The seed morphospace, a new contribution towards the multidimensional study of angiosperm sexual reproductive biology.

BACKGROUND: The evolutionary success of flowering plants is associated with the vast diversity of their reproductive structures. Despite recent progress in understanding angiosperm-wide trends of floral structure and evolution, a synthetic view of the diversity in seed form and function across angiosperms is lacking. SCOPE: Here we present a roadmap to synthesise the diversity of seed forms in extant angiosperms, relying on the morphospace concept, i.e. a mathematical representation which relates multiple traits and describes the realised morphologies. We provide recommendations on how to broaden the range of measurable traits beyond mass, by using key morphological traits representative of the embryo, endosperm, and seed coat but also fruit attributes (e.g., dehiscence, fleshiness). These key traits were used to construct and analyse a morphospace to detect evolutionary trends and gain insight into how morphological traits relate to seed functions. Finally, we outline challenges and future research directions, combining the morphospace with macroevolutionary comparative methods to underline the drivers that gave rise to the diversity of observed seed forms. CONCLUSIONS: We conclude that this multidimensional approach has the potential, although still untapped, to improve our understanding of covariation among reproductive traits, and further elucidate angiosperm reproductive biology as a whole.

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.

Seeds as natural capital.

Halting and reversing the current loss of biodiversity and habitats will be facilitated by a comprehensive valuation of all nature's contributions to people (NCPs), on which we rely. In this context, we explore the full natural capital value of seeds to reveal how this extends far beyond their economic value associated with mainstream agriculture and forestry. Seeds represent the main assets for nature-based solutions at species (i.e., unlocking neglected species properties and via seed banking) and ecosystem level (i.e., ecological restoration). Challenges remain to enhance their sustainable use in nature conservation and in supporting a sustainable development model. Such advances will depend on the comprehensive valuation of the natural capital value of seeds, which has so far been grossly underestimated.

Potential Distribution of Cedrela odorata L. in Mexico according to Its Optimal Thermal Range for Seed Germination under Different Climate Change Scenarios.

Cedrela odorata is a native tree of economic importance, as its wood is highly demanded in the international market. In this work, the current and future distributions of C. odorata in Mexico under climate change scenarios were analyzed according to their optimal temperature ranges for seed germination. For the present distribution, 256 localities of the species' presence were obtained from the Global Biodiversity Information Facility (GBIF) database and modelled with MaxEnt. For the potential distribution, the National Center for Atmospheric Research model (CCSM4) was used under conservative and drastic scenarios (RCP2.6 and RCP8.5 Watts/m2, respectively) for the intermediate future (2050) and far future (2070). Potential distribution models were built from occurrence data within the optimum germination temperature range of the species. The potential distribution expanded by 5 and 7.8% in the intermediate and far future, respectively, compared with the current distribution. With the increase in temperature, adequate environmental conditions for the species distribution should be met in the central Mexican state of Guanajuato. The states of Chihuahua, Mexico, Morelos, Guerrero, and Durango presented a negative trend in potential distribution. Additionally, in the far future, the state of Chihuahua it is likely to not have adequate conditions for the presence of the species. For the prediction of the models, the precipitation variable during the driest month presented the greatest contribution. When the humidity is not limiting, the thermal climatic variables are the most important ones. Models based on its thermal niche for seed germination allowed for the identification of areas where temperature will positively affect seed germination, which will help maximize the establishment of plant populations and adaptation to different climate change scenarios.

Thermal Niche for Seed Germination and Species Distribution Modelling of Swietenia macrophylla King (Mahogany) under Climate Change Scenarios.

Swietenia macrophylla is an economically important tree species propagated by seeds that lose their viability in a short time, making seed germination a key stage for the species recruitment. The objective of this study was to determine the cardinal temperatures and thermal time for seed germination of S. macrophylla; and its potential distribution under different climate change scenarios. Seeds were placed in germination chambers at constant temperatures from 5 to 45 °C and their thermal responses modelled using a thermal time approach. In addition, the potential biogeographic distribution was projected according to the Community Climate System Model version 4 (CCSM4). Germination rate reached its maximum at 37.3 ± 1.3 °C (To); seed germination decreased to near zero at 52.7 ± 2.2 °C (ceiling temperature, Tc) and at 12.8 ± 2.4 °C (base temperature, Tb). The suboptimal thermal time θ150 needed for 50% germination was ca. 190 °Cd, which in the current scenario is accumulated in 20 days. The CCSM4 model estimates an increase of the potential distribution of the species of 12.3 to 18.3% compared to the current scenario. The temperature had an important effect on the physiological processes of the seeds. With the increase in temperature, the thermal needs for germination are completed in less time, so the species will not be affected in its distribution. Although the distribution of the species may not be affected, it is crucial to generate sustainable management strategies to ensure its long-term conservation.

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.

Functional seed traits and germination patterns predict species coexistence in Northeast Mediterranean foredune communities.

BACKGROUND AND AIMS: The structure of plant communities, which is based on species abundance ratios, is closely linked to ecosystem functionality. Seed germination niche plays a major role in shaping plant communities, although it has often been neglected when explaining species coexistence. The aim of this work is to link the seed germination niche to community ecology, investigating how functional seed traits contribute to species coexistence. METHODS: Species selection was based on a database of 504 vegetation surveys from the Veneto coast (Italy). Through cluster analysis we identified the foredune community and selected all of its 19 plant species. By using the 'Phi coefficient' and frequency values, species were pooled in different categories (foundation species, accidental species of the semi-fixed dune and aliens), then the 19 species were grouped according to their germination responses to temperature and photoperiod through cluster analyses. For each germination cluster, we investigated germination trends against temperature and photoperiod by using generalized linear mixed models. KEY RESULTS: We identified four germination strategies: (1) high germination under all tested conditions ('high-germinating'); (2) high germination at warm temperatures in the dark ('dark warm-cued'); (3) high germination at warm temperatures in the light ('light warm-cued'); and (4) low germination, regardless of conditions ('low-germinating'). Foredune foundation species showed a narrow germination niche, being 'low-germinating' or 'dark warm-cued'. Annual species of semi-fixed dunes were 'high-germinating', while alien species were the only members of the 'light warm-cued' cluster. CONCLUSIONS: Our research suggests that different categories of species have dissimilar seed germination niches, which contributes to explaining their coexistence. Climatic events, such as rising temperature, could alter germination patterns, favouring seed regeneration of certain categories (i.e. alien and semi-fixed dune species) at the expense of others (i.e. foundation species, pivotal to ecosystem functioning), and hence potentially altering the plant community structure.

Native trees of Mexico: diversity, distribution, uses and conservation.

BACKGROUND: Mexico is one of the most floristically rich countries in the world. Despite significant contributions made on the understanding of its unique flora, the knowledge on its diversity, geographic distribution and human uses, is still largely fragmented. Unfortunately, deforestation is heavily impacting this country and native tree species are under threat. The loss of trees has a direct impact on vital ecosystem services, affecting the natural capital of Mexico and people's livelihoods. Given the importance of trees in Mexico for many aspects of human well-being, it is critical to have a more complete understanding of their diversity, distribution, traditional uses and conservation status. We aimed to produce the most comprehensive database and catalogue on native trees of Mexico by filling those gaps, to support their in situ and ex situ conservation, promote their sustainable use, and inform reforestation and livelihoods programmes. METHODS: A database with all the tree species reported for Mexico was prepared by compiling information from herbaria and reviewing the available floras. Species names were reconciled and various specialised sources were used to extract additional species information, i.e. endemic status, threat status, availability in seed collections, reports on plant uses and conservation actions currently in place. With this information, a comprehensive catalogue of native trees from Mexico was redacted. Available georeferenced records were used to map each species distribution and perform spatial analyses to identify gaps of information and priority areas for their conservation and exploration. RESULTS: Mexico has at least 2,885 native tree species, belonging to 612 genera and 128 families. Fabaceae is the most represented family and Quercus the most represented genus. Approximately 44% of tree species are endemic to the country. The southern part of the country showed the highest values of species richness. Six hundred and seventy-four species have at least one documented human use. In terms of conservation assessment, ca. 33% of species have been assessed by either the IUCN Red List (919) or the National protection catalogue "NORMA Oficial Mexicana NOM-059" (29) or both (45). Additionally, 98 species have been included in the CITES listing for protection. In terms of existing conservation efforts, 19% of species have ex situ protection in seed banks, while protected areas overlap with all the identified peaks of species richness, except for those in the states of Veracruz and Chiapas. This work constitutes a key milestone for the knowledge, management, and conservation of the Mexican native trees. The two areas with high density of tree species identified in Veracruz and Chiapas represent two priority areas for tree conservation in Mexico, where integrated in situ and ex situ conservation efforts should be focused.

Born to Eat Wild: An Integrated Conservation Approach to Secure Wild Food Plants for Food Security and Nutrition.

Overlooked in national reports and in conservation programs, wild food plants (WFPs) have been a vital component of food and nutrition security for centuries. Recently, several countries have reported on the widespread and regular consumption of WFPs, particularly by rural and indigenous communities but also in urban contexts. They are reported as critical for livelihood resilience and for providing essential micronutrients to people enduring food shortages or other emergency situations. However, threats derived from changes in land use and climate, overexploitation and urbanization are reducing the availability of these biological resources in the wild and contributing to the loss of traditional knowledge associated with their use. Meanwhile, few policy measures are in place explicitly targeting their conservation and sustainable use. This can be partially attributed to a lack of scientific evidence and awareness among policymakers and relevant stakeholders of the untapped potential of WFPs, accompanied by market and non-market barriers limiting their use. This paper reviews recent efforts being undertaken in several countries to build evidence of the importance of WFPs, while providing examples of cross-sectoral cooperation and multi-stakeholder approaches that are contributing to advance their conservation and sustainable use. An integrated conservation approach is proposed contributing to secure their availability for future generations.

Differential Interpretation of Mountain Temperatures by Endospermic Seeds of Three Endemic Species Impacts the Timing of In Situ Germination.

Predicting seed germination in the field is a critical part of anticipating the impact of climate change on the timing of wild species regeneration. We combined thermal time and soil heat sum models of seed germination for three endemic Mediterranean mountain species with endospermic seeds and morphophysiological dormancy: Aquilegia barbaricina, Paeonia corsica, and Ribes sandalioticum. Seeds were buried in the soil within the respective collection sites, both underneath and outside the tree canopy, and their growth was assessed regularly and related to soil temperatures and estimates of the thermal characteristics of the seeds. The thermal thresholds for embryo growth and seed germination of A. barbaricina assessed in previous studies under controlled conditions were used to calculate soil heat sum accumulation of this species in the field. Thermal thresholds of seed germination for P. corsica and R. sandalioticum were not previously known and were estimated for the first time in this field study, based on findings of previous works carried out under controlled conditions. Critical embryo length and maximum germination for A. barbaricina were reached in April, and in December for R. sandalioticum. Seeds of P. corsica stay dormant in the ground until the following summer, and the critical embryo length and highest germination were detected from September to December. Soil heat sum models predicted earlier germination by one month for all three species under two Intergovernmental Panel on Climate Change (IPCC) scenarios, based on the assumption that the estimated thermal thresholds will remain constant through climate changes. This phenological shift may increase the risk of mortality for young seedlings. The models developed provide important means of connecting the micro-environmental niche for in situ seed germination and the macro-environmental parameters under a global warming scenario.

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.

Effects of pre-treatments and temperature on seed viability and germination of Juniperus macrocarpa Sm.

The effects of collecting season, collection site, laboratory pre-treatments and temperatures on seed viability and germination of Juniperus macrocarpa were investigated. Ripe cones were collected in four Sardinian dune systems, in two seasons, from plant and soil. Warm (W) and cold (C) stratifications, two combinations of them (W+C, C+W), and no pre-treatment (0) were applied. Seeds were incubated in a range of constant (10-25°C) and an alternating (25/10°C) temperature regime. Seed viability was low (ca. 40%) and varied significantly according to the collecting season. Seed germination was also low (ca. 10%), the 0 and W were the most effective pre-treatments on stimulating germination. The best germination temperature, without any pre-treatment, was 15°C (ca. 20%). J. macrocarpa seeds are dormant and the achieved results suggested that the presence of secondary dormancy is induced by cold stratification. Spring appeared to be the best season for seed collecting, whereas autumn was the best for sowing. These results give new findings for restoration activities on this species.

Thermal niche for in situ seed germination by Mediterranean mountain streams: model prediction and validation for Rhamnus persicifolia seeds.

BACKGROUND AND AIMS: Mediterranean mountain species face exacting ecological conditions of rainy, cold winters and arid, hot summers, which affect seed germination phenology. In this study, a soil heat sum model was used to predict field emergence of Rhamnus persicifolia, an endemic tree species living at the edge of mountain streams of central eastern Sardinia. METHODS: Seeds were incubated in the light at a range of temperatures (10-25 and 25/10 °C) after different periods (up to 3 months) of cold stratification at 5 °C. Base temperatures (Tb), and thermal times for 50 % germination (θ50) were calculated. Seeds were also buried in the soil in two natural populations (Rio Correboi and Rio Olai), both underneath and outside the tree canopy, and exhumed at regular intervals. Soil temperatures were recorded using data loggers and soil heat sum (°Cd) was calculated on the basis of the estimated Tb and soil temperatures. KEY RESULTS: Cold stratification released physiological dormancy (PD), increasing final germination and widening the range of germination temperatures, indicative of a Type 2 non-deep PD. Tb was reduced from 10·5 °C for non-stratified seeds to 2·7 °C for seeds cold stratified for 3 months. The best thermal time model was obtained by fitting probit germination against log °Cd. θ50 was 2·6 log °Cd for untreated seeds and 2·17-2·19 log °Cd for stratified seeds. When θ50 values were integrated with soil heat sum estimates, field emergence was predicted from March to April and confirmed through field observations. CONCLUSIONS: Tb and θ50 values facilitated model development of the thermal niche for in situ germination of R. persicifolia. These experimental approaches may be applied to model the natural regeneration patterns of other species growing on Mediterranean mountain waterways and of physiologically dormant species, with overwintering cold stratification requirement and spring germination.

Geographic isolation affects inter- and intra-specific seed variability in the Astragalus tragacantha complex, as assessed by morpho-colorimetric analysis.

The effect of geographical isolation on the inter- and intra-specific seed variability of the Astragalus tragacantha complex was investigated by using a computer-aided imaging system. In particular, seed morphometric and colorimetric features of Astragalus balearicus, A. tegulensis, A. terraccianoi, A. thermensis and A. tragacantha were measured and the data were used to discriminate among regions of provenance, taxa and populations. Discriminant analysis of the data supports the accepted taxonomy of the group and the hypothesis that interspecific differentiation resulted from geographical isolation. The results also showed a positive correlation between the wideness of species' distribution and the levels of seed intra-specific variability.

Thermal thresholds as predictors of seed dormancy release and germination timing: altitude-related risks from climate warming for the wild grapevine Vitis vinifera subsp. sylvestris.

BACKGROUND AND AIMS: The importance of thermal thresholds for predicting seed dormancy release and germination timing under the present climate conditions and simulated climate change scenarios was investigated. In particular, Vitis vinifera subsp. sylvestris was investigated in four Sardinian populations over the full altitudinal range of the species (from approx. 100 to 800 m a.s.l). METHODS: Dried and fresh seeds from each population were incubated in the light at a range of temperatures (10-25 and 25/10 °C), without any pre-treatment and after a warm (3 months at 25 °C) or a cold (3 months at 5 °C) stratification. A thermal time approach was then applied to the germination results for dried seeds and the seed responses were modelled according to the present climate conditions and two simulated scenarios of the Intergovernmental Panel on Climate Change (IPCC): B1 (+1·8 °C) and A2 (+3·4 °C). KEY RESULTS: Cold stratification released physiological dormancy, while very few seeds germinated without treatments or after warm stratification. Fresh, cold-stratified seeds germinated significantly better (>80 %) at temperatures ≥20 °C than at lower temperatures. A base temperature for germination (T(b)) of 9·0-11·3 °C and a thermal time requirement for 50 % of germination (θ(50)) ranging from 33·6 °Cd to 68·6 °Cd were identified for non-dormant cold-stratified seeds, depending on the populations. This complex combination of thermal requirements for dormancy release and germination allowed prediction of field emergence from March to May under the present climatic conditions for the investigated populations. CONCLUSIONS: The thermal thresholds for seed germination identified in this study (T(b) and θ(50)) explained the differences in seed germination detected among populations. Under the two simulated IPCC scenarios, an altitude-related risk from climate warming is identified, with lowland populations being more threatened due to a compromised seed dormancy release and a narrowed seed germination window.

Seed germination responses to varying environmental conditions and provenances in Crucianella maritima L., a threatened coastal species.

Seed germination (effects of light, temperature, NaCl and KNO(3)) of the coastal endangered species Crucianella maritima was investigated by testing seeds from three different populations. Data were analyzed by means of Generalized Linear Mixed Model (GLMM). The principal results showed that germination of C. maritima seeds was characterized by photoinhibition, absence of primary dormancy and salt-induced secondary dormancy, with no need for high nutrient availability (KNO(3)). Intraspecific differences in germination pattern emerged, apparently due to a different seed mass. These results show important germination traits of C. maritima which should be taken into account in possible reintroduction attempts aimed at restoring threatened populations of this species.