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Table of Contents
REVIEW ARTICLE
Year : 2021  |  Volume : 7  |  Issue : 3  |  Page : 299-306

Reviewing threats to wild rhodiola sachalinensis, a medicinally valuable yet vulnerable species


1 Traditional Medicinals, Sustainability Department, 4515 Ross Road, Sebastopol, California, 95472, USA
2 School of Life Sciences, University of KwaZulu-Natal, King Edward Avenue, Pietermaritzburg, 3209, South Africa; School of Veterinary and Life Sciences, Murdoch University, 90 South St., Murdoch, WA, 6150, Australia
3 Bundesamt für Naturschutz (BfN), Konstantinstr. 110, Bonn, 53179, Germany

Date of Submission16-Feb-2021
Date of Acceptance31-Mar-2021
Date of Web Publication9-Aug-2021

Correspondence Address:
Prof. Josef A Brinckmann
Traditional Medicinals, Sustainability Department, 4515 Ross Road, Sebastopol, California 95472
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/wjtcm.wjtcm_47_21

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  Abstract 


Occurring in China, DPR Korea, Japan, and Russian Federation and classified in the Red List of Chinese Flora as a vulnerable species, Rhodiola sachalinensis Boriss. is used increasingly in cosmetics, dietary supplements, and Traditional Chinese Medicines (TCMs). The aim of this study was to evaluate the (i) conservation status, harvesting and trade levels of R. sachalinensis, (ii) current state of experimental and commercial farming, and (iii) evidence of substitution or interchangeable use of R. sachalinensis with other Rhodiola species. We assessed data from multiple disciplines and languages including studies on R. sachalinensis biology and ecology, information on impacts of wild harvest, management measures, and current levels of cultivation. Our assessment shows that while R. sachalinensis is increasingly produced by cultivation, wild populations are decreasing and face multiple threats. These include (a) habitat loss including due to oil and gas infrastructure development on Sakhalin island, (b) climate change impacts on alpine ecosystems, and (c) overexploitation of wild plants to satisfy the growing commercial demand. Assessments of the conservation status of R. sachalinensis should commence in each Range State, as well as resource assessments and monitoring of harvesting and trade of wild R. sachalinensis. Even with increased reliance on cultivation, biodiversity conservation, and genetic diversity in wild populations are relevant to future use of this species.

Keywords: Conservation, Rhodiola rosea ssp. sachalinensis, Rhodiola sachalinensis, sustainable production, Traditional Chinese Medicine


How to cite this article:
Brinckmann JA, Cunningham AB, V. Harter DE. Reviewing threats to wild rhodiola sachalinensis, a medicinally valuable yet vulnerable species. World J Tradit Chin Med 2021;7:299-306

How to cite this URL:
Brinckmann JA, Cunningham AB, V. Harter DE. Reviewing threats to wild rhodiola sachalinensis, a medicinally valuable yet vulnerable species. World J Tradit Chin Med [serial online] 2021 [cited 2022 Jan 19];7:299-306. Available from: https://www.wjtcm.net/text.asp?2021/7/3/299/323490




  Introduction Top


Rhodiola sachalinensis Borissova, Crassulaceae (“gaoshanhongjingtian” (

), high mountain rhodiola or “kuyehongjingtian” (

), Sakhalin rhodiola), is a rare species with a fragmented distribution[1] in China, DPR Korea, Russian Federation, and Japan.[2] R. sachalinensis has become a popular Rhodiola species[3] traded in Traditional Chinese Medicine (TCM) markets[4] and is also widely used in dietary supplements[5] and cosmetics. However, there are conservation concerns about this vulnerable (VU) species.[6],[7] This study evaluates the (i) conservation status, harvesting, and trade in R. sachalinensis, (ii) current cultivation, and (iii) evidence of interchangeable use of R. sachalinensis with other Rhodiola species.


  Methods Top


We reviewed published studies on R. sachalinensis biology and ecology, information on impacts of wild harvest, management measures, and on the current level of cultivation. Our data collection strategy involved using a group of search terms in multiple languages (Chinese, English, Japanese, Korean, and Russian). Search terms included R. sachalinensis, traditional medicine, wild collection, cultivation, export trade, harvesting, conservation status, protected, threatened, red list, and red book. We used the online academic search engine Google Scholar, China Academic Journals (CNKI) database, and ResearchGate, a professional network for scientists and researchers, as well as patent databases of the China National Intellectual Property Administration, Korean Intellectual Property Office, United States Patent and Trademark Office, and World Intellectual Property Organization. For information on R. sachalinensis occurrence, conservation, legal, and regulatory status, we searched the websites and databases of governmental organizations such as ministries of agriculture, environment, health, medicines, natural resources and ecology, and tourism, respectively.


  Results Top


Taxonomy

While “The Plant List”, Version 1.1. (2013) treats R. sachalinensis Borissova as a synonym of Sedum roseum (L.) Scop,[8] and the International Crassulaceae Network lists R. sachalinensis Borissova, Sedum sachalinense (Borissova) Voroschilov, and Rhodiola rosea ssp. sachalinensis (Borissova) S. Gontcharova as synonyms of R. rosea L.,[9] Chinese authorities on botany, taxonomy, threatened species, and TCM treat R. sachalinensis as a distinct article; for example, botanists at Flora of China,[2] and at the Ministry of Environmental Protection and Chinese Academy of Sciences (Red List of Chinese Flora),[6] as well as pharmacognosists at provincial TCM drug product administrations. Regardless of some differing taxonomic opinions, in China, R. rosea and R. sachalinensis are classified and traded as separate articles of commerce, sourced from separate geographic origins, R. rosea from Xinjiang and R. sachalinensis from Jilin and Heilongjiang, each with distinct characteristics described in monographs. As we reported earlier in Cunningham et al.,[10] we treat R. sachalinensis as a distinct species for three reasons. First, chemotaxonomic studies by Booker et al.[11] and Liu et al.,[12] show chemical differences between R. rosea (collected in Xinjiang) and R. sachalinensis (collected in Heilongjiang and Liaoning). While the observed differences in Liu et al.,[12] using a high performance liquid chromatography-diode array detection and ultraviolet spectrophotometric (HPLC-DAD/UV) method, based on eight compounds of four chemical classes (phenylpropanoids, phenylethanol derivatives, flavonoids, and phenolic acids) were only weak, Booker et al.,[11] using general metabolomic fingerprinting but also specific high-performance thin-layer chromatography (HPTLC) methods for testing of the rosavin and salidroside marker spectra, found compelling differences between R. rosea and R. sachalinensis samples. In a DNA barcoding study of six Rhodiola species, Zhang et al.[13] were able to identify and differentiate five of the six species including R. sachalinensis. Their analysis showed that five accessions of R. rosea, obtained from different locations, formed a clade (evolved from a common ancestor) with their only accession of R. sachalinensis as well as with one accession of R. tangutica (Maxim.) S. H. Fu (

-Tangut hong jing tian), noting that R. rosea and R. sachalinensis have strong morphological similarity. Second, treating R. rosea and R. sachalinensis as distinct species fits with the taxonomic perspectives of Flora of China,[2] and of Qin et al.[7] (threatened species list of Chinese higher plants), among other Chinese and Korean scientists. In the Flora of China, some morphological differences between R. sachalinensis and R. rosea are described. Third, while R. rosea has a circumpolar distribution, R. sachalinensis has a much more limited geographic distribution in Northeast China, DPR Korea, small parts of Japan, and the Russian Far East.

Chemistry and medicinal uses

The root and rhizome of R. sachalinensis contain phenylpropanoids such as the cinnamyl alcohol glycosides rosarin and rosavin, the phenylethanoid compound salidroside with its aglycone tyrosol, flavonols such as rhodionin and rhodiosin,[14] monoterpene glycosides (sachalosides I and II), flavonol bisdesmosides (sachalosides III and IV), and cyanogenic glycosides (sachaloside V).[15] The Jilin provincial standards for TCM materials require the herbal drug “Rhodiolae Sachalinensis Radix et Rhizoma” to contain not-less-than (NLT) 0.20% of salidroside and NLT 0.020% of tyrosol, calculated on a dried drug basis.[16] Less specifically, the Zhejiang provincial standards for TCM materials require pharmacopoeial quality R. sachalinensis to contain NLT 22.0% extractive matter and NLT 6.0% total rhodiola glycosides.[17] According to TCM theory, R. sachalinensis root and rhizome acts to invigorate qi and promote blood circulation and is indicated for treating conditions such as qi deficiency and blood stasis, chest pain, angina, stroke, hemiplegia (paralysis of one side of the body), fatigue, asthma, and panting.[16]

Ecology and distribution

The habitat of R. sachalinensis is described as forested slopes, gravel slopes, and alpine tundra in northeastern China (Jilin, Heilongjiang), DPR Korea, Russian Federation, and Japan,[2] as well as in rock crevices and stony sites on some volcanic oceanic islands of Japan and the Russian Federation.[18]

In China, R. sachalinensis is distributed mainly in the Changbai Mountain Range of northeastern Jilin province [Figure 1], and Heilongjiang province in the Zhangguangcai Mountains[19] and Daxingan Mountains.[20] It is found, in the Yanbian Korean Autonomous Prefecture of China's Jilin Province,[21] which borders both Primorsky Territory, Far Eastern Federal District, Russian Federation, as well as the northernmost province of DPR Korea, North Hamgyong Province. In the Changbai Mountains Nature Reserve (CMNR), R. sachalinensis is recorded at an altitude range of 1600–2500 m above sea level (a. s. l.)[22] and shares habitat with “changbaihongjingtian” (

, Rhodiola angusta Nakai).[5] In DPR Korea, R. sachalinensis occurs in the Baekdudaegan Mountain Range, growing in cracks near the tops of Mountains Paekdu, an active super volcano, between 1800 and 5000 m a. s. l., as well as on Mountains Potae and Mountains Rangrim.[23],[24]
Figure 1: A map showing the recorded geographic distribution of Rhodiola sachalinensis in yellow. This range extends from the type locality in the Russian Far East (Sakhalin Island) to the Changbai Mountains that span the border of China and DPR Korea, as well as the Kuril islands north of Hokkaido, Japan. Map content informed by Global Biodiversity Information Facility data, Kunming Institute of Botany iFlora database, Gage et al. (2006), Sundukov and Sundukov (2020), and for Sakhalin Island, herbarium specimens

Click here to view


It is reported to occur on Shikotan Island (a disputed territory claimed by Japan and Russia)[25] and on the uninhabited Ekarma Island (Russia), which consists of two overlapping volcanoes reaching 1170 m a. s. l.,[26] near the center of the Kuril Islands chain in the Sea of Okhotsk. Furthermore, the species occurs on the Habomai islets (disputed territory between Japan and Russia), in the southernmost Kuril Islands,[27] and on the Russian islands of Sakhalin and Moneron.[28] On Sakhalin Island, one of the largest islands in the boreal zone of the Pacific Ocean, R. sachalinensis occurs in ten of 13 recognized geobotanical areas, sharing habitat with R. rosea in eight of the 13 areas. In common with many other Rhodiola species, R. sachalinensis appears to favor habitat near perennial streams.[29]

R. sachalinensis is a long-lived, dioecious perennial that flowers between April and June and fruits from July to September. Regeneration is primarily from seed, although clonal sprouting from the rhizome is also likely to take place. The challenge posed by commercial harvesting is that removing whole plants (or entire rhizomes) prevents both reproduction from seed and through clonal sprouting. R. sachalinensis is known to be an outcrossing, insect pollinated species with wingless seeds.[30] Based on Random Amplified Polymorphic DNA analysis using 106 markers, a genetic difference has been discerned between R. sachalinensis plants from the Changbai Mountains compared to those in the Daxinganling Mountains.[20]

Furthermore, R. sachalinensis is known to be associated with 29 genera of endophytic fungi, some with economic potential as sources of novel antioxidant substances. Fifteen of these endophyte genera were found exclusively on R. sachalinensis compared to R. augusta and R. crenulata (Hook.f. & Thomson) H.Ohba.[5] A loss of wild populations of R. sachalinensis could also result in a loss of certain endophytes, along with their potential health benefits

Threats and trends

Human-induced threats are highly significant for several reasons. These include habitat loss due to infrastructure developments by the oil and gas industry,[31] habitat loss due to drying of streams and seepage areas, and encroachment by trees able to move to higher altitudes with a warmer climate,[32] and commercial exploitation. For example, Yan et al.[30] point out that: “The economic value of the plant has resulted in heavy collections in recent years, which induced its limited distribution and fragile habitat.”

While R. sachalinensis was classified as VU in the 2013 Red List of the Chinese Flora,[6] in the 2017 revision, its status was elaborated further to a classification of “VU B1ab (i, iii); D1”.[7] Criteria VU B1 means that the extent of occurrence in China is <20,000 km2. Furthermore, VU B1ab means that the geographic range is severely fragmented or that there are less than ten locations where the species is known to occur and that continuing decline is observed, estimated, inferred, or projected in (i) extent of occurrence and (iii) quality of habitat. The additional designation of VU D1 means that the population is very small or restricted or that the number of mature individuals is <1000.[33] [Table 1] summarizes the conservation status of wild R. sachalinensis in the countries where it reportedly occurs.
Table 1: Conservation status of Rhodiola sachalinensis

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Several factors are affecting the habitats where R. sachalinensis occurs, even within protected areas. On Sakhalin Island, economic development has been focused on resource extraction (forestry, fisheries, coal, oil, and gas), particularly since the mid-1990's.[39] Infrastructure development associated with the oil and gas industry has directly influenced Rhodiola habitat. Plans for the 800 km long onshore pipeline, proposed as a part of the “Sakhalin II Phase 2” development project, envisaged transport of oil and gas from the oil fields on the northeast of the island to Aniva Bay in the south, crossing two nature reserves, Makarovsky Reserve and Izubrovy Reserve, where Rhodiola species occur. The Environmental Impact Assessment (EIA) for this pipeline development was concerned about the following effects on habitat: “soil erosion and compaction, physical disturbance to surface watercourses, contamination of groundwater, due to release of sewage treatment plant effluent and hydrotest waters, habitat loss and fragmentation, and direct impacts to protected or rare species of fauna and flora.”[28] Furthermore, radioactive contamination of vegetation on Sakhalin Island due to fallout from the Fukushima Nuclear Power Plant in Japan might be an issue of concern. It has been shown that 137Cs levels were higher in mosses and lichens compared to herbaceous and woody plants;[40] however, further monitoring of wild harvested R. sachalinensis from the Sakhalin Oblast may be advisable, given the human consumption of this species.

The CMNR, which was declared in 1960, forms part of the Changbai Mountain Biosphere Reserve (CMBR)[41] and is considered to be well protected.[42] At a landscape scale, however, Ma et al.[43] showed that only 25.3% of protection objectives had achieved their conservation targets and concluded conservation efficiency was low. Infrastructure development associated with tourism on both the Chinese and North Korean sides of the border have also affected habitats on the mountain. As have infrastructure for bottled water from the Paektu Spa and for military installations on the North Korean side.

The effects of climate change also pose a challenge. A dendrochronology study in the Zhangguangcai Mountains, over a 211-year period (1803–2013) showed that northeast China has been affected by climate oscillations in the past, which might increase with current global warming, potentially reducing habitat suitability for R. sachalinensis.[32] While no studies have modeled impacts of climate change on R. sachalinensis populations, the implications of climate change, described by You et al.,[44] for declining habitat suitability for other high altitude Rhodiola species may be applicable.

Human impacts on R. sachalinensis fit in with trends in commercial exploitation in relation to other Rhodiola species. For example, based on fieldwork in China, Jiang et al.[45] considered that R. sachalinensis was “on the edge of extinction due to constant consumption and the disturbance of the habitats.” Based on their fieldwork on Changbai Mountain a decade later, Yan et al.[46] supported this concern about wild R. sachalinensis populations. While the Red List of Chinese Flora classification is “VU B1ab (i, iii); D1”[7] both Yan et al.[30] and Zhao et al.,[1] in their studies on the genetics of wild and ex situ populations, considered this species endangered.

Trade

Utilization

R. sachalinensis has become one of the most popular TCM materials obtained from Rhodiola species.[47] Official monographs for its use in TCM are published by provincial drug administrations.[16],[17] Moreover, as such, the herbal drug “Rhodiolae Sachalinensis Radix et Rhizoma” is traded at TCM markets such as the Hebei Anguo Medicinal Material Market.[4] R. sachalinensis also ranks among the most widely used Rhodiola species in dietary supplement products.[5] Yanbian University (Yanbian Korean Autonomous Prefecture, Jilin) holds a Chinese patent for production of a health food supplement product in the form of dispersible tablets containing an extract of R. sachalinensis with hypoglycaemic function.[48] The Chinese biotechnology company Taizhou Danding Biotechnology Co., Ltd. (Taizhou, Jiangsu) holds a U. S. patent, describing methods for extracting the pharmacologically active substance herbacetin from R. sachalinensis and other Rhodiola species.[49] Res Green Biological Engineering Group Co., Ltd (Liuyang, Hunan) holds a Chinese patent for production of a topical body milk product, composed mainly of an extract of R. sachalinensis root, indicated for use as a skin moisturizer, to slow down skin aging, and restore skin elasticity.[50] In Republic of Korea, extracts of R. sachalinensis are used as hair- and skin-care functional components of cosmetic products.[24]

Legal trade

Quantifying the level of international trade was not possible because there are no known species-specific harmonized system tariff codes (HS Codes) assigned in any country for any commercial forms of this species. Because it is reported that “gaoshanhongjingtian” (

, R. sachalinensis) may be traded, intentionally or unintentionally, as a substitute for “dahuahongjingtian” (

, Rhodiola crenulata) or could also be represented simply as “hongjingtian” (

, R. rosea), due to some authorities treating it as a synonym, the raw material (if exported) could be lumped in with other Rhodiola species raw materials under the general HS Code 1211.90 (other plants and parts of plants, of a kind used primarily in pharmacy). It is also conceivable that exports of extracts made from this species would be lumped in with other Rhodiola species extracts under the general HS Code 1302.19 (other vegetable saps and extracts). No evidence of illegal trade of R. sachalinensis was found.

Management measures and cultivation

National legal instruments

The “Regulations of the People's Republic of China on Wild Plants Protection”[51] have been in effect since 1997 and cover all activities concerning the protection, development, and utilization of wild plants. The regulation references a national list of wild plants under special state protection that is periodically updated by the government. A new list was in preparation in 2020. It is anticipated that several species of Rhodiola will be placed under second class protection, which would make issuance of a collection permit compulsory. In 2017, the conservation status of R. sachalinensis was assessed as Vulnerable (VU B1ab [i, iii]; D1) [Table 1].[7]

Management measures and challenges

Habitat conservation

R. sachalinensis occurs in several protected areas. The species is listed as a key protected plant species occurring in the Ecologically Critical Area of broad-leaved Korean pine mixed forest in the CMNR.[22] The occurrence of this species within the CMNR, which is also internationally recognized as a United Nations Educational, Scientific and Cultural Organisation Biosphere Reserve, are positive factors with regard to management. So is the fact that in 1986, the CMNR was officially recognized as a national-level nature reserve emphasizing forest protection.[42] R. sachalinensis is included on the list of wild plants under Jilin provincial protection in the CMNR for two reasons: It is (1) used in medicine (economic value); and (2) an alpine tundra seed plant, rare in quantity.[52] In 2000, the Changbai Mountain Academy of Sciences, Erdao Baihe Town Antu County, Jilin, began ex situ conservation of R. sachalinensis at the academy, which is within the CMNR. Seeds and seedlings were transplanted into an ex situ conservation area, situated only tens of kilometers from the main range of distribution of wild R. sachalinensis, sharing similar climatic conditions. About 500 individuals survived in the ex situ conservation site.[1] What could further strengthen these management measures is the recommendation by Tang et al.[53] for multiscale, multistakeholder conservation efforts in the Changbai/Paektu mountain range. Forming the northernmost part of the Baekdudaegan Mountain Range that stretches over 1400 km from Mountains Paektu at the Chinese/DPR Korean border to Mt. Jiri in Republic of Korea,[54] the cultural significance of this mountain range in both DPR Korea and Republic of Korea is a factor that may support transboundary conservation and landscape level management measures. Where R. sachalinensis occurs in the northern Baekdudaegan Mountain Range,[24] there are nationally protected areas such as national parks, provincial parks, and natural forests covering 3035 km2. 63.4% is state land, 1.9% is public land, and 34.7% is privately owned. A study has been carried out, aiming toward a collaborative strategy between China, DPR Korea, and Republic of Korea for an environmental protection management plan in the Mount Paektu and Tuman River area, where R. sachalinensis is listed as a protected species on the China side. The Tuman River forms a part of the international boundary between China, DPR Korea, and Russian Federation.[55]

In the Russian Federation, R. sachalinensis is protected within the state cadaster of specially protected natural areas (SPNAs) of regional significance in the Sakhalin Region.[56] R. sachalinensis also shares habitat with Rhodiola ishidae Hara, within an SPNA of federal significance, Kurilsky State Nature Reserve.[57] The reserve area is 65,861.5 ha (0.75% of the Sakhalin Oblast) and consists of three clusters: Two on Kunashir Island, Tyatinsky (northern), and Alekhinsky (southern), and one on the Lesser Kuril Chain, which includes Shikotan Island, where R. sachalinensis reportedly occurs.[58] On Sakhalin Island, R. sachalinensis occurs in two regionally significant protected areas, Makarovsky Reserve and Izubrovy Reserve, although these may be difficult to manage in consideration of the oil and gas pipelines.[31]

Cultivation and propagation

R. sachalinensis is cultivated as a field crop in Jilin, China.[59] Of the Rhodiola species cultivated in China, R. sachalinensis and R. angusta reportedly comprise the largest planting area.[5] Cultivation is challenging, however. First, due to low salidroside levels in cultivated plants (0.1%–0.5%) compared to wild populations on Changbai Mountain (0.5%–1.5%), and second, due to root rot[60] and leaf wilt[59] in cultivated material. From 2007 to 2011, 75%–95% of fields with cultivated R. sachalinensis in Siping District were affected by root rot caused by Fusarium verticillioides.[60] The effect of root rot gets worse where R. sachalinensis plants are grown at a high density, requiring the use of different antibacterial chemical treatments.[61] A South Korean patent was granted for methods to cultivate R. sachalinensis as a 4-year field crop, at a lower altitude range (700–1000 m a. s. l.), claiming to yield larger roots than those of wild populations at their higher altitude habitat.[23] A Chinese patent was also granted for the invention of domesticating wild R. sachalinensis at an altitude of 800 m a. s. l.[62] Other Chinese patents have been granted for new methods of breeding[63] and for cultivation of an improved variety of R. sachalinensis in a low-altitude plain area, claiming to solve the problems of poor seed germination, root rot, and low yield.[64] Growing R. sachalinensis as a shade crop using colored polyethylene shade has shown positive effects on the accumulation of bioactive compounds. While the use of red film slightly decreased root biomass of 3–4-year-old R. sachalinensis, it significantly increased salidroside content.[65] However, the use of yellow, blue, and/or green polyethylene shade significantly decreased the salidroside content of the roots.[66] A study aiming to acquire homozygous tetraploid germplasm of R. sachalinensis resulted in providing a scientific basis for polyploid breeding.[67] In northwestern Sichuan, 280,000 R. sachalinensis seedlings were also transplanted as a part of a desertification control demonstration project, with a reported survival rate of 40%–50%, according to Chengdu Tiandi Net Information Technology Ltd.[10]

Regarding experimental artificial propagation, in vitro cultures have been obtained from the stems and leaves, the latter proving to be best suited for shoot induction.[68] Biotechnological methods are also being explored to produce the pharmacological active compound salidroside at higher levels to wild or cultivated plants. In R. sachalinensis cell suspension cultures, the salidroside content was ten times higher than in wild-collected plants. This finding could lead to a preference for biotechnological production over obtaining active compounds from field cultivated or wild-collected R. sachalinensis.[14] A study that analyzed genetic and epigenetic differentiation in different populations of R. sachalinensis including three natural populations and an ex situ population found that that the ex situ population possessed significantly different genetic and epigenetic population structures and HPLC fingerprint patterns. The researchers suggest that the ex situ environmental factors caused by different altitudes may play an important role in keeping hereditary characteristics of R. sachalinensis ex situ populations.[1]

Adulteration and substitution

First, the 2019 Jilin Provincial Standards for Chinese Medicinal Materials provide a detailed monograph for R. sachalinensis root and rhizome with four methods of identification (macroscopic, microscopic, TLC, and HPLC) to verify botanical identity.[16] Compendial monographs such as the Jilin Provincial Standards require a combination of techniques (orthogonal testing) due to the fact that a single identification method does not offer a certainty of 100% confidence. The material must conform to all four identification tests. Second, the Herbal Medicines Compendium of the United States Pharmacopoeia lists R. sachalinensis as a potential confounding material in the supply of official R. crenulata.[69] Admixture or substitution with other similar looking Rhodiola species is known to occur in trade. Based largely on data from Booker et al.,[11] the Botanical Adulterants Bulletin of the American Botanical Council, American Herbal Pharmacopoeia, and the University of Mississippi's National Center for Natural Products Research[70] make this statement: “Although substitution of R. rosea products with R. crenulata is considered the main problem with respect to authenticity of R. rosea, field work data suggest that other species are being implicated. A particular case is R. sachalinensis, a species that has a similar composition to R. rosea, containing rosavins (the marker compounds used to identify R. rosea), as well as salidroside, and is considered by some botanists to be the same species as R. rosea. To complicate matters, different populations of R. sachalinensis may display differences in their HPLC-ultraviolet detection (UV) fingerprints, making accurate species identification based on chemical analysis difficult. However, substitution with R. sachalinensis may become less of a concern, since its growing range has decreased significantly and it is now considered to be critically endangered in China.” On the other hand, R. sachalinensis is also traded explicitly and therefore it is also possible that R. sachalinensis products could be adulterated or mixed with other Rhodiola species themselves. DNA barcoding and chemical methods could help to differentiate Rhodiola species in such cases. For example, Wang and Guo used rapid static headspace-gas chromatography–mass spectrometry to effectively differentiate the rhizomes of R. sachalinensis from those of another medicinal Rhodiola species, “shengdihongjingtian” (

, Rhodiola sacra (Prain ex Raym.-Hamet) S. H. Fu).[71] Other methods have been developed that distinguish R. sachalinensis samples from other Rhodiola species including R. rosea, using nuclear magnetic resonance spectroscopy, metabolomics, and HPTLC,[11] as well as HPLC-DAD/UV followed by principal component analysis and nuclear magnetic resonance (HCA).[12]


  Conclusions Top


While R. sachalinensis is increasingly produced by cultivation, wild populations are small, VU and decreasing due to multiple threats. These include anthropogenic factors such as (a) habitat loss due to oil and gas infrastructure development, (b) climate change impacts on alpine ecosystems, and (c) overexploitation of wild plants to satisfy the growing demand for any Rhodiola species that are used interchangeably. Yet, only China has published an assessment of its conservation status. Our findings suggest that resource assessments should be carried out and that monitoring of harvesting and trade of wild R. sachalinensis should commence in all countries where remaining populations exist, in order to facilitate sustainable exploitation. Furthermore, whether the raw material supply is obtained from farm operations or from wild populations, we propose there is a need to implement credible voluntary sustainability standards with independent third-party inspection and certification. Even with increasing reliance on cultivation, biodiversity conservation, and genetic diversity in wild populations are relevant for the future of TCM.

Acknowledgment

This paper has been prepared in the course of a project funded by the German Ministry of the Environment, Nature Conservation and Nuclear Safety (BMU) and managed by the Federal Agency for Nature Conservation (BfN) (FKZ 3519532056) that enabled us to assess the conservation and trade issues facing R. sachalinensis. We would like to thank Honglin Li (Chengdu Institute of Biology) for her help in obtaining some key references in Chinese and for searching for internet-based trade in R. sachalinensis in China. Dr Ben Legler (Collections Manager, Stillinger Herbarium, University of Idaho) is thanked for his rapid response with regard to the R. sachalinensis specimen, he collected on Sakhalin Island. Expert advice that contributed to this work was also received from Dr. Uwe Schippmann, former head of the Plant Conservation Division of BfN. We also thank Dr. Daniel Wolf (BfN) for his review and comments on the final draft.

Financial support and sponsorship

Nil.

Conflicts of interest

Prof. Josef A. Brinckmann is an editorial Board member of World Journal of Traditional Chinese Medicine. The article was subject to the journal's standard procedures, with peer review handled independently of this editorial board member and their research groups.



 
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