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).

Thecabius populi-conduplifolius (Cowen)

Pseudo Galls. Fundatrix solitary in leaf margin folded on underside; progeny living in colonies on underside of younger leaves folded under on midrib.

Collections. As winter host, in folded leaves of Populus “balsamifera” (probably P. candicans or P. deltoides) and P. sargenti as summer host on leaf bases of Ranunculus sp. Wyoming: Wheatland. Throughout Colorado and Utah. Fundatrices June 2 to 25, alate fundatrigeniae June 12 to Aug. 7 and alate sexuparae Sept. 21, apterous viviparae on Ranunculus Jan. 2 to April 23, alate vivi parae Sept. 13 to Oct. 4; rather common.

Chief Distinguishing Characters. Folded leaf pseudo gall

Thecabius affinis (Kaltenbach)

Galls occur on Populus spp., in May-June, mainly on P. nigra and its varieties, and are formed by folding of young leaves in half along mid-ribs; the outer, upper side of the leaf becomes blistered and yellowish or reddish (see influentialpoints.com/Gallery). These are secondary galls containing only the alatiform progeny of the fundatrix, which inhabits a small gall of its own formed by folding the edge of a leaf (fig. 131I).

T. affinis occurs on a wide range of Populus spp. throughout Europe and across Asia to east Siberia, Japan and Korea, and also in North America (see below).

COI barcode sequences have confirmed that T. affinis is present in North America (Skvarla et al. 2017). DNA data have also confirmed the existence of a separate North American species, Thecabius populiconduplifolius (Cowen), which has 2n=28 (Harper & Macdonald 1966). T. populiconduplifolius is virtually indistinguishable from T. affinis and has an identical biology, but with native poplars as primary hosts (Palmer 1952).

Thecabius populiconduplifolius (Cowen)

Galls on Lombardy poplar (Populus nigra L. var. italica Muenchhausen) Pseudogalls formed by folding of young terminal leaves of Lombardy poplar [also keys to Thecabius gravicornis]

Alates of this aphid were collected from pseudogalls similar to those already described for T. gravicornis above, on terminal leaves of Lombardy poplars in Pincourt, Ile Perrot. Only few alates were present, and these were present amongst large numbers of T. gravicornis alates. Separation of the alates of these two aphid species is readily possible on the structure of the antennae.

Because of the large numbers of leaves bearing pseudogalls and thus the very close association of the aphid species, it is quite possible that they may be variants of the same species, although they are currently regarded as separate. Harper (1966) collected aphids with asymmetrical antennae from pseudogalls on poplars in Alberta, one aphid showing characteristics of T. affinis and the other of T. populiconduplifolius.

T. populiconduplifolius was first reported from Populus monilifera Aiton (P. deltoides Marsh) in Colorado (Cowen 1895). Palmer (1952) also reported it from Colorado on Populus sargentii Dode, whilst Harper (1966) reported it from Populus balsamifera L. in Lethbridge, Alta. Gillette (1914) traced this aphid to populations on Ranunculus sp.

Thecabius populiconduplifolius Cowen

Pemphigus populiconduplifolius, Cowen, Hemiptera of Colorado, Bull. 31, Colo. Exp. Sta., p. 115, 1895. Hunter, Aphidida; of North America, p. 79, 1901. Gillette, Jour. Economic Ent. p. 355. 1909. Jackson, Cols. Hort. Soc. Vol. 22, p. 217, 1908. Contributions No. 29, Dep. Zool. and Ent., O. S. U., p. 217, 1908.
Pemphigus ranunculi n. sp., Davidson, Jour. Economic Ent. p. 372, 1910.
Pemphigus populiconduplifolius, Davidson, Jour. Economic Ent. p. 374, 1910.
Pemphigus californicus, Davidson, Jour, of Economic Ent. p. 414, 1911.
Pemphigus populiconduplifolius . Essig, Pom. Jour. Ent. p. 699, 1912.
Pemphigus californicus, Essig, Pom. Jour. Ent. pp. 699, and 700, 1912. Essig, Pom. Jour. Ent. p. 827, 1912.
Pemphigus populiconduplifolius. Patch, Bull. 213, Maine Exp. Sta. p. 76, 1913.

*These can hardly be populiconduplifolius, as the stem females were reported in both cases as being present in the colonies of developing lice, a condition which we have never found in Colorado where the types of the species were taken. Furthermore, I have a stem female from Massachusetts that was taken by Mr. L. C. Bragg, and it is readily distinguishable from any of the stem females that I have seen from Colorado by having remarkably thickened femora for all legs. The femora are very nearly twice as great in diameter as they are in the Colorado form and are of about the same length. Four winged migrants taken from Populus balsamifera (Ace. No. 47-10) in Maine by Dr. Edith M. Patch are before me, mounted in balsam. These seem to differ from Colorado examples principally by having weaker sensoria, which are also fewer in number, on the sixth joint of the antennae. I will suggest that this eastern form be known as Thecabius patchii, though it does not have the typical habit of most known examples of this genus of having the stem mother in a gall by herself.

The above literature may be briefly summarized as follows:

The original description by Mr. Cowen dealt with the alate fundatrigenia in the folded leaves of the cottonwoods with the mere mention of yellow apterous individuals, all from Colorado.

Hunter lists this species only.

The writer, in 1909, recorded the species from Massachusetts. Davidson, 1910, described the alate and apterous forms taken in California from the buttercup (Ranunculus Californicus) to which he gave the name ranunculi, but which is probably populiconduplifolius, as Mr. Bragg and Mr. Asa C. Maxson have repeatedly traced this species to the buttercup in Colorado, where it seems to be perfectly at home. On page 374 of the same paper Davidson records populiconduplifolius in the folded leaves of Populus trichocarpa and mentions seeing the stem mother.

Jackson merely quotes Cowen's original description. Davidson, finding the name ranunculi preoccupied, suggests californicus instead. Essig lists this species both as populiconduplifoliiis and californicus. Dr. Patch records several captures of this species in Maine on the leaves of Populus balsamifera and gives a figure showing the distribution of the wax glands of what she took to be the stem mother, and also an excellent figure of the antenna of the alate fundatrigenia, or summer migrant. This is a rather common but not abundant species in northern Colorado and the writer has also taken it at Wheatland, Wyoming, upon a broad-leaved cottonwood.

The fundatrix is never found in the leaves folded along the midrib in which the other lice occur, but is always found in a narrow fold on the margin of one of the first leaves to open and upon the under side, see figures 1 and 5a. The second generation, almost as soon as born, leave the pseudo-gall of the fundatrix and travel to the tenderest little opening leaves at the tip of the twig, where they locate, several to a leaf, upon the lower or ventral surfaces where they begin to feed, causing the leaves to fold along the midrib as shown at figure 5, b. Mr. Maxson in a letter makes the following statement in regard to his observations upon the early occurrence of the second brood:

"The first larvae of the second generation were observed June 18th. These were traced to the young leaves at the tips of the branches where they located on the underside. These leaves began to fold along the midrib and in a few days typical P. conduplifolius galls were formed."

This second brood all acquire wings and leave the cottonwoods and go to the buttercups. Ranunculus sp., so far as our observations go. At the present writing, December 24th, there are several thrifty colonies in the laboratory on buttercups where they have been since the migrants were put upon the plants in July. They attack, not the roots, but the crown and leaves and stems near the ground. The buttercup seems to be a permanent food plant for this species, upon which it seems to be able to live continuously throughout the year.

Thecabius populi-conduplifolius (Cowen).

This aphid folds the leaves of balsam poplar, Populus balsamifera and P. deltoides, producing a pseudogall along the midvein or parallel to it. The stem mothers may be found in galls near the margin of the leaf. The young of the stem mother do not remain in the gall with her, but migrate to the new leaves at the tips of the branches. All of the second generation become winged. They migrate to Ranunculus sp. where the third and several subsequent generations of apterous viviparous females are produced. These summer colonies give a cottony appearance to the base of the Ranunculus leaves and stems. The fall migrants (sexupara) appear during late summer and fall and migrate back to the cottonwoods where the sexual forms are produced.

Galls of the second generation are always on terminal leaves. However, late in the season, after the stem mother ceases producing, new terminal leaves are produced which do not become infested.

At Fruita, and along the stream below Capital Bridge, nearly all of the leaves on the young poplars were folded on June 27, 1926. By this time most of the aphids had migrated. Many of the aphids had been parasitized, but a few living specimens were obtained. These aphids were quite numerous in the galls at Randlett on July 14, 1927, and less so at the same time in the few collections made at Fort Duchesne and Vernal. Ordinarily, quite a number of aphids occur in each gall. When they were examined at St. George on July 9, 1925, only a few specimens remained in galls. Winged females were becoming abundant at Plain City, by June 15, 1928.

Thecabius populiconduplifolius Cowen

This species was first described from Populus monilifera Aiton (= P. deltoides Marsh) in Colorado (Cowen 1895). Palmer (1952) also reported it from Colorado on Populus sargentii Dode. In Canada T. populiconduplifolius has been found in New Brunswick on Populus balsamifera (M. E. MacGillivray, personal communication).

This species has been found on Populus balsamifera L. in a farm shelterbelt and in the St. Mary's River Valley near Lethbridge, Alberta. The fundatrix causes the leaf margin to fold under to form a gall (Fig. 3). Her offspring leave the gall and feed on the underside of newly emerging leaves causing the outer edges to fold inwards toward the centre (Fig. 4). These pseudogalls vary considerably in shape.

Palmer (1952) reported the summer host as Ranunculus L. in Colorado and California and considered Pemphigus ranunculi Davidson and P. californicus Davidson to be synonyms.

Palmer indicated that T. populiconduplifolius is similar to T. affinis (Kaltenbach) and that Mordvilko considered them to be inseparable. The species are separated in her key by the number of secondary sensoria on the sixth segment of the antennae of the fundatrigenia but she indicates that affinis is a European species. In a collection of aphids initially considered to be T. populiconduplifolius, from a few trees in one small area of southern Alberta, the author found specimens with characteristics of each species. In this collection some of the specimens were not bilaterally symmetrical and would have been placed in affinis on the basis of one antenna and populiconduplifolius on the basis of the other antenna.

Bodenheimer and Swirski (1957) reported the secondary host of affinis to be Ranunculus. As the secondary hosts of the two species are the same and some specimens have characteristics of both species, it appears that afinis and populiconduplifolius may be synonymous or perhaps that there is hybridization between the species.