Diversity and Distributions, (Diversity Distrib.) (2004) 10, 377–385
Blackwell Publishing, Ltd.
BIODIVERSITY
RESEARCH
Latitudinal trends in growth and
phenology of the invasive alien plant
Impatiens glandulifera (Balsaminaceae)
Johannes Kollmann* and María José Bañuelos
Department of Ecology, Royal Veterinary and
Agricultural University, Rolighedsvej 21, 1958
Frederiksberg C., Denmark
*Correspondence: Johannes Kollmann,
Department of Ecology, Royal Veterinary
and Agricultural University, Rolighedsvej 21,
1958 Frederiksberg C., Denmark.
Tel.: (+ 45) 3528 2814; Fax: (+ 45) 3528 2821;
E-mail: [email protected].
ABSTRACT
Geographical differentiation of populations can be interpreted as a result of adaptive
processes in response to environmental gradients and biotic interactions. Such
adaptations are particularly interesting in invasive alien species which have been
present in an area for a relatively short time. There are few observations of latitudinal
trends in alien plants, and no account exists for Impatiens glandulifera, a problematic
annual weed in most countries of central and north-western Europe. Here we
describe variation in growth and phenology in 26 populations of this species from
nine European regions in a common garden in Denmark. Above-ground biomass
(an estimate of fecundity), height and basal diameter were lower in the northern
populations which were first to produce flowers. Some differences were also
observed in biomass allocation to leaves, flowers and fruits, albeit without a latitudinal pattern. The latitudinal trends in growth and survival disappeared in a field
experiment, probably due to suboptimal site conditions. Most variation in plant
traits was explained by differences among regions with some minor effects of
populations within regions. Besides latitude, no other geographical, climatic or
population trait correlated with the observed differences in growth and phenology.
Differences in latitude may mainly represent variation in length of the growing
season. The causes and potential consequences of such latitudinal trends for population dynamics and dispersal of alien plants are discussed.
Keywords
Above-ground biomass, annual plant, biological invasions, flowering phenology,
population differentiation.
Biological invasions are a dynamic area of current ecological
research, because they can be used to address fundamental questions in ecology and evolution of species diversity and distribution (Drake et al., 1989; Lodge, 1993; Sakai et al., 2001; Hänfling
& Kollmann, 2002; Lee, 2002). Numerous studies have focused
on global and regional patterns in plant invasions, invasibility of
different communities, differences between phylogenetic groups,
life forms of invasive plants, and mechanisms and control of
biological invasions (e.g. Pysek & Prach, 1995; Pysek, 1998; Alpert
et al., 2000; Willis & Hulme, 2002; Woitke & Dietz, 2002). In contrast, surprisingly little information is available about regional
and local adaptations of invasive plants ( but see Parker et al., 2003),
although such adaptations have been demonstrated in non-invasive
species (Li et al., 1998; Imbert et al., 1999; Galloway & Fenster,
2000; Keller et al., 2000). Small colonizing populations often
have increased rates of evolution, and that might be particularly
true in invasive alien species (Eckert et al., 1996; Lee, 2002). One
example is the European grass Bromus tectorum which shows
local adaptations along an environmental gradient from arid steppe
vegetation to subalpine forests in western North America (Rice &
Mack, 1991). In the C4 African grass, Pennisetum setaceum, on the
other hand, phenotypic plasticity was more important than local
adaptation to dominance across diverse habitats on Hawaii
( Williams et al., 1995); similar results were reported for the invasive
alien Agrostis capillaris in New Zealand ( Rapson & Wilson, 1992).
Invasive alien plants are young floristic elements in the area of
introduction, and regional and local differentiation might still be
low compared with old inhabitants of the respective communities (e.g. Keller et al., 2000). However, such adaptations may
facilitate the colonization of new habitats ( Rice & Mack, 1991),
and thus the spread of invasive species (Lee, 2002). For example,
the Himalayan Impatiens glandulifera is more frost tolerant
than European populations (Beerling & Perrins, 1993). The
absence of geographical adaptations may at least partly explain
the ‘lag’ phase of many biological invasions (Kowarik, 1995), and
understanding such lag phases is relevant for predicting the
© 2004 Blackwell Publishing Ltd www.blackwellpublishing.com/ddi
377
INTRODUCTION
J. Kollmann and M. J. Bañuelos
(Beerling & Perrins, 1993); it was introduced to Europe in 1839
(Kew Gardens), became naturalized in England around 1855,
and has experienced an exponential increase in abundance and
distribution during the past 30–40 years (Beerling, 1993). The
species is now common in the lowlands and in the lower montane
belt below 800 m a.s.l. in 19 European countries within the latitudes
30 –64° N, and in the Alps it was recently found at 1550 m (H.
Buschmann, pers. comm.). Its northern distribution seems to be
controlled by length of the growing season, and the species might
spread northwards with rising global temperatures (Beerling,
1993). It is a tall therophyte without clonal growth and no long-lived
seed bank (Grime et al., 1988), but it is still not clear whether or
not the species can have persistent seeds (K. Prach, pers. comm.).
The flowers are self-fertile albeit protandrous; seeds are dispersed
by explosive capsules, hydrochory and human transport. Large
and dense stands are common on riverbanks, waste ground and
in open moist woodlands (Demuth, 1993). Crawley (1987) considered it to be one of the ‘top twenty’ British aliens, because it is
suppressing and endangering native species. It supports relatively
few phytophagous insects, but is quite attractive to insect pollinators (Schmitz, 1995; Titze, 2000) which can lead to reduced
pollination in native plants (Chittka & Schürkens, 2001).
effects of new invasions and for management strategies. The
degree of local adaptation may depend on the matching of
climatic and edaphic conditions in the native vs. the new range of
the respective species, and on the history of immigration.
The east-Asian Impatiens glandulifera is an important invasive
alien plant in Europe (Pysek & Prach, 1995; Dawson & Holland,
1999; Weber, 2000; Peltre et al., 2002) and North America ( Toney
et al., 1998). This tall annual plant was selected for the study
because it is currently expanding its European range (Beerling,
1993), and causes problems for ecosystem management (Wadsworth
et al., 2000). As the species has been in Europe for about
150 years and covers a broad geographical range, regional adaptations may be expected, for example along latitudinal gradients.
Such geographical differentiation was found in the invasive
perennials Solidago altissima and S. gigantea (Weber & Schmid,
1998), but no account exists for annual invasive alien plants.
Potential differentiation among regions along such gradients
should be compared with variation among populations within
regions, because the relative importance of regional and local
adaptation has rarely been studied in invasive alien plants. Transplant experiments are appropriate tools to study regional and
local adaptation and they should be done in multiple sites if they
are to be relevant to management.
This study reports on a common garden experiment with 26
populations of I. glandulifera from nine European regions. The
objectives were (1) to explore variation among regions in survival, growth and phenology; (2) to analyse the partitioning of
variation among regions and among populations within regions;
and (3) to correlate variation among all populations with site and
population characteristics, including latitude.
Seed populations
For the survey of regional and local adaptations, plant material
from nine European regions was used (Tables 1 and 2). The latitudinal gradient covered a large part of the European range of the
species from N Switzerland (47°) to N Sweden (63°), and a broad
longitudinal gradient (N England, 1°, to N Sweden, 20°). In each
region, seeds were collected in 1–5 populations that were at least
1 km apart; estimated population size varied from 50 to > 10,000
plants. The sampling could not be balanced due to local differences in number and size of the populations. Habitat types
included riverbanks, lakeshores, mesic forest edges, roadsides
and abandoned gardens; most sites had no management or only
irregular mowing.
METHODS
Study species
Impatiens glandulifera Royle (Balsaminaceae; 2n = 18, 20) is
native to the Himalayan mountains from Kashmir to Garhwal
Table 1 Site and seed characteristics of the 26 populations of Impatiens glandulifera. The nine regions (nearest town in parentheses) are ordered
by latitude, and every region is represented by 1–5 populations. The grand mean of seed mass is based on 50 seeds per population; for the
germination test 60 seeds per population were used
Region [no. of populations]
Latitude N
Longitude E
Altitude (m)
AnnT (°C)
N Sweden† (Umeå) [4]
E Denmark (Copenhagen) [5]
N England‡ (Durham) [2]
E Netherlands§ (Assens) [1]
E Germany (Halle-Leipzig) [5]
W Germany¶ (Hagen) [1]
S (W*) Czech Republic††
(Ceske Budejovice) [5]
E France** (Mulhouse) [2]
N Switzerland (Zurich) [1]
63°48′−63°50′
55°41′−55°47′
54°43′−54°45′
53°00′
51°19′−51°28′
51°20′
48°58′−50°15′
20°10′−20°20′
12°28′−12°36′
−1°33′−1°52′
06°38′
11°58′−12°20′
06°32′
13°00′−14°46′
10–37
2–19
50–140
5
99–108
120
356–439
2.0
8.0
9.1–9.4
9.0
9.0
9.5
7.2–7.9
47°45′
47°23′
7°24′−7°29′
8°34′
250
569
9.8
8.0
AnnP (mm)
700
602
593–718
767
559
903
600–628
786
1137
Seed mass (mg)
Germination (%)
11.9
12.1
19.0
10.8
13.8
13.5
15.2
68
83
92
76
88
58
80
16.5
19.1
58
82
*One population from Karlovy Vary in W Czech Republic. Sources of the climatic data: †Umeå, C. Nilsson, pers. comm.; ‡Durham, S.G. Willis, pers.
comm.; §Eelde; ¶Hagen and **Eimeldingen, Mühr (2003); ††Ceske Budejovice, K. Prach, pers. comm.; all others Rudloff (1981). AnnT, mean annual
temperature; and AnnP, mean annual precipitation.
378
Diversity and Distributions, 10, 377–385, © 2004 Blackwell Publishing Ltd
Latitudinal trends in growth and phenology of an annual invasive plant
Table 2 Site and population characteristics of the 19 populations of Impatiens glandulifera used to study partitioning of variation among
regions and among populations within regions. Population numbers refer to Table 3
Region
Population (No.)
Lat. N, Long. E
Altitude (m)
Habitat type
Population size
N Sweden
Baggböle (1)
Tomtebo (2)
Röbäck (3)
Sandbacka (4)
Bagværd Sø (1)
Lyngby Sø (2)
Hundesø (3)
Utterslev Mose (4)
Christianshavn (5)
Grosszschocher (1)
Altlindenau (2)
Burgholz (3)
Rabeninsel (4)
Preisnitz (5)
Ceske Budejovice (1)
Karlovy Vary (2)†
Ceske Budejovice (3)
Trebon (4)
Trebon (5)
63°50′,
63°48′,
63°50′,
63°50′,
55°46′,
55°47′,
55°46′,
55°43′,
55°41′,
51°18′,
51°20′,
51°28′,
51°28′,
51°28′,
49°00′,
50°15′,
48°58′,
49°01′,
49°00′,
35
37
10
25
18
18
17
19
2
108
104
102
100
99
374
356
380
439
430
Mesic roadside
Garden waste
Mesic roadside
Mesic park
Lakeshore
Lakeshore
Lakeshore
Swamp margin
Swamp margin
Riverbank
Riverbank
Riverbank
Riverbank
Riverbank
Riverbank
Riverbank
Riverbank
Pond margin
Riverbank
c. 200
c. 50
> 200
50 –75
1000 –5000
100 –200
> 10,000
30 –40
200 –300
> 1000
> 10,000
c. 10,000
c. 1000
200
> 1000*
> 1000*
> 1000*
> 1000*
> 1000*
E Denmark
E Germany
S (W) Czech Republic
20°10′
20°20′
20°13′
20°17′
12°28′
12°30′
12°33′
12°30′
12°36′
12°20′
12°20′
11°58′
11°58′
11°58′
14°27′
13°00′
14°27′
14°44′
14°46′
*Continuous populations along the riverbanks, †W Czech Republic.
Seeds were collected from 10 to 25 plants per population
(5–10 seeds per plant) in September–October 2001. Only ripe
capsules with brown or black seeds were harvested; unusually small
or empty seeds were discarded. We dried the seeds at room temperature for 1–2 weeks and stored them at 0 –5 °C for 5 months.
Seed mass was determined for five groups of 10 seeds per
population after drying at room temperature for 10 weeks. Seed
mass was negatively correlated with latitude (r 2 = 0.24, n = 25,
P = 0.01; Table 1).
Germination and growth conditions
In late March, seeds from all populations were put between moist
blotting paper in Petri dishes at 0–5 °C for a 3-week period of
stratification; a fungicide (1% Dithane M45) was added to
reduce fungal infections. At the end of this period some seeds
had already started germinating. Sixty seeds of each population
were laid out in transparent plastic boxes (12 × 8 × 5 cm3) with
blotting paper over a plastic bridge and 100 mL distilled water
(plus fungicide). The boxes were randomly placed and daily rearranged in a germination cupboard with a temperature regime of
12 °C at night (12 h), and 22 °C with light during daytime
(12 h). The experiment was terminated after 47 days as most
seeds had germinated in the first week. Germination was high in
all populations (58 –92%) and independent of latitude (r 2 = 0.008,
n = 26, P = 0.69; Table 1).
In mid April, 20 seedlings of each population were transferred
to a glasshouse and planted into plastic trays with individual
wells (5 cm diameter, 6 cm depth) filled with a peat-based substrate (N, 74 g m−3; P, 165 g m−3, K, 260 g m−3; pH 6.0); once a
Diversity and Distributions, 10, 377–385, © 2004 Blackwell Publishing Ltd
week the position of the trays was randomised. After 3 weeks
we transferred the plants to larger pots (12 cm diameter, 10 cm
depth) with the same substrate. Average day temperatures in the
glasshouse were 21.6 ± 0.8 °C (mean ± SE) with 77.6 ± 2.1% air
humidity and 10.0 ± 1.0 klux light (one record min−1). Nocturnal
values were 17.6 ± 0.4 °C, 83.4 ± 1.7% humidity and 1.7 ± 0.3
klux light.
In early June, eight randomly chosen individuals of each
population were placed outdoors for hardening before planting
into the common garden at the Royal Veterinary and Agricultural
University (55°41′ N, 12°33′ E). One week later one plant of each
population (total 130, cf. Tables 1 and 2) was planted randomly
in five double rows with two guard plants on both ends of the
rows (total 20 guard plants); the latter were excluded from the
analysis. The rows were N–S orientated, with 40–50 cm distance
between the plants within rows and 80–100 cm between rows,
and after about 4 weeks a closed canopy had developed. The
experimental plot was not shaded but slightly protected against
wind by adjacent buildings. Mean daytime temperatures were
19.9 ± 0.4 °C and light averaged 283.9 ± 14.3 W m−2; nocturnal
values were 17.1 ± 0.3 °C and 45.3 ± 6.3 W m−2 light (one record
min−1). The loamy soil had been tilled twice before planting, but
neither fertiliser nor herbicides were applied and water only
added when necessary. Little weeding was done because of rapid
growth of the study plants, which prevented other species from
establishing. Few herbivores were observed, except black aphids
on 4–6 individuals in late June albeit without a clear pattern
regarding populations or rows.
In late May, a second batch of plants from the same populations was planted with identical design in an experimental field
379
J. Kollmann and M. J. Bañuelos
at the university farm west of Copenhagen (55°40′ N, 12°19′ E).
As the plants were already 20 –35 cm tall and not sufficiently
robust, they were clipped just above the second node to reduce
initial mortality. The loamy moraine soil was tilled before planting
but otherwise no management occurred. Because this site was
more exposed to wind and neither watering nor weeding was done,
the growth conditions were harsher than in the common garden.
Plant measurements
In mid August, all plants were harvested in the common garden
at ground level; harvest of the root system was not feasible as the
species has fragile roots. At this time all plants were 4 months
old, had abundant flowers and fruits and showed no signs of
senescence. On fresh material we measured plant height and circumference at the second basal internode, whereas the number
of flowers and fruits could not be quantified because of their
ephemeral nature and continuous production. Because of the
quantity of material, plants had to be predried at 20 – 40 °C for
12 days in a glasshouse, followed by 3 days at 70 °C in a drying
oven. Biomass was determined separately for stems and branches
vs. leaves, flowers and fruits. We also recorded the date of first
flowering of all plants based on daily observations.
In the field experiment, no phenological records were done
but survival was monitored. All surviving plants were harvested
in late July, and above-ground biomass was determined after
3 days drying at 70 °C.
production were abundant. At harvest in mid August, aboveground biomass (ANOVA; F8,36 = 4.75, P < 0.001), plant height
(F8,36 = 5.91, P < 0.001), basal diameter (F8,36 = 6.83, P < 0.0001)
and time till flowering (F8,36 = 20.3, P < 0.001) were significantly
different among the nine European regions. No regional differences
occurred in relative allocation to leaves, flowers and fruits compared with total above-ground biomass (F8,36 = 2.56, P = 0.10).
In the field experiment, 17% mortality was observed after
1 week, and about 50% of the plants were dead after 2 weeks. At
harvest in late July, 34% of the plants had survived, with large differences among populations. Partly due to the initial clipping
most plants were rather small (93 ± 2 cm, mean ± SE) and highly
branched; the leaves were reddish and wrinkled, and flowering
and fruiting were low. Above-ground biomass (27.4 ± 1.9 g;
n = 55) was much less than that of the common garden experiment (73.7 ± 2.6 g; n = 140).
Partitioning of variation in growth and phenology
In the nested ANOVA most variation in above-ground biomass,
plant height and time till flowering was explained by differences
among regions (96–98%, Tables 3 and 4). The effect of populations within region was only significant for time till flowering,
but even so 98% of the variance was due to regional effects. No
differences among regions were observed in relative biomass of
leaves, flowers and fruits (F3,76 = 0.64, P > 0.05), but about 36%
of trait variance was explained by differences among populations
within regions (F15,76 = 3.8, P < 0.004).
Statistical analyses
We first explored regional variation in all plant traits by means of
one-way ANOVAs irrespective of the latitudinal gradient. For
this analysis we considered one randomly selected population
per region with five plants, respectively, because the full data set
of all populations was not balanced (cf. Table 1). To investigate
partitioning of variation among regions and among populations
within regions (five plants per population), nested ANOVAs
were calculated for five populations from the Czech Republic,
Denmark and Germany, respectively, and four from Sweden, considering region (fixed factor) and population (random factor) as
main effects (cf. Table 2). The four regions represented the total
length of the latitudinal European gradient. Population means of
all 26 populations were then correlated with the most important
site and population characteristics, including latitude. In the
multiple ANOVAs or regression analyses the P-values were
Bonferroni corrected to avoid Type I errors. All proportional data
were arcsine transformed and the other measurements log transformed in case of deviation from normality of the residuals and/
or unequal variance. All statistical analyses followed Zar (1999).
RESULTS
Correlation with site and population traits
In the common garden experiment, the differences between
regions in above-ground biomass, plant height and time till flowering followed a clear latitudinal gradient with lower values in
the northern populations (r 2 = 0.36–0.63, P < 0.02; Fig. 1). The
Swedish, Danish and English plants had about half the biomass
compared with plants from the Swiss, Czech and French populations. Time till flowering was about 10–15 days shorter in the
northern populations.
Latitude was correlated with some of the site variables, for
example, average annual temperature, minimum temperature and
elevation (P < 0.02). Therefore, we did not calculate correlations
with these variables as the results would not be independent. No
other regional or local factor, including maximum temperature,
annual precipitation and population size, showed any relationship with the measured plant traits (r 2 = 0.22, P > 0.32).
In the field experiment, the differences among the nine European regions in plant survival (r 2 = 0.01, P > 0.05) and biomass
revealed no significant latitudinal pattern (r 2 = 0.05, P > 0.05).
Because of the high mortality all plants per region were pooled
for this analysis.
Plant survival, growth and phenology
DISCUSSION
All transplants of Impatiens glandulifera survived in the common
garden experiment, and vegetative growth, flowering and fruit
This is one of the first reports on latitudinal trends in growth and
flowering phenology of an invasive alien annual plant, showing a
380
Diversity and Distributions, 10, 377–385, © 2004 Blackwell Publishing Ltd
Latitudinal trends in growth and phenology of an annual invasive plant
Table 3 Means of vegetative and reproductive traits in populations of Impatiens glandulifera in the common garden experiment (means ± SE).
Significant differences among populations within regions are indicated by superscript letters (Tukey posthoc test, P < 0.05); for statistical
differences among regions see Table 4. The regions are ordered by decreasing latitude, and populations within regions by decreasing values in
above-ground biomass. Population numbers are explained in Table 2
Population number
1
Above-ground biomass (g)
N Sweden
E Denmark
E Germany
S (W) Czech Republic
2
46.8 ± 3.2
97.2 ± 22.9
99.8 ± 23.7
97.0 ± 22.1
Height (cm)
N Sweden
E Denmark
E Germany
S (W) Czech Republic
147.2 ± 3.9
192.6 ± 9.9
184.8 ± 7.3
177.0 ± 7.5
Time till flowering (days)
N Sweden
E Denmark
E Germany
S (W) Czech Republic
3
44.1 ± 10.6
70.8 ± 7.6
87.9 ± 11.3
87.3 ± 10.3
131.4 ± 9.3
176.0 ± 3.4
192.4 ± 6.4
178.2 ± 8.8
74.4 ± 2.6
87.0 ± 2.4ab
86.4 ± 1.3
86.8 ± 1.7
64.8 ± 1.3
86.2 ± 2.0ab
92.0 ± 2.1
85.8 ± 3.0
4
5
37.7 ± 2.9
62.9 ± 9.0
76.8 ± 10.5
82.7 ± 6.1
33.7 ± 5.2
55.7 ± 8.1
65.4 ± 8.2
79.1 ± 10.7
—
51.4 ± 2.8
63.4 ± 3.5
71.1 ± 14.5
140.4 ± 11.5
177.0 ± 9.9
171.2 ± 3.4
177.8 ± 12.6
151.8 ± 12.1
186.4 ± 9.9
172.4 ± 9.1
170.2 ± 6.9
—
176.8 ± 4.7
200.0 ± 3.3
147.4 ± 6.3
72.4 ± 1.4
78.4 ± 1.2a
93.0 ± 3.3
89.6 ± 1.0
69.4 ± 0.5
84.2 ± 3.8ab
87.0 ± 1.4
83.2 ± 1.1
—
92.8 ± 2.9b
89.8 ± 0.8
82.8 ± 4.3
— No data available.
Table 4 Relative effect of region and population within region on
vegetative and reproductive traits of Impatiens glandulifera in the
common garden experiment. Results of nested ANOVAs, including
variance are explained by the two hierarchical levels (data log
transformed, significant results bold). For mean values per
population see Table 3
Source of variation
df
Above-ground biomass
Region
Population (Region)
Error
3
15
76
Plant height
Region
Population (Region)
Error
Time till flowering
Region
Population (Region)
Error
MS
Explained
variance (%)
F
P
4.27
0.26
0.20
15.89
1.29
< 0.004
0.88
95.5
0
4.47
3
15
76
5.86
0.39
0.23
14.86
1.66
< 0.004
0.28
96.1
0
3.91
3
15
76
47.59
2.14
0.67
22.28
3.18
< 0.004
< 0.04
98.0
0.59
1.35
increase in size and time till flowering for southern populations
in a common garden experiment. Similar latitudinal patterns in
growth have been observed in the invasive alien biennials Verbascum thapsus and Daucus carota in North America (Reinartz,
1984; Lacey, 1988) and in the invasive alien perennials Solidago
altissima and S. gigantea in Europe (Weber & Schmid, 1998), but
also in native populations of Arabidopsis thaliana (Li et al., 1998)
and Lythrum salicaria (Olsson & Ågren, 2002; Bastlová & Kvet,
Diversity and Distributions, 10, 377–385, © 2004 Blackwell Publishing Ltd
2003). In biennials and perennials the pre-reproductive period is
often longer for plants from high latitudes (Lacey, 1988), whereas
the opposite could be true for annuals where reproduction must
be completed within one growing season. Reciprocal transplant
experiments would be necessary to prove this hypothesis.
Most of the above studies used only one transplant site which
is unfortunate since the results can change depending on site
conditions. Even better would be reciprocal transplant experiments among natural populations which could help to assess
more precisely the degree of regional and local adaptation along
the geographical gradient (Lacey, 1988; Rice & Mack, 1991).
Obviously, such experiments are prohibitive in invasive plants as
they may hybridize and spread if not done in common gardens
(Parker et al., 2003). In our study the latitudinal patterns disappeared in the arable field which was apparently less suitable for I.
glandulifera because of episodic drought and windy conditions
which are unusual in natural populations of the species (Demuth,
1993). However, the same latitudinal patterns of growth and
phenology as in the common garden were also observed in a
greenhouse experiment where conditions were milder than in
natural populations (J. Kollmann, unpublished data).
The variation of plant traits among and within regions helps
to understand the main result of clinal variation in I. glandulifera.
Because variation among regions was markedly higher than
variation within regions, the latitudinal trends in growth and
flowering may largely be interpreted as adaptation to length of
the growing season. No other site and population characteristic
correlated with plant performance. Willis & Hulme (2002) showed
that the altitudinal limit of I. glandulifera is determined by temperature, as transplants were smaller and produced fewer seeds
with increasing elevation; maximum height and pod production
in this study were correlated with increasing postemergence heat
381
J. Kollmann and M. J. Bañuelos
Figure 1 Latitudinal trends in above-ground biomass, plant height
and time till flowering in 26 populations of Impatiens glandulifera
from nine European regions (mean values from five plants per
population). Results of a common garden experiment at latitude
55°41′ N; for origin of the populations see Table 1 (*P < 0.05).
382
sum (i.e. degree days > 5 °C). The factors explaining altitudinal
variation may be similar for the latitudinal gradient reported in
our study. Bastlová & Kvet (2003) also found higher variability
among than within regions in 10 (of 12) above-ground traits of
Lythrum salicaria. These authors observed higher variability
within regions only for 2 (of 2) root traits, which might be less
dependent on variation of the growing season and more on local
conditions. As a next step, native east-Asian populations of
I. glandulifera should now be investigated, because it is often
observed that plants differ in their native and in the introduced
range (Bastlová & Kvet, 2002; Keane & Crawley, 2002; Jakobs
et al., 2004).
Lower plant biomass in the northern populations may reduce
the competitive ability of I. glandulifera in case of transfer to central Europe, because high competitiveness is a key factor for
the success of the species in central European floodplains and
lakeshores (Demuth, 1993). In these moist and relatively nutrientrich sites other tall herbs (e.g. Epilobium hirsutum, Phalaris
arundinacea, Urtica dioica) may outcompete small-statured
genotypes of I. glandulifera (Tickner et al., 2001). This should lead
to lower fecundity of these plants, as above-ground biomass and
seed production are often correlated in annual species (Primack,
1979; Thompson et al., 1991). However, many plant species
do not show linear relationships between size and fecundity
(Samson & Werk, 1986; Aarssen & Taylor, 1992), and so far no
information is available for I. glandulifera. Plant size has also
been found to be critical for determining whether plants
reproduce at all, and many species have a minimum threshold
size before flowering (Weiner, 1988; Klinkhamer et al., 1992),
although not so much in annuals. In fact, none of the populations in our study remained under this threshold, and flowering
has been observed even in individuals only 5 cm tall (K. Prach,
pers. comm.).
Southern populations transferred to northern sites, on the
other hand, flower late in the face of a short growing season.
Further experiments are needed to predict more details of
population- and site-specific reproductive success, because lateflowering individuals achieved a larger size before flowering and
consequently possessed more resources for seed production, as
observed in Prunella vulgaris by Winn & Gross (1993). Unfortunately, flower and fruit production could not be quantified in the
present study. Seed production must be a key factor for population dynamics of I. glandulifera as this annual species develops no
seed or seedling bank (Beerling & Perrins, 1993).
As I. glandulifera has been in Europe for about 150 years,
many generations could have been involved in potential adaptations to the length of the growing season. However, the species
might be a more recent invader in some parts of its current
European range, but no precise information exists about its exact
dispersal history. Genotypic changes in height and timing of
flowering are relatively fast and often correlated because growth
is markedly reduced with onset of flowering. Recent research in
the annual weed Capsella bursa-pastoris revealed that only a few
genes are involved in flowering time, which is an important trait
for colonizing different habitats (Linde et al., 2001). Genotypes
flowering too late or too early at a certain latitude will most likely
Diversity and Distributions, 10, 377–385, © 2004 Blackwell Publishing Ltd
Latitudinal trends in growth and phenology of an annual invasive plant
produce fewer seeds and thus are negatively selected (O’Neil,
1999). Regional adaptation to differences in photoperiod has
been shown in a number of native non-invasive species, e.g.
Cardamine flexuosa (Kudoh et al., 1995) and Arabidopsis thaliana
(Pollard et al., 2001) but more rarely in invasive alien plants
(Weber & Schmid, 1998). We suspect that the observed variation
in growth and phenology is genetically based and correlated with
ecophysiological requirements for flower initiation.
An important limitation of our study is that maternal effects
could not be excluded (cf. Olsson & Ågren, 2002). Seed mass
(albeit not germination) was significantly different among
regions and showed a clear latitudinal gradient, and thus, at least
some differences in growth and flower initiation could actually
be related to initial seed size. Seeds from northern populations
might be smaller due to less favourable growth conditions, in
contrast to observations in Prunella vulgaris (Winn & Gross,
1993). Although we cannot tell whether or not variation in seed
mass and plant performance are the result of different genotypes
or phenotypic plasticity (cf. Winn & Gross, 1993), they will
translate into differential reproductive output in case of largedistance seed dispersal as in the study by Keller et al. (2000).
Impatiens glandulifera is a major problem for habitat management in Europe, because of the associated economic costs and
because of local extinction of native species. Control is difficult,
and suitable management strategies are still lacking for many
habitat types (Dawson & Holland, 1999; Wadsworth et al., 2000;
Shaw, 2003). Due to increasing mobility, new genotypes are likely
to be introduced and spread within Europe, and at least some
will become invasive. So far, most management plans ignore
regional and local differentiation of populations which could
reduce, for example the success of biological control. In addition,
mowing regimes need to be adapted to the flowering phenology
of the respective genotype. Regionally adapted populations may
be dispersed due to increasing human transport, and dispersal of
such genotypes could result in the formation of new hybrids with
increased invasiveness (Nagy, 1997; Vilà & D’Antonio, 1998).
These topics should be targeted by future research initiatives
(cf. Rice & Emery, 2003).
ACKNOWLEDGEMENTS
Our thanks go to Christer Nilsson, Dani Prati, Dick Pegtel, Ewald
Weber, Gabi Jakobs, Harald Auge, Karel Prach and Steve Willis
for supplying local seed material. Anne Jind, Elze Astrup,
Kristine Rasmussen and Mads Nielsen helped with the set up,
maintenance and harvest of the experiments. The study was
supported by grant 21-03-0204 of the Danish Research Agency to
JK; MJB received a postdoctoral fellowship from the Ministerio
de Educación, Cultura y Deporte, Spain (EX2002-0028).
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