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.     

Host Handling Time in a Polyembryonic Wasp is Affected both by Previous Experience and by Host State (Parasitized or Not)

Foraging behavior for hosts in parasitoids resembles that of predators with respect to finding, evaluating and manipulating of the prey. Host handling time may depend on the life history of the parasitoid and can be affected by oviposition experience. Additionally, handling time can be affected by host aggregation, species, size and state (parasitized or not). We studied handling times in the egg-larval parasitoid wasp Copidosoma koehleri. We allowed naïve female wasps to oviposit into three consecutive unparasitized hosts, and measured time until oviposition, and the duration of ovipositor insertion. We recorded the same data for naïve females ovipositing into already parasitized hosts. We found that both previous experience by females and previous parasitism of hosts reduced handling time. The results suggest that host handling durations reflect the interplay between host state and parasitoid internal state.     

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.     

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.     

Factors affecting sequential sex allocation in the parasitoid wasp Gryon japonicum

Female wasps of the solitary egg parasitoid Gryon japonicum (Hymenoptera: Platygastridae) allocate male and female offspring in a particular sequence to successive hosts. Male eggs are typically laid in the second host, and the sex allocation sequence is reset after a certain period of time. The present study aimed to examine the underlying mechanism to hold information and reset the sequence by using eggs of Riptortus pedestris (Heteroptera: Alydidae) as hosts. After completion of initial oviposition, a female wasp was treated by cold anesthesia for 1 h, exposure to a parasitized host for 3 h, or being kept at 15°C in darkness for 24 h, and then presented with three host eggs. Cold‐anesthetized females did not reset the sex allocation sequence, indicating that cold anesthesia did not block the mechanism of holding information about oviposition order. Frequent encounters with parasitized hosts were also insufficient to reset the sequence. However, being kept in cool, dark conditions significantly affected resetting, suggesting that low temperature lengthened the time required to reset the sequence. This implies that it is probable that the mechanism to hold information and reset sex allocation sequence in G. japonicum involves metabolism.     

Evidence for a marking pheromone in host discrimination byCephalonomia Stephanoderis (Hym.: Bethylidae)

The bethylidCephalonomia stephanoderis Betrem is an ectoparasitoid that prefers to oviposit on the prepupae and pupae of the coffe berry borerHypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). It has the ability to distinguish unparasitized from parasitized hosts and rarely lays more than one egg per host. The mechanism of this host discrimination byC. stephanoderis was investigated under laboratory conditions. For this, parasitoid eggs that had been deposited on host pupae were removed and pupae were then offered (individually and collectively) to individual female wasps. A total of 92% of individually offered hosts and 93% of collectively offered hosts were not parasitized. It is concluded thatC. stephanoderis recognizes a marking pheromone deposited into or onto the host, preceding, during, or after oviposition which enables female parasitoids to avoid self and conspecific superparasitism.     

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.     

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.     

Host Selection Behaviors and Progeny Suitability of Two Parasitic Wasps,Venturia canescens and Bracon hebetor,against Abnormal Host Conditions of Plodia interpunctella

Abilities of host search, oviposition and progeny development of both endoparasitoid, Venturia canescens, and ectoparasitoid, Bracon hebetor, were compared from four different abnormal host conditions of Plodia interpunctella. Wasps were allowed to parasitize normal, granulovirus-infected, frozen, tebufenozide-treated or multi-parasitized host larvae. Both wasps delayed at various times to locate most hosts that conditioned abnormally. The rates of antennal drumming and ovipositor probing of both wasps were reduced in frozen and multi-parasitized hosts. Particularly, V. canescens strongly avoided these behaviors in a host that previously parasitized by B. hebetor. Oviposition of V. canescens was completely absent in frozen and multi-parasitized hosts but suppressed in a tebufenozide-treated host. B. hebetor suppressed its oviposition only in a frozen host. In addition, the progeny development of both wasps was greatly reduced or absent in most abnormal conditions. However, B. hebetor successfully developed in a host that previously parasitized by V. canescens. Our results in overall indicate that each parasitic behaviors and progeny development are greatly dependent on different host conditions and provides a basis for studies on the mechanism underlying host-parasitoid interactions.     

Inter- and intra-specific host discrimination in gregarious and solitary endoparasitoid wasps

In nature, most species of Lepidoptera are attacked by parasitoids, and some species may be hosts for several parasitoid species. When hosts are parasitized by more than one female of the same species (=superparasitism) or females of different species (=multiparasitism), then intrinsic competition occurs for control of host resources. To reduce competition, some parasitoids are able to recognize the difference between parasitized and unparasitized hosts. Inter- and intra-specific host discrimination were investigated in the two sympatric species, the gregarious Cotesia kariyai (Watanabe) and solitary Meteorus pulchricornis (Wesmael), endoparasitoids of the Oriental armyworm Mythimna separata (Walker). To measure host discrimination, choice experiments were conducted in which females of both species foraged and chose between healthy host larvae and hosts initially parasitized by either C. kariyai or M. pulchricornis. An olfactory test was also performed to examine the discrimination behavior of the two parasitoids. Our results showed that, in oviposition choice tests, both braconid female wasps were able to discriminate between unparasitized hosts and from four to seven day-old hosts previously attacked by conspecific and heterospecific wasps. On the other hand, superparasitism and multiparasitism occurred even in host larvae that were parasitized two days earlier. However, once the immature parasitoids hosts are at larval stage (1st and 2nd instar), super- and multiparasitism were avoided in the two-choice test, but the latter often occurred in the multiple-choice experiment. Host discrimination abilities may have been based on plant volatile signals incurred from damaged plants and internal mechanisms from four to seven post-parasitized hosts.     

Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae)

The role of sex-controlling behaviour at oviposition in generating primary sex ratios, and the effect of larval competition on secondary sex ratios, were studied in the gregarious endoparasitoid, Trichogramma chilonis. The production of a fertilized (female) egg is indicated by the incorporation of a pause in abdominal movements during oviposition, while the absence of it indicates the production of an unfertilized (male) egg. During each ovipositional bout, the first male egg is deposited at the second oviposition, and thereafter at intervals of about eight eggs. This simple pattern enables the wasps to adjust their progeny sex ratios under local male competition to a wide range of host size. Inexperienced wasps do not distinguish between parasitized and healthy hosts. Immature mortality is not significantly different between the sexes when a host is attacked by a single wasp, while females suffer higher immature mortality than males when superparasitism occurs.     

Imperfect preference for singly parasitized hosts over doubly parasitized hosts in the semisolitary parasitoid Echthrodelphax fairchildii: implications for profitable self-superparasitism

Self‐superparasitism can be profitable (i.e., a fitness gain) when conspecific female adult parasitoids prefer singly parasitized hosts over doubly parasitized hosts. This preference is expected to evolve when the value (i.e., the fitness gain from oviposition) of doubly parasitized hosts is lower than that of singly parasitized hosts. We examined whether such a preference is found in the small brown planthopper, Laodelphax striatellus (Fallén) (Homoptera: Delphacidae), and its semisolitary infanticidal parasitoid Echthrodelphax fairchildii Perkins (Hymenoptera: Dryinidae). We compared the preferences and host values between each of four pairs of double and triple parasitism, each of which had the same time interval between the first and last oviposition bouts. Ovipositions on doubly and singly parasitized hosts occurred with similar frequencies in each of the four pairs, even though the doubly parasitized hosts were of lower value than the singly parasitized hosts. However, the value of doubly parasitized hosts with the first and second parasitoid offspring on the same side of the host was higher than that of hosts with the two offspring on different sides, and the value of the former did not differ significantly from that of singly parasitized hosts. The preferences between singly and doubly parasitized hosts with the two offspring on the same or different sides were as expected from differences in their values, except for one pair of double and triple parasitisms. This exception is considered attributable to an imperfect ability to evaluate hosts.     

Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer

Spathius agrili Yang (Hymenoptera: Braconidae) is a newly described and important idiobiont ectoparasitoid of the emerald ash borer (EAB) that has excellent potential as a biological control agent against EAB populations in the USA. In order to understand the ecological factors involved in the search and discovery of concealed hosts by S. agrili, we investigated the behavioral responses of adult female wasps to potential semiochemicals from host plants, hosts, and host frass as well as to vibration signals from host feeding and movement. Using a bioassay, we showed that S. agrili first finds the host’s habitats by detecting the volatile compounds emitted by ash. In the second phase of host location and acceptance, the parasitoids detect the mechanical vibrations produced by host feeding and movement under the surface of the bark and then probe to find the EAB larvae. Contact chemicals seem to play little or no role in short-range host finding. Female wasps avoided laying eggs on EAB larvae already parasitized and thus paralyzed. We hypothesized that female wasps were not attracted to these larvae due to their lack of feeding or movement. While an induced paralysis in the host is instrumental in avoiding superparasitism, we cannot rule out that S. agrili females also use an oviposition pheromone to deter conspecific females. Together, these results suggest that vibration and olfactory cues play significant roles in distinct phases of S. agrili host habitat and host location behaviors.     

Competition for hosts between two hyperparasitoids of aphids,Dendrocerus laticeps andDendrocerus carpenteri (Hymenoptera: Megaspilidae): The benefit of interspecific host discrimination

The two hyperparasitoids of aphids, Dendrocerus carpenteri(Curtis) and Dendrocerus laticeps(Hedicke), differ in their interspecific host discrimination behavior: D. carpenterireadily accepts hosts for oviposition previously parasitized by D. laticeps,whereas D. laticepsoften refrains from ovipositing on hosts previously parasitized by D. carpenteri.The two species also differ in their competitive abilities: D. carpenteriis competitively superior to D. laticepswhen the time between ovipositions is 1 h. D. carpenteri's superiority probably arises from (a) the action of the venom produced by the female to paralyze the host, as evidenced by the comparison of emergence patterns from naturally vs artificially parasitized hosts, and (b) its more rapid egg development. Because of its competitive abilities, D. carpenterigains only limited benefit from discriminating interspecifically, at least when encountering a host parasitized by a competitively inferior species, such as D. laticeps.In contrast, D. laticepsgains considerable benefit from recognizing hosts previously parasitized by D. carpenteri,as the probability to produce offspring from such hosts is greatly reduced.     

Effects of the gregarious parasitoids,Apanteles ruficrus and A. Kariyai,on host growth and development

Two gregarious parasitoids, Apanteles ruficrus and A. kariyai attack larvae of the common armyworm, Pseudaletia separata. Their growth pattern and growth rate of the parasitoids were not affected by host age at the time of oviposition, even though host weight increased exponentially with age. Consequently, the maximal weight of a single parasitoid larva was nearly constant regardless of host instar parasitized. Parasitoid females laid more eggs in later-instar hosts than in earlier-instar hosts. When parasitized at the same age, heavily parasitized hosts attained a larger mass than lightly parasitized larvae. Therefore, the ratio of the maximal weight of the host to the parasitoid mass was nearly constant. These results indicate that host growth is regulated by the parasitoids.     

Patch Time Allocation by the Parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). III. Effects of Kairomone Sources and Previous Parasitism

We investigated the effects of kairomone sources and previous parasitism on the patch-leaving behavior of Diadegma semiclausum, a solitary endoparasitoid of larval Plutella xylostella. Individual female wasps were released onto an experimental plant, and were allowed to freely leave for an alternative host plant placed upwind of the experimental plant in a wind tunnel. In one experiment, the experimental plant was either intact, contained host damage alone, or contained both hosts and host damage. In another experiment, the plant was infested with either unparasitized hosts, hosts parasitized previously by the female herself, or parasitized by Cotesia plutellae, another larval endoparasitoid of P. xylostella. We analyzed the influence of kairomone sources, host types, and within-patch foraging experience on the patch-leaving tendency of D. semiclausum by means of the proportional hazards model. Presence of host damage, and unsuccessful host encounters as a result of host defenses decreased the parasitoids' patch-leaving tendency, while successful oviposition, self-superparasitism, and rejection of parasitized hosts increased their patch-leaving tendency. A conceptual model of the parasitoid's patch-leaving behavior is proposed on the basis of the results of current and previous studies.     

Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology

Asobara japonica (Braconidae) is an endophagous parasitoid developing in Drosophila larvae. The present study shows that A. japonica was never encapsulated in Drosophila melanogaster, and that it caused an overall inhibition of the host encapsulation reaction since injected foreign bodies were never encapsulated in parasitized hosts. Both the number of circulating hemocytes and the phenoloxidase activity decreased in parasitized larvae, and the hematopoietic organ appeared highly disrupted. We also found that A. japonica venom secretions had atypical effects on hosts compared to other braconid wasps. A. japonica venom secretions induced permanent paralysis followed by death of D. melanogaster larvae, whether injected by the female wasp during an interrupted oviposition, or manually injected into unparasitized larvae. More remarkably, these effects could be reversed by injection of ovarian extracts from female wasps. This is the first report that the venom of an endophagous braconid parasitoid can have a deadly effect on hosts, and moreover, that ovarian extracts can act as an antidote to reverse the effects of the wasp's venom. These results also demonstrate that A. japonica secretions from both venom gland and ovary are required to regulate synergistically the host physiology for the success of the parasitoid.     

Oviposition behaviour inOstrinia nubilaus (Lep.: pyralidae) and consequences on host location and oviposition inTrichogramma brassicae (Hym.: Trichogrammatidae)

Before oviposition, Östrinianubilalis Hübner females sweep the surface of the plant with their abdominal tip extruded. The consequences of such behaviour were studied on host searching and oviposition behaviours of the parasitoidTrichogramma brassicae Bezdenko. Egg-masses ofO. nubilalis, associated or not with sweeping, were submitted toT. brassicae females. The behaviour ofT. brassicae females appeared to be very different between the two situations. The parasitoid in the vicinity of an egg-mass associated with sweeping spent more time on the corn leaf. Ninety percent of females located the egg-mass with sweeping, whereas only 40% located the egg-mass without sweeping. Eighty three percent ofT. brassicae females parasitized egg-masses with sweeping, but only 10% in the case without sweeping. Although no deposit was visible, a chemical trail was probably left behind and was found to arrest the parasitoid, to promote host recognition and to trigger oviposition. The amount of the scales left behind on the corn leaf during the sweeping behaviour was also taken into account but did not appear to constitute the trail. The passage over the trail followed by the egg-mass examination constituted behavioural steps which seemed necessary for oviposition in theT. brassicae female     

Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism

Abstract.

• 1 The pay-off from an egg laid in a parasitized host is an important parameter in models on adaptive superparasitism in solitary insect parasitoids.
• 2 For Leptopilina heterotoma, a parasitoid of larval Drosophila, the pay-off from a second egg laid in a host is 0.43 offspring when the interval between the two ovipositions is less than 3h. For longer intervals, this pay-off decreases to almost zero for an interval of 24 h.
• 3 When a female encountering a parasitized host is able to estimate the interval since the first oviposition, it is expected that she will take this into account in her host selection decisions. This is, however, not in the direct interest of the female that lays the first egg, and marks the host.
• 4 We studied whether superparasitism in hosts containing a young egg is more common than in hosts containing an older egg, when searching in a patch containing once-parasitized and unparasitized hosts.
• 5 The acceptance/encounter ratio of parasitized hosts increased for intervals longer than 6h, as predicted when the interests of the marking female and the longevity of the mark are taken into account.
• 6 Superparasitism occurred more often when parasitoids had previously searched a host patch 7 days before the experiment compared to when parasitoids had searched a patch 1 day before, a phenomenon predicted by dynamic optimal diet models.

     

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.