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Original Article

Mangrove Fruit Bioprospecting: Nutritional and Antioxidant Potential as a Food Source for Coastal Communities in the Rawa Aopa Watumohai National Park, Southeast Sulawesi, Indonesia

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ABSTRACT

The present study aimed to identify the nutritional and antioxidant potential of mangrove fruits of Xylocarpus granatum, Sonneratia alba, and Bruguiera gymnorrhiza growing in Rawa Aopa Watumohai National (RAWN) Park. The protein content of X. granatum fruits (4.50 mg/g) was recorded to be higher than that S. alba (0.93 mg/g) and B. gymnorrhiza (1.09 mg/g), while the fat content in fruits of X. granatum (4.88%), S. alba (4.42%), and B. gymnorrhiza (4.74%) was similar. The total sugar content in fruits of X. granatum (14.8 mg/100 g), S. alba (14.9 mg/100 g), and B. gymnorrhiza (13.52 mg/100 g) was also similar. The ascorbic acid content in X. granatum fruit (65 mg/100 g) was higher than that in S. alba (40 mg/100 g) and B. gymnorrhiza (41.87 mg/100 g). However, the fruits of S. alba contained much higher micronutrients of Mn (0.063 mg/g), Zn (0.72 mg/g), and Fe (0.51 mg/g) than those of in X. granatum (0.052, 0.52, and 0.38 mg/g, respectively), and B. gymnorrhiza (0.012, 0.11, and 0.34 mg/g, respectively). Moreover, the fruits of X. granatum contained much higher macronutrients of K and Na compared to fruits of other mangroves. Thus, the findings of this study showed the promising values of all studied mangrove fruits as bio-nutrition and antioxidant sources, and high potentiality to use as renewable food sources for the coastal communities in RAWN Park.

Introduction

Mangroves are well known to play many important roles, such as providing carbon and nutrients in coastal areas that support primary and secondary production in nearshore waters, mitigate climate change through sequestration of CO2, and protecting human communities from devastating storms and tsunamis (Cebrian, Citation2002; Clough, Citation1998; Rivera-Monroy et al., Citation1995, Citation1998; Twilley, Citation1995). Mangroves are also an important source of food (Abeywickrama and Jayasooriya, Citation2010; Jariyah et al., Citation2014; Patil and Chavan, Citation2013), but studies have largely focused on fish, shrimp, and crabs harvested from and around these ecosystems. Recent studies show mangrove fruits to have potential as a basic ingredient in processed foods that is useful for the growth, development, and intelligence of human. Many people, especially coastal communities, in the Java Island have used mangrove fruits as raw material in processed foods, such as syrups and other types of food (Jariyah et al., Citation2014). In spite of these roles, few studies realized the potential uses of mangroves fruits as a food and nutritional source for the coastal community in the tropical region of this part of the world. With increasing human population alongside depleting natural resources, there is a need to explore the nutritive potential of mangroves to extend further their possible uses.

Mangroves are an abundant natural resource in the Rawa Aopa Watumohai National (RAWN) Park, Southeast Sulawesi, Indonesia that supports high levels of plant diversity. Mangrove species found there include Rhizophora apiculata, R. mucronata, R. stylosa, Ceriops tagal, Xylocarpus granatum, X. moluchensis, Bruguierra gymnorrhiza, B. parviflora, Sonneratia alba, Avicennia alba, A. officinalis, Lumnitzera racemosa, and L. littorea (Analuddin et al., Citation2013). These trees produce many fruits annually and thus have the potential to provide a nutritious food source to local communities Southeast Sulawesi coastal areas, while the fruits of X. granatum, S. alba, and B. gymnorrhiza have been known to be used in the past as food source. Although the RAWN Park is an important conservation area that is under protection by the government, the sustainable harvesting of mangrove fruits would have a minimal effect on their natural regeneration, provide an alternative food resource, and reduce extraction/degradation of mangrove forests into other land uses by providing a lucrative alternative source of income to the local communities.

Previous studies conducted in Southeast Sulawesi have quantified mangrove biomass and carbon stocks, the potential uses of mangrove leaves as a green tea or other medicinal values, and the role mangroves play as a biofilter of heavy metal pollutants (Analuddin et al., Citation2016, Citation2017, Citation2018; Septiana et al., Citation2016). Our study on the value of mangrove fruits as a potential food resource would further contribute toward the sustainable management of mangroves ecosystem in this region as intact forests would provide a long-term sustainable income source rather than cutting trees down for unsustainable and short-term income from aquaculture ponds and illegal logging. Therefore, the findings from this study will provide a greater priority for the conservation of a larger area of mangrove forest located outside the Park. This study is also important as there has been no information about the nutritional value and antioxidant potential of the various mangrove fruits growing in the RAWN Park, knowledge which is crucially important for the sustainable management of intact and restored mangrove forests in this region and throughout South East Asia. The main objectives of this study were to: (1) determine the nutritional and antioxidant contents in fruits of several mangrove species growing in the RAWN Park and (2) identify the bioprospecting values of the mangrove fruits as a food source for the local community in the coastal region of the RAWN Park, Southeast Sulawesi, Indonesia.

Material and Methods

Study Site

The RAWN Park is located at the eastern part of the Kendari city (S: 04°33ʹ12.1″ and E: 122°0.3ʹ20.4″), Southeast Sulawesi, Indonesia. The mangrove forests in this Park cover about 6,000 hectares and are in pristine conditions and undisturbed by human activities. The Lanowulu and Roraya Rivers flow through the park providing freshwater, nutrients, and sediments that result in productive and well-developed mangroves (Rahim, Citation2015).

A high diversity of mangroves were found in the protected areas of the RAWN Park including Rhizophora sp, Bruguiera sp, Ceriops sp, Lumnitzera sp, Xylocarpus sp, Sonneratia sp, etc. (Analuddin et al., Citation2013). Degradation occurs in unprotected mangrove areas outside the RAWN Park, which is mainly due to the conversion of mangroves to marine ponds. These mangrove fruits are potential for various uses by the local community living near the RAWN Park. As a usual practice, many of the local people here catch fish, crabs, and shrimps in the mangroves forest.

Sampling and Preparation of Mangrove Fruits

The fruits of X. granatum, S. alba, and B. gymnorrhiza were sampled from the different locations at the RAWN Park () from 15 May to 20 June in 2017. These mangroves produce fruits nearly at the same period of time. The X. granatum and B. gymnorrhiza trees were typically found in the mangrove interior, near the mangrove-upland interface, while S. alba trees were found at the mangrove–ocean interface (). Mangrove fruits that were in good physical condition and without damage were collected from three individuals of mature trees for each species. The fruits were labeled according to the individual of each species, kept in a box containing dry ice, and brought back to the Forensic and Molecular laboratory located at Halu Oleo University. In the Laboratory, all fruit samples were washed thoroughly in tap and distilled water before being separated for the fresh and drying samples analysis, while shell of mangrove fruits peeled. For elemental analysis, the samples were dried in the oven at 500°C temperature and then ground into fine powder and stored in air-tight containers at 40°C for further analysis.

Figure 1. Study sites of mangrove fruits sampling (mangrove interior: red rectangle; mangrove edge: yellow rectangle) at Rawa Aopa Watumohai National Park, Southeast Sulawesi Sites.

Figure 1. Study sites of mangrove fruits sampling (mangrove interior: red rectangle; mangrove edge: yellow rectangle) at Rawa Aopa Watumohai National Park, Southeast Sulawesi Sites.

Extraction and Estimation of Total Protein

Approximately 500 mg of tissue was taken from X. granatum, S. alba, and B. gymnorrhiza fruits and homogenized with a pre-chilled mortar and pestle in ice-cold protein extraction buffer. The homogenized samples were then centrifuged at 10,000 rpm at 4°C for 30 min and resulting pellets were washed with 10% TCA and incubated overnight at 40°C. The pellets were suspended in 2 ml of 0.1 N NaOH. Total protein was then estimated from the slurry using spectrophotometry (V-630 UV-Vis JASCO, USA) at 750 nm and a bovine serum albumin (fraction V) standard curve and was expressed as mg per g of fresh weight (Lowery et al., Citation1951).

Extraction and Estimation of Total Sugar Content

Total sugar content of X. granatum, B. gymnorrhiza, and S. alba fruits was estimated using the method of Rangana (Citation1979). About 0.5 g of fresh fruit samples were taken and homogenized with 80% alcohol and centrifuged at 5,000 rpm for 20 min three times. The supernatant was then collected and placed in a fresh beaker with distilled water, and then heated on a hot plate until the smell of alcohol disappeared. The volume of solution was brought to 100 ml with distilled water and stored at room temperature of 25°C. Further analysis was done by measuring 1 ml of the 100 ml solution in a test tube and chilling it. After 10 min, 4 ml of Anthrone’s reagent was carefully run down the walls of the test tube. The test tubes were then immersed in ice water for 5 min, removed and brought to ambient temperature, and then boiled in water bath for 10 min. After proper cooling, the absorbance was measured at 625 nm. Total sugar content was calculated using a D-Glucose standard curve and expressed as mg per g of fresh weight.

Extraction and Estimation of Fat Content

The fat content of X. granatum, S. alba, and B. gymnorrhiza growing in RAWN Park was extracted by using a modified AOAC method of Conway and Adams (Citation1975). Fat was extracted from 1 g of sample by heating in alcoholic HCl and then adding 95% ethanol. The sample was allowed to cool, ether (1 mL) and sodium sulfate (1 mg) were added, and the mixture was then shaken. The acidic ethanol layer was re-extracted twice more with a mixture of ether and petroleum ether. The combined, recovered supernatants were allowed to evaporate in a ventilated area, and any trace of moisture was eliminated by drying in a forced air oven (103°C, 1.5 h) prior to gravimetric determination.

Extraction and Estimation of Ascorbic Acid Content

Ascorbic acid content in fruits of mangroves X. granatum, S. alba, and B. gymnorrhiza growing in RAWN Park was estimated following the method of Harris and Ray (Citation1935). Sample extraction of fruits from each mangrove species was done by grinding 0.5 g of sample material in 6% oxalic acid solution followed by centrifugation at 3,000 rpm for 10 min. The aliquot (or pellet) was then transferred to a clean beaker, brought up to 100 ml with distilled water, and 0.5 ml of the resulting supernatant was then added to 10 ml of 0.6% oxalic acid solution. This solution was then titrated (with NaOH 0.1 M) against a standard indophenols dye solution until a pale pink color was seen. Standardization of dye was done with standard ascorbic acid (1 mg/ml). Total ascorbic acid content (AAcontent; mg/100 g) of fruits was then calculated by:

(1) AAcontent=0.5mg/V1×V2/5ml×100ml/wt.ofthesample ×100(1)

where V1 was the volume of the titrant against the standard ascorbic acid and V2 was the volume of the titrant against the sample.

Extraction and Estimation of Carotenoid Content

Carotenoid content of X. granatum, S. alba, and B. gymnorrhiza fruits growing in the RAWN Park was evaluated following the standard method by Arnon (Citation1949). Approximately, 0.5 g of the sample powder of each mangrove fruits were weighed and homogenized in 80% acetone. The volume of solution was then brought to 50 ml and then centrifuged at 5,000 rpm for 20 min until the supernatant became transparent. The supernatant was taken and absorbance was measured at 645 and 663 nm.

Analysis of Total Tannin Content

Total tannin content of X. granatum, S. alba, and B. gymnorrhiza fruits was determined according to Rangana (Citation1979). One milliliter of extract was dissolved in 7.5 mL of distilled water and 0.5 mL Folin-Ciocalteu’s reagent (1:1) and 1.0 mL of saturated Na2CO3 (35%) was then added. The mixture was vortexed and kept in the dark for 30 min. The absorbance was then measured at 760 nm. A standard curve was prepared with tannic acid and the total tannin was expressed as the tannic acid equivalent in percentage of extract.

Macronutrient Analysis

Macronutrients of Sodium (Na), Potassium (K), and Calcium (Ca) were analyzed in X. granatum, S. alba, and B. gymnorrhiza fruits according to Basak et al. (Citation2016). About 0.5 g of fine powdered sample of fruits from each mangrove species was digested following wet digestion procedures using concentrated HNO3 and 30% H2O2. The digested samples were used for analysis of Na, K, and Ca using Flame photometer. Each sample was measured in triplicate.

Micronutrient Analysis

Micronutrients were analyzed in X. granatum, S. alba, and B. gymnorrhiza fruits according to Rout et al. (Citation2015). Approximately, 0.5 g of finely ground mangrove fruits were wet-digested using concentrated HNO3 and 30% H2O2. The digested samples were then analyzed for Iron (Fe), Copper (Cu), Manganese (Mn), and Zinc (Zn) concentrations using a flame atomic absorption spectrophotometer. Each sample was measured in triplicate. Distilled water was processed as described above and used as a blank solution. Quality controls were performed using certified reference materials of water and wastewater of SNI 6989.78:2011 (SNI, Citation2011).

Statistical Analysis

The data are expressed as mean ± standard error (SE) values. Mean nutritional and antioxidant values were statistically compared among the X. granatum, S. alba, and B. gymnorrhiza fruits using one-way analysis of variance. Pairwise comparisons were made using Fisher’s Least Significant Difference. All statistical comparisons were made in Kaleidagraph 4.0 at an alpha level of 0.05.

Results and Discussion

The protein content () in fruits of X. granatum (4.50 mg/g) was significantly higher (p < 0.01; F = 65.89; df = 2,6) compared to S. alba (0.93 mg/g) and B. gymnorrhiza (1.09 mg/g), but it was not significantly different between fruits of S. alba and B. gymnorrhiza. Similarly, total sugar content () did not significantly differ among X. granatum, S. alba, and B. gymnorrhiza fruits and was estimated as 14.8, 14.9, and 13.52 mg/100 g, respectively. However, the fat content () did not significantly differ among X. granatum, S. alba, and B. gymnorrhiza fruits and was estimated as 4.88%, 4.42%, and 4.74%, respectively.

Table 1. Comparative analysis of mean (±SE) nutritional parameters from fruits of mangroves growing in the RAWN Park, Southeast Sulawesi.

The ascorbic acid content () in fruits of X. granatum (65 mg/100 g) was significantly higher (p < 0.01; F = 2181.58) compared to S. alba (40 mg/100 g) or B. gymnorrhiza (41.87 mg/100 g), though it was not significantly different between S. alba and B. gymnorrhiza. Moreover, the content of beta carotene in fruits of S. alba (9.96 mg/g) was significantly higher (p < 0.01; F = 68.99) than that in X. granatum (7.99 mg/g) or B. gymnorrhiza (7.01 mg/g), but it was not significantly different between X. granatum and B. gymnorrhiza fruits.

Table 2. Comparison of mean (±SE) antioxidant content values from fruits of mangroves growing in the RAWN Park, Southeast Sulawesi.

The present results revealed that the protein content in fruits of X. granatum in this study was much higher than B. gymnorrhiza fruits (4.40 mg/g) sampled from Odisha coast, India as reported by Rout et al. (Citation2015), and S. apetala fruits (3.29 mg/g) sampled from Sundarbans, India as reported by Halder et al. (Citation2015), though the protein content of fruits of mangroves from this study were lower than Kandelia candel (15.6 mg/g) and R. apiculata (14.4 mg/g) fruits as reported by Rout et al. (Citation2015; ). The protein content of X. granatum grown in the RAWN Park was higher than protein (2.24%) of S. caseolaris fruits as reported by Patil and Chavan (Citation2013). However, the protein content in B. gymnorrhiza and S. alba fruits from this study was lower than that C. caseolaris (Patil and Chavan, Citation2013). Similarly, the fat content of fruits from all mangroves sampled in this study was higher compared to S. caseolaris fruits (0.86%) as reported by Patil and Chavan (Citation2013) and S. apetala fruits (8.24%) sampled from Sundarbans, India as reported by Halder et al. (Citation2015). The content of ascorbic acid in fruits of X. granatum was higher than that of B. parviflora (63.73 mg/100 g) and Heriteria fomes (49.06 mg/100 g) sampled from Odisha coast, India as reported by Basak et al. (Citation2016; ) or B. gymnorrhiza (53 mg/100 g) growing in Odisha coast, India as reported by Rout et al. (Citation2015; ). In addition, the ascorbic acid content in fruits of B. gymnorrhiza and S. alba from this study was also higher than Kandelia candel (40 mg/g) or B. gymnorrhiza (35 mg/g) sampled from Odisha coast, India as reported by Rout et al. (Citation2015; ) Moreover, the ascorbic acid content in fruits of all mangroves sampled were lower than B. cylindrica (101.86 mg/g) as reported by Basak et al. (Citation2016).

Table 3. Nutritional values of several mangroves fruits from previous studies.

The tannin content () in fruits of X. granatum (25.20%) was significantly higher (p < 0.01; F = 40.18) as compared to S. alba (22.65%) or B. gymnorrhiza (19.20%). In addition, tannin content in fruits of S. alba was significantly higher (p < 0.01) compared to B. gymnorrhiza. The high tannin content from our X. granatum or S. alba fruits compared to our B. gymnorrhiza fruits lowers the nutritional values of these two fruits to humans because tannin might precipitate proteins and various other organic compounds including amino acids and alkaloids. However, processing methods of fruits such as soaking for several hours before making powdered food supplements could be applied to reduce tannin levels. Nevertheless, fresh mangrove fruits are still likely to be a significant and important source rich in nutrients and antioxidants and useful for improving the health of coastal communities in Southeast Sulawesi, Indonesia.

The macronutrient content of Na () in fruits of X. granatum (517.86 mg/100 g) was significantly higher (p < 0.05; F = 5.90) compared to B. gymnorrhiza (43.72 mg/100 g), but it was not significantly different between X. granatum and S. alba or between B. gymnorrhiza and S. alba. On the contrary, the content of K () in fruits of X. granatum (189.89 mg/100 g) was not significantly different compared to B. gymnorrhiza (127.28 mg/100 g) or S. alba (136.84 mg/100 g). Meanwhile, the content of Ca () in fruits of B. gymnorrhiza (1251.08 mg/100 g) was significantly higher (p < 0.01; F = 60.71) compared to S. alba (225.13 mg/100 g) or X. granatum (485.21 mg/100 g), though it was not significantly different between S. alba and X. granatum.

Table 4. Comparative study of mean (±SE) macro-nutrient content values from fruits of mangrove trees growing in the RAWN Park, Southeast Sulawesi.

The present result of the macronutrient Ca content in mangrove fruits studied was much higher compared to values reported by Basak et al. (Citation2016) for fruits of B. cylidrica (280 mg/100 g), B. parviflora (240 mg/100 g), and Heritiera fomes (120 mg/100 g), and reported by Rout et al. (Citation2015) for fruits of K. candel (240 mg/g), B. gymnorrhiza (200 mg/g), and R. apiculata (200 mg/g). However, the macronutrients of Na content in fruits of all mangroves studied seemed to be lower than Na in fruits of B. cylidrica (700 mg/100 g), B. parviflora (1090 mg/100 g), or Heritiera fomes (1060 mg/100 g) as reported by Basak et al. (Citation2016), as well as K. candel (700 mg/g), B. gymnorrhiza (700 mg/g), or R. apiculata (690 mg/g) as reported by Rout et al. (Citation2015). Moreover, the macronutrient of K content in fruits all mangrove studied was also lower than B. cylidrica (250 mg/100 g), B. parviflora (480 mg/100 g), or Heritiera fomes (800 mg/100 g) as reported by Basak et al. (Citation2016), and K. candel (280 mg/g), B. gymnorrhiza (420 mg/g), or R. apiculata (680 mg/g) as reported by Rout et al. (Citation2015). In contrast, Na, K, and Ca contents of all mangrove fruits sampled in this study were much higher than S. apetala fruits growing in the Sundarbans area of India (Halder et al., Citation2015).

The present results show that micronutrient content () of Fe in fruits of S. alba (0.51 mg/g) was higher than that in X. granatum (0.38 mg/g) or B. gymnorrhiza (0.34 mg/g), though there were no significant differences among mangrove fruits. However, the content of Cu in fruits of B. gymnorrhiza (0.55 mg/g) was higher than that in X. granatum (0.084 mg/g) or S. alba (0.077 mg/g), although there were no significant differences. On the other hand, Mn content in fruits of S. alba (0.063 mg/g) was significantly higher (p < 0.01; F = 27.13) than that in X. granatum (0.052 mg/g) or B. gymnorrhiza (0.012 mg/g), but it was not significantly different between fruits of X. granatum and B. gymnorrhiza. Similarly, the content of Zn in fruits of S. alba (0.72 mg/g) was significantly higher (p < 0.01; F = 28.88) compared to X. granatum (0.52 mg/g) or B. gymnorrhiza (0.11 mg/g), but it was not significantly different between X. granatum and B. gymnorrhiza.

Table 5. Comparative study of mean (±SE) micro-nutrient content values from fruits of mangrove trees growing in the RAWN Park, Southeast Sulawesi.

Our study results show that the micronutrients Fe, Mn, Cu, and Zn contents in fruits of all mangroves studied were higher than that in fruits of Heriteria fomes sampled from Bhitarkanika of the Odisha coast, India (Basak et al., Citation2016). However, the micronutrients Fe, Mn, and Cu content in fruits of X. granatum, B. gymnorrhiza, and S. alba were lower than that in fruits of mangroves B. cylindrica and B. parviflora sampled from Bhitarkanika of the Odisha coast, India (Basak et al., Citation2016) and B. gymnorrhiza, Kandelia candel, and R. apiculata sampled from Bhitarkanika and Mahanadi delta of the Odisha coast, India (Rout et al., Citation2015). Moreover, the Zn content in fruits from all three mangroves sampled in this study were higher than B. gymnorrhiza, K. candel, and R. apiculata fruits sampled by Rout et al. (Citation2015) or B. cylindrica sampled by Basak et al. (Citation2016).

The nutritional and antioxidant values of fresh fruits from mangroves growing in the RAWN Park revealed their future potential and important use as a renewable food source for the coastal society and importance in safeguarding the health of the local community; while coastal people in the Java Island have used mangrove fruits in the past, they have mostly been processed into syrups or other foods and are not eaten fresh (Jariyah et al., Citation2014). It is known that fresh fruits are a major source of essential trace elements in the human diet and are required for proper growth and body development (Olu-Owolabi et al., Citation2007). Trace elements in fresh fruits are also important in maintaining functional mechanisms in the human body (Nasreddine et al., Citation2010; Olu-Owolabi et al., Citation2007; Radwan and Salama, Citation2006). Deficiencies of micronutrient in humans can induce several health problems including weak bone and teeth development, mental retardation, child developmental issues, anemia, insomnia, decreased immune function, and other health-related complications (Linder and Hazegh-Azam, Citation1996; Saracoglu et al., Citation2009; Tapiero and Tew, Citation2003). Consumption of X. granatum, B. gymnorrhiza, and S. alba fruits could potentially alleviate this.

Conclusion

Our results demonstrate the potential of mangrove fruits growing in the RAWN Park, Southeast Sulawesi, Indonesia as a potential food source for human communities. Fruits from X. granatum, B. gymnorrhiza, and S. alba may be promising sources of nutrient and antioxidant material. Consumption of mangrove fruits could potentially meet the daily recommended amounts of total sugar (50 g), protein (61 g), fat (66.6 g), beta-carotene (550 mcg), and ascorbic acid (82.5 mg) for Indonesia mature people. Mangrove fruits can also meet the daily needs of macronutrients of Na (1500 mg), K (4700 mg), and Ca (1000 mg), as well as micronutrients of Fe (19.5 mg), Cu (900 mcg), Mn (2.05 mg), and Zn (11.5 mg) for Indonesia mature people (Indonesia Ministry of Health, Citation2013). This suggests that mangrove fruits could be used to address many of the nutritional-related and may malnourishment concerns local communities in this region face . Our data also suggest that mangrove fruits may be used in the food industry production or as a bio-nutrition alternative. Thus, mangrove fruits could provide an alternative and sustainable income source to communities, encouraging them to conserve and protect their mangrove forests as opposed to cutting them down for short-term gains such as shrimp aquaculture ponds or charcoal production. The potential value of mangrove fruits as an income source also encourages communities to restore degraded or deforested mangrove forests located outside of RAWN Park.

Acknowledgments

We thank anonymous reviewers for very constructive comments and suggestions on this manuscript. We would like to thank Rector, and Head of Research Center Halu Oleo University, RAWN office, and voluntary students. We acknowledge also the inputs from Cheryl Rita Kaur, Head of the Centre for Coastal and Marine Environment of the Maritime Institute of Malaysia.

Additional information

Funding

This research was supported by the Ministry of Research, Technology and Higher Education, Republic of Indonesia with grant nos. 025/E3/2017 and 0045/E3/LL/2018.

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