Future application of an attention bias test to assess affective states in sheep
Jessica E. Monk
A B , Dana L. M. Campbell A and Caroline Lee A *
+ Author Affiliations
- Author Affiliations
A Agriculture and Food, CSIRO, Armidale, NSW, Australia.
B School of Environmental and Rural Science, University of New England, Armidale, NSW, Australia.
Animal Production Science 63(6) 523-534 https://doi.org/10.1071/AN22260
Submitted: 1 July 2022 Accepted: 30 January 2023 Published: 27 February 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
The affective states of animals comprise a key aspect of welfare that can be difficult to assess. An attention-bias test was developed for sheep, which assessed allocation of attention between a predator threat and a food reward, as a potential measure of affective state. The method was pharmacologically validated as a measure of anxiety-like states, finding that ‘anxious’ sheep were more vigilant, less likely to feed and spent more time looking towards the previous location of a dog than did ‘calm’ sheep. Across six further validation studies, the method was modified and explored as a measure of other types of affective states. This perspective article aims to provide guidance on what the method can tell us about affective state and make recommendations for further research by using this approach. Evidence was strongest across the studies for the test as a measure of anxiety-like states, but it is clear that there are other factors affecting animal behaviour during testing that need to be further investigated. One study showed potential for a modified method to assess depression-like states in sheep, while the impact of chronic stress on affect and attention bias remains unclear. It is likely that the test cannot be used to measure positive affect in sheep without further modification, due to the fear-eliciting nature of the test. Versions of the method using food as a positive stimulus allow for a clearer interpretation of attention than do versions using a conspecific photograph, and are recommended for use in future studies where appetite is not expected to be a confounding factor. In this context, vigilance behaviour may indicate trait anxiety or fearfulness, while other measures of attention may be more sensitive to transient changes in affect. Modifications to the method are suggested to allow for a clearer characterisation of attention in livestock species and to improve the practical application of the test. Overall, the attention-bias test shows promise as a measure of negative affective states, but the method is still very new and further research is needed to better determine its potential use as a welfare-assessment tool.
Keywords: anxiety, behaviour, cognitive bias, depression, euphoria, fear, livestock, Merino, ruminant, sheep, threat, welfare.
References
Anderson MG, Campbell AM, Crump A, Arnott G, Newberry RC, Jacobs L (2021) Effect of environmental complexity and stocking density on fear and anxiety in broiler chickens. Animals 11, 2383| Effect of environmental complexity and stocking density on fear and anxiety in broiler chickens.Crossref | GoogleScholarGoogle Scholar |
Atkinson L, Doyle RE, Woodward A, Jongman EC (2022) Exposure to humans after weaning does not reduce the behavioural reactivity of extensively reared Merino lambs. Behavioural Processes 201, 104709
| Exposure to humans after weaning does not reduce the behavioural reactivity of extensively reared Merino lambs.Crossref | GoogleScholarGoogle Scholar |
Australian Government (2008) ‘The Australian animal welfare strategy.’ Revised edn. (Australian Government)
Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg MJ, van IJzendoorn MH (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychological Bulletin 133, 1–24.
| Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study.Crossref | GoogleScholarGoogle Scholar |
Beausoleil NJ, Stafford KJ, Mellor DJ (2005) Sheep show more aversion to a dog than to a human in an arena test. Applied Animal Behaviour Science 91, 219–232.
| Sheep show more aversion to a dog than to a human in an arena test.Crossref | GoogleScholarGoogle Scholar |
Bethell EJ, Holmes A, MacLarnon A, Semple S (2012) Evidence that emotion mediates social attention in rhesus macaques. PLoS ONE 7, e44387
| Evidence that emotion mediates social attention in rhesus macaques.Crossref | GoogleScholarGoogle Scholar |
Boissy A, Erhard HW (2014) How studying interactions between animal emotions, cognition, and personality can contribute to improve farm animal welfare. In ‘Genetics and the behavior of domestic animals’. (Eds T Grandin, MJ Deesing) pp. 81–113. (Elsevier) https://doi.org/10.1016/B978-0-12-394586-0.00003-2
Boissy A, Aubert A, Désiré L, Greiveldinger L, Delval E, Veissier I (2011) Cognitive sciences to relate ear postures to emotions in sheep. Animal Welfare 20, 47–56.
| Cognitive sciences to relate ear postures to emotions in sheep.Crossref | GoogleScholarGoogle Scholar |
Bouissou MF, Vandenheede M (1995) Fear reactions of domestic sheep confronted with either a human or a human-like model. Behavioural Processes 34, 81–92.
| Fear reactions of domestic sheep confronted with either a human or a human-like model.Crossref | GoogleScholarGoogle Scholar |
Bradley BP, Mogg K, Millar N, White J (1995) Selective processing of negative information: effects of clinical anxiety, concurrent depression, and awareness. Journal of Abnormal Psychology 104, 532–536.
| Selective processing of negative information: effects of clinical anxiety, concurrent depression, and awareness.Crossref | GoogleScholarGoogle Scholar |
Bradley BP, Mogg K, Lee SC (1997) Attentional biases for negative information in induced and naturally occurring dysphoria. Behaviour Research and Therapy 35, 911–927.
| Attentional biases for negative information in induced and naturally occurring dysphoria.Crossref | GoogleScholarGoogle Scholar |
Brilot BO, Bateson M (2012) Water bathing alters threat perception in starlings. Biology Letters 8, 379–381.
| Water bathing alters threat perception in starlings.Crossref | GoogleScholarGoogle Scholar |
Brioni JD, Arolfo MP (1992) Diazepam impairs retention of spatial information without affecting retrieval or cue learning. Pharmacology Biochemistry and Behavior 41, 1–5.
| Diazepam impairs retention of spatial information without affecting retrieval or cue learning.Crossref | GoogleScholarGoogle Scholar |
Campbell DLM, Dickson EJ, Lee C (2019a) Application of open field, tonic immobility, and attention bias tests to hens with different ranging patterns. PeerJ 7, e8122
| Application of open field, tonic immobility, and attention bias tests to hens with different ranging patterns.Crossref | GoogleScholarGoogle Scholar |
Campbell DLM, Taylor PS, Hernandez CE, Stewart M, Belson S, Lee C (2019b) An attention bias test to assess anxiety states in laying hens. PeerJ 7, e7303
| An attention bias test to assess anxiety states in laying hens.Crossref | GoogleScholarGoogle Scholar |
Campbell AM, Johnson AM, Persia ME, Jacobs L (2022) Effects of housing system on anxiety, chronic stress, fear, and immune function in Bovan brown laying hens. Animals 12, 1803
| Effects of housing system on anxiety, chronic stress, fear, and immune function in Bovan brown laying hens.Crossref | GoogleScholarGoogle Scholar |
Cisler JM, Koster EHW (2010) Mechanisms of attentional biases towards threat in anxiety disorders: an integrative review. Clinical Psychology Review 30, 203–216.
| Mechanisms of attentional biases towards threat in anxiety disorders: an integrative review.Crossref | GoogleScholarGoogle Scholar |
Coulon M, Hild S, Schroeer A, Janczak AM, Zanella AJ (2011) Gentle vs. aversive handling of pregnant ewes: II. Physiology and behavior of the lambs. Physiology & Behavior 103, 575–584.
| Gentle vs. aversive handling of pregnant ewes: II. Physiology and behavior of the lambs.Crossref | GoogleScholarGoogle Scholar |
Crump A, Arnott G, Bethell E (2018) Affect-driven attention biases as animal welfare indicators: review and methods. Animals 8, 136
| Affect-driven attention biases as animal welfare indicators: review and methods.Crossref | GoogleScholarGoogle Scholar |
Cussen VA, Mench JA (2014) Personality predicts cognitive bias in captive psittacines, Amazona amazonica. Animal Behaviour 89, 123–130.
| Personality predicts cognitive bias in captive psittacines, Amazona amazonica.Crossref | GoogleScholarGoogle Scholar |
Doyle RE, Fisher AD, Hinch GN, Boissy A, Lee C (2010) Release from restraint generates a positive judgement bias in sheep. Applied Animal Behaviour Science 122, 28–34.
| Release from restraint generates a positive judgement bias in sheep.Crossref | GoogleScholarGoogle Scholar |
Doyle RE, Lee C, McGill DM, Mendl M (2015) Evaluating pharmacological models of high and low anxiety in sheep. PeerJ 3, e1510
| Evaluating pharmacological models of high and low anxiety in sheep.Crossref | GoogleScholarGoogle Scholar |
Dwyer CM (2004) How has the risk of predation shaped the behavioural responses of sheep to fear and distress? Animal Welfare 13, 269–281.
| How has the risk of predation shaped the behavioural responses of sheep to fear and distress?Crossref | GoogleScholarGoogle Scholar |
Dwyer CM (2009) Welfare of sheep: providing for welfare in an extensive environment. Small Ruminant Research 86, 14–21.
| Welfare of sheep: providing for welfare in an extensive environment.Crossref | GoogleScholarGoogle Scholar |
Eizenman M, Yu LH, Grupp L, Eizenman E, Ellenbogen M, Gemar M, Levitan RD (2003) A naturalistic visual scanning approach to assess selective attention in major depressive disorder. Psychiatry Research 118, 117–128.
| A naturalistic visual scanning approach to assess selective attention in major depressive disorder.Crossref | GoogleScholarGoogle Scholar |
Erhard HW, Elston DA, Davidson GC (2006) Habituation and extinction in an approach–avoidance test: an example with sheep. Applied Animal Behaviour Science 99, 132–144.
| Habituation and extinction in an approach–avoidance test: an example with sheep.Crossref | GoogleScholarGoogle Scholar |
Forkman B, Boissy A, Meunier-Salaün M-C, Canali E, Jones RB (2007) A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiology & Behavior 92, 340–374.
| A critical review of fear tests used on cattle, pigs, sheep, poultry and horses.Crossref | GoogleScholarGoogle Scholar |
Franklin JR, Hutson GD (1982) Experiments on attracting sheep to move along a laneway. III. Visual stimuli. Applied Animal Ethology 8, 457–478.
| Experiments on attracting sheep to move along a laneway. III. Visual stimuli.Crossref | GoogleScholarGoogle Scholar |
Fraser D, Duncan IJH (1998) ‘Pleasures’,‘pains’ and animal welfare: toward a natural history of affect. Animal Welfare 7, 383–396.
| ‘Pleasures’,‘pains’ and animal welfare: toward a natural history of affect.Crossref | GoogleScholarGoogle Scholar |
Guldimann K, Vögeli S, Wolf M, Wechsler B, Gygax L (2015) Frontal brain deactivation during a non-verbal cognitive judgement bias test in sheep. Brain and Cognition 93, 35–41.
| Frontal brain deactivation during a non-verbal cognitive judgement bias test in sheep.Crossref | GoogleScholarGoogle Scholar |
Hermans D, Vansteenwegen D, Eelen P (1999) Eye movement registration as a continuous index of attention deployment: data from a group of spider anxious students. Cognition & Emotion 13, 419–434.
| Eye movement registration as a continuous index of attention deployment: data from a group of spider anxious students.Crossref | GoogleScholarGoogle Scholar |
Howarth ERI, Kemp C, Thatcher HR, Szott ID, Farningham D, Witham CL, Holmes A, Semple S, Bethell EJ (2021) Developing and validating attention bias tools for assessing trait and state affect in animals: a worked example with Macaca mulatta. Applied Animal Behaviour Science 234, 105198
| Developing and validating attention bias tools for assessing trait and state affect in animals: a worked example with Macaca mulatta.Crossref | GoogleScholarGoogle Scholar |
Kauppinen T, Vainio A, Valros A, Rita H, Vesala KM (2010) Improving animal welfare: qualitative and quantitative methodology in the study of farmers’ attitudes. Animal Welfare 19, 523–536.
| Improving animal welfare: qualitative and quantitative methodology in the study of farmers’ attitudes.Crossref | GoogleScholarGoogle Scholar |
Kellough JL, Beevers CG, Ellis AJ, Wells TT (2008) Time course of selective attention in clinically depressed young adults: an eye tracking study. Behaviour Research and Therapy 46, 1238–1243.
| Time course of selective attention in clinically depressed young adults: an eye tracking study.Crossref | GoogleScholarGoogle Scholar |
Kremer L, Klein Holkenborg SEJ, Reimert I, Bolhuis JE, Webb LE (2020) The nuts and bolts of animal emotion. Neuroscience & Biobehavioral Reviews 113, 273–286.
| The nuts and bolts of animal emotion.Crossref | GoogleScholarGoogle Scholar |
Kremer L, Bus JD, Webb LE, Bokkers EAM, Engel B, van der Werf JTN, Schnabel SK, van Reenen CG (2021) Housing and personality effects on judgement and attention biases in dairy cows. Scientific Reports 11, 22984
| Housing and personality effects on judgement and attention biases in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Lee C, Verbeek E, Doyle R, Bateson M (2016) Attention bias to threat indicates anxiety differences in sheep. Biology Letters 12, 20150977
| Attention bias to threat indicates anxiety differences in sheep.Crossref | GoogleScholarGoogle Scholar |
Lee C, Cafe LM, Robinson SL, Doyle RE, Lea JM, Small AH, Colditz IG (2018) Anxiety influences attention bias but not flight speed and crush score in beef cattle. Applied Animal Behaviour Science 205, 210–215.
| Anxiety influences attention bias but not flight speed and crush score in beef cattle.Crossref | GoogleScholarGoogle Scholar |
Luo L, Reimert I, de Haas EN, Kemp B, Bolhuis JE (2019) Effects of early and later life environmental enrichment and personality on attention bias in pigs (Sus scrofa domesticus). Animal Cognition 22, 959–972.
| Effects of early and later life environmental enrichment and personality on attention bias in pigs (Sus scrofa domesticus).Crossref | GoogleScholarGoogle Scholar |
Lynch JJ, Hinch GN, Adams DB (1992) ‘The behaviour of sheep: biological principles and implications for production.’ (CSIRO: Melbourne, Vic., Australia)
Mendl M, Burman OHP, Paul ES (2010) An integrative and functional framework for the study of animal emotion and mood. Proceedings of the Royal Society B: Biological Sciences 277, 2895–2904.
| An integrative and functional framework for the study of animal emotion and mood.Crossref | GoogleScholarGoogle Scholar |
Monk JE, Doyle RE, Colditz IG, Belson S, Cronin GM, Lee C (2018a) Towards a more practical attention bias test to assess affective state in sheep. PLoS ONE 13, e0190404
| Towards a more practical attention bias test to assess affective state in sheep.Crossref | GoogleScholarGoogle Scholar |
Monk JE, Belson S, Colditz IG, Lee C (2018b) Attention bias test differentiates anxiety and depression in sheep. Frontiers in Behavioral Neuroscience 12, 246
| Attention bias test differentiates anxiety and depression in sheep.Crossref | GoogleScholarGoogle Scholar |
Monk JE, Belson S, Lee C (2019a) Pharmacologically-induced stress has minimal impact on judgement and attention biases in sheep. Scientific Reports 9, 11446
| Pharmacologically-induced stress has minimal impact on judgement and attention biases in sheep.Crossref | GoogleScholarGoogle Scholar |
Monk JE, Lee C, Belson S, Colditz IG, Campbell DLM (2019b) The influence of pharmacologically-induced affective states on attention bias in sheep. PeerJ 7, e7033
| The influence of pharmacologically-induced affective states on attention bias in sheep.Crossref | GoogleScholarGoogle Scholar |
Monk JE, Lee C, Dickson E, Campbell DLM (2020) Attention bias test measures negative but not positive affect in sheep: a replication study. Animals 10, 1314
| Attention bias test measures negative but not positive affect in sheep: a replication study.Crossref | GoogleScholarGoogle Scholar |
Monk JE, Colditz IG, Clark S, Lee C (2023) Repeatability of an attention bias test for sheep suggests variable influence of state and trait affect on behaviour. PeerJ 11, e14730
| Repeatability of an attention bias test for sheep suggests variable influence of state and trait affect on behaviour.Crossref | GoogleScholarGoogle Scholar |
Neave HW, Zobel G (2020) Personality of dairy goats affects competitive feeding behaviour at different feeder heights. Small Ruminant Research 192, 106222
| Personality of dairy goats affects competitive feeding behaviour at different feeder heights.Crossref | GoogleScholarGoogle Scholar |
Pergamin-Hight L, Naim R, Bakermans-Kranenburg MJ Pergamin-Hight L, Naim R, Bakermans-Kranenburg MJ (2015) Content specificity of attention bias to threat in anxiety disorders: A meta-analysis. Clinical Psychology Review 35, 10–18.
| Content specificity of attention bias to threat in anxiety disorders: A meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Raoult C, Gygax L (2018) Valence and intensity of video stimuli of dogs and conspecifics in sheep: approach–avoidance, operant response, and attention. Animals 8, 121
| Valence and intensity of video stimuli of dogs and conspecifics in sheep: approach–avoidance, operant response, and attention.Crossref | GoogleScholarGoogle Scholar |
Raoult CMC, Gygax L (2019) Mood induction alters attention toward negative–positive stimulus pairs in sheep. Scientific Reports 9, 7759
| Mood induction alters attention toward negative–positive stimulus pairs in sheep.Crossref | GoogleScholarGoogle Scholar |
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biological Reviews 82, 291–318.
| Integrating animal temperament within ecology and evolution.Crossref | GoogleScholarGoogle Scholar |
Red Meat Advisory Council Ltd (2015) Meat industry strategic plan MISP 2020. Red Meat Advisory Council, Canberra, ACT, Australia.
Reefmann N, Bütikofer Kaszàs F, Wechsler B, Gygax L (2009) Ear and tail postures as indicators of emotional valence in sheep. Applied Animal Behaviour Science 118, 199–207.
| Ear and tail postures as indicators of emotional valence in sheep.Crossref | GoogleScholarGoogle Scholar |
Salvin H, Cafe L, Lees A, Morris S, Lee C (2020) A novel protocol to measure startle magnitude in sheep. Applied Animal Behaviour Science 228, 104996
| A novel protocol to measure startle magnitude in sheep.Crossref | GoogleScholarGoogle Scholar |
Sanger ME, Doyle RE, Hinch GN, Lee C (2011) Sheep exhibit a positive judgement bias and stress-induced hyperthermia following shearing. Applied Animal Behaviour Science 131, 94–103.
| Sheep exhibit a positive judgement bias and stress-induced hyperthermia following shearing.Crossref | GoogleScholarGoogle Scholar |
Sasaki-Hamada S, Sacai H, Sugiyama A, Iijima T, Saitoh A, Inagaki M, Yamada M, Oka J-I (2013) Riluzole does not affect hippocampal synaptic plasticity and spatial memory, which are impaired by diazepam in rats. Journal of Pharmacological Sciences 122, 232–236.
| Riluzole does not affect hippocampal synaptic plasticity and spatial memory, which are impaired by diazepam in rats.Crossref | GoogleScholarGoogle Scholar |
Sherwood L, Klandorf H, Yancey PH (2005) ‘Animal physiology: from genes to organisms.’ (Thomson/Brooks/Cole: Australia)
Steimer T (2002) The biology of fear- and anxiety-related behaviors. Dialogues in Clinical Neuroscience 4, 231–249.
| The biology of fear- and anxiety-related behaviors.Crossref | GoogleScholarGoogle Scholar |
Torres-Hernandez G, Hohenboken W (1979) An attempt to assess traits of emotionality in crossbred ewes. Applied Animal Ethology 5, 71–83.
| An attempt to assess traits of emotionality in crossbred ewes.Crossref | GoogleScholarGoogle Scholar |
Vandenheede M, Bouissou MF (1994) Fear reactions of ewes to photographic images. Behavioural Processes 32, 17–28.
| Fear reactions of ewes to photographic images.Crossref | GoogleScholarGoogle Scholar |
Verbeek E, Colditz I, Blache D, Lee C (2019) Chronic stress influences attentional and judgement bias and the activity of the HPA axis in sheep. PLoS ONE 14, e0211363
| Chronic stress influences attentional and judgement bias and the activity of the HPA axis in sheep.Crossref | GoogleScholarGoogle Scholar |
Verbeek E, Dicksved J, Keeling L (2021) Supplementation of Lactobacillus early in life alters attention bias to threat in piglets. Scientific Reports 11, 10130
| Supplementation of Lactobacillus early in life alters attention bias to threat in piglets.Crossref | GoogleScholarGoogle Scholar |
Vögeli S, Wechsler B, Gygax L (2014) Welfare by the ear: comparing relative durations and frequencies of ear postures by using an automated tracking system in sheep. Animal Welfare 23, 267–274.
| Welfare by the ear: comparing relative durations and frequencies of ear postures by using an automated tracking system in sheep.Crossref | GoogleScholarGoogle Scholar |
Vögeli S, Wolf M, Wechsler B, Gygax L (2015) Housing conditions influence cortical and behavioural reactions of sheep in response to videos showing social interactions of different valence. Behavioural Brain Research 284, 69–76.
| Housing conditions influence cortical and behavioural reactions of sheep in response to videos showing social interactions of different valence.Crossref | GoogleScholarGoogle Scholar |
Welp T, Rushen J, Kramer DL, Festa-Bianchet M, de Passillé AMB (2004) Vigilance as a measure of fear in dairy cattle. Applied Animal Behaviour Science 87, 1–13.
| Vigilance as a measure of fear in dairy cattle.Crossref | GoogleScholarGoogle Scholar |
Wemelsfelder F, Farish M (2004) Qualitative categories for the interpretation of sheep welfare: a review. Animal Welfare 13, 261–268.
| Qualitative categories for the interpretation of sheep welfare: a review.Crossref | GoogleScholarGoogle Scholar |
Winters S, Dubuc C, Higham JP (2015) Perspectives: the looking time experimental paradigm in studies of animal visual perception and cognition. Ethology 121, 625–640.
| Perspectives: the looking time experimental paradigm in studies of animal visual perception and cognition.Crossref | GoogleScholarGoogle Scholar |
Zvielli A, Bernstein A, Koster EHW (2014) Dynamics of attentional bias to threat in anxious adults: bias towards and/or away? PLoS ONE 9, e104025
| Dynamics of attentional bias to threat in anxious adults: bias towards and/or away?Crossref | GoogleScholarGoogle Scholar |
