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Identification & Distribution

Adult apterae of Protrama nr. radicis are pale to dark brownish-green with variable, usually highly fragmented, dark dorsal cross-bars (see first picture below). The siphuncular cones are dark brown. Their antennae are about half the length of the body, and the antennal terminal process is 0.50-0.61 times the length of the base of antennal segment VI (cf Protrama radicis which has the antennal terminal process 0.33-0.69 times the length of the base of the sixth antennal segment). The hind tarsus is 0.71-0.88 times the length of the hind tibia (cf Protrama radicis which has the second segment of hind tarsus 0.72-0.87 of length of hind tibia). The body length of adult Protrama nr. radicis apterae is 2.7-3.8 mm.

Our colony of Protrama nr. radicis produced a number of alates (see second picture above) - which are unknown for Protrama radicis sensu stricto. Protrama nr. radicis have forewings with a 1-3 branched media, and antennal segment III has 5-7 rhinaria.

Protrama nr. radicis does not host host alternate, but lives all year around in ant-attended colonies on roots of globe artichoke (Artemisia vulgaris) - and possibly other members of the Asteraceae. No sexual morphs are known. It is found in Britain, and possibly throughout Europe.

 

Biology & Ecology

Colony culture

The aphids described on this page were found feeding on the roots of some globe artichokes (Cynara cardunculus) in mid-November by one of our correspondents, Maria Fremlin. We received the plant (a compact root-mass, with some leaves, plus damp earth) with its aphids and attendendant ants wrapped in polythene via post on 21 November. Being lightly-sclerotized, we tentatively identified the aphids as Protrama flavescens but, being unable to find any we were sure were mature apterae, we repacked them and put them in a cool outhouse in the hope of obtaining such - re-inspecting the colony every few weeks.

By mid-December we were reasonably sure we had adults, albeit less certain of our initial identification: They looked like Protrama flavescens, but most of the measurements indicated Protrama radicis.

On 22 March, during an unusually warm spell of weather, we re-checked the bag - expecting to find a sticky mess and little else. To our surprise we found 3 alates (2 of which were dead), and the ants still attending their aphids - plus a thriving mass of Collembola (springtails). In the hope of producing more alates we re-sealed the culture until mid-April, at which point the contents being clearly in rapid decline, we broke the root apart and extracted the surviving adults.

Taxonomy

They were confirmed as a Protrama species, rather than Trama (Neotrama), since the antennal terminal process was 0.54 times the length of base of last segment, and bore 12 hairs in addition to the usual apical ones (the antennal terminal process of Trama species is less than 0.35 times the length of base of last segment, and has fewer than 6 additional hairs).

Siphuncular pores were present, and there was some dorsal sclerotization, albeit very fragmented. This sclerotization is visible on the wingless adult in alcohol (above) and, less clearly, on the live adult (below).

Having established this was a Protrama rather than Neotrama species, we compared dimensions of the second segment of the hind tarsus to the length of the hind tibia. This gave ratios of 0.71-0.88 times. This was remarkably similar to the recorded range for Protrama radicis, namely 0.72-0.87 times the length of the hind tibia (Blackman et al., in press).

Taxonomically the data indicate that this is Protrama radicis, but for several reasons we have labelled it as Protrama nr. radicis:

  1. Although the adult aptera is clearly 'alatoid' (the head and prothorax are clearly demarcated), the dorsal bars are hardly darkened and the sclerotization is fragmented. Yet Protrama radicis apterae usually have well-marked dorsal sclerotic bars.

  2. Alatae have never been recorded for Protrama radicis, yet the colony that we maintained for a couple of months produced several alatae (see picture above). Eastop (1953) did not rear out any alates from his Protrama colony on Cynara so in this respect his colony differed from ours, although several months elapsed before our colony produced any.

  1. Eastop (1953) found that specimens of Protrama radicis collected from Cynara refused to feed on the normal hosts (Cirsium and Centaurea), suggesting to him the possible existence of host races. We did unfortunately have the facilities to carry out any food trials on our colony of Protrama.

We conclude that the Protrama that our colleague Maria Fremlin, and Vic Eastop, found on globe artichoke (Cynara cardunculus) is most likely a different host race, and possibly a previously undescribed species (assuming they are one in the same).

A few more images of the different stages of this species are shown below. Immatures of Protrama nr. radicis) are similar in appearance to immatures of other Protrama species (see picture below).

The long rostrum of Trama species is shown in this head-on view of an immature Protrama.

The picture below shows two adults.

Ant attendance

The Protrama species was attended by ants - specifically the yellow meadow ant (Lasius flavus). The image below shows an ant imbibing honeydew from the anus of one aphid.

If the aphid colony was disturbed, the aphids would start dispersing. The ants then picked up the aphids in their jaws and moved them to a safer, more secluded, feeding site.

 

Other aphids on the same host

Whilst Protrama radicis (sensu lato) has been recorded from Cynara species, until now it does not seem to have been recorded from Cynara cardunculus.

Blackman & Eastop list 16 species of aphid as feeding on globe artichoke (Cynara cardunculus) worldwide, and provide formal identification keys.

Of those aphid species, Baker (2015) lists 13 as occurring in Britain: Aphis fabae, Aphis gossypii, Aphis solanella, Aphis spiraecola, Brachycaudus cardui, Capitophorus carduinus, Capitophorus elaeagni, Hyperomyzus lactucae, Macrosiphum euphorbiae, Myzus persicae, Trama troglodytes, Uroleucon jaceae and Uroleucon sonchi.

Acknowledgements

We are extremely grateful to Maria Fremlin who sent us live Protrama colonies on globe artichokes from an allotment in Colchester, Essex.

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

  • Blackman, R.L. et al. (in press). Aphids - Anoeciinae, Lachninae, Eriosomatinae, Phloeomyzinae, Thelaxinae, Hormaphidinae, Mindarinae. Handbooks for the Identification of British Insects 2(8). Royal Entomological Society of London.

  • Eastop, V. (1953). A study of the Tramini (Homoptera-Aphididae). Ecological Entomology 104(10), 385-413. Abstract