Sticky plant traps insects to enhance indirect defence

Plant‐provided foods for predatory arthropods such as extrafloral nectar and protein bodies provide indirect plant defence by attracting natural enemies of herbivores, enhancing top‐down control. Recently, ecologists have also recognised the importance of carrion as a food source for predators. Sticky plants are widespread and often entrap and kill small insects, which we hypothesised would increase predator densities and potentially affect indirect defence. We manipulated the abundance of this entrapped insect carrion on tarweed (Asteraceae: Madia elegans) plants under natural field conditions, and found that carrion augmentation increased the abundance of a suite of predators, decreased herbivory and increased plant fitness. We suggest that entrapped insect carrion may function broadly as a plant‐provided food for predators on sticky plants.     

The three criteria for resistance by plant carrion‐provisioning: insect entrapment and predator enrichment on Mimulus bolanderi

1. Many sticky plants provision mutualistic scavenging arthropod predators with carrion, which in turn protect the plant from insect herbivores. While insect entrapment is a common trait across plants, which plants attract these predators and may derive protection is still largely unknown. 2. Three conditions were proposed that must be satisfied for observational data to suggest this defensive strategy: (i) the consistent presence of scavenging predators, (ii) positive correlation between predator numbers and carrion, and (iii) suitability of these predators for controlling known herbivores. 3. As a case study, we examined the fire‐following annual, Mimulus [Diplacus] bolanderi (Phyrmaceae), which is part of a well‐studied radiation of California monkeyflowers. Many monkeyflowers entrap insects, though attraction to predators has not been quantified in this genus. 4. A guild of scavenging arthropod predators on M. bolanderi (condition #1) was found, which correlated positively with carrion abundance (#2) and could consume the primary herbivore (#3), suggesting a carrion‐mediated defensive strategy. Lastly, as M. bolanderi is variable in time and space, these interactions are facultative, and these predators are quick to adopt ephemeral carrion resources on novel host plants.     

Prey preference,intraguild predation and population dynamics of an arthropod food web on plants

The theory of intraguild predation (IGP) largely studies effects on equilibrium densities of predators and prey, while experiments mostly concern transient dynamics. We studied the effects of an intraguild (IG) predator, the bug Orius laevigatus, on the population dynamics of IG-prey, the predatory mite Phytoseiulus persimilis, and a shared prey, the phytophagous two-spotted spider mite Tetranychus urticae, as well as on the performance of cucumber plants in a greenhouse. The interaction of the predatory mite and the spider mite is highly unstable, and ends either by herbivores overexploiting the plant or predators exterminating the herbivores. We studied the effect of IGP on the transient dynamics of this system, and compared the dynamics with that predicted by a simple population-dynamical model with IGP added. Behavioural studies showed that the predatory bug and the predatory mite were both attracted to plants infested by spider mites and that the two predators did not avoid plants occupied by the other predator. Observations on foraging behaviour of the predatory bug showed that it attacks and kills large numbers of predatory mites and spider mites. The model predicts strong effects of predation and prey preference by the predatory bugs on the dynamics of predatory mites and spider mites. However, experiments in which the predatory bug was added to populations of predatory mites and spider mites had little or no effect on numbers of both mite species, and cucumber plant and fruit weight.     

Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades

The ability of predators to elicit a trophic cascade with positive impacts on primary productivity may depend on the complexity of the habitat where the players interact. In structurally-simple habitats, trophic interactions among predators, such as intraguild predation, can diminish the cascading effects of a predator community on herbivore suppression and plant biomass. However, complex habitats may provide a spatial refuge for predators from intraguild predation, enhance the collective ability of multiple predator species to limit herbivore populations, and thus increase the overall strength of a trophic cascade on plant productivity. Using the community of terrestrial arthropods inhabiting Atlantic coastal salt marshes, this study examined the impact of predation by an assemblage of predators containing Pardosa wolf spiders, Grammonota web-building spiders, and Tytthus mirid bugs on herbivore populations (Prokelisia planthoppers) and on the biomass of Spartina cordgrass in simple (thatch-free) and complex (thatch-rich) vegetation. We found that complex-structured habitats enhanced planthopper suppression by the predator assemblage because habitats with thatch provided a refuge for predators from intraguild predation including cannibalism. The ultimate result of reduced antagonistic interactions among predator species and increased prey suppression was enhanced conductance of predator effects through the food web to positively impact primary producers. Behavioral observations in the laboratory confirmed that intraguild predation occurred in the simple, thatch-free habitat, and that the encounter and capture rates of intraguild prey by intraguild predators was diminished in the presence of thatch. On the other hand, there was no effect of thatch on the encounter and capture rates of herbivores by predators. The differential impact of thatch on the susceptibility of intraguild and herbivorous prey resulted in enhanced top-down effects in the thatch-rich habitat. Therefore, changes in habitat complexity can enhance trophic cascades by predator communities and positively impact productivity by moderating negative interactions among predators.     

Diet‐dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non‐matching diets, we scrutinized diet‐dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant‐derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen‐fed mothers were a more profitable prey than those from spider‐mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen‐fed protonymphs were earlier attacked by IG predator females than spider‐mite fed protonymphs. Spider mite‐fed N. californicus females attacked protonymphs earlier than did pollen‐fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio‐control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.     

Plant neighbours mediate bird predation effects on arthropod abundance and herbivory

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Effect of pollen supplement on intraguild predatory interactions between two omnivores: The importance of spatial dynamics

Arthropods often engage in complex trophic interactions such as intraguild predation (IGP), true omnivory (i.e., feeding on plants and prey), and apparent competition. Theoretical treatments of the effects of such interactions on herbivore populations have been concerned almost entirely with equilibrium conditions. Yet these interactions are common in non-equilibrium settings such as agroecosystems, where they are likely to have a strong influence on pest populations. We therefore tested short-term effects of IGP and food supplementation on interactions between two predators (the phytoseiid mite Neoseiulus cucumeris and the anthocorid bug Orius laevigatus) and their shared prey, Frankliniella occidentalis, on strawberry plants. All three consumers feed on strawberry pollen, both mites and bugs prey on thrips, and the bug also feeds on the mites (IGP). Strong IGP on mites (IG prey) by the bugs (IG predator) was recorded in structurally-simple arenas. In a more complex setting (whole-plants), however, the intensity of IGP differed among plant structures. Likewise, pollen supplementation reduced both IGP and predation on thrips in a structurally simple setting. In the whole-plant experiment, IGP was more intense on pollen-bearing than pollen-free flowers. The study illustrated how spatial dynamics, generated when consumers track food sources differently in the habitat and possibly when herbivorous and IG prey alter their distribution to escape predation, led to site-specific configuration of interacting populations. The intensity of resulting trophic interactions was weakened by food supplementation and by increased complexity of the habitat.     

Top predator control of plant biodiversity and productivity in an old-field ecosystem

Abstract Predators can have strong indirect effects on plants by altering the way herbivores impact plants. Yet, many current evaluations of plant species diversity and ecosystem function ignore the effects of predators and focus directly on the plant trophic level. This report presents results of a 3‐year field experiment in a temperate old‐field ecosystem that excluded either predators, or predators and herbivores and evaluated the consequence of those manipulations on plant species diversity (richness and evenness) and plant productivity. Sustained predator and predator and herbivore exclusion resulted in lower plant species evenness and higher plant biomass production than control field plots representing the intact natural ecosystem. Predators had this diversity‐enhancing effect on plants by causing herbivores to suppress the abundance of a competitively dominant plant species that offered herbivores a refuge from predation risk.     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

Negative interactions between chemical resistance and predators affect fitness in soybeans

Abstract 1. Plants may benefit from both chemical resistance traits and the presence of predators of herbivores. In past studies, the interaction between resistance and predators varies from complementary to antagonistic among different systems. However, this interaction has primarily been quantified by effects on predator abundance or vigor, not effects on plant fitness. 2. In this study, the combined effects of chemical resistance and predators on plant fitness were examined using soybeans (Glycine max), herbivorous Mexican bean beetles (Epilachna varivestis), and predaceous spined soldier bugs (Podisus maculiventris). Mexican bean beetles were reared in field cages in the presence or absence of spined soldier bugs on soybeans with or without strong constitutive chemical resistance. 3. Spined soldier bugs were more likely to feed on Mexican bean beetles that fed on susceptible than on resistant plants. 4. Susceptible plants with predators produced significantly more seeds than those without predators, while resistant plants did not produce significantly different numbers of seeds based on the presence or absence of predators. 5. Selection for the production of some types of chemical resistance in plants would thus be expected to be stronger with lower predation rates. 6. These results also suggest predator introductions would be more effective on plants without a strong constitutive chemical resistance to herbivores.     

Influence of predator‐specific defense adaptation on intraguild predation

The persistence of intraguild predation (IGP), the prey–predator interaction between competing species, is puzzling because simple IGP models readily predict species extinction. In this study, we explored a mathematical model incorporating predator‐specific defense adaptation of basal prey against intraguild prey and intraguild predator. The model explicitly described the dynamics of the defense effort against each predator under the assumption that anti‐predator defense was associated with reducing effort allocated to reproduction. The model predicted that defense adaptation (i.e. the ability to reallocate defense effort) would facilitate coexistence, particularly when system productivity is high; at low productivity, coexistence would be facilitated or inhibited depending on initial effort allocation prior to defense adaptation. In addition, we found that three‐species dynamics became more stable at higher adaptation rates. The results suggest that common behavioral changes, such as predator‐specific defense adaptation, have significant implications for the community structure and dynamics of IGP systems.     

Generalist and sticky plant specialist predators suppress herbivores on a sticky plant

Glandular trichomes are conventionally viewed as a type of direct defense against herbivores that carry indirect costs associated with the exclusion of numerous predators. We tested the hypothesis that predators are ineffective on sticky plants using a predator that is adapted to sticky plants, the harpactorine assassin bug Pselliopus spinicollis Champion, and a common surrogate generalist predator in analogous studies, the coccinellid Hippodamia convergens Guerin. We tested their top–down effects on herbivores using sticky and non-sticky races of common madia plants (Asteraceae: Madia elegans) and their native herbivores, a noctuid moth (Noctuiidae: Heliothodes diminutiva Hodges) and an aphid (Aphididae: Uroleucon madia Swain). We report that both predators were effective at reducing herbivore abundances on sticky and non-sticky plants, with greater efficacy on sticky plants.     

Contrasting cascades: insectivorous birds increase pine but not parasitic mistletoe growth

1. Intraguild predation occurs when top predators feed upon both intermediate predators and herbivores. Intraguild predators may thus have little net impact on herbivore abundance. Variation among communities in the strength of trophic cascades (the indirect effects of predators on plants) may be due to differing frequencies of intraguild predation. Less is known about the influence of variation within communities in predator-predator interactions upon trophic cascade strength. 2. We compared the effects of a single predator community between two sympatric plants and two herbivore guilds. We excluded insectivorous birds with cages from ponderosa pine Pinus ponderosa trees parasitized by dwarf mistletoe Arceuthobium vaginatum. For 3 years we monitored caged and control trees for predatory arthropods that moved between the two plants, foliage-feeding caterpillars and sap-feeding hemipterans that were host-specific, and plant damage and growth. 3. Excluding birds increased the abundance of ant-tended aphids on pine and resulted in an 11% reduction in pine woody growth. Mutualist ants protected pine-feeding aphids from predatory arthropods, allowing aphid populations to burgeon in cages even though predatory arthropods also increased in cages. By protecting pine-feeding aphids from predatory arthropods but not birds, mutualist ants created a three-tiered linear food chain where bird effects cascaded to pine growth via aphids. 4. In contrast to the results for tended aphids on pine, bird exclusion had no net effects on untended pine herbivores, the proportion of pine foliage damaged by pine-feeding caterpillars, or the proportion of mistletoe plants damaged by mistletoe-feeding caterpillars. These results suggest that arthropod predators, which were more abundant in cages as compared with control trees, compensated for bird predation of untended pine and mistletoe herbivores. 5. These contrasting effects of bird exclusion support food web theory: where birds were connected to pine by a linear food chain, a trophic cascade occurred. Where birds fed as intraguild predators, the reticulate food webs linking birds to pine and mistletoe resulted in no net effects on herbivores or plant biomass. Our study shows that this variation in food web structure occurred between sympatric plants and within plants between differing herbivore guilds.     

Invasion success in communities with reciprocal intraguild predation depends on the stage structure of the resident population

The probability of individuals being targeted as prey often decreases as they grow in size. Such size‐dependent predation risk is very common in systems with intraguild predation (IGP), i.e. when predatory species interact through predation and competition. Theory on IGP predicts that community composition depends on productivity. When recently testing this prediction using a terrestrial experimental system consisting of two phytoseiid mite species, Iphiseius degenerans as the IG‐predator and Neoseiulus cucumeris as the IG‐prey, and pollen (Typha latifolia) as the shared resource, we could not find the predicted community shift. Instead, we observed that IG‐prey excluded IG‐predators when the initial IG‐prey/IG‐predator ratio was high, whereas the opposite held when the initial ratio was low, which is also not predicted by theory. We therefore hypothesized that the existence of vulnerable and invulnerable stages in the two populations could be an important driver of the community composition. To test this, we first demonstrate that IG‐prey adults indeed attacked IG‐predator juveniles in the presence of the shared resource. Second, we show that the invasion capacity of IG‐predators at high productivity levels indeed depended on the structure of resident IG‐prey populations. Third, we further confirmed our hypothesis by mimicking successive invasion events of IG‐predators into an established population of IG‐prey at high productivity levels, which consistently failed. Our results show that the interplay between stage structure of populations and reciprocal intraguild predation is decisive at determining the species composition of communities with intraguild predation.     

Evidence for intraguild predation by Podisus maculiventris on a ladybeetle, Coleomegilla maculata: Implications for biological control of Colorado potato beetle, Leptinotarsa decemlineata

The potential for intraguild predation (IGP) between larval and adult life stages of twopolyphagous arthropod predators common in NorthAmerican agroecosystems was studied in thelaboratory. Predators examined were the spinedsoldier bug, Podisus maculiventris Say,and the twelve-spotted ladybeetle, Coleomegilla maculata Lengi. A shared preyitem, eggs of the Colorado potato beetle (CPB),Leptinotarsa decemlineata Say, was alsoprovided to the predators, both to provide analternate food source and to quantify theimpact of IGP on the potential for pestsuppression by these two predators. Experimentswere conducted on single potato leaves inplastic cup arenas, and, subsequently, in cagesenclosing whole potato plants. IGP occurredasymmetrically, with P. maculiventrisadults and nymphs only attacking C. maculata larvae. Even though ladybeetle adultswere generally smaller than soldier bug adults,they were never preyed upon. This appears to bethe first documented case of a coccinellidshowing differential larval and adult immunityto attack by a larger invertebrate predator.The impact of IGP, when it did occur, on CPBegg consumption was equivocal. IGP did notconsistently influence levels of predation onthe eggs. Conversely, even when IGP did notoccur, predation on CPB eggs by both predatorstogether did not increase significantly overlevels inflicted by either predator alone. Theimplications for biological control of CPB bythese predators, which are being considered foraugmentative release in potato and tomato cropsin the United States, are discussed.     

Multi-trophic effects of ungulate intraguild predation on acorn weevils

Predators and parasitoids may contribute to controlling the population sizes of phytophagous insects, and this has been shown to benefit plants. Phytophagous insects may also be killed by other herbivores (intraguild predation), usually larger-sized vertebrates that ingest insects accidentally while feeding on common food sources. We studied the intraguild predation on acorn weevils by ungulates and assessed the consequences for weevil populations. Infested acorns are prematurely abscised and the weevil larvae finish their development inside the acorns after being dropped. Our results show that weevil larvae were killed by ungulates eating the infested acorns on the ground. Ungulates did not discriminate between infested and sound acorns, and the probability of a larva being incidentally eaten was inversely related to acorn availability. Thus, predation risk was enhanced by the premature drop of infested acorns when acorn availability on the ground was low. Predation rates on infested acorns were much higher where ungulates were present, and acorn infestation rates were significantly lower. However, ungulates did not provide the oaks any net benefit, since the reduction of infestation rates was not enough to compensate for the large amounts of sound acorns eaten by ungulates. Seed predation is usually studied as a progressive loss of seeds by pre- and post-dispersal predators, but the interactions between them are usually not considered. We show that intraguild predation on insects by large ungulates had an effect on the structure of the foraging guild, as the proportion of acorns predated by insects decreased; however, replicating the same experimental design in different ecological scenarios would increase the strength of these results. In conclusion, the present study shows the importance of considering the multi-trophic interactions between seed predators in order to have a complete picture of granivory.     

The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression

Intraguild predation (IGP) occurs when consumers competing for a resource also engage in predatory interactions. A common type of IGP involves aphid predators and parasitoids: since parasitoid offspring develop within aphid hosts, they are particularly vulnerable to predation by aphid predators such as coccinellid beetles. Other intraguild interactions that include non-lethal behavioral effects, such as interference with foraging and avoidance of IGP, may also hamper parasitoid activity and reduce their effectiveness as biological control agents. In this study, we quantified mortality in and behavioral effects on Aphidius colemani Viereck (Hymenoptera: Aphidiidae) by its IG-predator Coccinella undecimpunctata L. (Coleoptera: Coccinellidae), and compared the impact of two release ratios of these natural enemies on aphid populations. Parasitoids did not leave the plant onto which they were first introduced, regardless of the presence of predators, even when alternative prey was offered on predator-free plants nearby. In 2-hour experiments, predator larvae interfered with wasp activity, and the level of aphid parasitism was lower in the presence of predators than in their absence. In these experiments, the parasitoids contributed more to aphid mortality than the predators and aphid suppression was higher when a parasitoid acted alone than in combination with a predator larva. These results were confirmed in a 5-day experiment, but only at one parasitoid:predator release ratio (4:3) not another (2:3). The over-all impact on aphid population growth was non-the-less stronger when both enemies acted together than when only one of them was present. Results indicate that for given release ratios and time scale, the negative lethal and non-lethal effects of the predator on parasitoid performance did not fully cancelled the direct impact of the predator on the aphid population.     

Positive indirect effect of aquatic insects on terrestrial prey is not offset by increased predator density

1. Changes in one prey species' density can indirectly affect the abundance of another prey species if a shared predator eats both species. Sometimes, indirect effects occur when prey straddle habitats, including when riparian predator populations grow in response to emergent aquatic insects and increase predation on terrestrial prey. However, predators may largely switch to aquatic insects or become satiated, reducing predation on terrestrial prey. 2. To determine the net indirect effect of aquatic insects on terrestrial arthropods via generalist spider predators, a field experiment was conducted mimicking midge influx and a wolf spider numerical response inside enclosures near an Icelandic lake. Lab mesocosms were also used to assess per capita rates of spider predation u nder differing levels of midge abundance. 3. Midges always decreased sentinel prey predation, but this effect increased with predator density. When midges were absent, predation increased 30% at a high spider density, but predation was equal between spider treatments when midges were present. In situ arthropods showed no effect of midge or spider treatments, although non‐significant abundance patterns were observed congruent with sentinel prey results. 4. In lab mesocosms, prey survivorship increased ≥50% where midges were present and rapidly saturated; the addition of 5, 20, 50, and 100 midges equivalently reduced spider predation, supporting predator distraction rather than satiation as the root cause. 5. The present results demonstrate a strong positive indirect effect of midges and broadly support the concept that predator responses to alternative prey are a major influence on the magnitude and direction of predator‐mediated indirect effects.     

Leaf domatia reduce intraguild predation among predatory mites

1. Although theory suggests that intraguild predation destabilises food webs and may result in exclusion of species, empirical observations of food webs reveal that it is a common interaction. It has been proposed that habitat structure reduces the interaction strength of intraguild predation, thus facilitating the coexistence of species. 2. This was tested using acarodomatia, tiny structures on plant leaves, and predatory mites, which usually reside in these domatia. Sweet pepper plants (Capsicum annuum L.) were used, which possess domatia consisting of tufts of hair, and coffee plants (Coffea arabica L.) with pit‐shaped domatia. 3. On sweet pepper, the predatory mites Neoseiulus cucumeris Oudemans and Iphiseius degenerans Berl. feed on each other's juveniles. Larvae of each of the species were therefore used as intraguild prey with adult females of the other species as intraguild predators. On coffee, a similar set‐up was used, with larvae and adult females of Amblyseius herbicolus Chant and Iphiseiodes zuluagai Denmark & Muma as intraguild prey and intraguild predators, respectively. 4. Domatia on detached, isolated sweet pepper and coffee leaves were either closed with glue or left open, after which larvae and adult predators were released. As a control, larvae were released on leaves with open or closed domatia without an adult predator. 5. Survival of larvae was high in the absence of the adult (intraguild) predator. In the presence of the intraguild predator, survival was significantly higher on leaves with open domatia than on leaves with closed domatia. 6. This shows that even such tiny structures as plant domatia may significantly affect the interaction strength of intraguild predation.     

Resource quality,resource availability,and intraguild predation among omnivorous mirids

Intraguild predation (IGP) among predatory species can influence many plant-arthropod associations. However, the relevance of IGP is poorly understood for truly omnivorous species such as those that can complete development on both animal and plant diets. Here we test the hypothesis that IGP among two omnivorous mirids is more common when extraguild food is either absent or not suitable. Laboratory experiments were performed in experimental cages in order to determine the effect of intraguild prey densities and diet availability on direction and intensity of IGP between Dicyphus tamaninii and Macrolophus caliginosus (Heteroptera: Miridae). Intraguild predation was symmetrical between the two mirid species in the absence of alternative food. Increasing densities of intraguild prey enhanced drastically the incidence of IGP. Intraguild predation was reduced when mirids were in the presence of green or red tomato fruits, but the presence of any other extraguild resources had no impact on IGP level. However, when given before the experiments, all resources with the exception of tomato leaves significantly reduced IGP. A second experiment was performed on live plants to compare the results of the previous trials with that obtained in a more natural setting. No IGP was observed when both mirid species were present on a plant. However, development of the intraguild prey (the more vulnerable stage) was hindered by the presence of the intraguild predator. The potential of such results is discussed from community ecology and biological control perspective.