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Temporal evaluation of the Conservation Priority Index for medicinal plants

ABSTRACT

We investigated, through a temporal comparison, the extraction of non-timber forest resources by quantitatively analyzing the Conservation Priority Index (CPI). The study focused on the Fulni-ô Indigenous Territory, in the municipality of Águas Belas, PE (Northeast Brazil), which is characterized by caatinga vegetation (seasonal dry forest). Information on the availability of the exploited resources and the reported use of the species were obtained from vegetation sampling and semi-structured interviews, respectively. Our results demonstrated a reduction in species richness overtime, which may be due to continued resource extraction in the area, and that some species with low densities were even more affected. The species reported as being at high risk in the current study apparently did not differ from their status in the previous study, which supports the idea that these species are most evident in this situation more for their high potential of use than for their high densities. When we associate these events together with the disappearance of some rare species, we can conclude that the CPI was not efficient in predicting changes, and that the combination of variables used with the biological variables of the species needs to be adjusted.

Keywords
biodiversity conservation; Conservation Priority Index; ethnobotany; ethnoecology; traditional ecological knowledge

Introduction

Traditional populations throughout the world appropriate of a vast diversity of plant resources to meet different demands, and they develop practices for the management and use of these resources ( Whitton & Rajakaruna 2001Whitton J, Rajakaruna N. 2001. Plant Biodiversity: an overview. In: Levin SL. (ed.) Encyclopedia of Biodiversity. San Diego, Academic Press. p. 621-630.; Albuquerque et al. 2009Albuquerque UP, Araújo TAS, Ramos MA, et al. 2009. How ethnobotany can aid biodiversity conservation reflections on investigations in the semi-arid region of NE Brazil. Biodiversity and Conservation 18: 127-150.; Ferreira Júnior et al. 2011Ferreira Júnior WS, Ladio AH, Albuquerque UP. 2011. Resilience and adaptation in the use of medicinal plants with suspected anti-inflammatory activity in the Brazilian Northeast. Journal of Ethnopharmacology 138: 238-252.). The extractive activities associated with the use of such plant resources have the potential to modify the population dynamics of species. In this context, adequate planning regarding their use is necessary in order to contribute to the conservation of natural stocks, as well as to ensure the persistence of these species for future generations ( Hamilton 2004Hamilton AC. 2004. Medicinal plants, conservation and livelihoods. Biodiversity and Conservation 13: 1477-1517.), especially for those that directly depend on them.

Several studies have attempted to explain variation in population dynamics of plant species managed by local communities, and use that information to develop methods of measuring local impact ( Marinho et al. 2016Marinho FP, Mazzochini GG, Magalhães AP, Weisser WW, Ganade G. 2016. Effects of past and present land use on vegetation cover and regeneration in a tropical dry forest. Journal of Arid Environments 132: 26-33.; Reddy et al. 2016Reddy CS, Manaswini G, Satish KV, Singh S, Jha, CS. 2016. Conservation priorities of forest ecosystems: Evaluation of deforestation and degradation hotspots using geospatial techniques. Ecological Engineering 91: 333-342.). The use of these methods has become more and more common in studies evaluating the impact caused by anthropic actions on vegetation ( Dhar et al. 2000Dhar U, Rawal RS, Upreti J. 2000. Setting priorities for conservation of medicinal plants: A case study in the Indian Himalaya. Biological Conservation 95: 57-65.; Kala 2000Kala CP. 2000. Status and conservation of rare and endangered medicinal plants in the Indian Trans-Himalaya. Biological Conservation 93: 371-379.; Dzerefos & Witkowski 2001Dzerefos CM, Witkowski ETF. 2001. Density and potential utilization of medicinal grassland plants from Abe Bailey Nature Reserve, South Africa. Biodiversity and Conservation 10: 1875-1896.; Badola & Pal 2003Badola HK, Pal M. 2003. Threatened medicinal plants and their conservation in Himachal Himalayas. Indian Forester 129: 55-68.; Dalle & Potvin 2004Dalle SP, Potvin CP. 2004. Conservation of useful plants: an evaluation of local priorities from two indigenous communities in eastern Panama. Economic Botany 58: 38-57.; Kala et al. 2004Kala CP, Farooquee NA, Dhar U. 2004. Prioritization of medicinal plants on the basis of available knowledge, existing practices and use value status in Uttaranchal, India. Biodiversity and Conservation 13: 453-469.; 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). Environmental Monitoring and Assessment 132: 189-206.; Brehm et al. 2010Brehm JM, Maxted N, Martins-Loução MA, Ford-Lloyd, BV. 2010 New approaches for establishing conservation priorities for socio-economically important plant species. Biodiversity Conservation 19: 2715-2740. ; Albuquerque et al. 2011aAlbuquerque UP, Soldati GT, Sieber SS, Lins Neto EMF, Sá JC, Souza LC. 2011a. Use and extraction of medicinal plants by the Fulni-ô Indians in northeastern Brazil - implications for local conservation. Sitientibus série Ciências Biológicas 11: 309-320.; bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.; Idohou et al. 2012Idohou R, Assogbadjo AE, Fandohan B, et al. 2012. National inventory and priorization of crop wild realtives: case study for Benin. Genetic resources and Crop Evolution 60: 1337-1352.; 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. Anais da Academia Brasileira de Ciências 85: 169-186.). Janni & Bastien (2000Janni KD, Bastien JW. 2000. Establishing ethnobotanical conservation priorities: A case study of the Kallawaya pharmacopoeia. SIDA 19: 387-398.), for example, recognized conservation priorities using the index of relative importance based on the proposal of Bennet & Prance (2000Bennet BC, Prance GT. 2000. Introduced plants in the indigenous pharmacopoeia of Northern South America. Economic Botany 54: 90-102.) to evaluate plants that have cultural use. Badola & Pal (2003)Badola HK, Pal M. 2003. Threatened medicinal plants and their conservation in Himachal Himalayas. Indian Forester 129: 55-68. aimed to highlight the available information on rare, sensitive and endangered medicinal plant species based on surveys in different scientific publications. Such impact indicators have emerged as useful tools, especially when the goal is to develop management and conservation plans for species that are of human interest, although they can possess weaknesses that compromise their reliability. For example, Albuquerque et al. (2011b)Albuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873. pointed out that the Conservation Priority Index, one of the tools used to measure impacts on medicinal plant populations, does not consider summed impacts when a species has multiple uses. In addition, when using such indicators, few studies assess their accuracy on a temporal scale.

Considering the limitations shown by some indicators of impact, as well as the need to verify their relevance on temporal scale, the present study proposes a temporal characterization for a period of seven years, using the Conservation Priority Index (CPI) as a quantitative analysis tool for assessing endangered species. The main goal of this study was to determine whether the temporal period from 2007 ( Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.) to 2014 was sufficient to detect changes in the population dynamics of medicinal species. For this investigation, we assumed that the environment experiences events of intense extraction of plant resources and that no, or almost no, conservation effort occurred during the time period.

Studies involving population dynamics report that several factors can influence the development of ecosystems, including changes to their current regeneration status leading plant populations into unknown patterns of dynamics ( Silveira & Silva 2010Silveira CS, Silva VV. 2010. Dinâmicas de regeneração, degeneração e desmatamento da vegetação provocadas por fatores climáticos e geomorfológicos: uma análise geoecológica através de SIG. Revista Árvore 34: 1025-1034.; O'Brien et al. 2012O’Brien K, Pelling M, Patwardhan A, et al. 2012. Toward a sustainable and resilient future. In: Field CB, Barros V, Stocker TF, et al. (eds.) Managing the risks of extreme events and disasters to advance climate change adaptation: A special report of working groups I and II of the Intergovernmental Panel on Climate Change (IPCC). Cambridge/New York, Cambridge University Press. p. 437-486.). The most commonly reported of these factors in the literature are climatic fluctuations and anthropic actions, the latter also including chronic anthropogenic disturbances ( Singh 1998Singh SP. 1998. Chronic disturbance, a principal cause of environmental degradation in developing countries. Environmental Conservation 25: 1-2.; Silveira & Silva 2010Silveira CS, Silva VV. 2010. Dinâmicas de regeneração, degeneração e desmatamento da vegetação provocadas por fatores climáticos e geomorfológicos: uma análise geoecológica através de SIG. Revista Árvore 34: 1025-1034.; Martorell & Peters 2005Martorell C, Peters EM. 2005. The measurement of chronic disturbance and its effects on the threatened cactus Mammillaria pectinufera. Biological Conservation 124: 199-207.; O'Brien et al. 2012O’Brien K, Pelling M, Patwardhan A, et al. 2012. Toward a sustainable and resilient future. In: Field CB, Barros V, Stocker TF, et al. (eds.) Managing the risks of extreme events and disasters to advance climate change adaptation: A special report of working groups I and II of the Intergovernmental Panel on Climate Change (IPCC). Cambridge/New York, Cambridge University Press. p. 437-486.), which can have a direct influence on forest cycles and altering the response time of plant communities ( Feeley et al. 2011Feeley KJ, Davies SJ, Perez R, Hubbel SP, Foster RB. 2011. Directional changes in the species composition of a tropical forest. Ecology 92: 871-882.). Chronic anthropogenic disturbances are continuous human actions of biomass removal from forest resources that have deleterious effects at population, community and ecosystem levels, but do not result in abrupt and complete environmental changes ( Singh 1998Singh SP. 1998. Chronic disturbance, a principal cause of environmental degradation in developing countries. Environmental Conservation 25: 1-2.; Martorell & Peters 2005Martorell C, Peters EM. 2005. The measurement of chronic disturbance and its effects on the threatened cactus Mammillaria pectinufera. Biological Conservation 124: 199-207.). These disturbances, in turn, do not represent an immediate risk to plant populations, but they have the capacity to cause changes in the biology of species, altering reproduction rates and making it difficult to re-establish plant cover ( Ribeiro et al. 2015Ribeiro EMS, Arroyo-Rodríguez V, Santos BA, Tabarelli M, Leal IR. 2015. Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. Journal of Applied Ecology 52: 611-620.; Ribeiro-Neto et al. 2016Ribeiro-Neto JD, Arnan X, Tabarelli M, Leal IR. 2016. Chronic anthropogenic disturbance causes homogenization of plant and ant communities in the Brazilian Caatinga. Biodiversity and Conservation 25: 943-956.). Assuming that the studied environment is subjected to the direct influence of anthropic action and was totally devoid of conservation efforts over time, this study aims to infer the current conservation status of species considered as conservation priorities in the first study. Given this scenario, we assume that species considered as priorities for conservation in the first period study will remain at risk, with the possible occurrence of changes in population dynamics, or even local extinction, if the extraction of plant resources continues without an appropriate management plan.

Materials and methods

Study area

The study was conducted in the Fulni-ô Indigenous Territory, located in the municipality of Águas Belas, state of Pernambuco, Northeast Brazil (9°06’45”S, 37°07’15”W), approximately 315 km from the state capital Recife ( CONDEPE/FIDEM 2006CONDEPE/FIDEM - Agência Estadual de Planejamento e Pesquisas de Pernambuco. 2006. Águas Belas: perfil municipal. Recife: Governo do Estado de Pernambuco/Secretaria de Planejamento .; IBGE 2015IBGE - Instituto Brasileiro de Geografia e Estatística. 2015. Cidades. http://www.ibge.gov.br/cidadesat/. 16 Oct. 2015.
http://www.ibge.gov.br/cidadesat/...
) ( Fig. 1). The territory of the Fulni-ô comprises three villages: the main village, which is approximately 500 m from the town, and the Ouricurí and Xixiakhlá villages, which have approximately 3,657 inhabitants and occupy a total area of approximately 11,500 ha ( FUNASA 2007FUNASA - Fundação Nacional de Saúde. 2007. Dados sobre a população Fulni-ô no ano de 2006. Recife, DSEI-PE/CORE-PE/FUNASA.; Silveira et al. 2011Silveira LMLC, Marques LR, Silva EH. 2011. Fulni-ô: história e educação de um povo bilíngue em Pernambuco. Caderno de Pesquisa, São Luís 19 : 31-41. ; CONDEPE 1981CONDEPE - Agência Estadual de Planejamento e Pesquisas de Pernambuco. 1981. As comunidades indígenas de Pernambuco. Recife: Governo do Estado de Pernambuco/Secretaria de Planejamento.). According to the climatic classification of Köppen-Geiger, the climate is semi-arid (BSh) and hot and humid, with an average temperature of 25 °C and annual precipitation of around 600 mm. The local vegetation is hyperxerophytic caatinga (dry forest).

Figure 1
Location of the Fulni-ô community in the semi-arid region of northeastern Brazil (municipality of Águas Belas, state of Pernambuco). Source: Albuquerque et al. (2011a) Albuquerque UP, Soldati GT, Sieber SS, Lins Neto EMF, Sá JC, Souza LC. 2011a. Use and extraction of medicinal plants by the Fulni-ô Indians in northeastern Brazil - implications for local conservation. Sitientibus série Ciências Biológicas 11: 309-320..

The research group's relationship with the Fulni-ô people started with the "Study Project of the Environmental and Cultural Sustainability of the Fulni-ô Medical System", which began in July 2007 and concluded in December 2008. This project was executed by the Associação Mista Cacique Procópio Sarapó (AMCPS) in partnership with the Área de Medicina Tradicional Indígena (AMTI), Project Visigus II, and with the Distrito Sanitário Especial Indígena de Pernambuco (DSEI-PE), National Health Foundation, and had as its main objectives: the development of proposals for interaction between the Fulni-ô medical system and the Subsystem of Attention to the Health of the Indigenous Peoples; identification of community and traditional strategies for the sustainability of Fulni-ô traditional medicine and presenting a Manipulation of Medicinal Plants Workshop; and valuing and strengthening the knowledge, practices and practitioners of traditional Fulni-ô medicine, among others. Through this relationship, the Fulni-ô group itself recognized a need to pursue research on environmental and cultural sustainability of their ethnicity. Given this situation, the research group resumed studies in 2014, with the purpose of continuing to develop research aimed at preserving Fulni-ô medicinal practices.

Fulni-ô ethnicity

The Fulni-ô are indigenous people who lived on the banks of the Ipanema River, which borders their indigenous territory. They were catechized and converted to Catholicism with the arrival of the Capuchins in 1685 ( Diaz 1983Diaz HJ. 1983. Os Fulni-ô: relações interétnicas e de classe em Águas Belas. MSc Thesis, Universidade Federal de Brasília, Brasília. ). They represented one of the only bilingual indigenous peoples of the Northeast Region of Brazil. Their languages are Yathee, which belongs to the Macro-Jê linguistic group, and Portuguese. Yathee is spoken daily by the community, and especially by the older members ( Diaz 1983Diaz HJ. 1983. Os Fulni-ô: relações interétnicas e de classe em Águas Belas. MSc Thesis, Universidade Federal de Brasília, Brasília. ).

The calendar of the Fulni-ô people is governed by the ritual of Ouricurí that occurs annually between the months of September and December. During this period, the entire population living in the main village and in the Xixiakhlá village move to the Ouricurí village (considered sacred by the Fulni-ô people), and the forest, which has the same name, becomes a main area for resource extraction, especially those resources destined for medicinal uses in rituals and celebrations ( Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.). Consequently, the forest is subjected to the direct impact of more than three thousand indigenous natives that transit the area and depend directly on the plant resources that are extracted there. Yathee is spoken and taught during this ritual, which represents an important means for the transmission of cosmology, history and traditional knowledge to younger generations. These cultural characteristics are protected by symbolism and secrecy adopted by the Fulni-ô, and it is practically impossible for a non-indigenous person to infer what actually happens during this ritual ( Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.; cAlbuquerque UP, Soldati GT, Sieber SS, Ramos MA, Sá JC, Souza LC. 2011c. The use of plants in the medical system of the Fulni-ô people (NE Brazil): a perspective on age and gender. Journal of Ethnopharmacology 133: 866-873 .).

Agriculture and small livestock breeds comprise the subsistence activities of the Fulni-ô people. Landowners generally do not use these areas for cultivation, preferring to lease them to a third party. As a result, only the most arid lands remain available for Fulni-ô subsistence agriculture. Several factors, such as unfavorable climatic conditions and rudimentary techniques, led to the idleness of a large part of the indigenous lands, and leading the Fulni-ô to other activities, such as handcrafts ( Silveira et al. 2011Silveira LMLC, Marques LR, Silva EH. 2011. Fulni-ô: história e educação de um povo bilíngue em Pernambuco. Caderno de Pesquisa, São Luís 19 : 31-41. ).

The Fulni-ô medical system

The Fulni-ô medical system consists of a set of knowledge and practices used for health maintenance and the prevention and treatment of diseases, according to indigenous methods ( Soldati & Albuquerque 2012Soldati GT, Albuquerque UP. 2012. A new application for the optimal foraging theory: the extraction of medicinal plants. Evidence-Based Complementary and Alternative Medicine 2012. doi:10.1155/2012/364564
https://doi.org/10.1155/2012/364564...
). Such knowledge can be found widely among the family circle, in which it is shared collectively, or remain only under the domain of traditional knowledge holders ( Souza 2006Souza LC. 2006. Documento técnico contendo os modelos explanatórios Fulni-ô (PE) sobre saúde, doença e cura, descrição etnográfica do itinerário terapêutico acompanhados e a compilação das narrativas coletada junto aos detentores de saberes tradicionais, com respectiva análise antropológica. Brasília, Área de Medicina Tradicional Indígena, Projeto VIGISUS II/FUNASA.; Soldati & Albuquerque 2012Soldati GT, Albuquerque UP. 2012. A new application for the optimal foraging theory: the extraction of medicinal plants. Evidence-Based Complementary and Alternative Medicine 2012. doi:10.1155/2012/364564
https://doi.org/10.1155/2012/364564...
). When a symptom or malaise is identified, the family circle is where the first care takes place, with diagnosis and the establishment of a therapy to cure the disease. Specialists and holders of traditional knowledge are summoned only in cases that are more complex and/or to cure diseases of their specialty. The milder diseases are usually treated with home remedies or "pharmacy remedies", but if the disease is considered severe and no success is observed in the first attempts of treatment, the indigenous people are taken to nearby cities that provide structure for more specialized treatment ( Souza 2006Souza LC. 2006. Documento técnico contendo os modelos explanatórios Fulni-ô (PE) sobre saúde, doença e cura, descrição etnográfica do itinerário terapêutico acompanhados e a compilação das narrativas coletada junto aos detentores de saberes tradicionais, com respectiva análise antropológica. Brasília, Área de Medicina Tradicional Indígena, Projeto VIGISUS II/FUNASA.). According to Souza (2006)Souza LC. 2006. Documento técnico contendo os modelos explanatórios Fulni-ô (PE) sobre saúde, doença e cura, descrição etnográfica do itinerário terapêutico acompanhados e a compilação das narrativas coletada junto aos detentores de saberes tradicionais, com respectiva análise antropológica. Brasília, Área de Medicina Tradicional Indígena, Projeto VIGISUS II/FUNASA. the Fulni-ô medical system is essentially shamanic. This is explained by the fact that its explanatory practices and models are directly related to the religion and ritual of the Ouricurí.

Legal aspects

A prior authorization by the Fulni-ô was necessary for the collection of data on their use of natural resources. For this, a Prior Informed Consent was issued, which was read and signed by the Pajé of the tribe. The research project was submitted and accepted by all institutions required by Brazilian law: National System of Ethics in Research (SISNEP, No. 50629015.9.0000.5207), National Historical and Artistic Patrimony Institute (IPHAN, No. 02000.003064/2013-11), National Research Council (CNPq, No. 84616/13), Biodiversity Information and Authorization System (SISBIO, No. 42874-1), and National Indian Foundation (FUNAI, No. 08620.031129/2014-88).

Establishment of conservation priorities

In order to identify species of conservation priority, we followed the protocol modified by Albuquerque et al. (2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.), which takes into account data on the availability of species in the environment together with data on the local uses attributed to each species. The present research considered this study as a starting point for the assessment of conservation priorities from a temporal perspective.

Information regarding the current availability of exploited resources were obtained from vegetation sampling performed between April and May 2014, in the territory belonging to the Fulni-ô indigenous people. The area sampled was exactly the same area inventoried in the initial study, since it is the only area in which non-indigenous people are permitted (see Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.). Due to its proximity to the main village, the forest experiences great pressure from exploitation, especially from September to November when the ritual of Ouricurí occurs. Because it is considered a place of collective appropriation, it suffers from unsustainable collection practices, even though it has limited access for non-indigenous people ( Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.).

The vegetation analysis was performed using the same quadrat sampling method used in the first study (see Cottam & Curtis 1956Cottan C, Curtis JT. 1956. The use of distance measures in phytosociological sampling. Ecology 37: 451-460.; Felfili et al. 2011Felfili JM, Roitman I, Medeiros MM, Sanchez M. 2011. Procedimentos e métodos de amostragem de vegetação. In: Felfili JM, Eisenlohr PV, Melo MMRF, Andrade LA, Meira-Neto JAA. (eds.) Fitossociologia no Brasil - Métodos e estudo de casos. Viçosa, Universidade Federal de Viçosa. p. 86-121.; Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.). The sites previously delimited by Albuquerque et al. (2011b)Albuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873., were demarcated with GPS and with the help of a local guide (one of the authors of Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.), aiming to define with greater precision the area in which the previous analyses were performed. One hundred quadrats were placed at each site for a total of 200 quadrats. The sampling design consisted of the creation of 10 lines of 50 m at each of two defined sites. The lines were installed perpendicular to the trails and the main roads that cross the forest, thus avoiding border areas and areas affected by the development of the city. They were spaced 10m from each other and one point was defined at each 10 m of each sampling line. The area around each point was divided into four quadrants (each with 90º) and for each quadrant, we sampled the diameter at ground level (including individuals with DNS ≥ 3 cm) for the specimen closest to the vertex of the quadrant ( Rodal et al. 2013Rodal MJN, Sampaio EVSB, Figueiredo MA. 2013. Manual sobre métodos de estudo florístico e fitossociológico - Ecossistema Caatinga. Brasília, Sociedade Botânica do Brasil.). From these data, we calculated the relative density of each species (RD), which is used to compose part of the Conservation Priority Index. In addition, in order to establish the total local diversity, botanical material was collected for species that were not included in the sample in order to include species that were not sampled in the phytosociological inventory. The species sampled were identified by their local names, according to what has already been established by Albuquerque et al. (2011b)Albuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873. in the same study area, taxonomically identified and incorporated into the collection of the herbarium Dárdano de Andrade Lima, at the Instituto Agronômico de Pernambuco - IPA ( Tab. 1).

Table 1
Current list of plants collected during the floristic inventory at the Fulni-ô Indigenous Village, Águas Belas (Pernambuco, Northeastern Brazil) with their respective local names. *Species indicated for medicinal use. Species that do not have values for absolute density (AD) and relative density (RD) are those that were not included in the sampling, and inserted in the vegetation listing in order to estimate total local diversity.

Information regarding the reported use of plant species included the data published by Albuquerque et al. (2011) Albuquerque UP, Soldati GT, Sieber SS, Lins Neto EMF, Sá JC, Souza LC. 2011a. Use and extraction of medicinal plants by the Fulni-ô Indians in northeastern Brazil - implications for local conservation. Sitientibus série Ciências Biológicas 11: 309-320. from 344 interviews conducted in 2007, representing the first period of study, and data referring from 396 interviews conducted between the years of 2014 and 2015, representing the current sample and the second period of study. This representative sample was divided among the regions of the village, according to the area served by each health agent, in order to include all 14 regions of the indigenous territory. Semi-structured interviews were performed, in which people were asked about plants known for medicinal use, as well as the therapeutic targets that are treated with the use of those plants. All interviews were conducted in the company of an indigenous person to facilitate communication between the researchers and the interviewees, and provide help in translating of some of the plant names that were often known only in the native language of Yathee.

For determining conservation priorities of medicinal plants, we used the Conservation Priority Index (CP), which takes into account a biological score (BS) and a risk of use score (RU) for the species. This technique was initially developed by Mander et al. (1997Mander J, Quinn N, Mander M. 1997. Trade in wildlife medicinals in South Africa. Pietermaritzburg, Institute of Natural Resources Investigational Report No. 154, INR.), first employed by Dzerefos & Witkowski (2001Dzerefos CM, Witkowski ETF. 2001. Density and potential utilization of medicinal grassland plants from Abe Bailey Nature Reserve, South Africa. Biodiversity and Conservation 10: 1875-1896.) and later adapted by Albuquerque et al. (2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.). The criteria used in the calculation are explained in Table 2. Conservation priority was calculated based on the formula: CP = 0.5 (BS) + 0.5 (RU).

Table 2
Criteria used for scoring the relative density, collection risks, local importance and diversity of use of medicinal plants (modified by Dzerefos & Witkowski 2001Dzerefos CM, Witkowski ETF. 2001. Density and potential utilization of medicinal grassland plants from Abe Bailey Nature Reserve, South Africa. Biodiversity and Conservation 10: 1875-1896. and Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.).

The Biological Score (BS) was calculated based on the relative density of each taxon: BS= D x 10, where D corresponds to the value obtained based on the relative density of each taxon (DRi) scored according to Table 2. For the calculation of the relative density, undamaged individuals were included as well as those that were partially cut, however, still in condition to offer products.

The highest value between the local importance (L) and the diversity of use (V) determined the value of use (U), which together with the value of the collection risk (H) provided the Risk of Utilization Score (RU) that reaches the maximum value of 100. The Risk of Utilization Score (RU) is calculated by the following formula: RU = 0.5 (H) + 0.5 (U) x 10. The value of the collection risk (H) is based on the biological consequences caused during collection, according to the part of the plant that will be removed ( Tab. 2). The value of local importance is determined by the percentage of the number of informants who indicated a particular species as medicinal, and the diversity of use (V) is related to the uses attributed to the species, with scores varying from 1 to 10 ( Tab. 2).

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). Environmental Monitoring and Assessment 132: 189-206.) suggest that there are limitations in the calculation of conservation priorities, since the formula used does not take into account other uses of medicinal plants that may be potentially more harmful. In order to take into account the observations made by Oliveira et al. (2007)Oliveira 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). Environmental Monitoring and Assessment 132: 189-206., Albuquerque et al. (2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.) added 10 scores into the variable "associated timber uses" (AT), which takes into account the multiple uses of woody medicinal plants used by the Fulni-ô, resulting in additional pressure on them. The new formula is presented as follows: PC = 0.5 (BS) + 0.5 (RU) x 10, with timber use being included only when the species presents this type of associated use. The data used to calculate the Risk of Utilization Score (RU) and Biological Score (BS), were extracted from the work of Albuquerque et al. (2011b)Albuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873..

The Conservation Priority Index was calculated for each of the sampled species. The score allowed the classification of medicinal plants into three categories: Category 1, CP ≥ 80, in which species of high priority for conservation were included, and for which collection should be performed by applying sustainable alternatives; Category 2, < 80 CP > 60, which includes species with potential to be collected according to location and specific quotas; and Category 3, CP ≤ 60, which are species suitable for high impact collection.

Data analysis

In order to test for significant differences among the Conservation Priority Index scores, we used the Wilcoxon test. This statistical analysis was used in order to evaluate the dynamics of the species reported as having some medicinal use, considering the values obtained in the two study periods, without taking into account segregation by categories of risk, as this is implemented in the Conservation Priority Index itself. Using the same type of test, and focusing on the same objective of the previous analysis, we performed an analysis for each risk category (≥ 80; < 80 > 60 and ≤ 60) between the scores of the first (2007) and the second (2014) periods of study.

In order to assess species richness in general, as well as richness of species reported to have medicinal use, we performed a chi-square test on contingency tables. All tests mentioned above were performed using the software Bioestat 5.3 ( Ayres et al. 2007Ayres M, Ayres JRM, Ayres DL, Santos AS. 2007. BioEstat 5.3. Aplicações estatísticas nas áreas das ciências biológicas e médicas. Belém, Sociedade Civil Mamirauá.), and p < 0.05 were considered significant.

Results

Species richness

The current survey sampled 34 species, of which 19 of were indicated as having medicinal use. Albuquerque et al. (2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.) recorded 44 species with 25 of medicinal use. Although the two samples were not significantly different statistically, there was a decrease in total richness and richness of medicinal plants (x² = 0.002, p = 0.8835). Ten species previously cataloged were not present in the current sampling, among which are eight heliophytes, which were already in low densities in the previous study: Spondias tuberosa, Caesalpinia leiostachya, Chorisia sp ., Croton heliotropifolius, Ditaxis malpighiacea with indications of medicinal use, and Acacia bahiensis, Enterolobium contortisiliquum, Ptilochaeta bahiensis, Ruprechtia laxiflora and Cardiospermum sp . with indications of medicinal. The other two species, Anemopaegma sp. and Capsicum parvifolium, are ombrophylous, and were also present in low densities in the previous study.

This reduction in species richness, indicating the disappearance of some species, may be the result of the continued extraction of resources in the indigenous territory since no management action has been implemented in the region in recent years.

Conservation Priority Index and risk categories

There were seven species (28 %) in the high-risk category of the previous study and five (26.31 %) in the current study, while 12 species (48 %) were in the medium-risk category in the previous study and nine (47.36 %) in the current study. Only six species (24 %) were in the low-risk category of the previous study and five (26.31 %) in the current study. Three species, Maytenus rigida, Chloroleucon foliolosum and Commiphora leptophloeos, moved to lower risk categories between the two study periods. Since these species did not exhibit pronounced changes in their relative densities, this change is likely due to a reduction in their use. In turn, two species, Ruellia asperula and Piptadenia stipulaceae, moved to higher risk categories. Ruellia asperula experienced an increased CP score due to a decrease in its density, while Piptadenia stipulaceae had an increase because of an increase in the number of people who reported it as medicinal, thereby increasing its use value ( Tab. 3).

Table 3
List of medicinal plants sampled in the Ouricuri Forest, Fulni-ô Indigenous Village, Águas Belas, Pernambuco. T1: corresponds to the first study in the year 2007; T2: corresponds to the second study in the year 2014; NI = number of individuals; RD = relative density; CR = collection risk; LI = local importance; NU = number of medicinal uses; DU = diversity of medicinal uses; VU = value of use; and CP = conservation priority index.

Regarding the species that did not exhibit changes in their CP score between the previous study and the current study, we can infer the following: the species considered high-risk remained so because of their reputation as species of wide local use. These species are: Anadenanthera colubrina, Myracrodruon urundeuva, Cynophalla hastata and Lippia gracilis. In general, these species are not present in high densities, but have been able to withstand significant impact from collection, because in addition to being used medicinally, they also have associated timber uses. The species of the medium-risk category that remained so ( Schinopsis brasiliensis, Mimosa tenuiflora, Guapira noxia, and Ziziphus joazeiro) exhibited only a small decrease in the number of individuals, as well as the number of attributed uses, although not significantly enough to influence the final value of the CP score. The species of the low-risk category that remained so ( Poincianella pyramidalis, Bauhinia cheilantha and Aspidosperma pyrifolium) exhibited a completely different situation from the species in the other categories that did not change. These species possessed high relative densities along with a high number of specimens in both the previous and current studies, and were also reported as of low local importance, being listed by less than 25 % of the informants.

The current CP scores of each species in each group (high, medium and low risk) were not significantly different from the previous scores. Thus, for high-risk (t = 1.3432, p>0.05) and medium-risk (V=2, p>0.05) and low-risk species (V=2, p>0.05), the CP scores remained the same. These results show that, in general, changes of little significance occurred over the years, both regarding relative densities and potential uses.

Discussion

Considering that one of the aims of this work was to perform a temporal comparative analysis, it is important to emphasize that the current study followed the same protocols used in the previous study. The results demonstrate a temporal reduction in the number of species, suggesting over-exploitation of the area over the seven year period, and that some species that were already present at low densities were even more affected, perhaps by an increase in use as medicinal plants, or perhaps because of other categories of use. The literature points out that most medicinal plants exploited by local communities in the caatinga also have other associated uses ( Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.; Lucena et al. 2007Lucena RFP, Araújo EL, Albuquerque UP. 2007. Does the local availability of Woody Caatinga plants (Northeastern Brazil) explain their use value? Economic Botany 61: 347-361.). Considering this, it seems that a technique that does not take into account uses other than medicinal uses, tends to underestimate the pressure on these populations, causing error in the measurement of impact. Gaoue & Ticktin (2007Gaoue OG, Ticktin T. 2007. Patterns of harvesting foliage and bark from the multipurpose tree Khaya senegalensis in Benin: Variation across ecological regions and its impacts on population structure. Biological Conservation 137: 424-436.) argued that species may be affected by a combination of different exploitive events, or by the level of damage to individuals or to the population. These exploitive events could be occurring in the study area, since there is a variety of reported uses other than just medicinal. This diversity of exploitive events can contribute to increased extractive pressure and cause much more damage when executed simultaneously ( Albuquerque et al. 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.).

The species found to be at high-risk in the current study apparently did not experience changes in their CP scores since they are the same species that were high-risk in the previous study. This can be interpreted to be more of a result of their high use potential, than by their densities, which vary from intermediate to high, according to the CP. Thus, it is believed that these populations will persist due to their local abundance, even if the levels of extraction continue to increase beyond the support capacity of the populations. Studies, such as Albuquerque et al. (2007Albuquerque UP, Medeiros PM, Almeida ALS, et al. 2007. Medicinal plants of the caatinga (semi-arid) vegetation of NE Brazil: A quantitative approach. Journal of Ethnopharmacology 114: 325-354.; 2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.) and Souza et al. (2016Souza AS, Souza APB, Lucena RFP. 2016. Relative importance of medicinal plants in the Semi-Arid Region of Paraíba: a case study in the Municipality of Congo (Paraíba, Northeast Brazil). Brazilian Journal of Biological Sciences 3: 83-86.), help us understand this scenario, by showing us that some species of the caatinga with relatively high importance, and consequently a high number of indications of therapeutic use, also reach great densities, as is the case of Myracrodruon urundeuva and Sideroxylon obtusifolium. Nonetheless, it is necessary to immediately develop strategies so that these populations will not become locally extinct in the near future, by proposing means for their sensible use within the capacity of their continued persistence.

Other factors that may influence CP are those that contribute to the distribution of the species, such as genetic and demographic variation, which regulate population size. Albuquerque et al. (2011bAlbuquerque UP, Soldati GT, Sieber SS, Medeiros PM, Sá JC, Souza LC. 2011b. Rapid ethnobotanical diagnosis of the Fulni-ô Indigenous Lands (NE Brazil): floristic survey and local conservation priorities for medicinal plants. Environment, Development and Sustainability 133: 866-873.) suggested that the dynamics of species used in the region need to be carefully studied, since some species tend to be highly valued due to the influence of the weight of some specific variables on the calculation of their CP. For example, Parapiptadenia zehntneri and Cynophalla flexuosa were considered species of conservation priority, having been allocated to Category 1 (CP ≥ 80). However, these species were observed exist in naturally low relative densities in both the previous and current studies, which increases their CP score to the "rare" category. On the other hand, variables considering use of these species were considerably low, which allows us to assume that these species were listed as priority for conservation due to their normal pattern of distribution in nature.

The strong indications of human presence in the area over the years, accompanied by intense and continuous extractive activity, may have led to the observed decrease in species richness between the two study periods. Ribeiro et al. (2015Ribeiro EMS, Arroyo-Rodríguez V, Santos BA, Tabarelli M, Leal IR. 2015. Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. Journal of Applied Ecology 52: 611-620.) found that even low-intensity disturbances, known as chronic anthropogenic disturbances, may have the potential to cause marked effects on plant communities by altering their richness. Activities involving the harvesting of leaves, fruits and bark for medicinal purposes usually do not result in abrupt changes of the environment. However, the continuous nature of their exploitation does not seem to allow populations and ecosystems to recover, causing reductions in the density of stems, basal area, species richness and community uniformity, thereby favoring species adapted to disturbances ( Sagar et al. 2003Sagar R, Raghubanshi AS, Singh JS. 2003. Tree species composition, dispersion and diversity along a disturbance gradient in a dry tropical forest region of India. Forest Ecology and Management 186: 61-71.; Ribeiro et al. 2015Ribeiro EMS, Arroyo-Rodríguez V, Santos BA, Tabarelli M, Leal IR. 2015. Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. Journal of Applied Ecology 52: 611-620.).

Although the collection of non-timber forest resources appears to be less damaging to ecosystems than the collection of actual timber, there are indications that excessive collection of bark, fruit and leaves may have consequences for plant populations, including, theoretically, a decrease in reproduction rates ( Gaoue & Ticktin 2007Gaoue OG, Ticktin T. 2007. Patterns of harvesting foliage and bark from the multipurpose tree Khaya senegalensis in Benin: Variation across ecological regions and its impacts on population structure. Biological Conservation 137: 424-436.; Baldauf & Santos 2013Baldauf C, Santos FAM. 2013. Ethnobotany, traditional knowledge, and diachronic changes in non-timber forest products management: a case study of Hymatanthus drasticus (Apocynaceae) in the brasilian savanna. Economic Botany 67: 110-120.; 2014Baldauf C, Santos FAM. 2014. The effect of management systems and ecosystem types on bark regeneration in Hymatanthus drasticus (Apocynaceae): recommendations for sustainable harvesting. Environmental Monitoring Assess 186: 349-359; 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: 341-349.; Gaoue et al. 2013Gaoue OG, Horvitz CC, Ticktin T, Steiner UK, Tuljapurkar S. 2013. Defoliation and bark harvesting affect life-story traits of tropical tree. Journal of Ecology 101: 1563-1571.). This reality is especially noticeable in seasonally dry forests in Brazil, wherein leaves and fruits are not available all year round. Given this situation, rural populations began to collect resources that were always available, such as the bark of the stem and roots ( Albuquerque 2006Albuquerque UP. 2006. Re-examining hypotheses concerning the use and knowledge of medicinal plants: a study in the Caatinga vegetation of NE Brazil. Journal of Ethnobiology and Ethnomedicine 2: 30.). There are indications that the excessive collection of these resources is causing a decrease in plant richness of some ecosystems, mainly due to the death of some individuals with larger stem diameters that are more frequently subjected to collection ( Soldati & Albuquerque 2011Soldati GT, Albuquerque UP. 2011. Impact assessment of the harvest of a medicinal plant ( Anadenanthera colubrina (Vell.) Brenan) by a rural semi-arid community (Pernambuco), Northeastern Brazil. International Journal of Biodiversity Science, Ecosystem Services & Management 1: 1-13.; 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. Journal of Etnhobiology and Ethnomedicine 10: 64.).

In associating the evidence of excessive collection with the disappearance of some rare species, we can conclude that CP was not effective at predicting changes, thus indicating that the combination of use variables and biological variables needs to be better determined. Based on this evidence, as well as the statistical analyses performed, it can be said that CP has not been reliable at determining species conservation priority. Therefore, it is recommended that a species-by-species level analysis be performed to determine all of the factors involved in measuring impacts on plant populations.

Acknowledgements

We would like to thank the Fulni-ô people for their hospitality, solicitude and valuable exchange of knowledge. We are also grateful to the following organizations and individuals: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for its support for this research; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the productivity grant awarded to UPA; and members of the Laboratory of Ecology and Evolution of Social-Ecological Systems for their contributions to this study.

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Publication Dates

  • Publication in this collection
    02 May 2017
  • Date of issue
    Apr-Jun 2017

History

  • Received
    20 Jan 2017
  • Accepted
    22 Feb 2017
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
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