Are networks of trophic interactions sufficient for understanding the dynamics of multi-trophic communities? Analysis of a tri-trophic insect food-web time-series.

Resource-consumer interactions are considered a major driving force of population and community dynamics. However, species also interact in many non-trophic and indirect ways and it is currently not known to what extent the dynamic coupling of species corresponds to the distribution of trophic links. Here, using a 10-year data set of monthly observations of a 40-species tri-trophic insect community and nonlinear time series analysis, we compare the occurrence and strengths of both the trophic and dynamic interactions in the insect community. The matching between observed trophic and dynamic interactions provides evidence that population dynamic interactions reflect resource-consumer interactions in the many-species community. However, the presence of a trophic interaction does not always correspond to a detectable dynamic interaction especially for top-down effects. Moreover a considerable proportion of dynamic interactions are not attributable to direct trophic interactions, suggesting the unignorable role of non-trophic and indirect interactions as co-drivers of community dynamics.

Shifting daylength regimes associated with range shifts alter aphid-parasitoid community dynamics.

With climate change leading to poleward range expansion of species, populations are exposed to new daylength regimes along latitudinal gradients. Daylength is a major factor affecting insect life cycles and activity patterns, so a range shift leading to new daylength regimes is likely to affect population dynamics and species interactions; however, the impact of daylength in isolation on ecological communities has not been studied so far. Here, we tested for the direct and indirect effects of two different daylengths on the dynamics of experimental multitrophic insect communities. We compared the community dynamics under "southern" summer conditions of 14.5-hr daylight to "northern" summer conditions of 22-hr daylight. We show that food web dynamics indeed respond to daylength with one aphid species (Acyrthosiphon pisum) reaching much lower population sizes at the northern daylength regime compared to under southern conditions. In contrast, in the same communities, another aphid species (Megoura viciae) reached higher population densities under northern conditions. This effect at the aphid level was driven by an indirect effect of daylength causing a change in competitive interaction strengths, with the different aphid species being more competitive at different daylength regimes. Additionally, increasing daylength also increased growth rates in M. viciae making it more competitive under summer long days. As such, the shift in daylength affected aphid population sizes by both direct and indirect effects, propagating through species interactions. However, contrary to expectations, parasitoids were not affected by daylength. Our results demonstrate that range expansion of whole communities due to climate change can indeed change interaction strengths between species within ecological communities with consequences for community dynamics. This study provides the first evidence of daylength affecting community dynamics, which could not be predicted from studying single species separately.

Low Levels of Artificial Light at Night Strengthen Top-Down Control in Insect Food Web.

Artificial light has transformed the nighttime environment of large areas of the earth, with 88% of Europe and almost 50% of the United States experiencing light-polluted night skies [1]. The consequences for ecosystems range from exposure to high light intensities in the vicinity of direct light sources to the very widespread but lower lighting levels further away [2]. While it is known that species exhibit a range of physiological and behavioral responses to artificial nighttime lighting [e.g., 3-5], there is a need to gain a mechanistic understanding of whole ecological community impacts [6, 7], especially to different light intensities. Using a mesocosm field experiment with insect communities, we determined the impact of intensities of artificial light ranging from 0.1 to 100 lux on different trophic levels and interactions between species. Strikingly, we found the strongest impact at low levels of artificial lighting (0.1 to 5 lux), which led to a 1.8 times overall reduction in aphid densities. Mechanistically, artificial light at night increased the efficiency of parasitoid wasps in attacking aphids, with twice the parasitism rate under low light levels compared to unlit controls. However, at higher light levels, parasitoid wasps spent longer away from the aphid host plants, diminishing this increased efficiency. Therefore, aphids reached higher densities under increased light intensity as compared to low levels of lighting, where they were limited by higher parasitoid efficiency. Our study highlights the importance of different intensities of artificial light in driving the strength of species interactions and ecosystem functions.

Trophic assimilation efficiency markedly increases at higher trophic levels in four-level host-parasitoid food chain.

Trophic assimilation efficiency (conversion of resource biomass into consumer biomass) is thought to be a limiting factor for food chain length in natural communities. In host-parasitoid systems, which account for the majority of terrestrial consumer interactions, a high trophic assimilation efficiency may be expected at higher trophic levels because of the close match of resource composition of host tissue and the consumer's resource requirements, which would allow for longer food chains. We measured efficiency of biomass transfer along an aphid-primary-secondary-tertiary parasitoid food chain and used stable isotope analysis to confirm trophic levels. We show high efficiency in biomass transfer along the food chain. From the third to the fourth trophic level, the proportion of host biomass transferred was 45%, 65% and 73%, respectively, for three secondary parasitoid species. For two parasitoid species that can act at the fourth and fifth trophic levels, we show markedly increased trophic assimilation efficiencies at the higher trophic level, which increased from 45 to 63% and 73 to 93%, respectively. In common with other food chains, δ(15)N increased with trophic level, with trophic discrimination factors (Δ(15)N) 1.34 and 1.49‰ from primary parasitoids to endoparasitic and ectoparasitic secondary parasitoids, respectively, and 0.78‰ from secondary to tertiary parasitoids. Owing to the extraordinarily high efficiency of hyperparasitoids, cryptic higher trophic levels may exist in host-parasitoid communities, which could alter our understanding of the dynamics and drivers of community structure of these important systems.

Experimental Evidence for the Population-Dynamic Mechanisms Underlying Extinction Cascades of Carnivores.

Species extinction rates due to human activities are high, and initial extinctions can trigger cascades of secondary extinctions, leading to further erosion of biodiversity. A potential major mechanism for secondary extinction cascades is provided by the long-standing theory that the diversity of consumer species is maintained due to the positive indirect effects that these species have on each other by reducing competition among their respective resource species. This means that the loss of one carnivore species could lead to competitive exclusion at the prey trophic level, leading to extinctions of further carnivore species. Evidence for these effects is difficult to obtain due to many confounding factors in natural systems, but extinction cascades that could be due to this mechanism have been demonstrated in simplified laboratory microcosms. We established complex insect food webs in replicated field mesocosms and found that the overharvesting of one parasitoid wasp species caused increased extinction rates of other parasitoid species, compared to controls, but only when we manipulated the spatial distribution of herbivore species such that the potential for interspecific competition at this level was high. This provides clear evidence for horizontal extinction cascades at high trophic levels due to the proposed mechanism. Our results demonstrate that the loss of carnivores can have widespread effects on other species at the same trophic level due to indirect population-dynamic effects that are rarely considered in this context.

Qualitative analysis of aphid and primary parasitoid trophic relations of genus Alloxysta (Hymenoptera: Cynipoidea: Figitidae: Charipinae).

Charipinae hyperparasitoids affect effectiveness of the primary parasitoids of aphids by decreasing their abundance and modifying their behavior. As a result, increase of aphid populations can cause severe yield losses in some crops. Therefore, ecological studies on the subfamily Charipinae have a great economical and biological importance. Host specificity of these hyperparasitoids is still under debate and for many Charipinae species very little is known about their trophic relations. Here, we give a comprehensive overview of the trophic relationships between the Charipinae species of the genus Alloxysta Förster and their aphid and primary parasitoids hosts, worldwide. Within this subfamily, Alloxysta arcuata (Kieffer), Alloxysta brevis (Thomson), Alloxysta fuscicornis (Hartig), and Alloxysta victrix (Westwood) are the most generalist species sharing many aphid hosts, while for primary parasitoid hosts these are A. arcuata, A. brevis, Alloxysta pleuralis (Cameron), and A. victrix. Alloxysta citripes (Thomson), Alloxysta halterata (Thomson), Alloxysta leunisii (Hartig), and Alloxysta ramulifera (Thomson) appear, up to now, as the most specialized in relation to the primary parasitoid hosts. Primary parasitoids of the genera Aphidius Nees, Lysiphlebus Förster, Praon Haliday, and Trioxys Haliday are the most common hosts for Alloxysta species, and the common host aphid species belong to the genera Aphis L., Uroleucon Mordvilko, Myzus Passerini, and Sitobion Mordvilko. Host range is analyzed for each Alloxysta species, as well as the extent of overlap between them. We used Jaccard's distance and a hierarchical cluster analysis to determine the host range dissimilarity. A permutation test has been applied to analyze if the host range dissimilarity is significantly different from what is expected by chance. We have calculated additional qualitative measures that complement well the Alloxysta niche overlap analysis and evaluated their host specificity using different indices and bipartite networks.

Application of nitrogen and carbon stable isotopes (δ(15)N and δ(13)C) to quantify food chain length and trophic structure.

Increasingly, stable isotope ratios of nitrogen (δ(15)N) and carbon (δ(13)C) are used to quantify trophic structure, though relatively few studies have tested accuracy of isotopic structural measures. For laboratory-raised and wild-collected plant-invertebrate food chains spanning four trophic levels we estimated nitrogen range (NR) using δ(15)N, and carbon range (CR) using δ(13)C, which are used to quantify food chain length and breadth of trophic resources respectively. Across a range of known food chain lengths we examined how NR and CR changed within and between food chains. Our isotopic estimates of structure are robust because they were calculated using resampling procedures that propagate variance in sample means through to quantified uncertainty in final estimates. To identify origins of uncertainty in estimates of NR and CR, we additionally examined variation in discrimination (which is change in δ(15)N or δ(13)C from source to consumer) between trophic levels and among food chains. δ(15)N discrimination showed significant enrichment, while variation in enrichment was species and system specific, ranged broadly (1.4‰ to 3.3‰), and importantly, propagated variation to subsequent estimates of NR. However, NR proved robust to such variation and distinguished food chain length well, though some overlap between longer food chains infers a need for awareness of such limitations. δ(13)C discrimination was inconsistent; generally no change or small significant enrichment was observed. Consequently, estimates of CR changed little with increasing food chain length, showing the potential utility of δ(13)C as a tracer of energy pathways. This study serves as a robust test of isotopic quantification of food chain structure, and given global estimates of aquatic food chains approximate four trophic levels while many food chains include invertebrates, our use of four trophic level plant-invertebrate food chains makes our findings relevant for a majority of ecological systems.

Evolutionary history and ecological processes shape a local multilevel antagonistic network.

Uncovering the processes that shape the architecture of interaction networks is a major challenge in ecology. Studies have consistently revealed that more closely related taxa tend to show greater overlap in interaction partners, fuelling the idea that interactions are phylogenetically conserved. However, local ecological processes such as exploitative or apparent competition (indirect interactions) might instead cause a decrease in overlap in interacting partners. Because of the taxonomic and geographic coarseness of existing studies, the structuring effect of such processes has been overlooked. Here, we assess the relative importance of phylogeny and ecological processes in a local, highly resolved, four-level antagonistic network. Across all network levels we consistently find that phylogenetic relatedness among resource species is correlated with consumer overlap but that phylogenetic relatedness among consumer species is not or negatively correlated with resource overlap. This pervasive pattern indicates that the antagonistic network has been shaped by both phylogeny on resource range and by exploitative competition limiting resource overlap among closely related consumer species. Intriguingly, the strength of phylogenetic signal varies in a consistent way across the network levels. We discuss the generality of our findings and their implications in a changing world.

The loss of indirect interactions leads to cascading extinctions of carnivores.

Species extinctions are biased towards higher trophic levels, and primary extinctions are often followed by unexpected secondary extinctions. Currently, predictions on the vulnerability of ecological communities to extinction cascades are based on models that focus on bottom-up effects, which cannot capture the effects of extinctions at higher trophic levels. We show, in experimental insect communities, that harvesting of single carnivorous parasitoid species led to a significant increase in extinction rate of other parasitoid species, separated by four trophic links. Harvesting resulted in the release of prey from top-down control, leading to increased interspecific competition at the herbivore trophic level. This resulted in increased extinction rates of non-harvested parasitoid species when their host had become rare relative to other herbivores. The results demonstrate a mechanism for horizontal extinction cascades, and illustrate that altering the relationship between a predator and its prey can cause wide-ranging ripple effects through ecosystems, including unexpected extinctions.

Potential for climate effects on the size-structure of host-parasitoid indirect interaction networks.

Communities of insect herbivores are thought to be structured mainly by indirect processes mediated by shared natural enemies, such as apparent competition. In host-parasitoid interaction networks, overlap in natural enemy communities between any pair of host species depends on the realized niches of parasitoids, which ultimately depend on the foraging decisions of individuals. Optimal foraging theory predicts that egg-limited parasitoid females should reject small hosts in favour of future opportunities to oviposit in larger hosts, while time-limited parasitoids are expected to optimize oviposition rate regardless of host size. The degree to which parasitoids are time- or egg-limited depends in part on weather conditions, as this determines the proportion of an individual's lifespan that is available to foraging. Using a 10-year time series of monthly quantitative host-parasitoid webs, we present evidence for host-size-based electivity and sex allocation in the common secondary parasitoid Asaphes vulgaris. We argue that this electivity leads to body-size-dependent asymmetry in apparent competition among hosts and we discuss how changing weather patterns, as a result of climate change, may impact foraging behaviour and thereby the size-structure and dynamics of host-parasitoid indirect interaction networks.

Indirect commensalism promotes persistence of secondary consumer species.

Local species extinctions may lead to, often unexpected, secondary extinctions. To predict these, we need to understand how indirect effects, within a network of interacting species, affect the ability of species to persist. It has been hypothesized that the persistence of some predators depends on other predator species that suppress competitively dominant prey to low levels, allowing a greater diversity of prey species, and their predators, to coexist. We show that, in experimental insect communities, the absence of one parasitoid wasp species does indeed lead to the extinction of another that is separated by four trophic links. These results highlight the importance of a holistic systems perspective to biodiversity conservation and the necessity to include indirect population dynamic effects in models for predicting cascading extinctions in networks of interacting species.

Ecosystem engineering and predation: the multi-trophic impact of two ant species.

1. Ants are ubiquitous ecosystem engineers and generalist predators and are able to affect ecological communities via both pathways. They are likely to influence any other terrestrial arthropod group either directly or indirectly caused by their high abundance and territoriality. 2. We studied the impact of two ant species common in Central Europe, Myrmica rubra and Lasius niger, on an arthropod community. Colony presence and density of these two ant species were manipulated in a field experiment from the start of ant activity in spring to late summer. 3. The experiment revealed a positive influence of the presence of one ant colony on densities of decomposers, herbivores and parasitoids. However, in the case of herbivores and parasitoids, this effect was reversed in the presence of two colonies. 4. Generally, effects of the two ant species were similar with the exception of their effect on Braconidae parasitoid densities that responded positively to one colony of M. rubra but not of L. niger. 5. Spider density was not affected by ant colony manipulation, but species richness of spiders responded positively to ant presence. This effect was independent of ant colony density, but where two colonies were present, spider richness was significantly greater in plots with two M. rubra colonies than in plots with one colony of each ant species. 6. To test whether the positive ecosystem engineering effects were purely caused by modified properties of the soil, we added in an additional experiment (i) the soil from ant nests (without ants) or (ii) unmodified soil or (iii) ant nests (including ants) to experimental plots. Ant nest soil on its own did not have a significant impact on densities of decomposers, herbivores or predators, which were significantly, and positively, affected by the addition of an intact nest. 7. The results suggest an important role of both ant species in the grassland food web, strongly affecting the densities of decomposers, herbivores and higher trophic levels. We discuss how the relative impact via bottom-up and top-down effects of ants depends on nest density, with a relatively greater top-down predatory impact at higher densities.

A positive trait-mediated indirect effect involving the natural enemies of competing herbivores.

Trait-mediated indirect effects can have important effects on food web dynamics but are still poorly understood in the field. In a previous population cage study of a small community of aphids and an aphid natural enemy it was found that a trait-mediated indirect effect involving the natural enemy's behaviour was key to understanding community persistence. Here evidence is presented that a related phenomenon involving some of the same species occurs in the field. Surveys showed that two species of aphid (Acyrthosiphon pisum and Megourella purpurea) tended to share a host plant with a third generally unpalatable species (Megoura viciae) more often than expected by chance. Further evidence suggested this was not due to differential plant suitability or location, but to a positive effect of M. viciae on the performance of the other two species. To test this, field experiments were set up comparing the size and persistence of A. pisum colonies sharing or not sharing a plant individual with M. viciae colonies. A. pisum colonies tended to be larger and persisted for a longer period of time in the presence of M. viciae, an effect that was significant for small colonies exposed to many predators. When protected from predation the presence of M. viciae had no effect on A. pisum colonies. The positive effects of M. viciae on A. pisum is thus likely to be natural-enemy mediated rather than plant mediated. How predation by Syrphidae, the major group observed in the study, is affected by M. viciae is discussed.

Ecological networks--beyond food webs.

1. A fundamental goal of ecological network research is to understand how the complexity observed in nature can persist and how this affects ecosystem functioning. This is essential for us to be able to predict, and eventually mitigate, the consequences of increasing environmental perturbations such as habitat loss, climate change, and invasions of exotic species. 2. Ecological networks can be subdivided into three broad types: 'traditional' food webs, mutualistic networks and host-parasitoid networks. There is a recent trend towards cross-comparisons among network types and also to take a more mechanistic, as opposed to phenomenological, perspective. For example, analysis of network configurations, such as compartments, allows us to explore the role of co-evolution in structuring mutualistic networks and host-parasitoid networks, and of body size in food webs. 3. Research into ecological networks has recently undergone a renaissance, leading to the production of a new catalogue of evermore complete, taxonomically resolved, and quantitative data. Novel topological patterns have been unearthed and it is increasingly evident that it is the distribution of interaction strengths and the configuration of complexity, rather than just its magnitude, that governs network stability and structure. 4. Another significant advance is the growing recognition of the importance of individual traits and behaviour: interactions, after all, occur between individuals. The new generation of high-quality networks is now enabling us to move away from describing networks based on species-averaged data and to start exploring patterns based on individuals. Such refinements will enable us to address more general ecological questions relating to foraging theory and the recent metabolic theory of ecology. 5. We conclude by suggesting a number of 'dead ends' and 'fruitful avenues' for future research into ecological networks.

Resource competition and shared natural enemies in experimental insect communities.

Much theory has been developed to explore how competition for shared resources (exploitation competition) or the presence of shared natural enemies (apparent competition) might structure insect and other communities. It is harder to predict what happens when both processes operate simultaneously. We describe an experiment that attempted to explore how shared natural enemies and resource competition structured a simple experimental insect community. Replicated communities were assembled in population cages consisting of the aphid species Acyrthosiphon pisum and Megoura viciae either alone or competing for a resource, their shared host plant Vicia faba. Each combination was set up with and without the parasitoid Praon dorsale which attacked both species of aphid. Population dynamic data show that interspecific resource competition was the dominant process structuring the community. Though juvenile parasitoids could develop successfully inside hosts of both species, they failed to suppress either aphid below their carrying capacities and were unable to persist on one species. We suggest that intense resource competition may reduce the value of individual aphids as hosts for parasitoids such that their population growth rate is less than zero and discuss whether this phenomenon occurs in natural and agricultural communities.

Direct and indirect effects of resource quality on food web structure.

The diversity and complexity of food webs (the networks of feeding relationships within an ecological community) are considered to be important factors determining ecosystem function and stability. However, the biological processes driving these factors are poorly understood. Resource quality affects species interactions by limiting energy transfer to consumers and their predators, affecting life history and morphological traits. We show that differences in plant traits affect the structure of an entire food web through a series of direct and indirect effects. Three trophic levels of consumers were influenced by plant quality, as shown by quantitative herbivore-parasitoid-secondary parasitoid food webs. We conclude, on the basis of our data, that changes in the food web are dependent on both trait- and density-mediated interactions among species.

Apparent competition, quantitative food webs, and the structure of phytophagous insect communities.

Phytophagous insects and their natural enemies make up one of the largest and most diverse groups of organisms on earth. Ecological processes, in particular negative indirect effects mediated by shared natural enemies (apparent competition), may be important in structuring phytophagous insect communities. The potential for indirect interactions can be assessed by analyzing the trophic structure of insect communities, and we claim that quantitative food webs are particularly well suited for this task. We review the experimental evidence for both short-term and long-term apparent competition in phytophagous insect communities and discuss the possible interactions between apparent competition and intraguild predation or shared mutualists. There is increasing evidence for the importance of trait-mediated as well as density-mediated indirect effects. We conclude that there is a need for large-scale experiments manipulating communities in their entirety and a greater integration of community and chemical ecology.