Experiments in Fluids

, Volume 43, Issue 5, pp 755–768 | Cite as

Swimming by microscopic organisms in ambient water flow

Research Article

Abstract

When microscopic organisms swim in their natural habitats, they are simultaneously transported by ambient currents, waves, and turbulence. Therefore, to understand how swimming affects the movement of very small creatures through the environment, we need to study their behavior in realistic water flow conditions. The purpose of the work described here was to develop a series of integrated field and laboratory measurements at a variety of scales that enable us to record high-resolution videos of the behavior of microscopic organisms exposed to realistic spatio-temporal patterns of (1) water velocities and (2) distributions of chemical cues that affect their behavior. We have been developing these approaches while studying the swimming behavior in flowing water of the microscopic larvae of various bottom-dwelling marine animals. In shallow marine habitats, the oscillatory water motion associated with waves can make dramatic differences to water flow on the scales that affect trajectories of microscopic larvae.

References

  1. Abelson A (1997) Settlement in flow: upstream exploration of substrata by weakly swimming larvae. Ecology 78:160–166Google Scholar
  2. Abelson A, Denny MW (1997) Settlement of marine organisms in flow. Annu Rev Ecol Syst 28:317–339CrossRefGoogle Scholar
  3. Baird ME, Atkinson MJ (1997) Measurement and prediction of mass transfer to experimental coral reef communities. Limnol Oceanogr 42:1685–1693CrossRefGoogle Scholar
  4. Barret TK (1989) Nonintrusive optical measurements of turbulence and mixing in a stabily stratified fluid. University of California, San Diego PhD DissertationGoogle Scholar
  5. Bingham BL, Young CM (1991) Larval behavior of the ascidian Ecteinascidia turbinata Herdman; an in situ experimental study of the effects of swimming on dispersal. J Exp Mar Biol Ecol 145:189–204CrossRefGoogle Scholar
  6. Butman CA (1987) Larval settlement of soft-sediment invertebrates: The spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamic processes. Oceanogr Mar Biol Ann Rev 25:113–165Google Scholar
  7. Butman CA, Grassle JP, Busky EJ (1988) Horizontal swimming and gravitational sinking of Capitella sp. 1 (Annelida: Polychaeta) larvae: implications for settlement. Ophelia 29:43–58Google Scholar
  8. Charters AC, Neushul M, Coon D (1973) The effect of water motion on algal spore adhesion. Limnol Oceanogr 18:884–896Google Scholar
  9. Chia F, Buckland-Nicks SJ, Young CM (1984) Locomotion of marine invertebrate larvae: a review. Can J Zool 62:1205–1222Google Scholar
  10. Cowen EA, Monismith SG (1997) A hybrid digital particle tracking velocimetry technique. Exp Fluids 22:199–211CrossRefGoogle Scholar
  11. Crimaldi JP, Koseff JR (2001) High-resolution measurements of the spatial and temporal scalar structure of a turbulent plume. Exp Fluids 31:90–102CrossRefGoogle Scholar
  12. Crimaldi JP, Thompson JK, Rosman JH, Lowe RJ, Koseff JR (2002) Hydronamics of larval settlement: The influence of turbulent stress events at potential recruitment sites. Limnol Oceanogr 47:1137–1151CrossRefGoogle Scholar
  13. Crisp DJ (1955) The behavior of barnacle cyprids in relation to water movement over a surface. J Exp Biol 32:569–590Google Scholar
  14. Crisp DJ (1974) Factors influencing the settlement of marine invertebrate larvae. In: Grant PT, Mackie AM (eds) Chemoreception in marine organisms. Academic, London p 177Google Scholar
  15. Cronin TW, Forward RB Jr (1986) Vertical migration cycles of crab larvae and their role in larval dispersal. Bull Mar Sci 39:192–201Google Scholar
  16. Eckman JE, Savidge WB, Gross TF (1990) Relationship between duration of cyprid attachment and drag forces associated with detachment of Balanus amphitrite. Mar Biol 107:111–118CrossRefGoogle Scholar
  17. Eckman JE, Werner FE, Gross TF (1994) Modeling some effects of behavior on larval settlement in a turbulent boundary layer. Deep Sea Res 41:185–208CrossRefGoogle Scholar
  18. Epifanio CE, Masse AK, Garvine RW (1989) Transport of blue crab larvae by surface currents off Delaware Bay, USA. Mar Ecol Prog Ser 54:35–41CrossRefGoogle Scholar
  19. Finelli CM, Hart DD, Fonseca DM (1999) Evaluating the spatial resolution of an acoustic Doppler velocimeter and the consequences for measuring near-bed flows. Limnol Oceanogr 44:1793–1801CrossRefGoogle Scholar
  20. Finelli CM, Wethey DS (2003) Behavior of oyster larvae (Crassostrea virginica) larvae in flume boundary layer flows. Mar Biol 143:703–711CrossRefGoogle Scholar
  21. Forward RB Jr, Cronin TW (1980) Tidal rhythms of activity and phototaxis of an estuarine crab larva. Biol Bull 158:295–303CrossRefGoogle Scholar
  22. Forward RB Jr, Tankersley RA, De Vries MC, Rittshof D (1995) Sensory physiology and behavior of blue crab (Callinectes sapidus) postlarvae during horizontal transport. Mar Freshw Behav Physiol 26:233–248CrossRefGoogle Scholar
  23. Fuchs HL, Mullineaux LS, Solow AR (2004) Sinking behavior of gastropod larvae (Ilyanassa obsoleta) in turbulence. Limnol Oceanogr 49:1937–1948CrossRefGoogle Scholar
  24. Gross TF, Nowell ARM (1983) Mean flow and turbulence scaling in a tidal boundary layer. Cont Shelf Res 2:109–126CrossRefGoogle Scholar
  25. Hadfield MG (1977) Chemical interactions in larval settling of a marine gastropod. In: Faulkner DJ, Fenical WH (eds) Marine natural products chemistry. Plenum, New York, pp 403–413Google Scholar
  26. Hadfield MG, Koehl MAR (2004) Rapid behavioral responses of an invertebrate larva to dissolved settlement cue. Biol Bull 207:28–43CrossRefGoogle Scholar
  27. Hadfield MG, Meleshkevitch EA, Boudko DY (2000) The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol Bull 198:67–76CrossRefGoogle Scholar
  28. Hadfield MG, Paul VJ (2001) Natural chemical cues for settlement and metamorphosis of marine-invertebrate larvae. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton,pp 431–461Google Scholar
  29. Hannan CA (1984) Planktonic larvae may act as passive particles in turbulent near-bottom flows. Limnol Oceanogr 29:1108–1116CrossRefGoogle Scholar
  30. 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
  31. Jonsson PR, Berntsson KM, Larsson AI (2004) Linking larval supply to recruitment: flow-mediated control of initial adhesion of barnacle larvae. Ecology 85:2850–2859CrossRefGoogle Scholar
  32. Jumars PA (1993) Concepts in biological oceanography. Oxford University Press, New York, p 348Google Scholar
  33. Katz CH, Cobb JS, Spaulding M (1994) Larval behavior, hydrodynamic transport, and potential offshore-to-inshore recruitment in the American lobster Homarus americanus. Mar Ecol Prog Ser 103:265–273CrossRefGoogle Scholar
  34. Koehl MAR (2007) Minireview: Hydrodynamics of larval settlement into fouling communities. Biofouling 23:1–12CrossRefGoogle Scholar
  35. Koehl MAR, Hadfield MG (2004) Soluble settlement cue in slowly moving water within coral reefs induces larval adhesion to surfaces. J Mar Syst 49:75–88CrossRefGoogle Scholar
  36. Koehl MAR, Powell TM (1994) Turbulent transport of larvae near wave-swept rocky shores: does water motion overwhelm larval sinking. In: Wilson H, Shinn G, Stricker S (eds) Reproduction and development of marine invertebrates. Johns Hopkins University Press, Baltimore, pp 261–274Google Scholar
  37. Koehl MAR, Powell TM, Dobbins EL (1997) Effects of algal turf on mass transport and flow microhabitat of ascidians in a coral reef lagoon. Proc 8th Int Coral Reef Symp 2:1087–1092Google Scholar
  38. Koehl MAR, Strother JA, Reidenbach MA, Koseff JR, Hadfield MG (2007) Individual-based model of larval transport to coral reefs in turbulent, wave-driven flow: effects of behavioral responses to dissolved settlement cues. Mar Ecol Prog Ser 335:1–18CrossRefGoogle Scholar
  39. Krug PJ (2006) Defense of benthic invertebrates against surface colonization by larvae: A chemical arms race. In: Fusetani N, Clare AS (eds) Marine molecular biotechnology, Springer, Berlin, pp 1–53Google Scholar
  40. Larsson AI, Jonsson PR (2006) Barnacle larvae actively select flow environments supporting post-settlement growth and survival. Ecology 87:1960–1966CrossRefGoogle Scholar
  41. Lowe RL, Koseff JR, Monismith SG (2005) Oscillatory flow through submerged canopies: 1. Velocity structure. J Geophys Res 110, Art. No. C10016Google Scholar
  42. Luckenbach MW, Orth RJ (1992) Swimming velocity and behavior of blue crab (Callinctes sapidus Rathbun) megalopae in still and flowing water. Estuaries 15:186–192CrossRefGoogle Scholar
  43. McHenry MJ, Strother JA (2003) The kinematics of phototaxis in larvae of the ascidian Aplidium constellatum. Mar Biol 142:173–184Google Scholar
  44. Mullineaux LS, Butman CA (1991) Initial contact, exploration, and attachment of barnacle (Balanus amphitrite) cyprids settling in flow. Mar Biol 110:93–103CrossRefGoogle Scholar
  45. Nowell ARM, Jumars PA (1984) Flow environments of aquatic benthos. Ann Rev Ecol Syst 15:303–328CrossRefGoogle Scholar
  46. Ólafsson EB, Peterson CH, Ambrose WG Jr (1994) Does recruitment limitation structure populations and communities of macro-invertebrates in marine soft sediments: the relative significance of pre- and post-settlement processes. Oceanog Mar Biol Ann Rev 32:65–109Google Scholar
  47. Palmer MA, Allan JD, Butman CA (1996) Dispersal as a regional process affecting the local dynamics of marine and stream benthic invertebrates. Trends Evol Ecol 11:322–326CrossRefGoogle Scholar
  48. Pawlik JR., Butman CA (1993) Settlement of a marine tube worm as a function of current velocity: interacting effects of hydrodynamics and behavior. Limnol Oceanogr 38:1730–1740CrossRefGoogle Scholar
  49. Pidgeon EJ (1999) An experimental investigation of breaking wave induced turbulence. Stanford University PhD DissertationGoogle Scholar
  50. Queiroga H, Blanton J (2005) Interactions between behaviour and physical forcing in the control of horizontal transport of decapod crustacean larvae. Adv Mar Bio 47:107–214Google Scholar
  51. Reidenbach MA, Koseff JR, Monismith SG, Steinbuck JV, Genin A (2006) The effects of waves and morphology on mass transfer within branched reef corals. Limnol Oceanogr 51:1134–1141CrossRefGoogle Scholar
  52. Reidenbach MA, Koseff JR, Monismith SG (2007) Laboratory experiments of fine-scale mixing and mass transport within a coral canopy. Phys Fluids 19:075107Google Scholar
  53. Rooney P, Cobb JS (1991) Effects of time of day, water temperature, and water velocity on swimming by postlarvae of the American lobster, Homarus americanus. Can J Fish Aquatic Sci 48:1944–1950CrossRefGoogle Scholar
  54. Rothlisberg PC, Church JA (1994) Processes controlling the larval dispersal and postlarval recruitment of Penaeid prawns. In: Sammarco PW, Heron ML (eds) Coastal and estuarine studies. American Geophysical Union, Washington, pp 235–252Google Scholar
  55. Rothlisberg PC, Church JA, Fandry CB (1995) A mechanism for near-shore concentration and estuarine recruitment of postlarval Penaeus plebeius Hess (Decapoda, Penaeidae). Est Coast Shelf Sci 40:115–138CrossRefGoogle Scholar
  56. Roughgarden J, Pennington JT, Stoner D, Alexander S, Miller K (1991) Collisions of upwelling fronts with the intertidal zone: The cause of recruitment pulses in barnacle populations of central California [USA]. Acta Oecol 12:35–52Google Scholar
  57. Shanks AL (1985) Behavioral basis of internal-wave-induced shoreward transport megalopae of the crab Pachygrapsus crassipes. Mar Ecol Prog Ser 24:289–295CrossRefGoogle Scholar
  58. Sleath JF (1987) Turbulent oscillatory flow over rough beds. J Fluid Mech 182:369–409CrossRefGoogle Scholar
  59. Stancyk SE, Feller RJ (1986) Transport of non-decapod invertebrate larvae in estuaries: an overview. Bull Mar Sci 39:257–268Google Scholar
  60. Tamburri MN, Finelli CM, Wethey DS, Zimmer-Faust RK (1996) Chemical induction of larval settlement behavior in flow. Biol Bull 191:367–373CrossRefGoogle Scholar
  61. Tankersley RA, Forward RB Jr (1994) Endogenous swimming rhythms in estuarine crab megalopae: Implications for flood-tide transport. Mar Biol 118:415–423CrossRefGoogle Scholar
  62. Tankersley RA, McKelvey LM, Forward RB (1995) Responses of estuarine crab megalopae to pressure, salinity and light: Implications for flood-tide transport. Mar Biol 122:391–400CrossRefGoogle Scholar
  63. Unabia C, Hadfield MG (1999) The role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar Biol 133:55–64CrossRefGoogle Scholar
  64. Woodin SA (1991) Recruitment of infauna: positive or negative cues? Amer Zool 31:797–807Google Scholar
  65. Worcester SE (1994) Adult rafting versus larval swimming: Dispersal and recruitment of a botryllid ascidian on eelgrass. Mar Biol 121:309–317CrossRefGoogle Scholar
  66. Young CM (1990) Larval ecology of marine invertebrates: a sesquicentennial history. Ophelia 32:1–48Google Scholar
  67. Young CM (1995) Behavior and locomotion during the dispersal phase of larval life. In: McEdward LR (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 249–278Google Scholar
  68. Young CM, Chia FS (1987) Abundance and distribution of pelagic larvae as influenced by predation, behavior and hydrographic factors. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Blackwell, Palo Alto, pp 385–463Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA

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