Compensation behaviour by insect herbivores and natural enemies: its influence on community structure

Insect herbivores feeding on low-quality plants often compensate by increasing their consumption of plant tissue. This usually results in a longer developmental time leading to a higher vulnerability to natural enemies. This has been termed the slow-growth, high-mortality hypothesis. To explore how compensation may shape the species composition of herbivore and natural enemy populations, we present a mathematical model of a tri-trophic system incorporating both the nutritional quality of plants and herbivores, and the compensatory ability of herbivores and their natural enemies. Using this model we predict the abundance of herbivores and natural enemies, and some characteristics of the composition of species of insect communities along a gradient of plant nutritional quality. Specifically, we make the following predictions: 1) In the absence of natural enemies, the abundance of the juvenile herbivores increases with plant quality, and only highly compensating herbivores persist at low plant nutritional quality. 2) If natural enemies are present, the abundance of the juvenile herbivores decreases with increasing plant quality due to more effective suppression by the natural enemies. Poorly compensating herbivores increase while their highly compensating counterparts decrease with lowered plant quality. 3) When the plants have low nutritional quality, natural enemies will only persist when either very highly compensating herbivores are present or if the natural enemy itself is highly compensating. 4) The abundance of adult herbivores in a community with natural enemies can either increase or decrease with increasing plant quality depending on the compensatory abilities of herbivores and natural enemies.     

Plant defence signals and Batesian mimicry

In a game theory context, we investigated conditions for an evolutionarily stable equilibrium of defended, signalling plants, and plants mimicking these signals – that is, conditions for a stable mimicry complex. We modelled this in three steps. First, we analysed conditions for selection for defended, signalling plants, in a population of undefended plants. Second, we analysed conditions for when mimicking plants can invade a population of defended, signalling plants, leading to a stable equilibrium between the two strategies. Third, we analysed how sampling of signalling plants by herbivores affects the equilibrium between the strategies. The predictions show that mimicry of plant defence signals may be common, and even imperfect mimics could invade a population of defended, signalling plants. Whether the latter prediction holds or not depends on how herbivores generalize over signals, and on the length of their avoidance sequence'. The length of the avoidance sequence is the number of signalling plants that a herbivore avoids to attack, after attacking a defended plant. If herbivores always sample signalling plants, then mimicry cannot evolve, whereas if herbivores have a long avoidance sequence, this may allow selection even for imperfect mimics.     

Host plant defences and voltinism in European butterflies

Abstract.  1. With respect to seasonal availability for herbivores, plants defended by synthesising qualitative compounds differ from those protected by accumulation of quantitative macromolecules, leaf toughness, and low water and/or nutrient content. While the palatability of the former plants remains relatively constant during the season, the palatability of the latter group decreases with leaf age.
2. It was hypothesised that in seasonal temperate environments, quantitative plant defences should restrict the annual numbers of insect generations. To test this hypothesis, European butterflies were used as a model, both non-corrected regressions and tests controlling for phylogeny were carried out, and potentially confounding factors such as body size or occurrence in short-season environments were treated as covariables.
3. Non-phylogenetically controlled regressions corroborated that butterflies feeding on quantitatively protected hosts (woody plants + grasses) form fewer generations than species feeding on qualitatively protected forbs. Plant defences fitted voltinism better than butterfly size, and remained significant even after controlling for short seasons. Using independent contrasts, feeding on woody plants plus grasses, and feeding on woody plants only, predicted fewer generations. These patterns, however, applied exclusively for foliage-feeding species.
4. The association between plant defences and voltinism represents a hitherto overlooked pattern in the ecology of temperate herbivores. It may explain why large insects tend to form fewer generations and feed on structurally complex hosts, and why some species remain monovoltine although they are not restricted by short season.     

How can automimicry persist when predators can preferentially consume undefended mimics?

It is common for species that possess toxins or other defences to advertise these defences to potential predators using aposematic ("warning") signals. There is increasing evidence that within such species, there are individuals that have reduced or non-existent levels of defence but still signal. This phenomenon (generally called automimicry) has been a challenge to evolutionary biologists because of the need to explain why undefended automimics do not gain such as a fitness advantage by saving the physiological costs of defence that they increase in prevalence within the population, hence making the aposematic signal unreliable. The leading theory is that aposematic signals do not stop all predatory attacks but rather encourage predators to attack cautiously until they have identified the defence level of a specific individual. They can then reject defended individuals and consume the undefended. This theory has recently received strong empirical support, demonstrating that high-accuracy discrimination appears possible. However, this raises a new evolutionary problem: if predators can perfectly discriminate the defended from the undefended and preferentially consume the latter, then how can automimicry persist? Here, we present four different mechanisms that can allow non-trivial levels of automimics to be retained within a population, even in the extreme case where predators can differentiate defended from undefended individuals with 100% accuracy. These involve opportunity costs to the predator of sampling carefully, temporal fluctuation in predation pressure, predation pressure being correlated with the prevalence of automimicry, or developmental or evolutionary constraints on the availability of defence. These mechanisms generate predictions as to the conditions where we would expect aposematically signalling populations to feature automimicry and those where we would not.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.     

Nutrient enrichment and food chains: can evolution buffer top-down control?

We show how evolutionary dynamics can alter the predictions of classical models of the effects of nutrient enrichment on food webs. We compare an ecological nutrient-plant-herbivore food-chain model without evolution with the same model, including herbivore evolution, plant evolution, or both. When only herbivores are allowed to evolve, the predictions are similar to those of the ecological model without evolution, i.e., plant biomass does not change with nutrient addition. When only plants evolve, nutrient enrichment leads to an increase in the biomass of all compartments. In contrast, when plants and herbivores are allowed to coevolve, although these two classical patterns are common, a wide variety of other responses is possible. The form of the trade-offs that constrain evolution of the two protagonists is then critical. This stresses the need for experimental data on phenotypic traits, their costs and their influence on the interactions between organisms and the rest of the community.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

Plant silicon effects on insect feeding dynamics are influenced by plant nitrogen availability

Although there is growing evidence that silicon (Si)‐based plant defenses effectively reduce both the palatability and digestibility of leaves, and thus impact nutrient assimilation by insect herbivores, much less is known about how this is affected by extrinsic and intrinsic factors. For example, do herbivores exhibit compensatory feeding on poor‐quality diets with Si or are Si defenses less effective in agroecosystems where high N availability increases plant quality? To investigate the interactive effects of N and Si on insect feeding, we conducted insect performance and compensatory feeding bioassays using maize, Zea mays L. (Poaceae), and the true armyworm, Pseudeletia unipuncta Haworth (Lepidoptera: Noctuidae). In the performance assay, the addition of Si alone resulted in increased larval mortality compared with the controls, likely because early instars with poorly developed mandibles could not feed effectively. However, larvae fed on plants treated with both Si and N survived better than on plants treated with Si only, although pupal mass did not differ between treatments. In our compensatory assay, Si addition reduced maize consumption, but increased both armyworm approximate digestibility and N assimilation efficiency, suggesting that enhanced post‐ingestion feeding physiology, rather than compensatory food intake, could have accounted for the lack of Si effects on pupal weight. Overall, our results demonstrate that, similar to other chemical and mechanical defenses, the effectiveness of plant Si defense is influenced by plant nutrient status and consumer compensatory ability.     

Linking herbivore-induced defences to population dynamics

1. Theoretical studies have shown that inducible defences have the potential to affect population stability and persistence in bi‐ and tritrophic food chains. Experimental studies on such effects of prey defence strategies on the dynamics of predator–prey systems are still rare. We performed replicated population dynamics experiments using the herbivorous rotifer Brachionus calyciflorus and four strains of closely related algae that show different defence responses to this herbivore. 2. We observed herbivore populations to fluctuate at a higher frequency when feeding on small undefended algae. During these fluctuations minimum rotifer densities remained sufficiently high to ensure population persistence in all the replicates. The initial growth of rotifer populations in this treatment coincided with a sharp drop in algal density. Such a suppression of algae by herbivores was not observed in the other treatments, where algae were larger due to induced or permanent defences. In these treatments we observed rotifer population densities to first rise and then decline. The herbivore went extinct in all replicates with large permanently defended algae. The frequency of herbivore extinctions was intermediate when algae had inducible defences. 3. A variety of alternative mechanisms could explain differential herbivore persistence in the different defence treatments. Our analysis showed the density and fraction of highly edible algal particles to better explain herbivore persistence and extinctions than total algal density, the fraction of highly inedible food particles or the accumulation of herbivore waste products or autotoxins. 4. We argue that the rotifers require a minimum fraction and density of edible food particles for maintenance and reproduction. We conjecture that induced defences in algae may thus favour larger zooplankton species such as Daphnia spp. that are less sensitive to shifts in their food size spectrum, relative to smaller zooplankton species, such as rotifers and in this way contributes to the structuring of planktonic communities.     

A herbivore that manipulates plant defence

Phytopathogens and herbivores induce plant defences. Whereas there is evidence that some pathogens suppress these defences by interfering with signalling pathways involved in the defence, such evidence is scarce for herbivores. We found that the invasive spider mite Tetranychus evansi suppresses the induction of the salicylic acid and jasmonic acid signalling routes involved in induced plant defences in tomato. This was reflected in the levels of inducible defence compounds, such as proteinase inhibitors, which in mite-infested plants were reduced to even lower levels than the constitutive levels in herbivore-free plants. Additionally, the spider mite suppressed the release of inducible volatiles, which are implicated in plant defence. Consequently, the mites performed much better on previously attacked plants than on non-attacked plants. These findings provide a new perspective on plant-herbivore interactions, plant protection and plant resistance to invasive species.     

Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators

Pollinators and herbivores can both affect the evolutionary diversification of plant reproductive traits. However, plant defences frequently alter antagonistic and mutualistic interactions, and therefore, variation in plant defences may alter patterns of herbivore‐ and pollinator‐mediated selection on plant traits. We tested this hypothesis by conducting a common garden field experiment using 50 clonal genotypes of white clover (Trifolium repens) that varied in a Mendelian‐inherited chemical antiherbivore defence—the production of hydrogen cyanide (HCN). To evaluate whether plant defences alter herbivore‐ and/or pollinator‐mediated selection, we factorially crossed chemical defence (25 cyanogenic and 25 acyanogenic genotypes), herbivore damage (herbivore suppression) and pollination (hand pollination). We found that herbivores weakened selection for increased inflorescence production, suggesting that large displays are costly in the presence of herbivores. In addition, herbivores weakened selection on flower size but only among acyanogenic plants, suggesting that plant defences reduce the strength of herbivore‐mediated selection. Pollinators did not independently affect selection on any trait, although pollinators weakened selection for later flowering among cyanogenic plants. Overall, cyanogenic plant defences consistently increased the strength of positive directional selection on reproductive traits. Herbivores and pollinators both strengthened and weakened the strength of selection on reproductive traits, although herbivores imposed ~2.7× stronger selection than pollinators across all traits. Contrary to the view that pollinators are the most important agents of selection on reproductive traits, our data show that selection on reproductive traits is driven primarily by variation in herbivory and plant defences in this system.     

Instar-specific sensitivity of specialist Manduca sexta larvae to induced defences in their host plant Nicotiana attenuata

1. The time delay associated with the activation of induced defences is thought to be a liability for this type of defence because it allows herbivores to remove biomass before the defence is fully induced. When defences are costly and plants grow with competitors, however, it may be more advantageous not to induce defences too fast and motivate the herbivore to move to the neighbour when it is most voracious. 2. Such a strategy can only work when the costs for the herbivore of moving to a neighbouring plant are smaller than the costs of staying on a fully induced plant. For lepidopteran herbivores, both the sensitivity to induced defences and the costs of moving may vary considerably between instars and this variation may constrain the plant's defensive opportunities. 3. This study was designed to examine whether the cost of moving, mimicked by a starvation period of 8 h, was larger than the cost of staying on a fully induced plant for each larval instar of the specialist Manduca sexta feeding on induced and control tissues of Nicotiana attenuata. 4. For first‐ and second‐instar larvae, the costs of moving were larger than the costs of staying on a fully induced plant. In contrast, feeding on induced plant material retarded development in third‐instar larvae more than did starvation, indicating that in this instar the costs of leaving are smaller than the costs of staying on an induced plant. More than 98% of the lifetime leaf mass consumed by a M. sexta larva is consumed during the fourth and fifth instars, and during these instars larval development was not affected by either induced defences or starvation. Thus the third instar, the stage just before larvae cause the majority of damage, represents a window of sensitivity to induced defences during which larvae can be motivated to change plants. 5. These results suggest that N. attenuata plants, which commonly compete with conspecifics in nature, have the opportunity to manipulate the behaviour of the specialist herbivore M. sexta to minimise the fitness effects of inducing defences when these defences are most costly, i.e. when plants grow under intraspecific competition.     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Predator-induced defense makes Daphnia more vulnerable to parasites

Inducible defensive traits against herbivores or predators are widespread in plants and animals. Theory predicts that defended morphs have greater fitness in the presence of predators, but lower fitness than undefended morphs in the absence of predators. If such costs did not exist, then a constitutively defended morph would be favored by natural selection; yet, evidence for such costs has been elusive. Our current work reveals a significant cost to inducible defenses. Using the waterflea (Daphnia) model system, we show that induced defended morphs are significantly more vulnerable to infection by a virulent yeast parasite than undefended morphs. In two independent experiments, the proportion of successful infections and the number of parasite spores were higher among defended versus undefended Daphnia. Thus, by demonstrating a previously unknown and environmentally relevant cost to inducible defenses, this study enhances our understanding of adaptive phenotypic plasticity and its evolution.     

Herbivory and Stoichiometric Feedbacks to Primary Production

Established theory addresses the idea that herbivory can have positive feedbacks on nutrient flow to plants. Positive feedbacks likely emerge from a greater availability of organic carbon that primes the soil by supporting nutrient turnover through consumer and especially microbially-mediated metabolism in the detrital pool. We developed an entirely novel stoichiometric model that demonstrates the mechanism of a positive feedback. In particular, we show that sloppy or partial feeding by herbivores increases detrital carbon and nitrogen allowing for greater nitrogen mineralization and nutritive feedback to plants. The model consists of differential equations coupling flows among pools of: plants, herbivores, detrital carbon and nitrogen, and inorganic nitrogen. We test the effects of different levels of herbivore grazing completion and of the stoichiometric quality (carbon to nitrogen ratio, C:N) of the host plant. Our model analyses show that partial feeding and plant C:N interact because when herbivores are sloppy and plant biomass is diverted to the detrital pool, more mineral nitrogen is available to plants because of the stoichiometric difference between the organisms in the detrital pool and the herbivore. This model helps to identify how herbivory may feedback positively on primary production, and it mechanistically connects direct and indirect feedbacks from soil to plant production.     

Root herbivory induces an above-ground indirect defence

Indirect plant defences have largely been studied within the scope of above‐ground interactions. Here we provide novel evidence that root herbivory can induce an above‐ground indirect defence. Cotton plants (Gossypium herbaceum) exposed to root‐feeding wireworms (Agriotes lineatus) increased their foliar extrafloral nectar production ten‐fold in comparison to undamaged control plants. Mechanical root damage also yielded an increase in nectar production. In nature, extrafloral nectar production allows plants to recruit predators, which in turn protect the plant against above‐ground insect herbivores. Our results show that root‐feeding herbivores may alter such above‐ground defensive interactions.     

Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems

• 1 Below‐ground organisms influence above‐ground interactions in both natural and agricultural ecosystems. Among the most important below‐ground organisms are mycorrhizal fungi, comprising ubiquitous and ancient plant mutualists that have significant effects on plant growth and fitness mediated by resource exchange with plants. In the present study, we focus on the effects of arbuscular mycorrhizal fungi (AMF) on crop defence against insect pests.
• 2 AMF alter the availability of resources used by crop plants to manufacture defences against pests and to compensate for pest damage. However, AMF also provide plants with nutrients that are known to increase insect performance. Through potentially opposing effects on plant nutritional quality and defence, mycorrhizal fungi can positively or negatively affect pest performance.
• 3 Additionally, AMF may directly affect gene expression and plant defence signalling pathways involved in the construction and induction of plant defences, and these effects are apparently independent of those caused by nutrient availability. In this way, AMF may still influence plant defences in the fertilized and highly managed systems typical of agribusiness.
• 4 Because AMF can affect plant tolerance to pest damage, they may have a significant impact on the shape of damage–yield relationships in crops. Potential mechanisms for this effect are suggested.
• 5 We highlight the need for continuing research on the effects of AMF identity and the abundance on crop defences and tolerance to pest attack. Much work is needed on the potential effects of mycorrhizal colonization on plant signalling and the induction of direct and indirect defences that may protect against pest damage.

     

Herbivory and plant tolerance: experimental tests of alternative hypotheses involving non‐substitutable resources

A mechanistic understanding of the highly variable effects of herbivores on plant production in different ecosystems remains a major challenge. To explain these patterns, the compensatory continuum hypothesis (CCH) predicts plants to compensate for defoliation when resources are abundant, whereas the growth rate hypothesis (GRH) makes the opposite claim of high herbivory tolerance under resource‐poor conditions. The limiting resource model (LRM) tries to reconcile this dichotomy by incorporating the indirect effects of herbivores on plant resources and predicts that the potential for plant compensation is dependent upon whether, and how, herbivory influences limiting resources. Although extensively evaluated in laboratory monocultures, it remains uncertain whether these models can also explain the response of heterogeneous and multi‐species natural plant communities to defoliation. Here we investigate community‐wide plant response to defoliation and report data from a field experiment in the arid and primarily water‐limited Trans‐Himalayan grazing ecosystem in northern India involving clipping, irrigation and nutrient‐feedback with herbivore dung. Without nutrient‐feedback, plants compensated for defoliation in absence of irrigation but failed to compensate under irrigation. Whereas, in the presence of nutrient‐feedback plants compensated for defoliation when irrigated. This divergent pattern is not consistent with the CCH and GRH, and is only partially explained by the LRM. Instead, these pluralistic results are consistent with the hypothesis that herbivory may alter the relative strengths of water and nutrient limitation since irrigation increased root:shoot ratio in absence of fertilization in unclipped plots, but not in the corresponding clipped plots. So, herbivory appears to increase relative strength of nutrient‐limitation for plants that otherwise seem to be primarily water‐limited. Extending the LRM framework to include herbivore‐mediated transitions between water and nutrient‐limitation may clarify the underlying mechanisms that modulate herbivory‐tolerance under different environmental conditions.     

Caterpillars on the run – induced defences create spatial patterns in host plant damage

Herbivores usually consume a mere fraction of available plant biomass. Spatial patterns in feeding damage may be attributable to induced defences by the host plant; a damaged plant reacts by lowering its nutritional value, thereby forcing herbivores to move on before food gets worse. In this study, we test this general hypothesis on a specific model system: caterpillars of the alpine butterfly Parnassius smintheus feeding on lance-leaved stonecrop Sedum lanceolatum. We first describe spatial patterns in host distribution and feeding damage within alpine meadows. We then use laboratory experiments to test a key assumption behind the proposed mechanisms: that the host plant exhibits an induced response with a negative impact on larval performance, and that this response is activated with a delay. Finally, we relate the patterns observed to the actual behaviour of Parnassius larvae.
Overall, we found the level of feeding damage to be low (on damaged plants, only 5% of all leaves were fed upon). Within meadows, both host plants and feeding damage were clumped at a small spatial scale. This pattern seemed directly explicable by the timing of the host's induced defence. Laboratory experiments revealed a delay of 1–2 d before the defence reached a level affecting larval performance, and wild larvae switch plants more quickly than this. A simulation model demonstrated that the spatial distribution of host plant damage can be generated by a simple random walk, based on the empirically observed step frequency, length and turning angles. Hence, as the most parsimonious explanation for the observed level and pattern of host plant damage, we offer a scenario where induced changes in host-plant quality limits the time spent per plant, but the herbivore moves throughout the landscape without any particular directionality.