Neoceruraphis viburnicola ( Gillette, 1909 )

Stekolshchikov, Andrey V., 2022, Revision of the genus Neoceruraphis Shaposhnikov, 1956 (Hemiptera: Aphididae), Zootaxa 5159 (1), pp. 23-63 : 44-58

Neoceruraphis viburnicola ( Gillette, 1909)

( Figs. 40–73 ; Tabl. 4–5 )

Aphis viburnicola Gillette, 1909: 280 [ Davis 1910: 492; Gillette & Bragg 1915: 102; Gillette & Bragg 1918: 329; Guyton 1924: 14; Hottes 1931: 64; Hottes & Frison 1931: 223; Gillette & Palmer 1932: 452; Burnham 1938: 187; Knowlton 1941: 67; Palmer 1952: 184]

Aphis viburnum Scopoli in Wilson 1910: 29

Anuraphis viburnicola ( Gillette, 1909) in Patch 1923: 298 [ Cutright 1925: 192; Leonard 1963: 66]

Ceruraphis viburnicola ( Gillette, 1909) in Börner 1926: 226 [ Shaposhnikov 1950: 215; Börner 1952: 96; Börner & Heinze 1957: 139; Eastop & Hille Ris Lambers 1976: 133; Smith & Parron 1978: 74; Robinson 1979: 25; Chakrabarti & Medda 1985: 129; Smith & Eckel 1996: 49; Remaudière & Remaudière 1997: 86; Zhang & Chen 1999: 267; Maw et al. 2000: 18; Kaygin et al. 2010: 2]

Yezabura (Ceruraphis) eriophori ( Walker, 1848) in Börner & Schilder 1932: 585

Neoceruraphis viburnicola ( Gillette, 1909) in Shaposhnikov 1956: 285 [ MacGillivray 1960: 704; Gittins et al. 1976: 20]

Material. 1 fundatrix, 6 emigrants, 11.vi.1909, USA, Colorado, Fort Collins, Viburnum sp. (metatype) (from collection of ZIN RAS); 1 male, 6 gynoparae, 12.x.1913 and 22.x.1913, USA, Colorado, Fort Collins, Viburnum opulus (from collection of MNHN); 1 emigrant, 24.v.1927, USA, Utah, Providence, Viburnum opulus (from collection of MNHN); 1 fundatrix, 6 emigrants, 6.vi.1938, USA, Colorado, Fort Collins, Viburnum opulus (from collection of NHM); 3 fundatrices, 21.iv.1957, USA, Utah, Moab, Viburnum sp. (from collection of NHM); 2 emigrants, 22.v.1958, USA, Utah, Brigham City, Viburnum opulus (from collection of NHM); 2 emigrants, 19.vi.1958, Canada, New Brunswick, Kingsclear, Viburnum trilobum Marshall (from collection of ZIN RAS); 3 gynoparae, 1 male, 3.x.1958, USA, Utah, Providence, taken flying (from collection of NHM); 1 male, 15.x.1958, USA, Utah, Logan Canyon, sweeping (from collection of NHM); 2 fundatrices, 26.v.1960, Canada, New Brunswick, Fredericton, Viburnum trilobum (from collection of ZIN RAS); 4 apterous viviparous females, 27.vi.1960, Canada, New Brunswick, Fredericton, Carex sp. (in culture) (from collection of ZIN RAS); 1 gynopara, 1 male, 21.x.1960, Canada, New Brunswick, Fredericton, Viburnum sp. (from collection of ZIN RAS); 3 gynoparae, 24.ix.1964, USA, Utah, Logan, taken flying (from collection of NHM); 1 emigrant, 17.vi.1965, USA, Manitoba, Winnipeg, Viburnum lentago L. (from collection of NHM); 1 gynopara, 16.x.1965, USA, Iowa, Ames, suction trap (from collection of MNHN); 6 emigrants, 5.vi.1966, USA, Pennsylvania, State College, Viburnum opulus (from collection of NHM); 10 gynoparae, 26.viii.1976, Canada, Québec, Saint-Gédéon, Viburnum sp. (from collection of MNHN); 9 gynoparae, 9 and 15.ix.1976, USA, Maine, Orono, Viburnum opulus and Viburnum sp. (from collection of MNHN); 1 gynopara, 13 oviparous females, 2.xi.1976, USA, Maine, Orono, Viburnum sp. (from collection of MNHN); 1 oviparous female, 31.x.1977, Canada, British Columbia, Vancouver, Viburnum trilobum (from collection of MNHN); 2 emigrants, 7.vi.1984, USA, Utah, Logan, Viburnum sp. (from collection of MNHN); 1 emigrant, 6.v.1986, USA, Idaho, Notus, Viburnum sp. (from collection of MNHN); 8 emigrants, 26 and 29.vi.1984, USA, Utah, Logan, Viburnum sp. (from collection of MNHN); 1 gynopara, 29.ix.1989, USA, Manitoba, Winnipeg, Kings Drive Park, Viburnum sp. (from collection of MNHN). Also used data from Gillette (1909), Gillette & Palmer (1932), Palmer (1952) and MacGillivray (1960).

Etymology. The name viburnicola derived from the generic name of host-plant “ Viburnum ” and the ending “- cola ” stand for “inhabitant of”. Gender: feminine.

Description. Fundatrix. Body broadly elliptical, sometimes almost round, 1.3–2.4 times as long as its width. Bluish white, due to the entire body, except the terminal segment of the abdomen, being covered with a white powder; without powder from light green to deep green; distal half of antennae (including processus terminalis), two last segments of rostrum, tibiae, tarsi, siphunculi, anal and genital plates and cauda dusky to black; distal halves of middle and hind femora dusky. Cleared specimens with basal halves of tibia almost black, two last segments of the antennae (or the apex of third and last segment in 4-segmented antennae), apices of fore femora, distal halves of middle and hind femora, distal halves of tibia, tarsi and siphunculi dark brown, antennae (except for the last two segments), last two segments of rostrum, sclerites and bands on tergites of the abdomen and peritremes, the subgenital and anal plates and cauda brown, head, coxae, trochanters, basal halves of fore and bases of middle and hind femora light brown. Dorsal surface of thorax and abdomen almost not sclerotized, sclerotized only rare small sclerites on abdominal tergites I–VII, band on tergite VIII, small marginal sclerites on segments I–VII and peritremes; sclerites on tergite VII sometimes grouped together in strongly interrupted band. Surface of dorsal side of head smooth, of ventral side of head with sparse pointed spinules; on dorsal side of thorax and abdominal tergites I–VI smooth, on marginal sclerites on abdominal segment VII with rows of large pointed spines; on tergite VII with rows of small pointed spinules which on tergite VIII partially fused and forming short scales; surface of ventral side of thorax smooth, of abdomen with long rows of small pointed spinules sometimes forming strongly stretched cells.

Marginal tubercles always present on pro-, meso- and metathorax and on abdominal segments II–IV, tubercles are absent on other body segments; total number of marginal tubercles on whole body—8–12. Spinal tubercles sometimes present on abdominal tergite VII. Setae on the whole body and appendages are finely pointed, except tibia, where some of setae pointed, but not finely pointed. Chaetotaxy of first tarsal segments 3,3,3. Head with weak traces of epicranial coronal suture or without such traces. Antennae 5-segmented or rarely 4-segmented as a result of fusing of 3rd and 4th segments or 3rd, 4th and 5th segments; antennae without secondary rhinaria. Rostrum reaching mesothorax; ultimate rostral segment short wedge-shaped with slightly concave edges. Legs shortened. Spiracles rounded reniform. Peritremes on abdominal sternites I and II separated by a distance more than diameter of peritreme. Siphunculi without setae. Cauda elongated escutcheon-shaped. Hind tibiae not noticeably swollen and with 7–17 pheromone plates on apices.

Alatae viviparous female (emigrant). Body egg-shaped, 1.8–2.3 times as long as its width. Head and thorax black, abdomen pale greenish yellow with dusky to blackish green lateral areas and dorsal bands; antennae, legs (except proximal ends of femora), rostrum, siphunculi, and anal and genital plates dusky to black; cauda pale to dusky. Cleared specimens with head, thorax, antennae (except processus terminalis of last antennal segment), distal halves of fore femora, middle and hind femora (except base), bases and apices of tibia (less often the whole tibia), tarsi and siphunculi dark brown; two last segment of rostrum, middle parts of tibiae, sclerites and bands on tergites and sternites of abdomen, marginal sclerites and peritremes on abdominal segments I–VII and subgenital and anal plates brown; processus terminalis, coxae, trochanters, basal halves of fore femora, base of middle and hind femora and cauda light-brown. Abdominal dorsum with sclerotized bands on all tergites and large marginal sclerites on segments I–VII; band on tergite I thin, sometimes divided into large separate sclerites; bands on tergites II–VII and marginal sclerites on segments V–VII fused in a sclerotized shield on which sometimes present a membranous area on the boundary between tergites; band on tergite II fused with sclerotized shield anterolaterally with a membranous area on the boundary between tergites II and III. Ventral side of abdomen with paired sclerotized maculae located along margins of sternites II–VI. Surface of dorsal side of head smooth, of ventral side of head with sparse pointed spinules; on the pronotum with large pointed spines, sometimes sparse, and sometimes located more or less along the contour of the cell; on the mesonotum and metanotum and on the ventral side of the thorax smooth; on abdominal tergites I–VI with large pointed spines, rare on the anterior tergites and more frequent on the posterior ones, where they form a more or less distinct cellular structure; on tergite VII cells begin to disintegrate, spines slightly smoothed out and forming short rows and on tergite VIII spines partially fused and forming short scales; marginal sclerites on tergites I–VII with rows of large pointed spines forming cellular structure; surface of ventral side of abdomen with long rows of small pointed spinules sometimes forming strongly stretched reticulate cells and spinules are expressed more clearly on sclerotized areas. Marginal tubercles always present on prothorax and abdominal segments I–IV; total number of marginal tubercles on whole body—8–10; they protuberant up to semicircular or papilliform, diameter of tubercles 1.1–2.6 times as long as high. Spinal tubercles always present on abdominal tergite VII and very rare also on tergite VI. Setae on the antennae, dorsal side of head, thorax, legs and on abdominal tergites I–V pointed or finely pointed, on abdominal tergites VI–VIII, on ventral side of head and body, rostrum, subgenital and anal plates and cauda finely pointed. Chaetotaxy of first tarsal segments 4,4,4, only rarely on one leg first tarsal segments with 3 or 5 setae. Head with or without weak traces of epicranial coronal suture, frontal tubercles are low, but distinct, median tubercle not reaching the level of antennal tubercles. Antennae 6-segmented and only small part of individual have one 5-segmented antenna as a result of fusing of 3rd and 4th segments; 3rd antennal segment with 8–28 secondary rhinaria spaced evenly along the segment, 4th segment with 0–8 and 5th segments with 0–3 secondary rhinaria. Secondary rhinaria elliptical or rounded, protuberant, with a domed swollen membrane surrounded by a sclerotized ridge and with external diameter 2.0–6.8 times as long as high of rhinaria. Rostrum reaching mesothorax—abdominal segment I; ultimate rostral segment elongated wedge-shaped with slightly concave margines. Peritremes on abdominal sternites I and II touching or fused and only rarely separated by a distance less than diameter of peritreme. Siphunculi without setae. Cauda escutcheon-shaped or elongated escutcheon-shaped. Hind tibia with 7–51 pheromone plates, they are round, protuberant from slightly convex to hemispherical.

Apterous viviparous female (exules). Body egg-shaped, 1.6–1.8 (1.7) times as long as its width. Body in life slightly powdery; newly developed adult with deep-pink head and cream-coloured abdomen; older adult with pink head, brownish dorsally and pink ventrally on abdomen. Cleared specimens with antennae (except processus terminalis), distal halves of fore femora, middle and hind femora (except base), bases and apices of tibia, tarsi and siphunculi dark brown; head, two last segment of rostrum, coxae, middle parts of tibiae, sclerites and bands on dorsal surfaces of thorax and abdomen, marginal sclerites and peritremes on abdominal segments I–VII, subgenital and anal plates and cauda brown; processus terminalis, trochanters, basal halves of fore femora, base of middle and hind femora light-brown. Dorsal surface of thorax and abdomen is almost completely sclerotized, bands and marginal sclerites on meso-, metathorax, and abdominal tergites I–VII fuse into a single shield; band on prothorax always fused with marginal sclerites; ventral surface of thorax and abdomen not sclerotized. Surface of head with rows of pointed spines sometimes forming indistinct cells, on the dorsal side of thorax and abdominal tergites I–VI reticulate, contours of cell are formed by pointed spines, with several spinules of the same type inside each cell, on tergite VII with rows of smoothed out spinules, which on tergite VIII partially fused and forming short scales; surface of ventral side of abdomen with long rows of small pointed spinules sometimes forming strongly stretched reticulate cells. Marginal tubercles always present on prothorax and abdominal segments I–IV and sometimes also on segment V; total number of marginal tubercles on whole body—10; they weakly protuberant, almost flat, diameter of tubercles 3.5–4.2 times as long as high. Small spinal tubercles sometimes present only on abdominal tergite VII. Setae on antennae, dorsal side of the head and thorax, and on abdominal tergites I–VI pointed; on legs pointed or finely pointed; on abdominal tergites VII–VIII, on ventral side of head, thorax and abdomen, rostrum, subgenital and anal plates and cauda finely pointed. First segments of tarsi with 3 or 4 setae. Head with weak traces of epicranial coronal suture, frontal tubercles almost not developed, frons almost flat. Antennae 6-segmented and only one individual has one 5-segmented antenna as a result of fusing of 3rd and 4th segments; 3rd antennal segment with 0–4 secondary rhinaria located in basal third of segment, 4th–5th segments without secondary rhinaria. Rostrum reaching mesothorax—abdominal segment II; ultimate rostral segment elongated wedge-shaped. Legs normal. Spiracles reniform. Peritremes on abdominal sternites I and II separated by a distance less than diameter of peritreme. Siphunculi are cylindrical or elongated-conical, without setae. Cauda escutcheon-shaped with a slight constriction at base, apex of cauda is in the form of a tubercle, slightly separated by a weak constriction and slightly less sclerotized than the rest of cauda. Hind tibia slightly wider than other tibiae, with 35–79 round, slightly convex pheromone plates on distal three-quarters.

Gynopara. Body egg-shaped, 1.9–2.3 times as long as its width. Head and mesothorax black, prothorax dusky brown, abdomen rusty brown at base, with darker transverse bands towards siphunculi, and is nearly or quite black upon the middle of dorsal portion; antennae, distal halves of femora, tibiae, tarsi, siphunculi, subgenital and anal plates black, rostrum dusky brown. Cleared specimens with distal halves of tibia dark brown and with coxae and basal halves of tibia brown. Band on abdominal tergite II very rarely fused anterolaterally with sclerotized shield on tergites III–VII. Paired sclerotized maculae located along margines of sternites II–VI are connected to each other by rows of small sclerites in such a way that strongly interrupted in the middle bands are formed. Surface of marginal sclerites with large pointed spines, located without a definite structure. Marginal and spinal tubercles absent.

Median frontal tubercle sometimes reaching the level of antennal tubercles. Third antennal segment with 20–37 secondary rhinaria spaced evenly along the segment, 4th segment with 0–13 and 5th segments with 0–6 secondary rhinaria. Rostrum reaching mesothorax. Hind tibia not noticeably swollen and with 0–21 pheromone plates.

Male. Alate. Body elongate elliptical, 2.1–3.0 times as long as its width. Head, thorax, antennae, legs (except bases of femora), siphunculi, anal and subgenital plates black, abdomen rusty brown, cauda dusky. Dorsal surface of abdomen with sclerotized bands on all tergites not uniting into a single shield and with large marginal sclerites on segments I–VII; bands on tergites I–II almost broken in the middle; marginal sclerite and band on segment VII always fused. Surface of marginal sclerites with large pointed spines located without a definite structure on segments I–V and grouped in rows on segments VI–VII. Marginal tubercles sometimes present on prothorax, spinal tubercles absent. First segments of tarsi with 3 or 4 setae. Head without traces of epicranial coronal suture. Third antennal segment with 34–44, 4th segment with 11–23 and 5th segment with 9–14 secondary rhinaria. Rostrum reaching meso- —metathorax. Peritremes on abdominal sternites I and II separated by a distance less than diameter of peritreme or fused. Cauda escutcheon-shaped with rounded apex. Hind tibiae without pheromone plates.

Oviparous female. Body elliptical, 1.6–1.8 times as long as its width. Salmon-pink, yellow or pale yellow, appendages pale to light brownish, apices of siphunculi and cauda blackish. Cleared specimens with head, antennae, two last rostral segments, distal halves of femur, tibia, tarsi and siphunculi brownish, bands on abdominal tergites, peritremes, subgenital and anal plates and cauda light brown. Dorsal surface of the thorax and abdomen is almost not sclerotized, only a wide disrupted band on the pronotum, small sclerites on abdominal tergite VII and band on tergite VIII, as well as peritremes on segments I–VII and very rarely comparatively small marginal sclerites on pro-—metathorax, I–IV and VII segments of the abdomen are sclerotized, light brown; sclerites on tergite VII sometimes fused and form very short band, or, on the contrary, completely disappear; band on tergite VIII sometimes disintegrate into two large sclerites; the ventral surface of the abdomen is not sclerotized. Surface of dorsal side of head smooth, of ventral side of head with sparse pointed spinules, on pronotum distinct reticulate, on meso- —metanotum and abdominal tergites I–VI indistinctly reticulate, almost smooth (contour of cells formed by thin, irregular line); surface of tergite VII with rows of small pointed spines, which on tergite VIII become larger and partially fuse. Marginal and spinal tubercles absent. Setae on dorsal surface of head, thorax, abdominal tergites I–VII, antennae and legs blunt, pointed or, very rarely, finely pointed, on abdominal segment VIII, ventral surface of body, rostrum, subgenital and anal plate and cauda finely pointed. Chaetotaxy of first tarsal segments 3,3,2 on most specimens, but some specimens with 3,3,3 or on one hind leg with 2 and on other legs with 3 setae. Antennae 5-segmented as a result of fusing of 3rd and 4th segments, without secondary rhinaria. Rostrum reaching mesothorax—abdominal segment I; ultimate rostral segment wedge-shaped with straight or slightly convex margines. Legs shortened and thickened. Peritremes on abdominal sternites I and II separated by a distance less than diameter of peritreme or fused. Surface of siphunculi with scales of weakly fused spinules or with rows of large pointed spines only sometimes partially fused into indistinct scales. Hind tibiae broad, with 99–159 round or elliptical pheromone plates of varying size throughout their length.

Systematic relationships. The differences between Neoceruraphis pseudosensoriata ( Pashtshenko, 1988) and N. viburnicola ( Gillette, 1909) are given in the key below.

Distribution. Canada: Alberta, British Columbia, Manitoba, New Brunswick, Northwest Territories, Ontario, Quebec ( Burnham 1938; MacGillivray 1960; Robinson 1979; Maw et al. 2000). USA: California, Colorado, Connecticut, Delaware, District of Columbia, Idaho, Illinois, Indiana, Kansas, Maryland, Massachusetts, Missouri, Montana, Nebraska, Nevada, New Jersey, New York, North Dakota, Ohio, Oklahoma, Oregon, Pennsylvania, South Dakota, Utah, Vermont, Virginia, Washington, Wisconsin ( Davis 1910; Gillette & Bragg 1915, 1918; Patch 1923; Guyton 1924; Cutright 1925; Hottes & Frison 1931; Gillette & Palmer 1932; Knowlton 1941; Leonard 1963; Gittins et al. 1976; Smith & Parron 1978).

Kaygin et al. 2010 record the presence of apterous individuals of Neoceruraphis viburnicola on Viburnum sp. in Turkey (Bartin and Inner Anatolia provinces) on 23 June and 29 July 2005. Aphids were reported to feed mainly on shoots, undersides of the leaves and flowers. It needs to be confirmed that these aphids were N. viburnicol a, since until now no other apterous morphs have been observed on Viburnum except for fundatrices and oviparous females, and the presence of either on Viburnum in mid-summer is unlikely. In addition, the habitat of aphids on flowers and shoots is very different from the typical habitat of the species in pseudogalls made of twisted leaves.

Biology. The primary hosts are Viburnum opulus L. and its varieties, and V. trilobum Marshall ( Gillette 1909; Davis 1910; Gillette & Bragg 1915; Guyton 1924; Hottes & Frison 1931; Gillette & Palmer 1932; Burnham 1938; Knowlton 1941; Palmer 1952; MacGillivray 1960; Leonard 1963; Gittins et al. 1976; Smith & Parron 1978).Aphids cause curling of leaves in spring and form pseudo-galls and after a short time emigrants leave their primary host. The beginning of the cycle and the appearance of aphids on Viburnum depend on latitude and in the south of the United States it occurs in April, and in Canada in late May–early June. For a long time, the secondary host of the species remained unknown, but in 1957 and 1959 MacGillivray successfully transferred aphids to Carex pallescens L. (= Carex pallescens var. neogaea Fernald ) and to Scirpus microcarpus J.Presl & C.Presl (= Scirpus rubrotinctus Fernald ) in greenhouse ( MacGillivray 1960). Colonies of apterae developed on these plants just above the soil level between the leaf blades. Unfortunately, until now, these aphids have not been found in natural conditions, either on these plants or on any others. Remigration to Viburnum starts in September, and gynoparae, together with individuals of the bisexual generation, can occur on leaves, for example, in Illinois, until the end of December ( Hottes & Frison 1931).

Figures

FIGURE 40. Fundatrix of Neoceruraphis viburnicola (Gillette, 1909), habitus.

FIGURES 41–44. Neoceruraphis viburnicola (Gillette, 1909), fundatrix. 41, antenna; 42, hind tibia; 43, siphunculus; 44, cauda.

FIGURE 45. Emigrant of Neoceruraphis viburnicola (Gillette, 1909), habitus.

FIGURES 46–49. Neoceruraphis viburnicola (Gillette, 1909), emigrant. 46, antenna; 47, hind tibia; 48, siphunculus; 49, cauda.

FIGURE 50. Apterous viviparous female (exule) of Neoceruraphis viburnicola (Gillette, 1909) habitus.

FIGURES 51–58. Neoceruraphis viburnicola (Gillette, 1909), apterous viviparous females (exules). 51, antenna; 52, head; 53, surface of cuticle on abdomen; 54, ultimate rostral segment; 55, hind tarsus; 56, hind tibia; 57, siphunculus; 58, cauda.

FIGURE 59. Gynopara of Neoceruraphis viburnicola (Gillette, 1909), habitus.

FIGURES 60–63. Neoceruraphis viburnicola (Gillette, 1909), gynopara. 60, antenna; 61, hind tibia; 62, siphunculus; 63, cauda.

FIGURE 64. Male of Neoceruraphis viburnicola (Gillette, 1909), habitus.

FIGURES 65–68. Neoceruraphis viburnicola (Gillette, 1909), male. 65, antenna; 66, hind tibia; 67, siphunculus; 68, cauda.

FIGURE 69. Oviparous female of Neoceruraphis viburnicola (Gillette, 1909), habitus.

FIGURES 70–73. Neoceruraphis viburnicola (Gillette, 1909), oviparous female. 70, antenna; 71, hind tibia; 72, siphunculus; 73, cauda.