Relationships Between Climate and Flowering of Eight Herbs in a Swedish Deciduous Forest

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1 Annals of Botany 87: 623±63, 21 doi:1.16/anbo , available online at on Relationships Between Climate and Flowering of Eight Herbs in a Swedish Deciduous Forest GERMUND TYLER Department of Ecology, SoilÐPlant Research, Lund University, Ecology Building, S Lund, Sweden Received: 27 October 2 Returned for revision: 5 December 2 Accepted: 19 January 21 Published electronically: 27 March 21 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±2) 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 5.5) correlations were found between owering and the conditions prevailing in April to MayÐthe main owering seasonðof the current year. # 21 Annals of Botany Company Key words: Climate, owering, rainfall, temperature, Anemone nemorosa, Cardamine bulbifera, Lamiastrum galeobdolon, Oxalis acetosella, Ranunculus caria, Stellaria holostea, Viola reichenbachiana, Viola riviniana. INTRODUCTION 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 prevailing in southeastern Sweden. The study was carried out during 12 consecutive years, from 1988/89 to 1999/ 2. 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. MATERIALS AND METHODS Site, species and eld work The site is a 5±8-year-old almost pure hornbeam (Carpinus betulus L.) forest stand located on a gentle ESE slope, 6 m a.s.l. and approx. 1 km from the shore, in the Stenshuvud nature reserve (5584 N, 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 75 ha 1 with a mean + s.e diameter at breast height of cm (n ˆ 14). 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 (FAO- Unesco 1997) developed from a non-calcareous sandy /1/ $35./ # 21 Annals of Botany Company

2 624 TylerÐRainfall, Temperature and Flowering silty moraine. The mean + s.e ph (.2 M KCl) of the A horizon was in 1988 and in 1998, measured using identical methods. Exchangeable (.2 M KCl) Al was mmol g 1 d. wt in 1988 and mmol g 1 in 1998 (Brunet and Tyler, 2); exchangeable Ca (neutral M ammonium acetate method) % C.E.C. (cation exchange capacity) in Thirty circular permanent observation plots (each 5 m 2 ), 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, 2). The four permanent quadrants in each sample plot (5 m 2 ) 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 1 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 2 were obtained from Swedish o cial meteorological statistics (SMHI, 1987±2) 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/ 1 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±199) mean annual temperature is 7.98C, with a mean of 16.68C in the warmest month (July) and.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 (6 mm). Martonne's humidity index (entire year) is close to 32. Interannual variability is fairly large. During the period 1987 to 2, annual mean temperatures varied from 6.58C (in 1987) to 9.78C (in 199), the mean temperature of the coldest month from 6.28C (January 1987) to 4.58C (January 1989), and the mean temperature of the warmest month from 15.28C (July 1987 and 1993) to 2.88C (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 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 (4 mm) and August to September 1997 (3 mm) were very dry, whereas September to October 1993 (2 mm), June 1991 (125 mm), July 1993 (134 mm), September 1994 (16 mm) and August 1999 (131 mm) were wet. The e ects of interannual variability in temperature and rainfall on owering frequencies were analysed. RESULTS A. nemorosa completely dominated the forest oor vegetation in April, covering (5-) 7±1 % 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 2±4 % in most plots). Of the species studied, O. acetosella (annual means ranging from 6.4±2 %), L. galeobdolon (3.7±9.3%) or S. holostea (.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

3 TylerÐRainfall, Temperature and Flowering Precipitation, monthly cumulative deviation from normal Temperature, monthly means deviation from normal A. nemorosa Relative flowering abundance (%) C. bulbifera L. galeobdolon O. acetosella R. ficaria S. holostea V. reichenbachiana V. riviniana FIG. 1. Precipitation, temperature and owering abundance during the study period. Precipitation (mm) given as cumulative deviation from normal (1961±199), starting at 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.

4 626 TylerÐRainfall, Temperature and Flowering TABLE 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 m 2 ; n ˆ 3) and year Species Year A. nemorosa C. bulbifera L. galeobdolon O. acetosella R. caria S. holostea V. reichenb. V. riviniana Data are means + s.e. TABLE 2. Correlation coe cients (r-values) of mean owering abundance (log 1 transformed data) per year (n ˆ 12; 1989± 2) and observation plot of the species studied A. nemorosa C. bulbifera L. galeobdolon O. acetosella R. caria S. holostea V. reichenbachiana C. bulbifera.78** L. galeobdolon.51.66* O. acetosella.48.7*.86*** R. caria.19.68*.67*.73** S. holostea.58*.4.61* V. reichenbachiana.44.68*.94***.85***.78**.54 V. riviniana.29.67*.78**.81**.68*.6.73** *** P 5.1, ** P 5.1, * P 5.5. 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 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 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 4.5) between mean owering abundance and vegetative development. Flowering of S. holostea was closely related to its ground cover (r ˆ.92; P 5.1). 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 5.5 to P 5.1) 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

5 TABLE 3. Correlations (values of r) with levels of signi cance between climate variables and mean annual owering abundance per year and plot A. nemorosa Year (c).74** Jan.(c).59* Precipitation Temperature Humidity C. bulbifera June (p).62* Oct.±Dec.(p).66* L. galeobdolon Jan.±March (c).59* Feb.(p).64* Aug.±Sept.(p).6* O. acetosella Year ( p).71** Aug.±Sept.(p).71** R. caria Year ( p).58* Aug.±Sept.(p).8** TylerÐRainfall, Temperature and Flowering 627 April (p).62* Aug.±Sept.(p).68* April (p).68* Aug.(p).66* Year (c).83*** Oct.±Dec.(p).58* Jan.(c).61* Year (c).66* Year (c).62* Jan.±March (c).59* Aug.±Sept.(p).64* Year (p).67* Aug.±Sept. (p).72** Jan.(p).61* Aug.±Sept. (p).8** March (p).61* Sept.(p).64* S. holostea Nov.(p).86*** Oct.(p).59* March (p).58* Nov.(p).87*** V. reichenb. Aug.±Sept.(p).66* March (c).61* Jan (p).78** Aug.±Sept.(p).59* Apr.±May (p).59* Aug.±Sept.(p).69* V. riviniana Aug.±Sept.(p).58* Aug.±Sept.(p).71** Aug.±Sept.(p).63* Variables and r values in italics mean that the owering (y) variable was log 1 transformed. Only r values 4.57 (P 5.5) are shown. Number of years ˆ 12 (1989±2). 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 log 1 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 4.5). 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.79; P 5.1) and humidity (r ˆ.75; P 5.1) 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.86; P 5.1, and.87; P 5.1, 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 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,

6 628 TylerÐRainfall, Temperature and Flowering A. nemorosa, mean C. bulbifera, mean A. nemorosa, 1989 A. nemorosa, C. bulbifera, 199 C. bulbifera, L. galeobdolon, mean O. acetosella, mean L. galeobdolon, O. acetosella, L. galeobdolon, O. acetosella, R. ficaria, mean S. holostea, mean R. ficaria, S. holostea, R. ficaria, S. holostea, V. reichenbachiana, mean V. riviniana, mean V. reichenbachiana, V. riviniana, V. reichenbachiana, V. riviniana, 1996 F IG. 2. Flowering phenology of the eight species studied: mean of all 12 years (1989±2), the `earliest' year (199; in A. nemorosa 1989) and the `latest' year (1996). Data given for periods of 1 d and calculated as % of the period with annual owering maximum. might be of importance to the number of owers produced and 199 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 1 April in Peak owering di ered by approx. 2 d between these years. The di erences between these two years were of the same magnitude or even larger (2±3 d) in the later owering species (Fig. 2). Flowering of all species ended approx. 2 d later in 1996 than in 1989 or 199, 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.21±.97; data not shown. When all species were considered as a group, the correlation was also non-signi cant (P ˆ.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

7 TylerÐRainfall, Temperature and Flowering 629 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 (199) was aprox. 3 d but it was less in A. nemorosa and V. reichenbachiana). The March to April temperatures deviated by 58C between 199 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, 198). 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., 2). 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, 199). Also moisture conditions may play a major role, at least in periodically dry areas. The period of greatest owering in a number of Australian myrtaceous trees occurred 9 months after a period of heavy rainfall (Law et al., 2). 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, 195), 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. LITERATURE CITED Allen RB, Platt KH Annual seedfall varition in Nothofagus solandri, Fagaceae, in Canterbury, New Zealand. Oikos 57: 199±26.

8 63 TylerÐRainfall, Temperature and Flowering Borchert R Phenology and ecophysiology of tropical trees. Erythrina poeppigiana. Ecology 61: 165±174. Brunet J, Tyler G. 2. Interannual variability in abundance of eld layer species in a south Swedish deciduous wood. Flora 195: 97±13. Donaldson J Mast-seeding in the cycad genus Encephalartos: A test of the predator satiation hypothesis. Oecologia 94: 262±271. Heikinheimo M, Lappalainen H Dependence of the owering bud burst of some plant taxa in Finland on e ective temperature sum: Implications for climate warming. Annales Botanici Fennici 34: 229±243. Hulte n E Atlas of the distribution of vascular plants in NW. Europe. Stockholm: Generalstabens Litogra ska Anstalt. Inghe O, Tamm CO Survival and owering of perennial herbs. IV The behaviour of Hepatica nobilis and Sanicula europaea on permanent plots during 1943±1981. Oikos 45: 4±42. Inghe O, Tamm CO Survival and owering of perennial herbs. V Patterns of owering. Oikos 51: 23±219. Law B, Mackowski C, Schoer L, Tweedie T. 2. Flowering phenology of myrtaceous trees and their relation to climatic, environmental and disturbance variables in northern New South Wales. Australian Ecology 25: 16±178. Mori G, Imanishi H, Sakanishi Y E ect of temperature on owering of Hymenocallis speciosa Salisb. Journal of the Japanese Society for Horticultural Science 6: 387±394. Mori G, Imanishi H, Sakanishi Y E ects of temperature on owering of Crinum x powelli Hort.ex Bak.cv.Album. Journal of the Japanese Society for Horticultural Science 61: 651±657. Packham JR, Willis AJ The e ects of shading on Oxalis acetosella. Journal of Ecology 65: 619±642. Packham JR, Willis AJ The in uence of shading and of soil type on the growth of Galeobdolon luteum. Journal of Ecology 7: 491±512. Rebele F, Werner P, Bornkamm R E ects of light intensity and light quality on the competition between the shadow plant Laminum galeobdolon and the half shadow plant Stellaria holostea. Flora 172: 251±266. Shirre s DA, Bell AD Rhizome growth and clone development in Anemone nemorosa. Annals of Botany 54: 315±324. SMHI. 1997±2. VaÈder och Vatten. MaÊnadsoÈversikter. NorrkoÈ ping, Sweden: Swedish Meteorological and Hydrological Institute. Taylor OR Jr., Inouye DW Synchrony and periodicity of owering in Frasera speciosa, Gentianaceae. Ecology 66: 521±527. Tyler G Spatial sporophore pattern of ectomycorrhizal fungi in a hornbeam (Carpinus betulus) forest. Forest Ecology and Management 65: 165±17. Waller DM Models of mast fruiting in trees. Journal of Theoretical Biology 8: 223±232. Werner P, Rebele F, Bornkamm R E ects of light intensity and light quality on the growth of the shadow plant Laminum galeobdolon and the half shadow plant Stellaria holostea. Flora (Jena) 172: 235±249.