Native insect predators and parasitoids can help regulate invasive insect pest species. The brown marmorated stink bug, Halymorpha halys (Hemiptera: Pentatomidae), is an introduced pest of fruits and vegetables in the eastern USA that originated in Asia. Surveys for native biological control agents of this pest detected the crabronid predatory wasp Astata unicolor (Hymenoptera: Crabronidae) and the generalist predatory bug Arilus cristatus (Hemiptera: Reduviidae) using the nymphs and adults of this introduced pest as prey. Temporal distribution of the wasp was determined from water pan traps and net collections over 5 years in floral provisioning strips that were established for pollinator conservation programs in tree fruit farms. Blue vane traps used for bee monitoring did not capture A. unicolor in pollinator plantings. Astata unicolor was not found in 6 commercial apple orchards that were monitored concurrently using either pan or blue vane traps over a 4 yr period.
Exotic species of arthropods, including pests, can provide new food resources for native predators, and may replace their food choice of native prey with new (exotic) species (Carlsson et al. 2009). Several examples of vertebrate predators switching to invasive prey include the previously threatened Lake Erie water snake, Nerodia sipedon insularum (Conant & Clay, 1937) (Squamata: Colubridae), whose preferred prey is now the exotic Eurasian round goby, Neogobius melanostomus (Pallas, 1814) (Perciformes: Gobiidae) (King et al. 2006), and the zebra mussel, Dreissena polymorpha (Pallas, 1771) (Veneroida: Dreissenidae), both of which invaded the Great Lakes and became important in the diet of turtles (Bulte & Bloudin-Demers 2008) and other predators such as birds (Petrie & Knapton 1999) in this region. Using superabundant invasive prey such as these would give predators of all types, including insects, a competitive advantage over other native predators that cannot physiologically and behaviorally adapt to new (invasive) food sources (Carlsson et al. 2009). Carlsson et al. (2009) argues that native predators can be an important regulatory factor not only of native species, but over time could be important in regulating non-native species as well. The examples used by Carlsson et al. (2009) mostly are of vertebrates, but numerous examples of exotic insect pests being regulated by native arthropod species exist. Examples of this are the European red mite control by the native coccinellid mite predator, Stethorus punctum LeConte (Coleoptera: Coccinellidae) (Biddinger et al. 2009), or numerous native parasitic wasp species which not only help regulate native tortricid pests in apple orchards, but also codling moth and Oriental fruit moth that were introduced from Asia (Biddinger et al. 1994; Allen 1962). Here we describe how a native predatory wasp (Astata unicolor Say [Hymenoptera: Crabronidae]), which specializes on stink bug as prey, has adapted to using the nymphs of the invasive Asian species of stink bug known as the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae).
First reported in 1996 (Hoebeke & Carter 2003), brown marmorated stink bug is a serious pest of fruits and vegetables in the mid-Atlantic states of the USA During the 2010 season, apple growers of this region lost an estimated $37 million due to fruit injury by brown marmorated stink bug (Seetin 2011). Brown marmorated stink bug is a highly mobile polyphagous pest that can fly long distances (Bakken et al. 2015). Different stages of brown marmorated stink bug are attacked by several species of native arthropod natural enemies (Abram et al. 2017; Dieckhoff et al. 2017). As an agricultural pest, it is a good candidate for biological regulation by predators and parasitoids, because it spends the majority of the year in non-managed, wooded habitats rather than in agricultural crops where pesticides often limit biological control.
As part of a multiyear survey conducted using different traps and hand netting for native biological control agents for brown marmorated stink bug, we observed the native wasp Bicyrtes quadrifasciata (Say) Hymenoptera: Crabronidae), which is a stink bug specialist predator, gathering brown marmorated stink bug nymphs, which was a preferred prey when nest provisions were examined (Biddinger et al. 2017). Bicyrtes quadrifasciata is from a group known as sand wasps (Bohart 1996), and often is found nesting communally in large numbers in sandy areas such as sand boxes and baseball fields (Evans & O'Neill 2007). During this survey, another closely related species of Crabronidae, A. unicolor (Say), also was observed carrying brown marmorated stink bug nymphs as prey and was photographed by Pennsylvania nature photographer Yurika Alexander (Fig. 1).
Astata unicolor adults are extremely fast fliers and hard to follow visually, but species of Astata seems to prefer nesting in heavier soils along the edges of woods and gardens (Evans 1957). Females of both genera provision tunnels with paralyzed prey in underground nests up to 20 cm deep, with Astata being more specialized in using only stink bug nymphs, whereas Bicyrtes also may use other hemipterans such as Coreidae, Alydididae, and Rophalidae, in addition to Pentatomidae. Nest provisioning strategies also differ between the 2 genera, with Bicyrtes digging 5 to 6 tunnel nests during her lifetime, with each tunnel having 1 to 3 cells, and each cell containing from 4 to 14 prey nymphs. In contrast, the smaller Astata females appear to dig only a single nest that may have from 12 to 14 provisioning cells, but with only 2 to 3 prey nymphs per cell and only a single egg laid in each cell (Evans 1957; Evans 1962; Parker 1962; Evans & O'Neil 2007).
While monitoring bees and other pollinators weekly with different types of visual pan and vane traps from 1 Apr to the end of Oct as described in Joshi et al. (2015), A. unicolor adults were not captured in 6 commercial apple and 4 commercial cherry orchards from 2010–2015. In concurrent monitoring of nearby floral provisioning strips consisting of many species of perennial native wild flowers to enhance pollinator populations, as described in Shugrue (2016), a total of 48 adults of A. unicolor were captured either by pan trap, vane trap, or by net collection during floral visits. Seasonal capture of A. unicolor in 2011 and 2012 suggests only a single generation that begins at the end of Jun, peaks in mid-Aug and ends by the beginning of Oct (Fig. 2). Of these adults, only 1 was a female, and the majority were trapped in colored pan traps. Finding almost exclusively male A. unicolor adults captured in traps and by net is probably due to the hill-topping behavior of the males (Alcock 2007). The majority of specimens were collected through pan traps (81%) followed by net collection (13%) and captures in vane traps (6%). Among water pan traps, most specimens were found in dark blue-colored pan traps (56%), followed by white (36%) and yellow (8%) pan traps. Specimens that were net-collected directly from flowers were found foraging on wild burgemont (Monarda fistulosa L. [Lamiales: Lamiaceae]), wild carrot (Daucus carota L. [Apiales: Apiaceae]), and swamp milkweed (Asclepias incarnata L. [Gentianales: Apocynaceae]).
During this survey, we also observed feeding on brown marmorated stink bug adults and nymphs in the field by the common reduviid predator known as the wheel bug, Arilus cristatus (L.) (Hemiptera: Reduviidae) and several species of large spiders. Predation by large generalist predators such as these, however, is not unexpected.
Considering the economic importance and polyphagous nature of brown marmorated stink bug, it is important to further explore the role of these native predators in regulating the long-term population dynamics of population in the Mid-Atlantic region and elsewhere in future studies. Additionally, it is also important to investigate if this host shift of native crabronid stink bug predators is due to a preference for brown marmorated stink bug or by just default, due to the greater abundance of brown marmorated stink bug, which may have displaced native prey.
The authors are grateful to the USDA-NIFA SCRI project 2011-01413-30937, Northeast IPM Center IPM Partnership Grant and the State Horticultural Society of Pennsylvania for the financial support of this project, and Yurika Alexander for allowing the use of Astata unicolor photograph.