RESEARCH ARTICLE

Ethnobiology and Conservation 2020, 9:28 (01 July 2020) doi:10.15451/ec2020­05­9.28­1­13 ISSN 2238­4782 ethnobioconservation.com Traditional management of Cactaceae by local populations in the semi­arid region of Brazil Kamila Marques Pedrosa1*; Sérgio de Faria Lopes1; Thamires Kelly Nunes Carvalho2; Camilla Marques de Lucena3; Ailza Maria de Lima­Nascimento4 and Reinaldo Farias Paiva de Lucena2*

ABSTRACT

Cactaceae species are important resources in the semi­arid region of Brazil and have been used and managed in a specific way by farmers to optimize and ensure the availability of cacti to rural communities. Thus, this study aimed to investigate management techniques used by residents of four rural communities in the municipality of Cabaceiras, Paraíba, Northeast Brazil. Only residents who claimed to perform some type of cacti management participated in this study, totaling 17 informants. Pilosocereus gounellei (F.A.C. Weber) Byles & Rowley subsp. gounellei, Cereus jamacaru DC. subsp. jamacaru, Pilosocereus pachycladus F. Ritter, Tacinga palmadora (Britton & Rose) N.P. Taylor & Stuppy, and Melocactus zehntneri (Britton & Rose) Luetzelb. Ex situ and in situ management techniques were recorded. The first one performed by transplantation of propagules and the second one by tolerance. The species propagation is carried out using shoots and vegetative parts. Of the species identified, only Cereus jamacaru subsp. jamacaru has more than one form of management. In addition to management, informants use rudimentary techniques such as burning the vegetative parts for fodder purposes.

Keywords: Caatinga; Traditional knowledge; Ethnobotany.

1* State University of Paraíba, Department of Biology, Campina Grande, Paraiba, Brazil.

2* Federal University of Paraíba. Exact and Natural Sciences Center. Department of Systematics and Ecology. Laboratory of Ethnobiology and Environmental Sciences. Campus I. João Pessoa, Paraíba, Brazil.

3* UNIESP University Center, Cabedelo, Paraíba, Brazil.

4 Federal University of Pernambuco, Biological Science Center, Recife, Pernambuco, Brazil. * Corresponding author. E‐mail address: KMP ([email protected]), SFL ([email protected]), TKNC ([email protected]), AMLN ([email protected]), RFPL ([email protected]).

SIGNIFICANCE STATEMENT

Throughout the dry season, species of cactus are one of the most important food sources used by the farmers to feed their animals. To understand the management of these species, it is important to support conservation practices, which approach local interests in an unpredictable future. In our study, we show how human groups managed species in domestic and natural environments. Investigations of traditional management can contribute to the discussion about plant domestication and conservation. Understanding how these people use and manage cactus species is also important because, due to climate change, these plants have been in demand for constant use, which may put them at imminent risk of local extinction.

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INTRODUCTION the time of land preparation and even after its preparation; [2] protection – it is based on The northeast region of Brazil is mostly practices such as removal of competitors, characterized by semi­arid climate and pest control and protection against occurrence of xerophytic vegetation (Sbrissa environmental effects; [3] promotion – et al. 2012), but despite these limiting practices that make possible the species environmental conditions, it is home to more population development, consisting of than 28 million people, most of them living in propagation of vegetative parts or seeds, rural areas (Silva et al. 2017). The use and and/or by pruning; [4] cultivation – occurs in management of plant resources, available for both wild and ex situ managed populations. various purposes (fodder, medicinal, rural The cultivation is carried out using seeds, constructions, and food), are common and vegetative parts or transplantation of young necessary for residents of rural communities plants to environments directly managed by (Lucena et al. 2015). Recent studies have the people; this practice is classified as ex frequently recorded the use of Cactaceae situ management (Casas et al. 1997a; species in this region of Brazil (Lucena et al. González­Insuasti and Caballero 2007). 2012, 2013, 2015; Lucena et al. 2017). Thus, there is a need to study the forms of Ethnobotanical and domestication studies management involving useful Cactaceae on these species have investigated the species, performed by rural communities in capacity of human activity to influence their the semi­arid region of Brazil, considering availability, considering their genetic and that each technique may interfere in different ecological aspects as a function of the use of ways and degrees of complexity with the different management practices (Apodoca environment and managed resource (Lucena 2001; Casas et al. 2001; Fuentes 2005; 2018). Furthermore, understanding how Fernández­Alonso 2006; Blancas et al. 2010; human experience contributes to the Lucena et al. 2012, 2013, 2015). development of strategies for using plants The understanding of the term may be useful in developing plans for management consists of intentional activities exploiting and conserving biodiversity. This (or not), which are practiced with the assertion is reinforced by the cultural and objective of maintaining or modifying a utilitarian importance of Cactaceae species, system and/or its elements (Gepts 2004). which are threatened with extinction due to Such activities may involve the use, indiscriminate exploitation, land use and conservation or restoration of a resource or occupation in Brazil and other regions of the environment (Casas and Parra 2016a). world (Martorell et al. 2012). Certain Cactaceae species are managed by Thus, this study aimed to investigate the human populations, specifically by selecting interest in traditional management specimens with characteristics that meet the techniques of Cactaceae species, between demand for consumption (Casas et al. 2001), residents of four rural communities in the and this occurs both in natural environments semi­arid region of Paraíba, northeastern (in situ) and outside them (ex situ) (Casas et Brazil. al. 2001, 2006). The in situ management has been characterized in [1] tolerance – when the resource is maintained in its environment at

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MATERIAL AND METHODS the Federal University of Paraíba. All participants signed the Free and Informed Study area Consent Form (ICF), allowing the publication of the obtained ethnobotanical information. This research involved residents of the rural communities of Tapera, Caiçara, Rio Ethnobotanical data Direito, and Caruatá de Dentro, located in the municipality of Cabaceiras (07º29´20´´S The study communities were selected due and 36º17´14´´O), state of Paraíba, to the fact there were family ties between northeastern Brazil (Figure 1). This one of the researchers and the communities’ municipality is 167 km from the state capital residents, which contributed to greater (João Pessoa), about 300 meters above sea access and reliability to obtain information level, accounting for a population of 5,035 from the respondents. It was not possible to inhabitants, of which 2,217 live in the urban interview all residents because some of them area and 2,818 in the rural area (IBGE were sick and others were absent when 2010). researchers visited their homes. The non­ The study area has a Bsh climate, hot participant observation technique was used semi­arid (Álvares et al. 2013), and annual to identify residents who performed the rainfall between 350 and 600 mm, highly traditional management of cacti variable in space and time (Moro et al. (Albuquerque et al. 2014). The data were 2015). The annual mean temperature is collected between November 2016 and 26°C, with minimum values in July and November 2017, using semi­structured August and maximum values in November questionnaires with specific questions about and December (Nascimento and Alves the management of Cactaceae species 2008). These climatic conditions determine a (Lucena et al. 2015). The questionnaire seasonally dry tropical forest (SDTF) addressed questions on the use, knowledge, vegetation, with physiognomic variety and and management of Cactaceae (e.g., What endemic biodiversity (Silva et al. 2017). The cacti do you use? Do you grow any cactus? region is characterized by the occurrence of How is the planting performed? Where do plant species physiologically and you collect the plants? What is the care for morphologically adapted to the weather the development of the plants?). conditions, such as trees and shrubs, with In situ and ex situ management small leaves, and twisted thorny stems, and categories (Casas 1997a, 2007, 2014; succulent species (Queiroz et al. 2017). Blancas et al. 2010) were considered to analyze how local populations perform Data collection traditional management techniques. Thus, in situ management may be performed through Legal and ethical aspects [1] collection (obtainment of useful plant parts), [2] tolerance (non­removal of wild This study was carried out after being plants from areas used for agropastoral approval (CEP/HULW No. 297/11) by the activity), [3] induction (propagation through Health Committee’s guidelines and vegetative parts of specimens of a given regulations (Resolution 196/96), through the population), and [4] protection (desirable Ethics and Research Committee (CEP) of plants are protected through management

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Figure 1. Location map of the municipality of Cabaceiras, Paraíba, northeastern Brazil. Photo: Diogo Fonseca (2020). practices), and ex situ management through de Dentro. The residents of the communities artificial propagation or planting (removal of of Tapera and Caiçara are farmers (men and vegetative parts of plants from their natural women) who have performed economic environment to anthropogenic areas) and activities focused on rural tourism and transplantation (removal of the whole plant associated with the “Pai Matheus” Farm for planting in a controlled environment). Hotel, which is included in the rural tourism Only residents who claimed to perform some cultural route in the region. Farmers are type of cacti management participated in this registered in the Rural Workers’ Association study, totaling 17 informants (15 men and 2 of Tapera. They are visited monthly by a women). All species cited by the informants health agent and have access to medical were collected, herborized, identified, and care. There is no school in these deposited in the Herbarium “Jaime Coelho communities and students are transported to de Morais” of the Federal University of attend classes in the urban center of Paraíba, Campus II, Areia, Paraíba, Brazil. Cabaceiras. In Tapera, there is a catholic chapel. The communities of Rio Direito and Socio­economic description of rural Caruatá de Dentro have family health care communities and are visited monthly by a health agent, who monitor the residents. The people in There are 14 residences in Tapera, 6 in these communities use a room as a medical Caiçara, 8 in Rio Direito, and 18 in Caruatá center with biweekly appointments. There is

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a public elementary school in these Pilosocereus gounellei (F.A.C. Weber) Byles communities (Municipal School of Primary & Rowley subsp. gounellei are planted by Education “Maria Neuly Dourado”). Primary eight and seven informants, respectively, and and secondary students take a school bus to only two people reported planting attend classes in Cabaceiras. These Melocactus zehntneri (Britton & Rose) communities have two Rural Associations Luetzelb. and Tacinga palmadora (Britton & managed by different political Rose) N.P. Taylor & Stuppy (Table 1). representatives, in addition to a Catholic Cereus jamacaru subsp. jamacaru is the church. only species managed in wild environments through tolerance. This fact is confirmed Data analysis mainly by the non­intentional removal of specimens, as the residents remove other The qualitative data obtained were plant species from agricultural environments analyzed through the interviewees’ discourse but leave C. jamacaru subsp. jamacaru. interpretation (Mourão and Nordi 2003), Also, transplantation of propagules may based on the diverse individual competences occur in environments controlled or disturbed union model (Hays 1976), which consists of by anthropogenic activities. In both considering all the information provided by situations, C. jamacaru subsp. jamacaru the interviewees. Information was grouped specimens are maintained as a form of by theme and used to interpret the results planning for future uses. and to ground aspects of the discussion. The specimens identified by the residents in ex situ environments are propagated by RESULTS transplantation, using the vegetative part or the entire plant, which are subjected to Forms of management were recorded for special care for their development (Table 1). five species, which are prone to some kind of Some species, such as M. zehntneri, anthropogenic interference in natural (in situ) were recorded as transplanted from young or domestic (ex situ) environments. plants (shoots). P. pachycladus and T. Regarding the type of propagation, the palmadora are also removed from their informants explained they perform this natural habitat to be planted near the practice by removing vegetative parts residences, in fences or edges of agricultural (cladodes) and/or individuals in the fields for ornamental purposes. P. gounellei regeneration process (shoots) (Table 1). No subsp. gounellei specimens are planted by collection, induction, promotion, and the propagation of vegetative parts protection management were recorded in (cladodes) in soil erosion areas for natural environments. Only Cereus jamacaru stabilization; thus, these plants are used in DC. subsp. jamacaru (mandacaru) has more the recovery of degraded areas. than one form of management. Regarding Some measures necessary for planting the collection, there is a preference for some were mentioned as factors that favor plant areas, such as yards, live fences, and areas growth. For C. jamacaru subsp. jamacaru, for agropastoral activity. e.g., damaged cladodes and those with signs All the informants reported planting of diseases are removed to prevent Cereus jamacaru subsp. jamacaru. contamination, and then the undamaged and Pilosocereus pachycladus F. Ritter and healthy ones are planted. P. gounellei subsp.

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Table 1. Legend: Species and their respective management recorded in the rural communities of Caiçara, Tapera, Rio Direito, and Caruatá de Dentro in the municipality of Cabaceiras, Paraíba, Northeast Brazil. Use categories: Ct = construction; Fo = food; Fu = fuel; Fd = fodder; Me = medicinal; Ot = other uses; Tc = technology. Forms of management: *TP = Transplantation of Propagules; T = Tolerance. Types of propagation: VP = Vegetative Part; S = Shoots.

gounellei and M. zehntneri have their and domestic animals, which may impede vegetative parts removed for planting and P. the development of cacti, was another pachycladus planting is performed using recorded form of ex situ management. shoots. Another technique consists of letting Moreover, the informants use rudimentary the cacti vegetative part wither to be later techniques such as the burning of cacti in planting in dry soil. The cacti cannot be natural areas to optimize the collection and planted in moist soil, because they do not facilitate fodder preparation for domestic withstand these conditions for its animals. Thirteen people burn these plants development. and four do not burn them because they rear After planting, some people perform ex no domestic species or because they buy situ management, a technique that helps in processed feed from industries. P. gounellei the development and protection of the subsp. gounellei is one of the most used species. The reports show that the residents species (14 use citations), followed by C. have adopted practices that influence the jamacaru subsp. jamacaru (13 use citations), number of specimens, subjecting them to P. pachycladus (8 use citations), and T. conditions that contribute to their palmadora (2 use citations) for fodder development after planting, such as the use purposes. of water for the growth of the planted ones. With regards to preferences, farmers The use of a drip irrigation system was prefer to burn the cacti, partially cutting the recorded in the communities, irrigating an branches, e.g., young branches, or burning area of Opuntia ficus­indica (L.) Mill., used as all branches or even the entire plant. Young fodder, and also benefiting some C. cacti are selected to be cut since they have jamacaru subsp. jamacaru specimens non­lignified stems. C. jamacaru subsp. (Figure 2), which, according to the jamacaru specimens are not burnt, but their informants, would also be used for fodder vegetative parts may be partially or fully cut. purpose in the future. Regarding cacti preparation for fodder In the dry season, the cacti near the purposes, some informants burn the residences are irrigated with water reused cladodes of all the species collected. For from household chores. Elimination of pests this, they use “coivaras”, which are fires

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Figure 2. Vegetative propagation irrigated by dripping in the community of Tapera (Cabaceiras, Paraíba, northeastern Brazil). A: Pilosocereus pachycladus F. Ritter in natural areas for fodder purpose; B: Plantation of Cereus jamacaru DC. subsp. jamacaru and Pilosocereus pachycladus F. Ritter in live fences; C: Plantation of Opuntia ficus­indica (L.) Mill.; D: Associated cultivation of Opuntia ficus­indica (L.) Mill. and Cereus jamacaru DC. subsp. jamacaru Photo: Kamila Pedrosa, 2017. made of species native to the Caatinga; then species, the residents collect them three they take the animals to feed in the place times a day, on average, and/or every day. where species were burnt or take the burnt species to feed the animals near the DISCUSSION residences (Figure 3). The species subjected to burning are The studied species are managed with a collected in rangelands (near the focus on the quality and maintenance of residences), small mountains, close to rivers, plants, as there is no evidence that people, small vegetable garden, and in areas of in that region, perform traditional native vegetation, with different frequencies management in search of a specific of collections according to the available time objective. These nuances are investigated in of each farmer; collections may be different ways through the socio­ecological performed only on weekends or every day. context of the populations (Casas et al. Depending on the abundance of species 2016b). In this way, local management and their respective uses, some collection characteristics indicate a continuous use of areas become the most preferred by the available species to meet current demands. locals. P. gounellei subsp. gounellei and C. The informants have no interest in caring jamacaru subsp. jamacaru are often for the cacti in the wild area; however, they collected; due to more frequent use of these are careful not to cut the entire cactus so that

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Figure 3. Pilosocereus pachycladus F. Ritter specimens subjected to burning for fodder purpose in the rural communities of Tapera, Caiçara, Caruatá de Dentro, and Rio Direito (Cabaceiras, Paraíba, northeastern Brazil). A: Burning performed by a resident; B: Animals feeding on burnt plants in loco; C: Use of a wheelbarrow to take the burnt vegetative parts to near the residence. Photo: Ribamar Lima and Thamires Carvalho, 2017. it can regenerate. Nevertheless, cutting residences, rather than to manage them in management of cladodes, recorded in our natural areas of difficult access. The study, may be associated with some type of propagation of young plants is appreciated management for protection, as it was found by people, as it is more likely to guarantee in Mexico (Casas et al. 1997b, 2014, 2017). the development of specimens. However, the Concomitantly, informants’ awareness of removal of young cacti for planting is parsimoniously using the cacti in natural motivated by their availability near the areas is considered in the literature as residents but it can be a limiting factor for the “tolerance management” (Casas et al. survival of these plants in natural 2014). The tolerance management is typical environments (Godínez­Álvarez et al. 2005). of semi­arid regions, due to conservation Moreover, when people select vegetative activities and socio­cultural value of cacti for parts for planting, non­relevant semi­arid populations, mainly for animal characteristics for plant development are feed. excluded. This selective process, over time, The techniques used for the management may influence the frequency of specimens of these species are similar to those used for resistant to the attributes non­selected by in situ management found in the literature people, as recorded for some columnar cacti (Casas et al. 1999, 2001, 2007). This fact native to Mexico (Casas et al. 2016b). leads us to reflect on the importance of cacti The management techniques performed management to local populations since they near the residences optimize the use of the prefer to plant these plants near their resource, causing the residents to spend

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less energy when collecting the species, and today, there is a concern regarding the maximize cactus’ utilitarian functions, both synergism between the different chronic because of the number of specimens anthropogenic disorders in the face of available next to the people and for ensuring climate changes (Rito et al. 2017). It is forage production (Alves et al. 2017; assumed that climate change can influence Albuquerque et al. 2019). periods of intense drought in the semi­arid Collection areas are associated with the region, which therefore implies the abundance of species and their respective distribution of these species (Bellard et al. uses, becoming the areas most preferred by 2012). Adverse environmental conditions locals. In the study communities, cacti are may increase the recurrence of traditional collected for fodder purposes, in areas management of cacti or affect their use by ranging from a more preserved vegetation to human populations (Lima­Nascimento et al. nearby residences. 2019). On the other hand, there is evidence that Cereus jamacaru subsp. jamacaru is the collection areas may be related to the type of farmers’ favorite species of cacti, since it resource used and the social characteristics morphologically differs from other species of of rural communities, bearing in mind that the Caatinga, presenting a larger size and food plants are usually consumed near areas fewer thorns, making its management easy, where people develop agricultural activities in addition to being palatable for cattle, (Cruz et al. 2013). Moreover, the frequency goats, and sheep (Lucena et al. 2015; of use in collection areas is related to the Lucena 2018). It is noteworthy that the practicality and the number of domestic techniques used in the management of C. animals to be fed, as reported by Lucena et jamacaru subsp. jamacaru, in other semi­arid al. (2015), Carvalho et al. (2019), and Lima­ regions, have led to incipient domestication Nascimento et al. (2019), in studies processes of this species (Lucena 2018). conducted in the semi­arid region of Brazil. Reflecting on the importance of the The predominance of the use of these residents for maintaining local populations of species is influenced by seasonality, which native species of Cactaceae in the study limits the productivity of animal feed (Santos area, and on how these people influence et al. 2010). Thus, in semi­arid regions of cacti management and conservation, it can Brazil, there is a fluctuation in the use and be stated that some species with valorization of species during dry seasons. characteristics that meet the demand of use Under these conditions, local populations are reproduced and consequently can have used strategies such as burning contribute as an alternative for the local cladodes of cacti where they are found, and conservation of these species, corroborating this practice has reduced the time to the studies by Rangel­Landa et al. (2017) transport animal feed by local populations; and Pedrosa et al. (2018). These authors although, intense daily use causes stress recorded the importance of maintaining and physiological limitation in cacti, important useful species, which contribute to especially in the Caatinga, as the species the maintenance of their future availability are sensitive to any anthropogenic changes and therefore consisting of an alternative to (Cavalcante and Resende 2007). conservation since it would no longer be Burning techniques may cause serious necessary to remove the resource from its damage to the caatinga vegetation and, natural environment.

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The management practices recorded in Cereus jamacaru subsp. jamacaru has more this study show how much the efficacy of use information regarding care and uses. and availability related to the forms of However, the management by burning allocation, determined by residents, are techniques stands out as the main way of important criteria for selecting strategies of providing fodder throughout the year. This use. However, it has been evidenced that fact evidences the importance of developing practices that ensure the use of plant projects for promoting the traditional resources may be modulated by cognitive management and conservation of these processes, as they vary in terms of use species. according to environmental or social factors (Santoro et al. 2018). Therefore, the ability of human beings to adapt to the environment is ACKNOWLEDGEMENTS a relevant condition for developing strategies that make possible better use of plant The authors thank the informants of the resources in regions with marked climatic study rural communities for their participation seasonality. in the research, the professor Leonardo This scenario allows us to observe the Pessoa Félix (CCA/UFPB) for the species extent to which management techniques identification, and the Coordenação de optimize the use of species, in addition to Aperfeiçoamento de Pessoal de Nível providing strategies for restructuring Superior (CAPES) for granting a master’s management practices over time (Abbo et al. scholarship to the first author. 2014; Casas et al. 2017). From this perspective, studies on the use and DATA AVAILABILITY management of cacti species are increasingly necessary to verify the pattern CONFLICTS OF INTEREST of techniques used, in order to analyze how much the influence of people on the The authors declare no conflicts of resources has changed plant structures over interest. time. Therefore, studies on the conservation of species important to local populations, in CONTRIBUTION STATEMENT dry forests, provide subsistence to socio­ ecological systems, bearing in mind that the KMP and TKNC collected and analyzed use of species will be increasingly motivated the data and wrote the manuscript; RFPL by local and global changes, leading people coordinated the field research and the writing to resort to their traditional management. of the manuscript. All authors read and approved the final version of the manuscript. CONCLUSIONS

Given the above, it is possible to elucidate the considerable cultural importance related to the uses of the study species by local populations. The species are managed in different ways but the ex situ propagation is the most prominent form of management.

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Received: 22 April 2020 Accepted: 27 June 2020 Published: 01 July 2020

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