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.     

拟寄生蜂搜索产卵过程中对寄主的竞争

综述拟寄生蜂搜索产卵过程中对寄主竞争的最新研究进展.这类竞争具有四种方式,即标记寄主、杀卵和杀幼、守护寄主和捕食寄主.（1）标记寄主常涉及寄主标记信息素,这是由雌蜂在产卵前、产卵时或产卵后分泌的化学物质.寄主标记信息素常介导拟寄生蜂对已寄生和健康寄主的辨别、减少过寄生和多寄生、减轻种内和种间竞争压力.（2）雌蜂遇到已寄生寄主时,很多种类杀死前一雌蜂遗留的卵和幼虫,再产下自己的卵.雌蜂使用三种方法杀卵和杀幼,即产卵器穿刺、取食和使用有毒物质.通过杀卵和杀幼,产卵雌蜂清除了前一雌蜂遗留的后代,主动改善了寄主品质,从而有利于自身后代的生存.（3）守护寄主在肿腿蜂科、缘腹细蜂科、金小蜂科、缨小蜂科和茧蜂科中均有报道,守护者驱逐入侵者以保护后代及健康寄主.（4）捕食寄主不仅减少了健康寄主数量,且直接导致已寄生寄主中拟寄生蜂卵和幼虫的死亡.雌蜂一般在体内成熟卵量较少时捕食寄主.讨论了研究拟寄生蜂搜索产卵过程中竞争寄主的理论意义和实际应用价值.     

烟粉虱两种寄生蜂生物学特性及寄主竞争关系研究

室内比较了寄生烟粉虱Bemisia tabaci的两种寄生蜂——丽蚜小蜂Encarsia formosa和浅黄恩蚜小蜂En. sophia的生物学特性,并研究了以烟粉虱为寄主时两种寄生蜂间的竞争关系。结果表明：两者的后足胫节长度间无显著差异。浅黄恩蚜小蜂的产卵器及卵均长于丽蚜小蜂的,但浅黄恩蚜小蜂的待产卵量显著少于丽蚜小蜂。浅黄恩蚜小蜂检测寄主所花时间短于丽蚜小蜂,但检查圈数显著多于丽蚜小蜂,产卵时间以丽蚜小蜂所花时间为多。以4龄初期的烟粉虱为寄主时,丽蚜小蜂的卵期为48 h,而浅黄恩蚜小蜂24 h即完成卵期的发育。后者的蛹历期也显著短于丽蚜小蜂的蛹历期。丽蚜小蜂由卵到成虫的总发育历期比浅黄恩蚜小蜂的要长72 h左右。一头丽蚜小蜂与一头浅黄恩蚜小蜂组合后的总产卵量为14.0粒,略高于两头丽蚜小蜂组合的总产卵量（10.2粒）,显著高于两头浅黄恩蚜小蜂组合的产卵量（9.5粒）;两种蜂组合的处理中被寄生寄主体内的着卵量为1.73粒,显著高于单独一种蜂组合中被寄生寄主的着卵量,后两者分别为1.29和1.39粒。在寄主竞争情况下,在被两种蜂均寄生的寄主体内丽蚜小蜂和浅黄恩蚜小蜂产入的卵量分别为1.21和1.43粒,显著高于仅被一种蜂寄生的寄主体内的对应蜂种的卵量,后者分别为1.06和1.19粒。结果提示两种蜂均能识别对方的存在,且浅黄恩蚜小蜂表现出更强的竞争能力。     

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.     

Heterospecific ovicide influences the outcome of competition between two endoparasitoids, Encarsia formosa and Encarsia luteola

Abstract.  1. Studies of inter-specific competition in parasitoids have largely focused on the outcome of within-host competition and the behavioural mechanisms by which female parasitoids prevent competition. Another, less well studied, possibility is oviposition preceded by 'heterospecific ovicide', the destruction of the other species' egg. Heterospecific ovicide essentially eliminates within-host competition.
2. This study investigated the mechanisms and outcome of within-host competition in Encarsia formosa and Encarsia luteola , solitary endoparasitoids of whitefly pests. These species are known to commit ovicide of conspecific eggs.
3. Competition experiments indicated that the offspring of second-ovipositing females had an apparent advantage in competition, regardless of whether the second female was E. formosa or E. luteola .
4. Observations of ovipositor movement through the cuticle of host whitefly nymphs showed that both species often committed heterospecific ovicide and then oviposited or host-fed. Multiparasitism and heterospecific host discrimination were less common and absent respectively.
5. Heterospecific ovicide appears to explain the second-female advantage in competition between these species. Second-female advantage is contrary to the paradigmatic view of multiparasitism, where the first-ovipositing female has an advantage in competition or one of the species consistently prevails in competition.     

Interspecific host discrimination and within-host competition between Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), two endoparasitoids of whiteflies (Hemiptera: Aleyrodidae)

Interspecific host discrimination and within-host competition between Encarsia formosa Gahan and Encarsia pergandiella (Howard), two endoparasitoids of whiteflies, were studied under laboratory conditions. Interspecific host discrimination was studied at two time intervals (0 h and 72 h after the first species had oviposited). Parasitized and unparasitized Trialeurodes vaporariorum (Westwood) hosts were accepted for oviposition at the same rate by the two parasitoid species. Host type did not affect the handling time of the two parasitoids. The outcome of within-host competition was investigated after females of the two species parasitized the hosts at various time intervals. In four treatments, E. pergandiella was allowed to oviposit 0, 24, 48 and 72 h after E. formosa while in the other two, E. formosa was allowed to oviposit 0 and 72 h after E. pergandiella. In four of these treatments: E. formosa following E. pergandiella at 0 and 72 h, and E. pergandiella following E. formosa at 0 and 24 h, E. pergandiella prevailed. In the host discrimination experiment (72 h interval), 20% of E. pergandiella eggs were killed by E. formosa females. Interspecific ovicide was also observed in the within-host competition experiment, in which 6% of 72-h-old E. pergandiella eggs were killed by E. formosa females.     

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.     

Factors governing host discrimination byOpius dimidiatus (Ashmead) (Hymenoptera: Braconidae)

The detection of, and response to, parasitized hosts by female parasitoids can involve a number of complex phenomena, including the ability of females to discriminate between unparasitized and parasitized hosts, the physiological state of females, and the nature and longevity of the cues they are detecting. The discriminatory ability of Opius dimidiatus,a solitary endoparasitoid of Liriomyza trifoliiwas examined. Experiments showed, first, that when presented with a choice of unparasitized hosts and hosts which they had previously parasitized, O. dimidiatusfemales could discriminate between them, both upon encounter (before probing) and after probing with the ovipositor. It was further demonstrated that the detection of parasitized hosts was time dependent: females could discriminate on the basis of antennal examination for up to 2.5 h after the first egg was laid. Postprobing discrimination lasted for up to 3.5 h. Some of the causal and evolutionary factors resulting in superparasitism are discussed.     

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.     

Biosteres longicaudatus: Developmental dependence on host (Anastrepha suspensa) physiology

Larvae of Anastrepha suspensa that were in the first day of the third instar were parasitized by females of the solitary endoparasitoid, Biosteres longicaudatus. At the end of the 6-hr oviposition period, larvae were ligated posterior to the ring gland so that some larvae had parasitoids anterior to the ligature while in others, the parasitoids were in the abdomen, posterior to the ligature. Ninety-two percent of the parasitoids anterior to the ligature hatched to the first through third instars. Parasitoids posterior to the ligature had a 75% egg hatch to the first instar only. No larval molts to the second or subsequent instars occurred in these parasitoids. Upon parabiosis to 3-day-old, unparasitized host pupae, the ligated larvae pupated and 97% of the first-instar parasitoids in these parabiosed larval abdomens molted to the second instar. Newly laid parasitoid eggs transplanted to 3-day-old pupal hosts had less than one-third of the egg hatch of those transplanted to first-day third-instar hosts. The data implicate the physiological state of the host (vis-a-vis pupation and associated events) as being an important factor in the development of the endoparasitoid.     

Host-searching behavior ofVenturia canescens (Grav.) (Hymenoptera: Ichneumonidae): Interference—the effect of mature egg load and prior behavior

The foraging behavior ofVenturia canescens, a solitary endoparasitoid of lepidopteran larvae, was investigated in the laboratory. Females with a greater number of mature eggs in their ovarioles and oviducts parasitized a greater number of hosts and won a greater proportion of encounters with other searching females. Wasps which had been exposed to hosts prior to an experimental trial lost a higher proportion ofagonistic encounters with conspecifics than wasps which had no prior exposure to hosts. The behavior of a wasp at the time of the encounter influenced the outcome of the encounter. Wasps involved in active search of the host medium with the ovipositor (probing) were more likely to win encounters than wasps in any other behavioral category. In a situation where the agonistic encounter was between two probing wasps, both contestants were equally likely to win. Results are discussed in the light of the idea that mutual interference arises, in this species, as a result of agonistic encounters between searching females and recent dynamic-programming models which suggest that parasitoid oviposition should be influenced by mature egg load.     

Intra- and interspecific host discrimination in two closely related egg parasitoids

Intraspecific host discrimination is frequently found in solitary parasitoids, but interspecific host discrimination, where female parasitoids recognize hosts already parasitized by females of other species, is rare. This particular behaviour appears to be adaptive only under specific circumstances. In this paper, we quantified intraspecific host discrimination in Anaphes n. sp. (Hymenoptera: Mymaridae), an endoparasitoid of the eggs of Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) and interspecific host discrimination toward eggs parasitized by Anaphes sordidatus (Girault), a sympatric species competing for the same resource in similar habitats. To examine host discrimination, choice experiments were used where the females had to choose between different categories of eggs (unparasitized, parasitized by Anaphes n. sp. or A. sordidatus). Superparasitism and multiparasitism were avoided in experiments where the female had a choice between unparasitized hosts and hosts parasitized by the same female, by a conspecific or by a female A. sordidatus. When all hosts available were parasitized, conspecific superparasitism occurred more often than self-superparasitism or multiparasitism. These results indicated that females Anaphes n. sp. were capable of self-, conspecific and interspecific discrimination. Self-discrimination followed recognition of an external marking while interspecific discrimination occurred mostly after insertion of the ovipositor. Interspecific discrimination could result from the recent speciation of these species and could be associated with a genotypic discrimination. This behavior appears to be adaptive because of the competition for common hosts between the two parasitoid species.     

Environmental and genetic determinants of ovicide in parasitic wasp Bracon hebetor

Superparasitism occurs when a parasitoid lays a second clutchof eggs on a host previously parasitised by herself or a conspecific.Ovicide refers to a parasitoid destroying an existing clutchof eggs on a parasitized host before laying a second clutch.We investigated environmental and genetic determinants of ovicidein the parasitic wasp Bracon hebstor. Characterization of egglayingbehavior revealed that B. hebetor commits ovicide during thehost examination phase of oviposition. The temporal costs ofovicide were found to be relatively small for females that experiencedlow rates of host encounter, whereas the costs of ovicide increasedfor females that experienced a high rate of host encounter.Individual wasps committed ovicide on conspecifically parasitizedhosts more frequently than on self-parasitized hosts. Manipulationexperiments suggested that B. hebetor females learn about theirenvironment while foraging and commit ovicide on the basis ofthe travel time between successive hosts. Significant differenceswere also found in ovicidal behavior among laboratory and fieldpopulations of B. hebetor. The implications of our results forclutch size theory and the evolution of ovicide are discussed.     

Fitness consequences of ovicide in a parasitoid wasp

Ovicide, superparasitism and host rejection are alternative reproductive tactics facing female parasitoid wasps encountering an already-parasitized host. Superparasitism is simply the addition of an egg or a clutch of eggs by the secondary parasitoid, but under ovicide the primary clutch is removed or destroyed. Host rejection occurs if the wasp leaves without laying a clutch. The ectoparasitoid Laelius pedatus (Say) (Hymenoptera: Bethylidae) performs ovicide in this situation. Clutch manipulation experiments show that secondary clutches suffer high mortality in competition with primary clutches, which increases with increasing time delay between clutches. Primary clutches however suffer little in competition with secondary clutches, even if there is minimal time delay between clutches. These data suggest that the offspring of ovicidal females are substantially fitter than the offspring of superparasitizing females. Handling time and clutch size do not differ significantly between first (sole) parasitoids and second (ovicidal) parasitoids. The same is true for offspring survival and development time. However, offspring of second females are slightly smaller. This suggests that parasitized and unparasitized hosts are resources of similar quality when ovicide is performed. These data strongly support the predictions of evolutionary models of ovicide. They may also give some insight into the taxonomic distribution of ovicide in parasitoids.     

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.

     

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.     

Sex allocation and egg distribution of an autoparasitoid, Encarsia pergandiella (Hymenoptera: Aphelinidae)

Abstract. 1. Encarsia pergandiella Howard females develop as primary parasitoids on immature whiteflies, and males develop as secondary parasitoids on females of their own or a related species. The hypothesis that the sex ratio reflects the relative abundance of the two host types was tested in the laboratory using petri dish arenas with varying proportions of early fourth instar greenhouse whitefly (Trialeurodes vaporariorum (West.)) (primary hosts) and pupal female E.pergandiella (secondary hosts). Egg distribution was analysed with respect to sex ratio, super-parasitism and host discrimination.
2. The proportion of primary and secondary hosts parasitized in each treatment reflected the relative availability of each host type. Thus females presented with 75% primary hosts laid more female eggs than male. However, in all treatments, a greater proportion of secondary hosts were parasitized than would be expected from the proportion of secondary hosts available. This indicates that more male eggs were laid than expected.
3. More secondary hosts than primary hosts were superparasitized.
4. Host discrimination analysis using a new test statistic showed that females generally laid eggs at random with regard to previous parasitism of primary or secondary hosts. However, females in one treatment with 50% of each host type appeared to preferentially oviposit in secondary hosts which did not contain any eggs.     

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.     

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.     

玉米螟赤眼蜂（Trichogramma ostriniae）寄主标记信息素和学习经历对产卵行为的影响

报道了标记信息素和雌蜂经历对玉米螟赤眼蜂Trichogramma ostriniae产卵行为的影响。研究结果表明,玉米螟赤眼蜂的寄主标记信息素是在其产卵过程中的收场阶段由产卵器产生的,并且标记在寄主卵表的化学物质;玉米螟赤眼蜂对标记信息素的识别不具有先天性,其必须先用产卵器插入寄生卵来检测是否被寄生,然后其触角不停地敲击,通过学习获得对标记信息素的识别能力,从而放弃了对寄生卵的选择,学习对初始放弃时间有着重要影响,改善了其对寄主搜索效率,这种学习行为是与寄主联系在一起学习的,它能根据寄主被寄生与否而对标记信息素作出反应与不反应。该研究丰富了生态学理论,为其在生防中更好的应用提供了科学依据。