On your terms or mine: pigs' response to imposed gentle tactile contact vs. free form interaction with a familiar human.
Agency
Expectancy violation
Human–animal interactions
Human–animal relationship
Naturalistic interactions
Positive animal welfare
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 Oct 2024
24 Oct 2024
Historique:
received:
13
06
2024
accepted:
14
10
2024
medline:
25
10
2024
pubmed:
25
10
2024
entrez:
25
10
2024
Statut:
epublish
Résumé
Positive human-animal interactions (HAIs) can be intrinsically rewarding and facilitate positive human-animal relationships. However, HAI paradigms vary across studies, and the influence of different interaction paradigms on the animal's response has been overlooked. We compared the behavioural responses of pigs (n = 28) individually tested with two types of gentle tactile interactions with a familiar human: 'free form (FF)' where the pig could voluntarily approach and interact as they normally would, and 'imposed contact (IC)' where the human imposed tactile contact on the pig according to a standardised protocol. Pigs did not differ in their level of engagement with the human between the two types of interactions. However, they differed in their behaviour as they explored the pen more during the FF test, while they emitted more low-pitched vocalisations (grunts) during the IC test. These differences can likely be imputed to the IC test differing to the pigs' habituation to human contact, which could have evoked greater attention to the human or triggered frustration due to violation of expectation. These findings highlight the influence of the predictability of the interaction or level of agency provided to the animal in HAI tests and relation to their previous experience of interacting.
Identifiants
pubmed: 39448780
doi: 10.1038/s41598-024-76451-5
pii: 10.1038/s41598-024-76451-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
25249Subventions
Organisme : Austrian Science Fund
ID : P 33669-B
Informations de copyright
© 2024. The Author(s).
Références
Waiblinger, S. et al. Assessing the human–animal relationship in farmed species: A critical review. Appl. Anim. Behav. Sci. 101, 185–242. https://doi.org/10.1016/j.applanim.2006.02.001 (2006).
doi: 10.1016/j.applanim.2006.02.001
Hemsworth, P. H. & Coleman, G. J. Human–animal interactions and animal productivity and welfare. in Human-Livestock Interactions: The Stockperson and the Productivity and Welfare of Intensively Farmed Animals 47–83. (2011).
Mellor, D. J. et al. The 2020 five domains model: including human–animal interactions in assessments of animal welfare. Animals 10, 1870. https://doi.org/10.3390/ani10101870 (2020).
doi: 10.3390/ani10101870
pubmed: 33066335
pmcid: 7602120
Leconstant, C. & Spitz, E. Integrative model of human–animal interactions: A one health-one welfare systemic approach to studying HAI. Front. Vet. Sci. 9, 656833. https://doi.org/10.3389/fvets.2022.656833 (2022).
doi: 10.3389/fvets.2022.656833
pubmed: 35968006
pmcid: 9372562
Acharya, R. Y., Hemsworth, P. H., Coleman, G. J. & Kinder, J. E. The animal–human interface in farm animal production: Animal fear, stress, reproduction and welfare. Animals 12, 487. https://doi.org/10.3390/ani12040487 (2022).
doi: 10.3390/ani12040487
pubmed: 35203194
pmcid: 8868546
Mellor, D. Enhancing animal welfare by creating opportunities for positive affective engagement. New Zealand Vet. J. 63, 3–8. https://doi.org/10.1080/00480169.2014.926799 (2015).
doi: 10.1080/00480169.2014.926799
Rault, J.-L., Hintze, S., Camerlink, I. & Yee, J. R. Positive welfare and the like: Distinct views and a proposed framework. Front. Vet. Sci. 7, 370. https://doi.org/10.3389/fvets.2020.00370 (2020).
doi: 10.3389/fvets.2020.00370
pubmed: 32714949
pmcid: 7343720
Rault, J.-L., Waiblinger, S., Boivin, X. & Hemsworth, P. The power of a positive human–animal relationship for animal welfare. Front. Vet. Sci. 7, 590867. https://doi.org/10.3389/fvets.2020.590867 (2020).
doi: 10.3389/fvets.2020.590867
pubmed: 33240961
pmcid: 7680732
Hemsworth, P. H. & Barnett, J. L. The effects of early contact with humans on the subsequent level of fear of humans in pigs. Appl. Animal Behav. Sci. 35, 83–90. https://doi.org/10.1016/0168-1591(92)90018-7 (1992).
doi: 10.1016/0168-1591(92)90018-7
Hayes, M. E., Hemsworth, L. M., Morrison, R. S., Tilbrook, A. J. & Hemsworth, P. H. Positive human contact and housing systems impact the responses of piglets to various stressors. Animals 11, 1619. https://doi.org/10.3390/ani11061619 (2021).
doi: 10.3390/ani11061619
pubmed: 34070802
pmcid: 8227335
Hemsworth, P. H., Price, E. O. & Borgwardt, R. Behavioural responses of domestic pigs and cattle to humans and novel stimuli. Appl. Animal Behav. Sci. 50, 43–56. https://doi.org/10.1016/0168-1591(96)01067-2 (1996).
doi: 10.1016/0168-1591(96)01067-2
Lensink, B. J., Boivin, X., Pradel, P., Le Neindre, P. & Veissier, I. Reducing veal calves’ reactivity to people by providing additional human contact. J. Animal Sci. 78, 1213. https://doi.org/10.2527/2000.7851213x (2000).
doi: 10.2527/2000.7851213x
Conley, M. J., Fisher, A. D. & Hemsworth, P. H. Effects of human contact and toys on the fear responses to humans of shelter-housed dogs. Appl. Animal Behav. Sci. 156, 62–69. https://doi.org/10.1016/j.applanim.2014.03.008 (2014).
doi: 10.1016/j.applanim.2014.03.008
Sokołowski, J., Janicka, K., Zięba, G., Junkuszew, A. & Rozempolska-Rucińska, I. Effect of gentle physical contact on behavioural indicators in sheep. Animal. 17, 100924. https://doi.org/10.1016/j.animal.2023.100924 (2023).
doi: 10.1016/j.animal.2023.100924
pubmed: 37611436
Claxton, A. M. The potential of the human–animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Appl. Animal Behav. Sci. 133, 1–10. https://doi.org/10.1016/j.applanim.2011.03.002 (2011).
doi: 10.1016/j.applanim.2011.03.002
Ward, S. J. & Melfi, V. The implications of husbandry training on zoo animal response rates. Appl. Animal Behav. Sci. 147, 179–185. https://doi.org/10.1016/j.applanim.2013.05.008 (2013).
doi: 10.1016/j.applanim.2013.05.008
Cloutier, S., Baker, C., Wahl, K., Panksepp, J. & Newberry, R. C. Playful handling as social enrichment for individually- and group-housed laboratory rats. Appl. Animal Behav. Sci. 143, 85–95. https://doi.org/10.1016/j.applanim.2012.10.006 (2013).
doi: 10.1016/j.applanim.2012.10.006
Baker, K. C. Survey of 2014 behavioral management programs for laboratory primates in the United States. Am. J. Primatol. 78, 780–796. https://doi.org/10.1002/ajp.22543 (2016).
doi: 10.1002/ajp.22543
pubmed: 26971575
pmcid: 4914436
Büttner, K., Czycholl, I., Basler, H. & Krieter, J. Effects of an intensified human–animal interaction on tail biting in pigs during the rearing period. J. Agric. Sci. 156, 1039–1046. https://doi.org/10.1017/S002185961800103X (2018).
doi: 10.1017/S002185961800103X
Baker, K. Benefits of positive human interaction for socially housed chimpanzees. Anim. welf. 13, 239–245. https://doi.org/10.1017/S0962728600026981 (2004).
doi: 10.1017/S0962728600026981
pubmed: 20505791
Lange, A., Bauer, L., Futschik, A., Waiblinger, S. & Lürzel, S. Talking to cows: Reactions to different auditory stimuli during gentle human–animal interactions. Front. Psychol. 11, 579346. https://doi.org/10.3389/fpsyg.2020.579346 (2020).
doi: 10.3389/fpsyg.2020.579346
pubmed: 33178082
pmcid: 7593841
Hosey, G. & Melfi, V. Human–animal interactions, relationships and bonds: A review and analysis of the literature. IJCP. https://doi.org/10.46867/ijcp.2014.27.01.01 (2014).
doi: 10.46867/ijcp.2014.27.01.01
Rodriguez, K. E., Herzog, H. & Gee, N. R. Variability in human–animal interaction research. Front. Vet. Sci. 7, 619600. https://doi.org/10.3389/fvets.2020.619600 (2021).
doi: 10.3389/fvets.2020.619600
pubmed: 33521092
pmcid: 7843787
Schmied, C., Waiblinger, S., Scharl, T., Leisch, F. & Boivin, X. Stroking of different body regions by a human: Effects on behaviour and heart rate of dairy cows. Appl. Animal Behav. Sci. 109, 25–38. https://doi.org/10.1016/j.applanim.2007.01.013 (2008).
doi: 10.1016/j.applanim.2007.01.013
Lange, A. et al. Effects of different stroking styles on behaviour and cardiac parameters in heifers. Animals 10, 426. https://doi.org/10.3390/ani10030426 (2020).
doi: 10.3390/ani10030426
pubmed: 32143274
pmcid: 7143138
Tallet, C. et al. Behavioural and physiological reactions of piglets to gentle tactile interactions vary according to their previous experience with humans. Livestock Sci. 167, 331–341. https://doi.org/10.1016/j.livsci.2014.06.025 (2014).
doi: 10.1016/j.livsci.2014.06.025
LaFollette, M. R., O’Haire, M. E., Cloutier, S., Blankenberger, W. B. & Gaskill, B. N. Rat tickling: A systematic review of applications, outcomes, and moderators. PLoS ONE 12, e0175320. https://doi.org/10.1371/journal.pone.0175320 (2017).
doi: 10.1371/journal.pone.0175320
pubmed: 28384364
pmcid: 5383284
Rehn, T., Handlin, L., Uvnäs-Moberg, K. & Keeling, L. J. Dogs’ endocrine and behavioural responses at reunion are affected by how the human initiates contact. Physiol. Behav. 124, 45–53. https://doi.org/10.1016/j.physbeh.2013.10.009 (2014).
doi: 10.1016/j.physbeh.2013.10.009
pubmed: 24471179
Terlouw, E. M. C. & Porcher, J. Repeated handling of pigs during rearing. I. Refusal of contact by the handler and reactivity to familiar and unfamiliar humans. J. Animal Sci. 83, 1653–1663. https://doi.org/10.2527/2005.8371653x (2005).
doi: 10.2527/2005.8371653x
Luna, D. et al. The effect of demonstrator social rank on the attentiveness and motivation of pigs to positively interact with their human caretakers. Animals 11, 2140. https://doi.org/10.3390/ani11072140 (2021).
doi: 10.3390/ani11072140
pubmed: 34359267
pmcid: 8300723
Lange, A. et al. Effects of restraint on heifers during gentle human–animal interactions. Appl. Animal Behav. Sci. 243, 105445. https://doi.org/10.1016/j.applanim.2021.105445 (2021).
doi: 10.1016/j.applanim.2021.105445
Manciocco, A., Chiarotti, F. & Vitale, A. Effects of positive interaction with caretakers on the behaviour of socially housed common marmosets (Callithrix jacchus). Appl. Animal Behav. Sci. 120, 100–107. https://doi.org/10.1016/j.applanim.2009.05.007 (2009).
doi: 10.1016/j.applanim.2009.05.007
Barber, O., Somogyi, E., McBride, A. E. & Proops, L. Children’s evaluations of a therapy dog and biomimetic robot: Influences of animistic beliefs and social interaction. Int. J. Soc. Robot. 13, 1411–1425. https://doi.org/10.1007/s12369-020-00722-0 (2021).
doi: 10.1007/s12369-020-00722-0
Redcay, E. & Schilbach, L. Using second-person neuroscience to elucidate the mechanisms of social interaction. Nat. Rev. Neurosci. 20, 495–505. https://doi.org/10.1038/s41583-019-0179-4 (2019).
doi: 10.1038/s41583-019-0179-4
pubmed: 31138910
pmcid: 6997943
Dale, R., Yu, C., Nagai, Y., Coco, M. & Kopp, S. Embodied approaches to interpersonal coordination: Infants, adults, robots, and agents. (2013).
Schilbach, L. et al. Toward a second-person neuroscience. Behav. Brain Sci. 36, 393–414. https://doi.org/10.1017/S0140525X12000660 (2013).
doi: 10.1017/S0140525X12000660
pubmed: 23883742
Pop, D., Rusu, A. S. & Miresan, V. The development of a canine para-agility program: Positive affects in children with autism and in therapy dogs. BUASVMCN-ASB 73, 66–71. https://doi.org/10.15835/buasvmcn-asb:11812 (2016).
FAOSTAT. Food and Agriculture Organization of the United Nations (FAO), Crops and livestock products. https://www.fao.org/faostat/en/#data/QCL (2024).
Marchant-Forde, J. N. & Herskin, M. S. Pigs as laboratory animals. in Advances in Pig Welfare 445–475. https://doi.org/10.1016/B978-0-08-101012-9.00015-0 (Elsevier, 2018).
Gerencsér, L., Pérez Fraga, P., Lovas, M., Újváry, D. & Andics, A. Comparing interspecific socio-communicative skills of socialized juvenile dogs and miniature pigs. Anim. Cogn. 22, 917–929. https://doi.org/10.1007/s10071-019-01284-z (2019).
doi: 10.1007/s10071-019-01284-z
pubmed: 31256339
pmcid: 6834752
Graves, H. B. Behavior and ecology of wild and feral swine (Sus Scrofa). J. Animal Sci. 58, 482–492. https://doi.org/10.2527/jas1984.582482x (1984).
doi: 10.2527/jas1984.582482x
Tallet, C., Brajon, S., Devillers, N. & Lensink, J. Pig–human interactions. in Advances in Pig Welfare 381–398. https://doi.org/10.1016/B978-0-08-101012-9.00008-3 (Elsevier, 2018).
Villain, A. S., Lanthony, M., Guérin, C. & Tallet, C. Manipulable object and human contact: Preference and modulation of emotional states in weaned pigs. Front. Vet. Sci. 7, 577433. https://doi.org/10.3389/fvets.2020.577433 (2020).
doi: 10.3389/fvets.2020.577433
pubmed: 33330698
pmcid: 7728720
Hemsworth, P. H., Gonyou, H. W. & Dziuk, P. J. Human communication with pigs: The behavioural response of pigs to specific human signals. Appl. Animal Behav. Sci. 15, 45–54. https://doi.org/10.1016/0168-1591(86)90021-3 (1986).
doi: 10.1016/0168-1591(86)90021-3
Day, J. E. L., Spoolder, H. A. M., Burfoot, A., Chamberlain, H. L. & Edwards, S. A. The separate and interactive effects of handling and environmental enrichment on the behaviour and welfare of growing pigs. Appl. Animal Behav. Sci. 75, 177–192. https://doi.org/10.1016/S0168-1591(01)00199-X (2002).
doi: 10.1016/S0168-1591(01)00199-X
Lürzel, S., Bückendorf, L., Waiblinger, S. & Rault, J.-L. Salivary oxytocin in pigs, cattle, and goats during positive human–animal interactions. Psychoneuroendocrinology 115, 104636. https://doi.org/10.1016/j.psyneuen.2020.104636 (2020).
doi: 10.1016/j.psyneuen.2020.104636
pubmed: 32160578
Miura, A., Tanida, H., Tanaka, T. & Yoshimoto, T. The influence of human posture and movement on the approach and escape behaviour of weanling pigs. Appl. Animal Behav. Sci. 49, 247–256. https://doi.org/10.1016/0168-1591(95)00658-3 (1996).
doi: 10.1016/0168-1591(95)00658-3
Reimert, I., Bolhuis, J. E., Kemp, B. & Rodenburg, T. B. Indicators of positive and negative emotions and emotional contagion in pigs. Physiol. Behav. 109, 42–50. https://doi.org/10.1016/j.physbeh.2012.11.002 (2013).
doi: 10.1016/j.physbeh.2012.11.002
pubmed: 23159725
Reimert, I., Fong, S., Rodenburg, T. B. & Bolhuis, J. E. Emotional states and emotional contagion in pigs after exposure to a positive and negative treatment. Appl. Animal Behav. Sci. 193, 37–42. https://doi.org/10.1016/j.applanim.2017.03.009 (2017).
doi: 10.1016/j.applanim.2017.03.009
Rius, M. M. et al. Tail and ear movements as possible indicators of emotions in pigs. Appl. Animal Behav. Sci. 205, 14–18. https://doi.org/10.1016/j.applanim.2018.05.012 (2018).
doi: 10.1016/j.applanim.2018.05.012
Ocepek, M., Newberry, R. C. & Andersen, I. L. Which types of rooting material give weaner pigs most pleasure?. Appl. Animal Behav. Sci. 231, 105070. https://doi.org/10.1016/j.applanim.2020.105070 (2020).
doi: 10.1016/j.applanim.2020.105070
Jensen, K. H. et al. Intermittent stress in pigs: Effects on behavior, pituitary—Adrenocortical axis, growth, and gastric ulceration. Physiol. Behav. 59, 741–748. https://doi.org/10.1016/0031-9384(95)02159-0 (1996).
doi: 10.1016/0031-9384(95)02159-0
pubmed: 8778861
Anderson, C., Von Keyserlingk, M., Lidfors, L. & Weary, D. Anticipatory behaviour in animals: A critical review. Anim. Welf. 29, 231–238. https://doi.org/10.7120/09627286.29.3.231 (2020).
doi: 10.7120/09627286.29.3.231
Dantzer, R., Arnone, M. & Mormede, P. Effects of frustration on behaviour and plasma corticosteroid levels in pigs. Physiol. Behav. 24, 1–4 (1980).
doi: 10.1016/0031-9384(80)90005-0
pubmed: 7189887
Arnone, M. & Dantzer, R. Does frustration induce aggression in pigs?. Appl. Animal Ethol. 6, 351–362. https://doi.org/10.1016/0304-3762(80)90135-2 (1980).
doi: 10.1016/0304-3762(80)90135-2
Hill, H. M. M. et al. Cetacean responses to violation of expectation paradigm in a free-swim context. Anim. Cogn. 26, 667–686. https://doi.org/10.1007/s10071-022-01704-7 (2023).
doi: 10.1007/s10071-022-01704-7
pubmed: 36333497
Völter, C. J., Tomašić, A., Nipperdey, L. & Huber, L. Dogs’ expectations about occlusion events: From expectancy violation to exploration. Proc. R. Soc. B. 290, 20230696. https://doi.org/10.1098/rspb.2023.0696 (2023).
doi: 10.1098/rspb.2023.0696
pubmed: 37464755
pmcid: 10354481
Špinka, M. Animal agency, animal awareness and animal welfare. Anim. welf. 28, 11–20. https://doi.org/10.7120/09627286.28.1.011 (2019).
doi: 10.7120/09627286.28.1.011
Tallet, C. et al. Encoding of situations in the vocal repertoire of piglets (Sus scrofa): A comparison of discrete and graded classifications. PLoS ONE 8, e71841. https://doi.org/10.1371/journal.pone.0071841 (2013).
doi: 10.1371/journal.pone.0071841
pubmed: 23967251
pmcid: 3742501
Marchant, J. N., Whittaker, X. & Broom, D. M. Vocalisations of the adult female domestic pig during a standard human approach test and their relationships with behavioural and heart rate measures. Appl. Animal Behav. Sci. 72, 23–39. https://doi.org/10.1016/S0168-1591(00)00190-8 (2001).
doi: 10.1016/S0168-1591(00)00190-8
Bensoussan, S., Tigeot, R., Meunier-Salaün, M.-C. & Tallet, C. Broadcasting human voice to piglets (Sus scrofa domestica) modifies their behavioural reaction to human presence in the home pen and in arena tests. Appl. Animal Behav. Sci. 225, 104965. https://doi.org/10.1016/j.applanim.2020.104965 (2020).
doi: 10.1016/j.applanim.2020.104965
Murphy, E., Nordquist, R. E. & Van Der Staay, F. J. A review of behavioural methods to study emotion and mood in pigs, Sus scrofa. Appl. Animal Behav. Sci. 159, 9–28. https://doi.org/10.1016/j.applanim.2014.08.002 (2014).
doi: 10.1016/j.applanim.2014.08.002
Rault, J.-L. et al. Gentle abdominal stroking (‘belly rubbing’) of pigs by a human reduces EEG total power and increases EEG frequencies. Behav. Brain Res. 374, 111892. https://doi.org/10.1016/j.bbr.2019.04.006 (2019).
doi: 10.1016/j.bbr.2019.04.006
pubmed: 30959126
Friard, O. & Gamba, M. BORIS: A free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330. https://doi.org/10.1111/2041-210X.12584 (2016).
doi: 10.1111/2041-210X.12584
Bateson, M. & Martin, P. Measuring Behaviour: An Introductory Guide (Cambridge University Press, 2021).
doi: 10.1017/9781108776462
Camerlink, I. & Ursinus, W. W. Tail postures and tail motion in pigs: A review. Appl. Animal Behav. Sci. 230, 105079. https://doi.org/10.1016/j.applanim.2020.105079 (2020).
doi: 10.1016/j.applanim.2020.105079
Camerlink, I., Proßegger, C., Kubala, D., Galunder, K. & Rault, J.-L. Keeping littermates together instead of social mixing benefits pig social behaviour and growth post-weaning. Appl. Animal Behav. Sci. 235, 105230. https://doi.org/10.1016/j.applanim.2021.105230 (2021).
doi: 10.1016/j.applanim.2021.105230
R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (2024).
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015) Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 .
Brooks, M. E. et al. (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400. https://doi.org/10.32614/RJ-2017-066 .
Field, A. Repeated-measures designs. Discovering Statistics Using SPSS 427–482. (2005).
Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists (Cambridge University Press, 2002).
doi: 10.1017/CBO9780511806384
Fox, J. & Weisberg, S. An R Companion to Applied Regression. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion (Sage, Thousand Oaks, 2019).
Lenth, R. V. Emmeans: Estimated Marginal Means, Aka Least-Squares Means. https://CRAN.R-project.org/package=emmeans (2023).
Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 65, 47–55. https://doi.org/10.1007/s00265-010-1038-5 (2011).
doi: 10.1007/s00265-010-1038-5
pubmed: 21297852
Dobson, A. J. & Barnett, A. G. An Introduction to Generalized Linear Models, 4th Edn. https://doi.org/10.1201/9781315182780 (Chapman and Hall/CRC, 2018).
Luke, S. G. Evaluating significance in linear mixed-effects models in R. Behav. Res. 49, 1494–1502. https://doi.org/10.3758/s13428-016-0809-y (2017).
doi: 10.3758/s13428-016-0809-y
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. (2017) lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26. https://doi.org/10.18637/jss.v082.i13 .
Therneau, T. M. & Grambsch, P. M. Modeling Survival Data: Extending the Cox Model. https://CRAN.R-project.org/package=survival (Springer, New York, 2000).
Kassambara, A., Kosinski, M. & Biecek, P. Survminer: Drawing Survival Curves Using ‘Ggplot2’. https://CRAN.R-project.org/package=survminer (2021).