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  <February 2015>  

Our previous blogs looked at several non-native aphids that we have come across in Britain. These included the bow-legged fir aphid, Cinara curvipes , an American species first recorded in UK in the 1990's, and the Monterey pine aphid, Essigella californica which we found in Kent shortly after its first UK sighting in Kew. Such species are commonly termed "invasive", defined as "non-native species which threaten ecosystems, habitats or species". Since these aliens are not uniformly threatening, let us examine some so-called invasive aphid species in Britain, and their threat to British agriculture and biodiversity.

Should we worry about non-native species - or can they add to our biodiversity?

Aphids, or at least Homoptera, tend to be over-represented in the invasive fauna lists. This is partly due to sampling bias - aphids often form large static colonies on plants readily visible to interested humans. But their prominence also relates to aphids' parthenogenetic mode of reproduction which, in summer, means that (at least theoretically) following the arrival of a single aphid, vast numbers can very rapidly breed. Most non-native aphid species enter Europe among imported plant material - sometimes when a plant species is first introduced, but often many years later. If most of these new arrivals did not die out, we would now be overrun. But, once established, human commerce and wind-assisted migration of winged forms disperse the successful arrivals.

The first documented case of aphid introduction to Europe was the woolly apple aphid, Eriosoma lanigerum That species originated in North America, but was noted in Europe for the first time in a nursery on the outskirts of London in 1787 (Balchowsky & Mesnil, 1935 ). By 1802 it had spread to Germany, where it caused extensive damage in nurseries. It reached France by 1812, Italy by 1841 and Switzerland by 1870, and has since spread to all temperate countries of the world. Since invasive aphids are not new to Europe - their arrival has little to do with global warming! There no evidence that the rate of 'invasion' is increasing - at least over the last forty years (Smith et al., 2007 ).

Not surprisingly, most invaders to (temperate) Europe originate from temperate parts of Asia and North America (Coeur d'acier et al., 2010 ). Those regions have the largest number of non-European aphid species adapted to a temperate climate. By 2010 Britain had the largest number of recorded invasives in Europe (64) partly because, until recently, Britain had the largest number of local taxonomists. 52 of the 102 alien species to Europe are classed as fruit and vegetable crop pests - including such important pests as Myzus persicae  and Macrosiphum euphorbiae

So what threat are all these alien species to UK crops and biodiversity?

An interesting approach to this issue was described by Davis et al. (2011),  summarised by the title of their paper: "Don't judge species on their origins". Whilst the authors fully accepted some alien species are major pests, and need to be controlled (which is certainly true for aphid crop-pests), they argue we should embrace the fact of 'novel ecosystems' and incorporate many alien species into management plans, rather than try to achieve the often impossible goal of eradicating them or drastically reducing their abundance.

We will consider these issues in relation to some of invasive species we have encountered in Britain during the last five years. Many of the 102 alien species of aphids have been in Europe for many years including: Aphis gossypii,  Macrosiphum euphorbiae,  Macrosiphum ptericolens,  Myzus ascalonicus,  Myzus ornatus,  Neomyzus circumflexus,  Rhopalosiphum oxyacanthae,  Toxoptera aurantii,  Chromaphis juglandicola,  Panaphis juglandis,  Periphyllus californiensis,  and Wahlgreniella nervata.  Some newer arrivals are described below.

 

The onion aphid - Neotoxoptera formosana

This is not really what your average shopper would expect to find on his onions from a supermarket in Scotland - but this is exactly what was found in Inverness in August 2013 (see picture below). The aphids came to us for identification and they turned out to be the onion aphid Neotoxoptera formosana

Aphids normally leave crops when they are harvested, but the onion aphid bucks that trend, and can build up large populations on stored bulbs - either on the farm, or on a supermarket shelf. The 'onion aphid' does not host alternate but spends it entire life cycle on onion (Allium). Lacking sexual forms, the species reproduces parthenogenetically all year round. Neotoxoptera formosana is native to east and south-east Asia, but is invasive in Australia, New Zealand, Hawaii, the Americas and north-west Europe.

Neotoxoptera formosana was first reported in Britain on onion at RHS Wisley in Surrey, England in October 1999 (Halstead, 2000 ). Attempts to eradicate it appeared successful at first, but it was found on onion at Wisley in May 2000 having probably overwintered on garlic cloves in a cold frame. Infested plants were sprayed and the pest was again considered eradicated at Wisley. Neotoxoptera formosana has since been trapped several times in 40ft aerial suction traps (MacLeod, 2007 ), and found in gardens in Surrey and London. Blackman (2010)  suggests it is now well established in Britain, but our observation was only the second record of the species from Scotland since it was first reported from Fife in 2008 (Reid, pers. comm.).

 

Second image copyright fera,  all rights reserved.

Of the various Neotoxoptera species, only Neotoxoptera formosana has turned up in temperate Europe thus-far, but another invasive member of the genus, the marigold aphid Neotoxoptera oliveri, prefers the warmer climes of southern Europe. Neotoxoptera formosana is distinguished by being shining magenta-red to dark reddish brown or almost black. Its winged forms are very dark-red to black, with the black borders on the wing veins of rather constant width along the lengths of the veins. In Neotoxoptera oliveri, the black borders widen out at the base and apex of each wing vein.

Given favourable conditions Neotoxoptera formosana populations can build up rapidly and, in Italy, some damage has been reported such as wilting, yellowing and desiccation (Barbagallo & Ciampolini, 2000 ). It may also transmit plant viruses. Nevertheless, considering how long Neotoxoptera formosana has been in Europe, the number of cases of reported damage are few, and a DEFRA report (MacLeod, 2007 ) suggests it is a relatively minor pest.

 

The lupin aphid - Macrosiphum albifrons

The lupin aphid (Macrosiphum albifrons ) is a North American species that was introduced to Europe in the 1970s, and first recorded in England in 1981. Its adults are unusually large pale bluish grey-green aphids dusted with white wax.

We have found lupin aphids in nurseries and gardens several times in southern England. Macrosiphum albifrons spends its entire life cycle on Lupin (Lupinus sp) living on the leaves, stems and flower spikes. In North America sexual forms develop in the autumn, and the aphid overwinters as eggs, but in Britain these aphids overwinter as viviparae.

Lupins contain quinolizidine alkaloids, which function as nitrogen transport and storage compounds and also as chemical defense against herbivores and pathogens. This chemical defense is effective against most aphid species, but not against Macrosiphum albifrons. These aphids are adapted to high alkaloid levels and sequester lupin alkaloids. As a result these aphids are unpalatable to predators, and very large populations may develop on lupins.

 

The plant above was growing in a churchyard and showing signs of extreme stress due to this aphid infestation.

Macrosiphum albifrons is now widely distributed, and considered an invasive pest species over much of Europe. Severe damage is caused to young lupin flowers, with whole spikelets being aborted - and a heavy infestation may kill the entire plant. This is a good example of where the economic damage outweighs any increase in biodiversity - local predators are unlikely to benefit because the aphid is protected by the plant's chemical defences.

 

Japanese elm aphids - Tinocallis spp.

Japanese elm aphids have been amongst the most successful species invasive to Europe. There are about 18 species usually associated with elms (Ulmaceae). One species (Tinocallis platani) has long been found in Europe, another (Tinocallis ulmifolii) in North America, and one in west Asia, but all others have until recently been restricted to the far east. As a result of the plant trade, several species have recently expanded their range from the far east to cover much of the world. Tinocallis platani is invasive in western North America where it occurs on American elm (Ulmus americana). Five species have been recorded or are now fully established over much of Europe. We have found two of these in Britain: the Japanese elm aphid (Tinocallis takachihoensis) and the pale Japanese elm aphid (Tinocallis nevskyi).

The Japanese elm aphid (Tinocallis takachihoensis ) was first recorded in England in 'the wild' by Döring (2007, 2008)  who collected it on whych elm (Ulmus glabra) in Berkshire. It has also been recorded in 2012 from Lincoln, UK by Mick Talbot.  It is indigenous to the far east, but has now been introduced to several European countries and the USA. In England it has been regularly found on imported Ulmus and Zelkova Bonsai plants in Britain (Roques & Auger-Rozenberg, 2006  ).

We first confirmed the presence of Tinocallis takachihoensis in East Sussex in July 2010 on elm trees at Friston Forest, although immatures we found in 2007 were probably of this species. Then in 2014 we found large numbers of Japanese elm aphids on elm in several locations in East Sussex (Middle Farm, West Dean, Ringmer) and West Sussex (Stanmer). It is unclear how Tinocallis takachihoensis is overwintering in Britain, but it seems likely that they produce sexual forms in autumn and overwinter as eggs.

Winged adults of the Japanese elm aphid (Tinocallis takachihoensis) are pale yellow-green with a shiny black head and thorax and characteristic black markings on the wing. They are also distinguished by having strange tubular processes on different parts of the body.

Tinocallis takachihoensis has two pairs of paired dorsal processes on the pronotum which can be seen in lateral view (above) and in dorsal view in the micrograph below. The posterior pair is large and dark, whilst the anterior pair is small and pale. There are also two pairs of pale paired dorsal processes on the abdominal dorsum. As for the function of these processes, perhaps they serve to improve crypsis  by breaking up the outline of the aphid - but it may be better to admit we have no idea what their function is.

 

The pale Japanese elm aphid (Tinocallis nevskyi ) feeds on elm (Ulmus). This species originated in central and south-west Asia, but has spread over much of Europe. In some European countries Tinocallis nevskyi is now among the most common aphid species, but we have only found it in one location in Britain, at the Railwayland Nature Reserve near Lewes in East Sussex.

Since it lacks the pigmented wings of Tinocallis takachihoensis, this invasive elm aphid is not quite so distinctive. The pale Japanese elm aphid is pale yellow, with pale or dusky antennae and legs (see picture below).

It too has various body processes. Its pronotum has two pairs of pale finger-like spinal processes, its mesonotum has one pair of large conical processes and its abdomen has spinal processes on tergites 1 and 2. Also, its wings are hyaline and the forewing veins are not dark bordered.

Japanese elm aphids may cause cosmetic damage to elm trees (and to cars parked under them) because of sooty moulds growing on honeydew excreted by these aphids. However, their honeydew provides food to many generalized predators and parasitoids of aphids, and thus on balance probably has a beneficial effect on biodiversity.

 

Bamboo aphids - Takecallis spp.

These are small delicate narrow-bodied aphids which feed on bamboo (Bambuseae). They appear not to have sexual forms, but reproduce all year parthenogenetically. This genus is oriental in origin, but several of its five species are now widely distributed.

 

The black-spotted bamboo aphid (Takecallis arundinariae ) has been introduced to many parts of the world including much of Europe, Australia and North and South America. Its reproduction is entirely parthenogenetic over most of the world.

Their winged adults are whitish-yellow with longitudinal dark stripes on the thorax, and paired elongate dark patches on each abdominal segment. Their antennae and (to a lesser extent) their thorax are covered in a bluish-white wax clearly visible in the photo below.

Takecallis arundinariae are found on the underside of mature leaves of bamboos, especially Arundinaria and Phyllostachys spp..

The picture above shows a rather curious effect of these aphids feeding on bamboo. The group of aphids creates a feeding 'sink' which increases the flow of nutrients to the infected part of the leaf. This keeps that part of the, otherwise senescent, leaf green.  

The black-tailed bamboo aphid (Takecallis arundicolens ) is another highly invasive species, originally found in China, Japan, and Korea but now also present in Europe and North America. It feeds on bamboo (Phyllostachys spp. and Sasa spp.) as well as common reed (Phragmites australis) (our own record in the UK). We have found it rather more frequently than the black-spotted bamboo aphid in southern Britain, although both species are fairly common.

The black-tailed bamboo aphid has a conspicuously black cauda (clearly visible in the picture at the rear of the aphid's abdomen) and has pale abdominal tergites, without any dark patches.

 

Some species of bamboo are now invasive weeds in parts of Europe, so (not being avid gardeners) it is hard to regard bamboo aphids as anything other than a beneficial component of Europe's biodiversity!

 

Rhododendron and Tulip tree aphids - Illinoia spp.

The rhododendron aphid, Illinoia lambersi is mainly found on the new shoots and flower buds of Rhododendron. Illinoia lambersi is indigenous to North America where it is widely distributed, and sexual forms occur. As a result of the plant trade this aphid is now also well established on Rhododendron in parts of Europe, including Denmark, England and the Netherlands, where it overwinters as viviparae.

Illinoia aphids have their siphunculi darkened and somewhat swollen on the distal half, with a constricted apical region. Both winged and wingless aphids exist as green, pink and yellow forms, which can occur in mixed populations.

We have found both the green and pink forms (see above) in southern England. Presence of the pink form is one indication that we are looking at Illinoia lambersi and not the closely related Illinoia azaleae which only has green forms.

The rhododendron aphid highlights the issue of whether a particular invading aphid is 'good' or 'bad'. Rhododendrons were introduced to Europe as flowering shrubs, along with their fauna. They are especially popular in England on large estates where their colourful blooms can put on a fine display.

Unfortunately one species of rhododendron (Rhododendron ponticum) is now itself regarded as an invasive pest having taken over large areas of native UK woodland. The aphid Illinoia lambersi might well have been introduced with a view to biological control - if it had not already beaten us to it and arrived with its host. Consequently the aphid is now regarded as a pest by rhododendron aficionados (albeit the level of damage is minimal), and a potential ally by conservationists concerned about native woodland (albeit there is no evidence of it being of any practical use in rhododendron control). At present the invasive rhododendron plants definitely have the upper hand.

 

That said, we would be remiss to ignore a new invasive rhododendron aphid,  Ericolophium holsti. This has been caught using suction traps in Britain, but has not yet been found on rhododendron in the field. These aphids have pale dark-tipped cylindrical siphunculi - not swollen like Illinoia. The most likely hosts to find them on are Rhododendron arboreum and Rhododendron morii. Since neither rhododendron has been flagged as invasive plant species, Ericolophium holsti may be regarded as a potential pest.

 

Our last invasive aphid is another Illinoia species, the tulip-tree aphid, Illinoia liriodendri These aphids feed on the undersides of the leaves of (yes - you guessed it!) the tulip tree, Liriodendron tulipifera. Illinoia liriodendri is native to North America, but in 1998 was found in France. This aphid has since been reported in other European countries and in Japan.

The wingless adults of Illinoia liriodendri are spindle shaped, pale green, and lightly dusted with wax. Their antennae and siphunculi are black, except at the bases. Sexual forms occur in autumn.

There is no evidence that the tulip-tree aphid causes any harm to the tulip tree, and given Europe has lots of tulip trees, we should probably regard the aphid as a positive gain to our biodiversity. Nevertheless dense populations of tulip tree aphids can build up, resulting in large deposits of honeydew on the leaves. So car owners may not agree, given the rain of honeydew on any parked cars beneath them, but at least cleaning said vehicles provides employment to human invasives seeking a new life in Europe...

So why 'hunt' for aphids?? 

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

  • Balachowsky, A. & Mesni, L. (1935) Les insectes nuisibles aux plantes cultivées. Paris, France: Mery L. 1921 pp.

  • Barbagallo, S. & Ciampolini, M. (2000). The onion aphid, Neotoxoptera formosana (Takahashi), detected in Italy. Bolletino di Zoologia Agraria at di Bachicoltura Serie II 32(3), 245-258. Abstract 

  • Blackman, R.L. (2010). Aphids - Aphidinae (Macrosiphini). Handbooks for the identification of British insects 2(7). Royal Entomological Society, London.

  • Coeur d'acier, A., Hidalgo, N.P. & Petrovic-Obradovic, O. (2010). Aphids (Hemiptera, Aphididae). Chapter 9.2. Biorisk 4 (1) 435-474. Full text 

  • Döring, T.F. (2007). Colonies of the Asian elm aphid Tinocallis takachihoensis Higuchi (Hemiptera: Aphididae) in Britain. The Entomologist's record and Journal of Variation 119(5), 226-227. Full text 

  • Döring, T.F. (2008). Further sightings of the Asian elm aphid Tinocallis takachihoensis Higuchi (Hemiptera: Aphididae) in Britain. The Entomologist's record and Journal of Variation 120, 32.

  • Davis, M.A., Chew, M.K., Hobbs, R.J. et al. (2011). Don't judge species on their origins. Nature 474153-154. Full text 

  • Halstead, A.J. (2000) An onion aphid, Neotoxoptera formosana (Takahashi) (Hemiptera: Aphididae), new to Britain. British Journal of Entomology & Natural History 13(2), 94. Full text 

  • Macleod, A. (2007). CSL Pest risk analysis for Neotoxoptera formosana. Full text 

  • Roques, A. & Auger-Rozenberg, M.-A. (2006). Tentative analysis of the interceptions of non-indigenous organisms in Europe during 1995-2004. Bulletin OEPP 36, 490-496.

  • Smith, R.M., Baker, R.H.A., Malumphy, C.P. et al. (2007). Recent non-native invertebrate plant pest establishments in Great Britain : origins, pathways, and trends. Agricultural and Forest Entomology 9, 307-326. Full text 

  • Wink, M. & Wiite, L. (1991). Storage of quinolizidine alkaloids in Macrosiphum albifrons and Aphis genistae (Homoptera: Aphididae). Entomol. Gener. 15(4), 237-254. Full text