Mutation Research 523–524 (2003) 109–117 Review Potential functional foods in the traditional Maori diet Richard C. Cambie a , Lynnette R. Ferguson b,∗ a b Department of Chemistry, The University of Auckland, Private Bag 92019, Auckland, New Zealand Department of Nutrition, The University of Auckland, Private Bag 92019, Auckland, New Zealand Received 8 January 2002; received in revised form 26 July 2002; accepted 23 August 2002 Abstract The Maori people were early New Zealand settlers of Polynesian descent. The incidence of non-infectious diseases appears to have been low in these people, perhaps in part due to the presence of protective chemical constituents within their food plant supply. Three of the tropical crops they introduced are still eaten here today: the sweet potato or kumara (Ipomoea batatas), the taro (Colocasia esculenta) and the cabbage tree or ti (Cordyline terminalis). Sporamins A and B, the major storage proteins of kumara tubers, act as proteinase inhibitors, and may have other anti-cancer properties. The tubers also contain the anti-coagulant coumarins, scopoletin, aesculetin, and umbelliferone. The corms of taro contain the anthocyanins, cyanidin 3-glucoside, pelargonidin 3-glucoside and cyanidin 3-rhamnoside, reported to have antioxidant and anti-inflammatory properties. Anthocyanins are also major components of a so-called “Maori potato”, a variety officially known as Ureniki, which has a purple skin and flesh and was widely eaten in the early 1900s. Anthocyanins are also present in ripe berries of the ramarama (Lophomyrtus bullata) and rohutu (Neomyrtus pedunculata). Both the leaves and seeds of the introduced cabbage tree (Cordyline terminalis) and the native Cordyline spp., C. australis, C. indivisa, and C. pumilo, were eaten. The seeds of C. australis, of some Astelia spp., and of hinau (Elaeocarpus dentatus) are good sources of various essential fatty acids, generally regarded as protective against cardiovascular disease. Shoots and leaves from a wide range of native species were traditionally eaten as greens, especially “sow thistle” or puha (Sonchus spp.), reportedly high in Vitamin C and various phenolics. “New Zealand spinach” (Tetragonia tetragonioides or T. expansa) has anti-ulcerogenic activity that has been traced to two cerebrosides and anti-inflammatory activity that has been traced to novel water-soluble polysaccharides, as well as antioxidant phenylpropanoids including caffeic acid. Leaves of the “hen and chickens” fern (Asplenium bulbiferum) contain antioxidant flavonoids such as kaempferol glucosides. Native seaweeds also have useful nutritive properties. © 2003 Elsevier Science B.V. All rights reserved. Keywords: New Zealand plants; Functional foods; Flavonoids; Polysaccharides; Antioxidants 1. Introduction The first humans to settle in New Zealand were Polynesians, later to be called Maori, who arrived between 1000 and 2000 years ago. The exact date is unknown but there is no hard evidence of settle∗ Corresponding author. Tel.: +64-9-373-7599x6372; fax: +64-9-373-7502. E-mail address: [email protected] (L.R. Ferguson). ment before a.d. 800 and recently the period a.d. 1000–1200 has been suggested. Early Maori obtained their food by hunting, fishing, shellfish gathering, gardening, and gathering native and semi-cultivated plants. However, in the temperate climate, gardening as practised elsewhere in Polynesia, was at best marginal and at worst impossible. There is considerable evidence to suggest that even in regions most amenable to horticulture, gardens contributed only about 50% of the means of subsistence [1]. 0027-5107/03/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0027-5107(02)00344-5 110 R.C. Cambie, L.R. Ferguson / Mutation Research 523–524 (2003) 109–117 Of the range of tropical crops that the Polynesian settlers probably tried to introduce, only six species survived until early European times, viz. the sweet potato or kumara (Ipomoea batatas; Fig. 2A and B), the taro (Colocasia esculenta; Fig. 2C and D), the “bottle gourd” or hue (Lagenaria siceraria), the cabbage tree or ti (Cordyline terminalis; Fig. 2E), the “paper mulberry” or aute (Broussonetia papyrifera), and the yam or uhi (Dioscorea alata and D. esculenta). Captain Cook in his journey of exploration in 1769 identified all six, but the yam and paper mulberry died out soon after [1]. The availability of food of the prehistoric Maori has been summarized by Young [2]. In this paper, our aim is to mention some of the early food plants and where possible, attempt to identify chemical compounds within them that may have contributed to their value as functional foods. The incidence of diabetes, cancer, and vascular-related diseases has been rising in Maori people over the last 30–40 years [3–6]. It may have been low in the early Maori settlers, due in part to the presence of protective chemical constituents within the plants that were eaten. Nevertheless, in prehistoric times the average age of the Maori at death has been estimated to be 31–32 years [7]. It has been suggested [8] that the possible carcinogenic effects of eating the root of bracken or aruhe (Pteridium esculentum) where the toxic principles have been identified as shikimic acid (1) and the sesquiterpenoid ptaquiloside (2) [9], contributed to this low age. However, the average age of death in prehistoric times in Europe, Asia, and America was also in the thirties [7,8], while cannibalism in New Zealand was also a hazard to longevity. 2. Starch sources Much has been written about the kumara which was by far the most important vegetable and the achievement of the early Maori in adapting it to an annual cycle in the temperate climate of New Zealand by storing the tubers in pits, is most impressive. Exactly how the kumara, an American plant, reached New Zealand or how its cultivation and storage in pits came about, remains a subject of speculation [1]. The chemical literature on the constituents of the tubers is extensive [10], and besides a series of stress metabolites (phy- toalexins), produced as a result of infection, injury, or fungicidal treatment, the major proteins which account for more than 80% of the total protein are sporamins A and B [11,12]. These are proteinase inhibitors and may have some anti-cancer properties [11]. The tubers also contain the coumarins scopoletin (3, R==H), aesculetin (3, R==OH), and umbelliferone (3, R==OMe), (Fig. 1) compounds which have anti-coagulation properties and which are reputed to inhibit HIV replication [13]. Taro roots are rich in starch (amylose, 28%, 4, and amylopectin, 72%, 5) [14] and the corms contain the anthocyanins, cyanidin 3-glucoside (6, R==OH), pelargonidin 3-glucoside (6, R==H), and cyanidin 3-rhamnoside (7) [14]. In common with flavonoids, the related anthocyanins are reputed to improve circulation by decreasing capillary fragility [15], to improve eyesight, to act as potent antioxidants, to act as anti-inflammatory agents, and to inhibit human cancer cell growth [16–18]. The corms of taro also contain calcium oxalate, an irritant, which prevents them being eaten raw or incompletely cooked [19]. Little is recorded about the use of the gourd as a food, its main use being the utilization of the shell as a container [20], but the cabbage tree (Cordyline terminalis) and the native Cordyline spp., C. australis (Fig. 2F), C. indivisa, and C. pumilo, were exploited for food. The inner blanched leaves and aerial stems were the parts generally eaten, although the white inner trunk and the fleshy taproot were also used [1]. The nutritive value of the edible portions have been analysed by Fankhauser (Table 1) [21]. Hydrolysis of the polysaccharides of the roots gives over 90% of fructose, which is sweeter than any other common sugar [8,22]. At its period of maximum polysaccharide production, C. australis contains more useable carbohydrate on a fresh weight basis than either sugar cane or sugar beet, and at one stage the cabbage tree was proposed as a commercial source of fructose [23]. With the arrival of the European, the potato (Solanum tuberosum; Fig. 2G) became the major vegetable of cultivation. In the early 1900s, there was interest in a so-called “Maori potato”, a variety officially known as Ureniki and which has small tubers with a purple skin and flesh (Fig. 2H). The colour is due to the presence of anthocyanins [24], the beneficial effects of which have been outlined above. R.C. Cambie, L.R. Ferguson / Mutation Research 523–524 (2003) 109–117 111 Fig. 1. Structures of the chemicals identified in the text. Shikimic acid (1), ptaquiloside (2), scopoletin (3, R==H), aesculetin (3, R==OH), umbelliferone (3, R==OMe), amylose (4), amylopectin (5), cyanidin 3-glucoside (6, R==OH), pelargonidin 3-glucoside (6, R==H), cyanidin 3-rhamnoside (7), ascorbic acid (8), cerebrosides (9, 10), caffeic acid (11), kaempferol glucosides (12), cinchophen (13), linoleic acid (14), karakin (15), ␥-linolenic acid (16), pantothenic acid (17). 3. Green leafy vegetables Andrew Crowe in his book “A Field Guide to the Native Edible Plants of New Zealand” [25] maintains that there are at least 190 edible native plants found in New Zealand, and that the early Maori used most of them. Shoots and leaves from a wide range of species were used as greens and chief among them was the “sow thistle” or puha (Sonchus asper). The introduced S. oleraceus (Fig. 3A) is still used today. The latter contains Vitamin C (ascorbic acid, 8) and phenolics and was used by Cook as an antiscorbutic [7]. Cook also collected boat-loads of “scurvy grass” (Lepidium oleraceum; Fig. 3C) [26] which is related botanically to water cress and which is a well-known antiscorbutic due to its Vitamin C content. Cook also 112 R.C. Cambie, L.R. Ferguson / Mutation Research 523–524 (2003) 109–117 Fig. 2. (A) Flowers and leaves, (B) edible portion of the kumara (Ipomoea batatas), (C) edible portion, (D) vegetative parts of the taro (Colocasia esculenta), (E) the introduced cabbage tree or ti (Cordyline terminalis), (F) the native cabbage tree (Cordyline australis), (G) flowers and leaves of the potato (Solanum tuberosum), and (H) S. tuberosum variety Ureniki. R.C. Cambie, L.R. Ferguson / Mutation Research 523–524 (2003) 109–117 113 Fig. 3. (I) puha (Sonchus oleraceus), (J) New Zealand spinach (Tetragonia tetragonioides), (K) scurvy grass (Lepidium oleraceum), (L) hen and chickens fern (Asplenium bulbiferum), (M) berries from the karaka tree (Corynocarpus laevigatus), (N) (Elaeocarpus dentatus), (O) Astelia trinerva, and (P) Porphyra columbina. 114 R.C. Cambie, L.R. Ferguson / Mutation Research 523–524 (2003) 109–117 Table 1 Food composition and nutritive value (%) of edible parts of Cordyline australis in relation to other starch sources commonly eaten in the South Pacific Food Water Ash Fat Carbohydrate Fibre Protein kcal/100 g kJ/100 g Potato Kumara Taro Yam Wheat-cooked Cordyline-root Cordyline-stem Cordyline-top 79.8 70.6 72.5 73.5 87.7 64.0 68.3 81.5 0.9 2.0 1.2 1.0 0.8 0.9 0.7 1.7 0.1 0.4 0.2 0.2 0.3 1.4 1.5 3.2 17.1 26.3 24.2 23.2 9.4 23.6 14.9 8.8 0.5 0.7 0.9 0.9 0.3 10.3 13.6 4.5 2.1 1.7 1.9 2.1 1.8 0.4 0.4 1.4 76 114 104 101 45 103 71 68 318 477 435 423 188 431 297 283 used the “New Zealand spinach” (Tetragonia tetragonioides or T. expansa; Fig. 3B), which has been shown to be effective against ulcer formation by sedative drugs [27]. It contains a number of compounds but the anti-ulcerogenic activity has been traced to two cerebrosides (9, 10), which are glycolipids [27]. The leaves also contain novel anti-inflammatory polysaccharides [28], saponins and phenylpropanoids, e.g. caffeic acid (11), which is an anti-hepatoxin [29]. Cook records [30] how he made a ‘Sour Kroutt’ from these plants and how he got his crew to eat it. “The Sour Kroutt, the men at first would not eat it, until I put it in practice—a method I never once knew to fail with seamen—and this was to have some of it dressed every day for the cabin table, and permitted all the officers, without exception, to make use of it, and left it to the option of the men either to take as much as they pleased or none at all; but this practice was not continued above a week before I found it necessary to put every one on board on an allowance; for such are the tempers and disposition of seamen. In general, that whatever you give them out of the common way— although it be ever so much for their good—it will not go down, and you will hear nothing but murmurings against the man who first invented it; but the moment they see their superiors set a value upon it, it becomes the finest stuff in the world and the inventor, an honest fellow.” The shoots and fiddleheads of the “hen and chickens fern” (Asplenium bulbiferum; Fig. 3D) were also eaten as a form of greens by the early Maori. The leaves contain flavonoids such as kaempferol glucosides (12) [31]. Several flavonoids show anti-inflammatory activity which is thought to be due to inhibition of some of the enzyme systems involved in the inflammation pro- cess. They also reduce the permeability and fragility of capillary walls, cause dilation of coronary blood vessels, have an anti-ulcer effect, have been used in the treatment of diabetes-related cataracts of the eyes, and exhibit both anti-viral and anti-cancer activity [16,29]. The leaves of Cordyline terminalis, eaten as a leaf vegetable commonly by the early Maori settlers, contain a compound closely related to cinchophen (13) which has antipyretic and analgesic properties [10]. The leaves also contain saponins, glycosidic compounds, which generally have antibacterial activity and various other beneficial properties [29]. 4. Seeds and berries The seeds of C. australis are one of the richest sources of linoleic acid (14), an “essential” fatty acid [32,33], the lack of which can give rise to skin complaints, and which is generally regarded to be a factor in heart disease [34]. The berries of numerous trees were consumed by the early Maori, but most have only a small amount of flesh surrounding the kernel or seed and a number have an undesirable turpentine flavour [35]. One exception is the berry from the karaka tree (Corynocarpus laevigatus; Fig. 3E) that, like the cabbage tree, was semi-cultivated. The outer flesh of the ripe orange berries is tasty but the bulk of the value is in the kernel, which is highly poisonous if eaten raw. The toxic principles are karakin (15) and four other related nitropropanoyl glucosides [36–38]. The kernels were steamed in an earth oven (hangi), steeped in running water, and then dried in the sun before use. This had R.C. Cambie, L.R. Ferguson / Mutation Research 523–524 (2003) 109–117 the effect of hydrolyzing the glycoside, thereby providing a rich source of carbohydrate. Ripe berries of the ramarama (Lophomyrtus bullata) and rohutu (Neomyrtus pedunculata) each contain anthocyanins [39], which are dealt with above. Colenso [40] rated hinau (Elaeocarpus dentatus; Fig. 3F) berries as the third most valuable food of the Maori. After separation of the stone, the flesh was moulded into a cake and cooked in a hangi. The flesh contains “essential” fatty acids [41] (see above). The berries of Astelia spp., e.g. A. solandri and A. trinerva (Fig. 3G), were eaten by the early Maori but there is no evidence to suggest that they were greatly valued. Up to 25% of the total seed oil is ␥-linolenic acid (GLA, 16) [42,43], which compares favourably with ca. 9% in the seeds of the evening primrose (Oenothera biennis), currently being actively promoted as a potential medicament for a range of medical conditions varying from pre-menstrual syndrome to multiple sclerosis [8]. GLA is an essential fatty acid required by the body as a metabolic precursor of prostaglandins, compounds which have a variety of beneficial functions. It is claimed that among other things, small doses of ␥-linolenic acid can overcome a deficiency caused by only using vegetable oils, can alleviate diabetes, and can slow the process of ageing [41,44]. The fatty acid profiles of the seeds and berries of a number of New Zealand native plants, some of which were eaten by the early Maori, is currently being examined in the Massey University Nutrition Laboratory, Institute of Food, Nutrition and Human Health. Seeds of New Zealand flax (Phormium tenax), rengarenga (Arthropodium cirratum), miro (Prumnopitys ferrugineus), and kohia (Tetrapthaea tetrandra) are reported to be good sources of linolenic acid while snowberry seeds (Gaultheria antipoda) are a rich source of ␣-linolenic acid [45]. 5. Seaweeds Seaweeds have received considerable attention in the search for native foods with beneficial nutritive properties. Their nutritional importance according to Crowe [25] lies mainly in their mineral content, especially as a rich source of iodine; seaweeds contain about 1000 times as much as any other food. Proteins 115 are usually about 10% of the dry weight although as much as 28% is present in one species, viz. karengo (Porphyra columbina; Fig. 3H) [25]. Seaweeds contain large amounts of carbohydrates, although only a fraction of algal carbohydrate is digestable. They are a good source of Vitamins A, B2 , B12 , and C, as well as sodium, potassium, and magnesium. They also contain pantothenic acid (17), a member of the Vitamin B complex, Vitamin D, and calcium. Early Maori made extensive use of seaweeds as a food but only a few species were eaten. Seaweed extracts such as agar, carrageen, furcellaran, and alginates are common ingredients of many foods [25]. The economic potential of seaweeds as a source of functional foods is discussed in “New Zealand’s Economic Native Plants” [8]. 6. Conclusions One fact that comes out of this survey is that few native plants have been examined for their nutritive value in any search for a useful food product. 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