Molecular Data Confirm Interspecific Limits of Four Alloxysta and One Phaenoglyphis Species of Parasitic Wasps within the Subfamily Charipinae (Cynipoidea: Figitidae).

The hymenopteran subfamily Charipinae (Cynipoidea: Figitidae) consist of a group of parasitic wasps that are exclusive hyperparasitoids of Hemipteran. The species boundaries in Charipinae have historically been unclear. While diagnostic morphological features have been established for the stepwise separation of species, it is recommended to confirm those limits using molecular data. Here, we focus on the genera Alloxysta Förster, 1869 and Phaenoglyphis Förster, 1869, both of which contain species that are hyperparasitoids of aphids. We sequenced three genes (mitochondrial COI and 16S rDNA, and nuclear ITS2 rDNA) from specimens that were identified as belonging to five species: Alloxysta brevis (Thomson, 1862), A. castanea (Hartig, 1841), A. ramulifera (Thomson, 1862), A. victrix (Westwood, 1833), and Phaenoglyphis villosa (Hartig, 1841). The phylogeny resulting from concatenating these genes supported the species status of the five morphologically identified taxa, with P. villosa nested within Alloxysta. Our study thus indicates that these molecular markers can successfully distinguish charipine species, and also indicates that the genera Alloxysta and Phaenoglyphis may be more closely related than previously hypothesized. We also present the first estimates of genetic distances for these species. Future studies that include more species, loci, and/or genomic data will complement our research and help determine species relationships within the Charipinae subfamily.

Characterising the north-western European species of Phaenoglyphis Förster, 1869 (Hymenoptera: Figitidae: Charipinae) with novel insights from DNA barcode data.

Background: The taxonomy of the hymenopteran parasitoid subfamily Charipinae (Hymenoptera: Cynipoidea: Figitidae) has, until recently, been in a state of chaos. While this situation has improved significantly in recent years, most of the efforts were focused on morphological data of typically old specimens. Here, we present the first integrative approach to describe the diversity of the genus Phaenoglyphis Förster, 1869 from north-western Europe. New information: For seven (of a total of 17) species, we provide DNA barcode data. Phaenoglyphisbelizini Pujade-Villar, 2018 and Phaenoglyphisevenhuisi Pujade-Villar & Paretas-Martínez, 2006 are recorded for the first time from Germany. All DNA barcodes and specimen data were added to the publicly available GBOL and BOLD reference database. The presence of a 6 bp long deletion in the CO1 barcode region that is characteristic to the genus and unique amongst Figitidae supports the monophyly of Phaenoglyphis.

Not All Field Margins Are Equally Useful: Effects of the Vegetation Structure of Margins on Cereal Aphids and Their Natural Enemies.

Differences in the semi-natural vegetation of field margins will affect the biological control services derived from the presence of these semi-natural habitats adjacent to fields. Of the plant functional traits that are most relevant for insects, plant life forms reflect different aspects of plant structure and functioning that can help predict the value of marginal vegetation for arthropods in agricultural systems. The aim of this study was to determine the effect of the vegetation structure of field margins on cereal aphids and on some of their natural enemies (parasitoids, hoverflies and ladybugs) in terms of plant life forms. We characterized margin vegetation using the relative cover of each life form and sampled insects in crops along transects parallel to field margins. Our results show that in the studied areas, the abundance of natural enemies was greater near margins dominated by annual plants than in margins dominated by perennial plants. On the other hand, the abundances of aphids and parasitism rates were higher near margins dominated by perennial woody plants than near margins dominated by perennial herbaceous plants. By promoting specific life forms in existing margins, farmers can enhance the conservation biological control and relieve aphid pressure on their crops.

Overview of the current status of Charipinae (Hymenoptera, Cynipoidea, Figitidae): taxonomy, distribution, and diversity.

The subfamily Charipinae (Hymenoptera: Cynipoidea: Figitidae) has had a problematic taxonomic history as many species have been described without comprehensive revisions being undertaken. Reliably identifying these species based on morphological assessment has been almost impossible. Recently, the types of all species have been re-examined and photographed, resulting in numerous taxonomic corrections that have been published elsewhere. Consequently, a summary checklist of all species that have ever been described within the Charipinae is provided with their current accepted status, including all associated references dealing with the historical nomenclatural changes and synonymy. We also provide up-to-date information on the diversity and distribution patterns of Charipinae to assist researchers working on these species in aphid biological control programs.

Hymenoptera Complex Associated with Myzus persicae and Hyalopterus spp. in Peach Orchards in Northeastern Spain and Prospects for Biological Control of Aphids.

Aphids are a serious pest for peach crops. They have traditionally been managed with insecticides, but there is increasing concern about the risk that insecticides pose to both humans and the environment. As a first step to use biological control in aphid management, we conducted a 3-year field survey in northeastern Spain to determine which parasitoids and hyperparasitoids were most prevalent on two aphids, Myzus persicae (Sulzer) and Hyalopterus spp. Koch, the most harmful to peach trees. We collected 11 parasitoid species from M. persicae, with Aphidius matricariae (Haliday) being the most abundant. Two parasitoid species were also collected from Hyalopterus spp., Aphidius transcaspicus Telenga and Praon volucre (Haliday). Hyperparasitoid species overlapped between these aphids but their relative abundances differed. We also discuss the possible impacts of hyperparasitoids on parasitoid populations. Our results suggest that it would be feasible to implement biocontrol methods for aphids in integrated pest management programmes in peach orchards. There are a number of primary parasitoid species associated with these aphids, and the nearby crops and wild vegetation in the vicinity and within the orchards may provide a suitable habitat for them. Additionally, some of them are commercially available and might be usable in augmentative releases.

Keys to world Charipinae (Hymenoptera, Cynipoidea, Figitidae).

Eight genera of Charipinae are defined, keyed out, and illustrated. Keys for all charipine species within each valid genus, including Alloxysta, Apocharips, Dilyta, Phaenoglyphis, and Thoreauana, are presented, except for Dilapothor, Lobopterocharips, and Lytoxysta, which are monotypic. Figures are provided to show the diagnostic morphological features as used in the keys.

Description of a new Synergus species from China and comments on other inquiline species (Hymenoptera: Cynipidae: Synergini).

A new species, Synergus mongolicus Pujade-Villar & Wang n. sp., is described from galls collected on twigs of Quercus mongolica. The morphological characters useful for differentiating the new species are also discussed. Three inquilines species are recorded from China for the first time: Saphonecrus shirakashii, Synergus belizinellus and S. symbioticus. Saphonecrus tianmushanus is considered a n. syn. of S. shirakashii based on comparison of the types. Saphonecrus taiwanensis Pujade-Villar new name is proposed for Saphonecrus lithocarpii Schwéger & Melika, 2015 by homonymy with S. lithocarpi Pujade-Villar, Guo, Wang & Chen, 2015 and finally Saphonecrus chinensis Tang & Schwéger, 2015 is considered a n. syn. of S. lithocarpi Pujade-Villar, Guo, Wang & Chen, 2015.

Species composition and seasonal dynamics of aphid parasitoids and hyperparasitoids in wheat fields in northern China.

Parasitoids are important natural enemies of aphids in wheat fields of northern China, and interest in them has increased in recent years. However, little is known regarding parasitoids of wheat aphids, which has hindered the study and understanding of aphid-parasitoid interactions. In the present study, three primary parasitoids and 15 hyperparasitoids were collected in wheat fields during a 2-year survey in northern China (2014, 2015) and a 2-year investigation at Langfang, Hebei Province (2015, 2016). Among them, Aphidius uzbekistanicus Luzhetski was found most frequently among the primary parasitoids, while Pachyneuron aphidis (Bouché) dominated the hyperparasitoid community. Investigation of the dynamics of wheat aphids and parasitoids revealed that the primary parasitoids appeared early in the growing period and that the hyperparasitoids appeared later. Analysis of the seasonal dynamics revealed that growth of the parasitoid population followed that of the aphid population and that the parasitism rates were highest in the late growing period.

Species composition and richness of aphid parasitoid wasps in cotton fields in northern China.

The cotton aphid, Aphis gossypii (Hemiptera: Aphididae), is a serious pest of cotton across the globe, particularly in the cotton agroecosystems of northern China. Parasitic wasps are deemed to be important natural enemies of A. gossypii, but limited information exists about their species composition, richness and seasonal dynamics in northern China. In this study, we combine sampling over a broad geographical area with intensive field trials over the course of three cropping seasons to describe parasitoid-hyperparasitoid communities in cotton crops. We delineate a speciose complex of primary parasitoids and hyperparasitoids associated with A. gossypii. Over 90% of the primary parasitoids were Binodoxys communis. Syrphophagus sp. and Pachyneuron aphidis made up most of the hyperparasitoids. Parasitism rates changed in a similar way following the fluctuation of the aphid population. Early in the growing period, there were more hyperparasitoids, while later, the primary parasitoids provided control of A. gossypii. The first systematic report of this cotton aphid parasitoid complex and their population dynamics in association with their hosts presented a comprehensive assessment of cotton parasitoid species and provided important information for the establishment and promotion of their biological control of cotton aphids.

Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition.

It has become increasingly evident that many organisms rely on microbial symbionts for defense against natural enemies, but the ecological importance of defensive symbionts for natural communities still needs to be investigated. A well-known example is Hamiltonella defensa, a heritable endosymbiotic bacterium commonly found in aphids. Laboratory experiments have shown that H. defensa strongly protects aphids against parasitic wasps (parasitoids), although this protection is not equally effective against different species of parasitoids, or even different genotypes of the same species. These results suggest that H. defensa plays an important role in reducing aphid mortality by parasitoids and presumably affects the community composition of parasitoids relying on aphids as a resource. However, there is little evidence that this is indeed the case under natural conditions. We tested this in a field experiment with black bean aphids (Aphis fabae) by setting up replicated field plots with genetically identical aphids that did or did not harbor H. defensa and following their colonization by natural enemies over a growing season. We observed a clear reduction in parasitism of symbiont-protected aphids, particularly by the parasitoids posing the highest risk. However, protected aphids did not develop larger populations than unprotected ones, possibly reflecting the balancing effect of costs associated with harboring H. defensa. We also observed shifts in the parasitoid species composition on aphids protected by H. defensa, showing that defensive symbionts have the potential to alter the diversity and structure of food webs, with likely consequences for their function and stability.

Flagellar Sensillar Equipment of Two Morphologically Closely Related Aphid Hyperparasitoids (Hymenoptera: Figitidae: Alloxysta).

The antennal sensillar equipment in the parasitic wasp family Figitidae was analyzed to date only in few species, despite some are associated with crop pests and can have an economic importance. It is the case of the genus Alloxysta, which includes hyperparasitoids of aphids which can potentially reduce effectiveness of primary pest parasitoids. Here we analyzed, through scanning electron microscopy, the diversity, morphology, and distribution of the antennal sensilla in males and females of Alloxysta consobrina (Zetterstedt) and Alloxysta victrix (Westwood), two species with overall very similar morphology. In both species, antennae are filiform and cylindrical, and flagellum was longer in A. victrix. Eight sensillar types have been recognized: four types of sensilla trichoidea (ST-A, ST-B, ST-C, ST-D), sensilla coeloconica, sensilla placoidea, sensilla campaniformia, and sensilla basiconica. ST-A, ST-B, ST-C, and sensilla placoidea were the most abundant types on the antennae and often increased in number and decreased in size toward the tip of antenna. The two species seem to have several differences in their sensillar equipment, possibly in accordance with the different degree of host range. On the other hand, sexual dimorphism is probably due to the different stimuli that have to be correctly processed. The comparison with the other species of Figitidae studied by far showed, at subfamily-level, that variability in sensillar equipment and phylogeny do not agree. This suggests a complex series of morphological changes during evolution of this group. The taxonomic sample should be thus substantially enlarged to disclose possible trends in sensillar equipment evolution in the family.

Qualitative analysis of aphid and primary parasitoid trophic relations of genus Alloxysta (Hymenoptera: Cynipoidea: Figitidae: Charipinae).

Charipinae hyperparasitoids affect effectiveness of the primary parasitoids of aphids by decreasing their abundance and modifying their behavior. As a result, increase of aphid populations can cause severe yield losses in some crops. Therefore, ecological studies on the subfamily Charipinae have a great economical and biological importance. Host specificity of these hyperparasitoids is still under debate and for many Charipinae species very little is known about their trophic relations. Here, we give a comprehensive overview of the trophic relationships between the Charipinae species of the genus Alloxysta Förster and their aphid and primary parasitoids hosts, worldwide. Within this subfamily, Alloxysta arcuata (Kieffer), Alloxysta brevis (Thomson), Alloxysta fuscicornis (Hartig), and Alloxysta victrix (Westwood) are the most generalist species sharing many aphid hosts, while for primary parasitoid hosts these are A. arcuata, A. brevis, Alloxysta pleuralis (Cameron), and A. victrix. Alloxysta citripes (Thomson), Alloxysta halterata (Thomson), Alloxysta leunisii (Hartig), and Alloxysta ramulifera (Thomson) appear, up to now, as the most specialized in relation to the primary parasitoid hosts. Primary parasitoids of the genera Aphidius Nees, Lysiphlebus Förster, Praon Haliday, and Trioxys Haliday are the most common hosts for Alloxysta species, and the common host aphid species belong to the genera Aphis L., Uroleucon Mordvilko, Myzus Passerini, and Sitobion Mordvilko. Host range is analyzed for each Alloxysta species, as well as the extent of overlap between them. We used Jaccard's distance and a hierarchical cluster analysis to determine the host range dissimilarity. A permutation test has been applied to analyze if the host range dissimilarity is significantly different from what is expected by chance. We have calculated additional qualitative measures that complement well the Alloxysta niche overlap analysis and evaluated their host specificity using different indices and bipartite networks.

Review of the Neotropical Charipinae (Hymenoptera, Cynipoidea, Figitidae)

A review of the Neotropical Charipinae is given, with 35 species from four genera: Alloxysta, Apocharips, Dilyta and Phaenoglyphis. One new species, Alloxysta centroamericana Ferrer-Suay & Pujade-Villar sp. nov. is described; six Alloxysta species, Alloxysta citripes (Thomson, 1862), Alloxysta fracticornis (Thomson, 1862), Alloxysta melanogaster (Hartig, 1841), Alloxysta piceomaculata (Cameron, 1886), Alloxysta postica (Hartig, 1841) and Alloxysta pusilla (Kieffer, 1902), are recorded for the first time from the Neotropical region; 10 new records for earlier known species are also given. Diagnoses and a key to all species are also provided.

Revision of Apocharips Fergusson (Hymenoptera: Figitidae: Charipinae) with description of three new species from Colombia.

The genus Apocharips is here revised. Three previously described species are considered as valid: Apocharips angelicae Pujade-Villar & Evenhuis, 2002, A. hansoni Menke, 1993, and A. trapezoidea (Hartig, 1841). Apocharips eleaphila (Silvestri, 1915) and A. peraperta (Silvestri, 1915) are synonymyzed with A. trapezoidea. Three new species are here described: Apocharips colombiana Ferrer-Suay & Pujade-Villar n. sp., Apocharips tamanii Paretas-Martinez & Pujade-Villar n. sp. and Apocharips tropicale Ferrer-Suay & Paretas-Martinez n. sp. A key to the six species included in Apocharips is given.