Gleasonian, population-centered explanation of community phenomena.The nomenclature of plants follows F. Ehrendorfer, 1973, Liste der Gefässpflanzen Mitteleuropas, 2. Aufl. G. Fischer, Stuttgart.Acknowledgements. We thank Pavel Kindlmann for helpful discussion. We are also grateful to reviewers for suggesting ways to improve this paper.     

Relative ascendency predicts food web robustness

Threats to ecosystems globally from anthropogenic disturbance and climate change requires us to urgently identify the most sensitive biological communities to ensure they are effectively preserved. It is for this reason that understanding and predicting food web stability has been topical within ecology. Food web stability is a multi-faceted concept that represents the ability of a food web to maintain its integrity following disturbance, it includes resistance, resilience and fragility. In this study, we examine the ability of four food web metrics to predict the fragility to random species extinctions in 120 qualitative food webs. We show that three information-based indices out performed food web connectance in predicting fragility, with relative ascendency having the strongest relationship. Relative ascendency was a much stronger predictor of fragility than MacArthur’s stability metric, Average Mutual Information and connectance as it accounted for both the distribution and number of links between species. We also find that most qualitative food webs persist around a central tendency of relative ascendency.     

Permanence does not predict the commonly measured food web structural attributes

Food web assembly algorithms show great promise for investigating issues involving the dynamics of whole webs, such as succession, rehabilitation, and invasibility. Permanence, which requires that all species densities remain positive and finite, has been suggested as a good stability constraint. This study tests the validity of the permanence constraint by comparing real webs and model webs from the literature to the predictions of three assembly algorithms: one constrained by permanence and feasibility, one constrained by feasibility alone, and one with no dynamical constraint. It is found that the addition of the permanence constraint does not improve the predictive ability of the algorithm. Its main effect is to increase the efficiency of species selected for the web. Dynamically constrained webs have lower connectance and indistinct trophic levels compared to real webs and webs from other models, which is a consequence of omitting species' physiology. Although webs are less likely to be permanent if they have high omnivory and cycling, the web-building process circumvents this constraint. The challenges of testing and justifying system-level hypotheses, including isolating and detecting their effects, are discussed.     

Species loss and secondary extinctions in simple and complex model communities

1. The loss of a species from an ecological community can trigger a cascade of secondary extinctions. Here we investigate how the complexity (connectance) of model communities affects their response to species loss. Using dynamic analysis based on a global criterion of persistence (permanence) and topological analysis we investigate the extent of secondary extinctions following the loss of different kinds of species. 2. We show that complex communities are, on average, more resistant to species loss than simple communities: the number of secondary extinctions decreases with increasing connectance. However, complex communities are more vulnerable to loss of top predators than simple communities. 3. The loss of highly connected species (species with many links to other species) and species at low trophic levels triggers, on average, the largest number of secondary extinctions. The effect of the connectivity of a species is strongest in webs with low connectance. 4. Most secondary extinctions are due to direct bottom-up effects: consumers go extinct when their resources are lost. Secondary extinctions due to trophic cascades and disruption of predator-mediated coexistence also occur. Secondary extinctions due to disruption of predator-mediated coexistence are more common in complex communities than in simple communities, while bottom-up and top-down extinction cascades are more common in simple communities. 5. Topological analysis of the response of communities to species loss always predicts a lower number of secondary extinctions than dynamic analysis, especially in food webs with high connectance.     

Dental topographic analysis of paromomyid (Plesiadapiformes,Primates) cheek teeth: more than 15 million years of changing surfaces and shifting ecologies*

Abstract

Plesiadapiforms, appearing near the Cretaceous-Paleogene boundary, represent the first primate radiation and show a diverse array of tooth morphologies. Dental topographic metrics provide quantitative data on occlusal surface shape. We used three metrics, Dirichlet Normal Energy, Relief Index, and 3D Orientation Patch Count Rotated, to assess changes in the morphology of lower fourth premolars and lower second molars in a taxonomically broad sample of one family of plesiadapiforms, Paromomyidae, stretching more than 15 million years. Our results indicate that paromomyids occupied a more diverse range of dietary categories than suspected. Whereas all paromomyids were likely omnivores, some species show higher levels of insectivory, while other taxa are inferred to have been mixed-feeding omnivores with high levels of fruit intake. The results also show that the more primitive members of the different paromomyid lineages were more insectivorous than the derived and more recent members of those lineages. Relief Index values also show taxonomic signals that are consistent with ancestor-descendant relationships hypothesised for species of Phenacolemur. These results suggest that dental topographic metrics are informative to the study of paromomyids for both dietary categorisation and for the distinction of species at a fine taxonomic level.     

The abundance effect on network nestedness is stronger for parasitic than herbivory interactions

多度对寄生型网络嵌套结构的影响大于食草型网络 因为物种多度显著影响种间互作频率,分析食物网结构对物种多样性和稳定性影响时,应基于能够反映物种真实偏好的网络(即偏好网),而不是直接观察得到的网络(即观察网)。食草网络中(植物为低营养级)的植物资源多度大于寄生网络中(动物为低营养级)寄主资源多度,因此我们假设：寄生网络的结构比食草网络的结构更易受到多度效应的影响。为验证这一假设,我们从已发表的文献中收集了80 个定量观察网络(包括34个植物-食草昆虫网络和46个寄生网络),应用有效多度模型去除物种多度对观察网络的影响,从而得出偏好网络。然后,我们应用weighted NODF和spectral radius两个嵌套系数表征网络嵌套性,分析了观察网和偏好网的物种链接数分布、相互作用均匀度、加权连通度和稳健性的差异。结果表明,在偏好网中,寄生网络的嵌套程度要低于食草网络,这可能是因为去除多度影响增加了种间作用频率的均匀度。偏好网的加权连通度和稳健性显著高于相应的观察网,表明偏好网比观察网具有更高的网络稳定性。未来的食物网研究不仅应关注互惠和拮抗网络的结构差异,还应该关注食草和寄生等不同类型拮抗食物网的结构差异。     

Agricultural intensification drives changes in hybrid network robustness by modifying network structure

Within ecological communities, species engage in myriad interaction types, yet empirical examples of hybrid species interaction networks composed of multiple types of interactions are still scarce. A key knowledge gap is understanding how the structure and stability of such hybrid networks are affected by anthropogenic disturbance. Using 15,169 interaction observations, we constructed 16 hybrid herbivore‐plant‐pollinator networks along an agricultural intensification gradient to explore changes in network structure and robustness to local extinctions. We found that agricultural intensification led to declines in modularity but increases in nestedness and connectance. Notably, network connectance, a structural feature typically thought to increase robustness, caused declines in hybrid network robustness, but the directionality of changes in robustness along the gradient depended on the order of local species extinctions. Our results not only demonstrate the impacts of anthropogenic disturbance on hybrid network structure, but they also provide unexpected insights into the structure‐stability relationship of hybrid networks.     

Using functional groups to investigate community response to environmental changes: two grassland case studies

Functional groups (FG) are an useful generalization to investigate environmental change effects on biotic communities. Assigning species to FGs is a contextual task and carries an arbitrary element, regardless of whether the grouping is obtained a priori or by sophisticated numerical methods. Using two grassland community case studies, we show that even simple FG allocation based on growth form, architecture and longevity (plants and mosses), or foraging characteristics (above-ground invertebrates) can be useful to increase our understanding of community processes. For example, the sensitivity of organisms to climate change increases with trophic rank and is higher in disturbed than in undisturbed communities. Complexity of interaction webs (in terms of web connectance), however, is larger in undisturbed than in disturbed communities. A significant and important relationship is likely to exist between anthropogenic disturbances, community complexity and the ecosystem effects of climate change. Trophic interactions may be disrupted much easier by climate changes in disturbed than in undisturbed communities where complexity may be buffering these effects.     

Increasing community size and connectance can increase stability in competitive communities

The relationship between community complexity and stability has been the subject of an enduring debate in ecology over the last 50 years. Results from early model communities showed that increased complexity is associated with decreased local stability. I demonstrate that increasing both the number of species in a community and the connectance between these species results in an increased probability of local stability in discrete-time competitive communities, when some species would show unstable dynamics in the absence of competition. This is shown analytically for a simple case and across a wider range of community sizes using simulations, where individual species have dynamics that can range from stable point equilibria to periodic or more complex. Increasing the number of competitive links in the community reduces per-capita growth rates through an increase in competitive feedback, stabilising oscillating dynamics. This result was robust to the introduction of a trade-off between competitive ability and intrinsic growth rate and changes in species interaction strengths. This throws new light on the discrepancy between the theoretical view that increased complexity reduces stability and the empirical view that more complex systems are more likely to be stable, giving one explanation for the relative lack of complex dynamics found in natural systems. I examine how these results relate to diversity-biomass stability relationships and show that an analytical solution derived in the region of stable equilibrium dynamics captures many features of the change in biomass fluctuations with community size in communities including species with oscillating dynamics.     

Food web stability and weighted connectance: the complexity-stability debate revisited

How the complexity of food webs relates to stability has been a subject of many studies. Often, unweighted connectance is used to express complexity. Unweighted connectance is measured as the proportion of realized links in the network. Weighted connectance, on the other hand, takes link weights (fluxes or feeding rates) into account and captures the shape of the flux distribution. Here, we used weighted connectance to revisit the relation between complexity and stability. We used 15 real soil food webs and determined the feeding rates and the interaction strength matrices. We calculated both versions of connectance, and related these structural properties to food web stability. We also determined the skewness of both flux and interaction strength distributions with the Gini coefficient. We found no relation between unweighted connectance and food web stability, but weighted connectance was positively correlated with stability. This finding challenges the notion that complexity may constrain stability, and supports the ‘complexity begets stability’ notion. The positive correlation between weighted connectance and stability implies that the more evenly flux rates were distributed over links, the more stable the webs were. This was confirmed by the Gini coefficients of both fluxes and interaction strengths. However, the most even distributions of this dataset still were strongly skewed towards small fluxes or weak interaction strengths. Thus, incorporating these distribution with many weak links via weighted instead of unweighted food web measures can shed new light on classical theories.     

Community assembly: when should history matter?

Community assembly provides a conceptual foundation for understanding the processes that determine which and how many species live in a particular locality. Evidence suggests that community assembly often leads to a single stable equilibrium, such that the conditions of the environment and interspecific interactions determine which species will exist there. In such cases, regions of local communities with similar environmental conditions should have similar community composition. Other evidence suggests that community assembly can lead to multiple stable equilibria. Thus, the resulting community depends on the assembly history, even when all species have access to the community. In these cases, a region of local communities with similar environmental conditions can be very dissimilar in their community composition. Both regional and local factors should determine the patterns by which communities assemble, and the resultant degree of similarity or dissimilarity among localities with similar environments. A single equilibrium in more likely to be realized in systems with small regional species pools, high rates of connectance, low productivity and high disturbance. Multiple stable equilibria are more likely in systems with large regional species pools, low rates of connectance, high productivity and low disturbance. I illustrate preliminary evidence for these predictions from an observational study of small pond communities, and show important effects on community similarity, as well as on local and regional species richness.