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Environmental Management

, Volume 61, Issue 2, pp 275–290 | Cite as

Resting Stage of Plankton Diversity from Singapore Coastal Water: Implications for Harmful Algae Blooms and Coastal Management

  • Aurore TrottetEmail author
  • Bryan Wilson
  • Genevieve Sew Wei Xin
  • Christaline George
  • Lemuel Casten
  • Claire Schmoker
  • Nurul Syazana Binte Modh Rawi
  • Moon Chew Siew
  • Ole Larsen
  • Hans S. Eikaas
  • Karenne Tun
  • Guillaume Drillet
Article
  • 353 Downloads

Abstract

Resting strategies of planktonic organisms are important for the ecological processes of coastal waters and their impacts should be taken into consideration in management of water bodies used by multiple industries. We combined different approaches to evaluate the importance of resting stages in Singapore coastal waters. We used molecular approaches to improve the knowledge on Singapore biodiversity, we sampled and extracted cysts from sediments to evaluate the density of resting stages in Johor Strait, and we compared systematically information on Singapore planktonic biodiversity to existing published information on resting stages from these reported organisms. This is the first study evaluating the importance of resting stages in Singapore waters. Above 120 species reported in Singapore are known to produce resting stages though no previous work has ever been done to evaluate the importance of these strategies in these waters. The results from the resting stage survey confirmed 0.66 to 5.34 cyst g−1 dry weight sediment were present in the Johor Strait suggesting that cysts may be flushed by tidal currents into and out of the strait regularly. This also suggest that the blooms occurring in Singapore are likely due to secondary growth of Harmful Algae Bloom species in the water rather than from direct germination of cysts from sediment. Finally, we discuss the importance of these resting eggs for three main national industries in Singapore (shipping, marine aquaculture and provision of drinking water through seawater desalination). We argue that this study will serve as a baseline for some of the future management of Singapore waters.

Keywords

phytoplankton zooplankton bacteria spores cysts dormancy 

Notes

Acknowledgements

We thank the National Parks of Singapore, the DHI-NTU Research Centre for the financial support of the project “Made In Plankton”. The work was also supported by Elite Forsk grants nb 10-093759 and 10-094773 from the Danish Agency for Science Technology and Innovation to Guillaume Drillet. Finally, we would like to thank the entire plankton team from the Environmental Laboratories in Singapore for their continuous support and attitude toward new challenges. The authors would like to thank the two anonymous reviewers provided helpful comments on previous versions of the manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefGoogle Scholar
  2. Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, Montresor M (2012) The globally distributed genus Alexandrium: Multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35Google Scholar
  3. Awad A, Haag F, Anil AC, Abdulla A (2014) GEF-UNDP-IMO GloBallast Partnerships Programme, IOI, CSIR-NIO and IUCN. Guidance on Port Biological Baseline Surveys. GEF-UNDP-IMO GloBallast Partnerships, London, UK, GloBallast Monograph No. 22Google Scholar
  4. Azanza RV, Siringan FP, San Diego-McGlone ML, Yniguez AT, Macalalad NH, Zamora PB, Agustin MB, Matsuoka K (2004) Horizontal dinoflagellate cyst distribution, sediment characteristics and benthic flux in Manila Bay, Philippines. Phycol Res 52:376–386Google Scholar
  5. Barnes RSK (1998) The diversity of living organisms. In: Barnes RSK (ed) Blackwell Science, Oxford, p 345Google Scholar
  6. Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27(4):313–323CrossRefGoogle Scholar
  7. Beachler M, Hill D (2003) Stirring up trouble? Resuspension of bottom sediments by recreational watercraft. Lake Reserv Manag 19(1):15–25CrossRefGoogle Scholar
  8. Belmonte G (1997) Resting eggs in the life cycle of Acartia italica and A. adriatica (Copepoda, Calanoida, Acartiidae). Crustaceana-International. J Crustace Res 70:114–117CrossRefGoogle Scholar
  9. Berkeley RC, Ali N (1994) Classification and Identification of endospore forming bacteria. J Appl Bacteriol 76 (Supplement 1): 1S–8SCrossRefGoogle Scholar
  10. Boero F, Bouillon J, Gravili C, Miglietta MP, Parsons T, Piraino S (2008) Gelatinous plankton: irregularities rule the world (sometimes). Mar Ecol Prog Ser 356:299–310CrossRefGoogle Scholar
  11. Bouchard JN, Purdie DA (2011) Temporal variation of caspase 3-like protein activity in cultures of the harmful dinoflagellates Karenia brevis and Karenia mikimotoi. J Plankton Res 33(6):961–972CrossRefGoogle Scholar
  12. Boxshall GA, Halsey SH (2004) An introduction to copepod diversity, Ray SocietyGoogle Scholar
  13. Bravo I, Vila M, Casablanca S, Rodriguez F, Rial P, Riobo P, Penna A (2012) Life cycle stages of the benthic palytoxin-producing dinoflagellate Ostreopsis cf. ovata (Dinophyceae). Harmful Algae 18:24–34CrossRefGoogle Scholar
  14. Briski E, Bailey SA, MacIsaac HJ (2011b) Invertebrates and their dormant eggs transported in ballast sediments of ships arriving to the Canadian coasts and the Laurentian Great Lakes. Limnol Oceanogr 56(5):1929–1939CrossRefGoogle Scholar
  15. Briski E, Cristescu ME, Bailey SA, MacIsaac HJ (2011a) Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biol Invasions 13(6):1325–1340CrossRefGoogle Scholar
  16. Brunold C, Schiff JA (1976) Studies of sulfate utilization by algae .15. Enzymes of assimilatory sulfate reduction in Euglena and their cellular localization. Plant Physiol 57(3):430–436CrossRefGoogle Scholar
  17. Calbet A, Schmoker C, Russo F, Trottet A, Mahjoub M-S, Larsen O, Tong HY, Drillet G (2016) Non-proportional bioaccumulation of trace metals and metalloids in the planktonic food web of two Singapore coastal marine inlets with contrasting water residence times. Sci Total Environ 560-561:284–294CrossRefGoogle Scholar
  18. Camus T, Zeng C (2009) The effects of stocking density on egg production and hatching success, cannibalism rate, sex ratio and population growth of the tropical calanoid copepod Acartia sinjiensis. Aquaculture 287(1-2):145–151CrossRefGoogle Scholar
  19. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267CrossRefGoogle Scholar
  20. Carlton JT, Gellar JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261(5117):78–82CrossRefGoogle Scholar
  21. Caron DA, Garneau M-È, Seubert E, Howard MD, Darjany L, Schnetzer A, Cetinić I, Filteau G, Lauri P, Jones B (2010) Harmful algae and their potential impacts on desalination operations off southern California. Water Res 44(2):385–416CrossRefGoogle Scholar
  22. Castellani C, Lucas IAN (2003) Seasonal variation in egg morphology and hatching success in the calanoid copepods Temora longicornis, Acartia clausi and Centropages hamatus. J Plankton Res 25(5):527–537CrossRefGoogle Scholar
  23. Chua K, Hawlader MNA, Malek A (2003) Pretreatment of seawater: results of pilot trials in Singapore. Desalination 159(3):225–243CrossRefGoogle Scholar
  24. Chua T-E (1970) A preliminary study on the plankton of the Ponggol Estuary. Hydrobiologia 35(2):254–272CrossRefGoogle Scholar
  25. Cohen AN, Dobbs FC (2015) Failure of the public health testing program for ballast water treatment systems. Mar Pollut Bull 91(1):29–34CrossRefGoogle Scholar
  26. Dale B (1983) Dinoflagellate resting cysts: ‘Benthic plankton’. In: Fryxell GA (ed) Survival strategies of the algae. Cambridge Univ. Press, CambridgeGoogle Scholar
  27. De Stasio BT (2007) Egg bank formation by aquatic invertebrates. In:Alekseev VR, De Stasio BT, Gilbert JJ (eds) Diapause in Aquatic invertebrates, Theory and human use. Monographiae Biologicae, Dordrecht, The NederlandsGoogle Scholar
  28. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072CrossRefGoogle Scholar
  29. Drillet G (2014a) Interesting Gaps between Science and Policy: 9 + 9 = less than 10; Do Size and Temperature Matter? In: International Conference on Ballast Water Management 2014. SingaporeGoogle Scholar
  30. Drillet G (2016) Food security: Protect aquaculture from ship pathogens. Nature 539:31CrossRefGoogle Scholar
  31. Drillet G, Chan. N, Drillet Z, Foulsham A, Ducheyne A (2014b) Opinions on the Sustainable Development of Aquaculture. J Fish & Livest Prod 2(118):2Google Scholar
  32. Drillet G, Frouël S, Sichlau MH, Jepsen PM, Højgaard JK, Joarder AK, Hansen BW (2011a) Status and recommendations on marine copepod cultivation for use as live feed. Aquaculture 315:155–166CrossRefGoogle Scholar
  33. Drillet G, Goetze E, Jepsen PM, Højgaard JK, Hansen BW (2008) Strain-specific vital rates in four Acartia tonsa cultures, I: Strain origin, genetic differentiation and egg survivorship. Aquaculture 280(1-4):109–116CrossRefGoogle Scholar
  34. Drillet G, Hansen BW, Kiørboe T (2011b) Resting egg production induced by food limitation in the calanoid copepod Acartia tonsa. Limnol Oceanogr 56(6):2064CrossRefGoogle Scholar
  35. Drillet G, Schmoker C, Trottet A, Mahjoub MS, Duchemin M, Andersen M (2013) Effects of temperature on type approval testing of ballast water treatment systems. Integr Environ Assess Manag 9(2):192–195CrossRefGoogle Scholar
  36. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461CrossRefGoogle Scholar
  37. Egan S, James S, Holmström C, Kjelleberg S (2001) Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicate. FEMS Microbiol Ecol 35(1):67–73CrossRefGoogle Scholar
  38. Engel M (2005) [Calanoid copepod resting eggs-a safeguard against adverse environmental conditions in the German Bight and the Kara Sea?] Die Berichte zur Polar-und Meeresforschung 508 ISSN 161 8–31 93Google Scholar
  39. Engel M, Hirche H-J (2004) Seasonal variability and inter-specific differences in hatching of calanoid copepod resting eggs from sediments of the German Bight (North Sea). J Plankton Res 26(9):1083–1093CrossRefGoogle Scholar
  40. Everson S, Fabbro L, Kinnear S, Wright P (2011) Extreme differences in akinete, heterocyte and cylindrospermopsin concentrations with depth in a successive bloom involving Aphanizomenon ovalisporum (Forti) and Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju. Harmful Algae 10(3):265–276CrossRefGoogle Scholar
  41. Fell PE (1974) Diapause in the Gemmules of the Marine Sponge. Haliclona loosanoffi, with a Note on the Gemmules of Haliclona oculata. Biol Bull 147(2):333–351CrossRefGoogle Scholar
  42. Figueroa RI, Garces E, Bravo I (2007) Comparative study of the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture. J Phycol 43(5):1039–1053Google Scholar
  43. Foissner W, Müller H, Agathaa S (2007) A comparative fine structural and phylogenetic analysis of resting cysts in oligotrich and hypotrich Spirotrichea (Ciliophora). European. J Protistol 43(4):295–314CrossRefGoogle Scholar
  44. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  45. Fukuyo Y, Sako Y, Matsuoka K, Imai I, Takahashi M, Watanabe M (2004) Biological Character of Red Tide Organisms. In: Tomotoshi. Okaichi (ed) Red Tides. Terra Scientific Publishing Company, TokyoGoogle Scholar
  46. Furio EF, Matsuoka K, Mizushima K, Baula I, Chan KW, Puyong A, Srivilai D, Sidharta BR, Fukuyo Y (2006) Assemblage and geographical distribution of dinoflagellate cysts in surface sediments of coastal waters of Sabah, Malaysia. Coast Mar Sci 30:62–73Google Scholar
  47. Genovesi B, Laabir M, Masseret E, Collos Y, Vaquer A, Grzebyk D (2009) Dormancy and germination features in resting cysts of Alexandrium tamarense species complex (Dinophyceae) can facilitate bloom formation in a shallow lagoon (Thau, southern France). J Plankton Res 31(10):1209–1224CrossRefGoogle Scholar
  48. Gin KY-H, Holmes MJ, Zhang S, Lin X (2006) Phytoplankton structure in the tropical port waters of Singapore. In: Wolanski E (eds) The Environment in Asia Pacific Harbours. Springer, DordrechtGoogle Scholar
  49. Gin KY-H, Lin X, Zhang S (2000) Dynamics and size structure of phytoplankton in the coastal waters of Singapore. J Plankton Res 22(8):1465–1484CrossRefGoogle Scholar
  50. Gin KY-H, Zhang S, Lee Y (2003) Phytoplankton community structure in Singapore’s coastal waters using HPLC pigment analysis and flow cytometry. J Plankton Res 25(12):1507–1519CrossRefGoogle Scholar
  51. Godhe A, Noren F, Kuylenstierna M, Ekberg C, Karlson B (2001) Relationship between planktonic dinoflagellate abundance, cysts recovered in sediment traps and environmental factors in the Gullmar Fjord, Sweden. J Plankton Res 23(9):923–938CrossRefGoogle Scholar
  52. Gomez F, Moreira D, Lopez-Garcia P (2010) Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161(1):35–54Google Scholar
  53. Gollasch S (2007) Is ballast water a major dispersal mechanism for marine organisms? Biol Invasions W Nentwig, Springe Berl Heidelb 193:49–57CrossRefGoogle Scholar
  54. Gollasch S, Lenz J, Dammer M, Andres H-G (2000) Survival of tropical ballast water organisms during a cruise from the Indian Ocean to the North Sea. J Plankton Res 22(5):923–937CrossRefGoogle Scholar
  55. Hairston NG, Caceres CE (1996) Distribution of crustacean diapause: Micro- and macroevolutionary pattern and process. Hydrobiologia 320(1-3):27–44CrossRefGoogle Scholar
  56. Hallegraeff GM, Anderson DM, Cembella AD, Enevoldsen HO (2003) Manual on Harmful Marine Microalgae, Intergovernmental Oceanographic Commission, UNESCO, ParisGoogle Scholar
  57. Hallegraeff GM, Bolch C (1992) Transport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture. J Plankton Res 14(8):1067–1084CrossRefGoogle Scholar
  58. Hansen BW, Drillet G (2013) Comparative oxygen consumption rates of subitaneous and delayed hatching eggs of the calanoid copepod Acartia tonsa (Dana). J Exp Mar Bio Ecol 442:66–69CrossRefGoogle Scholar
  59. Hansen BW, Drillet G, Kozmer A, Madsen KV, Pedersen MF, Sorensen TF (2010) Temperature effects on copepod egg hatching: does acclimatization matter? J Plankton Res 32:305–315CrossRefGoogle Scholar
  60. Hardy JT, Curl H (1968) Red snow caused by a new species of Trachelomonas. J Phycol 4(1):9–10CrossRefGoogle Scholar
  61. Hargraves PE (1976) Studies on marine plankton diatoms.2. Resting Spore Morphol J Phycol 12(1):118–128Google Scholar
  62. Harnstrom K, Godhe A, Saravanan V, Karunasagar I, Rehnstam-Holm A-S (2007) Tropical phytoplankton community development in mesocosms inoculated with different life stages. Mar Ecol Prog Ser 346:75–88CrossRefGoogle Scholar
  63. Hasle GR, Sims PA (1985) The morphology of the diatom resting spores Syringidium bicorne and Syringidium simplex. Br Phycol J 20:219–225CrossRefGoogle Scholar
  64. Hayes DF, Crockett TR, Ward TJ, Averett D (2000) Sediment resuspension during cutterhead dredging operations. J Waterw, Port, Coast, Ocean Eng 126(3):153–161CrossRefGoogle Scholar
  65. Herbert PDN, Beaton MJ (1990) Breeding system and genome size of the rhabdocoel turbellarian Mesostoma ehrenbergii. Genome 33(5):719–724CrossRefGoogle Scholar
  66. Hoban MA, Fryxell GA, Buck KR (1980) Biddulphioid diatoms-resting spores in antarctic Eucampia and Odontella. J Phycol 16(4):591–602CrossRefGoogle Scholar
  67. IMO (2004) (ed) International Convention for the Control and Management of the Ships’ Ballast Water and Sediments. IMO Publications, LondonGoogle Scholar
  68. Irvine KN, Chua LHC, Eikaas HS (2014) The four national taps of Singapore: a holistic approach to water resources management from drainage to drinking water. J Water Manag Model 1–11Google Scholar
  69. Ishii K-I, Ishikawa A, Imai I (2012) Newly identified resting stage cells of diatoms from sediments collected in Ago Bay, central part of Japan. Plankton and Benthos. Research 7(1):1–7Google Scholar
  70. James MR (1991) Sampling and preservation methods for the quantitative enumeration of microzooplankton. NZ J Mar Freshw Res 25(3):305–310CrossRefGoogle Scholar
  71. Jones HM, Simpson GE, Stickle AJ, Mann DG (2005) Life history and systematics of Petroneis (Bacillariophyta), with special reference to British waters. Eur J Phycol 40(1):61–87CrossRefGoogle Scholar
  72. Jones RJ (2011) Environmental effects of the cruise tourism boom: sediment resuspension from cruise ships and the possible effects of increased turbidity and sediment deposition on corals (Bermuda). Bull Mar Sci 87(3):659–679CrossRefGoogle Scholar
  73. Joshi KR, Gavin JB, Wheeler EE (1975) Ultrastructure of Prototheca-wickerhamii. Mycopathologia 56(1):9–13CrossRefGoogle Scholar
  74. Kasahara S, Uye S, Onbe T (1975) Calanoid copepod eggs in sea-bottom muds .2. Seasonal cycles of abundance in populations of several species of copepods and their eggs in inland Sea of Japan. Mar Biol 31(1):25–29CrossRefGoogle Scholar
  75. Katajisto T (2006) Benthic resting eggs in the life cycles of calanoid copepods in the northern Baltic Sea, PhD thesis, University of Helsinki, FinlandGoogle Scholar
  76. Khoo HW, Wee JY (1997) Phytoplankton monitoring and harmful algae occurrences in Singapore waters – historical perspective and status. In: Vigers G, Ong KS, McPherson C, Millson N, Watson I, Tang A (eds) ASEAN Marine Environmental Management: Quality Criteria and Monitoring for Aquatic Life and Human Health Protection. Proceedings of the ASEAN-Canada Technical Conference on Marine Science (24–28 June 1996), Penang, Malaysia. EVS Environmental consultants, North Vancouver and Department of Fisheries, Malaysia, pp 58–67Google Scholar
  77. Kim YO, Taniguchi A (1997) Seasonal variation of excystment pattern of the planktonic oligotrich ciliate Strombidium conicum. Mar Biol 28(2):207–212CrossRefGoogle Scholar
  78. Koester JA, Brawley SH, Karp-Boss L, Mann DG (2007) Sexual reproduction in the marine centric diatom Ditylum brightwellii (Bacillariophyta). Eur J Phycol 42(4):351–366CrossRefGoogle Scholar
  79. Lau SC, Zhang R, Brodie EL, Piceno YM, Andersen G, Liu W-T (2013) Biogeography of bacterioplankton in the tropical seawaters of Singapore. FEMS Microbiol Ecol 84(2):259–269CrossRefGoogle Scholar
  80. Laycock MV, Anderson DM, Naar J, Goodman A, Easy DJ, Donovan MA, Li A, Quilliam MA, Al Jamali E, Alshihi R (2012) Laboratory desalination experiments with some algal toxins. Desalination 293:1–6CrossRefGoogle Scholar
  81. Lee A (2014) 160 tonnes of dead fish found in farms along Johor Straits. Today OnlineGoogle Scholar
  82. Lei Y-L, Stummc K, Wickhama SA, Berninger U-G (2014) Distributions and Biomass of Benthic Ciliates, Foraminifera and Amoeboid Protists in Marine, Brackish, and Freshwater Sediments. Eukaryot Microbiol 61:493–508CrossRefGoogle Scholar
  83. Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130CrossRefGoogle Scholar
  84. 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 Zoology S31: 24–36Google Scholar
  85. Leray M, Knowlton N (2014) DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. PNAS 112(7):2076–2081CrossRefGoogle Scholar
  86. Li Z, Han MS, Matsuoka K, Kim SY, Shin HH (2015) Identification of the resting cyst of Cochlodinium polykrikoides Margalef (dinophyceae, gymnodiniales) in Korean coastal sediments. J Phycol 51(1):204–210CrossRefGoogle Scholar
  87. Lindholm T, Lindroos P, Mork AC (1988) Ultrastructure of the photosynthetic ciliate Mesodinium rubrum. Biosystems 21(2):141–149CrossRefGoogle Scholar
  88. Lindley JA, Hunt HG (1989) The distributions of Labidocera wollastoni and Centropages hamatus in the North Atlantic Ocean and the North Sea in relation to the role of resting eggs in the sediment. Reproduction, genetics and distributions of marine organisms. 104(2):407–413Google Scholar
  89. Madhupratap M, Onbé T (1986) Structure and species diversity of zooplankton community of the Inland Sea of Japan. Estuar, Coast Shelf Sci 23:725–737CrossRefGoogle Scholar
  90. Marcus NH (1989) Abundance in bottom sediments and hatching requirements of Centropages hamatus (Copepoda: Calanoida) from the Alligator harbor region, Florida. Biol Bull 176:142–146CrossRefGoogle Scholar
  91. Marcus NH (1996) Ecological and evolutionary significance of resting eggs in marine copepods: Past, present, and future studies. Hydrobiologia 320(1–3):141–152Google Scholar
  92. Marcus NH, Taulbee K (1992) Potential effects of a resuspension event on the vertical distribution of copepod eggs in the sea bed: a laboratory simulation. Mar Biol 114:249–251CrossRefGoogle Scholar
  93. Marcus NH (1979) Population biology and nature of diapause of Labidocera aestiva (Copepoda, Calanoida). Biol Bull 157(2):297–305CrossRefGoogle Scholar
  94. Marcus NH, Richmond C, Sedlacek C, Miller GA, Oppert C (2004) Impact of hypoxia on the survival, egg production and population dynamics of Acartia tonsa Dana. J Exp Mar Bio Ecol 301(2):111–128CrossRefGoogle Scholar
  95. Matsuoka K, Fukuyo Y (2000) Technical guide for modern dinoflagellate cyst study. WESTPAC-HAB, Japan Society for the Promotion of Science, Tokyo, JapanGoogle Scholar
  96. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618CrossRefGoogle Scholar
  97. McKinnon AD, Kimmerer WJ, Benzie JAH (1992) Sympatric sibling species within the genus Acartia (Copepoda: Calanoida): a case study from Westernport and Port Phillip Bays. Australian. J Crustace Biol 12:239–259CrossRefGoogle Scholar
  98. McQuoid MR, Godhe A, Nordberg K (2002) Viability of phytoplankton resting stages in the sediments of a coastal Swedish fjord. Eur J Phycol 37:191–201CrossRefGoogle Scholar
  99. Meier R, Shiyang K, Vaidya G, Ng PK (2006) DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Syst Biol 55(5):715–728CrossRefGoogle Scholar
  100. MEPC69/INF.25 (2016) Introduction of the same risk area concept in relation to the Ballast Water Management Convention and its Guidelines. IMOGoogle Scholar
  101. MEPC70/INF.21 (2016) A Study on Same Risk Area With Regards to Ballast Water Management Convention Regulation A-4 on Exemptions to Ships. IMOGoogle Scholar
  102. Mohamed ZA, Al-Shehri AM (2011) Occurrence and germination of dinoflagellate cysts in surface sediments from the Red Sea off the coasts of Saudi Arabia. Oceanologia 53(1):121–136CrossRefGoogle Scholar
  103. Montresor M, Di Prisco C, Sarno D, Margiotta F, Zingone A (2013) Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Mar Ecol Prog Ser 484:79CrossRefGoogle Scholar
  104. Montresor M, Zigone A, Sarno D (1998) Dinoflagellate cyst production at a coastal Mediterranean site. J Plankton Res 20:2291–2312CrossRefGoogle Scholar
  105. Moro I, La Rocca N, Dalla Valle L, Moschin E, Negrisolo E, Andreoli C (2002) Pyramimonas australis sp. nov (Prasinophyceae, Chlorophyta) from Antarctica: fine structure and molecular phylogeny. Eur J Phycol 37(1):103–114CrossRefGoogle Scholar
  106. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59(3):695–700Google Scholar
  107. Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Archives of Microbiology 164(3):165–172Google Scholar
  108. Nagai S, Imai I (1999) Factors inducing resting-cell formation of Coscinodiscus wailesii Gran (Bacillariophyceae) in culture. Plankton Biol Ecol 46(2):94–103Google Scholar
  109. Narale DD, Patil JS, Anil AC (2013) Dinoflagellate cyst distribution in recent sediments along the south-east coast of India. Oceanologia 55:979–1003CrossRefGoogle Scholar
  110. Nayar S, Goh BPL, Chou LM (2002) A portable, low-cost, multipurpose, surface–subsurface plankton sampler. J Plankton Res 24(10):1097–1105CrossRefGoogle Scholar
  111. Nehring S (1993) Mechanisms for recurrent nuisance algal blooms in coastal zones: resting cyst formation as life-strategy of dinoflagellates. In: Sterr H, Hofstade J, Plag H-P (eds) Interdisciplinary Discussion of Coastal Research and Coastal Management Issues and Problems. Lang, Frankfurt, p 454–467Google Scholar
  112. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64(3):548–572CrossRefGoogle Scholar
  113. Norrbin MF (1996) Timing of diapause in relation to the onset of winter in the high-latitude copepods Pseudocalanus acuspes and Acartia longiremis. Mar Ecol Prog Ser 142:99–109CrossRefGoogle Scholar
  114. Olli K (1996) Resting cyst formation of Eutreptiella gymnastica (Euglenophyceae) in the northern coastal Baltic Sea. J Phycol 32:535–542CrossRefGoogle Scholar
  115. Omura T, Iwataki M, Borja V, Takayama H, Fukuyo Y (2012) Marine Phytoplankton of the Western Pacific. Kouseisha, Kouseikaku, TokyoGoogle Scholar
  116. Onbe T (1985) Seasonal fluctuations in the abundance of populations of marine cladocerans and their resting eggs in the inland sea of Japan. Mar Biol 87(1):83–88CrossRefGoogle Scholar
  117. Onda DFL, Lluisma AO, Azanza RV (2014) Development, morphological characteristics and viability of temporary cysts of Pyrodinium bahamense var. compressum (Dinophyceae) in vitro. Eur J Phycol 49(3):265–275CrossRefGoogle Scholar
  118. Parsons ML, Aligizaki K, Bottein M-YD, Fraga S, Morton SL, Penna A, Rhodes L (2012) Gambierdiscus and Ostreopsis: Reassessment of the state of knowledge of their taxonomy, geography, ecophysiology, and toxicology. Harmful Algae 14:107–129CrossRefGoogle Scholar
  119. Pham MN, Tan HTW, Mitrovic S, Yeo HHT (2011) A checklist of the algae of Singapore. Raffles Museum of Biodiversity Research, National University of Singapore, Singapore, pp 1–100Google Scholar
  120. Pierce RW, Turner JT (1993) Global biogeography of marine tintinnids. Mar Ecol Prog Ser 94:11–11CrossRefGoogle Scholar
  121. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596CrossRefGoogle Scholar
  122. Quek C, Lim J (2010) Plankton bloom causes losses reaching hundreds of thousands of dollars, Strait Times. Accessed 10 Jan 2010Google Scholar
  123. Rahman H, Hawlader M, Malek A (2003) An experiment with a single-effect submerged vertical tube evaporator in multi-effect desalination. Desalination 156(1):91–100CrossRefGoogle Scholar
  124. Razouls C, de Bovée F, Kouwenberg J, Desreumaux N (2005–2014). Diversity and Geographic Distribution of Marine Planktonic Copepods. http://copepodes.obs-banyuls.fr/en
  125. Reid PPC, John AW (1978) Tintinnid cysts. J Mar Biol Assoc UK 58(03):551–557CrossRefGoogle Scholar
  126. Reynolds CS (2006) The ecology of phytoplankton. Cambridge University Press, CambridgeGoogle Scholar
  127. Rubino F, Moscatello S, Belmonte M, Ingrosso G, Belmonte G (2013) Plankton resting stages in the marine sediments of the Bay of Vlorë (Albania). Int J Ecol 12 pagesGoogle Scholar
  128. Ruiz GM, Rawlings TK, Dobbs FC, Drake LA, Mullady T, Huq A, Colwell RR (2000) Global spread of microorganisms by ships. Nature 408(6808):49–50CrossRefGoogle Scholar
  129. Santangelo JM, Rabelo Araújo L, de Assis Esteves F, Manca M, Bozelli RL (2011) Method for hatching resting eggs from tropical zooplankton: effects of drying or exposing to low temperatures before incubation. Acta Limnol Bras 23(1):42–47CrossRefGoogle Scholar
  130. Santella L, Ianora A (1990) Subitaneous and diapause eggs in Mediterranean populations of Pontella mediterranea (Copepoda: Calanoida): a morphological study. Mar Biol 105:83–90CrossRefGoogle Scholar
  131. Schlie C, Woelfel J, Rüdiger F, Schumann R, Karsten U (2011) Ecophysiological Performance of Benthic Diatoms from Arctic Waters. In: Seckbach J, Kociolek P (eds) The Diatom world. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 19. Springer, Dordrecht, pp 425–436Google Scholar
  132. Schmoker C, Mahjoub M-S, Calbet A, Hsiao S-H, Russo F, Larsen O, Trottet A, Drillet G (2014) A review of the zooplankton in Singapore waters. Raffles Bull Zool 62:726–749Google Scholar
  133. Schmoker C, Russo F, Drillet G, Trottet A, Mahjoub S-M, Hsiao S-H, Larsen O, Tun K, Calbet A (2016) Effects of eutrophication on the planktonic food web dynamics of marine coastal ecosystems: The case study of two tropical inlets. Mar Environ Res 119:176–188CrossRefGoogle Scholar
  134. Seebens H, Gastner M, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecol Lett 16(6):782–790CrossRefGoogle Scholar
  135. Seebens H, Schwartz N, Schupp PJ, Blasius B (2016) Predicting the spread of marine species introduced by global shipping. Proc Natl Acad Sci USA 113:5646–5651CrossRefGoogle Scholar
  136. Setlow P (2006) Spores of Bacillus subtilis: their resistance to radiation, heat and chemicals. J Appl Microbiol 101:514–525CrossRefGoogle Scholar
  137. Shikata T, Yoshikawa S, Matsubara T, Tanoue W, Yamasaki Y, Shimasaki Y, Matsuyama Y, Oshima Y, Jenkinson IR, Honjo T (2008) Growth dynamics of Heterosigma akashiwo (Raphidophyceae) in Hakata Bay, Japan. Eur J Phycol 43(4):395–411CrossRefGoogle Scholar
  138. Shoden S, Ikeda T, Yamaguchi A (2005) Vertical distribution, population structure and lifecycle of Eucalanus bungii (Copepoda: Calanoida) in the Oyashio region, with notes on its regional variations. Mar Biol 146(3):497–511CrossRefGoogle Scholar
  139. Sichlau MH, Hansen JLS, Andersen TJ, Hansen BW (2011) Distribution and mortality of diapause eggs from calanoid copepods in relation to sedimentation regimes. Mar Biol 158(3):665–676CrossRefGoogle Scholar
  140. Sim M (2010) Plankton bloom hits Pulau Ubin fish farms. The Straits Times, SingaporeGoogle Scholar
  141. Smayda TJ (1997) Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153CrossRefGoogle Scholar
  142. Smayda TJ (1998) Ecophysiology and bloom dynamics of Heterosigma akashiwo (Raphidophyceae). In: Anderson DM, Cembella AD, Hallegraef GM (eds) Physiological ecology of harmful algal blooms. Springer, BerlinGoogle Scholar
  143. Spencer M, Blaustein L (2001) Risk of predation and hatching of resting eggs in the ostracod Heterocypris incongruens. J Crustace Biol 21(3):575–581CrossRefGoogle Scholar
  144. Steele DH, Steele VJ (1972) The biology of Jaera spp. (Crustacea, Isopoda). In the northwestern Atlantic. 1. Jaerai ischiosetosa. Can J Zool 50:205–211CrossRefGoogle Scholar
  145. Steele VJ (1967) Resting stage in the reproductive cycles of Gammarus. Nature 214:1034CrossRefGoogle Scholar
  146. Tan TH, Leaw CP, Leong SCY, Lim LP, Chew SM, Teng ST, Lim PT (2016) Marine micro-phytoplankton of Singapore, with a review of harmful microalgae in the region. Raffles Bull Zool Suppl 34:78–96Google Scholar
  147. Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003) A plea for DNA taxonomy. Trends Ecol Evol 18:70–74CrossRefGoogle Scholar
  148. Tazioli S, Di Camillo CG (2013) Ecological and morphological characteristics of Ephelota gemmipara (Ciliophora, Suctoria), epibiontic on Eudendrium racemosum (Cnidaria, Hydrozoa) from the Adriatic Sea. European. J Protistol 49(4):590–599CrossRefGoogle Scholar
  149. Tham AK (1953) The plankton calendar of Singapore Straits with suggestions for a simplified methodology. Marine Biological Association of India, Special Issue 60–73Google Scholar
  150. Tham AK (1973) The sea. In: Chuang SH (ed) Animal life and nature in Singapore. Singapore University Press, Singapore, p 140–149Google Scholar
  151. Throndsen J (1996) The planktonic marine flagellates. In: Tomas CR (ed) Identifying marine phytoplankton. Academic Press, San Diego, pp 591–730Google Scholar
  152. Tiffany MA, Gonzalez MR, Swan BK, Reifel KM, Watts JM, Hurlbert SH (2007) Phytoplankton dynamics in the Salton Sea, California, 1997-1999. Lake Reserv Manag 23(5):582–605CrossRefGoogle Scholar
  153. Traag BA, Pugliese A, Eisen JA, Losick R (2013) Gene conservation among endospore-forming bacteria reveals additional sporulation genes in Bacillus subtilis. J Bacteriol 2013:253–260CrossRefGoogle Scholar
  154. Trujillo-Ortiz A, Burton RS, De La Rosa-Velez. J, Correa-Sandoval F (1995) Genetic variation in two populations of the marine calanoid copepod Acartia californiensis Trinast. Cienc Mar 21(1):39–58CrossRefGoogle Scholar
  155. Tsukazaki C, Ishii K-I, Saito R, Matsuno K, Yamaguchi A, Imai I (2013) Distribution of viable diatom resting stage cells in bottom sediments of the eastern Bering Sea shelf. Deep-Sea Res Part II 94:22–30CrossRefGoogle Scholar
  156. UNCTAD (ed) (2012) United Nation Conference on trade and development. Review of maritime transport. United Nation Publication. GenevaGoogle Scholar
  157. Uye S (1985) Resting egg production as a life history strategy of marine planktonic copepods. Bull Mar Sci 37(2):440–449Google Scholar
  158. Uye S, Kasahara S, Onbe T (1979) Calanoid copepod eggs in sea-bottom muds .4. Effects of some environmental-factors Hatching resting eggs. Mar Biol 51(2):151–156Google Scholar
  159. Walker GK, Maugel TK (1980) Encystment and excystement in hypotrich ciliates. II Diophrys scutum and remarks on comparative features. Protistologica 16:525–531Google Scholar
  160. Watson MW (1975) Flagellar apparatus, eyespot and behavior of Microthamnion-kuetzingianum (chlorophyceae) zoospores. J Phycol 11(4):439–448Google Scholar
  161. West GS (2010) Algae: Volume 1, Myxophyceae, Peridinieae, Bacillarieae, Chlorphyceae. Press CU, (ed) Cambridge University Press, New York, NY. p 490Google Scholar
  162. Yamaguchi A, Watanabe Y, Ishida H, Harimoto T, Furusawa K, Suzuki S, Ishizaka J, Ikeda T, Masayuki MT (2002) Community and trophic structures of pelagic copepods down to greater depths in the western subarctic Pacific (WEST-COSMIC). Deep-Sea Res Part I 49(6):1007–1025CrossRefGoogle Scholar
  163. Yamamoto Y, Nakahara H (2009) Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 10(3):185–193CrossRefGoogle Scholar
  164. Zillioux EJ, Gonzalez JG (1972) Egg dormancy in a neretic calanoid copepod and its implications to overwintering in boreal waters. 5th European marine biology symposium, In: Bruno Battaglia (ed) Venice, pp 217–230Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Aurore Trottet
    • 1
    Email author return OK on get
  • Bryan Wilson
    • 2
  • Genevieve Sew Wei Xin
    • 1
    • 3
  • Christaline George
    • 1
  • Lemuel Casten
    • 1
  • Claire Schmoker
    • 1
  • Nurul Syazana Binte Modh Rawi
    • 1
  • Moon Chew Siew
    • 1
  • Ole Larsen
    • 1
  • Hans S. Eikaas
    • 1
  • Karenne Tun
    • 4
  • Guillaume Drillet
    • 1
  1. 1.DHI Water and Environment-SingaporeSingaporeSingapore
  2. 2.Marine Microbiology Research Group, Department of BiologyUniversity of BergenBergenNorway
  3. 3.Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  4. 4.National Parks BoardSingaporeSingapore

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