Behavioral manipulation of host caterpillars by the primary parasitoid wasp Cotesia glomerata (L.) to construct defensive webs against hyperparasitism

Many parasitoids control the behavior of their hosts to achieve more preferable conditions. Decreasing predation pressure is a main aim of host manipulation. Some parasitoids control host behavior to escape from their enemies, whereas others manipulate hosts into constructing defensive structures as barriers against hyperparasitism. Larvae of the parasitoid wasp Cotesia glomerata form cocoon clusters after egression from the parasitized host caterpillar of the butterfly Pieris brassicae. After the egression of parasitoids, the perforated host caterpillar lives for a short period and constructs a silk web that covers the cocoon cluster. We examined whether these silk webs protect C. glomerata cocoons against the hyperparasitoid wasp Trichomalopsis apanteroctena. In cocoon clusters that were not covered by silk webs (bare clusters), only cocoons hidden beneath others avoided hyperparasitism. In covered cocoon clusters, both cocoons hidden beneath others and those with a space between them and the silk web avoided hyperparasitism, whereas cocoons that contacted the silk webs were parasitized. The frequency of cocoons that were hidden beneath others increased with the increasing number of cocoons in a cluster, but the defensive effect of cluster size was thought to be lower than that of silk webs. However, the rate of hyperparasitism did not differ between covered and bare clusters when we allowed the hyperparasitoids to attack the cocoon clusters in an experimental arena. This result was thought to have been caused by low oviposition frequency by these hyperparasitoids. As a result, silk webs did not guard the cocoons from hyperparasitoids in our experiments, but would protect cocoons under high hyperparasitism pressure by forming a space through which the ovipositors could not reach the cocoons.     

Suspending cocoons to evade ant predation in Meteorus pulchricornis, a braconid parasitoid of exposed-living lepidopteran larvae

We tested the hypothesis that cocoon suspension by a thread in hymenopteran parasitoids is a defense tactic against predators, by comparing predation against suspended and non-suspended cocoons of the braconid wasp Meteorus pulchricornis on a Quercus phillyraeoides hedge on which workers of the common small ant Crematogaster matsumurai were foraging. The lost proportion of non-suspended cocoons, which were artificially attached to leaves of Q. phillyraeoides , markedly decreased with cocoon age, indicating a critical phase of predation on young cocoons. No suspended cocoons at age 1–12 h at the beginning of exposure were lost within 12 h, whereas more than 75% of same-aged non-suspended cocoons were lost in the same period. Predation against such young cocoons would be a strong force driving the evolution of cocoon suspension in parasitoids of exposed-living host insects.     

Intra- and interspecific predation on the cocoons of Erpobdella octoculata (L.) (Annelida: Hirudinea)

In laboratory experiments, eleven out of twenty-one invertebrate species and all of the three fish species tested fed on freshly laid flaccid cocoons of Erpobdella octoculata, though predation was only severe from a dytiscid beetle, E. octoculata and the fish species. There was a tendency for more cocoons to be eaten by starved than fed predators. Only snail species damaged one-week-old tougher cocoons.Only one out of 471 E. octoculata collected during their breeding season from the stony shores of two eutrophic lakes had a cocoon in its gut.The role of cannibalism of and interspecific predation on cocoons in the control and regulation of lake-dwelling populations of the erpobdellid is discussed, and assessed to be relatively unimportant. A more likely regulatory mechanism may involve high juvenile mortality from as yet unknown causes.     

Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community

The enemy‐free space hypothesis (EFSH) contends that generalist predators select for dietary specialization in insect herbivores. At a community level, the EFSH predicts that dietary specialization reduces predation risk, and this pattern has been found in several studies addressing the impact of individual predator taxa or guilds. However, predation at a community level is also subject to combinatorial effects of multiple‐predator types, raising the question of how so‐called multiple‐predator effects relate to dietary specialization in insect herbivores. Here, we test the EFSH with a field experiment quantifying ant predation risk to insect herbivores (caterpillars) with and without the combined predation effects of birds. Assessing a community of 20 caterpillar species, we use model selection in a phylogenetic comparative framework to identify the caterpillar traits that best predict the risk of ant predation. A caterpillar species' abundance, dietary specialization, and behavioral defenses were important predictors of its ant predation risk. Abundant caterpillar species had increased risk of ant predation irrespective of bird predation. Caterpillar species with broad diet breadth and behavioral responsiveness to attack had reduced ant predation risk, but these ant effects only occurred when birds also had access to the caterpillar community. These findings suggest that ant predation of caterpillar species is density‐ or frequency‐dependent, that ants and birds may impose countervailing selection on dietary specialization within the same herbivore community, and that contingent effects of multiple predators may generate behaviorally mediated life‐history trade‐offs associated with herbivore diet breadth.     

Cocoon predation on diprionid sawflies: the effect of forest fertility

Predation by small mammals is thought to be one of the main regulators of outbreaking sawfly species. It has been suggested that predation may be lower in poor and dryish forests, and this is the reason why outbreaks often begin from this type of environment. We studied experimentally how fertility of the forest site affects cocoon predation experienced by two sawfly species, the common pine sawfly Diprion pini (Linnaeus) and the European pine sawfly Neodiprion sertifer (Geoffroy). We applied a fertilization treatment to selected pine-dominated barren forest sites in Finland, and 2–4 years later monitored predation on the sawfly cocoons in fertilized and control areas. The results did not support the idea that forest fertility was related to cocoon predation. We also could not verify that small mammal abundance was related to fertility of the forest. The most obvious pattern we observed was that the two sawfly species differed dramatically in predation experienced. N. sertifer has its cocoon phase in mid-summer and experienced only moderate predation (37%) whereas D. pini, with its cocoon phase in autumn, suffered from very heavy predation (96%). Our observations suggest that if predation is important in controlling the population dynamics of the species, its impact depends more on the sawfly species and season than on the fertility of the forest site. Received: 1 March 1998 / Accepted: 25 May 1998     

Problems of orientation associated with cocoon-spinning by Nemeritis

Abstract. 1. Larvae of Nemeritis that have reached full growth in a caterpillar of Ephestia invariably push the host remains towards the closed end of the host cocoon and pupate with their heads towards the open end. Larvae reaching full growth in a pupal host are usually orientated in the same direction, but occasionally in reverse.
2. The parasitoid does not orientate itself by direct reference to the host cocoon but in relation to the final position of the host. The host remains are probably used as a point of reference.
3. As the parasitoid spins its own cocoon, it isolates itself from some external stimuli and has need of a new point of reference. It provides this by incorporating guide marks, in the form of areas of specially woven threads, in successive layers of its cocoon.
4. The final mark, on the innermost layer, not only indicates the anterior end of the cocoon, but also may help the adult to bite its way out.
5. The presence of similar marks has been observed in the cocoons of five other species of Ichneumonidae, representing the two subfamilies Ophioninae and Cryptinae.
6. The significance of these provisions for correct orientation of ichneumon wasps is briefly discussed.     

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.     

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 .     

Shifting effects of host physiological condition following pathogen establishment

Understanding host persistence with emerging pathogens is essential for conserving populations. Hosts may initially survive pathogen invasions through pre-adaptive mechanisms. However, whether pre-adaptive traits are directionally selected to increase in frequency depends on the heritability and environmental dependence of the trait and the costs of trait maintenance. Body condition is likely an important pre-adaptive mechanism aiding in host survival, although can be seasonally variable in wildlife hosts. We used data collected over 7 years on bat body mass, infection and survival to determine the role of host body condition during the invasion and establishment of the emerging disease, white-nose syndrome. We found that when the pathogen first invaded, bats with higher body mass were more likely to survive, but this effect dissipated following the initial epizootic. We also found that heavier bats lost more weight overwinter, but fat loss depended on infection severity. Lastly, we found mixed support that bat mass increased in the population after pathogen arrival; high annual plasticity in individual bat masses may have reduced the potential for directional selection. Overall, our results suggest that some factors that contribute to host survival during pathogen invasion may diminish over time and are potentially replaced by other host adaptations.     

Life-history traits in closely related secondary parasitoids sharing the same primary parasitoid host: evolutionary opportunities and constraints

Thus far, few studies have compared life-history traits amongst secondary parasitoids attacking and developing in cocoons of their primary parasitoid hosts. This study examines development and reproduction in Lysibia nana Gravenhorst and Acrolyta nens Hartig (both Hymenoptera: Ichneumonidae), two related and morphologically similar secondary parasitoids that attack pupae of the gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae). On black mustard, Brassica nigra L. (Brassicaceae) plants in a field plot, adults of L. nana and A. nens frequently emerged from the same cocoon broods of C. glomerata . Based on similarities in their phylogeny and morphology, it was hypothesized that both species would exhibit considerable overlap in other life-history traits. In both L. nana and A. nens , adult wasp size increased with host cocoon mass at parasitism, although L. nana wasps were slightly larger than A. nens wasps, and completed their development earlier. Adult females of both species emerged with no eggs but matured eggs at similar rates over the following days. When provided with 20 host cocoons daily, fecundity in female L. nana was slightly more skewed towards early life than in A. nens , although lifetime fecundity did not differ between the two species. Longevity was significantly reduced in females of both species that were provided with hosts. Both parasitoids were found to exhibit strong similarities in life-history and development traits and in their ecological niche, thereby supporting our general hypothesis. Competition between L. nana and A. nens is presumably diffused because their preferred host ( C. glomerata ) is relatively abundant in open habitats.     

Bigger is not always better: Viability selection on body mass varies across life stages in a hibernating mammal

Body mass is often viewed as a proxy of past access to resources and of future survival and reproductive success. Links between body mass and survival or reproduction are, however, likely to differ between age classes and sexes. Remarkably, this is rarely taken into account in selection analyses. Selection on body mass is likely to be the primary target accounting for juvenile survival until reproduction but may weaken after recruitment. Males and females also often differ in how they use resources for reproduction and survival. Using a long‐term study on body mass and annual survival in yellow‐bellied marmots (Marmota flaviventer), we show that body mass was under stabilizing viability selection in the first years of life, before recruitment, which changed to positive directional selection as age increased and animals matured. We found no evidence that viability selection across age classes on body mass differed between sexes. By investigating the link between running speed and body mass, we show that the capacity to escape predators was not consistent across age classes and followed a quadratic relationship at young ages only. Overall, our results indicate that mature age classes exhibit traditional patterns of positive viability selection on body mass, as expected in a hibernating mammal, but that mass in the first years of life is subjected to stabilizing selection which may come from additional predation pressures that negate the benefits of the largest body masses. Our study highlights the importance to disentangle selection pressures on traits across critical age (or life) classes.     

How do host plant use and seasonal life cycle relate to insect body size: A case study on European geometrid moths (Lepidoptera: Geometridae)

We used European geometrid moths (>630 species) as a model group to investigate how life history traits linked to larval host plant use (i.e., diet breadth and host-plant growth form) and seasonal life cycle (i.e., voltinism, overwintering stage and caterpillar phenology) are related to adult body size in holometabolous insect herbivores. To do so, we applied phylogenetic comparative methods to account for shared evolutionary history among herbivore species. We further categorized larval diet breadth based on the phylogenetic structure of utilized host plant genera. Our results indicate that species associated with woody plants are, on average, larger than herb feeders and increase in size with increasing diet breadth. Obligatorily univoltine species are larger than multivoltine species, and attain larger sizes when their larvae occur exclusively in the early season. Furthermore, the adult body size is significantly smaller in species that overwinter in the pupal stage compared to those that overwinter as eggs or caterpillars. In summary, our results indicate that the ecological niche of holometabolous insect herbivores is strongly interrelated with body size at maturity.     

Comparative Proteome Analysis of Multi-Layer Cocoon of the Silkworm,Bombyx mori

Bombyx mori cocoon has a multi-layer structure that provides optimal protection for silkworm pupa. Research on the mechanical properties of the multi-layer structure revealed structure-property relationships of the cocoon. Here, we investigated the protein components of the B. mori cocoon in terms of its multi-layer structure. Liquid chromatography-tandem mass spectrometry identified 286 proteins from the multiple cocoon layers. In addition to fibroins and sericins, we identified abundant protease inhibitors, seroins and proteins of unknown function. By comparing protein abundance across layers, we found that the outermost layer contained more sericin1 and protease inhibitors and the innermost layer had more seroin1. As many as 36 protease inhibitors were identified in cocoons, showing efficient inhibitory activities against a fungal protease. Thus, we propose that more abundant protease inhibitors in the outer cocoon layers may provide better protection for the cocoon. This study increases our understanding of the multi-layer mechanism of cocoons, and helps clarify the biological characteristics of cocoons. The data have been deposited to the ProteomeXchange with identifier PXD001469.     

Hibernation is associated with increased survival and the evolution of slow life histories among mammals

Survival probability is predicted to underlie the evolution of life histories along a slow-fast continuum. Hibernation allows a diverse range of small mammals to exhibit seasonal dormancy, which might increase survival and consequently be associated with relatively slow life histories. We used phylogenetically informed GLS models to test for an effect of hibernation on seasonal and annual survival, and on key attributes of life histories among mammals. Monthly survival was in most cases higher during hibernation compared with the active season, probably because inactivity minimizes predation. Hibernators also have approximately 15 per cent higher annual survival than similar sized non-hibernating species. As predicted, we found an effect of hibernation on the relationships between life history attributes and body mass: small hibernating mammals generally have longer maximum life spans (50% greater for a 50 g species), reproduce at slower rates, mature at older ages and have longer generation times compared with similar-sized non-hibernators. In accordance with evolutionary theories, however, hibernating species do not have longer life spans than non-hibernators with similar survival rates, nor do they have lower reproductive rates than non-hibernators with similar maximum life spans. Thus, our combined results suggest that (i) hibernation is associated with high rates of overwinter and annual survival, and (ii) an increase in survival in hibernating species is linked with the coevolution of traits indicative of relatively slow life histories.     

Impact of cocoon predation and parasitism on endemic populations of the common pine sawfly, Diprion pini (L.) (Hymenoptera, Diprionidae) in different forest types

1 Predation and parasitism on litter‐buried cocoons of the common pine sawfly Diprion pini (L.) were compared in different forest types with endemic sawfly populations by field exposure of laboratory‐reared cocoons during three consecutive years (1993–1995). 2 The impact of cocoon predation was dependent on season and forest type. The highest predation (up to 95%) was found during autumn in forest stands with a dense understory vegetation. 3 Cocoon parasitism varied between year, season and forest type. The highest parasitoid attack was observed in pure pine forests with more or less barren soils, but did not exceed 24% of exposed cocoons. 4 Cocoons were exposed in small patches. Predators tended to exploit all cocoons of a patch, whereas parasitoids only attacked a few cocoons of a patch. Predation was similar on cocoons placed in the litter and those buried more deeply in the soil, whereas parasitism of soil‐buried cocoons was rare. 5 These results indicate that predators can have a remarkable potential for limiting endemic sawfly densities, if habitat conditions in a forest maintain their population and support their foraging behaviour. A notable effect of parasitoids on sawfly cocoons deposited in the litter is obviously restricted to typical pure and barren pine forests, but may play there a similar role as predation.     

Construction of Nest Defensive Structure According to Offspring Value and Its Effect on Predator's Attack Decision in Paper Wasps

Various organisms are known to build nests with defensive structures to protect their offspring from predation, but our understanding of plasticity in the nest structure remains poor. In this study, we investigated whether a paper wasp, Polistes chinensis antennalis, adjusted the construction of nest defensive structure according to the value of their offspring, and we also analysed the effect of adjusting the construction of the structure on predator's decision to attack. P. chinensis antennalis foundresses start a colony and maintain her nest alone until the emergence of workers. During this stage, foundresses often construct a defensive structure on cocoon caps of pupae using nest materials (pulp), which prevents predation of pupae by conspecifics from other nests. The value of pupae to the foundress varies among those in a nest, where the value is higher in pupae that spun the cocoon (and initiated pupation) earlier than other pupae in the nest. From field observations, we found that foundresses constructed a larger pulp structure on the cocoons of pupae that cocooned earlier in the order of cocoon spinning, even after considering confounding factors. We also found that the probability of a pupa being attacked by conspecific intruders decreased with the size of pulp structure on the cocoon. This indicates that intruders avoid attacking cocoons with larger pulp structures. Our study indicates that foundresses adjust the construction of nest defensive structures according to their offspring value, and this allows them to protect the high‐value offspring efficiently and effectively.     

A hierarchical Bayesian model to estimate the unobservable predation rate on sawfly cocoons by small mammals

Predation by small mammals has been reported as an important mortality factor for the cocoons of sawfly species. However, it is difficult to provide an accurate estimate of newly spun cocoons and subsequent predation rates by small mammals for several reasons. First, all larvae do not spin cocoons at the same time. Second, cocoons are exposed to small mammal predation immediately after being spun. Third, the cocoons of the current generation are indistinguishable from those of the previous generation. We developed a hierarchical Bayesian model to estimate these values from annual one‐time soil sampling datasets. To apply this model to an actual data set, field surveys were conducted in eight stands of larch plantations in central Hokkaido (Japan) from 2009 to 2012. Ten 0.04‐m² soil samples were annually collected from each site in mid‐October. The abundance of unopened cocoons (I), cocoons emptied by small‐mammal predation (M), and empty cocoons caused by something other than small‐mammal predation (H) were determined. The abundance of newly spun cocoons, the predation rate by small mammals before and after cocoon sampling, and the annual rate of empty cocoons that remained were estimated. A posterior predictive check yielded Bayesian P‐values of 0.54, 0.48, and 0.07 for I, M, and H, respectively. Estimated predation rates showed a significant positive correlation with the number of trap captures of small mammals. Estimates of the number of newly spun cocoons had a significant positive correlation with defoliation intensity. These results indicate that our model showed an acceptable fit, with reasonable estimates. Our model is expected to be widely applicable to all hymenopteran and lepidopteran insects that spin cocoons in soil.     

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.     

Overwinter mass loss of snowshoe hares in the Yukon: starvation, stress, adaptation or artefact?

1. Overwinter mass loss can reduce energetic requirements in mammals (Dehnel's phenomenon). Alternatively, mass loss can result from food limitation or high predation risk. 2. We use data from fertilizer, food-supplementation and predator-exclusion experiments in the Yukon during a population cycle from 1986 to 1996 to test the causes of overwinter mass loss by snowshoe hares (Lepus americanus). In all years, some hares on control sites gained mass overwinter. During the increase phase the majority gained mass, but in all other phases the majority lost mass. 3. Snowshoe hares weighing <1000 g in autumn always gained mass overwinter, as did the majority that weighed 1000-1400 g. Hares weighing >1800 g in autumn usually lost mass. 4. Snowshoe hares on the predator-exclosure + food site gained mass overwinter in all years. Hares on the food-supplementation sites lost mass during the decline but gained mass in all other phases. Fertilization had little effect on mass dynamics. 5. Snowshoe hares were more likely to lose mass during winters with low survival rates. Snowshoe hares on the predator-exclosure treatments were more likely to gain mass than were hares on control sites. 6. Overwinter mass loss was correlated with maximum snow depth. At equivalent snow depths, hares on food-supplemented areas lost 98 g (+/- 14.6 SE) less on average than hares on the controls and predator-exclosure treatment. 7. Bone-marrow fat was related to body mass and cause of death. Small hares had the lowest marrow fat. Hares killed by humans had higher marrow fat than those killed by predators; hares that simply died had the lowest marrow fat. Hares on food-supplemented sites had the highest kidney and marrow fat. 8. Overwinter-mass loss for snowshoe hares is explained interactively by winter conditions, food supply, predation risk and autumn mass. Some snowshoe hares lost mass overwinter in all years and on all treatments, suggesting that reducing body mass may facilitate survival, especially in cases where foraging costs are high energetically or increase predation risk.     

Defoliation tolerance affects the spatial and temporal distributions of larch sawfly and natural enemy populations

1. The monophagous larch sawfly, Pristiphora erichsonii, requires larch, Larix spp., shoots for oviposition and foliage for larval development. The hypothesis that chronic defoliation reduces shoot availability for adult females, causing shifts in host use within plantations of L. decidua and L. leptolepis , was evaluated over a 3-year period.
2. Larch productivity and sawfly abundance varied six- to 10-fold among individual trees within each plantation. Sawflies concentrated oviposition on the most rapidly growing trees, and had a marginal impact on shoot production. Consequently, sawfly herbivory on individual trees remained relatively constant for 3 years, failing to support the hypothesis that P. erichsonii defoliation causes shifts in host use.
3. Pristiphora erichsonii larval performance varied 20–30% among individual host trees. The oviposition event did not significantly affect larval performance or foliar nutrient content.
4. The relationship between cocoon survival and natural enemy abundance was evaluated among fifteen L. leptolepis trees. Parasites and predators killed over 65% of the 18 315 cocoons sampled. The proportion of cocoons killed by parasitoids declined significantly with P. erichsonii density, while predation rates increased under heavily infested trees. Overall, the proportion of cocoons killed by parasitoids and predators did not vary with sawfly density.
5. Results indicate that components of host vigour, herbivore performance and natural enemy guilds exhibit substantial spatial heterogeneity among trees within plantations of exotic Larix trees. Moreover, individual larch can tolerate repeated oviposition and herbivory without a rapid loss in shoot production. The potential for host plant physiological tolerance to herbivory to interact with natural enemy population dynamics and behaviour so as to stabilize herbivore population patterns is discussed.