Planning the future of plant systematics: Report on a special colloquium at the Royal Netherlands Academy of Arts and Sciences.

Abstract

Forty botanists from 13 countries met this March in Amsterdam at a special colloquium at the Royal Netherlands Academy of Arts and Sciences to discuss the future of plant systematics (“Beyond the Tree of Life: the Future of Plant Systematics”; Fig. 1). The meeting was funded by the Netherlands Royal Academy and organized by Erik Smets (Naturalis Biodiversity Center, Leiden, Netherlands) and colleagues*; it addressed several paradoxes in our field. First, with an ongoing planetary-scale biodiversity crisis, the need for plant systematists has never been greater, and yet taxonomic expertise appears to be in steady decline, as noted by repeated calls for action (e.g., de Carvalho et al., 2007; Drew, 2011). Despite this, new plant species are continuously being discovered, and plant systematics as a field has survived and even thrived, thanks to the common overarching goal of building and understanding the Tree of Life, spurred by the availability of new technology and powerful analytical frameworks. Yet, members of the public and colleagues outside biology often express surprise when new plant species are discovered or appear unaware that the Tree of Life is far from being fully resolved. In this context, how do we justify the importance of continued research on plant biodiversity and explain its importance to the general public, university administrators, funding agencies, and policy makers? The organizers identified three central questions for the colloquium to help address these issues: (1) What are the big questions for plant systematics? (2) How should we train the next generation of systematists? (3) How can we emphasize the prominent role of systematics to the outside world, to safeguard the future of our field? Group photograph of the colloquium participants, taken on the third day at the Trippenhuis in Amsterdam. From left to right, top to bottom: Chelsea Specht, Lars Chatrou, Timo van der Niet, Leni Duistermaat, Pedro Crous, Peter Linder, Vincent Merckx, Tod Stuessy, Eric Schranz, Wouter Los, Frederic Lens, Alexandre Antonelli, Niels Raes, Sandra Knapp, Marc Sosef, Pieter Baas, Jorinde Nuytinck, Karol Marhold, Sean Graham, Hans ter Steege, Paul Hoekstra, Muthama Muasya, Mike Thiv, Nina Rønsted, Erik Smets, Michelle Price, Hervé Sauquet, Saroj Ruchisansakun, James Byng. The structure of the meeting and the breadth of attendees were well suited to addressing these questions. Participants represented multiple branches of systematics, including descriptive taxonomy, morphology, phylogenetics, ecology, mycology, genomics, biodiversity informatics, and medicinal botany, and spanned the full range of career stages (from graduate students to senior professors) and diverse institutions (including universities and natural history museums). They came mostly from Europe (around half from the Netherlands), and included representatives from Asia, Canada, South Africa, and the United States. In the morning and early afternoon of each day, a small number of speakers gave short (half hour) talks on a broad diversity of relevant topics, ranging from work on contemporary floras and monographs, to next-generation phylogenetics and emerging computational tools for biodiversity informatics (Table 1). In addition, short shotgun sessions were included that gave all participants the chance to give flash talks or express opinions on topics of interest, and brainstorming discussion sessions concluded each day. Erik Smets started off the meeting by explaining the need for the colloquium. He argued that a critical problem is that society has a poor understanding of the relevance of plant systematics, in part because many people mistakenly think that we already know everything there is to know about plants. A key challenge for the future will thus be to bridge the gap between society and our science, to explain to humanity why it is important to address what we do not know yet about plant diversity, in all its guises. We outline here the major ideas that emerged from the invited talks and summarize conclusions from the discussion sessions. As we hope to demonstrate, this was a highly fruitful, interactive and enjoyable colloquium and a welcome opportunity to reflect on a field at a critical time of transformation. While it is important to acknowledge that the field has continuously changed and that introspection about and planning for the future of systematics has occurred on several occasions in the past (Ehrendorfer, 1970; Stevens, 2000; Sytsma and Pires, 2001), several of the challenges discussed during this meeting represent important new developments, in particular those related to new tools and methods, and to new forms of teaching and communication. Several speakers presented examples on the recent history of our field and how new approaches are transforming research. For example, Marcel Dicke (Wageningen University, Netherlands) introduced the concept of the phytobiome (macrobiome plus microbiome) of plants, and presented a large project on natural variation and biotic interactions of Arabidopsis thaliana. Pedro Crous (CBS Fungal Biodiversity Centre, Utrecht, Netherlands) presented work on fungal pathogens of plants, showing how specimen-level molecular phylogenies of fungal pathogens have become critical for trade control and human health, where traditional systematic approaches have largely failed. Alexandre Antonelli (University of Gothenburg, Sweden) reviewed the current state and future prospects for building and synthesizing the Tree of Life, using phylogenomic and new bioinformatic tools. Tod Stuessy (Ohio State University, Columbus, OH, USA) documented the history of classification principles. Concerning our knowledge about plant species, Peter Linder (University of Zurich, Switzerland) reviewed the history of species concepts to emphasize that describing and naming species had been one of the greatest enterprises ever undertaken by humanity. He presented species as a true “can of worms” and argued that we needed to start understanding the “worms” much better, by studying patterns of inheritance, gene flow, and selection. Mike Thiv (Natural History Museum, Stuttgart, Germany) argued for the need to link species concepts with next-generation sequencing (NGS) and epigenetic data, and insisted that facilitating feedback from plant systematics to conservation will be essential for preserving biodiversity. Timo van der Niet (University of KwaZulu-Natal, Durban, South Africa) reviewed current understanding of speciation processes, about which many unknowns remain, including understanding species and populations in contexts beyond relationships in the Tree of Life. Muthama Muasya (University of Cape Town, South Africa) noted that Africa represents an urgent gap in plant systematics, as the continent is home to 45,000 flowering plant species representing four major biogeographic regions. Although fundamental plant biodiversity research is not yet a funding priority in most African countries, a bright spot is that DNA barcoding has been embraced as a means of blending traditional and molecular approaches to documenting plant diversity. Genome-focused approaches hold the potential to revolutionize our understanding of the plant tree of life and plant biology. Sean Graham (University of British Columbia, Vancouver, BC, Canada) reviewed the use of NGS data in plant phylogenetics. Specifically, he showed how data from plastid genomes (e.g., Ross et al., 2016) and transcriptomes (1KP or One Thousand Plants initiative; Wickett et al., 2014) are already contributing to improving our understanding of higher-order plant phylogeny. He also pointed to exciting emerging NGS phylogenetic initiatives such as the PAFTOL (Plant and Fungal Trees of Life; http://science.kew.org/strategic-output/plant-and-fungal-trees-life) project at the Royal Botanic Gardens, Kew and GoFlag (http://flagellateplants.group.ufl.edu/), an NSF/Genealogy of Life funded project aiming to sequence all “flagellate plant” species (nonflowering land plants, including several lineages with nonflagellate sperm). Citing a recent example from the backbone of fern phylogeny (Rothfels et al., 2015), he pointed out that phylogenomic studies may end up refining rather than revolutionizing our understanding of plant relationships. Chelsea Specht (University of California, Berkeley, CA, USA) highlighted results from an ongoing study using targeted exon capture that successfully resolved relationships in Zingiberales, when whole plastid genomes turned out to be insufficient. She also presented ARBOR, a new platform to facilitate diverse comparative analyses based on the idea of customized and publishable workflows, including innovative data visualization tools currently under development (Harmon et al., 2013). Another example of a new tool was provided by Rutger Vos (Naturalis Biodiversity Center), who described SUPERSMART (Self-Updating Platform for Estimating Rates of Speciation and Migration, Ages, and Relationships of Taxa), a new pipeline for building and dating phylogenetic trees using GenBank data for any given clade or set of species (Antonelli et al., 2016). How do we train the next generation of plant systematists in increasingly competitive funding environments? Hervé Sauquet (Université Paris-Sud, France) presented a project for an Innovative Training Network (ITN) proposal submitted to the European Commission to prepare the next generation of botanists for service to society both in and outside academia through high-quality international training of 15 Ph.D. students. He explained how developing this proposed program with 10 other European laboratories led to a very fruitful reflection on the skill set and tool kits required for training “next-generation” botanists, which convinced him that sharing knowledge and passion about plant science with the general public is a critical communication skill that we all need to work on. The latter was illustrated in particular by the Massive Open Online Course (MOOC) on introductory botany created by the French association Tela Botanica (http://mooc.tela-botanica.org/), an associated partner in the ITN proposal. The MOOC (in French) has attracted more than 33,000 participants, demonstrating strong interest and demand from the general public in botany training opportunities. New teaching tools and approaches were also discussed with respect to undergraduates and the broader public. James Byng (Naturalis Biodiversity Center) presented the activities of The Flowering Plant Gateway, a nonprofit organization that teaches botanical courses and produces synthetic books at a time when some countries (such as the UK) have nearly abandoned student training in plant sciences (http://www.telegraph.co.uk/news/science/steve-jones/8001565/Where-have-all-the-British-botanists-gone-just-when-we-need-them.html). He argued, “We need more botanical bibles!” As a means of connecting plant systematics to a broader public, Nina Rønsted (University of Copenhagen, Denmark) explained how collections and plant systematics are important resources for improving human health, using examples from her work on medicinal plants. She presented a 2-minute snapshot of a future movie (“The Quest for Cinchona—A Phylogenetic Tale”) on a recent field trip in Bolivia to be used as a new case study for teachers and schools. Our community has an unfortunate tendency to lament the perception of systematics by the public and colleagues from other scientific disciplines. Alexandre Antonelli invited us to “stop complaining and do fantastic things!” He pleaded for the development of policy for the use of public databases in systematics, noting “If it's not in a database, it doesn't exist.” Concerning how systematists work, Sandy Knapp (Natural History Museum, London, UK) pointed that there is a mistaken perception that taxonomists/systematists work alone, in contrast to fields like physics where scientists are perceived to work in very large groups on ambitious projects. Increasingly, however, plant systematics is a massively collective endeavor, exemplified by large collaborative projects like The Plant List (http://www.theplantlist.org/), which build on several long-running databases including Tropicos (http://www.tropicos.org/) and the International Plant Names Index (http://www.ipni.org/). She also noted that, despite common complaints by taxonomists, it is also not necessarily the case that taxonomic papers are more poorly cited than other biological papers (Steiner et al., 2015), a concern so long as citation indices drive tenure and funding agencies. She also argued that finding ways to accelerate taxonomic discovery is an essential goal for our future, given that taxonomic capacity to describe species has stagnated in the past few decades (Bebber et al., 2014). Current informatics infrastructure such as JStor Global Plants, GBIF, and the Biodiversity Heritage Library are increasingly important tools to speed up the rate of species discovery and synthesis, but more could be done in this regard. In particular, making all biodiversity data open and freely available is an essential target. Field collections will continue to be central to plant systematic research. Knapp noted that we need to collect more, even in supposedly well-collected regions, and should clear up museum backlogs. However, she noted that the map of scientific collaboration looks quite colonial and warned against “helicopter science” or “science safaris” as the main means of improving knowledge of plant diversity outside the West. Indeed, a key problem in the field is that biodiversity experts are unevenly distributed across the planet. Muthama Muasya highlighted that of ∼2000 botanical collectors in South Africa, only 1% are black Africans. Exemplifying this, existing African floras have mostly been written outside Africa and have often not been updated, and existing botanical collections were once rooted in colonial ideals and mentality. Future priorities if resources continue to be limited may include revising priority genera and tapping into the power of citizen scientists. Continuing the theme of documenting plant diversity, Marc Sosef (National Botanic Garden, Meise, Belgium) pointed out, “We know an awful lot about awfully few species.” He reminded us that the first objective of the Global Strategy for Plant Conservation plan was to “know” plant diversity and that the first outcome of this initiative was the release of The Plant List in 2010, although the means for its continued update are unclear. The next global challenge is to produce an online flora of all known plants by 2020. However, we are still very far from meeting this target: floras and e-floras are being published independently by various countries on different platforms, often with slow rates of completion. The World Flora Online initiative was created to address this problem, but has not yet secured a major funding source to sustain long-term infrastructure and management. Karol Marhold (Slovak Academy of Sciences, Bratislava, Slovakia) presented a vision for the future of botanical monographs, which need to be considerably more integrated with online repositories and with other disciplines than they have traditionally been (Wen et al., 2015). Michelle Price (Conservatoire et Jardin botaniques de la Ville de Genève, Switzerland) presented the perspective of the Consortium of European Taxonomic Facilities (CETAF), an organization that she currently chairs. She outlined the need for a new publishing model in which neither the reader nor the contributor pays, which seems particularly critical in developing countries to allow for increasing access and contribution to taxonomic knowledge. She also presented the Code of Conduct and Best Practices produced by CETAF to accompany biodiversity researchers in legal and ethical aspects of fieldwork in the context of the new Nagoya Protocol (Bodegård et al., 2015). Finally, Wouter Los (University of Amsterdam, Netherlands), cofounder of the CETAF, concluded with an inspiring overview of the infrastructure needed to support the research process, from data capture and storage to data processing and sharing. He argued that existing initiatives cover less than half of this ideal infrastructure, and that considerable progress can be achieved in transforming how data are currently being captured and stored in biodiversity research, although it remains to be determined how this progress can be institutionalized internationally. A substantial portion of the colloquium was devoted to discussion sessions addressing general themes that emerged from the morning sessions, to explore possible paths forward in a transforming world, critical for the future of plant systematics. Participants divided into two groups each afternoon for workshop-style brainstorming sessions that covered the themes, summarized here, which the full assembly then synthesized in a broader discussion. The four themes below were collectively decided by the participants during discussions at the end of the first day. Funding was a recurrent issue, but it was eventually dismissed as a key question in the debate. A general consensus emerged that we need to spell out the key (scientific) questions in plant systematics today and for the future. Another important element that emerged is how to make the field more collaborative. We also tried to identify what makes plant systematics special compared with systematics in general. The first discussion session focused on ways to preserve and improve taxonomic competence of future generations. We considered options for building taxonomic and biodiversity awareness at all levels of the education system, from elementary to tertiary levels. Innovative ideas included the production of biodiversity MOOCs for kids, taking advantage of children's natural attraction to video media, and counteracting the often insufficient training and experience and limited time of teachers in natural history. Among ideas to improve taxonomic awareness at high school and undergraduate levels, a strong focus on getting them outside to explore the natural world through fieldwork and course experiences came as a recurrent suggestion. Increasing connectivity of taxonomic expertise among institutions and countries was recognized as key for preserving knowledge and skills at the graduate level and above. Some participants also came up with the idea of defining collections in natural history museums as the objects (biological samples) and associated people (taxonomists, curators) to better value the preservation of taxonomic knowledge and expertise as much as the physical collections. Other avenues for protecting existing knowledge included (unsurprisingly) continued reinforcement of electronic and open access to research products, including e-monographs and e-floras, tied in with existing databases (of accessions, names, occurrences, and traits). Our second discussion theme encouraged us to think outside the box and brainstorm on simple and wild ideas relating to the future of plant biodiversity science. An interesting and realistic suggestion that received a strong consensus was the definition of a next-generation collecting standard that could help current and future botanists make the most of costly and time-consuming field trips. In addition to current sample and data collection (including herbarium voucher, silica-gel-dried leaf samples, georeferencing, and digital photographs), our discipline would strongly benefit from the systematic implementation of better ethical practices, including systematic deposition of material in a herbarium of the country of origin. We dreamt of a new global infrastructure that would allow immediate deposition of digital collection data (including provisional identification name, georeference, and specimen photographs) to a public World Virtual Herbarium, with links to final herbarium sheet images and metadata once deposited and processed in physical herbaria. Such infrastructure could be used as a platform for linking all vouchers of genetic and genomic databases, facilitating accurate and up-to-date species identification and provenance tracking in downstream work. Once such standards and infrastructure are in place, major natural history institutions and funding agencies supporting fieldwork could promote their implementation by making their use compulsory. Currently, the vast majority of field notes and photographs still reside in personal notebooks, and it may take years or decades (if ever) until such highly valuable field data funded by public budgets make it to a public output. Future add-ons to the next-generation collecting standard might, one day, include on-the-spot three-dimensional computerized tomography (CT) scanning of specimens and whole-genome and transcriptome sequencing. We also discussed the great potential that collective fieldwork holds to purvey a positive image of plant biodiversity science as lively and exciting for broader audiences. Several of us have already started to use video and social media extensively to share thrilling fieldwork experience with family, friends, students, other colleagues, and the general public (e.g., https://www.youtube.com/user/vincentmerckx; Sauquet, 2015). Combining large, collective field trips—“BioBlitz” trips—would not only be excellent for scientific research (e.g., Merckx et al., 2015) and comprehensive biodiversity documentation, but could also have an immense positive impact on society if accompanied by professional communication plans. Such initiatives would increase plant biodiversity awareness and understanding of critical conservation and documentation needs, and contribute to promoting a stimulating and attractive image of plant systematists, inspiring interest in our field from new generations. To achieve these goals, it will be essential that communication strategies become more inclusive, focusing less on white male faculty from Western countries and more on student, female, and local biodiversity experts. The third discussion session aimed at formulating questions and solutions that plant systematists as a community may realistically target in the near future. Four tentative key questions emerged: (1) How is plant life related, and how is diversity distributed in time and space? (2) What are the processes generating biodiversity? (3) How many species are there, and what do we know about them? (4) How do we break the barriers for training and employing systematists in the developing world? To address these questions, we thought that a flagship international project aimed at collecting/synthesizing in public databases, the phenotype, interactome, and genome from 100 specimens each of 1000 species over their distribution range and ecological gradients could attract excitement and major sources of funding and provide significant, novel answers and new questions. Similar, widely collaborative projects already exist for genomes of Fungi (1000 Fungal Genomes Project, http://1000.fungalgenomes.org/) and plant transcriptomes (1KP, https://sites.google.com/a/ualberta.ca/onekp/). However, these projects do not yet systematically integrate the phenotypes or ecological interactions, or the intraspecific variation of the focal species, leaving important gaps to be filled by future major initiatives for better understanding the distribution and genesis of plant biodiversity on Earth. Additional tools identified to work toward these goals represented recurrent themes highlighted throughout the colloquium. They included the need to train the next generation of botanists and to develop joint international standards, best practices, and joint projects in plant biodiversity research, the critical necessity to develop global, dynamic, and well-curated long-term databases linking all dimensions of plant biodiversity, and better opportunities for funding joint and truly international fieldwork and capacity building. Our last discussion session focused on how to improve communication with the general public and policy makers. Several interesting suggestions emerged. First, most of us agreed that we should all be much more outspoken and play more active roles in sharing knowledge and passion for plant research in all forms of media. It is clear that the public is excited about new species discoveries, as seen from the press response to the recent descriptions of Sirdavidia solannona (Couvreur et al., 2015) and Solanum watneyi (Martine et al., 2016). Both examples played on name dedications (to Sir David Attenborough, the famous BBC author and presenter of natural history documentaries, and Mark Watney, the lead character from The Martian, a recent well-received science fiction book and film with a significant botanical spin). These can create initial baits to attract public interest and can be efficient channels for passing the message to the broadest audience that new plant species are still being discovered today. Following the lead of colleagues who are already very active in sharing plant news on Twitter, such as Sandy Knapp, Chris Martine, and Kent Holsinger, both authors of this paper decided to open an account on the microblogging platform during the colloquium. Several of us then decided to start a new series under hashtag #discoverplants. These are very small, individual actions but, collectively, have the potential to make a difference, similar to the very successful “Reclaim The Name: #iamabotanist” internet campaign started by the Botanical Society of America 2 years ago. To improve our communication and outreach skills in a fun environment, we also came up with the idea of a “communication bootcamp” for plant systematists to bring together students, professionals with proactive communication experience, and skeptical colleagues with communication anxiety to reflect, learn, and improve the impact on and understanding of our discipline by society. In general, we all agreed that we needed to be more positive and learn how to deliver clear, enthusiastic, and understandable messages to the general public. As a start, we thought that taxonomy and systematics are obscure terms that most nonscientific audiences poorly understand and that, unfortunately, may convey a negative, mistaken view of a long-dead, obsolete science for policy makers and even colleagues from other scientific disciplines. We might therefore start calling ourselves plant biodiversity experts instead when we talk to the general public, or perhaps even “species explorers”. Plant systematists need to learn to work together and train new generations of plant systematists more collaboratively than we do at present. Global plant biodiversity databases are urgently needed. Worldwide standards for plant collecting and data sharing are needed. Plant systematists need to communicate more actively and positively about our research with the general public. “Plant biodiversity science” may be a desirable alternative to “plant systematics” as a discipline name for current and future generations. The authors thank the organizers of the colloquium for inviting all of the participants to this meeting. They also gratefully acknowledge the Royal Netherlands Academy of Arts and Sciences for funding this event. The authors thank Pamela Diggle for inviting them to write this meeting report. Erik Smets, Frederic Lens, and Vincent Merckx and two reviewers kindly provided helpful comments on a draft of this paper.