Parasitoids

Unlike parasitoids of other insect orders that have host-seeking larvae, most parasitic hymenoptera lay their eggs on, in, or very close to a host individual [11]. This requires the adult female to find a suitable host, often with the aid of chemical cues from host frass, pheromones, plant volatiles emitted upon host feeding or egg-deposition, silk, honeydew and other secretions. She may then chemically mark the host following oviposition to reduce superparasitism by herself or intra- and inter-specific insects [11]. 

Tetratrophic interactions between a host plant, a phytophagous pest (primary host), a hymenopteran parasitoid or symbiont (secondary host) and a hymenopteran hyperparasitoid (which parasitizes the secondary host) are of considerable importance, because hyperparasitism can significantly reduce populations of economically beneficial parasitoids [11]. Hyperparasitoids use host-marking (=spacing) pheromones, sex pheromones [12], and host-detection cues [42], but they also show additional chemically mediated interactions with the other partners. These include detection of the primary host s secretions by the hyperparasitoid [43], detection of plant volatiles by the hyperparasitoid [44], and detection of the hyperparasitoid s secretions by the primary host [45] or by the secondary host. The latter causes the secondary host to avoid locations where the hyperparasitoid is foraging [46]. 

Parasitic hymenoptera hold promise in integrated pest management schemes, because they parasitize many economically important insect pests in a species-and stage-selective manner. The pheromones and kairomones of the parasitic hymenoptera have been studied for a long time, and there are many examples where there is evidence of chemical mediation of parasitoid behavior. This review emphasizes work done since the last major reviews [11, 12, 42] and, where it is available, on the primary bioassay-guided chemical identification of the semiochemical (Fig. 2 and Tables 3 and 4). 

Several long-range attractant sex pheromones have been identified (Table 3) or evidence for such a pheromone has been obtained in the past 13 years. The parasitoid Ascogaster reticulatus produces (9Z)-hexadec-9-enal 9 in a tibial gland [47]. The pheromone is spread by the females much like a trail on the substrate, and the males follow the mark to the source by close antennal contact with the substrate [48]. EAG studies have revealed that the males respond much more strongly to (9Z)-hexadec-9-enal than the females and that the response to the... 

Indication of a sex attractant has also been obtained for the noctuid pupal parasitoid Diapetimorpha introita (Ichneumonidae). Antennae from D. introita males gave EAG responses to diethyl ether extracts of female head, thorax or abdomen. Antennae from females did not respond to this chemical signal and male extracts elicited no activity. This suggested the presence of an extractable female-produced pheromone, to which the males respond. While live females were able to attract males, extracts were not active. This may be due to very low levels of biologically active material in the extracts [57]. 

Synergy between polar and nonpolar components is indicated for sex attraction in the larval parasitoid Eriborus terebrans (Ichneumonidae) [58]. Males show several behaviors when exposed to a polar component with chemical... 

In Alloxysta victrix, 6-methylhept-5-en-2-one 16, which is produced by both males and females, was identified as potentially attractive to the males and slightly repellent to the females in Y-tube olfactometer assays [60]. In this study, the activity was also dependent on prior exposure of the insects to the compound. Naive insects responded more strongly than previously exposed ones. This underscores a second difficulty in the bioassay-guided identification of parasitoid hymenopteran pheromones the responses are very dependent on the context and on prior exposure. Learning has been demonstrated in several species of parasitic hymenoptera [61-65]. 

Host marking pheromones are important in many species of parasitic hymen-optera, because they ensure that a female parasitoid focuses on non-parasitized hosts. This, in turn, ensures a more effective use of limited host resources. Marking pheromones can be internal (injected into the host at the time of oviposition) or external (applied to the host during inspection and/or ovipo-sition). The internal markers can be detected by sensory hairs on the parasitoid ovipositor [11]. The internal markers often also delay the development of the host. 

Defensive substances are often general irritants that can be used in a variety of contexts. For example, the alloxystine wasps (Cynipoidea), all hyperpara-sitoids of other hymenopteran parasitoids, produce a large number of compounds in their cephalic (mainly mandibular) glands. These compounds include m/p-xylol, 6-methylhept-5-en-2-one 16, various iridoids 21 and frans-dihydro-nepetalactone 22 [46,73]. 

Parasitic hymenoptera often eavesdrop on the pheromone communication of their host species. The type of host pheromone recognized depends on the host stage parasitized. Phoretic egg parasitoids are often attracted by the host sex pheromone, while species that parasitize later stages (larval, pupal) often do not respond to host sex pheromone components [ 11,42]. Larval parasitoids often recognize volatiles from the damaged host plant and/or host larval frass volatiles. Parasitoids of forest beetles respond to the beetle aggregation pheromones [42]. 

An example of a larval parasitoid that responds to the host sex pheromone is seen with Cotesiaplutellae (Braconidae), also a parasitoid of the diamondback moth. These insects were attracted equally to the pheromone blend (31,32,33, see above), the acetate 32, or aldehyde 31 components [80]. This larval parasitoid, however, was also strongly attracted to host frass volatiles, in particular, dipropyl disulfide 34, dimethyl disulfide 35, allyl isothiocyanate 36, and dimethyl trisulfide 37. In contrast, the egg parasitoid Trichogramma chilonis was only weakly attracted to 36. In both, T. chilonis and C. plutellae, plant volatiles, in particular (3Z)-hex-3-en-l-yl acetate 38, significantly enhanced attraction by the pheromone [80]. 

Several other examples of host plant recognition by hymenopteran parasitoids have been described recently. Six species of aphid parasitoids, Aphidius ervi, Trioxys sp., Praon sp., Aphelinus flavus, Lysiphlebus fabarum, and Aphidius rophalosiphi were most strongly attracted to their host aphid in combination with the damaged host plant [62]. For A. rhopalosiphi, three wheat volatiles were... 

Table 4 Recently identified parasitoid semiochemicals. Numbers in bold refer to chemical structures shown on Fig. 2... 

Taxon Host [stage] Kairomone [parasitoid response] Chemical Name(s) Ref. 

Egg-deposition also can induce the host plant to emit volatiles that attract egg parasitoids. For example, egg deposition by the elm leaf beetle (Xantho-galeruca luteola) causes its host plant, the field elm (Ulmus minor), to release a blend of mostly terpenoids that attract the egg parasitoid Oomyzus galleru-cae (Eulophidae) [ 86]. Although the specific compounds that initiate the volatile emission and that attract the egg parasitoid are unknown, the host plant response can be induced with jasmonic acid. 

One recent study addressed the response of a parasitoid to the host s spacing pheromone. Aphidius rhopalosiphi did not respond to the spacing pheromone of one host, the cherry-oat aphid Rhopalosiphum padi, which consists of 6-methylhept-5-en-2-one 16,6-methylhept-5-en-2-ol, tridecan-2-one and methyl salicylate. These compounds did not attract or repel the parasitoid. Because the aphid spacing pheromone can potentially be used to cause aphids to disperse, the failure of the parasitoid to respond to the spacing pheromone makes simultaneous use of the spacing pheromone and the parasitoid possible in aphid management [87]. 

Alarm signals produced by stressed hosts also attract parasitoids. For example, stressed aphids (Aphidius sp.) were attractive to female parasitoids of two... 

Detection of the hyperparasitoid by the primary parasitoid has also been recently described. The parasitoid Aphidius uzbekistanikus detects trans-fused iridoids 21 produced by females of the hyperparasitoid A. victrix as part of their defensive cephalic gland secretion. The iridoids cause avoidance behavior in A. uzbekistanikus [46]. 

Kainoh Y (1999) Parasitoids. In Hardie J, Minks AK (eds) Pheromones of non-lepi-dopteran insects associated with agricultural plants. CABI Publishing, New York, p 383... 

Phyletic links of apparent endemic species of the central Ebro valley with easternmost species were revealed after studying the insect communities at the Monegros region. These have a pre-Pleistocene origin of their relict distributions, associated with the persistence of steppe habitats over gypsiferous soils in the area since the Late Tertiary. Distributions of phytophages and their parasitoids on plants such as Krascheninnikovia ceratoides or Juniperus thurifera supported the continuity of their presence in the central Ebro valley through the Quaternary [14]. 

Zaki, F.N. and M.A. Gesraha. 1987. Evaluation of zertel and diflubenzuron on biological aspects of the egg parasitoid, Trichogramma evanescens Westw. and the aphid lion Chrysoperla camea Steph. Jour. Appl. Entomol. 104 63-69. 

At present only Trichogramma species and the scelionid egg parasitoid Telenomus remus (20) are known to respond to moth sex pheromones. However, this phenomenon could be much more widespread and overlooked because these wasps apparently do not fly to point sources and are not caught in pheromone traps. 

All of the long-range kairomones attractive to parasitoids that have been identified thus far are sex pheromones of the hosts. However, we are probably aware of only a small fraction of the predators and parasites that are eavesdropping on the pheromonal communications of their prey or hosts. While the evolution of individuals that are as inconspicuous as possible to their enemies is favored, it is impossible for a species to completely avoid emitting chemical signals. Thus, pheromones that are important to reproduction or other vital functions, and are good indicators of the presence of a species, are available for predators or parasitoids to exploit. 

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