ZOOSYSTEMATICA ROSSICA, 25(2): 226–232 27 DECEMBER 2016

Aphids of the family Eriosomatidae (Insecta: Homoptera) in Belarus Тли семейства Eriosomatidae (Insecta: Homoptera) Беларуси

S.V. BUGA, D.G. ZHOROV, N.V. LESHCHINSKAYA & A.V. STEKOLSHCHIKOV*

С.В. БУГА, Д.Г. ЖОРОВ, Н.В. ЛЕЩИНСКАЯ, А.В. СТЕКОЛЬЩИКОВ

S.V. Buga, Department of Zoology, Belarusian State University, 4 Nezavisimosti av., 220030 Minsk, Republic of Belarus. E-mail: [email protected] D.G. Zhorov, Department of Zoology, Belarusian State University, 4 Nezavisimosti av., 220030 Minsk, Republic of Belarus. E-mail: [email protected] N.V. Lyashchynskaya, Scientific and Practical Centre for Bioresources, 27 Akademicheskaja st., 220072 Minsk, Republic of Belarus. E-mail: [email protected] A.V. Stekolshchikov, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya nab., 199034 St Petersburg, Russia. E-mail: @zin.ru

Investigation of Eriosomatidae in Belarus started in the 1900s. However, a regional checklist of Eriosomatidae aphids was not published till now. Based on material preserved in the col- lections of Belarusian State University and the Zoological Institute of the Russian Academy of Sciences, and data scattered across publications we have compiled the first comprehen- sive list of Eriosomatidae recorded from Belarus and briefly analysed it from the geographical and ecological points of views. The list includes 12 genera and 27 species. Pemphigus passeki Börner, 1952 has been recorded from Belarus for the first time. The registered diversity is less abundant than in the adjacent Poland. In the accordance with the global pattern of aphids host plant connections, a single species permanently inhabit woody plants (monoecious spe- cies), the other ones are dioecious and migrate from woody plants to woody (eight species) or herbaceous (12 species) plants. Four species is anholocyclic. Исследования фауны тлей семейства Eriosomatidae в Беларуси были начаты еще в пер- вые десятилетия XX века, однако до настоящего времени ни одного регионального спи- ска эриосоматид не было опубликовано. Целью данной работы было обобщение сведе- ний о Eriosomatidae Беларуси, имеющихся в разрозненных публикациях, которые были дополнены данными, полученными в ходе собственных исследований. Это позволило впервые составить аннотированный список эриосоматид фауны Беларуси и кратко про- анализировать особенности их образа жизни. Список включает 27 видов из 12 родов. Pemphigus passeki Börner, 1952 впервые указан для фауны Беларуси. Выявленное на тер- ритории Беларуси число видов семейства оказалось меньше, чем в соседней Польше. Только один вид однодомен и постоянно обитает на одном растении-хозяине. Большин- ство тлей-эриосоматид фауны Беларуси являются двудомными и мигрируют с древес- ных растений на другие древесные (восемь видов) или травянистые (12 видов) растения; четыре вида неполноциклы, то есть развиваются без смены растений-хояев. Key words: gall-forming , monoecious, dioecious, Rhynchota, Homoptera, Eriosomati- dae, Aphidinae, invasive species Ключевые слова: галлообразующие насекомые, однодомные, двудомные, Rhynchota, Homoptera, Eriosomatidae, Aphidinae, инвазивные виды

* Corresponding author.

© 2016 Zoological Institute, Russian Academy of Scienсes S.V. BUGA ET AL. ERIOSOMATIDAE IN BELARUS 227

INTRODUCTION In 1955, G.Ch. Shaposhnikov recor- ded six species of Eriosomatidae, Erio- Belarus, a small (207 600 km2) Central soma lanuginosum, E. patchiae, Pachy- European country, is located in the tran- pappa warschavensis (Nasonov, 1894) (as sitional territory between two ecological Asiphum varsoviensis Mordv.), P. tremulae zones: the European deciduous forests and (as Asiphum tremulae Deg.), Pemphigus the North Eurasian evergreen coniferous borealis Tullgren, 1909, and Pemphigus im- forests. The country is divided into six ad- munis Buckton, 1896 (as Pemphigus lich- ministrative provinces (Fig. 1). tensteini Tullgr.), as pests of forest woody Study on Eriosomatidae was started in plants in Belarus (Shaposhnikov, 1955). the 1900s, when prof. A.K. Mordvilko col- After the 1950s a study of aphids, pests of lected aphids in different parts of Belarus. ornamental plans, was started in Belarus by Two species of Eriosomatidae, Eriosoma N.L. Losinskaya (1960) who recorded two lanuginosum (Hartig, 1839) and Kalten- species of Eriosomatidae in parks. Infor- bachiella (as Tetraneura) pallida (Haliday, mation on Eriosomatidae species was also 1838), are recorded for Grodno Province given in the monographies of S.V. Gorlenko by A.K. Mordvilko in his monography & N.A. Pan’ko (1967, 1972), S.V. Gorlenko, (Mordvilko, 1924) devoted to the wooly A.I. Blintsov & N.A. Pan’ko (1988). apple ( (Haus- Comprehensive studies of the aphid mann, 1802)) and other Eriosomea. In fauna in Belarus were started in the 1980s. 1930, Mordvilko listed for Eastern (Soviet Till now several papers on the local fauna part) Belarus 28 aphid species, including 13 of Belarusian regions have been published species of Eriosomatidae: Eriosoma patchiae (Buga, 1989, 1995; Stekolshchikov & Buga, (Börner et Blunck, 1916), E. lanuginosum, 2006; Buga et al., 2008; Rakauskas & Buga, Forda formicaria Heyden, 1837, F. mar- 2010; Stekolshchikov et al., 2008, 2010, ginata Koch, 1857 (as Forda trivialis Pass.), 2012), and a special attention was paid to Geoica urticularia (Passerini, 1856), Pachy- species damaging woody plants (Buga & pappa vesicalis Koch, 1856, P. (as Asiphum) Gorlenka, 1987; Buga, 1997, 2001; Buga & tremulae (Linnaeus, 1761), Pachypappella Stekolshchikov, 2009). However, a general (as Pachypappa) lactea (Tullgren, 1909), regional checklist of Eriosomatidae has not Paracletus cimiciformis von Heyden, 1837, been published yet. Pemphigus bursarius (Linnaeus, 1758), P. populinigrae (Schrank, 1801) (as P. fi- MATERIAL AND METHODS laginis B.d.F.), P. spyrothecae Passerini, 1856, and Thecabius affinis (Kaltenbach, The paper is based on the material col- 1843). At the same time several cecidologi- lected by authors since 1983. Although cal papers reported cecidia-forming aphis this information had been partly published of Western Belarus (territory of Poland at in Russian or Belarusian, we prefer to re- that time). Seven species of Eriosomatidae peat the collection data in English as elec- (Eriosoma ulmi (Linnaeus, 1758), Pachy- tronic supplementary material to this pa- pappa marsupialis Koch, 1856 (as Pemphi- per. We also listed the material collected by gus marsupialis Courch.), Pemphigus bursar- T.V. Tikhomirov, F.V. Sautkin, D.L. Petrov, ius, P. populinigrae (as P. filaginis B. d. F.), A.S. Roginsky & O.V. Sinchuk, and micro- P. spyrothecae, Prociphilus xylostei (de Geer, scope slides of Eriosomatids collected by 1773), and Thecabius (as Pemphigus) affi- A.K. Mordvilko and storaged in the col- nis) were recorded by Z. Fiedorowiczowna lection of the Zoological Institute of RAS (1930), and four species (Pemphigus bur- (St Petersburg). sarius, P. spyrothecae, P. xylostei, Tetraneura Microscope slides were prepared using (as Schizoneura) ulmi) by J. Perepeczko- Faure-Berlese mounting fluid or Canada Baumanowa (1934). balsam (Blackman & Eastop, 2000). The

© 2016 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 25(2): 226–232 228 S.V. BUGA ET AL. ERIOSOMATIDAE IN BELARUS

Fig. 1. Ad- ministrative provinces of Belarus and geographic points of aphid sam- pling and registration. material is deposited in the Department of Aphidoidea. This opinion was also sup- of Zoology of Belarusian State University ported by Heie & Wegierek (2009). (Minsk, Belarus) and the Zoological Insti- tute of RAS (St Petersburg). Data extract- Abbreviations ed from publications are given in a uniform Collectors: AM – A.K. Mordvilko, manner, but the completeness of the data AR – A.S. Roginsky, DZh. – D.G. Zhorov, depends on the original publications. When DP – D.L. Petrov, OS – O.V. Sinchuk, SB – different variants of transliteration of geo- S.V. Buga, VKh – V.I. Khvir, VT – V.N. Tik- graphical names are more or less widely homirov. used in the literature, we provide the ad- Localities: BBR – Berezina Biosphere ditional variants in parentheses after the Reserve, BPF – Belovezha Primeval Forest, main variant. The special keys proposed by CBG – Central Botany Gardens of the Na- B. Osiadacz & R. Hałaj (Hałaj & Osiadacz, tional Academy of Sciences of Belarus, hort. 2013; Osiadacz & Hałaj, 2014) have been cv. – cultivars, NBR – Naliboki Biological used for identification of Pemphigus Har- Reserve, PLR – Priluki landscape reserve, tig, 1839 species on the basis of galls formed RWS – railway station. on poplars. Aphid synonymy follows Rem- è è audi re and Remaudi re (1997) with sub- LIST OF SPECIES sequent additions (Eastop & Blackman, 2005; Holman, 2009; Blackman & Eastop, The list of species is published as an 2011; Favret, 2016). Aphid taxonomic clas- electronic supplementary material which is sification follows Shaposhnikov (1964). In available from: this classification, Eriosomatidae (as Pem- http://www.zin.ru/journals/zsr/content. phigidae) is considered as a separate family asp?year=2016.

© 2016 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 25(2): 226–232 S.V. BUGA ET AL. ERIOSOMATIDAE IN BELARUS 229

DISCUSSION species) plants. At least four Fordini spe- cies, Forda formicaria Heyden, 1837, F. mar- Presently, the fauna of Belarus includes ginata Koch, 1857, Geoica urticularia (Pas- 27 species from 12 genera of Eriosomati- serini, 1856), and Prociphilus cimiciformis ö dae. Pemphigus passeki B rner, 1952 has von Heyden, 1837, inhabit plant roots and been recorded from Belarus for the first are anholocyclic under the condition of Be- time on the basis of material collected in larus, because their primary host plants are 1900 by А.К. Mordvilko. Pachypappa po- exotic spp. and absent in the local puli (Linnaeus, 1758) was first mentioned flora. Secondary host plants of Pachypappa by S.V. Buga (2001) with reference to marsupialis Koch, 1856 and P. warshaven- A.K. Mordvilko (1930); however, reexami- sis (Nasonov, 1894) are unknown. Poplars nation of the cited publication revealed that (Populus spp.) are the primary hosts of 14 Mordvilko (1930) did not record this spe- species of Pemphigini, elms (Ulmus spp.) cies directly for Belarus. Three species of are the primary hosts of six species of Eriso- Pachypappa Koch, 1856 are considered for matini. Common spruce (Picea abies) is the Belarus according to literature data only secondary host plant for five Erisomatidae ó (Mordvilko, 1930; Fiedorowicz wna, 1930 species. Host plant species are represented and Shaposhnikov, 1955). by eight families. One anholocyclic species, The species richness in Belarus is not P. cimiciformis, is able to feed on the roots of so high compared with the neighbouring a great variety of plants. countries like Poland (49 species, 19 gen- Some Erisomatidae species, Pemphigus ł era) (Ha aj, Osiadacz & Poljaković-Pajnik, spyrothecae Passerini, 1856, P. bursarius ł 2016; Osiadacz & Ha aj, 2009, 2010, 2012; (Linnaeus, 1758), and Eriosoma ulmi (Lin- Wojciechowski et al., 2015). One of the rea- naeus, 1758), are common and harmful in sons of this is the absence of such thermo- ornamental green stands in Belarus. philic species as Aploneura lentisci (Passer- ini, 1856) or Mimeura ulmiphila (del Guer- ACKNOWLEDGEMENTS cio, 1917), etc. The Eriosomatidae were more extensively studied in Minsk Prov- We are grateful to F.V. Sautkin, D.L. Petrov, ince (Fig. 1). Data from Belarus Lakeland A.S. Roginsky, O.V. Sinchuk, V.N. Tikhomirov (Poozer’e) were received mainly from the for providing aphid and cecidological materials Gorodock Highland (Rakauskas & Buga, and to V.N. Tikhomirov (Belarusian State Uni- 2010). versity, Minsk) for his help in the identification of host plants. This study was supported partly The majority of registered species are by the Belarusian Republic Foundation for Basic common for Europe or the Palaearctic. At Research (grant no B15–063). least one species, Pemphigus borealis Tull- gren, 1909, is invasive and obviously has REFERENCES been brought from Far East (Shaposh- nikov, 1955) with saplings of introduced Blackman R.L. & Eastop V.F. 2000. Aphids on host plants such as poplar Populus laurifo- the World’s Crops, an Identification and In- lia. Pemphigus spyrothecae is common on formation Guide, 2nd Edition. Chichester: P. italica and very rare on other poplars. The John Wiley & Sons. 476 p. species have never been registered on “wild” Blackman R.L. & Eastop V.F. 2011. Additions trees of P. nigra growing in floodplain of Pri- and amendments to “Aphids on the World’s Plants”. Zootaxa, 2774: 57–68. pjat’ and other rivers in Belarusian Polesie. Blackman R.L. & Eastop V.F. 2016. Aphids on As opposed to the majority of Erisoma- the World’s Plants. An online identification tidae species, P. spyrothecae is monoecious. and information guide [online]. Available Dioecious aphids migrate from woody plants from: www.aphidsontheworldsplants.info to woody (eight species) or herbaceous (12 [updated 18 September 2016; visited 1 De-

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