Aphid Behaviour Research Articles

How aphids find their host plants, and how they don't

AbstractThere is a considerable interest in trying to understand how aphids find their host plants because they are a major cause of economic losses in agricultural and horticultural production systems. Indeed, the specific behavioural sequences during host finding by aphids are one of the main reasons for their prominent role as vectors of plant pathogenic viruses. This paper reviews the visual and olfactory stimuli involved in host‐finding behaviour of aphids, both basic and applied aspects are covered. Although controlling aphids by manipulation of visual and olfactory stimuli involved in host finding and host selection can be highly successful, as shown by research, most of these measures can still be further optimised and adoption in practice is currently limited. Research therefore needs to address some critical open questions, including (a) the effects of visual contrasts on aphid behaviour; (b) the specific responses of aphids to ultraviolet (UV) light during different stages in host finding; (c) the quantification of behavioural sequences in the field and (d) the response of aphid behaviour to plant diversity at varying spatial scales; further, (e) a much more comprehensive coverage of aphid taxa and aphid ecological groups is needed in host‐finding related research to uncover ecological principles underlying this critical behaviour.

Resistant poplar genotypes inhibit pseudogall formation by the wooly poplar aphid, Phloeomyzus passerinii Sign

Phloeomyzus passerinii can induce a pseudogall within the bark of susceptible poplar genotypes, while in resistant genotypes the induction seems to be impeded by lignification processes. Phloeomyzus passerinii is a major pest of poplar stands in Europe, North Africa and the Near East. This aphid feeds in the cortical parenchyma of different poplar species and hybrids, and can affect their growth and survival through unknown mechanisms. In some genotypes, however, resistance prevents either the settlement or the development of aphid colonies. For a better understanding of tree reactions to aphid probing, we compared the anatomical and biochemical modifications undergone within the bark of stem cuttings, after different delays of either aphid colonization or mechanical wounding. To assess how resistance may modulate tree reactions, the comparison was performed using three poplar genotypes exhibiting different resistance levels. In these three genotypes, mechanical wounding induced a similar, localized, wound periderm. In contrast, aphid colonization triggered more extended reactions, which differed among genotypes. In the susceptible genotype, aphids induced a reaction tissue, characterized after a month by thin-walled hypertrophied cells and a depletion of soluble phenolic compounds and starch. Anatomical features of this reaction tissue suggest that the aphid initiates a pseudogall in the cortical tissues of its susceptible host. In the resistant genotypes, however, the differentiation of the reaction tissue was totally or partially inhibited, probably because of extended lignification processes. The implications of a pseudogall induction on susceptible hosts’ physiology, and the impact of lignification on aphid development and behavior, are discussed.

Plant response to touch affects the behaviour of aphids and ladybirds

Touching between leaves of the same plant and/or by neighbouring plants is one of the most common mechanical stimuli to which an individual plant has to respond on a daily basis. The possible ecological implications of a plant’s response to touch on plant–insect interactions have not been explicitly investigated. We examined whether plant response to 1 min daily touching over a period of 6 days affects host plant acceptance by the bird cherry-oat aphid Rhopalosiphum padi L. on maize and by the black bean aphid Aphis fabae Scop. on bean, as well as olfactory preference of an aphid predator, seven-spotted ladybird Coccinella septempunctata L. Maize plants responded to touch with significant reduction in plant height, total plant biomass, leaf weight, leaf surface, shoot/root ratio and specific leaf area (SLA), while bean plants responded with reduced stem height and reduced SLA. Both aphid species showed significantly reduced acceptance of touched plants compared with untouched plants. The two aphid species and male and female ladybirds preferred volatiles from untouched plants over those from touched plants. Volatiles in the headspace of touched and untouched plants were collected and identified. Stepwise discriminant analyses identified (E)-nerolidol and (E)-β-caryophyllene in maize and 6-methyl-5-hepten-2-one and an unidentified sesquiterpene in bean as the best discriminating compounds in the volatile profiles of touched plants. Our study suggests that touch-induced changes in plants can potentially affect host plant selection by aphids and habitat searching by ladybirds. Thus, touch-induced changes in plants may have significant effects at higher trophic levels.

An ecological cost associated with protective symbionts of aphids

Beneficial symbioses are widespread and diverse in the functions they provide to the host ranging from nutrition to protection. However, these partnerships with symbionts can be costly for the host. Such costs, so called “direct costs”, arise from a trade-off between allocating resources to symbiosis and other functions such as reproduction or growth. Ecological costs may also exist when symbiosis negatively affects the interactions between the host and other organisms in the environment. Although ecological costs can deeply impact the evolution of symbiosis, they have received little attention. The pea aphid Acyrthosiphon pisum benefits a strong protection against its main parasitoids from protective bacterial symbionts. The ecological cost of symbiont-mediated resistance to parasitism in aphids was here investigated by analyzing aphid behavior in the presence of predatory ladybirds. We showed that aphids harboring protective symbionts expressed less defensive behaviors, thus suffering a higher predation than symbiont-free aphids. Consequently, our study indicates that this underlined ecological cost may affect both the coevolutionary processes between symbiotic partners and the prevalence of such beneficial bacterial symbionts in host natural populations.

Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host‐plant traits that mediate transmission by aphid vectors

The transmission of insect-vectored diseases entails complex interactions among pathogens, hosts and vectors. Chemistry plays a key role in these interactions; yet, little work has addressed the chemical ecology of insect-vectored diseases, especially in plant pathosystems. Recently, we documented effects of Cucumber mosaic virus (CMV) on the phenotype of its host (Cucurbita pepo) that influence plant-aphid interactions and appear conducive to the non-persistent transmission of this virus. CMV reduces host-plant quality for aphids, causing rapid vector dispersal. Nevertheless, aphids are attracted to the elevated volatile emissions of CMV-infected plants. Here, we show that CMV infection (1) disrupts levels of carbohydrates and amino acids in leaf tissue (where aphids initially probe plants and acquire virions) and in the phloem (where long-term feeding occurs) in ways that reduce plant quality for aphids; (2) causes constitutive up-regulation of salicylic acid; (3) alters herbivore-induced jasmonic acid biosynthesis as well as the sensitivity of downstream defences to jasmonic acid; and (4) elevates ethylene emissions and free fatty acid precursors of volatiles. These findings are consistent with previously documented patterns of aphid performance and behaviour and provide a foundation for further exploration of the genetic mechanisms responsible for these effects and the evolutionary processes that shape them.

Quantifying aphid behavioral responses to environmental change

AbstractAphids are the most common vector of plant viruses, and their feeding behavior is an important determinant of virus transmission. Positive effects of global change on aphid performance have been documented, but effects on aphid behavior are not known. We assessed the plant‐mediated behavioral responses of a generalist aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), to increased CO2 and nitrogen when feeding on each of three host species: Amaranthus viridis L. (Amaranthaceae), Polygonum persicaria L. (= Persicaria maculosa Gray) (Polygonaceae), and Solanum dulcamara L. (Solanaceae). Via a family of constrained Markov models, we tested the degree to which aphid movements demonstrate preference among host species or plants grown under varying environmental conditions. Entropy rates of the estimated Markov chains were used to further quantify aphid behavior. Our statistical methods provide a general tool for assessing choice and quantitatively comparing animal behavior under different conditions. Aphids displayed strong preferences for the same host species under all growth conditions, indicating that CO2‐ and N‐induced changes in plant chemistry have minimal effects on host preference. However, entropy rates increased in the presence of non‐preferred hosts, even when preferred hosts were available. We conclude that the presence of a non‐preferred host species affected aphid‐feeding behavior more than changes in plant leaf chemistry when plants were grown under elevated CO2 and increased N availability.

Classification of host plants of aphids (Homoptera, Aphidoidea) as related to their selection and use by aphids under the recent conditions of biogeocenosis transformation

Aphids are pests of agricultural crops and vectors of phytopathogenic viruses. At the same time they make up a very important component of biodiversity; for example, in Moldova only 9% of aphid species are pests. The trophic reactions of aphids related to selection and use of the host plants are far from being well-known. This paper presents an attempt at classification of the aphid host plants, based on analysis of the published data and those obtained by the authors in their studies in Leningrad Province of Russia and in the Republic of Moldova focused on the specific traits of epigenesis and population structure as well as the behavior, feeding, and reproduction of the aphids. The plants are classified by the degree of preference shown by the aphids.

Overexpression of IRM1 Enhances Resistance to Aphids in Arabidopsis thaliana

Aphids are insects that cause direct damage to crops by the removal of phloem sap, but more importantly they spread devastating viruses. Aphids use their sophisticated mouthpart (i.e. stylet) to feed from the phloem sieve elements of the host plant. To identify genes that affect host plant resistance to aphids, we previously screened an Arabidopsis thaliana activation tag mutant collection. In such mutants, tagged genes are overexpressed by a strong 35S enhancer adjacent to the natural promoter, resulting in a dominant gain-of-function phenotype. We previously identified several of these mutants on which the aphid Myzus persicae showed a reduced population development compared with wild type. In the present study we show that the gene responsible for the phenotype of one of the mutants is At5g65040 and named this gene Increased Resistance to Myzus persicae 1 (IRM1). Overexpression of the cloned IRM1 gene conferred a phenotype identical to that of the original mutant. Conversely, an IRM1 knockout mutant promoted aphid population development compared to the wild type. We performed Electrical Penetration Graph analysis to investigate how probing and feeding behaviour of aphids was affected on plants that either overexpressed IRM1 or contained a knockout mutation in this gene. The EPG results indicated that the aphids encounter resistance factors while reaching for the phloem on the overexpressing line. This resistance mechanism also affected other aphid species and is suggested to be of mechanical nature. Interestingly, genetic variation for IRM1 expression in response to aphid attack was observed. Upon aphid attack the expression of IRM1 was initially (after 6 hours) induced in ecotype Wassilewskija followed by suppression. In Columbia-0, IRM1 expression was already suppressed six hours after the start of the infestation. The resistance conferred by the overexpression of IRM1 in A. thaliana trades off with plant growth.

Volatile Exchange between Undamaged Plants - a New Mechanism Affecting Insect Orientation in Intercropping

Changes in plant volatile emission can be induced by exposure to volatiles from neighbouring insect-attacked plants. However, plants are also exposed to volatiles from unattacked neighbours, and the consequences of this have not been explored. We investigated whether volatile exchange between undamaged plants affects volatile emission and plant-insect interaction. Consistently greater quantities of two terpenoids were found in the headspace of potato previously exposed to volatiles from undamaged onion plants identified by mass spectrometry. Using live plants and synthetic blends mimicking exposed and unexposed potato, we tested the olfactory response of winged aphids, Myzus persicae. The altered potato volatile profile deterred aphids in laboratory experiments. Further, we show that growing potato together with onion in the field reduces the abundance of winged, host-seeking aphids. Our study broadens the ecological significance of the phenomenon; volatiles carry not only information on whether or not neighbouring plants are under attack, but also information on the emitter plants themselves. In this way responding plants could obtain information on whether the neighbouring plant is a competitive threat and can accordingly adjust their growth towards it. We interpret this as a response in the process of adaptation towards neighbouring plants. Furthermore, these physiological changes in the responding plants have significant ecological impact, as behaviour of aphids was affected. Since herbivore host plants are potentially under constant exposure to these volatiles, our study has major implications for the understanding of how mechanisms within plant communities affect insects. This knowledge could be used to improve plant protection and increase scientific understanding of communication between plants and its impact on other organisms.

Thiamine treatments alleviate aphid infestations in barley and pea.

Treatment of plants with thiamine (Vitamin B1) has before been shown to activate plant defence against microorganisms. Here, we have studied the effects of thiamine treatments of plants on aphid reproduction and behaviour. The work was mainly carried out with bird cherry-oat aphid (Rhopalosiphum padi L.) on barley (Hordeum vulgare L.). Aphid population growth and aphid acceptance on plants grown from seeds soaked in a 150μM thiamine solution were reduced to ca. 60% of that on control plants. R. padi life span and the total number of offspring were reduced on barley plants treated with thiamine. Healthy aphids and aphids infected with the R. padi virus were similarly affected. Spraying or addition of thiamine at 150μM to nutrient solutions likewise resulted in reduced aphid population growth to ca. 60%, as did plant exposure to thiamine odour at 4mM. Thiamine treatments resulted in reduced aphid population growth also when tested with grain aphid (Sitobion avenae F.) on barley and pea aphid (Acyrthosiphon pisum H.) on pea (Pisum sativum L.). There was no direct effect of thiamine on aphid reproduction or thiamine odour on aphid behaviour, as evaluated using artificial diets and by olfactometer tests, respectively. Two gene sequences regulated by salicylic acid showed higher transcript abundance and one gene sequence regulated by methyl jasmonate showed lower transcript abundance in thiamine-treated plants but not in control plants after aphid infestation. These results suggest that the aphid antibiosis and antixenosis effects may be related to priming of defence, but more studies are needed to explain the effects against aphids.

Modification of Non-Vector Aphid Feeding Behavior on Virus-Infected Host Plant

Virus-infected host plants can have positive, neutral or negative effects on vector aphids. Even though the proportion of non-vector aphids associated with a plant far exceeds that of vector species, little is known about the effect of virus-infected plants on non-vector aphids. In the present study, the English grain aphid Sitobion avenae (Fabricius) (Hemiptera: Aphididae), a non-vector of Wheat dwarf virus (WDV) and Cereal yellow dwarf virus-RPV (CYDV-RPV), was monitored on, virus-infected, virus-free and leafhopper/aphid-infested, and virus- and insect-free (control) barley, Hordeum vulgare L. (Poales: Poaceae), plants. Electrical penetration graph recordings were performed. Compared with the control plants, S. avenae on infected plants exhibited reduced non-probing and pathway phase, and increased phloem sap ingestion phase, and more aphids reached sustained phloem ingestion. However, the electrical penetration graph parameters described above showed no significant differences in aphid feeding behavior on virus-free and vector pre-infested plants and the control barley plants during S. avenae feeding. The results suggest that WDV/CYDV-RPV-infected host plants positively affected the feeding behavior of the non-vector aphid S. avenae. Based on these results, the reasons and trends among the virus-infected host plants' effects on the feeding behavior of non-vector aphids are discussed.

Ozone-mist spray sterilization for pest control in agricultural management

We developed a portable ozone-mist sterilization system to exterminate pests (harmful insects) in agricultural field and greenhouse. The system is composed of an ozone generator, an ozone-mist spray and a small container of ozone gas. The ozone generator can supply highly concentrated ozone using the surface dielectric barrier discharge. Ozone-mist is produced using a developed nozzle system. We studied the effects of ozone-mist spray sterilization on insects and agricultural plants. The sterilization conditions are estimated by monitoring the behavior of aphids and observing the damage of the plants. It was shown that aphids were exterminated in 30 s without noticeable damages of the plant leaves. The reactive radicals with strong oxidation potential such as hydroxyl radical (*OH), hydroperoxide radical (*HO2), the superoxide ion radical (*O2‒) and ozonide radical ion (*O3‒) can increase the sterilization rate for aphids.

A study of aphid behavior resulting in: A method of aphid repellence, the discovery of a strange descent of aphid, and variations in nourishment in development in kinds of aphid larvae

Aphids are very troublesome for farmers. However, pesticides often have an unexpected influence. In the first series of experiments, the team tested aphid's responses to odours and colours. They found crushed orange peel to be the most effective repellent and yellow to be the best attractive color. From this, they designed a simple method of keeping aphids away from plants. This team also noticed variation in larval body colors of a descent of aphids. In their second series of experiments, they discovered that this resulted in an asexually reproducing, winged adult and that larval nourishment requirements, survival rates, and ability to withstand fasting of this variation were different to other individuals of the same descent. They concluded that this adaptation had come about to enable the descent to survive even if the hosting plant is killed.

Recent Advances on Potato virus Y Research in Canada

Significant progress has been made in recent years in understanding pathological, serological and molecular properties of various strains of PVY and the aphid-mediated transmission. PVYO and PVYN appear to be the basic strain groups. Through genome recombination between these two groups, progeny groups whose genome possess one (e.g., PVYN:O or PVYN-Wi) to three (e.g., recombinant PVYNTN or European-PVYNTN) recombinant joints of PVYO and PVYN emerged. PVYN:O causes PVYN-like veinal necrosis in tobacco, but reacts to PVYO-specific antibody. PVYNTN causes potato tuber necrotic ringspot diseases in sensitive potato cultivars, and PVYN-like necrosis in tobacco plants, and reacts to PVYN-specific antibody. Through single nucleotide mutation(s), non-recombinant PVYNTN (or North American PVYNTN) also emerged from PVYN. It is also noteworthy that PVYN isolates originated from North America and Europe may have evolved separately; and to date most recombinant strains appear to be progenies of Eu-PVYN and PVYO. Several RT-PCR-based methodologies have been developed to characterize and detect various strains of PVY. A field survey revealed that PVYN:O has become a predominant strain in Manitoba and neighbouring states in USA. Moreover, three distinct variant groups inciting severe, intermediate and mild veinal/petiole/stem necrosis, respectively, on tobacco plants were observed within the PVYN:O isolates collected in Manitoba. Pathological and molecular diversity within PVYO strain group were revealed in New Brunswick, represented by PVYO-FL as a severe variant and by PVYO-RB as a mild variant. Studies on the transmission of PVY by various species of aphids revealed that aphid behavior plays an important role in the vector-mediated transmission. Application of mineral oil on the growing crop, especially in combination with use of crop borders, reduces aphid-mediated PVY transmission. Based on recent PVY research studies, Bartlett Superior 70 Oil was approved in 2011 for application to potato crops in Canada.

The potential of hydroxamic acids in tetraploid and hexaploid wheat varieties as resistance factors against the bird‐cherry oat aphid, Rhopalosiphum padi

AbstractThe potential for exploiting natural wheat resistance to control the cereal aphid Rhopalosiphum padi, the most important aphid pest of small grain cereals in the UK, was investigated as an alternative approach to the use of insecticides. The investigation focussed on a group of secondary metabolites, the hydroxamic acids or benzoxazinones, present naturally as glucosides, but which hydrolyse on tissue damage to give biologically active aglycones, e.g. 2,4‐dihydroxy‐7‐methoxy‐1,4‐benzoxazin‐3‐one (DIMBOA) which are associated with natural plant defence. These can be important for resistance against insects, fungi, bacteria and nematodes for a range of cultivated monocotyledonous plants and could ultimately be combined with other defence mechanisms to provide a general approach to cereal aphid control. Levels of hydroxamic acids, particularly DIMBOA‐glucoside, were determined in hexaploid (Triticum aestivum) and tetraploid (Triticum durum) wheat varieties and differences were found between species and varieties. The effect of feeding by R. padi on the level of hydroxamic acids in the leaf tissue was also investigated. Thus, after 24 h of aphid feeding, as an apparently localised hydrolytic defence reaction in the leaf, levels of DIMBOA‐glucoside decreased noticeably. When aphids were fed on sucrose solution containing low doses of DIMBOA there was a significant mortality compared to the sucrose control. However, the levels of and variation in hydroxamic acids in the wheat varieties investigated were insufficient for significant differences in aphid behaviour and development.

Evaluation of the Resistance of Different Tea Cultivars to Tea Aphids by EPG Technique

In order to investigate the resistance of tea plant to tea aphid, the feeding behavior of tea aphids on six different tea cultivars was monitored by (EPG) technique. The result showed that the duration of E1, E2 as well as (E1+E2) which was feeding waveforms of Toxoptera aurantii (Boyer) in tea phloem was significantly different by variance analysis (P<0.05) and so did the duration of the probing of T. aurantii in all the tea tissues. And the six tea cultivars were classified into three groups with cluster analysis, based on the six major parameters which were durations of np, C, E1, E2, F, and G waveforms, then the six major parameters of these three groups were detected by variance analysis, and the rank of six different tea cultivars' resistance to T. aurantii from strong to weak was Zhongcha 108, Sucha 1, Anjibaicha, Longjing 43, Xicha 5, and Sucha 120. As this result was in accord with the investigation into the tea field, we concluded that EPG technique was one of the most important means to examine tea plant resistance to T. aurantii and the durations of waveform E1, E2 and (E1+E2) were important parameters for evaluating resistance of tea plants to tea aphids.

Spatio-temporal dynamics of viruses are differentially affected by parasitoids depending on the mode of transmission.

Relationships between agents in multitrophic systems are complex and very specific. Insect-transmitted plant viruses are completely dependent on the behaviour and distribution patterns of their vectors. The presence of natural enemies may directly affect aphid behaviour and spread of plant viruses, as the escape response of aphids might cause a potential risk for virus dispersal. The spatio-temporal dynamics of Cucumber mosaic virus (CMV) and Cucurbit aphid-borne yellows virus (CABYV), transmitted by Aphis gossypii in a non-persistent and persistent manner, respectively, were evaluated at short and long term in the presence and absence of the aphid parasitoid, Aphidius colemani. SADIE methodology was used to study the distribution patterns of both the virus and its vector, and their degree of association. Results suggested that parasitoids promoted aphid dispersion at short term, which enhanced CMV spread, though consequences of parasitism suggest potential benefits for disease control at long term. Furthermore, A. colemani significantly limited the spread and incidence of the persistent virus CABYV at long term. The impact of aphid parasitoids on the dispersal of plant viruses with different transmission modes is discussed.

Stress response to acoustic stimuli in an aphid: A behavioral bioassay model

AbstractThe green peach aphid, Myzus persicae (Sulzer), feeds consistently and regularly throughout all stages of nymphs and adult. That is, honey dew production, which indicates a state of feeding, occurs at regular intervals within a given stage, and moving, which interrupts feeding, tends to occur rarely. We used these behaviors to test whether sound stimuli acted as a stress in this species. We conducted the playback experiment in which acoustic stimuli with a combination of five frequencies (100, 500, 1000, 5000, and 10000 Hz) and three intensity levels (66, 78, 90 dB SPL) were presented to all stages of aphids. Under all acoustic stimuli, honey dew production occurred less often, and moving occurred more often and for longer. The results of two‐way multivariate analysis of variance showed that the stimulus frequency was a significant factor for variation in aphid behaviors in the playback experiment. However, there was no intensity effect on the aphid's behavior. Based on the electrical penetration graph experiment, aphid feeding stopped frequently and lasted only for short durations under acoustic stimuli. The results of both experiments demonstrated that the acoustic stimuli were effective in inducing feeding suppression in this species. Thus, the acoustic stimuli may be a stressor in the green peach aphid. Furthermore, the behavioral bioassay employed in this study may be used to assess the effect of various stressors on aphids.

Interactions between tomato volatile organic compounds and aphid behaviour

In the tritrophic system consisting of tomato, Solanum lycopersicum (L.), the aphid Macrosiphum euphorbiae (Thomas) and its natural enemy, the parasitoid Aphidius ervi (Haliday), it has been shown that the release of volatile organic compounds following aphid attack is responsible for attracting aphid parasitoids in wind tunnel experiments. The main compounds involved in these multitrophic interactions have been characterized and quantified. In this work, the possible activity of such compounds on plant direct defences against the aphid M. euphorbiae was assessed in laboratory tests. The selected compounds were applied to uninfested tomato plants, either by evaporation or contact, and performance of aphids, in terms of plant acceptance, fixing behaviour and aphid development, calculated in standard conditions. The results showed that two compounds, namely methyl salicylate and cis-hex-3-en-1-ol, alter aphid performance. These two compounds have been reported to be those eliciting the best response by A. ervi in terms of flight behavior (wind tunnel bioassay) and antennal stimulation (EAG bioassay).

Activation of defence in sweet pepper, Capsicum annum, by cis‐jasmone, and its impact on aphid and aphid parasitoid behaviour

Two important pests of the sweet pepper, Capsicum annuum, are the peach potato aphid, Myzus persicae, and the glasshouse potato aphid, Aulacorthum solani. Current aphid control measures include the use of biological control agents, i.e., parasitic wasps, but with varying levels of success. One option to increase parasitoid efficiency is to activate plant defence. Therefore, sweet pepper plants were treated with the naturally occurring plant defence activator cis-jasmone, and its impact upon the behaviour and development of aphids and aphid parasitoids was investigated. Growth rate studies revealed that the intrinsic rate of population increase of A. solani and M. persicae on sweet pepper plants treated with cis-jasmone (cJSP) was not affected compared with untreated plants (UnSP), but the positive behavioural response of alate M. persicae towards the volatile organic compounds (VOCs) from UnSP was eliminated by cis-jasmone treatment 48 h previously (cJSP48). In addition, the aphid parasitoid Aphidius ervi preferred VOCs from cJSP48 compared with UnSP, and a significant increase in foraging time was also observed on cJSP. Analysis of VOCs collected from cJSP48 revealed differences compared with UnSP. There is evidence that treatment with cis-jasmone has the potential to improve protection of sweet pepper against insect pests.