Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect.

In holometabolous insects reproductive success is strongly determined by the nutritional resources available to the females. In addition to nutrients derived from adult feeding, resources for egg production may come from the limited reserves accumulated during the larval stages. The pattern of allocation of these larval reserves to egg production is expected to be strongly linked to the nutritional ecology of the adult. We investigate the temporal pattern of allocation of larval reserves to reproduction in a host-feeding parasitoid wasp. As predicted by the dynamics of allocation of an adult meal, larval reserves are the main source of nutrients for four or five days after emergence. However, despite the high frequency of host feeding and the high nutrient content of a haemolymph meal, which we predicted would lead to larval reserves being conserved in the event of host deprivation, larval reserves contribute to egg production throughout the lifetime of the female. We propose several mechanistic and adaptive explanations for our results, including the possible existence of a limiting or key nutrient for egg production of exclusively larval origin. We make further predictions concerning the pattern of allocation of larval resources in parasitoids with different adult nutritional requirements.     

Lifetime gains of host-feeding in a synovigenic parasitic wasp

Abstract. Understanding behavioural decisions relative to host use for feeding or reproduction by foraging parasitoids requires not only the study of metabolic pathways followed by nutrients, but also the quantification of lifetime fitness gains of each alternative behaviour. By using a combination of observational and manipulative approaches, the lifetime host‐feeding gains are measured both in terms of fecundity and longevity in the parasitoid Eupelmus vuilletti. Host‐feeding increases both egg production and longevity. The increase in fecundity is mainly determined by the amount of lipids obtained whereas the lifespan extension is mainly determined by carbohydrates. Proteins obtained through host‐feeding have been implicated previously in egg production by parasitoids but protein intake has no effect on fecundity and longevity in E. vuilletti. The amount of nutrients gained through host‐feeding and invested in eggs is variable and changes over the lifetime of the animal. Therefore, lifetime feeding gains are best understood through the construction of dynamical budgets running over the entire lifespan of an insect.     

Reproduction now or later: optimal host-handling strategies in the whitefly parasitoid Encarsia formosa

We developed a dynamic state variable model for studying optimal host‐handling strategies in the whitefly parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae). We assumed that (a) the function of host feeding is to gain nutrients that can be matured into eggs, (b) oögenesis is continuous and egg load dependent, (c) parasitoid survival is exponentially distributed and (d) parasitoids encounter hosts randomly, are autogenous and have unlimited access to non‐host food sources to obtain energy for maintenance and activity. The most important prediction of the model is that host feeding is maladaptive under field conditions of low host density (0.015 cm^?2) and short parasitoid life expectancy (maximum reproductive period of 7 d). Nutrients from the immature stage that can be matured into eggs are sufficient to prevent egg limitation. Both host density and parasitoid life expectancy have a positive effect on the optimal host‐feeding ratio. Parasitoids that make random decisions gain on average only 35% (0.015 hosts cm^?2) to 60% (1.5 hosts cm^?2) of the lifetime reproductive success of parasitoids that make optimal decisions, independent of their life expectancy. Parameters that have a large impact on lifetime reproductive success and therefore drive natural selection are parasitoid life expectancy and the survival probability of deposited eggs (independent of host density), the number of host encounters per day (when host density is low) and the egg maturation rate and number of host types (when host density is high). Explaining the evolution of host‐feeding behaviour under field conditions requires field data showing that life expectancy in the field is not as short as we assumed, or may require incorporation of variation in host density. Incorporating variation in walking speed, parasitised host types or egg resorption is not expected to provide an explanation for the evolution of host‐feeding behaviour under field conditions.     

寄生蜂取食寄主特性及其在害虫生物防治中的作用

许多寄生性天敌昆虫的雌虫不仅寄生寄主, 而且还能取食寄主。在卵育型（synovigenic）寄生蜂类群中, 取食寄主行为是较为普遍的现象。本文综合近20年相关研究进展, 从寄生蜂类群、取食类型、生态学意义及影响因子等方面对寄生蜂的取食寄主行为进行了归纳总结。寄生蜂通过取食不仅可以杀死寄主, 直接起到控制害虫种群数量的作用, 还能通过取食策略为卵的成熟和再生提供营养来源, 对延长雌虫的寿命也有一定的帮助。对取食寄主行为的了解可为筛选优势寄生性天敌种类、评估寄生蜂在害虫生物防治中的作用提供重要信息。     

Does synovigeny confer reproductive plasticity upon a parasitoid wasp that is faced with variability in habitat richness?

Understanding the factors that constrain the reproductive success of animals and their demographics requires detailed insight into the processes of resource acquisition and allocation in relation to habitat richness. Parasitoid wasp females are valuable models in this respect because their lifetime reproductive success is closely tied to host availability. Parasitoids that manufacture eggs throughout adult life (i.e. ‘synovigenic’ species) and characteristically acquire nutrients via feeding are predicted to be plastic in their allocation to egg manufacture. Using the synovigenic parasitoid wasp Venturia canescens, we tested whether this prediction holds when females are faced with variation in the availability of both hosts and food. Laboratory experiments were conducted to determine how environmental variation affects parasitoid reproductive success and the lifetime dynamics of egg load and of major nutrient types. Our results, surprisingly, show that female V. canescens lacks a significant degree of reproductive plasticity under our experimental conditions. In particular, allocation of resources to reproduction was high irrespective of host availability. We attribute this lack of flexibility to the low energy content of V. canescens' eggs and to features peculiar to the ecology of this species. Our findings shed new light on the physiological factors that constrain parasitoid lifetime reproductive success. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 621–632.     

Host-feeding strategies of parasitoid wasps

Summary Three models of the evolution of host-feeding behaviour in parasitoid wasps are developed. The first assumes that the wasp host feeds purely to obtain resources to mature eggs (limited resource model) while the second assumes that host feeding provides energy for maintenance (pro-ovigenic model). The third model assumes that host feeding provides resources for both maintenance and egg maturation (resource pool model). Two variants of the third model are examined: the first assumes that the risk of mortality is constant and state-independent, the second that resource-depleted individuals suffer a higher risk of mortality. The models are analysed using a combination of stochastic dynamic programming and analytical techniques. The models make different predictions about the relationships between the probability of host feeding and egg load and host density. The available experimental evidence best supports the resource pool model.     

THE RELATIVE CONTRIBUTIONS OF TIME AND EGGS TO THE COST OF REPRODUCTION

Whether the trade-off between current and future reproduction in insect parasitoids is mediated by the costs of time or eggs remains an issue of contention. Life-history models predict that parasitoids have some risk of exhausting their lifetime supply of oocytes. I develop a simple conceptual model that assesses the relative contributions of time and eggs to the cost of reproduction by placing them in a common currency: foregone future fitness returns. Although rates of egg limitation observed in nature are modest, eggs still often make the dominant contribution to the overall cost of oviposition. Therefore, models of parasitoid reproduction must recognize the costliness of both time and eggs.     

Importance of sterols acquired through host feeding in synovigenic parasitoid oogenesis

Eupelmus vuilleti (Hymenoptera; Eupelmidae) is a host feeding ectoparasitoid of fourth-instar larvae or pupae of Callosobruchus maculatus (Coleoptera; Bruchidae) infecting Vigna unguiculata seed and pods (Fabacae). Parasitoid females are synovigenic, i.e. they are born with immature eggs and need to feed from the host in order to sustain egg production. In this study, the role of sterols obtained through host feeding in parasitoid oogenesis are examined. Quantitative and qualitative analyses of the sterol contents in each partner of the tritrophic interaction show that a parasitoid female's larval sterol contents is sufficient to produce only 30% of the total number of eggs laid throughout a female's life cycle. In a second step, by manipulating the composition of the sterols hemolymph in the host, it is shown that cholesterol obtained through adult nutrition plays a crucial role in the eggs viability but does not affect the egg production quantitatively. This result has important implications for understanding both the nutrient allocation strategy in this species and the impact of cholesterol in parasitoid reproduction.     

Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field

We used field observations of freely foraging Aphytis aonidiae parasitoids in conjunction with results of laboratory studies of A. aonidiae and other Aphytis species to simulate lifetime patterns of behavior and reproduction. Field observations provided estimates of encounter rates with three classes of hosts, the mortality rate from predation on adult parasitoids, and host-handling times for oviposition and host feeding by adult wasps. A series of physiological parameters, including the egg maturation rate and the value of host-feeding meals, were estimated from previously published studies. Plasticity in parasitoid behavior was incorporated in two ways. For one set of simulations we used a behavioral rule derived empirically from observations of parasitoids made in the field, and for another we used a dynamic state-variable model to generate a set of behavioral rules that maximize lifetime reproductive success. As was expected, the empirically derived rule led to better matches with field observations than did simulations using the output of the dynamic model. Projections of lifetime reproductive success in the field ranged between three and 37 eggs within the 95% confidence intervals of the mortality rate and host encounter rate and depending on which behavioral rule was used. Lifetime reproductive success from the simulation with central estimates of the mortality and host encounter rates that incorporated the empirical rule was 6.25 eggs. Using the empirical versus the theoretical rule in the simulations led to a 10%-30% decline in projections of lifetime reproductive success, depending on mortality and host encounter rates. Regardless of the behavioral rule, the simulations underscored the observation that the host encounter rate was greater than the egg maturation rate. The overall oviposition rate was sufficiently high to lead to daily episodes of temporary egg limitation during which parasitoids must mature an egg before being able to oviposit.     

Dynamic egg maturation strategies in an aphid parasitoid

Abstract.  Females of the parasitoid Aphelinus albipodus both lay more eggs on younger stages of their aphid host, Aphis glycines , and contain more mature eggs in their ovaries when held with these younger host stages. This suggests that egg maturation is more rapid in the presence of younger host stages. Three factors explaining the difference in the egg loads of A. albipodus females exposed to various host stages are examined. These are (i) the number of host-feeding meals; (ii) the number of eggs laid; and (iii) the host stage utilized. Together, these factors explain 69% of the variance in A. albipodus egg load. The number of host-feeding meals taken by females is a strong predictor of egg load. More host meals are taken on young hosts, suggesting that host feeding contributes to the trend of faster egg maturation in the presence of younger hosts. Host stage has a strong impact on egg load even when the effect of host feeding is accounted for. There is no evidence for an effect of the oviposition rate on egg load. The results indicate that egg maturation by A. albipodus is dynamic; females mature eggs faster when in the presence of preferred hosts. It is hypothesized that this allows A. albipodus females to more closely match their reproductive effort to reproductive opportunities.     

Effect of temperature on parasitism and host-feeding of Trichogramma turkestanica (Hymenoptera: Trichogrammatidae) on Ephestia kuehniella (Lepidoptera: Pyralidae)

The egg parasitoid Trichogramma turkestanica Meyer is being evaluated as a biological control agent against the Mediterranean flour moth, Ephestia kuehniella Zeller, in flour mills. The longevity, parasitism and host-feeding of the parasitoid at four constant temperatures (15-30 degrees C) has been determined in the laboratory. The highest fecundity occurred at intermediate temperatures. The number of host eggs killed by host-feeding per female was highest at the two lower temperatures. A very conservative estimate of host-feeding showed that it accounts for approximately half of the mortality of host eggs at 20 and 25 degrees C and thus could constitute a major mortality factor for the flour moth population.     

Host-feeding and oviposition strategies of parasitoids in relation to host stage

Until now, mathematical models of parasitoid-host interactions have not incorporated the tendency for destructively host-feeding parasitoids to partition their feeding and oviposition behaviour in relation to different host stages. A literature survey reveals a trend for female parasitoids to feed preferentially or exclusively on earlier host stages and to oviposit preferentially or exclusively in/or later ones. We explore the relative advantages to host-feeding parasitoids of a number of possible host stage selection strategies. We develop hypotheses, formalizing and testing them using modifications to our earlier simulation model of host-feeding strategies (Jervis and Kidd, 1986). We conclude from our modelling that the advantage to be gained from feeding on early host stages and ovipositing in late ones is likely to be associated with: 1) reduced handling times when feeding on early stage hosts; 2) reduced wastage of progeny from mortality factors other than host-feeding by the parent parasitoid, achieved by confining oviposition to late host stages; and 3) reduced probability of progeny mortality resulting from the parent's host-feeding activities.     

Adult feeding and lifetime reproductive success in the parasitoid Aphytis melinus

The diet of adult females of the parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) includes host insects and sugar-rich foods such as nectar and honeydew. We compared the contributions of host feeding to longevity and fecundity in A. melinus females in the presence and in the absence of honey meals. First, we assessed the longevity of females that were not allowed to oviposit. While the longevity of females fed honey was significantly increased by host feeding (median ages were 30.5 days for host-fed females and 17 days for females not allowed to host feed), the lifespan of parasitoids not fed honey did not exceed 3 days for any individual and there was no effect of host feeding on longevity in this group. In the second set of experiments, we assessed the fecundity and longevity of females allowed to oviposit. We conducted two experiments, one in which honey was continuously available, and one in which honey was not available. In both experiments, daily observations were made of females that were either allowed to host feed or manually prevented from host feeding. In the presence of honey, host feeding significantly increased both fecundity and longevity, and in the absence of honey, parasitoids died within 2 days and host feeding had no significant effect on either fecundity or longevity. The lifetime fecundity of females fed honey but not hosts exceeded the initial egg complement by 60% on average. Approximately one host per day was used for host feeding whether honey was supplied or not, and each host-feeding meal contributed approximately 3.9 eggs to the lifetime fecundity of honey-fed females. In the last experiment, we compared the rate of egg resorption over a 36-h period in A. melinus females that were deprived of hosts and either fed honey or starved. While no egg resorption was detected in honey-fed females over this time period, starved females resorbed approximately 9 eggs. Thus, the availability of a sugar-rich food interacts strongly with host feeding in influencing longevity and fecundity and has a strong direct effect on egg resorption.     

Could hosts considered as low quality for egg-laying be considered as high quality for host-feeding?

When parasitoid females encounter a host, they can either lay an egg and thus invest in current reproduction or feed on the host and thus invest in future reproduction. However, hosts could have different values according to their parasitized status. Whereas already parasitized hosts represent poor quality for egg-laying, they could have a high nutritive value for feeding. Moreover, the optimal strategy adopted generally depends on the females’ physiological state. In this study, the impact of the females’ physiological state on their reproductive strategies was investigated in the solitary parasitoid Anisopteromalus calandrae. We analysed how their age and diet influenced (i) the use of hosts (feeding vs. oviposition) and (ii) host selection (previously parasitized vs. unparasitized). Our results show that both age and diet influence the reproductive strategy of A. calandrae females: old females fed with the poorer diet laid fewer eggs and made more host-feeding than others. Females also showed a preference for already parasitized hosts for feeding. This strategy cannot be explained by the nutritive value of haemolymph, as parasitized hosts carry fewer lipids. However, as parasitized hosts are also paralyzed, it could be less costly to feed on them than on unparasitized hosts.     

Host-feeding and acceptance by a parasitic wasp (Hymenoptera: Ichneumonidae) as influenced by egg load and experience in a patch

Optimal host selection models based on dynamic programming predict that the physiological state of a foraging insect, i.e. egg load, energy reserves etc., influences behavioral decisions. To test this prediction, the effect of physiological state on host acceptance of the ectoparasitic wasp Agrothereutes lanceolatus was investigated. Female wasps in plastic cups (regarded as patches) were presented with hosts, and their responses to the hosts were continuously observed. After observations, the wasps were dissected and the number of mature and immature eggs they carried were counted. The results showed that behavioral decisions by the female wasps were influenced by mature egg load, but not by wasp size or immature egg load. Hence the wasps with higher egg loads were more likely to oviposit. The number of hosts previously encountered in a patch (i.e. wasp experience) also had an independent effect on females' host acceptance, indicating that female informational state was updated during foraging in that patch. Female wasps host-fed only when mature egg load approached zero. Concurrent host-feeding was not observed. Parasitoid survival was almost zero when parasitoid eggs were transferred onto hosts that were fed upon, indicating that concurrent host-feeding could cause a high degree of offspring mortality. These three results supported the assumption and prediction of optimal host-feeding models. Parasitoid host selection and host-feeding are discussed in the context of recent models.     

A simple model of host-parasitoid interaction with host-feeding

Summary A simple mathematical model of host-parasitoid interaction with host-feeding was presented with special reference to the system of the greenhouse whitefly and the parasitoidEncarsia formosa. In the model, when a parasitoid encounters a host, it has a choice between feeding the host and ovipositing one egg in the host. It was shown that an intermediate value of the feeding ratio of all attacks gives the minimum equilibrium host density and the minimum amplitudes of fluctuation in the densities of the two species. Computer simulations of a modified model with time lags also gave the similar results. The model suggested for natural enemy introduction program that parasitoid species with host-feeding habits are promising agents for effective controls for pest insects and that the timing of introduction is very important. By an evolutionary analysis, it was shown that the feeding ratio evolves to minimize the host density under natural selection among parasitoids.     

Egg maturation, egg resorption and the costliness of transient egg limitation in insects

Although there is widespread agreement that the cost of oviposition underlies selective oviposition in insects, there is no consensus regarding which factors mediate the cost of oviposition. Models have suggested that egg costs are often paramount in those insects that do not continue to mature eggs during the adult stage (pro-ovigenic insects). Here we address the hypothesis that egg costs are generally less significant in synovigenic insects, which can replenish oocyte supplies through continuous egg maturation. A dynamic optimization model based on the biology of a highly synovigenic parasitoid, Aphytis aonidiae, suggests that the maximum rate of egg maturation is insufficient to balance the depletion of eggs when opportunities to oviposit are abundant. Transient egg limitation therefore occurs, which imposes opportunity costs on reproducing females. Thus, whereas the most fundamental constraint acting on the lifetime reproductive success of pro-ovigenic species is the fixed total number of eggs that they carry at eclosion, the most fundamental constraint acting on a synovigenic species is the maximum rate of oocyte maturation. Furthermore, the ability of synovigenic species to reverse the flow of nutrients from the soma to oocytes (i.e. egg resorption) has a dramatic influence on the cost of oviposition. Whereas females in hostrich environments may experience oviposition-mediated egg limitation, females in host-poor environments may experience oosorption-mediated egg limitation. Both forms of egg limitation are costly. Contrary to initial expectations, the flexibility of resource allocation that typifies synovigenic reproduction actually appears to broaden the range of conditions under which costly egg limitation occurs. Egg costs appear to be fundamental in mediating the trade-off between current and future reproduction, and therefore are an important factor favouring selective insect oviposition.     

The effect of ovariectomy on reproductive behaviour and physiology of adult female ring-legged earwigs, Euborellia annulipes

The effect of ovariectomy on feeding, mating, Juvenile Hormone (JH) production, and maternal behaviour was assessed in female ring-legged earwigs, Euborellia annulipes (Lucas) (Dermaptera: Carcinophoridae), during the first 16 days of adult life (the first gonadotrophic cycle and early brooding). Ovariectomy of 2-day-old adults did not affect weight gain, nor did it alter mating behaviour on day 7. Similarly, ovariectomy did not prevent the increase in JH biosynthesis that accompanies vitellogenesis in this species, which suggests a cycle of JH production that is not dependent on the presence of the ovaries. Both ovariectomy and mating status affected feeding behaviour. Most introduced eggs were consumed (i.e. disappeared) within 24 h, and younger (7-day-old) females consumed more eggs than did older ones. However, 12-day-old intact virgins and 16-day-old ovariectomized, mated females consumed fewest eggs, and allowed some hatching. Thus, ovariectomy did not abolish changes in feeding behaviour that normally accompany reproduction but, instead, appeared to delay the reduction in feeding that normally accompanies the completion of the cycle of egg development. By contrast, mating enhanced the reduction in feeding late in the reproductive cycle. Mating significantly enhanced maternal behaviour in both ovariectomized and sham-operated females. Hatching success from egg clutches introduced to day 16 virgin or mated females that had been ovariectomized or sham-operated on day 2, was significantly greater in the mated groups.     

Linking reproductive and feeding strategies in the parasitoid Ibalia leucospoides: does feeding always imply profit?

Resource acquisition and allocation to different biological functions over the course of life have strong implications for animal reproductive success. Animals can experience different environmental conditions during their lifetime, and this may play an important role in shaping their life-history and resource allocation strategies. In this study we investigate larval and adult resource allocation to reproductive and survival functions in the parasitoid wasp Ibalia leucospoides (family Ibaliidae). The pattern of larval resource allocation was inferred from the relationship between adult body size and ovigeny index (OI; a relative measure of investment in early reproduction determined as the ratio between the initial egg load and the potential lifetime fecundity); and adult resource allocation was explored through the influence of adult feeding on reproduction, maintenance and metabolism, in laboratory experiments. Food acquisition by this parasitoid in the wild was also examined. The relationship between size and OI was constant, suggesting no differential resource allocation to initial egg load and potential lifetime fecundity with size. This finding is in line with that predicted by adaptive models for the proovigenic egg maturation strategy (OI = 1). Despite of this, I. leucospoides showed a high OI of 0.77, which places this species among the weakly synovigenic ones (OI < 1). Adult feeding had no effect on post-emergence egg maturation. However, wasps extended their lifespan through feeding albeit only when food was provided ad libitum. Although the information we obtained on the feeding behaviour of free-foraging wasps is limited, our results suggest that food intake in the wild, while possible, may not be frequent in this parasitoid. We discuss the results relative to the environmental factors, such as reproductive opportunities and food availability, which may have driven the evolution of larval and adult pattern of resource allocation in parasitoids.     

Life history parameters of the microtype parasitoid fly Pales pavida (Diptera: Tachinidae), and effects of host age and number of eggs ingested by host on parasitism success

With the aim of developing better procedures for rearing the microtype tachinid fly Pales pavida (Meigen), we performed ecological studies in the laboratory using the natural host Mythimna separata (Walker), investigating larval development, mating behaviour, individual oviposition patterns and relationships between parasitisation and number of eggs ingested (NEI) per host. The host instar at the time of parasitoid egg ingestion significantly affected the development time of the immature parasitoid: development took longer when the hosts ingested eggs when at the fifth instar than at the sixth (last) instar. There was no difficulty obtaining mated females in the laboratory when day 0–1 female flies were kept with day 2–4 males. Mean lifetime fecundity was 5805?±?568 eggs per female. Daily rates of oviposition by individual females varied widely; the greatest number of eggs laid in a day was exactly 1700. When the NEI by day 1 fifth instars or day 0 or 3 last instars was 1, 3, 6 or 10, the parasitisation percentage tended to increase with increasing NEI, although it did not differ significantly between NEI 6 and 10. Therefore, the percentage adult emergence per egg ingested decreased from NEI 6 to 10, particularly in the case of last instars. Using day 0 last instars, with six eggs ingested per host, should increase parasitisation rates and shorten the development time of the parasitoid for rearing.