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.

Extinct in the wild: The precarious state of Earth's most threatened group of species.

Extinct in the Wild (EW) species are placed at the highest risk of extinction under the International Union for Conservation of Nature Red List, but the extent and variation in this risk have never been evaluated. Harnessing global databases of ex situ animal and plant holdings, we report on the perilous state of EW species. Most EW animal species-already compromised by their small number of founders-are maintained at population sizes far below the thresholds necessary to ensure demographic security. Most EW plant species depend on live propagation by a small number of botanic gardens, with a minority secured at seed bank institutions. Both extinctions and recoveries are possible fates for EW species. We urgently call for international effort to enable the latter.

Out-of-date datasets hamper conservation of species close to extinction.

International databases and data aggregators on species conservation status are powerful tools supporting the efforts of conservation biologists and practitioners in reducing the loss of biodiversity. However, out-of-date information and poor interoperability of databases can hamper conservation of highly threatened species or in extreme cases can result in their removal from conservation frameworks. Lack of common standards for database updates, slow update timing and incongruencies among datasets in terms of taxonomy, threats, conservation status and holding prevent proper conservation prioritization and actions. A simple survey to solve incongruencies between the BGCI PlantSearch Database and the IUCN Red List resulted in a change of status of 16 plant species, including the 'rehabilitation' of 12 species thought to be extinct.

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.

Do marginal plant populations enhance the fitness of larger core units under ongoing climate change? Empirical insights from a rare carnation.

Assisted gene flow (AGF) can restore fitness in small plant populations. Due to climate change, current fitness patterns could vary in the future ecological scenario, as highly performant lineages can undergo maladaptation under the new climatic contexts. Peripheral populations have been argued to represent a potential source of species adaptation against climate change, but experimental evidence is poor. This paper considers the consequences of within- and between-population mating between a large core population and the southernmost population, the rare Dianthus guliae, to evaluate optimal AGF design under current and future conditions. We performed experimental self-pollinations and within- and between-population cross-pollinations to generate seed material and test its adaptive value to aridity. Seed germination, seedling growth and survival were measured under current and expected aridity. Effects of population type, pollination treatment and stress treatment on fitness components were analysed by generalized linear models. Relative measures of inbreeding depression and heterosis were taken under different stress treatments. Self-pollination reduced fitness for all the considered traits compared to within- and between-population cross-pollination. Under current aridity regime, the core population expressed higher fitness, and a larger magnitude of inbreeding depression. This indicated the core unit is close to its fitness optimum and could allow for restoring the fitness of the small peripheral population. Contrarily, under increased aridity, the fitness of outbred core lineages decreased, suggesting the rise of maladaptation. In this scenario, AGF from the small peripheral population enhanced the fitness of the core unit, whereas AGF from the core population promoted a fitness loss in the peripheral population. Hence, the small peripheral population could improve fitness of large core units versus climate change, while the contrary could be not true. Integrating reciprocal breeding programmes and fitness analyses under current and predicted ecological conditions can support optimal AGF design in a long-term perspective.

Seventeen 'extinct' plant species back to conservation attention in Europe.

Seventeen European endemic plant species were considered extinct, but improved taxonomic and distribution knowledge as well as ex situ collecting activities brought them out of the extinct status. These species have now been reported into a conservation framework that may promote legal protection and in situ and ex situ conservation.

Reversing extinction trends: new uses of (old) herbarium specimens to accelerate conservation action on threatened species.

Although often not collected specifically for the purposes of conservation, herbarium specimens offer sufficient information to reconstruct parameters that are needed to designate a species as 'at-risk' of extinction. While such designations should prompt quick and efficient legal action towards species recovery, such action often lags far behind and is mired in bureaucratic procedure. The increase in online digitization of natural history collections has now led to a surge in the number new studies on the uses of machine learning. These repositories of species occurrences are now equipped with advances that allow for the identification of rare species. The increase in attention devoted to estimating the scope and severity of the threats that lead to the decline of such species will increase our ability to mitigate these threats and reverse the declines, overcoming a current barrier to the recovery of many threatened plant species. Thus far, collected specimens have been used to fill gaps in systematics, range extent, and past genetic diversity. We find that they also offer material with which it is possible to foster species recovery, ecosystem restoration, and de-extinction, and these elements should be used in conjunction with machine learning and citizen science initiatives to mobilize as large a force as possible to counter current extinction trends.

Ex situ collections and their potential for the restoration of extinct plants.

The alarming current and predicted species extinction rates have galvanized conservationists in their efforts to avoid future biodiversity losses, but for species extinct in the wild, few options exist. We posed the questions, can these species be restored, and, if so, what role can ex situ plant collections (i.e., botanic gardens, germplasm banks, herbaria) play in the recovery of plant genetic diversity? We reviewed the relevant literature to assess the feasibility of recovering lost plant genetic diversity with using ex situ material and the probability of survival of subsequent translocations. Thirteen attempts to recover species extinct in the wild were found, most of which used material preserved in botanic gardens (12) and seed banks (2). One case of a locally extirpated population was recovered from herbarium material. Eight (60%) of these cases were successful or partially successful translocations of the focal species or population; the other 5 failed or it was too early to determine the outcome. Limiting factors of the use of ex situ source material for the restoration of plant genetic diversity in the wild include the scarcity of source material, low viability and reduced longevity of the material, low genetic variation, lack of evolution (especially for material stored in germplasm banks and herbaria), and socioeconomic factors. However, modern collecting practices present opportunities for plant conservation, such as improved collecting protocols and improved cultivation and storage conditions. Our findings suggest that all types of ex situ collections may contribute effectively to plant species conservation if their use is informed by a thorough understanding of the aforementioned problems. We conclude that the recovery of plant species currently classified as extinct in the wild is not 100% successful, and the possibility of successful reintroduction should not be used to justify insufficient in situ conservation.

Colecciones Ex Situ y su Potencial para la Restauración de Plantas Extintas Resumen Las alarmantes tasas de extinción actuales y pronosticadas han incitado a los conservacionistas a esforzarse para evitar las futuras pérdidas de biodiversidad, pero para las especies que ya se encuentran extintas en vida silvestre existen pocas opciones. Nos preguntamos si estas especies pueden ser restauradas, y de ser así, qué papel pueden desempeñar las colecciones ex situ de plantas (es decir, jardines botánicos, bancos de germoplasma, herbarios) en la recuperación de la diversidad genética de las plantas. Revisamos la literatura relevante para evaluar la factibilidad de la recuperación de la diversidad genética perdida y la probabilidad de supervivencia subsecuente de las reubicaciones. Encontramos 13 intentos por recuperar especies extintas en vida silvestre, la mayoría de los cuales usó material preservado en jardines botánicos (12) y en bancos de semillas (2). También hubo un caso de una población eliminada localmente que fue recuperada con material de un herbario. Ocho (60%) de estos casos fueron reubicaciones exitosas o parcialmente exitosas de la especie o población focal; los otros cinco fallaron o era demasiado pronto para poder determinar el resultado. Los factores que limitan el uso de material proveniente de colecciones ex situ para la restauración de la diversidad genética de las plantas en vida silvestre incluyen la escasez de material original, la baja viabilidad y la longevidad reducida del material, la baja variación genética, la falta de evolución (especialmente para el material almacenado en herbarios y bancos de germoplasma) y los factores socioeconómicos. A pesar de esto, las prácticas modernas de colección representan una oportunidad para la conservación de las plantas, como los protocolos mejorados de recolección y las condiciones acrecentadas de cultivo y almacenamiento. Nuestros hallazgos sugieren que todos los tipos de colecciones ex situ pueden contribuir efectivamente a la conservación de especies de plantas si su uso está respaldado por un entendimiento a fondo de los problemas antes mencionados. Concluimos que la recuperación de especies de plantas que actualmente están clasificadas como extintas en vida silvestre no es 100% exitosa y que la posibilidad de una reintroducción exitosa no debería utilizarse para justificar una conservación in situ insuficiente.

Author Correction: Ex situ seed banks and the IUCN Red List.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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.

Planning for assisted colonization of plants in a warming world.

Assisted colonization is one way of facilitating range shifts for species that are restricted in their ability to move in response to climate change. Here we conceptualize and apply a new decision framework for modelling assisted colonization of plant species prior to in situ realization. Three questions were examined: a) Is species translocation useful in a certain area? b) where, and c) how long will it be successful in the future? Applying our framework to Carex foetida in Italy at the core of its distribution and its southern edge revealed that assisted colonization could be successful in short-term (2010-2039) climate conditions, partially in medium (2040-2069) but not in long-term (2070-2099) scenarios. We show that, for some species, it is likely that assisted colonization would be successful in some portions of the recipient site under current and short-term climate conditions, but over the mid- and long-term, climate changes will make species translocation unsuccessful. The proposed decision framework can help identify species that will need different conservation actions (seed banks and/or botanical gardens) when assisted colonization is unlikely to be successful. Furthermore it has broad applicability, as it can support planning of assisted migration in mountainous areas in the face of climate change.

Effects of Autumn and Spring Heat Waves on Seed Germination of High Mountain Plants.

Alpine plants are considered to be particularly vulnerable to climate change and related extreme episodes, such as heat waves. Despite growing interest in the impact of heat waves on alpine plants, knowledge about their effects on regeneration is still fragmentary. Recruitment from seeds will be crucial for the successful migration and survival of these species and will play a key role in their future adaptation to climate change. In this study, we assessed the impacts of heat waves on the seed germination of 53 high mountain plants from the Northern Apennines (Italy). The seeds were exposed to laboratory simulations of three seasonal temperature treatments, derived from real data recorded at a meteorological station near the species growing site, which included two heat wave episodes that occurred both in spring 2003 and in autumn 2011. Moreover, to consider the effect of increasing drought conditions related to heat waves, seed germination was also investigated under four different water potentials. In the absence of heat waves, seed germination mainly occurred in spring, after seeds had experienced autumn and winter seasons. However, heat waves resulted in a significant increase of spring germination in c. 30% of the species and elicited autumn germination in 50%. When heat waves were coupled with drought, seed germination decreased in all species, but did not stop completely. Our results suggest that in the future, heat waves will affect the germination phenology of alpine plants, especially conditionally dormant and strictly cold-adapted chorotypes, by shifting the emergence time from spring to autumn and by increasing the proportion of emerged seedlings. The detrimental effects of heat waves on recruitment success is less likely to be due to the inhibition of seed germination per se, but rather due to seedling survival in seasons, and temperature and water conditions that they are not used to experiencing. Changes in the proportion and timing of emergence suggest that there may be major implications for future plant population size and structure.

Climate warming could increase recruitment success in glacier foreland plants.

BACKGROUND AND AIMS: Glacier foreland plants are highly threatened by global warming. Regeneration from seeds on deglaciated terrain will be crucial for successful migration and survival of these species, and hence a better understanding of the impacts of climate change on seedling recruitment is urgently needed to predict future plant persistence in these environments. This study presents the first field evidence of the impact of climate change on recruitment success of glacier foreland plants. METHODS: Seeds of eight foreland species were sown on a foreland site at 2500 m a.s.l., and at a site 400 m lower in altitude to simulate a 2·7 °C increase in mean annual temperature. Soil from the site of origin was used to reproduce the natural germination substrate. Recruitment success, temperature and water potential were monitored for 2 years. The response of seed germination to warming was further investigated in the laboratory. KEY RESULTS: At the glacier foreland site, seedling emergence was low (0 to approx. 40 %) and occurred in summer in all species after seeds had experienced autumn and winter seasons. However, at the warmer site there was a shift from summer to autumn emergence in two species and a significant increase of summer emergence (13-35 % higher) in all species except two. Survival and establishment was possible for 60-75 % of autumn-emerged seedlings and was generally greater under warmer conditions. Early snowmelt in spring caused the main ecological factors enhancing the recruitment success. CONCLUSIONS: The results suggest that warming will influence the recruitment of glacier foreland species primarily via the extension of the snow-free period in spring, which increases seedling establishment and results in a greater resistance to summer drought and winter extremes. The changes in recruitment success observed here imply that range shifts or changes in abundance are possible in a future warmer climate, but overall success may be dependent on interactions with shifts in other components of the plant community.

Pollinator behaviour on a food-deceptive orchid Calypso bulbosa and coflowering species.

Food deception as a pollination strategy has inspired many studies over the last few decades. Pollinator deception has evolved in many orchids possibly to enhance outcrossing. Food-deceptive orchids usually have low pollinator visitation rates as compared to rewarding species. They may benefit in visitations from the presence (magnet-species hypothesis) or, alternatively, absence of coflowering rewarding species (competition hypothesis). We present data on pollinator visitations on a deceptive, terrestrial orchid Calypso bulbosa, a species with a single flower per plant and whose flowering period partly overlaps with rewarding, early flowering willows (Salix sp.) and later-flowering bilberry (Vaccinium myrtillus). When surveying inactive bumblebee queens on willows in cool weather, about 7% of them carried Calypso pollinia. Most common bumblebee species appeared to visit and thus pollinate Calypso. Bumblebees typically visited one to three Calypso flowers before flying away, providing some support for the outcrossing hypothesis. We conclude that, regarding the pollinations strategy, both magnet-species and competition hypotheses have a role in the pollination of Calypso, but on different spatial scales. On a large scale rewarding species are important for attracting pollinators to a given region, but on a small scale absence of competition ensures sufficient pollination rate for the deceptive orchid.