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

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Contents lists available atScienceDirect

Journal of Ethnopharmacology

j o u r n a l h o m e p a g e :w w w . e l s e v i e r . c o m / l o c a t e / j e t h p h a r m

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

Evert Thomas

^a,∗

, Ina Vandebroek

^b

, Sabino Sanca

^c

, Patrick Van Damme

^a

aLaboratory of Tropical and Subtropical Agriculture and Ethnobotany, Ghent University, Coupure links 653, B-9000 Ghent, Belgium

bInstitute of Economic Botany, The New York Botanical Garden, 2900 Southern Boulevard, NY 10458, USA

cAsociación de Jampiris de Apillapampa, Apillapampa, Bolivia

a r t i c l e i n f o

Article history:

Received 16 August 2008

Received in revised form 5 October 2008 Accepted 26 November 2008

Available online 3 December 2008

Keywords:

Informant consensus Emic perception of efﬁcacy Use quality

Andes

Quantitative ethnobotany Cultural importance indices

a b s t r a c t

Ethnopharmacological relevance:Medicinal plant use was investigated in Apillapampa, a community of subsistence farmers located in the semi-arid Bolivian Andes.

Aim of the study:The main objectives were to identify the culturally most signiﬁcant medicinal plant families and species in Apillapampa.

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, eight of them being traditional healers.

Results:Contingency table and binomial analyses of medicinal plants used versus the total number of inventoried species per family showed that Solanaceae is signiﬁcantly overused in traditional medicine, whereas Poaceae is underused. Also plants with a shrubby habitat are signiﬁcantly overrepresented in the medicinal plant inventory, which most likely relates to their year-round availability to people as compared 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.

1. Introduction

The taxonomic classiﬁcation of plants at the family level is an important factor in determining the usefulness of plant species to local people. Some plant families are clearly more useful in certain use categories than others (Phillips and Gentry, 1993a,b; Moerman, 1996; Moerman et al., 1999; Byg et al., 2006). The same reasoning holds true for individual plant species (Prance et al., 1987; Byg et al., 2006). Determining the usefulness of plant families generally pertains to the domain of scientiﬁc researchers (e.g. Moerman, 1996; Treyvaud Amiguet et al., 2006; Bennett and Husby, 2008), whereas local people are ideally placed to assess the usefulness of particular plant species for particular applications, as the latter can rely on empirical knowledge accumulated over several years to generations of practice.

Resource use preference by local people is often linked to purpose-speciﬁc characteristics of plants, such as durability and

∗ Corresponding author. Tel.: +32 92646093; fax: +32 92646241.

E-mail address:evert.thomas@gmail.com(E. Thomas).

ease of handling for roof thatch, strength of stems used in house construction, efﬁcacy to correct harmful symptoms or to elimi- nate causal factors associated with particular health conditions, etc.

(Casagrande, 2002; Byg et al., 2006). The concept of incorporating use quality in ethnobotanical indices was ﬁrst proposed byTurner (1988)who assigned qualitiesa priori, with the speciﬁc use type as the only criterion. For example, food uses received a score of 5 since they were considered more important by the author than medicinal uses that were assigned a quality score of 3. Other authors offered similar approaches to address the use preference of plants (e.g.Pieroni, 2001; Garibay-Orijel et al., 2007). Also,Prance et al.

(1987)indirectly included the quality of uses in their calculations of species’ use values by subjectively assigning a value of 1 to each major use and a value of 0.5 to minor uses.

However, since these methods rely at least partly on subjective decisions of researcher(s), it is unlikely that they are applied consistently by different researchers (Phillips, 1996). Therefore, an approach whereby participants themselves are encouraged to assess individual plant use qualities seems better suited.Carretero (2005) calculated ‘multiple values’ for Bolivian palm species by 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

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local participants and not by researchers. Also,Stagegaard et al.

(2002)encouraged participants to rate the usefulness of plants as either “usable but sub-optimal” (0.5), “suitable” (1.0) or “near optimal” (1.5) for five use categories. However, the downside of the latter method is that it does not allow for more than one quality assessment per use category. For example, according to the methodology ofStagegaard et al. (2002), a particular plant species that is reported to be a good remedy for treating three different health conditions will receive an identical quality assessment for the medicinal use category as a plant that is a good remedy for treating just one health condition. In this paper we therefore propose an alternative method, specifically for assessing local people’s perception of a medicinal plant’s efficacy to correct deleterious symptoms.

The overall goal of the present study is to identify the most important medicinal families and species for Apillapampa, a community of subsistence farmers from the Bolivian Andes. The importance of medicinal plant families was assessed by means of contingency table and binomial analyses as proposed byBennett and Husby (2008). To quantify the cultural signiﬁcance of medicinal plant species in Apillapampa, an index was developed that is based on an adaptation and combination of existing ethnobotanical indices.

2. Methodology

2.1. Research area

Apillapampa is located at about 3250 m.a.s.l. and 17^◦51S, 66^◦15W, along the road connecting Capinota with Arampampa (Fig. 1). No on-site climate data are available, but the nearest village of Capinota (2400 m.a.s.l.) is characterized by a semi-arid bioclimate with a pronounced dry season with 6–8 arid months and a mean annual temperature and precipitation of 17.8^◦C and 447 mm (Navarro, 2002). A somewhat lower temperature and higher precipitation can be expected in Apillapampa due to the higher altitude. At the time of research, Apillapampa consisted of about 430 households (2600 inhabitants) of Quechua-speaking subsistence farmers (Fepade, 1998). The main economic activity of most Apillapampe ˜nos is agriculture for domestic use. The vegetation consists of mainly xerophytic shrubs and small trees, which are supplemented with annual herbs during the rainy season (Navarro, 2002; Thomas, 2008). A more detailed description of the ethno- graphic and geographical background of the study area is provided inVandebroek et al. (2003, 2004a,b, 2008).

2.2. Data collection

The results presented in this paper were collected in two studies as described below.

Fig. 1.Location of the study area within Bolivia, the Department of Cochabamba and Capinota Province (map elaborated with DIVA-GIS (www.diva-gis.org)).

I. Between July 2000 and April 2001 a project on medicinal plant use in Apillapampa was carried out in collaboration with eight traditional healers from the semi-formal healers’ association called “Asociación de Jampiris de Apillapampa”. Methodological details of this study are provided inVandebroek et al. (2003, 2004a,b, 2008).

II. The second study, conducted between December 2002 and November 2003, focused on a comprehensive quantitative ethnobotanical inventory of all useful plant species in Apillapampa.

Plant species were collected in transects, homegardens, and during numerous ﬁeldtrips. Thirty-six transects of 50 m×2 m were installed such that they represented the vegetation occurring in the study area. In these transects, all plants with a mature growth height≥0.1 m were sampled (Thomas et al., 2008). Ethnobotan- ical information about 387 of the sampled plant species was gathered ex situ between December 2002 and December 2003 by means of semi-structured interviews with 8 male and 5 female inhabitants (age range 14–66 years). Only six of the eight traditional healers who participated in the ﬁrst study (Vandebroek et al., 2003) were involved in both investigations, as two of them no longer lived in Apillapampa at the time the second study was carried out. Other participants were selected through peer recommendations as described byDavis and Wagner (2003).

In both studies, interviews were conducted individually and included questions about local plant name(s), use(s), and preparation methods of plant species. Voucher specimens were used as a prop during interviewing (cf.Thomas et al., 2007). The total number of collected species that were presented to participants during ethnobotanical interviews amounted to 441. Ethnopharma- cological data of most species mentioned in this paper are listed in Vandebroek et al. (2003). Voucher specimens (ET1-600, IV1- 188, JBC1-63 and TC500-650) were identiﬁed and deposited in the Bolivian herbaria of Cochabamba (BOLV) and La Paz (LPB).

Acceptance of both projects by the Apillapampa community council (Subcentral), the local healers’ association Asociación de Jampiris de Apillapampa, and other participating community members was formalized by written agreements between researchers, indigenous representatives and the Centro de Biodiversidad y Genéticafrom theUniversidad Mayor de San Simon, Cochabamba.

Copies of these agreements and all details of the projects were sent to the Bolivian government (Ministerio de Desarrollo Sostenible y Planiﬁcación).

2.3. Informant indexing technique

Various analytical tools can be used to make a quantitative assessment of the cultural importance of individual plant species.

Recently,Tardío and Pardo-de-Santayana (2008) reviewed quantitative 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 on how use categories are deﬁned. Although efforts have been made to standardize the recording and grouping of ethnobotanical data

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(e.g.Cook’s Ethnobotanical Data Collection Standard, 1995), most scholars keep on using their own subjective classification systems (Tardío and Pardo-de-Santayana, 2008). Hence, there exist significant differences between various publications in the number of use categories, but also with respect to the choice of assigning certain plant uses to one category or another. To complicate matters even more, subjective allocations of plant uses to categories are hardly ever detailed or justified in scientific publications. Therefore, these indices are likely to generate different results, depending on the researcher who applies them. By contrast, indices based on individual plant uses as provided by respondents are far less prone to subjectivity because they do not require a classification of primary data into subjectively assigned categories. That is why in the present manuscript we used the informant indexing technique proposed by Phillips and Gentry (1993a). Estimates of the medicinal use value of each speciesswere calculated according to the simplified formula ofPhillips and Gentry (1993a):

UV_s=

_n

i=1U_is ns

whereby U_is equals the number of medicinal uses of species s mentioned by informanti. This approach has the advantage that, given a sufficient number of informants interviewed, minor uses or even mistakes will only minimally influence use values (Phillips and Gentry, 1993a). As such, the UV index provides an objective assessment of the cultural importance of plants. In their evaluation of three different indices that incorporate both informant consensus and the diversity of uses,Tardío and Pardo-de-Santayana (2008)concluded that the cultural importance (CI) index is likely to be most objective. However, the authors appropriately note that although both indices are defined in different ways, the CI index generates identical results as the UV index when based on individual plant uses instead of use categories. In other words,Tardío and Pardo-de-Santayana (2008)indirectly confirm the advantages of the UV index as compared to other existing indices.

One important aspect that is overlooked by the technique proposed byPhillips and Gentry (1993a)is the quality of individual plant uses. For the present study, we “extended” or reinterpreted the use value index proposed byPhillips and Gentry (1993a)by incorporating the quality of all individual plant uses. The “quality use value” of each speciesscan be deﬁned as:

QUV_s=

_n

i=1QU_is ns

whereby (1) QU_is equals

Q_is, or the sum of the qualities of all medicinal uses assigned to speciessby informantiand (2)n_sequals the number of participants interviewed for speciess. This implies that the quality of each medicinal use mentioned is to be assessed by each individual participant. In the present investigation, qualities were appraised on an ordinal scale, choosing between (a) good to excellent, (b) fair, or (c) bad, to which values of 1, 0.5 and 0.25 were attributed, respectively.

2.4. Contingency table and binomial analyses

In order to evaluate the local importance of different plant families and growth forms for traditional medicine in Apillapampa, we used the contingency table and binomial analysis techniques proposed by Bennett and Husby (2008). Expected numbers of medicinal species per family, or plant growth form, were calculated assuming that medicinal and non-medicinal species are allocated within a family or growth form according to the proportion of medicinal species in the ﬂora as a whole. Hence, the expected number of medicinal species in a family or growth form = (total

# of species in a family or growth form×(total # of medicinal

species/total # of species shown to participants)). To assess the under- or overrepresentation of certain medicinal plant families or plant growth forms in the ﬂora of Apillapampa, we performed an exact randomization test for Goodness of Fit (many expected values were smaller than 5 in our sample, ruling out reliable use of the chi-square Goodness of Fit statistic) (Bennett and Husby, 2008).

Calculations for the contingency table approach were performed in the statistical software package R (version 2.6.2, 2008).

In case the number of medicinal plants for the entire flora departs from the null model, individual families or growth forms can be examined by means of binomial analysis (Bennett and Husby, 2008). Hereby, the null hypothesis is that species from a particular family or growth form are no more likely to be used medicinally than would be the case for the flora as a whole. This means that the proportion of medicinal plants in a family or growth form equals the proportion of medicinal plants in the total flora. To test the significance of individual variation from a uniform proportion of medicinal plants among families or growth forms, binomialp- values were calculated for over- and underrepresentation, using Microsoft Excel’s BINOMDIST function as detailed inBennett and Husby (2008). All other statistical calculations were performed in SPSS 12.0.

3. Results and discussion

3.1. Most important medicinal plant families

A total of 341 medicinal plant species was recorded for Apil- lapampa: 181 during the ﬁrst study and 307 during the second, with 147 species overlapping between both studies. The number of Quechua participants interviewed per medicinal plant varied between 1 and 15 with an average of almost 10 (9.5±3.5). In abso- lute numbers, medicinal plant use in Apillapampa is not unusually high, since pharmacopoeias of more than 300 species have been reported for various societies around the world (e.g.Bastien, 1987;

Ankli et al., 1999; Etkin, 2002; Leonti et al., 2003; Shepard, 2004).

However, it is important to note that Apillapampa represents only one settlement of Quechua people, whereas most of the studies previously mentioned encompass several communities of people with a similar ethnical background. Intriguing in this respect are the Bolivian Kallawayas whose pharmacopoeia is composed of approx- imately one thousand different medicinal plant species (Bastien, 1987). The Kallawayas follow an Andean pattern of specialization in their medicinal practices at the community level (Bastien, 1987).

Specialized (Andean) communities are characterized by: (1) availability of speciﬁc resources at different ecological levels; (2) skills acquired by practice and passed along through oral traditions; (3) a community’s reputation, established by its specialists in traditional medicine; (4) maintenance of this reputation by the elders of the communities through a network of trust with other communities with whom resources are exchanged; and (5) reciprocity, i.e.

exchange of medicinal resources between specialized communities (Bastien, 1987). In another paper (Thomas et al., 2008), we discuss several factors that contibute to explaining the exceptionally high use of medicinal plants in Apillapampa.

The 341 medicinal plants are distributed over 80 botanical families. One fourth of all species are Asteraceae (85 species; 25%) followed by Fabaceae (27 species; 8%), Solanaceae (22 species; 6%), Lamiaceae (14 species; 4%) and Scrophulariaceae (10 species; 3%).

The popularity of Asteraceae has been attributed to the wide array of bioactive components they contain, as well as to the higher likeliness of people to experiment with members of this family as a consequence of the typical bitter phytochemicals they often contain (e.g. sesquiterpene lactones) (Heinrich et al., 1998; Casagrande, 2002). However, it is no coincidence that the botanically most diverse families in Apillapampa (leaded by Asteraceae) also provide

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the highest numbers of medicinal species. The number of medicinal plant species in a family correlates positively with the total number of species inventoried for that family (Kendall’sb= 0.83;p< 0.001).

Still, the exact Goodness of Fit Test on the contingency table for the Apillapampa flora as a whole revealed that medicinal species are not evenly distributed among families (p< 0.01). Subsequent binomial analysis yielded two families that differ significantly from the null model. Poaceae is underrepresented (p< 0.001) with only 5 medicinal species (while 17 species were inventoried and its predicted species number is 13). By contrast, 22 of 23 Solanaceae species had a medicinal use according to participants, which explains their statistical overuse (p= 0.02; expected species number is 18). If the significance level is increased from 0.05 to 0.1, Convolvulaceae (p= 0.06) and Scrophulariaceae (p= 0.07) would contain more medicinal species than expected from the null model.

Many studies that identiﬁed over/underutilization of certain plant families for medicinal purposes followed Moerman’s regression residual approach (seeMoerman, 1991, 1996). However, the statistical soundness of this technique has recently been questioned (Bennett and Husby, 2008). We agree with this critique and therefore used contingency table and binomial analysis instead. Among the literature sources that applied the regression residual approach, the most frequently and widely overused medicinal plant family is the Asteraceae (Moerman, 1996; Moerman et al., 1999; Leonti et al., 2003; Treyvaud Amiguet et al., 2006). In Apillapampa, Asteraceae is the most important medicinal family in terms of species used (85 out of 112), but it is not overused. The overuse of Solanaceae that we observed in Apillapampa seems less widespread. Nonetheless, the Solanaceae is a family well known to contain highly bioactive species, which in many cases relates to the presence of alkaloids (Moerman, 1996; Gurib-Fakim, 2006). The Poaceae ﬁgures among the three most underutilized families in nearly all studies in the literature, as well as in Apillapampa.

3.2. Life forms

More than half (51%) of all medicinal plants are herbs, while about one fourth (26%) are shrubs. In accordance with their rep- resentation in the entire inventoried ﬂora, a far lower number of vines, trees and ferns are used as medicines: 18 (5.3%), 16 (4.7%) and 12 (3.5%) species, respectively. All inventoried ferns and (hemi-)parasites (12 and 11 species, respectively) have a therapeutic value. This seems to conﬁrmBennett and Prance’s (2000) argument that parasitic plants have the reputation to be utilized more commonly as medicines as compared to other life forms.

The number of medicinal plants used per growth form correlates with the total number of species inventoried for each growth form in Apillapampa (Kendall’sb= 0.76;p= 0.002). However, medicinal species are not evenly distributed among growth forms (p< 0.01;

exact Goodness of Fit Test on contingency table). Binomial analysis shows that shrubs (p< 0.001) and ferns (p= 0.04) are overrepresented as medicinal species. Ninety (90) of 95 inventoried shrub species and all 12 fern species are used medicinally, while the predicted species numbers are 72 and 9, respectively. If␣increases from 0.05 to 0.1 (hemi-)parasites (p= 0.06) would contain more medicinal species than expected from the null model, whereas trees would contain less (p= 0.06).

The prevalence of herbaceous plants in the pharmacopoeia of Apillapampa is not a surprise. Various authors have linked the popularity of herbs in traditional medicine to their higher likeliness to contain bioactive phytochemicals as compared to woody growth forms (e.g.Stepp and Moerman, 2001; Stepp, 2004; Voeks, 2004).

The fact that nearly all inventoried shrub species are used medicinally is therefore less expected and we hypothesize that the local therapeutic importance of this growth form relates to its higher visibility and availability to people throughout the year (cf.Turner,

1988; Voeks, 2004; Thomas, 2008). Indeed, during the dry season, nearly all annual herbs disappear (except on irrigated land and in humid places). Woody plants persist during the dry season and therefore they are the only medicinal alternative during half of the year. For that reason, they are more likely to be better known by people, also as sources of herbal medicines (cf.Voeks, 2004; Thomas et al., 2008).

3.3. Culturally most relevant medicinal remedies and species 3.3.1. Medicinal plant remedies

A total of 1400 different plant remedies (i.e. medicinal plant uses) have been documented in Apillapampa. Aplant remedyor amedicinal plant useis defined here as the use of one particular plant species for one particular health condition (irrespective of preparation or plant part used) and as mentioned by one or more participants. Plotting the number of remedies against the number of participants who confirmed these remedies results in an inverted “J” curve, characterized by an exponentially decreasing number of medicinal remedies with increasing number of participants confirming remedies. On average, remedies were confirmed by 1.6 (±1.4) participants. Only 29% of all reported remedies (i.e.

406 remedies) were conﬁrmed by at least two participants. Such low level of consensus may seem surprising, especially when tak- ing into account that nearly half of our participants are traditional healers. Nonetheless, this ﬁnding corresponds to a widespread tendency (e.g. Friedman et al., 1986; Barrett, 1995; Alexiades, 1999; Casagrande, 2002) whereby the distribution of knowledge about plant remedies follows a pattern in which few remedies are known to almost everyone while most knowledge is idiosyncratic.

Casagrande (2002)hypothesized that this phenomenon reflects the existence of an upper limit to the amount of medicinal plant knowledge that can be transferred and distributed throughout pre-literate communities. On the other hand, the idiosyncratic nature of medicinal plant knowledge might be related to the fact that preparation and use of medicinal plants is more difficult to learn as compared to other use categories such as food. In this respect,Phillips and Gentry (1993b)have argued that learning and experimenting with medicinal plants, as opposed to food plants, can be a life-long process. For the study population of the second study (cf. methodology), we demonstrated indeed a highly significant linear relation between medicinal plant knowledge and participant age (R²= 0.46 andp< 0.001;Thomas, 2008). An alternative explanation for the idiosyncratic nature of medicinal knowledge could be that the population is progressively losing its medicinal plant knowledge due to modernization (Phillips and Gentry, 1993b).

Highest consensus was recorded for the remedies listed in Table 1. The majority of participants agreed on these uses and therefore the chance that these plants are bioactive may be higher than for other species. It is interesting to note that all these remedies consist of native plant species.

3.3.2. Quality of medicine

The fact that a plant species is used to treat a particular health condition does not necessarily mean that it is perceived as effective in alleviating symptoms or eliminating causal factors. When asked to systematically assess the quality of each remedy on an ordinal scale, people in Apillapampa assigned a score of “good to excellent”

to 64% of medicinal plant uses (on a total of 1119 responses), followed by “fair” (35%). Only 1% (10 responses) referred to the rather bad quality of herbal remedies. Of those remedies classiﬁed as “fair”, participants often declared that they are sometimes effective in alleviating particular symptoms, but on other occasions or in some patients do not help at all.

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Table 1

Medicinal plant remedies with highest participant consensus.

Scientiﬁc name Family Health

condition

Number of conﬁrming participants

Trixis aggregataRusby Asteraceae Bruises 12

Krameria lappacea (Dombey) Burdet &

B.B. Simpson

Krameriaceae Madre^a 11

Schinus molleL. Anacardiaceae Rheumatism 10

Echeveriasp. (ET468) Crassulaceae Otitis 10

Achyrocline ramosissima (Sch.Bip.) Britton ex Rusby

Asteraceae Cough 10

Gnaphalium

gaudichaudianumDC.

Asteraceae Cough 10

Passiﬂora umbilicata (Griseb.) Harms

Passiﬂoraceae Bruises 10

Tessaria fastigiata (Griseb.) Cabrera

Asteraceae Malnutrition 9

Calceolaria engleriana Kraenzl.

Scrophulariaceae Fracture/sprains 9

Mutisia ledifoliaDecne.

ex Wedd.

Asteraceae Cough 9

aCulture-bound syndrome associated with heavy labour on agricultural ﬁelds;

several of its symptoms correspond with the biomedical deﬁnition of a hernia, but according toVandebroek et al. (2008)it could be related to Chagas’ disease.

3.3.3. Medicinal plant species

On average, 4.3 (±1.4) participants provided ethnomedicinal information on a medicinal plant species. The medicinal use of 86 (25% of the total number of medicinal plants) and 147 species (43%) was conﬁrmed by only one and two participants, respectively.

Species with the most diverse ethnomedical applications are listed inTable 2. The majority of species in this list are also native ones.

The species presented inTable 2also obtained high scores for medicinal use values (UVs) and quality use values (QUVs) (Table 3), partly because medicinal UVs and QUVs values are correlated with the number of medicinal applications per species (Kendall’s b= 0.75 and 0.62, respectively;p< 0.001 for both). As shown in Table 2

Medicinal plant species with highest number of different medicinal applications.

Scientiﬁc name Family #part #med uses

Schinus molleL. Anacardiaceae 12 17

Medicago sativaL.^a Fabaceae 9 17

Trixis aggregataRusby Asteraceae 13 13

Schkuhria pinnata(Lam.) Kuntze ex Thell.

Asteraceae 12 13

Baccharis sagittalis(Less.) DC. Asteraceae 10 13 Otholobium pubescens(Poir.) J.W.

Grimes

Fabaceae 12 12

Cestrum parquiL’Hér. Solanaceae 11 12

Tripodanthus acutifolius(Ruiz &

Pav.) Tiegh.

Loranthaceae 10 12

Agalinis lanceolata(Ruiz & Pav.) D’Arcy

Scrophulariaceae 11 12

Solanum nitidumRuiz & Pav. Solanaceae 12 12

Ephedra americanaHumb. et Bonpl. ex Willd.

Ephedraceae 12 12

Sonchus asper(L.) Hill^a Asteraceae 10 12

Caiophora canarinoides(Lenné &

K. Koch) Urb. & Gilg

Loasaceae 12 11

Satureja boliviana(Benth.) Briq. Lamiaceae 5 11

Lepechinia meyenii(Walp.) Epling Lamiaceae 9 11

Rosa×noisettianaThory cf.^a Rosaceae 10 11

Valeriana decussataRuiz & Pav. Valerianaceae 10 11 Cheilanthes scariosa(Sw.) C. Presl. Pteridaceae 10 11

Ephedra rupestrisBenth. Ephedraceae 10 11

Calceolaria parvifoliaWedd. ssp.

parvifolia

Scrophulariaceae 8 10

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

aIntroduced species.

Table 3, medicinal quality use values are consistently lower than use values since not all reported ethnomedical applications of species are of “good” quality. To demonstrate the relevance of calculat- ing quality use values over use values, we regressed the medicinal quality use values of species on their medicinal use value. This regression results in aR²value of 81.6, which indicates that assigning a quality to medicinal uses explains nearly one ﬁfth (18.4%) of the variance in QUVsvalues.

A weakness of UVsis that it does not satisfactorily incorporate consensus among participants. For example, if three participants each name two different medicinal uses for species A, then its medicinal use value equals two ((2 + 2 + 2)/3) and the number of reported health conditions six. If these participants unanimously agree that species B is used for treating two different health conditions, the result is also a medicinal use value of two, while consensus for species A is zero and for species B it is 100%.

QUVsvalues seem to express participant consensus better than UVs. It is noticeable how ranking based on QUVsvalues (Table 3) includes species that have the highest consensus for particular remedies (Table 1) together with species that have the most diverse ethnomedical applications (Table 2). Ranking based on UVsvalues seems to favour the latter species more. This property of QUVsto partially incorporate participant consensus might be related to the fact that a higher consensus about remedies parallels a higher frequency of responses related to remedies that are considered to be of “good quality”. A technique that takes into account participant consensus and thus can be used to evaluate the latter assumption is the informant agreement ratio (IAR) for medicinal species. We interpreted the formula originally proposed byTrotter and Logan (1986)as follows:

0<IAR_s=nr−na

nr−1 <1

wherebynris the total number of medicinal responses registered for speciessandnais the number of ailments or health conditions that are treated with this species. The IAR_sof a medicinal species varies between 0 (when the number of health conditions treated equals the number of medicinal responses) and 1 (whereby all participants agree upon the exclusive use of the species for a particular health condition).

When applied to our data set, species’ IARsvalues correlate positively with the number and proportion of “good quality” responses per species (Kendall’s b= 0.30 (p< 0.001) and 0.14 (p= 0.004), respectively), conﬁrming our hypothesis that species for which participant consensus is higher also yield more “good quality”

responses. Hence, since a species’ QUVsis also positively correlated with the number of “good quality” medicinal responses per species (Kendall’sb= 0.64;p< 0.001), this may explain in part why QUVs

expresses consensus better than UV_s. These observations corrobo- rateCasagrande’s (2002)argument that emic perception of efﬁcacy is the variable that most accounts for the distribution of knowledge about medicinal plants. Other authors have also argued that, in many cases, consensus correlates with (pharmacological) efﬁcacy (Trotter and Logan, 1986; Moerman, 2007).

Table 4 lists medicinal species with the highest IARs values. Although both medicinal UVsand QUVscorrelate with IARs

(Kendall’sb= 0.41 and 0.30, respectively;p< 0.001 for both cases), ranking of species based on IARsvalues give different results as compared to ranking based on medicinal UVs and QUVs values (Table 3). The only species that occur in both tables areAchyrocline ramosissima, Tessaria fastigiata, Passiﬂora umbilicata, Gnaphalium gaudichaudianum and Minthostachys andina. This outcome is, at least in part, due to the fact that rankings based on UVsand QUVs

values favour plant species with multiple medicinal applications, whereas IAR_smainly selects species with high participant consensus. For example, a plant with only one medicinal application that

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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 IARsvalues are underlined in the corresponding columns.

Scientiﬁc name Family #med uses #part UVs QUVs IARs

Trixis aggregataRusby Asteraceae 13 13 2.46 2.00 0.61

Schinus molleL. 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 parquiL’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 sativaL.^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 tripartitumDunal Solanaceae 6 9 1.55 0.83 0.62

Solanum nitidumRuiz & 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 palitansC.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 gaudichaudianumDC. 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 englerianaKraenzl. Scrophulariaceae 7 14 1.29 1.17 0.65

Geranium sorataeR. Knuth Geraniaceae 5 8 1.13 1.13 0.50

Mentzelia fendlerianaUrb. & Gilg Loasaceae 5 5 1.20 1.10 0.20

is known to all interviewed participants will receive UV_sand QUV_s values of maximally 1, and therefore has little chance of being listed among the most important medicinal species. On the other hand, its IARsvalue would also be 1, acknowledging the maximum level of consensus. In line with this observation, the number of different medicinal uses per species is signiﬁcantly higher (p< 0.001;

Mann–Whitney) for species with high medicinal UVsand QUVsval- ues (listed inTable 3) than for species with high IARsvalues (listed inTable 4).

Use values imply that the local importance of a plant is primarily determined by its number of medicinal uses. This proposition has rarely been tested, butByg and Balslev (2001)were able to show a positive correlation between the perceived importance of palm species by local participants in Madagascar and their use values and number of uses. Although this relation might be valid whenall different plant uses are pooled together, it is not necessarily so for medicinal plant use. We believe that assessing the local importance

of a medicinal plant should not be based solely on the number of uses or use values of the respective species, but on a combination of the former and the level of consensus between participants. The QUVsand IARsindexes we proposed here seem highly suitable for this purpose. Medicinal QUVsvalues appear to be more sensitive to the number of ethnomedical applications per plant species and incorporate the emic perception of therapeutic qualities, whereas IARsvalues address informant consensus. Therefore, our proposal is to combine both parameters into the ‘Quality Use Agreement Value’

(QUAVs), which is deﬁned as:

QUAV_s=QUV_s×IAR_s

In Table 5, ranking of the twenty highest scoring medicinal species according to QUAVs values shows that species from the top twenty ranking according to IARsand QUVs, respectively are represented in relatively even proportions (10 and 13 species, respectively). Hence, this index seems to provide a valid and easily Table 4

IARsvalues 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 brachyacanthaMiers 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 viscosaJacq. Sapindaceae 14 17 5 0.75

Echeveriasp. (ET468) Crassulaceae 13 13 4 0.75

Gamochaeta americana(Mill.) Wedd. Asteraceae 10 9 3 0.75

Trichocereus tunariensisCardenas Cactaceae 8 9 3 0.75

Plantago orbignyanaSteinh. Plantaginaceae 11 9 3 0.75

Hypseocharis pimpinellifoliaRemy Oxalidaceae 13 13 4 0.75

Vassobia fasciculata(Miers) Hunz. Solanaceae 15 19 6 0.72

Gnaphalium melanosphaeroidesSch.Bip. ex Wedd. Asteraceae 9 8 3 0.71

Margyricarpus pinnatus(Lam.) Kuntze Rosaceae 10 8 3 0.71

Spathantheum orbignyanumSchott Araceae 13 15 5 0.71

Gnaphalium gaudichaudianumDC. Asteraceae 12 15 5 0.71

Rumex conglomeratusMurray^a Polygonaceae 8 11 4 0.70

Cosmos peucedanifoliusWedd. 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.

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Table 5

Ranking of medicinal species according to decreasing Quality Use Agreement Values (QUAVs). Species from the top twenty ranking of QUVsand 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 aggregataRusby 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 gaudichaudianumDC. 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 englerianaKraenzl. 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 parquiL’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 molleL. 17 14 2.14 1.42 0.45 0.64

Dodonaea viscosaJacq. 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 cheiranthifoliumLam. 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 sorataeR. 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 melanosphaeroidesSch.Bip. ex Wedd. 3 9 0.89 0.78 0.71 0.56

Solanum palitansC.V. Morton 8 9 1.44 1.33 0.42 0.56

Hypseocharis pimpinellifoliaRemy 4 13 1.00 0.73 0.75 0.55

derived estimation of a medicinal plant’s cultural signiﬁcance, at least for the case of Apillapampa.

4. Conclusions

Our ﬁndings add value to the observation in literature that indigenous pharmacopoeias around the world are far from random assemblages. Some families clearly hold more medicinal species than predicted by chance. The same reasoning also seems to apply to different life forms in Apillapampa, where plants with a shrubby habit are signiﬁcantly overused. It is hypothesized that this is related to the year-round availability of shrubs, as compared to most annual and herbaceous plants that disappear during the dry season.

Emic perception of medicinal plant efficacy varies from one species to another in Apillapampa. All local Quechua participants (both healers and laypeople) recognise that some species are more effective for treating particular symptoms or health conditions than others. Therefore, we believe that the quality of remedies should be taken into account when ranking plants according to their cultural importance. The applicability of the technique to incorporate the quality of plant use (i.e. quality use values; QUV_s), proposed by us in this paper provides a ‘novel’ way to approach and interpret plant use data, in the medicinal use category and beyond. In addition, we have shown that a combination of QUV_swith a re-interpreted consensus index regarding the medicinal use of species (IARs) in the QUAVs, might rep- 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) the perceived quality of those medicinal uses; and (3) participant consensus about those medicinal uses. In the top ranking of medicinal plants according to the present study using QUAVs, species from the top rankings according to IARsand QUVs, respectively, are represented in relatively even proportions. Therefore the QUAV_s index seems to provide an easily derived and valid assessment of a plant’s significance within a culture. Future pharmacological studies are needed to determine if these culturally most significant species also show the highest levels of bioactivity.

Acknowledgements

The ﬁrst study was funded by the Institute for the Promo- tion of Innovation through Science and Technology in Flanders (IWT), Belgium, by means of a post-doctoral grant to Ina Van- debroek. The second study was ﬁnanced by a doctoral research grant of the Bijzonder Onderzoeksfonds (BOF) of Ghent Univer- sity to Evert Thomas (Grant Number: B/03801/01 FONDS IV 1).

We are grateful to Jan-Bart Calewaert, Ben Michiels, Lisa De Munk, Trees Cousy, Frieke Heens and David Douterlungne for collaboration during data collection. Logistic support in Bolivia was provided by the Centre of Biodiversity and Genetics and the Herbarium Martin Cardenas of the Universidad Mayor de San Simon in Cochabamba. Special thanks are due to the inhabitants and Subcentral of the community of Apillapampa for their kind assistance in making this project successful. We are also indebted to the professional botanists who identiﬁed several collections. They are S. Beck (ﬂora of Bolivia), S. Clemants (Chenopodiaceae), E. Emshwiller (Oxalidaceae), H.-J. Esser (Euphor- biaceae), R. Faden (Commelinaceae), A. Freire (Polygalaceae), D.

Goyder (Asclepiadaceae), I. Jiménez (Bolivian Pteridophyta), A.

Krapovickas (Malvaceae), J. Müller (BaccharisandHieracium,Aster- aceae), G. Navarro (Cactaceae), M. Nee (Solanaceae), A. Planchuelo (Lupinus, Fabaceae), J. Pruski (Asteraceae), L. Rico (Fabaceae), C. Ulloa (Berberidaceae), R. Vasquez (Bromeliaceae and Orchi- daceae), D. Wasshausen (Asclepiadaceae), J. Wood (Asclepiadaceae and Salvia, Lamiaceae) and C. Xifreda (Dioscorea, Dioscore- aceae).

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