Stink bugs (Hemiptera: Pentatomidae) are primary pests responsible for millions of dollars in losses and cost of control in row crops. For example, nearly 130,000 bales of cotton (Gossypium hirsutum L.; Malvales: Malvaceae) nationwide were estimated lost due to pest stink bug species in 2014 (Williams 2015). In southwest Georgia, USA, corn (Zea mays L.; Poales: Poaceae) is one of the first crops available to stink bugs for feeding and oviposition (Tillman 2011a). Euschistus servus (Say) and Nezara viridula (L.) are the predominant stink bug species in this crop. Generally, peanut (Arachis hypogaea L.; Fabales: Fabaceae) is the next crop in which these 2 stink bug species occur (Tillman 2008). Stink bugs feed on vegetative parts of peanut plants (Tillman 2008) and thus are not considered economic pests. However, when E. servus and N. viridula inhabit peanut in peanut-cotton farmscapes, it leads to a negative impact on cotton because they develop on peanut and then disperse in cotton (Tillman et al. 2009). Both corn and peanut are unlikely hosts for Chinavia hilaris (Say) (Tillman 2013). Soybean (Glycine max [L.] Merr.; Fabales: Fabaceae) and cotton, though, are mid-to-late-season crops of C. hilaris, as well as E. servus and N. viridula (Bundy & McPherson 2000; Tillman et al. 2009). In cotton, stink bugs feed on developing seeds and lint, causing shedding of young bolls, yellowing of lint, reduction in yield, and transmission of a bacterial pathogen (Barbour et al. 1990; Medrano et al. 2009). In soybean, pod feeding by stink bugs results in reduction in oil content and yield (McPherson et al. 1995).

In farmscapes in the southeastern United States, numerous noncrop hosts of C. hilaris and E. servus, including black cherry (Prunus serotina Ehrh.; Rosales: Rosaceae), elderberry (Sambucus nigra subsp. canadensis [L.] R. Bolli; Dipsacales: Adoxaceae), and mimosa (Albizia julibrissin Durazz.; Fabales: Fabaceae), exist in woodlands bordering crops (Jones & Sullivan 1982; Tillman & Cottrell 2015). Black cherry is an early-season host plant; C. hilaris adults are present on trees from Apr until early Jul, and large nymphs occur on trees from late May through mid-Jul. Elderberry is an early-to-mid-season host plant; C. hilaris adults begin colonizing this shrub in mid-May, remaining on it through Jul. Large nymphs are then present on plants from mid-Jun through Jul. In mimosa, reproductive populations of C. hilaris are present from mid-Jul through Aug. Rattlebox (Sesbania punicea [Cav.] Benth.; Fabales: Fabaceae) is a newly discovered early-season host plant for C. hilaris (Tillman 2015). Except for occasionally developing on pokeweed (Phytolacca americana L.; Caryophyllales: Phytolaccaceae) in woodland borders near crops (Tillman et al. 2014), N. viridula has not been detected in woodland habitats in southwest Georgia.

Stink bugs move within and between closely associated crop and non-crop habitats throughout the growing season in response to deteriorating suitability of their current host plants (Velasco & Walter 1992; Panizzi 1997; Ehler 2000). Habitat edges include not only crop-to-crop interfaces but also woodland habitats next to crops. For C. hilaris, an edge effect in dispersal of adults was detected in cotton adjacent to woodlands (Tillman et al. 2014), indicating that the non-crop hosts in woodlands were sources of this stink bug in this crop. Spatiotemporal distribution of C. hilaris in cotton suggested that elderberry and mimosa were sources of this stink bug dispersing into this crop (Tillman & Cottrell 2015). Preliminary mark-recapture studies have shown that C. hilaris disperses from elderberry into cotton in mid Jul to early Aug (P. G. Tillman, unpublished). The timing of completion of development of C. hilaris on elderberry and the later appearance of this stink bug in adjacent soybean suggested that elderberry also was a source of this pest into this crop (Miner 1966; Jones & Sullivan 1982).

An understanding of natural biological control of stink bugs in both woodland habitats and crops is necessary for developing effective management strategies for these pests. Multiple studies have investigated parasitism of E. servus, C. hilaris, and N. viridula egg masses in crops (Schoene & Underhill 1933; Underhill 1934; Yeargan 1979; Orr et al. 1986; Jones et al. 1996; Koppel et al. 2009; Tillman 2010, 2011b), but data on parasitism of eggs of these stink bug species in woodlands are rare (Yeargan 1979; Koppel et al. 2009). Interestingly, stink bug egg parasitoids can disperse from crop to crop throughout the seasonal succession of crops in farmscapes composed of combinations of corn, peanut, and cotton to parasitize E. servus and N. viridula egg masses (Tillman 2011b). Considering the crop-to-crop dispersal of these stink bugs, their parasitoids are likely responding to host plant switching by their hosts.

However, very little is known as to whether parasitoids of stink bugs disperse from woodland habitats into crops. Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), an Asian egg parasitoid of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), was discovered parasitizing H. halys in a woodland habitat in Beltsville, Maryland (Talamas et al. 2015a). In contrast, H. halys egg masses were not parasitized by this parasitoid in nearby soybean and an abandoned apple orchard. Information regarding stink bug egg parasitoids in woodland habitats and crops is crucial now in Georgia because reproductive populations of H. halys recently have been detected in the state (P. G. Tillman, unpublished). This study was conducted for 10 field seasons to examine parasitism of naturally occurring C. hilaris and E. servus eggs in woodland habitats and crops alongside these habitats in southwest Georgia. Also, parasitism of sentinel eggs of N. viridula was examined in a woodland habitat.

Materials and Methods

DATA ANALYSES

All data were analyzed using SAS statistical software (SAS Institute 2010). Chi-squared tests were used to compare frequencies of parasitoid species parasitizing E. servus and C. hilaris egg masses in woodland and crop habitats (PROC FREQ). For parasitoids from E. servus, analyses were grouped by woodland habitats, an early-season crop, corn, and late-season crops including peanut, cotton, and soybean. For parasitoids from C. hilaris, analyses were grouped by woodland habitats and 2 late-season crops (cotton and soybean). Parasitism rates of E. servus and C. hilaris eggs among the various habitat groups were analyzed using PROC ANOVA (P < 0.05). Means were separated using Tukey's honest significance difference (HSD) test (P < 0.05) when appropriate. Seasonal presence of parasitized stink bug egg masses was determined for the woodland habitat, the early-season crop, and late-season crops.

Table 1.

Occurrence of stink bug egg parasitoid species attacking Euschistus servus in woodland habitats, an early-season (ES) crop, and late-season (LS) crops in Irwin County, Georgia, over a 10 yr period.

Results

Ten species of parasitoids parasitized naturally occurring egg masses of E. servus (Table 1). These included 7 scelionids, 2 eupelmids, and 1 encyrtid. Telenomus podisi was the most prevalent parasitoid of E. servus eggs in each of the 3 habitats, i.e., woodland, early-season corn, and late-season crops including peanut, cotton, and soybean. In corn, the percentage of eggs parasitized by male Anastatus adults was very low, and these eggs were found on the outermost row of corn in close association with a woodland habitat. Anastatus species did not parasitize E. servus eggs in late-season crops. However, in woodland habitats, 27.9% of the eggs were parasitized by Anastatus species, including Anastatus reduvii (Howard) and A. mirabilis (Walsh & Riley) females and Anastatus males. Less than 10% of the eggs were parasitized by any other parasitoid species for each of the 3 habitats. Trissolcus edessae Fouts parasitized E. servus eggs only in the woodland habitat and late-season crops. Trissolcus basalis and G. obesum attacked E. servus eggs only in crops.

Four species of parasitoids parasitized naturally occurring egg masses of C. hilaris (Table 2). These included 1 scelionid, 2 eupelmids, and 1 encyrtid. Trissolcus edessae was the most prevalent parasitoid of C. hilaris eggs in woodland habitats and the only parasitoid attacking C. hilaris eggs in late-season crops. Egg masses of C. hilaris were not detected in peanut. For corn, the only C. hilaris egg mass detected was parasitized by T. basalis in a location where N. viridula egg masses were present. In woodland habitats, 40.7% of the C. hilaris eggs were parasitized by Anastatus, including A. reduvii and A. mirabilis females and Anastatus males.

Table 2.

Occurrence of stink bug egg parasitoid species attacking Chinavia hilaris in woodland habitats and late-season (LS) crops in Irwin County, Georgia, over a 10 yr period.

In a woodland habitat, A. reduvii females, Anastatus males, and Ooencyrtus sp. (Hymenoptera: Encyrtidae) emerged from N. viridula sentinel egg masses. Overall, 6.6% of the eggs were parasitized.

Percentage of parasitism per egg mass was significantly influenced by habitat for E. servus (F = 28.19, df = 2, P = 0.0001) and C. hilaris (F = 11.41, df = 1, P = 0.001). Percentage of parasitism of E. servus eggs was higher in the early-season crop than in the other 2 habitats (Table 3). Percentage of parasitism was lowest for the woodland habitat. Percentage of parasitism of C. hilaris eggs was higher in woodland habitats than in late-season crops. Interestingly, in general terms, percentage of parasitism was similar for both E. servus and C. hilaris in woodlands.

In general, the first parasitoids of stink bug eggs for the season were present in an early-season crop, corn, in late May (Table 4). In this crop, egg masses of E. servus, but not C. hilaris, were detected (Tables 1 and 2). Most of the species that parasitized E. servus eggs over all habitats emerged from eggs in corn. However, T. edessae did not parasitize E. servus eggs, and male Anastatus rarely parasitized them in this crop. Parasitization of E. servus eggs continued in corn through Jul. By early Jun, parasitoids began parasitizing both E. servus and C. hilaris egg masses in woodland habitats (Table 4). Except for T. basalis and G. obesum, all parasitoid species attacking E. servus in corn were present in woodland habitats, but none of the Trissolcus species that parasitized E. servus eggs in corn emerged from C. hilaris eggs in woodlands (Tables 1 and 2). Each of the 2 Anastatus species and T. edessae also parasitized E. servus, as well as C. hilaris, in woodlands. Parasitized E. servus and C. hilaris egg masses were detected in woodlands through early Aug (Table 4). From 1 Aug through early Oct, parasitoids emerged from both E. servus and C. hilaris eggs in late-season crops. Except for Anastatus species, species present in corn and woodland habitats parasitized E. servus eggs in these crops (Tables 1 and 2). Only T. edessae parasitized C. hilaris eggs in cotton and soybean.

Table 3.

Mean (± SE) percentage of parasitism per egg mass (n) for naturally occurring egg masses of Euschistus servus and Chinavia hilaris in woodland and crop habitats in Irwin County, Georgia, over a 10 yr period.

Discussion

In southwest Georgia, E. servus and C. hilaris populations can begin developing on host plants in woodlands early in the season. For C. hilaris, diversity of egg parasitoids was greater and percentage of parasitism was higher in woodland habitats compared with those observed in crops. Of the 4 species of parasitoids of C. hilaris in woodlands, T. edessae and Anastatus species were the prevalent species. Anastatus species existed primarily in woodland habitats, and, thus, they may have a preference for woody trees and shrubs. Similarly, T. euschisti parasitized Podisus maculiventris (Say) (Hemiptera: Pentatomidae) eggs only on a woody non-crop host, hackberry (Celtis occidentalis L.; Rosales: Cannabaceae), when sentinel eggs were placed in both hackberry and alfalfa (Medicago sativa L.; Fabales: Fabaceae) (Okuda & Yeargan 1988). Parasitization of a couple of E. servus egg masses by Anastatus males in corn was likely due to their close proximity to a woodland habitat. Trissolcus edessae, though, apparently dispersed from woodland habitats into late-season crops. In contrast to C. hilaris, diversity of parasitoids of E. servus eggs was broad, 7 to 8 species per habitat, although not all parasitoid species were present in each habitat. Trissolcus edessae parasitized E. servus eggs only in woodlands and late-season crops (i.e., cotton and soybean), habitats in which C. hilaris reproduced on hosts. Again, this parasitoid species likely dispersed from woodland habitats into these late-season crops. Trissolcus brochymenae, T. euschisti, T. thyantae, T. podisi, and Ooencyrtus sp. attacking E. servus in corn and woodland habitats likely dispersed from these habitats into late-season crops, whereas T. basalis and G. obesum dispersed from corn into these late-season crops.

Table 4.

Seasonal presence of parasitized stink bug egg masses in an early-season (ES) crop, woodland habitats, and late-season (LS) crops in Irwin County, Georgia, over a 10 yr period.

Even though T. brochymenae, T. euschisti, T. edessae, T. thyantae, Ooencyrtus sp., T. basalis, and G. obesum parasitize Euschistus species, including E. servus, as in the current study, T. podisi is the predominant egg parasitoid of Euschistus species in crops or cropping systems (Yeargan 1979; Orr et al. 1986; Koppel et al. 2009; Tillman 2010, 2011b). Percentage of parasitism of eggs by T. podisi ranges from 70 to 100% for Euschistus species, 1 to 65% for C. hilaris, and 0 to 20% for N. viridula when Euschistus species coexist with one or both of the other two stink bugs species. Thus, T. podisi also tends to prefer egg masses of Euschistus species to those of C. hilaris and N. viridula. In the current study, C. hilaris eggs were not parasitized by T. podisi in woodlands or late-season crops. However, this egg parasitoid was previously recovered from this stink bug species in soybean (Yeargan 1979; Orr et al. 1986). Javahery (1990) also recovered a single T. podisi from a C. hilaris egg mass found on buckthorn (Rhamnus catharticus L.; Rosales: Rhamnaceae). This is the first report on parasitism of E. servus eggs in woodland habitats.

Based on the results of the current study and previous studies, overall percentage of parasitism of C. hilaris eggs ranged from 16 to 49% in crops (Yeargan 1979; Orr et al. 1986; Jones et al. 1996; Koppel et al. 2009). As in the current study, Jones et al. (1996) recovered only T. edessae from C. hilaris in soybean, even though these authors reported that T. basalis, T. euschisti, and T. podisi were also present in the crop. They also mentioned that T. edessae was the only parasitoid that emerged from C. hilaris egg masses collected from various host plants in a variety of habitats, but no information was provided on the species of host plants or habitats studied. The prevalent egg parasitoids of C. hilaris recovered by Orr et al. (1986) in soybean were T. edessae and T. euschisti. One C. hilaris egg mass was parasitized by Trissolcus cristatus Johnson. Koppel et al. (2009) recovered T. edessae, T. euschisti, and T. basalis from 6 C. hilaris egg masses in crops and basswood trees. Yeargan (1979) reported that T. podisi and T. euschisti emerged from 16 C. hilaris egg masses collected from soybean. Even though the current information on parasitism of C. hilaris eggs varies by study, T. edessae was recovered from eggs of this stink bug in 4 of the 5 studies. Except for the current study, parasitism of C. hilaris was studied primarily in crops. Because host plants of C. hilaris exist in woodlands, an investigation of parasitism within and between woodlands and crops is essential to our understanding of natural biological control of C. hilaris.

Trissolcus basalis tends to prefer N. viridula eggs over those of other stink bug species (Yeargan 1979; Orr et al. 1986; Jones et al. 1996; Koppel et al. 2009; Tillman 2010, 2011b). This may explain why levels of parasitism of E. servus by T. basalis were so low and only a single C. hilaris egg was parasitized by this parasitoid.

Anastatus species, including the two recovered in woodland habitats in the current study, A. reduvii and A. mirabilis, as well as Anastatus pearsalli Ashmead, have been reported as egg parasitoids of C. hilaris (Schoene & Underhill 1933; Underhill 1934; Yeargan 1979). Anastatus species have not been previously reported as egg parasitoids of E. servus, which may be due to the lack of studies on parasitism of E. servus eggs in woodland habitats. In the current study, N. viridula eggs were not detected in woodlands even though nymphs have occasionally been reported on black cherry and pokeweed (Jones & Sullivan 1982; Tillman et al. 2014). Anastatus species, though, have previously been reported to parasitize eggs of N. viridula (Jones 1988). However, Hokyo & Kiritani (1966) reported that Anastatus females could only be produced by host eggs larger than those of N. viridula. The current sentinel egg study revealed that Anastatus females can develop in sentinel eggs of N. viridula. The emergence of Anastatus females from sentinel eggs of N. viridula in a woodland habitat could be due to a preference of Anastatus for woody trees and shrubs or may be due to the association of elderberry where Anastatus species parasitize E. servus and C. hilaris eggs.

A few reports exist regarding naturally occurring parasitoids of E. servus and C. hilaris eggs on woody plant species. Euschistus sp. eggs were parasitized by T. euschisti on sassafras (Sassafras albidum [Nutt.] Nees; Laurales: Lauracea) (Yeargan 1979). Chinavia hilaris eggs were parasitized by T. basalis and T. edessae (35.2 and 20.7% parasitism of eggs, respectively) on basswood (Tilia americana L.; Malvales: Malvaceae) (Koppel et al. 2009) and by A. pearsalli on maple (Acer sp.; Sapindales: Sapindaceae) (Yeargan 1979).

Except for A. pearsalli and Telenomus utahensis Ashmead, parasitoid species that emerged from E. servus and C. hilaris egg masses in woodland habitats in southwest Georgia are reported to parasitize H. halys egg masses in crops in Delaware, Maryland, Virginia, and Pennsylvania (Rice et al. 2014). As in the current study for native species of stink bugs, species of parasitoids emerging from H. halys eggs can vary by habitat.

Certainly, conservation of the diverse species of parasitoids of stink bug eggs in woodland habitats has the potential to enhance natural biological control of stink bugs in agricultural ecosystems. The importance of nectar provision on parasitoid fitness has been demonstrated for various hymenopteran parasitoid species (Berndt & Wratten 2005; Araj et al. 2006). For T. podisi, incorporating buckwheat in soybean increased parasitism of E. servus egg masses in adjacent cotton (Tillman et al. 2015). Nectar provision along woodland field edges could provide a food source not only to parasitoids while in woodland habitats, but also as they disperse from woodlands into crops. Anastatus species were the most prevalent parasitoids emerging from naturally occurring eggs of H. halys in ornamental nurseries in Maryland (Jones et al. 2014). Providing nectar to Anastatus species near woodlands in Georgia is one of many management strategies available for managing this invasive pest in the state.

In conclusion, a diversity of parasitoid species parasitizes eggs of native stink bugs in southwest Georgia, and parasitoid species emerging from stink bugs eggs can vary by habitat. Spatial and temporal composition of host plants in various habitats also can influence species of parasitoids attacking stink bug species. Therefore, parasitism of stink bug eggs should be studied in the context of the ecosystem in which stink bug species and their parasitoids are reproducing.