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## Recent Publications

The Department of Entomology
The Robert H. Smith Faculty of Agriculture, Food and Environment
The Hebrew University of Jerusalem
Herzl 229, Rehovot 7610001, ISRAEL

Tel: 08-9489223
Fax: 08-9366768
Email: orlytal@savion.huji.ac.il

# Publications

2016
Kark, S. ; Sutherland, W. J. ; Shanas, U. ; Klass, K. ; Achisar, H. ; Dayan, T. ; Gavrieli, Y. ; Justo-Hanani, R. ; Mandelik, Y. ; Orion, N. ; et al. Priority questions and horizon scanning for conservation: A comparative study. PLoS ONE 2016, 11. Publisher's Version
Zidon, R. ; Tsueda, H. ; Morin, E. ; Morin, S. Projecting pest population dynamics under global warming: the combined effect of inter- and intra-annual variations. Ecological Applications 2016, 26, 1198-1210. Publisher's VersionAbstract
AbstractThe typical short generation length of insects makes their population dynamics highly sensitive not only to mean annual temperatures but also to their intra-annual variations. To consider the combined effect of both thermal factors under global warming, we propose a modeling framework that links general circulation models (GCMs) with a stochastic weather generator and population dynamics models to predict species population responses to inter- and intra-annual temperature changes. This framework was utilized to explore future changes in populations of Bemisia tabaci, an invasive insect pest-species that affects multiple agricultural systems in the Mediterranean region. We considered three locations representing different pest status and climatic conditions: Montpellier (France), Seville (Spain), and Beit-Jamal (Israel). We produced ensembles of local daily temperature realizations representing current and future (mid-21st century) climatic conditions under two emission scenarios for the three locations. Our simulations predicted a significant increase in the average number of annual generations and in population size, and a significant lengthening of the growing season in all three locations. A negative effect was found only in Seville for the summer season, where future temperatures lead to a reduction in population size. High variability in population size was observed between years with similar annual mean temperatures, suggesting a strong effect of intra-annual temperature variation. Critical periods were from late spring to late summer in Montpellier and from late winter to early summer in Seville and Beit-Jamal. Although our analysis suggested that earlier seasonal activity does not necessarily lead to increased populations load unless an additional generation is produced, it is highly likely that the insect will become a significant pest of open-fields at Mediterranean latitudes above 40° during the next 50 years. Our simulations also implied that current predictions based on mean temperature anomalies are relatively conservative and it is better to apply stochastic tools to resolve complex responses to climate change while taking natural variability into account. In summary, we propose a modeling framework capable of determining distinct intra-annual temperature patterns leading to large or small population sizes, for pest risk assessment and management planning of both natural and agricultural ecosystems.
Hendriksma, H. P. ; Shafir, S. Honey bee foragers balance colony nutritional deficiencies. 2016, 70, 509 - 517. Publisher's VersionAbstract
Honey bee colonies, foraging predominantly on a single pollen source, may encounter nutritional deficits. In the present study, we examined the nutritional resilience of honey bee colonies, testing whether foragers shift their foraging effort towards resources that complement a nutritional deficit. Eight honey bee colonies were kept in screened enclosures and fed for 1 week a pollen substitute diet deficient in a particular essential amino acid. Foragers were subsequently tested for a preference between the same diet previously fed, a different diet that was similarly deficient, or a diet that complemented the deficiency. Foragers preferred the complementary diet over the same or similar diets. Appetitive conditioning tests showed that bees were able to discriminate also between the same and similar diets. Overall, our results support the hypothesis that honey bees prefer dietary diversity, and that they do not just include novel sources but specifically target nutritionally complementary ones. Whereas we specifically focused on deficiencies in essential amino acids, we cannot rule out that bees were also complementing correlated imbalances in other nutrients, most notably essential fatty acids. The ability of honey bees to counter deficient nutrition contributes to the mechanisms which social insects use to sustain homeostasis at the colony level.
Hall, A. B. ; Papathanos, P. A. ; Sharma, A. ; Cheng, C. ; Akbari, O. S. ; Assour, L. ; Bergman, N. H. ; Cagnetti, A. ; Crisanti, A. ; Dottorini, T. ; et al. Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes. Proceedings of the National Academy of Sciences 2016, 113, E2114–E2123. Publisher's VersionAbstract
Interest in male mosquitoes has been motivated by the potential to develop novel vector control strategies, exploiting the fact that males do not feed on blood or transmit diseases, such as malaria. However, genetic studies of male Anopheles mosquitoes have been impeded by the lack of molecular characterization of the Y chromosome. Here we show that the Anopheles gambiae Y chromosome contains a very small repertoire of genes, with massively amplified tandem arrays of a small number of satellites and transposable elements constituting the vast majority of the sequence. These genes and repeats evolve rapidly, bringing about remodeling of the Y, even among closely related species. Our study provides a long-awaited foundation for studying mosquito Y chromosome biology and evolution.Y chromosomes control essential male functions in many species, including sex determination and fertility. However, because of obstacles posed by repeat-rich heterochromatin, knowledge of Y chromosome sequences is limited to a handful of model organisms, constraining our understanding of Y biology across the tree of life. Here, we leverage long single-molecule sequencing to determine the content and structure of the nonrecombining Y chromosome of the primary African malaria mosquito, Anopheles gambiae. We find that the An. gambiae Y consists almost entirely of a few massively amplified, tandemly arrayed repeats, some of which can recombine with similar repeats on the X chromosome. Sex-specific genome resequencing in a recent species radiation, the An. gambiae complex, revealed rapid sequence turnover within An. gambiae and among species. Exploiting 52 sex-specific An. gambiae RNA-Seq datasets representing all developmental stages, we identified a small repertoire of Y-linked genes that lack X gametologs and are not Y-linked in any other species except An. gambiae, with the notable exception of YG2, a candidate male-determining gene. YG2 is the only gene conserved and exclusive to the Y in all species examined, yet sequence similarity to YG2 is not detectable in the genome of a more distant mosquito relative, suggesting rapid evolution of Y chromosome genes in this highly dynamic genus of malaria vectors. The extensive characterization of the An. gambiae Y provides a long-awaited foundation for studying male mosquito biology, and will inform novel mosquito control strategies based on the manipulation of Y chromosomes.
Galizi, R. ; Hammond, A. ; Kyrou, K. ; Taxiarchi, C. ; Bernardini, F. ; O’Loughlin, S. M. ; Papathanos, P. A. ; Nolan, T. ; Windbichler, N. ; Crisanti, A. A CRISPR-Cas9 sex-ratio distortion system for genetic control. 2016, 6 31139. Publisher's VersionAbstract
Genetic control aims to reduce the ability of insect pest populations to cause harm via the release of modified insects. One strategy is to bias the reproductive sex ratio towards males so that a population decreases in size or is eliminated altogether due to a lack of females. We have shown previously that sex ratio distortion can be generated synthetically in the main human malaria vector Anopheles gambiae, by selectively destroying the X-chromosome during spermatogenesis, through the activity of a naturally-occurring endonuclease that targets a repetitive rDNA sequence highly-conserved in a wide range of organisms. Here we describe a CRISPR-Cas9 sex distortion system that targets ribosomal sequences restricted to the member species of the Anopheles gambiae complex. Expression of Cas9 during spermatogenesis resulted in RNA-guided shredding of the X-chromosome during male meiosis and produced extreme male bias among progeny in the absence of any significant reduction in fertility. The flexibility of CRISPR-Cas9 combined with the availability of genomic data for a range of insects renders this strategy broadly applicable for the species-specific control of any pest or vector species with an XY sex-determination system by targeting sequences exclusive to the female sex chromosome.
Malka, O. ; Shekhov, A. ; Reichelt, M. ; Gershenzon, J. ; Vassão, D. G. ; Morin, S. Glucosinolate Desulfation by the Phloem-Feeding Insect Bemisia tabaci. Journal of Chemical Ecology 2016, 42, 230–235. Publisher's VersionAbstract
Glucosinolates are plant secondary defense metabolites confined nearly exclusively to the order Brassicales. Upon tissue rupture, glucosinolates are hydrolyzed to various bioactive breakdown products by the endogenous plant enzyme myrosinase. As the feeding of chewing insect herbivores is associated with plant tissue damage, these insects have developed several independent strategies for coping with the glucosinolate-myrosinase defense system. On the other hand, our knowledge of how phloem-feeding insects interact with the glucosinolate-myrosinase system is much more limited. In fact, phloem feeders might avoid contact with myrosinase altogether so their susceptibility to intoxication by glucosinolate hydrolysis products is unclear. Previous studies utilizing Arabidopsis thaliana plants accumulating high levels of aliphatic- or indolic-glucosinolates indicated that both glucosinolate groups have moderate negative effects on the reproductive performance of Bemisia tabaci, a generalist phloem-feeding insect. To get a deeper understanding of the interaction between B. tabaci and glucosinolate-defended plants, adults were allowed to feed on artificial diet containing intact glucosinolates or on Brussels sprout and A. thaliana plants, and their honeydew was analyzed for the presence of possible metabolites. We found that B. tabaci is capable of cleaving off the sulfate group of intact glucosinolates, producing desulfoglucosinolates that cannot be activated by myrosinases, a mechanism described to date only in several chewing insect herbivores. The presence of desulfated glucosinolates in the honeydew of a generalist phloem-feeder may indicate the necessity to detoxify glucosinolates, likely due to some level of cellular damage during feeding, which results in glucosinolate activation, or as a mechanism to circumvent the non-enzymatic breakdown of indolic glucosinolates.
Roditakis, E. ; Morin, S. ; Baixeras, J. Is Bactra bactrana (Kennel, 1901) a novel pest of sweet peppers?. Bulletin of Entomological Research 2016, 106, 161-167. Publisher's VersionAbstract
This is the first report of Bactra bactrana (Kennel, 1901) (Lepidoptera: Tortricidae) attacking a major solanaceous crop, sweet pepper Capsicum annuum L. The infestation was detected in two greenhouses at the area of Tympaki (Southern Crete, Greece). The moth larvae caused typical symptoms of a fruit borer with numerous small holes on the surface of the peppers and extensive damage on the inside of the fruit as a result of the feeding activity. Unknown factors facilitated this major shift in host range since B. bactrana is typically a stem borer of sedges. In addition, the pest status of B. bactrana is currently under question, as in both cases the infestations by the moth were associated with significant yield losses. B. bactrana was moderately controlled with chemicals registered for Lepidoptera management in sweet pepper due to the boring nature of the infestation. Some comparative taxonomic notes are provided to facilitate accurate pest discrimination of related Bactra species. Finally, biological attributes of the species are summarized and are discussed from pest control and ecological perspectives. Because Bactra species have been used in augmentative releases for the control of sage, the implications of our findings on the release of biocontrol agents are placed in perspective.
Rader, R. ; Bartomeus, I. ; Garibaldi, L. A. ; Garratt, M. P. D. ; Howlett, B. G. ; Winfree, R. ; Cunningham, S. A. ; Mayfield, M. M. ; Arthur, A. D. ; Andersson, G. K. S. ; et al. Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences 2016, 113, 146–151. Publisher's VersionAbstract
Many of the world’s crops are pollinated by insects, and bees are often assumed to be the most important pollinators. To our knowledge, our study is the first quantitative evaluation of the relative contribution of non-bee pollinators to global pollinator-dependent crops. Across 39 studies we show that insects other than bees are efficient pollinators providing 39% of visits to crop flowers. A shift in perspective from a bee-only focus is needed for assessments of crop pollinator biodiversity and the economic value of pollination. These studies should also consider the services provided by other types of insects, such as flies, wasps, beetles, and butterflies—important pollinators that are currently overlooked.Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25–50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.
Kleijn, D. ; Winfree, R. ; Bartomeus, I. ; Carvalheiro, L. G. ; Henry, M. ; Isaacs, R. ; Klein, A. - M. ; Kremen, C. ; M’Gonigle, L. K. ; Rader, R. ; et al. Erratum: Corrigendum: Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. 2016, 7 10841. Publisher's VersionAbstract
Nature Communications 6: Article number: 7414 (2015); Published: 16 June 2015; Updated: 18 February 2016. The authors inadvertently omitted Kimiora L. Ward, who managed and contributed data, from the author list. This has now been corrected in both the PDF and HTML versions of the Article.
Pisanty, G. ; Afik, O. ; Wajnberg, E. ; Mandelik, Y. Watermelon pollinators exhibit complementarity in both visitation rate and single-visit pollination efficiency. Journal of Applied Ecology 2016, 53, 360-370. Publisher's VersionAbstract
Summary The concept of pollinator niche complementarity maintains that species-rich pollinator communities can provide higher and more stable pollination services than species-poor communities, due to contrasting spatial and/or temporal pollination activity among groups of pollinators. Complementarity has usually been examined in pollinators’ patterns of flower visitation or abundance, while largely neglecting the possibility of complementarity in patterns of single-visit contribution to fruit/seed set (pollination efficiency). However, variability in pollination efficiency can greatly affect pollinators’ overall pollination services and may therefore contribute an additional, important aspect of complementarity. In this study, we investigated the existence of pollinator complementarity in both visitation rates and pollination efficiencies. The study was conducted in 43 watermelon fields cultivated for seed consumption in a Mediterranean agro-natural landscape in central Israel. We studied spatiotemporal variation in pollinators’ visitation activity, measured by repeated observations and netting, and single-visit pollination efficiency, measured by the fruit and seed set rates of hermaphrodite flowers exposed to a single bee visit. Visitation and pollination efficiency were measured throughout the day and season, within and between fields with contrasting availability of nearby wild plants, and among flowers of different sizes. Pollinator species’ visitation rates as well as single-visit fruit set efficiencies, but not seed set efficiencies, exhibited significant spatiotemporal variation that contributed to their complementarity. Pollinators’ visit frequencies were affected by surrounding land use, location within field, time throughout the season, and time of day. Pollinators’ fruit set efficiencies were affected by ovary size and time of day. Synthesis and applications. Crop pollinators may exhibit complementarity in both their visitation rates and pollination efficiencies, which can promote the overall level and stability of their pollination services. Complementarity in pollination efficiencies suggests further diversity effects on crop yield, and calls for taking into account the variability in pollination efficiency along spatiotemporal scales rather than considering it a constant, species-specific trait. However, some modes of niche complementarity may not necessarily translate into increased pollination services and crop yield; the relevance and limitations of such mechanisms should be considered in the light of the specific crop and management system studied.
Carmel, I. ; Tram, U. ; Heifetz, Y. Mating induces developmental changes in the insect female reproductive tract. Current opinion in insect science 2016, 13, 106—113. Publisher's Version
Elgart, M. ; Stern, S. ; Salton, O. ; Gnainsky, Y. ; Heifetz, Y. ; Soen, Y. Impact of gut microbiota on the fly’s germ line. 2016, 7 11280. Publisher's VersionAbstract
Unlike vertically transmitted endosymbionts, which have broad effects on their host’s germ line, the extracellular gut microbiota is transmitted horizontally and is not known to influence the germ line. Here we provide evidence supporting the influence of these gut bacteria on the germ line of Drosophila melanogaster. Removal of the gut bacteria represses oogenesis, expedites maternal-to-zygotic-transition in the offspring and unmasks hidden phenotypic variation in mutants. We further show that the main impact on oogenesis is linked to the lack of gut Acetobacter species, and we identify the Drosophila Aldehyde dehydrogenase (Aldh) gene as an apparent mediator of repressed oogenesis in Acetobacter-depleted flies. The finding of interactions between the gut microbiota and the germ line has implications for reproduction, developmental robustness and adaptation.
Avila, F. W. ; Sánchez-López, J. A. ; McGlaughon, J. L. ; Raman, S. ; Wolfner, M. F. ; Heifetz, Y. Nature and Functions of Glands and Ducts in the Drosophila Reproductive Tract. In Extracellular Composite Matrices in Arthropods; Cohen, E. ; Moussian, B., Ed. Extracellular Composite Matrices in Arthropods; Springer International Publishing: Cham, 2016; pp. 411–444. Publisher's VersionAbstract
Successful reproduction requires interactions between males and females at many levels: the organisms, their cells (the gametes), and their molecules. Among the latter, secreted products of male and female reproductive glands are especially important. These molecules are particularly well understood in Drosophila melanogaster, because of this insect's excellent molecular genetic tools. Here, we discuss the biology of Drosophila reproductive glands, including their development, structure, and secreted products. These glands include important secretory centers, tissues that play roles in gamete maintenance and perhaps in modification, and organs that mediate dynamic transfer of gametes and molecules, and gamete support and/or discharge. Components of seminal fluid produced by male reproductive glands enter the female during mating. There, they interact with female proteins, neurons, and pathways to convert the female from a poised'' pre-mated state to an active post-mating state. This mated state is characterized by high levels of egg production, by sperm storage, and by post-mating behaviors related to re-mating, activity, and feeding. Female reproductive gland secretions include additional molecules important for sperm survival or egg transit. The interplay and coordination between male- and female-derived molecules is an area of intense study. Its conclusions are relevant to understanding reproduction in insects and, more broadly, in all animals, and as well as to questions about chemical communication, hormone biology and evolution.
Maoz, Y. ; Gal, S. ; Argov, Y. ; Domeratzky, S. ; Coll, M. ; Palevsky, E. Intraguild interactions among specialised pollen feeders and generalist phytoseiids and their effect on citrus rust mite suppression. Pest Management Science 2016, 72, 940-949. Publisher's VersionAbstract
Abstract BACKGROUND Antagonistic interactions among predators with shared prey are thought to hamper their ability to suppress herbivores. Our aim was to quantify intraguild interactions in omnivorous predatory mite assemblages in the presence of pollen, and assess their effect on pest populations. We focused on the following naturally occurring phytoseiid species in Israeli citrus orchards and their ability to suppress a key pest, the citrus rust mite (CRM) Phyllocoptruta oleivora (Eriophyidae): the generalists Amblyseius swirskii and Typhlodromus athiasae and the specialised pollen feeders Iphiseius degenerans, Euseius scutalis, E. stipulatus and E. victoriensis. Evaluations were performed on two spatial scales, tree seedlings and leaf discs. RESULTS On seedlings, experiments were conducted to quantify the interactions between predators in the presence of pollen and its effects on CRM suppression. On leaf discs, intraguild interactions were studied between pairs of phytoseiid species in the presence of pollen without CRM. On seedlings, the specialised pollen predators were more effective at suppressing CRM populations than the generalist predators. CONCLUSION In most cases, the more aggressive intraguild predator was the specialised pollen feeder. Similarly, leaf-disc experiments suggest that in these interactions the specialised pollen feeders tend to be the intraguild predators more often than the intraguild prey. © 2015 Society of Chemical Industry
Schuldiner-harpaz, T. ; Coll, M. ; Weintraub, P. G. Prey and Pollen Food Choice Depends on Previous Diet in an Omnivorous Predatory Mite. Environmental Entomology 2016, 45, 995-998. Publisher's VersionAbstract
The time allocated by omnivorous predators to consuming prey versus plant-provided foods (e.g., pollen) directly influences their efficacy as biocontrol agents of agricultural pests. Nonetheless, diet shifting between these two very different food sources remains poorly understood. We hypothesized that previous diet composition influences subsequent choice of prey and plant food types. We tested this hypothesis by observing the foraging choices of Amblyseius swirskii (Athias-Henriot) mites (Mesostigmata: Phytoseiidae), which were first maintained on either prey (broad mites) or corn pollen, and then offered familiar and unfamiliar foods. A. swirskii exhibited strong fidelity to familiar food, whether prey or pollen, suggesting there are physiological or behavioral costs involved in shifting between such different foods. Results illustrate the importance of previous diet for subsequent pest consumption by omnivorous natural enemies.
Dekel, A. ; Pitts, R. J. ; Yakir, E. ; Bohbot, J. D. Evolutionarily conserved odorant receptor function questions ecological context of octenol role in mosquitoes. 2016, 6 37330. Publisher's VersionAbstract
Olfaction is a key insect adaptation to a wide range of habitats. In the last thirty years, the detection of octenol by blood-feeding insects has been primarily understood in the context of animal host-seeking. The recent discovery of a conserved octenol receptor gene in the strictly nectar-feeding elephant mosquito Toxorhynchites amboinensis (TaOr8) suggests a different biological role. Here, we show that TaOR8 is a functional ortholog of its counterparts in blood-feeding mosquitoes displaying selectivity towards the (R)-enantiomer of octenol and susceptibility to the insect repellent DEET. These findings suggest that while the function of OR8 has been maintained throughout mosquito evolution, the context in which this receptor is operating has diverged in blood and nectar-feeding mosquitoes.
Ya'kobovitz, M. K. ; Butters, T. D. ; Cohen, E. Inhibition of α-glucosidase activity by N-deoxynojirimycin analogs in several insect phloem sap feeders. Insect Science 2016, 23, 59-67. Publisher's VersionAbstract
Abstract Secondary metabolites and synthetic iminosugars that structurally resemble monosaccharides are potent inhibitors of α-glucosidase activity. The enzyme is core in cleaving sucrose in phloem feeding insects and it also plays a crucial role of reducing osmotic stress via the formation of oligosaccharides. Inhibition of hydrolysis by iminosugars should result in nutritional deficiencies and/or disruption of normal osmoregulation. Deoxynojirimycin (DNJ) and 2 N-alkylated analogs [N-butyl DNJ (NB-DNJ) and N-nonyl DNJ (NN-DNJ)] were the major iminosugars used throughout the study. The extensive experiments conducted with α-glucosidase of the whitefly Bemisia tabaci indicated the competitive nature of inhibition and that the hydrophilic DNJ is a potent inhibitor in comparison to the more hydrophobic NB-DNJ and NN-DNJ compounds. The same inhibitory pattern was observed with the psyllid Cacopsylla bidens α-glucosidase. In contrast to the above pattern, enzymes of the aphids, Myzus persicae and Aphis gossypii were more sensitive to the hydrophobic iminosugars as compared to DNJ. In vivo experiments in which adult B. tabaci were fed dietary iminosugars, show that the hydrophilic DNJ was far less toxic than the lipophilic NB-DNJ and NN-DNJ. It is proposed that this pattern is attributed to the better accessibility of the hydrophobic NN-DNJ to the α-glucosidase membrane-bound compartment in the midgut. Based on the inhibitory effects of certain polyhydroxy N-alkylated iminosugars, α-glucosidase of phloem feeding hemipterans could serve as an attractive target site for developing novel pest control agents.