Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T02:10:05.424Z Has data issue: false hasContentIssue false

Navigation of micro-swimmers in steady flow: the importance of symmetries

Published online by Cambridge University Press:  02 December 2021

Jingran Qiu
Affiliation:
AML, Department of Engineering Mechanics, Tsinghua University, 100084 Beijing, PR China
Navid Mousavi
Affiliation:
Department of Physics, University of Gothenburg, SE-41296 Gothenburg, Sweden
Kristian Gustavsson
Affiliation:
Department of Physics, University of Gothenburg, SE-41296 Gothenburg, Sweden
Chunxiao Xu
Affiliation:
AML, Department of Engineering Mechanics, Tsinghua University, 100084 Beijing, PR China
Bernhard Mehlig
Affiliation:
Department of Physics, University of Gothenburg, SE-41296 Gothenburg, Sweden
Lihao Zhao*
Affiliation:
AML, Department of Engineering Mechanics, Tsinghua University, 100084 Beijing, PR China
*
Email address for correspondence: [email protected]

Abstract

Marine micro-organisms must cope with complex flow patterns and even turbulence as they navigate the ocean. To survive they must avoid predation and find efficient energy sources. A major difficulty in analysing possible survival strategies is that the time series of environmental cues in nonlinear flow is complex and that it depends on the decisions taken by the organism. One way of determining and evaluating optimal strategies is reinforcement learning. In a proof-of-principle study, Colabrese et al. (Phys. Rev. Lett., vol. 118, 2017, 158004) used this method to find out how a micro-swimmer in a vortex flow can navigate towards the surface as quickly as possible, given a fixed swimming speed. The swimmer measured its instantaneous swimming direction and the local flow vorticity in the laboratory frame, and reacted to these cues by swimming either left, right, up or down. However, usually a motile micro-organism measures the local flow rather than global information, and it can only react in relation to the local flow because, in general, it cannot access global information (such as up or down in the laboratory frame). Here we analyse optimal strategies with local signals and actions that do not refer to the laboratory frame. We demonstrate that symmetry breaking is required to find such strategies. Using reinforcement learning, we analyse the emerging strategies for different sets of environmental cues that micro-organisms are known to measure.

Type
JFM Papers
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alageshan, J.K., Verma, A.K., Bec, J. & Pandit, R. 2020 Machine learning strategies for path-planning microswimmers in turbulent flows. Phys. Rev. E 101, 043110.CrossRefGoogle ScholarPubMed
Barile, P.J., Stoner, A.W. & Young, C.M. 1994 Phototaxis and vertical migration of the queen conch (Strombus gigas linne) veliger larvae. J. Expl Mar. Biol. Ecol. 183 (2), 147162.CrossRefGoogle Scholar
Biferale, L., Bonaccorso, F., Buzzicotti, M., Di Leoni, P.C. & Gustavsson, K. 2019 Zermelo's problem: optimal point-to-point navigation in 2D turbulent flows using reinforcement learning. Chaos 29 (10), 103138.CrossRefGoogle ScholarPubMed
Bollens, S.M. & Frost, B.W. 1989 Predator-induced diet vertical migration in a planktonic copepod. J. Plankton Res. 11 (5), 10471065.CrossRefGoogle Scholar
Borgnino, M., Boffetta, G., De Lillo, F. & Cencini, M. 2018 Gyrotactic swimmers in turbulence: shape effects and role of the large-scale flow. J. Fluid Mech. 856, R1.CrossRefGoogle Scholar
Buskey, E.J., Lenz, P.H. & Hartline, D.K. 2002 Escape behavior of planktonic copepods in response to hydrodynamic disturbances: high speed video analysis. Mar. Ecol. Prog. Ser. 235, 135146.CrossRefGoogle Scholar
Carlotti, F.C.C.O., Bonnet, D. & Halsband-Lenk, C. 2007 Development and growth rates of Centropages typicus. Prog. Oceanogr. 72 (2-3), 164194.CrossRefGoogle Scholar
Cencini, M., Boffetta, G., Borgnino, M. & De Lillo, F. 2019 Gyrotactic phytoplankton in laminar and turbulent flows: a dynamical systems approach. Eur. Phys. J. E 42 (3), 31.CrossRefGoogle ScholarPubMed
Cohen, J.H. & Forward, R.B. Jr. 2002 Spectral sensitivity of vertically migrating marine copepods. Biol. Bull. 203 (3), 307314.CrossRefGoogle ScholarPubMed
Cohen, J.H., Last, K.S., Waldie, J. & Pond, D.W. 2019 Loss of buoyancy control in the copepod Calanus finmarchicus. J. Plankton Res. 41 (5), 787790.CrossRefGoogle ScholarPubMed
Colabrese, S., Gustavsson, K., Celani, A. & Biferale, L. 2017 Flow navigation by smart microswimmers via reinforcement learning. Phys. Rev. Lett. 118 (15), 158004.CrossRefGoogle ScholarPubMed
Colabrese, S., Gustavsson, K., Celani, A. & Biferale, L. 2018 Smart inertial particles. Phys. Rev. Fluids 3 (8), 084301.CrossRefGoogle Scholar
Durham, W.M., Climent, E., Barry, M., De Lillo, F., Boffetta, G., Cencini, M. & Stocker, R. 2013 Turbulence drives microscale patches of motile phytoplankton. Nat. Commun. 4, 2148.CrossRefGoogle ScholarPubMed
Durham, W.M., Climent, E. & Stocker, R. 2011 Gyrotaxis in a steady vortical flow. Phys. Rev. Lett. 106, 238102.CrossRefGoogle Scholar
Durham, W.M., Kessler, J.O. & Stocker, R. 2009 Disruption of vertical motility by shear triggers formation of thin phytoplankton layers. Science 323 (5917), 10671070.CrossRefGoogle ScholarPubMed
Fields, D. 2014 The sensory horizon of marine copepods. In Copepods: Diversity, Habitat and Behavior, pp. 157–179. Nova Science Publishers, Inc.Google Scholar
Fields, D.M. & Yen, J. 1997 Implications of the feeding current structure of Euchaeta rimana, a carnivorous pelagic copepod, on the spatial orientation of their prey. J. Plankton Res. 19 (1), 7995.CrossRefGoogle Scholar
Fraga, S. 1989 Chainforming dinoflagellates: an adaptation to red tides. Red Tides Biol. Environ. Sci. Toxicol. 281284.Google Scholar
Frisch, U. 1997 Turbulence. Cambridge Univeristy Press.Google Scholar
Fuchs, H.L. & Gerbi, G.P. 2016 Seascape-level variation in turbulence-and wave-generated hydrodynamic signals experienced by plankton. Prog. Oceanogr. 141, 109129.CrossRefGoogle Scholar
Fuchs, H.L., Gerbi, G.P., Hunter, E.J., Christman, A.J. & Diez, F.J. 2015 Hydrodynamic sensing and behavior by oyster larvae in turbulence and waves. J. Expl Biol. 218 (9), 14191432.Google Scholar
Fuchs, H.L., Hunter, E.J., Schmitt, E.L. & Guazzo, R.A. 2013 Active downward propulsion by oyster larvae in turbulence. J. Expl Biol. 216 (8), 14581469.Google ScholarPubMed
Gilbert, O.M. & Buskey, E.J. 2005 Turbulence decreases the hydrodynamic predator sensing ability of the calanoid copepod Acartia tonsa. J. Plankton Res. 27 (10), 10671071.CrossRefGoogle Scholar
Gunnarson, P., Mandralis, I., Novati, G., Koumoutsakos, P. & Dabiri, J.O. 2021 Learning efficient navigation in vortical flow fields. arXiv:2102.10536.Google Scholar
Gustavsson, K., Berglund, F., Jonsson, P.R. & Mehlig, B. 2016 Preferential sampling and small-scale clustering of gyrotactic microswimmers in turbulence. Phys. Rev. Lett. 116 (10), 108104.CrossRefGoogle ScholarPubMed
Gustavsson, K., Biferale, L., Celani, A. & Colabrese, S. 2017 Finding efficient swimming strategies in a three-dimensional chaotic flow by reinforcement learning. Eur. Phys. J. E 40 (12), 110.CrossRefGoogle Scholar
Gustavsson, K. & Mehlig, B. 2016 Statistical models for spatial patterns of heavy particles in turbulence. Adv. Phys. 61, 157.CrossRefGoogle Scholar
Hartl, B., Hb l, M., Kahl, G. & Zẗtl, A. 2021 Microswimmers learning chemotaxis with genetic algorithms. Proc. Natl Acad. Sci. 118 (19), e2019683118.CrossRefGoogle ScholarPubMed
Hays, G.C. 2003 A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Mig. Disp. Mar. Organ. 163170.Google Scholar
Huntley, M. & Brooks, E.R. 1982 Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar. Biol. 71 (1), 2331.CrossRefGoogle Scholar
Hwang, J.-S. & Strickler, R. 2001 Can copepods differentiate prey from predator hydromechanically? Zool. Stud. Taipei 40 (1), 16.Google Scholar
Incze, L.S., Hebert, D., Wolff, N., Oakey, N. & Dye, D. 2001 Changes in copepod distributions associated with increased turbulence from wind stress. Mar. Ecol. Prog. Ser. 213, 229240.CrossRefGoogle Scholar
Jakobsen, H.H. 2001 Escape response of planktonic protists to fluid mechanical signals. Mar. Ecol. Prog. Ser. 214, 6778.CrossRefGoogle Scholar
Jeffery, G.B. 1922 The motion of ellipsoidal particles immersed in a viscous fluid. Proc. R. Soc. Lond. Ser. A 102, 161179.Google Scholar
Jiang, H., Osborn, T.R. & Meneveau, C. 2002 The flow field around a freely swimming copepod in steady motion. Part I: theoretical analysis. J. Plankton Res. 24 (3), 167189.CrossRefGoogle Scholar
Jiang, H. & Paffenhöfer, G. 2004 Relation of behavior of copepod juveniles to potential predation by omnivorous copepods: an empirical-modeling study. Mar. Ecol. Prog. Ser. 278, 225239.CrossRefGoogle Scholar
Kabata, Z. & Hewitt, G.C. 1971 Locomotory mechanisms in caligidae (crustacea: Copepoda). J. Fish. Board Canada 28 (8), 11431151.CrossRefGoogle Scholar
Kamykowski, D., Reed, R.E. & Kirkpatrick, G.J. 1992 Comparison of sinking velocity, swimming velocity, rotation and path characteristics among six marine dinoflagellate species. Mar. Biol. 113 (2), 319328.CrossRefGoogle Scholar
Kessler, J.O. 1985 Hydrodynamic focusing of motile algal cells. Nature 313, 218220.CrossRefGoogle Scholar
Kim, S. & Karrila, S.J. 1991 Microhydrodynamics: Principles and Selected Applications. Butterworth-Heinemann.Google Scholar
Kiørboe, T., Andersen, A., Langlois, V.J. & Jakobsen, H.H. 2010 Unsteady motion: escape jumps in planktonic copepods, their kinematics and energetics. J. R. Soc. Interface 7 (52), 15911602.CrossRefGoogle ScholarPubMed
Kiørboe, T., Saiz, E. & Visser, A.E. 1999 Hydrodynamic signal perception in the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 179, 97111.CrossRefGoogle Scholar
Kiørboe, T. & Visser, A.W. 1999 Predator and prey perception in copepods due to hydromechanical signals. Acta Obstet. Gyn. Jpn 179 (3), 8195.Google Scholar
Kirk, K.L. & Gilbert, J.J. 1988 Escape behavior of polyarthra in response to artificial flow stimuli. Bull. Mar. Sci. 43 (3), 551560.Google Scholar
Knutsen, T., Melle, W. & Calise, L. 2001 Determining the mass density of marine copepods and their eggs with a critical focus on some of the previously used methods. J. Plankton Res. 23 (8), 859873.CrossRefGoogle Scholar
Lovecchio, S., Climent, E., Stocker, R. & Durham, W.M. 2019 Chain formation can enhance the vertical migration of phytoplankton through turbulence. Sci. Adv. 5 (10), eaaw7879.CrossRefGoogle Scholar
Maar, M., Visser, A.W., Nielsen, T.G., Stips, A. & Saito, H. 2006 Turbulence and feeding behaviour affect the vertical distributions of Oithona similis and Microsetella norwegica. Mar. Ecol. Prog. Ser. 313, 157172.CrossRefGoogle Scholar
Mackie, G.O., Singla, C.L. & Thiriot-Quievreux, C. 1976 Nervous control of ciliary activity in gastropod larvae. Biol. Bull. 151 (1), 182199.CrossRefGoogle ScholarPubMed
Martens, E.A., Wadhwa, N., Jacobsen, N.S., Lindemann, C., Andersen, K.H. & Visser, A. 2015 Size structures sensory hierarchy in ocean life. Proc. R. Soc. B: Biol. Sci. 282 (1815), 20151346.CrossRefGoogle ScholarPubMed
Mehlig, B. 2021 Machine Learning with Neural Networks. Cambridge University Press.CrossRefGoogle Scholar
Michalec, F.C.C.O., Souissi, S. & Holzner, M. 2015 Turbulence triggers vigorous swimming but hinders motion strategy in planktonic copepods. J. R. Soc. Interface 12 (106), 20150158.CrossRefGoogle ScholarPubMed
Millero, F.J., Chen, C., Bradshaw, A. & Schleicher, K. 1980 A new high pressure equation of state for seawater. Deep Sea Res. A. Oceanogr. Res. Papers 27 (3-4), 255264.CrossRefGoogle Scholar
Morris, M.J., Gust, G. & Torres, J.J. 1985 Propulsion efficiency and cost of transport for copepods: a hydromechanical model of crustacean swimming. Mar. Biol. 86 (3), 283295.CrossRefGoogle Scholar
Muiños-Landin, S., Fischer, A., Holubec, V. & Cichos, F. 2021 Reinforcement learning with artificial microswimmers. Sci. Robot. 6 (52), eabd9285.CrossRefGoogle ScholarPubMed
Park, J.G., Jeong, M.K., Lee, J.A., Cho, K. & Kwon, O. 2001 Diurnal vertical migration of a harmful dinoflagellate, Cochlodinium polykrikoides (Dinophyceae), during a red tide in coastal waters of Namhae Island, Korea. Phycologia 40 (3), 292297.CrossRefGoogle Scholar
Qiu, J., Huang, W., Xu, C. & Zhao, L. 2020 Swimming strategy of settling elongated micro-swimmers by reinforcement learning. Sci. China Phys. Mech. Astron. 63 (8), 284711.CrossRefGoogle Scholar
Schneider, E. & Stark, H. 2019 Optimal steering of a smart active particle. Europhys. Lett. 127 (3), 34003.CrossRefGoogle Scholar
Sengupta, A., Carrara, F. & Stocker, R. 2017 Phytoplankton can actively diversify their migration strategy in response to turbulent cues. Nature 543 (7646), 555558.CrossRefGoogle ScholarPubMed
Strickler, J.R. & Bal, A.K. 1973 Setae of the first antennae of the copepod Cyclops scutifer (Sars): their structure and importance. Proc. Natl Acad. Sci. 70 (9), 26562659.CrossRefGoogle ScholarPubMed
Sullivan, J.M., Swift, E., Donaghay, P.L. & Rines, J.E.B. 2003 Small-scale turbulence affects the division rate and morphology of two red-tide dinoflagellates. Harmful Algae 2 (3), 183199.CrossRefGoogle Scholar
Sutton, R.S. & Barto, A.G. 1998 Reinforcement Learning: An Introduction (Adaptive Computation and Machine Learning). MIT Press.Google Scholar
Taylor, G.I. 1923 VIII. Stability of a viscous liquid contained between two rotating cylinders. Phil. Trans. R. Soc. Lond. Ser. A, Contain. Pap. Math. Phys. Character 223 (605-615), 289343.Google Scholar
Titelman, J. 2001 Swimming and escape behavior of copepod nauplii: implications for predator-prey interactions among copepods. Mar. Ecol. Prog. Ser. 213, 203213.CrossRefGoogle Scholar
Titelman, J. & Kiørboe, T. 2003 Motility of copepod nauplii and implications for food encounter. Mar. Ecol. Prog. Ser. 247, 123135.CrossRefGoogle Scholar
Tsang, A.C.H., Tong, P.W., Nallan, S. & Pak, O.S. 2020 Self-learning how to swim at low Reynolds number. Phys. Rev. Fluids 5 (7), 074101.CrossRefGoogle Scholar
Verma, S., Novati, G. & Koumoutsakos, P. 2018 Efficient collective swimming by harnessing vortices through deep reinforcement learning. Proc. Natl Acad. Sci. 115 (23), 58495854.CrossRefGoogle ScholarPubMed
Visser, A. 2010 Small, Wet & Rational: Individual Based Zooplankton Ecology. Technical University of Denmark.Google Scholar
Visser, A.W. 2001 Hydromechanical signals in the plankton. Mar. Ecol. Prog. Ser. 222, 124.CrossRefGoogle Scholar
Watkins, C.J.C.H. & Dayan, P. 1992 Q-learning. Mach. Learn. 8 (3), 279292.CrossRefGoogle Scholar
Yamazaki, H. & Squires, K.D. 1996 Comparison of oceanic turbulence and copepod swimming. Mar. Ecol.-Prog. Ser. 144, 299301.CrossRefGoogle Scholar
Yen, J., Lenz, P.H., Gassie, D.V. & Hartline, D.K. 1992 Mechanoreception in marine copepods: electrophysiological studies on the first antennae. J. Plankton Res. 14 (4), 495512.CrossRefGoogle Scholar
Yen, J. & Strickler, J.R. 1996 Advertisement and concealment in the plankton: what makes a copepod hydrodynamically conspicuous? Invertebr. Biol. 191205.CrossRefGoogle Scholar
Zhao, L., Challabotla, N.R., Andersson, H.I. & Variano, E.A. 2015 Rotation of nonspherical particles in turbulent channel flow. Phys. Rev. Lett. 115 (24), 244501.CrossRefGoogle ScholarPubMed
Zhao, L., Gustavsson, K., Ni, R., Kramel, S., Voth, G.A., Andersson, H.I. & Mehlig, B. 2019 Passive directors in turbulence. Phys. Rev. Fluids 4, 054602.CrossRefGoogle Scholar