Mordwilkoja vagabunda

Pachypappa pseudobyrsa

Pemphigus betae

Pemphigus bursarius

Pemphigus tartareus

Pemphigus monophagus

Pemphigus nortonii

Pemphigus populicaulis

Pemphigus populiglobuli

Pemphigus populiramulorum

Pemphigus populitransversus

Pemphigus populivenae

Pemphigus spyrothecae

Thecabius gravicornis

Thecabius populimonilis

Aceria neoessigi

Aceria parapopuli

Thecabius populiconduplifolius

Mordwilkoja vagabunda

The stem mother attacks the terminal bud of shoots to form a hollow, convoluted, bladder-shaped structure (Figs. 4 and 5). This structure apparently represents a cluster of galls, with each gall induced from a single leaf (Gillette 1914). Large clusters may reach diameters of 80-95 mm and attain a thickness of about 50-60 mm (Gillette 1914). Galls in southern Alberta produce an average of 637 (range: 98-2,040) alatae, with emergence beginning in mid- to late July and being 90% complete by August 5 (Harper 1959b).

The primary host is P deltoides, on which empty galls are often retained during winter months (Palmer 1952; Harper 1959a). Secondary hosts have not been reported. The author has seen one case in Montana of this aphid on what appeared to be a hybrid between P deltoides and P angustifolia. The aphid can be common on individual trees, but its distribution seems to be highly localized (Gillette 1914; KF, pers. obs.).

Pachypappa pseudobyrsa (Walsh, 1863) 

Feeding by the stem mother induces a pocket-like pseudogall adjacent to the midrib of the leaf blade (Fig. 6). The gall projects up from the upper leaf surface, opening on the lower leaf surface. The gall is too small to contain the apterae, which crawl out to feed on the secondary leaf veins on the underside of the leaf. This feeding results in the lower leaf surface becoming coated with a powdery white wax formed by the apterae. Feeding also causes the two sides of the lower leaf surface to gradually bend toward one another to become almost parallel and form a purse-like pseudogall (Fig. 7). Galls are light green but occasionally have a tinge of red along the midvein of the leaf. Each gall may produce an average of 625 alatae (Alleyne and Morrison 1977). The species has also been referenced in the literature as Asiphum pseudobyrsum (Palmer 1952; Alleyne and Morrison 1977) and Pachypappa pseudobursa (Floate and Whitham 1993).

The primary host is P deltoides (Palmer 1952; Alleyne and Morrison 1977; Floate and Whitham 1993). Alatae are found in galls in mid-summer and presumably colonize unknown secondary hosts. This aphid has wide geographical distribution, with populations locally concentrated on individual trees.


Pemphigus betae Doane, 1900

(= P balsamiferae Williams, 1911) 

Galls are initiated on the upper leaf surface, usually along the midrib. Fully formed galls are pocket-like structures about 10 mm in length with a depth of 5 mm extending below the leaf surface. Developing galls are green, with mature galls frequently turning reddish. There is typically one gall per leaf that most often occurs near the base of the leaf blade. This location appears to be optimal for gall initiation and offspring reproduction to the extent that stem mothers will fight to exclude competitors from these sites (Whitham 1979). Gall densities can be highly variable, with particularly susceptible trees having five or more galls per leaf (Fig. 8). Sexuparae appear to have a limited ability to detect this susceptibility and will preferentially colonize those hosts on which stem mothers are most likely to be able to induce galls in the following spring (Moran and Whitham 1990). Galls in southern Alberta have been reported to produce an average of 41 (range: 2-180) alatae, with emergence beginning in late June to early July and being 90% complete by July 23 (Harper 1959b).

Primary hosts include P angustifolia, P balsamifera, and hybrid intermediates (Palmer 1952; Harper 1959a; Floate and Whitham 1993). Secondary hosts include sugar beet (Chenopodiaceae: Beta vulgaris L.), for which Pemphigus betae has been reported to vector curly top virus and virus yellows (refs. in Harper 1959a). Other secondary hosts in the family Chenopodiaceae include lamb's quarters (Chenopodium album L.), spinach (Spinacia oleraceae L.), Swiss chard (Beta vulgaris var. cicla), and dock (Rumex spp.). Other secondary hosts include lettuce (Asteraceae: Lactuca sativa L.) and pigweed (Amaranthaceae: Amaranthus sp.) (Harper 1959a). This aphid is common and has wide geographical distribution wherever its primary host species occurs.

Molecular analyses identify three co-occurring genetic "types" of P betae (Foottit et al. 2008). Further studies are needed to determine if these types represent sibling species and to identify mechanisms for their reproductive isolation.

Pemphigus bursarius (Linnaeus, 1758) 

Stem mothers form flask-shaped galls on the leaf petiole or occasionally on young shoots (Harper 1966). As many as three or four galls may occur on one leaf, each producing up to 78 alatae (Alleyne and Morrison 1977). First instars of this species include a "soldier" caste distinguished by their aggressive behaviour in attacking natural enemies (Rhoden and Foster 2002). Soldier aphids attack using sustained thrusts of their stylets to pierce the predator's cuticle. Alternatively, soldier aphids may use their legs to squeeze predators to rupture the cuticle and damage internal organs (Rhoden and Foster 2002). Such attacks are costly to the aphids but can kill predaceous maggots (Diptera: Syrphidae) to protect other aphids remaining in the gall.

Populus nigra L. var. italica is the primary host (Harper 1959a; Alleyne and Morrison 1977). Secondary hosts include lettuce, on which P bursarius is considered to be an economically important pest in Europe and in the United States (refs. in Harper 1966; Alleyne and Morrison 1977). Other secondary hosts include carrot (Apiaceae: Daucus sp.), lamb's quarters, and nipplewort Lampsana communis L. and Sonchus spp. (Asteraceae) (Palmer 1952). The aphid apparently has wide distribution in Canada, being previously reported from Alberta, Ontario, and Quebec (Harper 1966).

Pemphigus junctisensoriatus Maxson, 1934 

Galls resemble those of P populicaulis (see section 8), being more or less globular and incorporating tissues at the base of the leaf blade and the petiole. However, galls of P junctisensoriatus are primarily composed of petiole and have a long slit extending more than halfway around the gall. Galls of P. populicaulis are primarily composed of leaf blade tissues and have a small round opening (Maxson 1934). Palmer (1952) reported the species to be "rare." Alleyne and Morrison (1977) reported collections of P. junctisensoriatus from only one tree at Macdonald College Campus in Quebec. There have been no reports of this aphid from the grassland region, but its occurrence seems probable.

The primary host is P deltoides (Maxson 1934; Palmer 1952; Alleyne and Morrison 1977). Secondary hosts have not been reported.

Pemphigus monophagus Maxson, 1934. 

Stem mothers feed near the base of the leaf blade to form a roughly globular gall mainly comprising the swelling of the upper surface of the leaf blade and partially comprising the swelling and twisting of the leaf petiole (Palmer 1952). The gall has a circular opening on the underside of the leaf and is frequently bisected by a shallow groove, suggesting a double gall (Maxson 1934). This species does not have a secondary host, completing its entire life cycle on the Populus host. The only apparent generation of alatae are the sexuparae, which exit the gall in late August and early September. First instars of this species include a morphologically distinct subset of instars that are probably members of a soldier caste, although this has not been confirmed either experimentally or by direct observation (Aoki and Kurosu 1988).

Primary hosts include P angustifolia and P balsamifera (Palmer 1952; Alleyne and Morrison 1977) (P balsamifera = P tacamahaca in Palmer 1952). Palmer (1952) reports P monophagus to be "rather rare," although high densities of galls were reported on leaves of P. balsamifera at Pigeon Lake, Alberta (Alleyne and Morrison 1977).

Pemphigus nortonii Maxson, 1934. 

Descriptions of this gall vary. Maxson (1934) describes galls of this species as "similar" to those of P. populicaulis. Palmer (1952) states that galls of the two species are "indistinguishable." Harper (1959a) reports that galls of the two species are "somewhat similar" but can be distinguished. Whereas galls of P nortonii are formed solely from the swelling and twisting of the petiole and open via a long, semi-spiral slit, galls of P populicaulis include tissues of both the petiole and leaf blade and open via a small round exit hole (Harper 1959a). In southern Alberta, each gall produces an average of 315 (range: 20-812) alatae, with exiting beginning in late June to mid-July and being 90% complete by August 6 (Harper 1959b).

The primary host is P deltoides (Maxson 1934; Palmer 1952; Harper 1959a). Secondary hosts have not been reported. The aphid is reported to be uncommon (Palmer 1952).

Pemphigus populicaulis Fitch 1859 [Poplar leaf-petiole gall aphid]. 

Galls are initiated on the upper leaf surface, with blade and petiole becoming twisted to form a more or less globular structure at the juncture of the leaf petiole and the leaf blade. The structure is composed of petiole tissue but also includes tissues of the leaf blade that usually extend some distance down onto the gall (Figs. 9 and 10). Twisting of the leaf tissues forms a semi-spiral groove that extends two-thirds of the diameter of the gall. One or a few small round openings in the groove of mature galls provide an exit for alatae. An average of 410 alatae per gall was reported for Quebec (Alleyne and Morrison 1977). An average of 123 alatae per gall (range: 8-426) was reported for southern Alberta, with their exiting from galls beginning in late June to mid-July and being 90% complete by September 11 (Harper 1959b).

The primary host is P deltoides (Palmer 1952; Harper 1959; Alleyne and Morrison 1977; Floate and Whitham 1993). Rare occurrences of P populicaulis have been reported on intersectional hybrids (Gillette and Palmer 1934; Floate and Whitham 1993). Secondary hosts include water parsley (Apiaceae: Oenanthe sarmentosa C. Presl ex DC.) and possibly fleabane (Erigeron spp.) and goldenrod (Solidago spp.) (Asteraceae) (refs. in Harper 1959a). Harper (1959a) cited references that raised the possibility that P populicaulis might be synonymous with P brevicornis. This synonymy is not supported in more recent work (Eastop and Hille Ris Lambers 1976).

Pemphigus populiglobuli

Galls are semi-globular structures formed by the swelling of the leaf blade at the junction with the petiole and extend above the plane of the upper leaf surface (Fig. 11). Although morphologically similar to galls of P. populicaulis, galls of P. populiglobuli typically have a long, narrow slit between the modified tissues of the leaf blade and the petiole, whereas galls of P. populicaulis have a small, pore-like opening. Mature galls are green, often with a reddish tinge. In southern Alberta, galls produce an average of 56 (range: 8–174) alatae, with their exiting from galls beginning in late June to early July and being 90% complete by July 20 (Harper 1959 b). 

Primary hosts include P. angustifolia, P. balsamifera, and hybrid intermediates (Maxson and Knowlton 1929; Gillette and Palmer 1934; Harper 1959 a; Floate and Whitham 1993). However, the key in Alleyne and Morrison (1977) associates P. populiglobuli with P. deltoides .

Pemphigus populiramulorum Riley 1879 [Poplar twig gall aphid*]. 

Whereas galls of other Pemphigus species are formed from tissues of the leaf blade and/or petiole, galls of P. populiramulorum occur on twigs of the current year. Feeding on the young twigs causes swelling of the tissues that expand into a hollow globular structure that surrounds the stem mother and her offspring (Fig. 12). The exit opening is a narrow slit with slightly protruding lips. The location of galls on the woody tissues of the twig results in vacant galls frequently being retained on the tree during winter months. The point of attachment left by abscised galls is a characteristic flattened “button” region on the twig (Fig. 13). Galls in southern Alberta produced an average of 74 (range: 9–190) alatae, with gall exiting beginning in early to mid-July and being 90% complete by August 23 (Harper 1959 b). The primary host is P. deltoides (Palmer 1952; Harper 1959 a ; KF, pers. obs) . This aphid is described by Maxson and Knowlton (1929) as occurring on P. balsamifera , but this report has been questioned by Palmer (1952).

Pemphigus populitransversus Riley 1879 [Poplar petiolegall aphid*]. 

The stem mother feeds on petioles to cause the swelling of tissues that form a hollow, globular structure that surrounds both the stem mother and her offspring (Figs. 12 and 14). Mature galls have a transverse exit slit with margins that may be thickened and slightly protruding, reminiscent of lips. An average of 150 alatae per gall was found in Quebec (Alleyne and Morrison 1977). An average of 192 alatae per gall (range: 25–962) was found in southern Alberta, with gall exiting beginning in late June to mid-July and being 90% complete by August 23 (Harper 1959 b ). Jones and Gillette (1918) provide detailed taxonomic and life history information of this species on both primary and secondary hosts. 

The primary host is P. deltoides (Maxson and Knowlton 1929; Gillette and Palmer 1934; Harper 1959 a ; Alleyne and Morrison 1977; Floate and Whitham 1993). Secondary hosts include sugar beet, dock, cabbage, turnip, and lettuce (refs. in Alleyne and Morrison 1977). 

Pemphigus obesinymphae Aoki is a close relative of P. populitransversus and induces a gall that may be easily mistaken for that of the latter species (Aoki and Moran 1994). Pemphigus obesinymphae is not known to occur in Canada, but is reported to co-occur with P. populitransversus on P. deltoides in the United States (Abbott and Withgott 2004). The species is mentioned here to increase awareness of its possible presence in Canada.

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 spyrothecae (= spirothecae ) Passerini 1856. 

Feeding by the stem mother causes the leaf petiole to twist into spirals (usually three) that surround the aphid. The spirals swell, with their seams becoming tightly pressed together to form a hollow, spiral- shaped gall that completely surrounds the stem mother and her offspring (Fig. 15). Galls mature in late August or early September and are initially green, but often become reddish. Alatae exit the mature gall via a series of small pores that form along the seams of the spirals. Pemphigus spyrothecae does not have a secondary host and, as reported for P. bursarius and suspected for P. monophagus , has a morphologically distinct subset of first instars that form a soldier caste. Experimental studies show that galls containing 50 soldier and 50 non-soldier aphids versus 100 non-soldier aphids can be 10 times less likely to be attacked by predators under field conditions (Foster and Rhoden 1998). 

Populus nigra L. var. italica is the primary host (Alleyne and Morrison 1977). This aphid was first reported in North America from material collected in 1972–1973 in Quebec, where it was extremely common (Alleyne and Morrison 1974). Blackman and Eastop (1994) report its introduction into western Canada. In addition, high densities were observed by the author in 2003 at Kelowna, British Columbia.

Thecabius gravicornis (Patch, 1913) (Pemphigus) [Folded-leaf balsam aphid]. 

Feeding by the stem mother adjacent to the midrib on the lower surface of the leaf blade initiates a small cavity in which apterae are produced. The apterae leave the cavity to feed on expanding terminal leaves. Their feeding causes the leaves to fold ventrally along the midrib to form a purse-shaped pseudogall similar to that of P. pseudobyrsa . In Quebec, alatae appear in the pseudogalls from mid-June to early July (Alleyne and Morrison 1977). 

Primary hosts include P. balsamifera (Gillette and Palmer 1934) and P. angustifolia (Blackman and Eastop 1994). There has been one report of T. gravicornis on P. nigra L. var. italica (Alleyne and Morrison 1977). This aphid is apparently widespread but uncommon (Blackman and Eastop 1994). 

Thecabius populimonilis (Riley, 1879) (Pemphigus) [Bead-like cottonwood gall aphid]. 

The life cycle of this aphid is reviewed by Gillette (1913) and by Maxson and Knowlton (1929). The stem mother feeds on the underside of the leaf blade, causing formation of a blister-like pseudogall that projects above the upper plane of the leaf surface. Her offspring (the second generation) are apterae that leave the gall shortly after birth to each induce their own similarly shaped gall, either on the same leaf or on adjacent leaves of the same shoot. This results in one or more rows of galls forming parallel to the midrib, with each gall containing one aphid (Fig. 17). Most of these aphids become alatae that migrate to other trees. However, some individuals stay in the galls and remain as apterae to produce apterous offspring (the third generation). These apterae leave the gall to move onto adjacent leaves to induce new galls and produce offspring, a portion of which develop into winged sexuparae. Gillette (1913) reports that 10–12 sexuparae may occur in one gall with the parent. The sexuparae exit these galls in late summer to produce male and female sexuales, which mate and produce the overwintering egg from which the stem mother develops in the following spring. 

Primary hosts include P. angustifolia and P. balsamifera (Maxson and Knowlton 1929; Gillette and Palmer 1934; Harper 1959 a ; Floate and Whitham 1993). There is likely no secondary host.

Aceria neoessigi (Keifer, 1940) (Eriophyes). 

Mites overwintering in the buds of Populus emerge in the spring to attack the flowers of the catkin. Attacked flowers become malformed and enlarged and group tightly together such that the catkin forms a large pendant gall that may exceed 20 cm in length (Fig. 18). Galled catkins remain on the tree until early summer, long after unattacked catkins have dehisced. The species does not have a secondary host. Galled catkins may also contain Aceria populinquis Keifer, which occurs as an inquiline (Wilson and Oldfield 1966). In the United States, P. fremontii is the primary host (Wilson and Oldfield 1966). In Canada, the primary host is P. deltoides (KF, pers. obs.), which is closely related to P. fremontii (see Fig. 6 in Eckenwalder 1996).

Aceria parapopuli (Keifer, 1940) (Eriophyes). 

Mites overwinter in galls to exit in the spring and attack newly expanding vegetative and reproductive buds. Attacked buds form a woody, cauliflower-like gall that may exceed 3 cm in diameter (Fig. 19). Active galls normally persist for 1 year but can remain active for up to 15 years. New generations are produced every two to three weeks during summer months. Active galls are red and green, whereas dead galls are brown. Aceria parapopuli does not have a secondary host but can disperse between trees using wind currents (ref. on life history cited in McIntyre and Whitham 2003). 

Primary hosts include P. angustifolia , P. balsamifera , and hybrid intermediates (Floate and Whitham 1993).

Thecabius populiconduplifolius (Cowen, 1895) (Pemphigus) [Folded-leaf poplar aphid].

Feeding by the stem mother at the leaf margin causes the edge of the leaf blade to fold under and form a small gall (Fig. 16). The apterae produced in this gall exit to feed on the underside of expanding leaves, which produces galls similar to those of T. gravicornis.

Reported primary hosts include P. deltoides (Palmer 1952), P. balsamifera (Harper 1966), and P. nigra L. var. italica (Alleyne and Morrison 1977). Secondary hosts include species of Ranunculus (Swain 1919; Palmer 1952). Thecabius populiconduplifolius has an identical biology and is virtually indistinguishable from the Eurasian species T. affinis (Kaltenbach), although the two species can be separated by chromosome number (Blackman and Eastop 1994).

Gall-inducing aphids and mites associated with the hybrid complex of cottonwoods, Populus spp. (Salicaceae), on Canada’s grasslands