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Identification & Distribution

Adult apterae of Aphis oenotherae (see first picture below) are pale yellowish green to dark green, and are lightly wax powdered. The ratio of the antennal terminal process to the base of antennal segment six (PT/base) ranges from 1.9-2.5 and is usually more than 2 (cf. Aphis holoenotherae for which that ratio ranges from 1.5-2.3 and is usually less than 2). The length of the terminal process is more than 0.23 mm (cf. Aphis holoenotherae where the length of the terminal process is less than 0.22 mm.). There are no marginal tubercles on abdominal tergites 2-6 (cf. Aphis grossulariae  which has marginal tubercles on most of abdominal tergites 2-6). The siphunculi and cauda are completely pale (cf. Aphis nasturtii  which has the siphunculi darkened just at the apices). The body length of the adult Aphis oenotherae aptera is 1.5-2.0 mm.

The alate Aphis oenotherae (see second picture above) has the head and most of the thorax black, the abdomen green with dusky marginal sclerites, and the siphunculi dusky. Immatures (see picture below), especially of future alatae, have paired pale white wax patches on the dorsum.

The identity of anholocyclic populations in south and west Europe is uncertain, and specimens from there are sometimes classified as intermediate between Aphis oenotherae and Aphis holoenotherae. Specimens taken from the same colonies as those pictured on this page keyed out to Aphis oenotherae on the basis of the ratio of the antennal terminal process to the base of antennal segment 6 (values of 2.3-2.5 for 3 specimens). The pictures below show an adult aptera and an alate in alcohol.

In America Aphis oenotherae is thought (but not confirmed) to host alternate between currant species (Ribes spp.) and various members of the Onagraceae, including evening primrose (Oenothera biennis) and willowherbs (Epilobium spp.).

In Europe Aphis oenotherae was formerly thought to occur throughout Europe as invasive anholocyclic populations, mainly on evening primrose. However, those in northern and eastern Europe have now been described as another species, namely Aphis holoenotherae, based on DNA analysis. The identity of those in southern and western Europe (such as those pictured here) remains uncertain, but is currently accepted as Aphis oenotherae.

 

Biology & Ecology

Systematics

Aphis oenotherae is an American species that was introduced to Europe in the latter part of the 20th century. In Britain its arrival was first noted by Martin (2000).  Several European workers have since examined the taxonomy and systematics of aphids which are capable of living on evening primrose plants in Europe.

Turcinaviciene et al. (2006)  used molecular techniques to examine phylogenetic relationships among Aphis species inhabiting Palaearctic currant (Ribes) and/or willowherb (Onagraceae). Palaearctic species of the subgenus Bursaphis (= “grossulariae” species group of the genus Aphis) were shown to form a monophyletic group within the genus Aphis. Molecular data clearly showed that European Aphis oenotherae differ from the morphologically similar Aphis grossulariae. There are also differing ecological features. Aphis grossulariae alternates between Ribes species and Epilobium species and only occasionally occurs on Oenothera species, whilst Aphis oenotherae in Europe inhabits mainly Oenothera species. The DNA data strongly corroborated the viewpoint that Aphis oenotherae is a separate species and not an anholocyclic derivative of Aphis grossulariae. Genus Oenothera (evening primrose) seems to have a specific host plant status: only one aphid species (Aphis oenotherae) is well adapted for feeding on it (but see below for later research which identified Aphis holoenotherae). Other species colonize evening primrose only occasionally. This might be due to the specific biochemical compounds in Oenothera-species (Rostanski et al., 2004.)  Nevertheless, attempts to colonize Oenothera still occur, as recently parthenogenetic apterous and winged females, together with oviparae and males of Aphis epilobiaria  and Aphis praeterita,  were found on Oenothera secies in the Czech Republic. Winter eggs were deposited in great numbers but the fundatrices of these species were unable to feed on Oenothera in spring.

Rakauskas (2007)  noted that the recent description of the (northern and eastern) European species, Aphis holoenotherae, distinct from the American and (northern and eastern) European Aphis oenotherae, demonstrated the need for re-examining the current state of knowledge of Aphis species inhabiting evening primroses in Europe. His study, based on published original data, revealed nine aphid species of the genus Aphis which are capable of living on Oenothera plants in Europe. Only two of them are really dependent on Oenothera species during their life cycle: Aphis oenotherae and Aphis holoenotherae. They have different life cycles and host plant spectrum, although they are very close in their morphology. Antennal terminal process length appeared to be the most reliable morphological character in distinguishing between Aphis oenotherae and Aphis holoenotherae at the present time. Aphis grossulariae is not a typical Oenothera-feeder in Europe, occurring on evening primroses only by chance. Other Aphis species (epilobiaria,  fabae,  frangulae,  nasturtii,  praeterita,  sambuci ), are opportunistic inhabitants of evening primrose.

Ant attendance

Aphis oenotherae is often attended by ants which feed on the honeydew, and protect the aphids from some of their natural enemies (but not from the parasitoid Lysiphlebus fabarum - see below). In the USA Jones (1927)  recorded two species of ants attending Aphis oenotherae, Formica fusca and Myrmica brevinodis var. sulcinodoides.

We have found Lasius ants attending Aphis oenotherae on evening primrose.

The pubescence on the clypeus suggests this ant is Lasius niger.

Natural enemies

Despite being closely attended by Lasius ants, Aphis oenotherae is sometimes heavily parasitized by aphid parasitoids, especially by (possibly only by) Lysiphlebus fabarum (Tomanovic et al. (2003) ). We have tentatively identified the parasitoid below as Lysiphlebus fabarum.

 

Lysiphlebus fabarum has evolved various adaptations for foraging within ant-tended aphid colonies (Rasekh et al., 2010 ) and the ants make no attempt to stop these parasitoids from attacking the aphids.

In fact foraging Lysiphlebus fabarum females have been observed to remain longer, and parasitize more aphids, in ant-tended colonies than in unattended colonies (Völkl and Stechmann, 1998 ). The picture below shows a Lysiphlebus parasitoid in the act of parasitizing a fourth instar alatiform nymph.

The parasitoids benefit from having the ants protect their developing larvae, within the aphids, from predators.

Other species on the same host

Primary? hosts

Blackman & Eastop  list Aphis oenotherae on 8 Ribes species, including Ribes aureum (Golden currant), Ribes nigrum (blackcurrant), Ribes uva-crispa (gooseberry), and possibly Ribes rubrum (redcurrant).

Secondary? hosts

 

Damage

Aphis oenotherae lives on the flower buds, stem and leaves of evening primrose (Oenothera biennis).

It causes severe deformations to the growing tip and may completely stunt the plant. The picture below shows the growing tip of a stunted plant, about 30 cm high, infested with Aphis oenotherae.

Acknowledgements

We especially Bridget O'Dell for her kind assistance, and permission to sample.

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

  • Jones, C.R. (1927). Ants and their relation to aphids. PhD Thesis, University of Iowa. 51(1), 97-105. Abstract 

  • Martin, J.H et al. (2000). Two new British aphid introductions in 1999, in the context of other additions over the proceeding thirty years (Sternorrhyncha: Aphidoidea). Entomologist’s Gazette 51(1), 97-105. Google Scholar 

  • Rakauskas, R. (2008). Species of Aphis inhabiting European Oenothera: their biology, morphology and systematics (Hemiptera: Aphididae). Central European Journal of Biology 3(3), 307-319. Full text 

  • Rasekh, A. et al. (2010). Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum 10, Article 126. Full text 

  • Rostanski, K. et al. (2004). The genus Oenothera L. in Eastern Europe. Institute of Botany, Krakow, 134 pp.

  • Tomanovic, S. et al. (2003). Some adventive plant invaders as hosts of various aphid - aphid parasitoid associations. Ecologija 38 (1-2), 25-30. Abstract 

  • Turcinaviciene, J. et al. (2006). Phylogenetic relationships in the “grossulariae” species group of the genus Aphis (Hemiptera: Sternorrhyncha: Aphididae): Molecular evidence. European Journal of Entomology 103(1), 597-604. Full text 

  • Völkl, W & Stechmann, D.H. (1998). Parasitism of the black bean aphid (Aphis fabae) by Lysiphlebus fabarum (Hymenoptera, Aphidiidae): The influence of host plant and habitat. Journal of Applied Entomology 122, 201-206. Abstract