Jeffrey Harvey

Prof. Jeffrey Harvey PhD

Senior Researcher
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

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About

My research examines multitrophic interactions under abiotic stresses. Current focus is on the effects of climatic extremes i.e. heat waves, floods and drought on above-below ground multitrophic interactions and on the biology and ecology of spiders.

Biography

Steatoda grossa (male)
Male false widow spider, Steatoda grossa

Research groups

CV

Employment

  • 2000–Present
    Senior Scientist, Netherlands Institute of Ecology, The Netherlands
  • 2013–Present
    Visiting Professor, Free University, Amsterdam, The Netherlands
  • 1999
    Associate Editor, Nature (London), United Kingdom
  • 1997–1999
    Post-doctoral Associate, University of Wisconsin-Madison, United States
  • 1995–1997
    Post doctoral researcher, Wageningen University, The Netherlands
  • 1991–1995
    PhD, Liverpool University, United Kingdom
  • 1988–1991
    BSc, Liverpool University, United Kingdom

Ancillary activities

Publications

Peer-reviewed publications

  • Animal Behaviour
    01-12-2023

    The role of male body size in mating success and male–male competition in a false widow spider

    Yuting Dong, Jeff A. Harvey, Robin Steegh, Rieta Gols, Melissah Rowe
    In many animals, body size is correlated with reproductive success. Selection sometimes generates striking differences in body size between males and females (i.e. sexual size dimorphism, SSD). SSD is common in spiders (Araneae), and is typically explained by selection for larger, more fecund females and rapidly maturing, and consequently smaller, males. Within a species males and females also often vary in body size. In the false widow spider, Steatoda grossa, females are larger than males and males trade body size for rapid development and early maturation. Moreover, males vary considerably in body size, suggesting that under certain conditions there may be advantages to large size. Here, we tested the role of male body size on mating success under noncompetitive and competitive mating conditions (i.e. male–male competition) in S. grossa. We found that body size did not influence mating success or copulation duration under noncompetitive conditions, but that larger males were more successful at obtaining access to females under competitive mating conditions. Additionally, we found that total copulation duration was significantly lower when a rival male was present. Our results show a large male advantage under male–male competition, which we suggest may contribute to the high variation in male body size observed in S. grossa. We further suggest that the reduced copulation duration observed under competitive mating conditions may have potential ramifications for male and female reproductive success and we discuss how patterns of selection acting on male body size might limit the extent of SSD in this species.
    https://doi.org/10.1016/j.anbehav.2023.09.011
  • Agriculture, Ecosystems and Environment
    15-10-2023

    Integrating chemical plant trait- and ecological-based approaches to better understand differences in insect herbivory between cultivated and natural systems

    Rieta Gols, Jeff A. Harvey

    Cultivated plants are often much more susceptible to insect herbivores than wild-type plants. In addressing this observation, much attention has focused on a trait-based approach, and especially on how artificial selection via domestication has modified morphological and chemical traits, in particular levels of defensive secondary metabolites. However, larger scale ecological processes, such as the spatial distribution and diversity of species in a plant community, also determine how insects locate and exploit their food plants, and these differ profoundly between natural and agricultural ecosystems. In this paper we discuss these two approaches to better understand differences in levels of insect herbivory between agricultural and natural ecosystems. We argue that studies investigating the effects of secondary metabolites on insect herbivory are compromised by the methodological approach that is often used. Insect feeding assays testing the effect of reduced concentrations of secondary metabolites in domesticated plants rely on testing a limited subset of insect species, usually those that can easily be reared in the laboratory and often are agricultural pest species. The responses of these insects do not reflect the full range of responses of the species present in the plant's natural habitat. This may explain why reduced levels of secondary metabolites in crop plants may only partially explain increased susceptibility to herbivory. Hypotheses explaining larger scale patterns of insect herbivore abundance are often based on studies in agricultural settings. In our opinion, developing broad ecological hypotheses based on studies in agricultural systems do not necessarily apply to natural systems and vice versa. To fully understand how susceptibility or resistance to insect herbivory is affected by plant traits and habitat heterogeneity, these have to be studied together in both natural and agricultural settings.

    https://doi.org/10.1016/j.agee.2023.108643
  • Animal Behaviour
    09-2023

    Temperature affects the outcome of competition between two sympatric endoparasitoids

    T.P.M. Costaz, Peter W. de Jong, Jeff A. Harvey, Joop J.A. van Loon, Marcel Dicke, Rieta Gols

    Temperature is a major driver of species interactions as it determines many physiological and behavioural parameters of ectothermic organisms such as insects. Examining the effects of elevated temperature and extreme temperature events within and between different trophic levels is crucial for understanding their broader implications for community and ecosystem level processes. We compared parasitism success of two hymenopteran parasitoid species, Diadegma semiclausum and Cotesia vestalis, under different temperature regimes when foraging intra- and interspecifically. Both parasitoid species can be found in the same habitat and are important biological control agents of the cosmopolitan lepidopteran pest Plutella xylostella, the host species in this study. Because parasitoid density may influence parasitism success through interference competition, we first investigated the effect of parasitoid density (one to four females of the same species) on parasitism success at 22 °C. In all assays, parasitoid females were released in cages with a single plant infested with 30 hosts placed in a greenhouse or climate cabinets set at 22, 27 or 33 °C and removed after 3 h. All cages were returned to 22 °C until pupation of the parasitoids or hosts, which were then counted. When females of the same species foraged together, parasitism success increased with parasitoid density. However, when both species were foraging together, parasitism success of D. semiclausum decreased with increasing temperature at both tested densities, whereas the opposite was found for C. vestalis. Nevertheless, parasitism success of D. semiclausum was always higher than that of C. vestalis, irrespective of parasitoid density or temperature, but competitive superiority of D. semiclausum decreased with increasing temperature. Increases in the magnitude and frequency of extreme temperature events under climate change are likely to have differential effects on species involved in intimate interactions, depending on community species composition, as species may differ in thermal resilience.

    https://doi.org/10.1016/j.anbehav.2023.06.003
  • Ethology
    27-07-2023

    Sibling cannibalism in the false widow spider is dependent on spiderling density and the reliable availability of fresh prey

    Jeff A. Harvey, Robin Steegh, Yuting Dong, Rieta Gols
    Adult female spiders lay batches of eggs in silken egg sacs, and after hatching, the spiderlings live for transient periods in their mother's web before dispersing. Sibling cannibalism is frequently observed among spiderlings of many species under conditions of food deprivation. Here, we conducted assays in small Petri dishes with different densities of newly hatched (second instar) spiderlings of the false widow spider, Steatoda grossa, using a split-clutch design. Prey (freshly killed fruit flies) availability was manipulated both numerically and temporally. Offspring from 10 different females were separated as siblings into densities of two, four, or eight spiderlings per Petri dish and these were provided with either 0 flies (starvation control), two flies, four flies, or eight flies that were replenished weekly or every 3 weeks. A further control was conducted with solitary spiderlings in Petri dishes deprived of flies. The number of surviving spiderlings per Petri dish was counted every 3 days until only one remained (or until death of the solitary spiderling). Our results show that the rate of cannibalism was lower with increasing spiderling density and when fresh flies were replenished more frequently, whereas the number of flies that were provided did not affect cannibalism. In S. grossa, juvenile cannibalism occurs primarily under conditions of extreme food limitation, although in synanthropic habitats where the spider is abundant, it may be an adaptive strategy owing to the potential scarcity of prey. Under certain conditions, cannibalism in spiderlings is adaptive by eliminating competitors and providing nutrient-rich food.
    https://doi.org/10.1111/eth.13399
  • European Journal of Soil Biology
    01-07-2023

    Communities of nematodes, bacteria and fungi differ among soils of different wild cabbage populations

    Rieta Gols, Moniek Van Geem, James M. Bullock, Henk Martens, Roel Wagenaar, Wim H. van der Putten, Jeff A. Harvey
    Plants exhibit significant variation in morphological and chemical traits of shoots and roots in response to an array of biotic and abiotic selection pressures, and this variation in turn affects their interactions with the biotic and abiotic environment. Thus far, most studies examining these interactions have focused on the aboveground domain, which is easier to study than the belowground domain. However, soil organisms significantly affect plant fitness directly through mutualisms e.g. growth promotion, or antagonisms e.g. herbivory and disease. Natural populations of wild Brassica oleracea L. growing along the south coastline of Great Britain exhibit significant differences in growth form and secondary chemistry. Studies in the field have shown that these differences affect aboveground plant-insect interactions, whereas soil communities have not been explored. We sampled belowground communities of nematodes, bacteria and fungi associated with roots, rhizosphere and bulk soil in five coastal wild cabbage populations in Dorset, England, and found significant differences among these communities. Site-related differences in nematode community composition were primarily found for nematodes in bulk soil and were consistent over two years of sampling. Nematode communities in roots of wild cabbage did not significantly differ across the cabbage populations but did differ between the two years. Results for communities in rhizosphere soil were spatially and temporally variable. The composition of nematode communities in cabbage roots differed strongly from those in the rhizosphere and bulk soil, showing that plants attract a subset of nematodes from the bulk soil community. For microbes, we analysed only rhizosphere samples, and found that fungal communities differed more strongly among plant populations than bacterial communities. Thus, while there is spatio-temporal variation in belowground communities, soil and/or plant properties differentially affect the assembly of nematodes, fungi and bacteria.
    https://doi.org/10.1016/j.ejsobi.2023.103512
  • Biology
    18-04-2023

    Climate Change, Extreme Temperatures and Sex-Related Responses in Spiders

    Jeff A. Harvey, Yuting Dong
    Simple Summary
    Anthropogenic climate change is one of the greatest threats to biodiversity. Extreme temperature events associated with longer-term climate change are increasing in frequency, duration and intensity. The effects of climatic extremes on ectotherms, such as insects, have been well-studied in recent years. However, the effects of extreme temperatures on other arthropod groups, such as spiders, has received much less attention. Spiders are important organisms as predators in natural and agricultural ecosystems. In this paper, we describe spider responses to extreme temperatures and highlight the most important knowledge gaps that urgently need to be filled to better understand how vulnerable spiders are to climate change and climatic extremes. Unlike insects, traits such as body size and niche breadth may differ markedly in male and female spiders. Therefore, we argue that research needs to address the effects of heat exposure on the physiology, behavior and ecology of male and female spiders across multiple taxa. Observed declines in some terrestrial insects have been widely reported in recent years, with climate change, along with other anthropogenic threats, being implicated. Longer-term data on trends in spider abundance, where available, may also shed possible light on the role of climate change.

    Abstract
    Climatic extremes, such as heat waves, are increasing in frequency, intensity and duration under anthropogenic climate change. These extreme events pose a great threat to many organisms, and especially ectotherms, which are susceptible to high temperatures. In nature, many ectotherms, such as insects, may seek cooler microclimates and ’ride out´ extreme temperatures, especially when these are transient and unpredictable. However, some ectotherms, such as web-building spiders, may be more prone to heat-related mortality than more motile organisms. Adult females in many spider families are sedentary and build webs in micro-habitats where they spend their entire lives. Under extreme heat, they may be limited in their ability to move vertically or horizontally to find cooler microhabitats. Males, on the other hand, are often nomadic, have broader spatial distributions, and thus might be better able to escape exposure to heat. However, life-history traits in spiders such as the relative body size of males and females and spatial ecology also vary across different taxonomic groups based on their phylogeny. This may make different species or families more or less susceptible to heat waves and exposure to very high temperatures. Selection to extreme temperatures may drive adaptive responses in female physiology, morphology or web site selection in species that build small or exposed webs. Male spiders may be better able to avoid heat-related stress than females by seeking refuge under objects such as bark or rocks with cooler microclimates. Here, we discuss these aspects in detail and propose research focusing on male and female spider behavior and reproduction across different taxa exposed to temperature extremes.
    https://doi.org/10.3390/biology12040615
  • Ecological Monographs
    01-02-2023

    Scientists' warning on climate change and insects

    Jeff A. Harvey, Kévin Tougeron, Rieta Gols, Robin Heinen, Mariana Abarca, Paul K. Abram, Yves Basset, Matty P. Berg, Carol Boggs, Jacques Brodeur, Pedro Cardoso, Jetske G. de Boer, Geert de Snoo, Charl Deacon, Jane E. Dell, Nicolas Desneux, Michael E. Dillon, Grant A. Duffy, Lee A. Dyer, Jacintha Ellers, Anahí Espíndola, James Fordyce, Matthew L. Forister, Caroline Fukushima, Matthew J. G. Gage, Carlos García‐Robledo, Claire Gely, Mauro Gobbi, Caspar A Hallmann, Thierry Hance, John Harte, Axel Hochkirch, Christian Hof, Ary A. Hoffmann, Joel G. Kingsolver, Greg P. A. Lamarre, William F Laurance, Blas Lavandero, Simon R Leather, Philipp Lehmann, Cécile Le Lann, Margarita M. López‐Uribe, Chun‐Sen Ma, Gang Ma, Joffrey Moiroux, Lucie Monticelli, Chris Nice, Paul J. Ode, Sylvain Pincebourde, William J. Ripple, Melissah Rowe, Michael J Samways, Arnaud Sentis, Alisha A. Shah, Nigel Stork, John S. Terblanche, Maddy Thakur, Matthew B. Thomas, Jason M. Tylianakis, Joan Van Baaren, Martijn van de Pol, Wim H. van der Putten, Hans Van Dyck, Wilco C. E. P. Verberk, David L Wagner, Wolfgang W. Weisser, William C. Wetzel, H. Arthur Woods, Kris A G Wyckhuys, Steven L Chown
    Climate warming is considered to be among the most serious of anthropogenicstresses to the environment, because it not only has direct effects on biodiver-sity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly interms of threats to species preservation, as well as in the preservation of anarray of ecosystem services provided by biodiversity. Among the most affectedgroups of animals are insects—central components of many ecosystems—forwhich climate change has pervasive effects from individuals to communities.In this contribution to the scientists’warning series, we summarize the effectof the gradual global surface temperature increase on insects, in terms ofphysiology, behavior, phenology, distribution, and species interactions, as wellas the effect of increased frequency and duration of extreme events such as hotand cold spells, fires, droughts, and floods on these parameters. We warn that,if no action is taken to better understand and reduce the action of climatechange on insects, we will drastically reduce our ability to build a sustainablefuture based on healthy, functional ecosystems. We discuss perspectives onrelevant ways to conserve insects in the face of climate change, and we offerseveral key recommendations on management approaches that can beadopted, on policies that should be pursued, and on the involvement of thegeneral public in the protection effort.
    https://doi.org/10.1002/ecm.1553
  • Ecological Entomology
    25-01-2023

    Contrasting effects of nitrogen fertiliser application on the performance of closely related grasshoppers through changes in plant nutrient concentrations

    Yu Zhu, Quanhui Ma, Zhiwei Zhong, Ming Jiang, (Liesbeth) E.S. Bakker, Jeff A. Harvey, Ciska Veen, Cong Chen, Deli Wang
    Global environmental changes mediated by anthropogenic processes can affect the nutrient status of plants, with important consequences for the performance and dynamics of insect herbivores that feed on them.
    While it is well documented that insects from different feeding guilds (e.g., sap-feeders and leaf-chewers) can respond differently to altered food resources due to their distinct physiological and ecological characteristics, little is known about how ecologically similar insect species from the same feeding guild respond to changes in food nutrient status.
    Using nitrogen (N) fertiliser, the authors examined the effects of N inputs on two sympatric grasshopper species, Euchorthippus cheui and E. unicolor, that share the same host food plant, Leymus chinensis grass. The authors examined the effects of fertilisation on the individual feeding behaviour, performance and abundance of the two grasshopper species.
    The nutrient (protein) content of L. chinensis leaves was enhanced by fertilisation during the entire season. However, E. cheui and E. unicolor exhibited differing growth rates, development and body size responses to fertilisation.
    E. cheui preferred L. chinensis leaves from high-N fertilised treatments, while E. unicolor preferred leaves from low-N fertilised treatments. Moreover, fertilisation increased the abundance of E. cheui but had no significant effect on the abundance of E. unicolor in the field.
    The findings imply that effective management and conservation strategies for insects should target the needs of individual species rather than species groups or communities as a whole because nutritional and environmental requirements are often species-specific.
    https://doi.org/10.1111/een.13228
  • Frontiers in Applied Mathematics and Statistics
    24-01-2023

    Enhancing the predictability of ecology in a changing world

    C.J.M. Musters, Don L. DeAngelis, Jeff A. Harvey, Wolf M. Mooij, Peter M. van Bodegom, Geert de Snoo
    Ecology is usually very good in making descriptive explanations of what is observed, but is often unable to make predictions of the response of ecosystems to change. This has implications in a human-dominated world where a suite of anthropogenic stresses are threatening the resilience and functioning of ecosystems that sustain mankind through a range of critical regulating and supporting services. In ecosystems, cause-and-effect relationships are difficult to elucidate because of complex networks of negative and positive feedbacks. Therefore, being able to effectively predict when and where ecosystems could pass into different (and potentially unstable) new states is vitally important under rapid global change. Here, we argue that such better predictions may be reached if we focus on organisms instead of species, because organisms are the principal biotic agents in ecosystems that react directly on changes in their environment. Several studies show that changes in ecosystems may be accurately described as the result of changes in organisms and their interactions. Organism-based theories are available that are simple and derived from first principles, but allow many predictions. Of these we discuss Trait-based Ecology, Agent Based Models, and Maximum Entropy Theory of Ecology and show that together they form a logical sequence of approaches that allow organism-based studies of ecological communities. Combining and extending them makes it possible to predict the spatiotemporal distribution of groups of organisms in terms of how metabolic energy is distributed over areas, time, and resources. We expect that this “Organism-based Ecology” (OE) ultimately will improve our ability to predict ecosystem dynamics.
    https://doi.org/10.3389/fams.2023.1046185
  • Annual Review of Entomology
    23-01-2023

    The Biology and Ecology of Parasitoid Wasps of Predatory Arthropods

    Minghui Fei, Rieta Gols, Jeff A. Harvey

    Parasitoid wasps are important components of insect food chains and have played a central role in biological control programs for over a century. Although the vast majority of parasitoids exploit insect herbivores as hosts, others parasitize predatory insects and arthropods, such as ladybird beetles, hoverflies, lacewings, ground beetles, and spiders, or are hyperparasitoids. Much of the research on the biology and ecology of parasitoids of predators has focused on ladybird beetles, whose parasitoids may interfere with the control of insect pests like aphids by reducing ladybird abundance. Alternatively, parasitoids of the invasive ladybird Harmonia axyridis may reduce its harmful impact on native ladybird populations. Different life stages of predatory insects and spiders are susceptible to parasitism to different degrees. Many parasitoids of predators exhibit intricate physiological interrelationships with their hosts, adaptively manipulating host behavior, biology, and ecology in ways that increase parasitoid survival and fitness.

    https://doi.org/10.1146/annurev-ento-120120-111607
  • Ecology Letters
    01-2023

    Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities

    Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant–insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil ‘memories’ that influence aboveground plant community interactions in the next growing season. These soil-borne ‘memories’ can be altered by climate warming-induced plant range shifts and extreme drought.

    https://doi.org/10.1111/ele.14129
  • Community Ecology
    2023

    Generalism in nature: a community ecology perspective

    Hugh D. Loxdale, Jeff A. Harvey
    Life on Earth is complex and generally abounds in food webs with other living organisms in terms of an ecological community. Besides such complexity, and the fact that populations of most living organisms have never been studied in terms of their molecular ecology, it is best to tread carefully when describing a given species as a ‘generalist’, more especially in terms of dietary and habitat breadth. We very much doubt that population homogeneity ever exists—because populations are always undergoing molecular-genetic changes, sometimes rapid, in response to various ecological challenges (e.g. climate, intra- and interspecific competition). In any case, a population may already have begun to undergo cryptic speciation. Such entities can occupy different habitats or exhibit different dietary breadths as a result of various ecological interactions formed over different spatial scales. These scales include everything from local (including islands) to geographic. The fossil evidence reveals that specialisations have existed over vast swathes of time. Besides, as is well documented, evolution only occurs as a result of adaptations leading to specialisation, and ultimately, specialist entitles, i.e. species and lower levels of ecological-evolutionary divergence. Here, focusing on diet, we posit that the terms mono-, oligo-and polyphagous are more accurate in relation to the dietary breadth of animals, with omnivory adopted in the case of organisms with very different food items. Thus, we strongly urge that the dubious and unscientific term ‘generalism’ be dropped in favour of these more precise and scientifically accurate terms directly relating to levels of phagy.
    https://doi.org/10.1007/s42974-022-00130-6
  • Plants
    01-04-2022

    Effects of Light Quality on Colonization of Tomato Roots by AMF and Implications for Growth and Defense

    Haymanti Saha, Nikolaos Kaloterakis, Jeff A. Harvey, Wim H. van der Putten, Arjen Biere

    Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant’s SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading.

    https://doi.org/10.3390/plants11070861
  • Journal of Applied Entomology
    2022

    Artificially perforated holes in stems of small hogweed mimic ecosystem engineering by a moth

    Sanne E. Bethe, Rieta Gols, Jeff A. Harvey

    Ecosystem engineers are species that manipulate the physical state of ecosystems and thereby affect the behaviour and ecology of other species. Mature larvae of the parsnip webworm, Depressaria radiella Goeze, chew holes in the hollow stems of Heracleum sphondylium L. into which they pupate. The stems are separated into several compartments that are separated by filamentous membranes. Holes excavated by webworm larvae attract several beneficial species of arthropods that use them for shelter in autumn, including the common earwig (Forficula auricularia L.) and the common rough woodlouse (Porcellio scaber Latreille). If artificially made holes mimic the engineering effect of D. radiella, they could be made to attract (local) communities of beneficial arthropods and perhaps facilitate overwintering habitat. We conducted a field experiment to determine whether artificial holes perforated into stem compartments of H. sphondylium mimic the natural situation with D. radiella. At five sites near the city of Leiden, the Netherlands, H. sphondylium plants were exposed to different treatments: a single hole perforated in the first, second or third stem compartment, or in all three compartments. After 3 weeks, arthropod numbers were counted inside and around hogweed stems. The arthropod community in the stems differed from that surrounding the stems; the latter consisted mainly of woodlice and wolf spiders, whereas in the stems, in addition to woodlice, many earwigs were found and no wolf spiders. Both artificial and webworm-excavated holes that were present at one site were used by woodlice and earwigs. The position of the holes along the stem did not affect the number of arthropods found in that segment, although the arthropods exhibited a tendency to move up the stems. The results show that artificial holes mimic webworm-excavated holes in that both attract the same species of beneficial arthropods.

    https://doi.org/10.1111/jen.13071
  • Ecology and Society
    2022

    Reviewing the relationship between neoliberal societies and nature

    Jeanne M. Bogert, Jacintha Ellers, Stephan Lewandowsky, Meena Balgopal, Jeff A. Harvey

    How a society relates to nature is shaped by the dominant social paradigm (DSP): a society’scollective view on social, economic, political, and environmental issues. The characteristics of the DSP have important consequences for natural systems and their conservation. Based on a synthesis of academic literature, we provide a new gradient of 12 types of human-nature relationships synthesized from scientific literature, and an analysis of where the DSP of industrialized, and more specifically, neoliberal societies fit on that gradient. We aim to answer how the industrialized DSP relates to nature, i.e., what types of human-nature relationships this DSP incorporates, and what the consequences of these relationships are for nature conservation and a sustainable future. The gradient of human-nature relationships is based on three defining characteristics: (1) a nature-culture divide, (2) core values, and (3) being anthropocentric or ecocentric. We argue that the industrialized DSP includes elements of the anthropocentric relationships of mastery, utilization, detachment, and stewardship. It therefore regards nature and culture as separate, is mainly driven by instrumental values, and drives detachment from and commodification of nature. Consequently, most green initiatives and policies driven by an industrialized and neoliberal DSP are based on economic incentives and economic growth, without recognition of the needs and limits of natural systems. This leads to environmental degradation and social inequality, obstructing the path to a truly sustainable society. To reach a more ecocentric DSP, systemic changes, in addition to individual changes, in the political and economic structures of the industrialized DSP are needed, along with a change in values and approach toward nature, long-term sustainability, and conservation. Key Words: conservation; dominant social paradigm; environmental degradation; human-nature relationships; industrialized society; Sustainability

    https://doi.org/10.5751/ES-13134-270207
  • Journal of Insect Physiology
    2022

    Prey availability affects developmental trade-offs and sexual-size dimorphism in the false widow spider, Steatoda grossa

    In many spiders, females are significantly larger than males. Several theories have been postulated to explain sexual size dimorphism (SSD), including differential predation risks experienced by each sex early in life (including female cannibalism of males), male-male competition, and the more costly production of eggs than sperm. However, there is considerable intraspecific variation in the relative size of males and females that is reflected in trade-offs on traits such as growth rate and body size. When SSD favors female size, the body mass ratios between the smallest and largest males is expected to be much greater than in females. Here, growth trajectories and body masses of the false widow spider, Steatoda grossa, were compared in male and female spiders fed continually or intermittently. Males provided with unlimited prey (fruit flies and house crickets) took about 15 weeks to attain full size and sexual maturity and grew to a mean of 25 mg. By contrast, males fed only once every three weeks took approximately 6 weeks longer to reach maturity but were only about half as large (mean 13 mg) as males fed constantly. Females fed intermittently took almost twice as long (45 weeks versus 24 weeks) as constantly-fed females to reach maturity, but were almost 90% as large when fully grown. These results reveal that, although both sexes trade-off development time and body size to achieve the optimal phenotype, rapid development is more important than larger body size in males whereas the opposite is true in females. This finding supports life-history theory underpinning sexual-size dimorphism in some spider lineages.
    https://doi.org/10.1016/j.jinsphys.2021.104267
  • Annual Review of Entomology
    2022

    Extrinsic Inter- and Intraspecific Competition in Parasitoid Wasps

    P.J. Ode, Dhaval K. Vyas, Jeff A. Harvey
    The diverse ecology of parasitoids is shaped by extrinsic competition, i.e., exploitative or interference competition among adult females and males for hosts and mates. Adult females use an array of morphological, chemical, and behavioral mechanisms to engage in competition that may be either intra- or interspecific. Weaker competitors are often excluded or, if they persist, use alternate host habitats, host developmental stages, or host species. Competition among adult males for mates is almost exclusively intraspecific and involves visual displays, chemical signals, and even physical combat. Extrinsic competition influences community structure through its role in competitive displacement and apparent competition. Finally, anthropogenic changes such as habitat loss and fragmentation, invasive species, pollutants, and climate change result in phenological mismatches and range expansions within host-parasitoid communities with consequent changes to the strength of competitive interactions. Such changes have important ramifications not only for the success of managed agroecosystems, but also for natural ecosystem functioning.
    https://doi.org/10.1146/annurev-ento-071421-073524
  • Entomologia Experimentalis et Applicata
    2022

    Plant quantity affects development and reproduction of a gregarious butterfly more than plant quality

    Rieta Gols, Luuk Croijmans, Marcel Dicke, Joop J.A. van Loon, Jeff A. Harvey

    The larvae of insect herbivores feed on plants that may vary nutritionally (qualitatively and/or quantitatively) over the course of insect development. Plant quality may change in response to interactions with the biotic environment that in turn may affect development and biomass of the insects feeding on these plants. However, the larvae of many gregariously feeding herbivores feed on comparatively small plants with limited biomass and may also experience variation in the quantity of plant food available. Pieris brassicae L. (Lepidoptera: Pieridae) is a gregarious butterfly species laying clutches of 10–150 eggs that are often laid on small brassicaceous food plants, including the plant used in this study, Brassica nigra L. (Brassicaceae). A single B. nigra plant provides insufficient resources for the development of an entire brood of P. brassicae. In this study, we investigated the effect of both plant quality and quantity on the performance of P. brassicae when feeding on B. nigra plants. When we compared the effects of changes in plant quality induced by (1) aphid infestation, (2) exposure to pathogenic and non-pathogenic bacteria, and (3) inbreeding depression, which are all biotic stresses known to change plant quality, pupal mass and larval development time of P. brassicae were fairly similar. We then examined the effects of quantitative food constraints during immature development on pupal mass, which correlated strongly with adult size, longevity, and fecundity. Female pupal mass, longevity and fecundity were negatively correlated with the duration of starvation during larval development. No significant effect of male starvation was found on female reproduction and longevity. Thus, P. brassicae larvae were more affected by quantitative than by qualitative constraints in terms of pupal mass, which strongly correlated with female reproduction.

    https://doi.org/10.1111/eea.13192
  • Pacific Conservation Biology
    2022

    Evaluating the effects of the invasive cane toad (Rhinella marina) on island biodiversity, focusing on the Philippines

    Jeff A. Harvey, Priyanka Ambavane, Mark Williamson, Arvin Diesmos
    The negative ecological impacts of invasive species are well documented, although their effects are often more pronounced on islands than on the mainland. This is because many island species exhibit high degrees of endemism, have small geographic distributions, are rare, and exhibit low genetic diversity, which reduces their ability to respond to new emerging threats. One of the world's most notorious invasive species is the cane toad (Rhinella marina), which is a voracious predator that is native to the neo-tropics but was intentionally introduced in the early 20th century to many warm regions and islands to control crop pests. Cane toads produce two kinds of toxins in neck glands that are often lethal to non-adapted predators in the invasive range. Although well-studied in Australia, their ecological impacts on many islands have received much less attention. Australia is the sixth largest country on Earth, so the effects of cane toads on small island nations may differ considerably from there. Here, we discuss the potential ecological impacts of cane toads in the Philippines and on other island nations. Cane toads were introduced onto the largest Philippine island, Luzon, in 1930 and have since spread over all but a few of the 7641 islands that make up the country. We speculate that, unlike most biological invasions with predators or herbivores where the ecological effects are strictly 'top-down', cane toads, by virtue of their biology and ecology, may have even more serious effects on island fauna because they exhibit both 'top-down' and 'bottom-up' effects.
    https://doi.org/10.1071/pc21012
  • Geoderma
    15-11-2021

    Effects of soil biota on growth, resistance and tolerance to herbivory in Triadica sebifera plants

    Qiang Yang, Evan Siemann, Jeff A. Harvey, Jianqing Ding, Arjen Biere

    Interactions with soil microbes can strongly affect plant growth and defense against aboveground herbivores. Plant species often accumulate specific soil pathogens in their rhizosphere, leading to reduced growth of plants in soils originating from stands of conspecific plants compared to soils from heterospecific plants. However, whereas effects of such conspecific vs. heterospecific soil biota on plant growth have been well documented, their effects on plant resistance and tolerance to aboveground insect herbivores have not. We compared growth and defense of Triadica sebifera plants from populations where the species is native (China), when grown in sterilized soils, or in soils harbouring belowground biota from conspecific (native Triadica) or heterospecific (native grass) soils. In each of these soils, plants were exposed to a 15-day period of foliar herbivory by a specialist weevil (Heterapoderopsis bicallosicollis), a specialist caterpillar (Gadirtha inexacta), or no herbivory (cage), followed by a 60-day recovery period. Soil biota from conspecific and hetetospecific soils differed in their effects on plant growth and defense. First, in the absence of herbivory, soil biota from heterospecific soils slightly enhanced plant growth, whereas those from conspecific soils strongly reduced plant growth. Second, soil biota from conspecific soils strongly affected plant resistance and tolerance to foliar herbivory, whereas soil biota from heterospecific plants did not. The effects of soil biota on plant defense were herbivore-specific. In particular, conspecific soil biota reduced resistance to caterpillar but not to weevil feeding, whereas they enhanced tolerance to weevil but not to caterpillar feeding. Conspecific soil biota also mitigated induction of root flavonoids by herbivores and led to reduced root phenolics in response to herbivory. Conversely, caterpillar feeding increased AMF colonization, but under these conditions, AMF colonization was negatively associated with plant biomass. In addition to testing effects on native plants, we also tested effects of native soil biota on growth and resistance of plants from the introduced range (North America). Plants from the introduced range had higher shoot production, shoot-to-root ratio, and leaf phenolic and flavonoid production than plants from the native range, but their interactions with soil biota showed only minor differences compared to plants from the native range. Our results suggest that incorporating the effects of soil biota in interactions between plants and foliar herbivores is critical for understanding variations in growth, defense, and performance among plant populations at local and broader geographic scales.

    https://doi.org/10.1016/j.geoderma.2021.115191
  • Journal of Thermal Biology
    07-2021

    Within-patch and edge microclimates vary over a growing season and are amplified during a heatwave: Consequences for ectothermic insects

    R. Gols, L.M. Ojeda-Prieto, Keli Li, Wim H. van der Putten, Jeff A. Harvey

    Embedded in longer term warming are extreme climatic events such as heatwaves and droughts that are increasing in frequency, duration and intensity. Changes in climate attributes such as temperature are often measured over larger spatial scales, whereas environmental conditions to which many small ectothermic arthropods are exposed are largely determined by small-scale local conditions. Exposed edges of plant patches often exhibit significant short-term (daily) variation to abiotic factors due to wind exposure and sun radiation. By contrast, within plant patches, abiotic conditions are generally much more stable and thus less variable. Over an eight-week period in the summer of 2020, including an actual heatwave, we measured small-scale (1 m2) temperature variation in patches of forbs in experimental mesocosms. We found that soil surface temperatures at the edge of the mesocosms were more variable than those within mesocosms. Drought treatment two years earlier, amplified this effect but only at the edges of the mesocosms. Within a plant patch both at the soil surface and within the canopy, the temperature was always lower than the ambient air temperature. The temperature of the soil surface at the edge of a patch may exceed the ambient air temperature when ambient air temperatures rise above 23 °C. This effect progressively increased with ambient temperature. We discuss how microscale-variation in temperature may affect small ectotherms such as insects that have limited ability to thermoregulate, in particular under conditions of extreme heat.

    https://doi.org/10.1016/j.jtherbio.2021.103006
  • Biological Control
    2021

    Development and oviposition strategies in two congeneric gregarious larval-pupal endoparasitoids of the seven-spot ladybird, Coccinella septempunctata

    Minghui Fei, Haowu Hu, Rieta Gols, Shengnan Liu, Xiaolin Wan, Baoping Li, Jeff A. Harvey

    Aphids are serious pests of many crops in agroecosystems and their biological control is focused on enhancing the performance of specialized natural enemies of aphids such as parasitoid wasps and predators like ladybirds. However, ladybirds are often attacked by their own parasitoids in the fourth trophic level that can negatively affect ladybird performance and, hence, their effectiveness as control agents. The biology and ecology of these parasitoids has been less well explored. This study compared various life-history traits in two closely related parasitoids of the seven-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae): Oomyzus scaposus and O. spiraculus (Hymenoptera: Eulophidae), which naturally co-occur in eastern China and are facultatively gregarious koinobiont larval-pupal endoparasitoids of ladybird beetles. They can oviposit and develop in all four larval instars of their hosts but kill and emerge from the pupae. Both parasitoids did not have a clear oviposition preference for any host instar, but oviposition duration tended to increase in first to third instar hosts. Moreover, oviposition time was significantly longer for O. spiraculus than for O. scaposus. Adult eclosion from parasitized hosts (ranging between 35 and 45%) and sex ratios (85–90% female) were similar in both species and did not differ among host instars. Brood sizes were similar in both species but tended to increase in first to third instar hosts. Egg-to-adult development time was shorter and the eclosing adults of O. scaposus were heavier than those of O. spiraculus. In both species, development time decreased with host instar at parasitism, but instar-specific effects on biomass differed between the two species: heavier O. scaposus adults developed from second and third instar hosts, whereas biomass of for O. spiraculus tended to decrease with instar at parasitism. In both species, females were significantly larger than males. Our results show that expression of some of the life-history traits vary depending on which instar is parasitized, but do not point at a specific instar optimal for each of the parasitoids. Moreover, despite being closely related, there is some variability in the expression of life-history traits in both parasitoids.

    https://doi.org/10.1016/j.biocontrol.2021.104756
  • Biodiversity and Conservation
    2021

    Biodiversity conservation in climate change driven transient communities

    Peter Schippers, Euridice Leyequien Abarca, Jana Verboom, G. W. Wieger Wamelink, Claire C. Vos, Willem Fred De Boer, Jeff A. Harvey, Tijl Essens, Carla J. Grashof-Bokdam, Michiel F. WallisDeVries, Marleen Cobben

    Species responding differently to climate change form ‘transient communities’, communities with constantly changing species composition due to colonization and extinction events. Our goal is to disentangle the mechanisms of response to climate change for terrestrial species in these transient communities and explore the consequences for biodiversity conservation. We review spatial escape and local adaptation of species dealing with climate change from evolutionary and ecological perspectives. From these we derive species vulnerability and management options to mitigate effects of climate change. From the perspective of transient communities, conservation management should scale up static single species approaches and focus on community dynamics and species interdependency, while considering species vulnerability and their importance for the community. Spatially explicit and frequent monitoring is vital for assessing the change in communities and distribution of species. We review management options such as: increasing connectivity and landscape resilience, assisted colonization, and species protection priority in the context of transient communities.

    https://doi.org/10.1007/s10531-021-02241-4
  • Global Change Biology
    12-2020

    Climate change-mediated temperature extremes and insects

    Jeff A. Harvey, Robin Heinen, Rieta Gols, Maddy Thakur

    Insects are among the most diverse and widespread animals across the biosphere and are well-known for their contributions to ecosystem functioning and services. Recent increases in the frequency and magnitude of climatic extremes (CE), in particular temperature extremes (TE) owing to anthropogenic climate change, are exposing insect populations and communities to unprecedented stresses. However, a major problem in understanding insect responses to TE is that they are still highly unpredictable both spatially and temporally, which reduces frequency- or direction-dependent selective responses by insects. Moreover, how species interactions and community structure may change in response to stresses imposed by TE is still poorly understood. Here we provide an overview of how terrestrial insects respond to TE by integrating their organismal physiology, multitrophic, and community-level interactions, and building that up to explore scenarios for population explosions and crashes that have ecosystem-level consequences. We argue that TE can push insect herbivores and their natural enemies to and even beyond their adaptive limits, which may differ among species intimately involved in trophic interactions, leading to phenological disruptions and the structural reorganization of food webs. TE may ultimately lead to outbreak–breakdown cycles in insect communities with detrimental consequences for ecosystem functioning and resilience. Lastly, we suggest new research lines that will help achieve a better understanding of insect and community responses to a wide range of CE.

    https://doi.org/10.1111/gcb.15377
  • Pest Management Science
    01-06-2020

    Effects of elevated CO2 and temperature on survival and wing dimorphism of two species of rice planthoppers (Hemiptera: Delphacidae) under interaction

    Caiyun Wang, Minghui Fei, Ling Meng, Jeff A. Harvey, Baoping Li

    BACKGROUND: Anthropogenic climate change (ACC) may have significant impacts on insect herbivore communities including pests. Two of the most important climate-change related factors are increased atmospheric concentrations of carbon dioxide (CO 2), and increasing mean global temperature. Although increasing attention is being paid to the biological and ecological effects of ACC, important processes such as interspecific interaction between insect herbivores have been little explored. Here, in a field experiment using the FACE (free-air CO 2 enrichment) system, we investigated the effect of elevated CO 2 and temperature on survival and wing dimorphism of two species of rice planthoppers, Laodelphax striatellus and Nilaparvata lugens under interaction. RESULTS: The two species were grouped into five treatments of relative density (0/50, 13/37, 25/25, and 37/13, 50/0), each of which was allocated to one of a factorial combination of two CO 2 concentrations and two temperature treatments (elevated and ambient levels). Our results revealed that climatic treatment has no effects on survivorship of interspecific competing planthoppers. However, climatic treatment affected wing-form of planthoppers under interspecific interaction. For females of N. lugens, in the 37/13 ratio, proportion macropterours form was lower under elevated CO 2 + temperature than under the ambient environment or than under elevated temperature. For females of L. striatellus, proportion macropterous form did not differ among climatic treatments at each ratio treatment. CONCLUSION: These findings illustrate that climate change-related factors, by affecting the macropetry of interspecific competing planthoppers, may influence planthopper fitness. We provide new information that could assist with forecasting outbreaks of these migratory pests.

    https://doi.org/10.1002/ps.5747
  • Nature Ecology and Evolution
    01-02-2020

    International scientists formulate a roadmap for insect conservation and recovery

    Jeff A. Harvey, Robin Heinen, Inge Armbrecht, Yves Basset, James H Baxter-Gilbert, T. Martijn Bezemer, Monika Böhm, Riccardo Bommarco, Paulo A V Borges, Pedro Cardoso, Viola Clausnitzer, Tara Cornelisse, Elizabeth E Crone, Marcel Dicke, Klaas-Douwe B Dijkstra, Lee A. Dyer, Jacintha Ellers, Thomas Fartmann, Matthew L. Forister, Michael J Furlong, Andres Garcia-Aguayo, Justin Gerlach, Rieta Gols, Dave Goulson, Jan-Christian Habel, Nick M Haddad, Caspar A Hallmann, Sérgio Henriques, Marie E Herberstein, Axel Hochkirch, Alice C Hughes, Sarina Jepsen, T Hefin Jones, Bora M Kaydan, David Kleijn, Alexandra-Maria Klein, Tanya Latty, Simon R Leather, Sara M Lewis, Bradford C Lister, John E Losey, Elizabeth C Lowe, Craig R Macadam, James Montoya-Lerma, Christopher D Nagano, Sophie Ogan, Michael C Orr, Christina J Painting, Thai-Hong Pham, Simon G. Potts, Aunu Rauf, Tomas L. Roslin, Michael J Samways, Francisco Sanchez-Bayo, Sim A Sar, Cheryl B Schultz, António O Soares, Anchana Thancharoen, Teja Tscharntke, Jason M. Tylianakis, Kate D L Umbers, Louise E.M. Vet, Marcel E. Visser, Ante Vujic, David L Wagner, Michiel F. WallisDeVries, Catrin Westphal, Thomas E White, Vicky L Wilkins, Paul H Williams, Kris A G Wyckhuys, Zeng-Rong Zhu, Hans de Kroon
    https://doi.org/10.1038/s41559-019-1079-8
  • One Earth
    2020

    Climate Extremes, Rewilding, and the Role of Microhabitats

    Climate extremes are expected to become more commonplace and more severe, putting species and ecosystems at unprecedented risks. We recommend that rewilding programs can create conditions for ecosystems to endure and recover rapidly from climate extremes by incorporating ecosystem engineers of various body sizes and life forms.

    https://doi.org/10.1016/j.oneear.2020.05.010
  • Ecological Entomology
    2020

    Honeydew composition and its effect on life-history parameters of hyperparasitoids

    Frank A,C. van Neerbos, Jetske G. de Boer, Lucia Salis, W. Tollenaar, Martine Kos, Louise E.M. Vet, Jeff A. Harvey
    1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free-living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem-feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew-producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew-producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew-producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth-trophic-level organisms, not only those associated with honeydew-producing insects but also ?interlopers? without such a natural association.
    https://doi.org/10.1111/een.12799
  • Plant and Soil
    2020

    Antagonistic interactions between above- and belowground biota reduce their negative effects on a tree species

    Qiang Yang, Arjen Biere, Jeff A. Harvey, Jianqing Ding, Evan Siemann
    Aims: Plants in nature are confronted by a variety of beneficial and antagonistic above- and belowground organisms, including leaf herbivores, soil fungi, and soil nematodes. While their individual effects are usually well studied, their joint effects on plant performance are less well known. Synergistic or antagonistic interactions between these organisms would mean that their joint effects on plant performance are more or less detrimental or beneficial than expected from their individual effects. Methods: We conducted a factorial greenhouse experiment in which we manipulated the presence of aboveground herbivores (weevils), soil nematodes, and soil fungi using addition (weevil) or removal (fungicide, nematicide) treatments to test how these groups of organisms alone and in combination affect Triadica sebifera biomass production, when grown individually or under intraspecific competition. Results: Soil fungi and aboveground weevils alone each strongly decreased plant root and total biomass. Interestingly, soil nematodes alone slightly reduced plant biomass but they mitigated the negative impacts of aboveground weevils, indicating antagonism in their effects on plant biomass. However, in the presence of soil fungi this antagonism was less pronounced, illustrating the complexity of interactive effects of aboveground and belowground biota on plant biomass. Aboveground herbivory increased nematode infections, but only in the absence of soil fungi. Intraspecific competition strongly enhanced nematode infection loads and slightly decreased T. sebifera root biomass but did not modulate the direction or the strength of interactions among these aboveground and belowground biota. Conclusions: Our findings indicate that joint effects of antagonistic above- and belowground biota on plant performance can be less detrimental than expected from their individual effects. These results highlight the importance of considering the roles of plant aboveground and belowground interactions from a systems perspective.
    https://doi.org/10.1007/s11104-020-04642-w
  • Pest Management Science
    2020

    Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests

    Antonino Cusumano, Jeff A. Harvey, Mitchel E. Bourne, Erik H. Poelman, Jetske G. de Boer
    Insect hyperparasitoids are fourth trophic level organisms that commonly occur in terrestrial food webs, yet they are relatively understudied. These top‐carnivores can disrupt biological pest control by suppressing the populations of their parasitoid hosts, leading to pest outbreaks, especially in confined environments such as greenhouses where augmentative biological control is used. There is no effective eco‐friendly strategy that can be used to control hyperparasitoids. Recent advances in the chemical ecology of hyperparasitoid foraging behavior have opened opportunities for manipulating these top‐carnivores in such a way that biological pest control becomes more efficient. We propose various infochemical‐based strategies to manage hyperparasitoids. We suggest that a push‐pull strategy could be a promising approach to ‘push’ hyperparasitoids away from their parasitoid hosts and ‘pull’ them into traps. Additionally, we discuss how infochemicals can be used to develop innovative tools improving biological pest control (i) to restrict accessibility of resources (e.g. sugars and alternative hosts) to primary parasitoid only or (ii) to monitor hyperparasitoid presence in the crop for early detection. We also identify important missing information in order to control hyperparasitoids and outline what research is needed to reach this goal. Testing the efficacy of synthetic infochemicals in confined environments is a crucial step towards the implementation of chemical ecology‐based approaches targeting hyperparasitoids. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
    https://doi.org/10.1002/ps.5679
  • Molecular Ecology
    2020

    Detoxification of plant defensive glucosinolates by an herbivorous caterpillar is beneficial to its endoparasitic wasp

    Ruo Sun, Rieta Gols, Jeff A. Harvey, Michael Reichelt, Jonathan Gershenzon, Sagar S. Pandit, Daniel G. Vassão
    Plant chemical defences impact not only herbivores, but also organisms in higher trophic levels that prey on or parasitize herbivores. While herbivorous insects can often detoxify plant chemicals ingested from suitable host plants, how such detoxification affects endoparasitoids that use these herbivores as hosts is largely unknown. Here, we used transformed plants to experimentally manipulate the major detoxification reaction used by Plutella xylostella (diamondback moth) to deactivate the glucosinolate defences of its Brassicaceae host plants. We then assessed the developmental, metabolic, immune, and reproductive consequences of this genetic manipulation on the herbivore as well as its hymenopteran endoparasitoid Diadegma semiclausum. Inhibition of P. xylostella glucosinolate metabolism by plant-mediated RNA interference increased the accumulation of the principal glucosinolate activation products, the toxic isothiocyanates, in the herbivore, with negative effects on its growth. Although the endoparasitoid manipulated the excretion of toxins by its insect host to its own advantage, the inhibition of herbivore glucosinolate detoxification slowed endoparasitoid development, impaired its reproduction, and suppressed the expression of genes of a parasitoid-symbiotic polydnavirus that aids parasitism. Therefore, the detoxification of plant glucosinolates by an herbivore lowers its toxicity as a host and benefits the parasitoid D. semiclausum at multiple levels.
    https://doi.org/10.1111/mec.15613
  • Insects
    2020

    Range-expansion in processionary moths and biological control

    Global climate change is resulting in a wide range of biotic responses, including changes in diel activity and seasonal phenology patterns, range shifts polewards in each hemisphere and/or to higher elevations, and altered intensity and frequency of interactions between species in ecosystems. Oak (Thaumetopoea processionea) and pine (T. pityocampa) processionary moths (hereafter OPM and PPM, respectively) are thermophilic species that are native to central and southern Europe. The larvae of both species are gregarious and produce large silken ‘nests’ that they use to congregate when not feeding. During outbreaks, processionary caterpillars are capable of stripping foliage from their food plants (oak and pine trees), generating considerable economic damage. Moreover, the third to last instar caterpillars of both species produce copious hairs as a means of defence against natural enemies, including both vertebrate and invertebrate predators, and parasitoids. These hairs contain the toxin thaumetopoein that causes strong allergic reactions when it comes into contact with human skin or other membranes. In response to a warming climate, PPM is expanding its range northwards, while OPM outbreaks are increasing in frequency and intensity, particularly in northern Germany, the Netherlands, and southern U.K., where it was either absent or rare previously. Here, we discuss how warming and escape from co-evolved natural enemies has benefitted both species, and suggest possible strategies for biological control. View Full-Text. © 2020 by the authors. Licensee MDPI, Basel, Switzerland.
    https://doi.org/10.3390/insects11050267
  • Basic and Applied Ecology
    2020

    Shared enemies exert differential mortality on two competing parasitic wasps

    Dhaval K. Vyas, Ryan L. Paul, Michael W. Gates, Tristan Kubik, Jeff A. Harvey, Boris C. Kondratieff, Paul J. Ode
    Abstracta Classical biological control programs introduce primary parasitoids into new geographic regions, often exposing them to existing populations of hyperparasitoids. Hyperparasitoids are frequently implicated in the failure of parasitoid biological control agents to establish and provide control of insect pests. The outcome of competition among two or more parasitoid species may be altered if the parasitoids are differentially attacked by the same hyperparasitoids. A reliable assessment of the hyperparasitoid community is needed to understand how top-down trophic interactions influence the effectiveness of introduced parasitoids. We examined the diversity of hyperparasitoids attacking Cotesia glomerata in Colorado (USA), where the congener C. rubecula is absent. We compared this diversity with the hyperparasitoid community of C. glomerata and C. rubecula from Maryland (USA) where both wasps co-occur and use the imported cabbageworm (Pieris rapae) as their main host. Field collected C. glomerata broods were analyzed to examine the relationship between brood sizes and the adult sex ratio and the likelihood of attack by different hyperparasitoid species. A total of nine hyperparasitoid species were found in Colorado, of which four species also occurred in Maryland. While larger C. glomerata broods experienced increased odds of hyperparasitism, C. glomerata developing in larger broods had higher per capita survivorship than those developing in smaller broods. The proportion of adult male C. glomerata in a brood increased with brood size in both non-hyperparasitized and hyperparasitized broods, suggesting that female C. glomerata were not preferentially hyperparasitized. Hyperparasitoids inflicted greater mortality on C. rubecula than on C. glomerata. This differential hyperparasitism may enable the coexistence of C. glomerata with its congener C. rubecula, which usually outcompetes and displaces C. glomerata.
    https://doi.org/10.1016/j.baae.2020.04.007
  • Environmental Entomology
    2020

    Population- and Species-Based Variation of Webworm–Parasitoid Interactions in Hogweeds (Heracelum spp.) in the Netherlands

    Jeff A. Harvey, Paul J. Ode, Rieta Gols
    In three Dutch populations of the native small hogweed (Heracleum sphondylium L. [Apiales: Apiaceae]), and one of the invasive giant hogweed (H. mantegazzianum Sommeier and Levier [Apiales: Apiaceae]), interactions between a specialist herbivore, the parsnip webworm (Depressaria radiella), and its associated parasitoids were compared during a single growing season. We found host plant species-related differences in the abundance of moth pupae, the specialist polyembryonic endoparasitoid, Copidosoma sosares, the specialist pupal parasitoid, Barichneumon heracliana, and a potential hyperparasitoid of C. sosares, Tyndaricus scaurus Walker (Hymenoptera: Encyrtidae). Adult D. radiella body mass was similar across the three small hogweed populations, but moths and their pupal parasitoid B. heracliana were smaller when developing on giant than on small hogweeds where the two plants grew in the same locality (Heteren). Mixed-sex and all-male broods of C. sosares were generally bigger than all-female broods. Furthermore, adult female C. sosares were larger than males and adult female mass differed among the three small hogweed populations. The frequency of pupal parasitism and hyperparasitism also varied in the different H. sphondylium populations. These results show that short-term (intra-seasonal) effects of plant population on multitrophic insects are variable among different species in a tightly linked food chain.
    https://doi.org/10.1093/ee/nvaa052
  • Arthropod-Plant Interactions
    2020

    Exogenous application of plant hormones in the field alters aboveground plant–insect responses and belowground nutrient availability, but does not lead to differences in plant–soil feedbacks

    Robin Heinen, Katja Steinauer, Jon De Long, R. Jongen, Arjen Biere, Jeff A. Harvey, T. Martijn Bezemer
    Plant–soil feedbacks of plants that are exposed to herbivory have been shown to differ from those of plants that are not exposed to herbivores. Likely, this process is mediated by jasmonic acid (JA) and salicylic acid (SA) defense pathways, which are induced by aboveground herbivory. Furthermore, exogenous application of these phytohormones to plants alters belowground communities, but whether this changes plant–soil feedbacks in natural systems is unknown. We applied exogenous sprays of JA and SA individually and in combination to field plots in a restored grassland. Control plots were sprayed with demineralized water. After three repeated application rounds, we transplanted seedlings of the plant–soil feedback model plant Jacobaea vulgaris as phytometer plants to test the effects of potential phytohormone-mediated changes in the soil, on plant performance during the response phase. We further measured how exogenous application of phytohormones altered plant-related ecosystem characteristics (plot-level); soil chemistry, plot productivity, insect communities and predation. Biomass of the phytometer plants only co-varied with plot productivity, but was not influenced by phytohormone applications. However, we did observe compound-specific effects of SA application on insect communities, most notably on parasitoid attraction, and of JA application on soil nitrogen levels. Although we did not find effects on plant–soil feedbacks, the effects of exogenous application of phytohormones did alter other ecosystem-level processes related to soil nutrient cycling, which may lead to legacy effects in the longer term. Furthermore, exogenous application of phytohormones led to altered attraction of specific insect groups.
    https://doi.org/10.1007/s11829-020-09775-4
  • Insects
    10-2019

    Generalism in Nature ... The Great Misnomer: Aphids and Wasp Parasitoids as Examples

    Hugh D. Loxdale, Adalbert Balog, Jeff A. Harvey
    In the present article we discuss why, in our view, the term ‘generalism’ to define the dietary breadth of a species is a misnomer and should be revised by entomologists/ecologists with the more exact title relating to the animal in question’s level of phagy—mono-, oligo, or polyphagy. We discard generalism as a concept because of the indisputable fact that all living organisms fill a unique ecological niche, and that entry and exit from such niches are the acknowledged routes and mechanisms driving ecological divergence and ultimately speciation. The term specialist is probably still useful and we support its continuing usage simply because all species and lower levels of evolutionary diverge are indeed specialists to a large degree. Using aphids and parasitoid wasps as examples, we provide evidence from the literature that even some apparently highly polyphagous agricultural aphid pest species and their wasp parasitoids are probably not as polyphagous as formerly assumed. We suggest that the shifting of plant hosts by herbivorous insects like aphids, whilst having positive benefits in reducing competition, and reducing antagonists by moving the target organism into ‘enemy free space’, produces trade-offs in survival, involving relaxed selection in the case of the manicured agro-ecosystem.
    https://doi.org/10.3390/insects10100314
  • Ecological Research
    01-09-2019

    Invasive moth facilitates use of a native food plant by other native and invasive arthropods

    Jeff A. Harvey, Rieta Gols, Brittany Smith, Paul J. Ode
    Abstract Organisms that invade new habitats exploit new resources or niches and influence native species. Here, we examine how an invasive moth, the parsnip webworm (Depressaria radiella, formerly D. pastinacella), facilitates interactions with other arthropods in spatially separated populations of native cow parsnip (Heracleum maximum) in the Rocky Mountains (New Mexico and Colorado). We compare this with results on small hogweed (Heracleum sphondylium) in the Netherlands, where both the plant and herbivore are native. Larvae of D. radiella feed in webs on ripening fruits of their food plants. Mature caterpillars descend the hollow stems into which they chew a hole, enter the stem and pupate. Other arthropods enter the stems through these holes. Plants in all populations of cow parsnip/hogweed contained either moth pupae and/or webworms mummified by their main parasitoid, Copidosoma sosares that also been introduced into parts of the United States. In both countries, earwigs (Forficula auricularia), which are also invasive in the United States, were the dominant arthropod to utilize webworm-perforated stems, although there was more within-site variability in abundance of earwigs in the United States than in the Netherlands. The woodlouse, Porcelio scaber, which is native to Eurasia but also established in the United States, was abundant in stems of Dutch hogweeds but absent in stems of American cow parsnips. Other native herbivores (e.g., mirid bugs), were collected in stems at sites in both continents. Moreover, the number of various arthropods found in perforated stems correlate positively with the number of holes found in these stems.
    https://doi.org/10.1111/1440-1703.12035
  • Insects
    09-2019

    Variation in Performance and Resistance to Parasitism of Plutella xylostella Populations

    Rieta Gols, GAYLORD A. DESURMONT, Jeff A. Harvey
    Two major ecological factors determine the fitness of an insect herbivore: the ability to overcome plant resistance strategies (bottom-up effects) and the ability to avoid or resist attack by natural enemies such as predators and parasitoids (top-down effects). In response to differences in selection pressure, variation may exist in host-plant adaptation and immunity against parasitism among populations of an insect herbivore. We investigated the variation in larval performance of six different Plutella xylostella populations originating from four continents when feeding on a native Dutch plant species, Brassica rapa. One of the used populations has successfully switched its host plant, and is now adapted to pea. In addition, we determined the resistance to attack by the endoparasitoid Diadegma semiclausum originating from the Netherlands (where it is also native) and measured parasitoid performance as a proxy for host resistance against parasitism. Pupal mortality, immature development times, and adult biomass of P. xylostella differed significantly across populations when feeding on the same host plant species. In addition, parasitism success differed in terms of parasitoid adult emergence and their biomass, but not their development times. Variation among natural populations of insects should be considered more when studying interactions between plants and insects up the food chain.
    https://doi.org/10.3390/insects10090293
  • Ecology
    16-07-2019

    Rain downpours affect survival and development of insect herbivores: the specter of climate change?

    Cong Chen, Jeff A. Harvey, Arjen Biere, Rieta Gols
    Abstract Changes in the frequency, duration, and intensity of rainfall events are among the abiotic effects predicted under anthropogenic global warming. Heavy downpours may profoundly affect the development and survival of small organisms such as insects. Here, we examined direct (physically on the insects) and indirect (plant-mediated) effects of simulated downpours on the performance of caterpillars of two lepidopteran herbivores (Plutella xylostella and Pieris brassicae) feeding on black mustard (Brassica nigra) plants. Host plants were exposed to different rainfall regimes both before and while caterpillars were feeding on the plants in an attempt to separate direct and indirect (plant-mediated) effects of rainfall on insect survival and development. In two independent experiments, downpours were simulated as a single long (20 min) or as three short (5 min) daily events. Downpours had a strong negative direct effect on the survival of P. xylostella, but not on that of P. brassicae. Direct effects of downpours consistently increased development time of both herbivore species, whereas effects on body mass depended on herbivore species and downpour frequency. Caterpillar disturbance by rain and recorded microclimatic cooling by 5°C may explain extended immature development. Indirect, plant-mediated effects of downpours on the herbivores were generally small, despite the fact that sugar concentrations were reduced and herbivore induction of secondary metabolites (glucosinolates) was enhanced in plants exposed to rain. Changes in the frequency of precipitation events due to climate change may impact the survival and development of insect herbivores differentially. Broader effects of downpours on insects and other arthropods up the food chain could seriously impair and disrupt trophic interactions, ultimately destabilizing communities.
    https://doi.org/10.1002/ecy.2819
  • Entomologia Experimentalis et Applicata
    01-05-2019

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

    Rieta Gols, Vera I.D. Ros, Paul J. Ode, Dhaval K. Vyas, Jeff A. Harvey
    Abstract In natural populations of insect herbivores, genetic differentiation is likely to occur due to variation in host plant utilization and selection by the local community of organisms with which they interact. In parasitoids, engaging in intimate associations with their host during immature development, local variation may exist in host quality for parasitoid development. We compared the development of a gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae), collected in The Netherlands, in three strains and three caterpillar instars (L1?L3) of its main host, Pieris brassicae L. (Lepidoptera: Pieridae). Hosts had been collected in The Netherlands and France, and were reared in the laboratory for one generation. We also used an established Dutch laboratory strain that had not been exposed to parasitoids for at least 24 generations. Parasitoid survival to adulthood was inversely correlated with host instar at parasitism. Adult parasitoid body mass was largest when hosts were parasitized as L1 and smallest when hosts were parasitized as L3, whereas egg-to-adult development time was quickest on L3 hosts and slowest on L1 hosts. Higher survival and faster development of C. glomerata on French L2 hosts also showed that there is variation in host-instar-related suitability. Many L2 and most L3 caterpillars that were parasitized exhibited signs of pathogen infection and perished within a few days of parasitism, whereas this never happened when hosts were parasitized as L1 or in non-parasitized control caterpillars. Our results reveal that, irrespective of the host strain, L1 hosts are optimally synchronized with C. glomerata development. By contrast, the high precocious mortality of L3 larvae may be due to stress-induced regulation by the parasitoid in order to ?force? its developmental program into synchrony with the developing parasitoid larvae. Our results underscore a potentially important role played by pathogens in mediating herbivore?parasitoid interactions that are host-instar-dependent in their expression.
    https://doi.org/10.1111/eea.12765
  • Functional Ecology
    01-04-2019

    Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level

    Cong Chen, Rieta Gols, Arjen Biere, Jeff A. Harvey
    Abstract Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource?consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels). Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons). We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens. Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature-dependent. In turn, the observed effects of AGW on the functional responses of the hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article.
    https://doi.org/10.1111/1365-2435.13277
  • Oikos
    2019

    Simulated heatwave conditions associated with global warming affect development and competition between hyperparasitoids

    Cong Chen, S. Helena Donner, Arjen Biere, Rieta Gols, Jeff A. Harvey
    Anthropogenic global warming and attendant effects like heatwaves affect the biology and ecology of both individuals and species within and across different trophic levels. Here, we examined the effects of a simulated heatwave on development of and competition between two hyperparasitoid wasps, Lysibia nana and Acrolyta nens when attacking the same host, cocoons of the primary parasitoid, Cotesia glomerata. Parasitized hosts were exposed to three different day and night temperature regimes (low, medium and high) that reflect cool, normal and heatwave conditions in the Netherlands. We found that higher temperatures decreased survival to eclosion more strongly in the hyperparasitoids than in their host. Heatwave conditions also shortened development time and led to the production of smaller adult wasps of both hyperparasitoid species in singly parasitized hosts. In multiparasitized hosts, L. nana won most of the contests when it oviposited first, irrespective of the time interval between the first and second parasitism, whereas A. nens only dominated when it had a 24 h head start or longer. Most importantly, our results show that L. nana in particular benefited in competition at higher temperatures, perhaps due to an increase in the metabolic rate and more rapid egg and/or larval development. This may potentially reduce opportunities for coexistence following heat waves. Our results suggest that heatwaves associated with global warming will enhance the rate of development, but negatively affect survival and other fitness-related traits in (hyper)parasitoids. Moreover, the outcome of larval competition may be determined via physiological responses that are species-specific and thus influence phenology.
    https://doi.org/10.1111/oik.06538
  • BioControl
    2019

    Effects of temperature and food source on reproduction and longevity of aphid hyperparasitoids of the genera Dendrocerus and Asaphes

    Jetske G. de Boer, Lucia Salis, W. Tollenaar, L.J.M. van Heumen, T.P.M. Costaz, Jeff A. Harvey, Martine Kos, Louise E.M. Vet
    Hyperparasitoids of aphid parasitoids commonly occur in (sweet pepper) greenhouses, and can pose a threat to effective biological control of aphids. Here, we studied life history characteristics of laboratory colonies of Dendrocerus spp. Ratzeburg (Hymenoptera: Megaspilidae) and Asaphes spp. Walker (Pteromalidae) that originated from a commercial sweet pepper greenhouse. We aimed to clarify how these two hyperparasitoid taxa can coexist inside greenhouses. Hyperparasitoids of both taxa have a long lifespan that was extended significantly by food sources that are naturally available in a greenhouse environment, including aphid honeydew and sweet pepper flowers. Differences in sensitivity to decreased or increased temperatures did not appear to explain seasonal patterns in abundance of Dendrocerus spp. and Asaphes spp. in sweet pepper greenhouses. Instead, Dendrocerus spp. may have an advantage early in the season because it thrives on aphid honeydew, while Asaphes spp. may do better later in the season because of its long lifespan and extensive reproductive period.
    https://doi.org/10.1007/s10526-019-09934-4
  • Journal of Insect Behavior
    2019

    Reproduction and Offspring Sex Ratios Differ Markedly among Closely Related Hyperparasitoids Living in the Same Microhabitats

    Jeff A. Harvey, Lucas de Haan, Oriol Verdeny-Vilalta, Bertanne Visser, Rieta Gols
    Closely related species in nature usually exhibit very similar phylogenetically conserved traits, such as reproduction, behavior and development. Here, we compared fecundity schedules, lifetime reproductive success and offspring sex ratios in three congeneric facultative hyperparasitoid wasps that exhibit several overlapping traits and which co-occur in the same small-scale habitats. Gelis agilis, G. proximus and G. hortensis are abundant in meadows and forest edge habitats in the Netherlands. Gelis agilis is asexual (all female), whereas the other two species reproduce sexually. Here they developed on cocoons of the primary parasitoid Cotesia glomerata. When provided with unlimited hosts, lifetime reproductive success was three times higher in G. proximus than in G. agilis with G. hortensis producing intermediate numbers of offspring. All three species depleted their teneral reserves during their lives. Females of G. proximus and G. hortensis lived significantly longer than females of G. agilis. Offspring sex ratios in young G. proximus mothers were female-biased and marginally male-biased in G. hortensis. As mothers aged, however, the ratio of male:female progeny produced rapidly increased until no daughters emerged later in life. Our results reveal significant differences in reproductive traits among the three species despite them co-occurring in the same microhabitats, being very closely related and morphologically similar. The increase in the production of male progeny by Gelis mothers over time suggests a depletion in sperm number or viability with age. This is especially interesting, given that Gelis species are among the least fecund parasitoids thus far studied. It is likely that in the field most Gelis mothers are probably only able to parasitize a few hosts and to maintain the production of female offspring.
    https://doi.org/10.1007/s10905-019-09730-z
  • Oecologia
    2019

    Hyperparasitoids exploit herbivore-induced plant volatiles during host location to assess host quality and non-host identity

    Antonino Cusumano, Jeff A. Harvey, Marcel Dicke, Erik H. Poelman
    Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing hyperparasitoids to find their preferred hosts in heterogeneous environments.
    https://doi.org/10.1007/s00442-019-04352-w
  • Oecologia
    2019

    Ecological dissociation and re-association with a superior competitor alters host selection behavior in a parasitoid wasp

    Dhaval K. Vyas, Jeff A. Harvey, Ryan L. Paul, George E. Heimpel, Paul J. Ode
    Interspecific competition for limited resources can drive ecological specialization and trait expression. Organisms released from intense competition may exploit a broader range of resources, but if reunited with stronger competitors, survivorship may depend on foraging behaviors that reduce competition. We compared the host selection behavior of the parasitoid Cotesia glomerata from two North American populations that differ in their association with Cotesia rubecula, a superior competitor. Both parasitoids originate from Europe and attack the imported cabbageworm (a.k.a. small cabbage white) Pieris rapae, but C. glomerata was introduced into North America almost a century before C. rubecula. After re-association in North America, C. rubecula has displaced C. glomerata in several regions, but not in other regions. Host selection was measured in female C. glomerata from Maryland (MD) where it coexists with C. rubecula, and in conspecifics from Colorado (CO) where C. rubecula is absent. Unparasitized and C. rubecula-parasitized P. rapae hosts were used in choice tests to examine whether C. glomerata host selection behavior differed based on the population’s association history with C. rubecula. We found that C. glomerata from MD had a higher likelihood of avoiding hosts parasitized by C. rubecula (and thus avoiding competition) than did wasps from CO. The ability of C. glomerata to avoid hosts parasitized by C. rubecula may facilitate coexistence in MD; whereas, the lack of discrimination in CO populations of C. glomerata naïve to C. rubecula could contribute to the displacement of C. glomerata were C. rubecula to enter the same habitat.
    https://doi.org/10.1007/s00442-019-04470-5
  • Ecological Entomology
    2019

    Spatial and temporal diversity in hyperparasitoid communities of Cotesia glomerata on garlic mustard, Alliaria petiolata

    Robin Heinen, Jeff A. Harvey
    1. Interactions between two trophic levels can be very intimate, often making species dependent on each other, something that increases with specialisation. Some specialised multivoltine herbivores may depend on multiple plant species for their survival over the course of a growing season, especially if their food plants are short‐lived and grow at different times. Later generations may exploit different plant species from those exploited by previous generations.

    2. Multivoltine parasitoids as well as their natural enemies must also find their hosts on different food plants in different habitats across the season. Secondary hyperparasitoid communities have been studied on cocoons of the primary parasitoid, Cotesia glomerata (Hymenoptera: Braconidae), on black mustard (Brassica nigra) – a major food plant of its host, the large cabbage white (Pieris brassicae) – which grows in mid‐summer.

    3. Here, hyperparasitoid communities on C. glomerata pupal clusters were studied on an early‐season host, garlic mustard, Alliaria petiolata, over ‘time’ (one season, April–July) in six closely located ‘populations’ (c. 2 km apart), and within two different ‘areas’ at greater separation (c. 100 km apart). At the plant level, spatial effects of pupal ‘location’ (canopy or bottom) on the plant were tested.

    4. Although large‐scale separation (area) did not influence hyperparasitism, sampling time and small‐scale separation (population) affected hyperparasitism levels and composition of hyperparasitoid communities. Location on the plant strongly increased proportions of winged species in the canopy and proportions of wingless species in bottom‐located pupae.

    5. These results show that hyperparasitism varies considerably at the local level, but that differences in hyperparasitoid communities do not increase with spatial distance.
    https://doi.org/10.1111/een.12710
  • Journal of Insect Physiology
    21-03-2018

    Effects of plant-mediated differences in host quality on the development of two related endoparasitoids with different host-utilization strategies

    Jeff A. Harvey, Rieta Gols

    Among parasitoids that develop inside the bodies of feeding, growing hosts (so-called 'koinobiont' endoparasitoids), two strategies have evolved to dispose of host resources. The larvae of one group consumes most host tissues before pupation, whereas in the other the parasitoid larvae consume only host hemolymph and fat body and at maturity emerge through the host cuticle to pupate externally. Here we compared development and survival (to adult emergence) of two related larval endoparasitoids (Braconidae: Microgastrinae) of the diamondback moth, Plutella xylostella. Larvae of Dolichogenidea sicaria are tissue feeders whereas larvae of Cotesia vestalis are hemolymph feeders. Here, development of P. xylostella and the two parasitoids was compared on three populations (one cultivar [Cyrus], two wild, [Winspit and Kimmeridge]) of cabbage that have been shown to vary in direct defense and hence quality. Survival of P. xylostella and C. vestalis (to adult eclosion) did not vary with cabbage population, but did so in D. sicaria, where survival was lower when reared on the wild populations than on the cultivar. Furthermore, adult herbivore mass was significantly higher and development was significantly shorter in moths reared on the cultivar. The tissue-feeing D. sicaria was larger but took longer to develop than the hemolymph-feeder C. vestalis. The performance of both parasitoids was better on the cabbage cultivar than on the wild populations, although the effects were less apparent than in the host. Our results show that (1) differences in plant quality are diffused up the food chain, and (2) the effects of host quality are reflected on the development of both parasitoids.

    https://doi.org/10.1016/j.jinsphys.2018.03.006
  • Proceedings of the National Academy of Sciences of the United States of America
    2018

    Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids

    Feng Zhu, Antonino Cusumano, Janneke Bloem, Berhane T. Weldegergis, Alexandre Villela, Nina E. Fatouros, Joop J.A. van Loon, Marcel Dicke, Jeff A. Harvey, Heiko Vogel, Erik H. Poelman
    Symbiotic relationships benefit organisms in utilization of new niches. In parasitoid wasps, symbiotic viruses and venom that are injected together with wasp eggs into the host caterpillar suppress immune responses of the host and enhance parasitoid survival. We found that the virus also has negative effects on offspring survival when placing these interactions in a community context. The virus and venom drive a chain of interactions that includes the herbivore and its food plant and attracts the hyperparasitoid enemies of the parasitoid. Our results shed new light on the importance of symbionts associated with their host in driving ecological interactions and highlight the intricacy of how multispecies interactions are reflected in adaptations of individual species such as the host-finding behavior of hyperparasitoids.Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid's progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid's progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities.
    https://doi.org/10.1073/pnas.1717904115
  • BioScience
    2018

    Internet Blogs, Polar Bears, and Climate-Change Denial by Proxy

    Jeff A. Harvey, Daphne van den Berg, Jacintha Ellers, Remko Kampen, Tom Crowther, Peter Roessingh, Bart Verheggen, Rascha Nuijten, Eric S. Post, Stephan Lewandowsky, Ian Stirling, Meena Balgopal, Steven C. Amstrup, Michael E. Mann
    Increasing surface temperatures, Arctic sea-ice loss, and other evidence of anthropogenic global warming (AGW) are acknowledged by every major scientific organization in the world. However, there is a wide gap between this broad scientific consensus and public opinion. Internet blogs have strongly contributed to this consensus gap by fomenting misunderstandings of AGW causes and consequences. Polar bears (Ursus maritimus) have become a “poster species” for AGW, making them a target of those denying AGW evidence. Here, focusing on Arctic sea ice and polar bears, we show that blogs that deny or downplay AGW disregard the overwhelming scientific evidence of Arctic sea-ice loss and polar bear vulnerability. By denying the impacts of AGW on polar bears, bloggers aim to cast doubt on other established ecological consequences of AGW, aggravating the consensus gap. To counter misinformation and reduce this gap, scientists should directly engage the public in the media and blogosphere.
    https://doi.org/10.1093/biosci/bix133
  • Insect Science
    2018

    Finish line plant–insect interactions mediated by insect feeding mode and plant interference: a case study of Brassica interactions with diamondback moth and turnip aphid

    Mahmoud Soufbaf, Yaghoub Fathipour, Jeff A. Harvey, Cang Hui
    There are gaps in our understanding of plant responses under different insect phytophagy modes and their subsequent effects on the insect herbivores’ performance at late season. Here we compared different types of insect feeding by an aphid, Lipaphis erysimi, and a lepidopteran, Plutella xylostella, and how this affected defensive metabolites in leaves of 2 Brassica species when plants gain maturity. Thiocyanate concentrations after P. xylostella and L. erysimi feeding activities were the same. Total phenolics was higher after the phloem feeder feeding than the folivore activity. The plants compensatory responses (i.e., tolerance) to L. erysimi feeding was significantly higher than the responses to P. xylostella. This study showed that L. erysimi had higher carbon than P. xylostella whereas nitrogen in P. xylostella was 1.42 times that in L. erysimi. Population size of the phloem feeder was not affected by plant species or insect coexistence. However, there was no correlation between plant defensive metabolites and both insects’ population size and biomass. This suggests that plant root biomass and tolerance index after different insect herbivory modes are not necessarily unidirectional. Importantly, the interaction between the folivore and the phloem feeder insects is asymmetric and the phloem feeder might be a trickier problem for plants than the folivore. Moreover, as both plants’ common and special defenses decreased under interspecific interference, we suggest that specialist insect herbivores can be more challenged in ecosystems in which plants are not involved in interspecific interference.
    https://doi.org/10.1111/1744-7917.12439
  • Journal of Animal Ecology
    2018

    Responses of insect herbivores and their food plants to wind exposure and the importance of predation risk.

    Cong Chen, Arjen Biere, R. Gols, W. Halfwerk, Kees van Oers, Jeff A. Harvey
    Wind is an important abiotic factor that influences an array of biological processes, but it is rarely considered in studies on plant–herbivore interactions.
    Here, we tested whether wind exposure could directly or indirectly affect the performance of two insect herbivores, Plutella xylostella and Pieris brassicae, feeding on Brassica nigra plants.
    In a greenhouse study using a factorial design, B. nigra plants were exposed to different wind regimes generated by fans before and after caterpillars were introduced on plants in an attempt to separate the effects of direct and indirect wind exposure on herbivores.
    Wind exposure delayed flowering, decreased plant height and increased leaf concentrations of amino acids and glucosinolates.
    Plant‐mediated effects of wind on herbivores, that is effects of exposure of plants to wind prior to herbivore feeding, were generally small. However, development time of both herbivores was extended and adult body mass of P. xylostella was reduced when they were directly exposed to wind. By contrast, wind‐exposed adult P. brassicae butterflies were significantly larger, revealing a trade‐off between development time and adult size.
    Based on these results, we conducted a behavioural experiment to study preference by an avian predator, the great tit (Parus major) for last instar P. brassicae caterpillars on plants that were exposed to either control (no wind) or wind (fan‐exposed) treatments. Tits captured significantly more caterpillars on still than on wind‐exposed plants.
    Our results suggest that P. brassicae caterpillars are able to perceive the abiotic environment and to trade off the costs of extended development time against the benefits of increased size depending on the perceived risk of predation mediated by wind exposure. Such adaptive phenotypic plasticity in insects has not yet been described in response to wind exposure.
    https://doi.org/10.1111/1365-2656.12835
  • Journal of Ecology
    2018

    Plant community composition but not plant traits determine the outcome of soil legacy effects on plants and insects

    1.Plants leave species-specific legacies in the soil they grow in that can represent changes in abiotic or biotic soil properties. It has been shown that such legacies can affect future plants that grow in the same soil (plant-soil feedback, PSF). Such processes have been studied in detail, but mostly on individual plants. Here we study PSF effects at the community level and use a trait-based approach both in the conditioning phase and in the feedback phase to study how twelve individual soil legacies influence six plant communities that differ in root size.

    2.We tested if (I) grassland perennial species with large root systems would leave a stronger legacy than those with small root systems, (II) grass species would leave a more positive soil legacy than forbs and (III) communities with large root systems would be more responsive than small-rooted communities. We also tested (IV) whether a leaf chewing herbivore and a phloem feeder were affected by soil legacy effects in a community framework.

    3.Our study shows that the six different plant communities that we used respond differently to soil legacies of twelve different plant species and their functional groups. Species with large root systems did not leave stronger legacies than species with small root systems, nor were communities with large root systems more responsive than communities with root systems.

    4.Moreover, we show that when communities are affected by soil legacies, these effects carry over to the chewing herbivore Mamestra brassicae (Lepidoptera: Noctuidae) through induced behavioral changes resulting in better performance of a chewing herbivore on forb-conditioned soils than on grass-conditioned soils, whereas performance of the phloem feeder Rhopalosiphum padi (Hemiptera: Aphididae) remained unaffected.

    5.Synthesis: The results of this study shed light on the variability of soil effects found in previous work on feedbacks in communities. Our study suggests that the composition of plant communities determines to a large part the response to soil legacies. Furthermore, the responses to soil legacies of herbivores feeding on the plant communities that we observed, suggests that in natural ecosystems, the vegetation history may also have an influence on contemporary herbivore assemblages. This opens up exciting new areas in plant-insect research and can have important implications for insect pest management.
    https://doi.org/10.1111/1365-2745.12907
  • Journal of Chemical Ecology
    2018

    Ant-like Traits in Wingless Parasitoids Repel Attack from Wolf Spiders

    Jeff A. Harvey, Bertanne Visser, Marl Lammers, Janine Mariën, Jonathan Gershenzon, Paul J. Ode, Robin Heinen, Rieta Gols, Jacintha Ellers
    A recent study showed that a wingless parasitoid, Gelis agilis, exhibits a suite of ant-like traits that repels attack from wolf spiders. When agitated, G. agilis secreted 6-methyl-5-hepten-2-one (sulcatone), which a small number of ant species produce as an alarm/panic pheromone. Here, we tested four Gelis parasitoid species, occurring in the same food chain and microhabitats, for the presence of sulcatone and conducted two-species choice bioassays with wolf spiders to determine their degree of susceptibility to attack. All four Gelis species, including both winged and wingless species, produced sulcatone, whereas a closely related species, Acrolyta nens, and the more distantly related Cotesia glomerata, did not. In two-choice bioassays, spiders overwhelmingly rejected the wingless Gelis species, preferring A. nens and C. glomerata. However, spiders exhibited no preference for either A. nens or G. areator, both of which are winged. Wingless gelines exhibited several ant-like traits, perhaps accounting for the reluctance of spiders to attack them. On the other hand, despite producing sulcatone, the winged G. areator more closely resembles other winged cryptines like A. nens, making it harder for spiders to distinguish between these two species. C. glomerata was also preferred by spiders over A. nens, suggesting that other non-sulcatone producing cryptines nevertheless possess traits that make them less attractive as prey. Phylogenetic reconstruction of the Cryptinae reveals that G. hortensis and G. proximus are ‘sister’species, with G. agilis, and G.areator in particular evolving along more distant trajectories. We discuss the possibility that wingless Gelis species have evolved a suite of ant-like traits as a form, of mimicry to repel predators on the ground.
    https://doi.org/10.1007/s10886-018-0989-2
  • Frontiers in Ecology and Evolution
    2018

    Effects of soil organisms on aboveground plant-insect interactions in the field: patterns, mechanisms and the role of methodology

    Soil biota-plant interactions play a dominant role in terrestrial ecosystems. Through nutrient mineralization and mutualistic or antagonistic interactions with plants soil biota can affect plant performance and physiology and via this affect plant-associated aboveground insects. There is a large body of work in this field that has already been synthesized in various review papers. However, most of the studies have been carried out under highly controlled laboratory or greenhouse conditions.
    Here, we review studies that manipulate soil organisms of four dominant taxa (i.e. bacteria, fungi, nematodes and soil arthropods) in the field and assess the effects on the growth of plants and interactions with associated aboveground insects.
    We show that soil organisms play an important role in shaping plant-insect interactions in the field and that general patterns can be found for some taxa. Plant growth-promoting rhizobacteria generally have negative effects on herbivore performance or abundance, most likely through priming of defenses in the host plant. Addition of arbuscular mycorrhizal fungi (AMF) has positive effects on sap sucking herbivores, which is likely due to positive effects of AMF on nutrient levels in the phloem. The majority of AMF effects on chewers were neutral but when present, AMF effects were positive for specialist and negative for generalist chewing herbivores. AMF addition has negative effects on natural enemies in the field, suggesting that AMF may affect plant attractiveness for natural enemies, e.g. through volatile profiles. Alternatively, AMF may affect the quality of prey or host insects mediated by plant quality, which may in turn affect the performance and density of natural enemies. Nematodes negatively affect the performance of sap sucking herbivores (generally through phloem quality) but have no effect on chewing herbivores. For soil arthropods there are no clear patterns yet. We further show that the methodology used plays an important role in influencing the outcomes of field studies. Studies using potted plants in the field and studies that remove target soil taxa by means of pesticides are most likely to detect significant results. Lastly, we discuss suggestions for future research that could increase our understanding of soil biota-plant-insect interactions in the field.
    https://doi.org/10.3389/fevo.2018.00106
  • Chemoecology
    2018

    Seasonal and herbivore-induced dynamics of foliar glucosinolates in wild cabbage (Brassica oleracea)

    Rieta Gols, Nicole M. van Dam, Michael Reichelt, Jonathan Gershenzon, Ciska Raaijmakers, James M. Bullock, Jeff A. Harvey
    Levels of plant secondary metabolites are not static and often change in relation to plant ontogeny. They also respond to abiotic and biotic changes in the environment, e.g., they often increase in response to biotic stress, such as herbivory. In contrast with short-lived annual plant species, especially those with growing periods of less than 2–3 months, investment in defensive compounds of vegetative tissues in biennial and perennial species may also vary over the course of an entire growing season. In garden experiments, we investigated the dynamics of secondary metabolites, i.e. glucosinolates (GSLs) in the perennial wild cabbage (Brassica oleracea), which was grown from seeds originating from three populations that differ in GSL chemistry. We compared temporal long-term dynamics of GSLs over the course of two growing seasons and short-term dynamics in response to herbivory by Pieris rapae caterpillars in a more controlled greenhouse experiment. Long-term dynamics differed for aliphatic GSLs (gradual increase from May to December) and indole GSLs (rapid increase until mid-summer after which concentrations decreased or stabilized). In spring, GSL levels in new shoots were similar to those found in the previous year. Short-term dynamics in response to herbivory primarily affected indole GSLs, which increased during the 2-week feeding period by P. rapae. Herbivore-induced changes in the concentrations of aliphatic GSLs were population-specific and their concentrations were found to increase in primarily one population only. We discuss our results considering the biology and ecology of wild cabbage.
    https://doi.org/10.1007/s00049-018-0258-4
  • Journal of Scholarly Publishing
    01-10-2017

    Gold Open Access Publishing in Mega-Journals: Developing Countries Pay the Price of Western Premium Academic Output

    Jacintha Ellers, Tom Crowther, Jeff A. Harvey
    Open access publishing (OAP) makes research output freely available, and several national governments have now made OAP mandatory for all publicly funded research. Gold OAP is a common form of OAP where the author pays an article processing charge (APC) to make the article freely available to readers. However, gold OAP is a cause for concern because it drives a redistribution of valuable research money to support open access papers in ?mega-journals? with more permissive acceptance criteria. We present a data-driven evaluation of the financial ramifications of gold OAP and provide evidence that gold OAP in mega-journals is biased toward Western industrialized countries. From 2011 to 2015, the period of our data collection, countries with developing economies had a disproportionately greater share of articles published in the lower-tier mega-journals and thus paid article APCs that cross-subsidize publications in the top-tier journals of the same publisher. Conversely, scientists from Western developed countries had a disproportionately greater share of articles published in those same top-tier journals. The global inequity of the cross-subsidizing APC model was demonstrated across five different mega-journals, showing that the issue is a common problem. We need to develop stringent and fair criteria that address the global financial implications of OAP, as publication fees should reflect the real cost of publishing and be transparent for authors.
    https://doi.org/10.3138/jsp.49.1.89
  • Journal of Chemical Ecology
    06-2017

    Oviposition Preference for Young Plants by the Large Cabbage Butterfly

    Minghui Fei, Jeff A. Harvey, Yi Yin, Rieta Gols
    The effects of temporal variation in the quality of short-lived annual plants on oviposition preference and larval performance of insect herbivores has thus far received little attention. This study examines the effects of plant age on female oviposition preference and offspring performance in the large cabbage white butterfly Pieris brassicae. Adult female butterflies lay variable clusters of eggs on the underside of short-lived annual species in the family Brassicaceae, including the short-lived annuals Brassica nigra and Sinapis arvensis, which are important food plants for P. brassicae in The Netherlands. Here, we compared oviposition preference and larval performance of P. brassicae on three age classes (young, mature, and pre-senescing) of B. nigra and S. arvensis plants. Oviposition preference of P. brassicae declined with plant age in both plant species. Whereas larvae performed similarly on all three age classes in B. nigra, preference and performance were weakly correlated in S. arvensis. Analysis of primary (sugars and amino acids) and secondary (glucosinolates) chemistry in the plant shoots revealed that differences in their quality and quantity were more pronounced with respect to tissue type (leaves vs. flowers) than among different developmental stages of both plant species. Butterflies of P. brassicae may prefer younger and smaller plants for oviposition anticipating that future plant growth and size is optimally synchronized with the final larval instar, which contributes >80% of larval growth before pupation.
    https://doi.org/10.1007/s10886-017-0853-9
  • Royal Society Open Science
    22-03-2017

    Concurrence in the ability for lipid synthesis between life stages in insects

    Bertanne Visser, Denis S. Willett, Jeff A. Harvey, Hans T. Alborn
    The ability to synthesize lipids is critical for an organism’s fitness; hence, metabolic pathways, underlying lipid synthesis, tend to be highly conserved. Surprisingly, the majority of parasitoids deviate from this general metabolic model by lacking the ability to convert sugars and other carbohydrates into lipids. These insects spend the first part of their life feeding and developing in or on an arthropod host, during which they can carry over a substantial amount of lipid reserves. While many parasitoid species have been tested for lipogenic ability at the adult life stage, it has remained unclear whether parasitoid larvae can synthesize lipids. Here we investigate whether or not several insects can synthesize lipids during the larval stage using three ectoparasitic wasps (developing on the outside of the host) and the vinegar fly Drosophila melanogaster that differ in lipogenic ability in the adult life stage. Using feeding experiments and stable isotope tracing with gas chromatography/mass spectrometry, we first confirm lipogenic abilities in the adult life stage. Using topical application of stable isotopes in developing larvae, we then provide clear evidence of concurrence in lipogenic ability between larval and adult life stages in all species tested.
    https://doi.org/10.1098/rsos.160815
  • Journal of Insect Physiology
    2017

    Honey and honey-based sugars partially affect reproductive trade-offs in parasitoids exhibiting different life-history and reproductive strategies

    Jeff A. Harvey, Tijl Essens, Rutger Las, Cindy van Veen, Bertanne Visser, Jacintha Ellers, Robin Heinen, Rieta Gols
    Adult dietary regimes in insects may affect egg production, fecundity and ultimately fitness. This is especially relevant in parasitoid wasps where many species serve as important biological control agents of agricultural pests. Here, we tested the effect of honey and sugar diets on daily fecundity schedules, lifetime reproductive success and longevity in four species of parasitoid wasps when reared on their respective hosts. The parasitoid species were selected based on dichotomies in host usage strategies and reproductive traits. Gelis agilis and G. areator are idiobiont ecto-parasitoids that develop in non-growing hosts, feed on protein-rich host fluids to maximize reproduction as adults and produce small numbers of large eggs. Meteorus pulchricornis and Microplitis mediator are koinobiont endoparasitoids that develop inside the bodies of growing hosts, do not host-feed, and produce greater numbers of small eggs. Parasitoids were reared on diets of either pure honey (containing trace amounts of proteins), heated honey (with denatured proteins) and a honey-mimic containing sugars only. We hypothesized that the benefits of proteins in honey would enhance reproduction in the ectoparasitoids due to their high metabolic investment per egg, but not in the koinobionts. Pure honey diet resulted in higher lifetime fecundity in G. agilis compared with the honey-mimic, whereas in both koinobionts, reproductive success did not vary significantly with diet. Longevity was less affected by diet in all of the parasitoids, although there were variable trade-offs between host access and longevity in the four species. We argue that there are both trait-based and association-specific effects of supplementary nutrients in honey on reproductive investment and success in parasitoid wasps.
    https://doi.org/10.1016/j.jinsphys.2016.12.003
  • Ecological Entomology
    2017

    Comparing and contrasting life history variation in four aphid hyperparasitoids

    Rosemarije Buitenhuis, Jeff A. Harvey, Louise E.M. Vet, Guy Boivin, Jacques Brodeur
    1. In primary parasitoids, significant differences in life history and reproductive traits are observed among parasitoids attacking different stages of the same host species. Much less is known about hyperparasitoids, which attack different stages of primary parasitoids. 2. Parasitoids exploit hosts in two different ways. Koinobionts attack hosts that continue feeding and growing during parasitism, whereas idiobionts paralyse hosts before oviposition or attack non-growing host stages, e.g. eggs or pupae. 3. Koino-/idiobiosis in primary parasitoids are often associated with different expression of life history trade-offs, e.g. endo- versus ectoparasitism, high versus low fecundity and short versus long life span. 4. In the present study, life history parameters of two koinobiont endoparasitic species (Alloxysta victrix; Syrphophagus aphidivorus), and two idiobiont ectoparasitic species (Asaphes suspensus; Dendrocerus carpenteri) of aphid hyperparasitoids were compared. These hyperparasitoids attack eithe r the parasitoid larva in the aphid before it is killed and mummified by the primary parasitoid or the parasitoid prepupa or pupa in the dead aphid mummy. 5. There was considerable variation in reproductive success and longevity in the four species. The idiobiont A. suspensus produced the most progeny by far and had the longest lifespan. In contrast, the koinobiont A. victrix had the lowest fecundity. Other developments and life history parameters in the different species were variable. 6. The present results reveal that there was significant overlap in life history and reproductive traits among hyperparasitoid koinobionts and idiobionts, even when attacking the same host species, suggesting that selection for expression of these traits is largely association specific.
    https://doi.org/10.1111/een.12390
  • Chemoecology
    06-10-2016

    Effects of population-related variation in plant primary and secondary metabolites on aboveground and belowground multitrophic interactions

    Moniek Van Geem, Rieta Gols, Ciska Raaijmakers, Jeff A. Harvey
    Insects feeding on aboveground and belowground tissues can influence each other through their shared plant and this is often mediated by changes in plant chemistry. We examined the effects of belowground root fly (Delia radicum) herbivory on the performance of an aboveground herbivore (Plutella xylostella) and its endoparasitoid wasp (Cotesia vestalis). Insects were reared on three populations of wild cabbage (Brassica oleracea) plants, exhibiting qualitative and quantitative differences in root and shoot defense chemistry, that had or had not been exposed to root herbivory. In addition, we measured primary (amino acids and sugars) and secondary [glucosinolate (GS)] chemistry in plants exposed to the various plant population-treatment combinations to determine to what extent plant chemistry could explain variation in insect performance variables using multivariate statistics. In general, insect performance was more strongly affected by plant population than by herbivory in the opposite compartment, suggesting that population-related differences in plant quality are larger than those induced by herbivory. Sugar profiles were similar in the three populations and concentrations only changed in damaged tissues. In addition to population-related differences, amino acid concentrations primarily changed locally in response to herbivory. Whether GS concentrations changed in response to herbivory (indole GS) or whether there were only population-related differences (aliphatic GS) depended on GS class. Poor correlations between performance and chemical attributes made biological interpretation of these results difficult. Moreover, trade-offs between life history traits suggest that factors other than food nutritional quality contribute to the expression of life history traits.
    https://doi.org/10.1007/s00049-016-0222-0
  • Entomologia Experimentalis et Applicata
    05-2016

    Nutritional integration between insect hosts and koinobiont parasitoids in an evolutionary framework

    Jeff A. Harvey, Mima Malčická
    Mark Jervis was one of the world's foremost experts on life history and development strategies in parasitoids. He held a special place for the nutritional ecology of immature and adult parasitoids; his work on adult nutritional ecology and reproduction is considered seminal. Here, we discuss aspects of parasitoid growth and development, focusing on species that attack feeding, growing hosts (so-called koinobiont parasitoids). We provide a simple graphical model illustrating how selection pressures can alter host usage strategies, employing growth trajectories as a useful comparative tool. Furthermore, we discuss how the recent evolution of the hemolymph-feeding strategy in koinobionts has enabled these parasitoids to greatly expand the suitable size range of hosts, as well as providing additional adaptive functions such as gregarious development, resource sharing, and the use of the dying host as a ‘bodyguard’ against predators and hyperparasitoids. Overall, we conclude that koinobionts exhibit a wide array of strategies in exploiting and utilizing variably sized hosts in response to a suite of quite divergent selection pressures that influence their growth, development, and survival.
    https://doi.org/10.1111/eea.12426
  • Biological Control
    05-2016

    Dietary sugars and proline influence biological parameters of adult Trissolcus grandis, an egg parasitoid of Sunn pest, Eurygaster integriceps

    Nafiseh Hajirajabi, Morteza Movahedi Fazel, Jeff A. Harvey, Abbass Arbab, Shahriar Asgari
    Parasitoids are important natural enemies that are used in the biological control of insect herbivore pests. The egg parasitoid Trissolcus grandis Thompson (Hym. Scelionidae) is a major enemy of the Sunn pest, Eurygaster integriceps Puton (Hem. Scutelleridae), which in turn is one of the most destructive pests of wheat in the Middle East. Our objective was to develop an artificial diet to enhance the performance of T. grandis adults in biological control of the Sunn pest on wheat. We studied the combined effects of concentrations and the composition of sugars and proline on several life-history related parameters in T. grandis, including adult longevity, fecundity, fertility, sex ratio, oviposition period, the fecundity to oviposition period ratio, and reproductive index (e.g. intrinsic rate of increase) of T. grandis. Positive effects of sugar compounds and proline were observed on mean longevity in female and male wasps, as well as on offspring sex ratio (more females produced), oviposition period, fecundity, fertility and reproductive index. Our results thus reveal that the type of diet provided to T. grandis adults benefit the mass rearing efficiency of this important biological control agent
    https://doi.org/10.1016/j.biocontrol.2016.01.009
  • Environmental Entomology
    22-04-2016

    Black and Garlic Mustard Plants Are Highly Suitable for the Development of Two Native Pierid Butterflies

    Robin Heinen, Jeff A. Harvey, Rieta Gols
    In multivoltine insects that oviposit and develop on short-lived plants, different herbivore generations across a growing season often exploit different plant species. Here, we compare the development time, pupal mass, and survival of two closely related oligophagous herbivore species on two species of brassicaceous plants that grow in different habitats and which exhibit little overlap in temporal growth phenology. In central Europe, the green-veined white butterfly, Pieris napi L., is bivoltine, whereas the small cabbage white butterfly, Pieris rapae L., has two to three generations a year. Moreover, P. napi is primarily found in moist, open (e.g., meadow), and forest habitats, whereas P. rapae prefers drier, open habitats. Both butterflies were reared on Garlic mustard (Alliaria petiolata), which is shade-tolerant and grows early in spring in forest undergrowth, and Black mustard (Brassica nigra), which prefers open disturbed habitats and is most common in summer. Both host plant species differ in other traits such as secondary chemistry. We hypothesized that, owing to habitat preference, P. napi would develop equally well on both plants but that P. rapae would perform better on B. nigra The results provide partial support for this hypothesis, as both herbivores performed equally well on A. petiolata and B. nigra However, there were differences in these parameters that were species-specific: on both plants P. rapae developed faster and had larger pupae than P. napi Our results show that specialized herbivores can exploit different species of related plants that grow at different times of the season, enabling them to have multiple generations.
    https://doi.org/10.1093/ee/nvw024
  • Evolution
    01-2016

    Direct and indirect genetic effects in life-history traits of flour beetles (Tribolium castaneum)

    Esther D. Ellen, Katrijn Peeters, Merel Verhoeven, Rieta Gols, Jeff A. Harvey, Michael J. Wade, Marcel Dicke, Piter Bijma
    Indirect genetic effects (IGEs) are the basis of social interactions among conspecifics, and can affect genetic variation of nonsocial and social traits. We used flour beetles (Tribolium castaneum) of two phenotypically distinguishable populations to estimate genetic (co)variances and the effect of IGEs on three life-history traits: development time (DT), growth rate (GR), and pupal body mass (BM). We found that GR was strongly affected by social environment with IGEs accounting for 18% of the heritable variation. We also discovered a sex-specific social effect: male ratio in a group significantly affected both GR and BM; that is, beetles grew larger and faster in male-biased social environments. Such sex-specific IGEs have not previously been demonstrated in a nonsocial insect. Our results show that beetles that achieve a higher BM do so via a slower GR in response to social environment. Existing models of evolution in age-structured or stage-structured populations do not account for IGEs of social cohorts. It is likely that such IGEs have played a key role in the evolution of developmental plasticity shown by Tenebrionid larvae in response to density. Our results document an important source of genetic variation for GR, often overlooked in life-history theory.
    https://doi.org/10.1111/evo.12835
  • PLoS One
    2016

    Plant quantity affects development and survival of a gregarious insect herbivore and its endoparasitoid wasp.

    Minghui Fei, R. Gols, Feng Zhu, Jeff A. Harvey
    Virtually all studies of plant-herbivore-natural enemy interactions focus on plant quality as the major constraint on development and survival. However, for many gregarious feeding insect herbivores that feed on small or ephemeral plants, the quantity of resources is much more limiting, yet this area has received virtually no attention. Here, in both lab and semi-field experiments using tents containing variably sized clusters of food plants, we studied the effects of periodic food deprivation in a tri-trophic system where quantitative constraints are profoundly important on insect performance. The large cabbage white Pieris brassicae, is a specialist herbivore of relatively small wild brassicaceous plants that grow in variable densities, with black mustard (Brassica nigra) being one of the most important. Larvae of P. brassicae are in turn attacked by a specialist endoparasitoid wasp, Cotesia glomerata. Increasing the length of food deprivation of newly molted final instar caterpillars significantly decreased herbivore and parasitoid survival and biomass, but shortened their development time. Moreover, the ability of caterpillars to recover when provided with food again was correlated with the length of the food deprivation period. In outdoor tents with natural vegetation, we created conditions similar to those faced by P. brassicae in nature by manipulating plant density. Low densities of B. nigra lead to potential starvation of P. brassicae broods and their parasitoids, replicating nutritional conditions of the lab experiments. The ability of both unparasitized and parasitized caterpillars to find corner plants was similar but decreased with central plant density. Survival of both the herbivore and parasitoid increased with plant density and was higher for unparasitized than for parasitized caterpillars. Our results, in comparison with previous studies, reveal that quantitative constraints are far more important that qualitative constraints on the performance of gregarious insect herbivores and their gregarious parasitoids in nature.
    https://doi.org/10.1371/journal.pone.0149539
  • Journal of Insect Physiology
    2016

    Development of a solitary koinobiont hyperparasitoid in different instars of its primary and secondary hosts

    Jeff A. Harvey, Minghui Fei, Mark Lammers, Martine Kos, Feng Zhu, Robin Heinen, Erik H. Poelman, Rieta Gols
    Abstract Parasitoid wasps are excellent organisms for studying the allocation of host resources to different fitness functions such as adult body mass and development time. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism, whereas idiobiont parasitoids attack non-growing host stages or paralyzed hosts. Many adult female koinobionts attack a broad range of host stages and are therefore faced with a different set of dynamic challenges compared with idiobionts, where host resources are largely static. Thus far studies on solitary koinobionts have been almost exclusively based on primary parasitoids, yet it is known that many of these are in turn attacked by both koinobiont and idiobiont hyperparasitoids. Here we compare parasitism and development of a primary koinobiont hyperparasitoid, Mesochorus gemellus (Hymenoptera: Ichneumonidae) in larvae of the gregarious primary koinobiont parasitoid, Cotesia glomerata (Hymenoptera: Braconidae) developing in the secondary herbivore host, Pieris brassicae (Lepidoptera: Pieridae). As far as we know this is the first study to examine development of a solitary primary hyperparasitoid in different stages of its secondary herbivore host. Pieris brassicae caterpillars were parasitized as L1 by C. glomerata and then these parasitized caterpillars were presented in separate cohorts to M. gemellus as L3, L4 or L5 instar P. brassicae. Different instars of the secondary hosts were used as proxies for different developmental stages of the primary host, C. glomerata. Larvae of C. glomerata in L5 P. brassicae were significantly longer than those in L3 and L4 caterpillars. Irrespective of secondary host instar, every parasitoid cluster was hyperparasitized by M. gemellus but all only produced male progeny. Male development time decreased with host stage attacked, whereas adult male body mass did not, which shows that M. gemellus is able to optimally exploit older host larvae in terms of adult size despite their decreasing mass during the pupal stage. Across a range of cocoon masses, hyperparasitoid adult male body mass was approximately 84% as large as primary parasitoids, revealing that M. gemellus is almost as efficient at exploiting host resources as secondary (pupal) hyperparasitoids.
    https://doi.org/10.1016/j.jinsphys.2016.05.006
  • Basic and Applied Ecology
    2016

    Short-term seasonal habitat facilitation mediated by an insect herbivore

    Jeff A. Harvey, P.J. Ode, Mima Malčická, Rieta Gols
    In nature some organisms may facilitate others by creating shelter or other niches that they use for variable periods. We describe a natural tnultitrophic-species complex in the Netherlands involving a plant, the common hogweed (Heracteum sphondylium) a specialist chewing herbivore, the parsnip webworm (Depressaria pastinacella) and various arthropods associated with them. Larvae of D. pastinacella feed on H..sphondylium seeds and, after they have finished feeding, chew holes in the hollow stems where they pupate. In some areas of the country almost 50% of plants are attacked by webworms. The holes are used by other arthropods to gain access to the stems including herbivores, omnivores, predators and decomposers. The duration of plant occupancy varies between 3 and 4 months, until the plants die. Plants without moth-produced holes were always free of other arthropods, whereas plants with holes, in addition to pupae (and/or mummified-parasitized webworm larvae), often contained many woodlice, earwigs and/or spiders. Earwigs and woodlice perform important ecological functions as predators (in orchards) and decomposers respectively. Our results show that the simple biological activity of one herbivore species can have at least short-term effects on the local arthropod community.
    https://doi.org/10.1016/j.baae.2016.03.005
  • International Journal of Molecular Sciences
    2016

    Integrating insect life history and food plant phenology: flexible maternal choice is adaptive.

    Minghui Fei, Jeff A. Harvey, B.T. Weldegergis, T. Huang, K. Reijngoudt, Louise E.M. Vet, R. Gol
    Experience of insect herbivores and their natural enemies in the natal habitat is considered to affect their likelihood of accepting a similar habitat or plant/host during dispersal. Growing phenology of food plants and the number of generations in the insects further determines lability of insect behavioural responses at eclosion. We studied the effect of rearing history on oviposition preference in a multivoltine herbivore (Pieris brassicae), and foraging behaviour in the endoparasitoid wasp (Cotesia glomerata) a specialist enemy of P. brassicae. Different generations of the insects are obligatorily associated with different plants in the Brassicaceae, e.g., Brassica rapa, Brassica nigra and Sinapis arvensis, exhibiting different seasonal phenologies in The Netherlands. Food plant preference of adults was examined when the insects had been reared on each of the three plant species for one generation. Rearing history only marginally affected oviposition preference of P. brassicae butterflies, but they never preferred the plant on which they had been reared. C. glomerata had a clear preference for host-infested B. rapa plants, irrespective of rearing history. Higher levels of the glucosinolate breakdown product 3-butenyl isothiocyanate in the headspace of B. rapa plants could explain enhanced attractiveness. Our results reveal the potential importance of flexible plant choice for female multivoltine insects in nature
    https://doi.org/10.3390/ijms17081263
  • Evolutionary Ecology
    2016

    Divergent life history strategies in congeneric hyperparasitoids

    Bertanne Visser, Cécile Le Lann, Helen Snaas, Oriol Verdeny-Vilalta, Jeff A. Harvey
    Life histories can reveal important information on the performance of individuals within their environment and how that affects evolutionary change. Major trait changes, such as trait decay or loss, may lead to pronounced differences in life history strategies when tight correlations between traits exist. Here, we show that three congeneric hyperparasitoids (Gelis agilis, Gelis acarorum and Gelis areator) that have diverged in wing development and reproductive mode employ markedly different life history strategies. Potential fecundity of Gelis sp. varied, with the wingless G. acarorum maturing a much higher number of eggs throughout life compared with the other two species. Realized lifetime fecundity, in terms of total offspring number was, however, highest for the winged G. areator. The parthenogenic G. agilis invests its resources solely in females, whilst the sexually reproducing species both invested heavily in males to reduce competitive pressures for their female offspring. Longevity also differed between species, as did the direction of the reproduction-longevity trade-off, where reproduction is heavily traded off against longevity only in the asexual G. agilis. Resting metabolic rates also differed between the winged and wingless species, with the highest metabolic rate observed in the winged G. areator. Overall, these geline hyperparasitoids showed considerable divergence in life history strategies, both in terms of timing and investment patterns. Major trait changes observed between closely related species, such as the loss of wings and sexual reproduction, may contribute to the divergence in key life history traits.
    https://doi.org/10.1007/s10682-016-9819-6
  • Ecological Entomology
    2016

    Intrinsic competition between primary hyperparasitoids of the solitary endoparasitoid Cotesia rubecula

    Feng Zhu, Mark Lammers, Jeff A. Harvey, Erik H. Poelman
    1. In nature, competitive interactions occur when different species exploit similar niches. Parasitic wasps (parasitoids) often have narrow host ranges and need to cope with competitors that use the same host species for development of their offspring. When larvae of different parasitoid species develop in the same host, this leads to intrinsic and often contest com.petition. Thus far, m.ost studies on intrinsic competition have focused on primary parasitoids. However, competition among primary.hyperparasitoids, parasitic wasps that use primary parasitoids as a host, has been little studied. 2. This study investigated intrinsic competition between two primary hyperparasitoids, the gregarious Baryscapus galactopus and the solitary Mesochoru,s gemellu,s, which lay their eggs in primary parasitoid larvae of tesla rubecula, while those in turn are developing inside their herbivore host, Pieris rapae. The aims were to identify: (i) which hyperparasitoid is the superior competitor; and (ii) whether oviposition sequence affects the outcome of intrinsic competition. 3. The results show that B. galactopus won 70% of contests when the two hyperparasitoids parasitised the host at the same time, and 90% when 13. galactopus oviposited first. When M. gemellus had a 48 h head start, the two hyperparasitoids had an equal chance to win the competition. This suggests that M. galactopus is an intrinsically superior competitor to M. gemellu,s, Moreover, the outcome of competition is affected by time lags in oviposition events. 4. In contrast to what has been reported for primary parasitoids, we found that a. gregarious hyperparasitoid species had a competitive advantage over a solitary species.
    https://doi.org/10.1111/een.12303
  • European Journal of Entomology
    2016

    The cabbage moth or the sorrel moth (Lepidoptera: Noctuidae)?

    Jeff A. Harvey, Eke Hengeveld, Mima Malčická
    When insect herbivores develop over many generations on the same plant species, their descendants may evolve physiological adaptations that enable them to develop more successfully on that plant species than naive conspecifics. Here, we compared development of wild and lab-reared caterpillars of the cabbage moth, Mamestra brassicae, on a cultivar of cabbage Brassica oleracea (cv. Cyrus) and on a wild plant species, sorrel, Rumex acetosa, on which the wild strain had been collected and reared for two earlier consecutive generations. The lab strain had been reared on the same cabbage cultivar for more than 20 years representing > 200 generations. Survival to adult did not vary with strain or plant species. Both strains, however, developed significantly faster when reared on R. acetosa than B. oleracea. Pupae from the field strain were larger when reared on B. oleracea than on R. acetosa, whereas the identity of the plant species did not matter for the lab strain. Our results show that long-term rearing history on cabbage had little or no effect on M. brassicae performance, suggesting that some generalist herbivores can readily exploit novel plants that may be chemically very different from those on which they have long been intimately associated.
    https://doi.org/10.14411/eje.2016.041
  • Archives of Insect Biochemistry and Physiology
    2016

    WASP-ASSOCIATED FACTORS ACT IN INTERSPECIES COMPETITION DURING MULTIPARASITISM

    P.M. Magdaraog, T. Tanaka, Jeff A. Harvey
    Coexistence or displacement of parasitoids in hosts during intrinsic competitive interactions between different parasitoid species (multiparasitism) may depend on their life history traits and behavior. Intense competition for possession of hosts may lead to the elimination of the inferior competitor through physical attack and/or physiological suppression. However, the mechanisms of physiological suppression during multiparasitism remain unclear. Previous work has shown that first instar larvae of the solitary endoparasitoid Meteorus pulchricornis possess well-developed mandibles that are used to kill competitors. Two gregarious endoparasitoids, Cotesia kariyai and C. rufricus, share host resources especially when the time gap of oviposition is short. Here, we investigated the physiological influence of wasp-regulatory factors of the three endoparasitoids, M. pulchricornis, C. kariyai, and C. ruficrus, in their common host Mythimna separata. We found that MpVLP alone (or with venom) deleteriously affected the development of the two gregarious species. Similarly, CkPDV plus venom had toxic effect on M. pulchricornis eggs and immature larvae, although they were not harmful to immature stages of C. ruficrus. Cotesia kariyai and C. ruficrus were able to coexist mainly through the expression of regulatory factors and both could successfully emerge from a multiparasitized host. The injection of CkPDV plus venom after oviposition in L5 host larvae facilitated C. ruficrus development and increased the rate of successful parasitism from 9% to 62%. This suggests that the two gregarious parasitoid wasps exhibit strong phylogenetic affinity, favoring their coexistence and success in multiparasitized hosts. (C) 2016 Wiley Periodicals, Inc.
    https://doi.org/10.1002/arch.21321
  • Current Opinion in Insect Science
    12-2015

    Conserving host-parasitoid interactions in a warming world

    Anthropogenic global warming (AGW) represents a major threat to biodiversity at all levels of organization. Attendant changes with climate warming are abiotic effects such as changes in the duration and intensity of precipitation events, wind intensity and heat waves. Most importantly, AGW may unravel food webs by differentially affecting the biology and ecology of species involved in intimate interactions, where reciprocal selection forces are often strong. Amongst insects, plant–herbivoreparasitoid interactions fulfill this criterion, as many herbivores and parasitoids are highly specialized on specific food plants and hosts, respectively. Here, focusing on temperature-related effects of AGW, I discuss several potentially important eco-physiological herbivore and parasitoid responses to high temperatures. These include effects on plant traits such as volatile emissions and primary and secondary metabolism. In turn, how these will impact insect herbivores, their parasitoids, and thus trophic interaction webs is discussed. The possible direct metabolic effects of heat waves on insects are also described. I also argue that climate change does not affect biodiversity independently of other human-mediated environmental threats, including habitat loss and fragmentation, invasive species, and overuse of pesticides. Thus, the conservation of multitrophic interactions is critically dependent on reducing the impact of multiple anthropogenic stresses.
    https://doi.org/10.1016/j.cois.2015.09.001
  • Ecological Entomology
    2015

    Effects of plant diversity and structural complexity on parasitoid behaviour in a field experiment

    Olga Kostenko, Mark Lammers, Saskia S. Grootemaat, Thomas Kroon, Jeff A. Harvey, Moniek Van Geem, T. Martijn Bezemer
    1. In natural ecosystems, plants containing hosts for parasitoids are often embedded within heterogeneous plant communities. These plant communities surrounding host-infested plants may influence the host-finding ability of parasitoids.

    2. A release-recapture-approach was used to examine whether the diversity and structural complexity of the community surrounding a host-infested plant influences the aggregation behaviour of the leaf-miner parasitoid Dacnusa sibirica Telenga and naturally occurring local leaf-miner parasitoids. Released and locally present parasitoids were collected on potted Jacobaea vulgaris Gaertn.plants infested with the generalist leaf-miner Chromatomyia syngenesiae Hardy. The plants were placed in experimentally established plant communities differing in plant diversity (1–9 species) and habitat complexity (bare ground, mown vegetation, and tall vegetation). Additionally, parasitoids were reared out from host mines on the trap plants.

    3. Plant diversity did not influence the mean number of recaptured D. sibirica or captures of other locally present parasitoids but the number of recaptured parasitoids was influenced by habitat complexity. No D. sibirica parasitoids were recaptured in the bare ground plots or plots with mown vegetation. The mean number of recaptured D. sibirica generally increased with increasing complexity of the plant community, whereas locally present parasitoids were captured more frequently in communities with more bare ground. There was a unimodal relationship between the number of reared out parasitoids and diversity of the surrounding vegetation with the highest density of emerged parasitoids at intermediate diversity levels.

    4. The present study adds to the thus far limited body of literature examining the aggregation behaviour of parasitoids in the field and suggests that the preference of parasitoids to aggregate in complex versus simple vegetation is association specific and thus depends on the parasitoid species as well as the identity of the plant community.
    https://doi.org/10.1111/een.12251
  • Scientific Reports
    2015

    Multi-trait mimicry of ants by a parasitoid wasp

    Mima Malčická, T. Martijn Bezemer, Bertanne Visser, Mark Bloemberg, Charles J. P. Snart, Ian C. W. Hardy, Jeff A. Harvey
    https://doi.org/10.1038/srep08043
  • Functional Ecology
    2015

    Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis

    Rieta Gols, Roel Wagenaar, Erik H. Poelman, Marjolein Kruidhof, Joop J.A. van Loon, Jeff A. Harvey
    * Plant traits that enhance the attraction of the natural enemies of their herbivores have been postulated to function as an ‘indirect defence’. An important underlying assumption is that this enhanced attraction results in increased plant fitness due to reduced herbivory. This assumption has been rarely tested. * We investigated whether there are fitness consequences for the charlock mustard Sinapis arvensis, a short-lived outcrossing annual weedy plant, when exposed to groups of large cabbage white (Pieris brassicae) caterpillars parasitized by either one of two wasp species, Hyposoter ebeninus and Cotesia glomerata, that allow the host to grow during parasitism. Hyposoter ebeninus is solitary and greatly reduces host growth compared with healthy caterpillars, whereas C. glomerata is gregarious and allows the host to grow approximately as large as unparasitized caterpillars. Both healthy and parasitized P. brassicae caterpillars initially feed on the foliage, but later stages preferentially consume the flowers. * In a garden experiment, plants damaged by parasitized caterpillars produced more seeds than conspecific plants damaged by unparasitized caterpillars. Reproductive potential (germination success multiplied by total seed number) was similar for plants that were not exposed to herbivory and those that were damaged by parasitized caterpillars and lower for plants that were damaged by healthy unparasitized caterpillars. However, these quantitative seed traits negatively correlated with the qualitative seed traits, individual seed size and germination success, suggesting a trade-off between these two types of traits. * We show that parasitism of insect herbivores that feed on reproductive plant tissues may have positive fitness consequences for S. arvensis. The extent to which plant fitness may benefit depends on parasitoid lifestyle (solitary or gregarious), which is correlated with the amount of damage inflicted on these tissues by the parasitized host.
    https://doi.org/10.1111/1365-2435.12415
  • Ecological Entomology
    2015

    Host preference and offspring performance are linked in three congeneric hyperparasitoid species

    Jeff A. Harvey, Rieta Gols, Helen Snaas, Mima Malčická, Bertanne Visser
    1. The optimisation theory predicts that insect mothers should oviposit on resources on which they attain the highest exclusive fitness. The development of parasitoid wasps is dependent on limited host resources that are often not much larger than the adult parasitoid. 2. In the present study preference and development in three congeneric species of secondary hyperparasitoids attacking cocoons of two congeneric primary parasitoids that differ significantly in size were compared. Gelis agilis (Fabricius) and G. acarorum (L.) are wingless hyperparasitoids that forage in grassy habitats, whereas G. areator (Panzer) is fully winged and forages higher in the canopy of forbs. 3. The three species were reared on cocoons containing pupae of a small gregarious endoparasitoid, Cotesia glomerata (L.), and a larger solitary species, C. rubecula (Marshall), both of which develop in the caterpillars of pierid butterflies. 4. Adult mass was correlated with initial cocoon mass in all three species, whereas development time was unaffected. Wasps were larger when developing in C. rubecula. However, for a given host mass, wasps were larger when developing on the smaller host, C. glomerata. This suggests that there is a physiological limit to hyperparasitoid size that was exceeded when C. rubecula served as host. 5. All three hyperparasitoids strongly preferred to attack cocoons of the larger species, C. rubecula, often avoiding cocoons of C. glomerata entirely. 6. Preference and performance are correlated in the three Gelis species. However, owing to variation in the distribution and thus abundance of their hosts, it is argued that cumulative fitness may be still higher in the smaller host species.
    https://doi.org/10.1111/een.12165
  • Journal of Chemical Ecology
    2015

    Interactions between a belowground herbivore and primary and secondary root metabolites in wild cabbage

    Moniek Van Geem, Jeff A. Harvey, A.M. Cortesero, Ciska Raaijmakers, R. Gols
    Plants are attacked by both above- and belowground herbivores. Toxic secondary compounds are part of the chemical defense arsenal of plants against a range of antagonists, and are subject to genetic variation. Plants also produce primary metabolites (amino acids, nutrients, sugars) that function as essential compounds for growth and survival. Wild cabbage populations growing on the Dorset coast of the UK exhibit genetically different chemical defense profiles, even though they are located within a few kilometers of each other. As in other Brassicaceae, the defensive chemicals in wild cabbages constitute, among others, secondary metabolites called glucosinolates. Here, we used five Dorset populations of wild cabbage to study the effect of belowground herbivory by the cabbage root fly on primary and secondary chemistry, and whether differences in chemistry affected the performance of the belowground herbivore. There were significant differences in total root concentrations and chemical profiles of glucosinolates, amino acids, and sugars among the five wild cabbage populations. Glucosinolate concentrations not only differed among the populations, but also were affected by root fly herbivory. Amino acid and sugar concentrations also differed among the populations, but were not affected by root fly herbivory. Overall, population-related differences in plant chemistry were more pronounced for the glucosinolates than for amino acids and sugars. The performance of the root herbivore did not differ among the populations tested. Survival of the root fly was low (<40 %), suggesting that other belowground factors may override potential differences in effects related to primary and secondary chemistry.
    https://doi.org/10.1007/s10886-015-0605-7
  • Molecular Ecology
    2015

    Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles

    Feng Zhu, Colette Broekgaarden, Berhane T. Weldegergis, Jeff A. Harvey, Ben Vosman, Marcel Dicke, Erik H. Poelman
    Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant–hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.
    https://doi.org/10.1111/mec.13164
  • BioControl
    2015

    Development of two related endoparasitoids in larvae of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae)

    Mima Malčická, Jeff A. Harvey
    We compare the growth and development
    of two related solitary endoparasitoids (Braconidae,
    Microgastinae) in different instars (second and third)
    of the diamondback moth Plutella xylostella. Cotesia
    vestalis is a well-studied parasitoid whose larvae feed
    primarily on host hemolymph and fat body whereas
    Dolichogenidea sicaria is a parasitoid whose larvae
    consume the entire host caterpillar before pupation.
    Little is known about the biology of D. sicaria
    including its association with P. xylostella. When
    developing in L2 and L3 host instars, survival of both
    parasitoids to adult was similar. However, development
    time was longer in D. sicaria than in C. vestalis
    but the adult wasps were also larger. Both species were
    protandrous and exhibit sexual size dimorphism,
    where females were the larger sex. Our results suggest
    that D. sicaria is a promising new biological control
    agent of P. xylostella, augmenting better studied
    parasitoids such as C. vestalis.
    https://doi.org/10.1007/s10526-014-9627-2
  • Oecologia
    2015

    Habitat complexity reduces parasitoid foraging efficiency, but does not prevent orientation towards learned host plant odours

    Marjolein Kruidhof, A.L. Roberts, P.M. Magdaraog, P. Munoz, Rieta Gols, Louise E.M. Vet, T. Hoffmeister, Jeff A. Harvey
    It is well known that many parasitic wasps use herbivore-induced plant odours (HIPVs) to locate their inconspicuous host insects, and are often able to distinguish between slight differences in plant odour composition. However, few studies have examined parasitoid foraging behaviour under (semi-)field conditions. In nature, food plants of parasitoid hosts are often embedded in non-host-plant assemblages that confer both structural and chemical complexity. By releasing both naïve and experienced Cotesia glomerata females in outdoor tents, we studied how natural vegetation surrounding Pieris brassicae-infested Sinapis arvensis and Barbarea vulgaris plants influences their foraging efficiency as well as their ability to specifically orient towards the HIPVs of the host plant species on which they previously had a positive oviposition experience. Natural background vegetation reduced the host-encounter rate of naïve C. glomerata females by 47 %. While associative learning of host plant HIPVs 1 day prior to foraging caused a 28 % increase in the overall foraging efficiency of C. glomerata, it did not reduce the negative influence of natural background vegetation. At the same time, however, females foraging in natural vegetation attacked more host patches on host-plant species on which they previously had a positive oviposition experience. We conclude that, even though the presence of natural vegetation reduces the foraging efficiency of C. glomerata, it does not prevent experienced female wasps from specifically orienting towards the host-plant species from which they had learned the HIPVs.
    https://doi.org/10.1007/s00442-015-3346-y
  • American Naturalist
    2015

    Evolution of Plant Growth and Defense in a Continental Introduction

    Anurag A. Agrawal, Amy P. Hastings, Gideon S. Bradburd, Ellen C. Woods, Tobias Züst, Jeff A. Harvey, Tibor Bukovinszky
    Abstract Substantial research has addressed adaptation of nonnative biota to novel environments, yet surprisingly little work has integrated population genetic structure and the mechanisms underlying phenotypic differentiation in ecologically important traits. We report on studies of the common milkweed Asclepias syriaca, which was introduced from North America to Europe over the past 400 years and which lacks most of its specialized herbivores in the introduced range. Using 10 populations from each continent grown in a common environment, we identified several growth and defense traits that have diverged, despite low neutral genetic differentiation between continents. We next developed a Bayesian modeling approach to account for relationships between molecular and phenotypic differences, confirming that continental trait differentiation was greater than expected from neutral genetic differentiation. We found evidence that growth-related traits adaptively diverged within and between continents. Inducible defenses triggered by monarch butterfly herbivory were substantially reduced in European populations, and this reduction in inducibility was concordant with altered phytohormonal dynamics, reduced plant growth, and a trade-off with constitutive investment. Freedom from the community of native and specialized herbivores may have favored constitutive over induced defense. Our replicated analysis of plant growth and defense, including phenotypically plastic traits, suggests adaptive evolution following a continental introduction.
    https://doi.org/10.1086/681622
  • Plant Cell and Environment
    2014

    Alien interference: disruption of infochemical networks by invasive insect herbivores

    GAYLORD A. DESURMONT, Jeff A. Harvey, Nicole M. van Dam, SIMONA M. CRISTESCU, FLORIAN P. SCHIESTL, Salvatore Cozzolino, PETER ANDERSON, MATTIAS C. LARSSON, PAVEL KINDLMANN, HOLGER DANNER, TED C.J. TURLINGS
    Insect herbivores trigger various biochemical changes in plants, and as a consequence, affect other organisms that are associated with these plants. Such plant-mediated indirect effects often involve herbivore-induced plant volatiles (HIPVs) that can be used as cues for foraging herbivores and their natural enemies, and are also known to affect pollinator attraction. In tightly co-evolved systems, the different trophic levels are expected to display adaptive response to changes in HIPVs caused by native herbivores. But what if a new herbivore invades such a system? Current literature suggests that exotic herbivores have the potential to affect HIPV production, and that plant responses to novel herbivores are likely to depend on phylogenetic relatedness between the invader and the native species. Here we review the different ways exotic herbivores can disrupt chemically mediated interactions between plants and the key users of HIPVs: herbivores, pollinators, and members of the third (i.e. predators and parasitoids) and fourth (i.e. hyperparasitoids) trophic levels. Current theory on insect invasions needs to consider that disruptive effects of invaders on infochemical networks can have a short-term impact on the population dynamics of native insects and plants, as well as exerting potentially negative consequences for the functioning of native ecosystems.
    https://doi.org/10.1111/pce.12333
  • Journal of Chemical Ecology
    2014

    Chemical Defenses (Glucosinolates) of Native and Invasive Populations of the Range Expanding Invasive Plant Rorippa austriaca

    M. Huberty, K. Tielborger, Jeff A. Harvey, C. Muller, Mirka Macel
    Due to global warming, species are expanding their range to higher latitudes. Some range expanding plants have become invasive in their new range. The Evolution of Increased Competitive Ability (EICA) hypothesis and the Shifting Defense Hypothesis (SDH) predict altered selection on plant defenses in the introduced range of invasive plants due to changes in herbivore pressures and communities. Here, we investigated chemical defenses (glucosinolates) of five native and seven invasive populations of the Eurasian invasive range expanding plant, Rorippa austriaca. Further, we studied feeding preferences of a generalist and a specialist herbivore among the populations. We detected eight glucosinolates in the leaves of R. austriaca. 8-Methylsulfinyloctyl glucosinolate was the most abundant glucosinolate in all plants. There were no overall differences between native and invasive plants in concentrations of glucosinolates. However, concentrations among populations within each range differed significantly. Feeding preference between the populations by a generalist herbivore was negatively correlated with glucosinolate concentrations. Feeding by a specialist did not differ between the populations and was not correlated with glucosinolates. Possibly, local differences in herbivore communities within each range may explain the differences in concentrations of glucosinolates among populations. Little support for the predictions of the EICA hypothesis or the SDH was found for the glucosinolate defenses of the studied native and invasive R. austriaca populations.
    https://doi.org/10.1007/s10886-014-0425-1
  • Evolutionary Biology
    2014

    Convergence and Divergence in Direct and Indirect Life-History Traits of Closely Related Parasitoids (Braconidae: Microgastrinae)

    Jeff A. Harvey, Bertanne Visser, C. Le Lann, J. de Boer, J. Ellers, R. Gols
    [KEYWORDS: Cotesia Development Egg load Microplitis Phylogeny Reproduction] Closely related species in nature often show similarities in suites of direct and indirect traits that reveal aspects of their phylogenetic history. Here we tested how common descent affects trait evolution in several closely related parasitoid species in the genera Cotesia and Microplitis (Hymenoptera: Braconidae: Microgastrinae) by comparing development, resource use and allocation into reproduction and maintenance. Parasitoids in these genera exhibit traits, like haemolymph feeding as larvae and external pupation that are rare in most parasitoid lineages. The growth of parasitized hosts was reduced by 90 % compared with healthy hosts, and maximum host size depended to a large extent on adult parasitoid size. Development time was longer in the more generalist parasitoids than in the specialists. Adult body mass was sexually dimorphic in all Cotesia species, with females being larger, but not in Microplitis spp. In contrast, in one of the Microplitis species males were found to be the larger sex. Egg load dynamics during the first 6 days after emergence were highly variable but egg number was typically higher in Cotesia spp. compared to Microplitis spp. Longevity in the various species was only greater in female than in male wasps in two Microplitis sp. There was a clear inverse relationship between resource use and allocation, e.g. maximum egg load and longevity, in these parasitoids. Our results reveal that adaptation to constraints imposed by host quality and availability has resulted in trait convergence and divergence at the species, genus and subfamily level.
    https://doi.org/10.1007/s11692-013-9253-4
  • Arthropod Plant Interactions
    2014

    Small-scale spatial resource partitioning in a hyperparasitoid community

    Jeff A. Harvey, Helen Snaas, Mima Malčická, Bertanne Visser, T. Martijn Bezemer
    Plant-herbivore-natural enemy associations underpin ecological communities, and such interactions may go up to four (or even more) trophic levels. Here, over the course of a growing season, we compared the diversity of secondary hyperparasitoids associated with a common host, Cotesia glomerata, a specialized larval endoparasitoid of cabbage butterfly caterpillars that in turn feed on brassicaceous plants. Cocoon clusters of C. glomerata were pinned to similar to 30 Brassica nigra plants by pinning them either to branches in the canopy (similar to 1.5 m high) or to the base of the stem near the ground. The cocoons were collected a week later and reared to determine which hyper-parasitoid species emerged from them. This was done in four consecutive months (June-September). Cocoons placed in the canopy were primarily attacked by specialized winged hyperparasitoids (Lysibia nana, Acrolyta nens), whereas cocoons on the ground were attacked by both winged and generalist wingless hyperparasitoids Gelis acarorum, G. agilis), although this changed with season. There was much more temporal variation in the diversity and number of species attacking cocoons in the canopy than on the ground; the abundance of L. nana and A. nens varied from month to month, whereas P. semotus was only prevalent in August. By contrast, G. acarorum was abundant in all of the samples placed near the ground. Our results show that hyperparasitoids partition host resources at remarkably small vertical spatial scales. We argue that spatial differences in the distribution of natural enemies can contribute to the diversity patterns observed in the field.
    https://doi.org/10.1007/s11829-014-9319-y
  • Annual Review of Entomology
    2014

    Response of native insect communities to invasive plants

    Invasive plants can disrupt a range of trophic interactions in native communities. As novel resource they can affect the performance of native insect herbivores and their natural enemies such as parasitoids and predators, and this can lead to host shifts of these herbivores and natural enemies. Through the release of volatile compounds, and by changing the chemical complexity of the habitat, invasive plants can also affect the behavior of native insects such as herbivores, parasitoids and pollinators. Studies that compare insects on related native and invasive plants in invaded habitats show that the abundance of insect herbivores is often lower on invasive plants, but that damage levels are similar. The impact of invasive plants on the population dynamics of resident insect species has been rarely examined, but invasive plants can influence the spatial and temporal dynamics of native insect (meta)populations and communities, ultimately leading to changes at the landscape level.
    https://doi.org/10.1146/annurev-ento-011613-162104
  • Naturwissenschaften
    2014

    Development of a generalist predator, Podisus maculiventris, on glucosinolate sequestering and non-sequestering prey

    Moniek Van Geem, Jeff A. Harvey, R. Gols
    Insect herbivores exhibit various strategies to counter the toxic effects of plant chemical defenses. These strategies include the detoxification, excretion, and sequestration of plant secondary metabolites. The latter strategy is often considered to provide an additional benefit in that it provides herbivores with protection against natural enemies such as predators. Profiles of sequestered chemicals are influenced by the food plants from which these chemicals are derived. We compared the effects of sequestration and nonsequestration of plant secondary metabolites in two specialist herbivores on the development of a generalist predator, Podisus maculiventris. Profiles of glucosinolates, secondary metabolites characteristic for the Brassicaceae, are known to differ considerably both inter- and intraspecifically. Throughout their immature (=nymphal) development, the predator was fed on larval stages of either sequestering (turnip sawfly, Athalia rosae) or nonsequestering (small cabbage white butterfly, Pieris rapae) prey that in turn had been feeding on plants originating from three wild cabbage (Brassica oleracea) populations that have previously been shown to differ in their glucosinolate profiles. We compared survival, development time, and adult body mass as parameters for bug performance. Our results show that sequestration of glucosinolates by A. rosae only marginally affected the development of P. maculiventris. The effects of plant population on predator performance were variable. We suggest that sequestration of glucosinolates by A. rosae functions not only as a defensive mechanism against some predators, but may also be an alternative way of harmlessly dealing with plant allelochemicals.
    https://doi.org/10.1007/s00114-014-1207-x
  • New Phytologist
    2014

    Variation in plant defences among populations of a range-expanding plant: consequences for trophic interactions

    Taiadjana Fortuna, Silvia Eckert, Jeff A. Harvey, Louise E.M. Vet, Caroline Mueller, Rieta Gols
    Although plant-herbivore-enemy interactions have been studied extensively in cross-continental plant invasions, little is known about intra-continental range expanders, despite their rapid spread globally. Using an ecological and metabolomics approach, we compared the insect performance of a generalist and specialist herbivore and a parasitoid, as well as plant defence traits, among native, exotic invasive and exotic non-invasive populations of the Turkish rocket, Bunias orientalis, a range-expanding species across parts of Eurasia. In the glasshouse, the generalist herbivore, Mamestra brassicae, and its parasitoid, Microplitis mediator, performed better on non-native than on native plant populations. Insect performance did not differ between the two non-native origins. By contrast, the specialist herbivore, Pieris brassicae, developed poorly on all populations. Differences in trichome densities and in the metabolome, particularly in the family-specific secondary metabolites (i.e. glucosinolates), may explain population-related variation in the performance of the generalist herbivore and its parasitoid. Total glucosinolate concentrations were significantly induced by herbivory, particularly in native populations. Native populations of B.orientalis are generally better defended than non-native populations. The role of insect herbivores and dietary specialization as a selection force on defence traits in the range-expanding B.orientalis is discussed.
    https://doi.org/10.1111/nph.12983
  • Ecological Entomology
    2014

    Food plant and herbivore host species affect the outcome of intrinsic competition among parasitoid larvae

    Erik H. Poelman, Rieta Gols, Alex V. Gumovsky, Anne-Marie Cortesero, Marcel Dicke, Jeff A. Harvey
    1. In nature, several parasitoid species often exploit the same stages of a common herbivore host species and are able to coexist despite competitive interactions amongst them. Less is known about the direct effects of resource quality on intrinsic interactions between immature parasitoid stages. The present study is based on the hypothesis that variation in the quality or type of plant resources on which the parasitoids indirectly develop may be complementary and thus facilitate niche segregation favouring different parasitoids in intrinsic competition under different dietary regimes. 2. The present study investigated whether two herbivore species, the cabbage butterflies Pieris brassicae and Pieris rapae (Pieridae), and the quality of two important food plants, Brassica oleracea and Brassica nigra (Brassicaceae), affect the outcome of intrinsic competition between their primary larval endoparasitoids, the gregarious Cotesia glomerata (Braconidae) and the solitary Hyposoter ebeninus (Ichneumonidae). 3. Hyposoter ebeninus is generally an intrinsically superior competitor over C.glomerata. However, C.glomerata survived more antagonistic encounters with H.ebeninus when both developed in P.brassicae rather than in P.rapae caterpillars, and while its host was feeding on B.nigra rather than B.oleracea. Moreover, H.ebeninus benefitted from competition by its higher survival in multiparasitised hosts. 4. These results show that both plant and herbivore species mediate the battleground on which competitive interactions between parasitoids are played out and may affect the outcomes of these interactions in ways that enable parasitoids to segregate their niches. This in turn may promote coexistence among parasitoid species that are associated with the same herbivore host.
    https://doi.org/10.1111/een.12150
  • Pest Management Science
    2014

    Desiccation and cold storage of Galleria mellonella cadavers and effects on in vivo production of Steinernema carpocapsae

    X. Wang, H. Wang, Q.Z. Feng, X.Y. Cui, R.Y. Liu, Y.B. Sun, G.C. Li, H. Tan, D.M. Song, W. Liu, W.B. Ruan, Jeff A. Harvey
    BACKGROUNDDirect application of insect cadavers infected with entomopathogenic nematodes (EPN) can successfully control target pest insects. Little is known about the effects of environmental factors (desiccation and temperature) on the production process for infective juveniles (IJ) in insects. RESULTSWe examined the effects of desiccation time and cold storage (6.7 degrees C) on IJ production of the nematode Steinernemacarpocapsae in Galleriamellonella cadavers at 30.8 and 57% humidity. Under desiccation, the IJ yield in cadavers increased gradually and reached a maximum on day5. IJ yield gradually declined from day6 onwards and was almost zero by day15. In general, cold storage at 6.7 degrees C caused negative effects on IJ production in desiccated cadavers. Approximately 56h post infection was the time at which nematodes were most sensitive to low temperatures during development in cadavers. Five-day desiccated cadavers generated higher mortality and more rapid death of Galleriamellonella larvae than using newly (day0) desiccated cadavers. CONCLUSIONThis study describe methods of optimizing rearing techniques such as desiccation and cold storage to promote the mass production and application of EPN- infected host cadavers for the field control of insect pests. (c) 2013 Society of Chemical Industry
    https://doi.org/10.1002/ps.3685
  • Journal of Animal Ecology
    2014

    Seasonal phenology of interactions involving short-lived annual plants, a multivoltine herbivore and its endoparasitoid wasp

    Minghui Fei, R. Gols, Jeff A. Harvey
    Spatial-temporal realism is often missing in many studies of multitrophic interactions, which are conducted at a single time frame and/or involving interactions between insects with a single species of plant. In this scenario, an underlying assumption is that the host-plant species is ubiquitous throughout the season and that the insects always interact with it. We studied interactions involving three naturally occurring wild species of cruciferous plants, Brassica rapa, Sinapis arvensis and Brassica nigra, that exhibit different seasonal phenologies, and a multivoltine herbivore, the large cabbage white butterfly, Pieris brassicae, and its gregarious endoparasitoid wasp, Cotesia glomerata. The three plants have very short life cycles. In central Europe, B. rapa grows in early spring, S. arvensis in late spring and early summer, and B. nigra in mid to late summer. P. brassicae generally has three generations per year, and C. glomerata at least two. This means that different generations of the insects must find and exploit different plant species that may differ in quality and which may be found some distance from one another. Insects were either reared on each of the three plant species for three successive generations or shifted between generations from B. rapa to S. arvensis to B. nigra. Development time from neonate to pupation and pupal fresh mass were determined in P. brassicae and egg-to-adult development time and body mass in C. glomerata. Overall, herbivores performed marginally better on S. arvensis and B. nigra plants than on B. rapa plants. Parasitoids performance was closely tailored with that of the host. Irrespective as to whether the insects were shifted to a new plant in successive generations or not, development time of P. brassicae and C. glomerata decreased dramatically over time. Our results show that there were some differences in insect development on different plant species and when transferred from one species to another. However, all three plants were of generally high quality in terms of insect performance. We discuss ecological and evolutionary constraints on insects that must search in new habitats for different plant species over successive generations
    https://doi.org/10.1111/1365-2656.12122
  • Behavioral Ecology and Sociobiology
    2014

    Consequences of resource competition for sex allocation and discriminative behaviors in a hyperparasitoid wasp

    Bertanne Visser, C. Le Lann, Helen Snaas, I.W. Hardy, Jeff A. Harvey
    [KEYWORDS: Reproduction Local mate competition Local resource competition Sex ratio Parasitoid Gelis acororum] Population-wide mating patterns can select for equal parental investment in both sexes, but limiting resources, such as mates or developmental substrates, can increase competition leading to biased sex ratios in favor of either sex. Such competition for resources typically occurs in spatially structured populations, where dispersal is limited. In this laboratory study, we investigate if and how resource competition affects sex allocation, discriminative behaviors and competitive interactions of the wingless hyperparasitoid Gelis acororum, which exploits patchily distributed hosts. We show that G. acororum sex ratios are male-biased and that this is not a consequence of constrained reproduction by virgin females. Our results suggest that this pattern of reproductive investment, which is only rarely observed in parasitoids, is a consequence of resource limitation, in terms of hosts rather than mates. Further, G. acororum appears not to respond to intrinsic host quality or to prior oviposition in its host. When competing inter-specifically for host resources, G. acororum outcompetes its congener Gelis agilis, but does so mainly when ovipositing on the host first. Overall, our results suggest that host resource limitation could be an important environmental factor shaping sex allocation in G. acororum, with competition taking place both intra- and inter-specifically.
    https://doi.org/10.1007/s00265-013-1627-1
  • Basic and Applied Ecology
    2014

    Reciprocal interactions between native and introduced populations of common milkweed, Asclepias syriaca, and the specialist aphid, Aphis nerii

    Tibor Bukovinszky, R. Gols, A.A. Agrawal, C. Roge, T. Martijn Bezemer, Arjen Biere, Jeff A. Harvey
    Following its introduction into Europe (EU), the common milkweed (Asclepias syriaca) has been free of most specialist herbivores that are present in its native North American (NA) range, except for the oleander aphid Aphis nerii. We compared EU and NA populations of A. nerii on EU and NA milkweed populations to test the hypothesis that plant–insect interactions differ on the two continents. First, we tested if herbivore performance is higher on EU plants than on NA plants, because the former have escaped most of their herbivores and have perhaps been selected for lower defence levels following introduction. Second, we compared two A. nerii lines (one from each continent) to test whether genotypic differences in the herbivore may influence species interactions in plant–herbivore communities in the context of species introductions. The NA population of A. nerii developed faster, had higher fecundity and attained higher population growth rates than the EU population. There was no overall significant continental difference in aphid resistance between the plants. However, milkweed plants from EU supported higher population growth rates and faster development of the NA line of A. nerii than plants from NA. In contrast, EU aphids showed similar (low) performance across plant populations from both continents. In a second experiment, we examined how chewing herbivores indirectly mediate interactions between milkweeds and aphids, and induced A. syriaca plants from each continent by monarch caterpillars (Danaus plexippus) to compare the resulting changes in plant quality on EU aphid performance. As specialist chewing herbivores of A. syriaca are only present in NA, we expected that plants from the two continents may affect aphid growth in different ways when they are challenged by a specialist chewing herbivore. Caterpillar induction decreased aphid developmental times on NA plants, but not on EU plants, whereas fecundity and population growth rates were unaffected by induction on both plant populations. The results show that genetic variation in the plants as well as in the herbivores can determine the outcome of plant–herbivore interactions.
    https://doi.org/10.1016/j.baae.2014.07.004
  • Biological Control
    2014

    Trade-offs between developmental parameters of two endoparasitoids developing in different instars of the same host species

    Mima Malčická, Jeff A. Harvey
    Trade-offs amongst life history traits is a major theme in evolutionary biology. Parasitoid wasps are important biological control agents and make excellent organisms to examine trade-offs in fitness related traits such as size, development rate and survival. Here, we examined trait-related trade-offs in 2 solitary endoparasitoids developing in different stages (or instars) of the same caterpillar host, the cabbage moth Mamestra brassicae. Microplitis mediator is a small specialist parasitoid that attacks first (L1) to third (13) instars of M. brassicae; Meteorus pulchricornis is a larger highly generalized parasitoid that attacks L1-L4 instars of the same host species. When developing in early host instars (e.g. L1-L2), both parasitoids differently traded-off size against development time. In M. mediator, adult body mass was smaller in wasps developing in L1 than in L2 and L3 hosts, whereas development time was unaffected by instar. By contrast, adult body mass in M. pulchricornis was smaller and development time longer when developing in L1 and L2 than in L3 and L4 instars. Periodic starvation of M. brassicae caterpillars parasitized by M. pulchricornis further reduced adult mass and extended development time of wasps in L2 (but not L4) hosts. Maximum egg load in M. pulchricornis (but not M. mediator) was correlated with adult female body size. Our results imply that rapid development time is more important than body size for fitness in both species, although in M. pulchricornis both development time and adult size are traded off in determining the optimal phenotype. Developing a better understanding of association-specific patterns of development in parasitoids can assist in the optimization of mass rearing of these insects for biological control. (C) 2014 Elsevier Inc. All rights reserved. [KEYWORDS: Koinobiont Life-history Mamestra brassicae Meteorus pulchricornis Microplitis mediator PARASITOID WASPS
    https://doi.org/10.1016/j.biocontrol.2014.03.014
  • Oecologia
    2014

    Intra-specific variation in wild Brassica oleracea for aphid-induced plant responses and consequences for caterpillar–parasitoid interactions

    Y. Li, Marcel Dicke, Jeff A. Harvey, R. Gols
    [KEYWORDS: Cabbage Diadegma semiclausum Herbivory Leaf chewers Mamestra brassicae Microplitis mediator Plutella xylostella phloem feeders] Herbivore-induced plant responses not only influence the initiating attackers, but also other herbivores feeding on the same host plant simultaneously or at a different time. Insects belonging to different feeding guilds are known to induce different responses in the host plant. Changes in a plant’s phenotype not only affect its interactions with herbivores but also with organisms higher in the food chain. Previous work has shown that feeding by a phloem-feeding aphid on a cabbage cultivar facilitates the interaction with a chewing herbivore and its endoparasitoid. Here we study genetic variation in a plant’s response to aphid feeding using plants originating from three wild Brassica oleracea populations that are known to differ in constitutive and inducible secondary chemistry. We compared the performance of two different chewing herbivore species, Plutella xylostella and M. brassicae, and their larval endoparasitoids Diadegma semiclausum and M. mediator, respectively, on plants that had been infested with aphids (Brevicoryne brassicae) for 1 week. Remarkably, early infestation with B. brassicae enhanced the performance of the specialist P. xylostella and its parasitoid D. semiclausum, but did not affect that of the generalist M. brassicae, nor its parasitoid M. mediator. Performance of the two herbivore–parasitoid interactions also varied among the cabbage populations and the effect of aphid infestation marginally differed among the three populations. Thus, the effect of aphid infestation on the performance of subsequent attackers is species specific, which may have concomitant consequences for the assembly of insect communities that are naturally associated with these plants.
    https://doi.org/10.1007/s00442-013-2805-6
  • Journal of Chemical Ecology
    2014

    Body Odors of Parasitized Caterpillars Give Away the Presence of Parasitoid Larvae to Their Primary Hyperparasitoid Enemies

    Feng Zhu, Berhane T. Weldegergis, Boris Lhie, Jeff A. Harvey, Marcel Dicke, Erik H. Poelman
    Foraging success of parasitoids depends on the utilization of reliable information on the presence of their often, inconspicuous hosts. These parasitic wasps use herbivore-induced plant volatiles (HIPVs) that provide reliable cues on host presence. However, host searching of hyperparasitoids, a group of parasitoids that parasitize the larvae and pupae of other parasitoids, is more constrained. Their hosts do not feed on plants, and often are even concealed inside the body of the herbivore host. Hyperparasitoids recently have been found to use HIPVs of plants damaged by herbivore hosts in which the parasitoid larvae develop. However, hyperparasitoids that search for these parasitoid larvae may be confronted with healthy and parasitized caterpillars on the same plant, further complicating their host location. In this study, we addressed whether the primary hyperparasitoid Baryscapus galactopus uses caterpillar body odors to discriminate between unparasitized herbivores and herbivores carrying larvae of parasitoid hosts. We show that the hyperparasitoids made faster first contact and spent a longer mounting time with parasitized caterpillars. Moreover, although the three parasitoid hosts conferred different fitness values for the development of B. galactopus, the hyperparasitoids showed similar behavioral responses to caterpillar hosts carrying different primary parasitoid hosts. In addition, a two-chamber olfactometer assay revealed that volatiles emitted by parasitized caterpillars were more attractive to the hyperparasitoids than those emitted by unparasitized caterpillars. Analysis of volatiles revealed that body odors of parasitized caterpillars differ from unparasitized caterpillars, allowing the hyperparasitoids to detect their parasitoid host.
    https://doi.org/10.1007/s10886-014-0500-7
  • Biological Invasions
    2013

    A tritrophic approach to the preference–performance hypothesis involving an exotic and a native plant

    Taiadjana Fortuna, J. Woelke, Cees Hordijk, J. Jansen, Nicole M. van Dam, Louise E.M. Vet, Jeff A. Harvey
    [KEYWORDS: Exotic invasive species Volatiles Plant preference–performance Host shift Multitrophic interactions Bunias orientalis] Exotic plants often generate physical and chemical changes in native plant communities where they become established. A major challenge is to understand how novel plants may affect trophic interactions in their new habitats, and how native herbivores and their natural enemies might respond to them. We compared the oviposition preference and offspring performance of the crucifer specialist, Pieris brassicae, on an exotic plant, Bunias orientalis, and on a related native plant, Sinapis arvensis. Additionally, we studied the response of the parasitoid, Cotesia glomerata to herbivore-induced plant volatiles (HIPV) and determined the volatile blend composition to elucidate which compound(s) might be involved in parasitoid attraction. On both host plants we also compared the parasitism rate of P. brassicae by C. glomerata. Female butterflies preferred to oviposit on the native plant and their offspring survival and performance was higher on the native plant compared to the exotic. Although, headspace analysis revealed qualitative and quantitative differences in the volatile blends of both plant species, C. glomerata did not discriminate between the HIPV blends in flight-tent bioassays. Nevertheless, parasitism rate of P. brassicae larvae was higher on the native plant under semi-field conditions. Overall, P. brassicae oviposition preference may be more influenced by bottom-up effects of the host plant on larval performance than by top-down pressure exerted by its parasitoid. The potential for dietary breadth expansion of P. brassicae to include the exotic B. orientalis and the role of top-down processes played by parasitoids in shaping herbivore host shifts are further discussed.
    https://doi.org/10.1007/s10530-013-0459-2
  • Functional Ecology
    2013

    Variation in herbivore-induced plant volatiles corresponds with spatial heterogeneity in the level of parasitoid competition and parasitoid exposure to hyperparasitism

    Erik H. Poelman, Jeff A. Harvey, Joop J.A. van Loon, Louise E.M. Vet, Marcel Dicke
    Reproductive success for species in which offspring are confined to a distinct resource depends on the ability of parents to locate reproductive sites as well as the quality of these sites in terms of the food source, risk of predation and competition. To locate hosts for their offspring, parasitic wasps, or parasitoids, use plant odour blends induced by herbivore feeding. These herbivore-induced plant volatiles (HIPVs) may also be used by competitors and predators. Therefore, offspring of parasitoids that respond to the most conspicuous odours may find themselves more frequently involved in competition or predation risk. We studied cultivars of Brassica oleracea that are known to differ in volatile production that underlies attractiveness to parasitoids and asked whether variation in this parameter is associated with a heterogeneous distribution of intrinsic competition among parasitoid larvae and predation risk by hyperparasitoids that parasitize parasitoid larvae or pupae. We inoculated field-grown plants with Pieris caterpillars and, thereafter, exposed them to the natural parasitoid community. We measured the frequency of multiple incidences of parasitism in these herbivores. Cocoons of the parasitoids were collected to identify the degree of hyperparasitism associated with different Brassica cultivars. Pieris caterpillars on cultivars that were more attractive to Cotesia parasitoids were more commonly parasitized by several females of the same (superparasitism) or different wasp species (multiparasitism) than caterpillars on less attractive plants. Cocoons of parasitoids on attractive plants also more frequently produced hyperparasitoids. Our results show that there is heterogeneity in intrinsic competition and risk of hyperparasitism for parasitoids on different cabbage cultivars and that this heterogeneity is likely generated by variation in attraction of parasitoids to HIPVs of these cultivars. We conclude that parasitoids may find themselves between a rock and a hard place as cues for host presence may also predict high levels of competition and risk of predation. We speculate that this affects selection on parasitoid responses to plant odours and enhances selection on traits that make wasps better intrinsic or extrinsic competitors as well as selection for adaptive traits – such as crypsis – that protect them against hyperparasitoids.
    https://doi.org/10.1111/1365-2435.12114
  • Oikos
    2013

    Effect of belowground herbivory on parasitoid associative learning of plant odours

    Marjolein Kruidhof, M. De Rijk, D. Hoffmann, Jeff A. Harvey, Louise E.M. Vet, Roxina Soler
    Root herbivores can influence both the performance and the behaviour of parasitoids of aboveground insect herbivores through changes in aboveground plant quality and in the composition of the plant's odour blend. Here we show that root herbivory by Delia radicum larvae did not influence the innate preferences for plant odours of the two closely related parasitoid species Cotesia glomerata and C. rubecula, but did affect their learned preferences, and did so in an opposite direction. While C. glomerata learned to prefer the odour of plants with intact roots, C. rubecula learned to prefer the odour of root-infested plants. The learned preference of C. glomerata for the odour of plants with intact roots matches our previously published result of its better performance when developing in P. brassicae hosts feeding on this plant type. In contrast, the relatively stronger learned preference of C. rubecula for the odour of root-infested plants cannot be merely explained by its performance, as the results of our present study indicate that D. radicum root herbivory did not influence the performance of C. rubecula nor of its host P. rapae. Our results stress the importance of assessing the influence of root herbivores on both innate and learned responses of parasitoids to plant odours
    https://doi.org/10.1111/j.1600-0706.2012.00142.x
  • BioControl
    2013

    Inter- and intra-specific host discrimination in gregarious and solitary endoparasitoid wasps

    P.M. Magdaraog, T. Tanaka, Jeff A. Harvey
    In nature, most species of Lepidoptera are attacked by parasitoids, and some species may be hosts for several parasitoid species. When hosts are parasitized by more than one female of the same species (=superparasitism) or females of different species (=multiparasitism), then intrinsic competition occurs for control of host resources. To reduce competition, some parasitoids are able to recognize the difference between parasitized and unparasitized hosts. Inter- and intra-specific host discrimination were investigated in the two sympatric species, the gregarious Cotesia kariyai (Watanabe) and solitary Meteorus pulchricornis (Wesmael), endoparasitoids of the Oriental armyworm Mythimna separata (Walker). To measure host discrimination, choice experiments were conducted in which females of both species foraged and chose between healthy host larvae and hosts initially parasitized by either C. kariyai or M. pulchricornis. An olfactory test was also performed to examine the discrimination behavior of the two parasitoids. Our results showed that, in oviposition choice tests, both braconid female wasps were able to discriminate between unparasitized hosts and from four to seven day-old hosts previously attacked by conspecific and heterospecific wasps. On the other hand, superparasitism and multiparasitism occurred even in host larvae that were parasitized two days earlier. However, once the immature parasitoids hosts are at larval stage (1st and 2nd instar), super- and multiparasitism were avoided in the two-choice test, but the latter often occurred in the multiple-choice experiment. Host discrimination abilities may have been based on plant volatile signals incurred from damaged plants and internal mechanisms from four to seven post-parasitized hosts.
    https://doi.org/10.1007/s10526-013-9532-0
  • Entomologia Experimentalis et Applicata
    2013

    A bodyguard or a tastier meal? Dying caterpillar indirectly protects parasitoid cocoons by offering alternate prey to a generalist predator

    Jeff A. Harvey, D. Weber, P. De Clerq, R. Gol
    In some parasitic Hymenoptera the dying caterpillars remain attached or close to the parasitoid cocoons. It has been suggested that the caterpillars act as ‘bodyguards’ for the vulnerable cocoons and therefore protect them against predators and/or hyperparasitoids (the ‘usurpation hypothesis’). This hypothesis has been demonstrated in associations where the caterpillars remain active and/or aggressive after parasitism. However, in other associations the caterpillars are so physiologically depleted after parasitism that they are unable to physically defend the cocoons and instead sit atop them in a moribund state. In this study a generalist predator, the spined soldier bug, Podisus maculiventris Say (Hemiptera: Pentatomidae), was provided with cocoons of the gregarious endoparasitoid Cotesia glomerata L. and the solitary endoparasitoid Microplitis mediator Haliday (both Hymenoptera: Braconidae), in turn attended by their hosts, Pieris brassicae L. (Lepidoptera: Pieridae) and Mamestra brassicae L. (Lepidoptera: Noctuidae), respectively. Cotesia glomerata produces broods of up to 40 cocoons and the dying caterpillars sit atop the cocoons where they exhibit little response to physical stimuli. Previous studies reported that dying P. brassicae caterpillars were ineffective bodyguards against two species of hyperparasitoids. In both associations, the dying host caterpillars were significantly preferred as food by P. maculiventris over the parasitoid cocoons. However, in absence of caterpillars, the bugs readily attacked the C. glomerata cocoons. Alternatively, the survival of M. mediator was very low, irrespective of whether a caterpillar was present or not. Caterpillars attacked by M. mediator are several times smaller than those attacked by C. glomerata. Consequently, the predators ran out of food much more quickly in the former and switched from one prey to the other. We show that in some host–parasitoid associations the dying caterpillars provide more visually apparent or nutritionally superior prey, rather than acting as bodyguards.
    https://doi.org/10.1111/eea.12127
  • Annual Review of Entomology
    2013

    Intrinsic inter and intra-specific competition in parasitoid wasps

    Jeff A. Harvey, Erik H. Poelman, T. Tanaka
    Immature development of parasitoid wasps is restricted to resources found in a single host that is often similar in size to the adult parasitoid. When two or more parasitoids of the same or different species attack the same host, there is competition for monopolization of host resources. The success of intrinsic competition differs between parasitoids attacking growing hosts and parasitoids attacking paralyzed hosts. Furthermore, the evolution of gregarious development in parasitoids reflects differences in various developmental and behavioral traits, as these influence antagonistic encounters among immature parasitoids. Fitness-related costs (or benefits) of competition for the winning parasitoid reveal that time lags between successive attacks influence the outcome of competition. Physiological mechanisms used to exclude competitors include physical and biochemical factors that originate with the ovipositing female wasp or her progeny. In a broader multitrophic framework, indirect factors, such as plant quality, may affect parasitoids through effects on immunity and nutrition.
    https://doi.org/10.1146/annurev-ento-120811-153622
  • Frontiers in Plant Science
    2013

    The importance of aboveground-belowground interactions on the evolution and maintenance of variation in plant defence traits

    Moniek Van Geem, R. Gols, Nicole M. van Dam, Wim H. van der Putten, Taiadjana Fortuna, Jeff A. Harvey
    Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts. Aboveground - belowground studies have thus far focused on elucidating processes and underlying mechanisms that mediate the behavior and performance of invertebrates in opposite compartments. Less is known about genetic variation in plant traits as this applies to an above- belowground framework. For instance, although the field of genetic variation in aboveground plant traits on community-level interactions is well developed, most studies have ignored genetic variation in plant traits – such as defence - that may have evolved in response to pressures from the combined effects of above- and below ground interactions from antagonists and mutualists. Here, we discuss gaps in our understanding of genetic variation in plant- and consumer-related traits as they relate to aboveground and belowground multitrophic interactions. When metabolic resources are limiting, then multiple attack by antagonists in both domains may lead to trade-offs in where these resources are optimally invested. In nature, these trade-offs may critically depend upon their effects on plant fitness. Natural enemies of herbivores may also influence selection for different traits via top-down control. At larger scales these interactions may generate evolutionary ‘hotspots’ where the expression of various plant traits is the result of strong reciprocal selection via direct and indirect interactions. The role of abiotic factors in driving genetic variation in plant traits is also discussed.
    https://doi.org/10.3389/fpls.2013.00431
  • Molecular Ecology
    2013

    An ecogenomic analysis of herbivore-induced plant volatiles in Brassica juncea

    Vartika Mathur, T.O.G. Tytgat, Cees Hordijk, H.R. Harhangi, Jeroen Jansen, A.S. Reddy, Jeff A. Harvey, Louise E.M. Vet, Nicole M. van Dam
    [KEYWORDS: gene expression green leaf volatiles mustard parasitoids Spodoptera sulphides] Upon herbivore feeding, plants emit complex bouquets of induced volatiles that may repel insect herbivores as well as attract parasitoids or predators. Due to differences in the temporal dynamics of individual components, the composition of the herbivore-induced plant volatile (HIPV) blend changes with time. Consequently, the response of insects associated with plants is not constant either. Using Brassica juncea as the model plant and generalist Spodoptera spp. larvae as the inducing herbivore, we investigated herbivore and parasitoid preference as well as the molecular mechanisms behind the temporal dynamics in HIPV emissions at 24, 48 and 72 h after damage. In choice tests, Spodoptera litura moth preferred undamaged plants, whereas its parasitoid Cotesia marginiventris favoured plants induced for 48 h. In contrast, the specialist Plutella xylostella and its parasitoid C. vestalis preferred plants induced for 72 h. These preferences matched the dynamic changes in HIPV blends over time. Gene expression analysis suggested that the induced response after Spodoptera feeding is mainly controlled by the jasmonic acid pathway in both damaged and systemic leaves. Several genes involved in sulphide and green leaf volatile synthesis were clearly up-regulated. This study thus shows that HIPV blends vary considerably over a short period of time, and these changes are actively regulated at the gene expression level. Moreover, temporal changes in HIPVs elicit differential preferences of herbivores and their natural enemies. We argue that the temporal dynamics of HIPVs may play a key role in shaping the response of insects associated with plants.
    https://doi.org/10.1111/mec.12555
  • Journal of Insect Physiology
    2012

    Consequences of constitutive and induced variation in the host’s food plant quality for parasitoid larval development

    Tibor Bukovinszky, R. Gols, Hans M. Smid, G. Bukovinszkine-Kiss, Marcel Dicke, Jeff A. Harvey
    Constitutive and induced changes in plant quality impact higher trophic levels, such as the development 27 of parasitoids, in different ways. An efficient way to study how plant quality affects parasitoids is to 28 examine how the parasitoid larva is integrated within the host during the growth process. In two exper- 29 iments, we investigated the effects of varying nutritional quality of Brassica oleracea on parasitoid larval 30 development inside the host, the diamondback moth (Plutella xylostella). First, we compared larval 31 growth of the specialist Diadegma semiclausum and the generalist Diadegma fenestrale, when the host 32 was feeding on Brussels sprout plants that were either undamaged or were previously induced by cater- 33 pillar damage. Larvae of the generalist D. fenestrale showed lower growth rates than larvae of the special- 34 ist D. semiclausum, and this difference was more pronounced on herbivore-induced plants, suggesting 35 differences in host-use efficiency between parasitoid species. The growth of D. semiclausum larvae was 36 also analyzed in relation to herbivore induction on Brussels sprouts and on a wild B. oleracea strain. Par- 37 asitoid growth wasmore depressed on induced than on undamaged control plants, andmore on wild cab- 38 bage than on Brussels sprouts, which was largely explained by differences in host mass. The effects of 39 induction of wild Brassica on parasitoid development were pronounced early on, but as P. xylostella feed- 40 ing began inducing the previously undamaged control plants, the effect of induction disappeared, reveal- 41 ing a temporal component of plant–parasitoid interactions. This study demonstrates how insights into 42 the physiological aspects of host–parasitoid interactions can improve our understanding of the effects 43 of plant-related traits on parasitoid wasps.
    https://doi.org/10.1016/j.jinsphys.2011.12.017
  • Basic and Applied Ecology
    2012

    Performance of secondary parasitoids on chemically defended and undefended hosts

    S. van Nouhuys, J.H. Reudler, Arjen Biere, Jeff A. Harvey
    Defensive chemicals produced by plants can travel up the food chain by being sequestered by herbivores, and then in turn being sequestered by their parasitoids. Insect species with wide host ranges are predicted to perform poorly in the face of specific chemical defence. However, a species at a high trophic level is expected to have a wide host range. This creates a conflict for hyperparasitoids, many of which depend on specialized hosts. We studied the performance of two hyperparasitoids, Lysibia nana and Gelis agilis, both of which have wide host ranges, on two host species, one chemically defended and the other not. We predicted that both hyperparasitoids would perform better using the undefended host Cotesia glomerata than the defended host C. melitaearum, which sequesters terpenoid allelochemicals (iridoid glycosides). Furthermore, we expected that the progeny of G. agilis collected from an area where hosts defended by iridoid glycosides are absent (the Netherlands) would perform poorly using C. melitaearum in comparison with G. agilis collected from an area where C. melitaearum is a common host (angstrom land, Finland). In a series of laboratory experiments we found that, contrary to prediction, both hyperparasitoids performed well on both hosts, reaching a larger size on C. glomerata, but having a higher conversion efficiency and developing more quickly on the chemically defended C. melitaearum. Lysibia nana metabolized the plant derived iridoid glycosides, which are chemicals that it does not normally encounter. Cells agilis retained some of the iridoid glycosides. But whereas Finnish G. agilis retained both aucubin and catalpol, Dutch G. agilis mainly retained aucubin, illustrating that though generalists, local populations still cope differently with toxic allelochemicals.
    https://doi.org/10.1016/j.baae.2012.03.006
  • Ecological Entomology
    2012

    Intrinsic competition among solitary and gregarious endoparasitoid wasps and phenomenon of resource sharing

    P.M. Magdaraog, Jeff A. Harvey, T. Tanaka, R. Gols
    1. Intrinsic competition was compared in three species of braconid wasps, the solitary Meteorus pulchricornis Wesmael, and the gregarious Cotesia kariyai (Watanabe) and Cotesia ruficrus Haliday in caterpillars of their common host, the armyworm Mythimna separata Walker. Competition was determined in pair-wise contests consisting of simultaneous and subsequent parasitisms at various time intervals between the first and second attacks (
    https://doi.org/10.1111/j.1365-2311.2011.01338.x
  • PLoS Biology
    2012

    Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host

    Erik H. Poelman, M. Bruinsma, F. Zhu, B.T. Weldegergis, Y. Jongema, Joop J.A. van Loon, Louise E.M. Vet, Jeff A. Harvey, Marcel Dicke
    Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.
    https://doi.org/10.1371/journal.pbio.1001435
  • Journal of Insect Physiology
    2012

    The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid wasps

    Jeff A. Harvey, J. Cloutier, Bertanne Visser, J. Ellers, F.L. Wackers, R. Gols
    In nature adult insects, such as parasitic wasps or ‘parasitoids’ often depend on supplemental nutritional sources, such as sugars and other carbohydrates, to maximize their life-expectancy and reproductive potential. These food resources are commonly obtained from animal secretions or plant exudates, including honeydew, fruit juices and both floral and extra-floral nectar. In addition to exogenous sources of nutrition, adult parasitoids obtain endogenous sources from their hosts through ‘host-feeding’ behavior, whereby blood is imbibed from the host. Resources obtained from the host contain lipids, proteins and sugars that are assumed to enhance longevity and/or fecundity. Here we conducted an experiment exploring the effects of naturally occurring sugars on longevity and fecundity in the solitary hyperparasitoids, Lysibia nana and Gelis agilis. Although both species are closely related, L. nana does not host-feed whereas G. agilis does. In a separate experiment, we compared reproduction and longevity in G. agilis reared on either honey, a honey-sugar ‘mimic’, and glucose. Reproductive success and longevity in both hyperparasitoids varied significantly when fed on different sugars. However, only mannose- and water-fed wasps performed significantly more poorly than wasps fed on four other sugar types. G. agilis females fed honey produced twice as many progeny as those reared on the honey-sugar mimic or on glucose, whereas female longevity was only reduced on the mimic mixture. This result shows not only that host feeding influences reproductive success in G. agilis, but also that non-sugar constituents in honey do. The importance of non-sugar nutrients in honey on parasitoid reproduction is discussed.
    https://doi.org/10.1016/j.jinsphys.2012.03.002
  • Entomologia Experimentalis et Applicata
    2012

    Chemical and structural effects of invasive plants on herbivore-parasitoid/predator interactions in native communities

    Jeff A. Harvey, Taiadjana Fortuna
    The introduction and/or spread of exotic organisms into new habitats is considered a major threat to biodiversity. Invasive plants have been shown to negatively affect native communities, competing with and excluding other plants and disrupting a wide range of trophic interactions associated with them. In spite of this, thus far, few studies have explicitly studied the mechanisms underlying the displacement and potential local extinction of native herbivores and their natural enemies up to the third trophic level and even higher. Here, we formulate hypotheses on how structural and chemical characteristics of invasive plants may affect the plant-finding abilities of herbivores and the host- or prey-finding behavior of predators and parasitoids. The sudden incursion of an invasive plant into a native plant community may fragment native habitats and thus create structural barriers that impede dispersal and plant-finding ability for herbivores and prey- or host-finding ability for predators and parasitoids. At the same time, invasive plants may produce odors that are attractive to native insects and thus interfere with interactions on native plants. If invasive plants are both attractive and toxic to native insects, they may constitute ‘traps’ that are possibly beneficial against insect pests in agro-ecosystems, but have conservation implications for native herbivores and their natural enemies. However, we also suggest that some herbivores, and by association their parasitoids, may benefit from the establishment and spread of exotic plants because they increase the amount of available resources for them to exploit.
    https://doi.org/10.1111/j.1570-7458.2012.01252.x
  • Animal Behaviour
    2012

    Variation in the specificity of plant volatiles and their use by a specialist and a generalist parasitoid

    R. Gols, C. Veenemans, R.P.J. Potting, Hans M. Smid, Marcel Dicke, Jeff A. Harvey, Tibor Bukovinszky
    Herbivore-induced plant volatiles (HIPV) provide important information that influences host location behaviour for insect natural enemies, such as parasitoid wasps, that develop in the bodies of herbivorous insects. The dietary breadth of both the parasitoid and its host may affect the extent to which a searching parasitoid relies on HIPV. Specialist species are expected to rely on specific volatile cues to which they respond innately, whereas generalists are expected to show a higher degree of phenotypic plasticity that depends on foraging experience in the parasitoid. We compared the response to HIPV emitted by different plant species damaged by host and nonhost caterpillars for two congeneric parasitoid species, the specialist Diadegma semiclausum and the generalist Diadegma fenestrale, attacking caterpillars of the diamondback moth, Plutella xylostella. For the three tested plant species, Brassica oleracea, a feral Brassica population and Sinapis alba, both parasitoid species preferred volatiles from host-infested plants over those produced by undamaged plants. However, both parasitoid species only distinguished between volatiles induced by host and nonhosts when the caterpillars had been feeding on B. oleracea, the plant on which they had been reared. Chemical analysis of the volatile blends could not explain volatile preferences of the parasitoids. Despite the difference in their dietary breadth, the two parasitoids responded similarly to HIPV and experience treatments. A flexible response to a wide array of volatile blends by parasitoids is probably important in nature, given that different generations of the host and the parasitoid probably develop on different food plants.
    https://doi.org/10.1016/j.anbehav.2012.02.015
  • Biological Control
    2012

    Effects of an invasive plant on the performance of two parasitoids with different host exploitation strategies

    Taiadjana Fortuna, Louise E.M. Vet, Jeff A. Harvey
    In their new range, exotic plants create the possibility for novel interactions to occur with native consumers. Whereas there is evidence that these novel interactions can be negative for native insects, alien plants that are closely related to native species may in fact act as important food sources for native insects during the growing season. Thus far, studies with invasive plants have mostly focused on plant–herbivore interactions. However, to better understand how top-down and bottom-up processes may affect the success of potential invaders we also need to consider the effects of invasive plants on higher trophic levels. We examine multitrophic interactions on an exotic invasive crucifer, Bunias orientalis, and a native crucifer, Brassica nigra. The performance of a specialist herbivore, Pieris brassicae, and two of its gregarious endoparasitoids, the koinobiont Cotesia glomerata and the idiobiont Pteromalus puparum, was investigated. Emphasis was laid on parasitoid host-resource use strategies and how these may be differently affected by the quality of the exotic food plant. P. brassicae larvae performed poorly on the exotic plant, with lower survival, longer development time and a lower pupal mass, than on the native plant. The exotic plant affected the performance of the two parasitoid species in different ways. C. glomerata survival was strongly co-ordinated with the survival of its larval host, showing also high mortality. Adult wasps that survived on Bu. orientalis had an extended development time and small body size. By contrast, Pt. puparum survival was similar on pupal hosts reared on both plant species. Our results show that constraints imposed by differing plant quality of native and exotic plants on trophic interactions can depend on resource use strategies of the species involved, suggesting that effects of exotic species should be elucidated on a case-by-case basis.
    https://doi.org/10.1016/j.biocontrol.2012.05.003
  • Basic and Applied Ecology
    2012

    Contrasting patterns of herbivore and predator pressure on invasive and native plants

    Invasive non-nativeplant species often harbor fewer herbivorous insects than related nativeplant species. However, little is known about how herbivorous insects on non-nativeplants are exposed to carnivorous insects, and even less is known on plants that have recently expanded their ranges within continents due to climate warming. In this study we examine the herbivore load (herbivore biomass per plant biomass), predator load (predator biomass per plant biomass) and predatorpressure (predator biomass per herbivore biomass) on an inter-continental non-native and an intra-continental range-expanding plant species and two congeneric native species. All four plant species co-occur in riparian habitat in north-western Europe. Insects were collected in early, mid and late summer from three populations of all four species. Before counting and weighing the insects were classified to trophic guild as carnivores (predators), herbivores, and transients. Herbivores were further subdivided into leaf-miners, sap-feeders, chewers and gallers. Total herbivore loads were smaller on inter-continental non-native and intra-continental range-expanding plants than on the congeneric natives. However, the differences depended on time within growing season, as well as on the feeding guild of the herbivore. Although the predator load on non-nativeplants was not larger than on natives, both non-nativeplant species had greater predatorpressure on the herbivores than the natives. We conclude that both these non-nativeplant species have better bottom-up as well as top-down control of herbivores, but that effects depend on time within growing season and (for the herbivore load) on herbivore feeding guild. Therefore, when evaluating insects on non-nativeplants, variation within season and differences among feeding guilds need to be taken into account.
    https://doi.org/10.1016/j.baae.2012.10.005
  • Journal of Insect Physiology
    2012

    Development of a hyperparasitoid wasp in different stages of its primary parasitoid and secondary herbivore hosts

    Jeff A. Harvey, R. Gols, Louise E.M. Vet, Marjolein Kruidhof
    Parasitoid wasps are model organisms for exploring constraints on life history and development strategies in arthropods. Koinobiont parasitoids attack hosts that may vary considerably in size at parasitation. Thus far, studies exploring koinobiont development in hosts of different size have been exclusively done with primary parasitoids attacking insect herbivores. However, the larvae of primary koinobiont parasitoids may in turn be attacked by koinobiont hyperparasitoids. We examined development of the gregarious hyperparasitoid Baryscapus galactopus in different stages of its primary parasitoid host, Cotesia glomerata, itself developing in different stages of caterpillars of the cabbage butterfly, Pieris brassicae. This is the first study exploring hyperparasitoid development in different stages of a primary and secondary host. Second instar (L2) larvae of P. brassicae were parasitized by C. glomerata, and separate cohorts of L3 to L5 P. brassicae containing different stages of C. glomerata were then presented to B. galactopus females. B. galactopus was able to parasitize tiny larvae of C glomerata in L3 caterpillars of P. brassicae, but hyperparasitism efficiency increased in later instars of both C. glomerata and P. brassicae. Development time of B. galactopus was extended in younger C. glomerata/P. brassicae hosts, whereas adult mass was largest when C glomerata was attacked in L3 through early L5 P. brassicae. Our results show that B. galactopus adjusts its development rate in accordance with the size of both its primary and secondary hosts, in order to ensure survival. Adaptive responses to phylogenetic constraints on the development of primary hyperparasitoids are discussed
    https://doi.org/10.1016/j.jinsphys.2012.08.013
  • Journal of Evolutionary Biology
    2012

    The roles of ecological fitting, phylogeny and physiological equivalence in understanding realized and fundamental host ranges in endoparasitoid wasps

    Jeff A. Harvey, M.G. Ximenez de Embun, Tibor Bukovinszky, R. Gols
    Co-evolutionary theory underpins our understanding of interactions in nature involving plant–herbivore and host–parasite interactions. However, many studies that are published in the empirical literature that have explored life history and development strategies between endoparasitoid wasps and their hosts are based on species that have no evolutionary history with one another. Here, we investigated novel associations involving two closely related solitary endoparasitoids that originate from Europe and North America and several of their natural and factitious hosts from both continents. The natural hosts of both species are also closely related, all being members of the same family. We compared development and survival of both parasitoids on the four host species and predicted that parasitoid performance is better on their own natural hosts. In contrast with this expectation, survival, adult size and development time of both parasitoids were similar on all (with one exception) hosts, irrespective as to their geographic origin. Our results show that phylogenetic affinity among the natural and factitious hosts plays an important role in their nutritional suitability for related parasitoids. Evolved traits in parasitoids, such as immune suppression and development, thus enable them to successfully develop in novel host species with which they have no evolutionary history. Our results show that host suitability for specialized organisms like endoparasitoids is closely linked with phylogenetic history and macro-evolution as well as local adaptation and micro-evolution. We argue that the importance of novel interactions and ‘ecological fitting’ based on phylogeny is a greatly underappreciated concept in many resource–consumer studies.
    https://doi.org/10.1111/j.1420-9101.2012.02596.x
  • Journal of Chemical Ecology
    2012

    Root herbivore effects on aboveground multitrophic interactions: Patterns, processes and mechanisms

    In terrestrial food webs, the study of multitrophic interactions traditionally has focused on organisms that share a common domain, mainly above ground. In the last two decades, it has become clear that to further understand multitrophic interactions, the barrier between the belowground and aboveground domains has to be crossed. Belowground organisms that are intimately associated with the roots of terrestrial plants can influence the levels of primary and secondary chemistry and biomass of aboveground plant parts. These changes, in turn, influence the growth, development, and survival of aboveground insect herbivores. The discovery that soil organisms, which are usually out of sight and out of mind, can affect plant-herbivore interactions aboveground raised the question if and how higher trophic level organisms, such as carnivores, could be influenced. At present, the study of above-belowground interactions is evolving from interactions between organisms directly associated with the plant roots and shoots (e.g., root feeders - plant - foliar herbivores) to interactions involving members of higher trophic levels (e.g., parasitoids), as well as non-herbivorous organisms (e.g., decomposers, symbiotic plant mutualists, and pollinators). This multitrophic approach linking above- and belowground food webs aims at addressing interactions between plants, herbivores, and carnivores in a more realistic community setting. The ultimate goal is to understand the ecology and evolution of species in communities and, ultimately how community interactions contribute to the functioning of terrestrial ecosystems. Here, we summarize studies on the effects of root feeders on aboveground insect herbivores and parasitoids and discuss if there are common trends.We discuss the mechanisms that have been reported to mediate these effects, from changes in concentrations of plant nutritional quality and secondary chemistry to defense signaling. Finally, we discuss how the traditional framework of fixed paired combinations of root- and shoot-related organisms feeding on a common plant can be transformed into a more dynamic and realistic framework that incorporates community variation in species, densities, space and time, in order to gain further insight in this exciting and rapidly developing field.
    https://doi.org/10.1007/s10886-012-0104-z
  • Insect Science
    2012

    Effect of host-cocoon mass on adult size in the secondary hyperparasitoid wasp, Pteromalus semotus (Hymenoptera: Pteromalidae)

    Jeff A. Harvey, A. Gumovsky, R. Gols
    Parasitoids have long proven to be model organisms in studying resource-related constraints on immature development. Here we examine the relationship between host cocoon (= pupal) size in the gregarious endoparasitoid wasp, Cotesia glomerata, and development time and adult size in the solitary idiobiont hyperparasitoid, Pteromalus semotus. Little is known about the biology or ecology of this ecto-hyperparasitoid species, although it is one of the major secondary hyperparasitoids of C. glomerata. The size of the adult wasp covaried with the size of the host cocoon at parasitism. Moreover, female wasps were larger than male wasps for a given cocoon size. Adult wasps have remarkably long life-spans, 3 months on average. Longevity did not significantly differ with sex. We also examined how larvae of P. semotus exclude other potential competitors. P. semotus is protandrous, with females taking significantly longer to complete their development than males. In experiments where several eggs of P. semotus were placed on individual pupae of C. glomerata, newly hatched hyperparasitoid larvae moved rapidly over the surface of the host and destroyed the eggs of any conspecifics by biting them before they would initiate feeding on host tissues. Our results are discussed in relation to those with other studies with solitary ichneumonid idiobiont hyperparasitoids of C. glomerata.
    https://doi.org/10.1111/j.1744-7917.2011.01475.x
  • BioControl
    2012

    Root and shoot jasmonic acid induction differently affects the foraging behavior of Cotesia glomerata under semi-field conditions

    B.L. Qiu, Nicole M. van Dam, Jeff A. Harvey, Louise E.M. Vet
    Plants can accumulate and release defensive chemicals by activating various signaling pathways when they are damaged by herbivores or pathogens. The jasmonic acid pathway is activated after damage by chewing herbivores. Here we used jasmonic acid (JA) as an exogenous elicitor to induce feral cabbage plants. In this study, the effects of root JA (RJA) and shoot JA (SJA) induction on the foraging behavior of , a parasitoid of the large cabbage white butterfly , was investigated under semi-field conditions. In all combinations of differently induced plants (RJA, SJA and control plants), the percentages of shoot induced plants that were visited by at least one wasp were significantly higher than those of controls or root induced plants during 3 h of foraging. Consequently, parasitism rates of on shoot-JA induced plants were significantly higher than on plants induced with JA to the roots or control plants in all tests. However, this behavioral preference was not reflected in the allocation of offspring. The clutch sizes of eggs on control, root induced and shoot induced plants were not significantly different from each other in two-choice or three-choice experiments, but did differ with clutch size in the two-choice experiment of uninduced control plants versus SJA. This semi-field study helps to further understand the choice behavior and preferences of parasitoids in natural multitrophic communities in which plants induced with root or shoot herbivores occur together.
    https://doi.org/10.1007/s10526-011-9410-6
  • PLoS One
    2012

    Plant Volatiles Induced by Herbivore Egg Deposition Affect Insects of Different Trophic Levels

    N.E. Fatouros, D. Lucas-Barbosa, B.T. Weldegergis, F.G. Pashalidou, Joop J.A. van Loon, Marcel Dicke, Jeff A. Harvey, R. Gols, M.E. Huigen
    Plants release volatiles induced by herbivore feeding that may affect the diversity and composition of plant-associated arthropod communities. However, the specificity and role of plant volatiles induced during the early phase of attack, i.e. egg deposition by herbivorous insects, and their consequences on insects of different trophic levels remain poorly explored. In olfactometer and wind tunnel set-ups, we investigated behavioural responses of a specialist cabbage butterfly (Pieris brassicae) and two of its parasitic wasps (Trichogramma brassicae and Cotesia glomerata) to volatiles of a wild crucifer (Brassica nigra) induced by oviposition of the specialist butterfly and an additional generalist moth (Mamestra brassicae). Gravid butterflies were repelled by volatiles from plants induced by cabbage white butterfly eggs, probably as a means of avoiding competition, whereas both parasitic wasp species were attracted. In contrast, volatiles from plants induced by eggs of the generalist moth did neither repel nor attract any of the tested community members. Analysis of the plant’s volatile metabolomic profile by gas chromatography-mass spectrometry and the structure of the plant-egg interface by scanning electron microscopy confirmed that the plant responds differently to egg deposition by the two lepidopteran species. Our findings imply that prior to actual feeding damage, egg deposition can induce specific plant responses that significantly influence various members of higher trophic levels.
    https://doi.org/10.1371/journal.pone.0043607
  • Population Ecology
    2011

    Development of Mamestra brassicae and its solitary endoparasitoid Microplitis mediator on two populations of the invasive weed, Bunias orientalis

    Jeff A. Harvey, R. Gols
    The warty cabbage Bunias orientalis is an invasive pest in much of central Europe, including much of Germany since the 1980s, whereas in other countries, such as The Netherlands, it is a less common exotic species. Here, healthy larvae of Mamestra brassicae, which has been found feeding on B. orientalis plants in Germany, and larvae parasitized by one of its major larval endoparasitoids Microplitis mediator, were reared on both herbivoreinduced and noninduced leaves of B. orientalis originating from single large populations growing in The Netherlands and central Germany. Herbivore performance was less negatively affected than parasitoid performance by differences in plant quality. Development times in both M. brassicae and Mi. mediator were shorter on Dutch than German plants and also shorter on noninduced than induced plants. Moreover, survival and body size of the parasitoid was more strongly affected by plant population and induction than survival of healthy M. brassicae. Chemical analyses of defensive secondary metabolites [glucosinolates (GS)] revealed that concentrations of the major GS sinalbin were constitutively expressed in German plants whereas they were induced in Dutch plants. However, in separate feeding bioassays in which preference for induced and noninduced leaves was compared separately, L3 instars of M. brassicae preferred noninduced German plants over Dutch plants but induced Dutch plants over German plants, revealing that changes in primary metabolites or an unidentified non-GS compound mediates population- related differences in plant quality. The results reveal asymmetric effects of plant quality in exotic plants on organisms in the second and third trophic level.
    https://doi.org/10.1007/s10144-011-0267-4
  • Journal of Chemical Ecology
    2011

    Population-related variation in plant defense more strongly affects survival of an herbivore than its solitary parasitoid wasp

    Jeff A. Harvey, R. Gols
    The performance of natural enemies, such as parasitoid wasps, is affected by differences in the quality of the host’s diet, frequently mediated by species or population-related differences in plant allelochemistry. Here, we compared survival, development time, and body mass in a generalist herbivore, the cabbage moth, Mamestra brassicae, and its solitary endoparasitoid, Microplitis mediator, when reared on two cultivated (CYR and STH) and three wild (KIM, OH, and WIN) populations of cabbage, Brassica oleracea. Plants either were undamaged or induced by feeding of larvae of the cabbage butterfly, Pieris rapae. Development and biomass of M. brassicae and Mi. mediator were similar on both cultivated and one wild cabbage population (KIM), intermediate on the OH population, and significantly lower on the WIN population. Moreover, development was prolonged and biomass was reduced on herbivore-induced plants. However, only the survival of parasitized hosts (and not that of healthy larvae) was affected by induction. Analysis of glucosinolates in leaves of the cabbages revealed higher levels in the wild populations than cultivars, with the highest concentrations in WIN plants. Multivariate statistics revealed a negative correlation between insect performance and total levels of glucosinolates (GS) and levels of 3-butenyl GS. However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics. This result suggests that, in addition to aliphatic GS, other non- GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host. Remarkably, when developing on WIN plants, the survival of Mi. mediator to adult eclosion was much higher than in its host, M. brassicae. This may be due to the fact that hosts parasitized by Mi. mediator pass through fewer instars, and host growth is arrested when they are only a fraction of the size of healthy caterpillars. Certain aspects of the biology and life-history of the host and parasitoid may determine their response to chemical challenges imposed by the food plant.
    https://doi.org/10.1007/s10886-011-0024-3
  • Biological Journal of the Linnean Society
    2011

    The evolutionary improbability of ‘generalism’ in nature, with special reference to insects

    H. Loxdale, G. Lushai, Jeff A. Harvey
    Most organisms represent specialized forms that arose as a result of natural selection and genetic drift to occupy distinct ecological niches. In animals, this process of specialization includes the behaviour of the organisms concerned, honed by locally-induced adaptations to specific host food plants (in herbivores) or prey items (in predators and parasitoids), and possibly reinforced by kairomones, including sex pheromones. The major thrust of evolution is towards ecological specialization as a result of the direct effects of intra- and interspecific competition. Adaptation to new resources lowers such competition and allows survival in new habitats/niches. Other benefits of food resource/habitat switching include ‘enemy free space’. If specialism is the norm for the vast majority of species, what of so-called generalists and generalism, which are widely used terms, but perhaps wrongly so? Does generalism exist or is it a mirage that disappears the closer that it is inspected? We review some of the aspects of specialism and generalism and argue that even apparent generalists are filling distinct ecological niches. Often, generalists are rather specific in terms of food preferences, although they may nevertheless remain opportunistic with an overall broad niche/resource width. When apparent ‘good’ species are examined using molecular (DNA) markers, they are often found to comprise cryptic species. Many generalists may be of this kind. If so, generalism warrants additional investigation to establish its scope and credentials.
    https://doi.org/10.1111/j.1095-8312.2011.01627.x
  • Oikos
    2011

    Intrinsic competition between two secondary hyperparasitoids results in temporal trophic switch

    Jeff A. Harvey, F. Pashalidou, Roxina Soler , T. Martijn Bezemer
    Interspecific competition amongst parasitoids is important in shaping the evolution of life-history strategies in these insects as well as community structure. Competition for hosts may occur between adult female parasitoids (‘extrinsic’ competition) or their progeny (‘intrinsic’ competition). Here, we examined intrinsic competition between two solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis in cocoons of a primary parasitoid, Cotesia glomerata. Each species was allowed to sting hosts previously parasitized by the other at 24 h time intervals over the course of 144 h (6 days). When hosts were attacked simultaneously, neither species was dominant although the species to attack first won most encounters when it had a 24–48 h head start. However, after this time there was dramatic shift in the outcome with G. agilis dominating in all hosts > 72-h old, regardless of which species had parasitized C. glomerata first. G. agilis larvae, which initially had competed with L. nana for control of C. glomerata resources, began attacking the larvae of L. nana, whereas L. nana rejected hosts with older G. agilis larvae or pupae. Effects of multiparasitism also affected the development time and adult mass of the winning parasitoid. Our results reveal a shift in the trophic status of G. agilis from C. glomerata (in younger hosts) to L. nana (in older hosts), the first time such a phenomenon has been reported in parasitoids.
    https://doi.org/10.1111/j.1600-0706.2010.18744.x
  • Oecologia
    2011

    Tri-trophic effects of inter- and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea)

    Jeff A. Harvey, Nicole M. van Dam, C.E. Raiijmakers, J.M. Bullock, R. Gols
    The effect of direct chemical defences in plants on the performance of insect herbivores and their natural enemies has received increasing attention over the past 10 years. However, much less is known about the scale at which this variation is generated and maintained, both within and across populations of the same plant species. This study compares growth and development of the large cabbage butterfy, Pieris brassicae, and its gregarious pupal parasitoid, Pteromalus puparum, on three wild populations [Kimmeridge (KIM), Old Harry (OH) and Winspit (WIN)] and two cultivars [Stonehead (ST), and Cyrus (CYR)] of cabbage, Brassica oleracea. The wild populations originate from the coast of Dorset, UK, but grow in close proximity with one another. Insect performance and chemical profiles were made from every plant used in the experiment. Foliar glucosinolates (GS) concentrations were highest in the wild plants in rank order WIN > OH > KIM, with lower levels found in the cultivars. Caterpillar-damaged leaves in the wild cabbages also had higher GS levels than undamaged leaves. Pupal mass in P. brassicae varied signficantly among populations of B. oleracea. Moreover, development time in the host and parasitoid were correlated, even though these stages are temporally separated. Parasitoid adult dry mass closely approximated the development of its host. Multivariate statistics revealed a correlation between pupal mass and development time of P. brassicae and foliar GS chemistry, of which levels of neoglucobrassicin appeared to be the most important. Our results show that there is considerable variation in quantitative aspects of defensive chemistry in wild cabbage plants that is maintained at very small spatial scales in nature. Moreover, the performance of the herbivore and its parasitoid were both affected by differences in plant quality.
    https://doi.org/10.1007/s00442-010-1861-4
  • Journal of Chemical Ecology
    2011

    Smelling the wood from the trees: Non-linear parasitoid responses to volatile attractants produced by wild and cultivated cabbage

    R. Gols, J.M. Bullock, Marcel Dicke, Tibor Bukovinszky, Jeff A. Harvey
    Despite a large number of studies on herbivore-induced plant volatiles (HIPVs), little is known about which specific compounds are used by natural enemies to locate prey- or host- infested plants. In addition, the role of HIPVs in attracting natural enemies has been restricted largely to agricultural systems. Differences in volatile blends emitted by cultivars and plants that originate from wild populations may be attributed to potentially contrasting selection regimes: natural selection among the wild types and artificial selection among cultivars. A more realistic understanding of these interactions in a broader ecological and evolutionary framework should include studies that involve insect herbivores, parasitoids, and wild plants on which they naturally interact in the field. We compared the attractiveness of HIPVs emitted by wild and cultivated cabbage to the parasitoid Cotesia rubecula, and determined the chemical composition of the HIPV blends to elucidate which compounds are involved in parasitoid attraction. Wild and cultivated cabbage differed significantly in their volatile emissions. Cotesia rubecula was differentially attracted to the wild cabbage populations and preferred wild over cultivated cabbage. Isothiocyanates, which were only emitted by the wild cabbages, may be the key components that explain the preference for wild over cultivated cabbage, whereas terpenes may be important for the differential attraction among the wild populations. Volatile analysis revealed that parasitoid attraction cannot be explained by simple linear relationships. Our results suggest that unraveling which compound(s) are innately attractive to parasitoids of cabbage pests should include wild Brassicaceae.
    https://doi.org/10.1007/s10886-011-9993-5
  • Annals of the Entomological Society of America
    2011

    Differing success of defense strategies in two parasitoid wasps in protecting their pupae against a secondary hyperparasitoid

    Jeff A. Harvey, R. Gols, T. Tanaka
    During their larval development, endoparasitoids are known to dispose of host resources in several different ways. Some parasitoid wasps consume most or all tissues of the host, whereas others consume a small fraction of host resources and either ensure that the host moves away from the pupation site or allow the host to remain close to the parasitoid cocoon(s). Using a single host species, Mythimna separata Walker (Lepidoptera: Noctuidae), this study compares the success of the two pupation strategies in the solitary parasitoids Microplitis sp. and Meteorus pulchricornis Wesmael (Hymenoptera: Braconidae) against attack from a secondary hyperparasitoid, Gelis agilis F. (Hymenoptera: Ichneumonidae). The caudal appendages of M. separata caterpillars parasitized by Microplitis sp. remain physically attached to parasitoid cocoons and the caterpillars behave aggressively when disturbed. However, after Me. pulchricornis larvae emerge from caterpillars of their host, M. separata, the parasitoid larvae pupate in cocoons that are suspended by a single thick thread that hangs 1-2 cm from under a leaf. In choice tests conducted in petri dishes, significantly fewer cocoons of Microplitis sp. attended by caterpillars than unattended cocoons were hyperparasitized by G. agilis. By contrast, Me. pulchricornis cocoons that were hanging from corn, Zea mays L., plants were hyperparasitized as frequently as those which were attached to leaves. We discuss the potentially different selection pressures generated among natural enemies such as predators and hyperparasitoids in determining optimal pupal defense strategies in primary parasitoids.
    https://doi.org/10.1603/AN10192
  • Journal of Chemical Ecology
    2011

    Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata

    J.H. Reudler Talsma, Arjen Biere, Jeff A. Harvey, S. van Nouhuys
    The ability to cope with plant defense chemicals differs between specialist and generalist species. In this study, we examined the effects of the concentration of the two main iridoid glycosides (IGs) in Plantago lanceolata, aucubin and catalpol, on the performance of a specialist and two generalist herbivores and their respective endoparasitoids. Development of the specialist herbivore Melitaea cinxia was unaffected by the total leaf IG concentration in its host plant. By contrast, the generalist herbivores Spodoptera exigua and Chrysodeixis chalcites showed delayed larval and pupal development on plant genotypes with high leaf IG concentrations, respectively. This result is in line with the idea that specialist herbivores are better adapted to allelochemicals in host plants on which they are specialized. Melitaea cinxia experienced less post-diapause larval and pupal mortality on its local Finnish P. lanceolata than on Dutch genotypes. This could not be explained by differences in IG profiles, suggesting that M. cinxia has adapted in response to attributes of its local host plants other than to IG chemistry. Development of the specialist parasitoid Cotesia melitaearum was unaffected by IG variation in the diet of its host M. cinxia, a response that was concordant with that of its host. By contrast, the development time responses of the generalist parasitoids Hyposoter didymator and Cotesia marginiventris differed from those of their generalist hosts, S. exigua and C. chalcites. While their hosts developed slowly on high-IG genotypes, development time of H. didymator was unaffected. Cotesia marginiventris actually developed faster on hosts fed high-IG genotypes, although they then had short adult longevity. The faster development of C. marginiventris on hosts that ate high-IG genotypes is in line with the “immunocompromized host” hypothesis, emphasizing the potential negative effects of toxic allelochemicals on the host’s immune response.
    https://doi.org/10.1007/s10886-011-9983-7
  • Journal of Insect Behavior
    2011

    Differing host exploitation efficiencies in two hyperparasitoids: when is a 'match made in heaven'?

    Jeff A. Harvey, Roel Wagenaar, R. Gols
    Host exploitation behavior in two hyperparasitoids, Lysibia nana and Gelis agilis, was compared in single cocoon clusters of their primary parasitoid host, Cotesia glomerata. L. nana reproduces sexually, is fully winged, does not host-feed and matures eggs quite rapidly after eclosion, whereas G. agilis possesses opposite traits. Cohorts of individual hyperparasitoid females of differing age and physiological state were given access to single cocoon clusters of C. glomerata that also varied in age. These results reveal that the reproductive biology of L. nana is well matched to exploit cocoon broods in C. glomerata, suggesting strong a co-evolutionary history with this host. By contrast, G. agilis is much less efficient at exploiting host cocoons and is probably a generalist species that attacks other hosts in nature.
    https://doi.org/10.1007/s10905-010-9254-4
  • Biological Control
    2010

    Development and host utilization in Hyposoter ebeninus (Hymenoptera: Ichneumonidae), a solitary endoparasitoid of Pieris rapae and P. brassicae caterpillars (Lepidoptera: Pieridae)

    Jeff A. Harvey, Erik H. Poelman, R. Gols
    In many parts of the world, the larvae of the cabbage white butterflies, Pieris rapae and P. brassicae, are considered to be major pests in several economically important brassicaceous crops including various cultivars of cabbage and mustard. Thus far, biological control of these pests has focused on parasitoids including species in the genus Cotesia. We examined interactions between the solitary ichneumonid parasitoid, Hyposoter ebeninus, developing in 1st to 3rd (L1–L3) larval instars of both P. rapae and P. brassicae. H. ebeninus is common in central and southern Europe, but has thus far received little attention as a possible biological control agent of cabbage butterflies. Larvae of both pierids continued to grow after they were parasitized, and development was only arrested some 5–7 days later. Caterpillars parasitized in the third instar grew significantly larger than larvae parasitized as L1 or L2. Adult parasitoid body mass was inversely correlated with host instar parasitized, and female wasps were significantly larger than male wasps. Egg-to-adult development time in H. ebeninus did not vary between the two hosts, but the parasitoid exhibited protandry. Parasitoid survival was generally higher in larvae of P. rapae than in larvae of P. brassicae, but varied with instar in the two hosts. Our study shows that H. ebeninus has promise as a biological control agent, particularly against its more suitable host, P. rapae.
    https://doi.org/10.1016/j.biocontrol.2010.02.004
  • Biological Conservation
    2010

    Interactions between invasive plants and insect herbivores: A plea for a multitrophic perspective

    Invasive species represent one of the most important threats to biodiversity worldwide, with consequences for ecosystem functioning and the delivery of important ecological services to society. Several hypotheses have been generated to explain the success of exotic plants in their new ranges, with escape from their old natural enemies, such as pathogens and herbivores (the ‘enemy release hypothesis’) and novel defensive chemistry (the ‘novel weapons hypothesis’) receiving considerable attention. Thus far, virtually all studies of exotic plants and insects have been conducted in a strictly bi-trophic framework involving plants and herbivores. On the other hand, it has been argued that a better understanding of the forces regulating community structure and function should include natural enemies of the herbivores. Furthermore, indirect interactions between organisms in the plant roots (below-ground) and shoots (above-ground) are known to strongly effect the behaviour and performance of consumers in the opposite ‘compartment’. Here, we discuss a range of physiological, evolutionary and ecological aspects of plant–herbivore-natural enemy interactions involving exotic plants. Further, interactions between soil and above-ground organisms are explored with respect to studies with exotic plants. We argue that it is important to link population and community ecology to individual-level variation in the physiology and behaviour of insects across several trophic levels in studies with invasive plants. Future research with invaders should also aim to integrate physically separated compartments (e.g. plant roots and shoots). This will facilitate a more complete understanding of the factors underlying the success (or failure) of exotic plants to spread and become dominant in their new ranges. Moreover, these data will also help to unravel the relative importance of top-down and bottom-up processes in regulating communities in which exotic plants have become established. Lastly, we discuss consequences for conservation.
    https://doi.org/10.1016/j.biocon.2010.03.004
  • Biological Invasions
    2010

    Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis

    Jeff A. Harvey, Arjen Biere, Taiadjana Fortuna, Louise E.M. Vet, T. Engelkes, Elly Morrien, R. Gols, Koen Verhoeven, H. Vogel, Mirka Macel, H. Heidel-Fischer, K. Schramm, Wim H. van der Putten
    Exotic plants bring with them traits that evolved elsewhere into their new ranges. These traits may make them unattractive or even toxic to native herbivores, or vice versa. Here, interactions between two species of specialist (Pieris rapae and P. brassicae) and two species of generalist (Spodoptera exigua and Mamestra brassicae) insect herbivores were examined on two native crucifer species in the Netherlands, Brassica nigra and Sinapis arvensis, and an exotic, Bunias orientalis. Bu. orientalis originates in eastern Europe and western Asia but is now an invasive pest in many countries in central Europe. P. rapae, P. brassicae and S. exigua performed very poorly on Bu. orientalis, with close to 100% of larvae failing to pupate, whereas survival was much higher on the native plants. In choice experiments, the pierid butterflies preferred to oviposit on the native plants. Alternatively, M. brassicae developed very poorly on the native plants but thrived on Bu. orientalis. Further assays with a German Bu. orientalis population also showed that several specialist and generalist herbivores performed very poorly on this plant, with the exception of Spodoptera littoralis and M. brassicae. Bu. orientalis produced higher levels of secondary plant compounds (glucosinolates) than B. nigra but not S. arvensis but these do not appear to be important factors for herbivore development. Our results suggest that Bu. orientalis is a potential demographic ‘trap’ for some herbivores, such as pierid butterflies. However, through the effects of an evolutionary ‘lottery’, M. brassicae has found its way through the plant’s chemical ‘minefield’.
    https://doi.org/10.1007/s10530-010-9696-9
  • Ecology
    2010

    Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects

    T. Martijn Bezemer, M.T. Fountain, J.M. Barea, S. Christensen, S.C. Dekker, Henk Duyts, R. van Hal, Jeff A. Harvey, K. Hedlund, M. Maraun, J. Mikola, A.G. Mladenov, Catherine Robin, P.C. de Ruiter, S. Scheu, H. Setälä, P. Milauer, Wim H. van der Putten
    Soils are extremely rich in biodiversity, and soil organisms play pivotal roles in supporting terrestrial life, but the role that individual plants and plant communities play in influencing the diversity and functioning of soil food webs remains highly debated. Plants, as primary producers and providers of resources to the soil food web, are of vital importance for the composition, structure, and functioning of soil communities. However, whether natural soil food webs that are completely open to immigration and emigration differ underneath individual plants remains unknown. In a biodiversity restoration experiment we first compared the soil nematode communities of 228 individual plants belonging to eight herbaceous species. We included grass, leguminous, and non-leguminous species. Each individual plant grew intermingled with other species, but all plant species had a different nematode community. Moreover, nematode communities were more similar when plant individuals were growing in the same as compared to different plant communities, and these effects were most apparent for the groups of bacterivorous, carnivorous, and omnivorous nematodes. Subsequently, we analyzed the composition, structure, and functioning of the complete soil food webs of 58 individual plants, belonging to two of the plant species, Lotus corniculatus (Fabaceae) and Plantago lanceolata (Plantaginaceae). We isolated and identified more than 150 taxa/groups of soil organisms. The soil community composition and structure of the entire food webs were influenced both by the species identity of the plant individual and the surrounding plant community. Unexpectedly, plant identity had the strongest effects on decomposing soil organisms, widely believed to be generalist feeders. In contrast, quantitative food web modeling showed that the composition of the plant community influenced nitrogen mineralization under individual plants, but that plant species identity did not affect nitrogen or carbon mineralization or food web stability. Hence, the composition and structure of entire soil food webs vary at the scale of individual plants and are strongly influenced by the species identity of the plant. However, the ecosystem functions these food webs provide are determined by the identity of the entire plant community.
    https://doi.org/10.1890/09-2198.1
  • Basic and Applied Ecology
    2010

    Combined effects of patch size and plant nutritional quality on local densities of insect herbivores

    Tibor Bukovinszky, R. Gols, A.F.D. Kamp, F. De Oliveira-Domingues, P.A. Hambäck, Y. Jongema, T. Martijn Bezemer, Marcel Dicke, Nicole M. van Dam, Jeff A. Harvey
    Plant–insect interactions occur in spatially heterogeneous habitats. Understanding how such interactions shape density distributions of herbivores requires knowledge on how variation in plant traits (e.g. nutritional quality) affects herbivore abundance through, for example, affecting movement rates and aggregation behaviour. We studied the effects of plant patch size and herbivore-induced differences in plant nutritional quality on local densities of insect herbivores for two Brassica oleracea cultivars, i.e. white cabbage and Brussels sprouts. Early season herbivory as a treatment resulted in measurable differences in glucosinolate concentrations in both cultivars throughout the season. Herbivore induction and patch size both influenced community composition of herbivores in both cultivars, but the effects differed between species. Flea beetles (Phyllotreta spp.) were more abundant in large than in small patches, and this patch response was more pronounced on white cabbage than on Brussels sprouts. Herbivore-induction increased densities in all patches. Thrips tabaci was also more abundant in large patches and densities of this species were higher on Brussels sprouts than on white cabbage. Thrips densities were lower on induced than on control plants of both cultivars and this negative effect of induction tended to be more pronounced in large than in small patches. Densities of the cabbage moth (Mamestra brassicae) were lower on Brussels sprouts than on white cabbage and lower on herbivore-induced than on uninduced plants, with no effect of patch size. No clear effects of patch size and induction were found for aphids. This study shows that constitutive and herbivore-induced differences in plant traits interact with patch responses of insect herbivores.
    https://doi.org/10.1016/j.baae.2010.04.005
  • Proceedings of the National Academy of Sciences of the United States of America
    2010

    Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle

    Bertanne Visser, C. Le Lann, F.J. den Blanken, Jeff A. Harvey, J.J.M. van Alphen, J. Ellers
    Evolutionary loss of traits can result from negative selection on a specific phenotype, or if the trait is selectively neutral, because the phenotype associated with the trait has become redundant. Even essential traits may be lost, however, if the resulting phenotypic deficiencies can be compensated for by the environment or a symbiotic partner. Here we demonstrate that loss of an essential me-tabolic trait in parasitic wasps has evolved through environmental compensation. We tested 24 species for the ability to synthesize lipids de novo and collected additional data from the literature. We found the majority of adult parasitoid species to be incapable of synthesizing lipids, and phylogenetic analyses showed that the evolution of lack of lipogenesis is concurrent with that of parasitism in insects. Exploitive host manipulation, in which the host is forced to synthesize lipids to the benefit of the parasitoid, presumably facilitates loss of lipogenesis through environmental compensation. Lipogenesis re-evolved in a small number of parasitoid species, particularly host generalists. The wide range of host species in which generalists are able to develop may impede effective host manipulation and could have resulted in regaining of lipogenic ability in generalist parasitoids. As trait loss through environmental compensation is unnoticed at the phenotypic level, it may be more common than currently anticipated, especially in species involved in intricate symbiotic relationships with other species.
    https://doi.org/10.1073/pnas.1001744107
  • Neotropical Entomology
    2010

    Presence of the fire ant Solenopsis invicta (Westwood) (Hymenoptera: Formicidae) stimulates burrowiong behavior by larvae of the sandfly Lutzomyia longipalpis (Lutz &amp; Neiva)(Diptera: Psychodidae)

    Jeff A. Harvey, J.G.C. Hamilton, R.D. Ward
    The sandfly Lutzomyia longipalpis (Lutz & Neiva) vectors leishmaniasis in the neotropics. Although much is known about the biology of adult flies, little is known about interactions with its natural enemies. Here, we examined behavior of larvae of L4 L.longipalpis on a soil substrate when exposed to the fire ant Solenopsis invicata (Westwood). When ants were absent, most larvae tended to remain at or close to the soil surface, but when ants were present the larvae burrowed into the soil. Sandflies seek refuges in the presence of generalist predators, thus rendering them immune to attack from many potential enemies.
    https://doi.org/10.1590/S1519-566X2010000100020
  • Ecological Entomology
    2010

    Behaviour of male and female parasitoids in the field: influence of patch size, host density and habitat complexity

    T. Martijn Bezemer, Jeff A. Harvey, A.F.D. Kamp, Roel Wagenaar, R. Gols, Olga Kostenko, Taiadjana Fortuna, T. Engelkes, Louise E.M. Vet, Wim H. van der Putten, Roxina Soler
    1. Two field experiments were carried out to examine the role of patch size, host density, and complexity of the surrounding habitat, on the foraging behaviour of the parasitoid wasp Cotesia glomerata in the field. 2. First, released parasitoids were recaptured on patches of one or four Brassica nigra plants, each containing 10 hosts that were placed in a mown grassland area. Recaptures of females were higher than males, and males and females aggregated at patches with four plants. 3. In experiment 2, plants containing 0, 5 or 10 hosts were placed in unmown grassland plots that differed in plant species composition, on bare soil, and on mown grassland. Very low numbers of parasitoids were recaptured in the vegetated plots, while high numbers of parasitoids were recaptured on plants placed on bare soil or in mown grassland. Recaptures were higher on plants on bare soil than on mown grassland, and highest on plants containing 10 hosts. The host density effect was significantly more apparent in mown grassland than on bare soil. 4. Cotesia glomerata responds in an aggregative way to host density in the field. However, host location success is determined mostly by habitat characteristics, and stronger host or host-plant cues are required when habitat complexity increases.
    https://doi.org/10.1111/j.1365-2311.2010.01184.x
  • Entomologia Experimentalis et Applicata
    2010

    Impacts of belowground herbivory on oviposition decisions in two congeneric butterfly species

    Roxina Soler , Jeff A. Harvey, R. Rouchet, Sonja Schaper, T. Martijn Bezemer
    Root-feeding insects can affect the performance of aboveground insect herbivores when they are forced to feed on the same host plant. Here we explored whether the oviposition behaviour of two closely related herbivorous species (cabbage butterflies; Lepidoptera: Pieridae) is influenced by root-feeding insects, when they are given the chance to choose between host plants with and without root herbivores. Considering that egg load is an important physiological factor influencing the foraging behaviour of insects, we also examined whether root-feeding insects differentially influence oviposition preference in butterflies with low and high egg loads. Oviposition preference in both butterfly species with low and high egg loads was monitored using host plants with and without root herbivores. To ascertain the status of butterfly age with low and high egg loads, the oviducts of a separate group of butterflies was dissected to record the number of immature and mature eggs in butterflies of various ages. Pieris brassicae L. butterflies with low egg loads preferred plants without root herbivores over plants with root herbivores, and laid more egg clutches on the leaves of plants that were not attacked by root herbivores. Butterflies with comparatively high egg loads also selected a larger proportion of plants without root herbivores, but laid a similar number of egg clutches on the plant shoots independent of the presence or absence of root herbivores belowground. Independent of the age and egg load, Pieris rapae L. butterflies selected a larger proportion of plants not attacked by root herbivores to lay eggs, but the number of eggs laid was similar in plants with and without root herbivores. This study shows that belowground insects can influence behavioural decisions of aboveground insect herbivores. Interestingly, the strength of these interactions depends on the physiological state of the insects which is probably correlated with their perception of environmental quality.
    https://doi.org/10.1111/j.1570-7458.2010.01015.x
  • Annals of the Entomological Society of America
    2009

    Intraspecific competition between adult females of the hyperparasitoid Trichomalopsis apanteloctena (Hymenoptera: Chelonidae), for domination of Cotesia kariyai (Hymenoptera: Braconidae) cocoons

    Y. Nakamatsu, Jeff A. Harvey, T. Tanaka
    The development of parasitoid wasps is dependent on the finite resources contained in a single item of resource (=host) that is frequently not much larger than the adult parasitoid. When the costs of egg production are high, and host distribution is highly aggregated, parasitoid females may spend prolonged periods guarding their eggs and host resources as an adaptive strategy to optimize their inclusive fitness. Here, we examine aggressive interactions between the females of the secondary hyperparasitoid Trichomalopsis apanteloctena (Crawford) (Hymenoptera: Chelonidae), for control of cocoon clusters of their primary parasitoid host Cotesia kariyai (Watanabe) (Hymenoptera: Braconidae). Generally, larger female hyperparasitoids were more successful at defending cocoon clusters than smaller female hyperparasitoids. However, when first encountering host cocoons, larger females behaved more aggressively toward conspecific wasps than smaller females. After occupation of a host co! coon cluster, females of similar size rarely engaged in physical combat, but both females primarily exhibited threatening behavior toward each other. However, larger females usually displaced smaller females which had initially occupied cocoon clusters. Some small females chewed through the outer cocoon silk layer to avoid being displaced by larger females and these wasps were able to continue parasitizing cocoons of C. kariyai. Extended bouts of aggression tended to reduce the number of eggs laid by the guarding female because of disruption of oviposition behavior. The relationship between the size of host cocoons and body mass in T. apanteloctena was also examined. The size of hyperparasitoid progeny was strongly correlated with host size. However, the relationship between maternal size, the number of matured eggs in her ovarioles and body mass in her offspring was not significant.
    https://doi.org/10.1603/008.102.0120
  • Journal of Animal Ecology
    2009

    Interactions to the fifth trophic level: secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources

    1. Parasitoid wasps are highly efficient organisms at utilizing and assimilating limited resources from their hosts. This study explores interactions over three trophic levels, from the third (primary parasitoid) to the fourth (secondary parasitoid) and terminating in the fifth (tertiary parasitoid). 2. Host utilization and adult body mass of the secondary and tertiary parasitoid Gelis agilis was determined when developing on pre-pupae of its primary parasitoid host, Cotesia glomerata, and from pre-pupae of another secondary parasitoid, Lysibia nana that had developed initially on pre-pupae of C. glomerata. 3. In both C. glomerata and G. agilis, the body mass of emerging adult parasitoids was strongly positively correlated with initial cocoon mass. For a given cocoon mass at parasitism, emerging adult G. agilis wasps were almost 90% as large as C. glomerata adults developing in healthy cocoons of comparable mass. Furthermore, G. agilis adults were still 75% as large as C. glomerata adults even when developing on L. nana that in turn had developed on C. glomerata. Otherwise, in terms of adult body mass 4. Analyses of carbon and nitrogen in body tissues of the parasitoids over the third to the fifth trophic level revealed that percentage nitrogen was higher and carbon lower in G. agilis and L. nana than in C. glomerata. Furthermore, percentage carbon was lower in adult G. agilis wasps that had developed from L. nana than from C. glomerata. 5. We argue that the remarkable efficiency which characterizes the development of secondary and tertiary parasitoids is based on the very high nutritional quality of resources that increase in quality up the food chain and rigid selection optimizing allocation of limited host resources. Consequently, food webs involving secondary and tertiary parasitoids can go to levels hitherto unexplored thus far in empirical studies. The use of molecular markers in future studies may reveal just how long food c
    https://doi.org/10.1111/j.1365-2656.2008.01516.x
  • Annales Zoologici Fennici
    2009

    Preparing a paper for publication: an action plan for rapid composition and completion

    An important challenge for scientists, especially those early in their careers, is preparing an effective article for submission to a peer-reviewed journal. Here, I present a number of suggestions on how it could be accomplished. This action plan addresses (1) how to approach a topic by developing a story line connected with what is already known in the field, (2) how to most efficiently organize and sequence one's efforts by starting with the descriptive parts of the manuscript and subsequently moving to the more interpretive parts, and (3) the advantages of using bibliographic software to facilitate quick and accurate referencing. I suggest that authors should aim to produce a story that does not overcomplicate the topic under investigation while at the same time presenting a full and accurate coverage and interpretation of the data. Importantly, the preparation of manuscripts becomes easier with time and practice, as individuals hone their own style and approach to this task.
    https://doi.org/10.5735/086.046.0207
  • Functional Ecology
    2009

    Nonlinear effects of plant root and shoot jasmonic acid application on the performance of Pieris brassicae and its parasitoid Cotesia glomerata

    B. Qiu, Jeff A. Harvey, Ciska Raaijmakers, Louise E.M. Vet, Nicole M. van Dam
    1. Plant species employ several direct and indirect defence strategies to protect themselves against insect herbivores. Most studies, however, have focused on shoot-induced responses. Much less is known about interactions between below- and above-ground herbivores and how these may affect their respective parasitoids. 2. Here, we quantify the impact of below-ground induced responses vs. that of above-ground induced responses in a feral Brassica on the performance of Pieris brassicae and its endoparasitoid Cotesia glomerata. Jasmonic acid (JA) was applied to induce the plants above- or below-ground. The glucosinolate, sugar and amino acid levels of the leaves were analysed. 3. Pieris brassicae larvae grew significantly slower on shoot JA-induced (SJA) plants than on root JA-induced (RJA) and control plants, which were treated with acidic water. On RJA and control plants they showed similar developmental trajectories. Pupal masses, survival till eclosion and egg load, however, were similar on all plants. 4. The development of C. glomerata larvae on SJA plants was significantly longer than that on RJA and control plants. In contrast, the parasitoid's pupal stage lasted longer in hosts feeding on control plants. The total developmental times eventually were similar in all groups. However, the masses of male and female C. glomerata adults that developed hosts on control and RJA plants were significantly larger than those from hosts on SJA plants. JA application increased total glucosinolate conten 5. These results show that the differential effects of above- and below-ground-induced responses on herbivores also affect higher trophic levels in a nonlinear fashion via differential changes in host plant quality. In particular, the indirect effects that below-ground herbivores have on the performance of above-ground parasitoids may exceed the direct effects of plant chemistry on herbivore performance. Consequently, above-ground and below-ground interactions mediated by induced plant response
    https://doi.org/10.1111/j.1365-2435.2008.01516.x
  • Ecology Letters
    2009

    Plant invaders and their novel natural enemies: who is naive?

    Introduced exotic species encounter a wide range of non-coevolved enemies and competitors in their new range. Evolutionary novelty is a key aspect of these interactions, but who benefits from novelty: the exotic species or their new antagonists? Paradoxically, the novelty argument has been used to explain both the release from and the suppression by natural enemies. We argue that this paradox can be solved by considering underlying interaction mechanisms. Using plant defenses as a model, we argue that mismatches between plant and enemy interaction traits can enhance plant invasiveness in the case of toxin-based defenses, whereas invasiveness is counteracted by mismatches in recognition-based defenses and selective foraging of generalist herbivores on plants with rare toxins. We propose that a mechanistic understanding of ecological mismatches can help to explain and predict when evolutionary novelty will enhance or suppress exotic plant invasiveness. This knowledge may also enhance our understanding of plant abundance following range expansion, or during species replacements along successional stages.
    https://doi.org/10.1111/j.1461-0248.2008.01248.x
  • Entomologia Experimentalis et Applicata
    2009

    Intrinsic competition and its effects on the survival and development of three species of endoparasitoid wasps

    Jeff A. Harvey, R. Gols, M.R. Strand
    In natural systems, pre-adult stages of some insect herbivores are known to be attacked by several species of parasitoids. Under certain conditions, hosts may be simultaneously parasitized by more than one parasitoid species (= multiparasitism), even though only one parasitoid species can successfully develop in an individual host. Here, we compared development, survival, and intrinsic competitive interactions among three species of solitary larval endoparasitoids, Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae), Microplitis demolitor Wilkinson, and Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), in singly parasitized and multiparasitized hosts. The three species differed in certain traits, such as in host usage strategies and adult body size. Campoletis sonorensis and M. demolitor survived equally well to eclosion in two host species that differed profoundly in size, Pseudoplusia includens (Walker) and the larger Heliothis virescens (Fabricius) (both Lepidoptera: Noctuidae). Egg-to-adult development time in C. sonorensis and M. demolitor also differed in the two hosts. Moreover, adult body mass in C. sonorensis (and not M. demolitor) was greater when developing in H. virescens larvae. We then monitored the outcome of competitive interactions in host larvae that were parasitized by one parasitoid species and subsequently multiparasitized by another species at various time intervals (0, 6, 24, and 48 h) after the initial parasitism. These experiments revealed that M. croceipes was generally a superior competitor to the other two species, whereas M. demolitor was the poorest competitor, with C. sonorensis being intermediate in this capacity. However, competition sometimes incurred fitness costs in M. croceipes and C. sonorensis, with longer development time and/or smaller adult mass observed in surviving wasps emerging from multiparasitized hosts. Our results suggest that rapid growth and large size relative to competitors of a similar age may be beneficial in aggressive intrinsic competition.
    https://doi.org/10.1111/j.1570-7458.2008.00816.x
  • Entomologia Experimentalis et Applicata
    2009

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

    Thus far, few studies have compared life-history traits amongst secondary parasitoids attacking and developing in cocoons of their primary parasitoid hosts. This study examines development and reproduction in Lysibia nana Gravenhorst and Acrolyta nens Hartig (both Hymenoptera: Ichneumonidae), two related and morphologically similar secondary parasitoids that attack pupae of the gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae). On black mustard, Brassica nigra L. (Brassicaceae) plants in a field plot, adults of L. nana and A. nens frequently emerged from the same cocoon broods of C. glomerata. Based on similarities in their phylogeny and morphology, it was hypothesized that both species would exhibit considerable overlap in other life-history traits. In both L. nana and A. nens, adult wasp size increased with host cocoon mass at parasitism, although L. nana wasps were slightly larger than A. nens wasps, and completed their development earlier. Adult females of both species emerged with no eggs but matured eggs at similar rates over the following days. When provided with 20 host cocoons daily, fecundity in female L. nana was slightly more skewed towards early life than in A. nens, although lifetime fecundity did not differ between the two species. Longevity was significantly reduced in females of both species that were provided with hosts. Both parasitoids were found to exhibit strong similarities in life-history and development traits and in their ecological niche, thereby supporting our general hypothesis. Competition between L. nana and A. nens is presumably diffused because their preferred host (C. glomerata) is relatively abundant in open habitats.
    https://doi.org/10.1111/j.1570-7458.2009.00882.x
  • Oecologia
    2009

    Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism

    Tibor Bukovinszky, Erik H. Poelman, R. Gols, G. Prekatsakis, Louise E.M. Vet, Jeff A. Harvey, Marcel Dicke
    The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the field of ecology of multitrophic interactions. Scarcely studied aspects include the effects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the effects of constitutive and herbivore-induced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as first instars were low and did not differ among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed differences in encapsulation rates between plant populations could not be explained exclusively by differences in host growth on the different Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the first study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, affecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of fitness costs and benefits of herbivore diet on the third trophic level.
    https://doi.org/10.1007/s00442-009-1308-y
  • Ecological Entomology
    2009

    The effect of host developmental stage at parasitism on sex-related size differentiation in a larval endoparasitoid

    R. Gols, Jeff A. Harvey
    1. For their larval development, parasitoids depend on the quality and quantity of resources provided by a single host. Therefore, a close relationship is predicted between the size of the host at parasitism and the size of the emerging adult wasp. This relationship is less clear for koinobiont than for idiobiont parasitoids. 2. As size differentiation in host species exhibiting sexual size dimorphism (SSD) is likely to occur already during larval development, in koinobiont larval endoparasitoids the size of the emerging adult may also be constrained based on the sex of the host caterpillar. 3. Sex-specific growth trajectories were compared in unparasitised Plutella xylostella caterpillars and in second and fourth instar hosts that were parasitised by the solitary larval koinobiont endoparasitoid Diadegma semiclausum. Both species exhibit SSD, where females are significantly larger than males. 4. Healthy female P. xylostella caterpillars developed significantly faster than their male conspecifics. Host regulation induced by D. semiclausum parasitism depended on the instar attacked. Parasitism in second-instar caterpillars reduced growth compared to healthy unparasitised caterpillars, whereas parasitism in fourth-instar caterpillars arrested development. The reduction in growth was most pronounced in hosts producing male D. semiclausum. 5. Parasitism itself had the largest impact on host growth. SSD in the parasitoid is mainly the result of differences in growth rate of the parasitoid–host complex producing male and female wasps and differences in exploitation of the host resources. Female wasps converted host biomass more efficiently into adult biomass than males.
    https://doi.org/10.1111/j.1365-2311.2009.01130.x
  • Phytochemistry Reviews
    2009

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

    R. Gols, Jeff A. Harvey
    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.
    https://doi.org/10.1007/s11101-008-9104-6
  • Oikos
    2009

    Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps?

    R. Gols, Nicole M. van Dam, Ciska Raaijmakers, Marcel Dicke, Jeff A. Harvey
    In recent years, increasing attention has been paid in exploring the role of direct plant defence, through the production of allelochemicals, on the performance of parasitoid wasps and their hosts. However, few studies have determined if parasitoids can detect differences in plant quality and thus preferentially attack hosts on which their progeny develop most successfully. In this study we examined the development and preference of two endoparasitoids, Diadegmasemiclausum and Cotesia glomerata, developing in larvae of their respective hosts, Plutella xylostella and Pieris brassicae. In turn, these were reared on different wild populations of black mustard Brassica nigra originating in the Netherlands and Sicily (Italy), as well as single cultivated strains of B. nigra and brown mustard, B. juncea. Chemical analyses of foliar glucosinolates and volatile emissions by P. xylostella-damaged plants revealed large differences between B. nigra and B. juncea plants, with smaller differences among the B. nigra populations. The four mustard populations differentially affected development time and body mass of the herbivores and parasitoids. Contrasts among the means revealed significant differences mainly between B. nigra and B. juncea. Both parasitoids, however, preferred to alight on plants in which their progeny developed most successfully. In behavioural bioassays, D. semiclausum did not discriminate among the B. nigra populations and preferred to alight on B. juncea, which was the best plant population for parasitoid development. By contrast, C. glomerata females exhibited the lowest preference for Italian B. nigra populations, on which adult parasitoid size was the smallest. These results reveal that parasitoids can detect even small differences in plant quality presumably through their volatile blends and that plant preference and offspring performance in the two species are 'optimally synchronized'.
    https://doi.org/10.1111/j.1600-0706.2008.17231.x
  • Ecological Entomology
    2009

    Influence of presence and spatial arrangement of belowground insects on host-plant selection of aboveground insects: a field study

    J.J. Soler, Sonja Schaper, T. Martijn Bezemer, A.M. Cortesero, T.S. Hoffmeister, Wim H. van der Putten, Louise E.M. Vet, Jeff A. Harvey
    1. Several studies have shown that above- and belowground insects can interact by influencing each others growth, development, and survival when they feed on the same host-plant. In natural systems, however, insects can make choices on which plants to oviposit and feed. A field experiment was carried out to determine if root-feeding insects can influence feeding and oviposition preferences and decisions of naturally colonising foliar-feeding insects. 2. Using the wild cruciferous plant Brassica nigra and larvae of the cabbage root fly Delia radicum as the belowground root-feeding insect, naturally colonising populations of foliar-feeding insects were monitored over the course of a summer season. 3. Groups of root-infested and root-uninfested B. nigra plants were placed in a meadow during June, July, and August of 2006 for periods of 3 days. The root-infested and the root-uninfested plants were either dispersed evenly or placed in clusters. Once daily, all leaves of each plant were carefully inspected and insects were removed and collected for identification. 4. The flea beetles Phyllotreta spp. and the aphid Brevicoryne brassicae were significantly more abundant on root-uninfested (control) than on root-infested plants. However, for B. brassicae this was only apparent when the plants were placed in clusters. Host-plant selection by the generalist aphid M. persicae and oviposition preference by the specialist butterfly P. rapae, however, were not significantly influenced by root herbivory. 5. The results of this study show that the presence of root-feeding insects can affect feeding and oviposition preferences of foliar-feeding insects, even under natural conditions where many other interactions occur simultaneously. The results suggest that root-feeding insects play a role in the structuring of aboveground communities of insects, but these effects depend on the insect species as well as on the spatial distribution of the root-feeding insects.
    https://doi.org/10.1111/j.1365-2311.2008.01082.x
  • Physiological Entomology
    2008

    Comparing the physiological effects and function of larval feeding in closely-related endoparasitoids (Braconidae: Microgastrinae)

    Jeff A. Harvey, T. Martijn Bezemer, R. Gols, Nakamatsu Y., T. Tanaka
    The larvae of most endoparasitoid wasps consume virtually all host tissues before pupation. However, in some clades, the parasitoid larvae primarily consume haemolymph and fat body and emerge through the side of the host, which remains alive and active for up to several days. The evolutionary significance of this host-usage strategy has attracted attention in recent years. Recent empirical studies suggest that the surviving larva guards the parasitoid broods against natural enemies such as predators and hyperparasitoids. Known as the 'usurpation hypothesis', the surviving larvae bite, regurgitate fluids from the gut, and thrash the head capsule when disturbed. In the present study, the 'usurpation hypothesis' is tested in the association involving Manduca sexta, its parasitoid Cotesia congregata, and a secondary hyperparasitoid Lysibia nana. Percentage parasitoid survival is higher and hyperparasitism lower when cocoons of C. congregata are attached to the dorsum of M. sexta caterpillars. Fat body contents in several associations involving solitary and gregarious parasitoids feeding on haemolymph and fat body are also compared. The amount of fat body retained in parasitized caterpillars varies considerably from one association to another. In M. sexta and Pieris brassicae, considerable amounts of fat body remain after parasitoid emergence whereas, in Cotesia kariyai and Cotesia rufricus, virtually all of the fat body is consumed by the parsasitoid larvae. The length of post-egression survival of parasitized caterpillars differs considerably in several tested associations. In Pseudeletia separata, most larvae die within a few hours of parasitoid emergence whereas, in M. sexta, parasitized larvae live up to 2 weeks after parasitoid emergence. Larvae in other associations parasitized by gregarious and solitary endoparasitoids live for intermediate periods. The results are discussed in relation to the adaptive significance of different feeding strategies of immature parasitoids and of the costs and benefits of retaining the parasitized caterpillar in close proximity with the parasitoid cocoons.
    https://doi.org/10.1111/j.1365-3032.2008.00623.x
  • Nature
    2008

    Successful range-expanding plants experience less above-ground and below-ground enemy impact

    Many species are currently moving to higher latitudes and altitudes1, 2, 3. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects4, 5 in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range6, 7, 8. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.
    https://doi.org/10.1038/nature07474
  • Entomologia Experimentalis et Applicata
    2008

    Parasitoid load affects plant fitness in a tritrophic system

    R.C. Smallegange, Joop J.A. van Loon, S.E. Blatt, Jeff A. Harvey, Marcel Dicke
    Plants attacked by herbivorous insects emit volatile compounds that attract predators or parasitoids of the herbivores. Plant fitness increases when these herbivorous insects are parasitized by solitary parasitoids, but whether gregarious koinobiont parasitoids also confer a benefit to plant fitness has been disputed. We investigated the relationship between parasitoid load of the gregarious Cotesia glomerata (L.) (Hymenoptera: Braconidae), food consumption by larvae of their host Pieris brassicae L. (Lepidoptera: Pieridae), and seed production in a host plant, Brassica nigra L. (Brassicaceae), in a greenhouse experiment. Plants damaged by caterpillars containing single parasitoid broods produced a similar amount of seeds as undamaged control plants and produced significantly more seeds than plants with unparasitized caterpillars feeding on them. Increasing the parasitoid load to levels likely resulting from superparasitization, feeding by parasitized caterpillars was significantly negatively correlated with plant seed production. Higher parasitoid brood sizes were negatively correlated with pupal weight of Cotesia glomerata, revealing scramble competition leading to a fitness trade-off for the parasitoid. Our results suggest that in this tritrophic system plant fitness is higher when the gregarious parasitoid deposits a single brood into its herbivorous host. A prediction following from these results is that plants benefit from recruiting parasitoids when superparasitization is prevented. This is supported by our previous results on down-regulation of synomone production when Brassica oleracea was fed on by parasitized caterpillars of P. brassicae. We conclude that variable parasitoid loads in gregarious koinobiont parasitoids largely explain existing controversies about the putative benefit of recruiting these parasitoids for plant reproduction.
    https://doi.org/10.1111/j.1570-7458.2008.00693.x
  • Animal Behaviour
    2008

    Do parasitized caterpillars protect their parasitoids from hyperparasitoids? A test of the ‘usurpation hypothesis’

    Jeff A. Harvey, Martine Kos, Y. Nakamatsu, T. Tanaka, Marcel Dicke, Louise E.M. Vet, J. Brodeur, T. Martijn Bezemer
    Caterpillars that are attacked by some species of parasitoid wasps are known to survive for several days after the parasitoid larvae emerge and pupate. It has been argued that the behaviour of the parasitized larva is ‘usurped’ by the parasitoid and that it ‘guards’ the parasitoid cocoons against their own natural enemies such as hyperparasitoids (the ‘usurpation hypothesis'). We tested this hypothesis in the association involving a gregarious endoparasitoid, the wasp Cotesia glomerata; caterpillars of its host, the large cabbage white butterfly Pieris brassicae; and a pupal hyperparasitoid, the wasp Lysibia nana. In laboratory experiments, we presented cocoon broods of C. glomerata to single females of L. nana in arenas for 6 h. We tested several treatments for rates of primary parasitoid survival, including variation in the position of the caterpillar and the presence or absence of an additional silk web spun by parasitized caterpillars. Parasitized P. brassicae larvae survived longer than the period necessary for C. glomerata adults to emerge. Rates of parasitoid survival were, however, unaffected by the presence of a P. brassicae larva on the cocoon brood, although significantly more parasitoids emerged when the silk web was present. Analyses of the foraging behaviour of individual L. nana females in arenas, performed using Observer software, revealed that the wasps showed a greater tendency to leave cocoons when caterpillars and silk were present. The laboratory experiments only partially support the usurpation hypothesis. In nature, usurpation of the host of the primary parasitoid may be a more effective strategy against generalist predators than against more specialized and better-adapted hyperparasitoids.
    https://doi.org/10.1016/j.anbehav.2008.03.016
  • Entomologia Experimentalis et Applicata
    2008

    The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid

    R. Gols, L.M.A. Witjes, Joop J.A. van Loon, M.A. Posthumus, Marcel Dicke, Jeff A. Harvey
    Most studies on plant defenses against insect herbivores investigate direct and indirect plant defenses independently. However, these defenses are not necessarily mutually exclusive. Plant metabolites can be transmitted through the food chain and can also affect the herbivore's natural enemies. A conflict may arise when a natural enemy is attracted to a plant that is suboptimal in terms of its own fitness. In addition, plant defenses are often studied in cultivated plant species in which artificial selection may have resulted in reduced resistance against insect herbivores. In this study, we investigated both direct and indirect plant defenses in two closely related wild brassicaceous plant species, Brassica nigra L. and Sinapis arvensis L. The herbivore Pieris brassicae L. (Lepidoptera: Pieridae), which is specialized on brassicaceous plant species, developed faster and attained higher pupal mass when reared on B. nigra than on S. arvensis. In contrast, Cotesia glomerata L. (Hymenoptera: Braconidae), which is a gregarious endoparasitoid of P. brassicae caterpillars, developed equally well on P. brassicae irrespective of the food plant on which its host had been reared. The feeding strategy of the parasitoid larvae, that is, selectively feeding on hemolymph and fat body, is likely to allow for a much wider host-size range without affecting the size or development time of the emerging parasitoids. In flight chamber experiments, C. glomerata, which had an oviposition experience in a host that fed on Brussels sprout, exhibited significant preference for host-damaged B. nigra over host-damaged S. arvensis plants. Headspace analysis revealed quantitative and qualitative differences in volatile emissions between the two plant species. This parasitoid species may use a range of cues associated with the host and the host's food plant in order to recognize the different plant species on which the host can feed. These results show that there is no conflict between direct and indirect plant defenses for this plant–host–parasitoid complex.
    https://doi.org/10.1111/j.1570-7458.2008.00681.x
  • Evolutionary Ecology
    2008

    Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae)

    In most animals, the optimal phenotype is determined by trade-offs in life-history traits. Here, I compare development and reproductive strategies in two species of solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis, attacking pre-pupae of their primary parasitoid host, Cotesia glomerata. Parasitoid larvae of both species exploit a given amount of host resources with similar efficiency. However, adults exhibit quite different reproductive strategies. Both species are synovigenic, and female wasps emerge with no mature eggs. However, G. agilis must first host-feed to produce eggs, while L. nana does not host-feed but mobilizes internal resources carried over from larval feeding to initiate oogenesis. Further, G. agilis is wingless, produces large eggs, has a long life-span, and generates only small numbers of progeny per day, whereas these traits are reversed in L. nana. Given unlimited hosts, the fecundity curve in L. nana was “front-loaded,” whereas in G. agilis it was depressed and extended over much of adult life. In L. nana (but not G. agilis), wasps provided with honey but no hosts lived significantly longer than wasps provided with both honey and hosts. Differences in the fecundity curves of the two hyperparasitoids are probably based on differing costs of reproduction between them, with the wingless G. agilis much more constrained in finding hosts than the winged L. nana. Importantly, L. nana is known to be a specialist hyperparasitoid of gregarious Cotesia species that pupate in exposed locations on the food plant, whereas Gelis sp. attack and develop in divergent hosts such as parasitoid cocoons, moth pupae and spider egg sacs. Consequently, there is a strong match between brood size in C. glomerata and egg production in L. nana, but a mismatch between these parameters in G. agilis.
    https://doi.org/10.1007/s10682-007-9164-x
  • Agriculture, Ecosystems and Environment
    2008

    Effects of changes in plant species richness and community traits on carabid assemblages and feeding guilds

    Experiments were conducted between 2001 and 2003 in constructed plant communities that were set up in 1996 on abandoned agricultural land. The primary aim of the experiment was to study how different secondary vegetation succession scenarios influence community development of invertebrates in different trophic levels. The succession scenarios were obtained by sowing high diversity or low diversity seed mixtures of mid-successional plant species in 1996 in comparison with unsown plots where agriculture ceased in 1996 or 1999. Carnivorous carabid species generally preferred plots characterized by open vegetation, whereas herbivorous carabids generally favored plots associated with high plant diversity. However, carabid community composition was affected most by sampling year and there was also a dramatic shift over the three years in the relative proportion of the different trophic groups. Irrespective of treatment, the proportion of carnivores in the community declined with time, whereas phytophages increased over the course of the three years. By contrast, the proportion of omnivores peaked during the second year. These long-term changes were, at least to some extent, related to short-term changes in the structure and composition of the plant communities. The importance of local variation and temporal changes in plant species richness on carabids and other insect fauna are discussed.
    https://doi.org/10.1016/j.agee.2008.03.006
  • Botany
    2008

    Tolerence of Braccica nigra to Pieris brassicae herbivory

    S.E. Blatt, R.C. Smallegange, L. Hess, Jeff A. Harvey, D. Dicke, Joop J.A. van Loon
    Black mustard, Brassica nigra (L.) Koch, is a wild annual species found throughout Europe and fed on by larvae of the large cabbage-white butterfly, Pieris brassicae L. We examined the impact of herbivory from P. brassicae, a gregarious herbivore, on B. nigra grown from wild seed collected locally. In greenhouse studies, the response of B. nigra to four herbivore densities in two developmental stages of the plant was quantified by measuring leaf damage, plant height, days to flowering, silique number, and seed production. Pieris brassicae readily attacked B. nigra leaves, although the timing of the attack did not affect seed production; attacked plants produced as many seeds as as nonattacked plants. Plant height was affected when plants were attacked early, but not later, in development, suggesting a connection between their belowground zone of influence and ability to regain biomass. These results demonstrate that at the herbivore densities and timing of damage studied, B. nigra tolerates folivory from Pieris brassicae through compensation.
    https://doi.org/10.1139/B08-040
  • Annual Review of Entomology
    2008

    Resource acquisition, allocation, and utilization in parasitoid reproductive strategies

    M.A. Jervis, J. Ellers, Jeff A. Harvey
    Parasitoids display remarkable inter- and intraspecific variation in their reproductive and associated traits. Adaptive explanations have been proposed for many of the between-trait relationships. We present an overview of the current knowledge of parasitoid reproductive biology, focusing on egg production strategies in females, by placing parasitoid reproduction within physiological and ecological contexts. Thus, we relate parasitoid reproduction both to inter- and intraspecific patterns of nutrient allocation, utilization, and acquisition, and to key aspects of host ecology, specifically abundance and dispersion pattern. We review the evidence that resource trade-offs underlie several key intertrait correlations and that reproductive and feeding strategies are closely integrated at both the physiological and the behavioral levels. The idea that parasitoids can be divided into capital-breeders or income-breeders is no longer tenable; such terminology is best restricted to the females’ utilization of particular nutrients.
    https://doi.org/10.1146/annurev.ento.53.103106.093433
  • Journal of Chemical Ecology
    2008

    Oviposition cues for a specialist butterfly: plant chemistry and size

    J.H. Reudler Talsma, Arjen Biere, Jeff A. Harvey, S. van Nouhuys
    The oviposition choice of an insect herbivore is based on a complex set of stimuli and responses. In this study, we examined the effect of plant secondary chemistry (the iridoid glycosides aucubin and catalpol) and aspects of size of the plant Plantago lanceolata, on the oviposition behavior of the specialist butterfly Melitaea cinxia. Iridoid glycosides are known to deter feeding or decrease the growth rate of generalist insect herbivores, but can act as oviposition cues and feeding stimulants for specialized herbivores. In a previous observational study of M. cinxia in the field, oviposition was associated with high levels of aucubin. However, this association could have been the cause (butterfly choice) or consequence (plant induction) of oviposition. We conducted a set of dual- and multiple-choice experiments in cages and in the field. In the cages, we found a positive association between the pre-oviposition level of aucubin and the number of ovipositions. The association reflects the butterfly oviposition selection rather than plant induction that follows oviposition. Our results also suggest a threshold concentration below which females do not distinguish between levels of iridoid glycosides. In the field, the size of the plant appeared to be a more important stimulus than iridoid glycoside content, with bigger plants receiving more oviposition than smaller plants, regardless of their secondary chemistry. Our results illustrate that the rank of a cue used for oviposition may be dependent on environmental context
    https://doi.org/10.1007/s10886-008-9519-y
  • Ecology
    2008

    Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids

    R. Gols, Roel Wagenaar, Tibor Bukovinszky, Nicole M. van Dam, Marcel Dicke, J.M. Bullock, Jeff A. Harvey
    Populations of wild Brassica oleracea L. grow naturally along the Atlantic coastlines of the United Kingdom and France. Over a very small spatial scale (i.e.,
    https://doi.org/10.1890/07-0873.1
  • European Journal of Entomology
    2008

    Brood attending by females of the hyperparasitoid Trichomalopsis apanteloctena (Hymenoptera: Pteromalidae) on cocoon clusters of its host, Cotesia kariyai (Hymenoptera: Braconidae) and its effects on reproduction, development and survival

    N. Takai, Y. Nakamatsu, Jeff A. Harvey, K. Miura, T. Tanaka
    Theoretical models predict that brood guarding may evolve in situations where eggs are costly to produce or when handling times are long. This study reveals that females of the secondary hyperparasitoid Trichomalopsis apanteloctena guarded cocoon broods of Cotesia kariyai, a gregarious endoparasitoid. Hyperparasitoid females also monopolized host resources and protected their offspring by driving away other conspecific hyperparasitoid females. The females exhibited antagonistic behavior towards competitors through threatening body postures, biting and chasing. Using a video camera to determine how long a hyperparasitoid female attended and parasitized cocoons within a single host brood, it was found that after about 4 days, cocoon guarding behavior became much less apparent. Moreover, more than 90% of hosts were typically parasitized by a hyperparasitoid female over the course of 4 days after she commenced brood guarding. Observations of egg production during a female’s lifetime revealed a physiological interval rhythm that typically lasted 3–4 days, which correlates almost exactly with the period during which the cocoons were guarded. To confirm the giving-up time for a host cocoon brood, hyperparasitoid females were given access to 24 h-old cocoon clusters, each containing 60–100 individual cocoons. Ninety percent of the females remained on cocoons for approximately 72 h. Furthermore, twenty-five percent of wasps continued attending and presumably guarding host cocoon broods for more than 138 h after the female first attended the brood. C. kariyai larvae pupate within a few hours of egression from their host and emerge as adults about 5 days (120 h) later. Therefore, many hyperparasitoid females continued to guard older host cocoons of greatly reduced quality as a resource for their progeny and some even after eclosion of the primary parasitoid. Late-brood guarding enabled a hyperparasitoid female to protect her own progeny from other hyperparasitoid females that readily attacked and killed them when she was removed. Our study thus reveals that extended guarding behavior is an adaptive mechanism that probably plays an important role in the survival of the original brood.
  • Plant Signaling & Behavior
    2008

    Plants as green as phones: Novel insights into plant-mediated communication between below- and above-ground insects

    Roxina Soler , Jeff A. Harvey, T. Martijn Bezemer, J.F. Stuefer
    can act as vertical communication channels or ‘green phones’ linking soil-dwelling insects and insects in the aboveground ecosystem. When root-feeding insects attack a plant, the direct defense system of the shoot is activated, leading to an accumulation of phytotoxins in the leaves. The protection of the plant shoot elicited by root damage can impair the survival, growth and development of aboveground insect herbivores, thereby creating plant-based functional links between soil-dwelling insects and insects that develop in the aboveground ecosystem. The interactions between spatially separated insects below- and aboveground are not restricted to root and foliar plant-feeding insects, but can be extended to higher trophic levels such as insect parasitoids. Here we discuss some implications of plants acting as communication channels or ‘green phones’ between root and foliar-feeding insects and their parasitoids, focusing on recent findings that plants attacked by root-feeding insects are significantly less attractive for the parasitoids of foliar-feeding insects.
    https://doi.org/10.4161/psb.3.8.6338
  • Journal of Chemical Ecology
    2008

    Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations

    R. Gols, Tibor Bukovinszky, Nicole M. van Dam, Marcel Dicke, J.M. Bullock, Jeff A. Harvey
    Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.
    https://doi.org/10.1007/s10886-008-9429-z
  • Journal of Natural History
    2007

    The parasitoid complex associated with the herbivore Hadena bicruris (Lepidoptera: Noctuidae) on Silene latifolia (Caryophyllaceae) in the Netherlands

    Jelmer Elzinga, K. Zwakhals, Jeff A. Harvey, Arjen Biere
    Larvae of the moth, Hadena bicruris, constitute the most important predispersal seed predator on Silene latifolia (Caryophyllaceae). Parasitoids attacking the larvae of this specialist noctuid can potentially decrease the amount of damage to the plant. This paper describes and quantifies the parasitoid complex associated with H. bicruris in the Netherlands, and documents life history characters of its species. Forty-four percent of larval H. bicruris were parasitized by at least 13 species of parasitoids. The most prevalent of these were the braconids Microplitis tristis (22.9%) and Bracon variator (4.9%) and the ichneumonids Eurylabus tristis (11.7%) and Ophion pteridis (3.4%). Other species occurring sporadically were: the ichneumonids Scambus brevicornis, S. buolianae, Erigorgus cerinops, and Hyposoter sp.; the tachinids Phryxe vulgaris, P. nemea, Blondelia nigripes and Siphona geniculata; and a Mermithidae sp. The ichneumonid hyperparasitoid Mesochorus lanceolatus was fo! und occasionally in larvae of M. tristis. The hyperparasitoid ichneumonids Gelis agilis, G. hortensis and the chalcids Barvscapus endemus, Pteromalus chrysos and P. vibulenus were found in cocoons of both M. tristis and B. variator. The primary parasitoids M. tristis, E. tristis, and to a lesser extent, O. pteridis, are believed to be specialized on Hadena. The effect of the parasitoids on herbivory by their host is probably small because the most common parasitoid species are koinobionts that attack large, late instar hosts. Only B. variator and Scambus spp., which are ectoparasitoids, arrest host development immediately upon parasitism, but like the other parasitoids they kill mainly large L4 or L5 hosts. The gregarious M. tristis and B. variator produce clutches with a female-biased sex ratio, in contrast to the solitary E. tristis where the sex ratio approaches equality. The ectoparasitoid B. variator produces mostly single-sex clutches, probably avoiding deleterious ef! fects of inbreeding. The clutch size distributions suggest tha! t large clutches of M. tristis and B. variator are probably caused by multiple parasitisms.
    https://doi.org/10.1080/00222930601121668
  • Basic and Applied Ecology
    2007

    Temporal changes affect plant chemistry and tritrophic interactions

    R. Gols, Ciska Raaijmakers, Nicole M. van Dam, Marcel Dicke, Tibor Bukovinszky, Jeff A. Harvey
    In nature, individuals of short-lived plant species (e.g. annuals, biennials) may grow at different times during the growing season. These plants are therefore exposed to different season-related conditions such as light and temperature, which in turn may have consequences for primary and secondary chemistry of the plant. Despite this, many studies examining plant–consumer interactions are performed in single replicates, which may thus ignore temporal variation in the expression of phenotypic plant traits that affect multitrophic interactions. In the present study, we demonstrated that even under strictly controlled conditions in a greenhouse, secondary plant chemistry changes dramatically in plants growing at different times in a single year, i.e. July, August and November. Glucosinolate (GS) contents in herbivore-damaged leaves of two different crucifer species, Brassica oleracea and Sinapis alba were higher in the August and November replicates than in the July replicate and GS concentrations were 10–25 times higher in S. alba than in B. oleracea. The development of a specialist herbivore, Plutella xylostella, also varied significantly over the three replicates. Larvae of P. xylostella that had fed upon either S. alba or B. oleracea, attained the largest biomass and had the fastest development rate in the November replicate. Female P. xylostella moths grew larger on S. alba than on B. oleracea, whereas male biomass was not significantly affected by host-plant species. Plant species, but not season also affected performance of the endoparasitoid, Diadegma semiclausum. Similar to the performance of host females, parasitoid males developed faster and attained the highest biomass when attacking P. xylostella larvae feeding on S. alba. Most importantly, the performance of the herbivore and its parasitoid only appeared to partially conform to levels of GS in damaged leaves, indicating that there is a complex of factors involved in determining the effects of plant quality on higher trophic levels.
    https://doi.org/10.1016/j.baae.2006.09.005
  • Plant Ecology
    2007

    Nutritional suitability and ecological relevance of Arabidopsis thaliana and Brassica oleracea as foodplants for the cabbage butterfly, Pieris rapae

    Jeff A. Harvey, L.M.A. Witjes, Maria Benkirane, Henk Duyts, Roel Wagenaar
    The thale cress, Arabidopsis thaliana, is considered to be an important model species in studying a suite of evolutionary processes. However, the species has been criticized on the basis of its comparatively small size at maturity (and consequent limitations in the amount of available biomass for herbivores) and on the duration and timing of its life cycle in nature. In the laboratory, we studied interactions between A. thaliana and the cabbage butterfly, Pieris rapae, in order to determine if plants are able to support the complete development of the herbivore. Plants were grown in pots from seedlings in densities of one, two, or four per pot. In each treatment, one, two, or five newly hatched larvae of P. rapae were placed on fully developed rosettes of A. thaliana. In a separate experiment, the same densities of P. rapae larvae were reared from hatching on single mature cabbage (Brassica oleracea) plants. Pupal fresh mass and survival of P. rapae declined with larval density when reared on A. thaliana but not on B. oleracea. However, irrespective of larval density and plant number, some P. rapae were always able to complete development on A. thaliana plants. A comparison of the dry mass of plants in different treatments with controls (= no larvae) revealed that A. thaliana partially compensated for plant damage when larval densities of P. rapae were low. By contrast, single cress plants with 5 larvae generally suffered extensive damage, whereas damage to B. oleracea plants was negligible. Rosettes of plants that were monitored in spring, when A. thaliana naturally grows, were not attacked by any insect herbivores, but there was often extensive damage from pulmonates (slugs and snails). Heavily damaged plants flowered less successfully than lightly damaged plants. Small numbers of generalist plant-parasitic nematodes were also recovered in roots and root soil. By contrast, plants monitored in a sewn summer plot were heavily attacked by insect herbivores, primarily flea beetles (Phyllotreta spp.). These results reveal that, in natural populations of A. thaliana, there is a strong phenological mismatch between the plant and most of its potential specialist insect herbivores (and their natural enemies). However, as the plant is clearly susceptible to attack from non-insect generalist invertebrate herbivores early in the season, these may be much more suitable for studies on direct defense strategies in A. thaliana.
    https://doi.org/10.1007/s11258-006-9204-6
  • Journal of Chemical Ecology
    2007

    Development of an insect herbivore and its pupal parasitoid reflect differences in direct plant defense

    Jeff A. Harvey, R. Gols, Roel Wagenaar, T. Martijn Bezemer
    In nature, plants defend themselves by production of allelochemicals that are toxic to herbivores. There may be considerable genetic variation in the expression of chemical defenses because of various selection pressures. In this study, we examined the development of the small cabbage butterfly, Pieris rapae, and its gregarious pupal ectoparasitoid, Pteromalus puparum, when reared on three wild populations (Kimmeridge, Old Harry, Winspit) of cabbage, Brassica oleracea, and a Brussels sprout cultivar. Wild plant populations were obtained from seeds of plants that grow naturally along the south coast of Dorset, England. Significant differences in concentrations of allelochemicals (glucosinolates) were found in leaves of plants damaged by P. rapae. Total glucosinolate concentrations in Winspit plants, the population with the highest total glucosinolate concentration, were approximately four times higher than in the cultivar, the strain with the lowest total glucosinolate concentration. Pupal mass of P. rapae and adult body mass of Pt. puparum were highest when reared on the cultivar and lowest when developing on Kimmeridge plants, the wild strain with the lowest total glucosinolate concentration. Development of male parasitoids was also more negatively affected than female parasitoids. Our results reveal that plant quality, at least for the development of ‘adapted’ oligophagous herbivores, such as P. rapae, is not based on total glucosinolate content. The only glucosinolate compound that corresponded with the performance of P. rapae was the indole glucosinolate, neoglucobrassicin. Our results show that performance of ectoparasitoids may closely reflect constraints on the development of the host.
    https://doi.org/10.1007/s10886-007-9323-0
  • Archives of Insect Biochemistry and Physiology
    2007

    Cotesia kariyai larvae need an anchor to emerge from the host Pseudaletia separata

    Y. Nakamatsu, T. Tanaka, Jeff A. Harvey
    Mature larvae of the gregarious endoparasitoid Cotesia kariyai construct cocoons for pupation approximately 10 days after parasitization and emerge from their host Pseudaletia separata under a long day photo-regime (16L8D) at 25 ± 1°C. The parasitoid larvae make capsules in the host hemocoel just prior to their emergence. These capsules function as anchors, which enable them to press against the host integument from inside the host. It was predicted that this anchor might be composed of silk proteins secreted from the parasitoid larvae, because a previous study showed that the anchor was made up of a glycoprotein and that the silk gland of parasitoid larvae developed from 2nd larval stage. Fibroin-like proteins in C. kariyai larva mainly consist of two proteins with molecular masses of the 300.6 and 46.7 kDa estimated by SDS-PAGE. The fibroin-like proteins with the same molecular mass were detected from the anchor proteins just prior to parasitoid emergence. These results indicate that the anchor was assembled with fibrion-like proteins and was formed just before parasitoid emergence while in the host body cavity. Injection of bovine pancreatic trypsin inhibited the emergence of parasitoid larvae from the host because the anchor was decomposed by trypsin. Trypsin activity in the parasitized host hemolymph increased only after parasitoid emergence.
    https://doi.org/10.1002/arch.20189
  • Oecologia
    2007

    Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid

    The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.
    https://doi.org/10.1007/s00442-006-0649-z
  • Journal of Chemical Ecology
    2007

    Flower vs. leaf feeding by Pieris brassicae : Glucosinolate-rich flower tissues are preferred and sustain higher growth rate

    R.C. Smallegange, Joop J.A. van Loon, S.E. Blatt, Jeff A. Harvey, N. Agerbirk, Marcel Dicke
    Interactions between butterflies and caterpillars in the genus Pieris and plants in the family Brassicaceae are among the best explored in the field of insect–plant biology. However, we report here for the first time that Pieris brassicae, commonly assumed to be a typical folivore, actually prefers to feed on flowers of three Brassica nigra genotypes rather than on their leaves. First- and second-instar caterpillars were observed to feed primarily on leaves, whereas late second and early third instars migrated via the small leaves of the flower branches to the flower buds and flowers. Once flower feeding began, no further leaf feeding was observed. We investigated growth rates of caterpillars having access exclusively to either leaves of flowering plants or flowers. In addition, we analyzed glucosinolate concentrations in leaves and flowers. Late-second- and early-third-instar P. brassicae caterpillars moved upward into the inflorescences of B. nigra and fed on buds and flowers until the end of the final (fifth) instar, after which they entered into the wandering stage, leaving the plant in search of a pupation site. Flower feeding sustained a significantly higher growth rate than leaf feeding. Flowers contained levels of glucosinolates up to five times higher than those of leaves. Five glucosinolates were identified: the aliphatic sinigrin, the aromatic phenyethylglucosinolate, and three indole glucosinolates: glucobrassicin, 4-methoxyglucobrassicin, and 4-hydroxyglucobrassicin. Tissue type and genotype were the most important factors affecting levels of identified glucosinolates. Sinigrin was by far the most abundant compound in all three genotypes. Sinigrin, 4-hydroxyglucobrassicin, and phenylethylglucosinolate were present at significantly higher levels in flowers than in leaves. In response to caterpillar feeding, sinigrin levels in both leaves and flowers were significantly higher than in undamaged plants, whereas 4-hydroxyglucobrassicin leaf levels were lower. Our results show that feeding on flower tissues, containing higher concentrations of glucosinolates, provides P. brassicae with a nutritional benefit in terms of higher growth rate. This preference appears to be in contrast to published negative effects of volatile glucosinolate breakdown products on the closely related Pieris rapae.
    https://doi.org/10.1007/s10886-007-9350-x
  • Oikos
    2007

    Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

    Roxina Soler , Jeff A. Harvey, A.F.D. Kamp, Louise E.M. Vet, Wim H. van der Putten, Nicole M. van Dam, J.F. Stuefer, R. Gols, Cees Hordijk, T. Martijn Bezemer
    It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata, a parasitoid of the leaf herbivore Pieris brassicae, mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.
    https://doi.org/10.1111/j.0030-1299.2007.15501.x
  • Environmental Entomology
    2007

    Optimum and maximum host size at parasitism for the endoparasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) differ greatly between two host species

    J.H. Reudler Talsma, Jelmer Elzinga, Jeff A. Harvey, Arjen Biere
    Host size is considered a reliable indicator of host quality and an important determinant of parasitoid fitness. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism. In contrast with hemolymph-feeding koinobionts, tissue-feeding koinobionts face not only a minimum host size for successful development but also a maximum host size, because consumption of the entire host is often necessary for successful egression. Here we study interactions between a generalist tissue-feeding larval endoparasitoid, Hyposoter didymator Thunberg (Hymenoptera: Ichneumonidae) and two of its natural hosts, Spodoptera exigua Hübner and Chrysodeixis chalcites Esper (Lepidoptera: Noctuidae). Larvae of C. chalcites are up to three times larger than corresponding instars of S. exigua and also attain much higher terminal masses before pupation. We hypothesized that the range of host instars suitable for successful parasitism by H. didymator would be much more restricted in the large host C. chalcites than in the smaller S. exigua. To test this hypothesis, we monitored development of H. didymator in all instars of both host species and measured survival, larval development time, and adult body mass of the parasitioid. In contrast with our predictions, C. chalcites was qualitatively superior to S. exigua in terms of the survival of parasitized hosts, the proportion of parasitoids able to complete development, and adult parasitoid size. However, in both hosts, the proportion of mature parasitoid larvae that successfully developed into adults was low at the largest host sizes. Our results suggest that qualitative, as well as quantitative, factors are important in the success of tissue-feeding parasitoids.
    https://doi.org/10.1603/0046-225X(2007)36[1048:OAMHSA]2.0.CO;2
  • Ecological Entomology
    2007

    Effects of dietary nicotine on the development of an insect herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels

    Jeff A. Harvey, Nicole M. van Dam, L.M.A. Witjes, Roxina Soler , R. Gols
    Allelochemicals in herbivore diet are known to affect the development of higher trophic levels, such as parasitoids and predators. 2. This study examines how differing levels of nicotine affects the development of a herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels. Separate cohorts of the herbivore, Manduca sexta, were fed on artificial diets containing 0.0, 0.1, and 0.5% wet weights of nicotine. Some of the larvae in each cohort were separately parasitised in the first (L1) and third (L3) instars by the gregarious endoparasitoid, Cotesia congregata. Newly emerged parasitoid cocoons were, in 3. Pupal mass in M. sexta was negatively correlated with nicotine concentrations in the artificial diet, although larval development time was unaffected. 4. Hyperparasitoid survival was highest when there were low levels of nicotine in the diet of M. sexta. Cocoon mass in C. congregata and adult mass in L. nana were mostly affected by nicotine levels in host diet when L1 M. sexta larvae were parasitised. The effects were slightly stronger on L. nana than on C. congregata, indicating the presence of both qualitative and quantitative effects of nicotine concentration on both species. 5. The results suggest that allelochemicals in herbivore diet can have both direct and indirect effects on the performance of higher trophic levels. However, in multitrophic interactions these effects can vary with the stage of the herbivore attacked by the primary parasitoid, as well as with the strategy employed by the herbivore to deal with plant phytotoxins.
    https://doi.org/10.1111/j.1365-2311.2006.00838.x
  • Functional Ecology
    2007

    Foraging efficiency of a parasitoid of a leaf herbivore is influenced by root herbivory on neighbouring plants

    1. Root feeding insects can influence foliar quality of the host plant, which can affect the development and behaviour of leaf herbivores and parasitoids. Thus far, such interactions have been reported in situations where root and leaf associated organisms share a host-plant. We tested whether root herbivory influences searching behaviour of an above-ground parasitoid when the foliar feeding host of the parasitoid and the root herbivore are feeding on different plants. 2. We manipulated the proportion of 25 plants (ranging from 0 to 1) exposed to root herbivory by Delia radicum (neighbouring-plants). Five additional plants were infested above-ground with Pieris brassicae larvae (host-infested plants) and were placed in-between the neighbouring plants. We then released females of the parasitoid Cotesia glomerata which attacks P. brassicae and studied foraging efficiency of the parasitoid. 3. Overall, parasitoids located more host-infested plants during the maximum allowed searching time, and found their hosts about three times faster when neighbouring plants were exposed to root herbivory, than when neighbouring plants were not infested with D. radicum. Similar results were found when the host-infested plants were also exposed to root herbivory. 4. Our results show that the interaction between an above-ground foliar feeding insect and its parasitoid can be influenced by the presence of non-host herbivores feeding on the roots of neighbouring conspecific plants.
    https://doi.org/10.1111/j.1365-2435.2007.01309.x
  • Journal of Applied Entomology
    2006

    Development of the herbivore Pieris rapae and its endoparasitoid Cotesia rubecula on crucifers of field edges

    Jeff A. Harvey, Roel Wagenaar
    Several studies have reported that flowering herbs, which grow naturally or are sown adjacent to agricultural fields, may be an important source of nutrients for natural enemies. Many parasitoids readily feed on plant exudates such as floral nectar, which contain different types of sugars that enable the insects to optimize their longevity, mobility and reproductive success. However, leaf tissues of plants grown in the margins of agricultural fields may also provide food for immature stages of insect herbivores, such as caterpillars, that are in turn attacked by parasitoids. Herbivores and their parasitoids may later disperse into the crop, so the nutritional quality of surrounding plants, as this affects herbivore and parasitoid fitness, may also influence the success of biological control programmes, especially later in the season. Here, we compare the suitability of three species of cruciferous plants (Brassicaceae) on the development of Pieris rapae L. (Lep., Pieridae) and its solitary endoparasitoid, Cotesia rubecula Marshall (Hym., Bracondiae). Insects were reared on a feral population of cabbage, Brassica oleracea, on radish Raphanus sativus, which is widely sown in agricultural margins, and on hedge mustard, Sisymbrium officinale, a wild crucifer which often grows in medium to large stands along road verges and field edges. Development time in both the herbivore and parasitoid were extended on R. sativus, compared with the other two species, whereas C. rubecula completed its development most rapidly on B. oleracea. Moreover, adult butterflies and parasitoids were significantly smaller when reared on R. sativus plants. Our results reveal that differences in the quality of plants growing adjacent to agricultural fields can affect the development of key herbivores and their parasitoids. This should be borne in mind when establishing criteria for the selection of floral biodiversity.
    https://doi.org/10.1111/j.1439-0418.2006.01093.x
  • Acta Oecologica
    2006

    Long-term effects of sowing high or low diverse seed mixtures on plant and gastropod diversity

    I. Dedov, I.L. Stoyanov, L. Penev, Jeff A. Harvey, Wim H. van der Putten, T. Martijn Bezemer
    A number of studies have reported that consumers affect a range of community-level processes, and in turn their diversity and abundance is influenced by the structure and diversity of the plant community. Although gastropods are important generalist herbivores in many environments, few studies have examined the effects of plant species richness and plant community structure on gastropods. This study investigated gastropod species richness and interactions with various above-ground parameters of the vegetation on an experimental field with four plant treatments: low and high diversity of sown later succession plant species, natural colonization at the start of the experiment and natural colonization after 3 years of continued agricultural practice. The investigated gastropod assemblage contained only seven species and was highly dominated by two of them. Both in pitfalls and with hand-sorting the number of species collected per plot was highest in plots with natural plant colonization. Multivariate analysis revealed that overall gastropod abundance was positively associated with plant height and percentage cover of plants, and negatively with percentage grass cover. The same pattern holds for one of the dominant species-complex (Cochlicopa lubrica/lubricella). The other dominant gastropod species (Deroceras reticulatum) was more abundant in samples with higher percentages of moss cover and higher plant diversity, while less abundant at samples with higher plant cover, indicating that the gastropod species preferences may matter more than just their response to plant diversity. Two plant–gastropod species-level associations were observed: Senecio jacobaea with D. reticulatum and Tanacetum vulgare with Cochlicopa spp. The present study also demonstrated that pitfall-traps are suitable for collecting terrestrial gastropods, at least for species-poor grassland habitats. [KEYWORDS: Cochlicopa spp. ; Deroceras reticulatum ; Plant diversity ; Plant–gastropod interactions ; Terrestrial gastropod diversity ; Vegetation structure]
    https://doi.org/10.1016/j.actao.2006.03.004
  • Ecology
    2006

    Interplay between Senecio jacobaea and plant, soil and aboveground insect herbivore community composition

    T. Martijn Bezemer, Jeff A. Harvey, George Kowalchuk, H. Korpershoek, Wim H. van der Putten
    To elucidate the factors that affect the performance of plants in their natural environment, it is essential to study interactions with other neighboring plants, as well as with above- and belowground higher trophic organisms. We used a long-term field experiment to study how local plant community diversity influenced colonization by the biennial composite Senecio jacobaea in its native range in The Netherlands in Europe. We tested the effect of sowing later-succession plant species (0, 4, or 15 species) on plant succession and S. jacobaea performance. Over a period of eight years, the percent cover of S. jacobaea was relatively low in communities sown with 15 or 4 later-succession plant species compared to plots that were not sown, but that were colonized naturally. However, after four years of high abundance, the density of S. jacobaea in unsown plots started to decline, and the size of the individual plants was smaller than in the plots sown with 15 or 4 plant species. In the unsown plots, densities of aboveground leaf-mining, flower-feedin In a greenhouse experiment, we grew S. jacobaea in sterilized soil inoculated with soil from the different sowing treatments of the field experiment. Biomass production was lower when S. jacobaea test plants were grown in soil from the unsown plots than in soil from the sown plots (4 or 15 species). Molecular analysis of the fungal and bacterial communities revealed that the composition of fungal communities in unsown plots differed significantly from those in sown plots, suggesting that soil fu
    https://doi.org/10.1890/0012-9658(2006)87[2002:IBSJAP]2.0.CO;2
  • Journal of Insect Physiology
    2006

    Influence of nutrient deficiency caused by host developmental arrest on the growth and development of a koinobiont parasitoid

    Y. Nakamatsu, K. Kuriya, Jeff A. Harvey, T. Tanaka
    Koinobiont parasitoids utilize nutrients obtained from hosts that contine to feed and grow after parasitization. However, if the ecdysis of early host instars is prevented, parasitized larvae will fail to grow large enough to support the development of the parasitoid brood and both organisms will perish. When L5 instar larvae (the penultimate stage) of Pseudaletia separata were parasitized by Cotesia kariyai and injected with Euplectrus separatae venom (5PV), the development of these hosts was arrested before molting to the next stage and the caterpillars thus failed to gain weight. These hosts remained at approximately 300 mg until parasitoid emergence. In contrast, hosts parasitized as L5 but without the injection of venom (5P) exhibited an increase in weight after molting to the next stage and ultimately grew to approximately 700 mg. The inhibition of ecdysis reduced the amount of food resource (e.g. fat body) for the parasitoid larvae. On the other hand, when final (=L6) host instars were parasitized and injected with E. separatae venom (6PV), the maximum weight attained by these larvae was about 710 mg, although weight gain was depressed compared to hosts parasitized without the injection of E. separatae venom (6P). The adult weight of C. kariyai that emerged from 5PV hosts was less than conspecifics that emerged from 5P, 6P, and 6PV respectively, although the egg-pupal period of the parasitoid from 5PV hosts was extended. The offspring sex ratio (percentage males) of adult wasps did not vary significantly with treatment. Female parasitoids that eclosed from 5PV hosts laid almost the same number of eggs in day 0–6th host instars as those emerging from 5P, 6P, 6PV hosts. Their egg-pupal period was extended a
    https://doi.org/10.1016/j.jinsphys.2006.06.009
  • Archives of Insect Biochemistry and Physiology
    2006

    Remarkable similarity in body mass of a secondary hyperparasitoid Lysibia nana and its primary parasitoid host Cotesia glomerata emerging from cocoons of a comparable size

    Lysibia nana is a solitary, secondary idiobiont hyperparasitoid that attacks newly cocooned pre-pupae and pupae of several closely related gregarious endoparasitoids in the genus Cotesia, including C. glomerata. Prior to oviposition, the female wasp injects paralysing venom into the host, thus preventing further development. Here, host fate, emerging hyperparasitoid mass, and egg-to-adult development time was compared in hosts parasitized at different ages over 24-h intervals. Cocoons of C. glomerata were parasitized by L. nana at 12, 36, 60, 84, and 108 h post-egression from the secondary host, Pieris brassicae. Hyperparasitoid survival exceeded 80% in hosts parasitized within the first 60 h after pupation, but dropped thereafter, with no hyperparasitoids emerging in hosts aged 108 h. The mass of hyperparasitoids was positively correlated with the mass of the host cocoon, and this relationship remained consistent in hosts up to 60 h old. Within each host age cohort, the mass of male and female wasps was not significantly different. Development time in L. nana was uniform in hosts up to 60 h old, but increased significantly in 84-h-old hosts, and male wasps completed their development earlier than female wasps. Regulation of host growth varied with the age of the host at parasitism, with the early growth of older hosts reduced much more dramatically than young hosts. Unlike most parasitoids, pupal hyperparasitoids do not make cocoons but instead pupate within the already prepared cocoon of the host parasitoid. Consequently, for a given mass of cocoon, newly emerged L. nana adults were remarkably similar in size with male and female adults of C. glomerata. This reveals that L. nana is extremely efficient at exploiting its primary parasitoid host. [KEYWORDS: Cotesia glomerata ; development ; host quality ; hyperparasitoid ; idiobiont ; Lysibia nana]
    https://doi.org/10.1002/arch.20080
  • Journal of Chemical Ecology
    2005

    Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids

    Jeff A. Harvey, S. van Nouhuys, Arjen Biere
    Studies in crop species show that the effect of plant allelochemicals is not necessarily restricted to herbivores, but can extend to (positive as well as negative) effects on performance at higher trophic levels, including the predators and parasitoids of herbivores. We examined how quantitative variation in allelochemicals (iridoid glycosides) in ribwort plantain, Plantago lanceolata, affects the development of a specialist and a generalist herbivore and their respective specialist and generalist endoparasitoids. Plants were grown from two selection lines that differed ca. 5-fold in the concentration of leaf iridoid glycosides. Development time of the specialist herbivore, Melitaea cinxia, and its solitary endoparasitoid, Hyposoter horticola, proceeded most rapidly when reared on the high iridoid line, whereas pupal mass in M. cinxia and adult mass in H. horticola were unaffected by plant line. Cotesia melitaearum, a gregarious endoparasitoid of M. cinxia, performed equally well on hosts feeding on the two lines of P. lanceolata. In contrast, the pupal mass of the generalist herbivore, Spodoptera exigua, and the emerging adult mass of its solitary endoparasitoid, C. marginiventris, were significantly lower when reared on the high line, whereas development time was unaffected. The results are discussed with regards to (1) differences between specialist and generalist herbivores and their natural enemies to quantitative variation in plant secondary chemistry, and (2) potentially differing selection pressures on plant defense. [KEYWORDS: Chemical defense ; iridoid glycosides ; Melitaea cinxia ; multitrophic interactions ; Plantago lanceolata ; Spodoptera exigua]
    https://doi.org/10.1007/s10886-005-1341-1
  • Ecological Entomology
    2005

    Age-dependent clutch size in a koinobiont parasitoid

    Jelmer Elzinga, Jeff A. Harvey, Arjen Biere
    1. The Lack clutch size theory predicts how many eggs a female should lay to maximise her fitness gain per clutch. However, for parasitoids that lay multiple clutches it can overestimate optimal clutch size because it does not take into account the future reproductive success of the parasitoid. 2. From egg-limitation and time-limitation models, it is theoretically expected that (i) clutch size decreases with age if host encounter rate is constant, and (ii) clutch size should increase with host deprivation and hence with age in host-deprived individuals. 3. Clutch sizes produced by ageing females of the koinobiont gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) that were provided daily with hosts, and of females ageing with different periods of host deprivation were measured. 4. Contrary to expectations, during the first 2 weeks, clutch size did not change with the age of the female parasitoid, neither with nor without increasing host-deprivation time. 5. After the age of 2 weeks, clutch size decreased for parasitoids that parasitised hosts daily. The decrease was accompanied by a strong decrease in available eggs. However, a similar decrease occurred in host-deprived parasitoids that did not experience egg depletion, suggesting that egg limitation was not the only factor causing the decrease in clutch size. 6. For koinobiont parasitoids like M. tristis that have low natural host encounter rates and short oviposition times, the costs of reproduction due to egg limitation, time limitation, or other factors are relatively small, if the natural lifespan is relatively short. 7. Koinobiont parasitoid species that in natural situations experience little variation in host density and host quality might not have strongly evolved the ability to adjust clutch size. [KEYWORDS: Ageing ; clutch size adjustment ; egg limitation ; Hadena bicruris ; host deprivation ; time limitation]
    https://doi.org/10.1111/j.0307-6946.2005.00672.x
  • 2005

    The Life Cycle

    M.A. Jervis, M.J.W. Copland, Jeff A. Harvey
  • Journal of Animal Ecology
    2005

    Reduced foraging efficiency of a parasitoid under habitat complexity: implications for population stability and species coexistence

    R. Gols, Tibor Bukovinszky, L. Hemerik, Jeff A. Harvey, J.C. Van Lenteren, Louise E.M. Vet
    1. Habitat complexity may stabilize interactions among species of different trophic levels by providing refuges to organisms of lower trophic levels. 2. Searching behaviour of the parasitoid, Diadegma semiclausum, was followed in different semifield set-ups, a low and high-density monoculture of Brassica oleracea and two intercrops, B. oleracea with Sinapis alba (also a member of the Brassicaceae) and B. oleracea with Hordeum vulgare (Poaceae). 3. When a low-density monocrop of B. oleracea was compared with a high-density monocrop, no differences were found in the ability of the female wasps to locate a host-infested plant, B. oleracea, infested with Plutella xylostella that was placed in the centre of the set-up. 4. The efficiency of the parasitoid to locate the host-infested plant was differentially affected by the species composition of the vegetation. Wasps entered the Sinapis-Brassica set-up faster, but took more time to find the host-infested plant than in the Hordeum-Brassica set-up. 5. The horizontal arrangement, i.e. by mixing S. alba or H. vulgare with, or placing them as rows between B. oleracea, did not affect host-finding efficiency. 6. Plant height did influence host finding. Wasps found the host-infested plants earlier in the set-up with short Sinapis plants compared with tall Sinapis plants. 7. Once the wasps had landed on the host-infested plant, the surrounding vegetation did not affect time needed to parasitize five consecutive hosts on the same infested plant, regardless of the composition or horizontal/vertical arrangement of the set-up. 8. Chemical and structural refuges in complex landscapes may play an important role in the persistence of this system through dampening oscillations of parasitoid and host populations. [KEYWORDS: crucifers ; Diadegma semiclausum ; Plutella xylostella ; proportional hazards model ; refuges]
    https://doi.org/10.1111/j.1365-2656.2005.01003.x
  • Ecological Entomology
    2005

    Influence of adult nutrition on the relationship between body size and reproductive parameters in a parasitoid wasp

    1. An important constraint upon life-history evolution in parasitoids is the limit imposed by body size on allocation of limited metabolic resources to different fitness-related physiological functions such as reproduction and survival. 2. The influence of adult nutrition on reproductive and maintenance variables was studied in the synovigenic ectoparasitoid Mastrus ridibundus, and it was determined whether resource allocation to these different functions depends on body size. 3. Over the course of adult life there was a positive relationship between body size and the number of mature eggs in adult females both in the presence and absence of food. However, only in the presence of food did egg maturation rates increase significantly with body size. Starved wasps produced significantly smaller eggs than fed ones, which has not been documented before. Moreover, starved wasps produced fewer offspring than fed wasps, and attacked fewer hosts. 4. The availability of food had a major effect on longevity, with fed females living about 10 times longer than starved ones. There was also a positive relationship between body size and longevity. In starved wasps, this relationship was the same both in the presence and absence of hosts, but in fed wasps there was a positive relationship between body size and longevity in the absence of hosts only. Allocation to initial eggs relative to lifetime progeny production did not decline with body size 5. The data reveal that in M. ridibundus the trade-off between maintenance and reproduction varies with life expectancy. [KEYWORDS: Egg maturation ; egg production ; egg size ; reproductive strategies ; resource allocation ; sizefitness relationship ; synovigeny]
    https://doi.org/10.1111/j.0307-6946.2005.00726.x
  • Ecology Letters
    2005

    Soil community composition drives aboveground plantherbivoreparasitoid interactions

    T. Martijn Bezemer, Gerlinde De Deyn, T.M. Bossinga, Nicole M. van Dam, Jeff A. Harvey, Wim H. van der Putten
    Soil organisms can influence higher trophic level aboveground organisms, but only very few studies have considered such effects. We manipulated soil community composition of model grassland ecosystems by introducing nematode communities, microorganisms, neither or both groups. Above ground, aphids (Rhopalosiphum padi) and parasitoids (Aphidius colemani) were introduced, and we measured individual performance and population dynamics of plants, aphids and parasitoids. In microcosms with nematode inoculations either with or without microorganism inoculation, aphids offspring production was significantly reduced by 31%. Aphid populations on both host plants Agrostis capillaris and Anthoxanthum odoratum were lowest in microcosms with combined nematode and microorganism inoculations. Opposite results were found for parasitoids. While the number of emerged parasitoids did not differ between treatments, parasitoid mortality and the proportion of males were significantly lower in microcosms with nematode and microorganism inoculations. Parasitized aphids were significantly larger in microcosms with nematodes inoculated. Plant biomass did not differ, but in the preferred host plant A. odoratum, foliar phenolic content was reduced in the presence of nematodes, and also the concentration of amino acids in the phloem. This study shows that the composition of the soil community matters for aboveground multitrophic interactions. [KEYWORDS: Abovegroundbelowground interactions ; aphid ; Aphidius colemani ; fitness ; herbivory ; microcosm ; nematode ; parasitoid ; Rhopalosiphum padi]
    https://doi.org/10.1111/j.1461-0248.2005.00762.x
  • Journal of Animal Ecology
    2005

    Root herbivore effects on aboveground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality

    1. Plants and insects are part of a complex multitrophic environment, in which they closely interact. However, most of the studies have been focused mainly on bi-tritrophic above-ground subsystems, hindering our understanding of the processes that affect multitrophic interactions in a more realistic framework. 2. We studied whether root herbivory by the fly Delia radicum can influence the development of the leaf feeder Pieris brassicae, its parasitoid Cotesia glomerata and its hyperparasitoid Lysibia nana, through changes in primary and secondary plant compounds. 3. In the presence of root herbivory, the development time of the leaf herbivore and the parasitoid significantly increased, and the adult size of the parasitoid and the hyperparasitoid were significantly reduced. The effects were stronger at low root fly densities than at high densities. 4. Higher glucosinolate (sinigrin) levels were recorded in plants exposed to below-ground herbivory, suggesting that the reduced performance of the above-ground insects was via reduced plant quality. Sinigrin contents were highest in plants exposed to low root fly densities, intermediate in plants exposed to high root fly densities and lowest in plants that were not exposed to root herbivory. 5. Our results show, for the first time, that root herbivory via changes in plant quality can reduce the performance of an above-ground multitrophic level food chain. This underlines the importance of integrating a broader range of above- and below-ground organisms to facilitate a better understanding of complex multitrophic interactions and interrelationships. [KEYWORDS: above–below-ground interactions ; Cotesia glomerata ; Lysibia nana ; Pieris brassicae ; plant–insect interactions]
    https://doi.org/10.1111/j.1365-2656.2005.01006.x
  • Entomologia Experimentalis et Applicata
    2005

    Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity

    Parasitoid wasps have long been considered as model organisms for examining optimal resource allocation to different fitness functions, such as body size and development time. Unlike insect predators, which may need to consume many prey items to attain maturity, parasitoids generally rely on a limited amount of resources that are obtained from a single source (the host). This review discusses a range of ecophysiological constraints that affect host quality and concomitantly the evolution of development strategies in parasitoids. Two macroevolutionary differences in host usage strategies (idiobiosis, koinobiosis) are initially described. Over many years, particular attention has been paid in examining a range of quantitative host attributes such as size, age, or stage, as these affect idiobiont and koinobiont parasitoid development. Parasitoids and their hosts, however, constitute only a small part of an ecological community. Consequently, host quality may be affected by a broad range of factors that may operate over variable spatial and temporal scales. Intimate factors include aggressive competition with other parasitoids and pathogens for access to host resources, whereas less intimate factors include the effects of toxic plant compounds (allelochemicals) on parasitoid performance as mediated through primary and/or secondary hosts. It is suggested that future experiments should increase the levels of trophic complexity as these influence the evolution of life history and development strategies in parasitoids. This includes integration of a suite of direct and indirect mechanisms, including biological processes occurring in different ecological realms, such as above-ground and below-ground interactions. [KEYWORDS: koinobiont ; idiobiont ; host ; life history ; fitness ; development time ; body size ; longevity ; superparasitism ; multiparasitism ; pathogen ; multitrophic ; allelochemical ; secondary ; chemistry ; above-ground interactions ; below-ground interactions]
    https://doi.org/10.1111/j.1570-7458.2005.00348.x
  • Applied Entomology and Zoology
    2005

    Comparing and contrasting life history and development strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera : Ichneumonidae)

    Jeff A. Harvey, L.M.A. Witjes
    Since the concept of the 'niche' was proposed by Hutchinson almost 50 years ago, many researchers have investigated factors that enable species within 'guilds' (i.e., species that exploit a common resource and are likely to compete with one another) to co-exist and to persist. Here, development, host utilization, and life-history characteristics are compared in two species of solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis, attacking pre-pupae of their primary parasitoid host, Cotesia glomerata. More than 80% of the host cocoons presented to L. nana successfully produced adult hyperparasitoids compared with only about 20% for G. agilis. Adult hyperparasitoid body mass increased with host mass, but there was little difference in the mean overall body mass of either species. However, egg-to-adult development time for L. nana was significantly less than that for G. agilis. When provided with unlimited food (honey solution), G. agilis had a lifespan that was almost twice that of L. nana. However, dissections of the ovaries of adult wasps at death revealed that L. nana usually had accumulated more than 20 mature eggs, whereas G. agilis was effectively sterile. We suggest that several eco-physiological factors, as well as differing degrees of specialization amongst the guild of secondary hyperparasitoids attacking C glomerata cocoons, enable them to successfully co-exist in nature. [KEYWORDS: competition ; Cotesia glomerata ; guild ; hyperparasitoid ; niche construction]
    https://doi.org/10.1303/aez.2005.309
  • Ecological Entomology
    2004

    Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size

    Jeff A. Harvey, T. Martijn Bezemer, Jelmer Elzinga, M.R. Strand
    1. Many studies examining the relationship between host size, an index of host quality, and parasitoid fitness use development time and/or adult parasitoid size as currencies of fitness, while ignoring pre-adult mortality. Because the physiological suitability of the host may vary in different stages, sizes, or ages of hosts, a misleading picture of host quality may therefore be obtained in cases where fitness is based on only one or two developmental traits. 2. The development of the solitary koinobiont endoparasitoid Microplitis demolitor is examined in different larval age-classes of its host the soybean looper Pseudoplusia includens. Hosts were parasitised on days 1-8 after hatching from the egg, and development time, adult body size, and mortality of the parasitoid were compared. 3. A comparison of larval growth trajectories (using dry body mass) of M. demolitor revealed that parasitoid larvae attained over twice as much body mass in old hosts than in younger hosts. Similarly, adult parasitoid size at eclosion generally increased with host size, although parasitoids developing in smaller hosts lost a much lower proportion of mass between pupation and eclosion. 4. Overall egg-to-adult development was most rapid in intermediate-aged hosts, and longer in hosts at opposite ends of the age continuum. Moreover, parasitoid mortality varied non-linearly with host stage, and was generally higher in very young and older hosts. 5. Based on these results and other empirical data for koinobionts, it is argued that fitness functions in this group of parasitoids are not simply a positive function of host size or age, but instead may be distinctly dome-shaped, both patterns reflecting the degree of physiological and nutritional compatibility between the two organisms. [KEYWORDS: Development time ; host quality ; koinobiont ; Microplitis ; demolitor ; parasitoid ; Pseudoplusia ; includens size]
    https://doi.org/10.1111/j.0307-6946.2004.00568.x
  • Basic and Applied Ecology
    2004

    Trophic interactions in a changing world

    Wim H. van der Putten, P.C. de Ruiter, T. Martijn Bezemer, Jeff A. Harvey, M.J. Wassen, V. Wolters
    Across the biosphere, rapid and accelerating changes in land use, climate and atmospheric composition driven primarily by anthropogenic forces are known to exert major influences on the productivity, biodiversity and sustainable provision of ecosystem goods and services. Thus far, many studies assessing the ecological consequences of global change have focussed on single trophic levels. However, understanding these changes and predicting their consequences may benefit from unravelling how interactions between primary producers, primary, and secondary consumers (plants, herbivores and carnivores) are being affected. Conservation and restoration may be improved when assessing species and their interactions on appropriate scales, while acknowledging that above- and belowground biota are ecologically linked. Selection pressures on one species may depend on others, so that species loss means more for diversity than just loss of a single taxon. It may also result in the loss of other species of the same or different trophic levels and in the dilution, or even loss, of various selection pressures. We review a number of discussions on trophic interactions in a changing world in relation to (i) the scale of ecosystem response to environmental change with emphasis on the soil subsystem, (ii) the linkage of above- and belowground subsystems and (iii) natural selection and the stability of community structure and ecosystem functioning. We discuss the need to bring together isolated sub-disciplines of ecology in order to understand the implications of global changes for ecosystem processes. [KEYWORDS: Biodiversity; Global human-induced changes; Trophic level communities; Foodweb; Stablility; Ecosystem services; Sustainable land use; Above–belowground interactions]
    https://doi.org/10.1016/j.baae.2004.09.003
  • Environmental Entomology
    2004

    Development of hyperparasitoid wasp Lysibia nana (Hymenoptera: Ichneumonidae) in a multitrophic framework

    Jeff A. Harvey, L.M.A. Witjes, Roel Wagenaar
    Lysibia nana Gravenhorst (Hymenoptera: Ichneumonidae) is a solitary hyperparasitoid that attacks newly cocooned prepupae and pupae of braconid wasps in the subfamily Microgastrinae. One of its preferred hosts is Cotesia glomerata L. (Hymenoptera: Braconidae), a gregarious endoparasitoid of white butterfly caterpillars that feed exclusively on plants producing partly inducible glycoside toxins known as glucosinolates. Here, adult body size, egg-to-adult developmental time, and developmental mortality were compared in L. nana reared from prepupae of C. glomerata (the “primary host”) emerging from larvae of Pieris rapae (L.) and Pieris brassicae (L.) (Lepidoptera: Pieridae) that were in turn maintained on two related crucifers, Brassica oleracea L. and Brassica nigra L. (Brassicaceae). Moreover, offspring sex ratio of L. nana reared in the laboratory was compared with that of field populations of C. glomerata reared on P. brassicae. Hyperparasitoids attained larger mass when “originating” from P. brassicae than P. rapae, a pattern that closely reflected host quality for C. glomerata. However, for a given host cocoon mass at parasitism, hyperparasitoid mass was greater on P. brassicae reared from B. oleracea than from B. nigra. Developmental time was more uniform across the different species combinations. Sex ratios in L. nana were higher than in C. glomerata, irrespective of the secondary (herbivore) host. Our results suggest that plant and herbivore quality are important factors affecting the development of L. nana as mediated through the primary parasitoid host. Consequently, both qualitative and quantitative constraints characterize interactions among L. nana and lower trophic levels. [KEYWORDS: host quality ; hyperparasitoid ; idiobiont ; parasitoid]
    https://doi.org/10.1603/0046-225X-33.5.1488
  • Entomologia Experimentalis et Applicata
    2003

    Second and third trophic level effects of differences in plant species reflect dietary specialisation of herbivores and their endoparasitoids

    B. Sznajder, Jeff A. Harvey
    In natural populations, plants demonstrate an array of indirect and direct defence strategies that help to protect them from their herbivores and pathogens. Indirect defences include the release of odours that attract the natural enemies of herbivores, whereas direct defences may include the production of secondary compounds, allelochemicals that impair herbivore development or repel herbivore attack. Although both strategies have been well studied independently, comparatively little attention has been paid to examining the conflict that may arise between indirect and direct defences, such as when the performance of 'recruited' parasitoids or predators is negatively affected by plant allelochemicals. Here, we examine the growth and development of polyphagous and oligophagous folivores and their respective endoparasitoids on three crucifer species. One of the species, Brassica oleracea, was recently cultivated, whereas populations of B. nigra and Barbarea vulgaris occur naturally. Additionally, these species possess contrasting life-history patterns and are also known to exhibit differences in secondary chemistry. The development of the generalist herbivore-parasitoid system was much more variable over the three crucifers than that exhibited by the specialists. Moreover, generalist herbivore and/or parasitoid fitness-related traits (survival, development time, pupal, or adult size) were much more negatively affected on the wild crucifers than in the specialist association. Our results suggest that the relative importance of direct and indirect defences in plants may rest on the degree of dietary specialisation exhibited by herbivores and their natural enemies, and on the level of toxicity in the plant species under investigation [KEYWORDS: allelochemical parasitoid Spodoptera exigua Cotesia marginiventris Pieris brassicae Cotesia glomerata host quality Lepidoptera Noctuidae Pieridae Hymenoptera Braconidae]
    https://doi.org/10.1046/j.1570-7458.2003.00096.x
  • Basic and Applied Ecology
    2003

    Interactions between aboveground and belowground induced responses against phytophages

    Since their discovery about thirty years ago, induced plant responses have mainly been studied in interactions of plants with aboveground (AG) pathogens, herbivores and their natural enemies. Many induced responses, however, are known to be systemic and thus it is likely that responses induced by AG phytophages affect belowground (BG) phytophages feeding on the same plant, and vice versa. The awareness that interactions between AG and BG phytophages may be an important aspect in the evolution of induced responses came only recently and little research has been done to date. In this review we first summarise ecological studies that show how AG phytophages may affect BG phytophages, and vice versa. Then we focus on mechanisms governing interactions between AG and BG induced responses, such as cross-talk between signals. We chose the genus Nicotiana and the family Brassicaceae as two examples of plant groups that have been well studied for their induced responses both AG and BG – but not in concert – and explore how interactions between AG and BG induced compounds may link multitrophic interactions associated with these plants. We propose that future research on AG and BG interactions should focus on: 1). Identification of compounds and signalling pathways involved in AG and BG induced responses and analysis of their interaction mechanisms, 2). Evaluation of how induced responses affect interactions between BG and AG phytophages and their natural enemies, 3). Evaluation of the effects of AG and BG phytophages -in combination with their natural enemies- on plant fitness to identify keystone interactions that are driving the natural selection for induced responses in plants. Seit ihrer Entdeckung vor ca. dreißig Jahren werden induzierte pflanzliche Antworten der Pflanzen zumeist mit solchen Pathogenen, Herbivoren und deren natürlichen Feinden untersucht, die an oberirdischen Pflanzenteilen zu finden sind. Viele induzierte Antworten der Pflanzen können aber systemisch sein. Daher ist es wahrscheinlich, dass pflanzliche Antworten, die durch oberirdische Organismen induziert werden, auch solche Phytophagen beeinflussen, die unterirdisch an der Pflanze fressen, und umge [KEYWORDS: ecological costs; induced volatiles; insect herbivores; multitrophic interactions; mycorrhizal fungi; nematodes; pathogens; parasitoids; signal cross-talk; trade-offs]
    https://doi.org/10.1078/1439-1791-00133
  • Entomologia Experimentalis et Applicata
    2003

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

    Jelmer Elzinga, Jeff A. Harvey, Arjen Biere
    Gregarious koinobiont parasitoids attacking a range of host sizes have evolved several mechanisms to adapt to variable host resources, including the regulation of host growth, flexibility in larval development rate, and adjustment of clutch size. We investigated whether the first two mechanisms are involved in responses of the specialist gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) to differences in the larval weight and parasitoid load of its host Hadena bicruris Hufn. (Lepidoptera: Noctuidae). In addition, we examined the effects of parasitism on food consumption by the host. Parasitoids were offered caterpillars of different weight from all five instars, and parasitoid fitness correlates, including survival, development time, and cocoon weight, were recorded. Furthermore, several host growth parameters and food consumption of parasitized and unparasitized hosts were measured. Our results show that M. tristis responds to different host weights by regulating host growth and by adjusting larval development rate. In hosts with small weights, development time was increased, but the increase was insufficient to prevent a reduction in cocoon weight, and as a result parasitoids experienced a lower chance of successful eclosion. Cocoon weight was negatively affected by parasitoid load, even though host growth was positively affected by parasitoid load, especially in hosts with small weights. Later instars were more optimal for growth and development of M. tristis than early instars, which might reflect an adaptation to the life-history of the host, whose early instars are usually concealed and inaccessible for parasitism on its food plant, Silene latifolia Krause (Caryophyllaceae). Parasitism by M. tristis greatly reduced total host food consumption for all instar stages. Whether plants can benefit directly from the attraction of gregarious koinobiont parasitoids of their herbivores is a subject of current debate. Our results indicate that, in this system, the attraction of a gregarious koinobiont parasitoid can directly benefit the plant by reducing the number of seeds destroyed by the herbivore
    https://doi.org/10.1046/j.1570-7458.2003.00072.x
  • Physiological Entomology
    2003

    Effect of biotic and abiotic factors on reproductive parameters of the synovigenic endoparasitoid Venturia canescens

    P.A. Eliopoulos, Jeff A. Harvey, C.G. Athanassiou, G.J. Stathas
    The main effects and interactions of adult age, access to food and host deprivation, on the egg load of Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae), a larval parasitoid of Ephestia kuehniella (Lepidoptera: Pyralidae) and other pyralids, were studied in the laboratory. Intraspecific variation in the number of ovarioles was also studied. There was a positive and significant correlation between wasp size and both egg load and ovariole number, with the reproductive system of large wasps containing significantly more ovarioles and mature eggs than small wasps. Newly emerged adult wasps contained 27 ± 2.4 ovulated (mature) eggs in their lateral oviducts. Access to food and host deprivation were the only conditions under which egg load increased with parasitoid age. Wasps that had access to hosts immediately after emergence showed a significant decline in their egg complement, irrespective of food presence. Under conditions of both host and food deprivation, there was practically no alteration of egg load with parasitoid age. A three-way analysis of variance revealed that egg load varies significantly with food or host access but not with parasitoid age. All interactions among the three factors were significant. It is confirmed that there is no egg resorption in V. canescens and that egg production stops in the absence of food
    https://doi.org/10.1111/j.1365-3032.2003.00341.x
  • European Journal of Entomology
    2003

    Sexual size and development time dimorphism in a parasitoid wasp: an exception to the rule?

    Jeff A. Harvey, M.R. Strand
    Sexual dimorphisms in adult size (SSD) and development time (SDTD) occur in many groups of organisms. In insects, some of the best examples occur in parasitoid wasps where most studies report that females are larger than males but take longer to develop. Sex-specific differences in the effects of size on reproductive success is generally regarded as the main factor responsible for SSD in parasitoids. Most studies also assume that development time must be extended in order to achieve larger size. Here, SSD and SDTD were compared in the solitary endoparasitoid, Microplitis mediator that develops in larvae of the moth Pseudoplusia includens. The relationship between male and female body size and development time were isometric in M. mediator, but contradict most predictions of parasitoid development models. Across first to fourth instars at parasitism, male wasps were consistently larger than females but completed their development significantly faster. The longer development time in female wasps was due primarily to an extended pupal phase, whereas the duration of larval development did not vary significantly with offspring sex. Secondary sex ratios (percentage male) also did not vary with host instar. We conclude that SSD in M. mediator is not only a function of extended development time, but also because of several possible factors: (i) selection favours an increase in male size (relative to female size); (ii) female size is constrained because of predation risk, (iii) as a cost of reducing the cost of inbreeding or (iv) constraints on egg maturation rate. We argue that failure to look carefully at how parasitoids grow can lead to incorrect conclusions about the basis or significance of SSD. [KEYWORDS: Development; parasitoid; sexual dimorphism; Microplitis mediator; Pseudoplusia includens; size]
  • Journal of Animal Ecology
    2003

    Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid

    Jeff A. Harvey, Nicole M. van Dam, R. Gols
    Related plant species with different spatial and/or temporal life-history characteristics often possess differences in secondary chemistry and thus direct defensive capability. These differences are often attributed to a range of divergent selection pressures from herbivores and pathogens. Most studies of insect-plant interactions have examined the effects of plant defence on herbivore performance, with less attention being paid to higher trophic levels, such as parasitoid wasps. Moreover, to date it is not known whether secondary plant compounds may affect organisms in the fourth trophic level. Here, we study interactions in a four-trophic-level system. The development of a solitary secondary hyperparasitoid, Lysibia nana, and its primary endoparasitoid host, Cotesia glomerata, are compared when reared from a primary herbivore host, Pieris brassicae, which was itself reared on two cruciferous plants with contrasting life histories. Whereas L. nana is known to attack the pupae of a number of primary parasitoids in the genus Cotesia, both C. glomerata and P. brassicae are intimately asso Insects were reared from a feral population of the spring perennial, Brassica oleracea, and a naturally occurring population of a summer annual, B. nigra . Like other cruciferous plants, both species are known to produce glycoside toxins (= glucosinolates) after they are attacked by foliar herbivores. However, concentrations of glucosinolates were more than 3.5 times higher in young shoots of B. nigra than in corresponding shoots of B. oleracea . Cocoon weight in C. glomerata was unaffected by the foodplant on which P. brassicae was reared, whereas in 24-h-old host cocoons emerging adult hyperparasitoid body mass increased significantly with cocoon size and wasps were significantly larger, and survived better on B. oleracea than on B. nigra. Moreover, body mass in L. nana was typically larger in young (c. 24 h), than in older (c. 72 h) cocoons of C. glomerata. Egg-to-adult development time in L. nana generally increased with host size an Our results clearly demonstrate that qualitative differences in herbivore diet can differently affect the performance of interacting organisms across several trophic levels, and suggest that bottom-up forces may also play a role in mediating interactions involving plants-herbivores-parasitoids and hyperparasitoids [KEYWORDS: allelochemicals, Brassicaceae, Cotesia glomerata, hyperparasitoid, Lysibia nana, Pieris brassicae]
    https://doi.org/10.1046/j.1365-2656.2003.00722.x
  • Journal of Insect Physiology
    2003

    Cross-protection experiments with parasitoids in the genus Microplitis (Hymenoptera: Braconidae) suggest a high level of specificity in their associated bracoviruses

    K. Kadash, Jeff A. Harvey, M.R. Strand
    The immunological and developmental effects of bracoviruses (BVs) from three parasitoids in the genus Microplitis (Braconidae: Microgastrinae) were compared in the hosts Pseudoplusia includens and Heliothis virescens (Lepidoptera: Noctuidae). Southern blotting experiments indicated that viral DNAs from Microplitis demolitor bracovirus (MdBV) cross-hybridized with viral DNAs from Microplitis croceipes bracovirus (McBV) and Microplitis mediator bracovirus (MmBV) under conditions of high stringency. Injection of calyx fluid plus venom from each parasitoid species dose-dependently delayed development of P. includens and H. virescens. Each virus also inhibited pupation of P. includens but not H. virescens. In situ hybridization experiments indicated that MdBV and McBV persistently infect hemocytes in both hosts while MmBV persistently infects hemocytes in P. includens but not H. virescens. While MdBV infection induced a loss of adhesion by most plasmatocytes, McBV and MmBV infection induced a loss of adhesion in less than 50% of cells. Cross-protection experiments indicated that calyx fluid plus venom from one species usually protected progeny of another species from encapsulation but did not always promote successful development [KEYWORDS: Polydnavirus; Parasite; Encapsulation; Hemocytes; Development]
    https://doi.org/10.1016/S0022-1910(03)00064-7
  • Proceedings of the Royal Society B-Biological Sciences
    2002

    A plant pathogen reduces the enemy-free space of an insect herbivore on a shared host plant

    Arjen Biere, Jelmer Elzinga, S.C. Honders, Jeff A. Harvey
    An important mechanism in stabilizing tightly linked host-parasitoid and prey-predator interactions is the presence of refuges that protect organisms from their natural enemies. However, the presence and quality of refuges can be strongly affected by the environment. We show that infection of the host plant Silene latifolia by its specialist fungal plant pathogen Microbotryum violaceum dramatically alters the enemy-free space of a herbivore, the specialist noctuid seed predator Hadena bicruris, on their shared host plant. The pathogen arrests the development of seed capsules that serve as refuges for the herbivore's offspring against the specialist parasitoid Microplitis tristis, a major source of mortality of H. bicruris in the field. Pathogen infection resulted both in lower host-plant food quality, causing reduced adult emergence, and in twofold higher rates of parasitism of the herbivore. We interpret the strong oviposition preference of H. bicruris for uninfected plants in the field as an adaptive response, positioning offspring on refuge-rich, high-quality hosts. To our knowledge, this is the first demonstration that plant-inhabiting micro-organisms can affect higher trophic interactions through alteration of host refuge quality. We speculate that such interference can potentially destabilize tightly linked multitrophic interactions.
    https://doi.org/10.1098/rspb.2002.2147
  • Ecology
    2002

    The developmental strategies of endoparasitoid wasps vary with host feeding ecology

    Jeff A. Harvey, M.R. Strand
    Among the most important trade-offs in life history evolution is whether to grow larger at the cost of longer development time, or to develop more rapidly at the cost of reduced size. For insect herbivores, resolution of this trade-off is thought to be strongly influenced by feeding ecology and mortality risks. In contrast, how these factors might affect the developmental strategies of third trophic level organisms, like parasitoid wasps, is less understood. To address this question, we compared the development of larval endoparasitoids in the families Ichneumonidae and Braconidae that parasitize larval stage herbivores in the order Lepidoptera. The campoplegine ichneumonid Venturia canescens parasitized concealed hosts and exhibited a developmental strategy that favored progeny size over development time. In contrast, the closely related ichneumonid Campoletis sonorensis parasitized exposed hosts and exhibited the opposite strategy of favoring rapid development time over size. The microgastrine braconid Microplitis croceipes attacks partially concealed hosts and showed evidence of a trade-off between maximizing body size and minimizing development times. These results suggested that parasitoids attacking apparent, foliar-feeding hosts may favor rapid development time over size while parasitoids that attack concealed hosts favor size over development time. A broader survey of the literature supported the trends found in our experimental studies. The braconids and ichneumonids examined in this study also exhibit distinct differences in larval feeding and pupation behavior. These developmental traits did not appear to affect the size–development time continuum. However, these traits may affect the size range of hosts that larval endoparasitoids can successfully exploit. [KEYWORDS: Campoletis sonorensis, development, insect, herbivore, insect, insects, life history, Microplitis croceipes, parasitoid, Venturia canescens.]
    https://doi.org/10.1890/0012-9658(2002)083[2439:TDSOEW]2.0.CO;2
  • Trends in Ecology & Evolution
    2001

    Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists

    Plants function in a complex multitrophic environment. Most multitrophic studies, however, have almost exclusively focused on aboveground interactions, generally neglecting the fact that above- and belowground organisms interact. The spatial and temporal dynamics of above- and belowground herbivores, plant pathogens, and their antagonists, can differ in space and time. This affects the temporal interaction strengths and impacts of above- and belowground higher trophic level organisms on plants. Combining both above- and belowground compartments in studies of multitrophic interactions throughout the life cycle of plants will improve our understanding of ecology and evolution in the real world. [KEYWORDS: Arbuscular mycorrhizal fungi; biological-control; natural enemies; populations; resistance; challenges; responses; evolution; patterns; defense]
    https://doi.org/10.1016/S0169-5347(01)02265-0
  • Nature
    2001

    The natural economy

    Description: Towards the end of On the Origin of Species, Darwin pictures nature's riotous......
    https://doi.org/10.1038/35097209
  • Journal of Insect Behavior
    2001

    Lifetime reproductive success in the solitary endoparasitoid, Venturia canescens

    Jeff A. Harvey, I.F. Harvey, D.J. Thompson
    Parasitoid wasps have long been considered excellent organisms in studies examining the evolution of reproductive and life- history strategies. In examining the lifetime reproductive success of parasitoids in the laboratory, most investigations have provided the insects with excess hosts and food, where they exist in a relatively constraint-free environment. Importantly, these conditions may not accurately reflect the true heterogeneity of natural systems, where suitable hosts and food sources are likely to be limiting. This study examines the influence of differences in host and food availability on reproductive and life-history parameters in an asexual strain of the solitary endoparasitoid, Venturia canescens (Hymenoptera: Ichneumonidae). Lifetime reproductive success in V. canescens was measured in response to temporal variations in host and food (honey solution) access. Cohorts of parasitoids were provided with 200 fifth-instar larvae of the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae), and food for variable periods daily after eclosion. V. canescens is synovigenic, and host-deprived wasps continued to mature eggs over the first few days after eclosion until the egg storage capacity was reached in the oviducts. When these wasps were subsequently provided with hosts, oogenesis resumed and continued until later in adult life. Constantly fed wasps lived longer and produced more progeny than wasps from cohorts which were alternately fed and starved or were starved from eclosion. Moreover, wasps with constant host and food access produced most progeny early in life and usually experienced prolonged periods of postreproductive survival. In contrast, the reproductive period of wasps with limited host access was more evenly distributed throughout the adult life. Consequently, the cumulative progeny production by V. canescens with constant food access was fairly uniform irrespective of host availability. Longevity and fecundity in V canescens were positively correlated with adult size. However, variable host access had little effect on the longevity of wasps which were constantly supplied with honey. Over the first 2 days of adult life, variation in food access also had no effect on progeny production by V canescens. We argue that manipulating temporal host and food access to parasitoids in the laboratory more closely approximates natural conditions, where these resources are likely to be spatially separated. Moreover, our findings suggest that many highly synovigenic parasitoids like V. canescens, which produce microtype (=hydropic) eggs, have a considerably higher reproductive potential than ovary dissections have revealed. Our findings are discussed in relation to life-history evolution in the parasitic Hymenoptera. [KEYWORDS: parasitoid; reproductive success; Venturia canescens; Plodia interpunctella; synovigenic; life-history strategy Size-fitness hypothesis; egg load; parasitoid wasp; clutch size; oviposition decisions; plodia-interpunctella; host availability; hymenoptera; behavior; field]
    https://doi.org/10.1023/A:1012219116341
  • Journal of Animal Ecology
    2001

    Life-history strategies in parasitoid wasps: a comparative analysis of 'ovigeny'

    M.A. Jervis, G.E. Heimpel, P.N. Ferns, Jeff A. Harvey, N.A.C. Kidd
    1. Ecologists concerned with life-history strategies of parasitoid wasps have recently focused on interspecific variation in the fraction of the maximum potential lifetime egg complement that is mature when the female emerges into the environment. Species that have all of this complement mature upon emergence are termed 'pro-ovigenic', while those that do not are termed 'synovigenic'. We document and quantify the diversity of egg maturation patterns among 638 species of parasitoid wasps from 28 families. 2. We test a series of hypotheses concerning variation in 'ovigeny' and likely life- history correlates by devising a quantitative index - the proportion of the maximum potential lifetime complement that is mature upon female emergence. 3. Synovigeny, which we define as emerging with at least some immature eggs, was found to be by far the predominant egg maturation pattern (98.12% of species). Even allowing for some taxonomic bias in our sample of species, pro-ovigeny is rare among parasitoid wasps. 4. There is strong evidence for a predicted continuum in ovigeny index among parasitoid wasps, from pro-ovigenic (ovigeny index = 1) to extremely synovigenic species (ovigeny index = 0). 5. As predicted, synovigenic species are longer-lived than pro- ovigenic ones, and ovigeny index and life span are negatively correlated across parasitoid taxa, suggesting a life span cost of concentrating reproductive effort early in adult life. 6. There is equivocal evidence that host feeding (i.e, consumption of host haemolymph and/or tissues by adult wasps) is confined to synovigenic parasitoid wasps. It is also not certain from our analyses whether host feeding is associated with a relatively low ovigeny index. 7. As predicted, egg resorption capability is concentrated among producers of yolk-rich eggs. Also, the hypothesis that it is associated with a tendency towards a low ovigeny index is supported. Parasitoid species that produce yolk-rich eggs also exhibit a lower ovigeny index than species that produce yolk-deficient eggs. 8. Ovigeny index appears to be linked to parasitoid development mode (koinobiosis-idiobiosis). 9. We conclude that 'ovigeny' is a concept applicable to insects generally. [KEYWORDS: feeding strategies; pro-ovigeny; synovigeny; timing of reproduction Leptopilina-boulardi hymenoptera; host-feeding strategies; egg limitation; reproductive-biology; clutch size; independent contrasts; functional-response; asobara-tabida; drosophila-melanogaster; evolutionary argument]
    https://doi.org/10.1046/j.1365-2656.2001.00507.x
  • Nature
    2000

    Ecological scrabbel played in earnest. Fragile dominion: Complexity and the commons

    It takes no more than a casual observer to notice the many tell-tale signs......
    https://doi.org/10.1038/35009008
  • Ecological Entomology
    2000

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

    1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae. 2. Clutch size of C. glomerata was manipulated artificially, and the relationship between parasitoid burden and the maximum weight of the parasitised host (= host- parasitoid complex) was measured. In both hosts, the maximum complex weight was correlated positively with parasitoid burden. Compared with unparasitised hosts, however, the growth of P. rapae was increased at significantly lower parasitoid burdens than in P. brassicae. Emerging wasp size was correlated negatively with parasitoid burden in both host species, whereas development time was less affected. 3. After larval parasitoid egress, the weight of the host carcass increased slightly, but not significantly, with parasitoid burden, although there was a strong correlation between the proportion of host mass consumed by C. glomerata larvae during development and parasitoid burden. 4. Clutch size was generally correlated positively with instar parasitised in both hosts, and greater in P. brassicae than in P. rapae. Sex ratios were much more female biased in L1 and L2 P, rapae than in all other host classes. Adult parasitoid size was correlated inversely with host instar at parasitism, and wasps emerging from P. brassicae were larger, and completed development faster, than conspecifics emerging from P. rapae. 5. The data reveal that parasitism by C, glomerata has profound species-specific effects on the growth of both host species. Consequently, optimality models in which host quality is often based on host size at parasitism or unparasitised growth potential may have little utility in describing the development of gregarious koinobiont endoparasitoids. The results of this investigation are discussed in relation to the potential effectiveness of gregarious koinobionts in biological control programmes. [KEYWORDS: Cotesia glomerata; development; host quality; host regulation;parasitism; Pieris rapae; Pieris brassicae Acyrthosiphon-pisum homoptera; aphidius-smithi hymenoptera;pieris-brassicae; clutch size; oviposition decisions;reproductive strategy; nutritional ecology; cotesia-glomerata;food budget; pea aphid]
    https://doi.org/10.1046/j.1365-2311.2000.00265.x
  • Nature
    2000

    Competition induces adaptive shifts in caste ratios of a polyembryonic wasp

    Jeff A. Harvey, L.S. Corley, M.R. Strand
    An important transition in insect life-history evolution was the shift from a solitary existence to living in groups comprising specialized castes. Caste-forming species produce some individuals that reproduce and others with worker functions that have few or no offspring. Morphologically specialized castes are well known in eusocial species like ants and termites, but castes have also evolved in less-studied groups like thrips, aphids and polyembryonic wasps. Because selection acts at both the individual and the colony level, ratios of investment in different castes are predicted to vary with environmental factors like competition and resources. However, experimental evidence for adaptive shifts in caste ratios is limited owing to the experimental difficulty of manipulating factors thought to influence caste ratios, and because some species produce behaviourally flexible castes that switch tasks in response to colony needs. Unlike other caste-forming species, the broods of polyembryonic wasps develop clonally, so that increased production of one caste probably results in decreased production of the other. Here we show that the polyembryonic wasp Copidosoma floridanum alters caste ratios in response to interspecific competition. Our results reveal a distinct trade-off by C. floridanum between reproduction and defence, and show experimentally that caste ratios shift in an adaptive manner
    https://doi.org/10.1038/35018074
  • Journal of Insect Physiology
    1999

    Development of the parasitoid, Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation

    Jeff A. Harvey, M.A. Jervis, R. Gols, N. Jiang, Louise E.M. Vet
    Several recent models examining the developmental strategies of parasitoids attacking hosts which continue feeding and growing after parasitism (=koinobiont parasitoids) assume that host quality is a non-linear function of host size at oviposition. We tested this assumption by comparing the growth and development of males of the solitary koinobiont endoparasitoid, Cotesiarubecula, in first (L1) to third (L3) larval instars of its preferred host, Pierisrapae and in a less preferred host, Pierisbrassicae. Beginning 3 days after parasitism, hosts were dissected daily, and both host and parasitoid dry mass was determined. Using data on parasitoid dry mass, we measured the mean relative growth rate of C. rubecula, and compared the trajectories of larval growth of the parasitoid during the larval and pupal stages using non-linear equations. Parasitoids generally survived better, completed development faster, and grew larger in earlier than in later instars of both host species, and adult wasps emerging from P. rapae were significantly larger than wasps emerging from all corresponding instars of P. brassicae. During their early larval stages, parasitoids grew most slowly in L1 P. rapae, whereas in all other host classes of both host species growth to pupation proceeded fairly uniformly. The growth of both host species was markedly reduced after parasitism compared with controls, with the development of P. brassicae arrested at an earlier stage, and at a smaller body mass, than P. rapae. Our results suggest that C. rubecula regulates certain biochemical processes more effectively in P. rapae than in P. brassicae, in accordance with its own nutritional and physiological requirements. Furthermore, we propose that, for parasitoids such as C. rubecula, which do not consume all host tissues prior to pupation, that parasitoid size and host quality may vary independently of host size at oviposition and at larval parasitoid egression.
    https://doi.org/10.1016/S0022-1910(98)00113-9
  • Bulletin of Entomological Research
    1998

    The influence of host quality on progeny and sex allocation in the pupal ectoparasitoid, Muscidifurax raptorellus (Hymenoptera : Pteromalidae)

    Jeff A. Harvey, G.J.Z. Gols
    Muscidifurax raptorellus Kogan Legner is a gregarious pteromalid ectoparasitoid that attacks pupae and pharate adults from several families of the higher Diptera. Egg-to-adult development time, adult parasitoid size and emerging offspring (= secondary) sex ratio of hi. raptorellus were compared with clutch size in two hosts that differed greatly in mass, the small Musca domestica Linnaeus and the larger Calliphora vomitoria Linnaeus. The mean number of emerging parasitoids did not vary significantly with host species, although slightly higher clutch sizes were recorded in C. vomitoria. Irrespective of offspring sex, parasitoids completed development more rapidly in M. domestica than in C. vomitoria. In the small host, the development time and adult size of M. raptorellus were negatively correlated with clutch size. By contrast, female parasitoid size was unaffected by clutch size in the larger host, C. vomitoria. Ln both hosts, female parasitoids were significantly larger than male parasitoids. The secondary sex ratio (percentage males) of emerging parasitoids was significantly lower in C. vomitoria, and varied with clutch size in both hosts. In C. vomitoria, the greatest proportion of females emerged from hosts with the highest clutch sizes, whereas in M. domestica hosts with the highest clutch sizes produced the lowest proportion of female progeny. The results described here show that the development of M, raptorellus is profoundly affected by interspecific differences in host quality. Our results suggest that mating structure and host quality have potentially different effects on sex ratio decisions in M. raptorellus, and perhaps other gregarious parasitoids.
  • Physiological Entomology
    1998

    Nutritional ecology of the interaction between larvae of the gregarious ectoparasitoid, Muscidifurax raptorellus (Hym: Pteromalidae) and its pupal host, Musca domestica (Dipt: Muscidae)

    Jeff A. Harvey, Louise E.M. Vet, N. Jiang, R. Gols
    In this study we examined the relationship between clutch size and parasitoid development of Muscidifurax raptorellus (Hymenoptera: Pteromalidae), a gregarious idiobiont attacking pupae of the housefly, Musca domestica (Diptera: Muscidae). Host quality was controlled in the experiments by presenting female parasitoids with hosts of similar size and age. This is the first study to monitor the development of a gregarious idiobiont parasitoid throughout the course of parasitism. Most female wasps laid clutches of one to four eggs per host, although some hosts contained eight or more parasitoid larvae. In both sexes, parasitoids completed development more rapidly, but emerging adult wasp size decreased as parasitoid load increased. Furthermore, the size variability of eclosing parasitoid siblings of the same sex increased with clutch size. Irrespective of clutch size, parasitoids began feeding and growing rapidly soon after eclosion from the egg and this continued until pupation. However, parasitoids in hosts containing five or more parasitoid larvae pupated one day earlier than hosts containing one to four larvae. The results are discussed in relation to adaptive patterns of host utilization by gregarious idiobiont and koinobiont parasitoids.
    https://doi.org/10.1046/j.1365-3032.1998.232072.x
  • Entomologia Experimentalis et Applicata
    1997

    Venturia canescens parasitizing Galleria mellonella and Anagasta kuehniella: differing suitability of two hosts with highly variable growth potential

    Venturia canescens (Grav.) (Hymenoptera: Ichneumonidae) is a solitary larval koinobiont endoparasitoid, ovipositing in several larval instars of different pyralid moth species that are pests of stored food products. After oviposition, the host larva continues to feed and grow for at least several days, the precise time doing so depending on the stage attacked. We examined the relationship between host stage and body mass on parasitoid development in late second to fifth instars of two hosts with highly variable growth potential: the wax moth, Galleria mellonella (L) and the flour moth, Anagasta kuehniella (Zeller)(Lepidoptera: Pyralidae). G. mellonella is the largest known host of V. canescens, with healthy larvae occasionally exceeding 400mg at pupation, whereas those of A. kuehniella rarely exceed 40 mg at the same stage. Parasitoid survival was generally higher in early instars of G. mellonella than in later instars. By contrast, percentage adult emergence in A. kuehniella was highest in late fifth instar and lowest in late second instar. A. kuehniella was the more suitable host species, with over 45% adult emergence in all instars, whereas in G. mellonella we found less than 35% adult emergence in all instars. Adult parasitoid size increased and egg-to-adult development time decreased in a host size- and instar-specific manner from A. kuehniella. The relationship between host size and stage and these fitness correlates was less clear in G. mellonella. Although both host species were parasitized over a similar range of fresh weights, the suitability weight-range of A. kuehniella was considerably wider than G. mellonella for the successful development of V. canescens. However, in hosts of similar weight under 5 mg when parasitized, larger wasps emerged from G. mellonella than from A. kuehniella. Parasitoid growth and development is clearly affected by host species, and we argue that patterns of host utilization and resource acquisition by parasitoids have evolved in accordance with host growth potential and the nutritional requirements of the parasitoid.
    https://doi.org/10.1046/j.1570-7458.1997.00202.x
  • Ecological Entomology
    1997

    Factors affecting host selection in an insect host-parasitoid interaction

    S.M. Sait, M. Begon, D.J. Thompson, Jeff A. Harvey, R.S. Hails
    1. Many parasitoids can develop successfully in different stages of the same host but the costs of parasitism may vary between the stages. The stage of host attacked has generally been determined when there is no choice, giving a misleading impression of host selection or preference. 2. The rate of parasitism by a solitary endoparasitoid, Venturia canescens, of each larval stage of the Indian meal moth, Plodia interpunctella, was examined with and without a host refuge from parasitism. In addition, when given a choice of host stages, with and without a refuge, the influence of parasitoid age on host selection was examined. 3. Wasps were able to parasitize all except the first instar, but second instars experienced significantly reduced parasitism, in both refuge treatments, compared with third to fifth instars. Whilst parasitoid emergence was always significantly less when all host stages had a refuge, the reduction was only marginally significant when second instars were attacked. 4. When given a choice of second- and fifth-instar larvae, wasps consistently parasitized more fifth instars, both with and without a refuge. Moreover, significantly fewer second-instar larvae were parasitized in the presence of fifth instars than when presented alone to the wasps. This pattern of parasitism was unaffected by the increasing age of the parasitoids. 5. Host selection by V. canescens is discussed in terms of host-parasitoid population dynamics and structure.
    https://doi.org/10.1046/j.1365-2311.1997.t01-1-00051.x
  • Journal of Insect Physiology
    1996

    Venturia canescens parasitizing Galleria mellonella and Anagasta kuehniella: Is the parasitoid a conformer or regulator?

    The effects of parasitism by Venturia canescens (Hymenoptera: Ichneumonidae) on the growth of-Galleria mellonella and Anagasta kuehniella (Lepidoptera: Pyralidae) were examined by measuring the weight gain of hosts parasitized from the late second (LL2) to the fifth (L5) instar, Unparasitized G, mellonella are much larger than A, kuehniella in all corresponding stages of larval development. The development of V. canescens was more successful in A, kuehniella than G, mellonella, because late final instar parasitoids were usually unable to egress from the cuticle of G, mellonella, Parasitized G mellonella larvae (a) show a marked reduction in weight gain, which was more apparent the earlier that parasitism occurred, and (b) left their feeding chambers to spin precocious cocoons just prior to being destroyed by the parasitoid, Weight reduction was also shown by parasitized L2-L4 A, kuekniella compared with controls, although the relationship between host size at parasitism and subsequent weight reduction was not as clear as in G, mellonella. V. canescens was therefore partially able to control host weight gain, which varied between host species, and this control was probably mediated by the parasitoid larva, Although parasitized hosts continued to grow after parasitism, V, canescens clearly arrested the development of the larger host species, G, mellonella at an earlier stage than the smaller host species, A, kuehniella, The results suggest that V. canescens, and perhaps other so-called `conformer' koinobiont endoparasitoids, that exhibit flexible larval growth patterns, may also regulate host growth in response to their own nutritional and physiological requirements. Copyright (C) 1996 Elsevier Science Ltd
    https://doi.org/10.1016/S0022-1910(96)00069-8
  • Functional Ecology
    1996

    Parasitism of baculovirus-infected Plodia interpunctella by Venturia canescens and subsequent virus transmission

    S.M. Sait, M. Begon, D.J. Thompson, Jeff A. Harvey
    1. When parasitoids and pathogens compete for the same host there are often severe costs to the parasitoid. Wasps might be expected, then, to avoid parasitizing pathogen-infected hosts. 2. When the solitary endoparasitoid Venturia canescens was presented with healthy and granulosis virus-infected larvae of the Indian Meal Moth Plodia interpunctella, it did not exhibit any difference in contact or probing behaviour between healthy and infected hosts. 3. However, oviposition behaviour was influenced by the level of infection, with a significant reduction in the number of eggs laid in heavily infected hosts. 4. Transmission of the pathogen did not occur directly through oviposition. However, transmission through contamination of the environment by the parasitoid following oviposition in infected hosts was demonstrated.
    https://doi.org/10.2307/2390168
  • Entomologia Experimentalis et Applicata
    1996

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

    Jeff A. Harvey, D.J. Thompson, T.J. Heyes
    Many endoparasitoids develop successfully within a range of host instars. Parasitoid survival is highest when parasitism is initiated in earlier host instars, due to age-related changes in internal (physiological) host defences. Most studies examining fitness-related costs associated with differences in host instar have concentrated on the parasitoid, ignoring the effects of parasitism on the development of surviving hosts that have encapsulated parasitoid eggs. A laboratory experiment was undertaken examining fitness-related costs associated with encapsulation of Venturia canescens (Hymenoptera: Ichneumonidae) eggs by fifth (L5) instar larvae of Corcyra cephalonica (Lepidoptera: Pyralidae). Growth and development of both host and parasitoid were monitored in C. cephalonica larvae containing 0, 1, 2, or 4 parasitoid eggs. Adult size and fecundity of C. cephalonica did not vary with the number of eggs per host. However, there was a distinct increase in host mortality with egg number, although most parasitoids emerged from hosts containing a single egg. The most dramatic effect on the host was a highly significant increase in development time from parasitism to adult eclosion, with hosts containing 4 parasitoid eggs taking over 2.5 days longer to complete development than unparasitized larvae. The egg-to-adult development time and size of adult V. canescens did not vary with egg number per host, as demonstrated in a previous experiment using a different host (Plodia interpunctella). The results described here show that there are fitness-related costs to the host associated with resistance to parasitism.
  • Entomologia Experimentalis et Applicata
    1995

    The effect of host nutrition on growth and development of the parasitiod wasp Venturia-Canescens

    Jeff A. Harvey, I.F. Harvey, D.J. Thompson
    We investigated the effect of host (Plodia interpunctella; Lepidoptera: Pyralidae) nutritional status on development of the solitary endoparasitoid, Venturia canescens (Hymenoptera: Ichneumonidae). Parasitoids from 3rd (L3) instars reared on a deficient diet during early parasitism took longer to develop and suffered higher mortality than those reared from hosts fed ad libitum although there was not a significant difference in the size of eclosing wasps from the two groups. L5 hosts reared at high density produced smaller parasitoids, which developed more rapidly than those reared from hosts from low density containers, although mortality was higher in the latter. In a separate experiment we starved groups of 10-20 hosts (parasitized as L3) daily beginning on the 4th day after parasitism, to determine the host developmental stage required for successful parasitoid development to eclosion. Parasitoid survivorship increased with length of host access to food, while the egg-to-adult parasitoid development time increased throughout the experiment. Parasitoid size decreased with increasing periods of host starvation. The successful emergence of Venturia depends upon Plodia reaching the size normally attained in the mid-5th instar, or 50-70% of the mass of healthy late 5th instars. Our results show that when earlier instars are parasitized, host growth is essential for successful parasitoid development to eclosion. Furthermore, they suggest that, for many koinobionts, host suitability may be greatly influenced by feeding rate and food quality.
  • Entomophaga
    1995

    Host behaviour and its influence on foraging and acceptance by the solitary parasitoid wasp, Venturia canescens (Hym: Ichneumonidae)

    Jeff A. Harvey, D.J. Thompson
    Behavioural interactions between the solitary koinobiont parasitoid, Venturia canescens, and two of its hosts, Plodia interpunctella and Corcyra cephalonica, were investigated. The response of both hosts to simulated antennation using a two-haired brush was examined over instars 3 (L3) to 5 (L5). Young P. interpunctella larvae predominantly adopted escape tactics (writhe, trash) whereas L5 P. interpunctella usually froze after the stimulus was applied. L3 C. cephalonica larvae were more aggressive (headrear, flick) than P. interpunctella in response to the application of the stimulus, but older C. cephalonica responded less aggressively than in earlier instars. Although V. canescens readily jabbed its ovipositor at both hosts after antennation, P. interpunctella was considerably more susceptible to parasitoid attack than C. cephalonica, irrespective of size in the final (L5) instar. C. cephalonica, the larger, more aggressive host, actively resisted parasitism whereas P. interpunctella responded much more passively after parasitoid contact. Parasitoids examined and jabbed their ovipositors at dead hosts, but this behaviour was not sustained, implying that host movement stimulates parasitoid attack. On patches containing V. canescens, L5 C. cephalonica and P. interpunctella, most P. interpunctella larvae responded by freezing after parasitoid contact. P. interpunctella that froze usually avoided parasitism, whereas larvae that attempted to escape by crawling were pursued with vigour by V. canescens and usually parasitized. Irrespective of behaviour after parasitoid contact, C. cephalonica displayed more aggressive behaviour and had much greater success iri warding off parasitoid attack. Host acceptance by V. canescens is clearly affected by the size and species of the host it attacks. The influence of host defensive behaviour is discussed in relation to the evolution of parasitoid counter-defences and oviposition strategies.
    https://doi.org/10.1007/BF02373068
  • European Journal of Entomology
    1995

    Developmental interactions between the solitary endoparasitoid Venturia-Canescens (Hymenoptera, Ichneumonidae), and 2 of its hosts, Plodia-Interpuncetlla and Corcyra-Cephalonica (Lepidoptera, Pyralidae)

    Jeff A. Harvey, D.J. Thompson
    Developmental interactions between the solitary koinobiont endoparasitoid Venturia canescens, and two of its hosts, the pyralid moths Plodia interpunctella and Corcyra cephalonica, were investigated. Wasps reared from second (L2) through fifth (L5) instars of Corcyra were larger than those from the corresponding stages of Plodia, but took longer to complete development and generally suffered higher mortality. Starved L5 Plodia of a given mass produced significantly larger wasps than starved L5 Corcyra. Adult wasp size was positively correlated with the number of ovulated eggs in Venturia emerging from both hosts; thus, the larger wasps that emerged from Corcyra had higher egg complements than the smaller wasps from Plodia. The final size of parasitized L2-L4 Corcyra was influenced by Venturia, with all three instars significantly smaller than unparasitized larvae. For Venturia, developmental flexibility and host regulation are important adaptive mechanisms that allow the parasitoid to develop in a wide range of host instars. However, for koinobiont parasitoids differences in the biology of the host species strongly influence their development and fitness.
  • Ecology
    1994

    Flexible larval growth allows use of a range of host sizes by a parasitoid wasp

    Jeff A. Harvey, I.F. Harvey, D.J. Thompson
    Recent optimality models of host-parasitoid associations have assumed that host quality varies with host size or age at parasitism. This is based on the fact that larger hosts provide more resources, making size a reliable indicator of the amount of resources available for parasitoid development. Few studies have examined this in parasitoids that allow their hosts to continue development after parasitism (koinobiont parasitoids). In this study we compared growth trajectories of the koinobiont ichneumonid endoparasitoid Venturia canescens developing in four larval instars of one of its hosts, the moth Plodia interpunctella. Hosts were reared with excess food and parasitized as late second, third, fourth, and fifth instars. Hosts were dissected at intervals after parasitism, and host and parasitoid dry mass determined. The survivorship, development time, and size of eclosing adult wasps were also monitored. Hosts parasitized by Venturia continued to grow and become prepupae, although their maximum masses were progressively smaller the earlier that the hosts were parasitized: second-instar (L2) hosts grew to 70% of control (unparasitized) size, while L4 and L5 hosts reached control size. The maximum larval dry mass, as well as eclosing adult size, varied with host instar at parasitism. Venturia larvae spent prolonged periods as first instars when developing from L2 hosts and grew most rapidly during early stages in L5 larvae. The data shaw that for Venturia, host duality is not a direct function of host size at parasitism. Furthermore, the pattern of development shown by Venturia differs markedly from that shown by aphidiid koinobiont parasitoids.
    https://doi.org/10.2307/1937465
  • Ecological Entomology
    1993

    The effect of superparasitism on development of the solitary parasitoid wasp, Venturia Canescens (Hymenoptera, Ichneumonidae)

    Jeff A. Harvey, I.F. Harvey, D.J. Thompson
    1. The effects of superparasitism on the rate of development, adult size and mortality of Venturia canescens (Hymenoptera: Ichneumonidae) were investigated. Parasitoids were reared from third (L3) and fifth (L5) instars of one of its hosts, Plodia interpunctella (Lepidoptera: Pyralidae) containing one, two or four parasitoid eggs. 2. Superparasitism increased the development time of Venturia reared from both instars, but the developmental delay was more evident in wasps from L5 hosts. 3. The size of parasitoids from L3 hosts was unaffected by egg number, but wasps from both superparasitized L5 treatments were significantly smaller than those from singly parasitized hosts. 4. Parasitoid mortality was significantly higher in L5 than L3, but within instars did not differ significantly with egg number. 5. The results confirm that superparasitism may affect the fitness of both the adult female wasp and her progeny, and should therefore be incorporated into models of superparasitism as an adaptive foraging strategy.
    https://doi.org/10.1111/j.1365-2311.1993.tb01091.x

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