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Cite this article
* Klein Alexandra-Maria
,
* Vaissière Bernard E
,
* Cane James H
,
* Steffan-Dewenter Ingolf
,
* Cunningham Saul A
,
* Kremen Claire
and
* Tscharntke Teja
2007Importance of pollinators in changing landscapes for world cropsProc. R.
Soc. B.274303–313http://doi.org/10.1098/rspb.2006.3721
SECTION
* Abstract
* 1. Introduction
* 2. Material and methods
* 3. Results and discussion
* 4. Management conclusions and future directions
* Footnotes
Supplemental Material
You have access
IMPORTANCE OF POLLINATORS IN CHANGING LANDSCAPES FOR WORLD CROPS
Alexandra-Maria Klein
Alexandra-Maria Klein
Agroecology, University of GöttingenWaldweg 26, 37073 Göttingen, Germany
aklein2@gwdg.de
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Bernard E Vaissière
Bernard E Vaissière
Institut National de la Recherche Agronomique, Laboratoire de Pollinisation
Entomophile, UMR 406 INRA-UAPV Ecologie des Invertébrés84914 Avignon Cedex 9,
France
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James H Cane
James H Cane
USDA-ARS Bee Biology and Systematics Laboratory, Utah State UniversityLogan, UT
84322, USA
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Ingolf Steffan-Dewenter
Ingolf Steffan-Dewenter
Agroecology, University of GöttingenWaldweg 26, 37073 Göttingen, Germany
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Saul A Cunningham
Saul A Cunningham
CSIRO EntomologyBox 1700 Canberra, Australian Capital Territory 2601, Australia
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Claire Kremen
Claire Kremen
Department of Environmental Science, Policy and Management, University of
California137 Mulford Hall no. 3114, Berkeley, CA 94720, USA
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Teja Tscharntke
Teja Tscharntke
Agroecology, University of GöttingenWaldweg 26, 37073 Göttingen, Germany
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Alexandra-Maria Klein
Alexandra-Maria Klein
Agroecology, University of GöttingenWaldweg 26, 37073 Göttingen, Germany
aklein2@gwdg.de
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Bernard E Vaissière
Bernard E Vaissière
Institut National de la Recherche Agronomique, Laboratoire de Pollinisation
Entomophile, UMR 406 INRA-UAPV Ecologie des Invertébrés84914 Avignon Cedex 9,
France
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James H Cane
James H Cane
USDA-ARS Bee Biology and Systematics Laboratory, Utah State UniversityLogan, UT
84322, USA
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Ingolf Steffan-Dewenter
Ingolf Steffan-Dewenter
Agroecology, University of GöttingenWaldweg 26, 37073 Göttingen, Germany
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Saul A Cunningham
Saul A Cunningham
CSIRO EntomologyBox 1700 Canberra, Australian Capital Territory 2601, Australia
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Claire Kremen
Claire Kremen
Department of Environmental Science, Policy and Management, University of
California137 Mulford Hall no. 3114, Berkeley, CA 94720, USA
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Teja Tscharntke
Teja Tscharntke
Agroecology, University of GöttingenWaldweg 26, 37073 Göttingen, Germany
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Published:27 October 2006https://doi.org/10.1098/rspb.2006.3721
ABSTRACT
The extent of our reliance on animal pollination for world crop production for
human food has not previously been evaluated and the previous estimates for
countries or continents have seldom used primary data. In this review, we expand
the previous estimates using novel primary data from 200 countries and found
that fruit, vegetable or seed production from 87 of the leading global food
crops is dependent upon animal pollination, while 28 crops do not rely upon
animal pollination. However, global production volumes give a contrasting
perspective, since 60% of global production comes from crops that do not depend
on animal pollination, 35% from crops that depend on pollinators, and 5% are
unevaluated. Using all crops traded on the world market and setting aside crops
that are solely passively self-pollinated, wind-pollinated or parthenocarpic, we
then evaluated the level of dependence on animal-mediated pollination for crops
that are directly consumed by humans. We found that pollinators are essential
for 13 crops, production is highly pollinator dependent for 30, moderately for
27, slightly for 21, unimportant for 7, and is of unknown significance for the
remaining 9. We further evaluated whether local and landscape-wide management
for natural pollination services could help to sustain crop diversity and
production. Case studies for nine crops on four continents revealed that
agricultural intensification jeopardizes wild bee communities and their
stabilizing effect on pollination services at the landscape scale.
1. INTRODUCTION
Ecosystem services, defined as the benefits to human welfare provided by
organisms interacting in ecosystems, are considered to be at risk (Daily 1997;
Palmer et al. 2004). Pollination by wild animals is a key ecosystem service.
Although crop pollination is commonly cited as an example of an endangered
ecosystem service (Corbet 1991; Williams 1994; Ingram et al. 1996; Matheson et
al. 1996; Allen-Wardell et al. 1998; Kearns et al. 1998; Kevan & Phillips 2001;
Steffan-Dewenter et al. 2005, but see Ghazoul 2005), detailed studies of the
crop pollination systems are incomplete or out of date. Animal pollination is
important to the sexual reproduction of many crops (McGregor 1976; Crane &
Walker 1984; Free 1993; Williams 1994; Nabhan & Buchmann 1997; Westerkamp &
Gottsberger 2000) and the majority of wild plants (Burd 1994; Kearns et al.
1998; Larson & Barrett 2000; Ashman et al. 2004), which can also be important
for providing calories and micronutrients for humans (Sundriyal & Sundriyal
2004). Furthermore, the decline of pollinating species can lead to a parallel
decline of plant species (Biesmeijer et al. 2006).
For tropical crops, Roubik (1995) provided a detailed list for 1330 species and
compiled a list of potential breeding systems and pollinating taxa. From this
list, ca 70% of tropical crops seem to have at least one variety for which
production is improved by animal pollination.
For European crops, Williams (1994) assessed the pollinator needs for 264 crop
species and concluded that the production of 84% of these depends at least to
some extent upon animal pollination. Previous estimates have used mostly
secondary data and relied on crude guesses of the proportional contribution of
pollinators to crop production. These rough estimates can be deceptive as they
often neither consider variation in the level of dependence on animal
pollination nor take into account the importance of the crop to consumers. The
major caloric inputs in the human diet come from a few staple foods with large
world production for which animal pollination is irrelevant (Richards 2001;
Ghazoul 2005), or come indirectly via animals fed with these same staple crops.
Some authors provide coefficients of dependence on animal-mediated pollination
for several crops (Borneck & Merle 1989; Robinson et al. 1989a,b; Morse &
Calderone 2000), but despite their continuing acceptance, most of these reports
do not cite data sources, and so it is impossible to assess the reported level
of dependence. Williams (1994) provided coefficients for the dependence of
European crops on animal pollination and estimated the proportion of insect
pollinators that are honeybees, using information from Crane & Walker (1984) and
Free (1993). Both studies are less relevant today, because many new crop
varieties and pollination studies are available. To adequately evaluate the
importance of animal pollination for plant products in our food supply, and for
economic analyses of crop pollination by animals, we need a global review of
crops considering their breeding systems, their flower-visiting fauna and the
level of production increase resulting from animal visitation and pollination,
as supported by experimental evidence (Kevan & Phillips 2001).
Honeybees, mainly Apis mellifera, remain the most economically valuable
pollinators of crop monocultures worldwide (McGregor 1976; Watanabe 1994; also
shown for several single crops, e.g. Roubik 2002 for coffee in Panama) and
yields of some fruit, seed and nut crops decrease by more than 90% without these
pollinators (Southwick & Southwick 1992). When wild bees do not visit
agricultural fields, managed honeybee hives are often the only solution for
farmers to ensure crop pollination. Compared with the management of several wild
bees, honeybees are versatile, cheap and convenient, but for some crops they are
not the most effective pollinators on a per flower basis (reviewed in Parker et
al. (1987), Torchio (1990), Richards (1996), Cane (1997a) and Westerkamp &
Gottsberger (2000); see also Bosch & Blas (1994) for almond; Cane (1997b) and
Javorek et al. (2002) for blueberry; Kremen et al. (2002, 2004) for watermelon;
Klein et al. (2003a,b) for highland and lowland coffee; Cane (2005) for
raspberry and blackberry; Greenleaf & Kremen (in press) for field tomatoes;
Bosch et al. (2006) for cherry). Other crops await similar comparative
pollinator study. The numbers of managed honeybee colonies are declining in some
parts of the world (Williams et al. 1991; Matheson et al. 1996; Delaplane &
Mayer 2000; Anonymous 2005) largely owing to: (i) the spread of pests like
parasitic mites (Varroa jacobsoni, V. destructor and Acarapis woodi; Downey &
Winston 2001; Chen et al. 2004), the small hive beetle (Aethina tumida; Evans et
al. 2003) and the microsporidian parasite Nosema ceranae (Higes et al. 2006),
(ii) improper pesticide and herbicide use (Ingram et al. 1996), (iii) ageing of
the beekeeper population in Europe and North America, and (iv) lower market
prices for their products and services. Indeed, declining honeybee availability
led to recent concern over pollination shortfalls such as those seen for almonds
in California (www.almondboard.com). This situation also highlights the
potential risk of our sole reliance on honeybees for agricultural pollination.
Fragmentation and degradation of near- and semi-natural habitats can be
detrimental to bee communities (Rathcke & Jules 1994; Kremen et al. 2002, 2004;
Steffan-Dewenter et al. 2002, 2006; Larsen et al. 2005; Cane et al. 2006). The
main causal factor is loss or dissociation of important resources for food and
nesting (Hines & Hendrix 2005; Potts et al. 2005). Conservation of natural- and
semi-natural habitats in agricultural landscapes to increase and protect bee's
resources may be useful to improve pollination services. While landscape effects
are known to affect communities of herbivorous and predatory/parasitic insects
in agro-ecosystems (reviewed in Cronin & Reeve 2005; Tscharntke et al. 2005;
Bianchi et al. 2006), a similar evaluation of landscape impact on crop
pollination is lacking.
In this review, we summarize and evaluate information on three issues:
i. the identification of leading global crops that depend on animal
pollination for their production and their level of dependence on
pollinators,
ii. the influence of land-use changes at both local and landscape scales for
pollinator communities and their services, and
iii. future options for landscape and agricultural management to enhance wild
pollinators and ensure pollination services for crop production.
2. MATERIAL AND METHODS
We first estimated the proportion of crop production depending on animal
pollination. We selected the leading global crops on the world market out of the
FAO crop production list for the year 2004 (FAOSTAT 2005), such that the
aggregate represented 99% of total global food production (figure 1). We chose
single crops and commodities used for human food with an annual production of at
least 4 000 000 Metric tonnes (Mt). Production values are listed individually
for the single crops. Production of the commodity crops is pooled in not
elsewhere specified (NES) commodities. A commodity is an aggregation of
different crops (e.g. fresh vegetables NES includes 21 crops). Commodity
compilation is based on a questionnaire that countries fill out to include
important crops for the world market which are not listed as a single crop by
the FAO. Fifty-seven leading single crops and five commodities (including 67
commodity crops) represented 99% (94.5 and 4.5%, respectively) of the total
global food production.
Figure 1 Crop selection pathway to estimate the annual world production that is
influenced by animal pollination (electronic supplementary material 1; lower
left side) and to evaluate the levels of dependence on animal pollination for
crops important in the global market (electronic supplementary material 2; right
side). Single crops are crops directly listed with their production by the FAO
and commodity crops are combined to a commodity with an aggregated production
value.
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Although production quantities for each commodity group are known, there is no
breakdown for each commodity crop within these five groups, so we classified the
annual production of the commodities with respect to its pollinator dependence
as ‘unknown’. We individually classified each of the resulting 124 crops (57
leading single and 67 leading commodity crops) into four categories of
pollinator dependence:
i. production increase with pollinators for plant parts that we consume (we
define production as increased fruit set, fruit weight and/or quality, and
seed number and/or quality, when pollinators have access to the flowers in
contrast to pollinator exclusion experiments),
ii. increase in seed production with pollinators to produce the vegetative
parts that we consume,
iii. increase in seed production with pollinators for breeding alone, as the
plants reproduce vegetatively and we consume the vegetative parts, and
iv. no production increase with pollinators.
We next assessed the level to which animal pollination matters to global crops
directly used by humans. For this approach, we expanded our list using all the
crops listed to be important on the world market, not restricted to the leading
crops, as was the case for electronic supplementary material 1. We started with
the same list used for electronic supplementary material 1, the complete set of
137 single crops and 5 commodities (93 commodity crops) listed by the FAO for
the year 2004. We then reduced this list to 74 single crops and 33 commodity
crops, a total of 107, following the pathway illustrated in figure 1.
Free (1993) summarized the key references for pollination requirements for 75
out of the 107 crops. We extended and updated his review, including both more
recent literature and earlier studies not cited in Free (1993). For each listed
crop, we provide the following information:
i. Flower morphology and breeding system.
ii. Capacity of the crop to produce fruit and/or seeds without pollinators.
iii. Animal groups or species known to be important flower visitors or
pollinators; the primary pollinating species are identified if there is a
species for which at least 80% of their single flower visits result in a
fruit (Klein et al. 2003a,b) or species that improve fruit and seed
quality and quantity when abundant as compared with the level when all
flower visitors are excluded.
iv. Magnitude of the improvement in production and quality when pollinated by
animals. We scored the degree of production dependence into five classes:
(i) essential (production reduction by 90% or more without flower
visitors), meaning that production requires animal pollination, (ii) high
(40 to less than 90% reduction), (iii) modest (10 to less than 40%), (iv)
little (greater than 0 to less than 10%), (v) no reduction, and (vi)
unknown, meaning that no literature was available to adequately review the
breeding systems or draw conclusions about pollinator dependence.
3. RESULTS AND DISCUSSION
(A) IMPORTANCE OF ANIMAL POLLINATION FOR GLOBAL CROP PRODUCTION
Production of 39 of the leading 57 single crops increases with pollinating
animals (figure 2). In aggregate, these crops account for 35% (23×108 Mt) of
global food production (figure 2), but because most of these crops are not
entirely dependent on animal pollination, the amount of production directly
attributable to animals is lower than this value. In addition, production of 48
of the 67 crops of the five leading global commodities increases with
pollinating animals (figure 1). Only insects are demonstrated pollinators of the
single crops, while vertebrates pollinate very few commodity crops (e.g. feijoa
is pollinated by birds and durian seems to be pollinated by bats, electronic
supplementary material 2). Among the 57 single crops that show increased
production, 26 (55% with 12×108 Mt or 19% of global food) increase seed
production with animal pollination to produce vegetative parts for human food,
while an additional seven crops (8×108 Mt, 36%) show increased seed production
for breeding alone, as the plants reproduce vegetatively and only vegetative
parts are consumed (e.g. potatoes, sweet potatoes and manioc, electronic
supplementary material 1). The production increase with pollinators for seeds of
vegetatively propagated crops permits breeding progress and hybridization for
the development of new varieties.
Figure 2 Relative importance of animal pollination for the leading global crops
and commodities used for human food and selected by their annual production in
2004. We considered crops and commodities with an annual production greater than
4 000 000 Metric tonnes (Mt) as these comprise 99% of the 2004 total crop
production listed for human food. The number of crops and the production are
listed according to their production increase with pollinators (see electronic
supplementary material 1 for details). Single crops and commodity crops in NES*
commodities are separated. The category ‘unknown’ includes only commodity crops
for the number of crops while the ‘unknown’ production is the production of the
leading commodities, as the production value of each commodity crop is not
known. Crops in the ‘increase’ category could be classified into three
sub-categories with the following number of species and total production figure
for the individual crops: production increase with pollinators for plant parts
that we consume (fruits and/or seeds: 26 crops with 12 108 Mt=55%); increase in
seed production with pollinators to produce the vegetative parts that we consume
(six crops with 2108 Mt=9%); and increase in seed production with animals for
breeding alone, as the plants reproduce vegetatively and we consume the
vegetative parts (seven crops with 8108 Mt=36%). NES* is an abbreviation for not
elsewhere specified; leading commodities are fresh vegetables NES, fresh fruits
NES, fresh tropical fruits NES, roots and tubers NES and pulses NES. Commodity
crops are included based on a questionnaire that countries fill out to include
important crops for the world market which are not listed as single crops.
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Animal pollination is irrelevant to 18 of the leading single crops (comprising
60% or 39×108 Mt of the world production) and 10 of the leading commodity crops.
These are wind- or passively self-pollinated grasses (cereals and sugarcane),
dominating the leading global crop list (electronic supplementary material 1;
figure 2).
Twenty per cent of the overall crop production comes from crops that increase
fruit and vegetable production with animal pollination, and ca 15% comes from
crops that increase seed production with animal pollination. Our results further
show that a majority of global crops could experience production loss owing to
pollinator limitation (39 single crops increase fruit, vegetable or seed
production with pollinators compared with 18 that do not, and 87 of the
commodity crops increase production compared with 28 that do not; figure 2).
Included are many fruit crops that provide essential macro- and micronutrients
contributing to a healthy diet. These results support the contention of Richards
(2001) and Ghazoul (2005) that primary food production, and especially our
staple foods, is independent of insect pollination. Thinking beyond caloric
intake, however, our results support the opinion of Steffan-Dewenter et al.
(2005) that our diet would be greatly impoverished, both nutritionally and
culturally, if pollination services further decline.
In a second list (electronic supplementary material 2), we quantified the level
of dependence on animal pollination. We found empirical evidence for increased
production with pollinators in 92 out of 108 selected crops (figure 3). Among
these 92 crops, for the majority (82 crops), data were available from
experiments comparing measures of pollination (e.g. fruit set, number of seeds,
fruit or seed weight, or pollen deposition) at the level of flowers,
inflorescences or whole plants, with and without access to pollinators. For 10
crops, we classified the evidence for increased production with pollinators as
‘indirect evidence’, because experiments with pollinator exclusion were lacking,
but the experiments demonstrated, for example, self-incompatibility and a need
for cross pollination that could not be achieved by wind (electronic
supplementary material 2; figure 3). Animal pollination was found to be
essential for most varieties of the following 13 crops: atemoya, Brazil nut,
cantaloupe, cocoa, kiwi, macadamia nut, passion fruit, pawpaw (Indian banana),
rowanbarry, sapodilla, squashes and pumpkins, vanilla and watermelon. An
additional 30 crops showed increased fruit and/or seed production for most
species and varieties with animal pollination. Twenty-seven crops show a modest
increase in production, and for 21 crops, production of some species or
varieties increase little, others not at all. For seven crops, production did
not increase in the studies available: chick pea, garden and field peas and
lentil, which are passively self-pollinated, and olive, pepper, quinoa and
grapes, which rely on passive self- and wind-pollination. Pollination needs of
nine crops remain unknown (figure 3; electronic supplementary material 2).
Figure 3 Level of dependence on animal-mediated pollination. The selected crops
are those included directly in the production list published by the FAO for 2004
(FAOSTAT 2005). We further included commodity crops for which the production was
pooled in commodities with an annual 2004 commodity production greater than
4 000 000 Metric tonnes (Mt). Only crops that produce fruits or seeds for direct
human use as food were considered. We did not include: (i) crops for which seeds
are only used for breeding or to grow vegetable parts for direct human use or
for forage, and (ii) crops known to be only wind-pollinated, passively
self-pollinated or reproduced vegetatively. Essential, pollinators essential for
most varieties (production reduction by 90% more, comparing experiments with and
without animal pollinators); high, animal pollinators are extreme (40 to less
than 90% reduction); modest, animal pollinators are clearly beneficial (10 to
less than 40% reduction); little, some evidence suggests that animal pollinators
are beneficial (greater than 0 to less than 10% reduction); no increase, no
production increase with animal-mediated pollination; unknown, empirical studies
are missing.
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Gaps in our knowledge of pollination requirements are illustrated by the example
of highland coffee, one of the better studied crops. Although the breeding
systems are well studied and pollinators have been identified in different
coffee production regions, few varieties have been studied, and production of
some varieties may not increase with animal pollination as much as those studied
to date (A.-M. Klein, unpublished data). The need to consider different genetic
materials is also highlighted by the fact that varieties of many crops, such as
citrus, blueberries, most stone fruit crops, and almonds, show great production
variation with animal pollination (see Ortega et al. 2002 for almond). We also
do not know much about the mechanisms of pollination provided by most pollinator
species (Klein et al. 2003a), and flower-visiting insect communities of
different production regions across the world can differ greatly. For example,
the flower visitors to coffee in Ecuador with more than 95% social and less than
5% solitary bees (Veddeler et al. 2006) are very different from flower-visiting
communities in Indonesia with 70% social and ca 30% solitary bees (Klein et al.
2003a,b). Such differences may lead to differences in pollination success.
(B) CONSEQUENCES OF AGRICULTURAL MANAGEMENT AT LOCAL AND LANDSCAPE SCALES FOR
WILD VERSUS MANAGED POLLINATORS
Wild bees and other insects can pollinate many crops, but their value for crop
pollination has been overlooked for centuries. As their services are
increasingly being recognized for agriculture (e.g. O'Toole 1993; Cane 1997b;
Kevan & Phillips 2001; Klein et al. 2003a; Slaa et al. 2006), the adequate
management of local agro-ecosystems and the conservation of suitable natural or
semi-natural pollinator habitats in the surrounding landscapes are receiving
more attention. Little information exists on the ways in which local management
influences agricultural pollination (Richards 2001). Considering the 107 crops
listed in electronic supplementary material 2, we found increased production
with animal pollination of at least 10% or higher (categories essential, great
and modest) for 63 crops, when considering only the crops for which field
experiments were available (N=93). Therefore, we suggest that pollination of at
least these 63 crops should be vulnerable to agricultural intensification that
may reduce the diversity and abundance of pollinators (e.g. Kremen et al. 2002;
Klein et al. 2003a,b). Among the 63 crops, the production of 13 crops that are
entirely dependent on pollinators to set fruits might be severely impacted by
pollinator loss through agricultural intensification. This risk is the greatest
for crops that rely on a narrow range of pollinating species, such as passion
fruit and vanilla.
We found 16 studies on the effects of agricultural intensification on
pollination at local or landscape scale of nine crops on four continents (table
1). All of these studies show negative consequences of local and/or regional
agricultural intensification for pollination. For watermelon and coffee, higher
variation in pollination success was found in sites of intensified agriculture
isolated from natural or semi-natural habitats (Kremen et al. 2004;
Steffan-Dewenter et al. 2006).
TABLE 1
Pollinator and pollination limitation in crop plants in response to land-use and
landscape changes. (Significance *p<0.05; **p<0.01; ***p<0.001.)
View inlineView popup
Table 1Pollinator and pollination limitation in crop plants in response to
land-use and landscape changes. (Significance *p<0.05; **p<0.01; ***p<0.001.)
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species name (common crop name)land-use and landscape variablepollination
variable and significance level of reductionreferenceAnnona squamosa × A.
cherimola (sugar apple)comparison of sites near and far from forest
fragmentspollinator diversity*** (fruit set reduction with pollinator
exclusion***)Blanche & Cunningham (2005)Brassica napus and B. rapa (turnip rape,
canola and oilseed rape)comparison of organic, conventional and genetically
modified (GM) fieldsnumber of seeds per silique from a flower sample***Morandin
& Winston (2005)proportional area of uncultivated land around fields within a
750 m radiusnumber of seeds per silique from a flower sample*Morandin & Winston
(2006)Citrullus lanatus (watermelon)comparison of organic versus conventional
fieldsnumber of pollen grains/stigma, n.s.Kremen et al. (2002, 2004)proportional
area of oak woodland and chaparral habitatnumber of pollen
grains/stigma***Kremen et al. (2002, 2004)Citrus paradisi (grapefruit)distance
from forestnumber of pollen grains/stigma* number of pollen tubes/stigma*Chacoff
(2006) and Chacoff & Aizen (2006)Coffea arabica (coffee)coffee plants near,
intermediate and far from forest fragmentsnumber of pollen grains/stigma***,
fruit set*, seed mass**Ricketts (2004) and Ricketts et al. (2004)distance from
forestfruit set**Klein et al. (2003a)plant diversityfruit set**Klein et al.
(2003a)coffee monocultures versus agroforestryfruit set*De Marco & Coelho
(2004)comparison sites near and far from forest fragmentsfruit set*De Marco &
Coelho (2004)Coffea canephora (coffee)distance from forestfruit set**Klein et
al. (2003b)Dimocarpus longan (longan fruit)comparison sites near and far from
forest fragmentsnumber of fruits per centimetre panicle*Blanche et al. (in
press)Helianthus annuus (sunflower)proportional area of natural habitatwild bee
diversity and abundance*** (estimated increase in seed set via single visit
studies)Greenleaf & Kremen (2006)organic versus conventional farm managementwild
bee diversity and abundance, n.s.Greenleaf & Kremen (2006)Lycopersicon
esculentum (tomato)distance to natural habitatBombus vosnesenskii abundance***;
Anthophora urbana abundance, n.s. (fruit set and fruit weight reduction with
pollinator exclusion for variety with exserted stigma)Greenleaf & Kremen (in
press)Macadamia integrifolia (macadamia nut)percentage of eucalyptus forest
surrounding orchardsTrigona abundance (seed set reduction with pollinator
exclusion* and only Trigona pollinated*)Heard (1994) and Heard & Exley
(1994)comparison of sites near and far from forest fragmentsnumber of
fruits/raceme*Blanche et al. (in press)
The existing studies suggest that crops having a production increase with
pollinators of at least 10% might show reduced fruit set and increased variance
in fruit set at locations increasingly isolated from near-natural habitats
(figure 4). The impact of landscape context on visitation rates and fruit set of
crops has been assessed as the proportion of near-natural habitats in the
surrounding landscape (e.g. Kremen et al. 2004; Morandin & Winston 2006) or as
the linear isolation distance from near-natural habitat (e.g. Klein et al.
2003a,b; Chacoff & Aizen 2006). We found a linear positive relationship between
fruit set stability and isolation to the rainforest margin for lowland and
highland coffee (Klein et al. 2003a,b), whereas a log-linear relationship was
found for watermelons (Kremen et al. 2004). Agro-ecosystems with more
semi-natural habitats are often more pollinator-species rich (Steffan-Dewenter
et al. 2002; Kremen & Chaplin 2006; Steffan-Dewenter et al. 2006). There might
be a threshold level of diversity necessary to maintain lower variation or
higher stability in pollination. The exact shape of the function will depend on
the biology of crop, crop variety, pattern of the landscape and regional
pollinator community, but the available data indicate that pollination stability
will increase in landscapes with a diverse and abundant pollinator community.
The positive pollination effect on crop yield can however be reduced or hidden
when other factors affecting crop yield, such as soil nutrients, micro-climate,
water, pest or disease status are suboptimal. Further, agricultural land use is
not always expected to reduce pollination services. Some wild bees may benefit
from agriculture, such as ground-nesting bees that use disturbed areas for
nesting, or pollinators may benefit from pollen-rich crop fields, such as
oilseed rape (Westphal et al. 2003), or from ecosystems in which agricultural
areas provide a greater diversity, continuity or abundance of floral resources
than original habitat types (e.g. Winfree et al. in press). Therefore, knowledge
of the pollinator's resources and life-history traits is required to correctly
predict the likely pollination responses (Cane et al. 2006). Failure of wild
pollinators can be overcome by the provision of commercially managed bees, where
they are effective and manageable pollinators available (Kremen et al. 2002),
but this service generally comes at a cost. Finally, crops with little or no
dependence on animal pollination will exhibit no relationship between
pollination rates and isolation (figure 4).
Figure 4 Expected relationship between the loss of animal-mediated crop
pollination function (pollination variable usually measured as fruit or seed set
in pollination studies and the variation usually measured as the coefficient of
variation in the number or yield of fruits indicating crop production stability)
and the effect of isolation from near-natural habitats (which means the area and
distance of the main nesting and foraging habitats for the pollinators).
Expected relationships in the absence of pollinator introduction are given for
crops which are independent of animal pollination and for crops depending on
animal pollination. Mean, solid line; variation, dashed line.
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Unfortunately, none of the landscape studies have been conducted over enough
years to reliably estimate temporal variability in pollination. In some studies,
samples were taken in two consecutive seasons (Kremen et al. 2002, 2004;
Ricketts 2004; Ricketts et al. 2004), but a majority were carried out over only
one season.
Studies that compare fruit or seed set of flowers in treatments with and without
access by wild-pollinating species or with additional hand-pollination provide
important data to identify key pollinating species (Canto-Aguilar & Parra-Tabla
2000; Javorek et al. 2002; Cane & Schiffhauer 2003; Klein et al. 2003a,b;
Greenleaf & Kremen 2006, in press; Blanche et al. in press), but few such
studies are yet available. In spite of this information shortage, many reviews
mention the neglected potential of wild bee species for crop pollination
(O'Toole 1993; Corbet 1996; Williams 1996; Westerkamp & Gottsberger 2000;
Goulson 2003). Buchmann & Nabhan (1996) suggested that ca 80% of the 100 most
important staple crops (Prescott-Allen & Prescott-Allen 1990) are pollinated by
wild insects. We found evidence for only 24 out of the 57 leading crops (42%)
being pollinated by at least one wild bee species. We identified 57 species
(mainly bees and only two vertebrate species) as not only flower visitors, but
also true pollinators for the 107 global crops for direct human use (electronic
supplementary material 2; table 2). Considering these 107 crops, empirical
evidence with direct testing revealed that both honeybees (which can be managed
or feral) and wild pollinators are valuable pollinators for 35 crops. For 12
crops, empirical studies provided evidence only for honeybees contributing to
successful pollination, with wild pollinators mentioned as pollinators for 10 of
these 12 crops, but without empirical data. For those cases where there was
evidence for honeybees but not wild bees, the problem was generally a shortage
of evidence, rather than evidence that wild bees were in fact poor pollinators.
For nine crops, empirical studies showed evidence that wild pollinators
contributed to successful pollination without similar evidence for honeybees,
and for six (atemoya, cocoa, fig, passion fruit, oil palm and sapodilla) of
these nine crops honeybees were not mentioned as pollinators. These nine crops
depend strictly on, or production increased greatly with, wild pollinators, and
interestingly, three of these crops—atemoya, passion fruit and vanilla—are
produced by hand-pollination in many parts of the world, showing the severe lack
of wild pollinators.
TABLE 2
Species list of known pollinators for global crops that are grown for direct
human consumption.
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Table 2Species list of known pollinators for global crops that are grown for
direct human consumption.
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pollinator groupspecieshoney beesApis cerana Fabr., A. dorsata Fabr., A. florea
Fabr. and A. mellifera L.stingless beesMelipona favosa Fabr., M. subnitida
Ducke, M. quadrifasciata Lepeletier, Nanotrigona perilampoides Cresson, N.
testaceicornis Lepeletier, Trigona cupira Sm., T. iridipennis Smith, T.
(Lepidotrigona) terminata Smith, T. (Tetragonoula) minangkabau Sakagami, T.
toracica Smith and Scaptotrigona depilis Mourebumble beesBombus affinis Cresson,
B. californicus F. Smith, B. hortorum L., B. hypnorum L., B. impatiens Cresson,
B. lapidarius L., B. (Thoracobombus) pascuorum Scop., B. sonorus L., B.
terrestris L. and B. vosnesenskii Radoszkowskisolitary beesAmegilla chlorocyanea
Cockerell, A. (Zonamegilla) holmesi Rayment, Andrena ilerda Cam., Anthophora
pilipes Fabr., Centris tarsata Smith, Creightonella frontalis Fabr., Habropoda
laboriosa Fabr., Halictus tripartitus Cockerell, Megachile (Delomegachile)
addenda Cresson, M. rotundata Fabr., Osmia aglaia Sandhouse, O. cornifrons
Radoszkowski, O. cornuta Latreille, O. lignaria lignaria Say, O. lignaria
propinqua Cresson, O. ribifloris Cockerell, Peponapis limitaris Cockerell, P.
pruinosa Say, Pithitis smaragdula Fabr., Xylocopa (Zonohirsuta) dejeanii
Lepeletier, Xylocopa frontalis Oliver and Xylocopa suspecta
MourewaspsBlastophaga psenes L.hover flies and other fliesEristalis cerealis
Fabr., E. tenax L. and Trichometallea pollinosa TownsendbeetlesCarpophilus
hemipterus L. and Carpophilus mutilatus ErichsonthripsThrips hawaiiensis Morgan
and Haplothrips (Haplothrips) tenuipennis BagnallbirdsTurdus merula L. and
Acridotheres tristis L.
In most environments, both wild pollinators and honeybees will exploit flowers
of crop species. For example, males of wild bees searching for mates disturbed
honeybees during foraging, so that honeybees switched more often between lines
of hybrid sunflower, and carried more pollen, thereby increasing the overall
pollination service (Degrandi-Hoffmann & Watkins 2000; Greenleaf & Kremen 2006).
Strawberry flowers visited by both wild and honeybees are more likely to be
completely developed in contrast to flowers that are visited by only honeybees
or only wild bees that tended to have misshapen fruits (Chagnon et al. 1993).
Effects such as this have rarely been looked for, but may prove to be
widespread.
4. MANAGEMENT CONCLUSIONS AND FUTURE DIRECTIONS
(A) POLLINATOR MANAGEMENT
Populations of wild pollinators can enhance production of some crops and are, in
this way, an important natural resource; but populations of wild pollinators are
frequently too sparse to adequately pollinate crops in agriculturally intensive
environments (table 1). The landscape studies summarized in this review were all
published during the last 5 years. Although more research is needed on a
landscape scale, we are in a much better position today than we have been in the
past to recommend landscape management practices to enhance wild pollinators. We
need landscape management practices that boost native pollinator densities by
increasing habitat-carrying capacity. We suggest integrating the following
general practices into management plans: (i) increase nesting opportunities with
the particular nesting needs of different pollinating species in mind and these
may include gaps in surface vegetation or modifying cultivation practices
(Shuler et al. 2005), retaining neighbouring forest nesting sites for
ground-nesting bees (Cane 1997a,b) or leaving dead wood providing holes for
cavity-nesting bees (Westrich 1996), (ii) increase forage by providing suitable
diverse floral resources in the local area and the broader landscape during the
season of pollinator activity (Kevan et al. 1990; Banaszak 1992; Westrich 1996;
Goulson 2003; Ghazoul 2006). Crop rotation using these flowering plants should
be especially applied in intensified uniform agricultural landscapes and may
also help to enhance other ecosystem services such as soil improvement, pest
management by breaking cycles of damaging pests or erosion control, (iii)
enhance opportunities for colonization by connecting habitats with flowering
strips and hedgerows around arable fields, small forest patches or even single
trees as ‘stepping stones’ (Steffan-Dewenter et al. 2002, 2006; Pywell et al.
2006), and (iv) reduce the risk of population crashes in the field and the
surrounding habitats by foregoing use of broad-spectrum insecticides during
bloom, especially those with systemic or micro-encapsulated formulations that
can contaminate nectar and pollen (Kevan 1975; Wood 1979; Delaplane & Mayer
2000). Financial burdens of these recommendations could be ameliorated through
agro-environmental schemes, such as those in Europe and the United States, which
compensate farmers who apply management strategies to conserve biodiversity.
(B) RESEARCH NEEDS
In this review, we found that inadequate information is available on the
pollination biology and pollinator requirements of many crops, especially when
considering differences among modern varieties and the contribution to
pollination services by different pollinator species.
We need to assess the potential impact of pollinator loss for a given crop in a
given production area. For this, we need to collect the following data:
experimental fruit and seed set from flowers visited by animal pollinators
versus unvisited flowers and those receiving airborne pollen flow or any passive
self-pollination. As plants are often resource limited, treatments should
ideally be applied to entire plants and not just a few flowers or a single
branch, otherwise, extrapolation can overestimate pollen limitation (Ashman et
al. 2004; Knight et al. 2006). Multi-year data are valuable as periodic weather
perturbations are the norm and perennial plants tend towards alternate year of
fruit and seed production (e.g. Herrera et al. 1998; Pías & Guitián 2006).
Studies over multiple seasons are also necessary to truly understand the
stability of the pollination service, because insect communities often show high
temporal variation (Cane & Payne 1993; Roubik 2001) and habitat-specific
temporal species turnover (Williams et al. 2001; Cane et al. 2005; Tylianakis et
al. 2005).
Studies for only three crops (watermelon, highland- and lowland coffee) are
available to address the links between a landscape variable and the stability of
crop pollination. More research of this kind is needed. The list of pollinators
known to be important for global crops was only 57 species, mainly bees. We
found only one study showing birds to be effective pollinators on feijoa
(Stewart 1989). We still need experiments to determine to what extent
non-insects (birds, bats and other vertebrates) contribute to crop production.
In addition, to adequately judge the value of conserving and managing for wild
pollinators, key pollinators in the main producing areas must be identified,
their habitat requirements studied and the economic benefit of their presence
estimated (e.g. Cane 1997b; Larsen et al. 2005). Today, only few areas and crops
have all the necessary data elements to access the impact of pollinator loss.
Our four general recommendations for landscape management (nesting
opportunities, floral resources, habitat connectivity and reduction of
pesticides) can be applied to all crops dependent on animal pollination in all
production areas. For further specific recommendations, we emphasize the need to
monitor the effects of applied management practices on crop production and
stability in restoration programmes (e.g. Pywell et al. (2006) for pollinator
foraging resources and Albrecht et al. in press for the pollination of three
herb species). We also emphasize the collection of data for understanding the
effects of spatial and temporal pollinator resource availability and for
interaction effects between honeybees and other bee species for crop pollination
to recommend future management applications.
Therefore, we urgently need more research in crop pollination along with better
coordination of the research efforts at the community level in different
producing areas to help sustain production of the diverse crops that nourish
humanity.
We thank Nora Hornsdorf for helping to collect literature, Sarah Greenleaf and
Barbara Gemmill for help with the crop selection and two anonymous referees for
helpful comments on the manuscript. This work was partly conducted as a part of
the Restoring Pollination Services Working Group supported by the National
Center for Ecological Analysis and Synthesis, a Center funded by NSF (grant no.
DEB-00-72909), the University of California at Santa Barbara, and the State of
California, and with funding by the Sixth European Union Framework
programme—Assessing Large-scale Environmental Risks to Biodiversity with Tested
Methods (Project ALARM (GOCE-CT-2003-506675); www.alarmproject.net).
FOOTNOTES
Electronic supplementary material is available at
http://dx.doi.org/10.1098/rspb.2006.3721 or via
http://www.journals.royalsoc.ac.uk.
© 2006 The Royal Society
Next Article
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THIS ISSUE
07 February 2007
Volume 274Issue 1608
*
Article Information
* DOI:https://doi.org/10.1098/rspb.2006.3721
* PubMed:17164193
* Published by:Royal Society
* Print ISSN:0962-8452
* Online ISSN:1471-2954
History:
* Manuscript received24/07/2006
* Manuscript accepted29/08/2006
* Published online27/10/2006
* Published in print07/02/2007
License:
© 2006 The Royal Society
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Keywords
* pollination
* spatial ecology
* conservation
* wild bees
* biodiversity
* agriculture
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