Allocotaphis quaestionis (Börner, 1942)

Stekolshchikov, Andrey V. & Qiao, Ge-Xia, 2023, Revision of the genus Allocotaphis Börner, 1950 (Hemiptera, Homoptera, Aphididae, Macrosiphini), Zootaxa 5227 (1), pp. 63-99 : 79-92

Allocotaphis quaestionis (Börner, 1942)

( Figs. 39–64 , Tabl. 3–4 )

Neanuraphis quaestionis B̂rner, 1942: 260 [ Szelegiewicz 1968: 125; Eastop & Hille Ris Lambers 1976: 21; Remaudière & Remaudière 1997: 69; Zhang et al. 1999: 346]

Allocotaphis quaestionis (B̂rner, 1942) in B̂rner 1950: 4 [B̂rner 1952: 97; Weis 1955: 507; B̂rner & Franz 1956: 341; B̂rner & Heinze 1957: 140; Hille Ris Lambers & Wildbolz 1958: 317; Shaposhnikov 1964: 585; Szelegiewicz 1968: 125; Lampel 1975: 129; Lampel 1976: 199; Eastop & Hille Ris Lambers 1976: 21; Herczek et al. 1977: 77; Szelegiewicz 1978: 21; Tashev 1984: 26; Tashev 1985: 106; Czylok et al. 1988: 106; Nast et al. 1990: 113; Holman 1991: 21; Remaudière & Remaudière 1997: 69; Ben Halima-Kamel & Ben Mabrouk 1998: 55; Zhang et al. 1999: 347; Węgierek & Wojciechowski 2004: 255; Osiadacz & Hałaj 2010: 70; Ben Halima-Kamel 2012: 4]

Malaphis magna Shaposhnikov, 1951: 517 [ Mamontova 1955: 10; Shaposhnikov 1956: 283; Hille Ris Lambers & Wildbolz 1958: 317; Tashev 1959: 250; Szelegiewicz 1968: 125; Lampel 1976: 199; Eastop & Hille Ris Lambers 1976: 21; Remaudière & Remaudière 1997: 69]

Malachis magna Grigorov, 1980: 49 , double misprint for Malaphis Shap [oshnikov]

Material examined. Lectotype of Malaphis magna Shaposhnikov, 1951 (here designated to fix clearly the status of the taxon name): fundatrix, No. 2183 (collection number of ZIN RAS) (right specimen in lower row); label: “2183, Malaphis magna Shap., VI 51, G.Sh., fun., Morshin, 20. V.51, Malus sp. , In roll[ed] l[eaves]. Gr[een] with trans[verse] gr[een] strip[es]. With we[ak] whi[te] pulv[erulence].”; on cover glass: “Typus”. Paralectotypes of Malaphis magna Shaposhnikov, 1951 : one male, 16.x.1913, Georgia, Kakheti, Lagodekhi Municipality, Lagodekhi, Malus domestica Borkh. ; four gynoparae, 3.x.1949, Ukraine, Lviv Region, Morshyn, M. domestica ; one male, 3.x.1949, Ukraine, Lviv Region, Morshyn, M. domestica ; three gynoparae, six males, 6–15.x.1949, Ukraine, Lviv Region, Morshyn, M. domestica ; four oviparous females, 9.x.1949, Ukraine, Lviv Region, Morshyn, M. domestica ; three gynoparae, five males, six oviparous females, 19.x.1949, Ukraine, Lviv Region, Morshyn, M. domestica ; six gynoparae, seven males, six oviparous females, 26.x.1949, Ukraine, Lviv Region, Morshyn, Malus sp. ; four gynoparae, 23.ix.1949, Russia, Stavropol Krai, Predgorny District, Podkumok Vill., Malus sp. ; three fundatrices, one emigrant, 18.v.1951, Ukraine, Lviv Region, Morshyn, Malus sp. ; two fundatrices, five emigrants, from the same host plant, locality and the same data as lectotype; seven emigrants, 5.vi.1951, Ukraine, Lviv Region, Stryi Raion, Skole, Malus sp. Lectotype and all paralectotype from collections of ZIN RAS. Additional materials: three gynoparae, 13.x.1951, Russia, Karachay-Cherkess Republic, Karachayevsky District, Dombay Polyana, Malus sp. (from collections of ZIN RAS); 16 gynoparae, six oviparous females, 16–18.x.1951, Russia, Karachay-Cherkess Republic, Teberda Nature Reserve, Malus sp. (from collections of ZIN RAS); four gynoparae, 17.x.1951, Russia, Karachay-Cherkess Republic, Karachayevsky Urban Okrug, Teberda, Malus sp. (from collections of ZIN RAS); one gynopara, 4.x.1953, Georgia, Samtskhe-Javakheti, Borjomi, Malus orientalis Uglitzk. ex Juz. (from collections of ZIN RAS); 30 gynoparae, 11 males, one oviparous female, 18.x.1953, Georgia, Samtskhe-Javakheti, Borjomi, Malus sp. (from collections of ZIN RAS); one fundatrix, 16.v.1954, Russia, Republic of Adygea, Maykopsky District, Shuntuk, Malus sp. (from collections of ZIN RAS); 19 emigrants, 2.vi.1954, Russia, Republic of Adygea, Maykopsky District, Shuntuk, M. orientalis (from collections of ZIN RAS); five fundatrices, 17 emigrants, 20– 24.v.1955, Russia, Republic of Adygea, Maykopsky District, Shuntuk, M. orientalis (from collections of ZIN RAS); nine fundatrices, 69 emigrants, 26.v.1955, Russia, Republic of Adygea, Maykopsky District, Kamennomostsky (Khadjokh), M. domestica (from collections of ZIN RAS); one gynopara, one male, 16.x.1956, Czech Republic, Prague, Botanical Garden, Malus sylvestris (L.) Mill. (from collections of ZIN RAS); 1 gynopara, 1.x.1971, Czech Republic, Prague, Botanical Garden, Malus pumila Mill. (from collections of ZIN RAS); two apterous viviparous females, 14.viii.1986, Poland, Subcarpathian Voivodeship, Bieszczady Mountains, Terebowiec, Senecio nemorensis (from collections of DZUS); four gynoparae, 26.ix.1995, Russia, Krasnodar Krai, Sochi, Lazarevskoye Microdistrict, Malus sp. (from collections of ZIN RAS); two gynoparae, 24 oviparous females, 6–16.x.1995, Russia, Krasnodar Krai, Sochi, Lazarevskoye Microdistrict, Malus sp. (from collections of ZIN RAS); seven gynoparae, 35 oviparous females, 6–18.ix.2005, Russia, Orenburg Region, Gaysky District, Khmelyovka Vill., Malus sp. (from collections of ZIN RAS). Also used data from Shaposhnikov (1951).

Etymology. The specific name “ quaestionis ” (genitive singular feminine of the Latin words “ quaestiô ”) means as “under doubts”, “questioned”, and refers to the lack of knowledge about the species at the time of its description.

The apterous viviparous female is described in greatest detail. For the other morphs, the differences from the apterous vivipara or, for the alate morph, from the emigrant are pointed out.

Description. Fundatrix ( Figs. 39–47 ). Body almost rounded, 1.2–1.4 times as long as wide. Color when alive green, pale green or pale yellow-green, with dark green bands on the dorsal side of the body, which are interrupted in the middle on the metanotum and abdominal tergites I–IV; head green-gray, apices of antennae, tibiae and tarsi dark brown, siphunculi green, dark brown in apical half, shiny, anal plate and cauda pale brown-green; body with waxy pulverulence. Cleared specimens with apices of penultimate antennal segment, last antennal segment, ultimate rostral segments, apices of tibiae, tarsi and the very apices of the siphunculi brown; siphunculi (except the very apices), subgenital and anal plates, cauda and rarely band on abdominal segment VIII light-brown. Body not sclerotized, except for a sometimes occurring very pale brown band on abdominal tergite VIII. Setae on the whole body and appendages mostly finely pointed, only those on last antennal segment sometimes simply pointed or blunt. Antennae 5- or, rarely, 6-segmented, without secondary rhinaria. Rostrum reaching pro- or mesothorax. Ultimate rostral segment wedge-shaped, 1.9–2.7 times as long as its basal width. Legs shortened. Peritremes on abdominal segments I and II separated by a distance more than diameter of peritreme. Siphunculi slightly conical, sometimes close to bottle-shaped (almost cylindrical in the basal half, then tapering and again almost cylindrical at the apex).

Emigrants ( Figs. 48–56 ). Body elliptical or elongate elliptical, 1.8–2.5 times as long as wide. Color when alive green, with rust-brown thorax, black head, dorsal abdominal patch, antennae and siphunculi, legs yellow-brown, cauda pale green. Cleared specimens with head, sclerotized bands and macula on thorax and abdomen, antennal segments I–V (except base of antennal segment III) and base of antennal segment VI, coxae, distal three-quarters of femora and siphunculi dark brown; processus terminalis, ultimate rostral segments, tibia, tarsi, subgenital and anal plate brown; base of antennal segment III, trochanters, basal one-quarter of femora and cauda light-brown.Abdomen with large marginal sclerites, large muscle plates and rare small spinal sclerites on abdominal tergites I–II, bands and marginal sclerites on tergites III–VII fused into solid patch, transverse band on abdominal tergite VIII, and mediumsized sclerites at the edges of sternites IV–VII. Surface of head, thoracic dorsum and abdominal tergites I–VI smooth, sometimes weakly wrinkled, with very sparse small pointed spinules only on marginal sclerites on anterior abdominal segments; surface of abdominal tergite VII with rows of small smoothed spinules, which on tergites VIII partially fuse to form scales . Setae on antennae blunt, weakly capitate or finely pointed. Head without traces of epicranial suture. Antennal tubercles distinct, relatively high, median tubercle low but conspicuous. Antennal segment III with 43–86 secondary rhinaria spaced evenly along the segment, segment IV with 15–44 and segment V with 13–32. Rostrum reaching metathorax–abdominal segment II. Ultimate rostral segment 2.1–3.2 times as long as its basal width. Peritremes on abdominal segments I and II often fused.

Apterous viviparous female ( Figs. 57–65 ). Body elliptical, 1.7 times as long as wide. Color when alive unknown. Cleared specimens with head, sclerotized bands and shield on thorax and abdomen, antennal segments I–V (except base of antennal segment III) and base of antennal segment VI, coxae, distal three-quarters of femora, bases of tibia, siphunculi and subgenital plate dark brown; processus terminalis, III and ultimate rostral segment, tibia (except bases), tarsi, anal plate brown; base of antennal segment III, trochanters, basal one-quarter of femora and cauda light-brown. Dorsal surface of the thorax and abdomen is completely sclerotized, bands on the meso- and metathorax and abdominal tergites I–VII, marginal sclerites and peritremes on segments I–VII, as well as large sclerotized sclerites on abdominal sternites IV–VII fused into a single shield, only on border of mesothorax and metathorax cuticle somewhat lighter, slightly less sclerotized; prothorax and abdominal tergite VIII with transverse band. Surface of head, thoracic dorsum and abdominal tergites I–VII smooth, sometimes weakly wrinkled, with very sparse small pointed spinules; surface of abdominal tergite VIII with rows of smoothed partially fused spinules; cuticle on ventral side of abdomen smooth, only sternite VII and subgenital plate with sparse long rows of very small pointed spinules. Setae on the whole body and appendages finely pointed. Head with distinct traces of epicranial suture.Antennal tubercles distinct, but not high, median tubercle inconspicuous.Antennae 6-segmented, antennal segment III with 3–8 secondary rhinaria located at the very apex of the segment, segment IV with 27–32 and segment V with 22–27; external diameter of secondary rhinaria 2.0–2.9 times as long as high. Rostrum reaching abdominal segment III. Ultimate rostral segment elongated wedge-shaped, 2.6–2.8 times as long as its basal width. Peritremes on abdominal segments I and II separated by a distance less than diameter of peritreme. Siphunculi straight or very weakly curved outwards, cylindrical, slightly tapering towards apex, without setae. Cauda rounded, escutcheon-shaped.

Gynopara ( Figs. 66–74 ). Color when alive brown, greenish-brown, yellowish-brown or with rusty-yellow thorax and green abdomen, glistening; head, sclerites of thorax and abdomen, antennae, femora (except base), apices of tibiae, tarsi and siphunculi black, cauda pale gray or dirty green. Patch on abdominal tergites III–VI often with numerous transparent “windows” and sometimes divided into separate bands, which can be interrupted in the middle; band on abdominal tergite VII never fused with patch. Third antennal segment with 99–147, segment IV with 38–90 and segment V with 18–55 secondary rhinaria. Ultimate rostral segment 2.2–4.0 times as long as its basal width. Surface of siphunculi covered with thin and wide scales formed by partially fused strongly smoothed spinules.

Male ( Figs. 75–83 ). Alate. Body elongate elliptical, 2.2–3.0 times as long as wide. Living specimens with pale rusty brown thorax and abdomen, sometimes the abdomen is dirty green; head, sclerites on thorax, bands on abdomen, antennae, legs and siphunculi black, cauda pale. Abdomen with bands on all tergites, which are almost always interrupted in the middle on tergites I–III, sometimes band on tergite IV is also interrupted; bands on tergites V–VI or very rarely on tergites IV–VI sometimes fused into a strongly interrupted patch with numerous transparent “windows”. Antennal segment III with 106–156, segment IV with 38–77 and segment V with 19–43 secondary rhinaria. Rostrum reaching mesothorax—abdominal segment III. Ultimate rostral segment 2.1–4.3 times as long as its basal width. Cauda escutcheon-shaped.

Oviparous female ( Figs. 84–93 ). Body elliptical, sometimes broadly elliptical 1.5–2.0 times as long as wide. Color when alive yellowish green, greenish yellow, greenish brown, brownish yellow or green, dull glistening; transverse bands on thorax and abdomen gray or pale gray, antennae (except base and processus terminalis), legs (except base of femora) and siphunculi gray or dark gray, rarely almost black, tarsi black. Cleared specimens with head, sclerotized bands on abdomen, peritremes, antennae (except base of antennal segment III), ultimate rostral segments, coxae, femora (except base), tibia, siphunculi (except base), anal and subgenital plate brown; base of antennal segment III, trochanters, base of femora, tibia, base of siphunculi and cauda light brown. Abdomen with sclerotized bands on tergites VII–VIII and peritremes on all segments; band on tergite VII sometimes interrupted in the middle. Antennal tubercles very low, median tubercle inconspicuous. Antennae 6- or sometimes 5-segmented, without secondary rhinaria. Rostrum reaching mesothorax—abdominal segment II. Ultimate rostral segment 1.7–2.5 times as long as its basal width. Chaetotaxy of first tarsal segments 2, 2, 2 in many individuals, but often on one or more fore and middle tarsi first segment with 3 setae, up to 3, 3, 2. Siphunculi cylindrical, slightly tapering towards the apex. Cauda rounded escutcheon-shaped, almost semicircular. Hind tibiae more or less distinctly swollen with 6–213 (on average 71.5–162.8 in different populations) round or oval pheromone plates, more of them located on basal half.

Systematic relationships. The differences between A. quaestionis and known morphs of other species of the genus given in the key.

Distribution. Germany: State of Hessen, Dachsloch; Bavaria, Buchstein Mt. (B̂rner 1950, 1952; Weis 1955; B̂rner & Franz 1956). Austria: Styria, Admont and Dürrenscĥberl; Upper Austria, Enns and Ried im Innkreis (B̂rner 1942, 1952; Weis 1955; B̂rner & Franz 1956). Switzerland: Grisons, Arosa (Maran); Fribourg, Fribourg ( Hille Ris Lambers & Wildbolz 1958; Lampel 1975, 1976). Poland: Masurian Lakeland; Silesian Voivodeship, Brenna; Subcarpathian Voivodeship (B̂rner 1950, 1952; Szelegiewicz 1968, 1978; Czylok et al. 1988; Nast et al. 1990). Czech Republic: Prague ( Holman 1991). Bulgaria: Sofia Province, Selimitsa Peak ( Tashev 1959, 1985; Grigorov 1980). Ukraine: Lviv Oblast, Morshyn and Skole ( Shaposhnikov 1951, 1956). Russia: Republic of Adygea, Shuntuk and Kamennomostsky; Karachay-Cherkess Republic, Teberda; Stavropol Krai, Podkumok Vill. ( Shaposhnikov 1951, 1956; Mamontova 1955). Georgia: Kakheti, Lagodekhi ( Shaposhnikov 1951, 1956). Tunisia: Sousse, Chott Meriem ( Ben Halima-Kamel & Ben Mabrouk 1998; Ben Halima-Kamel 2012).

Kadyrbekov (2017) found three alate and five apterous viviparous females in leaf galls on Malus sieversii (Ledeb.) M.Roem. in Kyzylauyz Gorge (4.vi.2010, Altyn-Emel National Park, Almaty Region, Kazakhstan), which he identified like A. quaestionis . Describing the biology of the species, Kadyrbekov pointed out that A. quaestionis is not a migrating species, apparently based on the presence of apterous females on Malus . In fact, A. quaestionis has a dioecious life cycle, and apterous forms in its second and subsequent generations have never been found on a woody plant; there is some doubt on the reliability of the identification of material from Kazakhstan and thus this territory may not be in the species range.

Biology. The primary hosts of A. quaestionis are various species of the genus Malus ( M. domestica , M. sylvestris , M. fusca (Raf.) C.K.Schneid. , M. orientalis , M. pumila , Malus sp. ) ( Shaposhnikov 1951, 1956; Weis 1955; B̂rner and Franz 1956; Tashev 1959; Szelegiewicz 1968; Herczek et al. 1977; Holman 1991; Blackman & Eastop 2022). Adult fundatrices inside rolled-up leaves of Malus were observed in the Carpathians already in early May ( Shaposhnikov 1951, 1956). Later, fundatrices and nymphs of emigrants feed at the base of the central vein on the lower surface of the leaf and on the petiole of the leaf, which causes the petiole to twist, and the leaf is twisted rather strongly across or obliquely and often wrinkled. Usually, the entire rosette of leaves is damaged, mainly on stem shoots. In the Carpathians and the Alps, the entire second generation migrates completely from the apple tree in late May—early June ( Shaposhnikov 1951, 1956; Hille Ris Lambers & Wildbolz 1958), while in Bulgaria (Selimitsa Peak) at an elevation of 1300 meters above sea level in early June on Malus there were only fundatrices and nymphs of emigrants.

All individuals of the second generation are emigrants that migrate to the species of the genus Senecio ( S. doronicum , S. nemorensis ) and live there on the root collar and underside of the leaves ( Hille Ris Lambers & Wildbolz 1958; Czylok et al. 1988; Blackman & Eastop 2022). Szelegiewicz (1968) also lists Doronicum as the secondary host of A. quaestionis , without, however, providing any actual confirmation of these data. It is very likely that this is simply a consequence of an error when the specific epithet in the name Senecio doronicum was accidentally interpreted as the name of an existing genus.

Remigration to Malus begins in the Orenburg region ( Russia) in late August—early September, in the Lviv region of Ukraine, Austria, Switzerland, the Czech Republic, the Krasnodar Krai of Russia, the North Caucasus and Georgia a month later—from late September to mid-October ( Shaposhnikov 1951, 1956; B̂rner 1942; B̂rner & Franz 1956; Hille Ris Lambers & Wildbolz 1958; Lampel 1975, 1976; Holman 1991). Gynoparae lay their larvae usually at the base of the leaf blade, while they themselves often sit on the base of the petiole. Oviparous females from birth to adult stay on the leaves in a small but dense colony. By the time oviparous females become adults (about 7–10 days after birth), males appear in the colony and, after mating, females move to the shoot bark.

Figures

FIGURE 39. Fundatrix of Allocotaphis quaestionis (B̂rner, 1942), habitus.

FIGURES 40–47. Allocotaphis quaestionis (B̂rner, 1942), fundatrix. 40, antennae; 41, antennal segment III; 42, antennal segment VI; 43, head; 44, ultimate rostral segment; 45, hind tarsus; 46, siphunculus; 47, cauda.

FIGURE 48. Emigrant of Allocotaphis quaestionis (B̂rner, 1942), habitus.

FIGURES 49–56. Allocotaphis quaestionis (B̂rner, 1942), emigrant. 49, antennae; 50, antennal segment III; 51, antennal segment VI; 52, head; 53, ultimate rostral segment; 54, hind tarsus; 55, siphunculus; 56, cauda.

FIGURE 57. Apterous viviparous female of Allocotaphis quaestionis (B̂rner, 1942), habitus.

FIGURES 58–65. Allocotaphis quaestionis (B̂rner, 1942), apterous viviparous female. 58, antennae; 59, antennal segment III; 60, antennal segment VI; 61, head; 62, ultimate rostral segment; 63, hind tarsus; 64, siphunculus; 65, cauda.

FIGURE 66. Gynoparae of Allocotaphis quaestionis (B̂rner, 1942), habitus.

FIGURES 67–74. Allocotaphis quaestionis (B̂rner, 1942), gynoparae. 67, antennae; 68, antennal segment III; 69, antennal segment VI; 70, head; 71, ultimate rostral segment; 72, hind tarsus; 73, siphunculus; 74, cauda.

FIGURE 75. Male of Allocotaphis quaestionis (B̂rner, 1942), habitus.

FIGURES 76–83. Allocotaphis quaestionis (B̂rner, 1942), male. 76, antennae; 77, antennal segment III; 78, antennal segment VI; 79, head; 80, ultimate rostral segment; 81, hind tarsus; 82, siphunculus; 83, cauda.

FIGURE 84. Oviparous female of Allocotaphis quaestionis (B̂rner, 1942), habitus.

FIGURES 85–93. Allocotaphis quaestionis (B̂rner, 1942), oviparous female. 85, antennae; 86, antennal segment III; 87, last antennal segment; 88, head; 89, ultimate rostral segment; 90, hind tibia; 91, hind tarsus; 92, siphunculus; 93, cauda.