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.     

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.     

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.     

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.     

Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate

Theory predicts that the acceptance of hosts already parasitized by a conspecific will depend both on egg load and the availability of hosts. In the present laboratory study, we tested the effect of egg load and host encounter rate on the propensity of superparasitism in the solitary parasitoid Aptesis nigrocincta Gravenhorst (Hymenoptera, Ichneumonidae), a synovigeneous ectoparasitoid of prepupae of the European Apple Sawfly. Parasitoid females carry few voluminous eggs at a time and the egg maturation rate is less than one egg per day. Egg load was manipulated by giving females access to hosts one week prior to the start of treatments and host availability by giving females access to either one host cocoon every day or every other day. In the first treatment where females had a high egg load of 5.3 egg in their ovaries and encountered host cocoons at low rates, we found that parasitized hosts were accepted to the same degree as healthy hosts. In females with significantly decreased egg load (3.8 eggs) encountering hosts at the same rate we found a slight but non-significant decrease in the acceptance of parasitized hosts compared with healthy hosts. In contrast, A. nigrocincta females accepted significantly fewer parasitized hosts at a high host encounter rate that would lead them to the point of egg limitation in the near future. Within the range of egg loads tested, the host encounter rate appears to be the most important determinant for a females decision to oviposit onto hosts already parasitized by a conspecific.     

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.     

Sex Allocation Decision Under Superparasitism by the Parasitoid Wasp Eupelmus vuilleti

Superparasitism is a widespread phenomenon in parasitoids and may be advantageous in some circumstances. In this study, offspring sex ratio was analysed in three superparasitism situations: when the second egg was laid by a random Eupelmus vuilleti (Hymenoptera: Eupelmidae) female from a group, when an isolated female was allowed to lay two eggs on the same host (self-superparasitism) or laid one egg on a host already parasitized by a conspecific (conspecific superparasitism). Females produced a different offspring sex ratio according to the different superparasitism situations tested. These sex ratios are in line with the local mate competition theory. The results further suggest that females can discriminate between hosts parasitized by a conspecific or by themselves and adapt the sex of the eggs they lay accordingly.     

Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate

Theory predicts that the acceptance of hosts already parasitized by a conspecific will depend both on egg load and the availability of hosts. In the present laboratory study, we tested the effect of egg load and host encounter rate on the propensity of superparasitism in the solitary parasitoid Aptesis nigrocincta Gravenhorst (Hymenoptera, Ichneumonidae), a synovigeneous ectoparasitoid of prepupae of the European Apple Sawfly. Parasitoid females carry few voluminous eggs at a time and the egg maturation rate is less than one egg per day. Egg load was manipulated by giving females access to hosts one week prior to the start of treatments and host availability by giving females access to either one host cocoon every day or every other day. In the first treatment where females had a high egg load of 5.3 egg in their ovaries and encountered host cocoons at low rates, we found that parasitized hosts were accepted to the same degree as healthy hosts. In females with significantly decreased egg load (3.8 eggs) encountering hosts at the same rate we found a slight but non‐significant decrease in the acceptance of parasitized hosts compared with healthy hosts. In contrast, A. nigrocincta females accepted significantly fewer parasitized hosts at a high host encounter rate that would lead them to the point of egg limitation in the near future. Within the range of egg loads tested, the host encounter rate appears to be the most important determinant for a females decision to oviposit onto hosts already parasitized by a conspecific.     

Recognition of heterospecific parasitism: Competition between Aphidiid (Aphidius ervi) and Aphelinid (Aphelinus asychis) parasitoids of Aphids (Hymenoptera: Aphidiidae; Aphelinidae)

The solitary parasitoids Aphidius erviHaliday (Hymenoptera: Aphidiidae) and Aphelinus asychisWalker (Hymenoptera: Aphelinidae) attacked but generally did not oviposit in pea aphids parasitized by the other species. Wasps selectively oviposited in unparasitized hosts when given a choice. Host discrimination depended on the recognition of internal cues. Females of A. asychiseither could not recognize or ignored A. ervi'sexternal host marking pheromone. Under most conditions, A. ervisurvived in superparasitized hosts, killing competing A. asychislarvae by physical attack and possibly physiological suppression. The outcome of larval competition was not affected by oviposition sequence or age difference between larvae; A. asychissurvived only when it had substantially completed larval development before the host was superparasitized by A. ervi.It is suggested that competition for host resources incurs a cost, for the winner in terms of reduced size or increased development time and for the loser in terms of lost progeny and searching time. Consequently, heterospecific host discrimination can be functional. Internal, and probably general, cues enable wasps to recognize and avoid oviposition in hosts already parasitized by an unrelated species.     

Sex-ratios of the wasp Nasonia vitripennis from self-versus conspecifically-parasitized hosts: local mate competition versus host quality models

Sex ratio patterns in the parasitoid wasp Nasonia vitripennis are frequently cited in support of a major group of evolutionary sex ratio models referred to as local mate competition (LMC) models. It has been shown repeatedly that, as predicted by LMC models, females generally oviposit a greater proportion of sons in previously parasitized hosts than in unparasitized hosts. However, this sex ratio pattern is also a prediction of another group of sex ratio models, the host quality models. Here I test a prediction of LMC models that is not also a prediction of host quality models: a female should produce a greater proportion of sons when she parasitizes a host previously parasitized by a conspecific female than when she parasitizes a host previously parasitized by herself. Females made this predicted distinction between self- and conspecifically-parasitized hosts under some conditions. There was no evidence that a female recognizes a self-parasitized host when her exposure to the host is interrupted by exposure to an unparasitized host, or that a female can distinguish between hosts parasitized by sisters versus nonsisters.     

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.     

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.     

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.     

The Importance of the Parasitoid Egg in Host Discrimination by Cephalonomia stephanoderis , an Ectoparasitoid of the CoVee Berry Borer Hypothenemus hampei

A laboratory study was performed to examine the importance of the parasitoid egg in host discrimination by Cephalonomia stephanoderis Betrem (Hymenoptera: Bethylidae), an ectoparasitoid of the coVee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). C. stephanoderis was able to distinguish between parasitized and unparasitized hosts, and preferred to oviposit on the latter. This discriminative ability appeared to be innate, not learned. W hen the parasitoid egg was removed artificially the host was accepted for parasitism once more, suggesting that the presence of the egg is the most important factor in host discrimination. However, it was not possible to exclude the eVect of a chemical marker present either on or within the host, and/or associated with the presence of the parasitoid egg.     

Efficiency,intrinsic competition and interspecific host discrimination of Copidosoma desantisi and Trichogramma evanescens,two parasitoids of Phthorimaea operculella

Trichogramma evanescens West. (Hymenoptera: Trichogrammatidae) and Copidosoma desantisi Annecke & Mynhardt (Hymenoptera: Encyrtidae) are potential parasitoids of the potato tuber moth (PTM), Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae) in Egypt. Discrimination of a parasitized host from an unparasitized host would prevent wasting of time, eggs and reduce competition with conspecifics or heterospecifics. Therefore, we evaluated interspecific host discrimination, multiparasitism and intrinsic competition between the two wasp species. In a choice test, females of T. evanescens showed high interspecific host discrimination only when they were offered 2-day-old C. desantisi parasitized and unparasitized PTM eggs. In contrast, C. desantisi showed high host discrimination and preferred unparasitized eggs to PTM eggs harboring 2-h- or 2-day-old T. evanescens’ eggs. We also evaluated the effect of different introduction sequences on the efficacy of the two wasps. Dissection data indicated that the two parasitoids had a negative impact on each other. There was a significant reduction in the total number of deposited eggs as well as total number of parasitized hosts by each parasitoid. Regarding the rearing experiment, the total number of T. evanescens-induced black eggs or C. desantisi formed mummies in combined treatments was significantly lower than in single parasitoid treatments (control). Moreover, C. desantisi was inferior and did not develop from any multiparasitized host regardless of oviposition order. It was suggested that combined release of the two wasps would not elevate rate of parasitism over that of single parasitoid treatments and competition between them would reduce their efficacy.     

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.     

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.     

Host-discrimination by <Emphasis Type="Italic">Phymastichus coffea</Emphasis>, a parasitoid of the coffee berry borer

Phymastichus coffea (LaSalle) (Hymenoptera: Eulophidae) is an African endoparasitoid of the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) that has been introduced to several countries to control this important pest. In the present study we performed a series of laboratory experiments in order to determine if there was evidence of host discrimination and superparasitism in P. coffea. Our choice experiments demonstrate that P. coffea females showed significant preference to attack unparasitized hosts, rather than those parasitized conspecifically. No significant preferences were detected in self-specific attacks between parasitized hosts and the healthy ones. A further dissection of hosts sequentially attacked either self or conspecifically, revealed that there were no more than two eggs per host. As P. coffea is a species that normally allocates two eggs per host in a single attack, we assumed that females were able to attack already parasitized hosts, but they did not lay eggs in them. Based on this fact, we conclude that there is a host discrimination ability in P. coffea females. With respect to the superparasitism by P. coffea using non-choice experiments, there was no significant difference between self-specific or conspecific attacks with respect to the control after one or two successive attacks. Conspecific attacks yielded the largest numbers of eggs after 3rd, 4th and 5th attacks and significant differences were found between this treatment and the control. The maximum number of eggs found in a single host was six individuals (conspecific treatment). These results confirmed that P. coffea usually laid two eggs per host; however, when there are no hosts available, conspecific attacks can result in the superparasitism in this species.     

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.

     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.