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Research paper Can organoleptic properties explain the differential use of medicinal plants? Evidence from Northeastern Brazil Patrícia Muniz de Medeiros a,n , Bárbara Luzia Santos Pinto a , Viviany Teixeira do Nascimento b a Universidade Federal do Oeste da Bahia, Centro das Ciências Biológicas e da Saúde, Estrada para o Barrocão, s/n, Morada Nobre, 47800-000 Barreiras-BA, Brazil b Universidade do Estado da Bahia, Campus IX. Rodovia BR 242, km 4, s/n, Loteamento Flamengo, 47800-000 Barreiras-BA, Brazil article info Article history: Received 9 September 2014 Received in revised form 30 October 2014 Accepted 1 November 2014 Available online 11 November 2014 Keywords: Ethnomedicine Traditional medicine Medicinal plant selection Brazil abstract Ethnopharmacological relevance: This study examined how people classify plants in terms of their taste and smell, and how those organoleptic properties inuence the differential use of medicinal plants for treating different diseases. Methods: We conducted an ethnobotanical survey of household heads in the community of Sucruiu, located in Barreiras, Bahia, Brazil. The head of each family was questioned concerning their knowledge and use of medicinal plants, as well as the therapeutic indications (TIs), taste, and smell of each plant. We then tested for associations between the therapeutic indications and taste attributes of various plants using the Chi-squared test on a contingency table with Monte Carlo simulations. The same analysis was performed for associations between TIs and smell. Results: The study participants provided more details when classifying tastes than when classifying smells. We considered only the most cited TIs and attributes, and found signicant associations between both taste and therapeutic indications (p o0.001) and smell and therapeutic indications (p o0.0001). Conclusions: Our results showed that the taste and smell of a plant can inuence its differential medicinal use, since plants with certain tastes and smells prevailed in the treatment of distinct diseases. However, our results are valid only for the most popular TIs and organoleptic attributes. & 2014 Elsevier Ireland Ltd. All rights reserved. 1. Introduction One central interest of ethnobotanical research is to identify factors that inuence a plant's selection and differential use by local communities (Medeiros et al., 2013 a, 2013b). Previous investigations have sought to understand whether factors such as a species' availability (Lawrence et al., 2005; Lucena et al., 2012), bioactivity (Omar et al., 2000; Araújo et al., 2008) or organoleptic properties (Leonti et al., 2002; Molares and Ladio, 2009) may explain its popularity and application for treating certain disorders. A plant's taste and smell can play an important role in its selection for medicinal use by local populations, and such attri- butes are directly associated with the presence of certain second- ary plant metabolites. It is possible that some organoleptic attributes act as determinants of plant selection, clues of bioactiv- ity, or serve a mnemonic function (Medeiros et al. 2013a), which enables people to have taste-based and smell-based information that can be used for experimenting and innovating traditional knowledge (Heinrich, 2003; Molares and Ladio, 2008). Some ethnobotanical studies have reported the importance of organoleptic attributes when distinguishing between medicinal and non-medicinal plants (Ankli et al., 1999; Leonti et al., 2002). Furthermore, we believe that the differential use of medicinal plants (use of different plants for distinct purposes) can be explained by attributes such as taste and smell. While previous investigators have found that certain diseases are mostly treated with plants that have specic tastes or smells (Ankli et al., 1999; Leonti et al., 2002; Heinrich, 2003), these reports have been limited to only a few diseases. Our current study examined the association between a plant's taste and smell, and its selection for treatment of a wide variety of diseases, with the goal of determin- ing whether such an association can be generalized or is limited to particular diseases. We hypothesized that a plant's taste and smell inuence its selection for treating specic diseases, and examined whether the differential use of medicinal plants be explained by their organo- leptic properties. Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/jep Journal of Ethnopharmacology http://dx.doi.org/10.1016/j.jep.2014.11.001 0378-8741/& 2014 Elsevier Ireland Ltd. All rights reserved. n Corresponding author. Tel.: þ55 7736143113. E-mail address: [email protected] (P.M. de Medeiros). Journal of Ethnopharmacology 159 (2015) 4348

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Page 1: Can organoleptic properties explain the differential use of medicinal plants? Evidence from Northeastern Brazil

Research paper

Can organoleptic properties explain the differential use of medicinalplants? Evidence from Northeastern Brazil

Patrícia Muniz de Medeiros a,n, Bárbara Luzia Santos Pinto a,Viviany Teixeira do Nascimento b

a Universidade Federal do Oeste da Bahia, Centro das Ciências Biológicas e da Saúde, Estrada para o Barrocão, s/n, Morada Nobre,47800-000 Barreiras-BA, Brazilb Universidade do Estado da Bahia, Campus IX. Rodovia BR 242, km 4, s/n, Loteamento Flamengo, 47800-000 Barreiras-BA, Brazil

a r t i c l e i n f o

Article history:Received 9 September 2014Received in revised form30 October 2014Accepted 1 November 2014Available online 11 November 2014

Keywords:EthnomedicineTraditional medicineMedicinal plant selectionBrazil

a b s t r a c t

Ethnopharmacological relevance: This study examined how people classify plants in terms of their tasteand smell, and how those organoleptic properties influence the differential use of medicinal plants fortreating different diseases.Methods: We conducted an ethnobotanical survey of household heads in the community of Sucruiu,located in Barreiras, Bahia, Brazil. The head of each family was questioned concerning their knowledgeand use of medicinal plants, as well as the therapeutic indications (TIs), taste, and smell of each plant. Wethen tested for associations between the therapeutic indications and taste attributes of various plantsusing the Chi-squared test on a contingency table with Monte Carlo simulations. The same analysis wasperformed for associations between TIs and smell.Results: The study participants provided more details when classifying tastes than when classifyingsmells. We considered only the most cited TIs and attributes, and found significant associations betweenboth taste and therapeutic indications (po0.001) and smell and therapeutic indications (po0.0001).Conclusions: Our results showed that the taste and smell of a plant can influence its differentialmedicinal use, since plants with certain tastes and smells prevailed in the treatment of distinct diseases.However, our results are valid only for the most popular TIs and organoleptic attributes.

& 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

One central interest of ethnobotanical research is to identifyfactors that influence a plant's selection and differential use bylocal communities (Medeiros et al., 2013 a, 2013b). Previousinvestigations have sought to understand whether factors suchas a species' availability (Lawrence et al., 2005; Lucena et al., 2012),bioactivity (Omar et al., 2000; Araújo et al., 2008) or organolepticproperties (Leonti et al., 2002; Molares and Ladio, 2009)may explain its popularity and application for treating certaindisorders.

A plant's taste and smell can play an important role in itsselection for medicinal use by local populations, and such attri-butes are directly associated with the presence of certain second-ary plant metabolites. It is possible that some organolepticattributes act as determinants of plant selection, clues of bioactiv-ity, or serve a mnemonic function (Medeiros et al. 2013a), which

enables people to have taste-based and smell-based informationthat can be used for experimenting and innovating traditionalknowledge (Heinrich, 2003; Molares and Ladio, 2008).

Some ethnobotanical studies have reported the importance oforganoleptic attributes when distinguishing between medicinaland non-medicinal plants (Ankli et al., 1999; Leonti et al., 2002).Furthermore, we believe that the differential use of medicinalplants (use of different plants for distinct purposes) can beexplained by attributes such as taste and smell. While previousinvestigators have found that certain diseases are mostly treatedwith plants that have specific tastes or smells (Ankli et al., 1999;Leonti et al., 2002; Heinrich, 2003), these reports have beenlimited to only a few diseases. Our current study examined theassociation between a plant's taste and smell, and its selection fortreatment of a wide variety of diseases, with the goal of determin-ing whether such an association can be generalized or is limited toparticular diseases.

We hypothesized that a plant's taste and smell influence itsselection for treating specific diseases, and examined whether thedifferential use of medicinal plants be explained by their organo-leptic properties.

Contents lists available at ScienceDirect

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

Journal of Ethnopharmacology

http://dx.doi.org/10.1016/j.jep.2014.11.0010378-8741/& 2014 Elsevier Ireland Ltd. All rights reserved.

n Corresponding author. Tel.: þ55 7736143113.E-mail address: [email protected] (P.M. de Medeiros).

Journal of Ethnopharmacology 159 (2015) 43–48

Page 2: Can organoleptic properties explain the differential use of medicinal plants? Evidence from Northeastern Brazil

2. Methods

2.1. Study area

This study was conducted in 2012 in the rural community ofSucruiu (12112029,060 0S and 45115024,030 0W), located in the muni-cipality of Barreiras, in the Western region of the state of Bahia,Brazil (Fig. 1). The municipality covers 7859.225 km2 (IBGE, 2010),and has seasonally dry vegetation. Its population of 136,427inhabitants (IBGE, 2010) and the majority of economic activityare related to agribusiness.

Although commercial large-scale agriculture has a substantialpresence in Barreiras, it coexists with small-scale agriculturaloperations in local communities such as Sucruiu. Sucruiu is located25 km from the nearest urban area, and has 21 households and 38family chiefs.

In terms of ethnicity, Sucruiu is constituted of mixing races, asits inhabitants are descendants of European, African and Indigen-ous people. Researchers commonly use the terms ‘setanejos’ or‘cultura sertaneja’ (better translated as backcountry culture) todescribe mixed race farming communities from seasonally dryBrazilian areas (Lütkemeier, 2014). However, the ‘sertanejos’cannot be considered as culturally homogeneous, since differencescan be found in their social organization and subsistence activities.

Most men in Sucruiu are native to the community, while thewomen are mostly from neighboring communities, and migratedto Surruiu after marrying Scuruiu men. While the men are mostlydedicated to agricultural activities and the extraction of commer-cial forest products, women work in commerce, service, agricul-ture, and/or domestic activities.

The community has a Catholic church (main religion in thearea) and a public elementary public school. Students seekinghigher academic degrees must travel to neighboring communitiesor the Barreiras urban area. In terms of access to public health, thecommunity does not have a health center; however, health agentsfrom the Barreiras urban area often visit community members.

In term of therapeutic options, the community presents a pluralmedical system, since traditional and official medicines coexist.

Similar to other rural communities in Northeastern Brazil,young natives continuously migrate to urban centers, leading totheir decreased numbers in Sucruiu.

2.2. Data collection

This study was conducted in accordance with guidelinesdeveloped by the National Health Counsel by means of theResearch Ethics Committee (Resolution 196/96), and the protocolwas approved by that committee (CAAE 07488513.4.0000.5026).

The community of Sucruiu was fully informed concerning thegoals of this study, and members who agreed to participate wereinvited to sign a Free and Clarified Consent Term. We interviewed21 family chiefs (men and women). This number of participantswas reached because 17 individuals did not want to participate orwere not located even after several attempts. We performed afree-listing of medicinal plants that each individual knew of and/orhad used, including the parts utilized, their therapeutic indica-tions, and their attributes of taste and smell.

Species cited by the informants were collected and thenidentified by consultations with specialists and comparisons withherbarium material. The samples were deposited at the herbariumof the Universidade Federal do Oeste da Bahia, and the herbariumof the Universidade do Estado da Bahia (Campus IX).

2.3. Data analysis

The relative importance (RI) of each plant was calculated by themethod of Bennett and Prance (2000) using the following equa-tion: IR¼(NTIx/NTIVE)þ(NBSx/NBSVE), where NTIx is the numberof therapeutic indications (TIs) for the species x; NTIVE is thenumber of therapeutic indications for the most versatile species;NBSx is the number of body systems of the species x, and NBSVE is

Fig. 1. Map of the study area emphasizing the state of Bahia, Western region and the municipality of Barreiras.

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the number of body systems for the most versatile species. TheWorld Health Organization database was used to classify indica-tions according to their body systems (WHO, 2010).

The number of citations for each taste and smell was recorded.A citation was considered to be the ‘Species’-‘TIs’-‘Used part’-‘Taste’ link, and the ‘Species’-‘TIs’-‘Used part’-‘Smell’ link. Forexample, if the interviewee 1 cited the bitter seeds of Pterodonemarginatus Vogel to treat influenza and the same intervieweecited the bitter bark of Pterodon emarginatus to treat influenza, weconsidered them as two different citations. Therefore, any kind ofvariation in the species, therapeutic indication, used part, andtaste or smell led to a different citation.

The Chi-squared test on a contingency table was used to testwhether different therapeutic indications were treated with plantshaving distinct organoleptic properties (‘use’-‘taste’ association or‘use’-‘smell’ association). As many values on the contingencytables were o5, we adjusted the p-Value with Monte Carlosimulations (10,000 simulations). This test was developed in fourdifferent models: (1) considering all cited therapeutic indicationsand all perceived tastes; (2) considering all cited therapeuticindications and all perceived smells; (3) considering only thetherapeutic indications with 410 citations and tastes with 410citations; (4) considering only the therapeutic indications with410 citations and smells with 410 citations.

3. Results

3.1. Taste and smell perceptions

The study participants provided more details when classifyingtastes than when classifying smells. ‘Bitter taste’ had the mostcitations (36.4%), followed by ‘good taste’ (22%), ‘no taste’ (21.8%),‘bad taste’ (5.5%), and ‘sweet taste’ (2.7%); all these tastes had 410citations. Tastes with r10 citations included ‘acid’ and ‘astrin-gent’, as well as comparative tastes (‘orange-like taste’, ‘mint-liketaste’, etc).

Descriptions of smell were much less diverse, with 41.4% of thecitations recorded as ‘no smell’, 31.5% as ‘good smell’, and 7.1% as‘bad smell’. Furthermore, only those three smell attributes reached410 citations. Among the less cited attributes were comparativedescriptions such as ‘onion-like smell’, ‘mint-like smell’, ‘tick-likesmell’, and ‘disease-like smell’.

3.2. More versatile species and their organoleptic attributes

The species with the highest RIs were Melissa officinalis L. (2),Cymbopogon citratus (DC.) Stapf (1.92), Amburana cearensis (Alle-mão) A.C. Sm. (1.92), Aloe vera (L.) Burm. f. (1.58), and Pterodonemarginatus Vogel (1.58). Leaves were the most cited part forMelissa officinalis, Cymbopogon citratus, and Aloe vera, while seedswere most often cited for Amburana cearensis and Pterodonemarginatus.

Regarding the attribution of tastes to the most cited parts of themost versatile species (Table 1) we found a strong consensusamong the interviewee, given that at least 50% of them agreed onthe plant's taste for all cases. For the attributes of smell somehighly versatile species had 33% of agreement (Table 1).

3.3. Main therapeutic indications

The therapeutic indications with 410 citations are listed inTable 2. Three of those indications are associated with inflamma-tory processes (inflammation in general, throat inflammation, anduterine inflammation).

3.4. Association between therapeutic indications and organolepticproperties

When considering all cited therapeutic indications and tastes(model 1), the chi-squared test did not identify an associationbetween TI and taste (χ2¼772.4; p40.05). The same result wasfound for TI and smell in model 2 (χ2¼784.9; p40.05). However,when considering only the TIs and tastes with 410 citations(model 3), these two factors showed a significant association(χ2¼74.4; po0.001), and a similar result was shown for TI andsmell in model 4 (χ2¼58.6; po0.0001).

The association between TI and taste (for the most conspicuousTIs and tastes) was found because while plants classified as bitterdominated for some TIs, plants with good taste and no taste weremore commonly used to treat other TIs (Fig. 2). In addition, plantswith a ‘good smell’ predominated for some indications, whileplants with ‘no smell’ were more often cited for other indications(Fig. 3).

4. Discussion

4.1. Taste and smell perceptions

Previous studies have also shown a higher consensus on tasteclassification compared to smell classification (Molares and Ladio,2008, 2009). In addition, other studies also gathered more detailedinformation for taste than for smell, given that attributes of smellare often less numerous than attributes of taste; and/or theattribute ‘no smell’ often has more citations than the attribute‘no taste’ (Ankli et al., 1999; Leonti et al., 2002; Molares and Ladio,2008, 2009).

While some attributes of taste were well detailed for our study(e.g. bitter), others were restricted to ‘good’ and ‘bad’, with nofurther information. We believe that these two categories hideother taste attributes, such as sweetness, astringency etc., whichare commonly cited in other studies (Ankli et al., 1999; Leontiet al., 2002; Molares and Ladio, 2008, 2009).

The citation of plants classified as having both ‘no taste’ and ‘nosmell’ in this study and many other investigations can mean two

Table 1Attributes of taste and smell for the most cited parts of the most versatile (higher Relative Importance) medicinal plants of the community of Sucruiu, Northeasten Brazil.

Species Voucher numbera Main part % Most cited taste % Most cited smell %

Melissa officinalis L. b Leaf 100 Good taste 75 Good smell 87.5Cymbopogon citratus (DC.) Stapf BRBA 5.551 Leaf 85.7 Good taste 66.7 Good smell 83.3Amburana cearensis (Allemão) A.C. Sm. BRBA 5.484 Seed 88.9 Bitter taste 50 Good smell 50Aloe vera (L.) Burm. f. b Leaf 71.4 Bad taste 60 Tick-like smellNo smell 33Pterodon emarginatus Vogel BRBA 5.621 Seed 54.5 Bitter taste 83.3 No smell 33

%¼percentage of participants that indicated a plant part or organoleptic attribute for a given plant, considering only the participants that mentioned that plant.a Voucher numbers for the herbarium of the Universidade Federal do Oeste da Bahia.b Plant identification in the field.

P.M. de Medeiros et al. / Journal of Ethnopharmacology 159 (2015) 43–48 45

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things: (1) all of those plants were odorless and tasteless; (2) thelow familiarity with less popular plants having only slight tastesand smells can lead to a lower distinction of their attributes, evenif those low-popularity plants are offered for the interviewee tosmell and taste at the moment of the interview. In fact, althoughsome popular medicinal plants were considered as tasteless ofodorless, most species with these attributes were low-popularityplants.

The significance of a bitter taste among medicinal plants found inour study has been mentioned in other investigations (Ankli et al.,1999; Leonti et al., 2002; Heinrich, 2003), and a further discussion ofthis topic is found in Section 4.5 of this manuscript. However, otherstudies differed from ours concerning the importance of someattributes. For example, astringent taste was not commonly citedfor Sucruiu plants, but was a very relevant attribute in other studies(Ankli et al. 1999; Leonti et al., 2002).

4.2. More versatile species and their organoleptic attributes

The species with higher RI values in our study were oftenhighlighted in other investigations conducted in Brazil and eventhroughout the world (Albuquerque et al., 2007; Negrelle andFornazzari, 2007; Biswas et al., 2011; Medeiros et al., 2013b). Threeof five species with the highest RI values are highly popular exoticspecies (Melissa officinalis, Cymbopogon citratus and Aloe vera), andtwo are native to Brazil and often used in the Brazilian Cerrado(Pterodon emarginatus and Amburana cearensis).

Only a small number of studies have investigated the influenceof organoleptic properties on the differential use of medicinalplants. Therefore, it is difficult to assess whether the tastes andsmells as classified in Sucruiu are similarly classified in othergeographic areas. Leonti et al. (2002) reported that a speciesidentified as Aloe sp. was classified as having a ‘bad taste’ and a‘bitter taste’, which partially agrees with the ‘bad taste’ classifica-tion for Aloe vera in Sucruiu.

Finally, a study conducted in Argentinean Patagonia (Molaresand Ladio, 2009) showed that interviewees had 100% agreement

on both the taste and smell of Melissa officinalis. Our study alsoshowed high agreement on the taste and smell of this species,which supports the high perceptibility of these attributes for thisspecies.

4.3. Main therapeutic indications

Results of previous studies have shown certain similaritiesregarding the main therapeutic indications mentioned in ethno-botanical surveys. One of the most remarkable patterns is theprominence of digestive problems, in terms of citations or thenumber of plants used to treat these disorders (Felger and Moser,1974; Heinrich et al., 1998; Novais et al., 2004; Giday et al., 2007;Zone et al., 2007; Jeruto et al., 2008; Giday et al., 2009;Teklehaymanot, 2009; Weckerle et al., 2009; Afroz et al., 2011;Bruschi et al., 2011; Rehecho et al., 2011).

Respiratory disorders and inflammation are also prominentlymentioned in ethnobotanical surveys (Heinrich et al., 1998;Bradacs et al., 2011; Rehecho et al., 2011; Calvet-Mir et al., 2008).Although inflammation is commonly treated as a homogeneouscategory in the ethnobotanical literature, it is incorrect to do so.Ferreira-Júnior et al. (2011) studied plants from the Braziliansemiarid region used to treat inflammation, and recorded 37inflammation categories characterized by 26 different symptoms.Interestingly, they also found several differences concerning theplant-based treatment used for each type of inflammation. Thisfurther verified that inflammation could not be considered as auniform disorder. Our finding that different plant tastes prevailedin distinct inflammation categories also supports the heterogene-ity of these indications (e.g., ‘bitter taste’ for general inflammationand uterine inflammation, and ‘no taste’ for throat inflammation).

4.4. Association between therapeutic indications and organolepticproperties

Our finding that therapeutic indications and organolepticproperties were only associated in models 3 (only the most citedTIs and tastes) and 4 (only the most cited TIs and smells) have thefollowing implications: (1) taste and smell can only suggest aplant's medicinal use when it is a popular and characteristic tasteor smell; (2) taste and smell can only suggest a medicinal plant'suse in cases of popular diseases which frequently need treatment.

Some associations between organoleptic attributes and ther-apeutic indications reported in previous studies were also found inour current investigation, and this was especially true concerningattributes of taste. One interesting example can be found in astudy conducted by Leonti et al. (2002) among the MexicanPopoluca. Those study participants use a humoral classificationin which plants are considered ‘hot’ and ‘cold’; thus hot plants cantreat cold diseases and vice-versa (Leonti et al., 2002). Fever is agood example of a hot disease. For the Popoluca, bitter plants areconsidered as ‘hot’, and are only used to treat cold disorders

Table 2Therapeutic indications with more than 10 cita-tions in the community of Sucruiu, NortheasternBrazil.

Therapeutic indication No. of citations

Indigestion 57Inflammations in general 49Influenza 40Stomachache 20Cicatrizing 15Throat inflammation 14Calming 13Gastritis 12Fever 12Uterine inflammation 11

Fig. 2. Predominance (in terms of citations) of plant tastes for the most cited therapeutic indications in the community of Sucruiu, Northeastern Brazil (only tastes andindications with more than 10 citations). Therapeutic indications with wider bars were more cited than indications with narrower bars.

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(Leonti et al. 2002). Although there is no similar humoral classi-fication used in the community of Sucruiu, we did notice that nobitter tasting plants were used to treat fever, while all othercommon diseases (410 citations) were treated by at least onebitter plant.

4.5. Bitter taste and its medicinal application

The prevalence of a bitter taste among the medicinal plantsidentified in this study was not random. This taste is provided by awide variety of chemical compounds with the potential to treatseveral disorders. Bitter taste is common in plants containingterpenoids (Brieskorn, 1990; Ankli et al., 1999), alkaloids(Drewnowski, 1997), and phenols (Brieskorn, 1990). Among thephenols, flavonoids are especially notable for their bitter taste,given that high molecular weight phenols (tannins) are commonlyastringent (Noble, 1994; Drewnowski and Gomez-Carneros, 2000).

The role which bitter taste plays in medicinal plant selectionremains unclear. Studies focusing on food products suggest thatthis taste is directly related to toxicity, since most toxic com-pounds found in nature are bitter (Glendinning, 1994). Therefore,many animals (humans included) may have developed an adaptiveresponse so as to reject ingesting bitter tasting resources(Glendinning, 1994; Kurihara et al., 1994).

If the hypothesis of bitter-taste rejection as an adaptiveresponse is valid, the preferential consumption of bitter tastingmedicinal plants in the community of Sucruiu should be mostlyrelated to cultural learning rather than a genetically fixed recogni-tion mechanism based on sensorial markers. Therefore, bitter tasteprovides a clue to a plant's medicinal use rather than being adeterminant of its use via chemical recognition.

5. Conclusion

While the association between organoleptic properties andtherapeutic indications cannot be considered valid for the entiremedical system, it does apply for particular attributes and clinicalindications, and especially for the most popular ones in theSucruiu medical system. While we believe our results supportthe validity of this association, they are restricted to the studiedcommunity. Therefore, future studies should consider the entiremedical system (all tastes, smells and therapeutic indications) inorder to better understand the true role of organoleptic propertiesin the differential use of medicinal plants.

Acknowledgments

We thank the community of Sucruiu for their kind receptionand participation in this study. We especially thank Justino and

Claudina for their support and friendship. We also thank CNPq(141121/2010-6) for the grant given to the first author.

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Fig. 3. Predominance (in terms of citations) of plant smells for the most cited therapeutic indications in the community of Sucruiu, Northeastern Brazil (only smells andindications with more than 10 citations). Therapeutic indications with wider bars were more cited than indications with narrower bars.

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