Candidate For Classical Biological Control Research Articles

Survey for Adventive Populations of the Samurai Wasp, Trissolcus japonicus (Hymenoptera: Scelionidae) in Pennsylvania at Commercial Fruit Orchards and the Surrounding Forest.

Simple SummaryInvasive species that are freed of associated natural predators increase in population and disrupt the management plans of growers. The brown marmorated stink bug, Halyomorpha halys, is an invasive species that originated in Asia. A promising management tactic for the species is to release an associated parasitoid, the samurai wasp, Trissolcus japonicus. Populations of the samurai wasp have begun to adventively establish in several regions, including Pennsylvania. In order to monitor and use the species as an alternative management strategy to insecticides, it is imperative to understand the baseline populations during the early establishment phase. The aims of this study were to determine if the samurai wasp is already present in commercial orchards in Pennsylvania, where the brown marmorated stink bug has been present in high numbers since approximately 2010. Native Trissolcus wasps were also identified. This study found the samurai wasp in eight counties in Pennsylvania with several orchards containing populations of the species within orchard blocks. These baseline data provide a starting point for controlling H. halys naturally, which was previously controlled only with broad-spectrum insecticides.The samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), is an egg parasitoid associated with the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). Trissolcus japonicus is a candidate for classical biological control of H. halys populations. Since 2014, adventive populations of T. japonicus have been detected in 14 US states, in the Canadian provinces of British Columbia and Ontario, and in two European countries, Switzerland and Italy. Establishing baseline information about populations of T. japonicus is important, as this species is not host specific to H. halys and the potential ecological effects of the accidental introductions are not fully known. In this study, yellow sticky cards were deployed at commercial fruit orchards in nine counties in Pennsylvania separated by more than 400 km. Trissolcus japonicus was detected on cards in eight counties, and in two habitats, in the orchard and at the forest border. Other native species of Scelionidae known to attack the eggs of H. halys were also identified, including Trissolcus euschisti (Ashmead), Trissolcus brochymenae (Ashmead), and Telenomus podisi Ashmead (Hymenoptera: Scelionidae). These results are important baseline ecological knowledge for both T. japonicus, which appears to be established in orchards throughout Pennsylvania, and other native Scelionidae.

Two new species of Ooencyrtus (Hymenoptera, Encyrtidae), egg parasitoids of the bagrada bug Bagrada hilaris (Hemiptera, Pentatomidae), with taxonomic notes on Ooencyrtus telenomicida

In support of a biological control program in California, USA, against the bagrada bug,Bagrada hilaris(Burmeister) (Hemiptera, Pentatomidae), an invasive pest of Asian origin, colonies of two species ofOoencyrtusAshmead (Hymenoptera, Encyrtidae) are maintained usingB. hilariseggs as host. One of them,Ooencyrtus mirusTriapitsyn & Power,sp. nov., is of Pakistani origin. It displays natural preference for bagrada bug eggs and is being evaluated in quarantine as a candidate for classical biological control. The other,Ooencyrtus lucidusTriapitsyn & Ganjisaffar,sp. nov., appears to be native to California, and we believe it switched toB. hilarisfrom native pentatomid hosts. Both new species are described and illustrated, as is the Old World speciesOoencyrtus telenomicida(Vassiliev), for which a neotype is designated. The presented morphometric evidence as well as mitochondrial and nuclear ribosomal DNA sequence data separateOoencyrtus mirusfromO. telenomicida. A lectotype is designated forOoencyrtus californicusGirault from California, which is morphologically similar toO. lucidus.

Trissolcus japonicus (Hymenoptera: Scelionidae) Causes Low Levels of Parasitism in Three North American Pentatomids Under Field Conditions.

Trissolcus japonicus (Ashmead), an Asian parasitoid of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), was first detected in North America in 2014. Although testing in quarantine facilities as a candidate for classical biological control is ongoing, adventive populations have appeared in multiple sites in the United States, Canada, and Europe. Extensive laboratory testing of T. japonicus against other North American pentatomids and H. halys has revealed a higher rate of parasitism of H. halys, but not complete host specificity. However, laboratory tests are necessarily artificial, in which many host finding and acceptance cues may be circumvented. We offered sentinel egg masses of three native pentatomid (Hemiptera: Pentatomidae) pest species (Chinavia hilaris (Say), Euschistus conspersus Uhler, and Chlorochroa ligata (Say)) in a field paired-host assay in an area with a well-established adventive population of T. japonicus near Vancouver, WA. Overall, 67% of the H. halys egg masses were parasitized by T. japonicus during the 2-yr study. Despite the ‘worst case’ scenario for a field test (close proximity of the paired egg masses), the rate of parasitism (% eggs producing adult wasps) on all three native species was significantly less (0.4–8%) than that on H. halys eggs (77%). The levels of successful parasitism of T. japonicus of the three species are C. hilaris > E. conspersus > C. ligata. The potential impact of T. japonicus on these pentatomids is probably minimal.

First laboratory evaluation of Gryon gonikopalense (Hymenoptera: Scelionidae), as potential biological control agent of Bagrada hilaris (Hemiptera: Pentatomidae)

The pentatomid bug Bagrada hilaris is a severe invasive alien pest of Brassicaceae crops, which first appeared in California in 2008 and is expanding to several southern U.S. states and South America. To answer the demand of growers for sustainable management methods, a biological control program started in 2015. The egg parasitoid Gryon gonikopalense Sharma was collected in Pakistan, and after morphological identification here described, is being evaluated as a candidate for classical biological control against B. hilaris. Basic life history studies were performed in climatic chambers (22 ± 0.5 °C, RH 50 ± 5%, L/D 12:12). On average, Gryon gonikopalense developed in 25.1 ± 1.4 (mean ± sd) days and live 66.4 ± 30.7 days. Allowing females to oviposit reduced their lifespan by 52%, and food deprivation reduced it by 87%. During their life, females produced 59.2 ± 22.3 offspring on average with a maximum fecundity during the first week of their life. Mean progeny sex ratio was 46.3% female. Live host eggs from 1 to 4 days old were suitable for parasitoid oviposition, but eggs stored at −80 °C were not. Hence, the parasitoid could attack bagrada eggs for most of their development in the field but storage of bagrada eggs at very low temperature for later use in rearing or as sentinel eggs in the field is not recommended. These data provide a baseline for designing host specificity tests to help determine whether G. gonikopalense is suitable to use as a biocontrol agent of Bagrada hilaris.

First detection of the samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae), in Canada

We report the first detection of Trissolcusjaponicus, an exotic Asian egg parasitoid and the primary candidate for classical biological control of the invasive brown marmorated stink bug, Halyomorphahalys, in Canada. Twenty-eight Trissolcusjaponicus emerged from an H.halys egg mass from a site heavily infested by H.halys in Chilliwack, British Columbia, in 2018. This egg mass was deployed and retrieved as part of ongoing sentinel egg mass surveys for natural enemies of H.halys from 2017–2018 in coastal and interior British Columbia (total of 1,496 egg clusters at 16 sites). The identification of T.japonicus was based on biology (high levels of successful emergence from H.halys eggs), morphology, and mitochondrial DNA sequences. Trissolcusjaponicus was not detected at any other survey sites in 2017–2018; however, three species of indigenous egg parasitoids were found attending or emerging from H.halys egg masses at low levels (<4%) at several sites. The origin of the detected T.japonicus, the extent of its establishment in British Columbia, and its ultimate impact on H.halys populations remain to be determined. Nonetheless, the detection of this exotic biological control agent in Canada concurrently with regulatory review of its intentional importation and release is emblematic of the current uncertainty around regulatory control on the movement of biological control agents across borders.

Feasibility assessment for the classical biological control of Tamarix in Argentina

Saltcedars are woody plants in the genus Tamarix L. (Caryophyllales: Tamaricaceae) and are native to Eurasia and Africa. Several species have become invasive in the Americas, Australia and South Africa. In Argentina there are four species of Tamarix distributed in arid, semi-arid and coastal areas of most provinces. The taxonomic isolation of Tamarix spp. in Argentina, their widespread distribution, negative impact to natural areas and lack of impact from existing natural enemies all indicate that Tamarix is an ideal candidate for classical biological control in Argentina. Biological control of Tamarix spp. has been rapid and highly successful in the USA after the introduction of four Diorhabda spp. (Coleoptera: Chrysomelidae). Biological control of Tamarix spp. in Argentina could be implemented easily, rapidly, and at a low cost by utilizing the information developed in the USA.

The Brazilian Peppertree ThripsPseudophilothrips ichini(Thysanoptera: Phlaeothripidae) as a Biological Control Agent: A Reappraisal of the Timeline of Events and Attribution of Credit

Summary The thrips Pseudophilothrips ichini (Hood) (Thysanoptera: Phlaeothripidae), which is native to Brazil, is a candidate for classical biological control of the invasive Brazilian peppertree, Schinus terebinthifolia Raddi (Sapindales: Anacardiaceae), in the USA. This paper corrects errors of omission about the history of the Brazilian peppertree biological control program in Florida and several misstatements about the identity of the thrips in previously published literature.

Determining the host specificity of the biological control agent Trichomalus perfectus (Hymenoptera: Pteromalidae): the importance of ecological host range

We determined the host range of the parasitoid Trichomalus perfectus (Walker), a candidate for classical biological control of cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham), an important pest of canola in Canada. Studies were conducted in Europe and in North America. In laboratory experiments, the levels of parasitism (acceptance) of Ceutorhynchus turbatus Schultze, C. cardariae Korotyaev, C. omissus Fall and C. querceti (Gyllenhal) by T. perfectus were not significantly different than of the target host C. obstrictus. Although C. typhae (Herbst), C. pallidactylus (Marsham), C. americanus Buchanan, C. neglectus Blatchely and Ceutorhynchus sp. nr. nodipennis were parasitised by T. perfectus, the levels of parasitism were significantly lower on these species than on C. obstrictus. Ceutorhynchus peyerimhoffi Hustache, C. erysimi (Fabricius), C. alliariae H. Brisout, C. roberti Gyllenhal, Mogulones borraginis (Fabricius), Mononychus vulpeculus (Fabricius) and the leaf-mining fly Scaptomyza flava (Fallén) were not attacked. Ecological host range surveys in Europe corroborated the prediction that T. perfectus would attack C. cardariae at similar rates to C. obstrictus. In North America, the recent discovery of T. perfectus in a C. omissus population suggests that laboratory findings predicting that C. omissus is a preferred host may be the case in the field. We found that T. perfectus attacks larvae of some Ceutorhynchus spp. feeding on Brassicaceae and does not attack species outside of that host range. Thus, the parasitoid can be defined as narrowly oligophagous. These results demonstrate the value of ecological host range studies in the area of origin to validate hypotheses generated through laboratory host range experiments.

Predicting the distribution of Gonatocerus ashmeadi, an egg parasitoid of glassy winged sharpshooter, in New Zealand

The mymarid egg parasitoid Gonatocerus ashmeadi is a potential candidate for classical biological control of glassy winged sharpshooter (GWSS; Homalodisca vitripennis), should the pest arrive in New Zealand. However, the climate in the parasitoid's native range in the southern USA is considerably warmer than that in New Zealand, which may pose an obstacle to establishment. Although G. ashmeadi is a very effective biocontrol agent in Florida, Hawaii and Western Polynesia, it appears currently to be limited by cooler climate in central and northern California – regions that typically have climates more similar to those in New Zealand. A CLIMEX model was used to predict the survival of G. ashmeadi in New Zealand by comparison with known parameters in the USA and western Pacific Islands. The model indicates that the establishment and distribution of G. ashmeadi is likely to be limited by the climate in New Zealand, although it will probably persist in warmer parts of the North Island. These predictions indicate that biocontrol of GWSS in New Zealand using G. ashmeadi will also require active management through varying regional integrated pest management programmes. Should GWSS arrive in New Zealand, G. ashmeadi should be selected from a population that has adapted to cooler parts of California. However, such a population is not known at present, so preventing GWSS from establishing in New Zealand remains a crucial strategy.

Endophytic fungi associated with Fallopia japonica (Polygonaceae) in Japan and their interactions with Puccinia polygoni-amphibii var. tovariae, a candidate for classical biological control

Fallopia japonica (Polygonaceae), or Japanese knotweed, is now spreading globally, causing serious problems in Europe and North America in both natural and urban habitats. There is an urgent need for alternative management solutions, and classical biological control, using coevolved natural enemies found in the native range, is currently being investigated. Here, we isolated fungal endophytes from F. japonica in Japan, its natural habitat, to find endophytes that might increase the virulence of a coevolved rust pathogen, Puccinia polygoni-amphibii var. tovariae. A total of 1581 fungal endophytes were recovered from F. japonica and classified into 15 taxa. Five genera (Colletotrichum, Pestalotiopsis, Phoma, Phomopsis, and Alternaria) were dominant as endophytes in F. japonica. A greenhouse study of the dominant endophyte–pathogen interactions revealed three types of reactions: suppressive, synergistic, and neutral. In particular, one Phomopsis isolate – closely related to Diaporthe medusaea, based on ITS sequences – promoted the pathogenic aggressiveness of P. polygoni-amphibii var. tovariae and, therefore, this interaction is potentially useful to increase the effectiveness of the rust fungus as a biological control agent of F. japonica in its invasive range.

Efficiency of Phytoseiulus longipes Evans as a control agent of Tetranychus evansi Baker & Pritchard (Acari: Phytoseiidae: Tetranychidae) on screenhouse tomatoes

The spider mite Tetranychus evansi Baker & Pritchard can cause severe damage to tomato crops. The predatory mite Phytoseiulus longipes Evans was recently reported in association with T. evansi in Uruguaiana, Rio Grande do Sul State, Brazil. The objective of the present study was to evaluate the effects of P. longipes on the population of T. evansi on tomatoes under screenhouse condition. The study consisted on four experiments, in each of which 80 potted plantlets were distributed in two plots of 40 plantlets each. Two weeks later, each plantlet of both plots was infested with eight adult females of T. evansi; one week after, four adult females of P. longipes were released onto each plant of one plot. The population levels of T. evansi and the damage caused by these mites were significantly lower (P < 0.05; linear mixed-effect model) in the plots where P. longipes had been released. The results indicate the potential of this predator as a candidate for classical biological control of T. evansi by inoculative releases on tomato plants.

Biology and Host Preferences of Cryptorhynchus melastomae (Coleoptera: Curculionidae), a Possible Biocontrol Agent for Miconia calvescens (Melastomataceae) in Hawaii

The introduced plant Miconia calvescens (Melastomataceae) poses a grave threat to Hawaii's native ecosystems and biodiversity. One potential candidate for classical biological control is Cryptorhynchus melastomae (Coleoptera: Curculionidae: Cryptorhynchinae), a stem-boring weevil from Central and South America. This weevil feeds on M. calvescens in its native Costa Rica and has been successfully reared under greenhouse conditions. Comparison of its environmental conditions in Costa Rica with those in the Miconia infested areas of Hawaii indicates the latter is a suitable habitat for C. melastomae. C. melastomae has one or two generations per year. Adults feed on new stems, petioles, leaf buds, veins, and lamina, whereas larvae mine the stem until pupation. Adults appear to prefer saplings for oviposition and feeding. Under greenhouse conditions both adults and larvae can seriously damage and kill small M. calvescens. Preliminary host testing indicates that C. melastomae may be family specific on Melastomataceae. However, because Hawaii lacks native melastomes and has many other serious melastome weeds, a family specific insect may be suitable as a biocontrol agent in this case.

Assessing host specificity of a classical biological control agent against western corn rootworm with a recently developed testing protocol

Celatoria compressa (Wulp) (Diptera: Tachinidae), a parasitoid of adult chrysomelid beetles in the subtribe Diabroticina in North America, has been selected as a candidate for classical biological control of the alien invader, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae: Galerucinae), into Europe. We conducted host specificity testing to evaluate the fundamental host range of C. compressa and potential risks to native European coleopteran species. Nine potential non-target beetles were tested for host selection with D. v. virgifera in no-choice tests, sequential no-choice tests, choice tests and sequential choice tests in small experimental arenas in a quarantine laboratory. The nine representative non-target species were selected for experimentation based on (1) ecological host range information of C. compressa, (2) ecological similarities to D. v. virgifera, (3) close phylogenetic/taxonomic relationships, (4) safeguard considerations, (5) morphological similarities, geographical distributions, overlap of temporal occurrences with D. v. virgifera and C. compressa, and (6) accessibility and availability. Of the potential nine non-target hosts tested, gravid C. compressa only parasitized a few red pumpkin beetles, Aulacophora foveicollis (Chrysomelidae: Galerucinae), regardless of the presence or absence of D. v. virgifera. However, C. compressa significantly preferred D. v. virgifera (44.6% parasitized) over A. foveicollis (2.7%) in choice tests. Of the 1110 A. foveicollis tested among all experiment types, only 23 were parasitized and only one C. compressa successfully developed from the parasitism, demonstrating that A. foveicollis is a poor host. In conclusion, C. compressa has a fundamental host range restricted to the subtribes Diabroticina and Aulacophorina, and would therefore be unlikely to have a direct impact on indigenous species in Europe.

Slender Wheatgrass is Susceptible to Smut Caused by Ustilago phrygica from Turkey.

Slender wheatgrass (Elymus trachycaulus (Link) Gould ex Shinners subsp. trachycaulus), family Poaceae, tribe Triticeae, is a native North American grass that is used as a livestock forage. Ustilago phrygica, a systemic ovary-smut fungus, is native to Turkey and West Asia and is pathogenic on Aegilops spp. and Taeniatherum caput-medusae (L.) Nevski subsp. asperum (Simonk.) Melderis (medusahead), an invasive weed in the western United States that is targeted for biological control. An isolate of the fungus (U.S. National Fungus Collections, BPI 871725; GenBank Accession No. DQ139961) was collected from medusahead in Turkey and screened for possible use in classical biological control of this weed. Screening was done in quarantine in a BSL-3 facility of the Foreign Disease-Weed Science Research Unit, USDA, ARS, Ft. Detrick, MD. The focus of screening was determination of host range of the fungus among related native and agriculturally important grasses in North America. A procedure was developed to consistently and quickly produce disease on medusahead and other grasses. Without vernalization, plants inoculated with U. phrygica will not produce smutted spikes (seedheads). Teliospores of the fungus were vacuum inoculated (1) onto caryopses (seeds) of medusahead and slender wheatgrass, which were then placed on moist germination paper in a petri dish or on moist vermiculite in plastic boxes. The dishes, sealed with Parafilm, and the boxes, covered with lids, were placed in a dark refrigerator at 3°C. After 8 weeks, all seedlings were transplanted into pots on a greenhouse bench at 22 to 25°C and 14 h light (photosynthetic photon flux density [PPFD] 620 μmol·s-1·m-2). The plants began to flower and produce smutted spikes 40 days later. These tests were repeated once. Fourteen of sixty medusahead plants from inoculated caryopses incubated on germination paper and nine of twenty-four plants from caryopses incubated on vermiculite became smutted and produced numerous smutted spikes per plant. Partial systemic infection was the norm, and all diseased plants had some spikes that were not diseased. One slender wheatgrass plant of nine plants grown from inoculated caryopses incubated on germination paper was also smutted and produced three diseased spikes. Nielsen (2) indicated susceptibility of slender wheatgrass to U. phrygica, but only as a single entry in a table under the synonym Agropyron trachycaulum (Link) Malte ex H. F. Lewis in a report on susceptibility of Aegilops spp. to U. phrygica. Because this is an obscure mention of the susceptibility of slender wheatgrass to U. phrygica, the fungus-host association does not explicitly appear in literature and is absent from relevant databases. Our tests with the fungus confirm that slender wheatgrass is susceptible to U. phrygica and lead us to conclude that the fungus would not be a good candidate for classical biological control of medusahead in North America. This formal report should establish this fungus-host association in literature and ensure reference in plant disease databases.

Morphological variation in different populations of Aceria anthocoptes (Acari: Eriophyoidea) associated with the Canada thistle, Cirsium arvense, in Serbia

The russet mite, Aceria anthocoptes (Nal.), is the only eriophyid that has been recorded on Canada thistle, Cirsium arvense (L.) Scop. It has been noted in several European countries and recently in the USA. With its apparent host specificity and because of the damage it causes to its host plant, A. anthocoptes is being studied as a potential candidate for classical biological control. The aim of the present study was to examine quantitative morphological traits in four populations of A. anthocoptes living on two infraspecific host plant taxa (C. arvense var. arvense and C. arvense var. vestitum) in two geographically separate areas of Serbia in order to test the hypothesis of absence of the possible host plant impact on mite morphology. MANOVA analysis revealed significant differences between populations from different localities in Serbia. Populations of A. anthocoptes inhabiting two thistle varieties in the vicinity of Belgrade differed significantly from mites inhabiting the same two host varieties in the vicinity of the town of Ivanjica. Canonical discriminant analysis showed that the trait which best discriminates the populations of A. anthocoptes is the number of dorsal annuli. It was not possible to ascribe morphological differences to the impact of the host plant.

Supplementary host specificity testing of the sawfly Heteroperryia hubrichi, a candidate for classical biological control of Brazilian peppertree, Schinus terebinthifolius, in the USA

Supplementary host specificity tests were conducted with the defoliating sawfly Heteroperreyia hubrichi (Hymenoptera: Pergidae), a candidate for classical biological control of Brazilian peppertree, Schinus terebinthifolius (Sapindales: Anacardiaceae), in the United States. These tests were conducted as part of the environmental assessment required by the National Environmental Policy Act (NEPA). The suitability of the federally listed endangered native plant Rhus michauxii (Anacardiaceae) and the economically important Litchi chinensis (Sapindaceae) as potential host plants for H. hubrichi was evaluated in a series of no-choice larval development tests conducted in a Florida quarantine laboratory. Neonate larvae transferred to individual test plants failed to develop to the pupal stage on R. michauxii or L. sinensis, whereas Brazilian peppertree supported development of the sawfly to pupation. The results of the additional host specificity tests indicated these critical non-target plants are not at risk from attack by H. hubrichi if it were released in Florida, USA.