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.     

Autumnal emergence of Anagrus wasps,egg parasitoids of Empoasca vitis,from grapevine leaves and their migration towards brambles

• 1 The Anagrus‘atomus’ parasitoid group (Hymenoptera: Mymaridae), associated with Empoasca vitis (Göthe) (Homoptera: Cicadellidae), overwinters on vegetation surrounding vineyards. The emergence of parasitoid adults from grapevine leaves in autumn was studied in north‐eastern Italy, both in relation to the E. vitis egg‐laying period and to the presence of leafhoppers overwintering as eggs on Rubus bushes.
• 2 Autumnal peaks of Anagrus captured using yellow sticky traps were observed first on grapevines and then on brambles. Parasitoid captures in vineyards were observed for more than 1 month after the last first‐instar nymphs of the grape leafhoppers were noticed. Two species belonging to the A. ‘atomus’ group, Anagrus atomus and Anagrus ustulatus, were captured both on grapevines and brambles.
• 3 Parasitoids of the A.‘atomus’ group can emerge from third‐generation grape leafhopper eggs in accordance with two different development time patterns (i.e. normal or delayed). Individuals with delayed emergence required up to 2.2‐fold more time to develop from an egg to adult than individuals with normal emergence. This meant that some parasitoid adults emerged in autumn from eggs of grape leafhopper laid in August.
• 4 A delayed emergence as a result of a slower development ensures that the A.‘atomus’ parasitoid group is synchronized with the egg‐laying of leafhoppers that overwinter as eggs on Rubus spp.
• 5 Consequently, leafhoppers overwintering as eggs on brambles play a key role in the ecology of the relationship between grape leafhoppers and the A.‘atomus’ parasitoid group.

     

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.     

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 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.     

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.     

Host specificity of <Emphasis Type="Italic">Anagrus epos</Emphasis>: a potential biological control agent of <Emphasis Type="Italic">Homalodisca vitripennis</Emphasis>

Anagrus epos Girault (Hymenoptera: Mymaridae) is a candidate for a classical biological control program targeting the glassy-winged sharpshooter (GWSS), Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae), in California. Because mass production of GWSS is expensive and labor-intensive, a factitious host that is more economical to produce is desirable to mass produce A. epos for colonization and augmentation efforts. Here, we report the results of host specificity tests and potential rearing techniques for A. epos under laboratory conditions. Females discriminated and oviposited into eggs of seven cicadellid species: H. vitripennis, Circulifer tenellus (Baker), Erythroneura variabilis Beamer, Amblysellus grex (Oman), Graphocephala atropunctata (Signoret), Macrosteles severini Hamilton, and H. liturata Ball, and two cerambycid species: Phoracantha recurva Newman and P. semipunctata (F.). Anagrus epos successfully completed development in the eggs of H. vitripennis, C. tenellus, E. variabilis, A. grex, G. atropunctata, M. severini, and H. liturata. The use of a factitious host and potential nontarget effects of this generalist parasitoid are discussed.     

Production of Anagrus epos Girault (Hymenoptera: Mymaridae) on Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) eggs

Anagrus epos Girault (Hymenoptera: Mymaridae) is a natural enemy candidate for a classical biological control program targeting the glassy-winged sharpshooter (GWSS), Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae), in California. Little is known about the biology or ecology of A. epos when it utilizes GWSS eggs as a host. Here, we report the results of laboratory studies that describe the host age preference for oviposition, longevity of A. epos adults provided with different food sources, and developmental rates at six different constant temperature regimes. Anagrus epos is a gregarious parasitoid in GWSS eggs with up to 14 adults emerging from each GWSS egg. In choice and no-choice tests for oviposition, A. epos females successfully parasitized all developmental ages of GWSS eggs (1–8 days old). In choice tests, parasitism rates were significantly higher in 1-, 3-, 4-, and 5-day-old GWSS eggs than in 2-, 6-, 7-, and 8-day-old eggs. If provided with honey and water, honey only, water only, or no food or water, A. epos females lived on average 8.2, 4.7, 2.6, and 1.6 days, respectively. Anagrus epos required 294.1 degree-days above a lower temperature threshold of 12.4 °C to develop from egg to adult (eclosion). Our results provide baseline information useful in the development of an efficient parasitoid mass rearing program for A. epos release and evaluation in California.     

Long-distance dispersal by a parasitoid (Anagrus delicatus,Mymaridae) and its host

Summary We demonstrate that an egg parasitoid, Anagrus delicatus (Mymaridae, Hymenoptera) and its host, Prokelesia marginata (Delphacidae, Homoptera) regularly disperse 1 km or more in a north Florida saltmarsh. Anagrus delicatus were caught on yellow sticky traps on offshore islets and oyster bars throughout the spring, summer, and fall, whereas P. marginata were caught during one pulse in the spring. Parasitism rates were higher on offshore islets than at mainland sites, even though egg densities were higher at the mainland sites. The majority of parasitoids caught offshore were females. Long-distance dispersal by A. delicatus may be a cause of inverse density-dependent or density-independent spatial patterns of parasitism and may represent a risk-spreading strategy.     

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.     

On the optimal compromise for a dispersing parasitoid

Vector optimization concepts are used to demonstrate that key characteristics of searching and oviposition by the parasitoid Anagrus delicatus (Mymaridae, Hymenoptera) are consistent with the idea that it forages to achieve an optimal compromise, in an uncertain environment, between maximizing ovipositions at suitable sites and dispersing its eggs as widely as possible.     

The effect of Wolbachia on the lifetime reproductive success of its insect host in the field

Wolbachia is a widespread endosymbiont that induces dramatic manipulations of its host's reproduction. Although there has been substantial progress in the developing theory for Wolbachia–host interactions and in measuring the effects of Wolbachia on host fitness in the laboratory, there is a widely recognized need to quantify the effects of Wolbachia on the host fitness in the field. The wasp Anagrus sophiae, an egg parasitoid of planthoppers, carries a Wolbachia strain that induces parthenogenesis, but its effects on the fitness of its Anagrus host are unknown. We developed a method to estimate the realized lifetime reproductive success of female wasps by collecting them soon after they die naturally in the field, counting the number of eggs remaining in their ovaries and quantifying Wolbachia density in their body. We sampled from a highly infected A. sophiae population and found no evidence for Wolbachia virulence and possible evidence for positive effects of Wolbachia on realized reproductive success.     

Synthetic Herbivore-induced Plant Volatiles Increase Field Captures of Parasitic Wasps

Field evidence for attraction of parasitic wasps from the families Encyrtidae and Mymaridae to grapevines baited with synthetic versions of three herbivore-induced plant volatiles (HIPV) is presented. In a replicated experiment conducted in a juice grape vineyard, sticky cards in blocks baited with controlled-release dispensers of methyl salicylate (MeSA), methyl jasmonate (MeJA) or (Z)-3-hexenyl acetate (HA), trapped significantly greater numbers of Metaphycus sp. (Encyrtidae) than cards in unbaited blocks during May–September. Significantly greater numbers of Anagrus spp. (Mymaridae) were trapped in MeSA and MeJA-baited blocks than in unbaited blocks, during August–September. Greater numbers were recorded in HA-baited blocks in September only. Previous studies showed Encyrtidae and Anagrus spp. were not attracted to sticky cards baited with vials of MeSA, MeJA or HA. Possible reasons for attraction in this study are discussed including the possibility that synthetic, gaseous HIPV from controlled-release dispensers may stimulate plants to produce natural blends of parasitoid-attracting volatiles.     

Cross mating studies among five fruit fly parasitoid populations: potential biological control implications for tephritid pests

The reproductive compatibility between four different species/populations of the tephritid parasitoid Psyttalia (Walker) species from Kenya and individuals of the morphologically identical Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) from a laboratory culture in Italy used in augmentative biological control of olive fly, Bactrocera oleae (Gmelin) (Diptera: Tephritidae) was assessed through cross mating tests using single-pair and group mating methods. Reciprocal crosses among the species resulted in the production of viable offsprings up to the second generation. In spite of the successful production of viable offspring in the laboratory, Psyttalia species are known to have specific host fruit and/or host fly preferences and populations/species may be isolated in one way or the other. However, it is not known whether these populations/species interbreed in the field. We discuss the ability of these parasitoids to interbreed and the potential effects of that on their use as biological control agents, especially in environments where other closely related species are present or in situations where multiple parasitoid introductions are intended.     

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.     

A space-efficient contact toxicity bioassay for minute Hymenoptera, used to test the effects of novel and conventional insecticides on the egg parasitoids Anaphes iole and Trichogramma pretiosum

We developed and tested anovel bioassay method for assessment of contactresidues of pesticides to minute Hymenoptera. This method maintained a plant-toxin-insectinterface representative of natural conditionsin the field or greenhouse, and wasspace-efficient. The procedure was useful instudies with both foliar residues and systemicuptake. Furthermore, the method was relativelystraightforward, easy to setup, andinexpensive. Tests with the egg parasitoidsAnaphes iole Girault (Hymenoptera:Mymaridae) and Trichogramma pretiosumRiley (Hymenoptera: Trichogrammatidae)confirmed that this method provided consistent,repeatable assessment of concentration-responserelationships for several insecticide classes. Other researchers studying pesticide effects onminute Hymenoptera might find this bioassaymethod helpful, especially in situations wherespace is limited. We discovered differentialsusceptibility of these parasitoids tospinosad, thiamethoxam, and oxamyl. The orderof toxicity for A. iole wasspinosad>thiamethoxam>oxamyl, and for T. pretiosum wasthiamethoxam>spinosad>oxamyl. Our resultsunderscored the danger of generalizingpesticide effects across even closely relatedinsects, and demonstrated that novel`selective' insecticides are highly toxic toA. iole and T. pretiosum.     

Close-Range Host Searching Behavior of the Stemborer Parasitoids <Emphasis Type="Italic">Cotesia sesamiae</Emphasis> and <Emphasis Type="Italic">Dentichasmias busseolae</Emphasis>: Influence of a Non-Host Plant <Emphasis Type="Italic">Melinis minutiflora</Emphasis>

Studies were conducted on the host searching behavior of the larval parasitoid Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae) and the pupal parasitoid Dentichasmias busseolae Heinrich (Hymenoptera: Ichneumonidae), both of which attack lepidopteran (Crambidae, Noctuidae) cereal stemborers. The behavior of D. busseolae was observed in a diversified habitat that consisted of stemborer host plants (maize, Zea mays L. and sorghum, Sorghum bicolor (L). Moench (Poaceae)) and a non-host plant (molasses grass, Melinis minutiflora Beauv. (Poaceae)), while C. sesamiae was observed separately on host plants and molasses grass. In previous olfactometer studies, C. sesamiae was attracted to molasses grass volatiles while hboxD. busseolae was repelled. The aim of the present study was to investigate the influence of molasses grass on close-range foraging behavior of the parasitoids in an arena that included infested and uninfested host plants. Dentichasmias busseolae strongly discriminated between host and non-host plants, with female wasps spending most of the time on infested host plants and least time on molasses grass. Likewise, C. sesamiae spent more time on uninfested and infested host plants than it did on molasses grass in single choice bioassays. While on infested plants, the wasps spent more time foraging on the stem, the site of damage, than on other areas of the plant. Overall, the results indicate that presence of the non-host plant does not hinder close range foraging activities of either parasitoid.     

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     

Occurrence and activity of <Emphasis Type="Italic">Bemisia tabaci</Emphasis> parasitoids on cassava in different agro-ecologies in Uganda

Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) is the vector of cassava mosaic geminiviruses that cause cassava mosaic disease (CMD), which in turn causes devastating yield losses. Surveys were conducted from October 2000 to November 2001 in four agro-ecologies in Uganda to enhance the understanding of parasitoid fauna and parasitism of B. tabaci in cassava fields. Such an understanding is an essential prerequisite for the development of biological control methods of B. tabaci to complement current CMD control practices. Parasitoid abundance and parasitism efficiency varied between locations and sampling dates within the locations; highest parasitoid densities were observed at Namulonge in the Lake Victoria crescent while the lowest was at Kalangala. In all locations, parasitism was mainly due to Encarsia sophia Dodd and Girault and Eretmocerus mundus Mercet (all Hymenoptera: Aphelinidae). Two occasionally observed species included Encarsia mineoi Viggiani (Hymenoptera: Aphelinidae), only observed at Namulonge, and blackhead Encarsia (Hymenoptera: Aphelinidae) observed at Bulisa, Namulonge and Lyantonde. Parasitism efficiency was highest at Bulisa (57.9%), but ranged from 40.2 to 46.9% at the other three sites. This paper discusses the possible causes of variations in parasitoid abundance and parasitism efficiency, and proposes further studies that might be carried out to assess the potential for augmentation of parasitoids to control B. tabacipopulations and CMD.