Growth, development and consumption by four syrphid species associated with the lettuce aphid, Nasonovia ribisnigri, in California

The lettuce aphid, Nasonovia ribisnigri Mosley, was accidentally introduced into California from Europe during the late 1990s and soon became an economic pest of Romaine lettuce along California’s central coast region. Indigenous syrphid larvae attack the lettuce aphid and are believed to be effective in the management of this invasive pest, although there have been no studies on the capacity of the syrphid larvae to kill and consume lettuce aphids. We focused on four syrphid species commonly found in central coast lettuce fields: Allograpta obliqua (Say), Eupeodes fumipennis (Thomson), Sphaerophoria sulphuripes (Thomson), and Toxomerus marginatus (Say). Laboratory feeding experiments were conducted to estimate the development times of all juvenile stages, the daily growth rate of larvae, the number of third instar aphids killed, the aphid biomass killed, and the aphid biomass consumed as measures of predator performance. Results show that during larval development E. fumipennis killed the most third-instar aphids (507 aphids, 88 mg biomass killed) and reached the largest size, followed by A. obliqua (228 aphids, 39 mg killed), S. sulphuripes (194 aphids, 31 mg killed) and T. marginatus (132 aphids, 20 mg killed). Body size alone did not account for species differences in per-capita larval consumption rates. This information is discussed in relation to the predation potential of syrphids through the short cropping cycle of lettuce, and the choice of plant species to use for floral resource provisioning to enhance the activity of syrphids needed for effective management of lettuce aphids in California’s central coast fields.     

Role of syrphid larvae and other predators in suppressing aphid infestations in organic lettuce on California's Central Coast

Organic lettuce, Lactuca sativa L., growers on the Central Coast of California rely on conservation biological control to manage Nasonovia ribisnigri Mosley (Hemiptera: Aphididae) and other aphid pests of lettuce. In 2006, we carried out five replicated field trials to determine the importance of syrphid larvae in the suppression of N. ribisnigri and other aphids infesting organic romaine lettuce. We used Entrust, a spinosad-based insecticide approved for use on organic farms, to suppress syrphid larvae in aphid-infested romaine. Romaine treated with Entrust was unmarketable at harvest because of aphid infestation, whereas insecticide-free romaine was marketable. Syrphid larvae composed 85% or more of total predators in most trials, and they were the only predators consistently recovered from romaine that was infested with aphids early and largely aphid-free by harvest. The species mix of nonsyrphid predators varied from site to site. Applications of Entrust suppressed nonsyrphid predators in two trials, and so was an imperfect tool for selectively suppressing syrphid larvae. The relative importance of syrphid larvae and other predators in the conservation biological control of aphids in organic romaine is discussed. We conclude that syrphid larvae are primarily responsible for the suppression of aphids in organic romaine on California's Central Coast.     

东北大豆生态区捕食性食蚜蝇种类及其对大豆蚜的控害效应分析

食蚜蝇是蚜虫的主要天敌之一。通过对东北大豆生态区捕食性食蚜蝇的种类和种群数量调查,共发现9属15种捕食性食蚜蝇,其中,黑带食蚜蝇Episyrphus balteatus(De Geer)、大灰食蚜蝇Eupeodes corollae(Fabricius)、印度细腹食蚜蝇Sphaerophoria indiana(Bigot)和宽尾细腹食蚜蝇Sphaerophoria rueppelli(Wiedemann)为田间常见种;黑带食蚜蝇是大豆整个生长过程中的主要优势种,大灰食蚜蝇是大豆生长前期的优势种,细腹食蚜蝇是大豆生长中后期的优势种群;食蚜蝇幼虫发生高峰期与大豆蚜发生高峰期基本吻合。通过捕食量测定,发现黑带食蚜蝇平均每头幼虫对大豆蚜的理论最大捕食量为984头;在田间益害比为1∶150时,控害效果达到最大,近60%;而在1:250时单头控制蚜量最多,为102头,且控害效果可达到40%以上。以上研究结果表明,食蚜蝇对大豆蚜具有较强的捕食能力,具有很大的生防应用潜能。本文还提出了关于食蚜蝇田间保护的可行性措施。     

Syrphid flies suppress lettuce aphids

Syrphid flies are abundant in lettuce fields, where their larvae are key predators of aphids. However, the presence of predators in the field does not always result in economically significant levels of prey suppression. Even when predators are numerous, their effects on prey population dynamics may be variable. Over a two year period we surveyed lettuce fields in coastal California, USA to test whether syrphid flies are capable of colonizing fields with aphids and suppressing aphid population growth. The survey showed that female syrphids oviposited more eggs at locations with more aphids, and that greater numbers of syrphid larvae resulted in lower rates of increase in the aphid populations. We also directly manipulated syrphid densities by adding syrphid eggs to uncaged lettuce plants, and these syrphid additions resulted in lower aphid population growth. This research shows that syrphid flies have the ability to suppress aphid populations in lettuce fields.     

Fenologia y seleccion de habitat de las especies de sirfidos afidofagos (Dipt.: Syrphidae) mas frecuentes en cultivos cerealeros y forrajeros en la provincia de buenos aires,argentina

Phenology and habitat selection of the aphidophagous syrphid species most frequently found in crops and pastures in the Province of Buenos Aires, Argentina. The paucity in ecological studies on aphidophagous syrphid flies (Diptera, Syrphidae) of the neotropical region is particularly pronounced in Argentina. In order to increase the database on these natural enemies, the phenology and habitat selection of six syrphid flies (Dipt., Syrphidae):Syrphus phaeostigma (L.);Allograpta obliqua (Wied.);Allograpta exotica (Wied.);Pseudodorus clavatus (L.);Platycheirus carposcalis (L.) andOcyptamus argentinensis (Thorn.) were studied in the Province of Buenos Aires (Argentina). The moment of the year in which adults, eggs, larvae and pupae of these species are found was recorded. The phenologies found for the species in our area are similar to those found for other species of the same genera in other parts of the world. These aphidophagous syrphids are not evenly distributed in all the systems sampled, evidencing a preference for either one of the following types of habitat: cereal crop, lucerne, soya, bushes or prairies. These results are potentially useful in terms of crop and pest management practices.

     

Hoverfly (syrphidae) communities respond to varying structural retention after harvesting in canadian peatland black spruce forests

Variable retention harvesting (VRH), in which trees are removed at variable intensity and spatial configuration across the landscape, retains greater forest structural heterogeneity than traditional clear-cut harvesting and is being recommended as an alternative for sustainable management of the boreal forest. Little is known about its effects on forest fauna; thus, we studied the influence of one type of VRH (harvesting with advanced regeneration [HARP]) on the Syrphidae (Diptera) community in northern Ontario forests of peatland black spruce (Picea mariana). We examined the effects of varying structural retention (from unharvested through partial retention to clear-cut) on syrphid species richness and abundance, and abundance of functional assemblages. Greater species richness and population abundances were found generally in harvested than in unharvested forests. Overall species richness and the abundance of four species (Platycheirus rosarum, Toxomerus marginatus, Xylota annulifera, and X. tuberculata) and larval predators were all higher in both clear-cut sites and those with structural retention than in unharvested sites. Similarly, overall species richness and the abundance of nine species were higher in clear-cut than in unharvested sites. Species responses are discussed in an ecological context. Differences among the levels of forest retention harvesting were relatively minor compared with those of the clear-cut and unharvested area, suggesting that local habitat characteristics may play a more important role in determining the syrphid community than the landscape configuration. However, a landscape level effect was evident, suggesting that syrphids may be useful in reflecting changes in stand structure at the landscape scale.     

Feeding preferences of the aphidophagous hoverfly Sphaerophoria rueppellii affect the performance of its offspring

Provision of additional floral resources in the crop is a successful strategy of conservation biological control for attracting several natural enemies including predatory syrphids. However, the selection of flower species is mainly based on visiting preferences, paying little attention to the link between preference and performance. In this study, we assess the influence of feeding on flowers of two insectary plants (sweet alyssum and coriander) and flowers of a crop species (sweet pepper) on performance of the parental and first generation of the syrphid Sphaerophoria rueppellii (Wiedemann) (Diptera: Syrphidae). We found that floral preference of the adults was linked to developmental performance of their offspring. Sweet alyssum was the flower most frequently visited by syrphid adults, enhancing adult body size and egg-to adult survival of the F1 generation.     

Feeding and egg distribution studies of Heringia calcarata (Diptera: Syrphidae), a specialized predator of woolly apple aphid (Homoptera: Eriosomatidae) in Virginia apple orchards

Predation by the aphidophagous syrphid fly Heringia calcarata (Loew) on woolly apple aphid, Eriosoma lanigerum (Hausmann), was studied in the laboratory and in Virginia apple orchards. Feeding studies compared the prey suitability of three temporally sympatric aphid pests of apple: spirea aphid, Aphis spiraecola Patch; rosy apple aphid, Dysaphis plantaginea (Passerini); and woolly apple aphid. Significantly more H. calcarata larvae survived and completed development on a pure diet of woolly apple aphid than on rosy apple aphid, and none survived on spirea aphid. Final larval weights were significantly greater, and the larval developmental period was significantly shorter on woolly apple aphid than on rosy apple aphid, but neither the duration of pupal development nor adult weight differed between diets. H. calcarata larvae consumed an average of 105 woolly apple aphids during their development. Na?ve, neonate larvae given access to all possible pair combinations of woolly apple aphid, rosy apple aphid, and spirea aphid consumed significantly more woolly apple aphids in all pairings that included woolly apple aphid. When given a choice of rosy apple aphid and spirea aphid, significantly more rosy apple aphids were consumed. Weekly counts of syrphid eggs found in woolly apple aphid, rosy apple aphid, and spirea aphid colonies collected from apple trees showed that two generalist hover fly predators, Eupeodes americanus (Wiedemann) and Syrphus rectus Osten Sacken, were present in colonies of all three aphid species and that E. americanus was the most abundant syrphid predator in A. spiraecola and D. plantaginea colonies. H. calcarata eggs were found only in woolly apple aphid colonies and were more abundant there than E. americanus and S. rectus. These data suggest that H. calcarata is a specialized predator of woolly apple aphid in the apple ecosystem in Virginia.     

Black-tie dress code: two new species of the genus Toxomerus (Diptera, Syrphidae)

Toxomerus hauseri Mengual sp. n. and Toxomerus picudus Mengual sp. n. are described from Peru and Ecuador respectively. Toxomerus circumcintus (Enderlein, 1938) is treated as a valid species and not considered synonym of Toxomerus marginatus, and Toxomerus ovatus (Hull, 1942) is considered junior synonym of Toxomerus nitidus (Schiner, 1868). An identification key for the Toxomerus species with dark abdomens is given along with diagnoses for each studied species.     

First record of Lipaphis pseudobrassicae Davis (Hemiptera: Aphididae) and its association with predator insects, parasitoids and ants in kale (Cruciferae) in Brazil

This study describes the fauna of predator insects, parasitoids and ants associated with aphids on kale (Brassica oleracea L. var. acephala D.C.) in organic system. The aphid was identified as Lipaphis pseudobrassicae Davis, and this is the first record of the species attacking kale in Brazil. Primary parasitism by Diaeretiella sp. and Aphidius sp. and hyperparasitism by Aphydencyrtus sp., Alloxysta sp., Pachyneuron sp. and Syrphophagus sp. were observed. Twenty species of Coccinellidae were collected, and eight of them were observed in adult and larval stages attacking the aphid: Hyperaspis (Hyperaspis) festiva Mulsant, which was the most abundant (72.5% of all predator insects obtained), Cycloneda sanguinea (L.), Eriopis connexa Germar, Coleomegilla maculata DeGeer, Hippodamia convergens Guérin, Heterodiomus sp., Scymnus (Pullus) sp.1 and Scymnus (Pullus) sp.2. Aphidophagous Syrphidae larvae collected on leaves ofkale infested by L. pseudobrassicae belong to the species Allograpta exotica (Wiedemann) and Ocyptamus gastrostactus (Wiedemann). Larvae and pupae of Syrphidae were parasitized by Pachyneuron sp., Syrphophagus sp. and Diplazon laetatorius Fabricius. Larvae of Chrysopodes sp. were observed feeding on L. pseudobrassicae. Species of ants associated with the colony of this aphid were Ectatomma quadridens Fabricius and Pheidole sp.     

Immature stages of some aphidophagous syrphid flies of India (Insecta, Diptera, Syrphidae)

Immature stages, viz. egg, larva and puparium, of six species of the economically most important syrphid flies, Scaeva latimaculata (Brunetti), Ischiodon scutellaris (Fabricius), Episyrphus altemans (Macquart), Sphaerophoria Indiana Bigot, Metasyrphus confrater (Wiedemann), and M. latilunulatus (Collin), have been studied. These species are voracious feeders on three aphid species, Lipaphis erysimi (Kaltenbach), Myzus persicae (Sulzer) and Brevicoryne brassicae (L.), which are serious pests of mustard, Brassica campestris L.     

Use of selected flowering plants in greenhouses to enhance aphidophagous hoverfly populations (Diptera: Syrphidae)

The addition of floral resources in a crop is the most commonly used conservation biological control strategy. The influence of additional floral resources on the abundance of aphidophagous syrphids has been studied in Mediterranean sweet-pepper greenhouses, in southeast Spain. Sweet alyssum and coriander were the plant species used as flowering plants, distributed in the greenhouse in several monospecific patches. In our first experiment the influence on syrphid pre-imaginal stages (larvae and pupae) was studied and adult stages were studied in a second experiment. A higher number of pre-imaginal syrphids was recorded in two replicated greenhouses where flowers were introduced, compared with two control greenhouses (without additional floral resources). To evaluate the effect on adults, 4 greenhouses were divided into 2 plots in each greenhouse and flowers were introduced in one plot per greenhouse. More hoverfly adults were observed in the plots where flowers had been introduced than in the control. The three most abundant syrphid species found were Eupeodes corollae, Episyrphus balteatus and Sphaerophoria rueppellii. Specimens from these species were dissected, and their pollen content was analysed to assess the food potential of the introduced flowers. The three syrphid species fed on pollen from both the flowering plants, as well as on sweet-pepper pollen. This conservation biological control strategy is an effective method to enhance native syrphid populations in Mediterranean sweet-pepper greenhouses.     

The use of common elder Sambucus nigra to promote Aphidophagous syrphids in apple orchards

Elder shrubs (Sambucus nigra L.) were planted in an experimental apple orchard as bordering hedgerow with the objective of rearing syrphids (Diptera: Syrphidae) and consequently enhancing the biological control of the rosy apple aphid Dysaphis plantaginea (Passerini). The inoculative introduction of the specific elder aphid Aphis sambuci L. (Homoptera: Aphididae) in late March 2002 and again in 2003 led to the complete hedgerow turning into an early and productive alternative prey reservoir for indigenous syrphids. The species Scaeva pyrastri (L.), S. selenetica (Meigen), Syrphus ribesii (L.), S. vitripennis Meigen, Epistrophe eligans (Harris), E. nitidicollis (Meigen), Platycheirus scutatus (Meigen), Eupeodes corollae (F.), Meligramma triangulifera (Zetterstedt) and Episyrphus balteatus (De Geer) developed on the elder hedgerow during the spring 2002 taking advantage of the aphid infestation. The season 2003 was characterised by a quite different species abundance pattern as, contrary to the previous year when both monovoltine and polyvoltine species were equally represented, the monovoltine syrphids (Epistrophe spp.) represented the dominant group exploiting the elder aphids. A parallel analysis showed that the faeces of the first adult syrphids observed ovipositing on the elder hedgerow in spring contained digested pollen of mainly apple. Our observations indicate the possibility of establishing a local population of monovoltine syrphids in apple orchards by managing an aphid-infested elder hedgerow, without any additional pollen or nectar producing plants.     

A fly larva (Syrphidae: Ocyptamus) that preys on adult flies

Predatory syrphid larvae feed on relatively immobile prey, but here we report the first case (as far as we are aware) of obligatory predation on very mobile prey. Larvae of an undescribed species of Ocyptamus (Diptera: Syrphidae) were found in whitefly (Hemiptera: Aleyrodidae) aggregations on the undersides of citrus leaves. However, instead of preying on the whitefly nymphs (as would be expected), the larvae preyed on adult flies (Diptera) that were attracted to the honeydew. In the laboratory, larvae captured significantly more flies on whitefly infested leaves than on washed leaves, and generally abandoned leaves that lacked whiteflies. Most cases of successful prey capture involved flies that probed the anterior part of the larva's body with its proboscis (as if it were honeydew). The syrphid larva lashed out at the fly and entangled it in sticky oral secretion. The prey did not recover when they were removed from the larva, suggesting that this new predatory species also employs venom to subdue its prey. Although the larvae consumed some honeydew, they were unable to complete their development on this diet. Two parasitoids were reared from Ocyptamus puparia, Proaspicera sp. (Hymenoptera: Figitidae) and Paracarotomus sp. (Hymenoptera: Pteromalidae), both of which are endoparasitic koinobionts.     

Parasitoids and hyperparasitoids of Mythimna convecta (Walker) (Lepidoptera: Noctuidae) larvae infesting late-maturing maize in southern New South Wales

Abstract  After several reports of late-maturing maize in Murrumbidgee valley, southern New South Wales, Australia, being severely damaged by armyworm, five crops were surveyed for the presence of larvae in April 2003. Mythimna convecta Walker (Lepidoptera: Noctuidae) was the only species successfully reared from armyworm larvae collected in the field. Ninety-six per cent of armyworm larvae collected were parasitised. Five parasitoid species, Cuphocera sp. nr pilosa (Malloch), Ceromya horma (Malloch), Tritaxys scutellate (Macquart), Chaetophthalmus sp. (Diptera: Tachinidae) and Netelia sp. (Hymenoptera: Ichneumonidae) were reared from M. convecta larvae. Cuphocera sp. nr pilosa was the most frequently encountered parasitoid being reared from 83% of M. convecta larvae collected. Examination of maize plants at each collection site showed high numbers of tachinid puparia adhering to plants. Cuphocera sp. nr pilosa was the only species reared from these puparia. Of the Cu . sp. nr pilosa puparia collected, 23–83% were parasitised by five parasitoid wasps: Trichomalopsis sp. Crawford (Hymenoptera: Pteromalidae), Brachymeria sp. Westwood, Eupelmus sp. Dalman (Hymenoptera: Chalcididae), Perilampus sp. Latreille (Hymenoptera: Perilampidae) and a species belonging to the family Diapriidae.     

Prey capture by the crab spider Misumena calycina (Araneae: Thomisidae)

Summary Crab spiders Misumena calycina (L.) in pasture rose Rosa carolina flowers regularly attacked bumble bees, smaller bees, and syrphid flies that visited these flowers. Attacks reached a maximum rate of over 20/h during mid morning, but only 1.6% of the most important prey item, bumble bees, were captured. The next most important food source, the most frequently taken item, syrphid flies Toxomerus marginatus (Say), were captured in 39% of the attempts. Since these flies have a biomass only 1/60th that of bumble bees, they comprised a much less important food source than did bumble bees. Spiders would obtain over 7% more food by specializing on bumble bees than by attacking all insect visitors, and as much as 20% more food at certain times of the day. However, they did not show a tendency to specialize at any time.     

Larval interactions in aphidophagous predators: effectiveness of wax cover as defence shield of Scymnus larvae against predation from syrphids

Small-sized predators in the aphidophagous guild of Aphis gossypii Glover colonies on hibiscus trees in Japan exploit aphids at low prey abundance. Scymnus (Pullus) posticalis Sicard beetles were the first predatory species to attack aphids in the spring, and their larvae co-occurred with larvae of Eupeodes freguens (Matsumura) syrphids in aphid-infested leaves of hibiscus for 3 weeks in absence of large-sized coccinellid predators. Larval interaction between Scymnus and syrphid predators was examined in relation to effectiveness of wax cover of Scymnus against predation from syrphids. Waxless first instar larvae were not protected but wax-covered larvae of second, third and fourth instars were protected from predation by syrphid larvae. The protection was lower in the second instar which has a thin wax cover and significantly higher in the third and fourth instars having a thick wax cover. In addition, larvae from which the wax was removed were significantly more vulnerable to predation. Vulnerability of Scymnus larvae to predation from syrphids was directly related to the thickness of wax cover. Results suggest that the wax cover of Scymnus larvae act as an effective defence mechanism against predation from syrphid larvae.     

A new genus of oak gallwasps, Zapatella Pujade-Villar & Melika, gen. n., with a description of two new species from the Neotropics (Hymenoptera, Cynipidae, Cynipini)

A new genus of cynipid oak gallwasp, Zapatella Pujade-Villar & Melika, gen. n. (Hymenoptera: Cynipidae: Cynipini), with two new species, Zapatella grahami Pujade-Villar & Melika, sp. n. and Zapatella nievesaldreyi Melika & Pujade-Villar, sp. n., is described from the Neotropics. Zapatella grahami,known only from the sexual generation,induces galls in acorns of Quercus costaricensis and is currently known only from Costa Rica. Zapatella nievesaldreyi, known only from the asexual generation, induces inconspicuous galls in twigs of Quercus humboldtii, and is known only from Colombia. Diagnostic characters for both new species are given in detail. Five Nearctic species are transferred from Callirhytis to Zapatella: Zapatella cryptica (Weld), comb. n., Zapatella herberti (Weld), comb. n., Zapatella oblata (Weld), comb. n., Zapatella quercusmedullae (Ashmead), comb. n.,Zapatella quercusphellos (Osten Sacken), comb. n. (= Zapatella quercussimilis (Bassett), syn. n.). A key based on adults for the species belonging to Zapatella is also given. Generic limits and morphological characteristics of Zapatella and closely related genera are discussed.     

Seasonal abundance of resident parasitoids and predatory flies and corresponding soybean aphid densities, with comments on classical biological control of soybean aphid in the Midwest

Seasonal abundance of resident parasitoids and predatory flies, and corresponding soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), densities were assessed in soybean fields from 2003 to 2006 at two locations in lower Michigan. Six parasitoid and nine predatory fly species were detected in 4 yr by using potted plants infested with soybean aphid placed in soybean fields. The parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) and the predatory flies Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae), and Allograpta obliqua Say (Diptera: Syrphidae) were most numerous. Generally, L. testaceipes was more abundant late in the soybean growing season, but it also occurred during soybean vegetative growth; A. obliqua was more abundant during vegetative growth; and A. aphidimyza was common throughout the season. Soybean plants were visually inspected to estimate densities of soybean aphid, mummified aphids, and immature predatory flies. From 2003 to 2006, parasitism rates were inversely correlated with aphid density: percentage of parasitism was always very low (< or = 0.1%) at high aphid densities (> 100 aphids per plant), and higher parasitism, up to 17%, was observed at very low aphid densities (< 1 aphid per plant). Populations of immature predatory flies, particularly A. aphidimyza, generally increased in soybean fields with increasing soybean aphid populations, but aphids always outnumbered immature flies by 100-21,000-fold when flies were detected. Rearing field-collected aphid in 2006 substantiated that parasitism varied widely, with parasitism in most cases < 10%. Based on findings of low parasitism and predation, positive response to changing aphid densities by predatory flies but not parasitoids, early season abundance primarily of predatory flies, and past findings on these taxa's diversity and abundance, we discuss the potential use of exotic parasitoids and predatory flies to enhance soybean aphid biological control.