Native to East Asia, Drosophila suzukii has been a major invasive pest of soft-and thin-skinned fruits since it was first detected in 2008 in North America and Europe and has been found recently in South America. Drosophila suzukii is highly polyphagous, being able to oviposit and/or reproduce in various cultivated and wild fruits. Its fast development and high reproductive potential can lead to explosive population increases and significant economic losses to crops. Though various management strategies, including behavioral, biological, chemical and cultural approaches, have been implemented to suppress D. suzukii populations and reduce crop damage, current control programs rely heavily on insecticides that target adult flies in commercial crops. Because non-crop habitats can act as a reservoir for the fly’s reinvasion into treated crops, area-wide Integrated Pest Management strategies that reduce population densities at the landscape level need to be developed for such a highly mobile and polyphagous pest. To develop area-wide programs, it is critical to understand how D. suzukii populations persist and disperse in the landscape as the season progresses. Many environmental factors, such as local climatic and landscape traits, may trigger the dispersal of D. suzukii populations to escape resource-poor habitats or unfavorable weather conditions. Landscape composition surrounding cultivated crops, such as forests and shrub vegetation, could act as sinks, sources,blueberry grow pot shelters or overwinter sites for the fly populations.
For this reason, the availability of alternative hosts could play an important role in sustaining fly populations and dictating their local movement patterns when favorable hosts are not available. Researchers have provided a better understanding of local D. suzukii population dynamics. Still, there are gaps that limit our understanding of the relative importance of different hosts for D. suzukii within some geographical regions. For example, the seasonal periods of host utilization and the importance of non-crop hosts within the agricultural landscape need to be understood to develop area-wide programs. In this framework, this study aimed to illustrate the temporal dynamics of host use by D. suzukii in California’s San Joaquin Valley, one of the world’s major fruit growing regions. Drosophila suzukii was first detected in California when it was found infesting strawberries and cranberries in Santa Cruz County in 2008. Since then, damaging populations have been recorded from cherries, cranberries, mulberries, raspberries and strawberries, mainly in the coastal or northern California fruit growing regions with relatively mild summer. In comparison, California’s interior San Joaquin Valley has hotter summers and colder winters, and while D. suzukii is collected in cherry, citrus, fig, grape, kiwi, mulberry, nectarine, peach, persimmon, plum and pomegranate as well as in non-crop habitats surrounding the orchards, reported crop damage has been mainly on cherries. Adult fly captures show two main periods of activity—spring and fall—and low captures in winter and summer.
The number of captured flies was positively related between pairs of sampled sites based on their proximity, but it was negatively related to differences in fruit ripening periods among crops, suggesting that fly populations might move among crop and/or non-crop habitats during the year. Though adult flies are captured in various orchard crops, it is not clear whether these fruits are vulnerable and serve as hosts. For example, the potential impact of D. suzukii on wine grapes in Italy was discussed by Ioriatti et al., who observed D. suzukii oviposition in soft-skinned berries, and, in Japan, some grape cultivars were reported as hosts for D. suzukii. In Oregon, Lee et al. found that D. suzukii was able to successfully oviposit in some wine grape cultivars but that offspring survival was low , whereas other studies observed no or low levels of infestation of intact grapes in the field or laboratory. Some of the initial work in Japan reported that D. suzukii emerged only from fallen and damaged apple, apricot, loquat, peach, pear, persimmon and plum, but Sasaki and Sato reported that healthy peach fruit can be infested. However, in California, Stewart et al. reported that intact peach fruit are unlikely hosts. No doubt, many fruits with hard or hairy skin can be colonized if wounds are available to allow flies to oviposit in the pulp. In this study, we document the temporal patterns of host use by D. suzukii in California’s San Joaquin valley by sampling intact and damaged fruits of various crop and no-crop plants throughout the fruiting season. We evaluated the suitability of key fruits, including several unreported ornamental and wild host fruits as hosts for the fly, particularly focusing on the host status of grapes—considered to be a non-preferred host—and cherry—considered to be a preferred host. Wine grapes can contain uniquely high levels of organic acids that are important for producing wines less susceptible to microbial and oxidative damage and with more vibrant color.
The levels of acidity decrease as fruit are ripening, but they remain high throughout the ripening process. For this reason, we also examined the impact of tartaric acid concentrations on the fly’s fitness. For cherries, we examined the effects of cultivar and fruit size on the fly’s performance. We additionally monitored adult fly populations at different elevations—from the Valley floor east to the foothills and Sierra mountains—to determine if the fly is active at higher elevations during the hot summer when the fly populations were extremely low in the Valley’s agricultural areas. We discuss the implications of this information for area-wide management in the San Joaquin Valley. A total of 17 common fruits were sampled in a temporal sequence of fruit ripening, including twelve important crops , three ornamentals , and two wild host plants . Samples were taken from 2013 to 2015 at the University of California’s Kearney Agricultural Research and Extension Center, near Parlier, California and near Brentwood, California . Bitter cherry, Prunus emarginata Eaton , and the Cascara buckthorn, Frangula purshiana are endemic to western North America; these fruits were collected at higher elevations 1683 m near Shaver Lake, California . For all species, both intact fruit and damaged fruit were collected as available, as the fruit were at a susceptible ripening stage for D. suzukii oviposition. A total of 30–50 fruit were collected when at a susceptible ripening stage for each species, although the number of intact ornamental and wild fruits varied depending on the availability.Collected fruits were placed individually or in groups of 10–50 in deli cups and held under controlled conditions at the University of California’s Kearney Agricultural Research and Extension Center . Deli cups were covered with fine organdy cloth and fitted with a raised metal grid on the bottom to suppress mold growth. A piece of tissue paper was placed underneath the fruit to absorb any liquid accumulation. Emerged flies were collected every 2–3 d, frozen, and then identified as either D. suzukii or other drosophilids. Only those flies that emerged within 2 weeks following field collection were counted to exclude the possibility of second-generation flies.All laboratory studies were conducted under controlled conditions, as described above . A laboratory colony of D. suzukii was established from field collections of infested cherries at Kearney. The fly larvae were maintained on a standard cornmeal-based artificial diet using methods described by Dalton et al., and adult flies were held in Bug Dorm2 cages supplied with a 10% honey–water solution and petri dishes containing standard cornmeal medium sprinkled with brewer’s yeast for feeding and oviposition. Field-collected D. suzukii were introduced into the colony yearly to maintain the vigor of the colony. All tests used 1–2-week-old adult female flies that had been housed with males since emergence .To determine if D. suzukii can oviposit within and develop from damaged or rotting navel oranges , a single adult female D. suzukii was exposed to a whole fresh fruit, halved fresh fruit, rotting whole fruit,hydroponic bucket or halved rotting fruit for 24 h in the acrylic cage. To simulate the natural decay process of a fallen orange, fresh oranges were placed individually on wet sandy soil in deli cups until the fruit started to rot. The halved fruit were allowed the same amount of time as the whole fruit but were cut into halves just prior to the test. On average, rotted fruit had 42.3 ± 7.3% of their surface covered by mold growth. Following exposure, the numbers of eggs laid were counted, and the fruit was then held in the cage until the emergence of adult flies. Each treatment started with 25 replicates; however, a few replicates were discarded because of contamination by other drosophilids that likely occurred during the regular examination for the decay status of the fruit. A sub-sample of 10 fruit was measured to determine the Brix levels of fresh and rotting fruits.
To determine the possible effect of tartaric acid on D. suzukii survival and development, seven different concentrations of tartaric acid were mixed with a standard artificial diet. The powdered tartaric acid was purchased from a wine and beer brewing store in Fresno, CA, USA, and mixed with the diet just before the diet solidified. The content of tartaric acid in grapes can vary depending on cultivar, ripeness, and environmental conditions; for example, Kliewer et al. reported a tartaric acid content ranging from 3.7 to 13.2 g/L in different cultivars and from 3.4 to 9.2 g/L in early- vs. late-harvested cultivars. The doses used here covered these reported ranges. Each treatment had 20–22 replicates, and each replicate started with 10 D. suzukii eggs from the laboratory culture that were placed in drosophila vials over the diet. The number of developed adults was recorded. A sub-sample of 25 pupae from each treatment was measured for pupal length and width , and the volume of each pupa was estimated based on the formula 2. Apple cider vinegar traps were used to monitor fly populations at four different elevations from the Valley’s low agricultural areas to the Sierra Nevada: Kearney , lower foothills , higher foothills and Sierra mountains . Traps at Kearney were placed in a mixed stone fruit orchard; traps at the three higher elevations were along Highway 168, with the foothill sites in residential yards with fruit trees and the Sierra site at the forest’s edge in bitter cherry bushes. Three traps were placed at each location, approximately 200 m apart. Collection methods were similar to Wang et al.. Briefly, traps were constructed of plastic containers filled with apple cider vinegar and a small amount of Bon-Ami Free and Clear® unscented soap to serve as a surfactant. Traps were hung on tree branches at head-height and then checked and replaced weekly from June to November 2017. Captured arthropods were placed into 95% ethanol in small glass bottle and later examined under a dissecting microscope to count the number of D. suzukii.For host suitability tests, since fruit varied in weight, the percentage of D. suzukii eggs that successfully developed to adults was calculated based on eggs per gram fruit to standardize the comparison among different treatments. The egg density effect on the percentage of eggs developed to adults in cherry was analyzed using linear regression. The percentage of eggs that successfully developed to adults on different fruit species or different cherry cultivars were subject to further analysis of generalized linear model with binomial distribution and log-link function by considering the effect of both fruit species or cultivar and egg density per gram fruit, as well as the interactions of these two factors. To separate the means among different treatments, the percentage data were also arcsine transformed as needed to normalize the variance and analyzed using ANOVA. All analyses were performed using JMP V13 . A separate analysis with 10 different cherry cultivars did not yield a significant effect of the Brix on the percentage of eggs that successfully developed to adults, although we could not rule out the possibility that Brix and other chemical properties may affect other fitness parameters of the developed flies. Many of the differences in chemical traits among different fruits could be attributed to geographic location and differences in environmental and cultivation conditions rather than inherent varietal properties, such as in cherries. In the current study, chemical differences were controlled to some extent, as cherry cultivars used were grown in the same plot with the same fertilization and irrigation regimes. The physical properties of different cultivars did not seem to affect the fly’s oviposition.