Discussion
By examining the behavior of an agricultural pest in a remote, non-crop
setting, we can gain a better understanding of the ecological,
behavioral, and physiological plasticity of the insect. First, the high
infestation rates (eggs/g fruit) observed in the forested locations
suggest these areas are highly suitable to D. suzukiiestablishment. Distribution models for agricultural pests are trained on
occurrence data at a regional or global scale, however oftentimes, the
available data are collected in a non-random manner. For instance,D. suzukii sampling in the United States has mostly occurred in
and around susceptible cropping areas. As demonstrated with these data,
a common criticism of presence-only models is that they do not
adequately extrapolate to novel areas (Elith and Leathwick 2009, Roach
et al. 2017). Models trained on D. suzukii occurrence data from
North and South America performed worse in this ground truthing exercise
than the model trained on a global data set, suggesting improvements
could result from more diverse sampling schemes.
Second, wild blackberries were as or more susceptible to D.
suzukii oviposition at all ripeness stages than the cultivated
blackberries in this study. In an evolutionary sense, cultivated crops
are thought to be more exploitable by insect pests than wild relatives
due to human-mediated plant domestication selecting against plant
defensive traits (Chen et al. 2015, Whitehead et al. 2017). For
instance, bitter-tasting secondary metabolites that deter insect feeding
are greatly reduced in domesticated plant species (Wink 1988). Generally
speaking, domesticated fruits are also much larger than their wild
ancestors, and frugivores tend to prefer larger fruits, lending support
to this plant domestication-reduced defense hypothesis. Indeed, femaleD. suzukii laid more eggs into cultivated blueberries than wild
ones (Rodriguez-Saona et al. 2019). While we also saw the greatest eggs
per berry in cultivated ripe and purple fruit, there were significantly
more eggs in wild berries after mass was taken into account. Although we
do not know how larval competition affects survivability to adulthood in
these natural areas, laboratory studies have shown high D.
suzukii egg and larval densities can lower mean survivorship, however
host quality mediates this effect (Hardin et al. 2015).
A number of factors contribute to oviposition site selection in
herbivores, including previous experience, host condition, competition,
and predator avoidance (Jaenike 1978, Futuyma and Peterson 1985, Papaj
and Prokopy 1989, Carrasco et al. 2015). The higher oviposition we
observed in under-ripe wild berries may be, in part, related to shorter
ripening times. Wild blackberries are about a quarter the size of the
cultivated ‘Ouachita’ variety sampled here, and exhibited a swifter
progression from the blush to ripe stage during collection. ThatD. suzukii can and do develop on a wide variety of host plants
and even non-host plants suggests that larval nutritional needs are
plastic (Jaramillo et al. 2015, Young et al. 2018, Little et al. 2020).Drosophila suzukii avoid laying eggs in overripe fruit,
presumably to avoid interspecific competition, so it is reasonable to
expect a large spillover effect into under-ripe berries if a significant
determining factor for fitness is competition. The tradeoff to laying
eggs into less-ripe fruit may be small if the appropriate nutrients are
gathered as the berry ripens during the same length of time as larvae
develop. This strategy might not translate to oviposition in cultivated
blackberries because the fruit stay in each ripeness stage for a longer
period (see Swoboda-Bhattarai and Burrack 2017). In a sense, thatD. suzukii oviposit more readily into wild fruit suggests that
non-domesticated blackberries are more exploitable than their cultivated
counterpart.
Another consequence of fruit domestication is a change in fruit ripening
windows. Cultivated crops are selected to produce fruit where the
majority will ripen around the same time to reduce harvesting labor
cost, leaving less diversity among ripeness stages for female
oviposition selection (Heiser 1988). In cultivated berries, the number
of eggs per berry at each ripeness stage over the season were
consistently different from each other, suggesting that oviposition was
additive at each stage; the number of eggs per berry increased as a
function of time and ripeness. Contrastingly, there was no such pattern
in the wild berry samples, which is more indicative of a simultaneous
rather than sequential infestation.
Finally, we wanted to assess whether any of the observed difference in
oviposition among the cultivation types resulted from host preference.
In a direct preference comparison, females preferred laying eggs in
cultivated fruit when exposed to a single berry of each type, which may
indicate a size or surface area preference given the physical disparity
between the two fruit types. However, when offered an equal weight,
corresponding to a single cultivated versus several wild berries,
females laid more eggs in wild fruit. Long-range perception in
oviposition site selection relies heavily on visual cues; at a distance,
clusters of berries may appear as a single, large fruit, which could
explain why our lab preference results differed when the set-up changed.
The observed correlation between apparent fruit size and preference
agrees with other visual research on D. suzukii attraction and
its effects on oviposition behavior (Rice et al. 2016). Additional
experiments that eliminate visual cues will be needed to further assess
any preference among cultivated and wild blackberry fruits.
The pattern and timing of infestation we observed in wild-growing
berries from natural habitats in the eastern United States is consistent
with research in Hawaii, Europe and Japan that trapped adult D.
suzukii in montane habitats (Ometto et al. 2013, Mueller 2015,
Santioemma et al. 2019). In Japan, while most fruit crops were grown
below 600m, the majority of D. suzukii adults were trapped at
higher elevations (Ometto et al. 2013). The present study supports this
idea, finding a variety of susceptible host plants and high levels of
infestation in the most abundant resource, wild blackberry. We observed
that once fruit began to ripen, sometime between the green and blush
stage, the berries were exploited for oviposition by D. suzukiifemales.
Given this information about the presence of established populations ofD. suzukii in remote, montane regions of the southern Appalachian
Mountains, several new research questions arise. Within the wooded
landscape, D. suzukii may be affecting the local food web by
utilizing wild blackberries upstream of other organisms. What effect
does this invasive pest have on other blackberry feeders such as birds,
bears, or other invertebrates? In terms of agroecosystem impact, do
these types of forest populations serve as a potential source for
regional migration into crop habitats? No seasonal migration pattern has
been established for D. suzukii , though marked adults have been
caught at distances in excess of four times their flight capacity (Tait
et al. 2018, Wong et al. 2018). The full extent of current and future
impacts of D. suzukii in croplands and beyond has yet to be fully
realized.