EPPO Global Database

First record of Halyomorpha halys in Switzerland: addition to the EPPO Alert List

In August 2007, the Swiss Forest Protection Service received a sample of bug nymphs which had been collected from a garden at Erlenbach, near Lake Zürich, Switzerland (Wermelinger et al., 2008). These unusual bugs were observed feeding on various exotic ornamental shrubs. Nymphs were collected and reared on shoots of Buddleia davidii; the resulting adults could then be identified as Halyomorpha halys (Heteroptera: Pentatomidae – brown marmorated stink bug). Other specimens which had been collected in summer and autumn 2007 were also identified as H. halys. In total and in chronological order, the following specimens have been reported from the city of Zürich and its surroundings:

- 2 egg masses and several nymphs feeding on Asparagus at Zürich.

- 1 nymph feeding on a seed of Acer pseudoplatanus at Adliswil.

- numerous specimens were found in a garden at Erlenbach infesting ornamental shrubs at various levels (very heavy infestations found on Decaisnea fargesii, Stewartia pseudocamellia (1 attacked plant died), heavy infestations on Aralia elata, Tropaeolum majus, and minor infestations on Amelanchier lamarckii and Buddleia davidii).

- 1 nymph on an unknown plant in the Chinese Garden at Zürich-Riesbach.

- 1 adult found in an apartment at Zürich-Friesenberg.

The origin of the introduction of H. halys into Switzerland remains unknown but it is suspected that it was imported with woody plants. This is the first report of H. halys in Switzerland and in Europe.

H. halys is a highly polyphagous pest originating from Asia where it is considered as a pest on a wide variety of crops (soybean, fruit crops, woody ornamentals). H. halys has recently been introduced into the USA where its presence was first confirmed in 2001 in Pennsylvania. It then spread very rapidly to several Mid-Atlantic States and isolated populations were found on the Pacific coast (California and Oregon). It was primarily found on woody ornamentals and backyard fruit trees growing in urban or suburban environments, however since 2006 damage has started to be reported from commercial fruit tree orchards. In addition to plant damage, H. halys can become a nuisance in residential areas when it aggregates on buildings and houses seeking shelter for overwintering. Considering the invasive behaviour of H. halys in the USA, its polyphagy, and its recent introduction into Switzerland, the EPPO Secretariat decided to add H. halys to the EPPO Alert List.

Halyomorpha halys (Heteroptera: Pentatomidae – brown marmorated stink bug)

Why: The attention of the EPPO Secretariat was attracted by Dr G. Schrader (JKI, Germany) and Dr Wermelinger (Swiss Federal Institute WSL, CH) to the first record of Halyomorpha halys in Switzerland and in Europe. H. halys is a highly polyphagous pest of Asian origin which was recently introduced into the USA.

Where: H. halys originates from Asia. In the USA, it was first identified in 2001 in Allentown in Pennsylvania, although it is thought that it was present earlier (since 1996-1998). It is suspected to have been imported in packing crates from Asia. Within a few years, H. halys rapidly spread across Pennsylvania and New Jersey, and then to several Mid-Atlantic States, showing a invasive behaviour. Isolated populations were also found on the west coast in Oregon and California, probably transported there by human activities.

EPPO region: Switzerland (first found in 2007).

Asia: China (Anhui, Fujian, Guangdong, Guangxi, Guizhou, Hebei, Heilongjiang, Henan, Hubei, Hunan, Jiangsu, Jiangxi, Jilin, Liaoning, Neimenggu, Shaanxi, Shanxi, Sichuan, Xizhang, Yunnan, Zhejiang), Japan, Korea Republic, Taiwan.

North America: USA (California, Delaware, Maine, Maryland, Massachusetts, New Jersey, New York, Ohio, Oregon, Pennsylvania, Rhode Island, South Carolina, Virginia, West Virginia).

On which plants: H. halys is a highly polyphagous pest attacking more than 100 plant species, primarily fruit trees and woody ornamentals, but also field crops. Fruit crops: Citrus spp., Diospyros spp., Malus domestica (apple), Morus spp., Prunus armeniaca (apricot), P. avium (cherry), P. domestica (plum), P. persica (peach), Pyrus communis (pear), Rubus idaeus (raspberry) and Vitis vinifera (grapevine). Field crops: Asparagus, Glycine max (soybean), Phaseolus vulgaris (common bean), Zea mays (maize). Forest and ornamental trees/shrubs: Abelia, Acer, Buddleia davidii, Cryptomeria, Cupressus, Hibiscus, Lonicera, Paulownia tomentosa, Rosa rugosa, Salix. In Asia, H. halys has also been found on weeds (e.g. Actrium spp.).

Damage: In the USA, H. halys has one generation per year but in its native range 5-6 generations per year have been reported. It overwinters in the adult stage (diapause). Adults are 12-17 mm long, brownish or grayish, mottled and variable in size and colour. In summer, females lay eggs (50-150 eggs and up to 400 eggs, clustered by groups of 20-30) on the underside of the leaves. There are 5 larval stages (nymphs). The pronotum of the younger nymphs is armoured with spines, and the tibiae of instars 3 to 5 show a white band.

Pictures can be viewed on the Internet: http://www.insectimages.org/browse/subthumb.cfm?sub=9328&start=1
http://www.wsl.ch/forschung/forschungsunits/walddynamik/waldinsekten/aktuell/halyomorpha_EN

Like other true bugs, H. halys feeds by sucking plant juices. Adults generally feed on fruit, whereas nymphs feed on leaves, stems and fruit. The most important crop damage results from insect feeding on pome and stone fruits, and on seeds inside legume pods (e.g. beans and soybean). Leaf feeding is characterized by small lesions (3 mm diameter) which may then become necrotic and coalesce. Attacked fruits may present small necrotic spots or blotches, grooves and brownish discolorations. In cases of heavy infestations, fruit are severely disfigured and rendered unmarketable. In Asia, H. halys is considered as causing significant damage to soybean and various horticultural crops. In Northern Japan, apple crops have increasingly been damaged by H. halys. Forest trees are known hosts of H. halys, but no damage has been reported in Asian forests. However, in Japan H. halys is considered as a pest in nurseries producing seeds of cedar and cypress because it can feed on cones. In the USA, damage caused by H. halys was initially reported in suburban or urban environments on woody ornamentals (e.g. Buddleia davidii, Paulownia tomentosa) and backyard peach and pear trees. However in 2006, commercial fruit growers started to report damage in apple and pear orchards in eastern Pennsylvania and western New Jersey. In Pennsylvania, high populations were also found in soybean crops but without significant damage. H. halys is considered as a vector of Paulownia witches’ broom phytoplasma in Asia. Preliminary studies done in the USA did not detect any phytoplasma in the pest populations from Pennsylvania.

In addition to plant damage, H. halys can be a nuisance to humans because at the end of autumn, adults can aggregate in buildings and houses (on walls, window and door frames) seeking overwintering sites. When disturbed or crushed they discharge a characteristic pungent odour (unpleasant and long lasting!). In the USA, many homeowners are complaining about this nuisance.

Dissemination: H. halys is a strong flyer and a highly mobile pest which can move from host to host during the growing season (e.g. from early-ripening fruits to late-ripening ones). Over long distances, the pest can be disseminated by trade of host plants but also by movements of goods or vehicles. For example, in California it is suspected that the first bugs were introduced with household items as they were found on a property whose owner had recently moved from Pennsylvania. Until now, the pathways of introduction of H. halys into the USA or Switzerland remain unknown but it is suspected that the pest was introduced either as a hitchhiker on packing material or via plant imports.

Pathway: Plants for planting, fruits and seeds? packing material, hitchhiking on non-agricultural products.

Possible risks: In USA, new findings of H. halys have to be notified the authorities and it is considered that the pest has the potential to invade agricultural areas and pose a risk to an increasing number of crops as it continues to expand its geographic range. For many crops, it is not known whether existing management strategies already applied against other bugs or insect pests might also apply to H. halys. In the EPPO region, although more studies are needed to determine whether H. halys can establish and spread within the EPPO region, it cannot be excluded that H. halys might become a damaging pest, in particular on pome and stone fruit trees.

EPPO RS 2008/200
Panel review date: -	Entry date 2008-10

Sources

Bernon G, Bernhard KM, Hoebeke ER, Carter ME, Beanland L (2004) Halyomorpha halys (Heteroptera: Pentatomidae), the brown marmorated stink bug: are trees the primary host for this new invasive pest? Proceedings of the 15th USDA Interagency Research Forum on Gypsy Moth and Other Invasive Species (Annapolis, US, 200401-13/16), p 12.

Hiruki C (1999) Paulownia witches' broom disease important in East Asia. Acta Horticulturae no 496, 63-68.

Mitchell PL (2004) Heteroptera as vectors of plant pathogens. Neotropical Entomology 33(5), 519-545.

Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen der Schweizerischen Entomologischen Gesellschaft 81, 1-8.

INTERNET (last retrieved in 2008-11)

California Department of Food and Agriculture. California Plant Pest and Disease Report, July 2002 to July 2005, Volume 22(1), p 8-9. http://www.cdfa.ca.gov/PHPPS/ppd/PDF/CPPDR_2005_22-1.pdf

Massachusetts Natural Resources Collaborations. Introduced Pests Outreach Project. Brown marmorated stink bug found in Massachusetts (March 2007). http://massnrc.org/pests/linkeddocuments/pestalerts/BMSB

NPPO Phytosanitary Pest Alert System. http://www.pestalert.org

- Alert (2001-10-17) Asian stink bug infestation in Pennsylvania.

- Alert (2002-10-02) Brown marmorated stink bug, Halyomorpha halys in US (Pennsylvania)

- Alert (2003-11-05) The brown marmorated stink bug, Halyomorpha halys Stal (Heteroptera: Pentatomiidae) found in Hagerstown, Maryland

- Alert (2005-01-07) Brown marmorated stink bug (Halyomorpha halys) in Oregon.

North Dakota State University, Fargo. Halyomorpha halys Stal, 1855. http://www.ndsu.nodak.edu/ndsu/rider/Pentatomoidea/Species_Cappaeini/Halyomorpha_halys.htm

Ohio State University. Fact Sheet. Brown marmorated stink bug. http://ohioline.osu.edu/hyg-fact/pdf/FS_3824_08.pdf

PennState. Entomology Department. Entomological Notes. Brown marmorated stink bug. http://www.ento.psu.edu/extension/factsheets/pdfs/brMarmoratedStinkBug.pdf

Rutgers University of New Jersey. Agricultural Experiment Station. Brown marmorated stink bug – A non-native insect in New Jersey. Fact Sheet FS002. http://njaes.rutgers.edu/pubs/publication.asp?pid=fs002

Swiss Federal Institute for Forest, Snow and Landscape Research WSL. A new invasive species in Europe: The brown marmorated stink bug. http://www.wsl.ch/forschung/forschungsunits/walddynamik/waldinsekten/aktuell/halyomorpha_EN

University of Florida. Featured Creatures. Gyelstshen J, Bernon G, Hodges A (2008) Brown marmorated stink bug, Halyomoprha halys Stahl (Insecta: Hemiptera: Pentatomidae). http://creatures.ifas.ufl.edu/veg/bean/brown_marmorated_stink_bug.htm