The New York Botanical Garden Lichen Herbarium: A unique resource for fungal biodiversity research and education JAMES C. LENDEMER AND RICHARD C. HARRIS Institute of Systematic Botany, New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, USA; e-mail:
[email protected]
Abstract. The history and development of the lichen research program and herbarium at The New York Botanical Garden are reviewed. Key Words: Biodiversity inventory, biodiversity information synthesis, big data, conservation.
Since its founding in 1891, a core aspect of the scientific mission of The New York Botanical Garden has been its broadly inclusive interdisciplinary nature. Throughout 125 years of expeditions, employment of scientists, and publishing of scientific literature, the Garden has celebrated the diversity of taxonomic groups traditionally treated in the field of botany rather than excluding organisms such as algae, bryophytes, fungi, and lichens from its purview. The result has been the creation of a body of infrastructure (e.g., archival materials, digital resources, herbarium collections, library holdings) and taxonomically broad scientific capacity that are not easily surpassed. Among the unique resources assembled by Garden staff and collaborators is the herbarium of lichens and allied fungi, which at >260,000 accessioned specimens is the largest such collection in the Western Hemisphere and the second largest in the world. While the size of this collection is noteworthy, it is the breadth and depth of coverage, combined with phylogenetic organization and constant curation that truly render it unique. Here we review the history of the collection, place it in the context of current Biodiversity Information Synthesis (see Tripp & Hoagland, 2013), and outline directions for the future. Establishment of the collection (1891) The nucleus of the NYBG lichen herbarium derives from several New York City herbaria that were incorporated into the institution shortly after its founding in 1891. Of particular importance were the holdings of Columbia College, which
included the herbarium of John Torrey (1796– 1873), a seminal figure in American botany (see Gray, 1877). Although relatively small in size, the specimens that form the historical core of the herbarium comprise valuable collections made by botanists across the globe, including many type or authentic specimens. Building the foundations (1892–1979) The emphasis that NYBG founders Elizabeth and Nathaniel Britton placed on cryptogamic biodiversity inventory and taxonomy is one of paramount importance in the development of lichenology at the institution. Following the founding of the Garden in 1891, it immediately began an ambitious program of natural history expeditions on par with other major institutions of the period. Importantly, however, the founders and in particular Nathaniel Britton had a strong commitment to lichens as is illustrated by the funding of lichenologists such as Clara Cummings and Bruce Fink to collect for NYBG in the West Indies. Similarly, plant collectors who were not lichenologists were encouraged to also collect lichens as part of their work. Such efforts resulted in large collections from the West Indies, eastern North America, western North America and Andean South America. Also, beginning in this period, with the acquisition of W. A. Leighton’s (1805– 1889) duplicates and a gift of the H. E. Hasse (1836–1915) herbarium, a significant portion of the collection was acquired by gift, inheritance or purchase of large collections assembled by lichenologists. A particularly unique aspect of the
Brittonia, DOI 10.1007/s12228-016-9424-6 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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collections assembled during this time is that they represent not only large and conspicuous macrolichens, but also a remarkable diversity of crustose lichens. As such, the foundation of the lichen herbarium at NYBG encapsulates a snapshot of lichen diversity in the Americas on the verge of an era of rapid industrialization and urbanization. Revision and organization (1980–1990) Despite the attention that NYBG scientists and collectors paid to lichens during biodiversity inventories, as well as to the expansion of the lichen herbarium, the first lichenologist to work at the institution did not arrive until 1980. The arrival of Richard C. Harris (b. 1939) at NYBG initiated the first serious attempt to revise and organize the institutional holdings of lichens for use in modern systematic and floristic studies. When he joined NYBG, Harris immediately recognized the importance of the extensive historical holdings of lichen collections from Andean South America, Europe, North America, and the West Indies. Although routine curation had occurred previously, and lichenologist Mason Hale (1928–1990) of the Smithsonian Institution had estimated the size of the collection to be approximately 60,000 (M. Hale pers. comm. to R. Harris) as opposed to the figure of 100,000 specimens given in Index Herbariorum (Holmgren et al., 1981), no comprehensive revision and assessment of the collection had been performed before that time. As such, Harris began to systematically revise and curate the collection in conjunction with research carried out in the Neotropics and temperate North America by himself and other colleagues at NYBG. The first step towards reorganization involved a survey of the entire herbarium in 1990, wherein the specimens in each herbarium case were systematically counted to arrive at the first accurate count of accessioned specimens: 91,661 (as of June 1991), a number below the estimate cited in Index Herbariorum, corroborating Hale’s number allowing for over ten years of accessions. It was this count-based assessment that was then used as the baseline against which future accessions were totaled. Since counting the herbarium involved surveying the entire collection, this presented a logical time to evaluate how best to organize the collection. The lichens at NYBG had historically been
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arranged following the evolutionary Engler and Prantl system (Zahlbruckner, 1926), while in contrast the majority of lichen collections in other herbaria were arranged alphabetically. The widespread use of alphabetization in lichen herbaria was, and still is, due to a combination of factors, foremost among which is the need to facilitate curation at the many institutions where lichenologists are not employed. In addition, at that time employing a system that did not imply evolutionary relationships would have been advantageous because it avoided following Zahlbruckner’s system, expanded in the Catalogus Lichenum Universalis (Zahlbruckner, 1921–1940) which, by the 1980s was widely recognized as highly artificial and outdated (e.g., Santesson, 1952; Hertel & Rambold, 1985; Staiger, 2002; Gaya et al., 2003). Fortuitously, the period when reorganization of the collection was being considered coincided with the publication a landmark work in lichen systematics (Hafellner, 1984), which initiated a break from the Zahlbruckner system to a modern one based on previously under-utilized characters such as ascus structure. Thus rather than abandoning the use of an evolutionary system, Harris was inspired to adapt Zahlbruckner’s system to new taxonomic concepts as they emerged and expanded the system through de novo study of existing and newly collected specimens (e.g., Harris, 1989, 1990, 1995). The revision and reorganization of the collection that occurred during the 1980s led to the revelation that although large areas of the Americas remained poorly collected, patterns of biogeography, ecology and even phylogeny could be discerned even from the limited material available at that time. That this was the case was further affirmed by Harris during fieldwork in the West Indies carried out in tandem with bryologist William R. Buck’s (b. 1950) moss flora of that region (Buck, 1998). The pursuit of documenting and describing patterns of lichen biodiversity in the Americas led to the next stage in the development of the lichen herbarium: an ambitious program of biodiversity inventory. Modern growth: Phase 1 (1991–2006) Beginning in the early 1990s NYBG lichenologist Richard Harris and bryologist William Buck initiated a series of large scale lichen biodiversity inventories in eastern North America to parallel similar efforts that were underway throughout the
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West Indies and tropical South America, especially Brazil. Their first inventory covered the biologically diverse subtropical and tropical regions of southeastern North America, emphasizing the state of Florida. Subsequently, in collaboration with Douglas Ladd (b. 1953) of The Nature Conservancy, Missouri Chapter, they capitalized on the knowledge and experience gained from working in the Southeast and carried out a large scale study of the lichens of the Ozark Highlands, one the longest continuously exposed land areas on Earth. Concurrent with their inventory work, Harris and Buck established the Tuckerman Workshop, a (mostly) yearly field-meeting of professionals, advanced amateurs and students. The goal of the workshop was to facilitate knowledge transfer from a dwindling number of academic professionals to a body of skilled amateurs and students who could carry on the legacy of lichenology in North America until such a time when museums and universities would again hire lichenologists. During each workshop a group of ten to forty participants would meet to inventory field sites
in a concentrated geographic area that was of some biological interest and hosted significant natural areas (Buck, in press). Thus in addition to major efforts in Florida and the Ozarks, the NYBG researchers were able to conduct intensive inventories of smaller areas throughout the eastern United States and Canada over a period of more than 25 years (Fig. 1). The inventory efforts outlined above constituted the first phase of modern growth in lichen collection at NYBG. This phase, spanning sixteen years, established a trajectory of yearly accessions averaging 4,780+1542 collections and totaling 76,495, of which 37,327 were specimens newly collected by NYBG staff (Fig. 2). Indeed, during this period the collection grew from 103,868 to 176,530 accessioned specimens, an increase of 74% in less than two decades. Many of the specimens collected during this phase were recognized as undescribed species, more than one hundred of which were described by Harris during this period (see summary in Buck, 2009). Although large numbers of additional species that were new to science remained undescribed, these
FIG. 1. Locations of biodiversity inventory work carried out by Richard Harris and William Buck prior to 2006, with locations color-coded by decade.
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FIG. 2. Bar graph illustrating composition of newly accessioned lichen specimens 1990–2014.
were organized in the herbarium where new collections continued to accrue until time and resources were available to permit formal description. A particularly important aspect of this phase of growth was that Harris implemented a strict system of quality control wherein the identification of all newly accessioned specimens, regardless of whether received from others or collected by staff scientists, was verified prior to being incorporated into the herbarium. Though time consuming, this step was implemented primarily for pragmatic reasons (specimens were filed eight-per herbarium sheet and misidentified specimens would have to be removed and then affixed to different sheets). The downstream result after 16 years was that the identification and voucher data associated with much of the herbarium, especially for collections from eastern North America, had been carefully examined and verified. Thus a standard of high quality vetted data was established and maintained, encapsulating patterns of morphological and chemical characters as well as evolutionary history that would not otherwise have emerged. While rapid growth and output of taxonomic research occurred during the first phase of modern growth, the education and outreach efforts undertaken as part of the lichen research program also bore fruit. Participants of the Tuckerman Workshop increased their expertise, leading to
publications authored by newly trained amateurs (Dirig, 1990; May, 1997; Sheard & May, 1997; Hinds & Hinds, 1998, 2007; Printzen & May, 2002; Lay, 2004; LaGreca et al., 2005). Similarly, many graduate students who participated in workshops and other training completed their doctoral research in lichenology, publishing important contributions to lichen taxonomy, floristics and phylogenetics (Amtoft et al., 2008; Gueidan et al., 2009; Howe & Lendemer, 2011; Lendemer, 2013; McMullin, 2015). Among those trained as part of educational and outreach efforts was the first author of the present study, who attended Tuckerman Workshops from 2004 onwards, took part in the biodiversity inventory of the Ozarks, and eventually arrived at NYBG in 2007 to pursue an advanced degree in lichenology. Modern growth: Phase 2 (2007–present) If the first phase of modern growth in NYBG lichenology was characterized by substantial increases in collections, publications and outreach, the second phase can be defined by a further upward trend in activity. The second phase was initiated when the first author, James C. Lendemer (b. 1984), arrived at NYBG, leading to extensive collaboration between two full time lichen researchers, as well as a centralization in New York of a collaborative network of lichenologists
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FIG. 3. Cumulative accessions in the NYBG lichen herbarium 1990–2014.
carrying out taxonomic research on North American lichens. The nine years that elapsed from 2007 to 2016 saw an abrupt increase in the trajectory of yearly accessions, averaging 10,927+1476 collections and totaling 87,418, of which 48,083 were newly collected by NYBG staff (Fig. 2). While it took a century for the lichen herbarium to amass 103,868 accessions, and two decades for that to increase by 74% to 176,530, the second phase of modern growth resulted in an increase to 258,301 which constituted growth of an additional 79% from the end of the first phase in 2006
(Fig. 3). This number does not include many of the lichenicolous fungi, which are intercalated with their relatives in the NYBG Fungus Herbarium. The importance of well-curated, high quality biodiversity data anchored in verifiable natural history collections is a basic tenet of research in the biological sciences and conservation. Nonetheless, very few such resources were available for lichens in North America in the early 2000s. This was due to the fact that large scale biodiversity inventories on the continent had largely
FIG. 4. Comparison of georeferenced lichen voucher specimens collected by NYBG staff (right) and by individuals other than NYBG staff (left) in North America and surrounding regions.
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neither been taxonomically comprehensive (i.e., including crustose lichens and lichenicolous fungi) nor carried out by teams of highly trained experts with strict sampling protocols designed to facilitate comparisons across various scales and between studies in different areas. Capitalizing on the inventory program established by Harris and Buck, Lendemer initiated further large scale lichen biodiversity inventories to complement existing resources in the NYBG herbarium. The goal of these inventories being to both improve coverage of the lichen collection while simultaneously establishing modern baseline lichen biodiversity data to parallel that available for other better-studied taxonomic groups such as vertebrates and vascular plants. The first inventory, of the Commonwealth of Pennsylvania carried out in collaboration with the Western Pennsylvania Conservancy, confirmed that large scale studies of lichen biodiversity could be used to substantially advance both science and conservation. This effort was followed by inventories of the Great Smoky Mountains, Mid-Atlantic Coastal Plain, and southern Appalachian Mountains. A crucial advance in Phase 2 was the decision to database all newly accessioned specimens as they were incorporated into the collection. Importantly, databasing of new accessioned material included both full determination history and georeferencing of locality data, two steps that though time-intensive, substantially increased the value and usability of the data. The databasing of new accessions was then also complemented by systematic efforts to digitize existing holdings in the herbarium through targeted databasing of specific taxonomic groups and geographic regions that were relevant to research undertaken at NYBG. Although only roughly half of the NYBG lichen herbarium had been completely databased by 2016, the number of databased and georeferenced specimens totals more than 130,000 records that effectively cover large areas of North America and the West Indies (Fig. 4). It is important to note that education and outreach formed important components of all the activities carried out during the second phase of modern growth in the NYBG lichen herbarium. The Tuckerman Workshops that began more than 20 years earlier continue to train new lichenologists, foster collaboration, and promote knowledge transfer between generations of professionals and amateurs (see Buck, in press). NYBG lichenologists, their collaborators, and graduate students
routinely give presentations to the public, to colleagues at scientific meetings, teach courses at biological stations and NYBG, and advance appreciation for lichens through both traditional print publications and newer online media platforms. Conclusion The collective result of combining large scale verification and revision of natural history collections implemented in Phase 1, together with large scale databasing implemented in Phase 2, has been to vastly improve accessibility to the NYBG lichen biodiversity data. Further it has facilitated its use in the interdisciplinary studies that characterize the current Biodiversity Information Synthesis. While research continues to advance understanding of lichen taxonomy, systematics, biogeography, and ecology, these studies now broadly capitalize upon BBig Data^ resources established, maintained, and expanded for nearly four decades by NYBG scientists. Concurrently, these data and the studies that result from them increasingly inform conservation and management of species and ecosystems both directly and indirectly (Lendemer & Allen, 2014; Allen & Lendemer, 2015). In an era where biodiversity and society are ever more challenged by changing climates and ecosystem degradation, the lichen herbarium at NYBG stands as a unique resource that simultaneously documents the past and present while serving to illuminate possibilities for the future.
Acknowledgments The authors thank the reviewers of the manuscript for their helpful comments and constructive criticism.
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