Aphid-parasitoid System Research Articles

Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system

Societal Impact StatementArbuscular mycorrhizal fungi (AMF) impact the relationships between plants, aphids (insects that feed on plant phloem), and their natural enemies (insects that prey on or parasitize aphids). The presence of AMF influences the growth and population of different aphid species and affects the development of aphid‐killing wasps and their attraction to plants. This research has been conducted also considering the insects' feeding strategy and their feeding specialization. This study provides novel perspectives on how these fungi shape interactions in the natural world, offering potential insights for the development of sustainable pest management strategies in agriculture.Summary Arbuscular mycorrhizal fungi (AMF) are major root symbionts regulating plant physiology. Their presence affects the performance of aboveground insect herbivores in relation to their feeding strategy and their feeding specialization. For example, the effect of the arbuscular mycorrhizal (AM) symbiosis on chewing insects, positive for specialists and negative for generalists, has been previously demonstrated. Conversely, the impact of AMF on phloem‐suckers with relatively different levels of specialization remains unexplored. We tested the influence of the AM Funneliformis mosseae on the fitness of the specialist aphid Acyrthosiphon pisum and the generalist aphid Myzus persicae on Vicia faba plants. Further, we investigated the effects of AMF on the higher trophic level, the aphid parasitoids Aphidius ervi (specialist) and Aphidius colemani (generalist), by evaluating plant attractiveness and parasitoid fitness. To support the results of behavioral and biological bioassays we characterized the photosynthetic parameters, the volatilome and the transcriptome of tested plants. Mycorrhizal plants proved unsuitable for the generalist M. persicae but enhanced the fitness of the specialist A. pisum. The AM symbiosis had no effects on the behavioral response of A. colemani and enhanced the attraction and fitness of A. ervi. Volatilome and transcriptome profiling corroborated the results of bioassay highlighting a bottom‐up effect of the AMF across a plant–aphid–parasitoid system.

Effect of 6-Benzylaminopurine on Morphogenesis and Production Process of Sweet Pepper (Capsicum annuum L.)

Effect of 6-Benzylaminopurine on Morphogenesis and Production Process of Sweet Pepper (Capsicum annuum L.)

Phenological responses in a sycamore-aphid-parasitoid system and consequences for aphid population dynamics: A 20year case study.

Species interactions have a spatiotemporal component driven by environmental cues, which if altered by climate change can drive shifts in community dynamics. There is insufficient understanding of the precise time windows during which inter-annual variation in weather drives phenological shifts and the consequences for mismatches between interacting species and resultant population dynamics-particularly for insects. We use a 20year study on a tri-trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum platanoidis and Periphyllus testudinaceus and their hymenopteran parasitoids. Using a sliding window approach, we assess climatic drivers of phenology in all three trophic levels. We quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts and parasitoids, and then model the impacts of these mismatches, direct weather effects and density dependence on local-scale aphid population dynamics. Warmer temperatures in mid-March to late-April were associated with advanced sycamore budburst, parasitoid attack and (marginally) D. platanoidis emergence. The precise time window during which spring weather advances phenology varies considerably across each species. Crucially, warmer temperatures in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates thus generates marked shifts in the relative timing of spring events across trophic levels and mismatches in the phenology of interacting species. Despite this, we found no evidence that aphid population growth rates were adversely impacted by the magnitude of mismatch with their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong density dependence effects occurred in both aphid species and probably buffered populations, through density-dependent compensation, from adverse impacts of the marked inter-annual climatic variation that occurred during the study period. These findings explain the resilience of aphid populations to climate change and uncover a key mechanism, warmer winter temperatures delaying insect phenology, by which climate change drives asynchronous shifts between interacting species.

The impact of climate on the winter strategies of insects

The impact of climate on the winter strategies of insects

'Bottom-up' effects in a tritrophic plant-aphid-parasitoid system: Why being the perfect host can have its disadvantages.

In this study the host plant genotype effect on cabbage aphid, Brevicoryne brassicae (L.)(Hemiptera: Aphididae) preference and performance, the effect of aphid genotype on parasitoids performance, as well as the indirect effects of plant genotypes on aphid parasitoid performance, were tested using different population samples of the aphid and its primary endoparasitoid wasp, Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae). Experiments were run as fully-factorial randomized block design in a greenhouse. Accordingly, host plant cultivar had significant effects on the total number of aphids and aphid-load whilst the fitness of the aphid genotypes were also influenced by plant cultivar. The effect of parasitism on cabbage aphids was significantly different between plant cultivars. Overall, the results revealed that cabbage aphid is under different selective pressures arising from both higher (parasitoid) and lower (host plant cultivar) trophic levels. The host plant cultivar had a significant effect on both aphid fitness and parasitism rate on particular aphid genotypes. This indicates that host-plant-adapted aphid species can create much context-dependency in the nature and strength of 'fitness benefits parasitism', which may in turn alter the costs and benefits of host specialization.

Estimating parasitoid impact on aphid populations in the field

We developed a quantitative method to assess the capacity of parasitoids to reduce aphid populations in open fields. The method, designated as the propagated mortality analysis (PMA), estimates the impact of early parasitoid-induced mortality on forthcoming aphid populations and was built upon an existing model describing the bell-shaped population dynamics observed in many aphid species. The PMA was next used to assess the impact of the naturalized and most abundant parasitoid Aphelinus sp. on populations of the soybean aphid Aphis glycines under field conditions in north-eastern North America. Results from the PMA showed that Aphelinus sp. reduced both peak soybean aphid densities and cumulative aphid-days at the end of the pest management threshold period by only 1–7%, probably because of low levels of parasitism early in the season. The method we propose is simple to use, could apply to most aphid-parasitoid systems and would gain to be extended to other natural enemies.

Tritrophic effects of plant growth regulators in an aphid-parasitoid system

Plant growth regulators (PGRs) have the potential to negatively affect the outcome of biological control via plant architectural changes and plant chemical changes. Despite studies demonstrating the negative effects of PGRs on herbivore survival and development, to date, no studies have investigated the tritrophic effects of PGRs on parasitoid life history traits. In this study we investigated the effect of four commonly used PGRs on Myzus persicae abundance and suppression, and Aphidius colemani fitness in a greenhouse experiment. None of the PGRs reduced aphid abundance alone or affected aphid suppression by A. colemani. However, paclobutrazol reduced the number of mummies that developed on plants. PGRs had a range of negative effects on parasitoid fitness. No adult parasitoids eclosed from mummies on ancymidol treated plants. Paclobutrazol reduced parasitoid size, and paclobutrazol and uniconazole reduced female:total ratio. This study shows that PGRs can negatively affect parasitoid fitness, and reduce parasitism, suggesting the potential for negative long-term effects on the efficacy of biological control.

Winter host exploitation influences fitness traits in a parasitoid

AbstractOrganisms can either evade winter's unfavourable conditions by migrating or diapausing, or endure them and maintain their activities. When it comes to foraging during winter, a period of scarce resources, there is strong selective pressure on resource exploitation strategy. Generalist parasitoids are particularly affected by this environmental constraint, as their fitness is deeply linked to the profitability of the available hosts. In this study, we considered a cereal aphid–parasitoid system and investigated (1) the host–parasitoid community structure, host availability, and parasitism rate in winter, (2) the influence of host quality in terms of species and instars on the fitness of the aphid parasitoid Aphidius rhopalosiphi De Stefani‐Perez (Hymenoptera: Braconidae: Aphidiinae), and (3) whether there is a detectable impact of host fidelity on parasitism success of this parasitoid species. Host density was low during winter and the aphid community consisted of the species Rhopalosiphum padi L. and Sitobion avenae Fabricius (both Hemiptera: Aphididae), both parasitized by A. rhopalosiphi at non‐negligible rates. Aphidius rhopalosiphi produced more offspring when parasitizing R. padi compared with S. avenae, whereas bigger offspring were produced when parasitizing S. avenae. Although aphid adults and old larvae were significantly larger hosts than young larvae, the latter resulted in higher emergence rates and larger parasitoids. No impact of host fidelity on emergence rates or offspring size was detected. This study provides some evidence that winter A. rhopalosiphi populations are able to take advantage of an array of host types that vary in profitability, indicating that host selectivity may drop under winter's unfavourable conditions.

Molecular and chemical mechanisms involved in aphid resistance in cultivated tomato

*An integrated approach has been used to obtain an understanding of the molecular and chemical mechanisms underlying resistance to aphids in cherry-like tomato (Solanum lycopersicum) landraces from the Campania region (southern Italy). The aphid-parasitoid system Macrosiphum euphorbiae-Aphidius ervi was used to describe the levels of resistance against aphids in two tomato accessions (AN5, AN7) exhibiting high yield and quality traits and lacking the tomato Mi gene. *Aphid development and reproduction, flight response by the aphid parasitoid A. ervi, gas chromatography-mass spectrometry headspace analysis of plant volatile organic compounds and transcriptional analysis of aphid responsive genes were performed on selected tomato accessions and on a susceptible commercial variety (M82). *When compared with the cultivated variety, M82, AN5 and AN7 showed a significant reduction of M. euphorbiae fitness, the release of larger amounts of specific volatile organic compounds that are attractive to the aphid parasitoid A. ervi, a constitutively higher level of expression of plant defence genes and differential enhancement of plant indirect resistance induced by aphid feeding. *These results provide new insights on how local selection can offer the possibility of the development of innovative genetic strategies to increase tomato resistance against aphids.

Comparison of spatially implicit and explicit approaches to model plant infestation by insect pests

Spatial heterogeneities have been explored in many different ways in population dynamic models. We investigate here the way in which space should be considered in the dynamics of an aphid–parasitoid system in a melon greenhouse, in order to plan a biological control program at a wide scale. By comparing a non-spatial model with a spatially explicit model (a lattice one), we show a strong difference between predictions and we thus confirm that it is essential to take space into account in such closed and structured environments when describing the spatial heterogeneities observed in the field. The way in which space should be considered in such system is tested by comparing the spatially explicit model with a new implicit approach, which describes the level of plant infestation by a continuous variable corresponding to the number of plants with a given density of pests at a given time. When the explicit model needs as many equations as plants in the greenhouse, our novel approach has only a partial differential equation. We infer from the comparisons between the two spatial models that the predicted host–parasitoid dynamics are similar under most conditions. Some differences occur when local dispersal (considered only in the explicit model) is high and it can have a strong impact on population dynamics but does not change the conclusions for crop protection. We conclude that the new spatially implicit model thus generate relevant predictions with a more synthetic formalism than the common plant-by-plant model and it will thus be more adapted to test biological control strategies at a higher scale than the greenhouse.

Aggregation of parasitism risk in an aphid-parasitoid system: Effects of plant patch size and aphid density

Few studies have linked density dependence of parasitism and the tritrophic environment within which a parasitoid forages. In the non-crop plant-aphid, Centaurea nigra – Uroleucon jaceae system, mixed patterns of density-dependent parasitism by the parasitoids Aphidius funebris and Trioxys centaureae were observed in a survey of a natural population. Breakdown of density-dependent parasitism revealed that density dependence was inverse in smaller colonies but direct in larger colonies (>20 aphids), suggesting there is a threshold effect in parasitoid response to aphid density. The CV 2 of searching parasitoids was estimated from parasitism data using a hierarchical generalized linear model, and CV 2 >1 for A. funebris between plant patches, while for T. centaureae CV 2 >1 within plant patches. In both cases, density independent heterogeneity was more important than density-dependent heterogeneity in parasitism. Parasitism by T. centaureae increased with increasing plant patch size. Manipulation of aphid colony size and plant patch size revealed that parasitism by A. funebris was directly density dependent at the range of colony sizes tested (50–200 initial aphids), and had a strong positive relationship with plant patch size. The effects of plant patch size detected for both species indicate that the tritrophic environment provides a source of host density independent heterogeneity in parasitism, and can modify density-dependent responses. Wenige Studien haben eine Verbindung zwischen dichteabhängigem Parasitismus und der tritrophischen Umwelt hergestellt, in der ein Parasitoid nach Wirten sucht. In einem System aus Nicht-Nutzpflanze und Blattlaus, dem Centaurea nigra-Uroleucon jaceae -System, wurden gemischte Muster von dichteabhängigem Parasitismus durch die Parasitoiden Aphidius funebris und Trioxys centaureae bei einer Untersuchung einer natürlichen Population beobachtet. Der Zusammenbruch der dichteabhängigen Parasitierung zeigte, dass die Dichteabhängigkeit in kleinen Kolonien invers und in größeren Kolonien (>20 Blattläuse) direkt war, und lässt vermuten, dass es einen Schwelleneffekt in der Reaktion der Parasitoide auf die Blattlausdichte gibt. Der CV 2 der suchenden Parasitoide wurde abgeschätzt, indem hierarchisch generalisierte, lineare Modelle verwendet wurden. Für A. funebris wurde ein CV 2 >1 zwischen den Pflanzenvorkommen festgestellt, während T. centaureae einen CV 2 >1 innerhalb der Pflanzenvorkommen zeigte. In beiden Fällen war die dichteunabhängige wichtiger als die dichteabhängige Heterogenität der Parasitierung. Die Parasitierung durch T. centaureae nahm mit der Größe der Pflanzenvorkommen zu. Die Manipulation der Koloniegrößen der Blattläuse und der Größe der Pflanzenvorkommen zeigte, dass die Parasitierung durch A. funebris direkt dichteabhängig im Bereich der untersuchten Koloniegrößen (50-200 initiale Blattläuse) war und einen starken positiven Zusammenhang mit der Größe des Pflanzenvorkommens zeigte. Die Effekte der Größe der Pflanzenvorkommen, die bei beiden Arten festgestellt wurden, weisen darauf hin, dass eine tritrophische Umwelt eine Quelle für eine von der Wirtsdichte unabhängige Heterogenität in der Parasitierung darstellt und dichteabhängige Reaktionen modifizieren kann.

An implicit approach to model plant infestation by insect pests

Various spatial approaches were developed to study the effect of spatial heterogeneities on population dynamics. We present in this paper a flux-based model to describe an aphid–parasitoid system in a closed and spatially structured environment, i.e. a greenhouse. Derived from previous work and adapted to host–parasitoid interactions, our model represents the level of plant infestation as a continuous variable corresponding to the number of plants bearing a given density of pests at a given time. The variation of this variable is described by a partial differential equation. It is coupled to an ordinary differential equation and a delay-differential equation that describe the parasitized host population and the parasitoid population, respectively. We have applied our approach to the pest Aphis gossypii and to one of its parasitoids, Lysiphlebus testaceipes, in a melon greenhouse. Numerical simulations showed that, regardless of the number and distribution of hosts in the greenhouse, the aphid population is slightly larger if parasitoids display a type III rather than a type II functional response. However, the population dynamics depend on the initial distribution of hosts and the initial density of parasitoids released, which is interesting for biological control strategies. Sensitivity analysis showed that the delay in the parasitoid equation and the growth rate of the pest population are crucial parameters for predicting the dynamics. We demonstrate here that such a flux-based approach generates relevant predictions with a more synthetic formalism than a common plant-by-plant model. We also explain how this approach can be better adapted to test different management strategies and to manage crops of several greenhouses.

Ecological considerations for biological control of aphids in protected culture

AbstractSeveral braconid and aphelinid parasitoids, midges, lacewings, and ladybird beetles are used to control aphids in greenhouses. Here, I review three topics as ecological bases for the biological control of aphids in a protected culture: the preliminary evaluation of biological control agents, natural enemy release strategies, and the effects of intraguild predation (IGP) on biological control. A comparison of several parasitoid species was conducted to select agents for the biological control of aphids; the intrinsic rate of natural increase was a useful criterion in the preliminary evaluation. To compare predators as biological control agents, the aphid‐killing rate must be considered as a critical criterion, rather than reproductive criteria. The banker plant system (open rearing system) is used as a release method for Aphidius colemani and other natural enemies of aphids. Continuous release of parasitoid adults, which is the important characteristic of this method, has a stabilizing effect on population fluctuation in the aphid–parasitoid system. Two species of natural enemies can be used to control aphids in greenhouses. When one parasitoid and one predator are used simultaneously in a greenhouse, IGP of the parasitoid by the predator can occur, but the effect of IGP is less important in greenhouses than in the field.

An experimental investigation of patterns of parasitism at three spatial scales in an aphid-parasitoid system (Hymenoptera: Aphidiidae)

Density dependent host mortality in the interaction between the solitary endoparasitoid Aphidius colemani (Aphidiidae), and its host, the green peach aphid Myzus persicae, was examined on greenhouse peppers. The experimental approach attempted to eliminate spatial interdependence in the relationship between host density and host mortality by using different plants to measure parasitism at different spatial scales. Increasing host density at the plant scale caused a significant increase in the proportion of host mortality. However, at the shoot and leaf scale, increasing host density caused a significant decrease in host mortality. This may be one of the first experimental demonstrations of a switch from inverse to direct density dependence. The pattern is assumed to be a result of searching parasitoids using different cues at different spatial scales.

Intraguild interactions in aphid parasitoids

AbstractWe reviewed the literature on aphid parasitoids to determine the occurrence, nature and outcome of intraguild interactions. Intraguild interactions were described for larval, pupal and adult aphid parasitoids and by the type of natural enemy (fungus, predator, or parasitoid). They appear to be prevalent in most aphid parasitoid systems and, except for parasitoid‐parasitoid interactions, they are mostly asymmetric, with aphidophagous predators and pathogens killing parasitoids. The limited experimental evidence from field studies is insufficient to provide a comprehensive pattern of the consequences of intraguild interactions for aphid parasitoid populations in general and, more specifically, for the efficacy of biological control. However, because intraguild interactions are widespread in aphid‐natural enemy communities and mostly detrimental to aphid parasitoids, we conclude that intraguild interactions have a primary effect in driving fluctuations in aphid parasitoid populations. Drawing on case studies, we further argue that intraguild interactions can substantially alter the effectiveness of aphid parasitoids as biological‐control agents.

Hyperparasitoid defense strategies against spiders: the role of chemical and morphological protection

The aphid endohyperparasitoid Alloxysta brevis (Thomson) (Hymenoptera: Charipidae) applies defensive chemicals stored in mandibular gland reservoirs against attacking ants. Alloxystines can be divided into species capable of exploiting ant-attended resources and into species exclusively reared from unattended aphid-parasitoid systems. Mandibular secretions are found in species of both groups, with little variation in chemical composition. We show that the mandibular gland secretion does not only protect against ant attacks but acts as an overall defense agent against generalist predators like spiders. The protective success differed with the spider species. The web-building spider Agelena labyrinthica (Clerck) (Araneae: Agelinidae) killed 57% of attacked A. brevis females, but sucked out only 8%. The smaller free-hunting jumping spider Salticus scenicus (Clerck) (Araneae: Salticidae) failed in overwhelming or severely injuring A. brevis. The pattern of interactions showed striking similarities with interactions between A. brevis and the ant Lasius niger (Hymenoptera: Formicidae). Primary parasitoids which are lacking chemical defense and sufficient morphological protection suffered significantly higher mortality due to spider predation. Our results indicate that - additional to chemical defense- parasitoid survival depends on the specific morphological resistance against grip pressure during capture, and on the predator - prey size relationship.

Indirect interactions in aphid–parasitoid communities

AbstractIndirect interactions between populations of different species can be important in structuring natural communities. Indirect effects are either mediated by changes in population densities (trophic or density‐mediated effects) or by changes in the behavior of species that are not trophically connected (behavioral or trait‐mediated effects). We reviewed the literature on aphids and their parasitoids to explore the various possible indirect interactions that can occur in such communities. The review was motivated by our study of a particular aphid–parasitoid community in a natural (i.e., nonagricultural) habitat, and by the wealth of information that exists about aphid–parasitoid systems in agricultural settings. We focused our review on aphid–parasitoid interactions, but considered how these were influenced by the other aphid natural enemies and also by aphid mutualists and host plants. We conclude that indirect effects are likely to have a major effect in structuring aphid–parasitoid communities, and that the latter are a valuable model system for testing ideas about community interactions.

Delayed effects in aphid-parasitoid systems: Consequences for evaluating biological control species and their use in augmentation strategies

A particular feature of aphid-parasitoid systems is the existence of a delay between parasitisation (sting) and the death of the host (i.e. mummification). This biological trait is generally not considered important for population stability, except if the delay is very long, and hence it is ignored in most population dynamics studies. However, many crops have relatively short durations, and these time delays may have important consequences and cannot be ignored in a dynamics model. In this study, we are looking for the key-factors that influence an aphidparasitoid system population dynamics during a cropping cycle.