Louise Vet

Em. Prof. dr. Louise Vet

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Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands



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


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.



Director Netherlands Institute of Ecology (NIOO-KNAW)

Ancillary activities


Peer-reviewed publications

  • Water Research

    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.

  • ISME Journal

    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.
  • Biotechnology and Bioengineering

    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.
  • Ecological Entomology

    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.

  • Communications Biology

    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.

  • Microorganisms

    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.
  • Behavioral Ecology

    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.

  • Journal of Animal Ecology

    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.
  • Biological Reviews

    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.
  • Water Research

    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.
  • Nature Ecology and Evolution

    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
  • Ecological Entomology

    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.
  • 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.
  • Resources, Conservation and Recycling

    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.
  • Chemoecology

    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.
  • GCB Bioenergy

    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.
  • Frontiers in Ecology and Evolution

    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.
  • Frontiers in Ecology and Evolution

    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.

  • BioControl

    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.
  • Ecological Entomology

    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.
  • Frontiers in Ecology and Evolution

    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.
  • Journal of Neuroscience Methods

    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.
  • Ecological Entomology

    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.
  • Current Opinion in Insect Science

    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.
  • International Journal of Molecular Sciences

    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
  • Environmental Science and Technology

    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.
  • Frontiers in Behavioral Neuroscience

    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.
  • BMC Genomics

    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
    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.

    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.

    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.
  • Oecologia

    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.
  • Heredity

    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.
  • Animal Behaviour

    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.
  • New Phytologist

    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.
  • Oikos

    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
  • Functional Ecology

    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.
  • Chemoecology

    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.
  • Biological Invasions

    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.
  • Pest Management Science

    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.
  • Molecular Ecology

    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.
  • Plant Cell and Environment

    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.
  • Genes Brain and Behavior

    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.
  • PLoS Biology

    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.
  • PLoS One

    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]
  • Journal of Chemical Ecology

    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.
  • PLoS One

    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.
  • Phytochemistry

    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.
  • Journal of Insect Physiology

    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
  • BioControl

    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.
  • Biological Control

    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.
  • Journal of Chemical Ecology

    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.
  • Ecological Entomology

    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.
  • Proceedings of the Royal Society B-Biological Sciences

    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.
  • Functional Ecology

    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).
  • Entomologia Experimentalis et Applicata

    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.
  • Animal Behaviour

    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.
  • Ecological Entomology

    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.
  • Biological Invasions

    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’.
  • Insect Molecular Biology

    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.
  • Journal of Chemical Ecology

    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.
  • Ecological Entomology

    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.
  • Trends in Biotechnology

    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.
  • Ecology

    Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores

    Erik H. Poelman, Nicole M. van Dam, Joop J.A. van Loon, Louise E.M. Vet, Marcel Dicke
    Intraspecific variation in plants plays a major role in the composition and diversity of the associated insect community. Resistance traits of plants are likely candidates mediating community composition. However, it is debated whether total concentrations of chemical compounds or specific compounds determine herbivore resistance, and how chemical diversity among plant genotypes in turn affects the composition of the associated herbivore community. To study the role of specific chemical compounds in affecting the herbivore community, we used cultivated Brassica oleracea. The cultivars differ qualitatively in glucosinolate profile, i.e., foliar composition of different glucosinolate compounds, and only a little in total concentration of glucosinolates, the secondary metabolites specific for the Brassicaceae family. In field and laboratory experiments, we tested whether individual compounds explained differences in herbivore community compos In the field B. oleracea cultivars differed widely in species richness and composition of the herbivore community, as well as in the density of insects they harbored. Plants with high concentrations of the short side chain alkenyl glucosinolate, glucoiberin, harbored low herbivore diversity. Higher biodiversity was found when plants had glucosinolate profiles containing high concentrations of glucosinolates with elongated side chains, which are biosynthetically linked to glucoiberin. Although gl
  • Behavioral Ecology

    Competition and brood reduction: testing alternative models of clutch-size evolution in parasitoids

    J.J. Pexton, J.P. Boer, G.E. Heimpel, Louise E.M. Vet, J. Whitfield, P.J. Ode
    Competition between siblings occurs in many taxa including parasitoid wasps. Larvae of solitary species eliminate competitors by engaging in aggressive behavior, thus restricting brood size to a single individual. In gregarious species, more than one offspring can develop per host. There are 2 models by which gregariousness can arise in a population of solitary individuals: 1) through a reduction in larval mobility (with the retention of aggressive behavior) or 2) through a reduction in fighting behavior or ability. When more larvae are present than can be supported by available host resources, these 2 models make opposing predictions regarding the process of brood size reduction: Mortality occurring early in larval development under the reduced mobility hypothesis versus mortality occurring throughout larval development under the reduced aggression hypothesis. Here, we measure changes in brood size over the course of larval development of the gregarious parasitoid, Cotesia flavipes. Superparasitized hosts contained approximately twice as many C. flavipes eggs as hosts parasitized by a single parasitoid female. Brood sizes in superparasitized hosts declined gradually as C. flavipes individuals developed, whereas brood sizes remained constant during larval development in singly parasitized hosts. An absence of wounded or destroyed larvae suggested no aggressive behavior. Collectively, these results support the reduced aggression hypothesis.
  • Functional Ecology

    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.
  • Oikos

    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.
  • Functional Ecology

    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
  • Oecologia

    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.
  • Ecological Entomology

    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.
  • Animal Behaviour

    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.
  • Journal of Chemical Ecology

    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.
  • Genetics

    Experimental Support for Multiple-Locus Complementary Sex Determination in the Parasitoid Cotesia vestalis

    J.G. de Boer, P.J. Ode, A.K. Rendahl, Louise E.M. Vet, J. Whitfield, G.E. Heimpel
    Despite its fundamental role in development, sex determination is highly diverse among animals. Approximately 20% of all animals are haplodiploid, with haploid males and diploid females. Haplodiploid species exhibit diverse but poorly understood mechanisms of sex determination. Some hymenopteran insect species exhibit single-locus complementary sex determination (sl-CSD), where heterozygosity at a polymorphic sex locus initiates female development. Diploid males are homozygous at the sex locus and represent a genetic load because they are inviable or sterile. Inbreeding depression associated with CSD is therefore expected to select for other modes of sex determination resulting in fewer or no diploid males. Here, we investigate an alternative, heretofore hypothetical, mode of sex determination: multiple-locus CSD (ml-CSD). Under ml-CSD, diploid males are predicted to develop only from zygotes that are homozygous at all sex loci. We show that inbreeding for eight generations in the parasitoid wasp Cotesia vestalis leads to increasing proportions of diploid males, a pattern that is consistent with ml-CSD but not sl-CSD. The proportion of diploid males (0.27 ± 0.036) produced in the first generation of inbreeding (mother–son cross) suggests that two loci are likely involved. We also modeled diploid male production under CSD with three linked loci. Our data visually resemble CSD with linked loci because diploid male production in the second generation was lower than that in the first. To our knowledge, our data provide the first experimental support for ml-CSD.
  • Proceedings of the Royal Society B-Biological Sciences

    Species-specific acquisition and consolidation of long-term memory in parasitic wasps

    Hans M. Smid, G. Wang, Tibor Bukovinszky, J.L.M. Steidle, M.A.K. Bleeker, Joop J.A. van Loon, Louise E.M. Vet
    Long-term memory (LTM) formation usually requires repeated, spaced learning events and is achieved by the synthesis of specific proteins. Other memory forms require a single learning experience and are independent of protein synthesis. We investigated in two closely related parasitic wasp species, Cotesia glomerata and Cotesia rubecula, whether natural differences in foraging behaviour are correlated with differences in LTM acquisition and formation. These parasitic wasp species lay their eggs in young caterpillars of pierid butterflies and can learn to associate plant odours with a successful egg laying experience on caterpillars on the odour-producing plant. We used a classical conditioning set-up, while interfering with LTM formation through translation or transcription inhibitors. We show here that C. rubecula formed LTM after three spaced learning trials, whereas C. glomerata required only a single trial for LTM formation. After three spaced learning trials, LTM formation was complete within 4h in C. glomerata, whereas in C. rubecula, LTM formation took 3 days. Linking neurobiology with ecology, we argue that this species-specific difference in LTM acquisition and formation is adaptive given the extreme differences in both the number of foraging decisions of the two wasp species and in the spatial distributions of their respective hosts in nature.
  • Journal of Animal Ecology

    Time allocation of a parasitoid foraging in heterogeneous vegetation: implications for host–parasitoid interactions

    Tibor Bukovinszky, R. Gols, L. Hemerik, J.C. Van Lenteren, Louise E.M. Vet
    1. Changing plant composition in a community can have profound consequences for herbivore and parasitoid population dynamics. To understand such effects, studies are needed that unravel the underlying behavioural decisions determining the responses of parasitoids to complex habitats. 2. T he searching behaviour of the parasitoid Diadegma semiclausum was followed in environments with different plant species composition. In the middle of these environments, two Brassica oleracea plants infested by the host Plutella xylostella were placed. The control set-up contained B. oleracea plants only. In the more complex set-ups, B. oleracea plants were interspersed by either Sinapis alba or Hordeum vulgare. 3. Parasitoids did not find the first host-infested plant with the same speed in the different environments. Sinapis alba plants were preferentially searched by parasitoids, resulting in fewer initial host encounters, possibly creating a dynamic enemy-free space for the host on adjacent B. oleracea plants. In set-ups with H. vulgare, also, fewer initial host encounters were found, but in this case plant structure was more likely than infochemicals to interfere with the searching behaviour of pa 4. On discovering a host-infested plant, parasitoids located the second host-infested plant with equal speed, demonstrating the effect of experience on time allocation. Further encounters with host-infested plants that had already been visited decreased residence times and increased the tendency to leave the environment. 5. Due to the intensive search of S. alba plants, hosts were encountered at lower rates here than in the other set-ups. However, because parasitoids left the set-up with S. alba last, the same number of hosts were encountered as in the other treatments. 6. Plant composition of a community influences the distribution of parasitoid attacks via its effects on arrival and leaving tendencies. Foraging experiences can reduce or increase the importance of enemy-free space for hosts on less attractive plants.
  • Journal of Evolutionary Biology

    Complementary sex determination in the parasitoid wasp Cotesia vestalis (C. plutellae)

    J.G. de Boer, P.J. Ode, Louise E.M. Vet, J. Whitfield, G.E. Heimpel
    In the Hymenoptera, single locus complementary sex determination (sl-CSD) describes a system where males develop either from unfertilized haploid eggs or from fertilized diploid eggs that are homozygous at a single polymorphic sex locus. Diploid males are often inviable or sterile, and are produced more frequently under inbreeding. Within families where sl-CSD has been demonstrated, we predict that sl-CSD should be more likely in species with solitary development than in species where siblings develop gregariously (and likely inbreed). We examine this prediction in the parasitoid wasp genus Cotesia, which contains both solitary and gregarious species. Previous studies have shown that sl-CSD is absent in two gregarious species of Cotesia, but present in one gregarious species. Here, we demonstrate CSD in the solitary Cotesia vestalis, using microsatellite markers. Diploid sons are produced by inbred, but not outbred, females. However, frequencies of diploid males were lower than expected under sl-CSD, suggesting that CSD in C. vestalis involves more than one locus. [KEYWORDS: developmental mortality ; diamondback moth ; diploid males ; inbreeding ; mating system ; sex ratio ]
  • Heredity

    Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis

    J.G. de Boer, P.J. Ode, Louise E.M. Vet, J. Whitfield, G.E. Heimpel
    In the Hymenoptera, males develop as haploids from unfertilized eggs and females develop as diploids from fertilized eggs. In species with complementary sex determination (CSD), however, diploid males develop from zygotes that are homozygous at a highly polymorphic sex locus or loci. We investigated mating behavior and reproduction of diploid males of the parasitoid wasp Cotesia vestalis (C. plutellae), for which we recently demonstrated CSD. We show that the behavior of diploid males of C. vestalis is similar to that of haploid males, when measured as the proportion of males that display wing fanning, and the proportion of males that mount a female. Approximately 29% of diploid males sired daughters, showing their ability to produce viable sperm that can fertilize eggs. Females mated to diploid males produced all-male offspring more frequently (71%) than females mated to haploid males (27%). Daughter-producing females that had mated to diploid males produced more male-biased sex ratios than females mated to haploid males. All daughters of diploid males were triploid and sterile. Three triploid sons were also found among the offspring of diploid males. It has been suggested that this scenario, that is, diploid males mating with females and constraining them to the production of haploid sons, has a large negative impact on population growth rate and secondary sex ratio. Selection for adaptations to reduce diploid male production in natural populations is therefore likely to be strong. We discuss different scenarios that may reduce the sex determination load in C. vestalis.
  • Oikos

    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.
  • Oecologia

    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.
  • Ecological Informatics

    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]
  • Behavior Research Methods

    Enter the matrix: How to analyze the structure of behavior

    Lia Hemerik, Tibor Bukovinszky, Rieta Gols, Joop C. van Lenteren, Louise E.M. Vet
    Several methods are available for analyzing different aspects of behavioral transition matrices, but a comprehensive framework for their use is lacking. We analyzed parasitoid foraging behavior in environments with different plant species compositions. The resulting complex data sets were analyzed using the following stepwise procedure. We detected abrupt changes in the event log files of parasitoids, using a maximum likelihood method. This served as a criterion for splitting the event log files into two parts. For both parts, Mantel’s test was used to detect differences between first-order transition matrices, whereas an iterative proportional fitting method was used to find behavioral flows that deviated from random transitions. In addition, hidden repetitive sequences were detected in the transition matrices on the basis of their relative timing, using Theme. We discuss the results for the example from a biological context and the comprehensive use of the different methods. We stress the importance of such a combined stepwise analysis for detecting differences in some parts of event log files.
  • Animal Behaviour

    Differences in memory dynamics between two closely related parasitoid wasp species

    M.A.K. Bleeker, Hans M. Smid, J.L.M. Steidle, Marjolein Kruidhof, Joop J.A. van Loon, Louise E.M. Vet
    The two closely related parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae) coexist in The Netherlands where they occupy slightly different niches. When searching for their caterpillar hosts, they use host plant odours that are released upon feeding by the caterpillars. The species differ in their preference for plant odours during host searching after an associative learning experience. Cotesia glomerata changes its preference for the odour of a particular plant species after an oviposition experience on that plant, whereas C. rubecula does not alter its naïve preference. Using no-choice wind tunnel bioassays we tested, for both species, to what extent oviposition induces memory formation and whether this results from associative learning. In experiment 1 we characterized the temporal dynamics of the memory trace. In both species, oviposition experience induced increased response levels compared to those of naïve wasps. Memory dynamics differed between the species. A single associative learning experience induced a stable long-lasting memory trace that persisted for at least 5 days in C. glomerata. In C. rubecula a memory trace for the odour was present during the first day after the oviposition experience but waned over the following days. From a second experiment we concluded that the increased response could be attributed to a combination of nonassociative and associative learning. We furthermore formulate the learning paradigm for the parasitoids and hypothesize that adaptation to different spatial distributions of the preferred host species has led to the observed differences in memory dynamics.
  • Ecological Entomology

    Effects of aggregation pheromone on individual behaviour and food web interactions: a field study on Drosophila

    B. Wertheim, R. Allemand, Louise E.M. Vet, Marcel Dicke
    The effects of an aggregation pheromone on individual behaviour and food web interactions were investigated in two ecological communities, using Drosophila melanogaster and D. simulans as focal species. 2. Fruit substrates with aggregation pheromone were significantly more attractive to adult D. melanogaster and D. simulans than control fruit substrates, and the response was positively dose dependent. Competing species and natural enemies were also significantly attracted to substrates with the aggregation pheromone of D. melanogaster and D. simulans. 3. Significantly more eggs were deposited on pheromone-treated fruits than on control fruits, and the microdistribution of eggs within fruits was correlated to the microdistribution of the pheromone. The aggregation pheromone induced more females to share the breeding site. 4. The extremely high densities of fruit flies in the large aggregations appeared to reduce the oviposition rate of females. Physical interactions with conspecific and heterospecifics were frequently observed in the aggregations, and often led to patch leaving of the fruit flies. 5. Competition for food among larvae occurred at high densities and parasitism was density dependent. Aggregation pheromones can be directly responsible for these patterns through their effects on the con- and heterospecific behaviour. 6. The combined results show that aggregation pheromones affect a multitude of aspects in the ecology of interacting animals. The importance of incorporating the communication signals in ecological theory of aggregations is discussed. [KEYWORDS: Animal aggregations ; communication signals ; competition ; infochemicals ; natural enemies ; pheromone]
  • Journal of Chemical Ecology

    Impact of botanical pesticides derived from Melia azedarach and Azadirachta indica plants on the emission of volatiles that attract parasitoids of the diamondback moth to cabbage plants

    D.S. Charleston, R. Gols, Cees Hordijk, R. Kfir, Louise E.M. Vet, Marcel Dicke
    Herbivorous and carnivorous arthropods use chemical information from plants during foraging. Aqueous leaf extracts from the syringa tree Melia azedarach and commercial formulations from the neem tree Azadirachta indica, Neemix 4.5®, were investigated for their impact on the flight response of two parasitoids, Cotesia plutellae and Diadromus collaris. Cotesia plutellae was attracted only to Plutella xylostella-infested cabbage plants in a wind tunnel after an oviposition experience. Female C. plutellae did not distinguish between P. xylostella-infested cabbage plants treated with neem and control P. xylostella-infested plants. However, females preferred infested cabbage plants that had been treated with syringa extract to control infested plants. Syringa extract on filter paper did not attract C. plutellae. This suggests that an interaction between the plant and the syringa extract enhances parasitoid attraction. Diadromus collaris was not attracted to cabbage plants in a wind tunnel and did not distinguish between caterpillar-damaged and undamaged cabbage plants. Headspace analysis revealed 49 compounds in both control cabbage plants and cabbage plants that had been treated with the syringa extract. Among these are alcohols, aldehydes, ketones, esters, terpenoids, sulfides, and an isothiocyanate. Cabbage plants that had been treated with the syringa extract emitted larger quantities of volatiles, and these increased quantities were not derived from the syringa extract. Therefore, the syringa extract seemed to induce the emission of cabbage volatiles. To our knowledge, this is the first example of a plant extract inducing the emission of plant volatiles in another plant. This interesting phenomenon likely explains the preference of C. plutellae parasitoids for cabbage plants that have been treated with syringa extracts. [KEYWORDS: Botanical pesticides ; parasitoid behavior ; Plutella xylostella ; induced plant volatiles - elicitor]
  • Biological Control

    Impact of botanical extracts derived from Melia azedarach and Azadirachta indica on populations of Plutella xylostella and its natural enemies: A field test of laboratory findings

    D.S. Charleston, R. Kfir, Marcel Dicke, Louise E.M. Vet
    Differences between results from ecological laboratory studies and what actually happens in the field can be large. Therefore, field experiments are essential to validate laboratory findings. In previous laboratory trials we investigated the impact of aqueous leaf extracts from the syringa tree, Melia azedarach L. (Meliaceae) and commercial formulations from the neem tree, Azadirachta indica Juss. (Meliaceae), Neemix 4.5®, on the biology and behaviour of the diamondback moth Plutella xylostella and two of its most abundant parasitoids, Cotesia plutellae and Diadromus collaris. In the laboratory we had demonstrated that these botanical extracts had adverse effects on survival, fecundity, development, oviposition and feeding of P. xylostella, but no direct negative effects on the survival and foraging of the parasitoids. In the current study, we verified the importance of these previous laboratory findings through field experiments. We treated cabbage plants in the field with the neem product and syringa extract and assessed the infestation levels of P. xylostella and the parasitism rates by natural enemies. Infestation levels of P. xylostella were similar in the plots treated with the botanical extracts and the control plots. However, the damage in the treated plots was significantly lower than in the control plots, indicating that reduced feeding by P. xylostella was a more important factor in the reduction of damage than the actual population density. The proportion of marketable cabbages was significantly higher in the treatments than in the control. The proportion of parasitoids found emerging from P. xylostella was also significantly higher in the treated plots than in the control plots and direct observations indicated that parasitoids still visited cabbage plants that had been treated with the botanical extracts.
  • Archives of Insect Biochemistry and Physiology

    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]
  • Animal Biology

    Gustatory response and appetitive learning in Microplitis croceipes in relation to sugar type and concentration

    F.L. Wäckers, C. Bonifay, Louise E.M. Vet, W.J. Lewis
    Insects can be conditioned to respond to odours through associative learning. Various learning parameters, such as the rate of odour acquisition, are known to depend on the type of conditioned stimulus. Here we investigate to what extent appetitive conditioning in the parasitoid Microplitis croceipes is also affected by characteristics of the food reward (unconditioned stimulus). We tested 1 M solutions of eight sugars naturally occurring in nectar and honeydew with respect to their effect on parasitoid gustatory response and their suitability as an unconditioned stimulus in the process of associative odour learning. To test for concentration effects, a separate experiment compared parasitoid performance with 1 M and 0.25 M of sucrose, respectively. Only exposure to glucose, fructose, sucrose and melezitose enhanced feeding relative to control individuals provided water. Raffinose, mannose, galactose and melibiose did not increase or decrease consumption, indicating that these sugars are neither phagostimulants nor phagodeterrents. In the conditioning experiments, parasitoids were allowed to feed on a particular sugar solution while being exposed to the floral odour cineole. Parasitoids that had been trained with the stimulatory sugars subsequently showed a clear conditioned feeding response to the cineole. Conditioning with galactose, mannose and melibiose, on the other hand, did not lead to successful odour acquisition. Conditioning with raffinose increased the tendency of the parasitoid to exhibit a conditioned feeding response, even though this response was significantly shorter than the response following training with stimulatory sugars. The level of cineole response was not significantly influenced by the concentration of a sucrose solution, even though the 0.25 M concentration was a weaker feeding stimulant. Our findings indicate that gustatory perception is the principal unconditioned stimulus in appetitive learning. The results with raffinose indicate that postingestive feedback may be involved in food associative learning as well. [KEYWORDS: ODOUR LEARNING ; FOOD CONDITIONING ; REWARD QUALITY ; NECTAR ; HONEYDEW ; POST-INGESTIVE FEEDBACK]
  • Journal of Insect Behavior

    Flexible use of patch-leaving mechanisms in a prasitoid wasp

    J.S.M. Burger, Y. Huang, L. Hemerik, J.C. Van Lenteren, Louise E.M. Vet
    Classical optimal-foraging theory predicts that a parasitoid is less likely to leave a patch after a host encounter when the host distribution is aggregated, whereas a parasitoid is more likely to leave after a host encounter when the host distribution is regular. Field data on host distributions in the area of origin of the whitefly parasitoid Encarsia formosa showed that whiteflies aggregate at several spatial scales. However, infested leaves most likely contained a single host. This suggests that a host encounter is not enough to decide when to leave. We therefore tested the effect of host distribution and parasitoid experience on patch-leaving behavior. Each parasitoid was observed for several consecutive days in a three-dimensional arena with leaflets containing on average one host per leaflet in an either regular or aggregated host distribution. A proportional hazards model showed that a host encounter decreased the leaving tendency on a leaflet with one host when the time since the latest host encounter was short, but increased the leaving tendency when the time since the latest host encounter was long, independent of host distribution. We conclude that a parasitoid can switch from decreasing to increasing its tendency to leave a patch after a host encounter. We propose two hypotheses that may explain the evolution of such a switching mechanism. [KEYWORDS: optimal foraging ; patch-leaving behavior ; host distribution ; Encarsia formosa ; whitefly]
  • Journal of Chemical Ecology

    Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellén)

    Tibor Bukovinszky, R. Gols, M.A. Posthumus, Louise E.M. Vet, J.C. Van Lenteren
    Differences in allelochemistry of plants may influence their ability to attract parasitoids.We studied responses of Diadegma semiclausum (Hellén), a parasitoid of the diamondback moth (Plutella xylostella L.), to inter- and intraspecific variation in odor blends of crucifers and a non-crucifer species. Uninfested Brussels sprout (Brassica oleracea L. gemmifera), white mustard (Sinapis alba L.), a feral Brassica oleracea, and malting barley (Hordeum vulgare L.) were compared for their attractivity to D. semiclausum in a Y-tube bioassay. Odors from all plants were more attractive to the parasitoid than clean air. However, tested against each other, parasitoids preferred the volatile blend from the three cruciferous species over that of malting barley.Wasps also discriminated between uninfested crucifers: mustard was as attractive as feral B. oleracea, and both were more attractive than Brussels sprout. Attractivity of uninfested plants was compared with that of plants infested by larvae of the host P. xylostella. Host-infested mustard and Brussels sprout were more attractive than uninfested conspecifics. Interestingly, the volatile blends of uninfested white mustard and infested Brussels sprout were equally attractive.We also compared the volatile composition of different plant sources by collecting headspace samples and analysing them with GC-MS. Similarities of volatile profiles were determined by hierarchic clustering and non-metric scaling based on the Horn-index. Due to the absence of several compounds in its blend, the volatile profile of barley showed dissimilarities from blends of crucifers. The odor profile of white mustard was distinctly different from the two Brassicaceae.Feral Brassica oleracea odor profile was different from infested Brussels sprout, but showed overlap with uninfested Brussels sprout. Odor blends from infested and uninfested Brussels sprout were similar, and mainly quantitative differences were found. D. semiclausum appears to discriminate based on subtle differences in volatile composition of odor blends from infested and uninfested plants. [KEYWORDS: Diadegma semiclausum ; Plutella xylostella ; Hordeum vulgare ; Sinapis alba ; Brassica oleracea ; olfactometer ; headspace volatiles ; GC-MS]
  • Bulletin of Entomological Research

    Behavioural responses of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) to extracts derived from Melia azedarach and Azadirachta indica

    D.S. Charleston, R. Kfir, Louise E.M. Vet, Marcel Dicke
    The impact of three different doses of botanical insecticide derived from the syringa tree, Melia azedarach and the neem tree, Azadirachta indica was tested on the behaviour of the diamondback moth, Plutella xylostella (Linnaeus). Both botanical insecticides had a significant impact on larval behaviour. At higher doses the extracts showed feeding deterrent activity, with larvae preferring the untreated sides of cabbage leaves and consuming less of the treated half of cabbage leaves. The botanical insecticides had less of an effect on the oviposition behaviour of P. xylostella moths. In laboratory and glasshouse trials, significantly fewer eggs were oviposited on the plants that had been treated with syringa extracts. Therefore, the syringa extracts appear to have a repellent effect. In contrast, when exposed to the neem extracts the moths did not discriminate between control plants and treated plants. Behavioural observation indicated that, despite the lower number of eggs oviposited on cabbage treated with syringa extracts, the moths chose cabbage treated with the highest dose of syringa more often than they chose control cabbage plants. Similar observations were found in cabbage plants treated with neem, moths chose the medium dose more often than they chose the control. Oviposition and feeding deterrent properties are important factors in pest control, and results from this study indicate that botanical insecticides have the potential to be incorporated into control programmes for P. xylostella in South Africa. [KEYWORDS: Plutella xylostella ; Azadirachta indica ; Melia azedarach ; insecticides ; plant extracts ; South Africa ; control and damage control]
  • Entomologia Experimentalis et Applicata

    Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids

    R. Buitenhuis, Louise E.M. Vet, G. Boivin, J. Brodeur
    In studies of foraging behaviour in a multitrophic context, the fourth trophic level has generally been ignored. We used four aphid hyperparasitoid species: Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), Asaphes suspensus Walker (Hymenoptera: Pteromalidae), Alloxysta victrix (Westwood) (Hymenoptera: Alloxystidae) and Syrphophagus aphidivorus (Mayr) (Hymenoptera: Encyrtidae), to correlate their response to different cues with their ecological attributes such as host range and host stage. In addition, we compared our results with studies of primary parasitoids on the same plantherbivore system. First, the olfactory response of females was tested in a Y-tube olfactometer (single choice: plant, aphid, honeydew, parasitised aphid, aphid mummy, or virgin female parasitoid; dual choice: clean plant, plant with aphids, or planthost complex). Second, their foraging behaviour was described on plants with different stimuli (honeydew, aphids, parasitised aphids, and aphid mummies). The results indicated that olfactory cues are probably not essential cues for hyperparasitoid females. In foraging behaviour on the plant, all species prolonged their total visit time and search time as compared to the control treatment (clean plant). Only A. victrix did not react to the honeydew. Oviposition in mummies prolonged the total visit time because of the long handling time, but the effect of this behaviour on search time could not be determined. No clear correlation between foraging behaviour and host stage or host range was found. In contrast to specialised primary aphid parasitoids that have strong fixed responses to specific kairomones and herbivore-induced synomones, more generalist aphid hyperparasitoids seem to depend less on volatile olfactory stimuli, but show similarities with primary parasitoids in their use of contact cues while searching on a plant. [KEYWORDS: aphid parasitoid ; host search behaviour ; infochemical ; olfaction ; multitrophic interactions ; Hymenoptera ; Megaspilidae ; Pteromalidae ; Alloxystidae ; Encyrtidae ; Dendrocerus carpenteri ; Asaphes suspensus ; Alloxysta victrix ; Syrphophagus ; aphidivorus]
  • Oikos

    The role of pre- and post- alighting detection mechanisms in the responses to patch size by specialist herbivores

    Tibor Bukovinszky, R.P.J. Potting, Yann Clough, J.C. Van Lenteren, Louise E.M. Vet
    Experimental data on the relationship between plant patch size and population density of herbivores within fields often deviates from predictions of the theory of island biogeography and the resource concentration hypothesis. Here we argue that basic features of foraging behaviour can explain different responses of specialist herbivores to habitat heterogeneity. In a combination of field and simulation studies, we applied basic knowledge on the foraging strategies of three specialist herbivores: the cabbage aphid (Brevicoryne brassicae), the cabbage butterfly (Pieris rapae L.) and the diamondback moth (Plutella xylostella L.), to explain differences in their responses to small scale fragmentation of their habitat. In our field study, populations of the three species responded to different sizes of host plant patches (9 plants and 100 plants) in different ways. Densities of winged cabbage aphids were independent of patch size. Egg-densities of the cabbage butterfly were higher in small than in large patches. Densities of diamondback moth adults were higher in large patches than in small patches. When patches in a background of barley were compared with those in grass, densities of the cabbage aphid and the diamondback moth were reduced, but not cabbage butterfly densities. To explore the role of foraging behaviour of herbivores on their response to patch size, a spatially explicit individual-based simulation framework was used. The sensory abilities of the insects to detect and respond to contact, olfactory or visual cues were varied. Species with a post-alighting host recognition behaviour (cabbage aphid) could only use contact cues from host plants encountered after landing. In contrast, species capable with a pre-alighting recognition behaviour, based on visual (cabbage butterfly) or olfactory (diamondback moth) cues, were able to recognise a preferred host plant whilst in flight. These three searching modalities were studied by varying the in flight detection abilities, the displacement speed and the arrestment response to host plants by individuals. Simulated patch size density relationships were similar to those observed in the field. The importance of pre- and post- alighting detection in the responses of herbivores to spatial heterogeneity of the habitat is discussed.
  • Journal of Animal Ecology

    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]
  • American Naturalist

    Linking spatial processes to life-history evolution of insect parasitoids

    T.S. Hoffmeister, B.D. Roitberg, Louise E.M. Vet
    Understanding the evolutionary transition from solitary to group living in animals is a profound challenge to evolutionary ecologists. A special case is found in insect parasitoids, where a tolerant gregarious larval lifestyle evolved from an intolerant solitary ancestor. The conditions for this transition are generally considered to be very stringent. Recent studies have aimed to identify conditions that facilitate the spread of a gregarious mutant. However, until now, ecological factors have not been included. Host distributions and life-history trade-offs affect the distribution of parasitoids in space and thus should determine the evolution of gregariousness. We add to current theory by using deterministic models to analyze the role of these ecological factors in the evolution of gregariousness. Our results show that gregariousness is facilitated through inversely density-dependent patch exploitation. In contrast, host density dependence in parasitoid distribution and patch exploitation impedes gregariousness. Numerical solutions show that an aggressive gregarious form can more easily invade a solitary population than can a tolerant form. Solitary forms can more easily invade a gregarious, tolerant population than vice versa. We discuss our results in light of exploitation of multitrophic chemical cues by searching parasitoids and aggregative and defensive behavior in herbivorous hosts. [KEYWORDS: clutch size ; density dependence ; competition ; foraging behavior ; spatial heterogeneity ; multitrophic interactions]
  • Trends in Ecology & Evolution

    Candidate genes for behavioural ecology

    M.J. Fitzpatrick, Y. Ben-Shahar, Hans M. Smid, Louise E.M. Vet, G. Robinson, M. Sokolowski
    In spite of millions of years of evolutionary divergence, the conservation of gene function is common across distant lineages. As such, genes that are known to influence behaviour in one organism are likely to influence similar behaviours in other organisms. Recent studies of the evolution of behaviour and morphological adaptation support this notion. Thus, the candidate gene approach offers great potential to expand our understanding of behavioural ecology. Changes in the expression of candidate genes can reveal their contribution to behavioural variation and/or phenotypic plasticity. Knowledge of gene function also enables experimental manipulation of behaviour in the lab and in the field. The candidate gene approach provides an accessible and useful tool for generating insights about animals that are not typically associated with genetic experimentation.
  • Entomologia Experimentalis et Applicata

    Importance of host feeding for parasitoids that attack honeydew-producing hosts

    J.S.M. Burger, A. Kormany, J.C. Van Lenteren, Louise E.M. Vet
    Insect parasitoids lay their eggs in arthropods. Some parasitoid species not only use their arthropod host for oviposition but also for feeding. Host feeding provides nutrients to the adult female parasitoid. However, in many species, host feeding destroys an opportunity to oviposit. For parasitoids that attack Homoptera, honeydew is a nutrient-rich alternative that can be directly imbibed from the host anus without injuring the host. A recent study showed that feeding on host-derived honeydew can be an advantageous alternative in terms of egg quantity and longevity. Here we explore the conditions under which destructive host feeding can provide an advantage over feeding on honeydew. For 5 days, Encarsia formosa Gahan (Hymenoptera: Aphelinidae) parasitoids were allowed daily up to 3 h to oviposit until host feeding was attempted. Host feedings were either prevented or allowed and parasitoids had ad libitum access to honeydew between foraging bouts. Even in the presence of honeydew, parasitoids allowed to host feed laid more eggs per hour of foraging per host-feeding attempt than parasitoids that were prevented from host feeding. The higher egg-laying rate was not compromised by survival or by change in egg volume over time. In conclusion, host feeding can provide an advantage over feeding on honeydew. This applies most likely under conditions of high host density or low extrinsic mortality of adult parasitoids, when alternative food sources cannot supply enough nutrients to prevent egg limitation. We discuss how to integrate ecological and physiological studies on host-feeding behavior.
  • Journal of Animal Ecology

    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]
  • 2005

    Enter the matrix: how to analyze the structure of behaviour

    L. Hemerik, Tibor Bukovinszky, R. Gols, J.C. Van Lenteren, Louise E.M. Vet
  • Journal of Insect Behavior

    Close-range host searching behavior of the stemborer parasitoids Cotesia sesamiae and Dentichasmias busseolae: Influence of a non-host plant Melinis minutiflora

    L.S. Gohole, W.A. Overholt, Z.U. Khan, Louise E.M. Vet
    Studies were conducted on the host searching behavior of the larval parasitoid Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae) and the pupal parasitoid Dentichasmias busseolae Heinrich (Hymenoptera: Ichneumonidae), both of which attack lepidopteran (Crambidae, Noctuidae) cereal stemborers. The behavior of D. busseolae was observed in a diversified habitat that consisted of stemborer host plants (maize, Zea mays L. and sorghum, Sorghum bicolor (L). Moench (Poaceae)) and a non-host plant (molasses grass, Melinis minutiflora Beauv. (Poaceae)), while C. sesamiae was observed separately on host plants and molasses grass. In previous olfactometer studies, C. sesamiae was attracted to molasses grass volatiles while hboxD. busseolae was repelled. The aim of the present study was to investigate the influence of molasses grass on close-range foraging behavior of the parasitoids in an arena that included infested and uninfested host plants. Dentichasmias busseolae strongly discriminated between host and non-host plants, with female wasps spending most of the time on infested host plants and least time on molasses grass. Likewise, C. sesamiae spent more time on uninfested and infested host plants than it did on molasses grass in single choice bioassays. While on infested plants, the wasps spent more time foraging on the stem, the site of damage, than on other areas of the plant. Overall, the results indicate that presence of the non-host plant does not hinder close range foraging activities of either parasitoid. [KEYWORDS: Cotesia sesamiae ; Dentichasmias busseolae ; Melinis minutiflora ; stemborer parasitoids ; foraging behavior ; intercropping ; diversified habitat]
  • Ecosystems

    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]
  • Biological Control

    Impact of botanical pesticides derived from Melia azedarach and Azadirachta indica on the biology of two parasitoid species of the diamondback moth

    D.S. Charleston, R. Kfir, Marcel Dicke, Louise E.M. Vet
    The effect of two botanical pesticides was tested on two species of parasitoids, Cotesia plutellae and Diadromus collaris. Aqueous leaf extracts from the syringa tree, Melia azedarach and commercial formulations from the neem tree, Azadirachta indica, Neemix 4.5 were investigated in the laboratory and in a glasshouse. No direct negative effect was recorded on the longevity of the parasitoid species. However, hind tibia length was found to be significantly shorter in male C. plutellae that emerged from Plutella xylostella that had been exposed to syringa extracts. Whether this negatively affects the fitness of male C. plutellae remains unknown. The impact of the botanical extracts on the fitness of D. collaris could not be investigated because the pesticides resulted in a high mortality of P. xylostella hosts. In the glasshouse a significantly higher proportion of P. xylostella were parasitised by C. plutellae on plants treated with botanical pesticides than on the control plants. However, there were no significant differences between the treatments for the proportion of P. xylostella parasitised by D. collaris. Results indicate that these botanical pesticides have the potential to be combined with biological control programs for P. xylostella. [KEYWORDS: Botanical pesticides ; Melia azedarach ; Azadirachta indica ; Cotesia plutellae ; Diadromus collaris ; Plutella xylostella]
  • Annual Review of Entomology

    Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective

    B. Wertheim, E-J.A. van Baalen, Marcel Dicke, Louise E.M. Vet
    Although the use of aggregation pheromones has been reported for hundreds of nonsocial arthropod species, the evolutionary ecological aspects of this behavior have received little attention. Despite the elaborate literature on mechanisms, robust data on costs and benefits of aggregation pheromones are scant. Existing literature indicates that, in contrast to the diversity of mechanisms, the ecological conditions in which aggregation pheromones are used are more alike. This points to a few general categories for costs and benefits of aggregation pheromones, and these are discussed. We subsequently review interspecific interactions that may be affected by the use of aggregation pheromones. We encounter a strikingly frequent association of aggregation pheromones with fungi and microorganisms and address cross-attraction by competitor species and exploitation by natural enemies. We show that aggregative behavior by individuals through the use of pheromones can profoundly affect ecological interactions and advocate further evolutionary and ecological investigations of pheromone-mediated aggregation. [KEYWORDS: Infochemical ; costs ; benefits ; ecological interactions ; community ecology]
  • Oikos

    Reproduction now or later: optimal host-hanling strategies in the whitefly parasitoid Encarsia formosa

    J.S.M. Burger, L. Hemerik, J.C. Van Lenteren, Louise E.M. Vet
    We developed a dynamic state variable model for studying optimal host-handling strategies in the whitefly parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae). We assumed that (a) the function of host feeding is to gain nutrients that can be matured into eggs, (b) oögenesis is continuous and egg load dependent, (c) parasitoid survival is exponentially distributed and (d) parasitoids encounter hosts randomly, are autogenous and have unlimited access to non-host food sources to obtain energy for maintenance and activity. The most important prediction of the model is that host feeding is maladaptive under field conditions of low host density (0.015 cm2) and short parasitoid life expectancy (maximum reproductive period of 7 d). Nutrients from the immature stage that can be matured into eggs are sufficient to prevent egg limitation. Both host density and parasitoid life expectancy have a positive effect on the optimal host-feeding ratio. Parasitoids that make random decisions gain on average only 35% (0.015 hosts cm2) to 60% (1.5 hosts cm2) of the lifetime reproductive success of parasitoids that make optimal decisions, independent of their life expectancy. Parameters that have a large impact on lifetime reproductive success and therefore drive natural selection are parasitoid life expectancy and the survival probability of deposited eggs (independent of host density), the number of host encounters per day (when host density is low) and the egg maturation rate and number of host types (when host density is high). Explaining the evolution of host-feeding behaviour under field conditions requires field data showing that life expectancy in the field is not as short as we assumed, or may require incorporation of variation in host density. Incorporating variation in walking speed, parasitised host types or egg resorption is not expected to provide an explanation for the evolution of host-feeding behaviour under field conditions.
  • Microscopy Research and Technique

    Antennal sensilla of two parasitoid wasps: A comparative scanning electron microscopy study

    M.A.K. Bleeker, Hans M. Smid, A. van Aelst, Joop J.A. van Loon, Louise E.M. Vet
    Two closely related parasitoid wasp species, Cotesia glomerata (L.) and Cotesia rubecula (Marshall) (Hymenoptera:Braconidae), are different in their associative learning of plant odors. To provide a solid basis for our research on the mechanisms that underlie this difference, we described the morphology of the antennal sensilla of these two species using scanning electron microscopy complemented with transmission electron microscopy. Female and male antennae of both species have the same six types of sensilla. We classified these sensilla as sensilla trichodea without pores, sensilla trichodea with a tip pore, sensilla trichodea with wall pores, sensilla coeloconica type I, sensilla coeloconica type II, and sensilla placodea. We conclude that the morphology, numbers, and distribution of the sensory receptors are highly similar in these two closely related wasp species. Differences between species and sexes occurred only in sensilla placodea numbers. C. rubecula has more sensilla placodea than C. glomerata and males of both species have a larger number and a higher density of sensilla placodea compared to females of the same species. [KEYWORDS: Cotesia glomerata, Cotesia rubecula, insect, SEM, TEM]
  • Agriculture, Ecosystems and Environment

    Plant competition in pest-suppressive intercropping systems complicates evaluation of herbivore responses

    Tibor Bukovinszky, H. Tréfás, J.C. Van Lenteren, Louise E.M. Vet, J. Fremont
    In the light of current theories on the effects of intercropping on pest reduction, population responses of the diamondback moth (Plutella xylostella), the cabbage aphid (Brevicoryne brassicae) and the life history traits of the large white butterfly (Pieris brassicae) were studied in a Brussels sprout (Brassica oleracea gemmifera)/malting barley (Hordeum vulgare) additive row intercrop and a Brussels sprout monoculture. More P. xylostella adults were caught in the monoculture than in the intercrop. Numbers of P. xylostella larvae and pupae per sprout plant were lower in intercropped plots than in monocultures. However, more larvae and pupae were found per m2 leaf area in the inter- than in the monocrop. Both the densities per plant and per m2 leaf area of B. brassicae populations were lower in the inter- than in the monocrop. After the barley withered and competition with Brussels sprout abated, aphid densities became higher in the inter- than in the monocrop. These findings may be explained by interspecific plant competition resulting in stressed sprout plants with a smaller size and delayed phenology relative to monocropped plants. Effects of differences in plant nutritional quality on herbivore performance were studied by offering leaves of inter- and monocropped sprout plants to larval P. brassicae. Performance and food utilisation were significantly better on leaves from the intercrop (lower dry weight consumption, higher growth rates) than from the monocrop. Defoliation rate was also higher on leaves of intercropped plants than on monocropped ones. The studies indicate that plant stress and consequent changes in developmental rate and nutritional quality of plants are playing a role in herbivore population responses to intercropping. It is argued that such confounding effects of plant competition in intercropping designs can hamper the evaluation of herbivore responses in pest-suppressive agro-ecosystems. [KEYWORDS: Intercropping; Interspecific competition; "Host plant quality hypothesis"; Brevicoryne brassicae; Plutella xylostella; Pieris brassicae]
  • Ecological Entomology

    Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies

    R. Buitenhuis, G. Boivin, Louise E.M. Vet, J. Brodeur
    1. Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Most parasitoid species have evolved specific adaptations to exploit a single host stage. However, females of the aphid hyperparasitoid Syrphophagous aphidivorus (Mayr) (Hymenoptera: Encyrtidae) display a unique and atypical oviposition behaviour by attacking either primary parasitoid larvae in live aphids, or parasitoid pupae in dead, mummified aphids. 2. In the laboratory, the correlation between host suitability and host preference of S. aphidivorus on the host Aphidius nigripes Ashmead parasitising the aphid Macrosiphum euphorbiae (Thomas) was investigated. 3. The relative suitability of the two host stages was determined by measuring hyperparasitoid fitness parameters (survival, development time, fecundity, sex ratio, and adult size of progeny), and calculating the intrinsic rate of population increase (rm). Host preference by S. aphidivorus females and the influence of aphid defence behaviour on host selection was also examined. 4. Hyperparasitoid offspring performance was highest when developing from hosts in aphid mummies and females consistently preferred this host to hosts in parasitised aphids. Although aphid defensive behaviour may influence host selection, it was not a determining factor. Ecological and evolutionary processes that might have led to dual oviposition behaviour in S. aphidivorus are discussed. [KEYWORDS: Host suitability ; offspring fitness ; oviposition ; preference ; parasitoid life history]
  • Entomologia Experimentalis et Applicata

    Host feeding in insect parasitoids: why destructively feed upon a host that excretes an alternative?

    J.S.M. Burger, T.M. Reijnen, J.C. Van Lenteren, Louise E.M. Vet
    Host feeding is the consumption of host tissue by the adult female parasitoid. We studied the function of destructive host feeding and its advantage over non-destructive feeding on host-derived honeydew in the whitefly parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae). We allowed parasitoids to oviposit until they attempted to host feed. We either prevented or allowed host feeding. Parasitoids had access to sucrose solution, with or without additional access to honeydew. Parasitoids that were allowed to host feed did not have a higher egg load 20 or 48 h after host feeding than parasitoids prevented from host feeding. Host feeding did not increase the number of eggs matured within these periods, nor did the time spent host feeding positively affect any of these response variables. On the other hand, the presence of honeydew did have a positive effect on egg load 20 and 48 h after host feeding compared with parasitoids deprived of honeydew. Parasitoids with access to honeydew matured more eggs within these periods than honeydew-deprived parasitoids. Host feeding increased life expectancy, but this effect was nullified when honeydew was supplied after the host-feeding attempt. In conclusion, feeding on honeydew could be an advantageous alternative to host feeding in terms of egg quantity and longevity. This applies especially to parasitoids exploiting Homoptera, because these parasitoids can obtain honeydew from the host itself. It is possible that destructive host feeding has evolved to enable females to sustain the production of high-quality anhydropic eggs, which may be important in the parasitoid's natural environment. We argue that future studies should take natural alternative food sources into more consideration. [KEYWORDS: life history host-feeding behaviour honeydew fecundity anhydropic eggs longevity Encarsia formosa Hymenoptera Aphelinidae Trialeurodes vaporariorum Homoptera Aleyrodidae]
  • Ecological Entomology

    Natural history of whitefly in Costa Rica: an evolutionary starting point

    J.S.M. Burger, G. Gort, J.C. Van Lenteren, Louise E.M. Vet
    To understand evolution of foraging behaviour in the whitefly parasitoid Encarsia formosa (Hymenoptera, Aphelinidae), natural densities and distributions of whitefly (Homoptera, Aleyrodidae) were quantified in E. formosa's presumed area of origin, the Neotropics. Leaves were collected in Costa Rican nature areas along long transects (2-4 km), short transects (100 m), within 3-D plots (50 dm32.3 m3) and along suspension bridges within the canopy, and checked for presence of whitefly nymphs. Generalised linear mixed modelling revealed that the number of hosts on the lower side of a leaflet of an average plant within an average spot of an average transect could be described by a Poisson distribution with mean and variance equal to 0.241, in a ratio of I1:I2:I3:I4 = 0.14:0.23:0.26:0.37. The Poisson mean was affected largely by the plant and less by the spot or transect. Variation in leaf area explained little of the variation between plants. Based on the shape of the opening in vacate Semivariance analyses showed that in one of the three short transects, the numbers of whiteflies on leaves were spatially dependent. In four of seven 3-D plots at least one level of spatial dependence could be detected. Results are discussed in the context of understanding evolution of foraging behaviour by E. formosa. [KEYWORDS: Aleyrodidae Encarsia formosa ; foraging behaviour; Homoptera host ; density host distribution ; natural history Neotropics ; parasitoid whitefly]
  • IOBC/WPRS Bulletin

    Responses of insect herbivores to habitat texture: the role of foraging strategy

    Tibor Bukovinszky, R.P.J. Potting, Yann Clough, J.C. Van Lenteren, Louise E.M. Vet
  • Basic and Applied Ecology

    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]
  • Cell and Tissue Research

    Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C-rubecula

    Hans M. Smid, M.A.K. Bleeker, Joop J.A. van Loon, Louise E.M. Vet
    Two closely related parasitoid wasp species, Cotesia glomerata and C. rubecula, differ in their use of associative learning. To investigate the neural basis underlying these differences, it is necessary to describe the olfactory pathway of both wasp species. This paper focuses on the organization of the glomeruli in the antennal lobe. Glomeruli were stained by retrograde axon tracing of all axons in the antennal nerve and observed by confocal laser scanning microscopy. Stacks of optical sections were processed with AMIRA software, and 3D digital models of the glomeruli were produced. The combined use of 2D images and 3D surface models of the antennal lobes enabled the identification of a set of corresponding glomeruli in both wasp species. This offers unique opportunities for the study of subtle differences involved in synaptic plasticity that may occur at the glomerular level and factors regulating this plasticity [KEYWORDS: antennal lobe, glomerulus, confocal laser scanning microscopy, digital atlas, axonal tract tracing, Cotesia glomerata, C. rubecula (insecta)]
  • Environmental Entomology

    Effect of a nonhost plant on the location behavior of two parasitoids: The tritrophic system of Cotesia spp. (Hymenoptera : Braconidae), Pieris rapae (Lepidoptera : Pieridae), and Brassica oleraceae

    I. Perfecto, Louise E.M. Vet
    The effect of mixing Brussels sprouts with potato plants on the foraging behavior of two parasitoid species was examined within the tritrophic system of Brassica oleraccae, the herbivore Pieris rapae L. (Lepidoptera: Pieridae), and two parasitoids, Cotesia glomerata L. (Hymenoptera: Braconiadae) and Cotasia rubecula Marshall (Hymenoptera: Braconidae). The two parasitoids differ in the spectrum of host used: C. glomerata, has a wider host range, and C. rubecula has narrower host range, with P. rapae being its preferred host. The experimental design consisted of a completely crossed multifactorial design with the following factors: (1) plant diversity (monoculture and diculture), (2) species of parasitoid (C. glomerata and C. rubecula), and (3) level of experience (naive and experienced individuals). Results indicated that the effect of plant diversity was different for the two parasitoids. Naive C. glomerata, the parasitoid with the wider host range, were less efficient in the diculture than in the monoculture, but this difference disappeared after experience. Ill contrast, naive C. ritbecula were more efficient in the diculture than in the monoculture with experience having no effect. Response level increased for both species after oviposition experience, with G glomerata exhibiting a high degree of behavioral plasticity. Data indicates that the negative effect Of polyculture on the foraging efficiency of C. glomerata is a result of an attraction to the nonhost plant (potatoes) [KEYWORDS: Cotesia glomerata, Colexia rubecula, Pieris rapae, Brassica plants, polycultures, natural enemies]
  • Agriculture, Ecosystems and Environment

    Relative importance of vertebrates and invertebrates in epigeaic weed seed predation in organic cereal fields

    P.R. Westerman, A. Hofman, Louise E.M. Vet, W. Van der Werf
    Exclosure trials were conducted in four organic cereal fields in The Netherlands in 1999 and 2000 to determine the relative importance of vertebrates and invertebrates in weed seed predation. The trials showed that seed predation by vertebrates was rather consistent and predictable, occurring on all fields and both years, being low early in the season, increasing towards mid-June and decreasing thereafter. The occurrence and level of seed predation by invertebrates were unreliable and unpredictable over time. Predation by both vertebrates and invertebrates showed no apparent pattern related to field margin. Vertebrates, presumably mice, accounted for the larger part of weed seed consumption (30–88% per fortnight and farm). Invertebrates, probably granivorous ground beetles, accounted for the smaller part of seed consumption (4–38%). They were the dominant seed predators in only one out of eight cases in July 1999 (74%), and overall contributed little to variability in seed predation [KEYWORDS: Mice; Granivorous ground beetles; Exclosures; Spatial variability; Temporal variability]
  • Entomologia Experimentalis et Applicata

    Role of volatiles emitted by host and non-host plants in the foraging behaviour of Dentichasmias busseolae, a pupal parasitoid of the spotted stemborer Chilo partellus

    L.S. Gohole, W.A. Overholt, Z.U. Khan, Louise E.M. Vet
    The role of volatiles from stemborer host and non-host plants in the host-finding process of Dentichasmias busseolae Heinrich (Hymenoptera: Ichneumonidae) a pupal parasitoid of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) was studied. The non-host plant, molasses grass (Melinis minutiflora Beauv. (Poaceae)), is reported to produce some volatile compounds known to be attractive to some parasitoid species. The studies were conducted to explore the possibility of intercropping stemborer host plants with molasses grass in order to enhance the foraging activity of D. busseolae in such a diversified agro-ecosystem. Olfactometric bioassays showed that volatiles from the host plants maize, Zea mays L., and sorghum, Sorghum bicolor (L.) (Poaceae), were attractive to the parasitoid. Infested host plants were the most attractive. Volatiles from molasses grass were repellent to the parasitoid. Further tests showed that volatiles from infested and uninfested host plants alone were preferred over those from infested and uninfested host plants combined with the non-host plant, molasses grass. In dual choice tests, the parasitoid did not discriminate between volatiles from maize infested by either of the two herbivore species, C. partellus or Busseola fusca Fuller (Lepidoptera: Noctuidae). Volatiles from sorghum infested by C. partellus were preferred over those from C. partellus-infested maize. The study showed that the pupal parasitoid D. busseolae uses plant volatiles during foraging, with those from the plant-herbivore complex being the most attractive. The fact that volatiles from molasses grass were deterrent to the parasitoid suggested that intercropping maize or sorghum with molasses grass was not likely to enhance the foraging behaviour of D. busseolae. Volatiles from the molasses grass may hinder D. busseolae's host location efficiency
  • Journal of Chemical Ecology

    Effects of molasses grass, Melinis minutiflora volatiles on the foraging behavior of the cereal stemborer parasitoid, Cotesia sesamiae

    L.S. Gohole, W.A. Overholt, Z.U. Khan, J.A. Pickett, Louise E.M. Vet
    Olfactory responses of the cereal stemborer parasitoid Cotesia sesamiae to volatiles emitted by gramineous host and nonhost plants of the stemborers were studied in a Y-tube olfactometer. The host plants were maize (Zea mays) and sorghum ( Sorghum bicolor), while the nonhost plant was molasses grass (Melinis minutiflora). In single-choice tests, females of C. sesamiae chose volatiles from infested and uninfested host plants and molasses grass over volatiles from the control (soil). In dual-choice tests, the wasp preferred volatiles from infested host plants to those from uninfested host plants. There was no discrimination between molasses grass volatiles and those of uninfested maize, uninfested sorghum, or infested maize. The wasp preferred sorghum volatiles over maize. Combining uninfested maize or sorghum with molasses grass did not make volatiles from the combination more attractive as compared to only uninfested host plants. Infested maize alone was as attractive as when combined with molasses grass. Infested sorghum was preferred over its combination with molasses grass. Local growth conditions of the molasses grasses influenced attractiveness to the parasitoids. Volatiles from Thika molasses grass were attractive, while those from Mbita molasses grass were not. Growing the Thika molasses grass in Mbita rendered it unattractive and vice versa with the Mbita molasses grass. This is a case of the same genotype expressing different phenotypes due to environmental factors [KEYWORDS: Melinis minutiflora, Cotesia sesamiae, foraging behavior, parasitoid, sorghum, maize, molasses grass, stemborers, olfactometer, plant volatiles, intercropping]
  • Oikos

    Increased risk of parasitism as ecological costs of using aggression pheromones: laboratory and field study of Drosophila-Leptopilina interaction

    B. Wertheim, Louise E.M. Vet, Marcel Dicke
    Information conveyance plays an important role in parasitoid-host interactions. Several sources of information are available for searching parasitoids and exploitation of that information during the different phases of host location depends on its reliability, detectability and accuracy. One source of information especially suitable for exploitation by parasitoids is a host aggregation pheromone, because this often combines all three aspects. In laboratory and field experiments we studied the behavioural responses of the parasitoid Leptopilina heterotoma to the aggregation pheromone of the fruit fly Drosophila melanogaster, both for substrate selection and the behaviour on host substrates. Our results show that substrates with increasing dose of the host's aggregation pheromone attract increasingly more parasitoids, whereas we found no significant effects of pheromone on parasitoid searching behaviour on the substrates. Parasitoid searching behaviour on substrates was influenced by other host cues (e.g. larval excrements, traces of adults other than aggregation pheromone), which is discussed in relation to the expectations from reliability-detectability theory. The responses of the parasitoids were further influenced by substrate quality (i.e. yeast concentration) and the microscale distribution of pheromone. In several field experiments, the fraction of fruit fly larvae that was parasitised was significantly higher in substrates with aggregation pheromone than in control substrates, indicating an ecological cost to the use of aggregation pheromones in adult D. melanogaster
  • 2003

    Variations in natural-enemy foraging behaviour: essential element of a sound biological-control theory

    W.J. Lewis, Louise E.M. Vet, J.H. Tumlinson, J.C. Van Lenteren, D.R. Papaj
    Intraspecific intrinsic variation in foraging behaviour is a common but often overlooked feature of natural enemies. These variations result from adaptations to the variety of foraging circumstances encountered by individuals of the species. We discuss the importance of understanding the mechanisms governing these intrinsic variations and the development of technologies to manage them. Three major sources of variation in foraging behaviour are identified. One source for variation is genotypically fixed differences among individuals that are adapted for different foraging environments. Another source of foraging variation is the phenotypic plasticity that allows individuals to make ongoing modifications of behaviour through learning, which suits them for different host-habitat situations. A third factor in determining variation in foraging behaviour is the natural enemy's physiological state relative to other needs, such as food and mating. A conceptual model is presented for comprehensively examining the respective roles of these variables and their interactive net effect on foraging behaviour. We also discuss proposed avenues for managing these variations in applied biological control programmes.
  • Ecological Entomology

    Allee effect in larval resource exploitation in Drosophila: an interaction among density of adults, larvae and micro-organisms

    B. Wertheim, J. Marchais, Louise E.M. Vet, Marcel Dicke
    1. Aggregation pheromones can evolve when individuals benefit from clustering. Such a situation can arise with an Allee effect, i.e. a positive relationship between individual fitness and density of conspecifics. Aggregation pheromone in Drosophila induces aggregated oviposition. The aim of the work reported here was to identify an Allee effect in the larval resource exploitation by Drosophila melanogaster, which could explain the evolution of aggregation pheromone in this species. 2. It is hypothesised that an Allee effect in D.melanogaster larvae arises from an increased efficiency of a group of larvae to temper fungal growth on their feeding substrate. To test this hypothesis, standard apple substrates were infested with specified numbers of larvae, and their survival and development were monitored. A potential beneficial effect of the presence of adult flies was also investigated by incubating a varying number of adults on the substrate before introducing the larvae. A 3. Fungal growth was related negatively to larval survival and the size of the emerging flies. Although the fungal growth on the substrate was largely reduced at increased larval densities, the measurements of fitness components indicated no Allee effect between larval densities and larval fitness, but rather indicated larval competition. 4. In contrast, increased adult densities on the substrates prior to larval development yielded higher survival of the larvae, larger emerging flies, and also reduced fungal growth on the substrates. Hence, adults enhanced the quality of the larval substrate and significant benefits of aggregated oviposition in fruit flies were shown. Experiments with synthetic pheromone indicated that the aggregation pheromone itself did not contribute directly to the quality of the larval resource.
  • Chemoecology

    GC-EAG-analysis of volatiles from Brussels sprout plants damaged by two species of Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid wasp species

    Hans M. Smid, Joop J.A. van Loon, M.A. Posthumus, Louise E.M. Vet
    Feeding by Pieris brassicae or P. rapae caterpillars on Brussels sprouts plants induces the emission of synomones that attract natural enemies of the caterpillars, Cotesia glomerata, a generalist parasitoid, and C. rubecula, a specialist on P. rapae. Previous research on this tritrophic system has identified a large number of volatiles in the headspace of herbivore-damaged Brussels sprouts plants, and this paper addresses the question which of these volatiles are perceived by the two parasitoid species. Headspace odors from both P. brassicae- and P. rapae-damaged Brussels sprouts plants were analyzed by coupled gas chromatography electro- antennogram (GC-EAG) detection. Twenty volatiles evoked consistent EAG reactions in the antennae of both species and nineteen of these volatiles could be identified with GC-MS. One component that could not be identified due to its low concentration, evoked EAG responses in antennae of C. rubecula only. Possible consequences for searching behavior of the two parasitoid species are discussed. [KEYWORDS: Lepidoptera – Pieridae – Hymenoptera – Braconidae – Cotesia glomerata – Cotesia rubecula – Brussels sprouts – Brassicae oleracea – GC-EAG – tritrophic interactions – specialist – generalist]
  • Entomologia Experimentalis et Applicata

    Behavioural plasticity in support of a benefit for aggregation pheromone use in Drosophila melanogaster

    B. Wertheim, Marcel Dicke, Louise E.M. Vet
    We explored behavioural plasticity in the use of aggregation pheromone in the fruit fly Drosophila melanogaster Meigen (Diptera: Drosophilidae). Based on previous field observations, we formulated two hypotheses on a benefit of using aggregation pheromone for aggregated oviposition. One hypothesis concerns a benefit to the females themselves, where reduced harassment by males can enhance oviposition rate; the other concerns a benefit to their offspring, where larvae can exploit arduous substrates more efficiently. We derive contrasting expectations on the strength of the behavioural response to pheromone for substrates that differ in nutritional quality to larvae. High quality substrates relax the strength of larval competition, which allows for stronger aggregative responses of the females, but conversely, it may yield aggregation less necessary when the benefit is related to resource exploitation by the larvae. In indoor and outdoor dual choice set-ups, we tested the behavioural responses of the adults to the aggregation pheromone with substrates of varying quality, and examined oviposition behaviour. The response of adults to the aggregation pheromone was strong and robust for low quality substrates, but significantly weaker for a high quality substrate. This supports the hypothesis on a benefit to the larvae. Females retained aggregation pheromones in the absence of oviposition substrates for at least 24 h. In the outdoor set-up, substrate with aggregation pheromone received more than three times as many eggs as control substrates, and this was directly related to the number of adults that visited each substrate. Per capita, oviposition rates were not different for differently sized aggregations, and consequently, no evidence was found in support of the hypothesis on reduced harassment. The combination of aggregation pheromone possession and a mutualistic relationship with micro-organisms for Drosophila and other insects is discussed.
  • Proceedings of the section Experimental and Applied Entomology of the Netherlands Entomological Society

    Evaluating pest pressure in the Brussels sprout-barley intercropping system: influence of host plant patch size and surrounding vegetation

    Yann Clough, Tibor Bukovinszky, J.C. Van Lenteren, Louise E.M. Vet
  • Trends in Ecology & Evolution

    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]
  • Ecology Letters

    Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities

    M. Vos, S.M. Berrocal, F. Karamaouna, L. Hemerik, Louise E.M. Vet
    We have examined the effects of herbivore diversity on parasitoid community persistence and stability mediated by nonspecific information from herbivore-infested plants. First, we investigated host location and patch time allocation in the parasitoid Cotesia glomerata in environments where host and/or nonhost herbivores were present on Brassica oleracea leaves. Parasitoids were attracted by infochemicals from leaves containing nonhost herbivores. They spent considerable amounts of time on such leaves. Thus, when information from the plant is indistinct, herbivore diversity is likely to weaken interaction strengths between parasitoids and hosts. In four B. oleracea fields, all plants contained herbivores, often two or more species. We modelled parasitoid-herbivore communities increasing in complexity, based on our experiments and field data. Increasing herbivore diversity promoted the persistence of parasitoid communities. However, at a higher threshold of herbivore diversity, parasitoids became extinct due to insufficient parasitism rates. Thus, diversity can potentially drive both persistence and extinctions. [KEYWORDS: behaviour; diversity; extinction; food web; functional response; incomplete information; information network; parasitoids; persistence; redundancy; stability; synomones Infochemical use; c-rubecula; ecology; model; reliability; complexes; stability; systems; context; webs]
  • Canadian Entomologist

    Fitness, parasitoids and biological control: an opinion

    B.D. Roitberg, G. Boivin, Louise E.M. Vet
    Fitness, defined as the per capita rate of increase of a genotype with reference to the population carrying the associated genes, is a concept used by biologists to describe how well an individual performs in a population. Fitness: is rarely measured directly and biologists resort to proxies more easily measured but with varying connection to fitness. Size, progeny survival, and developmental rate are the most common proxies used in the literature to describe parasitoid fitness. The importance of the proxies varies between papers looking at evolutionary theories and those assessing ecological applications. The most direct measures of fitness for parasitoids are realised fecundity for females and mating ability for males, although these proxies are more difficult to measure under natural conditions. For practical purposes, measure of size, through body size or mass, is the proxy easiest to use while providing good comparative values; however, care must be taken when using a single proxy, as proxies can be affected differently by rearing conditions of the parasitoid. [KEYWORDS: LARVAL COMPETITION; QUALITY-CONTROL; CLUTCH SIZE; HOST; HYMENOPTERA; FIELD; SELECTION; WASP; SUPERPARASITISM; ICHNEUMONIDAE]
  • NWO Newsletter Stimulation Programme Biodiversity

    Studying movement patterns of a specialist parasitoid in simple and diverse cropping systems

    Tibor Bukovinszky, Felix J. J. A. Bianchi, T.M. Estay, H. Trefas, J.C. Van Lenteren, Louise E.M. Vet
  • Applied Entomology and Zoology

    Parasitoid searching efficiency links behaviour to population processes

    Parasitoid searching efficiency is central to parasitoid-host population dynamics, to the evolution of parasitoid and host behaviour, and to the application of parasitoids as natural enemies of insect pests in biological control. Students of parasitoid behaviour attempt to explain variability in parasitoid searching behaviour, while population dynamicists are more concerned with variation in the outcome of parasitism and how this affects the spatial distribution of host mortality and population stability. Unfortunately the links between behaviour and population processes have been rarely explicitly made. Parasitoid searching efficiency potentially links behaviour to population processes since it affects the temporal and spatial heterogeneity of host attacks. But which behaviours determine searching efficiency? In the present paper I attempt to identify some of these key behaviours. They involve responses to cues that help parasitoids to assess important characteristics of the spatial distribution of their hosts such as which food plants hosts are feeding on, the host distribution pattern on food plants and the host density and patch quality. Plant information plays an essential role in many of these processes. In the present paper I will discuss both the behavioural mechanisms involved and the potential effect for population processes. [KEYWORDS: population dynamics, foraging behaviour, tritrophic relationships, learning, spatial ecology]
  • Ecotoxicology

    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]
  • Oecologia

    Coexistence and niche segregation by field populations of the parasitoids Cotestia glomerata and C. rubecula in the Netherlands: predicting field performance from laboratory data

    J.B.F. Geervliet, M.S.W. Verdel, H. Snellen, J. Schaub, Marcel Dicke, Louise E.M. Vet
    Field experiments with foraging parasitoids are essential to validate the conclusions from laboratory studies and to interpret differences in searching and host selection behaviour of parasitoid species. Furthermore, field experiments can indicate whether the parameters measured in the laboratory are relevant to elucidation of the ecological processes under study, such as adaptation or species interactions. In previous extensive laboratory studies we studied plant- and host-searching behaviour, host acceptance, host suitability; host plant preference, and learning of two congeneric parasitoids of Pieris caterpillars: the generalist Cotesia glomerata, which has been reported to attack several Pieridae species, and C. rubecula, a specialist of the small cabbage white Pieris rapae. In the present field study our aim was to verify the importance of these previous laboratory findings for explaining the performance of these two species in the field. We investigated experimentally whether parasitism on three Pieris species varied with parasitoid species and with food plant of the caterpillars. We exposed different types of host plants, infested with different Pieris species, to parasitism by natural populations of Cotesia species, by setting the experimental plants out in Brussels sprouts cabbage fields. Furthermore we made direct observations of parasitoid foraging in the field. In general, the field results confirmed our predictions on the range of host plant and host species used in the field. The two Coresia species appear to coexist through niche segregation, since C. glomerata was mainly recovered from P. brassicae and C. rubecula from P. rapae. Although C. glomerata is a generalist at the species level, it can be a specialist at the population level under certain ecological circumstances. Our study shows the importance of variation in host plant attraction and host species acceptance in restricting host plant and host diet in the field. Furthermore the results suggest that, at least in the Netherlands, specialisation of C. glomerata on P. brassicae may occur as a result of C. rubecula outcompeting C. glomerata in P. rapae larvae [KEYWORDS: hymenoptera; infochemicals; tritrophic interactions; competition; learning]
  • Journal of Chemical Ecology

    From chemical to population ecology: infochemical use in an evolutionary context

    The marriage of chemistry with ecology has been a productive one, providing a wealth of examples of how chemicals play important roles in the loves and lives of living organisms. At first the marriage may have been a simple and monogamous one with the major scientific aim of making proximate analyses of chemically mediated, individual level interactions. But times have changed and chemical ecology is broadening, embracing different approaches and disciplines. There is, for example, increasing appreciation of variability in the systems under study and an increase in evolutionary thinking. Another promising development is greater recognition of the potential importance of chemically mediated interactions for population dynamics and for structuring communities and species coexistence. The latter is an utterly underexplored area in chemical ecology. The field of chemical ecology of insect parasitoids shows some of these promising developments. Responses of parasitoids to infochemicals are increasingly studied with an integrated approach of mechanism and function. This integration of how and why questions significantly enhances the evolutionary and ecological understanding of stimulus–response patterns. The future challenge in chemical ecology is to demonstrate how chemically mediated interactions steer ecological and evolutionary processes at all levels of ecological organization. To reach this goal there is a need for interdisciplinary collaboration among chemists and ecologists working at different levels of organization and with different approaches, with other disciplines as partners.
  • 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.
  • Journal of Insect Physiology

    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.
  • Entomologia Experimentalis et Applicata

    Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula (Hym: Braconidae)

    J.B.F. Geervliet, A.I. Vreugdenhil, Marcel Dicke, Louise E.M. Vet
    Comparison of closely related species can elucidate adaptive differences in species characteristics. The present study compares the effect of experience on the host-finding behaviour of two Cotesia (Hymenoptera: Braconidae) parasitoid species that differ in their degree of specialization. After multiple experiences with host larvae, females of the generalist parasitoid Cotesia glomerata showed a clear preference for volatiles from Pieris brassicae-infested Brussels sprouts leaves over P. rapae-infested Brussels sprouts leaves in two-choice tests (‘preference learning at herbivore level’). A single experience with a host did not lead to such preferences. Experience of adult C. glomerata with different P. brassicae-infested cabbage varieties or nasturtium (Tropaeolum majus L.) led to preferences for the experienced plant-host complex in most cases (‘preference learning at plant level’). No effect of rearing plant (early adult learning) on plant preference was found. In contrast to the generalist C. glomerata, females of the specialist C. rubecula did not show preference learning at the herbivore level. At the plant level, experience with different P. rapae-infested cabbage varieties in no case resulted in a difference in preference between treatments. The results support the hypothesis that learning plays a more important role in searching in generalists than in specialist parasitoids. The behaviour of the generalist C. glomerata was more easily changed by experience than that of the specialist C. rubecula.
  • Biological Control

    Long-distance assessment of patch profitability through volatile infochemicals by the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae)

    J.B.F. Geervliet, S. Ariëns, Marcel Dicke, Louise E.M. Vet
    Using two closely related larval parasitoids (Cotesiaspp.) ofPieriscaterpillars we tested the hypothesis that parasitoids are capable of assessing patchprofitability from a distance by showing differential responses to odors from plants infested with different host densities. We furthermore tested whether experience improves this assessment process. The effect of host densities on the olfactory responses of naive and experienced females was studied in two-choice wind tunnel experiments. Naive females ofCotesiaglomerataandC. rubeculadiscriminated between odors from plants with high and low densities. Responsiveness of naive females to odors from host-infested leaves increased with an increase in the total number of feeding hosts. InC. glomeratasensitivity to low host densities increased after experience. The effect of multiple oviposition experiences ofC. glomerataon different plants with different host densities was measured in two-choice situations. Females indeed use experienced host density of a patch as a cue to establish a preference, but the sequence of the experienced host densities influences the behavior to a great extent. The first experience does not entirely fix their behavior. ForC. glomerata,the retention time of learned odors was 3 days. This study illustrates the importance of quantitative differences in infochemicals to host-foraging decisions from a distance. It further demonstrates how experience can modify the parasitoid's response to variation in resource availability.
  • Animal Behaviour

    The effect of complete versus incomplete information on odour discrimination in a parasitic wasp

    Louise E.M. Vet, A. de Jong, E. Franchi, D.R. Papaj
    We studied the function of learning in the parasitoidLeptopilina heterotomaby looking at discrimination of odour stimuli used in foraging for a host. To optimize the rate of encounters with hosts, these parasitoids are expected to assess the extent to which variation in host–substrate odours is reliably associated with variation in the presence of hosts, that is, substrate profitability. Where the association is reliable, parasitoids should attend to variation in odours and discriminate between them; where it is not, they should ignore it. We hypothesized that foraging decisions are based on the completeness of information the animal has about differences in substrate profitabilities. Our laboratory studies showed that discrimination and non-discrimination of odour stimuli are dynamic behavioural decisions that can be related to the degree of substrate variation and to an animal's informational state. In wind-tunnel studies, females learned to discriminate between odours from substrates that were qualitatively different, for example, between odours from apple and pear substrates or between yeast substrates with different C6compounds added. They did not discriminate when differences were small (e.g. between odours from two apple varieties or between yeast patches with different concentrations of ethyl acetate), unless unrewarding experiences provided evidence of the absence of hosts in one of the substrates. Hence, we suggest that non-discrimination between odour stimuli inL. heterotomais not a lack of ability to discriminate but a functional decision by the parasitoid.
  • Entomologia Experimentalis et Applicata

    Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species)

    J. Brodeur, J.B.F. Geervliet, Louise E.M. Vet
    Host specificity and host selection by insect parasitoids are hypothesized to be correlated with suitability of the hosts for parasitoid development. The present study investigates the correlation between host suitability and earlier studied host-finding behaviour of two closely related braconid larval parasitoid species, the generalist Cotesia glomerata (L.) and the specialist C. rubecula (Marshall) (Hymenoptera: Braconidae). We compared the capability of both parasitoid species to parasitize and develop in three Pieris host species, i.e. P. brassicae (L.), P. rapae (L.) and P. napi (L.) (Lepidoptera: Pieridae). In laboratory experiments, we measured the effect of host species on fitness parameters such as survival, development, sex ratio and size of parasitoid progeny. The results show that C. glomerata is capable of developing in the three host species, with significant differences in parasitoid survival, clutch size and adult weight among Pieris species. The host range for development was more restricted for C. rubecula. Although C. rubecula is physiologically able to develop in P. brassicae larvae, parasitoid fitness is negatively affected by this host species, compared to its most regular host, P. rapae. A comparison of the present data on host suitability with earlier studies on host-searching behaviour suggests that the host-foraging behaviour of both parasitoid species not only leads to selection of the most suitable host species for parasitoid development, but also plays a significant role in shaping parasitoid host range.
  • Journal of Animal Ecology

    Patch exploitation by the parasitoids Cotesia rubecula and Cotesia glomerata in multi-patch environments with different host distributions

    M. Vos, L. Hemerik, Louise E.M. Vet
    1. We analysed the foraging behaviour of two closely related parasitoid species (Cotesia rubecula and Cotesia glomerata) with respect to leaving tendencies from patches in different environments. We investigated how intrapatch experiences like contact with feeding damage and encounters with hosts influence patch leaving decisions. We also estimated the effect of experiences in previously visited patches on leaving decisions in the present patch. 2. For this analysis we applied the proportional hazards model (Cox 1972) to data collected in three versions of a multiple patch set-up. These set-ups consisted of different host species or combinations of host species: (1) Pieris rapae, (2) Pieris brassicae and (3) both P. rapae and P. brassicae. The larvae of these hosts differ in their spatial distribution on plants: P. brassicae occur in clusters and the distribution of larvae is heterogeneous; P. rapae larvae feed solitarily. 3. The specialist parasitoid C. rubecula used a simple strategy: highest leaving tendency on empty leaves, lower leaving tendency on leaves infested with the non-preferred host P. brassicae, lowest leaving tendency on leaves infested with the preferred host, P. rapae. In the environment with both host species, the leaving tendency only decreased on leaves infested with P. rapae. 4. The generalist C. glomerata used a more complex set of rules. (a) Multiple ovipositions on the present patch decreased the leaving tendency on leaves containing the gregarious host. (b) Once the parasitoid had encountered two or more hosts, it had a lower leaving tendency during subsequent patch visits. (c) The leaving tendency increased with the number of visits on infested leaves. In environments where the less preferred host P. rapae was present, C. glomerata switched to the same simple type of rule as used by C. rubecula. 5. Neither of the two Cotesia species used a count-down rule, in which ovipositions increase the leaving tendency. We discuss how patch exploitation by both Cotesia species compares to the patch exploitation mechanisms as proposed by Waage (1979) and Driessen et al. (1995). 6. We formulate an ‘adjustable termination rate’ model for patch exploitation in both Cotesia species in multi-patch environments.
  • Physiological Entomology

    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.
  • Entomologia Experimentalis et Applicata

    Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes

    R.P.J. Potting, H. Snellen, Louise E.M. Vet
    The fitness consequences of superparasitism and the mechanism of host discrimination in Cotesia flavipes, a larval parasitoid of concealed stemborer larvae was investigated. Naive females readily superparasitized and treated the already parasitized host as an unparasitized host by allocating the same amount of eggs as in an unparasitized host. However, there was no significant increase in the number of emerging parasitoids from superparasitized hosts due to substantial mortality of parasitoid offspring in superparasitized hosts. Furthermore, the developmental time of the parasitoids in a superparasitized host was significantly longer than in a singly parasitized host and the emerging progeny were significantly smaller (body length and head width). Naive females entered a tunnel in which the host was parasitized 4 h previously and accepted it for oviposition. Experienced females (oviposition experience in unparasitized host) refused to enter a tunnel with a host parasitized by herself or by another female. In experiments where the tunnel and/or host was manipulated it was demonstrated that the female leaves a mark in the tunnel when she parasitizes a host. The role of patch marking in C. flavipes is discussed in relation to the ecology of the parasitoid.
  • Animal Behaviour

    Absence of odour learning in the stemborer parasitoid Cotesia flavipes

    R.P.J. Potting, H. Otten, Louise E.M. Vet
    Parasitic wasps are commonly found to learn olfactory and visual cues that are associated with successful host location. For many parasitoids the cues that are associated with hosts vary in space and time, and are therefore unpredictable. An ability to learn allows the wasp to concentrate on those cues that will lead it to new hosts most effectively in a particular area. In contrast, parasitoids that forage in a predictable homogeneous environment and/or make only a few foraging decisions do not need to learn and should rely on innate responses to specific cues. The role of learning in host foraging was studied inCotesiaflavipes(Hymenoptera: Braconidae), a parasitoid of stemborer larvae with an ecology where learning is expected to be of low adaptive value. There was no evidence thatC. flavipesuses odourlearning in host-micro-habitat location. There was no significant effect of the development and emergence environment on the response level or preference towards the odour of infested plants. Neither was there evidence that experience with a particular plant–host complex during foraging influences subsequent foraging decisions inC. flavipesfemales. The absence of learning inC. flavipeswhich seems an exception among the parasitoids studied, is discussed in relation to its ecology.
  • Bulletin of Entomological Research

    Geographic variation in host selection behaviour and reproductive success in the stemborer parasitoid Cotesia flavipes (Hymenoptera: Braconidae)

    R.P.J. Potting, Louise E.M. Vet, W.A. Overholt
    Local parasitoid populations may be adapted to their sympatric major plant host complex. Parasitoid strains may thus differ in their propensity to search for a particular micro-habitat or host or they may differ in their physiological compatibility with particular plant or host species. Cotesia flavipes Cameron, a larval parasitoid used worldwide in biological control against tropical stemborers, has a wide host range in diverse habitats. The existence of plant and/or host specific strains in C. flavipes has been postulated. To provide insight into the existence of strains in C. flavipes, we compared the plant/host complex selection behaviour, and physiological compatibility with different stemborers, of six different geographic strains of C. flavipes that differed in the plant/host complex they were obtained from. The results of the host selection experiments indicate that there is no intraspecific variation in host selection behaviour among C. flavipes strains. However, our comparative experiments show variation in reproductive success among strains. The most significant result was that the strain with the longest period of co-existence with the new host Diatraea saccharalis Fabricius had the highest reproductive success on this host species. We argue that the reported existence of C. flavipes strains is based not on differences in host selection behaviour, but on differences in physiological compatibility between local parasitoid and host population.
  • Journal of Chemical Ecology

    Comparative Analysis of Headspace Volatiles from Different Caterpillar-Infested or Uninfested Food Plants of Pieris Species

    J.B.F. Geervliet, M.A. Posthumus, Louise E.M. Vet, Marcel Dicke
    Plants that are infested by herbivores emit volatile cues that can be used by the natural enemies of the herbivores in their search for hosts. Based on results from behavioral studies, we investigated to what extent intact and herbivore-infested plant species and varieties from the food plant range of Pieris herbivore species differ in the composition of the volatile blends. Parasitoids of Pieris species, Cotesia glomerata and C. rubecula, show differential responses towards various herbivore-infested food plants, whereas differences in responses to plants infested by other herbivore species were less clear. Chemical analysis of the headspace samples of red cabbage, white cabbage, and nasturtium plants that were infested by P. brassicae or P. rapae larvae, or that were intact, yielded 88 compounds including alcohols, ketones, aldehydes, esters, nitriles, terpenoids, sulfides, (iso)thiocyanates, carboxylic acids, and others. The analysis revealed that herbivore-infested plants emit the largest number of compounds in the highest amounts. The plant species affected the volatile blend more than did the herbivore species, and differences between plant varieties were less pronounced than differences between plant species. Differences in headspace composition between plants infested by P. brassicae or P. rapae were mainly of a quantitative nature. Herbivore-infested nasturtium differed considerably from the cabbage varieties in a qualitative way. Headspace compositions of red and white cabbage varieties were comparable to that of the food plant Brussels sprouts (Brassica oleracea gemmifera cv. Titurel) as determined in earlier studies in our laboratory. With respect to plant response to herbivory, nasturtium differed considerably from the cabbage varieties analyzed so far and shows resemblance with Lima bean, cucumber, and corn. These plant species produce a greater quantity and variety of volatiles under herbivore attack than intact plants. The results of this study are discussed in relation to behavioral observations on C. glomerata and C. rubecula.
  • Entomologia Experimentalis et Applicata

    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.
  • Journal of Chemical Ecology

    Aggregation pheromones of Drosophila immigrans, D. phalerata and D. subobscura

    K. Hedlund, R.J. Bartelt, Marcel Dicke, Louise E.M. Vet
    Aggregation pheromones ofDrosophila immigrans, D. phalerata andD. subobscura were demonstrated by testing attraction of adult flies to hexane extracts of the flies in a windtunnel bioassay. Extracts of adult males of all species attracted conspecific males and females. However,D. subobscura flies were attracted only when the extract (cVA) in the extracts of adult maleD. immigrans andD. phalerata. Both species were attracted to synthetic cVA. Male and femaleD. phalerata. Both species were attracted to synthetic cVA. Male and femaleD. subobscura produced 5,9-pentacosadiene, 5-pentacosene, 2-methylhexacosene and 5,9-heptacosadiene, while only maleD. subobscura produced (Z)-5-tricosene and minor amounts of cVA
  • Entomologia Experimentalis et Applicata

    The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and a gregarious generalist parasitoid (Cotesia species)

    J. Brodeur, J.B.F. Geervliet, Louise E.M. Vet
    The main objective of this study was to determine the extent to which host acceptance behaviour as related to host species, age, and defensive behaviour might explain the differences in host use that exist between two congeneric and sympatric species of parasitic wasps. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). Cotesia species differed in their responses to host species (P. brassicae (L.), P. napi (L.) and P. rapae) and developmental stage (early and late 1st, 2nd and 3rd instars). In no-choice tests, host acceptance by C. rubecula was higher for P. rapae and females did not distinguish among the 6 host ages. In contrast, when foraging for P. brassicae and P. napi, C. rubecula females more readily attacked early first instar. Cotesia glomerata showed a higher degree of behavioural plasticity towards acceptance of Pieris host species and host age than did C. rubecula. Cotesia glomerata females parasitized the three Pieris species and showed higher acceptance of first and second instars over third instar. Oviposition success was also influenced by host defensive behaviour. The frequency and the effectiveness of defensive behaviour rose with increasing age of the host, P. brassicae being the most aggressive Pieris species. Furthermore, the mean duration of C. glomerata oviposition was significantly reduced by the defensive reactions of P. brassicae, which would likely affect parasitoid fitness as oviposition time is positively correlated to clutch size in C. glomerata. Acceptance frequencies corresponded well to field reports of Pieris-Cotesia associations and to patterns of parasitoid larval performance, suggesting that the acceptance phase might be used as a reliable indicator of Cotesia host-specificity.
  • Oikos

    Generalist and specialist parasitoid strategies of using odours of adult drosophilid flies when searching for their larval hosts

    K. Hedlund, Louise E.M. Vet, Marcel Dicke
    Parasitoids foraging for larvae of Drosophila flies can use odours of adults of their hosts as well as odours of the food of their host larvae. Adult Drosophila deposit volatile aggregation pheromones into a substrate when mating and ovipositing. In this paper three species of parasitoids with different degrees of host specialization are compared in bioassays with regard to innate responses to aggregation pheromones of adult drosophilid hosts. Specialist parasitoids are assumed to use more specific information about their hosts than generalist parasitoids. Two phylogenetically related eucoilid parasitoids, Leptopilina boulardi a host specialist, and L. heterotoma a generalist, were attracted to odours of adult hosts in windtunnel tests. L. heterotoma responded to odours of all species within its host range and one non-host. The specialist L. boulardi was attracted to odours of adult hosts within its range but also to some non-host species. Production of similar pheromonal compounds by non-host and host Drosophila species can explain the reponses by L. heterotoma and L. boulardi to non-host species. A phylogenetically unrelated braconid host specialist Asobara tabida did not respond to any odours of adult hosts. However, when A. tabida females were given an oviposition experience in the presence of host pheromones, they became attracted to aggregation pheromones of their host.
  • Journal of Insect Behavior

    Innate responses of the parasitoid Cotesia glomerata and Cotesia rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes

    J.B.F. Geervliet, Louise E.M. Vet, Marcel Dicke
    To determine and compare innate preferences of the parasitoid speciesCotesia glomerata andC. rubecula for different plant-herbivore complexes, long-range (1-m) foraging behavior was studied in dual-choice experiments in a wind tunnel. In this study we tested the hypothesis that naive females of the specialistC. rubecula should show more pronounced preferences for different plant-herbivore complexes than females of the generalistC. glomerata. The herbivore species used were the pieridsPieris brassicae, P. rapae, P. Napi, andAporia crataegi and the nonhostsPlutella xylostella andMamestra brassicae. All herbivore species feed mainly on cabbage and wild crucifers, exceptAporia crataegi, which feeds on species of Rosaceae. Both parasitoid species preferred herbivore-damaged plants over nondamaged plants. NeitherC. rubecula norC. glomerata discriminated between plants infested by different caterpillar species, not even between plants infested by host-and nonhost species. Both parasitoid species showed preferences for certain cabbage cultivars and plant species. No differences were found in innate host-searching behavior betweenC. glomerata andC. rubecula. The tritrophic system cabbage-caterpillars-Cotesia sp. seems to lack specificity on the herbivore level, whereas on the plant level differences in attractiveness to parasitoids were found.
  • Journal of Insect Behavior

    Egg- laying experience and acceptance of parasitized hosts by the parasitoid Leptopilina heterotoma

    M.M. Henneman, D.R. Papaj, A.J. Figueredo, Louise E.M. Vet
    The influence of egg-laying experience on the response of females of the eucoilid parasitoid,Leptopilina heterotoma, to parasitized and unparasitizedDrosophila melanogaster host larvae was examined under more controlled conditions than those used in past studies. In laboratory assays, we precisely manipulated both the number of eggs laid by females and the kind of larvae (parasitized versus unparasitized) in which the eggs were laid. We found that the tendency to avoid laying eggs in parasitized hosts depended markedly on whether or not eggs had been laid previously, but depended little on whether those eggs had been laid in parasitized or unparasitized hosts. The observed effect of general egg-laying experience on avoidance of parasitized hosts may reflect responses to either changes in the wasp's internal state (perhaps, changes in egg load) or changes in the wasp's neural representation of the external environment (such as those presumed to occur during learning). In light of these results, we offer a tentative reinterpretation of several earlier studies.
  • Journal of Chemical Ecology

    Host microhabitat location by stemborer parasitoid Cotesia flavipes: the role of herbivore volatiles and locally and systemically induced plant volatiles

    R.P.J. Potting, Louise E.M. Vet, Marcel Dicke
    The origin of olfactory stimuli involved in the host microhabitat location inCotesia flavipes, a parasitoid of stem-borer larvae, was investigated in a Y-tube olfactometer. The response of femaleC. flavipes towards different components of the plant-host complex, consisting of a maize plant infested with two or more larvae of the stem borerChilo partellus, was tested in dualchoice tests. The concealed lifestyle of the stem-borer larvae did not limit the emission of volatiles attractive to a parasitoid. A major source of the attractive volatiles from the plant-host complex was the stem-borer-injured stem, including the frass produced by the feeding larvae. Moreover, the production of volatiles attractive to a parasitoid was not restricted to the infested stem part but occurs systemically throughout the plant. The uninfested leaves of a stem-borer-infested plant were found to emit volatiles that attract femaleC. flavipes. We further demonstrate that an exogenous elicitor of this systemic plant response is situated in the regurgitate of a stem-borer larva. When a minor amount of regurgitate is inoculated into the stem of an uninfested plant, the leaves of the treated plant emit volatiles that attract femaleC. flavipes.
  • Physiological Entomology

    Relationships between parasitoid host range and host defense: a comparative study of egg encapsulation in two related parasitoid species

    J. Brodeur, Louise E.M. Vet
    Parasitoid host range may proceed from traits affecting host suitability, traits affecting parasitoid foraging behaviour, or both. We tested the hypothesis that encapsulation can be used as a reliable indicator of parasitoid host range in two closely related larval endoparasitoids of Lepidoptera. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and a generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). We determined the effects of host species (Pieris brassicae (L.), P. napi (L.) and P. rapae) (Lepidoptera: Pieridae) and host developmental stage (early first, second and third instar) on encapsulation of parasitoid eggs. Host species and parasitoid species, as well as the resulting interaction between these two factors had significant effects on encapsulation of Cotesia eggs. Encapsulation in Pieris hosts was much lower for C. glomerata (32%), even when the latter was parasitizing P. rapae. Encapsulation increased with the age of the larvae, although the only significant difference was for C. glomerata. Overall, P. rapae showed a stronger encapsulation reaction than P. brassicae and P. napi. Encapsulation levels of C. glomerata corresponded well to patterns of female host species and host age preference for oviposition and parasitoid larval performance. In contrast, percentages of encapsulation of C. rubecula were not consistent with host preference and host suitability. We argue that encapsulation alone is unlikely to provide a sufficient explanation for C. glomerata and C. rubecula host range.
  • Norwegian Journal of Agricultural Sciences

    Learned odour preferences in the parasitoid Cotesia glomerata

    J.B.F. Geervliet, S.J.A. Ariens, Louise E.M. Vet, Marcel Dicke
  • Journal of Animal Ecology

    Clutch size in a larval-pupal endoparasitoid: Consequences for fitness

    Louise E.M. Vet, A. Datema, A. Janssen, H. Snellen
    1. Aphaereta minuta (Hymenoptera: Braconidae) is a gregarious larval-pupal endoparasitoid of many Diptera species. Several larval instars can be parasitized and the size differences between host species can be considerable. After parasitization, however, the host larva continues to grow and the parasitoid's eggs hatch after the host pupates. We question whether this delay between the moment of oviposition and that of resource availability for offspring development hampered the ovipositing female in making optimal clutch size decisions. 2. Using an optimality approach we analysed the relationship between clutch size (number of eggs) and fitness in different instars of the host Delia antiqua in the laboratory. 3. Clutch size was artificially manipulated, and the relationship between clutch size and fitness was quantified using the following parameters: offspring egg to adult survival, sex ratio of emerging adults and size of emerging daughters (since size and number of eggs are positively correlated, size is a measure of fecundity). 4. Survival to adult stage was slightly positively correlated with clutch size in first instar host larvae and negatively correlated with clutch size in second instar host larvae. Sex ratio (proportion daughters) increased with increasing clutch size. The size of both males and females on emergence was negatively related to clutch size, and more strongly to the number of emerging adults. 5. The calculated Lack clutch size (whereby fitness is maximized per clutch) increased with larval host stage, as did the observed clutch size. 6. For each instar the observed clutch size was lower than the calculated Lack clutch size. We argue that under natural conditions females are selected to lay a clutch lower than the Lack clutch size.
  • Journal of Insect Behavior

    Foraging for solitarily and gregariously feeding caterpillars: a comparison of two related parasitoid species

    J.S.C. Wiskerke, Louise E.M. Vet
    In the present study we apply a comparative approach, in combination with experimentation, to study behavior of two parasitoid species that attack caterpillar hosts with different feeding strategies (gregarious or solitary). In a semifield setup, consisting of clean cabbage plants and plants infested with one of two host species, the foraging behavior of the specialistCotesia rubecula, on obligate parasitoid of solitarily feedingPieris rapae larvae, was compared to that of the generalistCotesia glomerata, a polyphagous parasitoid of several Pieridae species (mainly the gregariously feedingPieris brassicae).Cotesia glomerata displayed equal propensity to search for and parasitize larvae of both host species. AlthoughC. glomerata exhibited a relatively plastic foraging behavior in that it searched differently under different host distribution conditions, its behavior seems more adapted to search for gregariously feeding hosts. Females exhibited a clear area-restricted search pattern and were more successful in finding the gregariously feeding caterpillars.Cotesia rubecula showed a higher propensity to search forP. rapae than forP. brassicae, i.e., females left the foraging setup significantly earlier when their natural hostP. rapae was not present.C. rubecula showed a more fixed foraging behavior, which seems adapted to foraging for solitarily feeding host larvae. In a setup with onlyP. rapae larvae, the foraging strategies of the two parasitoid species were quite similar. In a choice situationC. glomerata did not show a preference for one of the host species, whileCotesia rubecula showed a clear preference for its natural host species. The latter was shown by several behavioral parameters such as the number of first landings, allocation of search time, and percentage parasitization.
  • Animal Behaviour

    Usurpation of host behaviour by a parasitic wasp

    J. Brodeur, Louise E.M. Vet
    Hostbehaviour manipulation was examined in caterpillars, Pieris brassicae , parasitized by the gregarious braconid wasp, Cotesia glomerata. Following egression of the parasitoids from the host, the moribund caterpillar remains on the pupating parasitoids, spins a web over the parasitoid cocoons, and responds aggressively when disturbed. Cross-species experiments indicated that C. glomerata, but not the congener C. rubecula, has the capacity to interfere with the post-egression behaviour of the host. Dying hosts are viewed as a transient 'functional extension' of the parasitoid that may contribute to parasitoid survival during pupal development by protecting the pupae from natural enemies. This is thought to be the first report on hostbehaviour manipulation that occurs beyond the intimate physical association between the parasite and the host.
  • Norwegian Journal of Agricultural Sciences

    The relation between clutch size and fitness in a larval-pupal endoparasitoid

    Louise E.M. Vet, A. Datema, A. Janssen, H. Snellen
  • Norwegian Journal of Agricultural Sciences

    Parasitoid of Drosophila larvae solves foraging problem through infochemical detour: conditions affecting employment of this strategy

    Marcel Dicke, Louise E.M. Vet, J.S.C. Wiskerke, O. Stapel
    Data are presented on long-distance location of hosts by a larval parasitoid of Drosophila simulans, Leptopilina heterotoma. Naive parasitoids responded strongly to a volatile aggregation pheromone, cis-vaccenyl acetate, that is deposited at the oviposition site by recently mated female hosts. This paper was presented at the 5th European Workshop on Insect Parasitoids held in Biri, Norway, on 24-28 May 1994.
  • Entomologia Experimentalis et Applicata

    Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoid Cotesia rubecula

    J.B.F. Geervliet, Louise E.M. Vet, Marcel Dicke
    The role of volatile stimuli in the long-range host-searching behaviour of the specialist parasitoidCotesia rubecula Marshall (Hymenoptera: Braconidae) was studied. Components from the plant-host-complex Brussels sprouts (Brassica oleracea L. var.gemmifera (DC.) Schulz. cv. ‘Titurel’)-Pieris rapae L. (Lepidoptera: Pieridae) were compared for their attractiveness in dual choice tests in a windtunnel. Stimuli from cabbage plants that were mechanically damaged or damaged byP. rapae caterpillars were more attractive to this parasitoid species than stimuli emitted by the host larvae or their faeces. Parasitoids preferred leaves from the plant-host-complex over artificially damaged leaves. Undamaged cabbage plants were the least attractive to the foraging females. These results indicate that in-flight searching behaviour ofC. rubecula is guided by plant-derived information and that for this specialist species more reliable and specific host-derived cues play a minor role at longer distances.
  • Oecologia

    Clutch size in a larval-pupal endoparasitoid: 1. Variation across and within host species

    Louise E.M. Vet, A. Datema, K. van Welzen, H. Snellen
    Clutch size decisions by Aphaereta minuta (Nees) (Hymenoptera: Braconidae), a polyphagous, gregarious, larval-pupal endoparasitoid, were studied under laboratory conditions. This parasitoid attacks larvae of Diptera inhabiting ephemeral microhabitats such as decaying plant and animal material. Females oviposit in young larval stages, but the eventual size of the host pupa determines host food availability for competing offspring. The size of the pupa can differ greatly between host species. We questioned how A. minuta females deal with this delay between the moment of oviposition and eventual host food availability, and whether they make clutch size decisions that benefit their fitness. It was shown that females indeed vary their clutch size considerably and in an adaptive way: (1) females lay larger clutches in larvae of host species that produce larger pupae, even when the larvae are the same size at the moment of oviposition, and (2) females lay larger clutches in larger larvae than in smaller larvae of the same host species. The latter seems functional as larvae parasitized at an older stage indeed developed into larger pupae compared to larvae parasitized at a younger stage. Furthermore, mortality of parasitized young host larvae was greater than that of both unparasitized larvae and parasitized older larvae. Under field conditions the risk of mortality of young host larvae is expected to be even higher due to the limited period of microhabitat (host food) availability, strong scramble type competition between the host larvae, and the longer period of being exposed to predation.
  • Journal of Chemical Ecology

    Relative importance of infochemicals from first and second trophic level in long-range host location by the larval parasitoid Cotesia glomerata

    S. Steinberg, Marcel Dicke, Louise E.M. Vet
    Recently parasitoids were hypothesized to encounter a reliability-detectability problem relating to chemical stimuli from the first and second trophic level, when searching for hosts. The relative role of infochemicals originating from the host,Pieris brassicae (second trophic level), and its food plant, cabbage (first trophic level), have been investigated with respect to long-range host location by the larval parasitoidCotesia glomerata. Flight-chamber dual choice tests showed that uninfested cabbage plants are least attractive to female wasps. Host larvae and their feces were more attractive than clean plants but far less attractive than artificially damaged and herbivore-damaged plants. The plant-host complex, with host larvae actively feeding on the plant, was the most attractive odor source for the parasitoids. The data indicate that one of the solutionsC. glomerata uses to solve the reliability-detectability problem is to respond to infochemicals that are emitted from herbivore-damaged plants. Whether these infochemicals are herbivore-induced synomones that are produced by the plant remains to be demonstrated. Infochemicals emitted by the herbivore or its by-products are of little importance in the foraging behavior ofC. glomerata.
  • Journal of Insect Behavior

    Host recognition by Pimpla instigator F. (Hymenoptera: Ichneumonidae): preferences and learned responses

    J. Schmidt, R.T. Cardé, Louise E.M. Vet
    This study identifies some previously unreported tactile and visual cues used by the pupal parasitoid Pimpla instigatorF. (Ichneumonidae) to recognize potential hosts. Paper cylinders were presented to the wasps as simple models of lepidopteran pupae. Acceptance of these models was evaluated by determining the frequency with which the wasps punctured the cylinders with their ovipositors. The length of the cylinders did not influence acceptance of the models; however, both surface texture and structural modifications to the ends of the cylinder did affect the frequency of punctures. Smooth cylinders were punctured more often than roughened cylinders, and cylinders with closed ends were frequently punctured, whereas open-ended cylinders were consistently rejected. The wasps also discriminated between blue and yellow cylinders and could be trained to associate blue or yellow with the presence of hosts. Preferences were established during a single 90- min training period and persisted for at least 4 days following training.
  • Journal of Insect Behavior

    Responses of a generalist and a specialist parasitoid (Hymenoptera: Eucoilidae) to Drosophilid larval kairomones

    Louise E.M. Vet, M. Sokolowski, D.E. MacDonald, H. Snellen
    Foraging parasitoids are thought to need more specific information than generalists on the presence, identity, availability, and suitability of their insect host species. In the present paper, we compare responses to host kairomones by two phylogenetically related parasitoid species that attack Drosophilidae and that differ in the width of their host range. As predicted, the behavioral response of the parasitoids to host kairomones reflected their difference in host range. The response of the specialist parasitoid Leptopilina boulardiwas restricted to contact kairomones from its natural hosts and one closely related species. In contrast, the generalist parasitoid Leptopilina heterotomaresponded to contact kairomones of a variety of Drosophilidae species.
  • Scientific American

    How Parasitic Wasps Find their Hosts

    J.H. Tumlinson, W.J. Lewis, Louise E.M. Vet
  • 1993

    Learning of host-finding cues by hymenopterous parasitoids

    T.C.J. Turlings, F.L. Wäckers, Louise E.M. Vet, W.J. Lewis, J.H. Tumlinson
  • Oecologia

    Larval parasitoid uses aggregation pheromone of adult hosts in foraging behaviour: a solution to the reliability-detectability problem

    J.S.C. Wiskerke, Marcel Dicke, Louise E.M. Vet
    Parasitoids that forage for herbivorous hosts by using infochemicals may have a problem concerning the reliability and detectability of these stimuli: host stimuli are highly reliable but not very detectable at a distance, while stimuli from the host's food are very detectable but generally not very reliable in indicating host presence. One solution to this problem is to learn to link highly detectable stimuli to reliable but not very detectable stimuli. Ample knowledge is available on how associative learning aids foraging parasitoids in the location of suitable microhabitats. However, in this paper we report on another solution to the reliability-detectability problem and present evidence for an essential, but as yet overlooked, aspect of Drosophila parasitoid ecology. For the first time it is shown that a parasitoid of Drosophila larvae spies on the communication system of adult Drosophila flies to locate potential host sites: naive parasitoids strongly respond to a volatile aggregation pheromone that is deposited in the oviposition site by recently mated female flies. Thus, the parasitoids resort to using highly detectable information from a host stage different from the one under attack (i.e. infochemical detour). The function and ecological implications of these findings are discussed.
  • Biological Control

    The influence of host site experience on subsequent flight behaviour in Microplitis croceipes (Cresson) (Hymenoptera: Braconidae)

    W.A. van Giessen, J. Lewis, Louise E.M. Vet, F.L. Wäckers
    The effect of selected experiences on subsequent flight behavior by the parasitoid Microplitis croceipes, after its arrival at a potential host site, was examined in a flight tunnel. Exposing M. croceipes to host frass from Helicoverpa zea (Boddie) larvae fed fresh cowpea leaves reinforced its sustained flight response to a hexane extract of that same frass, while an exposure to host frass followed by an oviposition reduced subsequent sustained flight responses to the hexane extract. When oviposition experience was given to M. croceipes outside its target area, or when host site appearance was changed after oviposition, no reduction in sustained flight responses was found. Our results suggest that M. croceipes is able to associatively learn the site of oviposition by linking oviposition experiences to spatial information, thereby reducing the frequency of revisitation and self-superparasitism. The ecological significance of these results is discussed.
  • Physiological Entomology

    Effects of experience on parasitoid movement in odour plumes

    Louise E.M. Vet, D.R. Papaj
    ID - 1199Insects commonly improve the effectiveness with which they locate biotic resources through learning, but the mechanism by which experience exerts its effects has rarely been studied in detail. The effect of oviposition experience on upwind movement of the eucoilid parasitoid, Leptopilina heterotoma (Thomson) (Hym.: Eucoilidae), in odour plumes of host microhabitats, was quantified with the use of a Kramer-type locomotion compensator. A 2h exposure to host Drosophila melanogaster larvae in either fermenting apple-yeast or decaying mushroom substrate (known to affect their preference for these odours in glasshouse and field choice experiments) had a number of effects on movement in plumes of each substrate. Females experienced with a particular substrate walked faster and straighter, made narrower turns and spent more time in upwind movement (i.e. toward the source) in a plume of odour from that substrate than in odour from an alternative substrate. Inexperienced females, by contrast, generally showed little or no significant difference in responses to alternative odours. In addition to affecting the mean values of movement parameters, experience also affected variability around those means. When walking speed or path straightness in an odour plume was increased by experience, variability among individuals was correspondingly decreased. The consequences of odour learning for microhabitat choice is discussed briefly.
  • Entomologia Experimentalis et Applicata

    Comparison of learning in related generalist and specialist eucoilid parasitoids

    M.T.T. Poolman Simons, B.P. Suverkropp, Louise E.M. Vet, G. de Moed
    Effects of learning in two microhabitat specialists, Leptopilina boulardi Barbotin et al. and L. fimbriata Kieffer were compared to previous and new results of learning in the microhabitat generalist L. heterotoma Thomson. Females were given one or more oviposition experiences on hosts in different types of substrate. In all species oviposition experience affected the choice for a substrate, although this effect of learning was considerably less in L. fimbriata compared to the other two species. Patch times, known to be highly determined by experience in the generalist L. heterotoma, were much less flexible in the specialists. L. boulardi and L. fimbriata have fixed patch times on their natural substrate and have variable patch times on other substrates only. In all three species one oviposition affected the choice for a substrate. Additional ovipositions showed no different effect. An accumulative effect of the number of ovipositions on patch times was found in L. heterotoma only. Retention of the learning effect was only studied in L. boulardi, and was shown to be similar to that reported for L. heterotoma, i.e. two to three days. Although learning was found in both the generalist and the specialist species studied, it seems to affect their foraging behaviour differently.
  • Behavioral Ecology

    Seasonal dynamic shifts in patch exploitation by parasitic wasps

    B.D. Roitberg, M. Mangel, R.G. Lalonde, C.A. Roitberg, J.J.M. van Alphen, Louise E.M. Vet
    We developed and tested predictions of a dynamic life history model that is concerned with how temperate-zone parasitic wasps adjust patch residence time and tendency to superparasitize when expectation of life and habitat quality varies. The theory predicts that wasps with short life expectancy should continue to search longer and superparasitize more frequently than similar wasps with long life expectancy. Similarly, wasps with long life expectancy that forage in habitats where patches are already heavily exploited should continue to search longer and superparasitize more frequently than similar wasps foraging in habitats where patches are relatively unexploited. In contrast, the theory predicts that wasps with short life expectancy will be insensitive to habitat quality. We tested the predictions on Drosophila parasitoids (Lep-topilina heterotoma) by (1) rearing wasps under fall and summer photoperiod (i.e., short versus long life expectancy) and (2) giving wasps foraging experience on different quality patches (i.e., exploited versus unexploited habitats). Results of the experiments corroborated our predictions. We discuss how parasitic wasp behavior can be shaped by globally predictable and locally unpredictable events.
  • Entomologia Experimentalis et Applicata

    Response of the braconid parasitoid Cotesia (=Apanteles) glomerata (L.) to volatile infochemicals: effects of bioassay set-up, parasitoid age and experience and barometric flux

    S. Steinberg, Marcel Dicke, Louise E.M. Vet, R. Wanningen
    Upon initiating a research project on the role of volatile infochemicals in the tritrophic system Cotesia (=Apanteles) glomerata (L.) - Pieris brassicae (L.) - cabbage, a bioassay was developed to investigate the response of C. glomerata. The bioassay should be effective in terms of high responsiveness and minimum variability and constructed through a comparative approach. Twenty seven treatments, organized in a factorial randomized block design, compared the effect of three bioassay set-ups (glasshouse flight chamber, wind-tunnel and Y-tube olfactometer), three parasitoid age groups (1-2, 4-5 and 8-9 days old females), three pre-treatment experiences (naive, damage experienced and oviposition experienced wasps) and the day-to-day effect on response of C. glomerata to clean cabbage (CC) and planthost complex (PHC) in a dual choice test. The best results with regard to the strength and consistency of response to the PHC were obtained in the glasshouse flight-chamber by 4-5 days old female wasps with either damage or oviposition experience (94 and 90~ respectively). It is therefore recommended as a suitable bioassay for studying the role of volatile infochemicals in host-habitat location by C. glomerata. A day-to-day variation in response was found in the glasshouse and wind-tunnel. It was correlated with the direction of change in barometric pressure within the time period of the experiment, showing that steadily increasing atmospheric pressure yields a significantly higher response than steadily decreasing or fluctuating barometric flux. To control for the day effect it is suggested to conduct further experiments in a block design, having day as a block. Several aspects of the infochemical ecology of C. glomerata are discussed.
  • Proceedings of the section Experimental and Applied Entomology of the Netherlands Entomological Society

    Comparison of two Cotesia species foraging for solitarily and gregariously feeding Pieris host species

    J.S.C. Wiskerke, Louise E.M. Vet
  • Netherlands Journal of Zoology

    How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids

    Louise E.M. Vet, F.L. Wäckers, Marcel Dicke
    Foraging parasitoids may use stimuli that are derived from their host or from the food of their host, often plants. But how usable are 2nd and 1st trophic level stimuli and what is their relative importance in parasitoid foraging? It is argued that foraging parasitoids are facing a reliability-detectability problem: host-derived stimuli are the most reliable in indicating host presence, accessibility and suitability but they are generally hard to detect. Plant stimuli, on the other hand, are easier to detect but arc generally less reliable indicators. Parasitoids have evolved different non-exclusive strategies to solve this problem. (1) Infochemical detour: parasitoids resort to information from other, more detectable, host stages than the one under attack. (2) Herbivore-induced synomones: parasitoids use specific plant produced volatiles that are released upon damage by a specific herbivore species. In the present paper we put most emphasis on a third strategy (3) Associative learning: through associative learning parasitoids link easy-to-detect stimuli to reliable but hard-to-detect stimuli. Specific mechanisms by which associative learning can improve foraging success are discussed.
  • Journal of Insect Behavior

    A variable-response model for parasitoid foraging behaviour

    Louise E.M. Vet, W.J. Lewis, D.R. Papaj, J.C. Van Lenteren
    An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insect's genetic constitution and physiological state, experience ultimately defines the behavioral repertoire under specified environmental circumstances. We present a conceptual variable-response model based on several major observations of a foraging parasitoid's responses to stimuli involved in the hostfinding process. These major observations are that (1) different stimuli evoke different responses or levels of response, (2) strong responses are less variable than weak ones, (3) learning can change response levels, (4) learning increases originally low responses more than originally high responses, and (5) hostderived stimuli serve as rewards in associative learning of other stimuli. The model specifies how the intrinsic variability of a response will depend on the magnitude of the response and predicts when and how learning will modify the insect's behavior. Additional hypotheses related to the model concern how experience with a stimulus modifies behavioral responses to other stimuli, how animals respond in multistimulus situations, which stimuli act to reinforce behavioral responses to other stimuli in the learning process, and finally, how generalist and specialist species differ in their behavioral plasticity. We postulate that insight into behavioral variability in the foraging behavior of natural enemies may be a help, if not a prerequisite, for the efficient application of parasitoids in pest management.
  • Journal of Chemical Ecology

    Odor learning and foraging success in the parasitoid, Leptopilina heterotoma

    D.R. Papaj, Louise E.M. Vet
    A brief 2-hr experience with hostDrosophila larvae in artificial apple-yeast or mushroom microhabitats had three effects on the foraging behavior of femaleLeptopilina heterotoma (Hymenoptera: Eucoilidae) parasitoids under field conditions. First, experienced females released at the center of circular arrays of apple-yeast and mushroom baits were more likely to find a microhabitat over the course of a daily census than naive ones. Second, for those females that found a microhabitat, experienced ones found it faster than naive ones (i.e., experience reduced travel times). Third, females experienced with a particular microhabitat were more likely to find that micro-habitat than an alternative one. Learned preferences were retained for at least one day and possibly as many as seven. Results generally did not depend on the host species (D. melanogaster orD. simulans) with which females were given experience. Females tended to arrive at baits upwind of the point of release, suggesting that odor is involved in finding host microhabitats and, in particular, in learning to find them more effectively. The implications of these results for the application of semiochemicals in biological control are discussed briefly.
  • Physiological Entomology

    A learning-related variation in electroantennogram responses of a parasitic wasp

    Louise E.M. Vet, R. de Jong, W.A. van Giessen, J. Visser
    Odour responses of parasitic insects, in search of their hosts, can change due to experience. Leptopilina heterotoma (Thomson) (Hymenoptera; Eucoilidae), a parasitic wasp of drosophilid larvae, is known to alter its preference for odours emanating from host food substrates through learning. These kinds of behavioural modifications in insects are assumed to be the result of complex processes in the brain. The results presented in this report, however, suggest that this learning-related behavioural variation is not restricted to brain processes but that it involves changes in sensitivity of olfactory receptor neurones.
  • Journal of Chemical Ecology

    Semiochemicals and learning in parasitoids

    Louise E.M. Vet, A.W. Groenewold
    There is increasing evidence that parasitoid responses to semiochemicals, important stimuli in the host location process, are influenced by experience. This paper focuses on the role of learning, in particular associative learning, in responses to odors. Emphasis is placed on associative learning during the adult stage, the influence of preadult experience is discussed briefly. New data on learning in the speciesLeptopilina heterotoma are given. It is demonstrated that females can learn to respond to a novel odor, which they subsequently use in microhabitat selection. Learning was shown to be associative whereby host products (contact kairomone) or an oviposition experience could function as the reinforcers (reward). The effect of learning seemed stronger when parasitoids were rewarded with an oviposition experience. The paper concludes with a discussion on the application of parasitoid learning in pest management.
  • Environmental Entomology

    Variations in parasitoid foraging behavior: Essential element of a sound biological control theory

    W.J. Lewis, Louise E.M. Vet, J.H. Tumlinson, J.C. Van Lenteren, D.R. Papaj
    Intraspecific intrinsic variation in foraging behavior is a common but often overlooked feature of parasitoids. These variations result from adaptations to the variety of foraging circumstances encountered by individuals of the species. We discuss the importance of understanding the mechanisms governing these intrinsic variations and the development of technologies to manage them. Three major sources of variation in foraging behavior are identified. One source for variation is genotypically fixed differences among individuals that are adapted for different foraging environments. Another source of foraging variation is the phenotypic plasticity that allows individuals to make ongoing modifications of behavior through learning, which suits them for different host-habitat situations. A third factor in determining variation in foraging behavior is the parasitoid's physiological state relative to other needs, such as food and mating. A conceptual model is presented for comprehensively examining the respective roles of these variables and their interactive net effect on foraging behavior. We also discuss proposed avenues for managing these variations in applied biological control programs.
  • Journal of Chemical Ecology

    How contact foraging experiences affect preferences for host-related odors in the larval parasitoid Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae)

    T.C.J. Turlings, J.W.A. Scheepmaker, Louise E.M. Vet, J.H. Tumlinson, W.J. Lewis
    Responses of individual females of the parasitoidCotesia marginiventris to the odors of four different complexes of host larvae feeding on leaves were observed in a four-arm olfactometer. The plant-host complexes were composed of fall armyworm (FAW) larvae or cabbage looper (CL) larvae feeding on either corn or cotton seedlings. Prior to testing, each female was given a brief foraging experience on a plant-host complex and was then exposed to the odors of the same complex in the olfactometer. The experienced females responded to familiar odors in a dose-related manner, and these responses were virtually identical to all four complexes. Preferences for the odors of one of two plant-host complexes were tested in dual choice situations. Generally, FAW odors were preferred over CL odors and corn odors over cotton odors. A short foraging experience significantly affected the females' odor preferences in favor of the odors released by the experienced complex. Additional experiments revealed that neither longer bouts of experience nor bouts that included ovipositions resulted in a stronger change in preference. Experience affected preference in combinations where only the host species was varied as well as in combinations where only the plant species was varied. The results, therefore, strongly indicate that both the plants and the hosts somehow are involved in the production and/or release of the semiochemicals that attractC. marginiventris.
  • Journal of Insect Behavior

    Beneficial arthropod behavior mediated by airborne semiochemicals. VIII. Learning of host-related odors induced by a brief contact experience with host by-products in Cotesia marginiventris (Cresson), a generalist larval parasitoid

    T.C.J. Turlings, J.H. Tumlinson, W.J. Lewis, Louise E.M. Vet
    Females of Cotesia marginiventris(Cresson), a generalist larval parasitoid, were observed to respond to host related odors in a four-arm olfactometer. The females were significantly more responsive to the odors after a brief contact experience with host-damaged leaves contaminated with host by products. During the experience, actual encounters with hosts were not required to improve subsequent responses to host-related odors. The response to odors of the plant-host complex with which parasitoids had experience was significantly higher than the response to odors of an alternative plant-host complex. This suggests that the experience effect is due, at least partly, to associative learning. We suspect that females of this generalist parasitoid, as was recently found for those of a specialist, recognize specific semiochemicals when they contact frass of suitable host larvae. The parasitoids, subsequently, associate the surrounding odors with the possible presence of hosts, and use these odors as cues in their search for more hosts. This could be an important component in the host-searching behavior of many parasitoids.
  • Netherlands Journal of Zoology

    Olfactory microhabitat selection in Leptopilina heterotoma (Thomson) (Hym.: Eucoilidae), a parasitoid of Drosophilidae

    Louise E.M. Vet, K. van Opzeeland
    Leptopilina heterotoma (Thomson) and Asobara tabida (Nees), solitary endoparasitoids of frugivorous Drosophila larvae, are assumed to be competitors. Olfactometer experiments showed, however, that the species differ in their preference for microhabitat odours. Whereas A. tabida prefers a fresh fermenting sugar/yeast medium, L. heterotoma prefers this medium in a later stage of decay. These results are confirmed by field observations. This temporal separation between the species, which is not complete because some multiparasitism does occur, may be one of the factors to their coexistence. Odour preference in L. heterotoma is not modified by larval conditioning, but conditioning of the adults significantly influenced their odour response. The ecological significance of such learning is discussed. It is argued that even though such behavioural flexibility may enhance foraging efficiency when resources are unpredictable, it may also influence the amount of competition between the two parasitoid species.
  • Netherlands Journal of Zoology

    Response to kairomones by some alysiine and eucoilid parasitoid species (Hymenoptera).

    Larval parasitoids of frugivorous Drosophila as well as related parasitoid species that attack Drosophila or Fannia species in mushrooms use water soluble larval kairomones in host location. Parasitoids of fungivorous flies allocate more searching time to patches containing a filtrate of mushrooms infested with host larvae compared to patches with a filtrate of uninfested mushrooms. Filtrates of mushrooms infested with a non-host species do not increase their searching time. Studies with parasitoids of frugivorous Drosophila showed that the ability to recognize kairomone is acquired through learning. Females without oviposition experience do not respond differently to patches with and without kairomone. Parasitoids that had learned the kairomone of one drosophilid host species also recognized the kairomone of another host species, which suggests that kairomones from Drosophilidae may be similar.
  • Oikos

    A comparative functional approach to the host detection behaviour of parasitic wasps. II. A quantitative study on eight eucoilid species

    Louise E.M. Vet, K. Bakker
    This paper reports on a comparative study of the host detection behaviour of 8 para- sitoid species belonging to three eucoilid genera. They attack larvae of Drosophilidae in different microhabitats. We measured behavioural variables such as time allocation to components like 'probing the substrate', 'walking' and 'standing still', frequency and duration of and variation in 'probes' and 'walks', searching efficiency and be- havioural reaction to host movement. Variation in several variables is largely con- gruent with the systematic classification of the species in the three genera, and is cor- related with the role different stimuli play in actual host location. There is a signifi- cant positive correlation between the percentage of time spent standing still and the percentage of hosts found through the sensing of host movement. Species that locate their hosts mainly by sensing host movement (Ganapsis spp.) spend most of their time standing still and use their ovipositor in a different way than species that mainly locate their hosts by regularly probing the substrate (Leptopilina spp.). Kleidotoma spp. use a combination of these two stimuli and so show a combined, more complex behaviour. Differences were also found between species of one genus and between strains of one species. Although in general the type of substrate females normally search on or the kind of host species that they attack does not seem to have influenced the searching be- haviour, some small differences between species could be considered adaptations to different environmental conditions. Different species that attack the same host spe- cies in the same microhabitat show great differences in host detection behaviour. For these parasitoid species this may provide a means by which they can coexist.
  • Netherlands Journal of Zoology

    Olfactory microhabitat location in some eucoilid and alysiine species (Hymenoptera), larval parasitoid of Diptera

    This paper is one in a series dealing with comparative studies on the searching behaviour of eucoilid and alysiine parasitoid species. Some aspects of olfactory microhabitat selection were studied in several parasitoids of Drosophilidae and in some related species that attack larvae of larger Diptera. Odour preference experiments showed that the parasitoids of Drosophilidae studied were specific in their response to microhabitat odours. None of the eucoilid parasitoids of Drosophilidae used volatile compounds related to the presence of their host in microhabitat selection. This ability was, however, found in a more host specific eucoilid species and in some Alysiinae species. In a polyphagous species it was shown that the rearing process could influence the response to olfactory host cues, which once again demonstrated the importance of learning in parasitoid behaviour
  • Oikos

    A Comparative Functional Approach to the Host Detection Behaviour of Parasitic Wasps. 1. A Qualitative Study on Eucoilidae and Alysiinae

    Louise E.M. Vet, J.J.M. van Alphen
    We studied host detection behaviour in Alysiinae (Braconidae; Ichneumonoidea) and Eucoilidae (Cynipoidea), the larvae of which are endoparasitoids of fly larvae and in- vestigated whether this behaviour is determined by their descent or can be considered an adaptation to different environments. We compared the searching behaviour of fe- males of 32 alysiine and 25 eucoilid species from a variety of microhabitats and from different dipteran hosts by using qualitative behavioural variables. Three main modes of searching were detected: vibrotaxis, ovipositor searching and antennal searching, and the species could be classified according to the role these different modes play in the detection of host larvae. The searching modes are largely dependent upon the taxonomic position of the species. In most cases species belonging to one genus show a similar behaviour pattern. However, we also encountered examples of radiation; closely related species that search differently. The function of the three searching modes has not been elucidated so far. Therefore we cannot say that similar searching modes in unrelated species are examples of adaptive convergence. Especially in Drosophila parasitoids we encountered great differences in searching behaviour be- tween different species living in the same microhabitat. We believe differences at all levels of searching, including host detection behaviour may contribute to niche segre- gation and create possibilites for different parasitoid species to coexist in the same microhabitat, even when they attack the same host species
  • Animal Behaviour

    Intra- and interspecifichost discrimination in Asobara (Hymenoptera), larval endo-parasitoids of Drosophilidae: comparison between closely related and less related species

    Louise E.M. Vet, M. Meyer, K. Bakker, J.J.M. van Alphen
    Host discrimination studies were conducted with different species of Asobara, which are larval endo-parasitoids of Drosophilidae. Results indicated variable host discrimination which depended on the relatedness of the species. The closely related sibling species Asobara tabida (Nees) and A. rufescens (Foerster) were not only capable of intraspecific discrimination, but also avoided multiparasitism by discriminating between unparasitized host larvae and larvae previously parasitized by females of the other species. This ability to discriminate interspecifically does not seem functional as each species occupies its own microhabitat. As it was shown to be absent in less closely related Asobara species we concluded that interspecific discrimination by A. tabida and A. rufescens was due to their close relationship
  • Oecologia

    The influence of conditioning on olfactory microhabitat and host location in Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae), larval parasitoids of Drosophilidae

    Louise E.M. Vet, K. van Opzeeland
    Olfactory responses of parasitoids can be variable. This was shown by olfactometer experiments with females of two sibling Asobara species, larval endoparasitoids of Drosophilidae. Oviposition experiences of adult female parasitoids significantly altered their behavioural responses in microhabitat and host location. Females needed prior exposure to a host before they were capable of using volatile compounds related to the presence of their host. Asobara tabida (Nees) attacks Drosophila in fermenting fruits and A. rufescens (Foerster) attacks Drosophilidae in decaying plant materials. Naïve females show a strong preference for the odour of their own microhabitat. After experience with their own host and microhabitat, females were repelled by odours of the other microhabitat. lsquoEnforcedrsquo experience with this repellent microhabitat in the laboratory modified the olfactory response from repellency to attraction. It was shown that even the microhabitat odour preference pattern could be changed through experience. This kind of behavioural flexibility may be the rule rather than the exception in many other Hymenopterous parasitoids.
  • Ecological Entomology

    Fitness of two sibling species of Asobara (Braconidae: Alysiinae), larval parasitoids of Drosophilidae in different microhabitats

    Louise E.M. Vet, C. Janse
    1. Two sibling species of larval endoparasitoids of Drosophilidae: Asobara tabida (Nees) and A.rufescens (Foerster) occur in the same macrohabitat, but inhabit different microhabitats. Each species is most attracted by odours of its own microhabitat. 2. In order to assess the adaptive value of the microhabitat preference we studied the survival of both parasitoids in the major host species that occur in these microhabitats. 3. Survival in the major host in the preferred microhabitat was shown to be 40% higher for A.tabida and 30% higher for A.rufescens when compared to survival in the major host in the non-preferred microhabitat. 4. Measurements of developmental rates, specific mortalities and dry weights of the parasitoids suggest that the differential survival is due to differences in synchronization with the hosts. 5. The possible evolutionary consequences of some biological characteristics in Asobara are discussed. Microhabitat selection, differential survival, development and mating behaviour are attributes likely to have played a role in the reduction of gene flow between populations of the ancestral species, either in primary or in secondary sympatry.
  • Oecologia

    Microhabitat location and niche segregation in two sibling species of Drosophilid parasitoids: Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae)

    Louise E.M. Vet, C. Janse, C. Van Achterberg, J.J.M. van Alphen
    Olfactometer tests with Asobara tabida (Nees 1834), a larval endo-parasitoid of frugivorous Drosophilidae showed that females are attracted to the odour of host food: a suspension of living yeast. This attraction decreased as the fermenting medium grew older and became less likely to contain suitable host stages. Olfactometer tests with — what was considered to be — A. tabida from two different microhabitats (fermenting fruits and decaying plants) showed a genetically determined difference in microhabitat odour preference between the two microhabitat lsquostrainsrsquo. Each lsquostrainrsquo preferred the odour of its own microhabitat. This odour preference was not modified by larval conditioning. Hybridization tests indicated that we were dealing with two sibling species: A. tabida and A. rufescens (Foerster 1862), reproductively isolated by a pre-mating isolation mechanism only. Enforced matings resulted in fertile female offspring. Some small morphological differences were detected. The two species live sympatrically, although each inhabits and is most attracted to its own microhabitat.
  • Netherlands Journal of Zoology

    Comparison of the behavioural response of two Leptopilina species (Hymenoptera: Eucoilidae), living in different microhabitats, to kairomones of their host (Drosophilidae)

    Louise E.M. Vet, R. van der Hoeven
    This paper reports on a comparative study on the response of two related parasitoids to kairomone of their hosts. Leptopilina heterotoma (Thomson) attacks larvae of Drosophila in fermenting fruits and Leptopilina fimbriata (Kieffer) attacks larvae of mainly Scaptomyza pallida (Zetterstedt) in decaying plants. In both species the response to water-soluble kairomone involves a reduction in walking speed and an increase in the frequency with which the substrate is probed. However, essential differences in some of the behavioural parameters between the two species were also discovered. Upon encountering a substrate with kairomone L. heterotoma starts to walk more with longer strolls, whereas L. fimbriata is arrested more strongly and starts to walk less with shorter strolls. The differences in response are possibly adaptations to differences in natural host distribution and density as found in the two microhabitats
  • Netherlands Journal of Zoology

    Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym.: Eucoilidae), a parasitoid of fungivorous Drosophila: the influence of conditioning

    This paper deals with the process of olfactory habitat location in Leptopilina clavipes, a larval endo-parasitoid of fungivorous Drosophilidae. Females show a response to the odour of decaying mushrooms in a state likely to contain host larvae. No long-range attraction to host larvae was detected. Attraction to odours from a different microhabitat (fermenting fruits) was shown to be influenced by different types of conditioning. When reared in hosts on a yeast medium, yeast odours were highly attractive to the emerged adult parasitoids, but mushroom odours were still preferred. Conditioning during oviposition (associative learning) was proven to be much stronger, as it did modify the habitat odour preference-pattern. The ecological significance of the learning process is discussed. It is suggested that the function of learning in search is to optimize the discovery and utilization of resources which fluctuate in abundance and time.
  • Physiological Entomology

    An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects

    Louise E.M. Vet, J.C. Van Lenteren, M. Heymans, E. Meelis
    A new type of airflow olfactometer is described, and results given of experiments using it to measure behavioural olfactory responses of hymenopterous parasitoids. Compared with Y-tube olfactometers it shows several advantages. In its exposure chamber four separate abutting odour fields are presented so that the test insect can readily enter and re-enter them. More than one odour (or different concentrations of one odour) can be tested at the same time, thereby providing complex preference test situations. The various behavioural measures that can be assessed in the apparatus are examined and discussed
  • Netherlands Journal of Zoology

    Host-habitat location and host location by Diachasma alloeum Muesebeck (Hym.; Braconidae), a parasitoid of Rhagoletis pomonella Walsh (Dipt.; Tephritidae)

    P.C.G. Glas, Louise E.M. Vet
    Three laboratory experiments were designed to elucidate some of the stimuli that are involved in host micro-habitat searching, the stimulation of host-searching behaviour and in host location by Diachasma alloeum. Visual orientation was found to play an important role in the location of fruits (Crataegus mollis) by D. alloeum. Equal numbers of landings were obtained on host-infested and uninfested haws. A description is presented of the host-searching behaviour by D. alloeum on haws. It was found that probing activity and duration of stay on the fruit are strongly influenced by the presence of a Rhagoletis pomonella larva in the fruit. A quantification was made of the accuracy with which D. alloeum probes the fruit in search of hosts. It is concluded that host movement is the prime stimulus for the location of hosts. Females on haws containing a moving larva exhibited non-random probing. It was found that parasitization of the host by D. alloeum is preceeded by paralyzation of the host. When paralyzed larvae were offered in the same set-up, D. alloeum exhibited random probing.
  • Netherlands Journal of Zoology

    Postovipositional web-spinning behaviour in a hyperparasite, Signiphora coquilletti Ashmead (Hymenoptera: Signiphoridae)

    J.B. Woolley, Louise E.M. Vet
    After oviposition the uniparental hyperparasite Signiphora coquilletti Ashmead was observed to spin a web over her host, Trialeurodes vaporariorum (Westwood) previously parasitized by Encarsia formosa Gahan. Signiphora coquilletti was subsequently reared from webbed T. vaporariorum pupae and from webbed pupae of Tetraleurodes mori (Quaintance), T. stanfordi (Bemis), Aleuroplatus coronatus (Quaintance), and A. gelatinosus (Cockerell). Oviposition and web-spinning behavior of S. coquilletti are described, and the ultrastructure of the webs is discussed. We believe that webs may function as a physical barrier to host searching females of competing Encarsia species, or that they may serve as an intraspecific host-marking device. Two additional hypotheses are that webs afford protection against predation of Signiphora immatures in host pupae, or that they reduce mortality of Signiphora by tying host pupae to leaf surfaces.
  • Journal of Applied Entomology

    The parasite-host relationship between Encarsia formosa Gah. (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Westw.) (Homoptera: Aleyrodidae). X. A comparison of three Encarsia spp. and one Eretmocerus sp. to estimate their potentialities in controlling whitefly on tomatoes in greenhouses with a low temperature regime

    Louise E.M. Vet, J.C. Van Lenteren
    A search was made in California (USA) for alternative parasites able to control the greenhouse whitefly T. vaporariorum (Westw.) on tomatoes in greenhouses with a low temperature regime. The preselection of candidate species for biological control by means of laboratory methods is discussed. Four aphelinid species (Encarsia formosa Gahan, E. pergandiella Howard, E. sp. near meritoria Gahan and Eretmocerus sp.) could be reared and a laboratory method was developed to test their parasitization efficiency at 17 ± 1°C constant temperature: the reproductive capacity of the four species was measured over a period of 20 days. The possible consequences of the different reproductive strategies of these last two species for their use as biological control agents are discussed. No definite answer to the question which of these two species would be most suitable for whitefly control under low temperature conditions could be given, therefore greenhouse experiments have been initiated in the Netherlands and the U.K.
  • Journal of Applied Entomology

    The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). IX. A review of the biological control of the greenhouse whitefly with suggestions for future research

    Louise E.M. Vet, J.C. Van Lenteren, J. Woets
    The parasitic wasp Encarsia formosa is used in many countries to control an important glasshouse pest, Trialeurodes vaporariorum. Increasing energy costs initiated research about breeding tomato varieties that can be grown at lower glasshouse temperatures than usual. Encarsia formosa is, however, not sufficiently efficient in controlling whitefly at these low temperatures. The great success of this biocontrol method forces us to search for a solution either by selecting cold-resistant E. formosa strains, or by screening of other parasites and predators. In this paper the current situation with regard to control of whitefly is evaluated, the knowledge about factors influencing the relationship between host and parasite is reviewed, data about other parasites and predators are given, and evaluation procedures of natural enemies are discussed.