WORKSHOP Asian Germplasm in American Horticulture: New Thoughts on an Old Theme Richard T. Olsen1 U.S. Department of Agriculture/Agricultural Research Service U.S. National Arboretum, Floral and Nursery Plants Research Unit, 10300 Baltimore Avenue, Beltsville, MD 20705 Additional index words. cultivated flora, disjuncts, invasive species, national access, ornamentals, plant exploration Abstract. North American horticulture cultivates an astonishing diversity of ornamental species, from nearly every floristic region, but its landscapes are dominated by temperate species drawn from eastern Asia. The East Asiatic floristic region is one of the most diverse in the world with a high level of endemism across taxonomic ranks and ancient relicts of a once widespread flora. From this, a large number of ornamental genera and species have been introduced, from either a long history of cultivation in Asia or directly from the wild, where they have since become fixtures in European and American gardens. The success of Asian germplasm in American horticulture is attributable, in part, to a shared evolutionary history, climate matching, and pre-adaptability. Continuing access to these genetic resources is now governed by national legislation and influenced by an evolving international regime of access and benefit-sharing influenced by the Convention on Biological Diversity. Furthermore, updated plant quarantine regulations have added additional requirements for the importation of foreign plant genetic resources. The newly created category within the USDA Animal and Plant Health Inspection Service (APHIS) Q37 regulations known as ‘‘not authorized pending pest risk analysis’’ (NAPPRA) restricts the import of plants for planting that may harbor pests or become pests that are not already established within the United States. To this end, scientists involved in the collection or use of Asian plant genetic resources are affected by recent changes in international and national laws, regulations, and access and benefit-sharing regimes.

‘‘The journey was over. But only the (Goetsch et al., 2005)—and past and future turned to Holland with plants of commercial journey. Not the exploration. This would prospects for Asian germplasm in American merit. Tea (Camellia sinensis), so widely cul- be continued, year after year, at the horticulture. tivated in eastern Asia, made its appearance flowering of the rhododendrons, in many in Dutch gardens by the 1680s at the same an English garden.’’ HISTORICAL CONTEXT time as the indian azalea (Rhododendron indicum) and garden mum (Chrysanthemum Francis Kingdon Ward (1937) The integration of Asian germplasm into ·morifolium) (Bretschneider, 1898). These The allure of plant exploration—journeys American horticulture is so pervasive that early introductions were often purchases made to exotic lands, the thrill of botanical discov- plants of Asiatic origin are ubiquitous com- from vendors in the ports of call; in fact, as a eries, and successful introduction of novel ponents of American gardens, from the result of heavy travel restrictions on foreigners germplasm—has entranced generations of signature plantings of evergreen azaleas in China and Japan, it was often the only horticulturists. From a plant centric view, (Rhododendron subgenus Tsutsusi)inthe means of procuring plants (Spongberg, 1990; the 19th century was the golden age of botany South to the cold-hardy deciduous Korean Tyler-Whittle, 1970). (Coats, 1970) which, combined with the Chi- rhododendrons (Rhododendron mucronulatum) The earliest but limited forays by traders noiserie aesthetic sweeping Europe, turned in the North and the florist azaleas (Rhodo- and missionaries from ports into the interiors botanical interests toward eastern Asia (Tyler- dendron simsii hybrids) cultivated through- of China and Japan in the late 17th and early Whittle, 1970). Francis Kingdon Ward (1885– out. Other genera first described from the 18th centuries provided new glimpses at the 1958) was one of the last of the collectors of European or American flora and cultivated in diversity and horticultural opportunities of the golden age of plant exploration, which our early gardens were invigorated by the the East Asian flora. For historical, techno- ended with the political upheavals in East Asia influx of their Asian congeners as well, logical, and geopolitical reasons, China and during the middle of the 21st century. Ward, including: barberries (Berberis), boxwood Japan were among the last frontiers opened to and much of the Western garden world, was (Buxus), forsythia (Forsythia), irises (Iris), Western botanists and horticulturists, where enamored with the genus Rhododendron. peonies (Paeonia), and roses (Rosa). How- plant explorers would be immortalized in This genus illustrates both the tremendous ever, many genera were completely new, Latin with their eponymous discoveries. diversity of species that occur in East Asia—as being either endemic to eastern Asia (Hosta The early physician-cum-naturalists such high as 90% of known Rhododendron species and Hemerocallis) or disjunct with North as Andreas Cleyer (e.g., Cleyera) and Eng- America (Hamamelis and Stewartia), but lebert Kaempfer (e.g., Kaempferia) stationed quickly embraced by gardeners. Moreover, in Japan in the 1680s and 1690s, respectively, many of these new introductions had already provided descriptions and images but appar- Received for publication 9 July 2013. Accepted for been cultivated for centuries in their respec- ently no living specimens of the Japanese publication 2 Aug. 2013. The mention of trade names or commercial products tive Chinese, Korean, or Japanese homelands garden flora. The first European to systemat- in this article is solely for the purpose of providing (Bretschneider, 1882–1895). The first living ically collect in China, albeit mostly as her- specific information and does not imply recommen- plants arriving by ship back to Europe af- barium specimens, was James Cunningham dations or endorsement by the U.S. Department ter the Portuguese ‘‘rediscovery’’ of China (e.g., Cunninghamia), a surgeon for the of Agriculture. The USDA is an equal opportunity (1511) and Japan (1543) were, like in the British East India Company (Bretschneider, employer. days of the Silk Road, of economic and 1898). In 1701, Cunningham was stationed This paper was part of the workshop ‘‘Good Genes agricultural importance such as the sweet in the trading port of Chusan (Zhoushan), from Asia—Contributions and Opportunities of orange (Citrus sinensis), which was either where he was able to collect 1000 specimens Asiatic Origin Crops to U.S. Horticulture’’ held introduced (Bretschneider, 1898) or reintro- representing nearly 600 species, including 3rd Aug. 2012 at the ASHS Conference, Miami, FL, and sponsored by the Working Group of Asian duced (Almeida, 2011; Gildemeister, 1913) such ornamentals as Acer buergerianum, Horticulture and The Association of Horticulturists in 1545. In the 17th century, the Iberian Camellia japonica, Gardenia jasminoides, of Indian Origin. monopoly on trade with eastern Asia was and Impatiens balsimina (Bretschneider, 1898). 1To whom reprint requests should be addressed; broken, in no small way by the Dutch East A frustratingly slow, and far from method- e-mail [email protected]. India Company, whose trade ships often re- ical, introduction of plants from eastern

HORTSCIENCE VOL. 48(9) SEPTEMBER 2013 1073 Asiacontinuedsuchthatbytheendofthe of the globe, yet by virtue of a predominantly latitude than eastern North America. Qian 18th century, relatively few ornamentals temperate climate, relies heavily on plants and Ricklefs (2000, 2004) have shown that were established in North America through derived from the Holarctic kingdom, the the number of genera per unit area (diversity) Europe, but these included the tree of heaven dominant floristic kingdom of the northern is greatest below this latitude, which corre- (Ailanthus altissima), ginkgo (Gingko biloba), hemisphere. The modern temperate flora is sponds in North America to the Gulf of crapemyrtle (Lagerstroemia indica), and jap- derived from an ancient boreotropical flora Mexico. The topography of eastern Asian is anese scholar tree (Styphnolobium japonicum) that spread during the warm, early Paleogene much more heterogeneous than eastern North (Rehder, 1940). Period (65 to 23 mya) through land bridges America with sharp contrasts in elevation Full-time plant collecting in East Asia that connected the northern hemisphere con- resulting in isolation of high-altitude forests began in the 19th century with the deploy- tinents. During the cooling climates of the by surrounding lowland subtropical or trop- ment of William Kerr (e.g., Kerria) by Kew Neogene Period (23 to 2.6 mya), this flora ical areas, especially at lower latitudes. Ac- in 1803. The invention of the Wardian case in evolved into a widespread mixed mesophytic cess and intermixing with tropical areas, 1834 for protecting live plants during long forest (Milne, 2006; Xiang and Soltis, 2001). coupled with gradients in elevation, would ocean voyages—because this was still pref- A floristic break between the New World have provided greater refugia for taxa escap- erable to seed collections (Tyler-Whittle, and Old World gradually grew as the North ing the effects of climate cooling and glaci- 1970)—significantly increased the success Atlantic land bridge fragmented in the Eo- ations during the late Paleogene and Neogene rate for introductions. This new technology cene Epoch (56 to 34 mya) separating North in eastern Asia than in North America (Guo was used heavily by Robert Fortune (e.g., America and Eurasia, whereas the break with and Ricklefs, 2000; Qian and Ricklefs, 2000, Fortunearia) who, under the auspices of the eastern Asia was completed much more re- 2004; Qian et al., 2003). As a result, eastern Royal Horticultural Society, began collecting cently, during the start of the Pliocene Epoch Asia has a greater number of endemic, relict in China in 1843. By the middle of the 19th (5.3 to 1.8 mya) (Milne, 2006; Milne and gymnosperm (e.g., Cathaya, Ginkgo, Metase- century, both China and Japan were effec- Abbott, 2002). The historically East Coast- quoia) and early diverging angiosperm genera tively opened through actual military action centric horticulture community in the U.S. (e.g., Cercidiphyllum, Davidia, Euptelea, Sino- (Opium Wars, 1839–60) or threat of military gardens in the North American Atlantic flo- wilsoniana) (Li, 2008; Qian et al., 2006) and action (Treaty of Kanagawa, 1854), respec- ristic region that encompasses the better part thus is often referred to as a ‘‘museum’’ of tively, and the golden age of plant explora- of the continental United States from the diversity (Li, 2008). To this title, one can now tion begun (Coats, 1970; Spongberg, 1990). Atlantic to Gulf States and through the Great add ‘‘cradle’’ of diversity. Xiang et al. (2004) The proverbial flood gates were open, and Plains. This floristic region is linked through compared net speciation rates for 10 disjunct numerous professional and amateur plant a common evolutionary path to the Eastern genera between eastern Asia and North Amer- hunters made contributions to the introduc- Asiatic floristic region, which encompasses ica using substitution rates for internal tran- tion of ornamental plants from Asia through parts of Far East Russia, the Korean peninsula, scribed spacer of nuclear ribosomal DNA the first decades of the 21st century. Bretsch- Japan, Taiwan, and mainland China to the sequence data for sister-species pairs and neider’s treatise on the early plant explora- eastern Himalayas. demonstrated that species richness increased tions in eastern Asia (1898) forms the basis The East Asiatic floristic region is one of as branch lengths increased with longer branch for chapters on Asia in contemporary works the most diverse in the world with a high lengths in eastern Asian species suggestive of on plant hunting (Coats, 1970; Spongberg, level of endemism across taxonomic ranks more rapid molecular evolution. They con- 1990; Tyler-Whittle, 1970) or works specific and ancient relicts of a once widespread flora. cluded that speciation rates in eastern Asia to Asia (e.g., Cox, 1961). Combined with the The flora of China (eFloras, 2013), which were greater than in North America and have biographies of notable plant hunters in Asia covers the majority of this region, has an played a significant role in the diversity [e.g., F.N. Meyer (Cunningham, 1984)], their estimated 31,318 species of vascular plants anomaly between the two floras (Xiang et al., travelogues (e.g., Ward, 1937; Wilson, 1913), (Li, 2008), or roughly 10% of the world’s 2004). enumerations of the collected flora [e.g. Plan- flora (Paton et al., 2008). Although the flora tae Wilsonianae (Sargent, 1913–1917)], and of North America has a shared evolutionary CURRENT GERMPLASM ISSUES historical plant records (e.g., U.S. Department past with eastern Asia, the diversity is asym- of Agriculture’s Germplasm Resource Infor- metrical with one-third less species (20,000 The exploration and importation of plants, mation Network: ), a comprehensive ar- (Flora of North America Editorial Commit- from East to West. North American plants, chive exists for researchers of ornamental tee, 1993+). This ‘‘diversity anomaly’’ is best especially conifers and popular broadleaf horticulture and botany. illustrated through the disparity in the num- trees, started to make their way into Chinese ber of species within genera disjunct between landscapes by the end of the 19th century FLORISTIC CONNECTIONS the two continents. Of the 100 or so disjunct (Sheng, 1979). By the 1940s, at least 14 genera genera, roughly half contain more species in of North American trees could be found in ‘‘Greatest of all the collecting districts, eastern Asia than in North America, whereas Chinese botanical gardens and landscapes; by for more than a century the most prolific only 26% have more species in North America the 1970s, that number would increase to 50 source of flowering plants in all the world, (Guo and Ricklefs, 2000; Qian and Ricklefs, genera (Sheng, 1979). The golden age of plant lay at the heart of Asia. Part was in India, 2004; Qian et al., 2003). This results in nearly exploration that ended with war and political and part in Burma, more in Tibet, most of twice as many East Asian species as North upheavals in Asia during the middle of the all in the three Chinese provinces of American for these disjunct genera (Qian and 21st century left both Western and Eastern Kansu, Szechuan, and Yunnan.’’ Ricklefs, 1999). Ornamentally significant horticulturists wanting for continued botani- Michael S. Tyler-Whittle (1970) genera illustrating this difference in species cal exchanges. numbers include Hydrangea (45 in Asia vs. Post-World War II ornamental plant ex- Explorations that reached the interior, five in North America), Lindera (80 vs. three), ploration in Asia by Americans is best illus- mountainous regions of southwestern China Osmanthus (15 vs. three) and Stewartia (nine trated by the activities of the U.S. Department and the Himalayas underscored the floristic vs. two) (Guo and Ricklefs, 2000). Explaining of Agriculture (USDA) Plant Introduction relationships emerging between East Asia this diversity anomaly calls on geological, Station at Glenn Dale, MD, and the New and North America that were identified by geographical, and climatic variables as well Crops Research Branch (NCRB), which led early botanists of the Linnaean period and as new molecular analyses. Eastern Asia spans plant exploration trips to Japan, Korea, north- expounded on by Asa Gray (Boufford and nearly 60 in latitude from tropical to polar ern India, and central Asia in lieu of access to Spongberg, 1983; Wen, 1999, 2001). North climates, the largest unbroken north–south China (Creech, 1968; Hodge and Loomis, American ornamental horticulture includes landmass in the northern hemisphere, with 1956). The U.S. National Arboretum (USNA) examples from nearly every floristic region significantly more landmass south of 30 N assumed leadership of ornamental crop

1074 HORTSCIENCE VOL. 48(9) SEPTEMBER 2013 introduction within the USDA after the clo- scientists to capitalize on its plant diversity to national access, China, Japan, and the sure of the NCRB in 1972, leading additional (Chen and Chen, 2006; Li and Zhou, 2005; Republic of Korea have mechanisms in place, collection trips to Japan, Korea, and finally Liu et al., 2003; Zhang and Dirr, 2004; Zhang although the degree to which these are en- China (Cunningham, 1987, 1988a, 1988b, et al., 1998; Zhao and Zhang, 2003). Zhao capsulated in their respective national laws 1988c). The 1980 Sino-American Botanical and Zhang (2003) highlight the ornamental is unclear. Long-established USDA policy Expedition was the first by American scientists plant resources of China, reviewing the in- mandates that materials in the National Plant into China since 1949 with USNA scientists herent diversity, contributions, and potential Germplasm System (NPGS) must be freely collecting and handling germplasm introduc- of its flora. They list 86 genera of globally available without restrictions and thus neces- tion and distribution to participants (Dosmann relevant ornamental genera where 50% of the sitates applicable agreements with source coun- and del Tredici, 2003). This joint expedition species are found in China. Rhododendrons tries. Best practices for in situ germplasm was the culmination of renewed relations be- are the extreme example with an estimated collecting include obtaining prior informed tween Chinese and North American botanical 650 out of 800 species in the world found in consent from the designated national author- institutes, aimed at capacity-building in China China (Zhao and Zhang, 2003). A number of ities; the involvement of host-country stake- through scientific exchange with peer insti- these genera have species that were intro- holders, researchers, or repositories; and the tutes in North America. A unifying theme was duced or reintroduced to the United States in establishment of mutually agreed terms for the need for further collaboration on floristic the 1990s such as Edgeworthia chrysantha procedures and limitations relating to benefits- surveys, taxonomic study, and conservation of and Distylium myricoides (Ward, 2004), yet sharing (Moore and Williams, 2011). Recent the flora of East Asia. By the 1990s, access for have already resulted in novel cultivars (E. NPGS plant explorations have been con- collecting in China was relatively open, and chrysantha ‘Gold Rush’, ‘Snow Cream’, and ducted in nations (e.g., Armenia, Azerbaijan, multiple expeditions were mounted in collab- ‘Winter Gold’) or contributed to new hybrids the Republic of Georgia) where the USDA oration with partner institutions of the North (e.g., Distylium ‘PIIDIST-I’ Emerald HeightsÒ has access and benefit-sharing agreements in America–China Plant Exploration Consor- and ‘PIIDIST-II’ Blue CascadeÒ)intheAmer- place. The breakup of the Soviet Union and tium (NACPEC), which sought to discover, ican nursery trade. Likewise, as the ornamen- rise of independent states in the Caucasus and reintroduce, and broaden the genetic diver- tal plant industry develops in China, advanced Central Asia provided access to these impor- sity available in cultivation for important selections and hybrids will join those from tant, and poorly documented, centers of bio- Chinese ornamental taxa (Aiello and Dosmann, Japan and Korea as exports to nursery markets diversity, resulting in 38 collecting trips since 2010; Meyer, 2010). Since 1991, NACPEC has like the United States. One introduction that 2000, including six for woody ornamental conducted 12 explorations, collecting 1261 portends this new trend is Taxodium ‘Nanjing landscape plants (Hellier, 2011). Recent living accessions, of which 698 are extant Beauty’, a hybrid between T. distichum and T. explorations in China have been limited to (A. Aiello, unpublished data). The genus mucronatum bred by the Nanjing Botanical instances when clear collecting objectives Acer (maples) was specifically targeted by Garden and introduced by the Stephen F. Austin focusing on specific genera facilitated access, NACPEC because China is the center of State University in 2004 (Creech et al., 2011). for instance targeting Chinese ash (Fraxinus diversity for the genus with 113 of the esti- As the 21st century progresses, a new plant spp.) for collecting novel germplasm to screen mated 156 species worldwide (Gibbs and Chen, from eastern Asia will increasingly be an for emerald ash borer resistance (Bachtell and 2009; Xu et al., 2008). Acer was the most advanced hybrid that competes in the global Siegel, 2010). collected genus, making up nearly 10% of market. The richness of the East Asian flora and original and extant accessions. Furthermore, Globalization and technology may have the generally conservative nature of adapta- the collections of Acer highlight an impor- increased physical access to plant genetic re- tions of plants to their environments (Qian tant facet of modern germplasm collecting. sources; however, legal access and subsequent and Ricklefs, 2004) have led to successful Although the collecting of new species is still use and conservation of these resources have introduction, cultivation, and integration of desired, more often than not, established in some cases been obfuscated by rapidly novel plant germplasm into American horti- species are recollected to extend the range evolving national legislation and international culture. Unfortunately, some too success- of intraspecific variation captured, sample benefit-sharing regimes. For many nations, the fully, because 29% of documented invasive new provenances that may confer greater genetic diversity within its jurisdiction is now plant species in the eastern United States adaptability to biotic or abiotic stresses, and viewed as a national resource requiring formal originates from East Asia (Fridley, 2008). ultimately increase the genetic diversity in access and benefit-sharing arrangements The majority, especially woody ornamentals, cultivation to aid in conserving threatened (National Research Council, 1991; Williams, were deliberate introductions for horticul- species ex situ. 2005). In some cases, the international re- tural use (Reichard and White, 2001). The Introductions in this second golden age of gimes for access and benefit-sharing have introduction of invasive insect pests and path- plant exploration were not limited to botanists been influenced by provisions of the Conven- ogens is another unintended byproduct of plant or academics, because more ready access and tion on Biodiversity (CBD). Article 15 of the introductions and the globalization of plant modern transportation meant more industry CBD covers access and benefits, specifically trade. Liebold et al. (2012) reviewed non- professionals and laypersons could contribute. recognizing the sovereign rights of states over native forest pests introduced in the United Collectively, these private, public, and aca- their natural resources and the authority to States in the last 150 years and found 70% of demic explorations have significantly increased determine access and fair and equitable shar- insect pests and 47% of forest pathogens could the number of East Asian taxa in cultivation. ing of benefits arising from their use (). When it comes increased volume in the live plant trade, where troductions to cultivation’’ by Grimshaw and into force, the Nagoya Protocol on Access to up to 12% of shipments are visibly infested, Bayton (2009), new tree species introduced Genetic Resources and the Fair and Equi- but as much of 72% of infestations go un- into cultivation in Europe and North America table Sharing of Benefits Arising from their detected, has created the need for updated in the last 40 years are reviewed. Of the 800+ Utilization might serve as the mechanism quarantine regulations (Liebold et al., 2012). species in 180 genera covered, 47% of them for guiding the development of national The USDA APHIS regulates the importa- came from China and the Sino-Himalayan benefit-sharing protocols and conditions for tion of live plants through Title 7 of the Code region, often through the efforts of individ- access (). The United of Federal Regulations, Part 319, Section 37 uals unassociated with botanical gardens or States is a signatory of the CBD but has not regulations ‘‘Nursery Stock, Plants, Roots, other institutions. ratified the treaty so is therefore not a party. All Bulbs, Seeds, and Other Plant Products’’ or The development of and access to a bo- of the countries in eastern Asia are parties to the Q37 for short. Before 2011, non-fruit or vege- tanical infrastructure in China, although in- CBD; however, only Japan and the Republic of table plants for importing were either pro- creasing opportunities for individual plant Korea have signed the Nagoya Protocol but hibited or restricted entry. In 2011, APHIS collectors and researchers, has also created neither has ratified it (< http://www.cbd.int/abs/ proposed amendments to the regulation that opportunities for Chinese horticulturists and nagoya-protocol/signatories/>). With regard would drop the use of ‘‘nursery stock’’ in favor

HORTSCIENCE VOL. 48(9) SEPTEMBER 2013 1075 of ‘‘plants for planting,’’ defined as plants CONCLUDING THOUGHTS Cunningham, I.S. 1987. The U.S. National Arbo- intended to remain planted, to be planted, or retum: Leader in ornamental plant germplasm replanted by the International Plant Protection American horticulture is intimately con- collection. Part 1. Diversity 12:20–21. Convention’s (IPPC) glossary of phytosanitary nected to Asia through the shared evolution- Cunningham, I.S. 1988a. The U.S. National Arbo- terms (). Plants are enrichment of our cultivated floras through plant exploration and exchange. The conti- Cunningham, I.S. 1988b. The U.S. National Arbo- defined by the IPPC as living plants and parts retum: Leader in ornamental plant germplasm thereof, including seed and germplasm. nuity of this connection is assured, because collection. Part 3. Diversity 14:28–29. The amendments created a new category, there is an ongoing need to revisit, reintro- Cunningham, I.S. 1988c. The U.S. National Arbo- NAPPRA, to restrict the import of plants for duce, and reinvent our ornamental plants retum: Leader in ornamental plant germplasm planting that may harbor pests or become through the use of Asian germplasm whose collection. Part 4. Diversity 15:33–34. pests themselves (§319.37-2a). The intent is flora is at once a storehouse and a driver of Dosmann, M. and P. del Tredici. 2003. Plant to use available scientific literature to identify genetic diversity. Although Chinese, Japanese, introduction, distribution, and survival: A case plant taxa that are quarantine pests or host and Korean plant genetic resources have study of the 1980 Sino-American botanical quarantine pests, give public notice of the been, and will continue to be, important for expedition. Bioscience 53:588–597. eFloras. 2013. 22 Jan. 2012. . Missouri Botanical Garden, St. Louis, MO, provide sufficient time for public comment, and Harvard University Herbaria, Cambridge, occurring as they open their borders. As a and the opportunity to conduct a pest risk MA. assessment to remove a taxon from the list result of their own set of political and histor- Flora of North America Editorial Committee (ed.). (). These changes to the Q37 regula- flora, are in need of much of the same UK. tions are a precursor to a consolidation of collaboration and capacity-building as seen Fridley, J.D. 2008. Of Asian forests and European federal codes that address all regulations for in China at the end of the 20th century. Future fields: Eastern U.S. plant invasions in a global plants for plantings into a simpler, easier-to efforts, in any country, are dependent on col- floristic context. PLoS One 3:1–7. Gibbs, D. and Y. Chen. 2009. The red list of maples. read and update format. 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