Vol. 16 | No.

4 |2203-2210| October - December | 2023

ISSN: 0974-1496 | e-ISSN: 0976-0083 | CODEN: RJCABP
http://www.rasayanjournal.com
http://www.rasayanjournal.co.in

PHYTOCHEMICAL PROFILE, FREE RADICAL SCAVENGING

ACTIVITY, AND α-GLUCOSIDASE INHIBITORY ACTIVITY
OF FRESHWATER SPONGES Oncosclera asiatica AND Eunapius
carteri FROM EAST JAVA, INDONESIA
E. Setiawan1, A. Yanuar2, C. Riani3, A. Budiharjo4,5, Y.F H. Firdaus6,
K. Phontree7, P. Phuwapraisirisan8 and R. Ramadhan6,9,
1
Department of Biology, Institut Teknologi Sepuluh Nopember, Kampus ITS Sukolilo, Surabaya
60111, Indonesia
2
PT. Milieu Elang Abadi, Pondok Wage Indah II Waru, Sidoarjo 61257, Indonesia
3
School of Pharmacy, Institut Teknologi Bandung, Jl. Ganesa No.10 Bandung 40132, Indonesia
4
Biotechnology Study Program, Faculty of Science and Mathematics, Diponegoro University, Jl.
Prof. Soedharto, Tembalang, Semarang Tengah 50275, Indonesia
5
Molecular and Applied Microbiology Laboratory, Central Laboratory of Research and Service-
Diponegoro University, Jl. Prof. Soedharto, Tembalang, Semarang Tengah 50275, Indonesia
6
Exploration and Synthesis of Bioactive Compounds Research Group (ESBC), University CoE-
Research Center for Bio-Molecule Engineering (BIOME), Campus C Universitas Airlangga,
Surabaya 60115, Indonesia
7
Division of Pharmacognosy and Toxicology, Faculty of Pharmaceutical Sciences, Khon Kaen
University. Khon Kaen 40002, Thailand
8
Center of Excellent in Natural Products (CENP), Department of Chemistry, Faculty of Science,
Chulalongkorn University, Bangkok 10330, Thailand
9
Department of Chemistry, Faculty of Science and Technology, Campus C Universitas
Airlangga, Surabaya 60115, Indonesia

Corresponding Author: [email protected]
ABSTRACT
Sponges from freshwater environments are poorly known producers of phytochemicals with pharmacological potency.
Oncosclera asiatica and Eunapius carteri are freshwater sponges from the Porong River, East Java province. They
can be considered promising new sources of bioactive compounds. This study aims to investigate the pharmacological
potency of O. asiatica and E. carteri extracts. Qualitative phytochemical and GC-MS analyses were performed on the
O. asiatica and E. carteri extracts. Antioxidant capacity was determined using DPPH and ABTS free radical
scavenging activities, whereas in vitro anti-diabetic activity was evaluated using α-glucosidase inhibition. The
phytochemicals were identified by GC-MS in O. asiatica and E. carteri extracts, such as fatty acid esters including
hexadecanoic acid, methyl ester; 9-hexadecenoic acid, methyl ester, (Z); 9,12-Octadecadienoyl chloride (Z, Z); 9-
Octadecenamide (Z); and decanedioic acid, dibutyl ester, and others. In addition, the n-hexane and ethyl acetate
fractions from E. carteri exhibited good α-glucosidase inhibitory activity. This study revealed that O. asiatica and E.
carteri extracts are potential sources of pharmaceutically useful bioactive compounds of natural origin.
Keywords: Antioxidant, α-glucosidase, Diabetes, Freshwater Sponges, Phytochemicals
RASĀYAN J. Chem., Vol. 16, No.4, 2023

INTRODUCTION
Bioprospection has developed into a vibrant scientific discipline that investigates fresh applications for the
use of natural goods. Most of the work in chemical research over the past 60 years or more has been
concentrated on metabolites from the sea.1 Evolutionary pressure from a wide range of species and
environments that are very different from those in terrestrial ecosystems has led to the creation of novel
Rasayan J. Chem., 16(4), 2203-2210(2023)
http://doi.org/10.31788/RJC.2023.1648435 This work is licensed under a CC BY 4.0 license.
 Vol. 16 | No. 4 |2203-2210| October - December | 2023

compounds that may be employed for a variety of pharmaceutical applications, including the treatment of
cancers and Alzheimer's disease.2 The river region is home to a variety of invertebrate animals, including
sponges, which contain natural chemicals that are crucial for the discovery and development of new drugs. 3
Freshwater sponges (Porifera) are a rare kind of sponge and their surroundings set them apart from their
marine counterparts. Sessile suspension feeders and freshwater sponges can be found adhering to
submerged surfaces in the majority of inland water habitats. Although roughly 150 species of sponge’s
dwell in freshwater areas such as lakes and rivers, the great majority of the estimated 15,000 sponges exist
in marine ecosystems.4 In contrast to marine natural products, there are comparatively few chemical
compounds from any freshwater animal or plant species that have been isolated and described. Alkaloids,
steroids, terpenoids, polyketides, polypeptides, and other phytochemicals have a variety of biological
effects, including cytotoxicity, antibiotic activity, antifungal activity, antiviral activity, antitumor activity,
and enzyme activity inhibitory effects.5 Sponges that live in freshwater environments are some of the
sources of secondary metabolites. Studies have shown that sponges may manufacture toxins as a defense
against predators and more than 10% of those substances showed cytotoxic actions. These animals'
chemical composition is made up of a wide range of fatty acids, sterols, and uncommon specialized
metabolites that are exclusive to freshwater sponges.6-8 These characteristics are highly valuable in
pharmacology and biotechnology, which raises the value of these organisms as a source of novel
bioproducts. The bioactivity of these animals against a number of therapeutic targets, including
acetylcholinesterase and malaria, has lately drawn attention to their unique metabolism. 9 Therefore, this
study was conducted to investigate the presence of phytochemicals in less studied species of Oncosclera
asiatica (Manconi & Ruengsawang, 2012) and Eunapius carteri (Bowerbank, 1863), which were discovered
in Porong River10, East Java province, Indonesia, and to assess their pharmacological potential in free
radical scavenging activity and α-glucosidase inhibitory activity. This study is also the first attempt to do
so.
EXPERIMENTAL
Material and Methods
Two freshwater sponges, Oncosclera asiatica (OA) and Eunapius carteri (EC), were freshly collected from
Porong River at 7°28'17.4 "S, 112°31'07.3 "E on July 25, 2020 in the city of Mojokerto using a sharp knife
for removing them from other encrusting. Identification of the sponges was based on their morphological
characteristics, DNA barcoding, and phylogenetic analysis by mitochondrial DNA (mtDNA) and Internal
transcribed spacer (ITS), which was carried out at the Zoology and Animal Engineering Laboratory of the
Faculty of Science and Data Analytics, Institut Teknologi Sepuluh Nopember. 10 Pro analysis of n-hexane,
dichloromethane, ethyl acetate, and methanol were purchased from Merck (Darmstadt, Germany). The
Baker’s yeast α-glucosidase, p-NPG (4-Nitrophenyl-α-D-glucopyranoside), butylated hydroxytoluene
(BHT), and butylated hydroxyanisole (BHA) were obtained from Sigma Aldrich. Meanwhile, DPPH (2,2
diphenyl-2-picrylhydrazyl) and ABTS ((2,2-Azinobis 3-ethyl benzothiazoline 6-sulfonic acid) were
obtained from TCI (Tokyo Chemical Industry).
Extraction Process
In ascending order of their polarity, n-hexane, dichloromethane, ethyl acetate, and MeOH were used to
extract the sponge materials. Using a vacuum rotary evaporator (BUCHI R-100) at 40°C to get the crude
extracts, the extracts were filtered and concentrated before being stored at 4°C until use. The extracts were
tested for antioxidant activity, α-glucosidase inhibitory activity, GC/MS analyses, and phytochemical
screenings.
Phytochemical Screenings
Qualitative phytochemical analysis was conducted on the four extracts (n-hexane, dichloromethane, ethyl
acetate, and MeOH) of sponge materials of O. asiatica and E. carteri. It was carried out in previous studies
to determine phytochemical components, such as alkaloids, flavonoids, saponin, phenolic, and
triterpenes.11,12
GS/MS Qualitative Analysis
The identification of bioactive compounds from n-hexane, dichloromethane, and ethyl acetate extract of
two freshwater sponges (O. asiatica and E. carteri) was characterized by Agilent 7890 GC series equipped
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with an HP-5 silica capillary column (5% diphenyl-and 95% dimethyl-polysiloxane, 30 m x 0.32 mm ID,
250 μm film thickness) coupled to mass spectrometry (MS) 5977B MS selective detector with slight
modification.13 The oven temperature was maintained at 40oC, then it was increased by 2oC/min to 230oC.
The identification was carried out using the NIST 2017 MS Library.
DPPH Free Radical Scavenging Activity
The free radical scavenging activity of four extracts (n-hexane, dichloromethane, ethyl acetate, and MeOH)
from sponge materials of O. asiatica and E. carteri was measured by DPPH free radical with some
modifications.14 Briefly, the reaction mixture containing 100 μL of DPPH solution and 20 μL of samples
with various concentrations was shaken vigorously and incubated for 30 minutes at room temperature.
Afterward, absorbance was read at 517 nm. The lower absorbance of the reaction mixture is indicated by
higher free radical scavenging activity. BHT and BHA were used as the antioxidant standard.
ABTS Free Radical Scavenging Activity
The ABTS free radical scavenging activity was examined using the previous method with some
modifications.15 Briefly, 20 μL of various concentrations of the samples were added to 100 μL of ABTS
solution. The reaction mixture was incubated at room temperature for 30 minutes, then the absorbance was
measured at 750 nm using a ThermoScientific Multiscan Sky High microplate reader. BHT and BHA were
used as the antioxidant standards.
α-Glucosidase Inhibitory Activity
The α-glucosidase inhibitory activity was slightly modified according to standard procedures following the
hydrolysis of nitrophenyl glycosides.16 Briefly, the reaction mixture contained 40 μL of enzyme solution
(Baker’s yeast α-glucosidase), 50 μL of p-NPG in buffer phosphate pH 6.9, and various concentrations of
test samples. The reaction mixture was incubated at 37oC for 20 minutes and the reaction was terminated
by adding Na2CO3 1M. After incubation, the absorbance was measured spectrophotometrically at 405 nm.
Acarbose was used as the positive standard.
RESULTS AND DISCUSSION
Table-1 shows the findings of the phytochemical screening test performed on the four different freshwater
sponge extracts. In short, it was observed that the process of partitioning from non-polar (n-hexane) to polar
solvent (methanol) demonstrated reasonably effective separation. All extracts of freshwater sponges (O.
asiatica and E. carteri) resulted in positive for the alkaloid test, except for the polar fraction (MeOH).
Furthermore, the n-hexane and dichloromethane extract of O. asiatica showed the presence of triterpenoids,
while the ethyl acetate extract of O. asiatica showed the presence of saponins. Meanwhile, the n-hexane
and dichloromethane extract of E. carteri showed the presence of alkaloids and triterpenoids.
Unfortunately, other phytochemicals such as flavonoids and phenolic were absent in all freshwater sponge
extracts. However, this finding is in line with previous studies that reported that sterols and long chains
(fatty acids) compounds were present in the genus of Metaniam and Drulia (Metaniidae), and
Ochridaspongia rotunda Arndt (Malawispongiidae) freshwater sponges.4,8,9

Table-1: Phytochemical Screening of Freshwaters Sponges (O. asiatica and E. carteri)

Phytochemicals
No Samples
Alkaloids Flavonoids Saponins Phenolic Triterpenoids
1 Oncosclera asiatica
n-Hexane fraction + - - - +
Dichloromethane fraction + - - - +
Ethyl acetate fraction + - + - -
MeOH fraction - - - - -
2 Eunapius carteri
n-Hexane fraction + - - - +
Dichloromethane fraction + - - - +
Ethyl acetate fraction + - - - -
MeOH fraction - - - - -
(+) presence; (-) absence
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To the best of the authors’ knowledge, no records of phytochemicals of O. asiatica and E. carteri freshwater
sponges inhabiting the Porong River area were found in any previous study.
Table-2 displays the results of a qualitative GC-MS analysis of the phytochemicals found in the n-hexane,
dichloromethane, and ethyl acetate extracts of the two freshwater sponges. 43 chemical components of O.
asiatica and E. carteri were found in the n-hexane, dichloromethane, and ethyl acetate extracts together
with their retention times. By comparing the peak retention time and mass spectrum fragmentations of both
freshwater sponge extracts to their analog published in the NIST library, the GC-MS chromatogram of n-
hexane, dichloromethane, and ethyl acetate extracts was identified (data not shown). Figure-1 shows that
four fractions of freshwater sponges O. asiatica and E. carteri contain a variety of secondary metabolites.
In this observation, the presence of fatty acid esters such as hexadecanoic acid, methyl ester; 9-
hexadecenoic acid, methyl ester, (Z); 9,12-Octadecadienoyl chloride (Z, Z); 9-Octadecenamide (Z); and
decanedioic acid, dibutyl ester demonstrated various biological activities, including analgesic, ulcerogenic,
anti-inflammatory, anti-bacterial, and hypolipidemic effect.17,18 Hexadecanoic acid, also known as methyl
ester of α-linoleic acid, was found in a prior study that showed its biological activity as an anticancer,
antibacterial, and anti-inflammatory agent.16
Table-2: Chemical Components of O. asiatica and E. carteri

Samples* Chemical Compounds RT**

Oncosclera asiatica
n-hexane 1-Hexadecanol 17.55
Tributyl acetylcitrate 21.24
Ethyl acetate 2-butyltetrahydrofuran 14.53
1-Hexadecanol 17.55
Hexadecanoic acid, methyl ester 18.00
1-Propene-1,2,3-tricarboxylic acid, tributyl ester 20.29
Tributyl acetylcitrate 21.29
9-Octadecenamide, (Z)- 22.14
Dichloromethane benzeneacetonitrile, alpha-[(4-cyanophenyl) methylene]-4-nitro 115.84
Morphinan-6-ol, 4,5-epoxy-N-methyl -, (5alpha., 6beta) 117.25
6-Bromo-1-methyl-2-oxoquinoline-4- carboxylic acid 117.85
Eunapius carteri
n-hexane 1,3,5,7-Cyclooctatetraene 4.32
2-butyltetrahydrofuran 14.51
Hexadecamethyl cyclooctasiloxane 15.23
Methyl tetradecanoate 15.87
1-Tetradecanol 16.61
Octadecamethyl cyclononasiloxane 16.99
9-Hexadecenoic acid, methyl ester, (Z) 17.80
Hexadecanoic acid, methyl ester 18.00
Didecyl phthalate 18.43
Cycloheptasiloxane, tetradecamethyl- 18.57
9,12-Octadecadienoyl chloride, (Z,Z) 19.75
Methyl tetradecanoate 19.94
13-Docosenamide, (Z)- 20.54
Tributyl acetylcitrate 21.23
9-Octadecenamide, (Z)- 22.15
Propanoic acid, 3-ethoxy-, ethyl ester 22.15
Ethyl acetate 1-Dodecanol 12.96
2-butyltetrahydrofuran 14.62
Cyclooctasiloxane, hexadecamethyl- 15.24
1-Hexadecanol 17.57
Hexadecanoic acid, methyl ester 18.00
1-Propene-1,2,3-tricarboxylic acid, tributyl ester 20.32
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Tributyl acetylcitrate 21.29

9-Octadecenamide, (Z) 22.20
1,3-Benzenedicarboxylic acid, bis(2-ethylhexyl) ester 25.20
Dichloromethane Decanedioic acid, dibutyl ester 82.60
Butyl citrate 86.78
4,5-Difluoro-2-methyl-phenyl) -(4-methyl-piperidin-1-yl)- 103.90
methanone
1-Naphthalenecarboxamide, N-(3-chlrophenyl) 104.70
9-Octadecenamide, (Z)- 105.73
6-Bromo-1-methyl-2-oxoquinoline-4-carboxylic acid 114.58
Benzamide, N-(3-methylphenyl)-2,3, 4-trifluoro 117.50
* GC/MS analysis was not performed on the methanol extract
** RT (retention time) in minutes
Tributyl acetyl citrate was also shown to offer the potential to be a flavoring component in pharmaceutical
medication production.19 Oleamide, also known as 9-octadecenamide (Z), is a fatty acid amide. It may bind
to cannabinoid receptors and cause a wide range of biological effects, including the induction of sleep,
immunosuppression, and the activation of the serotonin and GABA receptors. 20 These findings collectively
showed that the two freshwater sponges, O. asiatica and E. carteri, had a variety of secondary metabolites
with potential biological activities. The chemical makeup of O. asiatica and E. carteri has not yet been the
subject of any investigations that have been described in the literature.

Tributyl acetylcitrate 2-butyltetrahydrofuran Hexadecanoic acid, methyl ester

9-Hexadecenoic acid, methyl ester, (Z) 9,12-Octadecadienoyl chloride, (Z,Z)

9-Octadecenamide, (Z)Decanedioic acid, dibutyl ester

Fig.-1: GC-MS Detection of Possible Bioactive Compounds (selected) from two Freshwater Sponges (O. asiatica
and E. carteri)
The investigated biological activities of two freshwater sponges (O. asiatica and E. carteri) were further
determined using α-glucosidase inhibitory activity and free radical scavenging activity. In this study, two
different approaches were successfully employed to examine the antioxidant capacity of the two freshwater
sponges, namely DPPH and ABTS free radical scavenging activities presented in Fig.-2 and Fig.-3. These
results were compared with butylated hydroxytoluene (BHT) and butylated hydroxyanisole (BHA) as
positive standards.
The antioxidant activity of four fractions of the two freshwater sponges was determined on the basis of
DPPH free radical scavenging activity (Fig.-2). Among the samples, the n-hexane fractions of both O.
asiatica and E. carteri displayed the best percentage of inhibition values of 39.90% and 47.78%
respectively. Meanwhile, the other fractions exhibited the lowest percentage of inhibition at 10 mg/mL.
Different solvent extracts of the two freshwater sponges showed the potency scavenging activity in
descending order of n-hexane > dichloromethane > ethyl acetate > methanol.
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Fig.-2: DPPH Free Radical Scavenging Activity of O. asiatica and E. carteri

These results are quite similar to a previous study that reported that freshwater sponges from Lake Baikal
had very low antioxidant activity.21 Furthermore, the free radical scavenging activity of the two freshwater
sponges was also assessed using ABTS free radicals. The inhibition percentage (%) values of the two
freshwater sponge extracts against ABTS free radical are shown in Fig.-3. Unfortunately, all examined
extracts showed the lowest inhibition against ABTS free radicals.

Fig.-3: ABTS Free Radical Scavenging Activity of O. asiatica and E. carteri

To continue our investigation, the antidiabetic activity of O. asiatica and E. carteri fractions was also
evaluated against α-glucosidase. As presented in Table-3, among four O. asiatica fractions at concentrations
of 1, 5, and 10 mg/mL, n-hexane fraction demonstrated a concentration-dependent inhibitory activity
against α-glucosidase with percent inhibition of 10.46%, 11.64%, and 23.43% respectively. Unfortunately,
other fractions of O. asiatica showed no inhibitory activity against α-glucosidase.
Table-3: α-Glucosidase Inhibitory Activity of O. asiatica and E. carteri
Percent inhibition (%)a
No Samples
1 mg/mL 5 mg/mL 10 mg/mL
1 Oncosclera asiatica
n-Hexane fraction 10.46 ± 3.13 11.64 ± 0.55 23.43 ± 0.40
Dichloromethane fraction NIb NI NI
Ethyl acetate fraction NI NI NI
MeOH fraction NI NI NI
2 Eunapius carteri
n-Hexane fraction 38.96 ± 1.78 48.59 ± 1.63 55.86 ± 1.28
Dichloromethane fraction NI NI NI
Ethyl acetate fraction 60.07 ± 1.47 70.24 ± 1.20 79.96 ± 1.15
MeOH fraction NI NI NI
3 Quercetin 0.1 mg/mL 60.03 ± 1.79
Quercetin 1 mg/mL 87.56 ± 3.11
a
Data is shown as the mean of triplicate experiments ± SD.
b
No inhibition, inhibitory activities less than 10% at 10 mg/Ml
Furthermore, the inhibitory effects of α-glucosidase were measured also in four E. carteri fractions. The n-
hexane and ethyl acetate fractions demonstrated good inhibitory activity against α-glucosidase among the
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four fractions assayed. Surprisingly, as shown in Table-3, the ethyl acetate fraction of E. carteri exhibited
good inhibitory activity with a percent inhibition of 79.96% at a concentration of 10 mg/mL, whereas the
n-hexane fraction exhibited with percent inhibition of 55.86%. Quercetin, a positive standard α-glucosidase
inhibitor, also demonstrated a concentration-dependent inhibitory effect at 0.1 mg/mL and 1 mg/mL. These
results indicated that freshwater sponges O. asiatica and E. carteri can become a potential source with an
inhibitory effect against α-glucosidase. As far as the authors know, there has been no report of α-glucosidase
inhibitory activity in freshwater sponges O. asiatica and E. carteri. Taken all together, further research will
be directed toward a detailed chemical components analysis of these two freshwater sponges including
isolation and identification of phytochemicals that are responsible for the biological activities observed.
CONCLUSION
Unknown freshwater sponges from the Porong River in East Java province, such as Oncosclera asiatica
and Eunapius carteri, may contain a variety of pharmacological phytoconstituents. It has demonstrated
numerous pharmacological activities in the current investigation, including antioxidant and α-glucosidase
inhibitory action. This study's analysis of many phytochemicals, including fatty acids and sterols, suggested
that freshwater sponges from the Porong River may be a new supply of those substances for the
pharmaceutical sector. Consequently, more research is required to examine specific components of extracts
of freshwater sponges from the Porong River that could be responsible for other biological processes.
ACKNOWLEDGMENTS
The authors acknowledge the Directorate of Research and Community Service (DPRM)
of Institut Teknologi Sepuluh Nopember Surabaya, Universitas Diponegoro Semarang,
and Institut Teknologi Bandung for the consortium grant schemed as Program Penelitian Kolaborasi
Indonesia (PPKI) PTNBH 2021 number 1331/PKS/ITS/2021, 117-06/UN7.6.1/PP/2021, and
042/IT1.B07.1/SPP-LPPM/II/2021. In addition, the authors acknowledge the Department of Chemistry of
the Faculty of Science and Technology; Exploration and Synthesis of Bioactive Compounds Research
Group (ESBC); and University CoE-Research Center for Bio-Molecule Engineering (BIOME) at
Universitas Airlangga, Surabaya, Indonesia for their role in investigating chemical analyses. The authors’
gratitude also goes to the Chemical Division of Pharmacognosy and Toxicology, Faculty of Pharmaceutical
Sciences, Khon Kaen University and Center of Excellent in Natural Products (CENP), Department of
Chemistry, Faculty of Science, Chulalongkorn University Bangkok for assisting chemical analyses and
being international collaborators.
CONFLICT OF INTERESTS
The authors declare that there is no conflict of interest.
AUTHOR CONTRIBUTIONS
All the authors contributed significantly to this manuscript, participated in reviewing/editing, and approved
the final draft for publication. The research profile of the authors can be verified from their ORCID IDs,
given below:
E. Setiawan https://orcid.org/0000-0003-3947-3334
A. Yanuar https://orcid.org/0000-0002-2313-2765
C. Riani https://orcid.org/0000-0001-7082-0264
A. Budiharjo https://orcid.org/0000-0002-4815-5138
Y.F.H. Firdaus http://orchid.org/0009-0005-6642-5698
K. Phontree http://orchid.org/0009-0005-1952-3105
P. Phuwapraisirisan http://orchid.org/0000-0001-6481-7712
R. Ramadhan https://orcid.org/0000-0002-2565-7944
Open Access: This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s)
and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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[RJC-8435/2023]

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FRESHWATER SPONGES ONCOSCLERA ASIATICA AND EUNAPIUS CARTERI FROM EAST JAVA, INDONESIA E. Setiawan et al.