Climate variation alters the synchrony of host–parasitoid interactions

Observed changes in mean temperature and increased frequency of extreme climate events have already impacted the distributions and phenologies of various organisms, including insects. Although some research has examined how parasitoids will respond to colder temperatures or experimental warming, we know relatively little about how increased variation in temperature and humidity could affect interactions between parasitoids and their hosts. Using a study system consisting of emerald ash borer (EAB), Agrilus planipennis, and its egg parasitoid Oobius agrili, we conducted environmentally controlled laboratory experiments to investigate how increased seasonal climate variation affected the synchrony of host–parasitoid interactions. We hypothesized that increased climate variation would lead to decreases in host and parasitoid survival, host fecundity, and percent parasitism (independent of host density), while also influencing percent diapause in parasitoids. EAB was reared in environmental chambers under four climate variation treatments (standard deviations in temperature of 1.24, 3.00, 3.60, and 4.79°C), while O. agrili experiments were conducted in the same environmental chambers using a 4 × 3 design (four climate variation treatments × 3 EAB egg densities). We found that EAB fecundity was negatively associated with temperature variation and that temperature variation altered the temporal egg laying distribution of EAB. Additionally, even moderate increases in temperature variation affected parasitoid emergence times, while decreasing percent parasitism and survival. Furthermore, percent diapause in parasitoids was positively associated with humidity variation. Our findings indicate that relatively small changes in the frequency and severity of extreme climate events have the potential to phenologically isolate emerging parasitoids from host eggs, which in the absence of alternative hosts could lead to localized extinctions. More broadly, these results indicate how climate change could affect various life history parameters in insects, and have implications for consumer–resource stability and biological control.     

Are aphid parasitoids from mild winter climates losing their winter diapause?

Temperature is both a selective pressure and a modulator of the diapause expression in insects from temperate regions. Thus, with climate warming, an alteration of the response to seasonal changes is expected, either through genetic adaptations to novel climatic conditions or phenotypic plasticity. Since the 1980s in western France, the winter guild of aphid parasitoids (Hymenoptera: Braconidae) in cereal fields has been made up of two species: Aphidius rhopalosiphi and Aphidius matricariae. The recent activity of two other species, Aphidius avenae and Aphidius ervi, during the winter months suggests that a modification of aphid parasitoid overwintering strategies has taken place within the guild. In this study, we first performed a field survey in the winter of 2014/15 to assess levels of parasitoid diapause incidence in agrosystems. Then, we compared the capacity of the four parasitoid species to enter winter diapause under nine different photoperiods and temperature conditions in the laboratory. As predicted, historically winter-active species (A. rhopalosiphi and A. matricariae) never entered diapause, whereas the species more recently active during winter (A. avenae and A. ervi) did enter diapause but at a low proportion (maximum of 13.4 and 11.2%, respectively). These results suggest rapid shifts over the last three decades in the overwintering strategies of aphid parasitoids in Western France, probably due to climate warming. This implies that diapause can be replaced by active adult overwintering, with potential consequences for species interactions, insect community composition, ecosystem functioning, and natural pest control.     

Influence of experimental warming and shading on host–parasitoid synchrony

As the climate warms, many species are showing altered phenology patterns, potentially disrupting synchrony between interacting species. Recent studies have documented disrupted synchrony in plant–herbivore and predator–prey interactions. However, studies investigating climate‐related asynchrony in host–parasitoid interactions and exploring the relative responses of interacting hosts and parasitoids to climate change are lacking. This is an important gap in knowledge given the ubiquity of insect parasitoids and their importance in influencing the abundance and dynamics of their hosts. In the threatened marsh fritillary butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae) and its specialized parasitoid, Cotesia bignellii (Hymenoptera: Braconidae) phenological synchrony (and consequently population fluctuations) are thought to be weather‐dependent. To assess the likely influence of climate and microenvironment change on synchrony between E. aurinia and C. bignellii, we experimentally manipulated the exposure of sensitive‐stage host larvae and parasitoid pupae to temperature (ambient or elevated) and shading (shaded or unshaded) regimes. We also analysed a 20‐year population dynamic dataset from the United Kingdom for E. aurinia to investigate whether population variations could be explained by interannual variations in the thermal and sunshine environment. Development times were affected significantly by the experimental temperature and shading treatments for E. aurinia but not for C. bignellii. However, the contrasting responses were insufficient to significantly affect host availability for parasitoids. In the field, thermal and sunshine conditions did not influence population fluctuations, and population variations across a large (UK‐wide) scale were uncorrelated. Changes to the thermal and sunshine environment of the magnitude investigated in our experiment and within the range experienced by wild E. aurinia populations over the last 20‐years thus seem unlikely to cause breakdown in host–parasitoid synchrony. We suggest that experiments investigating the mechanistic responses of interacting species to environmental change are needed to support the analysis and interpretation of observational data on species' phenology.     

Diapause research in insects: historical review and recent work perspectives

All organisms on Earth have evolved biological rhythms to face alternation of periods of favorable and unfavorable environmental conditions, at various temporal scales. Diapause is a state of seasonal dormancy adapted to recurring periods of adverse environmental conditions and triggered by biotic and abiotic factors that precede the arrival of these conditions. Several monographs already review the mechanisms of diapause expression in arthropods, from initiation to termination phases. Rather than adding another review to the literature on this topic, this paper primarily aims to link past concepts on seasonal strategies with new perspective on diapause research in arthropods. By focusing on insects, I examine the legacy of diapause history research in terrestrial arthropods since antiquity but mostly over the past 3 centuries, its contribution to the understanding of insect seasonal ecology, and I explore some of the reasons why it is still relevant to study diapause. I highlight some of the topical issues on which current work focuses to better understand and integrate arthropod diapause with their ecology, especially in the climate change context and for the provision of ecosystem services.     

Histories of host shifts and cospeciation among free‐living parasitoids of Rhagoletis flies

Host shifts by specialist insects can lead to reproductive isolation between insect populations that use different hosts, promoting diversification. When both a phytophagous insect and its ancestrally associated parasitoid shift to the same novel host plant, they may cospeciate. However, because adult parasitoids are free living, they can also colonize novel host insects and diversify independent of their ancestral host insect. Although shifts of parasitoids to new insect hosts have been documented in ecological time, the long‐term importance of such shifts to parasitoid diversity has not been evaluated. We used a genus of flies with a history of speciation via host shifting (Rhagoletis [Diptera: Tephritidae]) and three associated hymenopteran parasitoid genera (Diachasma, Coptera and Utetes) to examine cophylogenetic relationships between parasitoids and their host insects. We inferred phylogenies of Rhagoletis, Diachasma, Coptera and Utetes and used distance‐based cophylogenetic methods (ParaFit and PACo) to assess congruence between fly and parasitoid trees. We used an event‐based method with a free‐living parasitoid cost model to reconstruct cophylogenetic histories of each parasitoid genus and Rhagoletis. We found that the current species diversity and host–parasitoid associations between the Rhagoletis flies and parasitoids are the primary result of ancient cospeciation events. Parasitoid shifts to ancestrally unrelated hosts primarily occur near the branch tips, suggesting that host shifts contribute to recent parasitoid species diversity but that these lineages may not persist over longer time periods. Our analyses also stress the importance of biologically informed cost models when investigating the coevolutionary histories of hosts and free‐living parasitoids.     

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.     

Heat tolerance variation reveals vulnerability of tropical herbivore–parasitoid interactions to climate change

Assessing the heat tolerance (CTmax) of organisms is central to understand the impact of climate change on biodiversity. While both environment and evolutionary history affect CTmax, it remains unclear how these factors and their interplay influence ecological interactions, communities and ecosystems under climate change. We collected and reared caterpillars and parasitoids from canopy and ground layers in different seasons in a tropical rainforest. We tested the CTmax and Thermal Safety Margins (TSM) of these food webs with implications for how species interactions could shift under climate change. We identified strong influence of phylogeny in herbivore–parasitoid community heat tolerance. The TSM of all insects were narrower in the canopy and parasitoids had lower heat tolerance compared to their hosts. Our CTmax-based simulation showed higher herbivore–parasitoid food web instability under climate change than previously assumed, highlighting the vulnerability of parasitoids and related herbivore control in tropical rainforests, particularly in the forest canopy.     

Changes in function and temporal variation in a guild of gall‐parasitoids across a temperature gradient in Australian subtropical rainforest

Parasitoids play an important role in ecosystem functioning through their influence on herbivorous insect populations. Theoretical and experimental evidence suggest that increased species richness can enhance and stabilize ecosystem function. It is important to understand how richness‐driven functional relationships change across environmental gradients. We investigated how temperature affected the relationship between parasitoid richness and parasitism rate in a guild of gall‐parasitoids along an elevational gradient. We collected galls at 15 sites along five elevational gradients (between 762 m and 1145 m asl) on six occasions over a year. A total of 1902 insects, including 1593 parasitoids, were reared from 12 402 galls. Parasitism rate increased significantly with temperature on all sampling occasions, except December and February. We found a significant, positive richness–parasitism relationship. This relationship, however, was weaker at higher elevations which may be linked to decreased functional efficiency of parasitoids at lower temperatures. Temporal variability in parasitism rate and parasitoid richness were significantly related, regardless of temperature. A stable functional guild of this kind may provide a more reliable ecosystem service under environmental changes.     

Evolution of a physiological trade‐off in a parasitoid wasp: how best to manage lipid reserves in a warming environment

Ectothermic animals, especially insects, are probably the ones most affected, for better or worse, by variable thermic environment, for example in the case of global warming, as their metabolic rate is controlled by the ambient temperature. Parasitoid insects, at the third trophic level, are widely distributed worldwide, and they influence the population dynamics of their highly diverse insect hosts. An important feature of parasitoid wasps is their supposedly limited or non‐existent capacity to synthesize lipids during adulthood. As lipid level can be expected to determine whether they engage in maintenance or reproduction, parasitoid wasps are useful biological models for investigating how evolutionary trade‐offs in energy allocation to maintenance or reproduction are likely to alter in response to global climate change. To address this, we developed a state‐dependent stochastic dynamic programming model, which we parameterized using empirically derived data. The model shed light on the adaptive response of parasitoids with regard to three traits: activity rate, initial egg load, and egg production over the adult female's life span. We show that in a warmer climate, parasitoids devote smaller amounts of lipids to their reproductive effort and favour maintenance over reproduction. However, the bias towards maintenance is reduced when the parasitoids are able to adapt their activity rate to the features of their environment. This model could be tailored to a wide range of organisms with limited energy intake during their adult life.     

Autumn, winter and spring dynamics of aphid Sitobion avenae and parasitoid Aphidius rhopalosiphi interactions

The potential of parasitoids for aphid control during summer has been well documented. Few results are available on the impact of parasitoid populations on aphid hosts during autumn and winter and on the dynamics of their interactions during this period. The population development of Sitobion avenae, in Belgium, is analysed, from October to April, in the presence and absence of the parasitoid Aphidius rhopalosiphi. In the presence of parasitoids in winter, aphid populations decreased markedly and remained low at the beginning of spring. Induction of winter diapause in A. rhopalosiphi was observed during November at a mean temperature of 6.3°C and a decreasing photoperiod from 9.5–8.5 h of day light. A large range of A. rhopalosiphi mummy colourations, between dark and light, was noticed. This range of colouration did not allow a clear-cut distinction between diapausing and non-diapausing individuals of A. rhopalosiphi. The influence of seasonal weather and particularly temperature conditions on parasitoid mortality, strategy for overwintering and aphid population dynamics are discussed.     

Nutritional ecology of endoparasitic insects and their hosts: An overview

The impact of insect endoparasites (parasitoids) on the physiology and behaviour of their hosts is reviewed within the context of the nutritional ecology of the parasitoids and their hosts. Alterations in the consumption, utilization and allocation of food by parasitized hosts are common, as are internal changes in their metabolic physiology. Gregarious parasitoid species frequently increase feeding by their host larvae whereas solitary parasitoid species often reduce feeding and growth of their hosts. Many parasitoid-associated changes in host physiology and behaviour are interpreted to be of adaptive significance to parasitoids. Substantial circumstantial evidence suggests, and a few direct tests of such adaptive significance indicate, that parasitoids alter their hosts in ways beneficial to their own fitness. However, most of the changes in parasitized hosts are of unknown cause and undocumented significance to the parasitoids. Several relevant hypotheses are presented, and these require extensive evaluation (often requiring novel experimental approaches) before a thorough understanding of parasitoid nutritional ecology is established.     

Response of insect parasitism to elevation depends on host and parasitoid life-history strategies

How global warming will affect insect parasitoids and their role as natural enemies of insect pests is difficult to assess within a short period of time. Considering that elevation gradients can be used as analogues for global warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate and elevation in natural and semi-natural environments. We also explored various covariates that may explain the observed responses. Both parasitism rates and parasitoid species richness significantly decreased with increasing elevation. The decrease was greater for ectoparasitoids and parasitoids of ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse and extreme climatic conditions occurring at higher elevations. Although our results suggest an increase of parasitism with increasing temperature, other factors regulating herbivorous insects have to be considered before concluding that climate warming will lead to a decrease in pest density.     

Evolutionary ecology of the interactions between aphids and their parasitoids

Many organisms, including entomopathogenous fungi, predators or parasites, use aphids as ressources. Parasites of aphids are mostly endoparasitoid insects, i.e. insects which lay eggs inside the body of an other insect which will die as a result of their development. In this article, we review the consequences of the numerous pecularities of aphid biology and ecology for their endoparasitoids, notably the Aphidiinae (Hymenoptera: Braconidae). We first examine the various mechanisms used by aphids for defence against these enemies. We then explore the strategies used by aphidiine parasitoids to exploit their aphid hosts. Finally, we consider the responses of both aphids and parasitoids to ecological constraints induced by seasonal cycles and to environmental variations linked to host plants and climate. The fundamental and applied interest of studying these organisms is discussed.     

Effects of climate warming on host–parasitoid interactions

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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.     

Host ontogeny determines parasitoid use of a forest caterpillar

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

Tracking the elusive history of diversification in plant–herbivorous insect–parasitoid food webs: insights from figs and fig wasps

The food webs consisting of plants, herbivorous insects and their insect parasitoids are a major component of terrestrial biodiversity. They play a central role in the functioning of all terrestrial ecosystems, and the number of species involved is mind‐blowing (Nyman et al. 2015 ). Nevertheless, our understanding of the evolutionary and ecological determinants of their diversity is still in its infancy. In this issue of Molecular Ecology, Sutton et al. ( 2016 ) open a window into the comparative analysis of spatial genetic structuring in a set of comparable multitrophic models, involving highly species‐specific interactions: figs and fig wasps. This is the first study to compare genetic structure using population genetics tools in a fig‐pollinating wasp (Pleistodontes imperialis sp1) and its main parasitoid (Sycoscapter sp.A). The fig‐pollinating wasp has a discontinuous spatial distribution that correlates with genetic differentiation, while the parasitoid bridges the discontinuity by parasitizing other pollinator species on the same host fig tree and presents basically no spatial genetic structure. The full implications of these results for our general understanding of plant–herbivorous insect–insect parasitoids diversification become apparent when envisioned within the framework of recent advances in fig and fig wasp biology.     

Diapause induction in aphid parasitoids

Diapause is one of the adaptations that insects have evolved for the synchronisation of their life cycle with seasonal climatic changes and resources. In aphid parasitoids, univoltine species have an obligatory, genetically determined diapause. Polyvoltine species, on the other hand, use a variety of abiotic (temperature, photoperiod) and biotic (host insect or/and host plant) signals for the induction of diapause. We present an overview of the role of these environmental cues in diapause induction in specialist and generalist aphid parasitoids, and discuss possible endocrine factors that may be involved in diapause induction.     

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.     

An integrative approach to understanding host–parasitoid population dynamics in real landscapes

Many of our advances regarding the spatial ecology of predators and prey have been attributed to research with insect parasitoids and their hosts. Host–parasitoid systems are ideal for spatial-ecological studies because of the small size of the organisms, the often discrete distribution of their resources, and the relative ease with which host mortality from parasitoids can be determined. We outline an integrated approach to studying host–parasitoid interactions in heterogeneous natural landscapes. This approach involves conducting experiments to obtain critically important information on dispersal and boundary behavior of the host and parasitoid, large-scale manipulations of landscape structure to reveal the impacts of landscape change on host–parasitoid interactions and temporal population dynamics, and the development of spatially realistic, behavior-based landscape models. The dividends from such an integrative approach are far reaching, as is illustrated in our research on the prairie planthopper Prokelisia crocea and its egg parasitoid Anagrus columbi that occurs in the tall-grass prairies of North America. Here, we describe the population structure of this system which is based on a long-term survey of planthoppers and parasitoids among host–plant patches. We also outline novel approaches to experimentally quantify and model the movement and boundary behavior of animals in general. The value of this information is revealed in a landscape-level field experiment that was designed to test predictions about how landscape change affects the spatial and temporal population dynamics of the host and parasitoid. Finally, with these empirical data as the foundation, we describe novel simulation models that are spatially realistic and behavior based. Drawing from this integrated approach and case study, we identify key research questions for the future.