Introduction
The niche breadth of polyphagous insect pests can be expansive due to a number of biological and abiotic factors including the ability to exploit diverse host types in heterogenous environments and the capacity to respond to changing conditions over time (Kennedy & Storer 2000, Sakai et al. 2001, Little et al. 2020). Species with broad host ranges also tend to have an outsized impact on crops as compared to monophagous or oligophagous insect species (Ward and Spalding 1993). It is reasonable to assume these substantial impacts may also occur in non-crop areas. Considerable research has been conducted in semi-natural lands adjacent to or near affected crops, as these are the areas thought to be highly influential to agroecosystem dynamics (Kennedy and Storer 2000, Rand et al. 2006, Mazzi and Dorn 2012).
For polyphagous pests, non-crop host plants occur throughout the landscape, including places far removed from agriculture. These areas, such as forests, are rarely assessed for the presence of agricultural insect pests unless they are also considered a forest pest, such as pear thrips, Taeniothrips inconsequens (Uzel) (Teulon et al. 1998), or the spotted lanternfly, Lycorma deliculata White (Barringer and Ciafré 2020). Nevertheless, studying non-forest crop pests in remote areas might be important for a number of reasons. First, these insects may impact forest food web dynamics through resource use competition of common host plants. Second, if these remote locations host established populations of agricultural pests, then they may be a source for seasonal migrants into cultivated areas. Third, understanding pest behavior outside of the agroecosystem may yield novel insights into pest behavior and ecology that may not be evident in highly human-influenced agricultural areas. Finally, such insights can then be used to improve modeling predictions for current and future range expansions.
Distribution modeling is a common way to model invasive species and is based on known life history traits and occurrence. However, ground truthing to inform or verify model-based inferences (e.g., likelihood of occurrence or density) often fails to venture outside of areas where the pest is causing direct economic damage, namely cropland in this case. Failure to fully verify these distribution models limits their usefulness and insight (Wright et al. 2006, Fitzpatrick et al. 2007, Sarquis et al. 2018). Furthermore, niche divergence may occur more readily in areas with more diverse habitat and can be indicative of ecological changes such as invasive species establishment, food web disruption, or climate change (Wright et al. 2006).
Drosophila suzukii (Matsumura) is a highly cosmopolitan agricultural pest of berry crops. Native to East Asia, D. suzukiiwas limited in spread until 2008 when accidental introductions led to a range expansion into Europe and continental North America, and in subsequent years to South America, Western Asia and most recently in Africa (Hauser et al. 2011, Calabria et al. 2012, Deprá et al. 2014, Parchami-Araghi et al. 2015, Hassani et al. 2020). Ripe fruit from cultivated berry crops and wild-growing native and non-native plant species serve as oviposition sites for female D. suzukii and nutritional resources for all life stages. The presence and movement of this fly has been well-studied in croplands and nearby disturbed or wooded areas that serve as potential refuge sites and often contain susceptible hosts (Bellamy et al. 2013, Lee et al. 2015, Klick et al. 2016, Elsensohn and Loeb 2018, Santoiemma et al. 2018). Some host plant species are regionally common and can be found well outside agroecosystems, including in backyards, roadsides, woods, and fields, among other places (e.g., Mitsui et al. 2010, Poyet et al. 2014, Ballman and Drummond 2017).
Several ecological models were created to assess the current and future distribution of D. suzukii around the world (Gutierrez et al. 2016, dos Santos et al. 2017, Fraimout and Monnet 2018, de la Vega and Corley 2019, Ørsted and Ørsted 2019). One species distribution model using global occurrence data indicated a higher likelihood of occurrence in the southern Appalachian Mountains of the eastern United States than in surrounding areas (Ørsted and Ørsted 2019). Contrastingly, a physiologically-based demographic model estimated a lower D. suzukii density in the same area (Gutierrez et al. 2016). Much of this region of the Appalachian Mountains, which ranges in elevation from 900-1850 m, is designated as federally protected National Forest land. No commercial plantings of cultivated D. suzukii hosts are known to occur within this area, although D. suzukii -susceptibleVaccinium and Rubus spp. native to North America grow well here (Powell and Searman 1990).
To date, no studies have sought to ground truth model-predicted occurrence sites sparsely populated by humans as potential population sources of D. suzukii . In Europe, altitudinal studies demonstrated an established presence of D. suzukii in high elevation, mountainous locations (Tait et al. 2018, Santoiemma et al. 2019), and documented recapturing marked adults over 9 km from the release site (Tait et al. 2018). This distance is suggestive of weather-assisted movement, as flight mill tests show the flight capacity of adults is less than 2 km (Wong et al. 2018). Insect dispersal through wind patterns is documented in several pest species (Hoelscher 1967, Compton 2002, Moser et al. 2009) and has been postulated as a potential means of yearly recolonization by D. suzukii at northern U.S. latitudes after winter temperatures kill the vast majority of overwintering flies (Rossi-Stacconi et al. 2016, Panel et al. 2018, Wallingford et al. 2018). Localized D. suzukii movement from shrubby or wooded landscapes into crop fields is well documented (Klick et al. 2016, Pelton et al. 2016, Tonina et al. 2018). Uncultivated and cultivated areas can be exploited concurrently or consecutively throughout the year, especially in areas where adults are caught year-round (Ballman and Drummond 2017, Elsensohn and Loeb 2018, Santoiemma et al. 2018). Uncultivated areas can enlarge or sustain pest populations that could spill back into crop areas through short or long-distance movement, and vice versa.
Some non-crop hosts may be preferred oviposition sites for femaleD. suzukii or offer better nutritional resources needed for larval development. Comparative work exploring oviposition preference between crop and non-crop host species found that preference depended on the specific fruit combinations used (Lee et al. 2015, Diepenbrock et al. 2016). The first direct comparison of D. suzukii oviposition preference between wild and cultivated fruit of the same crop type found that females laid more eggs into cultivated than wild blueberries (Rodriguez-Saona et al. 2019). However, these results may be confounded by differences in fruit size, weight, and surface area between domesticated and wild relatives.
Laboratory research into oviposition preference as a factor of fruit ripeness stage revealed that the ripe stage was the most preferred for oviposition while progressively under-ripe stages received fewer or no eggs (Lee et al. 2011, Kamiyama and Guédot 2019). In a field setting, fewer adults emerged from blackberry fruit infested during under-ripe stages than fruit infested later at the ripe stage (Swoboda-Bhattarai and Burrack 2017). These results align with laboratory studies that show a survival hierarchy with ripe fruit producing the lowest mortality rate (Lee et al. 2011, Bernardi et al. 2017, Kamiyama and Guédot 2019).
To better understand D. suzukii oviposition preference and general resource use in areas unaffected by spillover dynamics, we conducted an elevational gradient study in the southern Appalachian Mountain region. Here, modeling predictions are uncertain, but non-crop hosts are common. Over two years, we visited three natural areas and one roadside tract surrounded by National Forest lands in western North Carolina to collect wild-growing fruit at different stages of ripeness. The main objectives of this study were to: 1) document the presence or absence of D. suzukii in the unpopulated areas; 2) compare seasonal host use patterns of wild and cultivated blackberry fruits; and 3) assess host preference between wild and crop fruit in a laboratory setting.