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.     

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.     

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.     

Seasonal influence of brook trout and mottled sculpin on lower trophic levels in an Appalachian stream

1. In some situations fish have strong top‐down effects in stream communities while in others they seem to be relatively unimportant. Differences in the impact of fish may depend on a variety of factors including the foraging mode of the fish, interactions among fish species and temporal variation in environmental conditions and species interactions. 2. We investigated the effect of brook trout (Salvelinus fontinalis) and mottled sculpin (Cottus bairdi) on lower trophic levels in Appalachian streams and whether or not interactions between these fish changed their influence. Mesocosms were placed in a headwater stream in a randomized complete block design. Within blocks, mesocosms were randomly assigned to one of the following treatments: (i) no fish; (ii) sculpin only; (iii) trout only and (iv) both sculpin and trout. Fish biomass was the same in all three fish treatments. Invertebrate density and algal biomass in mesocosms were determined after 3 weeks. We repeated the experiment in the autumn, spring and summer to test for seasonality of fish effects. 3. The effect of fish on invertebrate assemblages was seasonal and depended on prey identity. Sculpin strongly suppressed grazer abundance in spring while trout had little effect on grazers in any season. The influence of both fish on insect predators was similar and relatively constant across seasons. We found little evidence of an interaction between sculpin and trout that strongly influenced their effect on prey across seasons. 4. None of the fish treatments influenced algal biomass during any of the seasons. Algal growth was also seasonal, with a two‐ to four‐fold increase in algal biomass in spring compared to autumn and summer. 5. Our results indicate that benthic and drift feeding fish differ in their effects on some, but not all prey. Furthermore, fish effects on prey were strongly seasonal for some, but not all prey types. While the temporal context is not commonly considered, our results indicate seasonality can be an important component of predator–prey interactions in streams.     

The biogeography of trophic cascades on US oyster reefs

Predators can indirectly benefit prey populations by suppressing mid‐trophic level consumers, but often the strength and outcome of trophic cascades are uncertain. We manipulated oyster reef communities to test the generality of potential causal factors across a 1000‐km region. Densities of oyster consumers were weakly influenced by predators at all sites. In contrast, consumer foraging behaviour in the presence of predators varied considerably, and these behavioural effects altered the trophic cascade across space. Variability in the behavioural cascade was linked to regional gradients in oyster recruitment to and sediment accumulation on reefs. Specifically, asynchronous gradients in these factors influenced whether the benefits of suppressed consumer foraging on oyster recruits exceeded costs of sediment accumulation resulting from decreased consumer activity. Thus, although predation on consumers remains consistent, predator influences on behaviour do not; rather, they interact with environmental gradients to cause biogeographic variability in the net strength of trophic cascades.     

Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour

Although human-mediated extinctions disproportionately affect higher trophic levels, the ecosystem consequences of declining diversity are best known for plants and herbivores. We combined field surveys and experimental manipulations to examine the consequences of changing predator diversity for trophic cascades in kelp forests. In field surveys we found that predator diversity was negatively correlated with herbivore abundance and positively correlated with kelp abundance. To assess whether this relationship was causal, we manipulated predator richness in kelp mesocosms, and found that decreasing predator richness increased herbivore grazing, leading to a decrease in the biomass of the giant kelp Macrocystis. The presence of different predators caused different herbivores to alter their behaviour by reducing grazing, such that total grazing was lowest at highest predator diversity. Our results suggest that declining predator diversity can have cascading effects on community structure by reducing the abundance of key habitat-providing species.     

A cyanobacterial bloom prevents fish trophic cascades

1. We experimentally compared the impacts of visually feeding zooplanktivorous fish and filter‐feeding omnivorous fish in shallow tropical Dakar Bango reservoir, Senegal. We provoked a cyanobacterial Anabaena bloom under mesotrophic to eutrophic N‐limited conditions in 18 enclosures assigned to six Nile tilapia life‐stage treatments, at typical biomasses: fishless control (C), zooplanktivorous fry (Z), omnivorous juveniles (O), herbivorous fingerlings (H) and two combinations (OZ, OH). 2. All fish grew well, but as prevalent inedible phytoplankton dampened fish effects, community‐level trophic cascades did not occur. Planktivore types acted independently and affected differentially the biomasses of total zooplankton, cyclopoids, nauplii, cladocerans, invertebrate carnivores, large herbivores, colonial cyanobacteria and Chlorophyta. They neither influenced the total biomass of phytoplankton, nor most water chemistry characteristics. Responses were apparently not fish‐biomass related. The bloom collapsed synchronously in all enclosures, coinciding with enrichment ending, with a return to clear water within 12 days. 3. Our results support the hypothesis that excess nutrients and prevalent inedible cyanobacteria inhibit the cascading effects of natural biomass levels of both visually feeding zooplanktivores and filter‐feeding omnivores. In N‐limited meso‐eutrophic shallow tropical lakes with predominantly small herbivorous zooplankton, neither the type nor the biomass of planktivorous fish present seems likely to prevent the transient outburst of cyanobacterial blooms. Such fragile ecosystems may thus not sustain a trophic state suitable for drinking water production, unless human impacts are restricted. The generality of restoration approaches based on ecological engineering should be further explored.     

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).     

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.     

Multi-level trophic cascades in a heavily exploited open marine ecosystem

Anthropogenic disturbances intertwined with climatic changes can have a large impact on the upper trophic levels of marine ecosystems, which may cascade down the food web. So far it has been difficult to demonstrate multi-level trophic cascades in pelagic marine environments. Using field data collected during a 33-year period, we show for the first time a four-level community-wide trophic cascade in the open Baltic Sea. The dramatic reduction of the cod (Gadus morhua) population directly affected its main prey, the zooplanktivorous sprat (Sprattus sprattus), and indirectly the summer biomass of zooplankton and phytoplankton (top-down processes). Bottom-up processes and climate-hydrological forces had a weaker influence on sprat and zooplankton, whereas phytoplankton variation was explained solely by top-down mechanisms. Our results suggest that in order to dampen the occasionally harmful algal blooms of the Baltic, effort should be addressed not only to control anthropogenic nutrient inputs but also to preserve structure and functioning of higher trophic levels.     

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.     

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.     

Trophic cascades in tropical rainforests: Effects of vertebrate predator exclusion on arthropods and plants in Papua New Guinea

Insect herbivores have the potential to consume large amounts of plant tissue in tropical forests, but insectivorous vertebrates effectively control their abundances, indirectly increasing plant fitness accordingly. Despite several studies already sought understanding of the top-down effects on arthropod community structure and herbivory, such studies of trophic cascades in old tropics are underrepresented, and little attention was paid to top-down forces in various habitats. Therefore, we examine how flying insectivorous vertebrates (birds and bats) impact arthropods and, consequently, affect herbivore damage of leaves in forest habitats in Papua New Guinea. In a 3-month long predator exclosure experiment conducted at four study sites across varying elevation and successional stage, we found that vertebrate predators reduced arthropod density by ∼52%. In addition, vertebrate predators decreased the mean body size of arthropods by 26% in leaf chewers and 47% in non-herbivorous arthropods but had only a small effect on mesopredators and sap suckers. Overall, the exclusion of vertebrate predators resulted in a ~ 41% increase in leaf damage. Our results, across different types of tropical forests in Papua New Guinea, demonstrate that flying vertebrate insectivores have a crucial impact on plant biomass, create a selective pressure on larger and non-predatory prey individuals and they prey partition with mesopredators.     

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.     

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.     

Water temperature determines strength of top-down control in a stream food web

1. We examined effects of water temperature on the community structure of a three trophic level food chain (predatory fish, herbivorous caddisfly larvae and periphyton) in boreal streams. We used laboratory experiments to examine (i) the effects of water temperature on feeding activities of fish and caddisfly larvae and on periphyton productivity, to evaluate the thermal effects on each trophic level (species‐level experiment), and (ii) the effects of water temperature on predation pressure of fish on abundance of the lower trophic levels, to evaluate how temperature affects top‐down control by fish (community‐level experiment). 2. In the species‐level experiment, feeding activity of fish was high at 12 °C, which coincides with the mean summer temperature in forested streams of Hokkaido, Japan, but was depressed at 3 °C, which coincides with the mean winter temperature, and also above 18 °C, which coincides with the near maximum summer temperatures. Periphyton productivity increased over the range of water temperatures. 3. In the community‐level experiments, a top‐down effect of fish on the abundance of caddisfly larvae and periphyton was clear at 12 °C. This effect was not observed at 3 and 21 °C because of low predation pressure of fish at these temperatures. 4. These experiments revealed that trophic cascading effects may vary with temperature even in the presence of abundant predators. Physiological depression of predators because of thermal stress can alter top‐down control and lead to changes in community structure. 5. We suggest that thermal habitat alteration can change food web structure via combinations of direct and indirect trophic interactions.     

From lynx spiders to cotton: Behaviourally mediated predator effects over four trophic levels

Food web studies often examine density and behaviourally mediated effects of predators on herbivores, but are less likely to assess the plant targeted by the herbivore. We conducted a study that incorporated four trophic levels examining the effect of two generalist predators (damsel bugs, Nabis kinbergii Reuter; and lynx spiders, Oxyopes molarius L. Koch) on damage to cotton bolls caused by green mirids (Creontiades dilutus (Stål)). First we tested whether lynx spiders and damsel bugs could control mirid numbers and cotton boll damage in field cages. We found that in cages containing mirids and only lynx spiders, lynx spiders reduced both mirid numbers and boll damage. However, in cages which contained mirids and both predators (lynx spiders and damsel bugs) only mirid numbers were reduced. To explain the negative effect of damsel bugs on boll damage, we examined the interactions between lynx spiders, damsel bugs and mirids. We found that lynx spiders were better mirid predators than damsel bugs, and that lynx spiders attacked damsel bugs, but not vice versa. Behaviourally, mirids responded to increasing predator pressure regardless of whether the predators were lynx spiders or damsel bugs. However, damsel bugs seemed to alter the behaviour of lynx spiders because in their presence, a higher proportion of lynx spiders moved to the top of the plant, towards the damsel bugs but away from the bolls found lower on the plant. These results suggest that the most likely explanation for the increase in boll damage in the presence of damsel bugs was that lynx spiders moved to the top of the plant in the presence of damsel bugs, which then exposed the bolls lower down on the plant to mirid attack. This work emphasizes the importance of behaviourally mediated effects in food webs extending over four trophic levels.     

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.     

Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades

Single trophic‐level studies of the relationship between biodiversity and ecosystem functioning highlight the importance of mechanisms such as resource partitioning, facilitation, and sampling effect. In a multi‐trophic context, trophic interactions such as intraguild predation may also be an important mediator of this relationship. Using a salt‐marsh food web, we investigated the interactive effects of predator species richness (one to three species) and trophic composition (strict predators, intraguild predators, or a mixture of the two) on ecosystem functions such as prey suppression and primary production via trophic cascades. We found that the trophic composition of the predator assemblage determined the impact of increasing predator species richness on the occurrence of trophic cascades. In addition, increasing the proportion of intraguild predator species present diminished herbivore suppression and reduced primary productivity. Therefore, trophic composition of the predator assemblage can play an important role in determining the nature of the relationship between predator diversity and ecosystem function.