{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T01:14:28Z","timestamp":1793236468474,"version":"4.5.0"},"reference-count":35,"publisher":"Wiley","issue":"1","license":[{"start":{"date-parts":[[2018,1,7]],"date-time":"2018-01-07T00:00:00Z","timestamp":1515283200000},"content-version":"vor","delay-in-days":6,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"name":"Cleveland Metroparks Zoo"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Zoo Biology"],"published-print":{"date-parts":[[2018,1]]},"abstract":"<jats:sec><jats:label\/><jats:p>Zoo\u2010housed bears are prone to exhibiting stereotypic behaviors, generally considered indicators of negative welfare. We explored the effects of a variable\u2010time feeding enrichment schedule on behavioral indicators of welfare in four bear species at Cleveland Metroparks Zoo. We distributed the diets of eight bears in one of five enrichment items, for two consecutive days each, and monitored behavior throughout the day. In Experiment 1, we compared variable\u2010time to fixed\u2010time presentation of enrichment over two, 10\u2010day periods. Overall, bears performed more exploratory behavior when enriched (<jats:italic>p\u2009<\/jats:italic>&lt;\u20090.0001). Furthermore, variable\u2010time enrichment was associated with a greater increase in exploratory behavior than fixed\u2010time enrichment when compared to baseline (<jats:italic>p\u2009<\/jats:italic>&lt;\u20090.001). Both fixed\u2010time (<jats:italic>p<\/jats:italic><jats:sub>unadjusted<\/jats:sub> &lt;0.05, <jats:italic>p<\/jats:italic><jats:sub>adjusted<\/jats:sub> =\u20090.07) and variable\u2010schedule (<jats:italic>p<\/jats:italic><jats:sub>unadjusted<\/jats:sub> &lt;0.05, <jats:italic>p<\/jats:italic><jats:sub>adjusted<\/jats:sub> =\u20090.09) enrichment were also associated with similar decreases in abnormal behavior compared to baseline. For Experiment 2, we tested habituation to enrichment over 30 days using multiple items and a semi\u2010variable presentation schedule. Again during the enrichment period, bears exhibited increased exploratory behavior (<jats:italic>p\u2009<\/jats:italic>&lt;\u20090.0001) and decreased abnormal behaviors compared to baseline (<jats:italic>p<\/jats:italic><jats:sub>unadjusted<\/jats:sub> =\u20090.05, <jats:italic>p<\/jats:italic><jats:sub>adjusted<\/jats:sub> =\u20090.09). We observed no habituation during the 30\u2010day sustained enrichment period for these behaviors. Collectively, these results suggest that daily, variable\u2010schedule feeding enrichment, with intermittent presentation of unique enrichment items, increases behavioral indicators of positive welfare and decreases behavioral indicators of negative welfare.<\/jats:p><\/jats:sec>","DOI":"10.1002\/zoo.21391","type":"journal-article","created":{"date-parts":[[2018,1,10]],"date-time":"2018-01-10T04:52:30Z","timestamp":1515559950000},"page":"3-15","source":"Crossref","is-referenced-by-count":29,"title":["A work\u2010for\u2010food enrichment program increases exploration and decreases stereotypies in four species of bears"],"prefix":"10.1002","volume":"37","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8973-0808","authenticated-orcid":false,"given":"Jason D.","family":"Wagman","sequence":"first","affiliation":[{"name":"Conservation and Science Cleveland Metroparks Zoo Wildlife Way Cleveland Ohio"},{"name":"Department of Biology Case Western Reserve University Cleveland Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristen E.","family":"Lukas","sequence":"additional","affiliation":[{"name":"Conservation and Science Cleveland Metroparks Zoo Wildlife Way Cleveland Ohio"},{"name":"Department of Biology Case Western Reserve University Cleveland Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia M.","family":"Dennis","sequence":"additional","affiliation":[{"name":"Conservation and Science Cleveland Metroparks Zoo Wildlife Way Cleveland Ohio"},{"name":"Department of Biology Case Western Reserve University Cleveland Ohio"},{"name":"Department of Veterinary Preventive Medicine Ohio State University Columbus Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark A.","family":"Willis","sequence":"additional","affiliation":[{"name":"Department of Biology Case Western Reserve University Cleveland Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joe","family":"Carroscia","sequence":"additional","affiliation":[{"name":"Animal Care Cleveland Metroparks Zoo Wildlife Way Cleveland Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Curt","family":"Gindlesperger","sequence":"additional","affiliation":[{"name":"Animal Care Cleveland Metroparks Zoo Wildlife Way Cleveland Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8248-0022","authenticated-orcid":false,"given":"Mandi W.","family":"Schook","sequence":"additional","affiliation":[{"name":"Conservation and Science Cleveland Metroparks Zoo Wildlife Way Cleveland Ohio"},{"name":"Department of Biology Case Western Reserve University Cleveland Ohio"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2018,1,7]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.1163\/156853974X00534"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20301"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.10065"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2006.05.029"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/0376-6357(91)90017-T"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.1430100103"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2015.04.002"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/425473a"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2006.05.033"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20138"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2288-2-8"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-2361(1999)18:5<363::AID-ZOO1>3.0.CO;2-H"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20253"},{"key":"e_1_2_8_15_1","first-page":"53","volume-title":"Giant pandas: Biology and conservation","author":"Garshelis D.","year":"2004"},{"key":"e_1_2_8_16_1","first-page":"199","article-title":"Stimulating natural behaviour in captive bears","volume":"12","author":"Grandia P. A.","year":"2001","journal-title":"Ursus"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0003-3472(05)80094-6"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20276"},{"key":"e_1_2_8_19_1","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1017\/S0962728600019618","article-title":"Effect of wood\u2010pile feeders on the behaviour of captive bush dogs (Speothos venaticus)","volume":"6","author":"Ings R.","year":"1997","journal-title":"Animal Welfare"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2008.09.004"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.10076"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2006.05.041"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20282"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2006.05.031"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.beproc.2004.02.008"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2004.10.015"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.applanim.2012.09.007"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0091-3057(02)00786-4"},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.21112"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20091"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2907.2007.00096.x"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20066"},{"key":"e_1_2_8_33_1","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1079\/9780851990040.0256","volume-title":"Stereotypic animal behaviour: Fundamentals and applications to welfare. 2nd ed","author":"Swaisgood R. R.","year":"2006"},{"key":"e_1_2_8_34_1","unstructured":"USDA (United States Department of Agriculture). (2013. Animal Welfare Act and Regulations [Blue Book]. United States Department of Agriculture."},{"key":"e_1_2_8_35_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.20027"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.1002\/zoo.21144"}],"container-title":["Zoo Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fzoo.21391","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/zoo.21391","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,26]],"date-time":"2023-09-26T05:21:24Z","timestamp":1695705684000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/zoo.21391"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,1]]},"references-count":35,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2018,1]]}},"alternative-id":["10.1002\/zoo.21391"],"URL":"https:\/\/doi.org\/10.1002\/zoo.21391","archive":["Portico"],"relation":{},"ISSN":["0733-3188","1098-2361"],"issn-type":[{"value":"0733-3188","type":"print"},{"value":"1098-2361","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,1]]}}}