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Identification & Distribution

The plump-bodied dark brown fundatrices of Anuraphis subterranea (not pictured) induce reddish leaf galls on pear (Pyrus communis) in spring. Brownish-black nymphs develop in the gall giving rise to alates which migrate to the secondary host, hogweed. There they form large colonies on the stem base and under leaf sheaths. These colonies are tented with earth by attending ants (see first picture below).

Adult apterae of Anuraphis subterranea on the secondary host are greenish-brown to pinkish-brown, and immatures are pink with faint greenish markings (see second picture below). Neither adults nor immatures are waxed (cf. Dysaphis species which are waxed to a greater or lesser extent). The antennae of the aptera are short with the terminal process of the last antennal segment longer than the base of that segment. Antennal segment III is usually slightly more than twice as long as segment IV (cf. Dysaphis species, which have antennal segment III slightly less than twice as long as IV). The dorsum has conspicuous longitudinal series of black dorso-lateral and marginal sclerites running from the anterior to the posterior tergites, and dark cross bars on tergites VI-VIII. There are large spinal and marginal tubercles on abdominal tergites I-VII. Anuraphis subterranea siphunculi are short and tapering and have close-set rows of minute fine spinules (these are very small!). The cauda of Anuraphis subterranea is helmet-shaped, not longer than its basal width in dorsal view, and has 11-12 hairs. The immatures are pale pink with greenish patches (this feature distinguishes Anuraphis subterranea from Anuraphis farfarae whose nymphs are yellowish-green). These immatures develop to brown emigrant alates. The body length of adult apterae is 2.3-3.5 mm.

Anuraphis subterranea alates (see third picture above) have a broad dark patch on abdominal tergites IV-VI. This patch is almost solid in spring migrants but is smaller, with a large window, in alates produced on the secondary host. The damage to the wings of the alate shown below is most likely caused by the attending ants which chew off the wings of alate aphids to prevent them leaving the colony.

The first two micrographs below show an adult aptera dorsal and ventral in isopropyl alcohol. The second two micrographs are a close-up of a siphunculus showing the transverse rows of minute spinules, and the cauda showing caudal hairs, again in alcohol.

The clarified slide mounts below show (first) an adult wingless female Anuraphis subterranea on the primary host, (second) an aptera on the secondary host, and (third) an alate female gynopara (a return, or autumn, migrant).

Micrographs of clarified mounts by permission of Roger Blackman, copyright AWP all rights reserved.

In spring Anuraphis subterranea fundatrices live in the rolled and crumpled leaves of their primary host pear (Pyrus). The living leaf tissue is turned characteristically reddish (cf. Anuraphis farfarae where the leaf tissue usually remains green). The species host alternates to summer hosts which are umbellifers such as hogweed (Heracleum sphondylium) and wild parsnip (Pastinaca sativa). Here Anuraphis subterranea live inside the lower leaf sheaths and at the stem bases where they are tented by the attending ants. Anuraphis subterranea is found throughout Europe, North Africa and eastward to Iran.

 

Biology & Ecology:

Life cycle

Brownish-black nymphs develop inside the red gall on pear. These all develop to alates and migrate to the secondary host, hogweed. Despite the occasional abundance of the aphid on the secondary host, the red gall on pear is seldom found and we have never observed it.

The secondary host, hogweed (Heracleum species) (see picture below) is fairly easy to distinguish from other umbellifers by the unequal petal sizes on flowers near the outside of the umbel.

The feeding habitat on the secondary host, a tiny chamber in the plant, termed a domatium, was described by Hansen et al. (2007). The stem-base leaf sheath is curved inwards, and the ants (usually Lasius niger) construct soil shelters on top of the domatium enclosing the aphids. This 'earth tent' blocks entry to aphid predators such as the 2-spot ladybird, Adalia bipunctata. As an adaptation to this environment, Anuraphis subterranea has an unusually long rostrum.

The picture above shows a partially removed domatium on hogweed revealing the colony of pear-hogweed aphid that we found at Winchelsea Beach in East Sussex.

The nymphs are a rather beautiful pink colour with greenish markings. Those below were living protected in a domatium in the hogweed root.

 

Other aphids on same host

Primary host:
Blackman & Eastop list 53 species of aphid as feeding on common pear (Pyrus communis) worldwide, and provide formal identification keys (Show World list). Of those aphid species, Baker (2015) lists 29 as occurring in Britain: (Show British list).

Secondary hosts:
 

Damage and control

The pear-hogweed aphid causes minimal damage to pear trees, and is not generally considered of any economic importance in this respect.

Anuraphis subterranea has been considered as an agent for biological control of the phototoxic invasive giant hogweed Heracleum mantegazzianum. Unfortunately the results of Hansen et al.'s (2006) experimental study on the three-way mutualistic relationship between the aphid Anuraphis subterranea, the plant Heracleum mantegazzianum and Lasius ants would appear to make this unlikely. They found a positive correlation between relative plant growth, ant activity, and the number of Anuraphis subterranea. Because of the restricted domatium size, Anuraphis subterranea populations were limited in growth, and consequently the damage they inflicted was limited. In contrast to the few other systems where three-partner mutualistic relationships have been described, these partners appeared to be well adapted to each other. The number of individuals of two leaf-feeding aphid species that were not attended by ants, namely Paramyzus heraclei and Cavariella theobaldi, were negatively correlated with the growth of giant hogweed in its native habitat.

Acknowledgements

Our particular thanks to Roger Blackman for images of his clarified slide mounts. We also thank Rye Harbour and King John's Nursery, East Sussex, for their kind assistance, and permission to sample.

Whilst we make every effort to ensure that identifications are correct, we cannot absolutely warranty their accuracy. We have mostly made 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

  • Hansen, S.O. et al. (2006). Mutualistic relationship beneficial for aphids and ants on giant hogweed (Heracleum mantegazzianum). Community Ecology 7(1), 43-52. Full text

  • Hansen, S.O. et al. (2007). Herbivorous arthropods on Heracleum mantegazzianum in its native and invaded distribution range. pp 170-188. In: Cock, M. et al. Ecology and management of giant hogweed (Heracleum mantegazzianum). Full text