Conservation and sustainable use of the medicinal Leguminosae plants from Angola

Data collection

Data on the Leguminosae plant species used in the traditional medicine in Angola was obtained by means of a comprehensive review conducted through the study of numerous herbarium specimens, and of published works and online databases. To provide a critical and updated review of Angola’s medicinal plants, interviews with indigenous healers were conducted over the last two decades in some regions of Angola.

Therefore, this study was made using four main sources:

1. The Angolan collections held in the Herbarium of the Instituto de Investigação Científica Tropical, University of Lisbon (LISC). This is the most comprehensive and representative collection of the Angolan flora comprising over 80,000 specimens that have been collected since the 19th century. Information recorded on the labels allowed us to get data on the medicinal and other uses (e.g., food, timber, fibers and forage), plant parts used, diseases treated, as well as growth form and distribution of each species within Angola.

2. A thorough investigation of the medicinal plant data described in literature. We review data available from the past (e.g.,  Ficalho, 1947; Gossweiler, 1953; Peres, 1959; Santos, 1967; Santos, 1989; Van-Dúnem, 1994; Bossard, 1996) and also more contemporary sources (e.g.,  Costa, Dombo & Paula, 2009; Leyens & Lobin, 2009; Costa & Pedro, 2013; Göhre et al., 2016; Bruschi et al., 2017; Heinze et al., 2017). Furthermore, species occurrences were compiled from specialized bibliography, namely in Conspectus Florae Angolensis (e.g.,  Exell & Mendonça, 1956; Exell & Fernandes, 1962; Exell & Fernandes, 1966).

3. Online databases, namely: (i) PROTA - The Plant Resources of Tropical Africa (https://www.prota4u.org/), which has detailed information on the taxonomy and uses of many African plants; (ii) IUCN - Red List of Threatened Species (http://www.iucnredlist.org) that provides useful information on each species assessed, threats and conservation actions; and (iii) Global Biodiversity Information Facility (GBIF) to get distribution data.

4. Field research carried out by one of the authors (E. Costa), which substantially contributed to updating and complementing the inventory of Angola’s medical flora. Field surveys were conducted in four provinces of Angola: Luanda, Bengo, Zaire and in the exclave province of Cabinda, located in the north of Angola (more information is provided in Data S1). In each rural community, a first meeting was held with the village chief (Soba –Portuguese name) and his advisors to inform them about the purposes of our work and get their support for the choice of the best skilled traditional healers in each community. The ethnobotanical surveys were conducted using semi-structured questionnaires, previously prepared and tested (Albuquerque et al., 2014). During the interviews each healer was previously informed about the objectives of the study and asked to get his informed consent to participate.

In the course of fieldwork, botanical samples were collected for herbarium vouchers. These specimens were preserved for later identification and are kept in the LISC Herbarium and LUA Herbarium (University of Agostinho Neto, Luanda Angola).

Database construction and calculation of pharmacological importance

Based on the best currently available knowledge, we combined ethnobotanical data to complete a database with all the Leguminosae medicinal species known from Angola. This database includes for each species the scientific name and subfamily; distribution in Angola; ethnobotanical data (e.g., plant part(s) used; group of diseases; and other uses such as food, timber, fibers and forage); and their conservation status and main threats, using the Threats Classification Scheme version 3.2 proposed by IUCN (Data S3) (http://www.iucnredlist.org/technical-documents/classification-schemes/threats-classification-scheme). Moreover, for each species it is indicated the number of different sources (e.g., herbarium specimens, published sources, and fieldwork) that refers to its medicinal uses, as a measure to provide more confidence in the legitimacy of usage data, and estimate the ethnobotanical importance of the species.

After compiling the database of the medicinal legumes of Angola, we calculated the pharmacological importance (PI) of each medicinal species by dividing the number of pharmacological properties attributed to the species by the maximum number of properties attributed to the most resourceful species (i.e., the species with the greatest number of pharmacological properties referred). The value of 1 is the highest possible value for PI, indicating the most versatile species with the greatest number of medicinal properties. Pharmacological importance was adapted from Bennett & Prance (2000) where is designated as “normalized pharmacological properties”. It is a widely used method to measure the species importance in traditional medicine and was previously applied in other studies (e.g., Albuquerque et al., 2007; Giday, Asfaw & Woldu, 2009; Oliveira et al., 2010).

Plant names have been checked and updated according to The Plant List (http://www.theplantlist.org) and the African Plant Database (http://www.ville-ge.ch/musinfo/bd/cjb/africa). The Leguminosae subfamilies were updated following the recent proposed classification of the “Legume Phylogeny Working Group”, which presently recognized six subfamilies: Caesalpinioideae (which also includes the former subfamily Mimosoideae), Cercidoideae, Detarioideae, Dialioideae, Duparquetioideae and Papilionoideae (LPWG, 2017).

Leguminosae species used in traditional medicine

The present study is the first survey carried out in Angola to document all the species used in traditional medicine, of one of the biggest plant families - Leguminosae. A total of 127 medicinal plant species were documented, 110 being native non-endemic species, while 17 are endemic species from Angola. Thirty percent of the species have been recorded for the first time as having medicinal uses. Of all the endemic species reported in our study, only three (i.e., Droogmansia gossweileri Torre; Eriosema albo-griseum Baker f.; and Philenoptera pallescens (Welw. ex Baker) Schrire) were reported in current literature about useful plants of tropical Africa (e.g., Burkill, 1994) or in PROTA Web site (http://www.prota.org).

An interesting result of our study was the comparison between our field data and the historical information based on botanical collections. It demonstrated that the Leguminosae medicinal plants recorded several decades ago were also mentioned by the informants during the recent ethnobotanical surveys. Furthermore, it was noted during the field surveys that the knowledge of medicinal plants in Angola is traditionally kept by local healers, but people living in rural areas also demonstrate a broad knowledge of plants and their properties. In general, they maintain a strong relationship with the surrounding environment throughout their lives, using natural resources to supply most of their needs. In fact, our study underlined that some species, which are widely distributed in Angola (e.g., Bauhinia thonningii; Erythrina abyssinica; and Pterocarpus angolensis), are used to treat a relatively large number of illnesses, demonstrating a wide and deep knowledge of medicinal plant properties across the country.

Our findings reveal that 65% of the species reported in our study have their traditional uses confirmed elsewhere in Africa (e.g., Burkill, 1994; PROTA), showing the potential of the Angolan native plants as a source of new compounds of therapeutic interest. The traditional use most frequently noted in our study was the treatment of infectious diseases (e.g., skin infections, intestinal problems and respiratory diseases), which remain the most serious diseases in Africa (Iwu, Duncan & Okunji, 1999). Many of the reported Leguminosae plants have already shown to have interesting biological activity in the treatment of infectious diseases, namely: Abrus precatorius L. is traditionally used in Nigeria to treat tuberculosis (Ibekwe et al., 2014); Albizia adianthifolia is an important medicinal plant in Guinea-Bissau for alleviating intestinal pain (Catarino, Havik & Romeiras, 2016); and Pterocarpus angolensis is used in South Africa for the treatment of parasitic infections affecting humans (Cock, Selesho & Vuuren, 2018).

Since the last decade of the 20th century the prevalence of infectious diseases in Africa increased significantly, and the most important contributing factors are attributed to increases in tuberculosis and HIV/AIDS (Iwu, Duncan & Okunji, 1999). The spread of HIV/AIDS infection has been particularly alarming in sub-Saharan Africa and several studies have focused on plants that can be used in the treatment of this disease (e.g., Mbonu, Borne & Vries, 2009; Becerra, Bildstein & Gach, 2016). Recently, several concerns about the increase of HIV/AIDS were also reported for Angola (e.g., Bártolo et al., 2014) and some species listed in our study (e.g., Abrus precatorius; Acacia goetzei; Afzelia quanzensis Welw.; Dichrostachys cinerea; Mucuna pruriens (L.) DC.; Peltophorum africanum; Sesbania sesban (L.) Merr.) have shown great promise in the treatment of infectious diseases including opportunistic HIV/AIDS infections (see more details in Chinsembu, 2016). These medicinal plants were highlighted as containing a broad-spectrum of antimicrobial agents used to treat: skin infections, sexually transmitted infections (STI), lung infections such as tuberculosis, pneumonia and cough, and also oral infections, revealing the potential properties of these species for the treatment of HIV/AIDS related diseases.

Similarly, there has been an increased scientific interest in the study of bioactive compounds extracted from plants in prevention and treatment of cancer (Greenwell & Rahman, 2015). For example, Albizia adianthifolia extracts collected in Cameroon have revealed considerable cytotoxic activities to fight cancer (Kuete et al., 2016) and ethanol extracts obtained from the roots of Albizia gummifera (J.F.Gmel.) C.A.Sm. in Madagascar have shown cytotoxicity against ovarian cancer (Cao et al., 2007). Both species were also reported in our study and the medicinal properties of these species are well-known in Angola (Costa & Pedro, 2013).

With this paper we contribute to update estimations of medicinal plants from Angola and it is highlighted the enormous therapeutic potential of the Leguminosae species in particular. However, the biological activities of these plants are poorly known and require further research in the laboratory, as only few studies (see Pompermaier et al., 2018) have been carried out with Angolan plants to specifically examine the relationships between the activity of the extracts and their medicinal properties.

Conservation of Leguminosae species in Angola

The preservation of local knowledge together with the conservation of biodiversity are currently regarded as being of major importance in the development of the sub-Saharan Africa (Okigbo, Eme & Ogbogu, 2008). However, there are still important gaps in available data on the conservation status of most of the African medicinal plants. Presently, it is widely accepted that the Red Lists provides the most comprehensive framework to identify and prioritize threatened species (Romeiras et al., 2016a) and several research initiatives were recently conducted across Africa (e.g., for Cameroon by Onana, Cheek & Pollard (2011), for Ethiopia and Eritrea by Vivero, Kelbessa & Demissew (2005), for Cabo Verde by Romeiras et al. (2016b) and for Morocco by Rankou et al. (2015); Lamrani-Alaoui & Hassikou (2018)). The IUCN Red List assessment for the flora of Angola has not yet been conducted, and only a preliminary survey was recently published (Costa, Dombo & Paula, 2009). In fact, assessing the conservation status of medicinal legumes from Angola is a key challenge, because only twelve species were globally evaluated according to the IUCN Red List Categories and Criteria, and only one species (Brachystegia bakeriana) was considered Vulnerable (Phiri, 1998). This assessment was published more than 20 years ago and is cleared outdated. This contrasts with some efforts made in other African countries. For example, the Red List of the Flowering Plants of Cameroon classify 815 species under threat categories, being 9% Leguminosae species (Onana, Cheek & Pollard, 2011), while the Red List of Endemic Trees and Shrubs of Ethiopia and Eritrea reports a worst scenario with 18% of the 135 endangered species, from the family Leguminosae (Vivero, Kelbessa & Demissew, 2005). Therefore, particular attention must be given to initiatives for conserving useful plant species, which corresponds to 21% of the threatening processes for vascular plant species assessed on the IUCN Red List (Bachman et al., 2016).

Angola urgently needs to promote actions that will conserve its great diversity of species and also its unique ecosystems, namely: Angolan Miombo woodlands, Angolan Montane Forest-Grassland Mosaic and Angolan scarp savanna, where several medicinal plants thrive. Our results revealed that 38 of the studied taxa are trees, of which 25 are widely used for timber as well as being medicinal. Several of these tree species have a restricted distribution in Angola, namely: (i) Brachystegia tamarindoides Benth. has limited distribution in Africa, occurring mainly in Angola in the Miombo area (Exell & Mendonça, 1956); (ii) Albizia gummifera and Pentaclethra macrophylla Benth. are mainly distributed in the Atlantic Equatorial forests of Cabinda (Exell & Mendonça, 1956); and (iii) Colophospermum mopane (Benth.) occurs only in the southern provinces of Angola, mainly in the Mopane woodlands (Makhado et al , 2014; Duvane et al., 2017). On the other hand, Brachystegia spiciformis, Burkea africana, Julbernardia paniculata and Pterocarpus angolensis are widespread in savannas and Miombo woodlands (Moura et al., 2017). However, several of these tree species are overexploited and are being cut down on a large scale because they are widely used for charcoal production and much valued as timber for furniture and construction, fetching high prices in international markets (Romeiras et al., 2014).

The sustainable management of the legume species is very important as it is crucial to conserve these unique genetic resources. When roots and whole-plants are harvested is clearly more destructive to medicinal plants than collecting their leaves, flowers or fruits (Hamilton, 2004; Kurian & Sankar, 2007). Therefore, vulnerability of species depends on the parts of plants used and how they are collected. For Angola good harvesting practices must be formulated, particularly when collecting roots, which correspond to 33% of the most frequently parts of legume plants used in traditional medicine (see Fig. 2).

For each medicinal species considered in our study, information on other uses was also compiled (i.e., forage; timber; and for human food and livestock feed), which in turn provided further inputs to identify potential threats to the Angola’s medicinal species. The most serious threats identified in our study were logging and wood harvesting and gathering terrestrial plants, which were generally related to over-harvesting, partly due to the collection of plants for other purposes than medicinal. Moreover, habitat degradation and human disturbance, were reported as main threats to species occurring in the surrounding areas of Luanda (the country’s capital and largest city), and in this field the potential threats are highlighted with regard to several endemic species, namely Acacia welwitschii Oliv. and Philenoptera pallescens, which occur in coastal areas from Luanda to southern parts of Angola.

Moreover, in the scope of this paper, Angola’s medicinal flora has been documented in accordance with their native distribution by the 18 provinces, and notwithstanding notable regional variations, more than half of the medicinal Leguminosae plants are found in southern areas of the country, namely in the regions of Huíla and Benguela, but also in Malanje in north-central Angola. A significant number of species were reported in these 3 provinces to treat a wide range of health conditions, thereby illustrating the need for conserving these species and threatened habitats. Although Angola has established a network of nature reserves and protected areas, encompassing more than 12% of the total land area (MINUA, 2014), there are some limitations in their management structures, namely insufficient financial and staffing commitments. The need for much greater effort and investment in the conservation of threatened species beyond protected areas where most plant diversity occurs, are currently stressed and considerable efforts have been made to identify Important Plant Areas (IPAs) throughout the world (Heywood, 2018). The IPA programme is a mean of identifying and protecting the most important sites for wild plant and habitats, and also offer protection to a wide range of species including medicinal plants, and many common but declining species (Anderson, 2002). IPAs have been delimited for several countries (e.g., De Dios et al., 2017 and specifically to conserve medicinal plants (Hamilton & Radford, 2007). The identification of IPAs in Angola could be based on the presence of threatened plant species under criterion A or based in high concentration of socio-economically important wild-harvested species (including medicinal plants, food plants, timber species, etc.) under sub-criterion B(iii) (Darbyshire et al., 2017). Therefore, our study could provide data towards long term conservation of key sites for plant diversity—IPAs, namely to preserve medicinal species on Huíla, Malanje and Benguela, where the protected area system is not yet representative and comprehensive for safeguarding its botanical diversity. It must be emphasized that in Huíla the existing protected area of Bicuar National Park was historically created to protect big mammals (e.g., black buffalo, antelopes, and elephants), and Cangandala National Park, in Malanje, to protect only one species—the giant sable antelope “Palanca Negra Gigante” (Hippotragus niger variani). Therefore, more studies are needed to understand whether medicinal plants are being overexploited within these protected areas in order to suggest conservation strategies for their future preservation.