Printer Friendly

Models of Cannabis Taxonomy, Cultural Bias, and Conflicts between Scientific and Vernacular Names.

Introduction

Controversies regarding the taxonomy and nomenclature of C. sativa have generated four recent publications in The Botanical Review. This present review is intended for a general audience, i.e., botanists not specializing in taxonomy and nomenclature. We address three issues considered opaque to generalists; specifically, how taxonomists: 1. circumscribe units into groups; 2. assign these groups to particular ranks; 3. assign names with due consideration to priority and other rules of nomenclature.

The first two points are subject to judgment: 1. Group circumscription may vary depending upon various taxonomic characters and species concepts. 2. Taxonomic ranks are relative levels within a hierarchy, and notoriously subjective. Darwin (1859) could not reconcile the continuous process of evolution with the discrete concept of taxonomic ranks. "I was much struck how entirely vague and arbitrary is the distinction between species and varieties."

The third point is governed by a legalistic document, the International Code of Nomenclature for Algae, Fungi, and Plants (ICN, McNeill, 2012). The ICN is periodically updated, and has become rather complicated. As our mentor Von Arx (1987) said, "nonspecialists have difficulties in understanding the code and adhering to its provisions." To be considered for formal recognition, a botanical name must meet several technical ICN provisions, e.g., effective and valid publication, typification (with herbarium specimens), and priority. The ICN is available online for consultation regarding these provisions. The names Cannabis sativa L. (Linnaeus, 1753) and C. indica Lam. (Lamarck, 1785) have met these provisions.

Despite C. sativa and C. indica holding nomenclatural legitimacy, their taxonomic acceptance remains a subjective decision, and depends on one's species concept. For example, many biologists (especially zoologists such as Ernst Mayr) conceptualize a species as all potentially interbreeding populations of an organism. C. sativa and C. indica are often presumed to have no physiological barriers to breeding (Small, 1972).

If C. sativa and C. indica are a single species according to Mayr's species concept, then only one name can be regarded as correct. The ICN decides this by priority, where the correct name for a taxon is its earliest legitimate epithet. "Correct" and "legitimate" have technical definitions in the ICN. So does "earliest." The ICN designates 1753--the publication year of Linnaeus's Species Plantarum--as the starting date of botanical nomenclature.

A review and discussion of Cannabis epithets in the scientific literature is urgently needed. A vernacular taxonomy of drug-type plants, "Sativa" and "Indica," has entangled and subsumed formal C. sativa and C. indica. Thousands of websites generalize about the morphological, phytochemical, organoleptic, and clinical properties of "Sativa" and "Indica." Tracing these collective generalizations to published sources is elusive; our search traces them back to Corral (2001) and Black and Capler (2003): "Sativa" is recommended for treating depression, headaches, nausea, and loss of appetite; it causes a stimulating and energizing type of psychoactivity. "Indica" is recommended for treating insomnia, pain, inflammation, muscle spasms, epilepsy, and glaucoma; it causes a relaxing and sedating psychoactivity. "Sativa" plants are said to produce much more [[DELTA].sup.9]-tetrahydrocannabinol (THC) than cannabidiol (CBD), and a terpenoid profile that smells "herbal" or "sweet." "Indica" plants are said to produce more CBD than "Sativa," and a THC-to-CBD ratio closer to 1:1. The terpenoid profile imparts an acrid or "skunky" aroma.

Small (2007) noted that "Sativa" and "Indica" were "quite inconsistent" with formal nomenclature, because C. sativa subsp. sativa should apply to non-intoxicant plants. Conflating formal and vernacular taxonomy has muddled otherwise excellent studies (e.g., Sawler et al., 2015; Lynch et al, 2015; Belendiuk et al, 2015). It even appears in Nature (Gould, 2015). Please stay alert to the fact that "Sativa" and "Indica" written in quote marks mean different things than C. sativa and C. indica written in italics.

The purpose of this paper is to provide historical context to these debates, beginning with the original protologues of C. sativa and C. indica. To this we add the protologues of several epithets that touch on the vernacular debate: C. ruderalis, C. sativa var. spontanea, C. indica var. kafirstanica, and C. indica var. afghanica. Lastly we review six prominent post-1970 treatments of these taxa, by Schultes, Anderson, Small, de Meijer, Hillig, and Gilmore. Our intent is to compare and contrast these existing taxonomic models, rather than to propose a new model.

Methods

This review utilized three search engines to collect literature (Google Scholar, PubMed, and Web of Science). We followed PRISMA guidelines for systematic reviews, including inclusion and exclusion criteria (details provided upon request by the corresponding author).

The 1CN defines a protologue as everything associated with a taxonomic name at its first valid publication. It includes the taxon's diagnosis or description, synonymy, discussion, illustrations, references, and type specimen (McNeill, 2012). A type specimen is a physical reference point linked to a taxonomic name: a dried plant stored in a herbarium. Type specimens authenticate a taxon's description, but they may not serve as exemplars of a taxon. Characters exhibited by type specimens may results from environmental modifications.

Fifteen herbaria were consulted, designated by herbarium acronyms in Index Herbariorum: B (Berlin), BM (British Museum, London), BPI (Beltsville, MD), CUP (Cornel University), F (Field Museum, Chicago), ECON (Economic botany, Harvard), GH (Gray, Harvard), IND (Bloomington, IN), K (Kew, London), LE ("Leningrad," St. Petersburg), LINN (Linnaeus, London), NY (Bronx, New York), P (Paris), PH (Philadelphia), US (Smithsonian, Washington DC), WIR (Vavilov Institute, St. Petersburg).

Results

The search algorithm identified many potential articles: Google Scholar, 1490 hits; PubMed, 362 hits; Web of Science, 16 hits. Screening revealed the majority of these were irrelevant (details provided upon request by the corresponding author). Our yield was greatly enhanced by screening retrieved articles for supporting citations, and retrieving these antecedent sources. The results of this systematic search are presented in a narrative review, structured from an historical perspective. To maintain narrative flow, fine details in this review are relegated to four Appendices.

Cannabis sativa L. Protologue

C. sativa L. 1753 holds priority under the ICN--the first Cannabis taxon appearing after the starting date of botanical nomenclature. Botanists prior to Species Plantarum also used the binomial, such as Caspar Bauhin and Leonhart Fuchs. The unrecognized author who first coined C. sativa was Ermolao Barbara, in a text published 23 years after his death (Barbara, 1516).

The description of C. sativa by Linnaeus (1753) was exceptionally brief: a generic account of flower parts, applicable to the genus Cannabis. Linnaeus described the seed (Latin: semen) as a nut (nux). Edwards and Vavasseur (1829) first referred to the seed as an achene. We shall refer to the seed as a seed, unless quoting someone else.

Linnaeus listed five facultative synonyms and their five authors. All synonyms and authors cited by Linnaeus came from northern Europe. Linnaeus notably excluded Asian taxa from the C. sativa synonymy. This departs from his earlier taxonomic synopsis of Cannabis, where Linnaeus (1737) synonymized several taxa assigned to psychoactive Asian Cannabis. These Asian taxa appeared in a 1746 draft of Species Plantarum (manuscript at the Linnean Society of London), but they were deleted from the final version.

Linnaeus's herbarium specimens also came from northern Europe. The type specimen, a seeded pistillate plant, is deposited at LINN (Fig. 1). Steam (1974) provided evidence that Linnaeus collected it in Sweden. Its morphology is consistent with a northern European fiber-type landrace. The inflorescences are loose, not dense; subtending floral leaves have a sparse covering of capitate-sessile glandular trichomes; perigonal bracts have a relatively sparse covering of capitate-stalked glandular trichomes. Seeds are large (4.8 x 2.5 mm), oblong in outline, pale green with a fine reticulated pattern, with a short and pointed base with a simple articulation. Other C. sativa specimens collected by Linnaeus (at BM) are consistent with "the old cultivated hemp stock of northern Europe" (Steam, 1974). We provide a full account of Linnaeus's description, synonymy, and references in Appendix 1 a.

Cannabis indica Lam. Protologue

Lamarck (1785) coined C. indica for plants with provenance from India, Southeast Asia, and South Africa. He cited six synonyms and their authors. For a full account of his protologue see Appendix 1 b. Lamarck's description of C. indica differed from his description of C. sativa by eight "very distinct" morphological characters in stalks, branching habitus, leaflets, and flowers. Lamarck also described chemotaxonomic differences: C. indica produced a strong odor, and was psychoactive, "The principal effect of this plant consists of going to the head, disrupting the brain, where it produces a sort of drunkenness that makes one forget one's sorrows, and produces a strong gaiety."

Lamarck's type specimen at P is annotated "Chanvre rapporte de l'Inde par M. Sonnerat." Pierre Sonnerat made extensive botanical collections around Pondicherry. The specimen's unpollinated pistillate ("sinsemilla") morphology is representative of a South Asian landrace. It shows vigorous branching, with shorter internodes than Linnaeus's specimen (Fig. 1). Its inflorescences are somewhat compact; subtending floral leaves have an abundant covering of capitate-sessile glandular trichomes; perigonal bracts express a moderate density of capitate-stalked glandular trichomes. The styles and stigmas are prominent, agglutinated with trichome exudate, and light brown in color.

Historical Bias in Usage of C. sativa and C. indica

Botanists soon rendered subjective decisions regarding Lamarck's concept of a polyspecific genus. Willdenow (1805) reduced C. indica to a synonym C. sativa, rather than a separate variety. He argued that no diagnostic differences existed between them, because both species showed alternate branching (Lamarck erroneously claimed C. indica was unique in this regard). Willdenow ignored Lamarck's seven other morphological differences. He also ignored Lamarck's phytochemical differences, possibly because Linnaeus (1751) rejected chemotaxonomic characters, such as fragrance and taste. Similarly, most British botanists in India cited C. sativa and ignored C. indica.

We find evidence of cultural bias influencing these taxonomic decisions, arising from personality cults surrounding Linnaeus and Lamarck. Today it is difficult to fathom Linnaeus's renown among botanists in the 18th-19th centuries, and the enmity provoked by Lamarck's deviation from Linnaean orthodoxy. See Appendix 2 for attestations. For example, Willdenow was a disciple of Linnaeus, and updated Species Plantarum after Linnaeus died. Willdenow (1805) rejected over half of Lamarck's new taxa (most have been reinstated by modern taxonomists). Early British botanists working in India were tutored by Johann Konig, a student of Linnaeus. William Roxburgh became the most influential member of Konig's "United Bretheren" in India. Roxburgh (1832) wrote, "I perfectly agree with Willdenow in thinking all the varieties, if even such they can be called, centre in one species."

It is expected that the distributions of C. sativa and C. indica (at species or subspecies rank) would occupy separate floristic regions. The distribution of plants that field botanists identified as C. sativa or C. indica in the 18th-19th centuries is presented in Fig. 2. The map shows no hint of endemic distribution, for either C. sativa or C. indica, within any single floristic region. Even allowing for zoochory (animal transport of germplasm, including humans) the distributions of C. sativa and C. indica randomly overlap. The penetration of "C. sativa" deep into Asia is particularly striking.

As field botanists explored Asia and Africa, they applied the names C. sativa or C. indica to plants inconsistent with the protologues of Linnaeus and Lamarck. In many locations, both names were applied, by different botanists. In general, botanists from Scandinavia and Great Britain used "C. sativa." French and Francophone Russian botanists used "C. indica" or coined new taxa, such as such as C. chinensis and C. gigantea. Some botanists deposited herbarium specimens, and our examination of their specimens verified erroneous determinations.

Wild-Type Cannabis

Reports of Cannabis growing in two phases of domestication--wild and cultivated-- trace back to Scythia, now Ukraine, in 440 BC (Herodotus, 2007). We prefer the phrase "wild-type," a term that includes a spectrum of plants. This spectrum was delineated by Small (1984, 2015), ranging from truly wild (i.e., native, indigenous, aboriginal), feral (i.e., weedy, naturalized), ruderal (either wild or weedy), to spontaneous (escapes of cultivated plants). Russian naturalists encountered wild-type Cannabis near present-day Saratov, and debated whether they were truly wild or escapes of cultivated plants (Lepechin, 1774; Pallas, 1793).

Zinger (1898) first described wild-type characteristics (Fig. 3). These included small seed size, a protuberant-and-tapered base with a prominent abscission zone, and a persistent perianth (seed covering). The perianth provides camouflage coloring--a matte surface (rather than a shiny pericarp) with irregular dark spots, called marbling, mottling, or mosaic by various authors. The protuberant base has been described as a horseshoe, circular torus, callus-ring, caruncle, basal constricted zone, or elaiosome.

Two botanists in Saratov, Dmitry Janischevsky and Nikolay Vavilov, studied wildtype Cannabis. Vavilov (1922) coined the taxon C. sativa var. spontanea. His description is brief and limited to wild-type seed morphology. He added a physiological trait: rapid seed disarticulation from the plant, due to a prominent abscission zone. Vavilov described C. sativa var. spontanea in greater detail in subsequent publications. For his full protologue and later descriptions, see Appendix 1c.

Vavilov's lectotype specimen at WIR is illustrated in Fig. 3. The specimen consists of the top 42 cm of what appears to be a tall plant, with internode spacing similar to Linnaeus's type specimen. Leaves have 3-5 leaflets, petioles short, leaflets narrow lanceolate, up to 130 x 10 mm. Inflorescences are loose; subtending floral leaves have a sparse covering of sessile glandular trichomes; perigonal bracts have few capitates-talked glandular trichomes and many cystolith trichomes. Seeds are medium-sized (3.8-4.0 mm long), with reticulate venation between irregular dark marbling, and a weakly protuberant base.

Janischevsky (1924) erected C. ruderalis, plus an alternative taxonomic rank: C. sativa var. ruderalis. "I am inclined to consider it a well marked variety." Janischevsky penned a 13-page protologue (Appendix Id), including a Latin diagnosis and two plates of illustrations (all of seeds). He described a moderately tall plant, usually 0.7-1.1 m but up to 2.1 m, branchier than domesticated plants, with wild-type seed characteristics. Janischevsky's lectotype specimen of C. sativa var. ruderalis was stored at LE (Small & Cronquist, 1976). It may be lost (McPartland, pers. observ., St. Petersburg, 2010). Janischevsky's bibliography is extensive; he cited literature by 22 authors.

Two taxonomic names that represent contaxic entities, based on different type specimens, are facultative synonyms. Vavilov's taxon has priority at the rank of variety, Janischevsky's taxon has priority at the rank of species. Soviet botanists in the 1930s set precedence by choosing C. ruderalis over C. sativa var. spontanea. We find evidence of cultural bias influencing their decisions, during the era of Lysenkoism. See Appendix Id for attestations.

Historical Bias, Part II

Vavilov traveled to Afghanistan in 1924, and encountered all phases of domestication--wild, weedy, and cultivated. He described Afghani farmers growing Cannabis exclusively for gashisha ("a grinded gray-green powder," i.e., sieved hashish). He assigned these plants to C. sativa (Vavilov & Bukinich, 1929), a concept that departed from Linnaeus's protologue of C. sativa as a European fiber-type plant.

Vavilov's error likely derived from Tatiana Serebriakova, his assistant in Russia. Vavilov sent seeds to Serebriakova, and she grew the accessions. Vavilov and Bukinich (1929) presented her data, and then made a statement that seems to quote her, "By all attributes it [Afghani plants] is linked directly with the Central Asian cultivated hemp, not with C. indica, which is distinguished by its small leaves, small fruits, and low height (up to 1 meter)." Serebriakova's concept of C. indica as a diminutive plant with small leaves is faulty--plants from India are relatively tall with large leaflets. Serebriakova and Vavilov likely never saw a specimen of C. indica from India. The herbarium collection at WIR lacks specimens from India (McPartland, pers. observ., St. Petersburg, 2010).

Vavilov discovered feral and wild-type plants in Afghanistan, and coined two new taxa for them. Vavilov (1926) assigned C. sativa f. afghanica to feral plants with obovate leaflets (a shape he said was not seen in European plants), medium height, and profuse branching. The plants "constitute a morphological link between the wild and the cultivated races of hemp." Subsequently he transferred the taxon to C. indica, as C. indica f. afghanica, and mentioned the alternative rank C. indica var. afghanica (Vavilov & Bukinich, 1929). Some botanists argue that afghanica designates a wildtype plant. But Vavilov's descriptions, illustrations, and other evidence indicate that afghanica was an escape of cultivated plants (Appendix le).

Vavilov and Bukinich (1929) coined C. indica var. kafirstanica for wild-type plants, with very small seeds, dark-colored and mottled, with a "horseshoe" (Appendix If). They muddied taxonomic waters by assigning afghanica to a third alternative rank, C. indica var. kafiristanica forma afghanica.

Vavilov (1931) extended the range of C. sativa var. spontanea to Central Asia, where he encountered wild-type plants. However, specimens deposited at WIR and LE show that Vavilov assigned C. sativa var. spontanea to plants that departed from his own protologue of the taxon--they are extremely short (<0.61 m), unbranched, with broad leaflets.

A new cultural bias appeared in the 1970s. Cannabis taxonomy became entangled in the USA legal system, due to perceived threats to society regarding increased Cannabis use. Whether Cannabis is polytypic (one species with many kinds) or polyspecific (more one than one species) became a polarized debate in court cases. The primary adversaries in these legal wrangles were Richard Evans Schultes, a Harvard ethnobotanist, and Ernest Small, a Canadian taxonomist who specialized in Cannabis.

Small, an expert witness on behalf of plaintiffs, argued for a single species, C. sativa. "This arrangement is in harmony with social needs and significance" (Small & Cronquist, 1976). He backed his legal testimony with a lot of data. Small and colleagues conducted cross-breeding experiments, and they assessed many taxonomic characters--morphological, biogeographical, developmental, and phytochemical (cannabinoid content, seed oil chemistry)--summing to 20 publications (Appendix 4).

Small and Cronquist (1976) stayed true to Linnaeus's concept of sativa, Lamarck's concept of indica (albeit as a subspecies), and Vavilov's concept of C. sativa var. spontanea. They treated C. indica f. afghanica as a feral escape of cultivated plants, separate from C. indica var. kafiristanica. They departed from Vavilov's concept of C. indica var. kafiristanica by extending the taxon to wild-type plants with narrow lanceolate leaflets, growing outside of Afghanistan, in India, Nepal, China, South Africa, and Columbia.

Small's taxonomic concept is relatively simple: a two-step hierarchic classification system (Fig. 4). The first step recognizes two subspecies based on THC content in dried female flowering tops (with 0.3% THC as the dividing point). The second step recognizes two varieties within each subspecies, based on their domestication phase. However, analysis of THC/CBD ratios revealed three chemovars. Type I: THC >0.3%, CBD <0.5%; Type II: THC >0.3%, CBD >0.5%; or Type III: THC <0.3%, CBD >0.5%.

Type I chemovars were drug-type plants, mostly with provenance from countries below the 30th parallel (30[degrees] N runs through Morocco, Iran, northern India, and southern China; 30[degrees] S runs through South Africa, South America, and Australia). Type III chemovars were fiber-type plants, mostly with provenance north of 30[degrees]N. Type II chemovars were a mix of daig- and fiber-type plants; Small stated that they may reflect hybridization between Type I and III.

Small's taxonomic concept is cited and accepted by many botanists, and attested on botanical websites (Appendix 4). Nevertheless his model has been criticized for being "not natural at all" and ignoring morphological diversity (De Meijer, 1999), and for methodological flaws (Hillig & Mahlberg, 2004). Small provided "passport data" regarding the provenance of his accessions, and deposited voucher specimens of each accession in several herbaria. Vouchers are critical for authenticating the identification of a taxon; they allow other researchers to retrospectively analyse accessions (Culley, 2013). Several accessions came from botanical gardens, of questionable provenance (e.g., three indica accessions with no measurable THC).

Schultes served an expert witness on behalf of defendants, whose attorneys argued that narcotics laws cited C. sativa, whereas the accused possessed C. indica, a species that was statutorily overlooked and technically legal. Schultes argued in favor of three Cannabis species by reversing his opinion on Cannabis, which he initially considered a monotypic genus (Schultes, 1970). Subsequently he recognized C. sativa, C. indica, and C. ruderalis, and summed his research in a single paper (Schultes et al., 1974). He changed his opinion based on analyses of herbarium specimens, a survey of the Mississippi Cannabis plantation, and "preliminary field work" in Afghanistan.

A former student explained that Schultes's "intense dedication" to libertarian beliefs led him to employ this "obscure taxonomic argument" (Davis, 1996). "In truth, the evidence for Schultes's position was somewhat dubious." Schultes et al. (1974) departed from the concepts of Lamarck, Vavilov, and Janischevsky:

* C. indica becomes narrowly typified to plants Schultes saw in Afghanistan, with broad, oblanceolate leaflets, densely branched, more or less conical in shape, and very short (< 1.3 m). Designating these plants as C. indica is faulty; Lamarck was entirely unfamiliar with Afghani Cannabis. Lamarck's protologue of C. indica describes plants that are relatively tall, laxly branched, with narrow leaflets.

* By assigning cultivated Afghani plants to C. indica, Schultes departs from Vavilov's concept of cultivated Afghani plants as C. sativa.

* Schultes eschews Vavilov's spontanea in favor of Janischevsky's ruderalis. He departs from Janischevsky's concept of C, ruderalis by applying the taxon to extremely short (<0.61 m), unbranched plants with broad leaflets from Central Asia, instead of Janischevsky's relatively tall, laxly branched plants with narrow leaflets from southeastern Europe.

Schultes's concepts were embraced by two other defense witnesses, William Emboden and Loran Anderson. Emboden (1972) originally considered Cannabis a monotypic genus. Emboden (1974) reversed his opinion. He recognized C. sativa (specimens from Afghanistan, Russia, Kansas), C. indica (specimens from Afghanistan, Turkey, India), and C. ruderalis (a specimen from Russia).

Anderson (1980) typified C. indica with plants Schultes collected in Afghanistan. He assigned C. sativa to plants consistent with Lamarck's C. indica--relatively tall, laxly branched, narrow leaflets, with provenance from India. His concept of C. ruderalis was consistent with Schultes, not Janischevsky. Anderson illustrated these concepts in a line drawing (Fig. 5) This illustration has become pervasive on the web as the poster child of vernacular nomenclature.

The Rise of Vernacular Taxonomy

Cannabis germplasm from Afghanistan was smuggled into the USA by the early 1970s. Differences were readily apparent between Afghani plants and drug plants previously grown in the USA (with provenance from below 30[degrees] N, e.g., Mexico, Columbia, Thailand). Stevens (1975) illustrated morphological differences between Thai and "Afghanistani" plants. Frank and Rosenthal (1978) explained Schultes's three-species concept, and conflated it with Small's three-chemotype concept.

After the publication of Anderson's line drawing (Fig. 5), Clarke (1981) referred to plants from Afghanistan "as type examples for Cannabis indica." He noted the unique smell of Afghani plants, an acrid odor rather than a sweet fragrance. Clarke (1987) first described the unique organoleptic properties of Afghani plants, a "slow flat dreary high."

Cherniak (1982) applied the name "Cannabis indica" to plants from Afghanistan. Their morphology, odor, and potency differed from "Cannabis sativa" strains. He assigned "Cannabis sativa" to plants of South Asian heritage (Nepal, Burma, Thailand), and their descendants in Columbia, Jamaica, and Mexico. However, Cherniak also categorized plants from India as "Cannabis indica." The earliest consistent use of "Sativa" and "Indica" we could find was in a Dutch seed catalog (Watson, 1985).

Schoenmakers (1986) collected "Ruderalis" germplasm near the Hungary-Ukraine border. His photos of "Ruderalis" show plants with strong apical dominance and little branching. These traits are consistent with a spontaneous escape of cultivated hemp, and depart from concepts by Vavilov and Janischevsky. Alternatively, Frank (1988) said that U.S. marijuana growers assigned "Ruderalis" to plants with "wide indica-like leaf blades, and these might be hybrids." In today's vernacular taxonomy, "Ruderalis" is applied to an increasingly protean assortment of plants. They exhibit one to three characteristics: CBD s THC, wild-type morphology, or early flowering (sometimes called "autoflowering," i.e., day-neutral, flowering not induced by light cycle).

Within "Sativa," "Indica," and "Ruderalis," plant breeders have designated "strain" names. Watson (1985) coined several well-known strain names, such as "Original Haze" and "Skunk #1". Cannabis breeders equate "strains" with "cultivare," which flouts another code, the International Code of Nomenclature for Cultivated Plants (ICNCP. Brickell, 2009). The ICNCP has rules for designating cultivare, such as valid publication, typification ("Nomenclatural Standard"), and priority.

Small (2015) pointed out that strains are conceptually identical to cultivare, but almost no Cannabis strains have met ICNCP requirements for cultivar recognition. Seedfinder (2015) listed 6510 strain names. Doyle (2007) referred to these names as ganjanyms. We elaborate upon this controversy in Appendix 4.

Since the courtroom days of Schultes and Small, other botanists have addressed C. sativa, C. indica, "Sativa," and "Indica." Google Scholar computes citation metrics for authors and their publications. Taxonomic publications garnering the greatest number of citations are by Etienne de Meijer, Karl Hillig, and Simon Gilmore.

De Meijer and colleagues analyzed cannabinoid profiles, morphological characters, developmental traits, host-parasite characters, inheritance of chemical phenotypes and SCAR markers, and sequence heterogeneity in cannabinoid synthase genes--summing to 11 publications (Appendix 4). De Meijer and van Soest (1992) introduced vernacular taxonomy to peer-reviewed literature: "Indica" referred to plants with broad leaflets, compact habit, and early maturation, typified by plants from Afghanistan. "Sativa" referred to plants with narrow leaflets, slender and tall habit, and late maturation, typified by plants from India and their descendants in Thailand, South- and East Africa, Colombia, and Mexico.

De Meijer (1999) argued for a single species, C. sativa, noting a lack of breeding barriers and morphological discontinuities within the genus. He subdivided the species into populations, using criteria from Schultes and Anderson. He disregarded priority by naming C. sativa var. spontanea a synonym of C. ruderalis. De Meijer considered cultivated and ruderal forms as extremes along a gradient, so he did not recognize wildtype plants as a separate taxon (de Meijer, pers. commun., 2010). De Meijer provided passport data regarding his accessions, but did not deposit voucher specimens in a herbarium. His model has been criticized for methodological flaws (Hillig & Mahlberg, 2004), and a faulty inheritance model (Weiblen et al., 2015).

Hillig and colleagues analyzed genetic (allozyme) variation, cannabinoid profiles, terpenoid profiles, morphological characters, developmental traits, and host-parasite characters--summing to ten publications (Appendix 4). Hillig sidestepped vernacular nomenclature. He applied the name "narrow-leaflet drug (NLD) biotype" to plants corresponding to "Sativa," and applied the name "wide-leaflet drug (WLD) biotype" to plants corresponding to "Indica." Hillig's use of NLD/WLD is reminiscent of Linnaeus's use of $ and <$ symbols to sort the confusing gender-based names applied by earlier botanists.

Hillig provided passport data and voucher specimens. He made efforts to identify and exclude hybrids, such as NDL x WLD drug crosses, whose recent breeding histories are documented (e.g., De Meijer, 1999). He analyzed landraces, rather than hybrid "strains," (see example at end of Appendix 4) to enhance phylogenetic distinctions. Although de Meijer (pers. commun., 2010) derides the exclusion of hybrids as "cherry-picking," it is a standard procedure (e.g., Kaplan & Fehrer, 2004). New software for inferring population structure makes it easier to identify and exclude hybrids (e.g., Cornille et al., 2013).

Hillig (2004, 2005) recognized two species, C. sativa and C. indica. The first species segregated into two biotypes--a domesticated phase that corresponded with Linnaeus's sativa, and a wild-type phase that corresponded with Vavilov's spontanea. He segregated C. indica into four biotypes. The NLD biotype corresponded with Lamarck's indica. The WLD biotype corresponded with Vavilov's afghanica. The "C. indica feral biotype" referred to wild-type plants from India and Nepal--accessions assigned to kafiristanica by Small and Cronquist (1976). The "C. indica hemp biotype" referred to fiber-type plants from East Asia. Hillig noted that some nineteenth century botanists segregated Chinese hemp from European C. sativa, reflecting their putative domestication from different gene pools. He traced the nomenclature to C. chinensis Delile, 1849, although this is a homonym of C. chinensis Fischer, 1810 (Appendix 3).

Hillig also proposed a third species, C. ruderalis. His concept of C. ruderalis as Central Asian in origin corresponded with the concepts of Schultes and Anderson, rather than Janischevsky. De Meijer (2014) criticized Hillig's model for an overreliance on characters subjected to human selection, such as cannabinoid profiles, although Hillig initially based his model on genetic data. Hillig's nomenclature has gained traction (e.g., McPartland & Guy, 2014; Russo, 2007; Lynch et al., 2015). Clarke and Merlin (2013) objected to biotype names based on leaflet shape. They erected a new biotype nomenclature, for example substituting Hillig's "wide-leaflet drug" with their "broad leaf drug" biotype. Botanically, "leaflet" is more accurate than "leaf."

Gilmore and colleagues conducted genetic studies, summing to six publications (Appendix 4). Gilmore et al. (2007) sequenced five polymorphic loci (cpDNA and mtDNA) from 76 CPRO accessions. Parsimony identified six haplogroups, which nested into three clades: Clade A comprised mostly European fiber plants. Clade B comprised a mix of Eurasian fiber plants, Central Asian drug plants, and hybrids. Clade C comprised drug plants from South Asia (India, Nepal) and their putative descendants. Gilmore noted that clade C corresponded with "drug-breeders taxon Sativa."

Some authors have tried to reconcile "Sativa" and "Indica" with formal C. sativa and C. indica. McPartland et al. (2000) noted that Afghani plants were mislabelled "Indica." They reassigned "Indica" to Vavilov's taxon, at species rank (C. afghanica) or varietal rank (C. sativa var. afghanica). McPartland and Guy (2014) and McPartland (2014) proposed reconciling vernacular and scientific nomenclature: "Sativa" is really indica, and "Indica" is actually afghanica, and "Ruderalis" is usually sativa.

The initial reaction to this proposition by recreational users was negative. An editorial in High Times characterized the reconciled nomenclature as "undoubtedly a little kooky" (Sirius, 2015). Researchers, however, are starting to take it on board (e.g., Henry, 2015). Clarke and Merlin (2016) erected a nearly identical reconciliation, without citing precedent publications. Two table headings in their respective taxonomic tables are exampled:

* Indica--Wrongly called "sativa" (Clarke & Merlin, 2016)

* Indica (formerly "Sativa") (McPartland. 2014)

Rather than reconciling nomenclature, some authors call for a new approach. Arno Hazekamp and colleagues analyzed cannabinoid and terpenoid profiles in hundreds of herb samples obtained from Dutch coffeeshops and other sources. Their methods segregated "Hemp," "Sativa," and "Indica." But they propose jettisoning all vernacular names in favor of a metabolomics approach, "from cultivar to chemovar" (Hazekamp & Fischedick, 2012; Hazekamp et al., 2016).

Other taxonomic projects have analyzed "Sativa" and "Indica" herb samples, rather than C. sativa and C. indica plants cultivated in a common garden experiment. Elzinga et al. (2015) measured THC and CBD content in 35 samples obtained from "chemotypical medicinal cannabis dispensaries." They assigned strains to "Indica," "Sativa," or "Hybrid" based on reports by the Leafly website. Their analysis "does not support the classification between indica and sativa as it is commonly presented."

Sawler et al. (2015) genotyped 43 fiber-type cultivars and 81 drug-type strains. Drug-type strains were classified along a gradient of ancestry (percent "Sativa" vs. percent "Indica") reported in online strain databases. Population stratification using SNP analysis with PLINK segregated clusters of fiber-type and drug-type samples, whereas clusters of "Sativa" and "Indica" overlapped. They concluded that "Sativa" and "Indica," as well as strain names, did not reflect a meaningful genetic identity.

Lynch et al. (2015) conducted a genotype-chemotype study with 195 samples obtained from medical dispensaries, breeders, or "by donation." Haplotypes based on SNP data were analyzed with FLOCK. This algorithm identifies the optimal number of clusters (K) to divide a population, and their data optimized at K = 3. They characterized the three groups as "broad leaflet drug" (e.g., "Afghan Kush," "Chemdawg"), "narrow leaflet drug" (e.g., "Durban Poison," "Easy Sativa"), and a polyphyletic "hemp" group (e.g., 'Finola,' "AC/DC," Chinese hemp, Dagestan plants). They obtained THC/CBD data for 54 of the 195 samples via the Strain Fingerprint[TM] database, developed by Steep Hill Labs. They presented histograms of mean THC% and CBD%, from which cannabinoid ratios can be estimated: BLD: 16.5/0.2 = 82.5, NLD: 14.2/ 2.2 = 6.45. Thus the latest THC/CBD ratios of twenty-first century ganjanyms show a stunning reversal compared to their corresponding 1970s--1990s landraces. See McPartland (2017) for an elaboration of this phenomenon.

Discussion

Considering the controversy over Cannabis taxonomy, it seems surprising that no one has yet presented full protologues of C. sativa and C. indica for comparison. The protologues by Linnaeus and Lamarck show taxonomic acumen for their time. We cannot know why Linnaeus omitted Asian material from the C. sativa protologue, but in retrospect it was a good decision. Lamarck chose taxonomic characters that modern botanists still use to demarcate subpopulations within the genus.

Linnaeus harbored a "Eurocentric bias" in taxonomy and nomenclature, and taxonomists following him showed "secret conservative sympathies" (Walters, 1986). We see this in the use of C. sativa and C. indica by 18th-19th century field botanists, which showed no bioregional endemicity (Fig. 2). Linnaeus's followers applied the name C. sativa to plants in Asia, whereas botanists unconnected to Linnaeus used C. indica or coined new taxa (Appendix 3). C. sativa became a metonym rather than a taxon. Various types of socio-economic biases are known to skew floristic distribution maps (Yang et al., 2014). Understanding patterns of Cannabis biogeography requires improvements in systematics, as well as hermeneutics (texual criticisms). We also see cultural bias in Soviet botanists's use of C. ruderalis during the Lysenko era, and judicial concerns in the 1970s skewed concepts of Cannabis as a monospecific versus polytypic genus.

We return to three issues in the first paragraph of our introduction: Taxonomists have circumscribed Cannabis populations using morphology, chemotaxonomy, and genetics. These characters have not provided robust taxonomic boundaries in recent studies. We attribute this to the inclusion of recently hybridized accessions, which makes it difficult to detect taxonomic dichotomies. Hillig did his best to exclude hybrids from analysis, which enabled him to differentiate WLD and NLD populations within C. indica.

Hybridization threatens Cannabis biodiversity, which has become endangered by widespread crossbreeding over the past 40 years. Wiegand (1935) first described extinction through introgressive hybridization. Introgression refers to the infiltration of genes between taxa through the bridge of F1 hybrids. Fertile offspring from these crosses may display hybrid vigor (enhanced fitness), and replace one or both parental populations (Ellstrand, 2003). Nearly 30 years ago, unhybridized plants of Indian heritage and Afghani landraces had already become difficult to obtain (Clarke, 1987). Small (2017) agrees that hybridization has largely obliterated population differences, "especially between the two kinds of fiber forms and between the two kinds of marijuana forms."

The issue of taxonomic rank continues to bedevil Cannabis taxonomy. Do C. sativa and C. indica segregate at the rank of species, subspecies, or varieties? Gilmore et al. (2007) found little sequence variation in Cannabis (approximately 1 polymorphism per 1 kb sequenced cpDNA), which suggested their haplotypes segregated at a rank below that of species. McPartland and Guy (2014) used similar loci (rbcL, matK, trnH-psbA, trnL-trnF, ITS) to measure divergence between plant populations. The mean divergence between C. sativa and C. indica equaled 0.41%. In comparison, a mean divergence of 0.43% existed between five pairs of plants considered different varieties (e.g., Camellia sinensis var. sinensis and C. sinensis var assamica). A mean divergence of 3.0% separated five pairs of plants considered different species (e.g., Humulus lupulus and H. japonicus).

Sawler et al. (2015) calculated the fixation index (FST) between groups. FST values range from 0 to 1; a zero value indicates the groups freely interbreed; a 1 value indicates the groups are completely isolated from one another. They calculated a FST of 0.156 between fiber- and drug-type groups. This is similar to the degree of genetic differentiation between human populations in Europe and East Asia. Lynch et al. (2015) calculated a FST value of 0.099 between fiber- and drug-type groups, and a FST of 0.036 between WLDs and NLDs.

The third issue--assigning names--is strictly governed by rules of nomenclature in the ICN and ICNCP. However, vernacular "Sativa," "Indica," and "Ruderalis" threaten to subsume formal ICN nomenclature. Many authors have derided the inaccuracy of vernacular taxonomy (e.g., McPartland et al, 2000; Small, 2007; Hazekamp & Fischedick, 2012; Russo, 2016; Clarke & Merlin, 2016).

In conclusion, this review traces the taxonomic histories of C. sativa and C. indica, beginning with protologues by Linnaeus and Lamarck. Disregard of these protologues and taxonomic bias by 18th-19th century botanists impacted upon reports of Cannabis biodiversity and distribution. Further disregard by twentieth century botanists laid the groundwork for "Sativa," "Indica," and "Ruderalis" concepts. These names do not align with formal botanical nomenclature, but they do represent population segregates that are threatened by extinction through introgressive hybridization. Even "the old cultivated hemp stock of northern Europe" (Stearn, 1974) is threatened by hybridization. Perhaps the first step in their preservation is taxonomic recognition, a subject for future publications.

DOI 10.1007/s12229-017-9187-0

Acknowledgements We thank Karl Hillig. Patricia Pruitt. and Ernest Small for reviews of the manuscript.

Literature Cited

Anderson LC. 1980. Leaf variation among Cannabis species from a controlled garden. Harvard University Botanical Museum Leaflets 28(1): 61-69.

Barbaro, E, ed. (Dioscorides P). 1516. In hoc volumin haec continentur, loannis Baptistae Egnatii in Dioscoridem ab Hermolao Barbaro tralatum annotamenta. Aloisius & Franciscus Barbari, Venice.

Belendiuk KA, Babson KA, Vandrey R, Bonn-Miller MO. 2015. Cannabis species and cannabinoid concentration preference among sleep-disturbed medicinal cannabis users. Addictive Behaviors 50: 178-181.

Black H, Capler R. 2003. Operational standards for the distribution of medicinal cannabis. British Columbia compassion Club Society, Vancouver, BC.

Brickell CD, ed. 2009. International code of nomenclature for cultivated plants, Eighth Edition. International Society for Horticultural Sciences, Leuven, Belgium.

Cherniak L. 1982. The great books of cannabis. Vol. I: Book II. Cherniak/Damele Publishing Co., Oakland CA.

Clarke RC. 1981. Marijuana Botany. And/Or Press, Berkeley, CA.

Clarke, RC. 1987. Cannabis evolution. MS thesis, Indiana University, Bloomington, IN.

Clarke RC, Merlin MD. 2013. Cannabis evolution and ethnobotany. University of California Press, Berkeley.

Clarke RC, Merlin MD. 2016. Cannabis taxonomy: The 'sativa' vs. 'indica' debate. HerbalGram 110: 44-49.

Cornille A, Gladieux P, Giraud T. 2013. Crop-to-wild gene flow and spatial genetic structure in the closest wild relatives of the cultivated apple. Evolutionary Applications 6: 737-748.

Corral VL. 2001. Differential effects of medical marijuana based on strain and route of administration: A three-year observational study. Journal of Cannabis Therapeutics 1(3/4): 43-59.

Culley TM. 2013. Why vouchers matter in botanical research. Applications in Plant Sciences 1(11): Apps. 1300076.

Darwin CR. 1859. On the origin of species. John Murray, London.

Davis W. 1996. One river Simon & Schuster, New York.

De Meijer EPM. 1999. "Cannabis germplasm resources," pp. 133-151 in. Ranalli P, ed. Advances in Hemp Research. Haworth Press New York.

De Meijer EPM. 2014. "The chemical phyotypes (chemotypes) of Cannabis," pp. 89-110 in Pertwee RG, ed. Handbook of cannabis. Oxford University Press, Oxford, UK.

De Meijer EPM, van Soest LJM. 1992. The CPRS Cannabis germplasm collection. Euphytica 62: 201-211.

Doyle R. 2007. The transgenic involution," pp. 70-82 in Kac E, ed. Signs of life. Massachusetts Insititute of Technology, Cambridge, MA.

Edwards HM, Vavasseur P (Togno J. Durand E, trans). 1829. A manual of materia medica and pharmacy. Carey Lea & Carey, Philadelphia.

Ellstrand NC. 2003. Dangerous liaisons? When cultivated plants mate with their wild relatives. Johns Hopkins University Press, Baltimore.

Elzinga S, Fishchedick J, Podkolinski R, Raber JC (2015) Cannabinoids and terpenes as chemotaxonomic markers in cannabis. Natural Products Chemistry & Research 3:4.

Emboden WA. 1972. "Ritual use of Cannabis sativa L.: A historical-ethnographic survey," pp 214-236 in. Furst P, ed. Flesh of the gods. Praeger Publ., NY.

Emboden WA. 1974. Cannabis--A polytypic genus. Economic Botany 28: 304-310.

Frank M. 1988. Marijuana grower's insider's guide. Red Eye Press, Los Angeles, CA.

Frank M, Rosenthal E. 1978. Marijuana grower's guide. And/Or Press, Berkeley.

Gilmore S, Peakall R, Robertson J. 2007. Organelle DNA haplotypes reflect crop-use characteristics and geographie origins of Cannabis sativa. Forensic Science International 172: 179-190.

Gould J. 2015. The cannabis crop. Nature 525: S2-S3.

Hazekamp A, Fischedick JT. 2012. Cannabis--From cultivar to chemovar. Drug Testing and Analysis 4: 660-667.

Hazekamp A, Tejkalova K, Papadimitriou S. 2016. Cannabis: From cultivar to chemovar II--A metabolomics approach to Cannabis classification. Cannabis and Cannabinoid Research 1(1): 202-215.

Henry. P. 2015. Genome-wide analyses reveal clustering in cannabis cultivars: The ancient domestication trilogy of a panacea. Peer J PrePrints https://pceij.com/preprints/1553.pdf.

Herodotus (Strassler RB, ed., Purvis AL, trans). 2007. The landmark Herodotus: The histories. Pantheon Books, NY.

Hillig KW. 2004. A chemotaxonomic analysis of terpenoid variation in Cannabis. Biochemical Systematics and Ecology 32: 875-891.

Hillig KW. 2005. Genetic evidence for speciation in Cannabis (Cannabaceae). Genetic Resources and Crop Evolution 52: 161 180.

Hillig KW, Mahlberg PG. 2004. A chemotaxonomic analysis of cannabinoid variation in Cannabis (Cannabaceae). American Journal of Botany 91(6): 966-975.

Janischevsky DE. 1924. [phrase omitted] (A form of cannabis in wild areas of south-eastern Russia). [phrase omitted] (Scientific Notes of the Saratov State University named after N. G. Chernyshevsky) 2(2): 3-17.

Kaplan Z, Fehrer J. 2004. Evidence for the hybrid origin of Potamogeton x cooperi (Potamogetonaccae): Traditional morphology-based taxonomy and molecular techniques in concert. Folia Geobotanica 39: 431-453.

Lamarck JB. 1785. Encyclopedie Methodique 1(2): 695. Panckoucke, Paris.

Lepechin II (Hare CH, trans). 1774. Tagebuch der Reise durch verschiedene Provinzen des Russischen Reiches, Erster Theil. Richterischen Buchhandlung, Altenburg.

Linnaeus C. 1737. Hortas Cliffortianus. Publisher not identified (George Clifford?), Amsterdam.

Linnaeus C. 1751. Philosophia Botanica. Kiesewetter, Stockholm.

Linnaeus C. 1753. Species Plantaram 2: 1057. Laurentii Salvii, Stockholm.

Lynch RC, Vergara D, Tittes S, White K, Schwartz CJ, Gibbs MJ, Ruthenburg TC, deCesare K, Land DP, Kane NC. 2015. Genomic and chemical diversity in cannabis. BioRxiv doi: 10.1101/034314.

McNeill J, chair. 2012. International code of nomenclature for algae, fungi, and plants (Melbourne code). Koeltz Scientific Books, Konigstein. Germany.

McPartland. JM. 2014. Corrected vernacular nomenclature: Indica, afghanica, sativa. O'Shaughnessy's Autumn 2014, p. 1.

McPartland JM. 2017. "Cannabis sativa and Cannabis indica versus "Sativa" and "Indica"", in Chandra S, Lata H. ElSohly, MA, cds. Cannabis Sativa: Botany and biotechnology. Springer International Publishing, Cham, Switzerland.

McPartland. JM, Guy. GW. 2014. A question of rank: Using DNA barcodes to classify Cannabis sativa and Cannabis indica. Proceedings of the 24th annual symposium on the Cannabinoids. International Cannabinoid Research Society, Research Triangle Park, NC.

McPartland JM, Clarke RC, Watson DP. 2000. Hemp diseases and pests--management and biological control. CABI Publishing, Wallingford, UK.

Pallas PS. 1793. Voyages de M. P. S. Pallas, en differentes provinces de l'empire de Russie. Tome Cinquieme. Maradan. Paris.

Roxburgh W (Carey W. ed.). 1832. Flora Indica; or, descriptions of Indian plants, volume 3. W. Thackery, Serampore and Calcutta.

Russo EB. 2007. History of Cannabis and its preparations in saga, science, and sobriquet. Chemistry & Biodiversity 4: 1614-1648.

Russo EB. 2016. The Cannabis sativa versus Cannabis indica debate: An interview with Ethan Russo, MD. Cannabis and Cannabinoid Research 1(1): 44-46.

Sawler J, Stout JM, Gardner KM, Hudson D, Vidmar J, Butler L, Page JE, Myles S. 2015. The genetic structure of marijuana and hemp. PLoS One 10(8): e0133292.

Schoenmakers N. 1986. The seed Bank 1986/1987 Catalogue. Drukkerij Dukenburg Printers, Nijmegen, The Netherlands.

Schultes RE. 1970. "Random thoughts and queries on the botany of Cannabis," pp. 11-38 in. Joyce CRB, Curry SH, eds. The botany and chemistry of cannabis. J.& A. Churchill, London.

Schultes RE, Klein WM, Plowman T, Lockwood TE. 1974. Cannabis: An example of taxonomic neglect. Harvard University Botanical Museum Leaflets 23: 337-367.

Seedfinder. 2015. Sccdfindcr online database. Available at: http://cn.sccdfinder.eu/.

Sirius, J. 2015. A scientific approach: Redefining weed. High Times Februrary 18, 2015.

Small E. 1972. Infertility and chromosomal uniformity in Cannabis. Canadian Journal of Botany 50: 1947-1949.

Small E. 1984. "Hybridization in the domesticated-weed-wild complex," pp. 195-210 in Grant WF, ed. Plant biosystematics. Academic Press, NY.

Small E. 2007. Cannabis as a source of medicinais, nutraceuticals, and functional foods. Advances in Medicinal Plant Research 2007: 1-39.

Small E. 2015. Evolution and classification of Cannabis Sativa (marijuana, hemp) in relation to human utilization. Botanical Review 81: 189-294.

Small E. 2017. Cannabis: a complete guide. CRC Press. Boca Raton. FL.

Small E, Cronquist A. 1976. A practical and natural taxonomy for Cannabis. Taxon 25(4): 405-435.

Stearn WT. 1974. Typification of Cannabis sativa L. Harvard University Botanical Museum Leaflets 23(9): 325-336.

Stevens M. 1975. How to grow marijuana indoors under lights, 3rd Ed. Sun Magic, Seattle.

Takhtajan AL (Crovello TJ transi, Cronquist A, ed). 1986. Floristic regions of the world. University of California Press, Berkeley.

Vavilov NI. 1922. Field crops of the southeast. [phrase omitted] (Bulletin of Applied Botany, Genetics, and Plant Breeding) 13 (Suppl. 23): 147-148.

Vavilov NI. 1926. The origin of the cultivation of "primary" crops, in particular cultivated hemp. [phrase omitted] 16(2): 221-233.

Vavilov NI. 1931. The role of Central Asia in the origin of cultivated plants. [phrase omitted] 26(3): 1-44.

Vavilov, NI, Bukinich, DD. 1929. Konopli. [phrase omitted] 33 (Suppl.): 380-382. Supplement published separately as: [phrase omitted] [Agricultural Afghanistan]. Izdanija Vsesojuznyj Instituia Prikladnoj Botaniki i Novych Kul'tur pri SNK. SSSR. i Gosudarstvcnnogo Instituta Opytnoj Agronomii NKZ, Leningrad.

Von Arx J A. 1987. Plant pathogenic fungi. Nova Hcdwigia Bcihcftc 87: 1-288.

Walters SM. 1986. The name of the rose. New Phytologist 104: 527-546.

Watson DP. 1985. Cultivator's choice catalog #4. Self-published. Amsterdam. Holland.

Weiblen GD, Wenger JP, Craft KJ, ElSohly MA, Mehmedic Z, Treiber EL, Marks MD. 2015. Gene duplication and divergence affecting drug content in Cannabis sativa. New Phytologist 208: 1241-1250.

Wiegand KM. 1935. A taxonomist's experience with hybrids in the wild. Science 81: 161-166.

Willdenow, CL. 1805. Caroli Linne Species Plantarum IV (2): 768-769. G. C. Nauk. Berlin.

Yang WJ, Ma KP, Kreft H. 2014. Environmental and socio-economic factors shaping the geography of floristic collections in China. Global Ecology and Biogeography 23: 1284-1292.

Zinger, N. 1898. Beitrage zur Kenntnis der weiblichen Bluthen und Infloresccnzen bei Cannabineen. Flora Oder Allgemeine Botanische Zeitung 85: 189-253.

Appendix 1 literature cited

Acosta C. 1578. Tractado de las drogas y medicinas de las Indias Orientales. Martin de Victoria. Burgos. Spain.

Adamovic L. 1907. Die Pflanzengeographische Stellimg und Gliederung der Balkanhalbinsel. Kaiserlich Koniglichen Hof- und Staatsdruckcrel, Vienna.

Alpini P. 1591. De Medicina Aegyptiorum. Francesco dei Franccschi. Venice.

Amman J. 1739. Stirpium rariorum in Imperio Rutheno sponte provenientium icones et descriptiones. Academia Scientiarum, St. Petersburg.

Anderson LC. 1980. Leaf variation among Cannabis species from a controlled garden. Harvard University Botanical Museum Leaflets 28(1): 61-69.

Ascherson P, Graebner P, eds. 1911. Cannabis. Synopsis der Mitteleuropaischen Flora 4: 598-601.

Becker A. 1858. Verzeichniss der um Sarepta wildwachs Pflanzcn. Bulletin de la Societe Imperiale des Naturalistes de Moscou 31(1): 1-85.

Bock. H (also Boch or Tragus) 1539. New Kreuter Buch. Wendel Rihel, Strassburg.

Bocsa I, Karus M. 1997. Der Hanfanbau: Botanik, Sorten, Anbau und Ernte. C.F. Millier, Hcildelberg.

Bogdan V.S. 1908. [phrase omitted], Tom I (Vegetation of the Turgayan-Uralian resettlement area, Vol. I). Tipo-lit. Dworzec. Orenburg.

Boissier E. 1879. Cannabis. Flora Orientalis sive enumeratio plantarum 4: 1152-1153.

Breistroffer M. 1948. Sur les dates exactes de parution dc quelques livres botaniques publics par D. Villars et dc Lamarck. Proces-verbaux mensuels de la Societe dauphinoise d'Ethnologie et d'Archeologie 24: 182-184.

Britton NL. 1889. Catalogue of plants found in New Jersey. John Murphy. Trenton NJ.

Brownjohn PW, Ashton JC. 2012. "Cannabinoid and neuropathic pain," pp. 79-102 in Udeagha CP, ed. Neuropathic pain. InTech, Rijeka, Croatia.

Burman J. 1737. Du Thesaurus Zevlanicus. Janssonio-Waesbergios and Salomon Schoutcn, Amsterdam.

Cervantes J. 2006. Marijuana horticulture: the indoor/outdoor medical grower's bible. Van Patten Publishing, Vancouver WA.

Chardin J. 1686. Journal du voyage du chevalier Chardin en Perse et aux Indes Orientales. Moses Pitt. London.

Christison A. 1850. On Cannabis indica, indian hemp. Transactions and Proceedings of the Botanical Society of Edinburgh 4: 59-69.

Chrtek J. 1981. Poznamky k rozsireni druhu Cannabis ruderalis v Cechach a na Morave. Casopis Narodniho musea. Oddil prirodovedny 150 (1-2): 21-24.

Chu, S. 1959. Cannabis. Dongbei caoben zhiwu zhi [Flora Plantarum Herbacearum Chinae Boreali-Orientalis] 2: 2-3.

Clarke RC, Merlin MD. 2013. Cannabis evolution and ethnobotany. University of California Press. Berkeley.

Clarke RC, Watson DP. 2002. "Botany of natural Cannabis medicines." pp. 3-14 in. Grotenhermen F. Russo EB, eds., Cannabis and Cannabinoids. Haworth Press, Binghamton, NY.

Claus KE. 1838. "Ueber die Flora und Fauna der kaspischen Steppe," pp. 216-246 in Gobel FT. ed. Reise in die Steppen des sudlichen Russlands, Zweiter Theil. C.A. Kluge. Dorpat.

Czernajew. VM. 1859. Conspectus Plantarum circa Charcoviam et in Ucrania sponte crescentium et vulgo cultarum, pg 56. Published by the author, Kharkov.

da Orta. G. 1563. Coloquios dos simples e drogas he comas medicinais da India. Ioannes Goa, Goa. [translation in: Mills JH. 2003. Cannabis Britannica. Oxford University Press, Oxford. UK],

de Candolle AP. 1855. Geographie Botanique. Victor Masson, Paris.

de Candolle, AP. 1869. Prodromus systematis naturalis regni vegetabilis 16 (1): 30-31.

de Gouvea A. 1606. Jornada do Arcebispo Aleteo de Menezes quando foy as Seira do Malaubar. Diogo Gomez Loureyro, impressor da Universidade, Coimbra, Portugal,

de L'Ecluse, C. 1567. Aromatum, et simplicium aliquot medicamentorum apud Indos nascentium historia ante biennium quidem Lusitanica lingua per dialogos conscripta D. Garcia ab Horto. Ex Officina Christophori Plantini, Antwerp.

Dimo NA, Keller BA. 1907. [phrase omitted] (In the semidesert regions). Saratov Provincial District Council, Saratov.

Doebley JF, Gaul BS, Smith BD. 2006. The molecular genetics of crop domestication. Cell 127: 1309-1321. dos Santos J. 1609. Ethiopia Oriental. Manoel de Lyra, Evora, Portugal.

Drury, R (Defoe D, ed.). 1729. Madagascar: or, Robert Drury's journal: during fifteen years' captivity on that island. W. Meadows, London.

Dukerley I. 1866. Note sur les differences que presente avec le chanvre ordinaire la variete de cette espece connue en Algerie sous les noms de kif et de tekrouri. Bulletin de la Societe Botanique de France 13: 401-406.

Emboden WA. 1974. Cannabis--a polytypic genus. Economic Botany 28: 304-310.

Erndtel, CH. 1730. Warsavia physice illustrata, sive de aere, aqvis, locis et incolis warsaviae, eorundemque moribus et morbis tractatus: cui annexum est. viridarium, vel catalogus plantarum circa warsaviam nascentium. Joh. Christoph. Zimmermanni. Dresden.

Falck, JP (Georgi JG, ed). 1786. Beytrage zur Topographischen Kenntniss des Russischen Reichs, Zwenter Band. Akademic der wissenschaften, St. Petersburg.

de Flacourt, E. 1661. Histoire de la grande isle de Madagascar. Nicolas Oudot, Paris.

Frank M. 1988. Marijuana grower's insider's guide. Red Eye Press, Los Angeles, CA.

Fryer J. 1698. A New account of East-India and Persia, in eight letters, being nine years travels, begun 1672 and finished 1681. R. Chiswell, London.

Fuchs, L. 1542. De Historia Stirpium Commentarii Insignes 2: 392-393.

Hanelt P, ed. 2001. Mansfeld's Encyclopedia of Agricultural and Horticultural Crops, Vol. 1. Springer-Verlag, Berlin.

Henry P. 2015. Genome-wide analyses reveal clustering in Cannabis cultivars: the ancient trilogy of a panacea. PeerJPrePrints https://peeij.com/prcprints/1553vl.pdf

Heuffel J. 1858. Enumeratio plantarum Banatu Temesiensi sponte crescentium ct frequentius cultarum. Verhandlungen des Zoologisch-Botanischen Vereins in Wien 8: 39-240.

Hillig KW, Mahlberg PG. 2004. A chemotaxonomic analysis of cannabinoid variation in Cannabis (Cannabaceae). American Journal of Botany 91(6): 966-975.

Hooke R. 1726. "Account of a plant, call'd Bangue, read before the Royal Society, Dec. 18, 1689," pp. 210-212 in Derham W, ed. Philosophical experiments and observations of the late eminent Dr. Robert Hooke. J. Innys, London.

Hooker JD. 1890. The Flora of British India, Vol. 5. L. Reeve & Co., London.

Ibn al-Baitar. 1985. Kitab al-Jami' li-mufradat al-adwiyah wa-al-aghdhiyah (The Comprehensive Book on Materia Medica and Foodstuffs). Institute for the History of Arabic-Islamic Science at the Johann Wolfgang Goethe University, Frankfurt am Main (facsimile of 1875 edition, Bulaq press, Cairo).

Janischevsky DE. 1924. [phrase omitted] (A form of cannabis in wild areas of south-eastern Russia). [phrase omitted] (Scientific Notes of Saratov State University named after N. G. Chernvshevsky) 2(2): 3-17.

Janischevsky DE. 1925. [phrase omitted] y Cannabis ruderalis Janisch. (Entomohoriya in Cannabis ruderalis Janisch.). Saratov Society of Naturalists, Saratov.

Jarvis CE. 2007. Order Out Of Chaos: Linnaean plant names and their types. Linnean Society of London in association with the Natural History Museum, London.

Kaempfer E. 1712. Amoenitatum exoticarum. Henry Wilhelm Meyer, Lemgo, Germany.

Kanitz A. 1881. Plantas Romaniae hucusque cognitas. Dcmjcn, Cluj, Romania.

Khrebtov AA. 1925 (1926). O atiKofi KOHonjic (About wild hemp). Economica (Perm) 2-3: 33-34.

Knorring OE, Minkvits ZA. 1912. [phrase omitted] (Vegetation of the Aulie-Ata district distict of the Syr-Darya region). Proceedings Soils and Botany Expedition, St. Petersburgh.

Knox R. 1681. An historical relation of the island of Ceylon in the East-Indies. Richard Chiswcll. London.

Kolb P. 1719. Caput Bonae Spei hodiernum, das ist, Vollstandige Beschreibung des africanischen Vorgeburges der Guten Hofhung. Peter Conrad Monath. Nurnberg.

Korotkova TI. 1978. H.H. BaBHJioB b CapaTOBC. 1917-1921: [phrase omitted] (N.I. Vavilov in Saratov, 1917-1921 : feature stories). Privolzhskoye Book Publishing House, Saratov.

Korshinskii SI. 1898. Tentamen Florae Rossiae orientalis. Memoires de l'Academie Imperiale des Sciences de St. Petersbourg 7(1): 1-566.

Krylov PN. 1909. [phrase omitted], Tom V (Flora of Altai and the Tomsk province, Vol. J). Tomsk.

Lamarck JB. 1785. Encyclopedie Methodique 1(2): 695. Panckoucke, Paris.

Laursen L. 2015. Botany: the cultivation of weed. Nature 525: S4-S5.

von Ledebour CF. 1847-49. Flora Rossica Vol III, Pars I. Sumptibus Librarme E. Schwcizcrbart, Stuttgart.

Lepechin II (Hare CH, trans). 1774. Tagebuch der Reise durch verschiedene Provinzen des Rmsischen Reiches, Erster Theil. Richterischen Buehhandlung, Altenburg.

Linder. J (Stenzel CG. ed). 1739. Jo. Lindenstolpe med. Doct. Liber de venenis. G. H. Schwartzius, Francofurti et Lipsiae.

Linnaeus C. 1737. Hortus Cliffortianus. George Clifford, Amsterdam.

Linnaeus C. 1749. Caroli Linnaei Materia medica, liber unus de plantis secundum genera, loca, nomina. Laurentii Salvii, Stockholm.

Linnaeus C. 1753. Species Plantarum 2: 1057. Laurentii Salvii, Stockholm.

Linnaeus C. 1754. Genera Plantarum, 5th ed. Laurentii Salvii, Stockholm.

Liou SZ. 1988. C. sativa var. ruderalis (Janischevsky) Flora Liaoningica 1: 289. Liaoning Science and Technology Press, Shenyang, Liaoning.

Ly-Tio-Fane M. 1976. Pierre Sonnerai 1748-1814. An account of his life and work. Imprimerie et Papeterie commerciale, Cassis, Mauritius.

Macedo MP, Kosmann C, Pujol-Luz JR. 2013. Origin of samples of Cannabis sativa through insect fragments associated with compacted hemp drug in South America. Revista Brasileira de Entomologia 57: 197-201.

Mak. E, Regel. EA. 1862. [phrase omitted] (Experience in the flora of Ussuriyskoy country). St. Petersburg.

Mal'tsev AI. 1939. [phrase omitted] CCCP, Tom II (Atlas of major species of weed plants of the USSR, Vol. II). Sel'khozgiz, Moscow.

McPartland JM. 1996. A review of Cannabis diseases. Journal of the International Hemp Association 3(1): 19-23.

McPartland JM, Guy G. 2004. "The evolution of Cannabis and coevolution with the cannabinoid receptor--a hypothesis." pp. 71-102 in. Guy G, Robson R. Strong K, Whittle B, eds. The Medicinal Use of Cannabis. London: Royal Society of Pharmacists.

McPartland JM, Clarke RC, Watson DP. 2000. Hemp Diseases and Pests--Management and Biological Control. CABI Publishing, Wallingford, UK.

Medvedev Z. 1969. The rise and fall of T.D. Lysenko. Columbia University Press, NY.

Nekrasova VL. "[phrase omitted] 18. Moraceac," pp. 43-48 in Keller BA, Lyubimcnno VI, Mal'tsev AI, Fcdtschenko BA, Schischkin BC, Roshevitz RJ, Kamensky KV, eds. 1934. [phrase omitted] CCCP, Tom II (Weed plants of the USSR, Vol. II). USSR Academy of Sciences, Leningrad.

Oganovsky NP. 1922. [phrase omitted] (Southern Altai. How we can use its wealth). All-Russian Central Union, Moscow.

Pallas. PS. 1793. Voyages de M. P. S. Pallas, en differentes provinces de l'empire de Russie. Tome Cinquieme. Maradan, Paris.

Parkinson J. 1640. Theatrum botanicum. Thomas Cotes, London.

Panik, G. 2012. Wild cannabis ruderalis bud and seeds--a lucky find. Available at: http://cannabisgrowing. wordpress.com/2012/09/19/wild-cannabis-ruderalis-bud-and-seeds-a-lucky-find

Petiver J. 1703. The eighth book of East India plants, sent from Fort St. George to Mr. James Petiver Apothecary, and F.R.S. with his remarks on them. Philosophical Transactions of the Royal Society of London 23: 1450-1460.

Plukenet L. 1696. Almagestum botanicum sive Phvtographiae Pluc'netianae. Sumptibus Autoris, London.

Popovsky M. 1984. The Vavilov affair. Archon Books, Hamden, CT.

Prain D. 1904. On the morphology, teratology and diclinism of the flowers of Cannabis. Scientific Memoirs by Officers of the Medical and Sanitary Departments of the Government of India 12: 51-82.

Prevost A, ed. 1768. Description des pays qui bordent La Cote Orientale D'Afrique, Depuis le Cap De Bonne-Esperance jusqu'ac Cap de Guardauf. Histoire generate des Voyages 6: 428-554.

Ray J. 1693. Historia Plantarum Generalis, Tomus Primus. Small & Walford, London.

van Rheede tot Drakestein. HA. 1690. Hortus Malabaricus 10: 119-120.

Rochel A. 1835. Botanische Reise in das Banat im Jahre 1835. Gustav Heckenast, Leipzig.

Rumpf, G [Rumphius], 1747. Herbarium Amboinense 5: 208-211.

Schultes RE, Klein WM, Plowman T, Lockwood TE. 1974. Cannabis: an example of taxonomic neglect. Harvard University Botanical Museum Leaflets 23: 337-367.

Schoenmakers N. 1986. The Seed Bank 1986/1987 Catalogue. Drukkerij Dukenburg Printers, Nijmegen, The Netherlands.

Sennert D. 1629. Practica Medicina, Liber Primus. Sumptibus Petri Ravaud, Lugduni.

Serebriakova, TY, Sizov, IA. 1940. "Cannabinaceae," pp. 1-53 in. Vavilov NI, Vul'f EV, eds., [phrase omitted] CCCP, Tom V (Cultural Flora of the USSR, Vol. 5). State Publishing House of Collective-farm and State-farm Literture, Moscow-Leningrad.

Sinskaya, EN. 1925. [phrase omitted] (On the fields crops of the Altai). [phrase omitted] (Bulletin of Applied Botany, Genetics, and Plant Breeding) 14: 367-370.

Shmal'gauzen, IF. 1897. [phrase omitted], Tom II (The flora of Central and Southern Russia, the Crimea and North Caucasus, Vol. 2). I.N. Kushnercv, Kiev.

Sievers. J. 1796. "Sievers Briefe aus Sibirien. Drifter Brief," pp. 168-181 in Pallas PS. Neue nordische Beytrage, Siebenter Band. Johann Zacharias Logan, St. Petersburg.

Small E. 1975a. Morphological variation of achenes of Cannabis. Canadian Journal of Botany 53: 978-987.

Small E. 1975b. On toadstool soup and legal species of marihuana. Plant Science Bulletin 21(3): 34-39.

Small E, Cronquist A. 1976. A practical and natural taxonomy for Cannabis. Taxon 25(4): 405-435.

Sojak. J. 1960. "Zur Verbreitung von Cannabis ruderalis Janisch.," pp. 19-20 in Novitates Botanicae et Delectus seminum fructuum, sporarumque anno 1960 collectorum, quae praefectus Horti botanici Universitas Carolina Pragensis. Botanicka Zahrada, Prague.

Sojak J. 1980. Fragmenta phytotaxonomica ct nomenclatorica, 1. Casopis Narodniho Muzea v Praze, Rada Prirodovedna 148(2): 77-80.

Sonnerat P. 1782. Voyage aux Indes Orientales et a la Chine. 2 vols. L'auteur, Paris.

Stafleu. FA, Cowan. RS. 1979. Taxonomic literature, Vol. II, H-Le. Bohn, Scheltema & Holkema, The Hague.

Stearn WT. 1974. Typification of Cannabis sativa L. Harvard University Botanical Museum Leaflets 23(9): 325-336.

Tennstedt D, Saint Remy A. 2009. "Cannabis et pcau," pp. 91-105 in Milpied B. ed. Progres en dermatoallergologie. Editions John Libbey Eurotext, Montrouge, France.

Thouin A. 1785. Observations sur le chanvre de la Chine. Memoires de la Societe d'Agriculture de Paris Trimestre d'Automne: xxvi-xxviii.

Van Linschoten, JH (Bry T de, ed.). 1601. Pars qvarta Indice Orientalis qva primvm varij generis animalia, fructus, arbores. M. Becker, Frankfurt.

Vavilov NI. 1922. [phrase omitted] (Field crops of the southeast). [phrase omitted] (Bulletin of Applied Botany, Genetics, and Plant Breeding) 13 (Suppl. 23): 147-148.

Vavilov NI. 1926. The origin of the cultivation of "primary" crops, in particular cultivated hemp. [phrase omitted] 16(2): 221-233.

Vavilov NI. 1931. The role of Central Asia in the origin of cultivated plants. [phrase omitted] 26(3): 1-44.

Vavilov NI (Dorofeyev VF, ed., Love D, transi). 1992. Origin and Geography of Cultivated Plants. Cambridge University Press, Cambridge UK.

Vavilov NI, Bukinich DD. 1929. Konopli. [phrase omitted] 33 (Suppl.): 380-382. Supplement published separately as: [phrase omitted] (Agricultural Afghanistan). Izdanija Vscsojuznyj Instituia Prikladnoj Botaniki i Novych Kul'tur pri SNK. SSSR i Gosudarstvcnnogo Instituta Opytnoj Agronomii NKZ. Leningrad.

Velenovsky J. 1898. Flora Bulgarica, Supplementum I. Rivnac, Prague.

Villiers JF. 1973. Cannabaccac. Flore du Gabon 22: 55-58.

Vysotsky GN. 1915. [phrase omitted] (Cultural and phytologically sketch). Proceedings of the Bureau of Applied Botany 8 (10): 1113-1443.

Yarmolenko, AV. 1936. "[phrase omitted] 375. [phrase omitted]--Cannabis L." pp. 383-384 in Komarov VL, ed. [phrase omitted] CCCP, Tom. V (Flora USSR, Vol. 5). USSR Academy of Sciences, Leningrad.

Zinger VY. 1885. [phrase omitted] (Compendium of information about the flora of Central Russia). Universitetskoi tipografii, Moscow.

Zhukovsky, PM (Hudson PS, transi.). 1962. Cultivated plants and their wild relatives. Abridged translation. Commonwealth Agricultural Bureaux, Famham Royal, UK.

Appendix 2 literature cited

Blunt W. 2001. Linnaeus: the compleat naturalist. Princeton University Press, Princeton NJ.

compte de Buffon, GLL. 1749. Histoire naturelle, generale et particuliere:: avec la description du Cabinet du Roi. Imprimerie Royale, puis Plassan. Paris.

compte de Buffon, GLL 1753. Histoire naturelle, generale et particuliere. Tome quatrieme. Imprimerie Royale, puis Plassan, Paris.

Corsi P. 1988. The age of Lamarck. University of California Press, Berkeley, CA.

Coxe W. ed. 1811. Literary life and selected works of Benjamin Stillingfleet, vol. I. J. Nichols and Son, London.

Cuvier G. 1836. Elegy of Lamarck. Edinburgh New Philosophical Journal 20: 1-22.

Dillenius JJ. 1741. Historia Muscorum. Thcatro Sheldoniano, Oxford.

Fleming J. 1801. "Mr. Fleming, Bengal Cons. 5th May, 1801," pp. 21-22 and 52-53 in Wissett R. 1808. A treatise on hemp. J. Harding, London.

Fleming J. 1810. A Catalogue of Indian Medicinal Plants and Drugs. Hindustani Press, Calcutta; Asiatick Researches 11: 153-196.

Frodin DG. 2001. Guide to Standard Floras of the World, 2nd Ed. Cambridge University Press, Cambridge, UK.

Hooker JD, Thomson T. 1855. Flora Indica: being a systematic account of the plants of British India, Vol I. Pamplin, London.

Hudson W. 1762 Flora anglica. J. Nourse & C. Moran, London.

Hull, DL. 1984. "Lamarck among the Anglos," pp. xl-lxvi in Lamarck's Zoological Philosophy. University of Chicago Press. Chicago, IL.

Lamarck JB. 1778. Flore francoise. 3 vols. Imprimerie Royale, Paris.

Lamarck JB. MSI. Encyclopedie Methodique, Botanique, Tome premier, part 1, p. 1-344. Panckoucke, Paris.

Lamarck JB. 1788. Encyclopedie Methodique, Botanique, Tome second, part 2. p. 401-774. Panckoucke, Paris.

Lamarck 1791. Tableau encyclopedique et methodique des trois regnes de la nature, Botanique, Premiere livraison. Panckoucke, Paris.

Lamarck JB. 1792. Philosophie botanique. Journal d'Histoire naturelle 1: 81-91.

Lamarck JB. 1809. Philosophie Zoologique, 2 vols. Dcntu, Paris.

Lamarck JB, Mirbel B. 1803. Histoire naturelle des vegetaux, Tome Premier. Crapelet Paris.

Linnaeus C. 1735. Systema Naturae. Joannis Wilhelmi dc Groot, Leiden.

Linnaeus C. 1737a. Critica Botanico. Conrad Wishoff, Leiden.

Linnaeus C. 1737b. Genera Plantarum. Conradum Wishoff, Leiden.

Linnaeus C. 1751. Philosophia Botanica. Kiesewetter, Stockholm.

Linnaeus C. 1753. Species Plantarum 2: 1057. Laurentii Salvii, Stockholm.

Locke J. 1690. An essay concerning human understanding. Tho. Basset, London.

Long G. ed. 1843. Carl Ludwig Willdenow. The Penny Cyclopaedia 27: 395-396. Charles Knight and Co., London.

Mayr E. 1942. Systematics and the Origin of Species. Columbia University Press, NY.

Miller P. 1768. The gardeners dictionary. 8th edition. J & J Rivington. London.

O'Shaughnessy WB. 1838-1840. On the . or gunjah (Cannabis indica): Their effects on the animal system in health, and their utility in the treatment of tetanus and other convulsive diseases. Transactions of the Medical and Physical Society of Bengal 1838-1840: 71-102, 421-461.

Roxburgh W (Carey W, ed.). 1832. Flora Indica; or, Descriptions of Indian plants. Volume 3. W. Thackery, Serampore and Calcutta.

Royle JF. 1840. Essay on the productive resources of India. W.H. Allen, London.

Smith. JE. 1821. A selection of the correspondence of Linnaeus and other naturalists, Vol. 2. Longman, Hurst, Rces, Orme, and Brown, London.

Smith, JE. 1824. The English Flora, Vol. I. Longman, Hurst, Rees, Orme, Borwn, and Green. London.

Staileu FA. 1971a. Linnaeus and the Linnaeans. A. Oosthoek, Utrecht.

Stafleu FA. 1971b. Lamarck: the birth of biology. Taxon 20: 397-442.

Stillingfleet. B. 1759. Miscellaneous tracts relating to natural history, husbandry, and physic. R. & J. Dodsley, S. Baker, and M. Cooper, London.

Wight R. Walker-Arnott GA. 1834. Prodromus Florae Peninsulae lndiae Orientalis, Vol. I. Parbury, Allen & Co., London.

Willdenow. CL. 1805b. Caroli Linne Species Plantarum IV (2): 768-769. G. C. Nauk, Berlin.

Williams RL. 2001. Botanophilia in eighteenth-century France. Kluwer Academic Publishers, Dordrecht.

Appendix 3 literature cited

Aitchison JET. 1864. Flora of the Jhclum District of the Punjab. Journal of the Linnean Society, Botany 8: 55-77.

Aitchison JET. 1888. The botany of the Afghan Delimitation Commission. Transactions of the Linnean Society, Botany 2nd Ser. 3(1): 1-139.

Aitchison JET. 1869. Lahul: its flora and vegetable products. Journal of the Linnean Society of London. Botany 10: 69-101.

Alefeld F. 1866. Landwirthschaftliche Flora. Wicgandt & Hempel, Berlin.

Amman J. 1739. Stirpium rarioram in Imperio Rutheno sponte provenientium icones et descriptiones. Academia Scientiarum, St. Petersburg.

Basiner TFJ. 1848. Naturwissenschaftliche Reise durch die Kirgisenstcppc nach Chiwa. Beitrage zur Kenntnis des Russischen Reiches und der angranzenden Lander Asiens 15: 1-375.

Becker A. 1873. Reise nach Baku, Lenkoran. Dcrbent, Madschalis. Kasum Kent, Achty. Bulletin de la Societe Imperiale des Naturalistes de Moscou 47: 229-258.

von Besser, WSJG. 1822. Enumeratio plantarum hucusque in Volhynia, Podolia, gub. Kiioviensi, Bessarabia, Cis-Tyraica et circa Odessam Collectarum. Typis Joscphi Zawadzki, Vilnac.

Boissier E. 1879. Cannabis. Flora Orientalis sive enumeratio plantarum 4: 1152-1153.

Boitard P. 1839. Manuels-Roret. Nouveau Manuel du Cordier. Roret, Paris.

Bretschneider E. 1882. Botanicon Sinicum: Notes on Chinese botany from native and western sources. Trubner & Co., London.

Blume CL. 1825. Bijdragen tot de flora van Nederlandsch Indie, 10de Stuk. Ter Lands Drukkerij, Batavia [Jakarta].

Buchanan M. 1807. A Journey from Madras Through the Countries of Mysore, Canara, and Malabar, Vol. I. Cadell and Davies, London.

von Bunge, AG. 1833. Enumeratio plantarum, quas in China Borealia collegit. Memoires presentes a l'Academie Imperiale des Sciences de St.-Petersboutg par Divers Savants et lus dans ses assemblees 2: 75-147.

von Bunge AG. 1851. Beitrag zur kenntniss der flor Russlands und der steppen Central-Asiens. Kaiserliche Akadcmic der Wisscnschaften, St. Petersburg.

Butter D. 1839. Outlines of the topography and statistics of the southern districts ofOud'h. G. H. Huttmann, Calcutta.

Chardin J (Langles L, ed). 1811. Voyages du Chevalier Chardin en Perse, Vol. 4. Normant. Paris.

Clarke RC, Merlin MD. 2013. Cannabis evolution and ethnobotany. University of California Press, Berkeley.

Claus KE. 1838. "Index plantarum in deserto caspio atquc regionibus vicinis obscrvatarum," pp. 247-322 in Gobel FT, ed. Reise in die Steppen des siidlichen Russlands, Zweiter Theil. C.A. Kluge, Dorpat.

Cleghorn HFC. 1866. Principal plants of the Sutlej Valley, with hill, botanical, and English names; together with approximate elevations, and remarks. Transactions of the Botanical Society of Edinburgh 8: 77-84.

Crevost, C. 1917. Chanvrc-Cannaeis sativa (Lin.) et Cannabis gigantea. Bulletin Economique de l'Indochine n.s. 19; 613-614.

Czernajew, VM. 1859. Conspectus Plantarum circa Charcoviam et in Ucrania sponte crescentium et vulgo cultarum, pg 56. Published by the author. Kharkov.

D'Andrieux P. 1771. Catalogue raisonne des graines, bulbes et plantes qu' on trouve chez le Sieur Andrieux, Marchand Grainier-fleuriste & Botaniste du Roi. Andrieux, Paris.

de Candolle. AP. 1869. Prodromus systematis namralis regni vegetabilis 16(1): 30-31.

de Courtive 1848. Hashisch etude historique, chimique et physiologique. These a l'Ecole de Pharmacie de Paris. Edouard Bautruche, Paris. Delile AR. 1849. Cannabis chinensis. Annales des Sciences Naturelles; Botanique 12: 365-366.

Delile AR. 1849. Cannabis chinensis. Index seminum Horti Regii Botanici Monspeliensis anni 1849, p. 7.

Dukerley I. 1866. Note sur les differences que presente avec le chanvre ordinaire la variete dc cette espece connue en Algerie sous les noms de kif et dc tekrouri. Bulletin de la Societe Botanique de France 13: 401-106.

Duthie, JF 1898. "The botany of the Chitral Relief Expedition, 1895," pp. 139-181 in Records of the Botanical Survey of India, Volume 1. Office of the Superintendent of Government Printing, Calcutta.

Dutt UC. 1877. Materia medica of the Hindus. Thacker, Spink & Co., Calcutta.

Eichwald CE. 1830. Naturhistorische Skizze von Lithauen, Volhynien und Podolien. Joseph Zawadzki, Vilnus.

Falck JP (Georgi JG, ed). 1786. Beytrage zur Topographischen Kenntniss des Russischen Reichs, Zwenter Band. Akademic dcr wisscnschaftcn, St. Petersburg.

Fischer, JB. 1810. "Cannabis chinensis," pp. 45 and 131 in Auf vierzehnjahrige Erfahrungen und Beobachtungen gegriindete Anweisung zum Anbau auslandischer Getraidarten und einiger Oelgewachse. Grattenaucrschen Buchhandlung, Crailsheim.

Fleming, J. 1810. A Catalogue of Indian Medicinal Plants and Drugs. Hindustani Press, Calcutta; Asiatick Researches 11: 153-196.

Forsskal, P (Niebuhr C, ed). 1775. Flora Aegyptiaco-Arabica. Mollcri, Copenhagen.

Gastinel JB. 1849. Memoire sur le haschisch et ses applications dans la therapeutique. Repertoire de Pharmacie 6: 129-142.

George S. 2005. 'Not strictly proper for a female pen': eighteenth-century poetry and the sexuality of botany. Comparative Critical Studies 2: 191-210.

Georgi JB. 1800. Geographisch-physikalische und naturhistorische Beschreibung des Russischen Reichs zur Uebersicht bisheriger Kenntnisse von demselben, Des dritten Theils vierter Band. Friedrich Nicolovius, Kdningsberg.

Gmelin JG (Gmelin SG, ed). 1768. Flora sibirica sive Historia plantarum Sibiriae, Vol. III. Typographia Acadcmiae Scientarum, Pctropolis.

Godard E. 1867. Egypte et Palestine. Victor Masson et Fils, Paris.

Good R. 1947. The geography of the flowering plants. Longmans, Green and Co., New York.

Griffith, W. 1847. Journals of Travels in Assam Burma Bootan Afghanistan and the Neighbouring Countries Bishop's College Press, Calcutta.

Guldenstadt JA (Pallas PS, ed). 1791. Reisen durch Russland und im Caucasischen Gebiirge, Zweiter Theil. Kayserlichen Akadcmic der Wissenschaften, St. Petersburg.

Guyon JLG. 1842. Hhachiche ou hhachis-indi, preparation en usage chez les orientaux. La Review Independante 3: 545-546.

Hardwicke T. 1801. Narrative of a Journey to Sirinagur. Asiatick Researches 6 (Miscellaneous tracts): 244-263.

Hasselquist F. 1766. Voyages and Travels in the Levant, in the Years 1749, 50, 51, 52. Davis and Reymers, London.

Hedde JCPI. 1848. Description methodique des produits divers recueillis dans un voyage en China, 1843-1846. Theolier Aine, Saint-Etienne.

Henderson G, Hume AO. 1873. Lahore to Yarkand: incidents of the route and natural history of the countries traversed by the expedition of 1870. L. Reeve & Co., London.

Herder FG. 1892. Plantae Raddeanae apetalae V. Acta Horti Petropolitani 12(1): 31-132.

Heuffel J. 1858. Enumeratio plantarum Banatu Temesiensi sponte crescentium et frequentius cultarum. Verhandhmgen des Zoologisch-Botanischen Vereins in Wien 8: 39 to 240.

Heuze G. 1860. Les Plantes Industrielles, Vol. 2. Hachette, Paris.

Hill J. 1760. Flora Britanica. Jacob Waugh, London.

Hillig KW. 2005. Genetic evidence for speciation in Cannabis (Cannabaceae). Genetic Resources and Crop Evolution 52: 161-180.

Hoffmann W. 1944. "Hanf, Cannabis sativa L.," pp. 314-341 in Roemer T, ed. Handbuch der Pflanzenzuchtung, Band IV: Ruben, Kartoffeln, Ol- und Gespinstpflanzen, Tabak. Parey, Berlin.

Hohenacker RF. 1838. Enumeratio plantarum quas in itinere perprovinciam Talysch. Societe Imperiale des Naturalistes, Moscow.

Honigberger JM. 1852. Thirty-five years in the East. H. Bailliere, London.

Hooker JD, Thomson T. 1855. Flora Indica: being a systematic account of the plants of British India, Vol I. Pamplin, London.

von Humboldt A. 1811. Essai politique sur le royaume de la Nouvelle-Espagne, Tome deuxieme. F. Schoell, Paris.

Ibn al-Baitar. 1985. Kitab al-Jami' li-mufradat al-adwiyah wa-al-aghdhiyah (The Comprehensive Book on Materia Medica and Foodstuffs). Institute for the History of Arabic-Islamic Science at the Johann Wolfgang Goethe University, Frankfurt am Main (facsimile of 1875 edition, Bulaq press, Cairo).

Itier J. 1846. Notes sur quelques produits de l'industrie chinoise recueillis par M. Jules Itier, inspecteur principal des douanes. Bulletin de la Societe d'Encouragement pour l'Industrie Nationale 45: 238-240.

Itier, J. 1853. "Compte-Rendu des Essais de Naturalisation en France et en Algcricr de plusieurs plantes textiles originaires de la Chine," pp. 366-391 in. Journal d'un Voyage en Chine en 1843, 1844, 1845, 1846, Vol. 3. Dauvin et Fontaine, Paris.

Jacquemont V. 1861. Correspondance de Victor Jacquemont avec sa famille et plusieurs de ses amis pendant son voyage dans l'Inde, Tome second. Garnier Freres, Paris.

Janischevsky DE. 1924. [phrase omitted] (A form of cannabis in wild arcas of south-eastern Russia). [phrase omitted] (Scientific Notes of the Saratov State University named after N. G. Chernvshevsky) 2(2): 3-17.

Jomard M. 1852. Compte rendu, par le president de la commission centrale, sur l'envoi des gaines de la Chine. Bulletin de la Societe de Geographie 1852 (Jan-Juin): 88-93.

Karelin GS, Kirilov IP, 1841. Enumeratio plantarum anno 1840, in regionibus altaicis et confinibus collcctarum. Bulletin de la Societe Imperiale des Naturalistes de Moscou 14(4): 703-840.

Kerr HC. 1877. Report of the cultivation of, and trade in, ganja in Bengal. British Parliamentary Papers 66: 94-154.

Koch, C[K], 1854. Cannabis chinensis. Annales des Sciences Naturelles Botanique (Series 4) 1: 352.

Korshinskii SI. 1898. Tentamen Florae Rossiae orientalis. Memoires de l'Academie Impeiale des Sciences de St. Petersbourg 7(1): 1-566.

Lamarck JB. 1785. Encyclopedie Methodique. Botanique, Tome premier, part 2, pp. 345-752. Panckoucke. Paris.

Lawrence WR. 1895. The valley of Kashmir. H. Frowde, London.

von Ledebour CF, von Meyer CA, von Bunge A. 1833. Flora Altaica, Vol. TV. Reimeri, Berlin.

von Ledebour CF. 1847-49. Flora Rossica Vol III, Pats 1. Sumptibus Librariac E. Schweizcrbart, Stuttgart.

Lepechin I (Hase CH, trans). 1774. Tagebuch der Reise durch verschiedene Provinzen des Russischen Reiches. Erster Theil. Richterischen Buchhandlung, Altcnburg.

Lindemann EE. 1881. Flora Chersonensis, Vol. I. G. Ul'rikha, Odessa.

de Loureiro J. 1790. Flora Cochincliinensis, Tomus I. Typis ct expensis academicis, Ulyssipone [Lisbon],

Mackenzie WC. 1893. Hashish in Egypt. Chemist and Druggist 43: 183.

von Maltzan H. 1869. Sittenbilder aus Tunis und Algerien. Dyk, Leipzig.

von Maltzan H. 1873. Reise nach Siidarabien und geographische Forschungen. F. Vieweg & Sohn, Braunschweig.

Marschall von Bieberstein FA. 1808. Flora taurico-caucasica, Vol. 2. Typis Academicis, Charkouiac.

Martius TWC. 1832. Grundriss der Pharmakognosie des Pflanzenreiches. Palm & Enkc, Erlangcn.

Meyer CA. 1831. Verzeichniss der Pflanzen, welche wahrend der auf Allerhochsten Befehl, in den Jahren 1829 und 1830 unternommenen Reise im Caucasus und in den Provinzen am westlichen Ufer des Caspischen Meeres gefiinden und eingesammeh worden sind. Kaiserliche Academic der Wissenschaften, St. Petersburg.

Mongeri L. 1865. Sur le hachisch, le cannabis et 1'esrar. Annuaire de Therapeutique 25: 59-65.

O'Shaughnessy WB. 1838-1840. On the preparations of the Indian hemp, or gunjah (Cannabis indica); Their effects on the animal system in health, and their utility in the treatment of tetanus and other convulsive diseases. Transactions of the Medical and Physical Society of Bengal 1838-1840: 71-102, 421-461.

Pabst. G, ed. 1887. "Cannabis sativa L.," p. 13 in Kohler's Medizinal-Pflanzen Band 1. Eugen Kohler. GeraUntermhaus.

Pallas PS. 1766. Elenchus zoophytorum sistens generum adumbrations. Pctrum van Cleef, Hagae-Comitum.

Pallas PS. 1774. Spicilegia zoologica. Lange, Berolini.

Pallas PS. 1776. Reise durch verschiedene Provinzen des Russischen Reichs, Dritter Tlteil. Gedruckt bey der kayserlichen Academic der Wissenschaftcn, St. Petersburg (pg. 266).

Pallas, PS. 1793. Voyages de M. P. S. Pallas, en differentes provinces de l'empire de Russie. Tome Cinquieme. Maradan. Paris.

Parlatore F. 1867. Flora Italiana, Vol. IV. Le Monnier, Firenze.

Polak JK. 1865. Persien. Das Land und seine Bewohner, Zweiter Theil. Brockhaus. Leipzig.

Presl JP, Presel KB. 1819. Flora Cechica. J.G. Calve, Prague.

Regel EA. 1880. Cannabineac. Acta Horti Petropolitani 6 (1): 476.

Rey P. 1835. Lettre M. Rey, sur le chanvre du Piemont. Annales de la Societe d'Horticulture de Paris 16: 395-397.

van Rheede tot Drakestein HA., 1690. Hortus Malabaricus 10: 119-120.

Rottler JP (Taylor W, ed.). 1836-7. A dictionary of the Tamil and English languages, Volume I, Part II. Vefery Mission Press, Madras.

Roxburgh W (Carey W, ed.). 1832. Flora Indica; or. Descriptions of Indian plants, Volume 3. W. Thackcry, Scrampore and Calcutta.

Royle JF. 1839. Illustrations of the botany and other branches of the natural history of the Himalayan Mountains, and of the flora of Cashmere, Vol. I. W. H. Allen, London.

Rumpf, G [Rumphius]. 1747. Herbarium Amboinense 5: 208-211.

Semenov PP (Thomas C, ed). 1998. Travels in the Tian'-Shan', 1856-1857. The Hakluyt Society. London.

Senac M. 1826. Chanvre de Piemont, chanvre de Bologne. Bulletin Universel des Sciences et de l'Industrie. Quatiieme section: Bulletin des Sciences Agricoles et Economiques 6: 156.

Shaw RB. 1880. A sketch of the Turki language as spoken in Eastern Turkistan (Kashghar and Yarkand), Part II. Vocaublary. Baptist Mission Press, Calcutta.

von Siebold PF. 1827. Synopsis plantarum economic-arum universi regni Japonici. Batavia.

Sievers, J. 1796. "Sievers Briefe aus Sibirien. Dritter Brief," pp. 168-181 in Pallas PS. 1796. Nene nordische Beytrage, Siebenter Band. Johann Zacharias Logan, St. Petersburg.

Sinskaya EN. 1925. [phrase omitted] (On the fields crops of the Altai). [phrase omitted] (Bulletin of Applied Botany, Genetics, and Plant Breeding) 14: 367-370.

Stephan F. 1792. Enumeratio stirpium agri Mosquensis. Littcris Sommcrianis, Moscow.

Stickman O (Linnaeus C, praeses). 1754. "Herbarium Ambionese," Amoenitates Academicae 4: 1-27.

Stokes J. 1812. A Botanical Materia Medica, Vol. TV. J. Johnson, London.

Takhtajan AL (Crovello TJ transi, Cronquist A. ed.). 1986. Floristic regions of the world. University of California Press, Berkeley.

Tatarinov A. 1858. "Bemcrkungen uber die Anwcndung schmerzstillender Mittel bei den Operationcn. und die Hydropathie in China," p. 467-473 in Abel C, Mecklenburg FA, eds. Arbeiten der Kaiserlich Russischen Gesandtschaft in Peking uber China, sein Volk, seine Religion, seine Institutionen, socialen Verhdltnisse, etc. Vol. 2. Heinicke, Berlin.

Thunberg CP. 1784. Flora laponicae. Lipsiae.

Thunberg CP. 1796. Voyages de C.P Thunberg au Japon par le Cap de Bonne-Esperance, les Isles de la Sonde, etc., 4 vols. Benoit Dandre, Paris.

Trautvettero ER. 1867. Enumeratio Plantarum Songoricarum a Dr. Alexander Schrenk annis 1840-1843 collectarum. Bulletin de la Societe itnperiale des naturalistes de Moscou 40(2): 50-123.

Turczaninow N. 1856. Flora Baicalensi-Dahurica, Vol. II, Fasc. 2. Typus Universitatis Caesareae. Moscow.

USDA (U.S. Department of Agriculture). 1912. Seeds and plants imported during the period from July 1 to September 30, 1911: Inventory No. 28. Bureau of Plant Industry--Bulletin No. 248. Government Printing Office. Washington. DC.

Valikhanov C (Michell J, Michell R. trans). 1865. The Russians in Central Asia. Edward Stanford, London.

Vambery A. 1868. Sketches of Central Asia. Allen & Co., London.

Vavilov NI. 1922. [phrase omitted] (Field crops of the southeast). [phrase omitted] (Bulletin of Applied Botany, Genetics, and Plant Breeding) 13 (Suppl. 23): 147-148.

Vavilov NI, Bukinich DD. 1929. [phrase omitted] (Cannabis). [phrase omitted] 33 (Suppl.): 380-382. Published separately as: [phrase omitted] (Agricultural Afghanistan). Izdanija Vsesojuznyj Instituta Prikladnoj Botaniki i Novych Kul'tur pri SNK. SSSR. i Gosudarstvennogo Instituta Opytnoj Agronomii NKZ, Leningrad.

Velenovsky J. 1898. Flora Bulgarica, Supplementum I. Fr. Rivnac, Prague.

Vilmorin P. ed. 1837. Notices Diverses. Sur le chanvre du Piemont. Bulletin des seances de la Societe d'agriculture, sciences, arts et commerce du Puy 1: 139-143.

Vilmorin L. 1851. Chanvre de China: Tsing-Ma, Cannabis gigantea. Revue Horticole (Series 3) 5: 109-111.

Vilmorin H. 1892. Les plantes de grande culture. Cereales, plantes fourrageres, industrielles et economiques. Vilmorin-Andricux & Co., Paris.

Wallich N. 1828-1849. Numerical list of dried specimens of plants in the Museum of the Honl. East India Company which have been supplied by Dr. Wallich, superintendent of the botanic garden at Calcutta. Kew, London.

Willdenow KL (Thungerg CP). 1787. Florae Berolinensis Prodromus. Wilhclm Viewiegii, Berlin.

Wulff JC. 1765. Flora Borussica. Hacr. Hartvgn, Rcgiomonti et Lipsiae.

Zawadzki A. 1835. Enumeratio plantarum Galicioe et Bucowinae. Wilhelm Gottlieb Korn, Breslau.

Zhang GL. 1990. (Cannabis ethnobotany and the toxicity of constituents). Doctoral thesis. Kunming Institute of Botany, Chinese Academy of Sciences.

Appendix 4 literature cited

Anderson LC. 1974. A study of systematic wood anatomy in Cannabis. Harvard Botanical Museum Leaflets 24(2): 29-36.

Anderson LC. 1980. Leaf variation among Cannabis species from a controlled garden. Han'ard University Botanical Museum Leaflets 28(1): 61-69.

Brickell CD, ed. 2009. International Code of Nomenclature for Cultivated Plants, Eighth Edition. International Society for Horticultural Sciences. Leuven, Belgium.

Cannabis Strain Database. 2010. Available at http://weed-forums.com/strain-bank/10861-cannabis-strain-database.html

Chandra S, Lata H, Khan I A, ElSohlv MA. 2013. "The role of biotechnology in Cannabis sativa propagation for the production of phytocannabinoids," pp. 123-148 in Chandra S, Lata H, Varma A. eds. Biotechnology for medicinal plants. Springer-Verlag, Berlin.

Clarke, RC. 2001. "Sinsemilla heritage--what's in a name," in King J. The Cannabible Ten Speed Press, Berkeley CA.

Clarke RC, Merlin MD. 2015. Letter to the editor: Small, Ernest. 2015. Evolution and classification of Cannabis sativa (marijuana, hemp) in relation to human utilization. Botanical Review 81: 295-305.

De Meijer, EPM. 1993a. Hemp variations as pulp source researched in the Netherlands. Pulp & Paper 67(7): 41-43.

De Meijer. EPM. 1993b. Evaluation and verification of resistance to Meloidogyne hapla Chitwood in a Cannabis germplasm collection. Euphytica 71: 49-56.

De Meijer. EPM. 1994a. Diversity in Cannabis. Doctoral thesis, Wageningen Agricultural University, Wageningen, The Netherlands.

De Meijer, EPM. 1994b. Variation of Cannabis with reference to stem quality for paper pulp production. Industrial Crops and Products 3: 201-211.

De Meijer. EPM. 1995. Fiber hemp cultivars: a survey of origin, ancestry, availability and brief agronomic characteristics. Journal International Hemp Association 2(2): 66-73.

Dc Meijer. EPM. 1999. "Cannabis germplasm resources," pp. 133-151 in. Ranalli P. ed. Advances in Hemp Research. Haworth Press New York.

De Meijer, EPM. 2004. "The breeding of Cannabis cultivars for pharmaceutical end uses," pp. 55-69 in Guy G, Robson R. Strong K, Whittle B. eds. The Medicinal Use of Cannabis. Royal Society of Pharmacists, London.

De Meijer. EPM. 2014. "The chemical phenotypes (chemotypes) of Cannabis," pp. 89-110 in Pertwee RG, ed. Handbook of Cannabis. Oxford University Press. Oxford. UK.

De Meijer, EPM, Hammond KM. 2005. The inheritance of chemical phenotype in Cannabis sativa L. (II): cannabigerol predominant plants. Euphytica 145: 189-198.

De Meijer. EPM, Keizer LCP. 1996. Patterns of diversity in Cannabis. Genetic Resources and Crop Evolution 43: 41-52.

De Meijer, EPM, van Soest LJM. 1992. The CPRS Cannabis germplasm collection. Euphytica 62: 201-211.

De Meijer, EPM, van der Kamp, HJ, van Eeuwijk FA. 1992. Characterization of Cannabis accessions with regard to cannabinoid content in relation to other plant characters. Euphytica 62: 187-200.

De Meijer. EPM, Bagatta M, Carboni A, Crucitti P, Cristiana Moliterni VM, Ranalli P, Mandolino G. 2003. The inheritance of chemical phenotype in Cannabis sativa L. Genetics 163: 335-346.

De Meijer, EPM, Hammond KM, Micheler M. 2009a. The inheritance of chemical phenotype in Cannabis sativa L. (III): variation in cannabichromene production. Euphytica 165: 293-311.

Dc Meijer, EPM, Hammond KM, Sutton A. 2009b. The inheritance of chemical phenotype in Cannabis sativa L. (IV): cannabinoid-free plants. Euphytica 168: 95-112.

Doyle R. 2007. The transgenic involution," pp. 70-82 in Kac E, ed. Sigtis of life. Massachussetts Insititute of Technology, Cambridge, MA.

Gilmore S, Peakall R. 2003. Isolation of microsatellite markers in Cannabis sativa L. (marijuana). Molecidar Ecology Notes 3: 105-107.

Gilmore S, Peakall R, Robertson J. 2003. Short tandem repeat (STR) DNA markers are hypcrvariable and informative in Cannabis sativa: implications for forensic investigations. Forensic Science International 131: 65-74.

Gilmore S, Peakall R, Robertson J. 2007. Organelle DNA haplotypes reflect crop-use characteristics and geographic origins of Cannabis sativa. Forensic Science International 172: 179-190.

Hanelt P, ed. 2001. Mansfeld's Encyclopedia of Agricultural and Horticultural Crops, Vol. 1. Springer-Verlag, Berlin.

Hillig KW. 2004a. A multivariate analysis of allozyme variation in 93 Cannabis accessions from the VIR germplasm collection. Journal of Industrial Hemp 9(2): 5-22.

Hillig KW. 2004b. A chemotaxonomic analysis of terpenoid variation in Cannabis. Biochemical Systematics and Ecology 32: 875-891.

Hillig KW. 2005a. Genetic evidence for speciation in Cannabis (Cannabaccac). Genetic Resources and Crop Evolution 52: 161-180.

Hillig, KH. 2005b. A systematic investigation of Cannabis. Doctoral Dissertation, Department of Biology, Indiana University, Bloomington, IN.

Hillig KW. 2005c. A combined analysis of agronomic traits and allozyme allele frequencies for 69 Cannabis accessions. Journal of Industrial Hemp 10(1): 17-30.

Hillig KW, Mahlberg PG. 2004. A chemotaxonomic analysis of cannabinoid variation in Cannabis (Cannabaceae). American Journal of Botany 91(6): 966-975.

Howard C, Gilmore S, Robertson J, Peakall R. 2008. Developmental validation of a Cannabis sativa STR multiplex system for forensic analysis. Journal Forensic Science 53: 1061 1067.

Howard C, Gilmore S, Robertson J, Peakall R. 2009. A Cannabis sativa STR genotype database for Australian seizures: forensic applications and limitations. Journal Forensic Science 54: 556-563.

Kojoma M, Seki H, Yoshida S, Muranaka T. 2006. DNA polymorphisms in the tetrahydrocannabinolic acid (THCA) synthase gene in "drug-type" and "fiber-type" Cannabis sativa L. Forensic Science International 159(2-3): 132-140.

Leafly. 2015. Leafy online database. Available at: https://www.lcafly.com

Lee MA. 2013. Project CBD update: the tango of supply and demand. O'Shaughnessy's Winter/Spring 2013: 22-23.

Mabberley DJ. 2008. Mabberley's plant book, 3rd Ed. Cambridge University Press, Cambridge. UK.

Mandolino G, Bagatta M, Carboni A, Panalli P, de Meijer E. 2003. Qualitative and quantitative aspects of the inheritance of chemical phenotype in Cannabis. Journal of Industrial Hemp 8(2): 51-72.

McPartland JM, Hillig KW. 2003. The hemp russet mite. Journal of Industrial Hemp 8(2): 107-112.

McPartland JM, Hillig KW. 2004. Striatum ulcerosa. Journal of Industrial Hemp 9(1): 89-96.

McPartland JM, Hillig KW. 2006. Host-parasite relationships in Cannabis. Journal of Industrial Hemp 10(2):85-I04.

Mukherjee A, Roy, SC. Bera, SD. Jiang. HE, Li, X, Li, CS, Bera, S. 2008. Results of molecular analysis of an archaeological hemp. (Cannabis sativa L.) DNA sample from North West China. Genetic Resources and Crop Evolution 55: 481-85.

Onofri C, de Meijer EPM, Mandolino G. 2015. Scqucncc heterogeneity of cannabidiolic- and tetrahydrocannabinolic acid-synthase in Cannabis sativa L. and its relationship with chemical phenotype. Phytochemistry 116: 57-68.

Pierson. D. 2016. Why chocolopc? To sell marijuana, you need a clever name. Los Angeles Times, Feb. 9. 2016.

Quimby MW, Doorenbos NJ, Turner CE, Masoud A. 1973. Mississippi-grown marihuana--Cannabis sativa cultivation and observed morphological variations. Economic Botany 27: 117-127.

Sawler J, Stout JM, Gardner KM, Hudson D, Vidmar J, Butler L, Page JE, Myles S. 2015. The genetic structure of marijuana and hemp. PLoS One 10(8): c0133292.

Schultes RE. 1970. "Random thoughts and queries on the botany of Cannabis," pp. 11-38 in. Joyce CRB, Curry Sh. eds. The Botany and Chemistry of Cannabis. J.& A. Churchill, London.

Schultes RE, Klein WM, Plowman T, Lockwood TE. 1974. Cannabis', an example of taxonomic neglect. Harvard University Botanical Museum Leaflets 23: 337-367.

Seedfinder., 2015. Seedfinder online database. Available at: http://cn.sccdfindcr.cu/.

Shipunov AB. 2010. [phrase omitted] (Cannabis L.) [On the taxonomy of hemp (Cannabis L.)] [phrase omitted] 3(19): 128-130.

Small E. 1972. Infertility and chromosomal uniformity in Cannabis. Canadian Journal of Botany 50: 1947-1949.

Small E. 1975. Morphological variation of achencs of Cannabis. Canadian Journal of Botany 53: 978-987.

Small E. 1979. The species problem in Cannabis: science & semantics, 2 vols. Corpus, Toronto.

Small E. 1984. "Hybridization in the domesticated-weed-wild complex," pp. 195-210 in Grant WF, ed. Plant biosystematics. Academic Press, NY.

Small E. 2007. Cannabis as a source of medicinals, nutraceuticals, and functional foods. Advances in Medicinal Plant Research 2007: 1-39.

Small E. 2015a. Evolution and classification of Cannabis sativa (marijuana, hemp) in relation to human utilization. Botanical Review 81: 189-294.

Small E. 2015b. Response to the erroneous critique of my Cannabis monograph by R. C. Clarke and M.D. Merlin. Botanical Review' 81: 306-316.

Small E, Antle T. 2003. A preliminary study of pollen dispersal in Cannabis sativa in relation to wind direction. Journal of Industrial Hemp 8(2): 37-50.

Small E, Beckstead HD. 1973a. Common cannabinoid phenotypes in 350 stocks of Cannabis. Lloydia 36: 144-116.

Small E, Beckstead HD. 1973b. Cannabinoid phenotypes in Cannabis sativa. Nature 245: 147-148.

Small E, Cronquist A. 1976. A practical and natural taxonomy for Cannabis. Taxon 25(4): 405-135.

Small E, Marcus D. 2003. Tetrahydrocannabinol levels in hemp (Cannabis sativa L.) germplasm resources. Economic Botany 57: 545-558.

Small E, Naraine SGU. 2015a. Expansion of female sex organs in response to prolonged virginity in Cannabis sativa (marijuana). Genetic Resources and Crop Evolution 63: 339-348.

Small E, Naraine SGU. 2015b. Size matters: evolution of large drug-secreting resin glands in elite pharmaceutical strains of Cannabis sativa (marijuana). Genetic Resources and Crop Evolution 63: 349-359.

Small E, Beckstead HD, Chan A. 1975. The evolution of cannabinoid phenotypes in Cannabis. Economic Botany 29: 219-232.

Small E, Jui P, Lefkovitch LP. 1976. A numerical taxonomic analysis of Cannabis with special reference to species delimitation. Systematic Botany 1: 67-84.

Small E, Pocock T, Cavers PB. 2003. The biology of Canadian weeds.

119. Cannabis sativa L. Canadian Journal of Plant Science 83: 217-237.

Watson DP. 1985. Cultivator's choice catalog #4. Self-published. Amsterdam, Holland.

Yang YH. 2003. [phrase omitted] [The classification history of the genus Cannabis]. China Plant Fibers and Products 25(1): 9-11.

Appendix 1: Protologues Appendix 1 a. Cannabis sativa L.

Diagnosis or description

Linnaeus (1753) classified C. sativa in Class Dioecia (dioecious plants), and Order Tetrandria (male plants have four stamens). These aspects of morphology are the only descriptive elements he provided in Species Plantarum. Even by Linnaeus's standards, this is an extremely brief description. For genera with only one species, such as Cannabis, Linnaeus provided a longer description in Genera Plantarum (Linnaeus, 1754). For this reason, the ICN explicitly links taxa coined in Species Plantarum with their descriptions in the fifth edition of Genera Plantarum. The Cannabis description in Genera Plantarum is limited to flower and seed morphology. Translated from Latin:

MALE. Calyx: Perianth five-parted: leaves oblong, acuminate-obtuse, concave. Corolla: absent. Stamens: filaments five in number, thread-like, short. Anthers: oblong, quadrangular.

FEMALE. Calyx: Perianth single-leaved, oblong, acuminate, opposite at the base, dehiscing longitudinally, persistent. Corolla: absent. Pistil: Ovary minute, Style divided, sharply pointed, long. Stigma acute. Perianth minimal. Calyx tightly closed. Seed: Nut globose-depressed, bivalvate.

Note a discrepancy: Species Plantarum Linnaeus (1753) described males with four stamens, whereas Genera Plantarum (Linnaeus, 1754) described plants with five stamens. Five stamens is correct. The correct version was passed down verbatim from the first edition of Genera Plantarum, written in 1737. Hence the 1753 error was typographic. Linnaeus corrected his mistake in the second edition of Species Plantarum in 1763.

Synonymy and references

Linnaeus (1753) cited five C. sativa synonyms by five authors, presented in his typical telegraphic style. We provide a translation of Linnaeus's abbreviations in Box 1. Note a typographic error: Linnaeus said C.foliis digitatis appeared in Materia Medica on page 475. In fact the taxon appears in Materia Medica on page 162 (Linnaeus, 1749).
Box 1 Translation of author and citation abbreviations by Linnaeus
(1753)

Cannabis fotiis digitatis Linnaeus. Hortos Cliffortianus (1738: p.
457); Linnaeus, Hortos Upsaliensis (1748: p. 297); Linnaeus,
Materia Medica (1749: p. 162, no. 457); Dalibard, Florae
Parisiensis Prodromus (1749: p. 200); van Royen, Florae Leydensis
prodromus (1740: p. 221).

Cannabis sativa Baullin, Pinax Theatri Botanici (1623: p. 320).
[female]

Cannabis mas Dalechamps (d'Alechamps), Historia generalis Plantarum
(1587: p. 497). [female]

Cannabis erratica Bauhin, Pinax Theatri Botanici (1623, p. 320).
[male]

Cannabis femina Dalechamps (d'Alechamps), Historia generalis
Plantarum (1587: 497). [male]


Linnaeus notably excluded taxa of Asian Cannabis from the C. sativa protologue. Sixteen years earlier, in his previous synopsis of Cannabis, Linnaeus (1737) discussed two taxa assigned to South Asian Cannabis by van Rheede tot Drakestein (1690), and two taxa assigned to East Asian fiber by Kaempfer (1712). Furthermore, Linnaeus (1737) cited three other authors, Bauhin, Ray, and Morison, who also coined taxa for psychoactive Asian Cannabis, distinct from European hemp. Linnaeus knew about those taxa--he cited taxa that Bauhin, Ray, and Morison assigned to European hemp--but he did not address them. In his Materia Medica, Linnaeus (1749) listed narcotica and inebrians as some of the attributes of Cannabis, which are adjectives used by the aforementioned authors who described Asian Cannabis.

Type specimen

Linnaeus's type specimen of C. sativa is stored in the Linnaean Herbarium (herb. LINN), specimen no. 1177.2, a lectotype designated by Villiers (1973). As noted by Jarvis (2007), Villiers holds a one-year priority over Schultes et al. (1974), who designated a different lectotype, Hortus siccus Cliffortianus (herb. BM) p. 457. Steam (1974) dedudced from the numbering system that Linnaeus collected 1177.2 in 1753. No type location is given, but in 1753 Linnaeus lived in Uppsala.

Lectotype 1177.2 consists of the uppermost 28 cm of a fruiting staminate plant. Leaves branch alternately from the stalk, palmately compound, light green, mostly with three leaflets, and with long petioles. Central leaflets are narrowly lanceolate, acuminate, with sharp serrations, up to 78-85 x 7-9.5 mm. Inflorescences are loose, not dense; subtending floral leaves have a sparse covering of capitate-sessile glandular trichomes; perigonal bracts (i.e., bracteole, calyx) have a relatively sparse covering of capitate-stalked glandular trichomes. Styles and stigmas are not prominent, pale green in color. The fruit includes a non-persistent perianth, achene large (4.8 x 2.5 mm), oblong in outline, pale green with a fine reticulated pattern, base short and pointed with a simple articulation.

The previously-recognized lectoype, Clifford Herbarium p. 457.1, is illustrated by Steam (1974). The flowering top is somewhat denser than 1172.2, with slightly larger leaves, 3-5 leaflets per leaf, leaflets broadly lanceolate, and with larger achenes (5.0 x 3.5 mm). The specimen likely dates to Linnaeus's time in Holland, and represents "the old cultivated hemp stock of northern Europe" (Steam, 1974).

Appendix 1b. Cannabis indica Lam.

Diagnosis or description

Lamarck (1785) provided a full description of C. sativa (not just its flower parts, like Linnaeus). Lamarck then separated C. indica from C. sativa by "very distinct" morphological and phytochemical differences. We translate from French: "It is smaller, more ramifications of the stalks, which are tough [woody] and more cylindrical, and distinguished particularly by alternating branches. Their leaflets are very narrow, linear-lanceolate, and very acuminate. The male individuals bear five to seven leaflets, but those that are female may exhibit as few as three for each petiole, and leaves at the top [of the plant] are even simple [not compound]. The female flowers have a velous calyx, and long styles that are alike."

We interpret "vellous calyx" to mean "velvety perigonal bract," due to a dense pubescence of capitate-stalked glandular trichomes. Lamarck noted that C. indica does not provide a good source of fiber, and it produces a strong odor "resembling somewhat that of tobacco." He mentioned the intoxicating properties of C. indica when smoked in a pipe. "The principal effect of this plant consists of going to the head, disrupting the brain, where it produces a sort of drunkenness that makes one forget ones sorrows, and produces a strong gaiety."

Synonymy and references

Lamarck cited six synonyms and their authors:

1. Cannabi similis exotica Bauhin (Pinax Theatri Botanici 1623: p. 320); Bauhin cited descriptions of Bangue by da Orta and Acosta, in Goa, India;

2. Kalengi-cansjava Rheede (Hortus Malabaricus 1690; 10: 119); assigned to male plants in Kochi, India;

3. Tsjeru-cansjava Rheede (Hortus Malabaricus 1690: 10: 121); assigned to male plants in Kochi, India;

4. Cannabis peregrina gemmis fructuum longioribus Morison (.Plantarum historice universalis Oxoniensis 1699; 3:433); Morison cited Bauhin and Rheede;

5. Cannabis indica Rumph (Herbarium Amboinense 1747; 5: 208), a "pre-Linnaean" (pre-1753) taxon assigned to plants in Indonesia;

6. Dakka ou Bangua Prevost (1768), an editorialized version of Kolb (1719) who described plants in South Africa.

Four authors in Lamarck's synonymy (1, 2, 3, 4) previously appeared in Linnaeus (1737). Lamarck omitted two synonyms cited by Linnaeus: Bangue cannabi Ray 1686, and Bangue cannabi simile J. Bauhin and Cherler 1651-2. Both Linnaeus and Lamarck omitted other "pre-Linnean" (pre-1753) authors who differentiated European hemp from psychoactive Cannabis. Going back in time: Linder (1739), Burman (1737), Drury (1729), Hooke (1726), Kaempfer (1712), Petiver (1703), Plukenet (1696), Fryer (1698), Ray (1693), Chardin (1686), Knox (1681), de Flacourt (1661), Parkinson (1640), Sennert (1629), dos Santos (1609), de Gouvea (1606), Van Linschoten (1601), Alpini (1591), Acosta (1578), de L'Ecluse (1567), da Orta (1563), Fuchs (1542), and Bock (1539). The first European to assign separate names to European and Asian Cannabis was Ibn-al-Baitar, around 1240, in Arabic. He differentiated qinnab (plants he knew in Spain) from plants he encountered in Egypt, qinnab hindi, "Indian hemp" (Ibn al-Baitar, 1985).

Type specimen

Lamarck's type specimen of C. indica is deposited at the Museum National d'Histoire Naturelle in Paris (herb. P). It consists of the uppermost 30 cm of a flowering, seedless pistillate plant. Lamarck's specimen shows more compact branching with shorter internodes than Linnaeus's specimen. Branching density may reflect differences in cultivation: Lamarck's specimen was presumably open-grown, and Linnaeus's specimen grown in typically dense hemp fields. However, the effects of sowing density upon branching density are minimal in the uppermost 30 cm of a flowering top. Leaves branch alternately from the stalk, palmately compound, medium green, mostly with three leaflets, and short petioles. Central leaflets are narrowly linear-lanceolate, acuminate, with sharp serrations, 55-58 x 5-7 mm. Inflorescence are somewhat compact; subtending floral leaves have an abundant covering of capitate-sessile glandular trichomes; perigonal bracts express a moderate density of capitate-stalked glandular trichomes. Styles and stigmas are prominent, agglutinized with trichome exudate, and light brown. The type specimen is a sample of sinsemilla, lacking fruits.

No type location is given. Lamarck (1785) wrote, "This plant, which Mr. Sonnerat gave us pieces he brought back from India..." According to Schultes et al. (1974), "we are at a loss to indicate a definite area, partly because of vagueness of geographical terminology in that period." In fact, we know when and where Pierre Sonnerat made his collections. He explored India and China between 1774 and 1781. In India he made extensive collections around Pondicherry (Ly-Tio-Fane, 1976), so Sonnerat likely collected C. indica near Pondicherry. Unfortunately he did not mention Cannabis in his travelogue (Sonnerat, 1782).

Discussion

Lamarck erroneously described C. indica with "alternately branching leaves" and C. sativa with opposite branches (i.e., decussate, the succeeding pairs turned 180[degrees]). In fact, both C. indica and C. sativa do both--opposite branching during vegetative growth, switching to alternate branching during flowering. Lamarck may have erred because the specimen he received from Sonnerat was a flowering top, with alternate branching. Lamarck cited authors who illustrations of Asian Cannabis also depicted flowering tops, with alternate branching habits (Acosta 1619, Rheede 1690, Rumpf 1747). Interestingly, the same year that Lamarck (1785) described C. indica, his coworker Andre Thouin was growing Chinese hemp. Thouin (1785) described chanvre de Chine with alternate branching.

Note that we cite 1785 as the year that Lamarck coined C. indica. See Breistroffer (1948) for evidence that the commonly cited date of 1783 is inapplicable. Each volume of Encyclopedie Methodique was printed in two parts; the second part of each was printed later than the date on the title page. We use the date specified by Stafleu and Cowan (1979).

Appendix 1c. Cannabis sativa var. spontanea Vav. Diagnosis or description

Vavilov (1922) collected wild-type germplasm near Saratov, Samara, Astrakhan, and Tsaritsyn (Volograd). "The study of this hemp in our laboratory by Varvara F. Antropova compels one to consider it to be. without doubt, wild." He described a series of forms that transition from the cultivated variety to the wild-type variety, "differing in the coloration of the seeds and in the size and form."

Plants at the wild end of the spectrum expressed anthocyanin in their stalks, and produced seeds that were dull (not shiny), elongated (not rounded), and smaller than seed from cultivated plants. Seed color ranged from light or white forms with a mosaic, to dark gray and light brown with marbling.

Vavilov provided a brief diagnosis, translated from Russian: "At the bases of the seeds there are formations that resemble 'horseshoes' (analogous to wild oats), along which there occurs a breaking off and a shedding of seeds at maturation. Frequently this horseshoe is clearly defined and undoubtedly is a morphological and biological feature clearly distinguishing it from the cultivated form. At maturation, the wild variety with the horseshoe is easily distinguishable fro the ordinary cultivated variety by the shedding of the seeds which have not yet reached full maturity. As was mentioned by Professor D. E. Janischevsky, wild forms of hemp appear primarily as dark-seeded marbled forms."

Synonymy and references

Vavilov (1922) cited no synonyms. He apparently overlooked Czernajew (1859), who assigned the name C. sativa var. spontanea to wild-type plants near Kharkiv, Ukraine. Czeraajew's taxon has no standing, because he did not describe the variety, and therefore did not meet a basic provision of the ICN (Small & Cronquist, 1976). Vavilov mentioned earlier work on wild hemp by Janischevsky, but did not cite a publication.

Type specimen

Several specimens labeled C. sativa var. spontanea are stored in Vavilov's herbarium at WIR. Small and Cronquist (1976) chose one as the lectotype, specimen Antropova 121. The label states the plant was grown in 1925 at the Kamenno-Stepnaya experiment station in Voronezh, from seeds collected near Saratov in 1921, by Vavilov's assistant, Varvara F. Antropova.

The specimen consists of the top 42 cm of what appears to be a large plant, with internode spacing similar to Linnaeus's type specimen. Leaves with 3-5 leaflets, petioles short, leaflets narrow lanceolate, up to 130 x 10 mm. Inflorescences are loose; subtending floral leaves have a sparse covering of capitate-sessile glandular trichomes; perigonal bracts have relatively few capitate-stalked glandular trichomes and many cystolith trichomes. Achenes are medium-sized (3.8-4.0 mm long), oblong in outline, pale green with a fine reticulated pattern overlaid by irregular dark marbling, and a weakly protuberant base.

Discussion

Vavilov (1926) debated whether C. sativa var. spontanea was truly wild, or a spontaneous escape of formerly cultivated plants. This question was also raised by Janischevsky regarding Cannabis ruderalis (see below). Both botanists were unaware that this debate arose earlier, regarding plants in the same location--Saratov. Three naturalists travelling together in 1768 encountered wild-type plants about 10 km downriver from Saratov. Lepechin (1774) said the plants did not differ from cultivated plants. He considered them feral escapes, sown by former inhabitants. "This Indian plant species cannot be native here." Nearby lay the ruins of Uvek, a trading center of the Kipchak Khanate, destroyed by Tirnur in 1395. Pallas (1793) said the wild-type hemp looked like cultivated plants, which he attributed to former inhabitants. Falck (1786) wrote, "On the Volga one finds the wild hemp especially on the sites of former cities." He noted branchiness in the wildtype plants, "These give no straight and uniform fibers."

Vavilov and Janischevsky both decided that plants around Saratov were truly wild. Small (1975a) throws a variable into the debate. He discovered that domesticated Cannabis reverted to a wild-type phenotype within 50 generations (years) of prohibition in Canada. This plasticity makes it difficult to distinguish truly wild plants from formerly cultivated plants that have reverted to wild-type phenotypes. Doebley et al. (2006) also emphasized that domesticated C. sativa easily escapes cultivation and reverts to a wild-type phenotype. Small and Cronquist (1976) suggested that truly indigenous, never-domesticated, wild-type Cannabis may be extinct. "If unaltered wild populations exist (which we doubt) they cannot be clearly distinguished from those contaminated by the influence of domestication."

Was there any reproductive isolation between wild-type and cultivated plants? Their geographic distributions overlapped (sympatry). Hybridization and introgression was limited by temporal (allochronic) isolation--Janischevsky noted that ruderalis matured in mid-June, while cultivars were still in the vegetative stage. There may have been some ecological inviability as well--a condition where hybrid offspring are normal but suffer lower viability because they cannot find an appropriate ecological niche. However, Vavilov and Janischevsky noted intermediate forms, which suggested some hybridization occurred between the populations.

Appendix 1d. Cannabis ruderalis Janisch.

Janischevsky (1924) coined the species name C. ruderalis, but added parenthetically an alternative taxonomic rank: C. sativa var. ruderalis. "I am inclined to consider it a well marked variety." We provide key details of his large protologue--a 13 page article.

Diagnosis or description

Translated from Latin: "Fruits rather small, rather hard, narrowly ovate, base attenuate, perianth marbled-spotted, persistent and enclosing [the fruit] at maturity, [the fruit] quickly dropping off [the plant]."

In addition to the Latin diagnosis, Janischevsky provided additional characters: Male flower produced shorter perianths and anthers than those in cultivated plants. Average seed size was 3.5 mm long x 2.5 mm wide, and rarely reached 4.5 x 3.0 mm. The female flower's perianth was persistent and stuck to the surface of the seed--not unlike hops (Hamulus lupulus). The seed had an elongated base in the form of a short pedicle. Within the pedicle Janischevsky detected cells with oily inclusions--so he considered the structure an elaiosome--an oil-rich body that attracts insects, which acts as a seed dispersal agent.

Vegetative characters included relatively short height, usually 0.7-1.1 m but up to 2.1 m, with a strongly branched habitus. Stalks were usually ribbed, with thick xylem at the base (i.e., woody), and with the upper stalk colored by anthocyanin. Leaves had 5-7 leaflets, colored deep green on the top side, and gray-white on the underside due to cystolith trichomes.

Janischevsky conducted common garden experiments, which showed that wild-type plants matured more rapidly than cultivars. They came into flower mid-June, and first seeds were collected July 10th (while cultivars were still in vegetative stage). Wild-type plants compared to cultivars showed greater drought tolerance, and more shade tolerance in forested areas. Wild-type seeds readily disarticulated from plants. The seeds demonstrated a prolonged period of dormancy and slow germination, whereas seeds of cultivated hemp had no period of dormancy.

Janischevsky described mutualism between wild hemp and an insect, Pyrrhocoris apterus. The insect sucked oil out of the elaiosome. The rest of the seed was left intact and capable of germination. In the process of feeding, the bug carried the seed "far distances," and facilitated the spread of wild hemp. The following year, Janischevsky (1925) wrote a whole article about wild hemp and P. apterus.

Synonymy and references

Janischevsky did not list any explicit synonyms under C. ruderalis. He did not mention C. sativa var. spontanea Czernajew (1859), or C. sativa var. spontanea Vavilov (1922). He noted that taxa other than C. sativa were coined by other Russian botanists, such as Messerschmidt (in Amman, 1739), Sievers (1796), Ledebour (1847,-49), and Korshinskii (1898). Yet others suggested that C. sativa, of Asiatic origin, may also be indigenous to Europe--but they expressed this opinion with great caution. Janischevsky took five pages to recount observations by 22 authors: Erndtel, 1730, Messerschmidt (in Amman, 1739), Sievers, 1796, Rochel, 1835, Claus, 1838, Ledebour (1847-49), Christison, 1850, de Candolle, 1855, Becker, 1858, Heuffel, 1858, Dukerley 1866, de Candolle 1869, Kanitz, 1881, Zinger, 1885, Shmal'gauzen, 1897, Korshinskii, 1898, Velenovsky 1898, Prain, 1904, Adamovic, 1907, Bogdan, 1908, Ascherson & Graebner, 1911, and Vavilov 1922.

Type specimen and illustrations

Janischevsky's lectotype specimen of C. sativa var. ruderalis, collected near Saratov, was stored at the Komarov herbarium (LE) in St. Petersburg (Small & Cronquist 1976). It may be lost (McP, pers. observ., St. Petersburg, 2010), and no suitable isolectotype was identified at LE. Small (1975b) provided a photograph of the lectotype.

Janischevsky provided two plates of line drawings, reproduced here as third-generation photocopies (Fig. 6, figure legend translated from Russian).

[phrase omitted]. 1. A fruit of hemp collected in the vicinity of Saratov (Dudakov ravine).

[phrase omitted]. 2. Two diagrammatic drawings of the longitudinal section of the fruits. [phrase omitted]. 2a. A section in the plane that goes through the edge of the fruit. [phrase omitted]. 2b. A section in the plane that goes between the edges of the fruit. I- perianth; II- pericarp, e- epicarp, E-endocarp, 5- point of insertion of perianth, 6-receptical transformed into elaiosome which juts out into the space among the carpels (see diagram B) in the form of rounded mases of tissue, v- vascular bundle.

[phrase omitted]. 3. A bug Pyrrhocoris apterus on a Carex leaf carrying a hemp fruit.

Discussion

Janischevsky (1924) said he found hemp growing in "wild circumstances" in 1897, near Buzuluk (Orenburg Oblast). It flourished along the Tok River, a right tributary of the Samara, in Bashkir tribal land where hemp was not cultivated. Janischevsky added that he began growing specimens of wild hemp in the botanical garden at Saratov University in 1914. Vavilov arrived at Saratov University in 1917, joining his senior colleague. Janischevsky and Vavilov took field trips together down the Volga (Korotkova, 1978). It seems likely that Janischevsky pointed Vavilov's attention to wild hemp. In Vavilov's archives, the subject of wild hemp first appeared in a 1920 letter to his assistant Evdokia A. Teplykh, "Collect wild or feral hemp on the borders and the ravines near Saratov from selected plants, at least 500 plants, in separate bags. Keep in mind that wild hemp seed falls off easily, so it must be carefully collected" (Korotkova, 1978).

Vavilov (1926) elaborated upon C. sativa var. spontanea. His review of the literature borrowed from Janischevsky (1924) in a few plagiarized sentences. Vavilov cited six of Janischevsky's 22 references (Erndtel, 1730, Ledebour, 1847-49, Korshinskii, 1898, Velenovsky, 1898, Adamovic, 1907, Bogdan, 1908). However, Vavilov added information about wild-type hemp from Mak & Regel, 1862, Boissier 1879, Hooker, 1890, Britton 1899, Dimo & Keller, 1907, Semenov (in Krylov, 1909), Knorring and Minkvitz Knorring & Minkvits, 1912, Vysotsky, 1915, Oganovsky, 1922, Sinskaya 1925, and Khrebtov, 1925.

Vavilov (1926) details work on wild-type hemp by his assistant Tatiana Ya. Serebriakova. She compared germplasm collected by Antropova in Saratov with germplasm collected by Eugeniya N. Sinskaya in the Altai (Sinskaya, 1925). Plants from both accessions grew 60-150 cm tall, with moderately thick stalks that were strongly branched. Leaves were medium sized, with 5-9 narrow leaflets. Seeds were small (2.7-3.0 mm long), dark, orbicular-elongated in shape, with horseshoes and a persistent, marbled perianth. Plants matured before cultivated plants, seeds rapidly dehisced from plants, and seed germination was usually slow and unequal.

Vavilov (1931) extended the range of C. sativa var. spontanea to Central Asia. While traversing the Tian Shan to Lake Issyk Kul via the Bedel Pass, he wrote, "Cannabis sativa var. spontanea is a very common plant in northern Tian Shan, especially on its north-facing slopes and valley." Herbarium specimens collected on the north-facing slopes of the Tian Shan look very different than Vavilov's type specimen (shorter, with more branches, and broad oblanceolate leaflets). Zhukovsky (1962) proposed that C. ruderalis had not been sufficiently explored in Central Asia, and some populations may be undescribed forms.

Lastly we come to the question of priority. Vavilov (1922) scooped his senior collegue by coining C. sativa var. spontanea. Janischevsky (1924) erected another Latin name for the same wild-type hemp growing near Saratov. The taxonomic name became a point of contention between the two authors: Janischevsky politely mentioned Vavilov's research, but always used the epithet ruderalis (Janischevsky, 1924, Janischevsky, 1925). Vavilov politely mentioned Janischevsky's work, but always used spontanea (Vavilov, 1926, 1931; Vavilov & Bukinich, 1929).

Two taxonomic names that represent contaxic entities, based on different type specimens, are facultative synonyms. Vavilov's earlier epithet has priority at the rank of variety. Janischevsky's taxon has priority at the rank of species.

Since then, botanists have altered the ranks of spontanea and ruderalis. Serebriakova and Sizov (1940) elevated spontanea from a variety to a subspecies. The subspecies rank has been adopted by several authors (e.g., Bocsa and Karus Bocsa & Karus, 1997; Hanelt, 2001; McPartland & Guy, 2004, Clarke & Merlin, 2013). Chu (1959) reduced ruderalis to a sub-varietal form, as C. sativa f. ruderalis. Liou (1988) brought Chu's taxon back to a variety, C. sativa var. ruderalis. Liou mistakenly believed he coined a var. novo. Sojak (1960) used Janischevsky's taxon to describe hybrids between wild hemp and cultivated hemp, which he named X C. intersita. He later changed the taxon to C. sativa subsp. intersita (Sojak, 1980).

A troika of influential Soviet texts set precedence by choosing C. ruderalis over C. sativa var. spontanea: Nekrasova (1934), Yarmolenko (1936), and Mal'tsev (1939). Soviet science at that time writhed under the rise of T. D. Lysenko. Lysenko became the pet scientist of Joseph Stalin. He fabricated genetic theories using the rhetoric of Marx and Michurin, and methodically annihilated his academic opponents. Lysenko labeled Vavilov a Trotskyite, which led to Vavilov's arrest (Popovsky, 1984). After Vavilov was arrested, his assistant Tatiana Serebriakova coauthored her final Cannabis paper with Ivan A. Sizov. He was a Lysenkoite who "began energetically to liquidate the remnants of Vavilov traditions" (Medvedev, 1969). Serebriakova and Sizov (1940) elevated Vavilov's taxon from a variety to a subspecies, but without his name in the basionym: C. sativa subsp. spontanea Serebriakova. C. ruderalis was synonymized under that taxon.

Schultes et al. (1974) treated C. ruderalis as a species separate from C. sativa. They expanded Janischevsky's taxon to Central Asia, and erroneously typified it with a specimen from Tajikistan. Furthermore they described ruderalis as a very short, unbranched plant with broad leaflets. This departs from the concepts of Vavilov and Janischevsky. Schultes et al. (1974) cited Schultes, and described ruderalis as a short plant. Anderson (1980) cited Schultes, and described ruderalis as a short plant with broad, oblanceolate leaflets.

Small and Cronquist (1976) kept Vavilov's taxon at the rank of variety. They recombined it as C. sativa ssp. sativa var. spontanea, typified by a Vavilov specimen from Saratov. They synonymized C. ruderalis under that taxon. They extended the range of spontanea to wild plants from Central Asia.

Schoenmakers (1986) introduced "Ruderalis" to underground Cannabis breeders. He collected germplasm near the Hungary-Ukraine border. His photos of "roadside ruderalis" illustrated an escape from cultivation, and not a wildtype plant. "The effect after smoking was stoney, but not high." Other Cannabis breeders assigned the name "ruderalis" to feral plants in North America--obviously escapes from cultivation, and not wild, indigenous plants (e.g., Panik, 2012. Frank (1988) stated that potent, psychoactive "Ruderalis" invariably turned out to be misidentified "Indica." This confusion persists: a 2013 web video about "Charlotte's Web" by CNN medical correspondent Sanjay Gupta portrayed "Ruderalis" plants that clearly have Afghanistan heritage.

Appendix 1e. Cannabis sativa f. afghanica Vav.

Vavilov encountered wild and weedy plants in Afghanistan. First he described C. sativa f. afghanica (Vavilov, 1926). His description is transcribed below, where we combine the best of two English translations (Vavilov, 1926, 1992):

Diagnosis or description

"We observed wild hemp ... in districts where hemp cultivation is entirely unknown. Belts of black hemp follow the sowings of corn and other cereals along the Kunar River (on the border between Afghanistan and India [now Pakistan]) from Chekosarai to Jalalabad, a distance of 160-200 km. In between Chekosarai and Jalalabad we discovered among the wild hemp a peculiar race with light-coloured, small seeds, and with a thin perianth easily taken away (f. afganica Vav.). The seeds of this race were very small (1000 seeds weighed 2.1-2.7 g), ten times smaller than the large-fruited races of the Far East (1000 seeds 26.0 g), the common Central Russian races (Orel, Kurst) show a weight of 17-19 g.

"The wild hemp collected on the Kunar River approached the cultivated type with respect to seed color and the slightly splitting pericarp, but is distinguished by readily shedding its seeds and in the development of "horse-shoes." When sown, the seeds germinate very slowly and unequally, i.e., the plants show features of a typical wild plant. The wild hemp displayed other new characteristics. The leaflets of these plants were distinguished their obovate naiTow shape, not observed by us among the European, Siberian and Turkestani forms... The wild Afghani races found along the frontier with Pakistan, with light-colored and easily splitting pericarps, have spread into Pakistan as well. The plants constitute a morphological link between the wild and the cultivated races of hemp with respect to the most important differentiating characteristics."

In an accompanying table, Vavilov provided results of a common-garden experiment of C. sativa f. afghanica by his assistant Serebriakova. Plants matured late in the season, and seed germination was slow and unequal. Plants grew 60-150 cm tall, with moderately thick stalks, and strongly branched. Leaves were small, with 5-9 leaflets, and narrowly obovate in shape. Seed was described in an either-or duality: Seed size was either small (2.7-3.0 mm) or medium (3.0-4.0 mm), seed color was either dark or light, seed shape was either orbicular-elongate or orbicular, the seed perianth was either persistant or easily removed, the seed base either with or without a horseshoe. Vavilov seemed to be describing two kinds of plants. He wrote, "the plants show features of a typical wild plant," followed by "the plants constitute a morphological link between the wild and the cultivated races of hemp."

Synonymy and references

Vavilov provided no synonymy and cited no references. Type specimen

No specimen labeled afghanica is deposited in Vavilov's herbarium at WIR. Serebriakova grew germplasm of Afghan provenance at the Kamenno-Stepnaya Experiment Station (Voronezh Oblast); these herbarium specimens are labelled C. sativa var. spontanea, and annotated "like aiderai" (WIR specimens 4031,4032,4034,4036,4038,4044,4046). All are immature, without seeds, and could be either afghanica or kafirstanica.

Discussion

The either-or duality in Vavilov (1926) got sorted 3 years later, when Vavilov and Bukinich (1929) named a second taxon of Afghan plants: C. indica var. kafirstanica. The either-or descriptions in Vavilov (1926) referred to either afghanica or kafirstanica. Vavilov and Bukinich described kafirstanica as truly wild, with tiny achenes that were dark-colored and marbled, with an elaiosome. They described and illustrated C. indica f. afghanica, with larger achenes that were light colored ("white"), and a colorless involcre (perianth?), with little or no "horseshoe" (Fig. 7). Vavilov and Bukinich considered afghanica a "specialized form" of kafirstanica, "transitional" between wild kafiristanica and cultivated C. indica. Their nomenclature was not consistent--they used C. indica var. afghanica on page 380 (see caption in Fig. 7), f. afghanica on page 381, and C. indica var. kafirstanica f. afghanica on page 382. Small and Cronquist (1976) argue that the caption (Fig. 7) erroneously reversed the ranks of two taxa, Cannabis indica f. kafiristanica and C. indica var. afghanica, so they are typographical errors.

We propose that Vavilov erred by describing afghanica as "transitional" between wild and cultivated plants. The afghanica was probably domesticated--a feral escape, or recently naturalized. Its seed lacked a "horseshoe" (elongated base in the form of a short pedicle), and lacked a persistent perianth. It resembled a small version of the Afghani "cultivated form" (Fig. 7). The size of the cultivated seed would have been augmented by irrigation and fertilizer. Vavilov and Bukinich described afghanica growing in "abandoned lots and neglected plots of land, in fertilized agricultural soil, and between agricultural fields." Arable land in Afghanistan is rarely abandoned and neglected.

Emboden (1974) assigned a varietal rank to the taxon, as C. indica var. afghanica. He gave seed size as 2.8 x 1.9 mm, without stating the provenance of his material. Small and Cronquist (1976) synonymized C. sativa f. afghanica Vav. under Lamark's taxon--a domesticated variety. Vavilov's taxon at the rank of species, as C. afghanica, was employed by McPartland (1996), McPartland et al. (2000), and Clarke and Watson (2002). Clarke (1998) used a varietal rank, C. indica var. afghanica. The taxon C. sativa var. afghan appeared in a U.S. patent (No. 6,403,530). Cervantes (2006) offered two ranks, C. afghanica and C. sativa var. afghanica. A subspecies rank, C. indica subsp. afghanica, was employed by McPartland and Hillig (2004) and Clarke and Merlin (2013). Recently the species rank, C. afghanica, has been applied by others (Tennstedt & Saint, 2009, Brownjohn & Ashton, 2012, Macedo et al., 2013, Henry, 2015, Laursen, 2015).

Appendix 1 f. Cannabis indica var. kafiristanica Vav.

Diagnosis or description

The description by Vavilov and Bukinich (1929) is translated from Russian: "Races of wild hemp in eastern Afghanistan have extremely small fruits with mosaic (1000 fruits weigh 2.1-2.7 g), i.e., 6-8 times smaller than small-seeded Central Russian cultivated hemp (Orel and Kursk hemp weighs 17-19 g). Characteristic for them is ready shattering of fruits due to the presence of a horseshoe, slow and uneven germination, i.e., the usual attributes of a wild plant. As regards to vegetative features, Afghan wild-weedy hemp is distinguished by small leaves with obovate leaflets of narrowed shape. In general, it is characterized by short stature, profuse branching from the first internode, and by short internodes."

Vavilov and Bukinich also mention its early ripening (90-100 days in Voronezh Oblast). They provided a drawing of the seed (Fig. 8). Although Vavilov and Bukinich described kafiristanica plants as short in stature, a photograph of plants identified as C. indica var. kafirstanica (Fig. 267 in Vavilov and Bukinich) shows plants that were equal in height to maize plants with tassels.

Synonymy and references

Vavilov provided no synonymy and cited no references. Type specimen

Several specimens labeled C. sativa var. kafiristanica are deposited in Vavilov's herbarium at WIR in St. Petersburg. Small and Cronquist (1976) chose one as the lectotype: WIR 3952, germplasm collected by Vavilov at Chekhosarai (now Asadabad) in 1924 and cultivated in 1927 at Pushkin Experiment Station (Detskoye Selo, St. Petersburg). A photograph of the lectotype appeared in Vavilov and Bukinich (1929), and appears here (Fig. 8). The entire plant is mounted on the herbarium sheet, about 30 cm tall. It is an immature pistillate plant, with tight internode spacing; nine pairs of opposite branches and only three alternate branches near the apex. Leaves with 5-7 overlapping leaflets, petioles long and thick, leaflets broad, oblanceolate, dark green, with coarse serrations, up to 46 x 18 mm. The inflorescences are immature but nevertheless compact and leafy, with an abundant covering of capitate-sessile glandular trichomes.

Discussion

Vavilov said afghanica and kafirstanica grew in the Kunar River valley--the border between Afghanistan and Pakistan--between Chighasaray (now Asadabad) and Jalalabad. We note a geographical contradiction: The Kunar River valley is not part of Kaflristan (present-day Nuristan Province), it lies in Kunar Province, populated by Pushtan Afghanis, not ethnic Kafirs. The place where Vavilov collected kafirstanica was not in Kafiristan.

Serebriakova and Sizov (1940) made no mention of afghanica and kafirstanica; they placed drug plants from Afghanistan in the taxon C. sativa subsp. culta prol. Asiatica var. narcotica. Emboden (1974) gave seed size of C. indica var. kafiristanica as 3.0 x 2.2 mm (larger than var. afghanica), without stating the provenance of his material.

Small and Cronquist (1976) recombined Vavilov's taxon as C. sativa subsp. indica var. kafiristanica. They considered it the wild-type associate of domesticated C. sativa subsp. indica var. indica. As such, they expanded the taxon's concept beyond Afghanistan to wild-type plants from India, Nepal, China, South Africa, and Colombia. Hillig and Mahlberg (2004) also extended kafiristanica beyond Afghanistan to feral populations from India and Nepal. The rank of kafiristanica has bounced around a bit, like that of afghanica. Chrtek (1981) elevated it to a species rank, C. kafiristanica. A subspecies rank, C. indica subsp. kafiristanica, was employed by McPartland and Guy (2004) and Clarke and Merlin (2013).

Appendix 2: Taxonomic bias and personality cults surrounding Linnaeus and Lamarck in the 18th--19th centuries

Carl Linnaeus (1707-1778) is the most famous naturalist of all time. "Linnaeus became the subject of hero worship after his death to an extent previously unknown in botany" (Stafleu, 1971a). Linnaeus's impact on biological thought and his renown among peers is difficult to convey today (Blunt, 2001). Linnaeus's four-point "revolution" developed in stages: the sexual system (Linnaeus, 1735), hierarchical taxonomic ranks (Linnaeus, 1735), generic reform as a set of theoretical axioms (Linnaeus, 1737a, and their practical application Linnaeus (1737b), and lastly binomial nomenclature (Linnaeus, 1753).

Linnaeus's genius was soon recognized. He became a Full Professor at age 34. The King of Sweden knighted him at age 46. A generation of devoted students trained under Linnaeus, and he served as supervisor ("praeses") for 186 Uppsala doctorates. Seventeen of his most committed scholars became known as the "apostles." Thanks to Linnaeus's connections with the Swedish East India Company, his apostles explored the world and spread Linnaean taxonomy. Seven apostles died on expedition. Five wrote about Cannabis (Hasselquist, Forsskal, Falk, Sparrman, Thunberg).

Linnaeus's innovations competed with other taxonomic systems at that time, by Ray, Morison, Rivinus, Tournefort, Herman, Boerhaave, Ludwig, and Magnol. The Linnaean system was embraced quickly in Holland (where he published 14 of his early works), and of course Sweden. Next came Great Britain. English literature soon dominated botany--particularly concerning Cannabis in India--so the reasons why British botanists became the staunchest supporters of Linnaeus are worth reviewing:

Linnaeus visited England in 1736, and impressed four leading botanists--Hans Sloane, Philip Miller, Peter Collinson, and John Dillenius. Dillenius (1741) introduced Linnaeus's work to English literature. Collinson organized the election of Linnaeus as a Fellow of the Royal Society in 1754. He asked Linnaeus to send an apostle to London; Linnaeus sent Daniel Solander, who gained a post at the British Museum. Solander soon proselytized Joseph Banks, and they botanized together with James Cook on the Endeavour.

Stillingfleet (1759) translated into English six essays from Linnaeus's "unrivalled school of natural history." Coxe (1811) referred to Stillingfleet as "one of the bodyguards of Linnaeus." Stillingfleet encouraged Hudson (1762) to organize Flora Anglica along Linnaean lines, which "marks the establishment of Linnean principles of botany in England" (Smith, 1824). Philip Miller, the influential author of Gardeners Dictionary and keeper of the Chelsea Physic Garden, announced that he "adopted in a great measure the system of Linnaeus" (Miller, 1768). James Edward Smith founded the Linnaean Society of London in 1788. Four years earlier, Smith had purchased Linnaeus's herbarium and library from his widow. Smith (1821) published a tome of Linnaeus's correspondence, and cemented London as the center of Linnaean studies.

The anti-Linnaeans

Stafleu (1971a) states that Linnaeus's authoritative pragmatism appealed strongly to the practical and bourgeois British, whereas French philosopher-naturalists, under sway of the Enlightenment, considered Linnaeus an authoritarian of the past.

Comte de Buffon (1707-1788) was a French naturalist and a proponent of the Enlightenment. Buffon became Linnaeus's primary scientific rival. He criticized three aspects of Linnaeus's four-point revolution. Buffon mocked Linnaeus's sexual system for being artificial. He sharply criticized Linnaeus for overthrowing Tournefort's generic reform based on arbitrary principles.

Linnaeus's hierarchical system of taxonomic ranks particularly rankled compte de Buffon (1749). He was under the influence of John Locke, an Enlightenment author, who argued against essentialism in favor of nominalism. Linnaeus's taxonomic system was essentialist to its core--he treated species as typological and immutable entities created by God. Buffon argued that we name a creature by its collection of observed qualities (nominalism), rather than classify a creature by its similarity to an eternal essence or prototype. Buffon repeated the argument in Locke (1690) that individuals can be observed, but "species" and "genera" are unobservable abstractions, unless they consist of a single individual.

Buffon clashed with Linnaeus over "species concepts"--an argument that continues today regarding Cannabis. Linnaeus saw sharp-cut delineations between species. Buffon argued that "Nature progresses by unknown gradations," and organisms were "not tied up in neat and orderly parcels." compte de Buffon (1749) asserted, "In Nature there actually exist only individuals; genera and orders and classes exist only in our imaginations." Subsequently, compte de Buffon (1753) recognized species, as a group that could interbreed, "a constant succession of similar individuals that can reproduce together." This concept makes him the founder of the biological species concept, usually attributed to Mayr (1942).

Jean-Baptiste Lamarck (1744-1829) was a protege of Buffon. Lamarck's supporters hailed him as "the French Linnaeus." He deviated from Linnaean orthodoxy in many ways. Lamarck (1778) published a flora that departed from Linnaeus's approach in two ways--it was written in vernacular French instead of Latin, and it used dichotomous keys for plant identification. Subsequently, Lamarck (1783) launched a new format for writing flora texts. He devised the new format as an alternative to the telegraphic Linnaean style. The format remains in use today (Frodin, 2001).

Lamarck criticized three aspects of Linnaeus's four-point revolution. Lamarck (1783) critiqued Linnaeus's systeme sexuel as defective. Lamarck (1788) presented a lengthy critique of Linnaeus's generic reform, "the so-called axioms and extremely laconic maxims with which he filled his Philosophia botanica and Critica botanica, rather than by solid proof which alone could convince those who were not impressed by mere authority." Lamarck (1778) repeated Buffon's nominalist stance that all hierarchical ranks above species were subjective creations of the human mind. He argued that the local European flora was too riddled with species gaps to enable a valid perception of higher ranks. Lamarck (1791) again asserted that higher ranks (Class, Family, Genera) were surely not the work of Nature, but artificial, the result of arbitrary human judgment. Lamarck (1792) enlarged upon this critique as a response to pushback from Linnaeans.

Lamarck's theory of evolution totally alienated Linnaeans. Lamarck (1809) recognized evolution as a gradual process. This made it difficult to find well-established, concrete lines of separation between taxonomic groups. In contrast, Linnaeus treated species as entities with fixed forms given to them by God. "Every genus is natural, created as such in the beginning, hence not to be rashly split up or stuck together by whim or according to anyone's theory" (Linnaeus, 1735). "We count as many species as there were forms created in the beginning" (Linnaeus, 1751). This dispute continues to echo in the modern quarrel between creationists and evolutionists.

The anti-Lamarckians

Despite Lamarck's departures from Linnaean orthodoxy, he praised Linnaeus as the greatest botanist in history. Late in his career he even regarded Linnaeus's artificial classification system as a useful device for identifying plants (Lamarck & Mirbel, 1803). Nevertheless, Lamarck's criticisms "were neither forgotten nor forgiven" by other botanists (Williams, 2001). "Those who had enjoyed Buffon's support and patronage, and those who accepted his model of natural history, underwent several institutional setbacks and bore the brunt of a massive theoretical offensive" (Corsi, 1988).

In Lamarck among the Anglos, Hull (1984) wrote about Lamarck's critics. "Few British or American scientists got their views of Lamarck by reading translations of Lamarck, let alone Lamarck's original works in French. In most instances, Lamarck's reputation was formed by descriptions of his views in secondary sources." Primary among those secondary sources was Georges Cuvier, an opponent of Buffon. Cuvier (1836) wrote a biting, ironic eulogy of Lamarck that was translated into English.

Carl Ludwig Willendow, a disciple of Linnaeus, updated Species Plantarum after Linnaeus died. Willendow did his best to dismantle Lamarckian taxonomy and nomenclature. A perusal of volume one (in two parts) reveals that Willdenow accepted 55 of Lamarck's taxa, but rejected 61 as synonyms. Willdenow synonymized Lamarck's taxa for the flimsiest reasons. Sometimes he just annotated a question mark after them (e.g., Lobelia nummularia). Willdenow reduced Coffea mauritiana to a variety of Coffea arabica, "it seems to me hardly different." He rejected several Eriocaulon species because they weren't illustrated. He rejected Fagara heterophylla because "it seems kind of mixed." He rejected Jasione perennis because it was "an imperfectly dried specimen."

Willdenow (1805) rejected Lamarck's C. indica on one morphological character--Lamarck described C. indica with alternate branching. Because C. sativa also showed alternate branching, Willdenow argued no differences existed between them. He ignored Lamarck's other morphological and phytochemical differences. Willdenow found one distinction in C. indica, "leaflets have a more tapered base, which is known to be very inconsistent." Willdenow incorporated C. indica into C. sativa, rather than name it a separate variety.

Willdenow's six-volume Species Plantarum was the most influential botanical work of its day, although it came under "severe criticisms for many manifest errors" (Long, 1843). Wight and Walker-Arnott (1834) initiated the process of "clearing up many doubtful synonyms in Willdenow," although they neglected C. indica. Botanists have reinstated nearly half of Willdenow's 61 rejected species names (as well as two genera,

Canthium and Nuxia), many reinstated as basionyms.

British botanists in India displayed a strong Linnaean bias. Their opinions were shaped by Johann Konig, a pupil of Linnaeus. Konig organized a botanical society in India, the "United Brotherhood," which included two influential British botanists, Fleming and Roxburgh. Fleming (1810) wrote, "Dela Marck [de Lamarck] is of the opinion that the Indian Ganja is a different species of Cannabis from the Cannabis sativa. But Willdenow assures us that ... he could not perceive any difference between them." Roxburgh (1832) confirmed, "I perfectly agree with Willdenow in thinking all the varieties, if even such they can be called, centre in one species." In Flora Indica, Hooker and Thomson (1855) wrote about "bhang and chirris" obtained from Cannabis sativa. "With regard to nomenclature, we shall not alter names established by Linnaeus." They degregate "hair-splitters," and criticize Lamarck's theory of evolution.

Lamarck's phytochemical character--C. indica caused intoxication--was dismissed by British botanists. Linnaeans adhered to Linnaeus (1751), who rejected phytochemical characters, such as fragrance and taste. Lacking knowledge of Mendelian inheritance, most Linnaeans believed that phytochemical traits depended entirely upon the environment--either climate or cultivation. Fiber-type plants "degenerated" into drug-type plants, and vice-versa, depending on how and where they were grown.

O'Shaughnessy (1838-1840) stated, "difference of climate seems to me more than sufficient to account for the absence of the resinous secretion, and consequent want of narcotic power ... the Cannabis sativa and Indica are identical." A cultivation argument was first put forward by Fleming (1801). He believed phenotypic variation was due to crop spacing--plants in Bengal were grown very far apart, often nine or ten feet, compared to closely-sown European hemp fields. Royle (1840) attributed differences between Indian hemp and European hemp to "openness of planting." The Indian method of growing plants 9-10 ft apart caused a loss in fiber softness and flexibility, and gave rise to "a full secretion of the principles."

Appendix 3: Details regarding alphanumerical sites in Fig. 2

Figure 2 illustrates the distribution of plants that field botanists in the 18th-19th centuries identified as C. sativa, C. indica, or other Cannabis species. Many more naturalists wrote about "hemp," but did not assign a Latin name to the plants.

Our narrative is divided in two parts: Part A. Plants assigned the name Cannabis sativa and segregates, and Part B. Plants assigned the name Cannabis indica and segregates. Within each part, the narrative is organized by floristic regions.

The map in Fig. 2 shows boundaries of ten floristic regions by Good (1964) and Takhtajan (1986): (1) Euro-Siberian region, west: (2) Euro-Siberian region, east; (3) Mediterranean region; (4) West and Central Asia (Irano-Turanian); (5) Sino-Japanese (East Asiatic); (6) African-Indian desert (Sahara-Arabian); (7) Sudano-Zambezian-Sindhia; (8) South Asia (Indian); (9) Continental Southeast Asia (Indochina). (10) Malayian (Malesian).

Part A . Cannabis sativa and segregates

(1) Euro-Siberian region, west:

Western Europe was blanketed by botanists who wrote scores of local floras. Many mentioned C. sativa growing wild, ruderal, or spontaneous. For this region, we present a geographic sample, rather than an exhaustive list. Early mentions include England (si. Hill, 1760), France and Switzerland (s2, Lamarck, 1785), Germany (s3, Willdenow, 1787), Bohemia (s4, Presl & Presel, 1819), Poland (s5, Wulff 1765), Hungary (s6, Heuffel, 1858), Galicia (s7, Zawadzki, 1835), Lithuania and Volhynia (s8, Eichwald. 1830), and the Moscow region (s9, Stephan, 1792).

Catherine the Great commissioned six physician-botanists to explore her new dominions--Pallas, Lepechin, Falck, Georgi, Gmelin, and Guldenstadt. Three of them studied under Linnaeaus (Lepechin, Falck. Georgi); Gmelin corresponded with him; Guldenstadt had no connection with him; and Pallas was anti-Linnaean--Pallas (1766) refuted Linnaeus's scala naturae, and Pallas (1774) laid out an animal classification meant to compete with Linnaeus's Systema Naturae. Guldenstadt and Pallas departed from Linnaean orthodoxy by coining new Cannabis species.

Pallas, Falck, and Lepechin wrote about wilder hanfnear Chetverosvyatsky monastery on the Volga, about 10 km downriver from Saratov (s10). A stone's throw from the monastery laid the ruins of Uvek, a trading center of the Tartars (i.e., Kipchak Khanate) until 1395. Pallas (1793) said wilder hanf looked like cultivated plants, and he attributed its presence to former inhabitants--the Tartars. Lepechin (1774) said the plants were feral escapes of crops sown by the Tartars. Falck (1786) assigned the plants to C. sativa, but noted a wild-type characteristic, "... only branched stems. These give no straight and uniform fibers."

Falck (1786) assigned C. sativa to feral plants along the Terek River in Northern Caucasus (s11). Georgi (1800) wrote of C. sativa, "We have indigenous or self-growing hemp in the Taurus mountains (s11), on the Terek (s11), along the Don, and the Dnieper in Novorossiya (s12)." Guldenstadt (1791) encountered wilder hanf in Ukraine and referred to it as "Cannabis" or a new name, Cannabis vulgaris (x1).

Russian exploration continued into the nineteenth century. Marschall von Bieberstein (1808) wrote a flora of the Caucasus and Crimea, and listed ruderal C. sativa, without naming a specific location (s13). Meyer (1831) reported C. sativa growing wild around villages below Mount Elbrus (s11). von Besser (1822) said C. sativa grew spontaneously near Kremenets in northwest Ukraine (s14).

Botanists started using variety names: Czemajew (1859) named wild hemp C. sativa var. spontanea, near Kharkiv in northeast Ukraine (s15). Lindemann (1881) applied Czernajew's taxon to wild hemp growing near Kherson (s12). Korshinskii (1898) applied C. sativa var. vulgaris to wild-type plants in southern Russia (s16). Vavilov and Janischevsky at Saratov (s10), assigned two taxa to the same population of wildtype plants: C. sativa var. spontanea (Vavilov, 1922) and C. sativa var. ruderalis (Janischevsky, 1924).

(2) Euro-Siberian region, east:

Daniel Messerschmidt and Johann Gmelin explored Siberia, 1720-1727 and 1733-1743, respectively. Messerschmidt, not a Linnaean, coined a prolix polynomial for plants in Transbaikal, east of Lake Baikal: "Cannabis erratica, montana, procera, daurica, folio minore semine lupidino similes, paruulo, guttato" (x2) (Amman, 1739). Gmelin (1768) was a Linnaean, and used Linnaeus's pre-1753 name, Cannabis foliis digitalis, for wild hemp between Krasnoyarsk and Irkutsk (s17).

Falck (1786) assigned C. sativa to feral plants in Bashkiria (s18). Georgi (1800) wrote of C. sativa, "We have indigenous or self-growing hemp ... in the Urals (s19), and the Ufa (s18), in Siberia between the rivers Yenisei and Irkutsk (s17)."

Pallas (1776) used Messerschmidt's polynomial for "a small wild hemp, which has a strange appearance" near Kyakhta (x2). Sievers (1796) assigned Cannabis erratica to wild-type plants growing in Transbaikal near Kyakhta (x2). Ledebour (1847-49) synonymized C. erratica by Messerschmidt and Sievers under a new varietal name, but tentatively, with a question mark: Cannabis sativa [beta]? davurica. Turczaninow (1856) synonymized Messerschmidt's taxon under C. sativa. Herder (1892) synonymized C. sativa (3 davurica and C. erratica under C. sativa.

von Ledebour et al. (1833) assigned C. sativa to wild-type plants growing along the Bukhtarma River in the eastern Kazakh steppe (s20) and along the Ulagan River in the Altai Mountains (s21). Nearly a century later, Sinskaya (1925) discovered a full spectrum of Cannabis morphologies in the Altai, from wild-type forms to fully domesticated plants (s21).

(3) Mediterranean region:

The headwaters region of the Po River in Italy is known as Piemonte (in Italian) and Piemont (in French). Lamarck (1785) described C. sativa as presque naturalisee in Piemont (s22). Other botanists assigned new names to a unique landrace in that region. D'Andrieux (1771) coined Cannabis sativa gigantea for chanvre de Piemont (x3). His son-in-law Vilmorin added cachet to chanvre du Piemont by giving it a new binomial name, C. maxima (x3) (Senac, 1826). Rey (1835) imported chanvre du Piemont from Carmagnola, and coined the taxon C. gigantea (x3). Vilmorin (1837) countered Rey's new binomial by coining his own, C. gigantea (x3). His son, Vilmorin (1892) assigned C. sativa excelsior to chanvre du Piemont (x3).

Elsewhere in Italy, Parlatore (1867) simply used C. sativa for feral hemp (s23). Velenovsky (1898) described spontaneous C. sativa in Bulgaria (s24). Across the Mediterranean in Algeria, Guyon (1842) wrote about hhachiche. He knew Lamarck's C. indica from the literature, but stated that the plants in Algeria were "none other than our common hemp, C. sativa" (s25). According to de Candolle (1869), Friedrich Noe, a German botanist working in Istanbul (s26), used the name Cannabis orientalis for plants in his herbarium collection, but did not publish the taxon. Noe's collaborator Boissier (1879) reduced C. orientalis (along with C. indica and C. chinensis) to a synonym of C. sativa.

(4) West and Central Asia (Irano-Turanian):

Samuel Gmelin corresponded with Linneaus, like his aforementioned uncle. He collected C. sativa near Lankaran and Astara (s27) in present-day Azerbaijan (Herder, 1892). Hohenacker (1838) also collected ruderal specimens of C. sativa in Azerbaijan, close to Lankaran and Astara on the border with Persia (s27).

Falck (1786) assigned C. sativa to feral plants in "Bukhara" (the closest he actually got to Bukhara was Orsk, s28) and "Soongaria" (a.k.a., Dzungaria--Falck's assistant Bardanes skirted the edge of Dzungaria in Semey, s29). Becker (1873) collected wild C. sativa near Kasumkent in Dagestan.

Chardin (1811), or rather his editor, assigned the taxon C. sativa to buen g plants in Isfahan, Persia (s30). Claus (1838) reported "abundant" C. sativa on islands dotting the Volga River delta (s31). Karelin and Kirilov (1841) assigned C. sativa to plants "in pratensibus adfl. Irtysch frequens [frequently in meadows near Irtysh River, s29], nec non in deserti Soongoro-Kirghisici [and certainly on the Kirghiz steppe, s32], arenosis ad lacum Noor-Saissan [growing on sand near Lake Zaysan, s29]."

Schrenk (in Trautvettero, 1867) collected C. sativa at three places in eastern Kazakhstan in 1840-1841: on Lake Alakol near the Dzungarian Gate (s32); the Kyskatsch mountains, between Lake Balkhash and Lake Zaysan (between s29 and s32); and near Khantau, between Lake Balkhash and Bishkek (s33). Griffith (1847) found Cannabis (no species name) at Jegdalek between Kabul and Jalalabad in Afghanistan (s34).

Basiner (1848) assigned C. sativa to a plant called kender in Khiva (s35). Bunge (1851) collected C. sativa near Kulagin on the Ural River, just north of the Caspian Sea (north of s31). Becker (in Herder, 1892) collected wild-type C. sativa along the lower Volga near Sarepta, Bogdo, Saratov, and Astrakhan (between s10 and s31). Semenov (1998) reported wild C. sativa growing near Kurmenty Pass northeast of Lake Issyk-Kul in 1857 (just east of s33). Seminov wasn't the best botanist--at herb. LE we saw a specimen he called "C. sativa" that was actually Humulus lupulus.

Valikhanov (1865) said hashish was extracted from C. sativa in Kasgar (s36). Shaw (1880) wrote a Turkic-English dictionary in Kasgar, and translated kaindir as the hemp plant, C. sativa (s36). Aitchison (1888) applied the name C. sativa to plants at Rui-Kauf in Persia (s37). Meyer (in USDA, 1912) collected C. sativa at Sanju oasis (s38), "a small-seeded variety of hemp ... used for seed oil and hashish made from the young tops."

(5) Sino-Japanese (East Asiatic)

Thunberg (1784), a student of Linnaeus, extended the C. sativa taxon to Nagasaki, Japan (s39). von Bunge (1833) found C. sativa growing "quasi-feral" in northern China (s40). Martius (1832) gave the name Cannabis sativa gigantea to plants growing 6 m tall in China. He did not give a location, but Canton (i.e., Guangzhou, s41) was the only Chinese port open to foreigners at that time. Bretschneider (1882), a Russian physician in Beijing (s42), assigned Chinese hemp to C. sativa.

(6) African-Indian desert (Saharo-Arabian)

Forsskal (1775), a student of Linneaus, assigned C. sativa to plants in Egypt (s43). Gastinel (1849) did not recognize C. indica as a species separate from C. sativa in Cairo (s43).

(7) Sudano-Zambezian-Sindhia

Griffith (1847) found "Cannabis" (no species name) in places that later became famous for charas'. DadurNala in Sindh (s44), and Burhan in Punjab (s45). Jacquemont (1861) assigned C. sativa to plants in Rajputana and Punjab (between s44 and s45). Aitchison (1864) described C. sativa in Punjab. Duthie (1898) reported wild C. sativa growing in three Chitral locations--Drosh. Dir, and Mirga (s46).

(8) South Asia (Indian)

Many botanists who knew Lamarck's taxon nevertheless adhered to the Linnaean party line, and applied C. sativa to plants throughout India--in Bengal (s47, Fischer, 1810, Roxburgh, 1832, Butter, 1839), in southern India (s48, Buchanan, 1807), and in the Himalaya (s49, Hardwicke, 1801, Royle, 1839, Hooker and Thomson, 1855). Wallich (1828-1849) applied C. sativa to plants all over South Asia--Calcutta (Bengal), Sudallapur (Kamataka), Bareilly (Uttar Pradesh), Hyderbad (Andhra Pradesh), and Kathmandu (Nepal).

(9) Continental Southeast Asia (Indochina)

de Loureiro (1790) assigned C. sativa to plants cultivated for fiber and drugs in "Cochinchina," southern Vietnam (s50). Wallich (1828-1849) collected C. sativa in the Toong Dong mountains near Innwa, Burma (s51). Griffith (1847) reported "C. sativa is found here" in Sassi (south of s51). Crevost (1917) coined the taxon Cannabis gigantea for plants grown for fiber and seed oil in the Tonkin highlands (x5).

(10) Malayian (Malesian)

Stickman (1754), a student of Linnaeus, assigned C. sativa to drug plants cultivated in the Moluccas islands, Indonesia (s52). Thunberg (1796), another student, wrote about C. sativa, known as ginje in Jakarta (3000 km west of s52).

Part B . Cannabis indica and segregates

(1) Euro-Siberian region, west

No plants native to this region were named C. indica by field botanists.

(2) Euro-Siberian region, east

No plants native to this region were named C. indica by field botanists.

(3) Mediterranean region

von Maltzan (1869) said hashish and kif in Algiers was made from C. indica (i1), whereas De Courtive (1848) and Dukerley (1866) equivocated between C. indica and C. sativa for plants from Algiers. Mongeri (1865) described C. indica cultivation at Izmit and Bursa, south of Istanbul (i2).

(4) West and Central Asia (Irano-Turanian)

Regel (1880) identified plants growing near Lake Issyk-Kul as a new variety, C. sativa [gamma] asperrima (i3). Polak (1865) assigned C. indica to medicinal plants at Tehran (i4). Vambery (1868) described beng or ben gis as "the poison produced from the Cannabis indica" in Bukhara and Khoqand (i5).

Henderson and Hume (1873) assigned C. indica to drug-type plants cultivated in Yarkand (i6). However, at the Kew Herbarium, a Yarkand specimen collected by Henderson is labeled "Cannabis sinensis." Vavilov and Bukinich (1929) found feral and wild Cannabis in Afghanistan, and named them C. indica f. afghanica and C. indica var. kafirstanica, respectively (i7).

(5) Sino-Japanese (East Asiatic)

Fischer (1810) erected a new taxon for Chinese hemp, Cannabis chinensis. He did not state provenance for the germplasm, but Canton (i.e., Guangzhou, a6) was the only Chinese port open to foreigners at that time, von Humboldt (1811) considered Chinese hemp a type of C. indica (i7). von Siebold (1827) described C. sativa b indica in Japan (i8). Boitard (1839) suggested that Chinese hemp was "probably the same species as Indian bangue."

Tatarinov (1858), a Russian physician in Beijing, assigned C. indica to local medical plants (i9). Hedde (1848) assigned C. indica to germplasm obtained from Shanti district, Guangzhou (i7). Itier (1846) assigned C. indica to germplasm obtained from Huangtian, 170 km N.E. of Guangzhou (i7).

Itier gave gcrmplasm to Delile (1849), who grew it in Montpellier. Delile was unaware of Fisher's publication, and re-coined Cannabis chinensis (x6). Koch (1854) noted that C. chinensis resembled drug plants from India. Vilmorin (1851) gave Chinese hemp a new name, "Cannabis gigantea Delile." This Latin name was an unfortunate choice, because it had previous been applied to chanvre de Piemont (x3) (Rey, 1835; Vilmorin, 1837).

Jomard (1852) wrote about Chinese hemp, to which he assigned Vilmorin's taxon C. gigantea. Itier (1853) also reassigned lo-ma to C. gigantea. Heuze (1860) synonymized Vilmorin's taxon with "Cannabis indica Lam." Alefeld (1866) assigned Cannabis sativa gigantea to "Chinese, Oberlander, or Picdmontese giant hemp"--in other words, to both C. gigantea Vilmorin, 1837 (Piedmontese hemp) and C. gigantea Delile ex Vilmorin, 1851 (Chinese hemp).

Pabst (1887) erected C. sativa var. chinensis, and described plants as "rich and protruding branches, 3-6 m high." Hoffmann (1944) coined Cannabis var. indica sub var. Gigantea for Chinese hemp, indicating its kinship with indica. Zhang (1990) noted relatively high levels of THC in some Yunnan landraces, which he named Cannabis sativa ssp. indica var. yunnanica (i10). These landraces may trace back to Sayyid Ajjal Sams al-Din Omar (1211-1279), a Muslim from Bukhara, appointed as Yunnan provincial governor by Kublai Khan. Hillig (2005) and Clarke and Merlin (2013) considered Chinese hemp a biotype of indica.

(6) African-Indian desert (Sahara-Arabian)

Ibn al-Baitar, a Spanish Moor who moved to Cairo around 1240, identified qinnab hindi (Indian hemp) growing in Egypt (ill), distinct from plants he knew in Spain, qinnab and qinnab barri (Ibn al-Baitar, 1985). Godard (1867) and Mackenzie (1893) describe hashish made from C. indica in Egypt (i11).

Hasselquist (1766), a student of Linnaeus, broke from Linnaean orthodoxy and assigned Cannabis vulgaris to plants cultivated in Palestine for chashis (x4). Stokes (1812) synonymized Hasselquist's taxon under C. indica (i12). Mongeri (1865) described C. indica cultivation at Mosul in present-day Iraq (i13).

(7) Sudano-Zambezian-Sindhia

von Maltzan (1873) lived in Aden, Yemen, where he encountered hashish made from C. indica (i14). Honigberger (1852) identified plants in Punjab and Kashmir as C. indica, due to their unique chemistry compared to C. sativa (i15).

(8) South Asia (Indian)

Rheede (1690) gave the names Kalengi-cansjava and Tsjeru-cansjava to male and female Cannabis, respectively, at Kochi on the Malabar coast (x7). O'Shaughnessy (1838-1840) employed the taxon C. indica, yet he considered "the Cannabis sativa and indica are identical" (i16). Kerr (1877) a British-trained Bengali botanist, referred to Bengal ganja as C. indica, distinct from C. sativa (i16).

Johann Friedrich Metz was a German missionary who collected plants on the Malabar coast (i17). His collection of "Cannabis indica" at herb. LE is a dense, lightly-seeded bud--the oldest specimen of manicured ganja we have seen. Rottler (1836-7), a Danish missionary at Tranquebar and Madras (i17), translated Tamil kancam as Cannabis indica. A few botanists in the Himalaya referred to local plants as C. indica (i18, Cleghorn, 1866, Aitchison, 1869, Lawrence, 1895).

(9) Continental Southeast Asia (Indochina)

Hedde (1848) assigned C. indica to germplasm obtained from Tourane, now Da Nang, Vietnam (i19).

(10) Malayian (Malesian)

Rumpf (1747) assigned C. indica to drug plants cultivated in the Moluccas islands, Indonesia (i20). Blume (1825), a German botanist who moved to Jakarta, used the taxon Cannabis sativa var. indica for plants with the local name ginji (3000 km west of i20).

Appendix 4: Taxonomic models in the 20th-21st century

The "species debate" became a cause celebre in 1970s court cases. The primary adversaries in this debate were Richard Evans Schultes (1915-2001), a Harvard ethnobotanist, and Ernest Small (1940-), a Canadian taxonomist who specialized in Cannabis. Their taxonomic debates in courtrooms often involved "an appreciable irrational emotive component" (Small, 1979). One taxonomic paper from that era made reference to "the Honorable Harry Anslinger," and the "menace" posed by Cannabis (Quimby et al., 1973).

Schultes's taxonomic work is limited to two publications. Initially, Schultes (1970) considered Cannabis a monotypic genus. Subsequently, Schultes et al. (1974) recognized C. sativa, C. indica, and C. ruderalis. Schultes changed his opinion based on an analysis of herbarium specimens, a survey of the Mississippi Cannabis plantation, and "preliminary field work" in Afghanistan.

Schultes collaborated with Loren C. Anderson at Florida State University. Anderson published two papers. Anderson (1974) compared wood anatomy in C. sativa (a feral hemp plant in Kansas, likely of Chinese provenance) and C. indica (a plant that Schultes collected in Afghanistan). Anderson (1980) compared leaf variation in four populations of Cannabis: 1. C. sativa (fiber varieties--tall, laxly branched plants), 2. C. sativa SS (Small-Seeded drug plants from India and Pakistan--relatively tall, with narrow leaflets), 3. C. indica (drug plants from Afghanistan--short, densely branched, with broad leaflets), and 4. C. ruderalis (wild plants, probably from Central Asia--very short and unbranched). Anderson illustrated his species concept in a line drawing (Fig. 5).

Small began Cannabis taxonomic research in 1971, under common-garden conditions on a three-acre farm near Ottawa, Canada. He grew nearly 400 Cannabis accessions obtained from the USD A, the UN, the University of Mississippi, and from botanical gardens around the world. Small and colleagues conducted cross-breeding experiments (Small, 1972, 1984). They assessed many taxonomic characters: cannabinoid content (Small & Beckstead, 1973a, b; Small et al., 1975; Small & Marcus, 2003), seed chemistry (Small et al., 1976), morphological variation in seeds (Small 1975), vegetative characters (Small et al., 1976), flower characters (Small & Naraine, 2015a, b), developmental characters (Small et al., 2003), and biogeographical aspects (Small, 2015a, b).

This work was summarized (Small and Cronquist, 1976), and elaboratored in a twovolume text (Small, 1979). His work continues to evolve--Small (2015a) has taken on aspects of Hillig's work regarding Chinese hemp. Small's classification and nomenclature is widely accepted around the world (e.g., Hanelt, 2001; Yang, 2003: Kojoma et al., 2006; Mukherjee et al., 2008; Mabberley, 2008; Shipunov, 2010; Chandra et al., 2013). Small's taxonomic scheme is attested on high-profile websites. Examples:

http://frps.eflora.cn, ru.wikipedia.org/wiki

http://plants.usda.gov/java

www.ars-grin.gov

www.theplantlist.org

www.tropicos.org

www.ncbi.nlm.nih.gov/taxonomy

Google Scholar (https://scholar.google.com) computes citation metrics for authors and their publications. We applied the "advanced search" algorithm, using the words "taxonomy," "cannabis," and author name. After screening for appropriate hits, we obtained the following results: Small: 18 publications, cited collectively by 675; Hillig: 7 publications, cited collectively by 299; de Meijer: 5 publications, cited collectively by 207; Schultes: 2 publications, cited collectively by 193; Gilmore: 5 publications, cited collectively by 179. No other authors were cited more than 150 times.

Hillig and colleagues cultivated 157 accessions under common-garden conditions at Indiana University. They obtained accessions from Small, the CPRO. Dutch seed banks, the Vavilov Institute, law enforcement agencies, field stations, and botanical gardens across Eurasia. Hillig analyzed genetic characters (Hillig, 2004a, 2005), cannabinoid profiles (Hillig & Mahlberg, 2004), terpenoid profiles Hillig, 2004b, seed morphology (Hillig, 2005b, c), leaflet characters (Hillig, 2005b, c), stalk morphology (Hillig, 2005b, c), developmental characters (Hillig, 2005b, c), host-parasite characters (Hillig, 2005b, c, McPartland & Hillig, 2003, 2004, 2006), and biogeographical aspects (Hillig, 2005a, b).

De Meijer and colleagues systematically investigated Cannabis under commongarden conditions at Wageningen University. They collected over 150 Cannabis accessions--now the CPRO collection. They obtained germplasm from the Vavilov Institute, IPK-Gatersleben Institute, Dutch seed banks, European breeders of fiber-type plants, and botanical gardens across Eurasia. De Meijer has continued Cannabis studies at GW Pharmaceuticals in the United Kingdom. De Meijer analyzed cannabinoid content (De Meijer & van Soest, 1992; De Meijer & Keizer, 1996), the inheritance of cannabinoid phenotypes (De Meijer et al., 2003; Mandolino et al., 2003; De Meijer & Hammond, 2005. De Meijer et al., 2009a, b), stalk morphology and chemistry (De Meijer, 1993a, 1994b, 1995), seed morphology and chemistry De Meijer & Keizer, 1996, leaflet characters (De Meijer et al., 1992; De Meijer & Keizer, 1996), host-parasite relationships (De Meijer, 1993b; De Meijer & Keizer, 1996), developmental characters (de Meijer & Keizer1996), sequence heterogeneity in THCA-synthase genes (Onofri et al, 2015), and biogeographical aspects (De Meijer, 1999, De Meijer, 2004, 2014).

Gilmore and colleagues researched Cannabis genetics at Australian National University. Their early work analyzed police-confiscated materials of unknown origin, lacking taxonomic inferences. They developed primers for microsatellite DNA loci, also called short tandem repeats (STRs), and validated their work for forensic purposes (Gilmore & Peakall, 2003; Gilmore et al., 2003, 2007; Howard et al., 2008, Howard et al., 2009). Gilmore et al. (2007) switched to polymorphic cpDNA and mtDNA loci, which they sequenced from known CPRO accessions.

"Strain" names

The International Code of Nomenclature for Cultivated Plants (ICNCP, Brickell, 2009) regulates the naming of plants whose recent evolution has been influenced by human selection. The ICNCP's basic unit of classification is the cultivar, "an assemblage of plants that (a) has been selected for a particular character or combination of characters, (b) is distinct, uniform, and stable in these characters, and (c) when propagated by appropriate means, retains those characters."

The ICNCP's rules for naming and describing cultivars involve valid publication, typification ("Nomenclatural Standard"), and priority. The ICNCP is available online for consultation regarding these provisions.

Cultivar names meeting ICNCP provisions are placed in single quotation marks. The best known Cannabis cultivar, judging from the number of Google search hits, is 'FINOLA'. The ICNCP also recognizes "Group" names, "All members of a Group must share the character(s) by which that Group is defined." Small (2015a) proposed six Group names for cultivated kinds of Cannabis and their hybrids.

Article 2.2 in ICNCP stipulates that the words "variety," "form," and "strain" must not be used for the word "cultivar" (Brickell, 2009). Notwithstanding Article 2.2, some national and international plant registries use "variety" interchangeably with "cultivar." The words "variety" and "form" also designate subspecies ranks in the ICN. "Strain" is not formally recognized by the ICN or ICNCP.

Segregates within "Sativa" and "Indica" are called "strains." Watson (1985) coined several well-known "strain" names, such as "Original Haze", "Skunk #1", "California Orange", "Afghani #1", and "Early Girl". Small (2015a) pointed out that strains are conceptually identical to cultivars, but almost no strains have met ICNCP requirements for cultivar recognition.

Clarke and Merlin (2015) took umbrage, and argued that "the bigger picture" justifies using "strain" and "cultivar" as equivalents. Small (2015b) retorted that they showed insufficient respect for codes of nomenclature, which hold pragmatic and moral status. "The botanical codes are by and large adhered to by scientists, commercial interests and editors because they provide stability and reliability to names that otherwise would result in confusion."

"Strain" names have proliferated exponentially. Watson (1985) named 10 strains. Within 15 years, Dutch seed companies offered 150 strains for sale (Clarke, 2001). A decade later, the number of strain names reached 900 (Cannabis Strain Database, 2010). Most recently, Leafly (2015) listed 1535 strain names, and Seedfinder (2015) listed 6510 strain names. Doyle (2007) referred to strains as ganjanyms. Most strains are recognized hybrids, characterized as "Sativa-dominant" or "Indica-dominant." In today's largely illicit market, strain names are swapped and counterfeited, and generally unreliable (Lee, 2013; Sawler et al., 2015; Pierson, 2016).

The strain "AK-47" examples the arbitrariness of vernacular classification: "AK-47" won "best Sativa" in the 1999 Cannabis Cup, and won "best Indica" 4 years later. The ancestry of "Super Silver Sour Diesel Haze" offers a window into this warren of questionable pedigrees (Box 2).
Box 2 Putative ancestry of "Super Silver Sour Diesel Haze", from
Seedfinder (2015)

Super Silver Sour Diesel Haze, a cross of Super Silver Haze x
Sour Diesel

* Super Silver Haze, a cross of {(Haze x Haze) x Skunk #1} x
{(Haze x Haze) x Northern Lights #5}

** Haze, a cross of landraces from Colombia, Mexico, Thailand,
and southern India

** Skunk #1, a cross of (Afghani x Colombian Gold) x Acapulco Gold

** Northern Lights #5, a murky pedigree, either pure Afghani, or a
Thailand x Afghani hybrid

* Sour Diesel, a cross of Original Diesel x DNL

** Original Diesel, a cross of Chemdawg x (MassSuperSkunk x SensiNL)

*** Chemdawg, of unknown lineage

*** MassSuperSkunk, a cross of Skunk #1 x Afghani

*** SensiNL, a cross of three Northern Lights strains of shared
pedigree, NL #1, NL #2, and NL #5

** DNL, a cross of (RFK Skunk x Hawaiian) x Northern Lights

*** RFK Skunk, likely derived from Skunk #1

*** Hawaiian, a "Sativa/Indica hybrid"

*** Northern Lights, as described above


John M. McPartland (1-2) * Geoffrey W. Guy (1)

(1) GW Pharmaceuticals. Sovereign House, Histon, Cambridge CB24 9BZ, UK

(2) Author for Correspondence; e-mail: mcpruitt@myfairpoint.net

Published online: 22 June 2017

Please note: Some non-Latin characters were omitted from this article

Caption: Fig. 1 Type specimens of C. sativa L. (left), and C. indica Lam. (right), photographs courtesy of McPartland and Herb. P, respectively

Caption: Fig. 2 Taxon names applied by field botanists. Locations of "C. sativa" labeled alphanumerically, s1, s2, etc. Locations of "C. indica" labeled alphanumerically, i1, i2, etc. Locations of other Cannabis taxa labeled alphanumerically, x1, x2, etc. Base map shows boundaries of ten floristic regions by Takhtajan (1986). For full citations of alphanumerical sites see Appendix 3

Caption: Fig. 3 The wild-type phenotype. Left: domesticated versus wild-type Cannabis fruits, illustrated by Zinger (1898). Right: type specimen of C. sativa var. spontanea Vav. (McPartland photo, herb. WIR)

Caption: Fig. 4 Classification of Cannabis sativa, according to Small & Cronquist, 1976

Caption: Fig. 5 Line drawing by Anderson (1980), courtesy of the Harvard University Herbaria and Botany Libraries

Caption: Fig. 6 Line drawings of C. ruderalis by Janischevsky (1924)

Caption: Fig. 7 Seeds illustrated by Vavilov and Bukinich (1929). Original caption: Left to right: 1. from northern Afghanistan--cultivated form--Cannabis sativa L.; 2. ordinary Russia hemp from Orel; 3. wild hemp from Saratov; 4., Cannabis indica f. kafiristanica Vav.; 5. Cannabis indica var. afghanica Vav. The upper row enlarged 6 times, the lower row showing the bases of achenes enlarged 10 times

Caption: Fig. 8 Type specimen of C. sativa var. kafiristanica Vav. (McPartland photo, taken at herb. WIR)
COPYRIGHT 2017 New York Botanical Garden
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2017 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:McPartland, John M.; Guy, Geoffrey W.
Publication:The Botanical Review
Article Type:Report
Date:Dec 1, 2017
Words:26440
Previous Article:Assessing the relevance of herbarium collections as tools for conservation biology.
Next Article:Biology of Amaranths.
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters