- Email: [email protected]
Environmental Control of Flowering in some NorthernCarexSpecies
Annals of Botany 79 : 319–327, 1997
Environmental Control of Flowering in some Northern Carex Species O. M. HEIDE Department of Biology and Nature Conseration, P.O. Box 5014, N-1432 Ac s, Norway Received : 17 June 1996
Accepted : 24 September 1996
The environmental control of flowering in some arctic-alpine Carex species has been studied in controlled environments. Carex nigra, C. brunnescens, C. atrata, C. norwegica and C. serotina all had a dual induction requirement for flowering. In all except C. nigra either low temperature (12 °C or lower) or short days (SD) over a wider range of temperatures were needed for primary floral induction and inflorescence formation. In C. nigra primary floral induction took place in SD only (9–21 °C), 8–10 weeks of exposure being required for a full response. In all these species long days (LD) were required for, or strongly promoted, culm elongation and inflorescence development (secondary induction). Quantitative ecotype differences in both primary and secondary induction were demonstrated. Unlike the other species, C. bicolor proved to be a regular LD plant which required LD only for inflorescence initiation and development. In all species leaf growth was strongly promoted by LD, especially in the higher temperature range (15–21 °C). In SD and temperatures below 15 °C the leaves became senescent and the plants entered a semi-dormant condition which was immediately reversed by LD. The results are discussed in relation to growth form and life history of shoots. # 1997 Annals of Botany Company Key words : Carex, dual induction, ecotypic diversity, flowering, growth, photoperiod, sedges, temperature.
INTRODUCTION The genus Carex comprises some 2000 species adapted to a wide range of climatic and edaphic conditions (Bernard, 1990). Despite their abundance and diversity as well as their importance in many ecosystems, very little is known about how flowering is controlled in these plants ; for example, the environmental control of flowering appears to have been studied experimentally only in C. bigelowii (Heide, 1992). This paper reports the results of a study of the floral induction requirements, especially of arctic-alpine species, for comparison with the dual induction requirement of most temperate grasses (Heide, 1994). Smith (1967, 1969), who studied in itro development of dissected inflorescence primordia of C. flacca and C. nigra (in some cases also C. hirta and C. panicea), observed that apices were undergoing the transition from the vegetative to the reproductive phase in late Jul. and Aug. in plants grown in the UK in an unheated greenhouse with no supplementary illumination. From preliminary observations, Smith (1969) suggested that inflorescence initiation in C. flacca and C. hirta required a number of light periods of not less than 12 h, although he also stated that no initiation took place in continuous light. However, in intact plants the young inflorescences became dormant by the end of Oct., and did not develop further until the following year (Smith, 1967). Formation of floral primordia the year before flowering is a common strategy among arctic-alpine plants adapted to a short growing season (e.g. Sørensen, 1941 ; Hodgson, 1966 ; Heide 1989, 1994), and it has also been observed in the wetland species C. lacustris and C. rostrata (Bernard, 1975, 1976) and in the dry upland species C. bigelowii (Carlsson 0305-7364}97}03031909 $25±00}0
and Callaghan, 1990). In a 5-year field study in northern Sweden the last species was found to have a low frequency of flowering and large between-year variation in flowering (Carlsson and Callaghan, 1990). Sparse and irregular flowering was also evident in this highly rhizomatous clonal species in the controlled environment experiments of Heide (1992), which demonstrated a dual induction requirement for flowering. The combination of short days (SD) and moderate temperatures for 10 or more weeks caused primary floral induction and initiation of inflorescence primordia, whereas subsequent chilling and long-day (LD) conditions stimulated culm elongation and inflorescence development (secondary induction). Temperature during SD induction proved to be very important, with an optimum at 12 to 15 °C. A strong correlation between flowering frequency (number of inflorescences) in the field and the temperature during the summer and autumn of the previous year could also be demonstrated (Heide, 1992 ; Carlsson and Callaghan, 1994). However, even the most effective phytotron conditions failed to induce flowering in all plants, and it was concluded that the high investment in vegetative reproduction in C. bigelowii seems to have developed at the expense of flowering (Heide, 1992). The three basic growth forms of Carex—matted, clumped and tussock—are mainly the result of different rhizome structures (Bernard, 1990). The matted type results from long (50–100 cm), spreading rhizomes as in C. bigelowii, whereas the contrasting tussock type is the result of very short rhizomes with more or less vertical growth. The intermediate, and most common, clumped growth form is found in species producing a varying mixture of long, spreading and short, clumping rhizomes (Bernard, 1990). It was observed by Handel (1978) that species with a compact
bo960343
# 1997 Annals of Botany Company
320
Heide—Flowering in Northern Carex Species
growth form tend to have higher rates of flowering and greater shoot production than species with long rhizomes. Because Carex shoots always die after flowering, this event has important implications for shoot longevity and life history. The present paper presents the results of experiments under controlled conditions on the control and abundance of flowering of a range of arctic-alpine Carex species varying in growth form as well as in edaphic adaptation.
inflorescence development (secondary induction). Some experiments examined the daylength requirements (number of LD cycles) for secondary induction. Percentage flowering plants and number of flowering stems per plant were used as the main criteria of flowering, while culm height and days to heading were used as additional criteria. Ten uniform plants (9 plants of C. bicolor) were used in each treatment, and the results are usually presented as means³standard error of the means (s.e.m.). With the clear-cut responses obtained, it was judged unnecessary to do further statistical analysis of the data.
MATERIALS AND METHODS Seedlings of the species and ecotypes shown in Table 1 were used for the experiments. Caryopses were collected in the field from at least 50 plants of each population. In some cases seed multiplication in the phytotron was necessary. Imbibed caryopses were chilled at 5 °C for 4 weeks and then germinated at fluctuating day}night temperatures (21}9 °C, 8}16 h). Seedlings were transplanted to 8 cm plastic pots in a standard potting compost (Einheitserde, Fruhstorfer, 1952). Except for C. bicolor, seedlings were raised at 21 °C in 24-h daylength before being exposed to a range of temperatures in short (8 h) and long days (24 h) for primary induction (Heide, 1994). C. bicolor plants were raised at 21 °C in 8-h daylength. Treatments were started after 4–5 weeks when the plants had developed about five main tiller leaves. The experiments were carried out in the A/ s phytotron under spring and summer daylight conditions. All plants received a basic illumination of 8 h daylight per day. Photoperiods of 8 and 24 h were established by moving the plants to adjacent matched growth rooms in either darkness (8-h photoperiod) or low-intensity light (5³0±05 µmol m−#s−") from 75W incandescent lamps for the rest of the day. Temperatures were controlled to ³0±5 °C and a water vapour pressure deficit of 530 Pa was maintained at all temperatures. After completion of the primary induction treatments the plants were moved to 18 °C–24-h photoperiod for
RESULTS Carex nigra Primary induction requirements were studied in two experiments. Plants from Rondane in southern Norway and Abisko in northern Sweden were exposed to a range of temperatures in SD and LD for 11 weeks. Leaf elongation was strongly inhibited by SD at all temperatures, final leaf length not exceeding 20 cm in SD, while in LD leaf length increased with increasing temperature from about 50 cm at 9 °C to 80 cm at 21 °C. At temperatures of 9 and 12 °C the leaves also became senescent in SD and, after 11 weeks, the plants had entered a semidormant state under these conditions. When transferred to 18 °C-LD the growth inhibition was immediately reversed but only those plants which had previously been grown in SD flowered (Fig. 1). The northern Abisko population had a somewhat lower temperature optimum for primary induction in SD (9–15 °C) than the more southern Rondane population. Figure 2 shows that 8–10 weeks of exposure to SD at 18 °C were required to saturate primary induction, whereas longer exposure was required at 12 °C. Dissection of a batch of plants exposed to 18 °C-SD for 10 weeks showed that the plants had formed fully differentiated inflorescence primordia in SD, but no stem elongation occurred before the plants were transferred to LD. In both populations, heading was fastest in plants
T 1 . Taxonomy, geographic origin and growth form of Carex species used for the experiments. The species are listed in order of decreasing wetness of natural growing sites. Nomenclature follows Lid and Lid (1994) Species}subspecies and geographic origin C. nigra (L.) Reichard, ssp. nigra Rondane, Ringebu, Norway Abisko, Kiruna, Sweden C. serotina Merat, ssp. serotina Vega/ r, Vega/ rshei, Norway Sagpollen, Tysfjord, Norway C. bicolor All. Børselv, Porsanger, Norway C. norwegica Retz., ssp. norwegica Rondane, Dovre, Norway C. atrata L. Rondane, Dovre, Norway C. brunnescens (Pers.) Poiret, var. brunnescens Rondane, Ringebu, Norway
Northern latitude
Altitude, (m above sea level)
Growth form
61°41« 68°21«
970 350
Matted Matted
58°47« 67°59«
190 1
Clumped Clumped
70°20«
1
Clumped
62°06«
820
Clumped
62°06«
820
Clumped
61°41«
970
Tussock
Heide—Flowering in Northern Carex Species
321
100
5
4
Flowering plants (%)
Rondane Rondane SD
3
50 Abisko Abisko
2
Flowering stems per plant
SD
1
LD
LD
0 9
12
15
18
21 9 Temperature (°C)
12
0
15
18
21
F. 1. Flowering of two populations of C. nigra at 18°C and 24-h photoperiod as affected by temperature and daylength during 11 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
18°C
5
Flowering plants (%)
4 18°C
12°C
3 50 2 12°C
Flowering stems per plant
100
1
0
0 0
4
6
8
10 0 Weeks in SD
4
6
8
10
F. 2. Flowering of C. nigra, Rondane population at 18 °C and 24-h photoperiod as affected by variation in the duration of short day (SD) primary induction at 12 and 18 °C. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
grown at 9 and 12 °C (12–13 d after transfer to 18 °C-LD) but it was progressively delayed with increasing temperature during primary induction up to 23–24 d at 21 °C. Culm height was greater in Abisko than Rondane plants, (30 s. 21 cm on average), but it was not affected by induction temperature. Carex brunnescens In this species, primary induction was governed by a pronounced interaction of temperature and daylength. At
low temperature (9 °C) primary induction was at least as effective in LD as in SD, whereas it was much reduced in LD at 15 °C and was absent in LD at 21 °C (Fig. 3). In SD, however, induction was complete at all temperatures and the number of inflorescences increased three-fold with a temperature increase from 9 to 21 °C. As in C. nigra, heading was fastest in plants from low temperature (Table 2). The very early heading in plants from 9 °C-LD indicates that stem elongation was already under way at the time of transfer to 18 °C. Culm height was little affected by daylength during primary induction, but
322
Heide—Flowering in Northern Carex Species 100
100
Flowering plants (%)
SD
50
50 LD
Flowering stems per plant
SD
LD 0
0 9
21 9 Temperature (°C)
15
15
21
F. 3. Flowering of C. brunnescens at 18 °C and 24-h photoperiod as affected by temperature and daylength during 11 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
T 2 . Effects of temperature and daylength during 11 weeks of primary induction on days to heading, culm height at anthesis and length of rosette leaes in C. brunnescens Temperature (°C)
Photoperiod (h)
Days to heading
Culm height (cm)
Leaf length (cm)
9
8 24 8 24 8 24
12±6³0±2 6±9³1±4 14±7³1±1 25±9³7±0 27±5³1±0 " 70
23±4³1±2 29±1³1±2 16±7³1±0 18±4³1±5 26±5³2±7 –
21±4³1±1 34±7³0±7 22±5³0±8 51±4³2±3 33±3³1±8 61±3³1±9
15 21
Following the primary induction, plants were transferred to 18 °C and 24-h photoperiod for secondary induction. The number of days to heading refer to the period after transfer to 18 °C. Values are means of ten plants ³s.e.m.
was less in plants from 15 °C than in those from 9 and 21 °C. Leaf length on the other hand, was much greater in LD than in SD plants, the daylength effect increasing with increasing temperature (Table 2). Carex atrata and C. norwegica These two closely-related species had almost identical primary induction requirements, with a marked interaction of temperature and daylength (Figs 4 and 5). At 9 °C primary induction was complete in both SD and LD after 9 to 10 weeks exposure. However, under LD conditions the effect was markedly reduced at 12 °C and it was totally absent at 15 °C and higher temperatures, whereas in SD, induction was unaffected by temperature or, as in C. atrata, it increased markedly with increasing temperature (inflorescence numbers, Fig. 4). Days to heading increased and
culm height decreased somewhat with increasing primary induction temperature (C. atrata, Table 3). Leaf length increased with increasing induction temperature in the LDtreated plants, but tended to decrease under the same conditions in SD. (Similar results for C. norwegica not shown).
Carex serotina (syn. C. oederi) In both populations studied, primary induction was complete after 10 weeks of exposure in both daylengths at 9 and 12 °C, while it decreased rapidly at higher temperatures, and more so under LD than SD conditions (Fig. 6). At 18 and 21 °C, only the southern Vega/ rshei population was partially induced in SD. At 9 and 12 °C, the northern Tysfjord population had the highest number of flowering stems, but this was reversed at higher temperatures (Fig. 6). An earlier experiment with the same populations and induction temperatures of 12 and 18 °C gave similar results (not shown). Even in this species heading was earliest, and the culms tallest, in plants induced at low temperatures, and heading occurred 1–2 weeks earlier in the Vega/ rshei than in the Tysfjord population, the difference increasing with increasing induction temperature. Although leaf growth was less affected by daylength in this small species than in the other species studied, the growth-inhibitory effect of SD was evident at the higher temperatures in both populations. (Results not shown). The LD requirements for secondary induction were studied in the same populations after 10 weeks of primary induction in SD at 12 °C. The results in Fig. 7 show that all plants of the Vega/ rshei population headed in continuous SD, while only 40 % of the Tysfjord population headed in SD, but heading was much delayed in SD, and the culms were
Heide—Flowering in Northern Carex Species
323
100
25 SD
15 50 SD 10 LD 5
LD
0 9
12
15
18
21 9 Temperature (°C)
12
15
Flowering stems per plant
Flowering plants (%)
20
0 18
21
F. 4. Flowering of C. atrata at 18 °C and 24-h photoperiod as affected by temperature and daylength during 9 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
100
10
50
5
SD LD
Flowering stems per plant
Flowering plants (%)
SD
LD 0
0 9
12
15
18
21 9 Temperature (°C)
12
15
18
21
F. 5. Flowering of C. norwegica at 18 °C and 24-h photoperiod as affected by temperature and daylength during 10 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
few and only 2–3 cm tall (Fig. 7). Dissection revealed that many inflorescences had aborted under continuous SD conditions. All these effects were particularly pronounced in the northern Tysfjord population which required more than 20 LD cycles for normal heading and culm elongation (Fig. 7). Carex bicolor Two experiments were carried out with this species. In a preliminary experiment plants were grown at 9, 12 and 15 °C in SD and LD. All the LD grown plants headed after
76, 51 and 38 d at 9, 12 and 15 °C, respectively, the number of culms increasing with increasing temperature (Table 4). When it was clear that all plants would flower in LD and none in SD, the SD plants were transferred to LD at 18 °C in order to determine whether induction had taken place in SD as well, i.e. whether SD were limiting for inflorescence development only, as in the other species studied. After transfer to LD, all plants headed and flowered, but only after 44 to 60 d, indicating that no induction had taken place in SD (Table 4). Therefore, in the main experiment the plants were raised
Heide—Flowering in Northern Carex Species
T 3 . Effects of temperature and daylength during 9 weeks of primary induction on days to heading, culm height at anthesis and length of rosette leaes in C. atrata Temperature (°C)
Photoperiod (h)
Days to heading
Culm height (cm)
Leaf length (cm)
9
8 24 8 24 8 24 8 24
24±5³0±8 28±6³1±7 24±0³1±5 27±8³1±8 31±5³0±8 " 70 32±9³1±2 " 70
57±9³1±3 52±4³2±5 57±8³0±2 45±0³1±3 50±4³1±1 — 43±3³1±7 —
54±6³1±0 56±8³1±2 56±8³1±7 55±2³1±4 51±1³0±9 68±5³1±8 50±8³0±9 74±4³1±4
12 15 21
Following the primary induction, plants were transfered to LD at 18 °C for secondary induction. Number of days to heading refer to the period after transfer to 18 °C. Culm height is the mean of the three tallest culms in each plant. Other values are means of ten plants ³s.e.m.
Flowering plants (%)
in SD at 21 °C and then exposed to LD for various lengths of time as shown in Fig. 8 and Table 5. Again, no heading occurred in plants maintained in SD, and flowering increased with increasing exposure to LD (Fig. 8). The LD response was strongly temperature-dependent with the fastest response at 18 and 21 °C. A high proportion of plants flowered after 4 weeks of LD exposure at 18 and 21 °C, whereas more than 4 weeks of LD exposure were required for any flowering at 12 °C, and more than 8 weeks were required at 9 °C. Thus, with increasing LD exposure, there was a gradual shift in temperature optimum to 12 °C in continuous LD. A temperature of 9 °C was, however, clearly sub-optimal even in continuous LD (Fig. 8). Similarly, culm height increased, and days to heading decreased, with increasing exposure to LD and increasing temperature up to 18 °C (Table 5).
Since no plants exposed to continuous SD flowered at any temperature (Fig. 8, Table 5), they were transferred to LD at 18 °C after 120 d for LD induction, at which stage the plants at 9 and 12 °C were semi-dormant with fully senescent leaves, and those at 15 °C partially so. When transferred to LD they immediately resumed growth, demonstrating that true dormancy had not developed. The flowering responses of the plants exposed to LD varied with the previous temperature conditions. Plants from 9, 12 and 15 °C headed within 2±5 weeks, whereas those from 18 °C headed after 5 weeks, and those from 21 °C after 8 weeks in LD (Table 6). These results indicate that, at the lower temperatures, floral induction and initiation had taken place during the 120 d SD exposure, whereas at 18 and 21 °C these events occurred after transfer to LD. However, not all plants from 9 and 12 °C flowered, possibly because of their wilted condition in SD. The number of flowering stems was highest in plants from high temperatures, whereas culm height reached an optimum at 15 °C (Table 6). DISCUSSION The results show that floral induction and development of the Carex species studied are under strict control of temperature and photoperiod. The dual induction control demonstrated in C. nigra, C. brunnescens, C. atrata, C. norwegica and C. serotina is also prevalent in temperate perennial grasses (Heide, 1994). On the other hand, the simple LD requirement found in C. bicolor is rare among northern perennial grasses (Heide, 1994). There is thus a striking similarity in the environmental mechanisms for the control of floral induction and development of northern perennial grasses and sedges. Existence of the same dual induction responses in Luzula (Salvesen, 1989) and Juncus species (O. M. Heide, unpubl. res.), suggest that this type of floral induction control is shared by most graminoid plants
100
10
50
5
0
0 9
12
15
18
21 9 Temperature (°C)
12
15
18
Flowering stems per plant
324
21
F. 6. Flowering of two populations of C. serotina (E, D, Tysfjord ; _, ^, Vega/ rshei) at 18 °C and 24-h photoperiod as affected by temperature and daylength (E, _, SD ; D, ^, LD) during 10 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
Heide—Flowering in Northern Carex Species
Tysfjord
50
5
° Vegarshei
Tysfjord
0 15
T 5 . Effects of temperature and daylength conditions on days to heading and culm height at anthesis in C. bicolor
10
° Vegarshei
Flowering stems per plant
Flowering plants (%)
100
Weeks in LD
Temperature (°C)
Days to heading
Culm height (cm)
0
9 12 15 18 21 9 12 15 18 21 9 12 15 18 21 9 12 15 18 21
" 120 " 120 " 120 " 120 " 120 " 120 " 120 81±3³1±9 40±1³2±3 31±2³2±8 " 120 62±3³6±4 49±9³2±8 36±8³1±1 38±1³2±4 112±4³4±7 74±0³2±3 47±3³2±5 35±2³0±9 38±2³1±9
— — — — — — — 2±7³0±3 7±4³0±9 14±8³1±0 — 4±0³0±3 16±1³1±9 24±4³0±9 24±1³3±0 10±3³1±9 24±2³1±7 27±0³2±2 29±7³1±7 21±7³2±1
4
8
0 81.0
50
Tysfjord
Continuous Culm height (cm)
° Vegarshei 30
9 ° Vegarshei
6
3
0
20
10
Tysfjord
0
4
Days to heading
40
12
12 16 8 20 Number of LD cycles
cont.
325
0
F. 7. Effects of increasing number of LD cycles (24 h) at 18 °C on flowering in two populations of C. serotina. (_, ^, Vega/ rshei ; +, *, Tysfjord) The plants had previously been exposed to 12 °C and 8-h photoperiod for 10 weeks for primary induction. (cont. ¯ continuous LD treatment). Open symbols and broken lines refer to the right axis.
of high-latitude and alpine origin. The dual control mechanism provides a high degree of reliability in the synchronization of plant development with seasonal climatic fluctuations (Heide, 1994), and it may also prove to be quite common among high-latitude perennial herbs (e.g. Heide,
Culm height refers to the tallest culm per plant. Values are means of nine plants ³s.e.m.
Pedersen and Dahl, 1990 ; Heide, 1995). The dual induction response is also compatible with the observations by Smith (1967, 1969) on flowering control in C. nigra and C. flacca. In contrast to the sparse and erratic flowering of C. bigelowii under the same conditions (Heide, 1992), flowering was regular and could be fully controlled in the present species. Even the closely-related C. nigra was distinct from C. bigelowii in this respect. In accordance with the observations of Handel (1978), fertility seemed to vary with the growth form of the species. Thus, the loosely-matted C. nigra had the lowest number of culms per plant, whereas C. brunnescens, which forms dense, flat tussocks, had by far the highest number, with up to 80 culms per plant, and the clumped species had intermediate numbers (Figs 1, 3–8). This variation agrees well with the fertility of the same species under natural conditions in the field (Lye, 1993). The sparsely, and irregularly, flowering C. bigelowii has even more vigorously spreading rhizomes than C. nigra, and the
T 4 . Effects of temperature and daylength conditions on flowering in C. bicolor Days to heading Temperature (°C)
Day-length conditions
Flowering plants (%)
9
LD–LD SD–LD LD–LD SD–LD LD–LD SD–LD
100 100 100 100 100 100
12 15
Flowering stems per plant
Culm height (cm)
from start
from transfer
3±8³0±5 1±8³0±3 9±3³1±3 2±7³0±7 11±0³0±7 7±3³0±9
24±5³3±9 11±0³5±5 31±8³0±6 17±3³4±9 32±5³1±6 22±8³1±7
76±0³3±4 110±0³0±7 51±5³3±4 118±0³9±5 37±8³4±9 127±5³3±8
— 44±0³0±7 — 51±0³9±5 — 60±5³3±8
The SD-LD plants were transfered to LD at 18 °C after 67 SD, whereas the LD–LD plants were maintained in LD at the respective temperatures throughout. Values are means of five plants ³s.e.m.
326
Heide—Flowering in Northern Carex Species Continuous LD
100
10
8 weeks LD 8 weeks LD
5
50 4 weeks LD 4 weeks LD
Continuous SD
Flowering stems per plant
Flowering plants (%)
Continuous LD
Continuous SD 0
0 9
12
15
18
21 9 Temperature (°C)
12
15
18
21
F. 8. Effects of temperature and daylength conditions on flowering in C. bicolor. The plants were maintained at the respective temperatures until anthesis or for up to 120 d if flowering had not occurred earlier. Values are means of nine plants ³s.e.m.
T 6 . Effects of temperature and daylength on flowering in C. bicolor Temperature (°C)
Flowering plants (%)
Flowering stems per plant
Days to heading
Culm height (cm)
9 12 15 18 21
45 78 100 100 100
0±4³0±3 2±1³0±7 5±4³0±6 6±7³1±4 8±0³2±1
16±3³2±8 16±9³3±3 18±2³1±3 34±8³4±3 56±0³2±4
7±8³1±2 13±1³2±1 19±4³1±7 16±6³1±5 14±8³1±3
Plants were grown in 8-h photoperiod at the temperatures indicated for 120 d and then transfered to 24-h photoperiod at 18 °C. Number of days to heading refer to the period after transfer to LD. Culm height refers to the tallest culm per plant. Values are means of nine plants ³s.e.m.
results thus support the hypothesis that a high investment in vegetative reproduction and spread may occur at the expense of flowering (Heide, 1992). It is possible to envisage a hormonal basis for such a relationship, with rhizome growth and flowering being controlled by a balance of growth-promoting and florigenic hormonal factors. Shoot and leaf growth were also strictly controlled by daylength and temperature (e.g. Tables 2–4), in a way that explains much of the growth rhythm of the sedges. Most temperate and arctic Carex species produce a large proportion of their shoots during late summer and autumn (Bernard, 1990). Due to the prevailing SD and low temperature, these pseudoculms will elongate very little in the autumn, but provided they have reached the critical size, they will undergo primary induction and form inflorescence primordia which, after overwintering will elongate and flower under the influence of the increasing daylength and temperature of the next spring and summer. For example, Bernard (1975) found a strong positive relationship between shoot length and basal diameter, and the presence of
inflorescences, in overwintering shoots of C. lacustris. However, shoots emerging in spring and midsummer, which elongated under the influence of LD, did not initiate inflorescence primordia but died in late autumn. Clearly, the time of appearance is crucial for the fate and life history of each shoot, the governing factor being the seasonal changes in daylength and temperature. Due to the dual floral induction control of most Carex species, the resulting winter requirement for primary induction, and the death of shoots after flowering, the individual shoot will have a biennial life cycle. This agrees with measurements of maximum shoot life spans of 14–24 months in a range of Carex species from temperate sites (Bernard, 1990). Because of high shoot mortality in many species, most shoots will not reach this age. However, Alexeev (1988) noted that many species of arctic-alpine regions have shoots that can survive for up to 5–7 years (cf. Callaghan, 1976 ; Solander, 1983). In such regions, with low temperature and short growing seasons, the shoots may need several years to reach the necessary size and ripeness to respond to inductive conditions. Alexeev (1988) found that species needing 7–8 years to flower in the field may, under cultivation, begin flowering in 3 years and, under optimal conditions in the phytotron the whole life cycle of species requiring dual induction can be completed in about 20 weeks. In species with simple LD induction such as C. bicolor, the individual shoot will have an annual life cycle, emerging in the spring and flowering the same year. Thus, in plants growing under natural LD in the phytotron during summer, new shoots flowered in succession as they emerged throughout the summer. In such species and under optimal conditions a shoot can complete the entire life cycle in about 10 weeks. These results do not indicate any connection between flowering response or rate of flowering, and taxonomic grouping or edaphic adaptation in these sedges. The species are distributed over four of the five commonly-recognized
Heide—Flowering in Northern Carex Species taxonomic sub-groups of Carex (Lid and Lid, 1994), and they show widely-different adaptations to moisture and soil conditions (Table 1 ; Lye, 1993 ; Lid and Lid, 1994). For example, the two dry-land species C. bigelowii and C. brunnescens present opposite extremes in fertility among the species studied. In the wetland species C. lacustris, Bernard (1975) observed a marked increase in flowering if the water table in the marsh was high the previous year. Although flooding may influence floral induction in such wet-land species, the abundant flowering of the dry upland species C. brunnescens indicates that this is not a general feature of sedges. On the other hand, in C. nigra and C. serotina, in which ecotypic variation was studied (Figs 1 and 6), marked differences were found which can be related to temperature and daylength conditions at the latitudes of origin of the ecotypes. Such ecotypic diversity is widespread in temperate grasses (e.g. Ha/ bjørg, 1979 ; Heide, 1994), and the results suggest that it may be common in Carex species as well. Not surprisingly, temperature and light climate appear to have been much more powerful than edaphic factors in the adaptation of plant development to local environmental conditions. Controlled environment experiments can provide important information on how these factors regulate growth and flowering patterns of the sedges and should therefore be extended to a wider range of species. A C K N O W L E D G E M E N TS I thank Professor KA Lye for verification of the taxonomic identity of the Carex species, as well as seed collection, and Mr K Pedersen for excellent technical assistance with the experiments. LITERATURE CITED Alexeev YE. 1988. Ontogenesis in Carex species. Aquatic Botany 30 : 39–48. Bernard JM. 1975. The life history of shoots of Carex lacustris. Canadian Journal of Botany 53 : 256–260. Bernard JM. 1976. The life history and population dynamics of shoots of Carex rostrata. Journal of Ecology 64 : 1045–1048.
327
Bernard JM. 1990. Life history and vegetative reproduction in Carex. Canadian Journal of Botany 68 : 1441–1448. Callaghan TV. 1976. Growth and population dynamics of Carex bigelowii in an alpine environment. Oikos 27 : 402–413. Carlsson BAI , Callaghan TV. 1990. Effects of flowering on the shoot dynamics of Carex bigelowii along an altitudinal gradient in Swedish Lapland. Journal of Ecology 78 : 152–165. Carlsson BAI , Callaghan TV. 1994. Impact of climatic change factors on the clonal sedge Carex bigelowii : implications for population growth and vegetative spread. Ecography 17 : 321–330. Frustorfer A. 1952. Die Entwicklung der Einheitserde. Gartenwelt 52 : 270–271. Ha/ bjørg A. 1979. Floral differentiation and development of selected ecotypes of Poa pratensis L. cultivated at six localities in Norway. Meldinger fra Norges landbrukshøgskole 58 (4) : 1–19. Handel SN. 1978. On the competitive relationship of three woodland sedges and its bearing on the evolution of ant-dispersal of Carex pendunculata. Eolution 32 : 151–163. Heide OM. 1989. Environmental control of flowering and viviparous proliferation in seminiferous and viviparous arctic populations of two Poa species. Arctic and Alpine Research 21 : 305–315. Heide OM. 1992. Experimental control of flowering in Carex bigelowii. Oikos 65 : 371–376. Heide OM. 1994. Control of flowering and reproduction in temperate grasses. The New Phytologist 128 : 347–362. Heide OM. 1995. Dual induction control of flowering in Leucanthemum ulgare. Physiologia Plantarum 95 : 159–165. Heide OM, Pedersen K, Dahl E. 1990. Environmental control of flowering and morphology in the high-arctic Cerastium regelii, and the taxonomic status of C. jenisejense. Nordic Journal of Botany 10 : 141–147. Hodgson HJ. 1966. Floral initiation in Alaskan gramineae. Botanical Gazette 127 : 64–70. Lid J, Lid DT. 1994. Norsk flora. Oslo : Det Norske Samlaget, pp. 776–835. Lye KA. 1993. Diaspore production in Norwegian Cyperaceae. Lidia 3 : 81–108. Salvesen PH. 1989. Sammenlignende dyrkingsforsøk med so$ rvestkyst– skyende planter. 2. Forsøk i kontrollert klima. Blyttia 47 : 143–153. Smith DL. 1967. The experimental control of inflorescence development in Carex. Annals of Botany 31 : 19–30. Smith DL. 1969. The role of leaves and roots in the control of inflorescence development in Carex. Annals of Botany 33 : 505–514. Solander L. 1983. Biomass and shoot production of Carex rostrata and Equisetum fluiatile in fertilized and unfertilized subarctic lakes. Aquatic Botany 15 : 349–366. Sørensen T. 1941. Temperature relations and phenology of the northeast Greenland flowering plants. Meddelelser om GroX nland 125 : 1–305.
Environmental Control of Flowering in some Northern Carex Species O. M. HEIDE Department of Biology and Nature Conseration, P.O. Box 5014, N-1432 Ac s, Norway Received : 17 June 1996
Accepted : 24 September 1996
The environmental control of flowering in some arctic-alpine Carex species has been studied in controlled environments. Carex nigra, C. brunnescens, C. atrata, C. norwegica and C. serotina all had a dual induction requirement for flowering. In all except C. nigra either low temperature (12 °C or lower) or short days (SD) over a wider range of temperatures were needed for primary floral induction and inflorescence formation. In C. nigra primary floral induction took place in SD only (9–21 °C), 8–10 weeks of exposure being required for a full response. In all these species long days (LD) were required for, or strongly promoted, culm elongation and inflorescence development (secondary induction). Quantitative ecotype differences in both primary and secondary induction were demonstrated. Unlike the other species, C. bicolor proved to be a regular LD plant which required LD only for inflorescence initiation and development. In all species leaf growth was strongly promoted by LD, especially in the higher temperature range (15–21 °C). In SD and temperatures below 15 °C the leaves became senescent and the plants entered a semi-dormant condition which was immediately reversed by LD. The results are discussed in relation to growth form and life history of shoots. # 1997 Annals of Botany Company Key words : Carex, dual induction, ecotypic diversity, flowering, growth, photoperiod, sedges, temperature.
INTRODUCTION The genus Carex comprises some 2000 species adapted to a wide range of climatic and edaphic conditions (Bernard, 1990). Despite their abundance and diversity as well as their importance in many ecosystems, very little is known about how flowering is controlled in these plants ; for example, the environmental control of flowering appears to have been studied experimentally only in C. bigelowii (Heide, 1992). This paper reports the results of a study of the floral induction requirements, especially of arctic-alpine species, for comparison with the dual induction requirement of most temperate grasses (Heide, 1994). Smith (1967, 1969), who studied in itro development of dissected inflorescence primordia of C. flacca and C. nigra (in some cases also C. hirta and C. panicea), observed that apices were undergoing the transition from the vegetative to the reproductive phase in late Jul. and Aug. in plants grown in the UK in an unheated greenhouse with no supplementary illumination. From preliminary observations, Smith (1969) suggested that inflorescence initiation in C. flacca and C. hirta required a number of light periods of not less than 12 h, although he also stated that no initiation took place in continuous light. However, in intact plants the young inflorescences became dormant by the end of Oct., and did not develop further until the following year (Smith, 1967). Formation of floral primordia the year before flowering is a common strategy among arctic-alpine plants adapted to a short growing season (e.g. Sørensen, 1941 ; Hodgson, 1966 ; Heide 1989, 1994), and it has also been observed in the wetland species C. lacustris and C. rostrata (Bernard, 1975, 1976) and in the dry upland species C. bigelowii (Carlsson 0305-7364}97}03031909 $25±00}0
and Callaghan, 1990). In a 5-year field study in northern Sweden the last species was found to have a low frequency of flowering and large between-year variation in flowering (Carlsson and Callaghan, 1990). Sparse and irregular flowering was also evident in this highly rhizomatous clonal species in the controlled environment experiments of Heide (1992), which demonstrated a dual induction requirement for flowering. The combination of short days (SD) and moderate temperatures for 10 or more weeks caused primary floral induction and initiation of inflorescence primordia, whereas subsequent chilling and long-day (LD) conditions stimulated culm elongation and inflorescence development (secondary induction). Temperature during SD induction proved to be very important, with an optimum at 12 to 15 °C. A strong correlation between flowering frequency (number of inflorescences) in the field and the temperature during the summer and autumn of the previous year could also be demonstrated (Heide, 1992 ; Carlsson and Callaghan, 1994). However, even the most effective phytotron conditions failed to induce flowering in all plants, and it was concluded that the high investment in vegetative reproduction in C. bigelowii seems to have developed at the expense of flowering (Heide, 1992). The three basic growth forms of Carex—matted, clumped and tussock—are mainly the result of different rhizome structures (Bernard, 1990). The matted type results from long (50–100 cm), spreading rhizomes as in C. bigelowii, whereas the contrasting tussock type is the result of very short rhizomes with more or less vertical growth. The intermediate, and most common, clumped growth form is found in species producing a varying mixture of long, spreading and short, clumping rhizomes (Bernard, 1990). It was observed by Handel (1978) that species with a compact
bo960343
# 1997 Annals of Botany Company
320
Heide—Flowering in Northern Carex Species
growth form tend to have higher rates of flowering and greater shoot production than species with long rhizomes. Because Carex shoots always die after flowering, this event has important implications for shoot longevity and life history. The present paper presents the results of experiments under controlled conditions on the control and abundance of flowering of a range of arctic-alpine Carex species varying in growth form as well as in edaphic adaptation.
inflorescence development (secondary induction). Some experiments examined the daylength requirements (number of LD cycles) for secondary induction. Percentage flowering plants and number of flowering stems per plant were used as the main criteria of flowering, while culm height and days to heading were used as additional criteria. Ten uniform plants (9 plants of C. bicolor) were used in each treatment, and the results are usually presented as means³standard error of the means (s.e.m.). With the clear-cut responses obtained, it was judged unnecessary to do further statistical analysis of the data.
MATERIALS AND METHODS Seedlings of the species and ecotypes shown in Table 1 were used for the experiments. Caryopses were collected in the field from at least 50 plants of each population. In some cases seed multiplication in the phytotron was necessary. Imbibed caryopses were chilled at 5 °C for 4 weeks and then germinated at fluctuating day}night temperatures (21}9 °C, 8}16 h). Seedlings were transplanted to 8 cm plastic pots in a standard potting compost (Einheitserde, Fruhstorfer, 1952). Except for C. bicolor, seedlings were raised at 21 °C in 24-h daylength before being exposed to a range of temperatures in short (8 h) and long days (24 h) for primary induction (Heide, 1994). C. bicolor plants were raised at 21 °C in 8-h daylength. Treatments were started after 4–5 weeks when the plants had developed about five main tiller leaves. The experiments were carried out in the A/ s phytotron under spring and summer daylight conditions. All plants received a basic illumination of 8 h daylight per day. Photoperiods of 8 and 24 h were established by moving the plants to adjacent matched growth rooms in either darkness (8-h photoperiod) or low-intensity light (5³0±05 µmol m−#s−") from 75W incandescent lamps for the rest of the day. Temperatures were controlled to ³0±5 °C and a water vapour pressure deficit of 530 Pa was maintained at all temperatures. After completion of the primary induction treatments the plants were moved to 18 °C–24-h photoperiod for
RESULTS Carex nigra Primary induction requirements were studied in two experiments. Plants from Rondane in southern Norway and Abisko in northern Sweden were exposed to a range of temperatures in SD and LD for 11 weeks. Leaf elongation was strongly inhibited by SD at all temperatures, final leaf length not exceeding 20 cm in SD, while in LD leaf length increased with increasing temperature from about 50 cm at 9 °C to 80 cm at 21 °C. At temperatures of 9 and 12 °C the leaves also became senescent in SD and, after 11 weeks, the plants had entered a semidormant state under these conditions. When transferred to 18 °C-LD the growth inhibition was immediately reversed but only those plants which had previously been grown in SD flowered (Fig. 1). The northern Abisko population had a somewhat lower temperature optimum for primary induction in SD (9–15 °C) than the more southern Rondane population. Figure 2 shows that 8–10 weeks of exposure to SD at 18 °C were required to saturate primary induction, whereas longer exposure was required at 12 °C. Dissection of a batch of plants exposed to 18 °C-SD for 10 weeks showed that the plants had formed fully differentiated inflorescence primordia in SD, but no stem elongation occurred before the plants were transferred to LD. In both populations, heading was fastest in plants
T 1 . Taxonomy, geographic origin and growth form of Carex species used for the experiments. The species are listed in order of decreasing wetness of natural growing sites. Nomenclature follows Lid and Lid (1994) Species}subspecies and geographic origin C. nigra (L.) Reichard, ssp. nigra Rondane, Ringebu, Norway Abisko, Kiruna, Sweden C. serotina Merat, ssp. serotina Vega/ r, Vega/ rshei, Norway Sagpollen, Tysfjord, Norway C. bicolor All. Børselv, Porsanger, Norway C. norwegica Retz., ssp. norwegica Rondane, Dovre, Norway C. atrata L. Rondane, Dovre, Norway C. brunnescens (Pers.) Poiret, var. brunnescens Rondane, Ringebu, Norway
Northern latitude
Altitude, (m above sea level)
Growth form
61°41« 68°21«
970 350
Matted Matted
58°47« 67°59«
190 1
Clumped Clumped
70°20«
1
Clumped
62°06«
820
Clumped
62°06«
820
Clumped
61°41«
970
Tussock
Heide—Flowering in Northern Carex Species
321
100
5
4
Flowering plants (%)
Rondane Rondane SD
3
50 Abisko Abisko
2
Flowering stems per plant
SD
1
LD
LD
0 9
12
15
18
21 9 Temperature (°C)
12
0
15
18
21
F. 1. Flowering of two populations of C. nigra at 18°C and 24-h photoperiod as affected by temperature and daylength during 11 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
18°C
5
Flowering plants (%)
4 18°C
12°C
3 50 2 12°C
Flowering stems per plant
100
1
0
0 0
4
6
8
10 0 Weeks in SD
4
6
8
10
F. 2. Flowering of C. nigra, Rondane population at 18 °C and 24-h photoperiod as affected by variation in the duration of short day (SD) primary induction at 12 and 18 °C. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
grown at 9 and 12 °C (12–13 d after transfer to 18 °C-LD) but it was progressively delayed with increasing temperature during primary induction up to 23–24 d at 21 °C. Culm height was greater in Abisko than Rondane plants, (30 s. 21 cm on average), but it was not affected by induction temperature. Carex brunnescens In this species, primary induction was governed by a pronounced interaction of temperature and daylength. At
low temperature (9 °C) primary induction was at least as effective in LD as in SD, whereas it was much reduced in LD at 15 °C and was absent in LD at 21 °C (Fig. 3). In SD, however, induction was complete at all temperatures and the number of inflorescences increased three-fold with a temperature increase from 9 to 21 °C. As in C. nigra, heading was fastest in plants from low temperature (Table 2). The very early heading in plants from 9 °C-LD indicates that stem elongation was already under way at the time of transfer to 18 °C. Culm height was little affected by daylength during primary induction, but
322
Heide—Flowering in Northern Carex Species 100
100
Flowering plants (%)
SD
50
50 LD
Flowering stems per plant
SD
LD 0
0 9
21 9 Temperature (°C)
15
15
21
F. 3. Flowering of C. brunnescens at 18 °C and 24-h photoperiod as affected by temperature and daylength during 11 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
T 2 . Effects of temperature and daylength during 11 weeks of primary induction on days to heading, culm height at anthesis and length of rosette leaes in C. brunnescens Temperature (°C)
Photoperiod (h)
Days to heading
Culm height (cm)
Leaf length (cm)
9
8 24 8 24 8 24
12±6³0±2 6±9³1±4 14±7³1±1 25±9³7±0 27±5³1±0 " 70
23±4³1±2 29±1³1±2 16±7³1±0 18±4³1±5 26±5³2±7 –
21±4³1±1 34±7³0±7 22±5³0±8 51±4³2±3 33±3³1±8 61±3³1±9
15 21
Following the primary induction, plants were transferred to 18 °C and 24-h photoperiod for secondary induction. The number of days to heading refer to the period after transfer to 18 °C. Values are means of ten plants ³s.e.m.
was less in plants from 15 °C than in those from 9 and 21 °C. Leaf length on the other hand, was much greater in LD than in SD plants, the daylength effect increasing with increasing temperature (Table 2). Carex atrata and C. norwegica These two closely-related species had almost identical primary induction requirements, with a marked interaction of temperature and daylength (Figs 4 and 5). At 9 °C primary induction was complete in both SD and LD after 9 to 10 weeks exposure. However, under LD conditions the effect was markedly reduced at 12 °C and it was totally absent at 15 °C and higher temperatures, whereas in SD, induction was unaffected by temperature or, as in C. atrata, it increased markedly with increasing temperature (inflorescence numbers, Fig. 4). Days to heading increased and
culm height decreased somewhat with increasing primary induction temperature (C. atrata, Table 3). Leaf length increased with increasing induction temperature in the LDtreated plants, but tended to decrease under the same conditions in SD. (Similar results for C. norwegica not shown).
Carex serotina (syn. C. oederi) In both populations studied, primary induction was complete after 10 weeks of exposure in both daylengths at 9 and 12 °C, while it decreased rapidly at higher temperatures, and more so under LD than SD conditions (Fig. 6). At 18 and 21 °C, only the southern Vega/ rshei population was partially induced in SD. At 9 and 12 °C, the northern Tysfjord population had the highest number of flowering stems, but this was reversed at higher temperatures (Fig. 6). An earlier experiment with the same populations and induction temperatures of 12 and 18 °C gave similar results (not shown). Even in this species heading was earliest, and the culms tallest, in plants induced at low temperatures, and heading occurred 1–2 weeks earlier in the Vega/ rshei than in the Tysfjord population, the difference increasing with increasing induction temperature. Although leaf growth was less affected by daylength in this small species than in the other species studied, the growth-inhibitory effect of SD was evident at the higher temperatures in both populations. (Results not shown). The LD requirements for secondary induction were studied in the same populations after 10 weeks of primary induction in SD at 12 °C. The results in Fig. 7 show that all plants of the Vega/ rshei population headed in continuous SD, while only 40 % of the Tysfjord population headed in SD, but heading was much delayed in SD, and the culms were
Heide—Flowering in Northern Carex Species
323
100
25 SD
15 50 SD 10 LD 5
LD
0 9
12
15
18
21 9 Temperature (°C)
12
15
Flowering stems per plant
Flowering plants (%)
20
0 18
21
F. 4. Flowering of C. atrata at 18 °C and 24-h photoperiod as affected by temperature and daylength during 9 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
100
10
50
5
SD LD
Flowering stems per plant
Flowering plants (%)
SD
LD 0
0 9
12
15
18
21 9 Temperature (°C)
12
15
18
21
F. 5. Flowering of C. norwegica at 18 °C and 24-h photoperiod as affected by temperature and daylength during 10 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
few and only 2–3 cm tall (Fig. 7). Dissection revealed that many inflorescences had aborted under continuous SD conditions. All these effects were particularly pronounced in the northern Tysfjord population which required more than 20 LD cycles for normal heading and culm elongation (Fig. 7). Carex bicolor Two experiments were carried out with this species. In a preliminary experiment plants were grown at 9, 12 and 15 °C in SD and LD. All the LD grown plants headed after
76, 51 and 38 d at 9, 12 and 15 °C, respectively, the number of culms increasing with increasing temperature (Table 4). When it was clear that all plants would flower in LD and none in SD, the SD plants were transferred to LD at 18 °C in order to determine whether induction had taken place in SD as well, i.e. whether SD were limiting for inflorescence development only, as in the other species studied. After transfer to LD, all plants headed and flowered, but only after 44 to 60 d, indicating that no induction had taken place in SD (Table 4). Therefore, in the main experiment the plants were raised
Heide—Flowering in Northern Carex Species
T 3 . Effects of temperature and daylength during 9 weeks of primary induction on days to heading, culm height at anthesis and length of rosette leaes in C. atrata Temperature (°C)
Photoperiod (h)
Days to heading
Culm height (cm)
Leaf length (cm)
9
8 24 8 24 8 24 8 24
24±5³0±8 28±6³1±7 24±0³1±5 27±8³1±8 31±5³0±8 " 70 32±9³1±2 " 70
57±9³1±3 52±4³2±5 57±8³0±2 45±0³1±3 50±4³1±1 — 43±3³1±7 —
54±6³1±0 56±8³1±2 56±8³1±7 55±2³1±4 51±1³0±9 68±5³1±8 50±8³0±9 74±4³1±4
12 15 21
Following the primary induction, plants were transfered to LD at 18 °C for secondary induction. Number of days to heading refer to the period after transfer to 18 °C. Culm height is the mean of the three tallest culms in each plant. Other values are means of ten plants ³s.e.m.
Flowering plants (%)
in SD at 21 °C and then exposed to LD for various lengths of time as shown in Fig. 8 and Table 5. Again, no heading occurred in plants maintained in SD, and flowering increased with increasing exposure to LD (Fig. 8). The LD response was strongly temperature-dependent with the fastest response at 18 and 21 °C. A high proportion of plants flowered after 4 weeks of LD exposure at 18 and 21 °C, whereas more than 4 weeks of LD exposure were required for any flowering at 12 °C, and more than 8 weeks were required at 9 °C. Thus, with increasing LD exposure, there was a gradual shift in temperature optimum to 12 °C in continuous LD. A temperature of 9 °C was, however, clearly sub-optimal even in continuous LD (Fig. 8). Similarly, culm height increased, and days to heading decreased, with increasing exposure to LD and increasing temperature up to 18 °C (Table 5).
Since no plants exposed to continuous SD flowered at any temperature (Fig. 8, Table 5), they were transferred to LD at 18 °C after 120 d for LD induction, at which stage the plants at 9 and 12 °C were semi-dormant with fully senescent leaves, and those at 15 °C partially so. When transferred to LD they immediately resumed growth, demonstrating that true dormancy had not developed. The flowering responses of the plants exposed to LD varied with the previous temperature conditions. Plants from 9, 12 and 15 °C headed within 2±5 weeks, whereas those from 18 °C headed after 5 weeks, and those from 21 °C after 8 weeks in LD (Table 6). These results indicate that, at the lower temperatures, floral induction and initiation had taken place during the 120 d SD exposure, whereas at 18 and 21 °C these events occurred after transfer to LD. However, not all plants from 9 and 12 °C flowered, possibly because of their wilted condition in SD. The number of flowering stems was highest in plants from high temperatures, whereas culm height reached an optimum at 15 °C (Table 6). DISCUSSION The results show that floral induction and development of the Carex species studied are under strict control of temperature and photoperiod. The dual induction control demonstrated in C. nigra, C. brunnescens, C. atrata, C. norwegica and C. serotina is also prevalent in temperate perennial grasses (Heide, 1994). On the other hand, the simple LD requirement found in C. bicolor is rare among northern perennial grasses (Heide, 1994). There is thus a striking similarity in the environmental mechanisms for the control of floral induction and development of northern perennial grasses and sedges. Existence of the same dual induction responses in Luzula (Salvesen, 1989) and Juncus species (O. M. Heide, unpubl. res.), suggest that this type of floral induction control is shared by most graminoid plants
100
10
50
5
0
0 9
12
15
18
21 9 Temperature (°C)
12
15
18
Flowering stems per plant
324
21
F. 6. Flowering of two populations of C. serotina (E, D, Tysfjord ; _, ^, Vega/ rshei) at 18 °C and 24-h photoperiod as affected by temperature and daylength (E, _, SD ; D, ^, LD) during 10 weeks of primary induction. Data from ten plants per treatment. Vertical bars denote ³s.e.m.
Heide—Flowering in Northern Carex Species
Tysfjord
50
5
° Vegarshei
Tysfjord
0 15
T 5 . Effects of temperature and daylength conditions on days to heading and culm height at anthesis in C. bicolor
10
° Vegarshei
Flowering stems per plant
Flowering plants (%)
100
Weeks in LD
Temperature (°C)
Days to heading
Culm height (cm)
0
9 12 15 18 21 9 12 15 18 21 9 12 15 18 21 9 12 15 18 21
" 120 " 120 " 120 " 120 " 120 " 120 " 120 81±3³1±9 40±1³2±3 31±2³2±8 " 120 62±3³6±4 49±9³2±8 36±8³1±1 38±1³2±4 112±4³4±7 74±0³2±3 47±3³2±5 35±2³0±9 38±2³1±9
— — — — — — — 2±7³0±3 7±4³0±9 14±8³1±0 — 4±0³0±3 16±1³1±9 24±4³0±9 24±1³3±0 10±3³1±9 24±2³1±7 27±0³2±2 29±7³1±7 21±7³2±1
4
8
0 81.0
50
Tysfjord
Continuous Culm height (cm)
° Vegarshei 30
9 ° Vegarshei
6
3
0
20
10
Tysfjord
0
4
Days to heading
40
12
12 16 8 20 Number of LD cycles
cont.
325
0
F. 7. Effects of increasing number of LD cycles (24 h) at 18 °C on flowering in two populations of C. serotina. (_, ^, Vega/ rshei ; +, *, Tysfjord) The plants had previously been exposed to 12 °C and 8-h photoperiod for 10 weeks for primary induction. (cont. ¯ continuous LD treatment). Open symbols and broken lines refer to the right axis.
of high-latitude and alpine origin. The dual control mechanism provides a high degree of reliability in the synchronization of plant development with seasonal climatic fluctuations (Heide, 1994), and it may also prove to be quite common among high-latitude perennial herbs (e.g. Heide,
Culm height refers to the tallest culm per plant. Values are means of nine plants ³s.e.m.
Pedersen and Dahl, 1990 ; Heide, 1995). The dual induction response is also compatible with the observations by Smith (1967, 1969) on flowering control in C. nigra and C. flacca. In contrast to the sparse and erratic flowering of C. bigelowii under the same conditions (Heide, 1992), flowering was regular and could be fully controlled in the present species. Even the closely-related C. nigra was distinct from C. bigelowii in this respect. In accordance with the observations of Handel (1978), fertility seemed to vary with the growth form of the species. Thus, the loosely-matted C. nigra had the lowest number of culms per plant, whereas C. brunnescens, which forms dense, flat tussocks, had by far the highest number, with up to 80 culms per plant, and the clumped species had intermediate numbers (Figs 1, 3–8). This variation agrees well with the fertility of the same species under natural conditions in the field (Lye, 1993). The sparsely, and irregularly, flowering C. bigelowii has even more vigorously spreading rhizomes than C. nigra, and the
T 4 . Effects of temperature and daylength conditions on flowering in C. bicolor Days to heading Temperature (°C)
Day-length conditions
Flowering plants (%)
9
LD–LD SD–LD LD–LD SD–LD LD–LD SD–LD
100 100 100 100 100 100
12 15
Flowering stems per plant
Culm height (cm)
from start
from transfer
3±8³0±5 1±8³0±3 9±3³1±3 2±7³0±7 11±0³0±7 7±3³0±9
24±5³3±9 11±0³5±5 31±8³0±6 17±3³4±9 32±5³1±6 22±8³1±7
76±0³3±4 110±0³0±7 51±5³3±4 118±0³9±5 37±8³4±9 127±5³3±8
— 44±0³0±7 — 51±0³9±5 — 60±5³3±8
The SD-LD plants were transfered to LD at 18 °C after 67 SD, whereas the LD–LD plants were maintained in LD at the respective temperatures throughout. Values are means of five plants ³s.e.m.
326
Heide—Flowering in Northern Carex Species Continuous LD
100
10
8 weeks LD 8 weeks LD
5
50 4 weeks LD 4 weeks LD
Continuous SD
Flowering stems per plant
Flowering plants (%)
Continuous LD
Continuous SD 0
0 9
12
15
18
21 9 Temperature (°C)
12
15
18
21
F. 8. Effects of temperature and daylength conditions on flowering in C. bicolor. The plants were maintained at the respective temperatures until anthesis or for up to 120 d if flowering had not occurred earlier. Values are means of nine plants ³s.e.m.
T 6 . Effects of temperature and daylength on flowering in C. bicolor Temperature (°C)
Flowering plants (%)
Flowering stems per plant
Days to heading
Culm height (cm)
9 12 15 18 21
45 78 100 100 100
0±4³0±3 2±1³0±7 5±4³0±6 6±7³1±4 8±0³2±1
16±3³2±8 16±9³3±3 18±2³1±3 34±8³4±3 56±0³2±4
7±8³1±2 13±1³2±1 19±4³1±7 16±6³1±5 14±8³1±3
Plants were grown in 8-h photoperiod at the temperatures indicated for 120 d and then transfered to 24-h photoperiod at 18 °C. Number of days to heading refer to the period after transfer to LD. Culm height refers to the tallest culm per plant. Values are means of nine plants ³s.e.m.
results thus support the hypothesis that a high investment in vegetative reproduction and spread may occur at the expense of flowering (Heide, 1992). It is possible to envisage a hormonal basis for such a relationship, with rhizome growth and flowering being controlled by a balance of growth-promoting and florigenic hormonal factors. Shoot and leaf growth were also strictly controlled by daylength and temperature (e.g. Tables 2–4), in a way that explains much of the growth rhythm of the sedges. Most temperate and arctic Carex species produce a large proportion of their shoots during late summer and autumn (Bernard, 1990). Due to the prevailing SD and low temperature, these pseudoculms will elongate very little in the autumn, but provided they have reached the critical size, they will undergo primary induction and form inflorescence primordia which, after overwintering will elongate and flower under the influence of the increasing daylength and temperature of the next spring and summer. For example, Bernard (1975) found a strong positive relationship between shoot length and basal diameter, and the presence of
inflorescences, in overwintering shoots of C. lacustris. However, shoots emerging in spring and midsummer, which elongated under the influence of LD, did not initiate inflorescence primordia but died in late autumn. Clearly, the time of appearance is crucial for the fate and life history of each shoot, the governing factor being the seasonal changes in daylength and temperature. Due to the dual floral induction control of most Carex species, the resulting winter requirement for primary induction, and the death of shoots after flowering, the individual shoot will have a biennial life cycle. This agrees with measurements of maximum shoot life spans of 14–24 months in a range of Carex species from temperate sites (Bernard, 1990). Because of high shoot mortality in many species, most shoots will not reach this age. However, Alexeev (1988) noted that many species of arctic-alpine regions have shoots that can survive for up to 5–7 years (cf. Callaghan, 1976 ; Solander, 1983). In such regions, with low temperature and short growing seasons, the shoots may need several years to reach the necessary size and ripeness to respond to inductive conditions. Alexeev (1988) found that species needing 7–8 years to flower in the field may, under cultivation, begin flowering in 3 years and, under optimal conditions in the phytotron the whole life cycle of species requiring dual induction can be completed in about 20 weeks. In species with simple LD induction such as C. bicolor, the individual shoot will have an annual life cycle, emerging in the spring and flowering the same year. Thus, in plants growing under natural LD in the phytotron during summer, new shoots flowered in succession as they emerged throughout the summer. In such species and under optimal conditions a shoot can complete the entire life cycle in about 10 weeks. These results do not indicate any connection between flowering response or rate of flowering, and taxonomic grouping or edaphic adaptation in these sedges. The species are distributed over four of the five commonly-recognized
Heide—Flowering in Northern Carex Species taxonomic sub-groups of Carex (Lid and Lid, 1994), and they show widely-different adaptations to moisture and soil conditions (Table 1 ; Lye, 1993 ; Lid and Lid, 1994). For example, the two dry-land species C. bigelowii and C. brunnescens present opposite extremes in fertility among the species studied. In the wetland species C. lacustris, Bernard (1975) observed a marked increase in flowering if the water table in the marsh was high the previous year. Although flooding may influence floral induction in such wet-land species, the abundant flowering of the dry upland species C. brunnescens indicates that this is not a general feature of sedges. On the other hand, in C. nigra and C. serotina, in which ecotypic variation was studied (Figs 1 and 6), marked differences were found which can be related to temperature and daylength conditions at the latitudes of origin of the ecotypes. Such ecotypic diversity is widespread in temperate grasses (e.g. Ha/ bjørg, 1979 ; Heide, 1994), and the results suggest that it may be common in Carex species as well. Not surprisingly, temperature and light climate appear to have been much more powerful than edaphic factors in the adaptation of plant development to local environmental conditions. Controlled environment experiments can provide important information on how these factors regulate growth and flowering patterns of the sedges and should therefore be extended to a wider range of species. A C K N O W L E D G E M E N TS I thank Professor KA Lye for verification of the taxonomic identity of the Carex species, as well as seed collection, and Mr K Pedersen for excellent technical assistance with the experiments. LITERATURE CITED Alexeev YE. 1988. Ontogenesis in Carex species. Aquatic Botany 30 : 39–48. Bernard JM. 1975. The life history of shoots of Carex lacustris. Canadian Journal of Botany 53 : 256–260. Bernard JM. 1976. The life history and population dynamics of shoots of Carex rostrata. Journal of Ecology 64 : 1045–1048.
327
Bernard JM. 1990. Life history and vegetative reproduction in Carex. Canadian Journal of Botany 68 : 1441–1448. Callaghan TV. 1976. Growth and population dynamics of Carex bigelowii in an alpine environment. Oikos 27 : 402–413. Carlsson BAI , Callaghan TV. 1990. Effects of flowering on the shoot dynamics of Carex bigelowii along an altitudinal gradient in Swedish Lapland. Journal of Ecology 78 : 152–165. Carlsson BAI , Callaghan TV. 1994. Impact of climatic change factors on the clonal sedge Carex bigelowii : implications for population growth and vegetative spread. Ecography 17 : 321–330. Frustorfer A. 1952. Die Entwicklung der Einheitserde. Gartenwelt 52 : 270–271. Ha/ bjørg A. 1979. Floral differentiation and development of selected ecotypes of Poa pratensis L. cultivated at six localities in Norway. Meldinger fra Norges landbrukshøgskole 58 (4) : 1–19. Handel SN. 1978. On the competitive relationship of three woodland sedges and its bearing on the evolution of ant-dispersal of Carex pendunculata. Eolution 32 : 151–163. Heide OM. 1989. Environmental control of flowering and viviparous proliferation in seminiferous and viviparous arctic populations of two Poa species. Arctic and Alpine Research 21 : 305–315. Heide OM. 1992. Experimental control of flowering in Carex bigelowii. Oikos 65 : 371–376. Heide OM. 1994. Control of flowering and reproduction in temperate grasses. The New Phytologist 128 : 347–362. Heide OM. 1995. Dual induction control of flowering in Leucanthemum ulgare. Physiologia Plantarum 95 : 159–165. Heide OM, Pedersen K, Dahl E. 1990. Environmental control of flowering and morphology in the high-arctic Cerastium regelii, and the taxonomic status of C. jenisejense. Nordic Journal of Botany 10 : 141–147. Hodgson HJ. 1966. Floral initiation in Alaskan gramineae. Botanical Gazette 127 : 64–70. Lid J, Lid DT. 1994. Norsk flora. Oslo : Det Norske Samlaget, pp. 776–835. Lye KA. 1993. Diaspore production in Norwegian Cyperaceae. Lidia 3 : 81–108. Salvesen PH. 1989. Sammenlignende dyrkingsforsøk med so$ rvestkyst– skyende planter. 2. Forsøk i kontrollert klima. Blyttia 47 : 143–153. Smith DL. 1967. The experimental control of inflorescence development in Carex. Annals of Botany 31 : 19–30. Smith DL. 1969. The role of leaves and roots in the control of inflorescence development in Carex. Annals of Botany 33 : 505–514. Solander L. 1983. Biomass and shoot production of Carex rostrata and Equisetum fluiatile in fertilized and unfertilized subarctic lakes. Aquatic Botany 15 : 349–366. Sørensen T. 1941. Temperature relations and phenology of the northeast Greenland flowering plants. Meddelelser om GroX nland 125 : 1–305.