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Stomaphis wojciechowskii

Pale giant oak aphid - A new species for Britain

Dransfield, R.D., Hodgson, J.F., Brightwell, R., Depa, L. & Brown, P.
Uploaded 9 July 2018. Updated 2 November 2018
On this page: Description  Biology & Ecology:  Discovery in Britain  Habitat  Ant attendance  Other aphids on the same host 

Identification & Distribution

Adult apterae of Stomaphis wojciechowskii are very large - the body length of wingless adults is 5.2-6.8 mm (much the same size as Stomaphis quercus  which are 5.3-7.0 mm, given this range is of a larger sample). The aptera is pale in colour (see pictures below) with darker spinal sclerites (cf. Stomaphis quercus which is dark green to dark brown, shiny and lacks clearly visible spinal sclerites). Given that the paired spinal sclerotic plates are wider than long, we may conclude that the first image (below) shows a fundatrix (Depa, pers. comm.). Like Stomaphis quercus they have an extraordinarily long rostrum, up to twice the body length, or more in nymphs. In the first image below the aphid is feeding so the rostrum is buried in the tree bark - in the second image the long rostrum is being carried under the body and can be seen protruding a full body length behind the insect, probably a nymph. The aptera has numerous densely placed, erect hairs on the body, antennae and legs. The dark grey siphuncular cones are rather small.

One criterion currently used for differentiation of Stomaphis species is the ratio of antennal length to body length. For Polish specimens this ratio is lower than 0.37 for Stomaphis wojciechowskii (cf. Stomaphis quercus where this ratio is more than 0.37). However this criterion did not hold for the smaller Cambridgeshire specimens of Stomaphis wojciechowskii (body length of 5.2 mm.) which had ratios of 0.38-0.39. Hence this character should be removed from keys covering this species (Blackman, pers. comm.).

Both images copyright Julian Hodgson,  all rights reserved.

The following current criteria for identification of Stomaphis wojciechowskii remain valid:

  • The ratio of the second hind tarsal segment to the first hind tarsal segment (HTII/HTI) is less than 2.85 with an average of 2.71 (cf. Stomaphis quercus where this ratio is more than 2.85 with an average of 2.95).
  • The ratio of second hind tarsal segment to the second mid-tarsal segment (HTII/MTII) is less than 1.31 with an average of 1.28 (cf. Stomaphis quercus where this ratio is more than 1.31 with an average of 1.33). For Stomaphis wojciechowskii fundatrices these criteria are slightly different (Depa & Mróz, 2012 ).

The images below show clarified mounts of an Stomaphis wojciechowskii adult fundatrix and aptera from Monks Wood, Cambridgeshire, UK. The aptera's forelegs and part of one antenna were removed for COI analysis.

Micrographs of clarified mount  copyright Roger Blackman, and Lukasz Depa, all rights reserved.

The winged dispersive form, or alate, is shown above. The alate has rather short, narrow wings with brown-bordered veins.

Image copyright Julian Hodgson,  all rights reserved.

Sexual forms, oviparae and small wingless males, occur in September to early November. Oviparae (shown below with newly-laid eggs) have been recorded mid-October in Britain.

Image copyright Julian Hodgson,  all rights reserved.

Recent work (Depa et al., 2017 ) indicates Stomaphis wojciechowskii has a wide host range: including other Quercus species, Alnus glutinosa, Juglans regia, Salix species (unidentified) and Tilia cordata. Stomaphis aphids are nearly always closely attended by ants. Stomaphis wojciechowskii is usually attended by the brown ant Lasius brunneus (cf. Stomaphis quercus, which is usually attended by Lasius fuliginosus, except for Sardinian populations of Stomaphis quercus, confirmed by COI barcoding, which are pale and are attended by Lasius brunneus - see Loi et al., 2012  and Depa et al., 2017 ).

Stomaphis wojciechowskii has been recorded from Central and Eastern Europe (Poland, Hungary, Romania, Slovakia) but has never previously been observed in Britain, and is well outside its currently predicted geographic range (Depa et al., 2017 ). However, its concealed life style resulted in it only recently being discovered in Europe by Depa et al. (2012) . Among closely ant-tended species winged forms tend to be rare or unknown, and in some cases, as in Trama troglodytes,  few winged forms are found because the ants bite off their wings. The rarity of alatae may explain why no Stomaphis has ever been recorded by Rothamsted Insect Survey suction-traps (Bell et al., 2015,  Appendix S2). No Stomaphis of either species are recorded on NBN Gateway (as of 11 July 2018). 

To date Stomaphis wojciechowskii has been observed in five parts of Cambridgeshire, but nowhere else in UK, nor west of Slovenia or Poland.
First observedby: J.F. HodgsonMay 2018at: Monks Wood N.N.R.
ThenAug.
-
Sep. 2018
at: Holme Fen N.N.R.
Raveley Wood
Aversley Wood
Woodwalton Fen

 

Biology & Ecology:

Discovery in Britain

In the spring of 2018 Julian Hodgson was sampling bark flies (Psocoptera) in Monks Wood National Nature Reserve when he found a small number of large aphids (ca 5-6 mm long) with a rostrum approximately twice the body length. Despite not having an entomological background, he correctly identified the aphid as belonging to the genus Stomaphis. The species of this genus are characterized by their large size (up to 7 mm in body length) and an extraordinarily long rostrum (up to twice the body length, or more in nymphs) - which enables them to probe through the bark crevices and feed deep inside oak and other trees. Stomaphis aphids are nearly always closely-attended by ants, which feed on their honeydew and help protect the aphids from predators and parasitoids.

Only a few Stomaphis species occur in Britain, and all are rare or very rare. The giant oak aphid Stomaphis quercus, (known as the "world's largest aphid" although no bigger than some other Stomaphis) occurs on oak and birch. The giant maple aphid, Stomaphis graffii, feeds on the trunks of maple and sycamore. Stomaphis longirostris, which feeds on willow and poplar, has also been reported but is unconfirmed (Baker, 2015 ).

Given that the Cambridgeshire Stomaphis was on the trunks of oak trees (Quercus robur), it was expected to be Stomaphis quercus. However, several points cast doubt on this:

  1. The aptera was pale in colour (see pictures above) with darker spinal sclerites. Older post-reproductive individuals are a little darker (see picture below) but are still quite unlike Stomaphis quercus  which is dark green to dark brown, shiny and lacks clearly visible spinal sclerites.

Image copyright Julian Hodgson,  all rights reserved.

  1. The aphid was not attended by Lasius fuliginosus which normally attends Stomaphis quercus on the surface of the bark, but by another Lasius species, Lasius brunneus (see picture above) which mainly resides in tunnels under the bark.
  2. Overall the aphid looked and behaved much more like Stomaphis wojciechowskii, a species of much the same size (Heie, 1995 ) as Stomaphis quercus, first described by Depa et al., (2012) 
  3. Stomaphis quercus had never previously been observed in Cambridgeshire - but then Stomaphis wojciechowskii had never been found west of Slovenia or Poland.

Julian contacted us at InfluentialPoints about his find and, given its similarlity to Stomaphis wojciechowskii, we advised him to make confirming its identity a top priority. The organization responsible for administering Monks Wood N.N.R., Natural England, proved extremely helpful in giving permission to sample.

Obtaining a sample was not as straightforward as one might imagine. Other than in May, when they were first discovered, the aphids and accompanying ants were only active at night. Hence sampling was restricted to the hours of darkness using a head lamp. Feeding aphids with their mouthparts deeply embedded in the trunk were located by the activities of the ants. Aphids were induced to withdraw their mouthparts by stroking them very gently with a soft-bristled paint brush. The ants locked their jaws on the paint brush, so a sample of ants was readily obtained by dipping the brush in alcohol. The aphids began to extract immediately after being stroked, but could take over an hour to complete the extraction (one was still attempting to do so after four hours).

Specimens were then preserved in 95% isopropyl alcohol (ideally they would have been preserved in 99% molecular biology grade ethanol, but it is not available to the public in UK). They were sent to Paul Brown and Roger Blackman at the London Natural History Museum for morphological identification, and to Lukasz Depa in the University of Silesia in Katowice, Poland for molecular identification. The ants were sent to Phil Attewell, county recorder of ants for Hertfordshire. By early September the ants had been confirmed as Lasius brunneus and both Dr Blackman and Dr Depa had confirmed the identity of the aphid as Stomaphis wojciechowskii. The COI sequence was most similar to a central European rather than western or southern population. A provisional molecular clock suggested they diverged less than about 30,000 years ago, and are a relic population.

Habitat

Elsewhere in Europe Stomaphis wojciechowskii has been recorded in ant shelters constructed within bark crevices and covered by soil on trunks of Quercus robur, up to about about 1.8 m above ground,

Julian found the first Stomaphis wojciechowskii specimens walking openly on the trunks of oak trees during daylight in May 2018. This behaviour subsequently proved to be exceptional. Some individual aphids were found feeding at the base of deep, open bark crevices, but this also appears to be exceptional. A few aphids were found walking up and down bark crevices at night, usually escorted by Lasius brunneus, though sometimes unescorted. Most aphids were found hidden from view beneath sections of bark crevices covered over either by bark or other material including moss, lichen fragments, or 'soil' deposited along the ant trails.

A favoured location for these aphids was at the upper terminations of bark crevices, where the bark has grown over the crevice to form a small chamber which is open only at the bottom end and is guarded by ants. Within these crevices small groups of aphids live and feed. These hidden groups typically contain about 5 or 6 aphids (with a range of 2 - 11), comprising 1 - 2 large adults (possibly fundatrices), 2 - 3 smaller adults and 1 - 2 nymphs. The image below shows such a typical group, photographed after the covering flakes of bark had been removed.

Image copyright Julian Hodgson,  all rights reserved

All such groups, found to date, were located from about 0.55 to 3 meters above ground. The upper limit given here is necessarily limited by the height of the observer, or how high he could easily climb, but the ant trails also continue much higher up the trees.

Ant attendance

Depa et al., 2017  found Stomaphis wojciechowskii usually attended by Lasius brunneus, but almost never Lasius fuliginosus - which they found 'visiting' one colony.

The Cambridgeshire Stomaphis wojciechowskii are attended exclusively by the brown ant (Lasius brunneus). There are good populations of this species on the oak trees. Activity of the brown ant is mainly nocturnal, so the best time to search for aphids being attended by these ants is at night. The ants in the two pictures below are engaged in feeding from the honeydew, stroking the aphid with their antennae to encourage honeydew production, and guarding the aphids from potential predators.

 

Both images copyright Julian Hodgson,  all rights reserved

If the aphids hidden in the crevices are exposed to light, the ants usually immediately begin escorting the aphids down the crevices to a place of safety within the moss-covered base of the trunks. The ants will occasionally pick up the smallest individuals (probably mostly nymphs) in their jaws and literally run down the crevice, sometimes falling in the process in their haste to remove the aphids. Similar behaviour has been observed with root aphids, in particular Smynthurodes betae. 

Like many aphid species we have observed, their attending ants do not seem very good at protecting the aphids from parasitoids. More curiously, ants may continue tending the resulting mummy. Several Stomaphis wojciechowskii mummies stuck firmly to the bark (first image below) seem to match the description and photo of Protaphidius wissmannii given by Kovács (2009).  We do not know if the parasitoid is producing kairomones to maintain ant protection, or if the aphid has low-volatility kairomones, but we have observed this behaviour in Lasius fuliginosus attending a Pterocomma rufipes  mummy, and Formica lugubris attending an empty mummy of Cinara juniperi

Image copyright Julian Hodgson,  all rights reserved.

 

Other aphids on same host:

Blackman & Eastop list 34 species of aphid  as feeding on common or pedunculate oak (Quercus robur) worldwide, and provide formal identification keys.

Of those aphid species, Baker (2015)  lists 15 as occurring in Britain: Hoplocallis picta,  Lachnus longirostris,  Lachnus roboris,  Moritziella corticalis, Myzocallis boerneri,  Myzocallis castanicola,  Phylloxera glabra,  Stomaphis quercus,  Stomaphis wojciechowskii, Thelaxes dryophila,  Thelaxes suberi,  Tuberculatus annulatus,  Tuberculatus borealis,  Tuberculatus neglectus  and Tuberculatus querceus.

Blackman & Eastop list Stomaphis species as feeding on 12 species of oak (Quercus) worldwide. Among those, Stomaphis japonica and Stomaphis quercus have been observed on the most species, followed by Stomaphis bratislavensis, Stomaphis wojciechowskii [and possibly Stomaphis longirostris & Stomaphis quercisucta].

Acknowledgements

We congratulate Julian Hodgson on finding this 'new to Britain' species of aphid, all the more remarkable at a reserve where the insect fauna has been fairly intensively studied over many years. All the photographs and field observations on this page have been provided by Julian.

We especially thank Lukasz Depa (University of Silesia, Poland ), Paul Brown and Roger Blackman (Natural History Museum, London ) for confirming the identity of these aphids, for their help and advice, and for the image of a clarified mount. We also thank Phil Attewell for confirming the ant identification, and Chris Evans, the Senior Reserves Manager for Cambridgeshire of Natural England,  for permitting Julian to sample ants and aphids at Monks Wood National Nature Reserve, Cambridgeshire.

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

  • Bell et al. (2015). Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. J. Anim Ecol. 2015; 84(1), 2134.  Full text 

  • Depa, L., Mróz, E. & Szawaryn, K. (2012). Molecular identity of Stomaphis quercus (Hemiptera: Aphidoidea: Lachnidae) and description of a new species. European Journal of Entomology 109, 435-444. Full text 

  • Depa, L. & Mróz, E. (2012). Description of fundatrix morph of Stomaphis wojciechowskii Depa 2012 (Aphidoidea: Lachnidae). International Journal of Invertebrate Taxonomy 23(3), 425-428. Full text 

  • Depa, L., Mróz, E., Bugaj-Nawrocka, A. & Orczewska, A. (2017). Do ants drive speciation in aphids? A possible case of ant-driven speciation in the aphid genus Stomaphis Walker (Aphidoidea, Lachninae). Zoological Journal of the Linnean Society 179, 41-61. Full text 

  • Heie, O.E. (1995). The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. VI: Family Aphididae: Part 3 of Tribe Macrosiphini of Subfamily Aphidinae, and Family Lachnidae, BRILL, 222 p.

  • Kovács, T. (2009). A Protaphidius wissmannii (Hymenoptera: Aphidiidae) életmódja és viselkedése. Folia Historico Naturalia Matraensis 33: 201204. Full text 

  • Loi, A., Luciano, P., Gilioli, G. & Bodini, A. (2012). Lasius brunneus (Formicidae Formicinae) and Stomaphis quercus (Aphidoidea Aphididae): Trophobionts harmful to cork oak forest in Sardinia (Italy). Redia 95, 21-29. Full text