{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T16:19:51Z","timestamp":1789661991394,"version":"4.0.1"},"reference-count":35,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2021,6,8]],"date-time":"2021-06-08T00:00:00Z","timestamp":1623110400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["RGPIN-2016-04620"],"award-info":[{"award-number":["RGPIN-2016-04620"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Rats (<jats:italic>Rattus norvegicus<\/jats:italic>) bred for research are typically confined with their litters until weaning, but will spend time away from pups when given the opportunity. We aimed to assess how dam welfare is affected by the ability to escape from their pups. Rat dams (n = 16) were housed in cages either with or without an elevated loft. We measured time dams spent in lofts, time spent nursing, and affective states using elevated plus maze and anticipatory behavior testing. We predicted that 1) dams housed with lofts would use them increasingly as pups aged, 2) dams without a loft would spend more time passively nursing (i.e. initiated by pups rather than the dam) and more total time nursing as pups aged, and 3) dams housed with lofts would show evidence of a more positive affective state. Dams housed with lofts spent more time in the loft with increasing pup age; dams spent on average (mean \u00b1 SE) 27 \u00b1 5% of their time in the loft when pups were 1 wk old, increasing to 52 \u00b1 5% of their time at 3 wks. When pups were 3 wks old, dams with lofts spent less time passively nursing (10 \u00b1 2% of total time, compared to 27 \u00b1 4% for dams without a loft) and less time nursing overall (36 \u00b1 4% of time versus 59 \u00b1 2% for dams without a loft). Rats without loft access showed increased anticipatory behavior potentially indicative of negative affective state (24.5\u00b11.8 behaviors per minute in wk 3 compared to 18.8\u00b11.0 in wk 1). These findings indicate that rat dams in laboratories choose to spend time away from their pups when provided the opportunity, particularly later in lactation; an inability to do so is associated with increased passive nursing and negative affect.<\/jats:p>","DOI":"10.1371\/journal.pone.0253020","type":"journal-article","created":{"date-parts":[[2021,6,8]],"date-time":"2021-06-08T18:22:26Z","timestamp":1623176546000},"page":"e0253020","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":10,"title":["A break from the pups: The effects of loft access on the welfare of lactating laboratory rats"],"prefix":"10.1371","volume":"16","author":[{"given":"Anna S.","family":"Ratuski","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0917-3982","authenticated-orcid":true,"given":"Daniel M.","family":"Weary","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,6,8]]},"reference":[{"issue":"4","key":"pone.0253020.ref001","doi-asserted-by":"crossref","DOI":"10.1016\/S0003-3472(69)80019-9","article-title":"Continuous recording of maternal behaviour in Rattus norvegicus","volume":"17","author":"LJ Grota","year":"1969","journal-title":"Anim Behav"},{"key":"pone.0253020.ref002","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1079\/9781845936594.0027","volume-title":"Animal Welfare","author":"M \u0160pinka","year":"2011"},{"key":"pone.0253020.ref003","article-title":"Animal agency, animal awareness and animal welfare.","author":"M \u0160pinka","year":"2019","journal-title":"Anim Welf"},{"issue":"4","key":"pone.0253020.ref004","first-page":"279","article-title":"Alternative housing for sows and litters. 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Friard","year":"2016","journal-title":"Methods Ecol Evol"},{"issue":"2","key":"pone.0253020.ref025","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.pbb.2010.08.014","article-title":"Absence of repeated-trial tolerance to the anxiolytic-like effects of chlordiazepoxide in the rat triple test","volume":"97","author":"TD Wehrmeister","year":"2010","journal-title":"Pharmacol Biochem Behav"},{"issue":"11","key":"pone.0253020.ref026","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0207804","article-title":"Repeated elevated plus maze trials as a measure for tracking within-subjects behavioral performance in rats (Rattus norvegicus)","volume":"13","author":"AJ Schrader","year":"2018","journal-title":"PLoS One"},{"issue":"1","key":"pone.0253020.ref027","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1177\/0023677214547404","article-title":"Effect of multilevel laboratory rat caging system on the well-being of the singly-housed sprague 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