Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.     

大蒜-小白菜间作套种对菜田节肢动物功能团的影响

2004年9-11月于福建省琅岐岛针对大蒜与小白菜间作(CG1)套种(CG2)对节肢动物群落功能团影响进行调查和分析。结果显示:CG1提高了植食性昆虫、寄生性和捕食性天敌丰盛度,CG2可在降低植食性昆虫数量的同时提高寄生性天敌的数量;多作田寄生性天敌物种丰富度、丰盛度和多样性指数均高于单作田;优势类群动态表现为菜蚜茧蜂与蚜虫种群在CG1出现"天敌跟随现象",多作田在整个生长期都有利于提高捕食者球腹蛛的控制效能;中性昆虫在生长前期和中期是菜蚜虫茧蜂和球腹蛛的替代寄主或猎物。因此合理的间作或套种,有利于提高菜田生境的多样化,强化自然天敌对害虫的生态控制作用。     

Geographical variation in food web structure in Nepenthes pitcher plants

Abstract. 1. Relative to Nepenthes species in West Malaysia near the evolutionary centre of the genus, outlying species of Nepenthes in the Seychelles, Sri Lanka and Madagascar have fewer species of both prey and predator living in them, fewer and smaller guilds of species, much apparently empty niche space, less complex food webs, and a greater connectance. The ratios of prey to predators, and of connectance (C₁) to the total number of trophic types present remain approximately constant.
2. Differences between the food webs appear to be related in a complex way to the size of the country and its degree of spatial and temporal isolation, the size of the local species pool capable of colonizing the pitchers, and the number of Nepenthes species present. However, the maximal length of food chains in the richest and most complex food webs is probably limited by energetic constraints or environmental predictability.
3. The data may illustrate how food webs change to become more complex, both by the addition of new guilds of species and the addition of species to existing guilds, while at the same time certain properties of the food web are kept approximately constant.     

Indirect Interactions in the High Arctic

Indirect interactions as mediated by higher and lower trophic levels have been advanced as key forces structuring herbivorous arthropod communities around the globe. Here, we present a first quantification of the interaction structure of a herbivore-centered food web from the High Arctic. Targeting the Lepidoptera of Northeast Greenland, we introduce generalized overlap indices as a novel tool for comparing different types of indirect interactions. First, we quantify the scope for top-down-up interactions as the probability that a herbivore attacking plant species i itself fed as a larva on species j. Second, we gauge this herbivore overlap against the potential for bottom-up-down interactions, quantified as the probability that a parasitoid attacking herbivore species i itself developed as a larva on species j. Third, we assess the impact of interactions with other food web modules, by extending the core web around the key herbivore Sympistis nigrita to other predator guilds (birds and spiders). We find the host specificity of both herbivores and parasitoids to be variable, with broad generalists occurring in both trophic layers. Indirect links through shared resources and through shared natural enemies both emerge as forces with a potential for shaping the herbivore community. The structure of the host-parasitoid submodule of the food web suggests scope for classic apparent competition. Yet, based on predation experiments, we estimate that birds kill as many (8%) larvae of S. nigrita as do parasitoids (8%), and that spiders kill many more (38%). Interactions between these predator guilds may result in further complexities. Our results caution against broad generalizations from studies of limited food web modules, and show the potential for interactions within and between guilds of extended webs. They also add a data point from the northernmost insect communities on Earth, and describe the baseline structure of a food web facing imminent climate change.     

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.     

The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

Structure and vertical stratification of plant galler–parasitoid food webs in two tropical forests

Abstract 1. Networks of feeding interactions among insect herbivores and natural enemies such as parasitoids, describe the structure of these assemblages and may be critically linked to their dynamics and stability. The present paper describes the first quantitative study of parasitoids associated with gall‐inducing insect assemblages in the tropics, and the first investigation of vertical stratification in quantitative food web structure. 2. Galls and associated parasitoids were sampled in the understorey and canopy of Parque Natural Metropolitano in the Pacific forest, and in the understorey of San Lorenzo Protected Area in the Caribbean forest of Panama. Quantitative host–parasitoid food webs were constructed for each assemblage, including 34 gall maker species, 28 host plants, and 57 parasitoid species. 3. Species richness was higher in the understorey for parasitoids, but higher in the canopy for gall makers. There was an almost complete turnover in gall maker and parasitoid assemblage composition between strata, and the few parasitoid species shared between strata were associated with the same host species. 4. Most parasitoid species were host specific, and the few polyphagous parasitoid species were restricted to the understorey. 5. These results suggest that, in contrast to better‐studied leaf miner–parasitoid assemblages, the influence of apparent competition mediated by shared parasitoids as a structuring factor is likely to be minimal in the understorey and practically absent in the canopy, increasing the potential for coexistence of parasitoid species. 6. High parasitoid beta diversity and high host specificity, particularly in the poorly studied canopy, indicate that tropical forests may be even more species rich in hymenopteran parasitoids than previously suspected.     

The impact of an ant–aphid mutualism on the functional composition of the secondary parasitoid community

1. Mutualistic and antagonistic interactions, although often studied independently, may affect each other, and food web dynamics are likely to be determined by the two processes working in concert. 2. The structure, and hence dynamics, of food webs depends on the relative abundances of generalist and specialist feeding guilds. Secondary parasitoids of aphids can be divided into two feeding guilds: (i) the more specialised endoparasitoids, which attack the primary parasitoid larvae in the still living aphid, and (ii) the generalist ectoparasitoids, which attack the pre‐pupa of the primary or secondary parasitoid in the mummified aphid. 3. We studied the effect of an ant–aphid mutualism on the relative abundance of these two functional groups of secondary parasitoids. We hypothesised that generalists will be negatively affected by the presence of ants, thus leading to a greater dominance of specialists. 4. We manipulated the access of ants (Lasius niger) to aphid colonies in which we placed parasitised aphids. Aphid mummies were collected and reared to determine the levels of endo‐ and ecto‐secondary parasitism. 5. When aphids were attended by L. niger the proportion of secondary parasitism by ectoparasitoids dropped from 26 to 8% of the total number of parasitised aphids, with Pachyneuron aphidis most strongly affected, while endoparasitoids as a group did not respond. However, among these Syrphophagus mamitus profited from ant attendance becoming the dominant secondary parasitoid, while parasitisation rates of Alloxysta and Phaenoglyphis declined. 6. The shift to S. mamitus as dominant secondary parasitoid in ant‐attended aphid colonies is likely due to the behavioural plasticity of this species in response to ant aggression, and a release from tertiary parasitism by generalist ectoparasitoids. 7. The reduction of secondary parasitism by generalist ectoparasitoids reduces the potential for apparent competition among primary parasitoids with consequences for the dynamics of the wider food web.     

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.     

Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest

Quantitative food webs were constructed to explore the community structure of leaf-mining moths in the family Gracillariidae and their parasitoid wasps in a deciduous forest in Hokkaido, Japan. A whole food web was constructed from data collected from June to October 2001. In the web, 16 leafminer species on seven tree species were attacked by 58 species of hymenopteran parasitoid; 376 links between leafminers and parasitoids were observed. Leafminers were specialist herbivores, but most parasitoids were generalists. Five webs were constructed for the seasonal prevalence of leafminers over the one-year period to reveal the temporal dynamics in community structure. Among the seasonal webs, the first web in June was distinctive because two tree species, Japanese umbrella tree Magnolia obovata and Japanese magnolia M. kobus, supported the community. Second to fourth webs from July to September were dominated by the leafminer species on Japanese oak Quercus crispula, and the fifth web was marked by that on Carpinus cordata. The extent of potential apparent competition among leafminers was evaluated using quantitative parasitoid overlap diagrams. These diagrams suggested that abundant host species are likely to have large indirect effects on less abundant species. Moreover, the potential for apparent competition between leafminer species inhabiting different host tree species can occur, although leafminers sharing the same tree species are prone to interact via shared parasitoids. In this system, particular leafminer species, acting as potential sources of apparent competition, can affect other species as sinks, and control whole-community dynamics. Directed apparent competition may potentially occur around oak trees.     

Quantitative food webs of dipteran leafminers and their parasitoids in Argentina

The quantitative structure of two host–parasitoid communities based on leaf-mining flies (Diptera, Agromyzidae) in Argentina is described. The two communities consisted of 29 and 27 hosts, 46 and 40 parasitoids, and 193 and 179 recorded host–parasitoid associations. Also, food webs were constructed for one community based solely on samples taken in the wet and dry seasons. Data were expressed as quantitative food webs, and the manner in which food web properties, such as connectance and compartmentalization, were influenced by sampling intensity was explored. The potential importance of indirect effects between hosts mediated by parasitoids (e.g. apparent competition) was assessed using quantitative parasitoid overlap diagrams. The studys results suggest that indirect effects are likely to be important in these highly connected communities. The limitations of the studys analysis, and how the conclusions can be tested experimentally, are discussed.     

Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.     

The Role of Natural Enemy Foraging Guilds in Controlling Cereal Aphids in Michigan Wheat

Insect natural enemies (predators and parasitoids) provide important ecosystem services by suppressing populations of insect pests in many agricultural crops. However, the role of natural enemies against cereal aphids in Michigan winter wheat (Triticum aestivum L.) is largely unknown. The objectives of this research were to characterize the natural enemy community in wheat fields and evaluate the role of different natural enemy foraging guilds (foliar-foraging versus ground-dwelling predators) in regulating cereal aphid population growth. We investigated these objectives during the spring and summer of 2012 and 2013 in four winter wheat fields on the Michigan State University campus farm in East Lansing, Michigan. We monitored and measured the impact of natural enemies by experimentally excluding or allowing their access to wheat plants infested with Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hemiptera: Aphidae). Our results indicate that the natural enemy community in the wheat fields consisted mostly of foliar-foraging and ground-dwelling predators with relatively few parasitoids. In combination, these natural enemy groups were very effective at reducing cereal aphid populations. We also investigated the role of each natural enemy foraging guild (foliar-foraging versus ground-dwelling predators) independently. Overall, our results suggest that, in combination, natural enemies can almost completely halt early-season aphid population increase. Independently, ground-dwelling predators were more effective at suppressing cereal aphid populations than foliar-foraging predators under the conditions we studied. Our results differ from studies in Europe and the US Great Plains where foliar foraging predators and parasitoids are frequently more important cereal aphid natural enemies.     

Effect of scavenging on predation in a food web

Scavenging can have important consequences for food web dynamics, for example, it may support additional consumer species and affect predation on live prey. Still, few food web models include scavenging. We develop a dynamic model that includes two facultative scavenger species, which we refer to as the predator or scavenger species according to their natural scavenging propensity, as well as live prey, and a carrion pool to show ramifications of scavenging for predation in simple food webs. Our modeling suggests that the presence of scavengers can both increase and decrease predator kill rates and overall predation in model food webs and the impact varies (in magnitude and direction) with context. In particular, we explore the impact of the amount of dynamics (exploitative competition) allowed in the predator, scavenger, and prey populations as well as the direction and magnitude of interference competition between predators and scavengers. One fundamental prediction is that scavengers most likely increase predator kill rates, especially if there are exploitative feedback effects on the prey or carrion resources like is normally observed in natural systems. Scavengers only have minimal effects on predator kill rate when predator, scavenger, and prey abundances are kept constant by management. In such controlled systems, interference competition can greatly affect the interactions in contrast to more natural systems, with an increase in interference competition leading to a decrease in predator kill rate. Our study adds to studies that show that the presence of predators affects scavenger behavior, vital rates, and food web structure, by showing that scavengers impact predator kill rates through multiple mechanisms, and therefore indicating that scavenging and predation patterns are tightly intertwined. We provide a road map to the different theoretical outcomes and their support from different empirical studies on vertebrate guilds to provide guidance in wildlife management.     

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA-based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species-specific parasitoid-hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.     

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.     

Predator and detritivore niche width helps to explain biocomplexity of experimental detritus-based food webs in four aquatic and terrestrial ecosystems

In the study of food webs, the existence and explanation of recurring patterns, such as the scale invariance of linkage density, predator–prey ratios and mean chain length, constitute long-standing issues. Our study focused on litter-associated food webs and explored the influence of detritivore and predator niche width (as δ¹³C range) on web topological structure. To compare patterns within and between aquatic and terrestrial ecosystems and take account of intra-habitat variability, we constructed 42 macroinvertebrate patch-scale webs in four different habitats (lake, lagoon, beech forest and cornfield), using an experimental approach with litterbags. The results suggest that although web differences exist between ecosystems, patterns are more similar within than between aquatic and terrestrial web types. In accordance with optimal foraging theory, we found that the niche width of predators and prey increased with the number of predators and prey taxa as a proportion of total taxa in the community. The tendency was more marked in terrestrial ecosystems and can be explained by a lower per capita food level than in aquatic ecosystems, particularly evident for predators. In accordance with these results, the number of links increased with the number of species but with a significantly sharper regression slope for terrestrial ecosystems. As a consequence, linkage density, which was found to be directly correlated to niche width, increased with the total number of species in terrestrial webs, whereas it did not change significantly in aquatic ones, where connectance scaled negatively with the total number of species. In both types of ecosystem, web robustness to rare species removal increased with connectance and the niche width of predators. In conclusion, although limited to litter-associated macroinvertebrate assemblages, this study highlights structural differences and similarities between aquatic and terrestrial detrital webs, providing field evidence of the central role of niche width in determining the structure of detritus-based food webs and posing foraging optimisation constraints as a general mechanistic explanation of food web complexity differences within and between ecosystem types.     

Virus mediated trophic interactions between aphids and their natural enemies

Microbial endosymbionts alter the phenotype of their host which may have cascading effects at both population and community levels. However, we currently lack information on whether the effects of viruses on both host phenotypic traits and host population demography can modify interactions with upper trophic levels. To fill this gap, we investigated whether a prevalent densovirus infecting the aphid Myzus persicae (i.e. MpDNV) can modify trophic interactions between host aphids and their natural enemies (i.e. predators and parasitoids) by influencing aphid phenotypic traits (i.e. body mass and defensive behaviours), population demography (i.e. density and age-structure) and susceptibility towards both predation and parasitism. We found that the virus decreased aphid body mass but did not influence their behavioural defences. At the population level, the virus had a minor effect on aphid adult mortality whereas it strongly reduced the density of nymphs and influenced the stage structure of aphid populations. In addition, the virus enhanced the susceptibility of aphids to parasitism regardless of the parasitoid species. Predation rate on adult aphids was not influenced by the virus but ladybeetle predators strongly decreased the number of aphid nymphs, especially for uninfected ones compared to infected ones. As a result, the virus decreased predator effect on aphid populations. By reducing both aphid quality and availability, increasing their susceptibility to parasitism, and modulating predator effect on aphid populations, we highlighted that viral endosymbionts can be prevalent drivers of their host ecology as they modify their phenotypes and interspecific interactions. These virus-mediated ecological effects may have consequences on enemies foraging strategies as well as trophic webs dynamics and structure.