The strategies of plants with advanced vs. delayed germination
Plants that germinated earlier in spring also had prolonged vegetative
growth and life cycle, even longer than those germinating in late
spring, but they had similar or lower performance in total mass and
reproduction as late-spring germinants. This was probably due to the
unfavorable environments in early and middle spring. Early germinants
may experience a higher risk of mortality, due to seasonal hazards such
as pathogens, predation, desiccation (Donohue, 2014; Jones & Sharitz,
1989; Mercer et al., 2011; Rice, 1990), in spite of the importance of
early emergence and establishment (Miller et al., 1994). Especially in
this study, although the season between April and May is in spring in
northeast of China, the climate then is usually chilling, with
unpredictable precipitation and frequent drought mortality, similar to
the situation of other studies (Weekley et al., 2007), when early
germination becomes a ‘high-risk high-gain’ strategy (ten Brink et al.,
2020). Spring-germinants had smaller leaves and more-vertical petioles,
which is a “shade avoidance” response (Wang et al., 2017; Wang &
Zhou, 2021), indicating they experienced stronger intraspecific
competition than those germinated in late spring and summer. Limited
resources may decelerate the growth of early seedlings, reducing the
differences between them and late seedlings (Verdu´ & Traveset, 2005).
Therefore, spring-germinants did not outperform late-spring germinants,
although their longer growing period allows a longer vegetative and
reproductive growth than the latter. The disadvantage of advanced
germination may partially explain why seed germination can spread over
several years via dormancy, to reduce the risk of failure within growth
seasons of fluctuating abiotic conditions (ten Brink et al., 2020). But
it is worth noting that in spite of the possible damage of early drought
stress and reduction in growth rate, plants with advanced germination
were still able to survive and perform better than those germinated too
late, by virtue of the benefits from longer growing period and greater
plant size, substantial seedling height and greater number of leaves
(Bianchi et al., 2019).
By contrast, plants germinated later in summer had accelerated growth,
and accumulated total biomass to the same level as spring germinants
within much shorter time. They shortened vegetative growth, to initiate
reproductive growth earlier, in order to complete their life cycles
before the climate became stressful or lethal. This may be achieved by
perceiving signals of shorter daylight, indicative of inadequate time
for completing life cycles. Finally, they also had increased
reproductive mass and allocation, compared to earlier germinants,
consistent with other results (Hartzler et al., 2004; Wu & Owen, 2014).
This to a large extent be due to the benefits of their increased
investment to leaf mass and allocation, and their responses of many
morphological traits, such as a greater number of leaves and
less-vertical petioles, lower stem mass and allocation, shorter and
thinner stems and roots, compared to spring germinants. If relative
plant size is associated with resource overlap, later germination could
promote resource partitioning (Leverett et al., 2018) or higher
efficiencies of resource allocation (Wu & Owen, 2014). Plants that
emerged in spring had increasing stem mass and allocation and decreasing
leaf mass and allocation as they grew larger, while those emerged in
summer had deceasing stem mass allocation over time, suggesting the
plants with delayed germination may give the priority to the growth of
leaves and reproduction, avoiding extensive stem growth, to ensure the
completion of an entire life cycle.
Plants emerged in late summer adopted the same strategy of reducing stem
growth and enhancing leaf mass and allocation. Delaying germination
further into late summer also led to a faster growth, but reduced total
mass and reproduction due to insufficient time for completing a life
cycle at the end of growth season. The delay of germination is costly to
fitness (Metcalf et al., 2003; Tuljapurkar, 1990), especially when it
led to incomplete life cycle. Plants germinated in late summer produced
flowers, but did not have time for fruit shaping and ripening. In
addition, delaying germination into late summer also led to decreased
mass allocated to roots and stems, but the highest leaf mass and
allocation of all, suggesting that trade-off not only occurs between
vegetative growth and reproductive growth, but also between different
vegetative organs. In response to the seasonal changes, late-summer
germinants also produced more and smaller leaves with shorter petioles
than other germinants. This may because the growth rate of individual
leaves or analogous repetitively generated organs is relatively fixed,
and it cannot be easily altered by environmental conditions, so that
plants can only increase the investment to leaf population by producing
a greater number of leaves.
Moreover, the increased allocation to leaves was at the cost of reduced
stem allocation, rather than root allocation. It suggested that the
canalization of root mass allocation is more important than stem
allocation for maintaining plant growth and functions. This was
supported by the attenuated effects of germination timing on the length
of main root and lateral roots over time, and plants with delayed
germination (GT3 and GT4) even had more lateral roots at the first or
second stage. And evidence also came from the more-stabilized root mass
allocation over different densities, compared to the responses of shoot
or above-ground modular mass allocation to density, as plants grew (Wang
et al., 2017, 2021). It demonstrated that A. theophrasti can
respond to germination timing though the plasticity in a number of
traits, and there were some differences in responses of allocation and
morphological traits. Firstly, plastic responses of morphological traits
may precede responses of biomass allocation (Wang et al., 2017).
Secondly, in response to delayed germination, they may first increase
root morphological traits such as lateral root numbers, then increase
the lengths of main root and lateral roots, in order to keep root mass
allocation stable, before enhancing leaf morphological traits such as
leaf size, leaf number, petiole angle and length, to increase the leaf
mass allocation, ultimately for canalizing reproductive efforts. In
other words, plasticity of root traits may occur before those of leaf
traits, in response to germination timing. It suggested root plasticity
plays a predominant role in plant response to environments, probably
orientating, regulating and determining the responses of above-ground
organs; or alternatively, root plasticity provides a basic premise for
growth and adjustments of other organs due to their important supporting
functions. Consequently, in face of any environmental changes, it is
more crucial for plants to maintain root mass allocation, whereas
investments put into stem or leaves can always be deliberated and
balanced depending on specific situations. When competition for light is
more emergent, the additional stem elongation can be at the cost of leaf
growth (Wang et al., 2017); if growth time becomes more limited, leaf
growth prevails over stem elongation, which can be sacrificed. Of
course, plants will always adjust or canalize vegetative organs in order
to achieve stable reproductive efforts.
In spite of the conspicuous disadvantages in comparison with late-spring
germinants, plants with advanced and delayed germination still can use
different strategies to reduce the adverse effects of germination
timing. Natural selection may favour germination at different times or a
mixed, bet-hedging strategy (Silvertown, 1988; Zhou et al., 2005).
Natural selection for competitive traits include large plant size (e. g.
height, total biomass) and long life span; conversely, small size, high
relative growth rate and reproductive allocation indicate ruderal
selection (Grime, 1979; Hodgson, 1999). Plants germinated earlier have
prolonged vegetative growth and life cycle, and delayed reproduction;
plants with delayed germination have compressed vegetative growth,
advanced reproduction, and shortened life cycles. Therefore, plants that
germinated in spring and late spring tended to adopt the strategies of
competitors (C), while those with delayed germination tended towards
ruderal strategies (R) (Zhou et al., 2005). The coexistence of multiple
germination strategies may result from the density dependence of plant
growth (Metcalf et al., 2015; Poethke et al., 2016), since plants were
growing in relatively dense population in this study. The phenotypic
plasticity in growth strategy may compete with bet hedging as a way to
deal with environmental variation (Donaldson-Matasci et al., 2013; Xue
& Leibler, 2018), if cues allow some aspects of the environment to be
measured or predicted (ten Brink et al., 2020). For future work, it is
worthwhile to study how variable conditions in growth season, such as
water, nutrients and light resources, affects germination strategies
(ten Brink et al., 2020).