Parasitism and predation of sentinel eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the southeastern US

Tillman, Glynn; Toews, Michael D.; Blaauw, Brett R.; Sial, Ashfaq A; Cottrell, Ted E.; Talamas, Elijah J.; Buntin, David; Joseph, Shimat V.; Balusu, Rammohan; Fadamiro, Henry Y.; Lahiri, Soumendra N.; Patel, Dilani K.

doi:10.1016/j.biocontrol.2020.104247

Cited by 42 publications

(39 citation statements)

References 48 publications

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“…The direct exposure of sentinel egg masses proved to be more effective than the use of cages, whose structure probably inhibited the entrance of parasitoids. Predation of sentinel egg masses did not represent a limiting factor, with a percentage of incidence lower than what has been recorded in other studies [17]. The fact that Tr.…”

Section: Discussionmentioning

confidence: 53%

“…Since Ailanthus altissima (Mill.) Swingle is considered a highly attractive species for H. halys [17], we selected 11 sites with Ai. altissima trees bordering apple orchards and vineyards ( Figure S1).…”

Section: Sentinel Egg Masses Exposure With Cagesmentioning

confidence: 99%

“…The monitoring of the abundance of H. halys egg parasitoids is commonly based on (a) exposure of sentinel egg masses [15,17], (b) field collection of H. halys egg masses [18,19], and c) the use of yellow sticky traps [20,21]. All of these methods present their advantages and drawbacks in terms of the time required to perform the different survey phases.…”

Section: Introductionmentioning

confidence: 99%

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

Zapponi

Bon

Fouani

et al. 2020

Insects

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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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Section: Discussionmentioning

confidence: 53%

Section: Sentinel Egg Masses Exposure With Cagesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Zapponi

Bon

Fouani

et al. 2020

Insects

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“…Only species observed in more than one site were included in the analyses. In the case of the Auer (Ora) site (Site 3), eggs from which no H. halys nymphs or parasitoids emerged were further assessed for other causes of mortality [32] under a Leica stereomicroscope (series MZ6) according to Morrison et al [33], and then ascribed to predation or to other causes of mortality (e.g., deformed and discolored eggs). For eggs where H. halys hatching or parasitoid emergence took place in the field before sampling, the category was assessed according to Jones et al [34], and eggs were classified as parasitized or hatched eggs.…”

Section: Sampling Sites and Laboratory Studymentioning

confidence: 99%

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

Scaccini

Falagiarda

Tortorici

et al. 2020

Insects

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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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“…Oencyrtus telenomicida attacks various European pentatomid species and is also able to attack and successfully develop in H. halys fresh sentinel eggs in Italy (Roversi et al 2016), while G. pennsylvanicum is known to be a natural enemy of Leptoglossus occidentalis Heidemann (Hemiptera, Coreidae) (Roversi et al 2011). Gryon obesum has been recorded from H. halys in the U.S.A. (Tillman et al 2020) and other Gryon species attack pentatomid hosts in North America and Asia (Felipe-Victoriano et al 2019;Martel et al 2019). Ooencyrtus telenomicida and G. pennsylvanicum originated from the permanent colonies maintained at CREA facilities on egg masses of H. halys and L. occidentalis as hosts, respectively (Sabbatini Peverieri et al 2012;Roversi et al 2016).…”

Section: Collection and Rearing Of The Insectsmentioning

confidence: 99%

Characteristics of the meconia of European egg parasitoids of Halyomorpha halys

Peverieri¹,

Giovannini²,

Benvenuti³

et al. 2020

JHR

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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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Parasitism and predation of sentinel eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the southeastern US

Cited by 42 publications

References 48 publications

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

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

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

Characteristics of the meconia of European egg parasitoids of Halyomorpha halys

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