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Metachronal swimming in Antarctic krill: gait kinematics and system design

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Abstract

Metachronal swimming, in which adjacent appendages stroke in sequence, is widespread among crustaceans inhabiting the transitional flow realm in which both viscosity and inertia effects are important. However, the design and operation of this propulsion system in response to various hydrodynamic, energetic, and behavioral needs have not been well investigated. We examine free-swimming Antarctic krill (Euphausia superba) as a model species and identify three distinct behavioral swimming gaits. The pleopod kinematics of these gaits, hovering, fast-forward swimming, and upside-down swimming, are quantified via image analysis of high-speed video. Pleopod stroke amplitude and frequency were found to vary significantly among these swimming modes. In order to increase swimming speed, krill were found first to increase stroke amplitude and secondarily to increase beat frequency. The kinematics of these distinct swimming modes provide insight as we consider multi-appendage metachronal swimming from a design standpoint. The ratio of the distance between adjacent appendage bases and appendage length is identified as a key parameter in metachrony, the value of which is constrained to a narrow range for a wide variety of species.

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References

  • Alben S, Spears K, Garth S, Murphy D, Yen J (2010) Coordination of multiple appendages in drag-based swimming. J R Soc Interface 7:1545–1557

    Article  Google Scholar 

  • Alexander DE (1988) Kinematics of swimming in two species of Idotea (Isopoda: Valvifera). J Exp Biol 138:37–49

    Google Scholar 

  • Alexander RM (2003) Principles of Animal Locomotion. Princeton University Press, Princeton

    Book  Google Scholar 

  • Anker A (2010) The shrimp genus Salmoneus Holthuis, 1955 (Crustacea, Decapoda, Alpheidae) in the tropical western Atlantic, with description of five new species. Zootaxa 2372:177–205

    Google Scholar 

  • Borazjani I, Sotiropoulos F, Malkiel E, Katz J (2010) On the role of copepod antennae in the production of hydrodynamic force during hopping. J Exp Biol 213:3019–3035

    Article  Google Scholar 

  • Boudrias MA (2002) Are pleopods just “more legs”? The functional morphology of swimming limbs in Eurythenes gryllus (Amphipoda). J Crustacean Biol 22:581–594

    Article  Google Scholar 

  • Campos EO (2009) Quick forward escape swimming in the stomatopod crustacean Odontodactylus havanensis. Berkeley McNair Res J 16:1–14

    Google Scholar 

  • Catton KB, Webster DR, Brown J, Yen J (2007) Quantitative analysis of tethered and free-swimming copepodid flow fields. J Exp Biol 210:299–310

    Article  Google Scholar 

  • Catton KB, Webster DR, Kawaguchi S, Yen J (2011) The hydrodynamic wake of two species of krill: Implications for signaling among schooling krill. J Exp Biol 214:1845–1856

    Article  Google Scholar 

  • Cheer AYL, Koehl MAR (1987) Paddles and rakes: fluid flow through bristled appendages of small organisms. J Theor Biol 129:17–39

    Article  Google Scholar 

  • Cowles DL (1994) Swimming dynamics of the mesopelagic vertically migrating penaeid shrimp Sergestes similis: Modes and speeds of swimming. J Crustacean Biol 14:247–257

    Article  Google Scholar 

  • Davis WJ (1968) Quantitative analysis of swimmeret beating in the lobster. J Exp Biol 48:643–662

    Google Scholar 

  • Ellington CP (1984) The aerodynamics of hovering insect flight. III. Kinematics. Phil Trans R Soc Lond B 305:41–78

    Article  Google Scholar 

  • Goldthwait S, Yen J, Brown J, Alldredge A (2004) Quantification of marine snow fragmentation by swimming euphausiids. Limnol Oceanogr 49(4):940–952

    Article  Google Scholar 

  • Hessler RR (1985) Swimming in crustacea. Trans R Soc Edinb 76:115–122

    Article  Google Scholar 

  • Ivanenko VN, Defaye D, Cuoc C (2007) A new calanoid copepod (Spinocalanidae) swarming at a cold seep site on the Gabon continental margin (Southeast Atlantic). Cah Biol Mar 48:37–54

    Google Scholar 

  • Jiang H, Kiørboe T (2011) Propulsion efficiency and imposed flow fields of a copepod jump. J Exp Biol 214:476–486

    Article  Google Scholar 

  • Johnson ML, Tarling GA (2008) Influence of individual state on swimming capacity and behaviour of Antarctic krill Euphausia superba. Mar Ecol Prog Ser 366:99–110

    Article  Google Scholar 

  • Kanda K, Takagi K, Seki Y (1982) Movement of the larger swarms of Antarctic krill Euphausia superba population off Enderby Land during 1976–1977 season. J Tokyo U Fish 68:25–42

    Google Scholar 

  • Kawaguchi S, King R, Meijers R, Osborn JE, Swadling KM, Ritz DA, Nicol S (2010) An experimental aquarium for observing the schooling behaviour of Antarctic krill (Euphausia superba). Deep-Sea Research II 57:683–692

    Article  Google Scholar 

  • Kils U (1981) Swimming behaviour, swimming performance, and energy balance of Antarctic krill, Euphausia superba. BIOMASS Sci Ser 3:1–122

    Google Scholar 

  • Kiørboe T, Andersen A, Langlois V, Jakobsen H (2010) Unsteady motion: escape jumps in planktonic copepods, their kinematics and energetics. J R Soc Interface 7:1591–1602

    Article  Google Scholar 

  • Knight-Jones EW, Macfadyen A (1959) The metachronism of limb and body movements in annelids and arthropods. Proc XVth Int Cong Zool, pp 969–971

  • Kohlhage K, Yager J (1994) An analysis of swimming in remipede crustaceans. Phil Trans R Soc Lond B 346:213–221

    Article  Google Scholar 

  • Laverack MS, Neil DM, Robertson RM (1977) Metachronal exopodite beating in the mysid Praunus flexuosus: a quantitative analysis. Proc R Soc Lond B 198:139–154

    Article  Google Scholar 

  • Lenz PH, Hower AE, Hartline DK (2004) Force production during pereiopod power strokes in Calanus finmarchicus. J Mar Syst 49:133–144

    Article  Google Scholar 

  • Lim JL, DeMont ME (2009) Kinematics, hydrodynamics and force production of pleopods suggest jet-assisted walking in the American lobster (Homarus americanus). J Exp Biol 212:2731–2745

    Article  Google Scholar 

  • Macmillan DL, Neil DM, Laverack MS (1976) A quantitative analysis of exopodite beating in the larvae of the lobster Homarus gammarus (L.). Phil Trans R Soc Lond B 274:69–85

    Article  CAS  Google Scholar 

  • Miyashita K, Aoki I, Inagaki T (1996) Swimming behaviour and target strength of isada krill (Euphausia pacifica). ICES J Mar Sci 53:303–308

    Article  Google Scholar 

  • Morgan E (1972) The swimming of Nymphon gracile (Pycnogonida): the swimming gait. J Exp Biol 56:421–432

    CAS  PubMed  Google Scholar 

  • Nicol S, Endo Y (1997) Krill fisheries of the world. FAO Fisheries Technical Paper. No. 367. FAO, Rome, pp 1–100

    Google Scholar 

  • Patria MP, Wiese K (2004) Swimming in formation in krill (Euphausiacea), a hypothesis: dynamics of the flow field, properties of antennular sensor systems and a sensory-motor link. J Plankton Res 26:1315–1325

    Article  Google Scholar 

  • Schabes M, Hamner W (1992) Mysid locomotion and feeding: Kinematics and water-flow patterns of Antarctomysis sp., Acanthomysis sculpta, and Neomysis rayii. J Crustacean Biol 12:1–10

    Article  Google Scholar 

  • Sensenig AT, Kiger KT, Shultz JW (2009) The rowing-to-flapping transition: ontogenetic changes in gill-plate kinematics in the nymphal mayfly Centroptilum triangulifer (Ephemeroptera, Baetidae). Biol J Linn Soc 98:540–555

    Article  Google Scholar 

  • Sleigh MA, Barlow DI (1980) Metachronism and control of locomotion in animals with many propulsive structures. In: Elder HY, Trueman ER (eds) Aspects of animal movement. Cambridge University Press, Cambridge, pp 49–70

    Google Scholar 

  • Stamhuis EJ, Videler JJ (1998a) Burrow ventilation in the tube-dwelling shrimp (Callianassa subterranea (Decapoda: Thalassinidea). I. Morphology and motion of the pleopods, uropods and telson. J Exp Biol 201:2151–2158

    CAS  PubMed  Google Scholar 

  • Stamhuis EJ, Videler JJ (1998b) Burrow ventilation in the tube-dwelling shrimp (Callianassa subterranea Decapoda: Thalassinidea). II. The flow in the vicinity of the shrimp and the energetic advantages of a laminar non-pulsating ventilation current. J Exp Biol 201:2159–2170

    CAS  PubMed  Google Scholar 

  • Stretch JJ, Hamner PP, Hamner WH, Michel WC, Cook J, Sullivan CW (1988) Foraging behavior of Antarctic krill Euphausia superba on sea ice microalgae. Mar Ecol Prog Ser 44:131–139

    Article  Google Scholar 

  • Swadling KM, Ritz DA, Nicol S, Osborn JE (2005) Respiration rate and cost of swimming for Antaractic krill, Euphausia superba, in large groups in the laboratory. Mar Biol 146:1169–1175

    Article  Google Scholar 

  • Tarling GA, Johnson ML (2006) Satiation gives krill that sinking feeling. Curr Biol 16(3):83–84

    Article  Google Scholar 

  • van Duren LA, Videler JJ (2003) Escape from viscosity: the kinematics and hydrodynamics of copepod foraging and escape swimming. J Exp Biol 206:269–279

    Article  Google Scholar 

  • Vannier J, Boissy P, Racheboeuf PR (1997) Locomotion in Nebalia bipes: a possible model for Palaeozoic phyllocarid crustaceans. Lethaia 30:89–104

    Article  Google Scholar 

  • Walker JA (2002) Functional morphology and virtual models: physical constraints on the design of oscillating wings, fins, and feet at intermediate Reynolds numbers. Integr Comp Biol 42:232–242

    Article  Google Scholar 

  • Wootton RJ (1999) Invertebrate paraxial locomotory appendages: design, deformation and control. J Exp Biol 202:3333–3345

    CAS  PubMed  Google Scholar 

  • Yen J, Strickler JR (1996) Advertisement and concealment in the plankton: what makes a copepod hydrodynamically conspicuous? Invertebr Biol 115:191–205

    Article  Google Scholar 

  • Yen J, Brown J, Webster DR (2003) Analysis of the flow field of the krill, Euphausia pacifica. Mar Fresh Behav Physiol 36:307–319

    Article  Google Scholar 

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Acknowledgments

This work was supported by a National Science Foundation East Asia–Pacific Summer Institute Award to D.W.M. and by National Science Foundation grant OCE-0928491 to J.Y. and D.R.W. The authors thank Nadir Kabir and Morgan Stephenson for help with data digitization and Rachel Lasley for help with statistics. All experiments complied with the current laws of the country in which they were performed. The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, GA, 30332-0355, USA

    D. W. Murphy & D. R. Webster

  2. Australian Antarctic Division, Kingston, TAS, 7050, Australia

    S. Kawaguchi & R. King

  3. School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332-0230, USA

    J. Yen

Authors
  1. D. W. Murphy
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  2. D. R. Webster
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  3. S. Kawaguchi
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  4. R. King
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  5. J. Yen
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Correspondence to D. W. Murphy.

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Communicated by A. Atkinson.

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Murphy, D.W., Webster, D.R., Kawaguchi, S. et al. Metachronal swimming in Antarctic krill: gait kinematics and system design. Mar Biol 158, 2541–2554 (2011). https://doi.org/10.1007/s00227-011-1755-y

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  • DOI: https://doi.org/10.1007/s00227-011-1755-y

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