First record of the adventive oriental aphid Schizaphis piricola (Matsumura, 1917) (Hemiptera, Aphididae) in Europe

Abstract The oriental aphid Schizaphis piricola (Matsumura) is recorded for the first time in Europe, on the ornamental pear tree Pyrus calleryana in landscaped areas in Madrid (Spain). Data on the morphology of the forms on primary host (apterous and alate fundatrigeniae and fundatrices), and their biology and distribution are given. The keys for identifying species of Schizaphis (Schizaphis) in the Iberian Peninsula are updated. Two species of aphids are also recorded for the first time on Pyrus calleryana: Schizaphis piricola and Aphis pomi.


Introduction
Th e genus Schizaphis Börner contains approximately 36 Palearctic species and 6 Nearctic ones. Is a genus resembling Rhopalosiphum Koch with little diff erences between both genus, and for this reason require further taxonomical and molecular study (Blackman and Eastop 1994;Foottit et al. 2008). Th e species of Schizaphis are characterised by more or less cylindrical siphunculi slightly constrained at the apex, ultimate rostral segment short and heart size, absence of dorsal cuticular ornamentation, and alatae with two branches on the medial vein of the wings (Fig. 1D) (Pérez Hidalgo and Mier Durante 2005). Most of the species in the genus are monoecious on species of Poaceae, Juncaceae and Cyperaceae but a few mainly oriental species, are dioecious with species of Pyrus as the primary host, where they lay their cold-resistant eggs (Blackman and Eastop 2006).
Twenty-seven species have been recorded in Europe (Holman 2009;Nieto Nafría et al. 2010 Of these, only S. pyri, has Pyrus communis as its primary host and Cyperaceae as its secondary host; the rest live on Poaceae or Cyperaceae without causing fi nancial loss, except for S. graminum which can be a cereal pest (Blackman and Eastop 2000).
A photograph of a colony of aphids on the pear tree of oriental origin Pyrus calleryana Decne in "Juan Carlos I park", Barajas (Madrid, Spain) ( Fig. 1) taken on 26th April, 2009 and posted on the "Biodiversidad Virtual" portal (http://www.biodiversidadvirtual.org/) enabled the oriental species Schizaphis piricola (Matsumura) to be detected for the fi rst time in Europe. Its presence was confi rmed in a study of samples collected the following spring on the same host and in the same place. Its route of entry into Europe is probably linked to when the host plant was imported, as is the case of many other species introduced into Europe (Coeur d 'acier et al. 2010).
Th is fi nding is yet another example of how social networks play an important role in our knowledge of biodiversity and the detection and/or monitoring of invasive or endangered species (Pérez Hidalgo et al. 2009;Silverton 2010).

Description of the forms of Schizaphis piricola on primary host
Th e apterous fundatrigeniae (Figs 1C, 2B, 3B, E, H) are between 1.47 and 2.50 mm long and yellowish green to green, with pale antennae and siphunculi bearing dark tips and dark tarsi. Antennae 0.65 to 0.90 times the body; processus terminalis of antennal segment VI 3.13 to 3.92 times its base, and 0.97 to 1.13 times antennal segment III. Antennae without secondary rhinaria. Apical rostral segment 0.90 to 1.09 times second segment of posterior tarsi and usually with 2 accessory setae. Dorsal sclerotization absent. Marginal papillae on abdominal segments I to VII, absent on III to V in some specimens. Dorsoabdominal setae of anterior terguites shorter (17 to 30 μm) than those of posterior (55 to 90 μm), ventral setae intermediate in size (45 to 60 μm). Siphunculi cylindrical, with weakly defi ned subapical constriction, 0.12 to 0.19 times body and 1.84 to 2.12 times cauda. Cauda 0.17 to 0.19 mm, 1.21 to 1.46 times basal width, bearing 7 to 9 setae. Tibiae of posterior legs 0.44 to 0.50 times body.
Alatae fundatrigeniae (Figs 1D, 2C, 3C, F, I) 2.10 to 2.52 mm, green, antennae and siphunculi dark, cauda lighter in colour. Well-pigmented marginal sclerites in ter- guites II to IV, postsiphuncular sclerites fully developed and spinopleural pigmented bands always present on abdominal segments VI to VIII and also occasionally on III to V. Antennae 0.71 to 0.80 times body; processus terminalis of antennal segment VI 3.41 to 5.18 times base; antennal segments III, IV and V bearing 15-32, 7-18, 0-6 secondary rhinaria, respectively. Siphunculi 1.68 to 1.80 times cauda. Th e remaining characters are similar to those of the apterae.

Distribution
Schizaphis piricola (Matsumura) is an aphid of oriental origin which, according to Holman (2009), had only been recorded in China (north east, south east and Taiwan), Japan and Korea, though Lee et al. (2002) have records for India and Pakistan.
Nevertheless, it is possible that S. piricola is now more widely distributed because Pyrus calleryana is a very commonly planted ornamental tree species. For example, in the United States there is evidence that this tree species is rapidly becoming invasive in much of its horticultural range (Vincent 2005) and it is possible that the aphid is present at this moment.

Biology
It is a holocyclic dioecious species with species of pear tree (Pyrus sp.) as its primary host and Cyperaceae (Carex spp. and Cyperus rotundus L.) as secondary host (Miyazaki 1988;Blackman and Eastop 1994;Eastop and Blackman 2005;Blackman and Eastop 2006). It has been recorded on Pyrus x bretschneideri Rehder, Pyrus communis L., Pyrus pyrifolia (Burm. Fil.) Nakai and Pyrus ursuriensis Maxim. (Blackman and Eastop 1994;Holman 2009). Th ere are also records on Prunus persica (L.) Batsch in Japan (Higuchi and Miyazaki 1969;Moritsu 1983) which we believe should be confi rmed. Based on all of these data, this is the fi rst record of an aphid species on P. calleryana (Fig. 1).
In spring in Spain, colonies of this species cause the leaves of P. calleryana to curl (Fig.  1B) as occurs in Pyrus pyrifolia in Japan, Korea and China (Essig and Kuwana 1918), and are attended by the ant Tapinoma nigerrimum (Nylander). Th e fundatrices appear at the beginning of April and the alatae leave the primary host in mid June to colonize their secondary hosts. Eff orts to locate the virginogeniae in these hosts in summer, or alatae re-migrating to the primary hosts in autumn, have so far produced no results.

Damage to the host plant
Th e direct action of sucking by the aphids (clearly seen in the curling of the leaves), and indirect damage caused by the honeydew they excrete, which covers the leaves, can aff ect the normal growth of the trees, all the more so if other aphid species (Aphis pomi De Geer 1773 and Dysaphis sp.) sometimes forming mixed colonies with S. piricola, are present.
Th e trees of Pyrus calleryana in "Juan Carlos I park" (Barajas, Madrid, Spain), which have been monitored more carefully, were planted two years ago and do not seem to have reached the height and size expected for this species. In any case, a more in-depth study of the population dynamics and auxiliary fauna (coccinellidae, syrphids, etc…) is necessary, taking into account other variables (humidity, temperature, etc…), to be able to reach conclusions on possible damage.

Identification keys
Th e following keys enable all the species in the subgenus Schizaphis recorded in the Iberian Peninsula to be separated.