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

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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Characteristics of the meconia of European egg parasitoids of Halyomorpha halys

Journal of Hymenoptera Research ◽

10.3897/jhr.77.52904 ◽

2020 ◽

Vol 77 ◽

pp. 187-201

Author(s):

Giuseppino Sabbatini-Peverieri ◽

Lucrezia Giovannini ◽

Claudia Benvenuti ◽

Luca Madonni ◽

Kim Hoelmer ◽

...

Keyword(s):

Biological Control ◽

Native Species ◽

Control Method ◽

Adult Emergence ◽

Classical Biological Control ◽

Egg Parasitoid ◽

Egg Parasitoids ◽

Halyomorpha Halys ◽

Parasitoid Species ◽

The Usa

Halyomorpha halys is a severe invasive Asian pest worldwide and classical biological control is foreseen as the most promising control method. Egg parasitoids appear to be the most important natural enemies of this pest, especially the Asian hymenopteran Trissolcus japonicus. In the invaded areas, only a few egg parasitoid species have been able to adopt H. halys as a host. Anastatus bifasciatus is the most common native egg parasitoid of H. halys in Europe, but reaches only low levels of parasitization, while several other native species are only occasionally found. Recently, adventive populations have been found both in the USA and in Europe of T. japonicus, and in Italy of a second Asian species, Trissolcus mitsukurii. Species identification based on morphological traits by specialists or by molecular analysis is a crucial step in the management of biological control programs. The ability to identify the genus or species within a narrow guild of egg parasitoids based on adult emergence holes and meconium features can be a simple and useful method to support management efforts. We present here detailed descriptions of the meconium of the most frequent parasitoid species attacking H. halys in Europe and the characteristics of their emergence holes of the adult wasps.

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Preempting the Arrival of the Brown Marmorated Stink Bug, Halyomorpha halys: Biological Control Options for Australia

Insects ◽

10.3390/insects12070581 ◽

2021 ◽

Vol 12 (7) ◽

pp. 581

Author(s):

Valerie Caron ◽

Tania Yonow ◽

Cate Paull ◽

Elijah J. Talamas ◽

Gonzalo A. Avila ◽

...

Keyword(s):

Biological Control ◽

Northeast Asia ◽

Egg Parasitoid ◽

Halyomorpha Halys ◽

Brown Marmorated Stink Bug ◽

Stink Bug ◽

Biological Control Agents ◽

Parasitoid Species ◽

Potential Effectiveness ◽

Control Options

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.

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

Insects ◽

10.3390/insects11090588 ◽

2020 ◽

Vol 11 (9) ◽

pp. 588

Author(s):

Livia Zapponi ◽

Marie Claude Bon ◽

Jalal Melhem Fouani ◽

Gianfranco Anfora ◽

Silvia Schmidt ◽

...

Keyword(s):

Biological Control ◽

Mitochondrial Gene ◽

Strong Support ◽

Egg Parasitoids ◽

Economic Losses ◽

Halyomorpha Halys ◽

Stink Bug ◽

Plant Host ◽

Egg Masses ◽

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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Physiological Host Range of Trissolcus Mitsukurii, A Candidate Biological Control Agent of Halyomorpha Halys

10.21203/rs.3.rs-362649/v1 ◽

2021 ◽

Author(s):

Lucrezia Giovannini ◽

Giuseppino Sabbatini-Peverieri ◽

Leonardo Marianelli ◽

Gabriele Rondoni ◽

Eric Conti ◽

...

Keyword(s):

Biological Control ◽

Host Range ◽

Biocontrol Agent ◽

Biological Control Agent ◽

Classical Biological Control ◽

Egg Parasitoid ◽

Control Agent ◽

Egg Load ◽

Halyomorpha Halys ◽

Stink Bug

Abstract The invasive stink bug Halyomorpha halys is a severe agricultural pest of worldwide importance, and chemical insecticides are largely sprayed for the control of its populations. Negative impacts and several failures in chemical pest management led to consider classical biological control as one of the most promising methods in a long-term perspective. The Asian egg parasitoid Trissolcus japonicus is the main candidate biocontrol agent of H. halys, but more recently a second Asian egg parasitoid, Trissolcus mitsukurii, is getting attention after adventive populations were found on H. halys egg masses in Europe. Before recommending the use of T. mitsukurii for biological control of H. halys, a risk analysis is necessary and therefore here we present the first study on the fundamental physiological host range of this parasitoid in Europe. Tests conducted with T. mitsukurii on different hemipterans, using three different experimental designs, revealed a broad physiological host range, comparable with the host range displayed by T. japonicus under similar laboratory conditions. Specifically, in addition to its coevolved host H. halys, T. mitsukurii successfully parasitized the majority of tested pentatomid species and one scutellerid, although with highly variable emergence rates. Host egg sizes positively affected parasitoid size and female egg load. Further studies, testing more complex systems that involve olfactory cues from host and host plants, will simulate different aspects of the parasitoid host location behavior under field conditions, allowing in-depth evaluation of the possible risks associated with the use of T. mitsukurii as a biocontrol agent of H. halys.

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Sensitivity of the Egg Parasitoid Trissolcus japonicus (Hymenoptera: Scelionidae) to Field and Laboratory-Applied Insecticide Residue

Journal of Economic Entomology ◽

10.1093/jee/toz127 ◽

2019 ◽

Vol 112 (5) ◽

pp. 2077-2084 ◽

Cited By ~ 7

Author(s):

David M Lowenstein ◽

Heather Andrews ◽

Anthony Mugica ◽

Nik G Wiman

Keyword(s):

Biological Control ◽

Untreated Control ◽

Egg Parasitoid ◽

Halyomorpha Halys ◽

Brown Marmorated Stink Bug ◽

Stink Bug ◽

Anthranilic Diamide ◽

Trissolcus Japonicus ◽

Organic Insecticides ◽

Urban Sites

Abstract The spread of adventive Trissolcus japonicus (Ashmead, 1904) populations in North America is anticipated to increase biological control of Halyomorpha halys (Stål; Hemiptera: Pentatomidae), the brown marmorated stink bug. In an agricultural context, biological control will succeed if it can be integrated in an environment with insecticide applications. We investigated T. japonicus compatibility with nine conventional and organic insecticides commonly used in integrated pest management in perennial crops. Through evaluating mortality and longevity in field and laboratory trials, we determined that T. japonicus fares poorly when exposed to residues of neonicotinoids and pyrethroids. Spinosad resulted in the highest percentage of T. japonicus mortality, 100% in the laboratory and 97% in a field trial. The anthranilic diamide, chlorantraniliprole, had the lowest lethality, with no differences compared to an untreated control. Trissolcus japonicus survived insecticide applications in hazelnut orchards, and over 50% of wasps remained alive after contact with the anthranilic diamides, chlorantraniliprole and cyantraniliprole, the biopesticide Chromobacterium, and an untreated control. Our results indicate that T. japonicus is unlikely to survive and parasitize H. halys in settings that coincide with broad-spectrum insecticide application. Future T. japonicus redistributions could continue in orchards treated with anthranilic diamides and Chromobacterium. As H. halys is a landscape-level pest, orchards may also benefit from biological control if T. japonicus are released in unsprayed areas adjacent to agriculture and in urban sites.

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An Insight into the Role of Trissolcus mitsukurii as Biological Control Agent of Halyomorpha halys in Northeastern Italy

Insects ◽

10.3390/insects11050306 ◽

2020 ◽

Vol 11 (5) ◽

pp. 306 ◽

Cited By ~ 3

Author(s):

Davide Scaccini ◽

Martina Falagiarda ◽

Francesco Tortorici ◽

Isabel Martinez-Sañudo ◽

Paola Tirello ◽

...

Keyword(s):

Biological Control ◽

Biological Control Agent ◽

Field Performance ◽

Egg Parasitoid ◽

Control Agent ◽

The Other ◽

Invasive Pest ◽

Halyomorpha Halys ◽

Wide Range ◽

Northeastern Italy

Sustainable strategies such as classical or augmentative biological control are currently being evaluated for the long-term management of the alien invasive pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). A three-year study carried out in northeastern Italy was performed to investigate the distribution and field performance of the H. halys egg parasitoid Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae), in comparison with other parasitoid species. In the study area, adventive populations of T. mitsukurii were present since 2016, representing the earliest detection of this species in Europe. Trissolcus mitsukurii was the most abundant parasitoid and showed a higher “parasitoid impact” (i.e., number of parasitized eggs over the total number of field-collected eggs) compared to the other species, i.e., Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae), Trissolcus basalis (Wollaston) and Trissolcus kozlovi Rjachovskij (Hymenoptera: Scelionidae). The hyperparasitoid Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) was also recorded. Phylogenetic analysis of T. mitsukurii population distinguished two clades, one covering samples from Italy, Japan and China, the other from South Korea. The present study provides promising results for the biological control of a pest that is having a dramatic impact on a wide range of crops worldwide.

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Коричнево-мраморный клоп – новая угроза овощеводству на юге России

Kartofel` i ovoshi ◽

10.25630/pav.2020.11.69.004 ◽

2020 ◽

Author(s):

I.M. Mityushev

Keyword(s):

Control Measures ◽

Invasive Pest ◽

Halyomorpha Halys ◽

Brown Marmorated Stink Bug ◽

Stink Bug ◽

Fruit Crops ◽

The South ◽

Krasnodar Krai ◽

Invasive Range ◽

First Time

Представлена информация о происхождении и географическом распространении коричнево-мраморного клопа Halyomorpha halys Stl (Hemiptera: Pentatomidae). Приведены данные об инвазивном ареале и вредоносности коричнево-мраморного клопа на юге России. Дано описание морфологических и биологических особенностей вредителя. Описаны методы мониторинга и борьбы с вредителем. Коричнево-мраморный клоп опасный инвазивный вредитель, происходящий из восточной Азии. Он повреждает значительное количество экономически значимых растений, включая различные овощные и плодовые культуры, а также лесные и декоративные растения. В Европе вредитель впервые был выявлен в 2004 году в Швейцарии и Лихтенштейне к 2020 году он распространился в 26 странах континента. На территории Евразийского экономического союза впервые зарегистрирован в России в 2014 году, на территории города Сочи в 2017 году впервые обнаружен в Казахстане. Сегодня происходит формирование инвазивного ареала вредителя на юге России: он распространился в Краснодарском крае и в республике Крым. Коричнево-мраморный клоп способен питаться на более чем 300 видах растений из 49 семейств, включая различные плодовые, овощные, декоративные и лесные растения. Из овощных культур наиболее сильно повреждает томаты, перец, баклажан, огурец, фасоль, горох и кукурузу, из плодовых культур яблоню, грушу, персик, черешню, цитрусовые, лещину, хурму и виноград. Уже в 2016-2017 годах H. halys нанес серьезный вред овощным и плодовым культурам в Краснодарском крае. Выявление очагов коричнево-мраморного клопа осуществляют методами визуального и феромонного мониторинга. Феромонный мониторинг позволяет выявлять вредителей даже при низкой численности, его осуществляют при помощи феромонных ловушек, которые размещают с мая по сентябрь. В Государственный каталог пестицидов и агрохимикатов, разрешенных к применению на территории Российской Федерации включено три инсектицида против этого вредителя, но препараты, разрешенные для защиты от него пасленовых и бобовых культур, сегодня в нем отсутствуют.The article provides information on origin and world distribution of the brown marmorated stink bug, Halyomorpha halys Stl (Hemiptera: Pentatomidae). The data on the invasive range and harmfulness of the pest in the South of Russia is presented. The description of morphological and biological features of the pest is given. The pest monitoring and control measures are described. The brown marmorated stink bug is a dangerous invasive pest of East Asia origin. It damages a number of economically important plants, including various vegetable and fruit crops, as well as forestry and ornamentals. In Europe, this pest has been recorded for the first time in 2004, in Switzerland and Liechtenstein as of 2020, it has been introduced to 26 countries of the continent. In the Eurasian Economic Union, the pest has been recorded for the first time in Russia in 2014, in the territory of Sochi in 2017 it has been recorded for the first time in Kazakhstan. The invasive range of the pest is currently being formed in the South of Russia. The pest has spread to the Krasnodar Krai and the Republic of Crimea. The brown marmorated stink bug feeds on more than 300 plant species from 49 families. The most severely damaged vegetable crops are tomatoes, peppers, aubergine, cucumber, beans, peas and corn among the fruit crops, the highest damage occurs in apples, pears, peaches, cherries, citrus fruit crops, hazel, persimmons, and grapes. As early as in 2016-2017, the brown marmorated stink bug caused serious damage to vegetable and fruit crops in the Krasnodar Krai. Detection of outbreaks of the brown marmorated stink bug is carried out by both visual and pheromone monitoring. Pheromone monitoring allows identifying pests even at low population densities it is carried out using pheromone traps, which are placed on the edges of fields from May to September. The State catalogue of pesticides and agrochemicals permitted for use on the territory of the Russian Federation includes 3 insecticides recommended for use against this pest, but so far there are no preparations permitted for protection of solanaceous and legume crops.

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Factors influencing the occurrence of fall armyworm parasitoids in Zambia

Journal of Pest Science ◽

10.1007/s10340-020-01320-9 ◽

2020 ◽

Author(s):

Léna Durocher-Granger ◽

Tibonge Mfune ◽

Monde Musesha ◽

Alyssa Lowry ◽

Kathryn Reynolds ◽

...

Keyword(s):

Biological Control ◽

Natural Enemies ◽

Smallholder Farmers ◽

Insect Pest ◽

Fall Armyworm ◽

Parasitoid Species ◽

Maize Crop ◽

Parasitism Rates ◽

Control Programmes ◽

Interest In Research

AbstractInvasive alien species have environmental, economic and social impacts, disproportionally threatening livelihood and food security of smallholder farmers in low- and medium-income countries. Fall armyworm (FAW) (Spodoptera frugiperda), an invasive insect pest from the Americas, causes considerable losses on maize to smallholder farmers in Africa since 2016. The increased use of pesticides to control FAW in Africa raises concerns for health and environmental risks resulting in a growing interest in research on biological control options for smallholder farmers. In order to evaluate the occurrence of local natural enemies attacking FAW, we collected on a weekly basis FAW eggs and larvae during a maize crop cycle in the rainy season of 2018–2019 at four locations in the Lusaka and Central provinces in Zambia. A total of 4373 larvae and 162 egg masses were collected. For each location and date of collection, crop stage, the number of plants checked and amount of damage were recorded to analyse which factors best explain the occurrence of the natural enemy species on maize. Overall parasitism rates from local natural enemies at each location varied between 8.45% and 33.11%. We identified 12 different egg-larval, larval and larval-pupal parasitoid species. Location, maize growth stage, pest density and larval stage significantly affected parasitoid species occurrence. Our findings indicate that there is potential for increasing local populations of natural enemies of FAW through conservation biological control programmes and develop safe and practical control methods for smallholder farmers.

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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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