Best practices, errors, and perspectives of half a century of plant translocation in Italy.

Conservation translocations are becoming common conservation practice, so there is an increasing need to understand the drivers of plant translocation performance through reviews of cases at global and regional levels. The establishment of the Italian Database of Plant Translocation (IDPlanT) provides the opportunity to review the techniques used in 186 plant translocation cases performed in the last 50 years in the heart of the Mediterranean Biodiversity Hotspot. We described techniques and information available in IDPlanT and used these data to identify drivers of translocation outcomes. We tested the effect of 15 variables on survival of translocated propagules as of the last monitoring date with binomial logistic mixed-effect models. Eleven variables significantly affected survival of transplants: life form, site protection, material source, number of source populations, propagation methods, propagule life stage, planting methods, habitat suitability assessment, site preparation, aftercare, and costs. The integration of vegetation studies in the selection of suitable planting sites significantly increased the success of translocation efforts. Although posttranslocation watering had a generally positive effect on translocation outcome, other aftercare techniques did not always increase transplant survival. Finally, we found that how funds were spent appeared to be more important than the actual amount spent. Plant translocations in Italy and in the Mediterranean area should account for the complexity of speciation, gene flow, and plant migrations that has led to local adaptations and has important implications for the choice and constitution of source material.

Mejores prácticas, errores y perspectivas tras medio siglo de reubicaciones botánicas en Italia Resumen Las reubicaciones son una práctica cada vez más común en la conservación, por lo que hay una necesidad creciente por entender los factores del desempeño de las reubicaciones botánicas por medio de la revisión de casos regionales y globales. La creación de la Italian Database of Plant Translocation (IDPlanT) proporciona una oportunidad para revisar las técnicas usadas para los casos de reubicación de 186 plantas realizados durante los últimos cincuenta años en el centro del punto caliente de biodiversidad mediterránea. Describimos las técnicas y la información disponible en IDPlanT y usamos estos datos para identificar los factores involucrados en los resultados de las reubicaciones. Usamos modelos logísticos binomiales de efectos mixtos para analizar el efecto de 15 variables sobre la supervivencia de los propágulos reubicados a partir de la última fecha de monitoreo. Once de las variables afectaron de manera significativa la supervivencia de las plantas: forma de vida, protección del sitio, fuente de materiales, cantidad de poblaciones originarias, método de propagación, etapa de vida del propágulo, método de siembra, evaluación de idoneidad del hábitat, preparación del sitio, cuidados posteriores y costos. La integración de los estudios botánicos a la selección de los sitios idóneos para plantar aumentó el éxito de los esfuerzos de reubicación. Aunque el riego posterior a la reubicación tuvo un efecto positivo general sobre el resultado, las otras técnicas de cuidado posterior no siempre incrementaron la supervivencia de la planta reubicada. Por último, descubrimos que parece ser más importante cómo se utilizan los fondos que la cantidad actual empleada. Las reubicaciones botánicas en Italia y en el área del Mediterráneo deben considerar lo complejo de la especiación, el flujo génico y la migración botánica que han derivado en adaptaciones locales y que han tenido implicaciones importantes para la elección y constitución del material de origen.

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.

Karyotypic diversity: a neglected trait to explain angiosperm diversification?

Evolutionary changes in karyotype provide genetic support to organisms' differentiation and adaptation; however, the association between karyotype diversity and species diversification in flowering plants (angiosperms) remains to be fully elucidated. We sought evidence for this association within a phylogenetic framework using a dataset comprising > 413,000 worldwide chromosome counts of 66,000 angiosperms species. Karyotypic diversity (e.g., number of distinct chromosome numbers) explains species richness and diversification rates at both family and genus levels highlighting that chromosome evolution has probably played, at least, an important role in reinforcing speciation that was already initiated or completed by other geographical or ecological drivers. Thus, research programs investigating chromosome variation as a direct or indirect driver of diversification should be encouraged.

Selecting the best candidates for resurrecting extinct-in-the-wild plants from herbaria.

Resurrecting extinct species is a fascinating and challenging idea for scientists and the general public. Whereas some theoretical progress has been made for animals, the resurrection of extinct plants (de-extinction sensu lato) is a relatively recently discussed topic. In this context, the term 'de-extinction' is used sensu lato to refer to the resurrection of 'extinct in the wild' species from seeds or tissues preserved in herbaria, as we acknowledge the current impossibility of knowing a priori whether a herbarium seed is alive and can germinate. In plants, this could be achieved by germinating or in vitro tissue-culturing old diaspores such as seeds or spores available in herbarium specimens. This paper reports the first list of plant de-extinction candidates based on the actual availability of seeds in herbarium specimens of globally extinct plants. We reviewed globally extinct seed plants using online resources and additional literature on national red lists, resulting in a list of 361 extinct taxa. We then proposed a method of prioritizing candidates for seed-plant de-extinction from diaspores found in herbarium specimens and complemented this with a phylogenetic approach to identify species that may maximize evolutionarily distinct features. Finally, combining data on seed storage behaviour and longevity, as well as specimen age in the novel 'best de-extinction candidate' score (DEXSCO), we identified 556 herbarium specimens belonging to 161 extinct species with available seeds. We expect that this list of de-extinction candidates and the novel approach to rank them will boost research efforts towards the first-ever plant de-extinction.

Long-term seed burial reveals differences in the seed-banking strategies of naturalized and invasive alien herbs.

Soil seed viability and germinability dynamics can have a major influence on the establishment and spread of plants introduced beyond their native distribution range. Yet, we lack information on how temporal variability in these traits could affect the invasion process. To address this issue, we conducted an 8-year seed burial experiment examining seed viability and germinability dynamics for 21 invasive and 38 naturalized herbs in the Czech Republic. Seeds of most naturalized and invasive species persisted in the soil for several years. However, naturalized herbs exhibited greater seed longevity, on average, than invasive ones. Phylogenetic logistic models showed that seed viability (but not germinability) dynamics were significantly related to the invasion status of the study species. Seed viability declined earlier and more sharply in invasive species, and the probability of finding viable seeds of invasive species by the end of the experiment was low. Our findings suggest that invasive herbs might take advantage of high seed viability in the years immediately after dispersal, while naturalized species benefit from extended seed viability over time. These differences, however, are not sufficiently strong to explain the invasiveness of the species examined.

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.

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.

A global phylogenetic regionalization of vascular plants reveals a deep split between Gondwanan and Laurasian biotas.

Existing global regionalization schemes for plants consider the compositional affinities among biotas, but these have not explicitly considered phylogenetic information. Here, we present for the first time, a phytogeographical delineation of the global vascular flora based on species-level evolutionary relationships. We analysed 8737 820 geographical occurrence records for vascular plants together with a time-calibrated phylogeny including 67 269 species. We constructed a global phylogenetic regionalization by estimating species composition and phylogenetic beta diversity among 200 km × 200 km grid cells across the world. We identified de novo 16 phytogeographical units that are deeply split into two clusters: Laurasian and Gondwanan. Our regionalization broadly matches previous schemes, but also highlights the separation of the Gondwanan biota into an Holotropical cluster and an Australian-Neozealandic-Patagonian cluster. In contrast, no clear split among Laurasian and Gondwanan biotas was retrieved when omitting phylogenetic information. The integration of phylogenetic and geographical information provides new insights into the delineation of phytogeographical areas and their historical relationships, enabling the identification of three large, clearly differentiated biotas, here referred to as kingdoms: Holarctic, Holotropical, and Austral. Our results provide further evidence for delineating transition zones and show a clear latitudinal pattern of increasing evolutionary distinctiveness towards the poles.

Persistent soil seed banks promote naturalisation and invasiveness in flowering plants.

With globalisation facilitating the movement of plants and seeds beyond the native range, preventing potentially harmful introductions requires knowledge of what drives the successful establishment and spread of alien plants. Here, we examined global-scale relationships between naturalisation success (incidence and extent) and invasiveness, soil seed bank properties (type and densities) and key species traits (seed mass, seed dormancy and life form) for 2350 species of angiosperms. Naturalisation and invasiveness were strongly associated with the ability to form persistent (vs. transient) seed banks but relatively weakly with seed bank densities and other traits. Our findings suggest that seed bank persistence is a trait that better captures the ability to become naturalised and invasive compared to seed traits more widely available in trait databases. Knowledge of seed persistence can contribute to our ability to predict global naturalisation and invasiveness and to identify potentially invasive flowering plants before they are introduced.

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.

A deep dive into the ancestral chromosome number and genome size of flowering plants.

Chromosome number and genome variation in flowering plants have stimulated growing speculation about the ancestral chromosome number of angiosperms, but estimates so far remain equivocal. We used a probabilistic approach to model haploid chromosome number (n) changes along a phylogeny embracing more than 10 000 taxa, to reconstruct the ancestral chromosome number of the common ancestor of extant angiosperms and the most recent common ancestor for single angiosperm families. Independently, we carried out an analysis of 1C genome size evolution, including over 5000 taxa. Our analyses revealed an ancestral haploid chromosome number for angiosperms of n = 7, a diploid status, and an ancestral 1C of 1.73 pg. For 160 families, inferred ancestral n are provided for the first time. Both descending dysploidy and polyploidy played crucial roles in chromosome number evolution. While descending dysploidy is equally distributed early and late across the phylogeny, polyploidy is detected mainly towards the tips. Similarly, 1C genome size also increases (or decreases) significantly in late-branching lineages. Therefore, no evidence exists of a clear link between ancestral chromosome numbers and ancient polyploidization events, suggesting that further insights are needed to elucidate the organization of genome packaging into chromosomes.

Phylogenetically informed spatial planning as a tool to prioritise areas for threatened plant conservation within a Mediterranean biodiversity hotspot.

Global plant diversity is at risk due to anthropogenic changes to ecosystems, but given severely limited conservation resources, a reliable prioritisation strategy for species and sites is needed. Our objective was to identify key areas for conserving the phylogenetic diversity (PD) of threatened vascular plants in Italy, one of the most species-rich regions in the Mediterranean Basin. We used spatial data and the conservation status of 995 threatened vascular plants and applied a phylogenetically informed spatial planning to minimize conservation costs. We then determined the degree of overlap with existing protected areas and evaluated whether this PD-based prioritisation of areas provides adequate protection for threatened phylogenetically distinctive species (EDGE). The cost-effective procedure identified as priority for conservation 12% of the study territory, while achieving over 90% of conservation targets (total PD). We showed that priority areas and protected areas are moderately spatially mismatched. We also showed that not all top-EDGE species were met by the procedure applied, hence we conclude that the PD-based model indicated key areas for protection, but nevertheless additional attention is needed to protect top-EDGE species. This study represents one of the most comprehensive analyses, to date, for the conservation of the native flora in the Mediterranean, incorporating both spatial distribution and evolutionary relationships. Our work on the prioritisation of threatened plant species across Italy can serve as a guide for future conservation applications.

Unscrambling phylogenetic effects and ecological determinants of chromosome number in major angiosperm clades.

As variations in the chromosome number are recognized to be of evolutionary interest but are also widely debated in the literature, we aimed to quantitatively test for possible relationships among the chromosome number, plant traits, and environmental factors. In particular, the chromosome number and drivers of its variation were examined in 801 Italian endemic vascular plants, for a total of 1364 accessions. We estimated phylogenetic inertia and adaptation in chromosome number - based on an Ornstein-Uhlenbeck process - and related chromosome numbers with other plant traits and environmental variables. Phylogenetic effects in chromosome number varied among the examined clades but were generally high. Chromosome numbers were poorly related to large scale climatic conditions, while a stronger relationship with categorical variables was found. Specifically, open, disturbed, drought-prone habitats selected for low chromosome numbers, while perennial herbs, living in shaded, stable environments were associated with high chromosome numbers. Altogether, our findings support an evolutionary role of chromosome number variation, and we argue that environmental stability favours higher recombination rates in comparison to unstable environments. In addition, by comparing the results of models testing for the evolvability of 2n and of x, we provide insight into the presumptive ecological significance of polyploidy.

Reproductive biology of the threatened Lilium pomponium (Liliaceae), a species endemic to Maritime and Ligurian Alps.

Pollination ecology and breeding system of Lilium pomponium L. were studied, and their effect on the reproductive outcome was assessed. This species has high conservation interest in Europe, because it is included in Annex V of the EU Habitat Directive and it is one out of the five Lilium species listed in IUCN Global Red List. To achieve our aim, the pollen vectors as well as the effect of bagging, emasculation and artificial pollination on reproductive output were studied. The most frequent visitor was the Lepidopteran Gonepteryx rhamnii. In general, reproductive outputs were close to zero for all the self-pollination treatments; however, geitonogamy and facilitated selfing seem slightly more efficient than autogamy, as also confirmed by self-compatibility and autofertility indices. Altogether, our results suggest a self-incompatible outcrossing breeding system, with a poor capacity for selfing. Nevertheless, climate change and anthropic threats might promote a shift toward self-fertilization, even maladaptive, favouring the few individuals able to produce selfed seeds.

Photophobia in Lilioid monocots: photoinhibition of seed germination explained by seed traits, habitat adaptation and phylogenetic inertia.

Background and Aims: Photoinhibition of seed germination, known to occur notably in species growing in dry and hot habitats, is considered an adaptation to avoid germination at the soil surface after unpredictable rainfall events during the dry season. Hence, the association of this ecophysiological response with plant life histories and the natural environment was investigated in Lilioid monocots, a group of plants where photoinhibition has been pre-eminently observed. Methods: A data set including germination in light and darkness of about 150 monocots was compiled. Habitat preference, local climate conditions, seed traits and temperature conditions used during germination experiments were retrieved. Factors driving the evolution of photoinhibition were analysed within a phylogenetic framework. Key Results: Significant phylogenetic signal was found in germination response (λ between 0.76 and 0.80) and photoinhibition (D = 0.406). Photoinhibition was mainly related to plant traits, namely seed coat colour, seed mass and plant height. A relationship with habitat light and moisture was also evident, but the association with climate as well as temperature conditions during incubation was rather poor. Conclusions: Whilst photoinhibition is prevalent in open habitats, the relationship with habitat moisture conditions and hot and dry climate is weak. Indeed, photoinhibition is also commonly observed in temperate and alpine climate geophytes growing in habitats that are much less susceptible to drought. Hence, phylogenetic inertia, probably mediated by seed morphological traits such as seed coat colour, may explain why temperate climate species have retained photoinhibition inherited from their Mediterranean ancestors.

Plant regeneration from seeds responds to phylogenetic relatedness and local adaptation in Mediterranean Romulea (Iridaceae) species.

Seed germination is the most important transitional event between early stages in the life cycle of spermatophytes and understanding it is crucial to understand plant adaptation and evolution. However, so far seed germination of phylogenetically closely related species has been poorly investigated. To test the hypothises that phylogenetically related plant species have similar seed ecophysiological traits thereby reflecting certain habitat conditions as a result of local adaptation, we studied seed dormancy and germination in seven Mediterranean species in the genus Romulea (Iridaceae). Both the across-species model and the model accounting for shared evolutionary history showed that cool temperatures (≤ 15°C) were the main factor that promoted seed germination. The absence of embryo growth before radicle emergence is consistent with a prompt germination response at cool temperatures. The range of temperature conditions for germination became wider after a period of warm stratification, denoting a weak primary dormancy. Altogether these results indicate that the studied species exhibit a Mediterranean germination syndrome, but with species-specific germination requirements clustered in a way that follows the phylogenetic relatedness among those species. In addition, species with heavier seeds from humid habitats showed a wider range of conditions for germination at dispersal time than species from dry habitats possessing lighter seeds. We conclude that while phylogenetically related species showed very similar germination requirements, there are subtle ecologically meaningful differences, confirming the onset of adaptation to local ecological factors mediated by species relatedness.

Testing the large genome constraint hypothesis: plant traits, habitat and climate seasonality in Liliaceae.

The factors driving genome size evolution in Liliaceae were examined. In particular, we investigated whether species with larger genomes are confined to less stressful environments with a longer vegetative season. We tested our hypotheses by correlating the genome size with other plant traits and environmental variables. To determine the adaptive nature of the genome size, we also compared the performances of Brownian motion (BM) processes with those inferred by Ornstein-Uhlenbeck (OU) models of trait evolution. A positive correlation of genome size with plant size, mean temperature and habitat moisture and a negative correlation with altitude and precipitation seasonality were found. Models of trait evolution revealed a deviation from a drift process or BM. Instead, changes in genome size were significantly associated with precipitation regimes according to an OU process. Specifically, the evolutionary optima towards which the genome size evolves were higher for humid climates and lower for drier ones. Taken together, our results indicate that the genome size increase in Liliaceae is constrained by climate seasonality.

Flower bouquet variation in four species of Crocus ser. Verni.

Flowering plants employ a wide variety of signals, including scent, to attract pollinators. The aim of this work was to examine whether flower volatiles in four closely related Crocus species are linked to species divergence and to the current knowledge on their pollination syndromes. Fragrances of freshly opened flowers in Crocus etruscus, C. ilvensis, C. neglectus, and C. vernus, all belonging to ser. Verni, were analyzed using GC/MS. Results coincide with present knowledge about systematic relationships among taxa. The four species fall into two main fragrance types, based on similarities of their volatile compounds. In C. etruscus, C. ilvensis, and C. neglectus, oxygenated monoterpenes (lilac aldehyde B and A) are most abundant, while C. vernus has a fragrance rich in monoterpene hydrocarbons (α-pinene and limonene). Our results point towards outcrossing mating strategies for C. etruscus, C. ilvensis, and C. neglectus, whose volatile compounds are known as pollinator attractants. This is in line with their flower architecture, showing a style of variable height, often overtopping stamens. On the other hand, a self-pollination strategy was repeatedly suggested in the literature for C. vernus, marked by flowers with the style deeply inserted in the stamens and also by a completely different flower bouquet.