Pemphigus populivenae Fitch Homoptera Aphididae

Natural History

Distribution. There has been considerable disagreement over the status of the Pemphigus species associated with crops in the plant family Chenopodia-ceae. Pemphigus betae Doane and P. populivenae Fitch are the names used most commonly in conjunction with this pest, though only one species with different forms or biotypes may be involved. Sugarbeet root aphid is native, and found principally in the range occupied by narrow-leaved poplar, Populus angustifo-lia—the principal overwintering host in the sexual life cycle. As a pest, it ranges principally the western states and provinces, including the Great Plains area. (See color figure 155.)

Host Plants. During the summer moths sugarbeet root aphid usually develops on roots of plants in the family Chenopodiaceae. Thus, the principal crops affected are beet, chard, quinoa, spinach, and sugar-beet. Weeds, particularly lambsquarters, Chenopodium album, and redroot pigweed, Amaranthus retroflexus, but also dock, Rumex spp., and smartweed, Polygonum spp., also support sugarbeet root aphid. Many crops and weeds have been reported to be summer hosts, but most old records are suspect owing to the difficulty in distinguishing among the several similar-appearing Pemphigus spp. Of 31 species of plants tested under greenhouse conditions, Harper (1963) cultured aphids readily on beet and sugarbeet, whereas chard and spinach were less suitable, and alfalfa was a poor host; the other species were unsuitable.

The overwintering, or primary, hosts of sugarbeet root aphid are poplar trees, primarily narrow-leaved cottonwood, Populus angustifolia, and balsam poplar, P. balsamifera, though in California P. trichocarpa is a suitable host. The Pemphigus form designated betae is reported to create leaf galls on the underside of the leaf blade and has an opening from the gall on the upper surface of the leaf. In contrast, the form designated populi-venae is reported to create leaf galls on the upper surface of the leaf and has the opening on the lower leaf surface.

Natural Enemies. Many predators feed on these aphids, both within the gall and below-ground. Among the predators found in galls are the flower fly Syrphus bigelowi Curran (Diptera: Syrphidae); Leu-copis pemphigae Malloch (Diptera: Chamaemiidae); and the lady beetle Scymnus sp. (Coleoptera: Coccinel-lidae). Found below-ground feeding on aphids are Scymnus spp. and Hippodamia convergens Guerin-Meneville (both Coleoptera: Coccinellidae); Thaumato-myia glabra (Meigen) (Diptera: Chloropidae); and several genera and species of flower flies (Diptera: Syrphidae). In the autumn, aphid dispersants to poplar trees fall prey to numerous predators including various ants (Hymenoptera: Formicidae); the pirate bug Anthocoris antevolens White (Hemiptera: Anthocori-dae); and such lady beetles as Coccinella spp. and Adalia bipunctata Say (all Coleoptera: Coccinellidae). Of all the natural enemies, the fly T. glabra is perhaps most frequently associated with root aphid colonies, but there is no evidence that it regulates aphid populations. A fungal disease, Erynia neoaphidis, sometimes causes epizeotics, and seemingly causes aphids to ascend to the soil surface (Summers and Newton, 1989).

Life Cycle and Description. Sugarbeet root aphid passes the winter in two forms, either as eggs on poplar trees or as wingless parthenogenetic females on the roots of plants. Those overwintering in the egg stage hatch in early spring, aphids feed on the overwintering host, and their offspring disperse. Several parthenogenetic generations occur annually on the summer or secondary host. In the autumn the aphids disperse back to poplars, produce sexual forms, and after mating the female produces an overwintering egg. In Alberta, hatching occurs in April, offspring are produced in June and July, dispersal to beets occurs in late June and July, dispersal back to poplars and production of sexual forms begins in September, and eggs are produced soon thereafter.

As noted earlier, however, some individuals fail to disperse to poplars, and remain below-ground on roots throughout the winter. Maxson (1948) reported that the aphids developing from overwintering females produced seven generations in Colorado. He found that there were three wingless generations on beet during the spring, followed by three additional generations consisting of both winged and wingless forms. The wingless aphids remained on the beets, forming the basis of the adult-overwintering population, whereas the winged aphids dispersed to poplar trees. The seventh generation is comprised of males and females; the females deposit overwintering eggs in cracks and crevices of poplar bark.

  1. The eggs overwinter on and beneath the bark of poplar trees, often in the lower regions of the trees. The egg is white initially, becoming yellowish-white with time, and then black. The elliptical egg measures about 0.54 mm long and 0.26 mm wide. The egg is usually deposited in a mass of filamentous waxy material. Females produce only a single egg, which must be exposed to cold weather before it will hatch.
  2. The nymphs, which display four instars, are pale-yellow to dark-greenish.
  3. The adult developing from an overwintering egg is wingless (apterous) and parthenogenetic, producing nymphs without mating. She is yellowish-green, with dark appendages. The body measures 2.32.5 mm long, and some wax secretion is found on the abdomen. This form feeds at the base of the leaf blade on poplar trees, and induces formation of a swelling or gall. The gall occurs along the midrib and is hollow. This structure provides protection and nourishment for both the adult and her offspring. The gall can only be induced to form on young, growing leaves. This female remains within the gall and continues to reproduce for 4-6 weeks. The fecundity of these females is estimated to average 163 nymphs, with some individuals producing over 200 offspring.

The offspring of the first females are winged (alate) and parthenogenetic. These aphids have a black head and thorax, and a yellowish or greenish abdomen. The appendages are dark. The body measures about 15 mm long. The wings are unmarked except for a dark area along the leading edge of the forewing. After dispersing from the poplar gall, these females each produce an average of 13.3 nymphs (range 11-16 nymphs), which are deposited on summer-host plants.

Additional generations of parthenogenetically reproducing apterous females occur on the summer hosts. This is the form that is damaging to crops. It is whitish to yellowish-green, with dark appendages and a dark head. A great amount of white, waxy, hair-like secretion is present on the abdomen. This form measures 1.5-2.5 mm long. The ability of this form to create colonies on beet and other susceptible plants is apparently related to their ability to gain access to plant roots. Plants growing in dry soil, especially in heavy soil, are most susceptible to infestation because cracks forming in the soil provide the aphids with ready access to the roots. The reproductive ability of this form has not been determined under field conditions, but Harper (1963) showed that a single aphid feeding below-ground for six weeks could result in a population of several hundred to over 1000 aphids. Under laboratory conditions mean fecundity was about 5065 progeny per female, depending on temperature (Campbell and Hutchison, 1995). The optimal temperature for reproduction is about 25-27°C. This form of the aphid, unlike most aphid species, seems unable to produce winged aphids that disperse to other summer hosts.

Late in the season the aphids on the summer hosts produce a winged parthenogenetic form that disperses to poplar and produces 5-6 offspring. This form greatly resembles the winged forms produced by the gall-forming females, but may be even darker in color, and bears tufts of waxy secretion on the thorax. The progeny of these aphids are sexual forms: males and oviparous females. This form can be produced both by summer populations derived from eggs overwintering on poplar and derived from adults overwintering below-ground on roots.

The sexual forms lack wings and functional mouth-parts. The female is yellowish-green with a dusky head and thorax. The appendages are whitish. The body measures only about 0.8 mm long. The males are even smaller, measuring about 0.6 mm long. They are yellowish-brown, with darker appendages. They mate and the female deposits her egg in September or October in bark cracks or beneath loose bark. Each female deposits only one egg. The females are larger than the males. The females and males may live for 8-12 and 3-5 days, respectively.

Pemphigus Populi Venae Betae
Adult female sugarbeet root aphid, wingless form.

The biology of sugarbeet root aphid was described by Grigarick and Lange (1962) and Harper (1963). Rearing was described by Campbell and Hutchison (1995). Sugarbeet root aphid was included in the keys by Palmer (1952), Smith (1981), and Blackman and Eastop (1984).

Damage

Aphids infest the roots of summer-host plants. Infested roots are unable to take up adequate water and nutrients, disrupting normal plant growth. The principal signs of infestation are yellowing and wilting of the above-ground portions of the plant. Root size and sugar content are decreased. These aphids also transmit beet curly top, beet mosaic, and beet yellows virus.

Management

Infested beets and spinach are easily detected by the presence of the bluish-white, filamentous masses of aphids on the roots. Such occurrences are rare except where host plants are grown continuously. Complete removal of summer-host plants greatly disrupts the population cycle, alleviating the need for aphid suppression. Summers and Newton (1989) recommended a three-year period between susceptible crops. Irrigation can be used to prevent soil from cracking, thus depriving aphids of easy access to the roots. Insecticides applied to the soil at planting or shortly afterward will eliminate damage.

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