Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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Een bij-zonder kleurrijk landschap in Land van Wijk en Wouden : handreiking 2.0 voor inrichting en beheer voor bestuivende insecten
Rooij, S.A.M. van; Cormont, A. ; Geertsema, W. ; Haag, Martijn ; Opdam, P.F.M. ; Reemer, M. ; Spijker, J.H. ; Snep, R.P.H. ; Steingröver, E.G. ; Stip, Anthonie - \ 2016
Wageningen : Alterra, Wageningen-UR (Alterra-rapport 2720) - 41 p.
biodiversiteit - insect-plant relaties - regionale planning - ecologische hoofdstructuur - landschap - zuid-holland - bestuivers (dieren) - apidae - lepidoptera - biodiversity - insect plant relations - regional planning - ecological network - landscape - pollinators
Het programma Groene Cirkels (van Heineken) heeft het initiatief genomen tot het realiseren van een duurzaam bijenlandschap in het land van Wijk en Wouden. Deze handreiking wil een impuls geven aan het realiseren daarvan. In Nederland hebben we zo’n 350 verschillende wilde bestuivende insectensoorten. Door variatie in onder andere bloemvormen en kelkdiepte en bloeiseizoen zijn er gespecialiseerde insecten nodig, aangepast op bloeivorm en het bloeiseizoen. Ook moet bestuiving plaats kunnen vinden onder verschillende omstandigheden: bij goed en slecht weer, in vroege en late voorjaren. Nu eens doet de ene soort het goed, dan is er weer een andere die het meeste werk verzet. Diversiteit aan bijen, hommels en zweefvliegen geeft zekerheid voor bestuiving door de jaren heen.
Crowdfunding site Muggenradar App
Koenraadt, C.J.M. ; Vliet, A.J.H. van; Vogels, C.B.F. - \ 2016
Wageningen University
flora - fauna - birds - lepidoptera - ecology - population dynamics
De Keizersmantel als indicator voor het herstel van lichte en viooltjesrijke hellingbossen
Omon, B. ; Veling, K. ; Wallis de Vries, M.F. - \ 2015
De Levende Natuur 116 (2015)5. - ISSN 0024-1520 - p. 204 - 207.
bosgebieden - bossen - soortenrijkdom - fauna - lepidoptera - nymphalidae - waardplanten - ecosystemen - habitats - zuid-limburg - bosbeheer - natuurbeheer - woodlands - forests - species richness - host plants - ecosystems - forest administration - nature management
Een deel van de soorten die eens kenmerkend waren voor de hellingbossen in Zuid-Limburg is afgenomen of zelfs verdwenen. Het dichtgroeien van de bossen na het beëindigen van hakhoutbeheer zou een verklaring kunnen zijn, maar is dat ook zo? In dit artikel worden de ecologische eisen van de fauna van hellingbossen besproken aan de hand van de Keizersmantel. Ingegaan wordt op de vraag in welke mate de ecologische randvoorwaarden voor de Keizersmantel worden bepaald door het aanbod van waardplanten en door het microklimaat.
Drought stress affects plant metabolites and herbivore preference but not host location by its parasitoids
Weldegergis, B.T. ; Zhu, F. ; Poelman, E.H. ; Dicke, M. - \ 2015
Oecologia 177 (2015)3. - ISSN 0029-8549 - p. 701 - 713.
volatile emissions - water-stress - abiotic factors - oviposition - genes - biosynthesis - consequences - lepidoptera - complexity - expression
One of the main abiotic stresses that strongly affects plant survival and the primary cause of crop loss around the world is drought. Drought stress leads to sequential morphological, physiological, biochemical and molecular changes that can have severe effects on plant growth, development and productivity. As a consequence of these changes, the interaction between plants and insects can be altered. Using cultivated Brassica oleracea plants, the parasitoid Microplitis mediator and its herbivorous host Mamestra brassicae, we studied the effect of drought stress on (1) the emission of plant volatile organic compounds (VOCs), (2) plant hormone titres, (3) preference and performance of the herbivore, and (4) preference of the parasitoid. Higher levels of jasmonic acid (JA) and abscisic acid (ABA) were recorded in response to herbivory, but no significant differences were observed for salicylic acid (SA) and indole-3-acetic acid (IAA). Drought significantly impacted SA level and showed a significant interactive effect with herbivory for IAA levels. A total of 55 VOCs were recorded and the difference among the treatments was influenced largely by herbivory, where the emission rate of fatty acid-derived volatiles, nitriles and (E)-4,8-dimethylnona-1,3,7-triene [(E)-DMNT] was enhanced. Mamestra brassicae moths preferred to lay eggs on drought-stressed over control plants; their offspring performed similarly on plants of both treatments. VOCs due to drought did not affect the choice of M. mediator parasitoids. Overall, our study reveals an influence of drought on plant chemistry and insect-plant interactions.
Moths in illuminated nights : articificial night effects on moth ecology
Geffen, K.G. van - \ 2015
Wageningen University. Promotor(en): Frank Berendse, co-promotor(en): Elmar Veenendaal; Roy van Grunsven. - Wageningen : Wageningen University - ISBN 9789462572300 - 116
lepidoptera - kunstlicht - nacht - belichting - dierecologie - effecten - geometridae - diergedrag - artificial light - night - illumination - animal ecology - effects - animal behaviour
Almost all terrestrial species on earth have evolved to be active in a certain part of the day, and as a result are adapted to certain light conditions. Diurnal species are active under high light intensities (the period known as the photophase, i.e. daytime), nocturnal species are active in low light intensities (the period known as the scotophase, i.e. night), and crepuscular species are in between, active in twilight (i.e. dusk and dawn). During the course of evolution, light intensity has been a very reliable cue for the on- and offset of activity of all these species, but recently, the night is no longer dark per definition. Mankind illuminates the night with artificial light sources, which has led to world-wide large-scale alterations of night-scapes. Levels of light pollution continuously rise, currently with approximately 6% per year on average
Insecten in je achtertuin (2) Praktisch: Zo krijg je meer vlinders en bijen in je tuin
Alebeek, Frans van - \ 2015
insects - apidae - lepidoptera - biotopes - habitats - gardens - construction - knowledge - biodiversity
Gunstige referentiewaarden voor populatieomvang en verspreidingsgebied van soorten van bijlage II, IV en V van de Habitatrichtlijn
Ottburg, F.G.W.A. ; Swaay, C.A.M. van - \ 2014
Wageningen : Wettelijke Onderzoekstaken Natuur & Milieu, Wageningen UR (WOt-rapport 124)
amphibia - lepidoptera - vissen - zoogdieren - ongewervelde dieren - mossen - korstmossen - reptielen - populatiebiologie - habitatrichtlijn - fishes - mammals - invertebrates - mosses - lichens - reptiles - population biology - habitats directive
This report presents the Favourable Reference Values for population size and range for the species listed in Annexes II, IV and V of the EU Habitats Directive. These reference values are used to assess the conservation status of species as required by Article 17 of the Habitats Directive. They were determined according to a protocol (checklist) and based on scientific information. Where the required scientific information was not readily available, expert judgement was used to fill the gaps. When determining the reference values, experts on each of the species groups were enlisted from the various voluntary conservation organisations, IMARES Wageningen UR (Texel and IJmuiden) and Alterra Wageningen UR. In addition, two extra questions were answered on how these reference values can be maintained or achieved, and the potential influence of climate warming.
Inheritance of electrophysiological responses to leaf saps of host- and nonhost plants in two helicoverpa species and their hybrids
Tang, Q.B. ; Huang, L.Q. ; Wang, C.Z. ; Tang, Q.B.T. ; Zhan, H. ; Loon, J.J.A. van - \ 2014
Archives of Insect Biochemistry and Physiology 86 (2014)1. - ISSN 0739-4462 - p. 19 - 32.
contact chemoreception - gustatory sensitivity - recognition cue - pieris-rapae - bombyx-mori - larvae - lepidoptera - caterpillars - noctuidae - evolution
The polyphagous cotton bollworm Helicoverpa armigera (Hubner) and the oligophagous oriental tobacco budworm Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae) display contrasting heritable feeding preferences for cotton and pepper leaves. In this study, electrophysiological response patterns to cotton and pepper leaf saps in gustatory sensilla styloconica on the maxillae of these two species, their reciprocal F1 hybrids, and backcrossed lines were investigated using the tip recording technique. The identity of the neurons responding to the two leaf saps has been established using action potential waveform analysis. The two plant leaf saps elicited neural activity in at least six of the eight taste neurons innervating the lateral and medial sensilla styloconica of the parental species and crosses. Discriminant analysis of this multineural input predicted that correct classification occurred in 87 - 92% of the cases. Differences in taste neuron responses between insect lines to the two plant saps were consistent with differences in feeding preference behaviors. Comparisons of taste neuron response patterns of parental species, F1 hybrids and backcrosses indicate that autosomal loci contributed to the difference in gustatory response patterns between the two Helicoverpa species with the H. armigera derived alleles being partly dominant to those carried by H. assulta. These findings contribute to the understanding of gustatory codes for preference and provide insight into taste evolution of lepidopteran insects.
Biodiversiteitsgraadmeters Noord-Holland : status en trend van ecosystemen en soorten
Greft-van Rossum, J.G.M. van der; Knegt, B. de; Wamelink, G.W.W. ; Clement, J. ; Frissel, J.Y. ; Pouwels, R. ; Puijenbroek, P. van; Sanders, M.E. ; Sparrius, L.B. ; Swaay, C.A.M. van; Wegman, R.M.A. - \ 2014
Wageningen : Alterra, Wageningen-UR (Alterra-rapport 2543) - 78
biodiversiteit - ecosystemen - vegetatietypen - fauna - lepidoptera - natuurwaarde - inventarisaties - noord-holland - biodiversity - ecosystems - vegetation types - natural value - inventories
Ondanks het ontbreken van kwantitatieve doelen voor natuurbehoud voor de provincie Noord-Holland kan vastgesteld worden dat het strategische doel van behoud en herstel van de biodiversiteit in de provincie momenteel niet gehaald wordt. De gemiddelde populatieomvang Rode Lijstsoorten is in de provincie Noord-Holland in 2013 gedaald tot 25% van het niveau ten opzichte van 1990. De huidige natuurkwaliteit van ecosystemen varieert tussen 30% en 55% ten opzichte van een ongestoorde situatie. De natuurkwaliteit van het agrarisch gebied, ten opzichte van 1970, bedraagt nog 40%. Deze mag niet direct worden vergeleken met de natuurkwaliteit van ecosystemen, vanwege een andere referentie. Het blijkt dat de totale voorraad biodiversiteit (als product van de oppervlakte natuur en de kwaliteit) is teruggelopen van 41% in 1900, via 26% halverwege de 20e eeuw tot 15% in de huidige situatie. Het areaal natuur neemt weer toe. De provincie Noord-Holland heeft in de beleidsagenda ‘Licht op Groen’ behoud en herstel van biodiversiteit als hoogste doel van het provinciale natuurbeleid geformuleerd. Om het beleid te kunnen monitoren en evalueren heeft Alterra een compacte set biodiversiteitsgraadmeters ontwikkeld die toestand en trend weergeven van biodiversiteit in Noord-Holland op strategisch niveau. Daarnaast worden knelpunten in ruimtelijke en milieucondities weergegeven die (mede) oorzaak zijn van het biodiversiteitsverlies.
Influence of host plant phenology and oviposition date on the oviposition pattern and offspring performance of the butterfly Phengaris alcon
Arnaldo, P.S. ; Gonzalez, D. ; Oliveira, I. ; Langevelde, F. van; Wynhoff, I. - \ 2014
Journal of Insect Conservation 18 (2014)6. - ISSN 1366-638X - p. 1115 - 1122.
maculinea-rebeli - conservation - lepidoptera - lycaenidae - selection - females - larvae
The timing of oviposition and selection of the phenological stage of the host plant can have significant consequences for development and success of offspring, and is particularly important for endangered specialist species with rare habitats, such as Phengaris alcon butterflies. Females of this species oviposit on marsh gentians, Gentiana pneumonanthe. For the first time, we evaluate the survival of eggs deposited by early and late flyers in relation to the phenological stage of marsh gentian flower buds, as well as caterpillar survival and development. An analysis was conducted on 127 gentian shoots, on which 837 eggs were monitored. We observed more frequent oviposition on the apical and youngest buds, with increased egg load by females during the first one-third of the flight period. Offspring survival of about 55 % was observed, with up to 15 caterpillars per bud. Offspring survival was significantly higher from eggs that were oviposited on larger flower buds and on flower buds in an early developmental stage. Also, early flyers’ offspring gave rise to better survival rates and the caterpillar development in flower buds differed significantly according to bud size, with more days required in smaller buds. Finally, the significant differences found across the entire study period illustrate that the understanding of oviposition through time is important to the conservation of this rare European species.
Adaptive developmental plasticity: Compartmentalized responses to environmental cues and corresponding internal signals provide phenotypic flexibility
Mateus, A.R.A. ; Marques-Pita, M. ; Oostra, V. ; Lafuente, E. ; Brakefield, P.M. ; Zwaan, B.J. ; Beldade, P. - \ 2014
BMC Biology 12 (2014). - ISSN 1741-7007 - 15 p.
butterfly bicyclus-anynana - color pattern - wing patterns - distal-less - evo-devo - evolution - size - lepidoptera - integration - eyespots
Background The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity. The effect of the environment on developmental outcomes is typically mediated by hormonal signals which convey information about external cues to the developing tissues. While such plasticity is a wide-spread property of development, not all developing tissues are equally plastic. To understand how organisms integrate environmental input into coherent adult phenotypes, we must know how different body parts respond, independently or in concert, to external cues and to the corresponding internal signals. Results We quantified the effect of temperature and ecdysone hormone manipulations on post-growth tissue patterning in an experimental model of adaptive developmental plasticity, the butterfly Bicyclus anynana. Following a suite of traits evolving by natural or sexual selection, we found that different groups of cells within the same tissue have sensitivities and patterns of response that are surprisingly distinct for the external environmental cue and for the internal hormonal signal. All but those wing traits presumably involved in mate choice responded to developmental temperature and, of those, all but the wing traits not exposed to predators responded to hormone manipulations. On the other hand, while patterns of significant response to temperature contrasted traits on autonomously-developing wings, significant response to hormone manipulations contrasted neighboring groups of cells with distinct color fates. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein. Conclusions Our results unravel the integration of different aspects of the adult phenotype into developmental and functional units which both reflect and impact evolutionary change. Importantly, our findings underscore the complexity of the interactions between environment and physiology in shaping the development of different body parts.
Ecdysteroid hormones link the juvenile environment to alternative adult life histories in a seasonal insect
Oostra, V. ; Mateus, A.R.A. ; Burg, K.R.L. van den; Piessens, T. ; Eijk, M. van; Brakefield, P.M. ; Beldade, P. ; Zwaan, B.J. - \ 2014
American Naturalist 184 (2014)3. - ISSN 0003-0147 - p. E79 - E92.
butterfly bicyclus-anynana - drosophila-melanogaster - phenotypic plasticity - developmental temperature - adaptive responses - thermal plasticity - wing pattern - lepidoptera - diapause - nymphalidae
The conditional expression of alternative life strategies is a widespread feature of animal life and a pivotal adaptation to life in seasonal environments. To optimally match suites of traits to seasonally changing ecological opportunities, animals living in seasonal environments need mechanisms linking information on environmental quality to resource allocation decisions. The butterfly Bicyclus anynana expresses alternative adult life histories in the alternating wet and dry seasons of its habitat as endpoints of divergent developmental pathways triggered by seasonal variation in preadult temperature. Pupal ecdysteroid hormone titers are correlated with the seasonal environment, but whether they play a functional role in coordinating the coupling of adult traits in the alternative life histories is unknown. Here, we show that manipulating pupal ecdysteroid levels is sufficient to mimic in direction and magnitude the shifts in adult reproductive resource allocation normally induced by seasonal temperature. Crucially, this allocation shift is accompanied by changes in ecologically relevant traits, including timing of reproduction, life span, and starvation resistance. Together, our results support a functional role for ecdysteroids during development in mediating strategic reproductive investment decisions in response to predictive indicators of environmental quality. This study provides a physiological mechanism for adaptive developmental plasticity, allowing organisms to cope with variable environments
Drie decennia dagvlinder - en broedvogelmonitoring in het Nationale Park De Hoge Veluwe
Wallis de Vries, M.F. ; Sanders, G. - \ 2014
De Levende Natuur 115 (2014)6. - ISSN 0024-1520 - p. 277 - 283.
lepidoptera - broedvogels - fauna - monitoring - nationale parken - veluwe - breeding birds - national parks
Het Nationale Park De Hoge Veluwe is één van de weinige overgeleven gebieden in Noordwest-Europa waar het heidelandschap zich nog op grote schaal en in zijn ruimtelijke verscheidenheid van stuifzand tot vennen manifesteert. Dankzij een vroeg begin van vlinder- en broedvogelmonitoring in het Park is er veel bekend over de veranderingen in de vlinder- en broedvogelfauna in de laatste drie decennia. Dit artikel vergelijkt de ontwikkelingen in het Park met de landelijke trends.
Food plant and herbivore host species affect the outcome of intrinsic competition among parasitoid larvae
Poelman, E.H. ; Gols, R. ; Gumovsky, A.V. ; Cortesero, A.M. ; Dicke, M. ; Harvey, J.A. - \ 2014
Ecological Entomology 39 (2014)6. - ISSN 0307-6946 - p. 693 - 702.
cotesia-rubecula hymenoptera - endoparasitoid wasps - insect parasitoids - heliothis-virescens - community structure - braconidae - superparasitism - discrimination - solitary - lepidoptera
1. In nature, several parasitoid species often exploit the same stages of a common herbivore host species and are able to coexist despite competitive interactions amongst them. Less is known about the direct effects of resource quality on intrinsic interactions between immature parasitoid stages. The present study is based on the hypothesis that variation in the quality or type of plant resources on which the parasitoids indirectly develop may be complementary and thus facilitate niche segregation favouring different parasitoids in intrinsic competition under different dietary regimes. 2. The present study investigated whether two herbivore species, the cabbage butterflies Pieris brassicae and Pieris rapae (Pieridae), and the quality of two important food plants, Brassica oleracea and Brassica nigra (Brassicaceae), affect the outcome of intrinsic competition between their primary larval endoparasitoids, the gregarious Cotesia glomerata (Braconidae) and the solitary Hyposoter ebeninus (Ichneumonidae). 3. Hyposoter ebeninus is generally an intrinsically superior competitor over C.¿glomerata. However, C.¿glomerata survived more antagonistic encounters with H.¿ebeninus when both developed in P.¿brassicae rather than in P.¿rapae caterpillars, and while its host was feeding on B.¿nigra rather than B.¿oleracea. Moreover, H.¿ebeninus benefitted from competition by its higher survival in multiparasitised hosts. 4. These results show that both plant and herbivore species mediate the battleground on which competitive interactions between parasitoids are played out and may affect the outcomes of these interactions in ways that enable parasitoids to segregate their niches. This in turn may promote coexistence among parasitoid species that are associated with the same herbivore host.
Field evaluation of the synergistic effects of neem oil with Beauveria bassiana (Hypocreales: Clavicipitaceae) and Bacillus thuringiensis var. kurstaki (Bacillales: Bacillaceae)
Togbe, C.E. ; Zannou, E. ; Gbehounou, G. ; Kossou, D. ; Huis, A. van - \ 2014
International Journal of Tropical Insect Science 34 (2014)4. - ISSN 1742-7584 - p. 248 - 259.
metarhizium-anisopliae - azadirachta-indica - natural enemies - cotton bollworm - compatibility - insecticides - coleoptera - curculionidae - coccinellidae - lepidoptera
In the present study, the synergistic effects of Beauveria bassiana (Bals.-Criv. Vuill.) (isolate Bb11) and Bacillus thuringiensis var. kurstaki (Berliner) with neem oil were evaluated in three agroecological zones in Be´nin. Four bioinsecticide treatments (neem oil, neem oil and B. bassiana used separately for different target pests, neem oil mixed with B. bassiana and neem oil mixed with B. thuringiensis) were compared with a calendar-based treatment using synthetic insecticides and a control without insecticides. The bioinsecticide treatments were less effective than the calendar-based treatment at controlling cotton pests. There was no difference in yields and the number of damaged bolls in plots under treatments with the four bioinsecticide formulations, suggesting an absence of synergy between neem oil and B. bassiana and neem oil and B. thuringiensis. The numbers of natural enemies in all the bioinsecticide treatment plots and the control plots were similar and higher than those in the calendar-based treatment plots. The highest yield and profitability were obtained with the calendar-based treatment. Screening the compatibility of plant-based products and biopesticides through bioassays is essential for a successful application of their combinations in any integrated pest management strategy.
Range of attraction of a 6-W moth light trap
Grunsven, R.H.A. van; Lham, D. ; Geffen, K.G. van; Veenendaal, E.M. - \ 2014
Entomologia Experimentalis et Applicata 152 (2014)1. - ISSN 0013-8703 - p. 87 - 90.
lepidoptera - conservation - distance - catches - decline
Tracking butterflies for effective conservation
Swaay, C.A.M. van - \ 2014
Wageningen University. Promotor(en): Michiel Wallis de Vries; Marcel Dicke. - Wageningen : Wageningen University - ISBN 9789461739988 - 218
lepidoptera - zoögeografie - biogeografie - populatiedynamica - natuurbescherming - monitoring - nederland - europa - zoogeography - biogeography - population dynamics - nature conservation - netherlands - europe
Dit proefschrift bestaat uit drie delen: het volgen van veranderingen in de verspreiding van vlinders, het volgen van veranderingen in de populatiegrootte van vlinders en hoe deze kennis te gebruiken voor hun bescherming.
Climbing the walls : behavioural manipulation of insects by baculoviruses
Houte, S. van - \ 2014
Wageningen University. Promotor(en): Just Vlak; Monique van Oers, co-promotor(en): Vera Ros. - Wageningen : Wageningen University - ISBN 9789461738301 - 228
baculoviridae - insecten - rupsen - lepidoptera - gastheer parasiet relaties - diergedrag - gedragsveranderingen - hyperactiviteit - moleculaire biologie - insects - caterpillars - host parasite relationships - animal behaviour - behavioural changes - hyperactivity - molecular biology

Parasites often have severe effects on their hosts by causing developmental and physiological alterations in their hosts. These alterations may contribute to parasite growth, reproduction and survival. For example, host development may be inhibited so that more nutrients become available for the parasite. Parasites can also interfere with host behavior as a strategy to increase parasite survival or transmission. This phenomenon is known as ‘parasitic manipulation’ or ‘behavioural manipulation’. Although many examples of parasitic manipulation are known, the genetic basis underlying such manipulations is largely unexplored. A thorough understanding of how parasites manipulate their hosts’ behavior is therefore lacking, but it can be hypothesized that parasites carry specific genes that induce these behavioural alterations. Such ‘behavioural’ parasite genes likely affect one or more host proteins directly or via the expression of specific target genes in the host, which subsequently leads to altered behaviour. Understanding the details of such interactions between parasite and host is important as parasitic manipulation is thought to be wide spread in nature and to be a strong driver of the co-evolutionary arms race between parasite and host. Furthermore, the strategies employed by parasites to alter behavior likely provide important insights in the molecular mechanism of many behavioural processes. Chapter 2 of this thesis reviews our current understanding of the mechanisms of behavioural manipulation in invertebrates. It discusses known examples of behavioural manipulation and the present knowledge on the mechanistic basis of these manipulations. Furthermore, an overview of host genes and proteins that play a conserved role in behavioural traits in different invertebrate species is given. These genes and proteins are worthwhile to be studied in more detail in the context of parasitic manipulation, as they might be suitable targets for parasites to induce behavioural changes.

This thesis focuses on behavioural manipulation in insect hosts by baculoviruses. Baculoviruses are DNA viruses that infect the larval stages of mainly lepidopteran insects. These viruses alter host behaviour in multiple ways. They induce hyperactivity in the larvae, which likely contributes to virus dispersal over a large area. In addition, baculoviruses alter host climbing behaviour leading to death at elevated positions, a phenomenon known as ‘tree-top disease’ or ‘Wipfelkrankheit’. This latter manipulation is thought to contribute to optimal virus dispersal on plant foliage. In the research described in this thesis baculoviruses and their lepidopteran insect hosts are used as a model system to study molecular mechanisms of behavioural manipulation. In Chapter 3 of this thesis the involvement of the protein tyrosine phosphatase (ptp) gene from the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) in the induction of hyperactivity of the beet armyworm Spodoptera exigua was studied. A homolog of this gene in Bombyx mori nucleopolyhedrovirus (BmNPV) was previously shown to be important in hyperactivity in the silkworm B. mori. The results in Chapter 3 showed that the AcMNPV ptp gene induces hyperactive behaviour in S. exigua larvae and that the phosphatase activity of the encoded PTP enzyme is crucial for this behavioural change. Phylogenetic inference revealed that the baculovirus ptp is presumably transferred from a (ancestral) lepidopteran host to a baculovirus. Within the family Baculoviridae, ptp is only present in group I NPVs, which are a group of phylogenetically related baculoviruses. It is hypothesized that ptp-induced hyperactivity is an evolutionarily conserved strategy of group I NPVs to manipulate host behaviour.

To obtain insights into the target proteins of the baculovirus PTP enzyme to achieve hyperactive behaviour in infected caterpillars, a PTP substrate analysis was performed. Chapter 4 describes host and viral proteins that were found to co-purify with AcMNPV PTP. Many of these host proteins are known to be important in signalling pathways and behavioural traits. For one of these proteins, 14-3-3 z, mRNA transcript levels were found to be significantly higher in wild type AcMNPV-infected S. exigua larvae as compared to larvae infected with a mutant virus from which the ptp gene has been deleted (AcMNPV Δptp). The 14-3-3 protein is a known activator of the enzymes tryptophan hydroxylase and tyrosine hydroxylase, which in turn are required for synthesis of the neurotransmitters serotonin and dopamine. These signalling molecules are both important determinants in hyperactive behaviour in various organisms, and are associated with behavioural manipulation in several parasite-host systems. In Chapter 9 a model is proposed of how the putative interaction between baculovirus PTP and host 14-3-3 zmay lead to hyperactive behaviour.

Within the baculoviruses two different genes that encode protein tyrosine phosphatases, ptp and ptp2, are found. While the ptp gene induces hyperactivity (described in Chapter 3), no function has yet been assigned to the ptp2 gene. Chapter 5 describes the functional

characterization of the baculovirus ptp2 gene. PTP2 protein carries a conserved consensus sequence that is characteristic for mitogen-activated protein kinase (MAPK) phosphatases. SeMNPV ptp2 induced a mild apoptosis and caspase activation in insect cells upon transient expression, which may be related to its putative function as MAPK phosphatase. Several host proteins that co-purified with SeMNPV PTP2 have known functions in apoptosis and/or MAPK signalling, rendering them promising candidate proteins to be involved in SeMNPV PTP2-induced apoptosis and possibly MAPK signalling. Whether PTP2 also has any behavioural effect is unknown, but the data from this chapter indicate that PTP2 likely has a cellular function during virus infection.

Baculoviruses are known to alter host climbing behaviour, commonly leading to death at elevated positions (tree-top disease). In Chapter 6 the hypothesis was tested that baculovirus-induced hyperactive behaviour and tree-top disease are induced by a single baculovirus gene. To this aim the effect of the hyperactivity-inducing ptp gene (Chapter 3) on tree-top disease was investigated. The results demonstrated that AcMNPV ptp, known to cause hyperactive behaviour in S. exigua, is not involved in tree-top disease in this host. This indicates that hyperactivity and tree-top disease induced by baculoviruses are governed by independent mechanisms. Furthermore, a moulting-dependent effect on tree-top disease in S. exigua was found, which may relate to physiological and/or ecological differences between moulted and unmoulted larvae. In the next chapter (Chapter 7) the effect of AcMNPV infection on tree-top disease was investigated for two different host species, Trichoplusia ni and S. exigua. Data show that in T. ni larvae AcMNPV induces tree-top disease, causing death at elevated positions. In contrast, in S. exigua a moulting-dependent effect on the height at death was observed, as was also described in Chapter 6. Furthermore, in this chapter the role of the AcMNPV egt gene, encoding ecdysteroid UDP glucosyl transferase, on tree-top disease in T. ni and S. exigua larvae was analysed. A homolog of this gene causes tree-top disease in Lymantria dispar larvae infected with L. dispar (Ld) MNPV. The results (Chapter 7) show that AcMNPV egt does not play a role in the observed death at elevated positions in the two host systems studied. This indicates that the role of egt in tree-top disease may not be conserved among members of the family Baculoviridae.

In addition to the mechanisms employed by the generalist baculovirus AcMNPV to alter climbing behaviour, the effect of the specialist baculovirus S. exigua (Se) MNPV on tree-top disease in its only known host S. exigua was studied. In Chapter 8 it is shown that SeMNPV induces tree-top disease by triggering an aberrant response to light, and this positive phototaxis leads to death at elevated positions. A hypothesis is put forward that SeMNPV hijacks a host behavioural pathway that is involved in light perception to induce this positive phototactic response.

Overall, the results of this thesis show that hyperactivity and tree-top disease are induced by baculoviruses through independent mechanisms and that distinct baculovirus species presumably use different genes and proximate mechanisms to induce tree-top disease. While the baculovirus ptp gene induces hyperactivity, possibly by targeting host 14-3-3 z, the baculovirus ptp2 gene may function as a pro-apoptotic gene. The baculovirus egt gene does not have a conserved function in tree-top disease, indicating that other viral genes may underlie this host manipulative strategy. This thesis also demonstrates that tree-top disease in SeMNPV-infected caterpillars is the result of a strong attraction to light.

Parasitic manipulation is a fascinating biological phenomenon that can provide crucial information on how behavioural traits are controlled at the molecular level. The research described in this thesis provides several new insights in the mechanisms by which parasites manipulate the behaviour of their hosts.

The Predictive Adaptive Response: Modeling the Life-History Evolution of the Butterfly
Heuvel, J. van den; Saastamoinen, M. ; Brakefield, P.M. ; Kirkwood, T.B. ; Zwaan, B.J. ; Shanley, D.P. - \ 2013
American Naturalist 181 (2013)2. - ISSN 0003-0147 - p. E28 - E42.
phenotypic plasticity - metabolic syndrome - body-size - adaptation - starvation - growth - flight - lepidoptera - temperature - hypothesis
A predictive adaptive response (PAR) is a type of developmental plasticity where the response to an environmental cue is not immediately advantageous but instead is later in life. The PAR is a way for organisms to maximize fitness in varying environments. Insects living in seasonal environments are valuable model systems for testing the existence and form of PAR. Previous manipulations of the larval and the adult environments of the butterfly Bicyclus anynana have shown that individuals that were food restricted during the larval stage coped better with forced flight during the adult stage compared to those with optimal conditions in the larval stage. Here, we describe a state-dependent energy allocation model, which we use to test whether such a response to food restriction could be adaptive in nature where this butterfly exhibits seasonal cycles. The results from the model confirm the responses obtained in our previous experimental work and show how such an outcome was facilitated by resource allocation patterns to the thorax during the pupal stage. We conclude that for B. anynana, early-stage cues can direct development toward a better adapted phenotype later in life and, therefore, that a PAR has evolved in this species
Effects of local variation in nitrogen deposition on butterfly trends in The Netherlands
Wallis de Vries, M.F. ; Swaay, C.A.M. van - \ 2013
Proceedings of the Netherlands Entomological Society meeting 24 (2013). - ISSN 1874-9542 - p. 25 - 33.
lepidoptera - fauna - stikstof - ammoniakemissie - nederland - nitrogen - ammonia emission - netherlands
Anthropogenic nitrogen deposition has been recognized as a factor affecting the dynamics and composition of plant communities. Its impact on insect communities is still largely unknown. Using data from the Dutch Butterfly Monitoring Scheme, we analyzed the variation in local trends of butterfly abundance in three Natura 2000 habitat types of known sensitivity to nitrogen deposition: coastal dunes (H2130), wet heathlands (H4010A) and species-rich Nardus grassland (H6230). We found evidence of a negative impact of increasing levels of nitrogen deposition on butterfly trends in all three habitat types. Interestingly, species from more nitrogen-rich habitats showed a similar, though less pronounced, response. The results constitute the first evidence of a significant dose-response relationship between nitrogen deposition and declines in insect abundance at a national scale.
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