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).