Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Open Access

Effects of temperature and viscosity on the metachronal swimming of crustaceans

Adrian Herrera-Amaya1, Nils B. Tack1, Zhipeng Lou2, Chengyu Li2, and Monica M. Wilhelmus1,*

  • *Contact author: mmwilhelmus@brown.edu

Phys. Rev. Fluids 10, 093101 – Published 10 September, 2025

DOI: https://doi.org/10.1103/l5l9-1mmm

Abstract

Temperature changes as small as 3∘C have been observed to significantly impact how self-propelled organisms move through their environment, especially for those inhabiting the transitional flow regime in which both viscous and inertial effects are important. Nonetheless, many oceanic species can successfully migrate across temperature changes in the order of 20∘C, corresponding to 40% differences in viscosity, via metachronal propulsion, suggesting that this propulsion mechanism is resilient to drastic changes in water column properties. We investigate marsh grass shrimp (Palaemon vulgaris) as a model organism to explore the combined physical and physiological effects on their locomotion at natural seasonal temperature extremes (6∘–20∘C). Experimentally, we manipulate temperature and viscosity independently to isolate physical and physiological effects. We then use the shrimp morphology and gait data to inform a computational fluid dynamics parametric study to estimate the force-to-power ratios of varying viscosity and beat frequencies through naturally occurring extremes. Our research demonstrates that shrimp do not modify their gait parameters to naturally occurring viscosity changes, and their swimming performance is impacted by less than 9%. The robustness of the metachronal gait is evidence of the ecological success of shrimp-like organisms in all climates, from the tropics to pole waters and inland freshwater.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (45)

  1. J. P. Abraham, M. Baringer, N. L. Bindoff, T. Boyer, L. J. Cheng, J. A. Church, J. L. Conroy, C. M. Domingues, J. T. Fasullo, J. Gilson, G. Goni, S. A. Good, J. M. Gorman, V. Gouretski, M. Ishii, G. C. Johnson, S. Kizu, J. M. Lyman, A. M. Macdonald, W. J. Minkowycz et al., A review of global ocean temperature observations: Implications for ocean heat content estimates and climate change, Rev. Geophys. 51, 450 (2013).
  2. R. D. Podolsky and R. B. Emlet, Separating the effects of temperature and viscosity on swimming and water movement by sand dollar larvae (Dendraster Excentricus), J. Exp. Biol. 176, 207 (1993).
  3. G. Koumoundouros, D. G. Sfakianakis, P. Divanach, and M. Kentouri, Effect of temperature on swimming performance of sea bass juveniles, J. Fish Biol. 60, 923 (2002).
  4. P. Larsen, C. Madsen, and H. Riisgård, Effect of temperature and viscosity on swimming velocity of the copepod Acartia tonsa, brine shrimp Artemia salina and rotifer Brachionus plicatilis, Aquat. Biol. 4, 47 (2008).
  5. B. J. Gemmell, J. Sheng, and E. J. Buskey, Compensatory escape mechanism at low Reynolds number, Proc. Natl. Acad. Sci. USA 110, 4661 (2013).
  6. L. A. Fuiman and R. S. Batty, What a drag it is getting cold: Partitioning the physical and physiological effects of temperature on fish swimming, J. Exp. Biol. 200, 1745 (1997).
  7. T. P. Johnson, A. J. Cullum, and A. F. Bennett, Partitioning the effects of temperature and kinematic viscosity on the C-start performance of adult fishes, J. Exp. Biol. 201, 2045 (1998).
  8. M. L. Byron, D. W. Murphy, K. Katija, A. P. Hoover, J. Daniels, K. Garayev, D. Takagi, E. Kanso, B. J. Gemmell, M. Ruszczyk, and A. Santhanakrishnan, Metachronal Motion across scales: Current challenges and future directions, Integr. Comp. Biol. 61, 1674 (2021).
  9. J. Bird, The Wonders of the Seas: Arthropods (Oceanic Research Group, North Reading, MA, 2022).
  10. M. Ruszczyk, D. R. Webster, and J. Yen, Trends in stroke kinematics, reynolds number, and swimming mode in shrimp-like organisms, Integr. Comp. Biol. 62, 791 (2022).
  11. D. W. Murphy, D. R. Webster, S. Kawaguchi, R. King, and J. Yen, Metachronal swimming in Antarctic krill: Gait kinematics and system design, Mar. Biol. 158, 2541 (2011).
  12. D. Bianchi, C. Stock, E. D. Galbraith, and J. L. Sarmiento, Diel vertical migration: Ecological controls and impacts on the biological pump in a one-dimensional ocean model, Global Biogeochem. Cycles 27, 478 (2013)20031.
  13. K. Meland, J. Mees, M. Porter, and K. J. Wittmann, Taxonomic review of the orders mysida and stygiomysida (Crustacea, Peracarida), PLoS ONE 10, e0124656 (2015).
  14. D. W. Murphy, D. R. Webster, and J. Yen, The hydrodynamics of hovering in Antarctic krill, Limnol. Oceanogr. Fluids Environ. 3, 240 (2013),.
  15. S. E. Hanson, W. J. Ray, A. Santhanakrishnan, and S. N. Patek, Mantis shrimp locomotion: Coordination and variation of hybrid metachronal swimming, Integr. Org. Biol. 5, obad019 (2023).
  16. K. Garayev and D. W. Murphy, Metachronal swimming of mantis shrimp: Kinematics and interpleopod vortex interactions, Integr. Comp. Biol. 61, 1631 (2021).
  17. S. Alben, K. Spears, S. Garth, D. Murphy, and J. Yen, Coordination of multiple appendages in drag-based swimming, J. R. Soc. Interface 7, 1545 (2010).
  18. S. Granzier-Nakajima, R. D. Guy, and C. Zhang-Molina, A numerical study of metachronal propulsion at low to intermediate Reynolds numbers, Fluids 5, 86 (2020).
  19. M. P. Ford, H. K. Lai, M. Samaee, and A. Santhanakrishnan, Hydrodynamics of metachronal paddling: Effects of varying Reynolds number and phase lag, R. Soc. Open Sci. 6, 191387 (2019).
  20. S. Oliveira Santos, N. Tack, Y. Su, F. Cuenca-Jiménez, O. Morales-Lopez, P. A. Gomez-Valdez, and M. M. Wilhelmus, Pleobot: A modular robotic solution for metachronal swimming, Sci. Rep. 13, 9574 (2023).
  21. N. B. Tack, S. O. Santos, and M. M. Wilhelmus, Going around the bend to understand the role of leg coalescence in metachronal swimming, J. Exp. Biol. 228, jeb249330 (2025).
  22. M. Mantovani and J. C. McNamara, Contrasting strategies of osmotic and ionic regulation in freshwater crabs and shrimps: Gene expression of gill ion transporters, J. Exp. Biol. 224, jeb233890 (2021).
  23. S. W. Nixon, S. Granger, B. A. Buckley, M. Lamont, and B. Rowell, A one hundred and seventeen year coastal water temperature record from Woods Hole, Massachusetts, Estuaries 27, 397 (2004).
  24. S. A. Baba and Y. Hiramoto, A quantitative analysis of ciliary movement by means of high-speed microcinematography, J. Exp. Biol. 52, 675 (1970).
  25. R. Mittal, H. Dong, M. Bozkurttas, F. M. Najjar, A. Vargas, and A. von Loebbecke, A versatile sharp interface immersed boundary method for incompressible flows with complex boundaries, J. Comput. Phys. 227, 4825 (2008).
  26. M. R. Visbal and D. P. Rizzetta, Large-eddy simulation on curvilinear grids using compact differencing and filtering schemes, J. Fluids Eng. 124, 836 (2002).
  27. T. E. Tezduyar, Finite element methods for fluid dynamics with moving boundaries and interfaces, in Encyclopedia of Computational Mechanics (John Wiley & Sons, New York, 2004), Sec. 17.
  28. C. Li, H. Dong, and K. Zhao, A balance between aerodynamic and olfactory performance during flight in Drosophila, Nat. Commun. 9, 3215 (2018).
  29. Z. Lou, M. Lei, H. Dong, and C. Li, Wing–antenna interaction reduces odour fatigue in butterfly odour-tracking flight, J. Fluid Mech. 998, A45 (2024).
  30. S. Lionetti, M. Lei, T. L. Hedrick, and C. Li, Benefits of low-speed flight in odor-tracking navigation for hawkmoths, Phys. Fluids 37, 021911 (2025).
  31. S. Lionetti, Z. Lou, A. Herrera-Amaya, M. L. Byron, and C. Li, A new propulsion enhancement mechanism in metachronal rowing at intermediate Reynolds numbers, J. Fluid Mech. 974, A45 (2023).
  32. C. Li, J. Jiang, H. Dong, and K. Zhao, Computational modeling and validation of human nasal airflow under various breathing conditions, J. Biomech. 64, 59 (2017).
  33. S. Lionetti, T. L. Hedrick, and C. Li, Aerodynamic explanation of flight speed limits in hawkmoth-like flapping-wing insects, Phys. Rev. Fluids 7, 093104 (2022).
  34. Z. Lou, N. Tack, M. M. Wilhelmus, and C. Li, Edge vortex interaction minimizes drag in shrimp swimming, Phys. Rev. Fluids 10, 043103 (2025).
  35. K. Schmidt-Nielsen, Animal Physiology: Adaptation and Environment, 5th ed. (Cambridge University Press, Cambridge, England, 1997).
  36. J. A. Walker, Functional morphology and virtual models: Physical constraints on the design of oscillating wings, fins, legs, and feet at intermediate reynolds numbers, Integr. Comp. Biol. 42, 232 (2002).
  37. M. P. Ford, W. J. Ray, E. M. DiLuca, S. N. Patek, and A. Santhanakrishnan, Hybrid metachronal rowing augments swimming speed and acceleration via increased stroke amplitude, Integr. Comp. Biol. 61, 1619 (2021).
  38. See Supplemental Material at http://link.aps.org/supplemental/10.1103/l5l9-1mmm for the time-resolved vorticity field of the shrimp CFD simulation.
  39. A. Herrera-Amaya and M. L. Byron, Propulsive efficiency of spatiotemporally asymmetric oscillating appendages at intermediate Reynolds numbers, Bioinspir. Biomim. 19, 066004 (2024).
  40. D. Barlow and M. A. Sleigh, Water propulsion speeds and power output by comb plates of the ctenophore pleurobrachia pileus under different conditions, J. Exp. Biol. 183, 149 (1993).
  41. R. T. Bauer, The Shrimps: An Overview, in Shrimps: Their Diversity, Intriguing Adaptations and Varied Lifestyles, edited by R. T. Bauer (Springer International, Cham, Switzerland, 2023), pp. 1–17.
  42. I. R. Jenkinson, Oceanographic implications of non-newtonian properties found in phytoplankton cultures, Nature (London) 323, 435 (1986).
  43. L. Seuront, D. Vincent, and J. G. Mitchell, Biologically induced modification of seawater viscosity in the Eastern English Channel during a Phaeocystis globosa spring bloom, J. Mar. Syst.Workshop Future Directions Modelling Physical-Biological Interactions (WKFDPBI), 61, 118 (2006).
  44. L. Seuront and D. Vincent, Increased seawater viscosity, Phaeocystis globosa spring bloom and Temora longicornis feeding and swimming behaviours, Mar. Ecol. Prog. Ser. 363, 131 (2008).
  45. A. Herrera-Amaya, N. B. Tack, Z. Lou, C. Li, and M. M. Wilhelmus, Data for Effects of temperature and viscosity on the metachronal swimming of crustaceans, https://doi.org/10.26300/v2jt-ar26 (2025).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation