Biological Control of Halyomorpha halys with Special Emphasis on Parasitoids

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Pest and Vector Management".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 40881

Special Issue Editors

CREA, Research Centre for Plant Protection and Certification, 50125 Firenze, Italy
Interests: entomology; integrated pest management; biological control; invasive insect species
Florida Department of Agriculture and Consumer Services, Gainesville, FL 32608, USA
Interests: systematics of Platygastroidea; parasitoids of stink bug eggs
Beneficial Insects Introduction Research Unit, USDA-ARS, Newark, DE, USA
Interests: entomology; biological control; invasive species

Special Issue Information

Dear Colleagues,

Halyomorpha halys is a destructive agricultural pest of East Asian origin. Damages on fruits and vegetables are severe, and control methods are generally biased toward chemical pesticides. This approach rarely leads to satisfactory pest control and often disrupts IPM strategies. Biological control, especially with egg parasitoids, is considered one of the most viable long-term solutions. In many regions of the world, classical or augmentative biological control by exotic and native parasitoid species is actively under investigation. Moreover, adventive populations parasitoids associated with brown marmorated stink bug (BMSB) eggs have been discovered in North America and Europe, emphasizing the need for a cosmopolitan perspective for solving this pest problem.

This Special Issue welcomes papers on various aspects of the biological control of H. halys, in particular with parasitoids.

Dr. Giuseppino Sabbatini-Peverieri
Dr. Elijah Talamas
Dr. Kim A. Hoelmer
Guest Editors

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Keywords

  • agricultural pest
  • parasitoid complex
  • natural enemy
  • Trissolcus

Published Papers (14 papers)

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Research

15 pages, 3185 KiB  
Article
Hyperparasitism of Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) on Two Biological Control Agents of Halyomorpha halys
by Alberto Mele, Davide Scaccini and Alberto Pozzebon
Insects 2021, 12(7), 617; https://doi.org/10.3390/insects12070617 - 08 Jul 2021
Cited by 4 | Viewed by 2447
Abstract
Halyomorpha halys (Stål) is an invasive Asian pest that causes severe crop losses on various crops. Nowadays, management strategies against this pest mainly rely on pesticide use, but biological control with egg parasitoids is considered the most promising long-term and sustainable solution. Trissolcus [...] Read more.
Halyomorpha halys (Stål) is an invasive Asian pest that causes severe crop losses on various crops. Nowadays, management strategies against this pest mainly rely on pesticide use, but biological control with egg parasitoids is considered the most promising long-term and sustainable solution. Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) are Asian egg parasitoids already present in Europe and are the most effective biological control agents of H. halys. Therefore, these two species are considered for biological control programs in Europe and other parts of the world. Acroclisoides sinicus (Huang and Liao) is a pteromalid parasitoid wasp that frequently emerged from H. halys egg masses collected in northern Italy. This species has been hypothesized to be a hyperparasitoid of Trissolcus spp. parasitoids. This study was carried out under laboratory conditions where A. sinicus was tested in no-choice and two-choice experiments to assess the host preference between T. japonicus and T. mitsukurii. Olfactory responses of A. sinicus from volatiles emitted from different potential hosts were also tested. In all trials, A. sinicus showed a clear preference for parasitizing H. halys eggs previously parasitized by T. mitsukurii compared to T. japonicus. In no-choice experiments, the impact of the hyperparasitoid on T. japonicus was low, showing an exploitation rate of 4.0%, while up to a 96.2% exploitation rate was observed on T. mitsukurii. Acroclisoides sinicus was also attracted by volatiles emitted by egg masses parasitized by T. mitsukurii, while no response was observed to egg masses parasitized by T. japonicus or not parasitized. Therefore, according to the results obtained here, A. sinicus could limit the population development of T. mitsukurii, while lesser effects are expected on T. japonicus. Full article
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15 pages, 898 KiB  
Article
Preempting the Arrival of the Brown Marmorated Stink Bug, Halyomorpha halys: Biological Control Options for Australia
by Valerie Caron, Tania Yonow, Cate Paull, Elijah J. Talamas, Gonzalo A. Avila and Kim A. Hoelmer
Insects 2021, 12(7), 581; https://doi.org/10.3390/insects12070581 - 28 Jun 2021
Cited by 9 | Viewed by 3080
Abstract
The brown marmorated stink bug Halyomorphahalys (Stål) (Hemiptera: Pentatomidae) is native to Northeast Asia, but has become a serious invasive species in North America and Europe, causing major damage to crops. While it has not established itself in Australia, it has been [...] Read more.
The brown marmorated stink bug Halyomorphahalys (Stål) (Hemiptera: Pentatomidae) is native to Northeast Asia, but has become a serious invasive species in North America and Europe, causing major damage to crops. While it has not established itself in Australia, it has been intercepted at the border several times, indicating that future incursions and establishment are a case of when, not if. Biological control is one of the few control options for this species and will be important for managing H.halys should it become established in Australia. Prioritizing species that could be used as biological control agents would ensure Australia is prepared. This study summarizes the literature on natural enemies of H. halys in its native and invaded ranges and prioritizes potential biological control agents of H.halys that could be used in Australia. Two egg parasitoid species were identified: Trissolcusjaponicus (Ashmead) and Trissolcusmitsukurii (Ashmead) (Hymenoptera: Scelionidae). Future efforts to develop biological control should focus on T. mitsukurii, as it is already present in Australia. However, little is known about this species and further work is required to: (1) assess its potential effectiveness in parasitizing H. halys, (2) determine its current distribution and (3) host range in Australia. Full article
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15 pages, 4299 KiB  
Article
Native and Non-Native Egg Parasitoids Associated with Brown Marmorated Stink Bug (Halyomorpha halys [Stål, 1855]; Hemiptera: Pentatomidae) in Western Slovenia
by Mojca Rot, Lara Maistrello, Elena Costi, Iris Bernardinelli, Giorgio Malossini, Luca Benvenuto and Stanislav Trdan
Insects 2021, 12(6), 505; https://doi.org/10.3390/insects12060505 - 31 May 2021
Cited by 24 | Viewed by 3380
Abstract
Halyomorpha halys (Hemiptera: Pentatomidae), native to East Asia, has become a globally invasive pest, as a serious threat to agricultural production and a notorious nuisance pest in urban areas. Considerable efforts have been made so far to develop effective pest control measures to [...] Read more.
Halyomorpha halys (Hemiptera: Pentatomidae), native to East Asia, has become a globally invasive pest, as a serious threat to agricultural production and a notorious nuisance pest in urban areas. Considerable efforts have been made so far to develop effective pest control measures to prevent crop damage. Biological control of this invasive stink bug by egg parasitoids has proven to be the most environmentally sustainable long-term solution. Knowledge of the native egg parasitoid fauna is of key importance when implementing a biological control program. Therefore, the main objective of our study was to detect egg parasitoid species associated with H. halys in the Goriška region (Western Slovenia) and to evaluate their impact on the pest population under field conditions. In the years 2019 and 2020, around 4600 H. halys eggs were collected in the wild and more than 3400 sentinel eggs were exposed to detect parasitoids in the field. Five egg-parasitoid species emerged from H. halys eggs: Anastatus bifasciatus (Hymenoptera: Eupelmidae), Telenomus sp., Trissolcus basalis, Trissolcus mitsukurii (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Hymenoptera: Encyrtidae), all of them are new records for Slovenia. The native species, An. bifasciatus, dominated in urban and suburban areas, while non-native Tr. mitsukurii prevailed in agricultural areas. Overall parasitism rates of naturally laid eggs by the parasitoid species complex in 2019 and 2020 was 3.0 and 14.4%, respectively. Rapid recruitment of native parasitoids, early detection of an effective alien parasitoid species and increasing overall parasitism rates are very encouraging results, which need to be followed and verified in future research. Full article
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30 pages, 62078 KiB  
Article
Modelling the Potential Geographic Distribution of Two Trissolcus Species for the Brown Marmorated Stink Bug, Halyomorpha halys
by Tania Yonow, Darren J. Kriticos, Noboru Ota, Gonzalo A. Avila, Kim A. Hoelmer, Huayan Chen and Valerie Caron
Insects 2021, 12(6), 491; https://doi.org/10.3390/insects12060491 - 25 May 2021
Cited by 16 | Viewed by 3518
Abstract
The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is native to northeast Asia. It was accidentally introduced to Europe and North America, where it has become a key pest, feeding on many important crops. Previous eco-climatic niche modelling indicates that H. [...] Read more.
The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is native to northeast Asia. It was accidentally introduced to Europe and North America, where it has become a key pest, feeding on many important crops. Previous eco-climatic niche modelling indicates that H. halys could expand its distribution vastly, and numerous border interceptions of this pest in many countries, including Australia and New Zealand, indicate that it would be prudent to prepare for its eventual arrival. Similar niche modelling was used to assess the potential distribution of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), the key parasitoid of H. halys in China. Trissolcus mitsukurii (Ashmead) is one of the main parasitoids of H. halys in Japan. It is known to have existed in Australia since the early 20th century and was also specifically introduced to Australia in the 1960s, and it has now also invaded Italy. We used CLIMEX to model the climatic niche of T. mitsukurii to estimate its global potential distribution. We found that T. mitsukurii should be able to significantly expand its range globally, and that there is a significant degree of overlap in the projected ranges of T. mitsukurii, T. japonicus and H. halys. From a biological control perspective, this implies that the two Trissolcus species may be able to help mitigate the potential impacts of H. halys. Full article
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15 pages, 1551 KiB  
Article
Molecular Identification of Trissolcus japonicus, Parasitoid of the Brown Marmorated Stink Bug, by Species-Specific PCR
by Maple N. Chen, Ricardo D. Santander, Elijah J. Talamas, Peter J. Jentsch, Marie-Claude Bon and Srđan G. Aćimović
Insects 2021, 12(5), 467; https://doi.org/10.3390/insects12050467 - 18 May 2021
Cited by 4 | Viewed by 2826
Abstract
The samurai wasp, Trissolcus japonicus (Ashmead), has been proposed as a biocontrol agent against brown marmorated stink bugs (BMSB), due to its ability to parasitize and kill BMSB eggs. However, the wasps’ small size makes it challenging for those untrained in morphological identification [...] Read more.
The samurai wasp, Trissolcus japonicus (Ashmead), has been proposed as a biocontrol agent against brown marmorated stink bugs (BMSB), due to its ability to parasitize and kill BMSB eggs. However, the wasps’ small size makes it challenging for those untrained in morphological identification to determine the wasps’ species. To circumvent this problem, a molecular method was created to identify T. japonicus. The method uses species-specific primers, designed in this study, which target the variable region of the mitochondrial Cytochrome Oxidase 1 (CO1) locus. After confirming successful DNA extraction from samples, the PCR amplification using our primers produced 227-bp PCR products for all T. japonicus specimens and no amplification in other microhymenoptera candidates. Additionally, DNA from BMSB-parasitized eggs gave positive PCR amplification, while the control BMSB samples showed no amplification. This indicates that PCR with our primers specifically and sensitively differentiates T. japonicus specimens from other similar wasp species and discriminates between T. japonicus-parasitized and non-parasitized BMSB eggs. Finally, an in silico analysis of CO1 sequences demonstrated that our primers match the sequences of four different haplotypes of T. japonicus, indicating that our diagnostic method could potentially be applied to analyze T. japonicus populations throughout North America, Europe, and parts of Asia. Full article
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14 pages, 1057 KiB  
Article
Trissolcus kozlovi in North Italy: Host Specificity and Augmentative Releases against Halyomorpha halys in Hazelnut Orchards
by Silvia Teresa Moraglio, Francesco Tortorici, Sara Visentin, Marco Giuseppe Pansa and Luciana Tavella
Insects 2021, 12(5), 464; https://doi.org/10.3390/insects12050464 - 18 May 2021
Cited by 7 | Viewed by 3042
Abstract
Trissolcus kozlovi (Hymenoptera: Scelionidae) emerged from field-laid eggs of Halyomorpha halys (Hemiptera: Pentatomidae) in North Italy, and it emerged in significantly higher numbers from fresh H. halys eggs compared to other native scelionids. Since few data on T. kozlovi are available, its host-specificity [...] Read more.
Trissolcus kozlovi (Hymenoptera: Scelionidae) emerged from field-laid eggs of Halyomorpha halys (Hemiptera: Pentatomidae) in North Italy, and it emerged in significantly higher numbers from fresh H. halys eggs compared to other native scelionids. Since few data on T. kozlovi are available, its host-specificity and some biological traits were investigated in laboratory tests, and its impact after augmentative releases was evaluated in two hazelnut orchards. Among the 12 tested bug species (Hemiptera: Pentatomidae, Scutelleridae), only Nezara viridula was an unsuitable host, while the highest offspring proportions were obtained from Arma custos, Pentatoma rufipes, and Peribalus strictus, followed by Acrosternum heegeri and Palomena prasina. Furthermore, when reared on P. strictus, T. kozlovi showed a high longevity as well as a high adaptation to H. halys eggs. In both hazelnut orchards, T. kozlovi emerged from H. halys eggs after field releases, but it was not found in the next two years. The physiological host range of T. kozlovi was quite similar to that of T. japonicus, and probably T. kozlovi has just begun to attack H. halys as a new host. This aspect needs to be further investigated, as well as its favorable environmental conditions, its distribution and also its possible interaction with T. japonicus, currently present in Italy. Full article
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14 pages, 1287 KiB  
Article
Seasonal Abundance and Diversity of Egg Parasitoids of Halyomorpha halys in Kiwifruit Orchards in China
by Gonzalo A. Avila, Juhong Chen, Wenjing Li, Maryam Alavi, Qianqian Mi, Manoharie Sandanayaka, Feng Zhang and Jinping Zhang
Insects 2021, 12(5), 428; https://doi.org/10.3390/insects12050428 - 10 May 2021
Cited by 6 | Viewed by 2190
Abstract
To develop effective and targeted biocontrol tactics for the brown marmorated stink bug, Halyomorpha halys, in crop habitats, a good understanding is essential of the abundance and diversity of its parasitoids in different crop habitats in its native range. To obtain information on [...] Read more.
To develop effective and targeted biocontrol tactics for the brown marmorated stink bug, Halyomorpha halys, in crop habitats, a good understanding is essential of the abundance and diversity of its parasitoids in different crop habitats in its native range. To obtain information on the egg parasitoid communities of H. halys in kiwifruit, surveys using sentinel egg masses were conducted in 2018 and 2019. These assessed the species composition of egg parasitoids of H. halys in green-fleshed ‘Hayward’ kiwifruit orchards, and quantified their season-long abundances in orchards under two different management systems. Parasitism was observed from June to August 2018 (mean parasitism: 48%) and from May to August 2019 (mean parasitism: 29%) across the experimental orchards. In total, five different parasitoid species were found across the two surveys seasons in the kiwifruit orchards, Trissolcus japonicus, T. cultratus, T. plautiae, Anastatus japonicus, and Acroclisoides sp., where T. japonicus and T. cultratus were the predominant species. Monthly T. japonicus abundance data had a unimodal distribution in 2018, peaking in July. There were two peaks (May–June and August) in the 2019 season. Overall, T. japonicus was significantly more abundant in the organic orchard than the conventionally managed orchard only in 2018, and its monthly abundance differed significantly in the two orchards in the two survey seasons. Results and their implications for future classical biological control for H. halys in kiwifruit are discussed. Full article
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12 pages, 6645 KiB  
Article
Add Germany to the List—Adventive Population of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) Emerges in Germany
by Christine Dieckhoff, Sophie Wenz, Maura Renninger, Anne Reißig, Helmut Rauleder, Claus P. W. Zebitz, Jana Reetz and Olaf Zimmermann
Insects 2021, 12(5), 414; https://doi.org/10.3390/insects12050414 - 04 May 2021
Cited by 20 | Viewed by 3157
Abstract
The brown marmorated stink bug, Halyomorpha halys, is a polyphagous pest species of worldwide economic importance. Since the mid-1990s, it has invaded and become established in various countries outside its native Asian range. In the newly invaded areas, biological control by native [...] Read more.
The brown marmorated stink bug, Halyomorpha halys, is a polyphagous pest species of worldwide economic importance. Since the mid-1990s, it has invaded and become established in various countries outside its native Asian range. In the newly invaded areas, biological control by native natural enemies has been shown to be insufficient in the long-term control of this severe pest. Adventive populations of Trissolcus japonicus, an important biological control agent of H. halys in Asia, have been reported from North America and some European countries since the mid-2010s. This egg parasitoid species seems to follow in the wake of the establishment of H. halys populations outside their native Asian range. Here, we report the first discovery of an adventive population of T. japonicus in Germany. In 2020, adult T. japonicus were recovered from parasitized H. halys egg masses (naturally laid and sentinel egg masses) and collected in ruderal areas using an insect suction sampler. The arrival of T. japonicus in Germany, unintentional through pathways yet unknown, corroborates a northbound expansion of its range within Europe. Further field surveys will show the extent of its dispersal and establishment capacities within this new distribution area. Full article
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11 pages, 1035 KiB  
Article
Survey for Adventive Populations of the Samurai Wasp, Trissolcus japonicus (Hymenoptera: Scelionidae) in Pennsylvania at Commercial Fruit Orchards and the Surrounding Forest
by Hillary M. Peterson, Elijah Talamas and Grzegorz Krawczyk
Insects 2021, 12(3), 258; https://doi.org/10.3390/insects12030258 - 19 Mar 2021
Cited by 7 | Viewed by 3218
Abstract
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. [...] Read more.
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. Full article
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12 pages, 2156 KiB  
Article
Seasonal Captures of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) and the Effects of Habitat Type and Tree Species on Detection Frequency
by Nicole F. Quinn, Elijah J. Talamas, Tracy C. Leskey and J. Christopher Bergh
Insects 2021, 12(2), 118; https://doi.org/10.3390/insects12020118 - 29 Jan 2021
Cited by 9 | Viewed by 1998
Abstract
Trissolcus japonicus, an important egg parasitoid of Halyomorpha halys in Asia, was first detected in the USA in 2014. To evaluate the effect of habitat and the seasonality of T. japonicus detections in the USA, yellow sticky traps were placed in the [...] Read more.
Trissolcus japonicus, an important egg parasitoid of Halyomorpha halys in Asia, was first detected in the USA in 2014. To evaluate the effect of habitat and the seasonality of T. japonicus detections in the USA, yellow sticky traps were placed in the canopy of Ailanthus altissima growing at the edge of isolated patches of trees, windbreaks, and woodlots in northern Virginia in 2018 and 2019. In both years, captures occurred from May to September, and peaked in July and August. While T. japonicus was detected in all habitats, there was not a consistent effect of habitat type on capture frequency. To evaluate tree species effects on T. japonicus captures, in 2017 and 2018, yellow sticky traps deployed in the canopy of A. altissima bordering apple orchards were paired with a nearby trap in one of several wild tree species along a common woods edge. In 2019, these traps were deployed in A. altissima, black walnut, and black locust growing in the same windbreaks. No consistent association between captures of T. japonicus or native parasitoids of H. halys and the tree species sampled was observed among years. Results are discussed in relation to the ecology and sampling optimization of T. japonicus. Full article
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12 pages, 881 KiB  
Article
Integrating Trissolcus japonicus (Ashmead, 1904) (Hymenoptera: Scelionidae) into Management Programs for Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Apple Orchards: Impact of Insecticide Applications and Spray Patterns
by Dalton C. Ludwick, Jessica Patterson, Layne B. Leake, Lee Carper and Tracy C. Leskey
Insects 2020, 11(12), 833; https://doi.org/10.3390/insects11120833 - 26 Nov 2020
Cited by 4 | Viewed by 2144
Abstract
Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) is an invasive species in the United States, where it has caused significant damage to specialty crops, including apples. While integrated pest management techniques have been developed for H. halys in apple, including spray application techniques, it [...] Read more.
Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) is an invasive species in the United States, where it has caused significant damage to specialty crops, including apples. While integrated pest management techniques have been developed for H. halys in apple, including spray application techniques, it is unknown how these techniques affect foraging, adventive Trissolcus japonicus (Ashmead, 1904) (Hymenoptera: Scelionidae), and its offspring. In this study, egg masses (unparasitized and 2 and 7 day parasitized pre-treatment) were placed in apple orchards in treated and untreated locations that received full block insecticide applications or reduced application techniques, including border row or alternate row middle applications. Bifenthrin, thiamethoxam + λ-cyhalothrin, clothianidin, and methomyl were evaluated. Egg masses were retrieved 24 h after spray applications. For 2 and 7 day parasitized pre-treatment, adult T. japonicus emergence was recorded from each egg mass. For unparasitized egg masses, T. japonicus females were given 24 h to forage and oviposit on post-treatment egg masses with female survivorship, and adult emergence from egg masses was recorded. Female survivorship was significantly lower on post-treatment egg masses retrieved from areas receiving bifenthrin applications. Emergence from post-treatment egg masses was affected by thiamethoxam + λ-cyhalothrin, bifenthrin, and methomyl in some treated areas, whereas less impact was observed on 2 and 7 day pre-treatment parasitized egg masses in general. These data provide further insights into H. halys management and the potential impact of T. japonicus in sprayed orchard agroecosystems. Full article
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23 pages, 2034 KiB  
Article
Hidden Host Mortality from an Introduced Parasitoid: Conventional and Molecular Evaluation of Non-Target Risk
by James R. Hepler, Kacie Athey, David Enicks, Paul K. Abram, Tara D. Gariepy, Elijah J. Talamas and Elizabeth Beers
Insects 2020, 11(11), 822; https://doi.org/10.3390/insects11110822 - 23 Nov 2020
Cited by 9 | Viewed by 2554
Abstract
Hidden trophic interactions are important in understanding food web ecology and evaluating the ecological risks and benefits associated with the introduction of exotic natural enemies in classical biological control programs. Although non-target risk is typically evaluated based on evidence of successful parasitism, parasitoid-induced [...] Read more.
Hidden trophic interactions are important in understanding food web ecology and evaluating the ecological risks and benefits associated with the introduction of exotic natural enemies in classical biological control programs. Although non-target risk is typically evaluated based on evidence of successful parasitism, parasitoid-induced host mortality not resulting in visible evidence of parasitism (i.e., nonreproductive effects) is often overlooked. The adventive establishment of Trissolcus japonicus, an exotic parasitoid of the introduced stink bug Halyomorpha halys, provides an opportunity to investigate the total impact of this parasitoid on target and non-target hosts in the field. We developed a new methodology to measure nonreproductive effects in this system, involving a species-specific diagnostic PCR assay for T. japonicus. We applied this methodology to field-deployed eggs of four pentatomid species, coupled with traditional rearing techniques. Nonreproductive effects were responsible for the mortality of an additional 5.6% of H. halys eggs due to T. japonicus, and were even more substantial in some of the non-target species (5.4–43.2%). The observed hidden mortality of native non-target species from an introduced parasitoid could change predictions about direct and indirect ecological interactions and the efficacy of biological control of the target pest. Full article
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15 pages, 2199 KiB  
Article
Rearing Trissolcus japonicus and Trissolcus mitsukurii for Biological Control of Halyomorpha halys
by Giuseppino Sabbatini-Peverieri, Christine Dieckhoff, Lucrezia Giovannini, Leonardo Marianelli, Pio Federico Roversi and Kim Hoelmer
Insects 2020, 11(11), 787; https://doi.org/10.3390/insects11110787 - 11 Nov 2020
Cited by 19 | Viewed by 3016
Abstract
Halyomorpha halys is a severe agricultural pest of Asian origin that has invaded many countries throughout the world. Pesticides are currently the favored control methods, but as a consequence of their frequent use, often disrupt Integrated Pest Management. Biological control with egg parasitoids [...] Read more.
Halyomorpha halys is a severe agricultural pest of Asian origin that has invaded many countries throughout the world. Pesticides are currently the favored control methods, but as a consequence of their frequent use, often disrupt Integrated Pest Management. Biological control with egg parasitoids is seen as the most promising control method over the long-term. Knowledge of the reproductive biology under laboratory conditions of the most effective candidates (Trissolcus japonicus and Trissolcus mitsukurii) for optimizing production for field releases is strongly needed. Rearing of these egg parasitoids was tested by offering three different host supply regimes using new emerged females and aged, host-deprived females in different combinations. Results showed a mean progeny per female ranging from 80 to 85 specimens for T. japonicus and from 63 to 83 for T. mitsukurii. Sex ratios were strongly female biased in all combinations and emergence rates exceeded 94% overall. Cumulative curves showed that longer parasitization periods beyond 10–14 days (under the adopted rearing regimes) will not lead to a significantly increase in progeny production. However, ageing females accumulate eggs in their ovaries that can be quickly laid if a sufficient number of host eggs are supplied, thus optimizing host resources. Our data showed that offering H. halys egg masses to host-deprived female Trissolcus once a week for three weeks allowed its eggs to accumulate in the ovary, providing the greatest number of offspring within a three week span. Full article
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8 pages, 576 KiB  
Communication
A Newly Reported Parasitoid, Pentatomophaga latifascia (Diptera: Tachinidae), of Adult Halyomorpha halys in Beijing, China
by Juhong Chen, Wenjing Li, Qianqian Mi, Feng Zhang, Shusen Shi and Jinping Zhang
Insects 2020, 11(10), 666; https://doi.org/10.3390/insects11100666 - 29 Sep 2020
Cited by 9 | Viewed by 2790
Abstract
Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a serious pest in agriculture and forests, as both adults and nymphs feed by piercing the surface of the plant and fruit tissues, causing damage. The eggs of H. halys are commonly attacked by parasitoids, however, the [...] Read more.
Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a serious pest in agriculture and forests, as both adults and nymphs feed by piercing the surface of the plant and fruit tissues, causing damage. The eggs of H. halys are commonly attacked by parasitoids, however, the nymph and the adult are rarely attacked by natural enemies. We surveyed the parasitoids of adult H. halys by collecting samples from overwintering populations at three different locations and checked their body surfaces for the presence of tachinid eggs. Any host adults carrying tachinid eggs were reared in a cage for further species identification. We found that the eggs of Pentatomophaga latifascia (Villeneuve) (Diptera: Tachinidae) were laid on the surface of H. halys, and the hatched larvae penetrated the host body and fed internally to develop. The last larval instar emerged from the host to develop into pupae, killing the host in the process. According to the field survey, the average parasitism of H. halys by P. latifascia was 2.42%. The parasitoids of adult H. halys in their native range have so far been little studied and may provide a complementary component of egg parasitoids for biological control against H. halys in invaded areas. Full article
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