Aquatic Botany 69 (2001) 89–108
Geographic variation in growth responses in
Phragmites australis
Olga A. Clevering a,∗ , Hans Brix b , Jaroslava Lukavská c
a
c
Department of Plant Population Biology, Netherlands Institute of Ecology,
P.O. Box 40, 6666 ZG Heteren, The Netherlands
b Department of Plant Ecology, University of Aarhus, Nordlandsvej 68, DK-8240 Risskov, Denmark
Section of Plant Ecology, Institute of Botany (CAS), Dukelská 145, CZ-37982 Třeboň, Czech Republic
Abstract
Phragmites australis is a cosmopolitan wetlands species occurring in a wide range of climatic
habitats. It can be assumed that adaptations to climate have evolved to enable the synchronization
of growth with the seasonality of the environment. To study these adaptations, European P. australis
was collected in different geographic regions, and grown in common environments situated in the
Czech Republic, Denmark and The Netherlands.
Phragmites australis originating from higher latitudes showed higher relative length growth
rates (RLGR), and flowered earlier in time than that from lower latitudes. Plants from Spain even
continued growth until the first autumn frosts. When grown in the different common environments,
population differences were found in RLGR, but no general trend was apparent. On average, shoots
started to grow 2 weeks earlier in The Netherlands than in Denmark and 6 weeks earlier than in
the Czech Republic. These differences could be largely related to lower spring temperatures in the
latter two countries. When shoot-growth was plotted against the temperature sum, no differences in
RLGR between Denmark and The Netherlands were apparent, whereas shoot-growth was slower
in the Czech Republic.
Results from a greenhouse experiment showed that seedlings from southern populations formed
taller but fewer shoots and thicker but shorter rhizomes than those from northern populations,
irrespective of total dry weight. They also allocated more dry matter to stems at the expense of
leaves, whereas no differences in allocation to below-ground plant parts were found.
It was concluded that populations of P. australis showed clinal variation in (i) the length of the
growing season, (ii) time of flowering, and (iii) morphology and biomass allocation. These results
∗ Corresponding author. Present address: Applied research for Arable farming and Field Production of
Vegetables. P.O. Box 430, 8200 AK Lolystad, The Netherlands. Tel.: +31-320-291673; fax: +31-320-230479.
E-mail addresses: [email protected], [email protected] (O.A. Clevering).
0304-3770/01/$ – see front matter © 2001 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 3 7 7 0 ( 0 1 ) 0 0 1 3 2 - 2
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O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
are discussed with respect to the possible effects of global warming on population functioning.
© 2001 Elsevier Science B.V. All rights reserved.
Keywords: Cline; Latitudinal gradient; Relative length growth rate; Flowering time; Morphology; Biomass
allocation; Phragmites australis
1. Introduction
Along a latitudinal gradient, plant species have to cope with gradually changing climatic
conditions in (i) the amount of solar radiation, (ii) contrasts between seasons, and (iii) relative day lengths. Although the annual mean value of day-length remains constant across
latitudes, the annual mean values of both the cumulative daily radiation and air temperature
decrease approximately linearly with increasing latitude (Charles-Edwards, 1982). Across
longitudes, seasonal and diurnal cycles in temperature and radiation may differ widely
between oceanic and continental habitats. Generally, oceanic habitats show smaller differences in summer and winter temperatures than continental habitats. Furthermore, oceanic
habitats typically have a higher proportion of overcast days, resulting in lower radiation
than in more continental habitats (Bannister, 1976).
It can be assumed that genetic variation has arisen in the synchronization of growth with
the diurnal and seasonal periodicities of the environment. For a large number of species
evidence for genetic variation has been found in (i) growth form, (ii) timing and length of the
growing season, and (iii) physiological adaptations (cf. Clausen et al., 1948; McNaughton,
1966, 1975; Clapham, 1998; Li et al., 1998). Generally, plants from higher latitudes are
more prostrate with a shorter length of the pre-flowering period than those from lower
latitudes (Li et al., 1998). Plants from higher latitudes often show a specialized form of
shading response, because of the combination of relatively low irradiation and enhanced
far-red ratios in higher as compared to lower latitudes (Hay, 1990). As a consequence
of low temperatures also soil nutrient cycling proceeds more slowly in higher latitudes,
which may result in more nutrient-stress tolerant plants in higher than in lower latitudes
(Chapin and Chapin, 1981). Not in all traits, clear or consistent patterns have been found
along latitudinal gradients. For example, the amount of variation found in seed size, relative
growth rates (RGR), biomass allocation patterns and plasticity in relation to climate differ
widely among species (Reinartz, 1984; Counts, 1993; Winn and Gross, 1993; Zhang and
Lechowicz, 1994; Li et al., 1998). These differences in adaptations are probably related to
differences in longevity and/or in strategies to cope with harsh winters and/or summers.
Phragmites australis (Cav.) Trin. ex Steud. is a cosmopolitan clonal species, occurring
in a wide range of climatic habitats. In the Northern hemisphere, the species occurs in both
oceanic and continental climates at latitudes between 70◦ N and the tropics (Haslam, 1972;
Clevering and Lissner, 1999). It is often the key-species in wetland ecosystems. In the last
decades, the species is dying back in many parts of Europe due to the interactive effects
of different man-induced environmental changes (cf. Van der Putten, 1997; Brix, 1999).
In the EU-project “Eureed” (Brix, 1999), we tried to predict the consequences of climatic
changes on the growth dynamics and stability of P. australis dominated wetlands. Because
of the slow turnover of clones, P. australis populations might be poorly adapted to changing
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91
climatic conditions (Callaghan et al., 1992; Chapin et al., 1993; Clevering, 1999; Clevering
and Lissner, 1999). In the present study, we wanted to elucidate some aspects of genetic
adaptations of P. australis to climate. Topics addressed are (i) timing of shoot growth and
panicle appearance, (ii) shoot growth rates and morphology, and (iii) seedling traits of P.
australis from different geographic origins.
2. Materials and methods
2.1. Populations
The selected populations occur along a latitudinal gradient from North Sweden to Spain.
They originated from both oceanic and continental climates (Table 1). Rhizomes and seeds
were collected between autumn 1995 and spring 1996. Except for the North Swedish population, sampling occurred in two transects of 500 m length with intervals of 50 m: one along
the open water and one along the succeeding terrestrial vegetation. This sampling scheme
was designed for a study on within-population differences (Clevering, 1999). Rhizome
material from the North Swedish population was collected randomly in an area of 1 ha.
After collection, rhizome-buds were sprouted in a heated greenhouse, and after sprouting
planted in 65 l. (diameter 60 cm; height 30 cm) containers in the experimental garden in
Heteren, The Netherlands. In each container, a single rhizome with sprouted buds was
planted in a mixture of unsorted river sand and peat (2:1 v/v). The substrate was kept
waterlogged using ground water. Clones were identified using random polymorphic DNA
(RAPD) and ploidy levels using flow cytometry. See Clevering (1999) and Clevering and
Lissner (1999) for results.
2.2. Experimental design
2.2.1. Transplantation experiment: shoot growth traits
Populations used in this study are shown in Table 1. Although we assumed that no
within-population differences in adaptations to climate would be apparent, we randomly
selected three clones from both the landward and waterward side of each population. The
North Swedish population consisted of four clones only.
Between April and June 1997, rhizomes with buds from a maximum number of six clones
per population were sent to Aarhus (Denmark), and Třeboň (Czech Republic), and were
re-planted in Heteren (The Netherlands). Since, flow cytometry did not become available
before the summer of 1997, we only discovered after sending rhizome material to the
different countries that the Romanian clones consisted of five octo- and one hexaploid,
whereas all other populations were tetraploid (Clevering, 1999). To allow for a comparison
between ploidy-levels, we grew six tetraploid Romanian clones in The Netherlands as well.
The North Swedish (due to a shortage in plant material) and the Danish (due to shortage in
personnel) population were not grown in the Czech Republic.
Clones were planted in unsorted river sand in similar containers as described above. The
substrate was kept waterlogged. Clones were fertilized bi-weekly during the growing season
of 1997, and weekly during the growing season of 1998, using 100 ml of a solution with
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10 g Macro nutrients (NPK 19-5-19+MgO) and trace-elements (Brøste, Lyngby Denmark).
The containers were placed in a randomized block design with the six clones per population
used as replicates.
In autumn 1997, shoot die-off was determined in Denmark and The Netherlands by counting the number of live leaves (i.e. leaf-blades with an area of >50% green tissue) of five shoots
per clone, bi-weekly. Counting commenced at the time of flowering or in non-flowering
shoots at the time of maximum shoot-length, and continued until all leaves had turned yellow.
In 1998, shoot-lengths were measured weekly or bi-weekly of five shoots per clone. Also
the time of panicle appearance was recorded. Autumn shoot die-off was recorded in the
Czech Republic and The Netherlands as described for 1997. After all shoots had died off,
the total number of shoots per container was recorded. In Denmark and The Netherlands,
lengths, diameters, and numbers of nodes were determined of the five longest shoots of
each clone.
Additionally, in The Netherlands, time of panicle appearance was recorded for all populations, including those not used in this shoot-growth experiment (Table 1).
2.2.2. Greenhouse experiment: seed size and seedling traits
In this study, we reanalyzed data from an earlier study on between- and within-population
differences in 10-week-old seedlings of P. australis (Clevering, 1999). Here we focussed
on latitudinal differences in seed size and seedling traits. The experimental design, and the
determination of seed size and seedling traits have been described in detail in Clevering
(1999). Contrary to Clevering (1999), we included the Dutch population (Table 1), and
separated the Romanian seedlings into tetra- and octoploids. In this study, we used data
of seedlings grown under optimal nutrient conditions only. Because, only six Romanian
tetraploid seedlings were present, we also randomly selected six seedlings (three from
the waterward and three from the landward side) in the other populations. The following
seedling traits were determined: (i) total dry weight, (ii) dry matter allocation to leaves,
stems with leaf-sheaths, rhizomes, and roots, (iii) leaf area ratio (LAR) and specific leaf
area (SLA), (iv) number of shoots and rhizomes, (v) length and diameter of the second
shoot, (vi) total rhizome length, specific rhizome length (SRL), and the diameter of the
second node of the first horizontal rhizome.
2.3. Data analyses and statistics
Lengths of five shoots per clone were plotted against time and temperature sum. The
temperature sum was used, because we expected that the onset of growth and relative shoot
length growth rates (RLGRs) were largely depended on the temperature in the different
common environments (cf. Goudriaan and Van Laar, 1994). The temperature sum was
calculated as the integral of the value with which the (average) temperature exceeds a
certain lower threshold (Goudriaan and Van Laar, 1994). Because this threshold level is not
known for P. australis, we used an arbitrary level of 5◦ C.
Per shoot, a logistic growth curve was fitted to the lengths recorded on the different census
days or ◦ C-days
Lt =
Lmax
1 + e−RLGR(xt −xmean )
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where Lt is the length at day or ◦ C-day t, Lmax the asymptotic maximum length, RLGR the
relative length growth rate per day or ◦ C-day, xt the time in days or ◦ C-days and xmean the
time in days or ◦ C-days when length growth is half way. Also mortality of leaves was fitted
against time in days using a logistic growth curve.
Data of the shoot-growth and shoot-morphology study were analyzed according to a
randomized block design with blocks nested within common environments, using SASprocedure GLM (SAS Institute, 1990). Prior to ANOVA, mean values of five shoots per
clone (replicate) were calculated, and data were tested for normality using Cochrans Q-test.
No statistics were applied on time of panicle appearance, because of heterogeneity of
variances. ANOVA was carried out with clones raised in Denmark and The Netherlands
only, because the South Swedish and Spanish clones grew poorly in the Czech Republic.
This poor growth was largely related to propagation difficulties rather than to climate. After
ANOVA, significant differences were calculated (i) between populations within the same
common environment, and (ii) between common environments for the same population
using the LSD-method (P < 0.05). Within common environments, Pearson correlations
were calculated between the latitude of origin of the populations and shoot characteristics.
To avoid confounding effects with ploidy-level, the Romanian octoploids were omitted from
all Pearson correlation analyses.
The mean time of panicle appearance was calculated for all populations grown in The
Netherlands. In the case of the non-flowering North Swedish population, the mean time
of length-growth cessation was recorded. Because the number of flowering clones differed
greatly between populations, Pearson correlations were calculated between latitude of origin
and mean date of panicle appearance.
Finally, seed size and seedling traits were correlated with the latitude of origin, omitting
the Romanian octoploids. Traits of seedlings were corrected for differences in total dry
weight. ANOVA was used to compare traits of Romanian octoploids and tetraploids.
3. Results
3.1. Climate of the native habitats and common environments
Between the sites of origin of the populations, large differences exist in temperature and
day-length (Table 1). In Spain, P. australis experiences relative short days with high temperatures, whereas in North Sweden it grows in long days with low temperatures. Oceanic
climates have mild summers and winters, while continental climates have relatively cold
winters and hot summers (Table 1).
In 1998, the Dutch common environment showed the highest mean temperature
(Table 1; Fig. 1A). The more continental character of the Czech climate was reflected
in lower winter but higher summer temperatures than the oceanic Danish and Dutch climate. The temperature- and radiation-sum were calculated from the point of time growth
started (Fig. 2A and B). Both were lower in Denmark than in The Netherlands. However,
the daily increase did not differ between these two countries. In the Czech Republic, sums
increased more rapidly during the first part of the growing season, at the end of the growing
season, however, this increase proceeded more slowly than in the other two countries.
O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
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Fig. 1. (A) Monthly mean temperatures of the common environments in Denmark (Dk), The Netherlands (Nl),
and the Czech Republic (Cz) in 1998. (B) Temperature and (C) radiation sums in these common environments
calculated from the day shoot-growth started. Start of shoot-growth was set at day 105, 83, and 125, respectively
for Denmark, The Netherlands, and the Czech Republic (see also Fig. 2A).
3.2. Transplantation experiment
3.2.1. Shoot growth parameters
Results of the calculated parameters of the logistic growth curves showed that, a common
environment by population interaction affected the asymptotic maximum length of shoots
(Table 2A). A common environment by population interaction affected also the relative
length growth rate (RLGR) per day, whereas that per ◦ C-day differed only between populations. Midpoint of length-growth based on both days and ◦ C-days differed independently
between common environments and populations (Table 2A).
On average, growth commenced 3 weeks earlier in The Netherlands than in Denmark
and 6 weeks earlier than in the Czech Republic (approximately day 83, 105 and 125,
respectively) (Fig. 2A). These differences were largely reflected in differences in midpoint of length-growth (Table 3). The Dutch and Romanian populations reached similar
shoot-lengths when grown in Denmark and The Netherlands, shoots of all other
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97
Table 2
F-values and significances of a GLM-procedure applied on shoot characteristics of P. australis populations grown
in common environments in Denmark and The Netherlandsa
Common
environment (c)
Population (p)
c×p
MS-error
(A) Shoot growth parameters
d.f.
(5/r)
Final length
0.9 ns
RLGR (day)
0.4 ns
RLGR (◦ C-day)
1.6 ns
Midpoint (day)
1.1 ns
Midpoint (◦ C-day)
0.7 ns
(1/10)
40.9∗∗∗
2.3 ns
2.9 ns
213.5∗∗∗
31.7∗∗
(6/r)
44.3∗∗∗
43.1∗∗∗
24.9∗∗∗
37.9∗∗∗
15.1∗∗∗
(6/r)
6.4∗∗∗
3.3∗∗
0.8 ns
0.7 ns
0.8 ns
r = 52
0.39
2.6 × 10−3
3.6 × 10−6
3.1 × 10−2
3.3
(B) Leaf mortality parameters
d.f.
(5/r)
RLMR (day)
1.9 ns
Midpoint (day)
1.4 ns
(1/10)
13.6∗∗
11.9∗∗
(6/r)
13.0∗∗∗
24.1∗∗∗
(6/r)
3.4∗∗
9.0∗∗∗
r = 53
0.11
0.02
(C) Morphology of the longest shoots
d.f.
(5/r)
Length
1.3 ns
Diameter
1.1 ns
No. of nodes
1.2 ns
Internode-length
0.5 ns
(1/10)
21.8∗∗
0.9 ns
34.1∗∗∗
7.5∗
(5/r)
73.5∗∗∗
87.5∗∗∗
22.3∗∗∗
6.5∗∗∗
(5/r)
8.1∗∗∗
4.2∗∗
4.4∗∗
6.1∗∗∗
r = 48
0.32
0.47
0.04
0.04
Trait
Block (b)
RLGR: relative length growth rate; RLMR: relative leaf mortality rate; midpoint = point in time when
growth or leaf-mortality is half-way; length = calculated maximum shoot length; growth characteristics based
on time in days or ◦ C-day; d.f.: degree of freedom; r: residual degrees of freedom. Significances of lengths and
numbers calculated after sqrt-transformation. ns = not significant.
∗ P < 0.05.
∗∗ P < 0.01.
∗∗∗ P < 0.001.
a
populations grew taller in The Netherlands than in Denmark (Fig. 2A; Table 3). In the
Czech Republic, the octoploid Romanian shoots became as tall as in the other two countries, whereas the Dutch shoots grew poorly in this country. The RLGR of North Swedish
plants was higher in the Danish than in the Dutch common environment, whereas the opposite was apparent for the Danish and South Swedish plants. In the Czech Republic, RLGR’s
were similar to those in the other two countries (Table 3). Since, RLGRs based on temperature sum did not differ between the Danish and Dutch common environment (Table 2A),
the significant lower midpoint of length-growth in Denmark could be related to the lower
final shoot-lengths in this country (Fig. 2B).
Among populations, large differences in growth curves were found (Table 3; Fig. 2A).
Generally, populations originating from higher latitudes started to grow somewhat earlier in
time than those from lower latitudes. For example, in The Netherlands, the North Swedish
plants already started to grow at the end of February when temperatures rose above 15◦ C
for a few days, and stopped when temperatures dropped again. Consequently, in March
1998, leaves of one of the clones became damaged by a combination of strong winds and
low temperatures. This clone was unable to recover from this event. In the Danish and
Dutch common environment, shoots of northern populations grew faster, but ceased growth
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Fig. 3. Mean date of panicle appearance of P. australis populations grown in The Netherlands. Pearson correlation
between latitude of origin and time of panicle appearance, or in the case of the North Swedish population time of
cessation of growth (n = 9). ns = not significant, ∗ P < 0.05; ∗∗ P < 0.01; ∗∗∗ P < 0.001 in this and subsequent
figures. The Romanian octoploids (large sized symbols) are omitted from the Pearson correlation analysis in this
and subsequent figure.
earlier in time than those of southern populations. The Romanian octoploids grew taller
with a higher RLGR than tetraploids, whereas time to reach half of the final length did not
differ between ploidy levels (Table 3).
3.2.2. Leaf mortality parameters
The relative leaf mortality rate (RLMR) and time when half of the leaves are dead (midpoint) were affected by a country by population interaction (Table 2B). No clear pattern
could be detected in this interaction (Table 4). In 1998, the RLMR increased with latitude in
The Netherlands. In both Denmark and The Netherlands, leaf mortality commenced earlier
in time in populations originating from higher than lower latitudes (Table 4).
3.2.3. Timing of panicle appearance
Generally, shoots flowered earlier in time in The Netherlands than in Denmark (Fig. 2A).
The clones from North Sweden did not flower in the common environments. In The Netherlands, only two of the six Spanish clones flowered (data not shown), whereas in Denmark,
none of the Romanian and Spanish clones flowered. In The Netherlands, including all
collected populations, the time of panicle appearance (or cessation of length-growth) was
significantly negatively correlated with latitude of origin (Fig. 3). No differences in flowering time between the Romanian tetra- and octoploids were found.
3.2.4. Shoot morphology
Length, diameter, number of nodes, and mean internode-length of the five longest shoots
were affected by a common environment by population interaction (Table 2C). Generally,
shoots grew taller with a higher number of nodes in The Netherlands than in Denmark,
whereas shoots were mostly wider in Denmark (Table 5). No general trend was apparent in the mean internode-length between the common environments. When populations
were grown in The Netherlands, lengths, number of nodes and mean internode-length decreased with latitude. When grown in Denmark, the number of nodes decreased with latitude, whereas the mean internode-length increased with latitude of origin. The Romanian
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Fig. 4. (A) Mean seed size, (B) total dry weight, (C) percentage leaf and stem of total dry weight, (D) percentage
rhizome and root of total dry weight, (E) LAR and SLA, (F) number of shoots and rhizomes, (G) total rhizome
length and length second shoot, (H) diameter of the first horizontal rhizome and of the second shoot, (I) SRL
of seedlings of nine P. australis populations. Pearson correlations between latitude of origin and (A) seed size,
and (B–I) different seedling traits. SLA: specific leaf area; LAR: leaf area ratio and SRL: specific rhizome length
(n = 54).
octoploids formed longer and wider shoots with a higher number of nodes than the tetraploids,
whereas the mean internode-length did not differ between ploidy levels (Table 5).
3.3. Greenhouse experiment: seed size and seedlings traits
No significant correlation was found between seed size in the native environment and
latitude of origin (Fig. 4A). Also, no latitudinal gradient was found in total dry weight of
seedlings (Fig. 4B). There was a trade-off between biomass allocation to leaves and stems,
O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
103
with southern populations investing more biomass into stems than northern populations
(Fig. 4C). No latitudinal differences in allocation to below-ground plant parts were found
(Fig. 4D). The higher LAR of northern than southern populations was related to the higher
biomass allocation to leaves rather than to differences in SLA (Fig. 4E). Although also
the SLA tended to increase with latitude (P = 0.054). Northern populations produced
more but shorter and thinner shoots, and longer but thinner rhizomes than southern populations (Fig. 4F–I). Contrasts showed that octoploids formed heavier seeds and higher total
dry weight than tetraploids. Octoploids formed also longer and wider shoots and thicker
rhizomes (P < 0.05).
4. Discussion
4.1. Timing of shoot growth and flowering
Populations from lower latitudes showed genetically determined longer growing seasons
than from higher latitudes. Within the same common environment, northern populations
started to grow at slightly lower temperatures than southern populations, but all populations
achieved their highest length growth rates in May–June 1998. Differences among populations were most pronounced in the rate of shoot-length growth and time of cessation of
growth. This latter trait denoted the time of panicle appearance. The most extreme northern
and southern populations were unable to make an optimal use of the growing season in the
different common environments. The Swedish populations grew most rapidly, but finished
growth too early in the season. The North Swedish plants, which flowered in their native
habitat, did not flower in Denmark and The Netherlands. In contrast, shoots of the southern
populations failed to complete the whole growth-cycle, i.e. did not flower in time, and were
therefore unable to set seed. Shoots, which ceased growth early in the season, also commenced to die-off earlier. As a matter of fact, leaves of the northern populations (Denmark
and Sweden) became infected by rust (Puccinia species), and were severely damaged by
aphids (Hyalopterus pruni Geoffr.) before they turned yellow. In contrast, leaves of the
Spanish population stayed green until the first frosts, indicating that this population was
unable to sense the onset of winter in time (Bannister, 1976). These differences in length of
the growing season and timing of flowering are commonly found in plants from different
latitudes, and seem to be a relatively easy evolutionary adjustment (Clausen et al., 1948;
McNaughton, 1966; Haslam, 1975; Bannister, 1976; Lambers et al., 1998).
Between oceanic and continental origins these growth differences were less distinct.
There seemed to be a trend that P. australis populations from more continental climates
started to grow earlier in time than expected from their position on the latitudinal gradient.
On the other hand, the time of panicle appearance seemed to be well correlated with distance across latitudes in The Netherlands. The most important difference between oceanic
and continental climates, might be the fact that populations from continental climates are
probably more tolerant to frost. To note, in the winter of 1996–1997, a part of the collected
Spanish clones died in The Netherlands due to severe frosts (O.A. Clevering, observations).
Although among geographic origins distinct genetically determined differences in the
length of the growing season were apparent, environmental cues were necessary to
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complete the whole seasonal cycle. In spring, the onset of growth in P. australis seemed
to be determined by temperatures rather than by day-lengths, which might be related to
the fact that the perennating organs are buried in mud, and therefore are unable to sense
differences in day-length. The later start of growth in the Danish and Czech as compared to
the Dutch common environment is supported by data on growth of natural stands in these
climatic habitats (Čı́žková, 1999). Generally, it has been shown that day- or night-length is
the cue for the start of the reproductive phase, and a combination of long nights and low
temperatures are cues for the onset of dormancy in winter (cf. Hay, 1990). The sensitivity
to day-length enable plants to synchronize their development with the climatic mean of
the weather pattern, and so avoid disruption by adverse weather conditions (Goudriaan and
Van Laar, 1994). The fact that plants flowered later in Denmark than in The Netherlands,
although Danish days are longer during the growing season, might indicate that photoperiod
is not an absolute requirement, but rather interacts with temperature.
4.2. Shoot relative length growth rate and morphology
The RLGR increased with increasing latitude of origin of the populations, whereas no
large differences in RLGR were found among the common environments. In contrast, populations in the native habitat showed a decrease in RLRG with increasing latitude (Čı́žková,
1999). These results indicate that genetically determined differences in RLGRs exist across
latitudes, but that temperature in a particular habitat largely determined RLGRs during the
period of exponential shoot-length growth. This is in accordance with Goudriaan and Van
Laar (1994), who stated that the development rate of a crop could be estimated quite well
by making use of the average air temperature. The low RLGRs based on temperature sum
of populations grown in the Czech Republic might be related to propagation difficulties
during the previous season. Although, it cannot be ruled out that due to the higher temperatures during the period of exponential shoot-growth, as compared to the other two common
environments, the higher respiration rates would have negatively affected growth rates.
Final shoot-lengths (and biomass) are strongly determined by the amount of carbohydrates available for growth (i.e. carbohydrates stored in rhizomes, and the capture and
utilization of resources during the season under study) (Haslam, 1970). Therefore, besides
differences in total radiation and temperature, the condition (size) of plants during the previous season might have a strong impact on shoot-lengths. When comparing the common
environments in Denmark and The Netherlands, final shoot-lengths of especially the more
southern populations were retarded in Denmark. These results are difficult to interpret,
because of the confounding effects of temperature, radiation, and condition of clones. Nevertheless, shoots of southern populations are probably not able to complete their whole
growth-cycle before the winter starts, when transplanted to higher latitudes. When transplanted to lower latitudes, differences in final shoot-lengths will become more pronounced
with southern populations producing the longest shoots.
4.3. Seed size and seedling traits
The absence of a relationship between geographic origin and size of seeds collected from
native habitats is in agreement with the results of McKee and Richards (1996). They stated
O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
105
that seed size is correlated with plant height rather than geographic origin. Since we did
not measure shoot length in the native habitats, where panicles were collected, we cannot
confirm this statement. On the other hand, environmental conditions might strongly affect
shoot-lengths in the field. Therefore, it cannot be ruled out that longer shoots with larger
seeds are produced in southern than northern latitudes.
A major disadvantage of growing seedlings from seeds collected in the field is that the
maternal environment conditions may have preconditioned seeds. The possible effects of
maternal environmental conditions on seedling traits have been discussed in Clevering
(1999). It was concluded that environmental conditions might have affected seed size and
therefore seedling size rather than traits as such. To overcome possible biased results due
to differences in total dry weight, we corrected morphological and biomass allocation traits
for differences in total dry weight.
P. australis seedlings from southern populations were taller with thicker rhizomes than
those from northern ones. These latter seedlings formed, however, a higher number of shoots
and rhizomes, and total rhizome length. Similar differences have been found by Haslam
(1975) and Véber (1981), and conform to morphological differences found in other species
(McNaughton, 1966; Seneca, 1974; Chapin and Chapin, 1981; Counts, 1993; Zhang and
Lechowicz, 1994). McNaughton (1966, 1975) suggested that northern Typha populations
are more subjected to density independent selection by frost and southern ones to density
dependent selection by competition for light. It is questionable whether selection by frost
explains the observed differences across latitudes in P. australis, since also clones from
continental habitats with severe winters produced tall shoots. A more plausible explanation
is that competition for light becomes more important with increasing length of the growing
season (cf. De Kroon and Kalliola, 1994).
Generally, plants from higher latitudes exhibit a higher biomass allocation to below-ground
plant parts than those from lower latitudes. This higher allocation to below-ground plant
parts has been related to lower nutrient availability at higher latitudes and to differences
in the amount of reserve-carbohydrates necessary to survive the winter period (Hay, 1990;
Chapin and Chapin, 1981; Reinartz, 1984; Kudo, 1995; Li et al., 1998). In this study, we
did not find any differences in biomass allocation to below-ground parts between latitudes.
As yet, we do not know whether nutrients limit growth of P. australis in higher latitudes.
Also, we do not know whether the amount of carbohydrates necessary to survive the winter
period is higher in higher than lower latitudes in this species. Although, the winter period
is longer and more severe in higher latitudes, soil oxygen concentrations will be higher and
respiration rates lower in high than in low latitudes. In the field, Čı́žková (1999) has found
a higher above/below-ground ratio with decreasing latitude in P. australis. She suggested
that rhizomes might become older in high than in low latitudes.
With increasing latitude, plants generally produce smaller leaves with a higher LAR,
but a lower leaf-turn over rate. At higher latitudes, often thicker leaves have been found
in species using leaves as a storage organ for resources, whereas the opposite seems to be
true for species using alternative storage-organs (Chapin and Chapin, 1981; Kudo, 1995; Li
et al., 1998; Hay, 1990). In P. australis, the allocation to leaves increased at the expense of
stems with increasing latitudes. The leaf turn-over rate was not determined in P. australis,
but plants originating from lower latitudes produced larger leaves (Clevering, unpublished
data) and a lower LAR, whereas also the SLA tended to be lower. In P. australis, the
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O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
production of larger leaves is strongly related to the production of taller stems in lower
latitudes. The higher LAR in P. australis might be a specialized form of shading response
to the lower irradiance accompanied with enhanced far-red to red ratios in higher latitudes
as has been found in other grasses (Hay, 1990). On the other hand, the trade-off between
allocation to leaves and stems in this species, in line with the production of taller shoots,
might also be related to the higher competition for light during the longer growing season
at lower latitudes.
4.4. Differences among Romanian ploidy levels
Shoots of octoploids grew faster than of tetraploids. From the results of the study, it
could also be concluded that octoploids generally show larger dimensions of the different
plant parts than tetraploids, whereas allocation to dry matter to the different plant parts
did not differ among ploidy levels. These latter results confirm to those found in the field,
and is a common response in higher ploidy levels (Stebbins, 1971). Ecological differences
between octo- and tetraploids have been discussed in detail by Clevering and Lissner (1999),
Paucă-Comănescu et al. (1999), and Hanganu et al. (1999).
4.5. Concluding remarks
Along a latitudinal gradient, P. australis showed genetically determined differences in
(i) length of the growing season, (ii) time of flowering, (iii) morphology, and (iv) biomass
allocation. These traits changed gradually with latitude, and therefore climatic clines rather
than ecotypes occur in this species.
The remaining question is what are the consequences of genetic adaptations to local climatic environments in P. australis when climatic conditions change? Generally, plants have
to cope with a combination of rising temperature, changes in nutrient and water availability,
rising CO2 , and increased probability of extreme temperature events (Bazzaz, 1996). Consequently, plants might either adapt to the new conditions, migrate to more suitable habitats
or become extinct (Bazzaz, 1996). Which scenario will prevail depends on the speed of
climate change and the ability of plants to develop new locally adapted genotypes, which
are better able to cope with resource modification. In the first stages of climate change, established P. australis clones might adjust by plastic responses. This is supported by the fact
that in the present study, the northward Danish and South Swedish populations grew very
well in The Netherlands. The total amount of plasticity in response to climate changes expressed in P. australis is impossible to predict from the present study. Especially so, because
of (i) the relative small climatic differences between common environments in this study,
and (ii) the complexity of the interacting environmental factors involved in climate change.
Results of other studies indicate that the most competitive, tallest, clones probably will
survive (Bazzaz, 1996). When climatic changes accelerate, it can be expected that plastic
responses are not sufficient anymore, and as a result, populations will become pauperized
and eventually die. Because, P. australis occupies the same niche on a worldwide scale, it
is not expected that other species will take over. The die-back of the existing populations
might create suitable sites for the sexual recruitment of clones better adapted to the changed
O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
107
climate (Clevering and Lissner, 1999). It is most likely that these clones show features of
the present more southward populations.
Acknowledgements
We thank the different partners in the Eureed-project and Prof. A. Melzer from the Limnology Station in Iffendorf (TU München) for hospitality during plant collection. Hans
Koelewijn (NIOO, Heteren) is thanked for collecting the clones from North Sweden. Heike
Koppitz (Humboldt University, Berlin) is thanked for DNA analysis of part of the collected
samples. Jos van Damme, Hans Koelewijn and two anonymous reviewers critically read
the manuscript. This work was funded by the Environment and Climate Programme of the
European Commission, contracts nos. ENV4-CT95-0147 and IC20-CT96-0020 (EUREED),
NIOO-CTO publication 2593.
References
Bannister, P., 1976. Introduction to Physiological Plant Ecology. Blackwell, Oxford.
Bazzaz, F., 1996. Plants in Changing Environments: Linking Physiological, Population, and Community Ecology.
Cambridge University Press, Cambridge.
Brix, H., 1999. The European research project on reed die-back and progression (Eureed). Limnologica 29, 5–10.
Callaghan, T.V., Carlsson, B.A., Jonsdottir, I.S., Svensson, B.M., Jonasson, S., 1992. Clonal plants and
environmental change: introduction to the proceedings and summary. Oikos 63, 341–347.
Chapin III, S.F., Chapin, M.C., 1981. Ecotypic differentiation of growth processes in Carex aquatilis along
latitudinal and local gradients. Ecology 55, 1180–1198.
Chapin III, S.F., Autumn, K., Pugnaire, F., 1993. Evolution of suites of traits in response to environmental stress.
Am. Nat. 142, 578–592.
Charles-Edwards, D.A., 1982. Physiological Determinants of Crop Growth. Academic Press, Sydney.
Čı́žková, H., 1999. Growth dynamics and ecophysiology of Phragmites in relation to the climatic conditions in
boreal-mediterranean and oceanic-continental gradients. In: Brix, H. (Ed.), Final Project Report to the European
Commission (contract no. ENV4-CT95-0147). University of Aarhus, Risskov, Denmark.
Clapham, D.H., 1998. Latitudinal cline of requirement for far-red light for the photoperiodic control of budset and
extension growth in Picea abies (Norway spruce). Phys. Plant. 102, 71–78.
Clausen, J., Keck, D.D., Hiesey, W.M., 1948. Experimental studies on the nature of species. III. Environmental
responses of climatic races of Achillea, Publication 581. Carnegie Institution of Washington, Washington, DC.
Clevering, O.A., 1999. Between- and within-population differences in Phragmites australis. I. The effects of
nutrients on seedling growth. Oecologia 121, 447–457.
Clevering, O.A., Lissner, J., 1999. Taxonomy, chromosome numbers, clonal diversity and population dynamics
of Phragmites australis (Cav.) Trin. ex Steud.. Aquat. Bot. 64, 185–208.
Counts, R.L., 1993. Phenotypic plasticity and genetic variability in annual Zizania spp. along latitudinal gradient.
Can. J. Bot. 71, 145–154.
De Kroon, H., Kalliola, R., 1994. Shoot dynamics of the giant grass Gynerium sagittatum in Peruvian Amazon
floodplains, a clonal plant that does show self-thinning. Oecologia 101, 124–131.
Goudriaan, J., Van Laar, H.H., 1994. Modelling Potential Crop Growth Processes. Kluwer Academic Publishers,
Dordrecht.
Hanganu, J., Mihail, G., Coops, H., 1999. Responses of ecotypes of Phragmites australis to increased seawater
influence: a field study in the Danube Delta, Romania. Aquat. Bot. 64, 351–358.
Haslam, S.M., 1970. The development of the annual population in Phragmites communis Trin.. Ann. Bot. 34,
571–591.
Haslam, S.M., 1972. Biological flora of the British Isles. Phragmites communis Trin.. J. Ecol. 60, 585–610.
108
O.A. Clevering et al. / Aquatic Botany 69 (2001) 89–108
Haslam, S.M., 1975. The performance of Phragmites communis Trin. in relation to temperature. Ann. Bot. 39,
881–888.
Hay, R.K.M., 1990. Tansley Review No. 26. The influence of photoperiod on the dry-matter production of grasses
and cereals. New Phytol. 116, 233–254.
Kudo, G., 1995. Leaf traits and shoot performance of an evergreen shrub, Ledum palustre ssp. decumbens, in
accordance with latitudinal change. Can. J. Bot. 73, 1451–1456.
Lambers, H., Chapin III, F.S., Pons, T.L., 1998. Plant Physiological Ecology. Springer, New York.
Li, B., Suzuki, J.-I., Hara, T., 1998. Latitudinal variation in plant size and relative growth rate in Arabidopsis
thaliana. Oecologia 115, 293–301.
McKee, J., Richards, A.J., 1996. Variation in seed production and germinability in common reed (Phragmites
australis) in Britain and France with respect to climate. New Phytol. 133, 233–243.
McNaughton, S.J., 1966. Ecotype function in the Typha community-type. Ecol. Monogr. 36, 297–325.
McNaughton, S.J., 1975. R- and k-selection in Typha. Am. Natur. 109, 251–261.
Paucă-Comănescu, M., Clevering, O.A., Hanganu, J., Gridin, M., 1999. Phenotypic differences among ploidy
levels of Phragmites australis growing in Romania. Aquat. Bot. 64, 223–234.
Reinartz, J.A., 1984. Life history variation of common mullein (Verbascum thapsus L.). II. Plant size, biomass
partitioning and morphology. J. Ecol. 72, 913–925.
SAS Institute, 1990. SAS/STAT User’s Guide. SAS Institute Inc., Cary, NC.
Seneca, E.D., 1974. Germination and seedling response of Atlantic and Gulf coasts populations of Spartina
alterniflora. Am. J. Bot. 61, 947–956.
Stebbins, G.L., 1971. Chromosomal Evolution in Higher Plants. Edward Arnold, London.
Van der Putten, W.H., 1997. Die-back of Phragmites australis in European wetlands: an overview of the European
Research Programme on Reed die-back and progression (1993–1994). Aquat. Bot. 59, 263–275.
Véber, K., 1981. Evaluation of introduced forms in experimental plantations of common reed (Phragmites
communis Trin.). Pol. Arch. Hydrobiol. 28, 35–42.
Winn, A.A., Gross, K.L., 1993. Latitudinal variation in seed weight and flower number in Prunella vulgaris.
Oecologia 93, 55–62.
Zhang, J., Lechowicz, M.J., 1994. Correlation between time of flowering and phenotypic plasticity in Arabidopsis
thaliana (Brassicaceae). Am. J. Bot. 75, 491–499.