The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens (Hymenoptera: Ichneumonidae)

Abstract.

• 1 The effects of superparasitism on the rate of development, adult size and mortality of Venturia canescens (Hymenoptera: Ichneumonidae) were investigated. Parasitoids were reared from third (L3) and fifth (L5) instars of one of its hosts, Plodia interpunctella (Lepidoptera: Pyralidae) containing one, two or four parasitoid eggs.
• 2 Superparasitism increased the development time of Venturia reared from both instars, but the developmental delay was more evident in wasps from L5 hosts.
• 3 The size of parasitoids from L3 hosts was unaffected by egg number, but wasps from both superparasitized L5 treatments were significantly smaller than those from singly parasitized hosts.
• 4 Parasitoid mortality was significantly higher in L5 than L3, but within instars did not differ significantly with egg number.
• 5 The results confirm that superparasitism may affect the fitness of both the adult female wasp and her progeny, and should therefore be incorporated into models of superparasitism as an adaptive foraging strategy.

     

Life tables of Venturia canescens (Hymenoptera: Ichneumonidae) parasitizing the Mediterranean flour moth (Lepidoptera: Pyralidae)

Effects of temperature, adult feeding, and host instar on life table parameters of Venturia canescens Gravenhorst (Hymenoptera: Ichneumonidae) parasitizing larvae of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) were studied in the laboratory. Experimental adults lived under various regimes of temperature (15, 20, 25, and 30 degrees C), food supply (with or without access to honey), and host instar (second, third, fourth, and fifth). Temperature increase resulted in higher values of the intrinsic rate of natural increase (r(m)), the net reproductive rate (R(o)), the finite capacity of increase (lambda), and the gross reproductive rate (GRR), whereas it was followed by decrease of the mean generation time (G) and the doubling time (DT) values. Feeding on honey caused remarkable increase of r(m), R(o), and GRR, whereas r(m) and lambda reached their maximum when full-grown hosts (fifth instar) were parasitized. This is the first time life table parameters of V. canescens have been studied. The findings of the current study are discussed on the basis of improving V. canescens performance as a biological agent against moth pests of stored products.     

On the adult longevity of the entomophagous parasite,Venturia canescens [Hymenoptera: Ichneumonidae]

The adult longevity of the California strain ofVenturia canescens (Gravenhorst) [Hymenoptera: Ichneumonidae], a larval parasite of the Mediterranean flour moth,Anagasta kuehniella (Zeller) [Lepidoptera: Phycitidae] was studied. The effects of the presence or absence of food (honey streak) in relationship to the ovipositional exertion as influenced by the presence or absence of hosts was considered. It was found that in the absence of any food, their longevity was drastically reduced and ovipositional exertion had no effect on this curtailment. However, in the presence of food, ovipositional activity was a major factor in the curtailment of adult longevity.     

Effects of lipophorin and 20-hydroxyecdysone on in vitro development of the larval endoparasitoid Venturia canescens (Hymenoptera: Ichneumonidae)

We previously reported that development of the embryos of the larval endoparasitoid Venturia canescens proceeded in the insect cell culture medium, MGM-450, and was promoted by the addition of a pupal extract from their host Galleria mellonella. The developmental promotion also was obtained by supplementing an equal amount of chicken egg yolk instead of the pupal extract to the medium. In this case, approximately 30% of the embryos developed into the second instar, but the value increased to more than 90% by treatment with 20-hydroxyecdysone. The medium supplemented with a G. mellonella pupal extract obtained by using Carlson's solution displayed growth-promoting ability, and in the extract, apolipophorin I was electrophoretically detected in large amounts. Both lipophorin purified from G. mellonella pupae and low density lipoprotein from chicken egg yolk acted as a growth-promoting substance for parasitoid development, although fetal bovine serum and 20-hydroxyecdysone were required as supplements to the medium for the expression of the ability. This indicated that lipophorin or lipophorin-transported lipids could act as a substance closely related to the growth-promoting factor(s) putatively involved in the host extract.     

Conspecific Avoidance During Foraging in Venturia canescens (Hymenoptera: Ichneumonidae): The Roles of Host Presence and Conspecific Densities

We explored the effects of the presence of conspecifics on host patch choice decisions made by the parasitoid Venturia canescens. Different odor sources were located in plastic boxes at the end of each arm of a glass Y-tube olfactometer. In a set of experiments, odor sources were either (a) host kairomone patches with or without conspecifics (5 or 20) or (b) two odor sources located in successive boxes (a host kairomone patch and a patch with 20 conspecifics in one arm versus a host patch and an empty patch in the other). Our results indicate that V. canescens avoids competition only at high conspecific densities. Avoidance occurs only when foraging wasps perceive the combined odors from host kairomones and conspecific females. Separating the host patch from conspecific parasitoids does not perturb avoidance behavior.     

Host behaviour and its influence on foraging and acceptance by the solitary parasitoid wasp,Venturia canescens (Hym: Ichneumonidae)

Behavioural interactions between the solitary koinobiont parasitoid,Venturia canescens, and two of its hosts,Plodia interpunctella andCorcyra cephalonica, were investigated. The response of both hosts to simulated antennation using a two-haired brush was examined over instars 3 (L3) to 5 (L5). YoungP. interpunctella larvae predominantly adopted escape tactics (writhe, trash) whereas L5P. interpunctella usually froze after the stimulus was applied. L3C. cephalonica larvae were more aggressive (headrear, flick) thanP. interpunctella in response to the application of the stimulus, but olderC. cephalonica responded less aggressively than in earlier instars. AlthoughV. canescens readily jabbed its ovipositor at both hosts after antennation,P. interpunctella was considerably more susceptible to parasitoid attack thanC. cephalonica, irrespective of size in the final (L5) instar.C. cephalonica, the larger, more aggressive host, actively resisted parasitism whereasP. interpunctella responded much more passively after parasitoid contact. Parasitoids examined and jabbed their ovipositors at dead hosts, but this behaviour was not sustained, implying that host movement stimulates parasitoid attack. On patches containingV. canescens, L5C. cephalonica andP. interpunctella, mostP. interpunctella larvae responded by freezing after parasitoid contact.P. interpunctella that froze usually avoided parasitism, whereas larvae that attempted to escape by crawling were pursued with vigour byV. canescens and usually parasitized. Irrespective of behaviour after parasitoid contact,C. cephalonia displayed more aggressive behaviour and had much greater success in warding off parasitoid attack. Host acceptance byV. canescens is clearly affected by the size and species of the host it attacks. The influence of host defensive behaviour is discussed in relation to the evolution of parasitoid counter-defences and oviposition strategies.     

Presence of a novel small RNA-containing virus in a laboratory culture of the endoparasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae)

Parasitoid wasps use a variety of mechanisms to alter their host's physiology to the benefit of the developing endoparasite inside the host larva. Association of certain wasps with viruses and virus-like particles (VLPs) that contribute to their success in parasitism is one of the fascinating evolutionary adaptations conferring active or passive protection for the endoparasite from the host immune system. Venturia canescens has been shown to produce VLPs that provide protection for the developing parasitoid egg inside the host, Ephestia kuehniella. Here, we report on the presence of a novel small RNA-containing virus from V. canescens, designated as VcSRV, occurring in the ovaries of the wasp. The virus particles are found together with VcVLPs in the lumen of the calyx region of the ovaries and are injected together with the egg and VcVLPs into E. kuehniella larvae where they enter hemocytes. Alignment of the RNA-dependent RNA polymerase gene of VcSRV indicates that the virus most likely belongs to the recently described genus Iflavirus.     

Geographical distribution and genetic relatedness of sympatrical thelytokous and arrhenotokous populations of the parasitoid Venturia canescens (Hymenoptera)

Theory predicts that asexual reproduction has a competitive advantage over sexual reproduction because of the twofold cost of producing males. Few systems are suitable for directly testing this prediction. In the solitary parasitoid wasp Venturia canescens both arrhenotokously (sexual) and thelytokously (asexual) reproducing individuals occur sympatrically. We sampled 922 wasps from 22 localities along the coast of south‐eastern France. Thelytokous wasps were less abundant (23%) than arrhenotokous wasps and were almost always found in sympatry with arrhenotokous ones. An analysis of genetic relatedness using amplified fragment length polymorphism (AFLP) markers showed the existence of a widespread thelytokous clone. In addition, a few thelytokous individuals were found to be closely related to arrhenotokous ones and vice versa. These data suggest the occurrence of occasional gene flow between both reproductive modes and/or recurrent origin of thelytokous clones from coexisting arrhenotokous populations in the area. The results are discussed in the context of the paradox of sex.     

The influence of the rearing host on the response of the parasitoid Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) to odours from Ephestia kuehniella and Plodia interpunctella in a Y-tube olfactometer

Venturia canescens (Gravenhorst) is an ichneumonid generalist parasitoid that successfully attacks the larvae of different lepidopteran pests that infest stored products. These pest species include Plodia interpunctella and Ephestia kuehniella. In this study, we aimed to evaluate the influence of the rearing host on the parasitoid’s ability to detect and respond to a new host different from the rearing species. For this reason, the trials tested the preference of parasitoids reared on P. interpunctella or E. kuehniella for products that were or were not infested with larvae of these hosts. The trials were conducted in a Y-tube olfactometer. Regardless of the rearing host species, the parasitoids showed no preference for uninfested products. The parasitoids were attracted to products infested with larvae of their rearing host in preference to uninfested products. They also showed preferential attraction to products infested with the new host over uninfested products. E. kuehniella was the preferred host, irrespectively of the parasitoid host rearing species. The results are discussed to develop a better understanding of the ecology of V. canescens for its application in biological control.     

Growth-promoting effects of ecdysteroids and juvenile hormone on in vitro development of the larval endoparasitoid,Venturia canescens (Hymenoptera: Ichneumonidae)

We previously reported that lipophorin, fetal bovine serum (FBS), and 20-hydroxyecdysone (20-HE) are essential for the development of the larval endoparasitoid Venturia canescens larvae in vitro. The present study was undertaken to determine the optimal concentrations of those three substances in the MGM-450 medium, and to examine the hormonal effects of ecdysteroids and juvenile hormone (JH) on the development of the parasitoid larvae in vitro. When the culture was started with embryos at the post-germband stage, concentrations of 3 mg/ml of lipophorin and 20% of FBS were most suitable for the development of the parasitoid. The growth-promoting effect of 20-HE increased in a concentration-dependent manner and peaked at a concentration of 1 &mgr;g/ml. Excess concentration led to malformations of the larvae. Three other ecdysteroids, ecdysone, 2-deoxy-20-hydroxyecdysone, and polypodine B had the same effect, although their activity was lower than that of 20-HE. Cholesterol had no effect; most larvae failed to develop. When the medium was supplemented with JH, the duration of the developmental period was significantly shortened, but this hormone was not found to be essential.     

Genetic variability of arrhenotokous and thelytokous Venturia canescens (Hymenoptera)

The ichneumonid wasp Venturia canescens (Hymenoptera) has been studied extensively for foraging behaviour and population dynamics of sexually (arrhenotokous) and parthenogenetically (thelytokous) reproducing individuals. Here we report the development of a set of microsatellite markers for V.canescens and use them to show that arrhenotokous individuals have more genetic variability than thelytokous ones, which are even homozygous for all tested loci. Crosses between arrhenotokous individuals suggested one marker, Vcan071, to be linked with the Complementary Sex Determiner (CSD) locus and one, Vcan109, with the Virus Like Protein (vlp-p40) locus. The genome size of V. canescens was estimated to be 274-279?Mb. We discuss how both reproductive modes can give rise to the observed genetic variability and how the new markers can be used for future genetic studies of V. canescens.     

Host-searching behavior ofVenturia canescens (Grav.) (Hymenoptera: Ichneumonidae): Superparasitism

The foraging behavior ofVenturia canescens, a solitary endoparasitoid of lepidopteran larvae, was investigated in the laboratory. FemaleVenturia canescens with a larger number of mature eggs to lay were found to have higher levels of superparasitism (measured as numbers of eggs laid per parasitized host). Increased parasitoid density was found to result in reduced levels of superparasitism by host-deprived (i.e.,undepleted) wasps. Females which had been allowed access to hosts before the experiment (depleted wasps) laid fewer eggs per parasitized host than undepleted wasps, although there was no significant difference in the levels of superparasitism among the depletion periods of 1, 2, 5, and 7 h. It was also found that an egg which was encountered less than 15 min after oviposition was much less likely to be avoided than one which was encountered after more than 15 min had elapsed.     

半闭弯尾姬蜂寄主搜索中的学习行为

研究了半闭弯尾姬蜂寄主搜索过程中的学习行为。结果表明,成虫期之前的饲养寄主所取食的寄主植物对成蜂行为没有影响,而雌蜂早期的短暂经历可对其随后的行为反应产生显著影响,从而对已经历的植物气味表现出显著的嗜好,但这种通过学习所表现出的嗜好又可因新的经历而改变。雌成蜂不仅能对其所经历的虫伤寄主植物释放的信息化合物进行学习,而且对其所经历的寄主幼虫的信息化合物也能进行学习。     

Life history of the spider parasitoid Zatypota percontatoria (Hymenoptera: Ichneumonidae)

The life history of polysphinctine parasitoids is poorly understood. As a result, their effect on their host has not been evaluated. Here, we present the phenology of Zatypota percontatoria, an ectoparasitoid wasp of theridiid spiders, using rich field, semi‐field and laboratory investigations of selected life‐history parameters. The wasps overwintered as larva attached to the spider abdomen and the imagos of the first generation emerged at the beginning of May. The sex ratio (F/M) of overwintered wasp larvae was 1.4. The wasp spent an average of 6.4 days in the egg stage, 27.67 days in the larval stage and 9.6 days in the pupal stage. Adult longevity was on average 14.34 days. Oviposition occurred on average 8.44 days following maturity. The wasp laid on average 0.35 eggs/day. The total fecundity was on average 7.4 eggs per wasp and decreased with age (data from unmated females). The developmental rate increased with experimental temperature up to 28 °C. The lower developmental threshold for pupae was estimated at 6.6 °C. The sum of effective temperatures for pupae was estimated at 157.8 degree days. Using daily temperature records from the Czech Republic over the last 41 years, we estimated an average of 3.5 generations of Z. percontatoria per year. Mortality was 48% in semi‐field conditions and 23% in the laboratory. The incidence of mortality was highest during egg and larval stages caused by the detachment of eggs or larvae during spider molting, the mortality of the spider‐host and egg deposition on the spider prosoma.     

Odor-mediated patch choice in the parasitoid Venturia canescens: temporal decision dynamics

Parasitoids foraging for hosts in a heterogeneous environment would greatly benefit if they could decide already from a distance in which areas search for resources would be most profitable and to avoid areas of low fitness returns. Interestingly, the temporal dynamics of the decision process in parasitoid patch choice have rarely been investigated. In a Y-tube olfactometer, we tested whether thelytokous and arrhenotokous females of the parasitoid wasp Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) respond to differences in cues indicating the quality of a host-containing patch and choose more profitable patches. Special attention was given to the time it took females to make their choices (patch choice time) when differences in patch quality were either qualitative (absence vs. presence of hosts and kairomone) or quantitative (various concentrations of hosts and kairomone, and presence of competitors). We found that both thelytokous and arrhenotokous wasps only chose the higher-quality patch based on odor cues when the difference was qualitative. When patches differed only with respect to the number of hosts, or the presence or absence of competing female parasitoids, no significant preference could be found in females of either strain of the parasitoid. In contrast, both the time until females reached the junction of the Y-tube olfactometer (response time) and the time until females decided for either patch (decision time) varied with parasitoid strain and odor treatment. Thelytokous wasps were faster than arrhenotokous wasps in their response time and in their decision time. However, females of both strains responded faster with increasing number of total hosts releasing kairomone. Yet, decision time for patches did not significantly vary as a function of patch quality offered to Venturia wasps.     

Factors determining the functional response of the parasitoid Venturia canescens

A series of experiments were undertaken to determine the factors responsible for the maximum number of hosts attacked by the parasitoid Venturia canescens (Gravenhorst) (Hymenoptera:Ichneumonidae) in the course of functional response experiments. Egg limitation is not a constraint on the maximum number of parasitoid progeny produced per day. Rather, the constraints arise from the requirement that eggs must be moved from the ovarioles to the oviducts and the rate at which this occurs, together with the existence of a positive relationship between the rate of parasitoid searching behaviour and the number of eggs in the oviducts.

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Résumé Le parasitoïde V. canescens produit 251±45 descendants au cours de sa vie. Les adultes ont à l'émergence 23,7±1,1 oeufs dans leurs oviductes ou descendant des ovarioles vers les oviductes à la vitesse de 1,78±0,06 oeuf/heure. II y avait une corrélation linéaire positive entre le temps dépensé par l'ichneumonide à sonder le substrat pour découvrir la larve d'un hôte et le nombre d'oeufs présents dans les oviductes. L'effectif d'oeufs pondus était proportionnel au temps passé à sonder. Le temps nécessaire à la maturation des oeufs et la relation entre le comportement de prospection et le nombre d'oeufs disponibles contribuent à limiter la vitesse de production de descendants au cours des expériences de réactions fonctionnelles. Ces facteurs ne limitent vraisemblablement pas le succès de la reproduction dans les conditions naturelles, à moins que le taux de rencontre des hôtes ne dépasse la vitesse de maturation des oeufs.

     

Automictic and apomictic parthenogenesis in psocids (Insecta: Psocoptera)

Karyotypes and meiosis patterns in three obligatory thelytokous Psocoptera species have been studied for the first time. Females of Aaroniella badonneli (Danks) display 9 chiasmatic bivalents in oocyte metaphase I (2n = 18), hence meiosis is of the automictic type. Females of Ectopsocus meridionalis Ribaga and Valenzuela sp. display 3n = 27, and 27 univalent chromosomes are present in oocyte metaphase I. Thus, meiosis in these species is of the apomictic type.     

Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera)

In the solitary parasitoid wasp Venturia canescens both arrhenotokously (sexual) and thelytokously (parthenogenetical) reproducing individuals occur sympatrically. We found in the laboratory that thelytokous wasps are able to mate, receive and use sperm of arrhenotokous males. Using nuclear (amplified fragment length polymorphism, virus-like protein) and mitochondrial (restriction fragment length polymorphism) markers, we show the occurrence of gene flow from the arrhenotokous to the thelytokous mode in the field. Our results reinforce the paradox of sex in this species.