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Research on animals is one of the most controversial ethical issues in our society. It is imperative that animal welfare is being considered and the harm and distress to animals used in research is minimized. This could be achieved through implementation of the so-called 3Rs principles for animal research, which are now implemented in many legislations worldwide. These principles serve as a basis for research without the use of animals (Replacement), with as few animals as possible (Reduction), and in which the animal’s welfare is as good as possible (Refinement). While there has been a lot of focus on implementation of these principles, only a few studies have documented the knowledge and adoption of the 3Rs among researchers. One field that has been particularly neglected is ecological research, which can involve many practices that affect animal welfare. Moreover, the knowledge, experience, and attitudes about animal use in ecological research and education has never been examined before. In order to close this gap, I conducted a survey among European ecologists. Responses from 107 respondents from 23 countries revealed that lethal and invasive research methods are prevalent, and that more than half of the respondents have never heard of the 3Rs principles for animal research. Major concerns are also the lack of calculation of the minimum sample size and widespread of dissection classes as part of education. Additionally, most respondents experienced ethical doubts about their research, and did not receive any training in animal welfare or ethics. These findings revealed that it is necessary to implement rigorous standards for ecological research and enforce the implementation of the 3Rs principles. Furthermore, the evaluation of current educational practices in ecology is urgently needed.
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Adamo, S.A. (2016) Do insects feel pain? A question at the intersection of animal behaviour, philosophy and robotics. Anim Behav, 118, 75-79. doi: 10.1016/j.anbehav.2016.05.005.
Avey, M.T., Fenwick, N. & Griffin, G. (2015) The use of systematic reviews and reporting guidelines to advance the implementation of the 3Rs. Journal of the American Association for Laboratory Animal Science, 54, 153-162. doi:
Bateson, M., Desire, S., Gartside, S.E. & Wright, G.A. (2011) Agitated honeybees exhibit pessimistic cognitive biases. Curr Biol, 21, 1070-1073. doi: 10.1016/j.cub.2011.05.017.
Bayvel, A.D. & Cross, N. (2010) Animal welfare: a complex domestic and international public-policy issue - who are the key players? Journal of Veterinary Medical Education, 37, 3-12. doi: 10.3138/jvme.37.1.3.
Beausoleil, N.J. (2014) Balancing the need for conservation and the welfare of individual animals. Dilemmas in Animal Welfare (ed. by M.C. Appleby, D.M. Weary and P. Sandoe), pp. 124-147. C.A.B. International, Wallingford, UK.
Blattner, C. (2014) 3R for farmed animals: a legal argument for consistency. Global Journal of Animal Law, 1, 1-26. doi:
Boynton, P.M. & Greenhalgh, T. (2004) Hands-on guide to questionnaire research: selecting, designing, and developing your questionnaire. Br Med J, 328, 1312-1315. doi: 10.1136/bmj.328.7451.1312.
Cooke, S.J., Birnie-Gauvin, K., Lennox, R.J., Taylor, J.J., Rytwinski, T., Rummer, J.L., Franklin, C.E., Bennett, J.R. & Haddaway, N.R. (2017) How experimental biology and ecology can support evidence-based decision-making in conservation: avoiding pitfalls and enabling application. Conservation Physiology, 5, cox043. doi: 10.1093/conphys/cox043.
Costello, M.J., Beard, K.H., Corlett, R.T., Cumming, G.S., Devictor, V., Loyola, R., Maas, B., Miller-Rushing, A.J., Pakeman, R. & Primack, R.B. (2016) Field work ethics in biological research. Biol Conserv, 203, 268-271. doi: 10.1016/j.biocon.2016.10.008.
Cox, L. & Montrose, T. (2016) How do human-animal emotional relationships influence public perceptions of animal use? The Journal of Animal Ethics, 6, 44-53. doi: 10.5406/janimalethics.6.1.0044.
Crook, R.J. & Walters, E.T. (2011) Nociceptive behavior and physiology of molluscs: animal welfare implications. ILAR J, 52, 185-195. doi: 10.1093/ilar.52.2.185.
Dignon, A. (2016) ‘I think it will eventually be done away with’: attitudes among healthcare professionals towards the current system of animal experimentation. Journal of Health Psychology, 21, 1630-1643. doi: 10.1177/1359105314559862.
Dillman, D.A., Smyth, J.D. & Christian, L.M. (2014) Internet, Phone, Mail, and Mixed-Mode Surveys: The Tailored Design Method, 4th edn. John Wiley & Sons Inc., Hoboken, NJ.
Drinkwater, E., Robinson, E.J. & Hart, A.G. (2019) Keeping invertebrate research ethical in a landscape of shifting public opinion. Methods in Ecology and Evolution, 10, 1265-1273. doi: 10.1111/2041-210X.13208.
Elwood, R.W. (2011) Pain and suffering in invertebrates? ILAR J, 52, 175-184. doi: 10.1093/ilar.52.2.175.
European Commission (2016) Special Eurobarometer 442: Attitudes of Europeans Towards Animal Welfare. http://data.europa.eu/euodp/en/data/dataset/S2096_84_4_442_ENG. doi: 10.2875/884639.
Field, K.A., Paquet, P.C., Artelle, K., Proulx, G., Brook, R.K. & Darimont, C.T. (2019) Publication reform to safeguard wildlife from researcher harm. PLoS Biol, 17, e3000193. doi: 10.1371/journal.pbio.3000193.
Franco, N.H. & Olsson, I.A.S. (2014) Scientists and the 3Rs: attitudes to animal use in biomedical research and the effect of mandatory training in laboratory animal science. Laboratory Animals, 48, 50-60. doi: 10.1177/0023677213498717.
Franco, N.H., Sandoe, P. & Olsson, I.A.S. (2018) Researchers' attitudes to the 3Rs - an upturned hierarchy? PLoS ONE, 13, e0200895. doi: 10.1371/journal.pone.0200895.
Fraser, D. & MacRae, A.M. (2011) Four types of activities that affect animals: implications for animal welfare science and animal ethics philosophy. Anim Welf, 20, 581-590. doi:
Gala, S.G. & Crandall, M.L. (2019) Global collaboration to modernize advanced trauma life support training. Journal of Surgical Education, 76, 487-496. doi: 10.1016/j.jsurg.2018.08.011.
Girard, I., Ouellet, J.P., Courtois, R., Dussault, C. & Breton, L. (2002) Effects of sampling effort based on GPS telemetry on home-range size estimations. J Wildl Manage, 66, 1290-1300. doi: 10.2307/3802962.
Grevemeyer, B. & Knight, A. (2018) The development of a clinical skills laboratory at Ross University School of Veterinary Medicine. ATLA, 46, 177-183. doi: 10.1177/026119291804600305.
Hagelin, J., Carlsson, H.E. & Hau, J. (2003) An overview of surveys on how people view animal experimentation: some factors that may influence the outcome. Public Understanding of Science, 12, 67-81. doi: 10.1177/0963662503012001247.
Harcourt, R.G., Turner, E., Hall, A., Waas, J.R. & Hindell, M. (2010) Effects of capture stress on free-ranging, reproductively active male Weddell seals. Journal of Comparative Physiology, 196, 147-154. doi: 10.1007/s00359-009-0501-0.
Hazel, S.J., Signal, T.D. & Taylor, N. (2011) Can teaching veterinary and animal-science students about animal welfare affect their attitude toward animals and human-related empathy? Journal of Veterinary Medical Education, 38, 74-83. doi: 10.3138/jvme.38.1.74.
Herzog, H.A. (2007) Gender differences in human-animal interactions: a review. Anthrozoos, 20, 7-21. doi: 10.2752/089279307780216687.
Hone, J., Drake, V.A. & Krebs, C.J. (2018) Evaluating wildlife management by using principles of applied ecology: case studies and implications. Wildl Res, 45, 436-445. doi: 10.1071/wr18006.
Hug, B. (2008) Re-examining the practice of dissection: what does it teach? Journal of Curriculum Studies, 40, 91-105. doi: 10.1080/00220270701484746.
Hurst, J.L. & West, R.S. (2010) Taming anxiety in laboratory mice. Nat. Methods, 7, 825-826. doi: 10.1038/nmeth.1500.
Johnstone, E.C., Frye, M.A., Lord, L.K., Baysinger, A.K. & Edwards-Callaway, L.N. (2019) Knowledge and opinions of third year veterinary students relevant to animal welfare before and after implementation of a core welfare course. Front Vet Sci, 6, 103. doi: 10.3389/fvets.2019.00103.
Keller, M. (2017) Feeding live invertebrate prey in zoos and aquaria: are there welfare concerns? Zoo Biol, 36, 316-322. doi: 10.1002/zoo.21378.
Kellert, S.R. & Berry, J.K. (1987) Attitudes, knowledge, and behaviors toward wildlife as affected by gender. Wildl Soc Bull, 15, 363-371. doi:
Lalley, J.P., Piotrowski, P.S., Battaglia, B., Brophy, K. & Chugh, K. (2010) A comparison of V-Frog to physical frog dissection. International Journal of Environmental and Science Education, 5, 189-200. doi:
Leenaars, M., Savenije, B., Nagtegaal, A., van der Vaart, L. & Ritskes-Hoitinga, M. (2009) Assessing the search for and implementation of the Three Rs: a survey among scientists. ATLA, 37, 297-303. doi: 10.1177/026119290903700312.
Lefort, M.-C., Cruickshank, R.H., Descovich, K., Adams, N.J., Barun, A., Emami-Khoyi, A., Ridden, J., Smith, V.R., Sprague, R., Waterhouse, B.R. & Boyer, S. (2019) Blood, sweat and tears: a review of non-invasive DNA sampling. bioRxiv, Retrieved from http://biorxiv.org/content/early/2019/07/02/385120.abstractdoi:
Lombardi, S.A., Hicks, R.E., Thompson, K.V. & Marbach-Ad, G. (2014) Are all hands-on activities equally effective? Effect of using plastic models, organ dissections, and virtual dissections on student learning and perceptions. Advances in Physiology Education, 38, 80-86. doi: 10.1152/advan.00154.2012.
Lund, T.B., Lassen, J. & Sandoe, P. (2012) Public attitude formation regarding animal research. Anthrozoos, 25, 475-490. doi: 10.2752/175303712x13479798785896.
Lund, T.B., Morkbak, M.R., Lassen, J. & Sandoe, P. (2014) Painful dilemmas: a study of the way the public's assessment of animal research balances costs to animals against human benefits. Public Understanding of Science, 23, 428-444. doi: 10.1177/0963662512451402.
MacRae, A.M., Makowska, I.J. & Fraser, D. (2018) Initial evaluation of facial expressions and behaviours of harbour seal pups (Phoca vitulina) in response to tagging and microchipping. Appl Anim Behav Sci, 205, 167-174. doi: 10.1016/j.applanim.2018.05.001.
Magnani, D., Ferri, N., Dalmau, A. & Messori, S. (2017) Knowledge and opinions of veterinary students in Italy toward animal welfare science and law. Vet Rec, 180, 225-233. doi: 10.1136/vr.103938.
McMahon, C.R., Bradshaw, C.J.A. & Hays, G.C. (2007) Applying the heat to research techniques for species conservation. Conserv Biol, 21, 271-273. doi: 10.1111/j.1523-1739.2006.00566.x.
Molina, S., Fuller, A.K., Morin, D.J. & Royle, J.A. (2017) Use of spatial capture–recapture to estimate density of Andean bears in northern Ecuador. Ursus, 28, 117-126. doi: 10.2192/URSU-D-16-00030.1.
Moro, C., Štromberga, Z., Raikos, A. & Stirling, A. (2017) The effectiveness of virtual and augmented reality in health sciences and medical anatomy. Anatomical Sciences Education, 10, 549-559. doi: 10.1002/ase.1696.
Oakley, J. (2013) "I didn't feel right about animal dissection". Dissection objectors share their science class experiences. Soc Anim, 21, 360-378. doi: 10.1163/15685306-12341267.
Ostovic, M., Mikus, T., Pavicic, Z., Matkovic, K. & Mesic, Z. (2017) Influence of socio-demographic and experiential factors on the attitudes of Croatian veterinary students towards farm animal welfare. Vet Med, 62, 417-428. doi: 10.17221/172/2016-vetmed.
Pawlowski, J.B., Feinstein, D.M. & Gala, S.G. (2018) Developments in the transition from animal use to simulation-based biomedical education. Simulation in Healthcare-Journal of the Society for Simulation in Healthcare, 13, 420-426. doi: 10.1097/sih.0000000000000310.
Pereira, G.D., Dieguez, J., Demirbas, Y.S. & Menache, A. (2017) Alternatives to animal use in veterinary education: a growing debate. Ank Univ Vet Fak Derg, 64, 235-239. doi: 10.1501/Vetfak_0000002804.
Phillips, C., Izmirli, S., Aldavood, J., Alonso, M., Choe, B., Hanlon, A., Handziska, A., Illmann, G., Keeling, L., Kennedy, M., Lee, G., Lund, V., Mejdell, C., Pelagic, V. & Rehn, T. (2011) An international comparison of female and male students’ attitudes to the use of animals. Animals, 1, 7-26. doi: 10.3390/ani1010007.
Plowright, C.M.S. (2017) Bumblebees at work in an emotion-like state. Learn Behav, 45, 207-208. doi: 10.3758/s13420-017-0265-2.
Pollo, S., Vitale, A., Gayle, V. & Zucco, F. (2004) The '3Rs' model and the concept of alternatives in animal research: a questionnaire survey. Lab Animal, 33, 47-53. doi: 10.1038/laban0704-47.
Poole, T. (1997) Happy animals make good science. Laboratory Animals, 31, 116-124. doi: 10.1258/002367797780600198.
Powell, R.A. & Proulx, G. (2003) Trapping and marking terrestrial mammals for research: integrating ethics, performance criteria, techniques, and common sense. ILAR J, 44, 259-276. doi: 10.1093/ilar.44.4.259.
Prescott, M.J. & Lidster, K. (2017) Improving quality of science through better animal welfare: the NC3Rs strategy. Lab Animal, 46, 152. doi: 10.1038/laban.1217.
R Core Team (2017) R: a language and environment for statistical computing. http://www.R-project.org. doi:
Rollin, B. (1989) The Unheeded Cry: Animal Consciousness, Animal Pain and Science. Iowa State University Press, Iowa.
Russell, W.M.S. & Burch, R.L. (1959) The Principles of Humane Experimental Technique. Methuen, London.
Russo, D., Ancillotto, L., Hughes, A.C., Galimberti, A. & Mori, E. (2017) Collection of voucher specimens for bat research: conservation, ethical implications, reduction, and alternatives. Mammal Rev, 47, 237-246. doi: 10.1111/mam.12095.
Smith, E.S.J. & Lewin, G.R. (2009) Nociceptors: a phylogenetic view. Journal of Comparative Physiology A, 195, 1089-1106. doi: 10.1007/s00359-009-0482-z.
Sneddon, L.U. (2018) Comparative physiology of nociception and pain. Physiology, 33, 63-73. doi: 10.1152/physiol.00022.2017.
Sneddon, L.U., Elwood, R.W., Adamo, S.A. & Leach, M.C. (2014) Defining and assessing animal pain. Anim Behav, 97, 201-212. doi: 10.1016/j.anbehav.2014.09.007.
Thaxter, C.B., Clark, N.A., Ross-Smith, V.H., Conway, G.J., Bouten, W. & Burton, N.H.K. (2017) Sample size required to characterize area use of tracked seabirds. J Wildl Manage, 81, 1098-1109. doi: 10.1002/jwmg.21283.
Törnqvist, E., Annas, A., Granath, B., Jalkesten, E., Cotgreave, I. & Öberg, M. (2014) Strategic focus on 3R principles reveals major reductions in the use of animals in pharmaceutical toxicity testing. PLoS ONE, 9, e101638. doi: 10.1371/journal.pone.0101638.
van Luijk, J., Cuijpers, Y., van der Vaart, L., Leenaars, M. & Ritskes-Hoitinga, M. (2011) Assessing the search for information on Three Rs methods, and their subsequent implementation: a national survey among scientists in the Netherlands. ATLA, 39, 429-447. doi: 10.1177/026119291103900505.
van Luijk, J., Cuijpers, Y., van der Vaart, L., de Roo, T.C., Leenaars, M. & Ritskes-Hoitinga, M. (2013) Assessing the application of the 3Rs: a survey among animal welfare officers in the Netherlands. Laboratory Animals, 47, 210-219. doi: 10.1177/0023677213483724.
Waugh, C.A. & Monamy, V. (2016) Opposing lethal wildlife research when nonlethal methods exist: scientific whaling as a case study. Journal of Fish and Wildlife Management, 7, 231-236. doi: 10.3996/072015-jfwm-061.
Wurbel, H. (2017) More than 3Rs: the importance of scientific validity for harm-benefit analysis of animal research. Lab Animal, 46, 164-166. doi: 10.1038/laban.1220.
Zemanova, M.A. (2017) More training in animal ethics needed for European biologists. Bioscience, 67, 301-305. doi: 10.1093/biosci/biw177.
Zemanova, M.A. (2019) Poor implementation of non-invasive sampling in wildlife genetics studies. Rethinking Ecology, 4, 119-132. doi: 10.3897/rethinkingecology.4.32751.
Zemanova, M.A. (2020) Towards more compassionate wildlife research through the 3Rs principles: moving from invasive to non-invasive methods. Wildl Biol, 2020, wlb.00623. doi: 10.2981/wlb.00607.
Zemanova, M.A., Knop, E. & Heckel, G. (2017a) Introgressive replacement of natives by invading Arion pest slugs. Scientific Reports, 7, 14908. doi: 10.1038/s41598-017-14619-y.
Zemanova, M.A., Perotto-Baldivieso, H.L., Dickins, E.L., Gill, A.B., Leonard, J.P. & Wester, D.B. (2017b) Impact of deforestation on habitat connectivity thresholds for large carnivores in tropical forests. Ecological Processes, 6, 21. doi: 10.1186/s13717-017-0089-1.