Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

Preference and performance of Anagrus nilaparvatae (Hymenoptera: Mymaridae): effect of infestation duration and density by Nilaparvata lugens (Homoptera: Delphacidae)

The effect of Nilaparvata lugens (St?l) infestation duration and density on the host preference and performance of Anagrus nilaparvatae Pang et Wang, an egg parasitoid of rice planthoppers, was determined. The results showed that the parasitoid preferred N. lugens eggs on the plants infested with 10 gravid N. lugens females for 1 d to those plants infested with 10 gravid females for 2 or 3 d. It was also found to prefer N. lugens eggs on plants infested with 10 or 20 adult females after 24 h of infestation to those plants infested with 5 or 80 females. The parasitoid's offsprings had lower survival rates, fecundities, female ratios, indexes of capacity for population increase, and longer developmental durations on plants when they were infested with high N. lugens density (80 adult females per plant). However, the performance of the parasitoid on plants infested with low N. lugens density (5 female adults per plant) was similar to those on plants with intermediate N. lugens density (10 or 20 adult females per plant). Low preference of the parasitoid for N. lugens eggs on plants with heavy or light infestation levels may be correlated with low host suitability and detectability, respectively. The result implies an important role of herbivore-induced rice volatiles in the host preference of the parasitoid A. nilaparvatae, by which the parasitoid perceives the host and its suitability.     

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.     

Behavioral responses of the parasitoid Psyllaephagus pistaciae (Hymenoptera: Encyrtidae) to host plant volatiles and honeydew

The behavioral responses of the parasitoid Psyllaephagus pistaciae, the major biocontrol agent of the common pistachio psylla, Agonoscena pistaciae, to volatiles emanating from its host plant and host honeydew, were examined using a four‐arm airflow olfactometer. In addition, the arrestment behavior of this parasitoid on clean and honeydew‐treated leaves of the pistachio, Pistacia vera, was monitored. The infested pistachio leaves were the most favored source of the volatile attracting the parasitoids. The parasitoid clearly distinguished and responded to infochemicals emitted by psyllid honeydew but at a lower level than to the volatiles from infested host plants. However, the searching time, locomotory behavior, antennal drumming and ovipositor probing were all affected when they encountered honeydew‐contaminated zones on pistachio leaves. These findings suggest that the psyllid honeydew releases kairomones that stimulate the parasitoids to greater searching activity, as well as providing a directional cue. The intensive searching activities in the presence of the volatiles tested were very similar to responses by the parasitoid females when encountering patches treated with psyllid honeydew. Such behavior could retain the parasitoid in a favorable area, thereby increasing the probability of additional host encounters.     

The role of contact chemoreception in the host location process of an egg parasitoid

Taste allows insects to detect palatable or toxic foods, identify a mate, and select appropriate oviposition sites. The gustatory system strongly contributes to the survival and reproductive success of many species, yet it is rarely studied in insect parasitoids. In order to locate and assess a host in which they will lay their eggs, female wasps actively search for chemical cues using their sensory organs present mainly on the antennae. In this paper, we studied the role of antennal taste sensilla chaetica in the perception of contact semiochemicals in Trissolcus brochymenae (Hymenoptera: Platygastridae), an egg parasitoid of the brassicaceae pest Murgantia histrionica (Heteroptera: Pentatomidae). Methanolic extracts obtained from male and female hosts elicited action potentials in taste neurons housed in antennal sensilla chaetica, indicating that these sensilla are involved in the perception of non volatile host kairomones. In behavioural assays, wasp females displayed an intense searching behaviour in open arenas treated with host extracts, thus confirming that these kairomones are soluble in polar solvents. We further investigated the extracts by Gas Chromatography-Mass Spectrometry (GC-MS) and found that they contain several compounds which are good candidates for these contact kairomones. This study contributes to better understanding contact chemoreception in egg parasitoids and identifying gustatory receptor neurons involved in the host location process.     

Pre‐Patch Experience Affects the Egg Distribution Pattern in a Polyembryonic Parasitoid of Moth Egg Batches

According to foraging theory, female parasitoids should alter their host choice in response to cues that indicate a limitation of resources. We tested whether females of the polyembryonic parasitoid Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), which attack egg batches of small ermine moths (Lepidoptera: Yponomeutidae), would alter their host acceptance pattern in response to different pre‐patch experience. We kept females of the parasitoid prior to a patch visit under different conditions, which should indicate different levels of competition for hosts. With increased competition as pre‐patch experience, females laid more eggs per host egg and self‐superparasitized more often, and the resultant egg distributions showed a trend from more regular distributions to increasingly Poisson and aggregated distributions. Consequently, females with a pre‐patch experience that would indicate low competition for hosts had the most even egg distributions. We conclude that pre‐patch experience of competitors may lead to a significant change of mutual interference patterns in egg‐laying A. fuscicollis wasps.     

Superparasitism as an ESS: to reject or not to reject, that is the question

A stochastic model is formulated to determine the optimal strategy for a solitary parasitoid which has discovered an already parasitized host. The model assumes that the parasitoid can count both the number of eggs already present in a host and the number of conspecifics searching in the same patch. The survival probability of an egg is assumed to depend on the total number of eggs in a host. The decision to (super)parasitize depends both on the degree to which the discovered host already is parasitized and on the number of conspecific females searching in the same patch. We consider both the case that egg laying does not involve any costs for the parasitoid and the case that it involves some marginal costs. Uniform behaviour of all the conspecific parasitoids in a patch, i.e. laying one additional egg in all encountered larvae containing a particular number of eggs, appears to be a pure evolutionary stable strategy (ESS). If either the probability that a parasitoid emerges from a host decreases with an increasing degree of parasitism, at least from a particular number of eggs onwards, or if parasitism involves marginal costs, the maximum number of eggs for which it is still profitable to superparasitize a host once more is limited. This number increases with the number of conspecifics searching in the patch. Large marginal costs (i.e. the expected gain of not parasitizing now) decrease the profit of superparasitism. For newly emerged parasitoids the rejection of an already parasitized host is not advantageous as long as the marginal costs of parasitism are small, because the host can never contain an egg of its own.     

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.

     

Host plants alter their volatiles to help a solitary egg parasitoid distinguish habitats with parasitized hosts from those without

When attacked by herbivores, plants emit volatiles to attract parasitoids and predators of herbivores. However, our understanding of the effect of plant volatiles on the subsequent behaviour of conspecific parasitoids when herbivores on plants are parasitized is limited. In this study, rice plants were infested with gravid females of the brown planthopper (BPH) Nilaparvata lugens for 24 hr followed by another 24 hr in which the BPH eggs on plants were permitted to be parasitized by their egg parasitoid, Anagrus nilaparvatae; volatiles from rice plants that underwent such treatment were less attractive to subsequent conspecific parasitoids compared to the volatiles from plants infested with gravid BPH females alone. Chemical analysis revealed that levels of JA and JA-Ile as well as of four volatile compounds—linalool, MeSA, α-zingiberene and an unknown compound—from plants infested with BPH and parasitized by wasps were significantly higher than levels of these compounds from BPH-infested plants. Laboratory and field bioassays revealed that one of the four increased chemicals—α-zingiberene—reduced the plant's attractiveness to the parasitoid. These results suggest that host plants can fine-tune their volatiles to help egg parasitoids distinguish host habitats with parasitized hosts from those without.     

Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci (Hymenoptera: encyrtidae), a solitary endoparasitoid of citrus mealybug, ++Planococcus citri (Hemiptera: pseudococcidae)

Oviposition and host discrimination behaviour of unmated Anagyrus pseudococci (Girault), an endoparasitoid of the citrus mealybug Planococcus citri (Risso), were investigated in the laboratory. Female parasitoids were able to discriminate between parasitized hosts and healthy ones. The mean number of ovipositions was significantly higher in unparasitized than in parasitized hosts. Conspecific-superparasitism occurred more often than self-superparasitism. Changes in consecutive ovipositions over three hours by A. pseudococci suggested that egg load influenced the discrimination behaviour of the parasitoids, with females which had low egg loads mostly avoiding oviposition in already parasitized hosts at time intervals ranging from 0 h to 96 h, and distributing their eggs in the high quality (unparasitized) hosts. The parasitized hosts were rejected more commonly through antennal perception of external markers than during ovipositor probing which could have encountered internal markers but this relationship changed with increasing time after oviposition. The parasitoid's oviposition rate in unparasitized and conspecific-parasitized hosts varied at the different oviposition time intervals when the females had fewer eggs in the ovaries. Percentage emergence of parasitized offspring was not significantly influenced by whether they developed in single or superparasitized mealybugs. The significance of host discrimination by A. pseudococci is discussed.     

Herbivore-induced plant volatiles as cues for habitat assessment by a foraging parasitoid

1. Animals usually require information about the current state of their habitat to optimize their behaviour. For this, they can use a learning process through which their estimate is continually updated according to the cues they perceive. Identifying these cues is a long-standing but still inveterate challenge for ecologists. 2. The use of plant cues by aphid parasitoids for the assessment of habitat profitability and the adaptation of patch exploitation was studied. Grounding on predictions from optimal foraging theory, we tested whether parasitoids exploited host patches less intensively after visiting heavily infested plants than after visiting plants bearing fewer aphids. 3. As predicted, after visiting heavily infested plants parasitoids reduced their residence time and attacked fewer hosts in the next patch. This was the case regardless of whether the aphids were actually present on the first plant, indicating that the cue came from the plant. Moreover, the level of infestation of a plant at some distance from the first plant visited affected parasitoid patch exploitation on the second plant in a similar manner, indicating that the cue was volatile. 4. These results highlight a novel role of herbivore-induced volatiles in parasitoid foraging behaviour, different from the widely studied attraction at a distance.     

Sex allocation in Telenomus busseolae, a solitary parasitoid of concealed eggs: the influence of host patch size

Telenomus busseolae Gahan (Hymenoptera: Scelionidae) is an important egg parasitoid of noctuid stem borers of gramineous crops, attacking egg masses of Sesamia spp. Under natural conditions, and whatever the host species attacked, these egg masses are generally concealed under the leaf sheaths or other narrow spaces, and vary greatly in size. In the work presented here, the influence of host patch size (4, 8, 16, 32, 64, or 128 eggs per mass) on the sex ratio and sex sequence pattern of ovipositing T. busseolae was investigated in the laboratory using Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae) as host. The results are similar to those described for other parasitoids of aggregated hosts, and are in accordance with the Local Mate Competition model. With increasing egg mass size, the overall sex ratio (proportion of males) decreased, although additional males were laid at the end of the sequence in the larger masses (64 and 128 eggs). Sex sequence pattern always followed a males‐first strategy, i.e., with a higher proportion of males at the beginning, but the whole sex ratio sequence was influenced by the size of the egg mass. Such results in a parasitoid of concealed eggs are compared to those observed in parasitoids of exposed eggs and discussed in terms of parasitoid reproductive strategies and evolutionary adaptations.     

Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid

Host age is an important determinant of host acceptance and suitability for egg parasitoids. As host embryonic development advances, the quality of resources available to the parasitoid offspring typically declines, usually resulting in reduced acceptance levels by foraging females and lower offspring fitness. We examined the ability of the parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) to parasitize and develop in Podisus maculiventris (Say) (Hemiptera: Pentatomidae) eggs of different ages. In laboratory experiments, we measured the effect of host age (6, 24, 48, 72, 96, or 120 h old) on parasitism rate and offspring fitness parameters such as survival, development time, sex ratio, and size. Contrary to our expectations, parasitism rate did not differ between host age treatments, nor did sex ratio allocation, offspring size, or the fecundity of newly emerged female offspring. However, parasitoid offspring had a longer development time with increasing host age. This trend was stronger for males than for females, which we suggest could reduce the degree of protandry among offspring emerging from older host eggs, thus increasing the rate of virginity upon leaving the emergence patch and resulting in more frequent off‐patch mating by female offspring in nature. Overall, our results suggest that all stages of P. maculiventris embryonic development are suitable for acceptance and development of T. podisi. Unlike most species of egg parasitoids, T. podisi has evolved mechanisms to utilize host resources, regardless of host developmental stage, with relatively minor fitness consequences.     

A simple Markov model for the assessment of host patch quality by foraging parasitoids

Insect parasitoids search for their hosts using a method that may be broken into three parts. First, they locate plants which may harbor their hosts, then they assess the quality of these plants to decide whether to search them further for hosts and, finally, if they decide to accept a plant for further search, they exploit the plant by searching for hosts and attacking them when they are found. We study the way that parasitoids assess plant quality by developing a mathematical model based on behavioral observations of foraging parasitoids that attack aphids which infest crucifers. Assessment of plants is based on the concentration of cues produced by hosts that inhabit them. Parasitoids are more likely to exploit plants on which more host cues are detected, and the willingness of a parasitoid to exploit a given plant depends on the quality of other plants that have been visited recently. Plants whose quality exceeds a certain threshold will be accepted for exploitation. The threshold for plant acceptance will change with the experience of the parasitoid, increasing when plants heavily infested with hosts are encountered, decreasing when uninfested plants are encountered. We analyze several rules that might describe how the acceptance threshold changes with parasitoid experience, and for each rule we show how the number of parasitoids willing to accept plants with various levels of infestation depends on the number of plants with various levels of infestation. We then consider different rules for exploitation of hosts on plants and find how the proportion of hosts attacked depends on host density. Received: 21 April 1998 / Accepted: 8 May 1998     

Light brown apple moth in California: a diversity of host plants and indigenous parasitoids

The light brown apple moth, Epiphyas postvittana (Walker), an Australia native tortricid, was found in California in 2006. A field survey of host plants used by E. postvittana was conducted in an urban region of the San Francisco Bay Area. An inspection of 152 plant species (66 families), within a 23-ha residential community, found E. postvittana on 75 species (36 families). Most (69 species) host plants were not Australian natives, but had a wide geographic origin; 34 species were new host records for E. postvittana. Heavily infested species were the ornamental shrubs Myrtus communis L., Pittosporum tobira (Thunb.) W.T. Aiton, Euonymus japonicus Thunb., and Sollya heterophylla Lindl. To survey for parasitoids, four urban locations were sampled, with E. postvittana collected from five commonly infested plants [M. communis, P. tobira, E. japonicus, Rosmarinus officinalis L., and Genista monspessulana (L.) L.A.S. Johnson]. Twelve primary parasitoid species and two hyperparasitoids were reared; the most common were the egg parasitoid Trichogramma fasciatum (Perkins), the larval parasitoids Meteorus ictericus Nees, and Enytus eureka (Ashmead), and the pupal parasitoid Pediobius ni Peck. Meteorus ictericus accounted for >80% of the larval parasitoids, and was recovered from larvae collected on 39 plant species. Across all samples, mean parasitism was 84.4% for eggs, 43.6% for larvae, and 57.5% for pupae. The results are discussed with respect to the potential for resident parasitoid species to suppress E. postvittana populations.     

Geographical variation in resistance of the parasitoid Asobara tabids against encapsulation by Drosophila melanoqaster larvae: the mechanism explored

Abstract. The braconid parasitoid Asobara tabida Nees attacks larvae of several Drosophila species in fermenting substrates. Northwestern and central European populations of the parasitoid attack mainly D.subobscura Collin. Southern European parasitoids attack mainly D.melanogaster Meigen. Larvae of this last species can defend themselves against parasitoids by encapsulating the parasitoid egg. Parasitoids from southern European populations are better able to resist encapsulation of their eggs than their northwestern and central European conspecifics. The eggs of southern European parasitoids appear to have a 'sticky' egg chorion. As a result of this 'stickiness' the eggs become embedded in host tissue where they are not completely covered by the host's blood cells. This leads to, at most, partial encapsulation of the egg. Parasitoid larvae can escape from partially closed capsules.     

Searching and Oviposition Behavior of Anagrus atomus L. (Hymenoptera: Mymaridae) on Four Host Plants of Its Host, the Green Leafhopper Empoasca decipiens Paoli (Homoptera: Cicadellidae)

Anagrus atomus L. is an important egg parasitoid of the green leafhopper Empoasca decipiens Paoli. In this study the ability of the parasitoid to locate and parasitize its host was investigated on four host plants, i.e., broad beans (Vicia faba L.), sweet pepper (Capsicum annuum L.), cucumber (Cucumis sativus L.), and French beans (Phaseolus vulgaris L.). For each plant species, the behavior of the parasitoid was observed on E. decipiens infested and noninfested plants. Searching and oviposition behavior were characterized by drumming, probing, and resting. Parasitoids spent significantly less time on non-infested than infested plants, 274.5 and 875.7 s, respectively, and no probing behavior was observed on non-infested plants. Frequency of resting behavior was significantly greater on non-infested than on infested plants. Total foraging time was significantly longer on infested than on non-infested plants, indicating that A. atomus females can efficiently discriminate between leaves with and without infestation. Parasitism of A. atomus was influenced by parasitoid density, with the highest parasitism rate (64.0%) obtained at a density of 10 A. atomus females/0.1356 m² but the number of parasitized eggs per female and the searching efficiency decreased with increasing parasitoid density.     

Use of time in a decision‐making process by a parasitoid

1. Time perception is seldom studied in invertebrates, with the limited experimental evidence being insufficient to provide a comprehensive pattern of the capacity of invertebrates to measure time and use it in decision‐making processes. 2. In this study, it was hypothesized that insect parasitoids have evolved the capacity to measure time precisely and to use it to optimize foraging decisions related to host exploitation. To examine time perception in females of the gregarious egg parasitoid Trichogramma euproctidis, the present study used their ability to adjust their investment (number of eggs laid) in a host to the initial transit duration (interval between the first contact with the host and the following contact with the substrate). Females utilize this method to assess host egg size, as a large egg necessarily requires more time to evaluate than a small host. In this study, the initial transit duration for a given sized egg was artificially extended by suspending it. 3. For similar sized hosts, female T. euproctidis significantly increased both oviposition duration and progeny allocation following a longer initial transit duration. 4. These results demonstrate the intrinsic capacity of this parasitoid to measure time and to adjust their progeny investment accordingly. This is believed to be one of the few demonstrations of a retrospective measure of time in an invertebrate.     

Effects of the Host Species and the Number of Parasitoids per Host on the Size of Some Trichogramma Species (Hymenoptera: Trichogrammatidae)

The size of some Trichogramma spp. adults and especially the ovipositor length depends on the species, but is also related to the host species and to the number of parasitoids per host. The length is greater in T. evanescens than in T. pretiosum itself greater than in T. exiguum, but the width is similar in the three species. For T. evanescens, the size obtained in Mamestra brassicae host when three or four insects emerged is similar to that obtained in Ephestia kuehniella host when singly parasitized. The size of the ovipositor is important because it may influence the possibility of in vitro egg laying in artificial host eggs. A shorter or a narrower ovipositor could cause difficulties in egg-laying into artificial host eggs composed of a membrane of unsuitable thickness.     

Influence of experience on the sequential and temporal organization of host-acceptance behavior inBrachymeria intermedia (Chalcididae), an endoparasitoid of gypsy moth

Experienced Brachymeria intermediafemales are almost twice as likely to accept a Lymantria disparpupa as inexperienced parasitoids. The sequence of parasitoid behaviors that leads to host acceptance is highly canalized. Experienced parasitoids, however, have a higher probability of initiating host investigation and making a transition from drumming to grasping, which in turn almost invariably leads to ovipositor insertion. Experienced females found the host more quickly than inexperienced females. Host-handling time did not change with experience but was longer in females that accepted rather than rejected the host. Females exposed to gypsy moth odor but not contacting pupae behaved similarly to females that never experienced host-related stimuli.