Forestry Studies | Metsanduslikud Uurimused, Vol. 73, Pages 43–51

Research paper

Decline of excelsior L. in parks of Saint Petersburg: Who is to blame – fraxineus or Diplodia spp.?

Dmitrii A. Shabunin1, Andrey V. Selikhovkin2,3*, Elena Yu. Varentsova2 and Dmitry L. Musolin2

Shabunin, D.A., Selikhovkin, A.V., Varentsova, E.Yu., Musolin, D.L. 2020. Decline of Fraxi- nus excelsior L. in parks of Saint Petersburg: Who is to blame – Hymenoscyphus fraxineus or Diplodia spp.? – Forestry Studies | Metsanduslikud Uurimused 73, 43–51, ISSN 1406-9954. Journal homepage: http://mi.emu.ee/forestry.studies

Abstract. The weakening and decline of European ash L. and other ash spe- cies have been recorded at different locations in the suburbs of Saint Petersburg, Russia. Dur- ing the summer of 2019 and spring of 2020, samples from leaves, petioles, and shoots were collected from the weakened and declining ash trees in three parks in Pushkin and Gatchina and maintained in humid chambers to induce the fructification of fungi. In total, 30 taxa of micromycetes belonging to 23 genera were identified using methods of light microscopy. Hymenoscyphus fraxineus, a putative agent of ash dieback, was not recorded in the samples collected in the crowns of trees, but only on the petioles of the fallen leaves in spring. Out of all the micromycetes recorded, only coelomycetes from the genus Diplodia Fr. (in particular, D. mutila) can damage the branches of ash trees and, thus, be considered pathogenic. It is likely that H. fraxineus opens “the entry of infection” and Diplodia spp. cause the major weak- ening and decline of branches. The data obtained can significantly change our understanding of the causes of ash dieback and possible methods of ash stand preservation. The reason for the low pathogenicity and activity of H. fraxineus, as well as the possible role of ascomycetes Diplodia spp. in the dieback of ash stands requires further research.

Key words: ash dieback, European ash, , tree health, invasive tree fungal patho- gen, urban greening.

Authors’ addresses: 1Department of Forest Selection, Saint Petersburg Forestry Research In- stitute, Institutskiy pr., 21, 194021, Saint Petersburg, Russian Federation; 2Department of For- est Protection, Wood Science and Game Management, Saint Petersburg State Forest Technical University, Institutskiy per., 5, 194021, Saint Petersburg, Russian Federation; 3Department of Biogeography and Environmental Protection, Saint Petersburg State University, Universitets- kaya nab., 7–9, 199034, Saint Petersburg, Russian Federation; *e-mail: [email protected]

Introduction tree stands are usually formed by species of woody plants that are not characteristic Urban and suburban green spaces fulfill a of the surrounding local forest ecosystems. very important function of creating a com- This is conditioned by the specific features fortable living environment. In large Eu- of the urban environment; predominant- ropean cities and urban agglomerations, ly, the aesthetic requirements and the im-

DOI: 10.2478/fsmu-2020-0013

© 2020 by the authors. Licensee Estonian University of Life Sciences, Tartu, . This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

43 D.A. Shabunin et al. pact of the negative anthropogenic factors, and urban plantings in Saint Petersburg such as air and soil pollution (Nowak et al., and its suburbs, deterioration of the health 2006; Alekseyev et al., 2019). For example, conditions of ash trees was noted: individ- city parks and urban plantings of Saint ual shoots were dying off and individual Petersburg, Russia, are mostly planted by trees or groups of trees died in Aleksan- the small-leaved lime Tilia cordata Mill., drovsky and Babolovsky Parks of Pushkin Norway maple Acer platanoides L., silver district of Saint Petersburg, as well as in birch Betula pendula Roth, Berlin poplar Gatchina Palace Park in Leningrad Prov- Populus × berolinensis Dippel, green ash ince (Figure 1). The dying trees often had Marsh, English oak symptoms characteristic of ash dieback in- Quercus robur L., and European white elm duced by H. fraxineus (Vasaitis & Enderle, Ulmus laevis Pall., whereas the forest eco- 2017). Thus, it was suggested that invasive systems of Saint Petersburg suburbs and H. fraxineus might be a pathogenic agent the surrounding Leningrad Province are causing death of ash trees in these parks. dominated by Scots pine Pinus sylvestris L., The aim of the study was to evaluate a Norway spruce Picea abies (L.) H. Karst., a possible role of H. fraxineus as well as other few species of birch Betula spp., European pathogenic fungi in the death of ash trees aspen Populus tremula L., and grey alder in the parks of Saint Petersburg and its Alnus incana (L.) Moench (Moschenikova, suburbs. 2011). The specific composition of woody vegetation and a strong influence of the factors compromising the resistance of Material and Methods woody plantings make these plantings highly susceptible to invasive pathogens In the second half of July and in August of and pests in the urban environment (Selik- 2018 and 2019, and in May 2020 surveys hovkin et al., 2018, 2020). were conducted in Aleksandrovsky Park Saint Petersburg is a big cultural center (59°43’30” N, 30°22’20” E) and Babolovsky that attracts millions of tourists every year Parks (59°43’03” N, 30°22’11” E) of Push- and also serves as a transportation hub. As kin district of Saint Petersburg as well as a result, the process of invasion of patho- in Gatchina Palace Park (59°33’51” N, gens and arthropod pests of woody plants 30°06’49” E) in Leningrad Province (Fig- is very intensive here (Shabunin et al., ure 1). We evaluated the health conditions 2012; Musolin et al., 2017; Selikhovkin et al., of European ash F. excelsior trees (aged 2018, 2020). The ascomycete Hymenoscy- 30 years and older; breast height diameter phus fraxineus (T. Kowalski) Baral, Queloz of 20 cm and more). In Aleksandrovsky & Hosoya (anamorph of Chalara fraxinea) Park, 37 ash trees that looked the most causing ash dieback is one of the phyto- weakened were checked and evaluated, in pathogenic invaders that recently reached Babolovsky Park – 35 trees, and in Palace the city. During the last 20 years, this fun- Park in Gatchina – 88 ash trees (Figure 2). gus has rapidly spread over the most of In Aleksandrovsky and Babolovsky Parks, Europe causing fast and almost complete ash dieback tended to have a cluster char- death of ash stands everywhere it was acter when diseased trees formed a group recorded (Enderle et al., 2017; Vasaitis & of near-growing ash trees (Figure 2). Enderle, 2017). This species was record- To evaluate the health condition of ed in Saint Petersburg as well, in particu- ash trees, we used standardized catego- lar, at Dudergof Heights in the drying-off ries adopted in the Russian Federation for stands of European ash Fraxinus excelsior L. surveys using six catego- (Shabunin et al., 2012). ries: (I) healthy trees, (II) weakened trees, During recent routine surveys of parks (III) heavily weakened trees, (IV) drying-out

44 Decline of Fraxinus excelsior L. in parks of Saint Petersburg: Who is to blame – Hymenoscyphus fraxineus or Diplodia spp.?

Figure 1. Location of the parks surveyed in this study.

Figure 2. Group weakening and decline of European ash Fraxinus excelsior trees in Babolovsky Park (photo by Bui Dinh Duc, with permission).

45 D.A. Shabunin et al. trees, (V) trees that had died during the from crowns were collected from the same current year, and (VI) trees that had died trees on all three dates. In total, 30 sam- during the previous year (categories ples were collected from 20 trees (namely, V and VI were combined in our surveys; 11 samples from 9 trees in Aleksandrovsky Mozolevskaya et al., 1984). Park, 5 samples from 3 trees in Babolovsky In 2019, a focused study was conducted Park, and 14 samples from 8 trees in Palace in the same locations with a purpose to de- Park). Samples were collected mostly from tect the presence and identify phytopath- heavily weakened trees (health category ogenic fungi causing deterioration of the III: 23 samples from 17 trees; Figure 3), ash trees’ health status. Three times during weakened trees (health category II: 5 sam- the summer season (on June 26, July 25, ples from 2 trees) followed by drying-out and August 27), we collected dried and trees (health category IV: 2 samples from damaged shoots with leaves from the low- 1 tree). er part of the crown of adult ash trees using The sampled leaves, petioles, and a 5.5 m long rod secateurs. The last year’s shoots were studied in a laboratory using fallen leaf petioles were collected on July stereomicroscope MBS-9. Then, the sam- 25, 2019. The next year, the collection of ples were incubated in a humid chamber the petioles was repeated on May 27, 2020. under room conditions with regular mon- In most cases, samples of leaves and shoots itoring of the emerging fruit bodies of mi- cromycetes. After 3–4 weeks of incubation, in most cases, all samples were covered with sterile mycelium and the observa- tions ceased. The identification of fungal species was carried out during the monitoring of the appearance of micromycetes fruiting in the humid chamber using morphological char- acteristics under the upright microscope Motic BA400. The appearance of the puta- tive pathogen H. fraxineus was monitored by observing the development of fungi in the humid chamber, as it was previously revealed that in the humid chamber fruit- ing of the imperfect stage of H. fraxineus develops quite quickly (Shabunin et al., 2012; Musolin et al., 2017).

Results

In all three parks (Aleksandrovsky, Bab- olovsky, and Palace Park), the group Figure 3. Typical appearance of European ash weakening and death of European ash Fraxinus excelsior of the health cat- trees having the symptoms characteristic egory III (heavily weakened trees) of ash dieback caused by H. fraxineus on from which samples were collected the crowns’ periphery were observed. All for the identification of pathogenic the surveyed ash trees had symptoms of micromycetes (Aleksandrovsky Park, Pushkin; photo by Andrey V. Selik- weakening, including the drying-out of hovkin). peripheral shoots, individual branches,

46 Decline of Fraxinus excelsior L. in parks of Saint Petersburg: Who is to blame – Hymenoscyphus fraxineus or Diplodia spp.?

Table 1. The health state of Fraxinus excelsior trees in the parks of Pushkin and Gatchina according to the surveys of 2018–2019.

Health state categories of trees Score Number of trees in each category for each park (%) Aleksandrovsky Park Babolovsky Park Palace Park I (healthy trees) 1 0 (0.0) 0 (0.0) 0 (0.0) II (weakened trees) 2 5 (13.5) 3 (8.6) 16 (18.2) III (heavily weakened trees) 3 20 (54.1) 12 (34.3) 54 (61.4) IV (drying-out trees) 4 10 (27.0) 15 (42.8) 15 (17.0) V (trees that had died during the current year) and VI (trees that 5 and 6 2 (5.4) 5 (14.3) 3 (3.4) had died during the previous year) combined Total 37 (100) 35 (100) 88 (100) Weighted score of the tree health 3.25 3.70 3.07 category and, in some cases, significant sections of and had been collected on May 27, 2020. the crowns. Dead trees were recorded in In contrast, fungi of the genus Diplodia all parks (Table 1). On average, the health were found in all three parks and during state score of ash stands was between all three months in 2019, although not at heavily weakened trees (category III) and each sampling collection session (Table 2). drying-out trees (IV), with the situation in Based on morphological characteristics, Babolovsky Park being the worst (Table 1). the samples collected in the beginning and Monitoring of the incubation of the in the middle of summer were identified as collected samples in the humid chamber Diplodia mutila (Fr.) Mont. (Figure 4). In the allowed to identify 30 taxa of micromy- samples collected in August 2019, conidia cetes belonging to 24 genera (Table 2). had a slightly larger size and somewhat We recorded 19 taxa of micromycetes be- different pigmentation. These specimens longing to 14 genera from the leaf tissues, were identified only up to the genus level 13 species (10 genera) from petioles, and (Diplodia sp.). All other fungi detected on 9 taxa (8 genera) from shoots (Table 2). All the collected samples do not induce ob- the registered fungal species are typical for served crown damage (Table 2). the ash mycobiota. The coelomycetes of the genus Diplodia were found throughout the entire observation period and were the Discussion most prevalent species. The ascomycete H. fraxineus, a putative The conducted survey demonstrated that agent of ash dieback, was not found in the symptoms of the weakening and dieback collected samples from the crowns of F. ex- of ash that are usually associated with celsior. The was not also found on H. fraxineus were found in many ash trees petioles of the fallen leaves collected on and in all three parks. In fact, there were July 25, 2019. Only in the next spring, typ- absolutely no healthy ash trees among ical dark brown pseudosclerotial tissues surveyed trees, and the average tree were observed. During the subsequent health score ranged from 3.07 (heavily incubation in a humid chamber, fruiting weakened trees) to 3.7 (almost drying-out bodies of the fungus appeared on the tis- trees). However, in our samples from tree sue samples that had overwintered on soil crowns, H. fraxineus was not found in any

47 D.A. Shabunin et al.

Table 2. Micromycetes from the leaves, petioles, and shoots of Fraxinus excelsior cultivated in a humidified incubator.

Date of Location of sampling and identified micromycetes sample collection Aleksandrovsky Park Babolovsky Park Palace Park June 26, *Codinaea sp. *Phomopsis sp. *Coniothyrium sp. 2019 *Stachybotrys sp. ***Diplodia mutila (Fr.) Mont. ***Diplodia mutila (Fr.) Mont. July 25, *Cladosporium herbarum (on *Cladosporium herbarum (on *Cladosporium herbarum (on 2019 galls of Dasineura fraxinea) galls of Dasineura fraxinea) galls of Dasineura fraxinea) *Phyllactinia fraxini (DC.) *Coniothyrium sp. Fuss *Trichothecium roseum (Pers.) Link. **Marasmius sp. **Phomopsis scobina (Cooke) Höhn. ***Diplodia mutila (Fr.) Mont. ***Hypoxylon fraxinophilum ***Coniothyrium sp. Pouzar. ***Diplodia mutila (Fr.) Mont. ***Trichothecium roseum (Pers.) Link. August *Alternaria sp. *Phyllactinia guttata *Alternaria sp. 27, 2019 *Botrytis sp. (B. cinerea?) *Cladosporium spp. *Cladosporium spp. *Gliomastix sp. *Gonatobotrys flava Bonord. *Periconia sp. *Hansfordia sp. *Phomopsis scobina (Cooke) *Harsia sp. Höhn. *Periconia cookei E.W. Mason *Phyllactinia sp. (possibly, P. et M.B. Ells guttata) *Periconia sp. *Phomopsis scobina (Cooke) Höhn. *Stachybotrys sp. *Trichothecium roseum (Pers.) Link. ***Diplodia sp. ***Diplodia sp. ***Diplodia sp. ***Gliomastix sp. ***Cytospora pruinosa (Fr.) ***Stachybotrys sp. Sacc. ***Trichoderma sp. ***Trichoderma sp. May 27, **Alternaria spp. **Alternaria sp. 2020 **Cladosporium sp. **Cladosporium macrocarpum **Fusicladium fraxini Aderh. Preuss **Hymenoscyphus fraxineus **Cladosporium sp. (T. Kowalski) Baral, Queloz & **Coniothyrium sp. Hosoya **Dictyochaeta sp. **Fusicladium fraxini Aderh. **Gyrothrix ramosa Zucconi & Onofri **Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz & Hosoya **Periconia cookei E.W. Mason & M.B. Ellis **Periconia sp. Notes: * – sampled on leaves; ** – sampled on petioles; *** – sampled on shoots.

48 Decline of Fraxinus excelsior L. in parks of Saint Petersburg: Who is to blame – Hymenoscyphus fraxineus or Diplodia spp.?

Figure 4. Conidia (left), conidia and conidiophores (right) of Diplodia mutila (Fr.) Mont. from shoots of Fraxinus excelsior collected on July 25, 2019 in Aleksandrovsky Park, Pushkin (left) and Palace Park, Gatchina (right) (photo by Dmitrii A. Shabunin). of the surveyed park and on any date. The cluding landscape characteristics (Gros- fungus was found only on the petioles of didier et al., 2020). However, the data fallen leaves in spring. This finding sug- obtained in Pushkin and Gatchina can sig- gests that the role of the highly pathogenic nificantly change our understanding of the H. fraxineus in the weakening and dieback causes of ash dieback and possible meth- of ash crowns in the surveyed parks is ods for the preservation of ash stands. The questionable. local foci of ash dieback caused by H. frax- Out of the 30 taxa of micromycetes be- ineus were recorded in ash plantations at longing to the 23 genera recorded in this Dudergof Heights (Shabunin et al., 2012) study (Table 2), only coelomycetes from the which is only 14–18 km away from Push- genus Diplodia Fr. can cause shoot blight of kin and Gatchina. It is also known that the such a kind (Merezhko, 1980). A few spe- presence of H. fraxineus was confirmed in cies of Diplodia are known to be associated 2011 in Saint Petersburg, where ash leaf with ash species (Alves et al., 2014). Among petioles with apothecia of the fungus were them, D. mutila is the most reported species found in the Botanical Garden (Dendrar- (Alves et al., 2014; Kowalski et al., 2016). We ium) of Saint Petersburg State Forestry identified this species among the samples Technical University and Botanical Garden collected in June and July 2019 in Aleksan- of the Botanical Institute of the Russian drovsky and Babolovsky Park (Table 2). In Academy of Sciences (Musolin et al., 2014, the samples collected in August 2019 in all 2017). Despite the pathogen’s presence, the three parks, Diplodia sp. was also present, decline of ash trees was not obvious at that but we failed to identify particular species. time and is not observed now. These foci of On average, Diplodia sp. was recorded on H. fraxineus are only 30–50 km northward 37.5–50.0% ash trees in the survey of 2019. from Pushkin and Gatchina. Given the fair- It is interesting to note that phytopath- ly close distance between all these points, ogenic Diplodia spp. were not recorded the low activity and pathogenicity of in the ash stands severely damaged by H. fraxineus in Pushkin and Gatchina are H. fraxineus in the Tellerman Experimen- interesting facts that require further re- tal Forestry located in Voronezh Province, search. Russia (Kolganikhina, 2018). Under the circumstances when H. frax- The pathogenicity of H. fraxineus is ineus was not recorded in the samples col- known to depend on various factors, in- lected from the ash trees with the symptoms

49 D.A. Shabunin et al. of dieback, the presence of Diplodia spp. can Acknowledgements. The work of D.L.M. indicate that these pathogenic ascomycetes was partly supported by the Russian Foun- cause the weakening and death of ash trees dation for Basic Research (grant #17-04- in the surveyed parks. However, data are 01486). We sincerely acknowledge Ekateri- scarce on the pathogenicity of Diplodia spp. na A. Tsytsulina for reading the paper and developing on deciduous woody plants in making constructive comments. general and on ash in Russia in particu- lar. There is evidence of the pathogenici- ty of these fungi to conifers, but the issue References is poorly studied in respect of ash species (Merezhko, 1980; Zhukov et al., 2013). Else- Alekseyev, A.S., Selikhovkin, A.V. Khodachek, where, it has been reported that young ash O.A. 2019. Factors that influence the health trees died because of spring frosts followed conditions of the coniferous stands in recreation by infection by Diplodia mutila, Gloeosporid- stands. (Факторы, воздействующие на состояние хвойных древостоев в iella turgida (Berk. & Broome) B. Sutton, and рекреационных насаждениях). – Regional Phomopsis scobina (Cooke) Höhn. in Austria Economy and Development of Territories, 1 in 2005 (Cech, 2006). Also, D. mutila was iso- (13), 128–133. (In Russian). Alves, A., Linaldeddu, B.T., Deidda, A., Scanu, B., lated from the affected shoots of ash in Po- Phillips, A.J.L. 2014. The complex of Diplodia land (Przybył, 2002; Kowalski & Łukomska, species associated with Fraxinus and some 2005) as well as in other European countries other woody hosts in Italy and Portugal. – Fungal Diversity, 67, 143–156. https://doi. (Alves et al., 2014). org/10.1007/s13225-014-0282-9. Cech, T.L. 2006. Striking damaging agents on forest trees in 2005. – Forstschutz Aktuell, 35, 6–7. (In German with English summary). Conclusions Enderle, R., Pliūra, A., Vasaitis, R. (eds.) 2017. Advances in Ash Dieback Research – and The pathogenic ascomycete H. fraxineus Some Other Invasive Diseases of Trees. – Baltic Forestry, 23, 1–333. was not found in the samples collected Grosdidier, M., Scordia, T., Ioos, R., Marçais, B. from the crowns of the weakened and heav- 2020. Landscape epidemiology of ash dieback. ily damaged F. excelsior trees in the parks – Journal of Ecology, 108, 1789–1799. https:// doi.org/10.1111/1365-2745.13383. of Pushkin and Gatchina. It was recorded Kolganikhina, G.B. 2018. Pathogenic and only on the overwintered petioles of fallen saprotrophic fungi on ash in the stands of the leaves. At the same time, the pathogenic as- Tellerman Experimental Forestry. – Forestry Bulletin, 22(6), 40–48. (In Russian with English comycetes Diplodia spp. and, in particular, summary). D. mutila colonized almost all shoots sam- Kowalski, T., Kraj, W., Bednarz, B. 2016. Fungi pled. Under such circumstances, we as- on stems and twigs in initial and advanced stages of dieback of European ash (Fraxinus sume that H. fraxineus opens “the entry of excelsior) in Poland. – European Journal of infection”, and Diplodia spp. cause the main Forest Research, 135, 565–579. https://doi. weakening and decline of branches. org/10.1007/s10342-016-0955-x. The data obtained suggest that there Kowalski, T., Łukomska, A. 2005. Study on ash dying in the Włoszczowa Forest Unit stands. are some specific factors that inhibit the – Acta Agrobotanica, 59 (2), 429–440. (In Polish activity and/or spreading of H. fraxineus with English summary). and, thus, promote dominance of other Merezhko, T.A. 1980. Fungal Flora of Ukraine. Spheropsidal Fungi. (Флора грибов phytopathogenic species of fungi. The fac- Украины. Сферопсидальные грибы). Kiev, tors determining the low activity of H. frax- Naukova Dumka. 208 pp. (In Russian). ineus as well as the role of Diplodia spp. in the weakening of F. excelsior stands in and around Saint Petersburg require further re- search.

50 Decline of Fraxinus excelsior L. in parks of Saint Petersburg: Who is to blame – Hymenoscyphus fraxineus or Diplodia spp.?

Moschenikova, N.B. 2011. Assessment of the Przybył, K. 2002. Fungi associated with necrotic ecological state of green spaces of St. Petersburg. apical parts of Fraxinus excelsior shoots. – (Оценка экологического состояния зелёных Forest Pathology, 32, 387–394. https://doi. насаждений Санкт-Петербурга). – Abstract org/10.1046/j.1439-0329.2002.00301.x. of the Dissertation for the degree of Candidate Selikhovkin, A.V., Baryshnikova, S.V., Denisova, of biological sciences. Moscow, Moscow State N.V., Timofeeva, Yu.A. 2018. Species University of Forest. 19 pp. (In Russian). composition and population dynamics Mozolevskaya, E.G., Kataev, O.A., Sokolova, of dominant dendrophagous moths E.S. 1984. Methods of Forest Pathological (Lepidoptera) in St. Petersburg and its Surveys of Foci of Stem Pests and Forest environs. – Entomological Review, 98(8), 963– Diseases. (Методы лесопатологического 978. обследования очагов стволовых вредителей Selikhovkin, A.V., Drenkhan, R., Mandelstam, и болезней леса). Moscow, Forest Industry. M.Yu., Musolin, D.L. 2020. Invasions of insect 152 pp. (In Russian). pests and fungal pathogens of woody plants Musolin, D.L., Bulgakov, T.S., Selikhovkin, into the northwestern part of European Russia. A.V., Adamson, K., Drenkhan, R., Vasaitis, – Vestnik of Saint Petersburg University, Earth R. 2014. Dothistroma septosporum, D. pini Sciences, 65(2), 263–283. (In Russian with and Hymenoscyphus fraxineus (Ascomycota) English summary). are pathogens of woody plants that cause Shabunin, D.A., Semakova, T.A., Davydenko, serious concern in Europe. (Dothistroma E.V., Vasaitis, R.A. 2012. Ash decline in the septosporum, D. pini и Hymenoscyphus nature monument Dudergof Heights, caused fraxineus (Ascomycota), патогены древесных by the fungus Hymenoscyphus pseudoalbidus, растений, вызывающие серьезную and morphological features of its . озабоченность в Европе). – Musolin, D.L., – Proceedings of the Saint Petersburg Forest Selikhovkin, A.V. (eds.). The Kataev Memorial Research Institute, 1–2, 70–79. (In Russian with Readings – VII. Pests and Diseases of Woody English summary). Plants in Russia. Proceedings of International Vasaitis, R., Enderle, R. (eds.). 2017. Dieback of Conference, Russia, Nov. 2014. St. Petersburg, European Ash (Fraxinus spp.) – Consequences 54–55. (In Russian). and Guidelines for Sustainable Management. Musolin, D.L., Selikhovkin, A.V., Shabunin, D.A., Uppsala, Swedish University of Agricultural Zviagintsev, V.B., Baranchikov, Y.N. 2017. Sciences. 299 pp. Between ash dieback and : Zhukov, A.M., Gninenko, Y.I., Zhukov, P.D. Two Asian invaders in Russia and the future of 2013. Dangerous and Poorly Studied Diseases ash in Europe. – Baltic Forestry, 23(1), 316–333. of Coniferous Trees in Forests of Russia. Nowak, D.J., Crane, D.E., Stevens, J.C. 2006. (Опасные малоизученные болезни хвойных Air pollution removal by urban trees and пород в лесах России). 2nd ed. Pushkino, shrubs in the United States. – Urban Forestry VNIILM. 128 pp. (In Russian). & Urban Greening, 4, 115–123. https://doi. org/10.1016/j.ufug.2006.01.007.

Received May 11, 2020, revised October 10, 2020, accepted November 23, 2020

51