Journal of Ethnopharmacology 122 (2009) 60–67

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Journal of Ethnopharmacology

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Cultural significance of medicinal plant families and species among Quechua farmers in Apillapampa,

Evert Thomas a,∗, Ina Vandebroek b, Sabino Sanca c, Patrick Van Damme a a Laboratory of Tropical and Subtropical Agriculture and , Ghent University, Coupure links 653, B-9000 Ghent, Belgium b Institute of Economic , The New York Botanical Garden, 2900 Southern Boulevard, NY 10458, USA c Asociación de Jampiris de Apillapampa, Apillapampa, Bolivia article info abstract

Article history: Ethnopharmacological relevance: Medicinal plant use was investigated in Apillapampa, a community of Received 16 August 2008 subsistence farmers located in the semi-arid Bolivian . Received in revised form 5 October 2008 Aim of the study: The main objectives were to identify the culturally most significant medicinal plant Accepted 26 November 2008 families and species in Apillapampa. Available online 3 December 2008 Materials and methods: A total of 341 medicinal plant species was inventoried during guided fieldtrips and transect sampling. Data on medicinal uses were obtained from fifteen local Quechua participants, Keywords: eight of them being traditional healers. Informant consensus Emic perception of efficacy Results: Contingency table and binomial analyses of medicinal plants used versus the total number of Use quality inventoried species per family showed that Solanaceae is significantly overused in traditional medicine, Andes whereas Poaceae is underused. Also plants with a shrubby habitat are significantly overrepresented in the Quantitative ethnobotany medicinal plant inventory, which most likely relates to their year-round availability to people as compared Cultural importance indices to most annual plants that disappear in the dry season. Our ranking of medicinal species according to cultural importance is based upon the Quality Use Agreement Value (QUAV) index we developed. This index takes into account (1) the average number of medicinal uses reported for each plant species by participants; (2) the perceived quality of those medicinal uses; and (3) participant consensus. Conclusions: According to the results, the QUAV index provides an easily derived and valid appraisal of a medicinal plant’s cultural significance. © 2008 Elsevier Ireland Ltd. All rights reserved.

1. Introduction ease of handling for roof thatch, strength of stems used in house construction, efficacy to correct harmful symptoms or to elimi- The taxonomic classification of plants at the family level is an nate causal factors associated with particular health conditions, etc. important factor in determining the usefulness of plant species to (Casagrande, 2002; Byg et al., 2006). The concept of incorporating local people. Some plant families are clearly more useful in certain use quality in ethnobotanical indices was first proposed by Turner use categories than others (Phillips and Gentry, 1993a,b; Moerman, (1988) who assigned qualities a priori, with the specific use type 1996; Moerman et al., 1999; Byg et al., 2006). The same reasoning as the only criterion. For example, food uses received a score of holds true for individual plant species (Prance et al., 1987; Byg et 5 since they were considered more important by the author than al., 2006). Determining the usefulness of plant families generally medicinal uses that were assigned a quality score of 3. Other authors pertains to the domain of scientific researchers (e.g. Moerman, offered similar approaches to address the use preference of plants 1996; Treyvaud Amiguet et al., 2006; Bennett and Husby, 2008), (e.g. Pieroni, 2001; Garibay-Orijel et al., 2007). Also, Prance et al. whereas local people are ideally placed to assess the usefulness (1987) indirectly included the quality of uses in their calculations of particular plant species for particular applications, as the latter of species’ use values by subjectively assigning a value of 1 to each can rely on empirical knowledge accumulated over several years major use and a value of 0.5 to minor uses. to generations of practice. However, since these methods rely at least partly on subjec- Resource use preference by local people is often linked to tive decisions of researcher(s), it is unlikely that they are applied purpose-specific characteristics of plants, such as durability and consistently by different researchers (Phillips, 1996). Therefore, an approach whereby participants themselves are encouraged to assess individual plant use qualities seems better suited. Carretero ∗ Corresponding author. Tel.: +32 92646093; fax: +32 92646241. (2005) calculated ‘multiple values’ for Bolivian palm species by E-mail address: [email protected] (E. Thomas). combining use quality and use frequency explicitly assigned by

0378-8741/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.jep.2008.11.021 E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67 61 local participants and not by researchers. Also, Stagegaard et al. I. Between July 2000 and April 2001 a project on medicinal plant (2002) encouraged participants to rate the usefulness of plants as use in Apillapampa was carried out in collaboration with eight either “usable but sub-optimal” (0.5), “suitable” (1.0) or “near opti- traditional healers from the semi-formal healers’ association mal” (1.5) for five use categories. However, the downside of the called “Asociación de Jampiris de Apillapampa”. Methodological latter method is that it does not allow for more than one qual- details of this study are provided in Vandebroek et al. (2003, ity assessment per use category. For example, according to the 2004a,b, 2008). methodology of Stagegaard et al. (2002), a particular plant species II. The second study, conducted between December 2002 and that is reported to be a good remedy for treating three different November 2003, focused on a comprehensive quantitative eth- health conditions will receive an identical quality assessment for nobotanical inventory of all useful plant species in Apillapampa. the medicinal use category as a plant that is a good remedy for treat- Plant species were collected in transects, homegardens, and dur- ing just one health condition. In this paper we therefore propose an ing numerous fieldtrips. Thirty-six transects of 50 m × 2mwere alternative method, specifically for assessing local people’s percep- installed such that they represented the vegetation occurring in tion of a medicinal plant’s efficacy to correct deleterious symptoms. the study area. In these transects, all plants with a mature growth The overall goal of the present study is to identify the most height ≥0.1 m were sampled (Thomas et al., 2008). Ethnobotan- important medicinal families and species for Apillapampa, a com- ical information about 387 of the sampled plant species was munity of subsistence farmers from the Bolivian Andes. The gathered ex situ between December 2002 and December 2003 by importance of medicinal plant families was assessed by means of means of semi-structured interviews with 8 male and 5 female contingency table and binomial analyses as proposed by Bennett inhabitants (age range 14–66 years). Only six of the eight tradi- and Husby (2008). To quantify the cultural significance of medic- tional healers who participated in the first study (Vandebroek et inal plant species in Apillapampa, an index was developed that is al., 2003) were involved in both investigations, as two of them based on an adaptation and combination of existing ethnobotanical no longer lived in Apillapampa at the time the second study indices. was carried out. Other participants were selected through peer recommendations as described by Davis and Wagner (2003). 2. Methodology In both studies, interviews were conducted individually and 2.1. Research area included questions about local plant name(s), use(s), and prepa- ration methods of plant species. Voucher specimens were used Apillapampa is located at about 3250 m.a.s.l. and 17◦51S, as a prop during interviewing (cf. Thomas et al., 2007). The total 66◦15W, along the road connecting Capinota with Arampampa number of collected species that were presented to participants (Fig. 1). No on-site climate data are available, but the nearest during ethnobotanical interviews amounted to 441. Ethnopharma- village of Capinota (2400 m.a.s.l.) is characterized by a semi-arid cological data of most species mentioned in this paper are listed bioclimate with a pronounced dry season with 6–8 arid months in Vandebroek et al. (2003). Voucher specimens (ET1-600, IV1- and a mean annual temperature and precipitation of 17.8 ◦C and 188, JBC1-63 and TC500-650) were identified and deposited in the 447 mm (Navarro, 2002). A somewhat lower temperature and Bolivian herbaria of Cochabamba (BOLV) and La Paz (LPB). higher precipitation can be expected in Apillapampa due to the Acceptance of both projects by the Apillapampa community higher altitude. At the time of research, Apillapampa consisted council (Subcentral), the local healers’ association Asociación de of about 430 households (2600 inhabitants) of Quechua-speaking Jampiris de Apillapampa, and other participating community mem- subsistence farmers (Fepade, 1998). The main economic activity of bers was formalized by written agreements between researchers, most Apillapampenos˜ is agriculture for domestic use. The vegeta- indigenous representatives and the Centro de Biodiversidad y tion consists of mainly xerophytic shrubs and small trees, which are Genética from the Universidad Mayor de San Simon, Cochabamba. supplemented with annual herbs during the rainy season (Navarro, Copies of these agreements and all details of the projects were sent 2002; Thomas, 2008). A more detailed description of the ethno- to the Bolivian government (Ministerio de Desarrollo Sostenible y graphic and geographical background of the study area is provided Planificación). in Vandebroek et al. (2003, 2004a,b, 2008). 2.3. Informant indexing technique 2.2. Data collection Various analytical tools can be used to make a quantitative assessment of the cultural importance of individual plant species. The results presented in this paper were collected in two studies Recently, Tardío and Pardo-de-Santayana (2008) reviewed quan- as described below. titative methods in ethnobotany. More specifically, the authors compared the validity of four indices for ranking plants according to cultural significance which are based on (i) ‘informant consensus’, or (ii) a combination of ‘informant consensus’ and the diversity of reported plant uses. Clearly, all these indices provide scholars with valuable means to analyse different aspects of plant use data. How- ever, we identify two basic problems with the indices that take into account both informant consensus and the diversity of reported plant uses. The first problem is that these indices only consider whether or not a plant is used within a particular use category and do not take into account multiple plant uses within different use categories. Obviously, this leads to the loss of valuable plant use data that could potentially affect the cultural importance value of plants. Second, since these indices are based on use categories instead of individual plant uses, there exists a certain degree of bias depending Fig. 1. Location of the study area within Bolivia, the Department of Cochabamba on how use categories are defined. Although efforts have been made and Capinota Province (map elaborated with DIVA-GIS (www.diva-gis.org)). to standardize the recording and grouping of ethnobotanical data 62 E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67

(e.g. Cook’s Ethnobotanical Data Collection Standard, 1995), most species/total # of species shown to participants)). To assess the scholars keep on using their own subjective classification systems under- or overrepresentation of certain medicinal plant families or (Tardío and Pardo-de-Santayana, 2008). Hence, there exist signifi- plant growth forms in the flora of Apillapampa, we performed an cant differences between various publications in the number of use exact randomization test for Goodness of Fit (many expected val- categories, but also with respect to the choice of assigning certain ues were smaller than 5 in our sample, ruling out reliable use of plant uses to one category or another. To complicate matters even the chi-square Goodness of Fit statistic) (Bennett and Husby, 2008). more, subjective allocations of plant uses to categories are hardly Calculations for the contingency table approach were performed in ever detailed or justified in scientific publications. Therefore, these the statistical software package R (version 2.6.2, 2008). indices are likely to generate different results, depending on the In case the number of medicinal plants for the entire flora researcher who applies them. By contrast, indices based on indi- departs from the null model, individual families or growth forms vidual plant uses as provided by respondents are far less prone to can be examined by means of binomial analysis (Bennett and Husby, subjectivity because they do not require a classification of primary 2008). Hereby, the null hypothesis is that species from a particular data into subjectively assigned categories. That is why in the present family or growth form are no more likely to be used medicinally manuscript we used the informant indexing technique proposed by than would be the case for the flora as a whole. This means that Phillips and Gentry (1993a). Estimates of the medicinal use value of the proportion of medicinal plants in a family or growth form each species s were calculated according to the simplified formula equals the proportion of medicinal plants in the total flora. To test of Phillips and Gentry (1993a): the significance of individual variation from a uniform proportion  of medicinal plants among families or growth forms, binomial p- n U i=1 is values were calculated for over- and underrepresentation, using UVs = ns Microsoft Excel’s BINOMDIST function as detailed in Bennett and Husby (2008). All other statistical calculations were performed in whereby Uis equals the number of medicinal uses of species s SPSS 12.0. mentioned by informant i. This approach has the advantage that, given a sufficient number of informants interviewed, minor uses 3. Results and discussion or even mistakes will only minimally influence use values (Phillips and Gentry, 1993a). As such, the UV index provides an objective 3.1. Most important medicinal plant families assessment of the cultural importance of plants. In their evalu- ation of three different indices that incorporate both informant A total of 341 medicinal plant species was recorded for Apil- consensus and the diversity of uses, Tardío and Pardo-de-Santayana lapampa: 181 during the first study and 307 during the second, (2008) concluded that the cultural importance (CI) index is likely with 147 species overlapping between both studies. The number to be most objective. However, the authors appropriately note that of Quechua participants interviewed per medicinal plant varied although both indices are defined in different ways, the CI index between 1 and 15 with an average of almost 10 (9.5 ± 3.5). In abso- generates identical results as the UV index when based on indi- lute numbers, medicinal plant use in Apillapampa is not unusually vidual plant uses instead of use categories. In other words, Tardío high, since pharmacopoeias of more than 300 species have been and Pardo-de-Santayana (2008) indirectly confirm the advantages reported for various societies around the world (e.g. Bastien, 1987; of the UV index as compared to other existing indices. Ankli et al., 1999; Etkin, 2002; Leonti et al., 2003; Shepard, 2004). One important aspect that is overlooked by the technique pro- However, it is important to note that Apillapampa represents only posed by Phillips and Gentry (1993a) is the quality of individual one settlement of Quechua people, whereas most of the studies plant uses. For the present study, we “extended” or reinterpreted previously mentioned encompass several communities of people the use value index proposed by Phillips and Gentry (1993a) by with a similar ethnical background. Intriguing in this respect are the incorporating the quality of all individual plant uses. The “quality Bolivian Kallawayas whose pharmacopoeia is composed of approx- use value” of each species s can be defined as: imately one thousand different medicinal plant species (Bastien, n 1987). The Kallawayas follow an Andean pattern of specialization i=1QUis QUVs = ns in their medicinal practices at the community level (Bastien, 1987).  Specialized (Andean) communities are characterized by: (1) avail- whereby (1) QUis equals Qis, or the sum of the qualities of all ability of specific resources at different ecological levels; (2) skills medicinal uses assigned to species s by informant i and (2) ns equals acquired by practice and passed along through oral traditions; (3) the number of participants interviewed for species s. This implies a community’s reputation, established by its specialists in tradi- that the quality of each medicinal use mentioned is to be assessed tional medicine; (4) maintenance of this reputation by the elders by each individual participant. In the present investigation, qualities of the communities through a network of trust with other commu- were appraised on an ordinal scale, choosing between (a) good to nities with whom resources are exchanged; and (5) reciprocity, i.e. excellent, (b) fair, or (c) bad, to which values of 1, 0.5 and 0.25 were exchange of medicinal resources between specialized communities attributed, respectively. (Bastien, 1987). In another paper (Thomas et al., 2008), we discuss several factors that contibute to explaining the exceptionally high 2.4. Contingency table and binomial analyses use of medicinal plants in Apillapampa. The 341 medicinal plants are distributed over 80 botanical fam- In order to evaluate the local importance of different plant fam- ilies. One fourth of all species are Asteraceae (85 species; 25%) ilies and growth forms for traditional medicine in Apillapampa, followed by Fabaceae (27 species; 8%), Solanaceae (22 species; 6%), we used the contingency table and binomial analysis techniques Lamiaceae (14 species; 4%) and Scrophulariaceae (10 species; 3%). proposed by Bennett and Husby (2008). Expected numbers of The popularity of Asteraceae has been attributed to the wide array medicinal species per family, or plant growth form, were calculated of bioactive components they contain, as well as to the higher like- assuming that medicinal and non-medicinal species are allocated liness of people to experiment with members of this family as a within a family or growth form according to the proportion of consequence of the typical bitter phytochemicals they often con- medicinal species in the flora as a whole. Hence, the expected tain (e.g. sesquiterpene lactones) (Heinrich et al., 1998; Casagrande, number of medicinal species in a family or growth form = (total 2002). However, it is no coincidence that the botanically most # of species in a family or growth form × (total # of medicinal diverse families in Apillapampa (leaded by Asteraceae) also provide E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67 63 the highest numbers of medicinal species. The number of medicinal 1988; Voeks, 2004; Thomas, 2008). Indeed, during the dry season, plant species in a family correlates positively with the total number nearly all annual herbs disappear (except on irrigated land and in of species inventoried for that family (Kendall’s b = 0.83; p < 0.001). humid places). Woody plants persist during the dry season and Still, the exact Goodness of Fit Test on the contingency table for therefore they are the only medicinal alternative during half of the the Apillapampa flora as a whole revealed that medicinal species year. For that reason, they are more likely to be better known by peo- are not evenly distributed among families (p < 0.01). Subsequent ple, also as sources of herbal medicines (cf. Voeks, 2004; Thomas binomial analysis yielded two families that differ significantly from et al., 2008). the null model. Poaceae is underrepresented (p < 0.001) with only 5 medicinal species (while 17 species were inventoried and its pre- dicted species number is 13). By contrast, 22 of 23 Solanaceae 3.3. Culturally most relevant medicinal remedies and species species had a medicinal use according to participants, which explains their statistical overuse (p = 0.02; expected species num- 3.3.1. Medicinal plant remedies ber is 18). If the significance level is increased from 0.05 to 0.1, A total of 1400 different plant remedies (i.e. medicinal plant Convolvulaceae (p = 0.06) and Scrophulariaceae (p = 0.07) would uses) have been documented in Apillapampa. A plant remedy or contain more medicinal species than expected from the null model. a medicinal plant use is defined here as the use of one particular Many studies that identified over/underutilization of certain plant species for one particular health condition (irrespective of plant families for medicinal purposes followed Moerman’s regres- preparation or plant part used) and as mentioned by one or more sion residual approach (see Moerman, 1991, 1996). However, the participants. Plotting the number of remedies against the num- statistical soundness of this technique has recently been questioned ber of participants who confirmed these remedies results in an (Bennett and Husby, 2008). We agree with this critique and there- inverted “J” curve, characterized by an exponentially decreasing fore used contingency table and binomial analysis instead. Among number of medicinal remedies with increasing number of partici- the literature sources that applied the regression residual approach, pants confirming remedies. On average, remedies were confirmed the most frequently and widely overused medicinal plant family is by 1.6 (±1.4) participants. Only 29% of all reported remedies (i.e. the Asteraceae (Moerman, 1996; Moerman et al., 1999; Leonti et al., 406 remedies) were confirmed by at least two participants. Such 2003; Treyvaud Amiguet et al., 2006). In Apillapampa, Asteraceae low level of consensus may seem surprising, especially when tak- is the most important medicinal family in terms of species used (85 ing into account that nearly half of our participants are traditional out of 112), but it is not overused. The overuse of Solanaceae that healers. Nonetheless, this finding corresponds to a widespread we observed in Apillapampa seems less widespread. Nonetheless, tendency (e.g. Friedman et al., 1986; Barrett, 1995; Alexiades, the Solanaceae is a family well known to contain highly bioactive 1999; Casagrande, 2002) whereby the distribution of knowledge species, which in many cases relates to the presence of alkaloids about plant remedies follows a pattern in which few remedies are (Moerman, 1996; Gurib-Fakim, 2006). The Poaceae figures among known to almost everyone while most knowledge is idiosyncratic. the three most underutilized families in nearly all studies in the Casagrande (2002) hypothesized that this phenomenon reflects the literature, as well as in Apillapampa. existence of an upper limit to the amount of medicinal plant knowl- edge that can be transferred and distributed throughout pre-literate 3.2. Life forms communities. On the other hand, the idiosyncratic nature of medic- inal plant knowledge might be related to the fact that preparation More than half (51%) of all medicinal plants are herbs, while and use of medicinal plants is more difficult to learn as compared about one fourth (26%) are shrubs. In accordance with their rep- to other use categories such as food. In this respect, Phillips and resentation in the entire inventoried flora, a far lower number Gentry (1993b) have argued that learning and experimenting with of vines, trees and ferns are used as medicines: 18 (5.3%), 16 medicinal plants, as opposed to food plants, can be a life-long (4.7%) and 12 (3.5%) species, respectively. All inventoried ferns and process. For the study population of the second study (cf. method- (hemi-)parasites (12 and 11 species, respectively) have a thera- ology), we demonstrated indeed a highly significant linear relation peutic value. This seems to confirm Bennett and Prance’s (2000) between medicinal plant knowledge and participant age (R2 = 0.46 argument that parasitic plants have the reputation to be utilized and p < 0.001; Thomas, 2008). An alternative explanation for the more commonly as medicines as compared to other life forms. idiosyncratic nature of medicinal knowledge could be that the pop- The number of medicinal plants used per growth form correlates ulation is progressively losing its medicinal plant knowledge due to with the total number of species inventoried for each growth form modernization (Phillips and Gentry, 1993b). in Apillapampa (Kendall’s b = 0.76; p = 0.002). However, medicinal Highest consensus was recorded for the remedies listed in species are not evenly distributed among growth forms (p < 0.01; Table 1. The majority of participants agreed on these uses and there- exact Goodness of Fit Test on contingency table). Binomial analysis fore the chance that these plants are bioactive may be higher than shows that shrubs (p < 0.001) and ferns (p = 0.04) are overrepre- for other species. It is interesting to note that all these remedies sented as medicinal species. Ninety (90) of 95 inventoried shrub consist of native plant species. species and all 12 fern species are used medicinally, while the pre- dicted species numbers are 72 and 9, respectively. If ␣ increases from 0.05 to 0.1 (hemi-)parasites (p = 0.06) would contain more 3.3.2. Quality of medicine medicinal species than expected from the null model, whereas trees The fact that a plant species is used to treat a particular health would contain less (p = 0.06). condition does not necessarily mean that it is perceived as effective The prevalence of herbaceous plants in the pharmacopoeia of in alleviating symptoms or eliminating causal factors. When asked Apillapampa is not a surprise. Various authors have linked the pop- to systematically assess the quality of each remedy on an ordinal ularity of herbs in traditional medicine to their higher likeliness to scale, people in Apillapampa assigned a score of “good to excellent” contain bioactive phytochemicals as compared to woody growth to 64% of medicinal plant uses (on a total of 1119 responses), fol- forms (e.g. Stepp and Moerman, 2001; Stepp, 2004; Voeks, 2004). lowed by “fair” (35%). Only 1% (10 responses) referred to the rather The fact that nearly all inventoried shrub species are used medic- bad quality of herbal remedies. Of those remedies classified as “fair”, inally is therefore less expected and we hypothesize that the local participants often declared that they are sometimes effective in therapeutic importance of this growth form relates to its higher alleviating particular symptoms, but on other occasions or in some visibility and availability to people throughout the year (cf. Turner, patients do not help at all. 64 E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67

Table 1 Table 3, medicinal quality use values are consistently lower than use Medicinal plant remedies with highest participant consensus. values since not all reported ethnomedical applications of species Scientific name Family Health Number of are of “good” quality. To demonstrate the relevance of calculat- condition confirming ing quality use values over use values, we regressed the medicinal participants quality use values of species on their medicinal use value. This Trixis aggregata Rusby Asteraceae Bruises 12 regression results in a R2 value of 81.6, which indicates that assign- Krameria lappacea Krameriaceae Madrea 11 ing a quality to medicinal uses explains nearly one fifth (18.4%) of (Dombey) Burdet & the variance in QUV values. B.B. Simpson s Schinus molle L. Anacardiaceae Rheumatism 10 A weakness of UVs is that it does not satisfactorily incorporate Echeveria sp. (ET468) Crassulaceae Otitis 10 consensus among participants. For example, if three participants Achyrocline ramosissima Asteraceae Cough 10 each name two different medicinal uses for species A, then its (Sch.Bip.) Britton ex medicinal use value equals two ((2+2+2)/3) and the number of Rusby Gnaphalium Asteraceae Cough 10 reported health conditions six. If these participants unanimously gaudichaudianum DC. agree that species B is used for treating two different health condi- Passiflora umbilicata Passifloraceae Bruises 10 tions, the result is also a medicinal use value of two, while consensus (Griseb.) Harms for species A is zero and for species B it is 100%. Tessaria fastigiata Asteraceae Malnutrition 9 QUV values seem to express participant consensus better than (Griseb.) Cabrera s Calceolaria engleriana Scrophulariaceae Fracture/sprains 9 UVs. It is noticeable how ranking based on QUVs values (Table 3) Kraenzl. includes species that have the highest consensus for particular Mutisia ledifolia Decne. Asteraceae Cough 9 remedies (Table 1) together with species that have the most diverse ex Wedd. ethnomedical applications (Table 2). Ranking based on UVs values a Culture-bound syndrome associated with heavy labour on agricultural fields; seems to favour the latter species more. This property of QUVs to several of its symptoms correspond with the biomedical definition of a hernia, but partially incorporate participant consensus might be related to the according to Vandebroek et al. (2008) it could be related to Chagas’ disease. fact that a higher consensus about remedies parallels a higher fre- quency of responses related to remedies that are considered to be 3.3.3. Medicinal plant species of “good quality”. A technique that takes into account participant On average, 4.3 (±1.4) participants provided ethnomedicinal consensus and thus can be used to evaluate the latter assumption information on a medicinal plant species. The medicinal use of is the informant agreement ratio (IAR) for medicinal species. We 86 (25% of the total number of medicinal plants) and 147 species interpreted the formula originally proposed by Trotter and Logan (43%) was confirmed by only one and two participants, respectively. (1986) as follows: Species with the most diverse ethnomedical applications are listed nr − na in Table 2. The majority of species in this list are also native ones. 0 < IARs = < 1 nr − 1 The species presented in Table 2 also obtained high scores for medicinal use values (UVs) and quality use values (QUVs)(Table 3), whereby nr is the total number of medicinal responses registered partly because medicinal UVs and QUVs values are correlated for species s and na is the number of ailments or health conditions with the number of medicinal applications per species (Kendall’s that are treated with this species. The IARs of a medicinal species b = 0.75 and 0.62, respectively; p < 0.001 for both). As shown in varies between 0 (when the number of health conditions treated equals the number of medicinal responses) and 1 (whereby all par- Table 2 ticipants agree upon the exclusive use of the species for a particular Medicinal plant species with highest number of different medicinal applications. health condition). When applied to our data set, species’ IAR values correlate pos- Scientific name Family #part #med uses s itively with the number and proportion of “good quality” responses Schinus molle L. Anacardiaceae 12 17 per species (Kendall’s = 0.30 (p < 0.001) and 0.14 (p = 0.004), Medicago sativa L.a Fabaceae 9 17 b Trixis aggregata Rusby Asteraceae 13 13 respectively), confirming our hypothesis that species for which Schkuhria pinnata (Lam.) Kuntze Asteraceae 12 13 participant consensus is higher also yield more “good quality” ex Thell. responses. Hence, since a species’ QUVs is also positively correlated Baccharis sagittalis (Less.) DC. Asteraceae 10 13 with the number of “good quality” medicinal responses per species Otholobium pubescens (Poir.) J.W. Fabaceae 12 12 (Kendall’s = 0.64; p < 0.001), this may explain in part why QUV Grimes b s Cestrum parqui L’Hér. Solanaceae 11 12 expresses consensus better than UVs. These observations corrobo- Tripodanthus acutifolius (Ruiz & Loranthaceae 10 12 rate Casagrande’s (2002) argument that emic perception of efficacy Pav.) Tiegh. is the variable that most accounts for the distribution of knowl- Agalinis lanceolata (Ruiz & Pav.) Scrophulariaceae 11 12 edge about medicinal plants. Other authors have also argued that, in D’Arcy Solanum nitidum Ruiz & Pav. Solanaceae 12 12 many cases, consensus correlates with (pharmacological) efficacy Ephedra americana Humb. et Ephedraceae 12 12 (Trotter and Logan, 1986; Moerman, 2007). Bonpl. ex Willd. Table 4 lists medicinal species with the highest IARs val- Sonchus asper (L.) Hilla Asteraceae 10 12 ues. Although both medicinal UVs and QUVs correlate with IARs Caiophora canarinoides (Lenné & Loasaceae 12 11 (Kendall’s = 0.41 and 0.30, respectively; p < 0.001 for both cases), K. Koch) Urb. & Gilg b Satureja boliviana (Benth.) Briq. Lamiaceae 5 11 ranking of species based on IARs values give different results as Lepechinia meyenii (Walp.) Epling Lamiaceae 9 11 compared to ranking based on medicinal UVs and QUVs values Rosa × noisettiana Thory cf.a Rosaceae 10 11 (Table 3). The only species that occur in both tables are Achyrocline Valeriana decussata Ruiz & Pav. Valerianaceae 10 11 ramosissima, Tessaria fastigiata, Passiflora umbilicata, Gnaphalium Cheilanthes scariosa (Sw.) C. Presl. Pteridaceae 10 11 Ephedra rupestris Benth. Ephedraceae 10 11 gaudichaudianum and Minthostachys andina. This outcome is, at Calceolaria parvifolia Wedd. ssp. Scrophulariaceae 8 10 least in part, due to the fact that rankings based on UVs and QUVs parvifolia values favour plant species with multiple medicinal applications, #part = participants interviewed; #med uses = medicinal uses. whereas IARs mainly selects species with high participant consen- a Introduced species. sus. For example, a plant with only one medicinal application that E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67 65

Table 3

Medicinal plant species with the highest medicinal use value (UV) and quality use value (QUV). The top ten species according to UV, QUV and IARs values are underlined in the corresponding columns.

Scientific name Family #med uses #part UVs QUVs IARs Trixis aggregata Rusby Asteraceae 13 13 2.46 2.00 0.61 Schinus molle L. Anacardiaceae 17 14 2.14 1.42 0.45 Otholobium pubescens (Poir.) J.W. Grimes Fabaceae 12 14 2.00 1.17 0.59 Cestrum parqui L’Hér. Solanaceae 12 14 1.86 1.15 0.56 Agalinis lanceolata (Ruiz & Pav.) D’Arcy Scrophulariaceae 12 14 1.79 1.04 0.54 Tessaria fastigiata (Griseb.) Cabrera Asteraceae 5 12 1.75 1.00 0.80 Minthostachys andina (Britton) Epling Lamiaceae 8 14 1.71 1.10 0.70 Medicago sativa L.a Fabaceae 17 15 1.60 0.65 0.30 Tripodanthus acutifolius (Ruiz & Pav.) Tiegh. Loranthaceae 12 14 1.57 0.55 0.48 Solanum tripartitum Dunal Solanaceae 6 9 1.55 0.83 0.62 Solanum nitidum Ruiz & Pav. Solanaceae 12 13 1.54 1.10 0.42 Baccharis sagittalis (Less.) DC. Asteraceae 13 12 1.50 1.29 0.29 Krameria lappacea (Dombey) Burdet & B.B. Simpson Krameriaceae 9 14 1.43 1.14 0.58 Solanum palitans C.V. Morton Solanaceae 7 9 1.44 1.33 0.62 Passiflora umbilicata (Griseb.) Harms Passifloraceae 7 12 1.33 1.22 0.80 Gnaphalium gaudichaudianum DC. Asteraceae 5 12 1.25 1.21 0.71 Achyrocline ramosissima (Sch.Bip.) Britton ex Rusby Asteraceae 2 10 1.30 1.17 0.92 Calceolaria engleriana Kraenzl. Scrophulariaceae 7 14 1.29 1.17 0.65 Geranium soratae R. Knuth Geraniaceae 5 8 1.13 1.13 0.50 Mentzelia fendleriana Urb. & Gilg Loasaceae 5 5 1.20 1.10 0.20

#part = participants interviewed; #med uses = medicinal uses. a Introduced species.

is known to all interviewed participants will receive UVs and QUVs of a medicinal plant should not be based solely on the number of values of maximally 1, and therefore has little chance of being listed uses or use values of the respective species, but on a combination among the most important medicinal species. On the other hand, of the former and the level of consensus between participants. The its IARs value would also be 1, acknowledging the maximum level QUVs and IARs indexes we proposed here seem highly suitable for of consensus. In line with this observation, the number of differ- this purpose. Medicinal QUVs values appear to be more sensitive ent medicinal uses per species is significantly higher (p < 0.001; to the number of ethnomedical applications per plant species and Mann–Whitney) for species with high medicinal UVs and QUVs val- incorporate the emic perception of therapeutic qualities, whereas ues (listed in Table 3) than for species with high IARs values (listed IARs values address informant consensus. Therefore, our proposal is in Table 4). to combine both parameters into the ‘Quality Use Agreement Value’ Use values imply that the local importance of a plant is primarily (QUAVs), which is defined as: determined by its number of medicinal uses. This proposition has = × rarely been tested, but Byg and Balslev (2001) were able to show QUAVs QUVs IARs a positive correlation between the perceived importance of palm In Table 5, ranking of the twenty highest scoring medicinal species by local participants in Madagascar and their use values species according to QUAVs values shows that species from the and number of uses. Although this relation might be valid when all top twenty ranking according to IARs and QUVs, respectively are different plant uses are pooled together, it is not necessarily so for represented in relatively even proportions (10 and 13 species, medicinal plant use. We believe that assessing the local importance respectively). Hence, this index seems to provide a valid and easily

Table 4

IARs values for medicinal plant species in Apillapampa. Only those species are listed for which the number of responses is higher than 3.

Scientific name Family #part #resp #med uses IARs Tessaria dodonaeifolia (Hook. et Arn.) Cabrera Asteraceae 8 3 1 1.00 Achyrocline ramosissima (Sch.Bip.) Britton ex Rusby Asteraceae 10 13 2 0.92 Passiflora umbilicata (Griseb.) Harms Passifloraceae 12 16 3 0.87 Dunalia brachyacantha Miers Solanaceae 8 7 2 0.83 Tessaria fastigiata (Griseb.) Cabrera Asteraceae 12 21 5 0.80 Bidens mandonii (Sherff) Cabrera Asteraceae 8 5 2 0.75 Dodonaea viscosa Jacq. Sapindaceae 14 17 5 0.75 Echeveria sp. (ET468) Crassulaceae 13 13 4 0.75 Gamochaeta americana (Mill.) Wedd. Asteraceae 10 9 3 0.75 Trichocereus tunariensis Cardenas Cactaceae 8 9 3 0.75 Plantago orbignyana Steinh. Plantaginaceae 11 9 3 0.75 Hypseocharis pimpinellifolia Remy Oxalidaceae 13 13 4 0.75 Vassobia fasciculata (Miers) Hunz. Solanaceae 15 19 6 0.72 Gnaphalium melanosphaeroides Sch.Bip. ex Wedd. Asteraceae 9 8 3 0.71 Margyricarpus pinnatus (Lam.) Kuntze Rosaceae 10 8 3 0.71 Spathantheum orbignyanum Schott Araceae 13 15 5 0.71 Gnaphalium gaudichaudianum DC. Asteraceae 12 15 5 0.71 Rumex conglomeratus Murraya Polygonaceae 8 11 4 0.70 Cosmos peucedanifolius Wedd. Asteraceae 12 11 4 0.70 Minthostachys andina (Britton) Epling Lamiaceae 14 24 8 0.70

#part = participants interviewed; #resp = responses; #med uses = medicinal uses. a Introduced species. 66 E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67

Table 5

Ranking of medicinal species according to decreasing Quality Use Agreement Values (QUAVs). Species from the top twenty ranking of QUVs and IARs, respectively, are marked in bold in the corresponding columns. Ethnomedical uses, botanical family and voucher numbers of these species are given in Appendix A.

Scientific name #med uses #part UVmed QUVmed IARs QUAVs Trixis aggregata Rusby 13 13 2.46 2.00 0.61 1.23 Achyrocline ramosissima (Sch.Bip.) Britton ex Rusby 2 10 1.29 1.17 0.92 1.08 Passiflora umbilicata (Griseb.) Harms 3 12 1.33 1.22 0.87 1.06 Gnaphalium gaudichaudianum DC. 5 12 1.25 1.21 0.71 0.86 Tessaria fastigiata (Griseb.) Cabrera 5 12 1.75 1.00 0.80 0.80 Minthostachys andina (Britton) Epling 8 14 1.71 1.10 0.70 0.77 Calceolaria engleriana Kraenzl. 7 14 1.29 1.17 0.65 0.75 Otholobium pubescens (Poir.) J.W. Grimes 12 14 2.00 1.17 0.59 0.69 Krameria lappacea (Dombey) Burdet & B.B. Simpson 9 14 1.43 1.14 0.58 0.66 Cestrum parqui L’Hér. 12 14 1.86 1.15 0.56 0.64 Vassobia fasciculata (Miers) Hunz. 6 15 1.27 0.88 0.72 0.64 Schinus molle L. 17 14 2.14 1.42 0.45 0.64 Dodonaea viscosa Jacq. 5 14 1.21 0.83 0.75 0.63 Tetraglochin cristatum (Britton) Rothm. 7 14 1.29 0.96 0.65 0.62 Gnaphalium cheiranthifolium Lam. 5 11 1.09 0.91 0.64 0.58 Agalinis lanceolata (Ruiz & Pav.) D’Arcy 12 14 1.79 1.04 0.54 0.56 Geranium soratae R. Knuth 5 8 1.13 1.13 0.50 0.56 Gamochaeta americana (Mill.) Wedd. 3 10 0.9 0.75 0.75 0.56 Gnaphalium melanosphaeroides Sch.Bip. ex Wedd. 3 9 0.89 0.78 0.71 0.56 Solanum palitans C.V. Morton 8 9 1.44 1.33 0.42 0.56 Hypseocharis pimpinellifolia Remy 4 13 1.00 0.73 0.75 0.55

#part = participants interviewed; #med uses = medicinal uses.

derived estimation of a medicinal plant’s cultural significance, at Acknowledgements least for the case of Apillapampa. The first study was funded by the Institute for the Promo- tion of Innovation through Science and Technology in Flanders 4. Conclusions (IWT), Belgium, by means of a post-doctoral grant to Ina Van- debroek. The second study was financed by a doctoral research Our findings add value to the observation in literature that grant of the Bijzonder Onderzoeksfonds (BOF) of Ghent Univer- indigenous pharmacopoeias around the world are far from random sity to Evert Thomas (Grant Number: B/03801/01 FONDS IV 1). assemblages. Some families clearly hold more medicinal species We are grateful to Jan-Bart Calewaert, Ben Michiels, Lisa De than predicted by chance. The same reasoning also seems to apply Munk, Trees Cousy, Frieke Heens and David Douterlungne for to different life forms in Apillapampa, where plants with a shrubby collaboration during data collection. Logistic support in Bolivia habit are significantly overused. It is hypothesized that this is was provided by the Centre of Biodiversity and Genetics and related to the year-round availability of shrubs, as compared to the Herbarium Martin Cardenas of the Universidad Mayor de most annual and herbaceous plants that disappear during the dry San Simon in Cochabamba. Special thanks are due to the inhab- season. itants and Subcentral of the community of Apillapampa for Emic perception of medicinal plant efficacy varies from one their kind assistance in making this project successful. We are species to another in Apillapampa. All local Quechua partici- also indebted to the professional botanists who identified sev- pants (both healers and laypeople) recognise that some species eral collections. They are S. Beck (flora of Bolivia), S. Clemants are more effective for treating particular symptoms or health (Chenopodiaceae), E. Emshwiller (Oxalidaceae), H.-J. Esser (Euphor- conditions than others. Therefore, we believe that the quality biaceae), R. Faden (Commelinaceae), A. Freire (Polygalaceae), D. of remedies should be taken into account when ranking plants Goyder (Asclepiadaceae), I. Jiménez (Bolivian Pteridophyta), A. according to their cultural importance. The applicability of the Krapovickas (Malvaceae), J. Müller (Baccharis and Hieracium, Aster- technique to incorporate the quality of plant use (i.e. quality use aceae), G. Navarro (Cactaceae), M. Nee (Solanaceae), A. Planchuelo values; QUVs), proposed by us in this paper provides a ‘novel’ way (Lupinus, Fabaceae), J. Pruski (Asteraceae), L. Rico (Fabaceae), to approach and interpret plant use data, in the medicinal use C. Ulloa (Berberidaceae), R. Vasquez (Bromeliaceae and Orchi- category and beyond. In addition, we have shown that a combi- daceae), D. Wasshausen (Asclepiadaceae), J. Wood (Asclepiadaceae nation of QUVs with a re-interpreted consensus index regarding and Salvia, Lamiaceae) and C. Xifreda (Dioscorea, Dioscore- the medicinal use of species (IARs) in the QUAVs, might rep- aceae). resent the cultural significance of medicinal plants better than existing indexes. This is particularly because such an approach takes into account (1) the average number of medicinal uses; (2) References the perceived quality of those medicinal uses; and (3) partici- pant consensus about those medicinal uses. In the top ranking Alexiades, M.N., 1999. Ethnobotany of the Ese Eja: plants, health, and change in an Amazonian society, Ph.D. Dissertation. City University of New York, New York. of medicinal plants according to the present study using QUAVs, Ankli, A., Sticher, O., Heinrich, M., 1999. Medical ethnobotany of the Yucatec species from the top rankings according to IARs and QUVs, respec- Maya: healers’ consensus as a quantitative criterion. Economic Botany 53, tively, are represented in relatively even proportions. Therefore 144–160. Barrett, B., 1995. Herbal knowledge on the Nicaragua Atlantic coast: Consensus the QUAVs index seems to provide an easily derived and valid within diversity. Journal of Community Health 20, 403–421. assessment of a plant’s significance within a culture. Future Bastien, J.W., 1987. Healers of the Andes. Kallawaya Herbalists and their Medicinal pharmacological studies are needed to determine if these cul- Plants. University of Utah Press, Salt Lake City, US. Bennett, B.C., Husby, C.E., 2008. Patterns of medicinal plant use: an examination turally most significant species also show the highest levels of of the Ecuadorian Shuar medicinal flora using contingency table and binomial bioactivity. analyses. Journal of Ethnopharmacology 116, 422–430. E. Thomas et al. / Journal of Ethnopharmacology 122 (2009) 60–67 67

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