Halyomorpha halys (Stål) (Hemiptera Heteroptera, Pentatomidae), commonly known as the brown marmorated stink bug (BMSB), is native to East Asia (China, Korea, and Japan) (Xu et al., 2014). The invasion of other regions by BMSB began in the mid-1990s in the USA when H. halys was recorded in Pennsylvania and after few years it had spread to 40 states (Hoebeke & Carter, 2003). This species is now established in the United States of America (Northeastern IPM Center, 2014), in Canada and in Central and Southern America (Haye et al., 2015). In Europe, it was first recorded from Switzerland in 2007 (Wermelinger et al., 2008). In Italy it has been reported from various different regions since 2012 (Maistrello et al., 2013; 2014; Cesari et al., 2015; Limonta et al., 2016). It is continuing to extend its distribution in Switzerland, France, Germany, Greece, Hungary, Liechtenstein, Romania, Austria, Serbia (Haye et al., 2015), Russia (Mityushev, 2016) and Spain (Dioli et al., 2016). H. halys has also been intercepted twice in Britain (Malumphy, 2014). As with other invasive pentatomids (Dioli & Grazioli, 2012), BMSB can rapidly spread to new areas through human transportation and the movement of goods, particularly agricultural commodities. The rapid spread of BMSB in Italy has also been facilitated by the climate, which provides excellent conditions for the survival and establishment of large populations of the pest (Zhu et al., 2012).
H. halys, like most pentatomids, has a broad host range that allows it to feed and survive in fruit orchards and legume crops. Lee et al. (2013a) report more than 100 host plants in 45 families from 45 Asian publications. Due to its great host flexibility, H. halys has rapidly become a key pest of many annual and perennial crops in invaded countries (Lee, 2015). In the United States, the insect has caused economic losses valued at 21 billion dollars due to direct commodity damage, market loss, management costs, and rejection of exports (USDA-NIFA SCRI, 2013; Leskey et al., 2012). In Italy, economic damages has been observed close to harvest in peach and pear orchards and also in apricots, plums, apples, persimmons, and tomatoes (Pansa et al., 2013; Bariselli et al., 2016).
Feeding injury by H. halys results in seed loss, punctures, fruit deformation, suberization, formation of spongy areas, fruit abortion, necrosis, and also destroyed pods (Lee, 2015). Adults and nymphs are extremely active and can readily move between different cultivated and ornamental host plants (Lee et al., 2013b).
Recently BMSB was detected in many of the rice areas in the Po plain in Italy, but due to its polyphagy its role in the crop remained uncertain. As a consequence, its status in rice needs to be further evaluated, despite the fact that BMSB is widely distributed in other rice-producing countries and rice has not been identified as a host plant in the published literature. Rice production in Europe has been threatened by the exotic rice water weevil Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae) which has compromised production in this economically important crop (Lupi et al., 2009; 2013a; 2013b), and consequently concern has arisen about the possible association of H. halys with rice. Several species of Pentatomidae are known to attack rice and to cause economic losses in many rice-producing countries (Table 1). Damage is caused by adults and nymphs feeding on kernels in milk and dough stage of maturation, resulting in partially or totally unfilled grains (Lee et al., 1993; Pathak & Khan, 1994; Patel et al., 2006, Kiritani, 2007). Trophic activity can also open an access to fungi and bacteria that are responsible for pecky rice, which leads to chalky discoloration around the feeding site (Hollay et al., 1987; Panizzi et al., 2000).
This study provides the first direct observations of BMSB feeding on cultivated rice crops.
Materials and Methods
The research was carried out in the rice growing areas of the Po Valley in the Lombardy region of Italy. The two main rice producing provinces (Milan and Pavia) are contiguous, and they are characterized by a fragmented landscape in which rice is the main crop and rice paddies are interspersed with populated areas. Due to the distinctive characteristics of the different instars of the insect (Hoebeke & Carter, 2003), visual observations were made directly in paddy fields and in nearby areas from late August to the end of October 2016.
Observations are discussed comparing previous records of BMSB (author’s communication, published records and the internet).
Results and discussion
Earlier records exist of Halyomorpha halys from different rice areas in Northern Italy and also from Milan and Pavia provinces, however the insect was has not previously been directly associated with rice crops. Even though rice is cultivated in 129 Piedmont and 216 Lombardy Municipalities (data courtesy of Italian National Rice Research Institute, 2016), only 14 records of this species have previously been reported from the rice area, mainly in 2016 (Table 2).
The observations carried out in rice crops in the Lombardy Region resulted in two records of BMSB on rice in Pavia Province: the first detection of the species on panicles was on the 24th September 2016 in Linarolo (45°9’47”88 N 09°16’15”60 E) and a second record was obtained a month later on 20th October 2016, in Zeme (45°11’74 N;8°38’25 E) nearly 60 km away. The probing activity on rice grain shown in Figure 1 provides evidence that the insect is attracted to rice for feeding.
Whilst the presence of H. halys in the Piedmont and Lombardy rice areas has been well documented, the nature and extent of the feeding damage that could be inflicted to rice by BMSB requires further investigation. The majority of municipalities in which H. halys has been detected so far are, have only low levels of rice production. The findings from 2014 in Novara and in 2016 in Pavia, the major rice areas in Piedmont and in Lombardy respectively, demonstrates that the insect is still spreading in the rice area and highlights the need for further work on the association between BMSB and rice.
As rice cultivars differ in susceptibility to invasive species attack (Lupi et al., 2009; 2013b) and also to the development of pecky rice in response to pentatomid feeding (Lorenz & Hardke, 2013), particular attention should be paid to the association of H. halys with specific cultivars and to the level of damage inflicted. The timing of feeding relative to the developmental stage of the crop should be assessed, as the amount and the type of rice stink bug damage depends upon the stage of rice kernel development.