How many flowering plants are pollinated by animals?

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Oikos 120: 321–326, 2011
doi: 10.1111/j.1600-0706.2010.18644.x
© 2011 The Authors. Oikos © 2011 Nordic Society Oikos
Subject Editor: Anna Traveset. Accepted 22 October 2010
How many flowering plants are pollinated by animals?
Jeff Ollerton, Rachael Winfree and Sam Tarrant
J. Ollerton (jeff[email protected]) and S. Tarrant, School of Science and Technology, Univ. of Northampton, Avenue Campus,
Northampton, NN2 6JD, UK. Present address for ST: RSPB UK Headquarters, The Lodge, Sandy, Bedfordshire, SG19 2DL, UK. –
R. Winfree, Dept of Entomology, Rutgers Univ., New Brunswick, NJ 08901, USA.
It is clear that the majority of flowering plants are pollinated by insects and other animals, with a minority utilising abiotic
pollen vectors, mainly wind. However there is no accurate published calculation of the proportion of the ca 352 000 species
of angiosperms that interact with pollinators. Widely cited figures range from 67% to 96% but these have not been based
on firm data. We estimated the number and proportion of flowering plants that are pollinated by animals using published
and unpublished community-level surveys of plant pollination systems that recorded whether each species present was
pollinated by animals or wind. The proportion of animal-pollinated species rises from a mean of 78% in temperate-zone
communities to 94% in tropical communities. By correcting for the latitudinal diversity trend in flowering plants, we
estimate the global number and proportion of animal pollinated angiosperms as 308 006, which is 87.5% of the estimated
species-level diversity of flowering plants. Given current concerns about the decline in pollinators and the possible resulting
impacts on both natural communities and agricultural crops, such estimates are vital to both ecologists and policy makers.
Further research is required to assess in detail the absolute dependency of these plants on their pollinators, and how this
varies with latitude and community type, but there is no doubt that plant–pollinator interactions play a significant role in
maintaining the functional integrity of most terrestrial ecosystems.
Plant–pollinator relationships may be one of the most ecologically important classes of animal–plant interaction:
without pollinators, many plants could not set seed and
reproduce; and without plants to provide pollen, nectar and
other rewards, many animal populations would decline, with
consequent knock-on effects for other species (Kearns et al.
1998). In addition, biotic pollination is thought to be a key
factor in the diversification of some major groups of plants
and animals (Dodd et al. 1999, Ollerton 1999). Human reliance on animal-pollinated crops demonstrates the value of
the ecosystem services provided by pollinators: 75% of the
world’s leading food crops show increased fruit or seed set
with animal pollination (Klein et al. 2007), with the economic value of this benefit being €153 billion annually, or
9.5% of the value of world agricultural production (Gallai
et al. 2009).
In part because of the functional importance of biotic
pollination, recent evidence for declines in native pollinator abundance and diversity has generated widespread
concern (Biesmeijer et al. 2006, Kosior et al. 2007, Colla
and Packer 2008, Grixti et al. 2009, Winfree et al. 2009,
though see Ghazoul 2005). In response to these concerns,
a number of national governments and organisations such
as the Convention on Biological Diversity have instigated
‘Pollinator initiatives’ to protect pollinators. Most recently,
the government of the UK, in consortia with the Wellcome
Trust, has committed funding of £10 million (approximately
$16.5 million) over the next five years for research aimed at
halting pollinator declines.
Surprisingly, however, if a policy-maker or conservation planner were to ask an ecologist the straightforward
question ‘How many species of flowering plants are pollinated by animals?‘ the answer would be: ‘ We do not
know’. There is no consensus nor even recent, evidencebased published estimate to which the questioner could be
referred. Some of the most cited sources, whose estimates
range from 67% to 96% of all angiosperm species being
animal pollinated, are obscure as to how these figures have
been calculated (Axelrod 1960, Renner 1996, Nabhan and
Buchmann 1997). In contrast to the case for crop plants,
which constitute ⬍ 0.1% of all flowering plant species but
have generated several recent reviews on animal pollination
(Klein et al. 2007, Aizen et al. 2009, Gallai et al. 2009),
there has been no systematic attempt to assess the fraction
of the global flora that uses pollinators.
In order to provide an accurate estimate of the number
and proportion of biotically pollinated flowering plant species
worldwide, we compiled a data set of published and unpublished community-level surveys of plant–pollinator interactions that quantified the means of pollination, whether by
animal or wind, for all plant species in the community. Our
goals were to determine: (1) the variation in the proportion
of animal pollinated flowering plants in terrestrial communities across latitudinal zones; (2) the global total number
321
and proportion of flowering plants that use animals as pollinators.
It is important to realize that the fact that a plant species
is pollinated by animals does not imply that all individual
plants of that species require animal pollination in order to
set seed at all times. Many species that use animal pollinators have a mixed mating system, meaning that individual
plants can self-pollinate without the assistance of animals.
However, at the species level, plants with mixed mating
systems still require animal pollination because long-term
selfing by all individuals would end inter-breeding among
individuals of the same species. In addition, many plant
species are either genetically self-incompatible or, although
self-compatible, require animal pollinators to move pollen
from the anthers to the stigma in order to self-pollinate.
Lastly, a global meta-analysis of studies assessing pollen
limitation in animal-pollinated plants suggests that individuals in many plant populations receive less pollen than
is required for full seed set, particularly in regions with high
plant diversity (Vamosi et al. 2006), which suggests that in
general there is a high dependency of flowering plants on
their pollinators.
Data set and methods
The data set of 42 surveys represents all of the available
published studies that we could locate, plus eight unpublished surveys by ourselves and colleagues (Appendix 1).
Studies were not included if they were restricted to particular life forms such as trees (Frankie 1980) or if they
repeated similar studies in the same geographical area (Carpenter et al. 2003, cf. Kato and Kawakita 2004). We also
excluded some potentially useful studies from Japan (Kato
et al. 1993, Yamazaki and Kato 2003) because they were
focussed mainly on animal pollinated species and excluded
many species of wind pollinated plants, thereby biasing the
community-scale estimates (M. Kato pers. comm. 2010).
We took an ecological, community-level approach because
we were interested in the ecological question of how many
plant species in typical terrestrial communities are animalpollinated, and how this fraction varies by latitude. An
alternative approach, not taken here, would be phylogenetic, and would use the species rather than the plant
community as the sampling unit. Such an approach is not
feasible at present, however, given the fact that for most
of the ca 352 000 species of flowering plants the mode of
pollination is currently unknown, and that there have been
repeated switches between wind and biotic pollination
within some plant families (e.g. Asteraceae).
In each data set, researchers categorized plant species
as either biotically pollinated (by insects and/or vertebrates) or wind pollinated based on observations of both
flower visitors and the floral phenotype. A limitation of
this approach is that it might misclassify plant species that
are obligately self pollinating or non-sexually reproducing
(e.g. seed production without fusion of gametes, such as
apomixis), which, if flower visitors were observed, might
be erroneously classified as biotically pollinated. Likewise,
apparently wind pollinated taxa (e.g. some grasses) could
also be obligate selfers or apomicts and would also be
322
misclassified, which would serve to balance the relative
proportions of biotically versus abiotically pollinated species. These errors should be small, however, because there
are relatively few obligately apomictic and self-pollinating
species and previous work suggests that these will be a
small proportion of the total number of species within
most terrestrial communities. For example, the studies by
Moldenke in California and Chile estimated that between
1% and 9% of all species in each community were obligate
selfers or apomicts, with up to 13% in Colorado communities (Moldenke 1979, Moldenke and Lincoln 1979). As
the authors acknowledged even these estimates are likely
to be too high due to low sampling effort for some species
combined with infrequent insect visitation rates, resulting in some species being misclassified as obligate selfers
when in fact they are animal pollinated (Moldenke and
Lincoln 1979, p. 353). Therefore the inclusion of flowering plants that do not engage in out-crossing or sexual
reproduction should not greatly affect the conclusions
drawn from this analysis, though future analyses using
more comprehensive data on plant breeding systems are
certainly welcome.
The plant communities were classified according to latitudinal zone following Ollerton et al. (2006): temperate (64°
to 40°), subtropical (39° to 30°), and tropical (29° to 0°).
For the purposes of this paper, the arctic was not included
as a zone as only one study meeting our criteria for inclusion could be found. Data were analysed using SPSS 17.0
for Windows.
Results and Discussion
The mean proportion of animal-pollinated plants increases
from 78% of species in temperate-zone communities, to
94% in tropical communities (Fig. 1). This confirms the
results of Regal (1982) who found that the proportion of
wind pollinated trees and shrubs declined in tropical communities, for reasons that are still far from clear (Schemske et al. 2009). Our findings that there are significantly
greater numbers of animal pollinated plants in tropical
communities (regardless of life form) parallels the increase
in the proportion of plants with functionally specialized
pollination systems (i.e. pollinated by only a single functional group of animals, such as birds, hawkmoths, etc.) in
tropical communities, as found by Ollerton et al. (2006).
Whether these two patterns are directly associated is not
known, but it is possible that the greater numbers of animal pollinated plants in the tropics has provided the impetus for the evolution of greater functional specialization
(Schemske et al. 2009).
Using a global mean across all data sets, without accounting for the distribution of plant species in relation to latitude,
we find that 85.0% of flowering plants are biotically pollinated; that is, 299 200 species, assuming a total figure of 352
000 species of angiosperms (Paton et al. 2008). However,
a more accurate estimate will take into account the relative
species richness of the different latitudinal zones, because the
tropics have more angiosperm species than temperate and
subtropical regions (Hillebrand 2004). Using the regional
estimates of plant species richness from Kier et al. (2005),
there is significantly greater ecological specialisation than
is normally found, such as southern Africa (Johnson et al.
2009). If wild pollinator declines continue, we run the risk
of losing a substantial proportion of the world’s flora.
Acknowledgements – We would like to thank the authors of the
published studies for their efforts, Nick Waser and Mary Price for
supplying unpublished data, and Vince Tepedino and Makoto Kato
for discussions. Thanks also to Linus Svensson and Anna Traveset
for valuable comments that improved the manuscript.
References
Figure 1. The mean (⫾SD) proportion of animal pollinated plant
species found in terrestrial communities at different latitudes. The
global average represents the mean of all studies used in the analysis.
The global (corrected) average takes into account the relative
distribution of plant diversity in the different zones. Data for the
three latitudinal zones were analyzed with a one way ANOVA:
F2,39 ⫽ 5.9, p ⫽ 0.006. LSD post-hoc test indicates that the only
significant differences are between tropical and the other latitudinal
zones.
we calculate that approximately 50.5% of angiosperm diversity is contained within the tropics, 27.7% in the subtropics
and 21.8% the temperate regions. The number and proportion of biotically pollinated flowering plants can therefore be
calculated as:
Σ(Pzone ⫻ D ⫻ Bzone)
where: Pzone ⫽ the proportion of flowering plants in each of
the three latitudinal zones; D ⫽ global angiosperm richness
(estimated as 352 000 species by Paton et al. 2008); Bzone ⫽
the proportion of biotically pollinated flowering plants in
each of the three latitudinal zones – Fig. 1.
Therefore the estimated number and proportion globally
is: (Ptropics ⫻ D ⫻ Btropics) ⫹ (Psubtropics ⫻ D ⫻ Bsubtropics) ⫹
(Ptemperate ⫻ D ⫻ Btemperate) ⫽ (0.505 ⫻ 352 000 ⫻ 0.939) ⫹
(0.277 ⫻ 352 000 ⫻ 0.830) ⫹ (0.218 ⫻ 352 000 ⫻ 0.784)
⫽ 308 006 species or 87.5% of all flowering plant species
(Fig. 1).
Our estimates are based upon a sample of approximately
4000 flowering plant species, or slightly more than 1% of the
estimated number of angiosperms, from a geographically
non-random distribution of communities (Appendix 1).
Nonetheless, this is the most comprehensive data set that
can currently be assembled to answer the question of how
many flowering plants are animal pollinated.
The high proportion of biotically pollinated flowering plants reinforces concerns about the potential consequences of pollinator losses for the world’s flora. Although
many plants are flexible as to their interactions with pollinators and there is significant substitutability in these communities (Alarcón et al. 2008), there is a point at which
ecological redundancy is exhausted with continued pollinator species loss particularly in parts of the world where
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Appendix 1. Studies used in the analysis.
Reference
Kress and Beach 1994
Burkill 1897
van Dulmen 2001
van Dulmen 2001
Corlett 2001
O’Brien 1980
Robertson 1928
Willis and Burkill 1895,
1903a, b,1908
Bernadello et al. 2001
Ramirez and Brito 1992
Momose et al. 1998
Herrera 1988
Pojar 1974
Waser and Price unpubl.
Ollerton unpubl.
Ostler and Harper 1978
Machado and Lopes 2004
Gottsberger and Gottsberger
2006
Moldenke and Lincoln 1979
Kato and Kawakita 2004
Kato 2000
Moldenke 1979
No. of
flowering
plant species
Percentage of
wind pollinated
species
Percentage of
biotically
pollinated species
Latitudinal
zone
La Selva, Costa Rica
coastal scrub, UK
upland rainforest, Colombia
flooded rainforest, Colombia
scrub/secondary forest, Hong Kong.
alpine pavement plain, California
prairie, Illinois
lower alpine, Scotland
277
37
86
101
83
15
391
143
2.5
24.3
0.0
2.0
0.0
13.3
3.8
4.9
97.5
75.7
100.0
98.0
100.0
86.7
96.2
95.1
tropical
temperate
tropical
tropical
tropical
subtropical
temperate
temperate
Juan Fernandez Islands, Chile
palm swamp, Venezuela
rainforest, Malaysia
semi-arid scrub, Spain
salt marsh, Canada
Sphagnum bog, Canada
subalpine meadow, Canada
grassland, Virginia Basin, Colorado
rainforest, Kumu, Guyana
savannah, Kumu, Guyana
grassland, Wahroonga, South Africa
scrub/grassland, Mantanay, Peru
scrub/grassland, Northampton - UK
coastal scrub, Bahia de Patano,
Venezuela
xerophytic scrub, Güimar Badlands,
Tenerife
woodland, USA
Caatinga, Brazil
Cerrado, Brazil
42
33
129
26
18
34
45
64
59
43
74
148
162
78
54.8
15.2
0.0
19.2
66.7
41.2
24.4
9.4
5.1
14.0
6.8
4.1
20.4
15.4
45.2
84.8
100.0
80.8
33.3
58.8
75.6
90.6
94.9
86.0
93.2
95.9
79.6
84.6
subtropical
tropical
tropical
subtropical
temperate
temperate
temperate
temperate
tropical
tropical
temperate
tropical
temperate
tropical
18
11.1
88.9
subtropical
125
147
301
36.0
2.0
13.0
64.0
98.0
87.0
temperate
tropical
tropical
not given
not given
not given
not given
not given
17.0
21.0
12.0
17.0
19.0
83.0
79.0
88.0
83.0
81.0
temperate
temperate
temperate
temperate
temperate
95
54
140
157
72
84
3.2
9.3
15.0
11.0
10.0
20.0
96.4
90.7
85.0
89.0
90.0
80.0
tropical
tropical
subtropical
subtropical
subtropical
subtropical
140
154
158
105
80
11.0
17
21
10
7
89.0
83
79
90
93
subtropical
subtropical
subtropical
subtropical
subtropical
Study site
alpine, montane Colorado
Aspen, montane Colorado
sage, montane Colorado
grassland, montane Colorado
spruce-fir woodland, montane
Colorado
all habitats, New Caledonia
all habitats, Amami Island, Japan
coastal scrub, Torrey Pines, California
chaparral, Japatul Valley, California
chaparral, Echo Valley, California
oak-pine forest, Mount Laguna,
California
desert scrub, Ocotillo, California
Papudo, Chile
Fundo Santa, Chile
Cero Porterillo, Chile
El Tofo, Chile
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