Parasitoids follow herbivorous insects to a novel host plant,generalist predators less so

The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.     

Enemy free space and the structure of ecological communities

We define 'enemy free space' as ways of living that reduce or eliminate a species' vulnerability to one or more species of natural enemies. Many aspects of species' niches, in ecological and evolutionary time have apparently been moulded by interactions with natural enemies for enemy free space. We review a large number of examples. Yet many ecologists continue to think and write as though classical resource based competition for food or space is the primary determinant of species' niches. Often it is not. The recognition that the struggle for enemy free space is an important component of many species' ecologies may have important consequences for studies of community convergence, limits to species packing, and the ratio of predator species to prey species in natural communities.     

Carbon dioxide effects on stomatal responses to the environment and water use by crops under field conditions

The structural complexity of habitats has been espoused as an important factor influencing natural-enemy abundance and food-web dynamics in invertebrate-based communities, but a rigorous synthesis of published studies has not heretofore been conducted. We performed a meta-analytical synthesis of the density response of natural enemies (invertebrate predators and parasitoids) to experimental increases and decreases in the structural complexity of their habitats using data from 43 published studies, reporting 62 independent taxa. Studies varied in structural complexity at two spatial scales (habitat and within-plant architecture) and comprised a diverse array of natural-enemy taxa (natural-enemy assemblage at large, the entire spider assemblage, hunting spiders, web-building spiders, mites, hemipterans, coccinellid beetles, carabid beetles, ants, and parasitoids). For all taxa combined, increasing habitat structure resulted in a large and significant increase in natural enemy abundance. Similarly, decreasing habitat structure significantly diminished natural enemy abundance. Separate meta-analyses at two spatial scales (habitat and within-plant architecture) found that increasing habitat complexity resulted in significant increases in abundance. In particular, manipulating levels of detritus at the habitat spatial scale had the strongest effect on natural enemy abundance. In general, most guilds of natural enemies were significantly affected when the structural complexity of the habitat was altered. Seven of nine natural enemy guilds were more abundant under conditions of increased habitat complexity, with hunting spiders and web-building spiders showing the strongest response followed by hemipterans, mites, and parasitoids. Spiders in particular were negatively affected when habitat structure was simplified. The mechanisms underlying the accumulation of natural enemies in complex-structured habitats are poorly known. However, refuge from intraguild predation, more effective prey capture, and access to alternative resources (alternative prey, pollen, or nectar), are possible candidates. Our analysis was unable to confirm that predators aggregate in complex-structured habitats because prey (mostly herbivores) are more abundant there. The results of this meta-analysis support the view that basal resources mediate top-down impacts on herbivores, and provide encouragement that manipulations of habitat complexity can be made in agroecosystems that will enhance the effectiveness of the natural enemy complex for more effective pest suppression.Electronic Supplementary Material Supplementary material is available in the online version of this article at     

Divergent pheromone-mediated insect behaviour under global atmospheric change

While the effects of global atmospheric changes on vegetation and resulting insect populations(‘bottom‐up interactions’) are being increasingly studied, how these gases modify interactions among insects and their natural enemies (‘top‐down interactions’) is less clear. As natural enemy efficacy is governed largely by behavioural mechanisms, altered prey finding and prey defence may change insect population dynamics. Here we show that pheromone‐mediated escape behaviours, and hence the vulnerability of insects to natural enemies, are divergent under atmospheric conditions associated with global climate change. Chaitophorus stevensis, a common aphid on trembling aspen trees, Populus tremuloides, have diminished escape responses in enriched carbon dioxide (CO₂) environments, while those in enriched ozone (O₃) have augmented escape responses, to alarm pheromone. These results suggest that divergent pheromone‐mediated behaviours could alter predator–prey interactions in future environments.     

Understanding biodiversity effects on prey in multi-enemy systems

Biodiversity–ecosystem functioning theory would predict that increasing natural enemy richness should enhance prey consumption rate due to functional complementarity of enemy species. However, several studies show that ecological interactions among natural enemies may result in complex effects of enemy diversity on prey consumption. Therefore, the challenge in understanding natural enemy diversity effects is to predict consumption rates of multiple enemies taking into account effects arising from patterns of prey use together with species interactions. Here, we show how complementary and redundant prey use patterns result in additive and saturating effects, respectively, and how ecological interactions such as phenotypic niche shifts, synergy and intraguild predation enlarge the range of outcomes to include null, synergistic and antagonistic effects. This study provides a simple theoretical framework that can be applied to experimental studies to infer the biological mechanisms underlying natural enemy diversity effects on prey.     

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.     

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.     

Assessing the impact of arthropod natural enemies on crop pests at the field scale

There are many reasons why it is important that we find ways to conserve, and better utilize natural enemies of invertebrate crop pests. Currently, measures of natural enemy impact are rarely incorporated into studies that purport to examine pest control. Most studies examine pest and natural enemy presence and/or abundance and then qualitatively infer impact. While this provides useful data to address a range of ecological questions, a measure of impact is critical for guiding pest management decision‐making. Often some very simple techniques can be used to obtain an estimate of natural enemy impact. We present examples of field‐based studies that have used cages, barriers to restrict natural enemy or prey movement, direct observation of natural enemy attack, and sentinel prey items to estimate mortality. The measure of natural enemy impact used in each study needs to be tailored to the needs of farmers and the specific pest problems they face. For example, the magnitude of mortality attributed to natural enemies may be less important than the timing and consistency of that mortality between seasons. Tailoring impact assessments will lead to research outcomes that do not simply provide general information about how to conserve natural enemies, but how to use these natural enemies as an integral part of decision‐making.     

广聚萤叶甲和豚草卷蛾对广西来宾豚草的联合控制作用

【背景】豚草已成功入侵广西来宾,对当地生物多样性、农业生产和居民健康造成了严重影响。广聚萤叶甲和豚草卷蛾均为豚草的重要专一性天敌,在湖南等地已有效抑制了豚草的扩散蔓延。【方法】为考查2种天敌在广西对豚草的联合控制作用,于2009年5月24日在广西来宾豚草入侵地区同时释放广聚萤叶甲和豚草卷蛾(2种天敌释放密度均为1170头.hm-2)。【结果】至2009年8月29日释放区内豚草植株死亡率达98%以上,且天敌迅速向邻近豚草发生区扩散,2种天敌对扩散区豚草的控制率可达50%～60%。【结论与意义】2种天敌对豚草具有显著的控制效果,建议在广西大面积推广应用。     

Predation risk cues associated with killed conspecifics affect the behavior and reproduction of prey animals

Organisms often perceive risk to be attacked by natural enemies through cues that accompany or persist after attacks on conspecifics. Under the risk of attack, preys may prioritize anti-enemy behaviours, sacrificing their feeding activities. These enemy-induced changes can affect the prey population growth. The presence of killed congeners is a past attack events cue but, in terrestrial prey–enemy systems, its effect on prey population biology is an open question. This was addressed here by studying both the space use and reproductive effort of aphids exposed to congeners killed by parasitoids. To test whether preys adjust their responses with the threat intensity, aphids' responses in presence of killed conspecifics were compared to those measured when directly exposed to non-consumptive parasitoids. The results showed that killed congeners are perceived by aphids and led to both changes in their space use and a strong decline in their population size. This experiment is the first to demonstrate that the presence of congeners killed by an enemy can contribute to the suppressive effects of natural enemies on prey populations.     

Defence against multiple enemies

Although very common under natural conditions, the consequences of multiple enemies (parasites, predators, herbivores, or even 'chemical' enemies like insecticides) on investment in defence has scarcely been investigated. In this paper, we present a simple model of the joint evolution of two defences targeted against two enemies. We illustrate how the respective level of each defence can be influenced by the presence of the two enemies. Furthermore, we investigate the influences of direct interference and synergy between defences. We show that, depending on certain conditions (costs, interference or synergy between defences), an increase in selection pressure by one enemy can have dramatic effects on defence against another enemy. It is generally admitted that increasing the encounter rate with a second natural enemy can decrease investment in defence against a first enemy, but our results indicate that it may sometimes favour resistance against the first enemy. Moreover, we illustrate that the global defence against one enemy can be lower when only this enemy is present: this has important implications for experimental measures of resistance, and for organisms that invade an area with less enemies or whose community of enemies is reduced. We discuss possible implications of the existence of multiple enemies for conservation biology, biological control and chemical control.     

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.     

Meta-analysis of tree diversity effects on the abundance,diversity and activity of herbivores' enemies

The natural enemies hypothesis predicts that the abundance and diversity of antagonists such as predators and parasitoids of herbivores increases with the diversity of plants, which can lead to more effective top-down control of insect herbivores. However, although the hypothesis has received large support in agricultural systems, fewer studies have been conducted in forest ecosystems and a comprehensive synthesis of previous research is still lacking.We conducted a meta-analysis of 65 publications comparing the diversity, abundance or activity of various groups of natural enemies (including birds, bats, spiders and insect parasitoids) in pure vs. mixed forest stands. We tested the effects of forest biome, natural enemy taxon and type of study (managed vs experimental forest).We found a significant positive effect of forest tree diversity on natural enemy abundance and diversity but not on their activity. The effect of tree diversity on natural enemies was stronger towards lower latitudes but was not contingent on the natural enemy taxon level.Overall, our study contributes toward a better understanding of the “natural enemies hypothesis” in forest systems and provides new insights about the mechanisms involved. Furthermore, we outline potential avenues for strengthening forest resistance to the growing threat of herbivorous insects.     

The dynamics of predation and competition in patchy environments

The model of N. D. Atkinson and B. Shorrocks (J. Anim. Ecol. 50, 461–471 (1981)) as two competing species distributing their progeny amongst patches according to independent negative binomial distributions. The resulting separation of the species increases the likelihood of coexistence. We have assumed a much simpler distribution of the competitors which has enabled us to explore analytically the dynamics of interactions with two competing species and a shared natural enemy in a patchy environment. Two types of natural enemy have been considered: a generalist predator whose dynamics are uncoupled from those of the two prey species, and a specialist (e.g., a parasitoid) whose dynamics are entirely coupled to those of its two prey. The following conclusions emerge. Non-aggregating generalist predators causing random predation across patches are generally destabilizing (although asymmetrical predation may in some case enhance coexistence as a result of preferential predation on the superior competitor). Predator aggregation in patches of high prey density, however, produces a switching effect which tends to promote stability. Coexistence is now even possible with high degrees of correlation in the distribution of the two prey and in situations of extreme competition where the competition coefficients exceed one. The main difference in the models with a specialist parasitoid as the natural enemy is a reduction in stability compared with the equivalent generalist-prey interaction. But stable coexistence can still readily occur if the natural enemies aggregate markedly in patches of high prey density.     

Is invasion success explained by the enemy release hypothesis?

A recent trend in invasion ecology relates the success of non‐indigenous species (NIS) to reduced control by enemies such as pathogens, parasites and predators (i.e. the enemy release hypothesis, ERH). Despite the demonstrated importance of enemies to host population dynamics, studies of the ERH are split – biogeographical analyses primarily show a reduction in the diversity of enemies in the introduced range compared with the native range, while community studies imply that NIS are no less affected by enemies than native species in the invaded community. A broad review of the invasion literature implies at least eight non‐exclusive explanations for this enigma. In addition, we argue that the ERH has often been accepted uncritically wherever (i) NIS often appear larger, more fecund, or somehow ‘better’ than either congeners in the introduced region, or conspecifics in the native range; and (ii) known enemies are conspicuously absent from the introduced range. However, all NIS, regardless of their abundance or impact, will lose natural enemies at a biogeographical scale. Given the complexity of processes that underlie biological invasions, we argue against a simple relationship between enemy ‘release’ and the vigour, abundance or impact of NIS.     

Nonlinearities Lead to Qualitative Differences in Population Dynamics of Predator-Prey Systems

Since typically there are many predators feeding on most herbivores in natural communities, understanding multiple predator effects is critical for both community and applied ecology. Experiments of multiple predator effects on prey populations are extremely demanding, as the number of treatments and the amount of labour associated with these experiments increases exponentially with the number of species in question. Therefore, researchers tend to vary only presence/absence of the species and use only one (supposedly realistic) combination of their numbers in experiments. However, nonlinearities in density dependence, functional responses, interactions between natural enemies etc. are typical for such systems, and nonlinear models of population dynamics generally predict qualitatively different results, if initial absolute densities of the species studied differ, even if their relative densities are maintained. Therefore, testing combinations of natural enemies without varying their densities may not be sufficient. Here we test this prediction experimentally. We show that the population dynamics of a system consisting of 2 natural enemies (aphid predator Adalia bipunctata (L.), and aphid parasitoid, Aphidius colemani Viereck) and their shared prey (peach aphid, Myzus persicae Sulzer) are strongly affected by the absolute initial densities of the species in question. Even if their relative densities are kept constant, the natural enemy species or combination thereof that most effectively suppresses the prey may depend on the absolute initial densities used in the experiment. Future empirical studies of multiple predator – one prey interactions should therefore use a two-dimensional array of initial densities of the studied species. Varying only combinations of natural enemies without varying their densities is not sufficient and can lead to misleading results.     

Effect of landscape composition and arrangement on biological control agents in a simplified agricultural system: A cost–distance approach

Landscape simplification has been clearly demonstrated to have negative impacts on the in-crop density and biological-control activity of natural enemies in agricultural landscapes. The role of spatial arrangement of the landscape, however, has not been investigated in agroecosystems. We applied cost–distance modeling to investigate the relationship between the in-crop density of natural enemies and the structural connectivity of non-crop land uses surrounding crops within Australian cotton landscapes. We further compared the explanatory power of this approach with the more commonly used spatially specific proportional-area approach, which considers landscape composition in terms of the proportional area of a given land use within a given radius. Cost–distance metrics offered a more significant explanation of in-crop density for the predatory beetle Dicranolaius bellulus (Coleoptera: Melyridae) than did the proportional-area approach. The in-crop density for this species was positively and significantly correlated with the connectivity of wooded land uses within a 3000 m radius. However, for natural enemy taxa that responded to landscape characteristics at smaller spatial scales (within a 750 m radius), namely Oxyopes spp. (Araneae: Oxyopidae) and Trichogramma spp., (Hymenoptera: Trichogrammatidae), the proportional-area approach gave a more significant explanation of in-crop density. Herbivore taxa responded weakly to proportional area at all scales and showed no correlation to cost–distance metrics. Findings indicate potential for simplified agricultural landscapes to be ‘selectively’ manipulated to enhance colonization of the crop by natural enemies, but not herbivores, by improving connectivity between crops and non-crop resources, through the presence of woody vegetation.     

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.     

An entomophage park to promote natural enemy diversity

Undisturbed habitats of natural vegetation near agricultural areas protect and enhance specific natural enemies and provide them with resources such as nectar, pollen, physical refuge, alternative prey, alternative hosts and mating sites. In order to reduce the pesticide-induced mortality of natural enemies and to improve natural enemy fitness and effectiveness, one such area (termed an ‘entomophage park’) was established at the Sher-e-Kashmir University of Agricultural Sciences and Technology of Jammu, at Chatha, India in 2007. Naturally occurring plants, weeds, cultivated crops and flowers were monitored regularly for natural enemies. Seven sampling methods were employed to compare the abundance of natural enemies in the entomophage park and adjoining crop fields. Both entomophage diversity and abundance in the park were much higher than in the adjacent agricultural fields of vegetables and cereals. A total of 61 species of natural enemies were recovered from the entomophage park, as compared to 22 and 20 species in cereal and vegetable fields, respectively. The abundance of parasitoids (ichneumonids, braconids, scelionids and chalcidoids) was significantly higher in the park as compared to surveyed agricultural fields, as was egg parasitism by scelionids (Telenomus spp.) and trichogrammatids, and parasitisation by the larval parasitoid Campoletis chlorideae on Helicoverpa armigera. The entomophage park also significantly enhanced the fecundity and survival of the ichneumonid C. chlorideae, when compared to individuals collected from vegetable and cereal fields. Seventeen species of plants were recorded as ‘insectary plants' (one providing substantial floral resources) in the entomophage park. Such parks may play an important role in maintaining the biodiversity of natural enemies and enhancing natural pest control.     

Influence of leaf trichome density on the efficiency of two polyphagous insect predators

Plant characteristics, such as leaf structure or hairiness, are important for the movement and attachment of insects. It has been suggested that increased trichome density on new Salix cinerea L. (Salicaceae) leaves, produced after grazing by the willow leaf beetle Phratora vulgatissima L. (Coleoptera: Chrysomelidae), function as an inducible defence against the beetle and especially its larvae. Here we studied whether and how two of the main natural enemies of P. vulgatissima, viz., Anthocoris nemorum L. (Heteroptera: Anthocoridae) and Ortothylus marginalis L. (Heteroptera: Miridae), were influenced by trichome density on S. cinerea leaves. The effect of trichome density on these two predators was studied on plants with different trichome densities, comparing natural enemy efficiency, measured as number of P. vulgatissima eggs consumed or larvae missing and/or killed. To obtain different trichome densities, cuttings of several different clones of S. cinerea were used. In the experiment using eggs as prey, an increase in trichome density was, in addition, induced through leaf beetle defoliation on half of the plants of each willow clone. Furthermore, a field study was performed to investigate whether trichome density was correlated with natural enemy abundance. The results indicate that neither the efficiency of these two natural enemies in the greenhouse, nor their abundance in the field was influenced by trichome density. A well‐known behavioural difference between the two predator species could probably account for the higher disappearance of larvae after exposure to the more active predator. These findings are relevant for the development of pest management programs, not least because the enemies are polyphagous predators. It is concluded that an induced increase in leaf hairiness in willows in response to leaf beetle grazing could be a plant resistance trait worthy of further study in this system, because no negative effects on the main natural enemies were observed.