Vertebrate predators have minimal cascading effects on plant production or seed predation in an intact grassland ecosystem

The strength of trophic cascades in terrestrial habitats has been the subject of considerable interest and debate. We conducted an 8-year experiment to determine how exclusion of vertebrate predators, ungulates alone (to control for ungulate exclusion from predator exclusion plots) or none of these animals influenced how strongly a three-species assemblage of rodent consumers affected plant productivity. We also examined whether predator exclusion influenced the magnitude of post-dispersal seed predation by mice. Both ungulates and rodents had strong direct effects on graminoid biomass. However, rodent impacts on plant biomass did not differ across plots with or without predators and/or ungulates. Deer mice removed more seeds from seed depots on predator exclusion plots, suggesting trait-mediated indirect effects of predators, but this short-term behavioural response did not translate into longer-term impacts on seed survival. These results suggest that vertebrate predators do not fundamentally influence primary production or seed survival in our system.     

Invasive species cause large-scale loss of native California oyster habitat by disrupting trophic cascades

Although invasive species often resemble their native counterparts, differences in their foraging and anti-predator strategies may disrupt native food webs. In a California estuary, we showed that regions dominated by native crabs and native whelks have low mortality of native oysters (the basal prey), while regions dominated by invasive crabs and invasive whelks have high oyster mortality and are consequently losing a biologically diverse habitat. Using field experiments, we demonstrated that the invasive whelk’s distribution is causally related to a large-scale pattern of oyster mortality. To determine whether predator–prey interactions between crabs (top predators) and whelks (intermediate consumers) indirectly control the pattern of oyster mortality, we manipulated the presence and invasion status of the intermediate and top trophic levels in laboratory mesocosms. Our results show that native crabs indirectly maintain a portion of the estuary’s oyster habitat by both consuming native whelks (density-mediated trophic cascade) and altering their foraging behavior (trait-mediated trophic cascade). In contrast, invasive whelks are naive to crab predators and fail to avoid them, thereby inhibiting trait-mediated cascades and their invasion into areas with native crabs. Similarly, when native crabs are replaced with invasive crabs, the naive foraging strategy and smaller size of invasive crabs prevents them from efficiently consuming adult whelks, thereby inhibiting strong density-mediated cascades. Thus, while trophic cascades allow native crabs, whelks, and oysters to locally co-exist, the replacement of native crabs and whelks by functionally similar invasive species results in severe depletion of native oysters. As coastal systems become increasingly invaded, the mismatch of evolutionarily based strategies among predators and prey may lead to further losses of critical habitat that support marine biodiversity and ecosystem function. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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: the primacy of trait-mediated indirect interactions

Trophic cascades are textbook examples of predator indirect effects on ecological systems. Yet there is considerable debate about their nature, strength and overall importance. This debate stems in part from continued uncertainty about the ultimate mechanisms driving cascading effects. We present a synthesis of empirical evidence in support of one possible ultimate mechanism: the foraging‐predation risk trade‐offs undertaken by intermediary species. We show that simple trade‐off behaviour can lead to both positive and negative indirect effects of predators on plant resources and hence can explain considerable contingency on the nature and strength of cascading effects among systems. Thus, predicting the sign and strength of indirect effect simply requires knowledge of habitat and resource use by prey with regard to predators’ presence, habitat use and hunting mode. The synthesis allows us to postulate a hypothesis for new conceptualization of trophic cascades which is to be viewed as an ultimate trade‐off between intervening species. In this context, different predators apply different rules of engagement based on their hunting mode and habitat use. These different rules then determine whether behavioural effects persist or attenuate at the level of the food chain.     

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.     

Environmental gradients and the evolution of tri‐trophic interactions

Long‐standing theory predicts herbivores and predators should drive selection for increased plant defences, such as the specific production of volatile organic compounds for attracting predators near the site of damage. Along elevation gradients, a general pattern is that herbivores and predators are abundant at low elevation and progressively diminish at higher elevations. To determine whether plant adaptation along such a gradient influences top‐down control of herbivores, we manipulated soil predatory nematodes, root herbivore pressure and plant ecotypes in a reciprocal transplant experiment. Plant survival was significantly higher for low‐elevation plants, but only when in the presence of predatory nematodes. Using olfactometer bioassays, we showed correlated differential nematode attraction and plant ecotype‐specific variation in volatile production. This study not only provides an assessment of how elevation gradients modulate the strength of trophic cascades, but also demonstrates how habitat specialisation drives variation in the expression of indirect plant defences.     

Predator diversity enhances secondary production and decreases the likelihood of trophic cascades

We manipulated the diversity of top predators in a three trophic level marine food web. The food web included four top benthic marine fish predators (black goby, rock goby, sea scorpion and shore rockling), an intermediate trophic level of small fish, and a lower trophic level of benthic invertebrates. We kept predator density constant and monitored the response of the lower trophic levels. As top predator diversity increased, secondary production increased. We also observed that in the presence of the manipulated fish predators, the density of small gobiid fish (intermediate consumers) was suppressed, releasing certain groups of benthic invertebrates (caprellid amphipods, copepods, nematodes and spirorbid worms) from heavy intermediate predation pressure. We attribute the mechanism responsible for this trophic cascade to a trait-mediated indirect interaction, with the small gobiid fish changing their use of space in response to altered predator diversity. In the absence of top fish predators, a full-blown trophic cascade occurs. Therefore the diversity of predators reduces the likelihood of trophic cascades occurring and hence provides insurance against the loss of an important ecosystem function (i.e. secondary production).     

Top‐down and bottom‐up diversity cascades in detrital vs. living food webs

Apex predators and plant resources are both critical for maintaining diversity in biotic communities, but the indirect (‘cascading’) effects of top‐down and bottom‐up forces on diversity at different trophic levels are not well resolved in terrestrial systems. Manipulations of predators or resources can cause direct changes of diversity at one trophic level, which in turn can affect diversity at other trophic levels. The indirect diversity effects of resource and consumer variation should be strongest in aquatic systems, moderate in terrestrial systems, and weakest in decomposer food webs. We measured effects of top predators and plant resources on the diversity of endophytic animals in an understorey shrub Piper cenocladum (Piperaceae). Predators and resource availability had significant direct and indirect effects on the diversity of the endophytic animal community, but the effects were not interactive, nor were they consistent between living vs. detrital food webs. The addition of fourth trophic level beetle predators increased diversity of consumers supported by living plant tissue, whereas balanced plant resources (light and nutrients) increased the diversity of primary through tertiary consumers in the detrital resources food web. These results support the hypotheses that top‐down and bottom‐up diversity cascades occur in terrestrial systems, and that diversity is affected by different factors in living vs. detrital food webs.     

Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

1. Predator–prey interactions have traditionally focused on the consumptive effects that predators have on prey. However, predators can also reduce the abundance of prey through behaviourally‐mediated non‐consumptive effects. For example, pea aphids (Acyrthosiphon pisum Harris) drop from their host plants in response to the risk of attack, reducing population sizes as a consequence of lost feeding opportunities. 2. The objective of the present study was to determine whether the non‐consumptive effects of predators could extend to non‐prey herbivore populations as a result of non‐lethal incidental interactions between herbivores and foraging natural enemies. 3. Polyculture habitats consisting of green peach aphids (Myzus persicae Sulzer) feeding on collards and pea aphids feeding on fava beans were established in greenhouse cages. Aphidius colemani Viereck, a generalist parasitoid that attacks green peach aphids but not pea aphids, was released into half of the cages and the abundance of the non‐host pea aphid was assessed. 4. Parasitoids reduced the population growth of the non‐host pea aphid by increasing the frequency of defensive drops; but this effect was dependent on the presence of green peach aphids. 5. Parasitoids probably elicited the pea aphid dropping behaviour through physical contact with pea aphids while foraging for green peach aphids. It is unlikely that pea aphids were responding to volatile alarm chemicals emitted by green peach aphids in the presence of the parasitoid. 6. In conclusion, the escape response of the pea aphid provided the opportunity for a parasitoid to have non‐target effects on an herbivore with which it did not engage in a trophic interaction. The implication is that natural enemies with narrow diet breadths have the potential to influence the abundance of a broad range of prey and non‐prey species via non‐consumptive effects.     

Habitat effects on the relative importance of trait- and density-mediated indirect interactions

Classical views of trophic cascades emphasize the primacy of consumptive predator effects on prey populations to the transmission of indirect effects [density-mediated indirect interactions (DMIIs)]. However, trophic cascades can also emerge without changes in the density of interacting species because of non-consumptive predator effects on prey traits such as foraging behaviour [trait-mediated indirect interactions (TMIIs)]. Although ecologists appreciate this point, measurements of the relative importance of each indirect predator effect are rare. Experiments with a three-level, rocky shore food chain containing an invasive predatory crab ( Carcinus maenas ), an intermediate consumer (the snail, Nucella lapillus ) and a basal resource (the barnacle, Semibalanus balanoides ) revealed that the strength of TMIIs is comparable with, or exceeds, that of DMIIs. Moreover, the sign and strength of each indirect predator effect depends on whether it is measured in risky or refuge habitats. Because habitat shifts are often responsible for the emergence of TMIIs, attention to the sign and strength of these interactions in both habitats will improve our understanding of the link between individual behaviour and community dynamics.     

Colonisation rate and adaptive foraging control the emergence of trophic cascades

Ecological communities are assembled and sustained by colonisation. At the same time, predators make foraging decisions based on the local availabilities of potential resources, which reflects colonisation. We combined field and laboratory experiments with mathematical models to demonstrate that a feedback between these two processes determines emergent patterns in community structure. Namely, our results show that prey colonisation rate determines the strength of trophic cascades – a feature of virtually all ecosystems – by prompting behavioural shifts in adaptively foraging omnivorous fish predators. Communities experiencing higher colonisation rates were characterised by higher invertebrate prey and lower producer biomasses. Consequently, fish functioned as predators when colonisation rate was high, but as herbivores when colonisation rate was low. Human land use is changing habitat connectivity worldwide. A deeper quantitative understanding of how spatial processes modify individual behaviour, and how this scales to the community level, will be required to predict ecosystem responses to these changes.     

Sensory cues of a top‐predator indirectly control a reef fish mesopredator

Behavioural trophic cascades highlight the importance of indirect/risk effects in the maintenance of healthy trophic‐level links in complex ecosystems. However, there is limited understanding on how the loss of indirect top–down control can cascade through the food‐web to modify lower level predator–prey interactions. Using a reef fish food‐web, our study examines behavioural interactions among predators to assess how fear elicited by top‐predator cues (visual and chemical stimuli) can alter mesopredator behaviour and modify their interaction with resource prey. Under experimental conditions, the presence of any cue (visual, chemical, or both) from the top‐predator (coral trout Plectropomus leopardus) strongly restricted the distance swum, area explored and foraging activity of the mesopredator (dottyback Pseudochromis fuscus), while indirectly triggering a behavioural release of the resource prey (recruits of the damselfish Pomacentrus chrysurus). Interestingly, the presence of a large non‐predator species (thicklip wrasse Hemigymnus melapterus) also mediated the impact of the mesopredator on prey, as it provoked mesopredators to engage in an ‘inspection’ behaviour, while significantly reducing their feeding activity. Our study describes for the first time a three‐level behavioural cascade of coral reef fish and stresses the importance of indirect interactions in marine food‐webs.     

Non-lethal effects of predation in birds

Predators can affect individual fitness and population and community processes through lethal effects (direct consumption or ‘density’ effects), where prey is consumed, or through non‐lethal effects (trait‐mediated effects or interactions), where behavioural compensation to predation risk occurs, such as animals avoiding areas of high predation risk. Studies of invertebrates, fish and amphibians have shown that non‐lethal effects may be larger than lethal effects in determining the behaviour, condition, density and distribution of animals over a range of trophic levels. Although non‐lethal effects have been well described in the behavioural ecology of birds (and also mammals) within the context of anti‐predation behaviour, their role relative to lethal effects is probably underestimated. Birds show many behavioural and physiological changes to reduce direct mortality from predation and these are likely to have negative effects on other aspects of their fitness and population dynamics, as well as affecting the ecology of their own prey and their predators. As a consequence, the effects of predation in birds are best measured by trade‐offs between maximizing instantaneous survival in the presence of predators and acquiring or maintaining resources for long‐term survival or reproduction. Because avoiding predation imposes foraging costs, and foraging behaviour is relatively easy to measure in birds, the foraging–predation risk trade‐off is probably an effective framework for understanding the importance of non‐lethal effects, and so the population and community effects of predation risk in birds and other animals. Using a trade‐off approach allows us to predict better how changes in predator density will impact on population and community dynamics, and how animals perceive and respond to predation risk, when non‐lethal effects decouple the relationship between predator density and direct mortality rate. The trade‐off approach also allows us to identify where predation risk is structuring communities because of avoidance of predators, even when this results in no observable direct mortality rate.     

Interspecific differences in milkweeds alter predator density and the strength of trophic cascades

Trophic cascades occur when predators benefit plants by consuming herbivores, but the overall strength of a trophic cascade depends upon the way species interactions propagate through a system. For example, plant resistance to, or tolerance of, herbivores reduces the potential magnitude of a trophic cascade. At the same time, plants can also affect predator foraging or consumption in ways that either increase or decrease the strength of trophic cascades. In this study, we investigated the effects of plant variation on cascade strength by manipulating predator access to aphid populations on two species of milkweed: the slower-growing, putatively more-defended Asclepias syriaca and the faster-growing, putatively less-defended Asclepias incarnata. Predatory insects increased plant growth and survival for both species, but the strength of these trophic cascades was greater on A. incarnata, which supported more aphid growth early in the season than did A. syriaca. More predators were observed per aphid on A. incarnata, and cage treatments generated significant patterns consistent with predator aggregation on A. incarnata, but not A. syriaca. Although predators strongly affected aphids, this effect did not differ consistently between milkweed species. Plant tolerance to herbivory may therefore be the primary driver of the difference in trophic cascade strength observed. Importantly, we observed that the timing of predator exclusion affected plant growth and survival differently, indicating that measures of “cascade strength” may change with phenology and plant physiological responses. Together, our results suggest a mechanism by which differences in resource allocation patterns could explain differences in growth, phenology, and cascade strength between species.     

Does the strength of cross‐ecosystem trophic cascades vary with ecosystem size? A test using a natural microcosm

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Effects of the presence of a predatory fish and the phenotype of its prey (a shredding shrimp) on leaf litter decomposition

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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.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Strength of a Trophic Cascade Between an Apex Predator,Mammalian Herbivore and Grasses in a Desert Ecosystem Does Not Vary with Temporal Fluctuations in Primary Productivity

There has long been debate regarding the primacy of bottom-up and top-down effects as factors shaping ecosystems. The exploitation ecosystems hypothesis (EEH) predicts that predators indirectly benefit plants because their top-down effects limit herbivores’ consumption of plants, and that the strength of trophic cascade increases with increasing primary productivity. However, in arid environments, pulses of primary productivity produced by irregular rainfall events could decouple herbivore–plant and predator–prey dynamics if high conversion efficiency from seed biomass to consumers allows the rapid build-up of consumer populations. Here, we test predictions of the EEH in an arid environment. We measured activity/abundances of dingoes, red kangaroos and grasses, and diet of dingoes, in landscapes where dingoes were culled or not culled over 3 years. Dingo activity was correlated with rainfall, and their tracks were less frequent at culled sites. Kangaroo abundance was greater at sites where dingoes were culled and increased with rainfall in the previous 6 months. Grass cover was greater at sites where dingoes were not culled and increased with rainfall in the previous 3 months. During a period of average rainfall, dingoes primarily consumed rodents and increased their consumption of kangaroos during a period of drier conditions. Our results are consistent with the hypothesis that suppression of an apex predator triggers a trophic cascade, but are at odds with the EEH’s prediction that the magnitude of trophic cascades should increase with primary productivity. Our study demonstrates that temporal fluctuations in primary productivity can have effects on biomasses of plants and consumers which are in many ways analogous to those observed along spatial gradients of primary productivity.     

Effects of environmental warming and drought on size‐structured soil food webs

Soil systems maintain important ecosystem processes crucial for plant life and food production. Especially agricultural systems are strongly affected by climate change due to low vegetation cover associated with high temperatures and drought. Nevertheless, the response of soil systems to climate change is little explored. We used microcosms with a simplified soil community to address effects of climate change using independent temperature and dryness gradients and addressed their effects on top–down control and litter decomposition. The community consisted of maize litter as a basal resource, fungi, springtails and as top predators mites and centipedes. As the body‐size structure is of high importance for communities, we included differently‐sized springtails and predator species. After seven weeks, the experiment was terminated, and the impact of climate change on direct feeding interactions and indirect effects across trophic levels was analysed. With increasing temperature and dryness, consumption rates increased, thereby amplifying the negative influence of consumer populations on their resources. Hence, these climate‐change variables increased the top–down control of 1) predators (mainly mites) on springtails and 2) fungi on litter decomposition. In addition, we found that the climate‐change variables strengthened trophic cascades from predators on fungi whose density was thus increasingly decoupled from top–down control by their springtail consumers. Their increased decomposition rates are of high importance for carbon cycling and may result in accelerated nutrient turnover. In conclusion, our results suggest that climate change may strongly influence the structure and functioning of soil systems by strengthening consumption rates and trophic cascades, which will have far reaching consequences for the nutrient turnover and productivity of agricultural ecosystems.