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.

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Reproduction and Offspring Sex Ratios Differ Markedly among Closely Related Hyperparasitoids Living in the Same Microhabitats
Harvey, Jeffrey A. ; Haan, Lucas de; Verdeny-Vilalta, Oriol ; Visser, Bertanne ; Gols, Rieta - \ 2019
Journal of Insect Behavior 32 (2019)3. - ISSN 0892-7553 - p. 243 - 251.
Gelis - Hymenoptera - Longevity - Realized lifetime fecundity - Secondary parasitoids

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

Effects of temperature and food source on reproduction and longevity of aphid hyperparasitoids of the genera Dendrocerus and Asaphes
Boer, Jetske G. de; Salis, Lucia ; Tollenaar, Ward ; Heumen, Lisa J.M. van; Costaz, Thibault P.M. ; Harvey, Jeffrey A. ; Kos, Martine ; Vet, Louise E.M. - \ 2019
BioControl 64 (2019)3. - ISSN 1386-6141 - p. 277 - 290.
Aphidius colemani - Fourth trophic level - Hymenoptera - Megaspilidae - Myzus persicae - Pteromalidae

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.

Data from: Stiffness gradients facilitate ovipositor bending and spatial probing control in a parasitic wasp
Cerkvenik, U. ; Leeuwen, J.L. van; Kovalev, Alexander ; Gorb, Stanislav N. ; Matsumura, Yoko ; Gussekloo, S.W.S. - \ 2019
Material and structural properties - Ovipositor biomechanics - Steering mechanism - Diachasmimorpha longicaudata - Hymenoptera
Many parasitic wasps use slender and steerable ovipositors to lay eggs in hosts hidden in substrates, but it is currently unknown how steering is achieved. The ovipositors generally consist of three longitudinally connected elements, one dorsal and two ventral valves that can slide along each other. For the parasitic wasp Diachasmimorpha longicaudata, it has been shown that protraction of the ventral valves causes incurving of the ventral valves towards the dorsal one, which results in a change in probing direction. We hypothesize that this shape change is due to differences in bending stiffness along the ovipositor. Alignment of the stiff tip of the dorsal valve with a more flexible ventral S-shaped region situated just behind the tip straightens this S-bend and results in upwards rotation of the ventral tip. We show that the S-shaped region of the ventral valves has a low bending stiffness because it contains soft materials such as resilin. In contrast, the large cross-sectional area of the dorsal valve tip area probably results in a high bending stiffness. Elsewhere, the dorsal valve is less stiff than the ventral valves. Our results support the hypothesis that the interaction between the stiff dorsal valve portion and the more flexible S-shaped region co-determines the configurational tip changes required for steering the ovipositor in any desired direction along curved paths in the substrate. This provides novel insights in the understanding of steering mechanisms of the hymenopteran ovipositor, and for application in man-made probes.
Varying degree of physiological integration among host instars and their endoparasitoid affects stress-induced mortality
Gols, Rieta ; Ros, Vera I.D. ; Ode, Paul J. ; Vyas, Dhaval ; Harvey, Jeffrey A. - \ 2019
Entomologia Experimentalis et Applicata 167 (2019)5. - ISSN 0013-8703 - p. 424 - 432.
Braconidae - Cotesia glomerata - host regulation - Hymenoptera - insect herbivores - Lepidoptera - multitrophic interactions - parasitoids - pathogens - Pieridae - Pieris brassicae

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

Ant-like Traits in Wingless Parasitoids Repel Attack from Wolf Spiders
Harvey, Jeffrey A. ; Visser, Bertanne ; Lammers, Marl ; Marien, Janine ; Gershenzon, Jonathan ; Ode, Paul J. ; Heinen, Robin ; Gols, Rieta ; Ellers, Jacintha - \ 2018
Journal of Chemical Ecology 44 (2018)10. - ISSN 0098-0331 - p. 894 - 904.
Batesian mimicry; Müllerian mimicry - Chemical defense - Formica - Gelis - Hymenoptera - Lasius - Predation

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

Semiochemical exploitation of host-associated cues by seven Melittobia parasitoid species : Behavioral and phylogenetic implications
González, Jorge M. ; Camino, Dakota ; Simon, Sabrina ; Cusumano, Antonino - \ 2018
Frontiers in Ecology and Evolution 5 (2018). - ISSN 2296-701X
Eulophidae - Host location process - Hymenoptera - Infochemicals - Parasitic wasps
Chemical compounds (infochemicals or semiochemicals) play an important role both in intra-specific and inter-specific communication. For example, chemical cues appear to play a key role in the host selection process adopted by insect parasitoids. In recent years significant advances have been made in order to understand the chemical ecology of insect parasitoids. However, little information is available about the evolution of semiochemical use in the host location process of insect parasitoids. Here we investigated the strategy adopted by seven closely related parasitoid species in the genus Melittobia when foraging for four different suitable hosts. By using an integrated approach that combined olfactometer bioassays and phylogenetic investigations, we found that: (1) exploitation of host-derived semiochemicals is widespread in the Melittobia genus; (2) there is specificity of attraction toward the different host species tested; in particular, the early-branching species in the Melittobia genus are attracted to odors associated with leaf cutting bees (Megachile rotundata) whereas the most-diverged species are attracted to odors associated with solitary mud dauber wasps (Trypoxyilon politum). Regardless of the phylogenetic relationships, no Melittobia species exhibited attraction toward odors of factitious laboratory hosts (i.e., the flesh fly Sarcophaga bullata). Interestingly, five Melittobia species are also attracted by odors associated with honeybees hosts which indicate that these parasitoids could be potential pests of honeybees. Our study shed light on the host location within the Melittobia genus and represents a first attempt to understand semiochemical use in an evolutionary perspective in the context of parasitoids' foraging behavior.
Maternal provision of non-sex-specific transformer messenger RNA in sex determination of the wasp Asobara tabida
Geuverink, Elzemiek ; Verhulst, E.C. ; Leussen, M. van; Zande, L. ; Beukeboom, Leo W. - \ 2018
Insect Molecular Biology 27 (2018)1. - ISSN 0962-1075 - p. 99 - 109.
Doublesex - Hymenoptera - Maternal provision - Sex determination - Transformer - Transformer-2
In many insect species maternal provision of sex-specifically spliced messenger RNA (mRNA) of sex determination genes is an essential component of the sex determination mechanism. In haplodiploid Hymenoptera, maternal provision in combination with genomic imprinting has been shown for the parasitoid Nasonia vitripennis, known as maternal effect genomic imprinting sex determination (MEGISD). Here, we characterize the sex determination cascade of Asobara tabida, another hymenopteran parasitoid. We show the presence of the conserved sex determination genes doublesex (dsx), transformer (tra) and transformer-2 (tra2) orthologues in As. tabida. Of these, At-dsx and At-tra are sex-specifically spliced, indicating a conserved function in sex determination. At-tra and At-tra2 mRNA is maternally provided to embryos but, in contrast to most studied insects, As. tabida females transmit a non-sex-specific splice form of At-tra mRNA to the eggs. In this respect, As. tabida sex determination differs from the MEGISD mechanism. How the paternal genome can induce female development in the absence of maternal provision of sex-specifically spliced mRNA remains an open question. Our study reports a hitherto unknown variant of maternal effect sex determination and accentuates the diversity of insect sex determination mechanisms.
Phengaris (Maculinea) teleius butterflies select host plants close to Myrmica ants for oviposition, but P. nausithous do not
Wynhoff, Irma ; Langevelde, Frank van - \ 2017
Entomologia Experimentalis et Applicata 165 (2017)1. - ISSN 0013-8703 - p. 9 - 18.
ant-mediated oviposition - Formicidae - host–parasite relation - Hymenoptera - Lepidoptera - Lycaenidae - myrmecophily - oviposition site choice
Many lycaenid butterfly species have interactions with ants, with 12% obligatorily depending on two sequential sources of larval food, namely host plants and host ants. When host plants are abundant but the density of host ant nests is relatively low, most host plants have no host ant nest in their vicinity and are thus unsuitable for larval survival. Obligatorily myrmecophilous female butterflies, whose caterpillars feed on ant larvae, would have a comparative advantage if they deposit eggs on host plants in the proximity of a host ant nest. However, this ant-mediated oviposition has been hotly debated. In an open-air insectory experiment, we tested whether oviposition is ant-mediated or not for two obligatory myrmecophilous butterfly species, Phengaris (Maculinea) nausithous Bergsträsser and Phengaris teleius Bergsträsser (Lepidoptera: Lycaenidae). Female butterflies could select host plants close to either no ant nest or a nest of one of the two Myrmica species (Hymenoptera: Formicidae) that are thought to be their host ant. Our results support ant-mediated oviposition in P. teleius, but also indicate that there is no preference for either of the Myrmica species. More eggs were deposited and more caterpillars were found on long flowerheads close to Myrmica ant nests than on those without nests. Our findings suggest that ant presence is more important than flowerhead phenology for females of P. teleius. In contrast, P. nausithous females were not attracted by ants but preferred long flowerheads with a low percentage of green coloration. With these findings, this study contributes to better understanding of the habitat requirements of two highly specialized butterfly species.
The chemical basis of mate recognition in two parasitoid wasp species of the genus Nasonia
Mair, Magdalena M. ; Kmezic, Violeta ; Huber, Stephanie ; Pannebakker, Bart A. ; Ruther, Joachim - \ 2017
Entomologia Experimentalis et Applicata 164 (2017)1. - ISSN 0013-8703 - p. 1 - 15.
chemical communication - cuticular hydrocarbons - Hymenoptera - parasitic wasp - pheromone - Pteromalidae - reproductive isolation - species discrimination
To recognize one's mate is essential for all sexually reproducing animals. In insects, mate recognition is often based on chemical cues such as hydrocarbons which are distributed over the insect's cuticle. In the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae), interspecific mating possibly occurs in microsympatry between Nasonia vitripennis Walker and Nasonia giraulti Darling despite post-zygotic isolation mechanisms preventing hybridization. Males of N. vitripennis are known to equally court con- and heterospecific females, which they recognize by means of cuticular hydrocarbons. A recent study surprisingly showed that this might not be the case in N. giraulti, leaving open how males of this species achieve the recognition of mating partners. In this study, we investigated chemical mate recognition in N. giraulti in more detail and compared observed behaviors with behaviors of N. vitripennis by conducting experiments with both species concurrently and under the same experimental conditions. We disentangled the role of female-derived non-polar cuticular lipids – i.e., cuticular hydrocarbons – and more polar cuticular lipids in the ability of males to recognize con- and heterospecific females. In addition, we tested whether females of the two species discriminate similarly between con- and heterospecific males. We demonstrate that, in contrast to N. vitripennis, males of N. giraulti prefer live conspecific females over heterospecific ones. Furthermore, in contrast to N. vitripennis, mate recognition in N. giraulti males is not based on cuticular hydrocarbons, but rather involves other chemical messengers, presumably more polar cuticular lipids. In both species, discrimination against heterospecific males decreases with female age.
Maximized complexity in miniaturized brains : morphology and distribution of octopaminergic, dopaminergic and serotonergic neurons in the parasitic wasp, Trichogramma evanescens
Woude, Emma van der; Smid, Hans M. - \ 2017
Cell and Tissue Research 369 (2017)3. - ISSN 0302-766X - p. 477 - 496.
Confocal laser scanning - Hymenoptera - Immunohistochemistry - Miniaturization - Monoamine

The parasitic wasp, Trichogramma evanescens, is an extremely small insect, with a body length as small as 0.3 mm. To facilitate this miniaturization, their brains may have evolved to contain smaller neural components and/or reduced neural complexity than larger insects. Here, we study whether the size and number of neurons are reduced in the miniaturized brain of T. evanescens, focusing on neurons that express serotonin (5HT), octopamine (OA) and dopamine (DA). We provide the first description of the distribution, projection patterns and number of 5HT-, OA- and DA-like immunoreactive cell bodies in T. evanescens and compare our observations with descriptions of much larger insects. The brains of T. evanescens contain comparable numbers of monoaminergic neurons to those of larger insects. Serotonergic neurons appear to be especially conserved; most of the clusters contain a similar number of neurons to those described in Apis mellifera and Drosophila melanogaster. This maintained complexity may have been facilitated by miniaturization of neuron size. However, many dopaminergic and some octopaminergic neuron clusters in T. evanescens contain fewer neurons than in larger insects. Modification of the complexity of these monoaminergic systems may have been necessary to maintain neuron functionality during brain miniaturization in T. evanescens. Our results reveal some of the evolutionary adaptations that may enable behavioural and cognitive complexity with respect to miniaturized brains.

Inoculation of susceptible and resistant potato plants with the late blight pathogen Phytophthora infestans : effects on an aphid and its parasitoid
Lazebnik, Jenny ; Tibboel, Marianne ; Dicke, Marcel ; Loon, Joop J.A. van - \ 2017
Entomologia Experimentalis et Applicata 163 (2017)3. - ISSN 0013-8703 - p. 305 - 314.
Aphididae - Aphidius colemani - Braconidae - genetic modification - Hemiptera - Hymenoptera - Myzus persicae - non-target effects - plant-pathogen-insect interactions - plant–insect interactions - Solanum tuberosum - trophic interactions

Plants are exposed to microbial pathogens as well as herbivorous insects and their natural enemies. Here, we examined the effects of inoculation of potato plants, Solanum tuberosum L. (Solanaceae), with the late blight pathogen Phytophthora infestans (Mont.) de Bary (Peronosporales: Pythiaceae) on an aphid species commonly infesting potato crops and one of the aphid's major parasitoids. We observed the peach-potato aphid, Myzus persicae Sulzer (Hemiptera: Aphididae), and its natural enemy, the biocontrol agent Aphidius colemani Viereck (Hymenoptera: Braconidae), on potato either inoculated with water or P. infestans. Population growth of the aphid, parasitism rate of its natural enemy, and other insect life-history traits were compared on several potato genotypes, the susceptible cultivar Désirée and genetically modified (GM) isogenic lines carrying genes conferring resistance to P. infestans. Effects of P. infestans inoculation on the intrinsic rate of aphid population increase and the performance of the parasitoid were only found on the susceptible cultivar. Insect traits were similar when comparing inoculated with non-inoculated resistant GM genotypes. We also tested how GM-plant characteristics such as location of gene insertion and number of R genes could influence non-target insects by comparing insect performance among GM events. Different transformation events leading to different positions of R-gene insertion in the genome influenced aphids either with or without P. infestans infection, whereas effects of position of R-gene insertion on the parasitoid A. colemani were evident only in the presence of inoculation with P. infestans. We conclude that it is important to study different transformation events before continuing with further stages of risk assessment of this GM crop. This provides important information on the effects of plant resistance to a phytopathogen on non-target insects at various trophic levels.

Effects of Isometric Brain-Body Size Scaling on the Complexity of Monoaminergic Neurons in a Minute Parasitic Wasp
Woude, Emma van der; Smid, Hans M. - \ 2017
Brain, behavior and evolution 89 (2017)3. - ISSN 0006-8977 - p. 185 - 194.
Allometry - Confocal laser scanning microscopy - Dopamine - Hymenoptera - Octopamine - Serotonin
Trichogramma evanescens parasitic wasps show large phenotypic plasticity in brain and body size, resulting in a 5-fold difference in brain volume among genetically identical sister wasps. Brain volume scales linearly with body volume in these wasps. This isometric brain scaling forms an exception to Haller's rule, which states that small animals have relatively larger brains than large animals. The large plasticity in brain size may be facilitated by plasticity in neuron size, in the number of neurons, or both. Here, we investigated whether brain isometry requires plasticity in the number and size of monoaminergic neurons that express serotonin (5HT), octopamine (OA), and dopamine (DA). Genetically identical small and large T. evanescens appear to have the same number of 5HT-, OA-, and DA-like immunoreactive cell bodies in their brains, but these cell bodies differ in diameter. This indicates that brain isometry can be facilitated by plasticity in the size of monoaminergic neurons, rather than plasticity in numbers of monoaminergic neurons. Selection pressures on body miniaturization may have resulted in the evolution of miniaturized neural pathways that allow even the smallest wasps to find suitable hosts. Plasticity in the size of neural components may be among the mechanisms that underlie isometric brain scaling while maintaining cognitive abilities in the smallest individuals.
Studies of laboulbeniales (Fungi, Ascomycota) on myrmica ants (II) : Variation of infection by Rickia wasmannii over habitats and time
Haelewaters, Danny ; Boer, Peter ; Gort, Gerrit ; Noordijk, Jinze - \ 2015
Animal Biology 65 (2015)3-4. - ISSN 1570-7555 - p. 219 - 231.
Ant-associated fungi - Auto- and allogrooming - Ectoparasites - Formicidae - Hymenoptera - Laboulbeniomycetes - Parasite prevalence - Variation of infection

One group of important insect parasites are the Laboulbeniales (Ascomycota), microscopic fungi that live attached to the exterior of their hosts, mainly beetles, but also mites, millipedes, earwigs, and ants. Rickia wasmannii is a common fungus in Europe and is limited to the ant genus Myrmica (Hymenoptera, Formicidae). This paper presents patterns of R. wasmannii infection in the Netherlands from three host species collected in three series of pitfall traps: Myrmica ruginodis, M. sabuleti, and M. scabrinodis. The infection rate of especially M. sabuleti was so high, that it allowed analyses of infection patterns over time and habitats. We found that only workers were infected, mostly the older ones with a hard cuticle. Gynes are probably never infected. This is supported with data from a nature restoration site: in this young area R. wassmannii is not abundant in contrast to close-by sites, so there probably is a build-up of infection by Rickia over time through worker contact. Taken over three periods throughout the year (spring, summer, autumn), parasite prevalence declined significantly in M. sabuleti, with a non-significant declining trend in M. scabrinodis. Increased allogrooming behavior in the nest in the winter may be the main contributing factor for this. New, largely uninfected cohorts of workers lead to decreased infection rate during the reproduction season. Finally, Rickia wasmannii occurs throughout a wide variety of habitats, from moist and cool to dry and warm.

Onderzoek naar de biologie en het parasiteringsgedrag van Telenomus nitidulus (Thomson) (Hymenoptera: Scelionidae), eiparasiet van de satijnvlinder, Leucoma salicis L.
Sonderen, L.M. van - \ 1985
Wageningen : De Dorschkamp (Rapport / Rijksinstituut voor Onderzoek in de Bos- en Landschapsbouw 'De Dorschkamp' no. 396) - 93
Hymenoptera - Lepidoptera - gastheer parasiet relaties - parasitisme - bosbouw - diergedrag - gewoonten - adaptatie - Telenomus nitidulus - Leucoma salicis - host parasite relationships - parasitism - forestry - animal behaviour - habits - adaptation
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