© Entomologica Fennica. 11 April 2014 First records of gall-inducing aphid Pemphigus populi (Hemiptera: Aphidoidea, Eriosomatidae) in Poland with gall-based key to Central and North European species of the genus Barbara Osiadacz & Roman Ha³aj Osiadacz, B. & Ha³aj, R. 2014: First records of gall-inducing aphid Pemphigus populi (Hemiptera: Aphidoidea, Eriosomatidae) in Poland with gall-based key to Central and North European species of the genus. Entomol. Fennica 25: 16 26. The paper presents first records of Pemphigus populi Courchet, 1879 (Hemipte- ra, Aphidoidea, Eriosomatidae) from Poland with a short description of the mor- phological characteristics of its fundatrix and fundatrigenia. Special attention is paid to the characteristics which distinguish this species from other Polish as well as the Central and North European representatives of this genus on poplars (Populus spp.). Information on the biology and distribution of P. populi in the world are given. A key to Central and North European species of Pemphigus, based on their galls formed on the primary host plants is also provided. B. Osiadacz, Poznañ University of Life Sciences, Department of Entomology and Environmental Protection, D¹browskiego 159, 60-594 Poznañ, Poland; E-mail: [email protected] R. Ha³aj, The Upper Silesian Nature Society, Huberta 35, 40-543, Katowice, Po- land; E-mail: [email protected] Received 25 April 2013, accepted 18 October 2013 1. Introduction Pemphigus spp. includes both holocyclic (with full developmental cycle) and heteroecious The worlds aphid fauna of Pemphigus Hartig, species (which in their seasonal cycle change the 1839 includes over 70 species (Remaudière & host) and anholocyclic (breeding only by parthe- Remaudière 1997, Blackman & Eastop2006, nogenesis) monoecious ones (Zwölfer 1958, Holman 2009), out of which 20 have been re- Lampel 1960, Heie 1980, Nieto Nafría et al. corded in Europe (Nieto Nafría et al. 2012). So 2002, Stroyan 2009) (Fig. 1), an exception being far 9 species have been reported from Poland the holocyclic and at the same time monoecious (Barczak 1987, Osiadacz & Ha³aj 2009, 2010). P. spyrothecae Passerini, 1856 (Urban 2002, Here we present the first records of Pemphigus Osiadacz & Ha³aj 2011). All the holocyclic Pem- populi Courchet, 1879 from Poland, thus intro- phigus spp. induce galls on their primary hosts ducing the 10th species of this aphid genus in the [Populus L. subgenus Eupopulus Dode, espe- country, with a short description of morphologi- cially of the section black Aigeiros Duby (Figaj cal characteristics of the fundatrix and funda- & Stecki 1979)] (e.g. Dunn 1960, Shaposhnikov trigenia as well as notes on the biology and distri- 1964, Whitham 1978, Smith 1985, Wool 2004, bution of the species. Pike et al. 2007). Both the gall shape and location ENTOMOL. FENNICA Vol. 25 First records of Pemphigus populi in Poland 17 Fig. 1. Life cycles of Central and North European Pemphigus spp. on the plant (Fig. 2) are characteristic enough to Populus nigra L. (Fig. 3). They were recorded at enable to differentiate particular species of four localities (Fig. 4) as follows: 15.V. (funda- Pemphigus spp. Accordingly, an original identi- trices and nymphs) and 8.VI.1996 (alatae fication key of North and Central European fundatrigeniae and nymphs), and 14.V.2011 Pemphigus species is presented on this basis. (fundatrices and nymphs), Ruda l¹ska-Byko- wina (Silesian Upland) UTM: CA47; 08.VI.2012 (alatae fundatrigeniae and nymphs), Górki near 2. Material examined Wilica (Nida Basin), UTM: DA87; 24.VI.2012 (alatae fundatrigeniae and nymphs), Gruczno The material consists of numerous fundatrices as (Lower Vistula Valley), UTM: CE21; 17.VI. well as numerous alate fundatrigeniae and 2012 (alatae fundatrigeniae and nymphs), Ligota nymphs which are all greyish green and highly Dolna-Kamienio³om (Silesian Upland) UTM: wax powdered in galls on leaves of black poplar BA99. 18 Osiadacz & Ha³aj ENTOMOL. FENNICA Vol. 25 Fig. 2. Gall-inducing Pemphigus spp. a. P. immunis.b.P. bo- realis.c.P. trehernei (modified draft based on Heie (1980)). d. P. bursarius.e.P. spyrothecae.f.P. protospirae.g.P. po- puli.h.P. passeki (modified draft based on Prinsen (1990)). i.P. gairi.j.P. phenax.k.P. populinigrae. 3. Main morphological characters length as IV; processus terminalis (VIb) 0.250.4 times as long as basal part (VIa) of antenna Fundatrix. Body 2.42.7 mm, abdominal wax segmet VI; secondary rhinaria on antenna seg- gland plates (secrete wax substances) consisting of ments IV and V rather oval and wide greater a few and rather large facets; anntenae 4-seg- than rhinaria on antenna segment III (Fig. 5a); the mented, about 0.17 times body length; antenna seg- number of secondary rhinaria on segment V are 1 ment III 0.70.95 times the length of segment IV. or 2; siphunculi pores absent (Fig. 5c). Fundatrigenia (Fig. 5). Body 1.52.4 mm, ab- The latter two traits are basic morphological domen with small but distinct marginal wax hints which helpquickly differentiate winged vi - gland plates; apical segmet of rostrum pointed viparous females (fundatrigenia) of this species (Fig. 5b), about 0.10.12 mm and 0.50.7 times (subgenus Pemphiginus Börner, 1930 (e.g. as long as the 2 segment of the hind tarsus; an- Börner 1952, Barbagallo et al. 1995, Nieto Nafría tenna segment III 0.92.4 times the length of seg- et al. 2002) from other species of Pemphigus in- ment IV; antenna segment V nearly the same festing poplars, belonging to Pemphigus s. str. ENTOMOL. FENNICA Vol. 25 First records of Pemphigus populi in Poland 19 Fig. 3. Gall-induc- ing Pemphigus populi. Fig. 4. Distribution of Pemphigus po- puli in Poland. 1: Gruczno, 2: Ligota Dolna, 3: Ruda l¹ska, 4: Górki. 20 Osiadacz & Ha³aj ENTOMOL. FENNICA Vol. 25 Fig. 5. Alate funda- trigenia of Pem- phigus populi.a. Flagellum. b. Ulti- mate rostral seg- ment.c.Tipofab- domen. 4. Biology break of September and October, reemigrantes (alate sexuparae) come back to the primary host Pemphigus populi is a holocyclic and hetero- plants (Furk & Prior 1975) and breed the sexual ecious species (see Fig. 1). Its primary host plants generation (oviparous females and males). The are various poplar species of Eupopulus subge- life cycle ends with laying eggs on poplar twigs nus, mainly the black poplar (Populus nigra)and (Fig. 1). its Italian variety (P. nigra Italica). The infesta- tion causes characteristic galls (Fig. 2g, 3). They 5. Zoogeography are induced by fundatrices, which hatch from fer- tilised overwintering eggs on the break of April Pemphigus populi has been reported on vast areas and May. The first young galls in Poland were ob- of the Palaearctic from the British Isles (Stroyan served in the first half of May (15.V.1996, 1957) to Western Siberia (Ivanovskaja 1977) 14.V.2011) and mature ones were seen already at (Fig. 6). A more detailed analysis shows that most the beginning of June (08.VI.2012) with numer- locations form a belt approximately along the ous alate fundatrigeniae feeding inside. The 40th parallel of north latitude from the Iberian opening of the galls and the flowing out of the Peninsula (e.g. González Funes & Michelena migrantes were noted in the second half of June Saval 1988, Pérez Hidalgo & Nieto Nafría 2003) (17 and 24.VI.2012). and other regions of the northern Mediterranean Secondary host plants for P. populi are vari- coast: Croatia, France-Corsica, Slovenia, Tur- ous species of Fabaceae (e.g. Lathyrus pratensis key, Italy (Courchet 1879, Çanakçioglu 1966, L., Medicago lupulina L., Melilotus altissimus 1972, Janeiè, 1978, 1981, 1989, Roberti 1993, Thuill.) and the infested place most often include Lampel 2001) through the Caucasus (Dzhibladze ground and underground plant parts, particularly 1968) to Central Asia (Narzikulov 1953, 1968, small roots (Danielsson 1976). Here the large Juchnevitch 1968, Bozhko 1976, Mukhamediev generation of wingless viviparous females 1979, Gabrid 1989). In some regions of the belt, a (apterous virginogenia) develops and on the clear shift of locations towards the 50th parallel is ENTOMOL. FENNICA Vol. 25 First records of Pemphigus populi in Poland 21 Fig. 6. Occurrence of Pemphigus populi in Western Palaearctic. obvious, particularly between 25th and 35th merid- 2003), Sweden (Danielsson 1976), and Finland ian of eastern longitude, as the localities from (Albrecht 2013), may indicate that it is increasing Bulgaria, Romania, Moldova and southern its range. The thesis seems to be supported by Ukraine (including Crimea) (e.g. Mamontova finding its new localities in Poland. In spite of 1949, 1955, Bozhko 1957, 1971, 1976, Veresh- rather detailed aphidological research conducted chagin & Vereshchagina 1962, Holman & in the previous century in Silesian Upland, Pintera 1981, Vereshchagin et al. 1985, Tashev Wielokopolsko-Kujawska Lowland or Nida Ba- 1985, Gabrid 1989, Chumak 2004) are in those sin on Ma³opolska Upland (Krzywiec 1970, areas. 1982, Olesinski & Szelegiewicz 1974, Achremo- Therefore, P. populi is a species of western wicz 1972, 1975, Klimaszewski et al. 1980, Sze- Palaearctic range and more exactly of a Mediter- legiewicz 1981, Czylok 1983, Czylok & Wojcie- ranean-Pannonian-Pontian-Central Asian ele- chowski 1987, Czylok et al. 1991, Karwañska ment. Some single reports from those centres of 1991, Ha³aj 1996, 1998, Ha³aj & Wêgierek 1998, occurrence, e.g. Lebanon (Bodenheimer & Osiadacz & Wieczorek 2003, Wieczorek & Swirski 1957) or the Sinai Peninsula in Egypt Osiadacz 2005) and finding many aphid taxa (El-Akkad & Zalat 2004), seem to corroborate there (Szelegiewicz 1968, Osiadacz & Ha³aj the species character (i.e. Mediterranean). 2009), the species in question was not found then. On the other hand, less numerous reports from It seems impossible that P. populi, with such other areas, e.g. from the Czech Republic (Lam- characteristic galls, had been overlooked.