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Development of a thin diatom layer observed in a stratified embayment in Japan

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Abstract

The temporal evolution of a thin phytoplankton layer was observed by field measurements using a research vessel and mooring instruments in the Yatsushiro Sea, a semi-enclosed narrow embayment in Japan, in early August 2013. The subsurface chlorophyll maximum developed into a thin layer within 2 days just below the pycnocline at around 10-m depth, where turbulent mixing (the dissipation rate of turbulent kinetic energy) was weak (low). The layer persisted for 1.5 to 2 days and declined after irradiance drastically decreased at the sea surface. At the peak period, the layer thickness, which is defined as the full-width at half-maximum of the peak in chlorophyll a concentration, ranged from 0.6 to 1.4 m, and the maximum concentration reached 42.3 mg m−3. The horizontal extent of the layer was approximately 10 km along the longitudinal axis of the bay. The phytoplankton population characterized by the layer was dominated by a chain-forming centric diatom, Chaetoceros spp. The formation mechanisms of the thin diatom layer were investigated using the observed data and a vertical one-dimensional model that includes physical and biological processes. The results suggest that the development of the thin layer was caused by in situ growth and aggregation due to nutrient-dependent sinking of the species under weak turbulence. The study highlights that continuous multidisciplinary observations and understanding species-specific physiological responses to environmental variations are necessary to elucidate drastically fluctuating phytoplankton dynamics in a coastal water.

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References

  • Anderson LW, Sweeney BM (1978) Role of inorganic ions in controlling sedimentation rate of a marine centric diatom Ditylum brightwelli. J Phycol 14:204–214

    Article  Google Scholar 

  • Barton AD, Dutkiewicz S, Flierl G, Bragg J, Follows MJ (2010) Patterns of diversity in marine phytoplankton. Science 327:1509–1511

    Article  Google Scholar 

  • Benoit-Bird KJ, Moline MA, Waluk CM, Robbins IC (2010) Integrated measurements of acoustical and optical thin layers I: vertical scales of association. Cont Shelf Res 30:17–28

    Article  Google Scholar 

  • Berdalet E, McManus MA, Ross ON, Burchard H, Chavez FP, Jaffe JS, Jenkinson IR, Kudela R, Lips I, Lips U, Lucas A, Rivas D, Ruiz-de la Torre MC, Ryan J, Sullivan JM, Yamazaki H (2014) Understanding harmful algae in stratified systems: review of progress and future directions. Deep-Sea Res II 101:4–20

    Article  Google Scholar 

  • Bienfang PK, Harrison PJ (1984) Sinking-rate response of natural assemblages of temperate and subtropical phytoplankton to nutrient depletion. Mar Biol 83:293–300

    Article  Google Scholar 

  • Bienfang PK, Harrison PJ, Quarmby LM (1982) Sinking rate response to depletion of nitrate, phosphate and silicate in four marine diatoms. Mar Biol 67:295–302

    Article  Google Scholar 

  • Bienfang P, Szyper J, Laws E (1983) Sinking rate and pigment responses to light-limitation of a marine diatom-implications to dynamics of chlorophyll maximum layers. Oceanol Acta 6:55–62

    Google Scholar 

  • Birch DA, Young WR, Franks PJS (2008) Thin layers of plankton: formation by shear and death by diffusion. Deep-Sea Res I 55:277–295

    Article  Google Scholar 

  • Cheriton OM, McManus MA, Stacy MT, Steinbuck JV (2009) Physical and biological controls on the maintenance and dissipation of a thin phytoplankton layer. Mar Ecol Prog Ser 378:55–69

    Article  Google Scholar 

  • Churnside JH, Donaghay PL (2009) Thin scattering layers observed by airborne lidar. ICES J Mar Sci 66:778–789

    Article  Google Scholar 

  • Conway HL, Harrison PJ (1977) Marine diatoms grown in chemostats under silicate or ammonium limitation. IV. Transient response of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida to a single addition of the limiting nutrient. Mar Biol 43:33–43

    Article  Google Scholar 

  • Cowles TJ, Desiderio RA, Carr ME (1998) Small-scale planktonic structure: persistence and trophic consequences. Oceanogr 11:4–9

    Article  Google Scholar 

  • Cullen JJ (2015) Subsurface chlorophyll maximum layers: enduring enigma or mystery solved? Ann Rev Mar Sci 7:207–239

    Article  Google Scholar 

  • Culver ME, Smith WO (1989) Effects of environmental variation on sinking rates of marine phytoplankton. J Phycol 25:262–270

    Article  Google Scholar 

  • d’Ovidio F, De Monte S, Alvain S, Dandonneau Y, Levy M (2010) Fluid dynamical niches of phytoplankton types. Proc Natl Acad Sci USA 107:18366–18370

    Article  Google Scholar 

  • Dekshenieks MM, Donaghay PL, Sullivan JM, Rines JE, Osborn TR, Twardowski MS (2001) Temporal and spatial occurrence of thin phytoplankton layers in relation to physical processes. Mar Ecol Prog Ser 223:61–71

    Article  Google Scholar 

  • Durham WM, Stocker R (2012) Thin phytoplankton layers: characteristics, mechanisms, and consequences. Ann Rev Mar Sci 4:177–207

    Article  Google Scholar 

  • Endoh T, Matsuno T, Yoshikawa Y, Tatsuyama Y, Ishizaka J (2009) Observations of wind driven deepening of the surface mixing layer in the Tsushima Strait. J Oceanogr 65:273–279

    Article  Google Scholar 

  • Eppley RW, Holmes RW, Strickland JD (1967) Sinking rates of marine phytoplankton measured with a fluorometer. J Exp Mar Biol Ecol 1:191–208

    Article  Google Scholar 

  • Farrell H, Gentien P, Fernand L, Lazure P, Lunven M, Youenou A, Reguera B, Raine R (2014) Vertical and horizontal controls of a haptophyte thin layer in the Bay of Biscay, France. Deep-Sea Res II 101:80–94

    Article  Google Scholar 

  • Finenko ZZ, Krupatkina-Akinina DK (1974) Effect of inorganic phosphorus on the growth rate of diatoms. Mar Biol 26:193–201

    Article  Google Scholar 

  • Franks PJS (1995) Thin layers of phytoplankton: a model of formation by near-ineartial wave shear. Deep-Sea Res I 42:75–91

    Article  Google Scholar 

  • Furnas MJ (1990) In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates. J Plankton Res 12:1117–1151

    Article  Google Scholar 

  • Gentien P, Luven M, Lehaître M, Duvent JL (1995) In situ depth profiling of particle sizes. Deep-Sea Res I 42:1297–1312

    Article  Google Scholar 

  • Harrison PJ, Conway HL, Holmes RW, Davis CO (1977) Marine diatoms grown in chemostats under silicate or ammonium limitation. III. Cellular chemical composition and morphology of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida. Mar Biol 43:19–31

    Article  Google Scholar 

  • Hirota R, Hara M (1975) Zooplankton investigations in Yatsushirokai, western Kyushu, I: regional and seasonal occurrences of the important zooplankton. J Oceanogr Soc Jpn 31:115–123

    Article  Google Scholar 

  • Hodges BA, Fratantoni DM (2009) A thin layer of phytoplankton observed in the Philippine Sea with a synthetic moored array of autonomous gliders. J Geophys Res 114:C10020. https://doi.org/10.1029/2009JC005317

    Article  Google Scholar 

  • Justić D, Rabalais NN, Turner RE, Dortch Q (1995) Changes in nutrient structure of river-dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuar Coast Shelf Sci 40:339–356

    Article  Google Scholar 

  • Lomas MW, Glibert PM (2000) Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J Phycol 36:903–913

    Article  Google Scholar 

  • Masunaga E, Yamazaki H (2014) A new tow-yo instrument to observe high-resolution coastal phenomena. J Mar Syst 129:425–436

    Article  Google Scholar 

  • McManus MA, Alldredge AL, Barnard AH, Boss E, Case JF, Cowles TJ, Donaghay PL, Eisner LB, Gifford DJ, Greenlaw CF, Herren CM, Holliday DV, Johnson D, MacIntyre S, McGehee DM, Osborn TR, Perry MJ, Pieper RE, Rines JEB, Smith DC, Sullivan JM, Talbot MK, Twardowski MS, Weidemann A, Zaneveld JR (2003) Characteristics, distribution and persistence of thin layers over a 48 hour period. Mar Ecol Prog Ser 261:1–19

    Article  Google Scholar 

  • Menden-Deuer S (2008) Spatial and temporal characteristics of plankton-rich layers in a shallow, temperate fjord. Mar Ecol Prog Ser 355:21–30

    Article  Google Scholar 

  • Miyamura K (2016) Population dynamics, prediction and countermeasures of Karenia mikimotoi red tides. In: Imai I, Yamaguchi M, Matsuoka K (eds) Advances in harmful algal bloom research. Koseisha-Koseikaku Co., Ltd., Tokyo, pp 191–200 (in Japanese)

    Google Scholar 

  • Murata K, Sakurada K (2009) The growth environment and reaction to Cochlodinium polykrikoides red tides in the Yatsushiro Sea. Bull Plankton Soc Jpn 56:52–55 (in Japanese with English abstract)

    Google Scholar 

  • Onitsuka G, Aoki K, Shimizu M (2015) Meteorological conditions preceding Chattonella bloom events in the Yatsushiro Sea, Japan, and possible links with the East Asian monsoon. Fish Sci 81:123–130

    Article  Google Scholar 

  • Onitsuka G, Shikata T, Kitatsuji S, Abe K, Yamamoto T, Ochiai H, Matsuo H (2016) Factors influencing maintenance and decline of a diatom bloom in the Yatsushiro Sea, Japan. J Oceanogr 72:617–627

    Article  Google Scholar 

  • Osborn TR (1980) Estimates of the local rate of vertical diffusion from dissipation measurements. J Phys Oceanogr 10:83–89

    Article  Google Scholar 

  • Parsons TR, Takahashi M, Hargrave B (1984) Biological oceanographic processes, 3rd edn. Pergamon Press, Oxford, p 330

    Google Scholar 

  • Prairie JC, Franks PJ, Jaffe JS, Doubell MJ, Yamazaki H (2011) Physical and biological controls of vertical gradients in phytoplankton. Limnol Oceanogr Fluids Environ 1:75–90

    Article  Google Scholar 

  • Richardson TL, Cullen JJ (1995) Changes in buoyancy and chemical composition during growth of a coastal marine diatom: ecological and biogeochemical consequences. Mar Ecol Prog Ser 128:77–90

    Article  Google Scholar 

  • Rines JEB, Donaghay PL, Dekshenieks MM, Sullivan JM, Twardowski MS (2002) Thin layers and camouflage: hidden Pseudo-nitzschia spp. (Bacillariophyceae) populations in a fjord in the San Juan Islands, Washington, USA. Mar Ecol Prog Ser 225:123–137

    Article  Google Scholar 

  • Rines JEB, McFarland MN, Donaghay PL, Sullivan JM (2010) Thin layers and species-specific characterization of the phytoplankton community in Monterey Bay, California, USA. Cont Shelf Res 30:66–80

    Article  Google Scholar 

  • Ríos F, Kilian R, Mutschke E (2016) Chlorophyll-a thin layers in the Magellan fjord system: the role of the water column stratification. Cont Shelf Res 124:1–12

    Article  Google Scholar 

  • Ryan JP, McManus MA, Paduan JD, Chavez FP (2008) Phytoplankton thin layers caused by shear in frontal zones of a coastal upwelling system. Mar Ecol Prog Ser 354:21–34

    Article  Google Scholar 

  • Ryan JP, McManus MA, Sullivan JM (2010) Interacting physical, chemical and biological forcing of phytoplankton thin-layer variability in Monterey Bay, California. Cont Shelf Res 30:7–16

    Article  Google Scholar 

  • Sakurada K, Kino S, Oyama N, Itoyama R (2007) The occurrence situation of harmful plankton in Yatsushiro Sea and a trial of prediction of blooming. Rep Kumamoto Pref Fish Res Cent 7:31–44 (in Japanese)

    Google Scholar 

  • Sarthou G, Timmermans KR, Blain S, Treguer P (2005) Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42

    Article  Google Scholar 

  • Shikata T, Sakurada K, Jomoto Y, Onji M, Yoshida M, Ohwada K (2010) Effects of temperature, salinity and light irradiance on phytoplankton growth in the Yatsushiro Sea. Nippon Suisan Gakk 76:34–45 (in Japanese with English abstract)

    Article  Google Scholar 

  • Shikata T, Onitsuka G, Abe K, Kitatsuji S, Yufu K, Yoshikawa Y, Honjo T, Miyamura K (2017) Relationships between light environment and subsurface daytime orientation in the red-tide dinoflagellate Karenia mikimotoi. Mar Biol 164:18

    Article  Google Scholar 

  • Shroyer EL, Benoit-Bird K, Nash JD, Moum JN (2014) Stratification and mixing regimes in biological thin layers over the Mid-Atlantic Bight. Limnol Oceanogr 59:1349–1363

    Article  Google Scholar 

  • Smayda TJ (1970) The suspension and sinking of phytoplankton in the sea. Oceanogr Mar Biol Ann Rev 8:353–414

    Google Scholar 

  • Spilling K, Tamminen T, Andersen T, Kremp A (2010) Nutrient kinetics modeled from time series of substrate depletion and growth: dissolved silicate uptake of Baltic Sea spring diatoms. Mar Biol 157:427–436

    Article  Google Scholar 

  • Stacey MT, McManus MA, Steinbuck JV (2007) Convergences and divergences and thin layer formation and maintenance. Limnol Oceanogr 52:1523–1532

    Article  Google Scholar 

  • Steele JH, Yentsch CS (1960) The vertical distribution of chlorophyll. J Mar Biol Assoc UK 39:217–226

    Article  Google Scholar 

  • Steinbuck JV, Stacey MT, McManus MA, Cheriton OM, Ryan JP (2009) Observations of turbulent mixing in a phytoplankton thin layer: implications for formation, maintenance, and breakdown. Limnol Oceanogr 54:1353–1368

    Article  Google Scholar 

  • Steinbuck JV, Genin A, Monismith SG, Koseff JR, Holzman R, Labiosa RG (2010) Turbulent mixing in fine-scale phytoplankton layers: observations and inferences of layer dynamics. Cont Shelf Res 30:442–455

    Article  Google Scholar 

  • Strickland JDH (1960) Measuring the production of marine phytoplankton. Bull Fish Res Bd Can 122:1–172

    Google Scholar 

  • Sullivan JM, Donaghay PL, Rines JE (2010a) Coastal thin layer dynamics: consequences to biology and optics. Cont Shelf Res 30:50–65

    Article  Google Scholar 

  • Sullivan JM, McManus MA, Cheriton OM, Benoit-Bird KJ, Goodman L, Wang Z, Ryan JP, Stacey M, Greenlaw C, Moline MA (2010b) Layered organization in the coastal ocean: an introduction to planktonic thin layers and the LOCO project. Cont Shelf Res 30:1–6

    Article  Google Scholar 

  • Takikawa K, Tanaka K, Mori E, Watanabe K, Hokamura T, Aoyama C (2004) Factorial analysis of environmental variables over Yatsushiro-Sea. Annual J Coast Eng JSCE 51:916–920 (in Japanese with English abstract)

    Google Scholar 

  • Timmerman AH, McManus MA, Cheriton OM, Cowen RK, Greer AT, Kudela RM, Sevadjian J (2014) Hidden thin layers of toxic diatoms in a coastal bay. Deep-Sea Res II 101:129–140

    Article  Google Scholar 

  • Tomaru Y, Fujii N, Oda S, Toyoda K, Nagasaki K (2011) Dynamics of diatom viruses on the western coast of Japan. Aquat Microb Ecol 63:223–230

    Article  Google Scholar 

  • Tsuruta A, Ueno S, Ohgai M, Yamada M (1986) Study on the seasonal and horizontal distributions of phytoplankton communities in Yatsushiro Sea, using a cluster analysis. Nippon Suisan Gakk 52:1947–1955 (in Japanese with English abstract)

    Article  Google Scholar 

  • Tsutsumi E, Matsuno T (2012) Observations of turbulence under weakly and highly stratified conditions in the Ariake Sea. J Oceanogr 68:369–386

    Article  Google Scholar 

  • Valle-Levinson A, Huguenard K, Ross L, Branyon J, MacMahan J, Reniers A (2015) Tidal and nontidal exchange at a subtropical inlet: destin Inlet, Northwest Florida. Estuar Coast Shelf Sci 155:137–147

    Article  Google Scholar 

  • Velo-Suárez L, González-Gil S, Gentien P, Lunven M, Bechemin C, Fernand L, Raine R, Reguera B (2008) Thin layers of Pseudo-nitzschia spp. and the fate of Dinophysis acuminata during an upwelling-downwelling cycle in a Galician Ría. Limnol Oceanogr 53:1816–1834

    Article  Google Scholar 

  • Velo-Suárez L, Fernand L, Gentien P, Reguera B (2010) Hydrodynamic conditions associated with the formation, maintenance and dissipation of a phytoplankton thin layer in a coastal upwelling system. Cont Shelf Res 30:193–202

    Article  Google Scholar 

  • Waite A, Bienfang PK, Harrison PJ (1992a) Spring bloom sedimentation in a subarctic ecosystem I. Nutrient sensitivity. Mar Biol 114:119–129

    Google Scholar 

  • Waite AM, Thompson PA, Harrison PJ (1992b) Does energy control the sinking rates of marine diatoms? Limnol Oceanogr 37:468–477

    Article  Google Scholar 

  • Waite A, Fisher A, Thompson PA, Harrison PJ (1997) Sinking rate versus cell volume relationships illuminate sinking rate control mechanisms in marine diatoms. Mar Ecol Prog Ser 157:97–108

    Article  Google Scholar 

  • Wang Z, Goodman L (2010) The evolution of a thin phytoplankton layer in strong turbulence. Cont Shelf Res 30:104–118

    Article  Google Scholar 

  • Wolk F, Yamazaki H, Seuront L, Lueck RG (2002) A new free-fall profiler for measuring biophysical microstructure. J Atmos Ocean Technol 19:780–793

    Article  Google Scholar 

  • Yamasaki Y, Ohmichi Y, Shikata T, Hirose M, Shimasaki Y, Oshima Y, Honjo T (2010) Species-specific allelopathic effects of the diatom Skeletonema costatum. Thalassas 27:21–32

    Google Scholar 

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Acknowledgements

The authors thank the captains and crews of R/V Shirafuji-maru for their cooperation in conducting the field observation. The authors also thank S. Kitatsuji for providing information about predators. The data by the mooring system at Stn. A were obtained with funding from the Japan Fisheries Agency-commissioned project for addressing red tides and oxygen-depleted water masses. The work was supported in part by the grant from JSPS KAKENHI Grant number 25340024, and by the Collaborative Research Program of Research Institute for Applied Mechanics, Kyushu University.

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Onitsuka, G., Yoshikawa, Y., Shikata, T. et al. Development of a thin diatom layer observed in a stratified embayment in Japan. J Oceanogr 74, 351–365 (2018). https://doi.org/10.1007/s10872-018-0466-0

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