Pemphigus betae

The aphid forms pouch-shaped galls on the leaf blades of its host; among its primary hosts are the balsam poplars, Populus section Tacamahaca (e.g., P. angustifolia James, P. balsamifera L.), and hybrids involving these species, and cottonwoods in Populus section Aigeiros (e.g., P. deltoides Marsh, P. fremontii S. Watson) (Fig. 1) (Palmer 1952; Harper 1959; Floate et al. 1997).

The taxonomic status of P. betae remains unclear. Pemphigus betae was originally described from specimens on sugarbeets, the gall form being unknown. Pemphigus balsamiferae Williams, described from the gall form, is currently considered a synonym of P. betae (Maxson 1916; Remaudiere and Remaudiere 1997). 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 balsamiferae Williams

Pemphigus betae Doane (questionable identification)

Collections. As winter hosts on Populus augustifolia and P. tacamahaca, in yellowish green to reddish pocketlike galls on underside with opening on upper side of leaves; as summer hosts on roots of both sugar and garden red beets (Beta vulgaris) and Chenopodium album, specimens apparently identical with this species taken on roots of Achillea sp., Agropyron sp., Aster multiflorus, Cycloloma atriplicifolium, head lettuce (Lactuca sativa), Poinsettia sp., Poly gonum aviculare, and Solidago sp. Throughout region. Fundatrices on Populus April 23 to July 10, apterous summer viviparae on summer hosts May 6 to Nov. 26, hiberating viviparae on summer hosts throughout the winter, alate viviparae on Populus July 4 to 11 and Sept. 23 to Oct. 28 and on summer hosts Aug. 27 to Nov. 23, sexuales on Populus Sept. 28 to Oct. 4; common often injurious. Fundatrix lives in gall with alate fundatrigeniae which leave for summer hosts, alate sexuparae return from the beet to the Populus where they deposit the sexuales.

Pemphigus betae Doane (= balsamiferae Williams)

Galls are yellowish green sometimes tinged with red, pocket-like, formed usually on the underside of the poplar leaf near its base, on or adjacent to the mid-rib, with little or no deformation of the leaf (Harper 1959a, Whitham 1978). The opening can be either on the upper side of the leaf or underneath along the mid-rib. Primary hosts are Populus angustifolia, P. balsamifera, or occasionally P. deltoides ssp. occidentalis or P. trichocarpa. Alatae (BL 1.5-2.1 mm) leave galls in late June-early August (Harper 1959b), to colonise roots of Beta vulgaris, and also perhaps on other Amaranthaceae (formerly Chenopodiaceae) such as Chenopodium album, and possibly Spinacia. Apterae on chenopods are yellowish aphids secreting white wax, with BL 1.9-2.4 mm. Anholocyclic populations can persist all year on secondary hosts (see Moran & Whitham 1988), and are widely distributed in North America. The life cycle was studied by Harper (1963) in southern Alberta, and by Moran & Whitham (1988) in Utah. This aphid's evolutionary ecology has been studied in some detail, including the territorial behaviour of first instar fundatrices in selection of galling sites (Whitham 1979), population dynamics in relation to galling site (Whitham 1978, 1980), genetics of resistance in the host plant (Paige & Capman 1993), induction of sexuparae (Moran et al. 1993a), and discrimination between host trees by returning sexuparae in autumn (Moran & Whitham 1990). However, interpretation of all this work is problematic as Foottit et al. (2010a) have demonstrated that there is a complex of Pemphigus species in western North America sharing the same cottonwood primary hosts. Taxonomic affinities with palaearctic populations of Pemphigus on chenopod roots (see P. fuscicornis) are unclear. See also Blackman & Eastop (2000).

Pemphigus betae

As with most host-alternating aphid species, the sugarbeet root aphid is restricted in its primary host range, but the secondary host range is more diverse. Pemphigus spp. prefer poplars in the genus Populus (Fig. 2) as their primary hosts (Blackman and Eastop 2006). Over the years, P. betae primary hosts have been identified as species within the Populus section Tacamahaca, including narrowleaf cottonwood (P. angustifolia James), balsam poplar (P. basamifera L.), and black cottonwood (P. trichocarpa Torr. & A. Gray) in North America (Parker 1915, Harper 1963, Whitham 1978, Floate et al. 1997, Dewar and Cooke 2006, Hein et al. 2009). Although there is some overlap in their geographical distribution, these primary hosts occupy relatively distinct regions in North America. For example, narrowleaf cottonwood is found primarily in the central and southern Rocky Mountain regions, the balsam poplar is found in the northern Rockies into Canada and extending east to the Great Lakes region, and the black cottonwood has a range stretching from Alaska, through western Canada, and primarily into the northwestern United States, but also sporadically down as far south as Baja, CA (U.S. Department of Agriculture [USDA] 2014). Additional ecological complexity of these aphid–primary host relationships was demonstrated by Floate et al. (1997) who found a dramatic increase in P. betae host acceptability for hybrids between the aphid’s primary hosts and other Populus spp.

Pemphigus betae Doane

Gall beside mid-rib on leaf of P. balsamifera or P. angustifolia (or, rarely, P. trichocarpa)

This species, which is a pest of beets, swiss chard, spinach, and lettuce, causes considerable damage each year to sugar beets in southern Alberta and in some areas of the United States. P. betae can spread curly top virus and virus yellows among sugar-beet plants (Bennett and Wallace, 1938; MacLean, 1953).

The galls are always on the leaf blades, usually next to the mid-ribs; generally there is only one per'leaf. Thev have been found in Alberta on the narrow-leaved cottonwood, P. mgustifolici; the balsam poplar, P. balsamifera; and, rarely, the black cottonwood P. trichocarpa. The fundatrix, which hatches from the overwintered egg, feeds near the mid-vein on the upper surface of the emerging leaf, causing the formation of a longitudinal depression, which increases in size to about half an inch long and a quarter of an inch deep (Fig. 1). Galls are usuallv green but may have a reddish tinge.

Records of the distribution of P. betae in Alberta are as follows (the year denotes the first record from the area): 1929, Picture Butte, beets, lamb'squarters, pigweed; 1934, Lethbridge( Hillspring, Barnwell, beets (MacNay, C. G. (in litt.) Entomology Division, Ottawa); 1950, Monarch, Coaldale, Magrath, Raymond, Beta wulgaris, Chenopodium album, poplars; 1954, Diamond City; 1956, Pincher Creek, Barons, Hays, Turin, Welling, Stirling, beets, lettuce, Populus balsamifera, P. angustifolia, P. trichocarpa; 1957, Lundbreck, Black Diamond, Coleman, poplars.

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 betae Doane

This insect is a native of the Rocky Mountain region, and is a rather general feeder upon the roots of plants during the summer season. The goosefoot family, especially sugar beets, garden beets and mangel wurtzels, are favorite food plants. Among our native plants and weeds, we have found this louse common upon the roots of Aster, goldenrod (Solidago), Iva xanthifolia, and lambsquarter, Chenopodium. While it does not seem necessary for this insect to take on a fall migratory habit, still, as near as we have been able to estimate, about one-half of the lice acquire wings during September and October and leave their summer hosts and fly to the cottonwoods. Apparently, only a small percentage ever find the desired host. In beet-growing sections it is common for these lice to fly in countless millions, like great swarms of ants, for- more than a month during the warmer portion of the day. Since the fall of 1910 we have known that this louse migrates to the cottonwoods, in large numbers in the fall to deposit the sexual males and females, but not until the past summer has it been definitely determined in what form this species appears upon the cottonwoods early in the summer. Mr. Asa C. Maxson, in charge of the experimental work in the Longmont district for the Great Western Sugar Company, who has been a collaborator with us in some plant louse studies, has succeeded the past summer in determining the form of gall produced by this louse upon the cottonwood leaves and in successfully colonizing the lice in large numbers upon the beets and in rearing from these colonies, the sexuparae. We extract from a report by Mr. Maxson upon his work as follows: "On May 4th . . . the larvae were located upon the upper side of the leaf which was light in color where the larvae were feeding, and showed a depression which, as it grew larger, entirely inclosed the insect and formed a gall on the under side of the leaf. This form of gall is produced by Pemphigus balsamiferae Williams."

Many observations by the writers tend to confirm the conclusions reached by Mr. Maxson whom we congratulate on the excellent life history work that he has done on this insect, which is one of the worst pests that the sugar beets have to contend against in the Rocky Mountain States.

It seems probable that Parker, in Journal of Economic Entomology, 1914, page 139, hit upon the correct gall for this louse, but referred to it on page 141 as by populicaulis Fitch, which produces a globular gall upon the petiole of the leaf. Furthermore, this gall occurs in the Middle and Eastern States, while P. betae seems to be strictly a Western species.

Pemphigus betæ Doane.

A pemphigid from beet roots grown at Pullman, Washington, was named "Pemphigus betae" and described by Doane in 1900. In 1910 Williams described Pemphigus balsamiferae. This aphid was taken at Squaw Creek, Nebraska, on Populus balsamifera. In 1914 the senior author discovered that the sugar-beet root-louse in Colorado is the summer and fall generations of P. balsamiferae from the narrow-leaved cottonwood, Populus angustifolia. Unless the beet is the host of two Pemphigus species and the one in Washington is different from the one feeding on beets in Colorado, P. balsamiferæ Williams, becomes a synonym of P. beta Doane. In this discussion P. balsamiferæ is considered the spring form of P. betae.

P. betae occurs on the balsam poplar within the western range of this tree and on Populus angustifolia where this tree occurs naturally. Its galls are located on the underside of the leaf. They may easily be confused with the galls of P. p.-venæ.

The following unpublished chapter in the life history of P. betae was worked out by the senior author in 1921.

Hibernating aphids were collected from the soil November 2d. These were confined in salve boxes in a greenhouse under ordinary greenhouse temperatures. The aphids collected November 2d. are designated the first generation. The second generation (young of the hibernating lice) appeared December 31st after nearly 2 months' inactivity on the part of the hibernating individuals. The third generation appeared January 21st; the fourth generation, February 24th ; the 5th, March 12th ; the 6th, March 24th; the 7th, April 8th, and the 8th, April 29th.

The age of the various generations when reproduction began was: second generation, 21 days old; third, 34 days; fourth, 16 days; fifth, 12 days; sixth, 15 days; and seventh, 21 days. The variation in ages is probably due to variations in temperature and the condition of the food supply. Low temperatures retard development and high temperatures quicken it.

The first, second, third, fourth, and fifth generations were all apterous viviparous females which began reproducing immediately upon becoming mature. The first alate forms (sexuparæ) appeared in the sixth generation. The sixth and seventh generations were composed of about equal numbers of apterous viviparous females and alate sexuparæ. The apterous females of the sixth and seventh generation began to reproduce as soon as mature. The offspring of the sixth generation were of four kinds. Those of the apterous forms were apterous viviparous females and sexuparæ; those of the sexuparæ, true males and females. The offspring of the seventh generation (the eighth generation) were of four kinds also. Those of the apterous viviparous females were apterous forms and sexuparæ. The fortner ceased feeding and became inactive upon reaching mature size. They sought out crevices in the soil where they became completely covered with the wax secreted by their wax glands. Those of the sexuparæ were true males and females. The hibernating forms of the eighth generation differ from the apterous forms of the sixth and seventh generations, since upon reaching sexual maturity they produce only apterous forms.

This change into hibernating forms appears to be biological function and not a temperature reaction.

This aphid has been collected in Utah from the following localities: Amalga, Benson, Brigham, Collinston, Cornish, Delta, Garland, Hoytsville, Hyde Park, Lehi, Lewiston, Logan, Madison, Millville, Richfield, Richmond, Salt Lake City, Smithfield, and Trenton.