The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is polyphagous insect pest, originated in East Asia including Korea, China, Japan and Taiwan (Hoebeke and Carter, 2003). This bug attacks leguminous crops, fruit trees and many ornamental trees. H. halys invaded recently U.S. and Europe (Hoebeke and Carter, 2003; Wermelinger et al., 2008), and has become a major agricultural threat in the mid-Atlantic region of U.S. In Jeju island, Korea, H. halys was considered as an occasional pest in citrus orchards and thought to typically inflict light damage on fruit (Kim et al., 2000). Recently, its' population is found far beyond economic level specially in harvesting season of organic citrus orchard following the pattern of arrowhead scale (Unaspis yanonensis (Kuwana)) and cottony cushion scale (Icerya purchasi Maskell) (Kim et al., 2011; Kim and Kim, 2013).

Many citrus farmers believe that the feeding punctures of H. halys cause fruit decay by providing the route for secondary infection during storage and distribution. Accordingly, some farmers spray insecticides aggressively in the late season, sometimes exceeding the MRL (maximum residue limit). Haphazard spray of synthetic chemical insecticides may induce serious problem in exported fruits. However, there is little information about damage of citrus fruits caused by H. halys feeding in late season, which serve as baseline knowledge for establishing the management guideline against H. Halys. This study was conducted with the aim to explore the feeding effect of H. halys on fruit drop and decay of Mandarine citrus.

Materials and Methods

Laboratory rearing of H. halys

Adult females and males (n = 10 pairs) of H. halys were originally collected from an organic citrus orchard of Jeju-city, Korea, during October and November, 2009. Adults were placed in an acrylic cage (1,100 × 700 × 550 mm) at 24 ± 1℃, 40-70% RH, and a photoperiod of 16:8 (L:D) h in the laboratory. The acrylic cage was mesh windowed (500 × 450 mm) on two narrow sides and closed by a sleeve of cloth mesh (Φ 140 mm) in the front with no holes at the back. Adult H. halys were fed on well dried peanuts (90%) and soybean bean seeds (10%) ad libitum. Twenty to thirty Peperomia plants in a flower pot (Φ 90 mm, 100 ml) were provided as a water source and oviposition substrate for adults and nymphs. The food sources were supplied every two to three weeks, and Peperomia plants were replaced whenever the plants were withered and died by the excessive feeding of H. halys. Wild population (n < 20) of H. halys were recruited a year after the first establishment in 2009. According to the rearing protocol, the population of H. halys was well established in the laboratory condition (see Appendix 11).

Feeding treatments in the laboratory and field

Effects of H. halys on harvested citrus fruits (2010).

Mandarin citrus fruits, Citrus unshiu (Swingle) Marcow were obtained on 11 November, 2010, from citrus orchard of Seogwipo Agricultural Center. For feeding treatment of H. halys, citrus fruits were placed one by one in an insect rearing cage (Φ 90 mm, height 80 mm). One or two adults of H. halys collected from the laboratory colony were introduced into each cage. After 24 h., H. halys adults were removed and the fruits were place in a standard paper box (upper side opened, capacity of 15 kg) for transportation aboard. The decay rate of fruits in paper boxes were examined after 40 d cold storage at 4℃.

Citrus fruits which had been kept for 24 h in cages without the introduction of H. halys were used as untreated control. Each treatments were replicated thrice (10 fruits per replicate).

Feeding effects of H. halys on citrus fruits before and after fruit coloring (2011). Citrus branches of dia. 1 - 2 cm including 9 - 10 fruits were caged using a plastic mesh sleeve (250 × 500 mm, # 1 mm) for feeding study of H. halys in the field. Before fruit coloring on 16 September 2011, 0, 1, 2 or 10 of H. halys adults (laboratory population; sex was not considered) were introduced into each sleeve cage, resulting in 0, 0.1, 0.2 and 1.0 adult per fruit, respectively. Rate of fruits drop was checked on 17 November, 2011 and undropped fruits were harvested. And then the fruits were stored at 4℃ as the same method above, and the decay rate was checked after 50 d. This experiment was replicated 10 times in an experimental orchard block of Mandarin citrus at Jeju National University, Jeju city.

To examine the feeding effect of H. halys on citrus fruits after fruit coloring, 5 adults (0.5/fruit) were introduced into sleeve cages on 6 October, 2011 in an orchard block at Seogwipo Agriculture Center, as the same method above. Fruits were harvested and examined on 17 November, 2011 as the same manner above. This experiment was replicated 9 times.

Statistical analysis. The data sets were subjected to the analysis of variance (ANOVA) to determine statistical differences among treatments (SAS Institute, 1999). Differences in means were then analyzed using Tukey's studentized range test at P = 0.05.

Results

Effects of H. halys feeding on harvested fruits

The feeding of H. halys on harvested citrus fruits did not induced a significant fruit decay during cold storage (F = 1.00, df = 2, 8, P > 0.05), which was based on the data sets obtained after 40 d cold storage at 4℃ after feeding treatment. The decay rate was 0.0, 0.03 and 0.0% in the treatment of 0.0, 1.0, and 2.0 adults per fruit, respectively (Table 1).

Effects of H. halys feeding before and after fruit coloring The feeding of H. halys before fruit coloring significantly affected citrus fruit drop (Table 1). The rate of fruit drop was significantly increased in accordance with increased number of H. halys introduced (F = 91.00, df = 3, 39, P < 0.05). Most citrus fruits were dropped in plots where H. halys was introduced in the rate of one adult per fruit, resulting in 76.1% fall. When 0.1 adult was introduced per fruit, the fruit drop rate was not significantly different with that of untreated control. The feeding of H. halys before and after fruit coloring did not affect significantly fruit decay rate during cold storage (F = 2.81, df = 3, 39, P > 0.05).

The feeding treatment of H. halys after fruit coloring (0.5 adult per fruit) resulted into a low fruit drop rate, being slightly higher than that of 0.1 adult introduction before fruit coloring.

Discussion

The feeding of H. halys on citrus fruits showed different results according to fruit developmental stage. The fruit drop rate in the plot of feeding treatment after fruit coloring (0.5 adults per fruit) was much lower than that in the plot of feeding treatment before fruit coloring, in spite of higher number of H. halys introduced. Lee et al. (2009) reported a similar result in sweet persimmon orchards. The feeding of H. halys during July caused severe fruit drop of sweet persimmon, while it was negligible during September feeding, just leaving pitting spot damage on the fruits. Fruit drop caused by H. halys has not been reported yet in apple, pear and peach orchards (Rings, 1957; Funayama, 2002; Gyeltshen et al., 2005; Kim, 2012). The response of fruits to the feeding of H. halys seems to be different according to fruit ages and the types of fruit trees. For this aspect, further researches are required.

Insect feeding punctures can provide a route for secondary infection for various airborne diseases (Broembsen and Pratt, 2013). This knowledge has been accepted widely by agricultural researchers and extensionists in citrus industry. As a result, late season sprays against plant bugs including H. halys have been justified to prevent the decay of citrus fruits during the storage and distribution in fruit markets. However, this study showed no effect of H. halys feeding on the decay of citrus fruits as well as on fruit drop in late season. The present study can provide baseline to reduce insecticide use against H. halys especially in late season, although fruit quality should be tested further when such sprays are not applied.