InfluentialPoints.com
Biology, images, analysis, design...
Aphids Find them How to ID AphidBlog
"It has long been an axiom of mine that the little things are infinitely the most important" (Sherlock Holmes)

 

 

Identification & Distribution:

On the primary host, elm, Tetraneura ulmi develop within galls on the leaves. The galls are stalked, approximately bean-shaped, smooth and shiny, and coloured reddish-green and/or yellow (see first picture below). The fundatrix, which stimulates production of the gall, is light green with the head, thorax, antennae and legs dark and transverse bands of light wax across the abdomen and thorax (see second picture below).

 

The offspring of the Tetraneura ulmi fundatrix develop within the gall to winged viviparous alates. These developing alates within the gall are shown in the first picture below. The adult alates (not pictured here) have a shiny black head, thorax, antennae and legs, and greyish black abdominal segments. The body length of Tetraneura ulmi alates is 1.8-2.6 mm.

 

The adult apterae on the secondary host, grass roots, are readily identified, being pale orange yellow, yellowish white or reddish (see second picture above). The head, prothorax and appendages are brown, and the body is (sometimes) lightly dusted with wax.

 

The micrographs above show a lateral view (first picture) and dorsal view (second picture) of an adult aptera on the secondary host.

Tetraneura ulmi host alternates. The winged forms of the elm-grass root aphid emerge from elm galls (Ulmus spp.) in June-July to colonize roots of grasses (Poaceae). Populations without sexual forms occur commonly on secondary hosts. In September winged forms make a return migration to elm where they produce larvae which feed on the bark, and mature to apterous males and females. Fertilized females only lay one egg each. Tetraneura ulmi is found in Europe, across Asia to eastern Siberia, and has been introduced to North America.

 

Biology & Ecology:

We have found Tetraneura ulmi galls on English elm (Ulmus procera) quite widely in southern Britain, although never very commonly. The elm-grass root aphid is little-researched compared to many other tree aphids.

Urban (2003)  describes the bionomics and harmfulness of Tetraneura ulmi during an outbreak in elms in Moravia in 2002. The aphid was most abundant on Ulmus minor, much less so on Ulmus glabra and absent from Ulmus laevis. The number of galls per leaf varied from 1-21 galls, with an average of 2.5 per leaf. Immature fundatrices were killed by insect and other predators in the initial stage of the gall formation. In 7.0% galls, immature fundatrices died in later stages of development due to the effect of a protective activity of plant tissues. Fundatrices matured within 3-4 weeks from hatching (from mid-May).

After maturation the fundatrices produced on average 35.2 offspring. By the beginning of June, galls reached 10.8 mm in length and 6.2 mm in width. 73.3% of galls produced viable alates. There was as low mortality of offspring of the fundatrices caused by Anthocoris confusus, larvae of Syrphidae, caterpillars of Pyralidae, and birds.

The pictures below show early stages in the development of a gall.

 

Dolgormaa & Munkhtsetseg (2015)  looked at the bionomics of Tetraneura ulmi in Mongolia. Tetraneura ulmi overwinters either as fertilized eggs on elm (Ulmus pumilla) laid by females of the sexuales generation at the beginning of autumn, or as apterous viviparae on roots of secondary host. The eggs hatch from mid-May and the development of fundatrices in the gall lasts for 23 days. Fecundity of the fundatrices ranged from 4 to 22 larvae. On affected leaves from 1 to 8 galls were recorded with 4-22 aphids per gall.

There has been even less work on the ecology of Tetraneura ulmi on its secondary host, the roots of grasses. What has been done is mostly focused on the interactions with ants. The pictures below show elm-grass root aphids on the roots of grasses attended by Lasius ants.

Depa & Wojciechowski (2008)  looked in nests of various ant species especially Lasius flavus and Lasius niger in Poland. Within the nests of Lasius flavus 8 species of aphids were recorded, most commonly Tetraneura ulmi. Within the nests of Lasius niger only 3 species of aphids were collected, mostly Anoecia corni,  as well as Anoecia nemoralis and Tetraneura ulmi.  Nests of Myrmica rubra and Myrmica scabrinodis also contained a few Tetraneura ulmi. Although some authors consider Tetraneura ulmi to be anholocyclic (see below), Depa & Wojciechowski concluded that Tetraneura ulmi in nests of Lasius flavus was predominantly holocyclic. This was based on winged morphs being found in two colonies of Tetraneura ulmi, located in the oak-forest. There were no signs of ants biting the wings off the alate forms of aphids.

Ivens et al. (2012a)  studied four root aphid species (Tetraneura ulmi, Geioca utricularia, Forda marginata and Forda formicaria ) in saltmarsh in the Netherlands. The sparse available literature suggested that all lived anholocyclically on the roots of secondary host grasses (Festuca rubra, Agrostis spp. and Elytrigia maritima) inside ant mounds. However, Tetraneura ulmi may also be holocyclic at several sites in Northwestern Europe and Scandinavia so they started the study with the hypothesis that both types of life cycle may be present in the Dutch population. However, results of the study gave a strong indication for asexuality being the dominant mode of reproduction, so that populations consist of multiple clonal lineages.

Ivens et al. (2012b)  investigated aphid diversity within and between ant nest mounds. The three focal species (Geoica utricularia, Forda marginata and Tetraneura ulmi) had considerable clonal diversity at the population level. Yet more than half of the ant mounds contained just a single aphid species, a significantly higher percentage than expected from a random distribution. Lasius flavus 'husbandry' is characterized by low aphid 'livestock' diversity per colony, especially at the nest-chamber level, but it lacks the exclusive monocultures known from other cultivation mutualisms. The ants appear to eat most of the early instar aphids, so that adult aphids are unlikely to face limited phloem resources and scramble competition with other aphids. Ivens et al. suggest that such culling of carbohydrate-providing symbionts for protein ingestion may maintain maximal host yield per aphid while also benefitting the 'domesticated' aphids as long as their clone-mates reproduce successfully.

 

Other aphids on same host:

Primary hosts:

Blackman & Eastop list about 75 species of aphids  as feeding on elms worldwide, and provides formal identification keys for aphids on Ulmus.

Secondary hosts:
Paul (1977)  found at least 16 aphid species recorded on grass roots in Britain: Anoecia corni,  Anoecia furcata (= A. nemoralis), Anoecia major, Anoecia (Paranoecia) pskovica Mordvilko, Anoecia vagans (= Anoecia willcocksi), Anoecia zirnitsi, Aploneura lentisci,  Baizongia pistaceae (=Pemphigus cornicularius), Forda formicaria,  Forda marginata, Geioca setulosa, Geioca utricularia, Paracletus cimiciformis, Rhopalosiphum insertum,  Smynthurodes betae and Tetroneura ulmi.

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

  •  Alvarez, R. et al. (2013). Histological study of galls induced by aphids on leaves of Ulmus minor: Tetraneura ulmi induces globose galls and Eriosoma ulmi induces pseudogalls. Arthropod-Plant Interactions 7, 643-650. Full text 

  •  Depa & Wojciechowski (2008) Ant-root aphid relations in different plant associations. Polish Journal of Entomology 77, 151-163. Full text 

  •  Dolgormaa, B. & Munkhtsetseg, B.(2015). Tetraneura ulmi Linnaeus, 1758 (Homoptera, Aphididae) on elm (Ulmus pumila) as its primary pest. Journal of agricultural sciences 15(02): 143-146. Full text 

  •  Ivens, A.B.F. et al. (2012a). Reproduction and dispersal in an ant-associated root aphid community. Molecular Ecology (2012). Full text 

  •  Ivens, A.B.F. et al. (2012b). Ants farm subterranean aphids mostly in single clone groups - an example of prudent husbandry for carbohydrates and proteins? BMC Evolutionary Biology 12: 106. Full text 

  •  Kmiec, K. & Kot, I. (2003). Tetraneura ulmi (L.) (Hemiptera, Eriosomatinae) on elm as its primary host. Aphids and Other Hemipterous insects 13, 145-149. Full text 

  •  Urban, J. (2003). Bionomics and harmfulness of Tetraneura ulmi (L.) (Aphidinea, Pemphigidae) in elms. Journal of Forest Science 49(4), 159-181. Full text 

 

Useful weblinks