Review

What is in a name? The need for accurate scientific nomenclaturefor plants

Diego Rivera a,n, Robert Allkin b, Concepción Obón c, Francisco Alcaraz a, Rob Verpoorte d,Michael Heinrich e,f

a Dpto Biología Vegetal, Campus de Espinardo, Universidad de Murcia, Murcia 30100, Spainb Royal Botanic Gardens Kew, London, United Kingdomc Dpto. Biología Aplicada, Escuela Politécnica Superior, Universidad Miguel Hernández, Ctra. Beniel Km 3.2, 03312 Orihuela, Alicante, Spaind Division of Pharmacognosy, Section Metabolomics, Institute Biology Leiden, Leiden University, Leiden, The Netherlandse Research Cluster Biodiversity and Medicines/ Centre for Pharmacognosy and Phytotherapy, UCL School of Pharmacy, University of London, London, UnitedKingdomf Department of Pharmaceutics and Industrial Pharmacy, Faculty of Pharmacy, King Abdulaziz University, Jeddah, Saudi Arabia

a r t i c l e i n f o

Article history:Received 24 September 2013Received in revised form15 December 2013Accepted 17 December 2013

Keywords:NomenclatureBotanical nomenclatureTaxonomy Latin binomialsPlant authenticationTraditional medicine

a b s t r a c t

Ethnopharmacological relevance: To avoid ambiguities and error, ethnopharmacological and any otherresearch on plants requires precise and appropriate use of botanical scientific nomenclature.Aims: This paper explores problems and impacts of ambiguous or erroneous use of botanical scientificnomenclature in ethnopharmacological studies. It suggests how the frequency and impact of such errorscan be reduced.Approach and methods: We assessed 214 articles published in the three first volumes of the Journal ofEthnopharmacology in 2012: 140(1) to 141 (3) and 214 articles in Phytomedicine (2012–2013): 19 (5) to20 (7).Results: Amongst the articles reviewed 308 articles cited plant names incorrectly. Among the articlesstudied 9178 Latin scientific names were cited and 3445 were incorrect in some respect. Simple principlesapplied in a systematic way and used together with open-access reference resources could help authors,referees and editors of ethnopharmacological, phytochemical, toxicological and clinical studies to reduceambiguity about the identity and name of the species involved and thus significantly improve the qualityof the final publication.Conclusions: We have identified a series of key steps needed to solve the taxonomic ambiguities anderrors. Aside from reinforcing existing policies, journals will have to implement better tools to ensure theproper authentication of materials. The new electronic publishing environments offer novel ways todevelop such botanical-taxonomic tools.

& 2013 Elsevier Ireland Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22. Objectives. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34. Results and discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

4.1. The scale and nature of the problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44.2. Systematic analysis of possible errors, their impact . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54.3. Lack of evidence for which plants are being studied and reported: “Are comprehensive specimen citations included?” . . . . . . . . . . . . . . 54.4. Lack of sufficient evidence for the identity of the specimens studied . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54.5. Scientific names are not used when referring to plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

Contents lists available at ScienceDirect

journal homepage: www.elsevier.com/locate/jep

Journal of Ethnopharmacology

0378-8741/$ - see front matter & 2013 Elsevier Ireland Ltd. All rights reserved.http://dx.doi.org/10.1016/j.jep.2013.12.022

Abbreviations: TPL, The Plant List; TCM, Traditional Chinese Medicinen Corresponding author: Tel.: þ34 868 884994; fax: þ34 868 883963.E-mail addresses: drivera@um.es (D. Rivera), b.allkin@kew.org (R. Allkin), cobon@umh.es (C. Obón), verpoorte@chem.leidenuniv.nl (R. Verpoorte),

m.heinrich@ucl.ac.uk (M. Heinrich).

Please cite this article as: Rivera, D., et al., What is in a name? The need for accurate scientific nomenclature for plants. Journal ofEthnopharmacology (2014), http://dx.doi.org/10.1016/j.jep.2013.12.022i

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4.6. Failure to use valid scientific names to refer to plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64.7. Failing to use appropriate fonts to formally differentiate scientific names from other text . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84.8. Using names and reflecting taxonomies that are not currently ‘accepted’ by modern regional floras and databases . . . . . . . . . . . . . . . . . 8

5. General recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

1. Introduction

All ethnopharmacological research needs to refer unambigu-ously to the plant species under study. At first glance one couldargue that this is stating the obvious but the evidence points to aneed to systematically address the challenges arising from this andto set clear standards for botanical nomenclature in pharmacolo-gical and ethnopharmacological work. Similar concerns exist inphytochemical, toxicological and clinical publications as well as awide range of biological and ecological studies that in one way oranother refer to vascular plants.

Over 90% of the organisms investigated in ethnopharmacolo-gical studies are vascular plants. Scientific names of plants follow aprecise and simple system of nomenclature used by scientists in allcountries. Every individual organism is treated as belonging to anindefinite number of taxa of consecutively subordinate rank (indescending sequence these are: kingdom, division or phylum,class, order, family, genus, and species), among which the rankof species is basic. The name of a species (written in Italics) is abinary combination consisting of the name of the genus (the firstletter is always capitalized) followed by a single specific epithet(never capitalized). In publications, it may be desirable, to cite theauthor(s) of the name concerned, using unambiguous standardforms. The application of names is determined by means ofnomenclatural types (either a single specimen conserved in oneherbarium or other collection or institution, or an illustration).Type specimens of names must be preserved permanently.

Neither vernacular names nor pharmacopoeia names are sub-ject to formal controls nor do they have any scientific merit sincethe meaning associated with these names are not ultimately tiedto reference specimens as is the case for scientific plant names(through the “type” specimen concept). Thus articles failing to citethe scientific name of a plant cannot guarantee the identity of theplants involved nor considered scientifically sound. Therefore, inscientific papers only valid scientific names are acceptable.

The International Code of Botanical Nomenclature (changed in2011 to International Code of Nomenclature for algae, fungi, andplants) aims at the provision of a stable method of naming plants(McNeill et al., 2011; McNeill and Turland, 2011). The Codeestablishes how new names for plants should be published andscientific publications should follow these rules. Most users ofscientific names will never need to consult the Code but can beconfident that its application reduces the ambiguity and errors inthe naming of plants. The rules that govern the scientific namingof algae, fungi, and green plants are revised at NomenclatureSection meetings at successive International Botanical Congresses.

For historical and geographical reasons one can find two ormore scientific names that apply to the same plant species, theapplication of principles including priority and typification ledto distinguish a more appropriate name from the rest (syno-nyms). Homotypic synonyms (nomenclatural synonyms) arenames based on the same type as that of another name, theseare unambiguous concerning the application of the name to aparticular taxon. Heterotypic synonyms (taxonomic synonyms)are names based on a type different from that of another namereferring to the same taxon. These are subjective and involve

ambiguity concerning the application of the name to aparticular taxon.

The Code seeks to stabilize the naming of plants—this system isthe reference point for currently ‘acceptable0 nomenclature, notany plant name databases. However, these binomials can beverified at sources such as TPL (2010) which attempt to faithfullyfollow the provisions of the code.

Additional, independent designations for special categories oforganisms used in agriculture, forestry, and horticulture (andarising either in nature or cultivation) are dealt with in theInternational Code of Nomenclature for Cultivated Plants (ICNCP)(Brickell et al., 2009), which defines the cultivar as its basiccategory.

To achieve scientific rigor and to communicate effectively(avoiding ambiguity and error), authors of research articles needto employ botanical nomenclature appropriately. While this is achallenge facing those working in all fields of botanical research, inrecent years the issues have become ever more pressing inethnopharmacology due to the significant increase in the numberof studies published on the medicinal properties of plants. Forexample, Chan et al. (2012) focused on the available resources forcorrect citation of Chinese Materia Medica. However, this does notonly affect studies on traditional Chinese medicine but is equallyrelevant to all ethnopharmacological studies (Allkin, 2006).

Evidence to support ethnopharmacological hypotheses requiresreliably documented materials and methods. Ambiguous or erro-neous use of botanical nomenclature can invalidate otherwisevaluable research findings since it will be impossible for readers toestablish which organisms the observations relate to (at least withany certainty). An exhaustive review of the ethnopharmacologicalliterature of the Near East and the Caucasus by Rivera et al. (2012)identified numerous articles that presented problems in the effec-tiveness of the communication through errors in either the nomen-clature or taxonomy used. These problems are not restricted to papersrelevant to the Near East or to TCM.

Other authors have already discussed these concerns and havesuggested more rigorous training and a better use of the existingresources (e.g. Bennett and Balick, 2008; Cotton, 1997; Martin,1996; Nesbitt et al., 2010. see also Heinrich et al., 2009; Allkin,2006, in press, see also Bennett and Balick, this issue), but theauthors have not necessarily been able to address this within thepublishing strategy of a specific journal or a group of journals.Clearly, this is also linked to the enormous problem of a lack ofbotanical (taxonomic and systematic) knowledge of many scien-tists, reductions in the training in these fields, a general lack oftrained taxonomists, and a constant decrease in the number ofresearch and training institutes dedicated to taxonomy, a problemwhich, however, is outside of this paper0s scope.

2. Objectives

In order to address and resolve this problem, a sound under-standing of the scope of the problem and of the specific classes oferror is needed. Using published articles in two leading academic

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journals in the field of medicinal plant research we sought toidentify these errors and to develop short and mid-term strategiesfor resolving them.

3. Methods

In order to analyze this further and to identify ways forward,we assessed 214 articles published in the three first volumes of theJournal of Ethnopharmacology in 2012: 140(1) to 141 (3) and equalnumber of articles in Phytomedicine (2012–2013): 19 (5) to 20 (7)(Table 1). The number of papers, 428, was chosen taking intoaccount the maximum coverage within a reasonable effort. Tofacilitate comparison we reviewed exactly the same number ofpapers in each of the journals. The taxonomic & nomenclaturalveracity was assessed by comparison with existing standardregional floras, most importantly Efloras (2012) for China andAmerica, and with the botanical literature available at BHL (2013),and databases: Euromed (2011), Tropicos (2012) and most impor-tantly the www.theplantlist.org (TPL). It was not necessary todevelop a strategy for resolving conflicts between TPL and othertaxonomic reference works, because none was detected forthe species treated. Brummitt and Powell (1992) provide

unambiguous standard forms for a large number of authors ofnames of organisms in conformity with Recommendation 46A ofthe International Code of Botanical Nomenclature (McNeill et al.,2011). These abbreviations, updated as necessary from the Inter-national Plant Names Index (www.ipni.org/ipni/authorsearchpage.do) have been used for detecting spelling or abbreviation errors inthe author string throughout this study.

The problems identified were analyzed both in terms of therelative frequency of ARTICLES published with erroneous names(Table 1) and in terms of the frequency which individual NAMES areused erroneously (Table 2). These data were used to review thetypes of error in each case (Tables 3–6). First we verified thereliability of the identity of the material studied recording whicharticles fail to provide any evidence of the plants actually studiedby not citing voucher specimens seen and used in the publishedstudy as well as which articles fail to provide details of how thosespecimens were identified (Table 3). We then analyzed articleswhich refer to plants without providing any scientific plant namefor the specimens used (Table 4). Third, we analyzed articles failingto use scientific plant names appropriately (through misspelling,inconsistent use of Italics, use of non-standard author abbrevia-tion, erroneous or missing authors) (Tables 5 and 6). Finally weanalyzed articles using names and reflecting taxonomies that are

Table 2Totals of plant names revised (including repeats) and of errors (including those concerning scientific names and those concerning reliability of the identification).Abbreviations: JEP, Journal of Ethnopharmacology. PHY, Phytomedicine.

Subject No. plantspecies ineach paper

Journal No. articlesciting plantnames

Scientificplant namesused

(%) Totals Scientificnames usedcorrectly

Incorrectscientificnames

Total oferrors

Specific plantmonographs

One JEP 119 3105 46 2337 768 867PHY 127 1749 72.8 774 975 1233

Medicinal plantscatalogues, studieson activesubstances

Two to many JEP 74 3671 54 2382 1289 1679PHY 24 653 27.2 240 413 583

Total 344 9178 5733 3445 4362

Table 1Scale and nature of issues found in papers reviewed. JEP: Journal of Ethnopharmacology. PHY: Phytomedicine.

Subject No. scientific plantnames in eachpaper

Journal Papers (%) Totals With correctbotanicalnomenclature

With incorrectbotanicalnomenclature (atleast in part)

With noscientific names(at least in part)

Specific plant monographs One JEP 119 55.6 30 89 3PHY 127 59.3 4 123 9

Medicinal plantscatalogues, studies onactive substances

Two to many JEP 74 34.6 1 73 16PHY 24 11.2 1 23 7

Articles not referring toplants

None JEP 21 9.8 N/A N/A N/APHY 63 29.5 N/A N/A N/A

Totals JEP 214 100 31 162 19PHY 214 100 5 146 16

Table 3Articles failing to provide evidence of which plants were studied (i.e. failing to provide details of the voucher specimens seen) or to provide sufficient evidence of the identityof the specimens studied by failing to establish how those specimens were identified. Abbreviations: See Table 1.

Subject No. plant species Journal (%) lack or inaccuratevoucher details

(%) with no details howspecimens were identified

Specific plant monographs One JEP 9.8 10.2PHY 23.4 27.1

Medicinal plants catalogues, Studies on active substances Numerous JEP 14.5 8.9PHY 3.7 3.7

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not currently ‘accepted0 by modern regional floras and databases(use of older synonyms, citing species more than once in listsunder alternative synonyms, older family delimitations) (Table 7).

4. Results and discussion

4.1. The scale and nature of the problem

Of the 214 articles published in the Journal of Ethnopharmacol-ogy (JEP) and 214 articles in Phytomedicine (PHY) (Table 1), 55.6%(JEP) and 59.3% (PHY), respectively, were devoted to plant species(with the scientific names usually appearing in the title). 34.6%(JEP) and 11.2% (PHY) of the published studies were of bioactiveconstituents, medicinal plant catalogues or reviews which alsoused scientific names of plants. Only 9.8% (JEP) and 29.5% (PHY) ofarticles did not refer to plants at all.

Thus of all the articles we reviewed, 90.2% (JEP) and 70.5%(PHY) referred to particular plants while only 81.3% (JEP) and 63.1%(PHY) use at least one botanical scientific name. Thus of all thepapers reviewed 35 (19 (JEP)þ16 (PHY)) referred to one or moreplants without citing their scientific plant names at all and rely

only upon their vernacular or pharmacopoeia names. Such articlesthus cannot reliably be associated with any particular species.

Amongst the articles reviewed which did cite scientific plantnames only 31 (16%, JEP) and 5 (3%, PHY) were free from anynomenclatural or taxonomic error and from errors in how speci-mens were cited. 162 articles (84%, JEP) and 146 (97%, PHY) citedplant names incorrectly.

Among the articles studied 9178 Latin scientific names werecited (6776 in JEP and 2402 in PHY). This includes all the namesused including repetitions in the same article, because in a singlearticle one species may appear named both correctly and incor-rectly. The proportion of errors amongst these names was found tobe different between different types of publication. Thus in paperswith lists of plants the error rate was 63.2% (PHY) and 35.1% (JEP)(in terms of percentage of erroneous names). For single-speciespapers however the error rates were slightly better for the JEP(24.7%) but also high for PHY (55.8%) (Table 2). Monographstherefore could have a higher error rate which may reflect uponthe journal policy and attitude of the editors.

We next conducted an more detailed evaluation of all theerrors identified (Table 2) including nomenclatural and taxonomicerrors detected in 214 JEP papers (2546 errors in total) and 214PHY papers (1816 errors). These figures suggest that on average

Table 4Articles failing to provide any scientific plant name of the specimens used. Abbreviations: See Table 1.

Subject No. plant species Journal (%) Articlesconcerning plants

(%) Without anyscientific plant name

Specific plant monographs One JEP 55.6 2.8PHY 59.3 4.6

Medicinal plants catalogues, Studies on active substances Numerous JEP 34.6 7.0PHY 11.2 3.2

Table 5Articles failing to use scientific plant names appropriately. Abbreviations: See also Table 1. D1: Misspelling of Genus or species name. D2: Inconsistent use of Italics. D3: Useof non-standard author abbreviation. D4: Erroneous author. D5: No author. D6: Misspelling of family name.

Subject Journal D1 (%) D2 (%) D3 (%) D4 (%) D5 (%) D6 (%)

Specific JEP 4.2 5.1 18.7 7.9 8.8 0.5PHY 3.3 9.8 16.8 5.6 28.9 0

Multispecies JEP 9.8 6.5 15.4 5.6 13.5 0.5PHY 1.9 1.4 2.3 2.3 4.7 0

Table 6Scientific plant names not appropriately used among the 6776 (JEP) and 2402 (PHY) names analysed. Abbreviations: See also Table 1. D1: Misspelling of Genus or speciesname. D2: Inconsistent use of Italics. D3: Use of non-standard author abbreviation. D4: Erroneous author. D5: No author. D6: Misspelling of family name.

Subject Journal (%) Erroneous names D1 (%) D2 (%) D3 (%) D4 (%) D5 (%) D6 (%)

Specific JEP 11.3 0.6 0.2 1.5 0.4 5.4 o0.01PHY 40.6 0.5 2.5 3.7 1.9 25.4 0

Multispecies JEP 19.0 0.7 0.6 4.9 0.3 5.5 o0.01PHY 17.2 0.2 0.2 0.7 0.7 10.9 0

Table 7Articles using names and reflecting taxonomies that are not currently ‘accepted’ by modern regional floras and databases, although this cannot be considered error.Abbreviations: see Table 1.

Subject Journal Use of oldersynonyms (%)

Older familyadscription (%)

Duplicate citation by simultaneoususe of synonyms in lists (%)

Specific JEP 4.2 3.2 0PHY 4.2 0.5 0

Multispecies JEP 2.8 2.3 0PHY 10.2 0 0

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there were more than ten errors per paper but this figure hidesenormous diversity with the percentage of erroneous names inany one paper varying from 0% to 100%.

Of the scientific plant names cited in these articles 69.6% (JEP)and 42.2% (PHY) were correct in every sense: spelled correctly,correct authors and unambiguous (Table 2), whilst 80.3% (JEP) and54.6% (PHY) were essentially correct other than for spelling orabbreviation errors in the author string (Table 6). Errors were lessfrequent among those scientific names used within papers thatdealt with only one species: 75.3% (JEP) and 44.2% (PHY) beingcorrect as compared to 64.9% (JEP) and 36.7% (PHY) of the namescited in multi-species papers.

Otherwise correct, but using names and reflecting taxonomiesthat are not currently ‘accepted’ by modern regional floras anddatabases) account for 4.7% (JEP) and 9.6% (PHY) of the total (320and 231 names respectively) which could mislead readers as to theGenus in which this plant is most closely relate, thus complicatingany comparison with other species sharing chemical characteris-tics (Table 7).

4.2. Systematic analysis of possible errors, their impact

Five different types of error have been identified through thisanalysis (Fig. 1). Specifically these include failures in

A. Providing any evidence of which plants were actually studiedby not providing details of the voucher specimens seen andrecorded;

B. Providing sufficient evidence of the identity of the specimensstudied by not providing details of how those specimens wereidentified;

C. Using scientific plant names;D. Using scientific plant names appropriately;E. Using a style appropriate to formally differentiate scientific

names from other text.A sixth category is also analyzed which includes names noterroneous but in some respect inappropriate.

F. Using names and reflecting taxonomies that are not currently‘accepted’ by modern regional floras and databases.

The impact of these different classes of error are different.While D, E and F have more modest impact, ‘A’ and ‘B’ errorsjeopardize the data (‘use’ or ‘property’) recorded in the manuscriptactually being related to the named species. Class ‘C’ errors mayresult in a reference to a totally different species, resulting inambiguity.

In the following we provide a snapshot of these problems andhighlight their impact on the scientific usefulness of the studies.For each problem we present alternative measures to guardagainst these issues. Some of these errors would be tractable byautomated checks on names: others will not. Some require aclearer policy (and enforcement) as to how specimens and namesare cited in articles.

4.3. Lack of evidence for which plants are being studied andreported: “Are comprehensive specimen citations included?”

The lack of, or inaccurate use of voucher specimens (denouncedby Chan et al., 2012; Rivera et al., 2012) seriously puts in questionthe reliability of the article. The repeatability of ethnopharmaco-logical or any botanical study depends on adequate description ofthe experimental methods used and evidence as to the plants used(citing voucher specimens). This is a common problem (Table 3)and dramatically reduces the scientific impact of a study. Merecitation of a living individual fromwhich samples were collected isnot a valid voucher specimen.

Regarding voucher specimens (plants, plant parts) the follow-ing metadata are generally needed: locality where the sample wascollected, the date of collection, time of day (botanically notrelevant but pharmacologically often extremely relevant), devel-opmental stage of the plant (e.g. just sprouting, fully developed, inbloom), collector and collector’s number. These are well estab-lished requirements but often not enforced. The absolute mini-mum to be cited within a paper (in order to establish the identityof the plants involved) are the collection locality, collector’s nameand the collector’s unique collection number. And, it is veryimportant the article also cites the herbarium in which eachspecimen was deposited. Voucher specimens should be depositedin herbaria accredited by Index Herbariorum (2013) and thestandard acronym of the specific herbarium should be given.

It could be considered the submission of photos of plantmaterial as supplementary material where relevant. This couldfor example be extremely useful when living material is used andcould be complementary to the mandatory use of voucher speci-mens (Fig. 2).

4.4. Lack of sufficient evidence for the identity of the specimensstudied

Erroneous identification is a serious problem which mayinvalidate the findings of a published article since any recordeduses or properties attributed may in fact relate to different speciesentirely. Such “misapplied” uses of plant names within theliterature are a permanent source of confusion for future research,search engines and databases.

How might a reviewer or reader detect such miss-identifica-tion? What can an author do to avoid this? Reviewers mustseriously consider: ‘Do we know how the author identified thevoucher specimens cited?’ Two methods are considered.

A. Identification by the authors of the paper. In this case theauthors should cite which identification keys, floras, fieldmanuals or other reference resources were used to identifythe specimens (Fig. 2). Herbarium collections with which thecited specimens were compared should be identified. Depend-ing on the nature of the sample (whole plant, plant fragments,powdered plant material, plant extract) the methodology(using binocular microscope, TLC, HPLC, specific reagents,etc.) for determining the identity may vary. All referencesconsulted (plant monographs, standard floras, pharmacognosymanuals, etc.) should be cited. While waiting to have acomprehensive global Flora, it is possible to find morphologicaldetails, habitats and distribution areas of most species used in

Fig. 1. Relative frequency of errors. Body size of letters is proportional to thepercentage of papers analyzed which present such an error.

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ethnopharmacological contexts in online floras of China,Pakistan, North America, etc. in Efloras (2012).

B. Identification by a botanical authority. Authors may rely uponthe authority of a colleague with botanical expertise or knowl-edge. Alternatively they may simply rely on the labeling of asample. Were a herbarium specimen previously seen andidentified by a taxonomic expert then their name will appearalongside the determination with the date of determination.The author of an article can cite that determination as evidencefor the identity of the plant material. However this does notreplace the specimen that vouches for the identity of materialused in a particular study. In the case of commercial labels thenit is essential to cite the literature consulted to identify thematerial. It is insufficient to merely say “the material wasauthenticated, verified, identified or certified by the specialist,taxonomist, X…” A deeper involvement in the papers ofbotanists and pharmacognosists could be of help in increasingaccurateness in plant identification and use of nomenclatureFig. 3.

A future means of checking correct identity may also comefrom barcoding using DNA sequencing. However this is still notunambiguous as it depends on the degree of similarity of closerelatives as well as on what is available in GenBank or othersources for comparison.

4.5. Scientific names are not used when referring to plants

There is confusion in the literature as to what are botanicalscientific names. Drug names written in Latin and used in apharmacopoeia, for example, are not scientific plant names. Thesame name can be applied to two or more herbal ingredients andinvolve different plants. For example, Crataegi folium cum floreor Crataegi fructus may be derived from Crataegus oxycanthoidesThuill. or Crataegus monogyna Jacq. (Rosaceae), or combinations ofthe two, or hybrids between the two. The meaning of suchPharmacopoeia names can change between national pharmaco-poeias or publications or authors and indeed change over time.The purpose in this context is to define material which can be usedas a medical preparation and not for defining a taxon (a plant).

They are, therefore, as ambiguous about the plant involved as are‘common names’.

Between 2.8% and 7% of the papers analyzed (depending on thetype of paper and journal) failed to use scientific plant names(Table 4). This accounts for 9.8% in JEP (19 out of 193 articles citingplant names) and PHY 10% (16 out of 151 articles citing plantnames). In this type of error any percentage above 0 is unaccep-tably high. Consequently, the biological entities actually studiedremain undefined and the research becomes void and of nofurther use. Ambiguity arises in two ways. (A) Different speciesmay have been studied and (B) a pharmacopoeia name for a herbalproduct may explicitly refer to 41 species. In the latter case thereaders and editors of the journal need to know which of thosespecies was studied in the article.

4.6. Failure to use valid scientific names to refer to plants

Some publications employ scientific names either withoutproper attention to (taxonomic) detail or without fully under-standing their value and how they should be cited. Use of non-standard author abbreviations, or of superfluous brackets are twoexamples. The most frequents are use of non-standard authorabbreviation (2.3% to 18.8% of papers and 0.7% to 4.9% of names),erroneous author (2.3% to 7.9% of papers and 0.3% to 1.9%), noauthor (4.7% to 28.9% of papers and 5.5% to 24.5% of names)(Tables 5 and 6). At best such errors simply demonstrate lack oftraining in nomenclature and finding the issue difficult but notnecessarily impair the effectiveness of the authors’ communica-tion. However a name without authors (or indeed a name withmisuse of an author abbreviation) in some contexts may beambiguous or even mislead readers since homonyms (identicalbinomials published by different authors at different times to referto different plants). For example. Pinus abies Lour. is a synonym forCunninghamia lanceolata (Lamb.) Hook. (in the Taxodiaceae) whilstPinus abies L. is a synonym of Picea abies (L.) H. Karst in thePinaceae. Thus the use of the author string “Lour.” or “L.” is notmerely decorative. An example of an important medicinal plant isPolygonum cuspidatum Willd. ex Spreng. This is a synonym ofPersicaria acuminata (Kunth) M. Gómez (a weed of tropical areas ofAmerica found naturalized abroad), though Polygonum cuspidatum

Fig. 2. Proposal for a taxonomic online form.

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Siebold & Zucc. is a synonym of Fallopia japonica (Houtt.) RonseDecr. (alternatively known as Reynoutria japonica Houtt.) which isa medicinal plant of temperate areas of the northern hemisphereand widely used in TCM. Clearly these two plants have verydifferent chemistry and such failures can have a significant impacton the scientific merit of a publication.

Misspelt genus or species names are an important problem.Again this may just show lack of training in nomenclature andfinding the issue difficult and be relatively benign. However onepossible outcome would be that the name included in the article isidentical to or very similar to the name of a completely different

plant again misleading readers into associating the publishedinformation with the wrong plant. The genus Argyreia Lour. is inthe family Convolvulaceae and includes climbing vines withhallucinogenic properties, but the genus Argyrella Naudin (asynonym of Dissotis Benth. in the Melastomataceae) includesmedicinal plants of tropical Africa, thus a small spelling difference(“i” or “ll”) has enormous relevance to the meaning of the text.Additional consequences of including misspelled names is that thepaper will not be found by researchers looking for information forthat plant when using search engines or indexing services. The useof misspelled names thus significantly reduces the probability of

Fig. 3. Proposal for a sequence for working with plant names in ethnopharmacological papers.

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the article being consulted or cited. A common cause of sucherrors is through automatic correction of texts by word processorswhich fail to recognize Latin of scientific names.

The baseline – the minimum –would be that a Latin name usedin a publication has actually been published in the botanicalliterature (and is thus scientifically meaningful i.e. it is notmisspelled or not just made up). It means that the article followsa “scientific” protocol.

4.7. Failing to use appropriate fonts to formally differentiatescientific names from other text

Inconsistent use of Italics, although not as serious as the aboveerrors, demonstrates lack of training in nomenclature and findingthe issue difficult. By placing scientific names in different fontsthey can be readily detected by computer and thus compared withstandard lists or detected by search engines. Such errors couldeasily be resolved during the preparation of the MS and as part ofthe editorial process.

4.8. Using names and reflecting taxonomies that are not currently‘accepted’ by modern regional floras and databases

It is common (and hard to avoid) that articles will use perfectlyacceptable published scientific names but which may no longer beconsidered the currently accepted name of that plant in moderntaxonomic treatments. Between 2.8% and 10% of papers did notused updated taxonomy at the time of their publication (Table 7).

The name used for a species in the paper will depend on thetaxonomic treatment being followed (which should be cited). Theinclusion of key synonyms, especially those used among the targetreadership, is also advisable to better communicate with thereadership. Names placed in synonymy may relate to differenttaxon concepts circumscribed in the sense of their taxon authors—end users of names may consider these concepts more useful andsensible than those ‘accepted’ names under which they are (oftentemporarily) placed. Classically trained pharmacologists know tosearch the literature for synonyms. To locate the synonymy for theplant the authors are studying Tropicos (2012) and TPL (2010)provide list of synonyms and subordinate taxa. Global initiativessuch as TPL (2010) provide the basic tools and help authors to keeptrack of accepted changes in the placement of taxa within generaand families. Our understanding of the evolutionary relationshipsbetween plant groups is developing fast including revisions basedupon new chemical, morphological and molecular evidence. About10 000 changes to plant names are published every year (achallenge for those institutions maintaining these global databasesAllkin, 2013) and ca. 40% of those occur when a taxonomist movesa species from one genus to another to better reflect the evidenceavailable. Another 40% relate to those cases where a species is splitinto two or more separate taxa or where two or more plants thatwere previously considered to be separate species become mergedinto one species. As these statistics indicate not all taxonomists orall taxonomic publications will agree and certainly over timeopinions as to the closest relationships of a species will change.

Using a published scientific name which is valid but is con-sidered to be an older synonym in current texts is thus notessentially wrong. However to use an older name which places aspecies within one genus when today it is considered to share anevolutionary history and consequently share more chemical as wellas morphological and molecular characteristics, can mislead readersas to which other plants are likely to have similar pharmacologicalprofiles.

Thus authors of pharmacological, phytochemical and ecologicalpapers, not skilled in the intricacies of plant taxonomy, againshould consult global databases like TPL (2010) which, even as a

working list will provide reviewed (“accepted”) scientific namesfor most plant species (c. 300 000) and further provide links to alltheir known synonyms. TPL (TPL) attempts to bring all plantnames together (merging existing digital taxonomic resourcesrecording synonymy) and imposes a single coherent classification.TPL relies on peer-reviewed monographic global treatments wherethese exist and where they do not resolves taxonomic conflictsamong the diverse regional data sets that were used. Reference toTPL may help overcome the requirement of including well knownsynonyms by the authors although the inclusion of synonyms in apaper (at least those that are most widely used) may make a papermore easily detected by search engines.

For now there is no search engine capable of making linksbetween synonyms, e.g. Tabernaemontana and Ervatamia. In thecontact of medicinal plant research and ethnopharmacology thismay be a manageable problem, but again requires a more stringentapproach by authors, reviewers and editors and more specifically,strategies for cross-linking taxonomic terms.

5. General recommendations

Basic requirements have been discussed above (e.g. the needfor depositing voucher specimens in recognized herbaria) andhere we provide some wider recommendations which go beyondthe current standards of individual journals. The application ofsimple principles in a systematic way and the use of some open-access resources can help authors, referees and editors of ethno-pharmacological papers to significantly improve in the use ofbotanical nomenclature and thus avoid the problems that com-promise the reliability, usefulness or impact of the articles. Whileof relevance in all fields where botanical nomenclature is essential,such recommendation must, by definition, be specific for eachjournal and require changes in the journal’s policy.

As part of the supplementary data authors should provide of alist of all scientific names of plants used in the text, tables andfigures carefully checked and corrected through consultation witha reliable database. Journals should provide (a template or onlineform (e.g. Fig. 2), and this includes reference to an appropriatevoucher specimen in a recognized herbarium (see above). Thesedatasheets could form part of the supplementary informationand require the author to provide all the data relevant from ataxonomic and botanical perspective.

As pointed out throughout this paper, rigorous assessment ofthe taxonomic nomenclature is a core part of this process. Itrequires a more proactive approach by all—authors, reviewers andeditors. Any procedure should start with a check (be it manual orautomatic) that the scientific names used have actually beenpublished. Concerning databases for checking names, there is aplethora of resources available on the web, including those linkedin the taxonomy browser of GenBank (NCBI, 2013), the EuroþMed(Euromed, 2011; Tropicos, 2012; USDA, 2013 and most importantlythe TPL (www.theplantlist.org). However, some of the aboveresources have considerable limitations, being restricted in termsof regional or taxonomic coverage.

Ideally an automated match would detect names embedded inthe article and “tag” these names with their unique identifierwithin a global database as the International Plant Name Index(IPNI, 2012). IPNI is the most complete and maintained referencesource for published plant names.

IPNI, however, does not offer information about synonymy nordistinguish between accepted names in the recent literature andolder synonyms. As a next step, therefore, prior to submissionauthors need to check their names against TPL (2010) which willidentify all scientific names and synonyms recorded so far.Currently, TPL contains more than one million scientific plant

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names and provides the accepted name for c. 300 000 species ofvascular plants and bryophytes and their known (480 000) syno-nyms. The remainder of the scientific names in TPL (240 000) arepotentially accepted species names (termed “unresolved”) but forwhich further peer review is still needed to confirm this.1

A second version of TPL was published in 2013.Of course, a prerequisite for working with TPL or IPNI is to

search the database entering the names to be used withoutorthographic error. The result will be a list of one to several nameslabeled as “accepted”, “unresolved”, �or “synonym”. Names labeledas accepted or unresolved may readily be used and are valid.Synomyms would be ideally replaced by their current acceptedname or at least cited together with the current accepted name.One advantage of such a check is that the author of the article (andthe editors) can be confident that the same species is not listedtwice within the article under alternative synonyms.

It is essential to cite the author(s) of the name concerned in acorrect and standardized form. Brummitt and Powell (1992)provide unambiguous standard abbreviations, in conformity withthe recommendations of the Code for a large number of authors ofplant names, e.g. L. for Linnaeus and not Linn. or Linne, Theseabbreviations, as mentioned in Rec. 46A Note 1 (McNeill et al.,2011), are also adopted and updated by the International PlantNames Index (IPNI, 2012) which is an extension and maintainedversion of Brummitt and Powell (1992). These standard abbrevia-tions should be used in the naming of plants (see ⟨http://www.ipni.org/ipni/authorsearchpage.do⟩). TPL (2010) uses names takenfrom many different databases—WCS, TROPICOS, ILDIS, IPNI, etc.which do not consistently use the same abbreviations. Wherepossible TPL follows usage in IPNI but this is not always the caseand should not be relied upon. For historical reasons (IndexKewensis) although standardized abbreviations are used exhaus-tively, the authorship of some combinations published in the 18th19th and early 20th centuries is not clearly stated in IPNI (2012).For example: Sideritis alopecuros Scop. is used instead of Sideritisalopecuros (L.) Scop. or Salvia armeniaca Grossh. instead of Salviaarmeniaca (Bordz.) Grossh. Therefore it is preferable to use TPL(2010 and later versions). These resources are being curated andimproved and will increasingly become more complete, betterintegrated, more current and more easily used to match lists ofplant names.

As the most simplistic but crucial take home message forauthors, it is essential to use the current version of TPL and thiswill resolve the vast majority of problems.

6. Conclusions

The above analysis gives rise to a range of short and mediumterm recommendations relevant to editors, publishers, reviewersand authors:

- Most journals in the field have a policy requiring authors todeposit voucher specimens in a recognized herbarium. It wouldbe advisable that journals reinforce this policy and that thesevoucher specimens are fully cited (with collector, collectornumber and herbarium) within the article. Furthermore, ajournal may want to require that electronic scans of thespecimens need to be included in the supplementary data,

most importantly in case of uncommon species, or wheretaxonomic identity may be ambiguous.

- In addition to the specimen citation it is advisable thatevidence for the identity of the plants seen is documented.This may be through the citation of the names of those thatidentified (determined) the specimens and the botanical refer-ence resources and keys used to undertake each identification.

- In view of the many errors with scientific names and taxonomicplacement it would be advisable to have within the journal’ssubmission process a mandatory section requiring authors toprovide a digital list of all names used which could then becompared against existing taxonomic databases most impor-tantly www.theplantlist.org. Alternatively the scientific namescited within articles could themselves be marked using semanticmark up so that they could be detected, searched for and checkedby machine.

- Journals and editors need to reinforce their policies on accurateand validated names of taxa. A key part of this could be a formlike the one proposed in Fig. 2. Instructions to authors mustunderline the need for using scientific plant names andstandard author abbreviations more clearly. A detailed reviewof the botanical nomenclature used in each article would bemore easily completed using the online resources cited above.

- Most critically, however, the issues of taxonomic identity andnomenclature would ideally be addressed at a much earlierstage in each research project and long before the manuscript isin preparation. During development and implementation ofany ethnopharmacological project, close attention should bepaid to these aspects, which in some areas may require morefocus on teaching and training. Taxonomic methodologies andpractices remain poorly covered in graduate and postgraduatetraining and reviewers need to more alert to the need for suchquality assurance.

While we have used two examples of journals important in thefield, the comments made here are relevant for a wide range ofjournals and random checks in other publications in the fieldhave highlighted similar problems in these journals. Therefore,while some parts are specific most importantly to the Journal ofEthnopharmacology, the overarching recommendations are rele-vant in the entire field. The fast developing electronic technologiesoffers multiple opportunities to achieve a more precise taxonomicidentity.

Acknowledgements

We would like to thank the input of Emilio Laguna, DennisJohnson, Patricio Martínez and the anonymous reviewers.

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