Short Distance Cues Used by the Adult Parasitoid <Emphasis Type="Italic">Microctonus hyperodae</Emphasis> Loan (Hymenoptera: Braconidae,Euphorinae) for Host Selection of a Novel Host <Emphasis Type="Italic">Listronotus oregonensis</Emphasis> (Coleoptera: Curculionidae)

Insect parasitoids use host kairomone to detect their hosts. However, in parasitoid species that attack adult hosts, the mobility of adult insect may mean that the host can move away for kairomone sources. The effect of Listronotus oregonensis LeConte (Coleoptera: Curculionidae) adult sex, feces and movement on host selection behavior by Microctonus’’ hyperodae Loan (Hymenoptera: Braconidae; Euphorinae) females was evaluated in the laboratory. We hypothesized that, in addition of using host kairomones, parasitoids of adult stage should use host movement for host selection. The sex of L. oregonensis did not affect the host selection behavior of M. hyperodae. However, host feces decreased the number of weevil antennations done by M. hyperodae. Microctonus hyperodae stopped less frequently near immobile L. oregonensis than near walking ones and these latter were frequently pursued by M. hyperodae. Host movement was the stimulus that elicited oviposition by M. hyperodae. The adaptive implications of these results are discussed.     

Host specificity testing and suitability of the parasitoidMicroctonus hyperodae (Hym.: Braconidae,Euphorinae) as a biological control agent ofListronotus bonariensis (Col.: Curculionidae) in New Zealand

The behaviour of the parasitoidMicroctonus hyperodae Loan was studied under quarantine conditions to determine its likely host range in New Zealand. The species was imported from South America as a potential biological control agent of Argentine stem weevil,Listronotus bonariensis (Kuschel). The study involved systematic evaluation of the parasitoid's behaviour when exposed to 24 non-host weevil species; all but three of these were native to New Zealand. Of those tested, four were found to sustain someM. hyperodae development. However, further examination showed that in all but one species,Irenimus aequalis (Broun), parasitoid development was impeded, with up to 50% of the larvae becoming encapsulated. Overall, those weevil species that were attacked produced only 19% of the parasitoids derived fromL. bonariensis controls. As an adjunct to this quarantine study, a review of the habitats of the native weevil and target pest populations indicated that refugia would probably exist for native alpine species. I. aequalis was not considered to be threatened byM. hyperodae as this weevil has benefited from the advent of European agricultural systems to the extent that it is now recognised as a minor pest. In view of its relatively oligophagous behaviour, the parasitoid was recommended as suitable for release.      

Effect of various pesticides on the non-target species Microctonus hyperodae, a biological control agent of Listronotus bonariensis

The parasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae) was introduced into New Zealand to control the weevil Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae), a major pest of graminaceous plants. Four experiments were conducted to investigate the effects of various pesticides that are commonly used in the pastoral environments of L. bonariensis and M. hyperodae. Topical applications of aqueous solutions prepared from commercial formulations of five herbicides were not toxic, but the surfactant Silwett L‐77 increased M. hyperodae mortality relative to the water‐treated controls. Laboratory assays showed that M. hyperodae adults were susceptible to chlorpyrifos residues on pasture foliage following application of the insecticide to field plots at ≥5 g a.i. ha^?1. Maintenance of L. bonariensis on ryegrass in the laboratory showed that treatment of the food plants with chlorpyrifos at ≥96 g a.i. ha^?1 reduced L. bonariensis survivorship and ultimately reduced M. hyperodae prepupal emergence from those hosts. Initially, mortalities of non‐parasitized L. bonariensis were significantly greater than for parasitized L. bonariensis. Maintenance of parasitized L. bonariensis on diflubenzuron‐treated ryegrass plants arrested M. hyperodae larval development in the host and ultimately reduced prepupal emergence of M. hyperodae from those hosts. Despite the arrested development of M. hyperodae, the mortality of L. bonariensis hosts was increased. Adult M. hyperodae successfully reared from hosts maintained on diflubenzuron (12.5 g a.i. ha^?1) treated food plants had reduced reproductive potential. The consequences of pasture management strategies that employ pesticides are discussed in relation to biocontrol of L. bonariensis by M. hyperodae.     

Evidence for parasitoid‐induced premature mortality in the Argentine stem weevil

The Argentine stem weevil Listronotus bonariensis Kuschel (Coleoptera: Curculionidae) is an exotic pest of New Zealand ryegrass and the adult‐stage is parasitized by the introduced solitary endoparasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae: Euphorinae). This biological control agent is effective, although, under both laboratory and field conditions, an unexplained source of premature mortality in the weevils is observed after exposure to M. hyperodae. This premature mortality may be affected to varying degrees by the length of time of parasitoid exposure, the physiological conditions of the host, and the host to parasitoid ratios, although it occurs naturally without any physical interruption to the parasitoid ovipositional process. In the present study, the premature mortality reported in earlier studies is confirmed and it is conjectured to be the result of injection of parasitoid venom without an egg. Moreover, the lack of premature mortality resulting from longer exposure periods indicates that there might be a curative effect resulting from subsequent oviposition; the egg reverses the toxic effect induced by the injection of venom only. As discussed, this phenomenon may not be restricted to the L. bonariensis/M. hyperodae system and, accordingly, there are evolutionary, biosecurity and general pest management questions to be considered.     

Influence of Clavicipitaceous Endophyte Infection in Ryegrass on Development of the ParasitoidMicroctonus hyperodaeLoan (Hymenoptera: Braconidae) inListronotus bonariensis(Kuschel) (Coleoptera: Curculionidae)

Laboratory experiments were conducted to examine the effect of ryegrass infection by the endophytic fungusAcremonium loliiLatch, Christensen and Samuels onMicroctonus hyperodaeLoan, a parasitoid ofListronotus bonariensis(Kuschel). Progression of parasitoids through the larval instar stages was shown to depend on adequate nutrition of the weevil host. Compared to confinement on endophyte-free ryegrass, parasitized weevils held on nonpreferred diets comprising leaf segments from endophyte-infected ryegrass and switchgrass contained parasitoid larvae with retarded development. Similarly, development of parasitoid larvae was retarded in hosts feeding on artificial diet containing diterpenes and alkaloids ofA. loliiorigin. Several diterpenes incorporated into the diet reduced survival of the parasitoid larvae. Attack rate of parasitoids was reduced when the quality of potential host weevils was compromised by confinement on nonpreferredA. lolii-infected ryegrass or without food for 14 days.     

Serratia marcescens as a rapid indicator of Microctonus hyperodae oviposition activity in Listronotus maculicollis and potential application of the technique to host-specificity testing

Listronotus maculicollis (Dietz) (Coleoptera: Curculionidae) is a potential novel host of the braconid parasitoid Microctonus hyperodae Loan, but initial studies have shown that levels of parasitism are lower than in the natural host L. bonariensis (Kuschel). A novel bacterial indicator test was used to determine whether the lower level of parasitism was due to behavioural factors, lack of oviposition, or host resistance. The incidence of ovipositor penetration by the parasitoid M. hyperodae into adult L. maculicollis was measured by immersing the ovipositor of the parasitoid in the facultative pathogen, Serratia marcescens Bizio. Adult weevils were then exposed to parasitoids for up to 72 h and rapid mortality used as an indicator of oviposition penetration. Survival was assessed after six days and surviving weevils were dissected and examined for parasitoid larvae. Mortality among L. maculicolis exposed to parasitoids treated with S. marcescens was significantly higher (P<0.001) than the controls but significantly lower (P<0.001) than in the natural host, L. bonariensis. Dissection of weevils exposed to uncontaminated parasitoids revealed that parasitism in L. maculicolis was significantly (P<0.001) less than parasitism in L. bonariensis. Serratia marcescens-induced mortality plus parasitism of surviving weevils in the parasitoid plus bacteria treatments produced a similar overall effect. Application of bacteria to the parasitoid ovipositor provided a rapid, simple test for ovipositor penetration, which shows potential for separation of behavioural and physiological defence mechanisms in parasitoid/host range studies.     

Contrasting host: parasitoid synchrony drives differing levels of biocontrol by two introduced Microctonus spp. in northern New Zealand pastures

Two species from the genus Microctonus Wesmael (Hymenoptera: Braconidae) have been introduced into New Zealand as biocontrol agents of pest weevils in pasture. Both parasitoids have similar life cycles and co-exist in pasture along with their respective weevil hosts. However, winter parasitism rates by M. hyperodae Loan are low in comparison to the Irish biotype of M. aethiopoides’ Loan. Population studies at two Waikato sites over three consecutive seasons of parasitoid activity showed that M. aethiopoides recovered from near extinction each spring and built up to effective levels by winter because hosts were available continuously throughout summer and autumn. In contrast, M. hyperodae began each season at higher larval populations and parasitism levels than M. aethiopoides, but populations and parasitism levels declined during late summer and early autumn due to low host availability. The contrast between species is consistent with the high levels of endophyte-conferred pest-resistant grass in the pastures, which impacts strongly on M. hyperodae’s host weevil abundance during summer but has no effect on M. aethiopoides’ host weevils which feed only on clovers. It was accentuated by a warming climate with the now regular occurrence of a third host generation after most M. hyperodae adult activity had ceased.

     

Consumption of carrot weevil,Listronotus oregonensis, [Coleoptera: Curculionidae] by four species of carabids on host plants in the laboratory

Four carabid species,Anisodactylus santaecrucis, Bembidion quadrimaculatum oppositum, Pterostichus lucublandus andPterostichus melanarius, abundant in carrot fields in southwestern Quebec, were tested for predation against the carrot weevil,Listronotus oregonensis, on host plants. The largest species,Pterostichus melanarius, consumed the greatest number of carrot weevil larvae and pupae.Bembidion quadrimaculatum oppositum did not prey on carrot weevil eggs laid on carrot leaves.      

An investigation into the reproductive characteristics ofMicroctonus hyperodae (Hym.: braconidae), a parasitoid ofListronotus bonariensis (Col.: Curculionidae)

The reproductive tract of the parasitoidMicroctonus hyperodae was found to comprise 6.1±0.2 ovarioles containing a total of 40–60 oöcytes. After oviposition into its hostListronotus bonariensis, the parasitoid's egg volume increased by 205 times prior to hatching. At 19.1°C ovipositingM. hyperodae survived for a mean 21±4 days and laid a mean of 48±8 eggs.M. hyperodae collected from Colonia, Uruguay laid a mean of 62±15 eggs which was significantly more than the other ecotypes. Under caging conditions with an ample supply of hosts,M. hyperodae laid 51% of its eggs in the first 72 hours and on average 41% of the species' life-span occurred after the exhaustion of its egg supply. Minimum temperature forM. hyperodae oviposition was found to be c. 5°C; beyond this the rate of increase in egg-laying was approximately linear until 30°C whereafter the rate fell abruptly. There was effectively no egg-laying at 39°C. The parasitoid showed no preference for one host sex or the other either in the laboratory or under field conditions. Compared to otherMicroctonus spp.,M. hyperodae appeared to show low fecundity and high longevity. The adaptive implications of this are discussed.     

Suitability of the maize weevil and angoumois grain moth as hosts for the parasitoidsAnisopteromalus calandrae andPteromalus cerealellae

Two parasitoids,Pteromalus cerealellae (Ashmead) andAnisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), were compared for their ability to parasitize two important internally-developing insect pests of stored maize (Zea mays L.). Parasitism byP. cerealellae was greater on Angoumois grain moth,Sitotroga cerealella (Olivier), than on maize weevil,Sitophilus zeamais Motschulsky, in no-choice experiments.Anisopteromalus calandrae parasitized more maize weevils than didP. cerealellae. The former parasitoid parasitized only a few Angoumois grain moths successfully in maize, but parasitized many in wheat if the hosts were younger than 3 weeks old. Thus, both host age and type of grain affect suitability for parasitism. The effects of parental host (species on which the female developed) and experimental host (species exposed to parasitism) on parasitism rate ofP. cerealellae were tested in a host-switching experiment. Parasitism by parasitoids reared on maize weevils was 23% lower than that of parasitoids reared on Angoumois grain moth. This effect was independent of which host the filial generation of parasitoids was tested on. However, the experimental host species had a much greater effect on parasitoid fecundity than the parental host species. Female progeny had smaller body sizes when emerging from maize weevil than from Angoumois grain moth, which may explain the parental host effect on fecundity. There was also a slight intergenerational effect of host species on parasitoid body size.     

Breakdown in classical biological control of Argentine stem weevil: a matter of time

Earlier study at a national scale has shown that insect pests in agriculture can develop resistance to natural enemies following ongoing expansion and simplification of agricultural systems. Here, we used 25 years of field-sampling data segmented into three distinct ecoregions in New Zealand to show that parasitism rate of a key pasture pest (Listronotus bonariensis, Argentine stem weevil) by the introduced parasitoid Microctonus hyperodae has significantly declined. However, this decline has not happened simultaneously in all three ecoregions but with a one year time-lag. The variation in parasitism rate trends might be attributed to subsets of the weevil populations that became resistant to their biocontrol agent once having been exposed to seven years selection pressure (ca. 14 generations) since the parasitoid releases. This result supports the hypothesis that adaptation leading to resistance might have similarly occurred in different parts of the country indicating that the genetic variation needed for the acquisition of resistance was equally present everywhere.     

Comparison of oviposition behavior of a solitary and a gregarious parasitoid (Hymenoptera: Mymaridae)

Anaphes victus Huber andAnaphes listronoti Huber (Hymenoptera: Mymaridae) are respectively solitary and gregarious egg parasitoids of the carrot weevil,Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae). We made detailed ethograms of the oviposition behavior on unparasitized and parasitized hosts for the two species. We then compared the behavior of virgin and mated females for the oviposition of male and female progenies. The two species did not always oviposit after insertion of the ovipositor, but these punctures without oviposition could be readily differentiated from oviposition.A. victus oviposited only once by puncture, whileA. listronoti deposited one to three eggs during the same sequence. The variability of the duration of the various components was generally lower for a given female than between females. Two components, the abdominal vibrations and the pause, were significantly shorter in ovipositions that resulted in male progency for the two species. However, an important overlap in duration prevents using these differences to sex the progeny at oviposition. Virgin females of both species, although capable of producing only males, exhibited both behaviors. Parasitized hosts were recognized through internal and external markings that were used in host discrimination.     

Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species

We measured the acceptance and suitability of four aphid species [Aphis gossypii Glover, Myzus persicae (Sulzer), Rhopalosiphum padi (L.), and Schizaphis graminum (Rondani)] (Homoptera: Aphididae) for the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Female parasitoids parasitized fewer R. padi than the other three aphid species, and fewer offspring successfully completed development in R. padi than in the other three host species. Sex ratios of emerging adults were more male‐biased from R. padi than from the other three aphid species, suggesting that R. padi is a poor quality host for this population of A. colemani. Ovipositing A. colemani encountered R. padi at a slower rate, spent more time handling R. padi, and parasitoid offspring died at a higher rate in R. padi compared to A. gossypii. Our results show that oviposition behavior and offspring performance are correlated. In each experiment, we tested the effect of the host species in which the parasitoids developed (parental host) on the number of hosts attacked, the proportion of each host species accepted for oviposition and the survival of progeny. Parental host affected maternal body size and, through its effect on body size, the rate of encounter with hosts. Other than this, parental host species did not affect parasitism.     

Sex Allocation by a Parasitoid Wasp (Hymenoptera: Ichneumonidae) to Different Host Species: A Question for the Mechanism of Host Size Estimation

Sex allocation by the polyphagous solitary pupal parasitoid wasp Pimpla luctuosa Smith to a small host species, Galleria mellonella (L.), and a large host species, Mamestra brassicae L., was investigated to test whether female wasps responded to hosts of different sizes across different host species. In the experiments, both host species were presented to each test female wasp. Primary and secondary sex ratio experiments revealed that female wasps laid more female eggs in larger pupae of each host species, indicating that female wasps recognized size differences within host species. The wasp sex ratio (male ratio) from M. brassicae, however, was much higher than that expected on the basis of the sex ratio curve from different-sized G. mellonella. Larger hosts of each host species yielded larger wasps, indicating that the host size estimation by female wasps across different host species was incomplete or was not simple. These results suggested that P. luctuosa evaluated host size not only by physical measures such as dimension but also by other unknown measures. A possible explanation for the adaptiveness of different sex ratio responses by Pimpla luctuosa to different host species was discussed.     

Intra- and interspecific host discrimination in two closely related egg parasitoids

Intraspecific host discrimination is frequently found in solitary parasitoids, but interspecific host discrimination, where female parasitoids recognize hosts already parasitized by females of other species, is rare. This particular behaviour appears to be adaptive only under specific circumstances. In this paper, we quantified intraspecific host discrimination in Anaphes n. sp. (Hymenoptera: Mymaridae), an endoparasitoid of the eggs of Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) and interspecific host discrimination toward eggs parasitized by Anaphes sordidatus (Girault), a sympatric species competing for the same resource in similar habitats. To examine host discrimination, choice experiments were used where the females had to choose between different categories of eggs (unparasitized, parasitized by Anaphes n. sp. or A. sordidatus). Superparasitism and multiparasitism were avoided in experiments where the female had a choice between unparasitized hosts and hosts parasitized by the same female, by a conspecific or by a female A. sordidatus. When all hosts available were parasitized, conspecific superparasitism occurred more often than self-superparasitism or multiparasitism. These results indicated that females Anaphes n. sp. were capable of self-, conspecific and interspecific discrimination. Self-discrimination followed recognition of an external marking while interspecific discrimination occurred mostly after insertion of the ovipositor. Interspecific discrimination could result from the recent speciation of these species and could be associated with a genotypic discrimination. This behavior appears to be adaptive because of the competition for common hosts between the two parasitoid species.     

No-choice host range tests for Allotropa sp. near mecrida,a parasitoid of the pink hibiscus mealybug,Maconellicoccus hirsutus (Hemiptera: Pseudococcidae)

Host range studies of the parasitoid Allotropa sp. near mecrida (Walker) (Hymenoptera: Platygastridae) were conducted prior to applying for a permit to release it against the pink hibiscus mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), in southern California. Using M. hirsutus as a control, four mealybug species were tested as potential hosts. Allotropa sp. near mecrida did not successfully reproduce in any of the mealybug species tested, except for the target species, M. hirsutus. The parasitoid was found to host feed upon one of the non-target species within the confined test environment. Subsequently a USDA-APHIS importation and release permit was granted.     

Response to host age of the egg parasitoid Anaphes n.sp. (Hymenoptera: Mymaridae)

The mymarid Anaphes n.sp. was observed to parasitize the eggs of the carrot weevil Listronotus oregonensis (LeConte) up to 138 h old at 23±1°C and 18L:6D. Adult emergence of the parasitoid was observed in 85%‐97.5% of the weevil eggs 42–138 h old and host embryogenesis was interrupted in nearly 100% of these eggs. In host eggs of 18 h old, parasitism was very high but not all parasitoids completed their development and their subsequent emergence was generally retarded. An.sp. could parasitize host eggs 162 h old, but such an attack rarely retarded the normal development of the host. The parasitoid was unable to complete its development in sterile carrot weevil eggs.     

Effect of container type on suitability of the pathogen Serratia marcescens - Microctonus hyperodae (Hym., Braconidae) association to indicate parasitoid oviposition attempts

To minimize the risk that introduced entomophagous biological control agents may pose to native and beneficial insect species, identification of likely nontarget hosts is required before release is considered. A novel technique, in which the parasitoid acts as a vector of a bacterium pathogenic to potential hosts, has been used as an indicator of parasitoid ovipositional activity even when subsequent development of the parasitoid egg within the 'host' does not occur. In this study the application of this technique was examined in relation to container type using the facultative bacterium Serratia marcescens in association with the parasitoid Microctonus hyperodae. Two permissive host weevil species, Listronotus bonariensis and Irenimus aequalis , were exposed for 72 h to M. hyperodae treated with either distilled water or S. marcescens suspension in either Petri dishes or cages. Weevil septicaemia was significantly higher when exposed to S. marcescens -treated parasitoids than water-treated parasitoids (P < 0.001), with no difference in mortality between weevil species. Septicaemia was significantly higher in the Petri dishes than in cages (P < 0.001). This was attributed to improved survival of S. marcescens in the Petri dishes compared with cages. Total parasitoid activity (combined septicaemia and parasitism) for I. aequalis was higher in Petri dishes than in cages and far exceeded field parasitism. Petri dishes provide an environment for constant interaction between parasitoid and target host and thereby provide a conservative indication of parasitoid host range. However, cages may be more suitable to conduct host range studies because the ability to manipulate the environment. Potential refinements to the parasitoid-bacteria technique include methodology that enhances viability of the bacterium under cage conditions.     

Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi

The reproductive success of female parasitoids is dependent on their ability to accurately assess the suitability of a host for larval development. For generalist parasitoids, which utilize a broad range of species and instars as hosts, a set of assessment criteria determines whether a host is accepted or rejected. The suitability of a host, however, can only be imperfectly assessed by the female parasitoid, which can result in the selection of lesser quality hosts for oviposition. In this study we explored the disparity between host quality and host preference using the generalist koinobiotic parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) and the host Aulacorthum solani (Harris) (Homoptera: Aphididae), the foxglove aphid. The second instar hosts produced the highest level of reproductive success, while third and fourth instars resulted in a substantially reduced reproductive performance. When given a choice of host instars, parasitoids preferred the older hosts for oviposition disregarding their reduced suitability for larval development. Results are discussed in context of mechanisms involved in A. ervi host selection and biases in the criteria used to assess hosts that may arise when parasitoids transfer host species between generations.     

Systematic mass rearing and release ofMicroctonus hyperodae (Hym.: Braconidae,Euphorinae), a parasitoid of the argentine stem weevilListronotus bonariensis (Col.: Curculionidae) and records of its establishment in New Zealand

The method whereby equal numbers of seven ecotypes of the parasitoidMicroctonus hyperodae Loan (Hymenoptera: Braconidae, Euphorinae) were reared and released is described along with the reasons for doing so. This was achieved by variably intense rearing effort depending on the number of founder females in that particular ecotype. The parasitoid was released in three regions of New Zealand as a control agent of theListronotus bonariensis Kuschel (Col.: Curculionidae), a severe pest of New Zealand pastures. It was later recovered from all three regions.