Use and traditional knowledge of Byrsonima crassifolia and B. coccolobifolia (Malpighiaceae) in a Makuxi community of the Roraima savanna, northern Brazil

Uso e conhecimento tradicional de Byrsonima crassifolia e B. coccolobifolia (Malpighiaceae) em uma Comunidade Makuxi na Savana de Roraima, extremo norte do Brasil

ABSTRACT

Byrsonima crassifolia and B. coccolobifolia, popularly known as mirixis, muricis, mantecos or nances, are common fruit species in the Amazonian savannas. Their fruits are used in the preparation of juices and other beverages, while the other parts of the plants are used for different purposes in some indigenous communities. The aim of the present ethnobotanical study was to investigate the knowledge and traditional uses of mirixis in the Darora Indigenous Community, of the Makuxi ethnicity, in the São Marcos Indigenous Land, state of Roraima, northern Brazil. The knowledge on these species among the residents was analyzed considering their gender and age. A survey was carried out by means of semi-structured interviews with 60 respondents (36 men and 24 women), between 18 and 84 years of age. Data from the interviewees was compared between genders and two age groups (< 40 and ≥ 40 years of age). Ethnobotanical indices (Informant diversity value; Informant equability value) were calculated, and no significant differences were found in the diversity of uses between genders (U = 283.0000, p > 0.05) and age groups (U = 359.5000, p > 0.05), indicating that the knowledge on the species is evenly distributed among residents. Results show that both species are used for different purposes in the food, fuelwood and medicinal categories in the Darora Community, and this knowledge is widely shared among adult men and women of all ages.

Keywords:
Fuel-use; food; medicinal plants; plant conservation; northern Brazilian Amazon

RESUMO

Byrsonima crassifolia e B. coccolobifolia, popularmente conhecidas como mirixis, muricis, mantecos ou nances, são espécies de frutíferas comuns que ocorrem nas savanas amazônicas. Os seus frutos são utilizados na preparação de sucos e outras bebidas, enquanto outras partes das plantas são utilizadas para diferentes fins em algumas comunidades indígenas. O objetivo do presente estudo etnobotânico foi investigar o conhecimento e usos tradicionais dos mirixis na Comunidade Indígena Darora, da etnia Makuxi, na Terra Indígena São Marcos, no estado de Roraima. Este trabalho analisou o conhecimento dessas espécies entre os moradores da comunidade. A pesquisa foi realizada por meio de entrevistas semi-estruturadas com 60 participantes (36 homens e 24 mulheres), entre 18 e 84 anos de idade. Os dados das entrevistas foram comparados entre gêneros e dois grupos de idade (< 40 anos de idade e ≥ 40 anos de idade). Índices etnobotânicos (Valor de diversidade do informante; Valor de equabilidade do informante) foram calculados, e não houve diferenças significativas na diversidade de usos entre os gêneros (U = 283,0000, p > 0,05) e grupos de idade (U = 359,5000, p > 0,05), indicando que o conhecimento das espécies é uniformemente distribuído entre os moradores. Os resultados mostraram que ambas as espécies são usadas com finalidades nas categorias alimentícia, combustível e medicinal na Comunidade Darora, e o conhecimento é amplamente compartilhado entre homens e mulheres, independentemente da faixa etária.

Palavras-chave:
Combustível; alimentação; plantas medicinais; conservação vegetal; extremo norte da Amazônia brasileira

INTRODUCTION

Mirixis, muricis or mantecos (nances, in English) are fruit species of the Malpighiaceae family, which are commonly found in the natural savanna regions of Amazonia (Benezar and Pessoni 2006). In the state of Roraima, northern Brazil, these fruits are popularly used in the preparation of juices and other beverages, especially those of the species Byrsonima crassifolia (L.) Kunth and B. coccolobifolia Kunth. Local indigenous communities use the timber for fuelwood, food and medicines. Regionally, the species are often found together (Barbosa et al. 2014; Neves et al. 2015). However, B. crassifolia is generally more abundant (Barbosa et al. 2005); it presents smaller fruits with pulp and seed aroma that can be described as fruity, sweet, floral, pungent and similar to rancid cheese odor, due to different chemical components (Rezende and Fraga 2008). According to Pott and Pott (1994), abundance and fruit size differ between the two species, allowing their easy identification.

Northeastern Roraima comprises the largest area of natural savanna in the Brazilian Amazonia, locally known as ´lavrado´, ´campos do rio Branco´ or ´campos de Roraima´, covering approximately 43.000 km² in area (Barbosa and Campos 2011). Roraima's savanna is part of the Rio Branco-Rupununi vegetation complex, which extends from Venezuela to the Republic of Guyana (Barbosa and Fearnside 2005), forming a large mosaic of non-forest ecosystems (open vegetation with low tree density) and forest (island forests, gallery forests, and buritizais), with dominance of open vegetation areas (Barbosa et al. 2007).

Several indigenous lands are located within this huge open vegetation area, including the Raposa/Serra do Sol Indigenous Land and the São Marcos Indigenous Land. The open savanna areas are important sources of plant products for native peoples, and the two sympatric Byrsonima species are traditionally used by many indigenous communities (Perez 2010).

The two Byrsonima species have been consistently reported in phytosociological studies from the Roraima savanna. The density of these species varies depending on the vegetation type. However, most often B. crassifolia presents greater numbers of individuals in relation to B. coccolobifolia (Miranda and Absy 2000; Miranda et al. 2002; Barbosa et al. 2005). Despite the common presence of these species in the open vegetation area, no studies have described the use and traditional knowledge by local indigenous communities (Guéze et al. 2015). The lack of ethnobotanical studies reduces the possibility of developing clear and effective conservation strategies for these important species at the level of local indigenous communities. This fact is directly related to two factors: (i) the intense modification Roraima savanna has suffered due to monocultures and afforestation of exotic species (Aguiar Jr et al. 2014.) and (ii) the displacement of most of the young people in search of employment and facilities in nearby urban centers (Heck et al. 2005). Both factors change the local social relationships, with direct influence on community structure. Since plant use preferences are conditioned by gender and different age groups, and these preferences are generally associated with the division of labor in the community (Voeks 2007; Camou-Guerrero et al. 2008; Almeida et al. 2012), these new relations of population and age structure may cause an erosion of traditional knowledge that is difficult to reverse.

In this context, studies on the population structure and ethnobotany of plant species used by people in the indigenous communities are important and necessary, so they can potentially be used as tools for management and conservation strategies. The present ethnobotanical study aimed to investigate the indigenous knowledge and the traditional uses of B. crassifolia and B. coccolobifolia in a community of the northern Amazonian savanna region. The knowledge on these species among the community residents was analyzed considering the gender and the age of the respondents.

MATERIALS AND METHODS

São Marcos Indigenous Land (TISM) comprises about 654110 ha and 42 indigenous communities of the Makuxi, Taurepang and Wapixana ethnicities. The present study involved a group of the Makuxi ethnicity of the Darora Community, that lives in a region known as Baixo São Marcos (3º 10'42" N; 60º 23'34" W). The study area is at 90 km from the state capital, Boa Vista (Figure 1). The local climate is tropical savanna (Aw), according to the Köppen classification, with average annual temperature of 27.8 °C, and average annual rainfall of ~1.650 mm. The driest period occurs between the months of December and March (± 9 % annual rainfall), and the wettest months are between May and August (± 70 % annual rainfall) (Barbosa 1997).

Figure 1
Location of the Darora Indigenous Community - São Marcos Indigenous Land (TISM), in the state of Roraima, northern Brazil.

The occupation of the Darora Community occurred around 1941, when some families from the Xumina Community (Raposa/Serra do Sol Indigenous Land) migrated to the region due to the difficulty of finding areas for agriculture. The community has a strong aptitude for agriculture and animal livestock, understood by them as necessary for food and sustenance. Extractivism is still used and is always related to the construction of houses, fences, and fruit collection.

There is also a small building where medical and dental care is regularly offered to residents by government agencies. According to the data of these government agencies, 40 families and 184 people live in Darora, of which 50 are men and 43 are women over 18 years old; and five are men and six are women over 60 years old. Residents cited a total of nine men and 12 women, but they were not found, since many of them move from the community to the city of Boa Vista searching for employment and further education. Seven residents were not included in the survey, since they are Makuxi from the Republic of Guyana, and have recently settled in the community. Only one woman declined to participate.

There are two public schools in the Darora Community: one for pre-school, supported by the Boa Vista City Hall, and one for elementary school and high school, supported by the State Government. All residents speak Portuguese fluently. The Makuxi language, from the Karib linguistic trunk, is taught in pre-school, but is rarely spoken by the residents, with only two teachers and one elderly speakers.

Ethics and legal aspects

This study is part of the research project "Use and conservation of plant resources by indigenous communities in northern Roraima", of the Graduate Program in Biological Sciences (Botany), of the National Institute of Amazonian Research (INPA) and Roraima State University. It was submitted to and approved by the Ethics Committee for Human Research of INPA and the National Commission of Ethics in Research with Humans (CEP-INPA/CONEP) (permit # 814.370 - 2014). The study was authorized by the National Foundation for Indigenous People (FUNAI) (process # 08620.002869/2014-15), and by the National Institute for Historical and Artistic Heritage (IPHAN) (process # 01450.001678/2014-88).

Ethnobotanical Survey

For the collection of ethnobotanical data, semi-structured interviews were carried out with 60 respondents (36 men and 24 women) of 38 families, between 18 and 84 years of age. All households in the community were visited, and each resident was invited to participate in the survey. The purpose of the research was explained, and those who agreed to participate in the interview were given an Informed Consent (TCLE) form to be signed.

The interviews were carried out from November 2014 to November 2015. At first, the respondents indicated the collection sites of the studied species in non-forest areas of savanna, and then the free list technique was used on the species they knew in this environment type, as suggested by Albuquerque et al. (2014). Mirixis obtained one of the highest number of citations. In a second phase, semi-structured interviews were carried out according to Albuquerque et al. (2014), with questions about mirixi collection, forms of use, and plant parts used. Responses were grouped into the categories Food, Medicinal, Fuel, and Handicraft, adapted from previous studies (Lins Neto et al. 2008; Lucena et al. 2012).

Botanical material was collected and identified, with the aid of parataxonomists and group-specific experts, and local floras and guides (Melo and Barbosa 2007; Flores and Rodrigues 2010). Samples were incorporated into the herbarium of the Federal University of Roraima (UFRR), with the numbers 8482 (Byrsonima crassifolia) and 8483 (B. coccolobifolia). Classification followed the Angiosperm Phylogeny Group IV (APG IV 2016).

Data analysis

Differences in the knowledge and use of species between men and women of different ages were analyzed. Data from the interviews were compared between genders and two age groups (< 40 and ≥ 40 years of age) (Albuquerque et al. 2014). Two quantitative measures were developed to analyze the knowledge and the use of species: the informant diversity value (IDV), and the informant equability value (IEV) (Byg and Balslev 2001). The IDV measures how respondents use the species and how their different uses are distributed among them, while the IEV measures the degree of homogeneity of the respondent's knowledge, regardless of the number of respondents. Age category 1 (< 40 years of age) had seven women and 14 men; and age category 2 (≥ 40 years) had 13 women and 24 men. The Mann-Whitney test was used to explore the differences between the values and the categories.

RESULTS

Use and local knowledge

Byrsonima crassifolia and B. coccolobifolia are known locally by indigenous people as mirixi vermelho (red mirixi) and mirixi branco (white mirixi), respectively. However, during the interviews, only five respondents distinguished the two species. The respondents affirmed that mirixi, mirixi vermelho and mirixi branco had the same uses. Respondents also reported that the difference between the two types of mirixis is based on the color of the flower (B. crassifolia is yellow, while B. coccolobifolia is white) (Figure 2), and on the shape of the leaves (B. coccolobifolia presents "rounder" leaves). In addition, B. crassifolia was reported to present darker red colored timber when compared with B. coccolobifolia.

Figure 2
(A) - Inflorescence of Byrsonima crassifolia; (B) - Inflorescence of B. coccolobifolia. Scale bar: A-B: 1 cm. This image is in color in the digital version.

The species are widely known to Darora residents, since 58 respondents (38 men and 20 women) confirmed having knowledge of at least one use for the two species (Figure 3). Although differences were recorded between the IEV for men and women, and between IDV and IEV for men and women ≥ 40 years of age, no significant differences were observed in the diversity of uses (IDV and IEV) (gender, U = 283.0000, p > 0.05; age, U = 359.5000, p > 0.05), indicating that the knowledge on the use of the species is equally distributed between the groups (Table 1).

Figure 3
Number of uses for the mirixis (Byrsonima crassifolia and B. coccolobifolia) by respondents (Men and Women)' age (years) from the Darora Indigenous Community, São Marcos Indigenous Land (TISM), Roraima, Brazil.

Table 1
Measurements of knowledge regarding the mirixis (Byrsonima crassifolia and B. coccolobifolia) in the Darora Community (Boa Vista, Roraima, Brazil). IDV - Informant Diversity Value, IEV - Informant Equability Value.

Variables	Values
Total respondents	58
Number of use citations	172
Types of use	11
Measures	Average and standard deviation (X ± SD)
Total IDV	0.271±0.088
Total IDV Women	0.277±0.075
IDV Women (< 40 years of age)	0.247±0.069
IDV Women (≥ 40 years of age)	0.294±0.076
Total IDV Men	0.268±0.096
IDV Men (< 40 years of age)	0.252±0.099
IDV Men (≥ 40 years of age)	0.277±0.095
Total IEV	0.593±0.195
Total IEV Women	0.610±0.165
IEV Women (< 40 years of age)	0.543±0.110
IEV Women (≥ 40 years of age)	0.646±0.166
Total IEV Men	0.584±0.210
IEV Men (< 40 years of age)	0.543±0.214
IEV Men (≥ 40 years of age)	0.608±0.208

Respondents indicated 11 different uses for mirixi, including: food, medicine, fuel and handicraft (Table 2). Six respondents (10.3%) described the use of mirixi bark for leather tanning and buriti palm (Mauritia flexuosa L.) fibers dyeing for artisanal purposes. This low number reflects the fact that the activity of leather tanning is no longer used, while the practice of dyeing buriti fibers is restricted to a few artisans in the community.

Table 2
Use categories and parts of mirixi plants (Byrsonima crassifolia and B. coccolobifolia) used in the Darora Community (Boa Vista, Roraima, Brazil). Number of respondents: 58 (38 men and 20 women). Age category < 40: seven women and 14 men; ≥ 40: 13 women and 24 men.

Use categories	Uses	Part of plant	Number of citations	Number of citations/ gender and age categories
				Women		Men
				< 40	≥ 40	< 40	≥ 40
Medicinal	Diarrhea	Bark	26	6	12	8	28
		Inner bark	3
	Cuts	Bark	11
		Inner bark	2
	General inflammation	Bark	7
		Inner bark	1
	Sore throat	Bark	2
	Utero inflammation	Bark	1
	Kidneys	Bark	1
Food	In natura comsumption	Fruit	15	8	15	17	20
	Juice	Fruit	45
Fuel	Fuelwood	Stem	49	4	14	12	22
	Charcoal	Stem	3
Handicraft	Tincture	Bark	6	1	1	1	3

The use of B. crassifolia and B. coccolobifolia as food was cited by 53 respondents (88.3%). Of these, in natura consumption of fruits (21% citations), and preparation of mirixi wine or fruit juice (79% citations) were the most commonly given responses, showing that the community has extensive knowledge on the use of the species as food.

The use in the medicinal category was cited by 41 respondents (68.3%), and bark soaked in water (88% of citations) and the inner bark (12% citations) were the most cited uses. The tea made with the bark and water for digestive system disorders (diarrhea and dysentery) comprised of 61% citations. General healing and anti-inflammatory purposes for uterine and kidney inflammation were also cited.

The use of both species as fuel was reported by 81.7% respondents, with 96% as fuelwood and 4% as charcoal. The use of mirixis as fuelwood for the production of cassava flour is a very common practice observed in the field, together with copal wood (Copaifera pubiflora Benth.).

DISCUSSION

Juice and in natura consumption of Byrsonima crassifolia and B. coccolobifolia fruits was very common in the Darora Community. Similarly, the fruit consumption of both species is very common in the savanna region by both indigenous and non-indigenous people (Melo and Barbosa 2007; Barbosa et al. 2005). This consumption is based on the fact that the taste and the aroma (flavour) are quite unique, and fruits can be used in their pure form or in a variety of products, such as juice, ice cream, candy and liqueurs (Benezar and Pessoni 2006).

Darora residents regularly use the two Byrsonima species as medicinal products for digestive disorders, such as diarrhea and dysentery. This finding is in accordance with an extensive scientific documentation about the medicinal use of Byrsonima spp., including their anti-inflammatory, antimicrobial and antioxidant activities (Sannomiya et al. 2005; Michelin et al. 2008; Sousa et al. 2014). Some specific examples are the molluscidal action of Byrsonima coccolobifolia against Biomphalaria glabrata, and its effective bactericidal action against Staphylococcus aureus, Bacillus cereus, Pseudomonas aeruginosa, and Escherichia coli (Alves et al. 2000; Pereira 2011). For B. crassifolia, methanol extracted from leaves showed strong giardicidal activity (Amaral et al. 2006), while ethyl acetate extracted from roots proved to be effective against Klebsiella pneumoniae, Pseudomonas aeruginosa, Salmonella typhi, Shigella flexneri, Staphylococcus aureus, S. epidermidis, Micrococcus luteus and Streptococcus pneumoniae (Martinez-Vazquez et al. 1999).

The two species are mostly used as source of energy for cooking in the Darora Community, since few homes use bottled gas for this purpose. In arid and semi-arid areas, the plants are also used as a source of energy for cooking food, especially where bottled gas is costly or difficult to be regularly obtained (Monteiro et al. 2006). In addition, use of B. coccolobifolia as fuelwood and charcoal, the species is also used as forage during animal feed shortage periods, as an ornamental plant, and as timber for furniture (Pott and Pott 1994).

The present results indicate that the knowledge on mirixis is evenly distributed among gender and age groups in the Darora community. Similarly, the knowledge on the tree species, Stryphnodendron rotundifolium Martius, showed no differences between gender and age groups in a community of the Brazilian Savanna (Feitosa et al. 2014). In arid environments, the knowledge of men and women is related to daily activities; women are the traditional holders of the knowledge on medicinal and food species (Voeks 2007), while men are the traditional holders of the knowledge on timber use (Silva et al. 2011; Monteiro et al. 2006). In contrast, the knowledge on the food species Spondias tuberosa Arruda was evenly distributed between men and women, despite gender differentiation in daily activities (Lins Neto et al. 2010).

Studies that indicate better knowledge on plant use among elder than among younger people are common (Monteiro et al. 2006). For instance, Hanazaki et al. (2000) carried out a study in two Caiçara communities in the Atlantic Forest, and observed that older people were more acquainted with craft and medicinal use of plants. The present study also showed no differences between age categories, despite a the slight trend for wider knowledge on Byrsonima among older men (55-70 years) and women (45-60 years) when compared with young inhabitants (see Figure 3). This suggests that the knowledge on plant species decreases after a certain age, as observed by Albuquerque et al. (2011), with the Fulni-ô indigenous people in Northeastern Brazil, and by Ayantunde et al. (2008), with ethnic groups in Southwestern Niger.

Conclusion

Mirixis, Byrsonima crassifolia and B. coccolobifolia, are used for different purposes in the food, fuel and medicinal categories in the Darora Indigenous Community. The knowledge on the indigenous people in Darora on mirixis is evenly distributed among gender and age groups.

ACKNOWLEDGEMENTS

The authors thank the Darora Indigenous Community for allowing the research in its traditional area; Sandra Kariny de Oliveira (Roraima State University - UERR), for supporting all field activities; Sebastião Salvino de Souza "Sabá" and Ricardo Oliveira Perdiz, for the botanical indentification; the UFRR Herbarium in Boa Vista, state of Roraima, and the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES), for granting a scholarship to the first author. The authors also thank anonymous reviewers for their valuable comments.

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Publication Dates

• Publication in this collection
  Apr-Jun 2017

History

• Received
  22 Mar 2016
• Accepted
  05 Mar 2017