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Identification & Distribution

Adult apterae of Therioaphis ononidis (see pictures below) are rather small and yellowish. The apical rostral segment (RIV+V) is longer than second hind tarsal segment (HTII), and has 8-12 accessory hairs. The dorsal hairs arise from pigmented bases and are mostly long and capitate. Abdominal tergites I-VII usually each bear 4 hairs, one spinal and one marginal on each side (cf. Therioaphis trifolii which has 7-10 hairs on each of abdominal segments I-V). The dusky siphunculi are stump-shaped, flangeless, and very short. As with other Therioaphis species, the cauda of Therioaphis ononidis is rather large, and has a constriction and a knob-like apex. The body length of adult apterae is 1.8-2.2 mm.

The alate Therioaphis ononidis (shown below) has brownish shadowing along the wing veins, ending in small brown triangular spots on the wing margins.

Both images above by permission copyright Ole Bidstrup, all rights reserved.

The micrographs below show an adult aptera of Therioaphis ononidis in isopropylalcohol, rear-dorsal and front-ventral views.

Therioaphis ononidis feeds on rest harrows (Ononis species), especially common rest harrow (Ononis repens) and spiny restharrow (Ononis spinosa). It does not host alternate, but remains all year on restharrow. Oviparae and alate males occur in October, with eggs laid on the stems and leaves of its host. The spotted restharrow aphid is found throughout Europe, the Middle East and Central Asia. Records from North America are thought to be misidentifications of Therioaphis trifolii.  

Biology & Ecology

Habitat

Therioaphis ononidis is considered by Stroyan (at least by implication) to be the least rare of the Therioaphis species in Britain - it is described as 'local' whilst the other species are described as rare or very rare. In Britain it feeds on common rest harrow (Ononis repens, see picture below) or spiny restharrow (Ononis spinosa).

We have so far only found the spotted restharrow aphid on common restharrow (Ononis repens), a plant largely restricted to chalk downland. Sites in East Sussex where the aphid occurs are Malling Down Nature Reserve, near Lewes and Birling Gap on the coast.

The plants at Malling Down were thriving, whilst those at Birling Gap were small stunted plants growing alongside a heavily used footpath beside an unpaved vehicle track (see picture above). Aphid numbers were quite low at each site, and populations were comprised only of viviparous apterae - we found no alatae nor any alatoid fourth instar nymphs.

Plant defences

For a member of the Leguminosae with a wide distribution, common restharrow (Ononis repens) has rather few aphid species living on it - only seven worldwide including two specialists - Therioaphis ononidis and Acyrthosiphon ononis. This may result from the leaves bearing glandular secreting trichomes, which are generally thought to have a defensive function against herbivores.

We can find no studies caried out on the glandular hairs of restharrow, but Corsi & Bottega (1999) looked at the glandular hairs of Salvia officinalis and their defensive function against insects that feed on that plant in Italy. We summarise the results of that work on our page on Aphis passeriniana.

The picture below shows the normal feeding position of Therioaphis ononidis.

On the leaf shown above the aphid is holding its body well above the glandular tips of the hairs. First instars move below the level of the glandular tips.

At Birling Gap the aphids (and their host plants) lived in a somewhat 'challenging environment' subject to repeated trampling. There they were well sprinkled with sand grains, and the occasional drop of exudate stuck to their body hairs, presumably as a result of the frequent disturbance.

Natural enemies

Cano & Saval (1998) report that Therioaphis ononidis (and other Therioaphis species) are parasitized by Praon exsoletum. Praon parasitoids differ from other Aphidiinae by pupating in a silk cocoon under the dead aphid, rather than within the dead aphid.

We recorded a different parasitoid species, probably an Aphidius species (see pictures below of aphid mummies).

The parasitoid is unfortunately unidentified as no adult parasitoids emerged from the mummies collected.

There seem to be rather few instances of recorded predators of Therioaphis ononidis. Hodek (2013) reports that in Central Asia when Aphis pomi populations on fruit trees crash in mid-July, many of the the Coccinella undecimpunctata predators migrate to alfalfa fields where they feed on Therioaphis ononidis and Acyrthosiphon pisum (but, since Thereioaphis ononids is not supposed to occur on alfalfa, this may be based on a misidentification of the Therioaphis species).

Another unusual looking hemipteroid species also lives on the trichome-rich rest harrow - a stilt bug Gampsocoris punctipes (family Berytidae). This fragile-looking species is xerophilic, being found especially in dry sandy areas. Hence it was not surprising to find it at Birling Gap, sometimes on the same plants as Therioaphis ononidis. Gampsocoris punctipes is currently thought to be entirely phyophagous on Ononis, sucking not only plant tissues but also the resinous drops on the glandular hairs (Taszakowski, 2015). The picture below shows a late instar nymph.

The picture below shows an adult of Gampsocoris punctipes.

We have found no reports of Gampsocoris punctipes predating Therioaphis aphids, but given the feeding habits of some other berytids, it certainly cannot be ruled out.

An increasing number of studies have shown that berytids, previously thought to be entirely phtyophagous, supplement their diets with animal food. The preference of most stilt bugs for plants with glandular hairs seems to enhance their chances of scavenging prey trapped in the sticky hairs of their various hosts. Various species have also now been shown to be active predators (e.g. Kohno & Hirose (1997) describe the stilt bug Yemma exilis predating Aphis gossypii on eggplant).

 

Other aphids on the same host

Therioaphis ononidis has been recorded from 4 Ononis species (Ononis diffusa, Ononis repens, Ononis spinosa, Ononis tridentata).

Blackman & Eastop list 18 species of aphid as feeding on restharrows Ononis spp. worldwide, and provide formal identification keys (Show World list). Of those aphid species, Baker (2015) lists 9 as occurring in Britain (Show British list).

Acknowledgements

We especially thank Ole Bidstrup for allowing us to reproduce two of the images shown above, and Danmarks Fugle og Natur for kindly passing our request to him.

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

  • Cano, V.A.S. & Saval, J.M.M. (1998) . Afidinos (Hymenoptera: Braconidae) y relaciones pulgón-parasitoide en la provincia de Valencia. Boln. Asoc. esp. Ent. 22 (3-4), 75-90.

  • Corsi, C. & Bottega, S. (1999). Glandular hairs of Salvia officinalis: New data on morphology, localization and histochemistry in relation to function. Annals of Botany 84, 657-664. Full text

  • Hodek, I. (2013) Biology of Coccinellidae. Chapter 5: Distribution in Habitats. Springer Science and Business Media.

  • Kohno, K & Hirose, Y. (1997) . The stilt bug Yemma exilis (Heteroptera: Berytidae) as a predator of Aphis gossypii (Homoptera: Aphididae) and Thrips palmi (Thysanoptera: Thripidae) on eggplant. Applied Entomology & Zoology 32(2), 406-409. Full text

  • Stroyan, H.L.G. (1977). Homoptera: Aphidoidea (Part) - Chaitophoridae and Callaphidae. Handbooks for the identification of British insects 2 (4a). Royal Entomological Society, London. Full text

  • Taszakowski, A. (2015) . Notes on the occurrence of Gampsocoris Fuss, 1852 (Hemiptera: Heteroptera: Berytidae) in Poland. Fragmentia Faunistica 58(1), 1-6. Full text