Pemphigus populivenae Fitch

Galls are elongate pocket-shaped or cock's comb-shaped, greenish or yellowish or pale red, arising alongside mid-rib on upper side of leaf, with a slit-shaped opening underneath. On heavily-infested trees, galls may occur on both sides of the leaf, and those on the underside may then be confused with those of P. betae (Maxson & Knowlton 1934; however see also Footit et al. 2010). Whitham (1978) reported that P. populivenae galling Populus fremontii in Utah caused chlorosis of the leaf distal to the gall. As in the case of P. betae, several species of cottonwoods and their hybrids are colonised (angustifolia, balsamifera, deltoides, fremontii and trichocarpa; the latter species in experimental conditions only). The fundatrix is yellowish green. Alatae (BL 1.1-1.8 mm) emerge in June-July and migrate to found colonies on roots of Amaranthaceae. Rumex (Polygonaceae) may also be colonised. The evidence for this host alternation is work in California by Grigorick & Lange (1962), who transferred sexuparae from sugar beet to poplar bark under controlled conditions and obtained fundatrices that produced galls specifically on P. trichocarpa. The alatae from these galls were identified as P. populivenae, and colonised roots of B. vulgaris and Chenopodium album. However, the suggested synonymy of both P. betae and P. balsamiferae with populivenae indicates some confusion of identity, and further work seems advisable to confirm that the correct name for populations damaging sugar beet in California (e.g. Summers & Newton 1989) is in fact populivenae rather than betae. Foottit et al. (2010) have found molecular evidence that at least three taxa with similar galls occur sympatrically on cottonwoods in Alberta.

Pemphigus populi-venae Fitch

Gall. Greenish or yellowish, sometimes with blush of red. Pocketlike excrescence vary ing from oblong to semicircular on upperside of leaf with slitlike mouth on underside next to midrib, similar to that of P. balsamiferae but on opposite surface of leaf.

Collections. As winter host on Populus angustifolia, in pocketlike leaf galls. Colorado: Masonville, Boulder, Longmont and Fort Collins. Utah: Hyrum. Fundatrices May 18 to July 4, alate fundatrigeniae June 11 to July 12; rare. This species is doubtfully separated from P. populi-globuli except by the character of the gall, located on leaf blade, not involving petiole.

Pemphigus populivenae Fitch

Galls beside mid-rib on upper side of leaf of P. balsamifera

P. populivenae occurs in Alberta in very small numbers. In every locality where it was found in Alberta it was associated with galls caused by P. betae or P. populiglobuli. This species feeds close to the mid-rib on the undersides of the leaves of P. angustifolia or P. balsamifera, causing a gall (Fig. 7) about one-quarter to one-half of an inch long and about a quarter of an inch deep on the upper side of the leaf. The gall is similar to that of P. betae but is on the opposite side of the leaf.

Records of the distribution of P. populivenae in Alberta are as follows: 1953, Edmonton (Strickland, 1953), Monarch, P. angustifolia, P. balsamifera; 1957, Lundbreck, Coaldale, P. balsamifera.

Pemphigus populivenae Fitch 1859 [Poplar vein gall aphid, also known as sugarbeet root aphid*].

Feeding by the stem mother on the underside of the leaf blade causes the leaf tissue to swell and form a pocket-shaped gall. Galls are oval to semi-oblong, open on the underside of the leaf, and project above the upper plane of the leaf blade. Galls are usually closely associated with the midrib or a primary vein. They attain a length of about 8– 12 mm, a depth of about 5 mm, and are green.

Primary hosts include P. angustifolia and P. balsamifera (Maxson and Knowlton 1929; Palmer 1952; Harper 1959 a). Whitham (1978) reports P. populivenae on Fremont cottonwood, P. fremontii S. Watson ( Aigeiros ), in the United States. Quinoa, Chenopodium quinoa (Chenopodiaceae), is a secondary host (Cranshaw et al. 1990).

Pemphigus populivenae

Grigarick and Lange (1962) considered P. betae to be synonymous with Pemphigus populivenae Fitch, which also forms pouch-shaped galls on the leaf blades of species in Populus section Tacamahaca. Summers and Newton (1989) used the name P. populivenae for aphids on sugarbeets in California. Harper (1959) designated aphids that formed galls projecting below the plane of the leaf blade on Populus hosts as P. betae (Fig. 1) and used the name P. populivenae for aphids forming galls that projected above the plane of the leaf blade. However, according to Maxson and Knowlton (1929), in heavy infestations the latter can occur in the position typical of P. betae. In addition, Pemphigus knowltoni Stroyan has been reported from Utah, where it forms galls similar to those of P. betae on P. angustifolia (Stroyan 1970). In Europe the species on beets and other Chenopodiaceae is named Pemphigus fuscicornis (Koch) and has no known associated primary host form (Blackman and Eastop 2000).

Collectively, these results identify at least three co-occurring populations forming similar galls on the same host trees.The concordance of the mitochondrial and nuclear data suggests that the three groups are reproductively isolated. Specimens from group A (Fig. 2) key to P. betae. Specimens from group C key to P. populivenae. Specimens from group B are intermediate. No specimens matched the state reported for P. knowltoni. The available evidence suggests that group B is an undescribed species. Other than P. betae, P. populivenae, and P. knowltoni, no North American Pemphigus species are known to regularly form elongate galls along the leaf midrib of species in Populus section Tacamahaca. Although group C was identified as P. populivenae, there are several inconsistencies. Galls of this species are reported to project above the plane of the leaf blade (Harper 1959), but galls sampled in the present study resembled those of P. betae, i.e., they project below the leaf blade. Galls of P. populivenae can apparently resemble those of P. betae when populations of the former are high (Maxson and Knowlton 1929). However, galls in the position normally ascribed to P. populivenae are uncommon in southern Alberta (Harper 1959; K.D.F., personal observations), whereas group C samples were common in our collections. These discrepancies are resolved if P. populivenae forms galls that can project either above or below the leaf blade regardless of population density. Alternatively, group C may represent an undescribed species morphologically similar to P. populivenae. Groups B and C co-occur in morphologically pure zones of P. balsamifera (samples from Cypress Hills and Lundbreck Falls, Alberta). Group B was not detected at sites where P. deltoides (section Aigeiros) or hybrids involving it occur.

It is apparent that several taxa form similar galls on the leaf blades of species and hybrids of Populus section Tacamahaca. The form of a gall in a given position (petiole, petiole2blade junction, along midvein), may depend as much on host physiology or morphology as on the inducing aphid species. Anecdotal observations that we made during recent collections indicate that midvein galls containing morphologically similar aphids tend to be more globular when close the leaf base than those located more distally, especially on thicker leaves, sometimes approaching the state characteristic of Pemphigus populiglobuli Fitch. Maxson and Kowlton (1929) noted galls similar to those of P. populivenae produced by aphids they identified as Pemphigus populicaulis Fitch and P. populiglobuli. Reliance on gall position and form as indicators of species identity is clearly not a viable approach for use with this group of Pemphigus species, given the current state of knowledge.

Pemphigus populi-venae

Light red coxcomb-like gall on mid-vein, aphid

Pemphigus populivenae [Russo seems to have completely mistaken Thecabius populimonilis for P populivenae]
[Page 62]

Hosts: cottonwoods

Often, the galls are located in rows along the midrib or along the edges of leaves.

PEMPHIGUS POPULI-VENAE Fitch

Thomas (1879), in the "Eighth Report of the State Entomologist of Illinois," lists a species of Pemphigus under this name but without definitely recording it from Illinois. This species has been rarely recorded in literature, and the only detailed description of its forms is that by Maxson and Knowlton (1929).

Our record establishing the occurrence of this species in Illinois is based upon the finding of the characteristic cockscomb-like galls upon the upper surfaces of leaves of Populus deltoides at Watson, Illinois, on November 13, 1930 (Frison and Ross).

Pemphigus populi-venæ Fitch

Pemphigus Populi-venæ was described by Dr. Asa Fitch in 1859. Since the original description was published, this species does not appear to have been recognized but appears to have been confused by some aphidologists with P. p.-caulis and P. p.-globuli.

In his studies of this species Dr. Fitch appears to have failed to recognize the real nature of the aphids in the galls. It seems altogether probable that his male and female larvæ and pupæ were the early stages of the alate females (fundatrigenia).

The winged individuals were so briefly described by Fitch that the description is valueless for purposes of identification. Identifying aphids by the plant deformities produced is very apt to lead to confusion. Easily distinguished species produce very similar deformities and a single species may produce more than one form of deformity.

The Galls.—Dr. Fitch describes the galls of P. P.-venæ as "an oblong compressed excrescence like a cock's comb, of a light red color varied with pale yellow growing from the midrib of balsam poplar leaves on their upper side with an orifice on the opposite side. They are nearly semi- circular and half as high as long, being usually over a half inch in length, with uneven surface, their walls thick, brittle and succulent. They are commonly placed near the base of the leaf but sometimes in its middle."

Galls similar to those described by Fitch were collected by the senior author at Oak Park, Minnesota, on balsam poplar and near Spreckles, California, on Populus trichocarpa.

The aphids from these galls have some of the characters of P. p.-caulis and P. P.-globuli but are not wholly like either. The most noticeable difference between P. P.-venæ and P. p.-caulis and P. P.-globuli is its smaller size. The senior author has taken all three species on a single balsam poplar tree in Minnesota. Because of the similarity of the size of these species to those described by Dr. Fitch and the likeness of the galls of P. p.-venæ as described by Dr. Fitch to those collected in Minnesota and California, the aphid here described is considered the P. p.-venæ of Fitch.

The Gall.—Dr. Fitch's description of the gall should be enlarged by stating that the galls vary in form from more or less oblong to semicircular and even almost triangular in outline. On heavily infested trees galls occur on both sides of the leaf. When on the underside they may be confused with those of P. beta, being similar in form and location.

Aphids collected at Hyrum, Utah, on June 20, 1926, seem to be the species described by Fitch. These aphids were producing galls on the leaves of the narrow-leaved cottonwood, Populus angustifolia.