Article Emerald Ash Borer Approaches the Borders of the European Union and Kazakhstan and Is Confirmed to Infest European Ash Mark G. Volkovitsh 1,*, Andrzej O. Bie ´nkowski 2 and Marina J. Orlova-Bienkowskaja 2 1 Zoological Institute, Russian Academy of Sciences, 199034 St. Petersburg, Russia 2 A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071 Moscow, Russia; [email protected] (A.O.B.); [email protected] (M.J.O.-B.) * Correspondence: [email protected] Abstract: Emerald ash borer (EAB), Agrilus planipennis, native to East Asia, is an invasive pest of ash in North America and European Russia. This quarantine species is a threat to ash trees all over Europe. Survey in ten provinces of European Russia in 2019–2020 showed that EAB had spread faster and farther than was previously thought. The new infested sites were first detected in St. Petersburg (110–120 km from the EU border: Estonia, Finland) and Astrakhan Province (50 km from the Kazakhstan border). The current range of EAB in Europe includes Luhansk Province of Ukraine and 18 provinces of Russia: Astrakhan, Belgorod, Bryansk, Kaluga, Kursk, Lipetsk, Moscow, Orel, Ryazan, Smolensk, St. Petersburg, Tambov, Tula, Tver, Vladimir, Volgograd, Voronezh, and Yaroslavl. Within these, only seven quarantine phytosanitary zones in five provinces are declared by the National Plant Protection Organization of Russia. EAB was not found in the regions along the Middle Volga: Mari El, Chuvash and Tatarstan republics, Nizhny Novgorod, Samara and Saratov Citation: Volkovitsh, M.G.; provinces. The infested sites in St. Petersburg and in the Lower Volga basin are range enclaves Bie´nkowski,A.O.; separated from the core invasion range by 470 and 370 km, correspondingly. It is possible that new Orlova-Bienkowskaja, M.J. Emerald Ash Borer Approaches the Borders of enclaves can appear in the cities of Eastern Europe and Kazakhstan far from the current known range. the European Union and Kazakhstan All previously known infestations in European Russia were in green ash (Fraxinus pennsylvanica), and Is Confirmed to Infest European which was introduced from North America, and individual trees of European ash (F. excelsior). A first Ash. Forests 2021, 12, 691. https:// confirmed case of mass decline of several thousand of EAB-infested European ash trees in Moscow doi.org/10.3390/f12060691 province is provided. Therefore, there is no more doubt that under certain conditions EAB can seriously damage native ash trees in European forests. Academic Editor: Young-Seuk Park Keywords: emerald ash borer; EAB; northwest Russia; St. Petersburg; southeast Russia; Fraxinus Received: 20 April 2021 excelsior; European ash Accepted: 24 May 2021 Published: 27 May 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- Emerald ash borer (EAB), Agrilus planipennis Fairmaire, 1888 is one of the most dev- iations. astating pests of ash (Fraxinus sp.) trees in the world [1–4]. Over the past few decades, from a little-known species whose native range was limited to East Asia [5], it has become one of the most dangerous invasive pests of forests and urban ash plantings in North America and European Russia. It was first detected outside its native range in the USA and Canada in 2002 [6,7], and in European Russia (Moscow City) in 2003 [8,9]. By late Copyright: © 2021 by the authors. 2020, EAB was reported in five provinces of Canada, 35 states of the USA [10], 16 provinces Licensee MDPI, Basel, Switzerland. This article is an open access article of Central European Russia and one province of Ukraine [11], having killed millions of distributed under the terms and ash trees [1,3,9,11–14]. This pest is regarded as a serious threat to the ash trees all over conditions of the Creative Commons Europe [14–22]. In 2018, the probability of its spread to Belarus, Ukraine, Estonia, Latvia Attribution (CC BY) license (https:// and Lithuania by 2022 was estimated as 15–40% [23]. However, recent discoveries have creativecommons.org/licenses/by/ shown that EAB spreads faster and farther than previously thought, since it was detected 4.0/). in Eastern Ukraine (Luhansk Province) in 2019 [24]. Forests 2021, 12, 691. https://doi.org/10.3390/f12060691 https://www.mdpi.com/journal/forests Forests 2021, 12, 691 2 of 13 Until recently, it was considered that EAB was spreading to the northwest from Moscow as far as the city of Tver [25] and its further natural expansion was regarded as extremely doubtful due to extensive ash-free areas [9,26–28]. No one expected that EAB had already established itself in St. Petersburg, far from the known northwest borders of its invasive range in Tver Province. However, the first information that EAB could be responsible for ash decline in the Petrodvorets District of St. Petersburg was posted by tree protection volunteers on the internet in late summer 2020 [29]. Therefore, it was necessary to verify this information by surveying ash trees in the mentioned district and assessing the potential risks from the sudden expansion of EAB to the northwest by almost 500 km, approaching the EU borders. Survey results were briefly reported at the conference “Kataev Memorial Readings XI” [30,31]. In this article, the results are described in detail. The distribution of EAB in the east of European Russia is still poorly known [11], so further survey is required to determine the eastern border of the pest’s invasive range. EAB can infest all ash species native to Europe [32]. The only native species in the greatest part of European Russia is European ash (Fraxinus excelsior L.); the second native species, Fraxinus angustifolia Vahl, occurs only in the Caucasus, far from the current EAB range. European ash is rare in the center and north of European Russia. Therefore, most infestations have referred to the green ash (Fraxinus pennsylvanica Marsh), which was intro- duced from North America and widely planted in the cities and along the roadsides [1,9,11]. The information about infestation of F. excelsior by EAB was scarce and referred only to urban plantings and artificial shelterbelts, where F. excelsior was planted together with F. pennsylvanica [1,14]. There were no data about the impact of EAB on European ash in natural forests. Therefore, there was a great deal of uncertainty regarding the potential impact of EAB on native ash in European forests [1,11]. The internet publication of the employee of the Federal Forestry Agency “Russian Center for Forest Protection” (“Roslesozaschita”) reported the severe damage by EAB to European ash in Kokinskij Forest nearby Ozherelie railway station, Kashira District of Moscow Province in 2014 [33]. However, this information was not officially confirmed by the National Plant Protection Organization of Russia (“Rosselkhoznadzor”) and no quarantine phytosanitary zone was declared there [34]. Therefore, the survey of this forest stand was needed to assess if European ash trees were infested by EAB and how severe was the damage if any. The objectives of the present study are as follows: 1. To assess if EAB had really spread to the northeast of European Russia as far as the city of St. Petersburg and if there were other infested sites in the city and adjacent districts of Leningrad Province. 2. To find out if the eastern border of the invasive range reached the Middle Volga Basin. 3. To check out if EAB moved further south of the previously known southern border of the range in the Lower Volga Basin. 4. To determine if EAB could severely damage forest stands of European ash. 2. Materials and Methods In 2019–2020, ash trees in ten provinces of European Russia extending from St. Peters- burg City and Leningrad Province in the northwest to Samara Province in the east and Astrakhan Province in the southeast were surveyed (Figure1). The first discovery of the EAB-infested ash trees in Martyshkino settlement (part of Lomonosov town, Petrodvorets District of St. Petersburg City) (Figure1) was made in late August, 2020 [35], later exit holes in the ash bark, dead EAB adults and other infestation signs were found in this locality [36]. This locality was repeatedly visited by the first author during September–November 2020 and more proofs of EAB infestation including larvae were found there. Some more EAB infested green ash trees (F. pennsylvanica) with exit holes were found along Gostilitskoe Hwy (about 4 km southward of the first locality). In addition, the roadside plantings of F. pennsylvanica and F. excelsior in 8 localities along the route Ropsha–Kipen–Ropsha–Orzhitsy–Vilpovitsy–Gostilitsy in Leningrad Province, and Forests 2021, 12, 691 3 of 13 Lomonosov–Staryi Peterhof in Petrodvorets District of St. Petersburg, as well as stands of native F. excelsior along the Baltic–Ladoga glint near Vilpovitsy were surveyed (Table1, localities 4–11). One locality with declined green ash trees along Pulkovskoe Hwy was Forests 2021, 12, x FOR PEER REVIEWalso inspected (Table1, locality 12). Meanwhile, one more EAB-infested locality in Staryi3 of 14 Peterhof (about 4 km eastward of first locality) was reported [35,37]. Figure 1. Surveyed sites ofof ashash treestrees inin EuropeanEuropean RussiaRussia inin2019–2020. 2019–2020.Red Redcircles—EAB circles—EAB is is detected, de- greentected, circles—EAB green circles—EAB is notdetected. is not detected. 1—St. 1—St Petersburg. Petersburg City, 2—KokinskijCity, 2—Kokinskij Forest Forest nearby nearby Ozherelie Ozherelie railway station (Moscow Province), 3—Nizhny Novgorod City, 4—Kozmodemyansk railway station (Moscow Province), 3—Nizhny Novgorod City, 4—Kozmodemyansk Town (Mari El Town (Mari El Republic), 5—Cheboksary City (Chuvash Republic), 6—Kazan City (Tatarstan Re- Republic), 5—Cheboksary City (Chuvash Republic), 6—Kazan City (Tatarstan Republic), 7—Samara public), 7—Samara City, 8—Saratov City, 9—Usovka Island (Saratov Province), 10—Volgograd City, 8—Saratov11—Nikolskoe City, Village 9—Usovka (Astrakhan Island Province (Saratov).