Importance of Pollinators in Changing Landscapes F PDF
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Review
Received 24 July 2006 303 This journal is q 2006 The Royal Society
Accepted 29 August 2006
304 A.-M. Klein et al. Review
Some authors provide coefficients of dependence on of natural- and semi-natural habitats in agricultural
animal-mediated pollination for several crops (Borneck & landscapes to increase and protect bee’s resources may
Merle 1989; Robinson et al. 1989a,b; Morse & Calderone be useful to improve pollination services. While landscape
2000), but despite their continuing acceptance, most of effects are known to affect communities of herbivorous
these reports do not cite data sources, and so it is impossible and predatory/parasitic insects in agro-ecosystems
to assess the reported level of dependence. Williams (1994) (reviewed in Cronin & Reeve 2005; Tscharntke et al.
provided coefficients for the dependence of European 2005; Bianchi et al. 2006), a similar evaluation of
crops on animal pollination and estimated the proportion landscape impact on crop pollination is lacking.
of insect pollinators that are honeybees, using information In this review, we summarize and evaluate information
from Crane & Walker (1984) and Free (1993). Both studies on three issues:
are less relevant today, because many new crop varieties
and pollination studies are available. To adequately (i) the identification of leading global crops that
evaluate the importance of animal pollination for plant depend on animal pollination for their production
products in our food supply, and for economic analyses of and their level of dependence on pollinators,
crop pollination by animals, we need a global review of (ii) the influence of land-use changes at both local and
crops considering their breeding systems, their flower- landscape scales for pollinator communities and
visiting fauna and the level of production increase resulting their services, and
from animal visitation and pollination, as supported by (iii) future options for landscape and agricultural
experimental evidence (Kevan & Phillips 2001). management to enhance wild pollinators and
Honeybees, mainly Apis mellifera, remain the most ensure pollination services for crop production.
economically valuable pollinators of crop monocultures
worldwide (McGregor 1976; Watanabe 1994; also shown
for several single crops, e.g. Roubik 2002 for coffee in
2. MATERIAL AND METHODS
Panama) and yields of some fruit, seed and nut crops
We first estimated the proportion of crop production
decrease by more than 90% without these pollinators
depending on animal pollination. We selected the leading
(Southwick & Southwick 1992). When wild bees do not
global crops on the world market out of the FAO crop
visit agricultural fields, managed honeybee hives are often
production list for the year 2004 (FAOSTAT 2005), such that
the only solution for farmers to ensure crop pollination.
the aggregate represented 99% of total global food pro-
Compared with the management of several wild bees,
duction (figure 1). We chose single crops and commodities
honeybees are versatile, cheap and convenient, but for
used for human food with an annual production of at least
some crops they are not the most effective pollinators on a
4 000 000 Metric tonnes (Mt). Production values are listed
per flower basis (reviewed in Parker et al. (1987), Torchio
individually for the single crops. Production of the commod-
(1990), Richards (1996), Cane (1997a) and Westerkamp &
ity crops is pooled in not elsewhere specified (NES)
Gottsberger (2000); see also Bosch & Blas (1994) for
commodities. A commodity is an aggregation of different
almond; Cane (1997b) and Javorek et al. (2002) for
crops (e.g. fresh vegetables NES includes 21 crops).
blueberry; Kremen et al. (2002, 2004) for watermelon;
Commodity compilation is based on a questionnaire that
Klein et al. (2003a,b) for highland and lowland coffee; Cane
countries fill out to include important crops for the world
(2005) for raspberry and blackberry; Greenleaf & Kremen
market which are not listed as a single crop by the FAO.
(in press) for field tomatoes; Bosch et al. (2006) for cherry).
Fifty-seven leading single crops and five commodities
Other crops await similar comparative pollinator study. The
(including 67 commodity crops) represented 99% (94.5
numbers of managed honeybee colonies are declining in
and 4.5%, respectively) of the total global food production.
some parts of the world (Williams et al. 1991; Matheson
Although production quantities for each commodity group
et al. 1996; Delaplane & Mayer 2000; Anonymous 2005)
are known, there is no breakdown for each commodity crop
largely owing to: (i) the spread of pests like parasitic
within these five groups, so we classified the annual production
mites (Varroa jacobsoni, V. destructor and Acarapis woodi;
of the commodities with respect to its pollinator dependence as
Downey & Winston 2001; Chen et al. 2004), the small hive
‘unknown’. We individually classified each of the resulting
beetle (Aethina tumida; Evans et al. 2003) and the
124 crops (57 leading single and 67 leading commodity crops)
microsporidian parasite Nosema ceranae (Higes et al.
into four categories of pollinator dependence:
2006), (ii) improper pesticide and herbicide use (Ingram
et al. 1996), (iii) ageing of the beekeeper population in (i) production increase with pollinators for plant parts that
Europe and North America, and (iv) lower market prices we consume (we define production as increased fruit
for their products and services. Indeed, declining honeybee set, fruit weight and/or quality, and seed number and/or
availability led to recent concern over pollination shortfalls quality, when pollinators have access to the flowers in
such as those seen for almonds in California (www. contrast to pollinator exclusion experiments),
almondboard.com). This situation also highlights the (ii) increase in seed production with pollinators to produce
potential risk of our sole reliance on honeybees for the vegetative parts that we consume,
agricultural pollination. (iii) increase in seed production with pollinators for
Fragmentation and degradation of near- and semi- breeding alone, as the plants reproduce vegetatively
natural habitats can be detrimental to bee communities and we consume the vegetative parts, and
(Rathcke & Jules 1994; Kremen et al. 2002, 2004; (iv) no production increase with pollinators.
Steffan-Dewenter et al. 2002, 2006; Larsen et al. 2005;
Cane et al. 2006). The main causal factor is loss or We next assessed the level to which animal pollination
dissociation of important resources for food and nesting matters to global crops directly used by humans. For this
(Hines & Hendrix 2005; Potts et al. 2005). Conservation approach, we expanded our list using all the crops listed to be
Yes
annual commodity No
35 commodity crops
production > 4*106 Mt?
Yes
No
57 single crops
67 commodity crops seeds to propage Yes
vegetative parts for 16 single crops
food? 16 commoditycrops
No
Appendix 2
72 single crops
35 commodity crops
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.
important on the world market, not restricted to the leading earlier studies not cited in Free (1993). For each listed crop,
crops, as was the case for electronic supplementary material we provide the following information:
1. We started with the same list used for electronic
supplementary material 1, the complete set of 137 single (i) Flower morphology and breeding system.
crops and 5 commodities (93 commodity crops) listed by the (ii) Capacity of the crop to produce fruit and/or seeds
FAO for the year 2004. We then reduced this list to 74 single without pollinators.
crops and 33 commodity crops, a total of 107, following the (iii) Animal groups or species known to be important
pathway illustrated in figure 1. flower visitors or pollinators; the primary pollinating
Free (1993) summarized the key references for pollination species are identified if there is a species for which at
requirements for 75 out of the 107 crops. We extended and least 80% of their single flower visits result in a fruit
updated his review, including both more recent literature and (Klein et al. 2003a,b) or species that improve fruit and
90
48
number of crops
single crops with
80 production > 4 millions Mt
commodity crops 40 × 108
70 39 with commodity
40 23 20 × 108
39
30
10
20 10 × 108
18
10
9
0 2 0
no increase increase unknown
impact of animal pollination
to production
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 MtZ55%); increase in seed production
with pollinators to produce the vegetative parts that we consume (six crops with 2108 MtZ9%); 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 MtZ36%). 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.
seed quality and quantity when abundant as compared vertebrates pollinate very few commodity crops (e.g. feijoa
with the level when all flower visitors are excluded. is pollinated by birds and durian seems to be pollinated by
(iv) Magnitude of the improvement in production and bats, electronic supplementary material 2). Among the 57
quality when pollinated by animals. We scored the single crops that show increased production, 26 (55% with
degree of production dependence into five classes: (i) 12!108 Mt or 19% of global food) increase seed
essential (production reduction by 90% or more production with animal pollination to produce vegetative
without flower visitors), meaning that production parts for human food, while an additional seven crops
requires animal pollination, (ii) high (40 to less than (8!108 Mt, 36%) show increased seed production for
90% reduction), (iii) modest (10 to less than 40%), (iv) breeding alone, as the plants reproduce vegetatively and
little (greater than 0 to less than 10%), (v) no reduction, only vegetative parts are consumed (e.g. potatoes, sweet
and (vi) unknown, meaning that no literature was potatoes and manioc, electronic supplementary material 1).
available to adequately review the breeding systems or The production increase with pollinators for seeds of
draw conclusions about pollinator dependence. vegetatively propagated crops permits breeding progress
and hybridization for the development of new varieties.
Animal pollination is irrelevant to 18 of the leading
3. RESULTS AND DISCUSSION single crops (comprising 60% or 39!108 Mt of the world
(a) Importance of animal pollination for global production) and 10 of the leading commodity crops.
crop production These are wind- or passively self-pollinated grasses
Production of 39 of the leading 57 single crops increases (cereals and sugarcane), dominating the leading global
with pollinating animals (figure 2). In aggregate, these crop list (electronic supplementary material 1; figure 2).
crops account for 35% (23!108 Mt) of global food Twenty per cent of the overall crop production comes
production (figure 2), but because most of these crops from crops that increase fruit and vegetable production
are not entirely dependent on animal pollination, the with animal pollination, and ca 15% comes from crops that
amount of production directly attributable to animals is increase seed production with animal pollination. Our
lower than this value. In addition, production of 48 of the results further show that a majority of global crops could
67 crops of the five leading global commodities increases experience production loss owing to pollinator limitation
with pollinating animals (figure 1). Only insects are (39 single crops increase fruit, vegetable or seed production
demonstrated pollinators of the single crops, while with pollinators compared with 18 that do not, and 87 of
27
25 increase in production, and for 21 crops, production of
21 some species or varieties increase little, others not at all. For
20 seven crops, production did not increase in the studies
15 13 available: chick pea, garden and field peas and lentil, which
9 are passively self-pollinated, and olive, pepper, quinoa and
10
7 grapes, which rely on passive self- and wind-pollination.
5 Pollination needs of nine crops remain unknown (figure 3;
0 electronic supplementary material 2).
essential high modest little no unknown Gaps in our knowledge of pollination requirements are
increase illustrated by the example of highland coffee, one of the
Figure 3. Level of dependence on animal-mediated pollina- better studied crops. Although the breeding systems are well
tion. The selected crops are those included directly in the studied and pollinators have been identified in different
production list published by the FAO for 2004 (FAOSTAT coffee production regions, few varieties have been studied,
2005). We further included commodity crops for which the and production of some varieties may not increase with
production was pooled in commodities with an annual 2004 animal pollination as much as those studied to date (A.-M.
commodity production greater than 4 000 000 Metric tonnes Klein, unpublished data). The need to consider different
(Mt). Only crops that produce fruits or seeds for direct genetic materials is also highlighted by the fact that varieties
human use as food were considered. We did not include: (i)
of many crops, such as citrus, blueberries, most stone fruit
crops for which seeds are only used for breeding or to grow
vegetable parts for direct human use or for forage, and (ii) crops, and almonds, show great production variation with
crops known to be only wind-pollinated, passively self- animal pollination (see Ortega et al. 2002 for almond). We
pollinated or reproduced vegetatively. Essential, pollinators also do not know much about the mechanisms of pollination
essential for most varieties (production reduction by 90% provided by most pollinator species (Klein et al. 2003a), and
more, comparing experiments with and without animal flower-visiting insect communities of different production
pollinators); high, animal pollinators are extreme (40 to regions across the world can differ greatly. For example, the
less than 90% reduction); modest, animal pollinators are flower visitors to coffee in Ecuador with more than 95%
clearly beneficial (10 to less than 40% reduction); little, some social and less than 5% solitary bees (Veddeler et al. 2006)
evidence suggests that animal pollinators are beneficial
are very different from flower-visiting communities in
(greater than 0 to less than 10% reduction); no increase,
Indonesia with 70% social and ca 30% solitary bees (Klein
no production increase with animal-mediated pollination;
unknown, empirical studies are missing. et al. 2003a,b). Such differences may lead to differences in
pollination success.
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 (b) Consequences of agricultural management
to a healthy diet. These results support the contention of at local and landscape scales for wild versus
Richards (2001) and Ghazoul (2005) that primary food managed pollinators
production, and especially our staple foods, is independent Wild bees and other insects can pollinate many crops, but
of insect pollination. Thinking beyond caloric intake, their value for crop pollination has been overlooked for
however, our results support the opinion of Steffan- centuries. As their services are increasingly being recog-
Dewenter et al. (2005) that our diet would be greatly nized for agriculture (e.g. O’Toole 1993; Cane 1997b;
impoverished, both nutritionally and culturally, if pollina- Kevan & Phillips 2001; Klein et al. 2003a; Slaa et al. 2006),
tion services further decline. the adequate management of local agro-ecosystems and the
In a second list (electronic supplementary material 2), conservation of suitable natural or semi-natural pollinator
we quantified the level of dependence on animal pollina- habitats in the surrounding landscapes are receiving more
tion. We found empirical evidence for increased production attention. Little information exists on the ways in which
with pollinators in 92 out of 108 selected crops (figure 3). local management influences agricultural pollination
Among these 92 crops, for the majority (82 crops), data (Richards 2001). Considering the 107 crops listed in
were available from experiments comparing measures of electronic supplementary material 2, we found increased
pollination (e.g. fruit set, number of seeds, fruit or seed production with animal pollination of at least 10% or
weight, or pollen deposition) at the level of flowers, higher (categories essential, great and modest) for 63 crops,
inflorescences or whole plants, with and without access when considering only the crops for which field experi-
to pollinators. For 10 crops, we classified the evidence ments were available (NZ93). Therefore, we suggest that
for increased production with pollinators as ‘indirect pollination of at least these 63 crops should be vulnerable to
evidence’, because experiments with pollinator exclusion agricultural intensification that may reduce the diversity
were lacking, but the experiments demonstrated, for and abundance of pollinators (e.g. Kremen et al. 2002;
example, self-incompatibility and a need for cross pollina- Klein et al. 2003a,b). Among the 63 crops, the production
tion that could not be achieved by wind (electronic of 13 crops that are entirely dependent on pollinators to set
supplementary material 2; figure 3). Animal pollination fruits might be severely impacted by pollinator loss through
was found to be essential for most varieties of the following agricultural intensification. This risk is the greatest for
13 crops: atemoya, Brazil nut, cantaloupe, cocoa, kiwi, crops that rely on a narrow range of pollinating species,
macadamia nut, passion fruit, pawpaw (Indian banana), such as passion fruit and vanilla.
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.)
Annona squamosa ! comparison of sites near and pollinator diversity Blanche & Cunningham
A. cherimola (sugar apple) far from forest fragments (fruit set reduction with (2005)
pollinator exclusion)
Brassica napus and B. rapa comparison of organic, number of seeds per silique Morandin & Winston (2005)
(turnip rape, canola and conventional and geneti- from a flower sample
oilseed rape) cally modified (GM) fields
proportional area of unculti- number of seeds per silique Morandin & Winston (2006)
vated land around fields from a flower sample
within a 750 m radius
Citrullus lanatus (watermelon) comparison of organic versus number of pollen grains/ Kremen et al. (2002, 2004)
conventional fields stigma, n.s.
proportional area of oak number of pollen grains/ Kremen et al. (2002, 2004)
woodland and chaparral stigma
habitat
Citrus paradisi (grapefruit) distance from forest number of pollen grains/ Chacoff (2006) and Chacoff &
stigma number of pollen Aizen (2006)
tubes/stigma
Coffea arabica (coffee) coffee plants near, intermedi- number of pollen grains/ Ricketts (2004) and Ricketts
ate and far from forest stigma, fruit set, seed et al. (2004)
fragments mass
distance from forest fruit set Klein et al. (2003a)
plant diversity fruit set Klein et al. (2003a)
coffee monocultures versus fruit set De Marco & Coelho (2004)
agroforestry
comparison sites near and far fruit set De Marco & Coelho (2004)
from forest fragments
Coffea canephora (coffee) distance from forest fruit set Klein et al. (2003b)
Dimocarpus longan (longan comparison sites near and far number of fruits per centi- Blanche et al. (in press)
fruit) from forest fragments metre panicle
Helianthus annuus (sunflower) proportional area of natural wild bee diversity and Greenleaf & Kremen (2006)
habitat abundance (estimated
increase in seed set via
single visit studies)
organic versus conventional wild bee diversity and abun- Greenleaf & Kremen (2006)
farm management dance, n.s.
Lycopersicon esculentum distance to natural habitat Bombus vosnesenskii Greenleaf & Kremen (in
(tomato) abundance; Anthophora press)
urbana abundance, n.s.
(fruit set and fruit weight
reduction with pollinator
exclusion for variety with
exserted stigma)
Macadamia integrifolia (maca- percentage of eucalyptus Trigona abundance (seed set Heard (1994) and Heard &
damia nut) forest surrounding orchards reduction with pollinator Exley (1994)
exclusion and only Trigona
pollinated)
comparison of sites near and number of fruits/raceme Blanche et al. (in press)
far from forest fragments
We found 16 studies on the effects of agricultural habitats (figure 4). The impact of landscape context on
intensification on pollination at local or landscape scale of visitation rates and fruit set of crops has been assessed as the
nine crops on four continents (table 1). All of these studies proportion of near-natural habitats in the surrounding
show negative consequences of local and/or regional landscape (e.g. Kremen et al. 2004; Morandin & Winston
agricultural intensification for pollination. For water- 2006) or as the linear isolation distance from near-natural
melon and coffee, higher variation in pollination success habitat (e.g. Klein et al. 2003a,b; Chacoff & Aizen 2006).
was found in sites of intensified agriculture isolated from We found a linear positive relationship between fruit set
natural or semi-natural habitats (Kremen et al. 2004; stability and isolation to the rainforest margin for lowland
Steffan-Dewenter et al. 2006). and highland coffee (Klein et al. 2003a,b), whereas a
The existing studies suggest that crops having a log-linear relationship was found for watermelons
production increase with pollinators of at least 10% (Kremen et al. 2004). Agro-ecosystems with more semi-
might show reduced fruit set and increased variance in natural habitats are often more pollinator-species rich
fruit set at locations increasingly isolated from near-natural (Steffan-Dewenter et al. 2002; Kremen & Chaplin 2006;
Table 2. Species list of known pollinators for global crops that are grown for direct human consumption.
honey bees Apis cerana Fabr., A. dorsata Fabr., A. florea Fabr. and A. mellifera L.
stingless bees Melipona 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 Moure
bumble bees Bombus 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 Radoszkowski
solitary bees Amegilla 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 Moure
wasps Blastophaga psenes L.
hover flies and other flies Eristalis cerealis Fabr., E. tenax L. and Trichometallea pollinosa Townsend
beetles Carpophilus hemipterus L. and Carpophilus mutilatus Erichson
thrips Thrips hawaiiensis Morgan and Haplothrips (Haplothrips) tenuipennis Bagnall
birds Turdus merula L. and Acridotheres tristis L.
need landscape management practices that boost native We need to assess the potential impact of pollinator loss
pollinator densities by increasing habitat-carrying capacity. for a given crop in a given production area. For this, we
We suggest integrating the following general practices into need to collect the following data: experimental fruit and
management plans: (i) increase nesting opportunities with seed set from flowers visited by animal pollinators versus
the particular nesting needs of different pollinating species unvisited flowers and those receiving airborne pollen flow
in mind and these may include gaps in surface vegetation or or any passive self-pollination. As plants are often resource
modifying cultivation practices (Shuler et al. 2005), limited, treatments should ideally be applied to entire
retaining neighbouring forest nesting sites for ground- plants and not just a few flowers or a single branch,
nesting bees (Cane 1997a,b) or leaving dead wood otherwise, extrapolation can overestimate pollen limitation
providing holes for cavity-nesting bees (Westrich 1996), (Ashman et al. 2004; Knight et al. 2006). Multi-year data
(ii) increase forage by providing suitable diverse floral are valuable as periodic weather perturbations are the norm
resources in the local area and the broader landscape and perennial plants tend towards alternate year of fruit and
during the season of pollinator activity (Kevan et al. 1990; seed production (e.g. Herrera et al. 1998; Pı́as & Guitián
Banaszak 1992; Westrich 1996; Goulson 2003; Ghazoul 2006). Studies over multiple seasons are also necessary to
2006). Crop rotation using these flowering plants should be truly understand the stability of the pollination service,
especially applied in intensified uniform agricultural land- because insect communities often show high temporal
scapes and may also help to enhance other ecosystem variation (Cane & Payne 1993; Roubik 2001) and habitat-
services such as soil improvement, pest management by specific temporal species turnover (Williams et al. 2001;
breaking cycles of damaging pests or erosion control, (iii) Cane et al. 2005; Tylianakis et al. 2005).
enhance opportunities for colonization by connecting Studies for only three crops (watermelon, highland-
habitats with flowering strips and hedgerows around arable and lowland coffee) are available to address the links
fields, small forest patches or even single trees as ‘stepping between a landscape variable and the stability of crop
stones’ (Steffan-Dewenter et al. 2002, 2006; Pywell et al. pollination. More research of this kind is needed. The list
2006), and (iv) reduce the risk of population crashes in the of pollinators known to be important for global crops was
field and the surrounding habitats by foregoing use of only 57 species, mainly bees. We found only one study
broad-spectrum insecticides during bloom, especially showing birds to be effective pollinators on feijoa (Stewart
those with systemic or micro-encapsulated formulations 1989). We still need experiments to determine to what
that can contaminate nectar and pollen (Kevan 1975; extent non-insects (birds, bats and other vertebrates)
Wood 1979; Delaplane & Mayer 2000). Financial burdens contribute to crop production. In addition, to adequately
of these recommendations could be ameliorated through judge the value of conserving and managing for wild
agro-environmental schemes, such as those in Europe and pollinators, key pollinators in the main producing areas
the United States, which compensate farmers who apply must be identified, their habitat requirements studied and
management strategies to conserve biodiversity.
the economic benefit of their presence estimated (e.g.
Cane 1997b; Larsen et al. 2005). Today, only few areas
(b) Research needs and crops have all the necessary data elements to access
In this review, we found that inadequate information is the impact of pollinator loss.
available on the pollination biology and pollinator Our four general recommendations for landscape
requirements of many crops, especially when considering management (nesting opportunities, floral resources,
differences among modern varieties and the contribution habitat connectivity and reduction of pesticides) can be
to pollination services by different pollinator species. applied to all crops dependent on animal pollination in all
production areas. For further specific recommendations, Bosch, J. & Blas, M. 1994 Foraging behaviour and pollinating
we emphasize the need to monitor the effects of applied efficiency of Osmia cornuta and Apis mellifera on almond
management practices on crop production and stability in (Hymenoptera, Megachilidae and Apidae). Appl. Entomol.
restoration programmes (e.g. Pywell et al. (2006) for Zool. 29, 1–9.
Bosch, J., Kemp, W. P. & Trostle, G. E. 2006 Bee population
pollinator foraging resources and Albrecht et al. in press
returns and cherry yields in an orchard pollinated with
for the pollination of three herb species). We also
Osmia lignaria (Hymenoptera: Megachilidae). J. Econ.
emphasize the collection of data for understanding the Entomol. 99, 408–413.
effects of spatial and temporal pollinator resource avail- Buchmann, S. L. & Nabhan, G. P. 1996 The forgotten
ability and for interaction effects between honeybees and pollinators. Washington, DC: Island Press.
other bee species for crop pollination to recommend future Burd, M. 1994 Bateman’s principle and reproduction: the
management applications. role of pollinator limitation in fruit and seed set. Bot. Rev.
Therefore, we urgently need more research in crop 60, 83–139.
pollination along with better coordination of the research Cane, J. H. 1997a Ground-nesting bees: the neglected
efforts at the community level in different producing areas pollinator resource for agriculture. Acta Hort. 437, 309–324.
Cane, J. H. 1997b Lifetime monetary value of individual
to help sustain production of the diverse crops that
pollinators: the bee Habropoda laboriosa at rabbiteye
nourish humanity. blueberry (Vaccinium ashei Reade). Acta Hort. 446, 67–70.
We thank Nora Hornsdorf for helping to collect literature, Cane, J. H. 2005 Pollination potential of the bee Osmia aglaia
Sarah Greenleaf and Barbara Gemmill for help with the crop for cultivated red raspberries and blackberries (Rubus:
selection and two anonymous referees for helpful comments Rosaceae). Hortscience 40, 1705–1708.
on the manuscript. This work was partly conducted as a part Cane, J. H. & Payne, J. A. 1993 Regional, annual and sesonal-
of the Restoring Pollination Services Working Group variation in pollinator guids — intriusic traits of bees
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