Non-additive effects of multiple natural enemies on aphid populations

The question of whether multiple natural enemies often interact to produce lower host mortality than single enemies acting alone has not yet been resolved. We compared the effects of four different combinations of natural enemies-parasitoids, predators, parasitoids plus predators, and no enemies-on caged aphid populations on marsh elder, Iva frutescens, in west-central Florida. Using starting densities of natural enemies commonly found in the field, we showed that parasitoid wasps reduced aphid population densities more than predatory ladybird beetles. The addition of predators to cages containing parasites reduced the ability of parasitoids to decrease aphid population densities. Because the experiments ran only over the course of one generation, such a reduction in the effectiveness of parasites is likely caused by interference of predators with parasitoid behavior. Parasitism in the cages containing both parasitoids and predators was reduced when compared to percent parasitism in parasitoid-only cages, but this could also be due to predation. Our experiments showed that ladybird beetles prey on parasitized aphids. Thus over the long-term, the effectiveness of parasites is impaired by the interference of predators on ovipositing parasitoids and by the predation of parasitized aphids. The effects of natural enemies in this system are clearly non-additive.     

Numbers,neighbors, and hungry predators: What makes chemically defended aposematic prey susceptible to predation?

Many chemically defended aposematic species are characterized by relatively low toxin levels, which enables predators to include them in their diets under certain circumstances. Knowledge of the conditions governing the survival of such prey animals—especially in the context of the co‐occurrence of similar but undefended prey, which may result in mimicry‐like interactions—is crucial for understanding the initial evolution of aposematism. In a one‐month outdoor experiment using fish (the common carp Cyprinus carpio) as predators, we examined the survival of moderately defended aposematic tadpole prey (the European common toad Bufo bufo) with varying absolute densities in single‐species prey systems or varying relative densities in two‐species prey systems containing morphologically similar but undefended prey (the European common frog Rana temporaria). The density effects were investigated in conjunction with the hunger levels of the predator, which were manipulated by means of the addition of alternative (nontadpole) food. The survival of the B. bufo tadpoles was promoted by increasing their absolute density in the single‐species prey systems, increasing their relative density in the two‐species prey systems, and providing ample alternative food for the predator. Hungry predators eliminated all R. temporaria individuals regardless of their proportion in the prey community; in treatments with ample alternative food, high relative B. bufo density supported R. temporaria survival. The results demonstrated that moderately defended prey did benefit from high population densities (both absolute and relative), even under long‐term predation pressure. However, the physiological state of the predator was a crucial factor in the survival of moderately defended prey. While the availability of alternative prey in general should promote the spread and maintenance of aposematism, the results indicated that the resemblance between the co‐occurring defended and undefended prey may impose mortality costs on the defended model species, even in the absence of actual mimicry.     

Is there any evidence that aphid alarm pheromones work as prey and host finding kairomones for natural enemies?

1. The aphid alarm pheromone (E)‐β‐farnesene (EBF) is often considered to be used by natural enemies as a prey/host finding kairomone. However, studies show opposing results, some appear to confirm an attraction of aphid natural enemies by EBF whereas others do not provide any evidence for the kairomone function of EBF. 2. To clarify if aphid natural enemies are attracted by the amounts of EBF naturally emitted by aphids, the existing literature was reviewed about EBF attractiveness to aphid natural enemies with consideration of the amounts of EBF used in the studies. 3. Thirty‐one publications that investigated the ability of EBF, aphid cornicle secretion, and attacked aphids, to attract aphid natural enemies were found. Several studies showed an attraction by EBF, but these used much higher amounts of EBF than usually emitted by aphids during a predator attack. Studies investigating EBF amounts similar to what is emitted by aphids are rare and failed to show attraction. Only two studies document an attraction of natural enemies by attacked aphids. 4. As EBF is emitted in very low amounts, not very stable, and only present after an attack, we suggest that aphid‐derived EBF is not a suitable kairomone for most natural enemy species, especially when they are able to use alternative cues. As EBF, amongst other volatiles, is also emitted by herbivore‐induced plants, we propose that natural enemies might use plant‐derived EBF as a synomone to identify aphid‐infested plants via an altered plant volatile bouquet.     

Apparent competition or apparent mutualism? An analysis of the influence of rose bush strip management on aphid population in wheat field

Abstract:  Apparent competition, mediated by a shared predator, plays a key role in conservation biological control. Appropriate agroecosystems management may favour this type of indirect interaction. In that context, our aim was to test the effect of rose bush [ Rosa rugosa (Thunb.)] strips on the building up of aphid populations and of their natural enemies in adjacent cereal habitats. Several aphid species are currently found on Rosa sp. including Metopolophium dirhodum (Walker) for which it is a primary host. Aphid predators and parasitoids may build their populations on the aphid population present on Rosa sp. and later on migrate to wheat field during the cereal aphid infestation. Moreover, the flowers of the rose bushes may provide a source of nectar and pollen to these natural enemies. Our experiment was conducted in three rose margin wheat plots with a strip of rose bushes of R. rugosa and three control plots. Plots were compared during 2 years (2003 and 2004). Aphid, parasitoid and predator densities were recorded from May to the harvest of wheat on rose bushes and in wheat. In 2003, the aphid densities were moderate but in 2004, the population of aphid was very high. Even if predator and parasitoids arrived earlier in rose margin field than in control ones, the presence of rose bushes did not influence the aphid population within the field. Metopolophium dirhodum did not seem to migrate from the rose bushes to wheat. The level of parasitism was weak in rose bushes and the natural enemy population was not different in rose margin wheat and in control plots. The causes of the lack of efficiency of this type of management are discussed as well as the high aphid population in wheat in 2004.     

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.     

Adaptive defense of pests and switching predation can improve biological control by multiple natural enemies

One of the most important questions in biological control is whether multiple natural enemies can provide greater suppression of agricultural pests than a single best enemy. Intraguild predation (IGP) among natural enemies has often been invoked to explain failure of biological control by multiple enemies, and classical theoretical studies on IGP have supported this view. However, empirical studies are inconclusive and have yielded both positive and negative results. We extend classical models by considering anti-predator behavior of pests and diet switching of omnivorous natural enemies, and examine their effects on pest control. We assume that the pest can adaptively allocate effort toward the specific defense against each predator, and that the omnivorous natural enemy can consume disproportionately more of the relatively abundant prey (switching predation) by type III functional responses to prey items. The model predicts that adaptive defense augments pests but favors introduction of multiple natural enemies for controlling pests if IGP is weak. In contrast, switching predation does not make pest control by multiple natural enemies advantageous as in classical studies, in the absence of adaptive defense. However, switching predation reduces the necessity of defense by the pest against the omnivore and offsets the effect of adaptive defense. Thus, it makes the introduction of multiple natural enemies advantageous for pest control when the pest employs adaptive defense even if IGP is strong. These results suggest that types and combinations of behavior of prey and predators may greatly affect qualitative outcomes of biological control by multiple natural enemies.     

Temporal relationships between the generalist predator,Orius insidiosus,and its two major prey in soybean

The generalist predator, Orius insidiosus (Say) is an important early-season predator of the soybean aphid, Aphis glycines Matsumura, a newly invasive pest of major concern in soybean crop management. We conducted a 3 year, multiple field study to characterize the dynamic relationships between the predator, the pest, and alternative prey in soybean. Using field sampling data, we showed that thrips were the only alternative prey to be well-established in fields prior to O. insidiosus arrival and were likely to promote predator colonization of soybean fields prior to the arrival of soybean aphid. The predator displayed a reproductive numerical response to thrips in one of the 3 years and a primarily aggregative response in another year. The predator did not respond numerically to soybean aphid in the majority of fields. Experimental manipulations of thrips populations in field plots temporarily reduced thrips densities but had a minimal effect on O. insidiosus densities, suggesting that the predator is resilient against temporary reductions in a major resource. In the 2 years O. insidiosus populations were well-established in fields prior to soybean aphid arrival, soybean aphid remained at low levels throughout the season. In the year soybean aphid arrived early with respect to the growing season and before O. insidiosus populations were established, soybean aphid reached outbreak levels in all fields. Future research efforts on the factors determining soybean aphid population dynamics need to address the relative importance of early-season soybean aphid colonization and generalist predator population dynamics on the potential for soybean aphid population outbreaks.     

Impact of wheat-mung bean intercropping on English grain aphid (Hemiptera: Aphididae) populations and its natural enemy

The effects of intercropping wheat, Triticum aestivum L., with mung bean, Vigna radiate L., on the populations of English grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae), and its natural enemies were evaluated by field and laboratory experiments. The population densities of aphids and their natural enemies were evaluated in the intercropped field against different row ratio combinations of wheat-mung bean. Results showed that wheat-mung bean intercropping caused a drop in aphid densities, and the ratio 12 wheat: 4 mung bean brought about the largest drop (> 8%). In addition, the population densities of coccinellids (ladybirds) and parasitoids and the species diversity of all the natural enemies of aphid were higher in the intercropped field than in the field planted only with wheat. However, intercropping did not influence the community indices (evenness and index of dominance concentration) of the natural enemies. Y-tube olfactometer bioassays were carried out in the laboratory to test whether odor blends of host and nonhost plants affect the host selection of S. avenae. Bioassays indicated that both apterous and alate aphids significantly preferred host plant odor over odor blends of host and intercropped species. Hence, the olfactory-based host location of aphids in the field might be affected by intercropping. The intercropping experiment clearly showed that increased crop species diversity suppresses aphid population growth and preserves the population of natural enemies of aphids. Our results also provide support for the "resource concentration hypothesis" and the "enemies hypothesis".     

Population dynamics of soybean aphid and biotic mortality at the edge of its range

The soybean aphid, Aphis glycines Matsumura, was introduced to north central North America from Asia in 2000, and it has become a major pest of soybean, Glycine max (L.) Merr. Understanding how natural enemies impact aphid populations in the field is an important component in developing a comprehensive management plan. We examined the impact of naturally occurring predators in the field by using exclusion cages during July-August 2004 and 2005. Field cages of different mesh diameters were used to exclude different sizes of natural enemies from aphid-infested plots. Plots were surveyed twice weekly for A. glycines and natural enemies. Densities were recorded. Cage effects on mean temperature and soybean growth were found to be insignificant. Significant differences in aphid density were found between treatments in both years of the study (2004 and 2005); however, aphid densities between years were highly variable. Orius insidiosus (Say) was the most commonly occurring predator in the field. Other natural enemies were present in both years but not in high numbers. Parasitoids were present in both years, but their numbers did not suppress aphid densities. Treatment differences within years were related to the abundance of natural enemies. The large differences in aphid abundance between years were associated with the higher number of O. insidiosus found in the field in 2005 (416 total O. insidiosus) than in 2004 (149 total O. insidiosus). This study suggests that naturally occurring predators, primarily O. insidiosus, can have a large impact on A. glycines populations when predator populations are established before initial A. glycines colonization.     

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.     

Aphid suppression by natural enemies in mulched cereals

Large populations of natural enemies are the basis for natural pest control. Effects of mulch on predator–prey interactions in arable fields are poorly known, despite its potential to enhance ground‐dwelling predators and thereby reduce pest infestations. We studied the densities of predators and parasitoids, and their impact on cereal aphids in the presence and absence of mulch. Released populations of the bird cherry aphid, Rhopalosiphum padi (L.) (Homoptera: Aphididae), and two naturally occurring aphid species, were monitored under experimentally reduced densities of: (i) ground‐dwelling predators, (ii) flying predators and parasitoids, and (iii) with straw mulch. The three treatments were applied in a 2 × 2 × 2 factorial design in a field of spring wheat (Triticum aestivum L.). The exclusion of ground‐dwelling predators increased aphid populations by 55% in June and 40% in July, respectively. Mulched plots had 25% lower aphid densities in June. This was presumably due to enhanced densities of spiders (Araneida) in mulched plots. The exclusion of flying predators and parasitoids led to 94% higher aphid populations in late July (109 vs. 56 individuals per 100 shoots), irrespective of mulch or ground predator manipulation. This was attributed to the larvae of gall midges Aphidoletes cf. aphidimyza (Rondani) (Diptera: Cecidomyiidae) and hoverflies (Diptera: Syrphidae). The results indicate that a scarcity of predators and a bare soil surface renders crops more susceptible to arthropod pests. Farming schemes should aim at enhancing both ground‐dwelling and flying predators for elevated levels of natural pest control.     

Lack of strong refuges allows top-down control of soybean aphid by generalist natural enemies

Refuges have been shown to be important mediators of predator–prey interactions, and in particular, have been proposed as a potential mechanism allowing herbivore populations to reach outbreak levels. However, very little research on the role of refuges has been conducted in systems dominated by generalist predators. We investigated the existence of refuges from predation for the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) at multiple scales. This species invaded North America and in spite of previous studies demonstrating strong suppression by generalist natural enemies, its populations periodically cause significant economic losses. Using naturally occurring populations of soybean aphid and its natural enemies, we tested for the presence of A. glycines spatial and dynamic refuges at the within-field, single plant, and within-plant scale. At the within-field level, we found only weak and transient spatial patterns in aphid populations suggesting the lack of spatial refuges at this scale. Similarly, at the plant level we found no individual colonies that escaped predation and aphid suppression was 9- to 28-fold greater in comparison with caged controls regardless of initial aphid density. When high aphid populations were exposed to predation they were rapidly reduced to levels close to the average field density and showed reduced per capita growth rates, indicating an absence of dilution of predation risk at increased aphid density. Finally, we found a significant shift in the distribution of aphids to the lower portions of the plant in the presence of generalist predators, suggesting a partial refuge from predation at the within-plant scale. Overall, we found the naturally occurring community of generalist predators to exert strong top-down suppression of soybean aphid populations at multiple scales, and no evidence that the presence of refuges at the scales studied can lead to outbreak populations. The partial refuge from predation at the within-plant scale revealed in our study may have important consequences for the within-season population dynamics of A. glycines, since it may be associated with low plant quality tradeoffs, and therefore warrants further research.     

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.     

Aggregation of polyphagous predators in response to multiple prey: ladybirds (Coleoptera: Coccinellidae) foraging in alfalfa

The spatial distribution of polyphagous predators may often reflect the integration of aggregative responses to local densities of multiple species of prey, and as such may have consequences for the indirect linkages among the prey sharing these predators. In a factorial field experiment in which we manipulated local prey densities within a field of alfalfa in Utah (USA), we tested whether aphidophagous ladybirds would aggregate not only in response to their primary aphid prey, but also in response to an abundant alternative prey, the alfalfa weevil (Hypera postica [Gyllenhal]). Native North American ladybirds (primarily Hippodamia convergens Guerin and H. quinquesignata quinquesignata [Kirby]) responded only to spatial variation in aphid density. In contrast, the introduced ladybird, Coccinella septempunctata L., aggregated also at local concentrations of the weevil late in the experiment when weevil density was high and aphid density was relatively low throughout all experimental plots. The results support the hypothesis that C. septempunctata is more responsive than are native ladybirds to the availability of alternative prey in alfalfa, which may account in part for the displacement of native ladybirds from alfalfa by the introduced species as aphid numbers have declined. The differing responses of the native and introduced ladybirds to spatial patterns of the alternative prey underscore the importance of extending the study of predator aggregation to understand better how polyphagous predators distribute themselves in response to spatial patterns of multiple species of potential prey.     

Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control

In agroecosystems, parasitoids and predators may exert top-down regulation and predators for different reasons may avoid or give preference to parasitised prey, i.e., become an intraguild predator. The success of pest suppression with multiple natural enemies depends essentially on predator–prey dynamics and how this is affected by the interplay between predation and parasitism. We conducted a simple laboratory experiment to test whether predators distinguished parasitised prey from non-parasitised prey and to study how parasitism influenced predation. We used a host-parasitoid system, Spodoptera frugiperda and one of its generalist parasitoids, Campoletis flavicincta, and included two predators, the stinkbug Podisus nigrispinus and the earwig Euborellia annulipes. In the experiment, predators were offered a choice between non-parasitised and parasitised larvae. We observed how long it took for the predator to attack a larva, which prey was attacked first, and whether predators opted to consume the other prey after their initial attack. Our results suggest that, in general, female predators are less selective than males and predators are more likely to consume non-parasitised prey with this likelihood being directly proportional to the time taken until the first prey attack. We used statistical models to show that males opted to consume the other prey with a significantly higher probability if they attacked a parasitised larva first, while females did so with the same probability irrespective of which one they attacked first. These results highlight the importance of studies on predator–parasitoid interactions, as well as on coexistence mechanisms in agroecosystems. When parasitism mediates predator choice so that intraguild predation is avoided, natural enemy populations may be larger, thus increasing the probability of more successful biological control.     

The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism

Natural enemies not only influence prey density but they can also cause the modification of traits in their victims. While such non-lethal effects can be very important for the dynamic and structure of prey populations, little is known about their interaction with the density-mediated effects of natural enemies. We investigated the relationship between predation rate, prey density and trait modification in two aphid-aphid predator interactions. Pea aphids (Acyrthosiphon pisum, Harris) have been shown to produce winged dispersal morphs in response to the presence of ladybirds or parasitoid natural enemies. This trait modification influences the ability of aphids to disperse and to colonise new habitats, and hence has a bearing on the population dynamics of the prey. In two experiments we examined wing induction in pea aphids as a function of the rate of predation when hoverfly larvae (Episyrphus balteatus) and lacewing larvae (Chrysoperla carnea) were allowed to forage in pea aphid colonies. Both hoverfly and lacewing larvae caused a significant increase in the percentage of winged morphs among offspring compared to control treatments, emphasising that wing induction in the presence of natural enemies is a general response in pea aphids. The percentage of winged offspring was, however, dependent on the rate of predation, with a small effect of predation on aphid wing induction at very high and very low predation rates, and a strong response of aphids at medium predation rates. Aphid wing induction was influenced by the interplay between predation rate and the resultant prey density. Our results suggests that density-mediated and trait-mediated effects of natural enemies are closely connected to each other and jointly determine the effect of natural enemies on prey population dynamics.     

Natural enemies act faster than endophytic fungi in population control of cereal aphids

1. Fast-growing populations of phytophagous insects can be limited by the presence of natural enemies and by alkaloids that are produced by symbiotic associations of many temperate grass species with endophytic fungi. It is unclear if and how acquired plant defences derived from endophytic fungi interact with natural enemies to affect phytophagous insect populations. 2. To assess the relative importance of endophytic fungi compared to that of natural enemies on the population dynamics of phytophagous insects, we carried out a fully factorial field experiment, in which the presence of natural enemies and the presence of endophytic fungi were manipulated simultaneously. Target colonies of aphids were monitored for 8 weeks starting from their natural appearance in the field to the end of the aphid season. 3. We show that on Lolium perenne increased natural enemy densities reduced the individual numbers of two common cereal aphids, Rhopalosiphum padi and Metopolophium festucae. 4. The presence of the endophytic fungi Neotyphodium lolii reduced the number of M. festucae but did not affect the number of R. padi. The reduction in R. padi numbers by predators and parasitoids was not influenced by the presence of endophytes. For adult M. festucae, however, the negative effects of natural enemies were significant only in the absence of endophytes. 5. Over the duration of the experiment, the effect of natural enemies on aphid colony growth was much stronger than the effect of the endophytic fungi N. lolii, presumably because predator and parasitoid action on aphid colonies is much faster than any effects of endophytes. 6. Our results demonstrate that with simultaneous action of acquired endosymbionts and natural enemies, both factors can control aphid colony growth but they generally act independently of each other.     

Changes in herbivore control in arable fields by detrital subsidies depend on predator species and vary in space

Prey from the decomposer subsystem may help sustain predator populations in arable fields. Adding organic residues to agricultural systems may therefore enhance pest control. We investigated whether resource addition (maize mulch) strengthens aboveground trophic cascades in winter wheat fields. Evaluating the flux of the maize-borne carbon into the food web after 9 months via stable isotope analysis allowed differentiating between prey in predator diets originating from the above- and belowground subsystems. Furthermore, we recorded aphid populations in predator-reduced and control plots of no-mulch and mulch addition treatments. All analyzed soil dwelling species incorporated maize-borne carbon. In contrast, only 2 out of 13 aboveground predator species incorporated maize carbon, suggesting that these 2 predators forage on prey from the above- and belowground systems. Supporting this conclusion, densities of these two predator species were increased in the mulch addition fields. Nitrogen isotope signatures suggested that these generalist predators in part fed on Collembola thereby benefiting indirectly from detrital resources. Increased density of these two predator species was associated by increased aphid control but the identity of predators responsible for aphid control varied in space. One of the three wheat fields studied even lacked aphid control despite of mulch-mediated increased density of generalist predators. The results suggest that detrital subsidies quickly enter belowground food webs but only a few aboveground predator species include prey out of the decomposer system into their diet. Variation in the identity of predator species benefiting from detrital resources between sites suggest that, depending on locality, different predator species are subsidised by prey out of the decomposer system and that these predators contribute to aphid control. Therefore, by engineering the decomposer subsystem via detrital subsidies, biological control by generalist predators may be strengthened.     

Contrasting effects of natural habitat loss on generalist and specialist aphid natural enemies

The greater susceptibility of higher trophic levels to habitat loss has been demonstrated to disrupt important trophic interactions such as consumer control of prey populations. This pattern is predicted to break down for generalist species that can use matrix habitats, yet empirical studies comparing generalist and specialist enemy pressure in response to natural habitat loss are lacking. Here we examined the effects of landscape simplification resulting from habitat conversion to agriculture on nettles, Urtica dioica , their specialized aphid herbivore, Microlophium carnosum , and associated natural enemies that varied broadly in their degree of specialization. Both nettles and their specialized aphid herbivore were significantly more abundant in complex than simple landscapes. Different enemy groups showed contrasting responses. Aphid specialists (parasitic wasps and cecidomyiid midges) reached higher densities in complex than simple landscapes, and this effect was primarily related to shifts in local resource abundance (i.e. nettle aphid densities). In contrast, densities of generalists (coccinellid beetles and spiders) were significantly higher in simple landscapes, presumably due to spillover of generalists from surrounding cropland habitats. Natural enemy-prey ratios did not differ significantly across landscape types for specialist groups but were significantly higher in simple than complex landscapes for generalist groups, suggesting that enemy pressure on nettle aphids likely increases with landscape simplification. This was supported by our finding that aphid population growth rates were lower in simple than complex landscapes, and declined significantly with increasing coccinellid densities. Thus, in marked contrast to previous work, our results suggest that natural habitat loss may augment rather than disrupt consumer–prey interactions, and this will depend greatly on the degree of specialization of functionally dominant natural enemies.     

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.