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1.  Noncrop flowering plants restore top-down herbivore control in agricultural fields 
Ecology and Evolution  2013;3(8):2634-2646.
Herbivore populations are regulated by bottom-up control through food availability and quality and by top-down control through natural enemies. Intensive agricultural monocultures provide abundant food to specialized herbivores and at the same time negatively impact natural enemies because monocultures are depauperate in carbohydrate food sources required by many natural enemies. As a consequence, herbivores are released from both types of control. Diversifying intensive cropping systems with flowering plants that provide nutritional resources to natural enemies may enhance top-down control and contribute to natural herbivore regulation. We analyzed how noncrop flowering plants planted as “companion plants” inside cabbage (Brassica oleracea) fields and as margins along the fields affect the plant–herbivore–parasitoid–predator food web. We combined molecular analyses quantifying parasitism of herbivore eggs and larvae with molecular predator gut content analysis and a comprehensive predator community assessment. Planting cornflowers (Centaurea cynanus), which have been shown to attract and selectively benefit Microplitis mediator, a larval parasitoid of the cabbage moth Mamestra brassicae, between the cabbage heads shifted the balance between trophic levels. Companion plants significantly increased parasitism of herbivores by larval parasitoids and predation on herbivore eggs. They furthermore significantly affected predator species richness. These effects were present despite the different treatments being close relative to the parasitoids’ mobility. These findings demonstrate that habitat manipulation can restore top-down herbivore control in intensive crops if the right resources are added. This is important because increased natural control reduces the need for pesticide input in intensive agricultural settings, with cascading positive effects on general biodiversity and the environment. Companion plants thus increase biodiversity both directly, by introducing new habitats and resources for other species, and indirectly by reducing mortality of nontarget species due to pesticides.
This study provides a comprehensive assessment of how habitat manipulation affects biocontrol services of a natural enemy community including both parasitoids and generalist predators. The trophic interactions between pests, parasitoids and predators were determined to achieve a better systemic understanding of top-down herbivore control, which can be strengthened when natural enemies complement each other or dampened by intraguild interactions. Our approach to selectively enhance the third trophic level to counteract specific herbivores was successful for both predators and parasitoids. Our results show significant positive effects of companion plants on predation of pest eggs and parasitism of pest larvae. Importantly, our data also suggest that carabids, staphylinids and spiders do not substantially interfere with parasitoid biocontrol as parasitoid DNA was rarely detected in predator guts.
PMCID: PMC3930038  PMID: 24567828
Biodiversity; Brassica oleracea; cabbage; companion plants; floral subsidies; natural enemies; parasitoids; predators; trophic interactions; wildflower strips
2.  Within-Plant Bottom-Up Effects Mediate Non-Consumptive Impacts of Top-Down Control of Soybean Aphids 
PLoS ONE  2013;8(2):e56394.
There is increasing evidence that top-down controls have strong non-consumptive effects on herbivore populations. However, little is known about how these non-consumptive effects relate to bottom-up influences. Using a series of field trials, we tested how changes in top-down and bottom-up controls at the within-plant scale interact to increase herbivore suppression. In the first experiment, we manipulated access of natural populations of predators (primarily lady beetles) to controlled numbers of A. glycines on upper (i.e. vigorous-growing) versus lower (i.e. slow-growing) soybean nodes and under contrasting plant ages. In a second experiment, we measured aphid dispersion in response to predation. Bottom-up and top-down controls had additive effects on A. glycines population growth. Plant age and within-plant quality had significant bottom-up effects on aphid size and population growth. However, top-down control was the dominant force suppressing aphid population growth, and completely counteracted bottom-up effects at the plant and within-plant scales. The intensity of predation was higher on upper than lower soybean nodes, and resulted in a non-consumptive reduction in aphid population growth because most of the surviving aphids were located on lower plant nodes, where rates of increase were reduced. No effects of predation on aphid dispersal among plants were detected, suggesting an absence of predator avoidance behavior by A. glycines. Our results revealed significant non-consumptive predator impacts on aphids due to the asymmetric intensity of predation at the within-plant scale, suggesting that low numbers of predators are highly effective at suppressing aphid populations.
PMCID: PMC3576406  PMID: 23431373
3.  New England Salt Marsh Recovery: Opportunistic Colonization of an Invasive Species and Its Non-Consumptive Effects 
PLoS ONE  2013;8(8):e73823.
Predator depletion on Cape Cod (USA) has released the herbivorous crab Sesarmareticulatum from predator control leading to the loss of cordgrass from salt marsh creek banks. After more than three decades of die-off, cordgrass is recovering at heavily damaged sites coincident with the invasion of green crabs (Carcinusmaenas) into intertidal Sesarma burrows. We hypothesized that Carcinus is dependent on Sesarma burrows for refuge from physical and biotic stress in the salt marsh intertidal and reduces Sesarma functional density and herbivory through consumptive and non-consumptive effects, mediated by both visual and olfactory cues. Our results reveal that in the intertidal zone of New England salt marshes, Carcinus are burrow dependent, Carcinus reduce Sesarma functional density and herbivory in die-off areas and Sesarma exhibit a generic avoidance response to large, predatory crustaceans. These results support recent suggestions that invasive Carcinus are playing a role in the recovery of New England salt marshes and assertions that invasive species can play positive roles outside of their native ranges.
PMCID: PMC3756972  PMID: 24009763
4.  Herbivore release through cascading risk effects 
Biology Letters  2009;5(6):773-776.
Predators influence prey through consumption, and through trait-mediated effects such as emigration in response to predation risk (risk effects). We studied top-down effects of (sub-) adult wolf spiders (Lycosidae) on arthropods in a meadow. We compared risk effects with the overall top-down effect (including consumption) by gluing the chelicers of wolf spiders to prevent them from killing the prey. In a field experiment, we created three treatments that included either: (i) intact (‘predation’) wolf spiders; (ii) wolf spiders with glued chelicers (‘risk spiders’); or (iii) no (sub-) adult wolf spiders. Young wolf spiders were reduced by their (sub-) adult congeners. Densities of sheetweb spiders (Linyphiidae), a known intraguild prey of wolf spiders, were equally reduced by the presence of risk and predation wolf spiders. Plant- and leafhoppers (Auchenorrhyncha) showed the inverse pattern of higher densities in the presence of both risk and predation wolf spiders. We conclude that (sub-) adult wolf spiders acted as top predators, which reduced densities of intermediate predators and thereby enhanced herbivores. Complementary to earlier studies that found trait-mediated herbivore suppression, our results demonstrate that herbivores can be enhanced through cascading risk effects by top predators.
PMCID: PMC2827993  PMID: 19586964
Araneae; Auchenorrhyncha; conservation biological control; predation risk; trait-mediated effect; trophic cascade
5.  Herbivory Drives the Spread of Salt Marsh Die-Off 
PLoS ONE  2014;9(3):e92916.
Salt marsh die-off is a Western Atlantic conservation problem that has recently spread into Narragansett Bay, Rhode Island, USA. It has been hypothesized to be driven by: 1) eutrophication decreasing plant investment into belowground biomass causing plant collapse, 2) boat wakes eroding creek banks, 3) pollution or disease affecting plant health, 4) substrate hardness controlling herbivorous crab distributions and 5) trophic dysfunction releasing herbivorous crabs from predator control. To distinguish between these hypotheses we quantified these variables at 14 Narragansett Bay salt marshes where die-off intensity ranged from <5% to nearly 98%. Nitrogen availability, wave intensity and plant growth did not explain any variation in die-off. Herbivory explained 73% of inter-site variation in die-off and predator control of herbivores and substrate hardness also varied significantly with die-off. This suggests that salt marsh die-off is being largely driven by intense herbivory via the release of herbivorous crabs from predator control. Our results and those from other marsh systems suggest that consumer control may not simply be a factor to consider in marsh conservation, but with widespread predator depletion impacting near shore habitats globally, trophic dysfunction and runaway consumption may be the largest and most urgent management challenge for salt marsh conservation.
PMCID: PMC3961439  PMID: 24651837
6.  Revisiting the Role of Individual Variability in Population Persistence and Stability 
PLoS ONE  2013;8(8):e70576.
Populations often exhibit a pronounced degree of individual variability and this can be important when constructing ecological models. In this paper, we revisit the role of inter-individual variability in population persistence and stability under predation pressure. As a case study, we consider interactions between a structured population of zooplankton grazers and their predators. Unlike previous structured population models, which only consider variability of individuals according to the age or body size, we focus on physiological and behavioural structuring. We first experimentally demonstrate a high degree of variation of individual consumption rates in three dominant species of herbivorous copepods (Calanus finmarchicus, Calanus glacialis, Calanus euxinus) and show that this disparity implies a pronounced variation in the consumption capacities of individuals. Then we construct a parsimonious predator-prey model which takes into account the intra-population variability of prey individuals according to behavioural traits: effectively, each organism has a ‘personality’ of its own. Our modelling results show that structuring of prey according to their growth rate and vulnerability to predation can dampen predator-prey cycles and enhance persistence of a species, even if the resource stock for prey is unlimited. The main mechanism of efficient top-down regulation is shown to work by letting the prey population become dominated by less vulnerable individuals when predator densities are high, while the trait distribution recovers when the predator densities are low.
PMCID: PMC3732237  PMID: 23936450
7.  Predator Diversity Effects in an Exotic Freshwater Food Web 
PLoS ONE  2013;8(8):e72599.
Cascading trophic interactions are often defined as the indirect effects of a predator on primary producers through the effect of the predator on herbivores. These effects can be both direct through removal of herbivores [density-mediated indirect interactions (DMIIs)] or indirect through changes in the behavior of the herbivores [trait-mediated indirect interactions (TMIIs)]. How the relative importance of these two indirect interactions varies with predator diversity remains poorly understood. We tested the effect of predator diversity on both TMIIs and DMIIs on phytoplankton using two competitive invasive dreissenid mussel species (zebra mussel and quagga mussel) as the herbivores and combinations of one, two or all three species of the predators pumpkinseed sunfish, round goby, and rusty crayfish. Predators had either direct access to mussels and induced both TMII and DMII, or no direct access and induced only TMII through the presence of risk cues. In both sets of treatments, the predators induced a trophic cascade which resulted in more phytoplankton remaining with predators present than with only mussels present. The trophic cascade was weaker in three-predator and two-predator treatments than in one-predator treatments when predators had direct access to dreissenids (DMIIs and TMIIs). Crayfish had higher cascading effects on phytoplankton than both pumpkinseed and round goby. Increased predator diversity decreased the strength of DMIIs but had no effect on the strength of TMIIs. The strength of TMIIs was higher with zebra than quagga mussels. Our study suggests that inter-specific interference among predators in multi-species treatments weakens the consumptive cascading effects of predation on lower trophic levels whereas the importance of predator diversity on trait mediated effects depends on predator identity.
PMCID: PMC3749145  PMID: 23991126
8.  Eco-Evolutionary Trophic Dynamics: Loss of Top Predators Drives Trophic Evolution and Ecology of Prey 
PLoS ONE  2011;6(4):e18879.
Ecosystems are being altered on a global scale by the extirpation of top predators. The ecological effects of predator removal have been investigated widely; however, predator removal can also change natural selection acting on prey, resulting in contemporary evolution. Here we tested the role of predator removal on the contemporary evolution of trophic traits in prey. We utilized a historical introduction experiment where Trinidadian guppies (Poecilia reticulata) were relocated from a site with predatory fishes to a site lacking predators. To assess the trophic consequences of predator release, we linked individual morphology (cranial, jaw, and body) to foraging performance. Our results show that predator release caused an increase in guppy density and a “sharpening” of guppy trophic traits, which enhanced food consumption rates. Predator release appears to have shifted natural selection away from predator escape ability and towards resource acquisition ability. Related diet and mesocosm studies suggest that this shift enhances the impact of guppies on lower trophic levels in a fashion nuanced by the omnivorous feeding ecology of the species. We conclude that extirpation of top predators may commonly select for enhanced feeding performance in prey, with important cascading consequences for communities and ecosystems.
PMCID: PMC3079755  PMID: 21526156
9.  Predator Cue and Prey Density Interactively Influence Indirect Effects on Basal Resources in Intertidal Oyster Reefs 
PLoS ONE  2012;7(9):e44839.
Predators can influence prey abundance and traits by direct consumption, as well as by non-consumptive effects of visual, olfactory, or tactile cues. The strength of these non-consumptive effects (NCEs) can be influenced by a variety of factors, including predator foraging mode, temporal variation in predator cues, and the density of competing prey. Testing the relative importance of these factors for determining NCEs is critical to our understanding of predator-prey interactions in a variety of settings. We addressed this knowledge gap by conducting two mesocosm experiments in a tri-trophic intertidal oyster reef food web. More specifically, we tested how a predatory fish (hardhead catfish, Ariopsis felis) directly influenced their prey (mud crabs, Panopeus spp.) and indirectly affected basal resources (juvenile oysters, Crassostrea virginica), as well as whether these direct and indirect effects changed across a density gradient of competing prey. Per capita crab foraging rates were inversely influenced by crab density, but they were not affected by water-borne predator cues. As a result, direct consumptive effects on prey foraging rates were stronger than non-consumptive effects. In contrast, predator cue and crab density interactively influenced indirect predator effects on oyster mortality in two experiments, with trait-mediated and density-mediated effects of similar magnitude operating to enhance oyster abundance. Consistent differences between a variable predator cue environment and other predator cue treatments (no cue and constant cue) suggests that an understanding of the natural risk environment experienced by prey is critical to testing and interpreting trait-mediated indirect interactions. Further, the prey response to the risk environment may be highly dependent on prey density, particularly in prey populations with strong intra-specific interactions.
PMCID: PMC3436757  PMID: 22970316
10.  Intraguild relationships between sympatric predators exposed to lethal control: predator manipulation experiments 
Frontiers in Zoology  2013;10:39.
Terrestrial top-predators are expected to regulate and stabilise food webs through their consumptive and non-consumptive effects on sympatric mesopredators and prey. The lethal control of top-predators has therefore been predicted to inhibit top-predator function, generate the release of mesopredators and indirectly harm native fauna through trophic cascade effects. Understanding the outcomes of lethal control on interactions within terrestrial predator guilds is important for zoologists, conservation biologists and wildlife managers. However, few studies have the capacity to test these predictions experimentally, and no such studies have previously been conducted on the eclectic suite of native and exotic, mammalian and reptilian taxa we simultaneously assess. We conducted a series of landscape-scale, multi-year, manipulative experiments at nine sites spanning five ecosystem types across the Australian continental rangelands to investigate the responses of mesopredators (red foxes, feral cats and goannas) to contemporary poison-baiting programs intended to control top-predators (dingoes) for livestock protection.
Short-term behavioural releases of mesopredators were not apparent, and in almost all cases, the three mesopredators we assessed were in similar or greater abundance in unbaited areas relative to baited areas, with mesopredator abundance trends typically either uncorrelated or positively correlated with top-predator abundance trends over time. The exotic mammals and native reptile we assessed responded similarly (poorly) to top-predator population manipulation. This is because poison baits were taken by multiple target and non-target predators and top-predator populations quickly recovered to pre-control levels, thus reducing the overall impact of baiting on top-predators and averting a trophic cascade.
These results are in accord with other predator manipulation experiments conducted worldwide, and suggest that Australian populations of native prey fauna at lower trophic levels are unlikely to be negatively affected by contemporary dingo control practices through the release of mesopredators. We conclude that contemporary lethal control practices used on some top-predator populations do not produce the conditions required to generate positive responses from mesopredators. Functional relationships between sympatric terrestrial predators may not be altered by exposure to spatially and temporally sporadic application of non-selective lethal control.
PMCID: PMC3733732  PMID: 23842144
Canis lupus dingo; Dingo; European red fox; Felis catus; Feral cat; Mesopredator release; Monitor lizard; Poison baiting; Predator control; Trophic cascade; Varanus spp.; Vulpes vulpes
11.  Non-Linear Interactions between Consumers and Flow Determine the Probability of Plant Community Dominance on Maine Rocky Shores 
PLoS ONE  2013;8(8):e67625.
Although consumers can strongly influence community recovery from disturbance, few studies have explored the effects of consumer identity and density and how they may vary across abiotic gradients. On rocky shores in Maine, recent experiments suggest that recovery of plant- or animal- dominated community states is governed by rates of water movement and consumer pressure. To further elucidate the mechanisms of consumer control, we examined the species-specific and density-dependent effects of rocky shore consumers (crabs and snails) on community recovery under both high (mussel dominated) and low flow (plant dominated) conditions. By partitioning the direct impacts of predators (crabs) and grazers (snails) on community recovery across a flow gradient, we found that grazers, but not predators, are likely the primary agent of consumer control and that their impact is highly non-linear. Manipulating snail densities revealed that herbivorous and bull-dozing snails (Littorina littorea) alone can control recovery of high and low flow communities. After ∼1.5 years of recovery, snail density explained a significant amount of the variation in macroalgal coverage at low flow sites and also mussel recovery at high flow sites. These density-dependent grazer effects were were both non-linear and flow-dependent, with low abundance thresholds needed to suppress plant community recovery, and much higher levels needed to control mussel bed development. Our study suggests that consumer density and identity are key in regulating both plant and animal community recovery and that physical conditions can determine the functional forms of these consumer effects.
PMCID: PMC3734138  PMID: 23940510
12.  Trophic Complexity and the Adaptive Value of Damage-Induced Plant Volatiles 
PLoS Biology  2012;10(11):e1001437.
Indirect plant defenses are those facilitating the action of carnivores in ridding plants of their herbivorous consumers, as opposed to directly poisoning or repelling them. Of the numerous and diverse indirect defensive strategies employed by plants, inducible volatile production has garnered the most fascination among plant-insect ecologists. These volatile chemicals are emitted in response to feeding by herbivorous arthropods and serve to guide predators and parasitic wasps to their prey. Implicit in virtually all discussions of plant volatile-carnivore interactions is the premise that plants “call for help” to bodyguards that serve to boost plant fitness by limiting herbivore damage. This, by necessity, assumes a three-trophic level food chain where carnivores benefit plants, a theoretical framework that is conceptually tractable and convenient, but poorly depicts the complexity of food-web dynamics occurring in real communities. Recent work suggests that hyperparasitoids, top consumers acting from the fourth trophic level, exploit the same plant volatile cues used by third trophic level carnivores. Further, hyperparasitoids shift their foraging preferences, specifically cueing in to the odor profile of a plant being damaged by a parasitized herbivore that contains their host compared with damage from an unparasitized herbivore. If this outcome is broadly representative of plant-insect food webs at large, it suggests that damage-induced volatiles may not always be beneficial to plants with major implications for the evolution of anti-herbivore defense and manipulating plant traits to improve biological control in agricultural crops.
PMCID: PMC3507926  PMID: 23209381
13.  Contrasting Effects of Different Mammalian Herbivores on Sagebrush Plant Communities 
PLoS ONE  2015;10(2):e0118016.
Herbivory by both grazing and browsing ungulates shapes the structure and functioning of terrestrial ecosystems worldwide, and both types of herbivory have been implicated in major ecosystem state changes. Despite the ecological consequences of differences in diets and feeding habits among herbivores, studies that experimentally distinguish effects of grazing from spatially co-occurring, but temporally segregated browsing are extremely rare. Here we use a set of long-term exclosures in northern Utah, USA, to determine how domestic grazers vs. wild ungulate herbivores (including browsers and mixed feeders) affect sagebrush-dominated plant communities that historically covered ~62 million ha in North America. We sampled plant community properties and found that after 22 years grazing and browsing elicited perceptible changes in overall plant community composition and distinct responses by individual plant species. In the woody layer of the plant community, release from winter and spring wild ungulate herbivory increased densities of larger Wyoming big sagebrush (Artemisia tridentata, ssp. wyomingensis) at the expense of small sagebrush, while disturbance associated with either cattle or wild ungulate activity alone was sufficient to increase bare ground and reduce cover of biological soil crusts. The perennial bunchgrass, bottlebrush squirretail (Elymus elymoides), responded positively to release from summer cattle grazing, and in turn appeared to competitively suppress another more grazing tolerant perennial grass, Sandberg’s blue grass (Poa secunda). Grazing by domestic cattle also was associated with increased non-native species biomass. Together, these results illustrate that ungulate herbivory has not caused sagebrush plant communities to undergo dramatic state shifts; however clear, herbivore-driven shifts are evident. In a dry, perennial-dominated system where plant community changes can occur very slowly, our results provide insights into potential long-term trajectories of these plant communities under different large herbivore regimes. Our results can be used to guide long-term management strategies for sagebrush systems and improve habitat for endemic wildlife species such as sage-grouse (Centrocercus spp.).
PMCID: PMC4324772  PMID: 25671428
14.  Predator-Induced Demographic Shifts in Coral Reef Fish Assemblages 
PLoS ONE  2011;6(6):e21062.
In recent years, it has become apparent that human impacts have altered community structure in coastal and marine ecosystems worldwide. Of these, fishing is one of the most pervasive, and a growing body of work suggests that fishing can have strong effects on the ecology of target species, especially top predators. However, the effects of removing top predators on lower trophic groups of prey fishes are less clear, particularly in highly diverse and trophically complex coral reef ecosystems. We examined patterns of abundance, size structure, and age-based demography through surveys and collection-based studies of five fish species from a variety of trophic levels at Kiritimati and Palmyra, two nearby atolls in the Northern Line Islands. These islands have similar biogeography and oceanography, and yet Kiritimati has ∼10,000 people with extensive local fishing while Palmyra is a US National Wildlife Refuge with no permanent human population, no fishing, and an intact predator fauna. Surveys indicated that top predators were relatively larger and more abundant at unfished Palmyra, while prey functional groups were relatively smaller but showed no clear trends in abundance as would be expected from classic trophic cascades. Through detailed analyses of focal species, we found that size and longevity of a top predator were lower at fished Kiritimati than at unfished Palmyra. Demographic patterns also shifted dramatically for 4 of 5 fish species in lower trophic groups, opposite in direction to the top predator, including decreases in average size and longevity at Palmyra relative to Kiritimati. Overall, these results suggest that fishing may alter community structure in complex and non-intuitive ways, and that indirect demographic effects should be considered more broadly in ecosystem-based management.
PMCID: PMC3116880  PMID: 21698165
15.  Plant Species Composition Alters the Sign and Strength of an Emergent Multi-Predator Effect by Modifying Predator Foraging Behaviour 
PLoS ONE  2013;8(8):e70258.
The prediction of pest-control functioning by multi-predator communities is hindered by the non-additive nature of species functioning. Such non-additivity, commonly termed an emergent multi-predator effect, is known to be affected by elements of the ecological context, such as the structure and composition of vegetation, in addition to the traits of the predators themselves. Here we report mesocosm experiments designed to test the influence of plant density and species composition (wheat monoculture or wheat and faba bean polyculture) on the emergence of multi-predator effects between Adalia bipunctata and Chrysoperla carnea, in their suppression of populations of the aphid Metopolophium dirhodum. The mesocosm experiments were followed by a series of behavioural observations designed to identify how interactions among predators are modified by plant species composition and whether these effects are consistent with the observed influence of plant species composition on aphid population suppression. Although plant density was shown to have no influence on the multi-predator effect on aphid population growth, plant composition had a marked effect. In wheat monoculture, Adalia and Chrysoperla mixed treatments caused greater suppression of M. dirhodum populations than expected. However this positive emergent effect was reversed to a negative multi-predator effect in wheat and faba bean polyculture. The behavioural observations revealed that although dominant individuals did not respond to the presence of faba bean plants, the behaviour of sub-dominants was affected markedly, consistent with their foraging for extra-floral nectar produced by the faba bean. This interaction between plant composition and predator community composition on the foraging behaviour of sub-dominants is thought to underlie the observed effect of plant composition on the multi-predator effect. Thus, the emergence of multi-predator effects is shown to be strongly influenced by plant species composition, mediated, in this case, by the provision of extra-floral nectar by one of the plant species.
PMCID: PMC3731319  PMID: 23936400
16.  Seasonal Trophic Niche Shift and Cascading Effect of a Generalist Predator Fish 
PLoS ONE  2012;7(12):e49691.
Few studies have examined how foraging niche shift of a predator over time cascade down to local prey communities. Here we examine patterns of temporal foraging niche shifts of a generalist predator (yellow catfish, Pelteobagrus fulvidraco) and the abundance of prey communities in a subtropical lake. We predicted that the nature of these interactions would have implications for patterns in diet shifts and growth of the predator. Our results show significant decreases in planktivory and benthivory from late spring to summer and autumn, whereas piscivory increased significantly from mid-summer until late autumn and also increased steadily with predator body length. The temporal dynamics in predator/prey ratios indicate that the predation pressure on zooplankton and zoobenthos decreased when the predation pressure on the prey fish and shrimps was high. Yellow catfish adjusted their foraging strategies to temporal changes in food availability, which is in agreement with optimal foraging theory. Meanwhile the decrease in planktivory and benthivory of yellow catfish enabled primary consumers, such as zooplankton and benthic invertebrates, to develop under low grazing pressure via trophic cascading effects in the local food web. Thus, yellow catfish shifts its foraging niche to intermediate consumers in the food web to benefit the energetic demand on growth and reproduction during summer, which in turn indirectly facilitate the primary consumers. In complex food webs, trophic interactions are usually expected to reduce the strength and penetrance of trophic cascades. However, our study demonstrates strong associations between foraging niche of piscivorous fish and abundance of prey. This relationship appeared to be an important factor in producing top-down effects on both benthic and planktonic food webs.
PMCID: PMC3522673  PMID: 23251347
17.  Plant Trait Assembly Affects Superiority of Grazer's Foraging Strategies in Species-Rich Grasslands 
PLoS ONE  2013;8(7):e69800.
Current plant – herbivore interaction models and experiments with mammalian herbivores grazing plant monocultures show the superiority of a maximizing forage quality strategy (MFQ) over a maximizing intake strategy (MI). However, there is a lack of evidence whether grazers comply with the model predictions under field conditions.
We assessed diet selection of sheep (Ovis aries) using plant functional traits in productive mesic vs. low-productivity dry species-rich grasslands dominated by resource-exploitative vs. resource-conservative species respectively. Each grassland type was studied in two replicates for two years. We investigated the first grazing cycle in a set of 288 plots with a diameter of 30 cm, i.e. the size of sheep feeding station. In mesic grasslands, high plot defoliation was associated with community weighted means of leaf traits referring to high forage quality, i.e. low leaf dry matter content (LDMC) and high specific leaf area (SLA), with a high proportion of legumes and the most with high community weighted mean of forage indicator value. In contrast in dry grasslands, high community weighted mean of canopy height, an estimate of forage quantity, was the best predictor of plot defoliation. Similar differences in selection on forage quality vs. quantity were detected within plots. Sheep selected plants with higher forage indicator values than the plot specific community weighted mean of forage indicator value in mesic grasslands whereas taller plants were selected in dry grasslands. However, at this scale sheep avoided legumes and plants with higher SLA, preferred plants with higher LDMC while grazing plants with higher forage indicator values in mesic grasslands.
Our findings indicate that MFQ appears superior over MI only in habitats with a predominance of resource-exploitative species. Furthermore, plant functional traits (LDMC, SLA, nitrogen fixer) seem to be helpful correlates of forage quality only at the community level.
PMCID: PMC3724891  PMID: 23922805
18.  Trophic Tangles through Time? Opposing Direct and Indirect Effects of an Invasive Omnivore on Stream Ecosystem Processes 
PLoS ONE  2012;7(11):e50687.
Omnivores can impact ecosystems via opposing direct or indirect effects. For example, omnivores that feed on herbivores and plants could either increase plant biomass due to the removal of herbivores or decrease plant biomass due to direct consumption. Thus, empirical quantification of the relative importance of direct and indirect impacts of omnivores is needed, especially the impacts of invasive omnivores. Here we investigated how an invasive omnivore (signal crayfish, Pacifastacus leniusculus) impacts stream ecosystems. First, we performed a large-scale experiment to examine the short-term (three month) direct and indirect impacts of crayfish on a stream food web. Second, we performed a comparative study of un-invaded areas and areas invaded 90 years ago to examine whether patterns from the experiment scaled up to longer time frames. In the experiment, crayfish increased leaf litter breakdown rate, decreased the abundance and biomass of other benthic invertebrates, and increased algal production. Thus, crayfish controlled detritus via direct consumption and likely drove a trophic cascade through predation on grazers. Consistent with the experiment, the comparative study also found that benthic invertebrate biomass decreased with crayfish. However, contrary to the experiment, crayfish presence was not significantly associated with higher leaf litter breakdown in the comparative study. We posit that during invasion, generalist crayfish replace the more specialized native detritivores (caddisflies), thereby leading to little long-term change in net detrital breakdown. A feeding experiment revealed that these native detritivores and the crayfish were both effective consumers of detritus. Thus, the impacts of omnivores represent a temporally-shifting interplay between direct and indirect effects that can control basal resources.
PMCID: PMC3507779  PMID: 23209810
19.  The relative importance of competition and predation in environment characterized by resource pulses – an experimental test with a microbial community 
BMC Ecology  2013;13:29.
Resource availability and predation are believed to affect community dynamics and composition. Although the effects of resource availability and predation on prey communities are usually studied in isolation, these factors can also have interactive effects, especially since the outcome of competition under shared predation is expected to depend on resource availability. However, there are few experimental studies that test the interactive roles of resources and predation on dynamics of more complex multispecies communities. Here, we examine the importance of competition and predation on microbial community dynamics in a resource pulse environment.
We manipulated resource availability and predation simultaneously in a microbial microcosm experiment, where a bacterial community was exposed to the protozoan predator Tetrahymena thermophila in three different resource concentrations (low, intermediate and high). The prey community consisted of three heterotrophic bacterial species: Bacillus cereus, Serratia marcescens and Novosphingobium capsulatum, all feeding on a shared plant detritus medium. In fresh culture media, all species grew in all resource concentrations used. However, during experiments without any addition of extra resources, the existing resources were soon depleted to very low levels, slowing growth of the three bacterial species. Prior to the microcosm experiment, we measured the competitive ability and grazing resistance, i.e. reduced vulnerability to predation, of each prey species. The three species differed in allocation patterns: in general, N. capsulatum had the best competitive abilities and B. cereus had good grazing resistance abilities. In the long-term microcosm experiment, N. capsulatum dominated the community without predation and, with predation, B. cereus was the dominant species in the intermediate and high resource environments.
Short-term, single-species assays revealed significant differences in the allocation of competitive and defensive traits among the prey species. Based on these differences, we were, to some extent, able to predict how the long-term community structure, e.g. species dominance, is modified by the resource availability and predation interaction in pulsed resource environments. Our results are consistent with theoretical predictions and also highlight the importance of interactive effects of resource competition and predation, suggesting that these factors should not be studied in isolation.
PMCID: PMC3766057  PMID: 24139511
Community dynamics; Diversity; Predator–prey interaction; Resource competition; Resource pulse; Tetrahymena thermophila; Trophic dynamics
20.  Local adaptation to temperature conserves top-down control in a grassland food web 
A fundamental limitation in many climate change experiments is that tests represent relatively short-term ‘shock’ experiments and so do not incorporate the phenotypic plasticity or evolutionary change that may occur during the gradual process of climate change. However, capturing this aspect of climate change effects in an experimental design is a difficult challenge that few studies have accomplished. I examined the effect of temperature and predator climate history in food webs composed of herbaceous plants, generalist grasshopper herbivores and spider predators across a natural 4.8°C temperature gradient spanning 500 km in northeastern USA. In these grasslands, the effects of rising temperatures on the plant community are indirect and arise via altered predator–herbivore interactions. Experimental warming had no direct effect on grasshoppers, but reduced predation risk effects by causing spiders from all study sites to seek thermal refuge lower in the plant canopy. However, spider thermal tolerance corresponded to spider origin such that spiders from warmer study sites tolerated higher temperatures than spiders from cooler study sites. As a consequence, the magnitude of the indirect effect of spiders on plants did not differ along the temperature gradient, although a reciprocal transplant experiment revealed significantly different effects of spider origin on the magnitude of top-down control. These results suggest that variation in predator response to warming may maintain species interactions and associated food web processes when faced with long term, chronic climate warming.
PMCID: PMC3158934  PMID: 21367789
adaptation; behaviour; climate change; food web; local climate; predator–prey
21.  Avian top predator and the landscape of fear: responses of mammalian mesopredators to risk imposed by the golden eagle 
Ecology and Evolution  2015;5(2):503-514.
Top predators may induce extensive cascading effects on lower trophic levels, for example, through intraguild predation (IGP). The impacts of both mammalian and avian top predators on species of the same class have been extensively studied, but the effects of the latter upon mammalian mesopredators are not yet as well known. We examined the impact of the predation risk imposed by a large avian predator, the golden eagle (Aquila chrysaetos, L.), on its potential mammalian mesopredator prey, the red fox (Vulpes vulpes, L.), and the pine marten (Martes martes, L.). The study combined 23 years of countrywide data from nesting records of eagles and wildlife track counts of mesopredators in Finland, northern Europe. The predation risk of the golden eagle was modeled as a function of territory density, density of fledglings produced, and distance to nearest active eagle territory, with the expectation that a high predation risk would reduce the abundances of smaller sized pine martens in particular. Red foxes appeared not to suffer from eagle predation, being in fact most numerous close to eagle nests and in areas with more eagle territories. This is likely due to similar prey preferences of the two predators and the larger size of foxes enabling them to escape eagle predation risk. Somewhat contrary to our prediction, the abundance of pine martens increased from low to intermediate territory density and at close proximity to eagle nests, possibly because of similar habitat preferences of martens and eagles. We found a slightly decreasing trend of marten abundance at high territory density, which could indicate that the response in marten populations is dependent on eagle density. However, more research is needed to better establish whether mesopredators are intimidated or predated by golden eagles, and whether such effects could in turn cascade to lower trophic levels, benefitting herbivorous species.
PMCID: PMC4314280
Intraguild predation; mesopredator suppression; pine marten; raptor; red fox; trophic interactions
22.  Cascading Effects of Ocean Acidification in a Rocky Subtidal Community 
PLoS ONE  2013;8(4):e61978.
Temperate marine rocky habitats may be alternatively characterized by well vegetated macroalgal assemblages or barren grounds, as a consequence of direct and indirect human impacts (e.g. overfishing) and grazing pressure by herbivorous organisms. In future scenarios of ocean acidification, calcifying organisms are expected to be less competitive: among these two key elements of the rocky subtidal food web, coralline algae and sea urchins. In order to highlight how the effects of increased pCO2 on individual calcifying species will be exacerbated by interactions with other trophic levels, we performed an experiment simultaneously testing ocean acidification effects on primary producers (calcifying and non-calcifying algae) and their grazers (sea urchins). Artificial communities, composed by juveniles of the sea urchin Paracentrotus lividus and calcifying (Corallina elongata) and non-calcifying (Cystoseira amentacea var stricta, Dictyota dichotoma) macroalgae, were subjected to pCO2 levels of 390, 550, 750 and 1000 µatm in the laboratory. Our study highlighted a direct pCO2 effect on coralline algae and on sea urchin defense from predation (test robustness). There was no direct effect on the non-calcifying macroalgae. More interestingly, we highlighted diet-mediated effects on test robustness and on the Aristotle's lantern size. In a future scenario of ocean acidification a decrease of sea urchins' density is expected, due to lower defense from predation, as a direct consequence of pH decrease, and to a reduced availability of calcifying macroalgae, important component of urchins' diet. The effects of ocean acidification may therefore be contrasting on well vegetated macroalgal assemblages and barren grounds: in the absence of other human impacts, a decrease of biodiversity can be predicted in vegetated macroalgal assemblages, whereas a lower density of sea urchin could help the recovery of shallow subtidal rocky areas affected by overfishing from barren grounds to assemblages dominated by fleshy macroalgae.
PMCID: PMC3628223  PMID: 23613994
23.  Susceptibility to Predation Affects Trait-Mediated Indirect Interactions by Reversing Interspecific Competition 
PLoS ONE  2011;6(8):e23068.
Numerous studies indicate that the behavioral responses of prey to the presence of predators can have an important role in structuring assemblages through trait-mediated indirect interactions. Few studies, however, have addressed how relative susceptibility to predation influences such interactions. Here we examine the effect of chemical cues from the common shore crab Carcinus maenas on the foraging behavior of two common intertidal gastropod molluscs. Of the two model consumers studied, Littorina littorea is morphologically more vulnerable to crab predation than Gibbula umbilicalis, and it exhibited greater competitive ability in the absence of predation threat. However, Littorina demonstrated a greater anti-predator response when experimentally exposed to predation cues, resulting in a lower level of foraging. This reversed the competitive interaction, allowing Gibbula substantially increased access to shared resources. Our results demonstrate that the susceptibility of consumers to predation can influence species interactions, and suggest that inter-specific differences in trait-mediated indirect interactions are another mechanism through which non-consumptive predator effects may influence trophic interactions.
PMCID: PMC3157367  PMID: 21857993
24.  Cascading effects from predator removal depend on resource availability in a benthic food web 
Marine Biology  2010;158(2):391-400.
We tested joint effects of predator loss and increased resource availability on the grazers’ trophic level and the propagation of trophic interactions in a benthic food web by excluding larger predatory fish from cages and manipulating nutrients in the coastal zone of the Baltic Sea. The combination of nutrient enrichment and excluding larger predators induced an increase in medium-sized predatory fish (three-spined stickleback). The meso-predator fish in turn did not change the total abundance of the invertebrate herbivores, but did cause a substantial shift in their community composition towards the dominance of gastropods by reducing amphipods by 40–60%, while gastropods were left unchanged. The shift in grazer composition generated a 23 times higher producer biomass, but only under nutrient enrichment. Our results show that top-predator declines can substantially shift the species composition at the grazers’ level, but that cascading effects on producers by a trophic cascade strongly depend on resource availability.
PMCID: PMC3873084  PMID: 24391255
25.  The Tri-Trophic Interactions Hypothesis: Interactive Effects of Host Plant Quality, Diet Breadth and Natural Enemies on Herbivores 
PLoS ONE  2012;7(4):e34403.
Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores.
PMCID: PMC3324533  PMID: 22509298

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