Global Change Biology (1997) 3 (Suppl. 1), 74–79
Response to simulated climatic change in an alpine and subarctic pollen-risk strategist, Silene acaulis J . M . A L A T A L O 1 and Ø . T O T L A N D 2 1Department of Systematic Botany, Goteborg University, Carl Skottsbergs Gata 22B, SE-413 19 Goteborg, Sweden ¨ ¨ 2Botanical Institute, University of Bergen, Allegaten 41, N-5007 Bergen, Norway
Abstract The aim of this study was to test if early flowering species respond with increased seed production to climate warming as is predicted for late-flowering seed-risk strategists. Experimental climate warming of about 3°C was applied to two populations of the cushion-forming plant Silene acaulis (L.) Jacq. The experiment was run at one subarctic site and one alpine site for 2 years and 1 year, respectively, using open-top chambers (OTC). The 2-year temperature enhancement at the subarctic site had a marked effect on the flowering phenology. Cushions inside the OTC started flowering substantially earlier than control cushions. Both the male and female phases developed faster in the OTCs, and maturation of capsules occurred earlier. The cushions also responded positively in reproductive terms and produced more mature seeds and had a higher seed/ovule ratio. After 1 year temperature enhancement at the alpine site there was a weak trend for earlier flowering, but there was no significant difference in seed production or seed/ ovule ratio. Keywords: climate change, Silene acaulis, reproductive biology, ITEX, subarctic, alpine
Introduction Arctic and alpine plant species vary considerably in their phenology, allocation, and growth. Consequently, they should also vary in their response to climatic warming (Shaver & Kummerow 1992). A study by Kummerow & Ellis (1984) on two arctic sedges suggested that higher mean temperatures in the Arctic will cause a sharp increase in sedge biomass production, and that a larger fraction of the photosynthates will be allocated to the root system. The fact that arctic and alpine plant species vary considerably in their response to experimental warming (Chapin & Shaver 1985) makes it necessary to gather more information in order to make predictions about the possible effect that climatic warming will have on arctic and alpine ecosystems. Wookey et al. (1994) showed that reproductive and vegetative development of Polygonum viviparum in a high arctic semi-desert (Svalbard) react differently to an increase in mean temperature during the growing season. Reproductive development increased significantly, but there was no significant effect on vegetative parameters. The effect of climate warming may differ between alpine, subarctic and high arctic sites and different species will respond Correspondence: J. Alatalo, fax: 146-31-773-2677, e-mail:
[email protected] © 1997 Blackwell Science Ltd.
differently. High arctic Dryas octopetala in Svalbard increased its seed production in response to experimental warming (Welker et al. 1997), whereas subarctic Empetrum hermaphroditum (Abisko, Northern Sweden) did not (Wookey et al. 1993). Vegetative growth of Cassiope tetragona responded positively to nutrient addition only at one subarctic heath site in Northern Sweden, whereas increased temperature and not nutrient addition enhanced growth at another nearby fell field site, and at a high arctic heath site on Svalbard (Havstro¨m et al. 1993). The response of arctic and alpine plant species to climate warming in terms of reproduction may also depend on the species flowering time (Molau 1993a). Early-flowering species possess several mechanisms to increase outbreeding rate; such as low self-compatibility, herkogamy, or diclinous mating systems, whereas lateflowering strategists can not afford waiting for pollinator agents, and are therefore highly self-compatible (Molau 1993a). Thus, early-flowering species have large losses of potential offspring every year due to high abortion rates, whereas in late-flowering species the seed set is drastically reduced in some years because of unsuitable climatic conditions (Molau 1993a). Since alpine and arctic species do not fit well into the
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C L I M AT E C H A N G E R E S P O N S E I N S I L E N E A C A U L I S classical r–K model (MacArthur & Wilson 1967), Molau (1993a) proposed a new classification for these different life-history strategies in alpine and arctic areas based on their correlation to flowering phenology (early- vs. lateflowering), i.e. the ‘pollen-risking’ and ‘seed-risking’ strategies. From these different strategies, it can be hypothesized that an eventual climate warming will alter the seed pool in alpine and arctic areas. Late-flowering seedrisk strategists are hypothesized to increase their seed production over time due to a prolonged vegetation period (Molau 1993a), whereas early-flowering pollenrisk strategists might not increase their seed production to the same extent, as early flowering pollen-risk strategists are not limited by time for ripening of seeds but instead by availability of pollinator agents. If earlyflowering species will not respond to climate warming in terms of seed production, the composition of alpine and arctic vegetation may eventually change in favour of late-flowering species, assuming that genet establishment and seed production are correlated. In the present study we examine the potential effect of climate warming on the flowering phenology and reproduction of Silene acaulis, an early-flowering species that can be classified as a pollen-risk strategist (Molau 1993a). S. acaulis occurs abundantly in alpine and arctic areas in the northern hemisphere, permitting the comparison of potential responses to global warming in an alpine and subarctic site. Specifically the following two questions were addressed: 1 Does an experimentally induced temperature enhancement influence the flowering phenology of S. acaulis? 2 Are there differences in fruit and seed production between cushions of S. acaulis experiencing an increased temperature, and control cushions?
Materials and methods Study area The study was carried out on two populations during 1994. One population was situated in northernmost Sweden at Latnjajaure Field Station (LFS) in the valley of Latnjavagge (68°21’N, 18°30’E c. 1000 m a.s.l.). The valley is snow-covered for most of the year, and the climate can be classified as middle arctic (Polunin 1951). The mean temperatures for the period June, July, and August in 1991–1993 were 4.3, 7.4, and 6.9°C, respectively, and the mean precipitation for the same period was, 45.3, 80.3, and 53.9 mm, respectively. The other study population was situated at Mt Sandalsnut, Finse, Hardangervidda, southwest Norway (60°37’N, 7°32’E). The climate in the Finse area may be characterized as alpine–oceanic, with relatively cold and rainy summers. Monthly average temperatures for
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June, July, and August, are 4.7, 8.0, and 7.5°C, respectively. Monthly average precipitation for the same months are 77, 115, and 116 mm, respectively (data from a Norwegian Meteorological Station at Finse, 1200 m a.s.l.). The studied population occurs at the south face of Mt Sandalsnut in the middle alpine zone, at an altitude of 1500 m a.s.l.
Study species Silene acaulis (L.) Jacq. (Caryophyllaceae) is a common cushion-forming plant in alpine and arctic open tundra areas throughout the northern hemisphere. It is a longlived perennial that forms light green moss-like cushions with pink flowers. The flowers have a continuous yellowish nectar band at the base of the petals (Swales 1979). S. acaulis is polymorphic with monoecious (Warming 1920), andromonoecious (Warming 1920), trioecious (Warming 1920, Philipp et al. 1990, Alatalo & Molau 1995), dioecious (Warming 1920) and gynodioecious (Shykoff 1988, Såstad 1991) populations reported. The hermaphrodites enter the male phase first, i.e. they are protandrous. In alpine areas bees and syrphids are known to visit them (Knuth 1908), but in alpine Norway and arctic areas they are mostly visited by dipteran species and less frequently by bumblebees and butterflies (Totland 1993). The S. acaulis population at Latnjavagge is trioecious and consists of female, male and hermaphrodite individuals. The population consists of mostly female and hermaphrodite individuals and has a slight female bias; male individuals are rare (Alatalo & Molau 1995). During 1994 the most frequent potential pollinator visitors to S. acaulis were dipteran species, but in other years bumblebee species are frequent visitors (JM Alatalo, unpublished data). The majority of the S. acaulis cushions at the Finse site are females and hermaphrodites. At the site S. acaulis initiate flowering rapidly after snowmelt (Totland 1993). Flies within the Anthomyiide and Muscidae families are the most frequent flower visitors (Totland 1993).
Temperature manipulations To increase the temperature to a similar level that is predicted to occur in 50 years (Bretherton et al. 1990, Mitchell et al. 1990), we used open-top chambers (OTCs) that have been specially designed for that purpose (Marion 1996) within The International Tundra Experiment (ITEX, Molau & Mølgaard 1996, Henry & Molau 1997). OTCs were built in a hexagonal design with a 60° incline of the sides. We used 30-cm-high OTCs with a 50-cm opening at the top made by Sun-Lite HP™ (3 mm thick), a fibreglass material (Solar Components Corp., Manchester, NH, USA) especially designed for solar
© 1997 Blackwell Science Ltd., Global Change Biology, 3 (Suppl. 1), 74–79
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J . M . A L ATA L O & Ø . T O T L A N D
applications. The material has a high solar transmittance in the visible wavelengths (86%) and a low transmittance in the infra-red (heat) range (,5%) (Marion 1996). The OTCs at Latnjavagge were left outside during the whole year starting from 1993, whereas those at Finse were erected immediately after snowmelt in 1994. The temperature was only enhanced during the snow-free period of the year.
Phenological and reproductive measurements At LFS the experiment was set up directly after snow-melt in late May 1993; 20 cushions of S. acaulis were marked both in OTCs and in control plots at an already ongoing ITEX study, four cushions in each of the five OTCs, and five control plots, respectively. The OTCs and control plots were organized in five pairs, each pair consisting of one OTC with four cushions and one control plot with four cushions. The following (ITEX) measures were monitored daily: 1 thawing date (Julian day—snow free), 2 number of days from thawing to first open flower (thaw—first open flower), 3 number of days from thawing to first open anther shedding pollen, 4 number of days from thawing to first stigma receptive, 5 number of days from thawing to capsule maturation (see Molau & Edlund 1996, for more details). Ten randomly selected capsules (or all if the number of capsules were fewer than 10) were collected for the reproductive measurements when the capsules were mature (when capsules started to open at apex). At Finse, 40 hermaphroditic cushions of S. acaulis were selected on 6 July 1994; 20 of them for OTC treatment (one cushion in each OTC), and 20 of them for control plots (one cushion in each plot); these were organized in 20 pairs of treatment/control. The members of each pair were separated by 1.5 to 3 m. None of the plants had initiated flowering and few buds had emerged. The members of a pair were randomly assigned to a treatment or a control group. OTCs were erected over each of the treatment cushions on 6 July. The number of open flowers on each cushion was counted every 3–5 days as time limitation prevented a daily visit to this site. On 31 August 1994 the number of capsules on each cushion was counted. Ten randomly selected capsules (or all if the number of capsules were fewer than 10) were collected on the same day the size of the cushions was measured. It is important to note that the plants at Finse were subjected to only one season of experimental warming, whereas those at LFS experienced two seasons of warming.
Statistical analysis For the data from LFS, the mean data from each of the four cushions within each plot were pooled into mean values
for each plot, whereas in Finse mean values were obtained from the single cushion in each plot. Treatment effect on quantitative reproductive characters were analysed by Analysis of Variance (ANOVA, Sokal & Rohlf 1981) using StatView 4.5 software for PowerMacintosh. No statistical analyses was performed on the phenological data since they are dependent on each other; further, no statistical analyses were performed on differences between sites since they were not receiving comparable treatments (1-year compared to 2-year effect at year of study).
Results Effect on phenology At LFS the cushions inside the OTCs thawed on average 2 days earlier than the cushions in the control plots (Table 1). Start of flowering occurred on average 7 days earlier in OTCs than in control plots (Table 1), start of male phase (first open anther) occurred in average 11 days earlier in the OTCs than in control plots (Table 1), while start of female phase (first receptive stigma) and capsule maturation occurred on average 7 days earlier in OTCs than in control plots (Table 1). Comparable phenological data from Finse are lacking due to time limitation. At Finse, peak flowering of OTC plants occurred c. 3 days earlier than for control plants (Fig. 1).
Effect on quantitative reproductive traits Cushions inside OTCs produced significantly more mature seeds than cushions in control plots at LFS (P50.002, Tables 2, 3) but not at Finse (P.0.50, Tables 2, 3). There was no significant difference at either site in number of undeveloped seeds (LFS, P50.15; Finse, P50.95, Tables 2, 3), or number of ovules (LFS, P50.20; Finse, P.0.50, Tables 2, 3). There was a significantly higher seed/ovule ratio of cushions in OTCs at LFS (P50.008, Tables 2, 3) but not at Finse (P.0.50, Tables 2, 3). No significant difference was found in seed weight (LFS, P50.44; Finse, P50.38, Tables 2, 3).
Discussion Effect on micro-climate The OTCs increase the average summer air temperature by c. 2 -3°C (U Nordenha¨ll, personal communication; Marion et al. 1997), which is within the range that is predicted for the average summer temperature increase in the Arctic (Mitchell et al. 1990). Since the OTCs work in a passive way, they had no impact on the winter air temperature that is predicted to have even greater increase than the summer air temperature (Mitchell et al. 1990). Winter temperatures
© 1997 Blackwell Science Ltd., Global Change Biology, 3 (Suppl. 1), 74–79
C L I M AT E C H A N G E R E S P O N S E I N S I L E N E A C A U L I S Table 1 Two-year effect on phenological and reproductive traits of Silene acaulis in controls and OTCs at Latnjavagge, northern Sweden. Mean values of thawing date (julian day), first flower open, start of male phase, start of female phase and capsule maturation (no. days from thawing date). Treatment Thawing date Control OTC First open flower Control OTC Start of male phase Control OTC Start of female phase Control OTC Capsule maturation Control OTC
n
Mean
SD
5 5
137.2 135.4
4.324 2.702
5 5
40.4 33.9
2.818 3.484
3 5
47.5 35.2
3.279 6.181
5 5
45.6 37.3
6.576 3.258
4 5
96.8 88.8
6.791 5.679
Fig. 1 One-year effect on flowering phenology of manipulated (OTC) and control plants of Silene acaulis at Finse, southwest Norway, in 1994.
above the snow-cover probably do not have any large effect on Silene acaulis, which typically grows on snow-covered sites. The cushions inside the OTCs at LFS did however thaw on average 2 days earlier than the controls, which is in line with predictions on earlier onset of growing season (Maxwell 1992). In May, the radiation is already strong, enabling the OTCs to heat up to a level above ambient air temperature from the moment they will appear from the embedding snow. The higher air temperature in the OTCs will cause the snow in the OTCs to melt faster than the surrounding snow cover.
Effect on phenology and quantitative reproductive traits The increase of temperature had a marked short-term (2 years) effect on the phenology of Silene acaulis at
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LFS. Cushions inside the OTCs started flowering on average 7 days earlier than cushions in the control plots. Both the male and female (stigmas receptive) phases developed earlier in the OTCs. Male phase was reached on average 11 days earlier in OTCs, and the female phase on average 7 days earlier. This affected the ripening of the seeds, and maturation of capsules started (capsules opened in the top) on average 7 days earlier in the OTCs. Apparently the seeds did not develop faster within the OTCs; the earlier maturation of capsules was the only function of earlier receptivity of the stigmas. These results are consistent with similar experiments from Svalbard, where the temperature was increased by 3.5°C (Wookey et al. 1993, Welker et al. 1997). Flowering of Dryas octopetala in the ‘tented’ plots started earlier than the untreated plots, furthermore the ‘tented’ plots had higher seed set and higher number of reproductive shoots (both those setting seed and those that had flowered without setting seed). The long-term effect of climatic warming on phenology will probably not differ from the short-term effect as phenology is probably not as dependent as quantitative reproductive characters such as capsule or seed number on resource availability. Instead, phenology has been shown to correlate with snowmelt (Kudo 1991) and temperature (Fitter et al. 1995; Le´vesque et al. 1997). Comparison of phenological responses of S. acaulis between LFS and Finse are difficult because different measurements were done, and because the plants at Finse were not warmed for as long as at LFS. However, the OTC plants at Finse reached peak flowering only about 3 days earlier than the control plants. Thus, it seems that the effect of the temperature enhancement treatment was not as pronounced at this site as at LFS. Cushions in OTCs produced on average significantly more developed seeds at LFS site but not at Finse; this may be the result of the one ‘extra’ season of temperature treatment that the LFS population received. The seed : ovule ratio was also on average significantly higher in the OTCs at LFS but not at Finse. This experiment showed that the early-flowering pollen-risk strategy (sensu Molau 1993a) that S. acaulis possesses can respond positively in terms of seed production to climate change. S. acaulis responded both in phenological traits and in quantitative reproductive traits at LFS. Thus, the predictions that early flowering species might suffer a disadvantage against late-flowering species might not hold true (Molau 1993). The question whether or not the increase in production of mature seeds in pollen-risk strategists will be enough to balance the hypothesized increase in seed production of lateflowering seed-risk strategists (Molau 1993) needs further studies. Climate change will probably also increase the number of pollinator-agents for the pollen-
© 1997 Blackwell Science Ltd., Global Change Biology, 3 (Suppl. 1), 74–79
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Table 2 ANOVA table for treatment effect on mean number of developed seeds, seed : ovule ratio, mean total number of ovules, mean number of undeveloped seeds and mean seed weight of Silene acaulis at Latnjavagge (2-year effect), northern Sweden and Finse (1-year effect), southwestern Norway, in 1994. Mean data for plots used for all anlyses. Latnjavagge Source of variation Developed seeds Treatment Residual Seed : ovule ratio Treatment Residual Total ovule number Treatment Residual Undeveloped seeds Treatment Residual Mean seed weight Treatment Residual
Finse
df
MS
F
P
df
F
P
1 8
32.873 1.691
19.438
0.002
1 16
3.693 9.380
0.394
0.54
1 8
0.055 0.004
12.422
0.008
1 16
0.006 0.025
0.246
0.63
1 8
5.628 2.903
1.939
0.20
1 16
2.816 15.978
0.176
0.68
1 8
11.295 4.380
2.579
0.15
1 16
0.062 14.591
0.004
0.95
1 8
0.001 0.002
0.670
0.44
1 16
0.008 0.010
0.798
0.38
MS
Table 3 Treatment effect on quantitative reproductive traits of controls and OTCs. Mean number of developed seeds, seed : ovule ratio, mean total number of ovules, mean number of undeveloped seeds, and mean seed weight of Silene acaulis at Latnjavagge (2-year effect), northern Sweden, and Finse (1-year effect), southwestern Norway. Latnjavagge Treatment Developed seeds Control OTC Seed : ovule ratio Control OTC Total ovule number Control OTC Undeveloped seeds Control OTC Mean seed weight (mg) Control OTC
Finse
n
Mean
SD
n
Mean
5 5
6.172 9.798
1.291 1.310
9 9
5.661 4.755
1.933 3.876
5 5
0.294 0.443
0.067 0.067
9 9
0.318 0.282
0.109 0.194
5 5
21.317 22.817
1.778 1.626
9 9
17.885 17.094
3.399 4.517
5 5
15.144 13.019
2.407 1.722
9 9
12.223 12.341
3.111 4.416
5 5
0.320 0.295
0.027 0.012
9 9
0.249 0.291
0.057 0.130
risk strategists in alpine and arctic areas, which in turn could further increase their seed production over time. An increase in temperature in the future will probably have the result of increasing overall seed production in alpine and arctic regions. The larger seed production does not automatically result in higher establishment of mature plants. Survival and establishment of the seedlings will depend on competition to established individuals: the increase in temperature may enhance vegetative growth of several plant species (Henry &
SD
Molau 1997), seedling establishment might instead decrease even though seed production increases.
Acknowledgements The authors thank the Abisko and Finse Scientific Research Stations and their staff for help and hospitality, Tho´ra Ellen Tho´rhallsdo´ttir and others at University of Iceland for providing room, equipment, and hospitality (for JMA), and Urban Nordenha¨ll, Priitta Po¨yhta¨ri, Karin Lindstro¨m, Anna Lindskog, and Tomas Pa¨rn for assistance in the field. Ulf Molau, Inga-Svala
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C L I M AT E C H A N G E R E S P O N S E I N S I L E N E A C A U L I S Jo´nsdo´ttir, Mats Havstro¨m and Jaqui Shykoff gave constructive criticism on an earlier draft of the manuscript. This study was supported by grants from the Royal Swedish Academy of Science ¨ verskotts(to JMA), Helge Ax:son Johnsons fond (to JMA), O fonden, University of Go¨teborg (JMA), Abisko Scientific Research Station (to JMA), P.A. Larssons stipendiefond, University of Go¨teborg (to JMA), Nordisk Forskerutdannings Akademi (NorFA; to JMA), and an NFR grant (no: 101535/720) to ØT are all gratefully acknowledged.
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