RESEARCH ARTICLES
http://dx.doi.org/10.17159/ sajs.2016/20160044

 

San and Nama indigenous knowledge: The case of |nhora (Pteronia camphorata) and its medicinal use

 

 

Isabel M. Hulley^I; Patricia M. Tilney^I; Sandy F. Van Vuuren^II; Guy PP Kamatou^III; Janneke M. Nortje^I; Alvaro M. Viljoen^III; Ben-Erik Van Wyk^I

^IDepartment of Botany and Plant Biotechnology, University of Johannesburg, Johannesburg, South Africa
^IIDepartment of Pharmacy and Pharmacology, University of the Witwatersrand, Johannesburg, South Africa
^IIIDepartment of Pharmaceutical Sciences, Tshwane University of Technology, Pretoria, South Africa

Correspondence

 

 

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ABSTRACT

A hitherto unidentified medicinal plant is here identified for the first time as Pteronia camphorata (L.) L., an aromatic shrub of the Asteraceae family endemic to the western and southern coastal region of South Africa. The plant was described in this journal by Laidler¹ in 1928 as 'D/nhora buchu', and is one of the important types of buchu used by the Nama people. We report the traditional medicinal uses among San and Nama people, based on our interviews with rural participants. These include the treatment of colds, influenza, chest ailments and tuberculosis, as well as convulsions, haemorrhoids and inflammation of the neck. The major and minor chemical compounds of the essential oil that is produced by the plant are identified, together with the site of accumulation of this volatile oil within the leaf. We also investigated the plant's antimicrobial activity against a selection of a yeast and two Gram-negative and one Gram-positive bacteria, all of which are associated with respiratory infections. P. camphorata is scientifically poorly known but is an important San and Nama traditional remedy. Our study not only prevents the potential loss of historically important indigenous knowledge, but also provides the first scientific evidence to validate the traditional use of |nhora against upper and lower respiratory tract infections, including tuberculosis. This detailed study has wider application in demonstrating the fragility of the oral-traditional knowledge of a scientifically neglected indigenous group. It also highlights the scientific and practical importance of preserving traditional plant-use knowledge within a botanically diverse region.
SIGNIFICANCE:
• Reveals the botanical identity of |nhora, an important Nama medicinal plant.
• Presents scientific evidence to validate the traditional uses.
• Contributes to the cultural heritage of a scientifically neglected indigenous group.
• Demonstrates the fragility of oral-traditional knowledge.

Keywords: Asteraceae; essential oil; ethnobotany; leaf anatomy; antimicrobial activity

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Introduction

The traditional Khoi and San practices of plant use in the botanically rich Cape region of South Africa are poorly documented. They are also rapidly diminishing because of the fragility of orally transferred indigenous knowledge, and the fact that modern medicine has almost completely replaced the traditional health care system. Because the Khoi and San peoples are ancestral to the rest of humanity, their ethnobotanical knowledge is of global significance. It provides insights into the early history and origins of medicinal plant use. We therefore hope to prevent the loss of profound ethnobotanical information relating to an important fynbos-endemic medicinal plant. Fynbos is a natural shrubland or heathland vegetation located in the south-western part of South Africa.

The hitherto unidentified plant described by Laidler¹ in 1928 as 'D/nhora', one of the important types of buchu used by the Nama people, is here identified for the first time as Pteronia camphorata (L.) L. (Asteraceae). 'Buchu' (boegoe) refers to aromatic plants that are used, often in powdered form, for medicinal and cosmetic purposes. Laidler used D/ to denote the voiceless (tenuis) dental click, but we use the pipe symbol (\) in accordance with the International Phonetic Alphabet. Some linguists still prefer the (1) symbol of the Doke / Beach convention.

The cultural and historical importance of this species came to light gradually, mainly because of ethnobotanical field survey work in Namaqualand.² Only ten elderly persons, two of whom are now deceased, had traditional knowledge about P. camphorata and its use in San and Nama medicine. Pteronia L. is a genus of roughly 70 small shrubs subendemic to southern Africa³ and has been the focus of recent ethnobotanical studies^4-6. Although these aromatic plants are of considerable local importance as sources of traditional medicine, their ethnobotany, leaf anatomy, essential oil chemistry and antimicrobial activity had previously not been studied systematically. P. camphorata is a small shrub of up to 0.8 m in height; it has a wide distribution in the Northern, Western and Eastern Cape provinces of South Africa. Four varieties have been distinguished (Figure 1), based on leaf arrangement (alternate or opposite) and the presence and density of white hairs (cilia) on leaf surfaces and margins.³

We wish to dispel the myth that indigenous knowledge is mainly of cultural and symbolic value, with limited practical use in health care. Our study explores the scientific rationale for the main use of |nhora in treating respiratory infections, including tuberculosis. For this purpose we conducted a detailed scientific study of the ethnobotany, leaf anatomy, essential oil chemistry and antimicrobial activity of P. camphorata.

 

Materials and methods

Materials studied

Three fresh samples of P. camphorata var. armata were collected at Kleinvlei, close to Wupperthal (32° S, 19° E), for the purpose of essential oil analysis and antimicrobial studies. Samples of all four varieties of P. camphorata were collected at various localities for anatomical study. Exact localities, voucher specimen details and authorities for names are shown in Table 1.

Ethnobotanical interviews

The recording of ethnobotanical data strictly adhered to all the ethical principles in the Code of Ethics⁷ of the International Society of Ethno-biology. These include the concepts of traditional resource rights, educated prior informed consent, and respect for the privacy and customs of rural people. Formal approval was also obtained (by B.E.V.W. and J.M.N.) from the ethics committee of the Faculty of Science at the University of Johannesburg. The data presented here form part of two extensive ethnobotanical surveys in Namaqualand and the Cederberg region. The ethical clearance reference numbers are UJ Protocol No. 13 January 2015 (B.E.V.W., Cederberg survey and other studies); UJ Protocol No. 20 May 2011 (J.M.N., Kamiesberg survey, for MSc) and UJ Protocol No. 7 July 2015 (J.M.N., Namaqualand survey, for PhD).

Interviews were conducted in the local language, Afrikaans, and we used the matrix method as previously described². An extensive network of local participants was interviewed: close to 100 people in Namaqualand and more than 30 people in the Cederberg region, including several local experts (Table 2). Our paper provides a firm starting date and geographical localities for the traditional knowledge associated with P. camphorata, including the identities of the knowledge holders.

Anatomical procedures

Dried leaf material of P. camphorata var. armata was rehydrated and placed in formaldehyde-acetic acid-alcohol (formaldehyde [40%] : glacial acetic acid : ethanol [96%] : distilled water, 2:1:10:7) together with fresh leaf material from the remaining three varieties, for 24 h. Thereafter the material was treated according to the methods described previously^4-6 (dehydration, infiltration with and embedding in glycol methacrylate, sectioning, staining and data capturing). Unstained slides were viewed under a polarising microscope to observe whether any crystals were present.

Distillation and analysis of essential oil

Leaves and twigs (roughly 300 g dry weight) from three different plants of P. camphorata var. armata (Table 3) were air-dried for 9 days, then subjected to hydro-distillation for 180 min using a Clevenger-type apparatus. The oils were weighed and stored in sealed vials in the dark at 4 °C before analysis.

The oils (20% diluted in hexane) were analysed by a gas chromatography-mass spectrometry system using standardised settings, as described previously⁴. Compounds were identified by their mass spectral data and retention indices, as well as library searches of the NIST^®, Mass Finder^® and Flavour® libraries.

Antimicrobial studies

Various extracts (Table 4) and the oil samples listed in Table 3 were invest igated for antimicrobial activities, using the minimum inhibitory concentration (MIC) microtitre plate method as previously described⁴. A yeast (Cryptococcus neoformans, American type culture collection [ATCC] 90112) as well as two Gram-negative bacteria (Moraxella catarrhalis ATCC 23246 and Klebsiella pneumoniae ATCC 13883) and one Gram-positive bacterium (Mycobacterium smegmatis ATCC 14468) were selected for the study. All cultures were selected on the basis of their respiratory pathogenesis, with the exception of M. smegmatis, which is a non-pathogenic Mycobacterium strain with a faster growth rate than that of M. tuberculosis - hence its ease of use. Cryptococcus neoformans is associated with lung infection, and M. catarrhalis is known to cause bronchitis, sinusitis and laryngitis. Klebsiella pneumoniae commonly causes pneumonia. The preparation of bacterial cultures and the methodology followed, including the preparation of extracts, were exactly the same as described previously.^4-6 MIC assays were undertaken in duplicate or triplicate on separate occasions, and the mean results are presented.

 

Results and discussion

Ethnobotany

A historically important ethnobotanical paper by Laidler¹, published in this journal in 1928, gave the names of several species of buchu used in Namaqualand. The use of buchu (powdered aromatic bushes, usually stored in tortoise shells) as a topical treatment of the skin is of San origin, and is well described in the literature.^4,8 Buchu, sab or P/nkaou (Laidler used P/ to denote the palatal or palato-alveolar click, ǂ) is said to have two varieties. The first is D/nhora (|nhora), D/khonsa (\khonsa) or haas buchu, and the other is P/kabourie (ǂkabourie). The botanical identities of these two plants have remained unknown, perhaps because Laidler was not a botanist or he saw only the powdered plant material. He described the use of the two buchu types as follows¹:

Considered by Hottentot to possess great virtues in curing disorders, and rarer forms are valuable to the Native. In powder used for dusting, for fire and sunburns Baby powder made of D/nhora kept in tortoise shell puff box, roasted with fat and dropped in ear for earache. Powder also mixed with C/ghoonabi, and acacia thorn sucker, and then considered a high class powder. The second rate powder used for babies was mixed with ground acacia thorn bark, and is named O/kai. D/ nhora Buku is roasted with oil and fat, mixed with mother's milk and dropped into the ear for earache. P/nkaou is rare and valuable, and a thimbleful is worth from a sheep to an ox. It is obtained in mountainous districts and when used is pounded and tied in a cloth over which hot water is poured.

According to Laidler¹, the name P/nkaou was given to him for what was known as 'Buchu barosma' or 'Letulina' at the time. This clearly refers to round-leaf buchu, Agathosma betulina (P.J. Bergius) Pillans, a species confined to the mountainous region of the Bokkeveld, Cederberg and Grootwinterhoek. It is understandable that this plant would be considered rare and valuable, because it was not available locally but had to be transported over a considerable distance from the Cederberg to Namaqualand; the Kamiesberg is roughly 300 km north of the Cederberg. P/kabourie (ǂkabourie) is not mentioned again, and the reader is left with the impression that this name also refers to P/nkaou.

The identification of D/nhora (|nhora) as P camphorata is the result of a few anecdotes spread over more than a decade. The first and most convincing was the explicit information given by Mr Willem 'Blikkies' Steenkamp at Nieuwoudtville, an area where the Namaqualand variety of the species (var. armata) also occurs naturally. All available ethnobotanical information on P. camphorata is shown in Table 2. Original anecdotes, recorded in Afrikaans, have been retained to ensure that subtle nuances about the plant and its uses are not lost in translation. P. camphorata shares with several other species the Afrikaans name gombossie.^9-11

The first reference to P. camphorata as a medicinal plant appears on a herbarium specimen (E.B. Watermeyer 6350 in PRE). According to the label information, the specimen was collected in January 1925 and the plant is known as koortsbos (meaning koorsbos, i.e. fever bush). Unfortunately, the locality is given imprecisely as 'Little Namaqualand'. The first-ever published ethnobotanical use for P. camphorata, namely the treatment of boils, was reported by Watt and Breyer-Brandwijk¹², who cite Kling¹³ as the source of their information. Curiously, the species was not included in Rev. Kling's¹³ booklet of 1923, so the origin of the information remains a mystery and appears to be based on a misinterpretation - uncritically cited by Arnold et al.¹⁴

The only other published ethnobotanical anecdote for the species was reported by Van Wyk and Gericke¹⁵, who cited Willem 'Blikkies' Steenkamp, an elderly man of Khoisan descent from the farm Oorlogskloof near Nieuwoudtville in the Northern Cape province of South Africa. The origin of the knowledge is Mr Steenkamp's grandfather, who was ethnically pure San. The plant is regarded as the most important of all the traditional medicines in the area, and is known locally as norraboegoe.

This word appears to be derived from a corruption of the word '|nhora' (| denoting the dental click) and boegoe (the common Khoisan term for aromatic bushes). It was explained to B.E.V.W. that the term |nhora in the San culture refers to the 'life force' in human beings, which is believed to be situated in the nape of the neck. Directly translated the name means 'life force buchu', reflecting the perceived importance of this plant species.

Recent enquiries in various parts of the Western and Northern Cape provinces (including the Cederberg region, where the species is quite common) revealed only a few known contemporary uses. In the Kamiesberg area of Namaqualand in Northern Cape, we located two herbalists with original knowledge about the species and its uses in the Nama culture. The late Anna 'Boom' Stewe was a herbalist from Leliefontein in the Kamiesberg, who obtained her medicinal knowledge from the late Jan 'Bordhoed' Beukes, a local bossiedokter - a term of honour for an acknowledged herb doctor. The plant, which Anna Stewe called |nôrraboegoe, is used in a mixture with org [Notobubon pearsonii (Adamson) Magee] and jantjie-bêrend [Sutherlandia frutescens (L.) R. Br. which is] [=Lessertia frutescens (L.) Goldblatt & J.C. Manning] to treat tuberculosis. A small glass (kelkie) of a hot water infusion (tea) of the leaves of the three species is taken three times a day, and is considered to be the best medicine for tuberculosis. This medicine was used by an elderly lady, whose name is no longer recalled, for convalescent tuberculosis patients. Powdered leaves mixed with other herbs can also be used medicinally as snuff, and infusions of a leafy twig in hot milk or water are used to alleviate toothache. Powdered leaves are applied to a piece of cotton wool and inserted into the ear for relief of earache (dit het 'n pyndodende effek - 'it has a painkilling effect'). The mixture can also be used for flatulence ('to remove wind'). The use against earache and flatulence was confirmed by three other local inhabitants of Kamiesberg, and another person added that an infusion can be used to treat rheumatism.⁸

The second local expert in the Kamiesberg was the late Gert 'Joelk' Dirkse, a herbal doctor from Paulshoek and one of the last professional bossiedokters in Namaqualand. He independently supplied information about P. camphorata. Powdered root is used to treat febrile convulsions in infants, and powdered leaves are used to treat convulsions and epilepsy in adults as well as for blood purification. Gert Dirkse stated that a decoction of the leaves, mixed with baarbos (Limeum africanum L.) and slangbos [Stoebe plumosa (L.) Thunb.] is taken orally and is very effective in treating general malaise (siek voel).

We also heard recent anecdotes from the small Namaqualand village of Spoegrivier. An experienced and highly knowledgeable midwife, Ouma Sarah 'Toesie' Fortuin, still remembered \ôrrôboegoe or \ôrrôbosboegoe. According to Sarah Fortuin, |ôrrô refers to the back of the neck, and the plant is used to treat inflammation and redness of the neck in children. It is also a medicine for chest ailments, and is considered highly effective (hierdie bos is baie goeie medisyne - 'this shrub is very good medicine'). Corneels 'Kaldei' Christiaan from the same village reported that the plant grows only in moist areas and is used for the treatment of haemorrhoids - hence his vernacular name for the plant, aambeiebos (haemorrhoids bush). Further south, near Vanrhynsdorp not far from Nieuwoudtville, Esau Flink reported that he uses a decoction of the leaves and twigs to treat influenza. He referred to it as t' ôrrôbos.

Given its obvious medicinal importance, it is surprising that the uses of P. camphorata have remained almost unknown to science until recently. We were fortunate to have the opportunity to record, and preserve for posterity, the rich knowledge of two very knowledgeable and experienced herbalists, Anna Stewe and Gert Dirkse. Sadly, neither of them had any apprentices to whom they could pass on their knowledge.

Anatomy

The leaves of P. camphorata are amphistomatic. They have a thin cuticle and the outer periclinal cell walls of the epidermal cells are markedly thickened. The mesophyll is composed of usually two layers of palisade parenchyma, more highly developed adaxially than abaxially, which surround the central spongy parenchyma (Figure 2). Secretory structures that can be referred to as oil glands or cavities occur in the spongy parenchyma adjacent to the phloem of some vascular bundles. Macroscopically they are visible as translucent dots (Figure 1). Secretory trichomes are situated in the medial adaxial groove, but can sometimes also be found in the corresponding position on the abaxial surface.

It appears that three types of secretory structures are present in the genus Pteronia, and the ethnobotanically relevant species can be classified into four groups based on their combinations. The structures are as follows: (1) globose oil glands or cavities, similar to those in Citrus, which are present in P. onobromoides D.C., P. stricta Aiton and P. succulent Thunb.; (2) oil ducts associated with the vascular bundles, mainly the midrib, which are present in P adenocarpa Harv.; (3) oil ducts associated with the vascular bundles as well as secretory trichomes, which occur in P. cinerea L.f., P. divaricata Less., P. incana D.C. and P. lucillioides D.C.; and (4) globose oil glands and secretory trichomes mainly in the medial grooves - this type is present in P. camphorata. The leaf anatomy of Pteronia species appears to be of considerable value in providing diagnostic characters, and has the potential to contribute to a better understanding of the infrageneric taxonomy and relationships of the genus.

Essential oil composition

We identified 21 to 25 volatile components in the three samples of P. camphorata var. armata that we analysed from Wupperthal (Table 3). A similar combination of main compounds was found in P. camphorata var. camphorata from Montagu Pass in the southern Cape, as studied by Coovadia¹⁶ and reported by Viljoen et al.¹⁷ The major compounds in one or both of the varieties are several monoterpenes as well as sesquiterpenes (Table 3). The two varieties agree in the presence of sabinene, limonene, 1,8-cineole, p-cymene and terpinene-4-ol as main compounds. In addition, (Z)-β-ocimene is a major constituent in Wupperthal samples but a minor constituent in Montagu Pass samples. Estragol occurs at relatively high levels at Montagu but only as minor compounds at Wupperthal. Methyl eugenol was a major compound in one of the Wupperthal samples. Both varieties have smaller amounts of a-pinene, β-pinene, γ-terpinene and (E)-β-ocimene.

A number of non-volatile diterpenes and other phenolic compounds have been isolated from P. camphorata and other Pteronia species.¹⁸ These include 3,4-dimethoxypropiophenone, eugenol methyl ether and several other more widespread compounds. The biological, chemotaxonomic and medicinal significance of these compounds are as yet unknown.

We compared the main essential oil compounds in P. camphorata with those of four other ethnobotanically relevant species for which data are available.¹⁶ The results showed the following general patterns: (1) sabinene, limonene, 1,8-cineole, p-cymene and myrcene are main constituents in most of the species, and the same pattern is evident for P. camphorata; (2) β-pinene is a major compound in P. adenocarpa and P. incana and is present as a minor compound in all other species; and (3) sesquiterpenoids appear to be more restricted in their distribution. There might well be a link between the essential oil composition and antimicrobial activity. A previous study showed that cineole and limonene may interact synergistically to exert enhanced antimicrobial activity.¹⁹

Antimicrobial activity

The results of our antimicrobial study on the extracts of P. camphorata are shown in Table 4, with noteworthy activity highlighted in bold text. Noteworthy activities for extracts were considered where MIC values were below 1.0 mg/ml^20-21 and for essential oil samples where MIC values were below 2.0 mg/ml²². The methanol-to-dichloromethane (MeOH : CH₂Cl₂) extracts were the most active against Mycobacterium smegmatis, with MIC values as low as 0.3 mg/ml to 0.5 mg/ml. The methanol-to-water (MeOH : H₂O) extracts were the most active against C. neoformans, with MIC values as low as 0.1 mg/ml to 0.2 mg/ml. The essential oils also showed strongest antimicrobial activity against C. neoformans, with the most noteworthy having an MIC value of 0.3 mg/ml.

Water and methanol-to-water extracts generally showed poor to no activity at the highest concentration tested, against all organisms studied except for C. neoformans. In the latter case, the mean MIC value was 0.5 (H₂O extract), with MIC values ranging from 1.5 mg/ml to 3.0 mg/ml (H₂O extracts) for the various Mycobacterium species tested.

 

Conclusion

P. camphorata is poorly known as a medicinal plant, but available information and recently recorded ethnobotanical data suggest it was once an important Khoisan remedy. Almost no local knowledge or local users could be found in most of the rural localities where the plants grow. The traditional uses include treatment of respiratory conditions (colds, fever, influenza, chest ailments and tuberculosis) and inflammation of the neck, convulsions and haemorrhoids. These uses suggest the plant has antimicrobial, anti-inflammatory and antipyretic properties.

The globose oil glands found in P. camphorata are similar to those of P. onobromoides, P. stricta and P. succulenta but not those of any other species. P. camphorata differs from the others by the presence of additional glandular trichomes in the medial grooves. The leaf anatomy appears to have some diagnostic value at the species level, and holds considerable potential as a source of taxonomic characters.

P. camphorata essential oil has a similar combination of main compounds as that found in other Pteronia species: sabinene, limonene, 1,8-cineole, p-cymene and terpinene-4-ol are the main constituents. Smaller amounts of a-pinene, β-pinene, (Z)-β-ocimene, γ-terpinene, (E)-β-ocimene and myrcene also occur in all or most of the samples of this species. The plant has small amounts of sesquiterpenes, such as bicyclogermacrene - which is a main compound in P. divaricata and a minor compound in P. incana.

Most of the extracts, as well as the essential oil of the plant, display activity against C. neoformans. The dichloromethane extracts and essential oil samples were active against M. smegmatis. The level of activity against these respiratory pathogens seems to support the reported efficacy of the traditional treatment against tuberculosis, colds and influenza.

 

Authors' contributions

I.M.H. prepared the samples and performed the experiments; P.M.T. provided anatomical know-how and infrastructure, and prepared the anatomical descriptions; S.F.V.V. was responsible for the experimental design of antimicrobial tests, and provided the microbial samples and infrastructure; G.PPK. performed the GC-MS analyses and calculations; J.M.N. contributed original ethnobotanical data; A.M.V made conceptual contributions, guided the essential oil analyses and provided the analytical infrastructure; and B.E.V.W. was the project leader, conceptualised the study, wrote the first draft and contributed taxonomic and ethnobotanical data.

 

Acknowledgements

Financial support from the National Research Foundation is gratefully acknowledged. We thank and honour Mr Willem 'Blikkies' Steenkamp of the farm Oorlogskloof near Nieuwoudtville; the late Ms Anna 'Boom' Stewe of Leliefontein; the late Mr Gert 'Joelk' Dirkse of Paulshoek; Mrs Sarah 'Toesie' Fortuin and Corneels 'Kaldei' Christiaan of Spoegrivier; and Mr Esau Flink of Vanrhynsdorp, for sharing their remarkable traditional knowledge on medicinal plants. We also thank Mr Paul Herman at the South African National Biodiversity Institute in Pretoria for kindly identifying the four varieties of P. camphorata used in this study.

 

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Correspondence:
Ben-Erik Van Wyk
bevanwyk@uj.ac.za

Received: 04 Feb. 2016
Revised: 05 May 2016
Accepted: 06 May 2016