Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-20T01:32:38.314Z Has data issue: false hasContentIssue false
  • English
  • Français

Decline and recovery in cell population densities of Heterosigma akashiwo (Raphidophyceae) as a novel bloom driver for the species

Published online by Cambridge University Press:  08 July 2021

Jerome Wai Kit Kok Open the ORCID record for Jerome Wai Kit Kok [Opens in a new window]  and
Sandric Chee Yew Leong
Jerome Wai Kit Kok*
Affiliation:
Department of Civil and Environmental Engineering, National University of Singapore, 1 Engineering Drive 2, Singapore 117576
Sandric Chee Yew Leong
Affiliation:
St. John’s Island National Marine Laboratory, Tropical Marine Science Institute, National University of Singapore, 18 Kent Ridge Road, Singapore 119227
*
Author for correspondence:*Jerome Wai Kit Kok, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The frequency and intensity of harmful algal bloom (HAB) events have been increasing in many places around the world. Heterosigma akashiwo is a marine raphidophyte species known to cause HABs in many places across tropical and temperate climates. Studies of temperate strains have identified that H. akashiwo blooms are driven by mass activation of cysts which, for this species, can only form at <15°C temperatures. Although these temperatures do not occur in the tropics, there have been no comparative studies for tropical H. akashiwo. This study aimed to investigate whether tropical H. akashiwo can form cysts under warm temperatures, therefore having different responses from temperate strains. Results showed that tropical H. akashiwo were similar with temperate strains and could only form round cyst-like structures at 5°C but not 25°C. We also observed novel response of a decline and recovery in cell densities at 25°C. The decline was interrupted when the cultures were diluted, implying a tendency for H. akashiwo to rapidly spread and accumulate within surrounding waters, thereby facilitating blooms. This behaviour presents unique bloom concerns. Close monitoring of H. akashiwo distribution patterns is needed for better assessment of the bloom threat posed within tropical waters.

Keywords

harmful algal bloomsHeterosigma akashiwolightraphidophyteResting cellstemperaturetropical
Type
Research Article
Information
Journal of Tropical Ecology , Volume 37 , Issue 2 , March 2021 , pp. 91 - 97
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Astuya, A, Rivera, A, Vega-Drake, K, Aburto, C, Cruzat, F, Ulloa, V, Caprile, T and Gallardo-Rodriguez, JJ (2018) Study of the ichthyotoxic microalga Heterosigma akashiwo by transcriptional activation of sublethal marker Hsp70b in Transwell co-culture assays. PLoS One 13, 23.CrossRefGoogle ScholarPubMed
Azanza, RZ and Taylor, FJRM (2001) Are Pyrodinium blooms in the Southeast Asian region recurring and spreading? A view at the end of the millennium. AMBIO A Journal of the Human Environment 30, 356–364.CrossRefGoogle Scholar
Berdalet, E, Fleming, LE, Gowen, R, Davidson, K, Hess, P, Backer, LC, Moore, SK, Hoagland, P and Enevoldsen, H (2015) Marine harmful algal blooms, human health and wellbeing: challenges and opportunities in the 21st century. Journal of the Marine Biological Association of the United Kingdom 96, 61–91.CrossRefGoogle Scholar
Bidle, KD and Falkowski, PG (2004) Cell death in planktonic, photosynthetic microorganisms. Nature Reviews Microbiology 2, 643–655.CrossRefGoogle ScholarPubMed
Branco, S, Menezes, M, Alves-de-Souza, C, Domingos, P, Schramm, MA and Proenca, LAO (2014) Recurrent blooms of Heterosigma akashiwo (Raphidophyceae) in the Piraque Channel, Rodrigo de Freitas Lagoon, southeast Brazil. Brazilian Journal of Biology 74, 529–537.CrossRefGoogle Scholar
Brosnahan, ML, Ralston, DK, Fischer, AD, Solow, AR and Anderson, DM (2017) Bloom termination of the toxic dinoflagellate Alexandrium catenella: vertical migration behaviour, sediment infiltration, and benthic cyst yield. Limnology and oceanography 62, 2829–2849.CrossRefGoogle ScholarPubMed
Choi, CJ, Brosnahan, ML, Sehein, TR, Anderson, DM and Erdner, DL (2017) Insights into the loss factors of phytoplankton blooms: the role of cell mortality in the decline of two inshore Alexandrium blooms. Limnology and Oceanography 62, 1742–1753.CrossRefGoogle ScholarPubMed
De Boer, MK, Koolmees, EM, Vrieling, EG, Breeman, AM and Van Rijssel, M (2005) Temperature responses of three Fibrocapsa japonica strains (Raphidophyceae) from different climate regions. Journal of Plankton Research 27, 47–60.CrossRefGoogle Scholar
Dursun, F, Tas, S and Koray, T (2016) Spring bloom of the raphidophycean Heterosigma akashiwo in the Golden Horn Estuary at the northeast Sea of Marmara. Ege Journal of Fisheries and Aquatic Sciences 33, 201–207.CrossRefGoogle Scholar
Engesmo, A, Eikrem, W, Seoane, S, Smith, K, Edvardsen, B, Horgaard, A and Tomas, CR (2016) New insight into the morphology and phylogeny of Heterosigma akashiwo (Raphidophyceae), with the description of Heterosigma minor sp. nov. Phycologia 55, 279–294.CrossRefGoogle Scholar
Espelta, JM, Arias-LeClaire, H, Fernandez-Martinez, M, Doblas-Miranda, E, Munoz, A and Bonal, R (2017) Beyond predator satiation: masting but also the effects of rainfall stochasticity on weevils drive acorn predation. Ecosphere 8, 13.CrossRefGoogle Scholar
Flynn, KJ and Mitra, A (2016) Why plankton modellers should reconsider using rectangular hyperbolic (Michaelis-Menten, Monod) descriptions of predator-prey interactions. Frontiers in Marine Science 3, 17.CrossRefGoogle Scholar
Gentien, P, Lunven, M, Lazure, P, Youenou, A and Crassous, MP (2007) Motility and autotoxicity in Karenia mikimotoi (Dinophyceae). Philosophical Transactions of the Royal Society B 362, 1937–1946.CrossRefGoogle Scholar
Guillard, RR and Ryther, JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Canadian Journal of Microbiology 8, 229–239.CrossRefGoogle ScholarPubMed
Hallegraeff, GM (1998) Transport of toxic dinoflagellates via ships’ ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies. Marine Ecology Progress Series 168, 297–309.CrossRefGoogle Scholar
Han, M-S, Kim, Y-P and Cattolico, RA (2002) Heterosigma akashiwo (Raphidophyceae) resting cell formation in batch culture: strain identity versus physiological response. Journal of Phycology 38, 304–317.CrossRefGoogle Scholar
Herndon, J and Cochlan, WP (2007) Nitrogen utilization by the raphidophyte Heterosigma akashiwo: growth and uptake kinetics in laboratory cultures. Harmful Algae 6, 260–270.CrossRefGoogle Scholar
Ikeda, CE, Cochlan, WP, Bronicheski, CM, Trainer, VL and Trick, CG (2016) The effects of salinity on the cellular permeability and cytotoxicity of Heterosigma akashiwo . Journal of Phycology 52, 745–760.CrossRefGoogle ScholarPubMed
Imai, I and Itakura, S (1999) Importance of cysts in the population dynamics of the red tide flagellate Heterosigma akashiwo (Raphidophyceae). Marine Biology 133, 755–762.CrossRefGoogle Scholar
Imai, I, Itakura, S and Itoh, K (1993) Cysts of the red tide Heterosigma akashiwo, Raphidophyceae, found in bottom sediments of Northern Hiroshima Bay, Japan. Nippon Suisan Gakkaishi 59, 1669–1673.CrossRefGoogle Scholar
Imai, I, Itakura, S, Yamaguchi, M and Honjo, T (1996) Selective germination of Heterosigma akashiwo (Raphidophyceae) cysts in bottom sediments under low light conditions: a possible mechanism of red tide initiation. In Yasumoto, T, Oshima, Y and Fukuyo, Y (eds), Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp. 197–200.Google Scholar
Imai, I and Yamaguchi, M (2012) Life cycle, physiology, ecology and red tide occurrences of the fish-killing raphidophyte Chattonella. Harmful Algae 14, 46–70.CrossRefGoogle Scholar
Itakura, S, Nagasaki, K, Yamaguchi, M and Imai, I (1996) Cyst formation in the red tide flagellate Heterosigma akashiwo (Raphidophyceae). Journal of Plankton Research 18, 1975–1979.CrossRefGoogle Scholar
Jonsson, PR, Pavia, H and Toth, G (2009) Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proceedings of the National Academy of Sciences of the United States of America 106, 11177–11182.CrossRefGoogle ScholarPubMed
Kim, J-H, Kim, JH, Wang, P, Park, BS and Han, M-S (2016) An improved quantitative real-time PCR assay for the enumeration of Heterosigma akashiwo (Raphidophyceae) cysts using a DNA debris removal method and a cyst-based standard curve. PLoS One 11, 17.Google Scholar
Kim, J-H, Park, BS, Wang, P, Kim, JH, Youn, SH and Han, M-S (2015) Cyst morphology and germination in Heterosigma akashiwo (Raphidophyceae). Phycologia 54, 435–439.CrossRefGoogle Scholar
Kok, JWK and Leong, SCY (2019) Nutrient conditions and the occurrence of a Karenia mikimotoi (Kareniaceae) bloom within East Johor Straits, Singapore. Regional Studies in Marine Science 27, 11.CrossRefGoogle Scholar
Kok, JWK, Yeo, DCJ and Leong, SCY (2015) Growth and physiological responses of a tropical toxic marine microalga Heterosigma akashiwo (Heterokontophyta: Raphidophyceae) from Singapore waters to varying nitrogen sources and light conditions. Ocean Science Journal 50, 491–508.CrossRefGoogle Scholar
Kok, JWK, Yeo, DCJ and Leong, SCY (2018) Growth, pigment and chromophoric dissolved organic matter responses of tropical Chattonella subsalsa (Raphidophyceae) to nitrogen enrichment. Phycological Research 67, 134–144.CrossRefGoogle Scholar
Le, TPQ, Billen, G, Garnier, J and Chau, VM (2015) Long-term biogeochemical functioning of the Red River (Vietnam): past and present situations. Regional Environmental Change 15, 329–339.CrossRefGoogle Scholar
Leles, SG, Souza, CAD, Faria, CDO, Ramos, AB, Fernandes, AM and Moser, GADO (2014) Short-term phytoplankton dynamics in response to tidal stirring in a tropical estuary (Southeastern Brazil). Brazilian Journal of Oceanography 62, 341–349.CrossRefGoogle Scholar
Leong, SCY, Lim, LP, Chew, SM, Kok, JWK and 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 Bulletin of Zoology 31, 24–36.Google Scholar
Lim, PT, Usup, G and Leaw, CP (2012) Harmful algal blooms in Malaysian waters. Sains Malaysiana 41, 1509–1515.Google Scholar
Martinez, R, Orive, E, Laza-Martinez, A and Seoane, S (2010) Growth response of six strains of Heterosigma akashiwo to varying temperature, salinity and irradiance conditions. Journal of Plankton Research 32, 529–538.CrossRefGoogle Scholar
Mohammad-Noor, N, Sing, OF and Anwar, EW (2012) Seasonal distribution of harmful algal bloom species in East Coast of Sabah, Malaysia. Journal of Fisheries and Aquatic Science 7, 431–438.CrossRefGoogle Scholar
Nafisyah, AL, Masithah, ED, Matsuoka, K, Lamid, M, Alamsjah, MA, Ohara, S and Koike, K (2018) Cryptic occurrence of Chattonella marina var. marina in mangrove sediments in Probolinggo, East Java Province, Indonesia. Fisheries Science 84, 877–887.CrossRefGoogle Scholar
Nakamura, Y and Umemori, T (1991) Encystment of the red tide flagellate Chattonella antiqua (Raphidophyceae): cyst yield in batch cultures and cyst flux in the field. Marine Ecology Progress Series 78, 273–284.CrossRefGoogle Scholar
Pedde, S, Kroeze, C, Mayorga, E and Seitzinger, SP (2017) Modelling sources of nutrients in rivers draining into the Bay of Bengal—a scenario analysis. Regional Environmental Change 17, 2495–2506.CrossRefGoogle Scholar
Powers, L, Creed, IF and Trick, CG (2012) Sinking of Heterosigma akashiwo results in increased toxicity of this harmful algal bloom species. Harmful Algae 13, 95–104.CrossRefGoogle Scholar
Rensel, JEJ (2007) Fish kills from the harmful alga Heterosigma akashiwo in Puget Sound: recent blooms and review. Technical Report for the National Oceanic and Atmospheric Administration Center for Sponsored Coastal Ocean Research (CSCOR). Washington, p. 59.Google Scholar
Shikata, T, Nagasoe, S, Matsubara, T, Yamasaki, Y, Shimasaki, Y, Oshima, Y and Honjo, T (2007) Effects of temperature and light on cyst germination and germinated cell survival of the noxious raphidophyte Heterosigma akashiwo. Harmful Algae 6, 700–706.CrossRefGoogle Scholar
Shikata, T, Nagasoe, S, Matsubara, T, Yoshikawa, S, Yamasaki, Y, Shimasaki, Y, Oshima, Y, Jenkinson, IR and Honjo, T (2008) Factors influencing the initiation of blooms of the raphidophyte Heterosigma akashiwo and the diatom Skeletonema costatum in a port in Japan. Limnology and Oceanography 53, 2503–2518.CrossRefGoogle Scholar
Skirycz, A, Claeys, H, Bodt, SD, Oikawa, A, Shinoda, S, Andriankaja, M, Maleux, K, Eloy, NB, Coppens, F, Yoo, S-D, Saito, K and Inze, D (2011) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signalling in cell cycle arrest. The Plant Cell 23, 1876–1888.CrossRefGoogle Scholar
Tang, YZ and Gobler, CJ (2012) The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts. Harmful Algae 20, 71–80.CrossRefGoogle Scholar
Tobin, ED, Grunbaum, D, Patterson, J and Cattolico, RA (2013) Behavioural and physiological changes during benthic-pelagic transition in the harmful alga, Heterosigma akashiwo: potential for rapid bloom formation. PLoS One 8, 29.CrossRefGoogle Scholar
Tomas, CR (1978) Olisthodiscus luteus (Chrysophyceae) II. Formation and survival of a benthic stage. Journal of Phycology 14, 314–319.CrossRefGoogle Scholar
Trombetta, T, Vidussi, F, Mas, S, Parin, D, Simier, M and Mostajir, B (2019) Water temperature drives phytoplankton blooms in coastal waters. PLoS One 14, 28.CrossRefGoogle ScholarPubMed
Wu, H, Shen, C, Wang, Q, Aronson, RB, Chen, C and Xue, J (2019) Survivorship characteristics and adaptive mechanisms of phytoplankton assemblages in ballast water. Journal of Oceanology and Limnology 37, 580–588.CrossRefGoogle Scholar