Arthropod-Plant Interactions (2018) 12:517–529 https://doi.org/10.1007/s11829-017-9583-8

ORIGINAL PAPER

Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in , , and Serbia: history of invasion, range expansion, early stages of establishment, and first records of damage to local crops

Dmitry L. Musolin1,6 · Aleksandra Konjević2 · Natalia N. Karpun3 · Vilena Ye. Protsenko3 · Lesik Ya. Ayba4 · Aida Kh. Saulich5

Received: 28 May 2017 / Accepted: 8 November 2017 / Published online: 15 November 2017 © Springer Science+Business Media B.V., part of Springer Nature 2017

Abstract Halyomorpha halys is native to Asia, but was recently accidentally introduced to North America and Europe. This species was recorded for the first time in Russia in 2013 (2014) and in both Serbia and Abkhazia in 2015. In 2015–2017, we con- ducted surveys in Russia, Serbia, and Abkhazia and found that H. halys had not only successfully survived its first winters in new regions, but also started to establish locally, spread, increase populations, and damage local crops. In Sochi (Russia) and Abkhazia, H. halys was recorded to feed on 32 species and cultivars from 16 plants families. In Serbia, it has so far been observed on only four species from four plant families. H. halys is already widely spread in Abkhazia and causes serious damage to many crops: in 2016, the yield of peach, mandarin orange, persimmon and other crops fell down by 13.2–87.4% if compared to the long-term means of yield. The losses are likely to be mostly caused by feeding of H. halys. We conclude that H. halys was accidentally introduced to Russia in 2012–2013 most likely with woody plants imported to Sochi from Italy or Greece for urban landscaping before the 2014 Winter Olympics. The species established in Sochi and quickly moved to Krasnodar (Russia), Abkhazia, and beyond—to . Populations in Serbia most likely arrived in 2015 traveling on railway cars or in commodities on the Bucharest–Belgrade railway line. We discuss phenology and prospects of further expansion of H. halys in Europe.

Keywords Exotic pest · Hemiptera · Invasion · Phenology · Range expansion · Secondary range

Handling Editor: Heikki Hokkanen. Introduction * Dmitry L. Musolin [email protected] The brown marmorated stink bug Halyomorpha halys

1 (Stål) (Heteroptera: Pentatomidae) is native to Asia, mostly Saint Petersburg State Forest Technical University, Institutskiy per., 5, Saint Petersburg, Russia 194021 to China (except Xinjiang and Qinghai provinces), Korea, 2 Japan (except Hokkaido), Myanmar, Vietnam, and Taiwan Faculty of Agriculture, University of Novi Sad, Trg Dositeja Obradovica, 8, Novi Sad 21000, Serbia (Wang and Liu 2005). This large pentatomid produces 1–3 3 complete generations per year and often has a high popula- All-Russian Research Institute of Floriculture and Subtropical Cultures, Jānis Fabriciuss str., 2/28, tion density (Yanagi and Hagihara 1980; Lee et al. 2013; Krasnodar Region, Sochi, Russia 354002 Haye et al. 2015; Hamilton et al. 2017; Saulich and Musolin 4 Institute of Agriculture, Academy of Sciences of Abkhazia, 2017). It overwinters in the adult stage and is often con- Gulia str., 22, Sukhum 384900, Abkhazia sidered a nuisance pest in urban areas due to its diapause- 5 Saint Petersburg State University, Universitetskaya nab., 7–9, related behavior, which manifests as large overwintering Saint Petersburg, Russia 194021 aggregations in houses and other artificial constructions 6 Department of Forest Protection, Wood Science (Rice et al. 2014; Musolin and Saulich 2017). In addition, and Game Management, Saint Petersburg State Forest H. halys is a highly polyphagous pest of many economically Technical University, Institutskiy per., 5, Saint Petersburg, important agricultural crops, including various vegetables, Russia 194021

Vol.:(0123456789)1 3 518 D. L. Musolin et al. fruit trees, soybean, and many more (Lee et al. 2013; Rice Materials and methods et al. 2014; Hamilton et al. 2017). In 2001, H. halys was recorded for the first time in the Russia USA, although it is believed that the first individuals were seen without an appropriate identification in 1996 in Penn- Following the early records of H. halys in two nearby loca- sylvania (Hoebeke and Carter 2003). Then the species spread tions in Sochi City in the early August 2014 (Mityushev to other parts of the USA and by 2004, had been recorded in 2016), in 2015–2017, we conducted regular surveys of the New Jersey, Delaware, Maryland, and Virginia (Leskey and species in and around Sochi paying special attention to dif- Hamilton 2010a, b). By 2009, H. halys had been detected in ferent host plants that could attract this polyphagous pest 17 additional states including California, Oregon, and North (Fig. 1). Fruit trees and various plants in agricultural fields, Carolina (Leskey and Hamilton 2011). By 2015, it had been orchards, parks, etc., were carefully inspected every 10 days recorded in at least 41 states and the District of Columbia in from April to November. Insects were collected by hand and the USA (Leskey and Hamilton 2015; Hamilton et al. 2017) by sweep nets. The presence of different stages of H. halys as well as in Canada (Gariepy et al. 2014). and their abundance were recorded. Abundance of H. halys In Europe, the first record of H. halys (from Switzerland was estimated using three comparative levels: sporadic (only and Liechtenstein) dates back to 2004 (Arnold 2009; Haye individual egg masses, nymphs, and/or adults recorded on et al. 2014). During the first years following the initial intro- individual specimens of a particular plant species), abun- duction, the European population was small and restricted to dant (some number of egg masses, nymphs, and/or adults the Canton Zurich area in Switzerland (Wermelinger et al. recorded on some specimens of a particular plant species), 2008), but soon the species invaded Central and Southern and highly abundant (numerous egg masses, nymphs, and/ European countries such as France, Germany, Italy, Greece, or adults recorded on many specimens of a particular plant and recently Spain and some others (Haye et al. 2015; Dioli species). Identity of H. halys was confirmed by Dr. V.V. et al. 2016). In 2017, H. halys was recorded in Kazakhstan Neimorovets (All-Russian Institute of Plant Protection, Saint (Esenbekova 2017). The species has been intercepted in the Petersburg, Russia). Voucher specimens were deposited in UK, although not in the wild, but in the luggage of a pas- the insect collection of the All-Russian Research Institute of senger traveling from the USA and also in a shipment from Floriculture and Subtropical Cultures (Sochi). China (Malumphy 2014). Rapid invasions of H. halys from Asia to both North Abkhazia America and Europe are commonly linked to the recently increased global trade and travel. The diapause-associated From September 2015 to August 2017, several special behavior of the adults aimed at searching for dark-protected research trips were organized by the All-Russian Research microhabitats suitable for overwintering including, e.g., rail- Institute of Floriculture and Subtropical Cultures (Sochi, way cars, trucks, luggage, and packaging material (Hamil- Russia) and Institute of Agriculture of Abkhazia Academy ton et al. 2017), and this behavior likely contributes to the of Science (Sukhum, Abkhazia) to different areas of Abk- species’ invasive speed and success. H. halys was recently hazia, a region neighboring Sochi, to check the presence of recorded for the first time in Russia (in 2013 or 2014; Gapon H. halys there (Fig. 1). Potential host plants were surveyed 2016; Mityushev 2016), Serbia (in 2015; Šeat 2015), and (as in Sochi, see above) and the presence of eggs, nymphs, Abkhazia (in 2016; Gapon 2016). First country records are and adults of H. halys was recorded. Voucher specimens interesting faunistic information which—without further were deposited in the insect collection of the All-Russian studies—cannot prove that the once recorded species has Research Institute of Floriculture and Subtropical Cultures successfully survived unfavorable seasons (usually winter), (Sochi). In addition, at the end of agricultural season of established locally, started to spread in the area, and build 2016, the data on yield of major local agricultural crops a local population. In this paper, we report the first data on were collected and compared to those for 1996–2015 with establishment of H. halys in these countries, provide infor- the purpose to estimate the losses of yield caused by feeding mation on local host plants, phenology, and first estimates of of H. halys (see Table 2 for details). the damage caused by this species to local crops. We define more precisely the first arrival of H. halys in Abkhazia: not Serbia in 2016, but already in 2015. Finally, we discuss how the species could have invaded these countries and the possi- H. halys bility of further invasive range expansion of this potentially Following the original record of in Belgrade and dangerous pentatomid in Eurasia. in the north-east of Serbia in October–December 2015 (Šeat 2015), in 2016, we conducted a survey of the spe- cies presence in the areas where the presence of H. halys

1 3 Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae)… 519

Fig. 1 Regions of the surveys. All countries and locations men- Romania: 7 Bucharest, 8 Timisoara; Serbia: 9 Vatin and Plandište tioned in the text are indicated. Cities/towns: Russia: 1 Krasnodar, (located very close to each other), 10 Vršac and Jasenovo (located 2 Maykop; 3 Sochi; Abkhazia: 4 , 5 Sukhum, 6 Gulripshi; very close to each other), 11 Belgrade was revealed a year before, in order to collect data about its (Mityushev 2016). A few months later, another record was current status and see whether the species survived winter, published claiming that several individuals of H. halys were spread, and increased its population (Fig. 1). In survey of seen in Sochi as early as in 2013 (Gapon 2016). 2016, the urban areas were covered along with agricultural Following the first records, a detailed survey was con- areas nearby. Different plant species were carefully exam- ducted in and around Sochi in 2015–2017 (this study). Dur- ined, with special attention paid to soybean, apple, pear, and ing the survey, different stadia of H. halys were repeatedly vegetables (Kuhar et al. 2012). Specimens of H. halys were recorded in large numbers in all four city districts of Sochi collected mostly by hand, during the visual inspections of (ranging from 43°91′N; 39°33′E to 43°39′N; 40°00′E) on above ground parts of the plants, including stems, leaves, 26 species and cultivars from 15 families of plants (Table 1; buds, and/or fruits. In certain crops, such as soybean, sweep Fig. 2a). On horticultural and vegetable plants, nymphs nets were used. The most intensive sampling was conducted and adults were mostly recorded on fruits, on ornamental during August and early September, 2016. Specimens col- plants—on leaves and fresh shoots. The damage was most lected from different plants were taken to the laboratory to significant on horticultural and vegetable plants: fruits were confirm field identification, based on morphological char- deformed on apples and pears; citrus, persimmon, and grape acters (Wyniger and Kment 2010). Voucher specimens were fruits failed to develop and fell down prematurely; kernels deposited in the true bugs collection at the Faculty of Agri- of hazelnut failed to develop, and so on (Fig. 2c, d). The culture, University of Novi Sad (Novi Sad). highest population density was recorded in the Adler district of Sochi (the Lowlands), the location of the major construction work and landscaping for the 2014 Winter Results and discussion Olympics. In September 2016, adults of H. halys were recorded Russia further northward—in Krasnodar City (close to the local airport, 45°03′N; 39°14′E; and in houses downtown, As reported earlier, in August 2014, one nymph of H. halys 45°02′N; 38°59′E; Fig. 1) on C. speciosa (Warder) Warder was recorded on leaves of rose Rosa sp. (Rosaceae) in ex Engelm. (Bignoniaceae) and in March 2017, further the park Riviera (43°35′N; 39°43′E) and two nymphs on eastward—in Maykop City (44°37′N; 40°07′E) in overwin- Pittosporum tobira (Thunb.) W.T. Aiton (Pittosporaceae) tering microhabitat (artificial construction) (both records: in Dendrarium (43°36′N; 39°42′E), both located in Sochi B.A. Borisov, personal communication). In summer of

1 3 520 D. L. Musolin et al. abundant 28–31, September 24–October 15, highly 15, highly 24–October 28–31, September abundant abundant; 2017: September 12–November abundant; 12–November 2017: September abundant 1, highly July 20–30, abundant July Abkhazia – – 2017: June 28–30, sporadic 2016: July 15–31, highly abundant 15–31, highly 2016: July – 2017: July 20–25, sporadic 2017: July 2016: July 5–31, August 5–31, highly 5–31, highly 5–31, August 2016: July 2015: September 1–30, sporadic; 2016: July 2016: July 1–30, sporadic; 2015: September 2016: July 15–31, highly abundant 15–31, highly 2016: July 2017: July 22–August 12, abundant 22–August 2017: July – 2016: September 24–October 15, highly 15, highly 24–October 2016: September – – 2017: July 20–25, sporadic 2017: July 2016: July 15–31, highly abundant; 2017: 15–31, highly 2016: July – dant; 2017: July 21, abundant dant; 2017: July - 4, Septem 25–August 2016: July radic; abundant 20, highly ber 15–October - abundant; 15–Novem 2017: September abundant ber 3, highly 15–31, highly abundant 15–31, highly Dates and estimated abundance, by region abundance, by Dates and estimated Russia 2017: August 14–16, sporadic 2017: August 2017: August 14–16, sporadic 2017: August 2017: June 28–30, sporadic 2016: July 15–31, highly abundant 15–31, highly 2016: July 2016: May 5–15, June 28, highly abun - 5–15, June 28, highly 2016: May 2017: July 21–August 12, abundant 21–August 2017: July 2016: June 1–10, sporadic abundant 5–31, highly 5–31, August July 2015: September 15–October 20, spo - 15–October 2015: September – – 2017: August 10–13, sporadic 2017: August 2016: September 21–October 20, highly 20, highly 21–October 2016: September 2017: August 15, sporadic 2017: August 2017: August 8, abundant 2017: August 2017: July 10–20, sporadic 2017: July 2015: July 20–25, sporadic; 2016: July 2016: July 20–25, sporadic; 2015: July 2017: August 15, sporadic 2017: August Halyomorpha halys of Halyomorpha Stages Nymphs of III instars, adults Nymphs Egg masses Nymphs of I–II instars Nymphs Nymphs of III–V instars Nymphs Egg masses Nymphs of II–IV instars Nymphs Nymphs of I–V instars Nymphs Adults Nymphs of III–V instars and adults Nymphs Nymphs of III–IV instars Nymphs Nymphs of II–III instars Nymphs Adults Nymphs of III–IV instars Nymphs Nymphs of III instar Nymphs Nymphs of III–IV instars Nymphs Nymphs of III–V instars and adults Nymphs Nymphs of IV–V instars Nymphs Parts of the plant Leaves Leaves Nuts Nuts Leaves Leaves Leaves, shoots Leaves, Leaves Leaves, fruits Leaves, Leaves Fruits Fruits Leaves Leaves Fruits, leaves Fruits, leaves Leaves in Russia (Sochi) and Abkhazia (based on the records from the surveys of 2015–2017) the (based on the from surveys records and Abkhazia (Sochi) in Russia plants and periodsHost halys of Halyomorpha of presence Liang et A.R. Ferguson Liang et A.R. ex Engelm. (A.A. Chev.) C.F. C.F. deliciosa (A.A. Chev.) Actinidia Chrysanthemum sp. Corylus pontica K. Koch (Warder) Warder Warder speciosa (Warder) Catalpa Cucumis sativus L. Diospyros kaki Thunb. Diospyros L. Hippophaë rhamnoides Gleditsia triacanthos L. L. Phaseolus vulgaris Robinia pseudoacacia L. Robinia 1 Table family) plant (by Host Actinidiaceae Asteraceae Betulaceae Bignoniaceae Cucurbitaceae Ebenaceae Elaeagnaceae Fabaceae

1 3 Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae)… 521 July 20–30, August 10–20, abundant 20–30, August July tember 23–24, sporadic abundant 15, highly abundant; 2017: September 15, highly 15, abundant 20–October abundant Abkhazia 2017: August 2–10, abundant 2017: August 2016: July 15–31, highly abundant; 2017: 15–31, highly 2016: July – – 2016: May 25, sporadic 2016: May – 2016: August 10–31, sporadic; 2017: Sep - 10–31, sporadic; 2016: August – 2016: July 5–31, August 5–31, highly 5–31, highly 5–31, August 2016: July – 2016: July 28–31, September 24–October 24–October 28–31, September 2016: July – 2016: May 5–15, sporadic 2016: May 2016: May 15, sporadic 2016: May 2016: June 10–20, July 4, sporadic 2016: June 10–20, July 2016: July 4, sporadic 2016: July 2016: July 4, sporadic 2016: July 2016: July 4, sporadic; 2017: July 20–30, 2017: July 20–30, 4, sporadic; 2016: July – – – – abundant dant; 2017: July 21, abundant dant; 2017: July 5–31, August 5–31, highly abundant 5–31, highly 5–31, August October 20, highly abundant 20, highly October 5–16, highly abundant 5–16, highly 15–20, sporadic Dates and estimated abundance, by region abundance, by Dates and estimated Russia 2017: July 2–10, August 1–5, sporadic 2–10, August 2017: July 2016: July 15–31, August 14–25, highly 14–25, highly 15–31, August 2016: July 2017: June 15–20, sporadic 2017: June 18–30, sporadic – 2017: July 25, sporadic 2017: July – 2016: May 5–15, June 28, highly abun - 5–15, June 28, highly 2016: May 2016: June 1–10, sporadic 2016: July 2016: July 2016: June 1–10, sporadic 2017: July 21–August 12, abundant 21–August 2017: July 2016: July 25–August 4, September 15– 4, September 25–August 2016: July 2015: August 8, sporadic; 2016: August 2016: August 8, sporadic; 2015: August 2016: May 11, sporadic 2016: May – 2016: June 13–17, sporadic 2016: June 21–30, sporadic; 2017: June 2016: June 21–30, sporadic; – 2017: July 20–30, sporadic 2017: July 2017: June 20–25, sporadic 2017: June 25–July 10, sporadic 2017: June 25–July 2017: August 14–16, sporadic 2017: August 2017: June 10–22, sporadic Halyomorpha halys of Halyomorpha Stages Nymphs of I–II instars Nymphs Nymphs of III–V instars Nymphs Egg Nymphs of I–II instars Nymphs Nymphs of III–V instars Nymphs Egg masses Nymphs of III–V instars Nymphs Egg masses Nymphs of I–V instars Nymphs Nymphs of II–IV instars Nymphs Adults Adults Egg masses Nymphs of I–II instars Nymphs Nymphs of III–V instars Nymphs Adults Nymphs of III instar Nymphs Nymphs of III instar Nymphs Egg masses Nymphs of I–III instars Nymphs Nymphs of IV instar Nymphs Adults Parts of the plant Fruits Fruits Leaves Leaves, fruits Leaves, Fruits Leaves Fruits Leaves Leaves, shoots Leaves, Leaves Leaves Leaves Leaves Leaves Fruits Fruits Leaves Fruits Leaves Fruits Fruits Leaves Ficus carica L. Ficus Morus alba L. L. excelsior Fraxinus L. Olea europaea (Thunb.) Steud. tomentosa Paulownia Pittosporum spp. Malus spp. Prunus avium (L.) L. Prunus L. domestica L. Prunus laurocerasus 1 Table (continued) family) plant (by Host Moraceae Oleaceae Paulowniaceae Pittosporaceae Rosaceae

1 3 522 D. L. Musolin et al. abundant abundant; 2017: October 14–November abundant; 14–November 2017: October 2, abundant 15, highly abundant; 14– 2017: October 15, highly 2, abundant November 2017: October 14–November 2, abundant 14–November 2017: October Abkhazia 2016: May 5–15, sporadic 2016: May 2016: June 10–20, July 4, sporadic 2016: June 10–20, July 2017: July 20–30, abundant 2017: July 2016: July 4, sporadic; 2017: July 20–30, 2017: July 4, sporadic; 2016: July 2016: May 5–15, sporadic 2016: May 2016: June 10–20, sporadic 2016: July 4, sporadic 2016: July 2017: August 26–27, sporadic 2017: August – – – – 2016: September 24–October 15, highly 15, highly 24–October 2016: September 2016: August 5–31, highly abundant 5–31, highly 2016: August 2016: July 28–31, September 24–October 24–October 28–31, September 2016: July 2016: September 1–9, abundant 2016: September 2016: September 28–October 15, abundant; 28–October 2016: September 20–30, sporadic 15–20, abundant dant Dates and estimated abundance, by region abundance, by Dates and estimated Russia 2016: May 11, sporadic 2016: May 2016: June 13–17, sporadic 2017: July 20–30, sporadic 2017: July 2016: June 21–30, sporadic; 2017: July 2017: July 2016: June 21–30, sporadic; – 2016: June 13–17, sporadic 2016: June 21–30, sporadic; 2017: June 2016: June 21–30, sporadic; 2015: August 8, sporadic 2015: August 2016: July 5, August 5–16, highly abun - 5–16, highly 5, August 2016: July 2017: August 15, sporadic 2017: August 2016: July 5, August 5–16 5, August 2016: July abundant highly 2016: August 10, sporadic 2016: August – – – – – Halyomorpha halys of Halyomorpha Stages Egg masses Nymphs of III–V instars Nymphs Nymphs of III–IV instars Nymphs Adults Egg masses Nymphs of III–V instars Nymphs Adults Adults Egg masses and adults Nymphs of III instar Nymphs Adults Egg masses and nymphs of I–II instars Egg masses and nymphs Adults Nymphs of I–V instars Nymphs Adults Nymphs of IV–V instars Nymphs Adults Parts of the plant Leaves Fruits Fruits Fruits Leaves Fruits Fruits Leaves Leaves Leaves Shoots Leaves Fruits Fruits Fruits, leaves Leaves, fruits Leaves, Leaves, fruits Leaves, (L.) Batsch Prunus persica Pyrus communis L. spp. cult. Rosa Citrus limon (L.) Osbeck Cítrus × meyeri Yu. Tanaka Macfad Citrus paradisi 1 Table (continued) family) plant (by Host Rutaceae

1 3 Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae)… 523 dant; 2017: August 10–13, abundant dant; 2017: August dant abundant; 2017: August 26–September 26–September abundant; 2017: August 16, abundant 28–31, September 28–October 15, highly 15, highly 28–October 28–31, September 2, abundant; 14–November 2017: October abundant highly 15, highly abundant; 14– 2017: October 15, highly abundant 2, highly November 2017: May 25, abundant 2017: May highly abundant; 10–14, 2017: September highly abundant highly 24–25, highly abundant; 2017: September 24–25, highly abundant 2–30, highly Abkhazia 2016: July 5, August 16–18, highly abun - 16–18, highly 5, August 2016: July 2016: July 5, August 16–18, highly abun - 16–18, highly 5, August 2016: July 2016: July 28–31, September 1–9, highly 1–9, highly 28–31, September 2016: July 2015: September 1–30, sporadic; 2016: July 2016: July 1–30, sporadic; 2015: September 2016: August 5–31, highly abundant 5–31, highly 2016: August 2016: July 28–31, September 24–October 24–October 28–31, September 2016: July 2016: October 1–10, highly abundant; 1–10, highly 2016: October – 2016: July 15–31, highly abundant 15–31, highly 2016: July 2017: July 22–August 12, abundant 22–August 2017: July 2016: July 15–31, highly abundant 15–31, highly 2016: July 2017: July 22–August 12, abundant 22–August 2017: July 2017: August 26–27, abundant 2017: August 2016: July 15–31, sporadic, August 5–31, August 15–31, sporadic, 2016: July 2016: August 1–8, sporadic September September 1–8, sporadic 2016: August abundant; 2017: August 10–13, sporadic abundant; 2017: August abundant; 2017: August 10–13, sporadic abundant; 2017: August September 6, highly abundant; 2017: 6, highly September 10, abundant 20–September August - 15–Octo 4, September 25–August July abundant; 2017: August ber 20, highly 10–November October 10–13, sporadic, 3, abundant highly abundant; 2–14, 2017: September highly abundant highly ber 5, highly abundant; 2017: September ber 5, highly abundant 2–30, highly Dates and estimated abundance, by region abundance, by Dates and estimated Russia 2016: June 25–July 3, August 4–8, highly 4–8, highly 3, August 2016: June 25–July 2016: June 28–July 3, August 8, highly 8, highly 3, August 2016: June 28–July 2016: July 25–August 8, August 31– 8, August 25–August 2016: July 2015: September 1–30, sporadic; 2016: 1–30, sporadic; 2015: September – 2017: October 10–November 3, sporadic 10–November 2017: October – 2016: August 5–16, highly abundant 5–16, highly 2016: August 2016: July 15–31, highly abundant 15–31, highly 2016: July – 2016: July 15–31, highly abundant 15–31, highly 2016: July – 2017: August 24–September 2, abundant 24–September 2017: August 2016: July 15–31, sporadic, August 5–31, August 15–31, sporadic, 2016: July - Septem from 1–8, sporadic 2016: August Halyomorpha halys of Halyomorpha Stages Egg masses Nymphs of I–II instars Nymphs Nymphs of IV–V instars Nymphs Adults Nymphs of I–V instars Nymphs Adults Adults Egg masses and nymphs of I–III instars Egg masses and nymphs Nymphs of III–V instars and adults Nymphs Nymphs of III–IV instars Nymphs Nymphs of III–V instars and adults Nymphs Nymphs of III–IV instars Nymphs Nymphs of II instars Nymphs Nymphs of III–V instars Nymphs Adults Parts of the plant Leaves Leaves, fruits Leaves, Leaves, fruits Leaves, Leaves, fruits Leaves, Fruits Fruits, leaves Shoots Leaves Fruits, leaves Fruits, leaves Fruits, leaves Fruits, leaves Leaves Fruits Fruits unshiu Tan. Blanco var. Citrus reticulata Citrus sinensis (L.) Osbeck Brugmansia sp. Capsicum sp. L. Solanum lycopersicum L. and its cultivars vinifera Vitis 1 Table (continued) family) plant (by Host Solanaceae Vitaceae

1 3 524 D. L. Musolin et al.

Fig. 2 Halyomorpha halys and examples of damage caused by the species to crops. a Newly hatched I instar nymphs of H. halys on a leaf of Satsuma man- darin Citrus reticulata Blanco var. unshiu Tan. (Rutaceae) in Sochi on August 4, 2016 (Photo: V.Ye. Protsenko). b One of the first images of H. halys taken in Serbia in 2015 (Photo: Z. Gavrilović, with permission). c Damaged fruit of Satsuma mandarin C. reticulata Blanco var. unshiu Tan. (Rutaceae), Gulripshi (Abkhazia), October 2016 (Photo: N.N. Karpun). d Damaged fruit of grapefruit C. paradisi Macfad., Gulrip- shi (Abkhazia), November 2016 (Photo: N.N. Karpun). e Adults of H. halys on fruits of V. vinifera, September, 2, 2017 (Photo: N.N. Karpun). f II instar nymphs of H. halys on a leaf of V. vinifera, September, 2, 2017 (Photo: N.N. Karpun)

2017, H. halys was abundant in different districts of Kras- Abkhazia nodar Kray (Region) in orchards, vegetable, and ornamen- tal crops. It was recently reported that 20 specimens of H. halys Our field observations of 2015–2017 suggest that the were collected in Pitsunda Town in October 2016 (Gapon species not only survived its first winters in the new area, 2016; Fig. 1). However, even before this record, our survey but also successfully passed the first stages of establish- of 2015–2016 revealed that in Abkhazia H. halys was dis- ment, actively reproduced, and started to build up the local tributed in all seven country districts, i.e., from the border population already causing noticeable damage. The field with Russia (43°39′N; 40°00′E) to the border with Georgia records from 2016 to 2017 in Sochi suggest that H. halys (42°62′N; 41°73′E). The pentatomid was recorded feeding can produce two or even three generations per year in the on 22 species and cultivars from 12 plant families (Table 1). region. Additional regular phenological and detailed eco- In western Abkhazia, H. halys reached the level at which physiological studies, focusing on the timing of diapause it can be considered a highly abundant and very common induction in the recently colonized area are needed to pest in 2015, whereas in the eastern Abkhazia—that hap- clarify these important characteristics. pened only in the late 2016. Based on the early field records

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(Table 1), phenology of H. halys in Abkhazia is similar to mostly on Platanus sp. (Platanaceae), and in the buildings that in Sochi. and other constructions while adults of H. halys were look- The damage caused by H. halys to agriculture seems to ing for overwintering microhabitats. These records were be very strong in Abkhazia: in 2016, in Sukhum and Gul- later checked and confirmed by professional heteropterists ripshi regions (Fig. 1), the yield of peach, mandarin orange, (Šeat 2015; Fig. 2b). persimmon, and other major agricultural crops fell down by In addition to these findings, in October 2015, adults of 13.2–87.4% if compared to the long-term means for these H. halys were also recorded by naturalists in two locations crops (Table 2). Even though direct controlled experiments in Belgrade: in the Botanical Garden Jevremovac located were not conducted, we could compare the yield obtained in the city core and in an urban zone in the western part in 2016 with mean yield obtained in previous years and of the city (Šeat 2015). These seemingly independent find- estimate the impact of H. halys. Monitoring of arthropod ings have one common feature—the railway line connecting pests and fungal pathogens suggested that a considerable Bucharest (Romania, where H. halys was reported in 2015; part of the damage (11.7–85.2%) is attributed to the active Macavei et al. 2015) and Belgrade Central Station passes feeding of H. halys. In Sukhum region, a few cases were Vršac on its way. We believe that this railway line is the most also recorded when crowns of Citrus sinensis (L.) Osbeck likely pathway of H. halys introduction to Serbia. In spite of (Rutaceae) fully or partly dried out because of the feeding the special efforts to find H. halys closer to the border with of H. halys: the pentatomid had population density of up to Hungary (where the species had been recorded in 2013 in 15 adults per 10 cm of branches with a branch diameter at Budapest and its surrounding; Vétek et al. 2014; Fig. 1), it its base of 3 cm. has not been found in the north of Serbia. Taking into consideration that H. halys was recorded not Serbia just in one but in two municipalities at the same time in 2015 and its potential threat for local agriculture, in 2016, In early October to early December 2015, 24 adults and the species was listed as a species under special supervision four nymphs of H. halys were recorded in north-east of Ser- in Serbia. bia, namely in Vršac (45°13′N; 21°30′E; 18 adults and one After the first records in the late autumn of 2015, indi- nymph; Fig. 1), Belgrade (44°49′N; 20°28′E; five adults and vidual, overwintered adults of H. halys were sporadically three nymphs), and Vatin (45°14′N; 21°15′E; one adult). recorded in the same locations in March and May 2016. These specimens were recorded by amateur naturalists The first nymphs were observed at the beginning of July

Table 2 Estimated effect of Halyomorpha halys on yield of selected crops in Abkhazia in 2016 (based on mean records from 15 enterprises located in Sukhum and Gulripshi regions in 2016 in comparison with mean data for 1996–2015) Crop Estimated abundance Long-term yield Mean yield in 2016 Estimated yield loss in 2016b (%) of H. halys in 2016­ a for 1996–2015 (mean ± SEM) (t/ha) (mean ± SEM) (t/ha) Total (100 − mean Caused Caused by other yield in 2016/long- by H. arthropod pests and term yield) halys fungal ­pathogensc

Persimmon Highly abundant 26.8 ± 2.2 6.1 ± 0.3 77.2 72.0 5.2 Peach Highly abundant 18.2 ± 3.6 2.3 ± 0.1 87.4 80.1 7.3 Grape Abundant 9.8 ± 1.2 7.0 ± 0.2 28.6 23.7 4.9 Mandarin orange Highly abundant 21.1 ± 2.5 14.1 ± 0.4 33.2 28.2 5.0 Apple Abundant 27.2 ± 3.4 19.3 ± 0.3 29.0 22.5 6.5 Pear Abundant 22.3 ± 2.1 11.8 ± 0.2 47.1 42.9 4.2 Fig Abundant 30.1 ± 3.2 3.8 ± 0.1 87.4 85.2 2.2 Plum Sporadic 27.7 ± 1.1 18.1 ± 0.2 34.7 29.9 4.8 Corn Abundant 9.1 ± 0.8 7.9 ± 0.1 13.2 11.7 1.5 a Halyomorpha halys was recorded for the first time in Abkhazia in 2015 and damage was limited in that year; noticeable abundance and damage were recorded in 2016 b The structure of yield loss in 2016 was estimated based on monitoring of development of fruits/seeds, field observations of arthropod pests, and symptoms caused by fungal pathogens. During the early part of the season, the expected yield was close to the multi-year means (± 5%). In 2016, weather and agro-chemical conditions were close to the long-term means c Other arthropod pests include tortricid moths (Cydia pomonella L., Grapholitha funebrana Тr., Grapholita molesta Busck), leaf mite Phyllo- coptruta oleivorus Ashm, and others; fungal pathogens are Taphrina deformans (Berk.) Tul., Venturia inaequalis (Cooke) G. Winter, Venturia pyrina Aderh., Botrytis cinerea Pers., Monilinia fructigena Honey and others

1 3 526 D. L. Musolin et al. in Belgrade and during August in Vršac, mostly on orna- In Russia, the situation seems to be different. Russia mental plants in urban zones. Hibiscus syriacus L. (Malva- is comparatively far from the center of the secondary ceae) seemed to be the most preferred plant for nymphs and range of H. halys in Europe (Haye et al. 2015; Fig. 1) and adults in early September 2016 in Vršac. Nymphs were also the natural penetration of H. halys into Russia from sur- recorded on soybean (45°17′N; 21°22′E) and pesticide-free rounding countries should be ruled out, as this species tomato S. lycopersicum L. (Solanaceae), but H. halys was has never been found in Moldova, Ukraine, and Turkey not found on apple and pear trees (44°98′N; 21°22′E). In (Gapon 2016). At the same time, Sochi hosted the 2014 soybean Glycine max (L.) Merr. (Fabaceae) fields, nymphs Winter Olympics. To prepare the city for the Games not were mostly concentrated on the outer edges, where they only sports infrastructure was built, but also many woody were often feeding on stems and leaves, together with plants were imported in 2011–2013 for massive urban numerous nymphs of the Southern green stink bug Nezara landscaping. Thousands of woody plants were bought viridula (L.) (Heteroptera: Pentatomidae), another inva- mostly from Northern Italy (but also from Spain and Bal- sive pentatomid established in Serbia in 2011 (Protić 2011; kan countries) because the local stock was insufficient for Kereši et al. 2012). Nymphs of both species were sometimes the large-scale landscaping and Italy and Sochi are simi- feeding on the same plants showing no apparent competitive lar in terms of climate. H. halys established in Greece in relationships. 2011 (Milonas and Partsinevelos 2014) and in Northern In late August to early September 2016, detailed field Italy in 2012 (Maistrello et al. 2013, 2016). It might be inspections revealed the presence of H. halys nymphs in soy- speculated that H. halys could arrive with cargoes or other bean fields in two new locations, namely town of Plandište goods to some Black Sea ports or directly to Sochi with (45°23′N; 21°11′E, municipality of Vršac; Fig. 1) and town the luggage of the Olympic teams or tourists and/or other of Jasenovo (44°94′N; 21°30′E, municipality of Bela Crkva). imported goods during the Games. However, we believe Although no egg masses were recorded, findings of adults that probability is much higher that H. halys arrived from and nymphs at the same time, a year after the first record in Northern Italy and Greece with woody plants for urban the area, served as proof of the initial stage of establishment landscaping, as such plants were imported to Sochi region of H. halys in Serbia. First findings in urban areas in 2015 in large numbers in 2012–2013 and there is evidence that along with the later findings on ornamental plants (Hibiscus the species was seen in Sochi as early as in 2013 (Gapon sp.), soybean, and tomato in 2016 strongly suggest that H. 2016). Apparently, the border phytosanitary control at the halys has found suitable conditions for its growth, reproduc- import checking point in that part of Russia was insuffi- tion, and overwintering in the area. Municipalities in which cient at that time. In 2014–2016, many new woody plant the species was repeatedly recorded are located close to the pests were registered in Sochi region (Karpun et al. 2015, railway line Bucharest–Belgrade suggesting that H. halys 2016, 2017; Shiryeva 2015). Currently, the highest popu- arrived to Serbia by railway traveling on railway cars or in lation density of H. halys is recorded in the Adler district commodities. of Sochi (the Imereti Lowlands), the former center of the major construction work and landscaping of the Olympics. Range expansion and establishment of H. halys An on-going population genetics analysis can shed light in Europe on the origin of H. halys in the Sochi area. Halyomorpha halys could easily arrive in Abkhazia from The collected data demonstrate that H. halys was recorded Sochi, because these are two neighboring regions (Fig. 1). for the first time in Russia in 2013 or 2014 and in Serbia Moreover, the species could start its journey from Sochi to and Abkhazia in 2015; that it has survived its first winters Abkhazia even before it established in Sochi (i.e., as early as in a new regions, established in these countries, has built up in 2013) because the temporary woody plant nurseries were local populations, to an economically important level, and located in Sochi within a distance of a few kilometers from has started to secondarily disperse. How did H. halys come the border with Abkhazia and accidentally imported adults to Russia and Serbia? of H. halys could have flown from the temporary woody As mentioned above, two intercepted findings ofH. halys plant nurseries not only further to Russia (to Sochi and, for in Serbia, closely related to the railway line Bucharest–Bel- example, to Krasnodar), but also directly to Abkhazia. grade (entering Serbia in Vatin; Fig. 1), suggest introduction From Abkhazia, H. halys could then naturally disperse assisted by the railway transport commodities. Although it further to Georgia (Fig. 1). Indeed, the species was recorded is possible to hypothesize that this strong flier could fly in, in Georgia for the first time in 2015 (Gapon 2016). This pos- this assumption is rejected due to the absence of records of sible scenario is further supported by the observation that H. halys in the regions between these two locations (Macavei H. halys is more numerous and already causing damage in et al. 2015; Ciceoi et al. 2016) as well as in and around the the western Georgia, but not in eastern part of the country closest town Timisoara. (Karpun 2016, unpublished data).

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Halyomorpha halys will definitely continue to spread in H. halys is also univoltine (Haye et al. 2014). Adults of the Europe. Bioclimatic modeling suggests that the species can summer generation emerge in mid-August when natural day (and most likely will) establish in the Mediterranean coun- length can be as short as 14 h 15 min. The critical photoper- tries of Europe, the middle East, north of Algeria, northern iod of the photoperiodic response of winter adult diapause Cameroon, and western Africa (Zhu et al. 2012; Haye et al. induction of the local population is not yet known, but it is 2015). The species is believed to be able to go as far north likely close to the one estimated for the Nagano population in Europe as latitudes 50°N (Zhu et al. 2012) or even 60°N (approximately 15 h). Short-day conditions apparently pre- (Jimerikin and Guliy 2014). Potential damage to agricul- vent reproduction of these adults and promote induction of ture and forestry might be huge. Multi- or bivoltine seasonal the winter adult diapause already in the first generation. To development can be expected in subtropical and warm tem- ensure successful realization of two complete generations, perate regions such as Sochi, whereas univoltine seasonal adults of the first generation should emerge no later than cycle is expected to be realized further north (Saulich and in late June when the day is longer than 15 h; this does not Musolin 2017). happen under natural conditions in Switzerland. The seasonal cycle of H. halys includes photoperiodically The available body of information on distribution and induced facultative winter adult diapause (Yanagi and Hagi- seasonal development of H. halys in its invasive range is hara 1980; Saulich and Musolin 2017). Timing of diapause so far limited and does not allow to confidently predict the induction is controlled by a critical photoperiod. In most further secondary range and voltinism of H. halys. CLIMEX insect species, this trait is flexible and often only a few gen- and other techniques suggest that H. halys will be able to erations or years are required for an invader to adapt to local complete up to three generations in southern Greece (e.g., climatic conditions (Saulich and Musolin 2017). Crete or East Peloponnese; Zhu et al. 2012). Such models In spite of the attention focused on this economically should be applied with caution as not only temperature, but important pentatomid, data on its seasonal development also photoperiodic response of facultative winter diapause are limited. In different parts of its native range in Asia, induction strongly affect voltinism, and so far nothing is the species produces usually 1–2 generations per year (Lee known about the photoperiodic response of European popu- et al. 2013), although there is an unreliable and not fur- lations of H. halys. ther confirmed report of 4–6 annual generations in southern Having only fragmentary data, it is difficult to predict China (23.0°N; Hoffman 1931). The detailed analysis of the size of the invasive range in Europe and elsewhere and the phenology of H. halys was based on experimental data estimate potential economic damage. Predictions of this type obtained both under laboratory and quasinatural conditions are difficult and not very reliable as there are too many fac- in Nagano (Japan, 36.5°N) and demonstrated that the facul- tors—sometimes not obvious—which are involved in range tative winter adult diapause in that population is controlled expansion and control of seasonal development and, thus, by a long-day type photoperiodic response with a critical day must be taken into consideration. Recent history of assisted length of about 15 h at 25 °С. In accordance with this criti- introduction programs of two predatory pentatomids, namely cal threshold, adults emerging after July 15–25 do not start Podisus maculiventris and Perillus bioculatus, to Europe reproduction, but directly enter winter diapause. Thus, even might serve as examples (Saulich and Musolin 2017). Thus, at the latitude of Nagano this species in univoltine (Yanagi further monitoring as well as detailed phenological studies and Hagihara 1980; Saulich and Musolin 2017). However, are highly desirable. at the western coast of Japan (Watanabe et al. 1978) and in the south of China (Lee et al. 2013), populations of H. halys Acknowledgements The present study was partially supported by the Russian Foundation for Basic Research (Grant No. 17-04-01486 for are bivoltine. In the case of a bivoltine seasonal cycle, adults DLM) and the EU COST Action FP1401 Global Warning (A global of the first generation emerge in late June or early July when network of nurseries as early warning system against alien tree pests; local day-length conditions do not limit the possibility of a http://www.cost.eu/COST_Actions/fps/FP1401). Survey conducted second generation because day length during the period of during 2016 in Serbia was supported by the Serbian Ministry of Agri- culture and Environmental Protection, Plant Protection Directorate. adult emergence is longer than the critical day length. As We sincerely thank Dr. D. Gillespie (AAFC Agassiz, retired), Dr. K. a result, adults of this generation are reproductive. In con- Tsytsulina and two anonymous reviewers for critical reading of the MS trast, adults of the second generation emerge in late August and helpful correction. or early September, do not reproduce, and enter facultative winter adult diapause because the natural day length at that time is already short (Saulich and Musolin 2017). The seasonal cycle of H. halys has been studied within References its invasive range too. In Pennsylvania and New Jersey (the USA), only one generation per year is recorded (Nielsen Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische fauna neu nachgewiesene wanzenart (Insecta: and Hamilton 2009; Leskey et al. 2012). In Switzerland,

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