Abstract
The prerogative of animal welfare science includes wild species and ecological studies. Yet, guidance enshrined in legislation is narrowly derived from studies involving laboratory rodents; legitimacy for non-mammalian free-ranging species is thus debatable. The European directive 2010/63/EU illustrates this problem. It includes this key statement: “Practices not likely to cause pain, suffering, distress or lasting harm equivalent to, or higher than, that caused by the introduction of a needle…” which determines if the directive shall apply. Protocols involving surgery clearly fall within the scope of the directive: procedures are scrutinized, investigators and technicians must be qualified and various agreements are required (e.g. issued by an ethical committee). By contrast, non-invasive procedures, like mark-recapture population studies, merely need a permit from wildlife authorities (at least in most countries). Yet, blood sampling that implies the introduction of a needle—one of the most common practices in animals—could shift any study on the constraining-side of the directive, on the grounds that puncture impacts individuals more severely than capture. We examined the validity of the needle-threshold using the stress response of free-ranging snakes. Our results based on physiological markers show that blood sampling does not add any stress to that triggered by capture, and thus questions the usefulness of the needle-threshold to gauge welfare in wild animals. The specificities of studying wild species should be considered to redress captivity biased animal welfare policy.
Similar content being viewed by others
References
Adamo SA (2019) Is it pain if it does not hurt? On the unlikelihood of insect pain. Can Entomol. https://doi.org/10.4039/tce.2019.49
Adler S, Basketter D, Creton S, Pelkonen O et al (2011) Alternative (non-animal) methods for cosmetics testing: current status and future prospects—2010. Arch Toxicol 85:367–485
Ajtić R, Tomović L, Sterijovski B, Crnobrnja-Isailović J, Djordjević S, Djurakić M, Golubović A, Simović A, Arsovski D, Andjelković M, Krstić M, Sukalo G, Gvozdenović S, Aïdam A, Michel CL, Ballouard JM, Bonnet X (2013) Unexpected life history traits in a very dense population of dice snakes. Zoologischer Anzeiger 252:350–358
Bonnet X, Fizesan A, Michel CL (2013) Shelter availability, stress level and digestive performance in the aspic viper. J Exp Biol 216:815–822
Broom DM, Galindo FA, Murgueitio E (2013) Sustainable, efficient livestock production with high biodiversity and good welfare for animals. Proc R Soc B 280:20132025
Brown MB, Brown CR (2009) Blood sampling reduces annual survival in cliff swallows (Petrochelidon pyrrhonota). Auk 126:853–861
Burghardt GM (2009) Ethics and animal consciousness: How rubber the ethical ruler? J Soc Issues 65:499–521
Carsten J (2011) Substance and relationality: blood in contexts. Annu Rev Anthropol 40:19–35
Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381
Clewley GD, Robinson RA, Clark JA (2018) Estimating mortality rates among passerines caught for ringing with mist nets using data from previously ringed birds. Ecol Evol 8:5164–5172
Clippinger AJ, Hill E, Curren R, Bishop P (2016) Bridging the gap between regulatory acceptance and industry use of non-animal methods. ALTEX Altern Anim Exp 33:453–458
Costantini D, Møller AP (2013) A meta-analysis of the effects of geolocator application on birds. Curr Zool 59:697–706
Dawkins MS (2017) Animal welfare and efficient farming: is conflict inevitable? Anim Prod Sci 57:201–208
DIRECTIVE 2010/63/EU (2010) Directive on the protection of animals used for scientific purposes. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:02010L0063-20190626
Drinkwater E, Robinson EJ, Hart AG (2019) Keeping invertebrate research ethical in a landscape of shifting public opinion. Methods Ecol Evol 10:1265–1273
Fauvel T, Brischoux F, Briand MJ, Bonnet X (2012) Do researchers impact their study populations? Assessing the effect of field procedures in a long-term population monitoring of sea kraits. Amphib Reptil 33:365–372
Franco N (2013) Animal experiments in biomedical research: a historical perspective. Animals 3:238–273
Fraser D (1999) Animal ethics and animal welfare science: bridging the two cultures. Appl Anim Behav Sci 65:171–189
Goldberg AM (2016) Farm animal welfare and human health. Curr Environ Health Rep 3:313–321
Goldstein DS (2003) Catecholamines and stress. Endocr Regul 37:69–80
Hamelin KM, James MC (2018) Evaluating outcomes of long-term satellite tag attachment on leatherback sea turtles. Anim Biotelem 6:18. https://doi.org/10.1186/s40317-018-0161-3
Isaza R, Andrews GA, Coke RL, Hunter RP (2004) Assessment of multiple cardiocentesis in ball pythons (Python regius). JAALAS 43:35–38
Johnstone CP, Reina RD, Lill A (2012) Interpreting indices of physiological stress in free-living vertebrates. J Comp Physiol B 182:861–879
Knight S, Vrij A, Bard K, Brandon D (2009) Science versus human welfare? Understanding attitudes toward animal use. J Soc Issues 65:463–483
Langkilde T, Shine R (2006) How much stress do researchers inflict on their study animals? A case study using a scincid lizard, Eulamprus heatwolei. J Exp Biol 209:1035–1043
Lee G, Goosens KA (2015) Sampling blood from the lateral tail vein of the rat. JoVE 99:e52766
Lindsjö J, Fahlman Å, Törnqvist E (2016) Animal welfare from mouse to moose -implementing the principles of the 3Rs in wildlife research. J Wildl Dis 52:S65–S77
McCulloch S, Reiss M (2018) A proposal for a UK ethics council for animal policy: the case for putting ethics back into policy making. Animals 8:88
McIntyre T (2015) Animal telemetry: tagging effects. Science 349:596–597
Mitchell L (2011) Moral disengagement and support for nonhuman animal farming. Soc Anim 19:38–58
Minteer BA, Collins JP (2005) Ecological ethics: building a new tool kit for ecologists and biodiversity managers. Conserv Biol 19:1803–1812
Miranda-De La Lama GC, Estévez-Moreno LX, Sepulveda WS, Estrada-Chavero MC, Rayas-Amor AA, Villarroel M, María GA (2017) Mexican consumers' perceptions and attitudes towards farm animal welfare and willingness to pay for welfare friendly meat products. Meat Sci 125:106–113
Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, Manteca X, Manteuffel G, Prunet P, van Reenen CG, Richard S, Veissier I (2007) Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiol Behav 92:317–339
Pandolfi F, Stoddart K, Wainwright N, Kyriazakis I, Edwards SA (2017) The ‘real welfare’ scheme: benchmarking welfare outcomes for commercially farmed pigs. Animal 11:1816–1824
Putman RJ (1995) Ethical considerations and animal welfare in ecological field studies. Biodivers Conserv 4:903–915
Ricceri L, Vitale A (2011) The law through the eye of a needle. EMBO Rep 12:637–640
Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255
Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model - a new model integrating homeostasis, allostasis and stress. Hormon Behav 55:375–389
Russell WMS, Burch RL (1959) The principles of humane experimental technique, vol 238. Methuen, London. https://altweb.jhsph.edu/pubs/books/humane_exp/het-toc#
Saraux C, Le Bohec C, Durant JM, Viblanc VA, Gauthier-Clerc M, Beaune D, Park YH, Yoccoz NG, Stenseth NC, Le Maho Y (2011) Reliability of flipper-banded penguins as indicators of climate change. Nature 469:203–206
Scroggie MP, Clemann N (2009) Handling-related tail loss in an endangered skink: incidence, correlates and a possible solution. J Zool 277:214–220
Sheldon LD, Chin EH, Gill SA, Schmaltz G, Newman AE, Soma KK (2008) Effects of blood collection on wild birds: an update. J Avian Biol 39:369–378
Silva BA, Mattucci C, Krzywkowski P, Murana E, Illarionova A, Grinevich V, Canteras NS, Ragozzino D, Gross CT (2013) Independent hypothalamic circuits for social and predator fear. Nat Neurosci 16:1731–1733
Skoluda N, Strahler J, Schlotz W, Niederberger L, Marques S, Fischer S, Thoma MV, Spoerri C, Ehlert U, Nater UM (2015) Intra-individual psychological and physiological responses to acute laboratory stressors of different intensity. Psychoneuroendocrinology 51:227–236
Smith RJ, Benson TJ, Carey M (2016) Blood sampling does not negatively affect apparent survival, recapture probability, or within-season site fidelity in Field Sparrows (Spizella pusilla). Auk 134:240–246
Sneddon LU, Elwood RW, Adamo SA, Leach MC (2014) Defining and assessing animal pain. Anim Behav 97:201–212
Sneddon LU, Lopez-Luna J, Wolfenden DC, Leach MC, Valentim AM, Steenbergen PJ, Bardine N, Currie AD, Broom DM, Brown C (2018) Fish sentience denial: Muddying the waters. Anim Sentience 3:1
Swierk L, Langkilde T (2018) Does repeated human handling of study animals during the mating season affect their offspring? J Exp Zool A 329:80–86
Tovote P, Esposito MS, Botta P, Chaudun F, Fadok JP, Markovic M, Wolff SBE, Ramakrishnan C, Fenno L, Deisseroth K, Herry C, Arber S, Lüthi A (2016) Midbrain circuits for defensive behaviour. Nature 534:206–2012
Tsiafouli MA, Thébault E, Sgardelis SP et al (2015) Intensive agriculture reduces soil biodiversity across Europe. Glob Change Biol 21:973–985
Voss M, Shutler D, Werner J (2010) A hard look at blood sampling of birds. Auk 127:704–708
Yokoo H, Tanaka M, Yoshida M, Tsuda A, Tanaka T, Mizoguchi K (1990) Direct evidence of conditioned fear-elicited enhancement of noradrenaline release in the rat hypothalamus assessed by intracranial microdialysis. Brain Res 536:305–308
Zemanova MA (2017) More training in animal ethics needed for European biologists. Bioscience 67:301–305
Acknowledgements
S. Mercier improved the English. We thank C. Parenteau and E. Seghrouchni for hormonal assays. We also thank four anonymous reviewers for their constructive comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Heldmaier.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bonnet, X., Billy, G. & Lakušić, M. Puncture versus capture: which stresses animals the most?. J Comp Physiol B 190, 341–347 (2020). https://doi.org/10.1007/s00360-020-01269-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-020-01269-2