New records of an alien aphid species Tinocallis (Sappocallis) takachihoensis from countries in central and northern Europe (Hemiptera, Aphididae, Calaphidinae)

Abstract The aphid genus Tinocallis Matsumura, 1919 (Hemiptera: Aphididae: Calaphidinae) in central and northern Europe is reviewed; it includes four species. The first records of the Asian elm aphid Tinocallis takachihoensis Higuchi, 1972 are reported from the Czech Republic, Denmark, and Poland. The record in Denmark is the first in Scandinavia. Alate viviparous females and nymphs of T. takachihoensis were collected from Ulmus glabra “Pendula” (the Czech Republic and Poland) and from U. minor (Denmark) in 2017. Tinocallis takachihoensis is the fourth Tinocallis species to be recorded from Poland and together with two other species from the subgenus Sappocallis, T. nevskyi and T. saltans, is a species of alien origin. The alate viviparous females are reviewed and re-described and their affinities and distribution in central and northern Europe are discussed. A key to the European species of Tinocallis based on the characters of live and slide-mounted specimens is also given.


Introduction
Of the approximately 1590 aphid species described or recorded from Europe (Nieto Nafría et al. 2013) to date, approximately 103 species are known to be of an alien origin from North America and Asia (Coeur d'acier et al. 2010, Pérez Hidalgo et al. 2011Rakauskas 2011;Panini et al. 2017). The area of Poland is one of the best recognised in terms of aphid fauna in Europe with 766 recorded species and subspecies (Wojciechowski et al. 2015;Kanturski et al. 2017) to date. In Poland, as many as 34 species of an alien origin were reported earlier (Wieczorek 2011). However, this number is continuously changing due to ongoing research and biological invasions (Kanturski et al. 2017;Walczak et al. 2017).
The aphid genus Tinocallis Matsumura, 1919 (Calaphidinae) comprises 18-19 species within four subgenera (Favret 2017;Lee and Lee 2017) and is the second largest Panaphidini genus (Quednau 2001;Favret 2017). The species of this genus are characterised by a small and delicate body and are mostly associated with Ulmaceae Eastop 1994, 2017). All of the viviparae are alate and they usually have paired spinal and marginal tubercular processes on the thorax and abdomen. The secondary rhinaria on antennal segment III are narrow, transversely elongated, or slit-like. The genus has caused many taxonomical difficulties due to its seasonal variations (Quednau 2001).
The Asian elm aphid, Tinocallis takachihoensis Higuchi, 1972, is one of the members of the subgenus Sappocallis Matsumura, 1919. This species was originally described from Japan and is known to be primarily distributed in Eastern Asia (Higuchi 1972). Tinocallis takachihoensis along with T. saltans (Nevsky, 1929), T. ulmiparvifoliae Matsumura, 1919, andT. zelkowae (Takahashi, 1919) have been introduced to other parts of the world (Blackman and Eastop 2017;Foottit et al. 2006;Quednau and Shaposhnikov 1988). In Europe, this species was reported for the first time from France (from a suction trap) (Leclant 1986). Since then, this species has been reported from the United Kingdom (Döring 2007(Döring , 2008 and the Mediterranean area (Patti and Barbagallo 1997;Mier Durante and Perez Hidalgo 2002;Barbagallo and Massimino Cocuzza 2014). Although recent observations of the occurrence of this species come from Greece (Papapanagiotou et al. 2012), Germany, and the Netherlands (Piron 2013), Piron's information comes from a personal communication from Schrameyer who received the name of the species in question from Thieme (T. Thieme, pers. comm.).
In this paper, the occurrence of T. takachihoensis from the Czech Republic, Denmark, and Poland is reported for the first time. Its affinities to other known Tinocallis species from these regions are also discussed and a morphological key to the identification of all European representatives of this genus is provided.

Material and methods
Alate viviparous females and nymphs of Tinocallis takachihoensis were collected in Opava (the Czech Republic) on 19.08.2017, Katowice (Poland) on 12.07.2017, and Copenha-gen (Denmark) on 16.06.2017. The aphids were transferred to 80% ethanol and prepared after the Kanturski and Wieczorek (2012)  For morphological comparison slides of Tinocallis specimens from other localities were used. The studied material is deposited in the Natural History Museum in London, UK (BMNH), and Zoological Institute, Polish Academy of Sciences, Warsaw, Poland (ZMPA).

Genus Tinocallis Matsumura, 1919 Figs 1-8
Tinocallis Matsumura, 1919: 100. Lutaphis Shinji, 1924 Diagnosis. This genus can be recognized by having narrow transversely elongated or slit-like secondary rhinaria on ANT III, and ABD III, V, and VII with laterally displaced spinal dorsal setae. Abdominal tergites I and II usually have finger-like dorsal tubercles.

Tinocallis (Sappocallis) takachihoensis Higuchi, 1972
Figs 1-8; Table 1 Redescription. Alate viviparous female Colour. Colour of live specimens: head and thorax black, ANT pale yellow with dark apices of segments, fore and middle legs pale yellow, hind legs pale yellow with black distal part of femora and proximal part of tibiae. Wings pigmented on the area of pterostigma, media and Cu 1b . Abdomen yellow (Fig. 1a, c). Pigmentation of mounted specimens: head and thorax brown (Fig. 1a). ANT pale with brown ANT I and ANT II and slightly darker apices of flagellar segments (Fig. 2a). Morphometric characters. ANT 0.76-1.00 × BL and 0.26-0.27 × HW. ANT III with 17-21 slit-like secondary rhinaria (Fig. 3a). PT 1.13-1.19 × BASE. Other antennal ratios: ANT VI/ANT III 0.57-0.64, ANT V/ANT III 0.52-0.54, ANT IV/ANT III 0.52-0.61. Ant I with 3 setae, Ant II with 2-3, ANT III with 9-13 setae, ANT IV with 2 setae, ANT V with 2-3 setae, ANT VI with one basal seta. URS 0.18 × ANT III, 0.28-0.32 × ANT VI, and 0.90-1.00 × HT II. Pronotum with two finger-like projections on the distal part ( Fig. 4a). Mesonotum with two large, imbricated projections with rounded apices (Fig. 5a). HT II 0.18-0.20 × ANT III and 0.31-0.32 × ANT VI. Forewings with distal branches of media bordered with fuscous and with more-or-less extensive fuscous patches at distal ends of Cu 1a and Cu 1b (Fig. 6a). Hind legs with dark distal part of femora and proximal part of tibiae (Fig. 7a). Abdomen pale, SIPH pale on basal part and pale brown on apex. Abdomen without sclerotisation besides very small darker projections on ABD III-V (Fig. 8a) Colour. Colour of live specimens: head and prothorax yellow with brown longitudinal stripes. The rest of thorax brown. ANT pale yellow with dark apices of segments, fore and middle legs pale yellow, hind legs with black femora and proximal part of tibiae. Wings pigmented on the area of pterostigma, media and Cu 1b . Abdomen yellow with brown extensive spots on the dorsal side (Fig. 1b). Nymphs pale yellow (Fig. 1d). Pigmentation of mounted specimens: head and thorax brown. ANT pale with brown ANT I, ANT II and slightly darker apices of flagellar segments (Fig. 2b). Morphometric characters. ANT 0.78-0.94 × BL and 0.25-0.27 × HW. ANT III with 16-26 slit-like secondary rhinaria (Fig. 3b). PT 0.23-0.25 × BASE. Other antennal ratios: ANT VI/ANT III 0.31-0.35, ANT V/ANT III 0.45-0.51, ANT IV/ANT III 0.55-0.60. Ant I with 3-4 setae, Ant II with 4, ANT III with 10-15 setae, ANT IV with 3-5 setae, ANT V with 2-4 setae, ANT VI with one basal seta. URS 0.18-0.20 × ANT III, 0.57 × ANT VI, and 1.04-1.09 × HT II. Pronotum without projections. Only very small protuberances, similar to those on the head are visible (Fig. 4b). Mesonotum without projections (Fig. 5b). HT II 0.17-0.18 × ANT III and 0.52-0.55 × ANT VI. Forewings without a radial sector. Stigma and media strongly bordered with fuscous basally as well as distally, with a dark spot over Cu 1b (Fig. 6b). Hind legs with uniformly dark brown femora and proximal part of tibiae (Fig. 7b). Abdomen robust, pale with brown more or less extensive dorsal sclerites or broken crossbars. SIPH dark brown (Fig. 8b).  Table 1 Redescription. Alate viviparous female. Colour. Colour of live specimens: head brown, ANT yellow with distinctly darker apices of ANT IV and V and almost whole ANT VI. Prothorax yellow or light brown, the rest of thorax dark brown to dark brown. Legs pale with visible darker distal part of hind femora. Abdomen yellow with brown with brown, small and rounded sclerites (Fig. 1e). Pigmentation of mounted specimens: head and thorax light brown to brown with lighter prothorax. The rest of body pale (Fig. 2c).

Redescription. Alate viviparous female
Colour. Colour of live specimens: whole body pale yellow to whitish yellow with poorly visible very small, brown abdominal sclerites. Wings not pigmented (Fig. 1f ).  Pigmentation of mounted specimens: head pale with light brown edges, ANT pale, pronotum pale with light brown longitudinal stripes. The rest of thorax brown (Fig. 2d).

1
Live specimens: head and thorax yellow or brown, abdomen yellow with or without brown patches. Mounted specimens: head and pronotum without projections (Fig. 4b) Live specimens: head and thorax brown, abdomen yellow with extensive brown patches (Fig. 1b). Mounted specimens: forewings pigmented, hind femora brown, abdomen with extensive, dark sclerotisation (Fig. 2b)  Live specimens: head and thorax black, abdomen yellow without dark sclerites (Fig. 1a, c). Pronotum with one pair of projections on distal part. Forewings pigmented. Hind legs with brown distal part of femora and proximal part of tibiae (Fig. 7a)  Live specimens: head and thorax brown, abdomen with clearly visible sclerites with projections or tubercles, wings clearly pigmented (Fig. 1e). Mounted specimens: ANT III secondary rhinaria transverse oval (Fig. 3c). Wings clearly pigmented. Abdomen with small, sclerotised, spinal projections on ABD IV (Fig. 8c) (Fig. 3d). Wings very poorly pigmented. Abdomen without small sclerotised spinal projections on ABD IV (with only two sclerites) (Fig. 8d) (Quednau 2003). Two of the Tinocallis species known from Europe, T. ulmiparvifoliae and T. zelkowae, are only known from south-western Europe and on bonsai trees imported into the United Kingdom, while the remaining taxa have been reported to occur more widely, especially in central and northern Europe. From the four species presented here, T. platani is characterised as being widely distributed, T. nevskyi in the central, western, and northern parts of the continent, while T. saltans is recorded mostly in the central and eastern parts of Europe, but also from Italy and Spain (Nieto Nafría and Mier Durante 1998). Earliest European records of T. takachihoensis were from southern France and Italy, with more recent records from Greece, Germany, Malta, and the Netherlands. Thus, it seems from the dispersion routes of this species in Europe, that for more than a decade it has preferred regions with milder climate (the Mediterranean Basin and the western coast of Europe). Its sexual generation is as yet only known from Malta (Patti and Barbagallo 1997). The recent finding in Central Europe indicates the possibility of either the overwintering of this species in the climatic conditions of this part of Europe or rapid early-summer migrations from the territory that is already occupied (Piron 2013). Despite some milder winters, which have occurred in Central Europe recently and have influenced aphid biology , the period of aphid collection in this case (June-August) indicates the second possibility. The species, however, requires observation as it may become a pest on ornamental plants or it may adapt to more severe climatic conditions.