{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T02:28:36Z","timestamp":1792808916936,"version":"4.5.0"},"reference-count":52,"publisher":"PeerJ","license":[{"start":{"date-parts":[[2019,11,25]],"date-time":"2019-11-25T00:00:00Z","timestamp":1574640000000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Poultry Hub Australia","award":["2017-20"],"award-info":[{"award-number":["2017-20"]}],"id":[{"id":"https:\/\/ror.org\/045p3tc45","id-type":"ROR","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000943","name":"Commonwealth Scientific and Industrial Research Organisation","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000943","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>\n                    Assessment of negative affective states is a key component of animal welfare research. In laying hens, excessive fearfulness results in reduced production and increased sensitivity to stress. Fearfulness can be defined as a response to a known threat, but anxiety is a response to an unknown threat and may have similar negative consequences. The open field test and tonic immobility test are commonly applied to measure fearfulness in laying hens. An attention bias test that measured individual hen\u2019s responses to playback of a conspecific alarm call in the presence of food was recently pharmacologically validated using an anxiogenic drug but was confounded by the hen\u2019s typical motionless response in a novel environment. The current study used 56-week old free-range layers to further assess the validity of an attention bias test to differentiate ranging treatment groups in comparison with the open field and tonic immobility tests. The selected hens varied in their range use patterns as tracked by radio-frequency identification technology. \u2018Indoor\u2019 hens did not access the range and \u2018outdoor\u2019 hens ranged daily; previous research has confirmed higher fearfulness in hens that remain indoors. The tonic immobility test did not differentiate ranging groups (\n                    <jats:italic>P<\/jats:italic>\n                    = 0.34), but indoor birds were slower to first step (\n                    <jats:italic>P<\/jats:italic>\n                    = 0.03) and stepped less (\n                    <jats:italic>P<\/jats:italic>\n                    = 0.02) in the open field test. The attention bias test occurred in an isolated wooden box using a conspecific alarm call playback (a threat) and mixed grain (a positive stimulus). The behavioural response of latency to resume eating following playback of the alarm call was measured to differentiate the anxiety states of the indoor and outdoor ranging birds. Before the attention bias test could occur, birds had to be habituated to the test box across three separate 5-minute sessions to increase the willingness to feed within the novel test environment. All birds ate faster across time (\n                    <jats:italic>P<\/jats:italic>\n                    &lt; 0.001) but the indoor birds were slower to eat than the outdoor birds (\n                    <jats:italic>P<\/jats:italic>\n                    &lt; 0.001). In this study, the latency to resume eating following an alarm call was determined to be a poor measure for highly anxious birds as they failed to eat at all. Forty-six percent of indoor hens were excluded for not eating across the 5-minute test. Of the birds that did eat, only 7% of indoor hens ate following playback of the alarm call, compared with 36% of outdoor hens. This repetition of an attention bias test for laying hens highlights the challenges in assessing hens with extreme fearful\/anxious responses and that information may be missed when non-performing hens are excluded from behavioural tests. We suggest that latency to eat in a novel arena without any alarm call playback is an informative measure of anxious state that can be applied to all hens but consideration must be made of potential differences in food motivation.\n                  <\/jats:p>","DOI":"10.7717\/peerj.8122","type":"journal-article","created":{"date-parts":[[2019,11,25]],"date-time":"2019-11-25T03:19:10Z","timestamp":1574651950000},"page":"e8122","source":"Crossref","is-referenced-by-count":66,"title":["Application of open field, tonic immobility, and attention bias tests to hens with different ranging patterns"],"prefix":"10.7717","volume":"7","author":[{"given":"Dana L.M.","family":"Campbell","sequence":"first","affiliation":[{"name":"Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Armidale, New South Wales, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily J.","family":"Dickson","sequence":"additional","affiliation":[{"name":"Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Armidale, New South Wales, Australia"},{"name":"School of Environmental and Rural Science, University of New England, Armidale, New South Wales, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Lee","sequence":"additional","affiliation":[{"name":"Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Armidale, New South Wales, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4443","published-online":{"date-parts":[[2019,11,25]]},"reference":[{"key":"10.7717\/peerj.8122\/ref-1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s40850-019-0039-8","article-title":"External body temperature and vigilance to a lesser extent track variation in predation risk in domestic fowls","volume":"4","author":"Beauchamp","year":"2019","journal-title":"BMC Zoology"},{"key":"10.7717\/peerj.8122\/ref-2","doi-asserted-by":"publisher","first-page":"S18","DOI":"10.1080\/10888705.2015.1075833","article-title":"A how-to guide for designing judgment bias studies to assess captive animal welfare","volume":"18","author":"Bethell","year":"2015","journal-title":"Journal of Applied Animal Welfare Science"},{"key":"10.7717\/peerj.8122\/ref-3","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/j.applanim.2014.06.004","article-title":"Vigilance and roosting behaviour of laying hens on different perch heights","volume":"157","author":"Brendler","year":"2014","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-4","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1098\/rsbl.2011.1200","article-title":"Water bathing alters threat perception in starlings","volume":"8","author":"Brilot","year":"2012","journal-title":"Biology Letters"},{"key":"10.7717\/peerj.8122\/ref-5","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.applanim.2016.09.004","article-title":"Fear and coping styles of outdoor-preferring, moderate-outdoor and indoor-preferring free-range laying hens","volume":"185","author":"Campbell","year":"2016","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-6","doi-asserted-by":"publisher","first-page":"26","DOI":"10.3390\/ani8020026","article-title":"Spatial cognition and range use in free-range laying hens","volume":"8","author":"Campbell","year":"2018","journal-title":"Animals"},{"key":"10.7717\/peerj.8122\/ref-7","doi-asserted-by":"publisher","first-page":"e7303","DOI":"10.7717\/peerj.7303","article-title":"An attention bias test to assess anxiety states in laying hens","volume":"7","author":"Campbell","year":"2019","journal-title":"PeerJ"},{"issue":"5","key":"10.7717\/peerj.8122\/ref-8","doi-asserted-by":"publisher","first-page":"28","DOI":"10.3390\/ani6050028","article-title":"Ranging behaviour of commercial free-range laying hens","volume":"6","author":"Chielo","year":"2016","journal-title":"Animals"},{"key":"10.7717\/peerj.8122\/ref-9","doi-asserted-by":"publisher","first-page":"136","DOI":"10.3390\/ani8080136","article-title":"Affect-driven attention biases as animal welfare indicators: review and methods","volume":"8","author":"Crump","year":"2018","journal-title":"Animals"},{"issue":"6","key":"10.7717\/peerj.8122\/ref-10","doi-asserted-by":"publisher","first-page":"e90577","DOI":"10.1371\/journal.pone.0090577","article-title":"Parents and early life environment affect behavioral development of laying hen chickens","volume":"9","author":"De\u00a0Haas","year":"2014","journal-title":"PLOS ONE"},{"key":"10.7717\/peerj.8122\/ref-11","doi-asserted-by":"publisher","first-page":"2259","DOI":"10.3382\/ps.2012-02996","article-title":"Fear, stress, and feather pecking in commercial white and brown laying hen parent-stock flocks and their relationships with production parameters","volume":"92","author":"De\u00a0Haas","year":"2013","journal-title":"Poultry Science"},{"key":"10.7717\/peerj.8122\/ref-12","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1016\/j.physbeh.2012.08.002","article-title":"The relation between fearfulness in young and stress-response in adult laying hens, on individual and group level","volume":"107","author":"De\u00a0Haas","year":"2012","journal-title":"Physiology & Behavior"},{"key":"10.7717\/peerj.8122\/ref-13","doi-asserted-by":"publisher","first-page":"113","DOI":"10.3389\/fvets.2017.00113","article-title":"Learning and judgment can be affected by predisposed fearfulness in laying hens","volume":"4","author":"De\u00a0Haas","year":"2017","journal-title":"Frontiers in Veterinary Science"},{"key":"10.7717\/peerj.8122\/ref-14","doi-asserted-by":"publisher","first-page":"1336","DOI":"10.1071\/AN17757","article-title":"Determination of range enrichment for improved hen welfare on commercial fixed-range free-range layer farms","volume":"59","author":"De Koning","year":"2018","journal-title":"Animal Production Science"},{"key":"10.7717\/peerj.8122\/ref-15","doi-asserted-by":"publisher","first-page":"483","DOI":"10.20506\/rst.24.2.1587","article-title":"Science-based assessment of animal welfare: farm animals","volume":"24","author":"Duncan","year":"2005","journal-title":"Revue scientifique et technique (International Office of Epizootics)"},{"issue":"7","key":"10.7717\/peerj.8122\/ref-16","doi-asserted-by":"publisher","first-page":"e103535","DOI":"10.1371\/journal.pone.0103535","article-title":"Personality predicts social dominance in male domestic fowl","volume":"9","author":"Favati","year":"2014","journal-title":"PLOS ONE"},{"key":"10.7717\/peerj.8122\/ref-17","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1016\/j.physbeh.2007.03.016","article-title":"A critical review of fear tests used on cattle, pigs, sheep, poultry and horses","volume":"92","author":"Forkman","year":"2007","journal-title":"Physiology & Behavior"},{"key":"10.7717\/peerj.8122\/ref-18","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1080\/00071660600610534","article-title":"Corticosterone and fear behaviour in white and brown caged laying hens","volume":"47","author":"Fraise","year":"2006","journal-title":"British Poultry Science"},{"key":"10.7717\/peerj.8122\/ref-19","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1016\/S0003-3472(80)80045-5","article-title":"An ethological analysis of open-field behaviour in chickens","volume":"28","author":"Gallup Jr","year":"1980","journal-title":"Animal Behaviour"},{"key":"10.7717\/peerj.8122\/ref-20","doi-asserted-by":"publisher","first-page":"79","DOI":"10.3758\/BF03336016","article-title":"Tonic immobility as a reaction to predation: artificial eyes as a fear stimulus for chickens","volume":"23","author":"Gallup Jr","year":"1971","journal-title":"Psychonomic Science"},{"key":"10.7717\/peerj.8122\/ref-21","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.applanim.2007.10.004","article-title":"Reaction of laying hens to humans in the home or a novel environment","volume":"113","author":"Graml","year":"2008","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-22","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1017\/S1751731115002463","article-title":"Relationships between range access as monitored by radio-frequency identification technology, fearfulness, and plumage damage in free-range laying hens","volume":"10","author":"Hartcher","year":"2016","journal-title":"Animal"},{"key":"10.7717\/peerj.8122\/ref-23","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/j.applanim.2014.12.002","article-title":"Acute stress enhances sensitivity to a highly attractive food reward without affecting judgement bias in laying hens","volume":"163","author":"Hernandez","year":"2015","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-24","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1079\/WPS19860008","article-title":"The tonic immobility reaction of the domestic fowl: a review","volume":"42","author":"Jones","year":"1986","journal-title":"World\u2019s Poultry Science Journal"},{"key":"10.7717\/peerj.8122\/ref-25","article-title":"Energy efficiency of commercial free-range laying hens of different body weight and ranging activity. 173, Proc. 22nd ESPN, June 10-13","author":"Kolakshyapati","year":"2019"},{"key":"10.7717\/peerj.8122\/ref-26","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1016\/j.applanim.2006.02.005","article-title":"The effects of short term enrichment on learning in chickens from a laying strain (Gallus gallus domesticus)","volume":"101","author":"Krause","year":"2006","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-27","doi-asserted-by":"publisher","first-page":"2356","DOI":"10.1017\/S1751731118000022","article-title":"Relationship between welfare and individual ranging behaviour in commercial free-range laying hens","volume":"12","author":"Larsen","year":"2018","journal-title":"Animal"},{"key":"10.7717\/peerj.8122\/ref-28","article-title":"LAYWEL \u2013Welfare implications of changes in production systems for laying hens (Deliverables D.3.1-D.3.3, WP3- Health)","author":"LayWel","year":"2006"},{"key":"10.7717\/peerj.8122\/ref-29","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1016\/j.applanim.2017.11.003","article-title":"Anxiety influences attention bias but not flight speed and crush score in beef cattle","volume":"205","author":"Lee","year":"2018"},{"issue":"6","key":"10.7717\/peerj.8122\/ref-30","doi-asserted-by":"publisher","first-page":"20150977","DOI":"10.1098\/rsbl.2015.0977","article-title":"Attention bias to threat indicates anxiety differences in sheep","volume":"12","author":"Lee","year":"2016","journal-title":"Biology Letters"},{"key":"10.7717\/peerj.8122\/ref-31","doi-asserted-by":"publisher","first-page":"738","DOI":"10.1080\/00071660400014267","article-title":"Outdoor use, tonic immobility, heterophil\/lymphocyte ratio and feather condition in free-range laying hens of different genotype","volume":"45","author":"Mahboub","year":"2004","journal-title":"British Poultry Science"},{"key":"10.7717\/peerj.8122\/ref-32","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.applanim.2009.02.023","article-title":"Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms","volume":"118","author":"Mendl","year":"2009","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-33","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1016\/j.anbehav.2005.08.018M","article-title":"Is fearfulness a trait that can be measured with behavioural tests? A validation of four fear tests for Japanese quail","volume":"71","author":"Miller","year":"2006","journal-title":"Animal Behaviour"},{"key":"10.7717\/peerj.8122\/ref-34","doi-asserted-by":"publisher","first-page":"246","DOI":"10.3389\/fnbeh.2018.00246","article-title":"Attention bias test differentiates anxiety and depression in sheep","volume":"12","author":"Monk","year":"2018","journal-title":"Frontiers in Behavioral Neuroscience"},{"key":"10.7717\/peerj.8122\/ref-35","doi-asserted-by":"publisher","first-page":"11446","DOI":"10.1038\/s41598-019-47691-7","article-title":"Pharmacologically-induced stress has minimal impact on judgement and attention biases in sheep","volume":"9","author":"Monk","year":"2019","journal-title":"Scientific Reports"},{"issue":"1","key":"10.7717\/peerj.8122\/ref-36","doi-asserted-by":"publisher","first-page":"e019040","DOI":"10.1371\/journal.pone.0190404","article-title":"Towards a more practical attention bias test to assess affective state in sheep","volume":"13","author":"Monk","year":"2018","journal-title":"PLOS ONE"},{"key":"10.7717\/peerj.8122\/ref-37","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1016\/S0003-3472(05)80485-3","article-title":"Exploratory activity as a measure of motivation in deprived hens","volume":"41","author":"Nicol","year":"1991","journal-title":"Animal Behaviour"},{"key":"10.7717\/peerj.8122\/ref-38","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.applanim.2011.02.008","article-title":"Laying hens selected for low mortality: behaviour in tests of fearfulness, anxiety and cognition","volume":"131","author":"Nordquist","year":"2011","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-39","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.applanim.2005.03.003","article-title":"Effect of sex composition on fear measured as tonic immobility and vigilance behaviour in large flocks of laying hens","volume":"95","author":"Od\u00e9n","year":"2005","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-40","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.tvjl.2006.12.013","article-title":"Pathological anxiety in animals","volume":"175","author":"Ohl","year":"2008","journal-title":"Veterinary Journal"},{"key":"10.7717\/peerj.8122\/ref-41","volume-title":"Model code of practice for the welfare of animals\u2014domestic poultry","author":"Primary Industries Standing Committee","year":"2002","edition":"4"},{"key":"10.7717\/peerj.8122\/ref-42","doi-asserted-by":"publisher","first-page":"2503","DOI":"10.3382\/ps\/pew238","article-title":"Use of space and its impact on the welfare of laying hens in a commercial free-range system","volume":"95","author":"Rodriguez-Aurrekoetxea","year":"2016","journal-title":"Poultry Science"},{"key":"10.7717\/peerj.8122\/ref-43","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.brainres.2010.12.007","article-title":"Cognitive bias in the chick anxiety-depression model","volume":"1373","author":"Salmeto","year":"2011","journal-title":"Brain Research"},{"key":"10.7717\/peerj.8122\/ref-44","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0168-1591(01)00156-3","article-title":"Domestication effects on foraging strategy, social behaviour and different fear responses: a comparison between the red junglefowl (Gallus gallus) and a modern layer strain","volume":"74","author":"Sch\u00fctz","year":"2001","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-45","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1002\/da.20914","article-title":"Attention biases. Anxiety, and development: toward or away from threats or rewards?","volume":"29","author":"Shechner","year":"2012","journal-title":"Depression & Anxiety"},{"key":"10.7717\/peerj.8122\/ref-46","doi-asserted-by":"crossref","first-page":"231","DOI":"10.31887\/DCNS.2002.4.3\/tsteimer","article-title":"The biology of fear- and anxiety-related behaviors","volume":"4","author":"Steimer","year":"2002","journal-title":"Dialogues in Clinical Neuroscience"},{"key":"10.7717\/peerj.8122\/ref-47","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1016\/j.applanim.2007.03.008","article-title":"The novel object test as predictor of feather damage in cage-housed Rhode Island Red and White Leghorn laying hens","volume":"109","author":"Uitdehaag","year":"2008","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-48","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1111\/j.1439-0310.1988.tb00243.x","article-title":"Chicks in a novel environment: effects of conspecific calls","volume":"78","author":"Vallortigara","year":"1988","journal-title":"Ethology"},{"key":"10.7717\/peerj.8122\/ref-49","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.applanim.2018.05.027","article-title":"Feather pecking genotype and phenotype affect behavioural responses of laying hens","volume":"205","author":"Van\u00a0der Eijk","year":"2018","journal-title":"Applied Animal Behaviour Science"},{"issue":"1","key":"10.7717\/peerj.8122\/ref-50","doi-asserted-by":"publisher","first-page":"e021136","DOI":"10.1371\/journal.pone.0211363","article-title":"Chronic stress influences attentional and judgement bias and the activity of the HPA axis in sheep","volume":"14","author":"Verbeek","year":"2019","journal-title":"PLOS ONE"},{"key":"10.7717\/peerj.8122\/ref-51","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.applanim.2007.12.003","article-title":"A note on fear reaction of three different genetic strains of laying hens to a simulated hawk attack in the hen run of a free-range system","volume":"113","author":"Zeltner","year":"2008","journal-title":"Applied Animal Behaviour Science"},{"key":"10.7717\/peerj.8122\/ref-52","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1016\/j.anbehav.2012.06.006","article-title":"Scent of the enemy: behavioural responses to predator faecal odour in the fowl","volume":"84","author":"Zidar","year":"2012","journal-title":"Animal Behaviour"}],"container-title":["PeerJ"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/peerj.com\/articles\/8122.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/8122.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/8122.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/8122.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,5]],"date-time":"2021-02-05T20:03:53Z","timestamp":1612555433000},"score":1,"resource":{"primary":{"URL":"https:\/\/peerj.com\/articles\/8122"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,25]]},"references-count":52,"alternative-id":["10.7717\/peerj.8122"],"URL":"https:\/\/doi.org\/10.7717\/peerj.8122","archive":["CLOCKSS","LOCKSS","Portico"],"relation":{"has-review":[{"id-type":"doi","id":"10.7287\/peerj.8122v0.1\/reviews\/1","asserted-by":"object"},{"id-type":"doi","id":"10.7287\/peerj.8122v0.1\/reviews\/2","asserted-by":"object"}]},"ISSN":["2167-8359"],"issn-type":[{"value":"2167-8359","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,25]]},"article-number":"e8122"}}