The grape berry moth (GBM), Paralobesia viteana (Clemens) (Lepidoptera: Tortricidae) is a highly destructive pest of grapes in eastern North America [1]. The larvae of this insect feed on grape clusters, causing mechanical injury and increasing the vulnerability to pathogen infection, ultimately, resulting in yield losses and decreased juice and wine quality. Management of GBM currently relies on insecticide sprays timed using a degree-day model developed by Tobin et al. [2]. Although insecticides confer some protection against this insect, their constant use poses human and environmental risks and can lead to the development of GBM resistance to the chemical active substances used [3]. With the long-term goal of developing more sustainable strategies for GBM control, this study focused on the identification of larval parasitoids in ‘Concord’ (Vitis labrusca L. or Vitis x labruscana L.H. Bailey) vineyards in northwestern Pennsylvania (U.S.A).

GBM is native to eastern North America and has coevolved with numerous natural enemies in its original habitat. Studies in the Finger Lakes area (New York), the Lake Erie Region (New York and Pennsylvania), and Michigan have identified several egg and larval parasitoids of GBM (Table 1). However, these studies date back several decades, underlining the need for new surveys to identify current GBM natural enemies that have endured increases in farming land, recurrent pesticide sprays, and climate changes in grape-growing regions. In a 2-year survey conducted in the Finger Lakes region in 1986–87, the natural community of egg and larval GBM parasitoids caused 12–42% mortality throughout the growing season [4]. The most abundant parasitoid in this study was Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) to which a large percentage of GBM mortality (20.2%) was attributed. Studies conducted in Michigan vineyards reported Sinophorus Förster (Hymenoptera: Ichneumonidae) as the most abundant parasitoid causing 11–76% GBM mortality in field conditions [5]. Surveys in Arkansas vineyards found GBM parasitism of 3.6–48.6% from ichneumonid and braconid parasitoids with no detail of the species reported [6]. Although some work has been conducted in the identification of GBM natural enemies, their efficacy in reducing insect infestations in field conditions remains untested except for one egg parasitoid species, Trichogramma minutum Riley. This is a native parasitoid that was found infesting GBM eggs in northwestern Pennsylvania, but its natural parasitism rates were very low to decrease pest populations [7]. Inundative releases of T. minutum in commercial vineyards showed a significant decrease in GBM damage [8], demonstrating the potential of natural enemies for controlling this pest.

The biology and ecology of GBM make the control of this insect particularly challenging. GBM evolved with wild grape hosts and became a pest in vineyards established east of the Mississippi River [1]. Adults typically emerge from overwintered pupae between May and June [9,10]. However, the termination of diapause is variable, lasting about six weeks [10], resulting in asynchronous egg laying over the growing season. Mated females oviposit on developing buds, flower clusters, or berries from wild and cultivated grapevines [1,11]. Females lay an average of 60 eggs in their lifetime, from which more than 86% successfully hatch in controlled conditions [12]. Larvae emerge after 3–4 days and create webs in the clusters [1,9]. Early in the season, larvae feed on buds or flower clusters, whereas later in the season, they burrow into the fruit within hours of egg-hatch. Inside the grape berries, larvae remain protected against chemical control while consuming the internal tissue of the berries. The larval period takes an average of 18.5 days at 25 ± 1 °C [12]. After fully developed, fourth instar larvae exit the berry and pupate by cutting a flap in a grapevine leaf and forming a silken chamber [9,10]. The pupa stage takes an average of 9.52 days to develop at 25 ± 1 °C, and the longevity of adults is on average 15.6 days in controlled conditions [12]. The oviposition period is 7.3 days on average, with some variation associated with the grape cultivar [12]. The number of GBM generations per season varies with temperature accumulation; there are two to three generations in the Lake Erie region and central New York State [1,13–15], whereas, in southern Missouri and Arkansas, there can be up to four generations [1,16]. In the Lake Erie region, the first GBM generation develops in wild grapes (Vitis spp. L), and subsequent generations develop in cultivated grapes, where they cause significant crop losses [7]. Access to widespread wild hosts, the cryptic feeding habit of the larvae, the prolonged oviposition period of females, and the large variation of diapause termination contribute to the challenges of controlling this insect.

The variation in diapause termination results in constant GMB pressure that reduces the effectiveness of chemical control that targets peaks of egg-laying [10]. Therefore, a long-lasting control strategy that reduces pest populations over several weeks would be ideal. Biological control using egg and larval parasitoids holds great potential for controlling GBM because they may have the capability of controlling the pest for several days. Additionally, parasitoids may be able to control GBM in both wild and cultivated grapes. Augmentative releases of parasitoids have great potential to reduce GBM populations below economic injury levels [7]. Furthermore, parasitoids could offer long-lasting pest control if they successfully establish in the field, but research is needed to determine the feasibility of this strategy.

In this study, we surveyed and assessed the parasitism rates of GBM larval parasitoids in six vineyards in Erie County (Pennsylvania) throughout the 2023 and 2024 growing seasons. We also developed a graphical taxonomic key to facilitate further identification of these species. Our results provide knowledge of the current diversity of GBM larval parasitoids in commercial vineyards of northwestern Pennsylvania and would be a practical basis for future studies to test the effectiveness of the identified species in controlling GBM in field conditions.

The GBM, P. viteana has an abundant number of larval parasitoids that provide significant natural control. We successfully identified eight hymenopteran parasitoids in samples from six commercial ‘Concord’ vineyards in northwestern Pennsylvania over two consecutive years (2023 and 2024). These vineyards were conventionally managed following current spray recommendations [33], indicating that natural control still occurs despite insecticide use. Field parasitism rates varied through the growing season and ranged from 0 to 39% in 2023 and from 0 to 52.1% in 2024. This study represents a first step toward our understanding of the native natural enemies present in the Lake Erie Region and their use in pest management programs.

The community of larval parasitoids identified in this study confirms previous species records and provides new findings. E. obliteratus, C. tortricidis, B. variabilis, and Scambus spp. have been previously reported parasitizing P. viteana [4,5,18], but G. fratellus, G. cf. depressa, G. cf. ohioensis, and G. cf. ignota are new reports for this species. In our samplings, the most abundant parasitoid species was B. variabilis accounting for 56.6% (in 2023) and 68.6% (in 2024) of all parasitoids found. However, in similar studies conducted in 1986–87 in the Finger Lakes region in New York, the most abundant species was the egg parasitoid T. pretiosum, followed by the larval parasitoids A. polychrosidis, and G. mutica from the eight species found [4]. In a 3-year (2003–2005) study in Michigan vineyards, Sinophorus sp. was the most abundant parasitoid, comprising 11–76% of all the specimens collected from 12 identified species [5]. These results confirm the presence of a large number of GBM parasitoids in the eastern U.S. and suggest that the community composition and abundance of these species vary in different grape-growing regions.

The field parasitism rates fluctuated over the growing season and habitat. In 2023, the highest percent of parasitism was from samples collected in wild grapes early in the season and ranged from 0 to 71.4% (Fig 1A; S2 Table). Similar results were found by Seaman et al. [4], who reported higher parasitism in wild grapes reaching up to 65%. The highest parasitism rates in cultivated grapes were found during the first week of August and ranged from 4.5 to 22.2% in 2023 and from 2 to 52.1% in 2024 (Fig 1; S2 and S3 Tables). In contrast, the lowest percentages of parasitism were found during the second week of July 2023 and the last week of June 2024. Similarly, Jenkins et al. [34] found a low abundance of parasitoids early in the season that increased in mid-August to levels of up to 30% and declined as the season progressed. In the Lake Erie region, the first generation of GBM emerges before the cultivated grapes bloom and feeds on developing blossoms from wild grapes. In comparison to later generations that burrow into grape berries, these larvae are highly exposed to parasitoids and predators despite building protective silk enclosures. Gleisner [18] suggested that berries may protect the larva from parasitoids with short ovipositors. The variation in parasitism through the season could be associated with varying availability of appropriate GBM instars for parasitoids to use, variation in GBM infestation levels, or asynchrony between parasites and the host [5,18]. Other possibilities include changes in the availability of alternate hosts for parasitoids or differences in the timing of diapause initiation for the parasitoids and the host later in the season.

All the GBM parasitoids found in this study have alternate hosts. The most abundant parasitoid species in our samplings was the ectoparasitoid B. variabilis, whose parasitism rates ranged from 1.3–37.3% in 2023 and from 1.6–51.1% in 2024. This species was previously reported parasitizing GBM in Van Buren and Berrien Counties in Michigan and in the Finger Lakes region in NY [4,5]. Other lepidopteran hosts of B. variabilis, include the nantucket pine tip moth, Rhyacionia frustrana (Scudder) (Lepidoptera: Tortricidae) in Georgia [35], the hickory shuckworm moth, Cydia caryana (Fitch) (Lepidoptera: Tortricidae) in Texas [36], and the alder tubemaker moth, Acrobasis rubrifasciella Packard (Lepidoptera: Pyralidae) in the Eagles Nest Lakes region, near Ely, Minnesota [37]. Bracon variabilis has also been reported parasitizing the curculionid flower beetle, Baris transversa (Say & T.) [38]. The endoparasitoid E. obliteratus was the second most abundant species with parasitism rates in commercial vineyards ranging from 1.3 to 9.4% in 2023 and from 1.5 to 16.3% in 2024. This species has been previously reported parasitizing GBM in Michigan State [5]. Enytus obliteratus also parasitizes larvae of the European GBM, Lobesia botrana (Denis & Schiffermüller) [39], and larvae of the oriental fruit moth, Grapholita molesta (Busck), an important pest of stone fruits (peaches, cherries, etc). It has also been reported as a parasitoid of Arogalea cristifasciella (Chambers) (Lepidoptera: Gelechiidae) larvae [40]. This genus has primarily a Nearctic and Palearctic distribution [41]. The ectoparasitoid G. fratellus had parasitism rates that fluctuated from 5.4 to 7.7% in 2023 and from 1 to 11.2% in 2024. To our knowledge, this is the first time this species has been reported preying on GBM. G. fratellus also parasitizes Acrobasis nuxvorella Neunzig (Lepidoptera: Pyralidae) [36]. This species has been reported in several States, including California, Nevada, Arizona, New Mexico, Georgia, Texas, Florida, South Carolina, Michigan, Connecticut, Massachusetts, Ontario, and Louisiana [23], without information about the hosts. The endoparasitoid C. tortricidis had parasitism rates below 2%. This species was first found by Cushman [20] in North East, Pennsylvania, parasitizing P. viteana, and was reported again by Gleissner [18] from GBM samples gathered between 1940–1943 in the same geographic location. It was also reported parasitizing the oriental fruit moth in Ohio [42]. Information on this species is scarce and the only other geographical record besides northwestern Pennsylvania is the one in Edmonton, Canada [43,44].

There were also three species of Glypta identified in this study: G. cf. depressa, G. cf. ohioensis, and G. cf. ignota, which together had field parasitism rates below 5%. To our knowledge, this is the first report of these species parasitizing GBM and no other hosts have been reported in the literature. Information on their geographic distribution is also limited. G. cf. depressa has been recorded in New Mexico, whereas G. cf. ohioensis has been found in Ohio, Louisiana, Michigan, New York, Pennsylvania, South Carolina, West Virginia and Ontario [21]. For G. cf. ignota, there is only one report in Nova Scotia [21]. Other species of this genus, such as G. animosa, G. vulgaris, and G. mutica are known parasitoids of P. viteana [5,17]. Natural parasitism rates of G. mutica in the Finger Lakes region ranged from 0.01 to 6.4% and in caged experiments varied from 3 to 7% [4]. Glypta species in general, are known parasites of several Lepidoptera families, including Cochylidae, Gelechiidae, Geometridae, Lasiocampidae, Lycaenidae, Lymantriidae, Momphidae, Noctuidae, Pyralidae and Tortricidae. This genus is found principally in the Holarctic and is less frequent in the Neotropical and Oriental regions.

Scambus spp. was a less frequent parasitoid found in our study only in the 2023 samplings, with parasitism lower than 1%. Two species within this genus have been previously identified parasitizing P. viteana: S. brevicornis and S. hispae in Michigan vineyards [5]. However, other Scambus species have been reported parasitizing other tortricids. For example, Scambus elegans (Woldstedt) parasitize L. botrana [45], whereas Scambus calobatus (Gravenhorst) and Scambus vesicarius (Ratzeburg) parasitize the European grapevine moth, Eupoecilia ambiguella (Hübner) (Lepidoptera: Tortricidae) [46–48]. There are also reports of Scambus species parasitizing Diptera and Coleoptera insects [49–51]. This genus is widely distributed in the Northern Hemisphere [19].

The abundance of the GBM parasitoids found in this study fluctuated over the course of the growing season. E. obliteratus, C. tortricidis and Glypta spp. were only present from June to mid-August, whereas B. variabilis and G. fratellus were found from late July to September (Fig 1). This temporal variation could be associated with different thermal requirements and diapause periods for the different species and could be helpful in reducing interspecific competition of parasitoids for the same prey.

We conclude that the American GBM, P. viteana is host for several larval parasitoids in commercial ‘Concord’ vineyards in Pennsylvania. We confirmed previous species reports and added four new records to the parasitoid list of this species. The parasitoid abundance differed over the season but was greatest in early August, reaching parasitism rates of up to 52.1%. Despite their importance, information about these parasitoids is limited; future research is needed to document the biology and ecology of the most promising species to identify ways to increase their natural populations in vineyards. Measurements should be taken to protect the community of natural enemies that prey on GBM in vineyards. Some strategies, include reducing the use of broad-spectrum insecticides, using economic thresholds to determine the need for insecticide applications, and protecting wild vegetation that provides food for parasitoid adults.