Annals of Botany 87: 623±630, 2001
doi:10.1006/anbo.2001.1383, available online at http://www.idealibrary.com on
Relationships Between Climate and Flowering of Eight Herbs in a Swedish
Deciduous Forest
G E R M U ND T Y LE R
Department of Ecology, SoilÐPlant Research, Lund University, Ecology Building, S-223 62 Lund, Sweden
Received: 27 October 2000 Returned for revision: 5 December 2000
Accepted: 19 January 2001 Published electronically: 27 March 2001
E€ects of annual variation in rainfall, temperature and humidity on ¯owering abundance of eight temperate woodland
plants (Anemone nemorosa, Cardamine bulbifera, Lamiastrum galeobdolon, Oxalis acetosella, Ranunculus ®caria,
Stellaria holostea, Viola reichenbachiana and Viola riviniana) were studied during 12 consecutive years (1989±2000) in a
hornbeam (Carpinus betulus) forest in southeast Sweden. Above-average rainfall/humidity in late summer to early
autumn of the preceding year increased ¯owering abundance in L. galeobdolon, O. acetosella, V. reichenbachiana,
V. riviniana and, especially, in R. ®caria, but not in S. holostea and A. nemorosa. Moreover, ¯owering of R. ®caria and
O. acetosella was positively related to rainfall/humidity during several parts of, or the entire, preceding year. On the
contrary, ¯owering of S. holostea and A. nemorosa was closely related to low values of rainfall/humidity in autumn
and/or winter of the preceding year and also to low humidity in the current year in A. nemorosa. Two long periods (3±4
years) of increasing rainfall de®cit coincided with decreasing ¯owering abundance in most of the species, but not with
decreasing vegetative development. Temperature variability was less consistently related to ¯owering. A cool period
during the preceding summer or autumn seemed important for ¯owering in L. galeobdolon, O. acetosella and the Viola
species, although these relations were, at least partly, caused by interactions with rainfall/humidity. No signi®cant
(P 5 0.05) correlations were found between ¯owering and the conditions prevailing in April to MayÐthe main
# 2001 Annals of Botany Company
¯owering seasonÐof the current year.
Key words: Climate, ¯owering, rainfall, temperature, Anemone nemorosa, Cardamine bulbifera, Lamiastrum
galeobdolon, Oxalis acetosella, Ranunculus ®caria, Stellaria holostea, Viola reichenbachiana, Viola riviniana.
I N T RO D U C T I O N
The vascular plant ¯ora of temperate deciduous forests is
composed of species with widely di€ering ¯owering
patterns, although there may be phenological similarities.
Nearly all species ¯ower between early spring and early
summer, when light conditions on the forest ¯oor enable
plants to assimilate the extra energy required to produce
¯owers and fruits. In other respects, however, there are
large di€erences between species. Even within the same
forest stand, some species do not ¯ower at all in some years
while others produce ¯owers every year, though usually
with considerable interannual variation in abundance.
Thus, the frequency and abundance of ¯owering in forest
¯oor plants may vary greatly, both among years and
species. Causes of this variation are not properly understood. While `endogenic' plant periodicity might be of some
importance, climatic factors in temperate and cool climates
may play a major, more direct role in the induction and
performance of ¯owering. Given the progressive changes in
climate, with indications of rising mean temperatures in
central and northern Europe at least in the colder half of
the year, more studies of the climatic conditions regulating
the ¯owering of plants are warranted.
The objectives of this study were to investigate relationships between precipitation (rain- and snowfall), humidity
and air temperature, on the one hand, and abundance and
periodicity of ¯owering in eight deciduous forest plant
species, on the other, under the climatic conditions
0305-7364/01/050623+08 $35.00/00
prevailing in southeastern Sweden. The study was carried
out during 12 consecutive years, from 1988/89 to 1999/
2000. It was hypothesized that temperature and rainfall
conditions during parts of the preceding year are of major
importance in determining ¯owering abundance, but that
di€erent species react di€erently to these conditions.
M AT E R I A L S A N D M E T H O D S
Site, species and ®eld work
The site is a 50±80-year-old almost pure hornbeam
(Carpinus betulus L.) forest stand located on a gentle ESE
slope, 60 m a.s.l. and approx. 1 km from the shore, in the
Stenshuvud nature reserve (558400 N, 148160 E) on the Baltic
coast in south Sweden. The stand is structurally uniform
with a closed canopy and no shrub layer. In 1993, the
number of C. betulus trunks was 750 ha ÿ1 with a mean +
s.e diameter at breast height of 20.7 + 0.5 cm (n ˆ 140).
The stand developed from a wooded semi-natural, nonfertilized pasture with much hazel (Corylus avellana L.) and
had not been thinned, grazed or otherwise managed for at
least 25 years, nor had any storm damage or other severe
mehanical disturbance a€ected the stand during, or several
years prior to, the study period. There is a native roe deer
population in the area, but the study site had not been
visibly a€ected by their grazing.
The soil is a well-drained Dystric Cambisol (FAOUnesco 1997) developed from a non-calcareous sandy# 2001 Annals of Botany Company
624
TylerÐRainfall, Temperature and Flowering
silty moraine. The mean + s.e pH (0.2 M KCl) of the A
horizon was 3.78 + 0.03 in 1988 and 3.67 + 0.02 in 1998,
measured using identical methods. Exchangeable (0.2 M
KCl) Al was 2.14 + 0.19 mmol g ÿ1 d. wt in 1988 and
3.44 + 0.19 mmol g ÿ1 in 1998 (Brunet and Tyler, 2000);
exchangeable Ca (neutral M ammonium acetate method)
19.1 + 0.9 % C.E.C. (cation exchange capacity) in 1988.
Thirty circular permanent observation plots (each 5 m2),
divided into four quadrants, were established as a 5 6
grid, being part of a larger grid used for other purposes.
The distance between the centres of adjacent plots was 4 m
in the down-slope and 8 m in the along-slope direction (see
also Tyler, 1994; Brunet and Tyler, 2000). The four
permanent quadrants in each sample plot (5 m2) were
assessed separately. Tramping of the plots was avoided
during the inspections.
Eight herbaceous species producing ¯owers, occurring in
all or most of the observation plots during the study period
were considered in this study. The number of ¯owers
(Anemone nemorosa L., Oxalis acetosella L., Ranunculus
®caria L.) or ¯owering shoots (Cardamine bulbifera (L.)
Crantz, Lamiastrum galeobdolon (L.) Ehrend.& Polatschek,
Stellaria holostea L., Viola reichenbachiana Jord.ex Boreau,
Viola riviniana Rchb.) were counted nine±ten times per
year, usually every 10 d between March and June, the entire
¯owering period of these forest ¯oor species in southern
Sweden. All species studied are perennials. O. acetosella and
A. nemorosa have widely propagating rhizomes located at,
or just a little below, the soil surface; the others have more
restricted rhizome formation or aerial runners. The few
seedlings observed during the course of the study were
mainly S. holostea and O. acetosella, occasionally Viola
species, but never C. bulbifera, which does not seem to
produce any viable seeds in Scandinavia despite ¯owering
regularly. A. nemorosa is almost exclusively dependent on
vegetative rhizome propagation. Its clones grow radially,
developing a hollow centre which quickly becomes occupied
by other clones. In a mature stand, old clones become
totally mixed (Shirre€s and Bell, 1984).
The total number of ¯owers/¯owering shoots per plot
and year was calculated as the sum of the number produced
within each quadrant. Total cover ( % biomass cover of the
ground, vertical projection) was assessed in late April for
the early fading species, A. nemorosa, C. bulbifera and
R. ®caria and in July for the remaining species. A. nemorosa
was dominant in spring, while O. acetosella, S. holostea or
L. galeobdolon were dominant in summer, although they
usually had considerably lower ground cover values.
Climate and meteorological data
Meteorological data, monthly temperature means and
total precipitation (rain- and snowfall) from January 1987
to May 2000 were obtained from Swedish ocial meteorological statistics (SMHI, 1987±2000) using the means of
four meteorological stations in the coastal area of the
province. These means and sums were either used directly in
the calculations, or grouped in periods of 2±3 months.
Several preliminary tests were made on how to group
monthly meteorological data, and those groups which, on
average, gave the best relationships to the biological
variables were chosen. Humidity (Martonne's index) was
calculated for each month, and for 2±3 month periods, as p/
10 ‡ T, where p is the precipitation sum and T the mean
temperature of the period, compared to periods of the same
duration.
The climate of the area is cool temperate, subhumid; the
long-term (1961±1990) mean annual temperature is 7.98C,
with a mean of 16.68C in the warmest month (July) and
ÿ0.48C in the coldest months (January±February). The
long-term mean annual precipitation is 579 mm (mainly
rainfall, but some snowfall in November±March). Mean
monthly precipitation is lowest in April (37 mm) and
highest in July (60 mm). Martonne's humidity index (entire
year) is close to 32.
Interannual variability is fairly large. During the period
1987 to 2000, annual mean temperatures varied from 6.58C
(in 1987) to 9.78C (in 1990), the mean temperature of the
coldest month from ÿ6.28C (January 1987) to 4.58C
(January 1989), and the mean temperature of the warmest
month from 15.28C (July 1987 and 1993) to 20.88C (August
1997). Temperatures deviated positively from normal
during most of the periods from 1988 to 1992, and
negatively in 1987, 1993 and 1996 (Fig. 1). Total annual
precipitation varied fom 465 and 467 mm (in 1989 and
1996) to 716 mm (in 1998). A periodicity in the cumulative
deviation from normal values was apparent with gradually
increasing precipitation sum de®cits from autumn 1988 to
early summer 1993, and from summer 1995 to autumn
1997. Recovery and compensation periods occurred from
summer 1993 to summer 1995 and again in 1998 to 1999
(Fig. 1). The periods May to June 1992 (with total
11 mm), March to May 1993 (40 mm) and August
to September 1997 (30 mm) were very dry,
whereas September to October 1993 (200 mm), June 1991
(125 mm), July 1993 (134 mm), September 1994 (160 mm)
and August 1999 (131 mm) were wet.
The e€ects of interannual variability in temperature and
rainfall on ¯owering frequencies were analysed.
R E S U LT S
A. nemorosa completely dominated the forest ¯oor vegetation in April, covering (50-) 70±100 % of the plots,
whereas R. ®caria was less abundant and its cover was more
variable among plots. C. bulbifera was evenly spread,
although lower in abundance. Coverage of the study species
was not as high in the summer (total cover was 20±40 % in
most plots). Of the species studied, O. acetosella (annual
means ranging from 6.4±20 %), L. galeobdolon (3.7±9.3 %)
or S. holostea (0.8±8.8 %) were dominant or co-dominant.
Other species made only small contributions to the total.
During the 12 years of observation, ¯owering abundance
of the species peaked in several di€erent years (Table 1).
However, mean number of ¯owers/¯owering shoots produced per year by the di€erent species correlated positively,
in many cases signi®cantly (Table 2). This means that there
were years in which ¯owering was generally bad or good in
most species. Low ¯owering abundances in all species were
especially apparent in 1998 and in several species in 1993
TylerÐRainfall, Temperature and Flowering
200
150
100
50
0
–50
–100
–150
–200
Relative flowering abundance (%)
8
6
4
2
0
–2
–4
–6
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
625
Precipitation, monthly
cumulative deviation from normal
1987 1988 1989
1990
1991
1992 1993
Temperature, monthly means
1994
1995 1996 1997 1998
1999
deviation from normal
A. nemorosa
C. bulbifera
1987
1988
1989
1990
1991
1992
1993
1994
1995
1991
1992 1993 1994 1995
1996
1997
1998
1999
L. galeobdolon
O. acetosella
R. ficaria
S. holostea
V. reichenbachiana
V. riviniana
1987 1988 1989
1990
1996 1997 1998 1999
F I G . 1. Precipitation, temperature and ¯owering abundance during the study period. Precipitation (mm) given as cumulative deviation from
normal (1961±1990), starting at 0 on 1 Jan. 1987; temperature (8C, monthly means) as deviation from normal. Relative ¯owering abundance of the
eight species studied given as mean number of ¯owers/¯owering shoots produced per year and sample plot, calculated as % of the year with the
largest number produced.
626
TylerÐRainfall, Temperature and Flowering
T A B L E 1. Number of ¯owers (A. nemorosa, O. acetosella, R. ®caria, V. reichenbachiana, V. riviniana) or ¯owering shoots
(C. bulbifera, L. galeobdolon, S. holostea) produced per plot (5 m2; n ˆ 30) and year
Species
Year
A. nemorosa
C. bulbifera
L. galeobdolon
O. acetosella
R. ®caria
S. holostea
V. reichenb.
V. riviniana
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
763 + 41
193 + 12
237 + 15
530 + 25
62 + 5
122 + 7
263 + 17
166 + 8
254 + 18
102 + 9
121 + 7
269 + 12
3.6 + 0.6
2.7 + 0.5
2.4 + 0.5
6.4 + 1.1
1.9 + 0.5
2.6 + 0.4
5.4 + 1.0
1.9 + 0.4
2.7 + 0.4
1.0 + 0.2
1.9 + 0.3
2.9 + 0.5
0.0 + 0.0
5.4 + 0.9
5.0 + 1.5
2.6 + 0.7
0.2 + 0.1
8.2 + 1.2
5.4 + 0.9
1.3 + 0.4
3.6 + 0.5
0.0 + 0.0
2.9 + 0.5
1.1 + 0.2
10.6 + 0.7
15.8 + 2.2
40.3 + 5.4
35.7 + 4.6
7.3 + 1.5
32.7 + 6.3
44.4 + 5.4
7.0 + 1.2
22.0 + 2.8
0.2 + 0.1
63.0 + 7.7
52.5 + 5.1
13.8 + 4.1
12.4 + 3.9
8.2 + 3.5
12.0 + 3.8
12.4 + 4.9
15.0 + 6.0
25.3 + 8.6
12.2 + 4.9
8.4 + 3.7
3.9 + 1.2
13.2 + 4.9
11.6 + 2.9
8.5 + 1.7
24.5 + 5.5
2.6 + 1.1
5.8 + 2.2
0.0 + 0.0
5.2 + 1.7
19.2 + 4.2
7.0 + 1.5
13.2 + 2.8
1.3 + 0.4
28.5 + 5.5
22.2 + 4.2
1.57 + 0.36
2.80 + 0.51
1.23 + 0.20
0.73 + 0.19
0.27 + 0.09
1.43 + 0.37
2.10 + 0.46
0.50 + 0.17
0.50 + 0.15
0.03 + 0.02
0.73 + 0.24
0.70 + 0.23
0.40 + 0.14
0.37 + 0.14
1.33 + 0.49
1.47 + 0.46
0.90 + 0.30
1.83 + 0.45
1.03 + 0.29
0.33 + 0.14
0.70 + 0.21
0.03 + 0.02
0.63 + 0.24
0.27 + 0.09
Data are means + s.e.
T A B L E 2. Correlation coecients (r-values) of mean ¯owering abundance (log10 transformed data) per year (n ˆ 12; 1989±
2000) and observation plot of the species studied
A. nemorosa
C. bulbifera
L. galeobdolon
O. acetosella
R. ®caria
S. holostea
V. reichenbachiana
V. riviniana
C. bulbifera
0.78**
0.51
0.48
0.19
0.58*
0.44
0.29
0.66*
0.70*
0.68*
0.40
0.68*
0.67*
L. galeobdolon
0.86***
0.67*
0.61*
0.94***
0.78**
O. acetosella
R. ®caria
0.73**
0.51
0.85***
0.81**
0.35
0.78**
0.68*
S. holostea
0.54
0.06
V. reichenbachiana
0.73**
*** P 5 0.001, ** P 5 0.01, * P 5 0.05.
All r values are positive.
(Fig. 1). Five of the species (L. galeobdolon, O. acetosella,
S. holostea, V. reichenbachiana, V. riviniana) produced no,
or almost no ¯owers in 1998, L. galeobdolon did not ¯ower
in 1989 or 1993, nor did S. holostea in 1993.
The ¯owering seasons of 1993 and 1998 were preceded by
several years of gradually increasing precipitation de®cits
(Fig. 1). There are signs of long-term cycles in the
precipitation pattern but no general trends were identi®ed
over the period studied. Temperatures were above normal in
spring 1993, but close to normal in spring 1998. The best
year for ¯owering was 1995 with above-average ¯owering
abundances in all species, although only R. ®caria reached
its maximum. This spring was preceded by about 2 years of
generally above-normal precipitation (Fig. 1), its temperature was close to normal but temperatures of the preceding
year (1994) were above normal.
None of the species considered displayed a signi®cant
time-trend in ¯owering abundance, per cent cover or
number of individuals per sample plot. Variability in
vegetative development may be important in determining
interannual di€erences in ¯owering frequencies. Tests were
made on this variability, with the exception of the Viola
species, which were not separable using vegetative characters and therefore could not be assessed in this respect.
With the notable exception of S. holostea, there were no
signi®cant correlations (P 4 0.05) between mean ¯owering
abundance and vegetative development. Flowering of
S. holostea was closely related to its ground cover
(r ˆ 0.92; P 5 0.001). Thus the environmental conditions
controlling or in¯uencing ¯owering of this species mainly
act through their in¯uence on its vegetative development,
and the number of ¯owering shoots is closely related to the
total biomass produced each year. This must be taking into
account when assessing the in¯uence of meteorological
factors on the ¯owering frequency of S. holostea.
Correlations between annual ¯owering abundance
(y-variable; number of ¯owers/¯owering shoots produced
per plot) and meteorological (x-variables) were calculated
(Table 3). In all species, signi®cant (P 5 0.05 to P 5 0.001)
values of r, both positive and negative, were obtained. Two
general features of this correlation study are apparent: (a)
no signi®cant values of r were found with conditions
prevailing in April to May of the current year, whereas (b)
conditions in August to September of the previous year
were clearly over-represented among variables with signi®cant r values. This indicates that, in the late (May) ¯owering
species, the ¯owering frequency is already `decided'
before April. It also indicates that conditions during the
main period of vegetative growth (August to September) in
several of the species studied are of considerable importance
TylerÐRainfall, Temperature and Flowering
627
T A B L E 3. Correlations (values of r) with levels of signi®cance between climate variables and mean annual ¯owering
abundance per year and plot
Precipitation
A. nemorosa
Temperature
Year (c) ÿ0.74**
Jan.(c) ÿ0.59*
C. bulbifera
Humidity
Year (c) ÿ0.83***
Oct.±Dec.( p) ÿ0.58*
Jan.(c) ÿ0.61*
June ( p) ÿ0.62*
Oct.±Dec.(p) ‡0.66*
Year (c) ÿ0.66*
L. galeobdolon
Jan.±March (c) ‡0.59*
Feb.( p) ÿ0.64*
Aug.±Sept.(p) ‡0.60*
April ( p) ‡0.62*
Aug.±Sept.( p) ÿ0.68*
Year (c) ‡0.62*
Jan.±March (c) ‡0.59*
Aug.±Sept.( p) ‡0.64*
O. acetosella
Year ( p) ‡0.71**
Aug.±Sept.(p) ‡0.71**
April ( p) ‡0.68*
Aug.(p) ÿ0.66*
Year ( p) ‡0.67*
Aug.±Sept. ( p) ‡0.72**
R. ®caria
Year ( p) ‡0.58*
Aug.±Sept.(p) ‡0.80**
Jan.(p) ‡0.61*
Aug.±Sept. ( p) ‡0.80**
March ( p) ‡0.61*
Sept.(p) ‡0.64*
S. holostea
Nov.( p) ÿ0.86***
Oct.(p) ‡0.59*
March ( p) ‡0.58*
Nov.( p) ÿ0.87***
V. reichenb.
Aug.±Sept.(p) ‡0.66*
March (c) ‡0.61*
Jan (p) ‡0.78**
Aug.±Sept.( p) ÿ0.59*
Apr.±May ( p) ÿ0.59*
Aug.±Sept.( p) ‡0.69*
V. riviniana
Aug.±Sept.(p) ‡0.58*
Aug.±Sept.( p) ÿ0.71**
Aug.±Sept.( p) ‡0.63*
Variables and r values in italics mean that the ¯owering (y) variable was log10 transformed. Only r values 4 0.57 (P 5 0.05) are shown.
Number of years ˆ 12 (1989±2000).
Climate variables considered: Precipitation (rain- and snowfall) sums, mean temperature and mean humidity (Martonne's index) for each
month, for the entire year, and for January±March, April±May, June±July, August±September and October±December. Climate variables either
calculated for the current year; up to the end of the ¯owering period (c) or for the previous year ( p).
The stepwise regression procedure presupposes linear functions. As no relationships between two variables, where at least one is `biological', are
perfectly linear, regression (and correlation) analysis always tends to produce low estimates of a relationship, due to curvilinearity. In those cases
where variables were log10 transformed, linearity was improved and this treatment therefore preferred. Where no transformation was introduced,
the relationship was better expressed by the untransformed data.
in determining the ¯owering frequency in the following
year. A third, though less apparent feature, is that
conditions during the late winter months of both the
current and the preceding year are of some importance to
¯owering.
In considering the individual species, however, several
di€erences are apparent (Table 3). Flowering of
A. nemorosa was negatively correlated with several
precipitation and humidity variables, but was not correlated with temperature variables (P 4 0.05). The data of
C. bulbifera, also with early fading shoots, are dicult to
evaluate. Low temperatures in June but high temperatures
in the autumn of the previous year seemed to favour
¯owering. As was the case with A. nemorosa, C. bulbifera
¯owered in all 12 study years, although with considerable
interannual variability.
Flowering of L. galeobdolon was signi®cantly correlated
with meteorological variables (Table 3) and positively
correlated with rainfall and humidity in several periods
during the current and previous year. As mentioned above,
¯owering of S. holostea was closely related to its vegetative
development (cover) of the current year, which seemed to
be favoured by low rainfall (r ˆ ÿ0.79; P 5 0.01) and
humidity (r ˆ ÿ0.75; P 5 0.01) in November of the
previous year. However, the correlation coecients were
even higher for ¯owering abundance as related to
these November variables (r ˆ ÿ0.86; P 5 0.001, and
ÿ0.87; P 5 0.001, respectively). In spite of the coincidence
of ¯owering failure and long periods of below-normal
precipitation (Fig. 1), it therefore seems likely that good
development and ¯owering of S. holostea was in some way
dependent on a dry period in late autumn.
The interannual variability of ¯owering in O. acetosella
has close similarities to that of L. galeobdolon (Tables 1 and
2) with very low values in 1993, 1996 and 1998. The
¯owering abundance of this ubiquitous forest plant was
positively related to precipitation and humidity of the
previous year, especially to the data for August
to September, and also correlated positively to the April
temperature of the previous year. In R. ®caria, a species
which spends the summer and autumn months exclusively
below ground, the humidity and precipitation of the
previous year, especially during August to September, was
important to ¯owering. Flowering of the two taxonomically
closely related species of Viola was also positively correlated
with rainfall and humidity in August to September of the
previous year but negatively correlated with temperature
(Table 3). In V. reichenbachiana, with a much more
southern distribution range in Sweden, temperatures
in January and March correlated positively with ¯owering.
Di€erences in phenology among years (Fig. 2), largely
controlled by temperature prior to and during ¯owering,
628
TylerÐRainfall, Temperature and Flowering
100
80
60
40
20
0
A. nemorosa, mean
100
80
60
40
20
0
C. bulbifera, mean
100
80
60
40
20
0
A. nemorosa, 1989
100
80
60
40
20
0
C. bulbifera, 1990
100
80
60
40
20
0
A. nemorosa, 1996
100
80
60
40
20
0
C. bulbifera, 1996
MARCH
APRIL
100
80
60
40
20
0
L. galeobdolon, mean
100
80
60
40
20
0
L. galeobdolon, 1990
100
80
60
40
20
0
L. galeobdolon, 1996
MARCH
APRIL
MAY
JUNE
MARCH
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
MAY
JUNE
O. acetosella, 1996
MARCH
100
80
60
40
20
0
S. holostea, mean
100
80
60
40
20
0
R. ficaria, 1996
100
80
60
40
20
0
S. holostea, 1990
100
80
60
40
20
0
R. ficaria, 1990
100
80
60
40
20
0
S. holostea, 1996
100
80
60
40
20
0
100
80
60
40
20
0
100
80
60
40
20
0
MAY
JUNE
V. reichenbachiana, mean
V. reichenbachiana, 1990
V. reichenbachiana, 1996
MARCH
APRIL
MAY
JUNE
JUNE
O. acetosella, 1990
R. ficaria, mean
APRIL
MAY
O. acetosella, mean
100
80
60
40
20
0
MARCH
APRIL
MARCH
100
80
60
40
20
0
V. riviniana, mean
100
80
60
40
20
0
V. riviniana, 1990
100
80
60
40
20
0
V. riviniana, 1996
MARCH
APRIL
MAY
JUNE
APRIL
MAY
JUNE
APRIL
MAY
JUNE
F I G . 2. Flowering phenology of the eight species studied: mean of all 12 years (1989±2000), the `earliest' year (1990; in A. nemorosa 1989) and the
`latest' year (1996). Data given for periods of 10 d and calculated as % of the period with annual ¯owering maximum.
might be of importance to the number of ¯owers produced.
1989 and 1990 were very `early' years with large positive
temperature anomalies in winter and early spring, whereas
1996 was `late' with temperatures much below normal
during this period. A. nemorosa had already started to
¯ower in the middle of March in 1989, but did not ¯ower
until about 10 April in 1996. Peak ¯owering di€ered by
approx. 20 d between these years. The di€erences between
these two years were of the same magnitude or even larger
(20±30 d) in the later ¯owering species (Fig. 2). Flowering
of all species ended approx. 20 d later in 1996 than in 1989
or 1990, the length of the ¯owering period thus being little
in¯uenced by temperature.
There was no signi®cant correlation between time of
¯owering maximum and ¯owering abundance when all years
were considered together for any species (P ˆ 0.21±0.97;
data not shown. When all species were considered as a group,
the correlation was also non-signi®cant (P ˆ 0.67). Thus it
seems that neither time of ¯owering maximum, nor duration
of the ¯owering period, in¯uenced ¯owering abundance.
The approximate start of ¯owering may be deduced from
Fig. 2. According to long-term studies of 11 species in
TylerÐRainfall, Temperature and Flowering
Finland (Heikinheimo and Lappalainen, 1997), a springtime temperature increase of 18C is expected to make ¯ower
buds burst approx. 4 d earlier. In most species included in
the present study, the di€erence in the start of ¯owering
between the `late' year (1996) and the `early' year (1990) was
aprox. 30 d but it was less in A. nemorosa and
V. reichenbachiana). The March to April temperatures
deviated by 58C between 1990 and 1996, which would
correspond to a delay of approx. 6 d per 18C. However,
general di€erences in climate and species may bias such
comparisons between these two studies.
DISCUSSION
Interannual di€erences in ¯owering might be caused by
long-term internal rhythms of individuals or populations
and by external factors. Under less variable climatic
conditions, plant development may be controlled endogenously, but adverse environmental conditions, such as
drought, might secondarily synchronize part of the
rhythmicity to seasonal climate changes (Borchert, 1980).
In trees, it seems that 1 year of profuse ¯owering (and
fruiting) is often followed by 1 or 2 years of very little
¯owering (Waller, 1979). This might be explained by the
need to restore energy and other resources used in
fructi®cation. Such a pattern, however, is dicult to discern
in the herbaceous plants of this study. Years of peak
¯owering were not usually followed by years of minimal
¯owering (Fig. 1).
Another hypothesis relates the frequency of `mast' years
and `bad' years to the satiation of a predator system, as
discussed by population biologists, e.g. Donaldson (1993).
However, it seems only hypothetical that this could be a
main factor contributing to the interannual variability in
the species and the habitat considered in the present study.
These species fructify rather sparsely and potential seed
predators would have many sources of food other than
herbaceous seeds.
Although not all interannual variability in ¯owering
abundance was accounted for by the meteorological data
considered, it seems most probable that this variability was
principally controlled by temperature and humidity/
moisture conditions of the site. Monthly means or totals,
however, may not always o€er the best predictions of
¯owering induction and success. Weather extremes, which
are not easy or impossible to account for, might sometimes
be more important. That ¯ower induction may be
controlled or in¯uenced by temperature or moisture
conditions during periods long before (even years; Taylor
and Inouye, 1985) the ¯owering event is documented in
many plants, especially in bulb geophytes (Mori et al.,
1991, 1992) but also in woody species (Law et al., 2000).
Formation of ¯ower primordia may be promoted by a
period of cool temperatures. However, in usually cool
climates, temperature at the time of ¯ower induction may
instead be positively related to ¯owering and seed
production (Allen and Platt, 1990). Also moisture conditions may play a major role, at least in periodically dry
areas. The period of greatest ¯owering in a number of
629
Australian myrtaceous trees occurred 9 months after a
period of heavy rainfall (Law et al., 2000).
Having observed ¯owering over a long period under
climatic conditions not too di€erent from those of the area
studied here, Inghe and Tamm (1985, 1988), concluded that
weather factors were probably not of great (direct)
importance to the ¯owering of Anemone hepatica L.,
whereas ¯owering of another forest ¯oor species, Sanicula
europaea L., was positively dependent on rainfall in July of
the previous year. Flowering abundance of S. europaea
varied more between years than that of A. hepatica, and
¯owering individuals tended not to do so in the following
year. This is explicable by the higher cost of reproduction in
S. europaea than in A. hepatica. However, S. europaea
usually grows on moister soil, thus physiological di€erences
in water demand may be part of the explanation.
No previous detailed studies have been published to date
documenting the in¯uence of climate variability on ¯owering abundance and frequency of the woodland species
considered here. As these eight species have somewhat
di€erent Swedish and world distributions (Hulten, 1950), it
is likely that temperature and rainfall conditions would
in¯uence their performance di€erently. Judging from their
distribution ranges in northern Europe, V. reichenbachiana,
L. galeobdolon and S. holosteaÐspecies occurring exclusively in the very south of ScandinaviaÐwould be the most
demanding of high temperatures (or long growing seasons),
whereas O. acetosella and V. riviniana would be the least
demanding. High temperatures during single months of the
preceding year were actually positively related to ¯owering
of the former species, but this was also the case with
O. acetosella (Table 3).
There are also di€erences in the demand for light among
these species, despite growing in the same plots.
O. acetosella and L. galeobdolon are known to be very
shade tolerant, whereas growth of S. holostea, in particular,
is favoured by high light (Rebele et al., 1982; Werner et al.,
1982). However, di€erences in light requirement and
utilization also exist between the ®rst two species. A greater
phenotypic plasticity may enable L. galeobdolon to adapt
better to more strongly lit sites than O. acetosella (Packham
and Willis, 1977, 1982). Throughout the period covered by
the current study, the hornbeam canopy was closed, with
only minor and rapidly transient sun-patches reaching the
forest ¯oor from about mid-May to early or mid-October.
It is certainly possible that some di€erences among years in
the amount of hornbeam leaf biomass produced might have
in¯uenced light conditions to some extent, though no data
were collected on this.
The ecophysiolgy of these species is not well known. It is
therefore dicult to identify the causes of di€erences in
their temperature and moisture requirements for growth or
¯owering. It seems premature to speculate about possible
mechanisms controlling these di€erences.
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