Presence of conspecifics triggers host searching behavior in an egg parasitoid wasp

Parasitoids and predators compete for host or prey species. The efficiency of obtaining prey or host items is reduced by intraspecific competition. As the optimal search behavior depends on the intensity of competition, it is important for the parasitoid or predator to obtain information on this intensity. Previous studies have shown that parasitoids can obtain information regarding competition from encounters with already parasitized hosts. They then change their host searching behavior accordingly. However, whether parasitoids obtain the information directly from observing the presence of conspecifics remains unclear. We used Tiphodytes gerriphagus (Marchal) (Hymenoptera: Scelionidae), the solitary egg parasitoid of water striders, for testing the effect of density of conspecifics on host searching behavior. Females of T. gerriphagus dive into the water to search for hosts and sometimes they dive without hosts present. Thus, we investigated whether T. gerriphagus changed underwater activities in response to the density of conspecifics in the absence of hosts. Four densities (1, 2, 4, and 8 female T. gerriphagus) were investigated. Females in competitive situations (groups of 2, 4, and 8 females) displayed host searching behavior, but the solitary females did not. This indicates that the presence of conspecifics triggers host searching behavior and that T. gerriphagus females obtain information on competition directly from conspecifics and use it for modifying their behavior.     

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.     

Dynamic egg maturation strategies in an aphid parasitoid

Abstract.  Females of the parasitoid Aphelinus albipodus both lay more eggs on younger stages of their aphid host, Aphis glycines , and contain more mature eggs in their ovaries when held with these younger host stages. This suggests that egg maturation is more rapid in the presence of younger host stages. Three factors explaining the difference in the egg loads of A. albipodus females exposed to various host stages are examined. These are (i) the number of host-feeding meals; (ii) the number of eggs laid; and (iii) the host stage utilized. Together, these factors explain 69% of the variance in A. albipodus egg load. The number of host-feeding meals taken by females is a strong predictor of egg load. More host meals are taken on young hosts, suggesting that host feeding contributes to the trend of faster egg maturation in the presence of younger hosts. Host stage has a strong impact on egg load even when the effect of host feeding is accounted for. There is no evidence for an effect of the oviposition rate on egg load. The results indicate that egg maturation by A. albipodus is dynamic; females mature eggs faster when in the presence of preferred hosts. It is hypothesized that this allows A. albipodus females to more closely match their reproductive effort to reproductive opportunities.     

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.     

Choosy egg parasitoids: Specificity of oviposition-induced pine volatiles exploited by an egg parasitoid of pine sawflies

Generalist parasitoids are well‐known to be able to cope with the high genotypic and phenotypic plasticity of plant volatiles by learning odours during their host encounters. In contrast, specialised parasitoids often respond innately to host‐specific cues. Previous studies have shown that females of the specialised egg parasitoid Chrysonotomyia ruforum Krausse (Hymenoptera: Eulophidae) are attracted to volatiles from Pinus sylvestris L. induced by the egg deposition of its host Diprion pini L. (Hymenoptera: Diprionidae), when they have previously experienced pine twigs with host eggs. In this study we investigated by olfactometer bioassays how specifically C. ruforum responded to oviposition‐induced plant volatiles. Furthermore, we studied whether parasitoids show an innate response to oviposition‐induced pine volatiles. Naïve parasitoids were not attracted to oviposition‐induced pine volatiles. The attractiveness of volatiles from pines carrying eggs was shown to be specific for the pine and herbivore species, respectively (species specificity). We also tested whether not only oviposition, but also larval feeding, induces attractive volatiles (developmental stage specificity). The feeding of D. pini larvae did not induce the emission of P. sylvestris volatiles attractive to the egg parasitoid. Our results show that a specialist egg parasitoid does not innately show a positive response to oviposition‐induced plant volatiles, but needs to learn them. Furthermore, the results show that C. ruforum as a specialist does not learn a wide range of volatiles as some generalists do, but instead learns only a very specific oviposition‐induced plant volatile pattern, i.e., a pattern induced by the most preferred host species laying eggs on the most preferred food plant.     

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.     

Searching and oviposition behavior of a mymarid egg parasitoid, Anagrus nigriventris, on five host plant species of its leafhopper host, Circulifer tenellus

Searching and oviposition behavior and parasitization ability of Anagrus nigriventris Girault (Hymenoptera: Mymaridae), an egg parasitoid of beet leafhopper, Circulifer tenellus (Baker) (Homoptera: Cicadellidae), were examined on five host plant species of beet leafhopper: sugar beet (Beta vulgaris L.), red stem filaree (Erodium cicutarium[L.]), peppergrass (Lepidium nitidum Nuttall), desert plantain (Plantago ovata Forsskal), and London rocket (Sisymbrium irio L.). Beet leafhopper embeds its eggs in the tissues of these plant species. For each plant species, A. nigriventris behavior was examined on plants with and without beet leafhopper eggs. Experimental design was a 5 (plant species) by 2 (host eggs present/absent) factorial. Additionally within each treatment, parasitoid behavior was observed over a 22-h period at five different observation periods: t=0, 3, 6, 9, and 22 h where t=0 h represents initial exposure of the insect with the plant. The behavioral events observed were: `fast walking' (general searching), `slow walking' (intensive searching), ovipositor probing, grooming, feeding, and resting. Significant differences (=0.05) among plant species in time spent on the plant, percentage of host eggs parasitized, and behavioral variables associated with intensive searching and oviposition all indicated that the plant species fell into two groups: `preferred' plants (sugar beet, London rocket, and peppergrass), and `unpreferred' plants (filaree and plantago). These variables also indicated that the parasitoids spent more time on, searched more, probed more, and oviposited more in plants with host eggs than plants without host eggs. Consistent effects of time (over the observation periods from t=0 to t=22 h) generally were detected only in the preferred plant species that had host eggs present. In these cases, intensive searching and probing decreased as time advanced, while variables related to general searching (`fast walking') and abandoning host egg patches (leaving the plant) tended to increase over time.     

Unequal distribution of local mating opportunities in an egg parasitoid

Abstract.  1. The Local Mate Competition (LMC) model predicts that, in gregarious and quasi-gregarious species, a lone female exploiting a host patch will lay only the minimal number of sons necessary to inseminate all daughters, but as the number of foundresses increases, the proportion of sons deposited by these females also increases.
2. For off-patch mating to occur, non-sperm-depleted males must leave the patch and find virgin females.
3. To investigate the distribution of matings among males, the sperm stock at dispersal and the time of dispersal were quantified for male Trichogramma turkestanica (Hymenoptera: Trichogrammatidae).
4. Matings were not distributed equally among males: some successful males acquired more matings than others. Because of this, a high variability in the sperm stock at dispersal was observed. While few males dispersed almost empty or almost full, the majority of males dispersed with enough sperm to be able to mate with females outside the emergence patch.
5. The mating capacity was thus higher than necessary for local mating and could be explained by an unequal distribution of mating opportunities and the occurrence of off-patch mating.     

Host color preferences and short-range searching behavior of the egg parasitoid Trichogramma ostriniae

The color of lepidopteran eggs often varies by species or egg condition, and parasitoids that attack lepidopteran eggs could therefore potentially use color to obtain information about host identity or quality. The objective of our study was to determine whether females of the egg parasitoid Trichogramma ostriniae Pang & Chen (Hymenoptera: Trichogrammatidae) showed differential responses to egg color when searching for hosts over short distances and when evaluating the suitability of encountered eggs. We examined the wasps’ host‐selection behavior in a Petri dish arena using white, yellow, green, and black clay beads as egg models presented against a green background (to mimic leaf color). In no‐choice tests, bead color had a significant effect on the proportion of tested wasps that accepted a bead for further examination, on the time it took wasps to find and begin examining a bead, and on the time that wasps spent examining the beads. However, bead color had only a marginally significant effect on the proportion of wasps attempting to drill into a bead with their ovipositors, and no significant effect on the amount of time they spent drilling. The wasps also showed significant color preferences when given a choice between two adjacent beads of different colors. The results of the no‐choice and choice trials taken together indicated a color preference ranking of yellow > white > green > black. The wasps’ higher preference for the yellow and white egg models generally corresponds to the white or yellowish‐white egg color of T. ostriniae's target host, the European corn borer moth, Ostrinia nubilalis Hübner (Lepidoptera: Crambidae). The wasps’ strong rejection of black egg models is likely to be an adaptive response that reflects the fact that eggs that are wholly or partially black are often unsuitable for parasitization due to advanced caterpillar development, damage to the egg, or previous parasitization.     

Suboptimal oviposition of tephritid flies supports parasitoid wasps

1. Female insects lay eggs on low‐quality plants, resulting in progeny with no or low reproductive potential; this is referred to as ‘suboptimal oviposition’ in this study. 2. Here, it is reported that suboptimal oviposition of a tephritid fly species (Tephritis femoralis) supports the populations of parasitoid wasp species in a Tibetan alpine meadow. 3. Suboptimal oviposition was confirmed because the adult flies emerging from Asteraceae species Anaphalis flavescens flowerheads did not survive cold winters. 4. DNA barcoding of puparia indicated that tephritid larvae developing from suboptimal oviposition hosted populations of at least five parasitoid wasp species. Consequently, suboptimal oviposition has significant effects on parasitoid population dynamics and species diversity.     

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.     

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.     

Flight orientation behavior of Ooencyrtus nezarae (Hymenoptera: Encyrtidae), an egg parasitoid of phytophagous bugs in soybean

We conducted field experiments to examine flight orientation behavior of Ooencyrtus nezarae Ishii, an egg parasitoid of soybean feeding bugs, using sticky traps with synthetic aggregation pheromones of the host, Riptortus clavatus (Thunberg). Experiments were conducted in plots either containing a soybean field or not containing one. When the traps were suspended at heights of 0.5, 1.5 and 3.0 m above a soybean field in Kobe, O. nezarae females were most frequently caught in the 0.5 m traps. In an open field on the same campus where the vegetation was predominantly tall goldenrod, females were more frequently trapped at 1.5 or 3.0 m. In a soybean field in Kumamoto, females were most frequently trapped in the 0.8 m traps, compared to traps placed at 2.0, 4.0 and 6.0 m. In an oat field in the same area, females were trapped most frequently at heights of 0.8 and 2.0 m. Unlike females, only a small number of males were trapped in the fields in both areas. The result that O. nezarae females were caught in traps at higher positions in non‐host habitats than in soybean fields probably reflects differences in host searching behavior in or movement between the habitats. In host habitats, females mainly walk on the plants or fly within the plant canopy to search for hosts. In non‐host habitats, females may not intensively search for hosts within the plants, and directly respond to host pheromones in the traps at heights equal to or a little higher than the plant canopy.     

Diamondback moth egg susceptibility to rainfall: effects of host plant and oviposition behavior

Oviposition patterns of the diamondback moth (DBM), Plutella xylostella L. (Lepidoptera: Plutellidae), differ between common cabbage (Brassica oleracea L. var. capitata) and Chinese cabbage (Brassica rapa L. var. pekinensis) (Brassicaceae) host plants. This study shows that the moth prefers to oviposit on adaxial rather than abaxial leaf surfaces and petioles of both host plants. More eggs were laid in leaf veins than on leaf laminas of both host plants, especially in Chinese cabbage, where 94.6% of eggs were laid in veins. On Chinese cabbage, very few eggs were laid in clusters (≥2 eggs), whereas on common cabbage approximately 30% of eggs were laid in groups of 2 or more eggs. Removal of wax from common cabbage leaves dramatically increased the number of eggs laid singly on the leaf lamina of treated plants, suggesting that leaf waxes affect how eggs are distributed by ovipositing DBM. Eggs were most susceptible to removal by rainfall from the plant surface immediately (<1 h) after oviposition and when close to hatching (>72h old) whereas they were least susceptible 24 h after oviposition. Eggs laid on common cabbage plants were more susceptible to simulated rainfall than eggs laid on Chinese cabbage plants. On common cabbage plants, egg susceptibility to rainfall on different plant parts ranked adaxial leaf surfaces>petioles = abaxial leaf surfaces>stem, but there was no difference in egg susceptibility to rainfall on the various plant parts of Chinese cabbage. Furthermore, on common cabbage plants, eggs laid on both adaxial and abaxial leaf surfaces were afforded significant protection from the effects of rainfall by leaves higher in the plant canopy. On common cabbage plants, oviposition patterns reduce the potential impact of rainfall on eggs, possibly reducing the effect of this important abiotic mortality factor in the field.     

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.     

Host handling behavior of the egg parasitoid Telenomus triptus to the egg mass of the stink bug Piezodorus hybneri

Host handling behavior of Telenomus triptus Nixon (Hymenoptera: Scelionidae) to an egg mass of Piezodorus hybneri Gmelin (Heteroptera: Pentatomidae) was studied in the laboratory. Five distinct behavioral events could be distinguished in the host handling behavior: drumming, ovipositor-insertion, marking, walking, and resting. Female wasps showed two types of behavioral sequence in an ovipositional bout. One consisted of drumming, ovipositor-insertion, and marking, and the other drumming, ovipositor-insertion, walking, and resting. Females did not seem to lay an egg when ovipositor-insertion was not followed by marking. This was observed frequently in the early oviposition bout, on average 2.9 times per female. Females finally succeeded in parasitizing all the eggs in a host egg mass in most cases. The durations of drumming, ovipositor-insertion, and marking on an egg mass were nearly constant, while the total time spent by a female on and beside a host egg mass varied considerably as a result of variable durations of walking and resting. Self-superparasitism occurred when almost all the eggs in a host egg mass were parasitized. Females laid the first male egg within the first four eggs; this could be an adaptation to small egg masses or single egg.