Chemical Ecology of the host searching behavior in an Egg Parasitoid: are Common Chemical Cues exploited to locate hosts in Taxonomically Distant Plant Species?

Parasitoids are known to exploit volatile cues emitted by plants after herbivore attack to locate their hosts. Feeding and oviposition of a polyphagous herbivore can induce the emission of odor blends that differ among distant plant species, and parasitoids have evolved an incredible ability to discriminate them and locate their hosts relying on olfactive cues. We evaluated the host searching behavior of the egg parasitoid Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) in response to odors emitted by two taxonomically distant host plants, citrus and Johnson grass, after infestation by the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae), vector of Citrus Variegated Chlorosis. Olfactory response of female parasitoids toward plants with no herbivore damage and plants with feeding damage, oviposition damage, and parasitized eggs was tested in a Y-tube olfactometer. In addition, volatiles released by the two host plant species constitutively and under herbivore attack were characterized. Females of C. annulicornis were able to detect and significantly preferred plants with host eggs, irrespectively of plant species. However, wasps were unable to discriminate between plants with healthy eggs and those with eggs previously parasitized by conspecifics. Analysis of plant volatiles induced after sharpshooter attack showed only two common volatiles between the two plant species, indole and ß-caryophyllene. Our results suggest that this parasitoid wasp uses common chemical cues released by many different plants after herbivory at long range and, once on the plant, other more specific chemical cues could trigger the final decision to oviposit.

Ovigeny strategy of the parasitic wasp Cosmocomoidea annulicornis (Hymenoptera: Mymaridae): effect of female age, feeding and host availability on reproductive traits.

The reproductive traits of the mymarid wasp Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) attacking eggs of the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae) were evaluated under laboratory conditions. Bioassays were carried out to estimate the realized fecundity and egg load of females. The ovigeny index was calculated and different biological traits, such as body size, oöcyte length, gaster length and wing length, were analysed to assess significant associations between these traits and the species fitness. In addition, the effect of host availability and feeding on longevity and potential fecundity throughout life and the effect of female age on egg maturation dynamics were assessed. The results showed that C. annulicornis is a strongly synovigenic species. A positive correlation was found between fecundity and longevity of the females and between body size and oöcyte length. Contrary to expected, body size was not related to fecundity and longevity. Females lived significantly longer in the presence of hosts and honey than when they were host-deprived and honey-fed or both host and honey deprived. Host availability had a significant effect on the amount of eggs laid by C. annulicornis females. Female age was negatively associated with oöcyte length. Furthermore, females were able to mature additional eggs as they aged, nevertheless, when host-deprived, senescent females presented significantly less mature eggs than younger ones, suggesting a possible egg oosorption. These results might contribute to a better understanding of the reproductive potential of this species as a biocontrol agent.

Information from the mitochondrial genomes of two egg parasitoids, Gonatocerus sp. and Telenomus sp., reveals a controversial phylogenetic relationship between Mymaridae and Scelionidae.

The taxonomic status and phylogenetic affinities of Mymaridae and Scelionidae are controversial, based on similarities between these families in the characteristics of adults, larvae, and eggs. In this study, we sequenced the mitochondrial (mt) genomes of representatives from these two families and found that the derived secondary structure of tRNA-Arg was the same in each family due to the absence of the D-stem. The segment of "cox1 trnL2cox2 trnK trnD atp8 atp6 cox3" in Gonatocerus sp. (Mymaridae) is conserved and distinct from those of four other species of Chalcidoidea but similar to that in Proctotrupoidea and Platygastroidea. However, phylogenetic analysis indicated that Gonatocerus sp. was sister group to other species of Chalcidoidea. Comparisons based on complete gene orders may be more useful in a phylogenetic and systematic context, as different branches may exhibit partially homoplastic gene orders.

Morphological and Molecular Identification of Anagrus 'atomus' Group (Hymenoptera: Mymaridae) Individuals from Different Geographic Areas and Plant Hosts in Europe.

Morphological identification and molecular study on the COI gene were simultaneously conducted on Anagrus Haliday 'atomus' group individuals collected in the field in Italy or supplied from a UK biofactory. Females were morphologically identified as A. atomus L. and A. parvus Soyka sensu Viggiani (=A. ustulatus sensu Chiappini). Alignment of COI gene sequences from this study permitted recognition of a total of 34 haplotypes. Phylogenetic and network analyses of molecular data not only confirmed that A. atomus is a species distinct from A. parvus, but also suggested that two species may be included within morphologically identified A. parvus. Different geographical distribution and frequency of haplotypes were also evidenced. For males considered in this study, morphometric analyses revealed a character that could be useful to discriminate A. atomus from A. parvus Both species were found in vineyards and surrounding vegetation, confirming the potential role of spontaneous vegetation as a source of parasitoids for leafhopper control in vineyards.

Anagrus avalae Soyka, 1956, a new synonym of A. bakkendorfi Soyka, 1946 (Hymenoptera: Mymaridae).

Soyka (1946) described the European fairyfly species Anagrus bakkendorfi Soyka (Hymenoptera: Mymaridae) from a single female collected on the same day, 7.x.1931, together with several non-type specimens incorrectly labeled as paratypes (Chiappini Triapitsyn 1999), on a window at its type locality, the former St. Ignatius Jesuit College in Valkenburg, Limburg, the Netherlands. Soyka (1956) did not mention type specimens of any of his species of Anagrus Haliday. He described Anagrus avalae Soyka (Soyka 1956) based apparently on a specimen collected on Mt. Avala, Belgrade, Serbia, former Yugoslavia, along with several other nominal species (some also from Valkenburg) that were later synonymized with A. avalae and A. bakkendorfi by Chiappini (1989) and Chiappini Triapitsyn (1999). The only, minor, morphological difference between the two nominal species is the length of the ovipositor in females relative to the length of the protibia, being at least 2.6× in A. bakkendorfi and at most 2.3× in A. avalae (Triapitsyn 2015). Specimens identifiable as both species were captured by the second author in 2000 by a Malaise trap in Iratibizkar, Irati Forest (Selva de Irati), Navarra, Spain. Chiappini Triapitsyn (1999) discussed both nominal species but despite recognizing their apparent conspecificity, no formal synonymy was proposed. Triapitsyn Berezovskiy (2004) and Triapitsyn (2015) also did not propose synonymy because at that time genetic evidence for conspecificity was lacking. However, Triapitsyn et al. (2019) obtained DNA and sequenced selected mitochondrial and nuclear ribosomal gene regions (COI and ITS2) from a specimen unambiguously identified by the first author as A. avalae that was collected in Sevenoaks, Kent County, England, United Kingdom. Because of this we decided to collect fresh specimens identifiable as A. bakkendorfi for molecular analysis and genetic comparison with those identifiable as A. avalae. Based on the previous record (Triapitsyn 2015), several females of A. bakkendorfi were successfully captured by the second author on 4.ix.2020 in Irati Forest, preserved in ethanol, and shipped to the first and third authors for morphological and molecular identification, respectively.

Host Specificity of the Parasitic Wasp Anaphes flavipes (Hymenoptera: Mymaridae) and a New Defence in Its Hosts (Coleoptera: Chrysomelidae: Oulema spp.).

The parasitic wasp Anaphes flavipes (Förster, 1841) (Hymenoptera: Mymaridae) is an important egg parasitoid of cereal leaf beetles. Some species of cereal leaf beetle co-occur in the same localities, but the host specificity of the wasp to these crop pests has not yet been examined in detail. A lack of knowledge of host specificity can have a negative effect on the use of this wasps in biological control programs addressed to specific pest species or genus. In this study, laboratory experiments were conducted to assess the host specificity of A. flavipes for three species of cereal leaf beetles (Oulema duftschmidi Redtenbacher, 1874, Oulema gallaeciana Heyden, 1879 and Oulema melanopus Linnaeus, 1758) in central Europe. For the first time, a new host defence against egg parasitoids occurring in O. gallaeciana from localities in the Czech Republic, a strong dark sticky layer on the egg surface, was found and described. The host specificity of A. flavipes was studied in the locality with the presence of this defence on O. gallaeciana eggs (the dark sticky layer) (Czech Republic) and in a control locality (Germany), where no such host defence was observed. Contrary to the idea that a host defence mechanism can change the host specificity of parasitoids, the wasps from these two localities did not display any differences in that. Respectively, even though it has been observed that eggs with sticky dark layer can prevent parasitization, the overall rate of parasitization of the three species of cereal beetles has not been affected. However, in our view, new host defence can influence the effects of biological control, as eggs of all Oulema spp. in the locality are protected against parasitization from the wasps stuck on the sticky layer of the host eggs of O. gallaeciana.

Molecular, Morphological, and Biological Differentiation between Anagrus virlai sp. n., an Egg Parasitoid of the Corn Leafhopper Dalbulus maidis (Hemiptera: Cicadellidae) in the New World, and Anagrus incarnatus from the Palaearctic Region (Hymenoptera: Mymaridae).

The common New World egg parasitoid of the corn leafhopper Dalbulus maidis (DeLong) (Hemiptera: Cicadellidae), an economically important pest of maize from Argentina to southern USA, has long been misidentified as the Palaearctic species Anagrus incarnatus Haliday or its synonym A. breviphragma Soyka (Hymenoptera: Mymaridae). Using a combination of genetic and morphometric methods, and available biological information, specimens reared from eggs of D. maidis in Argentina and Mexico, described and illustrated here as Anagrus (Anagrus) virlai Triapitsyn sp. n., are shown to be different from those of A. incarnatus from the Palaearctic region. Mitochondrial and nuclear ribosomal DNA sequence data provide clear evidence for the separation of the two species. Anagrus virlai is also known from Brazil, Colombia, Guadeloupe (France), and Guyana.

New records of Chalcidoidea (Hymenoptera) from the Maltese Islands with an updated checklist.

Thirty-three species of Chalcidoidea (Hymenoptera) are newly recorded from the Maltese Islands, of which, 19 include host data. An updated checklist for the 181 chalcidoid species recorded from Malta is also included, which belong to 17 families as follows: Agaonidae (3), Aphelinidae (21, 1 as new record), Azotidae (1), Chalcididae (8 species, 5 as new records), Encyrtidae (24, 1 as new record), Eulophidae (51, 16 are new records), Eupelmidae (9, 2 as new records), Eurytomidae (6, 1 as new record), Leucospidae (4), Megastigmidae (1), Mymaridae (2), Ormyridae (1), Perilampidae (1 new record), Pteromalidae (39, 5 as new records), Signiphoridae (2), Tetracampidae (1) and Torymidae (7, 1 as new record).

Anagrus dmitrievi sp. n. (Hymenoptera, Mymaridae), an egg parasitoid of Zyginidia eremita (Hemiptera, Cicadellidae), a pest of maize in Xinjiang, China.

A new Palaearctic species of Anagrus Haliday (Hymenoptera, Mymaridae), A. (Anagrus) dmitrievi Triapitsyn & Hu, sp. n., is described, diagnosed, and illustrated from Xinjiang Uyghur Autonomous Region of China. It was reared from parasitized eggs of the leafhopper Zyginidia (Zyginidia) eremita Zachvatkin (Hemiptera, Cicadellidae) on leaves of maize. A key to the 21 named species of Anagrus known from China is provided. Zyginidia eremita is an important economic pest in Xinjiang, occurring in approximately 90% of maize fields. The phenology and life cycle of Z. eremita is summarized. Parasitism of its eggs by A. dmitrievi in maize fields was 12-75 % (average about 38 %), thus making it a rather effective natural enemy.

Farm-scale evaluation of the impact of Cry1Ab Bt maize on canopy nontarget arthropods: a 3-year study.

The cultivation of Cry1Ab-expressing genetically modified MON810 (Bt maize) has led to public concern in Europe, regarding its impact on nontarget arthropods (NTAs). We have assessed the potential effects of DKC 6451 YG (MON810) maize on canopy NTAs in a farm-scale study performed in Central Spain during 3 years. The study focused on hemipteran herbivores (leafhoppers and planthoppers) and hymenopteran parasitic wasps (mymarids) collected by yellow sticky traps, which accounted for 72% of the total number of insects studied. The dynamics and abundance of these groups varied among years, but no significant differences were found between Bt and non-Bt maize, indicating that Bt maize had no negative effect on these taxa. Nonetheless, the Cry1Ab toxin was detected in 2 different arthropods collected from Bt maize foliage, the cicadellids Zyginidia scutellaris and Empoasca spp. A retrospective power analysis on the arthropod abundance data for our field trials has determined that Z. scutellaris and the family Mymaridae have high capacity to detect differences between the Bt maize and its isogenic counterpart. The use of these canopy NTAs as surrogates for assessing environmental impacts of Bt maize is discussed.

Anagrus nedotepae sp. n. (Hymenoptera: Mymaridae), an egg parasitoid of Nedotepa curta (Hemiptera: Cicadellidae), a pest of coconut palm in West Africa.

A new Afrotropical species of Anagrus Haliday (Hymenoptera: Mymaridae), A. nedotepae Triapitsyn sp. n., is described and illustrated. The type series was reared from parasitized eggs of the leafhopper Nedotepa curta Dmitriev (Hemiptera: Cicadellidae) during a survey for its natural enemies in Côte d'Ivoire. This peculiar leafhopper, recently described from Ghana (Dmitriev 2016), lays its eggs on leaflets of coconut palm, and could be an economically important pest of this crop in West Africa, particularly because it is a suspected vector of the phytoplasma associated with the Côte d'Ivoire Lethal Yellowing disease of coconut, as characterized by Arocha-Rosete et al. (2014). Coconut lethal yellowing diseases cause severe economic losses to the very important coconut growing industry in several West African countries and elsewhere, being considered a threat of global economic and social significance (Gurr et al. 2016). Thus, the parasitoid may be of potential importance for natural biological control of this pest and urgently needs a scientific name to be used in further publications on its biology and ecology. Such studies are currently underway by the second author, who collected the type series of the new species.

Two genera of Mymaridae (Hymenoptera) new to Africa, a remarkable new species of Anaphes and new generic synonymy.

Bakkendorfia Mathot, syn. n. is placed in synonymy under Cleruchus Enock and its only described species transferred as Cleruchus musangae (Mathot), comb. n.Anaphes quinquearticulatus Huber & Triapitsyn, sp. n. is described; it is the only known Anaphes Haliday species with a 5-segmented funicle in females. Two genera are reported for the first time from the Afrotropical region and two species are described: Paranaphoidea (Idiocentrus) africana Huber & Triapitsyn, sp. n., and Allanagrus occidentalis Huber & Triapitsyn, sp. n.

Egg Parasitoid Complex of the Corn Leafhopper, Dalbulus maidis (DeLong) (Hemiptera: Cicadellidae), in Argentina.

The corn leafhopper, Dalbulus maidis (DeLong), is the most important leafhopper pest of maize, Zea mays, in the Americas. A survey of the diversity of its egg parasitoids was carried out in northwestern Argentina. During summer from 2004 to 2007, the samples were collected, using sentinel eggs of D. maidis on corn leaves, exposed in 48 cornfields. Sixteen species belonging to four families of Chalcidoidea (Hymenoptera) were identified. Among the parasitoid groups, Trichogrammatidae was the most represented family with eight species, followed by Mymaridae with six species. The mymarid Anagrus incarnatus Haliday and the trichogrammatid Pseudoligosita longifrangiata (Viggiani) were the most abundant and frequent parasitoids. The mean percentage of parasitism of D. maidis eggs was 16.4% and varied greatly among the sites, ranging from 0 to 56.7%; generally, it was higher in Yungas and lower in Monte province sites. The species richness was higher in the localities within the Yungas, with 13 parasitoid species, of which two species were dominant, comprising 83.6% of the collected individuals. Monte was the province that showed the highest diversity index (H´ = 1.62). In addition, we present information on the distribution, known host associations of each parasitoid species and an identification key to all species of egg parasitoids of D. maidis in Argentina.

Introduction to the Mymaridae (Hymenoptera) of Bangladesh.

An identification key to the 15 genera of Mymaridae found so far in Bangladesh is given, based on about 520 specimens collected using yellow pan traps placed in agricultural habitats and at the edge of ponds, mainly at Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur. Species already reported from Bangladesh are listed and three more are added: Acmopolynema orientale (Narayanan, Subba Rao & Kaur), Himopolynema hishimonus Taguchi, and Mymar pulchellum Curtis.

Description of three new species of Arescon Walker (Hymenoptera, Mymaridae) from China.

Three new species of Arescon Walker, 1846, Arescon gaoligongensis Jin & Li, sp. n., Arescon sparsiciliatus Jin & Li, sp. n. and Arescon stenopterus Jin & Li, sp. n. are described. A key to the Chinese species is given and photomicrographs are provided to illustrate morphological characters. All the specimens are deposited in the insect collections of Northeast Forestry University, China.

First report of Dicopuslongipes (Subba Rao) (Hymenoptera: Chalcidoidea) from India with new distribution data on some species.

Dicopuslongipes (Subba Rao) (Hymenoptera: Chalcidoidea: Mymaridae) is recorded from India for the first time. New additional distribution records of Mymaridae from the southern Indian states of Tamil Nadu and Kerala are documented.

A taxonomic study of Ooctonus (Hymenoptera, Mymaridae) from Heilongjiang, China.

Five species of Ooctonus Haliday (Hymenoptera, Mymaridae) from Heilongjiang Province, China, are reviewed. One species, Ooctonushuberi sp. n., is described as new, and four species, Ooctonusorientalis Doutt, Ooctonussaturn Triapitsyn, Ooctonussublaevis Förster and Ooctonusvulgatus Haliday are reported as new to China. A key to the females of the 10 described Chinese species is given. All the specimens are deposited in the insect collections of Northeast Forestry University, China.

Density dependence of Anaphes sordidatus (Hymenoptera: Mymaridae) parasitism on eggs of Listronotus oregonensis (Coleoptera: Curculionidae).

Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) oviposits in carrot leaves and the larvae feed in carrot roots. Its eggs are parasitized by Anaphes sordidatus (Girault) (Hymenoptera: Mymaridae) throughout its oviposition period. This parasitoid is the major biotic mortality factor for L. oregonensis. Parasitism by A. sordidatus was studied for three years in sequentially sown plots of carrots, Daucus carota var. sativa. Over the scason, significantly fewer L. oregonensis eggs were oviposited in later sown carrots than in earlier sown carrots because oviposition started later in late sown plots of carrots. A positive temporal density-dependent relationship was observed each year between parasitism rates and host densities. This positive density dependence occurred in early and mid-summer for earlysown carrots where host density reached 1-2 host eggs per plant but disappeared in late summer when host density decreased while parasitism remained high. Latesown carrots had low host egg density (0.2 host egg per plant) and contributed little to the total number of eggs. In these late sown plots, parasitism increased rapidly to over 80% but no density dependence was observed. Spatially, few statistically significant regressions were found but all indicated a positive spatial density-dependence. Most non-significant regressions occurred because the range of egg density was too small between plots for a given date.

Intra- and interspecific host discrimination in two closely related egg parasitoids.

Intraspecific host discrimination is frequently found in solitary parasitoids, but interspecific host discrimination, where female parasitoids recognize hosts already parasitized by females of other species, is rare. This particular behaviour appears to be adaptive only under specific circumstances. In this paper, we quantified intraspecific host discrimination in Anaphes n. sp. (Hymenoptera: Mymaridae), an endoparasitoid of the eggs of Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) and interspecific host discrimination toward eggs parasitized by Anaphes sordidatus (Girault), a sympatric species competing for the same resource in similar habitats. To examine host discrimination, choice experiments were used where the females had to choose between different categories of eggs (unparasitized, parasitized by Anaphes n. sp. or A. sordidatus). Superparasitism and multiparasitism were avoided in experiments where the female had a choice between unparasitized hosts and hosts parasitized by the same female, by a conspecific or by a female A. sordidatus. When all hosts available were parasitized, conspecific superparasitism occurred more often than self-superparasitism or multiparasitism. These results indicated that females Anaphes n. sp. were capable of self-, conspecific and interspecific discrimination. Self-discrimination followed recognition of an external marking while interspecific discrimination occurred mostly after insertion of the ovipositor. Interspecific discrimination could result from the recent speciation of these species and could be associated with a genotypic discrimination. This behavior appears to be adaptive because of the competition for common hosts between the two parasitoid species.

A new species of Ptilomymar (Hymenoptera, Mymaridae) and a key to the described species.

Ptilomymar dianensis sp. n. (Hymenoptera, Mymaridae) from southwest China is described and illustrated. A key to the six described species is given. The type specimens are deposited in the insect collections of Northeast Forestry University, China.