STATUS AND VALUE OF POLLINATORS AND POLLINATION SERVICES -A REPORT TO THE DEPARTMENT FOR ENVIRONMENT, FOOD AND RURAL AFFAIRS (Defra)

This commissioned review (Defra) considered how key environmental and economic pressures (e.g. land-use, disease) affected pollinator populations and communities and the pollination services they provide to wild plants and crops. The review summarized the evidence (or gaps in knowledge) for how changes to pollinators may limit pollination services. The ecological and economic impacts were considered with a focus on the main managed and wild pollinator groups involved in pollination services. Throughout the review the evidence basis, sources of uncertainty, knowledge gaps and research priorities were made clear. This report was influential in directly helping to shape the resulting National Pollinator Strategy and call for a national Pollinator Monitoring Scheme by Defra.

[1]  Emmanuelle Porcher,et al.  Plant mating systems in a changing world. , 2010, Trends in ecology & evolution.

[2]  S. Potts,et al.  Ecological and life-history traits predict bee species responses to environmental disturbances , 2010 .

[3]  J. Derisi,et al.  A New Threat to Honey Bees, the Parasitic Phorid Fly Apocephalus borealis , 2012, PloS one.

[4]  M. Nowakowski,et al.  Comparing the efficacy of agri‐environment schemes to enhance bumble bee abundance and diversity on arable field margins , 2006 .

[5]  D. Schroeder,et al.  Deformed Wing Virus Implicated in Overwintering Honeybee Colony Losses , 2009, Applied and Environmental Microbiology.

[6]  J. Cresswell A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees , 2011, Ecotoxicology.

[7]  D. Bailey,et al.  Functional richness of local hoverfly communities (Diptera, Syrphidae) in response to land use across temperate Europe , 2006, Oikos.

[8]  L. Carvalheiro,et al.  Pollinator networks, alien species and the conservation of rare plants: Trinia glauca as a case study , 2008 .

[9]  B. Edens,et al.  The changing wealth of nations , 2011 .

[10]  D. vanEngelsdorp,et al.  A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010 , 2011 .

[11]  M. Araújo,et al.  Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth , 2007 .

[12]  Roy A. Sanderson,et al.  Quantifying and comparing bumblebee nest densities in gardens and countryside habitats , 2007 .

[13]  Jane Memmott,et al.  The impact of an alien plant on a native plant-pollinator network: an experimental approach. , 2007, Ecology letters.

[14]  Kirsty J. Park,et al.  The trade-off between agriculture and biodiversity in marginal areas: Can crofting and bumblebee conservation be reconciled? , 2011 .

[15]  L. Carvalheiro,et al.  Pollination services decline with distance from natural habitat even in biodiversity‐rich areas , 2010 .

[16]  L. Chittka,et al.  Can commercially imported bumble bees out‐compete their native conspecifics? , 2006 .

[17]  I. Bartomeus,et al.  Biodiversity ensures plant-pollinator phenological synchrony against climate change. , 2013, Ecology letters.

[18]  Ruben H. Heleno,et al.  Invaders of pollination networks in the Galápagos Islands: emergence of novel communities , 2013, Proceedings of the Royal Society B: Biological Sciences.

[19]  A F G Bourke,et al.  Bumble bee species' responses to a targeted conservation measure depend on landscape context and habitat quality. , 2011, Ecological applications : a publication of the Ecological Society of America.

[20]  P. Williams The Distribution and Decline of British Bumble Bees (Bombus Latr.) , 1982 .

[21]  É. Thébault,et al.  Plant Pollinator Networks along a Gradient of Urbanisation , 2013, PloS one.

[22]  D. Goulson,et al.  Decline and conservation of bumble bees. , 2008, Annual review of entomology.

[23]  B. Schmid,et al.  Diverse pollinator communities enhance plant reproductive success , 2012, Proceedings of the Royal Society B: Biological Sciences.

[24]  I. Fries,et al.  Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. , 2006, Journal of invertebrate pathology.

[25]  R. Pywell,et al.  The potential impact of global warming on the efficacy of field margins sown for the conservation of bumble-bees , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  J. Ollerton,et al.  How many flowering plants are pollinated by animals , 2011 .

[27]  Jason M Tylianakis,et al.  Specialization and Rarity Predict Nonrandom Loss of Interactions from Mutualist Networks , 2012, Science.

[28]  Kelvin Balcombe,et al.  Pollination services in the UK: how important are honeybees? , 2011 .

[29]  Carsten F. Dormann,et al.  Indicators for biodiversity in agricultural landscapes: a pan‐European study , 2007 .

[30]  S. Martin,et al.  Do the honeybee pathogens Nosema ceranae and deformed wing virus act synergistically? , 2013, Environmental microbiology reports.

[31]  J. Thomson,et al.  Does Pathogen Spillover from Commercially Reared Bumble Bees Threaten Wild Pollinators? , 2008, PloS one.

[32]  S. Evison,et al.  The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies , 2013 .

[33]  Jay D. Evans,et al.  A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder , 2007, Science.

[34]  C. Kremen,et al.  Urban land use limits regional bumble bee gene flow , 2013, Molecular ecology.

[35]  A. P. Schaffers,et al.  Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands , 2006, Science.

[36]  D. Goulson,et al.  Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae) , 2006, Molecular ecology.

[37]  A. Klein,et al.  Synergistic effects of non-Apis bees and honey bees for pollination services , 2013, Proceedings of the Royal Society B: Biological Sciences.

[38]  C. Kremen,et al.  Valuing pollination services to agriculture , 2011 .

[39]  Amedeo Caflisch,et al.  The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. , 2010, Ecology letters.

[40]  J. Jiménez,et al.  How natural infection by Nosema ceranae causes honeybee colony collapse. , 2008, Environmental microbiology.

[41]  Quentin Groom,et al.  Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants , 2013, Ecology letters.

[42]  N. Smirnoff,et al.  Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). , 2012, Zoology.

[43]  J. Osborne,et al.  Estimation of bumblebee queen dispersal distances using sibship reconstruction method , 2010, Molecular ecology.

[44]  J. P. González‐Varo,et al.  Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis) , 2009 .

[45]  Claire Kremen,et al.  Contribution of Pollinator-Mediated Crops to Nutrients in the Human Food Supply , 2011, PloS one.

[46]  R. Bommarco,et al.  Drastic historic shifts in bumble-bee community composition in Sweden , 2012, Proceedings of the Royal Society B: Biological Sciences.

[47]  David W. Inouye,et al.  ENDANGERED MUTUALISMS: The Conservation of Plant-Pollinator Interactions , 1998 .

[48]  M. E. K N I G H T,et al.  Bumblebee nest density and the scale of available forage in arable landscapes , 2009 .

[49]  D. Ehret,et al.  OUT-OF-SEASON RASPBERRY PRODUCTION IN BRITISH COLUMBIA, CANADA , 2002 .

[50]  Carsten F. Dormann,et al.  Specialization of Mutualistic Interaction Networks Decreases toward Tropical Latitudes , 2012, Current Biology.

[51]  A. Shenkute,et al.  Natural and within-farmland biodiversity enhances crop productivity. , 2011, Ecology letters.

[52]  J C Stout,et al.  Quantifying the impacts of bioenergy crops on pollinating insect abundance and diversity: a field‐scale evaluation reveals taxon‐specific responses , 2013 .

[53]  Roy A. Sanderson,et al.  Effects of land use at a landscape scale on bumblebee nest density and survival , 2010 .

[54]  C. Dormann,et al.  Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination , 2011, Proceedings of the Royal Society B: Biological Sciences.

[55]  J C Stout,et al.  The impacts of an invasive alien plant and its removal on native bees , 2009, Apidologie.

[56]  Richard G. Jones,et al.  Declines of managed honey bees and beekeepers in Europe , 2010 .

[57]  Teja Tscharntke,et al.  Mass flowering crops enhance pollinator densities at a landscape scale , 2003 .

[58]  P. Verburg,et al.  Quantifying and mapping ecosystem services: Demand and supply of pollination in the European Union , 2014 .

[59]  J. Ghazoul Pollen and seed dispersal among dispersed plants , 2005, Biological reviews of the Cambridge Philosophical Society.

[60]  R. Isaacs,et al.  Stability of pollination services decreases with isolation from natural areas despite honey bee visits. , 2011, Ecology letters.

[61]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Bridget A. Emmett,et al.  An Integrated Assessment of Countryside Survey data to investigate Ecosystem Services in Great Britain. Countryside Survey Technical Report No. 10/07 , 2010 .

[63]  Buszko,et al.  Valuing Changes in Forest Biodiversity , 2008 .

[64]  J. Settele,et al.  Economic valuation of the vulnerability of world agriculture confronted with pollinator decline , 2009 .

[65]  S. John,et al.  Making Space for Nature: A review of England's Wildlife Sites and Ecological Network , 2010 .

[66]  J. Ollerton,et al.  Landscape structure influences pollinator movements and directly affects plant reproductive success , 2012 .

[67]  J. Kerr,et al.  Do pathogen spillover, pesticide use, or habitat loss explain recent North American bumblebee declines? , 2012 .

[68]  R. Gegear,et al.  Plight of the bumble bee: Pathogen spillover from commercial to wild populations , 2006 .

[69]  S. Cunningham,et al.  Diurnal effectiveness of pollination by bees and flies in agricultural Brassica rapa: Implications for ecosystem resilience , 2013 .

[70]  M. Vilà,et al.  Combined effects of Impatiens glandulifera invasion and landscape structure on native plant pollination , 2010 .

[71]  R. Veldtman,et al.  Valuing Insect Pollination Services with Cost of Replacement , 2008, PloS one.

[72]  S. Potts,et al.  POLLINATION DEFICITS IN UK APPLE ORCHARDS , 2014 .

[73]  A. Klein,et al.  Importance of pollinators in changing landscapes for world crops , 2007, Proceedings of the Royal Society B: Biological Sciences.

[74]  S. Nilsson,et al.  How can we preserve and restore species richness of pollinating insects on agricultural land , 2008 .

[75]  David B. Roy,et al.  Declines in forage availability for bumblebees at a national scale , 2006 .

[76]  A. Klein,et al.  Biodiversity buffers pollination from changes in environmental conditions , 2013, Global change biology.

[77]  D. Goulson,et al.  Genetic diversity, parasite prevalence and immunity in wild bumblebees , 2011, Proceedings of the Royal Society B: Biological Sciences.

[78]  M. Aizen,et al.  A meta-analysis of bees' responses to anthropogenic disturbance. , 2009, Ecology.

[79]  T. Lennartsson Extinction thresholds and disrupted plant-pollinator interactions in fragmented plant populations , 2002 .

[80]  D. Goulson,et al.  Causes of rarity in bumblebees , 2005 .

[81]  E. Holmes,et al.  RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species , 2010, PloS one.

[82]  J. Biesmeijer,et al.  Avoiding a bad apple: Insect pollination enhances fruit quality and economic value☆ , 2014, Agriculture, ecosystems & environment.

[83]  Breno M. Freitas,et al.  Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance , 2013, Science.

[84]  J. Biesmeijer,et al.  Dispersal capacity and diet breadth modify the response of wild bees to habitat loss , 2010, Proceedings of the Royal Society B: Biological Sciences.

[85]  J. Derisi,et al.  Temporal Analysis of the Honey Bee Microbiome Reveals Four Novel Viruses and Seasonal Prevalence of Known Viruses, Nosema, and Crithidia , 2011, PloS one.

[86]  T. Murray,et al.  Rarity and decline in bumblebees - : A test of causes and correlates in the Irish fauna , 2007 .

[87]  Jane Memmott,et al.  The restoration of parasites, parasitoids, and pathogens to heathland communities. , 2009, Ecology.

[88]  D. Goulson,et al.  Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae) , 2006, Molecular ecology.

[89]  Teja Tscharntke,et al.  Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis , 2011, Proceedings of the Royal Society B: Biological Sciences.

[90]  J. Parnell,et al.  Pollination Ecology and Seed Production of Rhododendron Ponticum in Native and Exotic Habitats , 2006, Biodiversity & Conservation.

[91]  N. E. Raine,et al.  Impact of chronic exposure to a pyrethroid pesticide on bumblebees and interactions with a trypanosome parasite , 2014 .

[92]  Mark J. F. Brown,et al.  A qualitative model of mortality in honey bee (Apis mellifera) colonies infested with tracheal mites (Acarapis woodi) , 2009, Experimental and Applied Acarology.

[93]  Diego P. Vázquez,et al.  Indirect effects of an introduced ungulate on pollination and plant reproduction , 2004 .

[94]  J C Stout,et al.  Relative abundance of an invasive alien plant affects native pollination processes , 2011, Oecologia.

[95]  W. Sutherland,et al.  Post‐war changes in arable farming and biodiversity in Great Britain , 2002 .

[96]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[97]  M. Hoyle,et al.  Effect of pollinator abundance on self-fertilization and gene flow: application to GM Canola. , 2007, Ecological applications : a publication of the Ecological Society of America.

[98]  C. Kremen,et al.  Are ecosystem services stabilized by differences among species? A test using crop pollination , 2009, Proceedings of the Royal Society B: Biological Sciences.

[99]  Adam J. Vanbergen,et al.  Frontiers inEcology and the Environment Threats to an ecosystem service : pressures on pollinators , 2013 .

[100]  K. F. Conrad,et al.  The state of Britain's larger moths , 2006 .

[101]  D. Goulson,et al.  Biotope Associations and the Decline of Bumblebees (Bombus spp.) , 2006, Journal of Insect Conservation.

[102]  J. Biesmeijer,et al.  Biodiversity change is scale-dependent: an example from Dutch and UK hoverflies (Diptera, Syrphidae) , 2011 .

[103]  D. Goulson,et al.  Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production , 2012, Science.

[104]  L. Chittka,et al.  Winter Active Bumblebees (Bombus terrestris) Achieve High Foraging Rates in Urban Britain , 2010, PloS one.

[105]  J. Greenwood,et al.  Comparative Losses of British Butterflies, Birds, and Plants and the Global Extinction Crisis , 2004, Science.

[106]  I. Bartomeus,et al.  Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops , 2013, Global change biology.

[107]  A. Bourke,et al.  Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemes , 2007, Biology Letters.

[108]  Warren,et al.  The State of the UK's Butterflies 2011 , 2011 .

[109]  S. Cavers,et al.  Grazing alters insect visitation networks and plant mating systems , 2014 .

[110]  A. Bourke,et al.  Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus) , 2010, Molecular ecology.

[111]  James Regetz,et al.  Landscape effects on crop pollination services: are there general patterns? , 2008, Ecology letters.

[112]  Insect pollination enhances seed yield, quality, and market value in oilseed rape , 2012, Oecologia.

[113]  A. Klein,et al.  Wild pollination services to California almond rely on semi‐natural habitat , 2012 .

[114]  R. E. Page,et al.  Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on Feral Apis mellifera (Hymenoptera: Apidae) in California , 1995 .

[115]  S. Makino,et al.  Alien pollinator promotes invasive mutualism in an insular pollination system , 2011, Biological Invasions.

[116]  P. Rothery,et al.  Effects of resource availability and social parasite invasion on field colonies of Bombus terrestris , 2008 .

[117]  G. Budge,et al.  The occurrence of Melissococcus plutonius in healthy colonies of Apis mellifera and the efficacy of European foulbrood control measures. , 2010, Journal of invertebrate pathology.

[118]  C. Dick Genetic rescue of remnant tropical trees by an alien pollinator. , 2001, Proceedings. Biological sciences.

[119]  Mark Hill,et al.  Local frequency as a key to interpreting species occurrence data when recording effort is not known , 2012 .

[120]  Rodrigo Ramos-Jiliberto,et al.  Adaptive foraging allows the maintenance of biodiversity of pollination networks , 2013 .

[121]  Brian Huntley,et al.  Impacts of landscape structure on butterfly range expansion , 2001 .

[122]  M. Aizen,et al.  Long-Term Global Trends in Crop Yield and Production Reveal No Current Pollination Shortage but Increasing Pollinator Dependency , 2008, Current Biology.

[123]  V. Wolters,et al.  Oilseed rape crops distort plant-pollinator interactions. , 2010 .

[124]  W. Ritter,et al.  Varroa mites and honey bee health: can Varroa explain part of the colony losses? , 2010, Apidologie.

[125]  Jeffrey D. Lozier,et al.  Patterns of widespread decline in North American bumble bees , 2011, Proceedings of the National Academy of Sciences.

[126]  Marco Vighi,et al.  Impacts of a pesticide on pollinator species richness at different spatial scales , 2010 .

[127]  J. K. Hill,et al.  Rapid responses of British butterflies to opposing forces of climate and habitat change , 2001, Nature.

[128]  Jane Memmott,et al.  Tolerance of pollination networks to species extinctions , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[129]  S. Potts,et al.  Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss--a meta-analysis. , 2013, Ecology letters.

[130]  Tracy M. Turner The Measurement of Environmental and Resource Values , 2004 .

[131]  N. Mawdsley,et al.  Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest , 1998, Nature.

[132]  Debra Bailey,et al.  Prediction uncertainty of environmental change effects on temperate European biodiversity. , 2008, Ecology letters.

[133]  Rabih E. Jabbour,et al.  Iridovirus and Microsporidian Linked to Honey Bee Colony Decline , 2010, PloS one.

[134]  Robert E. Wright,et al.  Valuing the diversity of biodiversity , 2006 .

[135]  Xiaolong Yang,et al.  Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[136]  C. Zachariades,et al.  Effects of Habitat Fragmentation on Pollinator Diversity and Plant Reproductive Success in Renosterveld Shrublands of South Africa , 2002 .

[137]  P. Legendre,et al.  A distance-based framework for measuring functional diversity from multiple traits. , 2010, Ecology.

[138]  Teja Tscharntke,et al.  Functional group diversity of bee pollinators increases crop yield , 2008, Proceedings of the Royal Society B: Biological Sciences.

[139]  P. Schmid-Hempel,et al.  Parasites and flower choice of bumblebees , 1998, Animal Behaviour.

[140]  S. Williamson,et al.  Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees , 2013, Journal of Experimental Biology.

[141]  D. Goulson,et al.  Preferred nesting sites of bumblebee queens (Hymenoptera: Apidae) in agroecosystems in the UK , 2003 .

[142]  David Kleijn,et al.  A retrospective analysis of pollen host plant use by stable and declining bumble bee species. , 2008, Ecology.

[143]  Stefan Baumgärtner THE INSURANCE VALUE OF BIODIVERSITY IN THE PROVISION OF ECOSYSTEM SERVICES , 2005 .

[144]  Richard J. Gill,et al.  Combined pesticide exposure severely affects individual- and colony-level traits in bees , 2012, Nature.

[145]  M. Warren,et al.  The state of Britain's larger moths 2013 , 2006 .

[146]  Mickaël Henry,et al.  A Common Pesticide Decreases Foraging Success and Survival in Honey Bees , 2012, Science.

[147]  J. Biesmeijer,et al.  Combined effects of global change pressures on animal-mediated pollination. , 2013, Trends in ecology & evolution.

[148]  W. Meek,et al.  Crop flower visitation by honeybees, bumblebees and solitary bees: Behavioural differences and diversity responses to landscape , 2013 .

[149]  D. Goulson REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides , 2013 .

[150]  J. Biesmeijer,et al.  Agricultural Policies Exacerbate Honeybee Pollination Service Supply-Demand Mismatches Across Europe , 2014, PloS one.

[151]  Jane Memmott,et al.  Global warming and the disruption of plant-pollinator interactions. , 2007, Ecology letters.

[152]  D. Roy,et al.  National patterns of functional diversity and redundancy in predatory ground beetles and bees associated with key UK arable crops , 2014 .

[153]  J. Baudry,et al.  Solitary bee abundance and species richness in dynamic agricultural landscapes , 2013 .

[154]  G. Smagghe,et al.  Effects of Invasive Parasites on Bumble Bee Declines , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[155]  J. Osborne,et al.  Two Bee-Pollinated Plant Species Show Higher Seed Production when Grown in Gardens Compared to Arable Farmland , 2010, PloS one.

[156]  D. Thomson COMPETITIVE INTERACTIONS BETWEEN THE INVASIVE EUROPEAN HONEY BEE AND NATIVE BUMBLE BEES , 2004 .

[157]  W. Jordan,et al.  Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee species , 2012 .

[158]  T. Blacquière,et al.  Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment , 2012, Ecotoxicology.

[159]  Marcelo A. Aizen,et al.  The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination , 2009, Current Biology.

[160]  P. Schmid-Hempel,et al.  Incidence and effects of four parasites in natural populations of bumble bees in Switzerland , 1991 .

[161]  K. Arrow,et al.  Sustainability and the measurement of wealth , 2010, Environment and Development Economics.

[162]  L. Harder,et al.  Global growth and stability of agricultural yield decrease with pollinator dependence , 2011, Proceedings of the National Academy of Sciences.

[163]  I. Fries,et al.  Estimating the Density of Honeybee Colonies across Their Natural Range to Fill the Gap in Pollinator Decline Censuses , 2010, Conservation biology : the journal of the Society for Conservation Biology.

[164]  Geraldine A. Wright,et al.  Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees , 2013, Nature Communications.

[165]  D. Guez A common pesticide decreases foraging success and survival in honey bees: questioning the ecological relevance , 2013, Frontiers in Physiology.

[166]  N. Calderone,et al.  Insect Pollinated Crops, Insect Pollinators and US Agriculture: Trend Analysis of Aggregate Data for the Period 1992–2009 , 2012, PloS one.

[167]  T. Dines,et al.  New atlas of the British and Irish flora. An atlas of the vascular plants of Britain, Ireland, the Isle of Man and the Channel Islands. , 2002 .

[168]  I. Fries,et al.  Research strategies to improve honeybee health in Europe , 2010, Apidologie.

[169]  Peter Rothery,et al.  A general method for measuring relative change in range size from biological atlas data , 2002 .

[170]  Alana L. Burley,et al.  A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. , 2013, Ecology letters.

[171]  G. Budge,et al.  Quantifying the value of ecosystem services: a case study of honeybee pollination in the UK , 2010 .

[172]  Richard J. Gill,et al.  Chronic sublethal stress causes bee colony failure , 2013, Ecology letters.

[173]  Paul H. Williams,et al.  Bumblebee vulnerability and conservation world-wide , 2009, Apidologie.

[174]  W. Kunin Population size and density effects in pollination : Pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber , 1997 .

[175]  E. Barbier Capitalizing on Nature: Ecosystems as Natural Assets , 2011 .

[176]  K. M. Cobb,et al.  Global Honey Bee Viral Landscape Altered by a Parasitic Mite , 2012 .

[177]  Anna S. Persson,et al.  Gardens benefit bees and enhance pollination in intensively managed farmland , 2011 .

[178]  J. Ghazoul,et al.  Effects of population size on plant reproduction and pollinator abundance in a specialized pollination system , 2010 .

[179]  Sherman Robinson,et al.  The future of the global food system , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[180]  Tim G Benton,et al.  Scale matters: the impact of organic farming on biodiversity at different spatial scales. , 2010, Ecology letters.

[181]  I. Fries,et al.  Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis , 2007, Apidologie.

[182]  J. Cresswell,et al.  The influence of pollinator abundance on the dynamics and efficiency of pollination in agricultural Brassica napus: implications for landscape‐scale gene dispersal , 2006 .

[183]  N. Hanley,et al.  The "Crex crex" Lament: Estimating Landowners Willingness to Pay for Corncrake Conservation on Irish Farmland , 2009 .