On the role of sinigrin (mustard oil) in a tritrophic context: plant–aphid–aphidophagous hoverfly

1. Plant secondary metabolites can govern prey–predator interactions by altering the diet breadth of predators and sometimes provide an ecological refuge to prey. Brassicaceae plants and their specialist pests can be used as a model system for understanding the role of chemically mediated effects restricting the diet breadth of natural enemies, and consequently the occurrence of enemy‐free space for the specialist pest. 2. The objective of the present study was to test the performance of the generalist predator Episyrphus balteatus De Geer (Diptera: Syrphidae) fed on the specialist herbivore Brevicoryne brassicae L.(Homoptera: Aphididae), reared on two different brassica species: black mustard (Brassica nigra), a wild species with high levels of sinigrin; and canola (Brassica napus), a cultivated species without sinigrin. 3. The preference and performance of the predator and the performance of the prey were measured. Sinigrin was quantified by high‐performance liquid chromatography in both leaf samples and aphids reared on the two host plants. 4. The cabbage aphid performed better on canola than on black mustard. The performance of the predator on this aphid when reared on canola was clearly better than when reared on black mustard. Females had a higher overall preference for cabbage aphids reared on canola than on black mustard. 5. The ability of aphids reared on plants with high glucosinolate content to reduce the performance of their generalist predators indicates that the presence of B. nigra may provide enemy‐free space for the cabbage aphid from its predator, a concept that has useful application in the context of biological control for agricultural systems.     

Effects of starvation on the search path characteristics of Orius majusculus (Reuter) (Het., Anthocoridae)

Abstract: Orius majusculus (Reuter) is a polyphagous predator bug used to control western flower thrips Frankliniella occidentalis (Pergande). As physiological factors may be highly influential upon the predatory behaviour of Orius spp. we studied the possible impact of starvation on the search path of this bug. Orius majusculus was maintained on a diet of Ephestia kuehniella Zeller (Lep., Pyralidae) eggs in laboratory. Adults were collected immediately after the imaginal moult and were individually placed in Petri dishes with abundant food. Each adult was randomly assigned to one of the following five treatments: immediate observation or starved for 2, 6, 9 or 12 h prior to observation. The observation procedure consisted of placing a single O. majusculus adult at the centre of an empty arena. The displacement of each insect was recorded with a video camera until it had reached the limits of the arena. The recorded paths were digitized and the digitized search path was used to calculate the mean walking speed, the number of stops per second, the duration of stops and the diffusion rate. The results clearly show that, in comparison with unstarved bugs, insects that experienced 6 h of prey deprivation walked more slowly, stopped more frequently and for longer periods, and had a lower rate of diffusion away from the release point. In contrast, all search path variables returned to the levels measured in unstarved bugs in the group that experienced the longest period of starvation (12 h), whereas groups of O. majusculus that had experienced 2 or 9 h of prey deprivation presented intermediate values for all the variables tested. Starvation produced evident changes in the search path characteristics that we assume to be related to physiological states of hunger and energy availability. These behavioural changes related to physiological state could have consequences for the use of this pirate bug in biological control.     

Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras

A video technique that allows simultaneous behavioural observations of several experimental replicates under field and laboratory conditions is described. The technique was used to analyse predation risk of parasitised aphids in a sugar beet field. The images of 16 black and white video cameras were recorded by a video multiplexer in combination with a time-lapse video recorder. Each camera was weather protected and equipped with a single infrared diode to allow observations during night times. Single leaves carrying aphid mummies only or mummies and unparasitised aphids were monitored. All colonies were exposed to predation and parasitation by the community of natural enemies in the field. Colonies with mummies and unparasitised aphids were visited significantly more often by predators than those without additional aphids. Predators also stayed significantly longer in patches with unparasitised aphids. Although an equal proportion of aphid mummies were destroyed in both treatments, the video analysis showed differences in predator species spectrum between treatments. In patches with aphids, coccinellid and hemipteran predators preyed on mummies, while in patches with only mummies, chrysopids accounted for most of the damage. The decrease in parasitoid survival could be attributed to the increasing number of predator visits in aphid patches and to a lesser extent to the decreasing number of unparasitised aphids (alternative prey). Parasitoid survival in colonies without alternative prey was correlated with the number of predator visits and the time predators spent on a leaf.Continuous video observations gave additional behavioural information for the interpretation of field data. Other prospective research fields for the use of the multi video camera technique are outlined and general advantages and disadvantages are discussed.     

Predator-induced morphological shift in the pea aphid

Aphids exhibit a polymorphism whereby individual aphids are either winged or unwinged. The winged dispersal morph is mainly responsible for the colonization of new plants and, in many species, is produced in response to adverse environmental conditions. Aphids are attacked by a wide range of specialized predators and predation has been shown to strongly influence the growth and persistence of aphid colonies. In two experiments, we reared two clones of pea aphid (Acyrthosiphon pisum) in the presence and absence of predatory ladybirds (Coccinella septempunctata or Adalia bipunctata). In both experiments, the presence of a predator enhanced the proportion of winged morphs among the offspring produced by the aphids. The aphid clones differed in their reaction to the presence of a ladybird, suggesting the presence of genetic variation for this trait. A treatment that simulated disturbance caused by predators did not enhance winged offspring production. The experiments indicate that aphids respond to the presence of a predator by producing the dispersal morph which can escape by flight to colonize other plants. In contrast to previous examples of predator-induced defence this shift in prey morphology does not lead to better protection against predator attack, but enables aphids to leave plants when mortality risks are high.     

Suitability of greenbugs, cotton aphids, andHeliothis virescens eggs for development and reproduction ofOrius insidiosus

Development, fecundity, and longevity of the predator,Orius insidiosus (Say) (Heteroptera: Anthocoridae), when reared on greenbug [Schizaphis graminum (Rondani)], cotton aphid (Aphis gossypii Glover), or eggs of tobacco budworm [Heliothis virescens (F.)] with green beans or water were examined. Developmental time was shortest when predators were reared onH. virescens eggs and beans and longest when reared on cotton aphids and water. Predators were most fecund when fedH. virescens eggs. The inclusion of beans in the nymphal diet further enhanced fecundity when fed eggs. Longevity of both females and males was significantly shorter when reared on aphids than on eggs. Beans in the nymphal diet enhanced longevity of female predators only in combination with budworm eggs. FemaleO. insidiosus were largest when reared onH. virescens eggs. Addition of green beans in aphid treatments resulted in increased size ofO. insidiosus when compared to aphids and free water.     

Food quality of Ephestia eggs,the aphid Rhopalosiphum padi and mixed diet for Orius majusculus

We studied the food quality of the aphid Rhopalosiphum padi to the pirate bug Orius majusculus using Ephestia eggs as high-quality comparison prey. Several performance parameters were tested on individuals that had been reared and maintained on each of the two single-prey diets or on a mixed diet. All fitness parameters were lower in individuals fed aphids only, indicating poor food quality of this prey. Compared with the pure Ephestia egg diet, the mixed diet enhanced teneral mass, while adult survival and female starvation tolerance were negatively affected and all other traits were unaffected. Body protein proportions were constant across diets, whereas lipid proportion was low in the aphid treatment. Preference for aphids was lower following a monotypic aphid diet than when reared on Ephestia eggs or a mixed diet. The results confirm that R. padi is low-quality food for O. majusculus as it is for other generalist predators, even though O. majusculus may contribute significantly to population suppression of the aphid.     

Pairwise interactions between functional groups improve biological control

Ecologists have long debated whether predators primarily disrupt one another’s prey capture through interspecific interference, or instead complement one another by occupying different feeding niches. Resolution of this debate has been difficult because different experimental designs are typically used to study interference versus complementarity. We adopted a somewhat atypical approach, surveying communities of predatory insects on 73 free-growing Brassica oleracea plants, and then re-constructing each community in field cages to measure its impact on aphid prey. The predator communities naturally varied in species composition, richness, and relative abundance; in our experiment we kept total predator density constant to avoid confounding effects of differing overall abundance. The predator communities’ impacts on aphids differed by >10-fold. Using a generalized linear model, we found that pairings of several predators in the community improved aphid suppression while no pairings disrupted it. Indeed, accounting for the presence of the beneficial pairings provided more power than species richness to explain predators’ impacts on aphids. Altogether, our results suggest generally complementary or neutral, rather than disruptive, multi-predator effects in this community. Our approach may be useful for determining the frequency of complementary species-pairings in many other systems.     

Biological control of aphids in the presence of thrips and their enemies

Generalist predators are often used in biological control programs, although they can be detrimental for pest control through interference with other natural enemies. Here, we assess the effects of generalist natural enemies on the control of two major pest species in sweet pepper: the green peach aphid Myzus persicae (Sulzer) and the western flower thrips Frankliniella occidentalis (Pergande). In greenhouses, two commonly used specialist natural enemies of aphids, the parasitoid Aphidius colemani Viereck and the predatory midge Aphidoletes aphidimyza (Rondani), were released together with either Neoseiulus cucumeris Oudemans, a predator of thrips and a hyperpredator of A. aphidimyza, or Orius majusculus (Reuter), a predator of thrips and aphids and intraguild predator of both specialist natural enemies. The combined use of O. majusculus, predatory midges and parasitoids clearly enhanced the suppression of aphids and consequently decreased the number of honeydew-contaminated fruits. Although intraguild predation by O. majusculus on predatory midges and parasitoids will have affected control of aphids negatively, this was apparently offset by the consumption of aphids by O. majusculus. In contrast, the hyperpredator N. cucumeris does not prey upon aphids, but seemed to release aphids from control by consuming eggs of the midge. Both N. cucumeris and O. majusculus did not affect rates of aphid parasitism by A. colemani. Thrips were also controlled effectively by O. majusculus. A laboratory experiment showed that adult predatory bugs feed on thrips as well as aphids and have no clear preference. Thus, the presence of thrips probably promoted the establishment of the predatory bugs and thereby the control of aphids. Our study shows that intraguild predation, which is potentially negative for biological control, may be more than compensated by positive effects of generalist predators, such as the control of multiple pests, and the establishment of natural enemies prior to pest invasions. Future work on biological control should focus on the impact of species interactions in communities of herbivorous arthropods and their enemies.     

A non-trophic interaction chain links predators in different spatial niches

Non-trophic interactions, driven by one species changing the behavior but not density of another species, appear to be as pervasive as those involving consumption. However, ecologists have only begun to explore non-trophic interactions in species-rich communities. We investigated interactions within a community including two predator–prey linkages separated in space: ground-active predatory beetles and their fly egg prey on the ground, and lady beetles and their aphid prey in plant foliage. In field and greenhouse experiments we found that ground-active predators preyed heavily on fly eggs except when both aphids and lady beetles were present. The aphids drop from the foliage to escape foraging lady beetles, and once on the ground apparently triggered ground-active predators to switch from attacking fly eggs to attacking aphids. This suggests that the first non-trophic interaction in the foliage, mediated by aphid antipredator behavior, in turn initiated and accentuated a second non-trophic interaction on the ground, mediated by prey-switching behavior by ground predators. Our results demonstrate that successive non-trophic interactions can be propagated along chains of more than three species, and can serve to link species that are otherwise spatially isolated.     

Voracity and prey preference of insidious flower bug (hemiptera: anthocoridae) for immature stages of soybean aphid (hemiptera: aphididae) and soybean thrips (thysanoptera: thripidae)

The generalist predator, Orius insidiosus (Say), is an important natural enemy of the soybean aphid, Aphis glycines Matsumura. Soybean thrips, Neohydatothrips variabilis (Beach), serve as an important prey resource for O. insidiosus in soybeans, sustaining the predator's population before the arrival of the soybean aphid. Although generalist predators can forage on a broad range of prey, they may show distinct preferences for particular prey, attacking prey at levels disproportionate to their relative numbers. To assess the preference of O. insidiosus for soybean aphid and soybean thrips, attack rates of nymphal and adult O. insidiosus were measured in the laboratory. For both adults and nymphs, the number of prey attacked increased as more prey were provided. For nymphs, the total number of prey attacked increased as the predator matured. In general, the number of prey attacked by adult predators was relatively constant as the predator aged. Both O. insidiosus nymphs and adults displayed a preference for soybean thrips, by disproportionately attacking soybean thrips over soybean aphid regardless of the relative densities of the two prey. We discuss implications of this preference on O. insidiosus life history characteristics and the potential impact on O. insidiosus-prey dynamics in the field.     

Change in carbon stable isotope ratios of the predatory bug Orius majusculus after dietary shifts

Orius majusculus Reuter (Hemiptera: Anthocoridae) is an important component of the pest predatory complex in arable crops in Mediterranean areas. It moves between crops searching for prey, and improving knowledge on its dispersal abilities will help to develop conservation biological control strategies. Stable isotope ratios may be used as a tool for tracking insect movements, as the isotopic composition of insect tissues changes to reflect that of their diet when they undergo dietary shifts on moving between isotopically distinct crops. We carried out laboratory diet switch experiments with a stable isotope approach to infer information on dispersal of O. majusculus individuals among C3 and C4 crops to better understand isotopic field data collections. Switching the aphid food source caused a quick change in δ¹³C signatures, regardless of the original and final food source. Changes in the δ¹³C ratio of O. majusculus after diet switching fitted with an exponential model that showed similar turnover rates, and thus half‐lives, between shifting diets up to 20 days. Subsequently, whereas individuals feeding on C4 aphids did not survive, turnover rate decreased in individuals that switched from C4 to C3 aphids. However, δ¹³C traces from the original source remained in the predator until 25 days after switching, and this is enough time to help determine the movement of O. majusculus between crops in the field and to plan the timing of predator sampling and crop practices that may enhance predator ecological services. Orius majusculus that switched to a maize aphid diet showed different turnover rates between sexes, although this did not influence the pattern of switchover.     

Who eats whom in a pool? A comparative study of prey selectivity by predatory aquatic insects

Predatory aquatic insects are a diverse group comprising top predators in small fishless water bodies. Knowledge of their diet composition is fragmentary, which hinders the understanding of mechanisms maintaining their high local diversity and of their impacts on local food web structure and dynamics. We conducted multiple-choice predation experiments using nine common species of predatory aquatic insects, including adult and larval Coleoptera, adult Heteroptera and larval Odonata, and complemented them with literature survey of similar experiments. All predators in our experiments fed selectively on the seven prey species offered, and vulnerability to predation varied strongly between the prey. The predators most often preferred dipteran larvae; previous studies further reported preferences for cladocerans. Diet overlaps between all predator pairs and predator overlaps between all prey pairs were non-zero. Modularity analysis separated all primarily nectonic predator and prey species from two groups of large and small benthic predators and their prey. These results, together with limited evidence from the literature, suggest a highly interconnected food web with several modules, in which similarly sized predators from the same microhabitat are likely to compete strongly for resources in the field (observed Pianka's diet overlap indices >0.85). Our experiments further imply that ontogenetic diet shifts are common in predatory aquatic insects, although we observed higher diet overlaps than previously reported. Hence, individuals may or may not shift between food web modules during ontogeny.     

Monoclonal antibodies reveal changes in predator efficiency with prey spatial pattern

Spatially explicit predator–prey interactions can alter the predatory potential of natural enemies augmented through conservation biological control. To test hypotheses regarding such interactions and predatory efficiency, we used a combination of molecular techniques and mark–release–recapture to study the foraging behaviour of a generalist carabid predator, Poecilus cupreus , in response to spatial patterns of its cereal aphid prey ( Metapolophium dirhodum and Sitobion avenae ). Beetle and aphid numbers were measured across two grids of sampling locations, within which aphid spatial pattern had been manipulated to generate patchy and more homogenous distributions. Aphid consumption was measured by enzyme-linked immunosorbent assays (ELISA) of beetle gut contents, using an aphid-specific monoclonal antibody. Movement and distribution patterns suggest that P. cupreus does not aggregate at, nor instigate prey-taxis within, aphid patches. However, more than two-thirds of the 2169 P. cupreus tested by ELISA had consumed aphids and the proportion of beetles containing aphid proteins was positively related to aphid density. Against expectation, the proportion of predators feeding on aphids was greatest where prey were homogenously distributed, and this was attributed to the loss of partial refuges for prey in aphid patches. The functional value of this type of uniform foraging strategy is ideally suited to early colonization of the crop habitat, when aphid numbers are low, before populations build up and form strong spatial patterns.     

Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions

Generalist insect predators can significantly impact the dynamics of pest populations; and, using alternative prey, they can rapidly establish in disturbed agroecosystems. However, indirect interactions between prey can occur, leading to either increased or decreased predation on focal prey. The present paper demonstrates how alternative prey can disrupt predation by the hemipteran Orius insidiosus on the soybean aphid Aphis glycines via short-term indirect interactions. We used laboratory microcosms to measure the impact of the predator on the population growth of the aphid in the presence of alternative prey, soybean thrips Neohydatothrips variabilis, and we characterized the foraging behaviour of the predator to assess prey preference. We showed that O. insidiosus predation on aphids was reduced in the presence of thrips and that this positive impact on aphids increased as thrips density increased. Results from the behavioural experiment support the hypothesis of a prey preference toward thrips. When prey-pest ratio is aphid-biased, short-term apparent commensalism between prey occurs in favour of the most abundant prey (aphids) with no switching behaviour appearing in O. insidiosus. These results demonstrate that potential indirect interactions should be taken into account when considering O. insidiosus as a biocontrol agent against the soybean aphid.     

Habitat and food specificity in aphidophagous predators

Current knowledge of the processes underlying prey location and choice by aphidophagous predators is reviewed by considering the succession of behavioural mechanisms required for the predator to obtain prey. The predator may locate areas where prey are likely to be found by responding to physical aspects of the habitat, or to semiochemicals produced by the host plant. The predator may then respond to visual or olfactory cues to locate the aphid prey. The predator's readiness to attack and consume aphids is influenced by any behavioural or chemical defence strategies, and by the palatability or nutrient value of the aphids. Toxic allelochemicals ingested by aphids from their host plant may have a detrimental effect on predators.     

Predator avoidance behavior in the pea aphid: costs,frequency, and population consequences

Induced prey defenses can be costly. These costs have the potential to reduce prey survival or reproduction and, therefore, prey population growth. I estimated the potential for predators to suppress populations of pea aphids (Acyrthosiphon pisum) in alfalfa fields through the induction of pea aphid predator avoidance behavior. I quantified (1) the period of non-feeding activity that follows a disturbance event, (2) the effect of frequent disturbance on aphid reproduction, and (3) the frequency at which aphids are disturbed by predators. In combination, these three values predict that the disturbances induced by predators can substantially reduce aphid population growth. This result stems from the high frequency of predator-induced disturbance, and the observation that even brief disturbances reduce aphid reproduction. The potential for predators to suppress prey populations through induction of prey defenses may be strongest in systems where (1) predators frequently induce prey defensive responses, and (2) prey defenses incur acute survival or reproductive costs. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

The effect of powdery mildew on the number of prey consumed by Typhlodromus pyri (Acari: Phytoseiidae)

Abstract:  Prey consumption by Typhlodromus pyri Scheuten was studied in the presence and absence of apple powdery mildew, Podosphaera leucotricha (Ell. and Everh.) under constant laboratory conditions. Eggs of Tetranychus urticae Koch were offered to predatory mites as a prey. Seven densities ranging from five to 100 T. urticae eggs per arena were used. Mildew conidia (approximately 0.5 mg) were added to half of the arenas by brushing them from infected apple leaves. A single adult female of T. pyri was introduced onto each arena and number of prey eggs consumed was counted 12 h later when the predator was offered new T. urticae eggs again and the procedure was repeated once. Data showed that predators consumed in both experimental periods nearly all prey in experiments with densities up to 40 eggs per arena and no mildew. However, the number of eggs consumed decreased more than twofold when mildew conidia were supplied, even at high prey densities. Differences in predation rate between treatments with and without mildew were highly significant. The results thus indicate that availability of mildew as an alternative food can reduce prey suppression by T. pyri . Possible implications of these findings in biological control of spider mites by generalist predatory mites are discussed.     

Potential cotton aphid,Aphis gossypii,population suppression by arthropod predators in upland cotton

The cotton aphid, Aphis gossypii Glover, predation rate of convergent lady beetle, Hippodamia convergens Guerin‐Meneville, was determined by assigning a single predator randomly to each of four prey density treatments in the laboratory. Prey densities included 25, 50, 100, and 200 aphids per Petri dish arena. Predation response was recorded at 1, 4, 8, 16, 24, and 48 h after assigning predators to their prey treatments. Rate of consumption increased through time, with all 25 aphids consumed during the first 4 h of the experiment. At the highest density, adult lady beetle consumed on average 49, 99, 131, 163, 183, and 200 aphids within 1, 4, 8, 16, 24 and 48 h, respectively. Predators showed a curvilinear feeding response in relation to total available time, indicating that convergent lady beetles have the potential to suppress larger populations of aphids through continuous feeding by regulating their predation efficiency during feeding. The analysis of age‐specific mortality in absence of prey revealed that lady beetles could survive for an extended period of time (more than 2 weeks) without prey. The ability of a predator to survive without prey delays or prevents the rebound of pest populations that is a significant factor in natural biological control. A two‐year field sampling of 10 cotton arthropod predator species showed that spiders (27%) were the most dominant foliage dwelling predators in the Texas High Plains cotton followed by convergent lady beetles (23.5%), hooded beetles (13.5%), minute pirate bugs (11%), green lacewings (9.5%), bigeyed bugs (7.5%), scymnus beetles (3%), soft‐winged flower beetles (2%), damsel bugs (1.5%), and assassin bugs (1.5%). A field cage study showed that one H. convergens adult per plant released at prey density of one aphid per leaf kept the aphid population below economic threshold for the entire growing season.     

Life history characteristics of Orius insidiosus (Say) fed diets of soybean aphid, Aphis glycines Matsumura and soybean thrips, Neohydatothrips variabilis (Beach)

Field studies in soybeans have demonstrated that the endemic predator, Orius insidiosus (Say), is an important natural enemy of the soybean aphid, Aphis glycines Matsumura. Soybean thrips, Neohydatothrips variabilis (Beach), serve as an important prey resource for O. insidiosus in soybeans and may be important in sustaining O. insidiosus populations before the arrival of soybean aphid. Because soybean aphid is new to the US soybean system, the effects of a mixed diet of soybean aphid and soybean thrips on O. insidiosus life history is not known. We measured the survival, development, and reproduction of O. insidiosus when fed soybean thrips, and a mixed prey diet of soybean aphids and soybean thrips, and compared these results to a previous study of O. insidiosus life history fed soybean aphid alone. Nymphal development to adulthood (15.9 days) and fecundity (68.8 eggs per female) was improved for O. insidiosus fed ad libitum soybean thrips daily compared to O. insidiosus fed ad libitum soybean aphids daily. The contribution of alternative prey to O. insidiosus life history characteristics can be complex depending on the amount and quality of a particular prey item. At low levels of prey, the addition of prey appears to enhance O. insidiosus survival, development, and fecundity. However, as predators are fed more often, the predator’s response depends on the type of prey that predominates in the mixed prey diet. We discuss soybean thrips impact on O. insidiosus population ecology and soybean aphid dynamics.     

Predator impacts on stream benthic prey

The impact that predators have on benthic, macroinvertebrate prey density in streams is unclear. While some studies show a strong effect of predators on prey density, others show little or no effect. Two factors appear to influence the detection of predator impact on prey density in streams. First, many field studies have small sample sizes and thus might be unable to detect treatment effects. Second, streams contain two broad classes of predators, invertebrates and vertebrates, which might have different impacts on prey density for a variety of reasons, including availability of refuge for prey and prey emigration responses to the two types of predators. In addition, predatory vertebrates have more complex prey communities than predatory invertebrates; this complexity might reduce the impact that predatory vertebrates have on prey because of indirect effects. I conducted a meta-analysis on the results of field studies that manipulate predator density in enclosures to determine (1) if predators have a significant impact on benthic prey density in streams, (2) if the impacts that predatory invertebrates and vertebrates have differ, and (3) if predatory vertebrates have different impacts on predatory prey versus herbivorous prey. The results of the meta-analysis suggest that on average predators have a significant negative effect on prey density, predatory invertebrates have a significantly stronger impact than predatory vertebrates, and predatory vertebrates do not differ in their impact on predatory versus herbivorous invertebrate prey. Three methodological variables (mesh size of enclosures, size of enclosures, and experimental duration) were examined to determine if cross correlations exist that may explain the differences in impact between predatory invertebrates and vertebrates. No correlation exists between mesh size and predator impact. Over all predators, no correlation exists between experimental duration and predator impact; however, within predatory invertebrates a correlation does exist between these variables. Also, a correlation was found between enclosure size and predator impact. This correlation potentially explains the difference in impact between predatory invertebrates and predatory vertebrates. Results of the meta-analysis suggest two important areas for future research: (1) manipulate both types of predators within the same system, and (2) examine their impacts on the same spatial scale.