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Identification & Distribution:

In spring, Pemphigus bursarius form yellowish or reddish pouch-shaped galls (see first picture below) on the petioles of the leaves of their primary host, poplar (mainly Populus nigra). There may be more than one gall per petiole and the leaf lamina may curl and yellow.

 

Inside the gall the developing Pemphigus bursarius fundatrix (see second picture above) is green with brown head and legs, wax covered and has no siphunculi. The 4-segmented antennae of the mature fundatrix are about 0.12-0.15 times the length of the body. The fundatrix then produces large numbers of alate offspring (see picture below) which leave the gall in late May.

The winged viviparae (see pictures below) that emerge from these galls are greyish-green or greyish-brown with small siphuncular pores and are lightly covered with wax powder.

Their antennae are 0.33-0.4 times the length of the body and have a distinct terminal process. When the antennae are 6-segmented, the third antennal segment is 2.09-2.65 times longer than the fourth antennal segment (cf. Pemphigus gairi  where the the third antennal segment is 1.53-2.00 times longer than the fourth antennal segment). There is brown shadowing around the wing veins.

Pemphigus bursarius host alternates between poplar and members of the daisy family (Asteraceae), especially lettuce. In summer they live on the roots of the secondary host where they can be a serious pest of lettuce. Its distribution is almost cosmopolitan being found in Europe, western and central Asia, the Americas, northern and southern Africa and (possibly) Australia and New Zealand.

 

Biology & Ecology

Life cycle
Dunn (1959)  described the biology of the lettuce root aphid. Its favourite primary host is Lombardy poplar. Fundatrices hatch in spring from eggs that have overwintered on this host, and their feeding activity causes the development of hollow, flask-shaped galls on the leaf petioles. The first picture below shows the gall at an early stage of development, the second picture shows it more advanced.

 

A fundatrix becomes enclosed within a gall, where it matures (see picture below), and gives rise to between 100 and 250 young.

One problem faced by all gall dwellers is elimation of waste products. Pemphigus bursarius deal with this by coating each 'marble' of honeydew with wax (Pike et al. (2002). ).

The wax-covered honeydew 'marbles' can be seen in the two pictures above. Offspring of the fundatrix are all potential alatae, and upon developing wings they leave the gall and migrate to lettuce and other secondary hosts. Secondary hosts belong to the Asteraceae. Lettuce sown between mid-April and the end of May is most severely attacked, while lettuce sown in July escapes attack. Lettuce is preferred by the progeny of the fundatrix, but Lapsana communis and Sonchus asper may also host big colonies of Pemphigus bursarius on their roots. The size of the mature apterae varies between hosts and is largest on lettuce and Sonchus asper.

The picture below shows a developing alate living on the roots of lettuce.

All winged aphids produced on the secondary hosts are sexuparae and fly back to poplar. The sexuparae begin appearing on lettuce from about the last week in August. They generally come up to the soil surface and settle around the collar of the host plant, to mature and develop wings. Having flown back to the primary host, the sexuparae seek out crevices in the bark where they produce non-feeding sexual forms. The ovipara contains one egg, and after mating she crawls as far into a bark crevice as possible and oviposits.

But Dunn (1959)  found that some aphids on the roots of a summer host did not return to poplar. They instead successfully overwintered even though the (annual) host plant had died, and were then able to colonize the roots of a spring planted lettuce crop. Philips et al (1999)  investigated the biology and overwintering success of these asexual apterae. Both temperature and photoperiod are important in morph determination. The highest number of apterae (approximately 50% of progeny) was produced at 20°C, 18 hours light, 6 hours dark. Very few apterae were produced in an alatae-inducing environment, but the proportion increased over successive generations. Apterae remaining in the soil in the autumn overwintered successfully in large numbers and were able to reinfest directly the root systems of newly planted lettuce grown in the same field in the following growing season. Overwintered asexual populations also produced alates in July, which were able to colonise other lettuce plants, indicating that they were not sexuparae. Hence, Pemphigus bursarius can avoid the ecological dead-end that would occur through local patch extinction. Clones can therefore persist indefinitely as both asexual apterae and alatae without the need to return to poplar and undergo the sexual phase of the life-cycle.

Miller et al. (2005)  sought evidence for the existence of genetically distinct populations, associated with different secondary hosts, in Pemphigus bursarius. Microsatellite markers revealed that genetically distinct populations were present on three different secondary host species. Evidence was found for a distinct, cyclically parthenogenetic population that exploited lettuce (Lactuca sativa) as its secondary host. In contrast, populations associated with scentless mayweed (Matricaria inodora) appeared to be largely composed of obligate parthenogens or may even have been another species of Pemphigus. Populations on nipplewort (Lapsana communis) appeared to be a mixture of cyclical and obligate parthenogens and were more genetically heterogeneous than those on other secondary hosts, possibly due to founder effects.

Natural enemies

Dunn (1960)  described the natural enemies of Pemphigus bursarius. It suffers little from parasites and only fundatrices have been found attacked. The only species reared from parasitised individuals was the Pteromalid, Pachyneuron sp., which was assumed to be hyperparasitic. When the galls open at migration time, syrphid larvae and anthocorids can enter and attack the contents. Anthocoris nemorum and Anthocoris nemoralis are the main predators at this stage. Before they begin feeding, they kill all the aphids within a gall extremely quickly and efficiently. It is suggested that the aphids may be killed by a secretion from the stink glands of the anthocorids working as a fumigant within the confines of the gall. Several staphylinids and carabids are frequently associated with subterranean colonies of Pemphigus bursarius and are almost certainly predators. The larvae of two chloropids, Thaumatomyia glabra and Thaumatomyia notata, are common predators of Pemphigus bursarius in the soil. The alate sexuparae, both before they leave the lettuce plants and on their arrival on poplar, are attacked by three species of coccinellid.

 

Other aphids on same host:

Blackman & Eastop list 40 species of aphid  as feeding on Black, or Lombardy, poplar (Populus nigra) worldwide, and provide formal identification keys.

Of those aphid species, Baker (2015)  lists 17 as occurring in Britain: Aulacorthum solani,  Chaitophorus leucomelas,  Chaitophorus populeti,  Chaitophorus populialbae,  Pemphigus bursarius, Pemphigus gairi,  Pemphigus phenax, Pemphigus populi, Pemphigus populinigrae, Pemphigus protospirae,  Phloeomyzus passerinii, Pterocomma populeum,  Pterocomma tremulae,  Stomaphis longirostris, Thecabius affinis,  Thecabius lysimachiae, and Tuberolachnus salignus. 

Acknowledgements

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994)  and Blackman & Eastop (2006)  supplemented with Blackman (1974) , Stroyan (1977) , Stroyan (1984) , Blackman & Eastop (1984) , Heie (1980-1995) , Dixon & Thieme (2007)  and Blackman (2010) . 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

  •  Philips, S.W. et al. (1959). Escaping an ecological dead-end: asexual overwintering and morph determination in the lettuce root aphid Pemphigus bursarius L. Ecological Entomology 24 (3), 336-344. Abstract 

  •  Dunn, J.A. (1959). The biology of lettuce root aphid. Annals of Applied Biology 47 (3, 475-491. Abstract 

  •  Dunn, J.A. (1959). The survival in soil of apterae of the lettuce root aphid, Pemphigus bursarius (L.).. Annals of Applied Biology 47 (4), 766-771`. Abstract 

  •  Dunn, J.A. (1960). The natural enemies of the lettuce root aphid, Pemphigus bursarius (L.). Bulletin of entomological Research 51 (2), 271-278. Abstract 

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