Lupi, Dioli, and Limonta: First Evidence of Halyomorpha Halys (Stål) (Hemiptera Heteroptera, Pentatomidae) Feeding on Rice (Oryza Sativa L.)

First Evidence of Halyomorpha Halys (Stål) (Hemiptera Heteroptera, Pentatomidae) Feeding on Rice (Oryza Sativa L.)

Abstract

The brown marmorated stink bug, Halyomorpha halys (Stål) is a pest of numerous annual and perennial crops. Additional distribution records for H. halys are provided from northern Italy where rice is cultivated, and the presence of adults feeding on panicles gives the first evidence of an association between this pest and rice (Oryza sativa L.), a crop not previously recorded as a host plant.





Competing interest statement

The authors declare no potential conflict of interest.

Introduction

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.

Acknowledgements

The authors thank Roberto Scherini for the photo, the rice farmer Riccardo Braggio for observational records, and National Rice Research Institute rice production statistics.

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Figure 1.

Adult of Halyomorpha halys feeding on rice grain in the field (photo Roberto Scherini).

jear-2017-1-6679-g001.jpg
Table 1.

List of the major species of Hemiptera Pentatomidae associated to rice according to geographic distribution.

Distribution Species Literature
North America Oebalus pugnax (F.) Naresh & Smith, 1984; Foster et al., 1989; Espino et al., 2008
Scotinophara coarctata (F.) Heinrichs et al., 1987
Nezara viridula L. Viator et al., 1993
Central America (Cuba) Oebalus ornatus (Sailer) Pantoja et al., 1993
South America Oebalus peoecilus (Dallas) Albuquerque, 1993; Pathak & Khan, 1994
Oebalus ypsilon-griseus (De Geer) Pathak & Khan, 1994
Oebalus grisescens (Sailer) Pathak & Khan, 1994
Tantia antiguensis (Westwood) Litsinger et al. 1986
Tantia perditor (Fabricius) Litsinger et al. 1986
Tibraca limbativentris Stal. Alves et al., 2016
Europe Aelia rostrata Boheman Süss et al., 2008
Carpocoris pudicus (Pd.) Süss et al., 2008
Eurigaster Laporte Süss et al., 2008
Nezara viridula L. Süss et al., 2008
Asia Dolycoris indicus Stal. Litsinger et al. 1986
Eysarcoris ventralis (Westwood) Litsinger et al. 1986
Pygomenida varipennis (Westwood) Pathak & Khan, 1994
Pygomenida bengalensis (Westwood) Pathak & Khan, 1994
Scotinophara scotti Hovarth Litsinger et al. 1986
Nezara viridula L. Pathak & Khan, 1994
Asia (Southeast) Scotinophara coarctata (F.) Barrion et al., 1982
Scotinophara cinerea (Le Guillou) Mochida, 1988
Scotinophara latiuscola Bredding Mochida, 1988
Scotinophara lurida (Burmeister) Mochida, 1988
Scotinophara. serrata (Vollenhoven) Mochida, 1988
Asia (Philippines) Scotinopara tarsalis (Vollenhoven) Litsinger et al., 1986
Asia (Japan) Lagynotomus elongatus (Dallas) Takeuchi et al., 2004
Africa Aspavia armigera F. Ewete & Olagbaju, 1990
Macrina iuvenca Burmeister Litsinger et al., 1986
Nezara viridula L. Pathak & Khan, 1994
Tantia gelii Schout Litsinger et al., 1986
Australia Anaxilaus vesiculosus (Herrich-Schaeffer) Stevens et al. 2008
Eysarcoris trimaculatus (Distant) Stevens et al. 2008
Nezara viridula (L.) Stevens et al. 2008
Table 2.

Municipality in Piedmont and Lombardy rice areas where Halyomorpha halys (Stål) was detected.

Region Municipalities (Province) Rice area, Ha Geographic coordinates Sources
Piedmont Savigliano (Cuneo) 28.88 44°38′53″ N - 7°39′24″ E Pansa et al., 2013
Casale Monferrato (Alessandria) 1777.21 45°08′00″ N - 8°27′09″ E Pansa et al., 2013
S.Giuliano Nuovo (Alessandria) 88.42 44°54′33″ N - 8°36′36″ E Forum Ent. Ital., 2015
Roasio (Vercelli) 13.99 45°36′16″ N - 8°17′05″ E Forum Nat. Med., 2016
Novara 4387.97 45°26′48″ N - 8°37′16″ E Forum Nat. Med., 2014
Lombardy Settimo Milanese (Milano) 6 45°28’10”N - 9°42’64” E Forum Nat. Med.,.2013
San Donato Milanese (Milano) 36 45°23′38″ N - 9°17′27″ E Forum Nat. Med., 2013
Rice Park (Milano) 650 45°27′55″ N - 9°11′11″ E Forum Nat. Med., 2015
Lodi 91.82 45°18′35″ N - 9°30′03″ E Coldiretti 2016
San Martino Siccomario (Pavia) 481 45°09′48″ N - 9°08′26″ E Authors record 2016
Pavia 1318.35 45°11'7"44 N - 9°9'45" E La provincia pavese 2016
Voghera (Pavia) 22.46 44°59′29″ N - 9°00′42″ E Voghera news 2016
Mantova 6.27 45°09′37″ N - 10°47′52″ E Gazzetta di Mantova 2016
Ostiglia (Mantova) 80.27 45°04′11″ N - 11°08′05″ E Gazzetta di Mantova 2016
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