‘Males second’ strategy in the allocation of sexes by the parasitic wasp,Gryon japonicum

Summary Patterns of the sex ratio allocation of Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae), a solitary egg parasitoid of Riptortus clavatus (Thunberg) (Heteroptera: Alydidae), were investigated in the laboratory, and the result was checked against the field data on the sex composition of the parasitoid. When five host eggs were presented simultaneously to each of the females of G. japonicum in a laboratory experiment, they had a strong tendency to lay a male egg in second host egg and female eggs in the others. However, when four host eggs were presented to each female more than 3 h after the completion of oviposition on a host egg, most of the females laid male eggs in the third oviposition, i.e. the second host eggs after the experimental interruption of oviposition. These results indicated that there was a mechanism for G. japonicum to produce a male egg in the second host egg in consecutive ovipositions, and that the mechanism was reset by more than 3 h intervals of oviposition. By this mechanism, G. japonicum is thought to produce the precise sex ratio in response to the size of a host egg batch. Field data on the size of a host egg batch and the sex composition of the parasitoid in a host egg batch supported this view.     

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.     

Refrigeration of Riptortus clavatus (Hemiptera: Alydidae) eggs for the parasitization by Gryon japonicum (Hymenoptera: Scelionidae)

Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae) is a solitary egg parasitoid of Riptortus clavatus (Thunberg) (Hemiptera: Alydidae) one of the most important pests in soybean in Korean and Japan. Refrigeration of R. clavatus eggs for up to 120 days was evaluated as a method of mass production of G. japonicum. The refrigeration reduced the eclosion of eggs, thus no nymph emerged after 30 days of egg refrigeration. Increased duration of host acceptance behaviors by G. japonicum and some detrimental effects on parasitism rate, developmental time, longevity, and adult size of the parasitoid were found in refrigerated host eggs. However, all the biological parameters of G. japonicum were unaffected by the refrigeration of up to 30 days. Gryon japonicum parasitized 16 and 14 host eggs daily that were refrigerated for 15 and 30 days, respectively, which did not differ from parasitization of fresh host eggs. Furthermore, refrigeration of host eggs did not reduce the reproduction of the emerged adult parasitoids and emergence and sex ratio of their progeny. Gryon japonicum also parasitized 14 and 13 refrigerated host eggs per day kept at 26.3°C and 78.7% RH for 2 and 4 days of post-refrigeration without significant reduction, respectively. These results show that refrigeration of R. clavatus eggs can be a good method for mass rearing of the parasitoid, and the host eggs killed by cold storage can be supplemented in the field to boost field parasitism.     

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.     

Effect of fertilized,unfertilized, and UV‐irradiated hosts on parasitism and suitability for Trichogramma parasitoids

Trichogramma spp. (Hymenoptera: Trichogrammatidae) parasitoids have been commonly used as biological control agents in insect pest management. Host quality is believed to influence parasitism, host preference, and suitability for parasitoids. To date, limited studies have compared the parasitism of Trichogramma parasitoids on fertilized, unfertilized, and sterilized host eggs. Hence, we studied the performance of three Trichogramma egg parasitoids, Trichogramma japonicum Ashmead, Trichogramma chilonis Ishii, and Trichogramma leucaniae Pang & Chen, on fertilized, unfertilized, and ultraviolet (UV)‐irradiated fertilized (UVF) eggs of rice moth, Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). In a no‐choice test, T. japonicum and T. leucaniae parasitized significantly more fertilized or UVF than unfertilized hosts, and T. chilonis parasitized significantly more UVF than either fertilized or unfertilized hosts. In a choice test, all three Trichogramma parasitoids parasitized UVF hosts the most, and unfertilized hosts the least. There were similar percentages of adult emergence and female progeny among fertilized, unfertilized, and UVF hosts for all three Trichogramma parasitoids, except that T. japonicum had significantly lower adult emergence on fertilized hosts. We also found that all three Trichogramma parasitoids developed slower on unfertilized hosts. Regardless of host treatments, T. leucaniae had the longest developmental time and T. chilonis had the shortest. We conclude that Trichogramma parasitoids prefer parasitizing UVF eggs of C. cephalonica without negative effects on their emergence and sex allocation.     

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.     

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.     

Variable sex ratio strategy of Telenomus heliothidis (Hymenoptera: Scelionidae): adaptation to host and conspecific density

Summary The sex allocation behavior of the solitary egg parasitoid Telenomus heliothidis Ashmead was investigated by examining the response of females reared in isolation and under crowded conditions. Females reared in isolation adjusted their sex ratio with foundress and host number per patch in accordance with the predictions of local mate competition (LMC) theory. However, females did not shift their sex ratio in response to conspecifics foraging on the same host patch or to contact with previously parasitized hosts. Instead, shifts were associated with encounter rate and a sequence of oviposition. Females maintained under crowded conditions responded to host patches much differently. One-day-old females which had lived under crowded conditions for 24 h produced sex ratios similar to those of continuously isolated females. However, females reared under crowded conditions for 7 days consistently produced unbiased sex ratios, and exhibited a different sequence of oviposition. This shift appeared to be due directly to crowding rather than age, oviposition experience or sperm depletion since the effect could be reversed by subsequent isolation.     

The oviposition behavior ofAphidius ervi andMonoctonus paulensis (Hymenoptera: Aphididae) encountering different host species (Homoptera: Aphididae) in sequential patches

Two-day-old mated females ofAphidius ervi Haliday andMonoctonus paulensis (Ashmead) were each provided with two sequential host patches. Patches were comprised of plastic petri dishes containing either 15 pea aphids,Acyrthosiphum pisum (Harris), or 15 alfalfa aphids,Macrosiphum creelii Davis. Both wasp species parasitized more hosts in patches containing pea aphids than in those containing alfalfa aphids, regardless of sequence. Females ofA. ervi also laid more eggs per aphid in patches containing pea aphids than in patches containing alfalfa aphids. When both patches contained alfalfa aphids,M. paulensis females parsitized more aphids in the second patch than in the first. Fewer alfalfa aphids were parasitized in the second patch when the first patch contained pea aphids, and fewer eggs were laid per alfalfa aphid. Parasitoid females of both species exhibited consistently higher rates of oviposition into their preferred host species and adjusted their reproductive allocation to hosts and host patches as a function of their experience in previous patches.     

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.     

Winter survival and oviposition before and after overwintering of a parasitoid wasp, Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae)

Winter survival and oviposition before and after overwintering in Ooencyrtus nezarae, an egg parasitoid of phytophagous heteropterans, were examined in Osaka, Japan. Eggs of Riptortus clavatus parasitized by O. nezarae were kept under natural photoperiod and temperature. When honey was supplied, some female adults emerging from early September to late November overwintered. The percentage of overwintering individuals increased as the date of adult emergence advanced. Most female adults supplied with honey and hosts oviposited soon after emergence, then stopped laying eggs. Female adults emerging in mid‐October and early November laid eggs and then overwintered. The induction of diapause in the field seems to vary greatly depending on host availability. Without honey, the survival time of female adults was very short, whether host eggs were supplied or not. After overwintering, most females began to lay eggs in early May if host eggs were supplied, and they produced both male and female progeny. In the study area, a legume field in Osaka, parasitization by O. nezarae was observed from early July to November.     

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.     

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.     

Does superparasitism improve host suitability for parasitoid development? A case study in the Microplitis rufiventris-Spodoptera littoralis system

Superparasitism refers to the oviposition behavior of parasitoid females who lay their eggs in an already parasitized host. Recent studies have shown that allocation of additional eggs to an already parasitized host may be beneficial under certain conditions. In the present work, mortality of Microplitis rufiventris wasps was significantly influenced by both host instar of Spodoptera littoralis larvae at parasitism and level of parasitism. In single parasitization, all host instars (first through sixth) were not equally suitable. Percentage of emergence success of wasp larvae was very high in parasitized first through third (highly suitable hosts), fell to 60% in the fourth instar (moderate suitable) and sharply decreased in the penultimate (5th) instars (marginally suitable). Singly parasitized sixth (last) instar hosts produced no wasp larvae (entirely unsuitable), pupated and eclosed to apparently normal adult moths. The scenario was different under superparasitism, whereas supernumerary individuals in the highly suitable hosts were almost always killed as first instars, superparasitization in unsuitable hosts (4th through 6th) had significant increase in number of emergence success of wasp larvae. Also, significantly greater number of parasitoid larvae successfully developed in unsuitable hosts containing three wasp eggs than counterparts containing two wasp eggs. Moreover, the development of surplus wasp larvae was siblicidal in earlier instars and nonsiblicidal gregarious one in the penultimate and last “sixth” instars. It is suggested that the optimal way for M. rufiventris to deal with high quality hosts (early instars) is to lay a single egg, while the optimal way to deal with low quality hosts (late instars) might be to superparasitize these hosts.     

Host Stage Selection and Sex Allocation by Gyranusoidea tebygi (Hymenoptera: Encyrtidae), a Parasitoid of the Mango Mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae)

Host stage selection and sex allocation by Gyranusoidea tebygi Noyes (Hym,, Encyrtidae) were studied in choice and no-choice experiments in the laboratory. The parasitoid reproduced on first, second, and third instars of the mango mealybug, Rastrococcus invadens Williams (Hem., Pseudococcidae), and it avoided hosts that were already parasitized. Host feeding was occasionally observed. Sex ratios of the offspring produced by individual wasps were highly biased in favor of females, whereas the sex ratio of groups of wasps foraging under crowded conditions varied from male biased in smaller hosts to female biased in larger hosts. Females had longer developmental times than males, developed faster in larger mealybugs than in smaller ones, and were always larger than males emerging from the same host instar. Their size increased with the instar of the host at oviposition. About 90% of all ovipositions in second and third instar nymphs resulted from an attack with multiple stings, starting with a sting in the head of the host for the most part. The function of these head stings is either to assess quality of the host or to subdue hosts prior to oviposition. Encounter rates, number of attacks, and number of stings during one attack increased, while ovipositions decreased with host instar. Time investment per oviposition and time spent preening increased with increasing host age because older hosts defended themselves more vigorously than younger ones. Thus, while fitness of the parasitoid increased with host size, fitness returns per time decreased. The implications of this host selection behavior for the biological control of the mango mealybug are discussed.     

Effects of host age and host availability on developmental period,adult size,sex ratio,longevity and fecundity inLariophagus distinguendus Förster (Hymenoptera: Pteromalidae)

The effects of host age on parasitoid reproductive capacity are studied using the pteromalid parasitoid Lariophagus distinguendusFörster and its bruchid hosts, Callosobruchus chinensis (L.) and C. maculatus (F.). A series of experiments were performed to investigate relationships between age and size of host parasitized and the developmental period of pre-imaginal progeny, sex ratio, female size, longevity, fecundity and oviposition rate. There was no effect of host size on preimaginal parasitoid developmental period. Sex ratio varied from less than 5% females from young (small) hosts to 60% females from mature (large) hosts. Adult size, female longevity, fecundity, and oviposition rate were also positively related to host age. Females provided mature hosts lived longer than those provided either young hosts or no hosts, possibly because of an increased ability to host-feed from the larger hosts. The implications of these findings to parasitoid population reproductive capacity and host-parasitoid synchrony are discussed.     

Mixed sex allocation strategies in a parasitoid wasp

The sex allocation strategy of the parasitoid Laelius pedatus (Hymenoptera: Bethylidae) on different-sized hosts was investigated. The wasp lays from one to five eggs, and clutch size increases with host size. On the smallest hosts, single male eggs are laid, while on slightly larger hosts single female eggs are laid. On still larger hosts, gregarious clutches are laid which nearly always consist of a single male and one or more female eggs. The sex ratio strategy of the wasp appears to be influenced by a combination of local mate competition and conditional sex expression based on host quality. Received: 6 June 1996 / Accepted: 13 October 1996     

Parasitoid size as a function of host sex: potential for different sex allocation strategies

Parasitoid females are known to preferentially allocate female eggs to hosts with the higher resource value, usually leading to oviposition of female eggs in larger hosts and male eggs in smaller hosts. For koinobiont parasitoids, if male and female hosts are of equal size at time of oviposition, but differ in size in later developmental stages, the sex of the host could be used to indicate future resource value. Using parasitoids of the braconid genus Asobara, which are larval parasitoids of Drosophila, it is shown that parasitoids emerging from female hosts are larger than those from male hosts. Given this difference in resource value, ovipositing females should preferentially allocate female eggs to female hosts. An alternative strategy would be to decrease the difference in resource value between male and female hosts by castrating male hosts. The primary sex ratio of A. tabida in their two main host species does not differ between male and female hosts. In contrast to A. tabida, A. citri is known to partially castrate male hosts, but this does not decrease the size difference between male and female hosts. As in A. tabida, there is no difference in sex allocation to male and female hosts in A. citri. Despite the clear difference between the resource value of male and female hosts, these parasitoid species do not seem to make optimal use of this difference. They may not be able to discriminate between host sexes or, alternatively, there is a presently unknown fitness disadvantage to ovipositing in female hosts.     

Sex allocation and clutch size in the gregarious larval endoparasitoid wasp, Cotesia glomerata

The ability of the gregarious larval endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) to adjust progeny sex ratio and clutch size was investigated. The sex ratios (proportion of males) of field clusters were diverse, but many (70%) were female-biased. Nearly 10% yielded males only, suggesting a low percentage of unmated females in the field. In over half of the clusters containing females, the sex ratio was below 0.3. Superparasitism was common in the field, and females were believed to increase progeny sex ratio when attacking previously-parasitized hosts. However, in a single oviposition bout, sex allocation was not precisely controlled both in the field and laboratory. In the laboratory, the number of eggs laid in a day tended to decrease with increasing female age. For females which were offered two hosts per day and for those offered three hosts per day, this value became nearly the same several days after the start of oviposition. The total number of hosts which a female could parasitize during her lifetime was often less than 40. Some of the old females which attacked more than 40 hosts produced male-biased clutches; this was due to sperm depletion, because sperm remained viable throughout a female's lifetime. The amount of sperm used in a single oviposition bout seemed fixed and was not dependent on the number of eggs laid. Females with much oviposition experience did not produce new eggs to compensate for deposited eggs, and the efficiency of egg use (deposited eggs/total eggs) was more than 80%.     

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.