Thin phytoplankton layers: Characteristics, mechanisms, and consequences

Annual Review of Marine Science

Volumn 4, Issue , 2012, Pages 177-207

  Durham, William M ^a   Stocker, Roman ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

hydrodynamic shear; marine ecology; phytoplankton motility; trophic hotspot; turbulent dispersion

Indexed keywords

CELL BEHAVIORS; COMPLEX LINKAGES; FIELD OBSERVATIONS; HYDRODYNAMIC SHEAR; LAYER FORMATION; MARINE ECOLOGY; PHYSICAL ENVIRONMENTS; PHYSICAL PROCESS; THIN LAYERS; TROPHIC HOTSPOT; TROPHIC LEVEL; TURBULENT DISPERSION;

DISPERSIONS; ECOLOGY; PHYTOPLANKTON;

ALGAE CONTROL;

FIELD METHOD; HYDRODYNAMICS; MARINE ECOSYSTEM; MOTILITY; PERSISTENCE; PHOTOSYNTHESIS; PHYTOPLANKTON; TROPHIC LEVEL;

ARTICLE; DEMOGRAPHY; ECOSYSTEM; ENVIRONMENTAL MONITORING; PHYSIOLOGY; PHYTOPLANKTON; TROPIC CLIMATE;

DEMOGRAPHY; ECOSYSTEM; ENVIRONMENTAL MONITORING; PHYTOPLANKTON; TROPICAL CLIMATE;

EID: 83655202580     PISSN: 19411405     EISSN: 19410611     Source Type: Journal    
DOI: 10.1146/annurev-marine-120710-100957     Document Type: Article

References (121)

1. Alldredge AL, Cowles TJ, MacIntyre S, Rines JEB, Donaghay PL, et al. 2002. Occurrence and mechanisms of formation of a dramatic thin layer of marine snow in a shallow Pacific fjord. Mar. Ecol. Prog. Ser. 233:1-12
2. Armi L. 1978. Some evidence for boundary mixing in the deep ocean. J. Geophys. Res. 83:1971-79
3. Baek SH, Shimode S, Shin K, Han MS, Kikuchi T. 2009. Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: The role of vertical migration and cell division. Harmful Algae 8:843-56
4. Benoit-Bird KJ. 2009. Dynamic 3-dimensional structure of thin zooplankton layers is impacted by foraging fish. Mar. Ecol. Prog. Ser. 396:61-76
5. Benoit-Bird KJ, Cowles TJ, Wingard CE. 2009. Edge gradients provide evidence of ecological inter- actions in planktonic thin layers. Limnol. Oceanogr. 54: 1382-92
6. 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
7. Birch DA, Young WR ,Franks PJS. 2008. Thin layers of plankton: Formation by shear and death by diffusion. Deep-Sea Res. Part I 55: 277-95
8. Birch DA, Young WR, Franks PJS. 2009. Plankton layer profiles as determined by shearing, sinking, and swimming. Limnol. Oceanogr. 54:397-99
9. Bjornsen PK, Nielsen TG. 1991. Decimeter scale heterogeneity in the plankton during a pycnocline bloom of Gyrodinium aureolum. Mar. Ecol. Prog. Ser. 73:263-67
10. Bollens SM,Rollwagen-Bollens G, Quenette JA, Bochdansky AB. 2011. Cascadingmigrations and implications for vertical fluxes in pelagic ecosystems. J. Plankton Res. 33:349-55
11. Bracco A, Provenzale A, Scheuring I. 2000. Mesoscale vortices and the paradox of the plankton. Proc. R. Soc. B 267:1795-1800
12. Brahamsha B. 1999. Non-flagellar swimming in marine Synechococcus. J. Mol. Microbiol. Biotechnol. 1:59-62
13. Calbet A, Landry MR. 2004. Phytoplankton growth,microzooplankton grazing, and carbon cycling inmarine systems. Limnol. Oceanogr. 49:51-57
14. Cheriton OM,McManus MA, StaceyMT, Steinbuck JV. 2009. Physical and biological controls on the maintenance and dissipation of a thin phytoplankton layer. Mar. Ecol. Prog. Ser. 378:55-69
15. Cheriton OM, McManus MA, Steinbuck JV, Stacey MT, Sullivan JM. 2010. Towed vehicle observations of thin layer structure and a low-salinity intrusion in Northern Monterey Bay, CA. Cont. Shelf Res. 30:39-49
16. Churnside JH, Donaghay PL. 2009. Thin scattering layers observed by airborne lidar. ICES J. Mar. Sci. 66:778-89
17. Clift R, Grace JR,Weber ME. 1978. Bubbles, Drops, and Particles. New York: Academic
18. Cowles TJ. 2004. Planktonic layers: Physical and biological interactions on the small-scale. In Handbook of ScalingMethods in Aquatic Ecology:Measurement, Analysis, Simulation, ed. L Seuront, PG Strutton, pp. 31- 49. Boca Raton, FL: CRC
19. Cowles TJ, Desiderio RA, Carr ME. 1998. Small-scale planktonic structure: Persistence and trophic consequences. Oceanography 11:4-9
20. Cullen JJ. 1982. The deep chlorophyll maximum: Comparing vertical profiles of chlorophyll a. Can. J. Fish. Aquat. Sci. 39:791-803
21. Dekshenieks MM, Donaghay PL ,Sullivan JM, Rines JEB, 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
22. Donaghay PL, Osborn TR. 1997. Toward a theory of biological-physical control of harmful algal bloom dynamics and impacts. Limnol. Oceanogr. 42:1283-96
23. Donaghay PL, Rines HM, Sieburth JM. 1992. Simultaneous sampling of fine scale biological, chemical, and physical structure in stratified waters. Arch. Hydrobiol. Beih. 36:97-108
24. Doucette GJ, Harrison PJ. 1990. Some effects of iron and nitrogen stress on the red tide dinoflagellate Gymnodinium sanguineum. Mar. Ecol. Prog. Ser. 62:293-306
25. Drescher K, Leptos KC, Tuval I, Ishikawa T, Pedley TJ, Goldstein RE. 2009. Dancing Volvox: Hydrodynamic bound states of swimming algae. Phys. Rev. Lett. 102:168101
26. Durham WM, Climent E, Stocker R. 2011. Gyrotaxis in a steady vortical flow. Phys. Rev. Lett. 106:238102
27. Durham WM, Kessler JO, Stocker R. 2009. Disruption of vertical motility by shear triggers formation of thin phytoplankton layers. Science 323: 1067-70
28. Eckart C. 1948. An analysis of the stirring andmixing processes in incompressible fluids. J. Mar. Res. 7:265-75
29. Eppley RW, Holmes RW, Strickland JDH. 1967. Sinking rates of marine phytoplankton measured with a fluorometer. J. Exp. Mar. Biol. Ecol. 1:191-208
30. Fauchot J, Levasseur M, Roy S. 2005. Daytime and nighttime vertical migrations of Alexandrium tamarense in the St. Lawrence estuary (Canada). Mar. Ecol. Prog. Ser. 296:241-50
31. Fenchel T. 2001. How dinoflagellates swim. Protist 152:329-38
32. Fischer HB, List EJ, Koh RCY, Imberger J, Brooks NH. 1979. Mixing in Inland and Coastal Waters. New York: Academic
33. Franks PJS. 1995. Thin-layers of phytoplankton: A model of formation by near-inertial wave shear. Deep-Sea Res. Part I 42:75-91
34. Franks PJS. 1997. Models of harmful algal blooms. Limnol. Oceanogr. 42:1273-82
35. Gallager SM, Yamazaki H, Davis CS. 2004. Contribution of fine-scale vertical structure and swimming behavior to formation of plankton layers on Georges Bank. Mar. Ecol. Prog. Ser. 267:27-43
36. Gentien P, Donaghay PL, Yamazaki H, Raine R, Reguera B, Osborn T. 2005. Harmful algal blooms in stratified environments. Oceanography 18:172-83
37. Gjosaeter J, Lekve K, Stenseth NC, Leinaas HP, Christie H, et al. 2000. A long-term perspective on the Chrysochromulina bloom on the Norwegian Skagerrak coast 1988: A catastrophe or an innocent incident? Mar. Ecol. Prog. Ser. 207:201-18
38. Gross F, Zeuthen E. 1948. The buoyancy of plankton diatoms: A problem of cell physiology. Proc. R. Soc. Lond. Ser. B 135:382-89
39. Grünbaum D. 2009. Peter principle packs a peck of phytoplankton. Science 323:1022-23
40. Guasto JS, Rusconi R, Stocker R. 2012. Fluidmechanics of planktonic microorganisms. Annu. Rev. FluidMech. 44:1-28
41. Harder W. 1968. Reactions of plankton organisms to water stratification. Limnol. Oceanogr. 13:156-68
42. Harvey EL, Menden-Deuer S. 2011. Avoidance, movement, andmortality: The interactions between a protistan grazer and Heterosigma akashiwo, a harmful algal bloom species. Limnol. Oceanogr. 56:371-78
43. Heil CA, Glibert PM, Fan CL. 2005. Prorocentrum minimum (Pavillard) Schiller: A review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4:449-70
44. Hill NA, Häder DP. 1997. A biased random walk model for the trajectories of swimming micro-organisms. J. Theor. Biol. 186:503-26
45. 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
46. Holliday DV, Pieper RE, Greenlaw CF, Dawson JK. 1998. Acoustical sensing of small-scale vertical structures in zooplankton assemblages. Oceanography 11:18-23
47. Hutchinson GE. 1961. The paradox of the plankton. Am. Nat. 95:137-45
48. Ivey GN. 1987. Boundary mixing in a rotating stratified fluid. J. Fluid Mech. 183:25-44
49. Jester R, Lefebvre K, Langlois G, Vigilant V, Baugh K, Silver MW. 2009. A shift in the dominant toxinproducing algal species in central California alter phycotoxins in food webs. Harmful Algae 8:291-98
50. Johnston TMS, Cheriton OM, Pennington JT, Chavez FP. 2009. Thin phytoplankton layer formation at eddies, filaments, and fronts in a coastal upwelling zone. Deep-Sea Res. Part II 56:246-59
51. Johnston TMS, Rudnick DL. 2009. Observations of the transition layer. J. Phys. Oceanogr. 39:780-97
52. Kamykowski D, Reed RE, Kirkpatrick GJ. 1992. Comparison of sinking velocity, swimming velocity, rotation, and path characteristics among six marine dinoflagellate species. Mar. Biol. 113:319-28
53. Kamykowski D, YamazakiH. 1997. A study of metabolism-influenced orientation in the diel vertical migration of marine dinoflagellates. Limnol. Oceanogr. 42:1189-202
54. Karp-Boss L, Boss E, Jumars PA. 2000. Motion of dinoflagellates in a simple shear flow. Limnol. Oceanogr. 45:1594-602
55. Kasai A, Kurikawa Y, Ueno M, Robert D, Yamashita Y. 2010. Salt-wedge intrusion of seawater and its implication for phytoplankton dynamics in the Yura Estuary, Japan. Estuar. Coast. Shelf Sci. 86:408-14
56. Kessler JO. 1985. Hydrodynamic focusing of motile algal cells. Nature 313:218-20
57. Koukaras K, Nikolaidis G. 2004. Dinophysis blooms in Greek coastal waters (Thermaikos Gulf, NWAegean Sea). J. Plankton Res. 26:445-57
58. Kudela RM, Seeyave S, Cochlan WP. 2010. The role of nutrients in regulation and promotion of harmful algal blooms in upwelling systems. Prog. Oceanogr. 85:122-35
59. Kundu PK, Cohen IM. 2004. Fluid Mechanics. San Diego: Elsevier. 3rd ed.
60. Lasker R. 1975. Field criteria for survival of anchovy larvae: Relation between inshore chlorophyll maximum layers and successful first feeding. Fish. Bull. 73:453-62
61. Lebert M, Häder DP. 1996. How Euglena tells up from down. Nature 379:590
62. Lévy M. 2008. The modulation of biological production by oceanic mesoscale turbulence. In Transport and Mixing in Geophysical Flows, ed. JB Weiss, A Provenzale, pp. 219-261. Lect. Notes Phys. 744. Berlin: Springer-Verlag
63. MacIntyre JG, Cullen JJ, Cembella AD. 1997. Vertical migration, nutrition and toxicity in the dinoflagellate Alexandrium tamarense. Mar. Ecol. Prog. Ser. 148:201-16
64. MacKinnon JA, Gregg MC. 2003. Mixing on the late-summer New England shelf-solibores, shear, and stratification. J. Phys. Oceanogr. 33:1476-92
65. Marcos, Seymour J, Luhar M, Durham WM, Mitchell JG, et al. 2011. Microbial alignment in flow changes ocean light climate. Proc. Natl. Acad. Sci. USA 108:3860-64
66. McCarren J, Brahamsha B. 2009. Swimming motility mutants of marine Synechococcus affected in production and locations of the S-layer protein swmA. J. Bacteriol. 191:1111-14
67. McManus MA, Alldredge AL, Barnard AH, Boss E, Case JF, et al. 2003. Characteristics, distribution and persistence of thin layers over a 48 hour period. Mar. Ecol. Prog. Ser. 261:1-19
68. McManusMA, Kudela RM, Silver MW, Steward GF, Donaghay PL, Sullivan JM. 2008. Cryptic blooms: Are thin layers the missing connection? Estuar. Coasts 31:396-401
69. McPhee-Shaw E. 2006. Boundary-interior exchange: Reviewing the idea that internal-wave mixing enhances lateral dispersal near continental margins. Deep-Sea Res. Part II 53:42-59
70. Menden-Deuer S. 2008. Spatial and temporal characteristics of plankton-rich layers in a shallow, temperate fjord. Mar. Ecol. Prog. Ser. 355:21-30
71. Menden-Deuer S, Fredrickson K. 2010. Structure-dependent, protistan grazing and its implication for the formation, maintenance and decline of plankton patches. Mar. Ecol. Prog. Ser. 420:57-71
72. Menden-Deuer S, Grünbaum D. 2006. Individual foraging behaviors and population distributions of a planktonic predator aggregating to plankton thin layers. Limnol. Oceanogr. 51:109-16
73. Mitchell JG, Yamazaki H, Seuront L, Wolk F, Li H. 2008. Phytoplankton patch patterns: Seascape anatomy in a turbulent ocean. J. Mar. Syst. 69:247-53
74. Moline MA, Benoit-Bird KJ, Robbins IC, Schroth-Miller M,Waluk CM, Zelenke B. 2010. Integrated measurements of acoustical and optical thin layers II: Horizontal length scales. Cont. Shelf Res. 30:29-38
75. Mullin MM, Brooks ER. 1976. Some consequences of distributional heterogeneity of phytoplankton and zooplankton. Limnol. Oceanogr. 21:784-96
76. Nielsen TG, Kiorboe T, Bjornsen PK. 1990. Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar. Ecol. Prog. Ser. 62:21-35
77. Nixon SW. 1995. Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia 41:199-219
78. Osborn TR. 1998. Finestructure, microstructure, and thin layers. Oceanography 11:36-43
79. Paine RT. 1966. Food web complexity and species diversity. Am. Nat. 100:65-75
80. Park MG, Cooney SK, Kim JS, Coats DW. 2002. Effects of parasitism on diel vertical migration, phototaxis/ geotaxis, and swimming speed of the bloom-forming dinoflagellate Akashiwo sanguinea. Aquat. Microb. Ecol. 29:11-18
81. Pedersen F. 1994. The oceanographic and biological tidal cycle succession in shallow sea fronts in the North Sea and the English Channel. Estuar. Coast. Shelf Sci. 38:249-69
82. Phillips OM, Shyu J, Salmun H. 1986. An experiment on boundary mixing: Mean circulation and transport rates. J. Fluid Mech. 173:473-99
83. Polin M, Tuval I, Drescher K, Gollub JP, Goldstein RE. 2009. Chlamydomonas swims with two "gears" in a eukaryotic version of run-and-tumble locomotion. Science 325:487-90
84. Prairie JC, Franks PJS, Jaffe JS. 2010. Cryptic peaks: Invisible vertical structure in fluorescent particles revealed using a planar laser imaging fluorometer. Limnol. Oceanogr. 55:1943-58
85. Prairie JC, Franks PJS, Jaffe JS, Doubell MJ, Yamazaki H. 2011. Physical and biological controls of vertical gradients in phytoplankton. Limnol. Oceanogr. Fluids Environ. 1:75-90
86. PrestonMD, Pitchford JW, Wood AJ. 2010. Evolutionary optimality in stochastic search problems. J. R. Soc. Interface 7:1301-10
87. Ralston DK, McGillicuddy DJ, Townsend DW. 2007. Asynchronous vertical migration and bimodal distribution of motile phytoplankton. J. Plankton Res. 29:803-21
88. Richardson TL, Cullen JJ, Kelley DE, Lewis MR. 1998. Potential contributions of vertically migrating Rhizosolenia to nutrient cycling and new production in the open ocean. J. Plankton Res. 20:219-41
89. 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. 225:123-37
90. 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
91. Roberts AM, Deacon FM. 2002. Gravitaxis in motile micro-organisms: The role of fore-aft body asymmetry. J. Fluid Mech. 452:405-23
92. Ross ON, Sharples J. 2004. Recipe for 1-D Lagrangian particle tracking models in space-varying diffusivity. Limnol. Oceanogr. Methods 2:289-302
93. 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
94. 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
95. Sellner KG, Doucette GJ, Kirkpatrick GJ. 2003. Harmful algal blooms: Causes, impacts and detection. J. Ind. Microbiol. Biotechnol. 30:383-406
96. Seymour JR, Marcos, Stocker R. 2009. Resource patch formation and exploitation throughout the marine microbial food web. Am. Nat. 173:15-29
97. Simpson JH, Tett PB, Argoteespinoza ML, Edwards A, Jones KJ, Savidge G. 1982. Mixing and phytoplankton growth around an island in a stratified sea. Cont. Shelf Res. 1:15-31
98. Smayda TJ. 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42:1137-53
99. Stacey MT, McManus MA, Steinbuck JV. 2007. Convergences and divergences and thin layer formation and maintenance. Limnol. Oceanogr. 52: 1523-32
100. Steele JH. 1974. Spatial heterogeneity and population stability. Nature 248:83
101. 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: 442-55
102. 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: 1353-68
103. Stocker R, Imberger J. 2003. Horizontal transport and dispersion in the surface layer of a medium-sized lake. Limnol. Oceanogr. 48:971-82
104. Strickland JDH. 1968. A comparison of profiles of nutrient and chlorophyll concentrations taken from discrete depths and by continuous recording. Limnol. Oceanogr. 13: 388-91
105. Sullivan JM, Donaghay PL, Rines JEB. 2010a. Coastal thin layer dynamics: Consequences to biology and optics. Cont. Shelf Res. 30:50-65
106. Sullivan JM, Van Holliday D, McFarlandM,McManus MA,CheritonOM, et al. 2010b. Layered organization in the coastal ocean: An introduction to planktonic thin layers and the LOCO project. Cont. Shelf Res. 30:1-6
107. Tiselius P. 1992. Behavior of Acartia tonsa in patchy food environments. Limnol. Oceanogr. 37:1640-51
108. Tiselius P, Jonsson PR, Verity PG. 1993. A model evaluation of the impact of food patchiness on foraging strategy and predation risk in zooplankton. Bull. Mar. Sci. 53:247-64
109. Townsend DW, Bennett SL, Thomas MA. 2005. Diel vertical distributions of the red tide dinoflagellate Alexandrium fundyense in the Gulf of Maine. Deep-Sea Res. Part II 52:2593-602
110. Turner JT, Tester PA. 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr. 42:1203-14
111. Twardowski MS, Sullivan JM, Donaghay PL, Zaneveld JRV. 1999. Microscale quantification of the absorption by dissolved and particulate material in coastal waters with an ac-9. J. Atmos. Ocean. Technol. 16:691-707
112. Tyler MA, Seliger HH. 1978. Annual subsurface transport of a red tide dinoflagellate to its bloom area: Water circulation patterns and organism distributions in Chesapeake Bay. Limnol. Oceanogr. 23:227-46
113. Vanierland ET, Peperzak L. 1984. Separation of marine seston and density determination of marine diatoms by density gradient centrifugation. J. Plankton Res. 6:29-44
114. Villareal TA, Carpenter EJ. 2003. Buoyancy regulation and the potential for vertical migration in the oceanic cyanobacterium Trichodesmium. Microb. Ecol. 45:1-10
115. Visser AW. 1997. Using random walk models to simulate the vertical distribution of particles in a turbulent water column. Mar. Ecol. Prog. Ser. 158:275-81
116. Walsby AE. 1972. Structure and function of gas vacuoles. Bacteriol. Rev. 36:1-32
117. Waterbury JB, Willey JM, Franks DG, Valois FW,Watson SW. 1985. A cyanobacterium capable of swimming motility. Science 230:74-76
118. Waters RL,Mitchell JG, Seymour J. 2003. Geostatistical characterisation of centimetre-scale spatial structure of in vivo fluorescence. Mar. Ecol. Prog. Ser. 251:49-58
119. White AE, Spitz YH, Letelier RM. 2006. Modeling carbohydrate ballasting by Trichodesmium spp. Mar. Ecol. Prog. Ser. 323:35-45
120. Woodson CB,Webster DR,WeissburgMJ, Yen J. 2005. Response of copepods to physical gradients associated with structure in the ocean. Limnol. Oceanogr. 50:1552-64
121. Woodson CB, Webster DR, Weissburg MJ, Yen J. 2007. Cue hierarchy and foraging in calanoid copepods: Ecological implications of oceanographic structure. Mar. Ecol. Prog. Ser. 330:163-77