Animal-attached devices have transformed our understanding of vertebrate ecology. To minimize any associated harm, researchers have long advocated that tag masses should not exceed 3% of carrier body mass. However, this ignores tag forces resulting from animal movement. Using data from collar-attached accelerometers on 10 diverse free-ranging terrestrial species from koalas to cheetahs, we detail a tag-based acceleration method to clarify acceptable tag mass limits. We quantify animal athleticism in terms of fractions of animal movement time devoted to different collar-recorded accelerations and convert those accelerations to forces (acceleration × tag mass) to allow derivation of any defined force limits for specified fractions of any animal's active time. Specifying that tags should exert forces that are less than 3% of the gravitational force exerted on the animal's body for 95% of the time led to corrected tag masses that should constitute between 1.6% and 2.98% of carrier mass, depending on athleticism. Strikingly, in four carnivore species encompassing two orders of magnitude in mass (ca 2-200 kg), forces exerted by '3%' tags were equivalent to 4-19% of carrier body mass during moving, with a maximum of 54% in a hunting cheetah. This fundamentally changes how acceptable tag mass limits should be determined by ethics bodies, irrespective of the force and time limits specified.

Applied Sports Technology Exercise and Medicine Research Centre College of Engineering Swansea University Bay Campus Swansea SA1 8EN UK

College of Science Swansea University Fabian Way Swansea SA1 8EN UK

Department for the Ecology of Animal Societies Max Planck Institute of Animal Behavior Bücklestraβe 5 Konstanz D 78467 Germany

Department of Game Management and Wildlife Biology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague 165 00 Czech Republic

Germany and Department of Biology University of Konstanz Konstanz 78457 Germany

KSU Mammals Research Chair Zoology Department King Saud University Riyadh Saudi Arabia

Mammal Research Institute Department of Zoology and Entomology University of Pretoria Pretoria 0002 South Africa

Red Sea Research Centre King Abdullah University of Science and Technology Thuwal 23955 Saudi Arabia

School of Biological Sciences Queen's University Belfast Belfast BT9 5DL UK

School of Life and Environmental Sciences Deakin University Melbourne Burwood Campus 221 Burwood Highway Burwood VC 3125 Victoria Australia

Swansea Laboratory for Animal Movement Biosciences College of Science Swansea University Singleton Park Swansea SA2 8PP UK

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Proc Biol Sci. 2022 Feb 9;289(1968):20220120. doi: 10.1098/rspb.2022.0120. PubMed

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Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP. 2013. Observing the unwatchable through acceleration logging of animal behavior. Animal Biotelemetry 1, 1-20.

Kays R, Crofoot MC, Jetz W, Wikelski M. 2015. Terrestrial animal tracking as an eye on life and planet. Science 348, aaa2478. (10.1126/science.aaa2478) PubMed DOI

Wilson AM, Lowe JC, Roskilly K, Hudson PE, Golabek KA, McNutt JW. 2013. Locomotion dynamics of hunting in wild cheetahs. Nature 498, 185-189. (10.1038/nature12295) PubMed DOI

Block BA, et al. 2011. Tracking apex marine predator movements in a dynamic ocean. Nature 475, 86-90. (10.1038/nature10082) PubMed DOI

Wilson RP, McMahon CR. 2006. Measuring devices on wild animals: what constitutes acceptable practice? Front. Ecol. Environ. 4, 147-154. (10.1890/1540-9295(2006)004[0147:MDOWAW]2.0.CO;2) DOI

Saraux C, et al. 2011. Reliability of flipper-banded penguins as indicators of climate change. Nature 469, 203-206. (10.1038/nature09630) PubMed DOI

Culik BM, Wilson RP, Bannasch R. 1993. Flipper-bands on penguins: what is the cost of a life-long commitment? Marine Ecol. Progress Series 98, 209-241. (10.3354/meps098209) DOI

Rosen DA, Gerlinsky CG, Trites AW. 2017. Telemetry tags increase the costs of swimming in northern fur seals, Callorhinus ursinus. Marine Mammal Sci. 34, 385-402. (10.1111/mms.12460) DOI

Kay WP, et al. 2019. Minimizing the impact of biologging devices: using computational fluid dynamics for optimizing tag design and positioning. Methods Ecol. Evol. 10, 1222-1233. (10.1111/2041-210X.13216) DOI

Murray DL, Fuller MR. 2000. A critical review of the effects of marking on the biology of vertebrates. In Research techniques in animal ecology: controversies and consequences (eds Pearl MC, Biotani LF), pp. 15-64. New York, NY: Columbia University Press.

Stabach JA, et al. 2020. Short-term effects of GPS collars on the activity, behavior, and adrenal response of scimitar-horned oryx (Oryx dammah). PLoS ONE 15, e0221843. (10.1371/journal.pone.0221843) PubMed DOI PMC

Hopkins M, Milton K. 2016. Adverse effects of ball-chain radio-collars on female mantled howlers (Alouatta palliata) in Panama. Int. J. Primatol. 37, 213-224. (10.1007/s10764-016-9896-y) DOI

Krausman PR, Bleich VC, Cain JW III, Stephenson TR, DeYoung DW, McGarth PW, Swift PK, Pierce B,M, Jansen BD. 2004. Neck lesions in ungulates from collars incorporating satellite technology. Wildlife Soc. Bull. 1973-2006 32, 987-991.

Brooks C, Bonyongo C, Harris S. 2010. Effects of global positioning system collar weight on zebra behavior and location error. Wildlife Soc. 72, 527-534.

Rasiulis AL, Marco FB, Couturier S, Cote SD. 2014. The effect of radio-collar weight on survival of migratory caribou. J. Wildlife Manag. 78, 953-956. (10.1002/jwmg.722) DOI

Kenward RE. 2000. A manual for wildlife radio tagging. New York, NY: Academic press.

Brander RB, Cochran WW. 1969. Radio location telemetry. Washington, DC: The Wildlife Society.

Gessaman JA, Nagy KA. 1988. Transmitter loads affect the flight speed and metabolism of homing pigeons. Condor 90, 662-668. (10.2307/1368356) DOI

Thaxter CB, et al. 2016. Contrasting effects of GPS device and harness attachment on adult survival of lesser black-backed gulls Larus fascus and great skuas Stercorarius skua. Ibis 158, 279-290. (10.1111/ibi.12340) DOI

Bodey TW, Cleasby IR, Bell F, Parr N, Schultz A, Votier SC, Bearhop S. 2017. A phylogenetically controlled meta-analysis of biologging device effects on birds: deleterious effects and a call for more standardized reporting of study data. Methods Ecol. Evol. 9, 945-955.

Portugal SJ, White CR. 2018. Miniaturization of biologgers is not alleviating the 5% rule. Methods Ecol. Evol. 9, 1662-1666. (10.1111/2041-210x.13013) DOI

Barron DG, Brawn JD, Weatherhead PJ. 2010. Meta-analysis of transmitter effects on avian behaviour and ecology. Methods Ecol. Evol. 1, 180-187. (10.1111/j.2041-210X.2010.00013.x) DOI

Gleiss AC, Wilson RP, Shepard EL. 2011. Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure. Methods Ecol. Evol. 2, 23-33. (10.1111/j.2041-210X.2010.00057.x) DOI

Boutaayamou M, et al. 2015. Development and validation of an accelerometer-based method for quantifying gait events. Med. Eng. Phys. 37, 226-232. (10.1016/j.medengphy.2015.01.001) PubMed DOI

Dickenson MH, Farley CT, Full RJ, Koehl MAR, Kram R, Lehman S. 2000. How animals move: an integrative view. Science 288, 100-106. (10.1126/science.288.5463.100) PubMed DOI

Wilson RP, et al. 2020. Estimates for energy expenditure in free-living animals using acceleration proxies: a reappraisal. J. Anim. Ecol. 89, 161-172. (10.1111/1365-2656.13040) PubMed DOI PMC

Qasem L, Cardew A, Wilson A, Griffiths I, Halsey LG, Shepard ELC, Gleiss AC, Wilson R. 2012. Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector? PLoS ONE 7, e31187. (10.1371/journal.pone.0031187) PubMed DOI PMC

R Core Team. 2020. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Dewhirst OP, Evans HK, Roskilly K, Harvey RJ, Hubel TY, Wilson AM. 2016. Improving the accuracy of estimates of animal path and travel distance using GPS drift-corrected dead reckoning. Ecol. Evol. 6, 6210-6222. (10.1002/ece3.2359) PubMed DOI PMC

Wilson RP, Sala JE, Gomez-Laich A, Ciancio J, Quintana F. 2015. Pushed to the limit: food abundance determines tag-induced harm in penguins. Animal Welfare 24, 37-44. (10.7120/09627286.24.1.037) DOI

Pakanen V, Ronka N, Leslie TR, Blomqvist D, Koivula K. 2020. Survival probability in a small shorebird decreases with the time an individual carries a tracking device. J. Avian Biol. 51, e02555. (10.1111/jav.02555) DOI

Wilson RP, Grant WS, Duffy DC. 1986. Recording devices on free-ranging marine animals: does measurement affect foraging performance? Ecology 67, 1091-1093. (10.2307/1939832) DOI

Wu X, Pei B, Pei Y, Wu N, Zhou K, Hao Y, Wang W. 2019. Contributions of limb joints to energy absorption during landing in cats. Appl. Bionics Biomech 2019, 3815612. (10.1155/2019/3815612) PubMed DOI PMC

Biewener AA. 2006. Patterns of mechanical energy change in tetrapod gait: pendula, springs and work. J. Exp. Zool. A 305, 899-911. (10.1002/jez.a.334) PubMed DOI

Gregor RJ, Edgerton VR, Perrine JJ, Campion DS, DeBus C. 1979. Torque-velocity relationships and muscle fiber composition in elite female athletes. J. Appl. Physiol. 47, 388-392. (10.1152/jappl.1979.47.2.388) PubMed DOI

Alexander RM. 2002. Tendon elasticity and muscle function. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 133, 1001-1011. (10.1016/S1095-6433(02)00143-5) PubMed DOI

Farley CT, Glasheen J, McMahon TA. 1993. Running springs: speed and animal size. J. Exp. Biol. 185, 71-86. (10.1242/jeb.185.1.71) PubMed DOI

Wilson RP, Pütz K, Peters G, Culik B, Scolaro JA, Charrassin J-B, Ropert-Coudert Y. 1997. Long-term attachment of transmitting and recording devices to penguins and other seabirds. Wildlife Soc. Bull. (1973–2006) 25, 101-106.

Field IC, Harcourt RG, Boehme L, Bruyn PND, Charrassin JB, McMahon CR, Bester MN, Fedak MA, Hindell MA. 2012. Refining instrument attachment on phocid seals. Marine Mammal Sci. 28, E325-E332. (10.1111/j.1748-7692.2011.00519.x) DOI

Dickinson ER, Stephens PA, Marks NJ, Wilson RP, Scantlebury DM. 2020. Best practice for collar deployment of tri-axial accelerometers on a terrestrial quadruped to provide accurate measurement of body acceleration. Animal Biotelem. 8, 9. (10.1186/s40317-020-00198-9) DOI

Hodson-Walker N. 1970. The value of safety belts: a review. Can. Med. Assoc. J. 102, 391. PubMed PMC

Holewijn M. 1990. Physiological strain due to load carrying. Eur. J. Appl. Physiol. Occup. Physiol. 61, 237-245. (10.1007/BF00357606) PubMed DOI

Tikkanen O, Karkkainen S, Haakana P, Kallinen M, Pullinen T, Finni T. 2014. EMG, heart rate, and accelerometer as estimators of energy expenditure in locomotion. Med. Sci. Sports Exerc. 46, 1831-1839. (10.1249/MSS.0000000000000298) PubMed DOI

Young VKH, Blob RW. 2016. Comparative limb bone scaling and shape in turtles: relationships with functional demands. Integr. Comp. Biol. 56, E398.

Michael S, Gartrell B, Hunter S. 2013. Humeral remodeling and soft tissue injury of the wings caused by backpack harnesses for radio transmitters in New Zealand takahe (Porphyrio hochstetteri). J. Wildl Dis. 49, 552-559. (10.7589/2013-1-006) PubMed DOI

Pomilia MA, McNutt JW, Jorndan MR. 2015. Ecological predictors of African wild dog ranging patterns in northern Botswana. J. Mammalogy 96, 1214-1223.

Scantlebury DM, et al. 2014. Flexible energetics of cheetah hunting strategies provide resistance against kleptoparasitism. Science 346, 79-81. (10.1126/science.1256424) PubMed DOI

Pennisi E. 2011. Animal ecology. Global tracking of small animals gains momentum. Science 334, 1042. (10.1126/science.334.6059.1042) PubMed DOI

Holton MD, Wilson RP, Teilmann J, Siebert U. 2021. Animal tag technology keeps coming of age: an engineering perspective. Phil. Trans. R. Soc. Lond. B 376, 20200229. (10.1098/rstb.2020.0229) PubMed DOI PMC

Wilson RP, Spairani HJ, Coria NR, Culik BM, Adelung D. 1990. Packages for attachment to seabirds - what color do adelie penguins dislike least. J. Wildlife Manage. 54, 447-451. (10.2307/3809657) DOI

Wilson RP, et al. . 2021. Data from: Animal lifestyle affects acceptable mass limits for attached tags. Dryad Digital Repository. (10.5061/dryad.rjdfn2zbm) PubMed DOI PMC

Mammals show faster recovery from capture and tagging in human-disturbed landscapes

Development of a multisensor biologging collar and analytical techniques to describe high-resolution spatial behavior in free-ranging terrestrial mammals

A GPS assisted translocation experiment to study the homing behavior of red deer

Telemetry and Accelerometer Tracking of Green Toads in an Urban Habitat: Methodological Notes and Preliminary Findings

Animal lifestyle affects acceptable mass limits for attached tags

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