Effects of morphometric and biochemical parameters on collagen and pepsin-solubilized collagen yields of Holothuria tubulosa (Gmelin, 1790) and Holothuria (Roweothuria) poli (Delle Chiaje, 1823)

• Autorzy: Künili, İbrahim Ender
• Języki publikacji: EN

Abstrakty

EN

Due to their unique biochemical composition, sea cucumbers are highly prized marine echinoderm species. One of their most important properties is that they contain a high amount of collagen in their body wall. In this study, the relationship between collagen and pepsin-solubilized collagen yields from Holothuria tubulosa and Holothuria poli and morphometric and biochemical parameters were investigated. Collagen yields were in the range of 10.63–16.04% for H. tubulosa and 7.12–13.10% for H. poli. It was determined that they may be related to length, body wall weight, and biochemical composition at different length frequencies. Moreover, maturity may have a direct effect on the yield, as mature specimens were found to have lower content of collagen, whereas immature small specimens contained a higher percentage of collagen. It was found that with increasing pepsin concentration, the PSC yield increased to 1.83–1.89% in H. tubulosa and H. poli, respectively. It was determined that collagen from smaller individuals, which contained more moisture and ash, was likely more susceptible to pepsin hydrolyzation. This is the first published study demonstrating that collagen yield of sea cucumbers can vary with length, weight, maturity, and biochemical composition, in addition to species-specific differences.

Słowa kluczowe

EN

collagen yield; pepsin-soluble collagen; length–weight relationship; maturity; sea cucumber

• Czasopismo: Oceanological and Hydrobiological Studies
• Rocznik: 2022
• Tom: Vol. 51, No. 1
• Strony: 100--114
• Opis fizyczny: Bibliogr. 92 poz., map., rys., wykr.

Twórcy

autor

Künili, İbrahim Ender

• Department of Fishing and Processing Technology, Faculty of Marine Sciences and Technology, Çanakkale Onsekiz Mart University, Çanakkale, Turkey,

Bibliografia

• [1]. Adibzadeh, N., Aminzadeh, S., Jamili, S., Karkhane, A. A., & Farrokhi, N. (2014). Purification and characterization of pepsin-solubilized collagen from skin of sea cucumber Holothuria parva. Applied Biochemistry and Biotechnology, 173, 143-154. https://doi.org/10.1007/s12010-014-0823-4 PMID:24676570
• [2]. Antoniadou, C., & Vafidis, D. (2011). Population structure of the traditionally exploited holothurian Holothuria tubulosa in the south Aegean Sea. Cahiers de Biologie Marine, 52, 171-175.
• AOAC. (2000). Official Methods of Analysis of the AOAC International (17th). Association of Official Analytical Chemists.
• [3]. Asha, P. S., & Muthiah, P. (2008). Reproductive biology of the commercial sea cucumber Holothuria spinifera (Echinodermata: Holothuroidea) from Tuticorin, Tamil Nadu, India. Aquaculture International, 16, 231-242. https://doi.org/10.1007/s10499-007-9140-z
• [4]. Aydın, M. (2008). The commercial sea cucumbers fishery in Turkey. SPC Beche-de-mer Information Bulletin, 28, 40-43.
• [5]. Aydın, M., Sevgili, H., Tufan, B., Emre, Y., & Köse, S. (2011). Proximate composition and fatty acid profile of three different fresh and dried commercial sea cucumbers from Turkey. International Journal of Food Science & Technology, 46, 500-508. https://doi.org/10.1111/j.1365-2621.2010.02512.x
• [6]. Aydın, M., & Erkan, S. (2015). Identification and some biological characteristics of commercial sea cucumber in the Turkey coast waters. International Journal of Fisheries and Aquatic Studies, 3, 260-265.
• [7]. Aydın, M. (2019). Biometry, density and the biomass of the commercial sea cucumber population of the Aegean Sea. Turkish Journal of Fisheries and Aquatic Sciences, 19(6), 463-474. https://doi.org/10.4194/1303-2712-v19_6_02
• [8]. Aydın, M. (2020). Length-Weight Relationships and Condition Factor of Four Different Sea Cucumber Species in the Aegean Sea. Journal of Anatolian Environmental and Animal Sciences, 5, 80-85. https://doi.org/10.35229/jaes.677940
• [9]. Barzideh, Z., Latiff, A. A., Gan, C.-Y., Benjakul, S., & Karim, A. A. (2014). Isolation and characterisation of collagen from the ribbon jellyfish (Chrysaora sp.). International Journal of Food Science & Technology, 49, 1490-1499. https://doi.org/10.1111/ijfs.12464
• [10]. Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37, 911-917. https://doi.org/10.1139/y59-099 PMID:13671378
• [11]. Bechtel, P. J., Oliveira, A. C. M., Demir, N., & Smiley, S. (2013). Chemical composition of the giant red sea cucumber, Parastichopus californicus, commercially harvested in Alaska. Food Science & Nutrition, 1, 63-73. https://doi.org/10.1002/fsn3.12 PMID:24804015
• [12]. Benedetto, C. D., Barbaglio, A., Martinello, T., Alongi, V., Fassini, D., Cullorà, E., Patruno, M., Bonasoro, F., Barbosa, M. A., Carnevali, M. D., & Sugni, M. (2014). Production, characterization and biocompatibility of marine collagen matrices from an alternative and sustainable source: The sea urchin Paracentrotus lividus. Marine Drugs, 12(9), 4912-4933. https://doi.org/10.3390/md12094912 PMID:25255130
• [13]. Bordbar, S., Anwar, F., & Saari, N. (2011). High-value components and bioactives from sea cucumbers for functional foods—A review. Marine Drugs, 9, 1761-1805. https://doi.org/10.3390/md9101761 PMID:22072996
• [14]. Borrero-Pérez, G. H., González-Wangüemert, M., Marcos, C., & Pérez-Ruzafa, A. (2011). Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: The combined effects of historical processes and current oceanographical pattern. Molecular Ecology, 20, 1964-1975. https://doi.org/10.1111/j.1365-294X.2011.05068.x PMID:21463375
• [15]. Chen, J. (2003). Overview of sea cucumber farming and sea ranching practices in China. SPC Bech de mer Information Bulletin. 18:24-33.
• [16]. Arik Colakoglu, F., Ormanci, H. B., Berik, N., Künili, I. E., & Colakoglu, S. (2011). Proximate and elemental composition of Chamelea gallina from the southern coast of the Marmara Sea (Turkey). Biological Trace Element Research, 143, 983-991. https://doi.org/10.1007/s12011-010-8943-3 PMID:21225478
• [17]. Conand, C. (1981). Sexual cycle of three commercially important Holothurian species (Echinodermata) from the lagoon of New Caledonia. Bulletin of Marine Science, 31, 523-543.
• [18]. Conand, C. (1993). Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Marine Biology, 116, 439-450. https://doi.org/10.1007/BF00350061
• [19]. Coppola, D., Oliviero, M., Vitale, G. A., Lauritano, C., D’Ambra, I., Iannace, S., & de Pascale, D. (2020). Marine Collagen from Alternative and Sustainable Sources: Extraction, Processing and Applications. Marine Drugs, 18, 214. https://doi.org/10.3390/md18040214 PMID:32326635
• [20]. Coulon, P., & Jangoux, M. (1993). Feeding rate and sediment reworking by the holothuroid Holothuria tubulosa (Echinodermata) in a Mediterranean seagrass bed off Ischia Island, Italy. Marine Ecology Progress Series, 92, 201-204. https://doi.org/10.3354/meps092201
• [21]. Cui, F., Xue, C., Li, Z., Zhang, Y., Dong, P., Fu, X., & Gao, X. (2007). Characterization and subunit composition of collagen from the body wall of sea cucumber Stichopus japonicus. Food Chemistry, 100, 1120-1125. https://doi.org/10.1016/j.foodchem.2005.11.019
• [22]. Çakli, S., Cadun, A., Kisla, D., & Dincer, T. (2004). Determination of quality characteristics of Holothuria tubulosa, (Gmelin, 1788) in Turkish sea (Aegean Region) depending on sun drying process step used in Turkey. Journal of Aquatic Food Product Technology, 13, 69-78. https://doi.org/10.1300/J030v13n03_07
• [23]. Dereli, H., Türk Çulha, S. T., Çulha, M., Özalp, B. H., & Tekinay, A. (2016). Reproduction and population structure of the sea cucumber Holothuria tubulosa in the Dardanelles Strait, Turkey. Mediterranean Marine Science, 17, 47-55. https://doi.org/10.12681/mms.1360
• [24]. Despalatović, M., Grubelić, I., šimunović, A., Antolić, B., & Žuljević, A (2004). Reproductive biology of the holothurian Holothuria tubulosa (Echinodermata) in the Adriatic Sea. J. Mar. Biolog. Assoc.UK. 84:409-414. https://doi.org/10.1017/S0025315404009361h.
• [25]. Doyle, G. M., Hamel, J. F., & Mercier, A. (2012). A new quantitative analysis of ovarian development in echinoderms: The maturity stage index. Marine Biology, 159, 455-465. https://doi.org/10.1007/s00227-011-1823-3
• [26]. FAO. (2003). Analytical Methods for Carbohydrates (Chapter 2.3) in Food energy - methods of analysis and conversion factors. FAO Food and Nutrition Paper 77, Report of a Technical Workshop, Rome, Italy.
• [27]. FAO. (2020). Food and Agriculture Organization of the United Nations, Fisheries & Aquaculture Statistics, Global Production Statistics (online query). Retrieved, December 15, 2020, from http://www.fao.org/fishery/statistics/global-production/query/en
• [28]. Ferdouse, F. (1999). Beche-de-mer markets and utilization. Beche-de-mer Information Bulletin, 11, 3-8.
• [29]. Ferdouse, F. (2004). World markets and trade flows of sea cucumber/beche-de-mer. In: A. Lovatelli, C. Conand, S. Purcell, S. Uthicke, J.F. Hamel & A. Mercier (Eds.), Advances in Sea Cucumber Aquaculture and Management (pp. 101-118). Rome, Italy: FAO.
• [30]. Gao, F., Xu, Q., & Yang, H. (2011). Seasonal biochemical changes in composition of body Wall tissues of sea cucumber Apostichopus japonicus. Chinese Journal of Oceanology and Limnology, 29, 252-260. https://doi.org/10.1007/s00343-011-0041-7
• [31]. Gómez-Guillén, M. C., Giménez, B., López-Caballero, M. E., & Montero, M. P. (2011). Functional and bioactive properties of collagen and gelatin from alternative sources: A review. Food Hydrocolloids, 25(8), 1813-1827. https://doi.org/10.1016/j.foodhyd.2011.02.007
• [32]. González-Wangüemert, M., Aydin, M., & Conand, C. (2014). Assessment of sea cucumber populations from the Aegean Sea (Turkey): First insights to sustainable management of new fisheries. Ocean and Coastal Management, 92, 87-94. https://doi.org/10.1016/j.ocecoaman.2014.02.014
• [33]. González-Wangüemert, M., Valente, S., & Aydin, M. (2015). Effects of fishery protection on biometry and genetic structure of two target sea cucumber species from the Mediterranean Sea. Hydrobiologia, 743, 65-74. https://doi.org/10.1007/s10750-014-2006-2
• [34]. González-Wangüemert, M., Valente, S., Henriques, F., Domínguez-Godino, J. A., & Serrão, E. A. (2016). Setting preliminary biometric baselines for new target sea cucumbers species of the NE Atlantic and Mediterranean fisheries. Fisheries Research, 179, 57-66. https://doi.org/10.1016/j.fishres.2016.02.008
• [35]. González-Wangüemert, M., Domínguez-Godino, J. A., & Cánovas, F. (2018). The fast development of sea cucumber fisheries in the Mediterranean and NE Atlantic waters: From a new marine resource to its over-exploitation. Ocean and Coastal Management, 151, 165-177. https://doi.org/10.1016/j.ocecoaman.2017.10.002
• [36]. Günay, D., Emiroğlu, D., Tolon, T., Özden, O., & Saygi, H. (2015). Growth and survival rate of juvenile sea cucumbers (Holothuria tubulosa, Gmelin, 1788) at Various Temperatures. Turkish Journal of Fisheries and Aquatic Sciences, 15, 533-541. https://doi.org/10.4194/1303-2712-v15_2_41
• [37]. Haider, M. S., Sultana, R., Jamil, K., Zehra, L., Tarar, O. M., Shirin, K., & Afzal, W. (2015). A study on proximate composition, amino acid profile, fatty acid profile and some mineral contents in two species of sea cucumber. The Journal of Animal and Plant Sciences, 25, 168-169.
• [38]. Harriott, V. J. (1985). Reproductive biology of three congeneric sea cucumber species, Holothuria atra, Holothuria impatiens and Holothuria edulis, at Heron Reef, Great Barrier Reef. Marine and Freshwater Research, 36, 51-57. https://doi.org/10.1071/MF9850051
• [39]. Jin, H. X., Xu, H. P., Li, Y., Zhang, Q. W., & Xie, H. (2019). Preparation and evaluation of peptides with potential antioxidant activity by microwave assisted enzymatic hydrolysis of collagen from sea cucumber Acaudina molpadioides obtained from Zhejiang province in China. Marine Drugs, 17, 169. https://doi.org/10.3390/md17030169 PMID:30875949
• [40]. Kazanidis, G., Antoniadou, C., Lolas, A.P., Neofitou, N., Vafidis, D., Chintiroglou, C.C. & Neofitou, C. (2010). Population dynamics and reproduction of Holothuria tubulosa (Holothuroidea: Echinodermata) in the Aegean Sea. J. Mar. Biolog. Assoc.UK. 90: 895-901. https://doi.org/10.1017/S0025315410000251
• [41]. Kazanidis, G., Lolas, A., & Vafidis, D. (2014). Reproductive cycle of the traditionally exploited sea cucumber Holothuria tubulosa (Holothuroidea: Aspidochirotida) in Pagasitikos Gulf, western Aegean Sea, Greece. Turkish Journal of Zoology, 38, 306-315. https://doi.org/10.3906/zoo-1302-31
• [42]. Künili, I. E., & Colakoglu, F. A. (2018). Antioxidant and Antimicrobial Activity of Sea Cucumber (Holothuria tubulosa, Gmelin 1791) Extracts. Canakkale Onsekiz Mart University Journal of Marine Sciences and Fisheries, 1(2), 66-71.
• [43]. Künili, I. E., & Colakoglu, F. A. (2019). Chemical and Nutritional Characteristics of Holothuria tubulosa (Gmelin, 1788); A Seasonally Comparative Study. Journal of Aquatic Food Product Technology, 28, 716-728. https://doi.org/10.1080/10498850.2019.1637383
• [44]. Khong, N. M. H., Yusoff, F. M., Jamilah, B., Basri, M., Maznah, I., Chan, K. W., & Nishikawa, J. (2016). Nutritional composition and total collagen content of three commercially important edible jellyfish. Food Chemistry, 196, 953-960. https://doi.org/10.1016/j.foodchem.2015.09.094 PMID:26593577
• [45]. Khotimchenko, Y. S. (2015). The nutritional value of Holothurians. Russian Journal of Marine Biology, 41, 409-423. https://doi.org/10.1134/S1063074015060061
• [46]. Kołodziejska, I., Sikorski, Z. E., & Niecikowska, C. (1999). Parameters affecting the isolation of collagen from squid (Illex argentinus) skins. Food Chemistry, 66(2), 153-157. https://doi.org/10.1016/S0308-8146(98)00251-9
• [47]. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685. https://doi.org/10.1038/227680a0 PMID:5432063
• [48]. Lee, K. J., Park, H. Y., Kim, Y. K., Park, J. I., & Yoon, H. D. (2009). Biochemical Characterization of Collagen from the Starfish Asterias amurensis. Journal of the Korean Society for Applied Biological Chemistry, 52(3), 221-226. https://doi.org/10.3839/jksabc.2009.040
• [49]. Li, P.-H., Lu, W.-C., Chan, Y.-J., Ko, W.-C., Jung, C.-C., Le Huynh, D. T., & Ji, Y.-X. (2020). Extraction and characterization of collagen from sea cucumber (Holothuria cinarascens) and its potential application in moisturizing cosmetics. Aquaculture (Amsterdam, Netherlands), 515, 734590. https://doi.org/10.1016/j.aquaculture.2019.734590
• [50]. Lin, S., Xue, Y. P., San, E., Keong, T. C., Chen, L., & Zheng, Y. G. (2017). Extraction and Characterization of Pepsin Soluble Collagen from the Body Wall of Sea Cucumber Acaudina leucopocta. Journal of Aquatic Food Product Technology, 26, 502-515. https://doi.org/10.1080/10498850.2016.1222560
• [51]. Liu, Z., Oliveira, A. C., & Su, Y. C. (2010). Purification and characterization of pepsin-solubilized collagen from skin and connective tissue of giant red sea cucumber (Parastichopus californicus). Journal of Agricultural and Food Chemistry, 58, 1270-1274. https://doi.org/10.1021/jf9032415 PMID:20085374
• [52]. Liu, Z., Su, Y., & Zeng, M. (2011). Amino Acid Composition and Functional Properties of Giant Red Sea Cucumber (Parastichopus californicus) Collagen Hydrolysates. Journal of Ocean University of China, 10, 80-84. https://doi.org/10.1007/s11802-011-1787-4
• [53]. Liu, Y. X., Liu, Z. Q., Song, L., Ma, Q. R., Zhou, D. Y., Zhu, B. W., & Shahidi, F. (2019). Effects of collagenase type I on the structural features of collagen fibres from sea cucumber (Stichopus japonicus) body wall. Food Chemistry, 301, 125302. https://doi.org/10.1016/j.foodchem.2019.125302 PMID:31387034
• [54]. Mercier, A., & Hamel, J. F. (2009). Endogenous and exogenous control of gametogenesis and spawning in echinoderms. Advances in Marine Biology, 55, xi-xii, 1-291. https://doi.org/10.1016/S0065-2881(09)55008-0 PMID:19595321
• [55]. Mezali, K., Zupo, V., & Francour, P. (2006). Population dynamics of Holothuria (Holothuria) tubulosa and Holothuria (Lessonothuria) polii of an Algerian Posidonia oceanica meadow. Biologia Marina Mediterranea, 13, 158-161.
• [56]. Mezali, K., & Thandar, A. S. (2014). First record of Holothuria (Roweothuria) arguinensis (Echinodermata: Holothuroidea: Aspidochirotida: Holothuriidae) from the Algerian coastal waters. Marine Biodiversity Records, 7, E40(1-4). https://doi.org/10.1017/S1755267214000438
• [57]. Miller, A. T., Karmas, E., & Lu, M. F. (1983). Age-related-changes in the collagen of bovine corium studies on extractability, solubility and molecular-size distribution. Journal of Food Science, 48, 681-685. https://doi.org/10.1111/j.1365-2621.1983.tb14875.x
• [58]. Muthiga, N. A. (2006). The reproductive biology of a new species of sea cucumber, Holothuria (Mertensiothuria) arenacava in a Kenyan marine protected area: The possible role of light and temperature on gametogenesis and spawning. Marine Biology, 149, 585-593. https://doi.org/10.1007/s00227-005-0224-x
• [59]. Nagai, T., & Suzuki, N. (2000). Partial characterization of collagen from purple sea urchin (Anthocidaris crassispina) test. International Journal of Food Science & Technology, 35, 497-501. https://doi.org/10.1046/j.1365-2621.2000.00406.x
• [60]. Nielsen, P. M., Petersen, D., & Dambmann, C. (2001). Improved Method for Determining Food Protein Degree of Hydrolysis. Journal of Food Science, 66, 642-646. https://doi.org/10.1111/j.1365-2621.2001.tb04614.x
• [61]. Olive, P. J. W. (1995). Annual breeding cycles in marine invertebrates and environmental temperature: Probing the proximate and ultimate causes of reproductive synchrony. Journal of Thermal Biology, 20, 79-90. https://doi.org/10.1016/0306-4565(94)00030-M
• [62]. Nahla, E. S. E. S. O. (2013). Nutritional value of some Egyptian sea cucumbers. African Journal of Biotechnology, 12, 5466-5472. https://doi.org/10.5897/AJB2013.13020
• [63]. Park, S. Y., Lim, H. K., Lee, S., Hwang, H. C., Cho, S. K., & Cho, M. (2012). Pepsin-solubilised collagen (PSC) from Red Sea cucumber (Stichopus japonicus) regulates cell cycle and the fibronectin synthesis in HaCaT cell migration. Food Chemistry, 132, 487-492. https://doi.org/10.1016/j.foodchem.2011.11.032 PMID:26434320
• [64]. Pereira, D. M., Andrade, P. B., Pires, R. A., & Reis, L. E. (2014). Chemical ecology of echinoderms: impact of environment and diet in metabolomic profile. In E. Whitmore (Ed.), Echinoderms (pp. 57-76). Nova Publishers.
• [65]. Purcell, S. W. (2010). Managing sea cucumber fisheries with an ecosystem approach. A. Lovatelli, M. Vasconcellos, & Y. Yimin (Eds), FAO Fisheries and Aquaculture Technical Paper No: 520. Rome: FAO.
• [66]. Purcell, S. W. (2014). Value, market preferences and trade of Beche-de-mer from Pacific Island sea cucumbers. PLoS One, 9(4), e95075. https://doi.org/10.1371/journal.pone.0095075 PMID:24736374
• [67]. Purcell, S. W., Mercier, A., Conand, C., Hamel, J. F., Toral-Granda, M. V., Lovatelli, A., & Uthicke, S. (2013). Sea cucumber fisheries: Global analysis of stocks, management measures and drivers of overfishing. Fish and Fisheries, 14, 34-59. https://doi.org/10.1111/j.1467-2979.2011.00443.x
• [68]. Qi, H., Li, N., Zhao, X., Xu, Z., & Qi, L. (2017). Physicochemical Properties and Radical Scavenging Capacities of Pepsin-Solubilized Collagen from the Body Wall of Starfish (Asterina pectinifera). Journal of Aquatic Food Product Technology, 26(4), 376-389. https://doi.org/10.1080/10498850.2016.1186768
• [69]. Ramón, M., Lleonart, J., & Massutí, E. (2010). Royal cucumber (Stichopus regalis) in the north western Mediterranean: Distribution pattern and fishery. Fisheries Research, 105, 21-27. https://doi.org/10.1016/j.fishres.2010.02.006
• [70]. Regenstein, J. M., & Zhou, P. (2007). Collagen and gelatin from marine by-products. In F. Shahidi (Ed.), Maximising the Value of Marine By-Products (pp. 279-303). Woodhead Publishing. https://doi.org/10.1533/9781845692087.2.279
• [71]. Roggatz, C. C., González-Wangüemert, M., Pereira, H., Rodrigues, M. J., da Silva, M. M., Barreira, L., Varela, J., & Custódio, L. (2016). First report of the nutritional profile and antioxidant potential of Holothuria arguinensis, a new resource for aquaculture in Europe. Natural Product Research, 30, 2034-2040. https://doi.org/10.1080/14786419.2015.1107555 PMID:26551335
• [72]. Santos, R., Haesaerts, D., Jangoux, M., & Flammang, P. (2005). The tube feet of sea urchins and sea stars contain functionally different mutable collagenous tissues. The Journal of Experimental Biology, 208, 2277-2288. https://doi.org/10.1242/jeb.01641 PMID:15939770
• [73]. Saito, M., Kunisaki, N., Urano, N., & Kimura, S. (2002). Collagen as the major edible component of sea cucumber (Stichopus japonicus). Journal of Food Science, 67, 1319-1322. https://doi.org/10.1111/j.1365-2621.2002.tb10281.x
• [74]. Senadheera, T. R. L., Dave, D., & Shahidi, F. (2020). Sea Cucumber Derived Type I Collagen: A Comprehensive Review. Marine Drugs, 18, 471. https://doi.org/10.3390/md18090471 PMID:32961970
• [75]. Shi, S., Feng, W., Hu, S., Liang, S., An, N., & Mao, Y. (2016). Bioactive compounds of sea cucumbers and their therapeutic effects. Chinese Journal of Oceanology and Limnology, 34, 549-558. https://doi.org/10.1007/s00343-016-4334-8
• [76]. Sicuro, B., & Levine, J. (2011). Sea Cucumber in the Mediterranean: A Potential Species for Aquaculture in the Mediterranean. Reviews in Fisheries Science, 19, 299-304. https://doi.org/10.1080/10641262.2011.598249
• [77]. Sicuro, B., Piccinno, M., Gai, F., Abete, M. C., Danieli, A., Dapra, F., Mioletti, S., & Vilella, S. (2012). Food quality and safety of Mediterranean sea cucumbers Holothuria tubulosa and Holothuria polii in Southern Adriatic Sea. Asian Journal of Animal and Veterinary Advances, 7, 851-859. https://doi.org/10.3923/ajava.2012.851.859
• [78]. Silva, T. H., Moreira-Silva, J., Marques, A. L. P., Domingues, A., Bayon, Y., & Reis, R. L. (2014). Marine origin collagens and its potential applications. Marine Drugs, 12, 5881-5901. https://doi.org/10.3390/md12125881 PMID:25490254
• [79]. Singh, R., MacDonald, B. A., Lawton, P., & Thomas, M. L. H. (2001). The reproductive biology of the dendrochirote sea cucumber Cucumaria frondosa (Echinodermata: Holothuroidea) using new quantitative methods. Invertebrate Reproduction & Development, 40, 125-141. https://doi.org/10.1080/07924259.2001.9652713
• [80]. Tamacha, F. S., Soualili, D. L., & Mezali, K. (2019). Reproductive biology of Holothuria (Roweothuria) poli (Holothuroidea: Echinodermata) from Oran Bay, Algeria. SPC Beche-de-mer Information Bulletin, 39, 47-53.
• [81]. Tolon, T. M., & Engin, S. (2019). Gonadal development of the holothurian Holothuria polii (Delle Chiaje, 1823) in spawning period at the Aegean Sea (Mediterranean Sea). Su Ürünleri Dergisi, 36(4), 379-385. https://doi.org/10.12714/egejfas.36.4.09
• [82]. TSMS. (2020). Turkish State Meteorological Service, Seawater Temperature Statistics of the Marmara Sea (1970-2020). Retrieved February 10, 2021, from https://www.mgm.gov.tr/veridegerlendirme/il-ve-ilceler-istatistik.aspx?k=K
• [83]. Wang, W., Wu, Z., Dai, Z., Yang, Y., Wang, J., & Wu, G. (2013). Glycine metabolism in animals and humans: Implications for nutrition and health. Amino Acids, 45, 463-477. https://doi.org/10.1007/s00726-013-1493-1 PMID:23615880
• [84]. Widianingsih, Z., Zaenuri, M., Anggoro, S., & Kusumaningrum, H. P. S. (2016). Nutritional value of sea cucumber [Paracaudina australis (Semper, 1868)]. Aquatic Procedia, 7, 271-276. https://doi.org/10.1016/j.aqpro.2016.07.038
• [85]. Wilkie, I. (2005). Mutable Collagenous Tissue: Overview and Biotechnological Perspective. In V. Matranga (Ed.), Echinodermata (pp. 221-250). Springer. https://doi.org/10.1007/3-540-27683-1_10
• [86]. Valente, S., Serrão, E. A., & González-Wangüemert, M. (2015). West versus East Mediterranean Sea: Origin and genetic differentiation of the sea cucumber Holothuria polii. Marine Ecology (Berlin), 36, 485-495. https://doi.org/10.1111/maec.12156
• [87]. Zar, J. H. (1996). Biostatistical Analysis. Prentice Hall.
• [88]. Zhang, X., Liu, Y., Li, Y., & Zhao, X. (2017). Identification of the geographical origins of sea cucumber (Apostichopus japonicus) in northern China by using stable isotope ratios and fatty acid profiles. Food Chemistry, 218, 269-276. https://doi.org/10.1016/j.foodchem.2016.08.083 PMID:27719909
• [89]. Zhong, Y., Khan, M. A., & Shahidi, F. (2007). Compositional characteristics and antioxidant properties of fresh and processed sea cucumber (Cucumaria frondosa). Journal of Agricultural and Food Chemistry, 55, 1188-1192. https://doi.org/10.1021/jf063085h PMID:17243707
• [90]. Zhong, M., Chen, T., Hu, C., & Ren, C. (2015). Isolation and characterization of collagen from the body wall of sea cucumber Stichopus monotuberculatus. Journal of Food Science, 80, C671-C679. https://doi.org/10.1111/1750-3841.12826 PMID:25810305
• [91]. Zhou, X. Q., Wang, C. H., & Jiang, A. L. (2012). In vitro antitumor activities of low molecular sea cucumber Stichopus japonicus peptides sequentially hydrolyzed by proteases. Advanced Materials Research, 393-395, 1259-1262.
• [92]. Zhu, B. W., Dong, X. P., Zhou, D. Y., Gao, Y., Yang, J. F., Li, D. M., Zhao, X. K., Ren, T. T., Ye, W. X., Tan, H., Wu, H. T., & Yu, C. (2012). Physicochemical properties and radical scavenging capacities of pepsin-solubilized collagen from sea cucumber Stichopus japonicus. Food Hydrocolloids, 28, 182-188. https://doi.org/10.1016/j.foodhyd.2011.12.010

Uwagi

Opracowanie rekordu ze środków MEiN, umowa nr SONP/SP/546092/2022 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2022-2023).

Identyfikatory

DOI

10.26881/oahs-2022.1.09