I
nvasive plants can displace native species
through competition for nutrients, water,
light and space. Here we show that they
may also exert indirect pressure by compet-
ing for pollinators. We use the Asian plant
Impatiens glandulifera as an example — this
aggressive invader tempts bee pollinators
away from native flowers with its rich nectar,
which is more rewarding than that of any
known native plant in central Europe. This
causes a reduction of seed set in local plants
in the vicinity and enables I. glandulifera to
take over, reducing the fitness of native flora
before competition for other resources even
takes effect.
In just over a century since its introduc-
tion from the Himalayas, I. glandulifera (Fig.
1a) has conquered more than half of the
river banks in the Czech Republic
1
and is
spreading at a comparable rate elsewhere in
Europe
2
and in North America
3
. At over
2 metres high, it is the tallest annual in
Europe, with extensive branching of the
main stem ensuring monopoly of the aerial
environment. It also tolerates a wide range
of climates and soil types
4
, which con-
tributes to its success as a competitor. Each
plant produces about 2,500 seeds, which fall
to the ground at a density of 5,000–6,000 per
square metre (ref. 2).
Pollination systems may be viewed as
biological markets in which animals choose
between ‘products’ (flower species) on the
basis of their quality (sugar quantity in
nectar, for example) and the plants compete
for ‘customers’ (pollinators)
4–6
. We tested
whether competition for pollinators
4,5
could
be a mechanism by which I. glandulifera
successfully excludes other plants. We first
quantified the rewards they offer to pollina-
tors. The nectar sugar concentration of I.
glandulifera (48%) is well within the range
of bumblebee-pollinated plants
7
, but the
rate of sugar production (0.47DŽ0.12 mg per
flower per hour; nǃ213) is substantially
higher than in the other common bumble-
bee-visited species that we found associated
with I. glandulifera along river-banks near
Würzburg. These include Stachys palustris
(0.04DŽ0.02 mg per flower per hour;
nǃ167), Lythrum salicaria (0.02DŽ0.01 mg
per flower per hour; nǃ85) and Epilobium
hirsutum (0.01DŽ0.02 mg per flower per
hour; nǃ40).
The rate of sugar production by I. glan-
dulifera exceeds that recorded for any other
central European plant — of the nectar-
rewarding plant species, none produces
more than of 0.3 mg per flower per hour
and most generate less than 0.1 mg per
flower per hour
7–9
. I. glandulifera offers an
even richer reward than some flowers polli-
nated by hummingbirds (up to 0.27 mg per
flower per hour by Ipomopsis aggregata
10
).
Stachys palustris occurs along river-banks
in ‘pure’ patches, as well as in patches inter-
mingled with I. glandulifera, a convenient
arrangement for comparing the two species.
Because of its extraordinarily rewarding
nectar, visitation of I. glandulifera by bum-
blebees (mostly Bombus pascuorum) is fre-
quent (2.5DŽ1.5 visits per flower per 10-min
interval) — roughly fourfold more often
than to S. palustris (Fig. 1b).
We simulated invasion by I. glandulifera
by moving ten large I. glandulifera plants in
water buckets into previously pure S. palus-
tris patches (both plant types bore at least 30
flowers each). Bees readily accepted the new
plants and, although visitation (0.88DŽ0.19
visits per flower per 10 min) was less fre-
quent than in naturally occurring I. glan-
dulifera patches, it was still greater than to S.
palustris (Fig. 1b). We monitored the visita-
tion frequency to S. palustris patches for
1–2 days before and 1–3 days after introduc-
ing I. glandulifera (excluding the first 3 h),
by recording visitation to marked flowers in
7–50 short intervals (10 min per patch)
according to a random schedule. We found
that the number of visits to S. palustris was
reduced by almost 50% when I. glandulifera
was present (t-test, tǃ5.171, P ǃ0.0006).
If the presence of I. glandulifera alters the
visitation behaviour of pollinators to other
plants, the fitness of these plants may also be
affected. We therefore measured seed set in
102 inflorescences (with 2,567 flowers) from
15 pure patches of S. palustris , which were at
least 500 m from the nearest I. glandulifera
stand. We compared this seed set with that
in 102 inflorescences (with 2,541 flowers)
from 11 patches in which S. palustris grew
intermixed with I. glandulifera. Seed set in
the mixed patches was reduced by 25% rela-
tive to pure patches (Fig. 1c). A chi-squared
contigency test on the frequency of flowers
with 0, 1, 2, 3 or 4 seeds yielded a highly sig-
nificant result (ȡ
2
ǃ21; d.f.ǃ4; P <0.0001).
To control for possible effects of compe-
tition for resources other than pollination,
we repeated the experiment using potted S.
palustris plants and found that, again, seed
set in plants placed in I. glandulifera patches
(mean, 2.29; s.d., DŽ1.45) was significantly
lower than in pure patches (mean, 3.2; s.d.,
DŽ1.07; ȡ
2
ǃ16; d.f.ǃ4; P ǃ0.003).
Our results show that the presence of I.
glandulifera has a strong negative effect on
the fitness of native plants, simply because it
attracts many more pollinators. As such
‘economic’ choices may be made by bees
across large foraging ranges, competitive
interactions between exotic and native
plants may take place over much larger
distances than previously thought. I. glan-
dulifera and other exotic species may reduce
the fitness of neighbouring plants even
before competition for resources other than
pollinators becomes an issue.
L. Chittka, S. Schürkens
Zoologie II, Biozentrum, Am Hubland,
D-97074 Würzburg, Germany
e-mail: chittka@biozentrum.uni-wuerzburg.de
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brief communications
NATURE | VOL 411 | 7 JUNE 2001 | www.nature.com 653
Successful invasion of a floral market
An exotic Asian plant has moved in on Europe’s river-banks by bribing pollinators.
Figure 1 Impatiens glandulifera, an Asian beauty that has con-
quered Europe’s river-banks. a, The strongly scented flowers of I.
glandulifera are extremely rich in nectar and therefore very attrac-
tive to bumblebee pollinators. Photograph by J. Bitz. b, Pollinator
visitation to Stachys palustris growing in uninterrupted patches
(left) or in patches intermingled with I. glandulifera (right). c, Effect
of the presence of I. glandulifera (right) on seed set of S. palustris
(left, uninterrupted). S. palustris normally produces up to four
seeds per flower. Error bars indicate standard deviation.
0.8
0.6
0.4
0.2
0
5
4
3
2
1
0
No. of bee visits in 10 min
No. of seeds per flower
a
b c
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