Louise Vet

Em. Prof. dr. Louise Vet

Researcher

Bezoekadres

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

Netwerk

Over

Former-director (1999-2019) of the Netherlands Institute of Ecology (NIOO-KNAW), and emeritus professor in Evolutionary Ecology at Wageningen University.

Biografie

Louise E.M. Vet is former-director (1999-2019) of the Netherlands Institute of Ecology (NIOO-KNAW), and professor in Evolutionary Ecology at Wageningen University. Vet was awarded several international prizes for her research on multitrophic interactions, delivering basic knowledge for the sustainable development of agro-ecosystems (e.g. British Rank Prize in Nutrition). Vet is an elected member of the Royal Netherlands Academy of Arts and Sciences.
In addition to her research, Louise Vet actively disseminates the great importance of ecological knowledge for a sustainable economy to politicians, business, and the public. She is known as a fervent proponent of nature-based integral sustainability principles (regarding energy, circularity, and biodiversity), which she herself has put into practice when building the prize-winning sustainable NIOO laboratory-office complex in Wageningen, for which she received the 2012 Golden Pyramid state prize for excellence in commissioning work in architecture.
Vet serves on a diversity of national and international boards and committees. Selection: Urgenda; Circle-economy; Commonland; DOB-Ecology; WWF-NL. In addition, Vet initiated and is chairing a broad societal coalition of scientists, nature organizations, farmers and companies to bend the curve of biodiversity decline (Deltaplan Biodiversiteitsherstel). She provides scientific advice to the European Commission through the European Academies Science Advisory Council.
In December 2017 she was awarded the highest honour of the British Ecological Society. This Honorary Membership recognises exceptional contributions at international level to the generation, communication and promotion of ecological knowledge and solutions.
In 2018 she was elected number 1 in the Sustainable 100, the annual list of the Netherlands' "greenest thinkers and doers".
Upon her step-down as director of NIOO on October 31, 2019 she received the distinction of Knight in the Order of the Lion of the Netherlands, one of the highest royal decorations.

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Employment

  • 1999–2019
    Director Netherlands Institute of Ecology (NIOO-KNAW)
  • 2019–Present
    Guest researcher
  • 1997–Present
    Professor in Evolutionary Ecology (WUR)

Nevenfuncties

Publicaties

Peer-reviewed publicaties

  • Water Research
    15-05-2023

    Enhancing phosphorus removal of photogranules by incorporating polyphosphate accumulating organisms

    Lukas M. Trebuch, Jasper Sohier, Sido Altenburg, Ben Oyserman, Mario Pronk, Marcel Janssen, Louise E.M. Vet, René H. Wijffels, Tania Vasconcelos Fernandes

    Photogranules are a novel wastewater treatment technology that can utilize the sun's energy to treat water with lower energy input and have great potential for nutrient recovery applications. They have been proven to efficiently remove nitrogen and carbon but show lower conversion rates for phosphorus compared to established treatment systems, such as aerobic granular sludge. In this study, we successfully introduced polyphosphate accumulating organisms (PAOs) to an established photogranular culture. We operated photobioreactors in sequencing batch mode with six cycles per day and alternating anaerobic (dark) and aerobic (light) phases. We were able to increase phosphorus removal/recovery by 6 times from 5.4 to 30 mg/L/d while maintaining similar nitrogen and carbon removal compared to photogranules without PAOs. To maintain PAOs activity, alternating anaerobic feast and aerobic famine conditions were required. In future applications, where aerobic conditions are dependent on in-situ oxygenation via photosynthesis, the process will rely on sunlight availability. Therefore, we investigated the feasibility of the process under diurnal cycles with a 12-h anaerobic phase during nighttime and six short cycles during the 12 h daytime. The 12-h anaerobic phase had no adverse effect on the PAOs and phototrophs. Due to the extension of one anaerobic phase to 12 h the six aerobic phases were shortened by 47% and consequently decreased the light hours per day. This resulted in a decrease of phototrophs, which reduced nitrogen removal and biomass productivity up to 30%. Finally, we discuss and suggest strategies to apply PAO-enriched photogranules at large-scale.

    https://doi.org/10.1016/j.watres.2023.119748
  • ISME Journal
    30-03-2023

    High resolution functional analysis and community structure of photogranules

    Lukas M. Trebuch, Olivia M. Bourceau, Stijn M. F. Vaessen, Thomas R. Neu, Marcel Janssen, Dirk de Beer, Louise E.M. Vet, René H. Wijffels, Tania Vasconcelos Fernandes
    Photogranules are spherical aggregates formed of complex phototrophic ecosystems with potential for “aeration-free” wastewater treatment. Photogranules from a sequencing batch reactor were investigated by fluorescence microscopy, 16S/18S rRNA gene amplicon sequencing, microsensors, and stable- and radioisotope incubations to determine the granules’ composition, nutrient distribution, and light, carbon, and nitrogen budgets. The photogranules were biologically and chemically stratified, with filamentous cyanobacteria arranged in discrete layers and forming a scaffold to which other organisms were attached. Oxygen, nitrate, and light gradients were also detectable. Photosynthetic activity and nitrification were both predominantly restricted to the outer 500 µm, but while photosynthesis was relatively insensitive to the oxygen and nutrient (ammonium, phosphate, acetate) concentrations tested, nitrification was highly sensitive. Oxygen was cycled internally, with oxygen produced through photosynthesis rapidly consumed by aerobic respiration and nitrification. Oxygen production and consumption were well balanced. Similarly, nitrogen was cycled through paired nitrification and denitrification, and carbon was exchanged through photosynthesis and respiration. Our findings highlight that photogranules are complete, complex ecosystems with multiple linked nutrient cycles and will aid engineering decisions in photogranular wastewater treatment.
    https://doi.org/10.1038/s41396-023-01394-0
  • Biotechnology and Bioengineering
    25-02-2023

    N 2 ‐fixation can sustain wastewater treatment performance of photogranules under nitrogen limiting conditions

    Lukas M. Trebuch, Kobe Schoofs, Stijn M. F. Vaessen, Thomas R. Neu, Marcel Janssen, René H. Wijffels, Louise E.M. Vet, Tania Vasconcelos Fernandes
    Wastewater characteristics can vary significantly, and in some municipal wastewaters the N:P ratio is as low as 5 resulting in nitrogen-limiting conditions. In this study, the microbial community, function, and morphology of photogranules under nitrogen-replete (N+) and limiting (N−) conditions was assessed in sequencing batch reactors. Photogranules under N− condition were nitrogen deprived 2/3 of a batch cycle duration. Surprisingly, this nitrogen limitation had no adverse effect on biomass productivity. Moreover, phosphorus and chemical oxygen demand removal were similar to their removal under N+ conditions. Although performance was similar, the difference in granule morphology was obvious. While N+ photogranules were dense and structurally confined, N− photogranules showed loose structures with occasional voids. Microbial community analysis revealed high abundance of cyanobacteria capable of N2-fixation. These were higher at N− (38%) than N+ (29%) treatments, showing that photogranules could adjust and maintain treatment performance and high biomass productivity by means of N2-fixation.
    https://doi.org/10.1002/bit.28349
  • Ecological Entomology
    2022

    Effects of oviposition in a non-host species on foraging behaviour of the parasitoid Cotesia glomerata

    Jessica de Bruijn, Louise E.M. Vet, Hans M. Smid, Jetske G. de Boer

    Parasitoids lay their eggs in or on a host, usually another insect. During foraging, parasitoids can encounter insects that differ in terms of host suitability and quality. At one extreme end of this spectrum are non-hosts that are unsuitable for offspring development. Non-hosts are generally ignored but parasitization does occur and occasionally also results in egg deposition. Here, the authors investigate how oviposition in a non-host influences subsequent foraging behaviour of a parasitoid and whether this is mediated by learning. The study system consists of the endoparasitoid Cotesia glomerata and the presumed non-host caterpillar Mamestra brassicae. In the presence of Pieris brassicae hosts and/or their traces (frass), C. glomerata inserted its ovipositor into M. brassicae caterpillars. Eggs were deposited, but all eggs disappeared within 96 h, confirming the non-host status of M. brassicae. In contrast to the expectation, there was no memory retention after oviposition in a non-host and parasitoids did not alter their behaviour with respect to non-host contacts and ovipositions. Instead, C. glomerata became more motivated to forage on a non-host infested leaf. The authors propose that egg deposition in non-hosts by C. glomerata might be due to their high egg load, which is thought to make parasitoids less selective on host quality, especially when they have few reproductive opportunities. In such cases, fitness costs to individual females are low. Egg deposition in non-hosts might ultimately lead to host range expansion if parasitoids overcome the defence response of non-hosts over evolutionary time.

    https://doi.org/10.1111/een.13151
  • Communications Biology
    22-01-2021

    Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

    Jérémy Gauthier, Hélène Boulain, Joke Van Vugt, Lyam Baudry, Emma Persyn, Jean-Marc Aury, Benjamin Noel, Anthony Bretaudeau, Fabrice Legeai, Sven Warris, Mohamed A Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, Philippe Gayral, Karine Musset, Thibaut Josse, Diane Bigot, Christophe Bressac, Sébastien Moreau, Georges Periquet, Myriam Harry, Nicolas Montagné, Isabelle Boulogne, Mahnaz Sabeti-Azad, Martine Maïbèche, Thomas Chertemps, Frédérique Hilliou, David Siaussat, Joëlle Amselem, Isabelle Luyten, Claire Capdevielle-Dulac, Karine Labadie, Bruna Laís Merlin, Valérie Barbe, Jetske G. de Boer, Martial Marbouty, Fernando Luis Cônsoli, Stéphane Dupas, Aurélie Hua-Van, Gaelle Le Goff, Annie Bézier, Emmanuelle Jacquin-Joly, James B Whitfield, Louise E.M. Vet, Hans M. Smid, Laure Kaiser, Romain Koszul, Elisabeth Huguet, Elisabeth A Herniou, Jean-Michel Drezen

    Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

    https://doi.org/10.1038/s42003-020-01623-8
  • Behavioral Ecology
    2021

    Memory extinction and spontaneous recovery shaping parasitoid foraging behavior

    Jessica de Bruijn, Louise E.M. Vet, Hans M. Smid, Jetske G. de Boer

    Animals can alter their foraging behavior through associative learning, where an encounter with an essential resource (e.g., food or a reproductive opportunity) is associated with nearby environmental cues (e.g., volatiles). This can subsequently improve the animal's foraging efficiency. However, when these associated cues are encountered again, the anticipated resource is not always present. Such an unrewarding experience, also called a memory-extinction experience, can change an animal's response to the associated cues. Although some studies are available on the mechanisms of this process, they rarely focus on cues and rewards that are relevant in an animal's natural habitat. In this study, we tested the effect of different types of ecologically relevant memory-extinction experiences on the conditioned plant volatile preferences of the parasitic wasp Cotesia glomerata that uses these cues to locate its caterpillar hosts. These extinction experiences consisted of contact with only host traces (frass and silk), contact with nonhost traces, or oviposition in a nonhost near host traces, on the conditioned plant species. Our results show that the lack of oviposition, after contacting host traces, led to the temporary alteration of the conditioned plant volatile preference in C. glomerata, but this effect was plant species-specific. These results provide novel insights into how ecologically relevant memory-extinction experiences can fine-tune an animal's foraging behavior. This fine-tuning of learned behavior can be beneficial when the lack of finding a resource accurately predicts current, but not future foraging opportunities. Such continuous reevaluation of obtained information helps animals to prevent maladaptive foraging behavior.

    https://doi.org/10.1093/beheco/arab066
  • Journal of Animal Ecology
    2021

    Multi‐camera field monitoring reveals costs of learning for parasitoid foraging behaviour

    Jessica de Bruijn, Ilka Vosteen, Louise E.M. Vet, Hans M. Smid, Jetske G. de Boer
    1. Dynamic conditions in nature have led to the evolution of behavioural traits that allow animals to use information on local circumstances and adjust their behaviour accordingly, for example through learning. Although learning can improve foraging efficiency, the learned information can become unreliable as the environment continues to change. This could lead to potential fitness costs when memories holding such unreliable information persist. Indeed, persistent unreliable memory was found to reduce the foraging efficiency of the parasitoid Cotesia glomerata under laboratory conditions.

    2. Here, we evaluated the effect of such persistent unreliable memory on the foraging behaviour of C. glomerata in the field. This is a critical step in studies of foraging theory, since animal behaviour evolved under the complex conditions present in nature.

    3. Existing methods provide little detail on how parasitoids interact with their environment in the field, therefore we developed a novel multi‐camera system that allowed us to trace parasitoid foraging behaviour in detail. With this multi‐camera system, we studied how persistent unreliable memory affected the foraging behaviour of C. glomerata when these memories led parasitoids to plants infested with non‐host caterpillars in a semi‐field set‐up.

    4. Our results demonstrate that persistent unreliable memory can lead to maladaptive foraging behaviour in C. glomerata under field conditions and increased the likelihood of oviposition in the non‐host caterpillar Mamestra brassica. Furthermore, these time‐ and egg‐related costs can be context‐dependent, since they rely on the plant species used.

    5. These results provide us with new insight on how animals use previously obtained information in naturally complex and dynamic foraging situations and confirm that costs and benefits of learning depend on the environment animals forage in. Although behavioural studies of small animals in natural habitats remain challenging, novel methods such as our multi‐camera system contribute to understanding the nuances of animal foraging behaviour.
    https://doi.org/10.1111/1365-2656.13479
  • Microorganisms
    2021

    On-site blackwater treatment fosters microbial groups and functions to efficiently and robustly recover carbon and nutrients

    Eiko Kuramae, Mauricio Rocha Dimitrov, Gustavo Ribeiro da Silva, Adriano Reis Lucheta, L.W. Mendes, Ronildson Lima Luz, Louise E.M. Vet, Tania Vasconcelos Fernandes
    Background: Wastewater is considered as a renewable resource water and energy. An advantage of decentralized sanitation systems is the separation of the blackwater (BW) stream, which is highly contaminated with human pathogens, from the remaining household water. However, the composition and functions of the microbial community in BW are not known. In this study, we used shotgun metagenomics to assess the dynamics of microbial community structure and function throughout a new BW anaerobic digestion system installed at The Netherlands Institute of Ecology. Samples from the influent (BW), primary effluent (anaerobic digested BW), sludge and final effluent of the pilot upflow anaerobic sludge blanket (UASB) reactor and microalgae pilot tubular photobioreactor (PBR) were analyzed.

    Results: Our results showed a decrease in microbial richness and diversity followed by a decrease in functional complexity and co-occurrence along the different modules of the bioreactor. The microbial diversity and function decrease were reflected both changes in substrate composition and wash conditions. The most prevalent core functions in influent (BW) were related to metabolism of carbohydrates, response to chemicals and drugs, and nitrogen. The core functions in anaerobic digested BW and upflow anaerobic sludge blanket reactor were related to response to stress, viral processes and iron-sulfur metabolism. Methanogenesis-related functions were most abundant in upflow anaerobic sludge blanket reactor. Effluent from tubular photobioreactor presented high abundances of functions related to nitrogen utilization, metal ion binding and antibiotic biosynthetic processes. Interestingly, the abundance of sequences related to ‘pathogenesis’ decreased from influent BW to SP1 to effluent from tubular photobioreactor. Our wastewater treatment system also decreased potential microbial functions related to pathogenesis.

    Conclusions: The new sanitation system studied here fosters microbial groups and functions that allow the system to efficiently and robustly recover carbon and nutrients while reducing pathogenic groups, ultimately generating a final effluent safe for discharge and reuse.
    https://doi.org/10.3390/microorganisms9010075
  • Biological Reviews
    12-2020

    Next Generation Biological Control: The Need for Integrating Genetics and Evolution

    Kelley Leung, Erica Ras, Kim Ferguson, Simone Ariëns, Dirk Babendreier Babendreier, Piter Bijma, Kostas Bourtzis, Jacques Brodeur, Margreet Bruins, Alejandra Centurión, Sophie Chattington, Milena Chinchilla-Ramírez, Marcel Dicke, Nina E. Fatouros, Joel González Cabrera, Thomas de Groot, Tim Haye, Markus Knapp, Panagioata Koskinioti, Sophie Le Hesran, Manolis Lirakis, Angeliki Paspati, Meritxell Pérez-Hedo, Wouter Plouvier, Christian Schlötterer, Judith Stahl, Andra Thiel, Alberto Urbaneja, Louis van de Zande, Eveline Verhulst, Louise E.M. Vet, Sander Visser, John Werren, Shuwen Xia, Bas J Zwaan, Sara Magalhães, Leo W. Beukeboom, Bart A. Pannebakker
    Biological control is widely successful for controlling pests, but effective biocontrol agents are now more difficult to obtain due to more restrictive international trade laws. Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genomic approaches. Although they have been underutilised in the past, applying genetic and genomic techniques is becoming more feasible from both technological and economic perspectives. We review current methods and provide a framework for using them, incorporating evolutionary and ecological principles. First, it is necessary to identify which biocontrol trait to select and in what direction. Next, the genes or markers linked to these traits need be determined to better target their selection, followed by how to implement this information into a breeding program. Choosing a trait can be assisted by modelling to account for the proper agro-ecological context, and by knowing which traits have sufficiently high heritability values. We provide guidelines for designing genomic strategies in biocontrol programs, which depends on the organism, budget, and desired objective. Genomic approaches start with genome sequencing and assembly. We provide a guide for deciding the most successful sequencing strategy for biocontrol agents. Gene discovery involves quantitative trait loci (QTL) analyses, transcriptomic and proteomic studies, and gene editing. Improving biocontrol practices include marker-assisted selection, genomic selection and microbiome manipulation of biocontrol agents, and monitoring for genetic variation during rearing and post-release. We conclude by identifying the most promising applications of genetic and genomic methods to improve biological control efficacy.
    https://doi.org/10.20944/preprints201911.0300.v1
  • Water Research
    15-04-2020

    Impact of hydraulic retention time on community assembly and function of photogranules for wastewater treatment

    Lukas M. Trebuch, Ben Oyserman, Marcel Janssen, René H. Wijffels, Louise E.M. Vet, Tania Vasconcelos Fernandes
    Photogranules are dense, spherical agglomerates of cyanobacteria, microalgae and non-phototrophic microorganisms that have considerable advantages in terms of harvesting and nutrient removal rates for light driven wastewater treatment processes. This ecosystem is poorly understood in terms of the microbial community structure and the response of the community to changing abiotic conditions. To get a better understanding, we investigated the effect of hydraulic retention time (HRT) on photogranule formation and community assembly over a period of 148 days. Three laboratory bioreactors were inoculated with field samples from various locations in the Netherlands and operated in sequencing batch mode. The bioreactors were operated at four different HRTs (2.00, 1.00, 0.67, 0.33 days), while retaining the same solid retention time of 7 days. A microbial community with excellent settling characteristics (95–99% separation efficiency) was established within 2–5 weeks. The observed nutrient uptake rates ranged from 24 to 90 mgN L−1 day−1 and from 3.1 to 5.4 mgP L−1 day−1 depending on the applied HRT. The transition from single-cell suspension culture to floccular agglomeration to granular sludge was monitored by microscopy and 16S/18S sequencing. In particular, two important variables for driving aggregation and granulation, and for the structural integrity of photogranules were identified: 1. Extracellular polymeric substances (EPS) with high protein to polysaccharide ratio and 2. specific microorganisms. The key players were found to be the cyanobacteria Limnothrix and Cephalothrix, the colony forming photosynthetic eukaryotes within Chlamydomonadaceae, and the biofilm producing bacteria Zoogloea and Thauera. Knowing the makeup of the microbial community and the operational conditions influencing granulation and bioreactor function is crucial for successful operation of photogranular systems.
    https://doi.org/10.1016/j.watres.2020.115506
  • 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
  • Chemoecology
    2020

    Do plant volatiles confuse rather than guide foraging behavior of the aphid hyperparasitoid Dendrocerus aphidum?

    Jetske G. de Boer, Petra J. Hollander, Divya Jagger, Pim van Sliedregt, Lucia Salis, Martine Kos, Louise E.M. Vet
    Many species of parasitoid wasps use plant volatiles to locate their herbivorous hosts. These volatiles are reliable indicators of host presence when their emission in plants is induced by herbivory. Hyperparasitoids may also use information from lower trophic levels to locate their parasitoid hosts but little is known about the role of volatiles from the plant–host complex in the foraging behavior of hyperparasitoids. Here, we studied how Dendrocerus aphidum (Megaspilidae) responds to plant and host volatiles in a series of experiments. This hyperparasitoid uses aphid mummies as its host and hampers biological control of aphids by parasitoids in greenhouse horticulture. We found that D. aphidum females were strongly attracted to volatiles from mummy-infested sweet pepper plants, but only when clean air was offered as an alternative odor source in the Y-tube olfactometer. Hyperparasitoid females did not have a preference for mummy-infested plants when volatiles from aphid-infested or healthy pepper plants were presented as an alternative. These olfactory responses of D. aphidum were mostly independent of prior experience. Volatiles from the host itself were also highly attractive to D. aphidum, but again hyperparasitoid females only had a preference in the absence of plant volatiles. Our findings suggest that plant volatiles may confuse, rather than guide the foraging behavior of D. aphidum. Mummy hyperparasitoids, such as D. aphidum, can use a wide variety of mummies and are thus extreme generalists at the lower trophic levels, which may explain the limited role of (induced) plant volatiles in their host searching behavior.
    https://doi.org/10.1007/s00049-020-00321-5
  • Resources, Conservation and Recycling
    2020

    From toilet to agriculture

    Afnan Suleiman, Késia Lourenço, C Clark, Ronildson Lima Luz, Gustavo H.R. Silva, Louise E.M. Vet, Heitor Cantarella, Tania Vasconcelos Fernandes, Eiko Kuramae
    Human activities are pushing earth beyond its natural limits, so recycling nutrients is mandatory. Microalgae are highly effective in nutrient recovery and have strong potential as a sustainable wastewater treatment technology. Here, nutrients from black water (toilet wastewater) were recovered as microalgal biomass, which was dried and assessed as a fertilizer in pot experiments compared with inorganic fertilizer. We deciphered the effects of microalgal biomass as a biofertilizer on plant growth and quality and the biological processes linked to greenhouse gas (GHG) emissions. In addition, we elucidated the assembly of the active microbiome in bulk soil and rhizosphere during barley development. Microalgal biomass application and inorganic fertilizer (NPK) resulted in similar plant productivity (16.6 g pot−1). Cumulative nitrous oxide (N2O) emissions were 4.6-fold higher in the treatment amended with microalgal fertilizer (3.1% of applied N) than that with inorganic fertilizer (0.5% of applied N). Nitrification by bacteria was likely the main pathway responsible for N2O emissions (R2 = 0.7, p ≤ 0.001). The application of nitrogen fertilizers affected the structures of both the active bacterial and protozoan communities, but these effects were less obvious than the strong plant effect, as the recruited microbiota varied among different plant developmental stages. Both treatments enriched similar bacterial and protozoan taxonomic orders but with different distributions through time across the plant developmental stages. Furthermore, the bacterial community showed a clear trend of resilience from the beginning of the experiment until harvest, which was not observed for protozoa. Our results indicate that the use of microalgal biomass as a fertilizer is a viable option for recycling nutrients from wastewater into plant production.
    https://doi.org/10.1016/j.resconrec.2020.104924
  • 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
  • 2020

    Integrating biodiversity conservation in wider landscape management: Necessity, implementation and evaluation

    David Kleijn, Koos J.C. Biesmeijer, Raymond Klaassen, Natasja Oerlemans, Ivo Raemakers, Jeroen Scheper, Louise E.M. Vet
    Current conservation instruments, which for most species rely heavily on protected areas, are insufficient to halt biodiversity loss. Conservation initiatives in the wider landscape surrounding protected areas are needed to achieve the impact required for reversing negative biodiversity trends. Focussing on intensively used north-western European landscapes, we present a landscape-level conservation approach that coordinates, integrates and evaluates conservation management by different stakeholders in protected areas, farmland and public space. The starting point is the set of environmental conditions or the habitat characteristics that is needed to realize stable or positive biodiversity trends. Such sets are captured in Key Performance Indicators (KPIs) that can be quantified easily over large areas. Integrated monitoring and evaluation of the relationships between KPIs, management and biodiversity need to be used to validate initial assumptions and continuously improve conservation effectiveness. Evaluation relies on trend monitoring in areas with and without conservation management and extrapolations to landscape-level biodiversity trends based on the total area on which conservation is being implemented. The relationships between biodiversity and KPIs can subsequently be used to develop biodiversity-based business models and to inspire and help stakeholders within and outside these focal areas to actively join the initiative.
    https://doi.org/10.1016/bs.aecr.2020.08.004
  • GCB Bioenergy
    2019

    Serious mismatches continue between science and policy in forest bioenergy

    Michael L Norton, Andras Baldi, Vicas Buda, Bruno Carli, Pavel Cudlin, Mike B. Jones, Atte Korhola, Rajmund Michalski, Francisco Novo, Július Oszlányi, Filpe Duarte Santos, Bernhard Schink, John Shepherd, Louise E.M. Vet, Lars Walloe, Anders Wijkman
    Abstract In recent years, the production of pellets derived from forestry biomass to replace coal for electricity generation has been increasing, with over 10 million tonnes traded internationally?primarily between United States and Europe but with an increasing trend to Asia. Critical to this trade is the classification of woody biomass as ?renewable energy? and thus eligible for public subsidies. However, much scientific study on the net effect of this trend suggests that it is having the opposite effect to that expected of renewable energy, by increasing atmospheric levels of carbon dioxide for substantial periods of time. This review, based on recent work by Europe's Academies of Science, finds that current policies are failing to recognize that removing forest carbon stocks for bioenergy leads to an initial increase in emissions. Moreover, the periods during which atmospheric CO2 levels are raised before forest regrowth can reabsorb the excess emissions are incompatible with the urgency of reducing emissions to comply with the objectives enshrined in the Paris Agreement. We consider how current policy might be reformed to reduce negative impacts on climate and argue for a more realistic science-based assessment of the potential of forest bioenergy in substituting for fossil fuels. The length of time atmospheric concentrations of CO2 increase is highly dependent on the feedstocks and we argue for regulations to explicitly require these to be sources with short payback periods. Furthermore, we describe the current United Nations Framework Convention on Climate Change accounting rules which allow imported biomass to be treated as zero emissions at the point of combustion and urge their revision to remove the risk of these providing incentives to import biomass with negative climate impacts. Reforms such as these would allow the industry to evolve to methods and scales which are more compatible with the basic purpose for which it was designed.
    https://doi.org/10.1111/gcbb.12643
  • Frontiers in Ecology and Evolution
    2019

    Integrating Parasitoid Olfactory Conditioning in Augmentative Biological Control: Potential Impact, Possibilities, and Challenges

    Marjolein Kruidhof, Olga Kostenko, Hans M. Smid, Louise E.M. Vet
    Despite of the vast body of theoretical and empirical literature dealing with parasitoid learning, this knowledge has thus far rarely been exploited for manipulating the efficacy of augmentative biological pest control. This may be due to the fact that most studies on learning behavior were performed under laboratory conditions, whereas field trials remain scarce. However, the few studies that did investigate parasitoid foraging success under (semi-)field conditions show strong learning effects. Using so-called ‘parasitoid olfactory conditioning’ (POC), parasitoids can be trained to become more efficient in the different phases involved in the process of host searching and host acceptance. POC can thus result in a ‘foraging efficacy gain’, defined as the difference between the number of naive and conditioned parasitoids that need to be released to reach a certain parasitization level of the target-pest in the crop environment. This ‘gain’ increases with an improved parasitoid learning ability and depends on the interplay between the parasitoid, crop, target-pest species and parasitoid rearing method. Moreover, the ‘foraging efficacy gain’ depends on the technical implementation of POC, as this will determine the strength, duration and stability of the learning-induced behavioral change. In this perspective paper we will discuss a) the conditions that can enhance the ‘foraging efficacy gain’, b) the possible approaches to implementation of POC and their costs and benefits, and c) a stepwise approach to develop appropriate POC methods for the optimization of biological pest control.
    https://doi.org/10.3389/fevo.2019.00084
  • 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
  • Frontiers in Ecology and Evolution
    2019

    Applying the aboveground-belowground interaction concept in agriculture

    Ciska Veen, Jasper Wubs, Richard D. Bardgett, Edmundo Barrios, Mark Bradford, Sabrina Almeida de Carvalho, Gerlinde De Deyn, Franciska T. De Vries, Ken E. Giller, David Kleijn, Douglas A. Landis, Walter A.H. Rossing, Maarten Schrama, Johan Six, Paul C. Struik, Stijn van Gils, Johannes S.C. Wiskerke, Wim H. van der Putten, Louise E.M. Vet

    Interactions between aboveground and belowground organisms are important drivers of plant growth and performance in natural ecosystems. Making practical use of such above-belowground biotic interactions offers important opportunities for enhancing the sustainability of agriculture, as it could favor crop growth, nutrient supply, and defense against biotic and abiotic stresses. However, the operation of above-and belowground organisms at different spatial and temporal scales provides important challenges for application in agriculture. Aboveground organisms, such as herbivores and pollinators, operate at spatial scales that exceed individual fields and are highly variable in abundance within growing seasons. In contrast, pathogenic, symbiotic, and decomposer soil biota operate at more localized spatial scales from individual plants to patches of square meters, however, they generate legacy effects on plant performance that may last from single to multiple years. The challenge is to promote pollinators and suppress pests at the landscape and field scale, while creating positive legacy effects of local plant-soil interactions for next generations of plants. Here, we explore the possibilities to improve utilization of above-belowground interactions in agro-ecosystems by considering spatio-temporal scales at which aboveground and belowground organisms operate. We identified that successful integration of above-belowground biotic interactions initially requires developing crop rotations and intercropping systems that create positive local soil legacy effects for neighboring as well subsequent crops. These configurations may then be used as building blocks to design landscapes that accommodate beneficial aboveground communities with respect to their required resources. For successful adoption of above-belowground interactions in agriculture there is a need for context-specific solutions, as well as sound socio-economic embedding.

    https://doi.org/10.3389/fevo.2019.00300
  • Ecological Entomology
    2018

    Associative learning of host presence in non-host environments influences parasitoid foraging

    Marjolein de Rijk, V. Cegarra, Hans M. Smid, Bas Engel, Louise E.M. Vet, Erik H. Poelman
    1. Parasitoids are known to utilise learning of herbivore-induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non-suitable herbivores (non-hosts). Simultaneous infestation of plants by hosts and non-hosts has been found to result in induction of HIPVs that differ from host-infested plants. Each non-host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non-host herbivore also contain the host.

    2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non-hosts in the laboratory and in semi-field experiments.

    3. In two-choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant–host–non-host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non-host caterpillar Mamestra brassicae or the non-host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non-host caterpillars or aphids in a semi-field situation.

    4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.
    https://doi.org/10.1111/een.12504
  • Frontiers in Ecology and Evolution
    2018

    Costs of Persisting Unreliable Memory: Reduced Foraging Efficiency for Free-Flying Parasitic Wasps in a Wind Tunnel

    Jessica A.C. de Bruijn, Louise E.M. Vet, Hans M. Smid
    Parasitic wasps are known to improve their foraging efficiency after learning of herbivore-induced plant volatiles (HIPVs) upon encountering their hosts on these plants. However, due to spatial and temporal variation of herbivore communities, learned HIPV cues can become unreliable, no longer correctly predicting host presence. Little is known about the potential fitness costs when memories holding such unreliable information persist. Here we studied how persistent memory, containing unreliable information, affects the foraging efficiency for hosts in Cotesia glomerata. Wasps were conditioned to associate one of two types of HIPVs with either P. brassicae frass, 1 single oviposition in P. brassicae, 3 ovipositions in P. brassicae spaced in time or they were kept unconditioned. The following day, wasps were allowed to forage in a wind tunnel, in an environment that either conflicted or was congruent with their learned plant experience. The foraging environment consisted of host (P. brassicae) and non-host (Mamestra brassicae) infested plants. The conflicting environment had non-hosts on the conditioned plant species and hosts on the non-conditioned plant species, whereas the congruent environment had hosts on the conditioned plant species and non-hosts on the unconditioned plant species. Wasps had to navigate through five non-host infested plants to reach the host-infested plant. Since C. glomerata wasps do not distinguish between HIPVs induced by host and non-host caterpillars, the conflicting foraging situation caused a prediction error, by guiding wasps to non-host infested plants. Especially wasps given 3 spaced oviposition experiences, tested in a conflicting situation, spent significantly more time on non-host infested plants and showed a high tendency to oviposit in the non-hosts. As a result, they took significantly more time to find their hosts. Conditioned wasps, which were tested in a congruent situation, were more responsive than unconditioned wasps, but there was no difference in foraging efficiency between these two groups in the wasps that showed a response. We conclude that persistent memories, such as formed after 3 experiences spaced in time, can lead to maladaptive foraging behavior if the contained information becomes unreliable.
    https://doi.org/10.3389/fevo.2018.00160
  • Journal of Neuroscience Methods
    2018

    Automated high-throughput individual tracking system for insect behavior: Applications on memory retention in parasitic wasps

    Jessica A.C. de Bruijn, Louise E.M. Vet, Maarten A. Jongsma, Hans M. Smid
    Background Insects are important models to study learning and memory formation in both an ecological and neuroscience context due to their small size, behavioral flexibility and ecological diversity. Measuring memory retention is often done through simple time-consuming set-ups, producing only a single parameter for conditioned behavior. We wished to obtain higher sample sizes with fewer individuals to measure olfactory memory retention more efficiently. New method The high-throughput individual T-maze uses commercially available tracking software, Ethovision XT®, in combination with a Perspex stack of plates as small as 18 × 18 cm, which accommodates 36 olfactory T-mazes, where each individual wasp could choose between two artificial odors. Various behavioral parameters, relevant to memory retention, were acquired in this set-up; first choice, residence time, giving up time and zone entries. From these parameters a performance index was calculated as a measure of memory retention. Groups of 36 wasps were simultaneously tested within minutes, resulting in efficient acquisition of sufficiently high sample sizes. Results This system was tested with two very different parasitic wasp species, the larval parasitoid Cotesia glomerata and the pupal parasitoid Nasonia vitripennis, and has proven to be highly suitable for testing memory retention in both these species. Comparison with existing methods Unlike other bioassays, this system allows for both high-throughput and recording of detailed individual behavior. Conclusions The high-throughput individual T-maze provides us with a standardized high-throughput, labor-efficient and cost-effective method to test various kinds of behavior, offering excellent opportunities for comparative studies of various aspects of insect behavior.
    https://doi.org/10.1016/j.jneumeth.2018.09.012
  • 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
  • Current Opinion in Insect Science
    2016

    The complexity of learning, memory and neural processes in an evolutionary ecological context

    Hans M. Smid, Louise E.M. Vet
    The ability to learn and form memories is widespread among insects, but there exists considerable natural variation between species and populations in these traits. Variation manifests itself in the way information is stored in different memory forms. This review focuses on ecological factors such as environmental information, spatial aspects of foraging behavior and resource distribution that drive the evolution of this natural variation and discusses the role of different genes and neural networks. We conclude that at the level of individual, population or species, insect learning and memory cannot be described as good or bad. Rather, we argue that insects evolve tailor-made learning and memory types; they gate learned information into memories with high or low persistence. This way, they are prepared to learn and form memory to optimally deal with the specific ecologies of their foraging environments.
    https://doi.org/10.1016/j.cois.2016.03.008
  • 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
  • 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
  • Environmental Science and Technology
    2015

    Closing Domestic Nutrient Cycles Using Microalgae

    Tania Vasconcelos Fernandes, R. Shrestha, Yixing Sui, Gustavo Papini, Grietje Zeeman, Louise E.M. Vet, René H. Wijffels, Packo Lamers
    This study demonstrates that microalgae can effectively recover all P and N from anaerobically treated black water (toilet wastewater). Thus, enabling the removal of nutrients from the black water and the generation of a valuable algae product in one step. Screening experiments with green microalgae and cyanobacteria showed that all tested green microalgae species successfully grew on anaerobically treated black water. In a
    subsequent controlled experiment in flat-panel photobioreactors, Chlorella sorokiniana was able to remove 100% of the phosphorus and nitrogen from the medium. Phosphorus was depleted within 4 days while nitrogen took 12 days to reach depletion. The phosphorus and nitrogen removal rates during the initial linear growth phase were 17 and 122 mg·L−1·d−1, respectively. After this initial phase, the phosphorus was depleted. The nitrogen removal rate continued to decrease in the second phase, resulting in an overall removal rate of 80 mg·L−1·d−1. The biomass concentration at the end of the experiment was 11.5 g·L−1, with a P content of approximately 1% and a N content of 7.6%. This high algal biomass concentration, together with a relatively short P recovery time, is a promising finding for future post-treatment of black water while gaining valuable algal biomass for further application.
    https://doi.org/10.1021/acs.est.5b02858
  • Frontiers in Behavioral Neuroscience
    2015

    Differentially expressed genes linked to natural variation in long-term memory formation in Cotesia parasitic wasps

    Joke Van Vugt, Katja M. Hoedjes, Henri C. Van de Geest, Elio G.W.M. Schijlen, Louise E.M. Vet, Hans M. Smid
    BACKGROUND: Even though learning and memory are universal traits in the Animal Kingdom, closely related species reveal substantial variation in learning rate and memory dynamics. To determine the genetic background of this natural variation, we studied two congeneric parasitic wasp species, Cotesia glomerata and C. rubecula, which lay their eggs in caterpillars of the large and small cabbage white butterfly. A successful egg laying event serves as an unconditioned stimulus in a classical conditioning paradigm, where plant odors become associated to the encounter of a suitable host caterpillar. Depending on the host species, the number of conditioning trials and the parasitic wasp species, three different types of transcription-dependent long-term memory (LTM) and one type of transcription-independent, anesthesia-resistant memory (ARM) can be distinguished. To identify transcripts underlying these differences in memory formation, we isolated mRNA from parasitic wasp heads at three different time points between induction and consolidation of each of the four memory types, and for each sample three biological replicates, where after strand-specific paired-end 100 bp deep sequencing. Transcriptomes were assembled de novo and differential expression was determined for each memory type and time point after conditioning, compared to unconditioned wasps. Most differentially expressed (DE) genes and antisense transcripts were only DE in one of the LTM types. Among the DE genes that were DE in two or more LTM types, were many protein kinases and phosphatases, small GTPases, receptors and ion channels. Some genes were DE in opposing directions between any of the LTM memory types and ARM, suggesting that ARM in Cotesia requires the transcription of genes inhibiting LTM or vice versa. We discuss our findings in the context of neuronal functioning, including RNA splicing and transport, epigenetic regulation, neurotransmitter/peptide synthesis and antisense transcription. In conclusion, these brain transcriptomes provide candidate genes that may be involved in the observed natural variation in LTM in closely related Cotesia parasitic wasp species.
    https://doi.org/10.3389/fnbeh.2015.00255
  • BMC Genomics
    2015

    Learning-induced gene expression in the heads of two Nasonia species that differ in long-term memory formation

    Katja M. Hoedjes, Hans M. Smid, Elio G.W.M. Schijlen, Louise E.M. Vet, Joke Van Vugt
    Background
    Cellular processes underlying memory formation are evolutionary conserved, but natural variation in memory dynamics between animal species or populations is common. The genetic basis of this fascinating phenomenon is poorly understood. Closely related species of Nasonia parasitic wasps differ in long-term memory (LTM) formation: N. vitripennis will form transcription-dependent LTM after a single conditioning trial, whereas the closely-related species N. giraulti will not. Genes that were differentially expressed (DE) after conditioning in N. vitripennis, but not in N. giraulti, were identified as candidate genes that may regulate LTM formation.

    Results
    RNA was collected from heads of both species before and immediately, 4 or 24 hours after conditioning, with 3 replicates per time point. It was sequenced strand-specifically, which allows distinguishing sense from antisense transcripts and improves the quality of expression analyses. We determined conditioning-induced DE compared to naïve controls for both species. These expression patterns were then analysed with GO enrichment analyses for each species and time point, which demonstrated an enrichment of signalling-related genes immediately after conditioning in N. vitripennis only. Analyses of known LTM genes and genes with an opposing expression pattern between the two species revealed additional candidate genes for the difference in LTM formation. These include genes from various signalling cascades, including several members of the Ras and PI3 kinase signalling pathways, and glutamate receptors. Interestingly, several other known LTM genes were exclusively differentially expressed in N. giraulti, which may indicate an LTM-inhibitory mechanism. Among the DE transcripts were also antisense transcripts. Furthermore, antisense transcripts aligning to a number of known memory genes were detected, which may have a role in regulating these genes.

    Conclusion
    This study is the first to describe and compare expression patterns of both protein-coding and antisense transcripts, at different time points after conditioning, of two closely related animal species that differ in LTM formation. Several candidate genes that may regulate differences in LTM have been identified. This transcriptome analysis is a valuable resource for future in-depth studies to elucidate the role of candidate genes and antisense transcription in natural variation in LTM formation.
    https://doi.org/10.1186/s12864-015-1355-1
  • Animal Behaviour
    2014

    Unravelling reward value: the effect of host value on memory retention in Nasonia parasitic wasps

    Katja M. Hoedjes, Lejon E. M. Kralemann, Joke Van Vugt, Louise E.M. Vet, Hans M. Smid
    Learning can be instrumental in acquiring new skills or optimizing behaviour, but it is also costly in terms of energy and when maladaptive associations are formed: the balance between costs and benefits affects memory dynamics. Numerous studies have demonstrated that memory dynamics of animal species depend on the value of the reward during conditioning, even when animals are inexperienced with this reward. How an animal perceives reward value depends on a number of aspects, including the quantity or quality of the reward in terms of energy or fitness for the animal, the internal state of the animal and previous experience. The reliability of the learned association is another aspect, which can be assessed through the frequency of experiences, or through perception of inherent properties of the reward. The reward in oviposition learning of parasitic wasps is a host to parasitize. Different host species can differ in their reward value. This study focused on a specific aspect of reward value, namely host value, i.e. the number and size of emerging offspring, and tested the effect on oviposition learning in parasitic wasps of the genus Nasonia. We conditioned parasitic wasps of the species Nasonia vitripennis and Nasonia giraulti using three different host species as a reward, which differed greatly in their value as a host. However, for both parasitic wasp species, the resulting memory formation was independent of the value of the host. We discuss factors that may be responsible for this observation. (C) 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
    https://doi.org/10.1016/j.anbehav.2014.07.013
  • Heredity
    2014

    Introgression study reveals two quantitative trait loci involved in interspecific variation in memory retention among Nasonia wasp species

    K.M. Hoedjes, Hans M. Smid, Louise E.M. Vet, J.H. Werren
    Genes involved in the process of memory formation have been studied intensively in model organisms; however, little is known about the mechanisms that are responsible for natural variation in memory dynamics. There is substantial variation in memory retention among closely related species in the parasitic wasp genus Nasonia. After a single olfactory conditioning trial, N. vitripennis consolidates long-term memory that lasts at least 6 days. Memory of the closely related species N. giraulti is present at 24 h but is lost within 2 days after a single trial. The genetic basis of this interspecific difference in memory retention was studied in a backcrossing experiment in which the phenotype of N. giraulti was selected for in the background of N. vitripennis for up to five generations. A genotyping microarray revealed five regions that were retained in wasps with decreased memory retention. Independent introgressions of individual candidate regions were created using linked molecular markers and tested for memory retention. One region on chromosome 1 (spanning ~5.8 cM) and another on chromosome 5 (spanning ~25.6 cM) resulted in decreased memory after 72 h, without affecting 24-h-memory retention. This phenotype was observed in both heterozygous and homozygous individuals. Transcription factor CCAAT/enhancer-binding protein and a dopamine receptor, both with a known function in memory formation, are within these genomic regions and are candidates for the regulation of memory retention. Concluding, this study demonstrates a powerful approach to study variation in memory retention and provides a basis for future research on its genetic basis.
    https://doi.org/10.1038/hdy.2014.66
  • 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
  • Plant Cell and Environment
    2013

    A novel indirect defence in Brassicaceae: Structure and function of extrafloral nectaries in Brassica juncea

    Vartika Mathur, Roel Wagenaar, J.C. Caissard, A. Sankara Reddy, Louise E.M. Vet, A.M. Cortesero, Nicole M. van Dam
    While nectaries are commonly found in flowers, some plants also form extrafloral nectaries on stems or leaves. For the first time in the family Brassicaceae, here we report extrafloral nectaries in Brassica juncea. The extrafloral nectar (EFN) was secreted from previously amorphic sites on stems, flowering stalks and leaf axils from the onset of flowering until silique formation. Transverse sections at the point of nectar secretion revealed a pocket-like structure whose opening was surrounded by modified stomatal guard cells. The EFN droplets were viscous and up to 50% of the total weight was sugars, 97% of which was sucrose in the five varieties of B. juncea examined. Threonine, glutamine, arginine and glutamate were the most abundant amino acids. EFN droplets also contained glucosinolates, mainly gluconapin and sinigrin. Nectar secretion was increased when the plants were damaged by chewing above- and belowground herbivores and sap-sucking aphids. Parasitoids of each herbivore species were tested for their preference, of which three parasitoids preferred EFN and sucrose solutions over water. Moreover, the survival and fecundity of parasitoids were positively affected by feeding on EFN. We conclude that EFN production in B. juncea may contribute to the indirect defence of this plant species.
    https://doi.org/10.1111/j.1365-3040.2012.02593.x
  • 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
  • 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
  • Chemoecology
    2013

    Dealing with double trouble: consequences of single and double herbivory in Brassica juncea

    Vartika Mathur, T.O.G. Tytgat, R. de Graaf, V. Kalia, A.S. Reddy, Louise E.M. Vet, Nicole M. van Dam
    In their natural environment, plants are often attacked simultaneously by many insect species. The specificity of induced plant responses that is reported after single herbivore attacks may be compromised under double herbivory and this may influence later arriving herbivores. The present study focuses on the dynamics of induced plant responses induced by single and double herbivory, and their effects on successive herbivores. Morphological (leaf length, area and trichome density) and chemical changes (leaf alkenyl and indole glucosinolates) in Brassica juncea were evaluated 4, 10, 14 and 20 days after damage by the specialist Plutella xylostella alone, or together with the generalist Spodoptera litura. To assess the biological effect of the plant’s responses, the preference and performance of both herbivores on previously induced plants were measured. We found that alkenyl glucosinolates were induced 20 days after damage by P. xylostella alone, whereas their levels were elevated as early as 4 days after double herbivory. Trichome density was increased in both treatments, but was higher after double herbivory. Interestingly, there was an overall decrease in indole glucosinolates and an increase in leaf size due to damage by P. xylostella, which was not observed during double damage. S. litura preferred and performed better on undamaged plants, whereas P. xylostella preferred damaged plants and performed better on plants damaged 14 and 10 days after single and double herbivory, respectively. Our results suggest that temporal studies involving single versus multiple attacker situations are necessary to comprehend the role of induced plant responses in plant–herbivore interactions.
    https://doi.org/10.1007/s00049-012-0120-z
  • 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
  • Pest Management Science
    2013

    Genetic engineering of plant volatile terpenoids: effects on a herbivore, a predator and a parasitoid

    Martine Kos, B. Houshyani, A.J. Overeem, Harro J. Bouwmeester, B.T. Weldegergis, Joop J.A. van Loon, Marcel Dicke, Louise E.M. Vet
    BACKGROUND: Most insect-resistant transgenic crops employ toxins to control pests. A novel approach is to enhance the effectiveness of natural enemies by genetic engineering of the biosynthesis of volatile organic compounds (VOCs). Before the commercialisation of such transgenic plants can be pursued, detailed fundamental studies of their effects on herbivores and their natural enemies are necessary. The linalool/nerolidol synthase gene FaNES1 was constitutively expressed from strawberry in three Arabidopsis thaliana accessions, and the behaviour of the aphid Brevicoryne brassicae L., the parasitoid Diaeretiella rapae McIntosh and the predator Episyrphus balteatus de Geer was studied. RESULTS: Transgenic FaNES1-expressing plants emitted (E)-nerolidol and larger amounts of (E)-DMNT and linalool. Brevicoryne brassicae was repelled by the transgenic lines of two of the accessions, whereas its performance was not affected. Diaeretiella rapae preferred aphid-infested transgenic plants over aphid-infested wild-type plants for two of the accessions. In contrast, female E. balteatus predators did not differentiate between aphid-infested transgenic or wild-type plants. CONCLUSION: The results indicate that the genetic engineering of plants to modify their emission of VOCs holds considerable promise for facilitating biological control of herbivores. Validation for crop plants is a necessary next step to assess the usefulness of modified volatile emission in integrated pest management.
    https://doi.org/10.1002/ps.3391
  • PLoS One
    2012

    Optimal resource allocation to survival and reproduction in parasitic wasps foraging in fragmented habitats

    E. Wajnberg, P. Coquillard, Louise E.M. Vet, T. Hoffmeister
    Expansion and intensification of human land use represents the major cause of habitat fragmentation. Such fragmentation can have dramatic consequences on species richness and trophic interactions within food webs. Although the associated ecological consequences have been studied by several authors, the evolutionary effects on interacting species have received little research attention. Using a genetic algorithm, we quantified how habitat fragmentation and environmental variability affect the optimal reproductive strategies of parasitic wasps foraging for hosts. As observed in real animal species, the model is based on the existence of a negative trade-off between survival and reproduction resulting from competitive allocation of resources to either somatic maintenance or egg production. We also asked to what degree plasticity along this trade-off would be optimal, when plasticity is costly. We found that habitat fragmentation can indeed have strong effects on the reproductive strategies adopted by parasitoids. With increasing habitat fragmentation animals should invest in greater longevity with lower fecundity; yet, especially in unpredictable environments, some level of phenotypic plasticity should be selected for. Other consequences in terms of learning ability of foraging animals were also observed. The evolutionary consequences of these results are discussed.
    https://doi.org/10.1371/journal.pone.0038227
  • 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 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
  • Journal of Chemical Ecology
    2012

    Herbivore-mediated effects of glucosinolates on different natural enemies of a specialist aphid

    Martine Kos, B. Houshyani, B.B. Achhami, R. Wietsma, R. Gols, B.T. Weldegergis, Patrick Kabouw, Harro J. Bouwmeester, Louise E.M. Vet, Marcel Dicke, Joop J.A. van Loon
    The cabbage aphid Brevicoryne brassicae is a specialist herbivore that sequesters glucosinolates from its host plant as a defense against its predators. It is unknown to what extent parasitoids are affected by this sequestration.We investigated herbivore-mediated effects of glucosinolates on the parasitoid wasp Diaeretiella rapae and the predator Episyrphus balteatus. We reared B. brassicae on three ecotypes of Arabidopsis thaliana that differ in glucosinolate content and on one genetically transformed line with modified concentrations of aliphatic glucosinolates.We tested aphid performance and the performance and behavior of both natural enemies. We correlated this with phloem and aphid glucosinolate concentrations and emission of volatiles. Brevicoryne brassicae performance correlated positively with concentrations of both aliphatic and indole glucosinolates in the phloem. Aphids selectively sequestered glucosinolates. Glucosinolate concentration in B. brassicae correlated negatively with performance of the predator, but positively with performance of the parasitoid, possibly because the aphids with the highest glucosinolate concentrations had a higher body weight. Both natural enemies showed a positive performance-preference correlation. The predator preferred the ecotype with the lowest emission of volatile glucosinolate breakdown products in each test combination, whereas the parasitoid wasp preferred the A. thaliana ecotype with the highest emission of these volatiles. The study shows that there are differential herbivore-mediated effects of glucosinolates on a predator and a parasitoid of a specialist aphid that selectively sequesters glucosinolates from its host plant.
    https://doi.org/10.1007/s10886-012-0065-2
  • PLoS One
    2012

    Reward Value Determines Memory Consolidation in Parasitic Wasps

    Marjolein Kruidhof, F. Pashalidou, N.E. Fatouros, I.A. Figueroa, Louise E.M. Vet, Hans M. Smid, M.E. Huigens
    Animals can store learned information in their brains through a series of distinct memory forms. Short-lasting memory forms can be followed by longer-lasting, consolidated memory forms. However, the factors determining variation in memory consolidation encountered in nature have thus far not been fully elucidated. Here, we show that two parasitic wasp species belonging to different families, Cotesia glomerata (Hymenoptera: Braconidae) and Trichogramma evanescens (Hymenoptera; Trichogrammatidae), similarly adjust the memory form they consolidate to a fitness-determining reward: egg-laying into a host-insect that serves as food for their offspring. Protein synthesis-dependent long-term memory (LTM) was consolidated after single-trial conditioning with a high-value host. However, single-trial conditioning with a low-value host induced consolidation of a shorter-lasting memory form. For Cotesia glomerata, we subsequently identified this shorter-lasting memory form as anesthesia-resistant memory (ARM) because it was not sensitive to protein synthesis inhibitors or anesthesia. Associative conditioning using a single reward of different value thus induced a physiologically different mechanism of memory formation in this species. We conclude that the memory form that is consolidated does not only change in response to relatively large differences in conditioning, such as the number and type of conditioning trials, but is also sensitive to more subtle differences, such as reward value. Reward-dependent consolidation of exclusive ARM or LTM provides excellent opportunities for within-species comparison of mechanisms underlying memory consolidation. [KEYWORDS: long-term-memory trichogramma wasps cotesia-glomerata protein-synthesis natural variation apis-mellifera learning rate c-rubecula drosophila quality]
    https://doi.org/10.1371/journal.pone.0039615
  • 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
  • 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
  • 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
  • Phytochemistry
    2012

    Effects of glucosinolates on a generalist and specialist leaf-chewing herbivore and an associated parasitoid

    Martine Kos, B. Houshyani, R. Wietsma, Patrick Kabouw, Louise E.M. Vet, Joop J.A. van Loon, Marcel Dicke
    Glucosinolates (GLS) are secondary plant metabolites that as a result of tissue damage, for example due to herbivory, are hydrolysed into toxic compounds that negatively affect generalist herbivores. Specialist herbivores have evolved specific adaptations to detoxify GLS or inhibit the formation of toxic hydrolytic products. Although rarely studied, GLS and their breakdown products may also affect parasitoids. The objectives were to test the effects of GLS in a multitrophic system consisting of the generalist herbivore Spodoptera exigua, the specialist herbivore Pieris rapae, and the endoparasitoid Hyposoter ebeninus. Three ecotypes of Arabidopsis thaliana that differ in their GLS composition and concentrations and one transformed line that constitutively produces higher concentrations of aliphatic GLS were used, the latter allowing a direct assessment of the effects of aliphatic GLS on insect performance. Feeding by the generalist S. exigua and the specialist P. rapae induced both higher aliphatic and indole GLS concentrations in the A. thaliana ecotypes, although induction was stronger for indole than aliphatic GLS. For both herbivores a negative correlation between performance and aliphatic GLS concentrations was observed. This suggests that the specialist, despite containing a nitrile-specifier protein (NSP) that diverts GLS degradation from toxic isothiocyanates to less toxic nitriles, cannot completely inhibit the formation of toxic GLS hydrolytic products, or that the costs of this mechanism are higher at higher GLS concentrations. Surprisingly, performance of the parasitoid was positively correlated with higher concentrations of aliphatic GLS in the plant, possibly caused by negative effects on host immune responses. Our study indicates that GLS can not only confer resistance against herbivores directly, but also indirectly by increasing the performance of the parasitoids of these herbivores.
    https://doi.org/10.1016/j.phytochem.2012.01.005
  • Genes Brain and Behavior
    2012

    High throughput olfactory conditioning and memory retention test reveal variation in Nasonia parasitic wasps

    K.M. Hoedjes, J.L.M. Steidle, J.H. Werren, Louise E.M. Vet, Hans M. Smid
    Most of our knowledge on learning and memory formation results from extensive studies on a small number of animal species. Although features and cellular pathways of learning and memory are highly similar in this diverse group of species, there are also subtle differences. Closely related species of parasitic wasps display substantial variation in memory dynamics and can be instrumental to understanding both the adaptive benefit of and mechanisms underlying this variation. Parasitic wasps of the genus Nasonia offer excellent opportunities for multidisciplinary research on this topic. Genetic and genomic resources available for Nasonia are unrivaled among parasitic wasps, providing tools for genetic dissection of mechanisms that cause differences in learning. This study presents a robust, high-throughput method for olfactory conditioning of Nasonia using a host encounter as reward. A T-maze olfactometer facilitates high-throughput memory retention testing and employs standardized odors of equal detectability, as quantified by electroantennogram recordings. Using this setup, differences in memory retention between Nasonia species were shown. In both Nasonia vitripennis and Nasonia longicornis, memory was observed up to at least 5 days after a single conditioning trial, whereas Nasonia giraulti lost its memory after 2 days. This difference in learning may be an adaptation to species-specific differences in ecological factors, for example, host preference. The high-throughput methods for conditioning and memory retention testing are essential tools to study both ultimate and proximate factors that cause variation in learning and memory formation in Nasonia and other parasitic wasp species.
    https://doi.org/10.1111/j.1601-183X.2012.00823.x
  • Animal Behaviour
    2011

    Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps.

    M. Van den Berg, L. Duivenvoorde, G. Wang, S. Tribuhl, Tibor Bukovinszky, Louise E.M. Vet, Marcel Dicke, Hans M. Smid
    Animals form memory types that differ in duration and stability. The initial anaesthesia-sensitive memory (ASM) can be replaced by anaesthesia-resistant memory (ARM), and/or by protein synthesis-dependent, long-term memory (LTM). We previously showed that two closely related parasitic wasp species differ in learning rate and memory consolidation. In Cotesia glomerata, LTM lasting at least 24 h was formed after single-trial conditioning, whereas single-trial conditioning led to ARM that waned before 24 h in Cotesia rubecula. This species formed LTM only after repeated conditioning trials spaced in time. Here, we used artificial selection on learning rate to investigate whether selection for a low learning rate in C. glomerata would result in C. rubecula-like memory dynamics. Memory consolidation was tested by using cold-shock anaesthesia and protein synthesis inhibitors. After single-trial conditioning, ARM was consolidated within hours in unselected C. rubecula, but directly, without an intermediate ARM phase, into LTM in unselected C. glomerata. We obtained low learning rate selection lines of C. glomerata wasps that, like C. rubecula, did not form LTM after single-trial conditioning, to see whether such wasps would then consolidate ARM instead of LTM. We showed that this was not the case. The selected wasps formed LTM after repeated, spaced conditioning trials, but formed only ASM without consolidation of ARM or LTM after single-trial learning. Ecological consequences of this type of memory formation are discussed.
    https://doi.org/10.1016/j.anbehav.2010.11.002
  • Entomologia Experimentalis et Applicata
    2011

    Temporal dynamics of herbivore-induced responses in Brassica juncea and their effect on generalist and specialist herbivores

    Vartika Mathur, S. Ganta, Ciska Raaijmakers, A.S. Reddy, Louise E.M. Vet, Nicole M. van Dam
    Herbivore feeding may induce an array of responses in plants, and each response may have its own temporal dynamics. Precise timing of these plant responses is vital for them to have optimal effect on the herbivores feeding on the plant. This study measured the temporal dynamics of various systemically induced responses occurring in Brassica juncea (L.) Czern. (Brassicaceae) leaves after insect herbivory in India and The Netherlands. Morphological (trichomes, leaf size) and chemical (glucosinolates, amino acids, sugars) responses were analysed. The effects of systemic responses were assessed using a specialist [Plutella xylostella L. (Lepidoptera: Plutellidae)] and a generalist [Spodoptera litura Fabricius (Lepidoptera: Noctuidae)] herbivore. We tested the hypotheses that morphological responses were slower than chemical responses and that generalist herbivores would be more affected by induced responses than specialists. Glucosinolates and trichomes were found to increase systemically as quickly as 4 and 7 days after herbivore damage, respectively. Amino acids, sugars, and leaf size remained unaffected during this period. The generalist S. litura showed a significant feeding preference for undamaged leaves, whereas the specialist herbivore P. xylostella preferred leaves that were damaged 9 days before. Performance bioassays on generalist S. litura revealed that larvae gained half the weight on leaves from damaged plants as compared to larvae feeding on leaves from undamaged plants. These studies show that although morphological responses are somewhat slower than chemical responses, they also contribute to induced plant resistance in a relatively short time span. We argue that before considering induced responses as resistance factors, their effect should be assessed at various points in time with both generalist and specialist herbivores.
    https://doi.org/10.1111/j.1570-7458.2011.01122.x
  • Functional Ecology
    2011

    Relative importance of plant-mediated bottom-up and top-down forces on herbivore abundance on Brassica oleracea

    Martine Kos, C. Broekgaarden, Patrick Kabouw, K. Oude Lenferink, Erik H. Poelman, Louise E.M. Vet, Marcel Dicke, Joop J.A. van Loon
    1. Arthropod communities are structured by complex interactions between bottom-up (resource-based) and top-down (natural enemy-based) forces. Their relative importance in shaping arthropod communities, however, continues to be under debate. Bottom-up and top-down forces can be affected by intraspecific plant variation, for example by differences in concentrations of secondary metabolites that affect herbivore abundance through plant quality (bottom-up) or attract natural enemies of these herbivores (top-down). 2. Our objective was to investigate whether herbivore abundance is more strongly affected by plant-mediated bottom-up or top-down forces. 3. We used a model system of four cultivars of Brassica oleracea that show a high degree of variation in several plant traits, resistance to herbivores and attraction of natural enemies. During two field seasons, we recorded the abundance of several herbivorous and carnivorous insect species. To assess the relative importance of bottom-up and top-down forces, we quantified chemical and morphological traits of the cultivars (bottom-up) and assessed parasitization of herbivores and predator oviposition on plants inoculated with a controlled number of herbivores (top-down). 4. We show that intraspecific variation in plant chemistry and morphology consistently affects the abundance of insect herbivores and their natural enemies, resulting in cascading effects on tritrophic interactions in the associated insect community. Foliar profiles of glucosinolates and leaf toughness appeared most important for these effects. Brassica oleracea cultivars that harboured the largest numbers of herbivores also harboured the largest numbers of natural enemies. Differences in the fraction of herbivores parasitized and in predator oviposition on plants inoculated with a controlled number of herbivores could not explain the differences in natural abundance of herbivores. 5. Although abundance of herbivores is most likely influenced by a combination of bottom-up and top-down forces, it appears that in the tritrophic system investigated, bottom-up forces (plant chemistry and morphology) were more important for herbivore abundance than plant-mediated top-down forces (attraction and arrestment of natural enemies).
    https://doi.org/10.1111/j.1365-2435.2011.01871.x
  • Ecological Entomology
    2011

    Prey-mediated effects of glucosinolates on aphid predators

    Martine Kos, Patrick Kabouw, R. Noordam, K. Hendriks, Louise E.M. Vet, Joop J.A. van Loon, Marcel Dicke
    1. Plant resistance against herbivores can act directly (e.g. by producing toxins) and indirectly (e.g. by attracting natural enemies of herbivores). If plant secondary metabolites that cause direct resistance against herbivores, such as glucosinolates, negatively influence natural enemies, this may result in a conflict between direct and indirect plant resistance. 2. Our objectives were (i) to test herbivore-mediated effects of glucosinolates on the performance of two generalist predators, the marmalade hoverfly (Episyrphus balteatus) and the common green lacewing (Chrysoperla carnea) and (ii) to test whether intraspecific plant variation affects predator performance. 3. Predators were fed either Brevicoryne brassicae, a glucosinolate-sequestering specialist aphid that contains aphid-specific myrosinases, or Myzus persicae, a nonsequestering generalist aphid that excretes glucosinolates in the honeydew, reared on four different white cabbage cultivars. Predator performance and glucosinolate concentrations and profiles in B. brassicae and host-plant phloem were measured, a novel approach as previous studies often measured glucosinolate concentrations only in total leaf material. 4. Interestingly, the specialist aphid B. brassicae selectively sequestered glucosinolates from its host plant. The performance of predators fed this aphid species was lower than when fed M. persicae. When fed B. brassicae reared on different cultivars, differences in predator performance matched differences in glucosinolate profiles among the aphids. 5. We show that not only the prey species, but also the plant cultivar can have an effect on the performance of predators. Our results suggest that in the tritrophic system tested, there might be a conflict between direct and indirect plant resistance.
    https://doi.org/10.1111/j.1365-2311.2011.01282.x
  • Proceedings of the Royal Society B-Biological Sciences
    2011

    Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience

    K.M. Hoedjes, Marjolein Kruidhof, M.E. Huigens, Marcel Dicke, Louise E.M. Vet, Hans M. Smid
    Although the neural and genetic pathways underlying learning and memory formation seem strikingly similar among species of distant animal phyla, several more subtle inter- and intraspecific differences become evident from studies on model organisms. The true significance of such variation can only be understood when integrating this with information on the ecological relevance. Here, we argue that parasitoid wasps provide an excellent opportunity for multi-disciplinary studies that integrate ultimate and proximate approaches. These insects display interspecific variation in learning rate and memory dynamics that reflects natural variation in a daunting foraging task that largely determines their fitness: finding the inconspicuous hosts to which they will assign their offspring to develop. We review bioassays used for oviposition learning, the ecological factors that are considered to underlie the observed differences in learning rate and memory dynamics, and the opportunities for convergence of ecology and neuroscience that are offered by using parasitoid wasps as model species. We advocate that variation in learning and memory traits has evolved to suit an insect's lifestyle within its ecological niche.
    https://doi.org/10.1098/rspb.2010.2199
  • 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
  • Insect Molecular Biology
    2010

    CREB expression in the brains of two closely related parasitic wasp species that differ in long-term memory formation

    M. Van den Berg, P. Verbaarschot, S. Hontelez, Louise E.M. Vet, Marcel Dicke, Hans M. Smid
    The cAMP/PKA signalling pathway and transcription factor cAMP response element-binding protein (CREB) play key roles in long-term memory (LTM) formation. We used two closely related parasitic wasp species, Cotesia glomerata and Cotesia rubecula, which were previously shown to be different in LTM formation, and sequenced at least nine different CREB transcripts in both wasp species. The splicing patterns, functional domains and amino acid sequences were similar to those found in the CREB genes of other organisms. The predicted amino acid sequences of the CREB isoforms were identical in both wasp species. Using real-time quantitative PCR we found that two low abundant CREB transcripts are differentially expressed in the two wasps, whereas the expression levels of high abundant transcripts are similar.
    https://doi.org/10.1111/j.1365-2583.2010.00997.x
  • Journal of Chemical Ecology
    2010

    Identification of biologically relevant compounds in aboveground and belowground induced volatile blends

    Nicole M. van Dam, B. Qiu, Cees Hordijk, Louise E.M. Vet, Jeroen Jansen
    Plants under attack by aboveground herbivores emit complex blends of volatile organic compounds (VOCs). Specific compounds in these blends are used by parasitic wasps to find their hosts. Belowground induction causes shifts in the composition of aboveground induced VOC blends, which affect the preference of parasitic wasps. To identify which of the many volatiles in the complex VOC blends may explain parasitoid preference poses a challenge to ecologists. Here, we present a case study in which we use a novel bioinformatics approach to identify biologically relevant differences between VOC blends of feral cabbage (Brassica oleracea L.). The plants were induced aboveground or belowground with jasmonic acid (JA) and shoot feeding caterpillars (Pieris brassicae or P. rapae). We used Partial Least Squares—Discriminant Analysis (PLSDA) to integrate and visualize the relation between plant-emitted VOCs and the preference of female Cotesia glomerata. Overall, female wasps preferred JA-induced plants over controls, but they strongly preferred aboveground JA-induced plants over belowground JA-induced plants. PLSDA revealed that the emission of several monoterpenes was enhanced similarly in all JA-treated plants, whereas homoterpenes and sesquiterpenes increased exclusively in aboveground JA-induced plants. Wasps may use the ratio between these two classes of terpenes to discriminate between aboveground and belowground induced plants. Additionally, it shows that aboveground applied JA induces different VOC biosynthetic pathways than JA applied to the root. Our bioinformatic approach, thus, successfully identified which VOCs matched the preferences of the wasps in the various choice tests. Additionally, the analysis generated novel hypotheses about the role of JA as a signaling compound in aboveground and belowground induced responses in plants.
    https://doi.org/10.1007/s10886-010-9844-9
  • 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
  • Ecological Entomology
    2010

    Herbivore-induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

    Erik H. Poelman, Joop J.A. van Loon, Nicole M. van Dam, Marcel Dicke, Louise E.M. Vet
    1. Plant responses to herbivore attack may have community-wide effects on the composition of the plant-associated insect community. Thereby, plant responses to an early-season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early-season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early-season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf-chewing and sap-sucking guilds. 4. Our results show that community-wide effects of early-season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.
    https://doi.org/10.1111/j.1365-2311.2010.01179.x
  • Oikos
    2009

    Quantifying the impact of above- and belowground higher trophic levels on plant and herbivore performance by modeling

    Katrin Meyer, Matthijs Vos, Wolf M. Mooij, (Gera) W.H.G. Hol, Aad J Termorshuizen, Louise E.M. Vet, Wim H. van der Putten
    Growing empirical evidence suggests that aboveground and belowground multitrophic communities interact. However, investigations that comprehensively explore the impacts of above- and belowground third and higher trophic level organisms on plant and herbivore performance are thus far lacking. We tested the hypotheses that above- and belowground higher trophic level organisms as well as decomposers affect plant and herbivore performance and that these effects cross the soil–surface boundary. We used a well-validated simulation model that is individual-based for aboveground trophic levels such as shoot herbivores, parasitoids, and hyperparasitoids while considering belowground herbivores and their antagonists at the population level. We simulated greenhouse experiments by removing trophic levels and decomposers from the simulations in a factorial design. Decomposers and above- and belowground third trophic levels affected plant and herbivore mortality, root biomass, and to a lesser extent shoot biomass. We also tested the effect of gradual modifications of the interactions between different trophic level organisms with a sensitivity analysis. Shoot and root biomass were highly sensitive to the impact of the fourth trophic level. We found effects that cross the soil surface, such as aboveground herbivores and parasitoids affecting root biomass and belowground herbivores influencing aboveground herbivore mortality. We conclude that higher trophic level organisms and decomposers can strongly influence plant and herbivore performance. We propose that our modelling framework can be used in future applications to quantitatively explore the possible outcomes of complex above- and belowground multitrophic interactions under a range of environmental conditions and species compositions.
    https://doi.org/10.1111/j.1600-0706.2009.17220.x
  • 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
  • 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

    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
  • Functional Ecology
    2009

    Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids

    Erik H. Poelman, A.M.O. Oduor, C. Broekgaarden, Cees Hordijk, Jeroen Jansen, Joop J.A. van Loon, Nicole M. van Dam, Louise E.M. Vet, Marcel Dicke
    1. Herbivore-induced plant volatiles (HIPVs) play an important role in host location of parasitoid wasps and may benefit the plant by top–down control of its herbivorous attackers. Although many studies have shown that accessions of plants differ in attractiveness to parasitoid wasps under controlled laboratory studies, few studies have confirmed that the most attractive accessions also sustain highest parasitism rates in the field. Here, we tested whether in-flight preference of parasitoids for HIPVs from cultivars of Brassica oleracea in the laboratory reliably predicts the parasitism rates of herbivores feeding on these cultivars in the field. 2. In wind tunnel tests in the laboratory, we ranked cultivars of B. oleracea for the preference of two congeneric parasitoids ( Cotesia glomerata and C. rubecula ) for their HIPVs. The cultivars were then compared for their relative parasitism rates of caterpillars in the field. Throughout the growth season in the field, we infested the different cultivars with Pieris caterpillars on a weekly basis. The caterpillars were recollected after 3 days, dissected and scored for the rate of parasitism. 3. Cultivars of B. oleracea that we identified as most attractive to parasitoids in the laboratory also sustained highest proportions of parasitism in the field. The composition of the headspace of the B. oleracea cultivars damaged by P. rapae differs among these cultivars in the amounts of terpenoids and methyl salicylate emitted, which may be responsible for the differential attraction of parasitoids to the cultivars. 4. Our results show that intraspecific variation in HIPVs of plants is paralleled by differential parasitism of caterpillars in the field. The widely used laboratory assays on HIPV-based preferences of parasitoids provided reliable information on relative parasitism differences of herbivores as found in the field. 5. Thereby, our work confirms that through HIPVs plants attract parasitoids that effectively parasitize herbivores even under the complex and variable abiotic and biotic conditions in (agro-) ecosystems.
    https://doi.org/10.1111/j.1365-2435.2009.01570.x
  • Trends in Biotechnology
    2009

    Transgenic plants as vital components of integrated pest management

    Martine Kos, Joop J.A. van Loon, Marcel Dicke, Louise E.M. Vet
    Although integrated pest management (IPM) strategies have been developed worldwide, further improvement of IPM effectiveness is required. The use of transgenic technology to create insect-resistant plants can offer a solution to the limited availability of highly insect-resistant cultivars. Commercially available insect-resistant transgenic crops show clear benefits for agriculture and there are many exciting new developments such as transgenic plants that enhance biological control. Effective evaluation tools are needed to ascertain that transgenic plants do not result in undesired non-target effects. If these conditions are met, there will be ample opportunities for transgenic plants to become key components of environmentally benign and durable pest management systems. Here we discuss the potential and challenges for incorporating transgenic plants in IPM.
    https://doi.org/10.1016/j.tibtech.2009.08.002
  • 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
  • Journal of Chemical Ecology
    2008

    Barbarea vulgaris glucosinolate phenotypes differentially affect performance and preference of two different species of lepidopteran herbivores

    H. Van Leur, Louise E.M. Vet, Wim H. van der Putten, Nicole M. van Dam
    The composition of secondary metabolites and the nutritional value of a plant both determine herbivore preference and performance. The genetically determined glucosinolate pattern of Barbarea vulgaris can be dominated by either glucobarbarin (BAR-type) or by gluconasturtiin (NAS-type). Because of the structural differences, these glucosinolates may have different effects on herbivores. We compared the two Barbarea chemotypes with regards to the preference and performance of two lepidopteran herbivores, using Mamestra brassicae as a generalist and Pieris rapae as a specialist. The generalist and specialist herbivores did not prefer either chemotype for oviposition. However, larvae of the generalist M. brassicae preferred to feed and performed best on NAS-type plants. On NAS-type plants, 100% of the M. brassicae larvae survived while growing exponentially, whereas on BAR-type plants, M. brassicae larvae showed little growth and a mortality of 37.5%. In contrast to M. brassicae, the larval preference and performance of the specialist P. rapae was unaffected by plant chemotype. Total levels of glucosinolates, water soluble sugars, and amino acids of B. vulgaris could not explain the poor preference and performance of M. brassicae on BAR-type plants. Our results suggest that difference in glucosinolate chemical structure is responsible for the differential effects of the B. vulgaris chemotypes on the generalist herbivore. Electronic supplementary material The online version of this article (doi:10.1007/s10886-007-9424-9) contains supplementary material, which is available to authorized users.
    https://doi.org/10.1007/s10886-007-9424-9
  • 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
  • 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
  • Ecological Informatics
    2006

    Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics

    Matthijs Vos, Louise E.M. Vet, F.L. Wäckers, J.J. Middelburg, Wim H. van der Putten, Wolf M. Mooij, Carlo H.R. Heip, Ellen Van Donk
    Here we consider how information transfer shapes interactions in aquatic and terrestrial food webs. All organisms, whether they are dead or alive, release certain chemicals into their environment. These can be used as infochemicals by any other individual in the food web that has the biological machinery to sense and process such information. Such machinery has evolved in bacteria, plants and animals and has thus become an inextricable part of the mechanisms that underlie feeding relations in food webs. Organisms live in environments suffused with infochemicals and this information network can be tapped into by both predators and their prey. However, it also opens doors to confusion in the face of a bewildering abundance and complexity of information. Infochemical mixing, masking, crypsis and mimicry could cause such confusion, especially in species-rich communities. We provide a point of entry into this field of enquiry by identifying seminal papers and major reviews and by discussing research lines that might enhance our mechanistic understanding of interactions in food webs. We highlight empirical work on the ways in which individuals use infochemicals and discuss model results on how this mediates patterns of population dynamics. We consider implications for ecosystem management and indicate how classical models and novel approaches from ecological infor [KEYWORDS: Biodiversity ; Biological control ; Climate ; Dimethyl sulphide ; Global warming ; Individual based models ; Information networks in ecosystems ; Integration of laboratory and field data ; Learning ; Linking levels of ecological organization ; Lake restoration ; Phenotypic plasticity ; Trait-mediated interactions]
    https://doi.org/10.1016/j.ecoinf.2005.06.001
  • 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 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
  • 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
  • Ecosystems
    2005

    Ecological and evolutionary consequences of biological invasions and habitat fragmentation

    T.S. Hoffmeister, Louise E.M. Vet, Arjen Biere, K. Holsinger, J. Filser
    There is substantial evidence that environmental changes on a landscape level can have dramatic consequences for the species richness and structure of food webs as well as on trophic interactions within such food webs. Thus far, the consequences of environmental change, and particularly the effects of invasive species and the fragmentation and isolation of natural habitats, have most often been studied in a purely ecological context, with the main emphasis on the description of alterations in species abundance and diversity and trophic links within food webs. Here, we argue that the study of evolutionary processes that may be affected by such changes is urgently needed to enhance our understanding of the consequences of environmental change. This requires an approach that treats species as dynamic systems with plastic responses to change rather than as static entities. As such, phenotypic plasticity on an individual level and genotypic change as a population level response should be taken into account when studying the consequences of a changing world. Using a multidisciplinary approach, we report on recent advances in our understanding, identify some major gaps in our current knowledge, and point towards rewarding approaches to enhance our understanding of how environmental change alters trophic interactions and ecosystems. [KEYWORDS: evolutionary processes ; phenotypic plasticity ; genotypic change ; trophic interactions ; invasive species ; habitat fragmentation]
    https://doi.org/10.1007/s10021-003-0138-8
  • 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
  • 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
  • Ecotoxicology
    2000

    Field research for the authorisation of pesticides

    H.F.G. Van Dijk, L. Brussaard, A. Stein, F. Baerselman, H. De Heer, Th.C.M. Brock, Ellen Van Donk, Louise E.M. Vet, M.A. Van der Gaag, C.A.M. Van Gestel, N. Van der Hoeven, F.M.W. de Jong, A.M. van der Linden, P.C.M. Van Noort, P.A. Oomen, P.J.M. Van Vliet
    On request of the Dutch government a committee of the Health Council of the Netherlands has reviewed the role that results of field research in its broadest sense (i.e., including multi- species toxicity tests in the laboratory, research on model ecosystems et cetera) can play in ecotoxicological risk assessment for the authorisation of pesticides. The Committee believes that field research can provide valuable additional data about the exposure of non-target organisms and the resultant effects at population, community and ecosystem level. However, it frequently is unclear how these data might be used in reaching a decision about authorisation. To solve this problem, it is necessary to specify what is understood by "unacceptable damage". Both more clearly formulated protection goals of the government and a better understanding of the ecological significance of effects are needed to clarify this. Furthermore, the Committee points out that the statistical power of field trials must be sufficient to allow for the detection of changes that might be regarded as ecologically relevant. Finally, it recommends keeping a finger on the pulse in relation to authorised pesticides by monitoring their presence in environmental compartments and by investigating their role in suddenly occurring mortality among conspicuous animal species, such as birds, fish and honeybees. This kind of research forms a safety net for substances that have been wrongly authorised. [KEYWORDS: authorisation; field research; model ecosystems; monitoring; pesticides]
    https://doi.org/10.1023/A:1008920401180
  • 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
  • 1999

    Evolutionary aspects of plant-carnivore interactions

    Plants can respond actively to damage by herbivores. In addition to a mode of defence that is directly aimed at the herbivore itself, plants can emit volatiles that attract carnivores, i.e. the enemies of their enemies. Knowledge of the mechanisms underlying the induction of these herbivore-induced plant volatiles and of the responses of the carnivores is progressing rapidly. Inferences on the initial causes of evolution of herbivore-induced plant volatiles remain conjectural. However, once plant–carnivore interactions have evolved to the net benefit of both participants this mutualism is expected to have evolutionary and ecological consequences for the three trophic levels involved. When plant selection and foraging behaviour of natural enemies is linked to plant fitness this can influence different aspects of the plant defence strategy. The way carnivores perceive and process plant information may influence the evolution of the plant signal (i.e. quantitative and qualitative composition of the odour blend in response to herbivore damage). Vice versa, the signal-to-noise ratio of the information may influence the way carnivores respond to plant cues (innately or through learning). Selection will act on herbivores to disconnect the plant-carnivore link, for example by boycotting the informational value of herbivore-induced synomones. Through plant selection and feeding behaviour herbivores can influence their chance of being found by carnivores. Hence, responses of carnivores to plant cues can influence the evolution of food-plant use by herbivores. The conspiracy between plants and carnivores is at the heart of evolutionary ecology, and wide open for experimental and theoretical investigations.
    https://doi.org/10.1002/9780470515679.ch2
  • 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

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