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Priority conservation of medicinal woody plants from protected forests based on ecological and ethnobotanical data

Abstract

The combination of ethnobotanical and ecological knowledge is an important tool in indicating priority species for conservation. We sought to gather ethnobotanical knowledge on the diversity and use of woody medicinal plants in the Chapada Araripe region, assessing the real availability of woody medicinal resources in the Araripe Forests in the cerrado and carrasco areas, and indicate priority species for conservation. A total of 107 species were recorded in the ethnobotanical surveys, classified into 39 families and 83 genera, of which 92 species, 36 families and 70 genera for the cerrado areas, and 47 species, 25 families and 39 genera, for the carrasco areas. 59% were present in the phytosociological surveys for cerrado and 38% for carrascos. Species with high versatility of medicinal use did not necessarily have high local availability, and some were not recorded in the sampling. Thirteen species in cerrados and four in carrascos were indicated as conservation priorities. Use not aligned of species with the reality of the present time can indeed affect the vegetation landscape, and in a future scenario, not taking local measures to conserve protected forest resources, besides increasing the lists of local conservation priorities, can affect economic practices, increasing social and environmental conflicts.

Key words
Savanna; Carrasco; resource availability; conservation problems

INTRODUCTION

The conservation of biological diversity is a global challenge (Forzza et al. 2012FORZZA RC ET AL. 2012. New Brazilian Floristic List Highlights Conservation Challenges. Bioscience 62: 39-45. https://doi.org/10.1525/bio.2012.62.1.8., Ulloa-Ulloa et al. 2017ULLOA-ULLOA C ET AL. 2017. An integrated assessment of the vascular plant species of the Americas. Science 358 (6370): 1614-1617. https://doi.org/10.1126/science.aao0398., Archibald et al. 2020ARCHIBALD CL, BARNES MD, TULLOCH AIT, FITZSIMONS JA, MORRISON TH, MILLS M & RHODES JR. 2020. Differences among protected area governance types matter for conserving vegetation communities at-risk of loss and fragmentation. Biol Conserv 247: 108533. https://doi.org/10.1016/j.biocon.2020.108533.), especially in large countries with high physical and climatic heterogeneity, which are reflected in their different ecosystem types and biological diversity (Van-Wyk & Prinsloo 2018VAN-WYK AS & PRINSLOO G. 2018. Medicinal plant harvesting, sustainability and cultivation in South Africa. Biol Conserv 227: 335-342. https://doi.org/10.1016/j.biocon.2018.09.018., Schultz et al. 2020SCHULTZ F, ANYWAR G, WACK B, QUAVE C L & GARBE LA. 2020. Ethnobotanical study of selected medicinal plants traditionally used in the rural Greater Mpigi region of Uganda. J Ethnopharmacol 256: 112742. https://doi.org/10.1016/j.jep.2020.112742.).

One of the strategies adopted for the conservation of biological diversity has been the establishment of protected areas or conservation units - Ucs (Dias & Hoft 2013DIAS BS & HOFT R. 2013. Challenges facing implementation of the Global Strategy for Plant Conservation in Brazil. In: Martinelli G & Moraes MA (Eds), Red Book of Brazilian Flora. Centro Nacional de Conservação da Flora, Rio de Janeiro, p. 26-39.). However, these areas of protection do not necessarily prevent local people from making use of their resources (Andrade et al. 2015ANDRADE WM, RAMOS MA, SOUTO WMS, BENTO-SILVA JS, ALBUQUERQUE UP & LIMA EA. 2015. Knowledge, Uses and Practices of the Licuri Palm (Syagrus coronata (Mart.) Becc.) around Protected Areas in Northeastern Brazil Holding the Endangered Species Lear’s Macaw (Anodorhynchus leari). Trop Conserv Sci 8: 893-911. https://doi.org/10.1177/194008291500800403., Mammides 2020MAMMIDES C. 2020. Evidence from eleven countries in four continents suggests that protected areas are not associated with higher poverty rates. Biol Conserv 241: 108353. https://doi.org/10.1016/j.biocon.2019.108353.), as is the case near the Chapada do Araripe in Brazil (Zank & Hanazaki 2017ZANK S & HANAZAKI N. 2017. The coexistence of traditional medicine and biomedicine: A study with local health experts in two Brazilian regions. PLoS One 12(4): e0174731. https://doi.org/10.1371/journal.pone.0174731., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.).

The relationship between people and resources provides them with knowledge about the location, size, and availability of the exploited resource. This knowledge has been made available in ethnobotanical studies, and if added to the actual biological data of the availability of the resource in the forests and the socio-economic information of the populations, it enables actions for the development of management plans that consider the local conservation priorities (Albuquerque & Andrade 2002ALBUQUERQUE UP & ANDRADE LHC. 2002. Traditional botanical knowledge and conservation in a caatinga area in the State of Pernambuco (Northeast of Brazil). Acta Botanica Brasilica 16(3): 273-285., Kristensen & Braslev 2003KRISTENSEN M & BRALSLEV H. 2003. Perceptions, use and availability of woody plants among the Gourounsi in Burkina Faso. Biodivers Conserv 12: 1715-1739. https://doi.org/10.1023/A:1023614816878., Andrade et al. 2015ANDRADE WM, RAMOS MA, SOUTO WMS, BENTO-SILVA JS, ALBUQUERQUE UP & LIMA EA. 2015. Knowledge, Uses and Practices of the Licuri Palm (Syagrus coronata (Mart.) Becc.) around Protected Areas in Northeastern Brazil Holding the Endangered Species Lear’s Macaw (Anodorhynchus leari). Trop Conserv Sci 8: 893-911. https://doi.org/10.1177/194008291500800403.). The conservationist approach that considers local ecological knowledge brings the idea of a biocultural conservation scenario, which favors management actions that minimize socio-environmental conflicts in the regions (Monteiro et al. 2006MONTEIRO JM, ALBUQUERQUE UP, LINS NETO EMF, ARAÚJO EL & AMORIM ELC. 2006. Use patterns and knowledge of medicinal species among two rural communities in Brazil’s semi-arid northeastern region. J Ethnopharmacol 105: 173-186., Albuquerque et al. 2009ALBUQUERQUE UP, ARAÚJO TAS, RAMOS MA, NASCIMENTO V, LUCENA RFP, MONTEIRO JM, ALAENCAR N & ARAÚJO EL. 2009. How ethnobotany can aid biodiversity conservation: Reflections on investigations in the semi-arid region of NE Brazil. Biodivers Conserv 18: 127-150. https://doi.org/10.1007/s10531-008-9463-8., 2011, Lucena et al. 2013LUCENA RFP, LUCENA CM, ARAÚJO EL, ALVES AGC & ALBUQUERQUE UP. 2013. Conservation priorities of useful plants from different techniques of collection and analysis of ethnobotanical data. An Acad Bras Cienc 85: 169-186. https://doi.org/10.1590/S0001-37652013005000013., Campos et al. 2018CAMPOS JLA, ARAÚJO EL, GAOUE OG & ALBUQUERQUE UP. 2018. How can local representations of changes of the availability in natural resources assist in targeting conservation? Sci Total Environ 628-629: 642-649. https://doi.org/10.1016/j.scitotenv.2018.02.064., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.).

Among the uses of phytodiversity, the medicinal one has particular importance, especially for low-income populations, for the treatment of different diseases. The collection of bark, fruits and leaves of medicinal plants generates consequences for plant populations and may reduce the reproduction rate of some species (Baldauf & Santos 2013BALDAUF C & SANTOS FAM. 2013. Ethnobotany, Traditional Knowledge, and Diachronic Changes in Non-Timber Forest Products Management: A Case Study of Himatanthus drasticus (Apocynaceae) in the Brazilian Savanna. Econ Bot 67: 110-120. https://doi.org/10.1007/s12231-013-9228-5., 2014BALDAUF C & SANTOS FAM. 2014. The effect of management systems and ecosystem types on regeneration of Himatanthus drasticus (Apocynaceae) bark: recommendations for sustainable harvesting. Environ Monit Assess 186: 349-359. https://doi.org/10.1007/s10661-013-3378-x., Baldauf et al. 2014BALDAUF C, SILVA AS, SFAIR JC, FERREIRA R & SANTOS FAM. 2014. Harvesting increases reproductive activity in Himatanthus drasticus (Mart.) Plumel (Apocynaceae), a non-timber forest product of the Brazilian Savanna. Biotropica 46(3): 341-349., Gaoue et al. 2016GAOUE OG, JIANG J, DING W, AGUSTO FB & LANHART S. 2016. Optimal harvesting strategies for timber and non-timber forest products in tropical ecosystems. Theor Ecol 9: 287-297. https://doi.org/10.1007/s12080-015-0286-4.).

The medicinal use of plants in forests associated or not with the use of pharmaceutical drugs is old and frequent in several regions of the world (Monteiro et al. 2011MONTEIRO JM, RAMOS MA, ARAÚJO EDL, AMORIM ELC & ALBUQUERQUE UP. 2011. Dynamics of medicinal plants knowledge and commerce in an urban ecosystem (Pernambuco, Northeast Brazil). Environ Monit Assess 178: 179-202. https://doi.org/10.1007/s10661-010-1681., Petrovska 2012PETROVSKA BB. 2012. Historical review of medicinal plants’ usage. Pharmacogn Rev 6: 1-5. https://doi.org/10.4103/0973-7847.95849., Maldonado et al. 2013MALDONADO B, CABALLERO J, DELGADO-SALINAS A & LIRA R. 2013. Relationship between Use Value and Ecological Importance of Floristic Resources of Seasonally Dry Tropical Forest in the Balsas River Basin, México. Econ Bot 67: 17-29. https://doi.org/10.1007/s12231-013-9222-y., Zank & Hanazaki 2017ZANK S & HANAZAKI N. 2017. The coexistence of traditional medicine and biomedicine: A study with local health experts in two Brazilian regions. PLoS One 12(4): e0174731. https://doi.org/10.1371/journal.pone.0174731., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084., Cámara-Leret & Dennehy 2019CÁMARA-LERET R & DENNEHY Z. 2019. Indigenous Knowledge of New Guinea’s Useful Plants: A Review1. Econ Bot 73: 405-415., Paredes et al. 2020PAREDES R, HOPKINS AL & VILLANUEVA F. 2020. Ethnobotany in the North Coast of Peru: Use of Plants in the Fishing Community of Huanchaco for Subsistence. Econ Bot 74: 32-45. https://doi.org/10.1007/s12231-020-09486-0.). However, the collection of medicinal resources often generates local conservation problems, depending on the intensity of use, the size of the population and the part of the plant used. The solution to such a problem can be complex, especially in forests with great biological diversity and requires knowledge about the real availability of the flora species to define conservation priorities. Moreover, according to the availability hypothesis (Albuquerque et al. 2019ALBUQUERQUE UP, MEDEIROS PM, JÚNIOR WSF, SILVA TC, SILVA RRV & GONÇALVES-SOUZA T. 2019. Social-ecological theory of maximization: basic concepts and two initial models. Biol Theory 14(2): 73-85.), the local importance of a resource depends on its abundance, which can be influenced by different factors, and collectors adopt strategies that optimize the energy and time spent to obtain the resource.

Admitting that the definition of priority plants for conservation should be based on ecological, pharmacological, commercial aspects, and knowledge that people have about the resource used (Bisht et al. 2006BISHT AK, BHATT A, RAWAL RS & DRAR U. 2006. Prioritization and Conservation of Himalayan Medicinal Plants: Angelica glauca Edgew. as a case study. Ethnobot Res Appl 4: 011-024., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.), we aim in this study: 1. Gather ethnobotanical knowledge about the diversity of woody medicinal plants in the Chapada do Araripe region and their uses, 2. Evaluate the actual availability of woody medicinal resources in the Araripe FLONA, and 3. Indicate priority species for conservation.

Thus, we tried to answer the following questions: 1. Which species have the greatest versatilidade of therapeutic use? 2. Are species of high versatility of medicinal use species of high abundance in the forest patch? 3. which parts of the plants are most used? 4. Which species need priority actions for conservation?

MATERIALS AND METHODS

Field of study

The survey was conducted using secondary and primary data obtained in the region of the Chapada do Araripe. The studied communities are located in the states of Ceará and Pernambuco, within the Environmental Protection Area - APA Araripe (9400 km²), and the FLONA- Araripe (380 km²) (Figure 1). The Chapada do Araripe is inserted in the equatorial tropical climate zone - Equatorial hot type zone. Most of the Chapada region has a “semi-arid, tropical or subtropical” climate with an average temperature of 21-28°C and humidity of 60-70%. However, in the center of it, a small area is classified as “Sub-humid, tropical or subtropical” with average temperatures of 20-27°C and humidity 70-80% and another small area is classified as “Sub-humid dry, tropical or subtropical” with average temperatures of 20-27°C and humidity 65-76% (Brazil 2010BRAZIL. 2010. Plano territorial de desenvolvimento rural, sustentável e solidário do território do Cariri. http://sit.mda.gov.br/download/ptdrs/ptdrs_qua_territorio131.
http://sit.mda.gov.br/download/ptdrs/ptd...
).

Figure 1
Geographic location of the vegetation sample areas, Chapada do Araripe, Brazil.

In general, the plateau presents an altitude ranging from 700 m to 1000 m; average annual precipitation ranging from 600 mm to 1300 mm (Brazil 2010BRAZIL. 2010. Plano territorial de desenvolvimento rural, sustentável e solidário do território do Cariri. http://sit.mda.gov.br/download/ptdrs/ptdrs_qua_territorio131.
http://sit.mda.gov.br/download/ptdrs/ptd...
); different soil patches classified as Litolic, Red-Yellow Latosol, Red-Yellow Podzolic, Similar Structured Thighs and Vertissols and a mosaic of vegetational types classified as Spiny Caducifolic Forest, Rainforest Subcaducifolia Tropical Pluvial, Rainforest Subperenifolia Tropical Pluvio-Nebular and Xeromorfa Subcaducifolia Tropical (IPECE 2015), being the predominant cerrado vegetation, with about 27.5% of the total area of the Araripe National Forest, and the carrasco with the corresponding 6.67% of the total area of the FLONA (Costa et al. 2004COSTA IR, ARAÚJO FS & LIMA-VERDE LW. 2004. Flora e aspectos auto-ecológicos de um encrave de cerrado na chapada do araripe, Nordeste do Brasil. Acta Bot Brasilica 18: 759-770. https://doi.org/10.1590/S0102-33062004000400006., Ribeiro-Silva et al. 2012RIBEIRO-SILVA S, MEDEIROS MB, GOMES BM & SILVA MAP. 2012. Angiosperms from the Araripe National Forest, Ceará, Brazil. Check List 8: 744-751.).

Many rural communities (Serra do Zabelê, Barreiro Grande, Betânia, Matozinho, Estância, Serra do Zé Gomes, Mangueira, Minguiriba, Horizonte, Macaúba, Cacimbas and Baixa do Maracujá) are located inside the APA-Araripe and in the surroundings of the FLONA-Araripe, and collect timber and non-timber forest resources for different purposes (Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., Campos et al. 2015CAMPOS LZO, ALBUQUERQUE UP, PERONI N & ARAÚJO EL. 2015. Do socioeconomic characteristics explain the knowledge and use of native food plants in semiarid environments in Northeastern Brazil? J Arid Environ 115: 53-61. https://doi.org/10.1016/j.jaridenv.2015.01.002., Cavalcanti et al. 2015CAVALCANTI MCBT, RAMOS MA, ARAÚJO EL & ALBUQUERQUE UP. 2015. Implications from the Use of Non-timber Forest Products on the Consumption of Wood as a Fuel Source in Human-Dominated Semiarid Landscapes. Environ Manage 56: 389-401. https://doi.org/10.1007/s00267-015-0510-4., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.). The extraction pressure is higher in the cerrado vegetation, for being the predominant physiognomy for the Chapada do Araripe; while it is lower in the carrasco vegetation, for occupying a smaller territorial extension, and is located in a more central area and of difficult access, being part of the area where the forest management organs, do not allow collection of recuros by the communities of the Chapada do Araripe.

Besides, all communities present agriculture as the main economic activity, followed by other activities, including the trade of products in nature from the forests or manufactured by hand (Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., Feitosa et al. 2014FEITOSA IS, ALBUQUERQUE UP & MONTEIRO JM. 2014. Knowledge and extractivism of Stryphnodendron rotundifolium Mart. in a local community of the Brazilian Savanna, Northeastern Brazil. J Ethnobiol Ethnomed 10: 64., Campos et al. 2015CAMPOS LZO, ALBUQUERQUE UP, PERONI N & ARAÚJO EL. 2015. Do socioeconomic characteristics explain the knowledge and use of native food plants in semiarid environments in Northeastern Brazil? J Arid Environ 115: 53-61. https://doi.org/10.1016/j.jaridenv.2015.01.002., Cavalcanti et al. 2015CAVALCANTI MCBT, RAMOS MA, ARAÚJO EL & ALBUQUERQUE UP. 2015. Implications from the Use of Non-timber Forest Products on the Consumption of Wood as a Fuel Source in Human-Dominated Semiarid Landscapes. Environ Manage 56: 389-401. https://doi.org/10.1007/s00267-015-0510-4., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.).

Secondary data: ethnobotanical survey.

The ethnobotanical survey was based on secondary data, from the plant ecology laboratory of the Regional University of Cariri, which originated several dissertations from the postgraduate course in Molecular Bioprospecting - URCA, collected in eight communities surrounding Chapada do Araripe, in environments Cerrado and Carrasco, in the localities of Serra do Zabelê -Nova Olinda (Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042.), Barreiro Grande - Crato (Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952.), Betânia - Barbalha (Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952.) state of Ceará; Matozinho, Estância, Serra do Zé Gomes and Mangueira - Exu (Saraiva et al. 2015SARAIVA ME, ULISSES AVR, RIBEIRO DA, OLIVEIRA LGS, MACEDO DG, SOUSA BFFS, MENEZES IRA, SAMPAIO EVSB & SOUZA MMA. 2015. Plant species as a therapeutic resource in areas of the savanna in the state of Pernambuco, Northeast Brazil. J Ethnopharmacol 171: 141-153. https://doi.org/10.1016/j.jep.2015.05.034.) state of Pernambuco and Minguiriba on the border of the two states (Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001.).

The selection of these communities was based on similar criteria in the methodological procedure of conducting the research, where access to the ethnobotanical knowledge of all participants in the work was done through the semi-structured interview technique (Albuquerque et al. 2010ALBUQUERQUE UP, LUCENA RFP & ALENCAR NL. 2010. Métodos e técnicas para coleta de dados etnobiológicos. In: Albuquerque UP, Lucena RFP & Cunha LVFC (Eds), Métodos e técnicas na pesquisa etnobiológica e etnoecológica, 1ª ed., Recife, p. 39-64.), covering questions related to the medicinal uses of the species. The number for all areas was the total census, with one interview per household.

The study was approved by the Research Ethics Committee of the Regional University of Cariri, through Opinion No. nº 3.024.194, and registered with the National System for Management of Genetic Heritage and Associated Traditional Knowledge - SisGen.

Primary data: availability of species in the forests

To assess the local availability of species mentioned in ethnobotanical surveys (Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Saraiva et al. 2015SARAIVA ME, ULISSES AVR, RIBEIRO DA, OLIVEIRA LGS, MACEDO DG, SOUSA BFFS, MENEZES IRA, SAMPAIO EVSB & SOUZA MMA. 2015. Plant species as a therapeutic resource in areas of the savanna in the state of Pernambuco, Northeast Brazil. J Ethnopharmacol 171: 141-153. https://doi.org/10.1016/j.jep.2015.05.034., Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952.), four vegetational sampling areas were selected (2 cerrado and 2 carrasco areas - Figure 1). The criterion for selection of the areas was based on the regulations of the management plan of the protected area, and an area was selected for each physiognomy where access is allowed for the local population for collection, which is about 3 km from the community and another area, also for each type of vegetation studied, where access is not allowed, which is about 7 km from the community and functioned as control areas for observation of the effects of collection on resource availability.

Following the systematic sampling method, for the implementation of the sampling units in the different vegetation types, 60 plots of 10 x 20 m were allocated, totaling 4.8 hectares of vegetation sampling, for the areas with cerrado and carrasco. The plots were located at a distance of 10 m from each other, and for all were sampled all living individuals that at 30 cm from ground level had a stem diameter greater than 3 cm and height greater than 1 m. The plot method and the 3 cm diameter criterion were adopted because it is commonly used to study woody vegetation (Felfili et al. 2005FELFILI JM, CARVALHO A & HAIDAR RF. 2005. Manual para o monitoramento de parcelas permanentes nos Biomas Cerrado e Pantanal. Universidade de Brasília Departamento de Engenharia Florestal, Brasília., Araújo & Ferraz 2010ARAÚJO EL & FERRAZ EM. 2010. Amostragem da vegetação nos estudos etnobotânicos. In: Albuquerque UP, Lucena RFP & Cunha LVFC (Eds), Métodos e técnicas na pesquisa etnobiológica e etnoecológica. NUPPEA, Recife, p. 223-254).

The availability of the species was assessed based on the number of individuals in the sample (N) and on the phytosociological parameters of relative density (DRi), relative frequency (FR), relative dominance (DoR) and importance value (VI), which are the structural parameters that may be being altered as a result of the use/withdrawal of the parts of the vegetation, by the surrounding populations, and are also the usual numerical data for the calculation of conservation priority.

The sufficiency of floristic sampling was evaluated by the species accumulation curve, through the rarefaction method, and by the non-parametric richness estimation by Bootstrap (Efron 1979EFRON B. 1979. Bootstrap Methods: Another Look at the Jackknife. Ann Statist 7(1): 1-26.) and Chao (Chao 1984CHAO A. 1984. Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11: 265-270., 1987CHAO A. 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783-791.) estimators, calculated with the help of the R (R Development Core Team 2019R DEVELOPMENT CORE TEAM. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Disponível em: <https://www.R-project.org/>.
https://www.R-project.org/...
).

Identification of plant species

For the species cited as medicinal, and for the floristic survey of the areas, species found in the reproductive stage were collected with duplicates, by authorization of the Biodiversity Authorization and Information System - SISBIO, by nº63983-2, and taken to the Laboratory of Plant Ecology of the Regional University of Cariri, processed according to the usual techniques of herborization (Mori et al. 1989MORI LA, SILVA LAM, LISBOA G & CORADIN L. 1989. Manual de manejo do herbário fanerogâmico. Centro de Pesquisa do Cacau, Ilhéus.), and identified by the team of the Cariri Herbarium Dárdano de Andrade-Lima of the Universidade Regional do Cariri- URCA, by comparison with previously identified material and based on specialized literature. Those whose identification was not possible were sent to specialists from other herbaria for proper botanical identification.

Calculation for woody species with conservation priority.

As a quantitative analysis tool for the assessment of threatened species, the score- based technique developed by Dzerefos & Witkowski (2001)DZEREFOS CM & WITKOWSKI ETF. 2001. Density and potential utilization of medicinal grassland plants from Abe Bailey Nature Reserve, South Africa. Biodivers Conserv 10: 1875-1896. https://doi.org/10.1023/A:1013177628331. and modified by Albuquerque et al. (2011)ALBUQUERQUE UP, SOLDATI GT, SIEBER SS, MEDEIROS PM, SÁ JC & SOUZA LC. 2011. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environ Develop Sustain 13: 277-292. was used to identify possible species with priority for conservation. The criteria used to establish the scores are explained in Table I. The conservation priority index (CP) was calculated based on the formula: PC = 0.5 (EB) + 0.5 (RU), where EB corresponds to the Biological Score and RU to the Risk of Use. EB was calculated using the formula: EB = D x 10, where D corresponds to a score value (see Table I), assigned based on the relative density of each taxon (DRi) in the sampling. RU was calculated by the formula RU = 0.5 (H) + 0.5 (U) x 10, where H corresponds to the collection risk of the species (see a score in Table I) and U corresponds to the value of use, being determined by the sum of the means of local importance (L) and the diversity of use (V) of the species. The local importance value (L) was determined by the percentage of the number of informants who indicated a certain species as medicinal (Table I). The diversity of use (V) was scored based on the number of use types attributed to a species, ranging from 1 to 10. The use of wood for some species was associated with the calculations, adding 10 points (Table I). The PC index calculation allowed classifying medicinal plants into three categories (Dzerefos & Witkowski 2001): category 1: with a score value >80, including species that require high conservation priority, with the need for controlled collection and establishment of alternatives for their conservation; category 2: includes species with scores between 60 and 80, which have the potential to be collected, according to location and specific quotas; category 3: includes species with a value <60, which support higher collection intensity in the sampled area.

Table I
Score criteria for plants used, relative density, collection risk, local importance and diversity of use.

The relationship between the value of the use of the resource and its availability in the forests was evaluated through multiple regression, with a progressive stepwise procedure a posteriori, with the value of use being the independent variable and the relative pairings density, frequency and dominance the dependent variables. The analysis was performed with the help of the BioEstat 5.0 Program.

RESULTS

Diversity of medicinal plants of FLONA and APA do Araripe

The richness of medicinal species cited in the ethnobotanical studies was 107 species, belonging to 39 families and 83 genera (Table II), of which 92 species, 36 families and 70 genera registered in the cerrado areas and 47 species, 25 families and 39 genera registered in the carrasco areas. Of the 107 species, 31 were common to both types of vegetation. The most representative families for the cerrado and carrasco areas, respectively, were: Fabaceae (20 spp and 12 ssp), Euphorbiaceae (9 ssp and 5 ssp) and Apocynaceae (9 spp 5 spp).

Table II
Species with indications for use by the communities of the Chapada do Araripe, near cerrado (a) and carrasco (b) areas in northeastern Brazil .

The majority of species, from the cerrado and carrasco (aprox. 73%), had their medicinal uses linked to perennial structures (bark 29%, weaves 23% and roots 26%), also occurring the use of non-perennial structures (leaves 12%, fruits 8%, seeds 1%, and flowers 1%) and 66% of the species showed indication ofse of more than one structure and 34% had an indication of a single structure (Table II).

A total of 147 diseases were recorded, being coughs, colds, inflammations, scarring, and pain in general the most common (Table II). The diversity of therapeutic indications in the region of FLONA Araripe has been treated with the use of teas, emplasts, decoctions, lickers, baths with the use of species occurring in native vegetation, as well as with the use of exotic species, kept in the backyards and/or bought in free fairs.

The species with the greatest diversity of medicinal uses attributed by the population were: Copaifera langsdorffi and Ximenia americana (22 types of uses each), Hancornia speciosa (19 types of uses), Roupala montana (16 types of uses), Caryocar coriaceum, Himatanthus drasticus, Stryphnodendron rotundifolim (15 types of uses each), Myracrodruon urundeuva, Croton heliotropiifolius, Hymenaea courbaril (14 types of uses each), Rauvolfia sp 2, Libidibia ferrrea, Hybanthus ipecacuanha, Rosamarinus officinalis (13 types of uses each), Bowdichia virgilioides, Dimorphandra garderiana (12 types of uses each), Anacardium occidentale, Mentha spicata (11 types of uses each), Ziziphus joazeiro, Ruta graveolens, Kalanchoe pinata (10 types of uses each).

Availability of species in the cerrado and carrasco areas

In all four sampled areas there was sufficient floristic sampling, based on the species accumulation curves with rarefaction (Figure 2) and the Chao and Boot richness estimators (Table III). However, of the 92 woody medicinal plants reported by the interviewees for the cerrado areas, only 54 (59%) were present in the phytosociological surveys. In the carrasco area, of the 47 medicinal species reported, only 18 (38%) occurred in vegetation sampling (Tables IV and V).

Figure 2
Species accumulation curve, with rarefaction, for Cerrado and Carrasco areas.
Table III
Estimation of sampling sufficiency by Chao and Boot estimators, with their respective standard deviations.
Table IV
Availability of species in cerrado areas near (cerrado1 ) and far (cerrado 2) from the community. Chapada do Araripe.
Table V
Availability of the species in the areas de carrasco close (carrasco 1) and far away (carrasco 2) from the community, Chapada do Araripe.

In cerrado vegetation, the highest relative densities were Myrcia sp in the conserved área (C1) and Lochocarpus araripensis in the o area anthropogenic (C2) (Tables IV and V). The most frequent species in the sampled (Byrsonima sericea Fr 5.87 C1 and Fr 5.39 C2, and Myrcia sp Fr 6.29 C1 and Fr 3.47 C2) did not have relevant importance for local use. The dominant species were Byrsonima sericea and Copaifera langsdorffii, both by the size of their populations and the sum of their basal areas in both C1 and C2 (Table IV) and these had higher medicinal indications (Table II). Only Copaifera langsdorffi and Ximenia americana, species with higher indications in ethnobotanical surveys, were among those with higher densities and frequencies in the sampling. All other species indicated for medicinal use by the communities had low population densities or did not occur in the sampling. Some of them such as: Stryphnodendron rotundifolium, Anacardium microcarpum, Dimorphandra gardneriana, Croton heliotropiifolius, Hancornia speciosa and Roupala montana showed considerable versatility of medicinal use.

In the carrasco vegetation, the highest population density was recorded for Copaifera langsdorffii (Table V) and the highest frequencies were recorded for Maytenus rigida, Copaifera langsdorffii, Roupala montana and Psidium myrsinites (Table V) for both analyzed areas. Among these species, only Copaifera langsdorffii and Roupala montana were indicated with diverse medicinal uses in ethnobotanical studies. As in the cerrado areas, the species of low density or low frequency in the area sampled by the carrasco had diversified medicinal uses.

Species use values (Tables IV and V) had no significant relationship with their availability in the areas sampled in cerrado 1 (F(3.38)=0.76; p=0.52), cerrado 2 (F(3.30)=0.80; p=0.50) and carrasco 2 (F(3.10)=1.07; p=0.04), considering the relative parameters, density, frequency and dominance (Tables IV and V), but had a relationship in the area of Carrasco 1 (F(3.14)=3.24; p=0.053, being the frequency the only variable with significant explanatory power in the analysis (R2=38.5%; p=0.006).

Priority of conservation of medicinal plants

The conservation priority index (CP) allowed the separation of the cerrado species (54) and the carrasco (18) in the three conservation categories (Tables VI and VII).

Table VI
Conservation priority index (PC) of the medicinal plants of the Chapada do Araripe, northeastern Brazil.
Table VII
Conservation priority index (PC) of the medicinal plants of the Chapada do Araripe, northeastern Brazil.

Included in category 1 (highest conservation need) were 13 and 7 species in areas 1 and 2 of the Cerrado, and 3 and 4 species in areas 1 and 2 of the carrasco, respectively. The highlight of the category 1 species is perhaps because they presented low densities, frequencies, dominance and IVI, associated with a large number of citations of medicinal uses, and the indication of the use of their perennial structures. The species with the highest conservation priority scores within category 1 were Croton zehntneri and Secondatia floribunda in the cerrado, but C. zehntneri was only recorded in the most conserved area. In the carrasco the species were Ximenea americana, Croton heliotropifolius and Bowdichia virglioides, all having a record in both vegetation areas, although with higher importance value in the more conserved environment. In general, the species with the highest indications of use in folk medicine (Table II) appear in category 1, which is the most critical for conservation (Tables VI and VII).

Most species were classified in categories 2 or 3, which still support collection pressure in protected areas because they are still relatively available in vegetation. In category 2 there were 23 and 25 species in areas 1 and 2 of the cerrado and 8 and 2 species in areas 1 and 2 of the carrasco, respectively. In category 3 there were 4 and 2 species in areas 1 and 2 of the cerrado and 6 and 9 species in areas 1 and 2 of the carrasco, respectively (Tables VI and VII). Some species in categories 2 and 3 had diversified medicinal use, such as Roupala montana and Hymenaea courbaril (Table II) and others, although with diversified uses did not occur in the sampling, such as Libidibia ferrea (Tables III and IV).

DISCUSSION

Medicinal resources and conservation problems in protected forests

The gathered knowledge on medicinal plants showed that many diseases are treated by local populations with the use of species from the Araripe region, especially the Fabaceae, Euphorbiaceae and Apocynaceae families (Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., Saraiva et al. 2015SARAIVA ME, ULISSES AVR, RIBEIRO DA, OLIVEIRA LGS, MACEDO DG, SOUSA BFFS, MENEZES IRA, SAMPAIO EVSB & SOUZA MMA. 2015. Plant species as a therapeutic resource in areas of the savanna in the state of Pernambuco, Northeast Brazil. J Ethnopharmacol 171: 141-153. https://doi.org/10.1016/j.jep.2015.05.034., Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952.), both in the cerrado vegetation and in the carrasco (Table II). This finding was expected, since such families generally present considerable species richness in the different vegetational types of semi-arid environments (Tunholi et al. 2013TUNHOLI VP, RAMOS MA & SCARIOT A. 2013. Availability and use of woody plants in a Agrarian reform settlement in the cerrado of the state of Goiás, Brazil. Acta Bot Brasilica 27: 604-612. https://doi.org/10.1590/S0102-33062013000300018., Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Saraiva et al. 2015SARAIVA ME, ULISSES AVR, RIBEIRO DA, OLIVEIRA LGS, MACEDO DG, SOUSA BFFS, MENEZES IRA, SAMPAIO EVSB & SOUZA MMA. 2015. Plant species as a therapeutic resource in areas of the savanna in the state of Pernambuco, Northeast Brazil. J Ethnopharmacol 171: 141-153. https://doi.org/10.1016/j.jep.2015.05.034., Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., 2019, Santos et al. 2019SANTOS JEG ET AL. 2019. Ethnopharmacology and tradicional knowledge of therapeutical practices View project The biodiversity conservation at the landscape level: climate change and anthropogenic disturbance View project. J Agric Sci 11: 115-129. https://doi.org/10.5539/jas.v11n7p115., Macêdo et al. 2018MACÊDO MJF, RIBEIRO DA, SANTOS MO, MACEDO DG, MACEDO JGM, ALMEIDA BV, SARAIVA ME, LACERDA MNS & SOUZA MMA. 2018. Fabaceae medicinal flora with therapeutic potential in Savanna areas in the Chapada do Araripe, Northeastern Brazil. Brazilian J Pharmacogn 28: 738-750. https://doi.org/10.1016/j.bjp.2018.06.010., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.).

Besides, the local ethnobotanical knowledge compiled (Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., Saraiva et al. 2015SARAIVA ME, ULISSES AVR, RIBEIRO DA, OLIVEIRA LGS, MACEDO DG, SOUSA BFFS, MENEZES IRA, SAMPAIO EVSB & SOUZA MMA. 2015. Plant species as a therapeutic resource in areas of the savanna in the state of Pernambuco, Northeast Brazil. J Ethnopharmacol 171: 141-153. https://doi.org/10.1016/j.jep.2015.05.034., Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952.) showed that more than 70% of the species in the Araripe region have perennial structures such as bark/weaves and roots used in the treatment of diseases, confirming the emphasis given to these structures in other studies (Martínez-Moreno et al. 2017MARTÍNEZ-MORENO D, ALVARADO-FLORES R, MENDOZA-CRUZ M & BASURTO-PEÑA F. 2017. Plantas medicinales de cuatro mercados del estado de Puebla, México. Bot Sci 79: 79. https://doi.org/10.17129/botsci.1735., Bussman et al. 2007BUSSMANN RW, SHARON D, VANDEBROEK I, JONES A & REVENE Z. 2007. Health for sale: The medicinal plant markets in Trujillo and Chiclayo, Northern Peru. J Ethnobiol Ethnomed 3: 37. https://doi.org/10.1186/1746-4269-3-37., Oliveira et al. 2007OLIVEIRA RLC, LINS NETO EMF, ARAÚJO EL & ALBUQUERQUE UP. 2007. Conservation priorities and population structure of woody medicinal plants in an area of caatinga vegetation (Pernambuco State, NE Brazil). Environ Monit Assess 132: 189- 206. https://doi.org/10.1007/s10661-006-9528-7., Monteiro et al. 2010MONTEIRO JM, ARAÚJO EL, AMORIM ELC & ALBUQUERQUE UP. 2010. Local Markets and Medicinal Plant Commerce: A Review with Emphasis on Brazil. Econ Bot 64: 352-366. https://doi.org/10.1007/s12231-010-9132-1, Marinho et al. 2011MARINHO MGV, SILVA CC & ANDRADE LHC. 2011. Levantamento etnobotânico de plantas medicinais em área de caatinga no município de São José de Espinharas, Paraíba, Brasil. Rev Bras Plantas Med 13: 170-180. https://doi.org/10.1590/S1516- 05722011000200008., Macêdo et al. 2018MACÊDO MJF, RIBEIRO DA, SANTOS MO, MACEDO DG, MACEDO JGM, ALMEIDA BV, SARAIVA ME, LACERDA MNS & SOUZA MMA. 2018. Fabaceae medicinal flora with therapeutic potential in Savanna areas in the Chapada do Araripe, Northeastern Brazil. Brazilian J Pharmacogn 28: 738-750. https://doi.org/10.1016/j.bjp.2018.06.010., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.). Many species have renewable structures, such as leaves, as a part used in medicinal use (Hamayun et al. 2006HAMAYUN M, KHAN SA, SOHN EY & LEE I-J. 2006. Folk medicinal knowledge and conservation status of some economically valued medicinal plants of District Swat, Pakistan. Lyonia 11: 101-103., Kar & Borthakur 2007KAR A & BORTHAKUR SK. 2007. Wild vegetables sold in local markets of Karbi Anglong, Assam. Indian Journal of Traditional Knowledge. Indian J Tradic Knowlegde 6: 169-172., Monteiro et al. 2010MONTEIRO JM, ARAÚJO EL, AMORIM ELC & ALBUQUERQUE UP. 2010. Local Markets and Medicinal Plant Commerce: A Review with Emphasis on Brazil. Econ Bot 64: 352-366. https://doi.org/10.1007/s12231-010-9132-1), which generates fewer problems for conservation. The use of perennial structures tends to be more harmful to the conservation of plant species, especially if other aspects are taken into account, such as collection technique and intensity, marketing of the resource, versatility of uses and the availability of the resource in forests.

Although the medicinal resource is locally important for the treatment of human health, the collection, depending on the technique used, may cause injuries that compromise the plant life (Bernal et al. 2011BERNAL R, TORRES C, GARCÍA N, ISAZA C, LÓPEZ JAN, VALLEJO MI, GALEANO G & BALSLEV H. 2011. Palm Management in South America. Bot Rev 77: 607-646. https://doi.org/10.1007/s12229-011-9088-6., Feitosa et al. 2017FEITOSA IS, SOBRAL A, MONTEIRO JM, ARAÚJO EL & ALBUQUERQUE UP. 2017. Impact of collection on bark regeneration from Stryphnodendron rotundifolium Mart. in northeastern Brazil. Environ Monit Assess 189: 234. https://doi.org/10.1007/s10661-017-5908-4.), or may directly generate its death, in the case of root collection that often involves the removal of the entire plant from the substrate.

In addition, the form of collection may generate negative pressure for the renewal of the resource in forests (Oliveira et al. 2007OLIVEIRA RLC, LINS NETO EMF, ARAÚJO EL & ALBUQUERQUE UP. 2007. Conservation priorities and population structure of woody medicinal plants in an area of caatinga vegetation (Pernambuco State, NE Brazil). Environ Monit Assess 132: 189- 206. https://doi.org/10.1007/s10661-006-9528-7., Monteiro et al. 2010MONTEIRO JM, ARAÚJO EL, AMORIM ELC & ALBUQUERQUE UP. 2010. Local Markets and Medicinal Plant Commerce: A Review with Emphasis on Brazil. Econ Bot 64: 352-366. https://doi.org/10.1007/s12231-010-9132-1, Ribeiro et al. 2019RIBEIRO DA ET AL. 2019. Conservation priorities for medicinal woody species in a cerrado area in the Chapada do Araripe, northeastern Brazil. Environ Dev Sustain 21: 61-77. https://doi.org/10.1007/s10668-017-0023-9., Feitosa et al. 2017FEITOSA IS, SOBRAL A, MONTEIRO JM, ARAÚJO EL & ALBUQUERQUE UP. 2017. Impact of collection on bark regeneration from Stryphnodendron rotundifolium Mart. in northeastern Brazil. Environ Monit Assess 189: 234. https://doi.org/10.1007/s10661-017-5908-4., Macêdo et al. 2018MACÊDO MJF, RIBEIRO DA, SANTOS MO, MACEDO DG, MACEDO JGM, ALMEIDA BV, SARAIVA ME, LACERDA MNS & SOUZA MMA. 2018. Fabaceae medicinal flora with therapeutic potential in Savanna areas in the Chapada do Araripe, Northeastern Brazil. Brazilian J Pharmacogn 28: 738-750. https://doi.org/10.1016/j.bjp.2018.06.010.). Another aspect that increases the problem of conservation of marketed resources is the place of residence of local populations, because if they live far from the forests, people tend to collect and stock more of the resource to compensate for the cost of its locomotion (Lopes et al. 2011LOPES PFM, CLAUZET M, HANAZAKI N, RAMIRES M, SILVANO RAM & BEGOSSI A. 2011. Foraging Behaviour of Brazilian Riverine and Coastal Fishers: How much is explained by the optimal foraging theory? Conserv Soc 9: 236-246., Soldati & Albuquerque 2012, Feitosa et al. 2018FEITOSA IS, MONTEIRO JM, ARAÚJO EL, LOPES PFM & ALBUQUERQUE UP. 2018. Optimal Foraging Theory and Medicinal Bark Extraction in Northeastern Brazil. Hum Ecol 46: 917-922. https://doi.org/10.1007/s10745-018-0037-4.).

The versatility of medicinal use of the species is another characteristic that has implications on the conservation of the resource, especially if the species also has non- medical uses, by increasing its collection pressure in the region. This is the case, for example, of Ximenia americana and Caryocar coriaceum which were indicated for the treatment of 22 and 15 diseases, respectively (Table II). The diversity of medicinal uses of these species was found in other studies (Monteiro et al. 2011MONTEIRO JM, RAMOS MA, ARAÚJO EDL, AMORIM ELC & ALBUQUERQUE UP. 2011. Dynamics of medicinal plants knowledge and commerce in an urban ecosystem (Pernambuco, Northeast Brazil). Environ Monit Assess 178: 179-202. https://doi.org/10.1007/s10661-010-1681., Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952., Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.), but these species also have food and wood uses (Souza Júnior et al. 2013SOUZA JÚNIOR JR, ALBUQUERQUE UP & PERONI N. 2013. Traditional Knowledge and Management of Caryocar coriaceum Wittm. (Pequi) in the Brazilian Savanna, Northeastern Brazil. Econ Bot 67: 225-233. https://doi.org/10.1007/s12231-013-9241-8., Cavalcanti et al. 2015CAVALCANTI MCBT, RAMOS MA, ARAÚJO EL & ALBUQUERQUE UP. 2015. Implications from the Use of Non-timber Forest Products on the Consumption of Wood as a Fuel Source in Human-Dominated Semiarid Landscapes. Environ Manage 56: 389-401. https://doi.org/10.1007/s00267-015-0510-4., Campos et al. 2015CAMPOS LZO, ALBUQUERQUE UP, PERONI N & ARAÚJO EL. 2015. Do socioeconomic characteristics explain the knowledge and use of native food plants in semiarid environments in Northeastern Brazil? J Arid Environ 115: 53-61. https://doi.org/10.1016/j.jaridenv.2015.01.002., Nascimento et al. 2019NASCIMENTO LGS, RAMOS MA, ALBUQUERQUE UP & ARAÚJO EL. 2019. The use of fi rewood in protected forests: Collection practices and analysis of legal restrictions to extractivism. Acta Bot Brasilica 33: 292-302. https://doi.org/10.1590/0102-33062019abb0050.), which makes them target of greater impact in the region. In addition, some species had different parts (roots, flowers, seeds, bark) collected for medicinal use, as recorded for Psidium myrsinites, which also increase the anthropic pressure on the resource.

In addition, the fact that a species has high versatility of medicinal use does not imply that it is highly available in the forest to support the pressure of local use. In this study, woody species with many indications of medicinal use, such as Ximenia americana, Stryphnodendron rotundifolium, Dimorphandra gardneriana and Hancornia speciosa did not have high density in phytosociological sampling. Other species, such as Coutarea hexandra, had a considerable indication of medicinal use, but showed a small population size in the sample (Tables II, III and IV).

It is worth noting that this study recorded a low occurrence of woody medicinal species in the sampling plots, both in the cerrado (59%) and in the carrasco (38%). However, this low percentage does not necessarily indicate insufficient floristic sampling, as demonstrated by the rarefaction curve and Boot and Chao richness estimators. It is necessary to remember that the uses of medicinal plants were retrieved from secondary data from studies done in past times, while the sampling of vegetation was done in the present time (primary data). Thus, other possible explanations for the low recording of medicinal species in the plots could be: 1. Some species existed in the past, but are presently of low abundance or no longer exist in the area; 2. Some people may have used medicinal plants that were cultivated in their gardens; 3. It is possible that some species have an aggregate distribution pattern, and have not been recorded in the plots; 4. It is also possible that some are more typical of vegetational formations different from the cerrado and carrasco, for example, Mimosa tenuiflora, which is frequent in the caatinga vegetation and widely exploited also for other uses (Figueirôa et al. 2006FIGUEIRÔA JM, PAREYN FGC, ARAÚJO EL, SILVA CE, SANTOS VF, CUTLER DF, BARACAT A & GASSON P. 2006. Effects of cutting regimes in the dry and wet season on survival and sprouting of woody species from the semi-arid caatinga of northeast Brazil. For Ecol Manage 229: 294-303. https://doi.org/10.1016/j.foreco.2006.04.008.).

However, although we have not evaluated the reason for the inclusion or not of the species in the sampling, the fact is that often the collection is done without considering the real availability of the resource in the forest. According to Maldonado et al. (2013)MALDONADO B, CABALLERO J, DELGADO-SALINAS A & LIRA R. 2013. Relationship between Use Value and Ecological Importance of Floristic Resources of Seasonally Dry Tropical Forest in the Balsas River Basin, México. Econ Bot 67: 17-29. https://doi.org/10.1007/s12231-013-9222-y., the frequency was the phytosociological attribute that most influenced the value of the use of the species in central Mexico, in the categories medicinal, food, construction and firewood. However, in the case of medicinal use, density was another parameter that maintained a significant relationship in the use of the species. In the present study these findings was not confirmed for three of the sampled areas, which had already been observed in the study by de Silva et al. (2019)SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084. at FLONA Araripe. Only in carrasco area 1 there was a significant relationship between the value of use and the frequency of the resource, indicating that there is not always a clear relationship between the value of the use of the species and its local availability in the forests.

Ecologically, although destructive collection practices are negative for the conservation of the collected resource, the human action of removing a plant from the forest can be positive for the occurrence and or increase of populations of other species in the forest that need more illuminated environments for their growth. This is the case of Byrsonima sericea and the species of the genus Myrcia, which according to Araujo et al. (1998)ARAÚJO FS, SAMPAIO EVSB, RODAL MJN, FERNANDES AG & FIGUEIREDO MA. 1998. Composição florística da vegetação de carrasco, Novo Oriente, CE. Rev Bras Botânica 21: 105-116. https://doi.org/10.1590/s0100-84041998000200001., are considered pioneers and it needs a greater demand for light for their establishment. Although those species did not have presented high densities in the sampled area, despite their medicinal importance.

The low availability recorded in this study for some of the resources used in FLONA Araripe indicates that the establishment of conservation units, despite being an important strategy (Archibald et al. 2020ARCHIBALD CL, BARNES MD, TULLOCH AIT, FITZSIMONS JA, MORRISON TH, MILLS M & RHODES JR. 2020. Differences among protected area governance types matter for conserving vegetation communities at-risk of loss and fragmentation. Biol Conserv 247: 108533. https://doi.org/10.1016/j.biocon.2020.108533.), is not sufficient for forest conservation. In many protected areas the adequate use of the resource is not guided and monitored. According to Brites & Morsello (2017)BRITES AD & MORSELLO C. 2017. Beliefs about the Potential Impacts of Exploiting Non-Timber Forest Products Predict Voluntary Participation in Monitoring. Environ Manage 59: 898-911. https://doi.org/10.1007/s00267-017-0845-0., non-oriented resource uses tend to generate negative effects on biological diversity, such as alteration of the structure or reduction in population size, overloading of plant parts that are used, and possible changes in species richness of the community.

Untargeted resource uses have been recorded in other regions (Martins 2012MARTINS A. 2012. Conflitos ambientais em unidades de conservação: dilemas da gestão territorial no Brasil. Rev Bibliográfica Geogr y Ciencias Soc 17: 1-11., Andrade et al. 2015ANDRADE WM, RAMOS MA, SOUTO WMS, BENTO-SILVA JS, ALBUQUERQUE UP & LIMA EA. 2015. Knowledge, Uses and Practices of the Licuri Palm (Syagrus coronata (Mart.) Becc.) around Protected Areas in Northeastern Brazil Holding the Endangered Species Lear’s Macaw (Anodorhynchus leari). Trop Conserv Sci 8: 893-911. https://doi.org/10.1177/194008291500800403., Ulloa-Ulloa et al. 2017ULLOA-ULLOA C ET AL. 2017. An integrated assessment of the vascular plant species of the Americas. Science 358 (6370): 1614-1617. https://doi.org/10.1126/science.aao0398.), indicating diversity conservation and UC management a global challenge. In order to increase the efficiency of the UCs in the protection of biological diversity, it has been indicated that it is necessary that UC managers develop strategies to better understand the needs of local populations, with the promotion of actions that favor interaction with them and minimize local conflicts. It is also necessary that they consider the traditional ecological knowledge of the communities on the spatial distribution of species, collection areas, and ways of using and managing the resource (Hanazaki 2003HANAZAKI N. 2003. Becker, Goffman e a antropologia no Brasil. Biomemas 16: 23-47. https://doi.org/10.5007/%x.). Furthermore, it has been indicated the need for ecological studies more directed to the resource accessed, to evaluate its capacity to support collection pressure and the time needed for renewal of its populations (Guedje et al. 2007GUEDJE NM, ZUIDEMA PA, DURING H, FOAHOM B & LEJOLY J. 2007. Tree bark as a non-timber forest product: The effect of bark collection on population structure and dynamics of Garcinia lucida Vesque. For Ecol Manage 240: 1-12., Shackleton & Pandey 2014SHACKLETON CM & PANDEY AK. 2014. Positioning non-timber forest products on the development agenda. For Policy Econ 38: 1-7. https://doi.org/10.1016/j.forpol.2013.07.004., Andrade et al. 2015ANDRADE WM, RAMOS MA, SOUTO WMS, BENTO-SILVA JS, ALBUQUERQUE UP & LIMA EA. 2015. Knowledge, Uses and Practices of the Licuri Palm (Syagrus coronata (Mart.) Becc.) around Protected Areas in Northeastern Brazil Holding the Endangered Species Lear’s Macaw (Anodorhynchus leari). Trop Conserv Sci 8: 893-911. https://doi.org/10.1177/194008291500800403., Gaoue et al. 2016GAOUE OG, JIANG J, DING W, AGUSTO FB & LANHART S. 2016. Optimal harvesting strategies for timber and non-timber forest products in tropical ecosystems. Theor Ecol 9: 287-297. https://doi.org/10.1007/s12080-015-0286-4.).

The hypothesis of this study was confirmed, since the most versatile medicinal species necessarily were not the same ones with high abundance in the sampling. According to maximization theory (Albuquerque et al. 2019ALBUQUERQUE UP, MEDEIROS PM, JÚNIOR WSF, SILVA TC, SILVA RRV & GONÇALVES-SOUZA T. 2019. Social-ecological theory of maximization: basic concepts and two initial models. Biol Theory 14(2): 73-85.) this fact could be justified by the need that populations have to optimize time and energy in obtaining the resource. This need leads people to use the most easily found resources. In addition, other variables affect people’s use and knowledge of medicinal resources, such as socioeconomic variables (Albuquerque & Faria 2018ALBUQUERQUE UP & FARIA JLM. 2018. Como fatores socioeconômicos podem afetar o conhecimento de plantas medicinais? Revista Brasileira de Meio Ambiente 3(1): 033-036.). Another fact that must be considered is that many of the medicinal species are used by local populations for other purposes, such as firewood for example (Santos et al. 2015SANTOS GC, ALMEIDA ALS, SOUSA JUNIOR JR, CAMPOS LZO, FEITOSA IS, CAMPOS JLA, CAVALCANTE MCBT, SIVA RRV & ALBUQUERQUE UP. 2015. Espécies lenhosas de importancia econômica na Chapada do Araripe. In: Albuquerque UP & Meiado MV (Eds), Livro Sociobiodiversidade na Chapada do Araripe. Vol. 1, p. 381-396.), which increases local use pressure. The interaction of all these factors can have a major effect in explaining the availability of the resource in the area and need to be considered also in defining priority species for conservation.

Conservation priorities and importance of conservation actions

The findings of this study showed that 13 species in the cerrado (B. virgilioides, C. zehntneri, H. speciosa, C. heliotropiifolius, H. drasticus, S. floribunda, S. diversiflora, X. americana, P. cincinnata, P. heptaphyllum, S. japecanga, S. rotundifolium and D. gardneriana) and four in the carrasco (C. heliotropifolius, D. gardineriana, B. virglioides and X. americana), according to the criteria adopted in the classification (Table I) (Dzerefos & Witkowski 2001) no longer support the collection pressure and needs priority conservation actions. Of these, only four (H. drasticus, B. Virgilioides, H. speciosa and S. rotundifolium) were indicated as priorities for conservation based on the perception of people from three communities in the region (Silva et al. 2019SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084.).

Other species, like C. langsdorfi (Tables V and VI), which based on the calculated index still support collection pressure, in the study by Silva et al. (2019)SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084. were indicated a priority for local conservation, based on people’s perception. This difference in the indication of species may have occurred because the communities evaluated by Silva et al. (2019)SILVA NF, HANAZAKI N, ALBUQUERQUE UP, CAMPOS LA, FEITOSA IS & ARAUJO EL. 2019. Local Knowledge and Conservation Priorities of Medicinal Plants near a Protected Area in Brazil. Evidence- based Complement Altern Med 2019: 1-18. https://doi.org/https://doi.org/10.1155/2019/8275084. were different from those analyzed in the secondary data of the works considered in this study (Souza et al. 2014SOUZA RKD, SILVA MAP, MENEZES IRA, RIBEIRO DA, BEZERA LR & SOUZA MMA. 2014. Ethnopharmacology of medicinal plants of carrasco, northeastern Brazil. J Ethnopharmacol 157: 99-104. https://doi.org/10.1016/j.jep.2014.09.001., Ribeiro et al. 2014RIBEIRO DA, OLIVEIRA LGS, MACÊDO DG, MENZES IRA, COSTA JGM, SILVA MAP, LACERDA SR & SOUZA MMA. 2014. Promising medicinal plants for bioprospection in a Cerrado area of Chapada do Araripe, Northeastern Brazil. J Ethnopharmacol 155: 1522-1533. https://doi.org/10.1016/j.jep.2014.07.042., Saraiva et al. 2015SARAIVA ME, ULISSES AVR, RIBEIRO DA, OLIVEIRA LGS, MACEDO DG, SOUSA BFFS, MENEZES IRA, SAMPAIO EVSB & SOUZA MMA. 2015. Plant species as a therapeutic resource in areas of the savanna in the state of Pernambuco, Northeast Brazil. J Ethnopharmacol 171: 141-153. https://doi.org/10.1016/j.jep.2015.05.034., Macedo et al. 2016MACEDO DG ET AL. 2016. Versatility and consensus of the use of medicinal plants in an area of cerrado in the Chapada do Araripe, Barbalha - CE- Brazil. J Med Plants Res 10: 505-514. https://doi.org/10.5897/jmpr2015.5952.), but even if the localities and methodologies were different, the findings of this study reinforce the need for a priority look for B. virgilioides, H. drasticus, H. speciosa and S. rotundifolium. With the exception of the first specie, the others are: widely marketed, source of livelihood for many families in the region and are already on the lists of endangered species of the Ministry of Environment and the International Union for Conservation of Nature and Natural Resources-IUCN (MMA 2008MMA. 2008. Instrução Normativa N° 6, de 23 de Setembro de 2008. Brasil. https://www.normasbrasil.com.br/norma/instrucao-normativa-6-2008_77052.
https://www.normasbrasil.com.br/norma/in...
, Souza Júnior et al. 2013SOUZA JÚNIOR JR, ALBUQUERQUE UP & PERONI N. 2013. Traditional Knowledge and Management of Caryocar coriaceum Wittm. (Pequi) in the Brazilian Savanna, Northeastern Brazil. Econ Bot 67: 225-233. https://doi.org/10.1007/s12231-013-9241-8., IUCN 2019IUCN. 2019. Guidelines for Using the IUCN Red List Categories and Criteria. Version 14. https://www.iucnredlist.org/resources/categories-and-criteria.
https://www.iucnredlist.org/resources/ca...
, Baldauf & Santos 2013BALDAUF C & SANTOS FAM. 2013. Ethnobotany, Traditional Knowledge, and Diachronic Changes in Non-Timber Forest Products Management: A Case Study of Himatanthus drasticus (Apocynaceae) in the Brazilian Savanna. Econ Bot 67: 110-120. https://doi.org/10.1007/s12231-013-9228-5., Fereira Jr. et al. 2016, Feitoza et al. 2017, 2018).

However, attention is still recommended for species classified in category 2, which allows restricted use, especially for those with perennial structures (bark, weaves and roots) as the exploited part, as such uses may cause mortality and decrease of the exploited population in the future (Albuquerque et al. 2009ALBUQUERQUE UP, ARAÚJO TAS, RAMOS MA, NASCIMENTO V, LUCENA RFP, MONTEIRO JM, ALAENCAR N & ARAÚJO EL. 2009. How ethnobotany can aid biodiversity conservation: Reflections on investigations in the semi-arid region of NE Brazil. Biodivers Conserv 18: 127-150. https://doi.org/10.1007/s10531-008-9463-8., 2011), which reveals the need for actions to ensure the sustainability of these practices.

Environments considered conserved for both phytophysiognomies, had high species richness, as expected because the free access of local populations for collection of the resource was not allowed. Consequently, the areas conserved had more species in each category of the conservation. While areas of greater contact with the communities, had lower specific richness, followed by fewer species in each category.

The estimation of priority species for conservation, although it may be influenced by factors not considered in the indices adopted (Dzerefos & Wikowski 2001, Albuquerque et al. 2011ALBUQUERQUE UP, SOLDATI GT, SIEBER SS, MEDEIROS PM, SÁ JC & SOUZA LC. 2011. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environ Develop Sustain 13: 277-292.), is an important tool and assists in conservationist decisions (Dhar et al. 2000DHAR U, RAWAL RS & UPRETI J. 2000. Setting priorities for conservation of medicinal plants - A case study in the Indian Himalaya. Biol Conserv 95: 57-65. https://doi.org/10.1016/S0006-3207(00)00010-0., Oliveira et al. 2007OLIVEIRA RLC, LINS NETO EMF, ARAÚJO EL & ALBUQUERQUE UP. 2007. Conservation priorities and population structure of woody medicinal plants in an area of caatinga vegetation (Pernambuco State, NE Brazil). Environ Monit Assess 132: 189- 206. https://doi.org/10.1007/s10661-006-9528-7.), especially in megadiverse countries such as Brazil, which has biodiversity hotspots (Myers et al. 2000MYERS N, MITTERMELER RA, MITTERMELER CG, FONSECA GAB & KENT J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858. https://doi.org/10.1038/35002501.), with many endemic species in some vegetational formations. According to Eken et al. (2004)EKEN G ET AL. 2004. Key Biodiversity Areas as Site Conservation Targets. BioScience 54 (12): 1110-1118. it is necessary to consider the occurrence of endemism in the forest, because on a local scale endemic species can be rapidly extinct if negative environmental stochastic events occur, especially if the size of their populations are naturally reduced or have been reduced because they are intensely collected and used in the region, and a reduction in the planet’s biodiversity may occur.

CONCLUSIONS

The species with the highest indication of use do not coincide with those with the highest indices of availability. Thus, some are figuring within a expectro of necessary care, considering their uses and parts that are exploited. Calculating conservation priority alone is not fully effective in predicting which species need conservation plans, and it is necessary to combine factors such as intensity, frequency and type of use with the biological variables of the resource to better determine the conservation priorities of an area.

This research shows that ethnobiological studies combined with ecological studies are basic tools and need to be carried out periodically to define adjusted conservation actions, which can mitigate possible conflicts and local conservation problems. In areas with species of known conservation priorities, a species-by-species analysis is recommended to determine all factors involved in generating impacts on plant species and local populations.

ACKNOWLEDGMENTS

To the Universidade Federal Rural de Pernambuco, the Graduate Program in Ethnobiology and Nature Conservation and the Universidade Regional de Cariri, for the logistical support in developing the study, to obtain the PhD degree. To the Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior (CAPES) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support and scholarships granted to the authors (nº 303504/2018-8).

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Publication Dates

  • Publication in this collection
    12 Nov 2021
  • Date of issue
    2021

History

  • Received
    19 Nov 2020
  • Accepted
    31 May 2021
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