Tritrophic Interactions Research Articles

The ethological significance and olfactory detection of herbivore-induced plant volatiles in interactions of plants, herbivorous insects, and parasitoids

Tritrophic interactions play a pivotal role in maintaining a functional agroecosystem. After damaged by phytophagous insects, host plants release a blend of odorants called herbivore-induced plant volatiles (HIPVs) that are attractive to natural enemies including arthropod predators and, in particular, parasitoids. In the last three decades, the identities of HIPVs have been meticulously characterized in a variety of tritrophic systems by gas chromatography–mass spectrometry (GC–MS) analysis. A plethora of HIPV components have been physiologically screened by gas chromatography-electroantennogram detection (GC-EAD) and single sensillum recording (SSR). The effects of induced odorants on behavior of herbivores and parasitoids have been investigated using Y-tube olfactometer assays and wind tunnels in the laboratory and bait trap tests in the field. Given the potential utility of parasitic wasps for pest control, the understanding of olfactory mechanisms of how HIPVs are detected by herbivores and parasitic wasps could facilitate the exploitation of parasitoids as bio-control agents. As the advent of the genome sequencing and transcriptome analysis, a large repertoire of chemosensory protein genes including odorant receptors and odorant binding proteins has been identified in herbivores and parasitic wasps, providing an unprecedented opportunity to debunk the molecular basis of olfaction-based interactions. In this review, we will summarize the recent progresses in characterization of HIPVs, the studies of olfactory mechanisms underlying tritrophic interactions with a focus on parasitoids, Lepidopteran pests, and related host plants.

Chemical cues linked to risk: Cues from below‐ground natural enemies enhance plant defences and influence herbivore behaviour and performance

Abstract Chemical cues are essential for many ecological interactions. Previous studies of chemically mediated multitrophic interactions have typically focused on responses to cues from plants or herbivores above‐ground. It is increasingly clear, however, that below‐ground cues and those produced by organisms at higher trophic levels also have ecological importance. Prey animals often avoid predator odours to improve survival, and previous research has documented enhanced plant resistance following contact with below‐ground natural enemies, though the ecological basis was unknown. Here, we investigated plant and insect responses to chemical cues from below‐ground natural enemies and explored the ecological significance of these cues for multitrophic interactions. More specifically, we examined the influence of odours emitted by entomopathogenic nematodes (EPNs), a natural enemy of insect herbivores, on the performance and behaviour of their insect prey and the defence responses of nearby plants. Our findings revealed that EPN‐infected insect cadavers emit a characteristic blend of volatile compounds with bioactivity in plants and insects. EPN chemical cues influenced both performance and preference of a specialist herbivore, Colorado potato beetle (CPB, Leptinotarsa decemlineata), feeding on its host plant, potato (Solanum tuberosum). CPB larvae consumed less leaf tissue and gained less mass feeding on plants exposed to EPN cues compared to control plants. Female CPBs laid fewer eggs on plants with EPN cues than on controls, indicating deterrence by EPN cues or EPN‐altered plant defences. Plant defences were enhanced by exposure to live EPNs or EPN chemical cues. Potato plants exposed to EPN infective juveniles induced higher amounts of the defence hormone salicylic acid (SA) and had higher expression of the pathogenisis‐related gene PR‐1(PR4) in foliar tissue. Exposing plants to EPN cues primed induction of SA and jasmonic acid in response to feeding damage by CPB larvae. These findings suggest that herbivores avoid cues from their EPN natural enemies and plants respond to the beneficial nematodes by enhancing systemic defences that reduce herbivore performance. This work has important implications for the chemical ecology of tritrophic interactions as we report that the third trophic level can play direct and indirect roles in plant defence. A plain language summary is available for this article.

Role of Induced Volatile Emission Modelling Tritrophic Interaction

Plant population response to herbivore attack by releasing volatile organic compounds (VOCs) in a highly regulated fashion. The natural enemies of herbivores are attracted by such induced volatile. This type of mechanism is known as “indirect defense mechanism” for plants. A tritrophic interaction among the plants, herbivores and their carnivorous enemies is considered along with “indirect defense mechanism” of plants in recruitment rate of carnivorous enemies. A systematic analysis of the dynamics of plant–herbivore–carnivore system with Holling type II functional response is done in this paper. The conditions for existence and feasibility of boundary and interior equilibrium points of the system are also determined. The conditions for the global stability of positive equilibrium point is derived. Persistence of the system is studied. Here, different types of bifurcations are analyzed with respect to many parameters. A key role is played by immigration rate of carnivores in determining the eventual state of the ecosystem. Finally, numerical simulations are performed to validate the obtained results.

What do we know about birds’ use of plant volatile cues in tritrophic interactions?

The first study showing that birds can smell herbivore-induced plant volatiles was published ten years ago. Since then, only 12 studies have been published, showing contradictory results. This review evaluates the role of birds in relation to the crying for help hypothesis and their use of olfactory cues. In accordance with the methodologies used in previous studies, we herein provide a summary of experimental approaches and describe the advantages and disadvantages of experiments conducted in nature versus aviaries. Moreover, we recommend experimental methodologies which lead to a deeper knowledge of the topic, including reflection on the induction of plant defenses and adaptations of birds. Finally, we propose some interesting questions for future research to direct further studies towards a thorough and accurate description of birds' roles in tritrophic interactions.

Mint companion plants attract the predatory mite Phytoseiulus persimilis

Mint plants could theoretically serve as companion plants (CPs) that attract enemies of herbivores in tritrophic interactions. In order to explore the traits of mint volatiles as attractant cues for enemies of two-spotted spider mites, we performed Y-tube olfactometer assays of predatory mites, Phytoseiulus persimilis and Neoseiulus californicus, towards three mint species, apple mint, candy mint, and spearmint, as odor source. Clean candy mint and spearmint were attractive to P. persimilis, when compared with clean air and undamaged Phaseolus vulgaris plants serving as the target crop. Moreover, clean candy mint plants were even more attractive than volatiles from P. vulgaris plants damaged by spider mites. These predator responses were induced additively by candy mint volatiles plus volatiles from damaged P. vulgaris plants, as shown using both Y-tube olfactometer and open-space assay systems. However, the number of spider mite eggs consumed by P. persimilis on P. vulgaris plants did not differ in the presence compared to the absence of mint volatiles, indicating that mint volatiles affect the attraction but not the appetite of P. persimilis. Together, these findings suggest that the use of candy mint and spearmint as CPs is an ideal platform for spider mite pest management via the attraction of predatory mites.

A soil bacterium can shape belowground interactions between maize, herbivores and entomopathogenic nematodes

Entomopathogenic nematodes (EPN) use odor cues to locate and infect their insect hosts in the soil, making them an important tool in sustainable management of agricultural insect pests. However, very little information is available on the role of soil bacteria in mediating belowground interactions between plants, herbivores and the EPN. In this study, a maize-herbivore-entomopathogenic nematode complex was used to investigate the effect of plant root colonization by a soil bacterium on belowground tritrophic interactions. The impact of maize root colonization by Bacillus pumilus strain INR-7 on the preference of the EPN, Heterorhabditis bacteriophora was tested in four arm olfactometer bioassays in the presence or absence of the root herbivore Diabrotica virgifera LeConte (Coleoptera: Chrysomelidae). Plant volatiles were collected for profile characterization. Further preference assays were performed using plant volatile extracts and synthetic volatiles. In the absence of the root herbivore, the nematodes were attracted to maize roots whose seeds were coated with dead and living bacteria. In the presence of the herbivore, the nematodes selectively oriented towards infested plants whose seeds were treated with B. pumilus strain INR-7 than dead bacteria treated, untreated plants or sunshine sand mix. In contrast, plant volatile extracts or pure compounds did not reproduce the observed behavior. The study showed that bacterial coating of maize seeds with the tested strain may play an important role in shaping belowground tritrophic interactions through mechanisms that would require further investigations. The potential of B. pumilus strain INR-7 integration in maize rootworm management program is discussed.

Identification and Characterization of Differentially Expressed Proteins from Trichoderma harzianum During Interaction with Colletotrichum falcatum Causing Red Rot in Sugarcane

In continuation of our earlier findings on suppression of C. falcatum by T. harzianum, the present study was attempted to characterize differentially expressed proteins from T. harzianum during its growth over C. falcatum metabolites. Proteomic analysis clearly indicated the degradation of C. falcatum proteins and expression of newer proteins by T. harzianum through SDS–PAGE. Two-Dimensional Electrophoresis (2-DE) of individual protein bands eluted from SDS–PAGE resulted in clear separation of 15 protein spots from 3 differentially expressed protein bands viz., DEPb1, DEPb2 and DEPb3. MALDI-TOF analysis of these proteins revealed that the identified 8 proteins were belonging to two functional categories viz., stress and defence (choline dehydrogenase, FKBP-type peptidyl-prolyl cis–trans isomerase, superoxide dismutase (Cu/Zn) and Hex1) and unknown function (Hypothetical proteins). The stress-related proteins were reported to be involved in biological suppression of various pathogens in other crops. In addition to this, 7 unknown function proteins expressed from T. harzianum during interaction with C. falcatum may play a major role in degradation of metabolites. Role of identified proteins was further confirmed during in-planta expression analysis by qRT-PCR, which showed the upregulation of selected proteins with distinct patterns at all the time interval during the tritrophic interaction of host, pathogen and antagonist and corresponding reduction in symptom production.

A Review of the Genus Lipolexis Förster, 1862 (Hymenoptera, Braconidae: Aphidiinae) in the Fauna of Ukraine

Genus Lipolexis Förster, 1862 is represented by four species in the world fauna and only one species, Lipolexis gracilis Förster, 1862, in the fauna of Europe, and Ukraine as well. Data on the genus Lipolexis and its species L. gracilis are presented according to available published information and material from collection of I. I. Schmalhausen Institute of Zoology, NAS of Ukraine, identified by author. Lipolexis gracilis is distributed generally in Palaerctic and Oriental regions, where it prefers steppificated habitats. In Ukraine species is recorded in Cherkasy, Kirovohrad and Ternopil Regions, which are situated in Forest-Steppe Zone and Zone of Broadleaf Forests of Ukraine. Lipolexis gracilis is polyphagous species that parasitizes various aphid species mostly from subfamily Aphidinae, as well as aphids from subfamily Anoeciinae and subfamily Calaphidinaе. Data on tritrophic interactions of L. gracilis in the fauna of Ukraine is given and possibility of species application as a biocontrol agent is discussed. In Ukraine L. gracilis was reared from Aphis craccae L., Aphis craccivora Koch, Aphis fabae Scopoli, and Brachycaudus cardui L. Among hosts of L. gracilis, there are economically important aphids, and this species was previously used as biocontrol agent of soybean aphid, Aphis glycines Matsumura. On our opinion this aphidiine species could be considered as potential biocontrol agent of other economically important aphid species. To facilitate identification of L. gracilis a new morphological character is established: this is the ratio of the forewing length and the length of C+SC+R vein. This character will facilitate identification of broken specimens.

Study on host-seeking behavior and chemotaxis of entomopathogenic nematodes using Pluronic F-127 gel.

Pluronic F-127 gel (PF127) has proven to be a powerful medium in which to study host-finding behavior and chemotaxis for plant-parasitic nematodes. Pluronic gel can also be used to study host-habitat seeking behavior of entomopathogenic nematodes (EPN), which are natural enemies of root-feeding insect pests. In this study, PF127 was used to study tritrophic interactions among EPNs, host-habitat roots and insects. We also tested whether EPN aggregated to acetic acid (pH gradient) which mimicked the conditions near the roots. The chive root gnat Bradysia odoriphaga alone significantly attracted more nematodes than chive roots alone or the combination of roots plus insects. The attractiveness of B. odoriphaga differed (3.7-15.4%) among all tested species/strains of EPNs. In addition, we found that Heterorhabditis spp. and Steinernema spp. infective juveniles responded to pH gradients formed by acetic acid in Pluronic gel. The preferred pH ranges for strains of H. bacteriophora and H. megidis were from 4.32-5.04, and from 5.37-6.92 for Steinernema species, indicating that Heterorhabditis spp. prefer low pH conditions than Steinernema species. A narrow pH gradient between 6.84 and 7.05 was detected around chive root tips in which EPN was attracted. These results suggest that Pluronic gel can be broadly used for the study of host or host-habitat seeking behaviors and chemotaxis of nematodes.

Dispersal evolution in metacommunities of tri-trophic systems

Species interactions potentially affect dispersal evolution. However, previous studies about dispersal focused mostly on one or two species systems, and dispersal evolution in metacommunities composed of more than two interacting species is left to study. Here, we use a spatially explicit individual-based model to investigate the concurrent evolution of dispersal probabilities in metacommunities of tri-trophic interaction systems with one host, parasitoid, and hyperparasitoid species. We vary search efficiency (interaction intensity) of parasitoid on host and search efficiency of hyperparasitoid on parasitoid under different dispersal mortalities. Our results indicate that the tri-trophic system can persist in limited range of search efficiency of parasitoid and hyperparasitoid. Higher search efficiency of hyperparasitoid generally resulted in the evolution of higher dispersal probabilities of all species, while higher search efficiency of parasitoid increases only host and parasitoid dispersal probabilities but decreases hyperparasitoid dispersal probabilities. Dispersal mortality has a negative effect on emergent dispersal probabilities for all three species. Moreover, an increase in dispersal mortality desynchronizes population dynamics and widens the range of parasitoid and hyperparasitoid search efficiencies under which the tri-trophic system can persist.

Contribution of different predator guilds to tritrophic interactions along ecological clines.

The strengths of interactions between plants, herbivores, and predators are predicted to relax with elevation. Despite the fundamental role predators play in tritrophic interactions, high-resolution experimental evidence describing predation across habitat gradients is still scarce in the literature and varies by predator. With this opinion paper, we look at how tritrophic strength of systems including different vertebrate and invertebrate predator guilds changes with elevation. Specifically, we focus on how birds, ants, parasitoids, and nematodes exert top-down pressure as predators and propose ways, in which each group could be better understood through elevational gradient studies. We hope to enrich future perspectives for disentangling the different biotic and abiotic factors underlying predator-mediated trophic interactions in a diversity of habitats.

Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions.

Uninfested plants emit only trace quantities of volatiles (constitutively emitted plant volatiles). In contrast, some plants emit relatively large quantities of volatiles in response to herbivory (herbivory-Induced plant volatiles: HIPVs). Organisms belonging to different trophic levels use plant volatiles in context-dependent manners; consequently, volatiles can be adaptive, non-adaptive, or maladaptive to the emitter plants. In this review, we focus on the multifunctional aspects of HIPVs, which vary qualitatively and quantitatively in emitting plant species and infesting herbivore species, in plant-carnivore interactions, plant-herbivore interactions, and plant-omnivore interactions. Additionally, we review the evidence of plant-plant communication and its effects on tritrophic interactions involving plants, herbivores, and carnivores. Prospects on interactions mediated by plant volatiles induced by herbivorous arthropods are discussed.

Tree litter identity and predator density control prey and predator demographic parameters in a Mediterranean litter-based multi-trophic system

Plant litter decomposition is an essential process of ecosystem functioning, driven by a complex soil food web. The identity and density of the predators, as well as the quality and quantity of litter, could conjointly affect the strength of trophic interactions within a soil food web. Pine and oak are dominant tree species in temperate and Mediterranean forests and, although they exhibit distinct litter characteristics, no previous study attempted to decipher how these two litters can affect a litter-based multi-trophic system with varying predator density. Using a microcosm experiment, we aimed at understanding how different densities of a predatory Acari (Stratiolaelaps scimitus) and two Mediterranean litter species (Quercus pubescens and Pinus halepensis) may impact the demographic parameters of the predatory Acari, its Collembola prey (Folsomia candida) and the fungal biomass associated with litter. We did not observe any interactive effect of litter identity and predator density on both predator and prey demographic parameters. Survival and fecundity rates of the predator and its prey decreased at high predator density. However, demographic parameters of the predator and its prey were differentially affected by litter identity, with greater prey demographic parameters in Quercus litter and, in the opposite, greater predator demographic parameters in Pinus litter, probably due to differences in physical characteristics providing more or less refuge for the prey. We also observed a higher increase in fungal biomass in Pinus compared to Quercus litter, i.e. the litter with the fungivorous Collembola abundance reduced by the predatory Acari. Litter identity could thus strongly regulate these tri-trophic interactions (Fungi – fungivorous Collembola – predatory Acari) in forest ecosystems. Finally, the implications of our findings could be important as the distribution area of oak and pine forests may be altered in response to climate change with then potentially strong cascading effects on soil organisms and the processes they drive.

Exposure to Herbicides Prime P450-Mediated Detoxification of Helicoverpa armigera against Insecticide and Fungal Toxin.

With the long-term and large-scale use, herbicides have been well known to influence tritrophic interactions, particularly natural enemies of pests in agro-ecosystems. On the other hand, herbivorous insects, especially the generalist pests, have developed antagonistic interaction to different insecticides, toxic plant secondary metabolites, and even heavy metals. However, whether exposure to herbicides would affect resistance of insects against insecticides is largely unknown, especially in agricultural pests. Here, we first reported that pre-exposure to two widely used herbicides butachlor and haloxyfop-methyl for 48 h can prime the resistance of a generalist agricultural pest Helicoverpa armigera Hübner against insecticide methomyl and fungal toxin aflatoxin B1. In addition, there were no significant differences between control and herbicides-treated caterpillars on weight gain, pupal weight, and pupation rates, suggesting that exposure to herbicides induces resistance of H. armigera accompanied with no fitness cost. Moreover, by determining detoxifying enzyme activities and toxicity bioassay with additional inhibitor of cytochrome P450 piperonyl butoxide (PBO), we showed that exposure to herbicides might prime P450-mediated detoxification of H. armigera against insecticide. Based on these results, we propose that exposure to herbicides prime resistance of H. armigera against insecticide and fungal toxin by eliciting a clear elevation of predominantly P450 monooxygenase activities in the midgut and fat body.

Effects of limited volatiles release by plants in tritrophic interactions.

We introduce a mathematical model to describe the tritrophic interaction between crop,pest and the pest natural enemy where the release of Volatile Organic Compounds (VOCs) by crop istaken into account. The VOCs may be considered as an indirect defence mechanism of the plant asthey attract the pest natural enemies toward the attacked plants. The model dynamics is studied throughqualitative analysis and numerical simulations. The factors that may enhance pest disappearance areidentified. In particular, we show that VOCs may have a beneficial effect on the environment sincetheir release may be able to stabilize the model dynamics. Specifically, for the parameter values thatwe have explored, this effect can arise only when both the phenomena of VOCs basic plant release andVOCs plant release due to pest attack are present.

Diurnal rhythm of volatile emissions from damaged Brachypodium distachyon affects the temporal preferences of tritrophic interactions

ABSTRACT Diurnal rhythm of volatile emissions from grasses in response to herbivory may temporally affect the oviposition behaviors of the conspecific herbivores and prey searching of natural enemies of the herbivores in a diurnal cycle of the ecosystem. We assessed volatiles emitted from the temperate grass Brachypodium distachyon L. (Poaceae) damaged by Mythimna separata Walker (Noctuidae), a specialist herbivore of Poaceae, in light/dark cycle conditions. Volatiles were preferentially emitted from the damaged plants in both light and dark phases, but their quantitative compositions were different. The generalist predator Nesidiocoris tenuis Reuter (Miridae) was attracted to the damaged plants in both light and dark conditions. However, adult females of M. separata preferred to oviposit on undamaged plants mostly in the dark owing to the cue of undamaged plant volatiles, partly in a circadian rhythm-dependent manner. The findings suggested that volatiles released in the dark contribute to both plant-herbivore and plant-herbivore enemy communications.

The role of herbivore-induced plant volatiles (HIPVs) as indirect plant defense mechanism in a diverse plant and herbivore species; a review

When plants are attacked by herbivores, they release plant volatiles called herbivore-induced plant volatiles (HIPVs) to the environment to communicate with higher trophic levels. HIPVs play different ecological roles such as plant-plant interaction, plant-herbivore interaction, tritrophic interaction and other related interactions. Attractiveness of HIPVs to natural enemies in a tritrophic interaction varies depending on species diversity. Under natural and multiple cropping systems, tritrophic interaction is expected to be more complex than single tritrophic interaction with one species per trophic level. In complex tritrophic interaction, diversity of different trophic levels affects attractiveness of HIPVs to natural enemies. From plant diversity point of view, HIPVs mixture emanating from herbivore-damaged multiple plant species are reported to affect behavioral responses and foraging behavior of natural enemies under laboratory and field conditions. Similarly, from herbivore diversity point of view, in nature, plants are commonly attacked by more than one herbivore species. Constituents of HIPVs vary between plants infested by multiple and single herbivore species and this affects the behavioral responses and foraging behavior of natural enemies. This paper reviews recent findings on the role of HIPVs as indirect plant defense in systems with simple tritrophic interaction, and in diverse plants species and diverse herbivore species.

Ecological role of a flower-dwelling predator in a tri-trophic interaction in northwestern Patagonia

Flower-dwelling predators may play several ecological roles depending on their effects on the reproductive success of the plants that they use to forage. However, tri-trophic interactions often are context-dependent highlighting the importance of assessing both the overall top-down effect on plant fitness and predator behavioral and physiological attributes that shape that outcome. We studied the effect of the flower-dwelling crab spider Misumenops pallidus on the perennial herb Anemone multifida in a low-thicket in Northwestern Patagonia. We measured pollinator visitation frequency, florivory rate, plant fitness, spider abundance, and spider's physiological (e.g. camouflage) and behavioral attributes (e.g. host selection, fidelity) that aid to define its possible ecological role. Misumenops pallidus showed a generalist diet (mostly pollinators), camouflage strategies, and intraspecific selection for plants bearing higher number and longer trichomes. Additionally, it displayed host-fidelity with long periods of permanence in the selected host plant, occupying ∼25% of plant population. However, the presence of these spiders did not affect pollinator visitation rate, florivory or plant fitness, indicating a commensalism role. Our findings suggested that the asymmetric benefit in this plant-spider association may be attributed to a combination of factors. In particular, the low-to-moderate spider abundance, generalist diet and cryptic camouflage; all of which weaken the top-down effect on pollinators and plant fitness, especially whenever ecological redundant pollinators are present. However, temporal and/or spatial variation on spider population might enhance this asymmetric benefit for the spider, potentially changing its role from commensalism to antagonism.

Biocontrol Strategies to Manage Fungal Diseases in Sugarcane

Red rot, wilt, sett rot and seedling rot are the major fungal diseases for which biological control could be used as effective tool as a component of integrated disease management. Efficient fungal and bacterial antagonists have been identified against them, and their efficacy has been proved under in vitro and in vivo conditions. For red rot, fungal bioagents, viz. Chaetomium, Trichoderma, and bacterial antagonists individually and in combination of bacterial antagonists and fungicide were found to be effective in protecting the crop. Capability of bacterial antagonists in inducing resistance through induced systemic resistance against red rot was established. Delivery of the antagonists through sett treatment was standardized for field application. Further, pressmud formulation of Trichoderma was found effective against wilt under field conditions. Similarly, use of Trichoderma formulation was highly effective against seedling rot caused by Pythium spp. and it is used in seedling trays to manage the disease. Attempts were made to isolate and characterize antifungal genes/proteins capable of reducing the pathogenic potential of Colletotrichum falcatum, the red rot pathogen, and have yielded desirable results. Recently, molecular approaches have been applied to understand antagonistic mechanism between C. falcatum and Trichoderma harzianum. In vitro and in vivo studies during tritrophic interactions among the antagonist, the host plant and the pathogen revealed key pathogenicity genes/proteins in C. falcatum targeted by T. harzianum to reduce pathogenicity. Through interactive proteomics, many candidate antifungal proteins were identified from T. harzianum. Recent studies on biocontrol of sugarcane diseases have revealed scope for its application in the field to manage these diseases and T. harzianum as a bridge species to identify pathogenicity genes of red rot pathogen and identifying candidate antifungal genes.

Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implications for Integrated Pest Management

Soil abiotic factors and plant traits are able to trigger bottom-up effects along the tri-trophic plant–herbivore–natural enemy interactions. The consequences could be useful for controlling the insect herbivores. The South American tomato pinworm, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), a devastating invasive leaf-mining pest on tomato and other solanaceous plants, is currently threatening the tomato production worldwide. Recent knowledge of bottom-up effects on this pest has been gained, with fertilization, irrigation, plant resistance traits, as well as their interactions, being the major sources of these effects. Evidence is now emerging on how they impact on the performance of the moth from the perspective of tri-trophic interactions. In this review, we summarize the essential experiments studying the bottom-up effects on T. absoluta and discuss the implications of those findings for the Integrated Pest Management programs. Future promising research directions are then proposed.