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Eriosomatinae : Fordini : Paracletus cimiciformis
 

 

Paracletus cimiciformis

Vampire pistachio-grass root aphid

On this page: Identification, Lifecycle & Distribution Other aphids on the same host

Identification, Life-cycle & Distribution

The fundatrix of Paracletus cimiciformis induces a gall on its primary host, Pistachio (Pistacia spp.). The gall is a flat fold which develops from the leaf edge (see first picture below), retaining the original yellow-green colour of the leaf underside (cf. galls of Forda marginata on Pistacia, which turn bright red). The mature fundatrix (not pictured) in the gall is globose, yellow, with 6-segmented antennae, and a body length of about 1.5 mm. The second generation are all alatae which emerge from the gall in September-October.

The alate vivipara of Paracletus cimiciformis (not pictured) has large, prominent black eyes. The antennae are about 0.4 times body length, and have an extremely short terminal process (cf. various Forda species and Smynthurodes betae, which all have the terminal process as long as, or longer than, its basal width). Secondary rhinaria are distributed 39-50 on antennal segment III, 22-40 on segment IV, and 7-17 on segment V. The thorax is darker than the abdomen, and the sides are pale yellowish. The legs are mainly brown, but the femora bases and to some extent tibiae bases are yellowish. There are no siphunculi. The body length of these alatae is 1.5-2.0 mm.

These winged forms leave to found colonies, mainly of apterae, on their secondary hosts, the roots of many species of grasses (Poaceae, including Agrostis, Brachypodium, Dactylis, Festuca, Hordeum, Oryza, Poa, Polypogon, & Triticum).

First image reproduced by permission, copyright Nicolás Pérez, all rights reserved;
Second image copyright Anders Albrecht, under a Creative Commons Attribution 3.0 License.

On the secondary host, Paracletus cimiciformis has two alate morphs, the dispersive viviparae and sexuparae, plus two morphologically distinct wingless morphs. Until recently, the only known wingless root-dwelling morph in this species was a flat yellowish-white aphid (see pictures below) which lived within ants nests (Tetramorium spp). However, Roberti (1983, 1993) proposed the existence of two different wingless secondary host 'forms' in this species:

  • Form A, or 'round morph', then referred to as Paracletus rotunda; with 5-segmented antennae, eyes composed of just the triommatidium, straight hind tibiae and a round-shaped (= domed) body.
  • Form B, or 'flat morph', the accepted Paracletus cimiciformis; with 6-segmented antennae, eyes composed of several ommatidia in addition to the triommatidium, curved hind tibiae and flat-shaped body.

Roberti's suggestion was not generally accepted, until Ortiz-Rivas (2009) used molecular methods to confirm the synonomy of the 'round morph' (Paracletus rotunda) with the 'flat morph' (Paracletus cimiciformis). Each of these two morphs is able to produce both morphs through parthenogenesis, although the factors triggering the production of one morph or the other remain unknown.

Apterae of the 'round morph' of Paracletus cimiciformis are coloured dusky-olive to apple-green (the second picture above appears to represent this morph). Like other Fordini, they have a high domed body. The antennae are 5-segmented. The eyes are triommatidia. The hind tibiae are straight.

Apterae of the 'flat morph' of Paracletus cimiciformis are shining white or yellowish white (see two pictures below). The body is flattened, especially the margins, with longitudinal dorsal rows of muscle sclerites, and a ventral grove between the middle coxae. The cuticle is reticulate with numerous short hairs. There are indentations on the posterior edge of the genital plate, and in front of the anal plate. The antennae are about 0.3 times as long as the body, and are 6-segmented. Antennal segment III is about 2-3 times as long as segment II, and 1.1-1.5 times segment IV. The rostrum reaches past the hind coxae. The legs are strongly built, the hind tibiae are curved and very long. The body length of these adult apterae is 2.4-3.5 mm.

Both images above image copyright Hjalte Kjaerby under a Creative Commons Attribution 3.0 License.

Both apterous morphs interact closely with Tetramorium ants, but in rather different ways. The "round morphs" have a conventional mutualistic relationship with the ants, providing honeydew when subjected to antennal waving and antennation by the ants, and occasionally getting eaten by them. The "flat morphs" mimic the cuticular hydrocarbon profile of ant larvae, and when attended by the ants they respond by retracting their limbs and lying motionless. The ants then pick up the aphids (see first picture above) and transport them to the nest where they are licked, which sometimes produces some honeydew for the ants. They are then taken to the brood chamber and deposited amongst ant larvae (see second picture above, and picture below). There the "flat morph" aphids suck the ant larva haemolymph, a relationship described by Salazar (2015) as aggressive mimicry.

Image above image copyright Sean Birk Bek Craig under a Creative Commons Attribution 3.0 License.

Paracletus cimiciformis is holocyclic in warm climates, and host alternates between Pistacia (most commonly Pistacia terebinthus) and the roots of grasses. Host alternation takes place over a two year cycle. The eggs on Pistacia hatch in spring of year 1, and the fundatrix induces a gall. Her offspring live and develop in the gall, all becoming alatae, which move to the roots of grasses in autumn. Winter of year 1 & spring of year 2 are spent in the soil as the two different apterous morphs - the round (domed) morph on the roots of grasses, tended by ants, and the flat morph mainly feeding on ant larvae within the ants' nest. These flat morphs produce alate viviparae, which fly to other grasses, and in the summer of year 2, they produce sexuparae which migrate to Pistacia and produce apterous males and oviparae in autumn year 2. The oviparae lay the eggs which hatch the following spring. Paracletus cimiciformis has been recorded from Pistacia in southern Europe, Iran, Israel, Malta and Turkey. Anholocyclic populations on the roots of grasses occur outside the range of the primary hosts throughout Europe, in north Africa and across Asia to Japan, Korea and China.

 

Other aphids on the same host

Primary hosts

Paracletus cimiciformis has been recorded from 4 Pistacia species (Pistacia khinjuk, Pistacia palaestina, Pistacia terebinthus, Pistacia vera).

Secondary hosts

Blackman & Eastop list 66 species of aphid as feeding on grass roots (Poaceae) worldwide (Show world list).

Paul (1977) found at least 16 aphid species recorded on grass roots in Britain (Show British list).

Acknowledgements

We are grateful to Nicolás Pérez for permission to use his image of the gall, and to Anders Albrecht, Hjalte Kjaerby & Sean Birk Bek Craig for making their images of Paracletus cimiciformis available for use under a under a Creative Commons Attribution 3.0 License.

We have used the species accounts given by Heie (1980) together with information from Roberti (1983, 1993), Ortiz-Rivas, B. et al (2009), Salazar et al (2015), Albrecht (2015) and Roger Blackman & Victor Eastop in Aphids on Worlds Plants. We fully acknowledge these authors and those listed in the reference sections as the source for the (summarized) taxonomic information we have presented. Any errors in 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

  • Albrecht, A.C. (2015). Identification guide to Nordic aphids associated with mosses, horsetails and ferns (Bryophyta, Equisetophyta, Polypodiophyta) (Insecta, Hemiptera, Aphidoidea). European Journal of Taxonomy 145 1-55. Full text

  • Heie, O.E. (1980). The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. I. Fauna Entomologica Scandinavica 9, p.199.

  • Ortiz-Rivas, B. et al (2009). Molecular phylogeny of Iberian Fordini (Aphididae: Eriosomatinae): implications for the taxonomy of genera Forda and Paracletus. Systematic Entomology 34, 293-306. Abstract

  • Roberti, D. (1983). Note su alcune specie di Fordinae (Homoptera - Aphidoidea - Eriosomatidae). Entomologica, 28, 141-205.

  • Roberti, D. (1993). Gli Afidi d'Italia (Homoptera - Aphidoidea). Entomologica, 25, 3-387.

  • Salazar, A. et al (2015). Aggressive mimicry coexists with mutualism in an aphid. P N A S 112(4), 1101-1106 Full text

  • Theobald, F.V. (1929). The plant lice or Aphididae of Great Britain 3 p. 202