Energetics of collective movement in vertebrates

Yangfan Zhang; George V. Lauder

doi:10.1242/jeb.245617

journal article Oct 15, 2023

Energetics of collective movement in vertebrates

Yangfan Zhang

George V. Lauder

Journal of Experimental Biology Vol. 226 No. 20 · The Company of Biologists

View at Publisher Save 10.1242/jeb.245617

Abstract

ABSTRACT
The collective directional movement of animals occurs over both short distances and longer migrations, and is a critical aspect of feeding, reproduction and the ecology of many species. Despite the implications of collective motion for lifetime fitness, we know remarkably little about its energetics. It is commonly thought that collective animal motion saves energy: moving alone against fluid flow is expected to be more energetically expensive than moving in a group. Energetic conservation resulting from collective movement is most often inferred from kinematic metrics or from computational models. However, the direct measurement of total metabolic energy savings during collective motion compared with solitary movement over a range of speeds has yet to be documented. In particular, longer duration and higher speed collective motion must involve both aerobic and non-aerobic (high-energy phosphate stores and substrate-level phosphorylation) metabolic energy contributions, and yet no study to date has quantified both types of metabolic contribution in comparison to locomotion by solitary individuals. There are multiple challenging questions regarding the energetics of collective motion in aquatic, aerial and terrestrial environments that remain to be answered. We focus on aquatic locomotion as a model system to demonstrate that understanding the energetics and total cost of collective movement requires the integration of biomechanics, fluid dynamics and bioenergetics to unveil the hydrodynamic and physiological phenomena involved and their underlying mechanisms.

Topics

No keywords indexed for this article. Browse by subject →

References

114

[1]

Abrahams "Risk of predation, hydrodynamic efficiency and their influence on school structure" Environ. Biol. Fishes (1985) 10.1007/bf00000931

[2]

Adams "An unusually high upper thermal acclimation potential for rainbow trout" Conserv. Physiol. (2022) 10.1093/conphys/coab101

[3]

Alexander "The U, J and L of bird flight" Nature (1997) 10.1038/36196

[4]

Baudinette "Energetic cost of locomotion in the tammar wallaby" Am. J. Physiol. Regul. Integr. Comp. Physiol. (1992) 10.1152/ajpregu.1992.262.5.r771

[5]

Blocken "Aerodynamic drag in cycling pelotons: New insights by CFD simulation and wind tunnel testing" J. Wind Eng. Ind. Aerodyn. (2018) 10.1016/j.jweia.2018.06.011

[6]

Borazjani "Hydrodynamics of the bluegill sunfish C-start escape response: Three-dimensional simulations and comparison with experimental data" J. Exp. Biol. (2012) 10.1242/jeb.063016

[7]

Brehmer "Exploratory and instantaneous swimming speeds of amphidromous fish school in shallow-water coastal lagoon channels" Estuaries Coasts (2011) 10.1007/s12237-011-9409-3

[8]

Brett "Some considerations in the study of respiratory metabolism in fish, particularly salmon" J. Fish. Res. Board Can. (1962) 10.1139/f62-067

[9]

The Respiratory Metabolism and Swimming Performance of Young Sockeye Salmon

J. R. Brett

Journal of the Fisheries Research Board of Canada 1964 10.1139/f64-103

[10]

The Science and Translation of Lactate Shuttle Theory

George A. Brooks

Cell Metabolism 2018 10.1016/j.cmet.2018.03.008

[11]

Browning "Energetic cost and preferred speed of walking in obese vs. Normal weight women" Obesity Res. (2005) 10.1038/oby.2005.103

[12]

Calicchia "Reconstructing the pressure field around swimming fish using a physics-informed neural network" J. Exp. Biol. (2023) 10.1242/jeb.244983

[13]

Castro-Santos "Optimal swim speeds for traversing velocity barriers: An analysis of volitional high-speed swimming behavior of migratory fishes" J. Exp. Biol. (2005) 10.1242/jeb.01380

[14]

Cavagna "Mechanical work in terrestrial locomotion: Two basic mechanisms for minimizing energy expenditure" Am. J. Physiol. Regul. Integr. Comp. Physiol. (1977) 10.1152/ajpregu.1977.233.5.r243

[15]

Chiara "AnimalTA: A highly flexible and easy-to-use program for tracking and analysing animal movement in different environments" Methods Ecol. Evol. (2023) 10.1111/2041-210x.14115

[16]

Claireaux "Responses by fishes to environmental hypoxia: Integration through Fry's concept of aerobic metabolic scope" J. Fish Biol. (2016) 10.1111/jfb.12833

[17]

Clark "Hovering and forward flight energetics in Anna's and Allen's hummingbirds" Physiol. Biochem. Zool. (2010) 10.1086/653477

[18]

Conley "Limits to sustainable muscle performance: Interaction between glycolysis and oxidative phosphorylation" J. Exp. Biol. (2001) 10.1242/jeb.204.18.3189

[19]

Currier "Group swimming behaviour and energetics in bluegill Lepomis macrochirus and rainbow trout Oncorhynchus mykiss" J. Fish Biol. (2021) 10.1111/jfb.14641

[20]

Cygankiewicz "Heart rate variability" (2013) 10.1016/b978-0-444-53491-0.00031-6

[21]

Dabiri "An algorithm to estimate unsteady and quasi-steady pressure fields from velocity field measurements" J. Exp. Biol. (2014) 10.1242/jeb.092767

[22]

Daghooghi "The hydrodynamic advantages of synchronized swimming in a rectangular pattern" Bioinspir. Biomim. (2015) 10.1088/1748-3190/10/5/056018

[23]

Dawson "Energetic cost of locomotion in kangaroos" Nature (1973) 10.1038/246313a0

[24]

Di Santo "High postural costs and anaerobic metabolism during swimming support the hypothesis of a U-shaped metabolism–speed curve in fishes" Proc. Natl Acad. Sci. USA (2017) 10.1073/pnas.1715141114

[25]

Dial "Mechanical power output of bird flight" Nature (1997) 10.1038/36330

[26]

Dong "Wake topology and hydrodynamic performance of low-aspect-ratio flapping foils" J. Fluid Mech. (2006) 10.1017/s002211200600190x

[27]

Locomotor forces on a swimming fish: three-dimensional vortex wake dynamics quantified using digital particle image velocimetry

Eliot G. Drucker, George V. Lauder

Journal of Experimental Biology 1999 10.1242/jeb.202.18.2393

[28]

Eliason "Differences in thermal tolerance among sockeye salmon populations" Science (2011) 10.1126/science.1199158

[29]

Tomographic particle image velocimetry

G. E. Elsinga, F. Scarano, B. Wieneke et al.

Experiments in Fluids 2006 10.1007/s00348-006-0212-z

[30]

Farrell "Cardiorespiratory performance during prolonged swimming tests with salmonids: A perspective on temperature effects and potential analytical pitfalls" Philos. Trans. R. Soc. B Biol. Sci. (2007) 10.1098/rstb.2007.2111

[31]

Farrell "Tribute to P. L. Lutz: a message from the heart – why hypoxic bradycardia in fishes?" J. Exp. Biol. (2007) 10.1242/jeb.02781

[32]

Farrell "On-line venous oxygen tensions in rainbow trout during graded exercise at two acclimation temperatures" J. Exp. Biol. (2003) 10.1242/jeb.00100

[33]

Fish "Energy conservation by formation swimming: Metabolic evidence from ducklings" (1994) 10.1017/cbo9780511983641.014

[34]

Fish "Kinematics of ducklings swimming in formation: Consequences of position" J. Exp. Zool. (1995) 10.1002/jez.1402730102

[35]

Fish "Dolphin swimming–a review" Mammal. Rev. (1991) 10.1111/j.1365-2907.1991.tb00292.x

[36]

Fish "Hydrodynamic performance of aquatic flapping: efficiency of underwater flight in the Manta" Aerospace (2016) 10.3390/aerospace3030020

[37]

Flammang "Volumetric imaging of fish locomotion" Biol. Lett. (2011) 10.1098/rsbl.2011.0282

[38]

Fry (1947)

[39]

Fry "The relation of temperature to oxygen consumption in the goldfish" Biol. Bull. (1948) 10.2307/1538211

[40]

Gaesser "Metabolic bases of excess post-exercise oxygen consumption: a review" Med. Sci. Sports Exerc. (1984) 10.1249/00005768-198401000-00008

[41]

Gemelli "Oxidation of lactate in the compact and spongy myocardium of tuna fish (Thunnus thynnus thynnus L.)" Comp. Biochem. Physiol. B Comp. Biochem. (1980) 10.1016/0305-0491(80)90020-6

[42]

Haykowsky "Determinants of exercise intolerance in patients with heart failure and reduced or preserved ejection fraction" J. Appl. Physiol. (2015) 10.1152/japplphysiol.00049.2015

[43]

He "Tilting behaviour of the Atlantic mackerel, Scomber scombrus, at low swimming speeds" J. Fish Biol. (1986) 10.1111/j.1095-8649.1986.tb05013.x

[44]

Hedenström "High-speed stereo DPIV measurement of wakes of two bat species flying freely in a wind tunnel" (2010) 10.1007/978-3-642-11633-9_28

[45]

Herbert-Read "Understanding how animal groups achieve coordinated movement" J. Exp. Biol. (2016) 10.1242/jeb.129411

[46]

Hochachka "Protons and anaerobiosis" Science (1983) 10.1126/science.6298937

[47]

Holder "Are we any closer to understanding why fish can die after severe exercise?" Fish Fisher. (2022) 10.1111/faf.12696

[48]

Hoppeler "Endurance training in humans: Aerobic capacity and structure of skeletal muscle" J. Appl. Physiol. (1985) 10.1152/jappl.1985.59.2.320

[49]

Hoyt "Gait and the energetics of locomotion in horses" Nature (1981) 10.1038/292239a0

[50]

Ito "Aerodynamic effects by marathon pacemakers on a main runner" Trans. Jpn. Soc. Mech. Eng. B (2007) 10.1299/kikaib.73.1975

Showing 50 of 114 references

Metrics

31

Citations

114

References

Details

Published: Oct 15, 2023
Vol/Issue: 226(20)

Authors

Y

Yangfan Zhang

Harvard University Department of Organismic and Evolutionary Biology , , 26 Oxford Street , Cambridge, MA 02138 , USA

G

George V. Lauder

Harvard University Department of Organismic and Evolutionary Biology , , 26 Oxford Street , Cambridge, MA 02138 , USA

Funding

National Science Foundation Award: EFRI-830881

Natural Sciences and Engineering Research Council of Canada Award: PDF-557785-2021

Office of Naval Research Award: N00014-18-1-2673

Cite This Article

Yangfan Zhang, George V. Lauder (2023). Energetics of collective movement in vertebrates. Journal of Experimental Biology, 226(20). https://doi.org/10.1242/jeb.245617

Energetics of collective movement in vertebrates

You May Also Like