Aphis vitalbae

Identification & Distribution

The dorsum of adult Aphis vitalbae apterae has no wax (cf. Aphis clematidis, which is covered with powdery wax). The colour of the dorsum varies from very dark green (see first picture below) to mottled dark and pale green to pale green or yellowish (see second picture below). The antennae are pale, except for segment VI which has both the base and the terminal process darkened (cf. Myzus varians, which has conspicuously banded antennae). The antennal terminal process is 1.7-3.5 times the length of the base of antennal segment VI. The apical rostral segment is 1.1-1.7 times longer than the second segment of the hind tarsus (cf. Aphis clematidis, which has the apical rostral segment 0.75-1.0 times longer than the second segment of the hind tarsus). The siphunculi are either completely pale or dusky/dark at the apices (but see below for more discussion on this), and are 1.3-2.1 times as long as the cauda. The cauda is pale or dusky and is 0.17-0.21 mm long. The body length of the adult Aphis vitalbae aptera is 1.2-1.9 mm. Immature Aphis vitalbae show the same range of colour variation, but may show some light wax dusting.

Blackman (pers. comm) compared Aphis vitalbae from England, Austria, Italy and Bulgaria, and the pigmentation of the siphunculi was indeed surprisingly variable, with some of those from Italy having dark tips, and others dark enough to possibly appear black in life (including one ovipara). However, none of them had any of the dark dorsal markings of some of those pictured by Halaj. Halaj (pers. comm.) suggested that some of our specimens could be Aphis clematidis, but Roger Blackman of the British Museum (Natural History) has now confirmed the identity of our specimens as Aphis vitalbae following preparation of clarified mounts and measurement of the length of the apical rostral segment relative to the length of the second segment of the hind tarsus.

Aphis vitalbae feeds on the shoot tips, petioles and undersides of leaves of Clematis. It does not host alternate, but remains on clematis all year. In southern Europe and in England it is attended by ants. Oviparae and males have been recorded in Poland. Until recently Aphis vitalbae has been regarded as a southern European species, occurring in France, Greece, Italy and Spain. Since the 1960s (possibly earlier) the species has expanded its range northwards to include Bulgaria, Rumania, the Czech Republic, Poland, and Georgia. There are no previous published records this species in Britain, but the Natural History Museum holds two such records from 1945 and 2011. We have so far only found it in one British location on clematis growing in an industrial estate in Andover, Hampshire.

Our observations, all from the same location, comprise the third set of documented records for UK.
First observed	by: R.S. Bagnall	June, 1945	at: Box Hill, Surrey
Second	by: Jon H. Martin	07 Sept 2011	at: Portland, Dorset
Third	by: Influential Points	10 Sept 2016, 14 Aug 2017, 29 April 2018, 15 June 2019	at: Walworth Business Park, Andover, Hampshire

Biology & Ecology

Life cycle

In southern Europe Aphis vitalbae is probably anholocyclic, continuing to reproduce parthenogenetically on clematis through the winter. Further north, in Poland, Halaj & Osiadacz (2015) have found sexual forms in September and October, with the oviparae presumably laying overwintering eggs on clematis.

In England the situation regarding overwintering is unclear. We have found them for four years running on Clematis vitalbae at a site in Andover, Hants, so they appear to be successfully overwintering on site either as viviparae or as eggs. We have not yet been able to find any sexual forms.

In April 2018 we found a few immature aphids (see picture above) hiding beside buds on clematis, their existence only revealed by the activities of the ever present Lasius fuliginosus ants. These could either be developing fundatrices that have emerged from overwintering eggs, or they could be aphids that have overwintered as parthenogenetic apterae.

On our spring and late summer visits to the colony we were unable to find any alatae or developing immature alatae, despite high levels of crowding in late summer. In contrast on our visit in June 2019 we found numerous fourth instar developing alatae (see picture below).

There were also several alatae on the leaves receiving attention from the ever present ants.

There are likely to be several factors involved in inducing alate production in Aphis vitalbae, but the lack of any alate production in late summer when densities were highest suggests that day length and host condition rather than crowding were the most important factors.

Colour

Aphis vitalbae is extremely variable in colour, making it easy to confuse with other species. Some adult apterae (see picture below) have the domed dorsum very dark green to grey - almost black - surrounded by a much paler rim.

Most adult apterae are intermediate in colour between green and yellow, being either mottled green or mottled yellow (see pictures below).

Lastly some apterae are rather uniformly yellow (see picture below).

Immatures are similarly variable in colour.

Ant attendance

Nieto Nafria & Durante (2005) state that Aphis vitalbae is attended by ants. Other authorities have not mentioned this aspect of their behaviour, but the colonies we have found in Hampshire have always been attended by Lasius fuliginosus.

The ants subjected the aphids to vigorous antennation to encourage honeydew production.

Lasius fuliginosus also vigorously defends the colonies, attacking any source of disturbance. Our friend, who sampled the aphids for us when we were not around, termed them the "crazed killer ants" given their fierce defence of the aphids.

Competition & niche separation

In September 2017 we were sent a further sample from the Andover colony of Aphis vitalbae. Interestingly, the sample contained not only Aphis vitalbae, but also another clematis specialist. This was the peach-clematis aphid (Myzus varians, see picture below).

The two species are easy to tell apart from their antennae, with Myzus varians having conspicuously banded antennae and Aphis vitalbae having only antennal segment VI darkened. Dorsal colour is unreliable to differentiate species in the field, because some Aphis vitalbae are pale yellow thus resemble Myzus varians.

We are not aware of any niche differentiation between Aphis vitalbae and Myzus varians and the two species were feeding on the same leaves - except of course the former is monoecious whilst the latter host alternates between peach and clematis. Hence the period for potential competition on clematis is limited to mid-late summer.

Natural enemies

We have found evidence of parasitic attack of Aphis vitalbae in the Andover colonies (see picture below).

The adult wasps had already emerged from the 'mummies' and departed, and so could not be identified. The mummies were, however, similar to those made by Diaeretiella rapae which Stáry (1966) records as a parasitoid of this aphid.

A different species of parasitoid, Lysiphlebus fabarum was recorded by Kos et al. (2012) in Slovenia.

Other species on the same host

Blackman & Eastop list 23 species of aphid as feeding on clematis (Clematis) worldwide, and provide formal identification keys (Show World list). Of those aphid species, Baker (2015) lists 9 as occurring in Britain (Show British list).

Beneficial & detrimental effects

The image below shows the flowers of Clematis vitalba, old man's beard, or traveller's joy, a deciduous perennial climbing shrub native to central and southern Europe. It favours chalky soils, but is now widespread outside its native range, especially in waste areas in suburban habitats. In such situations it can form dense thickets blanketing trees and shrubs. As a result, Clematis vitalba is now considered an invasive pest.

Aphis vitalbae can play an important part in the biological control of Clematis vitalba. Halaj & Osiadacz (2015) observed that large colonies of Aphis vitalbae on the bottom part of clematis leaves causes premature drying of leaf ends and the deformation of young shoots.

Set against these beneficial effects, Aphis vitalbae may significantly lower the aesthetic value of decorative clematis varieties.

Acknowledgements We are extremely grateful to Dr Alex Shaw, who introduced us to a site near her office where we found several interesting aphid species including Aphis vitalbae. She also sent us further samples of aphids from the site in an attempt to obtain alatae and sexual forms. We are also very grateful to Dr Roman Halaj who sent us much useful information about Aphis vitalbae in Poland. We are also especially grateful to Test Valley Borough Council and the Walworth Enterprise Centre for preserving the habitat of this colony. Our particular thanks to Paul Brown (Senior Curator, Sternorrhyncha, Natural History Museum, London, UK) for preparing clarified slide mounts of our Aphis vitalbae, and to Roger Blackman for identifying the British Aphis vitalbae from them, and for his comments (summarised above). 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 Halaj, R. & Osiadacz, B. (2015). Note: Aphis vitalbae Ferrari, 1872 (Hemiptera: Aphididae): new finding on ornamental Clematis spp. in Poland. Phytoparasitica 43, 103-106. Full text Kos, K. et al. (2012). Aphidiinae (Hymenoptera, Braconidae, Aphidiinae) from Slovenia, with description of a new Aphidius species. Zootaxa 3456, 36-50. Full text Nieto Nafria, J.M. & Durante, M.P.M. (2005). Hemiptera: Aphididae III, Volume 28. CSIC Press. 362 pp. Stáry, P. (1966). Aphid parasites of Czechoslovakia. A review of Czechoslovak Aphidiidae (Hymenoptera). Praha:Academia, The Hague: Dr W. Junk B.V. 242 pp.