Volumetric quantification of fluid flow reveals fish's use of hydrodynamic stealth to capture evasive prey

Journal of the Royal Society Interface

Volumn 11, Issue 90, 2014, Pages

  Gemmell, Brad J ^a   Adhikari, Deepak ^a   Longmire, Ellen K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Animal fluid interaction; Hydrodynamic signals; Predation; Stealth predation; Strain rate; Tomography

Indexed keywords

ANIMAL-FLUID INTERACTION; FLUID MOTIONS; FORWARD SPEED; PARTICLE IMAGE VELOCIMETRIES; PLANKTIVOROUS FISH; PREDATION; STEALTH PREDATION; TROPHIC LEVEL;

ANIMALS; ENERGY TRANSFER; HYDRODYNAMICS; STRAIN RATE; TOMOGRAPHY;

FISH;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; COPEPOD; FEEDING; FLUID FLOW; HYDRODYNAMICS; MOUTH CAVITY; NONHUMAN; PARTICLE IMAGE VELOCIMETRY; PHARYNX; PREDATION; PREDATOR; PREY; SWIMMING; VELOCITY; ANIMAL; ANIMAL-FLUID INTERACTION; FEEDING BEHAVIOR; HYDRODYNAMIC SIGNALS; PHYSIOLOGY; STEALTH PREDATION; STRAIN RATE; TOMOGRAPHY; WATER FLOW; ZEBRA FISH;

ANIMAL-FLUID INTERACTION; HYDRODYNAMIC SIGNALS; PREDATION; STEALTH PREDATION; STRAIN RATE; TOMOGRAPHY;

ANIMALS; COPEPODA; FEEDING BEHAVIOR; HYDRODYNAMICS; PREDATORY BEHAVIOR; SWIMMING; WATER MOVEMENTS; ZEBRAFISH;

EID: 84889683164     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2013.0880     Document Type: Article

References (48)

1. Turner AM, Mittelbach GG. 1990 Predator avoidance and community structure: interactions among piscivores, planktivores, and plankton. Ecology 71, 2241-2254. (doi:10.2307/1938636)
2. Kerfoot WC, Sih A. 1987 Predation: direct and indirect impacts on aquatic communities. Hanover, NH: University Press of New England.
3. Aksnes DL, Nejstgaard J, Soedberg E, Sørnes T. 2004 Optical control of fish and zooplankton populations. Limnol. Oceanogr. 49, 233-238. (doi:10.4319/lo.2004.49.1.0233)
4. O'brien W. 1987 Planktivory by freshwater fish: thrust and parry in the pelagia. In Predation: direct and indirect impacts on aquatic communities (eds C Kerfoot, A Sih), pp. 3-16. Hanover, NH: University Press of New England.
5. Kiorboe T, Visser AW. 1999 Predator and prey perception in copepods due to hydromechanical signals. Mar. Ecol. Prog. Ser. 179, 81-95. (doi:10.3354/meps179081)
6. Visser AW. 2001 Hydromechanical signals in the plankton. Mar. Ecol. Prog. Ser. 222, 1-24. (doi:10.3354/meps222001)
7. Wainwright PC, Day SW. 2007 The forces exerted by aquatic suction feeders on their prey. J. R. Soc. Interface 4, 553-560. (doi:10.1098/rsif.2006.0197)
8. Holzman R, Wainwright PC. 2009 How to surprise a copepod: strike kinematics reduce hydrodynamic disturbance and increase stealth of suction-feeding fish. Limnol. Oceanogr. 54, 2201-2212. (doi:10.4319/lo.2009.54. 6.2201)
9. Drenner RW, Strickler JR, O'Brien WJ. 1978 Capture probability: the role of zooplankter escape in the selective feeding of planktivorous fish. J. Fish. Board Can. 35, 1370-1373. (doi:10.1139/f78-215)
10. Weihs D. 1980 Hydrodynamics of suction feeding of fish in motion. J. Fish Biol. 16, 425-433. (doi:10.1111/j.1095-8649.1980.tb03720.x)
11. Sanford CP, Wainwright PC. 2002 Use of sonomicrometry demonstrates the link between prey capture kinematics and suction pressure in largemouth bass. J. Exp. Biol. 205, 3445-3457.
12. Lowry D, Motta PJ. 2008 Relative importance of growth and behaviour to elasmobranch suction-feeding performance over early ontogeny. J. R. Soc. Interface 5, 641-652. (doi:10.1098/rsif.2007.1189)
13. Ferry-Graham LA, Wainwright PC, Lauder GV. 2003 Quantification of flow during suction feeding in bluegill sunfish. Zoology 106, 159-168. (doi:10.1078/0944-2006-00110)
14. Day SW, Higham TE, Cheer AY, Wainwright PC. 2005 Spatial and temporal patterns of water flow generated by suction-feeding bluegill sunfish Lepomis macrochirus resolved by particle image velocimetry. J. Exp. Biol. 208, 2661-2671. (doi:10.1242/jeb.01708)
15. Holzman R, Collar DC, Day SW, Bishop KL, Wainwright PC. 2008 Scaling of suction-induced flows in bluegill: morphological and kinematic predictors for the ontogeny of feeding performance. J. Exp. Biol. 211, 2658-2668. (doi:10.1242/jeb.018853)
16. Van Wassenbergh S, Aerts P. 2009 Aquatic suction feeding dynamics: insights from computational modelling. J. R. Soc. Interface 6, 149-158. (doi:10.1098/rsif.2008.0311)
17. Holzman R, Day SW, Wainwright PC. 2007 Timing is everything: coordination of strike kinematics affects the force exerted by suction feeding fish on attached prey. J. Exp. Biol. 210, 3328-3336. (doi:10.1242/jeb.008292)
18. Kiørboe T, Saiz E, Visser A. 1999 Hydrodynamic signal perception in the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 179, 97-111. (doi:10.3354/meps179097)
19. Waggett RJ, Buskey EJ. 2007 Copepod escape behavior in non-turbulent and turbulent hydrodynamic regimes. Mar. Ecol. Prog. Ser. 334, 193-198. (doi:10.3354/meps334193)
20. Fields DM, Yen J. 1997 The escape behavior of marine copepods in response to a quantifiable fluid mechanical disturbance. J. Plankton Res. 19, 1289-1304. (doi:10.1093/plankt/19.9.1289)
21. Vogel S. 1996 Life in moving fluids: the physical biology of flow. Princeton, NJ: Princeton University Press.
22. Strickler JR, Bal AK. 1973 Setae of the first antennae of the copepod Cyclops scutifer (Sars): their structure and importance. Proc. Natl Acad. Sci. USA 70, 2656-2659. (doi:10.1073/pnas.70.9.2656)
23. Buskey E, Lenz P, Hartline D. 2002 Escape behavior of planktonic copepods in response to hydrodynamic disturbances: high speed video analysis. Mar. Ecol. Prog. Ser. 235, 135-146. (doi:10.3354/meps235135)
24. Yen J, Lenz PH, Gassie DV, Hartline DK. 1992 Mechanoreception in marine copepods: electrophysiological studies on the first antennae. J. Plankton Res. 14, 495-512. (doi:10.1093/plankt/14.4.495)
25. Strickler J. 1985 Feeding currents in calanoid copepods: two new hypotheses. Physiol. Adapt. Mar. Anim. Symp. Soc. Exp. Biol. 39, 459-485.
26. Waggett RJ, Buskey EJ. 2007 Calanoid copepod escape behavior in response to a visual predator. Mar. Biol. 150, 599-607. (doi:10.1007/s00227-006-0384-3)
27. Coughlin DJ, Strickler Jr. 1990 Zooplankton capture by a coral reef fish: an adaptive response to evasive prey. Environ. Biol. Fish. 29, 35-42. (doi:10.1007/BF00000566)
28. Gemmell BJ, Buskey EJ. 2011 The transition from nauplii to copepodites: susceptibility of developing copepods to fish predators. J. Plankton Res. 33, 1773-1777. (doi:10.1093/plankt/fbr066)
29. Van Damme J, Aerts P. 1997 Kinematics and functional morphology of aquatic feeding in Australian snake-necked turtles (Pleurodira; Chelodina). J. Morphol 233, 113-125. (doi:10.1002/(SICI)1097-4687(199708)233:2<113:: AIDJMOR3>3.0.CO;2-7)
30. Lythgoe J, Partridge J. 1989 Visual pigments and the acquisition of visual information. J. Exp. Biol. 146, 1-20.
31. Stearns D, Forward R. 1984 Copepod photobehavior in a simulated natural light environment and its relation to nocturnal vertical migration. Mar. Biol. 82, 91-100. (doi:10.1007/BF00392767)
32. Epps BP, Techet AH. 2007 Impulse generated during unsteady maneuvering of swimming fish. Exp. Fluids 43, 691-700. (doi:10.1007/s00348-007-0401-4)
33. Murphy D, Webster D, Yen J. 2012 A high-speed tomographic PIV system for measuring zooplanktonic flow. Limnol. Oceanogr. Methods 10, 1096-1112. (doi:10.4319/lom.2012.10.1096)
34. Adhikari D, Longmire EK. 2013 Infrared tomographic PIV and 3D motion tracking system applied to aquatic predator-prey interaction. Meas. Sci. Technol. 24, 024011. (doi:10.1088/0957-0233/24/2/024011)
35. Adhikari D, Longmire E. 2012 Visual hull method for tomographic PIV measurement of flow around moving objects. Exp. Fluids 53, 943-964. (doi:10.1007/s00348-012-1338-9)
36. Catton KB, Webster DR, Yen J. 2012 The effect of fluid viscosity, habitat temperature, and body size on the flow disturbance of Euchaeta. Limnol. Oceanogr. Fluids Environ. 2, 80-92. (doi:10.1215/21573689-1894514)
37. Domenici P, Blake R. 1997 The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200, 1165-1178.
38. Summers AP, Darouian KF, Richmond AM, Brainerd EL. 1998 Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles. J. Exp. Zool. 281, 280-287. (doi:10.1002/(SICI)1097-010X(19980701)281:4<280::AID-JEZ4>3.0.CO;2-K)
39. Lauder GV, Prendergast T. 1992 Kinematics of aquatic prey capture in the snapping turtle Chelydra serpentina. J. Exp. Biol. 164, 55-78. (doi:10.1016/0022-0981(92)90136-X)
40. Lauder GV, Reilly SM. 1996 The mechanistic bases of behavioral evolution: a multivariate analysis of musculoskeletal function. In Phylogenies and the comparative method in animal behavior, pp. 104-137.
41. MacKenzie BR, Miller TJ, Cyr S, Leggett WC. 1994 Evidence for a dome-shaped relationship between turbulence and larval fish ingestion rates. Limnol. Oceanogr. 39, 1790-1799. (doi:10.4319/lo.1994.39.8.1790)
42. Gilbert OM, Buskey EJ. 2005 Turbulence decreases the hydrodynamic predator sensing ability of the calanoid copepod Acartia tonsa. J. Plankton Res. 27, 1067-1071. (doi:10.1093/plankt/fbi066)
43. 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, 171-181. (doi:10.3354/meps07123)
44. Hwang J-S, Strickler R. 2001 Can copepods differentiate prey from predator hydromechanically? Zool. Stud. 40, 1-6.
45. Van Duren LA, Videler JJ. 1995 Swimming behaviour of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Mar. Ecol. Prog. Ser. 126, 153-161. (doi:10.3354/meps126153)
46. Kjellerup S, Kiørboe T. 2012 Prey detection in a cruising copepod. Biol. Lett. 8, 438-441. (doi:10.1098/rsbl.2011.1073)
47. Flammang BE, Lauder GV, Troolin DR, Strand TE. 2011 Volumetric imaging of fish locomotion. Biol. Lett. 7, 695-698. (doi:10.1098/rsbl.2011.0282)
48. Flammang BE, Lauder GV, Troolin DR, Strand T. 2011 Volumetric imaging of shark tail hydrodynamics reveals a three-dimensional dualring vortex wake structure. Proc. R. Soc. B 278, 3670-3678. (doi:10.1098/rspb.2011.0489)