Impact of plant architecture and extraguild prey density on intraguild predation in an agroecosystem

Several models and experimental studies conducted in confined environments have shown that intraguild predation (IGP) can modulate population abundances and structure communities. A number of ecological and abiotic factors determine the nature and frequency of IGP. This study examined the effect of plant architecture and extraguild prey density, and their interactions, on the occurrence of IGP between two species of ladybird, Harmonia axyridis (Pallas) and Propylea quatuordecimpunctata L. (both Coleoptera: Coccinellidae). Theoretical concepts predict that IGP levels would increase with a decrease of both extraguild prey density and plant structural complexity. We conducted a factorial experiment in an open soybean field into which coccinellid larvae were introduced in experimental plots for a period of 5 days. We tested two levels of soybean aphid [Aphis glycines Matsumara (Hemiptera: Aphididae)] density, low and high (100 and 1 000 aphids per plot, respectively), and two levels of plant complexity, low (by removing half of the branches from the soybean plants) and high (by leaving plants intact). We used species‐specific molecular markers to detect the presence of P. quatuordecimpunctata in the digestive tract of H. axyridis. Molecular gut‐content analysis of H. axyridis revealed that rates of IGP were higher (20%) at low aphid density than at high aphid density (<6%). Decreased plant complexity did not impact the frequency of IGP. In accordance with existing literature, this study demonstrates that IGP is amplified at low extraguild prey density. We conclude that considering environmental factors, such as extraguild prey density, is crucial to improve our ability to predict the impact of intraguild predation on community structure and, from an applied perspective, biological control.     

Biodiversity Loss following the Introduction of Exotic Competitors: Does Intraguild Predation Explain the Decline of Native Lady Beetles?

Exotic species are widely accepted as a leading cause of biodiversity decline. Lady beetles (Coccinellidae) provide an important model to study how competitor introductions impact native communities since several native coccinellids have experienced declines that coincide with the establishment and spread of exotic coccinellids. This study tested the central hypothesis that intraguild predation by exotic species has caused these declines. Using sentinel egg experiments, we quantified the extent of predation on previously-common (Hippodamia convergens) and common (Coleomegilla maculata) native coccinellid eggs versus exotic coccinellid (Harmonia axyridis) eggs in three habitats: semi-natural grassland, alfalfa, and soybean. Following the experiments quantifying egg predation, we used video surveillance to determine the composition of the predator community attacking the eggs. The extent of predation varied across habitats, and egg species. Native coccinellids often sustained greater egg predation than H. axyridis. We found no evidence that exotic coccinellids consumed coccinellid eggs in the field. Harvestmen and slugs were responsible for the greatest proportion of attacks. This research challenges the widely-accepted hypothesis that intraguild predation by exotic competitors explains the loss of native coccinellids. Although exotic coccinellids may not be a direct competitor, reduced egg predation could indirectly confer a competitive advantage to these species. A lower proportion of H. axyridis eggs removed by predators may have aided its expansion and population increase and could indirectly affect native species via exploitative or apparent competition. These results do not support the intraguild predation hypothesis for native coccinellid decline, but do bring to light the existence of complex interactions between coccinellids and the guild of generalist predators in coccinellid foraging habitats.     

Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies

The soybean aphid, Aphis glycines Matsumura, has become a principal arthropod pest of soybean in the U.S. since its first detection in 2000. This species threatens soybean production through direct feeding damage and virus transmission. A diverse guild of insect predators feeds on soybean aphid in Michigan including the exotic coccinellid Harmonia axyridis, the native gall midge Aphidoletes aphidimyza and the native lacewing Chrysoperla carnea. In addition to feeding on A. glycines some members of this guild may also engage in intraguild predation. These interactions may produce positive, negative, or neutral impacts on A. glycines biological control. We explored the impact of intraguild predation on soybean aphid population dynamics by comparing aphid populations in microcosms with either A. aphidimyza larvae or C. carnea larvae alone, with both a H. axyridis adult and either A. aphidimyza or C. carnea larvae, and without predators. When H. axyridis was present with larval A. aphidimyza or C. carnea, the lady beetle acted as an intraguild predator. However, intraguild feeding did not result in a release of aphid populations compared with microcosms containing only the intraguild and aphid prey. A similar result was found in field cages. Cages allowing large predators had reduced numbers of A. aphidimyza and C. carnea larvae but also significantly fewer aphids compared with predator exclusion cages. Thus, in both lab and field studies the direct impact of H. axyridis on A. glycines overcame its negative impact as an intraguild predator. Together, these studies indicate that while the exotic H. axyridis does act as an intraguild predator and may contribute to local declines in A. aphidimyza and C. carnea, it is also currently important in overall biological control of A. glycines.     

Predation of cotton bollworm by green lacewings in the presence of cotton aphid as alternative prey on transgenic Bt and conventional cotton

Experiments were conducted in small arenas and on whole plants to explore the effect of cotton aphids, Aphis gossypii Glover (Hemiptera: Aphididae), as alternative prey on the predation of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) larvae by green lacewing larvae, Mallada signatus Schneider (Neuroptera: Chrysopidae). Transgenic Bt (Bollgard II^®) and conventional cotton plants were included to explore potential differences in the predator's performance on these cotton types. In small arenas, the presence of 20 aphids reduced predation on H. armigera larvae by 22% (from 5.5 to 3.3 of 10) by a single lacewing larva over a 24‐h period. The presence of H. armigera reduced predation on aphids by ca. 29% (from 16.8 to 11.0 of 20) over 24 h. On whole plants, the presence of alternative prey had no effect on the number of H. armigera larvae or aphids remaining after 3 days. The presence of H. armigera larvae alone, without the predator, caused a 24% reduction in the numbers of aphids on conventional, but not on Bt cotton plants. The combination of Bt cotton and lacewing larvae caused a 96.6% removal of early‐stage H. armigera larvae, a statistically significant increase over the addition of the proportions (91.6%) removed by each factor measured separately, providing evidence of synergism. These studies suggest that the presence of aphids as alternative prey would not necessarily disrupt the predation by green lacewing on larvae of H. armigera, especially on Bt cotton.     

Asymmetrical intraguild predation between natural enemies of the citrus mealybug

The ability of a predator to discriminate against parasitized prey determines the extent of asymmetrical intraguild predation, which is often crucial for the outcome of biological control. Anagyrus nr. pseudococci (Girault) (Hymenoptera: Encyrtidae), a parasitoid of the citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), suffers from intraguild predation by coccinellids occurring in the same habitat. The level of intraguild predation on A. nr. pseudococci by Nephus includens (Kirsch) (Coleoptera: Coccinellidae) at different immature stages has been investigated with and without simultaneous offer of extraguild prey. Larvae of A. nr. pseudococci appeared to face increased intraguild predation at early developmental stages, whereas mummification provided adequate protection against the predatory coccinellid. Different predation levels on unparasitized vs. parasitized hosts at various developmental stages in choice assays indicated that N. includens preferences might be determined not solely by palatability of the prey but also by its ability to protect itself.     

Invasion of the coccinellid community associated with a tropical annual agroecosystem

1. Detailed understanding of the mechanisms enabling or limiting the impacts of invasive generalist predators is needed. Harmonia axyridis is an invasive generalist coccinellid predator that may have destabilised coccinellid communities worldwide and is an excellent candidate for investigating invasion dynamics.
2. We evaluated four hypotheses: (1) Nine years after being detected in Central Brazil, Ha. axyridis has dominated the coccinellid community. This is facilitated by (2) its broader aphid prey range than the other aphidophagous coccinellids, (3) its superiority as an asymmetrical intraguild predator, and (4) the invasibility of the present coccinellid community.
3. We sampled the invertebrate communities associated with six organic vegetable farms in Brazil during 2017 and 2018, conducted a feeding trial to measure prey niche breadth and overlap, and estimated intra- and interspecific interaction strengths corresponding to first-order Lotka-Volterra parameters to evaluate the strength of intraguild predation and create a community matrix.
4. We found (1) Ha. axyridis comprised ≤8.3% of the coccinellid community. (2) Hi. convergens had the broadest prey niche and dominated the prey niche of Ha. axyridis. (3) We could not determine from the population data if Ha. axyridis was the dominant intraguild predator because its density was too low and constant. (4) The community matrix indicated that the present-day coccinellid community was stable.
5. We conclude Ha. axyridis has not become invasive in Central Brazil, in part because it does not have the broadest prey niche breadth and the present coccinellid community is stable to the present perturbation of Ha. axyridis.

     

Intra‐ and interspecific interactions between Nephus includens and Cryptolaemus montrouzieri

The introduced coccinellid Cryptolaemus montrouzieri is extensively used by biological control practitioners against mealybugs. Potential risks on native guilds of natural enemies have recently been recognized, as C. montrouzieri has managed to establish in many of the regions, it has been released. We investigated in the laboratory the direct trophic interactions between Cryptolaemus montrouzieri and Nephus includens, a predatory coccinellid native to the Mediterranean region. For both adult coccinellid species, predation rates on conspecific or heterospecific juvenile stages, with different amounts of shared prey, were recorded after 24 h. Both predators consumed eggs and larvae, but only C. montrouzieri preyed upon pupae. In general, cannibalism decreased with shared prey abundance, regardless of species. A high level of asymmetry was found on intraguild predation, in favour of C. montrouzieri. The probability of displacement threat of N. includens by C. montrouzieri in nature, in addition to possible effects of the studied trophic interactions on the outcome of biological control, is discussed.     

Intra‐ and interspecific interactions between aphidophagous ladybirds: the role of prey in predator coexistence

Cannibalism (CANN) and intraguild predation (IGP) may provide energy and nutrients to individuals and eliminate potential competitors. These negative competitive interactions could also affect the coexistence of predatory species. The co‐occurrence of aphidophagous ladybird species in crops creates opportunities for CANN and IGP, especially when aphids become scarce. The Lotka–Volterra model predicts the coexistence of two species if intraspecific competition is stronger than interspecific interference interactions. Cycloneda sanguinea L. and Eriopis connexa (Germar) (both Coleoptera: Coccinellidae) coexist in sweet pepper crops in La Plata (Argentina) consuming mainly Myzus persicae (Sulzer) (Hemiptera: Aphididae). The present study used laboratory experiments to estimate levels of CANN and IGP by adults and larvae on eggs, and by adults on larvae, in both the presence and absence of prey (i.e., M. persicae), to explain the effect of prey on coexistence of these two predators. Levels of CANN by C. sanguinea and E. connexa were high in the absence of aphids, and decreased when prey was present. Intraguild predation was bidirectional and asymmetric. Adults and larvae of E. connexa were more voracious IG predators of C. sanguinea than vice versa, the former being the stronger IG predator and interference competitor. Eriopis connexa always won when larvae of the same instar were compared, whereas the larger larva always won when larvae were of different instars, regardless of species. In the presence of prey, CANN by both species decreased, but IGP by E. connexa on C. sanguinea remained high, suggesting that E. connexa could displace C. sanguinea via interspecific interference competition. Other factors potentially affecting the coexistence of C. sanguinea and E. connexa in sweet pepper crops are discussed.     

Associations between Non‐Lethal Injury,Body Size,and Foraging Ecology in an Amphibian Intraguild Predator

Theoretical treatments of intraguild predation and its effects on behavioral interactions regard the phenomenon as a size‐structured binary response wherein predation among competitors is completely successful or completely unsuccessful. However, intermediate outcomes occur when individuals escape intraguild (IG) interactions with non‐lethal injuries. While the effects of wounds for prey include compromised mobility and increased predation risk, the consequences of similar injuries among top predators are not well understood, despite the implications for species interactions. Using an amphibian IG predator, Ambystoma opacum (Caudata: Ambystomatidae), we examined associations between non‐lethal injuries and predator body size, foraging strategy, microhabitat selection, and intraspecific agonistic interactions. Wounds were common among IG predators, generally increasing in frequency throughout larval ontogeny. Non‐lethal injuries were associated with differences in predator body size and behavior, with injured predators exhibiting smaller body sizes, increased use of benthic microhabitats, reduced agonistic displays, and increased risk of intraspecific aggression. While such effects were not ultimately associated with reduced foraging success, non‐lethal injury could contribute to niche partitioning between injured and healthy predators via habitat selection, but injured predators likely continue to exert predatory pressure on IG and basal prey populations. Our results indicate that studies of top‐down population regulation should incorporate injury‐related modifications to both prey and predator behavior and size structure.     

Combining lacewings and parasitoids for biological control of foxglove aphids in sweet pepper

The role of natural enemy diversity in biological pest control has been debated in many studies, and understanding how interactions amongst predators and parasitoids affect herbivore populations is crucial for pest management. In this study, we assessed the individual and combined use of two species of natural enemies, the parasitoid Aphidius ervi Haliday, and the predatory brown lacewing Micromus variegatus (Fabricius), on their shared prey, the foxglove aphid, Aulacorthum solani (Kaltenbach), on sweet pepper. We hypothesized that the presence of intraguild predation (IGP) and predator facilitation (through induced aphid dropping behaviour) might have both negative and positive effects on aphid control, respectively. Our greenhouse trial showed that overall, the greatest suppression of aphids occurred in the treatment with both the parasitoid and the lacewing. While the combination of lacewings and parasitoids significantly increased aphid control compared to the use of parasitoids alone, the effect was not significantly different to the treatment with only predators, although there was a clear trend of enhanced suppression. Thus, the combined effects of both species of natural enemies were between additive and non‐additive, suggesting that the combination is neither positive nor negative for aphid control. High levels of IGP, as proven in the laboratory, were probably compensated for by the strong aphid suppression provided by the lacewings, whether or not supplemented with some level of predator facilitation. For aphid management over a longer time scale, it might still be useful to combine lacewings and parasitoids to ensure stable and resilient aphid control.     

Predator–prey interactions in a ladybeetle–aphid system depend on spatial scale

The outcome of species interactions may manifest differently at different spatial scales; therefore, our interpretation of observed interactions will depend on the scale at which observations are made. For example, in ladybeetle–aphid systems, the results from small‐scale cage experiments usually cannot be extrapolated to landscape‐scale field observations. To understand how ladybeetle–aphid interactions change across spatial scales, we evaluated predator–prey interactions in an experimental system. The experimental habitat consisted of 81 potted plants and was manipulated to facilitate analysis across four spatial scales. We also simulated a spatially explicit metacommunity model parallel to the experiment. In the experiment, we found that the negative effect of ladybeetles on aphids decreased with increasing spatial scales. This pattern can be explained by ladybeetles strongly suppressing aphids at small scales, but not colonizing distant patches fast enough to suppress aphids at larger scales. In the experiment, the positive effects of aphids on ladybeetles were strongest at three‐plant scale. In a model scenario where predators did not have demographic dynamics, we found, consistent with the experiment, that both the effects of ladybeetles on aphids and the effects of aphids on ladybeetles decreased with increasing spatial scales. These patterns suggest that dispersal was the primary cause of ladybeetle population dynamics in our experiment: aphids increased ladybeetle numbers at smaller scales because ladybeetles stayed in a patch longer and performed area‐restricted searches after encountering aphids; these behaviors did not affect ladybeetle numbers at larger spatial scales. The parallel experimental and model results illustrate how predator–prey interactions can change across spatial scales, suggesting that our interpretation of observed predator–prey dynamics would differ if observations were made at different scales. This study demonstrates how studying ecological interactions at a range of scales can help link the results of small‐scale ecological experiments to landscape‐scale ecological problems.     

Orientation behavior of Propylaea japonica toward visual and olfactory cues from its prey–host plant combination

The lady beetle Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) is an important predator of aphids in agroecosystems. The inundative release of coccinellid beetles can be an effective biological control strategy. An understanding of how biological control agents perceive and use stimuli from host plants is the key to successfully implement commercially produced predators. Here, we studied the relative role of visual and volatile cues. Dual‐choice assays using foraging‐naïve and foraging‐experienced P. japonica adults were conducted using cotton plants [Gossypium hirsutum L. (Malvaceae)] with or without infestation by the cotton aphid, Aphis gossypii (Glover) (Hemiptera: Aphididae). Overall, experienced beetles were more attracted than naïve beetles toward cues associated with aphid‐infested plants. Experienced beetles were also more responsive to olfactory cues compared with naïve beetles. Both foraging‐naïve and ‐experienced lady beetles integrate olfactory and visual cues from plants infested with aphids, with an apparently greater reliance on olfactory cues. The results suggest that foraging experience may increase prey location in P. japonica.     

Delineating the effects of a plant trait on interactions among associated insects

Plant traits can affect ecological interactions between plants, herbivores, and predators. Our study tests whether reduced leaf wax in peas alters the interaction between the pea aphid ( Acyrthosiphon pisum), a foliar-foraging predator (a lady beetle, Hippodamia convergens) and a ground-foraging predator (a ground beetle, Poecilus scitulus). We performed a 2×2×2 factorial experiment in which wax level, presence of H. convergens, and presence of P. scitulus were manipulated. Experimental arenas consisted of a cage surrounding three pea plants. One plant in each cage was stocked with 15 pea aphids. In greenhouse and field cage experiments, we assessed the effect of each factor and their interactions on aphid density. As in previous studies, H. convergens foraged for aphids more effectively on reduced wax peas than on normal peas. Other interactions among H. convergens, P. scitulus , and A. pisum were the same on both types of peas. We consider how aphid movement, plant growth, and a high frequency of predation by P. scitulus on H. convergens influenced pea aphid density.     

Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids

Predator–prey interactions are influenced by nitrogen availability. Wheat (Triticum aestivum cv. Solstice) plants were provided with four levels of nitrogen and examined the responses of coccinellid predator, Harmonia axyridis to cereal aphids, Rhopalosiphum padi and Sitobion avenae. Increased nitrogen application improved nitrogen contents of the plants and also the body weight of cereal aphids feeding on them. In no‐choice feeding trials, H. axyridis consumed more aphids on low fertilised plants, suggesting a compensatory consumption to overcome reduced biomass (lower aphid size). Total biomass devoured by H. axyridis on all nitrogen fertiliser treatments was not statistically different. Logistic regression analysis of the proportion of prey consumed demonstrated that all developmental stages (larval and adult) of H. axyridis exhibited the type II functional response on all nitrogen fertiliser treatments. The rate of successful search (a′) of third and fourth instars and adults were the same across all fertiliser treatments suggesting that nitrogen fertilisation did not affect a′. Maximum handling time for the first instars of H. axyridis on R. padi (3.81 h^?1) and S. avenae (4.59 h^?1) was on the highest nitrogen treatment while minimum handling time was for the adults of H. axyridis on R. padi (0.20 h^?1) and S. avenae (0.20 h^?1) on the lowest nitrogen treatment. Handling time varied at varying fertiliser treatments within all instars and affected the predator's efficiency. The functional response curve, rate of successful search and handling time provide the information needed to understand the predator–prey interaction between H. axyridis and these cereals aphids. This could lead to the development of a better strategy for the biological control of R. padi and S. avenae at any particular level of nitrogen fertiliser regime in the field crops.     

Additive effects of predator diversity on pest control caused by few interactions among predator species

1. Studies of the impact of predator diversity on biological pest control have shown idiosyncratic results. This is often assumed to be as a result of differences among systems in the importance of predator–predator interactions such as facilitation and intraguild predation. The frequency of such interactions may be altered by prey availability and structural complexity. A direct assessment of interactions among predators is needed for a better understanding of the mechanisms affecting prey abundance by complex predator communities. 2. In a field cage experiment, the effect of increased predator diversity (single species vs. three‐species assemblage) and the presence of weeds (providing structural complexity) on the biological control of cereal aphids were tested and the mechanisms involved were investigated using molecular gut content analysis. 3. The impact of the three‐predator species assemblages of aphid populations was found to be similar to those of the single‐predator species treatments, and the presence or absence of weeds did not alter the patterns observed. This suggests that both predator facilitation and intraguild predation were absent or weak in this system, or that these interactions had counteracting effects on prey suppression. Molecular gut content analysis of predators provided little evidence for the latter hypothesis: predator facilitation was not detected and intraguild predation occurred at a low frequency. 4. The present study suggests additive effects of predators and, therefore, that predator diversity per se neither strengthens nor weakens the biological control of aphids in this system.     

Bacillus thuringiensis plants expressing Cry1Ac,Cry2Ab and Cry1F are not toxic to the assassin bug,Zelus renardii

Cotton‐ and maize‐producing insecticidal crystal (Cry) proteins from the bacterium, Bacillus thuringiensis (Bt), have been commercialized since 1996. Bt plants are subjected to environmental risk assessments for non‐target organisms, including natural enemies that suppress pest populations. Here, we used Cry1F‐resistant Spodoptera frugiperda (J.E. Smith) and Cry1Ac and Cry2Ab‐resistant Trichoplusia ni (Hübner) as prey for the assassin bug, Zelus renardii (Kolenati), a common predator in maize and cotton fields. In tritrophic studies, we assessed several fitness parameters of Z. renardii when it fed on resistant S. frugiperda that had fed on Bt maize expressing Cry1F or on resistant T. ni that had fed on Bt cotton expressing Cry1Ac and Cry2Ab. Survival, nymphal duration, adult weight, adult longevity and female fecundity of Z. renardii were not different when they were fed resistant‐prey larvae (S. frugiperda or T. ni) reared on either a Bt crop or respective non‐Bt crops. ELISA tests demonstrated that the Cry proteins were present in the plant at the highest levels, at lower levels in the prey and at the lowest levels in the predator. While Z. renardii was exposed to Cry1F and Cry1Ac and Cry2Ab when it fed on hosts that consumed Bt‐transgenic plants, the proteins did not affect important fitness parameters in this common and important predator.     

Direct and indirect top‐down effects of previous contact with an enemy on the feeding behavior of blowfly larvae

We investigated the addition of a trophic level to a simple food web. Direct and indirect effects caused by the presence of a new species in the food web were quantified by estimating survival and consumption rates on the basal resource. We focused on a blowfly intraguild prey–predator system with various ecological interactions taking place during the larval period. The experiments were designed to set Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae) as the intraguild prey and Chrysomya albiceps (Wiedemann) as the intraguild predator and/or cannibal. The generalist pupal parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) was introduced into the system during a non‐susceptible life stage of the interacting blowfly species. The cascading parasitoid effects induced behavioral changes in the blowfly larvae, increasing the impact of intraguild predation and cannibalism on blowfly survival. The results suggest that blowfly larvae can change their feeding behavior in response to the presence of a parasitoid.     

Habitat heterogeneity and mammalian predator–prey interactions

• 1 In predator–prey theory, habitat heterogeneity can affect the relationship between kill rates and prey or predator density through its effect on the predator's ability to search for, encounter, kill and consume its prey. Many studies of predator–prey interactions include the effect of spatial heterogeneity, but these are mostly based on species with restricted mobility or conducted in experimental settings.
• 2 Here, we aim to identify the patterns through which spatial heterogeneity affects predator–prey dynamics and to review the literature on the effect of spatial heterogeneity on predator–prey interactions in terrestrial mammalian systems, i.e. in freely moving species with high mobility, in non‐experimental settings. We also review current methodologies that allow the study of the predation process within a spatial context.
• 3 When the functional response includes the effect of spatial heterogeneity, it usually takes the form of predator‐dependent or ratio‐dependent models and has wide applicability.
• 4 The analysis of the predation process through its different stages may further contribute towards identifying the spatial scale of interest and the specific spatial mechanism affecting predator–prey interactions.
• 5 Analyzing the predation process based on the functional response theory, but separating the stages of predation and applying a multiscale approach, is likely to increase our insight into how spatial heterogeneity affects predator–prey dynamics. This may increase our ability to forecast the consequences of landscape transformations on predator–prey dynamics.

     

A sublethal effect on native Anthocoris nemoralis through competitive interactions with invasive Harmonia axyridis

1. The invasive ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) is implicated in declines of native ladybirds with intraguild predation identified as an underlying mechanism, however, less studied are the effects on non‐coccinellid predators. Intraguild predation between Anthocoris nemoralis Fabricius (Heteroptera: Anthocoridae) and H. axyridis and the relative effects of inter‐ and intraspecific competition on predators on potted Tilia cordata Mill. was investigated, at two aphid densities. 2. Intraguild predation was unidirectional in favour of H. axyridis in Petri dishes although a low level of ladybird egg predation by A. nemoralis occurred. However, on trees intraguild predation was rare. 3. A positive effect of aphid density on H. axyridis weight gain, and increased survival when reared with A. nemoralis on potted trees indicated stronger effects of intraspecific competition on H. axyridis. Consistent suppression of aphids by ladybirds revealed their superior competition for aphids. 4. Anthocoris nemoralis weight gain was reduced when reared with H. axyridis on potted trees, indicating a potential for a sublethal effect through interspecific competition. Survivorship of A. nemoralis did not differ between con‐ and heterospecific treatments, but high aphid density enhanced A. nemoralis survival. Overall, high mortality among nymphs across treatments suggested effects related to both inter‐ and intraspecific competition for resources. 5. Results provide evidence of a sublethal effect by invasive H. axyridis through resource competition, suggesting that where these predators co‐occur, competitive interactions for shared prey are more likely to affect A. nemoralis populations than intraguild predation by H. axyridis.     

Associational resistance or susceptibility: the indirect interaction between chemically‐defended and non‐defended herbivore prey via a shared predator

Many organisms possess chemical defences against their natural enemies, which render them unpalatable or toxic when attacked or consumed. These chemically‐defended organisms commonly occur in communities with non‐ or less‐defended prey, leading to indirect interactions between prey species, mediated by natural enemies. Although the importance of enemy‐mediated indirect interactions have been well documented (e.g. apparent competition), how the presence of prey chemical defences may affect predation of non‐defended prey in terrestrial communities remains unclear. Here, an experimental approach was used to study the predator‐mediated indirect interaction between a chemically‐defended and non‐defended pest aphid species. Using laboratory‐based mesocosms, aphid community composition was manipulated to include chemically‐defended (CD) aphids Brevicoryne brassicae, non‐defended (ND) aphids Myzus persicae or a mixed assemblage of both species, on Brassica oleracea cabbage plants, in the presence or absence of a shared predator (Chrysoperla carnea larvae). Aphid population growth rates, aphid distributions on host plants and predator growth rates were measured. In single‐species treatments, C. carnea reduced M. persicae population growth rate, but had no significant impact on B. brassicae population growth rate, suggesting B. brassicae chemical defences are effective against C. carnea. Chrysoperla carnea had no significant impact on either aphid species population growth rate in mixed‐species treatments. Myzus persicae (ND) therefore experienced reduced predation in the presence of B. brassicae (CD) through a predator‐mediated indirect effect. Moreover, predator growth rates were significantly higher in the M. persicae‐only treatments than in either the B. brassicae‐only or mixed‐species treatments, suggesting predation was impaired in the presence of B. brassicae (CD). A trait‐mediated indirect interaction is proposed, consistent with associational resistance, in which the predator, upon incidental consumption of chemically‐defended aphids is deterred from feeding, releasing non‐defended aphids from predatory control.