Ice-Ice Disease in Commercially Cultivated Seaweeds Kappaphycus spp. and Eucheuma spp.: A Review on the Causes, Occurrence, and Control Measures

Year 2021, Volume: 10 Issue: 3, 234 - 243, 22.09.2021

Albaris Tahiluddin , Ertuğrul Terzi

https://doi.org/10.33714/masteb.917788

Cited By: 15

Abstract

Kappaphycus spp. and Eucheuma spp. are two economically significant seaweed species cultivated globally due to their carrageenan content with numerous commercial applications. They are mainly cultivated in the Philippines, Indonesia, Malaysia, and Tanzania. The culture of these seaweeds also provides income sources for many coastal dwellers. In 2018, the total global production from these seaweeds was about 11 million tonnes. One of the primary problems that affect seaweed production is the incidence of ice-ice disease. In this article, we reviewed the reported scientific journals on the ice-ice disease of two commercially cultured seaweed species (Kappaphycus spp. and Eucheuma spp.), focusing mainly on causes, occurrence, and control measures. The ice-ice disease is caused by both abiotic and biotic factors manifested by the presence of white and soft parts in the infected seaweeds. The occurrence of this disease varies from species, places, and seasons. Control measures may include proper farm management, polyculture with other seaweeds, pre-soaking with antibacterial substances and nutrient enrichment before out-planting, and possibly using genetic engineering.

Keywords

Eucheuma, Ice-ice disease, Kappaphycus, Seaweed farming

References

• Achmad, M., Alimuddin, A., Widyastuti, U., Sukenda, S., Suryanti, E., & Harris, E. (2016). Molecular identification of new bacterial causative agent of ice-ice disease on seaweed Kappaphycus alvarezii. PeerJ Preprints. https://doi.org/10.7287/peerj.preprints.2016v1
• Ali, M. K. M., Critchley, A. T., & Hurtado, A. Q. (2020). The impacts of AMPEP K+(Ascophyllum marine plant extract, enhanced with potassium) on the growth rate, carrageenan quality, and percentage incidence of the damaging epiphyte Neosiphonia apiculata on four strains of the commercially important carrageenophyte Kappaphycus, as developed by micropropagation techniques. Journal of Applied Phycology, 32(3), 1907-1916. https://doi.org/10.1007/s10811-020-02117-0
• Alibon, R. D., Gonzales, J. M. P., Ordoyo, A. E. T., & Echem, R. T. (2019). Incidence of ice-ice disease associated with Kappaphycus alvarezii in the seaweed farms in Zamboanga Peninsula, Mindanao, Philippines. SSR Institute of International Journal of Life Sciences, 5(1), 2148-2155. https://doi.org/10.21276/SSR-IIJLS.2019.5.1.6
• Arasamuthu, A., & Edward, J. K. P. (2018). Occurrence of ice-ice disease in seaweed Kappaphycus alvarezii at Gulf of Mannar and Palk Bay, Southeastern India. Indian Journal of Geo-Marine Sciences, 47(6), 1208-1216.
• Aris, M. (2011). Identifikasi, patogenisitas bakteri dan pemanfaatan gen 16s-rrna untuk deteksi penyakit ice-ice pada budidaya rumput laut (Kappaphycus alvarezii) [Identification, pathogenicity of bacteria and the use of gene 16SrRNA for ice-ice detection on seaweed aquaculture (Kappaphycus alvarezii)]. [Ph.D. Thesis. Bogor Agricultural University].
• Arisandi, A., & Farid, A. (2014). Dampak faktor ekologis terhadap sebaran penyakit ice-ice. Jurnal Kelautan: Indonesian Journal of Marine Science and Technology, 7(1), 20-25.
• Azizi, A., Mohd Hanafi, N., Basiran, M. N., & Teo, C. H. (2018). Evaluation of disease resistance and tolerance to elevated temperature stress of the selected tissue-cultured Kappaphycus alvarezii Doty 1985 under optimized laboratory conditions. 3 Biotech, 8(8), 321. https://doi.org/10.1007/s13205-018-1354-4
• Badraeni, B., Syamsuddin, R., Haryati, H., & Samawi, F. (2020). Weeds, epiphytes and ice-ice disease on green-strained Kappaphycus alvarezii (doty) in Takalar waters, South Sulawesi in different seasons and locations of cultivation. Plant Archives, 20(Supplement 2), 2327-2332.
• Borlongan, I. A. G., Tibubos, K. R., Yunque, D. A. T., Hurtado, A. Q., & Critchley, A. T. (2011). Impact of AMPEP on the growth and occurrence of epiphytic Neosiphonia infestation on two varieties of commercially cultivated Kappaphycus alvarezii grown at different depths in the Philippines. Journal of Applied Phycology, 23(3), 615-621. https://doi.org/10.1007/s10811-010-9649-9
• Campbell, R., & Hotchkiss, S. (2017). Carrageenan industry market overview. In Anicia Q. Hurtado, Alan T. Critchley, & Iain C. Neish (Eds.), Tropical seaweed farming trends, problems and opportunities (pp. 193-205). Springer.
• Cottier-Cook, E., Nagabhatla, N., Badis, Y., Campbell, M., Chopin, T., Dai, W., Fang, J., He, P., Hewitt, C., & Kim, G. (2016). Safeguarding the future of the global seaweed aquaculture industry. United Nations University and Scottish Association for Marine Science Policy Brief. 12p. Retrieved from http://voices.nationalgeographic.com/files/2016/08/Final-unu-seaweed-aquaculturepolicy-for-printing.pdf
• FAO. (2020). The State of World Fisheries and Aquaculture, 2020. Sustainability in Action. Food & Agriculture Organization.
• Ganzon-Fortes, E., Azanza-Corrales, R., & Aliaza, T. (1993). Kappaphycus alvarezii (Doty) Doty Using P vs I Curve. Botanica marina, 36, 503-506.
• Handayani, T., Alimuddin, A., Widyastuti, U., Suryati, E., & Parenrengi, A. (2014). Binary vector construction and Agrobacterium tumefaciens-mediated transformation of lysozyme gene in seaweed Kappaphycus alvarezii. Biotropia, 21(2), 80-90.
• Harrison, P. J., & Hurd, C. L. (2001). Nutrient physiology of seaweeds: Application of concepts to aquaculture. Cahiers de Biologie Marine, 42(1-2), 71-82.
• Hayashi, L., Reis, R. P., dos Santos, A. A., Castelar, B., Robledo, D., de Vega, G. B., Msuya, F. E., Eswaran, K., Yasir, S. M., & Ali, M. K. M. (2017). The cultivation of Kappaphycus and Eucheuma in tropical and sub-tropical waters. In Anicia Q. Hurtado, Alan T. Critchley, & Iain C. Neish (Eds.), Tropical seaweed farming trends, problems and opportunities (pp. 55-90). Springer.
• Hurd, C. L., Harrison, P. J., Bischof, K., & Lobban, C. S. (2014). Seaweed ecology and physiology. Cambridge University Press.
• Hurtado, A. Q., & Critchley, A. T. (2013). Impact of Acadian marine plant extract powder (AMPEP) in Kappaphycus production. Malaysian Journal of Sciences, 32(SCS Supplement Issue), 239-252.
• Hurtado, A. Q., Critchley, A. T., Trespoey, A., & Bleicher-Lhonneur, G. (2008). Growth and carrageenan quality of Kappaphycus striatum var. sacol grown at different stocking densities, duration of culture and depth. In M. A. Borowitzka, A. T. Critchley, S. Kraan, A. Peters, K. Sjøtun, & M. Notoya (Eds.), Nineteenth international seaweed symposium. Developments in applied phycology. vol 2. Springer.
• Hurtado, A. Q., Critchley, A. T., Trespoey, A., & Lhonneur, G. B. (2006). Occurrence of Polysiphonia epiphytes in Kappaphycus farms at Calaguas Is., Camarines Norte, Philippines. Journal of Applied Phycology, 18(3-5), 301-306. https://doi.org/10.1007/s10811-006-9032-z
• Illud, H. (2020). Effects of organic fertilizers on the growth performance, “ice-ice” disease occurrence and carrageenan quality of farmed seaweed Kappaphycus striatus (F. Schmitz) Doty Ex. P.C. Silva. International Journal of Mechanical and Production Engineering Research and Development, 10(3), 12313-12330.
• Irmawati, Y., & Sudirjo, F. (2017). Infection Vibrio sp. bacteria on Kappaphycus seaweed varieties brown and green. IOP Conference Series: Earth and Environmental Science, 89, 012016. https://doi.org/10.1088/1755-1315/89/1/012016
• Kopprio, G. A., Cuong, L. H., Luyen, N. D., Duc, T. M., Ha, T. H., Huong, L. M., & Gardes, A. (2021). Carrageenophyte-attached and planktonic bacterial communities in two distinct bays of Vietnam: Eutrophication indicators and insights on ice-ice disease. Ecological Indicators, 121, 107067. https://doi.org/10.1016/j.ecolind.2020.107067
• Largo, D. B. (2002). Recent developments in seaweed diseases. In A. Q. Hurtado, N. G. Guanzon, Jr., T. R. de Castro-Mallare, & M. R. J. Luhan (Eds.), Proceedings of the National Seaweed Planning Workshop. Philippines. pp. 35-42.
• Largo, D. B., Fukami, K., Nishijima, T., & Ohno, M. (1995a). Laboratory-induced development of the ice-ice disease of the farmed red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 7(6), 539-543. https://doi.org/10.1007/Bf00003940
• Largo, D. B., Fukami, K., & Nishijima, T. (1995b). Occasional pathogenic bacteria promoting ice-ice disease in the carrageenan-producing red algae Kappaphycus alvarezii and Eucheuma denticulatum (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 7(6), 545-554. https://doi.org/10.1007/Bf00003941
• Largo, D. B., Fukami, K., & Nishijima, T. (1999). Time-dependent attachment mechanism of bacterial pathogen during ice-ice infection in Kappaphycus alvarezii (Gigartinales, Rhodophyta). Journal of Applied Phycology, 11, 129–136. https://doi.org/10.1023/A:1008081513451
• Largo, D. B., Fukami, K., Adachi, M., & Nishijima, T. (1998). Immunofluorescent detection of ice-ice disease-promoting bacterial strain Vibrio sp. P11 of the farmed macroalga, Kappaphycus alvarezii (Gigartinales, Rhodophyta). Journal of Marine Biotechnology, 6(3), 178-182.
• Largo, D. B., Msuya, F. E., & Menezes, A. (2020). Understanding diseases and control in seaweed farming in Zanzibar. FAO Fisheries and Aquaculture Technical Paper (662), 0_1-49.
• Loureiro, R. R., Cornish, M., & Neish, I. C. (2017a). Applications of carrageenan: with special reference to iota and kappa forms as derived from the eucheumatoid seaweeds. In Anicia Q. Hurtado, Alan T. Critchley, & Iain C. Neish (Eds.), Tropical seaweed farming trends, problems and opportunities (pp. 165-171). Springer
• Loureiro, R. R., Hurtado, A. Q., & Critchley, A. T. (2017b). Impacts of AMPEP on epiphytes and diseases in Kappaphycus and Eucheuma cultivation. In Anicia Q. Hurtado, Alan T. Critchley, & Iain C. Neish (Eds.), Tropical seaweed farming trends, problems and opportunities (pp. 111-119). Springer.
• Luhan, M. R. J., Avañcena, S. S., & Mateo, J. P. (2015). Effect of short-term immersion of Kappaphycus alvarezii (Doty) Doty in high nitrogen on the growth, nitrogen assimilation, carrageenan quality, and occurrence of “ice-ice” disease. Journal of Applied Phycology, 27(2), 917-922. http://dx.doi.org/10.1007/s10811-014-0365-8
• Maryunus, R. P. (2018). Pengendalian Penyakit Ice-ice Budidaya Rumput Laut, Kappaphycus alvarezii: Korelasi Musim dan manipulasi Terbatas Lingkungan [“Ice-ice” disease control of seaweed cultivation, Kappaphycus alvarezii: the correlation of season and limited environmental manipulation]. Jurnal Kebijakan Perikanan Indonesia, 10(1), 1-10.
• Mendoza, W. G., Montaño, N. E., Ganzon-Fortes, E. T., & Villanueva, R. D. (2002). Chemical and gelling profile of ice-ice infected carrageenan from Kappaphycus striatum (Schmitz) Doty “sacol” strain (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 14(5), 409-418.
• Msuya, F. E., & Porter, M. (2014). Impact of environmental changes on farmed seaweed and farmers: the case of Songo Songo Island, Tanzania. Journal of Applied Phycology, 26(5), 2135-2141. https://doi.org/10.1007/s10811-014-0243-4
• Mtolera, M. S. P., Collen, J., Pedersen, M., Ekdahl, A., Abrahamsson, K., & Semesi, A. K. (1996). Stress-induced production of volatile halogenated organic compounds in Eucheuma denticulatum (Rhodophyta) caused by elevated pH and high light intensities. European Journal of Phycology, 31(1), 89-95. https://doi.org/10.1080/09670269600651241
• Ndobe, S., Yasir, I., Salanggon, A.-I. M., Wahyudi, D., Adel, Y. S., & Moore, A. M. (2020). Eucheumatoid seaweed farming under global change-Tomini Bay seaweed trial indicates Eucheuma denticulatum (spinosum) could contribute to climate adaptation. Aquaculture, Aquarium, Conservation & Legislation, 13(5), 2452-2467.
• Necas, J., & Bartosikova, L. (2013). Carrageenan: A review. Veterinarni Medicina, 58(4), 187-205. https://doi.org/10.17221/6758-VETMED
• Pang, T., Liu, J. G., Liu, Q., Li, H., & Li, J. P. (2015). Observations on pests and diseases affecting a eucheumatoid farm in China. Journal of Applied Phycology, 27(5), 1975-1984. https://doi.org/10.1007/s10811-014-0507-z
• Parmar, N., Singh, K. H., Sharma, D., Singh, L., Kumar, P., Nanjundan, J., Khan, Y. J., Chauhan, D. K., & Thakur, A. K. (2017). Genetic engineering strategies for biotic and abiotic stress tolerance and quality enhancement in horticultural crops: A comprehensive review. 3 Biotech, 7(4), 239. https://doi.org/10.1007/s13205-017-0870-y
• Patadjai, R., Nur, I., & Kamri, S. (2019). Use of common lantana (Lantana camara Linn) extract to prevent ice-ice disease and trigger growth rate of the seaweed Kappaphycus alvarezii. IOP Conference Series: Earth and Environmental Science, 370, 012026. https://doi.org/10.1088/1755-1315/370/1/012026
• Rahman, S. A., Mutalib, Y., Sangkia, F. D., Athirah, A., Kadir, M., & Pattirane, C. P. (2020). Evaluation of inhibitory potential of mangrove leaves extract Avicennia marina for bacteria causing ice-ice diseases in seaweed Kappaphycus alvarezii. IOP Conference Series: Earth and Environmental Science, 564, 012056. https://doi.org/10.1088/1755-1315/564/1/012056
• Rhein-Knudsen, N., Ale, M. T., & Meyer, A. S. (2015). Seaweed hydrocolloid production: An update on enzyme assisted extraction and modification technologies. Marine Drugs, 13(6), 3340-3359. https://doi.org/10.3390/md13063340
• Riyaz, S. U. M., Nalini, S., Kavitha, G., Sutha, S. A. D., & Inbakandan, D. (2019). Characterization and identification of isolated bacteria from ice-ice disease infected seaweed Kappaphycus alvarezii. Indian Journal of Geo Marine Sciences, 48(8), 1286-1290.
• Riyaz, S. U. M., Prabhu, N. S., Nalini, S., Tejaswini, G., Christy, H. J., & Inbakandan, D. (2020). Microbiome identification from ice-ice disease infected Kappaphycus alvarezii using 16S rRNA gene sequence analysis and in silico docking studies against carrageenan degrading bacteria. Biocatalysis and Agricultural Biotechnology, 27, 101707. https://doi.org/10.1016/j.bcab.2020.101707
• Robles, R. J. F. (2020). Effects of different concentrations of ammonium phosphate on the yield and quality of carrageenan, Kappaphycus striatus (Schmitz) Doty ex Silva. Journal of Fisheries, Livestock and Veterinary Science, 01(01), 01-09. https://doi.org/10.18801/jflvs.010120.01
• Roleda, M. Y., & Hurd, C. L. (2019). Seaweed nutrient physiology: Application of concepts to aquaculture and bioremediation. Phycologia, 58(5), 552-562. https://doi.org/10.1080/00318884.2019.1622920
• Solis, M. J. L., Draeger, S., & dela Cruz, T. E. E. (2010). Marine-derived fungi from Kappaphycus alvarezii and K. striatum as potential causative agents of ice-ice disease in farmed seaweeds. Botanica Marina, 53(6), 587-594. https://doi.org/10.1515/Bot.2010.071
• Sulistiani, E., Suharsono, S., Supena, E. D. J., & Miftahudin, M. (2019). Agrobacterium-mediated genetic transformation of seaweed Kappaphycus alvarezii using Gα gene and callus cultures. Biotropia, 26(1), 40-50. https://doi.org/10.11598/btb.2019.26.1.989
• Sulistijowati, R., & Karim, Z. (2020). The inhibition of Vibrio alginolyticus by the flavonoid extract of Sonneratia alba fruit. Aquaculture, Aquarium, Conservation & Legislation - International Journal of the Bioflux Society, 13(1), 28-35.
• Syafitri, E., Prayitno, S., Ma’ruf, W., & Radjasa, O. (2017a). Genetic diversity of the causative agent of ice-ice disease of the seaweed Kappaphycus alvarezii from Karimunjawa Island, Indonesia. IOP Conference Series: Earth and Environmental Science, 55, 012044. https://doi.org/10.1088/1755-1315/55/1/012044
• Syafitri, E., Prayitno, S. B., Radjasa, O. K., & Ma’ruf, W. F. (2017b). The performance of mangrove leaf extract (Sonneratia alba) in combating bacterial associated with ice–ice disease of seaweed (Kappaphycus alvarezii). Advanced Science Letters, 23(7), 6413-6415. https://doi.org/10.1166/asl.2017.9639
• Tahiluddin, A. B. (2018). Influence of fertilization on the occurrence of Vibrio, “ice-ice” disease and growth of seaweed Kappaphycus striatus (F. Schmitz) Doty ex P.C. Silva. [M.Sc. Thesis. University of the Philippines Visayas].
• Tisera, W. L., & Naguit, M. R. A. (2009). Ice-ice disease occurrence in seaweed farms in Bais Bay, Negros Oriental and Zamboanga del Norte. The Threshold, 4, 1-16.
• Tokan, M. K., Dirawan, G. D., & Imakulata, M. M. (2015). Controlling of the ice-ice disease on seaweed through polyculture cultivation techniques. Asian Journal of Microbiology, Biotechnology & Environmental Sciences Paper, 17(1), 7-15.
• Trono, G., & Ohno, M. (1989). Seasonality in the biomass production of the Eucheuma strains in Northern Bohol, Philippines. In I. Umezaki (Ed.), Scientific Survey of Marine Algae and Their Resources in the Philippine Islands. A Technical Report of the Ministry of Education, Science and Culture, Japan, pp. 71–80
• Uyenco, F. R., Saniel, L. S., & Gomez, E. D. (1977). Microbiology of diseased Eucheuma striatum Schmitz. Journal of Phycology, 13(S 2), 3-78 (Abstract 403) https://doi.org/10.1111/j.1529-8817.1977.tb02421.x
• Vairappan, C. S. (2006). Seasonal occurrences of epiphytic algae on the commercially cultivated red alga Kappaphycus alvarezii (Solieriaceae, Gigartinales, Rhodophyta). Journal of Applied Phycology, 18(3-5), 611-617. https://doi.org/10.1007/s10811-006-9062-6
• Vairappan, C. S., Anangdan, S. P., Tan, K. L., & Matsunaga, S. (2010). Role of secondary metabolites as defense chemicals against ice-ice disease bacteria in biofouler at carrageenophyte farms. Journal of Applied Phycology, 22(3), 305-311. https://doi.org/10.1007/s10811-009-9460-7
• Ward, G. M., Faisan Jr, J. P., Cottier‐Cook, E. J., Gachon, C., Hurtado, A. Q., Lim, P. E., Matoju, I., Msuya, F. E., Bass, D., & Brodie, J. (2020). A review of reported seaweed diseases and pests in aquaculture in Asia. Journal of the World Aquaculture Society, 51(4), 815-828. https://doi.org/10.1111/jwas.12649