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Identification & Distribution:

Adult apterae of Protrama radicis are dirty-white to pale-yellow or pale brownish-green. Each segment of the dorsum has a transverse dark sclerotized bar (cf. Trama species which have no dark bars on the dorsum of the aptera). The bars may be more strongly sclerotized (see first picture below, thistle race) or rather less sclerotized (see second picture below, artichoke race). The head and appendages are dark. The antennal terminal process of Protrama radicis is 0.33-0.69 times the length of the base of the sixth antennal segment. The hind tarsus is 0.72-0.87 times the length of the hind tibia (cf. Protrama flavescens where the hind tarsus is only 0.59-0.70 times as long as the hind tibia). Siphunculi are present as pores placed on small brown cones. The body length of the adult aptera is 2.5-3.4 mm. The immatures are yellow brown with small siphuncular pores and resemble the immatures of Trama species.

Until now, only apterae and alatoid apterae have been described - alate Protrama radicis have been unknown. But we have recently reared alatae from a host race of Protrama radicis living on globe artichoke (see third picture above). The alate has sclerotized dorsal bars not quite reaching the marginal sclerites on most or all of the abdominal segments.

The images of preserved Protrama radicis below show (first) an adult aptera from thistle, (second) an adult aptera from globe artichoke and (third) an alate from globe artichoke.

Protrama radicis lives in ant attended colonies on the roots of various Asteraceae, especially thistles (Cirsium and Carduus) but also Arctium, Centaurea, and Cynara. They feed on the roots close to the soil surface. They reproduce parthenogenetically throughout the year, and no sexual morphs have been found.

 

Biology & Ecology

Host race on thistle

We first found Protrama radicis in August 2018 on the root of spear thistle (Cirsium vulgare) on Winchelsea Beach in East Sussex, very close to where we found Trama maritima on Picris echioides in 2016. Many of the spear thistle there had been ant-tented with sand grains and plant fragments by colonies of the short-haired thistle aphid (Brachycaudus lateralis). One tented spear thistle in 2018 instead had a large colony of Protrama radicis on the roots, just below the stem base. The picture below shows an adult (centre) surrounded by immatures.

The sclerotized dorsal bars can be seen more easily on the specimen below.

Immature Protrama radicis (see picture below) are usually a little more orange-yellow than those of Trama maritima.

Alternatively they may be light green (see picture below).

We have not found any alatae of this host race.

Host race on globe artichoke

- Colony culture

Our colony of Protrama radicis feeding on globe artichokes was derived from aphids 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 attendant ants wrapped in polythene via post on 21 November. Being lightly-sclerotized, we thought the aphids might be 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: Although they were only lightly sclerotized, most of the measurements indicated they were 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 fully-winged 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 of these 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 adult apterae.

- Taxonomy

The aphids on globe artichoke 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).

- Life cycle and presence of alatae

In the sample taken in November, most if not all the aphids were immatures. This strongly suggests that the species overwinters parthenogenetically, and no sexual forms have been found of this species. The immatures (see picture below) are similar in appearance to immatures of other Tramini species.

The long rostrum of Trama species is shown in this head-on view of an immature Protrama (see picture below).

The picture below shows two alatoid adults - note that the head is clearly demarcated from the rather sclerotized prothorax. True adult apterae of Protrama radicis are very rare.

Paul (1977) says that alatae Protrama radicis are rare, but both Eastop (1953) and Blackman et al. (in press) say that alatae have never been recorded for this species. Nevertheless, the colony that we maintained for a couple of months did produce several alatae (see picture below).

True Protrama radicis alatae have not been recorded previously (Blackman & Eastop, 2019).
First observedby: Influential Points22 March 2019in culture, originating from an allotment in Colchester, Essex, UK

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 not unfortunately have the facilities to carry out any food trials on our colony of Protrama, but conclude that the Protrama found by Vic Eastop and by our colleague Maria Fremlin most likely belonged to the same globe artichoke host race.

- Ant attendance

As with the aphids on thistle root, Protrama radicis on globe artichoke 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 same host:

Acknowledgements

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

We also thank Roger Blackman for his help in identifying them, and Rye Harbour Nature Reserve 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

  • 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.

  • Paul, R.G. (1977). Aspects of the biology and taxonomy of British myrmecophilous root aphids. PhD thesis. Imperial College, London. Full text