Review Article

Primary, Secondary Metabolites and Antioxidant Activity of Castanopsis Argantea, Artocarpus heterophyllus, and Aglaia tomentosa Fruit as Food for the Tapanuli Orangutan (Pongo tapanuliensis) in the Batang Toru Forest, North Sumatra

Herna Febrianty Sianipar1,2,3, Wahyu Widoretno1, Luchman Hakim1, Rezi Rahmi Amolia4, Fatchiyah Fatchiyah1,2,5*

1Department of Biology, Faculty of Mathematics and Natural Sciences, Brawijaya University, Jl. Veteran Malang, East Java, Indonesia; 2Research Center of Smart Molecule of Natural Genetics Resources, Brawijaya University, Jl. Veteran Malang, East Java, Indonesia; 3Depertment of Water Resource Management, Faculty of Engineering and Water Resource Management, Universitas HKBP Nommensen Pematangsiantar, Jl. Siopat Suhu, Pematangsiantar, North Sumatera, Indonesia; 4Yayasan Ekosistem Lestari, Jl. Bunga Sedap Malam IX Medan, North Sumatera, Indonesia; 5Biosains Institute, Brawijaya University, Jl. Veteran Malang, Indonesia.

Received | September 05, 2024; Accepted | October 27, 2024; Published | December 03, 2024

*Correspondence | Fatchiyah Fatchiyah, Department of Biology, Faculty of Mathematics and Natural Sciences, Brawijaya University, Jl. Veteran Malang, East Java, Indonesia; Email: [email protected]

Citation | Sianipar HF, Widoretno W, Hakim L, Amolia RR, Fatchiyah F (2025). Primary, secondary metabolites and antioxidant activity of Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa fruit as food for the Tapanuli orangutan (Pongo tapanuliensis) in the batang toru forest, North Sumatra. Adv. Anim. Vet. Sci. 13(1): 64-72.

DOI | https://dx.doi.org/10.17582/journal.aavs/2024/13.1.64.72

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright: 2025 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

INTRODUCTION

The Tapanuli orangutan (Pongo tapanuliensis), the newest species of great ape, is endemic to North Sumatra. These orangutans play a crucial role in forest ecosystems, acting as pollinators and seed dispersers, and are considered a keystone species. According to the IUCN (International Union for Conservation of Nature), they are classified as Critically Endangered due to drastic population declines caused by habitat loss, hunting, slow reproduction, and disease (Arief and Mijiarto, 2024).

The Tapanuli orangutan is found in the Batang Toru Forest, south of Lake Toba . The population has continued to decrease, with around 800 individuals recorded in 2017, and currently estimated between 577 and 760. Conservation efforts focus on maintaining their population through improved dietary resources (Rahman et al., 2019; Purwoko et al., 2022).

Food is fundamental for the growth, development, and behavior of primates (Wilson et al., 2014). Orangutans are selective feeders due to their large body size, primarily consuming fruit when available, and preferring soft pulp. They distinguish between preferred and fallback foods, with preference foods chosen when abundant (Arief et al., 2024; Lambert and Rothman, 2024). According to Arief and Mijiarto (2024), the fruits of Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa are preferred in the Batang Toru Forest.

Castanopsis argentea, locally known as chestnut or saninten, serves ecologically as a source of food, rest, and nesting for forest animals. Its fruit is consumed by wild boars and primates (Putri et al., 2022). Plant parts of Artocarpus heterophyllus such as stems, roots, leaves, and fruit have medicinal properties. Jackfruit leaves contain sapogenins, cycloartenone, cycloartenol, β-sitosterol, and tannins. It is a potential cytotoxic agent with high phenolic and flavonoid content (Utari and Warly, 2021), providing essential vitamins, minerals, and calories (Ranasinghe et al., 2019).

According to Widayati et al. (2023), fruit is rich in water, carbohydrates, and energy but low in protein, making it the primary food choice for orangutans. In contrast, seeds, flowers, young leaves, cambium, and young stems are selected as less preferred alternatives. The nutrient content is usually analyzed using the Proximate analysis method (Ganogpichayagrai and Suksaard, 2020). Onrizal and Auliah, (2019) examined the nutrient content of orangutan food in Tanjung Puting. They found two types of flowers eaten by orangutans (Dillenia sp and Xanthophyllum sp) which have higher protein levels than other food categories (18.1% and 16.6%).

The high nutritional value of Pongo tapanuliensis food is important for growth in tropical forests, as are the important chemical compounds found in fruit. The initial assessment of secondary metabolites in plants involves testing for color changes indicating alkaloids, flavonoids, tannins, saponins, and steroids. These secondary metabolites possess antibacterial and antioxidant properties (Contreras et al., 2022).

Differences in habitat conditions negatively impact animal life. The lack or poor quality of food sources and inadequate facilities and space in zoos lead to concerning conditions for many animals, including orangutans. Such conditions cause stress and even death (Sjahfirdi et al., 2023; Wolfensohn et al., 2018).

Stress contributes to the generation of free radicals. Evidence has long shown the involvement of free radicals and oxidative damage in metabolic disorders, incompatibility, and various diseases. Many chronic diseases are believed to originate from stress-induced free radicals and oxidative damage. Free radicals can be reduced by consuming fruits with natural antioxidants (Srivastava and Kumar, 2015). The type of fruit, along with its nutritional content, phytochemicals, and antioxidant activity, significantly influences the daily activities and health of the Tapanuli orangutan.

This research aimed to identify the primary and secondary metabolite, and antioxidant activity of Pongo tapanuliensis food. This study shows that the food of Tapanuli orangutans can be a potential source of phytochemicals, offering good medicinal and nutrition with strong antioxidant activity, which is important to consider in Tapanuli orangutan conservation efforts.

MATERIALS AND METHODS

Plant Material

This research was conducted from October 2023 to May 2024 at the Sustainable Ecosystem Foundation Orangutan Conservation Program Research Station in the Batang Toru Forest Area (Camp Mayang), North Sumatra Province, in collaboration with PT. Saraswanti Indo Genetech, the Bioscience Laboratory Center, and Brawijaya University. Plant samples were identified at the UPT Herbal Materia Medica Batu Laboratory in East Java Province.

Preparation and Extraction of Sample

Two hundred grams of ripe fruits from Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa were washed with clean water and dried in an oven at 60°C for 36 hours. They were then crushed with a blender to produce Simplicia powder. Ten grams of this powder was weighed, and 100 ml of 96% ethanol was added. The extraction was filtered, and the ethanol, capable of dissolving both polar and non-polar compounds , was concentrated using a rotary evaporator at 40°C and 90 rpm.

Proximate Analysis

The analysis was performed in triplicate using the crushed fruit powder, measuring carbohydrates, protein, lipids, energy from fat, total energy, ash, and water content according to the Indonesian National Standard method SNI 01-2891-1992 (Wijayanti et al., 2023).

Determination of Amino Acids

Amino acid levels were determined using fruit powder. Ultra Performance Liquid Chromatography (UPLC) was chosen for its ability to accurately separate components with similar chemical structures, allowing precise identification and quantification. Analyses were conducted in triplicate. UPLC was used to analyze L-histidine, L-isoleucine, L-leucine, and L-lysine according to Protocol 18-5- 17/MU/SMM-SIG. UPLC was performed using an AccQ, tag ultra C18 1.7μm Column (2.1 × 100mm). The mobile phase consisted of A: Eluent A concentrate Amino Acid Analysis AccQ.Tag Ultra; B: Amino Acid Analysis of Eluent B AccQ.Tag Ultra 10% in water; C: Aquabides; D: Amino Acid Analysis of Eluent B AccQ. Ultra Tags. The flow rate was set at 0.5mL/min. A photometric diode array (PDA) at a wavelength of 260nm was used as a detector (Fatchiyah et al., 2020).

Phytochemicals Test

Analyses were performed in triplicate. Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa extracts were filtered using Whatman No. 1 paper to assess phytochemical content. A positive result was indicated by a color change: alkaloids (brown precipitate), flavonoids (yellow), saponins (foam), steroids (green), tannins (blue-black), phenolics (blue-black), and quinoline (green) (Gonfa et al., 2023).

Determination of Total Flavonoid Content

Analyses were performed in triplicate. The total flavonoid content was determined by the colorimetric method. Extract (0.5 mL) was mixed with methanol (1.5 mL) and 5% NaNO2 solution (0.1 mL). After 5 minutes, 10% AlCl3 H2O solution (0.1 mL) was added, followed by 1M NaOH (0.1 mL) and distilled water (2.8 mL). Absorbance was measured at 700 nm (Phuyal et al., 2020).

LC-MS/MS

LC-MS/MS was used to determine phytochemical components. This technique allows accurate identification of structurally similar compounds. The concentrated extract was dissolved in methanol and filtered through a 0.2 μm nylon filter. Using a GIST C18 shim-pack column, 5 μL of filtrate was injected. The mobile phase, methanol, and water (1% HAc) (65:35, v/v), had a flow rate of 0.2 mL/min at 35 °C, with a detector set at 320 nm. Results were compared with compound composition percentages (Abu Bakar et al., 2020).

Antioxidant Activity with FRAP Method

Samples and positive controls (0, 2, 4, 6, 8, 10 µg/mL) were added to 2.5 mL of pH 6.6 phosphate buffer and 2.5 mL of 1% potassium ferricyanide, then incubated at 50 °C for 20 minutes in the dark. Following the addition of 2.5 mL of 10% TCA, 5 mL of distilled water, and 1 mL of 0.1% FeCl3 were derived from each solution. Absorbance was measured at 700 nm using a UV-Vis spectrophotometer. Ascorbic acid and quercetin, with the highest antioxidant capacity, were used as positive controls (Agustin et al., 2021).

Data Analysis

A statistical analysis of Tapanuli orangutan food content, including proximate and amino acids among Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa, was conducted using a t-test at a 95% confidence level. The Shapiro-Wilk test for normality showed p-values > 0.05, indicating normal distribution. Levene’s test for homogeneity of variance resulted in p-values > 0.05, suggesting homogenous variances. To analyze variations in food content among the three species, a one-way ANOVA and subsequent Tukey’s Post Hoc Test were performed at a 95% confidence level using SPSS version 16.0 and GraphPad Prism 8 (Dwiwibangga et al., 2022).

RESULTS AND DISCUSSION

Proximate Content

The highest proximate content was found in Castanopsis argantea, containing carbohydrates (84.09%), fat (3.07%), energy from fat (27.69 Kcal/100 g), and total energy (386.34 Kcal/100 g). The lowest was in Artocarpus heterophyllus with protein (5.56%), fat (0.46%), energy from fat (4.21 Kcal/100 g), and total energy (344.83 Kcal/100 g). Significant differences (p < 0.05) were observed among Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa in terms of carbohydrates, protein, fat, energy, total energy, ash, and water, except for protein and ash. This highlights the distinct nutritional profiles, as shown in Table 1.

Amino Acid Content

The highest amino acid content was found in Castanopsis argantea with L-Histidine (1721.09 ppm), L-Isoleucine (1329.17 ppm), and L-Lysine (1484.99 ppm). The lowest was in Artocarpus heterophyllus, with L-Histidine (754.95 ppm), L-Isoleucine (1065.25 ppm), and L-Leucine (2124.16 ppm). Significant differences (p < 0.05) were found among the species regarding L-Histidine, L-Isoleucine, L-Leucine, and L-Lysine, as in Table 2.

 

Table 1: Proximate content of Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa fruit.

Sample	Component proximate
	Carbohydrate (%)	Protein %	Lipid (%)	Energy from fat (Kcal/ 100 g)	Energy total Kcal/ 100 g	Ash (%)	Water (%)
Castanopsis argantea	84.09a	5.57b	3.07a	27.69a	386.34a	2.61c	4.64b
Artocarpus heterophyllus	79.59b	5.56c	0.46c	4.21c	344.83c	4.41b	9.96a
Aglaia tomentosa	77.7c	8.52a	1.94b	17.51b	362.39b	4.65a	1.94c

 

Note: Significant changes were noted by the different letters (Tukey’s HSD; P < 0.05).

 

Table 2: Amino acid content of Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa fruit.

Sample	Concentration (ppm)
	L- Histidine	L- Isoleucine	L- Leucine	L- Lysine
Castanopsis argantea	1721.09a	1329.17a	2736.28b	1484.99a
Artocarpus heterophyllus	754.95c	1065.25c	2124.16c	990.5b
Aglaia tomentosa	1398.75b	1314.17b	2880.18a	523.66c

 

Note: Significant changes were noted by the different letters (Tukey’s HSD; P < 0.05).

 

Table 3: Phytochemical test by color reactions.

Sample	Alkaloids	Flavonoids	Saponin	Steroids	Tannin	Phenolics	Quinolines
Castanopsis argantea	++	+	-	-	+	+	-
Artocarpus heterophyllus	++	+	-	-	+	+	+
Aglaia tomentosa	++	++	+	-	++	++	++

 

Note: Targeted compound absence (-); low target compound intensity (+); moderate target compound intensity (++);high target compound intensity (+++).

According to Herring et al. (2021), recommended dietary amino acid levels for omnivorous mammals in zoos are L-Histidine (38.6-48.8 ppm), L-Isoleucine (65.4-82.5 ppm), L-Leucine (132-176 ppm), and L-Lysine (100 ppm). All three orangutan food samples meet these requirements.

Phytochemicals Screening

Based on positive color change tests, the highest phytochemical components were found in Aglaia tomentosa containing alkaloids, flavonoids, saponins, tannins, phenolics, and quinolines. The lowest was in Castanopsis argantea, which showed only alkaloids, flavonoids, tannins, and phenolics, as detailed in Table 3.

Total Flavonoid Content

The total flavonoid content refers to the amount of secondary metabolite compounds derived from plants, quantified using a UV-Vis spectrophotometer. Aglaia tomentosa contained the highest flavonoid content (23.27 ± 3.46 mg QE/g), while Artocarpus heterophyllus had the lowest (3.44 ± 1.37 mg QE/g). Significant differences (p < 0.05) were observed among Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa, as shown in Table 4 and Figure 1. Higher flavonoid content in food is linked to greater potential health benefits for Tapanuli orangutans.

 

Table 4: Total flavonoids content.

Sample	Concentration (mgQE/g)
Castanopsis argantea	4.38± 3.25b
Artocarpus heterophyllus	3.44± 1.37c
Aglaia tomentosa	23.27±3.46a

 

Note: Significant changes were noted by the different letters (Tukey’s HSD; P < 0.05).

 

 

LC-MS/MS Analysis

LC-MS/MS analysis was carried out by providing a visual chromatogram as in Figure 2 to identify five bioactive compounds in Castanopsis argantea, including alkaloids (Caffeine), diterpenoids (D-Pinitol), flavonoids (Flazin), phenols (Dihydrocapsaicin), and terpenoids (Semiplenamide A).

Artocarpus heterophyllus contained two bioactive compounds: alkaloid (Synephrine) and quinoline (Schinifoline). In Aglaia tomentosa, nine bioactive components were

identified, including coumarins (Scopoletin and Fraxidin), alkaloids (Methysergide and Tryprostatin A), terpenoids (Santonin and 4alpha-(hydroxymethyl)-4alpha-demethylterritrem B), flavonoid (Artoindonesianin B), phenolic (2,5-Di-tert-butylhydroquinone), and a glycoside (5,7-Dihydroxy-2-(4-methoxyphenyl)-8-(3-methylbutyl)-4-oxo-4H-chromen-3-YL 6-deoxy-alpha-L-mannopyranoside), as presented in Table 5.

 

Antioxidant Activity

IC50 calculationshowed that Artocarpus heterophyllus (4.85 ± 1.13µg/mL) had the highest antioxidant content (4.85 ± 1.13 µg/mL), while Castanopsis argantea had the lowest (6.98 ± 1.46 µg/mL). Aglaia tomentosa (5.15 ± 0.16 µg/mL) was classified as having very strong antioxidant activity, as IC50 values < 50 µg/mL indicate very strong antioxidants. Significant differences (p < 0.05) were noted among the three foods, as illustrated in Figure 3. The lower the IC50 value, the higher the antioxidant activity, increasing the potential of the immune system in the Tapanuli orangutan (Aziz et al., 2023).

 

The relationship between orangutans and food plants is mutually beneficial, as orangutans aid in seed dispersion. Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa also serve as shelter and nesting sites for orangutans, help prevent landslides, and maintain soil fertility, crucial for orangutan habitats (Atmoko and Ma’ruf, 2009).

The Batang Toru forest, a dense tropical rainforest, features high humidity and consistent rainfall throughout the year. Soil temperatures of 24.9-25.8°C accelerate fruit ripening but may reduce acid and vitamin C levels, with soil pH ranging from 6.6 to 6.8. This optimal pH allows nutrients to dissolve easily and be absorbed by plants. Fruit sizes range from 3-5 cm for Castanopsis argantea, 4-8 cm for Artocarpus heterophyllus, and 1-3 cm for Aglaia tomentosa (Rahman et al., 2019).

Orangutans require proteins (6.1-26.0%), fats (2.9-9.8%), and energy (3.2-4.3 Kcal/100 g) (Dierenfeld, 1997). Castanopsis argantea can meet the fat and energy needs, Artocarpus heterophyllus meet the fat requirement, and Aglaia tomentosa provides protein and energy. For optimal nutrition, Sumatran orangutans prefer Polyalthia lateriflora for its water (62.13%), fat (0.10%), ash (0.21%), protein (13.72%), and carbohydrate (23.81%) content (Onrizal and Auliah, 2019). Jackfruit contains 7.3g carbohydrates, 1.6g protein, 0.2g fat, and 2.2g ash per 100g (Ranasinghe et al., 2019). Orangutans consume large fruit quantities during seasons of abundance and store nutrients as fat during shortages for energy (O’Connell et al., 2021). When fruit is in short supply, the nutrients are stored as fat, which can be used as a source of energy (O’Connell et al., 2021).

Muscle catabolism can result from calorie deficits. Amino acids like histidine, isoleucine, leucine, and lysine are crucial for various metabolic functions, including immune response (Herring et al., 2021; Lee et al., 2023). According to Herring et al. (2021), the dietary amino acid requirements

 

for omnivorous mammals in zoos are as follows: histidine (38.6-48.8 ppm), isoleucine (65.4-82.5 ppm), leucine (132-176 ppm), and lysine (100 ppm). The foods consumed by Tapanuli orangutans, specifically Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa, meet these amino acid needs. Amino acids are crucial for animal health, supporting various metabolic functions, including immune maintenance and response (Lee et al., 2023).

Based on phytochemical tests, several foods of Kalimantan orangutan contain phytochemical compounds such as alkaloids, flavonoids, and tannins, namely Hoya sp, Myristica lowiana, Diospyros siamang, Etlingera triorgyalis, Alseodaphne elmeri, Archidendron clypearia, and Campnospema coriacum (Atmoko and Ma’ruf, 2009). Based on the third table, samples of Castanopsis argantea, Artocarpus heterophyllus, and Aglaia tomentosa contain moderate levels of alkaloids, which can stimulate the nervous system, regulate blood pressure, and combat microbial infections (Dey et al., 2020). Additionally, flavonoids, tannins, and phenols offer significant benefits. Flavonoids support liver function and have anti-microbial and anti-viral properties (Ullah et al., 2020), as well as antioxidant effects that may reduce cardiovascular disease risk (Khan et al., 2021). Tannins possess antibacterial, antioxidant, and anti-diarrheal properties (Tong et al., 2022). Phenolic compounds protect against oxidative stress and inflammation and exhibit anti-inflammatory, anti-cancer, anti-aging, antibacterial, and antiviral activities (Zhang et al., 2022).

Kuswanda et al. (2021) conducted research in the Batang Toru Forest in North Sumatra, identifying food plants consumed by orangutans among the durian trees (Durio zibethinus). The total flavanol content of these plants ranges from 0.13 mg to 5.18 mg CE per 100 g FW (Aziz and Mhd, 2019). Flavonoids, metabolites produced and absorbed during photosynthesis, are bioactive polyphenols with antioxidant potential. The antioxidant capacity of Durio zibethinus, measured using the ferric reducing antioxidant power (FRAP) method, is between 71.84 and 749.08 µM TE per 100 g FW (Roy et al., 2022).

The FRAP testing method measures the antioxidant ability to reduce the ferric complex (Fe3+) to the ferrous complex (Fe2+) indicated by a color change to blue (Hsieh and Rajashekaraiah, 2021). Based on Table 6, Artocarpus heterophyllus (4.85 ± 1.13µg/mL) exhibits the highest antioxidant content due to its secondary metabolites such as phenols, flavonoids, and vitamin C (Konsue et al., 2023). Flavonoids demonstrate antioxidant activity by capturing free radicals and reducing the formation of singlet oxygen (O−). Based on their structure, flavonoids have more than one phenol group (-OH and aromatic groups) and have conjugated double bonds, enabling them to neutralize free radicals (Hassanpour and Doroudi, 2023).

 

Table 6: Antioxidant activity.

Sample	IC50 (µg/mL)	Level
Quercetin	5.16 ± 0.40c	Very strong
Ascorbic acid	5.17 ± 0.11b	Very strong
Castanopsis argantea	6.98± 1.46a	Very strong
Artocarpus heterophyllus	4.85± 1.13e	Very strong
Aglaia tomentosa	5.15 ± 0.16d	Very strong

 

Note: Significant changes were noted by the different letters (Tukey’s HSD; P < 0.05).

 

Future research should explore this fruit for bioactivity tests, including anti-inflammatory, antiparasitic, and antibacterial effects. Cultivation of this plant is crucial to support the survival of the Tapanuli orangutan.

CONCLUSIONS AND RECOMMENDATIONS

Based on primary metabolite tests, such as proximate analysis and amino acid profiling, Castanopsis argantea is identified as the optimal food for the Tapanuli orangutan, meeting its nutritional requirements. For secondary metabolites, Aglaia tomentosa excels in phytochemical screening and total flavonoid content. The bioactive compounds in Castanopsis argantea include caffeine and flazin; in Artocarpus heterophyllus, synephrine and schinifoline; and in Aglaia tomentosa, artoindonesianin B and 2,5-di-tert-butylhydroquinone. The highest antioxidant activity is observed in Artocarpus heterophyllus. A conservation strategy involving the cultivation of these three plants is recommended. This research also informs habitat restoration efforts, emphasizing plant species that are primary food sources for orangutans. Additionally, data on food content can be utilized to monitor orangutan population health.

ACKNOWLEDGMENTS

We would like to express our gratitude to the Higher Education Funding Agency (BPPT) of the Ministry of Education, Culture, Research, and Technology of the Republic of Indonesia, through the Education Fund Management Agency (LPDP), for funding this research (00723/J5.2.3./BPI.06/9/2022). We also thank Universitas HKBP Nommensen Pematangsiantar for supporting the provision of field laboratory equipment. Additionally, this research is partially supported by the Brawijaya University Professorship Research Grant 2024.

NOVELTY STATEMENT

There has been no research regarding the content of Tapanuli orangutan food such as amino acids, bioactive compounds, and antioxidant activity. Previous research was limited to the qualitative content of phytochemicals and their proximates. Data and information regarding phytochemical content, nutrition, and antioxidant activity will be useful for the health of Tapanuli orangutans.

AUTHORS’ CONTRIBUTIONS

Herna Febrianty Sianipar and Rezi Rahmi Amolia contributed to the data collection and manuscript drafting. The manuscript was corrected by Wahyu Widoretno, Luchman Hakim, and Fatchiyah Fatchiyah.

Conflict of Interest

The authors declare no conflict of interest regarding the publication of this article.

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