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Identification & Distribution

Adult apterae of Protaphis carlinae are dark blue-green, usually with reddish areas around the siphuncular bases. They have dark bars on the thoracic tergites and abdominal tergites VI to VIII, and dark patches on most of the other abdominal tergites. Both adults and immatures are wax-powdered. The antennal terminal process is 1.04-1.36 times as long as the base of antennal segment VI (cf. Protaphis terricola, which has the antennal process 0.80-0.95 times the base of that segment). Antennal segments III and IV are usually without rhinaria, and bear very short hairs, less than 0.3 times the basal diameter of antennal segment III (cf. Protaphis terricola, which usually has rhinaria on segments III & IV, and has somewhat longer hairs: 0.4-0.7 times the basal diameter of antennal segment III). Their siphunculi and cauda are very short. The cauda is pale or dusky, bluntly triangular, shorter than its basal width, and bears 10 or more hairs. The body length of adult apterae is 1.5-2.1 mm. Immature Protaphis carlinae are blue-green, with reddish areas around the siphuncular bases (cf. Protaphis terricola, which has light green immatures).

Note:
Blackman notes Protaphis carlinae is very similar to, and possibly synonymous with, Protaphis dudichi (recorded on roots of Matricaria and Tripleurospermum spp. in western Siberia, central and eastern Europe) albeit its appearance in life is unknown.

The alate Protaphis carlinae has fully sclerotized thoracic tergites, but is otherwise very similar to the aptera. The images below show an apterous and an alate adult in alcohol.

Protaphis carlinae has only been recorded feeding on the stem base and roots of carline thistles (Carlina spp.), especially the carline thistle (Carlina vulgaris) and the dwarf carline thistle (Carlina acaulis). Sexual forms develop in autumn, and the species overwinters as eggs. Protaphis carlinae are attended by ants. The species is present in south and eastern Europe, and is now known (from this report) to also be present in western Europe (southern England).

Our observations are the first UK records of this species.
First observedby: InfluentialPointsJuly 12, 2019at: Birling Gap, by Beachy Head, East Sussex
SecondJuly 23, 2019
ThirdSeptember 18, 2019

 

Biology & Ecology

Habitat

Osiadacz (2009) notes that, in the case of Protaphis species in Poland, it is their habitat - xerothermic grassland - that is especially rare, and not the host plant. In Poland the host plants of Protaphis species (such as Artemisia campestris, Carlina spp., Erigeron acris, Leontodon spp. and Centaureae spp) are relatively frequent. Although the aphids form large, ant-attended colonies, Osiadacz always found the aphids difficult to find and rare. The acidity of the soil has to be appropriate for the species, as has the degree of soil compaction - loose sand or gravel will not provide a suitable habitat.

We have so far only found the carline rosette aphid (Protaphis carlinae) on three occasions (in July & September) at one site in Britain - on the south coast at Birling Gap, East Sussex (see picture below). Colonised plants grew alongside well-trodden tracks, much used by tourists - the building in the background is Beachy Head lighthouse.

The vegetation is typical coastal downland, in other words xerothermic grassland, with low windswept bushes mainly of gorse Ulex spp.), short grass cropped by rabbits, and a scattering of downland flowers including carline thistles (Carlina vulgaris). The first picture below shows mature carline thistles in flower and the second picture shows young Carlina 'rosettes' in their first year of life.

Like all Protaphis species, Protaphis carlinae feeds at the stem base or roots of its host plant, where it is attended by ants. The aphids live close to the surface but are usually tented over with soil by the ants (see picture below).

We have only found colonies of Protaphis carlinae at the stem base and roots of 'rosette' stage carline thistles - in other words plants in their first year of life before they flower - but this may be because it is rather easier to see the ant-tenting over a rosette than around the base of a mature plant.

Life cycle

The overwintering eggs of Protaphis carlinae hatch in spring to give the founding stem mothers or fundatrices. These produce, by parthenogenetic reproduction, large numbers of offspring.

First and second instar larvae (see picture below) are pale green with a orange-red areas around and between their siphuncular bases.

Later-instar immatures (see pictures below) are dark blue-green, shading to pale green on the posterior tergites, with conspicuous dark crimson areas around and between the siphuncular bases.

The pictures above show (first) a third and (future) apterous fourth instar larva and (second) a (future) alate fourth instar larva. All instars of the immatures (see also pictures below) are rather lightly wax-powdered compared to the adults, which is not surprising because the wax has to be secreted again following each moult.

Adult apterae (see picture below) are similarly coloured to immatures, but the colours are more obscured by wax which accumulates over the adult's lifetime.

Among closely ant-tended species winged forms tend to be rare or unknown, and we only found winged forms on one occasion in mid-summer. The coloration of the abdomen may be completely obscured by the gray waxy deposit (see picture below).

Winged forms often have damaged wings, like the one pictured, most likely because the attending ants bite off their wings (see below) to prevent the alatae from leaving the colony (see Kunkel, 1973).

Ant attendance

Ant attendance is obligate for most Protaphis, and this certainly seems the case for Protaphis carlinae. The picture below shows an ant (possibly Lasius niger) which has just taken a droplet of honeydew from one of the aphids.

In the picture below an ant is guarding a colony of Protaphis carlinae, including an alate with a damaged wing.

We noted above that ants are known to bite the wings of alate aphids in order to prevent the alatae from leaving the colony, thus increasing the availability of honeydew to the ants. See also for Trama troglodytes. Note that ants can (and sometimes do) achieve the same objective by chemical means - a mandibular secretion of ants can inhibit alate development (Kleinjan & Mittler, 1975).

Natural enemies

The only predator we have so far found to be active in carline thistle rosette aphid colonies are wax-covered larvae of a Scymnus species of coccinellid, possibly Scymnus frontalis (see picture below). The brown head of the larva can be seen protruding from the waxy covering.

 

In some coccinellids alkaloids are known to constitute an effective defence against predators including ants and birds (Pasteels et al., 1973). However, only the aposematic coccinellids possess alkaloids - so Scymnus species (which are generally dull coloured) do not have this recourse to this chemical defense. Instead these coccinellids have wax-covered larvae. Völkl & Vohland (1996) tested the protective function of larval wax covers in two Scymnus species against predation and ant aggression. Although fourth instar larvae of larger ladybird species consumed Scymnus larvae independent of the presence or absence of waxes, by contrast, first-instar larvae had little success when attacking Scymnus larvae. Moreover, wax-covered Scymnus larvae survived attacks by ant workers significantly more often than larvae without wax covers. Agarwala & Yasuda (2001) demonstrated that the wax cover also provides an effective defence shield against predation from syrphid larvae.

The image above shows a Scymnus larva attacking a Protaphis carlinae. The aphid colony where we found the Scymnus larva was certainly ant-attended, but they did not seem to have interfered with the predatory activities of the Scymnus larva.

 

Other aphids on the same host

Blackman & Eastop list 7 species of aphid as feeding on carline thistle (Carlina vulgaris) worldwide, and provide formal identification keys (Show World list). Of those aphid species, Baker (2015) lists 5 as occurring in Britain (Show British list).

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

  • Agarwala, B.K. & Yasuda, H. (2001). Larval interactions in aphidophagous predators: effectiveness of wax cover as defence shield of Scymnus larvae against predation from syrphids. Entomologia Experimentalis et Applicata 100, 101-107. Full text

  • Kleinjan, J.E. & Mittler, T.E. (1975). A chemical influence of ants in wing development in aphids. Entomol. Exp. Appl. 18, 384-388. Abstract

  • Kunkel, H. (1973). Die Kotagabe der Aphiden (Aphidina, Hemiptera) unter Einfluss von Ameisen. Bonn. Zool. Beitr. 24, 105-121.

  • Osiadacz, B. et al. (2009). Rare aphid species /Hemiptera, Aphidoidea/ in Poland and the protection of biological diversity. Aphids and Other Hemipterous Insects 15, 49-59. Full text

  • Pasteels, J.M. et al. (1973). Distribution et activités des alcaloides défensifs des Coccinellidae. Journal of Insect Physiology 19, 1771-1784. Abstract

  • Völkl, W. & Vohland, K. (1996). Wax covers in larvae of two Scymnus species: Do they enhance coccinellid larval survival? Oecologia 107, 498-503. Abstract