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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.A.
Uploaded July 2018. Updated January 2019
On this page: Description Biology & Ecology: Discovery in Britain Life cycle Habitat Ant attendance Natural enemies Other aphids on the same host

Identification & Distribution

The apterae of Stomaphis wojciechowskii are light fuscous to light brownish, in colour (see first two pictures below) with darker spinal sclerites (cf. Stomaphis quercus which is dark green to dark brown, shiny and lacks clearly visible spinal sclerites). The first image below shows a Stomaphis wojciechowskii fundatrix, which is distinguished by having the paired spinal plates wider than long, and the second shows a rather old (possibly post-reproductive) apterous vivipara with the paired spinal plates approximately square. The extraordinarily long rostrum (visible in the third image below) is up to twice the body length (rather more in nymphs). The Stomaphis wojciechowskii aptera has numerous densely placed, erect hairs on the body, antennae and legs. The ratio 'length second hind tarsal segment (HTII) / length first hind tarsal segment (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 "HTII / length second mid tarsal segment (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 fundatrices these criteria are slightly different (see Depa & Mróz, 2012). The dark grey siphuncular cones are rather small. The body length of wingless adults is 5.2-6.8 mm.

The images below show a fundatrix, an adult aptera, and an alate Stomaphis wojciechowskii.

Images copyright Julian Hodgson, all rights reserved.

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

The images below are 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.

Note: One criterion originally 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.).

Stomaphis wojciechowskii has a wide host range which includes several oak (Quercus) species, alder (Alnus glutinosa), walnut (Juglans regia, Salix species (unidentified) and lime (Tilia cordata). Stomaphis wojciechowskii is nearly always closely attended by ants, usually the brown ant Lasius brunneus (cf. Stomaphis quercus, which is usually attended by Lasius fuliginosus). Sexual forms, oviparae and small wingless males, occur in September to early November.

Stomaphis wojciechowskii has been recorded from Central and Eastern Europe (Poland, Hungary, Romania, Slovakia). Until this report in July 2018 it had not previously been observed in Britain, but is now known to be widely distributed at least in Cambridgeshire. Its occurence in Britain is well outside its previously predicted geographic range (Depa et al., 2017). Its concealed life style delayed its discovery in Europe until recently (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 species are recorded on NBN Gateway (as of 29 Jan. 2018).

Julian's observations in five parts of Cambridgeshire are the first recorded occurrences of Stomaphis wojciechowskii in UK.
First observedby: J.F. HodgsonMay 2018at: Monks Wood N.N.R.
ThenAug. - Sep. 2018at: 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 (about 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 that 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.

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 in UK (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 fundatrix was pale in colour (see pictures above) with darker spinal sclerites. Apterous viviparae matured from being pale grey to light brown, quite unlike Stomaphis quercus which is dark green to dark brown shiny and lacks clearly visible spinal sclerites.
  2. 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.
  3. Overall the aphid looked and behaved much more like Stomaphis wojciechowskii, a species of very similar size (Heie, 1995) as Stomaphis quercus, first described by Depa et al., (2012).
  4. 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 similarity 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+ants 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.

Life cycle

The overwintering eggs of Stomaphis wojciechowskii hatch in spring and seem to mature rather slowly. Depa & Mróz, 2012 found mature fundatrices on common oak (Quercus robur in June, whilst Julian found them on the same host in Britain in May and June (see picture below).

Image copyright Julian Hodgson, all rights reserved.

The offspring of the fundatrix develop to viviparae - both apterous and alate- which are present through the summer months. The picture below shows a mature apterous vivivipara, possibly post-reproductive given the darknesss of the body colour.

Image copyright Julian Hodgson, all rights reserved.

Alatae seem to be relatively rare. The wings of Stomaphis are rather small for their body size. Depa (2013) suggests that the optimal way of dispersal for large, tree-trunk feeding aphids may be to climb to the top of the tree and undertake short flights from tree-top to tree-top, with a higher probability of landing on a branch in the dense tree-top layer of the forest.

Image copyright Julian Hodgson, all rights reserved.

Sexual forms - oviparae and small wingless males - were present in Monks Wood in October. Large yellow eggs were laid by the oviparae (see pictures below) in the ant runs.

 

Images copyright Julian Hodgson, all rights reserved.

Habitat

Depa et al. (2017), found Stomaphis wojciechowskii tends to infest trees of greater trunk diameter, which were older and had thicker bark cork, especially among Tillia cordata - but not Alus glutinosa.

Again, 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 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

Sibling aphid species are usually divergent on distinct host plants, but the sibling species Stomaphis quercus and Stomaphis wojciechowskii both live on oak trees. Their distributions indicate a high level of sympatry and their environmental requirements overlap. Depa et al., 2017 proposed that the divergence of these two species resulted from them having adapted to living with species of ants of distinct life modes and foraging strategies. Stomaphis quercus is nearly always attended by Lasius fuliginosus whilst Stomaphis wojciechowskii is usually attended by Lasius brunneus.

The newly discovered Cambridgeshire Stomaphis wojciechowskii are attended exclusively by the brown ant (Lasius brunneus). The ants live in decaying parts of living deciduous trees - under bark and in the wood - and mainly feed on honeydew of tree aphids. Lasius brunneus is a timid, non-aggressive ant with a rather cryptic life mode, and its foragers avoid open spaces. Activity of the brown ant is mainly nocturnal, so the best time to search for aphids being attended by these ants is at night. Some of the ants in the two pictures below are stroking the aphid with their antennae to encourage honeydew production, whilst others guard the aphids from potential predators.

 

Both images copyright Julian Hodgson, all rights reserved

As soon as a droplet of honeydew is produced, one of the ants consumes it.

If the aphids hidden in the crevices are exposed to light, the ants usually immediately begin escorting their 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.

 

Natural enemies

Several species of natural enemies have been observed predating Stomaphis wojciechowskii in Cambridgeshire including the ground beetle Carabus granulatus and an unidentified rove beetle (Staphylinidae). The aphids are also attacked by a parasitoid - the mummies are stuck firmly to the bark (see image below) .

These mummies appeared to match the description and photo of the Protaphidius wissmannii mummy given by Kovács (2009), and this identification was confirmed by Dr Gavin Broad of the Natural History Museum, London. A male (first picture) and a female (second picture) are shown below.

The 'protected' habitat of Stomaphis wojciechowskii under bark flakes is countered by the parasite having a telescopic ovipositor, which can be extended to equal the body length of the parasitoid. Kovács (2009) describes the searching behaviour of Protaphidius wissmannii. The antennae are inserted into the burrow entrance to detect the host. Sometimes one of the guarding ants may biting off the antennal tips of the parasitoid. Once a suitable host is found, the ovipositor is extended, inserted into the aphid and an egg laid.

Curiously, ants may continue tending the aphid after it has been mummified, and sometimes even after the adult parasitoid has emerged. We do not know if the parasitoid is producing kairomones to maintain ant protection, or if the aphid has low-volatility kairomones which continue to attract the ants even after it has been mummified, 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.

It is certainly to the parasitoid's advantage for ant-tending to continue, as predators will certainly attack and eat parasitized aphids just as much as healthy aphids. Indeed some predators seem to specialize in eating mummified aphids. Kovács (2009) found that very few experimentally marked mummies survived the winter, with many eaten by birds.

 

Other aphids on same host:

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].

Stomaphis wojciechowskii has been recorded from 3 Quercus species (Quercus cerris, Quercus petraea, Quercus robur), plus Tilia cordata, Alnus glutinosa, Juglans regia and a Salix (preseumidly Salix alba).

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 identification of Lasius brunneus, Ed Baker, Tree Preservation Officer, Cardiff Council, for helping identify the Protaphidius wissmannii, Gavin Broad of the Natural History Museum, London for confirming Ed's identification. Also 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.

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

  • 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), 21-34.  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. (2013). Life cycle of maple-tree aphid Stomaphis graffii Cholodkovsky, 1894 (Hemiptera, Aphididae). Animal Biology 63, 313-320. Abstract

  • 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: 201-204. 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