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The Oriental Chestnut Gall-wasp Dryocosmus Kuriphilus Yasumatsu, 1951, (Hymenoptera: Cynipidae) and Its Introduced and Native Parasitoids in Madeira Island, Portugal, with Notes on Some Other Parasitic Hymenoptera Reared from Gall Samples
Abstract
The accidental introduction to Madeira of the invasive chestnut gall wasp (CGW),
Dryocosmus kuriphilus, is reviewed, as is the subsequent biological control programme
implemented by the Regional authorities. This control programme was based on the importation of a non-native parasitoid, Torymus sinensis. Results from five years of parasitoid release are presented, including a list of native parasitoid species associated with D. kuriphilus galls in Madeira. Five species of Hymenoptera are listed as new records for Madeira: Dryocosmus kuriphilus Yasumatsu, 1951; Torymus sinensis Kamijo, 1982; Bootanomyia dorsalis (Fabricius, 1798); Colpoclypeus florus (Walker, 1839), and Ufens foersteri (Kryger, 1918)
The Asian chestnut gall wasp Dryocosmus kuriphilus Yasumatsu, native to China, was first detected in Europe in Italy in 2002. In Portugal it was declared in 2014, and it has since affected the Portuguese chestnut production. The introduction of its natural parasitoid Torymus sinensis Kamijo started through inoculative releases according to the National Action Plan for the Control of Dryocosmus kuriphilus, established by the Direção Geral de Agricultura e Veterenária (DGAV), in 2015. This research was carried out during 2018 and 2019, in five chestnut orchards in the Minho region (Northern Portugal). Between January and March 2018, at each location, three monthly harvests of 100 buds were carried out to determine the infestation level. Between April and June 2018, 240 galls were harvested every two weeks, with the purpose of studying the bioecology of D. kuriphilus. In each sampling site, 160 galls were placed in emergence boxes to follow adults of the D. kuriphilus population, and 80 galls were dissected with a binocular magnifying glass, to count and record the evolution of the larval stages of D. kuriphilus and of the parasitoids. The identification of T. sinensis and native parasitoids was carried out. The parasitism rates and Simpson diversity indices were determined. The percentage of buds infested by D. kuriphilus was high in all studied places, varying between 67% and 80%, regardless of the number of T. sinensis releases made and of the chestnut cultivars present in each orchard. The highest rate of parasitism by T. sinensis was 0.5044% and it was recorded in an orchard where there were two releases of T. sinensis in 2016 and 2017 (Arcos de Valdevez—Rio Cabrão—P1). Considering that the exotic parasitoid has already been released in the region since 2016, its establishment in all the chestnut orchards studied was confirmed, although with very low parasitism rates. The natural parasitism associated with the native parasitoid species of D. kuriphilus was confirmed in this work, recording values between 34% and 51% of the parasitized chestnut galls, with 11 species of native parasitoids having been identified: Eupelmus azureos, Eupelmus uruzonus, Eurytoma brunnivientris, Eurytoma pistaciae, Megastigmus dorsalis, Mesopolobus sp., Ormyrus pomaceus, Sycophila biguttata, Sycophila iracemae, Sycophila variegatta and Torymus flavipes.
Background:
The European species of the genus Tetrastichus (Insecta, Hymenoptera, Eulophidae, Tetrastichinae) are revised with 93 species, including 50 species described as new. The revision was conducted using an integrative taxonomic approach, based on DNA barcoding in combination with morphological characters. The Tetrastichinae are a biologically diverse and species-rich group of parasitoid wasps with numerous complexes of morphologically often very similar species that attack a wide range of hosts in over 100 insect families in 10 different orders. The genus Tetrastichus is, with almost 500 described species, the third largest genus of Tetrastichinae. Although biological information is lacking for most species, current data indicate that Tetrastichus species are gregarious koinobiont endoparasitoids developing on juvenile stages of mainly holometabolous insects. Due to their host specificity, several species of Tetrastichus are used as biological control agents.
New information:
The European species of Tetrastichus Haliday (Hymenoptera: Eulophidae) are revised using a combination of externo-morphological and DNA barcoding data. This is the first integrative approach for any of the large genera of the Tetrastichinae. A total of 93 species are included, of which 50 are described as new: T. agonussp. n., T. antonjanssonisp. n., T. argeisp. n., T. argutussp. n., T. asilissp. n., T. ballotussp. n., T. blediussp. n., T. broncussp. n., T. calcariussp. n., T. calmiussp. n., T. clisiussp. n., T. cosidissp. n., T. cumulussp. n., T. cyprussp. n., T. delvareisp. n., T. doczkalisp. n., T. elanussp. n., T. elodiussp. n., T. ennissp. n., T. enodissp. n., T. erinussp. n., T. evexussp. n., T. fadussp. n., T. fenrisisp. n., T. flacciussp. n., T. grediussp. n., T. iasisp. n., T. illydrissp. n., T. incanussp. n., T. inscitussp. n., T. intruitussp. n., T. johnnoyesisp. n., T. lacustrinussp. n., T. ladrussp. n., T. laniussp. n., T. laziussp. n., T. lixaliussp. n., T. lycussp. n., T. marcusgrahamisp. n., T. miniussp. n., T. mixtussp. n., T. nataliedaleskeyaesp. n., T. nymphaesp. n., T. pixiussp. n., T. scardiaesp. n., T. splendenssp. n., T. stisp. n., T. suecussp. n., T. tacitussp. n. and T. tartussp. n. Two keys for the identification of species are presented, one for females and one for males. Based on DNA barcode sequences for 70 of the species, a Maximum Likelihood tree to assess phylogenetic relationships within the genus is presented. These 70 species are also characterised by a combination of CO1 and morphological data. The remaining 23 species, without a DNA barcode, are characterised by morphological data. Using a combination of data from the morphology and CO1 or morphological data only, the species are separated into three species groups (clito-, hylotomarum-, murcia-groups) with 41 unplaced species outside these groups. Hosts are known for 27 of the species and they are gregarious, koinobiont endoparasitoids on a wide range of immature stages of holometabolous insects and appear to be very host specific. The first host record for Lepidoptera (Tineidae) in Europe is included.
The sexual generation of Dryocosmus destefanii Cerasa & Melika, 2018 that emerges from galls on Q. suber L. in Italy is described for the first time, establishing its heterogonic life cycle. We provide observations on its distribution, illustration of adults and galls and information on its biology as supported by morphological and molecular data. An illustrated identification key to Western Palaearctic Dryocosmus species is also given.
A phylogeny of the Torymidae (Chalcidoidea) is estimated using 4734 nucleotides from five genes. Twelve outgroups and 235 ingroup taxa are used, representing about 70% of the recognized genera. Our analyses do not recover Torymidae as monophyletic and we recognize instead two families: Megastigmidae (stat. rev.) and Torymidae s.s. (stat. rev.). Within Torymidae s.s., we recognize six subfamilies and six tribes, including Chalcimerinae, Glyphomerinae and Microdontomerinae (subf. nov.), and two new tribes: Boucekinini and Propalachiini (trib. nov.). Seven unclassified genera (i.e. Cryptopristus, Echthrodape, Exopristoides, Exopristus, part of Glyphomerus, Thaumatorymus, Zaglyptonotus) are assigned to tribes within our new classification. Five genera are restored from synonymy—Ameromicrus and Didactyliocerus from under Torymoides (stat. rev.), Iridophaga and Iridophagoides from under Podagrionella (stat. rev.) and Nannocerus from under Torymus (stat. rev.)—and three genera are synonymized—Allotorymus under Torymussyn. nov., Ditropinotus under Eridontomerussyn. nov. and Pseuderimerus under Erimerussyn. nov. A Palaearctic or Eurasian origin for Torymidae is proposed. The ancestral area of Megastigmidae is indicated as the Australian region. The most probable ancestral life strategy for Torymidae s.s. is ectoparasitism on gall-forming Cynipidae. The life strategy and putative hosts of the common ancestor of Megastigmidae remain uncertain.
The Asian chestnut gall wasp (ACGW), Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), is a global pest of
chestnut trees. This pest was first recorded in Slovenia in 2005. Despite strict phytosanitary measures it was present throughout the
country in native chestnut stands by 2013. We provide here the first overview of the parasitoids of ACGW in Slovenia recorded over a
4-year period and the direct interactions between parasitoid communities attacking hosts on chestnut and oaks at the same sites. A total
of 27 species of native parasitoids that normally parasitize oak cynipids emerged from ACGW galls. The most abundant species were
Torymus flavipes and Eupelmus urozonus. Seven species appear to be geographically well distributed in Slovenia. Twelve species of
oak gall wasp were parasitized by 19 species of parasitoids. All native parasitoids have broad host ranges, so a large parasitoid diversity
within this community can be expected. This is a novel study comparing the parasitoid communities associated with chestnut and oak
galls.
The associations occurring between the Asian chestnut gall wasp (ACGW) Dryocosmus kuriphilus Yasumatsu (Hymenoptera Cynipidae) and native parasitoids were investigated over the 3-year period 2010-2012 in a chestnut plantation located in the municipality of Castel del Rio (high Santerno Valley, Bologna province, Emilia Romagna, Italy). The chestnut trees were mixed with other plant species, including oaks, and were heavily infested by D. kuriphilus (which was first recorded in Emilia Romagna in 2008). In the survey period, a total of 12,015 spring galls were collected and an overall number of 7,094 insects emerged (5,182 D. kuriphilus and 1,912 parasitoids). The parasitoids, belonging to five families (Eupelmidae, Eurytomidae, Ormyridae,
Pteromalidae, Torymidae), were presumably recruited from oak gall wasps. They were identified using morphological characters and the most represented genus was Torymus. Within this genus, the morphospecies Torymus flavipes (Walker) was identified.Mesopolobus was the second most abundant genus in 2010 and 2011. The percentages of parasitism (calculated considering an average of 3.5 cells) were 3.06, 10.18 and 0.09 in 2010, 2011 and 2012, respectively. The dramatic reduction of parasitoids found
in 2012 might have been a consequence of biocoenotic dynamics, in particular of the instability of the interactions occurring between the ACGW and the generalist native parasitoids.
The world species of Bootanomyia Girault (Hymenoptera: Chalcidoidea, Torymidae) are reviewed. Nine species are transferred from Megastigmus to Bootanomyia as new combinations: B. almusiensis (Doganlar, 1989), B. dorsalis (Fabricius 1789), B. dumicola (Boucek 1982), B. habui (Kamijo, 1962), B. maculipennis (Yasumatsu and Kamijo, 1979), B. nipponicus (Yasumatsu and Kamijo, 1979), B. stigmatizans (Fabricious 1789), B. synophri (Mayr 1874), and B. zhaoi (Xu & He, 2003). Megastigmus bohemanii Ratzeburg, 1848 is reinstated as a species from synonymy under M. dorsalis Fabricius and transferred to Bootanomyia as B. bohemanii (Ratzeburg, 1848) (comb. and status n.). Seven species are described as new species: B. balikesirensis, B. emrezaferi, B. hepdurgunae, B. mehmeti, B. onuri, B. saragoldae, and B. shebnemae. An identification key for the world species of Bootanomyia is provided. Species of Bootanomyia are recorded as parasitoids of insect gall inducers in several plant parts.
Révision du genre Xyalaspis Hartig, 1843 (Hymenoptera: Figitidae: Anacharitinae) dans le Paléarctique occidental.Le genre Xyalaspis Hartig, 1843 (Hymenoptera: Anacharitinae) est révisé pour le Paléarctique occidental. Xyalaspis spinigera Reinhard, 1860 et Xyalaspis subulifera (Thomson, 1862) sont mis en synonymie avec Xyalaspis laevigata Hartig, 1843 et Xyalaspis rugosa Hartig, 1843 respectivement, et l'aire de distribution de ces espèces est étendue. Une nouvelle espèce est décrite pour la France : Xyalaspis pseudolaevigata n. sp. Xyalaspis laevis (Hedicke, 1914), est transféré au genre Aegilips Haliday, 1835. Les caractéristiques diagnostiques plus importantes sont illustrées. Des données sur la biologie, la distribution et la variabilité morphologique des espèces sont discutées. Une clé pour différencier les espèces ouest paléarctiques est rédigée.
Background and Purpose: Dryocosmus kuriphilus is a globally invasive insect pest, spreading very quickly in new habitats and making serious damage to sweet chestnut forests in Croatia and in several other European countries. Indigenous parasitoid species trophically associated with oak gallwasps have adapted to this new host but cannot effectively regulate its population density. Classical biological control using parasitoid Torymus sinensis has been proven to be the only effective method of controlling the populations of D. kuriphilus and has been successfully applied in Japan, South Korea, the USA and Italy. The aim of this review paper is to provide overview and up-to date knowledge about biological control of D. kurphilus and to describe first steps of introduction of T. sinensis to sweet chestnut forests in Croatia.
Conclusions and Future Prospects: Results presented in this paper show adapted biology and behavioural traits of T. sinensis to its host D. kuriphilus. The history and results of introductions of T. sinensis to Japan, the USA, Italy, France and Hungary are shown. The first report of release of T. sinensis to sweet chestnut forests in Croatia is given with discussion on native parasitoids attacking D. kuriphilus. Possible negative effects of T. sinensis on native parasitoid fauna and risks that could influence the successful establishment of T. sinensis in Croatia are discussed. Previous experiences have shown that T. sinensis can successfully control the population density of D. kuriphilus, slowing down the spread and mitigating negative impact of this invasive chestnut pest and keeping the damage of D. kuriphilus at acceptable level. High specificity of T. sinensis suggests that it has limited potential of exploiting native hosts but further detailed monitoring of native parasitoid and possible interactions with introduced T. sinensis is strongly suggested.
Considered as a major pest of Castanea species worldwide, the chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera, Cynipidae) can induce fruit production losses of 60-80%. Reported for the first time in Italy in 2002, this pest is now widespread across the French distribution of chestnut trees.
Based on successful attempts in other countries, a classical biological control program using the parasitoid Torymus sinensis Kamijo (Hymenoptera, Torymidae) has been implemented in France since 2011. Three main objectives were delineated for the program. The first is long-term control of chestnut gall wasp populations, be it in commercial orchards or in forests. The second objective is to take advantage of planned introduc- tions of T. sinensis to better understand factors that underpin the establishment and spread of exotic species. The third objective is to describe the recruitment of native parasitoids by invasive D. kuriphilus and to assess the impacts of T. sinensis on native communities.
During the two first years of this project, 42 releases of T. sinensis were achieved with an experimental manipulation of propagule pressure. Initial results indicate that: (i) T. sinensis has successfully established in at least 20 of the release sites; (ii) T. sinensis populations, as well as populations of native parasitoids, have a positive inter-annual growth rate; and (iii) no significant impacts of parasitoid introductions on the chestnut gall wasp have been observed yet.
The invasive chestnut gall wasp Dryocosmus kuriphilus (Cynipidae) is one of the most important insect pests on Castanea species worldwide (EPPO, 2005). In 2009, D. kuriphilus was found for the first time in southern Switzerland, most likely an invasion from nearby Italy (Forster et al., 2009). In summer 2010, in a five hectare chestnut orchard near Stabio, a twig dieback was observed in the crown of trees heavily infested with last season's D. kuriphilus galls (Fig. 1). This orchard showed one of the heaviest gall infestations in Switzerland. In spring 2010, more than 40% of the buds were infested with galls. An inspection after leaf fall revealed that young twigs (i.e. twigs formed in the current year or in the previous year) with galls were more likely to have symptoms of chestnut blight, caused by the fungus Cryphonectria parasitica (Diaporthales, Ascomycota). In contrast, no visible signs of C. parasitica infections were observed on young twigs without galls. Chestnut blight was first observed in southern Switzerland in 1948 and is currently widespread throughout the country (Heiniger & Rigling, 1994). To verify whether abandoned D. kuriphilus galls were infected with C. parasitica, and thus serve as a possible entry point for the fungus, 24 young twigs (half showing symptoms of the disease and half not) with abandoned galls were sampled in November 2010. Incidence of C. parasitica infection was determined from the collected galls (n=44) as described by Bissegger et al. (1997).Cultures were identified by comparing their morphology on potato dextrose agar with those of reference cultures from our collection and by determining their vegetative compatibility (vc) type (Bissegger et al., 1997). C. parasitica cultures were obtained from all 12 young twigs (one gall per twig) with visible signs of C. parasitica infections on the galls or on adjacent twig sections (Fig. 2).In contrast, the fungus was isolated from only four out of 32 galls from the 12 twigs with no visible signs of C. parasitica infections (Fig. 3). Pairing tests showed that all isolates belonged to vc-types present in southern Switzerland. Thus, young twigs with abandoned galls can be infected by C. parasitica. Isolation from asymptomatic tissue indicates that the fungus was either in an early stage of infection or endophytically present inside the abandoned gall. Although our data do not allow an unequivocal answer to the question whether the twigs are first colonised by D. kuriphilus or by C. parasitica, there is indirect evidence supporting a first colonisation by the gall wasp. D. kuriphilus mostly lays eggs inside healthy dormant buds (Itô, 1967), while C. parasitica needs wounds on the bark to penetrate and infect chestnut trees (Anagnostakis, 1987). The holes through which the adult females of D. kuriphilus emerge from the galls in summer may present an entrance opportunity for C. parasitica spores. The fungus may then saprophytically colonize the moribund tissue of abandoned galls eventually spreading into the adjacent twig, inducing the formation of cankers. More detailed information on the incidence of chestnut blight on twigs with galls would be helpful for better estimating the ecological effects of the interaction between these two invasive organisms.
Identification of Alebra leafhoppers is difficult because most species do not show specific differences in male genital structures. Colour pattern and host plant associations, the characters traditionally used in the recognition of these species, show considerable intraspecific variation. In the last decade, it was proved that the shape of male abdominal apodemes is the most reliable morphological character to separate species of this genus, and since then, some species have been splitted in two. To untangling the systematics of the European species it urges to revise data on host plants and distribution. For the Iberian Peninsula the actual species number was still uncertain because the taxonomic value of apodemes in Alebra was unknown when the faunistic records on this region were published. In this work it was analysed material from Spain, Portugal and the island of Madeira and three species were identified: A. albostriella (Fallén, 1826), A. coryli Le Quesne, 1976, new to the Iberian peninsula, and A. viridis Rey, 1894 sensu Gillham 1991, recorded for the first time to the fauna of Madeira and Spain. Resumen: La identificación de cigarrillas del género Alebra es difícil porque la mayoría de las especies no presentan diferencias específicas en las estructuras genitales de los machos. Los patrones de color y la asociación a sus plantas huéspedes, caracteres tradicionalmente utilizados en la separación de estas especies, muestran una considerable variación intraespecífica. En la última década, se ha probado que la forma de los apodemas abdominales de los machos es el carácter morfológico más fiable para separar las especies de este género, y desde entonces, algunas especies han sido separadas en dos. Para esclarecer la sistemática de las especies europeas de este género, es necesario hacer una revisión urgente de los datos existentes sobre sus plantas huéspedes y distribución. En la Península Ibérica el número real de especies conocidas todavía era incierto porque el valor taxonómico de los apodemas en Alebra era desconocido cuando fueron publicados los datos faunísticos sobre esta región. En este trabajo se ha estudiado material de España, Portugal y la isla de Madeira y han sido identificadas tres especies: A. albostriella (Fallén, 1826), A. coryli Le Quesne, 1976, nueva cita para la Península Ibérica, y A. viridis Rey, 1897 sensu Gillham 1991, referida por primera vez para la fauna de Madeira y España. Palabras clave: Hemiptera, Cicadellidae, cigarrillas, Alebra, Península Iberica, Madeira, distribución.
A new species of Colpoclypeus Lucchese (Hymenoptera: Eulophidae) is described and illustrated. Colpoclypeus michoa-canensis Sánchez & Figueroa attacks Argyrotaenia montezumae Walsingham (Lepidoptera: Tortricidae) on blackberry plants. A key is included to separate C. michoacanensis from C. florus (Walker), the only other species in this genus.
Twenty-one species of the family Braconidae (Hymenoptera) are added to the checklist of Braconidae from Madeira, resulting in 113 species, of which 17 species are endemic to Madeira Islands and 4 species are only known from Madeira and Canary Islands. Five species are reported new for the Selvagens Islands. Five new species are described and illustrated: Homolobus (Apatia) madeirensis spec. nov. (Homolobinae), Dinotrema glabriscutum spec. nov., D. brunneicornis spec. nov. and Orthostigma minusculum spec. nov. (Alysiinae: Alysiini) and Phaedrotoma flaveola spec. nov. (Opiinae: Opiini). Meteorus pendulus (Müller, 1776) is considered to be a Holarctic species, with as junior synonyms the Nearctic Perilitus communis Cression, 1872 (syn. nov.) and the Palaearctic Ichneumon gyrator Thunberg, 1822.
The chestnut gall wasp Dryocosmus kuriphilus is a global pest of chestnut (Castanea). Established as a pest in the mid 20th century in Japan, Korea and the USA, this species has now reached Europe. Successful
deployment of a biocontrol agent, Torymus sinensis, in Japan has led to its early release in Italy. Here we provide the first overview of the natural enemies associated with
D. kuriphilus in its native and invaded ranges, and discuss general patterns in community development. We then use what is known about
European oak gall wasp communities to predict possible future developments for D. kuriphilus, and possible interactions between parasitoid communities attacking hosts on chestnut and oaks.
Trissolcus semistriatus (Nees, 1834) (Hymenoptera: Scelionidae) is the most common and important egg parasitoid of Eurygaster integriceps Put., 1881 (Hemiptera: Scutelleridae). This study was conducted to determine discrimination E. Integriceps eggs parasitized by either self or a conspecific female of T. Semistriatus in choice and nochoice tests, and to establish effect of adult parasitoid density and host density on parasitism in the laboratory in 2016. Female parasitoids did not superparasitize self-parasitized host eggs. However, superparasitism of 18% (significantly lower than the 81% parasitism rate) of the eggs parasitized by another female occurred within 1 h of first parasitism. Superparasitism was significantly lower at 1% in no-choice tests than the 23% recorded in choice tests within 24 h of first parasitism. Parasitism significantly decreased with increasing host egg number, but parasitism did not change with increasing parasitoid density. Therefore, it is concluded that T. Semistriatus can discriminate between parasitized and unparasitized host eggs, with superparasitism infrequent when females encounter preparasitized host eggs within 48 h of first parasitism.
1. Biological invasions of exotic species pose a major threat to native biodiversity. Invaders are known to have direct impacts on native species; however, less well studied are the indirect impacts mediated through the integration of invaders into trophically linked communities.
2. A survey of the chalcid wasp parasitoid community attacking the chestnut gallwasp Dryocosmus kuriphilus was carried out over a 5‐year period at 26 sites in north‐western Italy. More than 415 000 galls were collected and more than 10 000 parasitoid specimens emerged. Twenty‐seven parasitoid species belonging to six families (Eurytomidae, Pteromalidae, Torymidae, Eupelmidae, Ormyridae, Eulophidae) were identified using morphological and molecular methods; seventeen are new records for the parasitoid community associated with D. kuriphilus in Italy. The morphospecies complexes Megastigmus dorsalis , Eupelmus urozonus, E. annulatus , and Eurytoma pistaciae were the dominant species; another six morphospecies were encountered regularly but at low frequency; and 13 species were recorded only occasionally. The attack rate of any individual parasitoid species was low, although the more common species appeared to be increasing their use of this novel host.
3. Biases observed in the sex ratios of parasitoids emerging from D. kuriphilus galls suggest that parasitoid individuals are making life‐history decisions to take advantage of the high abundance of this host. Overall, these patterns imply that there is an ongoing transfer of parasitoids between oak and chestnut galls, and hence a high potential for this invading species to have a major impact on native oak gall communities via indirect competition mediated through shared parasitoids.
The fast spread of Chinese gall wasp (Dryocosmus kuriphilus) represents a new constraint factor for chestnut stands and orchards in Italy. So far, the favourable effect of hypovirulence in Cryphonectria parasitica-Castanea sativa patho-system allowed the development of chestnut cultivation. This situation could be modified by the progressive weakening of the trees caused by intensive attacks of the new parasite. During recent surveys worrying blight damage recurrences were observed in different Italian chestnut areas (in Piemonte, Trentino and Toscana regions) which were highly infested by the Chinese wasp. While biological control treatments against the parasite are carried out, it is necessary to set up integrated protocols for the management of chestnut orchards to allow the survival of trees and their productivity.
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