A cross-ecosystem comparison of the strength of trophic cascades

Although trophic cascades (indirect effects of predators on plants via herbivores) occur in a wide variety of food webs, the magnitudes of their effects are often quite variable. We compared the responses of herbivore and plant communities to predator manipulations in 102 field experiments in six different ecosystems: lentic (lake and pond), marine, and stream benthos, lentic and marine plankton, and terrestrial (grasslands and agricultural fields). Predator effects varied considerably among systems and were strongest in lentic and marine benthos and weakest in marine plankton and terrestrial food webs. Predator effects on herbivores were generally larger and more variable than on plants, suggesting that cascades often become attenuated at the plant–herbivore interface. Top‐down control of plant biomass was stronger in water than on land; however, the differences among the five aquatic food webs were as great as those between wet and dry systems.     

Subsidy hypothesis and strength of trophic cascades across ecosystems

Ecosystems are differentially open to subsidies of energy, material and organisms. This fundamental ecosystem attribute has long been recognized but the influence of this property on community regulation has not been investigated. We propose that this environmental attribute may explain variation in the strength of trophic cascades among ecosystems. Simply because of gravity, we should predict that systems with convex profiles receive low amounts of subsidies whereas systems with concave profiles act as spatial attractors, and receive high amounts of subsidies. The subsidy hypothesis states that ecosystems with high amounts of allochthonous inputs will experience the strongest trophic cascades. To test this hypothesis, we derive ecosystem models and investigate the effect of location and magnitude of subsidies on the strength of trophic cascades. Predictions from our models support the subsidy hypothesis and highlight the need to consider ecosystems as open to allochthonous flows.     

Ecological factors associated with the strength of trophic cascades in streams

Trophic cascades are extensively documented in nature, but they are also known to vary widely in strength and frequency across ecosystems. Therefore, much effort has gone into understanding which ecological factors generate variation in cascade strength. To identify which factors covary with the strength of cascades in streams, we performed a concurrent experiment across 17 streams throughout the Sierra Nevada Mountains. We eliminated top consumers from experimental substrates using electrical exclusions and compared the strength of indirect effects of consumers on the biomass of primary producers relative to control patches. In each stream we 1) classified the dominant invertebrate herbivores according to life‐history traits that influence their susceptibility to predators, 2) determined the abundance and diversity of algae and herbivores, and 3) measured production‐to‐biomass ratios (P:B) of the stream biofilm. This allowed us to assess three common predictions about factors thought to influence the strength of trophic cascades: cascade strength 1) is weaker in systems dominated by herbivores with greater ability to evade or defend against predators, 2) is stronger in systems characterized by low species diversity, and 3) increases with increasing producer P:B. When averaged across all streams, the indirect effect of predators increased the biomass of periphyton by a mean 60%. However, impacts of predators on algae varied widely, ranging from effects that exacerbated algal loss to herbivores, to strong cascades that increased algal biomass by 4.35 times. Cascade strength was not related to herbivore traits or species diversity, but decreased significantly with increasing algal diversity and biofilm P:B in a stream. Partial regression analyses suggested that the relationship between cascade strength and algal diversity was spurious, and that the only significant covariate after statistically controlling for cross‐correlations was algal P:B. Our study contributes to the ongoing debate about why trophic cascade strength varies in nature and is useful because it eliminates factors that have no potential to explain variation in cascades within these stream ecosystems.     

Predation on mutualists can reduce the strength of trophic cascades

Ecologists have put forth several mechanisms to predict the strength of predator effects on producers (a trophic cascade). We suggest a novel mechanism – in systems in which mutualists of plants are present and important, predators can have indirect negative effects on producers through their consumption of mutualists. The strength of predator effects on producers will depend on their relative consumption of mutualists and antagonists, and on the relative importance of each to producer population dynamics. In a meta-analysis of experiments that examine the effects of predator reduction on the pollination and reproductive success of plants, we found that the indirect negative effects of predators on plants are quite strong. Most predator removal experiments measure the strength of predator effects on producers through the antagonist pathway; we suggest that a more complete understanding of the role of predators will be achieved by simultaneously considering the effects of predators on plant mutualists.     

Interspecific differences in antipredator strategies determine the strength of non‐consumptive predator effects on stream detritivores

Animal species differ considerably in their response to predation risks. Interspecific variability in prey behaviour and morphology can alter cascading effects of predators on ecosystem structure and functioning. We tested whether species‐specific morphological defenses may affect responses of leaf litter consuming invertebrate prey to sit‐and‐wait predators, the odonate Cordulegaster boltonii larvae, in aquatic food webs. Partly or completely blocking the predator mouthparts (mandibles and/or extensible labium), thus eliminating consumptive (i.e. lethal) predator effects, we created a gradient of predator‐prey interaction intensities (no predator < predator – no attack < predator – non‐lethal attacks < lethal predator). A field experiment was first used to assess both consumptive and non‐consumptive predator effects on leaf litter decomposition and prey abundances. Laboratory microcosms were then used to examine behavioural responses of armored and non‐armored prey to predation risk and their consequences on litter decomposition. Results show that armored and non‐armored prey responded to both acute (predator – non‐lethal attacks) and chronic (predator – no attack) predation risks. Acute predation risk had stronger effects on litter decomposition, prey feeding rate and prey habitat use than predator presence alone (chronic predation risk). Predator presence induced a reduction in feeding activity (i.e. resource consumption) of both prey types but a shift to predator‐free habitat patches in non‐armored detritivores only. Non‐consumptive predator effects on prey subsequently decreased litter decomposition rate. Species‐specific prey morphological defenses and behaviour should thus be considered when studying non‐consumptive predator effects on prey community structure and ecosystem functioning.     

Strong seasonality may attenuate trophic cascades: vertebrate predator exclusion in boreal grassland

We studied the indirect effects of vertebrate predator exclusion on plant communities in boreal grassland in western Finland to find out whether the removal of the top trophic level would result in a trophic cascade. Predators were excluded from 1996 to 2000 by eight predator-proof fences (each 0.5 ha) constructed on old fields. Despite a major increase in vole densities, the expected trophic cascade attenuated rapidly so that the indirect effects of predator exclusion were restricted to a few plant species. The cause for the rapid attenuation of the trophic cascade appeared to be strong seasonality, as peak densities of voles were attained at the end of the growing season of vegetation, and vole populations declined before the next growing season so that the herbivory pressure during the growing season remained low or moderate. Accordingly, most plants escaped the heaviest grazing pressure either in time (plants completed their reproduction and withered before winter) or in space (living parts hidden under frozen ground and ice). However, heavy winter herbivory reduced the biomass of available vegetation and killed woody species (willows) at vole peaks, which implies that predator exclusion may have a strong effect on secondary succession. During summer, voles reduced the coverage of only a few preferred food plants ( Elymus repens , Phleum pratense , Vicia cracca ). Voles also maintained annual and biennial species in the community by creating gaps in the closed vegetation. We conclude that abiotic factors (harsh winter conditions) limited peak numbers of herbivores below a threshold density where herbivores could have caused a community-level decline in the biomass of herbaceous plants during summer.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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Diurnal bottom feeding of predator fish strengthens trophic cascades to benthic algae in experimental flow-through pools

Mechanisms that determine the strength of trophic cascades from fish to benthic algae via algivorous invertebrates in stream communities have not been clarified. Using seven fish species, we tested the hypothesis that the interspecific variation of predatory behavior of fishes affects the strength of trophic cascades in experimental streams. One or two species of fish were introduced into flow-through pools of 2.5 m² and the abundances of benthic invertebrates and algae were monitored. Pike gudgeon, a diurnal benthic feeder, triggered a strong trophic cascade but masu salmon, a diurnal drift feeder, did not have a cascading effect. Japanese dace, which is both a diurnal benthic and drift feeder, increased the algal biomass, but the nocturnal benthic feeder cut-tailed bullhead had little cascading effect. The diurnal benthic feeder silver crucian carp also had a cascading effect, but no trophic cascade was triggered either by Asian pond loach or by Japanese common catfish, both of which are nocturnal benthic feeders. Thus, diurnal benthic fish exerted a stronger cascading effect than diurnal drift feeders or nocturnal fish. The combination of two fish species enhanced the per-capita strength of trophic cascades, probably because one of the two species, the benthic feeder, preyed on more invertebrates than in the single-species pools.     

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.     

Morphological drivers of trophic cascades

Worldwide, local anthropogenic extinctions have recently been reported to induce trophic cascades, defined as perturbations of top consumers that propagate along food chains down to primary producers. This focus on the effects of top‐consumer extinction (i.e. of species presence) ignores potential cascading effects of the rapid morphological changes that may precede extinction. Here, we show in an experimental, three‐level food chain including medaka fish, herbivorous zooplankton and unicellular algae that varying body length of a single fish from large (36.3 mm) to small (11.5 mm) induced a stronger trophic cascade than varying an average‐sized (23.8 mm) fish from being present to absent. The strength of fish predation on zooplankton scaled quasi linearly (not with a power exponent) with fish body length and associated gape width, suggesting that the resultant trophic cascade was morphology (not metabolism)‐dependent. The effect of fish body length was stronger on phyto‐ than on zooplankton, because large‐sized fish had the unique ability to suppress large‐sized herbivores, which in turn had high grazing capacities. Hence, our results show that consumer body size, by setting diet breadth, can both drive and magnify the strength of trophic cascades. In contrast, fish body shape had no significant effect on fish predatory performances when its allometric component (the effect of size on shape) was removed. In the wild, human‐induced body downsizing of top consumers is widespread, and mitigating the resultant perturbations to ecosystem function and services will require a paradigm shift from preserving species presence towards preserving species size structure.     

Leading indicators of trophic cascades

Regime shifts are large, long-lasting changes in ecosystems. They are often hard to predict but may have leading indicators which are detectable in advance. Potential leading indicators include wider swings in dynamics of key ecosystem variables, slower return rates after perturbation and shift of variance towards lower frequencies. We evaluated these indicators using a food web model calibrated to long-term whole-lake experiments. We investigated whether impending regime shifts driven by gradual increase in exploitation of the top predator can create signals that cascade through food webs and be discerned in phytoplankton. Substantial changes in standard deviations, return rates and spectra occurred near the switch point, even two trophic levels removed from the regime shift in fishes. Signals of regime shift can be detected well in advance, if the driver of the regime shift changes much more slowly than the dynamics of key ecosystem variables which can be sampled frequently enough to measure the indicators. However, the regime shift may occur long after the driver has passed the critical point, because of very slow transient dynamics near the critical point. Thus, the ecosystem can be poised for regime shift by the time the signal is discernible. Field tests are needed to evaluate these indicators.     

Effects of individual differences in foraging of pale chub on algal biomass through trophic cascades

The foraging behavior of pale chub, Zacco platypus in experimental ponds was observed and the fish were classified according to whether they predominantly employed near-bed cruising and bottom feeding (type B) or whether they exhibited sit-and-wait and near-surface cruising, with occasional drift and surface feeding (type S). Fish that exhibited both behaviors were classified as type I. The effects of pale chub on trophic cascades were examined in pools into which river water was pumped. Twenty pools were assigned to four treatments and contained either no fish, or six pale chub of type B, or of type I, or of type S. Fish behavior was consistent throughout the experiments, and was not related to body length or sex. All types of pale chub predominantly preyed on invertebrates, but type B consumed more benthic algae than did type S. The algal biomass in pools with types S and I was greater than that in pools without pale chub as a result of trophic cascades. In pools with type B fish, the number of algal-grazing invertebrates on the upper surface of tiles was reduced as in pools with types S and I, but algal biomass did not increase because of direct grazing by type B fish. The mechanisms of reduction of algal-grazing invertebrates were different between types B and S; type S predominantly preyed on invertebrates in the water current, whereas type B preyed on and threatened invertebrates on the upper surface of tiles and removed them. Individual differences in foraging mode had significant effects on the mechanism of trophic cascades.     

Differences in prey personality mediate trophic cascades

Functional trait approaches in ecology chiefly assume the mean trait value of a population adequately predicts the outcome of species interactions. Yet this assumption ignores substantial trait variation among individuals within a population, which can have a profound effect on community structure and function. We explored individual trait variation through the lens of animal personality to test whether among‐individual variation in prey behavior mediates trophic interactions. We quantified the structure of personalities within a population of generalist grasshoppers and examined, through a number of field and laboratory‐based experiments, how personality types could impact tri‐trophic interactions in a food chain. Unlike other studies of this nature, we used spatial habitat domains to evaluate how personality types mechanistically map to behaviors relevant in predator–prey dynamics and found shy and bold individuals differed in both their habitat use and foraging strategy under predation risk by a sit‐and‐wait spider predator. In the field‐based mesocosm portion of our study, we found experimental populations of personality types differed in their trophic impact, demonstrating that prey personality can mediate trophic cascades. We found no differences in respiration rates or body size between personality types used in the mesocosm experiment, indicating relative differences in trophic impact were not due to variation in prey physiology but rather variation in behavioral strategies. Our work demonstrates how embracing the complexity of individual trait variation can offer mechanistically richer understanding of the processes underlying trophic interactions.     

Understanding patterns and processes in models of trophic cascades

Climate fluctuations and human exploitation are causing global changes in nutrient enrichment of terrestrial and aquatic ecosystems and declining abundances of apex predators. The resulting trophic cascades have had profound effects on food webs, leading to significant economic and societal consequences. However, the strength of cascades–that is the extent to which a disturbance is diminished as it propagates through a food web–varies widely between ecosystems, and there is no formal theory as to why this should be so. Some food chain models reproduce cascade effects seen in nature, but to what extent is this dependent on their formulation? We show that inclusion of processes represented mathematically as density‐dependent regulation of either consumer uptake or mortality rates is necessary for the generation of realistic ‘top‐down’ cascades in simple food chain models. Realistically modelled ‘bottom‐up’ cascades, caused by changing nutrient input, are also dependent on the inclusion of density dependence, but especially on mortality regulation as a caricature of, e.g. disease and parasite dynamics or intraguild predation. We show that our conclusions, based on simple food chains, transfer to a more complex marine food web model in which cascades are induced by varying river nutrient inputs or fish harvesting rates.     

Intraspecific difference among herbivore lineages and their host‐plant specialization drive the strength of trophic cascades

Trophic cascades – the indirect effect of predators on non‐adjacent lower trophic levels – are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences trophic cascade strength in a terrestrial tri‐trophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores’ lineage and host‐plant specialization but are not associated with density‐dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of trophic cascade strength and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi‐trophic interactions.     

Trophic cascades and trophic trickles in pelagic food webs

Prey-dependent models, with the predation rate (per predator) a function of prey numbers alone, predict the existence of a trophic cascade. In a trophic cascade, the addition of a top predator to a two-level food chain to make a three-level food chain will lead to increases in the population size of the primary producers, and the addition of nutrients to three-level chains will lead to increases in the population numbers at only the first and third trophic levels. In contrast, ratio-dependent models, with the predation rate (per predator) dependent on the ratio of predator numbers to prey, predict that additions of top predators will not increase the population sizes of the primary producers, and that the addition of nutrients to a three-level food chain will lead to increases in population numbers at all trophic levels. Surprisingly, recent meta-analyses show that freshwater pelagic food web patterns match neither prey-dependent models (in pelagic webs, ''prey'' are phytoplankton, and ''predators'' are zooplankton), nor ratio-dependent models. In this paper we use a modification of the prey-dependent model, incorporating strong interference within the zooplankton trophic level, that does yield patterns matching those found in nature. This zooplankton interference model corresponds to a more reticulate food web than in the linear, prey-dependent model, which lacks zooplankton interference. We thus reconcile data with a new model, and make the testable prediction that the strength of trophic cascades will depend on the degree of heterogeneity in the zooplankton level of the food chain.     

Compensation masks trophic cascades in complex food webs

Ecological networks, or food webs, describe the feeding relationships between interacting species within an ecosystem. Understanding how the complexity of these networks influences their response to changing top-down control is a central challenge in ecology. Here, we provide a model-based investigation of trophic cascades — an oft-studied ecological phenomenon that occurs when changes in the biomass of top predators indirectly effect changes in the biomass of primary producers — in complex food webs that are representative of the structure of real ecosystems. Our results reveal that strong cascades occur primarily in low richness and weakly connected food webs, a result in agreement with some prior predictions. The primary mechanism underlying weak or absent cascades was a strong compensatory response; in most webs, predators induced large population level cascades that were masked by changes in the opposite direction by other species in the same trophic guild. Thus, the search for a general theory of trophic cascades in food webs should focus on uncovering features of real ecosystems that promote biomass compensation within functional guilds or trophic levels.     

Predator personality structures prey communities and trophic cascades

Intraspecific variation is central to our understanding of evolution and population ecology, yet its consequences for community ecology are poorly understood. Animal personality – consistent individual differences in suites of behaviours – may be particularly important for trophic dynamics, where predator personality can determine activity rates and patterns of attack. We used mesocosms with aquatic food webs in which the top predator (dragonfly nymphs) varied in activity and subsequent attack rates on zooplankton, and tested the effects of predator personality. We found support for four hypotheses: (1) active predators disproportionately reduce the abundance of prey, (2) active predators select for predator‐resistant prey species, (3) active predators strengthen trophic cascades (increase phytoplankton abundance) and (4) active predators are more likely to cannibalise one another, weakening all other trends when at high densities. These results suggest that intraspecific variation in predator personality is an important determinant of prey abundance, community composition and trophic cascades.     

Biogeographic differences between native and non-native populations of crayfish alter species coexistence and trophic interactions in mesocosms

Biogeographical comparisons of native and non-native populations allow researchers to understand the degree to which traits contributing to invasion success are intrinsic or change during the invasion process. Here, we investigate whether traits underlying interspecific competition change following invasion and whether these alter the impacts of two crayfish congeners that have invaded into each other’s native ranges. Specifically, we compared native and non-native populations of rusty (Faxonius rusticus) and virile crayfish (F. virilis). We compared native and non-native populations of each species using laboratory assays to examine aggression and large mesocosms with the congeners in sympatry to examine growth and survival as well as impacts on lower trophic levels. We found that non-native virile crayfish were more aggressive in response to a threat than native virile crayfish and exhibited greater growth and survival in sympatry with rusty crayfish. These intraspecific differences were large enough to alter coexistence between species in the mesocosm experiment, which is consistent with patterns of coexistence between these species in the field. We did not observe differences in traits between native and non-native rusty crayfish, but rusty crayfish were consistently competitively dominant over virile crayfish in paired laboratory assays. Non-native populations of both species had greater impacts on lower trophic levels than native populations. Taken together, these findings provide new evidence that trait changes during invasions may enhance ecological impacts of invasive animals and their ability to compete with closely related native species.