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To produce many small or a few large seeds: size-dependent germination strategies of herbs in a species-rich natural alpine grassland

X.-Q. Li

orcid.org/0009-0005-7891-5547

School of Ecology and Environment, Tibet University, Lhasa, China

Key Laboratory of Biodiversity and Environmental on the Qinghai-Tibetan Plateau, Ministry of Education, School of Ecology and Environment, Tibet University, Lhasa, China

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

These authors contributed equally to this work.

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H.-Y. Zhu,

H.-Y. Zhu

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

College of Forestry, Jiangxi Agricultural University, Nanchang, China

These authors contributed equally to this work.

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A. C. Ochola,

A. C. Ochola

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

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L. Qiong,

L. Qiong

School of Ecology and Environment, Tibet University, Lhasa, China

Key Laboratory of Biodiversity and Environmental on the Qinghai-Tibetan Plateau, Ministry of Education, School of Ecology and Environment, Tibet University, Lhasa, China

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Z.-M. Ye,

Z.-M. Ye

orcid.org/0000-0002-8290-0891

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

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C.-F. Yang,

Corresponding Author

C.-F. Yang

[email protected]

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

Correspondence

C.-F. Yang, State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China.

E-mail: [email protected]

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X.-Q. Li,

X.-Q. Li

orcid.org/0009-0005-7891-5547

School of Ecology and Environment, Tibet University, Lhasa, China

Key Laboratory of Biodiversity and Environmental on the Qinghai-Tibetan Plateau, Ministry of Education, School of Ecology and Environment, Tibet University, Lhasa, China

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

These authors contributed equally to this work.

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H.-Y. Zhu,

H.-Y. Zhu

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

College of Forestry, Jiangxi Agricultural University, Nanchang, China

These authors contributed equally to this work.

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A. C. Ochola,

A. C. Ochola

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

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L. Qiong,

L. Qiong

School of Ecology and Environment, Tibet University, Lhasa, China

Key Laboratory of Biodiversity and Environmental on the Qinghai-Tibetan Plateau, Ministry of Education, School of Ecology and Environment, Tibet University, Lhasa, China

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Z.-M. Ye,

Z.-M. Ye

orcid.org/0000-0002-8290-0891

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

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C.-F. Yang,

Corresponding Author

C.-F. Yang

[email protected]

State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China

Correspondence

C.-F. Yang, State Key Laboratory of Plant Diversity and Specialty Crops, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China.

E-mail: [email protected]

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First published: 25 July 2025

https://doi.org/10.1111/plb.70081

Editor: C. Wellstein

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Abstract

Seeds are the product of plant sexual reproduction and experience strong selection regarding resource investment. Seed germination strategy in response to environmental cues usually depends on seed mass and is believed to be strongly selected for successful seedling establishment. Selection for germination strategy and resource allocation pattern may be functionally interlinked; however, little is known about whether and how such interaction contributes to the diversity of plant communities.
This study investigated resource allocation pattern and germination strategy of 75 flowering herbs from a species-rich alpine grassland. We measured seed mass and seed number per fruit and germinated seeds under temperature and light fluctuations simulating the natural growing season. Final germination proportion (FGP) and germination synchrony (uncertainty index, UNC) were calculated. The relationship between seed size and number and the influences on FGP and UNC across germination conditions were analysed using phylogenetic approaches.
The results revealed a strong trade-off between seed mass and seed number per fruit across the investigated species. FGP for smaller seeds was more sensitive to environmental cues than for larger seeds. The response of germination UNC to environmental cues was independent of seed mass.
In this alpine grassland, species producing many small seeds showed greater germination sensitivity to environmental cues, while those producing few large seeds required more stable conditions for germination. The differences in seed germination strategies among species with varied seed masses may enhance population regeneration of diverse species in unpredictable conditions.

INTRODUCTION

Plants that produce seeds through sexual reproduction possess significant evolutionary advantages, for example, facilitating maintenance of genetic diversity and enhancing adaptability of their offspring, promoting colonization of more suitable habitats through seed dispersal (Wisnoski & Shoemaker 2022). Seeds may also enhance the adaptability of plants to environmental changes through specific germination strategies at both intra- and interspecific levels (Mondoni et al. 2012; Gremer & Venable 2014; Hoyle et al. 2015; Espinosa del Alba et al. 2025). Production of seeds is resource-consuming for plants because seeds are typically rich in organic substances (Hodgson et al. 2017). The production of large or small seeds may be a reflection of the allocation patterns of maternal resources to offspring, which could be of adaptive significance (Shaanker et al. 1988). Variation in seed size among plants is an intriguing ecological question (Moles et al. 2005) associated with many factors, such as plant growth form, habitat, geographic distribution, dispersal mode, predation pressure, and phylogeny (Leishman et al. 2000; Moles et al. 2007; Igea et al. 2017; Dylewski et al. 2020; Zhang & Wang 2024; Chen et al. 2025), and potentially influences community structure and plant coexistence (Leishman et al. 2000; Dylewski et al. 2020). Moreover, seed size is an important factor influencing germination (Fernández-Pascual et al. 2021; Notarnicola et al. 2023). However, the influence of the broad spread of seed size variation on maintenance of plant diversity through its impact on germination requires further investigations.

Theoretical and empirical evidence suggests that plants produce either a few large or many small seeds (Smith & Fretwell 1974; Hodgson et al. 2020). For large seeds, a failure in seedling survival after germination initiation means a heavier resource cost than for small seeds. However, plants in regions with stable climates tend to produce large seeds (Rubio de Casas et al. 2017). Large seeds are also thought to have advantages in tolerating unfavourable factors like drought or frost (Coomes & Grubb 2003). Conversely, small seeds may be more sensitive to environmental cues in initiating germination, which are related to their lighter seed coats (Wu et al. 2019), and benefit plants through limited resource use and early growth in a community. Although the survival of subsequent seedlings may be challenged under unpredictable conditions, producing a relatively large number of seeds could spread the risk (Leishman 2001). Hence, to enhance overall fitness of plants within a community growing under variable conditions, we expect that variations in seed mass among species is linked to both germination strategy and resource allocation pattern; however, this has seldom been evidenced in empirical studies.

Seeds of different sizes vary in starch and endosperm nutrient levels, potentially contributing to final germination proportion (FGP), speed of germination and seedling growth, and chance of seedling survival (Volis & Bohrer 2013). Large seeds may have more successful germination than smaller seeds because of the higher nutrient content (Fernández-Pascual et al. 2019; Mao et al. 2019). Nevertheless, there may be a negative correlation between seed mass and germination of alpine plants, as larger seeds may have comparatively strong dormancy because of their thick and hard seed coats (Bu et al. 2007; Ge et al. 2020). Small seeds tend to be more responsive to environmental cues than large seeds (Liu et al. 2013). In legumes, environments with stable climates select for taxa with large, fast-germinating seeds, while small seeds are more adapted to and predominate in seasonal habitats (Rubio de Casas et al. 2017). Climate has also shaped the relationship of seed mass to germination (Carta et al. 2022). Phylogenetic relatedness is also a significant factor contributing to heterogeneity in relationships between seed mass and germination proportion (Fernández-Pascual et al. 2019; Carta et al. 2022). Previous studies found a complex pattern that suggests seed mass variation and its influence on germination may be associated with environmental heterogeneity and phylogenetic relationship (Fernández-Pascual et al. 2021).

In addition to FGP, the level of synchronization in seed germination is also an important germination indicator, estimated by the germination uncertainty index (UNC). This index quantifies the scatter of germination through time and whether germination is synchronous (i.e., most seeds germinate around the mean germination time) or asynchronous (i.e., germination events are separated through time during the germination experiment). An asynchronous germination pattern may be a bet-hedging strategy by spreading the risk of seedling failure under variable environments (Simons 2011). Lower values of germination UNC indicate higher germination synchrony. Fernández-Pascual et al. (2021) found that in alpine plants, germination UNC increased when temperatures were relatively cold, which is an effective germination strategy against early-spring frost damage. In contrast, decreased germination UNC under warm conditions can benefit alpine seedling survival and population regeneration under favourable summer conditions (Fernández-Pascual et al. 2021). However, the relationship between germination synchronism and seed mass within plant communities in variable environments is not well understood but could contribute to our understanding of reproduction and regeneration mechanisms in different plants in response to changing environmental conditions.

Temperate alpine habitats are characterized by low temperatures, short growing seasons, and climate variability (Testolin et al. 2020). Plants in alpine habitats may face a dilemma when initiating germination. On the one hand, if they are sensitive to environmental cues and initiate growth early in the season, they may risk exposure to freezing events (Inouye 2008) and waste the resources allocated to the seeds. On the other hand, if their germination is attuned to specific summer cues, they might initiate growth at a relatively late time and thus not fully utilize the resources of the growing season, which might mean that they are not competitive in producing offspring with high performance (Cooper et al. 2011). Studies have indicated that alpine plants at different altitudes varied their responses to temperature fluctuations (Liu et al. 2013), suggesting an adaptive strategy in their seed germination. Nevertheless, in unpredictable alpine conditions, further investigation is needed to explore whether and how this germination strategy is interlinked with the seed resource allocation pattern, which will enrich knowledge on the seed ecology of alpine plants and, moreover, contribute to understanding the maintenance mechanisms of diverse plants within a community.

In this study, we hypothesize that, because of selection pressures from variable environmental conditions in alpine habitats, variation in germination strategy is interlinked with the allocation of seed resources across the plants. Specifically, species that produce smaller seeds are more sensitive to environmental cues for germination than larger seeds. However, an increase in seed number is necessary for small-seeded species to offset the potential risk of seedling failure in subsequent unfavourable conditions. We tested this hypothesis by investigating seeds of 75 herb species (including legumes) from a species-rich alpine natural grassland and their germination responses to environmental cues.

MATERIAL AND METHODS

Study site

The study species were selected from a species-rich alpine natural grassland (27°37′N, 99°47′ E; 3360 m a.s.l.) on the eastern edge of the Hengduan Mountains, China. This grassland lies in a small valley basin, encircled by mountains, and covers an area of ca. 2 ha. More than 120 entomophilous flowering herbs have been recorded in this grassland, and their flowering overlaps within a relatively short period, typically from late May to early September (Ye et al. 2024). These plants grow naturally without agronomic management. According to the China Meteorological Data Service, the mean annual temperature in this region is 6.3°C, with a minimum monthly average of −2.3°C (January) and a maximum monthly average of 13.9°C (July) (Zhang et al. 2023). Annual precipitation is 651.1 mm, with 71% of this occurring from June to September. The large diurnal temperature fluctuations and frequent summer rainstorms pose challenges to plant growth (Xu et al. 2018). Additionally, plants in this area must contend with unpredictable factors, such as frost, extremely low temperatures, and precipitation during the flowering season (Wu et al. 2025).

Seed collection and storage, seed number, and seed mass

We collected freshly ripe fruits or seeds at the time of their natural dispersal from July to September 2020. After collection, material was dried at room temperature (20°C, 50% relative humidity) for 3 weeks. Seeds were stored dry in a refrigerator at 4°C for 6 months in darkness until the start of the germination experiments (Rosbakh & Poschlod 2015). Studies have shown that dry-cold storage does not affect seed dormancy status (Liu et al. 2011; Peng et al. 2021), and maintain the natural attributes of germination responses to environmental cues (Li et al. 2024). To estimate seed number per fruit, we randomly selected at least 30 individual plants from each species, then randomly dissected one to three mature fruits (or infructescence) per plant (no data for Pedicularis dunniana). Three replicates of 100 mature seeds for each species were weighed to the nearest 0.01 mg to determine seed mass. Our study aims to illustrate the seed size–number relationship and its influence on germination. Therefore, we excluded grasses since they have only one seed per fruit and, moreover, seed number per infructescence is difficult to count for grasses. Finally, we successfully collected enough fully mature seeds (>600) from at least 30 individuals per species (including legumes), encompassing 75 species from 19 families, for germination experiments.

Germination experiments

To create a gradient of environmental cues and to promote germination, we simulated monthly day and night temperatures, as well as photoperiod, for the growing months in the study grassland. We used soil temperature and photoperiod data from the China Meteorological Data Network (https://data.cma.cn) to calculate monthly averages from April to October as germination conditions. We created five experimental conditions for seed germination. The alternating temperature of germination conditions (day/night) were set at 20/1°C (April), 22/4°C (May), 22/9°C (June–August, with similar average temperatures for all 3 months), 20/7°C (September), and 18/3°C (October). Similarly, the simulated photoperiods, based on onsite daylight duration, were 12 h 50 min (April), 13 h 30 min (May), 13 h 32 min (June–August; with similar values for all 3 months), 12 h 18 min (September), and 11 h 29 min (October). To investigate the effect of germination conditions on germination response variables, we calculated mean daily temperature for each germination condition based on day/night temperatures and their durations, expressed as a metrically scaled variable (Table 1).

Table 1. Mean of final germination proportion (FGP) and germination uncertainty (UNC) indicies under different germination conditions for the 75 study species.

month	daytime germination temperature	day length	nighttime germination temperature	night length	mean daily temperature	mean FGP	mean UNC
April	20°C	12.8 h	1°C	11.2 h	11.2°C	21.88%	1.28
May	22°C	13.5 h	4°C	10.5 h	14.1°C	35.86%	1.87
June–August	22°C	13.5 h	9°C	10.5 h	16.3°C	41.16%	2.18
September	20°C	12.3 h	7°C	11.7 h	13.7°C	39.41%	2.18
October	18°C	11.5 h	3°C	12.5 h	10.2°C	24.61%	1.50

The germination conditions (temperature and photoperiod) were established by simulating environmental conditions of the study grassland from April to October, which represents the growing season of the plants. Average soil temperature and photoperiod of the respective month at the study site were set up as germination conditions. Data were sourced from the China Meteorological Data Network (https://data.cma.cn). The mean daily temperature for each germination condition was calculated from day/night temperatures and their durations.

Before germination, seeds were sterilized in 5% (v/v) sodium hypochlorite (NaClO) for 5 min then rinsed three times with distilled water (Bae et al. 2016; Tian et al. 2021). For each species, three replicates of 40 intact seeds were incubated on moist filter paper in 9 cm diameter Petri dishes under each of the five germination conditions. Germination experiments were carried out in temperature- and light-controlled incubators (HP300GS-C, China) for 30 days. Seeds were scored as germinated when the primary root (radicle) emerged. We counted the number of germinated seeds every day. During germination experiments, empty and dead seeds observed in Petri dishes were excluded (Wang, Alvarez, et al. 2021).

Germination response variables

We used FGP and level of germination synchronization to characterize the germination response for all species under each treatment. FGP was calculated as number of seeds that had germinated at the end of the experiment out of all viable seeds in each treatment (Wang, Gowland, et al. 2021). Germination synchronization was estimated as the germination UNC (Fernández-Pascual et al. 2021). This index assesses the degree of dispersion of germination and was calculated using the package “GerminaR” in R (Lozano-Isla et al. 2019):

\mathrm{UNC}\kern0.5em =\kern0.5em -\sum \limits_{i=1}^k{f}_{\mathrm{i}}{\log}_2{f}_{\mathrm{i}},\kern0.5em \mathrm{where}\kern0.5em {f}_{\mathrm{i}}\kern0.5em =\kern0.5em \frac{n_{\mathrm{i}}}{\sum \limits_{i=1}^k{n}_{\mathrm{i}}}

(1)

where,

{n}_{\mathrm{i}}

is number of seeds germinated in the

{i}^{\mathrm{th}}

time; k is last day of germination evaluation; and

{f}_{\mathrm{i}}

is relative frequency of germination. When

{f}_{\mathrm{i}}

is zero, UNC equals zero. Lower values of UNC indicate higher germination synchrony.

Statistical analyses

We tested the relationship of seed mass variation with seed number per fruit and their interaction effect with germination conditions on seed germination (FGP and UNC). Since we were comparing traits of multiple species, and these species were not independent data points but connected by a shared phylogeny, we used phylogenetically explicit statistical tests. Specifically, we applied phylogenetic generalized least squares (PGLS) model to detect the relationship between seed mass and seed number per fruit among the species (i.e., seed number per fruit ~ Seed mass). The PGLS model, an extension of generalized least squares that incorporates phylogeny into the error structure as a variance–covariance matrix to address species non-independence (Mazel et al. 2016), was implemented using the “gls” function from the “nlme” R package (Pinheiro 2011). Additionally, we fitted phylogenetically generalized linear mixed models with Bayesian estimation (Markov Chain Monte Carlo generalized linear mixed models, MCMCglmms) using the “MCMCglmm” R package, in which the phylogenetic variance/covariance matrix is a random effect (Hadfield 2010). This matrix represents evolutionary relationships between species. Therefore, the model is able to account for the non-independence of observations related to different species and reduces potential bias in the estimation of species-level relationships. We used binomial MCMCglmms to model the FGP (ratio of count data) and Gaussian MCMCglmms for germination UNC. In these two models, seed mass, seed number per fruit, germination conditions (as a categorical variable), and their second-degree interactions were set as fixed terms. Seed mass and seed number were log₁₀-transformed to stabilize variance (reduce heteroscedasticity). These models used the reconstructed phylogeny and species as random effects.

The phylogenetic tree was generated using the “phylo.maker” function from the R package “V.PhyloMaker” (Jin & Qian 2019), utilizing the Angiosperm Phylogeny Group classification of flowering plants as a basis (Zanne et al. 2014). Each MCMCglmm model was run for 50 000 iterations, with a burn-in period of 1 000 and a thinning interval of 100. We used diagnostic plots to check for convergence of the model. We generated ca. 490 posterior distributions for each model. We calculated the mean parameter estimates and 95% highest posterior density and credible intervals (CI) from the resulting posterior distributions. The significance of model parameters was estimated by examining CIs, where parameters with CIs overlapping with zero were not significant. To estimate the phylogenetic signal, we used Pagel's λ (Pagel 1999), estimated simultaneously with the models by calculating mean of the posterior distribution and the 95% CI of λ. When λ = 0, related taxa are not more similar than expected by chance. When λ = 1, the trait is evolving following a constant variance random walk or Brownian motion model; intermediate values of λ indicate a phylogenetic correlation in trait evolution that deviates partially from a Brownian motion model (Pagel 1999).

The regression line for seed mass with seed number per fruit was extracted from the PGLS model, and visualized using the “plot_model” function in the R package “sjPlot” (Lüdecke 2021). We used the R package “visreg” (Breheny & Burchett 2017) to display the response of germination to changes in conditions for seeds with different masses. This differs from the purpose of the MCMCglmm model analysis, which aimed to compare the effects of seed mass on germination response variables (FGP and germination UNC) across different germination conditions. To do this, we refitted the models (as the “visreg” command cannot take MCMCglmm models) using the “glmer” function (in the “lme4” package) to make partial residual plots (Simpson et al. 2021). In these models, seed mass was log₁₀-transformed to address heteroscedasticity and approximate a linear relationship with the response variable, improving model fit and interpretability.

As the FGP follows a binomial distribution, we structured the response variable in both MCMCglmm and GLMM models using the cbind() function to create a binomial vector combining the number of successes (number of seeds germinated) and the number of failures (number of seeds minus number of seeds germinated) (Wayo et al. 2022). All statistical analyses were performed using R v. 4.2.3 (R Core Team 2023).

RESULTS

There was a considerable difference (635-fold) in seed mass, with a minimum of 1.83 mg (Micranthes pallida) and a maximum of 1163.90 mg (Iris bulleyana) across the study species. Seed number per fruit (or per infructescence) varied (266-fold) from 1.08 (Astragalus dumetorum) to 285.87 (Saxifraga diversifolia). Additionally, the FGP displayed substantial variation among species under each of the germination conditions (almost from 0% to 100%). Together with the change in simulated germination condition from coldest to warmest mean daily temperature, mean FGP of the study species was 24.61%, 21.88%, 39.41%, 35.86%, and 41.16%, respectively (Table 1). The range of germination UNC was from 0 to 3.77, and the means were 1.50, 1.28, 2.18, 1.87, and 2.18, respectively (Table 1).

The PGLS model revealed a significantly negative relationship between seed mass and seed number per fruit among species in the alpine natural grassland (P < 0.01; Fig. 1, Table S1); species with smaller seeds tended to have a higher seed number per fruit. The phylogenetic signal of the response of seed mass to seed number per fruit was relatively low (λ = 0.071; Table S1). Furthermore, species had a significant effect on FGP and the germination UNC in the MCMCglmm models (Fig. S1), indicating these traits are subject to interspecific variability. The phylogenetic signal of germination response (FGP and UNC) was significantly different from zero (Fig. S2).

Details are in the caption following the image — **Fig. 1**
Open in figure viewer PowerPoint

The relationship between seed number per fruit (log₁₀ transformed) and seed mass (log₁₀ transformed) among the study species revealed using a phylogenetic generalized least squares (PGLS) model. Fitted line derived from the PGLS model. Shaded area represents 95% confidence interval (estimated values in Table S1).

Results indicated that both FGP and germination UNC were negatively influenced by seed mass (P_MCMC = 0.037 and P_MCMC = 0.041, respectively; Fig. 2, Table S2), while seed number per fruit had no effect (Fig. 2, Table S2). Compared to large seeds, small seeds displayed higher FGP (Fig. 3a) and germination UNC (Fig. 3b). The MCMCglmm model also revealed that FGP at the lowest temperature (10.2°C) significantly differed by that of the reference temperature (16.3°C, the warmest), with comparatively higher FGP at the warmest temperature (Fig. 2a, Table S2). The partial residual plots of the germination response to changes in germination conditions showed that FGP was higher in warmer than in cooler simulated conditions (Fig. 3).

Moreover, the MCMCglmm model revealed that FGP was significantly affected by the interaction of germination condition and seed mass, whereas no such effect was found on the germination UNC (Fig. 2, Table S2). The interaction of seed number per fruit and germination conditions had no significant effect on seed germination (Table S2). The partial residual plots showed that the change of FGP in response to changes in germination conditions was more evident for small seeds than for large seeds (Fig. 3a, Table S3). In other words, for species with smaller seeds, changes in germination conditions (quantified by increase of germination temperature) had a more positive effect on FGP. While for species with larger seeds, the positive effect was weaker (Fig. 3a). Nonetheless, the effect of increasing temperature on germination UNC did not depend on seed mass (Fig. 3b, Table S3).

DISCUSSION

In general, most species in our studied alpine natural grassland had a relatively low germination proportion, indicating that dormancy might still affect the germination status. Deep physiological dormancy and low germination of seeds are common in alpine plants (Schwienbacher et al. 2011). Dormancy-breaking requires cold overwintering or an extended germination period (Tudela-Isanta et al. 2018). Postponing germination helps seedlings to avoid harsh winter conditions in the alpine environment. The factors determining dormancy-breaking likely vary widely among plant species (Hoyle et al. 2015) or among populations of the same plant (Satyanti et al. 2019), reflecting that variations in germination strategy (e.g., extent of dormancy) depend on plant species and environmental cues. The experimental treatments for germination in this study were separately controlled in stable conditions, which may not have fully satisfied the cumulative temperature requirements or dynamic photoperiod regulation needed to break dormancy in certain species (Hoyle et al. 2015). A further methodological limitation of this study concerns the pre-germination seed storage conditions, which did not fully replicate natural environmental parameters and thus could have influenced germination viability. Although we reported low germination rates for the studied alpine plants, the substantial variation in both FGP and germination UNC indicate that the species had several different germination strategies. The germination response to environmental cues varied across species with different seed masses, and moreover, this variation was associated with the resource allocation patterns of the species. Our findings suggest a potential link between selection on germination strategy and seed resource allocation pattern, which could enhance population regeneration of diverse plants in the grassland.

Alpine plant seeds preferably germinate in warmer conditions (Fernández-Pascual et al. 2021). Our results confirm that FGP was higher in warmer conditions. The severe inhibition of seed germination under cool conditions may explain this result (Shimono & Kudo 2005). Cold-adapted plants tend to have the warm-cued germination, which could be a physiological mechanism that reduces the risk of seedlings suffering from low temperatures and frost in autumn or early spring (Mattana et al. 2022). Moreover, photoperiod can be an additional factor that affects germination (Fernández-Pascual et al. 2021). FGP in our study was higher under longer duration of light exposure (day length).

A global-scale analysis revealed a positive influence of seed mass on germination (Fernández-Pascual et al. 2019), but we found a negative effect of seed mass on FGP. Heavier seeds have stronger dormancy due to thick and hard seed coats (Soltani et al. 2018). The negative effects reported in our study are similar to those reported by Bu et al. (2007) and Ge et al. (2020) from the Qinghai-Tibet plateau. Moreover, Vesela et al. (2020) indicated that heavier seeds from warm and arid regions germinate better, while lighter seeds from cold and wet regions exhibit higher germination proportions. This suggests that the influence of seed mass on germination might be associated with the flora of a given alpine area which has undergone selection pressure related to area-specific abiotic and/or biotic factors. For instance, the risk of early spring frosts delays seed germination of alpine plants (Jurado & Flores 2005). In plants subject to predators, seeds may increase seed coat thickness to avoid predation, thus intensifying physical dormancy (Paulsen et al. 2013). In addition, large seeds had lower germination UNC than small seeds, indicating that large seeds tend to germinate more synchronously. Compared to species with large seeds in the studied alpine grassland, the high FGP might leave species with small seeds at high risk in unstable conditions. Nevertheless, the comparatively low synchronous germination of small seeds may reduce the risk. Asynchronous germination can also spread the timing of seed germination, allowing species to share resources and habitats. This increases the chance of seedling survival in changeable conditions (Simons 2011; Volis & Bohrer 2013).

The selection of seed mass depends on availability of limiting resources. For a given amount of resources available to a parent plant, seed mass and seed number constrain one another (Shaanker et al. 1988), which is well supported in our observations of trade-offs between seed mass and seed number per fruit among phylogenetically different species in this species-rich alpine natural grassland. This indicates that plants in this alpine grassland have different resource allocation strategies for seeds, which might improve the general fitness of diverse plants in the community. Leishman (2001) found that species with larger seeds are more likely to win in the competition against species with smaller seeds. Moreover, small-seeded species may be superior colonists due to their greater seed number (Sonkoly et al. 2017). In addition, many plants also reproduce clonally and may have different strategies for resource allocation between seed mass and seed number, as resources can also be invested in asexual propagules.

Moreover, our result demonstrated that the changes in FGP across different germination conditions depends on seed mass. Previous studies indicate that the germination of small seeds is more sensitive to changes in environmental cues than germination of large seeds in both fluctuating temperature conditions (Fernández-Pascual et al. 2021) and across varying photoperiods (Fernández-Pascual et al. 2021; Ma et al. 2023). Large seeds contain more resources than small seeds and thus have better ability to survive environmental hazards, such as drought or frost (Coomes & Grubb 2003; Rubio de Casas et al. 2017). Large seeds can germinate at greater soil depths, protecting them from unfavourable environmental conditions (Fernández-Pascual et al. 2021). From a resource utilization perspective, inappropriate germination of large seeds under harsh conditions leading to seedling failure incur high resource costs. The less sensitive response of larger seeds to environmental cues suggests that they might depend more on physiological attributes than small seeds. Conversely, germination of small seeds is more responsive to environmental cues, which might be partially attributed to the comparatively thinner seed coats. This could potentially benefit these seedlings by allowing them to compete for resources and enjoy a relatively extended growing period, especially if they emerge early in the alpine grassland. However, in unpredictable alpine conditions, seedlings may also be at high risk of encountering subsequent unfavourable conditions, such as frost in early spring. Increased seed production by plants with small seeds could compensate for such risks. Regardless of seed mass, the change in germination UNC in response to environmental cues was similar, indicating that seeds actively respond to environmental changes through dispersed germination. This suggests that asynchronous germination is the prevailing strategy for most plants in alpine habitats to spread the risk of seedling production under unfavourable conditions (Hoyle et al. 2015; Satyanti et al. 2019). The germination strategies of the studied alpine plants are related to seed resource allocation patterns, which promote niche differentiation in terms of germination strategies among different species and facilitate the coexistence of multiple species in the community.

CONCLUSION

Our study revealed that interspecific variation in germination is significantly influenced by seed mass, with higher FGP and germination UNC indices for small seeds than for large seeds. Under warm conditions, FGP was highest, and germination of smaller seeds was more sensitive to environmental cues compared to larger seeds. However, the response of germination UNC to environmental cues was independent of seed mass, suggesting an overall risk-spreading strategy. Given that seedlings from small seeds have a comparatively high risk of encountering unfavourable conditions, our finding that small-seeded species always produce more seeds indicates that resource allocation patterns may help compensate for and spread such risks. The functional association of interspecific variation in germination strategy and resource allocation pattern serves as compelling evidence for ability of plants in this alpine natural grassland to overcome environmental instability and maintain diversity.

AUTHOR CONTRIBUTIONS

CFY and ZMY conceived and designed the experiment. XQL and HYZ performed the experiments and collected data, XQL performed statistical analysis, XQL and CFY drafted the manuscript. All authors contributed to improvement of the manuscript and gave their final approval for publication.

ACKNOWLEDGEMENTS

The authors thank Dr. Eduardo Fernández-Pascual and Dr. Si-Chong Chen for improving scientific merit and language, Yong-Deng He, Wen Huang, De-Xin Liu, Han-Ning Lun and Min Lv for assistance in the field, and Huan Liang for helpful discussion during the project. The study was supported by the National Natural Science Foundation of China (No. 32170241, 31770255 and 31970253).

CONFLICT OF INTEREST STATEMENT

The authors have no competing interests to declare that are relevant to the content of this article.

Open Research

DATA AVAILABILITY STATEMENT

Data and/or code are provided as private-for-peer review via the link: https://figshare.com/articles/dataset/26251307. All data will also be permanently archived.

Supporting Information

Filename

Description

plb70081-sup-0001-Fig.S1.zipZip archive, 780.8 KB

Fig. S1. Effect of the random factor of species on final germination proportion (FGP) and germination uncertainty index (UNC) according to MCMC generalized linear mixed model. Dots indicate posterior mean of species, and whiskers are 95% credible interval. The line of zero effect is shown.

Fig. S2. Phylogenetic signal of final germination proportion (FGP) and germination uncertainty index (UNC) according to MCMC generalized linear mixed model. Dots indicate posterior mean of lambda, and whiskers its 95% credible interval. When λ = 0, related taxa are no more similar than expected by chance; when λ = 1, the trait is evolving following a constant variance random walk or Brownian motion model.

plb70081-sup-0002-TableS1.docxWord 2007 document , 25 KB

Table S1. Statistics for phylogenetic generalized least squares model analysing the relationship between seed number per fruit and seed mass.

Table S2. The contributions of seed mass, seed number per fruit, and germination conditions to final germination proportion, and the germination uncertainty index according to MCMC generalized linear mixed model. When credible intervals overlap with zero, the effect is not significant.

Table S3. Results of generalized linear mixed-effects models showing the effects of seed mass, germination conditions, and their interactions on final germination proportion and germination uncertainty index.

Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

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Early View

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To produce many small or a few large seeds: size-dependent germination strategies of herbs in a species-rich natural alpine grassland

Abstract

INTRODUCTION