How to escape from insect egg parasitoids : a review of potential factors explaining parasitoid absence across the Insecta
Fatouros, N.E. ; Cusumano, A. ; Bin, F. ; Polaszek, A. ; Lenteren, J.C. van - \ 2020
Proceedings of the Royal Society. B: Biological Sciences 287 (2020)1931. - ISSN 0962-8452 - 1 p.
egg deposition - egg protection - herbivory - hymenoptera - oviposition site - parental care
The egg is the first life stage directly exposed to the environment in oviparous animals, including many vertebrates and most arthropods. Eggs are vulnerable and prone to mortality risks. In arthropods, one of the most common egg mortality factors is attack from parasitoids. Yet, parasitoids that attack the egg stage are absent in more than half of all insect (sub)orders. In this review, we explore possible causes explaining why eggs of some insect taxa are not parasitized. Many insect (sub)orders that are not attacked by egg parasitoids lack herbivorous species, with some notable exceptions. Factors we consider to have led to escape from egg parasitism are parental egg care, rapid egg development, small egg size, hiding eggs, by e.g. placing them into the soil, applying egg coatings or having thick chorions preventing egg penetration, eusociality, and egg cannibalism. A quantitative network analysis of host-parasitoid associations shows that the five most-speciose genera of egg parasitoids display patterns of specificity with respect to certain insect orders, especially Lepidoptera and Hemiptera, largely including herbivorous species that deposit their eggs on plants. Finally, we discuss the many counteradaptations that particularly herbivorous species have developed to lower the risk of attack by egg parasitoids.
The ovipositor actuation mechanism of a parasitic wasp and its functional implications
Meer, Noraly M.M.E. van; Cerkvenik, Uroš ; Schlepütz, Christian M. ; Leeuwen, Johan L. van; Gussekloo, Sander W.S. - \ 2020
Journal of Anatomy 237 (2020)4. - ISSN 0021-8782 - p. 689 - 703.
hymenoptera - kinematics - musculature - ovipositor - synchrotron X-ray micro-computed tomography
Parasitic wasps use specialized needle-like structures, ovipositors, to drill into substrates to reach hidden hosts. The external ovipositor (terebra) consists of three interconnected, sliding elements (valvulae), which are moved reciprocally during insertion. This presumably reduces the required pushing force on the terebra and limits the risk of damage whilst probing. Although this is an important mechanism, it is still not completely understood how the actuation of the valvulae is achieved, and it has only been studied with the ovipositor in rest position. Additionally, very little is known about the magnitude of the forces generated during probing. We used synchrotron X-ray microtomography to reconstruct the actuation mechanism of the parasitic wasp Diachasmimorpha longicaudata (Braconidae) in four distinct phases of the probing cycle. We show that only the paired first valvulae of the terebra move independently, while the second valvula moves with the metasoma (‘abdomen’). The first valvula movements are initiated by rotation of one chitin plate (first valvifer) with respect to another such plate (second valvifer). This is achieved indirectly by muscles connecting the non-rotating second valvifer and the abdominal ninth tergite. Contrary to previous reports, we found muscle fibres running inside the terebra, although their function remains unclear. The estimated maximal forces that can be exerted by the first valvulae are small (protraction 1.19 mN and retraction 0.874 mN), which reduces the risk of buckling, but are sufficient for successful probing. The small net forces of the valvulae on the substrate may still lead to buckling of the terebra; we show that the sheaths surrounding the valvulae prevent this by effectively increasing the diameter and second moment of area of the terebra. Our findings improve the comprehension of hymenopteran probing mechanisms, the function of the associated muscles, and the forces and damage-limiting mechanism that are involved in drilling a slender terebra into a substrate.
Extensive literature search for preparatory work to support pan European pest risk assessment: Trichilogaster acaciaelongifoliae RC/EFS/ALPHA/2014/07
Derkx, M.P.M. ; Brouwer, J.H.D. ; Breda, P.J.M. van; Helsen, H.H.M. ; Hoffman, M.H.A. ; Hop, M.E.C.M. - \ 2014
Parma, It. : EFSA (EFSA supporting publication 2015- EN-764) - 71
acacia - acacia longifolia - houtachtige planten als sierplanten - distributie - onkruiden - invasieve exoten - geïntroduceerde soorten - biologische bestrijding - organismen ingezet bij biologische bestrijding - hymenoptera - risicoschatting - europa - acacia - acacia longifolia - ornamental woody plants - distribution - weeds - invasive alien species - introduced species - biological control - biological control agents - hymenoptera - risk assessment - europe
The European Commission is currently seeking advice from EFSA (Mandate M-2012-0272) to assess for Arabis mosaic virus, Raspberry ringspot virus, Strawberry latent ringspot virus, Tomato black ring virus, Strawberry mild yellow edge virus, Strawberry crinkle virus, Daktulosphaira vitifoliae, Eutetranychus orientalis, Parasaissetia nigra, Clavibacter michiganensis spp. michiganensis, Xanthomonas campestris pv. vesicatoria, Didymella ligulicola and Phytophthora fragariae the risk to plant health for the EU territory and to evaluate the effectiveness of risk reduction options in reducing the level of risk. In addition, the Panel is requested to provide an opinion on the effectiveness of the present EU requirements against these organisms laid down in Council Directive 2000/29/EC. As a consequence EFSA needs insight in the cropping practices of Citrus spp., Fragaria x ananassa, Ribes spp., Rubus spp., Vaccinium spp., Humulus lupulus, Vitis vinifera, Prunus armeniaca, P. avium, P. cerasus, P. domestica and P. persica, which are host plants for these pests. An extensive and systematic literature search was done in which scientific and grey/technical literature was retrieved from the 28 EU Member States, Iceland and Norway. All references were stored in EndNote libraries, separately for scientific literature and grey/technical literature. For each reference information is provided on the source/search strategy, the crop, the country, the topic (cropping practice, propagation, protection or irrigation (only for Citrus)) and protected cultivation vs. field production. Yields of references depended on the crop and on the country. Over 27,000 references were provided to EFSA. This allows EFSA to quickly find information on crop production, both indoors and outdoors, of all crops that were studied in this extensive literature search. The data can be used by EFSA for the present mandate, but are also an excellent basis for other current and future mandates.
Introgression study reveals two quantitative trait loci involved in interspecific variation in memory retention among Nasonia wasp species
Hoedjes, K.M. ; Smid, H.M. ; Vet, L.E.M. ; Werren, J.H. - \ 2014
Heredity 113 (2014). - ISSN 0018-067X - p. 542 - 550.
long-term-memory - natural variation - parasitic wasps - learning rate - drosophila - evolution - consolidation - dynamics - pteromalidae - hymenoptera
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.
Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in The Netherlands
Scheper, J.A. ; Reemer, M. ; Kats, R.J.M. van; Ozinga, W.A. ; Linden, G.T.J. van der; Schaminee, J.H.J. ; Siepel, H. ; Kleijn, D. - \ 2014
Proceedings of the National Academy of Sciences of the United States of America 111 (2014)49. - ISSN 0027-8424 - p. 17552 - 17557.
pollinator interactions - multimodel inference - behavioral ecology - model selection - extinction risk - solitary bees - range size - land-use - conservation - hymenoptera
Evidence for declining populations of both wild and managed bees has raised concern about a potential global pollination crisis. Strategies to mitigate bee loss generally aim to enhance floral resources. However, we do not really know whether loss of preferred floral resources is the key driver of bee decline because accurate assessment of host plant preferences is difficult, particularly for species that have become rare. Here we examine whether population trends of wild bees in The Netherlands can be explained by trends in host plants, and how this relates to other factors such as climate change. We determined host plant preference of bee species using pollen loads on specimens in entomological collections that were collected before the onset of their decline, and used atlas data to quantify population trends of bee species and their host plants. We show that decline of preferred host plant species was one of two main factors associated with bee decline. Bee body size, the other main factor, was negatively related to population trend, which, because larger bee species have larger pollen requirements than smaller species, may also point toward food limitation as a key factor driving wild bee loss. Diet breadth and other potential factors such as length of flight period or climate change sensitivity were not important in explaining twentieth century bee population trends. These results highlight the species-specific nature of wild bee decline and indicate that mitigation strategies will only be effective if they target the specific host plants of declining species.
Natural variation in memory formation among Nasonia parasitic wasps : from genes to behaviour
Hoedjes, K.M. - \ 2014
Wageningen University. Promotor(en): Louise Vet; Marcel Dicke, co-promotor(en): Hans Smid. - Wageningen : Wageningen University - ISBN 9789461739483 - 191
nasonia - hymenoptera - geheugen - leervermogen - genetische factoren - dierecologie - diergedrag - genomen - nasonia - hymenoptera - memory - learning ability - genetic factors - animal ecology - animal behaviour - genomes
The ability to learn and form memory has been demonstrated in various animal species, ranging from relatively simple invertebrates, such as snails and insects, to more complex vertebrate species, including birds and mammals. The opportunity to acquire new skills or to adapt behaviour through learning is an obvious benefit. However, memory formation is also costly: it can be maladaptive when unreliable associations are formed and the process of memory formation can be energetically costly. The balance between costs and benefits determines if learning and memory formation are beneficial to an animal or not. Variation in learning abilities and memory formation between species is thought to reflect species-specific differences in ecology.
This thesis focused on variation in the number of trials required to form long-term memory (LTM). LTM is considered the most stable and durable type of memory, but also the most costly, because it requires protein synthesis. Many animal species require multiple learning experiences, which are spaced in time, to form LTM. This allows re-evaluation of information before an animal invests in costly LTM. There is, however, variation in the number of trials that animal species require to induce LTM formation. A number of insect species, including a number of parasitic wasp species, form LTM after only a single learning experience. Parasitic wasps can learn odours that guide them towards suitable hosts for their offspring, so-called oviposition learning. Substantial differences in LTM formation are observed among closely related species of parasitic wasps, which provides excellent opportunities for comparative studies. Both ecological and genetic factors involved in variation in LTM formation have been studied in this project. A multidisciplinary approach is essential to understand the evolution of variation in LTM formation, because the interaction between genes and environment shapes learning and memory formation.
LTM formation was studied in closely related species of the genus Nasonia. These small parasitic wasps (~2 mm in length) lay their eggs in various species of fly pupae and differences in the ecology of the four known species of this genus have been described. A high-throughput method for olfactory conditioning was developed in which the wasps associated an odour, either chocolate or vanilla, with the reward of a host. A T-maze olfactometer was designed for high-throughput testing of memory retention. Using these methods, variation in memory retention was observed between three Nasonia species. Both N. vitripennis and N. longicornis form a long-lasting memory after a single conditioning trial, which lasts at least 5 days. Nasonia giraulti, on the other hand, lost its memory after 1 to 2 days after a single conditioning trial. Further studies focused on the difference between N. vitripennis and N. giraulti, which was most pronounced. By inhibiting LTM with transcription and translation inhibitors, it was confirmed that N. vitripennis forms this type of memory after a single conditioning trial. LTM is visible 4 days after conditioning in N. vitripennis. Nasonia giraulti does not form LTM after a single conditioning trial. Long-lasting memory is only formed after two trials, with a 4-hour interval between them. This difference in LTM formation makes N. vitripennis and N. giraulti excellent model species to study both ecological and genetic factors involved in this difference.
Ecological factors such as the value of the reward and the reliability of the learned association have been shown to affect memory formation in a number of animal species. A recent study on oviposition learning in two parasitic wasp species demonstrated that LTM formation depends on the host species, i.e. the reward offered during conditioning. LTM was formed when a host with a higher quality was offered, but not when a host of lower quality was offered. The effect of host quality on memory retention of N. vitripennis and N. giraulti was tested. Either a large host, Calliphora vomitoria, a medium-sized host, Lucilia sericata, or a small host, Musca domestica, was offered during conditioning. These hosts were observed to differ significantly in their quality, i.e. in the number of parasitoid offspring that emerged and the size of the offspring. There was, however, no effect of host species on memory retention in either Nasonia species. These results suggest that host quality is not important for LTM formation in N. vitripennis and N. giraulti. This observation shows that ecological factors that are important for memory formation in one species may not be important for another species.
The genetic basis of memory formation is highly conserved among distant animal phyla. A large number of genes involved in LTM formation have been identified in genetic model organisms, including fruit flies, honeybees, the California sea hare, mice and rats, and the zebra finch.Genetic factors responsible for natural variation in LTM formation between species are currently unknown, however. Two approaches were used to study genetic factors responsible for the difference in LTM formation between N. vitripennis and N. giraulti. The first approach took advantage of the unique possibility to interbreed Nasonia species. Hybrid offspring of N. vitripennis and N. giraulti did not form LTM after a single conditioning trial, similar to N. giraulti. The dominant LTM phenotype of N. giraulti was then backcrossed into the genetic background of N. vitripennis for up to 5 generations. Using a genotyping microarray analysis and subsequent confirmation experiments, we detected two genomic regions (quantitative trait loci – QTLs) that both reduce long-lasting memory, but not completely remove this memory. These results indicate that multiple QTLs regulate the difference in LTM formation between the two Nasonia species. Concluding, our approach has provided insights in the genomic basis of a naturally occurring difference in LTM formation between two species. Excellent opportunities for fine-scale QTL mapping are available for the genus Nasonia. This will allow identification of decisive regulatory mechanisms involved in LTM formation that are located in the two genomic regions detected in this study.
The second approach took advantage of next-generation sequencing techniques that allow transcriptome-wide studies of gene expression levels. RNA from heads of N. vitripennis and N. giraulti was collected before conditioning and immediately, 4 hours, or 24 hours after conditioning. This RNA was sequenced strand-specifically using HiSeq technology, which allows detection of sense and antisense transcripts. Various genes, from a number of different signalling pathways known to be involved in LTM formation, were uniquely differentially expressed after conditioning in N. vitripennis. These genes are likely involved in the ongoing process of LTM formation in this species. A number of other genes with a known role in LTM formation,including genes involved in dopamine synthesis and in the Ras-MAPK and PI3K signalling pathways, were uniquely differentially expressed in N. giraulti. These genes may have a role in a LTM inhibitory mechanism in this species. Antisense transcripts were detected for a number of known memory genes, which may indicate a role inregulation of transcription, alternative splicing, or translation. This study is the first to compare gene expression patterns after conditioning between two species that differ in LTM formation. The results provide promising candidate genes for future studies in which the regulation of these genes, the function of specific splice variants, and spatial expression patterns in the brain should be studied to understand how these genes are involved in the regulation of LTM formation.
Learning and memory formation have an important role in animal and human behaviour.Novel and valuable insights on both ecological and genetic factors responsible for variation in LTM formation have been revealed by the research presented in this thesis. Integrating ecological factors and genetic factors is essential, as genes are the level on which ecological factors can drive the evolution of variation in learning and memory formation. The genus Nasonia has offered excellent opportunities for ecological research as well as unique opportunities for studies on genomic and genetic factors, which were addressed by comparing closely related species that differ in memory formation. This thesis provides the basis for the identification of genomic differences responsible for the difference in memory formation between Nasonia species, but it also characterized the consequences of these genomic differences on gene expression. The genetic basis of learning and memory formation are highly conserved among distant animal species and insights from this thesis are likely applicable to other animal species and humans, as well.Altogether, these small parasitic wasps allow us to understand and value differences in memory formation.
Development of a Nasonia vitripennis outbred laboratory population for genetic analysis
Zande, L. van de; Ferber, S. ; Haan, A. de; Beukeboom, L.W. ; Heerwaarden, J. van; Pannebakker, B.A. - \ 2014
Molecular Ecology Resources 14 (2014)3. - ISSN 1755-098X - p. 578 - 587.
parasitoid wasp nasonia - local mate competition - sex-ratio - drosophila-melanogaster - natural-populations - ectoparasitic wasp - hymenoptera - genome - evolution - recombination
The parasitoid wasp genus Nasonia has rapidly become a genetic model system for developmental and evolutionary biology. The release of its genome sequence led to the development of high-resolution genomic tools, for both interspecific and intraspecific research, which has resulted in great advances in understanding Nasonia biology. To further advance the utility of Nasonia vitripennis as a genetic model system and to be able to fully exploit the advantages of its fully sequenced and annotated genome, we developed a genetically variable and well-characterized experimental population. In this study, we describe the establishment of the genetically diverse HVRx laboratory population from strains collected from the field in the Netherlands. We established a maintenance method that retains genetic variation over generations of culturing in the laboratory. As a characterization of its genetic composition, we provide data on the standing genetic variation and estimate the effective population size (Ne ) by microsatellite analysis. A genome-wide description of polymorphism is provided through pooled resequencing, which yielded 417 331 high-quality SNPs spanning all five Nasonia chromosomes. The HVRx population and its characterization are freely available as a community resource for investigators seeking to elucidate the genetic basis of complex trait variation using the Nasonia model system
Convergence and Divergence in Direct and Indirect Life-History Traits of Closely Related Parasitoids (Braconidae: Microgastrinae)
Harvey, J.A. ; Visser, B. ; Lann, C. le; Boer, J.G. de; Ellers, J. ; Gols, R. - \ 2014
Evolutionary Biology 41 (2014)1. - ISSN 0071-3260 - p. 134 - 144.
wasp venturia-canescens - sexual size dimorphism - developmental strategies - reproductive strategies - evolutionary argument - development time - egg-production - body-size - host - hymenoptera
Closely related species in nature often show similarities in suites of direct and indirect traits that reveal aspects of their phylogenetic history. Here we tested how common descent affects trait evolution in several closely related parasitoid species in the genera Cotesia and Microplitis (Hymenoptera: Braconidae: Microgastrinae) by comparing development, resource use and allocation into reproduction and maintenance. Parasitoids in these genera exhibit traits, like haemolymph feeding as larvae and external pupation that are rare in most parasitoid lineages. The growth of parasitized hosts was reduced by 90 % compared with healthy hosts, and maximum host size depended to a large extent on adult parasitoid size. Development time was longer in the more generalist parasitoids than in the specialists. Adult body mass was sexually dimorphic in all Cotesia species, with females being larger, but not in Microplitis spp. In contrast, in one of the Microplitis species males were found to be the larger sex. Egg load dynamics during the first 6 days after emergence were highly variable but egg number was typically higher in Cotesia spp. compared to Microplitis spp. Longevity in the various species was only greater in female than in male wasps in two Microplitis sp. There was a clear inverse relationship between resource use and allocation, e.g. maximum egg load and longevity, in these parasitoids. Our results reveal that adaptation to constraints imposed by host quality and availability has resulted in trait convergence and divergence at the species, genus and subfamily level.
Toxic effects of hexaflumuron on the development of Cocccinella septempunctata
Caihong, Yu ; Maoran, Fu ; Ronghua, Lin ; Yan, Zhang ; Liu, Yongquan ; Hui, Jiang ; Brock, T.C.M. - \ 2014
Environmental Science and Pollution Research 21 (2014)2. - ISSN 0944-1344 - p. 1418 - 1424.
insect growth-regulators - beneficial arthropods - pesticides - hymenoptera - fields - nontarget - impact - lethal - hym.
Studying the toxic risk of pesticide exposure to ladybird beetles is important from an agronomical and ecological perspective since larval and adult ladybirds are dominant predators of herbivorous pest insects (e.g., aphids) in various crops in China. This article mainly deals with the long-term effects of a single application of the insect growth regulator hexaflumuron on Coccinella septempunctata. A 72- h and a 33-day toxicity test with hexaflumuron (single application) were performed, starting with the second instar larvae of C. septempunctata. Exposure doses in the long-term experiment were based on the estimated 72-h acute LR50 (application rate causing 50 % mortality) value of 304 g active ingredient (a.i.) ha-1 for second instar larvae of C. septempunctata. The long-term test used five hexaflumuron doses as treatment levels (1/50, 1/100, 1/200, 1/400, and 1/800 of the 72-h acute LR50), as well as a solvent control and blank control treatment. The measurement endpoints used to calculate no observed effect application rates (NOERs) included development time, hatching, pupation, adult emergence, survival, and number of eggs produced. Analyzing the experimental data with one-way analysis of variance showed that the single hexaflumuron application had significant effects on C. septempunctata endpoints in the 33-day test, including effects on development duration (NOER 1.52 g a.i. ha-1), hatching (NOER 3.04 g a.i. ha-1), pupation (NOER 3.04 g a.i. ha-1), and survival (NOER 1.52 g a.i. ha-1). These NOERs are lower than the reported maximum field application rate of hexaflumuron (135 g a.i. ha-1) in cotton cultivation, suggesting potential risks to beneficial arthropods.
Genetic incompatibility drives mate choice in a parasitic wasp
Thiel, A. ; Weeda, A.C. ; Boer, J.G. de; Hoffmeister, T.S. - \ 2013
Frontiers in Zoology 10 (2013). - ISSN 1742-9994 - 6 p.
complementary sex determination - field crickets - selection - mhc - preferences - hymenoptera - quality - extinction - increases - humans
Introduction: Allelic incompatibility between individuals of the same species should select for mate choice based on the genetic make-up of both partners at loci that influence offspring fitness. As a consequence, mate choice may be an important driver of allelic diversity. A complementary sex determination (CSD) system is responsible for intraspecific allelic incompatibility in many species of ants, bees, and wasps. CSD may thus favour disassortative mating and in this, resembles the MHC of the vertebrate immune system, or the self-incompatibility (SI) system of higher plants. Results: Here we show that in the monogamous parasitic wasp Bracon brevicornis (Wesmael), females are able to reject partners with incompatible alleles. Forcing females to accept initially rejected partners resulted in sex ratio distortion and partial infertility of offspring. Conclusions: CSD-disassortative mating occurred independent of kin recognition and inbreeding avoidance in our experiment. The fitness consequences of mate choice are directly observable, not influenced by environmental effects, and more severe than in comparable systems (SI or MHC), on individuals as well as at the population level. Our results thus demonstrate the strong potential of female mate choice for maintaining high offspring fitness in this species.
Boommier, Lasius brunneus (Formicidae), als gast in een bosmierennest
Mabelis, A.A. - \ 2013
Entomologische Berichten 73 (2013)1. - ISSN 0013-8827 - p. 25 - 25.
hymenoptera - formicidae - nestelen - diergedrag - hymenoptera - formicidae - nesting - animal behaviour
De boommier komt vooral in loofbossen voor, al bouwt hij zijn nest ook wel eens in een geïsoleerde boom. In huizen wordt hij soms aangetroffen in een oude balk. Meestal betreft het hout met een hoog vochtgehalte dat door een schimmel is aangetast. De boommier als bewoner van een bosmierennest is wel erg uitzonderlijk.
Interactive effect of reduced pollen availability and Varroa destructor infestation limits growth and protein content of young honey bees
Dooremalen, C. van; Stam, E. ; Gerritsen, L.J.M. ; Cornelissen, B. ; Steen, J.J.M. van der; Langevelde, F. van; Blacquiere, T. - \ 2013
Journal of Insect Physiology 59 (2013)4. - ISSN 0022-1910 - p. 487 - 493.
apis-mellifera l - hypopharyngeal glands - jacobsoni oud - colony losses - ectoparasitic mite - worker honeybees - life-span - hymenoptera - weight - apidae
Varroa destructor in combination with one or more stressors, such as low food availability or chemical exposure, is considered to be one of the main causes for honey bee colony losses. We examined the inter-active effect of pollen availability on the protein content and body weight of young bees that emerged with and without V. destructor infestation. With reduced pollen availability, and the coherent reduced nutritional protein, we expected that V. destructor infestation during the pupal stage would have a larger negative effect on bee development than without infestation. Moreover, when raised with ample pollen available after emergence, infested pupae were expected not to be able to compensate for early losses due to V. destructor. We found that both V. destructor infestation and reduced pollen availability reduced body weight, abdominal protein level, and increased the head to abdomen protein ratio. The availability of pol- len did indeed not result in compensation for reduced mass and protein content caused by V. destructor infestation in young bees after 1 week of their adult life. Both V. destructor and nutrition are top concerns for those studying honey bee health and this study demonstrates that both have substantial effects on young bees and that ample available pollen cannot compensate for reduced mass and protein content caused by V. destructor parasitism.
Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host
Poelman, E.H. ; Bruinsma, M. ; Zhu, F. ; Weldegergis, B.T. ; Boursault, A.E. ; Jongema, Y. ; Loon, J.J.A. van; Vet, L.E.M. ; Harvey, J.A. ; Dicke, M. - \ 2012
PloS Biology 10 (2012)11. - ISSN 1545-7885 - 13 p.
higher trophic levels - cotesia-glomerata - natural enemies - hymenoptera - braconidae - rubecula - quality - performance - arthropods - behavior
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.
High-throughput olfactory conditioning and memory retention test show variation in Nasonia parasitic wasps.
Hoedjes, K.M. ; Steidle, J.L.M. ; Werren, J.H. ; Vet, L.E.M. ; Smid, H.M. - \ 2012
Genes, Brain and Behavior 11 (2012)7. - ISSN 1601-1848 - p. 879 - 887.
long-term-memory - cotesia-glomerata - natural variation - learning rate - vitripennis - hymenoptera - drosophila - pteromalidae - dissection - preference
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.
Assessing non-target effects and host feeding of the exotic parasitoid Apanteles taragamae, a potential biological control agent of the cowpea pod borer Maruca vitrata
Dannon, A.E. ; Tamo, M. ; Huis, A. van; Dicke, M. - \ 2012
BioControl 57 (2012)3. - ISSN 1386-6141 - p. 415 - 425.
busseola-fusca lepidoptera - larval parasitoids - intrinsic competition - lethal interference - population-dynamics - natural enemies - arthropod pests - hymenoptera - braconidae - pyralidae
Apanteles taragamae Viereck is a larval parasitoid introduced in Benin for classical biological control of the cowpea pod borer Maruca vitrata Fabricius. In the laboratory, we evaluated the effects of A. taragamae on non-target herbivore species, and on another parasitoid of M. vitrata, i.e. the egg-larval parasitoid Phanerotoma leucobasis Kriechbaumer. Furthermore, we addressed the host feeding behaviour of A. taragamae. The host specificity of A. taragamae was assessed by offering six other lepidopteran species to the wasp. The competitive ability of A. taragamae was studied by providing the wasp with one- and two-days-old M. vitrata larvae that had hatched from eggs previously parasitized by P. leucobasis. Controls consisted of eggs and larvae offered only to P. leucobasis and A. taragamae, respectively. None of the other six lepidopteran species was successfully parasitized by A. taragamae. The larval parasitoid A. taragamae outcompeted the egg-larval parasitoid P. leucobasis when offered two-days-old host larvae. Competition between the two parasitoid species did not significantly affect one-day-old host larvae that were less suitable to A. taragamae. Host feeding by A. taragamae did not affect survival of one-day-old or two-days-old M. vitrata larvae. However, the percentage parasitism of two-days-old larvae was significantly reduced when exposed to female A. taragamae wasps that had been starved during 48 h. The data are discussed with regard to host specificity, host feeding patterns and to factors underlying the outcome of intrinsic competition between parasitoid species.
Development of a hyperparasitoid wasp in different stages of its primary parasitoid and secondary herbivore hosts
Harvey, J.A. ; Gols, R. ; Vet, L.E.M. ; Kruidhof, H.M. - \ 2012
Journal of Insect Physiology 58 (2012)11. - ISSN 0022-1910 - p. 1463 - 1468.
sex-ratio - heliothis-virescens - nutritional ecology - size - fitness - hymenoptera - growth - quality - constraints - suitability
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.
The roles of ecological fitting, phylogeny and physiological equivalence in understanding realized and fundamental host ranges in endoparasitoid wasps
Harvey, J.A. ; Ximenez De Embun, M.G. ; Bukovinszky, T. ; Gols, R. - \ 2012
Journal of Evolutionary Biology 25 (2012)10. - ISSN 1010-061X - p. 2139 - 2148.
hyposoter-didymator hym - microplitis-demolitor - developmental strategies - insect parasitoids - cotesia-kazak - arms-race - hymenoptera - evolution - plant - braconidae
Co-evolutionary theory underpins our understanding of interactions in nature involving plant-herbivore and host-parasite interactions. However, many studies that are published in the empirical literature that have explored life history and development strategies between endoparasitoid wasps and their hosts are based on species that have no evolutionary history with one another. Here, we investigated novel associations involving two closely related solitary endoparasitoids that originate from Europe and North America and several of their natural and factitious hosts from both continents. The natural hosts of both species are also closely related, all being members of the same family. We compared development and survival of both parasitoids on the four host species and predicted that parasitoid performance is better on their own natural hosts. In contrast with this expectation, survival, adult size and development time of both parasitoids were similar on all (with one exception) hosts, irrespective as to their geographic origin. Our results show that phylogenetic affinity among the natural and factitious hosts plays an important role in their nutritional suitability for related parasitoids. Evolved traits in parasitoids, such as immune suppression and development, thus enable them to successfully develop in novel host species with which they have no evolutionary history. Our results show that host suitability for specialized organisms like endoparasitoids is closely linked with phylogenetic history and macro-evolution as well as local adaptation and micro-evolution. We argue that the importance of novel interactions and 'ecological fitting' based on phylogeny is a greatly underappreciated concept in many resource-consumer studies.
Sex determination meltdown upon biological control introduction of the parasitoid Cotesia rubecula?
Boer, J.G. de; Kuijper, B. ; Heimpel, G.E. ; Beukeboom, L.W. - \ 2012
Evolutionary Applications 5 (2012)5. - ISSN 1752-4563 - p. 444 - 454.
ant solenopsis-invicta - pieris-rapae lepidoptera - determination mechanisms - bracon-hebetor - mating system - wasp - hymenoptera - population - glomerata - genetics
Natural enemies may go through genetic bottlenecks during the process of biological control introductions. Such bottlenecks are expected to be particularly detrimental in parasitoid Hymenoptera that exhibit complementary sex determination (CSD). CSD is associated with a severe form of inbreeding depression because homozygosity at one or multiple sex loci leads to the production of diploid males that are typically unviable or sterile. We observed that diploid males occur at a relatively high rate (8–13% of diploid adults) in a field population of Cotesia rubecula in Minnesota, USA, where this parasitoid was introduced for biological control of the cabbage white Pieris rapae. However, our laboratory crosses suggest two-locus CSD in a native Dutch population of C. rubecula and moderately high diploid males survival (approximately 70%), a scenario expected to produce low proportions of diploid males. We also show that courtship behavior of diploid males is similar to that of haploid males, but females mated to diploid males produce only very few daughters that are triploid. We use our laboratory data to estimate sex allele diversity in the field population of C. rubecula and discuss the possibility of a sex determination meltdown from two-locus CSD to effective single-locus CSD during or after introduction.
Demonstration of long-term memory in the parasitic wasp Nasonia vitripennis
Schurmann, D. ; Sommer, C. ; Schinko, A.P.B. ; Greschista, M. ; Smid, H.M. ; Steidle, J.L.M. - \ 2012
Entomologia Experimentalis et Applicata 143 (2012)2. - ISSN 0013-8703 - p. 199 - 206.
male sex-pheromone - lariophagus-distinguendus - microplitis-croceipes - host discrimination - natural variation - infochemical use - learning rate - dynamics - pteromalidae - hymenoptera
We studied the formation of protein synthesis-dependent long-term memory (LTM) in the parasitic wasp Nasonia vitripennis Walker (Hymenoptera: Pteromalidae), a parasitoid of fly pupae. Female wasps were trained in one of five different training procedures in the presence of hosts and the odour cinnamon. Six days later the reaction of the wasps towards the odour was tested in a static four-chamber olfactometer. When wasps were trained by a single drilling experience we could not find any reaction to cinnamon after 6 days. In contrast, when wasps were trained either via drilling plus host feeding, three drilling events (spaced training), 1 h training, or 24 h training including oviposition, they significantly preferred cinnamon 6 days later. Wasps which were injected the transcription inhibitor actinomycin D after a 1-h training to block protein synthesis showed normal memory retention up to 3 days, but did not react to cinnamon after 4 and 6 days. Control experiments showed no influence of actinomycin D on the natural behaviour and the general odour discrimination ability of N. vitripennis. This demonstrates that protein synthesis-dependent LTM has been formed. To our knowledge this is the first time that LTM formation after drilling plus host feeding but without oviposition is demonstrated in a parasitic wasp. These results were combined with additional findings about anaesthesia-sensitive memory, anaesthesia-resistant memory, and intermediate memory to develop a multiphase model of memory dynamics in N. vitripennis and to discuss ecological adaptations of memory formation in N. vitripennis and other parasitic wasp species.
Winter Survival of Individual Honey Bees and Honey Bee Colonies Depends on Level of Varroa destructor Infestation
Dooremalen, C. van; Gerritsen, L.J.M. ; Cornelissen, B. ; Steen, J.J.M. van der; Langevelde, F. van; Blacquiere, T. - \ 2012
PLoS ONE 7 (2012)4. - ISSN 1932-6203
apis-mellifera colonies - jacobsoni oud - oxalic-acid - life-span - population - acari - hymenoptera - longevity - physiology - declines
Background: Recent elevated winter loss of honey bee colonies is a major concern. The presence of the mite Varroa destructor in colonies places an important pressure on bee health. V. destructor shortens the lifespan of individual bees, while long lifespan during winter is a primary requirement to survive until the next spring. We investigated in two subsequent years the effects of different levels of V. destructor infestation during the transition from short-lived summer bees to long-lived winter bees on the lifespan of individual bees and the survival of bee colonies during winter. Colonies treated earlier in the season to reduce V. destructor infestation during the development of winter bees were expected to have longer bee lifespan and higher colony survival after winter. Methodology/Principal Findings: Mite infestation was reduced using acaricide treatments during different months (July, August, September, or not treated). We found that the number of capped brood cells decreased drastically between August and November, while at the same time, the lifespan of the bees (marked cohorts) increased indicating the transition to winter bees. Low V. destructor infestation levels before and during the transition to winter bees resulted in an increase in lifespan of bees and higher colony survival compared to colonies that were not treated and that had higher infestation levels. A variety of stress-related factors could have contributed to the variation in longevity and winter survival that we found between years. Conclusions/Significance: This study contributes to theory about the multiple causes for the recent elevated colony losses in honey bees. Our study shows the correlation between long lifespan of winter bees and colony loss in spring. Moreover, we show that colonies treated earlier in the season had reduced V. destructor infestation during the development of winter bees resulting in longer bee lifespan and higher colony survival after winter.