Abstract
Mangrove forests and adjacent creeks are known to be highly productive estuaries, which are partly supported by benthic microalgae that grow on the sediments. During surveys investigating the microalgal floras of mangrove swamps in the eastern part of Java Island, a mud sample unexpectedly included large numbers of a notorious fish killer, Chattonella-like motile cells, and its resting cysts. These motile cells were established as clonal cultures for further identification and physiological tests. The cysts were examined through palynological and molecular biological means. Identification based on light microscopy and ribosomal RNA gene sequences confirmed that these cells and cysts were Chattonella marina var. marina. While the strains were genetically identical to the temperate strains isolated from Japan and China, temperature experiments showed that the Indonesian strains possessed a high maximum quantum yield of photosystem II even after exposure to 34 °C, a temperature at which the Japanese strain could not survive. Salinity experiments showed adaptation of the strains to a salinity of 15. These findings, together with the discovery of populations of cysts in the mangrove sediment, highlight the tough and unique nature of the Indonesian strains, which are likely adapted to wide fluctuations of temperature and salinity in mangrove swamps, and pose a potential risk to fisheries in Indonesia.
Similar content being viewed by others
References
Adachi M, Sako Y, Ishida Y (1994) Restriction fragment length polymorphism of ribosomal DNA internal transcribed spacer and 5.8 S regions in Japanese Alexandrium species (Dinophyceae). J Phycol 30:857–863
Adesalu TA, Nwankwo DI (2008) Effect of water quality indices on phytoplankton of a sluggish tidal creek in Lagos, Nigeria. Pakistan J Biol Sci 11:836–844
Aksornkoae S (1993) Ecology and management of mangroves. IUCN, Bangkok
Alongi DM (1994) Zonation and seasonality of benthic primary production and community respiration in tropical mangrove forests. Oecologia 98:320–327
Anton A, Teoh PL, Mohd-Shaleh SR, Mohammad-Noor N (2008) First occurrence of Cochlodinium blooms in Sabah, Malaysia. Harmful Algae 7:331–336
Azanza RV, Benico G (2017) “Fish kills” in the Philippines associated with harmful algal blooms (HABs). In: 10th EASTHAB Symposium Harmful Algal Blooms in East Asia. Hakodate, Hokkaido, Japan, p. 17
Azanza RV, Fukuyo Y, Yap LG, Takayama H (2005) Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao, Pangasinan, Northern Philippines. Harmful Algae 4:519–524
Azanza RV, David LT, Borja RT, Baula IU, Fukuyo Y (2008) An extensive Cochlodinium bloom along the western coast of Palawan, Philippines. Harmful Algae 7:324–330
Balasubramaniam J, Prasath D, Jayaraj KA (2017) Microphytobenthic biomass, species composition and environmental gradients in the mangrove intertidal region of the Andaman Archipelago, India. Environ Monit Assess 189:231
Burford MA, Alongi DM, McKinnon AD, Trott LA (2008) Primary production and nutrients in a tropical macrotidal estuary, Darwin Harbour, Australia. Estuar Coast Shelf Sci 79:440–448
Castro P, Huber ME (2010) Marine Biology, 8th edn. McGraw-Hill, US
Cortés-Altamirano R, Alonso-Rodríguez R, Beltrán AS (2006) Fish mortality associated with Chattonella marina and C. cf. ovata (Raphidophyceae) blooms in Sinaloa (Mexico). Harmful Algae News 31:7–8
Cyrus DP, Blaber SJM (1992) Turbidity and salinity in a tropical northern Australian estuary and their influence on fish distribution. Estuar Coast Shelf Sci 35:545–556
Demura M, Noël M-H, Kasai F, Watanabe MM, Kawachi M (2009) Taxonomic revision of Chattonella antiqua, C. marina and C. ovata (Raphidophyceae) based on their morphological characteristics and genetic diversity. Phycologia 48:518–535
Edvardsen B, Imai I (2006) The ecology of harmful flagellates within Prymnesiophyceae and Raphydophyceae. In: Granéli E, Turner JT (eds) Ecology of Harmful Algae. Ecological Studies 189. Springer, Berlin, pp 67–79
Eong YS, Sulit VT (2017) Monitoring and identification of harmful algal blooms in Southeast Asia to support SDG 14.1. Fish People 15:39–46
Essien JP, Antai SP, Benson NU (2008) Microalgae biodiversity and biomass status in Qua Iboe Estuary mangrove swamp, Nigeria. Aquat Ecol 42:71–81
Fukazawa N, Ishimaru T, Takahashi M, Fujita Y (1980) A mechanism of “red tide” formation. I. Growth rate estimate by DCMU-induced fluorescence increase. Mar Ecol Prog Ser 3:217–222
Fukuyo Y, Kodama M, Omura T, Furuya K, Furio EF, Cayme M, Teen LP, Ha DV, Kotaki Y, Matsuoka K, Iwataki M, Sriwoon R, Lirdwitayaprasit T (2011) Ecology and oceanography of harmful marine microalgae (Project-2). In: Nishida S (ed) Coastal marine science in Southeast Asia—synthesis report of the Core University Program of the Japan Society for the Promotion of Science: Coastal Marine Science (2001–2010). TERRAPUB, Tokyo, pp 23–48
Hallegraeff GM (2004) Harmful algal blooms: a global overview. In: Hallegraeff GM et al (eds) Manual on harmful marine microalgae (second revision). UNESCO, Paris, pp 25–49
Higo S, Maung-Saw-Htoo-Thaw Yamatogi T, Ishida N, Hirae S, Koike K (2017) Application of a pulse-amplitude-modulation (PAM) fluorometer reveals its usefulness and robustness in the prediction of Karenia mikimotoi blooms: a case study in Sasebo Bay, Nagasaki, Japan. Harmful Algae 61:63–70
Imai I (2012) Biology and ecology of Chattonella red tides. Seibutsu Kenkyu Sha, Tokyo, pp 85–98
Imai I, Itoh K (1988) Cysts of Chattonella antiqua and C. marina (Raphidophyceae) in sediments of the Inland Sea of Japan. Bull Plankton Soc Japan 35:35–44
Imai I, Yamaguchi M (2012) Life cycle, physiology, ecology and red tide occurrences of the fish killing raphidophyte Chattonella. Harmful Algae 14:46–70
Imai I, Yamaguchi M, Hori Y (2006) Eutrophication and occurrences of harmful algal blooms in the Seto Inland Sea, Japan. Plankt Benthos Res 1:71–84
Iwataki M, Kawami H, Mizushima K, Mikulski CM, Doucette GJ, Relox JR, Anton A, Fukuyo Y, Matsuoka K (2008) Phylogenetic relationships in the harmful dinoflagellate Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) inferred from LSU rDNA sequences. Harmful Algae 7:271–277
Khoo EW (1985) Occurrences of “red tide” along Johor straits, Malaysia, resulted in heavy mortality of shrimp. World Maric Soc Newsl 16:4
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870
Leong SCY, Lim LP, Chew SM, Kok JWK, Teo SLM (2015) Three new records of dinoflagellates in Singapore’s coastal waters, with observations on environmental conditions associated with microalgal growth in the Johor Straits. Raffles Bull Zool 2015:24–36
Lim HC, Leaw CP, Tan TH, Kon NF, Yek LH, Hii KS, Teng ST, Razali RM, Usup G, Iwataki M, Lim PT (2014) A bloom of Karlodinium australe (Gymnodiniales, Dinophyceae) associated with mass mortality of cage-cultured fishes in West Johor Strait, Malaysia. Harmful Algae 40:51–62
López-Fuerte FO, Siqueiros-Beltrones DA, Navarro JN (2010) Benthic diatoms associated with mangrove environments in the northwest region of México. CONABIO, Gobierno Federal Méxicano, Mexico City. ISBN 978-607-7607-30-4
Maclean JL (1989) Indo-Pacific red tides, 1985–1988. Mar Pollut Bull 20:304–310
Matsuoka K, Fukuyo Y (2000) Technical guide for modern dinoflagellate cyst study. WESTPAC-HAB, Tokyo, pp 5–10
Matsuoka K, Ishii K (2018) Marine and freshwater palynomorphs preserved in surface sediments of Osaka Bay, Japan. Bull Osaka Mus Nat Hist 72:1–17
Matsuoka K, Iwataki M, Kawami H (2008) Morphology and taxonomy of chain-forming species of the genus Cochlodinium (Dinophyceae). Harmful Algae 7:261–270
Ministry of Marine Affairs and Fisheries (2015) Ministry of Marine Affairs and Fisheries work report 2014. KKP, Jakarta (in Bahasa Indonesia)
Mulyani Widiarti R, Wardhana W (2012) Spatial distribution of harmful algal bloom (HAB) species at the location of green mussel (Perna viridis) Kamal Muara, North Jakarta in May 2011. J Akuatika III:28–39 (in Bahasa Indonesia)
Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28(12):e63
Okaichi T (2003) Red-tide species and the environmental conditions. In: Takahashi M (ed) Red Tides. TERRAPUB, Tokyo, pp 323–332
Praseno DP, Wiadnyana NN (1996) HAB organisms in Indonesian waters. In: Penney RW (ed) Proceedings of the Fifth Canadian Workshop on Harmful Marine Algae. Department of Fisheries and Oceans, Newfoundland, Canada, pp 69-73
Putri SIP, Sari SHJ (2015) Community structure of phytoplankton and its relationship to nutrient availability and other water quality parameters. Depik 4:79–86 (in Bahasa Indonesia)
Raymond GP, Harahap N, Soemarno (2010) Community based management of mangrove forest in the Gending Subdistrict, Probolinggo. Agritek 18:185–200 (in Bahasa Indonesia with English abstract)
Sakamoto S, Yamaguchi M, Shikata T (2012) Development of a simple and rapid detection for harmful red tide algae by LAMP method. Abstracts, the 15th International Conference on Harmful Algae, pp 4–11
Sidabutar T (2016) Low dissolved oxygen concentration as the triggering factor of fish mass mortalities during algal bloom incidents in Jakarta Bay, Indonesia. Harmful Algae News 6–7
Sidabutar T, Praseno DP, Fukuyo Y (2001) Harmful algal blooms in Indonesian waters. In: Hallegraeff GM et al (eds) Ninth International Conference on Harmful Algal Blooms. UNESCO, Paris, pp 124–128
Sidabutar T, Thoha H, Bayu MD, Rachman A, Sianturi OR, Fitriya N, Muawanah Mulyadi HA, Likumahua S, Masseret E (2016) Occurence of Pyrodinium bahamense blooms related to cyst accumulation in the bottom sediments in the bays at Ambon, Lampung and Jakarta, Indonesia. Harmful Algae News 52:8–9
Sidharta BR (2004) Mass fish mortality in Jakarta Bay: HAB organisms as the culprit? Harmful Algae News 27:8–9
Su-Myat Koike K (2013) A red tide off the Myanmar coast: morphological and genetic identification of the dinoflagellate composition. Harmful Algae 27:149–158
Teixeira C, Tundisi J, Kutner MB (1964) Plankton studies in a mangrove environment. II. The standing stock and some ecological factors. Inst Ocean da USP 208:13–41
Thoha H, Adnan Q, Sidabutar T, Sugestiningsih (2007) Note on the occurrence of phytoplankton and its relation with mass mortality in the Jakarta Bay, May and November 2004. Makara 11:63–67
Thoha H, Rachman A, Sidabutar T, Fitriya N, Bayu MD, Iwataki M, Takahashi K, Masseret E (2015) First record of the harmful dinoflagellate Cochlodinium polykrikoides in Lampung Bay, Indonesia. Harmful Algae News 50:14–15
Usup G, Pin L, Teen L, Asmat A (2002) Probable toxin producer responsible for the first occurrence of paralytic shellfish poisoning on the east coast of Peninsula malaysia. Malaysian Appl Biol 31:29–35
Vicente HJ, Gaid RD, Dejarme HE, Roa EC, Azanza RV (2002) Harmful algal bloom in Iligan Bay, Southern Phillippines. Sci Diliman 14:59–65
Wagey GA (2002) Ecology and physiology of phytoplankton in Ambon Bay, Indonesia. PhD dissertation. University of British Columbia, Columbia
Wang Z, Qi Y, Chen J, Xu N, Yang Y (2006) Phytoplankton abundance, community structure and nutrients in cultural areas of Daya Bay, South China Sea. J Mar Syst 62:85–94
Wiadnyana NN, Sidabutar T, Matsuoka K, Ochi T, Kodama M, Fukuyo Y (1996) Note on the occurrence of Pyrodinium bahamense in eastern Indonesian waters. In: Yasumoto T et al (eds) Seventh International Conference on Toxic Phytoplankton. Intergovernmental Oceanographic Commission of UNESCO, Sendai, pp 53–56
Yamaguchi M, Imai I, Honjo T (1991) Effects of temperature, salinity and irradiance on the growth rates of the noxious red tide flagellates Chattonella antiqua and C. marina (Raphidophyceae). Nippon Suisan Gakkaishi 57:1277–1284 (in Japanese)
Yamaguchi M, Yamaguchi H, Nishitani G, Sakamoto S, Itakura S (2008) Morphology and germination characteristics of the cysts of Chattonella ovata (Raphidophyceae), a novel red tide flagellate in the Seto Inland Sea, Japan. Harmful Algae 7:459–463
Yamaguchi H, Mizushima K, Sakamoto S, Yamaguchi M (2010) Effects of temperature, salinity and irradiance on growth of the novel red tide flagellate Chattonella ovata (Raphidophyceae). Harmful Algae 9:398–401
Yurimoto T, Aue-umneoy D, Meeanan C, Tsutsui I (2015) Bloom of the two dinoflagellates Ceratium furca and Diplopsalis lenticula in a mangrove estuary of Thailand. Int Aquat Res 7:133–141
Acknowledgements
This work was supported by a Grant-in-Aid (KAKENHI no. 17H04625) for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan to K. K. The authors express their sincere gratitude to Ms. Tomoe Hikosaka-Katayama and Ms. Kanae Koike (Natural Science Center for Basic Research and Development, Hiroshima University) for assisting with the DNA analysis, as well as to Prof. Soetjipto, Dr., Ph.D., Institute of Tropical Disease Universitas Airlangga, who gave us information on transferring samples. We also thank Mr. Daniel Onny Setiyoko (Fisheries and Marine Faculty, Universitas Airlangga) for assisting with the specimen collection.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ayu-Lana-Nafisyah, Endang-Dewi-Masithah, Matsuoka, K. et al. Cryptic occurrence of Chattonella marina var. marina in mangrove sediments in Probolinggo, East Java Province, Indonesia. Fish Sci 84, 877–887 (2018). https://doi.org/10.1007/s12562-018-1219-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-018-1219-0