Skip to main content

Puncture versus capture: which stresses animals the most?

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

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

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Bonnet X, Fizesan A, Michel CL (2013) Shelter availability, stress level and digestive performance in the aspic viper. J Exp Biol 216:815–822

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Brown MB, Brown CR (2009) Blood sampling reduces annual survival in cliff swallows (Petrochelidon pyrrhonota). Auk 126:853–861

    Google Scholar 

  • Burghardt GM (2009) Ethics and animal consciousness: How rubber the ethical ruler? J Soc Issues 65:499–521

    Google Scholar 

  • Carsten J (2011) Substance and relationality: blood in contexts. Annu Rev Anthropol 40:19–35

    Google Scholar 

  • Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Costantini D, Møller AP (2013) A meta-analysis of the effects of geolocator application on birds. Curr Zool 59:697–706

    Google Scholar 

  • Dawkins MS (2017) Animal welfare and efficient farming: is conflict inevitable? Anim Prod Sci 57:201–208

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Franco N (2013) Animal experiments in biomedical research: a historical perspective. Animals 3:238–273

    PubMed  Google Scholar 

  • Fraser D (1999) Animal ethics and animal welfare science: bridging the two cultures. Appl Anim Behav Sci 65:171–189

    Google Scholar 

  • Goldberg AM (2016) Farm animal welfare and human health. Curr Environ Health Rep 3:313–321

    PubMed  Google Scholar 

  • Goldstein DS (2003) Catecholamines and stress. Endocr Regul 37:69–80

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Isaza R, Andrews GA, Coke RL, Hunter RP (2004) Assessment of multiple cardiocentesis in ball pythons (Python regius). JAALAS 43:35–38

    CAS  Google Scholar 

  • Johnstone CP, Reina RD, Lill A (2012) Interpreting indices of physiological stress in free-living vertebrates. J Comp Physiol B 182:861–879

    PubMed  Google Scholar 

  • Knight S, Vrij A, Bard K, Brandon D (2009) Science versus human welfare? Understanding attitudes toward animal use. J Soc Issues 65:463–483

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Lee G, Goosens KA (2015) Sampling blood from the lateral tail vein of the rat. JoVE 99:e52766

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • McIntyre T (2015) Animal telemetry: tagging effects. Science 349:596–597

    CAS  PubMed  Google Scholar 

  • Mitchell L (2011) Moral disengagement and support for nonhuman animal farming. Soc Anim 19:38–58

    Google Scholar 

  • Minteer BA, Collins JP (2005) Ecological ethics: building a new tool kit for ecologists and biodiversity managers. Conserv Biol 19:1803–1812

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Putman RJ (1995) Ethical considerations and animal welfare in ecological field studies. Biodivers Conserv 4:903–915

    Google Scholar 

  • Ricceri L, Vitale A (2011) The law through the eye of a needle. EMBO Rep 12:637–640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    PubMed  Google Scholar 

  • Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model - a new model integrating homeostasis, allostasis and stress. Hormon Behav 55:375–389

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Scroggie MP, Clemann N (2009) Handling-related tail loss in an endangered skink: incidence, correlates and a possible solution. J Zool 277:214–220

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Sneddon LU, Elwood RW, Adamo SA, Leach MC (2014) Defining and assessing animal pain. Anim Behav 97:201–212

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tsiafouli MA, Thébault E, Sgardelis SP et al (2015) Intensive agriculture reduces soil biodiversity across Europe. Glob Change Biol 21:973–985

    Google Scholar 

  • Voss M, Shutler D, Werner J (2010) A hard look at blood sampling of birds. Auk 127:704–708

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zemanova MA (2017) More training in animal ethics needed for European biologists. Bioscience 67:301–305

    Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Xavier Bonnet.

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.

Supplementary file1 (XLSX 17 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-020-01269-2

Keywords

  • Animal welfare
  • Blood sampling
  • Corticosterone
  • Glucose
  • Reptile
  • Stress markers