Received: 11 October 2022 | Accepted: 24 May 2023 DOI: 10.1002/pan3.10511 RESEARCH ARTICLE Cultural importance, availability and conservation status of Spanish wild medicinal plants: Implications for sustainability J. Mateo-­Martín1,2 | G. Benítez3 | A. Gras4,5 | M. Molina6 | V. Reyes-­García7,8 | J. Tardío 6 | A. Verde9 | M. Pardo-­de-­Santayana1,10 1 Departamento de Biología (Botánica), Universidad Autónoma de Madrid, Madrid, Spain; 2Programa de Doctorado en Biología, Escuela de Doctorado, Universidad Autónoma de Madrid, Madrid, Spain; 3Departmento de Botánica, Facultad de Farmacia, Universidad de Granada, Granada, Spain; 4Laboratori de Botànica—­Unitat Associada CSIC, Facultat de Farmàcia i Ciències de l'Alimentació—­Institut de Recerca de la Biodiversitat IRBio, Universitat de Barcelona (UB), Barcelona, Spain; 5Center for the Study of Human Health, Emory University, Atlanta, Georgia, USA; 6Instituto Madrileño de Investigación y Desarrollo Rural, Agrario y Alimentario (IMIDRA), Madrid, Spain; 7Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain; 8Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Barcelona, Spain; 9Instituto Botánico, Universidad de Castilla-­L a Mancha, Albacete, Spain and 10Centro de Investigación en Biodiversidad y Cambio Global (CIBC-­UAM), Universidad Autónoma de Madrid, Madrid, Spain Correspondence Manuel Pardo-­de-­Santayana Abstract Email: manuel.pardo@uam.es 1. The harvest of wild plants with medicinal uses is increasing globally, both for self-­ Funding information treatment and as a source of income. The increasing demand for these remedies Fundación Biodiversidad, Grant/Award could lead to the over-­harvest of some species. Despite a recent surge in the number Number: CA2015; H2020 European Research Council, Grant/Award of studies analysing wild medicinal plants management, little is known about the ef- Number: FP7-­771056-­LICCI; Ministerio fects of non-­commercial harvesting on the conservation status of medicinal plants. de Agricultura, Pesca y Alimentación, Grant/Award Number: TEC0003351 2. We explore the connection between the cultural importance (CI) of medicinal vas- and TEC0004583; Ministerio de Ciencia cular plants traditionally used in Spain for self-­treatment and their availability, con- e Innovación, Grant/Award Number: CEX2019-­0 00940-­M; Ministerio de servation and legal protection status, and discuss the implications of our results Economía y Competitividad, Grant/Award for sustainability. We focus on Spain, located in one of the world's 25 biodiversity Number: CSO2014-­59704-­P hotspots and the most diverse country in Europe regarding vascular plants (7071 Handling Editor: Carla Morsello species, 1357 endemic), while also being culturally and linguistically diverse. 3. Spain has a rich body of traditional knowledge referring to wild medicinal plants, with 1376 species with medicinal uses, which represents nearly a fourth (22%) of the total autochthonous vascular flora of the country (16% endemic). Species CI is positively correlated with abundance (ρ = 0.466) and occupancy area (ρ = 0.495). Only 8% of the wild medicinal plants traditionally used in Spain have an endan- gered conservation status and just 6% are fully or largely affected by protec- tion measures. Most species used for self-­treatment in Spain are common, highly available and not threatened. This suggests that domestic use alone does not result in overexploitation and that traditional knowledge systems of plant man- agement might ensure their sustainability. KEYWORDS biocultural conservation, ecosystem services, natural resources, pharmaceutical ethnobotany, Spain, wild plants gathering This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2023 The Authors. People and Nature published by John Wiley & Sons Ltd on behalf of British Ecological Society. People and Nature. 2023;00:1–14.  wileyonlinelibrary.com/journal/pan3 | 1 | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 2 People and Nature MATEO-­MARTÍN et al. 1 | I NTRO D U C TI O N While traditional harvest of medicinal plants might be sustain- able, the harvest of medicinal plants for commercial purposes may Around 7% of the 350,000 vascular plant species currently de- challenge sustainability by increasing extractive pressure and mod- scribed are considered medicinal (25,791 species; RBG Kew, 2020). ifying traditional norms that regulate extraction (Ganie et al., 2019; The World Health Organization estimates that between 70% and Niu et al., 2021). In that sense, there has been a recent surge in the 95% of the population in developing countries relies on traditional number of case studies analysing wild medicinal plants management medicines, mainly of plant origin, for primary healthcare (Robinson (e.g. Senkoro et al., 2019). These studies have considered elements & Zhang, 2011). Medicinal plants are not only used for self-­ such as species supply (i.e. availability) and demand (i.e. quantities treatment but also as an important source of income (IPBES, 2022). of plant material being exploited), conservation status and impact Moreover, the use of medicinal herbs is expanding, especially after of the harvesting method (e.g. harvesting subterranean parts vs. the COVID-­19 pandemic (Smith et al., 2021; Timoshyna et al., 2020; leaves; Benítez et al., 2010; Cunningham et al., 2019). Some stud- WHO, 2019), their global trade reaching USD 138 billion in 2019 ies have analysed the depletion risks of plants traditionally used (Industry Research Biz, 2020), with an average annual growth of as medicine, or have proposed strategies to improve coordination 2.4% in volume and 9.2% in value (Vasisht et al., 2016). Although between conservation scientists and medicinal plant practitioners China and India have historically dominated the medicinal plants’ (see e.g. Cheung et al., 2021; Gonçalves et al., 2022). Previous stud- market, the increasing global demand has already resulted in the ies empirically analysing the impact of harvest of medicinal plants expansion of the sector in other countries (Caporale et al., 2020). sustainability have focused on small geographical areas, on a single The growing demand for medicinal plants has led to unmonitored species of particular interest, or on the exploitation of medicinal commercial gathering, which has resulted in the over-­harvest of products for income; moreover, several of them only rely on har- some species (Ganie et al., 2019; Larsen & Olsen, 2007). Indeed, of vester's perceptions of scarcity as a measure of sustainability (e.g. the 5411 plants with medicinal use assessed by the International Chen et al., 2016; Cunningham et al., 2018; Kunwar et al., 2020; Union for the Conservation of Nature (IUCN) Red List of Threatened Papageorgiou et al., 2020; Timmermann & Smith-­Hall, 2019). Species, 723 (13%) are threatened (RBG Kew, 2020). Therefore, While informative, the case study approach predominant so far there is an urgent need for actionable knowledge that helps avoiding limits our ability to identify general trends, particularly considering that that the increasing use of medicinal plants jeopardizes their sustain- medicinal plants can be gathered in different places and display func- ability (Kumar et al., 2021). tional redundancy. To detect these general trends, national and global Over-­harvest of plants with medicinal uses is considered a level analyses of the impact of harvesting medicinal plants are more threat to their sustainability. While some tools have been proposed informative. For example, in a national study conducted in Indonesia, to quantify medicinal plants' vulnerability to overharvest (Castle Cahyaningsih et al. (2021) assessed the species' rarity, occurrence sta- et al., 2014), a main setback in assessing harvesting impact lies on tus, and part gathered to recommend the prioritization of several me- the lack of a consensual definition of sustainability. In strict sense, dicinal species for conservation. In the same line, a global assessment sustainable harvesting refers to harvest that does not lead to a pop- of the risks of medicinal plants gathering showed that medicinal plants ulation decline and allows for a population growth rate of at least 1.0 tend to have larger native ranges than species not reported as medici- (Svenning & Macı́a, 2002). Under such definition, assessing sustain- nal, and therefore have lower mean extinction risks (Howes et al., 2020), able harvesting requires in-­depth studies that consider the species' something that needs to be analysed in detail at the regional level. life form, growth and extraction rate, population size, part harvested Despite the potential contribution of analyses that go beyond the and extraction techniques used, in addition to other environmen- case study and engage in national or global analyses to detect the sus- tal variables such as climate (Ticktin, 2015). Given the difficulty of tainability of medicinal plant harvest, they are uncommon. To help fill collecting all these empirical data for all medicinal plant species, an this gap, in this work, we conduct a national-­level analysis exploring alternative operational definition of sustainable harvest refers to the the relations between the availability and the cultural importance (CI) long-­term use of a species without exhausting it. Indeed, research of wild medicinal vascular plants traditionally used in Spain. We then shows that many traditional societies have promoted strategies that discuss the implications of this relation for medicinal plant harvesting. accommodate the use of a species with its natural growth rate, thus In particular, we analyse the association between species' CI and (1) allowing its long-­term use (Morales et al., 2011; Turner et al., 2022; abundance, (2) occupancy area, (3) endemicity and (4) conservation Verschuuren et al., 2010). Examples of strategies intended to ensure and protection status. We focus on Spain because, being settled in sustainable harvest include limiting the proportion of individuals one of the world's 25 biodiversity hotspots, Spain is the most diverse gathered to allow reproduction (e.g. Sideritis raeseri Heldr. & Boiss; European country regarding vascular plants (CBD, 2020). Nearly a Tomasini, 2019); gathering only the part with active components quarter of Spanish flora (7071 species) is endemic: 1823 endemic thus diminishing plant damage (e.g. Paris polyphylla var. yunnanensis taxa, 1357 species (Aedo et al., 2013; Buira et al., 2020). Spain is also (Franch.) Hand.-­Mazz.; Qin et al., 2018); promoting species in their the European country with the highest number of species threatened natural environments through seeds dispersal (e.g. Angelica arch- with global extinction (Holz et al., 2022). Moreover, from a cultural angelica L.; Rautio et al., 2016); or transplanting species into home perspective, Spain has a high cultural and linguistic diversity that has gardens (e.g. Limnophila aromatica Merr.; Cruz-­Garcia & Struik, 2015). propitiated the constant exchange of plants, knowledge and practices, | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License MATEO-­MARTÍN et al. People and Nature 3 and a rich ethnobotanical tradition (El-­Gharbaoui et al., 2017). Recent field work and interviews, thus excluding reviews and meta-­analyses research estimates that 3000 vascular plants have traditionally been of pre-­existing data, and (2) they are written in English, Spanish, used in Spain (Pardo-­de-­Santayana et al., 2014), being medicinal Catalan, Basque or Galician (Pardo-­de-­Santayana et al., 2014). The plants the largest use category. Indeed, medicinal plants provided a repository has also been complemented with the original infor- main pillar for health self-­care in Spain until the 1950s, when deep mation contained in the database of the citizen science platform changes in lifestyle associated to industrialization and globalization CONECT-­e (http://www.conec​te.es/; Reyes-­García et al., 2021). At (Quave et al., 2012) led to a significant loss of this body of knowledge the time of conducting this analysis, the IECT repository included (Gómez-­Baggethun et al., 2010). Nowadays, the gathering of wild more than 500 publications. plant species to treat common illnesses continues to be prevalent in Information from the selected publications is collected and or- many rural households (Gras et al., 2020; Quave et al., 2012), their col- ganized in a database. Not all the publications selected have already lection being generally for self-­treatment. In fact, around 15 species been included in the database. Currently, the database includes a with medicinal use (e.g. Gentiana lutea L., Thymus spp., Chiliadenus glu- representative portion of the works in the repository, including pub- tinosus (L.) Fourr., Chamaemelum nobile (L.) All.) have been intensively lications that document the largest number of species and cover the harvested, although the gathering of these species is now in decline widest geographic area. To minimize repetition, when several pub- (Ministerio del Medio Ambiente, 2000). lications originate (or partially originate) from the same fieldwork (such as a thesis and subsequent publications), only the initial work and those follow-­up papers that add new species or uses have been 2 | M ATE R I A L S A N D M E TH O DS included. For the work presented here, the database was filtered to obtain only the list of wild autochthonous species for which medici- 2.1 | Data sources nal uses have been reported (Figure 1). A total of 158 publications (53 journal articles; 58 books; 30 This study combines ethnobotanical data, botanical data (from on- Ph.D. theses; 16 unpublished academic theses; one online database) line databases), and information from legal and conservation docu- appearing during 1982–­2020 met the aforementioned requirements. mentation (i.e. current conservation legislation and the Red list of The final list covers all the Spanish territory, as ethnobotanical pub- threatened species). Data are available at Zenodo (Mateo-­Martín lications were found for all the autonomous communities (the high- et al., 2023). est level of territorial organization in Spain; Figure 2; Mateo-­Martín Ethnobotanical data used in this work was collected as part of the et al., 2023: 1. Ethnobotanical references). Spanish Inventory of Traditional Knowledge Related to Biodiversity To estimate species' abundance, we used the online database of (IECT) project (Pardo-­de-­Santayana et al., 2014; Tardío et al., 2018). SIVIM (2022), which computerizes the phytosociological invento- Through the IECT project, during the last two decades, a team of ries carried out in Spain. Currently, the database includes 145,672 more than 130 ethnobotanical researchers has created a repository inventories. The species distribution area and endemicity was ob- of publications recording ethnobotanical uses documented in Spain. tained from Anthos (2022), an online platform containing taxonomic To populate the repository, IECT team members have located books, and cartographic information (based on bibliographical and herbaria theses, indexed and non-­indexed journal articles that meet two main geo-­referenced quotations) of the flora of the Iberian Peninsula, the criteria (1) they report ethnobotanical information that comes from Balearic Islands and the islands of Macaronesia. F I G U R E 1 Criteria considered for the selection of studies in the analysis of the sustainability of medicinal plant species in Spain. Complete list of final publications selected can be found in Mateo-­Martín et al. (2023: 1. Ethnobotanical references). | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 4 People and Nature MATEO-­MARTÍN et al. F I G U R E 2 Geographical reference of ethnobotanical documents used. The political division of Spain establishes three official levels of territorial organization: autonomous communities, provinces, and municipalities. Regions are traditional divisions of the territory that group several municipalities. The labels indicate the presence of at least one document at the administrative level specified. Species conservation status was obtained from the Spanish sources did not specify the used subspecies. This approach minimizes Red List of Vascular Plants (Red Book and Atlas of Endangered potential biases due to taxonomic disagreements. Plants, Moreno (2008), and its addendum, the National Red List of For the standardization of Iberian and Balearic plant names, we Endangered Flora, Bañares et al. (2010)). The document presents the followed Flora iberica Castroviejo (1986–­2021), and Arechavaleta list of threatened wild plants, highlighting the extinction risk they face, et al. (2010) for Canarian names not included in Flora iberica. This is and stablishing conservation priorities. The classification of threat especially pertinent for the scientific names included in the conser- levels follows the IUCN threat categories and sometimes refers only vation list and legal protection catalogues consulted, where differ- to threats at a subspecies level. Species included in the Red List are ent taxonomic treatments are used. In Mateo-­Martín et al. (2023) we not necessarily protected, as the list only indicates that the species provide the names used in each regulation and its synonyms (when threat status has been assessed. Protection status was sourced from applicable). Moreover, some species complexes, such as Taraxacum European, national, and autonomic legislation. For the European level, officinale L., Alchemilla vulgaris L. and Ornithogalum umbellatum L., we used the Habitats Directive (Council Directive 92/43/EEC of 21 are treated sensu lato since it was not possible to reassign their cita- May 1992); for the national level, we used the most recent National tions to currently accepted taxa. For the botanical families, we fol- Catalogue of Endangered Species dating from 2011 (Real Decreto lowed APG IV (APG, 2016). 139/2011); and for the autonomic level, we used the 17 autonomic We used Anthos (2022) to define species endemicity. Species conservation laws (Mateo-­Martín et al., 2023: 3. Legislation). were classified as mainland Spanish, Balearic and Canarian ende- misms depending on whether their occupancy area included grids exclusively in the Spanish portion of the Iberian Peninsula, in the 2.2 | Botanical and taxonomic treatment Balearic or the Canary Archipelagos. From each document, we extracted a list of wild autochthonous plant species used as medicine. For species that are both wild and culti- 2.3 | Variables studied vated (e.g. Laurus nobilis L., Rosmarinus officinalis L.), we included all ci- tations of medicinal use because it was difficult to distinguish whether For each medicinal plant in our list, we compiled data for six variables the published information referred to wild or cultivated plants. The re- grouped in three categories (i.e. CI, availability, and conservation and view was done at the species level because in most cases the original protection status). | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License MATEO-­MARTÍN et al. People and Nature 5 2.3.1 | Cultural importance where used, when species were mentioned by the European and national legislation, and when the regional legislation protected Species CI was defined as the sum of use-­reports (UR) of them in most or all areas where medicinal uses are documented. the species divided by the number of informants (Tardío & Pardo-­de-­Santayana, 2008). As in previous studies, each ethn- obotanical reference is treated as an informant (Tardío & Pardo-­de-­ 2.4 | Limitations of the study Santayana, 2016). Since we only consider one use category—­that is medicinal—­a species CI was calculated dividing the number of docu- Despite our efforts, compiling, standardizing, and using data from ments in which the species is mentioned as medicine (i.e. medicinal three different databases and several projects might have intro- UR) by the total number of references used (n = 158), obtaining an duced some bias, as each of our data sources has its own limita- index value that ranges from 0 to 1, where 1 means that the species tions. Ethnobotanical research in Spain shows a geographical bias was listed in the 158 documents used. in data collection, with some areas having received more scholar attention than others. As a consequence, some species may show higher frequency of citations, for example if their occupancy area 2.3.2 | Availability overlaps with better prospected areas (Reyes-­G arcía et al., 2021). We tried to minimize this bias by selecting works that encom- Species availability was assessed through abundance and occupancy pass the whole territory and are representative of the country. area. Species abundance was estimated with the number of phyto- Regarding abundance, researchers tend to focus on areas of higher sociological inventories on the online database SIVIM (2022), which botanical interest, or closer to research centres (Izco, 1981). Lack registers the presence of the species on a plot. We classified spe- of homogeneity in the distribution of the botanical information cies abundance into four categories: highly abundant (species pre- across the territory might bias our measure of both species' abun- sent >1000 inventories), moderately abundant (500–­999), common dance and occupancy areas. Besides, as this information was not (50–­99) and rare (<50). We followed IUCN (2012) to define occu- available, we only analysed the number of inventories for each pancy area as the area occupied by a taxon within its extent of oc- plant, without regarding the phytosociological index associated currence. Species occupancy area was estimated using the number with the plant in each inventory (from + and 1 to 5, different in of 10 × 10 km UTM grids in which each species was quoted in the each inventory; Braun-­B lanquet, 1928), which more accurately re- Anthos (2022) database. We established four categories for occu- flects its abundance in the inventoried space. pancy area: wide (species present >300 grids), moderate (100–­299), Dealing with species' protection categories can also be challeng- narrow (10–­99) and very narrow (<10 grids). ing, since autonomous communities legislation is not always founded on the assessment of species conservation status. Moreover, reg- ulations are highly diverse and do not have homogeneous criteria 2.3.3 | Conservation and protection status for protection as they are based on different conservation status categories. Thus, some laws refer to categories equivalent to the To determine a species conservation status, we analysed the pres- IUCN threat categories (e.g. AN 2012; CN 2010; Mateo-­Martín ence of medicinal plant species in the Spanish conservation list et al., 2023: 3. Legislation, 4. Protection), while others include cat- (Bañares et al., 2010; Moreno, 2008). As we worked at the spe- egories such as ‘special interest species’ (e.g. MC 2003; CT 2008), cies level, when a threat category was documented for one or ‘sensitive to habitat alteration’ (e.g. NC 1997; MD 1992), ‘regulated several subspecies present in Spain, we applied that threat cat- achievement’ or ‘preferential attention’ (e.g. CL 2007; Mateo-­Martín egory to the whole species. Infraspecific taxa not accepted by et al., 2023: 5. Protection categories). Regional protection laws also Castroviejo (1986–­2021) were not considered. To measure a spe- largely differ in the number of protected species (e.g. 188 species cies' protection status, we considered three levels of regulation: in Murcia, but only one in La Rioja and Cantabria). Some categories European, national and autonomic. Some species are protected allow the collection of specific quantities (e.g. a licence is required only in certain autonomous communities, or the protection affects for collecting more than 2 kg of Santolina oblongifolia Boiss. in Castile only one of its infraspecific taxa (e.g. Senecio pyrenaicus L. in Loefl. and Leon, where the species is considered under the category ‘reg- subsp. carpetanus (Willk.) Rivas Mart. (regulation EX 2001)). To re- ulated achievement’) while other categories restrict the collection flect this diversity, species were classified into three categories of the species in specific locations (e.g. the gathering of Digitalis ob- based on how the aforementioned legislations affects gathering: scura L. is strictly forbidden in the area of Cerros de Almatret, Lérida, (a) gathering always allowed, when the species do not appear in where the species is considered a ‘special interest species’). These any documents; (b) gathering allowed where used, when the au- specifications may indicate that a species is not genuinely protected tonomic legislation protects them in a small portion of the areas in the area where medicinal uses are documented or that a certain where medicinal uses had been documented, or when species are amount of it may be legally harvested, although the species is con- documented as medicinal in autonomous communities where they sidered protected, which may have led to an overestimation of the are not subject to legal protection; and (c) gathering restricted number of protected species. | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 6 People and Nature MATEO-­MARTÍN et al. 2.5 | Data analysis 3 | R E S U LT S Information was compiled in a Microsoft Excel datasheet (Mateo-­ 3.1 | Wild species used as medicine Martín et al., 2023). Here we provide a descriptive summary of the six variables studied, highlighting examples of representative medicinal The analysis of the 158 documents resulted in a list of 1376 autoch- wild species. We also test the level of correlation among three of the thonous wild vascular plant species traditionally used as medicine variables, that is, CI, abundance and occupancy area. We performed in Spain (Mateo-­Martín et al., 2023: 2. Medicinal species). These a Kolmogorov–­Smirnov test (with significance correction of Lilliefors) species belong to 120 botanical families: 38 ferns (13 families), that showed that none of the variables followed a normal distribution. 20 gymnosperms (four) and 1318 angiosperms (103). Asteraceae Therefore, to assess the correlation between pairs of variables, we (202 species, 15% of the medicinal species) and Lamiaceae (151, 11%) used a bilateral Spearman correlation test with a 99% of confidence are the botanical families with a higher number of species (Figure 3). level (α = 0.01). As the CI variable followed a gamma distribution, we A total of 160 (14%) medicinal species are considered endemic performed a gamma generalized linear model to compare CI averages to the study area. Six species in our list are endemic to the Balearic between the protected species and the whole dataset. All the statisti- Islands, 82 to the Canary Islands and 72 to mainland Spain (Figure 4; cal analyses were conducted in R v.4.1.1 (R Core Team, 2021). Mateo-­Martín et al., 2023: 2. Medicinal species). 2.6 | Ethics statement 3.2 | CI of medicinal wild species We followed the code of ethics of the International Society of On average, each species was mentioned in 5.4% of the documents Ethnobiology (ISE, 2006). (avg. CI = 0.054), with a great disparity in species' CI (standard deviation F I G U R E 3 Number and percentage of wild species used as medicine in Spain, per family (n = 1376). F I G U R E 4 Distribution of endemic plant species with medicinal use. | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License MATEO-­MARTÍN et al. People and Nature 7 F I G U R E 5 Cultural importance (CI, green bar), abundance (ABU, yellow dot) and occupancy area (OCP, purple dot) of the 35 wild species with medicinal use with CI > 0.35. 0.093; max = 0.80, min = 0.01). The five species with the highest CI are CI > 0.35, 32 (91%) have a wide distribution and the remaining three Rosmarinus officinalis (CI = 0.80), Malva sylvestris L. (0.70), Foeniculum (9%) have a moderate distribution (Figure 5). While some widely dis- vulgare Mill. (0.65), Origanum vulgare L. (0.63), and Sambucus nigra L. tributed species are very frequently used as medicine (e.g. Rubus ul- (0.63). Only 35 species (3% of the total) appear in more than 35% of mifolius Schott.; 1508 grids; CI = 0.47), for others, the medicinal use the documents (CI > 0.35; Figure 5), whereas 332 species (24%) appear is uncommon (e.g. Briza maxima L.; 975; CI = 0.01). in more than 5% (CI > 0.05). The less quoted 665 species (48%) had a CI Compared to the full sample, endemic species have a lower CI of 0.01 (i.e. were cited in less than 1% of the references). (0.014 vs. 0.054). Also, most endemic medicinal species have a nar- row (78% vs. 28%) or very narrow (12% vs. 3%) occupancy area, and according to their abundance, most can be considered common (42% 3.3 | Wild species availability vs. 34%) or rare (50% vs. 13%). On average, each species appears on 1157 inventories, although there is a very high variation among species abundance (standard 3.4 | Wild species conservation and deviation = 1719; max = 19,229; min = 1). About one third of the spe- protection status cies (34%) appeared in more than 1000 inventories and are thus cat- egorized as “highly abundant”, 18% of the species are “moderately Only 8% (89 species) of the medicinal plant species were found in abundant” and 34% are “common”. Only 13% of the species with me- the Spanish Red List of Endangered Flora (Moreno, 2008). Among dicinal use were cited in less than 50 inventories and are considered them, 12 are considered critically endangered, eight endangered, 45 “rare”. Of the 35 species with CI > 0.35, 28 (80%) are “highly abun- vulnerable and 24 belong to less threatened categories. For about dant”, 6 (17%) are moderately abundant and only one species (3%) half of the species in the list (41 species), the threatened conserva- is common (see Figure 5; Mateo-­Martín et al., 2023: 2. Medicinal tion status specifically pertains only to one of the various infraspe- species). Some very abundant plants have high CI (e.g. Crataegus cific taxa present in Spain. An example of this is Centaurea aspera L. monogyna Jacq.; 11,201 inventories; CI = 0.54), whereas others have that was considered as endangered, although only the subspecies low (e.g. Dactylis glomerata L.; 19,299; CI = 0.01). scorpiurifolia (Dufour) Nyman appeared in the Red List (see Mateo-­ Regarding occupancy area, a medicinal wild plant species was Martín et al., 2023: 4. Protection, for further details). found in an average of 274 UTM grids (standard deviation = 253.8; Only about one third of the medicinal plant species (n = 430, 31%) max = 1732; min = 1). Overall, 494 species (36%) had a wide occu- have some type of protection status, being found in the consulted legal pancy area, 461 (34%) a moderate, 386 (28%) a narrow, and only catalogues (Figure 6; Mateo-­Martín et al., 2023: 4. Protection). From 35 (3%) a very narrow occupancy area. Within the 35 species with these catalogues, 15 species are mentioned in the European legislation, | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 8 People and Nature MATEO-­MARTÍN et al. 17 in the National Catalogue, and 425 in autonomous communities' However, out of the 430 protected species, only 85 species (6% catalogues. There are only six species listed at the three levels, 15 spe- of the total sample) receive some level of protection in the specific cies at two and 409 species at one level, mostly the autonomous com- area where medicinal uses have been documented. This situation munity (Mateo-­Martín et al., 2023: 4. Protection). occurs either because they are included in the European or na- The level of protection of the species listed in the catalogues var- tional legislation (five species), because their use-­area overlaps with ies greatly across autonomous communities. About half of the 430 the provinces where regional laws protect them (63), or both (17). species with legal protection status are solely monitored for their Regional legislation does not restrict the gathering of the remain- uniqueness, scientific, ecological or cultural value, and belong to cat- ing 345 plants, which are mostly documented as medicinal in areas egories such as “regulated management”, which allows the gathering where they are not subject to legal protection. Thus, when consid- of specific amounts of plant material under certain circumstances. ering species that are not listed in the consulted catalogues and spe- However, 211 species (15% of the sample) fall into highly restrictive cies whose gathering is not restricted in areas where medicinal uses protection. These include three species in our list that are consid- are documented, we find that 1291 species (94%) are not affected by ered as “locally extinct” (Buxus balearica Lam. and Taxus baccata L. any protection measure (Figure 6). in Murcia and Glaucium flavum Crantz in Cantabria); 46 species that The 85 medicinal species affected by some level of protection are regarded as “endangered” (e.g. Laserpitium latifolium subsp. ne- were only mentioned in 2.7% of the ethnobotanical references, thus vadense Mart. Lirola, Molero Mesa & Blanca in Andalusia); and 164 their CI was lower than that of the total list (average protected spe- species considered “vulnerable” (e.g. Aconitum napellus L. in Castile-­La cies CI = 0.027 vs. 0.054; standard deviation = 0.046 vs. 0.093; max- Mancha and Community of Madrid; see Mateo-­Martín et al., 2023: 4. imum = 0.32 vs. 0.80, minimum = 0.01). Protection, and 5. Protection categories, for further details). In some cases, these categories imply the creation of restoration plans or spe- cies or habitat conservation plans. 3.5 | CI, availability and protection status of wild medicinal species Species' CI bears a positive and statistically significant association, although moderate, with both species' abundance (ρ = 0.466; p < 0.01; Figure 7a) and occupancy area (ρ = 0. 495; p < 0.01; Figure 7b). The highest correlation was found between species' occupancy area and abundance (ρ = 0.830; p < 0.01; Figure 7c), probably because both variables reflect the species' availability. This correlation was statis- tically significant and strong. The average CI of the protected species is significantly lower than that of the total list of medicinal species, as proved by the gen- eralized linear model performed (Pr(>F) = 0.0006). 4 | DISCUSSION F I G U R E 6 Protection status of Spanish medicinal plants Spain has a rich traditional knowledge referring to medicinal (n = 1376). plants. The 1376 wild plants with medicinal use reported in this F I G U R E 7 Scatterplots and correlation coefficient of cultural importance (CI), abundance (ABU) and occupancy area (OCP). (a) Correlation of CI and ABU. (b) Correlation of CI and OCP. (c) Correlation of ABU and OCP. | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License MATEO-­MARTÍN et al. People and Nature 9 work represent nearly one-­fourth (22%) of the total autochtho- inflorescences of Sideritis hyssopifolia L. to encourage reproduction, nous vascular flora of Spain (Aedo et al., 2013). This percentage is planting cuttings of Sambucus nigra (authors' personal obsesrvation) comparable to data from countries like Nepal (21%), smaller than in or cultivating species such as Thymus moroderi Pau ex Martínez at countries with richer medicinal ethnofloras (e.g. India 44%; Kunwar small scales (Marco-­Medina, 2010). A list of these and other exam- & Bussmann, 2008) but considerably higher than the global estima- ples is provided (Table 1: Examples of documented medicinal plants tion of 7% plant species with medicinal uses (RBG Kew, 2020). The management practices that might contribute to the long-­term via- botanical families with a higher proportion of wild medicinal plants bility of the species). Indeed, at least some evidence suggest that in Spain correspond to those dominant in the medicinal floras of the the abandonment of traditional landscape management practices world (Moerman et al., 1999) and belong to the most relevant fami- may have potentially resulted in the population decline of some lies in the Spanish flora: Asteraceae, Lamiaceae, Fabaceae, Rosaceae species with medicinal uses. For example, the population of bitter and Apiaceae (Buira et al., 2017). The medicinal use of the species chamomile (Chamaemelum nobile) has declined as a result of the with the highest CI (e.g., Rosmarinus officinalis, Malva sylvestris, meadows no longer being grazed, which encourages the growth of Foeniculum vulgare, Sambucus nigra or Matricaria chamomilla L.) has other species (Pardo-­de-­Santayana & Morales, 2006). been documented since ancient times (El-­Gharbaoui et al., 2017; The finding that a species CI correlates with its availability aligns Quave et al., 2012). The chemical compounds and main pharmaco- well with the premise that care and management practices of use- logical properties of these species have been largely studied (Barnes ful wild species often ensure the long term viability of the resource et al., 2007) and many of these species, or their derivates, are nowa- (Fisher et al., 2019; IPBES, 2022; Turner et al., 2022). Prior research days used in basic healthcare (Carvalho & Morales, 2010) as they are has shown that individuals place a higher value on species that are easily available, gathered from the wild, cultivated in home gardens, used in everyday life than on species that are gathered for commer- or purchased from herbal shops or supermarkets (Quave et al., 2012). cial purposes. When a species is emotionally valued, as opposed to Culturally important species with medicinal uses are generally just being collected for profit, it is more likely that it will be managed available, as defined by their abundance and occupancy area. The for long term viability (Freitas et al., 2020; Pardo-­de-­Santayana & 35 species with the highest CI had wide or moderate occupancy Macía, 2015; Quave & Pieroni, 2015; Senkoro et al., 2019). In fact, area, and just one (Matricaria chamomilla, a species that is commonly only 8% of the documented medicinal plants have an endangered cultivated or obtained from markets) was classified as common. conservation status, and have been included in the Spanish conser- We venture to guess that several of them would qualify as Cultural vation list. Furthermore, as in many cases the endangered status re- Keystone Species, due to their high CI, versatility and symbolism in fers only to infraspecific taxa, the share of medicinal plant species society (Cristancho & Vining, 2004; Garibaldi & Turner, 2004), al- with endangered conservation status might be even smaller. Most though—­so far—­only one, Urtica dioica L., has been documented in (69%) of the wild species with medicinal uses do not appear in any the latest compilation of cultural keystone species (Reyes-­García legal protection catalogues, and only 6% have a restrictive protec- et al., 2023). Among the species with highest CI there is an Iberian tion category that affects gathering in the area where they are used endemism, Thymus mastichina (L.) L., widespread in the territory and as medicines. Many medicinal plants seem to be used in areas where that has even been locally cultivated (Blanco, 1998a). The overlap they are common and abundant, and therefore not protected. While between species CI and availability dovetails with previous research current availability might be partly explained by decreasing use, the suggesting that most plant species used as traditional medicines are fact that most wild species with medicinal uses are highly available abundant (Gaoue et al., 2017), including weeds or plants present in and not protected seems to suggest that the current harvesting disturbed habitats (Stepp & Moerman, 2001). However, as the pos- of such species is regulated by management practices that ensure itive correlations between CI, abundance, and occupancy area are their long term viability, as it has also been documented in other not very strong and many widely available plants have low CI, our areas (Morales et al., 2011; Senkoro et al., 2019; Turner et al., 2022; findings also suggest that, besides availability, other criteria are rel- Verschuuren et al., 2010). Similar conclusions were found in a study evant in the selection of wild plants as medicines. Beyond species' that reviews the medicinal plants used globally (Howes et al., 2020). pharmacological properties, such criteria might include aspects such Our study allows to identify a few wild plants with medici- as aromatic or visual qualities (Leonti et al., 2020). nal uses with threatened status. One of the few cases in Spain in While the correlation found in our data between CI and avail- which gathering for medicinal purposes has promoted the species' ability does not explicitly imply causality, in the reviewed refer- scarcity and threat of extinction, is the case of Artemisia granaten- ences we found several examples signalling that, in Spain, local sis Boiss., an endemism of Sierra Nevada, highly marketed for its populations engage in care and management practices that might multiple medicinal uses (Molero-­Mesa et al., 2014). This species actively maintain medicinal plants' populations stable over time. For is included in the national and regional catalogues (Mateo-­Martín instance, Osmunda regalis L. collectors keep its location secret, har- et al., 2023: 3. Legislation), in the European Red List of Vascular vest only a part of the rhizome or even transplant it into their home Plants (Bilz et al., 2011), and in the European Red List of Medicinal gardens (Molina et al., 2009): all practices that protect the species. Plants (Allen et al., 2014) as critically endangered. Other medicinal Other practices documented in the references that might contrib- plant species that have suffered from intense gathering exacer- ute to protect medicinal species include gathering a part of the bated by their commercialization, include Arnica montana L., Atropa | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 10 People and Nature MATEO-­MARTÍN et al. TA B L E 1 Examples of documented medicinal plants management practices that might contribute to the long-­term viability of the species. Species Management or harvesting practice Reference Arbutus unedo L. Cultivated in home gardens Benítez (2009) Artemisia absinthium L. Cultivated in home gardens Benítez (2009) Artemisia alba Turra Only aerial parts are collected Authors' personal observation Informants indicate that they are aware of the scarcity and control its (Serranía de Cuenca, Spain) collection Centaurium erythraea Rafn Cultivated in home gardens Benítez (2009) Chiliadenus glutinosus (L.) Only aerial parts are harvested Authors' personal observation Fourr. Informants indicate that they are aware of the scarcity and control its (La Manchuela, Spain) collection Crataegus monogyna Jacq. Cultivated in home gardens Benítez (2009) Laurus nobilis L. Cultivated in home gardens Benítez (2009) Matricaria chamomilla L. Cultivated in home gardens Benítez (2009) Origanum vulgare L. Cultivated in home gardens Benítez (2009) Osmunda regalis L. Keeping the location secret Molina et al. (2009) Harvesting only a part of the rhizome Transplanting to home gardens Sambucus nigra L. Planting cuttings Authors' personal observation Sideritis hyssopifolia L. Gathering a part of the inflorescence Authors' personal observation Sideritis spp. Harvesters use lowland substitutes instead of using species of high summits Benítez et al. (2016) of these genera. Lowland species are more common. High summit ones are more restricted, less abundant, and mostly grow in protected areas where gathering is not allowed (e.g. S. glacialis vs. S. hirsuta) Tilia platyphyllos Scop. Harvesting only the flowers Authors' personal observation (Serranía de Cuenca, Spain) Thymus moroderi Pau ex Cultivated in home gardens Marco-­Medina (2010) Martínez Thymys zygis Loefl. ex L. Cultivated in home gardens Benítez (2009) Thymus spp. Harvesters use lowland substitutes instead of using species of high summits Benítez et al. (2016) of these genera. Lowland species are more common. High summit ones are more restricted, less abundant, and mostly grow in protected areas where gathering is not allowed (e.g. T. serpylloides vs. T. zygis) Valeriana officinalis L. Cultivated in home gardens Benítez (2009) belladonna L., Ceterach aureum (Cav.) Buch, Dictamnus hispanicus 5 | CO N C LU S I O N S Webb ex Willk., Gentiana lutea, Ruscus aculeatus L., Santolina ob- longifolia, Saxifraga vayredana Luizet and Thymus sp. pl., some of We present the first comprehensive list of wild plants tradition- them present in the Habitats Directive. A few of these traditionally ally used in Spain as medicine and their associated CI, availability used species had entered the pharmaceutical industry, which might and conservation and protection status. Our results suggest that, explain their high levels of exploitation. For example, Atropa bella- in Spain, most wild plants with documented medicinal uses are donna, which pharmacists intensely harvested during the 1950s and abundant, widely distributed and hold a non-­threatened conserva- 1960s, has currently disappeared from some of the areas where it tion status, for which they largely do not require protection. While was collected (Verde et al., 2008). In the case of Saxifraga vayre- determining the sustainability of the harvesting of wild plants with dana, a species endemic to a relatively narrow area in Catalonia, its medicinal uses, in the strict sense of the term, would require the use use transitioned from folkloric to industrial (Bonet & Vallès, 2006) of data that are not available for most species, based on our results as it became an ingredient of a phytomedicine, which increased the showing a correlation between species CI and availability, we argue pressure on the species (Seoane et al., 1991). Hundreds of tonnes that—­at large—­the harvest of wild plants for medicinal use does not of several species of Thymus are harvested, 90% of which are des- pose a threat to their sustainability. Our results also suggest that tined for export. Plants are directly uprooted, and although it has the situation is different for a few wild and uncommon species not been proven to have harmed their populations, it is considered used for commercial purposes, which also happen to be protected to accelerate soil erosion in an already particularly dry and arid en- by the current legislation. Together, the two findings make good vironment (Blanco, 1998b). ground to support the argument that traditional systems of care and | 25758314, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1002/pan3.10511 by Readcube (Labtiva Inc.), Wiley Online Library on [28/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License MATEO-­MARTÍN et al. People and Nature 11 management of important wild plant species do not threaten their A. Gras https://orcid.org/0000-0002-2256-3256 long-­term viability. M. Molina https://orcid.org/0000-0002-4987-8637 As bodies of local knowledge and associated management prac- V. Reyes-­García https://orcid.org/0000-0002-2914-8055 tices are rapidly being lost in western societies, the revitalisation J. Tardío https://orcid.org/0000-0003-1690-1666 and integration of this knowledge could promote the sustainable A. Verde https://orcid.org/0000-0002-6461-5472 use of biodiversity. It is imperative that the different stakeholders M. Pardo-­de-­Santayana https://orcid.org/0000-0001-9406-4758 interested in safeguarding these species, make more efforts to inte- grate traditional and scientific knowledge for achieving an effective, REFERENCES social, legitimate and sustainable relationship with nature. In many Aedo, C., Medina, L., & Fernández-­Albert, M. (2013). Species richness and regions, such as Spain, further research is needed to assess the rela- endemicity in the Spanish vascular flora. 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