Buzziness as usual? Questioning the global pollination crisis

doi:10.1016/j.tree.2005.04.026

Trends in Ecology & Evolution

Volume 20, Issue 7, July 2005, Pages 367-373

https://doi.org/10.1016/j.tree.2005.04.026 Get rights and content

Concerns have been raised that invertebrate pollinators of crops and wild plants are in decline as a result of modern agricultural practices, habitat degradation, and introduced pests and diseases. This has led to demands for a response by land managers, conservationists and political decision makers to the impending ‘global pollinator crisis’. In questioning this crisis, it becomes apparent that perceptions of a pollinator crisis are driven mainly by reported declines of crop-pollinating honeybees in North America, and bumblebees and butterflies in Europe, whereas native pollinator communities elsewhere show mixed responses to environmental change. Additionally, few staple food crops depend on pollinator services, and most crops that do are grown at small scales in diversified agro-ecosystems that are likely to support healthy pollinator communities, or in highly managed systems that are largely independent of wild pollinators. Consequently, justifying conservation action on the basis of deteriorating pollinator services might be misplaced. Nevertheless, existing initiatives to monitor pollinators are well founded, given the uncertainty about the dynamics of pollinator populations.

Section snippets

An unfolding crisis?

The spread of agriculture at the expense of natural vegetation has greatly reduced the local biodiversity of temperate regions 1, 2 and is doing so at unprecedented rates in the tropics [3]. This biodiversity crisis has been linked to the degradation of ecosystem services [4], such as nutrient cycling and water purification, which is touted as a major threat to the well being of economic systems and human welfare (4, 5). Pollination is generally presented as a crucial service in decline 6, 7, 8

Parameters of a pollinator-mediated food crisis

First, I consider the parameters of a pollinator-mediated food crisis. The loss of some pollinator species need not necessarily affect crop yields if crops are wind or self-pollinated, or if they are insured against specific losses by a diverse array of pollinator visitors. Crop productivity might also be limited by other considerations, such as nutrient or water availability. Thus, pollinator declines are only likely to cause an agricultural crisis for crops that are pollinator dependent,

Are pollinators declining?

The central assumption of the pollinator crisis is that pollinating species are declining. European honeybees (Figure 1a) in North America have suffered dramatic declines (up to 50% of managed colonies [23]) as a result of introduced parasitic mites and excessive pesticide use [24]. To a small extent, these losses are offset by the spread of Africanized honeybees that have greater resistance to mites, disease and certain pesticides [24]. Africanized honeybees have been successfully integrated

Thus, is there a problem?

The scientific information relating to pollinator services or declines must be evaluated critically before a crisis is declared lest we overplay our hand in demanding conservation action for the wrong reasons. It is possible that a global pollination crisis is, indeed, in progress, but I do not believe that evidence for such a crisis is currently strong. I suggest that the observed decline in managed honeybee colonies in the USA, and similar concerns about declining bumblebees in Europe, has

To bee or not to bee

In spite of some scepticism portrayed here about the reality of a global pollination crisis, environmental crises are, almost by definition, belatedly recognized. In view of this, some simple management recommendations could ensure that a pollinator crisis remains largely a myth.

Given that the heavy-dependence of modern agriculture on honeybees for pollination is at the heart of the pollination crisis 64, 65, diversifying the suite of crop-pollinating species has been proposed as an appropriate

Acknowledgements

I thank Dave Goulson for a pre-print of his paper and two photographs, and Timothy Spira for a copy of one of his papers. Saul Cunningham and Bill Kunin provided comments on the article, which also benefited from comments from four anonymous referees.

References (76)

I. Steffan-Dewenter et al.
Insect communities and biotic interactions on fragmented calcareous grasslands – a mini review
Biol. Conserv.
(2002)
A.J. Richards
Does low biodiversity resulting from modern agricultural practice affect crop pollination and yield?
Ann. Bot.
(2001)
C.L. Gross et al.
Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae)
Biol. Conserv.
(1998)
A. MacLeod
Attraction and retention of Episyrphus balteatus DeGeer (Diptera: Syrphidae) at an arable field margin with rich and poor floral resources
Agric. Ecosyst. Environ.
(1999)
J. Banaszak
Strategy for conservation of wild bees in an agricultural landscape
Agric. Ecosyst. Environ.
(1992)
D. Goulson
Causes of rarity in bumblebees
Biol. Conserv.
(2005)
R.L.H. Dennis et al.
Gains and losses of French butterflies: tests of predictions, under-recording and regional extinction from data in a new atlas
Biol. Conserv.
(2003)
R.L. Minckley
Spatial predictability and resource specialization of bees (Hymenoptera: Apoidea) at a superabundant, widespread resource
Biol. J. Linn. Soc.
(1999)
A.C. Weibull
Species richness in agroecosystems: the effect of landscape, habitat and farm management
Biodiv. Conserv.
(2003)
I.M. Turner
Species loss in fragments of tropical rain forest: a review of the evidence
J. Appl. Ecol.
(1996)

F.S. Chapin

Consequences of changing biodiversity

Nature

(2000)

G.C. Daily

Nature's Services: Societal Dependence on Natural Ecosystems

(1997)

G. Allen-Wardell

The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields

Conserv. Biol.

(1998)

G.C. Daily

Ecosystem Services: Benefits Supplied to Human Societies by Natural Ecosystems

(1997)

C.A. Kearns

Endangered mutualisms: the conservation of plant–pollinator interactions

Annu. Rev. Ecol. Syst.

(1998)

S. Buchmann et al.

The Forgotten Pollinators

(1996)

K.S. Delaplane et al.

Crop Pollination by Bees

(2000)

R.P. Macfarlane

Applied pollination in temperate areas

J. Banaszek

Strategy for conservation of wild bees in an agricultural landscape

Agr, Ecosyst. Environ.

(1992)

I.H. Williams

Aspects of bee diversity and crop pollination in the European Union

Ghazoul, J. Pollen and seed dispersal among dispersed plants. Biol. Rev. (in...

L.A. Turnbull

Are plant populations seed-limited? A review of seed sowing experiments

Oikos

(2000)

K.S. Bawa

Plant–pollinator interactions in tropical rain forests

Annu. Rev. Ecol. Syst.

(1990)

J. Ollerton et al.

Latitudinal trends in plant–pollinator interactions: are tropical plants more specialised?

Oikos

(2002)

N.M. Waser

Generalization in pollination systems, and why it matters

Ecology

(1996)

L. Ashworth

Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation?

J. Ecol.

(2004)

J. Bascompte

The nested assembly of plant–animal mutualistic networks

Proc. Natl. Acad. Sci. U. S. A.

(2003)

M.A. Aizen

Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter?

J. Veg. Sci.

(2002)

B. Kraus et al.

Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California

Environ. Entomol.

(1995)

S.S. Schneider

The African honey bee: factors contributing to a successful biological invasion

Annu. Rev. Entomol.

(2004)

E. Guzmannovoa et al.

The impact of Africanized bees on Mexican beekeeping

Am. Bee J.

(1994)

F. Ratnieks et al.

Agricultural impact of Africanized honey bees in Sinaloa, Mexico

Calif. Agri.

(1996)

M. Basualdo

Africanized honey bees (Hymenoptera: Apidae) have a greater fidelity to sunflowers than European bees

J. Econ. Entomol.

(2000)

D.W. Roubik

Pollination system stability in Tropical America

Conserv. Biol.

(2000)

T.P. Spira

Plant–pollinator interactions: a threatened mutualism with implications for the ecology and management of rare plants

Nat. Areas J.

(2001)

D.M. Caron

Africanized Honey Bees in the Americas

(2001)

R.A. Morse et al.

The value of honey bees as pollinators of U.S. crops in 2000

Bee Cult.

(2000)

C. Kremen

Crop pollination from native bees at risk from agricultural intensification

Proc. Natl. Acad. Sci. U. S. A.

(2002)

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View full text

Trends in Ecology & Evolution

Buzziness as usual? Questioning the global pollination crisis

Section snippets

An unfolding crisis?

Parameters of a pollinator-mediated food crisis

Are pollinators declining?

Thus, is there a problem?

To bee or not to bee

Acknowledgements

Biol. Conserv.

Ann. Bot.

Biol. Conserv.

Agric. Ecosyst. Environ.

Agric. Ecosyst. Environ.

Biol. Conserv.

Biol. Conserv.

Biol. J. Linn. Soc.

Species richness in agroecosystems: the effect of landscape, habitat and farm management

Biodiv. Conserv.

Species loss in fragments of tropical rain forest: a review of the evidence

J. Appl. Ecol.

Consequences of changing biodiversity

Nature

Nature's Services: Societal Dependence on Natural Ecosystems

The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields

Conserv. Biol.

Ecosystem Services: Benefits Supplied to Human Societies by Natural Ecosystems

Endangered mutualisms: the conservation of plant–pollinator interactions

Annu. Rev. Ecol. Syst.

The Forgotten Pollinators

Crop Pollination by Bees

Applied pollination in temperate areas

Strategy for conservation of wild bees in an agricultural landscape

Agr, Ecosyst. Environ.

Aspects of bee diversity and crop pollination in the European Union

Are plant populations seed-limited? A review of seed sowing experiments

Oikos

Plant–pollinator interactions in tropical rain forests

Annu. Rev. Ecol. Syst.

Latitudinal trends in plant–pollinator interactions: are tropical plants more specialised?

Oikos

Generalization in pollination systems, and why it matters

Ecology

Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation?

J. Ecol.

The nested assembly of plant–animal mutualistic networks

Proc. Natl. Acad. Sci. U. S. A.

Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter?

J. Veg. Sci.

Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California

Environ. Entomol.

The African honey bee: factors contributing to a successful biological invasion

Annu. Rev. Entomol.

The impact of Africanized bees on Mexican beekeeping

Am. Bee J.

Agricultural impact of Africanized honey bees in Sinaloa, Mexico

Calif. Agri.

Africanized honey bees (Hymenoptera: Apidae) have a greater fidelity to sunflowers than European bees

J. Econ. Entomol.

Pollination system stability in Tropical America

Conserv. Biol.

Plant–pollinator interactions: a threatened mutualism with implications for the ecology and management of rare plants

Nat. Areas J.

Africanized Honey Bees in the Americas

The value of honey bees as pollinators of U.S. crops in 2000

Bee Cult.

Crop pollination from native bees at risk from agricultural intensification

Proc. Natl. Acad. Sci. U. S. A.