The dynamics of egg production, oviposition and resorption in a parasitoid wasp

1. The extent to which parasitoid wasps are limited by their egg supply is very important in understanding their reproductive strategies. Egg reserves are dynamic, with most wasps maturing new eggs throughout their life (synovigeny) and many species resorbing eggs that are not used in oviposition. We investigated the extent to which a parasitoid modulates its egg reserves in the light of its experience in finding hosts.
2. The egg dynamics of the Encyrtid Wasp Leptomastix dactylopii , a solitary parasitoid of mealybugs, were studied in the laboratory. This species is synovigenic and practises egg resorption.
3. We allowed newly emerged wasps to experience one of four environments of increasing value in terms of reproductive opportunities. We proposed that wasps that experienced good quality environments would maintain more mature eggs ready for oviposition. Dissection of wasps subject to different periods of host deprivation after the experimental treatment failed to confirm the hypothesis: egg load was independent of experience.
4. We also proposed that any adjustment of egg supply to make up for eggs oviposited would be effected through a reduction in egg resorption. Instead, we found that the wasp quickly made up for eggs oviposited by increased egg production.     

Oviposition behavior of Anagrus nigriventris,an egg parasitoid of beet leafhopper, Circulifer tenellus

Oviposition behavior of Anagrus nigriventris,a parasitoid of the eggs of the beetleafhopper,Circulifer tenellus, wasdescribed on sugar beet. Ovipositor probes ofrelatively long duration were accompanied by a periodof abdominal vibrations toward the end of the probe. These periods began as high frequency, low amplitudevibrations in the abdomen, and climaxed as a tremblingof the whole body in an up and down direction.Oviposition by the parasitoid was associated with theoccurrence of abdominal vibrations during a probe andwith probe durations 50 s; however thepresence/absence of abdominal vibrations during aprobe was considered a more reliable indicator ofoviposition than was a threshold probe duration of 50s. The majority of probes (63% of all probes) were inempty plant tissue, lasted 15 s, and were notassociated with abdominal vibrations. While probeswithout abdominal vibrations at host egg sites (14%of all probes) lasted an average of 48 s, probes withabdominal vibrations at host egg sites (23% of allprobes) lasted an average of 102 s, and all were 50s. It is hypothesized that the relative frequency ofthe 3 types of probes could be affected by the degreeof wasp experience, by the level of host cues on thesubstrate, and by the relative importance of ovipositor probing (vs. antennation) in the hostdetection process. Data from the study suggest thatA. nigriventris is able to discriminate againstpreviously attacked host eggs.     

Plant-mediated decisions by an herbivore affect oviposition pattern and subsequent egg parasitism

Natural enemies are important mortality factors for herbivores and thus may influence herbivore population dynamics. In response to natural enemy pressure, herbivores can alter life history decisions, such as oviposition behavior, so that offspring are protected from natural enemies. One such strategy is to deposit eggs into structures where vulnerability to natural enemies is reduced or eliminated, i.e., use enemy-free space. The plant bug, Lygus lineolaris (Palisot de Beauvois), is native to North America and has a broad host range (>350 plant species), including crops. This bug’s eggs are attacked by a native parasitoid, Anaphes iole Girault, and parasitism levels vary greatly among host plant species. Weed hosts are critical to contemporary L. lineolaris life history because they serve as an ecological bridge from one crop growing season to the next. We investigated the egg distribution pattern of L. lineolaris on 11 host plant species (nine weeds and two crops), and parasitism by A. iole, to determine whether oviposition choices by L. lineolaris females protect their eggs from parasitism and to demonstrate the mechanism of this protection. Our results indicate that the reproductive structures of Erigeron annuus, as well as those of several other host plant species, provide a refuge from parasitism for most L. lineolaris eggs. This refuge is due to the deposition of host eggs deeper in plant tissue than the length of the ovipositor of A. iole. Also, overall parasitism levels were greater on non-Asteraceae host plant species compared with host plant species belonging to Asteraceae. Oviposition site choice by female bugs appears to be a selective strategy to take advantage of enemy-free space.     

Patch exploitation strategy by an egg parasitoid in constant or variable environment

Abstract.  1. In this paper, the foraging behaviour (the proximal mechanisms involved in patch-leaving rules and the egg dispersion) of an egg parasitoid, Anaphes victus , was analysed in environments containing either patches of constant quality (i.e. predictable environment) or patches of variable quality (i.e. unpredictable environment) in order to determine the motivational mechanisms used in patch-leaving strategies.
2. Comparison of the patch exploitation strategy of A. victus between the different habitats suggested that the response of A. victus to a given patch quality strongly depended on its past experiences. Females allocated more time and more eggs in a mixed quality patch after experiencing a poor quality patch than after experiencing a good quality patch. In a poor quality patch, females superparasitised more frequently after experiencing a poor quality patch than after experiencing a good quality patch. In a good quality patch, A. victus females laid more eggs after having visited two poor quality patches than after visiting good quality patches.
3. Recent foraging experiences are used to estimate both the availability and spatial distribution of hosts in the environment and adjust foraging decisions accordingly. The observed variability in the patch-leaving rules within the same species stresses the importance of previous experience when describing behaviours of female parasitoids.     

Kleptoparasitism as an explanation for paradoxical oviposition decisions of the parasitoid Asobara tabida

It is known that the braconid Asobara tabida, a parasitoid of Drosophila larvae, takes oviposition decisions in accordance with survival probabilities in several host species. Nevertheless, larvae of D. simulans, in which the survival probability is virtually zero, are readily accepted for oviposition by searching females. This even happens when they are offered together with D. melanogaster larvae, in which the parasitoid can develop. Here I show that A. tabida can act as a kleptoparasitoid in D. simulans larvae: it can develop in D. simulans larvae, once these larvae are parasitized by another parasitoid, the eucoilid Leptopilina boulardi. Analysis with an optimal foraging model suggests that the increase in survival probability and the occurrence of L. boulardi in the field are high enough to make this kleptoparasitic behaviour of A. tabida pay.     

Host gall size and oviposition success by the parasitoid Eurytoma gigantea

Abstract. 1. Eurytoma gigantea Walsh is a specialist parasitoid of the tephritid gallmaker Eurosta solidaginis (Fitch).
2. In the natural environment the incidence of parasitism by Eurytoma is greater in small galls than in large ones.
3. Laboratory experiments demonstrated that small galls are not more frequently discovered; however, oviposition attempts on small galls were more likely to be successful.
4. Eurytoma spends much time probing galls too big to penetrate; this leads to a decrease in foraging efficiency when many large galls are present.
5. The chance of successfully penetrating a gall depends on the thickness of the gall wall and the length of the parasitoid's ovipositor.
6. A simulation model was constructed which shows that a gallmak-er's chance of being parasitized depends on gall size, the number of parasitoids that discover the gall, and their ovipositor lengths.     

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.     

Influence of host deprivation on egg load and oviposition behaviour of Brachymeria intermedia, a parasitoid of gypsy moth

Abstract. Mated female Brachymeria intermedia (Hymenoptera: Chalcididae) deprived, since emergence, from pupae of their host Lymantria dispar (Lepidoptera: Lymantriidae), accumulated eggs but had a very low rate of hostacceptance. Parasitoids that were host-deprived after encountering pupae early in life also accumulated eggs, but maintained a high acceptance rate. Thus early exposure to hosts promoted active reproductive behaviour. Total egg production depended on the total number of pupae encountered, indicating that B.intermedia adjust their egg production to host availability. Hence, in B. intermedia both the physiological state of the parasitoid (age and egg load) and the informational state (in this case host-availability and experience) interact to shape oviposition behaviour.     

Effect of host deprivation on egg quality,egg load,and oviposition in a solitary parasitoid,Chetogena edwardsii (Diptera: Tachinidae)

Solitary parasitoids are limited to laying one egg per host because larvae compete within hosts. If host encounter rate is low, females should not increase the number of eggs/host in response. The tachinid fly, Chetogena edwardsii,was used to evaluate the effect of host deprivation on egg accumulation, oviposition behavior, and egg quality in a solitary parasitoid. Females deprived of hosts for 2– 7 days accumulate about 1 day's supply of eggs. Egg output of deprived females once hosts are restored does not differ from that of control females. Deprived females retain one egg in the uterus where it undergoes embryogenesis. Maggots emerging from retained eggs are more likely to survive in hosts molting in 40 h or less after receipt of an egg than are maggots emerging from eggs fertilized shortly before oviposition. Egg retention is a consequence of host deprivation that permits females to broaden the range of hosts they can exploit to include soon-to-molt hosts and possibly multiply parasitized hosts.     

An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid

Invasive alien species can act as ‘evolutionary traps’ for indigenous parasites and predators when the alien species is accepted as prey or a host but is unsuitable for consumption or development. We tested the relationship between acceptance and suitability of eggs of the invasive alien Halyomorpha halys (Hemiptera: Pentatomidae) in North America relative to eggs of the indigenous Podisus maculiventris (Pentatomidae) for the indigenous generalist egg parasitoid Telenomus podisi (Hymenoptera: Scelionidae). T. podisi accepted 0–24 h old H. halys eggs at a rate similar to P. maculiventris eggs (87.5 ± 6.0 and 70.2 ± 9.1 %, respectively). Successful development of T. podisi occurred in 98.3 % of attacked P. maculiventris eggs, but was not observed in H. halys eggs. Oviposition by T. podisi did, however, reduce the developmental success of H. halys embryos relative to unattacked controls by 24.1 % in 0–24 h old eggs and 29.6 % in 24–48 h old eggs. We suggest that as H. halys spreads and increases in abundance in North America, it could operate as an evolutionary trap for indigenous egg parasitoids, thereby indirectly causing an increase in population levels of indigenous pentatomids. This predicted indirect effect would be a result of H. halys eggs acting as an egg sink for T. podisi. We also introduce the concept of a ‘time sink’, which may be particularly relevant for parasitoids such as T. podisi that spend considerable time protecting their reproductive investments.     

Effect of insectary rearing on host preference and oviposition behavior of the fruit fly parasitoid Diachasmimorpha longicaudata

Diachasmimorpha longicaudata (Ashmead) has been produced in the laboratory for >160 generations on the larvae of oriental fruit fly, Bactrocera dorsalis (Hendel), the propagation hosts raised routinely on a semi-synthetic wheat diet formulation. Choice tests using modified stinging units were conducted in the laboratory to investigate whether insectary rearing had altered the host seeking and oviposition behavior of female parasitoids. Results showed that fruit fly larvae that developed in papaya, Carica papaya L. var. solo, were less preferred for oviposition than fruit fly larvae that developed on wheat diet when both were exposed concurrently to naive D. longicaudata females (= females without prior oviposition experience). The substrates (pureed papaya or wheat diet) in which treatment larvae were exposed to parasitoids did not affect oviposition preference of gravid D. longicaudata for wheat diet-reared fruit fly larvae. Our study demonstrated the possibility that rearing in an insectary system may have modified the parasitization behavior of female D. longicaudata.     

Maternally induced host regulation by the egg parasitoid Telenomus heliothidis

ABSTRACT. The egg parasitoid Telenomus heliothidis Ashmead (Hymenoptera: Scelionidae) arrested development and prevented emergence of its host, the egg of Heliothis virescens F. (Lepidoptera: Noctuidae). Arrestment was due to a factor injected by the ovipositing parasitoid just prior to egg release. T. heliothidis prevented hatching of H. virescens eggs up to 62 h old. Implantation of the distal region of the parasitoid common oviduct also prevented host emergence. Examination of the distal common oviduct revealed large numbers of protein-containing vesicles in the cytoplasm of the oviduct epithelial cells. These vesicles may be the source of the arrestment factor. The arrestment factor did not prevent emergence of Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae), an interspecific competitor of T. heliothidis.     

Dynamic host-feeding and oviposition behavior of an aphid parasitoid <Emphasis Type="Italic">Aphelinus asychis</Emphasis>

In order to maximize the lifetime reproductive success of parasitoids, they should be induced to dynamically accept individual hosts that have different suitability for oviposition. Parasitoids tend to exhibit higher host-selective behavior when their egg load is limited, and are less selective if they are facing time constraints. Here, we evaluated the effects of parasitoid age on egg load, fecundity and host instar preference of a honey-fed aphid parasitoid, Aphelinus asychis Walker (Hymenoptera: Aphelinidae). Host selective experiment was conducted to measure host-preference of honey-fed A. asychis females at different ages, using the second and fourth instars of the green peach aphid Myzus persicae as their hosts. The results showed that the choice of host-instar for oviposition was significantly influenced by the parasitoid age. Honey-fed parasitoids in the age groups of 1, 5, 10 and 20 days tended to parasitize predominantly second-instar aphids, whereas 15-days old parasitoids showed no significant preference of host instars. On the other hand, host-feeding preference was not affected by parasitoid age. Parasitoid females of all ages preferred younger aphids to older aphids. This result could help evaluate the effectiveness of A. asychis for biological control of M. persicae when they encountered mixed-instar aphids in the field. In addition, the results might be helpful in assessing the host killing effects of other host-feeding parasitoids.     

The effect of travel time on oviposition behavior and spatial egg aggregation: experiments with Drosophila

A higher degree of spatial egg aggregation is often observed in environments where resource patches are more sparsely distributed. This suggests a higher probability of species coexistence when resource distribution is sparse. However, it is still unclear how the degree of spatial egg aggregation increases. I propose a model to explain this phenomenon, which assumes that (i) egg load (the number of mature eggs in ovaries) increases in the travel period between resource patches and (ii) the retention of eggs in the ovaries is harmful (egg load pressure). With these assumptions, a female would lay accumulated eggs on arrival at a new resource patch, resulting in a higher degree of spatial egg aggregation. Laboratory experiments with three drosophilid species, Drosophila simulans Surtevant, Drosophila auraria Peng, and Drosophila immigrans Sturtevant, support the model. This study provides evidence that host availability affects the spatial egg aggregation via egg load.     

Penetration into caterpillar cells of virus-like particles injected during oviposition by parasitoid ichneumonid wasps.

Particles originating from the ovarial calyx epithelium of two different species of ichneumonid wasp are injected into host caterpillars during oviposition. At 1 3/4 h post oviposition, many calyx fluid particles are either associated with or have oenetrated through the basement membranes surrounding various tissues. Shortly thereafter, apparently intact particle nucleocapsids are observed in both the cytoplasm and nucleus of host cells. An unusual tubular protrusion of the viral envelope appears to be involved in either or both of penetration of basement membranes and entry of nucleocapsids into host cells.     

Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula

Abstract. The eggs of the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae), are successfully attacked by Trissolcus basalis (Woll.) (Hymenoptera: Scelionidae) and are recognized as hosts by a secretion applied to the egg chorion. This secretion is produced by the follicular cells in the proximal region of the ovariole of the female pentatomid and functions as an adhesive for attaching the eggs to the oviposition substrate. The adhesive and kairomone activity could be partially removed with water. This water extract elicited host recognition behaviour in T. basalis when applied to glass beads which stuck together as the extract dried. The adhesive and kairomonal activity was removed completely with acetone since acetone-washed host eggs were not recognized by T. basalis. Application of the acetone extract to glass beads stimulated ovipositional probes by T. basalis. The adhesive appeared to be composed of a mucopolysaccharide–protein complex.     

Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens

Superparasitism is a widespread phenomenon in insect parasitoids and may be advantageous in certain circumstances. In this paper, we distinguish two kinds of superparasitism with different adaptive consequences for an ovipositing parasitoid: self superparasitism, where a parasitoid oviposits in a host in which she has previously oviposited, and conspecific superparasitism, where she oviposits in a host containing egg(s) from a previous oviposition by a conspecific. Our studies on Trichogramma evanescens Westwood show that females lay smaller clutches on parasitized than on healthy hosts but make the same overall allocation of males and females, although the sequence of sexes during oviposition differs. No difference was found between allocation in self and conspecific superparasitism. These results are discussed in the light of theories for progeny and sex allocation.

---

Selbst- und konspezifisch-superparasitismus durch die schlupfwespe Trichogramma evanescens

Zusammenfassung Superparasitismus ist ein weitverbreitetes Phänomen in Parasitoiden von Insekten und es kann unter bestimmten Umständen vorteilhaft sein. Diese Arbeit macht Unterschied zwischen zwei Formen von Superparasitismus, jeder mit seiner eigenen adaptiven Konsequenz für die parasitierende Schlupfwespe: Selbst-Superparasitismus, wenn eine Schlupfwespe einen Wirt parasitiert die sie vorher selbst parasitiert hat, und Konspezifisch-Superparasitismus, wenn sie einen Wirt parasitiert die vorher von einem Artgenossen parasitiert worden ist. Unsere Untersuchungen an Trichogramma evanescens zeigen dass die Weibchen auf den belegten Wirten, aber das Gesamtverhältnis von männlichen und weiblichen Brut ist dasselbe, obschon die Reihenfolge in den die Eier der beiden Geschlechte abgelegt werden sich underscheiden. Keinen Unterschied wurde gefunden zwischen die Ablegung während elbst-Superparasitismus und Konspezifisch-Superparasitismus. Diese Ergebnisse werden diskutiert im Rahmen der Theorien für die Belegung des Wirtes in bezug auf die Anzahl und das Geschlecht der Eier.