Occurrence of different development time patterns induced by photoperiod in Anagrus atomus (Hymenoptera: Mymaridae), an egg parasitoid of Empoasca vitis (Homoptera: Cicadellidae)

The wasp Anagrus atomus L. parasitizes eggs of the cicadellid Empoasca vitis (Göthe) on grapevines during the vegetative season. In vineyards, abundant parasitoid emergence occurs in the autumn as a result of a developmental delay in part of the A. atomus population. In this context, physiological times required by the parasitoid to develop in E. vitis eggs are recorded during the summer. In early summer, all individuals develop fully, with physiological times in agreement with those reported in the literature. From early August onwards, an increasing proportion of parasitoids show a delay in development involving pre‐imaginal stages. Under transmission microscopy, larvae of A. atomus inside the eggs of E. vitis can be clearly differentiated as ‘light’ and ‘dark’ types, which are associated with normal and delayed development, respectively. The decreasing photoperiod as autumn approaches appears to promote the retardation of growth. This phenomenon can be considered a typical case of risk spreading because, when the availability of E. vitis eggs in vineyards is high (i.e. in early summer), A. atomus shows (i) only a normal developmental pattern that allows a faster population increase, whereas (ii) when E. vitis egg availability begins to be scarce (i.e. from mid summer), an increasing proportion of individuals having delayed development provides better fitness because it allows the parasitoid to synchronize its life history with leafhopper species that lay overwintering eggs on plants other than grapevines.     

Influence of grapevine cultivars on the leafhopper <Emphasis Type="Italic">Empoasca vitis</Emphasis> and its egg parasitoids

The leafhopper Empoasca vitis (Göthe) (Homoptera: Cicadellidae) can cause economic damage in European vineyards. Egg parasitoids, in particular Anagrus atomus (Linnaeus) (Hymenoptera: Mymaridae), are the most important natural enemies of the leafhopper. In four different years, leaves of ten grapevine cultivars, which were grown in a vineyard of north-eastern Italy, were collected at the end of the leafhopper 2nd generation to determine the total number of E. vitis eggs per leaf and the percentage of the E. vitis eggs parasitized. These data were analysed for correlation with leaf density and foliar pubescence. The E. vitis eggs per leaf and the percentage of eggs parasitized by Anagrus spp. were significantly influenced by the cultivar. The number of E. vitis eggs per leaf was positively correlated to leaf density, but it was not influenced by leaf hair density. The parasitization rate by Anagrus spp. was affected by foliar pubescence, especially by erect hairs on the veins. These findings could be used for integrated pest management. In particular, (1) the more susceptible cultivars can be used as early indicators of leafhopper infestation, (2) agronomic practices, that reduce leaf density, could decrease the E. vitis population level and (3) clones with glabrous leaves would favour egg parasitoid activity.     

Reducing the abundance of leafhoppers and thrips in a northern California organic vineyard through maintenance of full season floral diversity with summer cover crops

1 Maintenance of floral diversity throughout the growing season in vineyards in the form of summer cover crops of buckwheat (Fagopyrum esculentum Moench) and sunflower (Helianthus annus Linnaeus), had a substantial impact on the abundance of western grape leafhoppers, Erythroneura elegantula Osborn (Homoptera: Cicadellidae), and western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), and associated natural enemies. 2 During two consecutive years, vineyard systems with flowering cover crops were characterized by lower densities of leafhoppers and thrips, and larger populations and more species of general predators, including spiders. 3 Although Anagrus epos Girault (Hymenoptera: Mymaridae), the most important leafhopper parasitoid, achieved high numbers and inflicted noticeable mortality of grape leafhopper eggs, no differences in egg parasitism rates were observed between cover cropped and monoculture systems. 4 Mowing of cover crops forced movement of Anagrus and predators to adjacent vines resulting in the lowering of leafhopper densities in such vines. 5 Results indicate that habitat diversification using summer cover crops that bloom most of the growing season, supports large numbers of predators and parasitoids thereby favouring enhanced biological control of leafhoppers and thrips in vineyards.     

Influence of flowering cover crops on Anagrus parasitoids (Hymenoptera: Mymaridae) and Erythroneura leafhoppers (Homoptera: Cicadellidae) in New York vineyards

Abstract 1 We tested the hypothesis that providing nectar‐producing cover crops will enhance the biological control of grape leafhoppers (Erythroneura spp.) by Anagrus wasps in commercial vineyards in New York, U.S.A. 2 We established three cover crops between vine rows in a commercial vineyard: buckwheat (Fagopyrum esculentum (Moench)), clover (Trifolium repens L.) and mowed sod (Dactylis glomerata L.). 3 There was no effect of cover crop on adult Anagrus in 1996, whereas in 1997 adults were more abundant within edge vines with buckwheat compared to vines with clover or sod; adults were more abundant at the vineyard edge, especially early in the season. 4 Parasitism of ‘sentinel’ leafhopper eggs was higher on vines with buckwheat compared to parasitism on vines with clover or sod in 1996; a similar, non‐significant trend, was observed in 1997. 5 Neither the abundance nor the distribution of leafhoppers was influenced by cover crops, although in 1997 there was a trend toward greater numbers of nymphs on edge vines with buckwheat. 6 In a cage experiment, parasitism by Anagrus of leafhopper eggs on grapes was greater when adults had access to flowering buckwheat rather than buckwheat without flowers. 7 In a laboratory study, longevity of female Anagrus was increased when provided with honey or sugar water compared to water only or nothing. 8 Our results suggest that parasitism of grape leafhoppers by Anagrus may be enhanced by providing floral resources within vineyards in New York, although it is unclear whether this will produce meaningful reductions in pest abundance.     

Biology of Anagrus atomus (Hymenoptera: Mymaridae), an egg parasitoid of the grape leafhopper Arboridia kermanshah (Homoptera: Cicadellidae)

Biology, morphology and oviposition behavior of Anagrus atomus (Linnaeus), an egg parasitoid of the grape leafhopper Arboridia kermanshah Dlabola in Isfahan, Iran, were investigated. Adults were smaller than those so far reported from other regions. Females continuously drummed on plant surfaces with their antennae to search for host eggs. Parasitoid eggs hatched 2–3 days after oviposition, and A. atomus had two larval instars. First instar larvae were sacciform and immobile. Second instar larvae appeared 4 days after oviposition and were very active, and doubled their body length. The prepupal and pupal stages lasted for 1 and 5–6 days, respectively. Adult emergence began 16 days after oviposition, and peaked on day 17.     

The impact of sulfur on the reproductive success of <Emphasis Type="Italic">Anagrus</Emphasis> spp. parasitoids in the field

Pesticides targeted at pest species have often been demonstrated to have strong adverse effects on the survival of biological control agents in short-term laboratory bioassays; however, studies examining the influence of pesticides on the actual reproductive success of biological control agents in the field are rare. Because natural enemy reproduction is often directly tied to biological control success, effects of pesticides on reproduction are of central importance. Here we use a new technique to examine the influence of sulfur, a fungicide widely used in grape production, on the reproductive success of Anagrus erythroneurae (Hymenoptera: Mymaridae) and Anagrus daanei (Hymenoptera: Mymaridae), egg parasitoids of the grape leafhopper, Erythroneura elegantula (Homoptera: Cicadellidae). Sulfur has previously been shown to be highly toxic to Anagrus spp. in short-term laboratory and field bioassays, creating the expectation that sulfur should also reduce Anagrus reproductive success in the field. Surprisingly, in two studies, the first comparing the oviposition success of Anagrus collected live in paired sulfur-treated versus untreated vineyards and the second comparing the lifetime reproductive success of Anagrus collected at the end of their lives in unpaired sulfur-treated versus untreated vineyards, we found no effect of sulfur on parasitoid reproductive success. In this system, traditional short-term assays of laboratory toxicity do not appear to predict effects on parasitoid reproductive success, suggesting that demographic approaches to assessing the disruptive effects of pesticides may have an important role in designing IPM programs.     

The dynamics of grape leafhopper Empoasca vitis Göthe populations in southern Switzerland and the implications for habitat management

The life cycle of Empoasca vitis and its most important parasitoid Anagrus atomus in southern Switzerland can be divided into three phases. In phase I the adults of E. vitis move from overwintering sites, i.e. primarily conifers, over deciduous plants into the vineyards. The parasitoid A. atomus on the other hand, appears to overwinter in leafhopper eggs, mainly on roses and blackberries. It subsequently completes one generation in leafhopper eggs primarily on blackberries and hazelnuts, before it attacks E. vitis eggs in the vineyards. For phase II, a population model with time‐varying age structures and stochastic properties was constructed for E. vitis. For this purpose a time‐varying distributed delay model with attrition was constructed. Given the calibrated initial density of overwintering females, the model predicts an unacceptable number of E. vitis for the growing season. However, if egg parasitism of A. atomus and Stethynium triclavatum is introduced into the model as an external variable E. vitis densities are predicted which are economically irrelevant. Inphase III E. vitis adults leave the vineyards for the overwintering sites. The model shows the importance of the parasitoid A. atomus during phase II. A. atomus should be favoured by surrounding the vineyards with host plants carrying leafhoppers’ eggs. Consequently, habitat management measures for E. vitis control could be applied to the surroundings of the vineyards.     

Searching and Oviposition Behavior of Anagrus atomus L. (Hymenoptera: Mymaridae) on Four Host Plants of Its Host, the Green Leafhopper Empoasca decipiens Paoli (Homoptera: Cicadellidae)

Anagrus atomus L. is an important egg parasitoid of the green leafhopper Empoasca decipiens Paoli. In this study the ability of the parasitoid to locate and parasitize its host was investigated on four host plants, i.e., broad beans (Vicia faba L.), sweet pepper (Capsicum annuum L.), cucumber (Cucumis sativus L.), and French beans (Phaseolus vulgaris L.). For each plant species, the behavior of the parasitoid was observed on E. decipiens infested and noninfested plants. Searching and oviposition behavior were characterized by drumming, probing, and resting. Parasitoids spent significantly less time on non-infested than infested plants, 274.5 and 875.7 s, respectively, and no probing behavior was observed on non-infested plants. Frequency of resting behavior was significantly greater on non-infested than on infested plants. Total foraging time was significantly longer on infested than on non-infested plants, indicating that A. atomus females can efficiently discriminate between leaves with and without infestation. Parasitism of A. atomus was influenced by parasitoid density, with the highest parasitism rate (64.0%) obtained at a density of 10 A. atomus females/0.1356 m² but the number of parasitized eggs per female and the searching efficiency decreased with increasing parasitoid density.     

Life-table study of Anagrus atomus, an egg parasitoid of the green leafhopper Empoasca decipiens, at four different temperatures

The objective of our study was to assess thepotential of the egg parasitoid Anagrusatomus L. (Hymenoptera: Mymaridae) for controlof the greenhouse leafhopper Empoascadecipiens Paoli (Homoptera: Cicadellidae). Theegg-adult development time, survivorship andreproduction of A. atomus were evaluatedat four constant temperatures (16, 20, 24 and28°C). Developmental time ranged from33.6 days at 16°C to 13.3 days at 28°C. Based on a linear regression ofdevelopment rate on temperature the lowerthreshold was estimated at 8.39°C. Anagrus atomus required 263.2 degree-days tocomplete its development from egg to adult. Theegg-adult survival rate and the sex ratio weresignificantly lower at 28°C than at theother three temperatures tested. The intrinsicrate of increase (r _m) variedsignificantly between all four temperatures.The potential of A. atomus to attackdifferent host ages was additionallyinvestigated. Host eggs were parasitizedthroughout their development but rate ofparasitism was reduced in host eggs older thansix days. The number of eggs parasitized waspositively density dependent but the rate ofparasitism decreased with increasing hostdensity. A maximum rate of parasitism of 62.5%was recorded. The potential impact of the eggparasitoid on the population dynamics of E. decipiens is discussed.     

New techniques of rearingAnagrus flaveolus [Hym.: Mymaridae], an egg parasitoid of the brown planthopper

A small cage was designed to study the biology and behavior ofAnagrus flaveolus Waterhouse, an important egg parasitoid of the brown planthopper,Nilaparvata lugens (Stal), a pest of rice. A method of rearing moderate numbers of parasitoids on planthopper eggs in the laboratory was developed. Though the mymaridAnagrus flaveolus Waterhouse, a common egg parasitoid of rice planthoppers and leafhoppers all over Asia, reduces pest populations, its biological control potential has largely been overlooked because of its minute size and the lack of suitable techniques to study and rear it in the laboratory.Ôtake (1968, 1969) described some techniques to study the development, longevity and fecundity of a related speciesAnagrus nr.flaveolus Waterhouse. The cages described herein are much simpler to build and more efficient to use compared with those developed earlier. Rearing this important parasitoid in large numbers in the laboratory has not been done before.     

Habitat diversification tactic for improving biological control: parasitism of the western grape leafhopper

In a previous study we demonstrated greater abundance of the parasitoid Anagrus epos (Girault) in grape vineyards located downwind of prune trees that function as overwintering habitats. This study examines whether these higher A. epos numbers translated into higher egg parasitism rates of the grape leafhopper, Erythroneura elegantula (Osborn). Paired commercial wine-grape vineyard plots, one with and one without adjacent prune trees, were studied within a complete block design in northern and central California. A. epos was the key mortality factor affecting E. elegantula eggs. Point estimates of A. epos parasitism rates were significantly greater in vineyards associated with prune trees during the first E. elegantula generation in both 1991 and 1992. No consistent differences in parasitism rates were observed during the second or third generations. The results indicated that prune trees enhance early season parasitism rates. Cumulative estimates of egg parasitism across E. elegantula generations demonstrated that enhanced early-season parasitism resulted in a net season-long increase in the degree of mortality imposed by A. epos on E. elegantula eggs. Two factors were found to influence parasitism rates: the abundance of early-season A. epos adults moving into vineyards and the density of E. elegantula eggs in vineyards. Our results indicate that diversification of vineyards using prune trees supports overwintering populations of a specialist parasitoid and thereby alters host-parasitoid interactions to favor enhanced parasitism in vineyards.     

Larval development of Empoasca vitis and Edwardsiana rosae (Homoptera: Cicadellidae) at different temperatures on grapevine leaves

The grape leafhopper Empoasca vitis (Homoptera: Cicadellidae) is regarded as a major insect pest in many European grapevine growing areas, with an increasing importance realized in recent years maybe as a result of climatic change. Both larvae and adults feed on the phloem vessels of the leaves, causing characteristic symptoms also referred to as hopperburn. Phenology of adult leafhoppers was monitored in one vineyard in three successive years and indicated that immigration of a few hibernated E. vitis individuals into vineyards might take place already quite early in the year depending on winter temperatures and starts to progress in substantial numbers right at grapevine bud burst. In addition, these monitoring studies have shown that there are several other leafhopper species occurring on grapevine plants besides E. vitis, such as the rose leafhopper Edwardsiana rosae (Homoptera: Cicadellidae). Here, we report on the development of larval instars of both leafhopper species, E. vitis and E. rosae on grapevine leaves under different temperature regimes in the laboratory. Shortest larval developmental time was observed at night temperatures of 13–15°C and day temperatures of 23–25°C, which was in agreement with predicted optimal temperatures for both species. At the temperature regime of 20°C night and 30°C day temperature, either no egg hatch was observed or early development of first‐instar larvae was not successful for both species. These results suggest that warm (18°C) nights and moderately warm (28°C) days are representing the upper thermal threshold for development of both E. vitis and E. rosae embryonic stages on grapevine leaves, questioning current assumptions of an increasing importance of E. vitis as a grapevine pest under future climate change.     

Grapevine leaf gas exchange, plant growth, yield, fruit quality and carbohydrate reserves influenced by the grape leafhopper,Empoasca vitis

The impact of the grape leafhopper,Empoasca vitis, on leaf gas exchange, plant growth, yield, fruit quality and carbohydrate reserves of the grapevines,Vitis vinifera L., was studied. Gas exchange was measured on the discolored (red) and the green parts of infested main leaves and on leaves from uninfested vines. Photosynthesis and mesophyll conductance were severely reduced on main leaves showing leafhopper feeding symptoms. The stomatal conductance of the red leaf section of infested main leaves was lower than on undamaged control leaves. Additionally, the red leaf section of infested main leaves showed lower transpiration rates when compared to the green parts of the same leaves and to undamaged control leaves. Gas exchange processes of lateral leaves were not affected by leafhopper feeding. Leafhopperload on main leaves was correlated to visual damage symptoms. At 71.8 leafhopper-days per leaf up to 40% of the main leaf area of the infested plants was discolored from the borders towards the center. Lateral leaves showed no feeding symptoms. Shoot diameter, pruning weight and carbohydrate reserves in the wood were not affected by leafhoppers. Lateral leaf area growth was significantly stimulated on plants infested by leafhoppers. No decrease in yield and fruit quality with leafhopper-loads up to 71.8 leafhopper-days per leaf were observed.     

The effect of sulfur on biological control of the grape leafhopper, <Emphasis Type="Italic">Erythroneura elegantula</Emphasis>, by the egg parasitoid <Emphasis Type="Italic">Anagrus erythroneurae</Emphasis>

We examined the toxicity of a fungicide, sulfur, to the egg parasitoid Anagrus erythroneurae (Hymenoptera: Mymaridae) Trjapitsyn and Chiapini and the vineyard leafhopper pest Erythroneura elegantula Osborn (Homoptera: Cicadellidae) and tested whether or not the use of sulfur in the field affects biological control of E. elegantula. Using field cage bioassays, we demonstrated that sulfur is toxic to adult A. erythroneurae parasitoids, but not toxic to adult E. elegantula leafhoppers. We nonetheless found in a field experiment that sulfur produced no changes in rates of parasitism or E. elegantula egg density, and generated only a very small increase in the density of E. elegantula nymphs. These results suggest that sulfur, although toxic to A. erythroneurae, is not highly disruptive of E. elegantula biological control in vineyards. Our results suggest that simple bioassays of acute toxicity may not accurately predict the impact of agricultural chemicals on biological control.     

Non‐host plant essential oil volatiles with potential for a ‘push‐pull’ strategy to control the tea green leafhopper,Empoasca vitis

The tea green leafhopper, Empoasca vitis Göthe (Hemiptera: Cicadellidae), is an economically important pest of tea crops, Camellia sinensis (L.) O. Kuntze (Theaceae), in China. The use of non‐host plant essential oils for manipulation of E. vitis was investigated for potential incorporation into a ‘push‐pull’ control strategy for this pest. The effectiveness of 14 plant essential oils in repelling E. vitis was investigated in laboratory assays. Rosemary oil, geranium oil, lavender oil, cinnamon oil, and basil oil repelled leafhoppers in a Y‐shaped olfactometer. We also compared the efficacy of these five plant essential oils to repel E. vitis in the presence of a host plant volatile‐based leafhopper attractant, (Z)‐3‐hexenyl acetate, in a tea plantation. In the treatment combination, four plates (north, south, east, and west) treated with an essential oil surrounded a central sticky plate treated with (Z)‐3‐hexenyl acetate. Fewer E. vitis were found on the plates treated with rosemary oil (12.5% reduction) than on the four water‐sprayed control treatment plates surrounding a central plate with (Z)‐3‐hexenyl acetate. We compared the distribution of E. vitis on the plates, and the relative numbers of E. vitis on each plate were compared with similar plates in the control treatment. When four plates treated with rosemary oil surrounded a central (Z)‐3‐hexenyl acetate‐treated plate, the distribution of E. vitis on the different plates changed significantly compared with that of the control. Relatively fewer E. vitis were found on the east (13.0% reduction) rosemary oil‐treated plates and more E. vitis (11.3% increase) were found on the central attractant‐treated plate. Our findings indicate that rosemary oil is a promising leafhopper repellent that should be tested further in a ‘push‐pull’ strategy for control of E. vitis.     

Compatibility of Chemical Disease and Insect Management Practices Used in New York Vineyards with Biological Control by Anagrus spp. (Hymenoptera: Mymaridae), Parasitoids of Erythroneura Leafhoppers

Toxicity to Anagrus spp. of fungicides and insecticides used in grape production was assessed with laboratory and field bioassays. Field-equivalent rates of fungicides were relatively nontoxic to Anagrus spp. adults in laboratory bioassays. In bioassays with field-weathered residues, sulfur (9600 ppm) caused elevated mortality of adults for 14 to 21 days posttreatment. Residues of microencapsulated methyl parathion (600 and 1200 ppm) increased mortality relative to the control up to 43 days posttreatment. Duration of elevated mortality of adults exposed to carbaryl was dose dependent and ranged from 14 (at 1200 ppm) to >43 days (at 4800 ppm). Residues of carbaryl and methyl parathion applied over parasitized eggs had little effect on emergence, but may have delayed development. In a field trial, adults trapped in carbaryl-treated plots were significantly reduced starting 3 weeks after treatment. Subsequent lower trap catches may have been related to effects of residues on Anagrus spp. adults or to lower leafhopper egg densities in treated plots.     

Influence of adult diet on fitness and reproductive traits of the egg parasitoid Anagrus virlai (Hymenoptera: Mymaridae), a potential biocontrol agent against the corn leafhopper

Dalbulus maidis is the most important leafhopper pest of maize in the Americas. Anagrus virlai is an egg parasitoid commonly associated with the corn leafhopper. We evaluated whether the performance of A. virlai is dependent on different diets provided during 24 hr or throughout adult female lifetime. Additionally, functional response of A. virlai on D. maidis eggs using maize leaves containing honeydew plus honey was described. A. virlai is a mostly pro-ovigenic autogenic species whose females are able to parasitize eggs immediately after emergence. We found that wasps oviposit the majority of their eggs in the first day of their adult life. Realized lifetime fecundity and lifetime potential fecundity did not differ significantly among treatments, but longevity and egg production increased when honey was added to diet. Data were consistent with an intermediate functional response between type II and III, but closer to type II, indicating a high parasitism rate at low host densities and a decrease in the oviposition rate at high host densities, due to a possible egg limitation. Our results suggest that carbohydrate food sources (honeydew and honey) might not be the factor limiting reproductive success during the first 24 hr. Food supply, however, might influence egg maturation and survivorship of wasps, thus potentially enhancing biological pest control when hosts are scarce in the course of the first few days of adulthood.     

An integrative approach to species discrimination in the Anagrus atomus group sensu stricto (Hymenoptera: Mymaridae), with a description of a new species

Egg parasitoids of the genus Anagrus Haliday (Hymenoptera: Mymaridae) are natural enemies of many pests around the world. We used an integrative approach to characterize some species belonging to the Anagrus atomus group, using specimens reared from leafhoppers infesting some Lamiaceae. Starting from morphological identifications based on available keys, we carried out a multi-locus genetic characterization using phylogenetic and species delimitation analyses, and integrated it with biological and morphometric evidence. This approach revealed the existence of a new species, A. nepetellae sp. nov., here described along with its phenological traits. The approach also allowed us to characterize the expected taxonomic stability of other putative species within the group. We propose two new species groups called the atomus group sensu stricto and the vilis group, with the goal of streamlining the taxonomy of the atomus group. We also present a key for the identification of females of the European species of the atomus group sensu stricto. Some specimens show heterozygosity in 28S-D2 sequences, suggesting hybridization between A. atomus and A. nepetellae, which, if it is common between other species as well, could partly explain the taxonomic problems in the genus Anagrus. DNA sequencing of specimens reared by the same biofactory at different times suggests involuntary contamination leading to the displacement of a laboratory strain of A. atomus by A. nepetellae, which may have resulted from undetected partial reproductive compatibility.http://zoobank.org/urn:lsid:zoobank.org:pub:DFCD7654-5AA5-4E4F-AE48-24377BAACEFE     

Measuring the host preference of parasites: An aid in evaluating biotypes ofAnagrus epos [Hym.: Mymaridae]

Populations ofAnagrus epos Girault are being imported and evaluated for the biological control of variegated grape leafhopper,Erythroneura variabilis Beamer, a newly introduced pest of grapes in central California. To distinguish different biotypes, a field test was developed that quantifies host preference.E. epos collected from geographically isolated regions of western United States and northern Mexico showed different levels of preference towards the variegated leafhopper and its close relative the grape leafhopper,Erythroneura elegantula Osborn, a native to central California. Host preference values may aid in the identification of relased biotypes using leafhopper eggs on leaves sampled from release sites.      

Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape

1. Egg parasitoids in the genus Anagrus (Hymenoptera: Mymaridae) are important mortality factors for grape leafhoppers ( Erythroneura elegantula ; Homoptera: Cicadellidae) in California vineyards, yet must overwinter in habitats external to these vineyards. Existing evidence suggests that French prune trees, which harbour the overwintering host Edwardsiana prunicola , planted adjacent to vineyards may enhance early-season abundance of Anagrus.
2. Anagrus overwintering in French prune tree refuges were labelled with the trace element rubidium in four separate experiments. Rubidium-labelled Anagrus were captured in adjacent vineyards in two of the experiments, confirming that French prune trees contribute to early-season Anagrus populations. Anagrus from refuges were captured at the most distant sampling positions, 100 m from refuges.
3. Use of rare element labelling has, for the first time, enabled the relative contribution of different sources to early-season colonization by this parasitoid to be quantified. Refuges contributed 1% and 34% of Anagrus colonizing two of the experimental vineyards, respectively. The remainder originated from overwintering habitats external to the French prune/vineyard system.
4. The spatial patterns of Anagrus originating from external overwintering habitats suggest that the French prune trees are generating a 'windbreak effect'. Anagrus dispersing within the windstream colonized vineyards at a higher-than-average rate immediately downwind of refuges.
5. The amount of colonization by Anagrus from external overwintering habitats was apparently related to the distance to presumed overwintering habitats. These findings demonstrate that both the number of natural enemies emerging from a refuge and the composition of the surrounding landscape are important in determining the impact of local, small-scale habitat manipulations.