Terrestrial trophic cascades: how much do they trickle?

Although more consensus is now emerging on the magnitude and frequency of cascading trophic effects in aquatic communities, the debate over their terrestrial counterparts continues. We used meta-analysis to analyze field experiments on trophic cascades in terrestrial arthropod-dominated food webs to evaluate the overall magnitude of trophic cascades and conditions affecting their occurrence and strength. We found extensive support for the presence of trophic cascades in terrestrial communities. In the majority of experiments, predator removal led to increased densities of herbivorous insects and higher levels of plant damage. Cascades in which removing predators led to decreased herbivory also were detected but were less frequent and weaker, suggesting a predominantly three-trophic-level behavior of arthropod-dominated terrestrial food webs. Despite the clear evidence that cascades often decreased plant damage, residual effects of predation produced either no or only minimal changes in overall plant biomass. Agricultural systems and natural communities exhibited similarly strong effects of predation on herbivore abundance. However, resulting effects on plant damage and community-wide effects of trophic cascades on plant biomass usually were highly variable, and only in the managed agricultural systems did predators occasionally have strong indirect effects on plant biomass. Our meta-analysis suggests that the effects of trophic cascades on the biomass of primary producers are weaker in terrestrial than aquatic food webs.     

Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants

We present a quantitative synthesis of trophic cascades in terrestrial systems using data from 41 studies, reporting 60 independent tests. The studies covered a wide range of taxa in various terrestrial systems with varying degrees of species diversity. We quantified the average magnitude of direct effects of carnivores on herbivore prey and indirect effects of carnivores on plants. We examined how the effect magnitudes varied with type of carnivores in the study system, food web diversity, and experimental protocol. A metaanalysis of the data revealed that trophic cascades were common among the studies. Exceptions to this general trend did arise. In some cases, trophic cascades were expected not to occur, and they did not. In other cases, the direct effects of carnivores on herbivores were stronger than the indirect effects of carnivores on plants, indicating that top-down effects attenuated. Top-down effects usually attenuated whenever plants contained antiherbivore defenses or when herbivore species diversity was high. Conclusions about the strength of top-down effects of carnivores varied with the type of carnivore and with the plant-response variable measured. Vertebrate carnivores generally had stronger effects than invertebrate carnivores. Carnivores, in general, had stronger effects when the response was measured as plant damage rather than as plant biomass or plant reproductive output. We caution, therefore, that conclusions about the strength of top-down effects could be an artifact of the plant-response variable measured. We also found that mesocosm experiments generally had weaker effect magnitudes than open-plot field experiments or observational experiments. Trophic cascades in terrestrial systems, although not a universal phenomenon, are a consistent response throughout the published studies reviewed here. Our analysis thus suggests that they occur more frequently in terrestrial systems than currently believed. Moreover, the mechanisms and strengths of top-down effects of carnivores are equivalent to those found in other types of systems (e.g., aquatic environments).     

Nutrient-limited food webs with up to three trophic levels: feasibility, stability, assembly rules, and effects of nutrient enrichment

Community structure is controlled, among multiple factors, by competition and predation. Using the R* rule and graphical analysis, we analyse here the feasibility, stability and assembly rules of resource-based food webs with up to three trophic levels. In particular, we show that (1) the stability of a food web with two plants and two generalist herbivores does not require that plants' resource exploitation abilities trade-off with resistance to the two herbivores, and (2) food webs with two plants and either one generalist herbivore and a carnivore or two generalist herbivores and two generalist carnivores are not feasible because of cascade competition between top consumers. The relative strength of species interactions and the relative impacts of plants and herbivores on factors which control their growth also play a critical role. We discuss how community structure constrains assembly rules and yields cascades of extinctions in food webs.     

Food quality, nutrient limitation of secondary production, and the strength of trophic cascades

Recent meta‐analyses confirm that the strength of trophic cascades (indirect positive effects of predators on plant biomass through control of herbivores) varies among ecosystem types. In particular, most terrestrial systems show smaller cascades than most aquatic ones. Ecologists still remain challenged to explain this variation. Here, we examine a food quality hypothesis which states that higher quality plants should promote stronger trophic cascades. Food quality involves two components: digestion resistance of plants and magnitude of stoichiometric imbalance between plants and herbivores (where stoichiometry involves ratios of nutrient:carbon ratio of tissues). Both factors vary among ecosystems and could mediate conversion efficiency of plants into new herbivores (and hence control of plants by herbivores). We explored the food quality hypothesis using two models, one assuming that plant stoichiometry is a fixed trait, the other one allowing this trait to vary dynamically (but with a minimal nutrient:carbon ratio of structural mass). Both models produce the same suite of results. First, as expected, systems with more easily digested plants promote stronger cascades. Second, contrary to expectations, higher (fixed or minimal) nutrient:carbon ratio of plants do not promote stronger cascades, largely because of the net result of ecosystem feedbacks. Still, the model with dynamic stoichiometry permits positive correlations of realized plant nutrient:carbon ratio and cascade strength (as predicted), mediated through digestion resistance. Third, lower nutrient:carbon ratio of herbivores promotes stronger cascades. However, this result likely cannot explain variation in cascade strength because nutrient:carbon stoichiometry of herbivores does not vary greatly between terrestrial and aquatic ecosystems. Finally, we found that predation promotes nutrient limitation of herbivores. This finding highlights that food web processes, such as predation, can influence stoichiometry‐mediated interactions of plants and herbivores.     

Bottom-up trophic cascades and material transfer in terrestrial food webs

In contrast to top-down trophic cascades, few reviews have appeared of bottom-up trophic cascades. We review the recent development of research on bottom-up cascades in terrestrial food webs, focusing on tritrophic systems consisting of plants, herbivorous insects, and natural enemies, and attempt to integrate bottom-up cascade and material transfer among trophic levels. Bottom-up cascades are frequently reported in various tritrophic systems, and are important to determine community structure, population dynamics, and individual performance of higher trophic levels. In addition, we highlight several features of bottom-up cascades. Accumulation or dilution of plant nutritional and defensive materials by herbivorous insects provides a mechanistic base for several bottom-up cascades. Such a stoichiometric approach has the potential to improve our understanding of bottom-up cascading effects in terrestrial food webs. We suggest a future direction for research by integration of bottom-up cascades and material transfer among trophic levels.     

Keystone mutualism influences forest tree growth at a landscape scale

Interactions between ants and phloem‐feeding herbivores are characterised as a keystone mutualism because they restructure arthropod communities and generate trophic cascades. Keystone interactions in terrestrial food webs are hypothesised to depend on herbivore community structure and bottom‐up effects on plant growth. Here, we tested this prediction at a landscape scale with a long‐term ant‐exclusion experiment on hickory saplings in the context of spatial variation in herbivore community structure and habitat quality. We quantified top‐down effects of ants, herbivore communities as well as abiotic factors impacting hickory shoot growth. We found that ants influenced shoot growth via strong, context‐dependent, compensatory effects, with clear cascading benefits only when phloem‐feeders were present and chewing herbivore abundance was high. By contrast, while several landscape variables predicted hickory growth, they did not mediate the strength of cascading effects of ants. These results suggest that ant/sap‐feeder mutualisms may regulate forest productivity by mediating effects of multiple herbivore guilds.     

Contrasting cascades: insectivorous birds increase pine but not parasitic mistletoe growth

1. Intraguild predation occurs when top predators feed upon both intermediate predators and herbivores. Intraguild predators may thus have little net impact on herbivore abundance. Variation among communities in the strength of trophic cascades (the indirect effects of predators on plants) may be due to differing frequencies of intraguild predation. Less is known about the influence of variation within communities in predator-predator interactions upon trophic cascade strength. 2. We compared the effects of a single predator community between two sympatric plants and two herbivore guilds. We excluded insectivorous birds with cages from ponderosa pine Pinus ponderosa trees parasitized by dwarf mistletoe Arceuthobium vaginatum. For 3 years we monitored caged and control trees for predatory arthropods that moved between the two plants, foliage-feeding caterpillars and sap-feeding hemipterans that were host-specific, and plant damage and growth. 3. Excluding birds increased the abundance of ant-tended aphids on pine and resulted in an 11% reduction in pine woody growth. Mutualist ants protected pine-feeding aphids from predatory arthropods, allowing aphid populations to burgeon in cages even though predatory arthropods also increased in cages. By protecting pine-feeding aphids from predatory arthropods but not birds, mutualist ants created a three-tiered linear food chain where bird effects cascaded to pine growth via aphids. 4. In contrast to the results for tended aphids on pine, bird exclusion had no net effects on untended pine herbivores, the proportion of pine foliage damaged by pine-feeding caterpillars, or the proportion of mistletoe plants damaged by mistletoe-feeding caterpillars. These results suggest that arthropod predators, which were more abundant in cages as compared with control trees, compensated for bird predation of untended pine and mistletoe herbivores. 5. These contrasting effects of bird exclusion support food web theory: where birds were connected to pine by a linear food chain, a trophic cascade occurred. Where birds fed as intraguild predators, the reticulate food webs linking birds to pine and mistletoe resulted in no net effects on herbivores or plant biomass. Our study shows that this variation in food web structure occurred between sympatric plants and within plants between differing herbivore guilds.     

Spatial variation in vegetation damage relative to primary productivity,small rodent abundance and predation

The relative importance of top‐down and bottom‐up mechanisms in shaping community structure is still a highly controversial topic in ecology. Predatory top‐down control of herbivores is thought to relax herbivore impact on the vegetation through trophic cascades. However, trophic cascades may be weak in terrestrial systems as the complexity of food webs makes responses harder to predict. Alternatively, top‐down control prevails, but the top‐level (predator or herbivore) changes according to productivity levels. Here we show how spatial variation in the occurrence of herbivores (lemmings and voles) and their predators (mustelids and foxes) relates with grazing damage in landscapes with different net primary productivity, generating two and three trophic level communities, during the 2007 rodent peak in northern Norway. Lemmings were most abundant on the unproductive high‐altitude tundra, where few predators were present and the impact of herbivores on vegetation was strong. Voles were most common on a productive, south facing slope, where numerous predators were present, and the impacts of herbivores on vegetation were weak. The impact of herbivores on the vegetation was strong only when predators were not present, and this cannot be explained by between‐habitat differences in the abundance of plant functional groups. We thus conclude that predators influence the plant community via a trophic cascade in a spatial pattern that support the exploitation ecosystems hypothesis. The responses to grazing also differed between plant functional groups, with implications for short and long‐term consequences for plant communities.     

Copepods act as a switch between alternative trophic cascades in marine pelagic food webs

A recent meta‐analysis indicates that trophic cascades (indirect effects of predators on plants via herbivores) are weak in marine plankton in striking contrast to freshwater plankton ( Shurin et al. 2002 , Ecol. Lett., 5, 785–791). Here we show that in a marine plankton community consisting of jellyfish, calanoid copepods and algae, jellyfish predation consistently reduced copepods but produced two distinct, opposite responses of algal biomass. Calanoid copepods act as a switch between alternative trophic cascades along food chains of different length and with counteracting effects on algal biomass. Copepods reduced large algae but simultaneously promoted small algae by feeding on ciliates. The net effect of jellyfish on total algal biomass was positive when large algae were initially abundant in the phytoplankton, negative when small algae were dominant, but zero when experiments were analysed in combination. In contrast to marine systems, major pathways of energy flow in Daphnia‐dominated freshwater systems are of similar chain length. Thus, differences in the length of alternative, parallel food chains may explain the apparent discrepancy in trophic cascade strength between freshwater and marine planktonic systems.     

Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores

Small marine herbivores that live on the plants they consume often selectively eat seaweeds that are chemically defended from fishes. Their feeding is unaffected or stimulated by the plant metabolites that deter fishes, and these small herbivores dramatically reduce their susceptibility to predation by associating with host plants that are noxious to fishes. Ecological similarities between these small marine herbivores and numerous terrestrial insects suggest that herbivorous insects also may have evolved a preference for toxic plants because this diminishes their losses to predators, parasites and pathogens. Although marine and terrestrial plants and herbivores evolved in strikingly different environments, the ease of experimentation in some marine systems makes them ideal for addressing certain questions of fundamental importance to both terrestrial and marine workers.     

Bears benefit plants via a cascade with both antagonistic and mutualistic interactions

Predators can influence primary producers by generating cascades of effects in ecological webs. These effects are often non‐intuitive, going undetected because they involve many links and different types of species interactions. Particularly, little is understood about how antagonistic (negative) and mutualistic (positive) interactions combine to create cascades. Here, we show that black bears can benefit plants by consuming ants. The ants are mutualists of herbivores and protect herbivores from other arthropod predators. We found that plants near bear‐damaged ant nests had greater reproduction than those near undamaged nests, due to weaker ant protection for herbivores, which allowed herbivore suppression by arthropod predators. Our results highlight the need to integrate mutualisms into trophic cascade theory, which is based primarily on antagonistic relationships. Predators are often conservation targets, and our results suggest that bears and other predators should be managed with the understanding that they can influence primary producers through many paths.     

Convergence of trophic interaction strengths in grassland food webs through metabolic scaling of herbivore biomass

1. Food web theory hypothesizes that trophic interaction strengths of consumers should vary with consumer metabolic body mass (mass(0·75) ) rather than simply with consumer body mass (mass(1·0) ) owing to constraints on consumption imposed by metabolic demand for and metabolic capacity to process nutrients and energy. Accordingly, species with similar metabolic body masses should have similar trophic interaction strengths. 2. We experimentally tested this hypothesis by assembling food webs comprised of species of arthropod predators, small sap-feeding and large leaf-chewing insect herbivores and herbaceous plants in a New England, USA meadow grassland. The experiment comprised of a density-matching treatment where herbivore species were stocked into field mesocosms at equal densities to quantify baseline species identity and metabolic body mass effects. The experiment also comprised of a metabolic biomass-matching treatment where smaller sap-feeding herbivore (SH) species were stocked into mesocosms such that the product of their density and metabolic body mass (metabolic biomass) was equal to the large herbivore (LH) species. We compared the magnitude of the direct effects of herbivore species on plants in the different treatments. We also compared the magnitude of indirect effects between predators and plants mediated by herbivores in the different treatments. 3. Consistent with the hypothesis, we found that increasing metabolic biomass translated into a 9-14-fold increase in magnitude of herbivore direct effects and up to a fivefold increase in indirect effects on plants. Moreover, metabolic biomass matching caused interaction strengths among herbivore species to converge. This result came about through increases in the herbivore mean effects as well as decreases in variation in effects among treatment replicates as herbivore metabolic biomass increased. 4. We found, however, that herbivore feeding mode rather than herbivore metabolic biomass explained differences in the sign of indirect effects in the different food webs. 5. We conclude that increasing herbivore metabolic biomass not only strengthened the direct and indirect effects on plants but also made those effects more consistent across space. Nevertheless, metabolic biomass alone could not completely explain variation in the nature of indirect effects in the food web, suggesting that additional consideration of consumer traits like feeding mode will provide a more nuanced understanding of trophic interaction strengths in food webs.     

Intraguild predation,invertebrate predators,and trophic cascades in lake food webs

The top-down and bottom-up properties of model food webs that include intraguild predation and self-limiting factors such as cannibalism are investigated. Intraguild predation can dampen or even reverse the top-down effects predicted by food chain theory. The degree of self-limitation among the intraguild prey is a key factor in determining the direction and strength of the top-down response. Intraguild predation and self-limiting factors can also substantially alter the bottom-up effects of enrichment. These results can help explain the disparate results of trophic cascade experiments in lakes, where cascades are usually seen when large Daphnia are the primary herbivores, but not when smaller-bodied herbivores are dominant. Top-down manipulations should cascade at least modestly to phytoplankton in those lakes whose food web can be reasonably approximated by a chain (typically, those where Daphnia is the dominant herbivore), as predicted by food chain theory. On the other hand, smaller-bodied zooplankton are often preyed upon heavily by invertebrate predators as well as by planktivorous fish, thereby introducing elements of intraguild predation into these food webs. In this case, conventional food chain theory is likely to give incorrect predictions. Very large cascade effects may be due primarily to regime shifts between intraguild predation-dominated food webs and those that more resemble food chains, rather than due to the simple food chain cascade usually considered.     

A large trophic quilt

Plants and invertebrate herbivores are major constituents of terrestrial food webs. Identifying component species and tracing their interactions in highly diverse communities are a monumental task. Novotny et al. 2010 present the first broad conspectus of herbivore–plant interactions in a forest in Papua New Guinea. In more than 15 years, nearly 7000 feeding links were traced between about 200 plants and 1500 insect herbivores. Although staggering, these figures might represent only 15% of the total herbivore richness and interaction diversity in that lowland forest. Standardized comparisons also showed distinctive specialization and diversification patterns in different feeding guilds, restricting the possibility of using any single guild as surrogate for the entire assemblage.     

Invasive plants have different effects on trophic structure of green and brown food webs in terrestrial ecosystems: a meta‐analysis

Although invasive plants are a major source of terrestrial ecosystem degradation worldwide, it remains unclear which trophic levels above the base of the food web are most vulnerable to plant invasions. We performed a meta‐analysis of 38 independent studies from 32 papers to examine how invasive plants alter major groupings of primary and secondary consumers in three globally distributed ecosystems: wetlands, woodlands and grasslands. Within each ecosystem we examined if green (grazing) food webs are more sensitive to plant invasions compared to brown (detrital) food webs. Invasive plants have strong negative effects on primary consumers (detritivores, bacterivores, fungivores, and/or herbivores) in woodlands and wetlands, which become less abundant in both green and brown food webs in woodlands and green webs in wetlands. Plant invasions increased abundances of secondary consumers (predators and/or parasitoids) only in woodland brown food webs and green webs in wetlands. Effects of invasive plants on grazing and detrital food webs clearly differed between ecosystems. Overall, invasive plants had the most pronounced effects on the trophic structure of wetlands and woodlands, but caused no detectable changes to grassland trophic structure.     

A trophic cascade in a macrophyte-based food web at the land–water ecotone

Trophic cascades may purportedly be more common in aquatic than terrestrial food webs, but herbivory on freshwater vascular plants has historically been considered low. Water lilies are an exception, suffering severe grazing damage by leaf beetles. To test whether a central prediction of cascade models—that predator effects propagate downwards to plants—operates in a macrophyte-based food web, we experimentally manipulated predation pressure on a key herbivore of water lilies in the littoral zone of a lake in Michigan, USA. Field experiments comprised combinations of caging treatments to alter the number of predators (larvae of the ladybird beetle Coleomegilla maculata) that hunt the grazers of the macrophytes (larvae of the leaf beetles Galerucella nymphaeae) on the leaves of the water lily Nuphar advena. Predatory larvae of the ladybird beetles significantly reduced grazing damage to water-lily leaves by 35–43%. The predators reduced plant damage chiefly via density-mediated effects, when lower densities of grazers translated to significant declines in plant damage. Plant damage caused by the surviving herbivores was less than predicted from individual grazing rates under predator-free conditions. This suggests that trait-mediated effects may possibly also operate in this cascade. The observed strong effect of predators on a non-adjacent trophic level concurs with an essential component of the trophic cascade model, and the cascade occurred at the ecotone between aquatic and terrestrial habitats: Nuphar is an aquatic macrophyte with emergent and floating leaves, whereas both beetle species are semi-terrestrial and use the dry, emergent and floating leaves of the water lily as habitat. Also, the cascade is underpinned by freshwater macrophytes—a group for which trophic processes have often been underappreciated in the past.     

Stage-structured ontogeny in resource populations generates non-additive stabilizing and de-stabilizing forces in populations and communities

Demographic heterogeneity influences how populations respond to density dependent intraspecific competition and trophic interactions. Distinct stages across an organism's development, or ontogeny, are an important example of demographic heterogeneity. In consumer populations, ontogenetic stage structure has been shown to produce categorical differences in population dynamics, community dynamics and even species coexistence compared to models lacking explicit ontogeny. The study of consumer–resource interactions must also consider the ontogenetic stage structure of the resource itself, particularly plants, given their fundamental role at the basis of terrestrial food webs. We incorporate distinct ontogenetic stages of plants into an adaptable multi-stage consumer–resource modeling framework that facilitates studying how stage specific consumers shape trophic dynamics at low trophic levels. We describe the role of density dependent demographic rates in mediating the dynamics of stage-structured plant populations. We then investigate how these demographic rates interact with consumer pressure to influence stability and coexistence in multiple stage-specific consumer–resource interactions. Results detail how density dependent effects across distinct ontogenetic stages in plant development produce non-additivity in the drivers of dynamic stability both in single populations and in consumer–resource settings, challenging the ubiquity of certain traditional ecological dynamic paradigms. We also find categorical differences in the population variability induced by herbivores consuming separate plant stages. Consumer–resource models, such as plant–herbivore interactions, often average out demographic heterogeneity in populations. Here, we show that explicitly including plant demographic heterogeneity through ontogeny yields distinct dynamic expectations for both plants and herbivores compared to traditional consumer–resource formulations. Our results indicate that efforts to understand the demographic effect of herbivores on plant populations may need to also consider the effects of plant demographics on herbivores and the reciprocal relationship between them.     

Trickle-down effects of aboveground trophic cascades on the soil food web

Trophic cascades are increasingly being regarded as important features of aboveground and belowground food webs, but the effects of aboveground cascades on soil food webs, and vice versa, remains essentially unexplored. We conducted an experiment consisting of model synthesised communities containing grassland plant and invertebrate species, in which treatments included soil only, soil+plants, soil+plants+aphids, and soil+plants+aphids+predators; predator treatments consisted of the lacewing Micromus tasmaniae and ladybird beetle Coccinella undecimpunctata added either singly or in combination. Addition of Micromus largely reversed the negative effects of aphids on plant biomass, while both of the predator species caused large changes in the relative abundances of dominant plant species. Predators of aphids also affected several components of the belowground subsystem. Micromus had positive indirect effects on the primary consumer of the soil decomposer food web (microflora), probably through promoting greater input of basal resources to the decomposer subsystem. Predator treatments also influenced densities of the tertiary consumers of the soil food web (top predatory nematodes), most likely through inducing changes in plant community composition and therefore the quality of resource input to the soil. The secondary consumers of the soil food web (microbe‐feeding nematodes) were, however, unresponsive. The fact that some trophic levels of the soil food web but not others responded to aboveground manipulations is explicable in terms of top‐down and bottom‐up forces differentially regulating different belowground trophic levels. Addition of aphids also influenced microbial community structure, promoted soil bacteria at the expense of fungi, and enhanced the diversity of herbivorous nematodes; in all cases these effects were at least partially reversed by addition of Micromus. These results in tandem point to upper level consumers in aboveground food webs as a potential driver of the belowground subsystem, and provide evidence that predator‐induced trophic cascades aboveground can have effects that trickle through soil food webs.     

Omnivores as plant bodyguards—A model of the importance of plant quality

The importance of omnivores in ecological systems is increasingly being recognized, not least due to their intensified use as biocontrol agents in crop production. We model a simple plant–herbivore–omnivore (predator) system to explore the effects of plant suitability as food for omnivores on the outcome of omnivore–herbivore interactions. The model predicts that increasing plant suitability relative to herbivore suitability for the omnivore will catalyze the extinction of herbivores or omnivores, depending on the relative growth rate of omnivores feeding solely on plants or herbivores. When omnivore growth is higher on plants, either the omnivore or the herbivore goes extinct. When omnivore growth is higher on herbivores, the possible consequences are extinction, stable coexistence, and limit cycles, depending on the combination of species properties. Our results suggest that plants in some situations may evolve towards becoming more suitable to omnivores to escape detrimental herbivores and that breeders could manipulate crop suitability to omnivore species to reach a desired outcome of omnivore–herbivore interactions.