Total Phenolic and Starch Content of Arrowroot Tuber in The Agroforestry System

Abstract

Indonesia's tropical forest management faces several challenges owing to the growing demand for forest resources and increasing population. The forestry sector plays a significant role in supporting food security programs by harnessing the potential of forest resources. One solution to sustainable forest management and optimal forest land use is agroforestry techniques. Arrowroot (Maranta arundinacea) is tolerant to heavy shade and is a promising functional food crop that can contribute to food security programs. Starch content in arrowroot tuber plays an important role in meeting nutritional requirements and overcoming several health problems. Arrowroot tubers also contain phenolic compounds, the largest group of compounds that act as natural antioxidants in plants. This study aimed to analyze the total phenolic and starch contents of arrowroot tubers cultivated in agroforestry systems. We used a Randomized Complete Block Design with a planting pattern as treatment for the species combinations of Falcataria moluccana + arrowroot (FA), F. moluccana + arrowroot + Amomum cardamomum (FAC), and monoculture arrowroot (MA) with three blocks/replications. The arrowroot tubers were harvested from nine-month-old plants and composite samples representing each treatment were analyzed for total phenolic and starch contents. The total phenolic content in the arrowroot tubers was determined using the Folin-Ciocalteu reagent. Starch content was measured using the Modified Somogyi method, which involves preparing reagents, followed by hydrolysis and the reducing sugar determination methods. The results revealed that the planting pattern significantly affected starch content. The highest starch content was observed in the MA pattern of 23.99%, followed by the FAC and FA planting patterns of 22.75% and 18.44%, respectively. The planting pattern did not significantly affect phenolic content. The MA, FAC, and FA patterns yielded the highest to lowest phenolic contents of 218.02, 212.62, and 210.04 µg/g, respectively. Furthermore, the planting pattern significantly affected the total phenolic of tuber yield per plant, with the highest value of 214.48 mg yielded by MA pattern. Thus, agroforestry practices can maintain the phenolic and starch content of arrowroot tubers. The development of arrowroot in agroforestry system will be prospective not only for meeting food demand, but also for supporting forestry multi-business and social forestry programs to achieve sustainable forest management.

Keywords:

• Intercropping
• Falcataria moluccana
• Maranta arundinacea
• medicinal plant
• functional food crops

Introduction

Indonesia is the world’s largest archipelagic country, with 63% of its total land area amounting to 120.5 million hectares, is designated as state forest area (MoEFRI, 2022). The high community's demand for forest resources and the food crisis challenge which tends to getting worse due to the climate change impact, requiring efforts to increase forest land productivity, including through agroforestry practices. Farmers depend highly on tropical forest (Njurumana et al., 2020). Proper management to optimize limited forest resources in face of increasing population is necessary to meet the community’s increasing needs of land. The FAO (2021) states that conversion to agricultural land is the main cause of deforestation, reflecting the heavy communities reliance on these forests.

Recent data indicate an increase in the number of villages, from 31,957 to 39,147 villages, that interact closely with their surrounding forest, with 46.76% (39,147 villages) located on the forest periphery, 3.97% (3,324 villages) situated within forest areas (BPS, 2020; KLHK, 2018) and about 48.8 million people depend on tropical forests (MoEFRI, 2022). In addition, forestland has a great potential to provide food and medicinal plant habitat. Furthermore, food security is a global issue that all nations must address. As per Government Regulation No. 17 of 2015 concerning Food Security and Nutrition, forestry sector plays a crucial role for ensuring Food Security through the utilization of forest resources.

One promising solution for sustainable forest management and optimal forest land use to fulfill various community needs is agroforestry techniques. Agroforestry can improve land management systems that reduce deforestation rate and alleviate food crisis problem simultaneously. Such techniques also align with Sustainable Development Goals (SDGs) (Negash & Starr, 2021; van Noordwijk et al., 2018). It also contributes to increased community income, enhanced soil fertility, and conserved soil and water (Kiyani et al., 2017; Octavia et al., 2022; Octavia et al., 2023a).

Agroforestry also provides environmental services, including climate change mitigation, and holds significant potential for sustainable food production (Bettles et al., 2021; Bishaw et al., 2022). Developing the best practice of agroforestry is a strategic recommendations for achieving balanced environmental, social, and economic objectives in sustainable forest and landscape management. This requires the application of several silvicultural and crop cultivation techniques, among others (Octavia et al., 2022) planting pattern arrangement and species selection, the use of legumes and cover crops, the use of biofertilizers in agroforestry, and biodiversity enhancement. Optimized and increased forestland productivity is paramount for improving food security using diverse, fast-growing, multipurpose tree species, food crops, and medicinal plants.

Several widely known agroforestry practices include intercropping (alley cropping/hedgerow intercropping) or alley farming, multi-strata agroforestry/forest farming/multi-story cropping, and grass strip cropping. Alley cropping, sometimes called intercropping, is an agroforestry practice involving trees within agricultural croplands, particularly in tropical areas. It was initially promoted to enhance soil fertility and sustain crop production in nutrient-depleted soils (Grebner et al., 2013). Similarly, forest farming, also known as multi-story cropping, involves the cultivation of high-value crops under a forest canopy to enhance production, deliberately maintained to provide shade and favorable growth conditions. Forest farming involves intentionally cultivating edible, spice or medicinal crops in native/planted woodlands managed for wood and understory crops (AFTA, 2023). It is mainly appealing to farmers interested in maximizing multiple crop yield on the same land to improve whole-farm yield. Some studies have shown that forest farming involves intercropping practice had successfully enhanced land productivity. For example, the intercropping of three tuber crops (Maranta arundinacea, Canna edulis, Dioscorea esculenta) with five-year-old teak generated land equivalent ratio (LER) > 1. Meanwhile, for intercropping on teak under seven years old, only the combination with C. edulis reached LER > 1, which means that land productivity generated by agroforestry practices is higher than that by monoculture (Maharani et al., 2022). A value of LER > 1 has also reported for the intercropping and forest farming of Falcataria moluccana and peanut/Arachis hypogaea (Swestiani & Purwaningsih, 2013), F. moluccana and red chili/Capsicum annuum (Rachman & Hani, 2014). Mainstreaming agroforestry practice have the potential to sustain community livelihood particularly in social forestry areas (Octavia & Rachmat, 2020; Octavia et al., 2020; Yeny et al., 2021; Octavia et al., 2022).

One of the fast-growing legume species with potential multipurpose is sengon (Falcataria moluccana), while the spice/medicinal and food plant groups with significant development potential include arrowroot (Maranta arundinacea) and cardamom (Amomum cardamomum). Cardamom is a plant species generally cultivated in private forests and social forestry programs and has a high market value as an endemic plant species in Indonesia (Sanudin et al., 2023). These species have high community adoptability, economic value, and promising prospects for development (Hani and Octavia, 2020; Kusmawati et al., 2018; Mada et al., 2017; Zakiyah et al., 2017). In recent years, arrowroot starch has gained increased interest in the food industry, mainly among small producers encouraged by the international market price and the possibility of its use in the diet of those with celiac disease and diabetes (Amante, 2020).

Arrowroot (Maranta arundinacea) is a functional food crop and an alternative source of carbohydrates that has great potential to support food security programs (Oktafani et al., 2018). It also has potential use as a medicine and other utilization in the industry (Rohandi et al., 2017). There is increasing interest in the development of functional foods from local materials. Although it originated in the South American region of western Brazil (Kusbandari & Susanti., 2017), arrowroot is a locally well-grown tuber crop in Indonesia (Lestari et al., 2017). The starch yield of arrowroot tubers range from 15–20%. Starch is the principal component of tuber crops. Arrowroot has various health benefits, including as a prebiotic food and an immunostimulant that increases immunity, maintains gastrointestinal health, inhibits degenerative diseases, nourishes the digestive tract, and prevents stunting in children (Harmayani et al., 2011; Kumalasari et al., 2012). Moreover, it has antioxidant, antimicrobial, anti-inflammatory, antiulcer, antidiarrheal, vibriocidal, anticarcinogenic, and immunostimulatory properties (Pant et al., 2021). It has also been reported to have anti-cholesterol effects (Kusbandari & Susanti., 2017). Flour products have low glycemic index, therefore, they are easy to digest and very good for health (Deswina et al., 2021; Deswina & Priadi, 2020; Djaafar et al., 2010; Oktafani et al., 2018). Arrowroot starch plays an important role in meeting the nutritional needs and overcoming digestive problems. It is not only high in carbohydrates and rich in folate but also high in iron, calcium, phosphorus, potassium, zinc and is gluten free. Arrowroot has more complex carbohydrates and less sugar, making it suitable for a diabetic diet.

Arrowroot has a higher protein content than other tubers and its starch can meet the daily need for folate about 100%, and can be crucial for pregnant women (Amante et al., 2020; Kumparan, 2022). Generally, arrowroot starch has wide applications in the food industry (Valencia et al., 2015). A higher addition of arrowroot flour to the cookie resulted in a more easily crumble texture and lighter color. For example, in the food industry, the dietary fiber and resistant starch content of the cookie bar from the substitution of 30% arrowroot in the mixed ingredient formula was the highest when compared to substitution of 30% kidney bean and foxtail millet (Lestari et al., 2017). Snack bars with 70% arrowroot flour and 30% kidney beans had a low glycemic index of 25 and glycemic load of 9 (Indrastati & Anjani, 2016). Arrowroot starch contains 15.2% moisture content. The water solubility of arrowroot starch granules increases above a temperature of 60 °C. Owing to the high starch and amylose contents of its tubers, arrowroot is also a very promising source of starch for application in edible films (Nogueira et al., 2018).

Arrowroot tubers contain phenolic compounds. The many health benefits of arrowroot can be attributed to the essential phytoconstituents in their leaves and rhizomes. The leaves and rhizomes contain phenolics, flavonoids, alkaloids, tannins, terpenoids, steroids, and glycosides (Firoskhan & Muthuswamy, 2021). Phenolic is the largest group of compounds that act as natural antioxidants in plants (Mar'atirrosyidah & Estiasi, 2015; Muddathir et al., 2017; Lestari et al., 2022). A previous study reported that arrowroot tubers contain bioactive phenolic compounds that can function as antioxidants (amounting to 0.15 g/100 g). Tubers are potent sources of natural antioxidants (Ruba et al., 2013). Natural antioxidant compounds are produce starch, which contains high levels of carbohydrates (Hidayati et al, 2016). Starch is the most abundant primary metabolite in plants and is widely used in the food, paper and textile industries, and other applications are reported in pharmacies. The widespread use of starch of arrowroot tubers in the food industry is related to the physicochemical properties of starch, which can form a gel when cooled (Valencia et al., 2015). The post-harvest leaf, stem, and rhizome residue of arrowroot can be recycled and used in the food, pharmaceutical, and agricultural industries (Ieamkheng et al., 2022). Arrowroot fibers are shorter than other starches, therefore, they are easily digested and can be used as food for babies and children with autism and down syndrome (owing to its gluten free), as well as diets for the elderly and convalescing patients. The primacy of arrowroot in the origin, spread, propagation, benefits, and utilization of plants by the community has been reported (Deswina & Priadi, 2020). These two metabolites play an important role in providing the health benefits as described above.

Arrowroot is found in almost all regions of Indonesia (Wahyurini & Susilowati, 2020). Despite it has many uses as a source of carbohydrates, arrowroot has not been seriously cultivated in Indonesia. The land area for cultivated arrowroot in Yogyakarta ranges from 6,301 to 17,847 hectares, which is distributed across four regencies (Bantul, Kulon Progo, Gunung Kidul and Sleman). Arrowroot is already cultivated in Central Java (Sragen Regency) in an area of 7,828 ha and in East Java (Blitar, Malang and Sampang) where it has been planted in an area of 18,000 ha. Meanwhile, in West Java, arrowroot plants are found in several regencies (Garut, Ciamis, Tasikmalaya, Sumedang, Bogor and Cianjur). However, outside Java (West Sumatra, South Kalimantan, West Sulawesi, South Sulawesi and Maluku), they have not been intensively cultivated (Djaafar et al., 2010). To date, the use of arrowroot tubers as an alternative source of staple food especially for those with diabetes and metabolic syndrome is still rare. This limited adoption may be attributed to a lack of knowledge and awareness regarding arrowroot's substantial potential, necessitating broader promotion of its functional benefit and cultivation.

Although there have been many studies on arrowroots’ total phenolic and starch content, they have not been conducted within agroforestry systems. In addition, there have been no specific studies regarding the starch and phenolic contents of arrowroot tubers grown under tree shade of F.moluccana stands. This research is the first to analyze starch and total phenolic content in the agroforestry system. Regarding the optimizing of the use of forest land and the importance of arrowroot as a functional food which has various and high potential health benefits, the potential of total phenolic and starch content in arrowroot tubers under tree shade in agroforestry practices needs to be revealed to obtain various benefits from this functional food crop. Given the multitudinous benefits of arrowroot, this study aimed to analyze the total phenolic and starch contents of arrowroot in agroforestry systems.

Materials and Methods

Research Location

The research was conducted from October 2021 to September 2022 in Cikabayan Forest, IPB University, Bogor, West Java, Indonesia. The research location lies at coordinates of latitude -6° 32’49” S and longitude 106° 42’59” E with an altitude of 150–200 meters above sea level (Figure 1).

Figure 1. The research location at the Cikabayan Forest

Site Climate and Characteristics

The planting sites were identified and selected based on their suitability to meet the growing requirements of arrowroots, specifically, climatic and edaphic conditions including soil properties and nutrients, air temperature and humidity, rainfall intensity and altitude. Arrowroot grows well at 0–900 m altitudes in the tropics, optimally at 200–600 m above sea level. The best temperature for arrowroot’s growth is 20–30 °C with an annual rainfall of 1500–2000 mm. It requires crumbly, well-drained and slightly acidic soils (Reddy, 2015). The climate classification at the research site according to the Koppen-Geiger is classified as Af (equatorial climate or tropical rainforest) with monthly precipitation is more than 60 mm (Beck et al., 2018). It is characterized by rainfall throughout the year (non-seasonal forecast area) in the research area (Briliawan et al., 2022). The average air temperature was 28.9 °C, humidity of 79%, monthly rainfall of 290 milimeters and the annual rainfall of 3480 mm. In addition, in the research location, there were also the three-year-old sengon stands with regular spacing lines that could be used as shade trees for arrowroot.

Shade intensity of the sengon canopy was measured by using two units of light meter. Then, the values under the sengon canopy and in the open area simultaneously were read in five replications for representative area. The relative percentage of sunlight intensity was calculated and shade intensity was calculated by 100% minus relative light intensity.

Soil sampling was conducted before planting to determine soil fertility status. It was carried out compositely at the planting site as supporting data for analizing the physical and chemical properties of the soil which plays an important role in influencing plant growth. There were included pH, organic carbon (C), nitrogen (N), phosphorus (P), potassium (K), Cation exchange capacity (CEC), porosity and soil texture.

Planting Design

The experimental design used a Randomized Complete Block Design, with planting pattern of agroforestry as the treatment by the species combination in three models, namely: Falcataria moluccana + arrowroot (FA), F. molluccana + arrowroot + cardamom (FAC), and monoculture arrowroot (MA) in three replications, with observation unit (n) = 3 for each treatment. Further analysis was performed using Duncan's Multiple Range Test (DMRT) if the variance (F-test) showed a significant effect (P < 0.05). The planting pattern of combining arrowroot with cardamom takes into account the shade-tolerant characteristics of cardamom, apart from being a local species, it is also popular with farmers and has high economic value. Then, the phenolic and starch content of arrowroot tubers harvested from the three planting patterns was analyzed.

Planting Material and Sample Preparation of Arrowroot Tuber

The materials used were arrowroot tubers planted together with cardamom seedlings under three-year-old sengon stands with a spacing of 1.5 m × 1.5 m in three planting patterns and manure (organic fertilizer). The crops (arrowroot and cardamom) were planted in a 3 m × 3 m plot under the F. moluccana stands (in the agroforestry system) and monoculture consisted of 16 arrowroot tubers or cardamom seedlings (or their combination) for each treatment plote (Figure 2).

Figure 2. The planting pattern of arrowroot in agroforestry and monoculture

Note: FA=Falcataria moluccana+arrowroot; FAC=F. molluccana+arrowroot + cardamom; MA = Monoculture arrowroot

The arrowroot tubers used were Creol cultivar from West Java accessions selected (genotype and phenotype) from the germplasm collection in the experimental garden of Dawuan at Subang, National Research and Innovation Agency (BRIN). The arrowroot tubers were harvested from nine-month-old arrowroot plants and composite samples from arrowroot plants representing each planting pattern treatment (FA, FAC and MA), for analyzing the total phenolic and starch content. There are nine composite samples that represent each planting pattern of FA, FAC and MA in three blocks/replications.

Analysis of Total Phenolic Content

The total phenolic content in the arrowroot tubers was determined using the Folin-Ciocalteu reagent (Sulistiany et al., 2016) and a spectrophotometer at a wavelength of 765 nm (Benites et al., 2015). Firstly, 100 μL of extracts in methanol (1 g/L) were mixed with 1.0 mL of distilled water and 0.5 mL of Folin-Ciocalteu’s (1:10 v/v) reagent. Then, 1.5 ml of 2% sodium bicarbonate was added, and the mixture was allowed to stand for 30 min with intermittent shaking. Absorbance was measured at 765 nm using a spectrophotometer (Benites et al., 2015). The methanol solution was used as a blank. The total phenolic content was expressed as a gallic acid equivalent (GAE) in micrograms per gram (µg/g) of extract. Tubers weighed 50 g per test sample.

Analysis of Starch Content

Starch content was measured using the modified Somogyi method, including reagent preparation, hydrolysis and reducing sugar determination methods. Starch content was calculated based on the amount of reducing sugar (RS) in the sample using the formula, starch content (%) = 0.9 RS (JICA 1980).

Economic Feasibility Analysis

Apart from the above analysis, we also added the economic analysis to describe the gained benefit from the agroforestry planting pattern, including Benefit Cost Ratio (BCR) and net income provided (benefit minus cost). A business is supposed to be profitable and feasible if BCR value > 1. The BCR was calculated by dividing the present value of benefits (total revenue per ha) by the present value of costs per ha with the formula as follows (Dwijo, et al., 2020): $$\mathit{\text{BCR}}=\frac{\left(\mathit{\text{PV}}\right)B}{\left(\mathit{\text{PV}}\right)C}$$

Remarks:

• (PV) B = Present Value of Benefit

• (PV) C = Present Value of Cost

Statistical Data Analysis

The total phenolic and starch content of arrowroot tuber were analyzed with variance analysis (ANOVA) at a confidence level of 95% (α level of 0.05) using SAS 9.4 software. Further analysis was performed using Duncan's Multiple Range Test (DMRT) when the variance (F-test) showed a significant effect (P < 0.05). The productivity estimation of phenolic and starch from fresh tuber yield per hectare in each treatment was performed using Microsoft Excel software.

The total phenolic and starch of tuber yield per hectare were obtained as follows:

• The total phenolic of tuber yield per ha (kg)

• = Fenolic content (µg/g) × total fresh weight of arrowroot’s tuber per ha (ton) × 10⁻³.

• The total starch of tuber yield per ha (ton)

• = Starch content (%) × total fresh weight of arrowroot’s tuber per ha (ton).

• Total fresh weight of arrowroot’s tuber per ha (ton)

• = Total fresh weight of arrowroot’s tuber per plant (g) × arrowroot plant quantity per ha × 10⁻⁶

Results

Planting Site Characteristics

Shade intensity of 3-year-old F. moluccana ranged from 56–73%, averaging 65% (Figure 3). Soil has a clay texture, with clay content varying between 55–60% and slightly acid with average pH of 5.9, the cation exchange capacity values are 16.07–18.37 cmol(+)/kg (medium) and has good C-organic content (high category, C-org 3,4% generated soil organic matter 5,7%). Total nitrogen (N) was 0.26% (medium), available phosphorus (P) is 10.78 mg.kg-1 (medium), available potassium (K) is 146.1 mg.kg-1 (very high) and soil porosity of 57.1%. In this research, arrowroots grew up well at an altitude of 150–175 m above sea level, with the average temperature of 28.9 °C and the air humidity of 79%.

Figure 3. Canopy of F. moluccana, viewed from above (A) and under (B) the stand

The Total Phenolic and Starch Content of Arrowroot Tubers in Agroforestry Systems

The effects of planting pattern on phenolic and starch contents of arrowroot tubers were shown in Table 1.

Table 1. The total phenolic and starch content of arrowroot tubers in different planting patterns

Treatment	Total Phenolic (µg/g)	Starch content (%)	Total Phenolic of tuber yield per plant (mg)	Starch of tuber yield per plant (g)	Fresh tuber yield per plant (g)
Planting pattern
FA	210.037	18.443^b	130.06^b	114.38^b	616.64^b
FAC	212.617	22.753^a	117.56^b	125.75^b	552.87^b
MA	218.017	23.987^a	214.48^a	237.06^a	986.49^a
P-value	0.536	0.018*	0.003**	0.008**	<0.0001**

Note: P-values followed by a small star-like symbol/asterisk (*) and mean values followed by different letters within a column are significantly different (P < 0.05) indicating that the treatment has a significantly different effect. P-values followed by a small starlike symbol/asterisk (**) and mean values followed by different letters within a column indicate that the treatment had a highly significant effect (P < 0.01). Mean values in bold indicate the highest value among the treatments.

Table 1 shows that the planting pattern significantly affected the starch content, total phenolic and starch of tuber yield per plant, as well as fresh tuber yield per plant. However, the planting pattern did not significantly affect the total phenolic content. The highest starch content was generated in the MA planting pattern, amounting to 23.99% which was not significantly different from the agroforestry FAC planting pattern of 22.75%. Similarly, the highest total phenolic and starch of tuber yields per plant, as well as fresh tuber yield per plant were observed in the MA planting pattern. The highest to lowest phenolic content was generated by the MA, FAC, and FA patterns. The productivity of phenolic and starch from the fresh tuber yield per hectare for each treatment is presented in Table 2.

Table 2. Productivity of phenolic and starch from fresh tuber yield per hectare in each treatment

Treatment	Total phenolic of tuber yield per ha (kg)	Starch of tuber yield per ha (ton)	Fresh tuber yield per ha (ton)
FA	2.64 ± 0.278	2.32 ± 0.224	12.59 ± 1.397
FAC	2.40 ± 0.212	2.57 ± 0.084	11.28 ± 0.176
MA	4.39 ± 0.531	4.83 ± 0.210	20.13 ± 1.585

Note: Falcataria moluccana+arrowroot (FA); F.molluccana+arrowroot + cardamom (FAC); Monoculture arrowroot (MA). Mean values in bold indicate the highest value among the treatments. The values followed by standar deviation (SD).

Economic feasibility analysis

Apart from ecological benefits in implementing agroforestry with a combination of sengon, arrowroot and cardamom species, we also found that this agroforestry model provides feasible economic benefits with a benefit-cost ratio (BCR) of 3.21 and a positive annual net income of Rp. 383,184,375 (equal to USD 24,407) per hectare in four years period, considering a discount rate of 9%. Meanwhile, monoculture arrowroot provides feasible economic benefits with a BCR of 2.36 and a positive annual net income of Rp. 100,346,950 (equal to USD 6,392) per ha. BCR was calculated in period of 4 years because F. moluccana in Indonesia is generally harvested after 4 years old.

Discussion

In this research, arrowroot grew well under heavy shade, at the shade intensity (average of 65%) of 3–4-year-old F. moluccana. The previous research also reveals that arrowroot (M. arundinacea) is a shade-tolerant food-producing plant species that is adaptive to low light and has a good adaptation rate to heavy shade > 60% (Murniati, 2020; Oktafani et al., 2018; Swadija & Padmanabhan, 2013). The average air temperature (28.9 °C) and humidity (79%) on the research site at the low land (altitude of 150–175 meters above sea level) were good enough to support plant growth. Likewise, good physical and chemical soil properties support their better growth as well. Arrowroot can grow under tree stands as well as on marginal land, therefore, this functional food crop has the potential to be developed in forest land or yards. Arrowroot production reaches 17–20 tons/ha (1.7–3.4 tons of starch/ha), with harvesting ages from 6 months until maximum starch is reached at 12 months (Sedyowati, 2011).

The total phenolic content of the arrowroot tuber generated in the monoculture (MA) planting pattern was not significantly different from the arrowroot tubers in the planting pattern with species combination of F.moluccana + arrowroot + cardamom (FAC) and FA in the agroforestry system. The phenolic content of the MA pattern of 218.02 µg/g, with a content difference of 2.5–3.7% is higher than those in the agroforestry system of 212.62 and 210.04 µg/g, respectively. This result revealed that the two agroforestry models can sustain the phenolic content of arrowroot tuber, although this tuber was originated from an arrowroot crop grown under heavy shade with a mixture with the other two species. A study in India revealed that the total phenolic in arrowroot tubers was 160 µg/g (Ruba et al., 2013), but it was 379 µg/g in nine-month-old arrowroot in Cambodia (Ieamkheng et al., 2022) and 388.10 µg/g in Bantul, Yogyakarta, which is lower than that in its leaf because leaf contain more flavonoid (Kusbandari & Susanti, 2017). The total phenolic content of arrowroot varies in different parts of the plant (rhizome, leaves or stem residue), plant age, and sampling locations (Ieamkheng et al., 2022). Harvest maturity also significantly affects the total phenolic content (Han et al., 2019). In this research, the phenolic content of arrowroot tubers in monoculture system was slightly higher than in agroforestry system. The effects of light intensity on bioactive compounds vary among plant species and the types of bioactive compounds. Another study on Flourensia cernua found a higher content of total phenolic compounds under partially shaded conditions than under fully irradiated conditions (Pant et al., 2021). Meanwhile, in Mahonia, a higher yield of alkaloids was found in 50% of sunlight followed by 30% of sunlight compared to 10% and 100% (full) of sunlight (Li et al., 2018).

Table 1 shows that of the two agroforestry planting patterns implemented, FAC planting pattern (with combination of 3 species), produced a higher total phenolic and starch content than those in FA agroforestry planting pattern (with combination of 2 species). This finding indicates the potential for increasing the total phenolic content with a greater diversity of plant species in the agroforestry system. This could be caused by the efficient use of nutrients and lower competition among the three species for the same nutrients, owing to the different nutrient needs of species. Different types between the tree roots and crops root can reduce competition for nutrients in these plants. Tree roots that grow deeper act as a ‘nutrient safety net’ by absorbing nutrients not absorbed by food crops in the lower layers during the growing season. In an agroforestry system, deep tree roots act as ‘nutrient pumps’, moving nutrients from the lower layers to the upper layers to be utilized by annual crops with shallow roots (Allen et al., 2004). The species combination of trees and crops found in agroforestry practices can help to achieve food security and sustain soil fertility from litter decomposition, which can maintain soil organic C content as well as higher land productivity and biodiversity (Mulia & Nguyen, 2021; Negash & Star, 2021).

The presence of diverse secondary metabolites, including phenolic compounds, may contribute to antioxidant activity (Fathoni et al., 2022). Phenolic components act as antioxidant agents by donating hydrogen to deactivate free radicals (Aryal et al., 2019). Several studies have revealed a strong proportionate correlation between total phenolic contents and antioxidant capacity (Sari et al., 2015; Muddathir et al., 2017; Batubara et al., 2023). Thus, arrowroot plant can be an alternative source of antioxidants for maintaining immunity. Since it can grow easily and is distributed in various regions, including on marginal land, the existence of this functional food crop is very promising to support food security program.

In Indonesia, considering that more than 50% of villages are located near and within forest areas (KLHK, 2018; MoEFRI, 2022), arrowroot plants can be very promising to be developed by mainstreaming agroforestry in Social Forestry, which is mostly developed in the state forest. Besides functioning as an antioxidant owing to its total phenolic content, its high starch content also can helps reduce stunting in children. Based on data from the National Nutrition Status Survey year 2022 (SSGI), the prevalence of stunting in Indonesia is still 21.6%. Despite this value decreased compared to the previous year (24.4%), it still exceeded the threshold of the World Health Organization (WHO) of < 20% (Kemenkes, 2023; Eko & Fariz, 2023). Therefore, arrowroot is also encouraged to be a promising ‘food agroforestry’ besides coffee, another important agroforestry crop commodities. A recent study found that Robusta coffee extract is also a potential functional food crops because of its high total phenolic, alkaloid, and flavonoid content as well as antioxidant activity and as natural compounds against bacterial infections (Suryanti et al., 2023).

The starch produced in this research was around 17.40–25.81% with an average of 18.44% for FA model, 22.75% for FAC model and 23.99% for monoculture. Although the highest starch content of the arrowroot tuber produced from the MA pattern was significantly different from the arrowroot tubers from the agroforestry FA, it was not significantly different from the agroforestry FAC (22.75%), which ranged 1.4–9.5% higher than those in agroforestry system. The fresh tuber yield in the MA treatment was significantly higher than that in the FA and FAC treatments. Therefore, the starch and total phenolic content of the tubers produced per plant in the MA treatment were significantly higher than those in the FA and FAC treatments. Fresh tuber yield productivity in the monoculture treatment ranged from 18.4–21.4 tons/ha with a phenolic productivity of 4.0–5.0 kg/ha and tuber starch of 4.3–5.3 tons/ha. Meanwhile, the fresh tuber yield productivity in the agroforestry treatment ranged from 11.1–14.2 tons/ha with a phenolic productivity of 2.2–2.9 kg/ha and tuber starch of 2.1–2.6 tons/ha.

In this study, the starch content of arrowroot planted in agroforestry systems was higher than that reported in previous research on monoculture pattern in other regions. A previous study (Valencia et al., 2015) reported that arrowroot tubers have been considered as a potential food source with high starch content, ranging from 17.2–18.9%, cultivated in South America, Southeast Asia, the Caribbean islands, Philippines and India. Another study on monoculture practices revealed that the starch yield was around 15–20%. Resistant starch in arrowroot can be a prebiotic food (Harmayani et al., 2011). Meanwhile, the starch content in this research was lower than that reported by the other study, stating that arrowroot tuber from the Cibatu population produced the highest starch content of 27%. In contrast, the fresh weight of tuber yield in the agroforestry pattern in this study was higher than that of arrowroot tuber in the Cilawu and Cikajang populations in Garut District. There are significant differences in the morphophysiological characteristics, tuber yield and starch content among different locations of arrowroot populations (Rohandi et al., 2017).

Starch content and tuber yield were significantly affected by location/accession, altitude and tree shade. Tuber yield and plant biomass tended to decrease with increasing altitude. The growth parameters also showed a positive correlation with starch content and tuber biomass, indicating that arrowroot growth could be a good indicator for genotype selection to gain a better quality of starch content. The highest starch content and tuber biomass were produced by arrowroot crop cultivated in the lowland area under three-year-old-sengon stands rather than under one and two-year-old sengon stands. A light intensity of 25.2% produces a higher starch content, tuber biomass and yield (Sudrajat et al., 2023). Another study also reported that the physicochemical and nutrient contents of arrowroot varied, but there were no significant differences between monoculture and agroforestry system (Handayani et al., 2019). Yet another study confirmed that the productivity of arrowroot (Maranta arundinaceae) tubers under Melia azedarach trees in agroforestry and monoculture cropping patterns was not significantly different (Handayani et al., 2019). This could be caused by the wider planting distance of M. azedarach trees allowing more sunlight to penetrate the soil under the shade of the tree canopy, so that photosynthesis occur optimally under its canopy shade.

Arrowroot is adaptive to limited environmental conditions, tolerant to heavy shade levels, can grow on marginal lands and as a food source to substitute wheat flour and rice. The quality of arrowroot flour can also be influenced by the quality of the site where it is grown (Sholichah et al., 2019). This condition proved that arrowroot can adapt with a low input of fertilizer, and can grow better under the sengon stand in an agroforestry system. Agroforestry planting patterns through intercropping legume trees provide some advantages for the crops planted under the stands. The existence of trees can increase the physical and chemical fertility status of the soil included cation exchange capacity through litterfall and tree root activity (Gunawan et al., 2019), which increases the availability of soil nutrients and minimizes root competition between trees and crops to obtain nutrients to support crops growth (Pachas et al., 2019; Wirabuana et al., 2022).

The presence of trees in an agroforestry system provides many benefits for supporting crop growth under tree shade, including (1) as a source of organic material, fallen tree leaves and pruned leaves are returned to the soil where they can be decomposed, so that the soil becomes more crumbly, therefore, create a better conditions for root growth. Plant biodiversity in agroforestry, like natural forests, is able to maintain soil carbon balance, soil structure, soil nutrients and water balance, as well as soil-borne diseases (Widyati et al., 2022); (2) suppressing weed growth, the tree shade will reduce the light entering soil thereby maintaining soil moisture which can suppress the weed growth, especially alang-alang (Imperata cylindrica) and reduce the risk of fire in the dry season; (3) reducing nutrient loss, tree roots which generally grow deeper act as a “nutrient safety net” by absorbing nutrients that can not be absorbed by food crops in the lower layers, as well as as a “nutrient pump” which brings and moves nutrients from the lower to the upper layers so that can be utilized by annual crops with shallower roots (Allen et al., 2004); (4) improving the physical, chemical and biological soil properties through root activity which can improve the soil structure and porosity, where dead tree roots leave pore holes, thereby increasing infiltration and reducing run-off. The physical soil quality of complex agroforestry is similar to that of natural forest land, which has better structure, porosity and bulk density (Briliawan et al., 2022; Purnama et al., 2022). The presence of mycorrhiza at tree roots in the agroforestry system may have great potentials to improve soil fertility, and the existence of trees in the agroforestry system can improve soil pH, soil organic matter and bulk density (de la Cruz & Galang, 2006); (5) fixing nitrogen (N) from the air, especially legume trees that can fix N directly from the air, thereby reducing the amount of fertilizer that has to be applied to annual crops; (6) reducing the danger of erosion, through its effect on improving soil organic matter content and soil structure; (7) suppressing pest and disease attacks, the presence of trees can reduce the population of certain pests and diseases. Species diversity in agroforestry reduce the potential for plant disease incidence by changing biological control mechanisms (Widyati et al., 2022). A study in Indonesia (Jambi Province) revealed that bird diversity in young (three-year-old) and old oil palm (20-year-old) agroforestry plots was higher than that in oil palm (15-year-old) monoculture plot (Ridho et al., 2023). Another study in West Java Province revealed that coffee agroforestry systems generally sustain higher biodiversity than sun-exposed fields. However, their study found that there was no diference in the richness and abundance of invertebrates in coffee gardens between sun-exposed and shade-grown coffee (Campera et al., 2022); (8) maintaining the stability of the microclimate, trees with spacing planted closely enough can maintain the stability of the microclimate, reducing wind speed which has the potential causing damage to annual crops (tree as wind break, avoiding tilting/collapsing of crops), increasing soil moisture through the positive effects of shading tree canopy and falling litter, and lowers the air temperature from the high intensity of sunlight due to the beneficial partial shade of trees; and (9) tree roots anchoring and binding soil, reducing landslide in agroforestry area. The tree root systems of tree species with deep roots and grass mixtures with intense fine roots serves the highest stability on hillslopes and riverbanks (Hairiah et al., 2020).

Economic feasibility analysis in this study revealed that the agroforestry planting pattern is more economically profitable for farmers than the monoculture because in addition to obtaining short-term economic benefits, the yield of sengon wood is also used as savings to gain long-term benefits. The other studies also revealed the economic feasibility of agroforestry sengon with other crops. Agroforestry of sengon with cardamom had the BCR of 1.45 (Indrajaya & Sudomo, 2013), sengon with pineapple had the BCR of 4.86 (Lensari et al., 2021), sengon with clove had the BCR of 8.39 (Dwijo et al., 2020), arrowroot monoculture in Malang-East Java had the BCR of 2.07 (Baluk, 2021) and smallholder sengon plantation in Pati-Central Java had the BCR of 1.70 (Stewart et al., 2021). Many studies have confirmed that agroforestry, a sustainable management system on natural resources that integrates trees on farms in the agricultural landscape, has the capacity to provide multiple benefits and could be a viable option for overcoming the challenges of poverty, hunger and climate change. Diversifying various commodities in agroforestry such as wood producer, forages for cattle, crops and palms can also be an appropriate approach to enhance community livelihood (Burgess et al., 2022; Octavia et al., 2023a). Likewise, the land equivalent ratio (LER) value for these two agroforestry cropping patterns (FA and FAC) was 2.08 to 2.44 (LER > 1), indicating that land productivity of agroforestry models is higher than monoculture (Octavia et al., 2023b), which correlated to higher economic advantages. Another study also reported that combination of arrowroot with teak tree (Tectona grandis) provided LER > 1 (Maharani et al., 2022). It means the agroforestry models were beneficial than monoculture pattern ecologically and economically. Applying agroforestry enables farmers to have the opportunity to work and earn from various plant species throughout the year in a daily, monthly, yearly base from fruits, cash crops, food, wood and other by-products, for their families (Murniati et al., 2022). In social-economic aspects, many studies reported that livelihood was the most significant driving factor for developing agroforestry in Indonesia (Parhusip et al., 2019; Octavia & Rachmat, 2020). Further advantages, arrowroot is a sturdy crop, easy to grow and can withstand extreme climatic conditions such as typhoons and long dry seasons. In Philippines, tuber starch from this crop directs a good market price and it is used widely by cookie makers (Malinis & Pacardo, 2012). So far, there is not many references cencerning financial analysis of arrowroot in agroforestry have been studied.

The above results showed that the species diversity in agroforestry FAC planting pattern can sustain the phenolic and starch content of arrowroot tuber, which were not significantly different from the monoculture. Although the tuber yield of the monoculture planting pattern was higher than that of agroforestry pattern, but the land equivalent ratio for these two agroforestry models is > 1 (Octavia et al., 2023b), which indicated the increase of land productivity by implementing agroforestry systems. Likewise, more diversity of species can provide more benefits to the farmers from the increase in income and other ecological benefits. The recent study reported that soil organic matter in the agroforestry plot was still relatively high, reaching 5.03% in 10 months after planting. Even though there was a small decrease in soil organic carbon, the occurrence was lower in agroforestry plots compared to monoculture. In addition, agroforestry model can increase the 1.8-cineol content and essential oil yield of cardamom leaf combined to arrowroot plant under F. moluccana shade trees (Octavia et al., 2024). The growth of arrowroot tubers requires greater nutrient uptake including organic carbon in starch formation. Tuber crops are wasteful in absorbing nutrients (Agusalim et al. 2022), therefore, the agroforestry planting pattern for this species are considered more capable of maintaining land fertility and productivity, than monoculture. This may be caused by the positive effect of leaves litter and root activity of legume trees which provided soil nutrients. Agroforestry FAC also provides feasible economic benefits with a benefit-cost ratio (BCR) of 3.21 and a higher positive annual net income than monoculture.

Trees in agroforestry systems play an important role in maintaining soil fertility through root activity and litter input. Agroforestry practice can maintain better growth of arrowroot in generating good phenolic and starch contents. Agroforestry FAC provides more ecological and economic benefits to the community and environment to achieve sustainable development goals, especially goal 1 (no poverty), goal 2 (zero hunger), goal 13 (climate action) and goal 15 (life on land). This will encourage its development, not only to support food security, but also to support forestry multi business and social forestry programs to achieve sustainable forest management.

Conclusion

Overall, this research concluded the total phenolic and starch contents of the arrowroot tuber generated from agroforestry planting pattern of F.moluccana + arrowroot + cardamom (FAC) are not significantly different from that of the arrowroot tuber generated from monoculture (MA) planting pattern. The MA pattern gave the highest phenolic content of arrowroot tuber of 218.02 µg/g, with a total phenolic content difference of 2.5-3.7% higher than those in agroforestry system. The highest starch content of the arrowroot tuber of 23.99% was generated from the MA pattern. However, it was not significantly different from the FAC pattern in the agroforestry system of 22.75%, with a starch content difference of 1.4-9.5% higher than those in agroforestry system. Likewise, the integration of arrowroot under agroforestry not significantly reduced the quality of arrowroot tubers. The agroforestry practice can maintained the total phenolic and starch content of arrowroot tubers as well as provided more ecological and economic benefits to the farmers.

Author Contributions

All authors contributed equally to the discussion of conceptual ideas, conducted literature reviews, analyzed the data and finalized the manuscript. D.O performed the experiment, prepared the original draft, reviewed and edited the manuscript. N.W, S.W.B, I.B and S.S provided critical comments and feedback on the manuscript. All the authors have read and agreed to the published version of the manuscript.

Acknowledgments

The authors express their sincere gratitude to the National Research and Innovation Agency of Indonesia (BRIN), Center for Standardization of Sustainable Forest Management Instruments, Forest Research and Development Center - Ministry of Environment and Forestry, Tropical Biopharmaca Research Center for supporting this research, and the Faculty of Forestry and Environment - IPB University for providing the research location. The authors acknowledge the facilities, scientific and technical support provided by the Laboratory of the Department of Food Science and Technology (LDITP) of IPB University, and the Laboratory of Starch Technology through E-Layanan Sains (ELSA) of BRIN. The authors would like to thank Dr. Puspita Deswina and Nurhaidar Rahman for their support in providing the arrowroot tubers as planting material in this research, Anisa Putri Maulidya for technical data processing, Fariz Choirul Wildan for providing the map, and Etik Erna Wati Hadi for the initial formatting of the references.

Conflict of interest

The authors declared no conflicts of interest.

Additional information

Funding

This research was partially funded by the Center for Standardization of Sustainable Forest Management Instruments – the Ministry of Environment and Forestry and the National Research and Innovation Agency of Indonesia (BRIN).