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1 23 Environment, Development and Sustainability A Multidisciplinary Approach to the Theory and Practice of Sustainable Development ISSN 1387-585X Environ Dev Sustain DOI 10.1007/s10668-017-0023-9 Conservation priorities for medicinal woody species in a cerrado area in the Chapada do Araripe, northeastern Brazil Daiany Alves Ribeiro, Delmacia Gonçalves de Macedo, Liana Geraldo Souza de Oliveira, Maria de Oliveira Santos, Bianca Vilar de Almeida, et al. 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media B.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. 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Conservation priorities for medicinal woody species in a cerrado area in the Chapada do Araripe, northeastern Brazil Daiany Alves Ribeiro1 • Delmacia Gonc¸alves de Macedo1 • Liana Geraldo Souza de Oliveira1 • Maria de Oliveira Santos1 • Bianca Vilar de Almeida1 • Julimery Gonc¸alves Ferreira Macedo1 • Ma´rcia Jordana Ferreira Maceˆdo2 • Renata Kelly Dias Souza2 • Thatiane Maria de Souza Arau´jo1 • Marta Maria de Almeida Souza1 Received: 20 July 2017 / Accepted: 8 September 2017 � Springer Science+Business Media B.V. 2017 Abstract Current ethnobiological studies can offer positive aspects when they include the knowledge of traditional communities in developing different strategies for biodiversity conservation. This study aimed to classify medicinal woody species for priority conser- vation site in an area of cerrado disjoint in Chapada do Araripe, northeastern Brazil. The availability of woody medicinal plants and conservation priority scores were achieved by the relative density of the sampled forest fragment and ethnobotanical information obtained through semi-structured interviews with 50 local informants. Sixty-one woody medicinal plants were recorded, belonging to 26 families and 59 genera; 29 of these were available and have the use of bark and inner stem bark associated (46.6%). Himatanthus drasticus (Mart.) Plumel, Caryocar coriaceum Wittm., Ximenia americana L., Croton zehntneri Pax & K. Hoffm., Hymenaea courbaril L., Copaifera lansdorfii Desf., Sideroxylon obtusifolium (Roem. & Schult.) T.D.Penn., Anacardium ocidentale L. and Dimorphandra gardneriana Tull. are some of the priority species needing attention in carrying out conservation measures, in order to ensure the perpetuation of these species and the sustainability of traditional therapeutics practices. Keywords Availability � Biodiversity � Medicinal plants � Priority conservation � Risk collection � Use-values & Daiany Alves Ribeiro daiany_ars@hotmail.com 1 Departamento de Cieˆncias Biolo´gicas, Laborato´rio de Ecologia Vegetal, Universidade Regional do Cariri, Av. Cel. Antoˆnio Luiz, 1161, Crato, CE CEP: 63105-000, Brazil 2 Departamento de Quı´mica Biolo´gica, Universidade Regional do Cariri, Crato, CE 63105-000, Brazil 123 Environ Dev Sustain DOI 10.1007/s10668-017-0023-9 Author's personal copy 1 Introduction Identifying medicinal species with priority for conservation has been an important topic in ethnobiological research (Albuquerque et al. 2009; Oliveira et al. 2007; Souza et al. 2017) as a result of the growing loss of biodiversity caused mainly by man’s action on available natural resources (Andel et al. 2015; Albuquerque et al. 2011; Reddy et al. 2016). With the great interest in herbal medicine, approximately 80% of the world population uses traditional healing systems (Chia et al. 2017; Kong et al. 2009) and natural resources are increasingly being investigated for the development of new medicines (Albuquerque et al. 2012; Kong et al. 2009). In some cases, local practices may lead to unbridled extractivism with excessive collection of specific species, causing natural losses that are often irreversible. In this sense, ethnobotany has been outstanding in the development of strategies for the conservation of medicinal flora through the evaluation of traditional therapies (Albuquerque and Andrade 2002; Albuquerque et al. 2011; Chia et al. 2017; Oliveira et al. 2007). Brazil has one of the largest biodiversity in the world (Giulietti et al. 2005) with a wide diversification of vegetal species. Among the richest biomes, in terms of flora, is the Brazilian savannah area, also known as ‘‘cerrado,’’ which occupies about 24% of the national territory, with approximately 40% of endemic plant species (Borlaug 2002; IBGE 2012; Klink and Machado 2005; MMA 2011). On the other hand, it is one of the most exploited and threatened ecosystems, mainly due to the increase in pasture areas, expan- sion of agriculture and intense local use of woody species (Klink and Machado 2005). Considered one of the 34 global hot spots for biodiversity conservation (Myers et al. 2005), the Brazilian savannah ‘‘cerrado’’ still suffers from a lack of conservation areas for the maintenance of its genetic resources (Andrade et al. 2002) requiring considerably, due to its current situation, recommendations and functional strategies that allow the conservation of resources still available. In the northeast, the fragmented savannas (disjoint ‘‘cerrado’’) occur in the states of Pernambuco, Paraı´ba and Ceara´ (Moro et al. 2011) where there are enclaves mainly on the coastal areas, in the northern part of the Ibiapaba plateau and in the Chapada do Araripe at altitudes above 800 m (Costa et al. 2004). The Chapada do Araripe is located within a semiarid region and behaves like an island for certain vegetation types, presenting the only preserved cerrado area of Ceara´ (Costa et al. 2004). Even with lower species richness when compared to its core area (Costa et al. 2004), it is among the 27 areas of high biological value (Silva et al. 2004) containing approximately 51% of the native medicinal plants widely used by the traditional communities of the region (Bezerra 2004) for which the majority still do not have studies that prove their therapeutic indications (Ribeiro et al. 2014) which makes it deserving of attention since its exploitation may result in the reduction and/or loss of exclusive species. Considering the importance of the fragmented savannas (disjointed ‘‘cerrado’’), as well as the few studies that directly evaluate the traditional practices on forest resources, it is necessary to carry out research that provides conservation subsidies, through the devel- opment of strategies which prioritize the rational use of this biodiversity. Thus, this study aimed to determine the woody medicinal species with priority for local conservation in a disjoint area of the cerrado in the Chapada do Araripe, northeastern Brazil. D. A. Ribeiro et al. 123 Author's personal copy 2 Materials and methods 2.1 Study area The Chapada do Araripe is located at the border of the states of Ceara´, Piauı´ and Per- nambuco, presenting with a tabular surface, and an altitude ranging from 700 to 1000 m (FUNCEME 2006). The city of Nova Olinda is part of the Environmental Protection Area—Chapada do Araripe, in the south of the state of Ceara´ (IPECE 2011). The climate in the region is defined as Tropical Hot Sub-humid, Warm-Mild Tropical Semiarid, Warm Tropical Semiarid,presenting an average temperature ranging from 24� to 26 �C (IPECE 2011) (Fig. 1). Soils are Litolics, Red-Yellow Latosols, Red-Yellow Podzols, Red Nitosols and Vertisols. The vegetation types found in this region are the Thorny Deciduous Forest, the Tropical Underwater Rainforest, the Tropical Rain Forest Subperfusion and the Xeromorphic Tropical Sub-deciduous Forest (IPECE 2011), with the cerrado the main vegetation cover ([48.53%) presenting as a disjunction of its core area because it is inserted within a semiarid region (Costa et al. 2004; Bezerra 2004). Ethnobotanical research was carried out in two communities known as Sı´tio Serra do Zabeleˆ and Sı´tio Zabeleˆ, with latitudes 7�10042.900 and 07�10001.5400S and longitudes 39�37027.700 and 39�36020.4400W, both located in Nova Olinda, Ceara´, Brazil. The Serra do Zabeleˆ community consists of approximately 60 families. In the locality, the main activity is subsistence agriculture, followed by other practices, for example, the handling and sale of the vegetable ‘‘faveira’’ (Dimorphandra gardneriana Tul.). The second community (Zabeleˆ) presents approximately 50 families, at the margins of the CE-292 highway that cuts the community in half, which apparently brings the greatest influence of the urban areas. Its main activity is in the informal trade of in natura products and medicinal products manufactured by local people through the natural resources available in the area. 2.2 Data collection For the ethnobotanical survey, semi-structured interviews were carried out with 50 informants (men and women responsible for the visited homes), and information on their knowledge was granted after reading, allowing and signing an informed consent form. The interviews were carried out with local experts, residents recognized by the people of the community as knowledgeable on medicinal plants and their use, selected through the snowball technique (Albuquerque et al. 2010). Ethical approval was obtained by the Ethics and Research Committee of the Regional University of Cariri, under legal number 251.677. To evaluate the local availability of medicinal species, an area of apparently preserved cerrado located equidistantly, approximately 3 km, from each community was selected. The species availability was based on the analytical parameters calculated for the vegetal community in the forest fragment. A total of 25 plots with 20 9 20 m dimensions, sys- tematically distributed at intervals of 20 m, were demarcated, totaling one hectare, con- sidering all the individuals that met the inclusion criterion, with soil diameter of C3 cm and height C1 m. The phytosociological parameters (RD—relative density; RDo—relative dominance; RF—relative frequency; IV—importance value) that characterized the area were estimated using the program Fitopac 1.0 (Shepherd 1995). In the selected area, all botanical material that was in the reproductive stage was collected with the help of a resident (interviewed). This material was treated according to conventional herbalism techniques (Mori et al. 1989) and identified through specialized Conservation priorities for medicinal woody species in a… 123 Author's personal copy URBAN AREA CHAPADA DO ARARIPE ARARIPE NATIONAL FOREST LEGEND Atlantic Ocean S 0 900Km SE CO NE N N BRAZIL A t l a n t i c O c e a n PE PB PI RN 37°30 7°307°30 6°30 5°30 4°30 3°30 38°3039°3040°30 CEARÁ STATE Fortaleza 0 25 50 100 km Approximate scale NOVA OLINDA 500m 39°35’W39°40’W FLONA CEARA PERNAMBUCO MANÉ CÔCO SANTAN A DO CAR IRI NOVA OLINDA 39°45’W 7°15’S 7°10’S 7°05’S SANTANA DO CARIRI C R AT O CR AT O 0 5Km2.5 CE-292 Serra do Zabelê Zabelê Fig. 1 Geographical location of the area of study in Zabeleˆ and Serra do Zabeleˆ communitys, Chapada do Araripe, Ceara´, Brazil D. A. Ribeiro et al. 123 Author's personal copy literature, compared with botanical material identified and sent to specialists. The testi- monial material was incorporated into the collection of the Caririense Da´rdano de Andrade-Lima Herbarium of the Regional University of Cariri (HCDAL-URCA). The botanical classification system adopted was based on the Angiosperm Phylogeny Group III (APG III 2009). The species and abbreviations of the authors of the specific binomials were verified in the IPNI (the International Plant Names Index) database and in the Flora List of Brazil 2014. The authorization for the collection of botanical material was provided by the Biodiversity Information and Authorization System (SISBIO) of the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA), registered under number 35157-1. 2.3 Data analysis 2.3.1 Conservation priority for woody medicinal plants The local conservation priority (CP) was used according to the technique proposed by Dzerefos and Witkowski (2001) and adapted by Albuquerque et al. (2011). The phy- tosociological parameters (relative density) and the ethnobotanical data were used in the equations whose criteria and scores used are explained in Table 1. The formula is: CP = 0.5 (BS) ? 0.5 (UR), corresponding to the biological score (BS) calculated based on the relative density (RD) of each species: BS = RD 9 10. The usage risk (UR) score was obtained by the formula: UR = [0.5 (H) ? 0.5 (U)] 9 10. The average of the sum of the local importance (L) and the diversity of use (V) determined the value of use (U), together with the collection risk (H) score which is based on the biological consequences of the collection of the vegetal part removed (Table 1). The value of local importance (L) was determined by the percentage of informants who indicated a particular species as medic- inal, and the diversity of use (V) was based on the number of medicinal uses attributed to a species, with their score varying from 1 to 10 (Table 1). For the woody species that present wood usage (obtained through informal interviews with the local residents), the value of 10 points was added, as an additional usage pressure (Albuquerque et al. 2011). The score allowed to classify medicinal plants into three categories (Dzerefos and Witkowski 2001): category 1: where species with a value[80 require a high priority of conservation with controlled collection, associated with the establishment of alternatives; category 2: where species with a value between 60 and 80 are included, with the potential to be collected according to the area and with specific quotas; category 3: where species with a value of\60 are included, suitable for more intense collection. 3 Results and discussion 3.1 Richness of medicinal species In the ethnobotanical survey, 61 medicinal wood species, belonging to 26 families and 59 genera, were registered (Table 2). Among the species mentioned, some occur in other ecosystems, mainly in the ‘‘caatinga’’ (semiarid region restricted to northeastern Brazil), and the presence of these species in therapeutic indications is probably influenced by the proximity of the local community to this environment. The most representative botanical families were Fabaceae (17 spp.), Myrtaceae (5 spp.), Anacardiaceae, Apocynaceae and Conservation priorities for medicinal woody species in a… 123 Author's personal copy Euphorbiaceae (4 spp. each). Fabaceae (including the subfamily Faboideae, Caesalpin- ioideae and Mimosoideae) is among the most expressive families referenced in ethnob- otanical studies carried out in cerrado areas (Cunha and Bortolotto 2011; Guarim Neto and Morais 2003; Lima et al. 2012; Moreira and Guarim Neto 2009; Oliveira et al. 2010). Most of the woody medicinal species of this study are reported in the work of Ribeiroet al. (2014), for a variety of therapeutic uses, suggesting that they are extremely important for medicinal use and have great potential for bioactive compounds. Among the woody species, 68.8% had an arboreal habit while shrubs and lianas added up to 31.2%. In other cerrado areas, the arboreal species also prevail, indicating a domi- nance between medicinal plants (Botrel et al. 2006; Guarim Neto and Morais 2003; Tunholi et al. 2013). In the semiarid, the woody species represent a greater percentage of uses and indications, showing that the native trees are those of greater local medicinal importance (Albuquerque and Oliveira 2007; Albuquerque et al. 2007; Almeida et al. 2005). Of the plant parts used, bark and inner stem bark from the stem were the most cited representing 46.6% of the species, followed by leaves with 18.3%, fruits with 14.1% and roots with 10%. Flower, seed, root-tuber, resin and latex accounted for 10.8% of the citations. The use of bark and inner stem bark from the stem may be associated with the Table 1 Criteria and scores used to determine medicinal species with conservation priority from the ethnobotanical and phytosociological survey carried out in the Chapada do Araripe, northeastern Brazil. Source: Albuquerque et al. (2011), modified of Dzerefos and Witkowski (2001) Criteria Score A. Relative density in the fragment (RD) Non registered—very low (0–1) 10 Low (1\ 3.5) 7 Medium (3.5\ 7) 4 High (C7) 1 B. Risk of collection (H) Destructive plant collection, or over-exploitation of roots or bark. The collection represents the removal of the individual 10 Collection damages the perennial structures such as bark and roots, and removal of part of the stem for extraction of latex and resin. Collections without causing the death of the individual 7 Collection that permanently damages aerial structures such as leaves, which are removed. Collection that can affect the energy investment of plants, survival and long-term reproductive success 4 Collection that damages the transient overhead structures of the plant, such as flowers and fruits, which are removed. Regeneration of the population can be altered in the long term by collections from the seed bank, but the individual is not affected 1 C. Local use (L) High (species cited by[75% of local informants) 10 Moderately high (50–75% of local informants) 7 Moderately low (cited by 25–50% of local informants) 4 Muito baixo (cited by\25% of local informants) 1 D. Diversity of use (V) For each type of medicinal use, 1 point is added, for a maximum of 10 points 1–10 D. A. Ribeiro et al. 123 Author's personal copy Table 2 List of woody medicinal species registered in the ethnobotanical survey in two communities located in the Chapada do Araripe, northeastern Brazil Family/scientific name Vernacular name Habit Part used HN Anacardiaceae Anacardium occidentale L. Caju´ Tr Sb, Si, Fr 9250 Astronium fraxinifolium Schott Gonc¸alo-alves Tr Sb, Si, Le 9256 Myracrodruon urundeuva Allema˜o Aroeira Tr Sb, Si, Le 8908 Spondias lutea L. Cajazeira Tr Sb nc Annonaceae Annona coriacea Mart. Araticum Sh Sb, Si, Le 9261 Apocynaceae Himatanthus drasticus (Mart.) Plumel Janaguba Tr Sb, Le, La 9253 Hancornia speciosa Gomes. Mangaba Tr La, Sb, Fr, Le 9254 Rauvolfia sp. Quina-Quina Tr Sb, Si, Le nc Secondatia floribunda A.DC. Catuaba-de-rama Cp Le, Sb 9259 Boraginaceae Cordia rufescens A. DC. Uva-braba Sh Fr 9260 Bignoniaceae Tabebuia impetiginosa (Mart. ex DC.) Standl. Pau d’arco roxo Tr Sb nc Cactaceae Cereus jamacaru DC. Mandacaru´ Tr Sb nc Caryocaraceae Caryocar coriaceum Wittn. Pequi Tr Fr, Fl, Sb 9245 Celastraceae Maytenus sp. Engorda-bode Tr Fr 9290 Erythroxylaceae Erythroxylum vacciniifolium Mart. Catuaba Tr Sb, Le nc Euphorbiaceae Croton sp. Marmeleiro Tr Sb 9283 Croton zehntneri Pax & K.Hoffm. Velame-Branco Sh Ro, Le 9286 Jatropha molissima (Pohl) Baill. Pinha˜o-branco Sh Se, La nc Manihot sp. Manic¸oba Tr Ro, Fr 10,561 Fabaceae Amburana cearensis (Allema˜o) A.C.Sm. Imburana-de- cheiro Tr Sb nc Anadenanthera colubrina var. cebil (Griseb.) Altschul Angico Tr Sb, Si nc Bauhinia cheilantha (Bong.) Steud. Mororo´ Tr Le 9266 Bowdichia virgilioides Kunth Sucupira Tr Sb, Fr, Se 9268 Caesalpinia pyramidalis Tul. Catingueira Tr Fl 10,559 Centrosema sp. Alcanc¸u Sh Ro nc Copaifera langsdorffii Desf. Pau d’o´leo Tr Sb, Le, Ro 9833 Dimorphandra garderiana Tull. Faveira Tr Fr 10,564 Dioclea grandiflora Mart. ex. Benth. Mucuna˜ Cp Sb, Se 9257 Enterolobium contortisiliquum (Vell.) Morong Tamboril Tr Sb, Ro 9277 Conservation priorities for medicinal woody species in a… 123 Author's personal copy Table 2 continued Family/scientific name Vernacular name Habit Part used HN Hymenaea courbaril L. Jatoba´ Tr Sb, Si, Fr, Ro 9837 Leptolobium dasycarpum Vogel Pau-pra-tudo Sh Sb nc Libidibia ferrea (Mart. ex Tul.) L.P.Queiroz Pau-ferro Tr Sb, Se, Fr 9273 Lonchocarpus araripensis Benth. Angelim Tr Fr 9244 Machaerium acutifolium Vogel Corac¸a˜o-de-negro Tr Rt, Si 4368 Mimosa tenuiflora (Willd.) Poir. Jurema-preta Tr Sb, Si 9251 Stryphnodendron rotundifolium Mart. Barbatima˜o Tr Sb 9263 Lamiaceae Hyptidendron amethystoides (Benth.) Harley Tipi Sh Sb, Ro nc Lythraceae Lafoensia glyptocarpa Koehne Roma˜-braba Sh Fr 9247 Malpighiaceae Byrsonima sericea DC. Murici Tr Sb, Si, Le 9291 Malvaceae Ceiba glaziovii (Kuntze) K.Schum. Barriguda Tr Sb nc Guazuma ulmifolia Lam. Cabec¸a de negro Tr Si, Rt nc Myrtaceae Myrcia sp. Chumbinho Sh Sb, Fr nc Paramyrciaria cf. strigipes (O.Berg.) Sobral Cambuı´ Sh Sb, Fr 9246 Psidium myrsinites DC. Arac¸a´/Goiabinha Sh Le, Sb, Fr 9279 Psidium polianum sp. Arac¸a´ de veado Sh Le 10,558 Syzygium cumini (L.) Skeels Oliveira Tr Le, Fr 9835 Olacaceae Ximenia americana L. Ameixa Tr Sb nc Polygalaceae Bredemeyera floribunda Willd. Pau-gemada Cp Sb, Ro nc Bredemeyera brevifolia (Benth.) Klotzsch ex A.W.Benn. Mau-vizinho Tr Sb 9834 Proteaceae Roupala montana Aubl. Congonha Tr Le 9267 Rhamnaceae Colubrina cordifolia Reissek Joa˜o-vermelho Sh Le nc Ziziphus joazeiro Mart. Juazeiro Tr Sb, Si, Le 9836 Rubiaceae Coutarea haxandra (Jacq.) K. Schum Quina-quina roxa Tr Sb 9289 Guettarda viburnoides Cham. & Schltdl. Ange´lica Tr Le, Sb, Ro 9287 Tocoyena formosa (Cham. & Schlecht.) Schum. Jenipapo-brabo Tr Le, Sb, Si 9274 Rutaceae Zanthoxylum gardneri Engl. Quebra-faca Tr Sb, Si nc Sapotaceae Sideroxylon obtusifolium (Roem. & Schult.) T.D.Penn. Quixaba Tr Sb, Si nc D. A. Ribeiro et al. 123 Author's personal copy arboreal habitat, a situation frequently observed in Caatinga environments (Albuquerque and Oliveira 2007; Ju´nior et al. 2011). Bezerra (2004) states that in the Chapada do Araripe, the bark from medicinal species within the arboreal habitat is one of the most exploited resources. This practice can be justified because the cerrado studied is inserted in the semiarid climate and close to an environment with a predominant vegetation from the Caatinga, which may have influenced, in a cultural way, the local communities installed in the Chapada do Araripe through the transmission of knowledge. 3.2 Availability of species Of the 61 species used medicinally in both communities, 29 (47.5%) are available in the sampled forest fragment (Table 3). These species were distributed in 18 families and 60 genera. Fabaceae was the most representative (8 spp.), followed by Apocynaceae, Euphorbiaceae, Myrtaceae and Rubiaceae (2 spp. each). Among families, Fabaceae has been the most diversified in most of the studies conducted in cerrado areas (Assunc¸a˜o and Felfili 2004; Couto et al. 2009; Felfili et al. 2002; Gia´como et al.2013; Medeiros and Walter 2012). This high diversity combined with availability may influence and/or justify the high demand of this family for medicinal use. Lochocarpus araripensis, Ximenia americana, Byrsonima sericea and Copaifera langsdorffii were the most abundant species, with Lochocarpus araripensis being restricted to the northeast region, not occurring in nuclear areas of cerrado (Bridgewater et al. 2004). On the other hand, Copaifera langsdorffii is in the group of woody species of wide geographic distribution that dominate in the diverse physiognomies (Durigan et al. 2003; Ratter et al. 2003; Solo´rzano et al. 2012). The Ximenia americana presence among those with the highest number of individuals reinforces the existence of an interchange of cer- rado species with the Caatinga vegetation, a situation also observed in other areas by Ratter et al. (2006). Of the available species, 16 presented less than ten individuals in the sampled area; among them were Anacardium ocidentale, Annona coriacea, Himatanthus drasticus, Caryocar coriaceum, Croton zehntneri, Dimorphandra gardneriana, which occupy a prominent position for medicinal use in the communities studied, receiving large numbers of citations by local residents. Albuquerque et al. (2007) point out that the proximity of the sample area to the community apparently does not affect species richness, but may directly affect local abundance. Table 2 continued Family/scientific name Vernacular name Habit Part used HN Solanaceae Solanum sp. Sacatinga Sh Ro 9284 Solanum paniculatum L. Jurubeba Sh Ro, Fr 9275 Urticaceae Cecropia pachystachya Tre´cul Tore´ Tr Le, Sb nc Verbenaceae Lantana camara L. Camara´ Sh Le 9269 Tr tree, Sh shrubby, Cp climbing plants, Le leaf, Fl flower, Fr fruit, Se seed, Ro root, Rt root-tuber, Sb stem bark, Si stem inner bark, La latex, Re resin, HN herbarium number, nc number of collection in process by herbaria Conservation priorities for medicinal woody species in a… 123 Author's personal copy Table 3 List of woody medicinal species available in the forest fragment in a cerrado area of the Chapada do Araripe, northeastern Brazil Family/scientific name NI RD (%) RDo (%) RF (%) IV Anacardiaceae Anacardium ocidentale L. 2 0.09 0.16 0.24 0.49 Annonaceae Annona coriacea Mart. 7 0.32 0.05 0.96 1.33 Apocynaceae Himatanthus drasticus (Mart.) Plumel 10 0.45 0.22 0.72 1.39 Rauvolfia sp. 3 0.14 0.03 0.48 0.65 Boraginaceae Cordia rufescens A. DC. 47 2.12 0.75 3.61 6.47 Cariocaraceae Caryocar coriaceum Wittm. 1 0.05 0.21 0.24 0.50 Erythroxylaceae Erythroxylum vacciniifolium Mart. 23 1.04 0.60 1.20 2.84 Euphorbiaceae Croton zehntneri Pax & K. Hoffm. 5 0.23 0.28 0.48 0.98 Manihot sp. 1 0.05 0.06 0.24 0.35 Fabaceae Bauhinia cheilantha (Bong.) Steud. 4 0.18 0.06 0.72 0.96 Bowdichia virgilioides Kunth 49 2.21 4.66 4.09 10.9 Copaifera lansdorfii Desf. 77 3.47 2.83 2.64 8.94 Dimorphandra gardneriana Tull. 8 0.36 0.18 0.96 1.50 Dioclea grandiflora Mart. ex. Benth. 3 0.14 0.14 0.72 1.00 Hymenaea courbaril L. 17 0.77 2.49 1.20 4.46 Lochocarpus araripensis Benth. 452 20.37 5.78 5.29 31.4 Machaerium acutifolium Vogel 26 1.17 1.36 2.88 5.42 Laminaceae Hyptidendron amethystoides (Benth.) Harley 2 0.09 0.05 0.48 0.62 Malpighiaceae Byrsonima sericea DC. 128 5.77 3.89 4.81 14.4 Myrtaceae Myrcia sp. 26 1.17 1.36 2.88 5.42 Psidium myrsinites DC. 9 0.41 0.31 1.20 1.92 Olacaceae Ximenia americana L. 179 8.07 2.21 5.05 15.3 Polygalaceae Bredemeyera brevifolia (Benth.) Klotzsch ex. W.Benn. 4 0.18 0.08 0.48 0.74 Rubiaceae Guettarda viburnoides Cham. & Schltdl. 1 0.05 0.01 0.24 0.30 Tocoyena formosa (Cham. & Schlecht.) Schum. 45 2.03 1.52 2.64 6.20 Rutaceae Zanthoxylum gardneri Engl. 9 0.41 0.08 0.96 1.45 D. A. Ribeiro et al. 123 Author's personal copy The species with the highest importance values (IV) were Lochocarpus araripensis, Ximenia americana, Byrsonima sericea, Bowdichia virgilioides and Copaifera langsdorffii, also presenting the highest density values, dominance and relative frequency. In cerrado marginals, L. araripensis presented with one of the lowest IV and B. virgilioides is among the main species with a wide distribution occurring in more than 75% of Brazil cerrado areas as analyzed by Ratter et al. (2003). Of the medicinal species not available in the sampled area (32), some such as Han- cornia speciosa, Secondatia floribunda, Roupala montana, Ziziphus joazeiro and Stryphnodendron rotundifolium were observed in previous studies in the Chapada do Araripe (Costa et al. 2004; Costa and Arau´jo 2007; Ribeiro-Silva et al. 2012). Although these species have not been recorded as available, their relation to the local community is pertinent, since not all plants are used according to their availability (Torre-Cuadros and Islebe 2003), and are often acquired from third parties. On the other hand, the most abundant species that do not present medicinal use are more likely to be used in other ways, such as lumber. Thus, it is possible that even these abundant resources may decline over time, with consequences unknown to local vegetable communities (Albuquerque et al. 2009; Baldauf and Santos 2013; Lucena et al. 2007). 3.3 Woody medicinal species with conservation priority For the 29 medicinal species available in the forest fragment sampled, the local conser- vation priority score was applied (Table 4). Of the total number of species, 17.2% have their uses linked to non-perennial structures (leaves and fruits) and the others (82.7%) have the use of bark and inner stem bark associated with other plant parts (leaves, flowers, fruits, roots, tubercle root, resin and latex), covering structures (inner stem bark, resin, latex and roots) considered the ones that bring greater damage to the plant when unduly extracted. The collection intense and continuous of these plant structures can affect the resilience of the species, so that it does not allow populations and ecosystem to recover, causing reductions in the density and species richness favoring species adapted to disturbances (Baldauf and Santos 2014; Feitosa et al. 2014; Ribeiro et al. 2015; Souza et al. 2017), when it is not eliminated from the environment (Albuquerque et al. 2011; Ju´nior et al. 2011; Monteiro et al. 2006; Oliveira et al. 2007). Thirteen species were included in category 1, indicating that they need more attention regarding the applicability of conservation measures. In this category, five species stand out, Himatanthus drasticus, Caryocar coriaceum, Ximenia americana, Croton zehntneri and Hymenaea courbaril which require special attention, especially due to the high number Table 3 continued Family/scientific name NI RD (%) RDo (%) RF (%) IV Sapotaceae Sideroxylon obtusifolium (Roem. & Schult.) T.D.Penn. 35 1.58 1.74 2.64 5.96 Solanaceae Solanum paniculatum L. 10 0.45 0.32 0.96 1.73 Verbenaceae Lantana camara L. 2 0.09 2.55 0.48 3.12 NI number of individuals, RD relative density, RDo relative dominance, RF relative frequency, IV impor- tance value Conservation priorities for medicinal woody species in a… 123 Author's personal copy of therapeutic indications, as they are generally harvested in a destructive way and because they have low local availability, with the exception of X. americana, which showed a great number of individuals, even though their perennial structures were extensively explored. Likewise, C. zehntneri is in this category mainly due to the collection risk (10), as the extraction of its roots often results in the removal and death of the individual. Himatanthus drasticus presented the highest conservation priority values, being cited by approximately 80% of theinterviewees. This species is characterized by its latex, which has prohibited collection, resulting in a growing illegal market (Baldauf and Santos 2013), perhaps because of their proven pharmacological activities (Mousinho et al. 2011; Souza Table 4 List of species indicated for local conservation priority in the disjoint cerrado vegetation in the Chapada do Araripe, northeastern Brazil Species Number of citations BS H L V U UR CP CATG Anacardium occidentalea 24 100 7 4 6 5 60 90 1 Caryocar coriaceuma 33 100 7 7 10 8.5 77.5 98.75 1 Croton zehntneri 22 100 10 4 4 4 70 85 1 Guettarda viburnoidesa 10 100 7 1 5 3 52.5 86.25 1 Himatanthus drasticusa 44 100 7 10 8 9 157.5 138.75 1 Hymenaea courbarila 19 100 7 4 6 7 70 95 1 Hyptidendron amethystoidesa 6 100 7 1 4 2.5 47.5 83.75 1 Manihot sp. 13 100 10 4 2 3 65 82.5 1 Myrcia sp. 5 70 7 1 3 2 65 87.5 1 Rauvolfia sp.a 12 100 7 1 9 5 60 90 1 Sideroxylon obtusifoliuma 17 70 7 4 6 5 87.5 88.75 1 Ximenia americanaa 22 100 7 4 10 7 70 85 1 Zanthoxylum gardneria 5 100 7 1 6 3.5 52.5 86.25 1 Annona coriacea 22 100 7 4 1 2.5 47.5 73.75 2 Bauhinia cheilanthaa 12 100 4 4 4 4 40 80 2 Bowdichia virgilioidesa 10 70 7 1 7 4 55 72.5 2 Bredemeyera brevifolia 2 100 7 1 2 1.5 42.5 71.25 2 Byrsonima sericeaa 13 40 7 4 6 5 87.5 73.75 2 Copaifera langstorffiia 21 40 7 4 10 7 70 65 2 Dimorphandra garderianaa 18 100 1 4 8 6 35 77.5 2 Dioclea grandiflora 4 100 7 1 3 2 45 72.5 2 Erythroxylum vacciniifoliuma 15 70 7 4 2 3 50 70 2 Lantana camara 2 100 4 1 1 1 25 62.5 2 Machaerium acutifoliuma 2 70 7 1 3 2 45 67.5 2 Psidium myrsinites 14 100 7 4 2 3 52.5 76.25 2 Solanum paniculatum 5 100 10 1 4 2.5 47.5 73.75 2 Tocoyena formosa 27 70 7 7 5 6 65 67.5 2 Cordia rufescens 1 70 1 1 1 1 10 40 3 Lochocarpus araripensisa 1 10 1 1 1 1 10 20 3 BS biological scores, H collection risk, L local use (%), LI local importance, V diversity of use, U value of use, UR usage risk, CP conservation priority, CATG categories, category 1 a value[80, category 2 values between 60 and 80, category 3 a value\60 aLumber use D. A. Ribeiro et al. 123 Author's personal copy et al. 2010). Caryocar coriaceum presented low density and frequency values in the area, probably due to the high diversity of use. This species has significant cultural and eco- nomic importance in the region, being used for different purposes; among them, the extraction of fruits stands out (Sousa et al. 2013), which can compromise the conservation state of the species and limit the emergence of new individuals. Additionally, C. coriaceum is included in the list of endangered species of the International Union for the Conservation of Nature and Natural Resources (IUCN 2013), classified in the ‘‘Endangered’’ extinction category. Hymenaea courbaril is also one of the species that is at risk in the list of endangered species of the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA 1992), and its exploitation mainly occurs for wood and medicinal use. Among the species that make up category 1, some are best known in the Chapada do Araripe region, because of not only its medicinal but also economic importance, being a source of income for most of the local communities (Bezerra 2004), which as a conse- quence are the ones that suffer most usage pressure. In category 2, 14 species were registered, most of which are widely used both for medicinal purposes and for logging. Copaifera langsdorffii and Dimorphandra gardneri- ana presented a high diversity of use and a moderately low local importance, being mentioned by 25 and 50% of the local informants, but their values diverge in relation to their collection risk (H = 7 and 1) and local availability, with a relative density of 3.47 and 0.36, respectively. The D. gardneriana low values can be related to the exploitation of the fruit, vegetal part that does not affect the individual, but that can infringe on the regen- eration in the long term. The species is widely exploited to trade throughout the region, mainly to supply the pharmaceutical industry that extracts from its vegetable the rutin (Gomes and Gomes 2000). This high potential of use can lead to a decrease in the natural populations of this species, which already calls attention to its conservation in some studies (Landim and Costa 2012; Ribeiro-Silva et al. 2012). Most species present in category 2 are at a moderately high collection risk; among them, Copaifera langsdorffii, Erythroxylum vacciniifolium and Solanum paniculatum have their perennial parts and products (bark, resin, roots) used. The excessive and recurrent col- lection of C. langsdorffii and E. vacciniifolium for folk medicine and logging, intended for personal consumption and/or commercial purposes, may in the future compromise the regeneration of these species in the natural environment and decrease their populations (Lucena et al. 2007). Category 3 included only two species, Lochocarpus araripensis and Cordia rufescens. The inclusion of these species in the category indicates their high availability in the area and the great influence of the relative density on conservation priority indices. This situ- ation was also observed by Albuquerque et al. (2011) who emphasize that some species applied to the priority can be valued because of their local availability. Lochocarpus araripensis, although presenting a significant number of individuals and having little importance for both communities in relation to medicinal use (LI = 1), is among the most exploited species for wood purposes, which may compromise their availability in the future. Cordia rufescens probably applied to this category because it presented low local importance and only had one vegetal part linked to its use. According to Bezerra (2004), the most explored species in the Chapada do Araripe are Himatanthus drasticus, Caryocar coriaceum and Dimorphandra gardneriana. This state- ment corroborates with the results obtained, where the three species are among the most used by the community as medicinal of commercial value; thus, the pressures suffered by these species can increase their vulnerability. Other factors that may influence are those that contribute to the distribution of the species and which regulate population size, such as Conservation priorities for medicinal woody species in a… 123 Author's personal copy genetic variation. The gradual loss of genetic variability for all species of the biome is first damage occurs due to the pressure to establish productive activities the in communities local, which may result in disappearance of species under intense use (Baldauf and Santos 2014; Marinho et al. 2016; Souza et al. 2017). Moreover, among species related to con- servation priority C. coriaceum, Copaifera langsdorffii, D. garderiana, H. drasticus and Ximenia americana stand out in most of the ethnobotanical studies in the Chapada do Araripe region among species with greater versatility, due to the high number of thera- peutic properties attributed (Macedo et al. 2015; Ribeiro et al. 2014; Saraiva et al. 2015; Souza et al. 2014). Albuquerque et al. (2009) point out that the intensive use of the available resources can be directed toward a small population of plants better known and sought for reasons that depend on local cultural characteristics. Therefore, the species present in the two categories that deserve more attention in relation to the applicability of sustainable practices are directly considered conservation priorities. In addition, they need local strategies that balance human activities with local biodiversity, allowing the community to continue to enjoy the resources offered, but in a manner that ensures the resilience of plant populations stillavailable in the area (Andel et al. 2015; Albuquerque and Lucena 2005; Albuquerque et al. 2009; Chia et al. 2017; Ju´nior et al. 2011). 4 Conclusion The flora from the Chapada do Araripe has an important role in supplying woody medicinal plants to local populations. Of the vegetable species registered as medicinal, less than half are available in the forest fragment. Among the species that require controlled collection, associated with the establishment of alternatives considering those collected according to the site and with specific quotas, some are the most important in economic terms for the two communities and deserve great attention, as it has mainly its perennial structures compromised. 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Availability and use of woody plants in an agrarian reform settlement in the cerrado of the state of Goia´s, Brazil. Acta Botanica Brasilica, 27, 604–612. Conservation priorities for medicinal woody species in a… 123 Author's personal copy Conservation priorities for medicinal woody species in a cerrado area in the Chapada do Araripe, northeastern Brazil Abstract Introduction Materials and methods Study area Data collection Data analysis Conservation priority for woody medicinal plants Results and discussion Richness of medicinal species Availability of species Woody medicinal species with conservation priority Conclusion Acknowledgements References
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