In recent years, fruit flies (Drosophila spp.: Drosophilidae) have become an increasingly serious problem for cherry production in northern China. In this study, we examined the species composition and dynamics of fruit flies in cherry orchards using lure-baited traps placed at different heights, and in 3 different cherry cultivars, from Apr through Sep 2014 to 2016 in Qingdao, Shandong Province, China. The total number of fruit flies increased from yr to yr. Four species were captured: Drosophila melanogaster Meigen, Drosophila suzukii Matsumura, Drosophila hydei Sturtevant, and Drosophila immigrans Sturtevant (all Diptera: Drosophilidae). The dominant species was D. melanogaster, with 66.7% of the total captured, followed by D. suzukii (29.7%). Drosophila hydei and D. immigrans accounted for only 3.0 and 0.6%, respectively, and for these last 2 species, no peak period in abundance was observed. In general, Drosophila spp. appeared in Apr, and peaked around mid-Jul. Over the 3 yr span of the study, peak fruit fly abundance occurred later each yr, being at the end of Jun in 2014, and in the middle of Jul in 2015 and 2016. There were significant differences in the number of Drosophila species among cherry cultivars, as well as in the number of Drosophila trapped at different heights. The cultivar maturing in the middle of the season (cv. ‘Van') attracted the most fruit flies. The optimal height for trap placement was at 1 m above ground level, which is recommended as a standard height for Drosophila spp. population monitoring.
Cherry, Prunus avium L. (Rosaceae), is one of the most valuable orchard crops in northern China. Because of their high nutritional value, low levels of pesticide residues, and popularity with consumers, cherries are being produced on a rapidly expanding land area (Zhou 2016).
However, in recent years, pest and disease pressure on cherry have grown, and Drosophila have become an increasingly serious problem. Drosophila suzukii Matsumura (Diptera: Drosophilidae) fruit flies were first recorded on cherry in 1916 in Yamanashi, Japan (Yu et al. 2013), and in China in the early 1930s (Kanzawa 1936). Subsequently, D. suzukii was recorded in North Korea, South Korea (Chung 1955; Kang 1968), India (Parshad & Duggal 1965), Russia (Sidorenko 1992), Pakistan (Amin et al. 2005), Bangladesh (Pansa et al. 2011), Myanmar (Toda 1991), and Thailand (Okada 1976). By the 1980s, D. suzukii was observed throughout Hawaii, and first appeared in North America in California in 2008 (EPPO 2010). Drosophila suzukii quickly moved east in the US, being observed in Florida in 2009 (Steck et al. 2009) and the Carolinas in 2010 (Burrack 2010). Since then, they have invaded much of North and South America, Europe, and many other regions, causing serious economic damage (Cini et al. 2012).
Adults of Drosophila melanogaster Meigen (Diptera: Drosophilidae) were discovered first in China in 1997 in the city of Tianshui, Gansu Province (Guo 2007). Presently, the species can be found in Heilongjiang, Shandong, Zhejiang, Guangxi, and the Guizhou provinces of China, in Tibet and Taiwan, and 22 other provinces and autonomous regions (Qian & Zhang 2006), reportedly causing increasing damage (Wang et al. 2008, 2013; Hui et al. 2010; Yang et al. 2011; Lu et al. 2015;). Drosophila melanogaster usually is not considered to be a primary fruit pest in many regions of the world. However, in China it is abundant in cherry orchards, and even if it attacks only overly ripe or damaged fruit, its presence is a concern to producers because it can be confused with D. suzukii. In Aba in Sichuan Province, the damage attributed to D. melanogaster has reached 60% (Guo et al. 2007). Similarly, in Guizhou Province, the damage to Myrica rubra (Lour.) Siebold and Zucc. (Myricaceae) attributed to D. melanogaster has risen from 38% to 57% (Li et al. 2011). In Gansu Province, D. melanogaster reportedly damaged 35% of cherry fruits, with some cultivars suffering as much as 80% damage. Without timely prevention and control, D. melanogaster fruit fly damage to cherry crops in this region can exceed 60% (Guo 2007).
From 2014 to 2016, we monitored fruit fly populations in the cherry growing region of Qingdao in Shandong Province to determine the species present, the effect cherry variety had on Drosophila abundance, and also the effect trap height had on trapping.
Materials and Methods
STUDY SITE
This study took place at the Beizhai Experimental Orchard of Qingdao Academy of Agricultural Science in Laoshan District, Qingdao, Shandong Province, in a 2 ha orchard of cherry trees. When the survey started in 2014, the mean height of the trees was 2.1 m, reaching 2.4 m at the end of 2016. The cherry trees were surrounded by peach and apple trees. Due to the diversity of cherry varieties, the harvest period lasts from mid-May to mid- to late Jun, and there was a small amount of fruit falling onto the soil. Chemical treatments were restricted to 3 fungicide sprays per yr and no insecticides were used.
TRAPPING METHOD
Traps consisted of 600 mL plastic bottles. To allow flies to enter the bottle traps, we cut 8 holes (0.6 cm diam) in the upper half of the bottle in various places.
The attractant and killing solution consisted of 50 g of brown sugar, 80 mL of anhydrous ethanol, 50 mL of rice vinegar, 370 mL of water, and 2 g of 90% dichlorvos. One hundred fifty mL of the solution was added to each bottle, along with 10 g of ripe banana.
EFFECT OF CHERRY CULTIVAR ON DROSOPHILA SPECIES, CATCH RATE, AND FLY PHENOLOGY
Three cultivars of cherry were sampled: the early ripening cv. ‘Hongdeng,' mid-season ripening cv. ‘Van,' and the late ripening cv. ‘Summit.’ For each cultivar 5 trees were selected and a trap was suspended 1.2 m above the ground from each tree. Traps were replaced every 3 d and brought back to the laboratory to identify and count the fruit flies.
EFFECT OF TRAP HEIGHT ON CATCH
This experiment was conducted in the same orchard as the cultivar study. We used a 5 point sampling method (Pelz-Stelinski et al. 2006) in the study orchard, and at each point, the nearest same-cultivar cherry tree was selected to hang 1 trap at each of the 4 different test heights (at ground level, 1 m, 1.5 m, or 2 m above the soil). Traps were replaced every 3 d with new bottles containing fresh liquid bait. Old traps were brought back to the laboratory where fruit flies were removed, identified to species, and counted.
DATA ANALYSIS
Fly abundance was expressed as number of individuals per trap per 3 d. Data normality was checked using the 1-sample Kolmogorov-Smirnov test. In case of non-normality, we used a log transformation. In cases where normalization was unsuccessful, we used a non-parametric ANOVA to test for differences. Means were separated using LSD. Data were processed with Excel 2007, and ANOVA using the SPSS 20.0 statistics program (SPSS Inc., Chicago, Illinois, USA).
Results
FRUIT FLY ABUNDANCE
Four fruit fly species were collected in cherry orchards each yr from 2014 to 2016: Drosophila melanogaster Meigen, D. suzukii Matsumura, Drosophila hydei Sturtevant (Diptera: Drosophilidae), and Drosophila immigrans Sturtevant (Diptera: Drosophilidae). These 4 species accounted for 66.7, 29.7, 3.0, and 0.6% of the total, respectively (Fig. 1). Whereas D. melanogaster and D. suzukii peaked on 9 Jul and 12 Jul, respectively, the other 2 species were found only at low levels and did not have a distinct seasonal peak.
Considering the overall seasonal activity, the number of fruit flies in 2014 peaked around 24 Jun, significantly earlier than in 2015 (12 Jul) and 2016 (15 Jul), which is closely related to the phenology of fruit maturation (Fig. 2).
EFFECT OF CHERRY CULTIVARS ON FRUIT FLY CAPTURES
Peak trap captures of D. melanogaster differed significantly among cultivars (Hongdeng, Van, and Summit) on 12 Jul (F = 35.67; df = 2; P < 0.001) (Fig. 3). Peak trap captures of D. suzukii (on 3 Jul, 9 Jul, 9 Jul for cv. Hongdeng, Van, and Summit, respectively) differed significantly among cultivars (F = 49.35; df = 2; P < 0 .001) (Fig. 4).
In the cv. Hongdeng, all 4 Drosophila spp. were captured, but D. melanogaster was the dominant species, with peaks in mid-Jul and with an average peak among years of 30.4 ± 3.7 (± SD) individuals per trap per 3 d. The second most common species, D. suzukii, showed seasonal peaks of abundance in mid-Jun and early Jul, with an average peak abundance among yr of 25.6 ± 1.4 individuals per trap per 3 d.
In cv. Van, all 4 Drosophila flies were trapped, and D. melanogaster was the dominant species. Peak catches of D. melanogaster occurred in mid-Jul, with an average peak among yr of 78.6 ± 8.2 individuals per trap per 3 d. Drosophila suzukii showed peaks in mid-Jun and early Jul, with an average peak abundance among yr of 56.2 ± 7.3 individuals per trap per 3 d. The peak of D. suzukii on cv. Van was earlier than on cv. Hongdeng.
In cv. Summit, all 4 Drosophila flies were trapped, with D. melanogaster, the dominant species, peaking in mid-July at 62.6 ± 5.8 individuals per trap per 3 d; D. suzukii had peaks in trap capture in mid-Jun and early Jul (48.3 ± 2.9 individuals per trap per 3 d). The peak of fruit fly activity coincided with the flies in cv. Van. (Fig. 5).
EFFECT OF TRAP HEIGHT ON DROSOPHILA FRUIT FLY CAPTURES
Most fruit flies were captured by traps placed at 1 m above the soil (16.4 ± 0.9 individuals per trap per 3 d), significantly more (F = 139.56; df = 3; P < 0.001) than at other heights (Fig. 6). There was little fruit fly activity at ground level. During the entire investigation period, the mean relative proportions of fruit flies trapped at different heights were 17.5, 31.7, 28.9, and 22.2% at ground level, 1 m, 1.5 m, and 2 m, respectively.
The numbers captured at different heights followed the overall seasonal dynamics of fruit flies. The number of fruit flies peaked around 18 Jul (Fig. 7) with an average over the 3 yr of investigation of 8.2, 16.4, 14.1, 11.5 individuals per trap per 3 d at ground level, 1 m, 1.5 m, and 2 m above the soil.
At all 4 heights, the numbers of D. melanogaster flies captured were significantly greater than those of the other 3 flies. The maximum number (66.6 ± 21.5 individuals per trap per 3 d) of D. melanogaster were captured 1 m above the soil, but the maximum number (14.6 ± 1.6 individuals per trap per 3 d) of D. suzukii were captured 1.5 m above the soil. The trap numbers of D. hydei and D. immigrans were low at all 4 height levels (Table 1).
Discussion
A great deal of research has been done on the damage caused by Drosophila fruit flies. In Baqiao District, Shanxi Province, D. melanogaster and D. suzukii were found to be the dominant species, comprising 50.2 and 45.9% of the total number of Drosophila, respectively (Guo et al. 2014). Another study found D. melanogaster and Drosophila simulans Sturtevant (Diptera: Drosophilidae) to be the dominant species on Myrica rubra (Ming et al. 2008). In South Korea, D. suzukii is the principal fruit fly pest on cherry and other berries (Guerrieri 2016), whereas in Europe and Turkey, Rhagoletis cerasi (L.) (Diptera: Tephritidae) is the principal fruit fly pest in cherries (Kepenekci et al. 2015). In northeastern Chile, D. suzukii is the most important pest in cherries and strawberry (Arnó & Gabarra 2016). In northern China, we detected an increase in fruit fly abundance from 2014 to 2016, and the principal species were D. melanogaster, D. suzukii, D. hydei, and D. immigrans. Drosophila melanogaster was the dominant species. Drosophila melanogaster is also the dominant species in Sichuan Province, but D. immigrans is present (Guo et al. 2007). In Gansu Province, D. melanogaster is dominant, with D. suzukii and D. hydei also present (Guo 2007). The above reports are basically consistent with our survey. Regional and between-yr differences in fruit fly species presence and importance may be closely related to differences in climate, local environmental factors, and different cultivars.
The synchronization of fruit fly seasonal activity to their host fruits has been reported for various crops in several parts of the world (Lee et al. 2015; Joshi et al. 2017), as well as in China (Zhang et al. 2013; Guo et al. 2014). In the northeastern region of Spain, cherry and strawberry-feeding fruit flies reach their peaks from Mar to Apr (Arnó & Gabarra 2016). However, we found that cherry-feeding Drosophila fruit flies in cherry can be trapped in cherry fruit production. They peak in late Jun to mid-Jul before beginning to decrease. High temperatures usually reduce the number of fruit flies (Harris et al. 2014; Kinjo et al. 2015). We also found that the period of Drosophila fruit fly population decline coincided with high temperatures in Qingdao.
We found significant differences in the number of fruit flies attracted to different cherry cultivars. In our study, the cultivar maturing in the middle of the season (cv. Van) attracted the greatest numbers of fruit flies, followed by the late maturing cultivar (cv. Summit). The early maturing cultivar (cv. Hongdeng) attracted the fewest flies. Late-maturing cultivars usually attract more fruit flies (Guo et al. 2014). The greater occurrence of fruit flies on the mid-season ripening cherry is likely due to the warmer temperatures during this period. Early maturing cv. Hongdeng matured at the end of May, and fruit flies occurred in Jun and Jul. This suggests that the use of an early maturing cherry cultivar like cv. Hongdeng could be recommended to farmers as a way to reduce fruit fly infestation by achieving a harvest before the pest reaches peak abundance.
We also found significant differences in the effectiveness of traps suspended at different heights, with the greatest number of flies caught 1 to 1.5 m above the soil, a finding consistent with the most effective trapping height of 1 to 2 m reported by Darwish et al. (2015). The high fruit fly capture rate also may be related to the flight height of Drosophila fruit flies, though we have no data on this. Our data suggest that traps should be positioned at the 1 to 1.5 m height when monitoring fruit fly populations.
Table 1.
Mean trap captures (± SD) of fly catches by height and species.
Acknowledgments
Van Driesche Scientific Editing did the English editing. We would like to thank Qingmeng Liu and Lu Gong (Qingdao Agricultural University) for the investigation of Drosophila fruit flies in 2014 and 2015, Gabor Lover (Aarhus University, Aarhus, Denmark), and Nianwan Yang (Institute of Plant Protection, Chinese Academy of Agricultural Sciences) for comments and linguistic suggestions for improving the original manuscript. This research was supported by the National Key Research and Development Plan (2016YFC1201200), the Major Scientific and Technological Innovation Project of Shandong Province (2017CXGC0214), the National Natural Science Foundation (31772232), and the high-level talent fund of Qingdao Agricultural University, China.
