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Eriosomatinae : Pemphigus populitransversus
 

 

Pemphigus populitransversus

Poplar petiole gall aphid, Cabbage root aphid

On this page: Identification, Life cycle & Distribution Biology & Ecology Gall maintenance Intergall migration Other aphids on the same host Damage & Control

Identification, Life cycle & Distribution

Overwintering eggs of Pemphigus populitransversus on eastern cottonwood (Populus deltoides) hatch in spring. Immature fundatrices feed on the leaf petioles of its host. This induces the swelling of tissues that form a hollow globular structure - the gall - that surrounds each fundatrix and her offspring (see first picture below). This gall is green, often with some reddish shading, and usually has an open transverse slit (cf. the gall of Pemphigus populicaulis, which has one or two small openings in the semi-spiral groove, that extends two-thirds of the diameter of the gall, formed by the twisting of the petiole upon itself; and cf. the gall of Pemphigus populi-ramulorum, which develops upon the side of tender growing twigs). The adult Pemphigus populitransversus fundatrix is whitish to pale dirty greenish yellow (see second picture below). She produces 150-200 heavily waxed offspring which develop (at least most of them) within the protective cover of the gall (see third picture below).

Note: There are (at least) three other Pemphigid gall makers, apart from those mentioned above, which use Populus deltoides as host: namely Pemphigus obesinymphae, Pemphigus tartareus (= Pemphigus junctisensoriatus) and Pemphigus nortonii. Their galls, especially those of Pemphigus obesinymphae, are difficult to distinguish from Pemphigus populitransversus so it is recommended that identification is checked using the emigrant alatae (see below). Also, according to Blackman (Aphids on world's plants) it is still unclear whether the name Pemphigus populitransversus is being applied to a single species or to two different species. Bird et al. (1979) found that two forms of the 'species' with differences in gall shape, phenology and morphology occur sympatrically on Populus deltoides over much of eastern USA.

First two images above by permission, copyright Claude Pilon, all rights reserved.
Third image above copyright Ansel Oommen, Bugwood.org under a cc-by-nc-sa licence.

Alate Pemphigus populitransversus (see first picture below) start to emerge in July, with most having exited by late August. Under a microscope these emigrant alatae can be discriminated from those of closely related species. On antennal segment VI Pemphigus populitransversus has an enlarged primary rhinarium, with islands, like that on V. This rhinarium is less than 0.05-0.08 mm long, and occupies under half of the length of base of antennal segment VI. There are 2-7 Secondary rhinaria on 2-7 antennal segment III, 0-1 on segment IV, rarely 1 on segment V but none of the base of segment VI (cf. Pemphigus tartareus, which has 10-15 secondary rhinaria on segment III, 4-5 on segment IV, 2-4 on segment V and 3-5 on the base of segment VI). Separation from Pemphigus obesinymphae requires examination of the embryos within the emigrant alatae. Embryos of Pemphigus populitransversus have the tip of the rostrum not extending beyond the first segment of their fore tarsi (cf. Pemphigus obesinymphae, where embryos in the emigrant alatae have the tip of their rostrum extending beyond first segment of the fore tarsi). The Pemphigus populitransversus alatae have small siphuncular pores present.

First image above by permission, copyright Claude Pilon, all rights reserved.
Second image above copyright Alton N. Sparks Jr., University of Georgia, Bugwood under a cc-by-nc-sa licence.

Emigrant Pemphigus populitransversus alatae found colonies of aphids on the roots of cabbage (Brassicaceae), where it can be a serious pest (Royer et al. 1988). Jones & Gillette (1918) describe the wingless viviparae as being a 'sordid pale yellow, with head, antennae, and legs dusky brown to blackish and the tarsi and eyes black". There were apparently no wax glands on the body. However, in Bugwood Sparks & Riley describe the nymphs that develop on Brassica roots as being covered with a bluish-white wax (see their picture, second above) giving them a grey appearance. In their native America sexuparae return to cottonwood in September-October to produce sexuales which lay overwintering eggs on the bark. In areas where it has been introduced, the population remains on the roots of the secondary host throughout the year as an anholocyclic population.

First image above copyright CBG Photography Group under a CC BY-NC-SA license.
Second image above copyright Ida Bartolini, Servicio Nacional de Sanidad Agraria, under a CC BY-NC-SA license.

Pemphigus populitransversus is recorded throughout most of North America east of the Rocky Mountains. It has also been reported on Populus species in Mexico, Chile, South Africa and the Azores, and as anholocyclic populations on Brassicaceae roots in New Zealand and England.

 

Biology & Ecology

Gall maintenance

Pemphigus aphids have developed an efficient way of handling their excreted honeydew (which is sticky, encourages mould, and is otherwise problematic). They produce a hydrophobic (=water-repellent) wax, which coats every element inside the gall: the gall itself, the aphids, and the honeydew droplets. This secreted powdery wax has three distinct roles: (i) it is hydrophobic; (ii) it creates a microscopically rough inner gall surface made of weakly compacted wax needles, making the gall ultra-hydrophobic; and (iii) it coats the honeydew droplets, converting them into 'liquid marbles'. This, virtually non-stick environment, is of vital importance to occupants of that enclosed space (Pike, 2002).

The benefits of this can be seen in a rare series of images shown below of immature Pemphigus populitransversus ejecting wax-covered honeydew marbles from the gall. Such behaviour is of course only possible for inhabitants of 'open' galls, such as those of Pemphigus populitransversus.

Images above by permission, copyright Claude Pilon, all rights reserved.

Aoki (1980) was the first to report the role of soldier aphids in cleaning their gall in addition to defense against predators. (A number of gall-dwelling aphid species are eusocial and have defensive 'soldier' forms, usually of first-instar nymphs.) Benton & Foster (1992) then provided detailed observations on how soldiers of Pemphigus spyrothecae are responsible for manipulating marbles out of the gall opening by kicking them, pushing them with their head, or backside, or walking on their surface in an effort to make the marbles roll. In this way, at peak aphid populations, roughly 10 mm3 of honeydew is removed from each gall per day. If honeydew removal is prevented by blocking their gall opening, 90% of the aphids inside die within 5 days. These and other studies led Smith (1999) to conclude that the primary role of wax secreted by these gall-dwelling aphids was to prevent the aphids becoming contaminated by their own secreted honeydew and that of other members of the colony.

Intergall migration

It seems that Pemphigus populitransversus does not only exploit the advantage of having an open gall for waste disposal. Setzer (1980) found that second generation aphids of Pemphigus populitransversus exhibit surprising amounts of within-gall diversity for allozyme phenotypes. The patterns of this diversity were inconsistent with meiotically produced variation (produced by simple random mutation among the siblings). He found that wrapping galls in cloth bags to prevent the intrusion of aphids from neighboring galls eliminated this otherwise-unexplained variation within cloth-bagged gall coloniess, indicating that this variation was caused by among-gall dispersal of immature aphids.

Images above by permission, copyright Claude Pilon, all rights reserved.

The image sequence above shows immature Pemphigus populitransversus fleeing from the camera flashes, having been caught 'exploring' outside their gall - possibly prior to moving to a neighboring one, if such be sufficently close. Intergall migration is also known to occur in the aphid Pachypappa marsupialis - for more on this see Aoki (1982).

 

Other aphids on the same host

Primary hosts

The main primary hosts of Pemphigus populitransversus are eastern cottonwood (Populus deltoides deltoides and plains cottonwood (Populus deltoides occidentalis) but this aphid is also recorded from Populus balsamifera, Populus fremontii and Populus tremuloides. It is sometimes recorded from other Populus spp. (including Populus nigra) but these are questionable records, particularly those from western cottonwoods (Populus angustifolia, Populus trichocarpa and Populus acuminata).

Secondary hosts

Pemphigus populitransversus is recorded from 4 species of the Brassica genus (Brassica napus, Brassica nigra, Brassica oleracea, Brassica rapa), 1 species of Arabis (Arabis blepharophylla), 1 species of Cardamine (Cardamine pratensis) and 1 species of Raphanus (Raphanus raphanistrum).

 

Damage and control

Pemphigus populitransversus colonizes the roots of leafy greens (Brassica oleracea didyma), beginning in the autumn of each year, which can result in economic losses. In Georgia the only season where root aphids have been observed in leafy greens has been in the autumn or winter on fall-planted crops. Sparks & Riley in Bugwood noted that the only damage observed has been contamination of turnip roots, but this generally is not a problem if roots are cleaned before marketing. Hence it is not regarded as a economically important pest for Georgia.

In southern Texas however, since the late 1940s Pemphigus populitransversus has been considered to be one of the major pests on cruciferous vegetable in the Rio Grande Valley. Royer (1988) studied the bionomics and control of Pemphigus populitransversus on cabbage in Texas. They found that Pemphigus populitransversus normally migrates from poplar trees to cruciferous vegetables in September, and migrates back to the trees in early spring of the coming year. Heavy infestations in Brassica crops planted in September can lead to yield loss in the form of stunted plants with reduced growth. Thus in southern states the main recommended cultural control has been to delay planting till later in the fall.

However, some root-feeding aphids continued to be found on cruciferous vegetables in late spring and early summer. Those aphids were identified as a different, but very similar, species: Pemphigus obesinymphae. Chen et al. (2009) used molecular methods for identification in their study of the population dynamics of these two Pemphigus species. The two species were found to occur on cabbage at different times of the year, but to overlap from October to June. From May to October both species migrated to their primary hosts. The apterous aphids found on cabbage in winter were mainly Pemphigus obesinymphae, whereas in early spring more apterous Pemphigus populitransversus were recovered.

Acknowledgements

We are especially grateful to Claude Pilon for pictures of Pemphigus populitransversus (for more of her excellent pictures see and, and).

Identification of specimens photographed by Claude Pilon was confirmed by Eric Maw by microscopic examination of preserved specimens. For taxonomic details we have used the keys and species accounts of Palmer (1952) and Hottes & Frison (1931) as well as Blackman & Eastop (1994) and Blackman & Eastop (2006). We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure provided by Blackman & Eastop (2006).

Useful weblinks

References

  • Aoki, S. (1980). Occurence of a simple labour in a gall aphid, Pemphigus dorocola (Homoptera: Pemphigidae). Konyu 48, 71-73.

  • Aoki, S. (1982). Soldiers and altruistic dispersal in aphids. In Breed et al. The Biology of Social Insects. Proceedings of the Ninth Congress of the International Union for the Study of Social Insects, August 1982.

  • Benton, T.G. & Foster, W.A. (1992). Altruistic housekeeping in a social aphid. Proceedings of the Royal Society of London, Series B 247, 199-202. Abstract

  • Bird, J. et al. (1979). The morphs of Pemphigus populitransversus: allocation methods, morphometrics, and distribution patterns. Ann. ent. Soc. Am. 72, 767-774. Abstract

  • Chen, N. et al. (2009). Molecular identification and population dynamics of two species of Pemphigus (Homoptera: Pemphigidae) on cabbage. Insect Science, 16, 115-124. Full text

  • Hottes, F.C. & Frison, T.H. (1931). The Plant Lice, or Aphiidae, of Illinois. Illinois Natural History Survey Bulletin 19(3), 123-447. Full text

  • Jones, T.H. & Gillette, C.P. (1918). Life history of Pemphigus populi-transversus. Journal of Agricultural Research 14(13), 577-594. Full text

  • Palmer, M.A. (1952). Aphids of the Rocky Mountain Region: including primarily Colorado and Utah, but also bordering area composed of southern Wyoming, southeastern Idaho and northern New Mexico. Full text

  • Pike, N. et al. (2002). How aphids loose their marbles. Proceedings of the Royal Society of London B 269(4), 1211-1215.Full text

  • Royer, T.A. et al. (1988) Bionomics and control of Pemphigus populitransversus Riley in Brassica oleracea in South Texas. Texas Agricultural Experiment Station Progress Report, 4556, 1-14.

  • Setzer, R.W. (1980). Intergall migration in the aphid genus Pemphigus. Annals of the Entomological Society of America 73(3), 327-331. Full text

  • Smith, R.G. (1999). Wax glands, wax production and the functional significance of wax use in three aphid species (Homoptera: Aphididae). Journal of Natural History 33(4), 513-530. Abstract