337
Germinability of arctic plants is high in perceived
optimal conditions but low in the field
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Eike Müller, Elisabeth J. Cooper, and Inger Greve Alsos
Abstract: Sexual reproduction is crucial for plant populations to track and adapt to climate change, but it is uncertain to
what degree arctic vascular plants reproduce by seed. Several studies on arctic species show low germination. To re-examine
seed germination and evaluate factors limiting sexual reproduction, seeds of 6–22 arctic species were germinated in five different, increasingly more realistic, conditions. Thirteen out of 15 species that were tested in an earlier study in Svalbard,
Norway, germinated better in our study. Compared with perceived optimal conditions in a growth chamber, average germination per species was 6%–52% lower in five out of six species germinating at a colder temperature in soil, 36%–64% lower
when germinating outdoors in soil, 49%–91% lower when germinating in a moss covered moraine, and 55%–91% lower
when germinating in open soil on a moraine. Germination outdoors was below 5% in 10 out of 13 species and not correlated to germination in perceived optimal conditions. The high germination compared with earlier studies suggests that climate warming has already increased seed viability. However, caution should be taken when evaluating species-recruitment
potential based on laboratory studies, as germination in the field was limited by species-specific responses to low temperatures, moisture, predation, and safe-site availability.
Key words: arctic, germination, seeds, Svalbard, temperature, tundra.
Résumé : La reproduction sexuelle joue un rôle crucial chez les populations végétales permettant aux plantes de repérer et
de s'adapter au changement climatique, mais l'on ne sait pas à quel point les plantes vasculaires arctiques se reproduisent
par des graines. Plusieurs études sur les espèces arctiques témoignent de leur faible germination. Afin de réexaminer la germination des graines et d'évaluer les facteurs limitant la reproduction sexuelle, les auteurs ont fait germer les semences de
22 espèces arctiques sous cinq conditions différentes de plus en plus réalistes. Treize des 15 espèces préalablement testées
au Svalbard, Norvège, ont mieux germé dans cette étude. Comparée afin de percevoir les conditions optimales en chambre
de croissance, la germination moyenne par espèce a été de 6%–52 % plus faible chez cinq des six espèces à une température
plus froide dans le sol, de 36%–64% plus faible lorsque réalisée à l'extérieur dans le sol, de 49%–91% plus faible lorsqu'effectuée sur un sol de moraine couvert de mousse, et de 55%–91% lorsqu la germination a été faite sur un sol ouvert de moraine. La germination à l'extérieure est inférieure à 5% chez 10 des 13 espèces et ne montre pas de corrélation avec les
conditions optimales telles que perçues. La forte germination comparativement aux études antécédentes suggère que le réchauffement climatique aurait déjà augmenté la viabilité des graines. Cependant, on doit être prudent lorsqu'on évalue le recrutement potentiel des espèces, basé sur des études en laboratoire, puisque la germination sur le terrain est limitée par des
réactions spécifiques à l'espèce envers la basse température, l'humidité, la prédation et la disponibilité de sites sûrs.
Mots‐clés : arctique, germination, semences, Svalbard, température, toundra.
[Traduit par la Rédaction]
Introduction
It has been claimed that the importance of sexual reproduction in vascular plants is lower in arctic regions (Billings
and Mooney 1968; Born and Böcher 2001; but see Murray
1987) than at lower latitudes (Söyrinki 1939; Welling and
Laine 2000). This assumption is based on several types of
evidence. In arctic habitats, a lower proportion of species
seem to produce viable seeds (Sørensen 1941; Eurola 1972)
than in the northern boreal – alpine zone (Söyrinki 1939;
Bliss 1958), and arctic seeds seem to have poorer germination than seeds from the northern boreal – alpine zone (Bliss
1958; Eurola 1972). Additionally, it has been suggested that
a high proportion of arctic species are capable of reproducing
vegetatively (Billings and Mooney 1968; Billings 1987). The
numbers of seedlings encountered in most arctic habitats and
in seed addition experiments in the Arctic are low (Bell and
Bliss 1980; Klokk and Rønning 1987; Bliss and Gold 1999;
Received 1 December 2010. Accepted 3 March 2011. Published at www.nrcresearchpress.com/cjb on .
E. Müller. The University Centre in Svalbard (UNIS), Post Office Box 156, NO-9171 Longyearbyen, Norway; Department of Arctic and
Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, NO-9037 Tromsø, Norway.
E.J. Cooper. Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, NO9037 Tromsø, Norway.
I.G. Alsos. The University Centre in Svalbard (UNIS), Post Office Box 156, NO-9171 Longyearbyen, Norway; Tromsø University
Museum, NO-9037 Tromsø, Norway.
Corresponding author: Eike Müller (e-mail: [email protected]).
Botany 89: 337–348 (2011)
doi:10.1139/B11-022
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338
Cooper et al. 2004, but see Speed et al. 2010). It also has
been assumed that there are energetic advantages of asexual
reproduction (Chapin et al. 1980). Contrary to studies postulating low seed viability, low germination, and high proportions of clonal reproduction, other studies report medium to
high germination percentages of arctic species (Mooney and
Billings 1961; Bell and Bliss 1980; Bliss and Gold 1999; Hagen 2002). Also, many arctic species have high levels of genetic diversity (reviewed by Brochmann and Brysting 2008).
Even predominantly clonally reproducing species (Bistorta
vivipara (L.) S.F. Gray (Bauert 1996) and Saxifraga cernua
L. (Gabrielsen and Brochmann 1998)) and some northern
range populations of higher temperature demanding species
that have never been observed with ripe seeds in the Arctic
(Alsos et al. 2003) have medium to high levels of genetic diversity (Alsos and Engelskjøn 2002). Thus, sexual reproduction in the Arctic may be more frequent than previously
assumed.
We assume that the variation in germination rates observed
in different studies can be attributed to factors such as species
studied, temperature during seed development, pregermination treatment and dormancy state of the seeds, germination
temperature, water, substrate, and light conditions. Each of
these factors can reduce germination and increase variability
of germination success. Knowledge about germination and
pregermination treatment of seeds (storage, desiccation tolerance, and stratification) has improved, especially over the
past 30 years (Baskin and Baskin 1998; Tweddle et al. 2003;
Fenner and Thompson 2005). Hence, some of the low germination percentages reported in early studies may be caused
by inappropriate storage conditions or ineffective dormancybreaking methods.
The importance of temperature during seed production and
germination in arctic vascular plants has been demonstrated
in earlier studies. Experiments show that elevated temperatures result in increased seed production (Arft et al. 1999)
and also in higher germinability of seeds (Wookey et al.
1995). Temperature is also an indicator of the time of year
and may determine the timing of germination (Baskin and
Baskin 1998). Several studies show that temperature during
germination and germination success are positively correlated
in arctic and subarctic species (Mooney and Billings 1961;
Trudgill et al. 2000; Milbau et al. 2009). Many arctic species
germinate best at temperatures between 12 °C and 20 °C
(Mooney and Billings 1961; Bell and Bliss 1980).
Other studies have shown that light (Milberg et al. 2000),
water (Harper and Benton 1966), and substrate (Bell and
Bliss 1980), in addition to temperature, may affect germination. Most arctic species are either weakly affected or unaffected by light conditions (Bliss 1958). Responses to drought
stress vary between species; most common is a reduced viability and slower germination speed (Fenner and Thompson
2005). Substrate seems to be of lesser importance for seed
germination than temperature and water availability in laboratory experiments (Baskin and Baskin 1998). Under optimized
temperature and moisture conditions, using nondormant or
broken-dormancy seeds, one may expect that 100% of the
viable seeds will germinate. Germination percentages, therefore, reflect the proportion of viable seeds produced by a
plant population.
In contrast with germination in controlled laboratory ex-
Botany, Vol. 89, 2011
periments, germination under natural conditions in the Arctic
encounters many uncontrollable factors, e.g., low temperatures, wind, predation, and drought. The effect of substrate
may interact with temperature and moisture, and favorable
conditions for germination are often patchy and found in microsites, such as small cracks or moss mats, but rarely on exposed ridges (Bell and Bliss 1980; Svoboda and Henry
1987). Similarly, predation is heterogeneous and after primary dispersal, seeds may be subjected to discovery and consumption by avian predators (Holmes and Froud-Williams
2005). High wind speeds, in particular where vegetation is
sparse, not only relocate seeds after primary dispersal (Chambers and MacMahon 1994), but may also prevent germination
through seed burial in deep soil and increase seedling mortality by substrate removal and abrasion (Maun 1994). The few
seed-addition experiments in arctic areas report that germination in the field is very low (Bell and Bliss 1980; Klokk and
Rønning 1987), and plant establishment is only possible in
favorable years (Svoboda and Henry 1987).
About 165 native vascular plant species occur on the arctic
archipelago of Svalbard, Norway (Elven and Elvebakk 1996;
Alsos et al. 2010), where this study was conducted. Based on
observations in the field and studies partly from other regions, it is assumed that 60.2% of the vascular plants in Svalbard mainly reproduce sexually (Brochmann and Steen
1999). Based on genetic studies, Alsos et al. (2007) hypothesized that the establishment phase of reproduction (germination, survival, and local reproduction) limits vascular plant
colonization on Svalbard. However, the only comprehensive
study to date on germination of seeds collected in Svalbard
showed that 30% of 63 tested species did not germinate, and
the majority of the species had very low (<10%) germination
(Eurola 1972).
The first objective in this study was to examine if previous
studies in the Arctic, and especially in Svalbard, underestimated seed germination. Secondly, through a stepwise design, we investigated how germination changed by adding
natural factors, such as low temperature, wind, moisture limitation, and predation. In addition, we tested if germination
percentages in field conditions are correlated with germination percentages in perceived optimal conditions.
Material and methods
Collection of seeds
Seeds of the 22 most common species, including bulbils
from B. vivipara and S. cernua (hereafter included in the
term seeds) were collected between 22 August and 20
September 2007 in Adventdalen surrounding Longyearbyen
(78°13′N, 15°39′E), Svalbard (Fig. 1; Table 1). For some
species only a few seeds were found. For these species, seeds
were collected in several lowland locations near Longyearbyen and were mixed before germination (Table 1). The
collection site in Endalen is a very sheltered slope with a
southeast exposure and alternating Dryas and Cassiope
heath. Erigeron humilis R.C. Graham was collected in a
snow bed, and Luzula confusa Lindeb. was collected on an
exposed ridge in Endalen. The collection site at Hotellnesset
is a more open, plain habitat with sandy substrate, and the
vegetation is dominated by Silene acaulis (L.) Jacq. and Saxifraga oppositifolia L. Adventdalen is not as sheltered as EnPublished by NRC Research Press
Müller et al.
339
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Fig. 1. Maps of the Svalbard archipelago (left) and Adventdalen (right) showing where seeds were collected for germination experiments, and
where germination experiments in the field were performed.
dalen but provides habitats with higher soil moisture than at
Hotellnesset. Dryas octopetala L., L. confusa, and Luzula
nivalis (Laest.) Spreng. are the dominant species at the collection site in Adventdalen. All sites are classified as Cassiope tetragona L.D. Don. tundra (Elvebakk 2005), which
corresponds to the Cassiopo tetragonae – Dryadetum octopetalae (Hadač 1946), a vegetation type characteristic for bioclimatic zone C.
Pregermination treatment
All seeds were collected into paper bags. In the laboratory,
they were cleaned, counted into batches of 30 or 50 seeds,
and packed into coffee filter bags. From the end of September 2007 until germination at the start of spring 2008
(Table 2), the seeds were kept in an open cardboard box outdoors in Longyearbyen, Svalbard, at ambient temperatures to
experience natural temperature and moisture conditions. Between the end of storage and the start of the germination test
(Table 2), the seeds were stored at 1 °C. Species were allocated to the experiments based on seed availability.
Germination under perceived optimal conditions
(experiment 1)
Based on germination trials of Alsos et al. (2003), Cooper
et al. (2004), and Cooper (unpublished, 2001), 18 °C was
used as the perceived optimal temperature (Table 2). Boxes
were prepared with a water reservoir to keep filter papers
moist. Three replicates of 50 seeds for each species were
laid on filter papers (grade 1, Whatman, Maidstone, UK).
Every batch of 50 seeds was covered with a plastic cup to
keep the microclimate moist. The boxes were transferred to a
growth chamber at 4 °C without light, to stratify the seeds
under similar conditions as during snow melt. After 16 d,
the temperature was raised 4–4.5 K/d for three days until the
temperature reached 18 °C, and light (approximately 40 µmol
m–2 s–1 at seed surface, 35 W fluorescent tube, 840 HE (Osram, Munich, Germany)) was set to 24 h. All seeds were examined once a week for germination (appearance of radicle
or cotelydons), and the trial was continued until no new seedlings appeared in two successive weekly counts, which oc-
curred after 10 weeks. No attempts were made to determine
whether nongerminating seeds were dormant or dead.
Germination in controlled suboptimal conditions
(experiments 2 and 3)
Experiments 2 and 3 (Table 2) were prepared using a soil
mixture consisting of two-thirds greenhouse soil for seedlings
(Hasselfors Garden, Såjord, Örebro, Sweden; 125 g m–3 N,
60 g m–3 P, 135 g m–3 K, 240 g m–3 Mg, 1800 g m–3 Ca,
and 70 g m–3 S; pH 5.6–6.4) and one-third perlite (grain size
1.5–6.0 mm). Ten replicates of 50 seeds of each of six species (B. vivipara, D. octopetala, Oxyria digyna (L.) Hill,
Salix polaris Wahlenb., S. oppositifolia, and Silene acaulis)
were sown in pots of 70 mm × 70 mm, except for B. vivipara, for which 12 replicates were made. All pots were watered every 2–3 d with tap water. The pots were divided and
two experiments were carried out.
Experiment 2. Five pots of each species (seven for B. vivipara) were placed in a growth chamber to germinate seeds in
controlled conditions with suboptimal (low) temperatures.
The temperature in the chamber was set at 8 °C (Table 2),
but hovered between 6 °C and 12 °C owing to the functioning of the air-cooler control loop. After 6 weeks, technical
problems with the air cooler occurred, and the seeds were
subjected to approximately 20 °C for a maximum of 24 h.
By this time, all species had already completed germination,
except Silene acaulis, which had germinated to 27.2% and increased thereafter to the final amount (Table 1). All pots
were immediately moved to two smaller growth chambers
that had a minimum operating temperature of 12 °C.
Experiment 3. The other batch of prepared pots was placed
in controlled outdoor conditions on the flat roof of the building of the University Centre in Svalbard on 4 June 2008.
Seeds were protected against bird predation by a net and
against rodents by placement. Temperatures were monitored
with Tinytag Plus TG 12-0020 (Gemini Data Loggers, Chichester, UK) until 9 August 2008 when the logger memory
was full.
Emerging seedlings in both experiments were counted
weekly for 5 weeks and subsequently every 3rd week; the experiment ran for 12 weeks. Seedlings remained in the pots to
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340
Table 1. Collection dates, sites, and germination percentages±SD of seeds collected in Svalbard and germinated at different temperatures on different substrates.
Alopecurus magellanicus
Lam.
Bistorta vivipara (L.) S.F.
Gray
Cassiope tetragona L.D.
Don. ssp. tetragona L.
Cerastium arcticum
Lange coll.
Dryas octopetala L.
Erigeron humilis R.C.
Graham
Eriophorum scheuchzeri
Hoppe ssp. arcticum
Novoselova
Honckenya peploides (L.)
Ehrh. ssp. diffusa
(Hornem.) Á.Löve
Luzula confusa Lindeb.
Luzula nivalis (Laest.)
Spreng.
Oxyria digyna (L.) Hill
Papaver dahlianum
Nordh.
Pedicularis dasyantha
(Trautv.) Hadac
Pedicularis hirsuta L.
Salix polaris Wahlenb.
Saxifraga cernua L.
Saxifraga cespitosa L.
ssp. cespitosa
Saxifraga hirculus L. ssp.
compacta Hedberg
Saxifraga oppositifolia L.
ssp. oppositifolia
Silene acaulis (L.) Jacq.
Silene involucrata (Cham.
& Schltdl.) Bocquet
ssp. furcata (Raf.) V.V.
Petrovsky & Elven
Silene uralensis (Rupr.)
Bocquet ssp arctica
(Th.Fr.) Bocquet
This study,
growth chamber: filter
paper, 18 °C
8.7±2.3
This study,
moraine:
gravel, 6.7 °C*
—
This study,
moraine:
moss, 6.5 °C*
—
Eurola
(1972): peat,
15 °C*
0.1
—
Bell and
Bliss (1980):
filter paper,
20 °C
—
Hagen
(2002): peat
and sand,
22 °C
—
Söyrinki (1939,
1939): paper,
not given
—
9.5
—
90
—
Bliss
(1958): filter
paper, 22 °C
—
Collection date
in 2007
5 September
Collection
sites
Adventdalen
22 August
14 September
14 and 17
September
5 September
20 September
14 September
4 and 14
September
23 August
Hotellneset
Mine 7
Endalen
26.7±3.6
2.3±0.9
2.7±0.9
76.0±3.5
—
—
0
52.0
—
—
—
Adventdalen
Hotellneset
Endalen
Endalen
16.0±3.0
—
—
5.7
—
36
—
—
55.3±4.1
53.3±4.1
0
0
3.0±1.0
0
—
—
—
—
10
—
40
—
Endalen
10.0±2.4
—
—
—
—
—
55
23 August
9 September
Hotellneset
Moskushamn
6.7±2.0
—
—
—
—
—
—
—
17 September
5 September
Endalen
Adventdalen
78.7±3.3
25.3±3.5
2.7±0.9
—
3.3±1.0
—
27.5
0.3
—
—
—
—
80
—
82
—
23 August
22 August
Hotellneset
Endalen
92.7±2.1
0
1.7±0.7
0 (12.5±2.1)
2.0±0.8
0 (15.0±2.1)
5.6
0.2
—
—
30
—
70
80
94
—
4 and 6
September
9 September
6 September
17 September
4 September
14 and 17
September
20 September
Endalen
1.3±0.9
0 (2.4±1.1)
0 (4.1±1.2)
0.6
—
—
—
—
Moskushamn
Endalen
Endalen
Endalen
Endalen
0
76.7±3.5
95.3±1.7
97.3±1.3
0 (6.2±1.7)
7.3±1.5
3.7±1.1
—
0 (19.3±2.4)
27.3±2.62.1
22.0±2.4
—
0.5
1.2
3.1
—
—
—
—
—
—
—
96
65
—
—
—
—
—
—
88
95
Hotellneset
3.3±1.5
—
—
0
—
—
—
—
20 September
Hotellneset
72.0±3.7
—
—
—
—
Hotellneset
94.0±1.9
2.3±0.9 (20.0
±2.3)
19.7±2.3
1.9
23 August and
20 September
23 August
2.0±0.8
(20.0±2.1)
18.6±2.4
—
89.7
—
—
99
Hotellneset
98.7±0.9
0.7±0.5
4.7±1.2
—
—
—
—
—
5 September
6 and 9
September
Adventdalen
Endalen
99.3±0.7
—
—
—
—
—
—
—
0
—
5.4
Note: Values in parentheses are germination percentages obtained after a recount 1 year later. For comparison, germination percentages obtained in other studies with seeds collected on Svalbard (Eurola
1972; Hagen 2002), Unimat in low-arctic Alaska (Bliss 1958), King Christian Island in the polar desert part of Canada (Bell and Bliss 1980), and from alpine Scandinavia (Söyrinki 1939) are given. Nomenclature follows the Pan Arctic Flora project (Elven 2007). Collection sites are shown in Fig. 1.
*Temperatures are means of ambient temperatures.
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Germination percentages
341
Wind
No
No
Yes
Yes
Yes
Predation
No
No
No
Yes
Yes
Moisture
limitation
No
No
No
0.16±0.01*
0.07±0.03*
minimize removal disturbance and to monitor survival. However, using this counting frequency, the percentage of germinating seeds may have been slightly underestimated in
experiment 3, as some seedlings may have germinated and
died unnoticed. Owing to strong weather shifts with subzero
temperatures at the end of June, seedlings of three species
died. For these species, percentages given in Table 1 and
Fig. 2 and data used to compare experiments 2 and 3 are
based on maximum numbers of observed germinated seeds.
The data from experiment 3, used to compare with those
from experiment 4, however, are based on seedlings that survived by the end of the experiment. Seedlings were counted
for the last time on 22 August 2008.
Note: Shaded areas are factors reducing germination from optimal conditions.
*Averages and SD of hourly measured soil moisture are given as cubic metres of water per cubic metre of soil.
Temperature
fluctuations
Minimum
Minimum
Medium
High
High
Temperature,
average ± SD (°C)
18.0±0.5
8.0±0.5–12.0±0.5
6.6±2.6
6.5±3.5
6.7±3.5
Place
Indoor
Indoor
Outdoor
Outdoor
Outdoor
Substrate
Filter paper
Soil mixture
Soil mixture
Moss
Gravel
Germination start
2008
4 April
1 June
4 June
27 June–2 July
27 June–2 July
Stratification
end 2008
18 March
29 May
29 May
29 May
29 May
Experiment
1. Filter optimal
2. Indoor low
3. Outdoor protected
4. Outdoor moss
5. Outdoor gravel
Table 2. Germination conditions used to test factors influencing germination success in six arctic species in a stepwise design from perceived optimal to field conditions.
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Müller et al.
Germination in moss and on gravel in the field
(experiments 4 and 5)
In total, 20 seed-addition plots in two different sites were
established. The sites (78°11′N, 15°35′E) were on the flat
part of an old moraine of Larsbreen glacier on the lower part
of a north-facing slope on Sarkofagen, a hill close to Longyearbyen (Fig. 1). One site, hereafter called outdoor moss
(experiment 4), was mainly covered by moss and scattered
Salix polaris, whereas the other site, hereafter called outdoor
gravel (experiment 5), was characterized by frost-disturbed
open gravel with small vegetated patches of Salix polaris
and L. confusa in between. In the latter site, plots were established only on frost-disturbed open gravel and in the former
only on moss. Single plots were chosen for their homogeneity and were, therefore, nonrandom. All seeds were subjected
to natural temperature and moisture conditions. In addition,
there was no protection against seed predation. The most frequently observed potential seed predator was snow bunting
(Plectrophenax nivalis L.), whereas barnacle goose (Branta
leucopsis Bechstein.) and Svalbard rock ptarmigan (Lagopus
muta hyperborea Sundevall) were less frequently observed.
The influence of invertebrate seed predators can be neglected
on Svalbard (Coulson 2007). In the moss plots, small gaps
approximately 0.5–1 cm deep and 0.5 cm wide were made,
and seeds were sown into these gaps to prevent them from
being blown away. On the outdoor gravel site, enough small
cracks in the soil provided shelter for the seeds, therefore, no
artificial gaps were made. For each plot, 30 seeds per species
were sown with the aid of a frame that was 50 cm × 50 cm
with 16 subplots of 10 cm × 10 cm, which provided regular
distance and orientation. Each of the 13 species (B. vivipara,
D. octopetala, E. humilis, L. confusa, O. digyna, Papaver
dahlianum Nordh., Pedicularis dasyantha (Trautv.) Hadac,
Pedicularis hirsuta L., Salix polaris, S. cernua, S. oppositifolia, Silene acaulis, and Silene involucrata ssp. furcata) was
randomly allocated to the subplots. Loggers (HOBO Micro
Station, Onset Computer Cooperation, Pocasset, Massachusetts) were installed at these sites on 2–4 July 2008. The loggers were equipped with sensors for photosynthetically active
radiation (PAR), soil temperature, and moisture. PAR was
measured 1 m aboveground to avoid shading of the sensor;
soil temperature and moisture were measured approximately
1 cm below the surface. Average PAR in summer at the field
site was 234 µmol m–2 s–1 in 2008 (5 July to 31 August).
Seed germination was counted only on 30 August 2008 and
may thus be underestimated as some seedlings probably died
before being counted. The seed addition plots were recounted
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342
Botany, Vol. 89, 2011
Fig. 2. The germination percentages of six common arctic species with 95% confidence intervals obtained in five different experiments. The
germination conditions were (i) filter optimal (filter paper and 18 °C, perceived optimal conditions), (ii) indoor low (soil mixture and 8–12 °C),
(iii) outdoor protected maximum germination (soil mixture and ambient temperatures, seeds protected against predation) (the second line
indicates survived seedlings), (iv) outdoor moss (moss covered moraine plots), and (v) outdoor gravel (bare gravely soil plots on a moraine), see Table 2.
Bistorta vivipara
100
80
Germination (%)
Germination (%)
80
60
40
20
60
40
20
0
0
Filter
optimal
In door Outdoor Outdoor Outdo or
lo w protected moss
gravel
Filter
optimal
Oxyria digyna
80
Germination
rmination (%)
80
Germination
ermination (%)
100
60
40
60
40
20
20
0
0
Filter
optimal
100
Indo or Outdoor Outdo or Outdo or
low protected mo ss
g ravel
Salix polaris
100
Filter
op timal
Ind oor Outdoo r Outdoor Outdoor
lo w
protected moss
gravel
Saxifraga oppositifolia
In door Outdo or Outdoo r Outdoor
low
p rotected moss
gravel
Silene acaulis
100
80
Germination (%)
80
Germination (%)
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Dryas octopetala
100
60
40
20
60
40
20
0
0
Filter Indo orlow Outdoor Outdoor Outdoor
optimal
protected moss
g ravel
on 8 June, 26 August, and 10 September 2009 to determine
if any further seeds had germinated.
Germination percentages of other studies
Germination percentages were compiled from published
studies of seeds collected in Svalbard (Eurola 1972; Hagen
Filter
optimal
In door Outdoor Outdoor Outdoor
lo w protected moss
gravel
2002); Unimat, northern Alaska (Bliss 1958); and King
Christian Island, Northwest Territories (Bell and Bliss 1980).
The germination percentages of B. vivipara (≡Polygonum viviparum L.) and Silene acaulis taken from Bliss (1958) are
from seeds collected in alpine tundra in Wyoming. The only
other comprehensive study from the Arctic that we are aware
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Müller et al.
343
of, Sørensen’s (1941) study from NE Greenland, was excluded because no germination percentages were given. To
compare our data with data from an alpine area, germination
percentages from seeds collected in northern Scandinavia
(Söyrinki 1939) were included (Table 1). To increase the
sample size for exploring the correlation between germination in the field and under optimal conditions, data from
Bell and Bliss (1980) were used.
Spearman rank-order correlation coefficient (rs) is given.
Nevertheless, adding data from Bell and Bliss (1980) to our
data improved model fit to a LM. Model fit was evaluated
using diagnostic plots in R. All statistical analyses were
made with the statistic package R 2.7.2 (R Development
Core Team 2008).
Temperature during seed development
To compare temperatures during seed development for our
study with those for the most comprehensive study from
Svalbard (Eurola 1972), we calculated temperature sums using positive daily averages from 1 May to the last day of
seed collection (22 August 1969, Eurola 1972; 20 September
2007, this study). Also, the daily air average temperatures for
each of the summer months of May–September were compared. The temperature data were obtained from the Norwegian Meteorological Institute (http://met.no).
In 2007, the first daily average air temperature above 0 °C
was 11 d earlier than in 1969. June was significantly warmer
in 2007 (approximately 4 K, Wilcoxon’s signed-rank test,
W = 74, p < 0.001) than in 1969. The daily temperature
sum from 1 May until seed collection was 629.4 K in
2007 and 371.4 K in 1969 (i.e., 187.6 K higher), as well
as 16 more days that had positive daily average temperatures in 2007 than in 1969. Thus, the seeds that germinated
in our study had 1.7 the amount of heat during their development than those reported by Eurola (1972).
Germination in perceived optimal conditions
Twenty out of the 22 species (91%) germinated in perceived optimal conditions, and 10 of the tested species had
greater than 70% germination (Table 1). Two species, Papaver dahlianum and Pedicularis hirsuta, did not germinate,
whereas Alopecurus magellanicus Lam., Pedicularis dasyantha, Saxifraga hirculus L., and Honkenya peploides (L.)
Ehrh. had less than 9% germination.
Thirteen out of 15 species that were tested in both studies
had higher germination in our study than in Eurola’s (1972);
for half of the species the germination percentages were
25%–92% (Table 1). Two species (C. tetragona and S. hirculus) that did not germinate in Eurola’s study germinated in
our study, whereas the opposite was observed for two other
species (Papaver dahlianum and Pedicularis hirsuta). All
three species that were present in both our study and the one
by Bliss (1958) germinated at higher percentages in our
study. When compared with Bell and Bliss (1980), one species germinated equally well, two germinated at a higher percentage, and one germinated at lower percentages in our
study. In our study, B. vivipara and Papaver dahlianum had
lower germination than in the study by Hagen (2002) (Table 1), whereas D. octopetala and O. digyna germinated better, and L. confusa had similar germination (80%). All
species present in our study and the Scandinavian alpine
study by Söyrinki (1939) had very similar germination percentages, except Eriophorum scheuchzeri, which germinated
at a lower percentage in our study (Table 1).
Temperature during germination
Owing to exceptionally late snowmelt in 2008, the experiments on the moraine (experiments 4 and 5) were established
about 4 weeks later than the one under controlled outdoor
temperature (experiment 3). For experiments 4 and 5, averages of soil temperatures were calculated from logger measurements using the period from sowing until final counting
of the seedlings (Table 2). The average soil temperature of
the controlled outdoor experiment was calculated from the
day the experiment was set up until the logger memory was
full, 13 d before the final count.
Statistical analysis
To examine if different treatments affected the proportions
of germinating seeds, the generalized linear models (GLMs)
were specified with binomial error distribution as recommended for binomial data (Crawley 2007). Germination percentages of each experiment were analyzed at the species
level. If the residual deviance was larger than the degrees of
freedom, overdispersion in the GLM was assumed, and models were specified as quasibinomial instead of binomial. Confidence intervals (CI, 95%) were calculated with the R
package binGroup 1.0-7 (Zhang et al. 2010) after the Wilson
score method (Newcombe 1998). The standard deviations for
the germination data were calculated with a formula for binomial data (Collett 2003).
To test if germination in perceived optimal conditions (experiment 1) was correlated to germination in the field (experiments 4 and 5, separately), a Spearman Rank Order
correlation test was used because the data from our study fit
a linear model (LM) poorly. For the tested correlations, the
Results
Germination in field conditions
Of the 13 species tested in realistic field conditions, 8 germinated better on moss than on gravel, whereas Silene acaulis germinated at a similar percentage on both substrates and
had the highest germination of all species on the gravel plots
(19%, Table 1). With three exceptions (Salix polaris, S. cernua, and Silene acaulis), germination was less than 10%, and
four species (E. humilis, Papaver dahlianum, Pedicularis dasyantha, and Pedicularis hirsuta) did not germinate. Dryas
octopetala did not germinate on gravel, but some seedlings
were found in the plots with moss (3% germination). However, Papaver dahlianum and Pedicularis hirsuta germinated
at high percentages in 2009 from the seeds sown in 2008
(Table 1). Similarly, the percentage of S. oppositifolia seedlings increased from approximately 2% in 2008 to 20% in
2009. None of the other species in this experiment showed
any second year germination.
Stepwise realistic conditions
The temperature reduction and the change of substrate from
perceived optimal conditions (experiment 1, Table 2) to the indoor low temperature conditions (8–12 °C, experiment 2) reduced germination of D. octopetala, O. digyna, Silene acaulis,
Published by NRC Research Press
344
Botany, Vol. 89, 2011
Table 3. Results of the generalized linear models analyzing the germination of six species germinated in five different experiments, which
were compared stepwise.
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Experiments
compared
Filter optimal and
indoor low, experiments 1 and 2
Indoor low and outdoor protected, experiments 2 and 3
Outdoor protected
and outdoor moss,
experiments 3 and 4
Outdoor moss and
outdoor gravel, experiments 4 and 5
Environmental
factor added
Colder temperature
and different
substrate
Colder temperatures and wind
Different substrate,
moisture, and
predation
Different substrate
and decrease in
moisture
n
replicates
10
t or z
value
–7.90*
p
<0.001
15.70
6.81
11.24
16.25
6.32
3.43*
5.59
0.75
<0.001
<0.001
0.001
0.480
6
10
10.16
6.24
5.29
–4.50*
0.002
<0.001
10
10
10
10
8
8
8
8
—
7.30
19.35
17.69
—
–5.36*
–3.64
–5.01
—
<0.001
0.007
0.001
500
550
10
15
8
13
13.78
17.62
–5.04
7.51
0.001
<0.001
550
550
550
550
15
15
15
15
13
13
13
13
—
17.22
53.08
15.02
—
–8.37
–4.00
6.71
—
<0.001
0.033
<0.001
550
600
15
20
13
18
32.30
29.85
–0.09
0.20
0.93
0.847
600
600
600
20
20
20
18
18
18
—
21.75
88.02
—
0.29
2.86
—
0.777
0.010
600
600
20
20
18
18
25.12
67.39
0.39
0.16
0.702
0.869
Species
Bistorta vivipara
n total
500
Dryas octopetala
Oxyria digyna
Salix polaris
Saxifraga
oppositifolia
Silene acaulis
Bistorta vivipara
400
400
400
400
8
8
8
8
6
6
6
6
400
600
8
12
Dryas octopetala
Oxyria digyna
Salix polaris
Saxifraga
oppositifolia
Silene acaulis
Bistorta vivipara
500
500
500
500
Dryas octopetala
Oxyria digyna
Salix polaris
Saxifraga
oppositifolia
Silene acaulis
Bistorta vivipara
Dryas octopetala
Oxyria digyna
Salix polaris
Saxifraga
oppositifolia
Silene acaulis
df
8
Residual
deviance
5.06
Note: Assumed main limited environmental factors influencing germination at each step are shown.
*Binomial and z values are given, otherwise quasibinomial distribution and t values are given.
S. oppositifolia, and Salix polaris seeds. The smallest reduction (6%, not significant) was found in S. oppositifolia and
the largest was found in D. octopetala (51.7%, Table 3;
Fig. 2). The only species that grew better in the colder treatment was B. vivipara.
When germinating the seeds in protected outdoor conditions (experiment 3), the colder temperature and harsher environment reduced germination compared with the indoor
experiment at a low temperature (experiment 2) by 18.5%
(B. vivipara) to 34% (S. oppositifolia, experiment 3, Fig. 2
and Table 3). Germination was prevented in D. octopetala.
Bistorta vivipara bulbils, however, still grew better than on
filter paper at 18 °C (experiment 1, Fig. 2). During experiment 3, a high percentage of seedlings of three species died
(O. digyna, 55%; Salix polaris, 97%; and Silene acaulis,
41%, not shown in Table 1 or Fig. 2), whereas no seedling
mortality was observed for B. vivipara and S. oppositifolia.
Comparing only the seedlings that survived (O. digyna,
25.2%; Salix polaris, 0.4%; Silene acaulis, 19.2%; B. vivipara
and S. oppositifolia, see Table 1) in the protected outdoor experiment (experiment 3) with those counted in the outdoor
experiment on moss substrate on the moraine (experiment 4,
Table 1), the responses to the different conditions were species specific. The numbers of seedlings of B. vivipara, O. digyna, and S. oppositifolia on the moss plot were 22%–29%
lower compared with those in protected outdoor conditions.
Germination of Salix polaris was 20% higher on moss plots
than in the protected outdoor experiment (Table 3), and additionally, some D. octopetala seedlings germinated on the
moss plots (Table 1).
In the last experimental step (outdoor moss to outdoor
gravel), reduction of germination was small (below 0.1%)
and not significant for any species, except Salix polaris,
which germinated to 20% less in gravel than in moss plots
(Table 3, Fig. 2).
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Müller et al.
345
30
25
20
15
10
5
Germination Outdoor moss/ moist meadow (%)
data our study
data from Bell and Bliss (1980)
0
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Fig. 3. Germination percentages of nine species from our study that
germinated outdoor on a moss-covered moraine plotted against germination of the same species under perceived optimal conditions indoors at 18 °C on moist filter paper. Additional data from Bell and
Bliss (1980) is for seven species that germinated on a moist meadow
and are plotted against the same species germinated indoors on filter
paper. Adjusted R2 = 0.19, p = 0.049, df = 14.
0
20
40
60
80
100
Germination on filterpaper (%)
When comparing germination under stepwise more realistic conditions with perceived optimal conditions (B. vivipara
excluded), germination was reduced by 36%–64% under protected outdoor conditions (experiment 3), 49%–91% in the
outdoor moss plot, and 55%–91% lower in the gravel plots.
The largest decrease was seen in O. digyna with 91% fewer
seeds germinating from the best to harshest conditions. Only
B. vivipara germinated better under indoor low temperature
and outdoor protected conditions than at perceived optimal
conditions (Fig. 3).
Correlation between germination in field and optimal
conditions
For the species present in perceived optimal conditions
(experiment 1) and in both field experiments (experiments 4
and 5), germination success in perceived optimal conditions
was not correlated to seedling emergence in the field plots.
Both rs values were rather small and p values were large
(germination in optimal conditions and moss plot: rs = 0.43,
p = 0.25; in optimal conditions and gravel plots: rs = 0.18,
p = 0.64). The inclusion of data from the experiments by
Bell and Bliss (1980) resulted in a weak positive correlation
(Fig. 3).
Discussion
The generally high germination percentages obtained under
perceived optimal conditions in our study indicate that viability of seeds from the middle arctic tundra zone (bioclimatic
zone C) in Svalbard is higher than that reported in the only
larger previous study (Eurola 1972). Our data suggest similar
germinability in optimal conditions to that of Scandinavian
alpine areas (Söyrinki 1939). However, with stepwise more
realistic conditions, the proportions of germinating seeds
were strongly reduced. In addition to a suboptimal (lower)
germination temperature, other factors, such as wind, moisture limitations, predation, and soil properties, limited seed
germination in natural conditions. Furthermore, germination
in natural conditions was only weakly related to germination
under perceived optimal conditions, suggesting that the effects of factors limiting germinability under extreme arctic
field conditions are species specific.
Germination has been underestimated in former studies
The generally higher germination percentages found in our
study compared with those obtained by Eurola (1972) may
be due to the conditions during seed development or seed
germination. Eurola (1972) germinated the seeds on soil at
ambient temperatures with a mean temperature 3 °C lower
than the one we used, and that may have influenced germination. However, most of our germination percentages were
also higher than Eurola’s (1972) percentages of viable seeds,
which he determined with a tetrazolium test. Thus, conditions
during seed development might have been more favorable in
our study than in Eurola’s (1972). Daily average temperatures
above 0 °C were 11 d earlier in our study compared with
those of Eurola (1972), which may have favored spring phenology. Arctic species respond to earlier advancement of
spring (including earlier snowmelt) with rapid phenological
advancements (Høye et al. 2007), which is an important factor for developing seeds (Chambers 1989; Cooper et al.
2011). In addition, the later date of seed collection and
higher summer temperatures exposed developing seeds to a
greater temperature sum in 2007 (629.4 K) than in 1969
(371.4 K), which is important for seed viability and level of
maturity (Wookey et al. 1995). Thus, we assume that the
higher temperature sum during the ripening process of the
collected seeds is the most important factor explaining the
higher germination in our study compared with that of Eurola
(1972). This also emphasizes the importance of collecting
seeds when they are completely ripe.
Our study also showed higher germination percentages
than several other studies in the Arctic. The seeds germinated
by Bell and Bliss (1980) most likely experienced lower temperatures during development because they were collected in
a polar desert. The comparatively small differences in C. tetragona by Bliss (1958) and D. octopetala by Hagen (2002)
to our study were most likely caused by annual variability in
germination percentages within species, which seems especially pronounced in thermophilic species (Welker et al.
1997; Wada 1999). High annual variability in germination
within any tundra or alpine species has been largely attributed to date of snowmelt, timing of precipitation, ambient
temperatures, and soil temperatures (Chambers 1989; Cooper
et al. 2011). Thus, again we assume that a temperature difference during the development and ripening process of the
seeds was the most important factor for the higher germination percentages observed in our study.
Inappropriate stratification methods may account for the
lack of germination in Papaver dahlianum, Pedicularis dasyantha, and Pedicularis hirsuta in our study. Papaver has
morphophysiological dormancy, whereas Pedicularis has
physiological dormancy (Baskin and Baskin 1998). All three
species were observed germinating on both field plots (experiments 4 and 5) 1 year after sowing (Table 1), indicating
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that dormancy in these species can be broken with two cold
stratification periods and one warm stratification period.
Stepwise reduction from perceived optimalization
The reduction in germination percentages observed in five
out of six species in the first three experimental steps was
mainly an effect of decreasing temperatures, because moisture was kept optimal and there was no seed predation. The
impact of temperature reduction on germination, however,
differed among species. Thus, as with species from alpine
and temperate zones (Trudgill et al. 2000), arctic species
seem to have dissimilar temperature sensitivity.
The lower numbers of seedlings of B. vivpara, O. digyna,
and S. oppositifolia in both moss and gravel plots compared
with controlled outdoor conditions suggest that the factors
present in both field plots limited germination. As the temperature conditions were rather similar in all three plots, factors other than temperature were probably more important.
Seed predation, as well as the redistribution of seeds due to
abiotic processes, such as wind and rain, may reduce the
number of seeds available for germination (Vander Wall et
al. 2005). The germination of B. vivipara may have been reduced by predation, as nutrient-rich bulbils are popular food
items for snow buntings (P. nivalis) (Green and Summers
1975; Dolman 1995). The small seeds of S. oppositifolia
may have fallen into small cracks, landed in places that did
not meet germination conditions, or been overlaid owing to
soil movements or rain and thus entered the seed bank rather
than germinating. The higher germination percentages recorded 1 year later in this species suggest that a substantial
proportion of the seeds entered the seed bank only temporarily. It can be assumed that some of the large winged seeds of
O. digyna were moved from the plots by strong winds. Salix
polaris was the only species that had significant differences
in germination in moss (experiment 4) compared with gravel
plots (experiment 5). In addition, seedling numbers in the
moss plot were much higher than in the protected outdoor
experiment (experiment 3), suggesting that for this species,
moisture conditions may have been critical. Mossy substrates
slow down the surface drying process (Bell and Bliss 1980),
and for drought sensitive species, such as Salix (Densmore
and Zasada 1983), the substrate in natural conditions, therefore, matters. Thus, reduced germination in the outdoor plots
seems to be caused by different factors for different species.
Correlation between field and optimal germination
The low correlation between germination in the field and
under perceived optimal conditions is counter intuitive, as
one would expect that the species with the highest percentage
of viable seeds would also germinate best in the field. However, as our stepwise design demonstrates, temperature sensitivity is species specific, and for some species additional
factors, such as predation or lack of moisture, limit germination. Thus, there may not be any linear correlation between
seed viability and germination under current natural conditions. As temperature probably was the most limiting factor
for germination of four of the six species studied in detail
here (Fig. 2), the expected increasing temperatures (Christensen et al. 2007) may result in a stronger correlation between
seed viability and natural seedling occurrence. Nevertheless,
elevated temperatures in a given habitat may not benefit all
Botany, Vol. 89, 2011
species. As shown for S. oppositifolia by minor differences
in germination between experiments 1 and 2 (Fig. 2), some
species may even react contrarily in warmer conditions, e.g.,
B. vivipara (experiment 1, Fig. 2) and Ranunculus glacialis
L. (Totland and Alatalo 2002). Also, in a warmer climate,
competition may limit recruitment in some species (Totland
1999). Thus, caution should be taken when evaluating speciesrecruitment potential based on laboratory studies.
Conclusion
The higher proportion of species germinating and the
higher germination percentages observed in our study compared with those of earlier studies suggest that climate
change already has increased seed viability of arctic plants.
Thus, most of the arctic species have the ability to reshuffle
their genes and adapt to changing habitats. However, germination in the field is still strongly limited by both temperature
and other factors. Thus, sexual reproduction is lower in the
Arctic than in other areas. With an even warmer climate, this
may change, but the changes are expected to be species specific, because different factors limit recruitment in different
species.
Acknowledgements
We thank Karin Daniels Amby for help with seed collection, Marie-Hélène Jacques and Christopher Ware for help
during the germination tests, and Nigel Yoccoz for advice on
statistics. The project was funded by the University Centre of
Svalbard.
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