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.     

Effects of host age on the performance of >Diadromus collaris, a pupal parasitoid of >Plutella xylostella

The ichneumonid >Diadromus collaris(Gravenhorst) (Hymenoptera: Ichneumonidae) is amajor solitary, pupal endoparasitoid of thediamondback moth, >Plutella xylostella(Linnaeus) (Lepidoptera: Plutellidae).Experiments to examine parasitism of the hostpupae of different ages by the parasitoid wereconducted in the laboratory. >Diadromuscollaris preferred host pupae that were in thefirst half of their pupal development. Survivalfrom larva to adult, and size and parasitizingcapacity of the resultant female adultsdecreased dramatically as host pupal ageincreased. When ovipositions were made intohost pupae that were in the last quarter oftheir development, all parasitoids died beforeadult emergence. The performance of >D.collaris, as affected by host pupal age,agrees with the simple diet theory thatpredicts female wasps should select hosts ofhigher nutritional quality for oviposition.     

Superparasitism in Cotesia glomerata: response of hosts and consequences for parasitoids

Abstract.  1. Superparasitism occurs in Cotesia glomerata (Hymenoptera: Braconidae), a gregarious endoparasitoid of Pieris spp. (Lepidoptera: Pieridae). The response of P. brassicae larvae to superparasitism and the consequences for the parasitoid were examined in order to elucidate the ecological significance of this behaviour.
2. Field surveys of a Swiss population revealed that C. glomerata brood sizes from P. brassicae larvae ranged from three to 158, and both the female ratio and the body weight of emergent wasps correlated negatively with brood size. In the laboratory, single oviposition on P. brassicae larvae did not produce any brood size larger than 62, but brood size increased with superparasitism.
3. Laboratory experiments demonstrated that both naive and experienced female wasps were willing to attack hosts that had been newly parasitised by themselves or conspecifics. Superparasitism reduced survivorship but increased food consumption and weight growth in P. brassicae larvae. Superparasitism lengthened parasitoid development and prolonged the feeding period of host larvae.
4. Despite a trade-off between maximising brood size and optimising the fitness of individual offspring, two or three ovipositions on P. brassicae larvae resulted in a greater dry female mass than did a single oviposition on the host. Thus, superparasitism might be of adaptive significance under certain circumstances, especially when host density is low and unparasitised hosts are rare in a habitat.     

The development of the endoparasitoid wasp Venturia canescens in superparasitised Ephestia kuehniella

Using a molecular marker that allows the differentiation of two strains of the solitary endoparasitoid wasp Venturia canescens, the study investigated the influence of host mass and the time interval between ovipositions on the survival and development of larvae from both the first and second laid eggs in superparasitised Ephestia kuehniella. As the time interval between ovipositions increased both overall and superparasitism success decreased, however, time between, and order of, ovipositions had little effect on other developmental parameters. Adult size increased with host mass under both parasitism and superparasitism, while host mortality decreased with host mass under superparasitism. In addition, wasps emerging from superparasitised hosts were larger than wasps from parasitised hosts. The results confirm that for V. canescens on the host E. kuehniella both self- and conspecific-superparasitism will be an adaptive strategy when hosts are the limiting factor.     

The fecundity, development and host relationships of Ceratobaeus spp. (Hymenoptera: Scelionidae), parasites of spider eggs

Abstract. 1. Ceratobaeus spp. enter the nest of their host spider and oviposit into eggs through the thin silk eggsac.
2. Temperatures below 15° C limit oviposition by slowing parasites down.
3. Males emerge prior to females and mate with their sibs. Sex ratios of 6.6–6.0:1 in favour of females were observed in the field and laboratory for two species.
4. Even though females can oviposit almost immediately after emergence their full complement of eggs (= 65) is not reached until several days later.
5. Superparasitism is low and appears to occur from subsequent accidental ovipositions. No marking of the external surface of hosts was observed.
6. Parasites overwinter as adults under bark. They do not feed as adults nor do they reabsorb their eggs, but rather oviposit as soon as host eggs become available in spring.
7. Successful oviposition occurs in later stages of host eggs reared at 15° C and 20° C than it does at 25°C. Different rates of development between host and parasite is proposed as an explanation for this phenomenon.
8. The species studied show varying degrees of specificity but each has a dominant host. Location of hosts involves cues from the habitat (bark), silk nests of spiders, and some factor associated with host eggs.     

Host age and fitness-related traits in a koinobiont aphid parasitoid

Abstract.  1. Trade-offs play a key role in species evolution and should be found in host–parasitoid interactions where the host quality may differ between host age categories.
2. The braconid wasp, Aphidius ervi , is a solitary endoparasitoid that allows its aphid hosts to continue to feed and grow after parasitisation. The hypotheses that host age influences their quality and that female parasitoids exploit their hosts based on that quality were tested under laboratory conditions using no-choice tests.
3.  Aphidius ervi females accepted the aphid Myzus persicae for oviposition and their progeny developed successfully in all host ages. The fitness-related traits of parasitoids did not increase linearly with the host age in which they developed. Host quality was found to be optimal at intermediate host ages and the females preferred to parasitise these hosts. The shortest progeny development time and a more female-biased sex ratio were observed in hosts of intermediate age.
4. This study suggests the existence of multiple interactive trade-offs occurring during host–parasitoid interactions according to host age related quality.     

The effect of host stage and temperature on selected developmental parameters of the solitary endoparasitoid Meteorus gyrator (Thun.) (Hym., Braconidae)

Abstract:  The development of the solitary endoparasitoid Meteorus gyrator was compared in the six larval stages of its host, the tomato moth Lacanobia oleracea , and at five constant temperatures. The host instar at the time of parasitism had a marked effect on the larval developmental period of the parasitoid, such that larvae derived from eggs oviposited in first instar hosts took approximately 18 days to egress, whilst those derived from eggs oviposited in sixth instar hosts took <10 days. The weight of cocoons was greatest when oviposition was into final instar hosts, where female cocoons averaged 12.8 mg, and lowest in those derived from eggs oviposited into first instars (9.2 mg). The parasitoid's larval development rate in third instar hosts increased with temperature increments in a linear fashion up to 25°C , after which development times were only marginally increased. At 10°C, the mean larval development time was approximately 90 days and pupal development 35–40 days, whilst at 25°C development times were 10–11 days for larvae and 6–7 days for the pupae. In the majority of cases, overall development times were marginally longer (<1 day) in females than in males.     

Profitable self-superparasitism in an infanticidal parasitoid when conspecifics are present: self-superparasitism deters later attackers from probing for infanticide

Abstract.  1. To reveal the profitability of self-superparasitism when conspecifics are present, the total combined fitness returns from the first and second ovipositions under triple parasitism were compared with fitness returns from the first oviposition under double parasitism, using the small brown hopper Laodelphax striatellus and its semi-solitary infanticidal parasitoid Echthrodelphax fairchildii .
2. The total combined survival rate of the first and second comers under triple parasitism with oviposition intervals of 1/24 h (where 1 and 24 h represent the first-to-second and second-to-third oviposition intervals respectively) was nearly double the survival rate of the first comer under double parasitism with a 25-h oviposition interval, although there was no difference between these triple and double parasitisms in terms of head width and developmental time. Under the conditions of other oviposition intervals, self-superparasitism produced null (1/1- and 24/24-h intervals) or negative fitness returns (24/1-h intervals). This suggests that self-superparasitism on hosts that were self-parasitised 1 h previously is profitable when conspecifics are present.
3. When the female parasitoid laid an egg on a host harbouring the earlier comer(s) on the non-oviposition side, she often probed the non-oviposition side for infanticide, i.e. killing the first offspring. When the first and second comers were on different sides, the probing frequency at the third oviposition in triple parasitism with 1/24-h oviposition intervals was lower than that at the second oviposition in double parasitism with a 25-h oviposition interval. This difference was responsible for the above difference in survival rate between the triple and double parasitisms.     

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.     

Functional response and egg distribution among hosts by Pseudapanteles dignus,a larval endoparasitoid of Tuta absoluta

The functional response of a biocontrol agent has been classically pointed out as a quantitative evaluation criterion to understand its killing capacity to an arthropod pest. In this paper, we revisited the functional response of the internal larval parasitoid Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), a candidate for biocontrol of the South American tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), measured as the daily egg oviposition of single parasitoid females at increasing densities of T. absoluta larvae through dissection of hosts. The functional response curve of the number of parasitized hosts was fitted out taking into account the number of eggs laid and their distribution among hosts at each T. absoluta larval density. The data also allowed us to discuss the self-superparasitism strategy of this parasitoid as an adaptive trait. Pseudapanteles dignus showed a sigmoid shape functional response and a contagious distribution of eggs among hosts, favouring self-superparasitism and laying a similar number of eggs in each superparasitized host at each T. absoluta density. This research is firstly intended to ascertain about the oviposition behaviour of P. dignus and additionally to provide information on its reproduction to be applied in mass rearing procedures and augmentative releases against T. absoluta.     

Evidence for adaptive self-superparasitism in the dryinid parasitoid Haplogonatopus atratus when conspecifics are present

Self-superparasitism – ovipositing in or on a host that was previously parasitized by the same individual – had generally been considered maladaptive for solitary parasitoids. Recently, however, some researchers have suggested that self-superparasitized hosts produce higher fitness returns per host than singly parasitized hosts when these hosts are parasitized by conspecifics. The present study is the first to verify this possibility in the parasitoid Haplogonatopus atratus . Fitness returns from the first and second ovipositions under triple parasitism were compared with those from the first oviposition under double parasitism. Fitness returns were assessed in terms of survival rate, adult size, and developmental time. No differences were found between the two groups in adult size and developmental time. When the interval between the second and third ovipositions was 1 h, the total survival rate of the first and second comers under triple parasitism was higher than the survival rate of the first comer under double parasitism, and as high as the total survival rate of two first comers under double parasitism. This suggests that the value of self-parasitized hosts is as high as that of unparasitized hosts. When the second-to-third interval of triple parasitism was 24 h, self-superparasitism produced no fitness returns. Moreover, fitness returns from ovipositing into self-superparasitized hosts were similar to those from ovipositing into singly parasitized hosts.     

Discrimination of the age of conspecific eggs by an ovipositing ectoparasitic wasp

The recognition and avoidance of already parasitized hosts is a major issue in parasitoid behavioural ecology. A key factor affecting the fitness reward expected from superparasitism is the probability that the second or subsequent egg laid on a host will win the contest with the first-laid egg. The present study investigated the ability of females of the solitary ecto parasitoid Anisopteromalus calandrae Howard (Hymenoptera: Pteromalidae) to (i) discriminate between unparasitized Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) hosts and those parasitized by a conspecific, and (ii) discriminate between a host parasitized by an egg just laid (2 h) and one parasitized by an egg about to hatch (28 h). However, they did not adjust their offspring sex ratio on already parasitized hosts compared to unparasitized ones. Our results show that A. calandrae females can discriminate between parasitized and unparasitized hosts, as they lay more eggs on the latter. The probability of the second or subsequent egg laid on a host (superparasitism) winning the contest with a conspecific increases as the time between the two ovipositions decreases. Consequently, parasitoid females should lay more eggs on recently parasitized hosts than on those that have been parasitized for a long time (i.e., when the first eggs are about to hatch), and that is indeed what they were found to do. To increase their fitness in spite of the presence of already parasitized hosts, A. calandrae females have developed highly discriminative capacities regarding the parasitism status of hosts.     

Increased host acceptance in experienced females of the parasitoid Brachymeria intermedia: which types of oviposition behaviour contribute to experience?

Brachymeria intermedia (Nees) (Hymenoptera: Chalcididae) is a solitary endoparasitoid of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae). The probability that a wasp will parasitise this host is increased if she had a previous oviposition experience. We investigated which types of pre-oviposition and oviposition behaviour induced this change by comparing the acceptance behaviour of wasps with zero to five oviposition experiences as well as wasps with various partial host handling experiences (from no contact with a host to one complete oviposition sequence). The percentage of females accepting the host increased gradually with both the number of previous oviposition experiences and the amount of handling of a single host. Furthermore, the naive females were less likely (44%) to walk to the host than females with a variety of experiences (72–100%). A single antennal contact with the host was sufficient to increase the probability of walking to the host. Additional handling and additional oviposition experiences further elevated the propensity to oviposit. Thus, the modification of the acceptance behaviour through experience was essentially a gradual process in which antennal contact with a pupa was a major element. It is suggested that naive wasps learned the host odour when they first antennated a pupa. As a result, they were attracted to the host odour in subsequent encounters.     

Comparison of oviposition behavior of a solitary and a gregarious parasitoid (Hymenoptera: Mymaridae)

Anaphes victus Huber andAnaphes listronoti Huber (Hymenoptera: Mymaridae) are respectively solitary and gregarious egg parasitoids of the carrot weevil,Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae). We made detailed ethograms of the oviposition behavior on unparasitized and parasitized hosts for the two species. We then compared the behavior of virgin and mated females for the oviposition of male and female progenies. The two species did not always oviposit after insertion of the ovipositor, but these punctures without oviposition could be readily differentiated from oviposition.A. victus oviposited only once by puncture, whileA. listronoti deposited one to three eggs during the same sequence. The variability of the duration of the various components was generally lower for a given female than between females. Two components, the abdominal vibrations and the pause, were significantly shorter in ovipositions that resulted in male progency for the two species. However, an important overlap in duration prevents using these differences to sex the progeny at oviposition. Virgin females of both species, although capable of producing only males, exhibited both behaviors. Parasitized hosts were recognized through internal and external markings that were used in host discrimination.     

Ovicide in the whitefly parasitoid, Encarsia formosa

The oviposition decisions made by insect parasitoids when encountering hosts of variable quality have been the subject of extensive theoretical and experimental investigation. For parasitoids that lay their eggs inside the host, the possible outcomes of encounters with parasitized hosts have been assumed to include only oviposition (superparasitism), rejection, or in some cases feeding on host haemolymph. We document another outcome in Encarsia formosa Gahan (Hymenoptera: Aphelinidae), a species that has been a model system for the study of oviposition behaviour. In E. formosa, females may kill eggs previously laid within the host by jabbing them with their ovipositor before ovipositing themselves. (1) Our observations indicated that jabbed eggs were indeed killed. (2) In experimental arenas in the laboratory, ovicide occurred in the majority of encounters with parasitized hosts and at highest frequency in encounters resulting in oviposition. (3) There was no significant difference in the handling time associated with oviposition+ovicide in parasitized hosts in comparison with oviposition alone, suggesting that there is no time cost to ovicide. (4) Ovicide did not appear to be incidental to normal probing within a host. Radial analysis of the direction of ovipositor movement with respect to the centre of the previously laid egg within the host showed that females engaged in ovicidal bouts probed most often in the direction of the egg. This is the first well-documented study of ovicide in an endoparasitoid. We suggest ovicide may be under-reported in other endoparasitoid species due to the difficulty of observing it. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Effects of pre-adult and adult experience on host acceptance in choice and non-choice tests in two strains ofTrichogramma

The effect of adult learning through an oviposition experience, and pre-adult learning through development inside a host was investigated in two strains of an Australian egg parasitoid,Trichogramma nrivelae (Hymenoptera: Trichogrammatidae). Host response was measured in two types of laboratory preference tests. In single host tests, females reared on three lepidopteran hosts (Heliothis punctigera (Noctuidae),Papilio aegeus (Papilionidae), andHypolimnas bolina (Nymphalinae)) were presented host eggs individually, and allowed two ovipositions. Pre-adult experience affected host preference in only one strain, while acceptance of a host was increased in both strains when they had previously oviposited in this host species. An oviposition experience had a stronger effect on host preference than pre-adult experience. In choice tests, pairwise combinations of hosts were arranged in an alternating grid. The ratio of host acceptances to host contacts was computed for the whole test and up to the first oviposition. These indicated that effects of rearing host were weak or absent, but the host chosen initially had a strong effect on host preference. Relative size of the hosts had a strong effect on choice of the first host. The implications of learning inTrichogramma are discussed in relation to host preference testing procedures and the selection of candidate strains for mass rearing and inundative release.     

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.     

Patch-leaving rules for parasitoids with imperfect host discrimination

Abstract.

• 1 The solitary parasitoid Anagrus delicatus attacks hosts (plant-hopper eggs) that exist in distinct batches and that are readily detectable to the foraging parasitoid. However, Anagrus delicatus attacks only a small fraction of the available hosts within a batch of eggs and then disperses (Cronin & Strong, 1993a). Here we address the question: Why is A.delicatus abandoning seemingly high quality patches?
• 2 A parasitoid with an imperfect ability to discriminate between unparasitized hosts and hosts that it has attacked earlier within the same patch experiences a risk of self-superparasitism when attacking multiple hosts within a single patch. Self-superparasitism can incur costs in the form of lost time and eggs. Early patch leaving can be favoured as a means of avoiding the costs of self-superparasitism.
• 3 A simple static model demonstrates that patch leaving is favoured by low costs of travelling to a new patch, high error rates in discriminating previously self-parasitized hosts, and high levels of parasitism in the currently occupied patch.
• 4 A more detailed dynamic state variable model, parameterized for A.delicatus, demonstrates that this parasitoid's seemingly enigmatic behaviour can be explained under our hypothesis. In order for this to be the case, we predicted that A.delicatus cannot recognize previously parasitized hosts. Subsequent to our prediction, Cronin & Strong (1993b) demonstrated that experienced A.delicatus do not avoid ovipositing in previously self-parasitized hosts.
• 5 Optimal patch leaving rules can be highly sensitive to even very low host discrimination error rates, which may be widespread among parasitoids.

     

Plant wound compounds from oviposition scars used in host discrimination by a stem-galling sawfly

The stem-galling sawfly Euura lasiolepisuses one or more plant wound compounds resulting from oviposition scars as cues in host discrimination (avoiding sites occupied by conspecifics). Four experiments were conducted to test hypotheses about how Euurapartitions resources. Experiment 1 demonstrated that Euuraavoids ovipositing on nodes with scars from previous ovipositions. Experiment 2 showed no evidence that the sawfly uses oviposition-deterring pheromones and indicated there is a time lag following oviposition before the oviposition scar becomes a deterrent. Experiment 3 showed that sawflies avoid artificially formed scars, demonstrating that a plant cue alone can lead to host discrimination. Experiment 4 showed that visual or tactile cues are not necessary for host discrimination and indicated that a plant wound compound functions as an oviposition deterrent. Both experimental results and field surveys showed that Euuraoviposition scars were more uniformly distributed than expected if sawflies were ignoring previous ovipositions.