key: cord-0005389-bm54jqqf authors: Mokgolodi, Neo C.; Hu, Yan; Shi, Ling-ling; Liu, Yu-jun title: Ziziphus mucronata: an underutilized traditional medicinal plant in Africa date: 2011-08-06 journal: For DOI: 10.1007/s11632-011-0309-1 sha: ae5c80ddeff7b8740c2557b2a584315ff5e233f8 doc_id: 5389 cord_uid: bm54jqqf In Africa, rural people depend heavily, if not exclusively, on medicinal plants and indigenous healthcare knowledge to meet their medical needs. Over 80000 flowering plant species are used medicinally worldwide. Amongst them are the underutilized Ziziphus species in the Rhamnaceae family. In terms of abundance and economic value, Z. jujuba and Z. mauritiana are currently the most important, especially in China and India where they are cultivated and exploited for medicinal use and their edible fruits. We examined a related common species widely distributed in Africa, Z. mucronata, whose economic value has not, as yet, been explored. Local people in various African countries use its different parts to cure a large number of diseases, many of which are similar to those treated with Z. jujuba and Z. mauritiana. Several studies have shown that Z. mucronata has cyclopeptide alkaloids, i.e., mucronines F, G and H, with antibacterial properties. Conservation strategies to sustain and maximize the benefits of Z. mucronata to people are proposed. Medicinal plants contain inherent active ingredients used to cure diseases or relieve pain (Okigbo et al., 2008) . Traditional remedies made from these plants play an important role in maintaining the health of 70%-80% of people in rural and indigenous communities throughout Africa (Cunningham, 1993) . In fact, in some African countries, the number of traditional healers far outnumbers that of modern, westerneducated doctors (Table 1 ). Even where modern medical services are available, use of medicinal plants has remained a more feasible option. This is due to their affordable prices, relative accessibility, local availability, trust in their effi cacy, given the emergence of new and incurable diseases, such as HIV/AIDS, cancer, malaria and diabetes (Aumeeruddy-Thomas, 2002) . For example, both China and Mongolia are pursuing health care systems based on the practice of traditional medicine. In China, health care professionals use medicinal plants to treat and prevent diseases as well as to foster primary health of 40% of their patients (Brown, 1995; Zhang, 1998) . After the discovery of the fi rst infl uenza A virus (the subtype H1N1) in May 2009, for example, the Chinese government recommended a combination of western medicine and traditional Chinese medicine (TCM) as the primary course of treatment. In 2003, the SARS outbreak was also combated in the same way in China, resulting in 60% proven effi cacy among more than 5000 patients treated (Shan, 2010) . China has at least 800 manufacturers of herbal products, with an output worth about $1.8 billion per annum. Moreover, on a total planted area of 140836 ha for medicinal herbs, 13000 central farms specialize in the production for traditional medicine and 340000 farmers cultivate medicinal plants (WHO, 2001) . One of the medicinal plants used in China to cure diseases is Ziziphus jujuba Mill. (Chinese date or Chinese jujube) of the family Rhamnaceae. Over time, interest in expanding the use of underutilized crops, i.e., Ziziphus species, has been sporadic, especially in relation to rural development initiatives. In India, Z. mauritiana Lam. has already been included in the national program on underutilized crops (Pareek, 2001) . Similarly, Azerbaijan also recognized the underutilization of Ziziphus species and thus gave Chinese jujube a priority in its national programs (Pareek, 2001) . Different Ziziphus species, especially Z. mucronata in Africa, Z. mauritiana in India and Z. joazeiro in South America, are also valuable sources of traditional African, Indian and South American medicines, respectively. Our primary focus is on Z. mucronata. The objectives are: 1) to present an overview of traditional medicinal use of Z. mucronata in the African continent using available literature, 2) to outline briefl y similar medicinal use of Z. mucronata with other Ziziphus species and their economic value, 3) to highlight the potential economic importance of Z. mucronata in relation to other vital Ziziphus species and subsequently 4) to suggest some possible conservation measures necessary to ensure its lasting supply to the communities it serves. 2 Description of Z. mucronata Ziziphus mucronata Willd. subsp. mucronata belongs to the buckthorn family (Rhamnaceae) in the order Rhamnales. It is a plant species in the genus Ziziphus Tourn. ex L. (Azam-Ali et al., 2006) . The Latin name 'Ziziphus' means thorny and 'mucronata' refers to the pointed leaves of this species (World Agroforestry, 2010) . Ziziphus is a generic name derived from the Arabic word zizoufo (World Agroforestry, 2010) used for Z. lotus (L.) Desf., but also related to the ancient Persian words zizfum or zizafun; ancient Greeks used the word ziziphon for the jujube (Azam-Ali et al., 2006) . The genus Ziziphus is of some historical importance. It is believed that Christ's crown was made from Z. spina-christi Willd., a species which closely resembles Z. mucronata but grows from central Africa northwards (Palmer and Pitman, 1972) . Nevertheless, this is not certain, since Paliurus spina-christi Mill., synonym P. aculeatus, has also been proposed (Azam-Ali et al., 2006) . Generally, there is a consensus that the genus Ziziphus consists of approximately 86 species (Johnston, 1972; Hyde and Wursten, 2010) . Bhansali (1975) suggested that there could be up to 135 species and studies by some authors (Liu and Cheng, 1995; Islam and Simmons, 2006; Liu and Zhao, 2009) showed that there could be up to 170 species. A major factor contributing to this complexity may be that, in some cases, the same specifi c epithet has been used by different authors for different species. For example, Z. mauritiana Lam. has had the specifi c epithet of jujuba applied as Z. jujuba (L.) Lam. and Z. jujuba (L.) Gaertn. (Azam-Ali et al., 2006) . Moreover, inter-regional comparisons are sometimes not taken into consideration when naming the species. For instance, Johnston (1972) proposed possible affi nities between Z. lotus of Mauritania and the Sahara and also between Z. hamer of East Africa and Z. leucodermis (Baki) O. Schwartz of Arabia and as such suggested a more detailed study of the genus; but up to date no literature has been found to show that this has been done. Synonyms of Z. mucronata include Z. adelensis Del., Z. mitis A. Rich, Z. mucronata Willd. var. glabrata Sonder, Z. mucronata Willd. var. glauca Schinz, Z. mucronata Willd. var. inermis Engl. and Z. mucronata Willd. var. pubescens Sonder (World Agroforestry, 2010). The common English name of Z. mucronata is buffalo thorn. Alternative names include cape thorn, shiny leaf and wait-a-bit. Apart from Z. mucronata, other Ziziphus species widely found in Africa include Z. abyssinica Hochst. ex A. Rich. and Z. spina-christi Willd. (Azam-Ali et al., 2006) . Gelfand et al., 1985; World Bank, 1993; Cunningham, 1997 Note: TMP * , traditional medical practitioners; ** , region; *** , city; NA, data not available. Z. mucronata is a common, drought resistant species distributed throughout the summer rainfall areas of sub-Saharan Africa, extending from South Africa northwards to countries such as Eritrea, Ethiopia, Ghana and Senegal (Schmidt et al., 2002) . It also occurs in Yemen in the Arabian Peninsula (United States Department of Agriculture, 2010). Figure 1 shows its overall distribution. Z. mucronata regenerates naturally from seeds in various habitats with a mean annual temperature of 12-30°C and a mean annual rainfall of 446-1200 mm (Orwa et al., 2009; World Agroforestry, 2010) . However, it is more common on fl at and open woodlands, in alluvial soils along rivers, around pans as well as on termite mounds (Palgrave et al., 2002; Azam-Ali et al., 2006) . Z. mucronata occurs both in coastal regions and inland, up to 2000 m above the sea level (Orwa et al., 2009; World Agroforestry, 2010) . In addition, Z. mucronata can be propagated in nurseries, where it grows reasonably quickly from seeds or cuttings in any soil type and reaches 4 to 6 m in 4-5 years (Orwa et al., 2009 ; World Agroforestry, 2010). Z. mucronata is a shrub to medium-sized deciduous tree, up to 10 m in height, with an irregular spiky canopy (Shackleton et al., 2005) . It has a single trunk that is often crooked; its branches spread and droop, branching above ground or sometimes near the base (World Agroforestry, 2010). Z. mucronata has distinctive angular zigzag branchlets and twigs, together with the hooked and straight thorns. The thorns of this species, usually present at the base of the leaf, are often in pairs, reddish brown, one straight (up to 2 cm; World Agroforestry, 2010) and the other shorter, stronger and hooked. Leaves of Z. mucronata are shiny and light green, simple (30-80 mm × 20-50 mm), alternate or in tufts, with blade prominently 3-5 veined from their base (Schmidt et al., 2002) . The small (± 4 mm in diameter), yellowish-green star-shaped flowers are borne in dense clusters above each leaf during October and November (Shackleton et al., 2005) . The normally round fruits always appear thereafter from January to July (Shackleton et al., 2005) , which often stay attached to the plant long after the leaves have fallen. The fruits of Z. mucronata are green when young, usually up to 2.5 cm in diameter and turn to reddishbrown when ripe (Maundu et al., 1999) . They contain a large stone inside and as such have relatively little pulp which is usually dry and mealy. The seeds are usually solitary, elliptic and compressed. Mature trees produce about 500-2000 kg of seeds (Orwa et al., 2009; World Agroforestry, 2010). The bark of Z. mucronata is normally red-brown and smooth but only on young stems. In older trees, it is roughly mottled grey and often cracked in small rectangular blocks, revealing a stringy red under-bark. The main stem of Z. mucronata is green and hairy when young (Schmidt et al., 2002) . Modern scientific medicine is a highly regulated social and economic activity. However, most people, particularly in the developing countries, still rely on various forms of traditional medicine (Akerele, 1988) . In Africa, traditional healing systems exist in almost all countries. Table 2 shows medicinal roles of Z. mucronata in healing various health conditions in several African countries. Medicines, obtained from its roots, bark, leaves and/or fruits, are applied in various ways, usually as drinks, food and even as poultice. Common ailments treated using Z. mucronata include chronic cough, boils, toothache, rheumatism and swellings (Roodt, 1998; Iwalewa et al., 2007; Orwa et al., 2009 ). As noted by Pareek (2001) , most parts of the Ziziphus plants have medicinal value due to their inherent constituents. In particular, the traditional medicinal use of Z. mucronata can be attributed to the various cyclopeptide alkaloids it contains (Table 3) (Auvin et al., 1996; Pareek, 2001) . These include mucronines A -H (Moloto, 2004) , the recently discovered mucronine J (Auvin et al., 1996) , abyssenine A and frangufoline (sanjoinine A) which are isolated from the bark of its stem, root bark, roots and leaves (Auvin et al., 1996; Tan and Zhou, 2006) . The frangufoline (sanjoinine A), possessing a strong sedative property, has attracted increasing attention in chemical investigations of natural products since the mid 1960's (Tan and Zhou, 2006) . Together with mucronines F-H found in the bark of Z. mucronata stem, they give this traditional medicinal plant its antibacterial properties (Tan and Zhou, 2006) . McGaw et al. (2007) also support the antibacterial activity of Z. mucronata in a study using Escherichia coli, Enterococcus faecalis, Pseudomonas aeruginosa and Staphylococcus aureus bacterial strains in leaf extracts. The average antibacterial activities for these bacterial strains, expressed in minimum inhibitory concentration in mg·mL −1 , were > 7.1 in methane, > 7.8 in hexane and > 12.5 in water. For P. aeruginosa and E. coli, the antibacterial activity was more than 12.5 mg·mL −1 in all three extracts, while E. faecalis and S. aureus recorded 12.5 mg·mL −1 in water and 3.1 mg·mL −1 in hexane . A study by Moloto (2004) provides similar support for the use by traditional medical practitioners to treat bacterial infections such as gonorrhea, syphilis, cholera, dysentery and boils using Z. mucronata extracts, as shown in Table 2 . In addition, Z. mucronata has antifungal and antiplasmodial properties, probably due to the tetracyclic triterpenoid saponins and flavonoids in its fruits (Prozesky et al., 2001; Pillay et al., 2008) . The species is reported to have a high antisickling activity as well. Based on Mpiana et al. (2008) , the antisickling property arises from anthocyanins, extracted from its roots and bark. The bark of Z. mucronata has 12%-15% tannin (Orwa et al., 2009) , an astringent often used to treat diarrhea. Moreover, Ziziphus species, Z. mucronata included, commonly have a lot of vitamin C. Its concentration ranges from 70 to 165 mg per 100 g (Bal and Mann, 1978) , which is beyond the 30 mg daily intake recommended by Passmore et al. (1974) for adults. While some cyclopeptide alkaloids in the Rhamnaceae family, including the ones specifi ed for Z. mucronata, have shown antibacterial, antifungal, antiplasmodial and sedative activities, there have not been any potential applications of cyclopeptide alkaloids in new drug research and development (Tan and Zhou, 2006) . Therefore, this remains to be explored in the future. Due to its abundance, Z. mucronata is also a valuable source of food for all browsers such as giraffe, springboks, antelopes, black rhinos and elephants (Setshogo and Venter, 2003; Shackleton et al., 2005; Orwa et al., 2009 ). Its highly nutritious fruits are usually eaten by monkeys, baboons, warthog and birds. The fruits can be made into porridge and flour once they are dried and grounded (Roodt, 1998) . Sometimes the fruits are sucked by children and are reportedly sold in rural markets in Zimbabwe (van Wyk and Gericke, 2000) . If fermented properly, the fruits can also be made into a traditional beer (Setshogo and Venter, 2003) . Though rarely practiced, the seeds can be used as a coffee substitute (Maundu et al., 1999; Shackleton et al., 2005) . The leaves are edible and young ones can be cooked and eaten as spinach. They play a central role in the nutrition of larval caterpillars, such as Tuxentius melaena, T. calice calice and Zintha hintza (Orwa et al., 2009) . Z. mucronata are also used in Kerharo and Adam, 1974 Syphilis, gonorrhea Bark of underground parts, sap Bark powdered and locally applied, sap applied locally Kerharo and Adam, 1974 Urogenital infection, bilharzia, schistosomiasis Fruits Infusion taken orally Kerharo and Adam, 1974 (To be continued) Gelfand et al., 1985 Arthritis, cramp, kidney pain, lameness, rheumatism, muscular infl ammation Bark, branches, roots Infusion applied on scarifi cations, infusion taken orally Gelfand et al., 1985 Diarrhea, tape worms, malaria, hypertension, syphilis, gonorrhea, urinary, gynecological complaints Bark, leaves, roots NS* Palmer and Pitman, 1972; WHO/DANIDA, 1991 Note: NS*, not specifi ed. connection with burial rites by the Zulu tribe in South Africa and the Swazi tribe in Swaziland (Shackleton et al., 2005) . In Botswana as well as in most parts of South Africa, it is believed that Z. mucronata is immune against lightning, so anyone sheltering under it in a storm is considered to be safe. In rural areas, the termite resistant timber from Z. mucronata trees is used for a variety of household items such as tables, chairs, spoons and dishes (Palmer and Pitman, 1972) . The wood of Z. mucronata is fairly dense and can be used to make long burning fi rewood and charcoal. Z. mucronata is also commonly used as a live fence, for instance in schools and gardens, as well as a form of protection against animals in fi elds, homesteads and kraals, at least for 10 years before the crown is too high off the ground to act as a barrier (World Agroforestry, 2010). Moreover, Z. mucronata is considered to be a good indicator of underground water in areas where it naturally occurs (Setshogo and Venter, 2003) as well as a valuable source of nectar by beekeepers (Orwa et al., 2009) . Species in the genus Ziziphus are increasingly becoming popular due to their outstanding advantages, such as early bearing, high fruit yield, rich nutrition, multiple uses, long flowering season and high tolerance to drought and barren soils (International Centre for Underutilized Crops, 2001; Liu and Zhao, 2009 ). In addition to Z. mucronata, several other Ziziphus species are exploited for medicinal use in other parts of the world as well. Examples include Z. jujuba, Z. mauritiana and Z. spina-christi. Medicinal uses of these three species are generally similar to those of Z. mucronata in Africa. The fruits, leaves and seeds of Z. jujuba are commonly used in China to treat illnesses, such as irritability, insomnia, heart palpitations, constipation, lack of appetite, inflammation, sore throat and shortness of breath (Zhu, 1998; Azam-Ali et al., 2006; Jiang et al., 2007; Naftali et al., 2008) . Similar diseases treated with Z. mucronata in Africa cover psychiatric cases in Mali, rheumatism in Kenya and South Africa as well as measles in Botswana. Just like Z. mucronata, Z. jujuba possesses saponins which have some sedative effects. The saponins in Z. jujuba are ziziphin and jujubosides A and B, acetyljujuboside B and protojujubosides A, B and B1 (Azam-Ali et al., 2006) . In addition, this species also contains triterpenoic acids (e.g. oleanolic acid, betulonic acid, oleanonic acid and colubrinic acid) and some phospholipids (Lee et al., 2003; Jiang et al., 2007) . Some medicinal uses of Z. mauritiana in India are similar to those of Z. mucronata in Africa. These include the treatment of diarrhea, dysentery, nausea, vomiting, mental retardation, rheumatism, ulcers, wounds and fever (Ara et al., 2008) . The plant parts used in treatments are leaves, roots, seeds, bark and in some instances, fl owers. Alkaloids, such as mauritines A-H and J, amphibines B and D-F, frangufoline, hysodricanin A, scutianin F and aralionin C, are examples of cyclopeptide alkaloids found in Z. mauritiana (Jossang et al., 1996) . Moreover, traditional medicinal uses of Z. mucronata are comparable to those of Z. spina-christi. For instance, based on Dafni et al. (2005) , Z. spina-christi in Morocco is similarly used in snake bite treatments as Z. mucronata in Benin, Tanzania and Zimbabwe (Table 2) . Other ailments, such as arthritis, muscle pains, chest pains, headache, colds, measles, swollen organs and liver problems, treated with Z. spinachristi (Dafni et al., 2005) , are in certain African countries cured using Z. mucronata ( Table 2 ). The active components of Z. spina-christi include zizyphine F, Auvin et al., 1996; Tan and Zhou, 2006. jubanine A, amphibine H and spinanine A (Shappira et al., 1990) . Therefore, in view of these similarities, Z. mucronata is an equally potential source of medicine. The -Ali et al., 2006) . In South Korea, it has become a commercially cultivated fruit tree. In 2006, it was grown on roughly 150 million ha of land in China, with production of 3.05 million tons on a fresh weight basis, accounting for 99% of world production (Liu and Zhao, 2009) . Chinese date (jujube) is eaten as fresh fruit, or dried and soaked in water before use in savory and sweet dishes. A wine made from Z. jujuba fruits called "hong zao jiu" is also produced in China. In Korea, jujubes are called "daechu" and used in teas to help cure the common cold. Similar to Z. jujuba, Z. mauritiana (Indian jujube) is mainly cultivated for its fruits in India (Pareek, 2001) . It is one of the 17 Ziziphus species found in India (Ara et al., 2008) . Z. mauritiana is native from Yunnan Province, China, to Afghanistan, Malaysia and Australia (Kaaria, 1998) . It is also found in the Bahamas, Fiji, Colombia, Philippines and Venezuela. In 1939, six trees from Malaysia were introduced into Israel and fl ourished there. The USA has also imported germplasm of Z. mauritiana and a small number of trees are cultivated in southern Florida (Azam-Ali et al., 2006) . Between 1994 and 1995, 0.9 million tons of Z. mauritiana fruits were produced in India from an area of 88000 ha. Z. mauritiana can produce an annual fruit yield of 50-250 kg·tree −1 and is relatively easy and inexpensive to cultivate (International Centre for Underutilized Crops, 2001). Among India, Thailand and Pakistan, only Thailand exports Z. mauritiana fruits to the Middle East, Malaysia and the Far East throughout the year. About 175000 tons of Z. mauritiana fruits have been produced in Thailand between 1989 (International Centre for Underutilized Crops, 2001 . The ripe fruits of Z. mauritiana contain large amounts of vitamins A and C and are mostly eaten raw in India and sometimes stewed. In Indonesia, young leaves are cooked and eaten while in Venezuela, a jujube liqueur is made and sold. Z. mauritiana is also a source of fodder for cattle, sheep and goats. Plants have long provided mankind with herbal remedies for many infectious diseases and even today, they continue to contribute immensely as primary health remedies in developing countries. From a research and development point of view, many Ziziphus species have not received any major emphasis from governments and as such, they remain underutilized (Azam-Ali et al., 2006) . Nonetheless, we have shown that they serve valuable medicinal and cultural roles to millions of people. Z. mucronata helps in the treatment of diseases such as diarrhea, syphilis and gastric ulcers. It also helps heal boils, wounds and hypertension in many African countries. Moreover, it provides food to animals as well as material for handicrafts to local people in various African countries. As such, there is a need to preserve this species in order to ensure its lasting supply to local communities. Some possible conservation strategies are mentioned below. If Z. mucronata is to be maintained as a renewable resource, more domestication initiatives such as those taken for Z. jujuba and Z. mauritiana can be employed. This will likely take pressure off the existing wild stocks. Additionally, Z. jujuba, Z. spina-christi and Z. mauritiana have been successfully introduced in areas outside their natural habitats. They widely occur in almost all continents. Attempts can be made to introduce Z. mucronata to other continents as well, since it can tolerate various environmental conditions, just like the Ziziphus species mentioned earlier. Presently, the distribution of Z. mucronata is mainly restricted to Africa. Furthermore, to maximize the use of Z. mucronata, collaboration among nations is crucial in enhancing scientific research on the pharmacological potential of this species in the global market. A number of the traditional medicinal uses of Z. mucronata in various African countries are similar to those of the widely recognized Z. jujuba and Z. mauritiana. This indicates that with more research, Z. mucronata can be economically valuable as well. Compared to India and China, many African countries still have much to do in terms of effectively inte-grating medicinal plants and the associated indigenous healthcare knowledge in modern healthcare systems. To achieve this, the preservation and documentation of indigenous medicinal knowledge related to medicinal plants, i.e., Z. mucronata, with the involvement of traditional medical practitioners is vital. 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