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Encyclop'Aphid : l'encyclopédie des pucerons

Encyclop'APHID

Primary and secondary parasitoids

The parasitoids of aphids

The parasitoids are distinguished from parasites by their aptitude for killing their sole host through their larval development, accomplished either inside (endoparasitism) or on the outside (ectoparasitism) of that organism. They can be divided into koinobionts in the strategy where the host is not killed at the moment of egg-laying and idiobionts when the opposite is the case. The parasitoids of aphids belong to two orders of insects: the Diptera and the Hymenoptera. There are also some representatives of the class Arachnida, from the suborder Prostigmata (acarians, mites).

Dipteran parasitoids

In the Diptera only one parasitoid species is currently known in Europe (just 6 in the world). It is Endaphis perfida Kieffer, in the Cecidomyidae. The female of this species lays her egg near the aphid. Its larva is capable of seeking out its host over short distances. It enters the host actively through the latter’s inter-segmental junctions. It then develops into a koinobiont endoparasitoid. At the end of its cycle, it emerges by the aphid’s anus before undergoing nymphosis in the ground. The only known host is the common sycamore aphid, Drepanosiphum platanoidis.

Hymenopteran parasitoids

The parasitoid Hymenoptera of aphids are divided into primary (Aphelinidae and Braconidae families) and secondary (even tertiary) parasitoids or hyperparasitoids (the families Pteromalidae, Encyrtidae, Eulophidae, Megaspilidae, Charipidae).

Primary parasitoids

In the Aphelinidae family (Chalcidoidea) only the genera Aphelinus (about 30 species in Europe) and Protaphelinus (one species) have the ability to parasitize aphids.

The Aphelinus are small-sized chalcid wasps sometimes measuring less than 1mm. They are solitary koinobiont endoparasitoids. The egg is laid following a specific behaviour. With her antennae the female palpates her future host, briskly turns 180° and while moving backwards performs her egg-laying using a long tapering ovipositor. The larva accomplishes its whole development inside the aphid which is also the site for undergoing nymphosis. The aphid then becomes black and oblong as if mummified. The adult emerges after cutting a round opening, often in the hind area of the mummy. These insects have also adopted predatory behaviour. Some of the attacks they make involving injection aim to take nutrients for the female. She does this as if to lay an egg: she pierces the aphid with her ovipositor but instead of laying an egg, ingests haemolymph which oozes out of the aperture. This action causes the death of the aphid. Most aphid hosts of Aphelinus belong to the Aphididae family.

In the Braconidae family (Ichneumonoidea), only the subfamily Aphidiinae is strictly dependent on aphids. About 27 genera are concerned totalling about 120 parasitoid species in France (210 in Europe, 600 in the world).

The Aphidiinae are solitary koinobiont endoparasitoids. Their size varies from 1 to 3mm. After mating the female goes prospecting in aphid colonies for suitable hosts generally selected over a well-defined range (from just a single species of aphid to several tens parasitized depending on the specificity of parasite). Once the future host has been recognized by antennal palpation, the abdomen is brought forward between the legs until the ovipositor, which is quite short, comes into contact with the aphid, inoculating the egg into different parts of the body. The larva then proceeds with its whole development (3 larval stages) in the aphid’s general cavity. It does not attack the vital organs until the very end of its cycle, but this causes the death of the host. The larva weaves a cocoon, generally inside the aphid but sometimes also on the outside (Praon sp.). The aphid then looks like a mummy fixed to the support by silk thread. This globular mummy can be light coloured (white to coppery) or black according to species or genera. The adult parasitoid cuts an opening, often held by a hinge, and emerges.

At 20° the complete parasitoid cycle, from egg-laying to emergence, can be accomplished in 15 days. A female can lay about 300 eggs. The sex-ratio is mainly biased towards females. As is the rule in Hymenoptera, only eggs fertilized by males give rise to females. Nevertheless in the Aphidiinae (Lysiphlebus sp.) there are some examples of thelytoky (parthenogenesis whereby females engender females without fertilization). The adults of Aphidiinae feed essentially on honeydew but also on extrafloral nectaries of certain Fabaceae (leguminous plants).

See cycle of primary parasitoid

Hyperparasitoids

The hyperparasitoids can be divided into secondary parasitoids, when they develop at the expense of a primary parasitoid, or tertiary ones when the host is itself a hyperparasitoid.

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Acarian parasitoids

The acarians concerned are ectoparasitoids at the larval stage, but the adults are polyphagous predators which may also eat aphids.

The female of Allothrombium fuligineum, mated in the autumn or in spring, spends winter sheltering in the ground. The following spring, if fertilized, she lays 700 to 1500 spherical eggs in a small crack in bark or in the ground. On hatching these produce larvae which will actively seek a host to attach themselves to as an ectoparasite. To do that they need a period of a few days; any longer than a week still without a host and they are doomed. If successful they fix indiscriminately onto any part of the aphid’s body, taking just 3-4 days to draw enough nutrients from the host to continue their development. The aphid’s development is blocked and it soon dies. The larvae then let go to move onto the ground in preparation for their first metamorphosis. After one month a “pre-adult” acarian emerges, a predatory form that feeds on many types of prey, aphids included. In the autumn, a second metamorphosis occurs. The adult generally emerges before winter, ready to mate.

Classification of principal parasitoids