A Review on Phytochemicals and Biological Activities of Seagrass

Journal of Critical Reviews

ISSN- 2394-5125 Vol 7, Issue 7, 2020

A REVIEW ON PHYTOCHEMICALS AND BIOLOGICAL ACTIVITIES OF SEAGRASS

Kavitha D1,2, Kalaivani P1, Vanitha V1*

1Department of Biochemistry, Vels Institute of Science, Technology and Advanced Studies, Pallavaram, Chennai-600117, Tamil Nadu, India 2GIET School of Pharmacy, NH-16, Chaitanya Knowledge City, Rajahmundry -533296, Andhra Pradesh, India Corresponding author E-mail ID: [email protected]

Received: 01.02.2020 Revised: 05.03.2020 Accepted: 07.04.2020

Abstract Seagrasses are the residents of the coastal waters, globally which are rated as one of the most valuable ecosystems. During photosynthesis, they release oxygen to the water column and also pumps oxygen into the sediments through their roots to create an anoxic environment around roots to support extensive nutrient uptake. They are represented as one of the highly productive coastal ecosystem as well as of protects the shorelines against the erosion in the middle, lower intertidal and subtidal zones of the world. In folk medicine, seagrasses have been used for a variety of remedial purposes. But there is no review concerning various uses of seagrasses. In the presented study, an attempt had been made on various species of seagrass and find out the different phytochemicals and pharmacological uses.

Keywords: Seagrasses; Phytochemicals; Pharmacological uses; Anti cancer activity

INTRODUCTION: This review work provides an adequate knowledge about An ecosystem is a geographic area where plants, animals, and seagrasses, their phytochemical constituents, the biological effect other organisms together to form a bubble of life [1]. There is of recent findings such as antibacterial, anti-inflammatory, anti- plenty of ecosystems is existing in the galaxy [2]. The marine cancer, anti-viral, anti-oxidant, tranquillizer and their future ecosystem is one of a vital and complex ecosystem in the world perspectives. [3]. In the marine, Seagrasses are primary producer where most of the fish’s feeds [4]. When compared to the coral and mangrove In the present review, we discussed about species of sea grasses ecosystems, Sea grasses are one of the most widespread types of available around the world and their biological activities along coastal vegetation [5]. It is a ribbon-like grassy leaf and not a with phytochemical constituents. From the literature survey terrestrial Poaceae [6]. It is a flowering plant and completes its much information was not found regarding biological activity. So, life cycle when they are submerged in seawater [7]. Seagrass is a we focussed on biological activities and prolonged to current and hydrophyte that lives in tropical or subtropical coastal areas [8]. future scope of work on sea grass in order to step forward for These plants have developed unique physiological, researches to focus towards commercialization of natural morphological and ecological adaptations for a completely products from sea grass. submerged existence, which include submarine pollution, internal gas transport, marine dispersal and epidermal Various species of seagrasses in India chloroplasts which provide with important ecological services to Scientific communities and environmentalists have shown less the marine environment [9]. It is the lagoons around the islands priority on seagrass research in olden days. In the recent times, and extends a depth of 10-15 m along the open shores. They are alot of interest had been given on the seagrass researchdue to the critical aquatic plants as they maintain the quality of the water by different therapeutic activities were found in the seagrass. Six removing pollutant effectively from marine waters and genera and thirteen species of seagrass were seen in India [24], sediments in the coastal areas [10]. Around the world, there are in which maximum number of species were identified in the gulf fifty-two species of seagrasses were found so far in which 14 of mannar, palle bay harbor than Andaman and Nicobar species were identified in the east and west coastal part of India. Lakshadweep islands. These are belonging to the families of Zoseraceae, Cymodoceaceae, Posidoniaceae and Hydrocharitaceae [11]. Seagrass in India Biomass of seagrass has been used often as food and medicine by Class - Monocotyledons coastal indigenous society [12]. It has been known as marine Order - Helobiae forms can be used against microbial attack [13]. In addition to that, they have been used for traditional medicine such as fever Genera and Species [14], anti-inflammatory [15], muscle pain, anti-oxidant [16], skin Family-Hydrocharitaceae disease [17], anti-viral [18], stomach problems [19], anti-diabetic 1. Enhalus acoroides [20], wounds [21], tranquillizer [22] and anti-cancer activities 2. Halophila ovalis [23] etc., However, many seagrasses are vulnerable to 3. Halophila ovata degradation due to developmental activities in the coastal areas. 4. Halophila stipulacea If it is not properly protected, may not available to the next 5. Halophila beccarii generation. Therefore, there is a need to take some measurement 6. Halophila decipiens to safeguard the seagrass and ensure the availability of 7. Thalassia hemprichii therapeutic effects of seagrass to the needy in future. In the last Family –Polamogetanaceae two decades, several scientists all over the world had paid much 8. Cymodocea rotundata interest in seagrass and found with different therapeutic 9. Cymodocea serrulata activities. But there is no review on seagrass of the latest finding. 10. Halodule univervis 11. Halodule pinifolia

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12. Halodule wrightii 13. Syringodium isoetifolium.

Table 1: Morphology and uses of various seagrass species

Enhalus acorides

Common Name: Tape grass Distributed in gulf of mannar and Andaman & Nicobar Island Found is shallow area & muddy regions. They are used in the treatment of oxidative stress related diseases [25]

Halophila ovalis

Common Name: Paddle weed Distributed in Indo-west and pacific Found on more sheltered muddy substrate Used in the treatment of skin diseases [26](John etal., 2001)

Halophila Ovata

Common Name: Spoon grass Distributed at gulf of Kachchh, Konkan coast Small Marine herb grows just above the low water mark Used in treatment for dandruff and iron deficiency disease [27]

Halophila Stipulacea

Common Name: Minnipassi Distributed at Gulf of mannar and palk bay Fleshy and branched, pale green in colour with a length of 2-6cm. Found in tropical and sub tropical water [28]

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Halophila beccarii

Common Name: Ocean turf grass Distributed in Gulf of mannar, palk bay Long oval shaped leaves with 0.5cm long. Found in muddy sand and coastal area. Has antifungal activity [29]

Halophila decipiens

Common Name: Paddle grass Distributed in the gulf of mannar, palk bay and kalpani island Leaves are paddle shaped up to 25mm long and 6mm wide Found in both deep and shallow area [30]

Thalassia hemprichii

Common Name: Turtle grass Distributed in gulf of mannar, palk bay, Andaman & Nicobar Islands & Lakshadweep Islands Sickle shaped leaves with 0.5-1cm wide and 7-40 cm long Found in marine Used for the treatment of depression, fever and malaria [31]

Cymodocea rotundata

Common Name: Ribbon sea grass Distributed in Lakshadweep Islands, Gulf of mannar, palk Bay, Andaman and Nicobar Islands Long ribbon like leaves 7-15cm with blunt rounded tips Grown in clear water Used as tranquilizer for infants [22]

Cymodocea serrulata

Common Name: Karumbupassi Distributed in Gulf of Mannar, Andaman& Nicobar Islands, Palk Bay and Lakshadweep Islands Long ribbon like leaves with blunt and round tips Grown in muddy sand Has antibacterial activity [32]

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Halodule uninervis

Common Name: Sinnaeekkupassi Distributed in Tamilnadu coast, palk Bay, Lakshadweep islands Fast growing grass with patching appearance Found in low tide on cleans and benches

Has antimicrobial activity [33]

Halodule pinifolia

Common Name: Arugampul Passi Distributed in Lakshadweep islands palk Bay, Andaman & Nicobar Islands and Gulf of mannar Has narrow leaves with 3-15cm long Seen in muddy and coral areas Has antibacterial activity [34]

Halodule wrightii

Common name: Shoal grass Distributed in Gulf of mannar Grass like species with flat and bladdy appearance Seen in muddy & sandy place Used as tolerant of environmental conditions [35]

Syringodium isoetifolium

Common Name: Tube Grass Distributed in Gulf of manner, Andaman & Nicobar Islands Leaves with 5-10cm long with tubular leaves Seen in coral beds Used as larvicidal agent and has scavenging activity [36]

Photochemical constituents seagrasses was found to be very high compared to seaweed but There are many seagrasses are there in the world. Each one are the level of carbohydrate, lipid is very low. Photochemical getting differ from the others by not only its appearances but constituents of Indian seagrass were summarized in Table 2. also in the primary, secondary metabolites present in it and their Presence of these components in seagrass offers different quantities. These constituents are phenolic compounds, therapeutic activities such as antioxidant, anti-viral, anticancer, flavonoid, tannin, proteins, vitamins, sugar, steroid, alkolids, anti-inflammatory, pyretic muscle pain, skin disease stomach saponin, amino acids etc.,and all of them were confirmed by problems anti-diabetic wounds tranquillizer and protection of appropriate methods. The amount of amino acids in the plant proteins from ruminants.

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Table 2: Phytochemical Constituents of Indian Seagrass species Seagrass Phenol Alkaloids Sugar Tannin Steroid Saponin Amino Flavonoid acid

Enhalus acoroides ++ + - ++ + + - ++

Halophilia ovalis ++ ++ - ++ + + + ++

Halophilia Ovata ++ ------

Halophilia stipulacea + ------++

Halophilia Beccarii + + + ++ + + - ++

Thalassia hemprichi + + + ++ + + + ++

Cymodocea rotundata + + + ++ + ++ - +

Cymodocea Serulata ++ ++ + + + ++ + +

Halodule Uninervis + + - - + - - +

Halodule Pinifolia + ++ + + + + + ++

Halodule Wrightii + - + - - - - +

Syringodium isoetifolium + + ++ + ++ + ++ + ++

(+) Positive sign indicates present, (-) Negative sign Indicates Absent (++) indicates higher concentration

Anti-oxidant agents methanolic extracts had shown remarkable antioxidant activity Anti-oxidants are defending your body cell from damage caused with a remarkable IC50 value of 78.95±1.15 and 85.40±3.40. by free radicals when they accumulated may cause oxidative stress. It is controlled by anti-oxidant therapy. The synthetic Inexpensive antioxidants in the leaves of eight species of antioxidants are producing more side effects, while natural seagrass by first time using DPPH radical scavenging method and antioxidants play a major role in scavenging of free radicals FRAP assay have been found by [39]. Leaves of Halophila without side-effect. stipulacea and Halophila pinifolia were exhibited the highest percentage of antioxidant score than the other species in DPPH Qualitative, quantitative level of phytochemicals and antioxidant method and FRAP assay because of having huge quantities of activity of extracts of leaves of Enhalus acoroides were phenolic compounds. The available phenolic content had been investigated [37]. The extracts were prepared from chloroform, shown a correlation of radical scavenging power and reducing hexane, water, ethanol and ethyl acetate solvents and assessed the power of the seagrass. He also suggested that isolation and their antioxidant activities by FRAP assay, DPPH, NO, H2O2 and characterization of individual phenolic compounds were ABTS methods. The result reveals that these extracts possessing required to treat the oxidative stress in future. a significant amount of flavonoids, steroids, phenols, tannins, saponins etc., The content of phenol and flavonoids in aqueous The antioxidant activity of seven seagrasses species in the south- extracts were found to be 78.36 mgGAE/g and 57.52 mgQu/g east coast of India through DPPH radical scavenging method respectively and exhibited excellent antioxidant activity with a were found by [40]. Initially, the component of these seagrasses maximum percentage of inhibition of free radicals. was extracted with suitable polar and a non-polar solvent such as ethyl acetate, butanol, aqueous and petroleum ether and Anti-oxidant effect of an ethanolic extract of leaf, root and identified the levels by TLC bioautography method. Later, each rhizome of Enhalus acorodies (L.F) Royle by using DPPH and extracted was screened for antioxidant activity DPPH radical FRAP assay was identified [18]. The result indicated that all the scavenging method. The result indicated that Thalassia extracts were exhibited promising antioxidant activity due to the hemprichii and Cymodocea serrulata were shown the highest presence of phenolic compounds and proanthocyanidins. They percentage of radical scavenging when compared to the others. found high percentage in leaf than root and rhizome of Enhalus acorodies (L.F) Royle. Therefore, the leaf extract had been shown The phytochemicals and antioxidant activity of extracts from sea the highest percentage of antioxidant activity in DPPH radical grass of Halodule pinifolia were identified by [41]. The result scavenging method (25.76±0.04), as well as excellent reducing indicated that the ethanolic extract of mentioned sea grass power, was observed in FRAP method (18.060±0.073) containing tannins, flavonoids, steroids, saponins and responsible for the above activities of Enhalus acorodies (L.F) triterpenoids etc., and also exhibited highest antioxidant activity Royle. (18.7 ppm) in DPPH radical scavenging method and FRAP assay (1.749). A set of five species of seagrasses and six of seaweeds of water, methanol extracts by using hydrogen peroxide, NO radical Twelve bacteria were identified from seagrass Syringodium scavenging methods were investigated [38]. All of them were isoetifolium bacterial symbionts by using 16srDNA PCR method shown significant anti-oxidant activity with the lowest IC50 value and found with carotenoid, peridinin and fucoxanthin etc., [42]. compared to tocopherol. Seagrass Halophila ovalis of water and The coloured pigments were isolated using methanol and screened for antioxidant activity through DPPH free radical scavenging method. The result reveals that the isolated bacterias

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were Bacillus amloliquefaciens and shown a significant effect of metabolites were significantly controlled the growth of the antioxidant activity due to the presence of carotenoids pigments pathogen in a less concentration and exhibited excellent present in it. antibacterial activity. The phytochemicals and antioxidant effect of four seagrass Phytochemical investigation and antibacterial activity of seagrass species called Thalassia hemprichii, Syringodium isoetifolium, Cymodocae rotundata were performed by [48] by using well Enhalus acoroides, Halodule pinifolia were evaluated by [43]. diffusion method. The active compounds of seagrass such as The aqueous methanolic extracts were prepared from the above- tannins, resins, proteins, saponins, acidic compounds terpenoids, metioned seagrass and calculated the phenolic content, alkaloids, phenols, steroids, catechols and cardiac glycosides antioxidant activity by using DPPH radical scavenging assay. The were extracted with ethanol, acetone and water. The result result suggested that seagrass had been maintaining the phenolic suggested that these extracts had been shown admirable content in the rage of 0.2878-1.0807 mg and offered admirable antibacterial activity on ten pathogen used due to the presence of antioxidant activity. phytochemicals. Among the different extract, ethanolic extract had been shown significant activity against pathogen than others. Anti-microbial An agent that kills and controls the growth of the pathogenic Anti-cancer organism is called anti-microbial agents and they classified based Cancer is a class of disease characterized by unrestrained cell on action against the micro-organisms. An agent kills the division. Any agents which control the growth of cancerous or organism is known as a disinfectant, whereas intended to inhibit malignancy cell is known as anticancer agents. They are mainly the growth called as anti-septic. Both of them were utilized to used to treat cancer, malignancy, carcinoma, sarcoma, tumour manage the disease and prophylaxis. They are producing high and leukaemia etc., These cancer cells are rapidly developing resistance against the micro-organism soon during the resistance against anticancer drugs. Therefore, there is need to treatment. Therefore, a novel agent is required to treat microbial come up with the new anticancer drug from a natural source infections. which offers nil resistance against cancer cells. The antibacterial properties of leaf and root extracts of Anti-proliferative activity of Halodule pinifolia by using MTT Syringodium isoetifolium seagrass using MIC and MBC methods assay against MCF & human breast cancer cells were reported were investigated [44]. The extract containing phosphatase [49]. The result suggested that ethyl acetate fraction of H. producing Actinoycetes sp. and Streptomyces sp. were Pinifolia was shown maximum activity against the cancer cell and responsible for a broad spectrum of activity against pathogenic no such effect had been seen against the normal cell. In addition bacteria. GC-MS was used to identify the 1,4 dihydroxy-2-3- to that, it can be used as an alternative treatment of cancer. hydroxybutyl)-9,10 anthraquinone 9,10-anthrac in Actinoycetes species. The result reveals that Actinoycetes, Streptomyces The in-vitro anticancer activity of Cymodecea serrulate seagrass species had been played a major role to achieving antibacterial against HeLa cell using MTT assay was investigated [50]. The effect of Syringodium isoetifolium seagrass. active components were extracted from leaves by admixing with ethyl acetate (semipolar), n-hexane (non-polar) and ethanol The antimicrobial activity of seagrass species Syringodium (polar). The results suggested that non-polar extract has isoetifolium and Cymodocea serrulata against different bacterial negligible activity against cancer cell, whereas semipolar and pathogens such as Bacillus cereus, Pseudomonas mirabilis, polar solvent exhibited admirable anticancer activity as standard Proteus vulgaris , Pseudomonas aeruginosa, paraheamolyticus, drug doxorubicin. In addition to that, the fresh leave of salmonella enteritidis and staphylococcus aureus using agar Cymodecea serrulate in ethyl acetate containing an alkaloid, diffusion method were carried out by [45]. Initially, the active polyphenol, terpenoid and flavonoid etc. components of these seagrasses were extracted with dichloroethane, acetone ethanol and methanol and then In another report stated that Zosteracaespitosa Miki seagrass performed the antibacterial activity. The result reveals that the had been shown significant antitumor properties against antibacterial activities of ethanolic and methanolic extract of S. HUVECs and the mouse macrophage cell line Raw 264.7 using isoetifolium found to be more potent against E. coli, V. MTT assay [51]. An apigalacturonan-rich polysaccharide and paraheamolyticus and P. aeruginosa, whereas same extracts ZPMC were extracted through admixing with solvents. The were exhibiting minimum activity against S. aureus. Cymodocea isolated compounds were confirmed by acidic, pectinase serrulate had been reduced the bacterial growth in all nine degradation, mass spectrometer and NMR spectroscopy. species of bacteria. Anti-viral Antibacterial, haemolytic and cytotoxic effect of aqueous Antiviral agents are control the growth of virus, so that they are methanolic extracts of six seagrasses such as Halodule pinifolia, exclusively used against virus infections. These agents are Enhalus acoroids, Thalassiah emprichii, Syringodium causing harm to the virus by inhibiting the penetration, isoetifolium, Cymodocea serrulate and Cymodocea rotundata uncoating, protein synthesis and viral replications etc., The using disc diffusion, minimum inhibitory concentration, brine prolonged treatment of anti-viral therapy causes resistance on shrimp lethality assay and haemolytic assay were reported by antiviral drugs, therefore virus is growing without any problem [46]. The result reveals that Halodule pinifolia and Cymodocea in the presence of anti-viral drugs. It has been controlled by rotundata were shown significant activity against all type of newer antiviral agent from natural sources. human pathogens and Syringodium isoetifolium had been offered lesser cytotoxicity compared to the other species. In A new series of HIV integrase inhibitor had been identified and addition to that, H pinifolia had been exhibited low haemolytic isolated form Thalassia testudinum seagrass [52]. Thalassiolins activity. flavones was a key ingredient present in the mentioned seagrass showing considerable differences from other flavones by Phytochemicals of Cymodocea nodosa were isolated from the substitution of sulfated Beta D-glucose at 7th position. The organic extract by [47] and performed an antibacterial activity molecular modeling results suggested that the thalassiolins using minimum inhibitory concentration method. binded effectively with the core domain of HIV-1 intergrase and Diarylheptanoids, monoterpenoids and brominated offered excellent activity. briarnediterpene are the metabolites found in the seagrass were utilized for the assessment of the antibacterial activity against multidrug resistant pathogens. The result reveals that all the

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Nutritional Value 3. Barbier, E.B., 2017. Marine ecosys serv. Curr Biol. 27,431- Seagrass species E.acoroides , H.beccarii , H.ovalis , C.rotundata , 510. c,serrulata , H. Pinifolia and S.isoetifolium has numerous calorific 4. Zarco-Perello, S., Enriquez, S., 2019. Remote underwater content and the above eight species of seagrass were collected video reveals higher fish diversity and abundance in and analyzed for biochemical constitutents [53]. Differences seagrass meadows and habitat differences in trophic were studied using ANOVA. It was found that calorific values are interactions. Sci Rep. 9,6596. present in rhizomes and leaves of seagrass, but the presence of 5. Nordlund, L.M., Jackson, E.L., Nakaoka, M., 2018. Seagrass phenol and tannins if removed by proper way it can be used in ecosystem services-What’s next. Marine poll Bull. 134,145- human diet. 151. 6. Newmaster, A.F., Berg, K.J., Ragupathi, S., 2011. Local Bio-Indicator knowledge and conservation of seagrasses in the Tamilnadu Several studies repoted that seagrass as a bioindicator for metal state of India. J Ethnobiol Ethnomed. 7,37. monitoring purposes. Trace metal such as cadmium Nickel, lead, 7. Ahmad-Kamil, E.I., Ramli, R., Jaaman, S.A., 2013. The effects zinc creates environmental pollution whereas E-acroides used as of water parameters on monthly seagrass percentage cover a potential bioindicator of metal pollution [54]. Several studies in lawas, East Malaysia. Scient World J. 892746,1-8. were done by numerous research and findings revealed that root, 8. Nelson, W.G., 2017. Development of an epiphyte indicator of rhizomes and blades of E.acroides are capable of accumulating nutrient enrichment: a critical evaluation of observational (cadmium, copper, nickel, lead and zinc).Therefore E.acorides is a and experimental studies. Ecol Indic 79,207-227. potential bioindicator in estuarine ecosystems. 9. Orth, R.J., Carruthers, T.J.B., Dennison, W.C., 2006. A Global crisis for seagrass ecosystems. Bio Sci 56(12),987-996. Current and Future Research on Seagrass Natural Products 10. Gumusay, M.U., Bakirman, T., Kizilkaya, T., 2019. A review of What we found the activities from seagrass in less and it is need seagrass detection, mapping and monitoring applications to scrutiny more and get lot of biological activity from them, if it using acoustic systems. Eur J Remote Sens. 52(1),1-29. is done the vast research. Seagrass is a one of the trusted and well-known natural source offering different biological activity 11. Ugarelli, K., Chakrabarti, S., Laas, P., 2017. The seagrass on human beings. At present many of the scientist had been holobiont and its microbiome. Micororganisms. 5(4),81. taken seagrass because of their versatility and identified the 12. Vieira, M.N.C.S., Lopes, I.E., Creed, J.C., 2018. The biomass- different biological activities. Protocol for establishing the cell density relationship in seagrasses and its use as an suspension culture for three seagrass species (H. pinifolia, H. ecological indicator. BMC Ecol. 18(44),2-16. ovalis, and C. serrulata) was achieved recently. Though it can be 13. Macreadie, P.I., Atwood, T.B., Seymour, J.R., 2019. used in many purposes, the components of seagrass responsible Vulnerability of seagrass blue carbon to microbial attack for their activities yet to identify. Therefore, many of researchers following exposure to warming and oxygen. Sci Total want to select their domain as seagrass and find out each Environ. 686,264-275. components of seagrass and their activities. Recently, the 14. Nordlund, L.N., Koch, E.W., Barbier, E.B., 2016. Seagrass phenolic profile of callus and in vitro suspension cultured cells ecosystem services and their variability across genera and (SCC) of seagrasses provedundoubtedly that seagrasses can be geographical regions. PLoS One. 11(10), e0163091. used as the alternate source for the biosynthesis of natural 15. Yuvaraj, N., Kanmani, P., Sathishkumar, R., 2012. Seagrass as antioxidants and can be synthesizedin relatively large quantities a potential source of natural antioxidant and anti- by SCC. inflammatory agents. Pharm Bio. 50(4),458-467. 16. Osukoya, O.A., Adegbenro, D., Onikanni, S.A., 2016. CONCLUSION Antinociceptive and antioxidant activities of the methanolic With the aid of various literatures on seagrass, we enlisted here extract of Telfairiaoccidentalis seed. Anc Sci Life. 36(2),98- different seagrass types and their occurrence, phytochemical 103. constituents, pharmacological activities and future perspectives. 17. Unsworth, R.K.F., McKenie, L.J., Collier, C.J., 2019. Global All the literatures reveal that high therapeutic profile of seagrass challenges for seagrass conservation. Ambio. 48,801-815. as an 18. Kannan, R.R.R., Arumugam, R., Anantharaman, P., 2010. anti-microbial, antioxidant, cytotoxic, anti-viral etc., in the last Antibacterial potential of three seagrasses against human two decades. In the recent time, it could be turned as vital pathogens. Asian pac J Trop Med. 890-893. resource for getting different pharmacological effects in several 19. Torre-Castro, M., Carlo, G.D., Jiddawi, N.S., 2014. Seagrass countries. It is a correct time to take some more research on importance for a small-scale fishery in the tropics: The need seagrass and find the different pharmacological activities with nil for seascape management. Marine pollution Bulletin. side-effects because they are considered as a trusted natural 83(2),398-407. source. 20. Styshova, O.N., Popov, A.M., Artyukov, A.A., 2017. Main constituents of polyphenol complex form seagrasses of the Source of funding genus zostera, their anti diabetic properties and There is no external funding for this project. 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