Towards An Understanding of Factors Controlling Seed Bank Composition and Longevity in The Alpine Environment

Bot. Rev.
(2015) 81:70–103
DOI 10.1007/s12229-014-9150-2
Towards an Understanding of Factors Controlling Seed

Bank Composition and Longevity
in the Alpine Environment
Ganesh K. Jaganathan1,3 & Sarah E. Dalrymple2 &

Baolin Liu1
1
Institute of Biothermal Technology, University of Shanghai for Science and Technology, Shanghai 20009,
China
2
James Parsons Building, School of Natural Sciences and Psychology, Liverpool John Moores University,
Byrom Street, Liverpool L3 3AF, UK
3
Author for Correspondence; e-mail: [email protected]
Published online: 17 January 2015
# The New York Botanical Garden 2015
Abstract The ability of seeds to regenerate from soil seed banks has long been
recognized as a key survival strategy for plants establishing new niches in highly
variable climates of alpine environments. However, the fundamental aspects of
evolutionary/selective forces for seed bank development in alpine ecosystems are
largely unknown. Here, we developed a model that describes dormancy, a high
temperature requirement and a specific light/darkness regime at the time of seed
shedding can preclude autumn germination, thus contributing to seed persistence until
the next growing season. The benefits of these factors synchronising germination with
the growing season are reviewed. Additionally, the importance of climatic variations of
maternal environment affecting some of these factors is also discussed. It is suggested
that the environmental conditions during the growing season partly control the seed
persistence and seeds that fail to germinate are carried over to the next season. Species
that have small (<3 mg) and round-shaped seeds tend to persist more easily in soil for
over 5 years, than do the large or flat seeds. However, some large-seeded species also
have the potential to establish short-term persistence bank. A literature survey reveals
88 % of the alpine seeds have a mass <3 mg. Seed size has only a weak relationship
with mean germination timing (MGT) indicating that reduced persistence in large-
seeded species cannot be counteracted by quicker germination, but combined effects of
other factors stimulating germination remain an open area to be studied. It is proposed
that long distance dispersal (LDD) is limited in most-but not all-species, primarily due
to the absence of specialized dispersal structures. However, among numerous dispersal
modes, most species tend to be dispersed by wind. Thus, spermatophytes of alpine
environments have a greater tendency to establish seed banks and spread the risk of
germination to many years, rather than being dispersed to other micro-climates.
Keywords Alpine tundra . Climate change . Dormancy. Germination . Phylogeny. Seed

size . Seedling establishment . Light requirement . Seed dispersal
Seed Bank Composition and Longevity in the Alpine Environment 71
Introduction
The ecological significance of seeds in establishing plant communities has been

extensively documented for an appreciable number of alpine species (Bliss, 1958;
Baskin & Baskin, 1998; Molau & Larsson, 2000; Welling & Laine, 2000; Welling
et al., 2004; Bu et al., 2009; Ma et al., 2011). Unlike other ecosystems, alpine seed
germination is principally determined by the short and erratic growing season (Bell &
Bliss, 1980). Consequently, seeds do not often have a favorable germination environ-
ment and would be expected to enter the soil seed bank to postpone the germination to
a later year when more favorable conditions occur (reviewed by Arroyo et al., 1999;
Cavieres & Arroyo, 2001; Welling et al., 2004). However, there is some evidence to
show that the unfavorable conditions preventing seed germination may sometimes
persist for two consecutive years (Körner, 2003). Therefore, it is not surprising to
discover that evolutionary and ecological processes have resulted in most, if not all,
species adapted to alpine regions having seeds with a longevity of at least 2 years.
The ability of alpine seeds to form long-term seed banks is considered as an
important ecological trait for population dynamics and species establishment
(McGraw & Vavrek, 1989; Körner, 2003). One of the important means by which seeds
persist in the soil is by preventing germination immediately after dehiscence. Early
efforts to understand alpine soil seed bank dynamics have mostly focused on the seed
germination timing per se (see Baskin & Baskin, 1998), thus the mechanisms control-
ling germination have not been treated adequately. Even less attention has been paid to
recognize the factors influencing seed persistence in alpine environments. This dearth
of knowledge has become an acute problem, especially given that the effects of global
warming conspicuously affect the alpine ecosystem as a whole rather than impacting
upon specific species (Walther et al., 2002; Gottfried et al., 2012). Such predictions
explicitly require a profound understanding of seed adaptation and it is imperative
to model the imminent alpine flora community changes that may result from
climate shifts.
The important goal of this review is to explore some of the mechanisms evolved in
alpine species that determine how seeds enter and leave the soil. Our model depicts
dormancy, a requirement for relatively high temperatures and specific light/darkness
regimes are the key factors affecting seed persistence in alpine environment. Moreover,
when considering seed persistence in an ecological context, it is imperative to place
special emphasis on the comparative biology of alpine plants including the phenology
of seed size, germination traits and dispersal affecting the seed turnover and contrib-
uting to persistence. We do not mean to imply that only these factors are the pertinent
adaptive traits for seed persistence in alpine species; however, our view is that many
unknowns impede our understanding and this oversight can be only resolved by paying
more attention to these areas. We aim to identify these critical gaps and suggest possible
future research directions, rather than summarizing the overwhelming information
available on soil seed banks per se, a topic covered in myriad literature (e.g.,
McGraw & Vavrek, 1989; Körner, 2003; Baskin & Baskin, 1998). To this end, the
focus of discussion is limited only to seed bank establishment and persistence. Thus,
we do not address topics such as seed density in relation to seed numbers, and species
competition during emergence etc. Nevertheless, understanding these subjects is vital,
yet out knowledge is rudimentary, but somewhat detailed information can be found
72 G.K. Jaganathan et al.
elsewhere (see Chambers et al., 1991; Chambers & MacMahon, 1994; Forbis, 2003;
Körner, 2003; Bu et al., 2007a, 2008, 2009).
Definitions and Terms
At the outset, it is necessary to explain our terms. Here we consider a seed to be the
product of sexual reproduction dispersed at natural dispersal time with all its dispersal
structures, e.g., wings, plumes etc. We do not use specific terms such as achenes, and
refer to all these propagules as seeds. We also adopt the seed bank classification scheme
of Bakker et al. (1996) and Thompson et al. (1997) on a broader level. Hence, seeds
that persist in soil for less than 1 year are termed as ‘transient’. Whereas, seeds that
persist for more than 1 year but less than 5 years are characteristically considered as
‘short-term persistent’ and any species that continue to persist in soil for more than
5 years are ‘long-term persistent’. Although, in most of the discussion, the term
‘transient’ and ‘persistent’ are loosely used to differentiate the seed longevity of less
than or more than 1 year respectively, whenever possible, clear distinctions of seed
bank types are made. We define dormancy as a state in which seed germination does
not take place even when the favorable environmental factors (temperature, moisture,
light/dark etc.) that stimulated germination in a non-dormant or dormancy broken seed
are provided. Five types of dormancy have been recognized in seeds (Baskin & Baskin,
1998, 2004) namely physiological (PD), morphological (MD), morpho-physiological
(MPD), physical (PY) and combinational (PD + PY), we attempt to specify dormancy
types when information is available. For the purpose of this review, we define
‘long-distance dispersal’ (LDD) as seed movement which is over 100 m (sensu
Cain et al., 2000).
Dormancy
Dormancy is one of the remarkable traits evolved in seeds that synchronize germination
with the most favorable season for seedling survival (Vleeshouwers et al., 1995; Baskin
& Baskin, 1998; Thompson, 2000; Bewley et al., 2013). Since Amen (1966) reviewed
the extent and role of seed dormancy in alpine species, there has been an abrupt
increase in the number of studies documenting alpine dormancy from species to
community level (Baskin & Baskin, 1998; Liu et al., 2011). This increase in literature
has refuted two of the early notions that (i) dormancy is a rare phenomenon in alpine
systems (see Amen, 1966) and (ii) dormancy is highly associated with seed-coat
inhibition (Billings & Mooney, 1968). The literature available on alpine seed dormancy
is in fact growing and this topic has been comprehensively reviewed periodically
(Billings & Mooney, 1968; Kaye, 1997; Baskin & Baskin, 1998). It is beyond the
scope here to present such an exhaustive review yet again. Instead, we discuss the role
of dormancy (and breaking requirements) in seed persistence.
Cavieres (1999) and Cavieres and Arroyo (2001) postulated that dormant seeds have
some advantage in establishing persistent seed banks in temporally and spatially
unpredictable alpine environments. This is partly because seeds shed in the autumn
are mostly dormant and require a period of cold-stratification satisfied under snow
before they germinate in spring (see below) and partly due to the ability of the seeds to
re-enter dormancy (in the case of PD) if they did not germinate. This view is in fact
supported by (i) Rees’ (1996) assertions that in order to maximize the progeny number,
species adapted to an environment that varies from 1 year to another select dormancy as
an adaptive trait (also see Rees & Long, 1992) and (ii) as Bewley et al. (2013) recently
generalized, the number of species with dormant seeds is likely to increase with
poleward movement because the unpredictability in climate increases.
Apart from these simple theoretical considerations, direct evidence delineating
whether or not dormancy contributes to seed persistence in alpine regions is scarce.
This is ascribable to the paucity of information amassed on a specific species for which
both the dormancy and longevity are known. Some progress has been made recently by
Schwienbacher et al. (2011) to bridge this gap (but see conclusion section). In an
attempt to investigate the seed dormancy types in 28 alpine species of central European
Alps, Austria, those authors concluded 26 species were dormant and only 2 species
were non-dormant. Out of 26 dormant species, PD (with all sub-classes namely non-
deep, intermediate and deep) was present in 20 species. MD and PY were recognized in
4 and 2 species respectively. In addition to assigning the type of dormancy, their study
included 9 species for which the seed longevity had previously been assessed by
artificial burial method (Schwienbacher et al., 2010). The findings of their study clearly
indicate that all seeds survived for at least 2 years in an artificial burial experiment (see
‘Seed size and persistence’, below) and had some type of dormancy - mostly PD or PY
(Table 1).
The assertion that dormant seeds persist in soil is in marked contrast with Thompson
et al. (2003) who concluded that “dormancy is neither a necessary nor a sufficient
condition for the accumulation of a persistent seed bank, and there is no realistic
prospect of predicting persistence from dormancy” based on their data from north-west
Europe (Thompson et al., 1997). They further supported this conclusion by showing
that most of the temperate shrubs have deep dormancy, but these species rarely persist
in soil. However, we presume that two different issues have been raised and these can
be encapsulated in the questions (1) do seeds of species establishing persistent seed
banks have dormancy and (2) do all dormant seeds enter persistent seed banks? Thus,
Table 1 List of species for which soil persistence and dormancy type have been estimated [Adapted from
(Schwienbacher et al., 2010, 2011)]. Nomenclature used in the original works was as such retained. For the
abbreviations of dormancy types see text. Seed size was calculated using digitizer option in origin 8.6
Species Family Seed mass (mg) Seed bank type Dormancy type
Achillea moschata Asteraceae 0.21 Short-term Persistence PD

Artemisia genipi Asteraceae 0.25 Short-term Persistence PD
Anthyllis alpicola* Fabaceae 2.41 Long-term Persistence PY
Geum reptans Rosaceae 0.54 Transient PD
Linaria alpina Veronicaceae 0.14 Long-term Persistence PD
Oxyria digyna Polygonaceae 0.55 Transient PD
Saxifraga aizoides* Saxifragaceae 0.04 Long-term Persistence PD
Saxifraga oppositifolia* Saxifragaceae 0.08 Short-term Persistence PD
Trifolium pallescens* Fabaceae 0.60 Long-term Persistence PY
*Classified as transient by Cerabolini et al. (2003)

not all dormant seeds persist in alpine soil, but being non-dormant could reduce the
ability of seeds to enter persistent seed bank in alpine environments. For example,
despite Geum reptans and Oxyria digyna being dormant (Table 1), they were both
short-term persistent corroborating the claim that some dormant seeds are also short-
lived in soil.
Indeed, it was initially thought that factors such as light requirements, germi-
nation inhibitors etc. cause dormancy in alpine seeds (Amen, 1965). Consequently,
Billings and Mooney (1968) concluded ‘seed dormancy in most alpine species is
under environmental control’. In the central European Alps, however,
Schwienbacher et al. (2011) explicitly classified the dormancy type in accordance
with Baskin and Baskin (2004), therefore these species do not represent ‘enforced
dormancy’. One plausible reason for the disagreement observed between North
West Europe and central European Alps datasets may lie in the geographical
distribution of the species. In the alpine environment, many species (ca. >70 %
as estimated by Baskin & Baskin, 1998 cited in Schwienbacher et al., 2011)
produce dormant seeds. Further evidence to safely conclude that most alpine seeds
are likely to produce dormant seeds comes from the data set assembled by Jurado
and Flores (2005) which suggests plants growing in environments with frost and/
or drought contain some form of seed dormancy (PD, MPD and PY) than species
in more benign environment.
It is generally agreed that seeds dispersed in autumn are held in seed banks until
spring because of dormancy breaking requirements (Fig. 1, Table 2). These dormant
seeds overwinter under snow cover and alleviate dormancy mostly by cold-wet strat-
ification. They then germinate at the first opportunity immediately after the snow melt
in spring to maximize growing periods in favorable conditions (Baskin & Baskin,
1998). Germination of non-dormant seeds in autumn, on the other hand, is exclusively
controlled by the local microclimate of a particular year. Interannual variation in
autumn temperature should therefore impose selective pressures on alpine communities
conferring advantages on species with dormant seeds (Rees & Long, 1992; Allen &
Meyer, 1998).
The influence of environmental conditions acting as selective force in the evolution
of seed dormancy is gaining recognition. Studies focusing on alpine species, e.g.,
Chenopodium bonus-henricus (Dorne, 1981), Artemisia tridentata ssp. vaseyana
(Meyer & Monsen, 1991), genus Penstemon (Meyer & Kitchen, 1994b; Meyer et al.,
1995), Linum perenne (Meyer & Kitchen, 1994a) Phacelia secunda (Cavieres &
Arroyo, 2001), and Koenigia islandica (Wagner & Simons, 2008), revealed seeds
collected from lower altitudes are non-dormant or conditionally dormant, seeds from
mid-altitudes are dormant and require cold-stratification for dormancy alleviation, and
seeds from high-altitudes are dormant and require longer cold-wet stratification dura-
tion compared to seeds collected from mid-altitudes. Insights gained from these studies
suggest dormancy and longer stratification duration must have co-evolved in seeds
adapted to higher altitudes. The differential effects of environmental conditions on
dormancy may also explain why Oxyria digyna has been classified both as dormant
(Stöcklin & Bäumler, 1996; Schwienbacher et al., 2011) and non-dormant (Mooney &
Billings, 1961; Mondoni et al., 2012). This species is common to both arctic and alpine
communities and therefore is subject to a range of conditions which may or may not
induce dormancy.
Fig. 1 Fate of a seed after dispersal from the mother plant. The horizontal dotted line distinguishes the
transient and persistent bank. If the seeds buried in soil (or close to the surface) germinate or die within 5 years,
they are transient seed banks. The remainder develop persistent seed banks. Seeds can die or be dispersed to
other locations at any stage of this model (see also Chambers & MacMahon, 1994). Similarly, the soil surface
may have increased seed rain, due to dispersed seeds from other locations reaching the local micro-site. For the
purpose of this model, ‘soil surface’ means the buried depth at which seeds can receive dormancy breaking
cues and/or light, germinate and establish seedlings. Seeds buried in the soil undergo seasonal cycling in
dormancy status and the depth of the dormancy changes with season
The opposite situation was observed in some of the recent studies which showed
seeds of many alpine plants lack dormancy when they develop and therefore germinate
immediately in autumn. Seed germination experiments performed in 37 endemic rare or
endangered taxa of Sierra Nevada high mountain (SE Spain), for instance, showed most
of the species tested were non-dormant and do not require any pretreatment for
germination (Lorite et al., 2007). Giménez-Benavides et al. (2005) reached a similar
conclusion when working with 20 species collected from high altitudes of Spain. It is
possible that these areas experience Mediterranean climate and seeds develop in a
slightly warmer temperature than in true alpine locations, to be less dormant (see also
conclusion). One recent study by Sommerville et al. (2013) shows species with non-
endospermic seeds did not require any stratification to germinate, however,
endospermic seeds needed 8 weeks of cold stratification for germination. Although
they concluded that ‘alpine species with endospermic seed and a restricted distribution
are most likely to contract in range under climate change and would be appropriate to
prioritize for ex-situ conservation’, non-endospermic seeds are also at risk in warming
climates as the absence of dormancy/breaking requirement impose the risk of autumn
germination and seedling mortality in winter, particularly on exposed sites (see
Mondoni et al., 2012).
Dormancy has generally not been specifically addressed in studies of seed persistence in
the soil. Nevertheless, the available evidence makes it tempting to conclude that dormancy
plays a crucial role in persistence at least for alpine vegetation. However, it is too early to
Table 2 Species that exhibit dormancy at the time of dispersal in autumn and the conditions shown to
alleviate initiate dormancy and progress seeds towards germination
Species Key results References
Carex pendula L. and C.remota L. Seeds stratification at low temperature Brändel and Schütz (2005)
alleviates dormancy effectively than
higher temperature. Seeds of
C. pendula and C. remota did not
germinate below 9 and 15 °C
respectively. Germination
requirements and dormancy patterns
ceased germination until late spring
and summer.
Fritillaria tubiformis subsp Seeds are dormant (MD) when dis- Carasso et al. (2012)
moggridgei persed in autumn, but low tempera-
ture (4 °C) experienced in winter
breaks dormancy and seeds readily
germinate in spring.
Aquilegia nivalis, Lagotis Seeds of these three perennial species Dar et al. (2009)
cashmeriana and Meconopsis require longer period of pre-chilling
latifolia during winter to break dormancy
and germinate in following spring.
Pre-chilling coupled with GA3 ap-
plication stimulated germination in
all three species, thus supporting
overwintering is mandatory for seed
germination and germination is pre-
cluded in the autumn.
Centaurium somedanum Non-deep MPD in seeds controls the Fernandez-Pascual et al.
germination timing in alpine climate. (2012)
Seeds come out of dormancy early
in spring readily germinate at 15–
22 °C, allowing the successful
seedling establishment in late spring
and summer.
Sempervivum vicentei subsp. paui, Germination in freshly collected seeds Giménez-Benavides et al.
Ranunculus ollissiponensis subsp. was generally poor. Cold (2005)
alpinus, Veronica fruticans subsp. stratification (4 °C) for 3 months in
cantabrica and Luzula hispanica. complete darkness improved
germination, suggesting the
dormancy breaking requirement in
seeds.
Empetrum nigrum Seeds are dormant at the time of Graae et al. (2008) and
dispersal from plant and require Baskin et al. (2002)
warm stratification followed by cold
stratification for germination. The
seeds can also induce a secondary
dormancy if the climate during the
growing season is unfavorable.
Stachys germanica L. subsp. bithynica Freshly collected seeds did not Güleryüz et al. (2011)
germinate. Dormancy breaking
requirements to break PD are
satisfied by overwintering in soil
surface (but GA3 and Kinetin break
dormancy in the laboratory). Thus
Table 2 (continued)
the species persist in soil until spring

and germinate readily once
dormancy in broken.
Vicia sativa, V. angustifolia, V. amoena Seeds dispersed in autumn have PD or Hu et al. (2013)
and V. unijuga PY or combined (PY + PD) and
require overwintering to break
dormancy. Once dormancy is broken
seeds germinate in spring.
Euphrasia minima and Although seeds can germinate at low Liebst and Schneller
E. salisburgensis temperature (5 °C constant (2008)
temperature or 3–10 °C varying
temperature) at the time of
collection, after-ripening widens the
temperature at which seeds germi-
nate. Thus, germination synchro-
nizes with spring. This feature
spread the germination over 3 years,
thus these seeds formed a persistent
seed bank.
Silene elisabethae Increase in duration of cold Mondoni et al. (2009)
stratification increased the
germination percentage indicating
the cold stratification requirement to
alleviate the non-deep PD. This re-
quirement for dormancy alleviation
should happen through
overwintering in nature (but GA3 in
laboratory) stimulating germination
in spring.
Polygonum cuspidatum and Only moist chilling (cold-wet Nishitani and Masuzawa
P. weyrichii var. alpinum stratification) was effective in (1996)
breaking dormancy of high-altitude
adapted P.weyrichii var. alpinum.
Seeds germinate at 5 °C following
the dormancy breaking treatment,
compared to 35 °C requirement at
the time of collection in autumn.
Peucedanum ostruthium After-ripening requirement for breaking Novak et al. (2011)
(non-deep)-morphophysiological
dormancy and high temperature
requirement (26 °C) delayed
germination until spring.
Achillea moschata, Hieracium Seeds sown in autumn only germinated Stöcklin and Bäumler
staticifolium, Oxyria digyna and in the spring suggesting cold (1996)
Rumex scutatus stratification is required for
germination in these species.
Anemone narcissiflora var. Seeds of E.nigrum, A. narcissiflora and Shimono and Kudo (2005)
sachalinensis, Arnica G. nipponica did not germinate at all
unalaschkensis, Bryanthus gmelinii, irrespective of treatment. However,
Bupleurum ranunculoides var. now it is now known that E.nigrum
triradiatum, Carex flavocuspis, C. needs additional dormancy breaking
pyrenaica, C. stenantha var. treatment. Similarly, with the
Table 2 (continued)
taisetsuensis, Diapensia lapponica exception of D. lapponica, V.

var. obovata, Empetrum nigrum var. uliginosum, P. frutescens, P.
japonicum, Fauria crista-galli ssp. cuneifolia and C. flavocuspis, all
japonica, Gentiana nipponica, other species germinated to higher
Loiseleuria procumbens, Patrinia percentage under warm temperatures
sibirica, Pennelianthus frutescens, (35/25 °C or 30/20 °C). Cold-wet
Peucedanum multivittatum, stratification given at 0 °C for
Phyllodoce aleutica, Potentilla 2 months significantly reduced the
matsumurae, Primula cuneifolia, temperature required for germination
Rhododendron aureum, Sieversia and cumulative germination per-
pentapetala, Solidago virga-aurea centage at all temperature regimes
ssp. leiocarpa, Therorhodion tested, i.e., 35/25 °C, 30/20 °C, 25/
camtschaticum, Tilingia ajanensis, 15 °C, 20/10 °C and 15/5 °C.
Vaccinium ovalifolium, V.
uliginosum, V. vitis-idaea and Ve-
ronica stelleri var. longistyla.
Caltha leptosepala At the time of dispersal, seeds are Forbis and Diggle (2001)
MPD. Dormancy is alleviated by
stratification at 2.5 °C, embryo
growth begins within 1 month and
germination begins in 4 to 7 months
of storage. PD determines the
germination timing.
Seeds form ‘transient’ seed bank break dormancy by cold-wet stratification/after-ripening conditions in the
soil. The ability of these non-dormant seeds to germinate the following spring is largely determined by
environmental conditions. Data on the seed longevity of these species to differentiate short-term or long-term
persistent bank are currently unavailable
generalize at ecosystem level. This is mainly due to the species-specific breaking require-
ments evolved in spermatophytes adapted to alpine environment (Table 2). Given most
species with PD, these seeds can cycle back to dormancy if the conditions are unfavorable
during early spring. Such cycling is also expected to be common in buried seeds (Baskin &
Baskin, 1998). The evolution of a dormancy cycle, regardless of the seed position in soil,
can be viewed asa specific control in preventing germination outside growing season. For
example, if the buried seeds are brought back to the soil surface (Fig. 1), dormancy cycling
checks the germination time to synchronize with growing season. Supposing such seasonal
change of dormancy had not evolved in alpine species, there would be a chance for buried
seeds (when they reach soil surface) to germinate any time of the year, provided other
environmental conditions are satisfied.
Temperature Requirement for Germination
Most of the seeds endemic to alpine environments do not germinate immediately after
shedding because the temperature required for germination is high (Sayers & Ward,
1966; Billings & Mooney, 1968; Densmore & Zasada, 1983; Nishitani & Masuzawa,
1996; Baskin & Baskin, 1998; Cavieres & Arroyo, 2001; Shimono & Kudo, 2003) and
in autumn this temperature is rarely - if ever - met. After overwintering, cold-wet

stratification reduces the high temperature requirement and seeds develop a tendency to
germinate at a wide range of temperatures (Baskin & Baskin, 1998; Table 1).
It is not uncommon for some alpine species to shed nondormant seed that remain
ungerminated during autumn due to the prevailing low temperatures (Billings &
Mooney, 1968). Seeds of Oxyria digyna can germinate immediately after dispersal if
the temperature is between 10 and 15 °C, but some seeds can even germinate below
10 °C, if the temperatures fluctuate between 13 and 2 °C and have light for 12 h
(Mooney & Billings, 1961). Neither cold-wet stratification, nor after-ripening is a strict
requirement for germination, rather the germination after seed shedding was impaired
by prevailing low temperatures in autumn. In accordance with this view, a warmer
autumn temperature is likely to increase the germination of some nondormant seeds,
e.g., Geum reptans, Veronica alpina and Oxyria digyna to autumn (Mondoni et al.,
2012). Such seeds are poorly represented in alpine communities, as the winter temper-
atures decimate seedlings (but see below).
Typically, 25 to 35 °C is the most favorable temperature eliciting autumn germina-
tion in the proportion of non-dormant/conditionally dormant seeds (Clebsch & Billings,
1976; Kibe & Masuzawa, 1994; Nishitani & Masuzawa, 1996; Körner, 1999; Novak
et al., 2011). Autumn germination is facilitated further if the temperature fluctuates
between 20 and 30 °C (Sayers & Ward, 1966; McDonough, 1970). However, these
relatively high temperatures do not occur in alpine environments during autumn
(Billings, 1974; Bell & Bliss, 1980; Reynolds, 1984). Elkington (1971) showed freshly
collected seeds of Dryas octopetala germinated to 48 % when sown at 25 °C under
controlled germination conditions, but field sown seeds in autumn germinated only in
the following spring, suggesting the temperature required for germination was not met.
Likewise, Marchand & Roach (1980) also reported seeds of Arenaria groenlandica,
Juncus trifidus and Potentilla tridentata germinated to 88, 88 and 52 % when tested in
laboratory at 23 to 28 °C, 19 to 23 °C and 21 to 26 °C respectively, however, only 38,
17 and 6 % of the seeds germinated in the field.
The mean autumn, spring and summer temperatures decrease with altitude. In addition,
snow cover often comes early but lasts longer at higher elevations (Lütz, 2011). Evidence
is mounting that the autumn and spring temperature optima for germination is different for
species occurring at different altitudes. In general, seeds from higher altitudes where
temperature minima is low have a tendency to germinate at lower temperature after cold
stratification, but seeds from lower altitudes experiencing warmer conditions during seed
development require higher temperature than high-altitude species (Dorne, 1981; Mariko
et al., 1993; Nishitani & Masuzawa, 1996). Thus, seeds moved from a low altitude in a
reciprocal transplant experiment germinated in the autumn at higher elevations, but when
seeds from higher altitudes were moved to lower altitudes seeds germinated only in the
second spring following transplant (Jaganathan et al., unpublished).
A simple germination experiment using Polygonum weyrichii var. alpinum and
P. cuspidatum seeds at a range of temperatures including 5, 10, 20, 25 and 35 °C,
showed that germination of seeds of both species could only be achieved in the autumn
at temperatures of 35 °C both in light and dark conditions (Nishitani & Masuzawa,
1996). Importantly, after cold-wet stratification, seeds of P. cuspidatum from Mt. Fuji (a
site experiencing relatively high temperatures) germinated equally well at 10, 20,
25 °C, contrasting with the poor germination of seeds from Shizuoka (relatively
moderate temperatures) at 10 °C. Similarly, in the case of Phacelia secunda, freshly

collected seeds did not germinate under simulated diurnal fluctuations at 20/10 °C or at
10/5 °C at the time of collection in autumn, but seed germination increased propor-
tionately with cold wet stratification duration (Cavieres & Arroyo, 2000). In particular,
seeds from low altitudes required lesser stratification duration and germinated equally
well at both the temperatures tested than did seeds from higher elevations (Cavieres &
Arroyo, 2000). In another study, Blionis & Vokou (2005) confirmed the ability of
higher altitude seeds to germinate at low temperature after overwintering in Campanula
populations. Also, Mondoni et al. (2009) showed seeds of Silene elisabethae collected
from the coldest site in their investigation germinated better at low temperature after
cold-wet stratification.
Vera (1997) studying the effect of altitude and seed size on germination and seedling
establishment of Calluna vulgaris, Erica cinerea and E. vagans collected from heath-
lands in northern Spain found that small sized seeds originating at higher altitudes
germinated well at 20 °C. A more recent study by Liu et al. (2013) on seed germination
of 445 species in a grassland community on the eastern Tibet Plateau, demonstrated that
after-ripened seeds germinate better at alternating temperatures (either at 5/25 °C or 10/
20 °C) than at a constant temperature of 15 °C especially if they were small forbs. More
studies are needed to offer clearer understanding of autumn and spring germination
ecology especially at the community level.
The local microclimate in fellfield environments is harsher than that of snowbeds
due to little snow accumulation, and reduced snow cover thickness and duration
(Körner, 2003). Snow patches covering soil for a longer time in snowbed fields offer
refuge to the seeds from low temperature. For instance, seeds under snow cover are
held in stasis and showed significantly lower level of damage and mortality than seeds
kept artificially snow free (Williams, 1987). On average, growing season length
decreases by 30–50 % from fell-field to snow-bed. Thus, habit-specific temperature
requirement for autumn germination is expected but there is no evidence for this trend.
For example, seeds of Potentilla matsumurae collected from both fellfield and snowbed
failed to germinate at the time of collection at 15/5 °C, but with increasingly warm
temperature cycles (20/10 °C, 25/15 °C, 30/20 °C, 35/25 °C) the germination percent-
age increased (Shimono & Kudo, 2003).
In the same study, Shimono and Kudo (2005) disclosed that seeds of some
species e.g., Arnica unalaschkensis, Bupleurum ranunculoides, Vaccinium
ovalifolium at the time of dispersal in autumn have a more moderate optimum
temperature regime, thus germination at higher temperatures of 35/25 °C is
unfavorable. However, in these species cold-wet stratification has widened the
temperature at which germination occurs. Overall, it seems logical to conclude
that the temperature requirement for germination both in autumn and after
overwintering in field is highly species-specific. Despite this, several sound pieces
of evidence indicate that it is safe to generalize that the requirement for high
temperatures for germination in autumn in alpine species can be beneficial to
postpone germination to spring, especially in non-dormant seeds. Furthermore,
studies that document germination temperature requirements have revealed both
inter and intra-species variation in autumn germinating temperature, but acknowl-
edge that the temperatures required for germination are not likely to be met in
autumn.
Light Requirement
Light is an important environmental factor stimulating germination in many seeds

(Milberg et al., 2000). The requirement of light for germination has been one of the
potential determinants driving species to accumulate a persistent seed bank (Baskin &
Baskin, 1998; Milberg et al., 2000; Pons & Fenner, 2000). A strict light requirement in
some alpine species not only prevents germination in late autumn, it also cues the timing
of germination to spring (Densmore, 1997; Fig 1).
Seasonally changing day length acts as a bottle neck in controlling alpine seed
germination. In Alaska, nonstratified seeds of Diapensia lapponica, Chamaedaphne
calyculata, Saxifraga tricuspidata and Ledum decumbens showed no or few germinat-
ing seeds under short-day conditions (Densmore, 1997). However, cold stratification
increased the proportion of germinated seeds of all species, significantly both under
short-day and long-day conditions. Similarly, longer-day conditions promoted germi-
nation in all PD seeds tested, except Poa alpina (see below; Schwienbacher et al.,
2011). Haggas et al. (1987) reported that seeds of Carex paysonis collected in
Beartooth Mountain achieved good germination only under complete darkness follow-
ed by light conditions at constant temperature (25 °C). Seeds incubated at 25 °C under
complete light or darkness resulted in poor germination. In addition to being dormant,
seeds of C. pendula required light for germination even after the dormancy is broken
(Brändel & Schütz, 2005). Seeds of Silene elisabethae, showed increased germination
percentage with increase in cold-wet stratification duration, but germination was tightly
controlled by light (Mondoni et al., 2009). Novak et al. (2011) also noted seeds of
Peucedanum ostruthium are better germinated at 26 °C only in light. These studies
clearly depict light plays a pivotal role in controlling the timing of seed germination
form seed banks.
By contrast, for some alpine species light is not required for germination, instead
light inhibits it. Examples of dark-requiring species include Poa alpina (Acharya, 1989;
Schwienbacher et al., 2011), Trifolium pallescens (Schwienbacher et al., 2011),
Anthyllis vulneraria subsp. alpicola (Schwienbacher et al., 2011), Agropyron latiglume
(Acharya, 1989), and Koenigia islandica (Heide & Gauslaa, 1999; Wagner & Simons,
2009). Both dark and light requirement in seeds can play a pivotal role in delaying
germination, thus contributing to seed persistence (Fenner & Thompson, 2005; Bewley
et al., 2013). Therefore, it seems reasonable to suppose that dormancy and light
requirement both circumvent autumn germination in alpine species, thus affecting the
composition of soil seed banks. In dark-requiring species (e.g., Trifolium pallescens),
dormancy can act as the main mechanism in preventing seed germination until the
growing season (Table 1). However, in spring, seeds experience light/dark cycles,
therefore it is not known if cold-stratification in winter imposes a light requirement
in the otherwise dark-requiring seed.
Important results from recent ecological studies suggest that environmental condi-
tions significantly contribute to the development of a light requirement in alpine
species. Seeds of Koenigia islandica collected from Iqaluit (Nunavut, Canada),
Yukon (Canada), and Jasper (Alberta, Canada) did not have a significant light-require-
ment for germination, whereas seeds collected from more severe climates, Svalbard
(Norway) and Colorado (USA), required light for germination (Wagner & Simons,
2009). Mondoni et al. (2012) showed that seeds of Oxyria digyna germinated at 2 °C
higher than the current alpine climate (12/12 h photoperiod) achieved higher germina-
tion, but that there is a tendency for the seeds to become autumn germinators because
dormancy is lacking. Unfortunately, the role of light in germination control was not
considered in their study. However, Billings & Mooney (1968) worked with O. digyna
seeds and reported that those collected from an American alpine location had greater
cumulative germination in light than in dark, but seeds of arctic origin did not have
strict requirement for light. The aforementioned studies suggest the evolution of a
requirement for light is more likely location-specific.
Light requirement in seeds has also been reported to be of great significance in
controlling the depth of burial at which germination occurs (Pons & Fenner, 2000).
Since light can only penetrate a few millimeters from the top of the soil surface, seeds
found below this depth do not germinate; and even in dark-requiring species, those
seedlings would die before reaching the soil surface, especially if they are small owing
to the smaller seedling size (see below). Data on other ecosystems suggest that seeds
that are smaller are more likely to require light for germination than larger seeds
(Milberg et al., 2000; Jankowska-Blaszczuk & Daws, 2007). In a recent study, Wu
et al. (Wu et al., 2013) found a similar pattern in alpine species of Qinghai-Tibetan
Plateau. Using twenty species, those authors reported significant negative correlation
between strength of light required for germination and seed mass, thus large-seeded
species were less likely to require light for germination than those of small-seeded
species. If small seeds are buried to greater depths, the strong requirement for light in
small-seeded species suggests that disturbance is an inevitable requirement in the
germination of seeds from seed banks. Nothing, however, is known of the light
requirement of seed in different stages of the seed bank cycle (Fig. 1).
While the studies illustrated above lend some support to the assertion that light plays
an important role in controlling seed persistence, this perspective requires detailed
experimental investigations. Because our knowledge on the relationship between light
requirement and germination is limited merely to genus Carex (Amen & Bonde, 1964;
Schütz & Rave, 1999; Schütz, 2002) and Koenigia islandica (Heide & Gauslaa, 1999;
Wagner & Simons, 2008, 2009), the understanding of the role of light in controlling the
autumn germination of some non-dormant alpine seeds is still rudimentary.
Nevertheless, we surmise that the long-day requirement for germination might be
common (but not ubiquitous) in alpine species. This is because, in any year with an
unfavorable growing season, long-day conditions will not be repeated until the follow-
ing year, a condition typical to all alpine environments. However, in favorable years, a
significant amount of light reaches the soil surface due to the lack of taller plants
(Billings, 1974; Densmore, 1997). Hence, in addition to dormancy, light requirements
also hold germination in check, thus contributing to seed persistence in soil.
Factors Affecting Seed Persistence
In many alpine species, the evolution of highly specific germination requirements, such
as those described above, delay the germination of autumn-dispersed seeds until spring.
Thus, the interplay of factors including dormancy, specific temperature requirement to
germinate and highly specific light or dark requirements in a particular species offers
triple safety measures against the harsh alpine climate; without these controls seeds are
more likely to have asynchronous germination thereby posing a serious risk of seedling
mortality (Billings & Bliss, 1959). For example, when seeds develop in a relatively
warm climate due to interannual variation, the degree of dormancy (sensu Baskin &
Baskin, 1998) may be reduced. In such cases, autumn germination may be prevented
by a high temperature requirement and/or light requirement instead of the depth of
dormancy acting as the primary obstacle to germination. If only one mechanism for
preventing germination has been evolved in alpine seeds, then the autumn germination
ability is likely to depend on the maternal environmental condition during seed
development and opportunistic temperature at autumn. Evolution of such complex
germination requirements is not unique to all ecosystems around the world. The
obvious example are flood meadows, where many seeds are non-dormant but germi-
nation is controlled by light and a narrow temperature requirement, hence dormancy
has no role in seed persistence (Hölzel & Otte, 2004 and references therein).
In addition to a complex suite of responses to varying environmental cues, it has
been suggested that not all the seeds of a particular species may respond to germination
cues stimulated by seasonal temperature cycles in alpine environments, thus carryover
of a proportion of seeds to next year is expected to maximize species fitness (Meyer &
Kitchen, 1994a; Meyer et al., 1995). Carry over mechanisms are common in unpre-
dictable conditions because the risk of germination is spread to different years. For
some alpine species, e.g., Carex frigida, low germination in the growing season tends
to favor carry over mechanisms (Schütz, 2002). Although the success of seeds carried
over to germinate in the next year depends on various phenotypic and genotypic factors
(Meyer & Kitchen, 1994a), how a species selects potential candidates for carry over is
not understood completely. Thus, it is not known if the seeds to be carried over were
predetermined at the time of shedding or the selection is a result of phenotypic
variability or simply that all the non-germinated seeds at the end of growing season
are carried over (but see Meyer & Kitchen, 1994a). However, the degree of dormancy,
position of seeds in soil and local microclimate are certainly important factors deter-
mining which seeds are carried over. Furthermore, for various reasons that are typical to
alpine environments, e.g., frequent summer frost (Marcante et al., 2012), only a
proportion of seeds germinate even in favorable growing seasons (Cavieres &
Arroyo, 2001), leaving the reminder to be part of the persistent seed bank.
Seed Size and Persistence
A commonly accepted prerequisite for seeds to enter persistent seed banks is the small
size and round shape (Thompson et al., 1993). Despite their suggestion that this
phenomenon is likely to be universal, subsequent studies testing the prevalence of
small, round seeds in persistent seed banks have argued both for (Bekker et al., 1998;
Thompson et al., 2001; Zhao et al., 2011), and against (Leishman & Westoby, 1998;
Moles et al., 2000; Yu et al., 2007) the hypothesis. There have been few works that
studied the significance of seed size in establishing persistent seed bank in alpine
landscapes. In Argentinean mountain grassland, the available evidence demonstrated
that small seeded species have an increased likelihood of entering the persistent
seed bank (Funes et al., 1999; Fig. 2). Conversely, Cerabolini et al. (2003) showed
a negative correlation between seed size and persistence in species tested on
Italian Alps (Fig. 2).
Fig. 2 Relationship between seed mass (log scale) in mg and variance of seed dimension adopted from (a)
Italian Alps; 114 species (re-drawn only for alpine species from Cerabolini et al., 2003 with permission), b
Central Austrian Alps (Schwienbacher et al., 2010) after excluding the standard deviation given in the original
data set and c Argentinean mountain grassland; 71 species (re-drawn from Funes et al., 1999 with permission).
(Δ ) Transient, (●) Long-term persistence, (■) short-term persistence, and (♦) persistence (but no information on
whether short or long-term), (X) uncertain or could not classified. More detailed information of how to
calculate the variance of dimension can be found in Thompson et al. (1993). In order to make some extremely
small seeded data point readable in the Argentinean mountain grassland (c) we have rescaled the x-axis of this
study to begin from 0.001
Recent years have witnessed a surge of studies determining seed longevity in soil using
artificial burial experiments. Schwienbacher et al. (2010) conducted such an experiment in
the Central European Alps (ca. 3500 m a.s.l; Austria) for Achillea moschata, Artemisia
genipi, Anthyllis vulneraria subsp. Alpicola, Geum reptans, Linaria alpina, Oxyria digyna,
Saxifraga aizoides, S. oppositifolia and Trifolium pallescens. Seed germination following
excavation at 1, 2 and 5 years revealed, with exception of Geum reptans and S. oppsitifolia
(which have extremely tiny seeds), at least some of the seeds buried at a depth of 3 cm
survived for a minimum of 2 years (Fig. 1; Table 2). However, their study had two surprising
results. Firstly, in contrast to the suggestion that round seeded species have increased
tendency to enter the persistent seed bank, flattened L. alpina seeds survived for 5 years
forming a long-term persistent bank, whereas other flattened seeds of O. digyna did not
survive for 5 years. Secondly, species classified as transient by Cerabolini et al. (2003), were
shown to form short-term persistent or long-term persistent seed banks (Table 1). The only
other attempt to use an artificial burial approach to test seed viability for >1 year in alpine
tundra was a study in the Chilean Alps (Arroyo et al., 2004). From a total of 15 species
studied, all but two species namely Senecio magellanicus (with cylindrical shape but smaller
size) and Berberis buxifolia (6.33 mg), survived for 2 years. However, they terminated the
experiment in 2 years, therefore a distinction between short-term and long-term seed
persistence is not feasible.
There are several lines of evidence showing that small seeds easily become buried,
thereby escaping post-dispersal predation, remaining in the same environment in which
they had developed and becoming part of the persistent seed bank (Peco et al., 2003;
Ma et al., 2010b). If this holds true then seeds at depth in the soil are expected to be
smaller than the seeds in the surface layer. However, there are only a few experimental
studies addressing the vertical movement of seeds in alpine flora. In the Austrian Alps,
Klug-Pümpel and Scharfetter-Lehrl (2008) found small seeded species move to greater
depths than large seeded species, but Ma et al. (2010b) failed to find such pattern in 122
species of Tibetan Plateau, China. The important question perhaps then is: what depth
is safe for seeds? Ma et al. (2010b) showed that seeds buried (naturally) to 15 cm can
germinate when excavated and sown in optimal germinating conditions. Seeds artifi-
cially buried to 3 cm deep germinated after 5 years (Schwienbacher et al., 2010;
Table 1). However, over the same time period but at 8–10 cm depth, Adzhiev et al.
(2011) reported no germination in 45 out of 63 species of the Northwest Caucasus.
It is difficult to draw any firm conclusion on the impacts of seed size on persistence
in alpine seed banks from these studies mainly because of the overriding effect of other
factors influencing results, three of which are discussed here. The first to be considered
is the type of soil surface where seeds land. If seeds are deposited on a surface having
smaller particles, there is an increased likelihood that small seeded species rather than
those with large seeds, and those with adhesive seed coats are trapped amongst the soil
particles and buried in the soil (Chambers et al., 1991; Chambers, 1995, 2000). Small
soil particle size may enable the large seeded species to move horizontally over longer
distances until they encounter soils with large particle sizes. The smaller seeds fre-
quently trapped by soil of smaller particle size often move to a deeper position than the
larger seeds trapped in large particle soil. In contrast, both small and large seeded
species are buried easily if seeds were deposited on soil surface having larger particle
size (see Chambers et al., 1991 for a detailed discussion).
A second confounding factor when trying to generalize on the relationship between
seed size and persistence is derived from the understanding that entry to the soil seed
bank confers longevity. It is perhaps an over-simplification to say that ease of burial
improves the longevity of small seeded species in the alpine system. Indeed, seeds
buried to greater depths do not germinate, unless the soil is overturned but, if distur-
bance is very infrequent, these species may be lost from the aboveground community
and eventually from the seed bank also. For example, in the central Chilean Andes,
Arroyo et al. (1999) found buried seeds of Chaetanthera pusilla were viable, although
the species did not occur in the standing vegetation. Similar results were obtained in the
alpine regions of Tibet for a wide range of species: a total of 87 species were identified
in the soil seed banks, but only 62 appeared in the standing vegetation (Ma et al.,
2010a). There are no data available on how long these seeds can be viable but
presumably, this longevity will be species-specific. Nonetheless, dating by accelerator
mass spectrometry revealed seeds of Carex bigelowii and Luzula parviflora in Alaskan
tundra had at least persisted for two to three centuries (McGraw et al., 1991).
A third problem with linking seed size and persistence is the inconsistency in
methods with which seed longevity is determined; this causes subsequent confusion
when trying to build causal relationships between size and viability. For example, seeds
of some species classified as transient by Cerabolini et al. (2003), survived more than
1 year when tested with artificial burial experiments (Table 2). It has been suggested
that the discrepancy in the findings of these studies has resulted from different methods
employed in testing seed longevity (Schwienbacher et al., 2010). Cerabolini et al.
(2003) used published information and germination experiments conducted with
seeds excavated from soil kept in glass houses to classify the seed bank type,
whereas Schwienbacher et al. (2010) classified the seed bank type based on data from
artificial burial experiment. Each method has its own advantages and disadvantages; the
artificial burial approach often overlooks the mechanism of burial, which is arguably a
complex process itself (Thompson et al., 1997). Therefore, the conclusion of
Schwienbacher et al. (2010) that Linaria alpina retains its viability in the soil for
5 years as estimated by artificial burial experiments, can be called into question because
the soil environment may not enable adequate burial and subsequent avoidance of
disturbance to maintain the conditions generated in their experiment. Thus, whether
shape is a good predictor for seed persistence or not, remains largely equivocal for
alpine species. More meaningful answers to this question will only come from novel
seed bank studies that combine both natural soil sampling and artificial burial approach
incorporating small and large seeds.
While some small seeded species more easily enter persistent seed banks than large
seeded species, careful consideration of seed persistence studies point to the possibility
that not all small seeded species can potentially establish persistent seed banks (Fig. 2).
Similarly, generalizations on large seeded species are inappropriate as some of these
can also establish short-term persistent seed banks (Fig. 2). As yet, there is no evidence
available to demonstrate whether large seeded species possess a long-term persistent
seed bank in alpine landscapes (Fig. 2). However, a short-term persistent seed bank
tends to be adequate for maintaining species in alpine conditions, because the favorable
weather conditions can occur at least once every few years (Körner, 2003).
Furthermore, most of the plants adapted to alpine tundra are perennials and produce
seeds in fairly large amount, at least in the favorable years, and although a long-term
persistent seed bank is adaptive to the alpine climate, it is not necessary for a species to
succeed in colonization.
Seedling Establishment
An additional factor that complicates our understanding of the significance of seed size
in persistence is the hypothesis related to seedling establishment. With finite resources
allotted to reproductive success, a given species may produce more small seeds or less
large seeds, leading to a variation in seed mass often spanning five to six orders of
magnitude across species found in a particular ecosystem (Thompson, 1987; Jakobsson
& Eriksson, 2000; Leishman et al., 2000; Leishman & Murray, 2001). A growing body
of literature is specifically devoted to understand how such variation in seed size
influences the fitness of plant communities (Leishman & Murray, 2001). Although
small-seeded species benefit by producing more number of seeds than large seeded-
species and have an increased likelihood of entering soil banks, the latter group might
counteract the advantage by establishing high number of successful seedlings than the
small seeded-species.
Because seed germination is an irreversible event, timing of germination is a critical
component in the life-cycle of alpine plant species. Seeds, once germinated, have to
continue growing or die. Seedling establishment in alpine environments is a slow
process and often lasts for several years (Jaganathan, personal observation). Although
some of the seeds germinating under snow cover are very slow requiring up to 6 months
to achieve 50 % germination (Meyer et al., 1995), spring germinators must attain a
suitable size to tolerate subsequent winter conditions (see Leishman et al., 2000), if not,
seedling mortality becomes prevalent. If this holds true, then it is reasonable to
expect that large-seeded species establish seedlings more quickly and there may be
a trade-off between seed size and mean germination time (MGT). Consequently,
we anticipate that large-seeded species must germinate faster than small ones to
maintain an advantage over the seed bank strategy prevalent in small-seeded
species.
We tested this hypothesis in 653 Qinghai-Tibet Plateau species (original data from
Bu et al., 2007a; Wu et al., 2013). Species were only included in this analysis if they
were recorded as germinated. Hence, species recorded with MGT of 0 (failed germi-
nation) were excluded from this analysis. In this way, we were able to select a total of
585 species from 39 families. We performed a linear regression to explain the relation-
ship between seed mass and their respective MGT. In contrast to our expectation, we
observed no significant relationship between seed mass and MGT (slope=1.8, R2=
0.01, d.f.=584, p>0.05) (Fig. 3).
If large seed size does not confer an advantage with respect to MGT an alternative
benefit may be bestowed through greater seedling size (Vera, 1997; Moles & Westoby,
2004). However, dormancy can regulate germination only in terms of when in the
growing season emergence occurs for more successful seedling establishment. Further,
there is little evidence that large-seeded species have some advantage in survival over
small-seeded species (even within same genus, see Vera, 1997). We conclude that this
advantage may not counterbalance the large number of seeds produced by small-seeded
species and their ability to persist in soil.
Fig. 3 The relationship between seed mass and MGT (Mean Germination Time) estimated for 565 Qinghai-
Tibet Plateau species. Number of days required for germination increased with increase in seed size (slope=
1.8) but the relationship is not significant (R2=0.01, d.f.=584, p>0.05). Each point represents one species
Seed Dispersal
At the ecosystem level, microhabitat and seed availability determine the composition
and diversity of species (Bullock et al., 1995; Tackenberg et al., 2003; Ozinga et al.,
2004). Seed dispersal has a marked effect on seed availability in any given location and
the distribution of the ‘seed rain’ is potentially very different to that of the parent plants.
Plants adapted to short-growing seasons in unpredictable environments are believed to
disperse seeds over a longer distance, so that seeds experience different weather
conditions and germinate in the environments where conditions are favorable
(Bakker et al., 1996; Baskin & Baskin, 1998; Tackenberg et al., 2003). Given the
unpredictability in climate, it is reasonable to expect alpine species have long distance
dispersal (LDD). In spite of a pullulating interest on understanding the seed dispersal in
low-altitude ecosystems, our knowledge on seed-dispersion patterns for alpine ecosys-
tem remains conjectural (McGraw & Vavrek, 1989; Muñoz & Arroyo, 2002). In
particular, research on alpine seed dispersal has mostly concerned the mode of seed
movement, rather than precisely estimating how long seeds could move. One reason for
this lacuna is the difficulty in tracking all routes a seed could move from mother plant
to the germination site. Even for the studies that attempted to quantify the distance,
results were influenced by several other factors such as height from which seeds are
dispersed; size and morphology of seeds; morphological adaptations for dispersal;
dispersal vectors availability; wind speed at the time of dispersal and wind direction.
Seed movement within alpine landscapes involves numerous dispersal vectors. Most
frequently seeds are dispersed by wind (Van der Pijl, 1982; Willson et al., 1990;
Table 3). A simulation model in the glacier foreland of the Dischma Valley,
Switzerland has shown that more than half of the alpine species were dispersed a long
distance by wind, whereas only 25 % of low altitude species tend to have LDD
(Tackenberg & Stöcklin, 2008). Because the horizontal movement of seed can be
affected by the wind speed, Tackenberg and Stöcklin (2008) also measured the wind
speed in alpine and low-altitude, but found only a small difference between these two
environments. However, wind speed may not only vary between season but also years
(Billings & Bliss, 1959). Furthermore, secondary movement of seeds also depends on
the soil characteristics (Chambers et al., 1991; Chambers, 1995, 2000). The small-sized
Table 3 Distance seeds moved by wind
Species Distance Reference

moved
Ranunculus adoneus 30 cm Scherff et al. (1994)

Arenaria groenlandica, Juncus trifidus, Potentilla tridentata and 1m Marchand and Roach
Diapensia lapponica (1980)
Erythronium grandiflorum 1m Weiblen and Thomson
(1995)
Campanula thyrsoides <10 m Frei et al. (2012)
Epilobium fleischeri, Senecio incanus, Geum reptans, Oxyria >100 m Tackenberg and Stöcklin
digyna, Saxifraga bryoides, Doronicum clusii, Linaria alpina, (2008)
Poa alpina and Leucanthemopsis alpina
seeds frequently trapped by smaller particle size move vertically, thus do not move to
long-distances (see Chambers et al., 1991 for a detailed discussion). Therefore, it is not
known if the simulation model has overestimated the role of soil characteristics and
wind speed in secondary seed dispersal.
The dogma that seed dispersal agents are rare in alpine environments (McGraw &
Vavrek, 1989), has been disproved by active research over the last two decades. Seeds
of many alpine plants could successfully survive passage through the intestinal tract of
animals, i.e., endozoochory (Bruun et al., 2008; Yu et al., 2012). For some species, this
passage promoted germination, whereas for others it suppressed the total percentage of
germinated seeds. A good example is the Andean (Chile) shrub Berberis empetrifolia
dispersed in the faecal deposition of Liolaemus bellii. After passing through the
digestive tract, germination increased significantly when compared to the untreated
control (Celedon-Neghme et al., 2008).
In the alpine forest of southwestern China, species of Pinus armandii, P. densata,
Abies sp. and Viburnum sp. were predated by rodents (Wang et al., 2012). Two years of
a seed caching experiment showed not only that seeds of P. armandii were dispersed to
<10 m but also rodent seed selection for caching was size-specific. In the experiments
conducted with two populations of endangered Spanish black pine P. nigra in the
Cuenca Mountains of Central Spain, seed predation in a mast year was significantly
lower compared to the low seed producing year (Lucas-Borja et al., 2012) suggesting
seed predation varies between years. Mountain snowberries (Gaultheria depressa)
endemic to New Zealand alpine ecosystems was consumed by scree weta
(Deinacrida connectens) and moved long distances (Larsen & Burns, 2012), however
such dispersal events are rare.
The ability of ants to disperse seeds was assessed experimentally in Central Chilean
Andes for Sisyrinchium arenarium (Iridaceae) (Muñoz & Arroyo, 2002). Insightful
measurements made at two different altitudes (2700 m and 2000 m) revealed greater
activity of ants and birds at higher altitude compared to lower altitude, however, the
overall seed removal by ants was significantly greater than birds at both elevations. In a
subsequent study those authors showed that 9 species namely Alstroemeria pallida,
Anarthrophyllum cumingii, Chuquiraga oppositifolia, Laretia acaulis, Rhodophiala
rhodolirion, Sisyrinchium arenarium, Taraxacum officinale, Azorella monantha and
Pozoa coriacea, were dispersed by ants and birds, but only over a short distance
(Muñoz & Cavieres, 2006). In the sub-alpine locations of Mt. Norikura, Kita-Alps,
Japan, seeds of Dicentra peregrina were observed to be dispersed by Formica
gagatoides, but the distance is not known (Komatsu et al., 2014). To the best our
knowledge, experimental evidence of ants dispersing seeds in other alpine environment
has not been documented elsewhere. However, a growing number of studies are
explicitly showing the significance of seed dispersal by birds in other alpine locations.
For instance, in New Zealand, some fruit species were dispersed only by a fruit-eating
parrot, kea (Nestor notabilis) (Young et al., 2012), but the specific distance of seed
movement was not measured.
In New Zealand, 10 Veronica species disperse their seeds by the mechanism of
hygrochasy (Garnock‐Jones & Lloyd, 2004; Pufal et al., 2010). Hygrochasy is gener-
ally understood as the ability of seed holding structures to dehisce when the moisture
content of those structures increases to a certain threshold level. This mechanism of
seed dispersal is common in desert species, where water availability and seed dispersal
(and germination) must coincide. The evolution of hygrochasy beyond these alpine
endemics needs further clarification, although it is assumed that this mode of dispersal
does not favor LDD.
Many alpine species were able to float in water for more than 1 year, when
empirically tested (Danvind & Nilsson, 1997). Nevertheless, long-distance movement
of seeds by floating may be constrained by several factors (Danvind & Nilsson, 1997).
Since alpine landscapes are covered by snow for most of the year, there is a greater
probability that the seeds dispersed outside the snow-free growing season land on the
snow blanket. Although these seeds are dispersed by wind (Matlack, 1989; Chambers
& MacMahon, 1994), accumulating snow cover precludes further movement once the
seed has come into contact with the snow surface. During snow melting these seeds
move, but only over a short distance. For example, the work by Scherff et al. (1994)
showed melting snow moved seeds of Ranunculus adoneus only to a distance of 10 cm.
Similarly, Glaser (1981) observed extremely scarce movement of seeds when snowbeds
melted in Mount McKinley National Park, Alaska. Evidence of this kind clearly
demonstrates that the distance seeds move by this mode is inconsequential (Greene
& Johnson, 1997).
In recent years, the influence of humans on alpine vegetation has become more
pronounced. The construction of roads or walkways, regular visits to specific areas for
research and education, and the recent surge of interest in mountain tourism frequently
disturb vulnerable alpine communities. In addition, man and man-made machines are
more likely to move lowland seeds in to alpine environments. Emerging studies have
just started to understand the severity of the consequences for alpine plants, but for
some lengthy treatment of this subject consult Pauli et al. (2001). Trampling damage
due to walkers entering the Central Tasmanian alpine vegetation affects the shrubs,
shrubland and grassland, although fen tend to be more resistant (Whinam & Chilcott,
1999). Non-native seeds belonging to 17 families have been identified in polar regions
as a result of accidental transport by visitors (Ware et al., 2012). In Mount Norikura
(Japan), construction of road has changed the species composition as a result of
alteration in canopy and soil nutrition (Takahashi & Miyajima, 2010).
Except for wind dispersal, our knowledge of seed movement and potential dispersal
distances by other modes remains far from satisfactory. Indirect evidence suggests that
limited seed availability due to short-distance dispersal impedes the regeneration
potential in open alpine landscapes rather than microhabitat availability. For example,
restricted dispersal of Vaccinium myrtillus, Rhinanthus minor, Rumex acetosa,
Cicerbita alpina, Trollius europaeus and Campanula thyrsoides appears to be the
foremost reason for the patchy distribution, because seeds added manually to unoccu-
pied sites resulted in successful germination (Lindgren et al., 2007; Frei et al., 2012).
It has been argued above that LDD is a sporadic event in alpine species. Whilst this
is based on limited evidence, we nonetheless expect a larger set of data might yield
similar results. As of now, the notion that LDD is rare in alpine species should be
viewed as a working hypothesis rather than conclusion.
Dispersal vs. Persistence
Given finite reserves of energy to establish their off-spring successfully, many plants
have evolved different ways of ensuring dispersal to different locations or persistence in
soil to reduce the so-called ‘colonizing effect’. One way is to invest in seed dispersal
structures to attain longer dispersal. Information regarding the seed dispersal structures
for alpine flora are incomplete, but a few alpine plants have been reported to invest in
seed dispersal structures (Chambers & MacMahon, 1994). Bu et al. (2008) provided
substantial data on the seed dispersal structure at community level in eastern Qinghai-
Tibet plateau (Fig. 4). This data set suggests that most of the alpine plants present do
not invest in any specific dispersal structures (Fig. 4), although a few species do invest
in wind dispersal structures. In their work on comparing seed dispersal patterns for
various plant communities, Willson et al. (1990) noted many alpine species could have
morphological adaptations for wind, thus seed dispersal by wind may be common,
amongst other available dispersal vectors.
While the studies by Willson et al. (1990) and Bu et al. (2008) generally agree that
most alpine species neither invest in specialized morphological structure nor move long
distances, the question as to why this is the case cannot be answered from available
evidence. There may be several plausible explanations, although none of them have
been rigorously treated in experimental works. Due to plant development in extremely
cold-climates, the parent plant may have only limited resources allocated for seed
development (Forbis, 2003; Körner, 2003). Larger seeds with specific dispersal struc-
ture means augmented investment, a reason that might explain why there were fewer
fleshy seeded species observed by Willson et al. (1990). Furthermore, seed develop-
ment must take place in a short time, if not, the development is carried over to next year
– principally because most alpine plants (and plant parts) are held in stasis by the snow
cover except the seed producing and growing season.
A decade ago, Körner (2003) tentatively concluded that most of the alpine species
may have seed mass of less than 4 mg. Extending his suggestion to a larger data set of
more than 1000 species by reworking the data presented by Ma et al.(2010b), Funes
et al. (1999), Cerabolini et al. (2003), Körner (2003), Giménez-Benavides et al. (2005),
Fig. 4 Dataset of 633 species collated by Bu et al. (2008) showing number of species investing in specific
dispersal structure
Pluess et al. (2005), Shimono and Kudo (2005), Bu et al. (2007a), Schwienbacher et al.
(2010), Ma et al. (Ma et al., 2013) [from the seed size summary data] and Wu et al.
(2013), we show that 88 % of the species have seed mass below 3 mg and nearly 93 %
have seed mass below 4 mg, reinforcing the selection of small-seeded species in alpine
vegetation. Furthermore, in literature where seed mass data are not presented for
individual species, those studies have some useful summary of seed mass range. For
example, of the 122 species reported in the study by Ma et al. (2010b), only few were
above 3 mg, with the seed mass of 4.3618 mg (Vicia multicaulis) as the largest seed.
Baker (1972) first proposed that seed weight decreases with elevation using a data
set from California. However, successive studies have either rejected (Mariko et al.,
1993; Pluess et al., 2005) or accepted (Bu et al., 2007b; Guo et al., 2010; Dainese &
Sitzia, 2013) this proposition, thereby undermining the generality of this pattern. One
plausible reason for lack of unanimity in results is because in these studies the climatic
conditions in which the seeds have developed were poorly measured or ignored. It has
been stated that the short length of summer and low temperatures at high-altitude
potentially limits the seed development duration and ‘there may simply be inadequate
time available for producing and stocking large, heavy seeds’ (Baker, 1972). To
support this view, seed developmental studies of Gentianella germanica comparing
histogenesis and maturation drying over 3 years, have indicated that seeds developed in
colder years were smaller and poorly developed when compared with seeds from the
warmer year (Wagner & Mitterhofer, 1998). Similar conclusions have been presented
for numerous species including Potentilla pulcherrima (Stinson, 2004).
Another limitation of the debate on the impact of seed size is due to the differing
objectives and methods used to determine if a relationship exists between seed size and
elevation. For Baker (1972) the average seed weight of species occurring at a particular
altitude compared with the mean seed weight at a different (higher) altitude shows a
decreasing trend, although discussions on one (Penstemon) genera and possibly same
results on other genera were presented. Pluess et al. (2005) measured the seed size in 29
Swiss alpine congeneric species and found seed size increased with altitude for 55 % of
the species tested, but decreased or remained equal for 3 % and 41 % of species
respectively. Nevertheless, populations of Scabiosa lucida, Saxifraga oppositifolia,
Epilobium fleischeri and Carex flaccafound occurring at different altitudes showed a
decrease in seed size with altitude. Mariko et al. (1993) working with Reynoutria
japonica seeds collected from various altitudes of Mt. Fuji, concluded that mean seed
weight of the upland population was significantly heavier than that of the lowland
populations. Interestingly, the proposition that seed size increases with altitude is
attributed to the fact that seedlings from larger seeds are more likely to survive extreme
conditions than seedlings developed from small seeds. However, if seedling size
advantage is a reason for the increased seed size observed with altitudes, this does
not explain why large seeded species are rare in high altitudes (Table 4). Although we
are inclined to believe that having a larger seed in comparison to low altitude species
may be advantageous for alpine species of higher altitudes, we also accept that this
‘trend’ is not universal - even within an individual plant the seeds produced vary in size
significantly, presumably due to numerous intrinsic and extrinsic factors, e.g., maternal
environment, heteromorphism etc.
The underlying hypothesis describing the evolution of alpine plants has not yet been
completely understood. However, it is suggested that some of the spermatophytes
Table 4 Seed size of 1011 species collected from the published literature, Ma et al.(2010b), Funes et al.
(1999), Cerabolini et al. (2003), Körner (2003), Giménez-Benavides et al. (2005), Lorite et al. (2007), Pluess
et al. (2005), Shimono and Kudo (2005), Bu et al. (2007a), Schwienbacher et al (2010), Ma et al. (Ma et al.,
2013) [from the seed size summary data] and Wu et al. (2013)
Seed size (mg) Number of species
0–3 886 (87.6 %)

3–6 82 (8.1 %)
6–9 20 (1.9 %)
9–12 9 (0.9 %)
12–15 5 (0.5 %)
15–18 3 (0.3 %)
18–21 1 (0.1 %)
21–24 2 (0.1 %)
27–30 1 (0.1 %)
36–39 1 (0.1 %)
63–66 1 (0.1 %)
Grand total 1011
For some species, seed mass was determined by searching the seed information database (Royal Botanic
Gardens Kew Seed Information Database (SID))
colonized tundra vegetation by dispersing seeds with differing phenotypes, some of

which could survive extremely complex and uncertain alpine weather (Billings &
Mooney, 1968; Marchand & Roach, 1980). The exact empirical evidence verifying
this hypothesis cannot be possibly secured, but this view appears true, especially in
terms of recent literature contemplating the encroachment of low-altitude species into
the alpine vicinity as a consequence of global warming providing optimal survival
conditions (e.g., Pauli et al., 1996; Gottfried et al., 2001; Parolo & Rossi, 2008; Walther
et al., 2009).
Many theories have been proposed to explain the drivers behind evolution of seed
selection and adaptation. Hubbell’s (2001) neutral theory of biodiversity assumes all
individuals of all species are functionally equivalent, thus species abundance in a
community is driven by the stochastic events such as dispersal, local extinction and
speciation. This is in contrast to niche theory, which claims each species has its own
traits and these independent species co-exist within a community (Coomes et al., 2002).
Leishman and Murray (2001) argued that seeds of early successional species were often
smaller with good dispersal capacities. Such seed traits were advantageous in evolution,
as a higher number of seed increases the probability to find different climates and
germinate on suitable microsite. However when succession proceeds, both small and
large-seeded species become more common, possibly due to the ability to persist in soil
seed banks (either influenced by environment or maternal affects). More recent studies
have therefore rejected the prediction of neutral theory (McGill, 2003; Gilbert et al.,
2006), indirectly supporting the overriding role of environment in selecting the
phenotype.
It has been shown in Qing-Hai Tibet Plateau that early successional species were
small but achieved high abundances, thus, seed size acted as a main determinant of
species abundance (Chu et al., 2007). In addition, seed mass was negatively related to
species density early in the succession and this relationship became insignificant with
time, implying large-seeded species started colonizing in later successional stages. This
idea has been reinforced by examining the community assembly changes in Qinhghai-
Tibetan Plateau China, where abundant species in an early-successional meadow were
shown to be small-seeded species (Zhang et al., 2012). However, the question as to
what extent environment acted as a selective pressure and determined the evolutionary
origin of alpine seeds along the successional gradient still remains unclear.
These studies, although few in number, offer insights suggesting that, owing to the
advantage that species with smaller seeds have in entering seed banks (Funes et al.,
1999; Cerabolini et al., 2003; Schwienbacher et al., 2010), most alpine species may
benefit from the seed banks rather than dispersal. Furthermore, seeds in alpine soil
remain frozen most of the year and therefore secondary dispersal could be limited
during these periods. This feature essentially drives the seeds to establish a soil seed
bank. Consequently, entry into a seed bank may be critically advantageous not only
because little to no investment for separate structures is required but also because the
low soil temperature ensuring increased longevity of seeds (McGraw et al., 1991). We
therefore suggest that most alpine seeds have an increased tendency to be found in a
seed bank in the model developed by Chambers and MacMahon (1994).
This review has thus far dealt with various factors that influence the entry and exit of
seeds into alpine seed banks but all of these bar the external environment are strongly
affected by the phylogeny of the species themselves. The relatedness of taxa in alpine
systems therefore has the potential to explain some of the variation in seed size and
morphology, dispersal strategy, dormancy mechanisms and response to germination
cues, all of which affect the composition of seed banks. Links between phylogeny and
traits affecting seed bank membership have been made in temperate systems (Mazer,
1989; Leishman et al., 1995), tropical communities (Norden et al., 2009) and alpine/
subalpine vegetation (Bu et al., 2007a, 2008; Xu et al., 2014; Zhang et al., 2004). More
generally, Finch-Savage and Leubner-Metzger (2006) highlight the common evolution-
ary path for dormancy that means it is present throughout the higher plant families with
only a few exceptions, and in all major climate zones. However, associations between
phylogenetic groupings and germinability (measured as germination percentage, ger-
mination time, or both) whilst being significant, are very variable and models point to a
number of sometimes unidentified alternative explanators. For example, Bu et al.
(2008) could explain only 12 % of the variation of germination time in a one way
ANOVA by using phylogeny, whilst Bu et al. (2007a, 2007b) attributed 65.4 % of
germinability variation to genus-level groupings using GLMs that also included habitat,
a non-significant explanatory variable. In addition to these ambiguous results, there is a
geographic focus to the plateau communities of central Asia and until researchers in
other regions emulate their efforts, no generalities can be made.
Conclusions/Future Research Needs
Understanding how alpine seeds establish seed banks is of extensive ecological and
practical importance, because changes induced by global warming directly affect seed
regeneration potential, thus influencing the floristic changes of alpine environments.
Our ecological understanding of seed persistence in alpine ecosystems is still in

its infancy, although seed persistence in soil seed banks is clearly an ecolog-
ically important trait for most alpine species. It is therefore not surprising that
most of our discussion stems from studies addressing seed adaptation in alpine
environment, rather than seed bank studies per se. Many areas have received
only sporadic attention and data from those studies can be subjected to criti-
cism for their disagreement in results and also due to bias in sampling. For
example, a handful of studies (e.g., Schwienbacher et al., 2011) have stored
seeds at a condition that would benefit the physiological changes favoring
dormancy alleviation and progress the seeds towards germination before being
used in original experiments. Needless to say, such shortcomings must to be
avoided in order to precisely understand the effects of maternal environments
imposed on seed development. In addition, we have identified several areas that
require future research with emphasis on the following:
(1) The inherited traits of dormancy, germination temperature and light requirement
could be affected to some extent by the maternal environment, which exert a
selective pressure in developing physiological mechanisms that are location-
specific. The effect of maternal climate affecting some of the adapted traits clearly
suggests that these traits are likely to be altered in a future warming climate.
Evidence for these patterns is already becoming apparent in some of the alpine
locations. However, much remains to be studied.
(2) It is suggested that climatic conditions in the growing season only partly controls
seed carry-over. Because of specific germination temperatures required for each
species present in a population, some temperatures preclude germination in some
species and carry the seeds forward; the same temperature would initiate germi-
nation in other species. Since not all dormant and small seeded species enter
persistence seed banks, there is a possibility that some other (physiological)
factors are also involved in persistence under alpine climate. In addition to finding
such factors, if any, contributing persistence, we need more rigorous appraisal of
seed characteristics in relation to the environment. These approaches should also
take inter alia inter-annual and inter-population variability into account. Thus,
more specific studies delineating the point at which seeds bury in the model
(Fig. 1) are needed.
(3) Driving forces selecting seeds for seed banks must be evaluated in detail. Seed
loss by germination and dispersal should be documented clearly. More especially,
knowledge on dispersal is important in spatial demography studies particularly on
soil seed banks. Many studies have shown vegetation of alpine regions is patchy
possibly due to limited dispersal. LDD rarely occurs in alpine regions. If seeds do
migrate to long-distance, habitat-dependent germination requirement are not met
often, thereby seeds either germinate asynchronously to the dispersed environ-
ment or remain in soil for long time.
(4) While a limited number of recent studies mostly on Qinghai-Tibet plateau, China,
have focused on dispersal structure, little –if any- information exists on commu-
nities from other locations. This limited data on seed dispersal structure and
dispersal distance dataset clearly underpins the need for more community level
studies, paying particular attention to altitudinal and climatic influence.
(5) Further phylogenetic investigations are needed to tease out the relationships
between the key traits affecting the entrance to, and persistence in, the alpine
seed bank and evolutionary origins of various responses to alpine environments.
Furthermore, research in many more alpine regions other than central Asia
is needed. Phylogenetic explanators of seed bank membership, if they exist,
would allow more insightful predictions of responses to environmental
change where species composition of the above- and below-ground com-
munities is known, but responses of seed germination under warming
conditions is untested.
(6) A critical understanding of the germination requirements of local and invading
species is essential. Many species probably survive changing climate by migrating
to the locations where the originally adapted-for conditions still prevail (Hughes,
2000; Walther et al., 2009). Climate change has now surpassed a threshold,
inexorably forcing us to get a glimpse of types of plants that would survive in
the future climate and in so doing, more meaningful conservation strategies can be
devised. There is persuasive evidence that global warming will result in migration
of low-altitude plants to alpine environments. The lower likelihood of alpine seeds
reaching new environments highlight the need to recognize the interaction of
encroached species with the endemic alpine seeds germinate from soil seed banks.
In the future climate, these interactions essentially determine the species compo-
sition in alpine environment.
Insights into these areas will essentially help reveal the selective forces behind the
seed adaptation/selection in alpine environment. Such results also would provide more
understanding on how warming climate affects alpine seed banks.
Acknowledgments We thank Prof. Carol C. Baskin, Prof. Mary A. Leck and two anonymous reviewers for
critically reading and suggesting numerous improvements on an earlier version of this manuscript. It is a
pleasure to thank Xiao Qun for her help in preparing Table 4 and verifying plant names throughout. We are
indeed thankful to the financial support by NSFC (Grant No.51076108) and the program for Professor of
Eastern Scholar.
Literature Cited
Acharya, S. N. 1989. Germination response of two alpine grasses from the Rocky Mountains of Alberta.
Canadian Journal of Plant Science 69: 1165–1177.
Adzhiev, R., V. Onipchenko & D. Tekeev. 2011. Viability of buried plant seeds from alpine plant
communities (Northwest Caucasus): results of a five year experiment. Zhurnal obshchei biologii 73:
453–458. Abstract in English.
Allen, P. S. & S. E. Meyer. 1998. Ecological aspects of seed dormancy loss. Seed Science Research 8: 183–
192.
Amen, R. D. 1965. Seed dormancy in the alpine rush, Luzula Spicata L. Ecology 46: 361–364.
——— 1966. The extent and role of seed dormancy in alpine plants. Q. Rev. Biol. 41: 271–281.
——— & E. K. Bonde. 1964. Dormancy and germination in alpine Carex from the Colorado front range.
Ecology 45: 881–884.
Arroyo, M. T. K., L. A. Cavieres, C. Castor & A. M. Humaña. 1999. Persistent soil seed bank
and standing vegetation at a high alpine site in the central Chilean Andes. Oecologia 119: 126–
132.
———, ——— & A. M. Humaña. 2004. Experimental evidence of potential for persistent seed bank
formation at a subantarctic alpine site in Tierra del Fuego, Chile. Annals of the Missouri Botanical Garden
91: 357–365.
Baker, H. G. 1972. Seed weight in relation to environmental conditions in California. Ecology 53: 997–
1010.
Bakker, J., P. Poschlod, R. Strykstra, R. Bekker & K. Thompson. 1996. Seed banks and seed dispersal:
important topics in restoration ecology. Acta Botanica Neerlandica 45: 461–490.
Baskin, C. C. & J. M. Baskin. 1998. Seeds: ecology, biogeography, and evolution of dormancy and
germination. Academic Pr.
———, O. Zackrisson & J. M. Baskin. 2002. Role of warm stratification in promoting germination of seeds
of Empetrum hermaphroditum (Empetraceae), a circumboreal species with a stony endocarp. American
Journal of Botany 89: 486–493.
Baskin, J. M. & C. C. Baskin. 2004. A classification system for seed dormancy. Seed Science Research 14:
1–16.
Bekker, R., J. Bakker, U. Grandin, R. Kalamees, P. Milberg, P. Poschlod, K. Thompson & J. Willems.
1998. Seed size, shape and vertical distribution in the soil: indicators of seed longevity. Functional
Ecology 12: 834–842.
Bell, K. L. & L. Bliss. 1980. Plant reproduction in a high arctic environment. Arctic and Alpine Research 12:
1–10.
Bewley, J. D., K. . Bradford, H. W. Hilhorst, & H. Nonogaki 2013. Environmental Regulation of
Dormancy and Germination. (3rd edition), Springer.
Billings, W. 1974. Adaptations and origins of alpine plants. Arctic and Alpine Research 6: 129–142.
——— & L. Bliss. 1959. An alpine snowbank environment and its effects on vegetation, plant development,
and productivity. Ecology 40: 388–397.
——— & H. A. Mooney. 1968. The ecology of arctic and alpine plants. Biological Reviews 43: 481–529.
Blionis, G. J. & D. Vokou. 2005. Reproductive attributes of Campanula populations from Mt. Olympos,
Greece. Plant Ecology 178: 77–88.
Bliss, L. 1958. Seed germination in arctic and alpine species. Arctic 11: 180–188.
Brändel, M. & W. Schütz. 2005. Temperature effects on dormancy levels and germination in temperate forest
sedges (Carex). Plant Ecology 176: 245–261.
Bruun, H. H., R. Lundgren & M. Philipp. 2008. Enhancement of local species richness in tundra by seed
dispersal through guts of muskox and barnacle goose. Oecologia 155: 101–110.
Bu, H., X. Chen, Y. Wang, X. Xu, K. Liu & G. Du. 2007a. Germination time, other plant traits
and phylogeny in an alpine meadow on the eastern Qinghai-Tibet Plateau. Community Ecology
8: 221–227.
———, ———, X. Xu, K. Liu, P. Jia & G. Du. 2007b. Seed mass and germination in an alpine meadow on
the eastern Tsinghai–Tibet plateau. Plant Ecology 191: 127–149.
———, G. Du, X. Chen, X. Xu, K. Liu & S. Wen. 2008. Community-wide germination strategies in an
alpine meadow on the eastern Qinghai-Tibet plateau: phylogenetic and life-history correlates. Plant
Ecology 195: 87–98.
———, G. Z. Du, X. L. Chen, Y. Wang, X. L. Xu & K. Liu. 2009. The evolutionary significance of seed
germinability in an alpine meadow on the eastern Qinghai-Tibet Plateau. Arctic, Antarctic, and Alpine
Research 41: 97–102.
Bullock, J., B. C. Hill, J. Silvertown & M. Sutton. 1995. Gap colonization as a source of grassland
community change: effects of gap size and grazing on the rate and mode of colonization by different
species. Oikos 72: 273–282.
Cain, M. L., B. G. Milligan & A. E. Strand. 2000. Long-distance seed dispersal in plant populations.
American Journal of Botany 87: 1217–1227.
Carasso, V., A. Fusconi, F. R. Hay, S. Dho, B. Gallino & M. Mucciarelli. 2012. A threatened alpine species,
Fritillaria tubiformis subsp moggridgei: Seed morphology and temperature regulation of embryo growth.
Plant Biosystems 146: 74–83.
Cavieres, L. A. 1999. Persistent seed banks: delayed seed germination models and their application to alpine
environments. Revista Chilena De Historia Natural 72: 457–466.
——— & M. T. Arroyo. 2000. Seed germination response to cold stratification period and thermal regime in
Phacelia secunda (Hydrophyllaceae)–altitudinal variation in the Mediterranean Andes of central Chile.
Plant Ecology 149: 1–8.
——— & M. T. K. Arroyo. 2001. Persistent soil seed banks in Phacelia secunda (Hydrophyllaceae):
experimental detection of variation along an altitudinal gradient in the Andes of central Chile (33 degrees
S). Journal of Ecology 89: 31–39.
Celedon-Neghme, C., L. A. San Martin, P. F. Victoriano & L. A. Cavieres. 2008. Legitimate seed dispersal
by lizards in an alpine habitat: The case of Berberis empetrifolia (Berberidaceae) dispersed by Liolaemus
belii (Tropiduridae). Acta oecologica 33: 265–271.
Cerabolini, B., R. M. Ceriani, M. Caccianiga, R. D. Andreis & B. Raimondi. 2003. Seed size, shape and
persistence in soil: a test on Italian flora from Alps to Mediterranean coasts. Seed Science Research 13:
75–85.
Chambers, J. C., J. A. MacMahon & J. H. Haefner. 1991. Seed entrapment in alpine ecosystems: effects of
soil particle size and diaspore morphology. Ecology 72: 1668–1677.
——— & ———. 1994. A day in the life of a seed: movements and fates of seeds and their implications for
natural and managed systems. Annual Review of Ecology and Systematics 25: 263–292.
——— 1995. Disturbance, life history strategies, and seed fates in alpine herbfield communities. American
Journal of Botany 82: 421–433.
——— 2000. Seed movements and seedling fates in disturbed sagebrush steppe ecosystems: implications for
restoration. Ecological Applications 10: 1400–1413.
Chu, C. J., Y. S. Wang, G. Z. Du, F. T. Maestre, Y.-J. Luo & G. Wang. 2007. On the balance
between niche and neutral processes as drivers of community structure along a successional
gradient: insights from alpine and sub-alpine meadow communities. Annals of Botany 100: 807–
812.
Clebsch, E. E. & W. Billings. 1976. Seed germination and vivipary from a latitudinal series of populations of
the arctic-alpine grass Trisetum spicatum. Arctic and Alpine Research 8: 255–262.
Coomes, D. A., M. Rees, P. J. Grubb & L. Turnbull. 2002. Are differences in seed mass among species
important in structuring plant communities? Evidence from analyses of spatial and temporal variation in
dune‐annual populations. Oikos 96: 421–432.
Dainese, M. & T. Sitzia. 2013. Assessing the influence of environmental gradients on seed mass variation in
mountain grasslands using a spatial phylogenetic filtering approach. Perspectives in Plant Ecology,
Evolution and Systematics 15: 12–19.
Danvind, M. & C. Nilsson. 1997. Seed floating ability and distribution of alpine plants along a northern
Swedish river. Journal of Vegetation Science 8: 271–276.
Dar, A. R., Z. Reshi & G. H. Dar. 2009. Germination studies on three critically endangered endemic
angiosperm species of the Kashmir Himalaya, India. Plant Ecology 200: 105–115.
Densmore, R. & J. Zasada. 1983. Seed dispersal and dormancy patterns in northern willows: ecological and
evolutionary significance. Canadian Journal of Botany 61: 3207–3216.
——— 1997. Effect of day length on germination of seeds collected in Alaska. American Journal of Botany
84: 274–274.
Dorne, A. J. 1981. Variation in seed germination inhibition of Chenopodium bonus-henricus in relation to
altitude of plant growth. Canadian Journal of Botany 59: 1893–1901.
Elkington, T. 1971. Biological flora of the British Isles: Dryas Octopetala L. Journal of Ecology 59: 887–
905.
Fenner, M. & K. Thompson. 2005. The ecology of seeds. Cambridge Univ Pr.
Fernandez-Pascual, E., B. Jimenez-Alfaro, A. I. Garcia-Torrico, F. Perez-Garcia & T. E. Diaz. 2012.
Germination ecology of the perennial Centaurium somedanum, a specialist species of mountain springs.
Seed Science Research 22: 199–205.
Finch-Savage, W. E. & G. Leubner-Metzger. 2006. Seed dormancy and the control of germination. New
Physiologist 171: 501–523.
Forbis, T. A. 2003. Seedling demography in an alpine ecosystem. American Journal of Botany 90: 1197–
1206.
——— & P. K. Diggle. 2001. Subnivean embryo development in the alpine herb Caltha leptosepala
(Ranunculaceae). Canadian Journal of Botany 79: 635–642.
Frei, E. S., J. F. Scheepens & J. Stoecklin. 2012. Dispersal and microsite limitation of a rare alpine plant.
Plant Ecology 213: 395–406.
Funes, G., S. Basconcelo, S. Díaz & M. Cabido. 1999. Seed size and shape are good predictors of seed
persistence in soil in temperate mountain grasslands of Argentina. Seed Science Research 9: 341–345.
Garnock‐Jones, P. J. & D. G. Lloyd. 2004. A taxonomic revision of Parahebe (Plantaginaceae) in New
Zealand. New Zealand Journal of Botany 42: 181–232.
Gilbert, B., W. F. Laurance, E. G. Leigh Jr & H. E. Nascimento 2006. Can Neutral Theory Predict the
Responses of Amazonian Tree Communities to Forest Fragmentation?. The American Naturalist 168:
304–317.
Giménez-Benavides, L., A. Escudero & F. Pérez-García. 2005. Seed germination of high mountain
Mediterranean species: altitudinal, interpopulation and interannual variability. Ecological Research 20:
433–444.
Glaser, P. H. 1981. Transport and deposition of leaves and seeds on tundra: a late-glacial analog. Arctic and
Alpine Research 13: 173–182.
Gottfried, M., H. Pauli, K. Reiter & G. Grabherr. 2001. A fine‐scaled predictive model for changes in
species distribution patterns of high mountain plants induced by climate warming. Diversity and
Distributions 5: 241–251.
———, ———, A. Futschik, M. Akhalkatsi, P. Barancok, J. L. Benito Alonso, G. Coldea, J. Dick, B.
Erschbamer, M. R. Fernandez Calzado, G. Kazakis, J. Krajci, P. Larsson, M. Mallaun, O.
Michelsen, D. Moiseev, P. Moiseev, U. Molau, A. Merzouki, L. Nagy, G. Nakhutsrishvili, B.
Pedersen, G. Pelino, M. Puscas, G. Rossi, A. Stanisci, J.-P. Theurillat, M. Tomaselli, L. Villar, P.
Vittoz, I. Vogiatzakis & G. Grabherr. 2012. Continent-wide response of mountain vegetation to climate
change. Nature Clim. Change 2: 111–115.
Graae, B. J., I. G. Alsos & R. Ejrnaes. 2008. The impact of temperature regimes on development, dormancy
breaking and germination of dwarf shrub seeds from arctic, alpine and boreal sites. Plant Ecology 198:
275–284.
Greene, D. & E. Johnson. 1997. Secondary dispersal of tree seeds on snow. Journal of Ecology 85: 329–340.
Güleryüz, G., S. Kırmızı, H. Arslan & F. S. Sakar. 2011. Dormancy and germination in Stachys germanica
L. subsp. bithynica (Boiss.) Bhattacharjee seeds: Effects of short-time moist chilling and plant growth
regulators. Flora-Morphology, Distribution, Functional Ecology of Plants 206: 943–948.
Guo, H., S. J. Mazer & G. Du. 2010. Geographic variation in seed mass within and among nine species of
Pedicularis (Orobanchaceae): effects of elevation, plant size and seed number per fruit. Journal of Ecology
98: 1232–1242.
Haggas, L., R. W. Brown & R. S. Johnston. 1987. Light requirement for seed germination of Payson sedge.
Journal of range management 40: 180–184.
Heide, O. M. & Y. Gauslaa. 1999. Developmental strategies of Koenigia islandica, a high-arctic annual
plant. Ecography 22: 637–642.
Hölzel, N. & A. Otte. 2004. Ecological significance of seed germination characteristics in flood-meadow
species. Flora-Morphology, Distribution, Functional Ecology of Plants 199: 12–24.
Hu, X., T. Li, J. Wang, Y. Wang, C. C. Baskin & J. M. Baskin. 2013. Seed dormancy in four Tibetan
Plateau Vicia species and characterization of physiological changes in response of seeds to environmental
factors. Seed Science Research 23: 133–140.
Hubbell, S. P. 2001. The unified neutral theory of biodiversity and biogeography (MPB-32). Princeton
University Press.
Hughes, L. 2000. Biological consequences of global warming: is the signal already apparent? Trends in
ecology & evolution 15: 56–61.
Jakobsson, A. & O. Eriksson. 2000. A comparative study of seed number, seed size, seedling size and
recruitment in grassland plants. Oikos 88: 494–502.
Jankowska-Blaszczuk, M. & M. Daws. 2007. Impact of red: far red ratios on germination of temperate forest
herbs in relation to shade tolerance, seed mass and persistence in the soil. Functional Ecology 21: 1055–
1062.
Jurado, E. & J. Flores. 2005. Is seed dormancy under environmental control or bound to plant traits? Journal
of Vegetation Science 16: 559–564.
Kaye, T. N. 1997. Seed dormancy in high elevation plants: implications for ecology and restoration. Pp 115–
120. In: T. N. Kaye, A. Liston, R. Love, D. Luoma, R. Meinke, & M. Wilson (eds). Conservation and
management of native Plants and Fungi. Native Plant Society of Oregon, Corvallis.
Kibe, T. & T. Masuzawa. 1994. Seed germination and seedling growth of Carex doenitzii growing on alpine
zone of Mt. Fuji. Journal of Plant Research 107: 23–27.
Klug-Pümpel, B. & G. Scharfetter-Lehrl. 2008. Soil diaspore reserves above the timberline in the Austrian
Alps. Flora-Morphology, Distribution, Functional Ecology of Plants 203: 292–303.
Komatsu, T., T. Itino & S. Ueda. 2014. First report of seed dispersal by ants in Dicentra peregrina
(Papaveraceae), an alpine plant in the Japanese Alps. Entomological Science. doi:10.1111/ens.12110.
Körner, C. 1999. Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, New
York.
——— 2003. Alpine plant life: functional plant ecology of high mountain ecosystems. Springer Verlag
Larsen, H. & K. C. Burns. 2012. Seed dispersal effectiveness increases with body size in New Zealand
alpine scree weta (Deinacrida connectens). Austral Ecology 37: 800–806.
Leishman, M. & M. Westoby. 1998. Seed size and shape are not related to persistence in soil in Australia in
the same way as in Britain. Functional Ecology 12: 480–485.
———, M. Westoby & E. Jurado. 1995. Correlates of seed size variation: a comparison among five
temperate floras. Journal of Ecology 83: 517–530.
———, I. J. Wright, A. T. Moles & Westoby, M. 2000 The evolutionary ecology of seed size. pp 31–57 in
Fenner, M. (Ed) Seeds: the ecology of regeneration in plant communities, CAB International.
——— & B. R. Murray. 2001. The relationship between seed size and abundance in plant communities:
model predictions and observed patterns. Oikos 94: 151–161.
Liebst, B. & J. Schneller. 2008. Seed dormancy and germination behaviour in two Euphrasia species
(Orobanchaceae) occurring in the Swiss Alps. Botanical Journal of the Linnean Society 156: 649–656.
Lindgren, Å., O. Eriksson & J. Moen. 2007. The impact of disturbance and seed availability on germination
of alpine vegetation in the Scandinavian mountains. Arctic, Antarctic, and Alpine Research 39: 449–454. Liu,
K., J. M. Baskin, C. C. Baskin, H. Bu, M. Liu, W. Liu & G. Du. 2011. Effect of storage conditions on
germination of seeds of 489 species from high elevation grasslands of the eastern Tibet Plateau and some
implications for climate change. American Journal of Botany 98: 12–19.
———, ———, ———, ———, G. Du & M. Ma. 2013. Effect of diurnal fluctuating versus constant
temperatures on germination of 445 species from the Eastern Tibet Plateau. PloS one 8: e69364.
Lorite, J., A. M. Ruiz-girel & J. Castro. 2007. Patterns of seed germination in Mediterranean mountains:
study on 37 endemic or rare species from Sierra Nevada, SE Spain. Candollea 62(1): 1–12.
Lucas-Borja, M. E., T. F. Fonseca, J. L. Lousada, P. Silva-Santos, E. Martinez Garcia & M. Andres
Abellan. 2012. Natural regeneration of Spanish black pine Pinus nigra Arn. ssp salzmannii (Dunal)
Franco at contrasting altitudes in a Mediterranean mountain area. Ecological Research 27: 913–921.
Lütz, C. 2011. Plants in Alpine Regions: Cell Physiology of Adaption and Survival Strategies. Springer.
Ma, M., X. Zhou & G. Du. 2010a. Role of soil seed bank along a disturbance gradient in an alpine meadow
on the Tibet plateau. Flora-Morphology, Distribution, Functional Ecology of Plants 205: 128–134.
———, ———, G. Wang, Z. Ma & G. Du. 2010b. Seasonal dynamics in alpine meadow seed banksalong
an altitudinal gradient on the Tibetan Plateau. Plant and soil 336: 291–302.
———, ——— & G. Du. 2011. Soil seed bank dynamics in alpine wetland succession on the Tibetan
Plateau. Plant and soil 346: 1–10.
———, ———, W. Qi, K. Liu, P. Jia & G. Du. 2013. Seasonal dynamics of the plant community and soil
seed bank along a successional gradient in a subalpine meadow on the Tibetan Plateau. PloS one 8:
e80220.
Marcante, S., A. Sierra‐Almeida, J. P. Spindelböck, B. Erschbamer & G. Neuner. 2012. Frost as a
limiting factor for recruitment and establishment of early development stages in an alpine glacier
foreland? Journal of Vegetation Science 23: 858–868.
Marchand, P. J. & D. A. Roach. 1980. Reproductive strategies of pioneering alpine species: seed production,
dispersal, and germination. Arctic and Alpine Research 12: 137–146.
Mariko, S., H. Koizumi, J.-I. Suzuki & A. Furukawa. 1993. Altitudinal variations in germination and
growth responses of Reynoutria japonica populations on Mt Fuji to a controlled thermal environment.
Ecological Research 8: 27–34.
Matlack, G. 1989. Secondary dispersal of seed across snow in Betula lenta, a gap-colonizing tree species. The
Journal of Ecology 77: 853–869.
Mazer, S. J. 1989. Ecological, taxonomic and life history correlates of seed mass among Indiana dune
angiosperms. Ecological Monograph 59: 153–175.
McDonough, W. T. 1970. Germination of 21 species collected from a high-elevation rangeland in Utah.
American Midland Naturalist 84: 551–554.
McGill, B. J. 2003. A test of the unified neutral theory of biodiversity. Nature 422: 881–885.
McGraw, J., M. Vavrek & C. Bennington. 1991. Ecological genetic variation in seed banks I. Establishment
of a time transect. The Journal of Ecology 79: 617–625.
——— & M. C. Vavrek 1989. The Role of Buried Viable Seeds in Arctic and Alpine plant communities in
Leck, M.A., Parker, V.T. and Simpson, R.L. (Eds) Ecology of soil seed banks, Academic Press.
Meyer, S., S. Kitchen & S. Carlson. 1995. Seed germination timing patterns in intermountain Penstemon
(Scrophulariaceae). American Journal of Botany 82: 377–389.
Meyer, S. E. & S. B. Monsen. 1991. Habitat-correlated variation in mountain big sagebrush (Artemisia
tridentata ssp. vaseyana) seed germination patterns. Ecology 72: 739–742.
——— & S. G. Kitchen. 1994a. Life history variation in blue flax (Linum perenne: Linaceae): seed
germination phenology. American Journal of Botany 81: 528–535.
——— & ———. 1994b. Habitat-correlated variation in seed germination response to chilling in Penstemon
Section Glabri (Scrophulariaceae). American Midland Naturalist 132: 349–365.
Milberg, P., L. Andersson & K. Thompson. 2000. Large-seeded spices are less dependent on light for
germination than small-seeded ones. Seed Science Research 10: 99–104.
Molau, U. & E. L. Larsson. 2000. Seed rain and seed bank along an alpine altitudinal gradient in Swedish
Lapland. Canadian Journal of Botany 78: 728–747.
Moles, A. T., D. W. Hodson & C. J. Webb. 2000. Seed size and shape and persistence in the soil in the New
Zealand flora. Oikos 89: 541–545.
——— & M. Westoby. 2004. Seedling survival and seed size: a synthesis of the literature. Journal of Ecology
92: 372–383.
Mondoni, A., M. I. Daws, J. Belotti & G. Rossi. 2009. Germination requirements of the alpine endemic
Silene elisabethae Jan: effects of cold stratification, light and GA(3). Seed Science and technology 37: 79–
87.
———, G. Rossi, S. Orsenigo & R. J. Probert. 2012. Climate warming could shift the timing of seed
germination in alpine plants. Annals of Botany 110: 155–164.
Mooney, H. A. & W. Billings. 1961. Comparative physiological ecology of arctic and alpine populations of
Oxyria digyna. Ecological Monographs 31: 1–29.
Muñoz, A. A. & M. T. K. Arroyo. 2002. Postdispersal seed predation on Sisyrinchium arenarium
(Iridaceae) at two elevations in the central Chilean Andes. Arctic, Antarctic, and Alpine Research
34: 178–184.
——— & L. A. Cavieres. 2006. A multi-species assessment of post-dispersal seed predation in the central
Chilean Andes. Annals of Botany 98: 193–201.
Nishitani, S. & T. Masuzawa. 1996. Germination characteristics of two species of Polygonum in relation to
their altitudinal distribution on Mt. Fuji, Japan. Arctic and Alpine Research 28: 104–110.
Norden, N., M. I. Daws, C. Antoine, M. A. Gonzalez, N. C. Garwood & J. Chave. 2009. The relationship
between seed mass and mean time to germination for 1037 tree species across five tropical forests.
Functional Ecology 23: 203–210.
Novak, J., C. Wawrosch, C. Schmiderer, C. M. Franz & B. Kopp. 2011. Germination responses of
Peucedanum ostruthium (Apiaceae) to genotype, light, temperature and gibberellic acid. Seed Science
and technology 39: 552–558.
Ozinga, W. A., R. M. Bekker, J. H. J. Schaminee & J. M. Van Groenendael. 2004. Dispersal potential in
plant communities depends on environmental conditions. Journal of Ecology 92: 767–777.
Parolo, G. & G. Rossi. 2008. Upward migration of vascular plants following a climate warming trend in the
Alps. Basic and Applied Ecology 9: 100–107.
Pauli, H., M. Gottfried & G. Grabherr. 1996. Effects of climate change on mountain ecosystems–upward
shifting of alpine plants. World Resource Review 8: 382–390.
———, ——— & ——— (eds). 2001. High summits of the Alps in a changing climate. Kluwer Academic/
Plenum Publ, New York.
Peco, B., J. Traba, C. Levassor, A. M. Sánchez & F. M. Azcárate. 2003. Seed size, shape and persistence in
dry Mediterranean grass and scrublands. Seed Science Research 13: 87–95.
Pluess, A., W. Schütz & J. Stöcklin. 2005. Seed weight increases with altitude in the Swiss Alps between
related species but not among populations of individual species. Oecologia 144: 55–61.
Pons, T. L.& M. Fenner 2000 Seed responses to light. pp 237–260 in Fenner, M. (Ed) Seeds: the ecology of
regeneration in plant communities, CABI
Pufal, G., K. G. Ryan & P. Garnock-Jones. 2010. Hygrochastic capsule dehiscence in New Zealand alpine
veronica (Plantaginaceae). American Journal of Botany 97: 1413–1423.
Rees, M. & M. J. Long. 1992. Germination biology and the ecology of annual plants. American Naturalist
139: 484–508.
——— 1996. Evolutionary ecology of seed dormancy and seed size. Philosophical Transactions of the Royal
Society of London. Series B: Biological Sciences 351: 1299–1308.
Reynolds, D. N. 1984. Alpine annual plants: phenology, germination, photosynthesis, and growth of three
Rocky Mountain species. Ecology 65: 759–766.
Royal Botanic Gardens Kew Seed Information Database (SID). Seed Information Database (SID). Version 7.1.
Available from: http://data.kew.org/sid/ (March 2014).
Sayers, R. L. & R. T. Ward. 1966. Germination responses in alpine species. Botanical Gazette
127: 11–16.
Scherff, E., C. Galen & M. Stanton. 1994. Seed dispersal, seedling survival and habitat affinity in
a snowbed plant: limits to the distribution of the snow buttercup, Ranunculus adoneus. Oikos
69: 405–413.
Schütz, W. & G. Rave. 1999. The effect of cold stratification and light on the seed germination of temperate
sedges (Carex) from various habitats and implications for regenerative strategies. Plant Ecology 144:
215–230.
——— 2002. Dormancy characteristics and germination timing in two alpine Carex species. Basic and
Applied Ecology 3: 125–134.
Schwienbacher, E., S. Marcante & B. Erschbamer. 2010. Alpine species seed longevity in the soil in relation
to seed size and shape-A 5-year burial experiment in the Central Alps. Flora-Morphology, Distribution,
Functional Ecology of Plants 205: 19–25.
———, J. A. Navarro-Cano, G. Neuner & B. Erschbamer. 2011. Seed dormancy in alpine species. Flora-
Morphology, Distribution, Functional Ecology of Plants 206: 845–856.
Shimono, Y. & G. Kudo. 2003. Intraspecific variations in seedling emergence and survival of Potentilla
matsumurae (Rosaceae) between alpine fellfield and snowbed habitats. Annals of Botany 91: 21–
29.
——— & ———. 2005. Comparisons of germination traits of alpine plants between fellfield and snowbed
habitats. Ecological Research 20: 189–197.
Sommerville, K. D., A. J. Martyn & C. A. Offord. 2013. Can seed characteristics or species distribution be
used to predict the stratification requirements of herbs in the Australian Alps? Botanical Journal of the
Linnean Society 172: 187–204.
Stinson, K. A. 2004. Natural selection favors rapid reproductive phenology in Potentilla pulcherrima
(Rosaceae) at opposite ends of a subalpine snowmelt gradient. American Journal of Botany 91: 531–539.
Stöcklin, J. & E. Bäumler. 1996. Seed rain, seedling establishment and clonal growth strategies on a glacier
foreland. Journal of Vegetation Science 7: 45–56.
Tackenberg, O., P. Poschlod & S. Bonn. 2003. Assessment of wind dispersal potential in plant species.
Ecological Monographs 73: 191–205.
——— & J. Stöcklin. 2008. Wind dispersal of alpine plant species: a comparison with lowland species.
Journal of Vegetation Science 19: 109–118.
Takahashi, K. & Y. Miyajima. 2010. Effects of roads on alpine and subalpine plant species distribution along
an altitudinal gradient on Mount Norikura, central Japan. Journal of Plant Research 123: 741–749.
Thompson, K. 1987. Seeds and seed banks. New Phytologist 106: 23–34.
———, S. Band & J. Hodgson. 1993. Seed size and shape predict persistence in soil. Functional Ecology 7:
236–241.
———, J. P. Bakker & R.M. Bekker. 1997. The soil seed banks of North West Europe: methodology,
density and longevity. Cambridge Univ Pr.
——— 2000 The functional ecology of soil seed banks. pp 215–235 in Fenner, M. (Ed) Seeds: the ecology of
regeneration in plant communities, CABI
———, A. Jalili, J. G. Hodgson, B. Hamzeh’ee, Y. Asri, S. Shaw, A. Shirvany, S. Yazdani, M.
Khoshnevis & F. Zarrinkamar. 2001. Seed size, shape and persistence in the soil in an Iranian flora.
Seed Science Research 11: 345–356.
———, R. M. Ceriani, J. P. Bakker & R. M. Bekker. 2003. Are seed dormancy and persistence in soil
related? Seed Science Research 13: 97–100.
Van der Pijl, L. 1982. Principles of seed dispersal in higher plants. Principles of seed dispersal in higher
plants.
Vera, M. 1997. Effects of altitude and seed size on germination and seedling survival of heathland plants in
north Spain. Plant Ecology 133: 101–106.
Vleeshouwers, L., H. Bouwmeester & C. Karssen. 1995. Redefining seed dormancy: an attempt to integrate
physiology and ecology. Journal of Ecology 83: 1031–1037.
Wagner, I. & A. M. Simons. 2008. Intraspecific divergence in seed germination traits between high- and low-
latitude populations of the arctic-alpine annual Koenigia islandica. Arctic Antarctic and Alpine Research
40: 233–239.
——— & ———. 2009. Divergence in germination traits among arctic and alpine populations of Koenigia
islandica: light requirements. Plant Ecology 204: 145–153.
Wagner, J. & E. Mitterhofer. 1998. Phenology, seed development, and reproductive success of an
alpine population of Gentianella germanica in climatically varying years. Botanica Acta 111: 159–
166.
Walther, G. R., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. C. Beebee, J. M. Fromentin, O.
Hoegh-Guldberg & F. Bairlein. 2002. Ecological responses to recent climate change. Nature 416: 389–
395.
———, S. Beißner & C. A. Burga. 2009. Trends in the upward shift of alpine plants. Journal of Vegetation
Science 16: 541–548.
Wang, B., G. Wang & J. Chen. 2012. Scatter-hoarding rodents use different foraging strategies for seeds
from different plant species. Plant Ecology 213: 1329–1336.
Ware, C., D. M. Bergstrom, E. Muller & I. G. Alsos. 2012. Humans introduce viable seeds to the Arctic on
footwear. Biological Invasions 14: 567–577.
Weiblen, G. D. & J. D. Thomson. 1995. Seed dispersal in Erythronium grandiflorum (Liliaceae). Oecologia
102: 211–219.
Welling, P. & K. Laine. 2000. Characteristics of the seedling flora in alpine vegetation, subarctic Finland, I.
Seedling densities in 15 plant communities. Helsinki: Societas Biologica Fennica 37: 69–76.
———, A. Tolvanen& K. Laine. 2004. The alpine soil seed bank in relation to field seedlings and standing
vegetation in subarctic Finland. Arctic, Antarctic, and Alpine Research 36: 229–238.
Whinam, J.& N. Chilcott. 1999. Impacts of trampling on alpine environments in central tasmania. Journal of
Environmental Management 12: 205–220.
Williams, R. 1987. Patterns of air temperature and accumulation of snow in subalpine heathlands and
grasslands on the Bogong High Plains, Victoria. Australian journal of ecology 12: 153–163.
Willson, M. F., B. Rice & M. Westoby. 1990. Seed dispersal spectra: a comparison of temperate plant
communities. Journal of Vegetation Science 1: 547–562.
Wu, G.-L., G.-Z. Du & Z.-H. Shi. 2013. Germination strategies of 20 alpine species with varying seed mass
and light availability. Australian Journal of Botany 61: 404–411.
Young, L. M., D. Kelly & X. J. Nelson. 2012. Alpine flora may depend on declining frugivorous parrot for
seed dispersal. Biological Conservation 147: 133–142.
Xu, J., W. Li, C. Zhang, W. Liu & G. Du. 2014. Variation in seed germination of 134 common species on the
Eastern Tibetan plateau: phylogenetic, life history and environmental correlates. Plos one 9: e98601. Yu, S.,
M. Sternberg, P. Kutiel & H. Chen. 2007. Seed mass, shape, and persistence in the soil seed bank of
Israeli coastal sand dune flora. Evolutionary Ecology Research 9: 325–340.
Yu, X., C. Xu, F. Wang, Z. Shang & R. Long. 2012. Recovery and germinability of seeds ingested by yaks
and Tibetan sheep could have important effects on the population dynamics of alpine meadow plants on
the Qinghai-Tibetan Plateau. Rangeland Journal 34: 249–255.
Zhang, H., B. Gilbert, X. Zhang & S. Zhou. 2012. Community assembly along a successional gradient in
sub-alpine meadows of the Qinghai-Tibetan Plateau, China. Oikos 122: 952–960.
Zhang, S. T., G. Z. Du & J. K. Chen. 2004. Seed size in relation to phylogeny, growth form and longevity in
a subalpine meadow on the East of the Tibetan plateau, China. Folia Geobotanica 39: 129–142.
Zhao, L. P., G. L. Wu & J. M. Cheng. 2011. Seed mass and shape are related to persistence in a sandy soil in
northern China. Seed Science Research 21: 47–53.

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Bot. Rev.

Towards an Understanding of Factors Controlling Seed

Ganesh K. Jaganathan1,3 & Sarah E. Dalrymple2 &

Keywords Alpine tundra . Climate change . Dormancy. Germination . Phylogeny. Seed

The ecological significance of seeds in establishing plant communities has been

Definitions and Terms

Achillea moschata Asteraceae 0.21 Short-term Persistence PD

*Classified as transient by Cerabolini et al. (2003)

Species Key results References

Species Key results References

the species persist in soil until spring

Species Key results References

taisetsuensis, Diapensia lapponica exception of D. lapponica, V.

Temperature Requirement for Germination

in autumn this temperature is rarely - if ever - met. After overwintering, cold-wet

moderate temperatures) at 10 °C. Similarly, in the case of Phacelia secunda, freshly

Light is an important environmental factor stimulating germination in many seeds

Factors Affecting Seed Persistence

Seed Size and Persistence

Table 3 Distance seeds moved by wind

Species Distance Reference

Ranunculus adoneus 30 cm Scherff et al. (1994)

Dispersal vs. Persistence

Seed size (mg) Number of species

0–3 886 (87.6 %)

colonized tundra vegetation by dispersing seeds with differing phenotypes, some of

Conclusions/Future Research Needs

Our ecological understanding of seed persistence in alpine ecosystems is still in

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