Patterns of host selection by four species of aphidiid (Hymenoptera) parasitoids: influence of host switching

Abstract.

• 1 We tested switching behaviour in four species of aphidiid parasitoids, using a two-aphid experimental system consisting of second-instar nymphs of pea aphid (Acyrthosiphon pisum (Harris)) and alfalfa aphid (Macrosiphum creelii Davis) feeding on broad beans in the laboratory.
• 2 Aphidius ervi Haliday, A.pisivorus Smith, A.smithi Sharma & Subba Rao, and Pram pequodorum Viereck showed an innate preference for pea aphid when both host species were provided in equal numbers.
• 3 Wasps encountered both aphid species equally but differed in their acceptance of alfalfa aphid. Females of A.pisivorus and P.pequodorum accepted alfalfa aphids when few pea aphids were available, but A. smithi always concentrated attacks on pea aphid. Aphidius ervi super-parasitized an increasing proportion of pea aphids as their availability declined.
• 4 Switching to the alfalfa aphid occurred in A.ervi and P.pequodorum (but not in A.pisivorus and A.smithi) under the condition of a 1:3 ratio of pea aphids:alfalfa aphids. Wasps did not switch when more pea aphids than alfalfa aphids were provided (3:1 ratio).
• 5 Alfalfa aphids were more likely than pea aphids to escape from parasitoid attack.
• 6 Switching to the most abundant host may not be adaptive in these four species of aphid parasitoids. A foraging wasp incurs a potentially higher cost in lost opportunity time when attacking (and failing to oviposit in) alfalfa aphids. In addition, alfalfa aphids may have lower host quality than pea aphids, a difference that could influence offspring fitness.

     

The influence of plant species on attraction and host acceptance inCotesia glomerata (Hymenoptera: Braconidae)

Females of the larval parasitoidCotesia glomerata (L.) use plant-associated cues to locate their lepidopteran host,Pieris rapae L. In this study we investigated the influence of four host plant species,Brassica oleracea var.acephala (‘Vates’ kale),Tropaeolum majus (nasturtium),Lunaria annua (honesty), andCleome spinosa (spider flower), on two components of the host selection process inC. glomerata, namely, attraction and host acceptance. Choice tests in a flight tunnel showed that parasitoids were attracted to some host plant species more than to others in the absence of host larvae.B. oleracea was the most attractive plant species, followed byL. annua, T. majus, andC. spinosa. In previous studies it was shown thatB. oleracea carries highly suitable hosts forC. glomerata and that, in the field, parasitization rates on this plant were the highest. When host larvae were reared on the four host plant species and then transferred to a common substrate (B. oleracea var.capitata, cabbage), plant species that had served as diet for the hosts did not have a significant effect on acceptance for parasitization. Thus, parasitoids were attracted to host plant species differentially, but they did not discriminate among host larvae based on the dietary history of their hosts. ForC. glomerata, it appears that phytochemistry mediates host selection more by influencing parasitoid attraction than it does by affecting host acceptance.     

The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and gregarious generalist parasitoid (Cotesia species)

The main objective of this study was to determine the extent to which host acceptance behaviour as related to host species, age, and defensive behaviour might explain the differences in host use that exist between two congeneric and sympatric species of parasitic wasps. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). Cotesia species differed in their responses to host species (P. brassicae (L.), P. napi (L.) and P. rapae) and developmental stage (early and late 1st, 2nd and 3rd instars). In no-choice tests, host acceptance by C. rubecula was higher for p. rapae and females did not distinguish among the 6 host ages. In contrast, when foraging for P. brassicae and P. napi, C. rubecula females more readily attacked early first instar. Cotesia glomerata showed a higher degree of behavioural plasticity towards acceptance of Pieris host species and host age than did C. rubecula. Cotesia glomerata females parasitized the three Pieris species and showed higher acceptance of first and second instars over third instar. Oviposition success was also influenced by host defensive behaviour. The frequency and the effectiveness of defensive behaviour rose with increasing age of the host, P. brassicae being the most aggressive Pieris species. Furthermore, the mean duration of C. glomerata oviposition was significantly reduced by the defensive reactions of P. brassicae, which would likely affect parasitoid fitness as oviposition time is positively correlated to clutch size in C. glomerata. Acceptance frequencies corresponded well to field reports of Pieris-Cotesia associations and to patterns of parasitoid larval performance, suggesting that the acceptance phase might be used as a reliable indicator of Cotesia host-specificity.     

The use of visual cues in host evaluation by aphidiid wasps I. Comparison between threeAphidius parasitoids of the pea aphid

Host evaluation behaviour was examined in three species of aphid parasitoids,Aphidius ervi haliday,A. pisivorus Smith, andA. smithi Sharma & Subba Rao (Hymenoptera: Aphidiidae). Parasitoids were provided under laboratory conditions with three kinds of hosts representing two aphid species: (green) pea aphid,Acyrthosiphon pisum (Harris), and green and pink colour morphs of the alfalfa aphid,Macrosiphum creelii Davis. Females of all threeAphidius species distinguished between aphids on the basis of colour, movement, and host species. Patterns of host acceptance by parasitoids were species-specific. InA. ervi, host preference was the same in light and dark conditions: pea aphid>green alfalfa aphid≫pink alfalfa aphid. In contrast,A. pisivorus attacked and accepted pea aphid and green alfalfa aphid equally in the light and preferred both of these over pink alfalfa aphid; however, it made no distinction between pea aphid and pink alfalfa aphid in the dark. Females ofA. smithi attacked all three kinds of hosts (pea aphid>green alfalfa aphid≫pink alfalfa aphid) but apparently laid eggs only in pea aphid. The frequencies of attack and oviposition by all wasps were higher on ‘normal’ pea aphids than on those anaesthetized with CO₂. Host recognition is confirmed by chemical cues in the aphid cuticle that are detected during antennation, and host acceptance is dependent on an assessment of host quality during ovipositor probing.     

The role of experience in plant foraging by the aphid parasitoidDiaeretiella rapae (Hymenoptera: Aphidiidae)

Experiments were conducted to test the hypothesis that plant learning by a relative plant-specialist parasitoid wasp should influence the probability of orienting to plant odors (plant finding) and the duration of searching on a plant after landing (plant examining). The insect tested was Diaeretiella rapaeM'Intosh (Hymenoptera: Aphidiidae), a parasitoid wasp that usually attacks aphids on cruciferous plants, but occasionally on other plants. Laboratory experiments using collard as the cruciferous plant and potato as the novel plant demonstrated that postemergence (adult) plant experience affected plant examining only on the less preferred plant, potato, and was reversible and relatively long-term (that is, lasted >2 days). Postemergence experience with potato did not increase orientation to potato odor in a wind tunnel, but postemergence experience with collard resulted in a trend of increased likelihood of flying to collard odor. Preemergence treatments affected plant finding but not plant examining.     

Kairomonal effect of an aphid cornicle secretion onLysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae).

In laboratory bioassays, whole-body homogenates and fresh cornicle wax of Rhopalosiphum padi(L.) (the bird-cherry oat aphid) elicited antennal examination and attack behavior in naive females of the polyphagous aphidiid parasitoid, Lysiphlebus testaceipes (Cresson). No such response was elicited by either homogenates or cornicle wax of Aphis nerii(Boyer de Fonscolombe) (another known host of the parasitoid) or by preparations of the aphid alarm pheromone, (E)--farnesene. The response to R. padiproducts was independent of rearing host and appears to be innate. Application of R. padicornicle wax to the dorsum of a nonhost aphid [Acythosiphum pisum(Harris)] increased the frequency with which this species was attacked by L. testaceipes.There was a tendency for the kairomonal activity of the cornicle secretion to decline as the wax dried, although parasitoid attack behavior was still elicited by wax which had been allowed to dry for up to 30 min before testing.     

Learning of host microhabitat form byExeristes roborator (F.) (Hymenoptera: Ichneumonidae)

Females of the polyphagous, ichneumonid ectoparasitoid, Exeristes roborator(F.), learned the form of artificial host microhabitats in the laboratory. Females given hosts only in a microhabitat of one form subsequently concentrated their responses on this microhabitat when given a choice between it and a microhabitat of another form, neither of which contained hosts. Control females did not display similar preferences. The parasitoid did not appear to distinguish the form of a microhabitat until after it contacted it. When hosts were present in test microhabitats, learning of form was apparently overridden, possibly because the parasitoids detected the presence of hosts before they assessed form or because their responses were shaped by learning of host-related factors. Together with learning of other microhabitat characteristics, learning of form may contribute to recognition of plant structures that are likely to contain suitable hosts by E. roborator.     

Influence of adult experience on host microhabitat location by the generalist parasitoid,Campoletis sonorensis (Hymenoptera: Ichneumonidae)

The effect of adult experience on microhabitat location behavior of the generalist parasitoid Campoletis sonorensis (Cameron)was examined in a wind tunnel bioassay. Responses were tested to the odors of two host plants (cotton and sesame) of Heliothis virescens (F.) or a nonhost plant (potato), either damaged and infested with host larvae and host products (host/plant complex) or intact, clean and uninfested. Parasitoid females remained naive or were allowed one oviposition experience on either of the plants, 1 min, 2 h, or 24 h prior their introduction into the wind tunnel. In a no-choice test, parasitoids experienced 1 min prior to bioassay completed significantly more flights to sesame and potato host/plant complexes than did naive parasitoids. However, 24 h after experience, only females experienced on potato completed more flights to the host/ plant complex than did naive females. Parasitoids experienced 1 min prior to flight to undamaged plants showed a slight increase in flight response (significant only for potato) but, after 24 h, completed only as many flights as naive parasitoids. In a dual-choice situation, parasitoids did not show a preference for either of the two host plants but did prefer a host to a nonhost plant. This innate plant preference was not changed by a single oviposition experience. The potential significance of these results to the microhabitat location behavior of C. sonorensisin the field is discussed.     

Influence of host behavior and host size on the success of oviposition ofCotesia urabae andDolichogenidea eucalypti (Hymenoptera: Braconidae)

Behavioral interactions among Cotesia urabaeAustin and Allen, Dolichogenidea eucalyptiAustin and Allen (Hymenoptera: Braconidae), and their host Uraba lugensWalker, the gum leaf skeletonizer (Lepidoptera: Noctuidae), were observed at three host sizes over a 20-min period. These sizes were first instar (small, gregarious), fourth-fifth instar (mid, gregarious), sixth-seventh instar (large, solitary) larvae. Unlike C. urabae, D. eucalyptiused its legs to hold small larvae before ovipositor insertion. D. eucalyptialso visited patches of small larvae more frequently, proceeded less often through patches of mid larvae, and made significantly fewer ovipositions in mid and large larvae. Small larvae responded to both parasitoids by dispersing outward, while mid larvae responded to parasitoids by moving inward to form a denser group. Larvae reared or thrashed after each parasitoid visit, especially mid larvae, and some continued to do so for up to 2h after parasitoid departure. Mid and large larvae occasionally injured parasitoids by biting their appendages. By rearing or thrashing immediately prior to an encounter with a parasitoid, mid and large larvae decreased the likelihood of being parasitized by up to 50%.     

Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae)

Abstract. 1. A study of searching behaviour on wheat and host preference of Aphidius rhopalosiphi (DeStefani-Perez) is described.
2. Parasitoids divided their time equally between the leaves but spent very little time on the ear.
3. After contact with honeydew or an aphid host, parasitoids were arrested in a particular area and increased the time spent searching.
4. Aphids feeding on the ear were parasitized less successfully, since their position between the grains protected them from parasitoid attacks.
5. A.rhopalosiphi exhibited no preference for Metopolophium dirhodum (Walker) or Sitobion avenae (Fabricius), although the handling time for the latter was significantly longer; this resulted in fewer S.avenae being parasitized when it was abundant. Parasitoids did not switch between hosts in these experiments.
6. As a result of its searching behaviour, A.rhopalosiphi will encounter and parasitize M.dirhodum feeding on the leaves more frequently than S.avenae, which feeds on the ear. This will limit the parasitoid's ability to regulate populations of the cereal aphid S. avenae.     

Factors governing host discrimination byOpius dimidiatus (Ashmead) (Hymenoptera: Braconidae)

The detection of, and response to, parasitized hosts by female parasitoids can involve a number of complex phenomena, including the ability of females to discriminate between unparasitized and parasitized hosts, the physiological state of females, and the nature and longevity of the cues they are detecting. The discriminatory ability of Opius dimidiatus,a solitary endoparasitoid of Liriomyza trifoliiwas examined. Experiments showed, first, that when presented with a choice of unparasitized hosts and hosts which they had previously parasitized, O. dimidiatusfemales could discriminate between them, both upon encounter (before probing) and after probing with the ovipositor. It was further demonstrated that the detection of parasitized hosts was time dependent: females could discriminate on the basis of antennal examination for up to 2.5 h after the first egg was laid. Postprobing discrimination lasted for up to 3.5 h. Some of the causal and evolutionary factors resulting in superparasitism are discussed.     

Effects of early adult experience on host selection in insects: Some experimental and theoretical results

A field experiment with Drosophila melanogasterrevealed that when flies encounter a particular food type soon after emergence, the probability of their subsequently being attracted to such a resource is increased. In this experiment, the length of time flies experienced their postemergence environments was under the control of the flies themselves. The experiment thus realistically mimicked one form of experiential effect that may be important in nature. A theoretical model is developed which shows that enhanced adult preferences for the types of resources fed on as larvae can substantially increase the degree of host-based genetic subdivision within a polyphagous population.     

Influence of physiological state and experience on the responsiveness ofLysiphlebus testaceipes (Cresson) (hymenoptera: aphidiidae) to aphid honeydew and to host plants

The effect of physiological state (hunger) and experience on the responsiveness of the aphid parasitoid, Lysiphlebus testaceipes(Cresson), to clean and honeydew-contaminated host plants was investigated in laboratory bioassays. Both fed and unfed parasitoids spent significantly longer examining honeydew-contaminated plants compared to uncontaminated controls, but the presence of honeydew did not influence attack latency (i.e., the speed with which naive parasitoids found and attacked hosts). Hunger, however, had a significant negative effect on attack latency, presumably as a result of a physiologically based shift from host- to food-location behavior in starved parasitoids. The parasitoid 's response to clean plants was significantly increased as a result of classical conditioning procedures, whereas the response to honeydew-contaminated plants was not.     

Uncoupling physical and chemical cues: The independent roles of scale cover size and kairomone concentration on host selection byAphytis melinus DeBach (Hymenoptera: Aphelinidae)

The ectoparasitoidAphytis melinus initially selects its host, California red scale,Aonidiella aurantii (Maskell) (Homoptera: Diaspididae), using characteristics of the host’s cover before assessing the quality of the scale body beneath. Host suitability is known to increase with host size until the scale insect reaches maturity, after which it is no longer available for parasitism. The wasp uses a combination of scale cover size and a kairomone,O-caffeoyltyrosine, in the cover for initial assessment. Under natural conditions these two factors are frequently coupled. We quantified the relative importance of cover size and kairomone concentration independently by removing and selectively reapplying controlled doses of syntheticO-caffeoyltyrosine to scale covers of known size. In the absence of the kairomone, wasps did not discriminate among scale covers differing in size. Wasps showed a curvilinear response to kairomone dose for each scale cover age group. Wasps preferred low doses ofO-caffeoyltyrosine on young, small scale covers, and high doses on old, large scale covers. The ability of wasps to respond quantitatively to the kairomone may be used in the field to differentiate small second-instar from larger and more suitable third-instar scale insect larvae.     

Olfactory host location and learning in the granary weevil parasitoidLariophagus distinguendus (Hymenoptera: Pteromalidae)

The sources of volatiles that attract the parasitoid Lariophagus distinguendus(Först.) to its hosts, the larvae of the granary weevil Sitophilus granarius(L.) infesting grains of Triticum aestivumL., were investigated in bioassays. The influence of oviposition experience on the responsiveness of the parasitoids to the sources of volatiles was considered. The potential sources of attractants are the host larvae, their feces, and the grain infested by the host. Weevil larvae were not attractive. Feces were attractive to females without and females with oviposition experience. Infested grains from which the larvae and feces were removed were slightly attractive to inexperienced, but very attractive to experienced females. Healthy and artificially damaged grains were attractive to experienced parasitoids only. Refering to the “variable response model,” we discuss the effect of experience on the response of the parasitoids to the several stimuli. Stimuli from different trophic levels are used by the foraging parasitoids: feces of the host larvae is an important source of attractants, but also the grains, particularly after experience.     

Effects of pre-adult and adult experience on host acceptance in choice and non-choice tests in two strains ofTrichogramma

The effect of adult learning through an oviposition experience, and pre-adult learning through development inside a host was investigated in two strains of an Australian egg parasitoid,Trichogramma nrivelae (Hymenoptera: Trichogrammatidae). Host response was measured in two types of laboratory preference tests. In single host tests, females reared on three lepidopteran hosts (Heliothis punctigera (Noctuidae),Papilio aegeus (Papilionidae), andHypolimnas bolina (Nymphalinae)) were presented host eggs individually, and allowed two ovipositions. Pre-adult experience affected host preference in only one strain, while acceptance of a host was increased in both strains when they had previously oviposited in this host species. An oviposition experience had a stronger effect on host preference than pre-adult experience. In choice tests, pairwise combinations of hosts were arranged in an alternating grid. The ratio of host acceptances to host contacts was computed for the whole test and up to the first oviposition. These indicated that effects of rearing host were weak or absent, but the host chosen initially had a strong effect on host preference. Relative size of the hosts had a strong effect on choice of the first host. The implications of learning inTrichogramma are discussed in relation to host preference testing procedures and the selection of candidate strains for mass rearing and inundative release.     

Resource utilization and sex allocation in response to host size in two ectoparasitoid wasps on subcortical beetles

Patterns of host resource utilization and sex ratio manipulation in relation to host size were investigated for two solitary ectoparasitoid wasps,Atanycolus initiator andSpathius brevicaudis (Hymenoptera Braconidae). Both species parasitize subcortical beetles on the trunks of Japanese pine trees.A. initiator is on average 8 times larger in body weight and has an ovipositor that is 3.7 times longer than that ofS. brevicaudis. In both parasitoids, the size of emerging wasps was positively correlated with host size, but the host/wasp size regressions were linear for all three major host species inA. initiator, whereas inS. brevicaudis the regression was logarithmic for a relatively large host species. The sex ratios (proportion of males) of both parasitoids emerging from different host species decreased with increasing host size, but the overall sex ratio on each host species was male-biased inA. initiator, while female-biased inS. brevicaudis. How the proportion of host consumed changed in response to host size, differed between the two parasitoids for the same host species. In the field survey, the size and sex ratio of the emerging two parasitoids from a dead tree were closely related to host size. However, the spatial distribution of the two parasitoids depended on the bark thickness of the trunk. The data suggest that differences in the relative evaluation of host size and in ovipositor length may enable the coexistence of the two parasitoid wasps.     

Host recognition byPimpla instigator F. (Hymenoptera: Ichneumonidae): Preferences and learned responses

This study identifies some previously unreported tactile and visual cues used by the pupal parasitoid Pimpla instigatorF. (Ichneumonidae) to recognize potential hosts. Paper cylinders were presented to the wasps as simple models of lepidopteran pupae. Acceptance of these models was evaluated by determining the frequency with which the wasps punctured the cylinders with their ovipositors. The length of the cylinders did not influence acceptance of the models; however, both surface texture and structural modifications to the ends of the cylinder did affect the frequency of punctures. Smooth cylinders were punctured more often than roughened cylinders, and cylinders with closed ends were frequently punctured, whereas open-ended cylinders were consistently rejected. The wasps also discriminated between blue and yellow cylinders and could be trained to associate blue or yellow with the presence of hosts. Preferences were established during a single 90- min training period and persisted for at least 4 days following training.     

Recognition of heterospecific parasitism: Competition between Aphidiid (Aphidius ervi) and Aphelinid (Aphelinus asychis) parasitoids of Aphids (Hymenoptera: Aphidiidae; Aphelinidae)

The solitary parasitoids Aphidius erviHaliday (Hymenoptera: Aphidiidae) and Aphelinus asychisWalker (Hymenoptera: Aphelinidae) attacked but generally did not oviposit in pea aphids parasitized by the other species. Wasps selectively oviposited in unparasitized hosts when given a choice. Host discrimination depended on the recognition of internal cues. Females of A. asychiseither could not recognize or ignored A. ervi'sexternal host marking pheromone. Under most conditions, A. ervisurvived in superparasitized hosts, killing competing A. asychislarvae by physical attack and possibly physiological suppression. The outcome of larval competition was not affected by oviposition sequence or age difference between larvae; A. asychissurvived only when it had substantially completed larval development before the host was superparasitized by A. ervi.It is suggested that competition for host resources incurs a cost, for the winner in terms of reduced size or increased development time and for the loser in terms of lost progeny and searching time. Consequently, heterospecific host discrimination can be functional. Internal, and probably general, cues enable wasps to recognize and avoid oviposition in hosts already parasitized by an unrelated species.