Collection of wild ginseng in North America for Asian consumer markets began during the early 1700s following an exchange by Jesuit missionaries (Carlson, 1986; Wang, 2007). In 1716, the Jesuit priest Joseph Francois Lafitau, with help from the Iroquois tribes, recognized ginseng in the vicinity of Montreal, Canada from botanical descriptions of the Chinese relative Asian ginseng (Panax ginseng C.A. Mey.) provided by Jartoux in 1714. Commercial exports from Canada to China commenced the following year and by mid-century populations were already declining or extirpated from over-collection near Montreal where the species was first “discovered” (Benson, 1987).

Export and harvest records indicate nearly continuous commercial exploitation of wild ginseng in eastern North America during the past 300 years (Carlson, 1986; United States Fish and Wildlife Service (USFWS), 2020). Export statistics reveal that over 13.7 million kg of ginseng root was exported from the United States during 182–1899 (Figure 1), for example. This would have been comprised entirely of wild root since there are no reports of commercial cultivation before the late 1800s (as discussed in section “Cultivation as a Sustainable Use Solution”). During the twentieth century, about half the volume of the previous century (roughly 7 million kg) was exported, and in the first two decades of the 21st century only 500,000 kg was reported to United States Fish and Wildlife Service (United States Fish and Wildlife Service (USFWS), 2020). Harvest amounts of wild ginseng have not exceeded 250,000 kg/decade after the year 2000, which is less than 1/10 of the historic peak in the late 1800s. All these statistics do not account for the quantity marketed and utilized domestically which would not have been recorded in export or, more recently, harvest records.

The long trade history associated with ginseng suggests that the exploitation of wild ginseng throughout eastern North America during the past three centuries has resulted in significant impacts to the species in the wild. United States vary widely in export quantities (Figure 2) and while year-to-year export volume can reflect socio-economic conditions rather than availability (Schmidt et al., 2019), the gradual and significant declines in export volumes are likely indicative of declining wild populations —especially when coupled with contemporary botanical field observations (McGraw et al., 2013; NatureServe, 2021). Ginseng is presently listed as “vulnerable” in the United States and out of 33 states where ginseng occurs as an indigenous forest species, seven consider the species to be “critically imperiled” (S1); four “imperiled” (S2); fourteen “vulnerable” (S3); and eight “apparently secure” (S4) (NatureServe, 2021). The species has been listed as “endangered” in Canada since 1999, with exports of wild ginseng prohibited altogether (Ontario Ministry of Agriculture and Food (OMAFRA), 2005; NatureServe, 2021).

Destructive root harvests exert the most negative impacts on population dynamics among the various types of plant parts harvested (Ticktin, 2004). With wild ginseng collection, the entire root and attached short rhizome (known as the “neck”) are generally taken, resulting in plant mortality. Collector attention to population structure (i.e., growth stages present) and harvest restraint are therefore necessary for continuous, sustained harvests (Van der Voort and McGraw, 2006; McGraw et al., 2013). Even given proper attention, recovery rates can be slow, and years of “rest” between harvests may be required (ibid). On average, about 90 roots, and therefore plants, are required to yield one kg of dry product (Burkhart and Jacobson, 2009; Unpublished data provided by Pennsylvania Department of Conservation and Natural Resources).

Ginseng is a slow-growing perennial herb, requiring at least three growing seasons before reaching reproductive or harvestable stages under cultivation (Ontario Ministry of Agriculture and Food (OMAFRA), 2005) and five or more years in forested habitats (Charron and Gagnon, 1991; McGraw et al., 2013; Davis and Persons, 2014; McGraw, 2020). Regeneration and recruitment occur primarily through seed production and therefore fecundity and seedling survival are important, and often constraining, life history traits. Reproduction is often delayed by years and fecundity is lower in wild plants, in comparison with cultivated plants, which means that wild plants must persist longer in forested habitats to contribute to recruitment (ibid). Moreover, all United States export states have regulations restricting harvest to mature stages, which effectively then inadvertently encourages wild collectors to remove reproductive plants from populations once mature stages are attained, thereby lowering recruitment potential over time (Van der Voort and McGraw, 2006).

In addition to collection for commercial markets, immediate threats to wild ginseng in the United States include loss/degradation of supportive forest habitat types, over-browsing by white-tail deer (Odocoileus virginianus Zimmerman), and poaching/theft (McGraw et al., 2013; McGraw, 2020). The last of these, ginseng poaching, is fueled by widespread stakeholder recognition that laws around theft are difficult to enforce and/or successfully prosecute, especially on privately owned lands where jurisdictional boundaries can limit enforcement activities (Pokladnik, 2008; Burkhart et al., 2012). During the past decade, this situation has only gotten worse as United States “reality” television shows (e.g., Appalachian Outlaws, Smoky Mountain Gold) have helped to “normalize” ginseng poaching by unfortunately portraying ginseng diggers, competitive digging, and theft from others as part of a cultural and industry “outlaw” identity (West Virginia Public Broadcasting, 2014).

In the United States, ginseng trade is monitored by both state and federal governments following its 1975 listing in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). CITES is an international agreement between governments with the shared goal to ensure that international trade in specimens of wild animals and plants does not threaten their survival (Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), 2021). Appendix II status is reserved for “species not necessarily threatened with extinction, but in which trade must be controlled in order to avoid utilization incompatible with their survival” (ibid).

The United States Fish and Wildlife Service (USFWS), which is part of the Department of the Interior, is responsible for CITES implementation in the United States (Burkhart et al., 2012; Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), 2021). The USFWS has the Division of Management Authority to address policy and permitting issues, and the Division of Scientific Authority (DSA) to deal with scientific issues relating to CITES implementation. Under CITES, ginseng exports must be legal and not detrimental to the survival of the species in the wild. The USFWS has approved export of wild ginseng from the United States on a state-by-state basis since 1978. The DSA relies on individual states’ data and determination in making its “non-detriment” determination, as a compliance measure to CITES when approving export of “wild” American ginseng (ibid).

The nineteen approved United States for wild ginseng export (Figure 2) have all experienced declines in reported harvest amounts since the species was first listed in CITES in 1975 (United States Fish and Wildlife Service (USFWS), 2019). Accordingly, the question of how effectively CITES is working as a conservation mechanism remains unclear, as is any influence of CITES listing on black market smuggling. At a minimum, a CITES listing elevates the conservation visibility around the species and helps to provide a mechanism for tracking and regulating trade. However, there is disagreement amongst stakeholders as to whether CITES regulations are helping ginseng conservation efforts (Burkhart, 2011; Burkhart et al., 2012; Beyfuss, 2019).

In a case study of CITES implementation in the United States of Pennsylvania, the impact of a CITES-driven “top-down” regulatory approach to wild ginseng conservation was found to be limited (Burkhart et al., 2012). While there was general support amongst stakeholders (e.g., diggers, growers, traders) for conservation efforts, study participants widely shared the belief that many harvest restrictions are not easily enforced—a reality that was externally validated by the fact that law enforcement is often constrained by complex jurisdictional boundaries. Moreover, Burkhart et al. (ibid) found that a lack of public confidence in ginseng conservation efforts stemmed in large part from a perceived failure of natural resource agencies to recognize and stop ginseng habitat loss, serving as justification to adopt critical attitudes toward any government involvement in the trade. Importantly, and relevant to this current paper, is the finding that the most widespread support uncovered for government driven ginseng efforts was involvement of stakeholders as “partners” for in situ planting, farming, and restoration.

The first attempts to cultivate ginseng in North America began in the late 1800s, following more than a century of wild harvest and trade, in the Appalachian and Mid-Atlantic regions of the United States. One prominent figure during this early period was George Stanton, who started experimental forest beds at his home in Apulia Station, New York around 1885 (Stanton, 1892; Davis and Persons, 2014). Known in later years as the “Father” of American ginseng cultivation, he investigated both forest- and artificial shade-based horticulture. Stanton’s introduction of artificial shading around 1890 was intended to speed up plant development following the observation that ginseng grew very slowly in forest beds. The cultural system he employed featured wooden panels perched upon posts 6-7 feet above raised garden beds to facilitate 70% shade since ginseng is a shade-obligate species. In his pursuit of successful husbandry, Stanton used wild ginseng ecology as his model and attempted to duplicate natural conditions in every respect.

However, it was in Marathon County, Wisconsin that the Fromm brothers perfected the commercial methods still largely used today in artificially shaded field production of ginseng (Polczinski, 1982). Like Stanton, the Fromm brothers developed practices that essentially mimicked the natural requirements for optimum growth and reproduction by carefully observing the occurrence of plants in the wild. The practices they and others adopted included the use of raised beds to provide soil moisture drainage; the application of winter mulches; proper seed stratification to ensure germination; and the construction of lathing to create favorable shade conditions (Van Fleet, 1913; Hardacre, 1974).

Presently, the majority of ginseng is cultivated using these methods in two regions of North America: the upper Midwest United States (Wisconsin) and ON, Canada (Ontario Ministry of Agriculture and Food (OMAFRA), 2005; Ginseng Board of Wisconsin, 2021; Ontario Ginseng Growers Association (OGGA), 2021). Although there are no accurate statistics on production by country, four countries—South Korea, China, Canada, and the United States—are the biggest cultivated producers with a total ginseng root production (fresh weight) of approximately 79,769 tons, which is more than 99 percent of the estimated total world production of 80,080 tons (Baeg and So, 2013). These estimates include all ginseng species known to be cultivated (P. quinquefolius, P. ginseng, P. notoginseng Burk, P. japonicus C.A. Meyer), however. Artificial shade cultivation (also known as “field cultivation”) of ginseng in the North America has supplied export markets and thereby helped conserve wild ginseng by providing an affordable and accelerated alternative to wild. Ginseng cultivation under artificial shade is the primary horticultural arrangement for large-scale production in Ontario, Canada and Wisconsin, United States which are estimated to produce 6,486 and 1,504 tons of ginseng annually, respectively (Baeg and So, 2013). Ginseng farmers utilize artificial shade cropping to mechanize their production and better manage diseases, which in turn shortens the number of years to maturity, increases yields, and reduces labor needs (Ontario Ministry of Agriculture and Food (OMAFRA), 2005; Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA), 2021).

However, the cultural predilections of some Asian consumers, especially within TCM, continue to drive a niche demand for wild ginseng since they are attracted to “wild” labeling and accompanying product characteristics. Ginseng grown in situ in forests are likely to possess “wild” traits that are traditionally favored by Asian consumers including taste, shape, color, and texture (Hu, 1976; Guo et al., 1995; Roy et al., 2003). Desirable characteristics include old age, which is demonstrated by a long “neck” (rhizome) with many “neck scars:” transverse “stress rings” on the main body of the root; and variable rhizome branching, with one or more variously shaped tubers attached (Hu, 1976; Upton, 2012; Figure 3). By contrast, cultivated ginseng roots tend to be larger, more uniform, younger, and lack many of the subtle characters such as “stress rings.”

The market price for wild-appearing ginseng roots is as much as 100 times greater than for artificially shaded field cultivated roots (Figure 4; Burkhart and Jacobson, 2009). Such high price premium of ginseng with “wild” traits over products cultivated in artificial shade field have driven continued wild harvests as well as the interest in forest farming in the United States (Davis and Persons, 2014).

In the eastern United States, in situ forest-based ginseng cultivation was first adopted beginning in the late 1800s (Butz, 1897; Harding, 1912; Hardacre, 1974). The cultivation of crops in an existing forestland understory is referred to, and in recent decades promoted as, “forest farming” in the United States (Gold et al., 2000; Mudge and Gabriel, 2014). Forest farming has been defined as “the integration and management or intentional cultivation of high-value non-wood/timber forest crops such as medicinal and edible plants under the canopy of well-managed forest” (ibid). It is one of five agroforestry practices recognized and promoted by the United States Department of Agriculture National Agroforestry Center (NAC) nationwide (National Agroforestry Center (NAC), 2021). The specific husbandry practices associated with forest farming of ginseng form a husbandry continuum from management in situ, using enrichment plantings (“wild-simulated”), to intensive cultivation in situ using beds and/or tillage (“woods-cultivated”) (Hill and Buck, 2000; Pritts, 2010; Davis and Persons, 2014; National Agroforestry Center (NAC), 2021). Regardless of the approach, ginseng forest farming has the potential to be highly profitable, even at a small scale (Burkhart and Jacobson, 2009; Davis and Persons, 2014). Outside of the United States, ginseng forest farming methods are also being developed and encouraged in rural, mountainous regions within China and South Korea, where it is referred to as “wild-cultivated,” “mountain ginseng,” “forest-cultivated,” or simply “wild” ginseng production (International Federation of Organic Agriculture Movements (IFOAM), 2011).

Because ginseng forest farming has only recently been recognized in the United States, and because of the complexity associated with identifying growers (as discussed under section “Regarding Research”), there have been few efforts to date attempting to track adoption and production. An effort to estimate forest farmer numbers in 1994 estimated the total number of producers in 20 United States at 814 woods-cultivated and 3,334 wild-simulated growers farming 566 total hectares of forestlands (Persons, 1995). In 2000, estimates were again made with a resulting 750 and 3,416 forest farmers suggested, for a total of 818 hectares of woods-cultivated and wild-simulated producers, respectively (Persons, 2000). These estimates are incomplete, and perhaps even under-representative, as they were compiled by simply querying contacts in each state rather than by examining any type of official industry data (ibid).

Immediate advantages of forest farming are realized by producers through production cost savings. Since ginseng is shade obligate, significant investments in artificial shade structure are necessary when plants are grown in open field settings, with materials and associated labor costs averaging $75,000 (US$) per hectare (Ontario Ministry of Agriculture and Food (OMAFRA), 2005; Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA), 2021). Moreover, ginseng is commonly plagued by fungal diseases under field cultivation which requires frequent and costly use of fungicides (Ontario Ministry of Agriculture and Food (OMAFRA), 2005). Depending on production methods, forest farmed ginseng may not be impacted as much or at all by fungal diseases, by contrast (Davis and Persons, 2014). The cultivation of forest plants in situ may therefore eliminate or reduce disease problems and, in turn, the need for pesticide use, thereby facilitating access to “organic” and other niche markets.

Disadvantages associated with forest farming include a slower growth rate, requiring 10 or more years to reach harvestable size, and generally lower yields when compared with field production (Ontario Ministry of Agriculture and Food (OMAFRA), 2005; Burkhart and Jacobson, 2009; Davis and Persons, 2014). In ON, Canada, field production under artificial shade can result in root yields as high as 2,950 kg per hectare (Ontario Ministry of Agriculture and Food (OMAFRA), 2005; Ontario Ginseng Growers Association (OGGA), 2021). By comparison, top yields of 670 kg per hectare are obtained under forest farming production (Burkhart and Jacobson, 2009; Davis and Persons, 2014). Thus, forest farming may be 1/10 as productive as field cultivation when yields alone are considered. These lower yields result from a combination of reduced ginseng biomass production and the heterogenous nature of forest cropping environment which creates both micro-site variation as well as physical barriers (e.g., rocks and boulders, basal tree stems) to cropping. Additionally, forest farmers typically rely heavily on labor for forest-based husbandry activities to minimize site disturbance, which prevents any efficiencies that might be gained through mechanization. In situ ginseng farming is also subject to many of the same threats facing wild ginseng populations including targeted theft, wildlife predation, and farming habitat changes resulting from invasive species and/or climate change (Pokladnik, 2008; Davis and Persons, 2014; McGraw, 2020).

Despite these diverse challenges, in situ forest farming of ginseng as a conservation strategy can generate direct benefits to ginseng and associated forestland habitats. In particular, the practice of in situ enrichment plantings can preserve understory forest biodiversity, and function in wild population restoration or augmentation (Burkhart, 2013; International Union for Conservation of Nature (IUCN), 2013; Chittum et al., 2019). Forest farming offers multiple economic and ecological benefits while also being attractive to forest landowners since the practice has the potential to increase income while maintaining forest integrity (Hill and Buck, 2000). Income derived from forest cultivation is received at shorter intervals than timber, giving private forest landowners more revenue options, enabling them to pay annual taxes and other carrying costs. Facilitating private landowner adoption of forest farming can therefore drive interest in forest stewardship, raise awareness about indigenous forest plants, and positively influence silvicultural decisions (Burkhart and Jacobson, 2009).

An immediate challenge confronting ginseng forest farmers is the “cultivated” vs. “wild” binary labeling derived from CITES. The present ginseng trade lexicon under CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), 2021) is used by many United States on trade paperwork. It identifies “cultivated” plants as “artificially propagated” and in Resolution Conf. 11.11 (Rev. CoP14) defines these as follows:

Any ginseng that does not meet these criteria is “wild” under CITES and at present, de facto, by USFWS and State export programs. Burkhart et al. (2021) suggest that this dichotomous lexicon is far too simplistic to account for the breadth of forest farming practices that are being employed to produce roots ultimately sold as “wild.” When forced into this dichotomy, forest farmers often choose to report their product as wild, fearing pricing disparities (discussed below), theft, taxation, and disagreement over what constitutes “wild” (ibid).

However, while self-declaring forest farmed ginseng as “wild” can bring higher profit for farmers, it also increases exportation barriers due to CITES restrictions. The complexities and costs associated with applying for export permits also prevents forest farmers from legally selling their products directly to customers in China and east Asia via e-commerce platforms. Additionally, forest farmers often do not have the knowledge or financial resources to apply for CITES permits to sell small amounts of wild-cultivated ginseng internationally (Burkhart, pers. comm. with producers). The burden of applying for CITES export/import permits may be one of the reasons that very few or no vendors sell wild and wild-cultivated ginseng on e-commerce platforms in Hong Kong, China, Singapore, and Taiwan (Arik et al., 2020).

In the online retail market survey mentioned in section “Cultivation as a Sustainable Use Solution,” each of the named countries or regions, e.g., Mainland China, Hong Kong China, is an independent CITES entity, with its own national or equivalent domestic laws and authorities to carry out CITES regulations. Even though Hong Kong is part of the China, it has its own CITES related domestic laws, scientific and management authorities (Agriculture, Fisheries, and Conservation Department of Hong Kong, 2020). In addition, while Taiwan is not a CITES signatory authority because it is not a member of the United Nations, it participates in CITES and abides by the rules of this international convention voluntarily (Forestry Bureau of Republic of Taiwan, 2016). Import of ginseng into these countries and regions requires a CITES export permit issued by the authority of the exporting country and a license to import from the import country’s managing authority.

Another significant challenge to the forest farming in the eastern United States is that it remains a largely secretive and poorly documented. In eight years of annual surveying of Pennsylvania sellers, Burkhart et al. (2021) found that “wild” exports consisted of a mix of collected, planted (along with various husbandry practices), and forest farmed product. A complex suite of husbandry practices was found to be involved in modern wild ginseng occurrence and these practices obscure and complicate distinctions between “wild” and “cultivated.”

Importantly, Burkhart et al. (ibid) also found that attempts by United States to clarify the origins of “wild” ginseng through forest farming terminology in point-of-sale paperwork are often resisted or falsified because sellers harbor concerns regarding buyer-trader pricing and crop taxation. Regarding the former, it is recognized that many buyers pay less for wild-cultivated product even when it is indistinguishable from wild so that they can re-sell for a higher profit margin. Rumors of unfair pricing have resulted in low rates of seller compliance when asked to report forest farming activities in some United States that have worked to implement measures for differentiating wild-cultivated from wild ginseng (ibid).

Regarding collaboration: