Protecting Goldenseal: How Status Assessments Inform Conservation

Issue: 119 Page: 40-55 by Leah E. Oliver, Danna J. Leaman, PhD HerbalGram. 2018; American Botanical Council Summary A recently published global assessment of the conservation status of goldenseal (Hydrastis canadensis, Ranunculaceae) has found that the species is Vulnerable to Extinction (i.e., it faces a higher risk of extinction in the wild throughout its distribution in the United States and Canada than many other species). However, the extinction risk is not yet at the level of Endangered (very high risk of extinction) or Critically Endangered (extremely high risk of extinction). This article explains two complementary conservation ranking methods — the International Union for the Conservation of Nature (IUCN) Red List and NatureServe — and the criteria applied to assess the conservation status of goldenseal. These assessments consider all primary threats to goldenseal conservation, including the impact of habitat loss and other factors, such as domestic and international trade, and propose measures to support in situ and ex situ conservation of this species. Introduction In 2017, the IUCN published the first comprehensive global Red List assessment of goldenseal, which concluded that the species is globally Vulnerable, a category that indicates a high risk of extinction in the wild.1,2 To determine risks of extinction, the IUCN Red List of Threatened Species uses a scientifically rigorous approach that is applicable to all species. It has become a world standard, providing information and analyses on the status, trends, and threats to species in order to inform and catalyze action for biodiversity conservation.3 The assessment was authored by NatureServe, a nonprofit network of scientists that provides access to and analysis of current data on biodiversity. The 2017 IUCN assessment followed and built on NatureServe’s 2012 global ranking update, which classified goldenseal as G3G4 — a range rank that spans G3 (Vulnerable; a moderate risk of extinction) and G4 (Apparently Secure; some cause for long-term concern).4 Over the last two decades, the North American herb industry has made substantial efforts to recognize threats to goldenseal populations, raise industry and consumer awareness about the need for goldenseal conservation, and invest in commercial-scale cultivation of the species.5-7 However, wild-collectors, cultivators, conservationists, and other members of the herbal community have questioned the rationale for the IUCN and NatureServe conservation assessments and the information on which they are based. This article aims to provide transparency about these assessments by explaining the history, rationale, and challenges behind them, and to explore what the conservation status of goldenseal signifies for the current and future sustainability of this important North American herb. What is Goldenseal? Goldenseal is a long-lived, perennial plant that is native only to North America, where it grows in densely shaded, deciduous forests. Naturally growing populations are known to occur in 26 states in the eastern United States, ranging from southern Vermont, west to Minnesota, and south to Georgia, Alabama, and Arkansas. In Canada, naturally growing populations are known to occur only in southwestern Ontario.1,8 The core part of its range includes the Ohio River Valley states of Indiana, Kentucky, Ohio, and West Virginia.9,10 There are no state-level or range-wide population estimates for goldenseal, which is typical of most wild-harvested plant species.11 Goldenseal appeared in early records of medicinal uses of North American plants.12 Native Americans and Canadian First Nations have used various parts of this plant — especially the rhizomes and roots — in traditional remedies for cancer, eye ailments, inflammation, digestive problems, pneumonia, and heart problems.13 European colonists adopted and popularized some of these applications. In the 1900s, increased demand for goldenseal was caused in part by its unfounded reputation for masking illicit or performance-enhancing drugs in urine tests.14-16 This myth apparently grew from a murder mystery published in 1900 in which goldenseal bitters were erroneously identified as strychnine, which inspired an otherwise unfounded association of goldenseal with chemical testing errors in American folklore.15,17 Demand for goldenseal has increased over time, as applications have expanded beyond traditional and local uses and interest has been renewed in herbal medicines in North America and internationally.4,17 More recently, the identification of the alkaloids berberine, hydrastine, and canadine in goldenseal provided a scientific basis for its use in certain conditions.18 Goldenseal currently is used mainly as a component of traditional herbal medicine formulations marketed as licensed Natural Health Products (NHPs) in Canada19 and as dietary supplements in the United States. The export market is relatively small and limited primarily to countries with Western herbal medicine traditions, such as Australia and the United Kingdom. Goldenseal also is exported to Europe in small quantities for use in two traditional German systems of medicine: anthroposophical medicine and homeopathic medicine (J. Brinckmann email to C. Yearsley, March 17, 2018). The World Health Organization includes goldenseal rhizome (Rhizoma Hydrastis) among materials that have global importance in alternative medicine, with its main use described in pharmacopeias and “well established documents” as a treatment for digestive complaints, in addition to a variety of other traditional uses.20 Conservation Concerns Wild goldenseal subpopulations have declined dramatically due to habitat loss and degradation through forest conversion for agricultural use, urban expansion, road intrusion, and recreational use. Population decline also has been caused by commercial collection that began in the mid-1800s.17,21 Concerns about the conservation of goldenseal have existed since at least 1884, when American pharmacist John Uri Lloyd (author of the aforementioned murder mystery novel) and his brother, mycologist Curtis Gates Lloyd, observed that goldenseal rhizome harvesting and habitat loss were causing significant declines in goldenseal subpopulations.22 Botanists’ observations from this period onward provide anecdotal and observational evidence of the continued decline and loss of goldenseal subpopulations from habitat loss and degradation and increasing demand for wild-collected rhizomes.23-39 Approximately 80% of the original forests in New England have been lost to land conversion, which reached its peak during the 1800s.40 In the Canadian portion of goldenseal’s range, less than 5% of its forest habitat remains from pre-settlement times.8 Although goldenseal was cultivated on a small scale for more than a century throughout its native range, most of its domestic and international trade until the early 2000s came from wild-harvested rhizomes and roots.10 There have been efforts to account for harvest and trade volumes in national and international trade by using records of phytosanitary certificates issued by the US Department of Agriculture (USDA) and by tracking trends in supply and demand (e.g., using wholesale prices published in US herb catalogs).39 However, in the absence of any official monitoring and reporting requirements, it was not possible to accurately quantify the volumes of roots harvested, traded in domestic markets, or exported from North America.5,41 Subpopulations in Canada were first assessed as Threatened in 1991 by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC).42,43 By the mid-1990s, goldenseal in the United States was considered Critically Imperiled, Imperiled, or Uncommon in 17 of the 26 states in which it occurs.39,44 According to Bannerman (1997), wild harvest was prohibited in a number of states due to concerns about population decline.5 Herbalists also are concerned. United Plant Savers (UpS), a nonprofit organization dedicated to the conservation of native American medicinal plants, included goldenseal in its original list of “Species At-Risk” that identified plants in decline due to expanding popularity and shrinking habitat and range. This list was created in 1997 by “concerned herbalists and conservation-minded plant enthusiasts” to encourage practical and educational programs and to promote organic cultivation of “At-Risk” herbs.6,45 CITES Listing In 1997, the North American office of TRAFFIC: The Wildlife Trade Monitoring Network formally petitioned the US Fish and Wildlife Service (USFWS) to propose goldenseal for inclusion in Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES).17 The proposal was adopted at the 10th meeting of the Conference of the Parties to CITES in June 1997.39 While conservation experts and officials in importing countries were concerned that supplies of goldenseal would fall and prices would rise if goldenseal were included in Appendix II, the conference decided to adopt the proposal. Goldenseal was listed in Appendix II on September 18, 1997, with an annotation to focus on trade in “whole and sliced roots and parts of roots, excluding manufactured parts or derivatives such as powders, pills, extracts, tonics, teas and confectionary.” This listing means that all international exports and re-exports of goldenseal roots and rhizomes, whether wild, forest-grown, or cultivated, require permits issued by the CITES Scientific Authority to enable monitoring and control of materials and volumes in international trade. A CITES export permit signifies that the transaction is legal and does not threaten the species’ survival in the wild.46 Obtaining a permit to export goldenseal also requires proof that the roots, rhizomes, or seeds came from legally acquired parental material and from plants that were at least four years old.47 Increased export of powdered goldenseal roots and rhizomes from the US after 1997 made it difficult to monitor international trade48,49 and led the USFWS to amend the annotation for goldenseal in 2007 to include “underground parts (i.e., roots, rhizomes): whole, parts and powdered,”49 (emphasis added) so that all of the major goldenseal products in international trade could be monitored. Inclusion of goldenseal in Appendix II stimulated industry investment in research and education campaigns supporting commercial cultivation of the species.5 For example, propagators and growers worked for more than a decade to improve seed stratification requirements of goldenseal so that the germination rate would support sexual propagation (E. Fletcher email to C. Yearsley, March 21, 2018). The herbal industry also implemented measures to track wild and cultivated production.6,7 Although nearly all material in trade continued to come from wild collection until the early 2000s, there has been a shift in the international market to cultivated sources in recent years.50-52 The CITES Trade Database (2000-2016) indicates that the majority of material in international trade is now from artificially propagated plants. Industry surveys of raw herbal materials producers in the United States undertaken by the American Herbal Products Association (AHPA), a trade association for the US herb industry, documented an increase in cultivated goldenseal roots and rhizomes (compared to wild-collected materials) from a low of 2% cultivated in 1998 to a high of 41% cultivated between 2000 and 2010.51,52 Although CITES and industry trade data indicate that cultivated goldenseal makes up an increasing portion of international trade, the most recent publicly available AHPA survey data from 2010 suggest that the majority of goldenseal raw material in US domestic trade was sourced from wild collection. For example, in 2010, 59,197 pounds of goldenseal root and rhizome and 10,791 pounds of leaf were reported from wild sources, while cultivated sources accounted for 17,931 pounds of root and rhizome and 782 pounds of leaf.51,53 History, Rationale, and Challenges behind the Recent NatureServe and IUCN Conservation Status Assessments The transition of international trade of goldenseal from wild-harvested to cultivated sources has had an impact on goldenseal conservation. In 2012, the US CITES Scientific Authority, part of the USFWS, initiated a status review of the species. USFWS engaged NatureServe to carry out the review, with a focus on filling gaps in information about goldenseal’s abundance, population trends, life history, core range states, and current threats, particularly the impacts of ongoing wild harvest. This new information was used to update NatureServe’s state, national, and global rankings for goldenseal and to complete a global (United States and Canada) IUCN Red List assessment of this species. The CITES Scientific Authorities in the United States and Canada rely on these and other data sources to determine whether international trade is detrimental to the survival of the listed species. This determination is referred to as a non-detriment finding (NDF). Although CITES permits and monitoring focus on material in international trade, for the purposes of making an NDF, the Scientific Authority “should consider the volume of legal and illegal trade (known, inferred, projected, estimated) relative to the vulnerability of the species (intrinsic and extrinsic factors that increase the risk of extinction of the species),” and, “in considering whether an export may be detrimental, the sustainability of the overall harvest will usually be a necessary consideration.”54 Methods and Processes of the Conservation Assessments Information from scientific literature and databases was collated to update the population status and threat information already contained in NatureServe’s central databases and in IUCN’s Species Information Service (SIS), the database used to compile and manage Red List assessments. NatureServe carried out formal status assessments based on both NatureServe’s global ranks55 and IUCN’s Red List categories and criteria.2 Each assessment entailed compiling information relevant to understanding the risk of extinction for a species: geographic distribution; population size; number, size, and distribution of subpopulations; population and habitat trends; type and scale of threats; and existing conservation actions. Although published literature contains a wealth of useful data about conservation status factors, active field researchers have the most current information about the status of wild populations. In 2012, the NatureServe team contacted botanists at state and federal agencies, natural heritage programs, and universities, among other experts, to gather information on factors contributing to goldenseal’s conservation status. NatureServe engaged these botanists by distributing a survey that included questions about goldenseal’s distribution on state, federal, and private lands, and protection and regulation on those lands. A section of the survey focused on information about population size, viability, and evidence of wild collection. Additionally, botanists were asked for information about cultivation and wild collection in each state. The synthesized data from the scientific literature and expert surveys provided higher quality and more current rank factor values, which were entered into NatureServe’s global rank calculator and IUCN’s Red List assessment. Draft assessments using both the NatureServe rank calculator and IUCN’s SIS were completed and peer reviewed. Results of the Assessments NatureServe previously assessed goldenseal’s global population as Apparently Secure (G4), indicating that the species is uncommon but not rare, and that there is some cause for concern due to decline over the long term.1,4 The updated global conservation status of goldenseal using NatureServe’s rank calculator and ranking guidance is Vulnerable/Apparently Secure (G3G4), which suggests that there is uncertainty about which of these two ranks (G3 or G4) best reflects the available information about the species.1,4,55 The G3 rank indicates that the species’ status may have declined to Vulnerable (i.e., at moderate risk of extinction due to a restricted range, relatively few subpopulations or occurrences, or recent and widespread declines or other threats).55,56 Due to uncertainty about ongoing loss of habitat, population estimates across the species’ range, and actual levels of wild collection for the domestic market, G3G4 is believed to convey the most accurate extinction risk for goldenseal. Based on the available biological and trade information, including the NatureServe assessment, goldenseal remains in Appendix II of CITES so that international trade does not reduce the wild population to a level that would threaten its survival. The first IUCN Red List global assessment of goldenseal from 2017 determined that the species is Vulnerable.1 This category indicates that it faces a higher risk of extinction in the wild throughout its distribution than many other species, but that the extinction risk is not yet at the level of Endangered or Critically Endangered. The 2017 IUCN assessment is based on indicators that goldenseal’s population has declined by at least 30% over the past three generations of the plant and the assumption that this trend will continue in the absence of more effective conservation measures. The indicators of population reduction include: inferred population decline based on firsthand observations in some subpopulations10,11,63; suspected population decline based on observed and estimated declines in habitat availability and quality8,21,23; and suspected population decline based on observed harvest impacts and suspected levels of exploitation.23 Suspected levels of exploitation also were based on increasing numbers of requests for wild-harvest permits for goldenseal, as reported by the Indiana Natural Heritage Program. Adequate evidence was available to determine that, in the recent past, the area occupied by all known subpopulations has declined within goldenseal’s native range, habitat quality has declined, and exploitation of wild subpopulations has reduced the number of individuals. These are continuing threats. Assessment Challenges Related to Population Size and Trends Knowledge of population biology and trends for goldenseal is more extensive than for many native species of medicinal herbs, yet estimating the total number of individuals and the rate of population decline for goldenseal is challenging because of its widely scattered distribution, relatively long generation length for an herbaceous plant, clonal habit of reproduction, and the absence of high-quality population monitoring and genetic diversity data. Scattered Distribution Anecdotal information from historical documents indicates that goldenseal subpopulations have declined significantly throughout its range since the early 1800s, but little quantitative trend data are available for the last 30 years (approximately three generations).64 Botanical accounts of goldenseal since the mid-1800s describe dramatic reduction of once-abundant subpopulations to isolated, scattered patches in parts of its range, and attribute these declines to habitat destruction, collection for medicinal uses, and increasing pressure on managed and previously unharvested subpopulations.21,23,25,65 Declines in goldenseal subpopulations have been qualitatively documented in New York, West Virginia, and Indiana (P. Harmon personal communication to L. Oliver, November 28, 2012; C. Floyd email to L. Oliver, November 30, 2012).40,63 Fewer subpopulations, patches per subpopulation, and ramets (genetically identical individuals of clonal species) per patch provide additional evidence of subpopulation decline.63 /b> The most significant challenge in determining the IUCN Red List assessment ranking of Vulnerable was providing evidence that goldenseal population decline has been and will continue to be at least 30% over three generations. According to the IUCN Red List Guidelines, “generation length should be averaged over asexually and sexually reproducing individuals in the population, weighted according to their relative frequency” in the population.64 Because these parameters are unknown for goldenseal (as indeed they are unknown for most plant species), it is accepted practice to estimate generation length as the age at first flowering and fruiting, believed to be seven to nine years for goldenseal.66 (An expert reviewer of this article noted that there are instances of goldenseal’s life cycle being three to four years in cultivation settings.) The IUCN assessment, however, eventually settled on an estimated generation length of 10 years. Clonal Reproduction Like many plant species, goldenseal reproduces both sexually and clonally, but this mixed-mating system makes it difficult to visually distinguish genetically distinct individuals from clonally identical individuals (ramets) in a population. Sanders (2004) described goldenseal subpopulations as forming “dense patches of a few to greater than 1,000 ramets with patches frequently sparsely distributed across the landscape, such that many patches are isolated from others by great distances.”67 Plant species that reproduce clonally create a baffling situation for field biologists attempting to count or estimate numbers of reproductive individuals in a subpopulation or the total population. The count of ramets (individual stems in a clone) and estimates of subpopulation sizes overestimate the number of genetically distinct individuals and genetic diversity in the population because the ramets of each clone are genetically identical. Goldenseal ramets have a single stem, so it is not possible to visually differentiate genetically distinct individuals. The current IUCN Red List guidance recommends that assessors define an individual as the smallest entity capable of independent survival and reproduction (sexual or asexual),64 but this guidance does not adequately account for concerns about limited genetic diversity within and between such populations that cannot be equated to species that reproduce only sexually (e.g., mammals). Genetic Diversity Several recent studies have begun to fill a long-standing gap in information about the genetic diversity of goldenseal. Torgerson (2012) reported low genetic variation across subpopulations examined in North Carolina.68 In a study that compared the genetic variation between cultivated and natural populations of goldenseal in Ohio, Pennsylvania, West Virginia, and North Carolina, genetic diversity in both settings was found to be low.69 Six cultivated and 11 wild subpopulations shared a high degree of genetic similarity, which is not surprising, the authors noted, given that the original plants in cultivation were propagated from wild genetic material. For most crop species, plants in cultivation typically have far less genetic diversity than those in the wild, but this may not be the case for goldenseal. Preliminary evidence, based on small sample sizes, suggests that goldenseal’s genetic diversity is low both in the wild and in cultivation.69,70 Wild subpopulations for most crops are genetic reservoirs that can be accessed to breed disease resistance or environmental tolerance (e.g., drought resistance) into cultivated stock. Overall, low genetic diversity in wild populations means there is less adaptive capacity for environmental stressors, disease, and other pathogens for both wild and cultivated plants. High genetic diversity that is spread across subpopulations implies frequent gene flow from pollination events among the subpopulations. In contrast, if genetic diversity is higher within a subpopulation than among them, this suggests that the subpopulations are genetically isolated from one another, with little pollination occurring among them. Goldenseal follows the latter scenario. Inoue et al. (2013) found the highest levels of genetic variation within subpopulations, and low genetic similarity across subpopulations.69 These results support the hypothesis that goldenseal subpopulations are isolated from one another, and that pollen exchange among subpopulations occurs with limited frequency.67 Habitat Loss, Population Extirpations, and Decline in Habitat Quality Recognizing that complete information about population size and trends is lacking for many species, the IUCN Red List criteria are designed to support the use of other types of information, such as inference of long-term and short-term population reductions from observed declines in the area occupied by species subpopulations and in the number of subpopulations or occurrences.64 Observations of substantial long-term decline of goldenseal’s forest habitat since the early 1800s contributed to the conservation concerns that led to the listing of goldenseal in CITES Appendix II. While the pace of land conversion has slowed since then, habitat loss remains a threat to goldenseal throughout its range. These ongoing threats have been corroborated by personal communications with more than a dozen natural heritage botanists from 12 US states with goldenseal populations.8 Another source of information used in the conservation status assessments was data on population extirpations (local extinctions) in the heart of goldenseal’s range. In Ohio, a state in the core of the species’ range, a study by Mulligan and Gorchov (2004) found that nine of 71 historical occurrences were extirpated.21 Of the 42 goldenseal sites documented in Ohio from 1977-1998, 14 sites were extirpated as of 2002. If the rate of extirpation is assumed to be constant, approximately 1.6% of goldenseal subpopulations are extirpated each year in Ohio, amounting to an approximately 30% decline in the number of subpopulations over a 20-year period (D. Gorchov email to L. Oliver, November 1, 2012).21 The observed rate of extirpation of goldenseal occurrences in Ohio is likely to be about the same or higher in states on the periphery of goldenseal’s distribution, where subpopulations are smaller and more scattered. This rate of decline meets the threshold criterion for the IUCN Red List category Vulnerable, inferring from the estimated rate of subpopulation decline an overall population reduction of at least 30% over the past three generations (21-28 years).1,2 Mulligan and Gorchov determined that only 13% of documented extirpations in Ohio were due to deforestation, which suggests that threats other than land conversion caused most of the observed extirpations of goldenseal subpopulations.21 Decline in the quality of goldenseal habitat also results from ongoing impacts of agricultural expansion, urbanization, recreational use of forests, and road building and maintenance. Other threats leading to habitat degradation include loss or disturbance by flooding and/or fire, invasive species, trampling,8,71 and browsing by deer.21 Population Impacts of Wild Collection Continuing decline in the global goldenseal population resulting from habitat threats is exacerbated by wild collection. Mulligan and Gorchov attributed 10% of the observed rate of decline in goldenseal subpopulations in Ohio to wild harvesting.21 They also noted that goldenseal subpopulations in Ohio are smaller, with fewer flowering plants than goldenseal subpopulations in Ontario, and suggested that the difference may be attributed to wild collection being permitted in Ohio and prohibited in Ontario. Christensen and Gorchov (2010) observed that goldenseal harvesters usually collect rhizomes of the largest individuals. They explain that this practice, over time, results in smaller subpopulation sizes and smaller proportions of large, reproductive individuals by adversely affecting population regeneration through both sexual and asexual reproduction.10 The volume of wild goldenseal rhizomes and roots exported from the United States and Canada has been monitored and documented based on CITES permit data since the end of 1997 in compliance with these countries’ obligations as signatories of CITES.52 These trade data indicate that wild-harvested goldenseal material has substantially declined relative to the increasing supply of cultivated material in the international market. As mentioned previously, herbal industry surveys of relatively small numbers of primary raw material producers of goldenseal documented an average of 40 tons of goldenseal root (wild and cultivated) in trade per year in the United States between 2004 and 2010.51 These surveys also indicated that 75% of the tonnage of wild goldenseal in US trade from 1999-2010 was wild harvested. In the absence of more comprehensive and systematic monitoring and documentation of wild goldenseal baseline population data and volumes in domestic trade in the United States, the harvest pressure on the wild population is not quantifiable. Some illegal wild harvest of goldenseal subpopulations in Canada occurs.71,72 Wild harvest in some parts of the species’ range in the United States is likely increasing, especially where wild collection remains an important source of income and unemployment is high.47 In Indiana, for example, collection pressure has increased dramatically over the last decade (C. Floyd email to L. Oliver, November 30, 2012). Current Outlook and Moving Forward Conservation concerns that led to goldenseal’s inclusion in CITES Appendix II in 1997 stimulated research on what is needed for goldenseal to survive in its remaining natural habitat, much of which informed the updated NatureServe ranking in 20124 and the first global IUCN Red List assessment in 2017.1 Without the inclusion of goldenseal in CITES Appendix II and the subsequent shift in the international commercial goldenseal market from wild-harvested to cultivated supply, it is probable that this species would now be more seriously threatened with extinction than it appears to be at present. CITES permit requirements reduce unsustainable wild harvest and promote protection of goldenseal and its habitat, and removing these requirements could eliminate the most effective mechanism currently available to avoid greater extinction risk. Failure of resource managers and the herbal industry to take stronger actions to reduce the main threats — population decline from habitat loss and unsustainable levels of wild harvest — risks the viability of the species, commerce, and the livelihoods of those that rely on this resource. In Situ Conservation Goldenseal is not listed under the US Endangered Species Act and therefore is not protected under US federal law. Protection within states varies considerably, both in terms of how states designate and protect imperiled plants in general, and goldenseal’s protection across the states in which it occurs. The USDA PLANTS database tracks state-level legal protection. In 2018, goldenseal was considered Endangered, Threatened, Vulnerable, or of Special Concern in 12 out of the 26 states in which it occurs.73 Another measure of species imperilment at the state level is NatureServe’s state conservation rankings. According to NatureServe’s state ranks, goldenseal is Critically Imperiled or Imperiled in 12 states on the periphery of its range; Vulnerable in seven states, some of which are in the core of its range; and Apparently Secure or Secure in the remaining seven core-range states where it is native.4 There is a need to more adequately assess whether state regulations are sufficient to protect wild populations of goldenseal. Targeted field studies are warranted to ensure that the population integrity (area occupied and conditions) meets the lower threshold of each state’s NatureServe ranking. Field inventory is an ideal method to inform these thresholds; however, they are typically reserved for the “rarest of the rare” species due to limitations in resources. Given goldenseal’s economic and medicinal value and the ongoing threats that it faces, states should consider prioritizing goldenseal for field inventory to avoid further decline in its habitat and population. Many subpopulations throughout goldenseal’s range occur on land managed by national, state, local, or private organizations, including some subpopulations within Nature Conservancy preserves. Plant collecting on federal land is either forbidden (e.g., on National Park Service land) or requires permits (e.g., on Forest Service land). Harvest regulations differ from state to state. Some states, such as Pennsylvania, require permits for collection on State Forest land or the written permission of landowners for collection on privately owned land.74 But harvest and interstate commerce of goldenseal root and rhizome as a botanical commodity remain largely unregulated and unmonitored. The Indiana Department of Natural Resources reported an increased demand for this species and concern that the volume of material exported from Indiana will lead to decline of the species in the state. Plants on public and protected lands need protection from illegal collecting71 and application of good stewardship practices (e.g., late-season harvest to allow seed dispersal) where collecting is permitted.74 Existing regulations protecting goldenseal and other non-timber forest products on public and protected lands need to be better integrated into forest and other resource management plans and practices.75 Goldenseal was assessed as threatened by COSEWIC in 199142 and reassessed as threatened in 2000.43 Goldenseal has federal protection in Canada under the Species at Risk Act and in the province of Ontario under Ontario’s Endangered Species Act. Monitoring undertaken in Ontario in 1998 documented the loss of three previously known subpopulations but an overall stable, or possibly increasing, colony size.76 A recovery strategy for goldenseal in Ontario was published in 2016 in compliance with federal and provincial requirements for species at risk, and it recommended measures “to maintain existing populations at sustainable levels.”71 International trade of wild-collected goldenseal from Canada has not been permitted since the species was listed in CITES Appendix II because all wild harvest is considered by the Canadian CITES Scientific Authority (Canadian Wildlife Service, Environment and Climate Change Canada) to be detrimental to the survival of the Canadian subpopulations. All herbal medicinal products containing goldenseal, whatever their origin, must contain only cultivated material to receive marketing authorization and a product license for commercial sale in Canada.19 The NatureServe and IUCN conservation status assessments of goldenseal highlight “habitat depletion as one of the biggest negative impacts on goldenseal” and the need for legal protection “that prevents the destruction of habitat where goldenseal grows natively,” according to Ed Fletcher, the director of quality and sustainability at Herbal Ingenuity, a raw material supplier based in Wilkesboro, North Carolina (E. Fletcher email to C. Yearsley, March 17, 2018). Josef Brinckmann, the medicinal plants and botanical supply chain research fellow at Traditional Medicinals, a wellness teas company based in Sebastopol, California, explained that habitat loss through deforestation and land use change threatens “all wild forest plants, including goldenseal. Our last remaining biodiverse forests need to be conserved and expanded through reforestation,” he wrote (J. Brinckmann email to C. Yearsley, March 21, 2018). One such example of wild forest conservation is the 379-acre UpS Sanctuary in Rutland, Ohio, and other sanctuaries maintained by UpS members.77 Potential for Sustainable Wild Collection In his monograph on goldenseal published in 2011, herbal expert, photographer, and author Steven Foster wrote, “One of the big questions facing the future of goldenseal is whether there is enough supply, especially of wild-harvested root, to meet the demand.”17 Although loss of forest habitat has been the primary cause of decline of goldenseal over time, the sustainability of wild harvest is also a concern. A conservation assessment of goldenseal prepared by the USDA Forest Service in 200378 recommended that “to successfully maintain and increase the existing Hydrastis canadensis populations [on Forest Service lands], harvesting should not be allowed.”17 In 1997, ecologist and educator Joy Bannerman, in an HerbalGram article from issue 41, wrote: There is presently no scientifically valid guideline for “ethical and sustainable harvesting” [of goldenseal] in the wild since significant aspects of population and reproductive biology are unknown. Statements by herbal companies that such material has been “ethically wildcrafted” or the assurance that such is the case by having collectors or sellers sign a document to this effect is scientifically indefensible at this time.5 Since then, however, there has been more research on what goldenseal needs to survive and population dynamics of this species (low instances of seed production, high energetic cost of flowering, low genetic diversity, and small, isolated populations), and work on protocols for sustainable wild harvest of medicinal plants in general also has advanced.79-82 The herbal industry is in a better position now to demonstrate that goldenseal can be wild harvested sustainably. The USDA requires implementation of a detailed, audited, and monitored sustainable resource management plan for wild-collected herbs in the United States that are certified as organic under the National Organic Program in compliance with the Organic Wild-crop Harvesting Practice Standard.83 In addition, AHPA has developed voluntary guidelines for Good Agricultural and Collection Practices (GACPs) that focus on desired quality and long-term sustainability for botanicals in general.81 AHPA’s recommendations include: Obtain necessary permits, licenses, and permissions for access to public or private property. Choose collection sites that contain “healthy stands of plants growing in their normal range and in large enough quantities for collection to be sustainable.” Use “collection practices that are appropriate to each species and collection area and that minimize damage to the local habitat.” Avoid harvest of “species listed as endangered or that are not allowed to be harvested under state regulations due to concerns about over-harvest.” Collect mature plants “only from stands … that are abundant and healthy, with multiple plants of differing ages (seedling, juvenile, and mature).” Use collection practices for specific plant parts “that maintain population stability.” Use “propagation and regeneration techniques during harvest.” Use “habitat stewardship techniques during harvest.” Maintain records “that document information and collection practices that ensure the sustainability of the harvest.” Ensure all harvested plants are identified correctly. Develop a “comprehensive written wild collection plan.” While general guidance on good harvesting practices is a step forward, companies are not required to develop standard operating procedures to implement AHPA’s GACP guidelines. There is a significant gap in assurance and rigor between recommendations and audited standards. Species that are at high risk of unsustainable harvest require a management system that includes careful evaluation of sustainable yield, monitoring of harvest impacts, verification of good practices, and traceability from the source to the market. Two verification schemes that focus specifically on these aspects include the FairWild Standard and the Pennsylvania Certified Organic (PCO) Forest Grown Verification Program. The FairWild Standard is an independent, third-party-audited certification program.80 It is, according to Brinckmann, “arguably the most rigorous voluntary international standard designed specifically for sustainable wild collection of medicinal plants” (J. Brinckmann email to C. Yearsley, March 17, 2018). The FairWild Standard has been implemented in Europe, Africa, and Asia, but not yet in North America. The PCO Forest Grown Verification Program is a voluntary, third-party-audited certification scheme for non-timber forest products.84 Although it primarily focuses on organic principles, the program may address some of the sustainability concerns about the effects of non-local plants with limited genetic diversity on wild subpopulations of goldenseal. American ginseng (Panax quinquefolius, Araliaceae) root, for example, is currently available with this certification,85 and a USDA Conservation Innovation Grant was awarded to Rural Action, Inc. and UpS to support the development of Forest Grown Verification standards for goldenseal and several other wild-harvested species in the eastern United States.86 Conservation of Goldenseal as a Crop Wild Relative Techniques for cultivated and forest-grown botanical species have become better known and more accessible (e.g., Davis and Persons 2014),47 and the positive effect of cultivation on product quality has become better understood.87 However, little information is available about the degree to which cultivation of goldenseal depends on wild sources of propagating stock (i.e., goldenseal roots, rhizomes, and/or seeds). The continued growth and viability of commercial goldenseal cultivation, including forest-grown, will rely on the availability of germplasm from genetically diverse and ecologically robust wild sources.88 Availability of locally adapted germplasm is particularly important for the expansion of forest-grown operations. Conservation of in situ wild populations of crop species and ex situ conservation of genetically diverse and viable seed and other genetic material (e.g., using tissue culture for clonal species or species with recalcitrant seeds) for propagation are essential to maintaining and improving agricultural production. Wild populations of species in cultivation may have “traits that infer protection from environmental stressors and disease.”61 As molecular and genetic techniques become more cost effective, they can be used to identify and select the desired genetically beneficial traits for crop plants.61 Ex situ conservation of goldenseal germplasm and other genetic material is also important for restoration in its natural habitat. US government agencies, led by the Bureau of Land Management, have created a National Seed Strategy to provide plant material for cultivation and restoration of native plant species.89 If goldenseal has relatively low genetic diversity within and across its wild subpopulations, as indicated by preliminary studies,69 a major conservation objective for this species should be to maintain genetic diversity in isolated wild subpopulations (both large and small), and to carefully select and store genetically diverse plants ex situ.63,69 Additionally, safeguarding the genetic variability of goldenseal will require ensuring the persistence of even the smallest patches until the genetic variability on a regional scale has been established. A Path Forward A successful conservation plan for goldenseal must ensure that the species persists, and it must also satisfy a persistent commercial market. A research, protection, management, and communication plan that focuses on the distribution of goldenseal across the landscape in patches and on the importance of each patch, and that combines the efforts of regulators, resource managers, researchers, industry, and conservationists, offers a way forward. We (the authors) propose an emphasis on: Field inventory in key states with the highest reported abundance of goldenseal to verify state conservation status ranks; Improved protection of wild goldenseal subpopulations across its remaining distribution; Population viability analyses to better understand patch extinction risk, growth, and response to harvest by region; Application of a robust monitoring and management system of wild harvest where it can be sustainable, and that builds on traditional, local knowledge and practices of experienced harvesters; Adoption of ecologically sound protocols for forest-grown production; Use of goldenseal sourced from verifiable and traceable sustainable production systems, whether cultivated, wild-harvested, or forest-grown (and willingness to support related additional costs); Genetic studies by region to identify and locate patches with different genotypes; Preservation of seed for genotypes identified, and creation of sources of root and rhizome stock for cultivators by region; and Use of new kinds of data to track the status of goldenseal, including remote sensing, genetic sampling, citizen science, and social media. Conclusion The IUCN Red List and NatureServe criteria and processes are designed to draw upon the best available information about a species to assess the species’ risk of extinction. This includes information about a species’ population distribution, size, and trends, as well as its ecology, habitat preferences, impacts of threats, and existing conservation actions. Another aim of these complementary assessments is to provide transparency and documentation in the process of assigning a conservation rank. Conservation status assessments of economically important species such as goldenseal can be controversial, given what is at stake: the species’ conservation, market demand, and livelihoods of harvesters and others involved in the industry. However, these risk-ranking protocols have been shown to reliably forecast extinction risk even when there is some degree of data uncertainty.90 Neither IUCN Red List assessments nor NatureServe rankings are directly linked to legislative or regulatory responses. Their intended use is to inform the development of policy, legislation, and conservation actions at local, regional, national, and international levels to prevent extinction and improve conservation status.91 In the case of goldenseal, maintaining monitoring and control of international trade, strengthening monitoring and control of domestic wild-harvest and trade, and improving in situ and ex situ conservation of subpopulations in the United States and Canada will help ensure that this popular medicinal herb continues to be available to the herbal industry and consumers. Leah E. Oliver is a senior research botanist at NatureServe, where she assesses the conservation status of plants native to North America. For more than 15 years, she has collaborated with botanists in the United States and Canada on topics related to threats and trends impacting plant conservation through the lens of NatureServe and IUCN methodologies. Her research interests include medicinal and economically important plants, endemism and rarity, bioinformatics, and non-vascular plants. Danna J. Leaman, PhD, is an ethnobotanist and conservation biologist. She co-chairs the Medicinal Plant Specialist Group of the Species Survival Commission of the IUCN and is currently the IUCN Red List Authority for medicinal plant assessments. She is a member of the American Botanical Council Advisory Board, a trustee of the FairWild Foundation, and a non-government science member of COSEWIC. SIDEBAR Conservation Status Assessments Conservation status assessments are key to ensuring the implementation of appropriate conservation measures. These unbiased metrics of conservation condition are used to identify which species are most at risk of extinction, and are separate from governmental regulation and policy. For example, analyses of NatureServe’s data have repeatedly shown that the number of species listed under the US Endangered Species Act is an order of magnitude less than the number of at-risk species in the United States — a disparity that stems largely from politics and lack of resources.57 As a result, federal and subnational (i.e., state or provincial) organizations and government agencies in the United States and Canada rely on NatureServe’s status assessments, called “ranks,” for conservation prioritization. Internationally, the IUCN Red List assessments are the most widely used methodology for conservation prioritization. NatureServe Ranks and IUCN Red List Categories NatureServe is a nonprofit biodiversity conservation organization made up of a network of more than 80 Natural Heritage Programs in the United States and Latin America, and provincial or regional Conservation Data Centers in Canada. The NatureServe Network collects comprehensive information about imperiled species and entire ecosystems, transforms the data into knowledge products and visualizations, and provides meaning through expert analyses to guide decision-making, implement action, and enhance conservation outcomes. NatureServe rankings are undertaken on three geographic scales: Subnational (S ranks), National (N ranks), and Global (G ranks). The IUCN Red List is organized and published by the IUCN with assessments contributed by a large network of expert specialist groups, Red List authorities, and Red List partners. It is considered to be the global standard for conservation status assessments. Red List assessors assign a category of extinction risk using a rule-based system of criteria and thresholds that accommodate both data-poor and data-rich species. Assessment categories and criteria are applied on a global scale,1 with adjustments for national- and regional-scale applications.58 NatureServe’s ranks and Red List assessments consider similar factors related to each species’ distribution, threats, and trends, but weigh and evaluate the data differently (Table 1).59,60 These differences produce complementary interpretations of extinction risk and provide users with nuanced perspectives to make informed conservation decisions. Recent publications have compared the two systems and provide a more detailed overview of the similarities and differences.59,61 Both systems enable assessors to objectively apply rules for conservation status assessments. The IUCN Red List assessments require two external reviewers of content, information quality, and consistency with the Red List methodology. As the North American Red List Authority for plants and a Red List partner institution, NatureServe has years of experience applying Red List criteria to assess species. Similarity between the two systems makes it more cost-efficient to assign Red List categories and global ranks at the same time rather than separately. NatureServe’s database is broadly compatible with IUCN’s Red List database, the Species Information Service (SIS), so the information can be shared across platforms. A species assessment is considered a snapshot in time, or a reflection of the knowledge available when the species was assessed. Due to changing threats, conservation actions, and natural events, the conservation status of a species can change over time. Consequently, conservation status must be regularly reviewed. NatureServe and the Red List both recommend that assessments be updated at least once every 10 years. Data Uncertainty and Risk Tolerance The incompleteness and imperfect quality of available information that is considered relevant to extinction risk and the potential for assessors to be biased toward more precautionary (i.e., risk-averse) assessments are common concerns about assessing the conservation status of species. These concerns are valid because complete population data are not available for most plant species, and there is evidence suggesting that the tolerance of risk (i.e., a tendency toward lower or higher levels of risk in assessments) is most inconsistent for valuable, exploited species.62 Conservation status assessments for valuable, exploited species often require more and higher-quality data, and are more rigorously reviewed, so that the burden of proof is more stringent than assessments for less-valued species. To this end, NatureServe’s ranks and Red List assessments have standardized methods and tools to address uncertainty so that the resulting rank or category is comparable to those of other species. Additionally, NatureServe and the IUCN Red List have steps built into their assessment methodologies to reduce the potential for bias. NatureServe assessors, for example, are required to use a rank calculator that weighs factor information and determines a rank. The IUCN Red List requires consistency checks and two reviewers who are knowledgeable about the species and the Red List process. Both NatureServe and Red List assessments can be updated with new information or a new interpretation of existing information. References Oliver L. Hydrastis canadensis. The IUCN Red List of Threatened Species 2017: 2017e.T44340011A44340071. Available at: http://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T44340011A44340071.en. Accessed February 26, 2018. IUCN. 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