The effect of temperature on progeny allocation and short interval timing in a parasitoid wasp

Abstract The parasitoid wasp Trichogramma dendrolimi Matsumura sets the number of progeny allocated to its insect egg hosts according to the duration of its initial transit walk across the host surface. Although cooling the wasp reduces its walking speed, reduced temperature does not affect progeny allocation. By locally heating and cooling the wasps, the initial transit can be thermally uncoupled from the subsequent oviposition. Using this technique we show that the timing of initial transit duration is temperature-dependent. These findings suggest that short interval timing by Trichogramma differs physiologically from the temperature compensated clocks that have been described for other insects.     

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.     

Effects of spatio-temporal intervals between newly-hatched larvae on larval survival and development inMonochamus alternatus (Coleoptera: Cerambycidae)

The effects of distance between hatching larvae on survival and development were investigated inMonochamus alternatus. Two newly-hatched larvae were inoculated intoPinus densiflora bolts at a distance of 2.5 cm or 10 cm, simultaneously or at an interval of 2 weeks. Some larvae were inoculated singly as a control. When larvae were inoculated simultaneously, mortality of the closely-inoculated larvae was significantly higher than that of distantly-inoculated larvae. Such high mortality was identified as due to conspecific bites. When the two larvae were inoculated asynchronously, the first-inoculated larvae killed some second-inoculated larvae but were never killed by them. Consequently, mortality was higher in second-inoculated larvae than in first-inoculated larvae. In particular, there was a significant difference in mortality between them when the larvae had been inoculated closely. The mortality of second-inoculated larvae was higher in the closely-inoculated group than in the distantly-inoculated group although there was no significant difference between them. In the case of two simultaneously-inoculated larvae, the initial distance between them had no significant effect on the development and growth in the early larval stage. When the larvae were inoculated asynchronously, the first-inoculated larvae grew more quickly than singly-inoculated control larvae.     

Specificity of systemically released rice stem volatiles on egg parasitoid,Trichogramma japonicum Ashmead behaviour

The yellow stem borer, Scirpophaga incertulas Walker (YSB), infested rice plants emit chemicals through the surface of their infested stems. These induce attractant activity and cause arrestment responses and ovipositional stimulation in its egg parasitoid, Trichogramma japonicum Ashmead. Laboratory experiments on short‐range host searching and oviposition were performed to assess the how these crude stem extracts and their fractions influence the biological control efficiency of Trichogramma. The activity of these chemicals as long‐range attractants was confirmed through wind tunnel bioassays. Stem borer‐infested plant extracts had enhanced the parasitization rate of T. japonicum, whereas host eggs treated with the extract from undamaged stems or solvent‐treated control failed to evoke changes in the parasitoid’s behaviour. A preliminary GC‐MASS analysis indicated the presence of several hydrocarbon compounds. The analysis also revealed qualitative and quantitative differences between the chemical profiles of the infested and non‐infested plants. We hypothesized that herbivore‐induced plant chemicals are released through the stem surfaces and attract T. japonicum, even over long distances. These cues elicit parasitoid arrestment on pest‐damaged plants and subsequently lead to the successful parasitization of the stem borer.     

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.     

Effect of expected offspring survival probability on host selection in a solitary parasitoid

Optimal Foraging Theory predicts that parasitoid females should optimize their host selection to maximize their lifetime fitness gain and parasitize the most profitable hosts. In particular, in solitary parasitoids, females should avoid superparasitism, at least when sufficient unparasitized hosts are available. However, when unparasitized hosts are scarce, they should prefer, among already parasitized hosts, those that provide the best survival probability to their progeny, which depends on the age and the developmental stage of the first parasitoid. To test this hypothesis in a solitary ectoparasitoid, Pachycrepoideus vindemmiae Rondani (Hymenoptera: Pteromalidae), we first assessed the survival probability of a second parasitoid according to the time elapsed since initial parasitism. We then analyzed the female selection behavior in patches containing a mixture of hosts parasitized over various time intervals. Our results showed that the older the opponent larva was, the lower the survival probability of the second parasitoid was. However, when the first individual had reached the prepupal stage, both individuals could complete their development. At this stage, the survival probability of the second parasitoid was surprisingly high but such individuals were reduced in size. Our study also showed that host acceptance by females was strongly correlated with the survival probability of their progeny when the first parasitoid was from 0 to less than 10 days‐old. When the first parasitoid had reached the prepupal stage, females usually rejected these hosts, although the survival probability of the offspring was quite high. This discordance between female host selection behavior and progeny survival probability is discussed.     

Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid

Host age is an important determinant of host acceptance and suitability for egg parasitoids. As host embryonic development advances, the quality of resources available to the parasitoid offspring typically declines, usually resulting in reduced acceptance levels by foraging females and lower offspring fitness. We examined the ability of the parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) to parasitize and develop in Podisus maculiventris (Say) (Hemiptera: Pentatomidae) eggs of different ages. In laboratory experiments, we measured the effect of host age (6, 24, 48, 72, 96, or 120 h old) on parasitism rate and offspring fitness parameters such as survival, development time, sex ratio, and size. Contrary to our expectations, parasitism rate did not differ between host age treatments, nor did sex ratio allocation, offspring size, or the fecundity of newly emerged female offspring. However, parasitoid offspring had a longer development time with increasing host age. This trend was stronger for males than for females, which we suggest could reduce the degree of protandry among offspring emerging from older host eggs, thus increasing the rate of virginity upon leaving the emergence patch and resulting in more frequent off‐patch mating by female offspring in nature. Overall, our results suggest that all stages of P. maculiventris embryonic development are suitable for acceptance and development of T. podisi. Unlike most species of egg parasitoids, T. podisi has evolved mechanisms to utilize host resources, regardless of host developmental stage, with relatively minor fitness consequences.     

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.     

The time and egg budget of Leptopilina clavipes, a parasitoid of larval Drosophila

Abstract.

• 1 For the understanding of the influence of natural selection on the persistence of host selection behaviour in populations of Drosophila parasitoids it is important to know whether parasitoids will become time- or egg-limited. We investigated whether the Drosophila parasitoid Leptopilina clavipes (Hartig) meets egg- or time-limited conditions in the field.
• 2 To this end the following aspects of the parasitoid's life were studied: egg load at emergence, travelling velocity between patches, patch residence times, oviposition rates and life expectancy. Together with the results from earlier studies on host and patch distributions, this formed the input of a ‘Monte Carlo’ simulation model, in which the life history of an individual parasitoid can be traced.
• 3 The simulations revealed that under the conditions found in the field 12.9% of the parasitoid population is egg-limited. The model was also run for a number of scenarios which reflect ‘good’ or ‘bad’ circumstances. In most cases a significant proportion of the parasitoid population proved to be egg-limited.
• 4 For the measurement of travelling velocities and patch residence times a marking method, especially applicable to small-sized parasitoids such as L.clavipes, is described. Marking did not affect survival, host habitat location or host detection rate. Parasitoids were found to be attracted to the odour of fruit-bodies of Phallus impudicus, the most important breeding substrate of their hosts.

     

The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis

1. A series of experiments was conducted to measure the impact of plant genotype, plant growth rate, and intraspecific competition on the oviposition preference and offspring performance of the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and Solidago gigantea (Asteraceae). Previous research has shown that both host races prefer to oviposit on their own host plant where survival is much higher than on the alternate host plant. In this study, neither host race showed any relationship between oviposition preference and offspring performance in choosing among plants of their natal host species. 2. The larval survival of both host races differed among plant genotypes when each host race oviposited on its natal host species. In one experiment, altissima host race females showed a preference among plant genotypes that was not correlated with offspring performance on those genotypes. In all other experiments, neither the altissima nor gigantea host race demonstrated a preference for specific host plant genotypes. 3. Eurosta solidaginis had a preference for ovipositing on rapidly growing ramets in all experiments, however larval survival was not correlated with ramet growth rate at the time of oviposition. 4. Eurosta solidaginis suffered high mortality from intraspecific competition in the early larval stage. There was little evidence, however, that females avoided ovipositing on ramets that had been attacked previously. This led to an aggregated distribution of eggs among ramets and strong intraspecific competition. 5. There was no interaction among plant genotype, plant growth rate, or intraspecific competition in determining oviposition preference or offspring performance.     

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.     

Influence of egg load and host size on host-feeding behaviour of the parasitoid Aphytis lingnanensis

Abstract.

• 1 Direct behavioural assays were used to investigate the influences of host size and parasitoid egg load on the decision to host feed versus oviposit made by the parasitoid Aphytis lingnanensis Compere. Egg load was manipulated without concurrent influences on the history of host contact by exploiting size-related variation in fecundity and by holding parasitoids at different temperatures to vary the rate of oocyte maturation.
• 2 Host feeding comprised a series of feeding bouts, separated by renewed probing of the scale insect body. Successive feeding bouts were progressively shorter, suggesting that hosts represent ‘patches’ yielding resources at a decelerating rate.
• 3 Parasitoids were significantly more likely to host feed on smaller hosts and oviposit on larger hosts.
• 4 Neither egg load nor the treatment variables (parasitoid size and holding temperature) exerted significant influences on the decision to host feed versus oviposit on second instar (low quality) hosts.
• 5 The failure to observe an effect of egg load on host-feeding decisions was not simply a reflection of the parasitoids being entirely insensitive to egg load; significant effects of egg load on parasitoid search intensity and clutch size decisions were observed.
• 6 Parasitoids developing on second instar (low quality) hosts experienced high levels of mortality late during development and yielded very small adults.
• 7 The discord between these experimental results and predictions regarding the importance of egg load underscores the need for additional work on the proximate basis for host-feeding decisions and the nutritional ecology of insect parasitoids.

     

A comparison between the amino acid composition of an egg parasitoid wasp and some of its hosts

Amino acid compositions of the eggs of five lepidopteran hosts for Trichogramma minutum were compared with each other and with a non-host species, Rhodnius prolixus, in which T. minutum oviposits but does not develop. Host eggs are quite homogeneous, particularly when compared according to groupings of potentially interconvertible amino acids. Combined mole percent values for glycine, serine and alanine were higher in hosts (27.5–29.2 mole%) than in R. prolixus eggs (21.5 mole%), in bovine serum albumin (14.9%), which has been used as a protein source in artificial diets for T. minutum, or in many of the mixtures used in published diets for this species. Since these three amino acids make up 26.3 mole% of the adult amino acid content of T. minutum, their deficiency in diets could require metabolic compensation detrimental to development.Adult T. minutum arising from eggs of Manduca sexta, Choristoneura fumiferana, and Sitotroga cerealella are similar in amino acid composition to each other and, in general, to their hosts. Variability appears greater in hosts than in adult wasp composition, suggesting some interconversion of host amino acids to accommodate inflexible nutritional requirements of T. minutum.In the three host species tested, free amino acids constituted 15.8–19.3% by weight of the amino acid in egg contents. In M. sexta eggs, glycine, serine and alanine together make up 28.4% by weight of the total free amino acid, a much higher proportion than in many published diets. The four free amino acids (isoleucine, leucine, phenylalanine and histidine) reported to be oviposition stimulants in experiments on encapsulated diets are present in sufficient concentrations to induce oviposition in the host species tested and in R. prolixus. S. cerealella egg contents having approximately 1.8 g amino acid, yield one or rarely two adult T. minutum (1g amino acid/insect). In contrast, M. sexta eggs with 94 g amino acid each yield an average of 10–12 adults (8.2g amino acid/insect). This suggests that small hosts are allocated few eggs which can only develop into small adults because of nutrient supply (parasitoid size in metabolically restricted), whereas much larger hosts are allocated proportionately fewer eggs than the former resulting in larger, and presumably more viable and fecund, adults (parasitoid size is established behaviourally).     

Host-feeding and oviposition by parasitoids on hosts of different fitness value: Influences of egg load and encounter rate

A dynamic optimization model is presented for the decision to host feed or oviposit on hosts by female parasitoids. Optimal host utilization decisions are compared between two host types with different fitness payoffs for oviposition. The model predicts that hosts of higher fitness value should always be used for oviposition unless the egg load approaches zero. This general prediction is not influenced by levels of host availability or metabolic reserves, the age of the parasitoid, or the magnitude of the fitness difference. An egg-load threshold is predicted above which lower value hosts should be used for oviposition and below which they are used for host feeding. The position of this egg-load threshold is higher when the difference in fitness between host types is larger. The threshold is also higher when overall host availability is high or metabolic reserves for the production of new eggs are low. The threshold for oviposition on low-value hosts decreases to zero near the end of the parasitoid’s life. Under conditions where high-value hosts are rarely encountered compared to low-value hosts, the model predicts that lower value hosts should be accepted for oviposition at a lower egg-load threshold.     

Egg and time limitation mediate an egg protection strategy

The number of mature eggs remaining in the ovaries and the time left for oviposition determine the reproductive decisions of the hyperdiverse guild of insects that require discrete and potentially limiting resources for oviposition (such as seeds, fruits or other insects). A female may run out of eggs before all available oviposition sites are used (egg limitation), or die before using all of her eggs (time limitation). Females are predicted to change clutch size depending on whether eggs or time is the limiting resource. We extend this framework and ask whether the same constraints influence a strategy in which females modify eggs into protective shields. In response to egg parasitism cues, female seed beetles (Mimosestes amicus) lay eggs in vertical groups of 2–4, modifying the top 1–3 eggs into shields in order to protect the bottom egg from attack by parasitoids. We made contrasting predictions of how egg and time limitation would influence egg size and the incidence and level of egg protection. By varying access to seed pods, we manipulated the number of remaining eggs a female had at the time she received a parasitism cue. Although egg size was not affected, our results confirm that egg‐limited females protected fewer eggs and time‐limited females protected more eggs. Female body size explained the number of eggs in a stack rather than host deprivation or the timing of parasitoid exposure. Our results clearly show that host availability relative to female age influences the incidence of egg protection in M. amicus. Furthermore, our study represents a novel use of life history theory to explain patterns in an unusual but compelling defensive behaviour.     

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。     

繁育寄主对三种赤眼蜂个体大小及抱卵量的影响

【目的】繁育寄主及成蜂日龄均会影响赤眼蜂体内的抱卵量,为了解繁育寄主及育出赤眼蜂个体大小与赤眼蜂抱卵量的关系,我们在室内研究了米蛾 Corcyra cephalonica（Stainton）卵和亚洲玉米螟 Ostrinia furnacalis （Güenée）卵作为繁育寄主对3种赤眼蜂雌蜂大小、抱卵量的影响。【方法】在光周期14L:10D、温度25±1℃的室内条件下,以米蛾卵、亚洲玉米螟卵作为繁育寄主,解剖不同日龄（羽化后12-72 h）松毛虫赤眼蜂 Trichogramma dendrolimi Matsumura、玉米螟赤眼蜂Trichogramma ostriniae Pang et Chen以及稻螟赤眼蜂Trichogramma japonicum Ashmead,观察雌蜂抱卵量,测量成蜂的大小,分析雌蜂抱卵量与其日龄、个体大小以及繁育寄主的关系【结果】在羽化后48 h以内,3种蜂的抱卵量随雌蜂日龄的增长而增加。羽化后72 h,除米蛾卵繁育的玉米螟赤眼蜂及玉米螟卵繁育的松毛虫赤眼蜂的抱卵量比羽化后48 h时略高外,其他组合均出现下降。以亚洲玉米螟卵为繁育寄主时的玉米螟赤眼蜂的抱卵量显著高于对应日龄的以米蛾卵为繁育寄主时的抱卵量,而松毛虫赤眼蜂（除羽化后12和24 h外）和稻螟赤眼蜂则相反;以米蛾卵为繁育寄主时,相同日龄的赤眼蜂中,松毛虫赤眼蜂抱卵量最高,稻螟赤眼蜂的抱卵量最低;以亚洲玉米螟卵为繁育寄主时,玉米螟赤眼蜂抱卵量最高,稻螟赤眼蜂抱卵量最低。雌蜂抱卵量与雌蜂个体大小呈线性正相关,相关程度随雌蜂日龄增加而更加明显。【结论】后足胫节长度可以作为评价松毛虫赤眼蜂、玉米螟赤眼蜂和稻螟赤眼蜂质量的指标。赤眼蜂抱卵量受繁育寄主、赤眼蜂蜂种及雌蜂日龄的显著影响,寄主的适合性也会影响育出赤眼蜂的大小,筛选合适的繁育寄主有助于提高赤眼蜂的质量。     

Response of parasitoid egg load to host dynamics and implications for egg load evolution

A theoretical debate about whether parasitoids should be time or egg limited now recognizes both as feasible, and interest has turned to determining the circumstances under which each might arise in the field, and their implications for parasitoid behaviour and evolution. Egg loads of parasitoids sampled from the field are predicted to show a negative response to host availability, but empirical support for this relationship is scarce. We measured how a parasitoid's egg load responded to seasonal fluctuations in host population density and recorded the predicted correlation. In early summer, parasitoids were at high risk of time limitation due to low host availability, and in late summer, their offspring were at greater risk of egg limitation due to high host availability. Despite clear seasonal changes in selection pressures on egg load and lifespan, the parasitoid showed no evidence of seasonal variation in its reproductive strategy. We made minor modifications to a previously published model to explore the effects of seasonal variation in host availability on optimal investments in eggs and lifespan and obtained several new results. In particular, under circumstances analogous to some of those observed in our field study, temporal stochasticity in reproductive opportunities can cause investments in eggs to increase, rather than decrease as previously predicted. Our model results helped to explain the parasitoid's lack of a seasonally varying reproductive strategy. Understanding the evolution of parasitoid egg load would benefit from a shift of research emphasis from purely stochastic variation in parasitoid reproductive opportunities to greater consideration of host dynamics.     

卵液成分改变及卵表涂施引诱剂对玉米螟赤眼蜂产卵发育的影响

试验通过部分改变人造卵卵液成分和在人造卵表涂施引诱剂2种途径来试图提高人造卵繁育玉米螟赤眼蜂Trichogramma ostriniae Panget Chen的成功率。结果表明,不同比例的亚洲玉米螟OstriniafurnacalisGuenée幼虫和蛹匀浆替代部分柞蚕蛹匀浆后,对赤眼蜂寄生率有明显提高,但赤眼蜂在人造卵内的化蛹率和羽化率均较低,赤眼蜂发育至老熟幼虫因卵液过剩而被淹死;在原卵液卵表涂施亚洲玉米螟卵和鳞片正己烷提取液后,评价繁蜂成功率的各项参数都有明显提高,赤眼蜂可以完成发育,羽化成蜂,但繁蜂成功率还较低。综合上述试验结果,应用人造卵繁殖玉米螟赤眼蜂研究重点要解决卵液过剩以及其它相关的营养学问题。