Asian Germplasm in American Horticulture: New Thoughts on an Old Theme

in HortScience

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.

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 journey. Not the exploration. This would be continued, year after year, at the flowering of the rhododendrons, in many an English garden.”

Francis Kingdon Ward (1937)

The allure of plant exploration—journeys to exotic lands, the thrill of botanical discoveries, and successful introduction of novel germplasm—has entranced generations of horticulturists. From a plant centric view, the 19th century was the golden age of botany (Coats, 1970) which, combined with the Chinoiserie aesthetic sweeping Europe, turned botanical interests toward eastern Asia (Tyler-Whittle, 1970). Francis Kingdon Ward (1885–1958) was one of the last of the collectors of the golden age of plant exploration, which ended with the political upheavals in East Asia during the middle of the 21st century. Ward, and much of the Western garden world, was enamored with the genus Rhododendron. This genus illustrates both the tremendous diversity of species that occur in East Asia—as high as 90% of known Rhododendron species (Goetsch et al., 2005)—and past and future prospects for Asian germplasm in American horticulture.

HISTORICAL CONTEXT

The integration of Asian germplasm into American horticulture is so pervasive that plants of Asiatic origin are ubiquitous components of American gardens, from the signature plantings of evergreen azaleas (Rhododendron subgenus Tsutsusi) in the South to the cold-hardy deciduous Korean rhododendrons (Rhododendron mucronulatum) in the North and the florist azaleas (Rhododendron simsii hybrids) cultivated throughout. Other genera first described from the European or American flora and cultivated in our early gardens were invigorated by the influx of their Asian congeners as well, including: barberries (Berberis), boxwood (Buxus), forsythia (Forsythia), irises (Iris), peonies (Paeonia), and roses (Rosa). However, many genera were completely new, being either endemic to eastern Asia (Hosta and Hemerocallis) or disjunct with North America (Hamamelis and Stewartia), but quickly embraced by gardeners. Moreover, many of these new introductions had already been cultivated for centuries in their respective Chinese, Korean, or Japanese homelands (Bretschneider, 1882–1895). The first living plants arriving by ship back to Europe after the Portuguese “rediscovery” of China (1511) and Japan (1543) were, like in the days of the Silk Road, of economic and agricultural importance such as the sweet orange (Citrus sinensis), which was either introduced (Bretschneider, 1898) or reintroduced (Almeida, 2011; Gildemeister, 1913) in 1545. In the 17th century, the Iberian monopoly on trade with eastern Asia was broken, in no small way by the Dutch East India Company, whose trade ships often returned to Holland with plants of commercial merit. Tea (Camellia sinensis), so widely cultivated in eastern Asia, made its appearance in Dutch gardens by the 1680s at the same time as the indian azalea (Rhododendron indicum) and garden mum (Chrysanthemum ×morifolium) (Bretschneider, 1898). These early introductions were often purchases made from vendors in the ports of call; in fact, as a result of heavy travel restrictions on foreigners in China and Japan, it was often the only means of procuring plants (Spongberg, 1990; Tyler-Whittle, 1970).

The earliest but limited forays by traders and missionaries from ports into the interiors of China and Japan in the late 17th and early 18th centuries provided new glimpses at the diversity and horticultural opportunities of the East Asian flora. For historical, technological, and geopolitical reasons, China and Japan were among the last frontiers opened to Western botanists and horticulturists, where plant explorers would be immortalized in Latin with their eponymous discoveries. The early physician-cum-naturalists such as Andreas Cleyer (e.g., Cleyera) and Englebert Kaempfer (e.g., Kaempferia) stationed in Japan in the 1680s and 1690s, respectively, provided descriptions and images but apparently no living specimens of the Japanese garden flora. The first European to systematically collect in China, albeit mostly as herbarium specimens, was James Cunningham (e.g., Cunninghamia), a surgeon for the British East India Company (Bretschneider, 1898). In 1701, Cunningham was stationed in the trading port of Chusan (Zhoushan), where he was able to collect 1000 specimens representing nearly 600 species, including such ornamentals as Acer buergerianum, Camellia japonica, Gardenia jasminoides, and Impatiens balsimina (Bretschneider, 1898). A frustratingly slow, and far from methodical, introduction of plants from eastern Asia continued such that by the end of the 18th century, relatively few ornamentals were established in North America through Europe, but these included the tree of heaven (Ailanthus altissima), ginkgo (Gingko biloba), crapemyrtle (Lagerstroemia indica), and japanese scholar tree (Styphnolobium japonicum) (Rehder, 1940).

Full-time plant collecting in East Asia began in the 19th century with the deployment of William Kerr (e.g., Kerria) by Kew in 1803. The invention of the Wardian case in 1834 for protecting live plants during long ocean voyages—because this was still preferable to seed collections (Tyler-Whittle, 1970)—significantly increased the success rate for introductions. This new technology was used heavily by Robert Fortune (e.g., Fortunearia) who, under the auspices of the Royal Horticultural Society, began collecting in China in 1843. By the middle of the 19th century, both China and Japan were effectively opened through actual military action (Opium Wars, 1839–60) or threat of military action (Treaty of Kanagawa, 1854), respectively, and the golden age of plant exploration begun (Coats, 1970; Spongberg, 1990). The proverbial flood gates were open, and numerous professional and amateur plant hunters made contributions to the introduction of ornamental plants from Asia through the first decades of the 21st century. Bretschneider’s treatise on the early plant explorations in eastern Asia (1898) forms the basis for chapters on Asia in contemporary works on plant hunting (Coats, 1970; Spongberg, 1990; Tyler-Whittle, 1970) or works specific to Asia (e.g., Cox, 1961). Combined with the biographies of notable plant hunters in Asia [e.g., F.N. Meyer (Cunningham, 1984)], their travelogues (e.g., Ward, 1937; Wilson, 1913), enumerations of the collected flora [e.g. Plantae Wilsonianae (Sargent, 1913–1917)], and historical plant records (e.g., U.S. Department of Agriculture’s Germplasm Resource Information Network: <http://www.ars-grin.gov/npgs/searchgrin.html>), a comprehensive archive exists for researchers of ornamental horticulture and botany.

FLORISTIC CONNECTIONS

“Greatest of all the collecting districts, for more than a century the most prolific source of flowering plants in all the world, lay at the heart of Asia. Part was in India, and part in Burma, more in Tibet, most of all in the three Chinese provinces of Kansu, Szechuan, and Yunnan.”

Michael S. Tyler-Whittle (1970)

Explorations that reached the interior, mountainous regions of southwestern China and the Himalayas underscored the floristic relationships emerging between East Asia and North America that were identified by early botanists of the Linnaean period and expounded on by Asa Gray (Boufford and Spongberg, 1983; Wen, 1999, 2001). North American ornamental horticulture includes examples from nearly every floristic region of the globe, yet by virtue of a predominantly temperate climate, relies heavily on plants derived from the Holarctic kingdom, the dominant floristic kingdom of the northern hemisphere. The modern temperate flora is derived from an ancient boreotropical flora that spread during the warm, early Paleogene Period (65 to 23 mya) through land bridges that connected the northern hemisphere continents. During the cooling climates of the Neogene Period (23 to 2.6 mya), this flora evolved into a widespread mixed mesophytic forest (Milne, 2006; Xiang and Soltis, 2001). A floristic break between the New World and Old World gradually grew as the North Atlantic land bridge fragmented in the Eocene Epoch (56 to 34 mya) separating North America and Eurasia, whereas the break with eastern Asia was completed much more recently, during the start of the Pliocene Epoch (5.3 to 1.8 mya) (Milne, 2006; Milne and Abbott, 2002). The historically East Coast-centric horticulture community in the U.S. gardens in the North American Atlantic floristic region that encompasses the better part of the continental United States from the Atlantic to Gulf States and through the Great Plains. This floristic region is linked through a common evolutionary path to the Eastern Asiatic floristic region, which encompasses parts of Far East Russia, the Korean peninsula, Japan, Taiwan, and mainland China to the eastern Himalayas.

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. The flora of China (eFloras, 2013), which covers the majority of this region, has an estimated 31,318 species of vascular plants (Li, 2008), or roughly 10% of the world’s flora (Paton et al., 2008). Although the flora of North America has a shared evolutionary past with eastern Asia, the diversity is asymmetrical with one-third less species (≈20,000 species) present in all of North America (Flora of North America Editorial Committee, 1993+). This “diversity anomaly” is best illustrated through the disparity in the number of species within genera disjunct between the two continents. Of the 100 or so disjunct genera, roughly half contain more species in eastern Asia than in North America, whereas only 26% have more species in North America (Guo and Ricklefs, 2000; Qian and Ricklefs, 2004; Qian et al., 2003). This results in nearly twice as many East Asian species as North American for these disjunct genera (Qian and Ricklefs, 1999). Ornamentally significant genera illustrating this difference in species numbers include Hydrangea (45 in Asia vs. five in North America), Lindera (80 vs. three), Osmanthus (15 vs. three) and Stewartia (nine vs. two) (Guo and Ricklefs, 2000). Explaining this diversity anomaly calls on geological, geographical, and climatic variables as well as new molecular analyses. Eastern Asia spans nearly 60° in latitude from tropical to polar climates, the largest unbroken north–south landmass in the northern hemisphere, with significantly more landmass south of 30° N latitude than eastern North America. Qian and Ricklefs (2000, 2004) have shown that the number of genera per unit area (diversity) is greatest below this latitude, which corresponds in North America to the Gulf of Mexico. The topography of eastern Asian is much more heterogeneous than eastern North America with sharp contrasts in elevation resulting in isolation of high-altitude forests by surrounding lowland subtropical or tropical areas, especially at lower latitudes. Access and intermixing with tropical areas, coupled with gradients in elevation, would have provided greater refugia for taxa escaping the effects of climate cooling and glaciations during the late Paleogene and Neogene in eastern Asia than in North America (Guo and Ricklefs, 2000; Qian and Ricklefs, 2000, 2004; Qian et al., 2003). As a result, eastern Asia has a greater number of endemic, relict gymnosperm (e.g., Cathaya, Ginkgo, Metasequoia) and early diverging angiosperm genera (e.g., Cercidiphyllum, Davidia, Euptelea, Sinowilsoniana) (Li, 2008; Qian et al., 2006) and thus is often referred to as a “museum” of diversity (Li, 2008). To this title, one can now add “cradle” of diversity. Xiang et al. (2004) compared net speciation rates for 10 disjunct genera between eastern Asia and North America using substitution rates for internal transcribed spacer of nuclear ribosomal DNA sequence data for sister-species pairs and demonstrated that species richness increased as branch lengths increased with longer branch lengths in eastern Asian species suggestive of more rapid molecular evolution. They concluded that speciation rates in eastern Asia were greater than in North America and have played a significant role in the diversity anomaly between the two floras (Xiang et al., 2004).

CURRENT GERMPLASM ISSUES

The exploration and importation of plants, although not one way, was historically biased from East to West. North American plants, especially conifers and popular broadleaf trees, started to make their way into Chinese landscapes by the end of the 19th century (Sheng, 1979). By the 1940s, at least 14 genera of North American trees could be found in Chinese botanical gardens and landscapes; by the 1970s, that number would increase to ≈50 genera (Sheng, 1979). The golden age of plant exploration that ended with war and political upheavals in Asia during the middle of the 21st century left both Western and Eastern horticulturists wanting for continued botanical exchanges.

Post-World War II ornamental plant exploration in Asia by Americans is best illustrated by the activities of the U.S. Department of Agriculture (USDA) Plant Introduction Station at Glenn Dale, MD, and the New Crops Research Branch (NCRB), which led plant exploration trips to Japan, Korea, northern India, and central Asia in lieu of access to China (Creech, 1968; Hodge and Loomis, 1956). The U.S. National Arboretum (USNA) assumed leadership of ornamental crop introduction within the USDA after the closure of the NCRB in 1972, leading additional collection trips to Japan, Korea, and finally China (Cunningham, 1987, 1988a, 1988b, 1988c). The 1980 Sino-American Botanical Expedition was the first by American scientists into China since 1949 with USNA scientists collecting and handling germplasm introduction and distribution to participants (Dosmann and del Tredici, 2003). This joint expedition was the culmination of renewed relations between Chinese and North American botanical institutes, aimed at capacity-building in China through scientific exchange with peer institutes in North America. A unifying theme was the need for further collaboration on floristic surveys, taxonomic study, and conservation of the flora of East Asia. By the 1990s, access for collecting in China was relatively open, and multiple expeditions were mounted in collaboration with partner institutions of the North America–China Plant Exploration Consortium (NACPEC), which sought to discover, reintroduce, and broaden the genetic diversity available in cultivation for important Chinese ornamental taxa (Aiello and Dosmann, 2010; Meyer, 2010). Since 1991, NACPEC has conducted 12 explorations, collecting 1261 living accessions, of which 698 are extant (A. Aiello, unpublished data). The genus Acer (maples) was specifically targeted by NACPEC because China is the center of diversity for the genus with 113 of the estimated 156 species worldwide (Gibbs and Chen, 2009; Xu et al., 2008). Acer was the most collected genus, making up nearly 10% of original and extant accessions. Furthermore, the collections of Acer highlight an important facet of modern germplasm collecting. Although the collecting of new species is still desired, more often than not, established species are recollected to extend the range of intraspecific variation captured, sample new provenances that may confer greater adaptability to biotic or abiotic stresses, and ultimately increase the genetic diversity in cultivation to aid in conserving threatened species ex situ.

Introductions in this second golden age of plant exploration were not limited to botanists or academics, because more ready access and modern transportation meant more industry professionals and laypersons could contribute. Collectively, these private, public, and academic explorations have significantly increased the number of East Asian taxa in cultivation. In the monumental “New trees: Recent introductions to cultivation” by Grimshaw and Bayton (2009), new tree species introduced into cultivation in Europe and North America in the last 40 years are reviewed. Of the 800+ species in 180 genera covered, 47% of them came from China and the Sino-Himalayan region, often through the efforts of individuals unassociated with botanical gardens or other institutions.

The development of and access to a botanical infrastructure in China, although increasing opportunities for individual plant collectors and researchers, has also created opportunities for Chinese horticulturists and scientists to capitalize on its plant diversity (Chen and Chen, 2006; Li and Zhou, 2005; Liu et al., 2003; Zhang and Dirr, 2004; Zhang et al., 1998; Zhao and Zhang, 2003). Zhao and Zhang (2003) highlight the ornamental plant resources of China, reviewing the inherent diversity, contributions, and potential of its flora. They list 86 genera of globally relevant ornamental genera where 50% of the species are found in China. Rhododendrons are the extreme example with an estimated 650 out of 800 species in the world found in China (Zhao and Zhang, 2003). A number of these genera have species that were introduced or reintroduced to the United States in the 1990s such as Edgeworthia chrysantha and Distylium myricoides (Ward, 2004), yet have already resulted in novel cultivars (E. chrysantha ‘Gold Rush’, ‘Snow Cream’, and ‘Winter Gold’) or contributed to new hybrids (e.g., Distylium ‘PIIDIST-I’ Emerald Heights® and ‘PIIDIST-II’ Blue Cascade®) in the American nursery trade. Likewise, as the ornamental plant industry develops in China, advanced selections and hybrids will join those from Japan and Korea as exports to nursery markets like the United States. One introduction that portends this new trend is Taxodium ‘Nanjing Beauty’, a hybrid between T. distichum and T. mucronatum bred by the Nanjing Botanical Garden and introduced by the Stephen F. Austin State University in 2004 (Creech et al., 2011). As the 21st century progresses, a new plant from eastern Asia will increasingly be an advanced hybrid that competes in the global market.

Globalization and technology may have increased physical access to plant genetic resources; however, legal access and subsequent use and conservation of these resources have in some cases been obfuscated by rapidly evolving national legislation and international benefit-sharing regimes. For many nations, the genetic diversity within its jurisdiction is now viewed as a national resource requiring formal access and benefit-sharing arrangements (National Research Council, 1991; Williams, 2005). In some cases, the international regimes for access and benefit-sharing have been influenced by provisions of the Convention on Biodiversity (CBD). Article 15 of the CBD covers access and benefits, specifically recognizing the sovereign rights of states over their natural resources and the authority to determine access and fair and equitable sharing of benefits arising from their use (<http://www.cbd.int/convention/text/>). When it comes into force, the Nagoya Protocol on Access to Genetic Resources and the Fair and Equitable Sharing of Benefits Arising from their Utilization might serve as the mechanism for guiding the development of national benefit-sharing protocols and conditions for access (<http://www.cbd.int/abs/>). The United States is a signatory of the CBD but has not ratified the treaty so is therefore not a party. All of the countries in eastern Asia are parties to the CBD; however, only Japan and the Republic of Korea have signed the Nagoya Protocol but neither has ratified it (< http://www.cbd.int/abs/nagoya-protocol/signatories/>). With regard to national access, China, Japan, and the Republic of Korea have mechanisms in place, although the degree to which these are encapsulated in their respective national laws is unclear. Long-established USDA policy mandates that materials in the National Plant Germplasm System (NPGS) must be freely available without restrictions and thus necessitates applicable agreements with source countries. Best practices for in situ germplasm collecting include obtaining prior informed consent from the designated national authorities; the involvement of host-country stakeholders, researchers, or repositories; and the establishment of mutually agreed terms for procedures and limitations relating to benefits-sharing (Moore and Williams, 2011). Recent NPGS plant explorations have been conducted in nations (e.g., Armenia, Azerbaijan, the Republic of Georgia) where the USDA has access and benefit-sharing agreements in place. The breakup of the Soviet Union and rise of independent states in the Caucasus and Central Asia provided access to these important, and poorly documented, centers of biodiversity, resulting in 38 collecting trips since 2000, including six for woody ornamental landscape plants (Hellier, 2011). Recent explorations in China have been limited to instances when clear collecting objectives focusing on specific genera facilitated access, for instance targeting Chinese ash (Fraxinus spp.) for collecting novel germplasm to screen for emerald ash borer resistance (Bachtell and Siegel, 2010).

The richness of the East Asian flora and the generally conservative nature of adaptations of plants to their environments (Qian and Ricklefs, 2004) have led to successful introduction, cultivation, and integration of novel plant germplasm into American horticulture. Unfortunately, some too successfully, because 29% of documented invasive plant species in the eastern United States originates from East Asia (Fridley, 2008). The majority, especially woody ornamentals, were deliberate introductions for horticultural use (Reichard and White, 2001). The introduction of invasive insect pests and pathogens is another unintended byproduct of plant introductions and the globalization of plant trade. Liebold et al. (2012) reviewed non-native forest pests introduced in the United States in the last 150 years and found 70% of insect pests and 47% of forest pathogens could be attributed to the trade in live plants. The increased volume in the live plant trade, where up to 12% of shipments are visibly infested, but as much of 72% of infestations go undetected, has created the need for updated quarantine regulations (Liebold et al., 2012).

The USDA APHIS regulates the importation of live plants through Title 7 of the Code of Federal Regulations, Part 319, Section 37 regulations “Nursery Stock, Plants, Roots, Bulbs, Seeds, and Other Plant Products” or Q37 for short. Before 2011, non-fruit or vegetable plants for importing were either prohibited or restricted entry. In 2011, APHIS proposed amendments to the regulation that would drop the use of “nursery stock” in favor of “plants for planting,” defined as plants intended to remain planted, to be planted, or replanted by the International Plant Protection Convention’s (IPPC) glossary of phytosanitary terms (<https://www.ippc.int/publications/glossary-phytosanitary-terms>). Plants are defined by the IPPC as living plants and parts thereof, including seed and germplasm. The amendments created a new category, NAPPRA, to restrict the import of plants for planting that may harbor pests or become pests themselves (§319.37-2a). The intent is to use available scientific literature to identify plant taxa that are quarantine pests or host quarantine pests, give public notice of the intent to add a taxon to the NAPPRA list, provide sufficient time for public comment, and the opportunity to conduct a pest risk assessment to remove a taxon from the list (<http://www.aphis.usda.gov/import_export/plants/plant_imports/Q37/nappra/index.shtml>). These changes to the Q37 regulations are a precursor to a consolidation of federal codes that address all regulations for plants for plantings into a simpler, easier-to read and update format. Accordingly, the importation of all plants, with few exceptions, requires a phytosanitary certificate from the country of origin and are prohibited, restricted, or not authorized pending pest risk analysis.

The importance and need for these new regulations, as they affect woody ornamental plants, is illustrated effectively with just one potential insect pest, the citrus longhorned beetle (CLB) (Anoplophora chinensis). CLB is a wood-boring insect with both an extensive natural range and host plant list in Asia, that unlike its relative, the asian longhorned beetle (Anoplophora glabripennis), is spread through live plants rather than wood packaging. CLB has been detected on multiple occasions at inspection stations and on one occasion discovered but eradicated in a commercial nursery (Liebold et al., 2012). Seventy-two genera are listed as plant hosts for CLB and, with some exceptions, are prohibited to import. The prohibited list includes a significant number of important ornamental genera: Acer, Aesculus, Betula, Camellia, Catalpa, Cercis, Cornus, Cotoneaster, Cryptomeria, Fagus, Hibiscus, Ilex, Lagerstroemia, Liquidambar, Malus, Pinus, Platanus, Prunus, Pyrus, Quercus, Rhododendron, Rosa, Salix, Styrax, Ulmus, and Viburnum. The NAPPRA designation prohibits all but seeds and cut flowers or greenery for these taxa until individual pest risk analyses have been conducted. Seed collection efforts to enhance germplasm collections or botanical exchange are unaffected. However, the importation of asexual propagules is effectively prohibited and thus severely impacts nursery exports from eastern Asia of novel plant genetic resources. The nursery industry, researchers, and regulators will need new and sustained collaborations aimed at identifying specific risk mitigation procedures for NAPPRA taxa to assure future imports of asexual propagules of these important ornamental taxa.

CONCLUDING THOUGHTS

American horticulture is intimately connected to Asia through the shared evolutionary paths of our respective native floras and enrichment of our cultivated floras through plant exploration and exchange. The continuity of this connection is assured, because there is an ongoing need to revisit, reintroduce, and reinvent our ornamental plants through the use of Asian germplasm whose flora is at once a storehouse and a driver of genetic diversity. Although Chinese, Japanese, and Korean plant genetic resources have been, and will continue to be, important for North American horticulture, new explorations to Myanmar, Laos, and Vietnam are occurring as they open their borders. As a result of their own set of political and historical circumstances, these Southeast Asian countries, rich in mountainous Sino-Himalayan flora, are in need of much of the same collaboration and capacity-building as seen in China at the end of the 20th century. Future efforts, in any country, are dependent on collaborative efforts among governments, institutes, industry, and individuals to assure proper access and use of plant genetic resources. From the earliest days of plant exploration, the plant diversity of eastern Asia was viewed through the lens of commercialization. Although still an important component, the need for conserving this diversity, and protecting North America’s, has gained importance as habitat loss, urbanization, invasive species, and climate change come to bear on our collective floras.

Literature Cited

  • AielloA.DosmannM.S.2010By the numbers: Twenty years of NACPEC collectionsArnoldia682039

  • AlmeidaD.P.F.2011Asian crops in Renaissance Europe as a result of the discoveries: Bypassing the Silk RoadActa Hort.9168392

  • BachtellK.R.SiegelO.2010Chinese ashes, Fraxinus sppArnoldia687374

  • BouffordD.E.SpongbergS.A.1983Eastern Asian–eastern North American phytogeographical relationships—A history from the time of Linnaeus to the twentieth centuryAnn. Mo. Bot. Gard.70423439

    • Search Google Scholar
    • Export Citation
  • BretschneiderE.1882–1895Botanicum sinicum: Notes on Chinese botany from native and western sources. 3 Vol. Trubner London UK

  • BretschneiderE.1898History of European botanical discoveries in China. S. Low Marston London UK

  • ChenL.ChenD.2006Endemic ornamental plant resources in ChinaActa Hort.7142128

  • CoatsA.M.1970The plant hunters: Being a history of the horticultural pioneers their quests and their discoveries from the Renaissance to the twentieth century. McGraw-Hill New York NY

  • CoxE.H.M.1961Plant hunting in China; A history of botanical exploration in China and the Tibetan marches. Oldbourne London UK

  • CreechD.ZhouL.YunlongY.Eguiluz-PiedraT.2011Can Taxodium be improved?Arnoldia691120

  • CreechJ.L.1968The ARS-Longwood plant explorationsPlants and Gardens235056 86

  • CunninghamI.S.1984Frank N. Meyer: Plant hunter in Asia. Iowa State University Ames IA

  • CunninghamI.S.1987The U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 1Diversity122021

  • CunninghamI.S.1988aThe U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 2Diversity132324

  • CunninghamI.S.1988bThe U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 3Diversity142829

  • CunninghamI.S.1988cThe U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 4Diversity153334

  • DosmannM.del TrediciP.2003Plant introduction, distribution, and survival: A case study of the 1980 Sino-American botanical expeditionBioscience53588597

    • Search Google Scholar
    • Export Citation
  • eFloras201322 Jan. 2012. <http://www.efloras.org>. Missouri Botanical Garden St. Louis MO and Harvard University Herbaria Cambridge MA

  • Flora of North America Editorial Committee (ed.). 1993+. Flora of North America North of Mexico. 16+ Vols. New York NY and Oxford UK

  • FridleyJ.D.2008Of Asian forests and European fields: Eastern U.S. plant invasions in a global floristic contextPLoS One317

  • GibbsD.ChenY.2009The red list of maples. Bot. Gardens Conserv. Intl. Richmond UK

  • GildemeisterE.1913The volatile oils by E. Gildemeister and Fr. Hoffmann. 2nd Ed. Wiley New York NY

  • GoetschL.EckertA.J.HallB.D.2005The molecular systematic of Rhododendron (Ericaceae): A phylogeny based upon RPB2 gene sequencesSyst. Bot.30616626

    • Search Google Scholar
    • Export Citation
  • GrimshawJ.BaytonR.2009New trees: Recent introductions to cultivation. Kew Publishing Royal Botanic Gardens Kew UK

  • GuoQ.RicklefsR.E.2000Species richness in plant genera disjunct between temperate eastern Asia and North AmericaBot. J. Linn. Soc.134401423

    • Search Google Scholar
    • Export Citation
  • HellierB.C.2011Collecting in central Asia and the Caucasus: U.S. National Plant Germplasm System plant explorationsHortScience4614381439

    • Search Google Scholar
    • Export Citation
  • HodgeW.H.LoomisH.F.1956Federal plant introduction gardensNat. Hort. Mag.3586106

  • LiD.-Z.2008Floristics and plant biogeography in ChinaJ. Intergrative Plant Biol.50771777

  • LiX.-X.ZhouZ.-K.2005Endemic wild ornamental plants from northwestern Yunnan, ChinaHortScience4016121619

  • LieboldA.M.BrockerhoffE.G.GarrettL.J.ParkeJ.L.BrittonK.O.2012Live plant imports: The major pathway for forest insect and pathogen invasions of the USFront. Ecol. Environ10135143

    • Search Google Scholar
    • Export Citation
  • LiuK.ZhangD.WangX.2003Hunan (China) flora with rich ornamental plantsActa Hort.620403409

  • MeyerP.2010The return to China, mother of gardensArnoldia68411

  • MilneR.I.2006Northern hemisphere plant disjunctions: A window on tertiary land bridges and climate change?Ann. Bot. (Lond.)98465472

  • MilneR.I.AbbottR.J.2002The origin and evolution of tertiary relict florasAdv. Bot. Res.38281314

  • MooreG.WilliamsK.2011Legal issues in plant germplasm collecting. In: Guarino L. R.V. Ramanatha and E. Goldberg (eds.). Collecting plant genetic diversity: Technical guidelines—2011 update. Bioversity International Rome Italy. 26 June 2013. <http://cropgenebank.sgrp.cgiar.org/index.php?option=com_content&view=article&id=390&Itemid=557>

  • National Research Council1991Managing global genetic resources: The U.S. National Plant Germplasm system. National Academy Press Washington DC

  • PatonA.J.BrummittN.GovaertsR.HarmanK.HinchcliffeS.AllkinB.LughadhaE.N.2008Towards target 1 of the global strategy for plant conservation: A working list of all known plant species—Progress and prospectsTaxon57602611

    • Search Google Scholar
    • Export Citation
  • QianH.RicklefsR.E.1999A comparison of the taxonomic richness of vascular plants in China and the United StatesAmer. Nat.154160181

  • QianH.RicklefsR.E.2000Large-scale processes and the Asian bias in species diversity of temperate plantsNature407180182

  • QianH.RicklefsR.E.2004Geographical distribution and ecological conservatism of disjunct genera of vascular plants in eastern Asia and eastern North AmericaJ. Ecol.92253265

    • Search Google Scholar
    • Export Citation
  • QianH.SongJ.-S.KrestovP.GuoQ.WuZ.ShenX.GuoX.2003Large-scale phytogeographical patterns in East Asia in relation to latitudinal and climatic gradientsJ. Biogeogr.30129141

    • Search Google Scholar
    • Export Citation
  • QianH.WangS.HeJ.-S.ZhangJ.WangL.WangX.GuoK.2006Phytogeographical analysis of seed plant genera in ChinaAnn. Bot. (Lond.)9810731084

    • Search Google Scholar
    • Export Citation
  • RehderA.1940Manual of cultivated trees and shrubs hardy in North America exclusive of the subtropical and warmer temperate regions. 2nd Ed. Macmillan New York NY

  • ReichardS.H.WhiteP.2001Horticulture as a pathway of invasive plant introductions in the United StatesBioscience51103113

  • SargentC.S. (ed.). 1913–1917Plantae Wilsonianae; An enumeration of the woody plants collected in western China for the Arnold arboretum of Harvard university during the years 1907 1908 and 1910 by E.H. Wilson. 3 Vol. Cambridge University Cambridge MA

  • ShengC.K.1979Introduction of North American trees into ChinaArnoldia39271277

  • SpongbergS.A.1990A reunion of trees: The discovery of exotic plants and their introduction into North American and European landscapes. Harvard Univ. Press Cambridge MA

  • Tyler-WhittleM.S.1970The plant hunters. Chilton Philadelphia PA

  • WardB.J.2004The plant hunter’s garden: The new explorers and their discoveries. Timber Press Portland OR

  • WardF.K.1937Plant hunter’s paradise. Jonathan Cape London UK

  • WenJ.1999Evolution of eastern Asian and eastern North American disjunct distributions in flowering plantsAnnu. Rev. Ecol. Syst.30421455

    • Search Google Scholar
    • Export Citation
  • WenJ.2001Evolution of eastern Asian–eastern North American biogeographic disjunctions: A few additional notesIntl. J. Plant Sci.S117S122

    • Search Google Scholar
    • Export Citation
  • WilliamsK.A.2005An overview of the U.S. National Plant Germplasm System’s exploration programHortScience40297301

  • WilsonE.H.1913A naturalist in western China with vasculum camera and gun: Being some account of eleven years’ travel exploration and observation in the more remote parts of the flowery kingdom. Doubleday Page New York NY

  • XiangQ.Y.SoltisD.E.2001Dispersal-vicariance analyses of intercontinental disjuncts: Historical biogeographical implications for angiosperms in the northern hemisphereIntl. J. Plant Sci.S29S39

    • Search Google Scholar
    • Export Citation
  • XiangQ.Y.ZhangW.H.RicklefsR.E.QianH.ChenZ.D.WenJ.LiJ.H.2004Regional differences in rates of plant speciation and molecular evolution: A comparison between eastern Asia and eastern North AmericaEvolution5821752184

    • Search Google Scholar
    • Export Citation
  • XuT.ChenY.de JongP.C.OterdoomH.J.ChangC.-S.2008Aceraceae: Acer p. 516–553. In: Wu Z. and P.H. Raven (eds.). Flora of China. Vol. 11. Scientific Press Beijing China

  • ZhangD.DirrM.A.2004Potential new ornamental plants from China. Proc. Southern Nurs. Res. Conf. 49:607–609

  • ZhangD.T.LasseigneT.DirrM.1998A survey of Chinese native plants of potential ornamental and economic value for the southeastern United StatesJC Raulston Arboretum Newsletter3–92735

    • Search Google Scholar
    • Export Citation
  • ZhaoL.ZhangD.2003Ornamental plant resources from ChinaActa Hort.620365375

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Contributor Notes

The mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendations or endorsement by the U.S. Department of Agriculture. The USDA is an equal opportunity employer.

This paper was part of the workshop “Good Genes from Asia—Contributions and Opportunities of Asiatic Origin Crops to U.S. Horticulture” held 3rd Aug. 2012 at the ASHS Conference, Miami, FL, and sponsored by the Working Group of Asian Horticulture and The Association of Horticulturists of Indian Origin.

To whom reprint requests should be addressed; e-mail Richard.Olsen@ars.usda.gov.

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Article References

  • AielloA.DosmannM.S.2010By the numbers: Twenty years of NACPEC collectionsArnoldia682039

  • AlmeidaD.P.F.2011Asian crops in Renaissance Europe as a result of the discoveries: Bypassing the Silk RoadActa Hort.9168392

  • BachtellK.R.SiegelO.2010Chinese ashes, Fraxinus sppArnoldia687374

  • BouffordD.E.SpongbergS.A.1983Eastern Asian–eastern North American phytogeographical relationships—A history from the time of Linnaeus to the twentieth centuryAnn. Mo. Bot. Gard.70423439

    • Search Google Scholar
    • Export Citation
  • BretschneiderE.1882–1895Botanicum sinicum: Notes on Chinese botany from native and western sources. 3 Vol. Trubner London UK

  • BretschneiderE.1898History of European botanical discoveries in China. S. Low Marston London UK

  • ChenL.ChenD.2006Endemic ornamental plant resources in ChinaActa Hort.7142128

  • CoatsA.M.1970The plant hunters: Being a history of the horticultural pioneers their quests and their discoveries from the Renaissance to the twentieth century. McGraw-Hill New York NY

  • CoxE.H.M.1961Plant hunting in China; A history of botanical exploration in China and the Tibetan marches. Oldbourne London UK

  • CreechD.ZhouL.YunlongY.Eguiluz-PiedraT.2011Can Taxodium be improved?Arnoldia691120

  • CreechJ.L.1968The ARS-Longwood plant explorationsPlants and Gardens235056 86

  • CunninghamI.S.1984Frank N. Meyer: Plant hunter in Asia. Iowa State University Ames IA

  • CunninghamI.S.1987The U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 1Diversity122021

  • CunninghamI.S.1988aThe U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 2Diversity132324

  • CunninghamI.S.1988bThe U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 3Diversity142829

  • CunninghamI.S.1988cThe U.S. National Arboretum: Leader in ornamental plant germplasm collection. Part 4Diversity153334

  • DosmannM.del TrediciP.2003Plant introduction, distribution, and survival: A case study of the 1980 Sino-American botanical expeditionBioscience53588597

    • Search Google Scholar
    • Export Citation
  • eFloras201322 Jan. 2012. <http://www.efloras.org>. Missouri Botanical Garden St. Louis MO and Harvard University Herbaria Cambridge MA

  • Flora of North America Editorial Committee (ed.). 1993+. Flora of North America North of Mexico. 16+ Vols. New York NY and Oxford UK

  • FridleyJ.D.2008Of Asian forests and European fields: Eastern U.S. plant invasions in a global floristic contextPLoS One317

  • GibbsD.ChenY.2009The red list of maples. Bot. Gardens Conserv. Intl. Richmond UK

  • GildemeisterE.1913The volatile oils by E. Gildemeister and Fr. Hoffmann. 2nd Ed. Wiley New York NY

  • GoetschL.EckertA.J.HallB.D.2005The molecular systematic of Rhododendron (Ericaceae): A phylogeny based upon RPB2 gene sequencesSyst. Bot.30616626

    • Search Google Scholar
    • Export Citation
  • GrimshawJ.BaytonR.2009New trees: Recent introductions to cultivation. Kew Publishing Royal Botanic Gardens Kew UK

  • GuoQ.RicklefsR.E.2000Species richness in plant genera disjunct between temperate eastern Asia and North AmericaBot. J. Linn. Soc.134401423

    • Search Google Scholar
    • Export Citation
  • HellierB.C.2011Collecting in central Asia and the Caucasus: U.S. National Plant Germplasm System plant explorationsHortScience4614381439

    • Search Google Scholar
    • Export Citation
  • HodgeW.H.LoomisH.F.1956Federal plant introduction gardensNat. Hort. Mag.3586106

  • LiD.-Z.2008Floristics and plant biogeography in ChinaJ. Intergrative Plant Biol.50771777

  • LiX.-X.ZhouZ.-K.2005Endemic wild ornamental plants from northwestern Yunnan, ChinaHortScience4016121619

  • LieboldA.M.BrockerhoffE.G.GarrettL.J.ParkeJ.L.BrittonK.O.2012Live plant imports: The major pathway for forest insect and pathogen invasions of the USFront. Ecol. Environ10135143

    • Search Google Scholar
    • Export Citation
  • LiuK.ZhangD.WangX.2003Hunan (China) flora with rich ornamental plantsActa Hort.620403409

  • MeyerP.2010The return to China, mother of gardensArnoldia68411

  • MilneR.I.2006Northern hemisphere plant disjunctions: A window on tertiary land bridges and climate change?Ann. Bot. (Lond.)98465472

  • MilneR.I.AbbottR.J.2002The origin and evolution of tertiary relict florasAdv. Bot. Res.38281314

  • MooreG.WilliamsK.2011Legal issues in plant germplasm collecting. In: Guarino L. R.V. Ramanatha and E. Goldberg (eds.). Collecting plant genetic diversity: Technical guidelines—2011 update. Bioversity International Rome Italy. 26 June 2013. <http://cropgenebank.sgrp.cgiar.org/index.php?option=com_content&view=article&id=390&Itemid=557>

  • National Research Council1991Managing global genetic resources: The U.S. National Plant Germplasm system. National Academy Press Washington DC

  • PatonA.J.BrummittN.GovaertsR.HarmanK.HinchcliffeS.AllkinB.LughadhaE.N.2008Towards target 1 of the global strategy for plant conservation: A working list of all known plant species—Progress and prospectsTaxon57602611

    • Search Google Scholar
    • Export Citation
  • QianH.RicklefsR.E.1999A comparison of the taxonomic richness of vascular plants in China and the United StatesAmer. Nat.154160181

  • QianH.RicklefsR.E.2000Large-scale processes and the Asian bias in species diversity of temperate plantsNature407180182

  • QianH.RicklefsR.E.2004Geographical distribution and ecological conservatism of disjunct genera of vascular plants in eastern Asia and eastern North AmericaJ. Ecol.92253265

    • Search Google Scholar
    • Export Citation
  • QianH.SongJ.-S.KrestovP.GuoQ.WuZ.ShenX.GuoX.2003Large-scale phytogeographical patterns in East Asia in relation to latitudinal and climatic gradientsJ. Biogeogr.30129141

    • Search Google Scholar
    • Export Citation
  • QianH.WangS.HeJ.-S.ZhangJ.WangL.WangX.GuoK.2006Phytogeographical analysis of seed plant genera in ChinaAnn. Bot. (Lond.)9810731084

    • Search Google Scholar
    • Export Citation
  • RehderA.1940Manual of cultivated trees and shrubs hardy in North America exclusive of the subtropical and warmer temperate regions. 2nd Ed. Macmillan New York NY

  • ReichardS.H.WhiteP.2001Horticulture as a pathway of invasive plant introductions in the United StatesBioscience51103113

  • SargentC.S. (ed.). 1913–1917Plantae Wilsonianae; An enumeration of the woody plants collected in western China for the Arnold arboretum of Harvard university during the years 1907 1908 and 1910 by E.H. Wilson. 3 Vol. Cambridge University Cambridge MA

  • ShengC.K.1979Introduction of North American trees into ChinaArnoldia39271277

  • SpongbergS.A.1990A reunion of trees: The discovery of exotic plants and their introduction into North American and European landscapes. Harvard Univ. Press Cambridge MA

  • Tyler-WhittleM.S.1970The plant hunters. Chilton Philadelphia PA

  • WardB.J.2004The plant hunter’s garden: The new explorers and their discoveries. Timber Press Portland OR

  • WardF.K.1937Plant hunter’s paradise. Jonathan Cape London UK

  • WenJ.1999Evolution of eastern Asian and eastern North American disjunct distributions in flowering plantsAnnu. Rev. Ecol. Syst.30421455

    • Search Google Scholar
    • Export Citation
  • WenJ.2001Evolution of eastern Asian–eastern North American biogeographic disjunctions: A few additional notesIntl. J. Plant Sci.S117S122

    • Search Google Scholar
    • Export Citation
  • WilliamsK.A.2005An overview of the U.S. National Plant Germplasm System’s exploration programHortScience40297301

  • WilsonE.H.1913A naturalist in western China with vasculum camera and gun: Being some account of eleven years’ travel exploration and observation in the more remote parts of the flowery kingdom. Doubleday Page New York NY

  • XiangQ.Y.SoltisD.E.2001Dispersal-vicariance analyses of intercontinental disjuncts: Historical biogeographical implications for angiosperms in the northern hemisphereIntl. J. Plant Sci.S29S39

    • Search Google Scholar
    • Export Citation
  • XiangQ.Y.ZhangW.H.RicklefsR.E.QianH.ChenZ.D.WenJ.LiJ.H.2004Regional differences in rates of plant speciation and molecular evolution: A comparison between eastern Asia and eastern North AmericaEvolution5821752184

    • Search Google Scholar
    • Export Citation
  • XuT.ChenY.de JongP.C.OterdoomH.J.ChangC.-S.2008Aceraceae: Acer p. 516–553. In: Wu Z. and P.H. Raven (eds.). Flora of China. Vol. 11. Scientific Press Beijing China

  • ZhangD.DirrM.A.2004Potential new ornamental plants from China. Proc. Southern Nurs. Res. Conf. 49:607–609

  • ZhangD.T.LasseigneT.DirrM.1998A survey of Chinese native plants of potential ornamental and economic value for the southeastern United StatesJC Raulston Arboretum Newsletter3–92735

    • Search Google Scholar
    • Export Citation
  • ZhaoL.ZhangD.2003Ornamental plant resources from ChinaActa Hort.620365375

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