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Aphidinae : Neotoxoptera formosana
 

 

Identification & Distribution

Adult apterae of Neotoxoptera formosana (see first picture below) are shining magenta-red to dark reddish brown or almost black. The first and second antennal segments and the distal parts of the femora are all black (cf. Myzus ascalonicus, which has the first and second antennal segments, and the distal parts of the femora, all pale). The minimum diameter of the 'stem' of the siphunculi is greater than the diameter of the hind tibia at its midpoint (cf. Myzus ascalonicus, which has minimum diameter of the 'stem' of the siphunculi slightly less than the diameter of the hind tibia at its midpoint). The body length of the adult aptera is 1.6-2.3 mm. Immature Neotoxoptera formosana (see second picture below) are similarly coloured to adult apterae.

Neotoxoptera formosana alatae are very dark red to black with the wing veins heavily black-bordered. The borders on the wing veins of Neotoxoptera formosana are of rather constant width along the lengths of the veins (cf. Neotoxoptera oliveri where the borders widen out at the base and apex of each vein).

The clarified slide mounts below are of adult viviparous female Neotoxoptera formosana : wingless, and winged.

Micrographs of clarified mounted aptera & alate courtesy PaDIL. Copyright Qing-Hai Fan (Ministry for Primary Industries, NZ) under Commons Attribution 3.0 Australian License.

The onion aphid does not host alternate, but spends it entire life cycle on onion (Allium), either on the leaves or on bulbs in store. There are no sexual forms, so 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, North & South America, and north-west Europe.

 

Biology & Ecology:

Invasive in Europe

Neotoxoptera formosana was first found in Europe in 1984 in France (Leclant, 1999). Since then, the onion aphid has been observed regularly in low numbers in Britain and other European countries. Interception of Neotoxoptera formosana by Finland on onion bulbs from The Netherlands suggests that it may have been present in The Netherlands in 1994. Van Dijk (1993) reported that various Allium species grown in pots in the open and in glasshouses at Wageningen in The Netherlands, were at times found heavily infested with aphids which may have been Neotoxoptera formosana. In July 2000, Neotoxoptera formosana was reported for the first time in Italy. It was found on Allium schoenoprasum (chives) grown under glass as a continuous crop (Barbagallo & Ciampolini, 2000). It was reported from Germany in 2008 (Schrameyer 2008), and confirmed from The Netherlands in 2008 (Piron, 2010).

The onion aphid was first reported in Britain on onion at RHS Wisley in October 1999 (Halstead, 2000). Attempts to 'eradicate' Neotoxoptera formosana in Britain appeared successful, although the pest was again found on Allium at Wisley in May 2000 having probably overwintered on garlic cloves in a cold frame. Infested plants were sprayed and the pest was considered eradicated at Wisley. Winged aphids (see picture below) have since been trapped several times in 40ft aerial suction traps (MacLeod, 2007), but for some time it was unclear whether these were migrants from resident British populations or from mainland Europe.

Image copyright fera, all rights reserved.

We first came across Neotoxoptera formosana in Britain as a flourishing colony on an onion purchased at a supermarket in Inverness, Scotland in August 2013 (see picture below). At that time this was only the second record of the species from Scotland since it was first reported from Fife in 2008 (Reid, pers. comm.).

We have since received several reports of likely Neotoxoptera formosana infestation in Britain, and were able to confirm identifications for records in 2016 from Norfolk and from Hertfordshire. Pictures of those found in in Hertfordshire are shown below.

Both images above copyright Alan Outen, all rights reserved.

Then in August 2020 we received a report from a garden in Kent. Sharp-eyed readers may note several cecidomyiid larvare among this colony.

Image above copyright Chris Wallwork, Agrii, all rights reserved..

Two months later (October 2020) we received a report of large numbers of dark aphids on chives (Allium schoenoprasum) in Abbotts Ann, Andover, Hants.

Image above copyright Alex Shaw, all rights reserved.

We were able to examine a sample of the aphids on chives and confirmed their identity as Neotoxoptera formosana (see picture below).

The frequency of observations of field populations by us and other workers (e.g. Wieczorek et al., 2019) supports the view by Blackman (2010) that the species is now widespread and well established in Britain.  

Development & behaviour

Rather few observations seem to have been made on the biology of Neotoxoptera formosana. Costa et al.(2012) assessed the development and reproduction of the chrysopid Chrysoperla externa when fed with Neotoxoptera formosana. They concluded that the aphid is a viable food source for Chrysoperla externa and that the predator's potential for pest management programmes should be investigated.

Piron (2010) observed that the 'crowding effect' (the development of winged forms when food runs out) - did not to seem to operate for onion aphids since no alates developed in his food-stressed colonies. However, different aphid species uses different environmental cues (for example day length) and one cannot conclude (as Piron did) that the aphid has poor dispersal abilities.

Hori & Komatsu (1997) investigated the olfactory behaviour of Neotoxoptera formosana to host and non-host plant odours. They were attracted by odours of Allium species, and repelled by odours of some non-host plants, namely rosemary and pennroyal. Hori (2007) identified the two sulphur compounds in Allium plants, dipropyl trisulphide and diallyl sulphide, responsible for attracting the aphids, and concluded that they used these as olfactory cues to find the host plants.

 

Other aphids on same host

Neotoxoptera formosana has been recorded on 19 species within the Allium genus.

 

Damage and control

Neotoxoptera formosana populations can build up rapidly to damaging levels. Feeding damage on Allium schoenoprasum, reported in Italy, include wilting, yellowing and desiccation (Barbagallo & Ciampolini, 2000). Neotoxoptera formosana may also transmit plant viruses. In Japan, it has been shown to transmit Garlic latent virus (GarLV) between Allium species (Sako et al., 1990). It can also transmit Alstroemeria mosaic virus (AlMV) (Yasuda et al., 1998) and an unidentified virus that produces mosaic symptoms, leaf curling, yellowing and dwarfing in garlic (Abiko et al., 1980).

Acknowledgements

We thank fera for the image of Neotoxoptera formosana alates, and Alan Watson Featherstone for providing us a live colony on onion. We also thank Alan Outen (founder of the Bedfordshire Invertebrate Group) and Chris Wallwork (Agrii) for providing us with pictures of the aphid colonies. We especially thank Dr Alex Shaw for sending us live specimens of Neotoxoptera enabling us to take several of the pictures included on the page.

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

  • Abiko, K. et al. (1980). Studies on garlic mosaic. I. Causal virus. Bulletin of the Vegetable and Ornamental Crops Research Station, A. 7, 139-147. Abstract

  • 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

  • Costa, M. B. et al. (2012). Development and reproduction of Chrysoperla externa (Neuroptera: Chrysopidae) fed with Neotoxoptera formosana (Hemiptera: Aphididae). Revista Columbiana de Entomologia 38(2), 187-190. Full text

  • Van Dijk, P. (1993). Survey and characterisation of potyviruses and their strains on Allium species. Netherlands Journal of Plant Pathology, 99 (Supplement 2), 1-48. Abstract

  • 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

  • Hori, M. & Komatsu, H. (1997). Repellency of rosemary oil and its components against the onion aphid, Neotoxoptera formosana (Takahashi) (Homoptera: Aphididae). Applied Entomology & Zoology 32(2), 303-310. Abstract

  • Hori, M. (2007). Onion aphid (Neotoxoptera formosana) attractants, in the headspace of Allium fistulosum and A. tuberosum leaves. Journal of Applied Entomology 131(1), 8-12. Abstract

  • Leclant, F. (1999). Les pucerons des plantes cultivées. Clefs d'identification. II. Cultures maraîchères. Acta/INRA.

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

  • Piron, P. G. M. (2010). Appearance of Neotoxoptera formosana (Homoptera: Aphididae) in The Netherlands. Entomologische Berichten 70 (1), 10-12. Full text

  • Sako I. et al. (1990). Transmission and translocation of garlic latent virus in rakkyo (Allium chinense G. Don.). Proceedings of the Kansai Plant Protection Society 32, 21-27. Abstract

  • Schrameyer, K. (2008). Blattläuse auch bei Allium-Arten. Gemüse 2/2008: 24-25.

  • Wieczorek, K. et al. (2019). The composition of the aphid fauna (Insecta, Hemiptera) of the Royal Botanic Gardens, Kew. Scientific Reports 9, Article no. 10000 Abstract

  • Yasuda S, et al. (1998). Characterisation and serodiagnosis of alstroemeria mosaic potyvirus. Japanese Journal of Tropical Agriculture 42, 85-93.