Botanic garden solutions to the plant extinction crisis

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors, Plants, People, Planet © New Phytologist Trust 1Science & Conservation, The Morton Arboretum, Lisle, IL, USA 2Botanic Gardens Conservation International, Surrey, UK 3Botanic Gardens Conservation International-US, San Marino, CA, USA


| INTRODUC TI ON
The environmental movement today is focused on several major themes including climate change, deforestation, and biodiversity loss, but the specific loss of plant diversity is often overlooked, despite the fact that an estimated 80,000 (>20%) plant species are threatened with extinction (Brummitt et al., 2015). To put this in context, there are likely more threatened plant species than all described birds, mammals, reptiles, amphibians, and fishes combined (IUCN, 2020). It is well known that plant conservation receives a disproportionately small amount of funding relative to animal conservation (Havens, Kramer, & Guerrant Jr., 2014;Negrón-Ortiz, 2014;Roberson et al., 2020). Yet, plants are the framework that terrestrial ecosystems are built upon, providing critical habitat, food, and ecosystem services (Brummitt et al., 2015). The pressing environmental crises of climate change and biodiversity loss can be addressed with plant-based solutions. Conserving plant diversity ensures that we have more potential solutions in our toolkit to address future global challenges. Botanic gardens and arboreta (hereafter referred to as gardens) sit at the nexus of an unparalleled set of skills, facilities, and expertise that make them uniquely placed to save plant diversity and prevent extinctions (Cannon & Kua, 2017;Chen & Sun, 2018;Krishnan & Novy, 2016;Mounce, Smith, & Brockington, 2017;O'Donnell & Sharrock, 2017;Smith, 2018;Volis, 2017). With added capacity and funding, the garden community is poised and ready to expand its role in leading a global force to ensure plant diversity is secure and thriving in healthy ecosystems for the benefit of humans and nature.
In this article, we summarize how the role of botanic gardens in society has evolved over millennia from pleasure gardens of the elite, to reference collections for intellectuals, to plant conservation champions in the 21st Century. We then present four challenges to conserving plant diversity that gardens today are particularly well positioned to overcome, and we postulate what the future could be if gardens were sufficiently funded to tackle these challenges and reverse the plant extinction crisis we face today.

| THE E VOLUTI ON OF G ARDEN S: FROM REFEREN CE COLLEC TI ON S TO CONS ERVATION CHAMPIONS
Botanic garden concepts have existed since ancient civilizations in Egypt, Rome, Mesopotamia, India, China, and Mexico (to name a few) began cultivating medicinal plants, exotic fruit trees, and spices in royal palaces, religious sites, and private estates of the wealthy (Spencer & Cross, 2017). The early modern "physic gardens" of the 1500s in Europe, such as the walled botanic garden at the University of Padua, focused on plants with medicinal properties that were used for teaching purposes in university medical schools or monasteries. The 1500-1800s was an era of extensive botanical exploration and expansion, with new botanic gardens being established all over the world, largely as a result of European colonialism. During this period, botanic gardens were critical to the advent of the scientific fields of botany, plant taxonomy and systematics (the naming and categorization of species). While contributing greatly to the world's collective botanical knowledge, these early modern gardens, with their strong focus on economic botany, drove the global distribution of valuable plant-based commodities such as rubber, tea, coffee, cinchona, and opium, resulting in large-scale land use change (Krishnan & Novy, 2016;Spencer & Cross, 2017). Given their historical role in driving broad land use change and the commoditization of plants, it is apt that modern gardens should have a role in securing plant diversity for future human innovation, adaptation, and resilience (Smith, 2018).
According to the Botanic Gardens Conservation International (BGCI) Manual on Planning, Developing and Managing Botanic Gardens, a botanic garden today can be defined as "an institution holding documented collections of living plants for the purposes of scientific research, conservation, display and education" (Gratzfeld, 2016, p. vii; originally from Peter Wyse Jackson). Gardens today include over 3,000 institutions worldwide, employing over 60,000 botanical experts such as plant scientists, educators, and specialist horticulturists. Gardens house world-class facilities including seed banks, herbaria, greenhouses, nurseries, and research laboratories. Living plant collections still form the core of a garden and are crucial resources for taxonomy, systematics, and teaching, but today, these collections serve many additional scientific and conservation purposes. Plant collections support ex situ conservation of threatened species, provide a source of material for restoration of threatened species and degraded habitats in the wild, and are the subject of research studies investigating population genetics, climate change responses, pest and disease susceptibility, and plant adaptive capacity (Chen & Sun, 2018;Dosmann & Groover, 2012;Griffith et al., 2019). Gardens today hold at least one third of all known plant species in their collections, including over 40% of threatened species, as well as dozens of species that are extinct in the wild (Mounce et al., 2017).
Modern gardens are also a key link between people and plants.
In increasingly urbanized societies, gardens provide urban green space that may be the only access many people have to plants and nature. This exposure to nature can provide many physical, mental, and social benefits to the people of these cities (Turner-Skoff & Cavender, 2019). In addition, gardens now provide extensive education programs for everyone from preschoolers to PhD students and beyond. Public engagement is a cornerstone of garden missions; K E Y W O R D S arboretum, biodiversity hotspot, capacity building, ex situ conservation, exceptional species, in situ conservation, integrated plant conservation, landscape restoration no longer are gardens restricted in access to an elite few. Today the world's ~3,000 gardens welcome over half a billion visitors a year (based on our unpublished analysis of BGCI's GardenSearch database; https://www.bgci.org/resou rces/bgci-datab ases/garde nsear ch/), with a growing focus on expanding access, diversity, and inclusion for garden audiences, and preserving and celebrating local and indigenous plant knowledge and biocultural heritage (Gratzfeld, 2016). Gardens also interface with community groups, NGOs, industry, corporations, government agencies, universities, and other sectors to conduct research, advance conservation efforts, and build awareness for the importance of plant diversity.
Despite the long and evolving history of gardens, and the fact that the thousands of gardens currently in existence are all unique, gardens today collectively fulfill an inimitable conservation role, positioned at the intersection of plant science, living collections, horticulture, in situ conservation, and public outreach and education ( Figure 1).

| CHALLENG E S TO SAVING PL ANT D IVER S IT Y: WHERE C AN G ARDEN S HAVE THE B I G G E S T IMPAC T ?
Gardens are uniquely placed to address several challenges to conserving the world's plant diversity, if sufficient resources are allocated. Gardens are already rising to meet these challenges in innovative ways, and there are great opportunities to increase the garden community's collective plant conservation impact. In the following sections, we outline four specific challenges to conserving plant diversity, highlighting what gardens are already doing to address these challenges, and we describe what could be achieved in the future if gardens were sufficiently resourced to overcome each challenge.

| Mobilizing and coordinating plant conservation and capacity building, especially in biodiverse regions
Currently, gardens tend to engage in plant conservation projects that are locally focused, often funded for the short term through "soft money" (e.g., restricted grants), and relatively small in scale, such as conducting habitat restoration on site or nearby the garden itself (Hardwick et al., 2011;A. Meyer, unpublished data from GardenSearch and the North American Plant Conservation and Biodiversity Benchmarking tool, American Public Gardens Association, https://www.publi cgard ens.org/commu nicat ing-clima te-conse rvation). Some gardens with higher capacity (particularly in high-income economy countries) have large conservation departments and are able to deploy their tools and expertise further afield and even internationally, but that is not currently the norm in all countries. There is a great imbalance in garden conservation capacity in different regions of the world. For example, according to BGCI's GardenSearch database, two thirds of the 551 gardens that report having a plant conservation program are from high-income economy countries as defined by the World Bank (GardenSearch, 2020). Indeed, a fundamental challenge that must be overcome is that the majority of the world's botanic gardens are https://www.cepf.net/our-work/biodi versi ty-hotsp ots/hotsp otsdefined). Unfortunately, it is these regions holding the majority of the world's plant diversity (including the most undescribed species) that have low capacity for conservation and need the most support (Heywood, 2017;Joppa, Roberts, Myers, & Pimm, 2011).
In order to address a challenge at the scale of the global plant extinction crisis, garden-led conservation efforts must be massively scaled up and coordinated across institutions, sectors (government agencies, universities, NGOs, etc.), geographies, and political boundaries. Furthermore, botanical capacity must be channeled to support existing gardens and create new gardens in biodiversity hotspots F I G U R E 1 Gardens fulfill a unique conservation role, positioned at the intersection of plant science, living collections, horticultural expertise, in situ conservation, and public outreach and education F I G U R E 2 Two thirds of the world's 3,000+ gardens are located outside the world's 36 defined biodiversity hotspots. Map credit: Julie Ho, The Huntington Library, Art Collection, and Botanical Gardens, and BGCI-US (2019) and low-income economy countries of greatest conservation priority. Successful mobilization and coordination of plant conservation efforts requires robust, active networks led by trusted, inclusive organizations, to share best practices and meet standards, aggregate information to inform and prioritize action, and scale up initiatives and mobilize expertise when and where it is needed most. Successful models for this within the garden community already exist and with greater financial support significant conservation outcomes can be achieved, especially in the most biodiverse regions.
As an example, BGCI (bgci.org), the world's largest plant conservation network, promotes a rational, cost-effective 'Global System' for the conservation of all threatened plant diversity (Smith, 2016).
This models the United Nations Food and Agriculture Organization  Table 1). BGCI also establishes and coordinates regional garden networks in priority plant diversity areas including Southeast Asia, Africa, and South America. Action is further supported through BGCI's directories of expertise, extensive plant conservation training programs, and targeted financial support (e.g., the Global Botanic Garden Fund), which all prioritize conservation capacity building for gardens in biodiversity hotspots.
ArbNet (arbnet.org), the interactive network of arboreta, is another support structure for tree-focused gardens around the world.
ArbNet works to catalyze the establishment of new arboreta, sets standards and best practices among the global arboretum community, offers funding and international arboretum partnership opportunities, provides professional training, and offers an arboretum accreditation program (Westwood, 2015). ArbNet's global database of over 2,000 tree-focused gardens (the Morton Register of Arboreta) and online resource library complement BGCI's databases, fostering collaboration and growth among the global arboretum community (Table 1). In addition to these global networks dedicated to supporting gardens, there are also many regional or national garden networks which could deliver greatly increased plant conservation outcomes with additional funding. Australia, China, France, Indonesia, Japan, Mexico, South Africa, and the U.S. are some of the countries with robust national garden networks that support and coordinate plant conservation efforts among their members.
There are also many conservation-focused collaborative initiatives led by gardens which involve mobilizing expertise, focusing efforts, and/or providing funding for specific plant conservation activities. For example, the Center for Plant Conservation's National Collection of Endangered Plants preserves more than 1,600 of the TA B L E 1 Examples of garden-led or garden-focused databases that aggregate, standardize, and disseminate data in support of global plant biodiversity and conservation. Each supports one or more of the targets of the Global Strategy for Plant Conservation (GSPC)  (Smith, 2015).

| Quantifying the scope of the plant extinction crisis
The world is entering a sixth mass extinction, which is driven by human activity. We are losing plant species before they have even been described, and much faster than the average background rate  (Sharrock, 2012). This shortfall is not due to a lack of skills or commitment, but a lack of funding. Many of the rarest plants, especially those in the least developed countries and biodiversity hotspots, will either be not evaluated or deemed "Data Deficient" because of a lack of information on species distributions, population decline rates, and threats. Yet, these are the species that will most likely be on the verge of extinction (Joppa et al., 2011;Pimm & Joppa, 2015). In some cases, the data are in fact available, but there are simply not enough people working on the global threat assessment effort to evaluate every plant species. Another reason these efforts are likely to fall short of their goal is the sheer scale of the task: there are around 380,000 validly named plant species on Earth, with an estimated 70,000 more yet to be formally described F I G U R E 3 Progress (as of March, 2020) on the Global Tree Assessment, an ambitious, garden-led initiative to evaluate by 2020 all ~60,000 of the world's tree species for their risk of extinction (Pimm & Joppa, 2015;Raven, 2020

| Conserving "exceptional species" to preserve genetic diversity
To conserve plant diversity and prevent species extinctions, it is widely accepted that an integrated approach that leverages in situ and ex situ conservation approaches is the best strategy (Oldfield and Newton, 2012;Heywood, 2017;Volis, 2017   • Growing >16,000 tree species in garden collections • Establishing best practices and guidance for collecting, propagating, and planting trees • Conducting and publishing cutting-edge applied tree science • Engaging in local and regional landscape restoration and reforestation initiatives Successful models/programs • Ecological Restoration Alliance of Botanic Gardens • Plant Conservation Alliance National Seed Strategy (U.S.) • More informed, resilient, and productive landscape restoration efforts across the globe, successfully sequestering carbon and supporting biodiversity • Initiatives reach critical regions and ecosystems in need of restoration/reforestation through expanded and strengthened networks and initiatives • Gardens are engaged and a trusted voice in planning large-scale restoration and reforestation initiatives • Large-scale tree planting efforts are scientifically informed and used appropriately, effectively, and strategically to achieve climate mitigation and biodiversity objectives capacity building in biodiverse regions; (b) relies on updated threat assessments and accurate biodiversity data to inform conservation priorities, and promotes data sharing and documentation of collections; and (c) is founded on conserving exceptional plant species.
Gardens around the world are poised to replicate the GCCO model, and additional global conservation consortia are being established to focus on other priority exceptional plant groups, including cycads, magnolias, maples, and rhododendrons. But with likely tens of thousands of species falling into some level of exceptionality (i.e., unable to be conventionally seed banked), there is a great opportunity to deploy this strategy more widely, especially for tropical trees.
With increased support to individual gardens and garden networks leading these types of initiatives, the global garden community could operate a robust network of taxonomically focused conservation consortia, integrating ex situ and in situ efforts, engaging local communities, and ensuring that no threatened exceptional plant species go extinct.

| Using plant-based solutions effectively to combat biodiversity loss and climate change
Governments, corporations, and civil society are now well aware of the intertwined challenges of climate change and biodiversity loss, and the need to address these challenges. The recent Intergovernmental Panel on Climate Change (IPCC) report makes it clear that land use change is required in order to mitigate climate change and reduce global CO 2 emissions (IPCC, 2018). This will mean halting deforestation, reducing meat consumption, and planting more trees. Indeed restoration and reforestation initiatives at many scales are already underway, such as the Bonn Challenge (https:// www.bonnc halle nge.org/) to restore 350 Mha of degraded land by

2030.
As well as a climate crisis, we have a biodiversity crisis -over a million species of plants and animals face extinction due to the activities of humans (Díaz et al., 2019;IPBES, 2019). So, what will global-scale reforestation mean for biodiversity? More forests do not necessarily mean more biodiversity. In fact, the effect can be the opposite, as already seen in many tree plantations in both tropical and temperate regions (Chen et al., 2019;Zhai, Xu, Dai, Cannon, & Grumbine, 2013). To avoid even greater pressure on native ecosystems around the world, governments, corporations, and tree-planting organizations need to factor in biodiversity and ecosystem services other than carbon sequestration, such as erosion control, soil health, water provision and resilience to pests, diseases, and fire. Furthermore, it has been shown that forests with high biodiversity have higher productivity (Liang et al., 2016;Osuri et al., 2020).
Unfortunately, there is increasing evidence that humanity's response to the call to plant more trees is to plant as many trees as possible on any available sites, without due consideration to the long-term benefits and costs (Bond, Stevens, Midgley, & Lehman, 2019;Lewis, Wheeler, Mitchard, & Koch, 2019). The reasons for this are largely to do with the lack of regionally appropriate and diverse planting material, information, knowledge, and availability of land. As a wide range of sectors and stakeholders start to embark on large-scale tree-planting and restoration initiatives that, collectively, will cover hundreds of millions of hectares, it is essential that they have access to the best science and practical advice, as well as suitable native plant material.
The world's botanic gardens and arboreta grow at least one third of all known plant species, including >16,000 tree species (Mounce et al., 2017;PlantSearch, 2019). This professional community of >60,000 scientists and horticulturists specializes in both fundamental research and applied practice, and can offer data, skills, and advice to address this challenge. Gardens are of course specialists in growing diverse species assemblages in transformed landscapes (garden collections), but not generally at a large scale.
Over the past decade or so gardens have increasingly become involved in the science and practice of ecological restoration (Chen, Cannon, & Hu, 2009;Hardwick et al., 2011

| CON CLUS IONS
The concept of a botanic garden has been around for millennia, but the garden's role in society has changed over time, from a pleasure garden for the elite in ancient times, to establishing the disciplines of botany and systematics, to today being a driving force for plant conservation. Today, gardens are uniquely placed to save plants from extinction, and are the key actors to address some of the greatest challenges facing plant diversity, including: (a) mobilizing and coordinating plant conservation efforts, especially in biodiversity hotspots, (b) quantifying the scope of the plant extinction crisis, (c) conserving exceptional plant species, and (d) using plant-based solutions effectively to combat biodiversity loss and climate change ( Table 2). The garden community already has innovative, proven models of initiatives and programs that overcome these obstacles. What is lacking is the support and capacity to scale these efforts up to amplify impact and deliver cost-effective results for biodiversity conservation.
The support that the garden community needs could take many forms. First and foremost, financial support is needed, including donations, grants, operating support, tax credits, and fees for services. . Gardens provide an impactful conduit for presenting consistent messages and fact-based information on important or controversial topics such as climate change, evolution, biotechnology, food security, and the fundamental importance of plant biodiversity. Now, more than ever, there is an urgent need for trusted institutions providing science-based services and information that help to ensure successful conservation outcomes. Gardens can and should send a strong conservation message to their millions of visitors, as a shift in public opinion towards valuing plant diversity will also drive resources and funding to plant conservation.
Botanic gardens and arboreta are hubs of botanical expertise, they are the critical link between people and plants, and they are the world's greatest force for plant conservation. But, gardens will not be able to achieve the results needed to avert the plant extinction crisis without a revolution in the way resources, funding, and public attention are focused. This includes not only the need for more funding overall for garden-led plant conservation initiatives but also more reliable, long-term, steady funding sources that reflect the time scales necessary to secure threatened plant species, especially long-lived species like trees. We call on funders, governments, corporations, and global citizens to recognize and support gardens as a critical part of the solution to tackling the world's most pressing environmental crises, including the loss of plant diversity.

ACK N OWLED G M ENTS
The authors thank Jessica B. Turner-Skoff and two anonymous reviewers for providing insightful comments on the manuscript. We also thank Peter Raven and the symposium organizers for the invitation to present this article at the National Geographic Symposium, A World of Plants, which led to valuable discussions on this topic.

AUTH O R S ' CO NTR I B UTI O N S
All four authors collaboratively conceived of the ideas presented in this opinion piece. M. Westwood presented the article at the "A World of Plants" symposium at the National Geographic Society in October, 2019, and was the editor of the manuscript.