Parasitoid dispersal and colonization lag in disturbed habitats: biological control of cereal leaf beetle metapopulations

Natural enemies of insect pests of annual crops have been hypothesized either to lag, or alternatively not to lag, behind their prey in dispersing to and colonizing new habitat. We examined parasitoid dispersal and parasitism of the cereal leaf beetle (Oulema melanopus [L.]; Coleoptera: Chrysomelidae) by the host‐specific wasp Tetrastichus julis [Walker] (Hymenoptera: Eulophidae) in wheat fields of northern Utah to assess whether a colonization lag occurred. Equally high rates of parasitism of beetle larvae (including second instars early in the year) occurred in 2010 and 2011 in fields that were newly planted to wheat vs. in fields where wheat had been grown also the previous year. A caging experiment demonstrated that parasitism in these newly planted wheat fields did not arise from parasitoid adults that had matured within the fields; instead, upon emerging in other fields, parasitoid females dispersed a minimum of 100–250 m to parasitize beetle larvae early in the spring in the newly planted fields. A transect study in 2012 revealed that T. julis females dispersed rapidly at least 600 m into a newly planted wheat field to parasitize most of the early maturing beetle larvae, which occurred at very low density. Thus, the parasitoid has very strong ability to match its host in dispersal over long distances across a highly disturbed agricultural landscape, and colonization lag appears of little importance in affecting biological control associated with this host–parasitoid interaction.     

Parasitoid genus‐specific manipulation of orb‐web host spiders (Araneae,Araneidae)

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The effects of host weight at parasitism on fitness correlates of the gregarious koinobiont parasitoid Microplitis tristis and consequences for food consumption by its host, Hadena bicruris

Gregarious koinobiont parasitoids attacking a range of host sizes have evolved several mechanisms to adapt to variable host resources, including the regulation of host growth, flexibility in larval development rate, and adjustment of clutch size. We investigated whether the first two mechanisms are involved in responses of the specialist gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) to differences in the larval weight and parasitoid load of its host Hadena bicruris Hufn. (Lepidoptera: Noctuidae). In addition, we examined the effects of parasitism on food consumption by the host. Parasitoids were offered caterpillars of different weight from all five instars, and parasitoid fitness correlates, including survival, development time, and cocoon weight, were recorded. Furthermore, several host growth parameters and food consumption of parasitized and unparasitized hosts were measured. Our results show that M. tristis responds to different host weights by regulating host growth and by adjusting larval development rate. In hosts with small weights, development time was increased, but the increase was insufficient to prevent a reduction in cocoon weight, and as a result parasitoids experienced a lower chance of successful eclosion. Cocoon weight was negatively affected by parasitoid load, even though host growth was positively affected by parasitoid load, especially in hosts with small weights. Later instars were more optimal for growth and development of M. tristis than early instars, which might reflect an adaptation to the life‐history of the host, whose early instars are usually concealed and inaccessible for parasitism on its food plant, Silene latifolia Krause (Caryophyllaceae). Parasitism by M. tristis greatly reduced total host food consumption for all instar stages. Whether plants can benefit directly from the attraction of gregarious koinobiont parasitoids of their herbivores is a subject of current debate. Our results indicate that, in this system, the attraction of a gregarious koinobiont parasitoid can directly benefit the plant by reducing the number of seeds destroyed by the herbivore.     

Reciprocal influences and costs of parasitism on the development of Corcyra cephalonica and its endoparasitoid Venturia canescens

Many endoparasitoids develop successfully within a range of host instars. Parasitoid survival is highest when parasitism is initiated in earlier host instars, due to age-related changes in internal (physiological) host defences. Most studies examining fitness-related costs associated with differences in host instar have concentrated on the parasitoid, ignoring the effects of parasitism on the development of surviving hosts that have encapsulated parasitoid eggs. A laboratory experiment was undertaken examining fitness-related costs associated with encapsulation of Venturia canescens (Hymenoptera: Ichneumonidae) eggs by fifth (L5) instar larvae of Corcyra cephalonica (Lepidoptera: Pyralidae). Growth and development of both host and parasitoid were monitored in C. cephalonica larvae containing 0, 1, 2, or 4 parasitoid eggs. Adult size and fecundity of C. cephalonica did not vary with the number of eggs per host. However, there was a distinct increase in host mortality with egg number, although most parasitoids emerged from hosts containing a single egg. The most dramatic effect on the host was a highly significant increase in development time from parasitism to adult eclosion, with hosts containing 4 parasitoid eggs taking over 2.5 days longer to complete development than unparasitized larvae. The egg-to-adult development time and size of adult V. canescens did not vary with egg number per host, as demonstrated in a previous experiment using a different host (Plodia interpunctella). The results described here show that there are fitness-related costs to the host associated with resistance to parasitism.     

Does Manipulation by the Parasitoid Wasp Cotesia glomerata (L.) Cause Attachment Behaviour of Host Caterpillars on Cocoon Clusters?

Some parasitoid wasps appear to control the behaviour of their hosts. However, altered behaviours of parasitised hosts are not necessarily caused by parasitoids but are sometimes the result of traumatic side effects of parasitism. However, it was difficult for us to discriminate the cause of host's behaviours between manipulation by parasitoids and traumatic side effects. Larvae of the parasitoid wasp Cotesia glomerata form cocoon clusters after egression from the parasitised host caterpillar Pieris brassicae . Following parasitoid egression, host caterpillars survive for several days and remain near the cocoon clusters. These caterpillars may repel solitary pteromalid hyperparasitoid wasps, Trichomalopsis apanteloctena , that attempt to parasitise fresh C. glomerata pupae. We allowed hyperparasitoids to attack cocoon clusters in the field and laboratory and then assessed the costs and benefits to C. glomerata of attachment by the parasitised caterpillars. The eclosion success of C. glomerata in cocoon clusters with attached caterpillars was higher than that in clusters without attached caterpillars in both field and laboratory experiments. This difference was attributed to shorter hyperparasitoid visits to cocoon clusters with attached host caterpillars. However, large cluster size was potentially costly for host attachment, because the duration of host caterpillar attachment decreased with increasing numbers of C. glomerata per caterpillar. This trade-off may be related to shortages of fat body resources, which are shared between the development of wasp larvae and the survival of host caterpillars. Therefore, we concluded that caterpillar attachment satisfied some requirements of host manipulation by C. glomerata .     

Varying degree of physiological integration among host instars and their endoparasitoid affects stress‐induced mortality

In natural populations of insect herbivores, genetic differentiation is likely to occur due to variation in host plant utilization and selection by the local community of organisms with which they interact. In parasitoids, engaging in intimate associations with their host during immature development, local variation may exist in host quality for parasitoid development. We compared the development of a gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae), collected in The Netherlands, in three strains and three caterpillar instars (L1–L3) of its main host, Pieris brassicae L. (Lepidoptera: Pieridae). Hosts had been collected in The Netherlands and France, and were reared in the laboratory for one generation. We also used an established Dutch laboratory strain that had not been exposed to parasitoids for at least 24 generations. Parasitoid survival to adulthood was inversely correlated with host instar at parasitism. Adult parasitoid body mass was largest when hosts were parasitized as L1 and smallest when hosts were parasitized as L3, whereas egg‐to‐adult development time was quickest on L3 hosts and slowest on L1 hosts. Higher survival and faster development of C. glomerata on French L2 hosts also showed that there is variation in host‐instar‐related suitability. Many L2 and most L3 caterpillars that were parasitized exhibited signs of pathogen infection and perished within a few days of parasitism, whereas this never happened when hosts were parasitized as L1 or in non‐parasitized control caterpillars. Our results reveal that, irrespective of the host strain, L1 hosts are optimally synchronized with C. glomerata development. By contrast, the high precocious mortality of L3 larvae may be due to stress‐induced regulation by the parasitoid in order to ‘force’ its developmental program into synchrony with the developing parasitoid larvae. Our results underscore a potentially important role played by pathogens in mediating herbivore–parasitoid interactions that are host‐instar‐dependent in their expression.     

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.     

The parasitoid wasp Eruga unilabiana Pádua & Sobczak,sp. nov. (Hymenoptera: Ichneumonidae) induces behavioral modification in its spider host

Some polysphinctine parasitoid wasps can alter the web building behavior of their host spiders. In this paper, we describe and illustrate a new species Eruga unilabiana sp. nov. and report for the first time, to the best of our knowledge, the interaction between this parasitic wasp and the linyphiid spider Dubiaranea sp. We investigated the wasp's host selection, development, and manipulation of host behavior. We found that most of the parasitized spiders were intermediate‐sized adult females that probably provide sufficient resources for parasitoid larvae and are less vulnerable for parasitoid females than larger host individuals at attack. The cocoon web of Dubiaranea sp. consists of a complex three‐dimensional tangle structure with several non‐stick radial lines that converge at the cocoon. In addition, E. unilabiana individuals construct their cocoons horizontally, which differ from cocoons of the majority of polysphinctine wasps. This study provides important information and discussion to further understand the evolution of parasitoid wasp–spider interactions.     

Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness

1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae. 2. Clutch size of C. glomerata was manipulated artificially, and the relationship between parasitoid burden and the maximum weight of the parasitised host (= host–parasitoid complex) was measured. In both hosts, the maximum complex weight was correlated positively with parasitoid burden. Compared with unparasitised hosts, however, the growth of P. rapae was increased at significantly lower parasitoid burdens than in P. brassicae. Emerging wasp size was correlated negatively with parasitoid burden in both host species, whereas development time was less affected. 3. After larval parasitoid egress, the weight of the host carcass increased slightly, but not significantly, with parasitoid burden, although there was a strong correlation between the proportion of host mass consumed by C. glomerata larvae during development and parasitoid burden. 4. Clutch size was generally correlated positively with instar parasitised in both hosts, and greater in P. brassicae than in P. rapae. Sex ratios were much more female biased in L1 and L2 P. rapae than in all other host classes. Adult parasitoid size was correlated inversely with host instar at parasitism, and wasps emerging from P. brassicae were larger, and completed development faster, than conspecifics emerging from P. rapae. 5. The data reveal that parasitism by C. glomerata has profound species‐specific effects on the growth of both host species. Consequently, optimality models in which host quality is often based on host size at parasitism or unparasitised growth potential may have little utility in describing the development of gregarious koinobiont endoparasitoids. The results of this investigation are discussed in relation to the potential effectiveness of gregarious koinobionts in biological control programmes.     

Does aggregation behavior of codling moth larvae,Cydia pomonella,increase the risk of parasitism by Mastrus ridibundus?

Mastrus ridibundus is a specialist hymenopteran parasitoid that parasitizes last-instar larvae or prepupae of the codling moth, Cydia pomonella. Foraging females eavesdrop on an aggregation pheromone produced by cocooning larvae. We investigated whether larvae that cocoon in aggregation experience a greater rate of parasitism than larvae that cocoon in isolation. In wind tunnel experiments, 10 larvae in aggregations were more readily located by female M. ridibundus than 10 larvae well separated from each other. Similarly, aggregations of 30 larvae were more attractive to female M. ridibundus than those of 3 larvae. In cage experiments, larval cocooning in aggregation or isolation had no effect on the mean rate of parasitism and the mean number of eggs deposited per parasitized host. In Petri-dish experiments, the location of larvae within an aggregation significantly affected their rate of parasitism, with those in the center of an aggregation completely shielded from parasitism. Our data suggest that aggregation behavior by C. pomonella larvae does not appear to increase the rate of parasitism. The increased risk of aggregated larvae to be detected by M. ridibundus is likely offset by diluted parasitism risk and structural refugia effects that larvae in aggregation experience. As an egg-limited parasitoid, female M. ridibundus can parasitize on average only one larva in an aggregation, with the likelihood of parasitism for each larva being inversely proportional to the number of larvae in that aggregation.     

Suitability of the maize weevil and angoumois grain moth as hosts for the parasitoidsAnisopteromalus calandrae andPteromalus cerealellae

Two parasitoids,Pteromalus cerealellae (Ashmead) andAnisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), were compared for their ability to parasitize two important internally-developing insect pests of stored maize (Zea mays L.). Parasitism byP. cerealellae was greater on Angoumois grain moth,Sitotroga cerealella (Olivier), than on maize weevil,Sitophilus zeamais Motschulsky, in no-choice experiments.Anisopteromalus calandrae parasitized more maize weevils than didP. cerealellae. The former parasitoid parasitized only a few Angoumois grain moths successfully in maize, but parasitized many in wheat if the hosts were younger than 3 weeks old. Thus, both host age and type of grain affect suitability for parasitism. The effects of parental host (species on which the female developed) and experimental host (species exposed to parasitism) on parasitism rate ofP. cerealellae were tested in a host-switching experiment. Parasitism by parasitoids reared on maize weevils was 23% lower than that of parasitoids reared on Angoumois grain moth. This effect was independent of which host the filial generation of parasitoids was tested on. However, the experimental host species had a much greater effect on parasitoid fecundity than the parental host species. Female progeny had smaller body sizes when emerging from maize weevil than from Angoumois grain moth, which may explain the parental host effect on fecundity. There was also a slight intergenerational effect of host species on parasitoid body size.     

Host behavior modification of Achaearanea tingo (Araneae: Theridiidae) induced by the parasitoid wasp Zatypota alborhombarta (Hymenoptera: Ichneumonidae)

Behavioral manipulation involving Zatypota (Ichneumonidae: Pimplinae) parasitoids and their spider hosts is usually associated with an increase in web complexity at the location where the parasitoid larva builds its cocoon. A higher number of web threads at this location may improve stability and provide a physical barrier against potential predators. However, we observed that parasitized individuals of Achaearanea tingo attacked by Z. alborhombarta change the three‐dimensional structure of their webs to a very simple and strong structure composed of two cables attached to the surrounding vegetation. This structure holds the curled leaf formerly used by the spider as a shelter. The parasitoid larva remains protected within this shelter after killing the host. The architectural pattern of the cocoon webs of A. tingo indicates that host manipulation is characterized by the repetition of one specific subroutine involved in web construction. Similar alterations have been previously described for cocoon webs constructed by parasitized orb‐weavers, but not for the three‐dimensional webs of theridiids.     

Winter host exploitation influences fitness traits in a parasitoid

Organisms can either evade winter's unfavourable conditions by migrating or diapausing, or endure them and maintain their activities. When it comes to foraging during winter, a period of scarce resources, there is strong selective pressure on resource exploitation strategy. Generalist parasitoids are particularly affected by this environmental constraint, as their fitness is deeply linked to the profitability of the available hosts. In this study, we considered a cereal aphid–parasitoid system and investigated (1) the host–parasitoid community structure, host availability, and parasitism rate in winter, (2) the influence of host quality in terms of species and instars on the fitness of the aphid parasitoid Aphidius rhopalosiphi De Stefani‐Perez (Hymenoptera: Braconidae: Aphidiinae), and (3) whether there is a detectable impact of host fidelity on parasitism success of this parasitoid species. Host density was low during winter and the aphid community consisted of the species Rhopalosiphum padi L. and Sitobion avenae Fabricius (both Hemiptera: Aphididae), both parasitized by A. rhopalosiphi at non‐negligible rates. Aphidius rhopalosiphi produced more offspring when parasitizing R. padi compared with S. avenae, whereas bigger offspring were produced when parasitizing S. avenae. Although aphid adults and old larvae were significantly larger hosts than young larvae, the latter resulted in higher emergence rates and larger parasitoids. No impact of host fidelity on emergence rates or offspring size was detected. This study provides some evidence that winter A. rhopalosiphi populations are able to take advantage of an array of host types that vary in profitability, indicating that host selectivity may drop under winter's unfavourable conditions.     

Infection of the immature stages of Diadegma semiclausum, an endolarval parasitoid of the diamondback moth, by Beauveria bassiana

Interactions between the immature stages of Diadegma semiclausum, an endolarval parasitoid of Plutella xylostella, and the fungal entomopathogen Beauveria bassiana were investigated in the laboratory. Detrimental effects of B. bassiana on D. semiclausum cocoon production and adult parasitoid emergence increased with increasing pathogen concentration and some parasitoid larvae became infected by B. bassiana within hosts. The negative impact of B. bassiana on D. semiclausum cocoon production decreased as temporal separation between parasitism and pathogen exposure increased. Adult parasitoid emergence was significantly compromised by the highest rates of B. bassiana tested even when exposure of host larvae to the pathogen was delayed until one day before predicted parasitoid cocoon formation. Parasitoid pupae were infected by the pathogen in all B. bassiana treatments which did not preclude their development.     

Development of the gregarious ectoparasitoid Nasonia vitripennis using five species of necrophagous flies as hosts and at various developmental temperatures

The utility of five species of necrophagous flies (Diptera) as pupal hosts for Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) was examined by comparing incidences of parasitism, fecundity, and several features of wasp development at three rearing temperatures. Species differences in host suitability were evident in all life history features examined, with the highest incidences of parasitism, largest clutches and adult body sizes, and shortest periods of development occurring when the sarcophagid Sarcophaga bullata Parker served as hosts, regardless of temperature in which the wasps developed. Puparia of the calliphorids Lucilia illustris Meigen, Phormia regina Meigen, and Protophormia terraenovae Robineau‐Desvoidy were also accepted as hosts by the female parasitoids, albeit not equally so, and each yielded large, female‐biased broods. By contrast, pupae of the calliphorid Chrysomya rufifacies (Macquart) were not well suited to serve as an oviposition site or support the development of N. vitripennis. When successful parasitism did occur on any host species, duration of parasitoid development increased, adult body sizes were truncated, male‐biased sex ratios were produced, and mortality from egg hatch to adult emergence elevated with increasing rearing temperature. Unlike with the four other fly species, C. rufifacies did not yield any adult parasitoids when the rearing temperature was 35 °C. The results argue that developmental data determined for this wasp derived from a single host species is not sufficient for applying to all scenarios in which wasp development is necessary to estimate a postmortem interval or periods of insect activity.     

The effect of host nutrition on growth and development of the parasitoid waspVenturia canescens

We investigated the effect of host (Plodia interpunctella; Lepidoptera: Pyralidae) nutritional status on development of the solitary endoparasitoid,Venturia canescens (Hymenoptera: Ichneumonidae). Parasitoids from 3rd (L3) instars reared on a deficient diet during early parasitism took longer to develop and suffered higher mortality than those reared from hosts fedad libitum although there was not a significant difference in the size of eclosing wasps from the two groups. L5 hosts reared at high density produced smaller parasitoids, which developed more rapidly than those reared from hosts from low density containers, although mortality was higher in the latter. In a separate experiment we starved groups of 10–20 hosts (parasitized as L3) daily beginning on the 4th day after parasitism, to determine the host developmental stage required for successful parasitoid development to eclosion. Parasitoid survivorship increased with length of host access to food, while the egg-to-adult parasitoid development time increased throughout the experiment. Parasitoid size decreased with increasing periods of host starvation. The successful emergence ofVenturia depends uponPlodia reaching the size normally attained in the mid-5th instar, or 50–70% of the mass of healthy late 5th instars. Our results show that when earlier instars are parasitized, host growth is essential for successful parasitoid development to eclosion. Furthermore, they suggest that, for many koinobionts, host suitability may be greatly influenced by feeding rate and food quality.     

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.     

The cost of a bodyguard

Host manipulation by parasites not only captures the imagination but has important epidemiological implications. The conventional view is that parasites face a trade-off between the benefits of host manipulation and their costs to fitness-related traits, such as longevity and fecundity. However, this trade-off hypothesis remains to be tested. Dinocampus coccinellae is a common parasitic wasp of the spotted lady beetle Coleomegilla maculata. Females deposit a single egg in the haemocoel of the host, and during larval development the parasitoid feeds on host tissues. At the prepupal stage, the parasitoid egresses from its host by forcing its way through the coccinellid's abdominal segments and begins spinning a cocoon between the ladybird's legs. Remarkably, D. coccinellae does not kill its host during its development, an atypical feature for parasitoids. We first showed under laboratory conditions that parasitoid cocoons that were attended by a living and manipulated ladybird suffered less predation than did cocoons alone or cocoons under dead ladybirds. We then demonstrated that the length of the manipulation period is negatively correlated with parasitoid fecundity but not with longevity. In addition to documenting an original case of bodyguard manipulation, our study provides the first evidence of a cost required for manipulating host behaviour.     

Role of a parasitoid with a low fecundity,Praestochrysis shanghaiensis (Hymenoptera: Chrysididae), in the population dynamics of its host

1. Analysis of life tables of the oriental moth, Monema flavescens, obtained for 8 generations over 4 years, disclosed that the cocoon parasitoid, Praestochrysis shanghaiensis, acted as a density-disruptive factor.
2. The density of the host cocoon remained stable (max./min.=3.2), whereas that of the host adult varied (max./min.=14.3) although both showed similar fluctation patterns.
3. Stability of the host population was associated with the density-dependence in the ratio of first generation cocoons to overwintered generation moths, which was the key factor for the rate of change throughout the year. Chrysidid parasitism among the first generation cocoons ranged from 37.7 to 70.1%, and that among the second generation cocoons from 16.7 to 63.2%, each showing an inverse density-dependence and acting as the main determinant (key-factor) of the between-year variation in the density of the adult moths.
4. The density-dependence of the rate of change from overwintered generation adults to first generation cocoons was so strong that the parasitism on the second generation hosts had not effect on the cocoon density of the first generation. On the other hand, the density-dependence of the rate of change from first generation adults to second generation cocoons was weak, and the parasitism on the first generation hosts became the key factor for the between-year variation of the second generation cocoons.
5. It is suggested that the stability of the parasitoid-host system will be disrupted without three parasitism-restricting factors: asynchrony in the parasitoid attack on the second generation hosts, high mortality among parasitoid larvae of the second generation, and the high proportion of those first generation parasitoids that enter diapause. These factors are considered to be effective only in cooler parts of the distribution of the parasitoid.

     

Host ontogeny determines parasitoid use of a forest caterpillar

For most organisms, patterns of natural enemy‐mediated mortality change over the course of development. Shifts in enemy pressure are particularly relevant for organisms that exhibit exponential growth during development, such as juvenile insects that increase their mass by several orders of magnitude. As one of the dominant groups of insect herbivores in most terrestrial plant communities, larval lepidopterans (caterpillars) are host to a diverse array of parasitoids. Previous research has described how the frequency of herbivore parasitism varies among host plants or habitats, but much less is known about how parasitism pressure changes during host development. To test whether the two major parasitoid taxa, wasps and flies, differentially attack shared hosts based on host developmental stage, we simultaneously exposed early‐ and late‐instar Euclea delphinii Boisduval (Lepidoptera: Limacodidae) caterpillars to parasitism in the field. We found strong evidence that parasitoids partition hosts by size; adult female wasps preferentially parasitized small caterpillars, whereas adult female flies preferred to attack large caterpillars. Our results demonstrate that host ontogeny is a major determinant of parasitoid host selection. Documenting how shifts in enemy pressure vary with development is important to understanding both the population biology and evolutionary ecology of prey species and their enemies.