Indian Journal of Traditional Knowledge Vol. 12(2), April 2013, pp. 195-201

Marketable wild of Sarawak, Borneo: Their mode of consumption, uses and sugar profiles

S Muhd Arif Shaffiq 1*, B Japar Sidik 1, Z Muta Harah 2 & R Shiamala Devi 1 1Department of Animal Science and Fisheries, Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia Bintulu Sarawak Campus, 97008 Bintulu, Sarawak, Malaysia 2Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia E-mail: [email protected]

Received 21.06.12; revised 28.08.12

Eleven wild species documented with fruits mainly used for food and other uses were based on the acquired knowledge passed from elders that has provided local people with wide selection of in their diets. Based on the information obtained, 11 wild species were investigated for their sugar concentrations. Taste preference (e.g., mainly sweet, sour, bitter), flavour and ripeness were observed to be important for mode of consumption and uses. HPLC method was used to quantify the major sugars in the fruits. The retention times of sucrose, glucose, and fructose measured were 10.3, 12.7, and 15.1 min, respectively. Artocarpus odaratissimus has significantly high amounts of glucose (39.9 gm kg-1 DW) and fructose (48.5 gm kg-1 DW) whereas indum and magnifica had higher sucrose contents in comparison with other wild fruits. Etlingera elatior was found to have the lowest sugar content. Multivariate analysis (PCA) showed 3 groups of fruits species can be separated based on their sugar contents. With respect to glucose/fructose ratio, Artocarpus odoratisimus and Dialium indum have high amounts of fructose, which may induce fructose malabsorption if taken in excessive amount. Information on the wild plant species and their fruit sugar content is essential to determine their potential for further market utilization and human consumption.

Keywords: HPLC, Sarawak, Sugar-Pak I, Sugar profile, Wild fruits IPC Int. Cl.8: A61K 36/00, A01G 17/00, B65B 25/01, A01D 46/00, A23B 7/00, A23, C08B, A47G 19/26, A47J 39/02, C07H 5/06, C07H 1/00, C13B 30/14

Borneo, the largest island in the world, has about their fruits determine the selection and mode of 3,000 species of diverse plants of which more than consumption or uses. Wild fruits are usually small in 265 species are dipterocarps and about 155 are size, but are high in fibre content. They often taste endemic to Borneo1. Sarawak, which is a part of sour or even astringent and therefore, are considered Borneo, has a vast tropical rainforest covering an area to have low sugar levels as compared to other of 8,700,000 hectares, which mainly contributes to the cultivated fruits4. Wild fruits are a source of food unique and bizarre plant diversity of Borneo. Forests and income for rural people since they are have always been an indispensable source of food, available in large quantities and are seasonally shelter, and income to the local people residing at its traded in local markets. Wild fruits have reportedly vicinity. Some wild plants and fruits serve as a source high amounts of vitamins and minerals, relatively of food in local community diets. These supplement lower amounts of carbohydrate and calories, and are other food sources, particularly seasonal agricultural free of any synthetic chemicals5. Significant amounts crops and sometimes are even used as emergency of high sugar contents have also been recorded in food supplies, like in conditions of drought and wild cultivars (e.g., in Laurocerasus officinalis) as war 2, 3. Acquired knowledge passed from elders on compared to the cultivated ones, which suggests the wild plants has provided the local people with use of wild fruits as a good source of free sugar wide selection of plants and fruits in their diets. Taste in our diet6. (e.g., sweet, sour, bitter) and flavour of plants and Carbohydrates are a major component and are —————— usually the structural block of plants. They provide *Corresponding author energy and serve as preparatory materials for the 196 INDIAN J TRADITIONAL KNOWLEDGE VOL 12, NO. 2 APRIL 2013

biological synthesis of other constituents in the Willughbeia augustifolia (Miq.), Mangifera pajang human body7. Generally, our food contains two main Kosterm. (embang/embawang), Salacca affinis types of carbohydrates: simple carbohydrates (sugar) Griff. (asam ridan), Salacca magnifica J. P. Mogea and complex carbohydrates8 glucose, fructose, and (remayong), Durio kutejensis (Hassk.) Becc. (durian sucrose are the major constituents of fruit sugars. nyekak), Garcinia parvifolia Benth (asam kundong), Fructose naturally occurs in all fruits as a free Dialium indum L. (keranji), Artocarpus odoratissimus reducing sugar and is considered as the sweetest Blanco (terap), Xanthophyllum escarinatum Chodat sugar. Sucrose is prevalent in almost all plant (langgir), Vitis triloba Roth (lakum/lakom), and kingdoms whereas glucose is synthesized during Etilengera eliator (Jack.) R.M. Smith (kantan, kechala). photosynthesis and is stored in the form of starch in The study samples for sugar content analysis consisted plants9. Wild forest fruits are a free source of sugar of ripe fruits of 11 species of plants that are found in and energy to the local people. Moreover, their the forests of Sarawak, Borneo. availability in the market with affordable prices makes them cheap sources of energy for the rural Sample preparation people. The demand for wild fruits is limited in the All fruits were washed under the running tap water urban area due to their seasonal availability and to remove the dirt and soil. The edible parts of fruits limited commercialization of indigenous fruits10. were sliced and were dried in an air circulating oven Investigations on the sugar profiles of 19 Thai wild at 60ºC for 24 hrs. The dried fruit slices were then fruits in the Asian regions suggest that these fruits are separately ground into fine powders and were kept in a good source of free sugar11. Despite the potential of airtight containers and desiccators for further analysis. wild fruits, yet no studies have been conducted that Determination of sugar content by HPLC provide composition trends or content on the sugar, Extraction and separation of the samples were especially glucose, fructose, and sucrose levels, of carried out based on the Johansen et al.15 and Xiaoli et wild fruits found in Sarawak. al.16 method. One gram of each dried fruits were Wild plants species and their other components extracted in 10 ml of 80% ethanol (80 ml absolute such as fruits, leaves, twigs, flowers, barks and roots ethanol: 20 ml water) at 80ºC in a water bath for were consumed, traded and used for other purposes 60 min. The extracted solutions were centrifuged for such as medicine and household needs. It is hard to 20 min at 2500 x g. The supernatants were then distinguish the plant function either for food or evaporated till dryness in a water bath at 80ºC. The medicine and has been reflected in several studies that residues were then mixed with 0.5 ml of 0.001 M plants were consumed as food and also used for Ca-EDTA17. The prepared samples were then filtered medicine 12, 13, 14. Thus, the main objective of this through a 0.45 µm membrane filter (Advantec-mixed study was to record the mode of consumption of cellulose ester). selected marketable wild fruits available in local The calibration curves were obtained by preparing markets of Sarawak and estimate their sugar standard solutions of D (+) glucose, D (-) fructose, composition. A more detailed knowledge on the and D (+) sucrose (Sigma Chemical Co.) in 50 ppm variability of sugar contents of fruits could be a Ca-EDTA and ultra pure water. Concentrations of the desirable feature for breeding wild fruit selections standard solutions used in this study ranged from 0.05 with improved nutritional quality.

Methodology

Survey, study sites and sample collection Surveys pertaining to the local produce mainly wild fruits were recorded from the local markets of Sarawak, mainly from Bintulu, Sibu, Sarikei, and Lundu (Fig. 1). The surveys obtained from local traders and suppliers provided information on 11 species in 10 families of diverse wild plants, components utilized and, their mode of consumption Fig. 1—Map of Sarawak showing location of native markets and uses. The wild fruits belonged to the species surveyed. MUHD ARIF SHAFFIQ et al. : MARKETABLE WILD FRUITS OF SARAWAK, BORNEO 197

to 1.00 mg ml-1. Soluble sugars were then analyzed by (sucrose) were found in the fruits (Table 2). Results the high-performance liquid chromatography (HPLC) indicated that the sugars commonly found in all fruits method (Waters Alliance 2695). The HPLC was fitted were glucose and fructose ranged from 2.1 to 39.8 gm with a controller (Waters Delta 600 pump) and an kg-1 dry weight (DW) and 1.9 to 48.5 gm kg-1 DW, inline degasser-AF (Waters) connected with a respectively. Previously published literatures also refractive index (RI) detector (Waters 2414) using a indicate that glucose and fructose are higher as Sugar-Pak I column (Waters). The mobile phase compared to sucrose in Thai wild fruits11. Some reports (0.001 M Ca-EDTA in ultra pure water) was pumped have recorded high amount of fructose and glucose in through the column at a flow rate of 0.4 ml per min. wild fruits. In the 13 sweet cherry cultivars of Slovenia, The temperature of the column was set at 70ºC and of glucose is predominant followed by sucrose21. As ripe the RI detector at 40ºC. The amounts of soluble fruits were used in this study (except V. triloba), the sugars were identified based on their retention times. high contents of fructose and glucose may be attributed The standard retention times for sucrose, glucose, and to the hydrolysis of sucrose during ripening22. fructose are 10.3, 12.7, and 15.1 min., respectively. Generally, the fruits with high content of fructose and These sugars were further quantified based on the glucose are consumed raw by the locals, however, standards: D (+) glucose, D (-) fructose, and D (+) fruits with lower content of this sugar usually mixed in sucrose (Sigma Chemical Co.). cooking or eaten with other ingredients. High contents of glucose (39.9 gm kg-1 DW) and fructose (48.5 gm kg-1 Statistical analysis DW) were detected in A. odoratissimus while Sugar contents of the 11 fruit species were other fruits were found to have substantially low compared by using one way analysis of variance contents of glucose (Fig. 2). Artocarpus odoratissimus (ANOVA) and Duncan’s New Multiple Range Test fruit has a pleasant aroma and a sweet taste23 and ripe (DNMRT) using the Statistical Analysis System fruits are eaten fresh. Sucrose levels were significantly (SAS) for Windows software (Version 9.00). higher at p<0.05 in D. indum (17.1 gm kg-1 DW) Principle component analysis based on Bray Curtis whereas V. triloba (2.3 gm kg-1 DW), S. affinis similarity index was carried out using PRIMER 5 (1.9 gm kg-1 DW), G. parvifolia (1.9 gm kg-1 DW) (Version 5.2.8) to obtain the relationship between and E. eliator (1.3 gm kg-1 DW) contained low sugar components and wild fruits species. amounts of sucrose, fructose and glucose. Results indicated that sweeter fruits contain more amounts of Results and discussion fructose and glucose and usually eaten fresh. Sugar Wild fruits traded in the markets are possessing contents in wild fruits ranged from 101.6 gm kg-1 DW mixtures of diverse taste from sweet, sour to bitter. (A. odoratissimus) to 5.3 gm kg-1 DW (E. eliator) The uses of the plants’ fruit, their other components (Fig. 2). Several factors, such as seasonal variations, and, mode of consumption and uses based on the local soil types, fertilizers, environmental conditions and knowledge are summarized in the (Table 1). Fruits genetic factors, contribute to the sugar level in fruits24. with sour or bitter taste are still traded in the market The carbohydrate component of fruits is one of the due to their importance for flavouring in the local main indicators of the fruit’s sweetness parameter25. cooking recipes. Wild plants are not only consumed Wild plants are not cultivated by human, thus their for their fruits, they also have other variety of quality is usually based on their selection process traditional uses derived from the leaves, flowers, during harvesting. Consumer preferences of fruits are and barks used as food and to treat ailments. based on the sweetness, acidity, and characteristic Traditional knowledge passed from elders supported flavours of fruits26. Therefore, the market availability the local people of the different mode of consumption of wild fruits depends mainly on consumer demands and uses of the plants’ fruits and other components. and the selection procedure made by rural people For example, E. eliator and V. triloba fruits are used (fruit sellers) based on their knowledge of the edible as flavouring in cooking. Furthermore, V. triloba can wild fruits. Some consumer tends to buy exotic fruits caused irritation of the mouth if consumed raw. Some due to the uniqueness taste of the fruits. Consumption of the plants are also used as body and hair care such of fruits and vegetables render excellent health and as X. escarinatum dried exocarp is used as shampoo. help in preventing diseases. Fruits are also proven to Significantly different (p<0.05) contents of reducing reduce the risk of obesity27 and lowering the risk of (glucose and fructose) and non-reducing sugars coronary artery disease28. 198 INDIAN J TRADITIONAL KNOWLEDGE VOL 12, NO. 2 APRIL 2013

Table 1—Mode of consumption and uses of the wild fruits and plants’ other components by the locals Family/ species Vernacular Parts used Mode of consumption and uses Data obtained from name/Tribe Apocynaceae Willughbeia augustifolia Akar kubal Fruit Fruits are sweet and consumed raw. The current study (Miq.) Mgf. (Iban) Anarcadiaceae Mangifera pajang Kosterm. Mawang Fruit Ripen sweet fruits are consumed raw. The current study (Iban), Ripen sour fruits are usually consumed embang with condiments e.g., mixture of sugar (Malay) and dried chilli powder. Young fruits are eaten as salad. Boiled ripe exocarp is eaten as salad. Leaves Young leaves are eaten as salads and The current study vegetables. Leaves Leaf extracts are used in the treatment Mat Salleh and Latiff (2002)18 of cholera while the root sap is used to induce appetite. Bark Decoctions of the bark are used in the Mat Salleh and Latiff (2002)18 treatment of stomach ache and cholera. Latex Latex is used in the treatment of skin Mat Salleh and Latiff (2002)18 diseases, such as fungal infection and ringworm. Salacca affinis Griff. Ridan Fruit Fruits are sour and seldom consumed The current study (Iban) fresh. The locals usually consumed the arils with pounded fermented shrimp paste and fresh chilli. Salacca magnifica Remayong Fruit Fruits have a slight bitterness taste The current study J. P. Mogea (Iban) and are consumed raw. Bombaceae Durio kutejensis (Hassk.) Durian nyekak Fruit Fruits are sweet and consumed raw. The current study Becc. (Malay) Do not have strong smell as compared to common durians (Durio zibethinus). Clusiaceae Garcinia parvifolia Benth. Buah kuno Fruit The white sweet flesh of the fruit is The current study (Iban), consumed raw and the dried fruit asam kundong exocarp is used as a flavouring agent (Malay) in cooking due to it sourness. Leguminosae Dialium indum L. Keranji (Malay) Fruit The tangy powdery orange flesh is The current study eaten raw. Moraceae Artocarpus odoratissimus Terap (Malay) Fruit Ripe arils are very sweet and The current study Blanco consumed raw, Young fruits are usually eaten as vegetables. Seed are boiled or roasted and are eaten as a snack as they have a nutty taste. Leaves Ash obtained from leaves is used as Chai (2006)19 an antidote for centipede bites and scorpion stings. Hanging the leaves on the door of the house will dispel malevolent spirits. (Contd.)

MUHD ARIF SHAFFIQ et al. : MARKETABLE WILD FRUITS OF SARAWAK, BORNEO 199

Table 1—Mode of consumption and uses of the wild fruits and plants’ other components by the locals (Contd.) Family/ species Vernacular Parts used Mode of consumption and uses Data obtained from name/Tribe Polygalaceae Xanthophyllum escarinatum Langgir Fruit, The white sweet flesh of the fruit is The current study Chodat (Iban,Malay) dried eaten raw. The exocarp of the fruit exocarp is dried and used as a hair and body shampoo. Fruit Ash of the fruit is used to treat Chai (2006)19 unidentified body pains while ash obtained from twigs are used as a pesticide. Vitaceae Vitis triloba Roth Lakom/ lakum Fruit Fruit is usually used as a flavouring The current study (Iban) agent due to its sourness. Fruit is not consumed raw as it causes mouth irritation. Zingiberaceae Etilengera eliator (Jack.) Kechala (Iban), Fruit Fruits are sour, mixed with other The current study R.M. Smith kantan (Malay) vegetables or added as flavour in cooking. Decoction of the fruits are usually Burkill (1966)20 used as ear drops. Leaves Young leaves are consumed as salad. The current study Flower Flowers are usually used as a The current study flavouring agent in cooking for aroma, believed to induce the appetite. Flower Women consume the flowers to Mat Sallleh and Latiff (2002)18 prevent ageing. Rhizome Rhizomes are eaten with betel leaves Mat Sallleh and Latiff (2002)18 to reduce bloating in conceived woman.

Table 2—Composition and content of sugars in fruits of 11 wild plant species. Family/ scientific name Individual sugar ( gm kg-1 DW) Glucose/Fructose Total Sugar (gm kg-1 DW) Sucrose Glucose Fructose Apocynaceae Willughbeia augustifolia (Miq.) Mgf. 3.8±0.01F 7.8±0.01B 7.2±0.01B 10.8±0.01BC 18.9±0.01BC Anarcadiaceae Mangifera pajang Kosterm. 10.4±0.03E 6.6±0.04BC 6.8±0.03B 9.6±0.03BCD 3.9±0.10BC Arecaceae Salacca affinis Griff 1.9±0.003D 4.7±0.04CDE 4.6±0.04BC 10.2±0.03CD 11.2±0.08D Salacca magnifica J. P. Mogea 15.0±0.05B 4.7±0.05CDE 5.1±0.01BC 9.2±0.06CD 24.7±0.05BC Bombaceae Durio kutejensis (Hassk.) Becc. 13.0±0.04CD 2.3±0.03E 2.5±0.02C 9.0±0.07CD 17.8±0.08C Clusiaceae Garcinia parvifolia Benth. 1.9±0.01G 5.2±0.08BCD 3.7±0.05BC 14.1±0.06A 10.8±0.14D Leguminosae Dialium indum L. 17.1±0.01A 4.0±0.01CDE 4.8±0.01BC 8.4±0.02D 25.9±0.03B Moraceae Artocarpus odoratissimus Blanco 13.2±0.07C 39.8±0.24A 48.5±0.55A 8.2±0.06D 101.6±0.31A Polygalaceae Xanthophyllum escarinatum Chodat 11.8±0.10D 4.5±0.05CDE 5.0±0.03BC 8.8±0.05D 21.3±0.16BC Vitaceae Vitis triloba Roth 2.3±0.02G 3.1±0.01DE 2.9±0.03C 10.9±0.09B 8.3±0.04D Zingiberaceae Etilengera eliator (Jack.) R.M. Smith 1.3±0.01G 2.1±0.05E 1.9±0.06C 11.5±0.17B 5.3±0.13D Note: The data presented here represents samples ± standard error (SE). Different superscript alphabet within the column indicate significant values at p<0.05.

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Fig. 3—The distribution of the 11 wild fruits against the first Fig. 2—Composition and content of sugars in the selected 11 wild two PC’s scores. I, II, III are group based on Bray Curtis fruit species of Sarawak. similarity index. ([1] Willughbeia augustifolia, [2] Mangifera pajang, [3] Salacca affinis, [4] Salacca magnifica, [5] Durio Table 3—Principal components analysis: Eigenvalues and kutejensis, [6] Garcinia parvifolia, [7] Dialium indum, percentage of variation described by the first four components. [8] Artocarpus odoratissimus, [9] Etilengera eliator, [10] Vitis triloba, [11] Xanthophyllum escarinatum). PC’s Eigenvalues %Variation Cum.%Variation 1 3.12 78.0 78.0 Table 4—Eigenvectors for variables used in PCA of the sugar 2 0.87 21.9 99.9 composition data, indicating the strengths of the correlations 3 0.00 0.1 100.0 between variables and the principle components (axes). 4 0.00 0.0 100.0 Variables PC1 PC2 PC3 The 11 wild fruits were ordinated with PCA using Sucrose -0.262 0.948 0.173 4 variables (sucrose, fructose, glucose and total sugar). Glucose -0.551 -0.245 0.260 In a principal component analysis the first three Fructose -0.555 -0.204 0.490 principal components explained 100.00% of the total Total sugar -0.566 0.000 -0.814 variance with PC1, PC2 and PC3 accounted 78.0%, 21.9% and 0.1% respectively of the total variations The glucose/fructose ratio of the 11 fruits, found in (Table 3). Since PC3 showed low contribution to the this study, ranged from 1.41 to 0.80. A higher ratio total variation, it is not discussed further here. The was found in A. odoratissimus (0.84), X. escarinatum eigenvectors of the 4 variables were presented in (0.88) and D. indum (0.82), while a lower ratio Table 4. In PC1 there were negative relations for all of 1.41 was observed in G. parvifolia. The ratio the variables. However, sucrose and total sugar were greater than 1 indicates a higher proportion of positively correlated with PC2 while glucose and glucose/fructose and vice versa. The glucose/fructose fructose showed negative relationship. Based on the ratio is important for determining the amount of Bray-Curtis Similarity index at 50% similarity, 11 wild free fructose in fruits. This information may help fruits were grouped into 3 main groups (I, II and III) us to avoid fruits having high fructose levels as (Fig. 3). The first group was A. odoratissimus (8), consumption of a high fructose diet may induce 29 which has higher glucose and fructose content. The fructose malabsorption in humans . second group comprising M. pajang (2), S. magnifica (4), D. kutejensis (5), D. indum (7) and E. eliator (9) Conclusion have higher value of sucrose while W. augustifolia (1), The documentation on the 11 wild plant species, S. affinis (3), G. parvifolia (6), V. triloba (10) and their mode of consumption and uses are important in X. escarinatum (11) were clustered together in the order to conserve and preserved the local knowledge third group consist of low sugar content fruits. The from cultural erosion. The results of the current study results also indicated that S. affinis and S. magnifica suggest that these 11 wild fruits are a good source of were clustered in different group even though they are sugar and energy. Information on the sugar profiles of from the same family. This indicated that sugar content wild fruits can help agronomists in determining the of the fruits was not dependable on the family. potential of the wild fruits as a new crop. Results also MUHD ARIF SHAFFIQ et al. : MARKETABLE WILD FRUITS OF SARAWAK, BORNEO 201

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