Large and non-spherical seeds are less likely to form a persistent soil seed bank.

There is some evidence that seed traits can affect the long-term persistence of seeds in the soil. However, findings on this topic have differed between systems. Here, we brought together a worldwide database of seed persistence data for 1474 species to test the generality of seed mass-shape-persistence relationships. We found a significant trend for low seed persistence to be associated with larger and less spherical seeds. However, the relationship varied across different clades, growth forms and species ecological preferences. Specifically, relationships of seed mass-shape-persistence were more pronounced in Poales than in other order clades. Herbaceous species that tend to be found in sites with low soil sand content and precipitation have stronger relationships between seed shape and persistence than in sites with higher soil sand content and precipitation. For the woody plants, the relationship between persistence and seed morphology was stronger in sites with high soil sand content and low precipitation than in sites with low soil sand content and higher precipitation. Improving the ability to predict the soil seed bank formation process, including burial and persistence, could benefit the utilization of seed morphology-persistence relationships in management strategies for vegetation restoration and controlling species invasion across diverse vegetation types and environments.

Spatial variability in herbaceous plant phenology is mostly explained by variability in temperature but also by photoperiod and functional traits.

Whereas temporal variability of plant phenology in response to climate change has already been well studied, the spatial variability of phenology is not well understood. Given that phenological shifts may affect biotic interactions, there is a need to investigate how the variability in environmental factors relates to the spatial variability in herbaceous species' phenology by at the same time considering their functional traits to predict their general and species-specific responses to future climate change. In this project, we analysed phenology records of 148 herbaceous species, which were observed for a single year by the PhenObs network in 15 botanical gardens. For each species, we characterised the spatial variability in six different phenological stages across gardens. We used boosted regression trees to link these variabilities in phenology to the variability in environmental parameters (temperature, latitude and local habitat conditions) as well as species traits (seed mass, vegetative height, specific leaf area and temporal niche) hypothesised to be related to phenology variability. We found that spatial variability in the phenology of herbaceous species was mainly driven by the variability in temperature but also photoperiod was an important driving factor for some phenological stages. In addition, we found that early-flowering and less competitive species characterised by small specific leaf area and vegetative height were more variable in their phenology. Our findings contribute to the field of phenology by showing that besides temperature, photoperiod and functional traits are important to be included when spatial variability of herbaceous species is investigated.

Habitat-based biodiversity responses to macroclimate and edaphic factors in European fen ecosystems.

Understanding large-scale drivers of biodiversity in palustrine wetlands is challenging due to the combined effects of macroclimate and local edaphic conditions. In boreal and temperate fen ecosystems, the influence of macroclimate on biodiversity is modulated by hydrological settings across habitats, making it difficult to assess their vulnerability to climate change. Here, we investigate the influence of macroclimate and edaphic factors on three Essential Biodiversity Variables across eight ecologically defined habitats that align with ecosystem classifications and red lists. We used 27,555 vegetation plot samples from European fens to assess the influence of macroclimate and groundwater pH predictors on the geographic distribution of each habitat type. Additionally, we modeled the relative influence of macroclimate, water pH, and water table depth on community species richness and composition, focusing on 309 plant specialists. Our models reveal strong effects of mean annual temperature, diurnal thermal range, and summer temperature on biodiversity variables, with contrasting differences among habitats. While macroclimatic factors primarily shape geographic distributions and species richness, edaphic factors emerge as the primary drivers of composition for vascular plants and bryophytes. Annual precipitation exhibits non-linear effects on fen biodiversity, with varying impact across habitats with different hydrological characteristics, suggesting a minimum requirement of 600 mm of annual precipitation for the occurrence of fen ecosystems. Our results anticipate potential impacts of climate warming on European fens, with predictable changes among habitat types and geographic regions. Moreover, we provide evidence that the drivers of biodiversity in boreal and temperate fens are closely tied to the ecological characteristics of each habitat type and the dispersal abilities of bryophytes and vascular plants. Given that the influence of macroclimate and edaphic factors on fen ecosystems is habitat specific, climate change research and conservation actions should consider ecological differentiation within functional IUCN ecosystems at continental and regional scales.

Global seed dormancy patterns are driven by macroclimate but not fire regime.

Seed dormancy maximizes plant recruitment in habitats with variation in environmental suitability for seedling establishment. Yet, we still lack a comprehensive synthesis of the macroecological drivers of nondormancy and the different classes of seed dormancy: physiological dormancy, morphophysiological dormancy and physical dormancy. We examined current geographic patterns and environmental correlates of global seed dormancy variation. Combining the most updated data set on seed dormancy classes for > 10 000 species with > 4 million georeferenced species occurrences covering all of the world's biomes, we test how this distribution is driven by climate and fire regime. Seed dormancy is prevalent in seasonally cold and dry climates. Physiological dormancy occurs in relatively dry climates with high temperature seasonality (e.g. temperate grasslands). Morphophysiological dormancy is more common in forest-dominated, cold biomes with comparatively high and evenly distributed precipitation. Physical dormancy is associated with dry climates with strong seasonal temperature and precipitation fluctuations (e.g. deserts and savannas). Nondormancy is associated with stable, warm and wetter climates (e.g. tropical rain forest). Pyroclimate had no significant effect on the distribution of seed dormancy. The environmental drivers considered in this study had a comparatively low predictive power, suggesting that macroclimate is just one of several global drivers of seed dormancy.

Low availability of functional seed trait data from the tropics could negatively affect global macroecological studies, predictive models and plant conservation.

BACKGROUND: Plant seeds have many traits that influence ecological functions, ex situ conservation, restoration success and their sustainable use. Several seed traits are known to vary significantly between tropical and temperate regions. Here we present three additional traits for which existing data indicate differences between geographical zones. We discuss evidence for geographical bias in availability of data for these traits, as well as the negative consequences of this bias. SCOPE: We reviewed the literature on seed desiccation sensitivity studies that compare predictive models to experimental data and show how a lack of data on populations and species from tropical regions could reduce the predictive power of global models. In addition, we compiled existing data on relative embryo size and post-dispersal embryo growth and found that relative embryo size was significantly larger, and embryo growth limited, in tropical species. The available data showed strong biases towards non-tropical species and certain families, indicating that these biases need to be corrected to perform truly global analyses. Furthermore, we argue that the low number of seed germination studies on tropical high-mountain species makes it difficult to compare across geographical regions and predict the effects of climate change in these highly specialized tropical ecosystems. In particular, we show that seed traits of geographically restricted páramo species have been studied less than those of more widely distributed species, with most publications unavailable in English or in the peer-reviewed literature. CONCLUSIONS: The low availability of functional seed trait data from populations and species in the tropics can have negative consequences for macroecological studies, predictive models and their application to plant conservation. We propose that global analyses of seed traits with evidence for geographical variation prioritize generation of new data from tropical regions as well as multi-lingual searches of both the grey- and peer-reviewed literature in order to fill geographical and taxonomic gaps.

Climate shapes the seed germination niche of temperate flowering plants: a meta-analysis of European seed conservation data.

BACKGROUND AND AIMS: Interactions between ecological factors and seed physiological responses during the establishment phase shape the distribution of plants. Yet, our understanding of the functions and evolution of early-life traits has been limited by the scarcity of large-scale datasets. Here, we tested the hypothesis that the germination niche of temperate plants is shaped by their climatic requirements and phylogenetic relatedness, using germination data sourced from a comprehensive seed conservation database of the European flora (ENSCOBASE). METHODS: We performed a phylogenetically informed Bayesian meta-analysis of primary data, considering 18 762 germination tests of 2418 species from laboratory experiments conducted across all European geographical regions. We tested for the interaction between species' climatic requirements and germination responses to experimental conditions including temperature, alternating temperature, light and dormancy-breaking treatments, while accounting for between-study variation related to seed sources and seed lot physiological status. KEY RESULTS: Climate was a strong predictor of germination responses. In warm and seasonally dry climates the seed germination niche includes a cold-cued germination response and an inhibition determined by alternating temperature regimes and cold stratification, while in climates with high temperature seasonality opposite responses can be observed. Germination responses to scarification and light were related to seed mass but not to climate. We also found a significant phylogenetic signal in the response of seeds to experimental conditions, providing evidence that the germination niche is phylogenetically constrained. Nevertheless, phylogenetically distant lineages exhibited common germination responses under similar climates. CONCLUSION: This is the first quantitative meta-analysis of the germination niche at a continental scale. Our findings showed that the germination niches of European plants exhibit evolutionary convergence mediated by strong pressures at the macroclimatic level. In addition, our methodological approach highlighted how large datasets generated by conservation seed banking can be valuable sources to address questions in plant macroecology and evolution.

Regeneration from seed in herbaceous understorey of ancient woodlands of temperate Europe.

BACKGROUND AND AIMS: European ancient woodlands are subject to land use change, and the distribution of herbaceous understorey species may be threatened because of their poor ability to colonize isolated forest patches. The regeneration niche can determine the species assembly of a community, and seed germination traits may be important descriptors of this niche. METHODS: We analysed ecological records for 208 herbaceous species regarded as indicators of ancient woodlands in Europe and, where possible, collated data on seed germination traits, reviewed plant regeneration strategies and measured seed internal morphology traits. The relationship between plant regeneration strategies and ecological requirements was explored for 57 species using ordination and classification analysis. KEY RESULTS: Three regeneration strategies were identified. Species growing in closed-canopy areas tend to have morphological seed dormancy, often requiring darkness and low temperatures for germination, and their shoots emerge in early spring, thus avoiding the competition for light from canopy species. These species are separated into two groups: autumn and late winter germinators. The third strategy is defined by open-forest plants with a preference for gaps, forest edges and riparian forests. They tend to have physiological seed dormancy and germinate in light and at higher temperatures, so their seedlings emerge in spring or summer. CONCLUSION: Seed germination traits are fundamental to which species are good or poor colonizers of the temperate forest understorey and could provide a finer explanation than adult plant traits of species distribution patterns. Seed dormancy type, temperature stratification and light requirements for seed germination are important drivers of forest floor colonization patterns and should be taken in account when planning successful ecological recovery of temperate woodland understories.

Seed ecology of European mesic meadows.

BACKGROUND AND AIMS: European mesic meadows are semi-natural open habitats of high biodiversity and an essential part of European landscapes. These species-rich communities can be a source of seed mixes for ecological restoration, urban greening and rewilding. However, limited knowledge of species germination traits is a bottleneck to the development of a competitive native seed industry. Here, we synthesize the seed ecology of mesic meadows. METHODS: We combined our own experimental data with data obtained from databases to create a combined dataset containing 2005 germination records of 90 plant species from 31 European countries. We performed a Bayesian meta-analysis of this dataset to test the seed germination response to environmental cues including scarification, stratification, temperature, alternating temperature and light. We also used multivariate ordination to check the relationship between seed traits (germination and morphology) and species ecological preferences, and to compare the seed ecology of mesic meadows with that of other herbaceous plant communities from the same geographic area. KEY RESULTS: The seed ecology of mesic meadows is characterized by (1) high seed germinability when compared with other herbaceous plant communities; (2) low correspondence between seed traits and species ecological preferences; and (3) a deep phylogenetic separation between the two major families, Poaceae and Fabaceae. Poaceae produce many light seeds that respond to gap-detecting germination cues (alternating temperatures and light); Fabaceae produce fewer heavy seeds, which need scarification to break their physical dormancy. CONCLUSIONS: High germinability of meadow seeds will reduce their capacity to form persistent seed banks, resulting in dispersal limitations to passive regeneration. For centuries, human activities have shaped the regeneration of meadows, leading to a loss of seed dormancy and decoupling seeds from seasonal cycles, as has been found in many domesticated species. The same anthropic processes that have shaped semi-natural mesic meadows have left them dependent on continued human intervention for their regeneration, highlighting the importance of active restoration via seed supply.

Global DNA methylation and cellular 5-methylcytosine and H4 acetylated patterns in primary and secondary dormant seeds of Capsella bursa-pastoris (L.) Medik. (shepherd's purse).

Despite the importance of dormancy and dormancy cycling for plants' fitness and life cycle phenology, a comprehensive characterization of the global and cellular epigenetic patterns across space and time in different seed dormancy states is lacking. Using Capsella bursa-pastoris (L.) Medik. (shepherd's purse) seeds with primary and secondary dormancy, we investigated the dynamics of global genomic DNA methylation and explored the spatio-temporal distribution of 5-methylcytosine (5-mC) and histone H4 acetylated (H4Ac) epigenetic marks. Seeds were imbibed at 30 °C in a light regime to maintain primary dormancy, or in darkness to induce secondary dormancy. An ELISA-based method was used to quantify DNA methylation, in relation to total genomic cytosines. Immunolocalization of 5-mC and H4Ac within whole seeds (i.e., including testa) was assessed with reference to embryo anatomy. Global DNA methylation levels were highest in prolonged (14 days) imbibed primary dormant seeds, with more 5-mC marked nuclei present only in specific parts of the seed (e.g., SAM and cotyledons). In secondary dormant seeds, global methylation levels and 5-mC signal where higher at 3 and 7 days than 1 or 14 days. With respect to acetylation, seeds had fewer H4Ac marked nuclei (e.g., SAM) in deeper dormant states, for both types of dormancy. However, the RAM still showed signal after 14 days of imbibition under dormancy-inducing conditions, suggesting a central role for the radicle/RAM in the response to perceived ambient changes and the adjustment of the seed dormancy state. Thus, we show that seed dormancy involves extensive cellular remodeling of DNA methylation and H4 acetylation.

The seed germination spectrum of alpine plants: a global meta-analysis.

Assumptions about the germination ecology of alpine plants are presently based on individual species and local studies. A current challenge is to synthesise, at the global level, the alpine seed ecological spectrum. We performed a meta-analysis of primary data from laboratory experiments conducted across four continents (excluding the tropics) and 661 species, to estimate the influence of six environmental cues on germination proportion, mean germination time and germination synchrony; accounting for seed morphology (mass, embryo : seed ratio) and phylogeny. Most alpine plants show physiological seed dormancy, a strong need for cold stratification, warm-cued germination and positive germination responses to light and alternating temperatures. Species restricted to the alpine belt have a higher preference for warm temperatures and a stronger response to cold stratification than species whose distribution extends also below the treeline. Seed mass, embryo size and phylogeny have strong constraining effects on germination responses to the environment. Globally, overwintering and warm temperatures are key drivers of germination in alpine habitats. The interplay between germination physiology and seed morphological traits further reflects pressures to avoid frost or drought stress. Our results indicate the convergence, at the global level, of the seed germination patterns of alpine species.

Seeds of future past: climate change and the thermal memory of plant reproductive traits.

Plant persistence and migration in face of climate change depends on successful reproduction by seed, a central aspect of plant life that drives population dynamics, community assembly and species distributions. Plant reproduction by seed is a chain of physiological processes, the rates of which are a function of temperature, and can be modelled using thermal time models. Importantly, while seed reproduction responds to its instantaneous thermal environment, there is also evidence of phenotypic plasticity in response to the thermal history experienced by the plant's recent ancestors, by the reproducing plant since seedling establishment, and by its seeds both before and after their release. This phenotypic plasticity enables a thermal memory of plant reproduction, which allows individuals to acclimatise to their surroundings. This review synthesises current knowledge on the thermal memory of plant reproduction by seed, and highlights its importance for modelling approaches based on physiological thermal time. We performed a comprehensive search in the Web of Science and analysed 533 relevant articles, of which 81 provided material for a meta-analysis of thermal memory in reproductive functional traits based on the effect size Zr. The articles encompassed the topics of seed development, seed yield (mass and number), seed dormancy (physiological, morphological and physical), germination, and seedling establishment. The results of the meta-analysis provide evidence for a thermal memory of seed yield, physiological dormancy and germination. Seed mass and physiological dormancy appear to be the central hubs of this memory. We argue for integrating thermal memory into a predictive framework based on physiological time modelling. This will provide a quantitative assessment of plant reproduction, a complex system that integrates past and present thermal inputs to achieve successful reproduction in changing environments. The effects of a warming environment on plant reproduction cannot be reduced to a qualitative interpretation of absolute positives and negatives. Rather, these effects need to be understood in terms of changing rates and thresholds for the physiological process that underlie reproduction by seed.

Habitat-related seed germination traits in alpine habitats.

Understanding the key aspects of plant regeneration from seeds is crucial in assessing species assembly to their habitats. However, the regenerative traits of seed dormancy and germination are underrepresented in this context. In the alpine zone, the large species and microhabitat diversity provide an ideal context to assess habitat-related regenerative strategies. To this end, seeds of 53 species growing in alpine siliceous and calcareous habitats (6230 and 6170 of EU Directive 92/43, respectively) were exposed to different temperature treatments under controlled laboratory conditions. Germination strategies in each habitat were identified by clustering with k-means. Then, phylogenetic least squares correlations (PGLS) were fitted to assess germination and dormancy differences between species' main habitat (calcareous and siliceous), microhabitat (grasslands, heaths, rocky, and species with no specific microhabitats), and chorology (arctic-alpine and continental). Calcareous and siliceous grasslands significantly differ in their germination behaviour with a slow, mostly overwinter germination and high germination under all conditions, respectively. Species with high overwinter germination occurs mostly in heaths and have an arctic-alpine distribution. Meanwhile, species with low or high germinability in general inhabit in grasslands or have no specific microhabitat (they belong to generalist), respectively. Alpine species use different germination strategies depending on habitat provenance, species' main microhabitat, and chorotype. Such differences may reflect adaptations to local environmental conditions and highlight the functional role of germination and dormancy in community ecology.

Environmental filtering drives the shape and breadth of the seed germination niche in coastal plant communities.

Background and Aims: A phylogenetic comparative analysis of the seed germination niche was conducted in coastal plant communities of western Europe. Two hypotheses were tested, that (1) the germination niche shape (i.e. the preference for a set of germination cues as opposed to another) would differ between beaches and cliffs to prevent seedling emergence in the less favourable season (winter and summer, respectively); and (2) the germination niche breadth (i.e. the amplitude of germination cues) would be narrower in the seawards communities, where environmental filtering is stronger. Methods: Seeds of 30 specialist species of coastal plant communities were collected in natural populations of northern Spain. Their germination was measured in six laboratory treatments based on field temperatures. Germination niche shape was estimated as the best germination temperature. Germination niche breadth was calculated using Pielou's evenness index. Differences between plant communities in their germination niche shape and breadth were tested using phylogenetic generalized least squares regression (PGLS). Key Results: Germination niche shape differed between communities, being warm-cued in beaches (best germination temperature = 20 °C) and cold-cued in cliffs (14 °C). Germination niche was narrowest in seawards beaches (Pielou's index = 0·89) and broadest in landwards beaches (0·99). Cliffs had an intermediate germination niche breadth (0·95). The relationship between niche and plant community had a positive phylogenetic signal for shape (Pagel's λ = 0·64) and a negative one for breadth (Pagel's λ = -1·71). Conclusion: Environmental filters shape the germination niche to prevent emergence in the season of highest threat for seedling establishment. The germination niche breadth is narrower in the communities with stronger environmental filters, but only in beaches. This study provides empirical support to a community-level generalization of the hypotheses about the environmental drivers of the germination niche. It highlights the role of germination traits in community assembly.

Simulating the germination response to diurnally alternating temperatures under climate change scenarios: comparative studies on Carex diandra seeds.

BACKGROUND AND AIMS: Environmental temperature regulates plant regeneration via seed in several superimposed ways, and this complex regulation will be disrupted by climate change. The role of diurnally alternating temperatures (ΔT) in terminating dormancy will be a major factor in this disruption, as its effects on seed germination are immediate. METHODS: The effect of ΔT on seed germination was modelled using two populations of the wetland sedge Carex diandra, one from a montane site and one from a subalpine site. A cardinal-temperature model was fitted to germination results obtained from a thermal gradient plate, and the model was used to simulate changes in germination under two possible future climate scenarios (RCP2·6 and RCP8·5, for representative concentration pathways) as defined by the Intergovernmental Panel on Climate Change. KEY RESULTS: Scenario RCP2·6 projected moderate increases in average temperatures and ΔT, whereas RCP8·5 projected greater warming and higher ΔT. Increasing ΔT decreased the base temperature for seed germination and the thermal time required for germination. The effect of higher ΔT together with the higher temperatures increased germination under both climate scenarios. CONCLUSIONS: Carex diandra germination is highly responsive to potential changes in ΔT, and thus this study highlights the role of ΔT in seed responses to climate change. Comprehensive cardinal-temperature models, encompassing the different effects of temperature on seed germination, are needed to understand how climate change will affect plant regeneration.

A local dormancy cline is related to the seed maturation environment, population genetic composition and climate.

BACKGROUND AND AIMS: Seed dormancy varies within species in response to climate, both in the long term (through ecotypes or clines) and in the short term (through the influence of the seed maturation environment). Disentangling both processes is crucial to understand plant adaptation to environmental changes. In this study, the local patterns of seed dormancy were investigated in a narrow endemic species, Centaurium somedanum, in order to determine the influence of the seed maturation environment, population genetic composition and climate. METHODS: Laboratory germination experiments were performed to measure dormancy in (1) seeds collected from different wild populations along a local altitudinal gradient and (2) seeds of a subsequent generation produced in a common garden. The genetic composition of the original populations was characterized using intersimple sequence repeat (ISSR) PCR and principal co-ordinate analysis (PCoA), and its correlation with the dormancy patterns of both generations was analysed. The effect of the local climate on dormancy was also modelled. KEY RESULTS: An altitudinal dormancy cline was found in the wild populations, which was maintained by the plants grown in the common garden. However, seeds from the common garden responded better to stratification, and their release from dormancy was more intense. The patterns of dormancy variation were correlated with genetic composition, whereas lower temperature and summer precipitation at the population sites predicted higher dormancy in the seeds of both generations. CONCLUSIONS: The dormancy cline in C. somedanum is related to a local climatic gradient and also corresponds to genetic differentiation among populations. This cline is further affected by the weather conditions during seed maturation, which influence the receptiveness to dormancy-breaking factors. These results show that dormancy is influenced by both long-and short-term climatic variation. Such processes at such a reduced spatial scale highlight the potential of plants to adapt to fast environmental changes.