Causes and consequences of pollinator decline EU Pollinator Initiative Workshop 15/03/2018 BELSPO (Belgian Science Policy Office), Avenue Louise 231, 1050 Brussels

Dr Adam Vanbergen NERC Centre for Ecology & Hydrology (CEH) Edinburgh [email protected] ex-USSR USA Germany

China Argentina Spain Drivers of change in pollinators

• Land use change • Land management (intensity, GMO etc.) • Pesticides (insecticides, herbicides) • Pollinator diseases & bee husbandry • Climate change • Invasive alien species Land use change

• Reduction in food, nesting or other resources Loss of habitat Fragmentation Degradation • Applies to agricultural, natural, urban and biocultural areas • Loss of practices based on Indigenous and Local Knowledge, which can be beneficial to nature Land-use change, pollinator networks & plant mating

UNGRAZED n=4

34 N= 10 32

30

28 N= 10 26

24

22

20 Ungrazed Grazed

Flowering plant species richness species plant Flowering Birch Woods

GRAZED n=5

0.8 1.0 = fully outcrossed AICc wi = 0.88 AICc wi = 0.44

)

m 0.9 0.7 0.6 0.8 0.5 0.7 0.4 0.6 0.3

0.5 0.2

Network Connectance

Outcrossing rate (t rate Outcrossing 0.4 0.1 4 6 8 10 12 14 16 18 20 22 24 0.2 0.4 0.6 0.8 Floral Species Richness Standardised Connectance

Vanbergen et al. (2014) Functional Ecology 28 178-189 Intensive agriculture

• Loss of non-cultivated habitat patches • Large field sizes and monocultures • High inputs of fertilizers, pesticides, herbicides etc. • Intensive grazing Pesticides

• Broad range of lethal and sub-lethal effects • Impacts vary with compound toxicity, exposure level, location and pollinator species • Risks can be increased if: Labelling is insufficient or not respected Application equipment is faulty or not fit-for-purpose Risk assessment or regulations are insufficient Neonicotinoid use & pollinator decline: a 17 year correlation

Oilseed rape cover (+ve) Volunteer surveys of bees -18% BWARS Bees, Wasps & Ants Recording Society

Red = Actual trend; Neonicotinoid use (-ve) Blue = Estimated trend if NNI were benign

Bees feedingOSR Foragers on rape negatively affected Non-foragers

Other pesticides (ns) Probability

Negative Positive

B.A. Woodcock et al. (2016) Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nature Communications 7, 12459. doi:10.1038/ncomms12459 Neonicotinoids (NNI) & bee health: a landscape experiment

Potential negative • Negative & positive effects interacting factors on honeybee colony health • Negative effects on reproduction of wild bee species (B. terrestris, O. bicornis)

Bee diet: Worse where • More persistent in oilseed rape forms soil than expected much of diet 700 Germany 600 Hungary UK

500 Image credit: Bayer credit: Image 400 300 200

New New queens 100 0 Bee health: Worse 0 1 2 3 4 5 6 7 8 9 where bees have high Neonicotinoid residues found in nests (ng g-1) disease load

B. A. Woodcock et.al. (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science. 356, 6345, 1393-1395 doi: 10.1126/science.aaa1190 Pests & pathogens

Varroa mite (Varroa Deformed Wing Virus destructor) on a electron density image honeybee. Source: Pavel Plevak Source: Rob Paxton

Nosema ceranae Asian hornet (Vespa velutina) a fungal parasite eating a honeybee. of honeybees Source Alain C. Source: Ingemar Fries Bee trade, pests and pathogens

Ryabov et al. 2014. PLoS Pathog 10 Wilfert et al 2016. Science 351 Martin et al 2012. Science 336 Szabo et al 2012.Conservation Letters 5 Furst et al 2014. Nature 506 McMahon et al . 2015. JAE 84 Moritz et al 2005. Ecoscience 12 Vanbergen et al. 2018, Nature Ecology & Evolution 2 Climate Change • For some pollinators (e.g. bumblebees and butterflies): Range changes Altered abundance Shifts in seasonal activities Risk of disruption of future crop pollination • Climate shifts across landscapes may exceed species dispersal abilities

Jeremy T. Kerr et al. Science 2015;349:177-180 Invasive alien species • Identity and evolutionary history of the invader & recipient ecosystem matters…

Asian hornet (Vespa velutina) and honeybee

Bartomeus, et al. 2010.. Journal of Ecology 98. Vila, et al. 2009. PRSB 276. Lopezaraiza-Mikelet al 2007. Ecology Letters 10 Vanbergen et al. 2018, Nature Ecology & Evolution 2 Multiple impacts across biological scales

Vanbergen A.J. and the Insect Pollinators Initiative (2013). Threats to an ecosystem service: pressures on pollinators. Frontiers in Ecology and the Environment Other potential drivers • Pollution - Heavy metals - Nutrients (e.g. Nitrogen) - Particulates (e.g. diesel) - EMR: visible light; other wavelengths (e.g. 3/4/5G) • Fungicides & their interactions Risks of pollinator decline

• More than 75% of leading food crops • Almost 90% of the world’s flowering plants Rely, at least in part, on animal pollination Status of insect-pollinated wild plants

Non-conservation status plant species • Insect pollinator dependence correlated with plant decline

t = 5.23, d.f.= 465.72, P<0.001

Conservation status plant species • Threatened plants dependent on pollinators declined >4x rate of species not dependent

t = 3.53, d.f= 48.63 P<0.001 Vanbergen A.J., Heard, M.S., Breeze, T., Potts, S.G. & Hanley, N. (2014) Status and value of pollinators and pollination services - A report for the Department for Environment, Food and Rural Affairs (Defra UK) Contract number: PH0514. Status of insect-pollinated wild plants

Non-conservation status plant species • Insect pollinator dependence correlated What are the consequenceswith plant declinefor the organisms, above and belowground, t = 5.23,linked d.f.= 465.72, P<0.001 to declining pollinator- Conservation statusdependent plant species plants?• Threatened plants dependent on pollinators declined >4x rate of Is pollination a keystonespecies interaction? not dependent

t = 3.53, d.f= 48.63 P<0.001 Vanbergen A.J., Heard, M.S., Breeze, T., Potts, S.G. & Hanley, N. (2014) Status and value of pollinators and pollination services - A report for the Department for Environment, Food and Rural Affairs (Defra UK) Contract number: PH0514. Pollinators increase crop yields

•CropWild pollination insect visitation services enhances crop production & stability • Honey bee visitation has weaker effect, which supplements, but does not replace, the pollination service by wild insects

Rader et al. (2015) PNAS.

Garibaldi et al. Science 2013 339:1608-1611 Crop pollination: by few species

• ~80% of crop pollination delivered by 2% of bee species • These are common & perhaps robust to agricultural intensification But pollinator diversity may provide resilient pollination services

Kleijn, et al (2015) Nature Communincations, 6. Crop pollination: diversity matters Crop• Diversity pollination and identity services of pollinators varies between crops • Species pool varies for a given crop across geographic regions

Rader et al. PNAS 2015 doi/10.1073/pnas.1517092112 Potential crop pollination deficits? • Bee species richness or functional diversity

• Modelled from species occurrence records-0.25 - -0.125 -0.125 - 0 0 - 0.125 • Related to agricultural statistics (e.g. crop0.125 cover - 0.25 )

High FD Low FD

National distribution of functional diversity of native crop pollinators. Note potential deficits in areas of important crop production

Woodcock, et al (2014) Journal of Applied Ecology, 51, 142-151. Source: Polce et al. (2013) PLoS ONE, 8, e76308 ‘Causes’ – key messages

• Multiple anthropogenic drivers affect pollinators and pollination, and some of which may interact

• Drivers can have negative, but sometimes positive, effects on pollinators & pollination

• Often difficult to link drivers to declines over time; but can be inferred from short-term impact studies

• Considerable knowledge gaps remain about the effects of different drivers, their interplay, and relative importance ‘Consequences’ – key messages

Threats to pollinators risks: • Disrupting wild plant pollination • Altering wider ecological interactions & functions? • Reducing delivery of sustained crop pollination services • Impacts on crop production and stability of yield • Economic, social and health costs to humans Acknowledgements • The Chairs, authors, TSU & secretariat of the IPBES assessment • The authors of all the studies highlighted here • European Commission for this nascent pollinator initiative and hosting this workshop