Publications by authors named "Jeffrey A Harvey"

83 Publications

The Tarnished Silver Lining of Extreme Climatic Events.

Trends Ecol Evol 2021 05 8;36(5):384-385. Epub 2021 Mar 8.

Vrije Universiteit Amsterdam, Department of Ecological Sciences - Animal Ecology, Amsterdam, The Netherlands.

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http://dx.doi.org/10.1016/j.tree.2021.02.005DOI Listing
May 2021

Climate change-mediated temperature extremes and insects: From outbreaks to breakdowns.

Glob Chang Biol 2020 Dec 16;26(12):6685-6701. Epub 2020 Oct 16.

Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.

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.
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http://dx.doi.org/10.1111/gcb.15377DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7756417PMC
December 2020

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

Mol Ecol 2020 10 15;29(20):4014-4031. Epub 2020 Sep 15.

Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.

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.
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http://dx.doi.org/10.1111/mec.15613DOI Listing
October 2020

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

Environ Entomol 2020 08;49(4):924-930

Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands.

In three Dutch populations of the native small hogweed (Heracleum sphondylium L. [Apiales: Apiaceae]), and one of the invasive giant hogweed (H. mantegazzianum Sommeier & 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.
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http://dx.doi.org/10.1093/ee/nvaa052DOI Listing
August 2020

Range-Expansion in Processionary Moths and Biological Control.

Insects 2020 Apr 28;11(5). Epub 2020 Apr 28.

Department of Terrestrial Ecology, Netherlands Institute of Ecology, Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands.

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 () and pine () 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.
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http://dx.doi.org/10.3390/insects11050267DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7290706PMC
April 2020

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

Pest Manag Sci 2020 Jun 31;76(6):2087-2094. Epub 2020 Jan 31.

Department of Entomology, College of Plant Protection, Nanjing Agriculture University, Nanjing, P. R. China.

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 ), 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 enrichment) system, we investigated the effect of elevated CO 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 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  + 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. © 2020 Society of Chemical Industry.
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http://dx.doi.org/10.1002/ps.5747DOI Listing
June 2020

Ramanujan's influence on string theory, black holes and moonshine.

Authors:
Jeffrey A Harvey

Philos Trans A Math Phys Eng Sci 2020 Jan 9;378(2163):20180440. Epub 2019 Dec 9.

Enrico Fermi Institute and Department of Physics, University of Chicago, 5640 Ellis Ave., Chicago, IL 60637, USA.

Ramanujan influenced many areas of mathematics, but his work on -series, on the growth of coefficients of modular forms and on mock modular forms stands out for its depth and breadth of applications. I will give a brief overview of how this part of Ramanujan's work has influenced physics with an emphasis on applications to string theory, counting of black hole states and moonshine. This paper contains the material from my presentation at the meeting celebrating the centenary of Ramanujan's election as FRS and adds some additional material on black hole entropy and the AdS/CFT correspondence. This article is part of a discussion meeting issue 'Srinivasa Ramanujan: in celebration of the centenary of his election as FRS'.
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http://dx.doi.org/10.1098/rsta.2018.0440DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6939228PMC
January 2020

The ecological role of bacterial seed endophytes associated with wild cabbage in the United Kingdom.

Microbiologyopen 2020 01 13;9(1):e00954. Epub 2019 Nov 13.

Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

Endophytic bacteria are known for their ability in promoting plant growth and defense against biotic and abiotic stress. However, very little is known about the microbial endophytes living in the spermosphere. Here, we isolated bacteria from the seeds of five different populations of wild cabbage (Brassica oleracea L) that grow within 15 km of each other along the Dorset coast in the UK. The seeds of each plant population contained a unique microbiome. Sequencing of the 16S rRNA genes revealed that these bacteria belong to three different phyla (Actinobacteria, Firmicutes, and Proteobacteria). Isolated endophytic bacteria were grown in monocultures or mixtures and the effects of bacterial volatile organic compounds (VOCs) on the growth and development on B. oleracea and on resistance against a insect herbivore was evaluated. Our results reveal that the VOCs emitted by the endophytic bacteria had a profound effect on plant development but only a minor effect on resistance against an herbivore of B. oleracea. Plants exposed to bacterial VOCs showed faster seed germination and seedling development. Furthermore, seed endophytic bacteria exhibited activity via volatiles against the plant pathogen F. culmorum. Hence, our results illustrate the ecological importance of the bacterial seed microbiome for host plant health and development.
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http://dx.doi.org/10.1002/mbo3.954DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6957406PMC
January 2020

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

Pest Manag Sci 2020 Feb 4;76(2):432-443. Epub 2019 Dec 4.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.1002/ps.5679DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7004005PMC
February 2020

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

Insects 2019 Sep 24;10(10). Epub 2019 Sep 24.

Department of Terrestrial Ecology, Netherlands Institute of Ecology, Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands.

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--, , or . 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 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 in the case of the manicured agro-ecosystem.
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http://dx.doi.org/10.3390/insects10100314DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6835564PMC
September 2019

Variation in Performance and Resistance to Parasitism of Populations.

Insects 2019 Sep 11;10(9). Epub 2019 Sep 11.

Department of Terrestrial Ecology, Netherlands Institute of Ecology, Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands.

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 populations originating from four continents when feeding on a native Dutch plant species, 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 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 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.
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http://dx.doi.org/10.3390/insects10090293DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6780392PMC
September 2019

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

Oecologia 2019 Oct 24;191(2):261-270. Epub 2019 Jul 24.

Graduate Degree Program in Ecology and Department of Bioagricultural Sciences and Pest Management, Colorado State University, 1177 Campus Delivery, Fort Collins, CO, 80523-1177, USA.

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.
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http://dx.doi.org/10.1007/s00442-019-04470-5DOI Listing
October 2019

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

Ecology 2019 11 20;100(11):e02819. Epub 2019 Aug 20.

Laboratory of Entomology, Wageningen University & Research, Droevendaalsesteeg 1, Wageningen, 6708 PB, The Netherlands.

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.
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http://dx.doi.org/10.1002/ecy.2819DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6899732PMC
November 2019

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

Oecologia 2019 Mar 5;189(3):699-709. Epub 2019 Feb 5.

Laboratory of Entomology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.1007/s00442-019-04352-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6418317PMC
March 2019

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

J Chem Ecol 2018 Oct 31;44(10):894-904. Epub 2018 Jul 31.

Department of Ecological Sciences, Section Animal Ecology, VU University Amsterdam, De Boelelaan 1085, 1081, HV, Amsterdam, The Netherlands.

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.
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http://dx.doi.org/10.1007/s10886-018-0989-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6153775PMC
October 2018

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

Chemoecology 2018 10;28(3):77-89. Epub 2018 May 10.

5Department of Terrestrial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands.

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 (), 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 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 . 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.
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http://dx.doi.org/10.1007/s00049-018-0258-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5988764PMC
May 2018

Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids.

Proc Natl Acad Sci U S A 2018 05 30;115(20):5205-5210. Epub 2018 Apr 30.

Laboratory of Entomology, Wageningen University, 6700 AA Wageningen, The Netherlands;

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.
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http://dx.doi.org/10.1073/pnas.1717904115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960289PMC
May 2018

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

J Anim Ecol 2018 07 14;87(4):1046-1057. Epub 2018 May 14.

Department of Terrestrial Ecology, Netherlands Institute of Ecology, Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.1111/1365-2656.12835DOI Listing
July 2018

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

Bioscience 2018 Apr 28;68(4):237. Epub 2018 Mar 28.

Department of Meteorology and Atmospheric Science at Pennsylvania State University, in University Park.

[This corrects the article DOI: 10.1093/biosci/bix133.].
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http://dx.doi.org/10.1093/biosci/biy033DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5894075PMC
April 2018

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

Bioscience 2018 Apr 29;68(4):281-287. Epub 2017 Nov 29.

Department of Meteorology and Atmospheric Science at Pennsylvania State University, in University Park.

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.
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http://dx.doi.org/10.1093/biosci/bix133DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5894087PMC
April 2018

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

J Insect Physiol 2018 May - Jun;107:110-115. Epub 2018 Mar 16.

Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 4, 6708 PB Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.1016/j.jinsphys.2018.03.006DOI Listing
September 2019

Oviposition Preference for Young Plants by the Large Cabbage Butterfly (Pieris brassicae ) Does not Strongly Correlate with Caterpillar Performance.

J Chem Ecol 2017 Jun 15;43(6):617-629. Epub 2017 Jun 15.

Laboratory of Entomology, Wageningen University and Research, Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.1007/s10886-017-0853-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501907PMC
June 2017

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

R Soc Open Sci 2017 Mar 22;4(3):160815. Epub 2017 Mar 22.

Chemistry Research Unit, Center of Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service , United States Department of Agriculture , 1600 SW 23rd Drive, Gainesville, FL 32608, USA.

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 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.
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http://dx.doi.org/10.1098/rsos.160815DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383825PMC
March 2017

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.

Insect Sci 2018 Aug 8;25(4):690-702. Epub 2017 May 8.

Department of Mathematical Sciences, Centre for Invasion Biology, Stellenbosch University, Matieland, South Africa.

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.
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http://dx.doi.org/10.1111/1744-7917.12439DOI Listing
August 2018

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

J Insect Physiol 2017 04 23;98:134-140. Epub 2016 Dec 23.

Laboratory of Entomology, Wageningen University, Droevendaasesteeg 1, 6700 EH Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.1016/j.jinsphys.2016.12.003DOI Listing
April 2017

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

Chemoecology 2016 6;26(6):219-233. Epub 2016 Oct 6.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands ; Department of Ecological Sciences, Section Animal Ecology, VU University, Amsterdam, The Netherlands.

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 () herbivory on the performance of an aboveground herbivore () and its endoparasitoid wasp (). Insects were reared on three populations of wild cabbage () 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.
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http://dx.doi.org/10.1007/s00049-016-0222-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5063910PMC
October 2016

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

J Chem Ecol 2016 Oct;42(10):1099

Plant Ecology, University of Tübingen, Auf der Morgenstelle 3, 72076, Tübingen, Germany.

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http://dx.doi.org/10.1007/s10886-016-0773-0DOI Listing
October 2016

Integrating Insect Life History and Food Plant Phenology: Flexible Maternal Choice Is Adaptive.

Int J Mol Sci 2016 Aug 3;17(8). Epub 2016 Aug 3.

Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.

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.
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http://dx.doi.org/10.3390/ijms17081263DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5000661PMC
August 2016