Next Article in Journal
Lysophosphatidylcholine Acetyltransferase 2 (LPCAT2) Influences the Gene Expression of the Lipopolysaccharide Receptor Complex in Infected RAW264.7 Macrophages, Depending on the E. coli Lipopolysaccharide Serotype
Previous Article in Journal
Network Pharmacology, Molecular Docking, and Molecular Dynamics Simulation Analysis Reveal Insights into the Molecular Mechanism of Cordia myxa in the Treatment of Liver Cancer
Previous Article in Special Issue
World Spread of Tropical Soda Apple (Solanum viarum) under Global Change: Historical Reconstruction, Niche Shift, and Potential Geographic Distribution
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Biology
Volume 13
Issue 5
10.3390/biology13050316
biology-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The First Records of Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera, Scelionidae), Alien Egg Parasitoids of Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) in Serbia

by
Aleksandra Konjević
1,
Luciana Tavella
2 and
Francesco Tortorici
2,*
1
Center of Excellence, Faculty of Agriculture, University of Novi Sad, Trg Dositeja Obradovica 8, 21000 Novi Sad, Serbia
2
Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), University of Torino, largo P. Braccini 2, 10095 Grugliasco, Italy
*
Author to whom correspondence should be addressed.
Biology 2024, 13(5), 316; https://doi.org/10.3390/biology13050316
Submission received: 13 March 2024 / Revised: 26 April 2024 / Accepted: 27 April 2024 / Published: 1 May 2024
(This article belongs to the Special Issue Risk Assessment for Biological Invasions)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

In Serbia, there is a growing concern over the Brown Marmorated Stink Bug, which damages plants and creates aggregates in urban areas during the winter season. The bug population has increased, causing significant economic damage to crops. A study conducted in 2022 has discovered nine egg parasitoid species, including two foreign species, Trissolcus japonicus and Tr. mitsukurii, which were found in only one city in Serbia. This is the first time these species have been recorded in Serbia.

Abstract

Serbia has recently begun facing a serious problem with the Brown Marmorated Stink Bug, Halyomorpha halys (Stål), which was first recorded in October 2015. This species belongs to the Pentomidae family and is notorious for causing extensive damage to plants. During the winter, it tends to gather in urban areas, such as houses and different man-made facilities, which has raised concerns among producers and citizens. The population of this species has rapidly increased, causing significant economic damage to cultivated plants. However, despite the alarming situation no natural enemies have yet been identified in Serbia. Therefore, research in 2022 was focused on collecting stink bug eggs to investigate the presence of egg parasitoids. The study identified two foreign Hymenoptera species for the European region, Trissolcus japonicus (Ashmead) and Tr. mitsukurii (Ashmead) (Scelionidae), recorded for the first time in Serbia. Additionally, the list of egg parasitoid species belonging to the Hymenoptera order includes seven local species: Anastatus bifasciatus (Geoffroy), from the Eupelmidae family; Ooencyrtus sp., from the Encyrtidae family; and Telenomus turesis (Walker), Tr. basalis (Wollaston), Tr. belenus (Walker), Tr. colemani (Crawford), and Tr. semistriatus (Nees von Esenbeck), from the Scelionidae family. In total, nine egg parasitoid species were, for the first time, reported as parasitizing H. halys and related species in Serbia.

Graphical Abstract

1. Introduction

From its native range in eastern Asia, Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) has spread throughout the Holarctic region and in a few countries in South America [1], to the point that it has become a worldwide invasive pest with more than 100 host plants reported [2].
Due to the severe damage caused by the stink bug and the resulting economic losses, the use of insecticides has increased as the control of this pest relies mainly on pesticides [3,4]. Because of the application of pesticides, including broad-spectrum insecticides, beneficial insects are also killed and integrated pest management programs are negatively impacted [5].
Among the natural enemies of H. halys, considerable emphasis has been placed on egg parasitoids. In its native range, the stink bug is regulated by several egg parasitoids. Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) are predominant and the most effective parasitoids in the native area [6,7,8].
In Europe, associated parasitoids belonging to Scelionidae (Trissolcus spp., Telenomus spp.), Eupelmidae (Anastatus spp.), and Encyrtidae (Ooencyrtus spp.) were found to parasitize H. halys eggs [9,10,11,12,13,14,15,16], but they were not fully effective in controlling H. halys populations. In particular, Anastatus bifasciatus (Geoffroy) and Trissolcus kozlovi Rjachovskij are the two native egg parasitoids in Europe that have shown some potential for the control of H. halys and have been considered for augmentative biological control strategies [10,13,17,18,19,20].
Several studies have been carried out to explore the ability of parasitoids to attack H. halys eggs in their native area as well as in the newly invaded areas worldwide [9,11,13,21]. Actually, only the two Asian species Tr. japonicus and Tr. mitsukurii appear to be promising candidates as biological control agents [8,22,23,24,25]. Since 2014, Tr. japonicus started to be detected in the USA [26], then in 2017 in Europe [18], and now the distribution area is widespread [27,28,29]. The first detection of Tr. mitsukurii outside the native area (i.e., in Italy) was in 2016 [30], and then the parasitoid spread to France [31].
In Serbia, H. halys was detected in October 2015 [32]. In the following years, research was conducted to assess the distribution of the species and the damage to local crops [33], when it was confirmed that the species had become established in the newly invaded areas, and at that time the list of endangered plant species was relatively short. Since 2018, monitoring using pyramid dead-in traps (AgBio Company) with aggregation pheromones (Tréce lures) has been carried out in agricultural and urban areas. The number of traps in the country increased from 20 to 47 in 2022 (Figure 1), and monitoring results showed a continuous spread throughout the country and an increase in the population. The list of endangered host plants has been significantly increased and includes both cultivated and ornamental plants [34]. Moderate to high-level damage has been reported in many cultivated plants since 2020, especially in hazelnuts, apples, cherries, peaches, and pears (Konjević, unpublished data). The protection of cultivated plants in Serbia relies almost entirely on chemical treatments, which have sometimes proven to be insufficiently effective.
Parasitoids of stink bugs, especially of exotic species, in Serbia were not monitored until 2022. In 2021, there were two accidental captures of three native parasitoid species, Trissolcus basalis (Wollaston), Tr. belenus (Walker), and Telenomus sp., which were morphologically identified at the Faculty of Biology, University “Al. I. Cuza” in Romania (Konjević and Popovici, unpublished data). Still, there was no evidence of the presence of exotic parasitoid species, or the autochthonous A. bifasciatus, to the eggs of H. halys.
Recent studies have estimated that in invaded areas, Tr. japonicus and Tr. mitsukurii are still spreading throughout much of the western Palearctic territory and have shown potential high habitat suitability in Serbia [28,29]. Therefore, the aim of this research was to monitor H. halys in urban and semi-urban environments and assess whether egg parasitoids are potentially present in such conditions.
Biology 13 00316 g001
Figure 1. Sites with field-collected parasitized egg masses in 2022. Black rhombus: sites where Tr. japonicus and Tr. mitsukurii emerged from H. halys eggs. White rhombus: sites where only native parasitoid species were found. Gray circles: sites where dead-in traps were set in 2022 and the range of sampled H. halys specimens.
Figure 1. Sites with field-collected parasitized egg masses in 2022. Black rhombus: sites where Tr. japonicus and Tr. mitsukurii emerged from H. halys eggs. White rhombus: sites where only native parasitoid species were found. Gray circles: sites where dead-in traps were set in 2022 and the range of sampled H. halys specimens.
Biology 13 00316 g001

2. Materials and Methods

2.1. Field Collection and Laboratory Rearing of Stink Bug Egg Masses

The field survey was conducted from May to September 2022 at 27 different locations, mainly in the central and northern parts of Serbia, where the population of H. halys is regularly found in dead-in traps baited with aggregation pheromones. Firstly, the monitoring of egg masses started in the urban area of the second largest city in Serbia, Novi Sad, where three city parks were examined each week. Later, egg masses were sampled at the borders with Hungary, Croatia, and Romania in two visits during 2022, mainly urban and semi-urban environments. In addition, egg masses were occasionally collected in hazelnut, plum, and walnut orchards, and in a soybean field. All urban and semi-urban sites were characterized by a variety of plant species, but the search for eggs was focused on Catalpa sp., Paulownia sp., Sambucus nigra L., Acer sp., Styphnolobium japonicum (L.) Schott, and Koelreuteria sp., on which adults and nymphs of H. halys were observed. In many of these areas, there were no insecticide applications, except in orchards, where insecticide treatments were carried out regularly based on production needs.
Sampling in all areas was carried out in the morning hours, between 8 and 12 AM. The inspection time in each site was 1 h per person, looking at different parts of the same site. During the survey, woody and shrubby plant species were visually inspected by checking the leaves, especially the undersides where stink bugs usually lay their eggs. All field-collected stink bug eggs were brought to the laboratory and separated by sampling points and by insect species, comparing the morphology of the egg masses with images published on https://www.halyomorphahalys.com/wanzeneier-stink-bug-eggs.html (accessed on 7 February 2023) [35]. Eggs were then placed into petri dishes (10 or 15 cm in diameter) and stored under the room conditions for the emergence of either stink bug nymphs or adult parasitoids. All emerged parasitoids were stored in 96% ethanol at −4 °C, until their identification.

2.2. Species Identification

The parasitoid adults, previously stored in ethanol, were dried for morphological examination. A Wild M5 stereo microscope with up to 200× magnification was used for morphological diagnosis. Species of Trissolcus were determined using the characters and identification keys of Talamas et al. [36], Tortorici et al. [37], and Moraglio et al. [17]. Species of Anastatus were identified according to Peng et al. [38]. Species of Telenomus were determined using the keys of Kozlov and Kononova [39] and Johnson [40]. Images of the specimens were taken using a Canon 90D camera (Canon Inc., Tokyo, Japan) equipped with an extension tube and 10× and 20× LWD microscope lenses mounted on a macro-rail and illuminated with two speedlite flashes. The frames were merged with Zerene Stacker (PMax algorithm, Zerene Systems LLC, Richland, Washington, USA). All specimens used for morphological analysis were deposited in the Dipartimento di Scienze Agrarie, Forestali e Alimentari, University of Turin, Italy.

3. Results

A total of 568 naturally laid egg masses were collected, belonging to three pentatomid species: H. halys, Nezara viridula (L.), and an Asopinae (Hemiptera, Pentatomidae) (Table 1). Out of the 27 locations examined, parasitized egg masses were obtained from 12, reported in Table 1, while in the remaining locations either no eggs were recorded or only unparasitized eggs were found. Most of the eggs were collected on hazelnuts, in three orchards, while most of the parasitized eggs were sampled in the urban areas, on St. japonicum and Sa. nigra. Other host plants on which parasitized egg masses were collected are walnut, catalpa, plum, maple, paulownia, rose, and tomato. In total, parasitoid adults emerged successfully from 29 egg masses. Among the sampled eggs, there were eggs that were different in colour from the viable eggs, like dark yellow or brown, from which neither stink bug nymphs nor parasitoid adults emerged. Some eggs were already damaged by predators at the time of sampling.
Most of the parasitized eggs were found in areas where high numbers of H. halys specimens were monitored by dead-in traps, varying from 501 to 1000 per year/season (Figure 1).
Anastatus bifasciatus was the most abundant species emerging from the eggs of H. halys and N. viridula (Table 2). Ooencyrtus sp. emerged from the eggs of both H. halys and N. viridula, while Telenomus turesi Walker emerged only from the eggs of H. halys (Table 2). Based on morphological analyses, Trissolcus specimens were identified as Tr. basalis, Tr. belenus, Tr. colemani (Crawford), and Tr. semistriatus (Nees von Esenbeck), and also as the exotic Tr. japonicus and Tr. mitsukurii. These two exotic parasitoid species emerged at the site of Novi Sad from egg masses of H. halys (Figure 1).
Trissolcus japonicus emerged from four egg masses and Tr. mitsukurii from one egg mass together with the first. The two species perfectly matched with the description in Talamas et al. [36] and morphological diagnosis in Sabbatini Peverieri et al. [41], and they did not show morphological anomalies that would complicate confirmation of species identity based on morphology alone. Anastatus bifasciatus emerged from nine egg masses of H. halys and four egg masses of N. viridula. Multiparasitism was recorded in four egg masses of H. halys and three egg masses of N. viridula with Ooencyrtus sp., Te. turesis, Tr. basalis, and Tr. japonicus. Furthermore, Ooencyrtus sp. shared the same egg masses together with Tr. japonicus.
Trissolcus japonicus and Tr. mitsukurii belong to the flavipes-group and the basalis-group, respectively [36]. The two species can be distinguished from other species in their respective groups by the following characteristics:
Trissolcus japonicus—Vertex between lateral ocelli with uniform and robust hyperoccipital carina (hoc) (Figure 2B,E). Microsculpture finely colliculate along the line between the dorsal margin of the hyperoccipital carina and the posterior margin of the anterior ocellus (haol) (Figure 2E). At intersection with malar sulcus, orbital furrow (of) expanded with medial margin well-defined (Figure 2D). Clypeus with four setae (cs) (Figure 2C). Antenna with five clavomeres (A7–A11 with basiconic sensilla) with moderately large clava (Figure 2A). Mesoscutum with notauli (not) and without median mesoscutal carina (mmc) (Figure 2B,E). The finely colliculated sculpture on the mesoscutum is uniformly extensive, reaching the posterior margin between the notauli (Figure 2B,E). Mesopleuron with episternal foveae (eps) forming a continuous line of cells from postacetabular sulcus (ats) to mesopleural pit (mpp) (Figure 2D). Sublateral seta absent on each side of tergite 1 (Figure 2B,E). Laterotergite 1 without a line of setae along dorsal margin (Figure 2A,D). Tergite 2 with striae present throughout anterior half of tergite (Figure 2B).
Trissolcus mitsukurii—Vertex between lateral ocelli without hyperoccipital carina (Figure 3B,E). Clypeus with six setae (cs) (Figure 3C). Antenna with five clavomeres (A7–A11 with basiconic sensilla) with distinctly large clava (Figure 3A). Mesoscutum with notauli (not) (Figure 3B,E). Mesopleuron with two episternal foveae (eps) distant from postacetabular sulcus (ats) and mesopleural pit (mpp) (Figure 3D). Metapleuron without setae below metapleural sulcus (mtps) (Figure 3D). One or two sublateral seta (ss) present on each side of tergite 1 (Figure 3B,E). Laterotergite 1 with a line of setae along dorsal margin (slt1) (Figure 3C,D). Frons, from vertex to antennal scrobe, mesoscutum, and mesoscutellum coarsely rugose (Figure 3B,C,E).

4. Discussion

The parasitized egg masses collected at Novi Sad represent the first record of the exotic Tr. japonicus and Tr. mitsukurii in Serbia and indicate the presence of an established adventive population of both parasitoids. This is confirmed by the fact that there have been neither deliberate releases of these species for classical biological control nor any known laboratory colonies in the area. Models of the potential interaction between H. halys and these two parasitoid species hypothesized that Tr. mitsukurii and Tr. japonicus exhibit high and medium-high habitat suitability in Serbia, respectively [29], and the record of the adventive populations of these two parasitoids in the same area confirms what was predicted. For the purpose of evaluating a biological control program, the model proposed by the same authors argues that Tr. mitsukurii shows better suitability than Tr. japonicus in northern Serbia, but the habitat suitability of both scelionids overlaps in much of the country. By contrast, in the southern-most mountainous areas of the country, the probability of the suitability of both parasitoids is very low.
Since the two exotic parasitoids are well characterized and distinguishable from the western Palearctic species [36], only morphological identification was performed here. Further molecular-based investigations could assess the similarity of these adventive populations to the haplotypes distributed in the newly invaded and/or native areas and in this way trace the origin of the populations found in Serbia.
The means of arrival of Tr. japonicus and Tr. mitsukurii in Serbia is unknown, but we can suppose that their arrival is connected with the transport of goods and passengers. As the most likely means of arrival of H. halys was as a stowaway in the transport of goods and passengers [42,43,44], it is very likely that the parasitoid species also arrived in the same way [45]. Namely, as of 2020 there are several foreign construction companies located in Novi Sad and its surroundings, which have the majority of necessary equipment arriving from abroad. A few of them are located at sites close to the point where both exotic parasitoid species were found in a park. It should be emphasized that the traffic between the headquarters, or the companies’ place of business, and this park runs smoothly by the busy roads, leaving the possibility for their spread by vehicles. In contrast, in hazelnut orchards where the sampling was conducted in 2022 chemical treatments were carried out to control H. halys, which makes it difficult, although not impossible, to record and find potentially surviving parasitoid specimens. Also, hazelnut orchards are often located far from the main motorways; therefore, the spread of exotic parasitic species to those locations might need more time. These are the two main reasons why this survey was focused more on ornamental and not cultivated host plants in urban and semi urban areas.
The two species Tr. japonicus and Tr. mitsukurii can now be considered widespread throughout most European countries [18,27,30,31,41,46]. At present, in Serbia the two species were only found in one urban site and confirmed their preference for H. halys as the primary host. Since only a few specimens were found at one collection site, this may suggest that the spread of the adventive populations is in its early stage; therefore, the impact of the two parasitoids on the H. halys population cannot yet be evaluated. In subsequent years, the spread of both scelionids and their impact on the host population can be assessed by increasing the number of sites and expanding the collection season.
The Holarctic species A. bifasciatus is a generalist parasitoid [15,47], and its interspecific competition [48,49,50] makes it able to develop in different hosts and sharing a single egg mass together with other parasitoid species. Data obtained in the present study are consistent with those of other European studies and confirm the behaviour for this species. Very interesting are the data on other indigenous parasitoid species that emerged from H. halys eggs in a quantity similar to A. bifasciatus, particularly Tr. basalis and Te. turesis, which therefore deserve special attention to assess their possible adaptation and contribution to the control of the exotic pest. Due to the limited number of specimens of these native species found in the eggs of H. halys, it is difficult to predict if their presence has already affected or will potentially affect the decline of the alien and/or autochthonous stink bug species.
Given the economic importance of H. halys in Serbia, it will likely be beneficial to attract exotic parasitoids to agricultural fields and commercial fruit orchards, e.g., by increasing ecological infrastructures [51,52], and support them in a conservation biological control approach [53]. In this context, it may be warranted to further investigate the current status of the species in terms of spatial distribution and range of native hosts. Although laboratory studies were recently carried out [23,25,54], the interactions between populations of Tr. japonicus and Tr. mitsukurii in the field deserve close attention.

5. Conclusions

The brown marmorated stink bug, H. halys, is a serious threat to plant protection worldwide. Control strategies for this pest in Europe and America rely mainly on repeated application of chemical pesticides. From the perspective of an integrated control strategy with low pesticide use, attention has turned to natural enemies, such as egg parasitoids, which can be a valid strategy. To ensure the effectiveness of biological, a good knowledge of the pest and associated BCAs, including their biology, distribution, and diversity, is needed.
This study reports for the first time the presence of Tr. japonicus and Tr. mitsukurii in Serbia, thus providing additional valuable information on the geographic distribution of the two exotic parasitoids. Several countries are evaluating the introduction of these two parasitoids in classical biological control programs, and in some countries the release of either species is already underway. Knowing the spontaneous spread of both species is of paramount importance and can help better target and rationalize the control means, and guide scientists in implementing successful biological control strategies.

Author Contributions

Conceptualization, methodology, formal analysis, A.K., F.T. and L.T.; investigation, resources, data curation, A.K. and F.T.; writing—original draft preparation, review and editing, A.K., F.T. and L.T.; funding acquisition, A.K. and F.T. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by the Plant Protection Directorate of the Ministry of Agriculture, Forestry, and Water Management of the Republic of Serbia, Agriserbia d.o.o., and Ferrero Trading Lux S.A. The study was also supported by the Ministry of Science, Technological Development, and Innovation of the Republic of Serbia, project number 451-03-47/2023-01/200117, and Agreement on the realization and co-financing of the scientific research work of the accredited Center of Exceptional Values in 2023—Agreement No. 451-03-1524/2023-04/16. This study was carried out within the Agritech National Research Center and received funding from the European Union Next-Generation EU (PIANO NAZIONALE DI RIPRESA E RESILIENZA (PNRR)—MISSIONE 4 COMPONENTE 2, INVESTIMENTO 1.4—D.D. 1032 17/06/2022, CN00000022). This manuscript reflects only the authors’ views and opinions; neither the European Union nor the European Commission can be considered responsible for them.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

A.K. would like to thank Verna Brdar, Milos Petrovic, and Nikola Lacarac from the Faculty of Agriculture, University of Novi Sad, Serbia, for their help in sampling.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. EPPO. Halyomorpha halys (HALYHA) [World Distribution] EPPO Global Database. Available online: https://gd.eppo.int/taxon/HALYHA/distribution (accessed on 14 November 2022).
  2. Bergmann, E.J.; Venugopal, P.D.; Martinson, H.M.; Raupp, M.J.; Shrewsbury, P.M. Host Plant Use by the Invasive Halyomorpha halys (Stål) on Woody Ornamental Trees and Shrubs. PLoS ONE 2016, 11, e0149975. [Google Scholar] [CrossRef] [PubMed]
  3. Kuhar, T.P.; Kamminga, K. Review of the Chemical Control Research on Halyomorpha halys in the USA. J. Pest Sci. 2017, 90, 1021–1031. [Google Scholar] [CrossRef]
  4. Leskey, T.C.; Nielsen, A.L. Impact of the Invasive Brown Marmorated Stink Bug in North America and Europe: History, Biology, Ecology, and Management. Annu. Rev. Entomol. 2018, 63, 599–618. [Google Scholar] [CrossRef] [PubMed]
  5. Rice, K.B.; Bergh, C.J.; Bergmann, E.J.; Biddinger, D.J.; Dieckhoff, C.; Dively, G.; Fraser, H.; Gariepy, T.; Hamilton, G.; Haye, T.; et al. Biology, Ecology, and Management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae). J. Integr. Pest Manag. 2014, 5, A1–A13. [Google Scholar] [CrossRef]
  6. Yang, Z.Q.; Yao, Y.X.; Qiu, L.F.; Li, Z.X. A New Species of Trissolcus (Hymenoptera: Scelionidae) Parasitizing Eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with Comments on Its Biology. Ann. Entomol. Soc. Am. 2009, 102, 39–47. [Google Scholar] [CrossRef]
  7. Lee, D.H. Current Status of Research Progress on the Biology and Management of Halyomorpha halys (Hemiptera: Pentatomidae) as an Invasive Species. Appl. Entomol. Zool. 2015, 50, 277–290. [Google Scholar] [CrossRef]
  8. Zhang, J.P.; Zhang, F.; Gariepy, T.D.; Mason, P.G.; Gillespie, D.; Talamas, E.J.; Haye, T. Seasonal Parasitism and Host Specificity of Trissolcus japonicus in Northern China. J. Pest Sci. 2017, 90, 1127–1141. [Google Scholar] [CrossRef] [PubMed]
  9. Abram, P.K.; Hoelmer, K.A.; Acebes-Doria, A.L.; Andrews, H.; Beers, E.H.; Bergh, J.C.; Bessin, R.; Biddinger, D.; Botch, P.; Buffington, M.L.; et al. Indigenous Arthropod Natural Enemies of the Invasive Brown Marmorated Stink Bug in North America and Europe. J. Pest Sci. 2017, 90, 1009–1020. [Google Scholar] [CrossRef]
  10. Costi, E.; Haye, T.; Maistrello, L. Surveying Native Egg Parasitoids and Predators of the Invasive Halyomorpha halys in Northern Italy. J. Appl. Entomol. 2019, 143, 299–307. [Google Scholar] [CrossRef]
  11. Dieckhoff, C.; Tatman, K.M.; Hoelmer, K.A. Natural Biological Control of Halyomorpha halys by Native Egg Parasitoids: A Multi-Year Survey in Northern Delaware. J. Pest Sci. 2017, 90, 1143–1158. [Google Scholar] [CrossRef]
  12. Fusu, L.; Andreadis, S.S. Ooencyrtus mirus (Hymenoptera, Encyrtidae), Discovered in Europe Parasitizing Eggs of Halyomorpha halys (Hemiptera, Pentatomidae). J. Hymenopt. Res. 2023, 96, 1045–1060. [Google Scholar] [CrossRef]
  13. Haye, T.; Fischer, S.; Zhang, J.P.; Gariepy, T.D. Can Native Egg Parasitoids Adopt the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J. Pest Sci. 2015, 88, 693–705. [Google Scholar] [CrossRef]
  14. Rondoni, G.; Bertoldi, V.; Malek, R.; Foti, M.C.; Peri, E.; Maistrello, L.; Haye, T.; Conti, E. Native Egg Parasitoids Recorded from the Invasive Halyomorpha halys Successfully Exploit Volatiles Emitted by the Plant–Herbivore Complex. J Pest Sci 2017, 90, 1087–1095. [Google Scholar] [CrossRef]
  15. Stahl, J.M.; Babendreier, D.; Haye, T. Using the Egg Parasitoid Anastatus bifasciatus against the Invasive Brown Marmorated Stink Bug in Europe: Can Non-Target Effects Be Ruled Out? J. Pest Sci. 2018, 91, 1005–1017. [Google Scholar] [CrossRef] [PubMed]
  16. Tillman, G.; Toews, M.D.; Blaauw, B.R.; Sial, A.A.; Cottrell, T.E.; Talamas, E.J.; Buntin, D.G.; Joseph, S.V.; Balusu, R.R.; Fadamiro, H.; et al. Parasitism and Predation of Sentinel Eggs of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the Southeastern US. Biol. Control 2020, 145, 104247. [Google Scholar] [CrossRef]
  17. Moraglio, S.T.; Tortorici, F.; Visentin, S.; Pansa, M.G.; Tavella, L. Trissolcus kozlovi in North Italy: Host Specificity and Augmentative Releases against Halyomorpha halys in Hazelnut Orchards. Insects 2021, 12, 464. [Google Scholar] [CrossRef] [PubMed]
  18. Stahl, J.; Tortorici, F.; Pontini, M.; Bon, M.C.; Hoelmer, K.A.; Marazzi, C.; Tavella, L.; Haye, T. First Discovery of Adventive Populations of Trissolcus japonicus in Europe. J. Pest Sci. 2019, 92, 371–379. [Google Scholar] [CrossRef]
  19. Stahl, J.; Babendreier, D.; Marazzi, C.; Caruso, S.; Costi, E.; Maistrello, L.; Haye, T. Can Anastatus bifasciatus Be Used for Augmentative Biological Control of the Brown Marmorated Stink Bug in Fruit Orchards? Insects 2019, 10, 108. [Google Scholar] [CrossRef] [PubMed]
  20. Zapponi, L.; Tortorici, F.; Anfora, G.; Bardella, S.; Bariselli, M.; Benvenuto, L.; Bernardinelli, I.; Butturini, A.; Caruso, S.; Colla, R.; et al. Assessing the Distribution of Exotic Egg Parasitoids of Halyomorpha halys in Europe with a Large-Scale Monitoring Program. Insects 2021, 12, 316. [Google Scholar] [CrossRef]
  21. Herlihy, M.V.; Talamas, E.J.; Weber, D.C. Attack and Success of Native and Exotic Parasitoids on Eggs of Halyomorpha halys in Three Maryland Habitats. PLoS ONE 2016, 11, e0150275. [Google Scholar] [CrossRef]
  22. Sabbatini Peverieri, G.; Dieckhoff, C.; Giovannini, L.; Marianelli, L.; Roversi, P.F.; Hoelmer, K.A. Rearing Trissolcus japonicus and Trissolcus mitsukurii for Biological Control of Halyomorpha halys. Insects 2020, 11, 787. [Google Scholar] [CrossRef] [PubMed]
  23. Costi, E.; Di Bella, E.; Iotti, D.; Maistrello, L. Biocontrol Implications of Multiparasitism by Trissolcus mitsukurii and Trissolcus japonicus on the Invasive Brown Marmorated Stink Bug. Entomol. Exp. Appl. 2022, 170, 772–781. [Google Scholar] [CrossRef]
  24. Giovannini, L.; Sabbatini Peverieri, G.; Marianelli, L.; Rondoni, G.; Conti, E.; Roversi, P.F. Physiological Host Range of Trissolcus mitsukurii, a Candidate Biological Control Agent of Halyomorpha halys in Europe. J. Pest Sci. 2022, 95, 605–618. [Google Scholar] [CrossRef]
  25. Giovannini, L.; Sabbatini-Peverieri, G.; Simoni, S.; Cervo, R.; Alan Hoelmer, K.; Federico Roversi, P. Interspecific Competition between Trissolcus japonicus and Trissolcus mitsukurii, Two Promising Candidates for Biocontrol of Halyomorpha halys. Biol. Control 2022, 176, 105068. [Google Scholar] [CrossRef]
  26. Talamas, E.J.; Herlihy, M.V.; Dieckhoff, C.; Hoelmer, K.A.; Buffington, M.L.; Bon, M.C.; Weber, D.C. Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) Emerges in North America. J. Hymenopt. Res. 2015, 43, 119–128. [Google Scholar] [CrossRef]
  27. Rot, M.; Maistrello, L.; Costi, E.; Bernardinelli, I.; Malossini, G.; Benvenuto, L.; Trdan, S. Native and Non-Native Egg Parasitoids Associated with Brown Marmorated Stink Bug (Halyomorpha halys [Stål, 1855]; Hemiptera: Pentatomidae) in Western Slovenia. Insects 2021, 12, 505. [Google Scholar] [CrossRef]
  28. Yonow, T.; Kriticos, D.J.; Ota, N.; Avila, G.A.; Hoelmer, K.A.; Chen, H.; Caron, V. Modelling the Potential Geographic Distribution of Two Trissolcus Species for the Brown Marmorated Stink Bug, Halyomorpha halys. Insects 2021, 12, 491. [Google Scholar] [CrossRef]
  29. Tortorici, F.; Bombi, P.; Loru, L.; Mele, A.; Moraglio, S.T.; Scaccini, D.; Pozzebon, A.; Pantaleoni, R.A.; Tavella, L. Halyomorpha halys and Its Egg Parasitoids Trissolcus japonicus and T. mitsukurii: The Geographic Dimension of the Interaction. NeoBiota 2023, 85, 197–221. [Google Scholar] [CrossRef]
  30. Scaccini, D.; Falagiarda, M.; Tortorici, F.; Martinez-Sañudo, I.; Tirello, P.; Reyes-Domínguez, Y.; Gallmetzer, A.; Tavella, L.; Zandigiacomo, P.; Duso, C.; et al. An Insight into the Role of Trissolcus mitsukurii as Biological Control Agent of Halyomorpha halys in Northeastern Italy. Insects 2020, 11, 306. [Google Scholar] [CrossRef]
  31. Bout, A.; Tortorici, F.; Hamidi, R.; Warot, S.; Tavella, L.; Thomas, M. First Detection of the Adventive Egg Parasitoid of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in France. Insects 2021, 12, 761. [Google Scholar] [CrossRef]
  32. Šeat, J. Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a New Invasive Species in Serbia. Acta Entomol. Serbic 2015, 20, 167–171. [Google Scholar] [CrossRef]
  33. Musolin, D.L.; Konjević, A.; Karpun, N.N.; Protsenko, V.Y.; Ayba, L.Y.; Saulich, A.K. Invasive Brown Marmorated Stink Bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Serbia: History of Invasion, Range Expansion, Early Stages of Establishment, and First Records of Damage to Local Crops. Arthropod-Plant Interact. 2018, 12, 517–529. [Google Scholar] [CrossRef]
  34. Konjević, A. True Bugs (Heteroptera) as Pests in Ornamentals. In Sustainable Practices in Horticulture and Landscape Architecture; Ostojić, J., Cig, A., Eds.; Iksad: Ankara, Turkey, 2022; pp. 123–144. [Google Scholar]
  35. Haye, T.; Wyniger, D. Stink Bug Eggs—The Marbled Stink Bug, Halyomorpha halys. Available online: https://www.halyomorphahalys.com/wanzeneier-stink-bug-eggs.html (accessed on 7 February 2023).
  36. Talamas, E.J.; Buffington, M.L.; Hoelmer, K.A. Revision of Palearctic Trissolcus Ashmead (Hymenoptera, Scelionidae). J. Hymenopt. Res. 2017, 56, 3–185. [Google Scholar] [CrossRef]
  37. Tortorici, F.; Talamas, E.J.; Moraglio, S.T.; Pansa, M.G.; Asadi-Farfar, M.; Tavella, L.; Caleca, V. A Morphological, Biological and Molecular Approach Reveals Four Cryptic Species of Trissolcus Ashmead (Hymenoptera, Scelionidae), Egg Parasitoids of Pentatomidae (Hemiptera). J. Hymenopt. Res. 2019, 93, 153–200. [Google Scholar] [CrossRef]
  38. Peng, L.; Gibson, G.A.P.; Tang, L.; Xiang, J. Review of the Species of Anastatus (Hymenoptera: Eupelmidae) Known from China, with Description of Two New Species with Brachypterous Females. Zootaxa 2020, 4767, 351–401. [Google Scholar] [CrossRef]
  39. Kozlov, M.A.; Kononova, S.V. Telenominae of the Fauna of the USSR; Nauka: Leningrad, Russia, 1983. [Google Scholar]
  40. Johnson, N.F. Systematics of Nearctic Telenomus: Classification and Revisions of the podisi and phymatae Species Groups (Hymenoptera: Scelionidae). Bull. Ohio Biol. Surv. 1984, 6, 1–113. [Google Scholar] [CrossRef]
  41. Sabbatini Peverieri, G.; Talamas, E.J.; Bon, M.C.; Marianelli, L.; Bernardinelli, I.; Malossini, G.; Benvenuto, L.; Roversi, P.F.; Hoelmer, K.A. Two Asian Egg Parasitoids of Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) Emerge in Northern Italy: Trissolcus mitsukurii (Ashmead) and Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae). J. Hymenopt. Res. 2018, 67, 37–53. [Google Scholar] [CrossRef]
  42. Haye, T.; Wyniger, D.; Gariepy, T. Recent Range Expansion of Brown Marmorated Stink Bug in Europe. In Proceedings of the 8th International Conference on Urban Pests, Zurich, Switzerland, 20–23 July 2014; Müller, G., Pospischil, R., Robinson, W.H., Eds.; Executive Committee of the International Conference on Urban Pests: Zurich, Switzerland, 2014; pp. 309–314. [Google Scholar]
  43. Cesari, M.; Maistrello, L.; Ganzerli, F.; Dioli, P.; Rebecchi, L.; Guidetti, R. A Pest Alien Invasion in Progress: Potential Pathways of Origin of the Brown Marmorated Stink Bug Halyomorpha halys Populations in Italy. J. Pest Sci. 2015, 88, 1–7. [Google Scholar] [CrossRef]
  44. Konjević, A. First Records of the Brown Marmorated Stink Bug Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Republic of North Macedonia. Acta Zool. Bulg. 2020, 72, 687–690. [Google Scholar]
  45. Buffington, M.L.; Talamas, E.J.; Hoelmer, K.A. Team Trissolcus: Integrating Taxonomy and Biological Control to Combat the Brown Marmorated Stink Bug. Am. Entomol. 2018, 64, 224–232. [Google Scholar] [CrossRef]
  46. Dieckhoff, C.; Wenz, S.; Renninger, M.; Reißig, A.; Rauleder, H.; Zebitz, C.P.W.; Reetz, J.; Zimmermann, O. Add Germany to the List—Adventive Population of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) Emerges in Germany. Insects 2021, 12, 414. [Google Scholar] [CrossRef] [PubMed]
  47. Noyes, J. Universal Chalcidoidea Database—World Wide Web Electronic Publication. Available online: https://www.nhm.ac.uk/our-science/data/chalcidoids/database/ (accessed on 27 March 2023).
  48. Konopka, J.K.; Haye, T.; Gariepy, T.D.; McNeil, J.N. Possible Coexistence of Native and Exotic Parasitoids and Their Impact on Control of Halyomorpha halys. J. Pest Sci. 2017, 90, 1119–1125. [Google Scholar] [CrossRef]
  49. Stahl, J.M.; Babendreier, D.; Haye, T. Life History of Anastatus bifasciatus, a Potential Biological Control Agent of the Brown Marmorated Stink Bug in Europe. Biol. Control 2019, 129, 178–186. [Google Scholar] [CrossRef]
  50. Mi, Q.; Zhang, J.P.; Haye, T.; Zhang, B.; Zhao, C.; Lei, Y.; Li, D.; Zhang, F. Fitness and Interspecific Competition of Trissolcus japonicus and Anastatus japonicus, Egg Parasitoids of Halyomorpha halys. Biol. Control 2021, 152, 104461. [Google Scholar] [CrossRef]
  51. Olson, D.M.; Wäckers, F.L. Management of Field Margins to Maximize Multiple Ecological Services. J. Appl. Ecol. 2007, 44, 13–21. [Google Scholar] [CrossRef]
  52. Winkler, K.; Wäckers, F.; Pinto, D.M. Nectar-Providing Plants Enhance the Energetic State of Herbivores as Well as Their Parasitoids under Field Conditions. Ecol. Entomol. 2009, 34, 221–227. [Google Scholar] [CrossRef]
  53. Abram, P.K.; Mills, N.J.; Beers, E.H. Review: Classical Biological Control of Invasive Stink Bugs with Egg Parasitoids—What Does Success Look Like? Pest Manag. Sci. 2020, 76, 1980–1992. [Google Scholar] [CrossRef]
  54. Scala, M.; Fouani, J.M.; Zapponi, L.; Mazzoni, V.; Wells, K.E.; Biondi, A.; Baser, N.; Verrastro, V.; Anfora, G. Attraction of Egg Parasitoids Trissolcus mitsukurii and Trissolcus japonicus to the Chemical Cues of Halyomorpha halys and Nezara viridula. Insects 2022, 13, 439. [Google Scholar] [CrossRef]
Biology 13 00316 g002
Figure 2. Female of Tr. japonicus. (A) head, mesosoma, metasoma, lateral view; (B) head, mesosoma, metasoma, dorsal view; (C) head, anterolateral view; (D) head, mesosoma, lateral view; (E) head, mesosoma, metasoma, dorsolateral view. A7–A11 = 5 clavomers; hoc = hyperoccipital carina; not = notauli; cs = clypeal setae; of = orbital furrow; mpp = mesopleural pit; eps = episternal foveae; ats = postacetabular sulcus; haol = line between the dorsal margin of hyperoccipital carina and posterior margin of anterior ocellus.
Figure 2. Female of Tr. japonicus. (A) head, mesosoma, metasoma, lateral view; (B) head, mesosoma, metasoma, dorsal view; (C) head, anterolateral view; (D) head, mesosoma, lateral view; (E) head, mesosoma, metasoma, dorsolateral view. A7–A11 = 5 clavomers; hoc = hyperoccipital carina; not = notauli; cs = clypeal setae; of = orbital furrow; mpp = mesopleural pit; eps = episternal foveae; ats = postacetabular sulcus; haol = line between the dorsal margin of hyperoccipital carina and posterior margin of anterior ocellus.
Biology 13 00316 g002
Biology 13 00316 g003
Figure 3. Female of Tr. mitsukurii. (A) head, mesosoma, metasoma, lateral view; (B) head, mesosoma, metasoma, dorsal view; (C) head, mesosoma, anterolateral view; (D) head, mesosoma, lateral view; (E) head, mesosoma, metasoma, dorsolateral view. A7–A11 = 5 clavomers; not = notauli; ss = sublateral seta; cs = clypeal setae; slt1 = setation of laterotergite 1; mpp = mesopleural pit; eps = episternal foveae; ats = postacetabular sulcus.
Figure 3. Female of Tr. mitsukurii. (A) head, mesosoma, metasoma, lateral view; (B) head, mesosoma, metasoma, dorsal view; (C) head, mesosoma, anterolateral view; (D) head, mesosoma, lateral view; (E) head, mesosoma, metasoma, dorsolateral view. A7–A11 = 5 clavomers; not = notauli; ss = sublateral seta; cs = clypeal setae; slt1 = setation of laterotergite 1; mpp = mesopleural pit; eps = episternal foveae; ats = postacetabular sulcus.
Biology 13 00316 g003
Table 1. Sites in Serbia, where parasitized stink bug egg masses were collected in 2022. Hh, Halyomorpha halys; Nv, Nezara viridula; As, Asopinae. The asterisks (*) indicate cases of multiparasitisms.
Table 1. Sites in Serbia, where parasitized stink bug egg masses were collected in 2022. Hh, Halyomorpha halys; Nv, Nezara viridula; As, Asopinae. The asterisks (*) indicate cases of multiparasitisms.
IDSiteHabitatCoordinatesAltitude (m asl)Total Number of Egg MassesParasitized Egg Masses
1Backi PetrovacHazelnut orchard 45°19′38″ N
19°41′24″ E		801Hh (1)
2Backi VinogradiSemi-urban rural area, border with Hungary46°7′26″ N
19°51′34″ E		952Hh (2)
3HorgosSemi-urban rural area, border with Hungary46°8′50″ N
19°58′11″ E		825Hh (1)
4KaravukovoRural area, border with Croatia45°30′10″ N
19°12′22″ E		822Hh (1 *)
5LacarakSemi-urban rural area44°59′49″ N
19°34′37″ E		813Nv (2)
6Ljukovo Hazelnut orchard 45°0′32″ N
20°0′52″ E		101306Hh (1)
7Mala RemetaAgricultural area, orchards45°5′40″ N
19°45′1″ E		20510Hh (1)
8Novi SadUrban park45°14′23″ N
19°50′36″ E		10071Hh (6 *), Nv (3 *), As (1)
9PalicSemi-urban rural area46°6′14″ N
19°47′14″ E		981Hh (1)
10RibariHazelnut orchard 44°42′9″ N
19°25′10″ E		93150Hh (3)
11SomborWalnut orchard45°45′53″ N
19°4′48″ E		8412Hh (2 *),
Nv (3 *)
12Srpski Miletic Semi-urban rural area45°33′27″ N
19°12′46″ E		835Nv (1)
Table 2. Total number of individuals of A. bifasciatus (Ab), Ooencyrtus sp. (Oo), Te. turesis (Tt), Tr. basalis (Tba), Tr. belenus (Tbe), Tr. colemani (Tc), Tr. japonicus (Tj), Tr. mitsukurii (Tm), Tr. semistriatus (Ts) emerged from H. halys, N. viridula, and Asopinae egg masses.
Table 2. Total number of individuals of A. bifasciatus (Ab), Ooencyrtus sp. (Oo), Te. turesis (Tt), Tr. basalis (Tba), Tr. belenus (Tbe), Tr. colemani (Tc), Tr. japonicus (Tj), Tr. mitsukurii (Tm), Tr. semistriatus (Ts) emerged from H. halys, N. viridula, and Asopinae egg masses.
SpeciesNo. Egg MassesNo. and Species of Parasitoids Emerged in Laboratory
Halyomorpha halys1949 Tba, 32 Ab, 31 Tj, 19 Tt, 10 Oo, 3 Tc, 2 Tm
Nezara viridula962 Ab, 37 Tba, 26 Ts, 1 Oo
Asopinae14 Tbe
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Konjević, A.; Tavella, L.; Tortorici, F. The First Records of Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera, Scelionidae), Alien Egg Parasitoids of Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) in Serbia. Biology 2024, 13, 316. https://doi.org/10.3390/biology13050316

AMA Style

Konjević A, Tavella L, Tortorici F. The First Records of Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera, Scelionidae), Alien Egg Parasitoids of Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) in Serbia. Biology. 2024; 13(5):316. https://doi.org/10.3390/biology13050316

Chicago/Turabian Style

Konjević, Aleksandra, Luciana Tavella, and Francesco Tortorici. 2024. "The First Records of Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera, Scelionidae), Alien Egg Parasitoids of Halyomorpha halys (Stål) (Hemiptera, Pentatomidae) in Serbia" Biology 13, no. 5: 316. https://doi.org/10.3390/biology13050316

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop