Sains Malaysiana 51(11)(2022): 3523-3537

http://doi.org/10.17576/jsm-2022-5111-02

 

Rate and Efficiency of Organic Carbon Assimilation by Aquacultured Juvenile Sandfish Holothuria scabra

(Kadar dan Kecekapan Asimilasi Karbon Organik oleh Ikan Pasir Juvenil Holothuria scabra Akuakultur)

 

A’AN JOHAN WAHYUDI1,*, LISA FAJAR INDRIANA2, MUHAMMAD FIRDAUS2, HANIF BUDI PRAYITNO1 & HANNY MEIRINAWATI1

 

1Research Center for Oceanography, National Research and Innovation Agency, Pasir Putih 1, Ancol Timur, Jakarta 14430 Indonesia

2Research Center for Marine and Terrestrial Bio Industry, National Research and Innovation Agency, Teluk Kodek, Pemenang, Lombok Utara 83352 Indonesia

 

Diserahkan: 9 Februari 2022/Diterima: 28 Jun 2022

 

Abstract

Diet assimilation rate is crucial to the growth and survival of Holothuria scabra juveniles during culture. To understand the assimilation rate and efficiency we assess organic carbon assimilation, which is closely related to the growth and source of variations in diet. We conducted a two-factor experiment, i.e., juvenile origin (cultured and wild H. scabra juveniles), and diet treatment (one control with no additional diet, and three additional diets, i.e., rice bran, dried cow manure, and seagrass Enhalus acoroides extract). We monitored the amounts of each diet that the juveniles consumed and the fecal pellets they egested. The diet, sediment, body walls, and organic carbon content of the fecal pellets were measured using an elemental analyzer combined with an isotope ratio mass spectrometer. Exponential growth was seen in the juveniles fed with rice bran, which had a fecal pellet egestion of 0.12–0.21 gC/d. Stable isotope analysis showed that the contribution of the diet proportion to the growth of the sandfish did not exceed 30%. The range of the assimilation rate was 35.3–62.4 gC/d. The average assimilation efficiency of organic carbon was 43.6 ± 27.7% (max 57.9%). Considering the assimilation rate and efficiency, we suggest a feeding interval of once every two days or twice per week at a rate of 3–5% of the total H. scabra biomass for a juvenile culture system.

 

Keywords: Assimilation; growth rate; Holothuria scabra; organic carbon; rearing culture sandfish

 

Abstrak

Kadar asimilasi diet adalah penting untuk pertumbuhan dan kemandirian juvenil Holothuria scabra semasa pengkulturan. Untuk memahami kadar asimilasi dan kecekapan, kami menilai asimilasi karbon organik, yang berkait rapat dengan pertumbuhan dan punca variasi dalam diet. Kami menjalankan uji kaji dua faktor, iaitu, asal juvenil (juvenil H. scabra yang dikultur dan liar) dan rawatan diet (satu kawalan tanpa diet tambahan dan tiga diet tambahan; dedak padi, baja tahi lembu dan ekstrak rumput laut Enhalus acoroides). Kami memantau jumlah setiap diet yang diambil oleh juvenil dan pelet najis yang dikeluarkan. Diet, sedimen, dinding badan serta kandungan karbon organik pelet najis diukur menggunakan penganalisis unsur yang digabungkan dengan spektrometer jisim nisbah isotop. Pertumbuhan eksponen dilihat pada juvenil yang diberi makan dedak padi, yang mempunyai penghadaman pelet najis 0.12–0.21 gC/d. Analisis isotop stabil menunjukkan bahawa sumbangan perkadaran diet kepada pertumbuhan ikan pasir tidak melebihi 30%. Julat kadar asimilasi ialah 35.3–62.4 gC/d. Purata kecekapan asimilasi karbon organik ialah 43.6 ± 27.7% (maks 57.9%). Memandangkan kadar asimilasi dan kecekapan, kami mencadangkan sela pemakanan sekali setiap dua hari atau dua kali seminggu pada kadar 3-5% daripada jumlah biojisim H. scabra untuk sistem kultur juvenil.

 

Kata kunci: Asimilasi; Holothuria scabra; kadar pertumbuhan; karbon organik; ternakan ikan pasir

 

RUJUKAN

Ahmed, H., Shakeel, H., Naeem, S. & Sano, K. 2018. Pilot study on grow-out culture of sandfish (Holothuria scabra) in bottom-set sea cages in lagoon. SPC Beche-de-mer Information Bulletin 38: 45-50.

Altamirano, J.P., Recente, C.P. & Rodriguez, J.C. 2017. Substrate preference for burying and feeding of sandfish Holothuria scabra juveniles. Fisheries Research 186: 514-523. https://doi.org/10.1016/j.fishres.2016.08.011

Battaglene, S.C., Seymour, J.E. & Ramofafia, C. 1999. Survival and growth of cultured juvenile sea cucumbers, Holothuria scabra. Aquaculture 178(3-4): 293-322. https://doi.org/10.1016/S0044-8486(99)00130-1

Bordbar, S., Anwar, F. & Saari, N. 2011. High-value components and bioactives from sea cucumbers for functional foods - A review. Marine Drugs 9(10): 1761-1805. https://doi.org/10.3390/md9101761

Bowman, W. 2012. Sandfish production and development of sea ranching in Northern Australia. In Asia-Pacific Tropical Sea Cucumber Aquaculture, edited by Hair, C., Pickering, T. & Mills, D. Proceedings of an International Symposium, Noumea, New Caledonia, 15-17 February, 2011. Australian Centre for International Agricultural Research, Canberra. pp. 75-78. 

Capone, D.G., Bronk, D.A., Mulholland, M.R. & Carpenter, E.J. 2008. Nitrogen in the marine environment. In Nitrogen in the Marine Environment, 2nd ed., edited by Capone, D.G., Bronk, D.A., Mulholland, M.R. & Carpenter, E.J. Elsevier. https://doi.org/10.1016/B978-0-12-372522-6.X0001-1

Ceccarelli, D.M., Logan, M. & Purcell, S.W. 2018. Analysis of optimal habitat for captive release of the sea cucumber Holothuria scabra. Marine Ecology Progress Series 588: 85-100. https://doi.org/10.3354/meps12444

Chen, J., Ren, Y., Wang, G., Xia, B. & Li, Y. 2018. Dietary supplementation of biofloc influences growth performance, physiological stress, antioxidant status and immune response of juvenile sea cucumber Apostichopus japonicus (Selenka). Fish & Shellfish Immunology 72: 143-152. https://doi.org/10.1016/j.fsi.2017.10.061

Domínguez-Godino, J.A. & González-Wangüemert, M. 2019. Assessment of Holothuria arguinensis feeding rate, growth and absorption efficiency under aquaculture conditions. New Zealand Journal of Marine and Freshwater Research 53(1): 60-76. https://doi.org/10.1080/00288330.2018.1480499

Domínguez-Godino, J.A., Slater, M.J., Hannon, C. & González-Wangüermert, M. 2015. A new species for sea cucumber ranching and aquaculture: Breeding and rearing of Holothuria arguinensis. Aquaculture 438: 122-128. https://doi.org/10.1016/j.aquaculture.2015.01.004

Drazen, J.C., Reisenbichler, K.R. & Robison, B.H. 2007. A comparison of absorption and assimilation efficiencies between four species of shallow- and deep-living fishes. Marine Biology 151(4): 1551-1558. https://doi.org/10.1007/s00227-006-0596-6

Duarte, C. 1990. Seagrass nutrient content. Marine Ecology Progress Series 67: 201-207. https://doi.org/10.3354/meps067201

Duy, N.D. 2012. Large-scale sandfish production from pond culture in Vietnam. In Asia-Pacific Tropical Sea Cucumber Aquaculture, edited by Hair, C., Pickering, T. & Mills, D. Proceedings of an International Symposium, Noumea, New Caledonia, 15-17 February, 2011. Australian Centre for International Agricultural Research, Canberra. pp. 34-39.

Duy, N.D.Q., Francis, D.S. & Southgate, P.C. 2017. The nutritional value of live and concentrated micro-algae for early juveniles of sandfish, Holothuria scabra. Aquaculture 473: 97-104. https://doi.org/10.1016/j.aquaculture.2017.01.028

Eeckhaut, I., Lavitra, T., Rasoforinina, R., Rabenevanana, M.W., Gildas, P. & Jangoux, M. 2008. Madagascar Holothurie SA: The first trade company based on sea cucumber aquaculture in Madagascar. SPC Beche-de-mer Information Bulletin 28: 22-23.

Fry, B. & Sherr, E.B. 1989. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. In Stable Isotopes in Ecological Research. Ecological Studies, vol. 68, edited by Rundel, P.W., Ehleringer, J.R. & Nagy, K.A. New York: Springer-Verlag. 

Gao, Q.F., Wang, Y., Dong, S., Sun, Z. & Wang, F. 2011. Absorption of different food sources by sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea): Evidence from carbon stable isotope. Aquaculture 319(1-2): 272-276. https://doi.org/10.1016/j.aquaculture.2011.06.051

Hair, C., Pickering, T., Meo, S., Vereivalu, T., Hunter, J. & Cavakiqali, L. 2011. Sandfish culture in Fiji Islands. SPC Beche-de-mer Information Bulletin 31: 3-11.

Hair, C., Mills, D.J., McIntyre, R. & Southgate, P.C. 2016. Optimising methods for community-based sea cucumber ranching: Experimental releases of cultured juvenile Holothuria scabra into seagrass meadows in Papua New Guinea. Aquaculture Reports 3: 198-208. https://doi.org/10.1016/j.aqrep.2016.03.004

Indriana, L., Wahyudi, A. & Kunzmann, A. 2018. Assimilation dynamics of different diet sources by the sea cucumber Holothuria scabra, with evidence from stable isotope signature. Annual Research & Review in Biology 28(2): 1-10. https://doi.org/10.9734/ARRB/2018/42591

Indriana, L.F., Firdaus, M., Supono, S. & Munandar, H. 2017. Survival rate and growth of juvenile sandfish (Holothuria scabra) in various rearing conditions. Marine Research in Indonesia 42(1): 11. https://doi.org/10.14203/mri.v41i2.156

Juinio-Meñez, M.A., Tech, E.D., Ticao, I.P., Gorospe, J.R., Edullantes, C.M.A. & Rioja, R.A.V. 2017. Adaptive and integrated culture production systems for the tropical sea cucumber Holothuria scabra. Fisheries Research 186: 502-513. https://doi.org/10.1016/j.fishres.2016.07.017

Lavitra, T., Rasolofonirina, R. & Eeckhaut, I. 2010. The effect of sediment quality and stocking density on survival and growth of the sea cucumber Holothuria scabra reared in nursery ponds and sea pens. West Indian Ocean Journal Marine Science 9: 153-164. 

Liu, Y., Dong, S., Tian, X., Wang, F. & Gao, Q. 2010. The effect of different macroalgae on the growth of sea cucumbers (Apostichopus japonicus Selenka). Aquaculture Research 41(11): e881-e885. https://doi.org/10.1111/j.1365-2109.2010.02582.x

Mathieu-Resuge, M., Le Grand, F., Schaal, G., Kraffe, E., Lorrain, A., Letourneur, Y., Lemonnier, H., Benoît, J. & Hochard, S. 2020. Assimilation of shrimp farm sediment by Holothuria scabra: A coupled fatty acid and stable isotope approach. Aquatic Living Resources 33: 3.

Meirinawati, H., Prayitno, H.B., Indriana, L.F., Firdaus, M. & Wahyudi, A.J. 2020. Water quality assessment and monitoring of closed rearing system of the sea cucumber Holothuria scabra. ASEAN Journal on Science and Technology for Development 37(2): 73-80. https://doi.org/10.29037/AJSTD.624

Mercier, A., Battaglene, S.C. & Hamel, J.F. 1999. Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. Journal of Experimental Marine Biology and Ecology 239(1): 125-156. https://doi.org/10.1016/S0022-0981(99)00034-9

Mills, D., Duy, N.D., Juinio-Me˜nez, M.A., Raison, C. & Zarate, J. 2012. Overview of sea cucumber aquaculture and sea ranching research in the South-East Asian region. In Asia-Pacific Tropical Sea Cucumber Aquaculture, edited by Hair, C., Pickering, T. & Mills, D. Proceeding of an International Symposium, Noumea, New Caledonia, 15-17 February 2011. Australian Centre for International Agricultural Research, Canberra. pp. 22-31.

Mohammadizadeh, F., Ehsanpor, M., Afkhami, M., Mokhlesi, A., Khazaali, A. & Montazeri, S. 2013. Evaluation of antibacterial, antifungal, and cytotoxic effects of Holothuria scabra from the North Coast of the Persian Gulf. Journal de Mycologie Médicale 23(4): 225-229. https://doi.org/10.1016/j.mycmed.2013.08.002

Namukose, M., Msuya, F., Ferse, S., Slater, M. & Kunzmann, A. 2016. Growth performance of the sea cucumber Holothuria scabra and the seaweed Eucheuma denticulatum: Integrated mariculture and effects on sediment organic characteristics. Aquaculture Environment Interactions 8: 179-189. https://doi.org/10.3354/aei00172

Nelson, E.J., MacDonald, B.A. & Robinson, S.M.C. 2012. The absorption efficiency of the suspension-feeding sea cucumber, Cucumaria frondosa, and its potential as an extractive integrated multi-trophic aquaculture (IMTA) species. Aquaculture 370-371: 19-25. https://doi.org/10.1016/j.aquaculture.2012.09.029

Olavides, R.D., Rodriguez, B.D. & Juinio-Me˜nez, M.A. 2011. Simultaneous mass spawning of Holothuria scabra in sea ranching sites in Bolinao and Andamunicipalities, Philippines. SPC Beche-de-mer Information Bulletin 31: 23-24.

Panigrahi, A., Sundaram, M., Chakrapani, S., Rajasekar, S., Syama Dayal, J. & Chavali, G. 2019. Effect of carbon and nitrogen ratio (C:N) manipulation on the production performance and immunity of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) in a biofloc‐based rearing system. Aquaculture Research 50(1): 29-41. https://doi.org/10.1111/are.13857

Peterson, B.J., Howarth, R.W. & Garritt, R.H. 1985. Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227(4692): 1361-1363. https://doi.org/10.1126/science.227.4692.1361

Piola, R.F., Moore, S.K. & Suthers, I.M. 2006. Carbon and nitrogen stable isotope analysis of three types of oyster tissue in an impacted estuary. Estuarine, Coastal and Shelf Science 66(1-2): 255-266. https://doi.org/10.1016/j.ecss.2005.08.013

Post, D.M. 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 3: 703-718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2

Purcell, S.W. 2004. Criteria for release strategies and evaluating the restocking of sea cucumbers. In Advances in Sea Cucumber Aquaculture and Management, FAO Fisheries Technical Paper No. 463, edited by Lovatelli, A., Conand, C., Purcell, S., Uthicke, S., Hamel, J-F. & Mercier, A. Rome: FAO. pp. 181-191.

Purcell, S.W. & Simutoga, M. 2008. Spatio-temporal and size-dependent variation in the success of releasing cultured sea cucumbers in the wild. Reviews in Fisheries Science 16(1-3): 204-214. https://doi.org/10.1080/10641260701686895

Purcell, S.W., Williamson, D.H. & Ngaluafe, P. 2018. Chinese market prices of beche-de-mer: Implications for fisheries and aquaculture. Marine Policy 91: 58-65. https://doi.org/10.1016/j.marpol.2018.02.005

Purcell, S.W., Hair, C.A. & Mills, D.J. 2012. Sea cucumber culture, farming, and sea ranching in the tropics: Progress, problems, and opportunities. Aquaculture 368-369: 68-81. https://doi.org/10.1016/j.aquaculture.2012.08.053

Robinson, G. & Pascal, B. 2012. Sea cucumber farming experiences in south-west Madagascar. In Asia-Pacific Tropical Sea Cucumber Aquaculture, edited by Hair, C.A., Pickering, T.D. & Mills, D.J. Australian Centre for International Agricultural Research, Canberra. pp. 142-155.

Robinson, G., Slater, M.J., Jones, C.L.W. & Stead, S.M. 2013. Role of sand as substrate and dietary component for juvenile sea cucumber Holothuria scabra. Aquaculture 392-395: 23-25. https://doi.org/10.1016/j.aquaculture.2013.01.036

Sembiring, S.B.M., Wardana, I.K., Giri, N.A. & Haryanti, H. 2017. Keragaan rematurasi gonad induk teripang pasir, Holothuria scabra dengan pemberian jenis pakan berbeda. Jurnal Riset Akuakultur 12(2): 147-159. https://doi.org/10.15578/jra.12.2.2017.147-159

Skewes, T., Dennis, D., Donovan, A. & Ellis, N. 2004. Conversion Ratios for Commercial beche-de-mer Species in Torres Strait. Australian Fisheries Management Authority Torres Strait Research Program Final Report. In Project Number: R02/1195.

Shi, C., Dong, S., Wang, F., Gao, Q. & Tian, X. 2015. Effects of the sizes of mud or sand particles in feed on growth and energy budgets of young sea cucumber (Apostichopus japonicus). Aquaculture 440: 6-11. https://doi.org/10.1016/j.aquaculture.2015.01.028

Sinsona, M.J. & Juinio-Meñez, M.A. 2018. Effects of sediment enrichment with macroalgae, Sargassum spp., on the behavior, growth, and survival of juvenile sandfish, Holothuria scabra. Aquaculture Reports 12: 56-63. https://doi.org/10.1016/j.aqrep.2018.09.002

Song, X., Xu, Q., Zhou, Y., Lin, C. & Yang, H. 2017. Growth, feed utilization, and energy budgets of the sea cucumber Apostichopus japonicus with different diets containing the green tide macroalgae Chaetomorpha linum and the seagrass Zostera marina. Aquaculture 470: 157-163. https://doi.org/10.1016/j.aquaculture.2016.12.035

Sroyraya, M., Hanna, P.J., Siangcham, T., Tinikul, R., Jattujan, P., Poomtong, T. & Sobhon, P. 2017. Nutritional components of the sea cucumber Holothuria scabra. Functional Foods in Health and Disease 7(3): 168. https://doi.org/10.31989/ffhd.v7i3.303

Stock, B.C. & Semmens, B.X. 2016. MixSIAR GUI User Manual. Version 3.1. https://doi.org/10.5281/zenodo.47719

Sun, Z., Gao, Q., Dong, S., Shin, P. & Wang, F. 2012. Estimates of carbon turnover rates in the sea cucumber Apostichopus japonicus (Selenka) using stable isotope analysis: The role of metabolism and growth. Marine Ecology Progress Series 457: 101-112. https://doi.org/10.3354/meps09760

Taylor, A.L., Nowland, S.J., Hearnden, M.N., Hair, C.A. & Fleming, A.E. 2016. Sea ranching release techniques for cultured sea cucumber Holothuria scabra (Echinodermata: Holothuroidea) juveniles within the high-energy marine environments of northern Australia. Aquaculture 465: 109-116. https://doi.org/10.1016/j.aquaculture.2016.08.031

Wang, X., Lu, X., Li, F. & Yang, G. 2014. Effects of temperature and carbon-nitrogen (C/N) ratio on the performance of anaerobic co-digestion of dairy manure, chicken manure and rice straw: Focusing on ammonia inhibition. PLoS ONE 9(5): e97265. https://doi.org/10.1371/journal.pone.0097265

Wahyudi, A.J. & Afdal. 2019. The origin of the suspended particulate matter in the seagrass meadow of tropical waters, an evidence of the stable isotope signatures. Acta Oceanologica Sinica38: 136-143. https://doi.org/10.1007/s13131-019-1380-z

Wahyudi, A.J., Afdal, A. & Meirinawati, H. 2019. Stable carbon isotope signature of particulate organic matter in the Southwestern Sumatran Waters of the Eastern Indian Ocean. ASEAN Journal on Science and Technology for Development 36(2): 35-43. https://doi.org/10.29037/ajstd.555

Wahyudi, A.J., Meirinawati, H., Prayitno, H.B., Suratno, Surinati, D. & Hernawan, U.E. 2019. The material origin of the particulate organic matter (POM) in the Eastern Indonesian waters. AIP Conference Proceedings. 2175(1): 020047. https://doi.org/10.1063/1.5134611

Wahyudi, A.J., Wada, S., Aoki, M. & Hama, T. 2013. Stable isotope signature and pigment biomarker evidence of the diet sources of Gaetice depressus (Crustacea: Eubrachyura: Varunidae) in a boulder shore ecosystem. Plankton and Benthos Research 8(2): 55-67. https://doi.org/10.3800/pbr.8.55

Watanabe, S., Sumbing, J.G. & Lebata-Ramos, M.J.H. 2014. Growth pattern of the tropical sea cucumber, Holothuria scabra, under captivity. Japan Agricultural Research Quarterly 48(4): 457-464. https://doi.org/10.6090/JARQ.48.457

Xu, Q., Zhang, L., Zhang, T., Zhang, X. & Yang, H. 2017. Functional groupings and food web of an artificial reef used for sea cucumber aquaculture in northern China. Journal of Sea Research 119: 1-7. https://doi.org/10.1016/j.seares.2016.10.005

Yokoyama, H. 2013. Growth and food source of the sea cucumber Apostichopus japonicus cultured below fish cages - Potential for integrated multi-trophic aquaculture. Aquaculture 372-375: 28-38. https://doi.org/10.1016/j.aquaculture.2012.10.022

Yu, Z., Zhou, Y., Yang, H., Ma, Y. & Hu, C. 2014. Survival, growth, food availability and assimilation efficiency of the sea cucumber Apostichopus japonicus bottom-cultured under a fish farm in southern China. Aquaculture 426-427: 238-248. https://doi.org/10.1016/j.aquaculture.2014.02.013

 

*Pengarang untuk surat-menyurat; email: aanj001@brin.go.id

 

 

 

   

sebelumnya