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The Department of Entomology
The Robert H. Smith Faculty of Agriculture, Food and Environment
The Hebrew University of Jerusalem
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Senapathi, D. ; Fruend, J. ; Albrecht, M. ; Garratt, M. P. D. ; Kleijn, D. ; Pickles, B. J. ; Potts, S. G. ; An, J. ; Andersson, G. K. S. ; Baensch, S. ; et al. Wild insect diversity increases inter-annual stability in global crop pollinator communities. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 2021, 288.Abstract
While an increasing number of studies indicate that the range, diversity and abundance of many wild pollinators has declined, the global area of pollinator-dependent crops has significantly increased over the last few decades. Crop pollination studies to date have mainly focused on either identifying different guilds pollinating various crops, or on factors driving spatial changes and turnover observed in these communities. The mechanisms driving temporal stability for ecosystem functioning and services, however, remain poorly understood. Our study quantifies temporal variability observed in crop pollinators in 21 different crops across multiple years at a global scale. Using data from 43 studies from six continents, we show that (i) higher pollinator diversity confers greater inter-annual stability in pollinator communities, (ii) temporal variation observed in pollinator abundance is primarily driven by the three-most dominant species, and (iii) crops in tropical regions demonstrate higher inter-annual variability in pollinator species richness than crops in temperate regions. We highlight the importance of recognizing wild pollinator diversity in agricultural landscapes to stabilize pollinator persistence across years to protect both biodiversity and crop pollination services. Short-term agricultural management practices aimed at dominant species for stabilizing pollination services need to be considered alongside longer term conservation goals focussed on maintaining and facilitating biodiversity to confer ecological stability.
Daughenbaugh, K. F. ; Kahnonitch, I. ; Carey, C. C. ; McMenamin, A. J. ; Wiegand, T. ; Erez, T. ; Arkin, N. ; Ross, B. ; Wiedenheft, B. ; Sadeh, A. ; et al. Metatranscriptome Analysis of Sympatric Bee Species Identifies Bee Virus Variants and a New Virus, Andrena-Associated Bee Virus-1. VIRUSES-BASEL 2021, 13.Abstract
Bees are important plant pollinators in agricultural and natural ecosystems. High average annual losses of honey bee (Apis mellifera) colonies in some parts of the world, and regional population declines of some mining bee species (Andrena spp.), are attributed to multiple factors including habitat loss, lack of quality forage, insecticide exposure, and pathogens, including viruses. While research has primarily focused on viruses in honey bees, many of these viruses have a broad host range. It is therefore important to apply a community level approach in studying the epidemiology of bee viruses. We utilized high-throughput sequencing to evaluate viral diversity and viral sharing in sympatric, co-foraging bees in the context of habitat type. Variants of four common viruses (i.e., black queen cell virus, deformed wing virus, Lake Sinai virus 2, and Lake Sinai virus NE) were identified in honey bee and mining bee samples, and the high degree of nucleotide identity in the virus consensus sequences obtained from both taxa indicates virus sharing. We discovered a unique bipartite + ssRNA Tombo-like virus, Andrena-associated bee virus-1 (AnBV-1). AnBV-1 infects mining bees, honey bees, and primary honey bee pupal cells maintained in culture. AnBV-1 prevalence and abundance was greater in mining bees than in honey bees. Statistical modeling that examined the roles of ecological factors, including floral diversity and abundance, indicated that AnBV-1 infection prevalence in honey bees was greater in habitats with low floral diversity and abundance, and that interspecific virus transmission is strongly modulated by the floral community in the habitat. These results suggest that land management strategies that aim to enhance floral diversity and abundance may reduce AnBV-1 spread between co-foraging bees.
Cole, L. J. ; Kleijn, D. ; Dicks, L. V. ; Stout, J. C. ; Potts, S. G. ; Albrecht, M. ; Balzan, M. V. ; Bartomeus, I. ; Bebeli, P. J. ; Bevk, D. ; et al. A critical analysis of the potential for EU Common Agricultural Policy measures to support wild pollinators on farmland. JOURNAL OF APPLIED ECOLOGY 2020, 57, 681-694.Abstract
Agricultural intensification and associated loss of high-quality habitats are key drivers of insect pollinator declines. With the aim of decreasing the environmental impact of agriculture, the 2014 EU Common Agricultural Policy (CAP) defined a set of habitat and landscape features (Ecological Focus Areas: EFAs) farmers could select from as a requirement to receive basic farm payments. To inform the post-2020 CAP, we performed a European-scale evaluation to determine how different EFA options vary in their potential to support insect pollinators under standard and pollinator-friendly management, as well as the extent of farmer uptake. A structured Delphi elicitation process engaged 22 experts from 18 European countries to evaluate EFAs options. By considering life cycle requirements of key pollinating taxa (i.e. bumble bees, solitary bees and hoverflies), each option was evaluated for its potential to provide forage, bee nesting sites and hoverfly larval resources. EFA options varied substantially in the resources they were perceived to provide and their effectiveness varied geographically and temporally. For example, field margins provide relatively good forage throughout the season in Southern and Eastern Europe but lacked early-season forage in Northern and Western Europe. Under standard management, no single EFA option achieved high scores across resource categories and a scarcity of late season forage was perceived. Experts identified substantial opportunities to improve habitat quality by adopting pollinator-friendly management. Improving management alone was, however, unlikely to ensure that all pollinator resource requirements were met. Our analyses suggest that a combination of poor management, differences in the inherent pollinator habitat quality and uptake bias towards catch crops and nitrogen-fixing crops severely limit the potential of EFAs to support pollinators in European agricultural landscapes. Policy Implications. To conserve pollinators and help protect pollination services, our expert elicitation highlights the need to create a variety of interconnected, well-managed habitats that complement each other in the resources they offer. To achieve this the Common Agricultural Policy post-2020 should take a holistic view to implementation that integrates the different delivery vehicles aimed at protecting biodiversity (e.g. enhanced conditionality, eco-schemes and agri-environment and climate measures). To improve habitat quality we recommend an effective monitoring framework with target-orientated indicators and to facilitate the spatial targeting of options collaboration between land managers should be incentivised.
Shapira, T. ; Henkin, Z. ; Dag, A. ; Mandelik, Y. Rangeland sharing by cattle and bees: moderate grazing does not impair bee communities and resource availability. ECOLOGICAL APPLICATIONS 2020, 30.Abstract
Rangelands are a dominant anthropogenic land use and a main driver of natural habitat loss worldwide. Land sharing, the integration of agricultural production and biodiversity conservation, may provide a platform for managing rangelands to fulfill multiple ecosystem services. However, livestock grazing can greatly affect biodiversity and little is known about its effects on providers of focal ecosystem services, such as pollinators. We investigated the effect of cattle grazing on bee communities and their foraging and nesting resources in Mediterranean rangelands. Specifically, we explored the effect of moderate cattle grazing on flowering plant abundance, species richness and composition, the diversity of nesting substrates, and consequently, the possible effects on wild bee and honey bee foraging activity, species diversity, and community composition. We conducted field research in the Mediterranean rangelands of Israel during the main bee activity season, in the spring of 2012 and 2013, comparing paired cattle-grazed and ungrazed areas. The availability of floral and nesting resources for bees was unaffected or positively affected by grazing. Similarly, wild bee abundance, species richness, and composition were not affected by grazing, but were instead shaped by spatiotemporal factors. Nor was honey bee activity level impaired by grazing. The foraging preferences of bees, as well as flower species composition and peak bloom differed between grazed and ungrazed areas. Therefore, in our studied rangelands, grazing had its main effect on the foraging choices of honey bees and wild bees, rather than on their abundance and diversity. Moreover, our results indicate the potentially important role of ungrazed patches in increasing nectar and pollen diversity and availability in rangelands for both honey bees and wild bees in the spring. Hence, maintaining a mosaic of moderately grazed and ungrazed patches is expected to provide the greatest benefits for wild bee conservation and honey bee activity in Mediterranean rangelands. Our findings support the notion of rangeland sharing by cattle and bees in Mediterranean ecosystems under moderate grazing intensities, mimicking the coexistence of honey bees, wild bees, and cattle in Mediterranean ecosystems on an evolutionary timescale.
Lotan, A. ; Kost, R. ; Mandelik, Y. ; Peled, Y. ; Chakuki, D. ; Shamir, S. Z. ; Ram, Y. National scale mapping of ecosystem services in Israel - Genetic resources, pollination and cultural services. One Ecosystem 2018, 3. Publisher's VersionAbstract
The Israel - National Ecosystem Assessment (I-NEA) project aims to present a comprehensive picture of the state and trends of Israel’s ecosystem services across all ecosystems, by integrating existing data and information collected from a wide range of sources. Although there is a lack of information about the spatial distribution of ecosystem services’ provisioning in Israel, their mapping constitutes an important part of the assessment. In this paper, we present a national-scale mapping of three ecosystem services, each of them implemented using different methods: 1) Genetic resources service, mapped using spatial observations of the Crop Wild Relatives species; 2) potential of pollination service, which is provided by wild bees, mapped using an expert-based habitat model related to land use and land cover; and 3) cultural service of recreation, mapped by analysing the distribution of geotagged digital photographs uploaded to social media resources. The derived maps visualise, for the first time in Israel, the spatially distributed values of the three ecosystem services. Supply hotspots with high values for all three services were identified, as well as spatial differences amongst the ecosystem services. These nationalscale maps provide overlooked insights and can be very useful for strategic discussions of stakeholders and decision-makers but should be regarded with caution given existing knowledge gaps and possible inaccuracies due to data scarcity and low resolution. © Lotan A et al.
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
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.