Startseite Parasitism of Halyomorpha halys and Nezara viridula (Hemiptera: Pentatomidae) sentinel eggs in Central Florida
Artikel Open Access

Parasitism of Halyomorpha halys and Nezara viridula (Hemiptera: Pentatomidae) sentinel eggs in Central Florida

  • Sarah Birkmire , Norman C. Leppla EMAIL logo , Cindy L. McKenzie , Matthew R. Moore , Lance S. Osborne , Martin L. Seehausen , Elijah J. Talamas , P. Glynn Tillman und Amanda C. Hodges
Veröffentlicht/Copyright: 25. September 2025
Artikel downloaden (PDF)
Florida Entomologist
Aus der Zeitschrift Florida Entomologist Band 108 Heft 1

Abstract

Egg parasitoids of Halyomorpha halys (Stål) and Nezara viridula (L.) (Hemiptera: Pentatomidae) were identified from sentinel egg masses and yellow sticky traps deployed in Central Florida from March 2021 to March 2022. The eggs and traps were placed in two peach orchards, a vegetable farm, and a vineyard. Approximately 3,300 eggs were deployed and the 1,472 eggs not consumed by predators or lost yielded 61 parasitoids. Parasitoid wasps (Hymenoptera) that emerged from eggs of both host species included Anastatus spp. (Eupelmidae), Anastatus nr. hirtus (Ashmead), Anastatus tenuipes (Bolivar y Pieltain), and Trissolcus solocis Johnson (Scelionidae). Five species of parasitoids were obtained only from H. halys eggs: Anastatus mirabilis (Walsh and Riley), Ooencyrtus sp. 2 (Encyrtidae), Ooencyrtus johnsoni (Howard), Trissolcus brochymenae (Ashmead), and Trissolcus hullensis (Harrington). These are new host-parasitoid associations for Florida. Ooencyrtus sp. and Psix striaticeps (Dodd) (Scelionidae) were obtained only from N. viridula eggs. Mitochondrial DNA sequencing using CO1 identified 11 parasitoid species: P. striaticeps, T. brochymenae, T. hullensis, T. solocis, Ooencyrtus sp. 1, Ooencyrtus sp. 2, O. johnsoni, Anastatus nr. hirtus, Anastatus sp. 1, A. tenuipes, and A. mirabilis. Another 13 specimens of Anastatus were not conclusively identified to species. The yellow sticky traps captured 26 egg parasitoids, including Telenomus spp. (Scelionidae), Hadronotus spp. (Scelionidae), P. striaticeps and a Trissolcus sp. This research provided preliminary information for augmentative biological control of pentatomids in Florida crops.

Resumen

Huevos de Halyomorpha halys (Stål) y Nezara viridula (L) (Hemiptera: Pentatomidae) se identificaron parasitoides de a partir de masas de huevos centinela y trampas adhesivas amarillas colocadas en Florida Central entre marzo de 2021 y marzo de 2022. Los huevos y las trampas se colocaron en dos huertos de duraznos, una huerta y un viñedo. Aproximadamente 3300 huevos fueron depositados, y los 1,472 huevos no consumidos por depredadores o perdidos dieron lugar a 61 parasitoides. Las avispas parasitoides (Hymenoptera) que emergieron de los huevos de ambas especies hospedadoras incluyeron Anastatus spp. (Eupelmidae), Anastatus nr. hirtus (Ashmead), Anastatus tenuipes (Bolivar y Pieltain) y Trissolcus solocis Johnson (Scelionidae). Cinco especies de parasitoides se obtuvieron solo de huevos de H. halys: Anastatus mirabilis (Walsh y Riley), Ooencyrtus sp. 2 (Encyrtidae), Ooencyrtus johnsoni (Howard), Trissolcus brochymenae (Ashmead) y Trissolcus hullensis (Harrington). Estas son nuevas asociaciones huésped-parasitoide para Florida. Ooencyrtus sp. y Psix striaticeps (Dodd) (Scelionidae) se obtuvieron solo de huevos de N. viridula. La secuenciación de ADN mitocondrial utilizando CO1 identificó 11 especies de parasitoides: P. striaticeps, T. brochymenae, T. hullensis, T. solocis, Ooencyrtus sp. 1, Ooencyrtus sp. 2, O. johnsoni, Anastatus nr. hirtus, Anastatus sp. 1, A. tenuipes y A. mirabilis. Otros 13 especímenes de Anastatus no fueron identificados concluyentemente. Las trampas adhesivas amarillas capturaron 26 parasitoides de huevos, incluyendo Telenomus spp. (Scelionidae), Hadronotus spp. (Scelionidae), P. striaticeps y un Trissolcus sp. Esta investigación proporcionó información preliminar para el control biológico aumentativo de pentatómidos en cultivos de Florida.

Keywords: biological control; sentinel eggs; stink bugs; egg parasitoids; sticky traps
Palabras clave: control biológico; huevos centinela; chinches hediondas; parasitoides de huevos; trampas adhesivas

1 Introduction

Adventive pentatomids, such as the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), and the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae), are included in the complex of invasive species of Hemiptera that could become significant pests of Florida crops (Leskey et al. 2012; McPherson 2018; Panizzi 2015; Penca and Hodges 2018). In addition to these two species, pentatomids recently established in the U.S. include the bagrada bug, Bagrada hilaris (Burmeister) (Palumbo and Natwick 2010; Palumbo et al. 2016) and the kudzu bug, Megacopta cribraria (F.) (Eger et al. 2010). A total of 14 species of herbivorous stink bugs were recently collected from tomato and sorghum crops in North Florida, N. viridula being one of the most abundant (Leppla et al. 2023). Nezara viridula is a polyphagous cosmopolitan pest that feeds on at least 145 plant species within 32 taxonomic families (Panizzi et al. 2000) but prefers legumes (Esquivel et al. 2018; Todd 1989). The brown marmorated stink bug consumes similar plants (Rice et al. 2014). Some of these host plants are important crops in Florida and the southeastern U.S., such as strawberry, tomato, sweet corn, blueberry, snap bean, and cabbage (FDACS 2024). These pentatomids also feed on some ornamental plants for which Florida is one of the leading producers in the U.S. (Hayk et al. 2022). Due to the potential economic impact of these invasive stink bugs, research is being conducted on integrated pest management tactics that incorporate augmentative biological control (Birkmire 2022; Cornelius et al. 2016).

Egg parasitoids of H. halys and N. viridula include the microhymenopteran genera Anastatus Motschulsky (Eupelmidae), Apsilocera Bouček (Pteromalidae), Ooencyrtus Ashmead (Encyrtidae), and Hadronotus Förster, Psix Kozlov & Lê, Telenomus Haliday, and Trissolcus Ashmead (Scelionidae) (Abram et al. 2017; Dieckhoff et al. 2017; Johnson and Masner 1985; Koppel et al. 2009). Some Scelionidae are especially effective for classical and augmentative biological control because they locate host eggs efficiently, have high rates of reproduction, lack hyperparasitoids, synchronize with host populations and adjust to their densities, and are easy to rear (Martel et al. 2019; Nakasuji et al. 1966; Ogburn et al. 2016; Orr 1988; Turner 1983). Telenomus nakagawai Watanabe, for example, is a successful parasitoid of N. viridula due to its efficient host finding ability (Nakasuji et al. 1966). Telenomus spp. are more effective biological control agents of Lepidoptera than Trichogramma spp. because of their extended oviposition period, efficient searching ability, and adult longevity (Hirose 1986). The high reproductive rate of Gryon aetherium Talamas from Pakistan makes it a promising biological control agent of Bagrada hilaris in California (Martel et al. 2019; Talamas et al. 2021).

In the southeastern U.S., most research on egg parasitoids of pentatomids has been conducted in Louisiana, Georgia and Alabama (Moonga et al. 2018; Orr et al. 1986; Tillman 2010, 2011, 2016; Tillman et al. 2020). In Florida, Temerak and Whitcomb (1984) observed egg parasitism of three predaceous stink bug species in soybean crops, including Alaeorrhynchus grandis (Dall.), Euthyrhynchus floridanus (L.), and Podisus maculiventris (Say) and five phytophagous species: Chinavia marginatum (Palisot de Beauvois), Euschistus servus (Say), N. viridula, Piezodorus guildinii (Westw.), and Proxys punctulatus (Palisot de Beauvois). Hymenopteran parasitoids that emerged from these eggs were Telenomus pentatomus Kieff, Telenomus podisi Ashmead, Trissolcus basalis (Wollaston), Trissolcus eddessae Fouts, and a Gryon sp. The most common scelionids, T. podisi and T. basalis, attacked both predaceous and phytophagous stink bugs. Trissolcus basalis also emerged from egg masses of N. viridula collected from sweet alyssum in Florida (Haseeb et al. 2018). Additionally, Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) was reported as a new parasitoid of Megacopta cribaria F. (Hemiptera: Pentatomidae) in Florida (Diedrick et al. 2020).

Before egg parasitoids can be used in augmentative biological control against invasive stink bugs in Florida and the southeastern U.S., the parasitoid species must be identified and their host associations and abundance determined. The objectives of this study therefore were to: 1) deploy previously frozen nonviable H. halys and N. viridula sentinel egg masses and yellow sticky traps in peach orchards, selected vegetable crops and a vineyard to detect and determine the prevalence of their parasitoids, 2) identify the parasitoid species that emerge from the egg masses of each host species and are captured on the traps, and 3) determine the occurrence of each parasitoid species in the four sites.

2 Materials and methods

2.1 Sources of stink bug eggs

The H. halys and N. viridula eggs used in this study were derived from colonies maintained for several generations in Gainesville, Florida. Halyomorpha halys eggs were obtained from a colony established in the quarantine laboratory at the Florida Department of Agriculture and Consumer Services, Division of Plant Industry. This colony was initiated in 2011 using adults collected from Camden County, New Jersey and reared for several years at the New Jersey Department of Agriculture (NJDA), Philip Alampi Beneficial Insect Laboratory (Dorsey and Lovero 2014). The N. viridula eggs came from a colony at the University of Florida, Biosecurity Research and Extension Laboratory. This colony was founded in 2019 with specimens collected at the North Florida Research and Education Center-Suwannee Valley; Florida Agricultural and Mechanical University, Viticulture Center; University of Florida, Institute of Food and Agricultural Sciences, Plant Science Research and Education Unit; and several commercial farms in Lake County, Florida.

2.2 Stink bug rearing for sentinel eggs

Halyomorpha halys was reared in round, mesh-ventilated, polystyrene containers (BioQuip Products, Inc., Rancho Dominguez, California): 15.2 cm diameter × 5.1 cm high for first and second instar nymphs, 17.8 cm diameter × 7.6 cm high for third to fifth instar nymphs, and 8.9 cm diameter × 25.4 cm high for adults. The containers were lined with paper towel and placed in a plant growth chamber (Percival, Perry, Iowa) maintained at 26 ± 2 °C and 50–55 % relative humidity (RH) with a 16:8 L:D photoperiod (Medal et al. 2012). At night, the RH was increased to 60 % and the temperature decreased to 25 ± 2 °C. The insects were fed whole sweetcorn, snap peas, peanuts, and organic baby carrots (Funayama 2006). Distilled water was supplied on cotton balls in a 5.5 cm diameter plastic Petri dish (Thomas Scientific, Swedesboro, New Jersey). The food and water were replaced twice per week. Egg masses no more than 3 days old were collected from the paper towel three times per week and frozen at −80 °C. The colony periodically failed to produce enough egg masses so more were obtained from the original NJDA colony.

Nezara viridula was reared in 40 cm wide × 40 cm deep × 61 cm high mesh insect cages (BioQuip Products, Inc., Rancho Dominguez, California) in a room maintained at 24 ± 1 °C and 50 % RH with a 16:8 L:D photoperiod. The cages were lined with paper towel and the insects were fed organic tomatoes, shelled peanuts, organic baby carrots, and sweet corn (Jones 1985). Distilled water was dispensed on cotton balls in a 5.5 cm diameter plastic Petri dish. The food and water were replaced twice per week. The paper towel with stink bug egg masses attached was collected three times per week and the masses were removed and frozen at −80 °C (McIntosh et al. 2019). When deployed in the field, previously frozen and fresh stink bug eggs were frequently parasitized and both yielded microhymenopteran egg parasitoids (Tillman et al. 2023).

2.3 Preparation, placement and deployment of sentinel egg masses

Most of the egg masses used in this study were frozen for 1–2 months but periodically it was necessary to use egg masses frozen for a wider time range from 10 days to 4 months. Individual frozen egg masses were attached to a 3 × 3 cm square of waterproof paper (Rite in the Rain, All-Weather Universal, Tacoma, Washington) using Elmer’s glue. The number of eggs per mass was counted and recorded on the paper to assess egg loss and predation in the field. There was an average of 15 eggs per mass. The paper squares supporting egg masses were attached to leaves of plants using insect pins or placed on metal stakes within the field. Under canopies of peach trees and grapevines, egg masses were positioned at a height of approximately 1.5 m. Egg masses were placed in mixed vegetable crops on stakes at a height of approximately 20 cm, rather than on leaves, to prevent damage to marketable produce. Halyomorpha halys egg masses were located in the center of the field, and N. viridula egg masses were placed on the edges (Tillman et al. 2020).

An egg mass was deployed at each of four sites in Lake County, Florida, once per week from 4 March 2021 to 21 March 2022. Site 1 (28.926257°N, 81.903985°W) was an abandoned 1 ha peach orchard bordered by weedy areas and hardwood trees located inside a residential community. The orchard had been managed using conventional or organic practices before being used in the study. Site 2 (28.744277°N, 81.894306°W) was within a 3.2 ha vegetable farm surrounded by woodlands. Over 120 varieties of vegetable crops were rotated at the farm seasonally, particularly tomatoes, cabbage, kale, lettuce, broccoli, carrots, bok choy, onions, and peppers. Site 3 (28.625368°N, 81.771256°W) was a 28 ha muscadine grape vineyard bordered by a thin strip of forest and a lake. The study was conducted in a 10.3 ha block inside the vineyard. Site 4 (28.627127°N, 81.756309°W) was a 1 ha organic peach orchard adjacent to an orange grove. The farm had hardwood trees on the northern edge. At each of these sites, N. viridula adults were observed and the presence of H. halys was confirmed using yellow pyramid traps baited with a combination of the H. halys male aggregation pheromone and a synergistic aggregation pheromone (Trécé BMSB DUAL lure; Trécé Pherocon; Adair, Oklahoma).

2.4 Recovery and parasitism of sentinel egg masses

The egg masses were exposed in the field for 72 h, then collected and transported to the quarantine facility at the University of Florida, Entomology and Nematology Department, and held for parasitoid emergence in sealed 10 cm diameter × 2.5 cm high polystyrene Petri dishes. Eggs in the masses were recounted to determine losses in the field. The quarantine laboratory was maintained at 26 ± 2 °C and 50–55 % RH with a 16:8 L:D photoperiod monitored with a HOBO MS 1101 data logger (Onset, Bourne, Massachusetts). The egg masses were observed daily for 4 weeks to record emergence of parasitoid adults. Parasitoids were stored in labeled vials containing 95 % ethanol and identified morphologically using the keys of Johnson and Masner (1985) for Psix, Burks (1967) for Anastatus, Talamas et al. (2015) for Trissolcus, and Goulet and Huber (1993) for all other hymenopteran taxa.

2.5 Deployment and assessment of yellow sticky traps

Three 12.7 × 8.9 cm yellow sticky traps (BASF; Ludwigshafen, Germany) were deployed at each site along with the sentinel eggs. At Sites 1 and 4, the traps were located within the central rows of the orchards. The traps were positioned along the edges of the crops at Sites 2 and 3. After 72 h in the field, the traps were placed in individual plastic Ziploc food storage bags (SC Johnson, Racine, Wisconsin), returned to the laboratory, and stored at 4–5 °C until the parasitoids were identified using the keys referenced previously for the sentinel egg masses.

2.6 Molecular analysis

DNA was extracted from whole specimens (Birkmire et al. 2021) and a NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, Waltham, Massachusetts) was used to quantify the extracts. Using primers LCO1490 and HCO2198 (Folmer et al. 1994), the 5′-CO1 barcode region was amplified. CO1 barcoding failed in a few samples of some Encyrtidae. Therefore, a fragment of 28S D2-D3 also was targeted for PCR analysis and sequenced using the primer 28S-D23F/28S-b (Park and Foighil 2000; Whiting et al. 1997). HiFi HotStart DNA Polymerase (Kapa Biosystems, Wilmington, Massachusetts) was used for the PCR analysis with a volume of 25 µL. PCR products were verified by electrophoresis in 1.5 % agarose gels and purified in preparation for sequencing with a QIAquick Gel Extraction Kit (QIAGEN Group, Hilden, Germany). Using the BigDye Terminator v3.1 on a SeqStudio Genetic Analyzer (Applied Biosystems, Thermo Fischer Scientific, Waltham, Massachusetts), the purified PCR products were bidirectionally sequenced. To trim the sequence reads and assemble the contigs, a Sequencher 5.4.6 (Gene Codes Corporation, Ann Arbor, Michigan) was utilized. The CO1 and 28S sequences were aligned with the default settings of MUSCLE (Edgar 2004). The resulting individual sequence alignments were concatenated for analysis. Newly generated sequences were deposited in GenBank (CO1: OR548197–OR548215, 28S: OR552762–OR552794).

Maximum-likelihood tree searches were performed in the IQ-tree web server (Trifinopoulos et al. 2016). The sequence data matrix was partitioned for each gene. The best fit model of sequence evolution was determined by the Bayesian information criteria in ModelFinder (Kalyaanamoorthy et al. 2017). Node support values were calculated using 10,000 ultrafast bootstrap replicates (Hoang et al. 2017). The bootstrap consensus tree was visualized in the Interactive Tree of Life v5 web portal (Letunic and Bork 2021). Additionally, parasitoid 28S sequences were queried to GenBank via MegaBLAST searches to assess matches to available data (Altschul et al. 1990; Morgulis et al. 2008). Parasitoid CO1 sequences were queried to the BOLD identification portal (Ratnasingham and Hebert 2007).

3 Results

3.1 Parasitoid species from host eggs and traps

A total of 61 parasitoids emerged from the sentinel eggs deployed in Central Florida (Table 1). Initially, approximately 3,300 egg masses were deployed, 50 % from each host, and 1,472 eggs were recovered. Many eggs disappeared but others were damaged by predators that punctured and chewed through the chorions. The 61 parasitoids obtained from the intact eggs included 11 species, Anastatus tenuipes (Bolivar y Pieltain), Anastatus sp. 1, and Anastatus nr. hirtus (Ashmead) being the most common. The other eight species were obtained only 1–2 times. Of the 11 species, five came exclusively from H. halys eggs, two from N. viridula eggs, and four from both hosts. The overall parasitism was about 4 % (61/1,472). Site 1 produced the highest percentage of parasitized egg masses (41 %), followed in order by Sites 2 (39 %), 3 (13 %), and 4 (7 %). The yellow sticky traps captured 26 egg parasitoids in four genera: Telenomus (18), Hadronotus (6), Psix (1), and Trissolcus (1). Telenomus spp. were obtained from all four sites, Hadronotus from Sites 1–3, Psix from Site 2, and Trissolcus from Site 3.

Table 1:

Parasitoid species that emerged from Halyomorpha halys and Nezara viridula sentinel egg masses deployed in Central Florida.

Species Number recovered Sitea Sex ratio ♀:♂ Months recovered Host egg species
Anastatus sp. 1 17 2, 3, 4 0:17 April–December H. halys

N. viridula
Anastatus mirabilis 1 3 0:1 July H. halys
Anastatus nr. hirtus 6 1, 2 6:0 April–June H. halys

N. viridula
Anastatus tenuipes 26 1, 2, 3 26:1 April–September H. halys

N. viridula
Ooencyrtus sp. 1 2 4 2:0 October N. viridula
Ooencyrtus sp. 2 1 1 1:0 June H. halys
Ooencyrtus johnsoni 2 2:0 April–May H. halys
Psix striaticeps 1 2 1:0 June N. viridula
Trissolcus brochymenae 1 2 1:0 April H. halys
Trissolcus hullensis 2 2 2:0 May, December H. halys
Trissolcus solocis 2 1, 4 1:1 March, December H. halys

N. viridula

  1. aSite 1 abandoned peach orchard, Site 2 vegetable farm, Site 3 vineyard, and Site 4 organic peach orchard.

3.2 Morphological and molecular identification of parasitoid species

Of the 61 parasitoids that emerged from the sentinel egg masses, 36 were suitable for identification using morphological and molecular methods (Supplementary 1). These specimens comprised 11 species that were used to construct a phylogenetic tree with 13 strongly supporting nodes and terminal clusters (Figure 1). The species groupings included Psix striaticeps (Dodd), Trissolcus brochymenae (Ashmead), Trissolcus hullensis (Harrington), Trissolcus solocis (Johnson), Ooencyrtus sp. 1, Ooencyrtus sp. 2, Ooencyrtus johnsoni, Anastatus nr. hirtus, Anastatus sp. 1, A. tenuipes, and Anastatus mirabilis (Walsh and Riley). Anastatus sp. included 13 specimens that could not be identified to species.

Figure 1: Maximum-likelihood bootstrap consensus tree of concatenated 28S and CO1 sequences for parasitoids that emerged from Halyomorpha halys and Nezara viridula sentinel egg masses deployed in Central Florida. Molecular operational taxonomic units are highlighted by color. Ultrafast bootstrap support values ≥95 % appear under the corresponding branches.
Figure 1:

Maximum-likelihood bootstrap consensus tree of concatenated 28S and CO1 sequences for parasitoids that emerged from Halyomorpha halys and Nezara viridula sentinel egg masses deployed in Central Florida. Molecular operational taxonomic units are highlighted by color. Ultrafast bootstrap support values ≥95 % appear under the corresponding branches.

The models used in the IQtree analysis included TIM3e+I (LogL = −2,486.3580; BIC = 5,005.4284) and K3Pu+F+G4 (LogL = −2,973.4944; BIC = 5,005.4284). Through CO1 barcoding, we confirmed our morphological identifications of P. striaticeps, T. brochymenae, T. hullensis, and T. solocis. The molecular analysis suggested three species of Ooencyrtus, and five species of Anastatus: A. tenuipes, A. mirabilis and three undetermined species, one of which was near A. hirtus.

4 Discussion

The 1,472 recovered host eggs yielded 61 parasitoids that comprised 11 species in four genera: Anastatus, Ooencyrtus, Psix, and Trissolcus. Anastatus sp. 1, A. mirabilis, A. nr. hirtus, A. tenuipes, Ooencyrtus sp. 2, O. johnsoni (Howard), T. brochymenae, T. hullensis, and T. solocis were obtained from H. halys egg masses. This is the first time these host-parasitoid interactions were found in Florida. It is important to note that the eggs had been frozen and were not viable, fresh eggs have a much higher incidence of parasitism (Tillman et al. 2023). Trissolcus brochymenae, T. solocis, an Ooencyrtus sp. and A. mirabilis emerged from H. halys eggs in Georgia (Tillman et al. 2023). In the current study in Central Florida, N. viridula eggs yielded Anastatus sp. 1, A. nr. hirtus, A. tenuipes, Ooencyrtus sp. 1, P. striaticeps, and T. solocis. Species of Ooencyrtus, Trissolcus and Telenomus emerged from sentinel eggs of N. viridula in Georgia (Tillman et al. 2023). Two of the parasitoid species, Anastatus nr. hirtus and A. tenuipes, are new host records for H. halys and N. viridula in the U.S. Anastatus tenuipes is a widespread parasitoid of cockroach eggs (Burks 1967), so our retrieval of this specimen from stink bug eggs is noteworthy and may indicate a host shift in this species. Alternatively, it may represent an undescribed species that cannot presently be distinguished from A. tenuipes, and will require a taxonomic revision for resolution. Except for the new records and T. hullensis, most of the parasitoid species that emerged from these hosts in Florida were previously reported in Georgia and Alabama (Balusu et al. 2019a,b; Birkmire et al. 2021; Tillman 2011, 2016; Tillman et al. 2020).

The number of parasitoid species obtained from sentinel eggs exposed at the four sites varied due to differences in the crops, borders and management practices. The greatest number of species (6) came from eggs located at Site 2, the vegetable farm surrounded by woodlands. Included were three Anastatus spp. and two Trissolcus spp. plus P. striaticeps. Fewer species (4) emerged from eggs recovered in the unmanaged peach orchard, Site 1, two Anastatus spp., Ooencyrtus sp. 2, and T. solocis. The fewest species (3 each) were from Site 3, the vineyard, and Site 4, the organic peach orchard. Eggs from Site 3 yielded only Anastatus spp., whereas Anastatus sp. 1, Ooencyrtus sp. 1, and T. solocis emerged from eggs at Site 4. Thus, Anastatus spp. were encountered at all four sites, Trissolcus spp. were present at all except the vineyard, Ooencyrtus spp. were at the peach orchards, and P. striaticeps occurred only at the vegetable farm. Various species of Anastatus, Ooencyrtus, and Trissolcus have been collected from H. halys sentinel eggs in woodland, orchard, vegetable, row crop, and vineyard habitats in Alabama and Georgia (Tillman et al. 2020). An Ooencyrtus sp. was the most abundant in vegetables but also was common in woodlands, orchards, row crops, and vineyards (Tillman et al. 2020). Trissolcus brochymenae and A. mirabilis also were prevalent in woodland and orchard habitats (Tillman et al. 2023).

Yellow sticky traps captured Telenomus and Hadronotus species that did not emerge from sentinel eggs. However, the sticky traps trapped fewer than half as many parasitoids as were obtained from egg masses. Psix striaticeps came from both sentinel eggs and sticky traps deployed at the vegetable farm. Now that many egg parasitoids of H. halys and N. viridula have been detected in Florida, they can be evaluated for augmentative biological control of invasive pentatomids.

The 28S and CO1 sequencing partially identified 36 parasitoids that emerged from H. halys and N. viridula sentinel egg masses deployed in Florida crops (Table S1). Seven were identified to species: P. striaticeps, T. brochymenae, T. hullensis, T. solocis, O. johnsoni, A. tenuipes, and A. mirabilis (Figure 1). The remainder of the molecular identifications were only to genus. Molecular data (28S) was inadequate to identify 17 of 20 Anastatus parasitoids to species. Advances in the phylogenetics of Eupelmidae may result in the development of better primers for this taxon.

This initial survey of egg parasitoids based on recovery of N. viridula and H. halys sentinel egg masses and sticky traps revealed several previously unknown parasitoid–host associations in Central Florida. Two species parasitized only N. viridula eggs, five only H. halys eggs, and four both host species, including the scelionid, T. solocis, and eupelmids Anastatus sp. 1, A. nr. hirtus, and A. tenuipes. Anastatus spp. were the most abundant and occurred in all the habitats. They separated into four clades: 1) A. nr. hirtus and an unidentified Anastatus sp., 2) two Anastatus sp., 3) A. tenuipes, and 4) A. mirabilis plus 13 unidentified Anastatus sp. specimens. Anastatus mirabilis parasitized H. halys but the host range could not be determined for the other 13 specimens. The potential host range is also unknown for the scelionid, P. striaticeps, that was discovered in Florida in 2021 (Birkmire et al. 2021). It has been recovered from wild egg masses of the pentatomids, Chinavia marginata (Palisot) and N. viridula, and coreid, Clavigralla scutellaris (Westwood) (synonym Acanthomia brevirostris Stål). In our study, overall parasitism of the stinkbugs was about 4 % but this low level could have been due to the sampling methods and limitations. The potential for using any of these hymenopteran egg parasitoids for biological control of pest stink bugs will depend on identifying each species and determining its host range, seasonal abundance, geographic distribution, and impact.

Corresponding author: Norman C. Leppla, Entomology and Nematology Department, University of Florida, 1881 Natural Area Drive, Gainesville, FL 32611, USA, E-mail:

Funding source: USDA, ARS, Floriculture and Nursery Research Initiative (FNRI)

Award Identifier / Grant number: 58-6034-3-009

Funding source: USDA, APHIS, PPQ, Plant Protection Act

Award Identifier / Grant number: AP20PPQFO000C390

Acknowledgments

We thank Jennifer Carr, Heather Kalaman, Jordyn Diaz, and Sarah Tafel of the UF Biosecurity Research and Extension (BRE) Laboratory for the rearing N. viridula and Nicole Benda and Daniel Freed at Florida Department of Agriculture and Consumer Services, Division of Plant Industry (FDACS-DPI) for rearing H. halys. Adam Pitcher and Cameron Zuck of the UF, BRE Laboratory assisted with preparation and placement of sentinel egg masses. We also thank Amy Murdock of Lady Lake Peaches, Jessica Gentry of Bountiful Farms, Benny McLean of Uncle Matt’s Citrus, and Ron Guzzetta of Lakeridge Winery for providing the field sites where we deployed sentinel eggs and sticky cards. Elijah Talamas and Matthew Moore were supported by the FDACS-DPI.

  1. Research ethics: Not applicable.

  2. Informed consent: Not applicable.

  3. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  4. Use of Large Language Models, AI and Machine Learning Tools: None declared.

  5. Conflict of interest: The authors state no conflict of interest.

  6. Research funding: USDA, APHIS, PPQ, Plant Protection Act Agreement No. AP20PPQFO000C390 entitled “Characterization of Brown Marmorated Stink Bug Establishment in Florida to Support Biological Control and Mitigation.” Additional funding was provided by the USDA, ARS, Floriculture and Nursery Research Initiative (FNRI); Agreement Number 58-6034-3-009.

  7. Data availability: Available data on the molecular analysis is in the attached Supplementary Material. Newly generated sequences were deposited in GenBank (CO1: OR548197-OR548215, 28S: OR552762-OR552794). Data in master’s thesis available at University of Florida digital collections (https://ufdc.ufl.edu/UFE0059564/00001/pdf).

References

Abram, P.K., Hoelmer, K.A., Acebes-Doria, A., Andrews, H., Beers, E.H., Bergh, J.C., Bessin, R., Biddinger, D., Botch, P., Buffington, M.L., et al.. (2017). Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. J. Pest Sci. 90: 1009–1020, https://doi.org/10.1007/s10340-017-0891-7.Suche in Google Scholar

Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403–410, https://doi.org/10.1016/S0022-2836(05)80360-2.Suche in Google Scholar PubMed

Balusu, R.R., Cottrell, T.E., Talamas, E.J., Toews, M.D., Blaauw, B.R., Sial, A.A., Buntin, D.G., Vinson, E.L., Fadamiro, H.Y., and Tillman, G.P. (2019a). New record of Trissolcus solocis (Hymenoptera: Scelionidae) parasitizing Halyomorpha halys (Hemiptera: Pentatomidae) in the United States of America. Biodivers. Data J. 7: e30124, https://doi.org/10.3897/BDJ.7.e30124.Suche in Google Scholar PubMed PubMed Central

Balusu, R.R., Talamas, E.J., Cottrell, T.E., Toews, M.D., Blaauw, B.R., Sial, A.A., Buntin, D.G., Fadamiro, H.Y., and Tillman, G.P. (2019b). First record of Trissolcus basalis (Hymenoptera: Scelionidae) parasitizing Halyomorpha halys (Hemiptera: Pentatomidae) in the United States. Biodivers. Data J. 7: e39247, https://doi.org/10.3897/BDJ.7.e39247.Suche in Google Scholar PubMed PubMed Central

Birkmire, S. (2022). Assessment of egg parasitoids of Halyomorpha halys (Stål) and Nezara viridula (L.) in Central Florida, M.S. thesis. Gainesville, Florida, USA, University of Florida.Suche in Google Scholar

Birkmire, S., Penca, C., Talamas, E.J., Moore, M.R., and Hodges, A.C. (2021). Psix striaticeps (Dodd) (Hymenoptera, Scelionidae): an Old World parasitoid of stink bug eggs arrives in Florida, USA. J. Hymenopt. Res. 87: 503–521, https://doi.org/10.3897/jhr.87.76191.Suche in Google Scholar

Burks, B.D. (1967). The North American species of Anastatus Motschulsky (Hymenoptera, Eupelmidae). Trans. Am. Entomol. Soc. 93: 423–432.Suche in Google Scholar

Cornelius, M.L., Dieckhoff, C., Hoelmer, K.A., Olsen, R.T., Weber, D.C., Herlihy, M.V., Talamas, E.J., Vinyard, B.T., and Greenstone, M.H. (2016). Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys (Stål) in Mid-Atlantic USA ornamental landscapes. Biol. Control 103: 11–20, https://doi.org/10.1016/j.biocontrol.2016.07.011.Suche in Google Scholar

Dieckhoff, C., Tatman, K.M., and Hoelmer, K.A. (2017). Natural biological control of Halyomorpha halys by native egg parasitoids: a multi-year survey in northern Delaware. J. Pest. Sci. 90: 1143–1158, https://doi.org/10.1007/s10340-017-0868-6.Suche in Google Scholar

Diedrick, W.A., Kanga, L.H., Haseeb, M., Legaspi, J.C., and Srivastava, M. (2020). First record of Ooencyrtus nezarae (Hymenoptera: Encyrtidae), a parasitoid of Megacopta cribraria (Hemiptera: Plataspidae) in Florida. Fla. Entomol. 103: 293–295, https://doi.org/10.1653/024.103.0222.Suche in Google Scholar

Dorsey, T.W. and Lovero, A. (2014). NJDA Non-diapause laboratory rearing and colony maintenance of the brown marmorated stink bug, Halyomorpha halys. New Jersey Department of Agriculture Trenton, New Jersey, https://www.northeastipm.org/neipm/assets/File/BMSB-Resources/BMSB-IWG-Dec-2014/5-NJDA-Non-Diapause-Laboratory-Rearing-Dorsey-Lovero-Mayer.pdf (Accessed 17 June 2025).Suche in Google Scholar

Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797, https://doi.org/10.1093/nar/gkh340.Suche in Google Scholar PubMed PubMed Central

Eger, J.E., Ames, L.M., Suiter, D.R., Jenkins, T.M., Rider, D.A., and Halbert, S.E. (2010). Occurrence of the Old World bug Megacopta cribraria (Fabricius) (Heteroptera: Plataspidae) in Georgia: a serious home invader and potential legume pest. Insecta Mundi 0121: 1–11.Suche in Google Scholar

Esquivel, J.F., Musolin, D.L., Jones, W.A., Rabitsch, W., Greene, J.K., Toews, M.D., Schwertner, C.F., Grazia, J., and McPherson, R.M. (2018). Nezara viridula (L.). In: McPherson, J.E. (Ed.). Invasive stink bugs and related species (Pentatomoidea). CRC Press, Boca Raton, Florida, pp. 351–423.10.1201/9781315371221-7Suche in Google Scholar

FDACS (Florida Department of Agriculture and Consumer Services) (2024). Florida Agricultural Statistics Service (FASS), https://www.fdacs.gov/Agriculture-Industry/Florida-Agricultural-Statistics-Service (Accessed 17 June 2025).Suche in Google Scholar

Folmer, O., Black, M., Hoeh, W., Lutz, T., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3: 294–299.Suche in Google Scholar

Funayama, K. (2006). A new rearing method using carrots as food for the brown-marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). Appl. Entomol. Zool. 41: 415–148, https://doi.org/10.1303/aez.2006.415.Suche in Google Scholar

Goulet, H. and Huber, J.T. (1993). Hymenoptera of the world: an identification guide to families. Agriculture Canada, Ottawa, Canada.Suche in Google Scholar

Haseeb, M., Gordon, T.L., Kanga, L.H., and Legaspi, J.C. (2018). Abundance of natural enemies of Nezara viridula (Hemiptera: Pentatomidae) on three cultivars of sweet alyssum. J. Appl. Entomol. 142: 847–853, https://doi.org/10.1111/jen.12552.Suche in Google Scholar

Hayk, K., Knuth, M., Hodges, A., and Hall, C. (2022). Florida nursery and landscape industry economic contributions report. University of Florida Institute of Food and Agricultural Sciences Electronic Data Information System FE1114. https://doi.org/10.32473/edis-fe1114-2022.Suche in Google Scholar

Hirose, Y. (1986). Biological and ecological comparison of Trichogramma and Telenomus as control agents of lepidopterous pests. Z. Angew. Entomol. 101: 39–47, https://doi.org/10.1111/j.1439-0418.1986.tb00831.x.Suche in Google Scholar

Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q., and Vinh, L.S. (2017). UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35: 518–522, https://doi.org/10.1093/molbev/msx281.Suche in Google Scholar PubMed PubMed Central

Johnson, N.F. and Masner, L. (1985). Revision of the genus Psix Kozlov and Lȇ (Hymenoptera: Scelionidae). Syst. Entomol. 10: 33–58, https://doi.org/10.1111/j.1365-3113.1985.tb00562.x.Suche in Google Scholar

Jones, W.A. (1985). Nezara viridula. In: Singh, P. and Moore, R.F. (Eds.). Handbook of insect rearing, 1. Elsevier, New York, pp. 339–343.Suche in Google Scholar

Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A., and Jermiin, L.S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14: 587–589, https://doi.org/10.1038/nmeth.4285.Suche in Google Scholar PubMed PubMed Central

Koppel, A.L., Herbert, D.A., Kuhar, T.P., and Kamminga, K. (2009). Survey of stink bug (Hemiptera: Pentatomidae) egg parasitoids in wheat, soybean, and vegetable crops in Southeast Virginia. Environ. Entomol. 38: 375–379, https://doi.org/10.1603/022.038.0209.Suche in Google Scholar PubMed

Leppla, N.C., Stacey, K.J., Rooney, L.M., Lennon, K.M., and Hodges, A.C. (2023). Stink bug (Hemiptera: Pentatomidae) occurrence, reproduction, and injury to fruit in an organic tomato crop bordered by sorghum. J. Econ. Entomol. 116: 144–152, https://doi.org/10.1093/jee/toac194.Suche in Google Scholar PubMed

Leskey, T.C., Hamilton, G.C., Nielsen, A.L., Polk, D.F., Rodriguez-Saona, C., Bergh, J.C., Herbert, D.A., Kuhar, T.P., Pfeiffer, D., Dively, G.P., et al.. (2012). Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag. 23: 218–226, https://doi.org/10.1564/23oct07.Suche in Google Scholar

Letunic, I. and Bork, P. (2021). Interactive tree of life (iTOL) v5. An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49: W293–W296, https://doi.org/10.1093/nar/gkab301.Suche in Google Scholar PubMed PubMed Central

Martel, G.M., Augé, M., Talamas, E., Roche, M., Smith, L., and Sforza, R.F.H. (2019). First laboratory evaluation of Gryon gonikopalense (Hymenoptera: Scelionidae), as potential biological control agent of Bagrada hilaris (Hemiptera: Pentatomidae). Biol. Control 135: 48–56, https://doi.org/10.1016/j.biocontrol.2019.04.014.Suche in Google Scholar

McIntosh, H., Lowenstein, D.M., Wiman, N.G., Wong, J.S., and Lee, J.C. (2019). Parasitism of frozen Halyomorpha halys eggs by Trissolcus japonicus: applications for rearing and experimentation. Biocontrol Sci. Technol. 29: 478–493, https://doi.org/10.1080/09583157.2019.1566439.Suche in Google Scholar

McPherson, J.E. (2018). Invasive stink bugs and related species (Pentatomoidea). CRC Press, Boca Raton, Florida.10.1201/9781315371221Suche in Google Scholar

Medal, J., Smith, T., Fox, A., Santa Cruz, A., Poplin, A., and Hodges, A. (2012). Rearing the brown marmorated stink bug Halyomorpha halys (Heteroptera: Pentatomidae). Fla. Entomol. 95: 800–802, https://doi.org/10.1653/024.095.0339.Suche in Google Scholar

Moonga, M.N., Kamminga, K., and Davis, J.A. (2018). Status of stink bug (Hemiptera: Pentatomidae) egg parasitoids in soybeans in Louisiana. Environ. Entomol. 47: 1459–1464, https://doi.org/10.1093/ee/nvy154.Suche in Google Scholar PubMed

Morgulis, A., Coulouris, G., Raytselis, Y., Madden, T.L., Agarwala, R., and Schäffer, A.A. (2008). Database indexing for production MegaBLAST searches. Bioinformatics 15: 1757–1764, https://doi.org/10.1093/bioinformatics/btn322.Suche in Google Scholar PubMed PubMed Central

Nakasuji, F., Nobuhiko, H., and Kiritani, K. (1966). Assessment of the potential efficiency of parasitism in two competitive scelionid parasites of Nezara viridula L. (Hemiptera: Pentatomidae). Appl. Entomol. Zool. 1: 113–119, https://doi.org/10.1303/aez.1.113.Suche in Google Scholar

Ogburn, E.C., Bessin, R., Dieckhoff, C., Dobson, R., Grieshop, M., Hoelmer, K.A., Mathews, C., Moore, J., Nielsen, A.L., Poley, K., et al.. (2016). Natural enemy impact on eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in organic agroecosystems: a regional assessment. Biol. Control 101: 39–51, https://doi.org/10.1016/j.biocontrol.2016.06.002.Suche in Google Scholar

Orr, D.B. (1988). Scelionid wasps as biological control agents: a review. Fla. Entomol. 71: 506–528, https://doi.org/10.2307/3495011.Suche in Google Scholar

Orr, D.B., Russin, J.S., Boethel, D.J., and Jones, W.A. (1986). Stink bug (Hemiptera: Pentatomidae) egg parasitism in Louisiana soybeans. Environ. Entomol. 15: 1250–1254, https://doi.org/10.1093/ee/15.6.1250.Suche in Google Scholar

Palumbo, J.C. and Natwick, E.T. (2010). The bagrada bug (Hemiptera: Pentatomidae): a new invasive pest of cole crops in Arizona and California. Plant Health Prog. 11: 50, https://doi.org/10.1094/PHP-2010-0621-01-BR.Suche in Google Scholar

Palumbo, J.C., Perring, T.M., Millar, J.G., and Reed, D.A. (2016). Biology, ecology, and management of an invasive stink bug, Bagrada hilaris, in North America. Annu. Rev. Entomol. 61: 453–473, https://doi.org/10.1146/annurev-ento-010715-023843.Suche in Google Scholar PubMed

Panizzi, A.R. (2015). Growing problems with stink bugs (Hemiptera: Heteroptera: Pentatomidae): species invasive to the U.S. and potential Neotropical invaders. Am. Entomol. 61: 223–233, https://doi.org/10.1093/ae/tmv068.Suche in Google Scholar

Panizzi, A.R., McPherson, J.E., James, D.G., Javahery, M., and McPherson, B.A. (2000). Stink bugs (Pentatomidae). In: Schaefer, C.W. and Panizzi, A.R. (Eds.). Heteroptera of economic importance. CRC Press, Boca Raton, Florida, pp. 421–474.10.1201/9781420041859.ch13Suche in Google Scholar

Park, J. and Foighil, D.O. (2000). Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments. Mol. Phylogenet. Evol. 14: 75–88, https://doi.org/10.1006/mpev.1999.0691.Suche in Google Scholar PubMed

Penca, C. and Hodges, A.C. (2018). First report of brown marmorated stink bug (Hemiptera: Pentatomidae) reproduction and localized establishment in Florida. Fla. Entomol. 101: 708–711, https://doi.org/10.1653/024.101.0413.Suche in Google Scholar

Ratnasingham, S. and Herbert, P.D.N. (2007). BOLD: the barcode of life data system. Mol. Ecol. Notes 7: 355–364, https://doi.org/10.1111/j.1471-8286.2007.01678.x.Suche in Google Scholar PubMed PubMed Central

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.. (2014). Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J. Integr. Pest Manag. 5: A1–A13, https://doi.org/10.1603/IPM14002.Suche in Google Scholar

Talamas, E.J., Bremer, J.S., Moore, M.R., Bon, M.C., Lahey, Z., Roberts, C.G., Combee, L.A., McGathey, N., van Noort, S., Timokhov, A.V., et al.. (2021). A maximalist approach to the systematics of a biological control agent: Gryon aetherium Talamas, sp. nov. (Hymenoptera, Scelionidae). In: Lahey, Z. and Talamas, E.J. (Eds.), Advances in the systematics of Platygastroidea III. J. Hymenopt. Res. 87: 323–480. https://doi.org/10.3897/jhr.87.72842 Suche in Google Scholar

Talamas, E.J., Johnson, N.F., and Buffington, M. (2015). Key to Nearctic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), natural enemies of native and invasive stink bugs (Hemiptera, Pentatomidae). J. Hymenopt. Res. 43: 45–110, https://doi.org/10.3897/JHR.43.8560.Suche in Google Scholar

Temerak, S.A. and Whitcomb, W.H. (1984). Parasitoids of predaceous and phytophagous pentatomid bugs in soybean fields at two sites of Alachua County, Florida. Z. Angew. Entomol. 97: 279–282, https://doi.org/10.1111/j.1439-0418.1984.tb03749.x.Suche in Google Scholar

Tillman, P.G. (2010). Parasitism and predation of stink bug (Heteroptera: Pentatomidae) eggs in Georgia corn fields. Environ. Entomol. 39: 1184–1194, https://doi.org/10.1603/EN09323.Suche in Google Scholar PubMed

Tillman, P.G. (2011). Natural biological control of stink bug (Heteroptera: Pentatomidae) eggs in corn, peanut, and cotton farmscapes in Georgia. Environ. Entomol. 40: 303–314, https://doi.org/10.1603/EN10154.Suche in Google Scholar

Tillman, P.G. (2016). Diversity of stink bug (Hemiptera: Pentatomidae) egg parasitoids in woodland and crop habitats in southwest Georgia, USA. Fla. Entomol. 99: 286–291, https://doi.org/10.1653/024.099.0220.Suche in Google Scholar

Tillman, P.G., Grabarczyk, E.E., Balusu, R., Kesheimer, K., Blaauw, B., Sial, A., Vinson, E., and Cottrell, T.E. (2023). Predation and parasitism of naturally occurring and sentinel stink bug egg masses of Halyomorpha halys (Stål) and Nezara viridula (L.) (Hemiptera: Pentatomidae) in various southeastern habitats. J. Insect Sci. 23: 9, https://doi.org/10.1093/jisesa/iead012.Suche in Google Scholar PubMed PubMed Central

Tillman, P.G., Toews, M., Blaauw, B., Sial, A., Cottrell, T., Talamas, E., Buntin, D., Joseph, S., Balusu, R., Fadamiro, H., et al.. (2020). Parasitism and predation of sentinel eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in the southeastern US. Biol. Control 145: 104247, https://doi.org/10.1016/j.biocontrol.2020.104247.Suche in Google Scholar

Todd, J.W. (1989). Ecology and behavior of Nezara viridula. Annu. Rev. Entomol. 34: 273–292, https://doi.org/10.1146/annurev.ento.34.1.273.Suche in Google Scholar

Trifinopoulos, J., Nguyen, L.T., von Haeseler, A., and Minh, B.Q. (2016). W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44: W232–W235, https://doi.org/10.1093/nar/gkw256.Suche in Google Scholar PubMed PubMed Central

Turner, J.W. (1983). Influence of plant species on the movement of Trissolcus basalis Wollaston (Hymenoptera: Scelionidae)-a parasite of Nezara viridula L. Aust. J. Entomol. 22: 271–272, https://doi.org/10.1111/j.1440-6055.1983.tb01895.x.Suche in Google Scholar

Whiting, M.E., Carpenter, J.C., Wheeler, Q.D., and Wheeler, W.C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst. Biol. 46: 1–68, https://doi.org/10.1093/sysbio/46.1.1.Suche in Google Scholar PubMed

Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/flaent-2025-0015).

Received: 2025-05-02
Accepted: 2025-07-26
Published Online: 2025-09-25

© 2025 the author(s), published by De Gruyter on behalf of the Florida Entomological Society

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

  1. Frontmatter
  2. Research Articles
  3. Parasitism of Halyomorpha halys and Nezara viridula (Hemiptera: Pentatomidae) sentinel eggs in Central Florida
  4. Genetic differentiation of three populations of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), in Mexico
  5. Tortricidae (Lepidoptera) associated with blueberry cultivation in Central Mexico
  6. First report of Phidotricha erigens (Lepidoptera: Pyralidae: Epipaschiinae) injuring mango inflorescences in Puerto Rico
  7. Seed predation of Sabal palmetto, Sabal mexicana and Sabal uresana (Arecaceae) by the bruchid Caryobruchus gleditsiae (Coleoptera: Bruchidae), with new host and distribution records
  8. Genetic variation of rice stink bugs, Oebalus spp. (Hemiptera: Pentatomidae) from Southeastern United States and Cuba
  9. Selecting Coriandrum sativum (Apiaceae) varieties to promote conservation biological control of crop pests in south Florida
  10. First record of Mymarommatidae (Hymenoptera) from the Galapagos Islands, Ecuador
  11. First field validation of Ontsira mellipes (Hymenoptera: Braconidae) as a potential biological control agent for Anoplophora glabripennis (Coleoptera: Cerambycidae) in South Carolina
  12. Field evaluation of α-copaene enriched natural oil lure for detection of male Ceratitis capitata (Diptera: Tephritidae) in area-wide monitoring programs: results from Tunisia, Costa Rica and Hawaii
  13. Abundance of Megalurothrips usitatus (Bagnall) (Thysanoptera: Thripidae) and other thrips in commercial snap bean fields in the Homestead Agricultural Area (HAA)
  14. Performance of Salvinia molesta (Salviniae: Salviniaceae) and its biological control agent Cyrtobagous salviniae (Coleoptera: Curculionidae) in freshwater and saline environments
  15. Natural arsenal of Magnolia sarcotesta: insecticidal activity against the leaf-cutting ant Atta mexicana (Hymenoptera: Formicidae)
  16. Ethanol concentration can influence the outcomes of insecticide evaluation of ambrosia beetle attacks using wood bolts
  17. Post-release support of host range predictions for two Lygodium microphyllum biological control agents
  18. Missing jewels: the decline of a wood-nesting forest bee, Augochlora pura (Hymenoptera: Halictidae), in northern Georgia
  19. Biological response of Rhopalosiphum padi and Sipha flava (Hemiptera: Aphididae) changes over generations
  20. Argopistes tsekooni (Coleoptera: Chrysomelidae), a new natural enemy of Chinese privet in North America: identification, establishment, and host range
  21. A non-overwintering urban population of the African fig fly (Diptera: Drosophilidae) impacts the reproductive output of locally adapted fruit flies
  22. Fitness of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) on four economically important host fruits from Fujian Province, China
  23. Carambola fruit fly in Brazil: new host and first record of associated parasitoids
  24. Establishment and range expansion of invasive Cactoblastis cactorum (Lepidoptera: Pyralidae: Phycitinae) in Texas
  25. A micro-anatomical investigation of dark and light-adapted eyes of Chilades pandava (Lepidoptera: Lycaenidae)
  26. Scientific Notes
  27. Early stragglers of periodical cicadas (Hemiptera: Cicadidae) found in Louisiana
  28. Attraction of released male Mediterranean fruit flies to trimedlure and an α-copaene-containing natural oil: effects of lure age and distance
  29. Co-infestation with Drosophila suzukii and Zaprionus indianus (Diptera: Drosophilidae): a threat for berry crops in Morelos, Mexico
  30. Observation of brood size and altricial development in Centruroides hentzi (Arachnida: Buthidae) in Florida, USA
  31. New quarantine cold treatment for medfly Ceratitis capitata (Diptera: Tephritidae) in pomegranates
  32. A new invasive pest in Mexico: the presence of Thrips parvispinus (Thysanoptera: Thripidae) in chili pepper fields
  33. Acceptance of fire ant baits by nontarget ants in Florida and California
  34. Examining phenotypic variations in an introduced population of the invasive dung beetle Digitonthophagus gazella (Coleoptera: Scarabaeidae)
  35. Note on the nesting biology of Epimelissodes aegis LaBerge (Hymenoptera: Apidae)
  36. Mass rearing protocol and density trials of Lilioceris egena (Coleoptera: Chrysomelidae), a biological control agent of air potato
  37. Cardinal predation of the invasive Jorō spider Trichophila clavata (Araneae: Nephilidae) in Georgia
  38. Retraction
  39. Retraction of: Examining phenotypic variations in an introduced population of the invasive dung beetle Digitonthophagus gazella (Coleoptera: Scarabaeidae)
https://doi.org/10.1515/flaent-2025-0015
Schlagwörter für diesen Artikel
biological control; sentinel eggs; stink bugs; egg parasitoids; sticky traps
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Frontmatter
  2. Research Articles
  3. Parasitism of Halyomorpha halys and Nezara viridula (Hemiptera: Pentatomidae) sentinel eggs in Central Florida
  4. Genetic differentiation of three populations of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), in Mexico
  5. Tortricidae (Lepidoptera) associated with blueberry cultivation in Central Mexico
  6. First report of Phidotricha erigens (Lepidoptera: Pyralidae: Epipaschiinae) injuring mango inflorescences in Puerto Rico
  7. Seed predation of Sabal palmetto, Sabal mexicana and Sabal uresana (Arecaceae) by the bruchid Caryobruchus gleditsiae (Coleoptera: Bruchidae), with new host and distribution records
  8. Genetic variation of rice stink bugs, Oebalus spp. (Hemiptera: Pentatomidae) from Southeastern United States and Cuba
  9. Selecting Coriandrum sativum (Apiaceae) varieties to promote conservation biological control of crop pests in south Florida
  10. First record of Mymarommatidae (Hymenoptera) from the Galapagos Islands, Ecuador
  11. First field validation of Ontsira mellipes (Hymenoptera: Braconidae) as a potential biological control agent for Anoplophora glabripennis (Coleoptera: Cerambycidae) in South Carolina
  12. Field evaluation of α-copaene enriched natural oil lure for detection of male Ceratitis capitata (Diptera: Tephritidae) in area-wide monitoring programs: results from Tunisia, Costa Rica and Hawaii
  13. Abundance of Megalurothrips usitatus (Bagnall) (Thysanoptera: Thripidae) and other thrips in commercial snap bean fields in the Homestead Agricultural Area (HAA)
  14. Performance of Salvinia molesta (Salviniae: Salviniaceae) and its biological control agent Cyrtobagous salviniae (Coleoptera: Curculionidae) in freshwater and saline environments
  15. Natural arsenal of Magnolia sarcotesta: insecticidal activity against the leaf-cutting ant Atta mexicana (Hymenoptera: Formicidae)
  16. Ethanol concentration can influence the outcomes of insecticide evaluation of ambrosia beetle attacks using wood bolts
  17. Post-release support of host range predictions for two Lygodium microphyllum biological control agents
  18. Missing jewels: the decline of a wood-nesting forest bee, Augochlora pura (Hymenoptera: Halictidae), in northern Georgia
  19. Biological response of Rhopalosiphum padi and Sipha flava (Hemiptera: Aphididae) changes over generations
  20. Argopistes tsekooni (Coleoptera: Chrysomelidae), a new natural enemy of Chinese privet in North America: identification, establishment, and host range
  21. A non-overwintering urban population of the African fig fly (Diptera: Drosophilidae) impacts the reproductive output of locally adapted fruit flies
  22. Fitness of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) on four economically important host fruits from Fujian Province, China
  23. Carambola fruit fly in Brazil: new host and first record of associated parasitoids
  24. Establishment and range expansion of invasive Cactoblastis cactorum (Lepidoptera: Pyralidae: Phycitinae) in Texas
  25. A micro-anatomical investigation of dark and light-adapted eyes of Chilades pandava (Lepidoptera: Lycaenidae)
  26. Scientific Notes
  27. Early stragglers of periodical cicadas (Hemiptera: Cicadidae) found in Louisiana
  28. Attraction of released male Mediterranean fruit flies to trimedlure and an α-copaene-containing natural oil: effects of lure age and distance
  29. Co-infestation with Drosophila suzukii and Zaprionus indianus (Diptera: Drosophilidae): a threat for berry crops in Morelos, Mexico
  30. Observation of brood size and altricial development in Centruroides hentzi (Arachnida: Buthidae) in Florida, USA
  31. New quarantine cold treatment for medfly Ceratitis capitata (Diptera: Tephritidae) in pomegranates
  32. A new invasive pest in Mexico: the presence of Thrips parvispinus (Thysanoptera: Thripidae) in chili pepper fields
  33. Acceptance of fire ant baits by nontarget ants in Florida and California
  34. Examining phenotypic variations in an introduced population of the invasive dung beetle Digitonthophagus gazella (Coleoptera: Scarabaeidae)
  35. Note on the nesting biology of Epimelissodes aegis LaBerge (Hymenoptera: Apidae)
  36. Mass rearing protocol and density trials of Lilioceris egena (Coleoptera: Chrysomelidae), a biological control agent of air potato
  37. Cardinal predation of the invasive Jorō spider Trichophila clavata (Araneae: Nephilidae) in Georgia
  38. Retraction
  39. Retraction of: Examining phenotypic variations in an introduced population of the invasive dung beetle Digitonthophagus gazella (Coleoptera: Scarabaeidae)
Jetzt anmelden und 20% sparen
Institutioneller Zugang
Wie funktioniert Authentifizierung?
Haben Sie eine Idee, wie wir unsere Website verbessern können?
Bitte schreiben Sie uns.
© 2025 De Gruyter Brill
Heruntergeladen am 24.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/flaent-2025-0015/html
Button zum nach oben scrollen