Collections in the Plant Research Laboratory of The New York Botanical Garden LISA M. CAMPBELL New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, USA; e-mail: [email protected]

Abstract. The Plant Research Laboratory at The New York Botanical Garden maintains a variety of research samples for biodiversity studies. The collections are the products of botanical exploration, laboratory research, collaborations, and donations from the scientific community. These collections are enumerated, and information about herbarium voucher specimens, the history of the collections, and their current use is provided. Key Words: Botanical research collections, DNA repository, leaf venation, microscope slides, phytochemistry, pollen, resin.

Among the resources at The New York Botanical Garden (NYBG) supporting diverse avenues of research are those housed in the Plant Research Laboratory (PRL). The collections are used by NYBG researchers and the national and international scientific community for investigations on descriptive (e.g., Gustafsson, 2000) and comparative plant anatomy (e.g., Carlquist, 1960) and morphology (e.g., Campbell & Stevenson, 2007); phylogeny (e.g., Labiak et al., 2014) and systematics (e.g., Goldenberg et al., 2015); genomics (e.g., Pabón Mora et al., 2015); DNA barcoding (e.g., Little, 2014); phytochemistry (e.g., Meurer-Grimes & Stevenson, 1994); conservation (see Sastre-D. & Santiago-Valentín, 1996); paleo-botany and ecology; archaeology (e.g., Lentz & Dickau, 2005); human health (e.g., see Maguire, Mertz Library Archives); laboratory techniques (e.g., Vasco et al., 2014); and collections management (e.g., Campbell et al., 2012). Laboratory collections are instrumental in the Garden’s training of graduate students (see Lentz & Bellengi, 1996; Kelly, 2016, this issue) and post-doctoral researchers (e.g., Nicolas & Plunkett, 2012). They have been used to illustrate presentations to educational groups and public audiences, and are a reference tool for non-commercial applied fields, such as forensics and human health. The Laboratory collections have a long history, but have experienced pronounced growth during two initiatives at the Garden: botanical exploration for the 1953–1989 Flora of the Guayana

Highland series by Bassett Maguire and Collaborators (Howard & Boom, 1990; Boom, 1996a; see Buck, 1990 for full citations), and the development of the Cullman Program for Molecular Systematics (Boom, 1996b), established in 1994 in collaboration with the American Museum of Natural History (Stevenson, 2016, this issue). This paper summarizes the research collections housed in the PRL (http://www.nybg.org/sciencenew/tour/lab-collections.php), their development, and provides selected references of their current use.

Structural botany collections The collections and preparations housed in the PRL are mostly the products of research conducted at NYBG, emphasizing taxa from the Americas, and the collections have strength in Pteridophytes; cycads and other gymnosperms; monocots, particularly palms, orchids, and Poales; Clusiaceae; and Ericales. The taxonomic and geographic scope has been broadened through preparations, such as microscope slides, made from NYBG collections returned by other researchers (e.g., Acanthaceae, S. Glasl-Tazreiter, pers. comm.); through exchange (L. Klebieko, pers. com.; Mertz Library Archives); and through donations of samples and preparations from retired researchers. These include Charles J. Chamberlain’s cycad and gymnosperm liquid-preserved samples, and

Brittonia, DOI 10.1007/s12228-016-9425-5 ISSN: 0007-196X (print) ISSN: 1938-436X (electronic) © 2016, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

BRITTONIA

microscope slides and embedded pteridophyte samples from Alma G. Stokey and Lenette R. Atkinson. The most substantial donation was from Barbara Palser in 1993 at the time of her retirement from a career of research and mentoring students on the anatomy of Ericales and Saxifragaceae. Palser’s material reflects the global distribution of Ericaceae, particularly northern and southern hemisphere temperate taxa. One hundred collectors supplied her with samples (http://www.nybg.org/science-new/explore/laboratory-research.php) that were fixed for anatomical research; many are vouchered in several herbaria, including CHRB, MO, and NY. LIQUID PRESERVED COLLECTIONS

The liquid preserved collections are estimated to contain about 9000 samples. Growth of the collection escalated from specimens made for the Flora of the Guayana Highland, gatherings that include many endemic genera and species, and samples from tepuis and other remote areas that are now difficult to revisit. These collections have been eclipsed in volume by continued botanical exploration in that region (e.g., see Colella-Franco, 1999) and elsewhere (see Boom, 1996a; Thomas, 2016), as well as taxon-based foci, and the large donation from Palser. In addition to the plant groups mentioned above, the liquid preserved collection includes Richard White’s substantial specimens of tree ferns (e.g., see Lucansky & White, 1976), and numerous collections of Lobelioids from Hawaii, and Proteaceae collected in Australia. A section of the growing collection is maintained for teaching purposes.

[VOL

MICROSCOPE SLIDE COLLECTION

The microscope slide collection is organized as a pollen slide collection contained in a single cabinet (Fig. 1) and boxes of slides made for individual’s anatomical and systematic research, and teaching. About 3700 pollen slides were prepared under the direction of Bassett Maguire during his tenure as Senior Curator (see Fig. 11 in Howard & Boom, 1990) for use in research on systematics, palynology, paleoecology, and human health (López-Martínez et al., 2010) and now are also applied to interpreting the effects of climate change (e.g., Rull et al., 2013). A majority of these were prepared to advance the knowledge of plant groups occurring on the Guiana Shield (e.g., see Struwe et al., 2002). Other microscope slides, also documenting pollen morphology (e.g., Campbell & Stevenson, 2007) and other plant morphology and anatomy, may amount to 10,000 in number. The largest number are Ericales, including Lecythidaceae (e.g., Tsou, 1993), Clethraceae, Ericaceae from the Andes (e.g., Luteyn, 1983), and especially the Ericaceae floral slides produced during Palser’s prolific career. Slides for teaching plant structure and diversity occupy about 200 boxes.

LEAF CLEARINGS

This modest collection is mostly of cycads (Stevenson, 1990); monocots, including palms and reticulate-leaved taxa (e.g., Conover, 1991), and Ericales (e.g., Huang et al., 2008; Fig. 2). Others prepared from NYBG specimens are housed in the National Cleared Leaf Collection at the

FIG. 1. The pollen microscope slide collection at The New York Botanical Garden. The sealed slides are stored horizontally in numeric order.

2016]

CAMPBELL: LABORATORY COLLECTIONS

FIG. 2. Cleared leaf of Coccoloba uvifera L.

Smithsonian Institution (http://peabody.research. yale.edu/nclc/), some via the Peabody Museum, Yale University. Voucher specimens are mostly at NY; others are at F, GH, and MO (Conover, 1991). THE N. L. BRITTON AND P. WILSON REFERENCE SEED COLLECTION

This collection was begun in the late 1800s with collections made in the vicinity of the Gar-

den. The geographic scope was quickly broadened, reflecting the interest of Nathaniel L. Britton and his colleagues in documenting the flora of southern Florida (e.g., Small, 1913; Mertz Library Archives), the Bahamas (e.g., Britton & Millspaugh, 1920), and West Indies (Boom, 1996a; Sastre-D. & Santiago-Valentín, 1996). Although the collection is global in extent, currently, about 70 percent of the seed samples are from the U.S.A. and Caribbean. The nearly 3000 samples representing 145 plant families are primarily used as an identification tool (Fig. 3) in conjunction with the herbarium specimens and other resources in the William and Lynda Steere Herbarium (NY; see Pace et al., 2016, this issue) and Library (e.g., Fraser & Wheeler, 2016, this issue). Fabales, Fagales, and palms (Arecaceae) are the taxonomic groups with the largest number of samples. Numerous collectors have contributed to the Seed Collection. The most prolific collector was Percy Wilson (Fig. 4), Britton’s assistant, and later Associate Curator. He apparently strove to grow the collection (Gleason, 1944), which has increased by ninety percent since Britton’s 1929 retirement. More recent accessions include a large number from the Jardín Botánico de Cienfuegos

FIG. 3. The N. L. Britton and P. Wilson Reference Seed Collection (New York Botanical Garden).

[VOL

BRITTONIA

University in 1899, were sent to the Peabody Museum (Yale University) in 1983 (Mertz Library Archives). The majority of wood samples collected by NYBG staff continue to be sent, along with voucher specimens, to the USDA Forest Service Xylarium, University of Wisconsin, Madison (MADw; http://www.fpl.fs.fed.us/research/centers/woodanatomy/index.php). Additionally, some of the collections from the Flora of the Guayana Highland program were exchanged with the Institute of Systematic Botany, Utrecht University, or sent to experts in particular taxonomic groups (e.g., Baretta-Kuipers, 1976). DNA repository These collections were described in Campbell et al. (2012). Tissue samples are from the geographic foci of NYBG’s biodiversity exploration, whereas the genomic DNA samples emphasize taxonomic groups studied by staff and collaborators. Herbarium specimen vouchers are at NY and/or in host country herbaria. Phytochemical collections J. H. LANGENHEIM RESIN COLLECTION

FIG. 4. Percy Wilson, Associate Curator, New York Botanical Garden, who was instrumental in developing the Reference Seed Collection (reprinted from the Journal of The New York Botanical Garden 45, 1944).

through the national garden’s (Havana, Cuba) first seed exchange (U.H. & A.C.C., 1968; Fig. 5), and an appended collection of conifer cones made from the Garden’s Beneson Ornamental Conifer Collection. Fossils and wood samples were never an emphasis of the PRL collections, although a minor number of specimens utilized in individuals’ research and teaching are kept in the Laboratory (e.g., fossils for cycad and gymnosperm research; Ericaceae wood). Larger collections of wood and fossil samples, formerly housed within the Steere Herbarium, were dispersed to institutions with active research programs using and curating these specimens (e.g., Hickey, 1973; Cassens & Miller, 1981), making them accessible to the scientific community. The Garden’s fossil collection, including those transferred from Columbia 1

Collections made from the garden in Cienfuegos in 1968 are attributed to Ovidio Ponce and R. Castillo (E. R. Bécquer, pers. comm.).

This collection was donated to NYBG (2003) when Jean H. Langenheim retired from the University of California Santa Cruz after a distinguished career (Langenheim, 2010). The collection comprises 590 samples of copal and fossilized resin and incorporates the collections for her students’ doctoral studies and those used by N. T. Mirov for his research on Pinus (Mirov 1961, 1967). Samples were collected throughout the world, and all of the major useful resinous plant f a m i l i e s ( S i m p s o n & O g o r z a l y, 2 0 0 1 ; Langenheim, 2003) are represented; the collection contains many Dipterocarpaceae, and Hymenaea copal from Brazil. These collections were the foundation for research conducted by Langenheim (see Langenheim, 2003) and students (Lee & Langenheim, 1975; Gianno, 1986, 2003) on the chemistry, structural and ecological distribution, and human use of resins. Some resin samples associated with Henry H. Rusby are housed with the Langenheim collection, whereas others are curated in other NYBG collections. The resin collections continue to be used by researchers in the field of plant exudate chemistry (e.g., Lambert et al., 2010), and in forensic research on artifacts (e.g., A. Harrison, Smithsonian Institution, pers. comm.).

2016]

CAMPBELL: LABORATORY COLLECTIONS

FIG. 5. Index Seminum from the Jardín Botánico Nacional de Cuba from which seed samples were accessioned in the Reference Collection at The New York Botanical Garden. A. Cover of the first issue (1968). B. Page of seed offerings showing 414 Syagrus flexuosa Becc. C. Seed sample of S. flexuosa (the collection number is obscured at the lower right on the label).

BRITTONIA PHYTOCHEMICAL SURVEY COLLECTIONS

In addition to herbarium specimen vouchers, NYBG’s past participation in biodiversity prospecting resulted in about 45,000 laboratory samples. These projects were collaborations with several organizations that analyzed the alcohol based extracts produced in the PRL and further developed promising constituents. Samples were collected in the Americas, Europe, South Africa, Asia, and the Pacific, representing a broad spectrum of vascular plants. A reference library of extracts is maintained and the dried tissue samples retained to voucher the extracts have been successfully used to amplify DNA. In conclusion, it is worth noting that other NYBG resources greatly augment the value of the Laboratory Collections: the Steere Herbarium, houses and curates most voucher specimens—many are databased, georeferenced, and digitized, allowing rapid identification for researchers and specialists worldwide (http://sweetgum.nybg.org/science/); collectors’ field notebooks and correspondence referencing the collections archived in the Mertz Library; and laboratory facilities, including a scanning electron microscope and computer cluster, for routine and complex sample processing and data analysis. Acknowledgments The efforts of numerous technicians, students, and volunteers who physically curated and cataloged the PRL collections, thus preserving their integrity and enhancing their accessibility, is gratefully acknowledged. E. R. Bécquer Granados (HAJB); L. Klebieko, M. Tulig, K. Watson, A. Weiss (Steere Herbarium); S. Sinon and J. Dorfman (Mertz Library) provided collections information for this manuscript or assistance with the web references cited herein. P. K. Holmgren and D. W. Stevenson made valuable comments on an earlier draft of this manuscript. Collections refurbishment and curation was supported by the National Science Foundation (BRC-0846412 and DBI-1203278).

Literature cited Baretta-Kuipers, T. 1976. Comparative wood anatomy of Bonnetiaceae, Theaceae and Guttiferae. Leiden Botanical Series 3: 76–101.

[VOL

Boom, B. M. 1996a. Botanical expeditions of The New York Botanical Garden. Brittonia 48: 297–284. ———. 1996b. One hundred years of botanical research and scholarly publishing at The New York Botanical Garden. An introduction to the historical issue of Brittonia. Brittonia 48: 281–306. Britton, N. L. & C. F. Millspaugh. 1920. The Bahama flora. Published by the authors, NY. Buck, W. R. 1990. Indices to BThe Botany of the Guayana Highland^. Memoirs of The New York Botanical Garden 64: 45–122. Campbell, L. M. & D. Wm. Stevenson. 2007. Inflorescence architecture and floral morphology of Aratitiyopea lopezii (Xyridaceae). Aliso 23: 227–233. ———, M. E. Quenzer, G. Dröge, J. Simpson, A. Kirchgessner & M. Tulig. 2012. Tissue and DNA banking at The New York Botanical Garden. Collections Forum 26: 120–129. Carlquist, S. 1960. Anatomy of Guayana Xyridaceae: Abolboda, Orectanthe, and Achlyphila. Memoirs of The New York Botanical Garden 10(2): 65–117. Cassens, D. L. & R. B. Miller. 1981. Wood anatomy of the New World Pithecellobium (sensu lato). U.S. Forest Products Laboratory, Madison, WI. Colella-Franco, M. 1999. Systematic placement of Rapateaceae (Commelinales). Ph.D. dissert., City University of New York. Photocopy: UMI Dissertation Services, Ann Arbor, MI. Conover, M. V. 1991. Epidermal patterns of the reticulateveined Liliiflorae and their parallel-veined allies. Botanical Journal of the Linnean Society 107: 295–312. Fraser, S. & D. Wheeler. 2016, this issue. The LuEsther T. Mertz Library: The evolution of a modern, digitally integrated botanical library. Brittonia 68(3). Gianno, R. 1986. Resin classification among the Semelai of Tasek Bera, Pahang, Malaysia. Economic Botany 40: 186– 200. ———. 2003. Semelai culture and resin technology. Memoirs of the Connecticut Academy of Arts and Sciences 22. Gleason, H. A. 1944. Percy Wilson—an appreciation. Journal of The New York Botanical Garden. 45: 49–53. Goldenberg, R., F. Almeda, K. Sosa, R. C. Ribeiro & F. A. Michelangeli. 2015. Rupestrea: A new Brazilian genus of Melastomataceae, with anomalous seeds and dry indehiscent fruits. Systematic Botany 40: 561–571. Gustafsson M. H. G. 2000. Floral morphology and relationships of Clusia gundlachii with a discussion of floral organ identity and diversity in the genus Clusia. International Journal of Plant Sciences 161: 43–53. Hickey, L. J. 1973. Classification of the architecture of dicotyledonous leaves. American Journal of Botany 60: 17–33. Howard, R. A. & B. M. Boom. 1990. Bassett Maguire—An annotated biography. Memoirs of The New York Botanical Garden 64: 1–28. Huang, Y.-Y., S. A. Mori & G. T. Prance. 2008. A phylogeny of Cariniana (Lecythidaceae) based on morphological and anatomical data. Brittonia 60: 69–81. Kelly, L. 2016, this issue. Training the next generation: Graduate studies at The New York Botanical Garden, with emphasis on 1996–2015. Brittonia 68(3). Labiak, P. H., M. Sundue, G. Rouhan, J. Garrison Hanks, J. T. Mickel & R. C. Moran. 2014. Phylogeny and historical biogeography of the lastreopsid ferns

2016]

CAMPBELL: LABORATORY COLLECTIONS

(Dryopteridaceae). American Journal of Botany 101: 1207–1228. Lambert, J. B., E. A. Heckenbach, Y. Wu & J. A. SantiagoBlay. 2010. Characterization of plant exudates by principal-component and cluster analyses with nuclear magnetic resonance variables. Journal of Natural Products 73: 1643–1648. Langenheim, J. H. 2003. Plant resins: Chemistry, evolution, ecology, and ethnobotany. Timber Press, Portland, OR. ———. 2010. The odyssey of a woman field scientist: A story of passion, persistence, and patience. Xlibris, Bloomington, IN. Lee, Yin-Tse & J. H. Langenheim. 1975. Systematics of the genus Hymenaea L. (Leguminosae, Caesalpinioideae, Detarieae). University of California Press, Berkeley. Lentz, D. L. & M. Bellengi. 1996. A brief history of the Graduate Studies Program at The New York Botanical Garden. Brittonia 48: 404–412. ——— & R. Dickau. 2005. Seeds of Central America and southern Mexico: the Economic species. Memoirs of The New York Botanical Garden 91. Little, D. P. 2014. Authentication of Ginkgo biloba herbal dietary supplements using DNA barcoding. Genome 57: 513–516. López-Martínez, C., A. Lara, V. Rull, L. Campbell & S. Nogué. 2010. Additions to the Pantepui pollen flora (Venezuelan Guayana): the Maguire collection. Collectanea Botanica 29: 31–49. Lucansky, T. W. & R. A. White. 1976. Comparative ontogenetic studies in young sporophytes of tree ferns. Part 1: A primitive and an advanced taxon. American Journal of Botany 63: 463–472. Luteyn, J. 1983. Ericaceae—Part I. Cavendishia. Flora Neotropica Monographs 35. Mirov, N. T. 1961. Composition of gum turpentines of pines. U.S. Dept. of Agriculture, Washington, DC. ———. 1967. The genus Pinus. Ronald Press Co., NY. Meurer-Grimes, B. & D. Stevenson. 1994. The biflavones of the Cycadales revisited: Biflavones in Stangeria eriopus, Chigua restrepoi and 32 other species of Cycadales. Biochemical Systematics and Ecology 22: 595–604. Nicolas, A. N. & G. M. Plunkett. 2012. Untangling Azorella, Laretia, and Mulinum (Apiaceae, Azorelloideae): Insights from phylogenetics and biogeography. Taxon 61: 826–840. Pabón Mora N., H. Suarez-Baron, B. A. Ambrose & F. González. 2015. Expression of perianth identity candidate genes in the basal angiosperm Aristolochia fimbriata (Aristolochiaceae). Frontiers in Plant Science 6: 1095. doi: 10.3389/fpls.2015.01095.

Pace, M. C., N. Tarnowski, E. D. Bloch, A. Weiss, C. Zimmerman & B. M. Thiers. 2016, this issue. An updated description of the collections and history of The New York Botanical Garden Herbarium (NY): 1995–2015. Brittonia 68(3). Rull, V. E. Montoya, S. Nogué, T. Vegas-Vilarrúbia & S. Safont. 2013. Ecological paleaeoecology in the neotropical Gran Sabana region: Long-term records of vegetation dynamics as a basis for ecological hypothesis testing. Perspectives in Plant Ecology, Evolution and Systematics 6: 338–349. Sastre-D. , I. J. & E. Santiago-Valentín. 1996. Botanical explorations of Puerto Rico by N. L. Britton and E. G. Britton: Their significance in plant conservation, horticulture, and education. Brittonia 48: 322–336. Simpson, B. B. & M. C. Ogorzaly. 2001. Economic botany: Plants in our world. McGraw-Hill, Boston. Small, J. K. 1913. The flora of the Florida Keys; being descriptions of the seed-plants growing naturally on the islands of the Florida reef from Virginia Key to Dry Tortugas. The Author, NY. Stevenson, D. W. 1990. Morphology and Systematics of the Cycadales. Memoirs of The New York Botanical Garden 57: 8–55. ———. 2016, this issue. 125 years of laboratory research in botany at The New York Botanical Garden. Brittonia 68(3). Struwe, L., J. W. Kadereit, J. Klackenberg, S. Nilsson, M. Thiv, K. B. von Hagen & V. A. Albert. 2002. Systematics, character evolution, and biogeography of Gentianaceae, including a new tribal and subtribal classification. Pp. 21–209. In: L. Struwe & V. A. Albert (eds). Gentianaceae: Systematics and natural history. Cambridge University Press, Cambridge. Thomas, W. W. 2016. 125 years of floristic research and collecting at The New York Botanical Garden. Brittonia 68(3) (this issue). Tsou, C.-H. 1993. Applications of comparative embryology to plant taxonomy—taking the Lecythidaceae as an example. Academia Sinica Monograph Series 13: 293–302. [U.H. & A.C.C.] Univeridad de la Habana & Academia de Ciencias de Cuba. 1968. Index Seminum. Havanna, Cuba. Vasco, A., M. Thadeo, M. Conover & D. C. Daly. 2014. Preparation of samples for leaf architecture studies, a method for mounting cleared leaves. Applications in Plant Sciences 2(9): 1400038. doi: http://dx.doi.org/10.3732/ apps.1400038.