INTRODUCTION
Addressing the impact of global warming on plants requires an
understanding of multiple traits across plant life stages, not only
within but also across generations. Warming, as associated with climate
change, has a strong effect on phenotypic traits throughout a plant’s
life cycle. Warmer temperatures generally lead to increased biomass and
vegetative growth (Debouk, de Bello, & Sebastià, 2015; King, Pregitzer,
& Zak, 1999; Lin, Xia, & Wan, 2010; Walker et al., 2006), reduced
flower numbers and seed production (Hedhly, Hormaza, & Herrero, 2009;
Liu, Mu, Niklas, Li, & Sun, 2012), increased mortality at both seedling
and adult stages (Allen et al., 2010; Hovenden et al., 2008; Milbau,
Vandeplas, Kockelbergh, & Nijs, 2017), delays and decreases in seedling
emergence (Cochrane, Hoyle, Yates, Wood, & Nicotra, 2015), and
potentially can lead to local extirpation of the species (Panetta,
Stanton, & Harte, 2018). Phenology, the timing of biological events –
e.g. bud burst, flowering, seed set, and senescence – is thought to be
the characteristic that is most sensitive to warming and hence, most
observations of responses to climate change have focused on shifts in
phenology (Arft et al., 1999; Cadman, Toorop, Hilhorst, & Finch-Savage,
2006; Cleland, Chuine, Menzel, Mooney, & Schwartz, 2007; Farnsworth,
Nunez-Farfan, Careaga, & Bazzaz, 1995; Jin et al., 2011; Körner &
Basler, 2010; Menzel et al., 2006; Moore & Lauenroth, 2017; Munson &
Sher, 2015; Peñuelas & Filella, 2001; Rathcke & Lacey, 1985; Root et
al., 2003; Sherry et al., 2007; Walther et al., 2002).
Warming responses of vegetative growth, reproductive output and
phenological traits (including senescence) should not, however, be
viewed in isolation (Hoffmann & Sgrò, 2011; Leblans et al., 2017;
Merilä & Hendry, 2014; Nicotra et al., 2010). Rather, variation in
trait values and timing of phenological events determines subsequent
interactions of the individual with the environment and because of this
co-dependence, the responses to environmental change are likely to be
quite complex. For example, germination timing (spring versus autumn)
determines the seasonal conditions and duration of seedling exposure as
well as the conditions in which subsequent life stages occur.
Accordingly, germination timing determines conditions at flowering time,
reproductive period and lifespan in annuals (Donohue, 2009; Lu, Tan,
Baskin, & Baskin, 2016). Time to flowering, likewise, could determine
the season of seed maturity with implications for germination timing,
and the germination timing could in turn determine whether the offspring
will become annual or biennial (Galloway, 2005; Galloway & Etterson,
2007). Thus, a shift in the timing of one phenological event can have
cascading effects for the subsequent life events. However, these shifts
do not necessarily all occur in concert, for example, early flowering in
response to warming is not always followed by a change in timing of
cessation of flowering and thus may result in the expansion or
contraction of the flowering period (CaraDonna, Iler, & Inouye, 2014).
Warming effects may also be highly species- or even population-specific.
For example, prairie species that have early-flowering (spring to
mid-summer) start to flower even earlier, and conversely, late-flowering
species (mid-summer to autumn), delay their flowering when exposed to
warming treatments (Dunnell & Travers, 2011; Sherry et al., 2007). In
the sub-arctic herb Cerastium fontanum, plants from warmer
microsites (populations) flower earlier than those from colder
microsites but when grown in much warmer common gardens, plants from
warmer microsites start to flower later than plants originating from
colder microsites (Valdés, Marteinsdóttir, & Ehrlén, 2019). In the
alpine herb Aciphylla glacialis, seedlings growing under an open
top chamber exhibit higher mortality (but surviving individuals grow
faster) than those under ambient conditions (Geange, Holloway-Phillips,
Briceño, & Nicotra, 2020), regardless of the population source
(Briceño, Harris-Pascal, Nicotra, Williams, & Ball, 2014). Species
response to warming may also be dictated by functional traits. Between
geographically co-occurring species, the seedlings of fast-growingBanksia coccinea, characterized by higher SLA (specific leaf
area) and leaf growth rate, can maintain growth at high temperatures
better than its slow-growing congeneric B. baxteri (Cochrane,
Hoyle, et al., 2015). Within a plant’s life cycle, response to elevated
temperatures can also be trait-specific. For example, inArabidopsis thaliana warming advances flowering time, accelerates
vegetative development and fruit production but not plant mortality
(Springate & Kover, 2014). So far, the studies on plant responses to
climate change often focus only on particular suites of traits (e.g.
leaf traits or flowering phenology) and only at a certain life stage
(mostly adult reproductive), which may lead to incomplete assessments
and failure to predict the cascading effects of warming on species’
persistence, and thus community composition and ecosystem functions and
services.
While research on the adaptive capacity of plants under future climate
is increasing, we still lack understanding of plant plasticity and their
capacity to evolve when challenged by new environmental conditions,
especially for germination and the seedling stage (Parmesan & Hanley,
2015). Studies across ontogeny that span whole life events, and multiple
generations, are also lacking. Maternal conditions may have carry-over
effects across generations and could determine the life history of the
progeny (Donohue, 1998; Donohue, 2009). When these maternal effects
increase offspring fitness, this trans-generational plasticity may be
adaptive (Galloway, 2001a, 2001b, 2005; Galloway & Etterson, 2007;
Herman & Sultan, 2011). For example, warmer temperatures during seed
development generally reduce the degree of primary seed dormancy
(Bernareggi, Carbognani, Mondoni, & Petraglia, 2016; Gutterman, 2000;
Hoyle, Steadman, Daws, & Adkins, 2008; Huang, Footitt, Tang, &
Finch-Savage, 2018), enabling individuals to start growing and to reach
reproductive stage earlier in the season and thus have a longer duration
for seed production and potentially produce more seeds (Donohue, de
Casas, Burghardt, Kovach, & Willis, 2010; Roach & Wulff, 1987).
Climate induced variation in seed dormancy status, in turn, may play
shift timing of germination or variance therein, providing a buffer
against disturbances that may be a bet-hedging strategy. Changes in
dormancy may also affect seedling growth rate and establishment
(Satyanti, Guja, & Nicotra, 2019), or physiological traits such as
water use efficiency, reproductive phenology and senescence (Kimball,
Angert, Huxman, & Venable, 2010, 2011). Understanding the extent to
which germination strategy, particularly the degree of dormancy and how
it is lost over time, could change with warming and whether maternal
temperature interacts with offspring germination requirements to affect
germination success will be valuable for predicting species persistence
in the face of a changing climate.
Alpine regions are recognized as one of the most vulnerable ecosystems
under warming climates – impacts are forecast to be pronounced and
detectable earlier than in other biomes (Grabherr, Gottfried, & Pauli,
2010). Alpine plants that are adapted to low temperature and a short
growing season are particularly responsive to warming (Anadon-Rosell et
al., 2014; Arft et al., 1999; Bjorkman, Elmendorf, Beamish, Vellend, &
Henry, 2015; Cao et al., 2016; Geange et al., 2017; Geange et al., 2020;
Kudernatsch, Fischer, Bernhardt-Römermann, & Abs, 2008; Kudo & Suzuki,
2003; Oberbauer et al., 2013). Perhaps paradoxically, seeds of alpine
plants generally require relatively high soil temperature to trigger
germination (Hoyle et al., 2013; Schütz, 2000; Schütz & Milberg, 1997)
and hence, warming could have a positive effect on recruitment via seed.
In strongly seasonal and unpredictable environments, plants often evolve
specific seed dormancy that leads to divergence in germination strategy
(Hoyle et al., 2015; Satyanti et al., 2019; Willis et al., 2014).
Variation of germination strategy across alpine species is common (Hoyle
et al., 2015; Körner, 2003; Satyanti, 2018), but more strikingly,
intraspecific variation in germination strategy with environment and
elevation is also documented (e.g. Hoyle et al., 2015; Satyanti et al.,
2019; Vidigal et al., 2016; Wagner & Simons, 2009). Such variation in
germination strategy may help to facilitate the regeneration and
survival of plants in short growing seasons, and highly variable
environments, as reported from (Satyanti et al., 2019).
Oreomyrrhis eriopoda (Apiaceae) is a native rosette-forming herb
from the Australian Alps that exhibits has four germination strategies:
immediate, staggered, postponed, and postponed-deep (Satyanti et al.,
2019). Populations with an immediate strategy produce non-dormant seed
and thus “autumn seedlings”. Populations that produce dormant seeds
(postponed strategy) produce “spring seedlings”. Populations
categorised as postponed-deep germinate (usually in spring) after
exposure to multiple cycles of winter conditions. Populations that
exhibit the staggered strategy produce both non-dormant and postponed
seeds in the same accession and thus both “autumn” and “spring
seedlings” occur (e.g. Hoyle et al., 2015; Satyanti et al., 2019). The
among-population variation in germination strategy in O. eriopodaleads to substantial differentiation of seedling growth among and within
populations (in staggered populations autumn seedlings grow faster than
spring seedlings) (Satyanti et al., 2019).
So far, we know little about the extent of intraspecific germination
strategy variation in plant responses to warming. Particularly, to what
extent plants are able to increase growth rate and to adjust phenology
to maximise reproductive capacity and fitness. Using O. eriopoda ,
we aim to understand the effect of warming across all life stages
(vegetative growth, reproductive output, phenology and the germination
traits of the seed produced), and to explore whether populations of
different germination strategies show variation in those warming
responses in the current and subsequent generation. We hypothesised
that: (i) Warming would interact with germination strategies and overall
would enhance growth at the cost of flower and fruit production, and
likely with an increase in plant mortality; (ii) Plant responses to soil
temperature would depend on germination strategy; (iii) Germination
strategy of the offspring will be affected by warming of the maternal
environment.