Host-locating response by the aphid parasitoid Aphidius ervi to tomato plant volatiles

Abstract

The blend of volatile compounds emitted by tomato plants (Solanum lycopersicum) infested with the potato aphid (Macrosiphum euphorbiae) has been studied comparatively with undamaged plants and aphids themselves. Aphid-infested plants were significantly more attractive towards Aphidius ervi than undamaged plants and aphids themselves. Oriented response towards host-damaged plant, from which aphids were removed just before running the bioassay, did not differ from that recorded for infested plants. Collection of the volatiles and analysis by gas chromatography revealed only quantitative differences between uninfested and aphid-infested plants. Nine compounds, α-pinene, (Z)-3-hexen-1-ol, α-phellandrene, limonene, (E)-β-ocimene, p-cymene, methyl salicylate, (E)-β-caryophyllene and an unknown compound, were emitted at higher levels from aphid-infested plants than from undamaged control plants, whilst no differences were noted for hexanal, 6-methyl-5-hepten-2-one, and humulene (=α-caryophyllene). Synthetic standards of these compounds were tested in wind tunnel bioassays and all elicited a significant increase in oriented flight and landings on the target by the aphid parasitoid Aphidius ervi. (E)-β-caryophyllene resulted the most attractive towards female wasps. These results corroborate the hypothesis that the volatiles produced by the plant in response to aphid attack derive from both jasmonic and salicylic acid pathways, and are exploited by A. ervi as olfactory cues to locate its hosts.     

Chemically mediated associative learning in the host foraging behavior of the aphid parasitoidAphidius ervi (Hymenoptera: Braconidae)

The effect of experience on the responsiveness of the braconid parasitoidAphidius ervi to host(Acyrthosiphon pisum)-associated cues was investigated on bean plants(Vicia faba) using a wind tunnel bioassay. Oviposition experience on the plant-host complex significantly increased the oriented flight and landing responses ofA. ervi females to an undamaged plant and to a plant-host(A. pisum) complex. However, oviposition experience onA. pisum aphids when isolated from the plant did not change their responses to the intact plant and the complex. Searching on an unwashed plant which had been previously damaged byA. pisum also increased their response to an undamaged plant and a host-damaged plant, whereas the experience of searching on an undamaged plant did not significantly change their responses to undamaged plants. However, when parasitoids were allowed to search on an undamaged plant which had been sprayed withA. pisum honeydew, this significantly increased their response to an undamaged plant. Oviposition experience on the plant-host complex and foraging experience on a host-damaged plant or an undamaged plant sprayed with honeydew also significantly reduced the mean time taken by the parasitoids to respond in the wind tunnel. The behavioral changes associated with such experience were acquired within 30 min and persisted for at least 3 days. The results demonstrate the capacity ofA. ervi to learn associatively olfactory cues from plants, host-damaged plants, and plant-host complexes and confirm the role of aphid honeydew as a host recognition kairomone forA. ervi.     

The influence of a parasitoid's response to temperature on the performance of a tri‐trophic food web

1. Food web interactions are complex and can respond to environmental changes in unpredictable ways that do not necessarily equate to the individual responses of each of the components of the food web. 2. Biomass can be used to evaluate the productivity of the three individual trophic levels, in the form of the Net Generational Productivity (NGP) and the performance of the entire food web with the newly developed tri‐trophic food web performance ratio (?_3t). 3. These parameters were used to evaluate the performance of nine plant‐based tri‐trophic food webs composed of: potato, Solanum tuberosum L. and two cultivars of bell pepper Capsicum annuum L; three biotypes of the aphid Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) and the parasitoid wasp Aphidius ervi (Haliday) (Hymenoptera: Braconidae). 4. The NGP showed that the thermal window for biomass productivity for each trophic level is different and is reduced by approximately 4 °C with respect to the inferior level. Aphidius ervi had the smallest thermal window for biomass productivity and development. 5. The present results showed that the performance (?_3t) of the tested food webs is influenced in a top‐down fashion, where the intra‐specific variation of the food web, namely the host plant, played a major role in the productivity of each of the subsequent trophic levels. 6. The ?_3t suggested that exposure to high and low temperatures might severely affect the effectiveness of A. ervi as a biocontrol agent of the aphid M. euphorbiae in bell pepper and potato crops.     

The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus

Plant viruses and aphids can interact via contest competition for plant resources and induce changes in plant physiology, which can have effects on a third trophic level. The aim of this study was to determine how the interactions between a circulative plant virus and its aphid vector may affect the performance of an endoparasitoid and how parasitism may affect the efficiency of virus transmission by its aphid vector. The timing when parasitized aphids were transferred to virus-infected lettuce leaves was critical for the performance of A. ervi. Higher parasitoid larvae mortality, longer developmental times and lower percentages of mummification were detected on viruliferous/parasitized aphid nymphs when the time lag between parasitism and exposure to the virus was less than 24 h. No significant differences were detected in virus transmission rate between parasitized and non-parasitized M. euphorbiae aphids.     

Effect of Adult Experience on in-Flight Orientation to Plant and Plant–Host Complex Volatiles inAphidius erviHaliday (Hymenoptera, Braconidae)

The effect of adult experience on in-flight orientation to plant–host complex volatiles byAphidius erviHaliday was studied in a wind tunnel bioassay, usingAcyrthosiphon pisum(Harris), maintained on broad bean plants (Vicia faba) as host. A short oviposition experience (15 s) on the plant–host complex (PHC) was sufficient to induce a drastic decrease of flight propensity and stimulated a foraging behavior characterized by intense walking activity. However, flight activity resumed to normal levels 1 h after the oviposition experience on the PHC occurred. For parasitoids conditioned on the PHC for at least 1 min the recorded proportion making oriented flights to the PHC was significantly higher than that for naive females. In contrast, oviposition experience in the absence of plant material did not influence theA. erviflight response. Oviposition attempts on aphid dummies without egg release did not reduce flight activity. WhenA. ervifemales were exposed to glass beads coated withAc. pisumcornicle secretion, a priming effect was observed, resulting, compared with naive females, in a significantly higher rate of oriented flights to the PHC. In contrast, oviposition attempts visually induced by colored aphid dummies did not influence flight behavior. A strong reaction to volatile cues from uninfested plants was induced by oviposition experience on newly infested broad bean plants. This appears to be a case of associative learning. In fact, uninfested broad bean plants are basically unattractive to naiveA. ervifemales. The results demonstrate that adult experience has a considerable influence onA. ervibehavior and may have important implications for biological control of natural pest aphid populations.     

A comparison between two strains from Japan and Europe of Aphidius ervi

A European strain of Aphidius ervishall be introduced into Japan for the control of Macrosiphum euphorbiaeon greenhouse tomatoes. We compared this strain, which is originating from The Netherlands (EVP), with a native strain from Hokkaido, Northern Japan (SPR) in several characteristics. The percentage of parasitism of SPR and EVP was significantly different, when attacking three aphid species: 13% and 30% on M. euphorbiaeon tomato, 68% and 93% on Acyrthosiphon pisumon broad bean and 10% and 42% on Aulacorthum solanion sweet pepper, respectively. SPR and EVP differed morphologically (in the colouration of the petiole) and in the esterase banding patterns. Furthermore, cross mating experiments showed that SPR and EVP are partially reproductively isolated from each other. Complete reproductive isolation is evident in the one direction cross (EVP females and SPR males).     

Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi （Hymenoptera： Aphidiinae）

Intraguild predation （IGP） can be an important factor influencing the effective- ness of aphid natural enemies in biological control. In particular, aphid parasitoid foraging could be influenced by the presence of predators. This study investigated the effect of larvae of the predatory hoverfly Episyrphus balteatus DeGeer （Diptera： Syrphidae） and the multicolored Asian ladybird Harmonia axyridis Pallas （Coleoptera： Coccinellidae） on the foraging behavior of the aphid parasitoid, Aphidius ervi Haliday （Hymenoptera： Aphidiidae） in choice experiments using a leaf disc bioassay. Wasp response to chemical tracks left by those predator larvae was also tested. Parasitoid behavior was recorded using the Observer （Noldus Information Technology, version 5.0, Wageningen, the Netherlands）. The experiments were conducted under controlled environmental conditions using leaves of the broad bean plant, Viciafaba L. （Fabaceae） with Myzus persicae Sulzer （Homoptera： Aphididae） as the host complex. A. ervi females avoided aphid patches when larvae of either predator were present. A similar avoidance response was shown by A. ervi to aphid patches with E. balteatus larval tracks, whereas no significant response was observed to tracks left by H. axyridis larvae. It was concluded that IG predator avoidance shown by the aphid parasitoid A. ervi may be a factor affecting their distribution among host patches.     

Vector activity of three aphid species (Hemiptera: Aphididae) modulated by host plant selection behaviour on potato (Solanales: Solanaceae)

Viral diseases non-persistently transmitted by aphids are of great economic importance in several annual crops. Transmission efficiency of these non-persistent phytoviruses is dependant on vector efficiency (i.e. vector intrinsic ability to transmit the virus) but also on the vector activity that implies the early steps of aphid host plant selection process (i.e. brief intracellular stylet punctures after landing) and to their interplant movement ability. In Europe, Macrosiphum euphorbiae (Thomas 1878) is considered as one of the most serious virus vectors on potato (Solanum tuberosum L. 1753). Nevertheless, several alate aphid species that do not colonise potato plants are trapped in potato crops. Therefore, we investigated, through laboratory experiments, vector activity of one potato colonising aphid, M. euphorbiae, and two non-colonising potato aphids, the bird cherry-oat aphid Rhopalosiphum padi (L. 1758) and the pea aphid Acyrthosiphon pisum (Harris 1776). A settling experiment was used to evaluate dispersal activity, and the electrical penetration graph (EPG) technique was used to investigate probing activity on potato plants. Results showed that M. euphorbiae exhibited a better vector activity than other two aphid species in terms of landing and probing. By contrast, interplant movements were only recorded on non-colonising aphids, suggesting a better vector activity than M. euphorbiae in terms of locomotive behaviour. These data confirm the involvement of A. pisum and R. padi in the spread of non-persistent viruses.     

Co‐occurrence of defensive traits in the potato aphid Macrosiphum euphorbiae

1. Insecticide usage selects strongly for resistance in aphid populations, but this could entail fitness costs in other resistance traits. The potato aphid Macrosiphum euphorbiae Thomas exhibits intraspecific variation in susceptibility to parasitism by braconid wasps and provides a suitable species to study the relation between the defensive traits of parasitism and insecticide resistance. 2. Clonal lines (23 in total) of M. euphorbiae were established from aphids collected in 2013 from geographically separate populations in the U.K. Clonal lines belonged to five aphid genotypes, but one genotype predominated (78% of samples), and the facultative endosymbiont Hamiltonella defensa was detected in c. 40% of lines. 3. Total esterase activity in aphid tissues varied significantly between aphid genotypes and collection areas, but there was no clear pattern in relation to H. defensa infection or between collection sites likely to differ in insecticide pressures. 4. Five clonal lines representing low to moderate levels of enzyme activity, which included different aphid genotypes and presence/absence of H. defensa infection, were assayed for their susceptibility to the parasitoid wasp Aphidius ervi Haliday. Aphid mummification varied significantly between aphid genotypes, with low values in one genotype of aphids irrespective of H. defensa presence. 5. The results revealed that aphid lines belonging to the parasitism‐resistant genotype exhibited moderate levels of total esterase activity, indicating a competitve advantage for this genotype of M. euphorbiae when exposed to chemical and biological control factors in agroecosystems.     

Effects of jasmonate-induced defenses in tomato on the potato aphid, Macrosiphum euphorbiae

Jasmonates such as jasmonic acid (JA) are plant‐signaling compounds that trigger induced resistance (IR) to a broad range of arthropod herbivores. JA‐dependent defenses are known to reduce the growth and survivorship of many chewing insects, but their impact on piercing–sucking insects such as aphids has not been extensively investigated. In this study, induced resistance was activated in tomato (Lycopersicon esculentum Mill) (Solanaceae) using a foliar application of synthetic JA, and control plants were treated with carrier solution. The life parameters of individual potato aphids and their progeny (Macrosiphum euphorbiae Thomas) (Hemiptera: Aphididae) were evaluated on the unsprayed leaves of plants in order to access the systemic effects of the foliar treatments. IR significantly reduced the longevity and net reproduction of adult aphids, as well as the percentage of juveniles to survive to maturity. These results indicate that JA application induces systemic defenses in tomato that have a direct negative impact on aphid survivorship. This study also examined aphid honeydew excretion, in order to evaluate the potential influence of induced resistance on aphid feeding behavior. The average honeydew production per aphid was comparable on plants with or without JA treatment, indicating that JA‐dependent defenses did not deter feeding. This suggests that the observed effects of JA on aphid survivorship were due to antibiotic rather than antixenotic factors. In addition to studying the effects of JA treatment on a tomato cultivar that is susceptible to aphids, this study also examined the effects of exogenous application of JA on tomato plants that carry the aphid resistance gene, Mi‐1.2. JA application did not significantly enhance or inhibit aphid control on resistant tomato. These findings expand our understanding of the effects of JA‐dependent defenses on piercing–sucking insects, and of the potential interactions between induced resistance and R‐gene mediated aphid resistance in tomato.     

Effects of honeydew sugar composition on the longevity of Aphidius ervi

Feeding on sugar‐rich foods such as nectar and honeydew is important for survival of many adult parasitoids. Especially in agricultural systems, honeydew is often the most prevalent carbohydrate source. However, relative to plant nectar, honeydew may be relatively unsuitable, as a result of an unfavourable sugar composition or the presence of secondary plant compounds. We studied survival of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) on honeydew collected from various aphid species feeding on potato (Solanum tuberosum L., cv. Desiree) (Solanaceae), wheat (Triticum aestivum L., cv. Bobwhite) (Poaceae), or artificial diet, as well as the sugar composition of the different honeydews. Honeydews from the tested aphid species on potato, wheat, or artificial diet were found to be relatively suitable food sources for adult A. ervi, although not always as suitable as a 2 M sucrose solution. There were differences in honeydew sugar composition among the different aphid species on the various host plants. Multivariate statistics showed that the factor ‘aphid species’ had a significant influence on the sugar composition of the honeydew, explaining 27% of the variation in the potato system and 89% in the wheat system. When exploring the relationship between carbohydrate composition of the honeydews from aphids on potato and wheat plants, and their nutritional value for A. ervi, data revealed that differences in parasitoid longevity can to some extent be explained by carbohydrate composition. Furthermore, our results confirm that sucrose and its hexose components glucose and fructose are very suitable carbohydrate sources for hymenopteran parasitoids and show that parasitoid survival on an equimolar solution of the two monosaccharides glucose and fructose does not exceed performance on the disaccharide sucrose.     

Immediate alteration of Macrosiphum euphorbiae host plant-selection behaviour after biotic and abiotic damage inflicted to potato plants

The effects of potato [Solanum tuberosum L. (Solanaceae)] plant damage on the host plant-selection behaviour of the potato aphid, Macrosiphum euphorbiae Thomas (Homoptera: Aphididae), were studied. The damage inflicted to the plant was only of short duration and observations on aphid behaviour were made immediately following plant damage. The underlying questions of the study were to know how much time it takes for plant defence mechanisms to be activated and if this activation had noticeable repercussions on aphid behaviour. We considered stresses of various natures: biotic (pre-infestation by conspecifics or by Colorado potato beetles) and abiotic (scissor cuts). Aphid responses to host plant semiochemicals were investigated using a darkened arena bioassay and the probing behaviour was assessed using the electrical penetration graph technique. Aphids were attracted to their host plant (undamaged or damaged). In a preference test (undamaged plant vs. damaged plant), plants previously infested by conspecifics were preferred to undamaged plants, but this preference was not observed for heterospecific and abiotic damage. However, aphid probing behaviour was not modified on plants previously infested by conspecifics, whereas some changes were observed subsequently to heterospecific and abiotic damages. Our data present evidence that plants can respond to biotic and abiotic stresses soon after the damage is inflicted and when the damage is of short duration. The diverse consequences of these various local plant responses on M. euphorbiae behaviour are discussed in the context of plant defence strategies against aphid colonization.     

The Effect of Abiotic Factors on the Male Mate Searching Behavior and the Mating Success of Aphidius ervi (Hymenoptera: Aphidiidae)

The effect of wind speed and distance from the source on the male response of the aphid parasitoid, Aphidius ervi (Hymenoptera: Aphidiidae), to a pheromone source was studied in a wind tunnel. The number of males taking flight, entering the plume and successfully reaching the source, decreased at wind speeds >50 cm/s. Furthermore, the proportion of those attempting upwind flight that fell to the ground increased with increasing wind speed. In contrast, distance from the source had no significant effect on any of the parameters examined. While male flight behavior was significantly reduced at 70 cm/s, some males walked to the source when there was a bridge connecting the pheromone source and the release platform. This suggests that ambulatory behavior could be a significant component of male mate searching in A. ervi when wind conditions are too strong for upwind flight. The possible effects of variation in atmospheric pressure on male flight behavior to the long distance pheromone, as well as to the short distance one, were also investigated. No significant effects of atmospheric pressure were observed. These findings differ significantly from those previously reported for another aphid parasitoid, A. nigripes, and the reasons for such differences are discussed.     

The molecular bases of plant resistance and defense responses to aphid feeding: current status

Plant genes participating in the recognition of aphid herbivory in concert with plant genes involved in defense against herbivores mediate plant resistance to aphids. Several such genes involved in plant disease and nematode resistance have been characterized in detail, but their existence has only recently begun to be determined for arthropod resistance. Hundreds of different genes are typically involved and the disruption of plant cell wall tissues during aphid feeding has been shown to induce defense responses in Arabidopsis, Triticum, Sorghum, and Nicotiana species. Mi‐1.2, a tomato gene for resistance to the potato aphid, Macrosiphum euphorbiae (Thomas), is a member of the nucleotide‐binding site and leucine‐rich region Class II family of disease, nematode, and arthropod resistance genes. Recent studies into the differential expression of Pto‐ and Pti1‐like kinase genes in wheat plants resistant to the Russian wheat aphid, Diuraphis noxia (Mordvilko), provide evidence of the involvement of the Pto class of resistance genes in arthropod resistance. An analysis of available data suggests that aphid feeding may trigger multiple signaling pathways in plants. Early signaling includes gene‐for‐gene recognition and defense signaling in aphid‐resistant plants, and recognition of aphid‐inflicted cell damage in both resistant and susceptible plants. Furthermore, signaling is mediated by several compounds, including jasmonic acid, salicylic acid, ethylene, abscisic acid, giberellic acid, nitric oxide, and auxin. These signals lead to the development of direct chemical defenses against aphids and general stress‐related responses that are well characterized for a number of abiotic and biotic stresses. In spite of major plant taxonomic differences, similarities exist in the types of plant genes expressed in response to feeding by different species of aphids. However, numerous differences in plant signaling and defense responses unique to specific aphid–plant interactions have been identified and warrant further investigation.     

Exogenous application of liquid diet,previously fed upon by pea aphids Acyrthosiphon pisum (Harris), to broad bean leaves induces volatiles attractive to the specialist parasitic wasp Aphidius ervi (Haliday)

Proof of the existence of aphid-derived molecules that induce emission of volatile organic compounds as indirect defensive responses in plants (hereafter called elicitors) has not yet been obtained. We showed here the presence and some aspects of the chemical nature of these elicitors. Exogenous application of the fed diet (liquid diet previously fed on by the Pea aphid, Acyrthosiphon pisum) on the damaged part of leaves of broad bean plants, made the plants more attractive to a parasitic wasp, Aphidius ervi, than application of the unfed diet. This result suggested that elicitors existed in the fed diet. Chemical characterization using ultrafiltration and subsequent bioassay revealed that the responsible factor was larger than 3 kDa. Heating of the fed diet did not inactivate its ability to induce attractive volatiles, which suggested thermotolerance of the elicitor. These results contribute to the mechanistic understanding of plant defenses against aphids.     

The role of physical cues in the regulation of host recognition and acceptance behavior ofAphidius ervi Haliday (Hymenoptera: Braconidae)

The role of color and shape in the host recognition and acceptance behavior ofAphidius ervi Haliday was studied. A quantitative analysis of the oviposition behavior ofA. ervi was carried out with a computer-aided analysis of 150 video-recorded oviposition sequences on its natural host,Acyrthosiphon pisum (Harris). The importance of visual stimuli was assessed in a choice condition bioassay, observing the behavioral reaction of female parasitoids to various test materials flame-sealed into glass capillaries. Glass beads 2 and 6 mm in diameter and a flat arena were coated with cornicle secretion ofA. pisum, and their acceptance rates by both naive and experienced female parasitoids were assessed under no-choice conditions. In most cases,A. ervi females switched from random searching to attack position when the host was within a range of 1 cm, suggesting that host recognition is regulated in part by cues acting before physical contact. The glass capillary bioassay indicated that visual cues are important factors in the host recognition and acceptance phases. Pea aphid color alone can elicit the oviposition response of naiveA. ervi females, and this response is enhanced when color is combined with aphid shape. The cornicle secretion ofA. pisum stimulated an oviposition response which was stronger in naive females ofA. ervi than in experienced ones and was not significantly affected by the glass bead size or flat surface. These results, along with those from previous studies, suggest that manipulation of the oviposition behavior ofA. ervi is feasible under laboratory conditions.     

Specificity of induced resistance in the tomato, Lycopersicon esculentum

Specificity in the induced responses of tomato foliage to arthropod herbivores was investigated. We distinguished between two aspects of specificity: specificity of effect (the range of organisms affected by a given induced response), and specificity of elicitation (ability of the plant to generate distinct chemical responses to different damage types). Specificity of effect was investigated by examining the effect of restricted feeding by Helicoverpa zea on the resistance of tomato plants to an aphid species (Macrosiphum euphorbiae), a mite species (Tetranychus urticae), a noctuid species (Spodoptera exigua), and to a phytopathogen, Pseudomonas syringae pv. tomato. Prior H. zea feeding was found to increase the resistance of tomato plants to all four organisms. Specificity in elicitation was investigated by examining the effect of aphid feeding on the activities of four defense-related proteins and on the suitability of foliage for S. exigua. Aphid feeding was found to induce peroxidase and lipoxygenase activities but not polyphenol oxidase and proteinase inhibitor activities; this response is distinct from the response to H. zea feeding, which induces polyphenol oxidase and proteinase inhibitors but not peroxidase. Leaflets which had been fed upon by aphids were better sources of food for S. exigua than were leaflets which had not been fed upon by aphids. Studies of both these aspects of specificity are needed to understand the way in which plants coordinate and integrate induced responses against insects with other physiological processes. Received: 20 December 1996 / Accepted: 2 July 1997     

The effect of different plant nutrient regimes on the aphid Macrosiphum euphorbiae growing on petunia

Three experiments were conducted to study how nutrient content of the host plant, Petunia axillaris hybrida Villm. Grandiflora Group, affects the performance of Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae). Aphid performance was analysed in relation to plant nutrient levels and the ratio of nitrogen to potassium (N/K). Phosphorus (P) had a positive effect on several parameters of aphid performance. Both P and K were associated with a short development time but a strong correlation between P and K content made it impossible to detect their relative importance. In one experiment aphid performance was significantly lower on unfertilised plants with low N content, suggesting a positive effect of N. A high N/K ratio did not, in general, increase aphid performance. The complexity of plant nutrient content on aphid performance suggests that not only nutrient levels but also ratios of nutrients must be considered.     

Waxy bloom in peas influences the performance and behavior of Aphidius ervi, a parasitoid of the pea aphid

Leaf surface waxy bloom can influence the predator–prey interactions that take place on peas. We tested whether the interaction between the pea aphid Acyrthosiphon pisum Harris (Homoptera: Aphidae) and a parasitoid, Aphidius ervi Haliday (Hymenoptera: Aphidiidae), is affected by reduced wax. We performed greenhouse experiments comparing aphid parasitism by individual A. ervi on two varieties of reduced wax peas to two normal wax sister varieties. We also observed the behavior of individual A. ervi in the greenhouse and measured field parasitism in small plots of reduced wax and normal wax peas. In the greenhouse, individual A. ervi parasitized more aphids on the reduced wax varieties than on their normal wax counterparts. Wasps spent more time actively foraging on reduced wax pea plants, which may contribute to the higher parasitism observed on those varieties. The greenhouse results suggested that the improved performance of individual A. ervi on reduced wax peas might contribute to a higher parasitism on reduced wax peas in the field. Field parasitism was significantly higher in reduced wax pea plots during 2000. Overall parasitism was higher in 2000 than in 2001 and 2002. In the latter years, parasitism was higher on reduced wax plants, but not significantly different from normal wax plants. Improved foraging by individual A. ervi resembles improved foraging by other carnivorous insects on reduced wax peas. The advantages of reduced wax for biological control of the pea aphid may hold when any of several different natural enemies is abundant.     

Ecology of the aphid pests of protected pepper crops and their parasitoids

Myzus persicae, Macrosiphum euphorbiae, Aphis gossypii and Aulacorthum solani (Homoptera: Aphididae) are principal pests of protected pepper crops in southeastern Spain. Our goal was to determine the incidence of aphids on pepper crops and the role of vegetation surrounding greenhouses as a source of aphids and their parasitoids. The population dynamics were followed in six commercial greenhouses during 3 years. Another 82 greenhouses and their surrounding vegetation were surveyed occasionally. Myzus persicae had the highest incidence in pepper greenhouses followed by M. euphorbiae and A. solani. Parasitism of all aphid species in greenhouses was low, Aphidius matricariae and Aphidius colemani being the most abundant parasitoids. Myzus persicae and Macrosiphum euphorbiae were the most abundant and polyphagous aphids, being present on 77 and 55% of the plants sampled outside greenhouses, respectively; species of Brassicaceae were the main hosts for both aphids. Aulacorthum solani was only present on Malva parviflora and at low numbers. Outside greenhouses, A. matricariae was the most common parasitoid of M. persicae, followed by Diaeretiella rapae and A. colemani. Aphidius matricariae was the most polyphagous, being present in 10 out of 22 aphid species. Macrosiphum euphorbiae and A. solani were both parasitised by A. ervi and Praon volucre. Aphelinus asychis was found on A. solani. Parasitoids were found in other aphids not attacking pepper. The role of natural vegetation as a reservoir of aphid pests of pepper and of parasitoids is discussed.