Pemphigus populitransversus

The North American aphid Pemphigus populi-transversus Riley (Hemiptera: Aphididae: Pemphiginae) forms galls on the leaves of the eastern cottonwood (Populus deltoides; Salicaceae) throughout the eastern and central United States. From the 1940s to the 1990s, Dr. Robert Sokal and his associates published extensively on character and geographical variation in P. populi-transversus in the central and eastern United States (citations summarized in Sokal et al. 1991). One of their more intriguing observations was that most populations surveyed exhibited two distinct gall types, which they named ‘‘elongate’’ and ‘‘globular,’’ based on their shapes (Bird et al. 1979; Sokal and Riska 1981). The aphids forming the two types differed at several allozyme loci and in the seasonal production of sexuals, with the sexuals of the elongate-type appearing in the fall and those of the globular-type appearing in the spring (Faith 1979a,b; Rhomberg 1980; Setzer 1980). Faith (1979a,b) hypothesized that the unusual gall polymorphism could reflect these underlying differences in life cycles, suggesting a rare case of incipient allochronic speciation.

The relationship between P. populi-transversus and a closely related aphid species, P. obesinymphae Aoki, has been of the most confusing among North American Pemphigus species (Aoki and Moran 1994; Blackmon and Eastop 1994). Pemphigus obesinymphae was originally described in the southwestern United States on Populus fremontii (a cottonwood that is likely the sister taxon of P. deltoides; Eckenwalder 1996). Pemphigus obesinymphae was found to share many morphological and life-history characters with the globular-gall morph of P. populi-transversus, including the globular gall shape and the spring sexuals noted by Faith (1979a,c). Then, in groundwork for this study, we found that the globular morph is in actuality a distinct population of P. obesinymphae, and not a morph of P. populi-transversus. We clarify this relationship here to coordinate our study with the existing literature on P. populi-transversus. Hereafter, to limit further confusion, we will recognize the species that forms the elongate gall alone as P. populi-transversus. The species that forms the globular gall is P. obesinymphae, and is distributed across the United States on two hosts: the eastern cottonwood P. deltoides (on which it is sympatric with P. populi-transversus) and the Fremont cottonwood (on which P. populi-transversus is absent).

This analysis is necessary because of the complex distribution of P. obesinymphae: as we have described, the species consists of two lineages, one sympatric with P. populi-transversus on P. deltoides, and one restricted to southwestern North America on Populus fremontii (Aoki and Moran 1994; Abbot and Moran 2002).

In early spring, a first burst of growth occurs from embryonic leaves that have overwintered in the buds. These ‘‘early’’ leaves are followed by a ‘‘late’’ flush of summer leaves, most of which are newly initiated on the growing shoots. Pemphigus populi-transversus foundresses, having overwintered as eggs, form galls on the early, spring leaves. Pemphigus obesinymphae, by contrast, returns to P. deltoides after the first flush of spring leaves, and forms galls on the late flush of summer leaves. Having appeared later on trees than P. populi-transversus, it also remains longer, well into the fall after P. populi-transversus has departed for its secondary hosts (Bird et al. 1979; Fig. 1).

As expected, there was no evidence that P. populi-transversus forms galls on Fremont cottonwoods, despite a westerly distribution on P. deltoides that overlaps with the eastern boundary of P. fremontii’s range (Fig. 2). Overall, the distribution of P. populi-transversus is in complete accord with the surveys of Sokal and associates.

Pemphigus populitransversus Riley

Gall. Same color as petiole but often with reddish tinge. Size, usually 12-18 mm in di ameter, occasionally 25.

Collections. As winter host on Populus sargenti in petiole galls, as summer host on cruciferous plants (in Louisiana, not recorded on summer hosts in this region, but to be expected); Colorado: throughout state. Utah: Farmington and Santa Clara. Fundatrices June 8 to Aug. 29, alate fundatrigeniae June 12 to August 31; not abundant.

Chief Distinguishing Characters. Petiole gall with transverse mouth

Pemphigus populitransversus Riley

The gall is formed by swelling and bending of petioles of the leaves of Populus deltoides (incl. ssp. occidentalis) and P. fremontii; it is green, globular to ovoid, with a usually transverse slit (see influentialpoints.com/Gallery). Sometimes recorded from other Populus spp. (acuminata, angustifolia, balsamifera, nigra, tremuloides, trichocarpa) However, some of these records, particularly those from western cottonwoods, may apply to other species. The fundatrix is whitish to pale dirty greenish yellow (Palmer 1952). Alatae (BL 1.7-2.0 mm) emerge in July and found colonies of pale yellow aphids in flocculent wax on roots of Brassicaceae (Jones & Gillette 1918), where it can be a serious pest (Royer & Edelson 1991). Sexuparae return to cottonwood in September-October to produce sexuales which lay overwintering eggs on the bark. Geographic variation in eastern USA has been studied extensively using multivariate methods (Sokal & Riska 1981). Bingham & Sokal (1986) studied host tree effects on morphology. P. populitransversus is recorded throughout most of North America east of the Rocky Mountains. However it is still unclear whether the name is being applied to a single species; apart from the confusion with P. obesinymphae (q.v.), Bird et al. (1979) found that two forms with different gall shape and phenology, and corresponding morphological differences in fundatrices and emigrant alatae, occur sympatrically on P. deltoides over a large area of the USA east of the continental divide. It should be noted that the morphology of their aphids from globular galls on late flushing leaves does not correspond with that described for P. obesinymphae.

Pemphigus identified as P. populitransversus have been found on Populus sp. in Mexico (BMNH collection, leg. R. Peña) and Chile (BMNH collection, leg. G. Monsalve); it has also been introduced to South Africa (Müller & Scholl 1958), where it occurs on Populus nigra (BMNH collection, leg. E McC. Callan) and P. deltoides, and the Azores (on Populus sp.; BMNH collection, leg. A. van Harten). Presumed anholocyclic populations also occur in New Zealand on Eutrema wasabi roots (BMNH collection, leg. L.M. Emms), and aphids collected on Arabis roots in England (BMNH collection, leg. G. Fox-Wilson) may also be this species. 2n=20.

Pemphigus populitransversus Riley

Gall on petiole of Populus sargentii [deltoides] with transverse slit

P. populitransversus occurs on Populus sargentii in some localities along river banks and in shelter belts in irrigated areas of southern Alberta. According to MacNay (in litt.), this species was reported occasionally on Populus deltoides, P. tremuloides, and P. angustifolia in Alberta from 1929 to 1957. Although Essig (1926, pp. 259-261) indicated that this species may live on sugar beets, dock, and lettuce, it has not been found on these hosts in Alberta. Wene and White (1953) stated that P. populitransversus is an important pest of cabbage in Texas. Altllough no secondary host has been found in Alberta, winged forms were taken in Iargc numbers from turnips and cabbage in plots at the Lethbridge laboratory in 1954. However, when these lots were harvested and the roots of the plants examined, no aphids were found.

Galls are caused by the feeding of this species on the petiole of the popIar leaf. As the aphid feeds, the petiole swells on each side of the point of feeding and a spherical, green gall with a transverse slit is produced (Fig. 4). The galls vary in size from one-quarter to three-quarters of an inch in diameter. Although the galls generally have transverse slits, some were found near Cranford, Alberta, with vertical, transverse, or anguIar slits (Figs. 11-13).

Records of the distribution of P. populitransversus in Alberta are as follows: 1929, Lethhridge, Bow River, -Arrowwood, Orkney, Macleod, Populus deltoides, Populus angustifolia, Populus tremuloides (MacNay, C. G. (in litt.)); 19.50, Turin, Picture Butte, Iron Springs; 1953, Medicine Hat; 1957, Barnwell, Taber, Vauxhall, Populus sargentii.

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 transversus

Pemphigus populi-transversus

This oval gall is formed midway of the petiole, on one side, with the opening opposite the petiole and transverse. Not common. On poplar, Populus.

Pemphigus populitransversus

Pemphigus obesinymphae, n. sp. is closely related to Pemphigus knowltoni Stroyan and, especially, to Pemphigus populitransversus Riley. We hypothesize that the three constitute a monophyletic species group within the genus Pemphigus. Both P. obesinymphae and P. populitransversus form galls only on Populus fremontii, whereas P. knowltoni uses only Populus angustifolia. When adult fundatrigeniae are not present, the presence of a gall ostiole and morphological features of the 1 st and 2nd instar fundatrigeniae can be used in order to distinguish P. obesinymphae and P. populitransversus in galls on Populus fremontii (Table 1).

[Table 1 shows that obesinymphae is known from Populus fremontii in AZ and UT and likely in NM, CO and northern Mexico, is found on petioles typically near the leaf blade, has an ostiole as well as a slit, colonizes Populus fremontii in the spring and galls late flushing leaves; that populitransversus is known from Populus fremontii throughout North America, is found near the center or elsewhere on petioles of first flush leaves, colonizes its host in fall, has no ostiole; that knowltoni is known from Populus angustifolia in UT, possibly also in ID, CO, WY, MT, galls leaf midribs, colonizes first flush leaves of its host in the fall]

Pemphigus populitransversus

Oval petiole galls with transverse openings and near middle of leaf stem, aphid, summer

Pemphigus populitransversus
[Page 61]

Hosts: Populus fremontii, balsamifera subsp trichocarpa, angustifolia, tremuloides

Rapid growth of the petiole often causes a bend at the site of the gall.

Pemphigus populitransversus

Galls on Populus deltoides, formed by swelling of petiole. Galls bear a transverse slit-like opening

This aphid, which is indigenous to North America, forms galls on cottonwood poplars. The gall resembles that of P. bursarius but migrant release is by means of a transverse slit on the lip (Fig. 6). An average of 150 migrants of this aphid were produced by 20 galls. P. populitransversus has been the subject of many investigations in the United States. Jones and Gillette (1918) showed that this aphid attacked turnips in summer. More recently Wene and White (1953), Wolfenbarger (1965), Chalfant (1969), and Harding (1971) have found this aphid to be a serious pest on cabbage. MacNay (1955) recorded this species in Alberta on Populus deltoides, P. tremuloides, and P. angustifolia.

Pemphigus populitransversus [the "elongate morph"]

Gall initiation by Pemphigus populitransversus was found to occur at two clearly separate times during the summer of 1975. Gall initiation is first detected as a slight swelling and bending of the petiole at the point where a fundatrix nymph has begun feeding. In this early stage, the young fundatrix is not enclosed and appears as a small black spot in the pocket formed by the swelling and bending of the petiole. Transverse galls first began forming, along with oblique galls, around May 15 on cottonwoods in the vicinity of Stony Brook. At this time, the early leaves of the tree were expanding and provided suitable sites for gall initiation. The trees were checked carefully on successive days, and after two or three days, there was no further gall initiation. Then, on June 15, more transverse galls began forming on the newly formed late leaves. This dimorphism in the timing of gall initiation resulted in a set of galls on the early leaves and a set of galls on the late leaves of the shoots.

A dimorphism in gall shape, life history, and aphid morphology has been described for this species by Senner and Sokal (1974). The morph they refer to as "elongate" produces galls that are more elongate in shape than those of the other morph called "globular." The question immediately arose whether the presence of early and late transverse galls was related to the globular-elongate dimorphism. An analysis of the early and late transverse galls confirms the suspected relationship (Table 1). The late galls are larger than the early galls, and more spherical, as shown by the ratios of gall dimensions. The values in Table 1 resemble those of the sample from West Point, Georgia, shown in Table 3 of Senner and Sokal (1974). The early and late galls were significantly different for each character. Corroborating tests were run following methods developed by Senner and Sokal (1974). The gall dimensions and their ratios split a mixed sample of 71 galls into early and late classes fairly well. Only two galls would be misclassified by time of gall formation when the sample was split according to gall depth and only 4 galls would be so misclassified on the basis of length/width ratio. It is highly probable that the early and late galls correspond to the elongate and globular morphs, respectively.

Pemphigus populitransversus [the "elongate morph"]

Gall initiation by Pemphigus populitransversus was found to occur at two clearly separate times during the summer of 1975. Gall initiation is first detected as a slight swelling and bending of the petiole at the point where a fundatrix nymph has begun feeding. In this early stage, the young fundatrix is not enclosed and appears as a small black spot in the pocket formed by the swelling and bending of the petiole. Transverse galls first began forming, along with oblique galls, around May 15 on cottonwoods in the vicinity of Stony Brook. At this time, the early leaves of the tree were expanding and provided suitable sites for gall initiation. The trees were checked carefully on successive days, and after two or three days, there was no further gall initiation. Then, on June 15, more transverse galls began forming on the newly formed late leaves. This dimorphism in the timing of gall initiation resulted in a set of galls on the early leaves and a set of galls on the late leaves of the shoots.

A dimorphism in gall shape, life history, and aphid morphology has been described for this species by Senner and Sokal (1974). The morph they refer to as "elongate" produces galls that are more elongate in shape than those of the other morph called "globular." The question immediately arose whether the presence of early and late transverse galls was related to the globular-elongate dimorphism. An analysis of the early and late transverse galls confirms the suspected relationship (Table 1). The late galls are larger than the early galls, and more spherical, as shown by the ratios of gall dimensions. The values in Table 1 resemble those of the sample from West Point, Georgia, shown in Table 3 of Senner and Sokal (1974). The early and late galls were significantly different for each character. Corroborating tests were run following methods developed by Senner and Sokal (1974). The gall dimensions and their ratios split a mixed sample of 71 galls into early and late classes fairly well. Only two galls would be misclassified by time of gall formation when the sample was split according to gall depth and only 4 galls would be so misclassified on the basis of length/width ratio. It is highly probable that the early and late galls correspond to the elongate and globular morphs, respectively.

Pemphigus populi-transversus Riley

This aphid has, as its summer host, plants belonging to the family Cruciferæ. Jones states that Populus balsamifera, P. monilifera, P. trichocarpa and P. fremontii have been mentioned as hosts. He also gives cabbage, turnip, mustard (Brassica nigra), cauliflower, broccoli, (B. oleracca botrytis), Brussels sprouts, rape, and several weeds belonging to the family cruciferæ as hosts of the subterranean forms. While this aphid has been reported as damaging certain cruciferous crops in the south, no damage in the northern portions of its range has been reported. In Utah this aphid was collected at Farmington, on June 28, 1923. At this time spring migrants and pupal nymphs were present in galls formed on the petiole near the leaf of cottonwood, Populus deltoides. Galls and stem-mothers apparently of this species, were collected at Santa Clara by Dr. H. J. Pack, during June, 1928.