PHENOTYPIC SELECTION BY PARASITOIDS ON THE TIMING OF LIFE HISTORY IN A LEAFMINING MOTH

Direct measurements of phenotypic selection by parasitoids on quantitative traits in herbivorous insects have been rare. I analysed episodes of phenotypic selection on the timing of life-history events in a multivoltine leafmining moth, Phyllonorycter mespilella, and assessed the importance of hymenopterous parasitoids as selective influences. Phyllonorycter mespilella has two consecutive stages of larval development, the sap-feeding (SF) and tissue-feeding (TF) stages. Adult parasitoids host feed predominantly on SF larvae, and oviposit predominantly on TF larvae. Oviposition attack on TF larvae caused positive directional selection on the date of transition to the the TF stage (TF date) in the third generation of P. mespilella in one population in 1991. Overwinter mortality caused negative directional selection on TF date in the third generation in a second population in 1993. No directional or variance selection on TF date was detected in the second population in the second generation of 1993. Parasitoid females accepted SF larvae for oviposition more often in the fall generation than in summer generations in both populations. The relative frequencies of SF and TF larvae may alter the pattern of oviposition attack by parasitoids, and thus the form of phenotypic selection on TF date.     

Evolution of life-history timing in a leafmining moth: Phenotypic selection in patches with manipulated development time

Phyllonorycter mespilella (Hübner) is a leafmining moth with two stages of larval development: the initial sap-feeding (SF) stage followed by the tissue-feeding (TF) stage. Phenotypic selection by parasitoids on the duration of the SF stage (SF duration) was measured in artificial patches of larvae placed in the field during the diapausing generation. Pretreatment of larvae with different photoperiods allowed creation of patches that varied in the time-course of appearance of TF larvae. The shorter the photoperiod pretreatment, the sooner TF larvae tended to appear. Some patches were left exposed and others were caged to exclude parasitoids. Positive directional selection on SF duration was detected in exposed patches, and no selection was detected in caged patches. Directional selection in exposed patches was caused by both parasitoid oviposition and other unidentified sources of mortality. The other sources of mortality may have included host feeding by parasitoids on TF larvae. A larger proportion of parasitoid eggs were oviposited on TF larvae in patches where TF larvae appeared the earliest, but this variation in parasitoid oviposition did not result in significant differences in directional selection intensity among patches with early, intermediate and late appearance of TF larvae. Although the general form of the fitness function was very similar when compared among patch types, no significant directional selection could be detected in patches where TF larvae appeared late, and the causes of directional selection appeared to vary between patches where TF larvae appeared at early and intermediate dates.     

Host-feeding and oviposition by parasitoids in relation to host stage: Consequences for parasitoid-host population dynamics

Among parasitoids which host-feed destructively, there is a tendency for females to partition their feeding and oviposition behaviour in relation to different host stages, feeding preferentially or exclusively on earlier host stages and ovipositing preferentially or exclusively in (or on) later ones. We explored the dynamic implications of this behaviour for parasitoid-host population dynamics, using modifications of the age-structured simulation models of Kidd and Jervis (1989, 1991). Using the new versions of the models, we compared the situation where parasitoids practice host stage discrimination with respect to feeding and oviposition, with the situation where they do not. Additionally, we examined the effects of host stage discrimination on populations by (a) having generations either discrete or overlapping, (b) varying initial age structure, (c) having varying degrees of density dependence acting on host adult mortality, and (d) varying parasitoid develoment times in relation to the length of host development. With either discrete or overlapping generations of the host population, a reduction in the parasitoid development time had a destabilizing influence on the parasitoid-host population interaction. With discrete generations stage discrimination had no effect on the risk of extinction, irrespective of either the degree of density dependence acting on the host population, or the initial age structure of the host population. When parasitoid search was uncoupled from the insect's adult energy requirements, the interaction was always unstable. With continuous generations, stage discrimination affected stability at certain parasitoid development times, but not at others. The relative lengths of parasitoid and host development times also influenced the tendency of the host population to show discrete or overlapping generations.     

Interaction of a solitary larval endoparasitoid, Microplitis mediator, with its host, Mamestra brassicae: host acceptance and host suitability

Abstract:  Microplitis mediator (Haliday) (Hym., Braconidae) is an important parasitoid of early instar larvae of the European cabbage moth, Mamestra brassicae L. (Lep., Noctuidae). In the laboratory, we examined attack responses of female M. mediator to the first three larval instars of M. brassicae . Females were presented with M. brassicae larvae either one individual at a time in a no-choice experiment, or three individuals, one from each instar, simultaneously in a choice experiment. Whether or not there was choice, naïve female parasitoids attacked a high proportion of larvae and did not discriminate among instars. In the no-choice experiment, attacked larvae were reared, and parasitoid cocoons were produced from about 76% of larvae attacked as first and second instars, but from only 19% of larvae attacked as third instars. Dissections of attacked larvae from the choice experiment showed that about 79% of attacks on first and second instars resulted in oviposition compared with only 49% for third instars. When given choice, frequency and number of attacks on first instar larvae increased with increasing parasitoid experience. Our results suggest that first and second instar larvae of M. brassicae are suitable hosts for M. mediator , but that third instar larvae are suboptimal both because oviposition attempts were frequently unsuccessful and because immature parasitoids failed to complete development. Nevertheless, naïve attacking parasitoids exhibited minimal discrimination among instars, although experienced parasitoids most frequently attacked first instar larvae. The host selection behaviour of M. mediator is discussed in the context of optimal foraging theory and implications for biological control.     

Effects of Bacillus thuringiensis on Adults of Cotesia plutellae (Hymenoptera: Braconidae), a Parasitoid of the Diamondback Moth, Plutella xylostella (Lepidoptera: Plutellidae)

To complement existing information on the mortality of larvae of the wasp Cotesia plutellae attacking moth caterpillars infected with Bacillus thuringiensis (Bt) we tested the direct and indirect effects of the bacterium on adult wasp longevity and oviposition behaviour. In one experiment with female parasitoids, mean longevity (SEM) was not significantly different between females exposed to Bt (1.98 +/- 0.08 days) and those not exposed (2.18 +/- 0.13 days). In a second experiment with both males and females, Bt treatment did not significantly effect either male or female parasitoids exposed to Bt. To observe the possible effects of Bt on oviposition behaviour of C. plutellae each of 10 females were given five larvae that had been treated with Bt and five untreated larvae at the same time. All parasitoids were observed to make oviposition attempts in both untreated and treated larvae. Upon dissection of the host larvae, one or more C. plutellae eggs were found in each of the larvae in which a parasitoid attempted oviposition. There was no effect of Bt treatment on parasitoid oviposition. The mean number of ovipositions in treated larvae (4.3 +/- 0.3) was not significantly different from untreated larvae (4.7 +/- 0.2).     

Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies

Abstract.  1. Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Most parasitoid species have evolved specific adaptations to exploit a single host stage. However, females of the aphid hyperparasitoid Syrphophagous aphidivorus (Mayr) (Hymenoptera: Encyrtidae) display a unique and atypical oviposition behaviour by attacking either primary parasitoid larvae in live aphids, or parasitoid pupae in dead, mummified aphids.
2. In the laboratory, the correlation between host suitability and host preference of S. aphidivorus on the host Aphidius nigripes Ashmead parasitising the aphid Macrosiphum euphorbiae (Thomas) was investigated.
3. The relative suitability of the two host stages was determined by measuring hyperparasitoid fitness parameters (survival, development time, fecundity, sex ratio, and adult size of progeny), and calculating the intrinsic rate of population increase ( r _m). Host preference by S. aphidivorus females and the influence of aphid defence behaviour on host selection was also examined.
4. Hyperparasitoid offspring performance was highest when developing from hosts in aphid mummies and females consistently preferred this host to hosts in parasitised aphids. Although aphid defensive behaviour may influence host selection, it was not a determining factor. Ecological and evolutionary processes that might have led to dual oviposition behaviour in S. aphidivorus are discussed.     

Regulation of host diapause by an insect parasitoid

Abstract. 1. The interaction between larval development and parasitism by the braconid wasp Cotesia koebelei (Riley), was investigated in a population of the butterfly Euphydryas editha (Boisduval) (Nymphalidae). In this population, the butterfly host has an obligatory overwintering larval diapause.
2. It was found that E. editha larvae harbouring parasitoids were more likely to pass through an extra feeding instar before entering diapause than were non-parasitized conspecifics.
3. In addition, some individuals that were experimentally exposed to multiple parasitoid attacks bypassed diapause completely; these larvae passed through five or six feeding instars, reaching sizes typical of final instar post-diapause larvae.
4. The observed effect of superparasitism occurred regardless of whether the host larvae subsequently produced mature parasitoids, suggesting that parasitoid attack is sufficient to invoke the response.
5. It is proposed that the parasitoid C.koebelei regulates the number of pre-diapause feeding instars of its insect host E. editha, and that some component of the female venom, injected at oviposition, is responsible for this regulation.     

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.     

螟蛉盘绒茧蜂的过寄生行为及其对子代生长发育的影响

【目的】过寄生现象普遍存在于寄生蜂寄生过程中。本研究旨在探究螟蛉盘绒茧蜂Cotesia ruficrus的过寄生对子代发育的影响及影响过寄生行为的主要因素。【方法】室内研究了螟蛉盘绒茧蜂在其寄主稻纵卷叶螟Cnaphalocrocis medinalis3龄幼虫上过寄生行为的发生,不同产卵次数对寄主存活及子代蜂生长发育的影响,研究了不同接蜂时间和不同接蜂密度对过寄生发生的影响。【结果】螟蛉盘绒茧蜂存在过寄生行为,无论雌蜂有无产卵寄生经历,均能在被自身寄生过和同种不同个体寄生过的寄主内产卵。寄生蜂茧量随着被产卵次数的增加而增加,被产卵3~5次的寄主体内死亡的寄生蜂幼虫数随着增大。寄主在育出蜂前的死亡率随着被产卵寄生次数的增加而增加,被产卵5次时,寄主育出蜂前死亡率达50%。过寄生使螟蛉盘绒茧蜂子代蜂卵-蛹的历期延长,羽化率和雌雄性比下降,雌蜂体型随寄生次数的增加显著变小。过寄生率随着接蜂密度及接蜂时间的增加而增加。【结论】在寄主上产卵2次对螟蛉盘绒茧蜂子代发育是最适合的,产卵3次及以上为过寄生。过寄生使蜂子代发育适合度降低,不利于子代生长发育。在室内大量繁殖螟蛉盘绒茧蜂时,应减少接蜂密度和接蜂时间,从而减少过寄生的发生。     

Comparing and contrasting life history variation in four aphid hyperparasitoids

1. In primary parasitoids, significant differences in life history and reproductive traits are observed among parasitoids attacking different stages of the same host species. Much less is known about hyperparasitoids, which attack different stages of primary parasitoids. 2. Parasitoids exploit hosts in two different ways. Koinobionts attack hosts that continue feeding and growing during parasitism, whereas idiobionts paralyse hosts before oviposition or attack non‐growing host stages, e.g. eggs or pupae. 3. Koino‐/idiobiosis in primary parasitoids are often associated with different expression of life history trade‐offs, e.g. endo‐ versus ectoparasitism, high versus low fecundity and short versus long life span. 4. In the present study, life history parameters of two koinobiont endoparasitic species (Alloxysta victrix; Syrphophagus aphidivorus), and two idiobiont ectoparasitic species (Asaphes suspensus; Dendrocerus carpenteri) of aphid hyperparasitoids were compared. These hyperparasitoids attack either the parasitoid larva in the aphid before it is killed and mummified by the primary parasitoid or the parasitoid prepupa or pupa in the dead aphid mummy. 5. There was considerable variation in reproductive success and longevity in the four species. The idiobiont A. suspensus produced the most progeny by far and had the longest lifespan. In contrast, the koinobiont A. victrix had the lowest fecundity. Other developments and life history parameters in the different species were variable. 6. The present results reveal that there was significant overlap in life history and reproductive traits among hyperparasitoid koinobionts and idiobionts, even when attacking the same host species, suggesting that selection for expression of these traits is largely association specific.     

Active defence of herbivorous hosts against parasitism: Adult parasitoid mortality risk involved in attacking a concealed stemboring host

Phytophagous insects have several defence strategies to defend themselves against attack by parasitic wasps. Larval lepidopteran hosts can defend themselves actively to prevent oviposition by the parasitoid. Among the aggressive kinds of behaviour exhibited by hosts against parasitoids are violent wriggling, biting and spitting. The behaviour of the braconid parasitoid Cotesia sesamiae attacking stemboring larvae inside their feeding tunnel in the plant stem was investigated in maize and sugarcane stem pieces and transparent artificial tunnels. Attacking a defending stemborer host inside the confined space of a tunnel was shown to be risky for the female parasitoid. A considerable proportion (25%) of female wasps were killed in their attempt to attack the spitting and biting host. No difference was found in the behaviour of C. sesamiae attacking the suitable host Sesamia calamistis or the unsuitable host Eldana saccharina. The consequences of this high mortality risk involved in each host attack is discussed in relation to the ecology of the parasitoid.     

The role of volatiles from cruciferous plants and pre-flight experience in the foraging behaviour of the specialist parasitoid Cotesia plutellae

The braconid Cotesia plutellae is an important larval parasitoid of the diamondback moth (Plutella xylostella), a major pest of crucifers in the tropics and sub-tropics. The in-flight searching behaviour of C. plutellae was investigated in a wind tunnel and the close-range attack behaviour observed in cages. The relative importance of volatile stimuli emanating from the plant-host-complex, oilseed rape (Brassica napus) – P. xylostella, in the long-range attraction of C. plutellae was investigated. Plants that were mechanically damaged, or damaged by P. xylostella larvae, were attractive to the parasitoid. Host-damaged leaves remained attractive to the parasitoid after removal of the host larvae. These results indicate that C. plutellae predominantly uses plant derived stimuli in its in-flight searching behaviour. An oviposition experience or contact with a host-damaged leaf prior to the bioassay significantly increased the response to these volatile cues. The foraging behaviour of C. plutellae is compared with other braconid larval parasitoids attacking lepidopteran hosts on crucifers.     

Egg allocation by Bracon hylobii Ratz., the principal parasitoid of the large pine weevil (Hylobius abietis L.), and implications for host suppression

1 The braconid parasitoid Bracon hylobii Ratz. is one of the few specialist natural enemies of the large pine weevil, Hylobius abietis L., a destructive pest of conifer transplants. An assessment of its role as an agent of biological control requires a detailed knowledge of the allocation of its reproductive effort. 2 Parasitoid females were continuously observed in laboratory culture with individually reared host larvae in bark discs. The outcome of sequential parasitoid–host encounters was recorded by subsequent examination of hosts and by rearing all parasitoids. 3 Parasitoids avoided ovipositing on host larvae < 100 mg fresh weight, even though such larvae represented sufficient biomass for complete parasitoid development. All larger larvae were vulnerable to attack, which leaves a window of vulnerability for parasitoids of about 90% of weevil larval life. 4 Parasitoids presented with a range of host sizes showed no preference above 100 mg for the size of host first attacked, but allocated more eggs and a greater total handling time to larger hosts. 5 Most eggs were deposited on the first host attacked, with progressively fewer allocated to subsequent hosts. However, oviposition experience did not affect the time spent on the next host. 6 From these results it is anticipated that when weevil larval size is reduced by less favourable feeding substrates, fewer parasitoid eggs will be allocated to each but more host larvae will ultimately be attacked. 7 Generation time, host finding, oviposition rate, clutch size, life expectancy and diapause induction are strongly affected by temperature. Life expectancy is substantially shorter for parasitoids deprived of non‐host food supplement. At 15 and 20 °C the number of hosts attacked and the number of eggs deposited decreased with female age. 8 Bracon hylobii is inevitably poorly synchronized with a variable life‐cycle host; it is egg‐limited and can enter diapause at a relatively high field temperature. None of these characteristics suggest that it could stabilize the abundance of its host below an economically acceptable threshold density. However, the reproductive potential of the parasitoid suggests that it could make a significant contribution to larval mortality and suppress adult recruitment, thus complementing other control strategies.     

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 parasitism on wing development in male and female pea aphids

Wing formation in presumptive alate morphs (virginoparae and males) was observed for the pea aphid, Acyrthosiphon pisum, exposed to attack by the parasitoid, Aphidius ervi, at different stages of host development. Morphological abnormalities in parasitized aphids such as complete apterization (development of a wingless form), formation of rudimentary wing buds, and deformed wings indicate a possible disruption of the endocrine system. Changes in the body shape and the number of olfactory secondary rhinaria on the antennae could indicate an influence of juvenile hormone in parasitized A. pisum but the development of fifth-stadium supernumerary larvae (indicated by an extra moult and which can be induced by exogenous juvenile hormone treatments) was not found in parasitized aphids. In addition, while apterization of virginoparae can also be induced by the pro-allatocidal compound Precocene III, this was not possible in the male. Males which survived parasitoid attack without forming aphid mummies (indicating that oviposition had not occurred) developed as wingless individuals suggesting that the reproductive-tract-fluids from the female parasitoid were important in the wing inhibition process. Teratocytes from the parasitoid appeared to promote developmental arrest in parasitized aphids.     

Organic and conventional fertilizer effects on a tritrophic interaction: parasitism,performance and preference of Cotesia vestalis

Interest in sustainable farming methods that rely on alternatives to conventional synthetic fertilizers and pesticides is increasing. Sustainable farming methods often utilize natural populations of predatory and parasitic species to control populations of herbivores, which may be potential pest species. We investigated the effects of several types of fertilizer, including those typical of sustainable and conventional farming systems, on the interaction between a herbivore and parasitoid. The effects of fertilizer type on percentage parasitism, parasitoid performance, parasitoid attack behaviour and responses to plant volatiles were examined using a model Brassica system, consisting of Brassica oleracea var capitata, Plutella xylostella (Lepidoptera) larvae and Cotesia vestalis (parasitoid). Percentage parasitism was greatest for P. xylostella larvae feeding on plants that had received either a synthetic ammonium nitrate fertilizer or were unfertilized, in comparison to those receiving a composite fertilizer containing hoof and horn. Parasitism was intermediate on plants fertilized with an organically produced animal manure. Male parasitoid tibia length showed the same pattern as percentage parasitism, an indication that offspring performance was maximized on the treatments preferred by female parasitoids for oviposition. Percentage parasitism and parasitoid size were not correlated with foliar nitrogen concentration. The parasitoids did not discriminate between hosts feeding on plants in the four fertilizer treatments in parasitoid behaviour assays, but showed a preference for unfertilized plants in olfactometer experiments. The percentage parasitism and tibia length results provide support for the preference–performance hypothesis.     

Temperature influences host instar selection in an aphid parasitoid: support for the relative fitness rule

The relative fitness rule states that parasitoid females should adopt risk‐prone reproductive behaviours when expecting low reproductive success. Temperature influences the reproductive success of insects by affecting their basal metabolic rate during development, their egg load at emergence, and their life expectancy as adults. Using an aphid–parasitoid model system, we investigated the influence of developmental and adult temperature on the risk‐sensitive decision‐making of females. We considered the use of a low‐quality host nymphal instar by the aphid parasitoid Aphidius ervi to be a risk‐prone behaviour. Immature females were reared at 12, 20 or 28 °C and had access to the four nymphal instars of the potato aphid Macrosiphum euphorbiae for oviposition at one of these temperatures. Host selection behaviour was continuously recorded during exploitation of an aphid patch. We observed that warm‐developed females and parasitoids foraging at high temperature attacked low‐quality hosts more frequently than females from other treatments. These results support the hypothesis that a decrease in expected parasitoid reproductive success resulted in risk‐prone behaviours. To our knowledge, this is the first experimental evidence suggesting that temperature influences host stage selection and risk‐sensitive making decision in parasitoids, and the present study is the first to support the relative fitness rule. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●●, ●●–●●.     

Host selection and survival of the parasitoidEncarsia formosa on greenhouse whitefly,Trialeurodes vaporariorum, in the presence of hosts infected with the fungusAschersonia aleyrodis

Successful control of greenhouse whitefly may be achieved by complementary activity of the parasitoidEncarsia formosa and the fungusAschersonia aleyrodis. One way to obtain an additive mortality effect of both entomopathogen and parasitoid would be achieved by the selection of healthy hosts by the parasitoid and rejection of fungus-infected hosts. Third and fourth instar larvae ofTrialeurodes vaporariorum which had been treated with a spore suspension ofA. aleyrodis 0, 4, 7, 10 or 14 days beforehand, were presented to female parasitoids. The parasitoids adopted the oviposition posture on untreated hosts as well as on treated hosts, irrespective of the different stages of infection in the hosts. However, significantly more hosts were parasitized byE. formosa in the control treatment than in the fungal treatment. The parasitoids offered treated hosts, showed rejection behaviour after probing on hosts showing detectable signs of infection (containing hyphal bodies or mycelium in the haemolymph). For instance, when hosts were offered seven days after spore treatment, the parasitoids showed an oviposition posture on a total of 83 (95.4%) out of 87 infected larvae, but laid only 4 eggs (4.6%). In contrast, on 48 (94.1%) out of 51 noninfected (or showing no detectable signs of infection) hosts an oviposition posture was adopted and 40 eggs (78.4%) were found after dissection. When infected hosts were encountered the oviposition posture lasted less than 1′40″ while rejection of non-infected hosts occurred after more than 1′40″. Other experiments were carried out offering treated hosts for 24 h to the parasitoids. The hosts were dissected afterwards. Again, significantly more eggs were laid in the non-infected hosts. When hosts were parasitized shortly after fungal spore treatment they were colonized by the fungus and the parasitoids did not develop. Transmission of the entomopathogen after probing infected hosts was observed to a limited extent. In conclusion,A. aleyrodis andE. formosa can be used together in a glasshouse situation. The parasitoid will be most effective when introduced more than seven days after application ofA. aleyrodis, because from that time onwards it is able to detect and reject fungus-infected hosts.     

Coexistence of Competing Parasitoid Species on a Host with a Variable Life Cycle

Several special cases of a general model in which two parasitoid species attack different developmental stages of a single host species are presented. The inclusion of different mathematical forms of a maturation weighting function allows us to investigate the effect of several aspects of variation in immature stage durations on the outcome of competitition between the parasitoids. The two parasitoid species cannot coexist if the host developmental stages are fixed in duration. The outcome of competition depends in part on the relative duration of the two stages attacked by the parasitoid species. However, coexistence is possible if there is sufficient variation in the time that different host individuals remain in each stage. Distributed host developmental delays promote coexistence because they cause the host population to be composed of a mixture of host types with different relative egg versus larval stage durations. Each host type is thus largely available to only one of the parasitoid species.