The importance of burrowing, climbing and standing upright for laboratory rats
Open accessAbstract
Standard laboratory cages prevent rats (Rattus norvegicus) from performing many behaviours that they perform in the wild, but little is known about how this may affect their welfare. The aims of this study were (i) to record the propensity to burrow, climb and stand upright in 3-, 8- and 13-month old laboratory rats housed in semi-naturalistic environments and (ii) to compare the frequency of lateral stretching in semi-naturalistic versus standard-housed rats; we predicted standard-housed rats would perform more lateral stretches to compensate for the inability to stretch upright. Rats' propensity to burrow remained constant as they aged (approx. 30 bouts per day totalling 20–30 min), suggesting burrowing is important to rats. Climbing decreased from 76 to 7 bouts per day at 3 versus 13 months, probably because of declining physical ability. Upright standing decreased from 178 to 73 bouts per day, but continued to be frequently expressed even in older rats. Standard-housed rats stretched much more frequently than semi-naturalistic-housed rats (53 versus 6 bouts per day at 13 months), perhaps in compensation for inability to stretch upright and to relieve stiffness caused by low mobility associated with standard housing. These findings suggest that standard laboratory cages interfere with important natural behaviours, which is likely to compromise rat welfare.
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Previous Canadian Council on Animal Care guidelines mandated a minimum cage height that did not allow upright standing for most rats; current guidelines recommend a minimal height equivalent to the nose-to-tail-base distance plus 4 cm, which would allow upright standing.
“Previous guidelines from the Canadian Council on Animal Care (CCAC) mandated a minimum cage height that did not allow upright standing for most rats; however, the current guidelines recommend a minimal height equivalent to the nose-to-tail-base distance plus 4 cm, which would allow upright standing.16,28”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [28]
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Experimental — accuracy not yet measuredThe observed behavior of increased upright standing is consistent with another study that also observed an increase in upright standing in a permissive environment.
“The observed behavior is consistent with another study that also observed an increase in upright standing in a permissive environment.28”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [28]
The Results (Main study; page unavailable) report frequent upright standing in semi-naturalistic cages, and the Conclusion says standard cages prevented rats from standing upright. The paper does not report an increase in upright standing after a change to a permissive environment; it reports that standing declined as the rats aged. (LLM, conf=0.82)
Experimental — accuracy not yet measuredRats that have the opportunity will stand upright; when unable to do so, they will stretch laterally more frequently, suggesting that the ability to extend the body is important.
“Consistent with the implied benefit of increased vertical space, rats that have the opportunity will stand upright; when unable to do so, they will stretch laterally more frequently, suggesting that the ability to extend the body is important.”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [28]
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Cites
Higgins, E. T. (1997) · American Psychologist · doi:10.1037/0003-066x.52.12.1280 · Cited by 6,775 · see citing works
The ecology and sociology of the Norway rat
Calhoun, J. B. (1963) · doi:10.5962/bhl.title.112283 · Cited by 1,040 · cited 2× · see citing works
“In the wild, rats construct and live inside burrows that they expand and modify frequently [15,16].”
Background“Control” laboratory rodents are metabolically morbid: Why it matters
Martin, B., Ji, S., Maudsley, S., & Mattson, M. P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912955107 · Cited by 354 · see citing works
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- [1]Richter CP 1959 Rats, man, and the welfare state. Am. Psychol. 14, 18– 28. (doi:10.1037/h0043834) · DOI
- [3]Lindsey JR 1979 Historical foundations. In The laboratory rat (eds Baker HJ, Lindsey JR, Weisbroth SH), pp. 1– 36. New York, NY: Academic Press Inc.
- [7]NRC. 2011 Guide for the care and use of laboratory animals, 8th edn Washington, DC: The National Academies Press. 21595115
- [8]CCAC. 1993 Housing and environment. In Guide to the care and use of experimental animals, vol. 1 (eds Offert ED, Cross BM, McWilliam AA).
- [9]Büttner D 1993 Upright standing in the laboratory rat—time expenditure and its relation to locomotor activity. J. Exp. Anim. Sci. 36, 19– 26. (doi:10.1038/2091178c0) 8312384 · DOI
- [10]Pullen AH 1976 A parametric analysis of the growing CFHB (Wistar) rat. J. Anat. 121, 371– 383. 931783 PMC1231806
- [11]Benard M, de Cock Buning T 2013 Exploring the potential of Dutch pig farmers and urban-citizens to learn through frame reflection. J. Agric. Environ. Ethics 26, 1015– 1036. (doi:10.1007/s10806-013-9438-y) · DOI
- [12]Boogaard BK, Boekhorst LJS, Oosting SJ, Sørensen JT 2011 Socio-cultural sustainability of pig production: citizen perceptions in the Netherlands and Denmark. Livest. Sci. 140, 189– 200. (doi:10.1016/j.livsci.2011.03.028) · DOI
- [13]Vanhonacker F, Verbeke W, Van Poucke E, Tuyttens FAM 2008 Do citizens and farmers interpret the concept of farm animal welfare differently? Livest. Sci. 116, 126– 136. (doi:10.1016/j.livsci.2007.09.017) · DOI · Paper page
- [16]Pisano RG, Storer TI 1948 Burrows and feeding of the Norway rat. J. Mammal. 29, 374– 383. (doi:10.2307/1375126) · DOI
- [17]Barnett SA 1975 The rat: a study in behavior, revised edn Chicago, IL: The University of Chicago Press.
- [18]Huck UW, Price EO 1976 Effect of the post-weaning environment on the climbing behaviour of wild and domestic Norway rats. Anim. Behav. 24, 364– 371. (doi:10.1016/S0003-3472(76)80044-9) 937767 · DOI
- [19]Hill DA, Robertson HA, Sutherland WJ 1983 Brown rats (Rattus norvegicus) climbing to obtain sloes and blackberries. J. Zool. 200, 302 (doi:10.1111/j.1469-7998.1983.tb05796.x) · DOI
- [20]Grant EC, Mackintosh JH 1963 A comparison of the social postures of some common laboratory rodents. Behaviour 21, 246– 259. (doi:10.1163/156853963X00185) · DOI
- [21]Boice R 1977 Burrows of wild and albino rats: effects of domestication, outdoor raising, age, experience, and maternal state. J. Comp. Physiol. Psychol. 91, 649– 661. (doi:10.1037/h0077338) 559696 · DOI
- [22]Peplow M 2004 Lab rats go wild in Oxfordshire. Nat. News (doi:10.1038/news040202-2) · DOI
- [23]Modlińska K, Stryjek R, Pisula W 2015 Food neophobia in wild and laboratory rats (multi-strain comparison). Behav. Processes 113, 41– 50. (doi:10.1016/j.beproc.2014.12.005) 25572457 · DOI
- [24]Timberlake W, Silva KM 1995 Appetitive behavior in ethology, psychology, and behavior systems. In Perspectives in ethology. 11. Behavioral design (ed. Thompson NS), pp. 211– 255. New York, NY: Plenum Press.
- [25]Price EO 1999 Behavioral development in animals undergoing domestication. Appl. Anim. Behav. Sci. 65, 245– 271. (doi:10.1016/S0168-1591(99)00087-8) · DOI
- [26]Stryjek R, Modlińska K, Pisula W 2012 Species specific behavioural patterns (digging and swimming) and reaction to novel objects in wild type, Wistar, Sprague-Dawley and Brown Norway rats. PLoS ONE 7, e40642 (doi:10.1371/journal.pone.0040642) 22815778 PMC3398036 · DOI
- [27]Price EO 1977 Burrowing in wild and domestic Norway rats. J. Mammal. 58, 239– 240. (doi:10.2307/1379585) · DOI
- [28]Casadesus G, Shukitt-Hale B, Joseph JA 2001 Automated measurement of age-related changes in the locomotor response to environmental novelty and home-cage activity. Mech. Ageing Dev. 122, 1887– 1897. (doi:10.1016/S0047-6374(01)00324-4) 11557287 · DOI
- [29]Martin JR, Fuchs A, Bender R, Harting J 1986 Altered light/dark activity difference with aging in two rat strains. J. Gerontol. 41, 2– 7. (doi:10.1093/geronj/41.1.2) 3941251 · DOI
- [30]Spangler EL, Waggie KS, Hengemihle J, Roberts D, Hess B, Ingram DK 1994 Behavioral assessment of aging in male Fischer 344 and brown Norway rat strains and their F1 hybrid. Neurobiol. Aging 15, 319– 328. (doi:10.1016/0197-4580(94)90027-2) 7936056 · DOI
- [31]Soffié M, Buhot MC, Poucet B 1992 Cognitive and noncognitive processes involved in selective object exploration: comparison between young adult and old rats. Physiol. Behav. 52, 1029– 1035. (doi:10.1016/0031-9384(92)90387-H) 1484835 · DOI
- [32]Goettl VM, Wemlinger TA, Colvin AE, Neff NH, Hadjiconstantinou M 2001 Motoric behavior in aged rats treated with GM1. Brain Res. 906, 92– 100. (doi:10.1016/S0006-8993(01)02559-8) 11430865 · DOI
- [33]Dawkins MS 1988 Behavioural deprivation: a central problem in animal welfare. Appl. Anim. Behav. Sci. 20, 209– 225. (doi:10.1016/0168-1591(88)90047-0) · DOI · Paper page
- [35]Dawkins MS 1983 Battery hens name their price: consumer demand theory and the measurement of ethological ‘needs’. Anim. Behav. 31, 1195– 1205. (doi:10.1016/S0003-3472(83)80026-8) · DOI
- [36]Galef BG, Durlach P 1993 Should large rats be housed in large cages? An empirical issue. Can. Psychol. 34, 203– 207. (doi:10.1037/h0078763) · DOI
- [39]Slonaker JR 1907 The normal activity of the white rat at different ages. J. Comp. Neurol. Psychol. 17, 342– 359. (doi:10.1002/cne.920170404) · DOI
- [40]Adams N, Boice R 1983 A longitudinal study of dominance in an outdoor colony of domestic rats. J. Comp. Psychol. 97, 24– 33. (doi:10.1037/0735-7036.97.1.24) · DOI · Paper page
- [41]Baenninger R 1997 On yawning and its functions. Psychon. Bull. Rev. 4, 198– 207. (doi:10.3758/BF03209394) 21331826 · DOI
- [42]Fraser AF 1989 Pandiculation: the comparative phenomenon of systematic stretching. Appl. Anim. Behav. Sci. 23, 263– 268. (doi:10.1016/0168-1591(89)90117-2) · DOI
- [43]Altmann J 1974 Observational study of behavior: sampling methods. Behaviour 49, 227– 267. (doi:10.1163/156853974X00534) 4597405 · DOI · Paper page
- [44]Patterson-Kane EG 2003 Shelter enrichment for rats. Contemp. Top. Lab. Anim. Sci. 42, 46– 48. 19757626
- [45]Blanchard RJ, Blanchard DC 1990 Anti-predator defense as models of animal fear and anxiety. In Fear and defense (eds Brain PF, Parmigiani RJ, Blanchard DC, Mainardi D), pp. 89– 108. London, UK: Harwood Academic Publishers.
- [46]Schlingmann F, Pereboom WJ, Remie R 1993 The sensitivity of albino and pigmented rats to light: a mini review. Anim. Technol. 44, 71– 85.
- [48]Poole S, Stephenson JD 1977 Body temperature regulation and thermoneutrality. Q. J. Exp. Physiol. 62, 143– 149. (doi:10.1113/expphysiol.1977.sp002384) 585477 · DOI
- [49]Wiedenmayer C 1997 Causation of the ontogenetic development of stereotypic digging in gerbils. Anim. Behav. 53, 461– 470. (doi:10.1006/anbe.1996.0296) · DOI
- [50]Chmiel DJJ, Noonan M 1996 Preference of laboratory rats for potentially enriching stimulus objects. Lab. Anim. 30, 97– 101. (doi:10.1258/002367796780865790) 8783168 · DOI
- [51]Bradshaw AL, Poling A 1991 Choice by rats for enriched versus standard home cages: plastic pipes, wood platforms, wood chips, and paper towels as enrichment items. J. Exp. Anal. Behav. 55, 245– 250. (doi:10.1901/jeab.1991.55-245) 16812635 PMC1323058 · DOI
- [52]Sherwin CM, Haug E, Terkelsen N, Vadgama M 2004 Studies on the motivation for burrowing by laboratory mice. Appl. Anim. Behav. Sci. 88, 343– 358. (doi:10.1016/j.applanim.2004.03.009) · DOI
- [53]Strauman TJ, Socolar Y, Kwapil L, Cornwell JFM, Franks B, Sehnert S, Higgins ET 2015 Microinterventions targeting regulatory focus and regulatory fit selectively reduce dysphoric and anxious mood. Behav. Res. Ther. 72, 18– 29. (doi:10.1016/j.brat.2015.06.003) 26163353 PMC4529777 · DOI
- [55]Higgins ET, Shah J, Friedman R 1997 Emotional responses to goal attainment: strength of regulatory focus as moderator. J. Pers. Soc. Psychol. 72, 515– 525. (doi:10.1037/0022-3514.72.3.515) 9120782 · DOI · Paper page
- [56]Franks B, Higgins ET, Champagne FA 2014 A theoretically based model of rat personality with implications for welfare. PLoS ONE 9, e95135 (doi:10.1371/journal.pone.0095135) 24755737 PMC3995697 · DOI
- [57]Franks B, Higgins ET, Champagne FA 2012 Evidence for individual differences in regulatory focus in rats, Rattus norvegicus. J. Comp. Psychol. 126, 347– 354. (doi:10.1037/a0027244) 22390620 PMC3386359 · DOI
- [58]Franks B, Reiss D, Cole P, Friedrich V, Thompson N, Higgins ET 2013 Predicting how individuals approach enrichment: regulatory focus in cotton-top tamarins (Sanguinus oedipus). Zoo Biol. 32, 427– 435. (doi:10.1002/zoo.21075) 23649664 · DOI
- [59]Willig F, Palacios A, Monmaur P, M'Harzi M, Laurent J, Delacour J 1987 Short-term memory, exploration and locomotor activity in aged rats. Neurobiol. Aging 8, 393– 402. (doi:10.1016/0197-4580(87)90033-9) 3683720 · DOI
- [60]Goodrick CL 1971 Variables affecting free exploration responses of male and female Wistar rats as a function of age. Dev. Psychol. 4, 440– 446. (doi:10.1037/h0030942) · DOI
- [61]Wallace JE, Krauter EE, Campbell BA 1980 Motor and reflexive behavior in the aging rat. J. Gerontol. 35, 364– 370. (doi:10.1093/geronj/35.3.364) 7410787 · DOI
- [62]Fraser AF 1988 Behavioural needs in relation to livestock maintenance. Appl. Anim. Behav. Sci. 19, 368– 376. (doi:10.1016/0168-1591(88)90021-4) · DOI
- [63]Bertolucci LF 2011 Pandiculation: nature's way of maintaining the functional integrity of the myofascial system? J. Bodywork Mov. Ther. 15, 268– 280. (doi:10.1016/j.jbmt.2010.12.006) 21665102 · DOI
- [65]Makowska IJ, Weary DM 2016 Differences in anticipatory behaviour between rats (Rattus norvegicus) housed in standard versus semi-naturalistic laboratory environments. PLoS ONE 11, e0147595 (doi:10.6084/m9.figshare.2061945) 26820978 PMC4731070 · DOI
- [67]Watters JV 2014 Searching for behavioral indicators of welfare in zoos: uncovering anticipatory behavior. Zoo Biol. 33, 251– 256. (doi:10.1002/zoo.21144) 25042907 · DOI
- [68]Spruijt BM, Van den Bos R, Pijlman FTA 2001 A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Appl. Anim. Behav. Sci. 72, 145– 171. (doi:10.1016/S0168-1591(00)00204-5) 11278033 · DOI · Paper page
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Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats
Bigelow, L. J., Cohen, A. J., Pimm, R., Knight, J. B., & Bernard, P. B. (2022) · Journal of the American Association for Laboratory Animal Science · doi:10.30802/aalas-jaalas-21-000024 · Cited by 9 · see citing works
- Authors
- Makowska, I. J., & Weary, D. M.
- Affiliations
- University of British Columbia (CA)
- Corresponding author
- Makowska, I. Joanna
- Venue
- Royal Society Open Science
- Publisher
- The Royal Society
- Published
- 2016-06
- Volume
- 3
- Issue
- 6
- Pages
- 160136
- ISSN
- 2054-5703 (ISSN-L)
- PMC
- PMC4929907
- OpenAlex
- W2471802517
- Cited by
- 71
- References
- 3
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 8 · 2023: 8 · 2022: 10 · 2021: 8 · 2020: 5 · 2019: 9 · 2018: 3 · 2017: 4
- FWCI
- 8.20
- Type
- journal article
- Language
- en
- Update notices
- correction (2017-01-01)
- Open access
- gold
- doi.org
- Locations
- Royal Society Open Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Natural Sciences and Engineering Research Council of Canada (F10-05562)
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Health Sciences › Veterinary › Small Animals › Animal testing and alternatives
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- burrowing behavior, climbing behavior, standing, cage enrichment
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