Phenological diversity in the interactions between winter moth (Operophtera brumata) larvae and parasitoid wasps in sub-arctic mountain birch forest

Population cycles of the winter moth (Operophtera brumata) in sub-arctic coastal birch forests show high spatiotemporal variation in amplitude. Peak larval densities range from levels causing little foliage damage to outbreaks causing spatially extensive defoliation. Moreover, outbreaks typically occur at or near the altitudinal treeline. It has been hypothesized that spatiotemporal variation in O. brumata cycle amplitude results from climate-induced variation in the degree of phenological matching between trophic levels, possibly between moth larvae and parasitoids. The likelihood of mismatching phenologies between larvae and parasitoids is expected to depend on how specialized parasitoids are, both as individual species and as a guild, to attacking specific larval developmental stages (i.e. instars). To investigate the larval instar-specificity of parasitoids, we studied the timing of parasitoid attacks relative to larval phenology. We employed an observational study design, with sequential sampling over the larval period, along an altitudinal gradient harbouring a pronounced treeline outbreak of O. brumata. Within the larval parasitoid guild, containing seven species groups, the timing of attack by different groups followed a successional sequence throughout the moth's larval period and each group attacked 1-2 instars. Such phenological diversity within parasitoid guilds may lower the likelihood of climate-induced trophic mismatches between victim populations and many/all of their enemies. Parasitism rates declined with increasing altitude for most parasitoid groups and for the parasitoid guild as a whole. However, the observed spatiotemporal parasitism patterns provided no clear evidence for or against altitudinal mismatch between larval and parasitoid phenology.     

The impact of habitat fragmentation on trophic interactions of the monophagous butterfly <Emphasis Type="Italic">Polyommatus coridon</Emphasis>

Theory predicts that habitat fragmentation, including reduced area and connectivity of suitable habitat, changes multitrophic interactions. Species at the bottom of trophic cascades (host plants) are expected to be less negatively affected than higher trophic levels, such as herbivores and their parasitoids or predators. Here we test this hypothesis regarding the effects of habitat area and connectivity in a trophic system with three levels: first with the population size of the larval food plant Hippocrepis comosa, next with the population density of the monophagous butterfly species Polyommatus coridon and finally with its larval parasitism rate. Our results show no evidence for negative effects of habitat fragmentation on the food plant or on parasitism rates, but population density of adult P. coridon was reduced with decreasing connectivity. We conclude that the highly specialized butterfly species is more affected by habitat fragmentation than its larval food plant because of its higher trophic position. However, the butterfly host species was also more affected than its parasitoids, presumably because of lower resource specialization of local parasitoids which also frequently occur in alternative hosts. Therefore, conservation efforts should focus first on the most specialized species of interaction networks and second on higher trophic levels.     

Sources of variation in larval parasitism of two sympatrically outbreaking birch forest defoliators

1. Studies of insect communities rarely support the parasitoid–host regulation hypothesis. Spatio‐temporal variation in parasitoid prevalence due to complex food web interactions or abiotic factors may prevent parasitoids from regulating hosts. 2. We examined the relative contribution of spatial (altitude) and temporal (years) sources to total variation in parasitoid prevalence rates in outbreaks of Epirrita autumnata Borkhausen and Operophtera brumata Linnaeus populations. We tested whether prevalence rates of generalist parasitoids were correlated between sympatric host populations and to what extent any of the parasitoids were host density dependent. 3. Four larval parasitoids (two specialists and two generalists) exhibited significantly structured spatio‐temporal dynamics over years and altitudes. The prevalence rates of one of the generalists were spatio‐temporally correlated between the two host species, while for the other they were not. 4. Three parasitoids showed tendencies for direct or delayed positive density dependence as expected from numerical and functional responses to their hosts. However, the effects were weak and minute compared to the variation attributed to year and altitude. 5. We conclude that unknown aspects of the larval parasitoid ecology that co‐vary with altitude and year in the study system dominate their prevalence dynamics and thus act to hinder density‐dependent responses that could potentially regulate host populations.     

Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20 year case study

Species interactions have a spatiotemporal component driven by environmental cues, which if altered by climate change can drive shifts in community dynamics. There is insufficient understanding of the precise time windows during which inter‐annual variation in weather drives phenological shifts and the consequences for mismatches between interacting species and resultant population dynamics—particularly for insects. We use a 20 year study on a tri‐trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum platanoidis and Periphyllus testudinaceus and their hymenopteran parasitoids. Using a sliding window approach, we assess climatic drivers of phenology in all three trophic levels. We quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts and parasitoids, and then model the impacts of these mismatches, direct weather effects and density dependence on local‐scale aphid population dynamics. Warmer temperatures in mid‐March to late‐April were associated with advanced sycamore budburst, parasitoid attack and (marginally) D. platanoidis emergence. The precise time window during which spring weather advances phenology varies considerably across each species. Crucially, warmer temperatures in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates thus generates marked shifts in the relative timing of spring events across trophic levels and mismatches in the phenology of interacting species. Despite this, we found no evidence that aphid population growth rates were adversely impacted by the magnitude of mismatch with their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong density dependence effects occurred in both aphid species and probably buffered populations, through density‐dependent compensation, from adverse impacts of the marked inter‐annual climatic variation that occurred during the study period. These findings explain the resilience of aphid populations to climate change and uncover a key mechanism, warmer winter temperatures delaying insect phenology, by which climate change drives asynchronous shifts between interacting species.     

Warming counteracts defoliation‐induced mismatch by increasing herbivore‐plant phenological synchrony

Climate change is altering phenology; however, the magnitude of this change varies among taxa. Compared with phenological mismatch between plants and herbivores, synchronization due to climate has been less explored, despite its potential implications for trophic interactions. The earlier budburst induced by defoliation is a phenological strategy for plants against herbivores. Here, we tested whether warming can counteract defoliation‐induced mismatch by increasing herbivore‐plant phenological synchrony. We compared the larval phenology of spruce budworm and budburst in balsam fir, black spruce, and white spruce saplings subjected to defoliation in a controlled environment at temperatures of 12, 17, and 22°C. Budburst in defoliated saplings occurred 6–24 days earlier than in the controls, thus mismatching needle development from larval feeding. This mismatch decreased to only 3–7 days, however, when temperatures warmed by 5 and 10°C, leading to a resynchronization of the host with spruce budworm larvae. The increasing synchrony under warming counteracts the defoliation‐induced mismatch, disrupting trophic interactions and energy flow between forest ecosystem and insect populations. Our results suggest that the predicted warming may improve food quality and provide better growth conditions for larval development, thus promoting longer or more intense insect outbreaks in the future.     

Effects of landscape context on herbivory and parasitism at different spatial scales

Local community structure and interactions have been shown to depend partly on landscape context. In this paper we tested the hypothesis that the spatial scale experienced by an organism depends on its trophic level. We analyzed plant-herbivore and herbivore-parasitoid interactions in 15 agricultural landscapes differing in structural complexity using the rape pollen beetle ( Meligethes aeneus ), an important pest on oilseed rape ( Brassica napus ), and its parasitoids. In the very center of each landscape a patch of potted rape plants was placed in a grassy field margin strip for standardized measurement. Percent non-crop area of landscapes was negatively related to plant damage caused by herbivory and positively to the herbivores' larval mortality resulting from parasitism. In a geographic scale analysis, we quantified the structure of the 15 landscapes for eight circular sectors ranging from 0.5 to 6 km diameter. Correlations between parasitism and non-crop areas as well as between herbivory and non-crop area were strongest at a scale of 1.5 km, thereby not supporting the view that higher trophic levels experience the world at a larger spatial scale. However, the predictive power of non-crop area changed only slightly for herbivory, but greatly with respect to parasitism as scales from 0.5 to 1.5 km and from 1.5 to 6 km diameter increased. Furthermore, the effect of non-crop area tended to be stronger in parasitism than herbivory suggesting a greater effect of changes in landscape context on parasitoids. This is in support of the general idea that higher trophic levels should be more susceptible to disturbance.     

The slow‐growth high‐mortality hypothesis: direct experimental support in a leafmining fly

1. Based on the slow‐growth high‐mortality (SGHM) hypothesis, which predicts that prolonged larval development increases mortality from their natural enemies, studies have often assumed that low quality of plants that slows larval development would function as a defence against insect herbivores. However, empirical support for the SGHM hypothesis has been limited, especially in natural and ecologically relevant contexts. 2. In a leafminer Amauromyza flavifrons Meigen (Agromyzidae, Diptera), the SGHM hypothesis was tested along with four other hypotheses (e.g. prey size, mine appearance, density‐dependent parasitism, and plant quality hypotheses) to control for spurious associations between development time and parasitism that are primarily driven by other larval traits. Two host plant species, Saponaria officinalis and Silene latifolia, were grown under varying nitrogen levels, and leafminers developing on these plants were exposed to, or protected from, a natural assembly of parasitoids across the entire course of larval development. 3. On both host plant species, leafminers that survived to an adult stage in the presence of parasitoids had a shorter development time than those in the absence of parasitoids, indicating that parasitoids disproportionately kill leafminers with longer larval development. The results provided concrete evidence for the SGHM hypothesis within the natural ecological context for these interacting species. Moreover, reduced plant quality was associated with higher larval mortality on Sa. officinalis only in the presence of parasitoids, suggesting that low quality could function as indirect plant resistance via SGHM under some tri‐trophic interactions.     

Landscape geometry and travelling waves in the larch budmoth

Travelling waves in cyclic populations refer to temporal shifts in peak densities moving across space in a wave‐like fashion. The epicentre hypothesis states that peak densities begin in specific geographic foci and then spread into adjoining areas. Travelling waves have been confirmed in a number of population systems, begging questions about their causes. Herein we apply a newly developed statistical technique, wavelet phase analysis, to historical data to document that the travelling waves in larch budmoth (LBM) outbreaks arise from two epicentres, both located in areas with high concentrations of favourable habitat. We propose that the spatial arrangement of the landscape mosaic is responsible for initiating the travelling waves. We use a tri‐trophic model of LBM dynamics to demonstrate that landscape heterogeneity (specifically gradients in density of favourable habitat) alone, is capable of inducing waves from epicentres. Our study provides unique evidence of how landscape features can mould travelling waves.     

Food web associations and effect of trophic resources and environmental factors on parasitoids expanding their host range into non‐native hosts

Trophic interactions and environmental conditions determine the structure of food webs and the host expansion of parasitoids into novel insect hosts. In this study, we investigate plant–insect–parasitoid food web interactions, specifically the effect of trophic resources and environmental factors on the presence of the parasitoids expanding their host range after the invasion of Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae). We also consider potential candidates for biological control of this non‐native pest. A survey of larval stages of Plusiinae (Lepidoptera: Noctuidae) and their larval parasitoids was conducted in field and vegetable greenhouse crops in 2009 and 2010 in various locations of Essex and Chatham‐Kent counties in Ontario, Canada. Twenty‐one plant–host insect–host parasitoid associations were observed among Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), C. chalcites, and larval parasitoids in three trophic levels of interaction. Chrysodeixis chalcites, an old‐world species that had just arrived in the region, was the most common in our samples. The larval parasitoids Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae), Cotesia vanessae (Reinhard), Cotesia sp., Microplitis alaskensis (Ashmead), and Meteorus rubens (Nees) (all Hymenoptera: Braconidae) expanded their host range into C. chalcites changing the structure of the food web. Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae) was the most common parasitoid of T. ni that was not found in the invasive species. Plant species, host abundance, and agro‐ecosystem were the most common predictors for the presence of the parasitoids expanding their host range into C. chalcites. Our results indicate that C. sonorensis, C. vanessae, and C. floridanum should be evaluated for their potential use in biological control of C. chalcites and T. ni.     

Travelling wave dynamics and self-organization in a spatio-temporally structured population

We analyse spatial population dynamics showing that periodic or period-like chaotic dynamics produce self-organization structures, such as travelling waves. We suggest that self-organized patterns are associated with spatial synchrony patterns that often depend on geographical distance between subpopulations. The population dynamics also show statistical spatial autocorrelation patterns. We contrast our theoretical simulations with empirical data on annual damages in young sapling stands caused by voles. We conclude, on the basis of the periodicity, synchrony, and spatial autocorrelation patterns, and our simulation results, that vole dynamics represent travelling waves in population dynamics. We suggest that because such synchrony patterns are frequently observed in natural populations, spatial self-organization may be more common in population dynamics than reported in the literature.     

设施农业景观下破碎化麦田麦蚜及寄生蜂种群的最小适生面积

最小适生面积(MASH)指在一定的时空范围内物种能稳定存在的最小生境面积,它是种群生存力分析(PVA)的重要方法之一.本文采用基于种群数量-面积关系原理的MASH模型模拟了银川平原设施农业景观下破碎化麦田麦蚜、初寄生蜂与重寄生蜂种群发生的MASH.研究表明：密度 面积、增长速度-面积关系模型间存在反比例函数关系,不同物种存在的函数关系明显不同,尤其在不同营养级别的物种间,其函数关系差异更为明显.根据密度-面积关系,利用多项式回归模型计算了麦二叉蚜、麦长管蚜、燕麦蚜茧蜂、烟蚜茧蜂与蚜虫宽缘金小蜂的MASH,其营养级间的MASH差异显著.不同物种的MASH与营养级高低、体型大小、生境质量等有关.初寄生蜂最高的寄生率出现在800～1000 m²,可作为利用初寄生蜂自然控制麦蚜的依据,而不同营养级物种MASH差异可用于害虫的种群控制.     

Spatial aggregation across ephemeral resource patches in insect communities: an adaptive response to natural enemies?

Although an increase in competition is a common cost associated with intraspecific crowding, spatial aggregation across food-limited resource patches is a widespread phenomenon in many insect communities. Because intraspecific aggregation of competing insect larvae across, e.g. fruits, dung, mushrooms etc., is an important means by which many species can coexist (aggregation model of species coexistence), there is a strong need to explore the mechanisms that contribute to the maintenance of this kind of spatial resource exploitation. In the present study, by using Drosophila-parasitoid interactions as a model system, we tested the hypothesis whether intraspecific aggregation reflects an adaptive response to natural enemies. Most of the studies that have hitherto been carried out on Drosophila-parasitoid interactions used an almost two-dimensional artificial host environment, where host larvae could not escape from parasitoid attacks, and have demonstrated positive density-dependent parasitism risk. To test whether these studies captured the essence of such interactions, we used natural breeding substrates (decaying fruits). In a first step, we analysed the parasitism risk of Drosophila larvae on a three-dimensional substrate in natural fly communities in the field, and found that the risk of parasitism decreased with increasing host larval density (inverse density dependence). In a second step, we analysed the parasitism risk of Drosophila subobscura larvae on three breeding substrate types exposed to the larval parasitoids Asobara tabida and Leptopilina heterotoma. We found direct density-dependent parasitism on decaying sloes, inverse density dependence on plums, and a hump-shaped relationship between fly larval density and parasitism risk on crab apples. On crab apples and plums, fly larvae benefited from a density-dependent refuge against the parasitoids. While the proportion of larvae feeding within the fruit tissues increased with larval density, larvae within the fruit tissues were increasingly less likely to become victims of parasitoids than those exposed at the fruit surface. This suggests a facilitating effect of group-feeding larvae on reaching the spatial refuge. We conclude that spatial aggregation in Drosophila communities can at least in part be explained as a predator avoidance strategy, whereby natural enemies act as selective agents maintaining spatial patterns of resource utilisation in their host communities.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

Effects of simulated heat waves on an experimental community of pepper plants,green peach aphids and two parasitoid species

Heat waves – extended periods of abnormally hot weather – are predicted to increase in severity and frequency under climate change. The severity of heat waves should impact communities and food webs through effects on performance of individual species and through changes in the strength of interactions between them. This study tested the effects of severity of simulated heat waves, with daily maxima of either 32°C or 40°C, on a tritrophic food web consisting of plants, Capsicum anuum, aphids, Myzus persicae and two parasitoids, Aphidius matricariae and Aphelinus abdominalis. Osmolarity of plant sap (concentration of dissolved solids) was highest under 40°C heat waves, suggesting the presence of secondary plant compounds involved with stress responses. Population growth of aphids was lower under heat waves (both 32°C and 40°C daily maxima), compared to environments with periodic hot days. Development time of parasitoids was longer under heat waves. Heat waves decreased the proportion of winged aphids in the population. When both parasitoid species were present, impacts on aphid populations were greater in heat wave environments than environments with periodic hot days. When either parasitoid species was by itself, heat waves did not affect the interaction between parasitoids and aphids. Numbers of A. matricariae were reduced in heat wave environments, whereas numbers of A. abdominalis were not. In addition to direct effects on individual species, we also obtained indirect evidence for the effects of heat waves on the bottom–up effects of plant stress compounds on herbivore performance, and on the strength of inter and intra‐specific competition. Our results demonstrate that heat waves could have important effects on community structure, and on important, community‐level processes such as intra‐guild interactions and trophic cascades.     

High nymphal host density and mortality negatively impact parasitoid complex during an insect herbivore outbreak

Insect herbivore outbreaks frequently occur and this may be due to factors that restrict top-down control by parasitoids, for example, host-parasitoid asynchrony, hyperparasitization, resource limitation and climate. Few studies have examined hostparasitoid density relationships during an in sect herbivore outbreak in a n atural ecosystem with diverse parasitoids. We studied parasitization patterns of Cardiaspina psyllids during an outbreak in a Eucalyptus woodland. First, we established the trophic roles of the parasitoids through a species-specific multiplex PCR approach on mummies from which parasitoids emerged. Then, we assessed host-parasitoid density relationships across three spatial scales (leaf, tree and site) over one yeas We detected four endoparasitoid species of the family Encyrtidae (Hymenoptera);two primary parasitoid and one heteronomous hyperparasitoid Psyllaephagus species (the latter with female development as a primary parasitoid and male development as a hyperparasitoid), and the hyperparasitoid Coccidoctonuspsyllae. Parasitoid development was host-synchronized, although synchrony between sites appeared constrained during winter (due to temperature differences). Parasitization was predominantly driven by one primary parasitoid species and was mostly inversely host-density dependent across the spatial scales. Hyperparasitization by C. psyllae was psyllid-density dependent at the site scale, however, this only impacted the rarer primary parasitoid. High larval parasitoid mortality due to density-dependent nymphal psyllid mortality (a consequence of resource limitation) compounded by a summer heat wave was incorporated in the assessment and resulted in density independence of host-parasitoid relationships. As such, high larval parasitoid mortality during insect herbivore outbreaks may contribute to the absence of host density-dependent parasitization during outbreak events.     

Plankton time — space dynamics in German Bight — a systems approach

Summary Long term continuous plankton measurements at Helgoland (North Sea) have provided a set of data which could be used for ecological functional analysis with respect to prey predator theory. Local dynamics display trophic feedback between selected populations. Phytoplankton, small copepods, Noctiluca miliaris, Pleurobrachia pileus and Beroe gracilis conform with theoretical assumptions. The functional relationships are less significant in averaged population dynamics compared with single ear processes. The local prey-predator cycles are to be understood as population waves travelling through German Bight. Such population waves over an area of 18 000 km² have been investigated and are displayed for the above given zooplankton populations as computer graphics and analysed in their progression for the population of P. pileus.     

Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer

Host plant nutritional quality can directly and indirectly affect the third trophic levels. The aphid–parasitoid relationship provides an ideal system to investigate tritrophic interactions (as the parasitoids are completely dependent for their development upon their hosts) and assess the bottom up forces operating at different concentrations of nitrogen applications. The effects of varying nitrogen fertilizer on the performance of Aphidius colemani (V.) reared on Sitobion avenae (F.) and Aphidius rhopalosiphi (D.) reared on Rhopalosiphum padi (L.) were measured. Parasitism and percent emergence of parasitoids were positively affected by nitrogen fertilizer treatments while developmental duration (egg, larval, and pupal stages) was not affected by increasing nitrogen inputs. In males and females of both parasitoid species, adult longevity increased with the increasing nitrogen fertilizer. Hind tibia length and mummy weight of both parasitoid species increased with nitrogen fertilizer concentrations, as a result of larger aphids. This study showed that nitrogen application to the soil can have important consequences for aboveground multitrophic interactions.     

Climate change effects on migration phenology may mismatch brood parasitic cuckoos and their hosts

Phenological responses to climate change vary among taxa and across trophic levels. This can lead to a mismatch between the life cycles of ecologically interrelated populations (e.g. predators and prey), with negative consequences for population dynamics of some of the interacting species. Here we provide, to our knowledge, the first evidence that climate change might disrupt the association between the life cycles of the common cuckoo (Cuculus canorus), a migratory brood parasitic bird, and its hosts. We investigated changes in timing of spring arrival of the cuckoo and its hosts throughout Europe over six decades, and found that short-distance, but not long-distance, migratory hosts have advanced their arrival more than the cuckoo. Hence, cuckoos may keep track of phenological changes of long-distance, but not short-distance migrant hosts, with potential consequences for breeding of both cuckoo and hosts. The mismatch to some of the important hosts may contribute to the decline of cuckoo populations and explain some of the observed local changes in parasitism rates of migratory hosts.     

Host–parasitoid interaction as affected by interkingdom competition

Although still underrepresented in ecological research, competitive interactions between distantly related organisms (so-called “interkingdom competition”) are expected to be widespread in various ecosystems, with yet unknown consequences for, e.g. trophic interactions. In the model host–parasitoid system Drosophila melanogaster–Asobara tabida, toxic filamentous fungi have been shown to be serious competitors that critically affect the density-dependent survival of host Drosophila larvae. This study investigates the extent to which the competing mould Aspergillus niger affects key properties of the well-studied Drosophila–parasitoid system and how the host–parasitoid interaction influences the microbial competitor. In contrast to slightly positive density-dependent host mortality under mould-free conditions, competing A. niger mediated a strong Allee effect for parasitised larvae, i.e. mortality decreased with increasing larval density. It was found that the common toxic fungal metabolite kojic acid is not responsible for higher death rates in parasitised larvae. Single parasitised Drosophila larvae were less harmful to fungal reproduction than unparasitised larvae, but this effect vanished with an increase in larval density. As predicted from the negative effect of fungi on host survival and thus on parasitoid fitness at low larval densities, A. tabida females spent less time foraging in fungus-infested patches. Interestingly, even though high host larval densities increased host survival, parasitoids still reduced their search efforts in fungus-infested patches, indicating a benefit for host larvae from feeding in the presence of noxious mould. Thus, this experimental study provides evidence of the potentially important role of interkingdom competition in determining trophic interactions in saprophagous animal communities and the dynamics of both host–parasitoid and microbial populations.     

Larval parasitism rate increases in herbivore‐damaged trees: a field experiment with cyclic birch feeding moths

Indirect plant defence mechanisms enhance the effectiveness of natural enemies of herbivores. Herbivore‐induced plant volatiles (HIPVs) attract the parasitoids of insect herbivores as shown both in numerous choice tests conducted under laboratory conditions and in relatively few common‐garden setups in agro‐ecosystems. However, the importance of this indirect defence trait at higher levels of biological organization has yet to be investigated through natural field experiments. Here, we report a field experiment of larval parasitism of two cyclic geometrid defoliators in herbivore‐damaged and fairly intact mountain birch Betula pubescens ssp. czerepanovii under natural conditions. Parasitism rates in larvae of the autumnal (Epirrita autumnata) and winter moth (Operophtera brumata) exposed for 30 h on defoliated trees were more than twice as high as those on control trees. This finding indicates that hymenopteran parasitoids were attracted to previously defoliated trees by some cues from the host plants, HIPVs being the most likely candidates. The third trophic level should thus be considered in natural plant herbivore interactions. Furthermore, parasitoids and food resources are key factors in the population regulation of forest insect pests, and indirect plant defences could be important in their interactions. Our research also emphasizes the quality of control treatments in field experiments, since immediate plant responses easily obscure the results as soon as control trees become infested by herbivorous insects.