Primer design for identifying economically important Liriomyza species (Diptera: Agromyzidae) by multiplex PCR

Leafminer flies, especially, Liriomyza huidobrensis, Liriomyza sativae and Liriomyza trifolii, are quarantine species in many countries. Their morphological similarity makes identification difficult. To develop a rapid, reliable, sensitive and simple molecular identification method using multiplex PCR, we newly sequenced the mitochondrial cytochrome oxidase I (COI) genes of Liriomyza bryoniae, Liriomyza chinensis, L. huidobrensis, L. sativae, L. trifolii, Chromatomyia horticola and four parasitoid species. We aligned them with all the COI sequences of the leafminer flies found in the international DNA nucleotide sequence databases (DDBJ/EMBL/GenBank). We then designed species‐specific primers to allow us to differentiate between L. bryoniae, L. chinensis, L. huidobrensis, L. sativae, and L. trifolii.     

Effects of host instar and size on parasitization efficiency and life history parameters ofOpius dissitus

The braconid parasitoidOpius dissitus Muesebeck (Hymenoptera, Braconidae) produced 1.7 to 3 times more offspring when provided second and third instar leafminers (Liriomyza sativae Blanchard) as compared to first instars. Females arising from parasitization of different instars did not differ significantly in numbers of chorionated eggs in their ovaries at adult eclosion. Development time was prolonged by about two days when parasitoid oviposition occurred in first, as compared to third instar hosts. Parasitoid length was positively correlated with host weight (r²=0.75). Because only 7% of variation in host weight could be explained by host density, parasitoid length varied considerably among hosts reared at the same density. Longevity and lifetime fecundity of parasitoids were inversely related to the weight of their hosts.     

Parasitic hymenoptera fauna on agromyzidae (diptera) colonizing weeds in ecological compensation areas in northern Italian agroecosystems

Parasitoids (Hymenoptera) associated with agromyzid leafminers (Diptera: Agromyzidae) were studied in three rural farms located in northern Italy. The parasitoids were reared from mined foliage of weeds growing in field margins. We reared 998 Hymenoptera specimens, representing five families, 23 genera, and 53 species, from leafminers infesting weeds. Eulophidae was the most abundant family (67.64%), followed by Braconidae (28.86%), Eucoilinae (1.40%), Tetracampidae (1.40%), and Pteromalidae (0.7%). Braconids was the most species rich family, accounting for 28 species; eulophids were represented by 19 species, pteromalids by four species, and eucoilins and tetracampids by one species each. The dominant parasitoid was the eulophid Pediobius metallicus (Nees), representing 18.17% of the total, followed by Diglyphus isaea (Walker) (12.73%), and Neochrysocharis formosa (Westwood) (10.82%). The most abundant braconid parasitoid was Dacnusa maculipes Thomson (9.62%). More than 80% of parasitoids were recovered from 10 plant species: Cirsium arvense (L.) Scopoli, Plantago lanceolata L., Sonchus asper (L.) Hill, Papaver rhoeas L., Picris echioides L., Lactuca serriola L., Myagrum perfoliatum L., Ranunculus velutinus Tenore, Arctium lappa L., and Medicago sativa L. The retention and the management of wild plants within field margins can be crucial tools to enhance the populations of biological control agents of agromyzids and to conserve rare parasitic wasp species.     

Identifying factors determining the altitudinal distribution of the invasive pest leafminers Liriomyza huidobrensis and Liriomyza sativae

Abiotic and biotic factors that change with altitude can influence the distribution of herbivorous insects. We examined factors influencing the distribution of the generalist leafminers Liriomyza sativae Blanchard and Liriomyza huidobrensis Blanchard (Diptera: Agromyzidae), two pests of agricultural crops, in the tropical Dieng mountainous area of Central Java, Indonesia. Liriomyza huidobrensis predominated at altitudes above 700 m a.s.l. and was the only species collected above 1 400 m a.s.l. In contrast, L. sativae predominated below 600 m a.s.l. and was not found above 1 200 m where the average temperature was 20.7 °C. Parasitoid diversity decreased with altitude, but parasitism did not change. The distribution of neither species was affected by parasitoids; L. huidobrensis predominant at high altitudes was preferred by Opius parasitoids common at these altitudes. Intra‐ and interspecific competition was detected in laboratory experiments where larval density was high, but led to coexistence rather than species displacement. No competition was detected in a field experiment when larval density was low. However, L. sativae failed to reproduce at the highest altitude, whereas L. huidobrensis established at all altitudes. Host composition varied with altitude and one host (faba beans) preferred by L. huidobrensis was common at high altitudes. By relating published data on the performance of the leafminer species to altitudinal temperature changes, we were partly successful in predicting the altitude at which the dominant species switched. Temperature plays an overriding influence on the altitudinal distribution of leafminers.     

Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest

Quantitative food webs were constructed to explore the community structure of leaf-mining moths in the family Gracillariidae and their parasitoid wasps in a deciduous forest in Hokkaido, Japan. A whole food web was constructed from data collected from June to October 2001. In the web, 16 leafminer species on seven tree species were attacked by 58 species of hymenopteran parasitoid; 376 links between leafminers and parasitoids were observed. Leafminers were specialist herbivores, but most parasitoids were generalists. Five webs were constructed for the seasonal prevalence of leafminers over the one-year period to reveal the temporal dynamics in community structure. Among the seasonal webs, the first web in June was distinctive because two tree species, Japanese umbrella tree Magnolia obovata and Japanese magnolia M. kobus, supported the community. Second to fourth webs from July to September were dominated by the leafminer species on Japanese oak Quercus crispula, and the fifth web was marked by that on Carpinus cordata. The extent of potential apparent competition among leafminers was evaluated using quantitative parasitoid overlap diagrams. These diagrams suggested that abundant host species are likely to have large indirect effects on less abundant species. Moreover, the potential for apparent competition between leafminer species inhabiting different host tree species can occur, although leafminers sharing the same tree species are prone to interact via shared parasitoids. In this system, particular leafminer species, acting as potential sources of apparent competition, can affect other species as sinks, and control whole-community dynamics. Directed apparent competition may potentially occur around oak trees.     

Comparison of the suitability of Liriomyza chinensis and L. trifolii (Diptera: Agromyzidae) as hosts for Neochrysocharis okazakii (Hymenoptera: Eulophidae)

Effective parasitoid production or mass-rearing is one of the key components in practicing biological control with parasitoids. Selection of host species for rearing parasitoids is a major approach to improve the production efficiency. The stone leek leafminer Liriomyza chinensis (Kato) is a destructive pest of onion crops in many Asian countries, which is difficult to control with chemicals. The present study examined whether the production of Neochrysocharis okazakii Kamijo, a promising native biological agent of L. chinensis, could be effective if kidney bean-Liriomyza trifolii (Burgess) system was used as an alternative rearing procedure. The suitability of L. chinensis and L. trifolii as hosts of N. okazakii was investigated in the laboratory. Neochrysocharis okazakii completed its development on both two host species, and the total development time was similar on these hosts. Longevity of N. okazakii females provided with L. chinensis was longer than those on L. trifolii. There were no significant differences in fecundity and offspring sex ratio when females had been provided with these two host species. The adult parasitoids emerged from L. chinensis were significantly larger than those from L. trifolii. However, the intrinsic rate of increase was higher, and mean generation time was lower, for L. trifolii than L. chinensis. Thus, mean net reproductive rate (Ro) was higher when L. trifolii was used as host. Although the two host species were equally suitable as host for N. okazakii, our findings suggested that L. trifolii and kidney bean is an ideal system for N. okazakii production.     

Displacement in two invasive species of leafminer fly in different localities

Liriomyza sativae was displaced by L. trifolii in the USA probably due to the lower insecticide susceptibility of L. trifolii, but L. trifolii was displaced by L. sativae in Japan. To know the possible causes of the species displacement observed in Japan, differences in the insecticide susceptibility, fecundity, effects of natural enemies, and reproductive interference between L. trifolii and L. sativae were evaluated. As a result, the higher fecundity of L. sativae and differential effects of parasitoids on the two Liriomyza species are considered to be contributing factors.     

甘肃白银地区潜叶蝇及其寄生蜂的组成和发生调查

【目的】明确严重危害甘肃省白银地区作物的潜叶蝇及天敌寄生蜂的多样性和种群组成。【方法】采用五点取样法田间调查潜叶蝇危害的蔬菜、花卉、杂草并采样,室内对潜叶蝇及其寄生蜂进行形态鉴定和分子鉴定。【结果】在2016-2020年在甘肃白银地区采集的样本中发现6种常见潜叶蝇,包括本地种豌豆彩潜蝇Chromatomyia horticola和葱斑潜蝇Liriomyza chinensis,入侵种南美斑潜蝇L. huidobrensis、三叶草斑潜蝇L. trifolii、番茄斑潜蝇L. bryoniae和美洲斑潜蝇L. sativae。其中,豌豆彩潜蝇为优势种,可危害多科寄主植物;葱斑潜蝇仅在大葱上发现危害;南美斑潜蝇在温室内的蔬菜上发生严重;三叶草斑潜蝇首次在白银市发现;番茄斑潜蝇与美洲斑潜蝇的危害相对较轻。此外,调查的潜叶蝇寄生蜂包括3科12属24种,优势种包括豌豆潜蝇姬小蜂Diglyphus isaea、芙新姬小蜂Neochrysocharis formosa、万氏潜蝇姬小蜂D. wani和西伯利亚离颚茧蜂Dacnusa sibirica。【结论】一方面白银市应加强监测和预警入侵性潜叶蝇的发生,另一方面白银市潜叶蝇的天敌寄生蜂种类丰富,对田间主要危害的潜叶蝇可能发挥着重要的自然防控作用,建议保护利用本地寄生蜂天敌。     

Adult experience modifies attraction of the leafminer parasitoidOpius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals

Oviposition-experienced females of Opius dissitus Muesebeck, a braconid parasitoid of Liriomyza sativaeBlanchard, preferentially landed on leafminer-infested rather than uninfested lima bean (Phaseolus lunatus L.) plants in a flight tunnel assay. Both naive and oviposition-experiencedparasitoids responded strongly to odors of infested lima bean plants in a four-arm olfactometer in comparison with odors of uninfested plants, suggesting that volatile semiochemicals are used in host location. Parasitoids with an oviposition experience on lima bean (lima-experienced) spent significantly more time in the infested odor than naive individuals, however, eggplant-experienced wasps did not spend significantly more time in the infested odor field than naive wasps. When parasitoids reared on leafminers in lima bean were provided a choice between the odor of infested lima bean and the odor of infested eggplant or cotton, naive and lima-experienced wasps preferred infested lima odor. An oviposition experience on the other plant species resulted in a dramatic shift in preference. It was concluded that the experience effect was due, at least in part, to associative learning, as has been reported for other parasitoids. The parasitoids may perceive unconditioned stimuli during host contact and oviposition on an infested leaf and may associate those stimuli with volatile semiochemicals emanating from the leaf or host. Subsequently, the volatiles associated with the presence of hosts are used in directing the search for hosts.     

Species diversity of lepidopteran stem borer parasitoids in cultivated and natural habitats in Kenya

Field surveys were conducted during 2005 to 2007 to assess the species diversity of stem borer parasitoids in cultivated and natural habitats in four agroecological zones in Kenya. In total, 33 parasitoid species were recovered, of which 18 parasitized six stem borer species feeding on cereal crops, while 27 parasitized 21 stem borer species feeding on 19 wild host plant species. The most common parasitoids in cultivated habitats were Cotesia flavipes Cameron, Cotesia sesamiae (Cameron), Pediobius furvus Gahan and the tachinid Siphona sp., whereas in natural habitats, Siphona sp. was the most common. The majority of parasitoids were stenophagous species; only five species –Cotesia sp., Enicospilus ruscus Gauld and Mitchell, Pristomerus nr. bullis, Sturmiopsis parasitica (Curran) and Syzeuctus ruberrimus Benoit – were monophagous. In both cultivated and natural habitats, parasitoid species diversity was highest on the most dominant stem borers Busseola spp. and Chilo spp. On cereal crops, parasitoid diversity was highest on maize and among wild host plants, it was highest on Setaria spp. The ingress‐and‐sting attack method was the most common strategy used by parasitoids in both habitats. In all agroecological zones, parasitoid species diversity was significantly higher in natural than in cultivated habitats. Furthermore, the majority of parasitoid species were common to both cultivated and natural habitats. It was concluded that natural habitats surrounding cereal crops serve as refugia for sustaining the diversity of stem borer parasitoids from adjacent cereal fields.     

Effects of selected insecticides on adults of two parasitoid species of Liriomyza trifolii: Ganaspidium nigrimanus (Figitidae) and Neochrysocharis formosa (Eulophidae)

Abstract Liriomyza trifolii is an important pest of vegetables and ornamental crops around the world. This pest is attacked by many parasitoid species. The principal management tactic used against L. trifolii is insecticide application. Insecticides vary in their effects on parasitoid species and insecticides that have less harmful effects should be preferred for the control of this pest. In this study, novaluron, abamectin, λ‐cyhalothrin and spinetoram were investigated for their lethal effects on adults of Neochrysocharis formosa and Ganaspidium nigrimanus, two important parasitoids of L. trifolii. Three different bioassays were used on adult parasitoids: direct insecticide application, insecticide intake and insecticide residue. Adult parasitoid response to novaluron exhibited the least lethal effects among the bioassays and insecticides tested. Abamectin had significant mortality to both parasitoid species in the direct application and insecticide intake bioassays and mortality were high for G. nigrimanus in the residue bioassay. Spinetoram was the most harmful insecticide to the adult parasitoids in all three bioassays. λ‐cyhalothrin effects varied between the two parasitoids. In the direct application, it was harmful to G. nigrimanus and had no effect on N. formosa. In the insecticide intake bioassay λ‐cyhalothrin had no effect in survival of either species, and in the residue bioassay it reduced parasitoid survival of both species. Potential tolerance of N. formosa to λ‐cyhalothrin is discussed.     

Parasitoid assemblages reared from geometrid defoliators (lepidoptera: geometridae) of larch and fir in the alps

1 Geometrid larvae were collected from larch and fir in the Swiss Alps in 1991–94. Eight geometrid species were found in sufficient numbers to rear out parasitoids: Agriopis aurantiaria, Bupalus piniarius, Epirrita autumnata, Eupithecia lariciata, Odontopera bidentata, Lycia isabellae and Semiothisa liturata were collected from larch, and Puengeleria capreolaria was obtained from fir. 2 Parasitoid species belonging to five different guilds and four families were obtained; however, the taxonomic status of some of these is not completely resolved. 3 The parasitoid complex of the larch‐feeding species was totally different from that of Tortricidae and Tenthredinidae, which feed on the same host tree. In general, there was little overlap in the parasitoid complexes of the larch geometrids, with the most dominant parasitoid of each species reared from only one host. By contrast, many parasitoid species found during our study are also known to attack the same hosts or closely related hosts on different host tree species in different environments, suggesting that host specificity in geometrid parasitoids is more related to host taxonomy than to host plant or habitat.     

Intraspecific size variation in polyphagous parasitoids (Hym.: Parasitica), of leaf miners and its relation to host size

Wing and body lengths of polyphagous parasitoids of leafminers are analyzed in order to understand the relationship between host and parasitoid sizes. A distinct positive relationship was observed: within each parasitoid species, smaller individuals were reared from smaller hosts. There was no difference between idio-and koinobionts in sexual dimorphism, with females being significantly larger than males in both groups.     

Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae)

Determining the impact of genetically modified (GM) crops on beneficial organisms is an important aspect of the environmental risk assessment of GM crops. In the present study, the impact of Bt maize expressing Cry1Ab on the development and behaviour of the parasitoid Campoletis sonorensis was compared to individuals reared on hosts fed conventionally bred plants partially resistant to the European corn borer (Ostrinia nubilalis Hübner) and on susceptible maize hybrids. Adult parasitoids reared on Bt maize-fed Spodoptera frugiperda larvae were significantly smaller (15–30%) than those reared in hosts fed either of the conventional maize hybrids. The magnitude of this effect was dependent on the size of the host at oviposition and its subsequent growth rate. The development time of C. sonorensis was not affected by the maize treatment. In choice tests, female parasitoids displayed no preference for hosts fed a specific maize hybrid. No Cry1Ab was detected within adult parasitoids.     

Species composition and population dynamics of leafmining flies and their parasitoids in Victoria

Abstract  Mined leaves were sampled from unsprayed sites in Victoria to record the range of leafminers and their parasitoids. Three agromyzid leafminers, Liriomyza brassicae (Riley), Liriomyza chenopodii (Watt) and Chromatomyia syngenesiae Hardy, and one drosophilid leafminer, Scaptomyza flava (Fallén), were collected, along with 15 parasitoids, mainly Eulophidae. The most common parasitoids were Hemiptarsenus varicornis (Girault) (42.5%), Diglyphus isaea (Walker), 14.6%, Closterocerus mirabilis Edwards & La Salle (10.5%), and Opius cinerariae Fisher (8.5%). Most parasitoids were collected from two or more leafminer hosts. Weekly collections from Chinese cabbage ( Brassica rapa var. pekinensis ) infested with L. brassicae and S. flava , and beetroot ( Beta vulgaris var. crassa ) infested with L. chenopodii were made over two seasons at Knoxfield, Victoria to assess the relative impact of these parasitoids on agromyzid fly populations in crops. A further two parasitoid species were identified at low densities. Hemiptarsenus varicornis and D. isaea were the most numerous parasitoids collected in both crops. A different sampling method in the second year showed that O. cinerariae made up 25% of the sample from Chinese cabbage and was probably more common than estimated in the first season. Control exerted by local parasitoids was high, with 100% control of L. chenopodii reached in beets within 1–3 weeks of mines appearing and 100% control of L. brassicae within 6 weeks.     

The interaction between host and host plant influences the oviposition and performance of a generalist ectoparasitoid

The successful development of parasitoids of herbivores depends on the quality of their host, which is often affected by the host plant. Therefore, a parasitoid’s oviposition decisions will directly depend on the host, but also on plant quality. Here, we investigated the direct effects of host species and the indirect effects of the host’s food plant on the oviposition decisions and performance of the gregarious ectoparasitoid Euplectrus platyhypenae Howard (Hymenoptera: Eulophidae). With a series of no‐choice experiments, we determined the oviposition and performance of the parasitoid on: (1) two caterpillar species, fall armyworm, Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae), and velvet armyworm, Spodoptera latifascia Walker, reared on maize (Zea mays L., Poaceae), (2) the same caterpillars reared on maize, bean (Phaseolus vulgaris L., Fabaceae), or squash (Cucurbita pepo L., Cucurbitaceae) leaves, and (3) S. latifascia caterpillars reared on leaves of wild and cultivated lima bean, Phaseolus lunatus L. All these insects and plants originate from Mesoamerica where they have coexisted for thousands of years in the traditional agricultural system known as Milpa in which maize, beans, and squash are planted together. We found that the preferred and best combination of host and host plant for parasitoid performance was S. frugiperda on maize. Parasitoids laid larger clutches, had higher survival, and more females and larger adults emerged from S. frugiperda reared on maize. However, when both caterpillar species were reared on squash, S. latifascia was the better host. Contrary to the literature, S. frugiperda was not able to develop on bean plants. Results from the lima bean experiment showed that parasitoid performance was best when S. latifascia was reared on leaves of cultivated compared to wild lima bean. These findings are discussed in the context of mixed cropping in which the ability of generalist parasitoids to switch among hosts and host plant species could be advantageous for pest management.     

Parasitoid complexes (Hymenoptera,Eulophidae) of leafminers of the genus <Emphasis Type="Italic">Phyllonorycter</Emphasis> (Lepidoptera,Gracillariidae) in the Middle Volga Basin

The parasitoid complexes of 22 species of the genus Phyllonorycter reared from 20 host plants were studied in the Middle Volga Basin. From a total of 124 host-parasitoid associations analyzed, 88 had been previously unknown. Minotetrastichus frontalis, Sympiesis sericeicornis, Pnigalio soemius, Closterocerus formosus, and S. gordius were the most frequent species. The highest percentage of parasitoids reared was observed in Ph. ulmifoliella (58.6%) and Ph. sylvella (54%), and the lowest one, in Ph. salictella (15%). Ph. corylifoliella (95.7%), Ph. populifoiella (95.5%) and Ph. insignitella (95.5%) had the highest mortality due to parasitoids. The number of endoparasitoid species prevailed over that of ectoparasitoids in the parasitoid complexes of the genus Phyllonorycter, but the number of individuals reared was 4 times greater for ectoparasitoids. The parasitoid complexes were the most similar in Ph. harrisella and Ph. quercifoliella on Quercus robur. The gregarious ectoparasitoid M. frontalis predominated over parasitoids of Phyllonorycter.     

Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer

Host plant nutritional quality can directly and indirectly affect the third trophic levels. The aphid–parasitoid relationship provides an ideal system to investigate tritrophic interactions (as the parasitoids are completely dependent for their development upon their hosts) and assess the bottom up forces operating at different concentrations of nitrogen applications. The effects of varying nitrogen fertilizer on the performance of Aphidius colemani (V.) reared on Sitobion avenae (F.) and Aphidius rhopalosiphi (D.) reared on Rhopalosiphum padi (L.) were measured. Parasitism and percent emergence of parasitoids were positively affected by nitrogen fertilizer treatments while developmental duration (egg, larval, and pupal stages) was not affected by increasing nitrogen inputs. In males and females of both parasitoid species, adult longevity increased with the increasing nitrogen fertilizer. Hind tibia length and mummy weight of both parasitoid species increased with nitrogen fertilizer concentrations, as a result of larger aphids. This study showed that nitrogen application to the soil can have important consequences for aboveground multitrophic interactions.     

Suitability of the maize weevil and angoumois grain moth as hosts for the parasitoidsAnisopteromalus calandrae andPteromalus cerealellae

Two parasitoids,Pteromalus cerealellae (Ashmead) andAnisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), were compared for their ability to parasitize two important internally-developing insect pests of stored maize (Zea mays L.). Parasitism byP. cerealellae was greater on Angoumois grain moth,Sitotroga cerealella (Olivier), than on maize weevil,Sitophilus zeamais Motschulsky, in no-choice experiments.Anisopteromalus calandrae parasitized more maize weevils than didP. cerealellae. The former parasitoid parasitized only a few Angoumois grain moths successfully in maize, but parasitized many in wheat if the hosts were younger than 3 weeks old. Thus, both host age and type of grain affect suitability for parasitism. The effects of parental host (species on which the female developed) and experimental host (species exposed to parasitism) on parasitism rate ofP. cerealellae were tested in a host-switching experiment. Parasitism by parasitoids reared on maize weevils was 23% lower than that of parasitoids reared on Angoumois grain moth. This effect was independent of which host the filial generation of parasitoids was tested on. However, the experimental host species had a much greater effect on parasitoid fecundity than the parental host species. Female progeny had smaller body sizes when emerging from maize weevil than from Angoumois grain moth, which may explain the parental host effect on fecundity. There was also a slight intergenerational effect of host species on parasitoid body size.