Marine Biology

, Volume 162, Issue 10, pp 1939–1954 | Cite as

Zooplankton in flowing water near benthic communities encounter rapidly fluctuating velocity gradients and accelerations

  • Rachel E. Pepper
  • Jules S. Jaffe
  • Evan Variano
  • M. A. R. Koehl
Original Paper

Abstract

The fine-scale temporal patterns of water velocities, accelerations, and velocity gradients encountered by individual zooplankters carried in ambient flow can affect their dispersal, behavior, and interaction with other organisms, but have not yet been measured in realistic flow environments. We focused on zooplankton in wavy turbulent boundary layer flow near benthic communities because such flow affects important processes, including larval settlement and prey capture by benthic zooplanktivores. Flow across fouling communities measured in the field was mimicked in a wave flume, where time-varying velocity fields over biofouled surfaces were quantified using particle image velocimetry (PIV). Trajectories of simulated zooplankters seeded into these flow fields were followed to quantify temporal patterns of velocity gradients and accelerations that individuals encountered. We found that such zooplankters are not subjected to steady velocities or velocity gradients, but rather encounter rapidly fluctuating accelerations and velocity gradients with peaks reaching several orders of magnitude above mean values and lasting fractions of a second, much shorter than the wave period. We calculated the proportion of time zooplankters spent affected (e.g., being damaged, changing behavior) by accelerations or velocity gradients and found that a small increase in mean velocity can cause a much larger increase in time affected. Animal reaction threshold and reaction time also changed the fraction of time they were affected by the flow. Using different PIV spatial resolutions showed that inter-vector spacing should be ≤0.5 Kolmogorov length (smallest eddy scale) to accurately capture velocity gradients along trajectories, but coarser resolutions (≤2–6 × Kolmogorov length) are sufficient for velocities, accelerations, and zooplankton trajectories.

Notes

Acknowledgments

We are grateful to B. Nedved, L. Perotti, and M. Shipley for help with the fieldwork, and to T. Cooper for technical assistance with the wave tank experiments and particle image velocimetry analysis. Wave tank studies were conducted at the Kewalo Marine Laboratory, University of Hawaii, and we thank M. Hadfield and his research group for logistical support and useful discussions. This research was supported by National Science Foundation grant Integrative Organismal Systems 0842685 (to MK), and the Miller Institute for Basic Research in Science (fellowship to RP).

Supplementary material

Online Resource 1 An example of flow measured in a wave flume in the laboratory with vectors determined using PIV (particle image velocimetry). This is an example of the higher energy flow and is slowed down by a factor of two. (MPG 8618 kb)

Online Resource 2Phestilla Sibogae (sea slug) larvae swimming in a petri dish. Larvae are about 200 microns long and 100 microns across. They swim using ciliated organs called velum. Note that one larva bumps into another and responds to the mechanical cue by retracting its velum. Slowed down by a factor of two. (MPG 1738 kb)

References

  1. Abelson A, Denny M (1997) Settlement of marine organisms in flow. Annu Rev Ecol Syst 28:317–339CrossRefGoogle Scholar
  2. Antonia RA, Mi J (1993) Corrections for velocity and temperature derivatives in turbulent flows. Exp Fluids 14:203–208CrossRefGoogle Scholar
  3. Antonia RA, Zhu Y, Kim J (1993) On the measurement of lateral velocity derivatives in turbulent flows. Exp Fluids 15:65–69Google Scholar
  4. Antonia RA, Zhu Y, Kim J (1994) Corrections for spatial velocity derivatives in a turbulent shear flow. Exp Fluids 16:411–413CrossRefGoogle Scholar
  5. Biewener AA, Full RJ (1992) Force platform and kinematic analysis. In: Biewener AA (ed) Biomechanics: structures and systems: a practical approach, Oxford University Press, New York, pp 45–73Google Scholar
  6. Bram JB, Page HM, Dugan JE (2005) Spatial and temporal variability in early successional patterns of an invertebrate assemblage at an offshore oil platform. J Exp Mar Biol Ecol 317:223–237CrossRefGoogle Scholar
  7. Bretherton FP (1962) The motion of rigid particles in a shear flow at low Reynolds number. J Fluid Mech 14(2):284–304Google Scholar
  8. Butman CA, Grassle JP, Buskey EJ (1988) Horizontal swimming and gravitational sinking of Capitella sp. I (Annelida: Polychaeta) larvae: implications for settlement. Ophelia 29:43–57CrossRefGoogle Scholar
  9. Buxton ORH, Laizet S, Ganapathisubramani B (2011) The effects of resolution and noise on kinematic features of fine-scale turbulence. Exp Fluids 51(5):1417–1437Google Scholar
  10. Chan KYK (2012) Biomechanics of larval morphology affect swimming: insights from the sand dollars Dendraster excentricus. Integr Comp Biol 52:458–469CrossRefGoogle Scholar
  11. Chia F-S, Buckland-Nicks J, Young CM (1984) Locomotion of marine invertebrate larvae: a review. Can J Zool 62:1205–1222CrossRefGoogle Scholar
  12. Clay TW, Grünbaum D (2010) Morphology-flow interactions lead to stage-selective vertical transport of larval sand dollars in shear flow. J Exp Biol 213:1281–1292CrossRefGoogle Scholar
  13. Clay TW, Grünbaum D (2011) Swimming performance as a constraint on larval morphology in plutei. Mar Ecol Prog Ser 423:185–196CrossRefGoogle Scholar
  14. Crimaldi JP, Zimmer RK (2014) The physics of broadcast spawning in benthic invertebrates. Annu Rev Mar Sci 6:141–165CrossRefGoogle Scholar
  15. Crisp DJ (1955) The behaviour of barnacle cyprids in relation to water movement over a surface. J Exp Biol 32:569–590Google Scholar
  16. Davidson PA (2004) Turbulence: an introduction for scientists and engineers. Oxford University Press, USAGoogle Scholar
  17. De Jong J, Cao L, Woodward SH et al (2008) Dissipation rate estimation from PIV in zero-mean isotropic turbulence. Exp Fluids 46:499–515CrossRefGoogle Scholar
  18. Denny MW, Nelson EK, Mead KS (2002) Revised estimates of the effects of turbulence on fertilization in the purple sea urchin, Strongylocentrotus purpuratus. Biol Bull 203:275–277CrossRefGoogle Scholar
  19. Donzis DA, Yeung PK, Sreenivasan KR (2008) Dissipation and enstrophy in isotropic turbulence: resolution effects and scaling in direct numerical simulations. Phys Fluids 20:045108–1–045108–16CrossRefGoogle Scholar
  20. Durham WM, Kessler JO, Stocker R (2009) Disruption of vertical motility by shear triggers formation of thin phytoplankton layers. Science 323:1067–1070CrossRefGoogle Scholar
  21. Finelli CM, Wethey DS (2003) Behavior of oyster (Crassostrea virginica) larvae in flume boundary layer flows. Mar Biol 143:703–711CrossRefGoogle Scholar
  22. Fuchs HL, Mullineaux LS, Solow AR (2004) Sinking behavior of gastropod larvae (Ilyanassa obsoleta) in turbulence. Limnol Oceanogr 49:1937–1948CrossRefGoogle Scholar
  23. Fuchs HL, Hunter EJ, Schmitt EL, Guazzo RA (2013) Active downward propulsion by oyster larvae in turbulence. J Exp Biol 216:1458–1469CrossRefGoogle Scholar
  24. Fuchs HL, Gerbi GP, Hunter EJ et al (2015) Hydrodynamic sensing and behavior by oyster larvae in turbulence and waves. J Exp Biol 218:1419–1432CrossRefGoogle Scholar
  25. Gaylord B, Hodin J, Ferner MC (2013) Turbulent shear spurs settlement in larval sea urchins. Proc Natl Acad Sci 110:6901–6906CrossRefGoogle Scholar
  26. Greene JK, Grizzle RE (2007) Successional development of fouling communities on open ocean aquaculture fish cages in the western Gulf of Maine, USA. Aquaculture 262:289–301CrossRefGoogle Scholar
  27. Gross TF, Werner FE, Eckman JE (1992) Numerical modeling of larval settlement in turbulent bottom boundary layers. J Mar Res 50:611–642CrossRefGoogle Scholar
  28. Grunbaum D, Strathmann RR (2003) Form, performance and trade-offs in swimming and stability of armed larvae. J Mar Res 61:659–691CrossRefGoogle Scholar
  29. Hadfield MG, Koehl MAR (2004) Rapid behavioral responses of an invertebrate larva to dissolved settlement cue. Biol Bull 207:28–43CrossRefGoogle Scholar
  30. Holm ER, Nedved BT, Phillips N et al (2000) Temporal and spatial variation in the fouling of silicone coatings in Pearl Harbor, Hawaii. Biofouling 15:95–107CrossRefGoogle Scholar
  31. Hunter T (1988) Mechanical design of hydroids: flexibility, flow forces, and feeding in Obelia longissima. University of California, BerkeleyGoogle Scholar
  32. Jeffery GB (1922) The motion of ellipsoidal particles immersed in a viscous fluid. Proc Royal Soc Lond A 102:161–179Google Scholar
  33. Jimenez J (1997) Oceanic turbulence at millimeter scales. Sci Mar 61:47–56Google Scholar
  34. Jonsson PR, Andre C, Lindegarth M (1991) Swimming behavior of marine bivalve larvae in a flume boundary-layer flow—evidence for near-bottom confinement. Mar Ecol Prog Ser 79:67–76CrossRefGoogle Scholar
  35. Karp-Boss L, Jumars PA (1998) Motion of diatom chains in steady shear flow. Limnol Oceanogr 43:1767–1773CrossRefGoogle Scholar
  36. Karp-Boss L, Boss E, Jumars PA (2000) Motion of dinoflagellates in a simple shear flow. Limnol Oceanogr 45:1594–1602CrossRefGoogle Scholar
  37. Koehl MRA (2007) Mini review: hydrodynamics of larval settlement into fouling communities. Biofouling 23:357–368CrossRefGoogle Scholar
  38. Koehl MAR, Cooper T (2015) Swimming in a turbulent world. Integr Comp Biol 55(4):683–697CrossRefGoogle Scholar
  39. Koehl MAR, Strother JA, Reidenbach MA et al (2007) Individual-based model of larval transport to coral reefs in turbulent, wave-driven flow: behavioral responses to dissolved settlement inducer. Mar Ecol Prog Ser 335:1–18CrossRefGoogle Scholar
  40. Koehl MAR, Crimaldi JP, Dombroski DE (2013) Wind chop and ship wakes determine hydrodynamic stresses on larvae settling on different microhabitats in fouling communities. Mar Ecol Prog Ser 479:47–62Google Scholar
  41. Lavoie P, Avallone G, Gregorio F et al (2007) Spatial resolution of PIV for the measurement of turbulence. Exp Fluids 43:39–51CrossRefGoogle Scholar
  42. Mathews JH, Fink KD (1999) Numerical methods using MATLAB. Prentice Hall, Upper Saddle River, NJGoogle Scholar
  43. Maxey MR, Riley JJ (1983) Equation of motion for a small rigid sphere in a nonuniform flow. Phys Fluids 26:883–889CrossRefGoogle Scholar
  44. McDonald KA (2012) Earliest ciliary swimming effects vertical transport of planktonic embryos in turbulence and shear flow. J Exp Biol 215:141–151CrossRefGoogle Scholar
  45. McEdward LR (1995) Ecology of marine invertebrate larvae. CRC Press, Boca RatonGoogle Scholar
  46. Mead KS, Denny MW (1995) The effects of hydrodynamic shear stress on fertilization and early development of the purple sea urchin Strongylocentrotus purpuratus. Biol Bull 188:46–56CrossRefGoogle Scholar
  47. Meneveau C (2011) Lagrangian dynamics and models of the velocity gradient tensor in turbulent flows. Annu Rev Fluid Mech 43:219–245CrossRefGoogle Scholar
  48. Nowell ARM, Jumars PA (1984) Flow environments of aquatic benthos. Annu Rev Ecol Syst 15:303–328CrossRefGoogle Scholar
  49. Okamura B (1984) The effects of ambient flow velocity, colony size, and upstream colonies on the feeding success of bryozoa. I. Bugula stolonifera Ryland, an arborescent species. J Exp Mar Biol Ecol 83:179–193CrossRefGoogle Scholar
  50. Peters F, Marrasé C (2000) Effects of turbulence on plankton: an overview of experimental evidence and some theoretical considerations. Mar Ecol Prog Ser 205:291–306CrossRefGoogle Scholar
  51. Pope SB (2000) Turbulent flows, 1st edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  52. Rabiner LR, Gold B (1975) Theory and application of digital signal processing. Prentice-Hall, Englewood Cliffs, NJGoogle Scholar
  53. Raffel M, Willert CE, Kompenhans J (1998) Particle image velocimetry: a practical guide. Springer, BerlinGoogle Scholar
  54. Raupach MR, Antonia RA, Rajagopalan S (1991) Rough-wall turbulent boundary layers. Appl Mech Rev 44:1–25CrossRefGoogle Scholar
  55. Robinson H, Finelli CM, Buskey EJ (2007) The turbulent life of copepods: effects of water flow over a coral reef on their ability to detect and evade predators. Mar Ecol Prog Ser 349:171–181CrossRefGoogle Scholar
  56. Robinson HE, Finelli CM, Koehl MAR (2013) Interactions between benthic predators and zooplanktonic prey are affected by turbulent Waves. Integr Comp Biol 53:810–820CrossRefGoogle Scholar
  57. Saarenrinne P, Piirto M (2000) Turbulent kinetic energy dissipation rate estimation from PIV velocity vector fields. Exp Fluids 29:S300–S307CrossRefGoogle Scholar
  58. Schabes M (1992) Mechanical consequences of the association between the solitary ascidian, Styela clava Herdman, 1881, and its epibiota. M.S. Thesis, University of California, BerkeleyGoogle Scholar
  59. Strathmann RR, Grunbaum D (2006) Good eaters, poor swimmers: compromises in larval form. Integr Comp Biol 46:312–322CrossRefGoogle Scholar
  60. Sutherland JP, Karlson RH (1977) Development and stability of the fouling community at Beaufort, North Carolina. Ecol Monogr 47:425–446CrossRefGoogle Scholar
  61. Sutherland KR, Dabiri JO, Koehl MAR (2011) Simultaneous field measurements of ostracod swimming behavior and background flow. Limnol Oceanogr Fluids Environ 1:135–146CrossRefGoogle Scholar
  62. Szmant AM, Meadows MG (2006) Developmental changes in coral larval buoyancy and vertical swimming behavior: implications for dispersal and connectivity. In: Proceedings of 10th international coral reef Symposium, pp 431–437Google Scholar
  63. Tanaka T, Eaton JK (2007) A correction method for measuring turbulence kinetic energy dissipation rate by PIV. Exp Fluids 42:893–902CrossRefGoogle Scholar
  64. Thomas F (1994) Physical properties of gametes in three sea urchin species. J Exp Biol 194:263–284Google Scholar
  65. Thomas WH, Gibson CH (1990) Effects of small-scale turbulence on microalgae. J Appl Phycol 2:71–77CrossRefGoogle Scholar
  66. Thorpe SA (2007) An introduction to ocean turbulence. Cambridge University Press, CambridgeGoogle Scholar
  67. Toschi F, Bodenschatz E (2009) Lagrangian properties of particles in turbulence. Annu Rev Fluid Mech 41:375–404CrossRefGoogle Scholar
  68. Townsend AA (1980) The structure of turbulent shear flow. Cambridge University Press, CambridgeGoogle Scholar
  69. Variano EA, Cowen EA (2008) A random-jet-stirred turbulence tank. J Fluid Mech 604:1–32CrossRefGoogle Scholar
  70. Vogel S (2013) Comparative biomechanics: life’s physical world, 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  71. Welch P (1967) The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust 15:70–73CrossRefGoogle Scholar
  72. Wheeler JD, Helfrich KR, Anderson EJ et al (2013) Upward swimming of competent oyster larvae Crassostrea virginica persists in highly turbulent flow as detected by PIV flow subtraction. Mar Ecol Prog Ser 488:171–185CrossRefGoogle Scholar
  73. Wheeler JD, Helfrich KR, Anderson EJ, Mullineaux LS (2015) Isolating the hydrodynamic triggers of the dive response in eastern oyster larvae. Limnol Oceanogr 60(4):1332CrossRefGoogle Scholar
  74. Worth NA, Nickels TB, Swaminathan N (2010) A tomographic PIV resolution study based on homogeneous isotropic turbulence DNS data. Exp Fluids 49:637–656CrossRefGoogle Scholar
  75. Yeung P (2002) Lagrangian investigations of turbulence. Annu Rev Fluid Mech 34:115–142CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Rachel E. Pepper
    • 1
  • Jules S. Jaffe
    • 2
  • Evan Variano
    • 3
  • M. A. R. Koehl
    • 4
  1. 1.Department of PhysicsUniversity of Puget SoundTacomaUSA
  2. 2.Scripps Institution of OceanographyUniversity of California San DiegoLa JollaUSA
  3. 3.Department of Civil and Environmental EngineeringUniversity of California BerkeleyBerkeleyUSA
  4. 4.Department of Integrative BiologyUniversity of California BerkeleyBerkeleyUSA

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