Causes and consequences of pollinator declineEU Pollinator Initiative Workshop 15/03/2018

BELSPO (Belgian Science Policy Office), Avenue Louise 231, 1050 Brussels

Dr Adam VanbergenNERC Centre for Ecology & Hydrology (CEH)

EdinburghAJV@ceh.ac.uk

China

USAex-USSR Germany

Argentina Spain

• Land use change

• Land management (intensity, GMO etc.)

• Pesticides (insecticides, herbicides)

• Pollinator diseases & bee husbandry

• Climate change

• Invasive alien species

Drivers of change in pollinators

• Reduction in food, nesting or other resources

Loss of habitatFragmentationDegradation

• 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

Land-use change, pollinator networks & plant mating

Birch Woods

Ungrazed GrazedFlo

we

rin

g p

lan

t s

pe

cie

s r

ich

ne

ss

20

22

24

26

28

30

32

34

N= 10

N= 10

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

Floral Species Richness

4 6 8 10 12 14 16 18 20 22 24

Ne

two

rk C

on

nec

tan

ce

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8 AICc wi = 0.44

GRAZED n=5

UNGRAZED n=4

Standardised Connectance

0.2 0.4 0.6 0.8

Ou

tcro

ssin

g r

ate

(t m

)

0.4

0.5

0.6

0.7

0.8

0.9

1.0 AICc wi = 0.88= fully outcrossed

• Loss of non-cultivated habitat patches

• Large field sizes and monocultures

• High inputs of fertilizers, pesticides, herbicides etc.

• Intensive grazing

Intensive agriculture

• 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

Pesticides

Neonicotinoid use & pollinator decline: a 17 year correlation

Other pesticides (ns)

Oilseed rape cover (+ve)

Neonicotinoid use (-ve)

Volunteer surveys of

bees

BWARSBees, Wasps & AntsRecording Society

-18%

Red = Actual trend;

Blue = Estimated trend if NNI

were benign

Pro

bab

ility

Non-foragersOSR Foragers

Negative Positive

Bees feeding on rape

negatively affected

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

interacting factors

Bee diet: Worse where

oilseed rape forms

much of diet

Bee health: Worse

where bees have high

disease load

• Negative & positive effects

on honeybee colony health

• Negative effects on

reproduction of wild bee

species (B. terrestris, O.

bicornis)

• More persistent in

soil than expected

Image cred

it: Bayer

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

0

100

200

300

400

500

600

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0 1 2 3 4 5 6 7 8 9

GermanyHungaryUK

Neonicotinoid residues found in nests (ng g-1)

New

qu

een

s

Deformed Wing Viruselectron density image Source: Pavel Plevak

Asian hornet (Vespa velutina) eating a honeybee. Source Alain C.

Varroa mite (Varroa destructor) on a honeybee. Source: Rob Paxton

Nosemaceranaea fungal parasite of honeybees Source: IngemarFries

Pests & pathogens

Bee trade, pests and pathogens

Ryabov et al. 2014. PLoS Pathog 10Wilfert et al 2016. Science 351Martin et al 2012. Science 336Szabo et al 2012.Conservation Letters 5Furst et al 2014. Nature 506McMahon et al . 2015. JAE 84Moritz et al 2005. Ecoscience 12Vanbergen et al. 2018, Nature Ecology & Evolution 2

• 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

Climate Change

Jeremy T. Kerr et al. Science 2015;349:177-180

Invasive alien species

• Identity and evolutionary history of the

invader & recipient ecosystem matters…

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

Asian hornet (Vespa velutina) and honeybee

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

• More than 75% of leading food crops

• Almost 90% of the world’s flowering plants

Rely, at least in part, on animal pollination

Risks of pollinator decline

Status of insect-pollinated wild plants

• Insect pollinator

dependence correlated

with plant decline

• Threatened plants

dependent on pollinators

declined >4x rate of

species not dependent

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

t = 3.53, d.f= 48.63 P<0.001

Non-conservation status plant species

Conservation status plant species

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

• Insect pollinator

dependence correlated

with plant decline

• Threatened plants

dependent on pollinators

declined >4x rate of

species not dependent

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

t = 3.53, d.f= 48.63 P<0.001

Non-conservation status plant species

Conservation status plant species

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.

What are the consequences for the organisms, above and belowground,

linked to declining pollinator-dependent plants?

Is pollination a keystone interaction?

Crop pollination services• Wild insect visitation enhances crop production & stability• Honey bee visitation has weaker effect, which supplements, but does

not replace, the pollination service by wild insects

Garibaldi et al. Science 2013 339:1608-1611

Rader et al. (2015) PNAS.

Pollinators increase crop yields

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 services

Rader et al. PNAS 2015 doi/10.1073/pnas.1517092112

• Diversity and identity of pollinators varies between crops • Species pool varies for a given crop across geographic

regions

Crop pollination: diversity matters

Potential crop pollination deficits?

-0.25 - -0.125

-0.125 - 0

0 - 0.125

0.125 - 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

• Bee species richness or functional diversity • Modelled from species occurrence records• Related to agricultural statistics (e.g. crop cover)

‘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

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

‘Consequences’ – key messages

• 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

Acknowledgements