Measuring on-farm welfare in rabbits: a review with emphasis on animal-based indicators

Angela Trocino

https://orcid.org/0000-0001-9045-6156

Italy

University of Padua image/svg+xml

Dept. of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE), University of Padova

Clara Tolini

https://orcid.org/0000-0002-4527-0210

Italy

University of Padua image/svg+xml

Dept. of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE), University of Padova

----

Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna “Bruno Ubertini”

 

|

Accepted: 2024-10-18

|

Published: 2024-12-30

DOI: https://doi.org/10.4995/wrs.2024.22647
Funding Data

Downloads

Keywords:

welfare consequences, protocols, indicators, positive welfare, rabbit

Supporting agencies:

This research was not funded

Abstract:

Based on current definitions, animal welfare has to be linked to a life worth living, as perceived by animals, thanks to positive experiences rather than to the mere absence of negative ones. The measure of on-farm welfare of livestock is crucial to improve farming systems, identify critical points and compare different farming systems in view of welfare labelling protocols. To this end, species-specific protocols are necessary, which should use different types of indicators, i.e. resources-based indicators, management-based indicators and, especially, animal-based indicators. These indicators should work under different farming systems and for different animal categories and can be used to assess welfare in the short term or during the productive life of the animal. Last but not least, indicators should be able to measure the affective state of animals in terms of positive emotions. In this scenario, rabbits are quite unique, as little information is available about i) their behavioural needs under farming conditions; ii) the degree of suffering associated with the behavioural restrictions that can occur under farming conditions; iii) the indicators to be used in the very different housing and management conditions in which rabbits can be farmed; and iv) the relationships between emotions and affective states of animals as well as the effect on resiliency of rabbits under different conditions. In this context, the present review is aimed at summarising the state of the art and designing a road map for assessing on-farm rabbit welfare based on the most recent knowledge and approaches with special emphasis on candidate animalbased indicators for measuring both negative and positive affective states of rabbits. The identification of positive welfare indicators is a big challenge, given the biological and behavioural characteristics of rabbits. Accordingly, a comprehensive and robust assessment of rabbit welfare on farms cannot do without structure- and management-based indicators, which should be included in validated and standardised protocols using a multi-indicator approach.

Show more Show less

References:

Birolo M., Trocino A., Zuffellato A., Pirrone F., Bordignon F., Xiccato G. 2022. Use of gnawing hay blocks: effects on productive performance, behavior and reactivity of growing rabbits kept in parks with different sex-group compositions. Animals 12: 1212. https://doi.org/10.3390/ani12091212

Blokhuis H.J., Veissier I., Miele M., Jones B. 2010. The Welfare Quality® project and beyond: safeguarding farm animal wellbeing. Acta Agriculturae Scandinavica, Section A – Anim. Sci., 60: 129-140. https://doi.org/10.1080/09064702.2010.523480

Botelho N., Vieira-Pinto M., Batchelli P., Pallisera J., Dalmau A. 2020. Testing an animal welfare assessment protocol for growing-rabbits reared for meat production based on the Welfare Quality Approach. Animals, 10: 1415. https://doi.org/10.3390/ani10081415

Buijs S., Tuyttens F.A.M. 2015. Evaluating the effect of semi-group housing of rabbit does on their offspring’s fearfulness: can we use the open-field test? Applied Animal Behav. Sci., 162: 58-66. https://doi.org/10.1016/j.applanim.2014.11.008

Cohen S., Ho C. 2023. Review of rat (Rattus norvegicus), mouse (Mus musculus), guinea pig (Cavia porcellus), and rabbit (Oryctolagus cuniculus) indicators for welfare assessment. Animals, 13: 2167. https://doi.org/10.3390/ani13132167

Dal Bosco A., Castellini C., Mugnai C., 2002. Rearing rabbits on a wire net floor or straw litter: behaviour, growth and meat qualitative traits. Livest. Prod. Sci., 75: 149-156. https://doi.org/10.1016/S0301-6226(01)00307-4

Dal Bosco A., Cartoni Mancinelli A., Hoy S., Martino M., Mattioli S., Cotozzolo E., Castellini C., 2020. Assessing the preference of rabbit does to social contact or seclusion: results of different investigations. Animals, 10: 286. https://doi.org/10.3390/ani10020286

Dalle Zotte A., Princz Z., Matics Zs., Gerencsér Zs., Metzger S., Szendrő Zs. 2009. Rabbit preference for cages and pens with or without mirrors. Appl. Anim. Behav. Sci., 116: 273-278. https://doi.org/10.1016/j.applanim.2008.08.011

Dalmau A., Moles X., Pallisera J. 2020. Animal welfare assessment protocol for does, bucks, and kit rabbits reared for production. Front. Vet. Sci., 7: 445. https://doi.org/10.3389/fvets.2020.00445

de Jong I.C., Reuvekamp B.F., Rommers J.M. 2011. A welfare assessment protocol for commercially housed rabbits. Report 532. Wageningen UR Livestock Research. Lelystad, The Netherlands.

Delibes-Mateos M., Rödel H.G., Rouco C., Alves P.C., Carneiro M., Villafuerte R. 2021. European Rabbit Oryctolagus cuniculus (Linnaeus, 1758), in: Handbook of the Mammals of Europe. Springer, Cham., 1-39. https://doi.org/10.1007/978-3-319-65038-8_13-1

EFSA. 2005. Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a request from the Commission related to “The Impact of the current housing and husbandry systems on the health and welfare of farmed domestic rabbits.” EFSA Journal, 3: 267. https://doi.org/10.2903/j.efsa.2005.267

EFSA Panel on Animal Health and Welfare (AHAW) 2012. Statement on the use of animal-based measures to assess the welfare of animals. EFSA Journal, 10: 2767. https://doi.org/10.2903/j.efsa.2012.2767

EFSA Panel on Animal Health and Welfare (AHAW), Saxmose Nielsen S., Alvarez J., Bicout D.J., Calistri P., Depner K., Drewe J.A., Garin-Bastuji B., Gonzales Rojas J.L., Gortázar Schmidt C., Michel V., Miranda Chueca M.Á., Roberts H.C., Sihvonen L.H., Spoolder H., Stahl K., Velarde Calvo A., Viltrop A., Buijs S., Edwards S., Candiani D., Mosbach-Schulz O., Van der Stede Y., Winckler C. 2020. Health and welfare of rabbits farmed in different production systems. EFSA Journal, 18: e05944. https://doi.org/10.2903/j.efsa.2020.5944

EFSA Panel on Animal Health and Welfare (AHAW), Nielsen S.S., Alvarez J., Bicout D.J., Calistri P., Canali E., Drewe J.A., Garin-Bastuji B., Gonzales Rojas J.L., Gortázar Schmidt C., Herskin M., Miranda Chueca M.Á., Michel V., Padalino B., Pasquali P., Roberts H.C., Spoolder H., Stahl K., Velarde A., Viltrop A., Edwards S., Ashe S., Candiani D., Fabris C., Lima E., Mosbach-Schulz O., Gimeno C.R., Van der Stede Y., Vitali M., Winckler C. 2022. Methodological guidance for the development of animal welfare mandates in the context of the Farm to Fork Strategy. EFSA Journal, 20: e07403. https://doi.org/10.2903/j.efsa.2022.7403

EURCAW-Poultry-SFA. 2023. List of welfare indicators and methods of assessment for rabbits on farm. DL. 2.1.5 Available at: https://zenodo.org/records/7930482. Accessed June 2024.

Farkas T.P., Szendrő Zs., Matics Zs., Radnai I., Nagy I., Gerencsér Zs. 2018. Preference of rabbit does among different nest materials. World Rabbit Sci., 26: 81-90. https://doi.org/10.4995/wrs.2018.7373

González-Mariscal G., Hoy S., Hoffman K.L. 2022. Rabbit maternal behavior: A perspective from behavioral neuroendocrinology, animal production, and psychobiology, in: González-Mariscal G. (Ed.), Patterns of parental behavior: from animal science to comparative ethology and neuroscience, Advances in Neurobiology. Springer International Publishing, Cham., 131-176. https://doi.org/10.1007/978-3-030-97762-7_5

Gümüş H.G., Agyemang A.A., Romantsik O., Sandgren R., Karlsson H., Gram M., Vallius S., Ley D., van den Hove D.L.A., Bruschettini M. 2018. Behavioral testing and litter effects in the rabbit. Behav. Brain Res., 353: 236-241. https://doi.org/10.1016/j.bbr.2018.02.032

ITAVI. 2018. Evaluer le bien-être des lapins en maternité et en croissance. Protocole EBENE. Available at: https://www.itavi.asso.fr/publications/protocole-ebene-guide-pour-lesutilisateurs/download/627bbc3fcf0cd_EBENE_Protocole_Lapin.pdf. Accessed June 2024.

Jirkof P., Rudeck J., Lewejohann L. 2019. Assessing affective state in laboratory rodents to promote animal welfare—what is the progress in applied refinement research? Animals 9: 1026. https://doi.org/10.3390/ani9121026

LIFT, 2024. Positive Animal Welfare - LIFT - Cost Action CA21124. Available at: https://liftanimalwelfare.eu/about/positiveanimal-welfare/. Accessed June 2024.

Littlewood K.E., Heslop M.V., Cobb M.L. 2023. The agency domain and behavioral interactions: assessing positive animal welfare using the Five Domains Model. Front. Vet. Sci., 10: 1284869. https://doi.org/10.3389/fvets.2023.1284869

Lockley R.M. 1961. Social structure and stress in the rabbit warren. J. Anim. Ecol., 30: 385-423. https://doi.org/10.2307/2305

Mellor D.J. 2016. Updating animal welfare thinking: Moving beyond the “Five Freedoms” towards “a Life Worth Living”. Animals, 6: 21. https://doi.org/10.3390/ani6030021

Mellor D.J., Reid C.S.W., 1994. Concepts of animal well-being and predicting the impact of procedures on experimental animals. In: Improving the Well-being of Animals in the Research Environment; Baker, R.M., Jenkin, G., Mellor, D.J., Eds.; Australian and New Zealand Council for the Care of Animals in Research and Teaching: Glen Osmond, Australia, 1994; pp. 3–18. Available online: Concepts of animal well-being and predicting the impact of procedures on experimental animals . Accessed December 2024.

Mellor D.J., Beausoleil N.J. 2015. Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Anim. Welfare 24: 241-253. https://doi.org/10.7120/09627286.24.3.241

Mellor D.J., Beausoleil N.J., Littlewood K.E., McLean A.N., McGreevy P.D., Jones B., Wilkins C. 2020. The 2020 Five Domains model: including human-animal interactions in assessments of animal welfare. Animals, 10: 1870. https://doi.org/10.3390/ani10101870

Mikó A., Szendrő Zs., Matics Zs., Radnai I., Odermatt M., Nagy I., Gerencsér Zs. 2012. Free choice of rabbit does between cages with different sizes. In Proc.: 10th World Rabbit Congress. 3-6 September 2012, Sharm El-Sheikh, Egypt. 1069-1073. Available at: http://world-rabbit-science.com/WRSA-Proceedings/Congress-2012-Egypt/Egypt-2012-a.htm#welfare. Accessed on June 2024.

Ministero della Salute, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna 2023. Valutazione del benessere animale nell’allevamento del coniglio: Manuale esplicativo controllo ufficiale Classyfarm. Available at: https://www.classyfarm.it/images/documents/VET-UFFICIALE_AGGIORNATO_06-23/Manuale_controllo_ufficiale_coniglio_def_rev.pdf. Accessed June 2024.

Morisse J.P., Boilletot E., Martrenchar A. 1999. Preference testing in intensively kept meat production rabbits for straw on wire grid floor. Applied Anim. Behav. Sci., 64: 71-80. https://doi.org/10.1016/S0168-1591(99)00023-4

Paulović T., de Jong I., Ouweltjes W., Martin Valls G.E., Llonch Obiols P., Ko H.L., Kieffer V., Lapeyre C., Campana C., Wille H., Jasinska A., Spoolder H. 2024. Development of a roadmap for action for the project More Welfare: towards new risk assessment methodologies and harmonised animal welfare data in the EU. EFSA Supporting Publications 21: 8566E. https://doi.org/10.2903/sp.efsa.2024.EN-8566

Princz Zs., Dalle Zotte A., Radnai I., Bíró-Németh E., Matics Zs., Gerencsér Zs., Nagy I., Szendrő Zs., 2008. Behaviour of growing rabbits under various housing conditions. Applied Animal Behaviour Science 11: 342-356 https://doi.org/10.1016/j.applanim.2007.06.013

Rault J.L., Newberry R.C., Semrov M.Z. 2023. Editorial: Positive welfare: from concept to implementation. Front. Anim. Sci., 4: 1289659. https://doi.org/10.3389/fanim.2023.1289659

Rödel H.G. 2022. Aspects of social behaviour and reproduction in the wild rabbit - Implications for rabbit breeding? World Rabbit Sci., 30: 47-59. https://doi.org/10.4995/wrs.2022.15954

Rödel H.G., Monclús R., von Holst D. 2006. Behavioral styles in European rabbits: social interactions and responses to experimental stressors. Physiol. Behav., 89: 180-188. https://doi.org/10.1016/j.physbeh.2006.05.042

Szendrő Zs., McNitt J.I. 2012. Housing of rabbit does: Group and individual systems: A review. Livest. Sci., 150: 1-10. https://doi.org/10.1016/j.livsci.2012.09.017

Szendrő Zs., Trocino A., Hoy S., Xiccato G., Villagrá A., Maertens L., 2019. A review of recent research outcomes on the housing of farmed domestic rabbits: reproducing does. World Rabbit Sci., 27: 1-14. https://doi.org/10.4995/wrs.2019.10599

Trocino A., Xiccato G. 2006. Animal welfare in reared rabbits: a review with emphasis on housing systems. World Rabbit Sci., 14: 77-93. https://doi.org/10.4995/wrs.2006.553

Trocino A., Xiccato G. 2024. Alojamiento de conejos sin jaulas: luces y sombras. In Proc.. 48 Symposium de Cunicultura ASESCU, 23-24/04/2024, Córdoba, Spain.

Trocino A., Majolini D., Tazzoli M., Filiou E., Xiccato G., 2013. Housing of growing rabbits in individual, bicellular and collective cages: fear level and behavioural patterns. Animal, 7: 633-639. https://doi.org/10.1017/S1751731112002029

Trocino A., Filiou E., Tazzoli M., Bertotto D., Negrato E., Xiccato G. 2014. Behaviour and welfare of growing rabbits housed in cages and pens. Livest. Sci., 167: 305-314. https://doi.org/10.1016/j.livsci.2014.05.035

Trocino A., Filiou E., Zomeño C., Birolo M., Bertotto D., Xiccato G., 2018. Behaviour and reactivity of female and male rabbits housed in collective pens: effects of floor type and stocking density at different ages. World Rabbit Sci., 26: 135-147. https://doi.org/10.4995/wrs.2018.7747

Trocino A., Zomeño C., Filiou E., Birolo M., White P., Xiccato G. 2019. The use of environmental enrichments affects performance and behavior of growing rabbits housed in collective pens. Animals, 9: 537. https://doi.org/10.3390/ani9080537

Turner P.V. 2019. Moving beyond the absence of pain and distress: focusing on positive animal welfare. ILAR J., 60: 366-372. https://doi.org/10.1093/ilar/ilaa017

Verga M., Luzi F., Carenzi C. 2007. Effects of husbandry and management systems on physiology and behaviour of farmed and laboratory rabbits. Hormones and Behavior, Reproductive Behavior in Farm and Laboratory Animals, 52: 122-129. https://doi.org/10.1016/j.yhbeh.2007.03.024

Verga M., Luzi F., Petracci M., Cavani C. 2009. Welfare aspects in rabbit rearing and transport. It. J. Anim. Sci., 8: 191-204. https://doi.org/10.4081/ijas.2009.s1.191

Villafuerte R., Moreno S. 1997. Predation risk, cover type, and group size in European rabbits in Doñana (SW Spain). Acta Theriologica, 42: 225-230. https://doi.org/10.4098/AT.arch.97-23

von Holst D., Hutzelmeyer H., Kaetzke P., Khaschei M., Schönheiter R. 1999. Social Rank, Stress, Fitness, and Life Expectancy in Wild Rabbits. Naturwissenschaften, 86: 388-393. https://doi.org/10.1007/s001140050638

von Holst D., Hutzelmeyer H., Kaetzke P., Khaschei M., Rödel H.G., Schrutka H. 2002. Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behavior. Ecol. Sociobiol., 51: 245-254. https://doi.org/10.1007/s00265-001-0427-1

Warin L., Mika A., Souchet C., Bouvarel I. 2021. Feasibility and repeatability of the EBENE® Welfare Assessment measures for rabbits. In Proc.: 12th World Rabbit Congress, 3-5 November 2021, Nantes, France, Communication E-17. Available at: http://world-rabbit-science.com/WRSAProceedings/Congress-2021-Nantes/Nantes-2021-01.htm#etho. Accessed June 2024.

Show more Show less