Does the Polyphagous Egg Parasitoid <Emphasis Type="Italic">Trichogramma platneri</Emphasis> Nagarkatti (Hymenoptera: Trichogrammatidae) Display Behavioral Plasticity When Parasitizing Different Hosts?

Trichogramma platneri oviposition behavior on Amorbia cuneana egg masses was investigated under laboratory conditions. No relationship was detected between host surface area, number of edge turning on host eggs, and parasitoid clutch size. It was also observed that females parasitized the egg mass randomly by drilling into the egg mass and parasitizing individual eggs without using stereotypical behaviors to assess individual hosts (i.e. drumming and turning). However, clutch size did change due to ovipositional experience as naïve wasps with little or no ovipositional experience (<6 eggs parasitized), allocated significantly more progeny per host than wasps with longer ovipositional experience (24-h oviposition experience on a single egg mass). Moreover, naïve wasps parasitized significantly more eggs on the outer edge of the egg mass than experienced wasps. We contend that the physical characteristics of A. cuneana eggs and egg masses preclude T. platneri from completely discriminating between individual eggs. However, because T. platneri may be using kairomones from the egg mass, this described oviposition strategy remains effective.     

Oviposition Behavior and Conspecific Host Discrimination in Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a Fruit Fly Parasitoid

We studied conspecific host discrimination and oviposition behavior of Diaschasmimorpha longicaudata (Ashmead), in third instar Anastrepha ludens (Loew) under laboratory conditions. The complete process of oviposition in D. longicaudata required an average of 29±11.7 s (Mean±SE), during which time the female remained completely immobile. This contrasts with attempts to oviposit for lesser durations (2-4 s), during which the female constantly moved her antennae and abdomen. In order to determine the host discrimination ability of this species (i.e., the capacity to distinguish between parasitized and non-parasitized hosts), third-instar A. ludens non-parasitized or parasitized 24 h earlier, were exposed simultaneously to individual female wasps with or without previous oviposition experience. An identical test was performed using larvae parasitized 48 h earlier. Both types of females showed a similar behavioral pattern of oviposition, but with significant differences in the number of eggs laid in parasitized and non-parasitized larvae. Experienced females showed reduced incidence of oviposition in parasitized larvae as well as a greater number of probes that did not lead to parasitism (rejection), although this difference was only significant in the 24-h test. This suggests that the host discrimination capacity of this parasitoid is innate and that previous oviposition experience increases the discrimination ability of females.     

Host discrimination modulates brood guarding behaviour and the adaptive superparasitism in the parasitoid wasp Trissolcus semistriatus (Hymenoptera: Scelionidae)

Because hosts utilized by parasitoids are vulnerable to further oviposition by conspecifics, host guarding benefits female wasps. The present study aims to test whether female adults regulate brood guarding behaviour by host discrimination in a solitary parasitoid Trissolcus semistriatus by presenting an intact or parasitized host egg mass to a female adult. Virgin females without oviposition experience have host discrimination ability, which enables them to adjust the number of eggs laid in the hosts. Mating experience increases superparasitism by female adults, whereas mated females achieve a higher discrimination ability as a result of oviposition experience and show a lower superparasitism rate. As expected, females exhibit brood guard after parasitizing an intact host egg mass, whereas those females visiting a previously parasitized host egg mass, do not. Because the survival of eggs in superparasitized hosts is relatively low, regulating brood guarding behaviour by host discrimination is adaptive for female wasps.     

Could hosts considered as low quality for egg-laying be considered as high quality for host-feeding?

When parasitoid females encounter a host, they can either lay an egg and thus invest in current reproduction or feed on the host and thus invest in future reproduction. However, hosts could have different values according to their parasitized status. Whereas already parasitized hosts represent poor quality for egg-laying, they could have a high nutritive value for feeding. Moreover, the optimal strategy adopted generally depends on the females’ physiological state. In this study, the impact of the females’ physiological state on their reproductive strategies was investigated in the solitary parasitoid Anisopteromalus calandrae. We analysed how their age and diet influenced (i) the use of hosts (feeding vs. oviposition) and (ii) host selection (previously parasitized vs. unparasitized). Our results show that both age and diet influence the reproductive strategy of A. calandrae females: old females fed with the poorer diet laid fewer eggs and made more host-feeding than others. Females also showed a preference for already parasitized hosts for feeding. This strategy cannot be explained by the nutritive value of haemolymph, as parasitized hosts carry fewer lipids. However, as parasitized hosts are also paralyzed, it could be less costly to feed on them than on unparasitized hosts.     

Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes

The fitness consequences of superparasitism and the mechanism of host discrimination in Cotesia flavipes, a larval parasitoid of concealed stemborer larvae was investigated. Naive females readily superparasitized and treated the already parasitized host as an unparasitized host by allocating the same amount of eggs as in an unparasitized host. However, there was no significant increase in the number of emerging parasitoids from superparasitized hosts due to substantial mortality of parasitoid offspring in superparasitized hosts. Furthermore, the developmental time of the parasitoids in a superparasitized host was significantly longer than in a singly parasitized host and the emerging progeny were significantly smaller (body length and head width). Naive females entered a tunnel in which the host was parasitized 4 h previously and accepted it for oviposition. Experienced females (oviposition experience in unparasitized host) refused to enter a tunnel with a host parasitized by herself or by another female. In experiments where the tunnel and/or host was manipulated it was demonstrated that the female leaves a mark in the tunnel when she parasitizes a host. The role of patch marking in C. flavipes is discussed in relation to the ecology of the parasitoid.     

Differential Host Handling Behavior between Feeding and Oviposition in the Parasitic Wasp <Emphasis Type="Italic">Haplogonatopus hernandezae</Emphasis>

Lifetime fitness is directly influenced by the decision to use resources for either current or future reproduction. Thus, females should weigh the costs and benefits of each reproductive opportunity and allocate resources accordingly. Here, we explore decision-making and the time spent handling hosts of different instars in the parasitoid Haplogonatopus hernandezae, which uses a single planthopper host to either oviposit (i.e., current reproduction) or feed (i.e., future reproduction). Our results indicate that manipulation time in attacks that led to either oviposition and feeding increased with host instar and size. Consequently, attacks were less successful on older host instars than younger ones. Similarly, attack and handling time during oviposition was greater when manipulating fifth instar nymphs compared to younger ones, but oviposition time was similar. Surprisingly, host grasping by the chelate forelegs differed between oviposition and feeding events, and the specific chelate foreleg morphology of H. hernandezae facilitates the specific grasp of the clypeus and gena of the host. We also link this previously undescribed host grasping and differential handling behavior in this species to the final decision to oviposit or feed. Given the differences in handling time and effort among different host instars, we found that older hosts were more often chosen for consumption than younger hosts, and younger hosts were chosen more often for oviposition. Our study suggests that the tradeoff between current and future benefits is influenced by the investment in handling hosts of different instars, and the assessment of host suitability for successful offspring survival.     

Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations

It is generally assumed that resistance to parasitism entails costs. Consequently, hosts evolving in the absence of parasites are predicted to invest less in costly resistance mechanisms than hosts consistently exposed to parasites. This prediction has, however, rarely been tested in natural populations. We studied the susceptibility of three naïve, three parasitized and one recently isolated Asellus aquaticus isopod populations to an acanthocephalan parasite. We found that parasitized populations, with the exception of the isopod population sympatric with the parasite strain used, were less susceptible to the parasite than the naïve populations. Exposed but uninfected (resistant) isopods from naïve populations, but not from parasitized populations, exhibited greater mortality than controls, implying that resistance entails survival costs primarily for naïve isopods. These results suggest that parasites can drive the evolution of host resistance in the wild, and that co‐existence with parasites may increase the cost‐effectiveness of defence mechanisms.     

Host choice decisions in the polyembryonic wasp Copidosoma koehleri (Hymenoptera: Encyrtidae)

Female parasitoids often reject hosts of poor quality, where the survival and fitness of their offspring are expected to be low. In polyembryonic parasitoid wasps, a clone of genetically identical embryos develops from one egg in a host. In the wasp Copidosoma koehleri, each female clone produces one soldier larva that attacks competing clones inside the host. Aggression by soldiers is directed usually towards unrelated clones. Accordingly, it may be predicted that females will prefer nonparasitized over parasitized hosts, especially if the latter have been parasitized previously by a mated unrelated female, as a result of the reduced chances of survival for their offspring inside these hosts. In accordance with these predictions, females prefer nonparasitized hosts over self‐parasitized hosts when they are presented simultaneously. By contrast to the predictions, females prefer hosts parasitized by an unrelated conspecific over nonparasitized hosts when presented simultaneously. Females do not distinguish hosts parasitized by conspecifics from self‐parasitized hosts when presented simultaneously. They reject self‐parasitized hosts significantly more often than hosts parasitized by conspecifics when each host type is presented alone. Females faced with two previously parasitized hosts are not affected in their choice by the mating status (i.e. virgin or mated) of the previous parasitizing females. The combined results suggest that females are limited in their ability to assess the risk that their offspring will be attacked by a soldier, or that this risk is balanced by the relative advantages of ovipositing in a host parasitized by conspecifics. A possible advantage may be increased out‐breeding opportunities for the emerging offspring.     

Host discrimination of a larval parasitoid: the quick movement of Microplitis demolitor

Many parasitoids discriminate previously parasitised hosts from unparasitised ones to avoid mortality of offspring. Parasitoids that parasitise aggressive hosts such as lepidopteran larvae are known to attack hosts very quickly to avoid being attacked. However, little is known about host discrimination of such quick attacking parasitoids. We investigated host discrimination of Microplitis demolitor (Wilkinson) (Hymenoptera: Braconidae) a quick attacking parasitoid of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Results showed that ratios of female wasps that rejected the hosts after antennal examination did not differ between parasitised and unparasitised hosts, indicating that M. demolitor did not discriminate hosts by antennal examination. However, 95% of females that inserted ovipositor into unparasitised hosts actually laid eggs, whereas it was only 31% for parasitised hosts, indicating that females discriminated hosts by oviposition insertion. Analyzing video recordings revealed that the ovipositor exploration of the host took 0.3 s. Female wasps that had experienced high-host density of unparasitised hosts readily rejected parasitised hosts, while wasps with experience of low host availability of parasitised hosts tended to accept parasitised hosts. This suggests that host discrimination behaviour of M. demolitor is affected by previous experience of different host availability and host quality.

     

Putative Host Volatiles Used by <Emphasis Type="Italic">Habrobracon hebetor</Emphasis> (Hymenoptera: Braconidae) to Locate Larvae of <Emphasis Type="Italic">Plodia interpunctella</Emphasis> (Lepidoptera: Pyralidae)

Indianmeal moth, Plodia interpunctella (Hubner) (Lepidoptera: Pyralidae), is a post-harvest pest of grains, milled and processed food, processing plants, warehouses and bakeries. The parasitoid, Habrobracon hebetor (Say) is among the most important natural enemies of Pyralidae infesting stored grains and grain products. Many parasitoids use semiochemicals originating from their hosts, or host’s habitat as cues to locate hosts, hosts’ food or habitat. The authors used Y-tube and four-way olfactometers to assay responses to stimuli with the moth host and thereby understand the role of host-associated semiochemicals in host location by H. hebetor. Responses of mated parasitoid females were assayed to the following stimuli: P. interpunctella sex pheromone, female adults, larvae, or hexane extracts of residue of the rearing medium. Generally, host-related odor sources generated stimuli that elicited better responses than those to blank controls. Previous exposure to odor sources from the host shortened latency periods and response times compared to naïve females. Odors emanating from live moth larvae elicited the strongest responses. When responses from the four odor sources were compared in a four-way olfactometer, it was confirmed that volatiles from larval moths elicited the strongest attraction to the parasitoid. The involvement of host-specific chemical cues in both long and short range host location by female parasitoid is discussed.     

Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species

The oviposition behaviour of Dendrocerus carpenteri (Curtis), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids was examined. Hyperparasitoids were provided in the laboratory with pea aphids ( Acyrthosiphon pisum ) which had been parasitized by three different species of aphidiine wasps ( Aphidius ervi, Ephedrus californicus and Praon pequodorum ) ranging in physiological age from the late larval stage to the late pupal stage. Females accepted only the hosts inside mummified aphids; they ignored live aphids, and did not accept dead, but not yet mummified aphids, although the latter were sometimes probed with the ovipositor. Female behaviour in handling A. ervi or E. californicus mummies did not change with experience; handling and oviposition times were stereotypic. However, naive females needed experience to locate the cocoon of P. pequodorum and distinguish it from the empty aphid mummy. Host acceptance and specificity were influenced more by the developmental stage than the species of the primary parasitoid. In dichotomous choice tests, hyperparasitoids 'preferred' prepupae over younger pupae of A. ervi , but they did not distinguish between these stages of E. californicus; older pupae were accepted at a low rate. Host preference was not influenced by conditioning on the rearing host. We consider several constraints on the host range of D. carpenteri , and discuss alternative explanations of differential hyperparasitism in the field.     

Short-range cues mediate parasitoid searching behavior on maize: The role of oviposition-induced plant synomones

Host searching by egg parasitoids faces a main constraint due to low detectability of cues from host eggs. Therefore egg parasitoids have developed distinctive strategies by exploiting cues that originate from non-target instars of the host and/or from plants. The scelionid Telenomus busseolae is specialized on concealed eggs of Sesamia nonagrioides and other noctuid stemborers. In this paper we show that oviposition by S. nonagrioides induces changes in the cues present on maize leaf surface, which arrest naïve females of T. busseolae. The induction appears to be systemic as the parasitoid also responds to leaves and leaf portions that are not directly affected by ovipositing females. Such oviposition-induced, short-range, plant synomones, acting in sequence with the kairomonal cues from scales left on the plant by the ovipositing host female, significantly increases parasitoid efficiency during host finding. The elicitor of plant response originates from the host female reproductive system, being contained both in the host’s ovarian eggs and in the colleterial gland secretion. Induction starts 24 h after oviposition and lasts at least till 72 h. The ecological role of this oviposition-induced plant synomone in host searching by T. busseolae is discussed.     

Oviposition behaviour ofEphedrus cerasicola [Hym.: Aphidiidae] parasitizing different instars of its aphid host

The parasitoidEphedrus cerasicola Starý oviposited in all 4 nymphal instars and in newly moulted adults ofMyzus persicae (Sulzer). The different host categories were offered with no choice. The duration of an oviposition increased with the age of nymphs, being about 13, 18, 21, 22, and 17 s from 1 st instars to adults, respectively. Observations of number of stabbing attacks prior to oviposition, percent of the encounters not resulting in oviposition, time from first encounter to oviposition, handling time and aphid defensive behaviour also indicated that 1 st instarM. persicae are most easily parasitized. The behaviour ofE. cerasicola in encounters with unparasitized and parasitized hosts, suggested that the parasitoid could discriminate. In encounters with parasitized 1 st to 4th instar aphids,E. cerasicola used only the antennae in 80% of the encounters that resulted in discrimination.     

Host Stage Selection and Sex Allocation by Gyranusoidea tebygi (Hymenoptera: Encyrtidae), a Parasitoid of the Mango Mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae)

Host stage selection and sex allocation by Gyranusoidea tebygi Noyes (Hym,, Encyrtidae) were studied in choice and no-choice experiments in the laboratory. The parasitoid reproduced on first, second, and third instars of the mango mealybug, Rastrococcus invadens Williams (Hem., Pseudococcidae), and it avoided hosts that were already parasitized. Host feeding was occasionally observed. Sex ratios of the offspring produced by individual wasps were highly biased in favor of females, whereas the sex ratio of groups of wasps foraging under crowded conditions varied from male biased in smaller hosts to female biased in larger hosts. Females had longer developmental times than males, developed faster in larger mealybugs than in smaller ones, and were always larger than males emerging from the same host instar. Their size increased with the instar of the host at oviposition. About 90% of all ovipositions in second and third instar nymphs resulted from an attack with multiple stings, starting with a sting in the head of the host for the most part. The function of these head stings is either to assess quality of the host or to subdue hosts prior to oviposition. Encounter rates, number of attacks, and number of stings during one attack increased, while ovipositions decreased with host instar. Time investment per oviposition and time spent preening increased with increasing host age because older hosts defended themselves more vigorously than younger ones. Thus, while fitness of the parasitoid increased with host size, fitness returns per time decreased. The implications of this host selection behavior for the biological control of the mango mealybug are discussed.     

Oviposition decisions in an endoparasitoid under self-superparasitism conditions

Superparasitism is a widespread phenomenon. Having accepted superparasitism, mated female parasitoids must decide on the sex of each egg they subsequently lay into the same host. Theory predicts that this decision is either based on host quality, when more male eggs are laid in hosts that are already parasitized because they are perceived to be of poorer quality; or more eggs are laid of the sex that is most likely to be a strong larval competitor, i.e. generally females.Anastatus disparis is a facultative endoparasitic egg parasitoid. We used ‘artificial’ hosts to explore outcomes of decision making by A. disparis during superparasitism under a manipulated absence of larval competition. When only one egg was laid it was always female. As the number of eggs laid increased, so more of them were male. This supports the theory that oviposition decisions are based on host quality; more male eggs were laid in hosts that were already parasitized and thus of poorer quality.In a second experiment, eggs were exposed to parasitoids for different periods of time. Half the eggs were dissected to determine the number of parasitoid eggs that had been laid. The remaining eggs were incubated and the number and sex of offspring that ultimately emerged, following larval competition, were recorded. Under superparasitism conditions fierce larval competition ensued; only one offspring survived and they were predominantly female.In conclusion, oviposition decisions by female A. disparis accepting self-superparasitism were made based on host quality.     

Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp

Most parasitoid female wasps can distinguish between unparasitized and parasitized hosts and use this information to optimize their progeny and sex allocation. In this study, we explored the impact of mating on oviposition behaviour (parasitism and self‐ and conspecific superparasitism) on both unparasitized and already parasitized hosts in the solitary parasitoid wasp Eupelmus vuilleti (Crw.) (Hymenoptera: Eupelmidae). Virgin and mated females had the same oviposition behaviour and laid eggs preferentially on unparasitized hosts. The sex ratio (as the proportion of females) of eggs laid by mated females in parasitism and conspecific superparasitism was 0.67 ± 0.04 and 0.57 ± 0.09, respectively. Likewise, females laid more eggs in conspecific superparasitism than self‐superparasitism under our experimental conditions. These experiments demonstrate that E. vuilleti females can (i) discriminate between unparasitized and parasitized hosts and adapt the number of eggs they lay accordingly, and (ii) probably discriminate self from conspecific superparasitized hosts. Finally, mating does not appear to influence the host discrimination capacity, the ovarian function, or the oviposition behaviour.     

The parasitoidOoencyrtus nezarae (Hymenoptera: Encyrtidae) prefers hosts parasitized by conspecifics over unparasitized hosts

Summary Two laboratory experiments were conducted to examine the ovipositional preferences of the egg parasitoidOoencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) for parasitized and unparasitizedMegacopta punctatissimum Montandon (Hemiptera: Plataspidae). Females that had never oviposited or that had not oviposite for 3 days preferred recently parasitized hosts more than unparasitized hosts. The preference for recently parasitized hosts appeared to be mediated by the punctures in already parasitized hosts made by the ovipositor of the first female. Survival of the parasitoid progeny was lower in recently parasitized hosts than in unparasitized hosts. However, handling time of parasitized hosts was extremely short relative to that of unparasitized hosts, because the superparasitizing female could use the punctures made by the previous females. It is concluded that the females preferred the parasitized hosts over unparasitized hosts because the benefit of saving time and energy for drilling was more than the cost of progeny survival.     

Host selection and larval interactions among three primary parasitoids ofPlathypena scabra (Lep.: noctuidae)

Three hymenopteran parasitoids that attackPlathypena scabra (F.) larvae often oviposit into consecutive instars of the host. We investigated host discrimination by adults and competitive interactions among larvae of these three parasitoid species. Avoidance of superparasitism byCotesia marginiventris (Cresson) andDiolcogaster facetosa Ashmead was tested. Females of each species were presented either withP. scabra parasitized by a different female of the same species 6 h earlier or unparasitizedP. scabra. Under these conditions,C. marginiventris attacked similar numbers of parasitized and unparasitized hosts.D. facetosa attacked 31% fewer parasitized than unparasitizedP. scabra. The avoidance of multiple parasitism byD. facetosa was studied in a similar bioassay. AlthoughD. facetosa females parasitized fewerP. scabra that had been attacked byC. marginiventris 6 h previously, the reduction in parasitism was only about 23%. In competition studies, immatureD. facetosa were better competitors than immatureC. marginiventris. Aleiodes (=Rogas) nolophanae (Ashmead) was an inferior competitor against bothC. marginiventris andD. facetosa when the duration between parasitism events was 1 h, but their competitive ability increased when they multiply parasitized hosts at least 32 h after the initial oviposition.     

Role of volatile semiochemicals in host location by the egg parasitoid Anagrus breviphragma

Recent investigations conducted on several tritrophic systems have demonstrated that egg parasitoids, when searching for host eggs, may exploit plant synomones that have been induced as a consequence of host oviposition. In this article we show that, in a system characterized by host eggs embedded in the plant tissue, naïve females of the egg parasitoid Anagrus breviphragma Soyka (Hymenoptera: Mymaridae) responded in a Y‐tube olfactometer to volatiles from leaves of Carex riparia Curtis (Cyperaceae) containing eggs of one of its hosts, Cicadella viridis (L.) (Hemiptera: Cicadellidae). The wasp did not respond to host eggs or to clean leaves from non‐infested plants compared with clean air, whereas it showed a strong preference for the olfactometer arm containing volatiles of leaves with embedded host eggs, compared with the arm containing volatiles of leaves from a non‐infested plant or host eggs extracted from the plant. When the eggs were removed from an infested leaf, the parasitoid preference was observed only if eggs were added aside, suggesting a synergistic effect of a local plant synomone and an egg kairomone. The parasitoid also responded to clean leaves from an egg‐infested plant when compared with leaves from a non‐infested plant, indicating a systemic effect of volatile induction.     

Foraging Behavior and Patch Time Allocation by Fopius arisanus (Hymenoptera: Braconidae), an Egg-Larval Parasitoid of Tephritid Fruit Flies

This study quantitatively describes the host-searching behavior of Fopius arisanus (Sonan) (Hymenoptera: Braconidae), an important egg-larval parasitoid of tephritid fruit fly pests, on coffee berries infested with host eggs of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). We also investigate the parasitoid's response to local variation in host patch quality. The temporal pattern of behavioral organisation was examined by constructing an ethogram. The parasitoid spent over 90% of its foraging time in detecting and locating hosts after arriving on a host-infested fruit, and displayed a relatively fixed behavioral pattern leading to oviposition. Patch residence time increased in the presence of host-associated cues, following successful ovipositions, and with increasing size of host clutches per fruit, but decreased with each successive visit to the same host patch and with increasing availability of alternative host patches. The parasitoid females discriminated against previously parasitized hosts and spent significantly less time and searching effort on patches previously exploited by herself or by conspecific females. The effective host-searching behavior, perfect host discrimination ability, and success-motivated searching strategy shown by F. arisanus ensured a thorough exploitation of host resources by this parasitoid.