Systematics and systematists at The New York Botanical Garden DOUGLAS C. DALY Institute of Systematic Botany, New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, USA; e-mail: [email protected]

Abstract. This paper examines systematics at The New York Botanical Garden (NYBG), providing an historical backdrop but emphasizing the diversified skills of the modern systematist and some of the developments since the Garden’s centennial. It reviews some of the factors making NYBG a world center for plant and fungal systematics, including some of the giants in its history, its almost matchless resources for conducting systematics research, some of the landmarks and benchmarks the Garden’s systematists have produced, and some indicators that suggest the productivity is continuing apace at the very least. Some aspects of systematics research are unchanged or virtually so, but numerous dimensions and requisite skills have been added to the systematist’s toolbox, such that graduate students in systematics are now expected to be ‘masters of all trades.’ Outreach and service to the scientific community and the public, including direct influence on conservation, comprise a significant portion of the modern systematist’s activities. The staff and research projects of NYBG’s systematists are remarkable for their geographic and phylogenetic Bcoverage^: the Garden’s geographic research programs are much more global than before, and the Garden has staff researching virtually all major groups of plants and fungi. Another remarkable feature of the Garden’s team of systematists is that it has had staff working on several important taxonomic groups for many decades. Looking ahead to NYBG’s 150th anniversary, the staff will be transformed and the botanist’s toolkit will continue to expand rapidly, but the mission of documenting and conserving the plants and fungi of the world will remain the same. Key Words: Botany, conservation, research, taxonomy.

In the Act of Incorporation of The New York Botanical Garden (NYBG), dated 28 April 1891, the mission of the new institution centered around the Badvancement of botanical science and knowledge and the prosecution of original researches therein and in kindred subjects.^ Starting out with coffee around a table in Henry Allan Gleason’s office in the Museum (now Library) Building, staff and students and visitors have met around what became known as the Lunch Table to talk about botany and Bkindred subjects.^ Over the years, those sitting at the Lunch Table included Gleason, Bassett Maguire, Wendell Holmes BRed^ Camp, Harold W. Rickett, Richard S. Cowan, Arthur Cronquist and Ghillean T. Prance—many of them familiar names in botany and more than a few of them great explorers and great thinkers of the botanical pantheon. Rupert Barneby, one of the most productive botanists in history, who published 6500 pages of hard-core taxonomy (an average of one

published page every three days for 59 years), tended not to frequent the Lunch Table, but anyone was welcome down the hall in his office at 4 p.m. on any day to have tea and learn something about plants and life in general. Stature NYBG has figured prominently in systematics and other aspects of botany since its inception. The initially controversial BAmerican Code^ of botanical nomenclature was first published in 1904 in the Bulletin of the Torrey Botanical Club, to which most if not all NYBG curators belonged; the Garden has had a voice in the evolution of the Code continuously since then. Gleason provocatively shredded the Clementsian dogma of climax communities with his Bindividualistic concept of plant associations^ (Gleason, 1926). Camp and Charles Louis Gilly

Brittonia, DOI 10.1007/s12228-016-9415-7 ISSN: 0007-196X (print) ISSN: 1938-436X (electronic) © 2016, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

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were part of a lively debate on species concepts (Camp & Gilly, 1943). Arthur Cronquist was one of the great synthesists of plant phylogeny in the twentieth century, and his monumental Integrated System (Cronquist, 1981) can be regarded as the point of departure for the adjustments brought by subsequent cladistic and molecular phylogenetic approaches. Dennis Stevenson was responsible in large part for shepherding NYBG into the postCronquist period, and today the Garden’s Plant Research Laboratory is the site of cutting-edge molecular phylogenetic and genomics research and collaborations with other major research institutions. NYBG has great gravitas as a resource for systematics research, not only historically but also on-line. The herbarium has grown tremendously, but so has the number of specimens that have been digitized. The library (now the LuEsther T. Mertz Library) has gone through two reincarnations and relocations, in 1965 and 2002; ironically, for many years it was invaluable because of the many references residing here and almost nowhere else, whereas in recent years it has been invaluable as one of the most important contributors to the Biodiversity Heritage Library, making rare works available worldwide. The Garden was chosen as the repository for the archives of the massive Taxonomic Literature project of Stafleu and Cowan (1976–1988); it has also served as the base for the Flora Neotropica monograph series and recently as one of the core institutions for the World Flora Online project. The Botanical Review, a product of the NYBG Press, publishes papers that explore in-depth major issues of current concern in botany, and the Memoirs of The New York Botanical Garden is a diversified outlet for larger-scale monographs, vegetation studies, biographies, and larger papers on systematics, while Brittonia takes shorter papers on a range of botanical subjects related to floras and systematics. Milestones Some of the publications produced by systematists at NYBG have been landmarks, and some have been benchmarks, setting new standards of quality. Examples of the former are Britton and Brown’s Illustrated Flora of the Northern United States (1913); Britton and Rose’s The Cactaceae (1919–1923); and Gleason and Cronquist’s Manual of the Vascular Plants of Northeastern

United States and Adjacent Canada (e.g., 1963); no doubt the New Manual now being thoroughly revised by Rob Naczi and collaborators will prove to be a new landmark. As a counterpoint to Cronquist’s Integrated System, Rupert Barneby produced a series of landmark monographs, at least one in each of the three major lineages of the legumes. Some remarkable outputs of Garden scientists have set new standards in their genres. These benchmarks, all of them winners of national awards, included Barneby’s (1991) Sensitivae censitae: Description of the genus Mimosa Linnaeus (Mimosaceae) in the New World; the Intermountain Flora (e.g., Cronquist et al., 1997); the Guide to the Vascular Plants of Central French Guiana (Mori et al., 1997); and the Pteridophyte Flora of Oaxaca, Mexico (Mickel & Beitel, 1988). In fact, as a measure of the esteem of the botanical community, since 1991 hardly a year has gone by without at least one Garden systematist winning a major national or international award. In the digital age, Garden systematists have set standards or at least helped set the bar very high with such achievements as the Lecythidaceae Pages (http:// sweetgum.nybg.org/lp/index.php), the Miconieae (Melastomataceae) Planetary Biodiversity Inventory Web site (http://sweetgum.nybg.org/ melastomataceae/index.php), the Elaphoglossum Pages (http://sweetgum.nybg.org/elaphoglossum/ index.php), and the site for Megalastrum: An Electronic Monograph (http://sweetgum.nybg.org/ megalastrum/index.php). These achievements show the difference one or two persons can make. Applying some rather rough metrics for assessing recent achievements, during Fiscal Year 2015 curators in the Institute of Systematic Botany (ISB) produced 1101 published pages in 74 peer-reviewed publications, not counting Web sites and Web content. Returning to the perspective of the past 25 years since the Garden’s centennial, during that time Garden systematists have published some 1050 new taxa (discounting overlapping authorship), including 37 genera and nine tribes, families or superfamilies. What is a systematist today? The past few decades have been as remarkable for what has not changed in systematics as for what has. Many tasks are easier, but there are many more of them. The systematist’s toolkit is simply bulging.

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There is no substitute for extensive Bface time^ with the organisms under study, both in situ (field work) and in sicco (the herbarium). Some aspects of field work do not seem to have changed in a century, as some expeditions still entail long travel, such as by riverboat in Amazonia, by small ship in Patagonia, and on foot—with two or three porters for each botanist to help carry all the gear and specimens—in Myanmar and Colombia. The botanist still records crucial observations about habitats and morphological variation. And the preparation and appearance of a good herbarium specimen today is indistinguishable from an historic one—except for the barcode down in the corner of the sheet. What has changed in field work over the past several decades is the fact that the botanist can precisely map the location of every specimen collected, moreover, the exact whereabouts of the expeditions can be tracked remotely and an expedition can send a signal requesting emergency evacuation if necessary. Some botanists no longer record field data in field books, instead voice-recording for later transcription and/or using a tablet or other compact device. In addition to digital photographs, liquid-preserved plant parts, and the occasional wood sample, the botanist now routinely collects leaf material in silica gel of most or all specimens for molecular studies. In the herbarium, that specimen barcode is an indicator of continuing sea-changes in how systematists interact with specimens. Behind the barcode is software for managing entire collections, which facilitates accessing and managing massive amounts of field data, field images, specimen images, and taxonomic history. An exciting new advance is the development of Web applications designed to streamline descriptive taxonomy, making it possible to analyze and perform functions on data, generate graphics, and make data and results easier to collect, more consistent, retrievable, exchangeable, and reproducible than ever before (http://www.nybg.org/science-new/ explore/monographia.php). In the lab, advances in molecular techniques that help determine genetic expression in discrete tissues have led to renewed emphasis on structural botany (Stevenson, 2016, this issue). And in the library, systematists preparing revisions and monographs still have to agonize over nomenclatural issues, but now at their fingertips (on the keyboard) they have the literature and, increasingly, high-resolution images of crucial specimens in far-flung herbaria.

The modern systematist has ever more powerful resources and tools at hand, and the freshly minted Ph.D. in systematics is expected to be ‘master of all trades,’ to distort an old saying. (S)he is expected to be virtuosic in the use and interpretation of molecular systematic tools. Current doctoral dissertations are likely to contain elements way beyond traditional taxonomy: Our ability to integrate taxonomy, phylogenies (see Stevenson, 2016, this issue), and our knowledge of plant distributions make it possible for doctoral students to examine historical biogeography, phylogeography and population genetics, analytical use of GIS, morphometrics (with plenty of statistics), character evolution, niche modeling, developmental anatomy studies of various organs, histology, karyology, or perhaps all of the above. Recent dissertations at NYBG have included creative use of microphotography and of the analytical tools for comparative biology. Moreover, before graduation, the Ph.D. candidate hoping to land a research position is expected to have several articles published in high-impact journals. The down-side of this depth, of developing this impressive array of skills, is that learning and demonstrating some mastery of them all but precludes gaining broad knowledge of a taxonomic group. The Garden maintains a list of taxonomic groups and the specialists who are willing and able to receive specimens in those groups for identification, and there has been a steady erosion of that list over the past 25 years. The solitary specialist who can identify hundreds or in a few cases thousands of species is becoming a thing of the past. That said, there is now a tendency to form consortia to collaborate on multi-faceted studies of large, complex taxonomic groups, e.g., the Melastomataceae-Miconieae (http:// www.nybg.org/science-new/explore/miconieae. php), but it is questionable whether enough of these will be formed to meet the enormous need for identifications. Outreach and service For NYBG’s centennial in 1991, Richard Cowan wrote that Bif a science cannot articulate its worth as well as its needs, it tends to wither on the vine…^ (Cowan, 1991: 357). That is even truer today. Up until the 1980s, a prevailing philosophy among taxonomists was that they produced data that others could use to advance conservation. Two of the most important services that

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systematists at NYBG contribute are still the identification of specimens (thousands per year) and deciphering and publishing research on taxonomic groups (now averaging more than 1000 published pages per year), but systematists now can and must respond to and anticipate environmental crises and needs, and increasingly they seize opportunities to do so. They make much more direct contributions to conservation and sustainable management of plant and fungal resources (see Boom, 2016, this issue). ISB staff have had direct input in the creation of new protected areas in Brazil, French Guiana, and a number of other countries. One ISB curator successfully proposed the first lichen species for IUCN Red Listing as Globally Threatened (http://www.iucnredlist.org/ details/70386009/0), and others spearheaded the development of an alternative and more rapid approach to assessing the conservation status of plants (Miller et al., 2012, 2013). Garden scientists contribute a dizzying array of services to the scientific community and the public. ISB systematists serve on the board of the Rainforest Trust, as president of the New Fern Society (and recently of the American Mycological Society), on the IAPT Nomenclatural Committee for Fungi, and as editors-in-chief of six journals and scholarly series (Brittonia, The Botanical Review, Memoirs of The New York Botanical Garden, Flora Neotropica, Cladistics, and Opuscula Philolichenum). They teach graduate courses and workshops, and advise numerous graduate students (see Kelly, 2016, this issue). They review many manuscripts, thesis proposals, and proposals for the National Science Foundation. They present the results of their research at national and international scientific meetings and give lectures to conservation groups, amateur societies, continuing education students and the general public. They advise the Brazilian Forest Service on personnel and field protocols for that country’s national forest inventory. BCoverage^ – geographic Both the botanical exploration and taxonomic research of NYBG were mostly oriented toward the New World for much of its history, but in the past 25 years the Garden’s geographic coverage has become much more global (Thomas, 2016, this issue; Fig. 1). International communications and collaborations have improved, and Garden researchers have been increasingly successful at

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garnering grants for international projects, but the most important factor has been the global perspective on plant and fungal lineages made possible by the ever-accelerating evolution of molecular phylogenetic studies. Current tools make it possible to study the evolution and relationships groups of organisms worldwide, and this global perspective has allowed us to Blook East,^ pointing the way for systematic research particularly in various parts of (sub)tropical Asia, as well as Madagascar and Australia. The Garden recently added Myanmar and Vanuatu to its list of formal geographic research programs. During the week of March 1, 2015, Garden researchers were collecting plants in Brazil, Colombia, China, Jamaica, Costa Rica, and Vanuatu; it is not unusual for Garden systematists to maintain active research programs in two or three countries simultaneously. Meanwhile, several of the Garden’s researchers focus primarily on North America. The global perspective of the Garden’s research is evidenced by the fact that Garden systematists contributed treatments of nine families to Kubitzki’s Families and Genera of Vascular Plants (e.g., Daly et al., 2011). In the current age of Big Data, Garden systematists are or recently were co-Principal Investigators in national and international collaborations to advance understanding of large groups of organisms, as with the National Science Foundation’s Planetary Biodiversity Initiative (Solanaceae, Melastomataceae-Miconieae), or projects involving multiple groups of organisms, such as the National Science Foundation’s Dimensions of Biodiversity program. Garden systematists are core investigators in three Dimensions projects. One is correlating biogeographic and environmental patterns across major clades in order to explain and predict the distribution of animal and plant species in the endangered yet megadiverse Brazilian Atlantic forest. Another is uncovering the factors that impact diversity and distributions of obligate symbiotic lichens, focusing on a global lichen diversity hotspot, the southern Appalachian Mountains of the southeastern U.S. A third is using a comparative approach cutting across systematics, population biology, ecosystem structure and function, geology, earth systems modeling and environmental history to examine where to find the greatest biodiversity in Amazonia, how the modern Amazonian biota and its environment assembled across space and time, and how past climate

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FIG. 1. In the past 25 years the Garden’s geographic coverage has become much more global. Some of the locations of NYBG field work. A. North America. B. Cuba. C. Brazil (Amazon). D. Brazil (Atlantic Coastal Forest). E. Myanmar. F. Australia. Photo credits: Lawrence Kelly (A), Fabián Michelangeli (B, D), Douglas Daly (C), Katherine Armstrong (E), Roy Halling (F).

changes affected species of plants and animals (and therefore how future changes will affect them). BCoverage^ – phylogenetic One of the most remarkable qualities of the systematics research staff at the Garden is its phylogenetic breadth, that is, the Garden has specialists to Bcover^ all major groups of plants and fungi: green algae, bryophytes (mosses and hornworts), pteridophtyes, cycads, other gymnosperms, several groups of monocots, most if not all major groups of dicots of the APG-III system (APG, 2009), basidiomycetes, and lichens (which include innumerable ascomycetes; Fig. 2). This ensures a growing and well-rounded herbarium

(Pace et al., 2016, this issue); in the age of genomics it also means that Garden systematists are well-positioned along the big nodes on the plant and fungal trees of life and able to inform the posing and answering of larger questions in broad comparative studies. Two recent examples are studies on the evolution of fruits, and a genomics consortium study of the evolution of traits that confer drought resistance and efficient nitrogen uptake in poor soils; the latter study compares related plant groups in similar but disjunct habitats. Continuity No less valuable is the ISB staff’s coverage of a number of major taxonomic groups, decades-long

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FIG. 2. Garden systematists are well-positioned along the big nodes on the plant and fungal trees of life and able to address larger evolutionary questions in broad comparative studies. A. Fungi. B. Lichens. C. Green algae. D. Bryophytes (mosses). E. Pteridophytes (fern). F. Gymnosperm (Gingko). G. Cycad. H. Flowering plant. Photo credits: Roy Halling (A), James Lendemer (B), Dario Cavaliere (C), Robbin Moran (D, E), Dennis Stevenson (F, G), Fabián Michelangeli (H).

and in some cases almost continuous since the Garden’s founding. The specimens collected by Garden-based systematists, plus the large number of specimens sent to them as gifts for determination, result in reference collections of often

incomparable depth and breadth for those groups. The knowledge and experience of active staff at NYBG who research those groups attract top talent in the pool of prospective graduate students and post-doctoral fellows.

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The most remarkable of these taxonomic groups is the bryophytes, the study of which began with Elizabeth Britton and has continued most recently with Bill Buck; other groups are the Leguminosae (Rupert Barneby, Dick Cowan, and now Ben Torke), Melastomataceae (Henry Allan Gleason, John Wurdack and now Fabián A. Michelangeli), pteridophytes (Lucien M. Underwood, John Kunkel Small, John Mickel and now Robbin Moran), Cyperaceae (K. K. Mackenzie, Tetsuo Koyama, and currently Wayt Thomas and Rob Naczi), and until recently the Ericaceae, which was studied by A. C. Smith, W. H. BRed^ Camp, James Luteyn, and Paola Pedraza. Other groups that have been studied at the Garden for merely 25–30 years include Solanaceae and Cucurbitaceae (Michael Nee, now retired), lichens (Dick Harris and James Lendemer; Lendemer & Harris, 2016, this issue), palms (Andrew Henderson and Michael Balick), Lecythidaceae (Ghillean Prance and Scott Mori, now retired), Anacardiaceae (John D. Mitchell), and Burseraceae (Douglas Daly). Looking ahead The mission of NYBG systematists to explore, discover, document, identify, map, analyze, interpret, and conserve plant and fungal diversity is increasingly urgent. As Henry Allan Gleason wrote with prescience in 1950, BWe need still more such concentrated knowledge… There have been times, and there may come other times when you will need that knowledge and experience very much and very quickly^ (Gleason, 1991: 321). Coincidentally, the team of systematists at the Garden has entered a period of high turnover as senior staff retire, and those who will be celebrating the Garden’s 135th anniversary, not to mention its 150th, will be an almost entirely different group. It will be essential that the new ranks of systematists not only comprise a critical mass of researchers but also that the Garden keep up the geographic and phylogenetic coverage it now maintains. No doubt they will be extremely well-trained in the use of an array of powerful tools. Their challenge will be to broaden their knowledge of the groups of organisms they study, and to translate the greatly enhanced abilities of evolving systematics into greatly enhanced research output. The Lunch Table is likely to still be there in 25 years, but most of the faces will be different. We

sincerely hope it will be crowded with systematists, but we have no doubt that the people around it will be very busy as productive researchers and shouldering ever more responsibilities to science and society. Once again, what Henry Alan Gleason (Gleason, 1991: 319) wrote in 1950 absolutely holds true today: BAnd have we found all the plants? By no means.^ Acknowledgments I thank all the members of the Institute for Systematic Botany at NYBG for their input, and Ben Torke, Fabián Michelangeli, and Lawrence Kelly for their careful edits of the manuscript.

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BRITTONIA ——— & A. Cronquist. 1963 (and later editions). Manual of vascular plants of Northeastern United States and adjacent Canada. Van Nostrand, Princeton. Kelly, L. M. 2016, this issue. Training the next generation: Graduate studies at The New York Botanical Garden, with emphasis on 1996–2015. Brittonia 68(3). Lendemer, J. C. & R. C. Harris. 2016, this issue. The NYBG Lichen Herbarium: A unique resource for fungal biodiversity research and education. Brittonia 68(3). Mickel, J. T. & J. M. Beitel. 1988. Pteridophyte flora of Oaxaca, Mexico. Memoirs of The New York Botanical Garden 46: 1–568. Miller, J. S., H. A. Porter-Morgan, H. Stevens, B. Boom, G. A. Krupnick, P. Acevedo-Rodríguez, J. Fleming & M. Gensler. 2012. Addressing target two of the Global Strategy for Plant Conservation by rapidly identifying plants at risk. Biodiversity and Conservation 21(7): 1877–1887. ———, G. A. Krupnick, H. Stevens, H. Porter-Morgan, B. Boom, P. Acevedo-Rodríguez, J. Ackerman, D. Kolterman, E. Santiago, C. Torres & J. Velez. 2013. Toward Target 2 of the Global Strategy for Plant Conservation: An expert analysis of the Puerto Rican flora to validate new streamlined methods for assessing

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