Assemblage of the Egg Parasitoids of the Invasive Stink Bug Halyomorpha halys: Insights on Plant Host Associations

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an invasive alien species and a key agricultural pest. Its native parasitoids (Trissolcus japonicus Ashmead and Tr. mitsukurii Ashmead) have been registered in several countries where H. halys brought dramatic economic losses and where biological control is considered to be the most effective long-term solution. By searching for stink bug egg masses and exposing sentinel egg masses, we monitored the distribution of native and exotic egg parasitoids in Trentino-Alto Adige (Italy), an area where both the host and parasitoids are in expansion. We recorded ten pentatomids, seven parasitoid species, with the first report of Tr. japonicus in this area and a hyperparasitoid. In the assemblage, Anastatus bifasciatus (Geoffroy) and Tr. mitsukurii were the dominant parasitoids, with a different distribution in terms of context and host plants. Sycamore was the host plant where the highest number of naturally laid parasitized egg masses (26%) were recorded. Trissolcus mitsukurii showed the highest parasitism rate, and was often found in apple orchards. The emergence of exotic parasitoids showed a temporal delay compared to native ones. Sequence analysis of 823 bp of the CO1 mitochondrial gene revealed that the recovered Tr. japonicus and Tr. mitsukurii harbored one single haplotype each. These haplotypes were previously found in 2018 in Northern Italy. While sentinel egg masses proved to be very effective in tracking the arrival of exotic Trissolcus species, the collection of stink bug egg masses provided fundamental data on the plant host species. The results lend strong support to the adaptation of exotic Trissolcus species to the environmental conditions of the range of introduction, providing new information on plant host-associations, fundamental for the development of biological control programs.

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Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys (Stål) in Mid-Atlantic USA ornamental landscapes

Biological Control ◽

10.1016/j.biocontrol.2016.07.011 ◽

2016 ◽

Vol 103 ◽

pp. 11-20 ◽

Cited By ~ 41

Author(s):

Mary L. Cornelius ◽

Christine Dieckhoff ◽

Kim A. Hoelmer ◽

Richard T. Olsen ◽

Donald C. Weber ◽

...

Keyword(s):

Biological Control ◽

Halyomorpha Halys ◽

Stink Bug ◽

Egg Masses ◽

Exotic Invasive

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Potentials of some entomopathogens against the brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae)

Egyptian Journal of Biological Pest Control ◽

10.1186/s41938-019-0176-y ◽

2019 ◽

Vol 29 (1) ◽

Author(s):

Elif Tozlu ◽

Islam Saruhan ◽

Göksel Tozlu ◽

Recep Kotan ◽

Fatih Dadaşoğlu ◽

...

Keyword(s):

Biological Control ◽

Chemical Control ◽

Mortality Rates ◽

Fungal Isolate ◽

Economic Losses ◽

Halyomorpha Halys ◽

Pest Species ◽

Brown Marmorated Stink Bug ◽

Stink Bug ◽

Bacterial Isolates

AbstractThe brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae), is an invasive harmful pest species due to its economic losses. Its wide host range and continuous movement make its control difficult with insecticides. Biological control has recently gained importance due to the negative aspects of chemical control. The study evaluated the biological control tools by testing the entomopathogens against the pest by 11 bacteria strains and 1 fungal isolate. Brevibacillus, Bacillus, Pantoea, Vibrio, Pseudomonas, and Beauveria were tested against the nymphs of H. halys under controlled conditions. All applied entomopathogens had potentials for controlling H. halys. Mortality rates of 75 and 100% were obtained by the bacteria strains and 76.19% by the fungus, B. bassiana. Successfully reaching a 100% control rate, the bacterial isolates of the Bacillus cereus GC subgroup B and Pantoea agglomerans GC subgroup were recorded to have a greater potential than the others.

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Hyperparasitism of Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) on Two Biological Control Agents of Halyomorpha halys

Insects ◽

10.3390/insects12070617 ◽

2021 ◽

Vol 12 (7) ◽

pp. 617

Author(s):

Alberto Mele ◽

Davide Scaccini ◽

Alberto Pozzebon

Keyword(s):

Biological Control ◽

Management Strategies ◽

Parasitoid Wasp ◽

Choice Experiments ◽

Egg Parasitoids ◽

Halyomorpha Halys ◽

Biological Control Agents ◽

Egg Masses ◽

Exploitation Rate ◽

The Impact

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.

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Surveys in northern Utah for egg parasitoids of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) detect Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae)

Biodiversity Data Journal ◽

10.3897/bdj.8.e53363 ◽

2020 ◽

Vol 8 ◽

Author(s):

Mark Holthouse ◽

Zachary Schumm ◽

Elijah Talamas ◽

Lori Spears ◽

Diane Alston

Keyword(s):

Biological Control ◽

North America ◽

Native Species ◽

Insect Pest ◽

Egg Parasitoids ◽

Halyomorpha Halys ◽

Wasp Species ◽

Egg Masses ◽

Trissolcus Japonicus ◽

Northern Utah

The highly polyphagous and invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has become a significant insect pest in North America since its detection in 1996. It was first documented in northern Utah in 2012 and reports of urban nuisance problems and plant damage have since increased. Biological control is the preferred solution to managing H. halys in North America and other invaded regions due to its alignment with integrated pest management and sustainable practices. Native and non-native biological control agents, namely parasitoid wasps, have been assessed for efficacy. Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is an effective egg parasitoid of H. halys in its native range of southeast Asia and has recently been documented parasitising H. halys eggs in North America and Europe. Field surveys for native and exotic egg parasitoids using wild (in situ) and lab-reared H. halys egg masses were conducted in suburban and agricultural sites in northern Utah from June to September 2017–2019. Seven native wasp species in the families Eupelmidae and Scelionidae were discovered guarding H. halys eggs and adult wasps from five of these species completed emergence. Native species had low mean rates of adult emergence from wild (0.5–3.7%) and lab-reared (0–0.4%) egg masses. In 2019, an adventive population of T. japonicus was discovered for the first time in Utah, emerging from 21 of the 106 wild H. halys egg masses found that year, and none from lab-reared eggs. All T. japonicus emerged from egg masses collected on Catalpa speciosa (Warder). Our results support other studies that have observed biological control of H. halys from T. japonicus and improved parasitoid wasp detection with wild as compared to lab-reared H. halys egg masses.

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First Report of Native Parasitoids of Halyomorpha halys (Hemiptera: Pentatomidae) in Greece

Insects ◽

10.3390/insects12110984 ◽

2021 ◽

Vol 12 (11) ◽

pp. 984

Author(s):

Stefanos S. Andreadis ◽

Nikoloz E. Gogolashvili ◽

Georgios T. Fifis ◽

Emmanouel I. Navrozidis ◽

Thomas Thomidis

Keyword(s):

Biological Control ◽

Crop Production ◽

Egg Parasitoids ◽

Halyomorpha Halys ◽

Green Beans ◽

Northern Greece ◽

Egg Masses ◽

Control Programs ◽

Native Parasitoids ◽

Wide Range

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an endemic species of East Asia; it was introduced into Europe in 2007. It has a wide range of hosts as it feeds on over 170 host plant species and significantly impacts crop production. In Greece, H. halys causes significant losses in the production of kiwi, peaches, and green beans; thus, control of this species (including biological control) is essential. Here, we focus on the potential impact of native natural enemies of H. halys in Greece. From June to October 2020, we sampled naturally field-laid H. halys egg masses to recover native parasitoids. A total of 20 egg masses of H. halys were collected from infested fields from different locations in northern Greece. Out of 529 eggs, 45 parasitoids managed to hatch successfully. The overall parasitism rate was 8.5%. We found two species of Hymenopteran egg parasitoids attacking H. halys eggs—Anastatus bifasciatus (Geoffrey) (Hymenoptera: Eupelmidae) and Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae), with the former comprising 58% of all parasitoids that were recovered. These results contribute to the knowledge about the natural enemy community that attacks H. halys in Greece, and the use of these native egg parasitoids in biological control programs may be a viable H. halys management strategy.

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Native and Non-Native Egg Parasitoids Associated with Brown Marmorated Stink Bug (Halyomorpha halys [Stål, 1855]; Hemiptera: Pentatomidae) in Western Slovenia

Insects ◽

10.3390/insects12060505 ◽

2021 ◽

Vol 12 (6) ◽

pp. 505

Author(s):

Mojca Rot ◽

Lara Maistrello ◽

Elena Costi ◽

Iris Bernardinelli ◽

Giorgio Malossini ◽

...

Keyword(s):

Biological Control ◽

Egg Parasitoid ◽

Egg Parasitoids ◽

Control Measures ◽

Crop Damage ◽

Invasive Pest ◽

Halyomorpha Halys ◽

Stink Bug ◽

Parasitoid Species ◽

Parasitism Rates

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.

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Rearing Trissolcus japonicus and Trissolcus mitsukurii for Biological Control of Halyomorpha halys

Insects ◽

10.3390/insects11110787 ◽

2020 ◽

Vol 11 (11) ◽

pp. 787

Author(s):

Giuseppino Sabbatini-Peverieri ◽

Christine Dieckhoff ◽

Lucrezia Giovannini ◽

Leonardo Marianelli ◽

Pio Federico Roversi ◽

...

Keyword(s):

Biological Control ◽

Control Method ◽

Egg Parasitoids ◽

Halyomorpha Halys ◽

Progeny Production ◽

Asian Origin ◽

Frequent Use ◽

Trissolcus Japonicus ◽

Cumulative Curves

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.

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A morphological, biological and molecular approach reveals four cryptic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), egg parasitoids of Pentatomidae (Hemiptera)

Journal of Hymenoptera Research ◽

10.3897/jhr.73.39052 ◽

2019 ◽

Vol 73 ◽

pp. 153-200 ◽

Cited By ~ 4

Author(s):

Francesco Tortorici ◽

Elijah J. Talamas ◽

Silvia T. Moraglio ◽

Marco G. Pansa ◽

Maryam Asadi-Farfar ◽

...

Keyword(s):

Biological Control ◽

Egg Parasitoids ◽

Brown Marmorated Stink Bug ◽

Stink Bug ◽

Stink Bugs ◽

Biological Control Agents ◽

Ecological Studies ◽

Key To Species ◽

Accurate Identification ◽

The Subject

Accurate identification of parasitoids is crucial for biological control of the invasive brown marmorated stink bug, Halyomrpha halys (Stål). A recent work by Talamas et al. (2017) revised the Palearctic fauna of Trissolcus Ashmead, egg-parasitoids of stink bugs, and treated numerous species as junior synonyms of T. semistriatus (Nees von Esenbeck). In the present paper, we provide a detailed taxonomic history and treatment of T. semistriatus and the species treated as its synonyms by Talamas et al. (2017) based on examination of primary types, molecular analyses and mating experiments. Trissolcus semistriatus, T. belenus (Walker), T. colemani (Crawford), and T. manteroi (Kieffer) are here recognized as valid and a key to species is provided. The identification tools provided here will facilitate the use of Trissolcus wasps as biological control agents and as the subject of ecological studies.

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An effective cold storage method for stockpiling Halyomorpha halys eggs for field surveys and laboratory rearing of Trissolcus japonicus

10.1101/2020.04.30.071183 ◽

2020 ◽

Cited By ~ 2

Author(s):

Warren H. L. Wong ◽

Matt A. Walz ◽

Angela B. Oscienny ◽

Jade L. Sherwood ◽

Paul K. Abram

Keyword(s):

Current Method ◽

Field Studies ◽

Egg Parasitoid ◽

Halyomorpha Halys ◽

Stink Bug ◽

Time Activity ◽

Egg Masses ◽

Fitness Consequences ◽

Laboratory Colony ◽

Trissolcus Japonicus

AbstractAn effective stockpiling method for egg masses of the invasive brown marmorated stink bug (Halyomorpha halys [Stål]; Hemiptera: Pentatomidae) would be useful for rearing and field studies of its egg parasitoid Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae). The current method of stockpiling H. halys egg masses at sub-zero temperatures has lethal and sublethal fitness consequences for T. japonicus. We show that parasitoid emergence from egg masses refrigerated at 8°C for up to two months before parasitism is higher than from frozen egg masses and usually has minimal or no sublethal fitness effects (sex ratio, development time, activity, fecundity, longevity, and weight) on emerging T. japonicus. Only after two months of host egg refrigeration did the emergence of T. japonicus begin to decrease significantly (by 9.6% relative to untreated viable egg masses), whereas egg masses previously frozen at -80°C had a 58.8% reduction in parasitoid emergence after 14 days of storage. Refrigerated egg masses that were subsequently exposed to average field temperatures (warm: 22.9°C; cool: 13.2°C) were still suitable for T. japonicus parasitism after 7 days, while viable egg masses exposed to warm temperatures for 7 days before parasitism had 24.1% lower parasitoid emergence. Our results demonstrate that refrigeration at 8°C, while resulting in complete mortality of H. halys embryos after 10 days, are more suitable for T. japonicus parasitism than those stored at sub-zero temperatures. The quantity and quality of H. halys eggs that can be stockpiled with this method could facilitate T. japonicus laboratory colony maintenance, field monitoring, and releases.

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