Cited by 37Animal Behavior and Welfare StudiesAnimal testing and alternativesVeterinary Pharmacology and Anesthesia

Evaluation of the effects of space allowance on measures of animal welfare in laboratory mice

Open access
Bailoo, Jeremy D., Murphy, Eimear, Varholick, Justin A., Novak, Janja, Palme, Rupert, Würbel, Hanno·2018·Scientific Reports

Abstract

We studied how space allowance affects measures of animal welfare in mice by systematically varying group size and cage type across three levels each in both males and females of two strains of mice (C57BL/6ByJ and BALB/cByJ; n = 216 cages, a total of 1152 mice). This allowed us to disentangle the effects of total floor area, group size, stocking density, and individual space allocation on a broad range of measures of welfare, including growth (food and water intake, body mass); stress physiology (glucocorticoid metabolites in faecal boli); emotionality (open field behaviour); brain function (recurrent perseveration in a two-choice guessing task); and home-cage behaviour (activity, stereotypic behaviour). While increasing group size was associated with a decrease in food and water intake in general, and more specifically with increased attrition due to escalated aggression in male BALB mice, no other consistent effects of any aspect of space allowance were found with respect to the measures studied here. Our results indicate that within the range of conditions commonly found in laboratory mouse housing, space allowance as such has little impact on measures of welfare, except for group size which may be a risk factor for escalating aggression in males of some strains.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-017-18493-6

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Cage/tank/housing system (type and dimensions) affects behaviour.

    “Cage/tank/housing system (type and dimensions) | Affects behaviour [177] and fear learning [178].”

    From Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0 (2020) · cites this paper as [177]

    The Discussion reports increased aggression with larger group sizes and floor areas in male BALB mice, so the paper supports an effect on that specific behaviour. It also says space allowance had little effect on the other behaviours studied; the Results sections report no differences in home-cage activity or open-field behaviour across cage conditions. The unqualified claim that housing type and dimensions affect behaviour overstates this limited finding. Fear learning is attributed to a different citation. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 44

  1. [1]Latham N Mason G From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory Appl. Anim. Behav. Sci. 2004 86 261 289 10.1016/j.applanim.2004.02.006 · DOI
  2. [2]Whittaker AL Howarth GS Hickman DL Effects of space allocation and housing density on measures of wellbeing in laboratory mice: a review Lab. Anim. 2012 46 3 13 10.1258/la.2011.011049 22114068 · DOI
  3. [3]Garber JC On the care and use of US lab animals Nature 2011 4763 152 10.1038/476152a 21833072 · DOI
  4. [4]Jennings M Refining rodent husbandry: the mouse. Report of the Rodent Refinement Working Party Lab. Anim. 1998 32 233 259 10.1258/002367798780559301 9718472 · DOI
  5. [5]Smith A Corrow D Modifications to husbandry and housing conditions of laboratory rodents for improved well-being ILAR J. 2005 46 140 147 10.1093/ilar.46.2.140 15775023 · DOI
  6. [6]Smith AL Mabus SL Stockwell JD Muir C Effects of Housing Density and Cage Floor Space on C57BL/6J Mice Comp. Med. 2004 54 656 663 15679264
  7. [7]Smith A Mabus SL Muir C Woo Y Effects of Housing Density and Cage Floor Space on Three Strains of Young Adult Inbred Mice Comp. Med. 2005 55 368 376 16158912
  8. [8]Anton AH Effect of Group Size, Sex and Time on Organ Weights, Catecholamines and Behavior in Mice Physiol. Behav. 1969 4 483 487 10.1016/0031-9384(69)90142-5 · DOI
  9. [9]Laber K Veatch LM Lopez MF Mulligan JK Lathers DMR Effects of housing density on weight gain, immune function, behavior, and plasma corticosterone concentrations in BALB/c and C57BL/6 mice J. Am. Assoc. Lab. Anim. Sci. 2008 47 16 23 18351717 PMC2653995
  10. [10]Van Loo PLP Mol JA Koolhaas JM Van Zutphen BFM Baumans V Modulation of aggression in male mice: Influence of group size and cage size Physiol. Behav. 2001 72 675 683 10.1016/S0031-9384(01)00425-5 11336999 · DOI · Paper page
  11. [11]Greenberg G The effects of ambient temperature and population density on aggression in two inbred strains of mice, Mus musculus Behaviour 1972 42 119 30 10.1163/156853972X00130 5065365 · DOI
  12. [12]Fullwood S Hicks TA Brown JC Norman RL Mcglone JJ Floor Space Needs for Laboratory Mice: C57BL / 6 Males in Solid-bottom Cages with Bedding ILAR J. 1998 39 29 36 10.1093/ilar.39.1.29 11406686 · DOI
  13. [13]Nicholson A The Response of C57BL/6J and BALB/cJ Mice to Increased Housing Density J. Am. Assoc. Lab. Anim. Sci. 2009 48 740 753 19930822 PMC2786928
  14. [14]Chvédoff M Clarke MR Irisarri E Faccini JM Monro AM Effects of housing conditions on food intake, body weight and spontaneous lesions in mice. A review of the literature and results of an 18-month study Food Cosmet. Toxicol. 1980 18 517 522 10.1016/0015-6264(80)90167-4 7203299 · DOI
  15. [15]Christian JJ Effect of population size on the adrenal glands and reproductive organs of male mice in populations of fixed size Am. J. Physiol. 1955 182 292 300 13258805
  16. [16]McGlone JJ Anderson DL Norman RL Floor space needs for laboratory mice: BALB/cJ males or females in solid-bottom cages with bedding Contemp. Top. Lab. Anim. Sci. 2001 40 21 5 11353520
  17. [21]Möstl E Palme R Hormones as indicators of stress. in Domestic Animal Endocrinology 2002 23 67 74 10.1016/S0739-7240(02)00146-7 12142227 · DOI · Paper page
  18. [22]Touma C Palme R Measuring Fecal Glucocorticoid Metabolites in Mammals and Birds: The Importance of Validation Ann. N. Y. Acad. Sci. 2005 1046 54 74 10.1196/annals.1343.006 16055843 · DOI · Paper page
  19. [24]Touma C Palme R Sachser N Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones Horm. Behav. 2004 45 10 22 10.1016/j.yhbeh.2003.07.002 14733887 · DOI
  20. [25]Denenberg VH Open-Field Behavior in the Rat: What does it mean? Ann. N. Y. Acad. Sci. 1969 159 852 859 10.1111/j.1749-6632.1969.tb12983.x 5260302 · DOI · Paper page
  21. [26]Carola V D’Olimpio F Brunamonti E Mangia F Renzi P Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice Behav. Brain Res. 2002 134 49 57 10.1016/S0166-4328(01)00452-1 12191791 · DOI · Paper page
  22. [27]Whimbey AE Denenberg V Two independent behavioral dimensions in open-field performance J. Comp. Physiol. Psychol. 1967 63 500 504 10.1037/h0024620 6064396 · DOI
  23. [28]Bailoo JD Jordan RL Garza XJ Tyler AN Brief and long periods of maternal separation affect maternal behavior and offspring behavioral development in C57BL/6 mice Dev. Psychobiol. 2013 56 674 685 10.1002/dev.21135 23775283 · DOI
  24. [29]Bailoo JD Bohlen MO Wahlsten DL The precision of video and photocell tracking systems and the elimination of tracking errors with infrared backlighting J. Neurosci. Methods 2010 188 45 52 10.1016/j.jneumeth.2010.01.035 20138914 PMC2847046 · DOI
  25. [30]Garner JP Reverse-translational biomarker validation of Abnormal Repetitive Behaviors in mice: an illustration of the 4P’s modeling approach Behav. Brain Res. 2011 219 189 196 10.1016/j.bbr.2011.01.002 21219937 PMC3062660 · DOI
  26. [31]Latham N Mason G Frustration and perseveration in stereotypic captive animals: is a taste of enrichment worse than none at all? Behav. Brain Res. 2010 211 96 104 10.1016/j.bbr.2010.03.018 20230861 · DOI
  27. [32]Gross AN Engel AKJ Richter SH Garner JP Würbel H Cage-induced stereotypies in female ICR CD-1 mice do not correlate with recurrent perseveration Behav. Brain Res. 2011 216 613 20 10.1016/j.bbr.2010.09.003 20837068 · DOI
  28. [33]Gross AN Richter SH Engel AKJ Würbel H Cage-induced stereotypies, perseveration and the effects of environmental enrichment in laboratory mice Behav. Brain Res. 2012 234 61 68 10.1016/j.bbr.2012.06.007 22721674 · DOI
  29. [34]Novak J Bailoo JD Melotti L Würbel H Effect of cage-induced stereotypies on measures of affective state and recurrent perseveration in CD-1 and C57BL/6 mice PLoS One 2016 11 e0153203 10.1371/journal.pone.0153203 27145080 PMC4856387 · DOI
  30. [38]Novak J Effects of stereotypic behaviour and chronic mild stress on judgement bias in laboratory mice Appl. Anim. Behav. Sci. 2016 174 162 172 10.1016/j.applanim.2015.10.004 · DOI
  31. [39]Jansen RG Wiertz L Meyer ES Noldus LPJJ Reliability analysis of observational data: Problems, solutions, and software implementation Behav. Res. Methods, Instruments, Comput. 2003 35 391 399 10.3758/BF03195516 14587547 · DOI
  32. [40]Gordon, C. J. Temperature Regulation in Laboratory Rodents. (Cambridge University Press, 1993).
  33. [41]Gordon CJ Relationship between autonomic and behavioral thermoregulation in the mouse Physiol. Behav. 1985 34 687 690 10.1016/0031-9384(85)90365-8 4034706 · DOI
  34. [42]Gordon C Becker P Ali JS Behavioral thermoregulatory responses of single- and group-housed mice Physiol. Behav. 1998 65 255 262 10.1016/S0031-9384(98)00148-6 9855474 · DOI
  35. [43]Reiss D Wolter-Sutter A Krezel W Ouagazzal AM Effects of social crowding on emotionality and expression of hippocampal nociceptin/orphanin FQ system transcripts in mice Behav. Brain Res. 2007 184 167 173 10.1016/j.bbr.2007.07.010 17697718 · DOI
  36. [44]Velez L Sokoloff G Miczek KA Palmer AA Dulawa SC Differences in Aggressive Behavior and DNA Copy Number Variants Between BALB/cJ and BALB/cByJ Substrains Behav. Genet. 2010 40 201 210 10.1007/s10519-009-9325-5 20033273 PMC3722062 · DOI
  37. [45]Walker M Mixed-strain housing for female C57BL/6, DBA/2, and BALB/c mice: validating a split-plot design that promotes refinement and reduction BMC Med. Res. Methodol. 2016 16 11 10.1186/s12874-016-0113-7 26817696 PMC4729181 · DOI
  38. [46]Leppaenen PK Ravaja N Ewalds-Kvist SBM Twenty-three generations of mice bidirectionally selected for open-field thigmotaxis: Selection response and repeated exposure to the open field Behav. Processes 2006 72 23 31 10.1016/j.beproc.2005.11.010 16386379 · DOI
  39. [48]Priebe K Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: A cross-fostering study Dev. Psychobiol. 2005 47 398 407 10.1002/dev.20098 16284964 · DOI
  40. [49]Palumbo ML Stress induced cognitive deficit is differentially modulated in BALB/c and C57Bl/6 mice: Correlation with Th1/Th2 balance after stress exposure J. Neuroimmunol. 2010 218 12 20 10.1016/j.jneuroim.2009.11.005 19942299 · DOI
  41. [50]Olsson IAS Dahlborn K Improving housing conditions for laboratory mice: a review of ‘environmental enrichment’ Lab. Anim. 2002 36 243 270 10.1258/002367702320162379 12144738 · DOI
  42. [52]Hurst JL Barnard C Tolladay U Nevison C West C Housing and welfare in laboratory rats: effects of cage stocking density and behavioural predictors of welfare Anim. Behav. 1999 58 563 586 10.1006/anbe.1999.1165 10479372 · DOI · Paper page
  43. [53]Moons CP Van Wiele P Odberg FO To enrich or not to enrich: providing shelter does not complicate handling of laboratory mice Contemp Top Lab Anim Sci 2004 43 18 21 15264764
  44. [54]Swetter BJ Karpiak CP Cannon JT Separating the effects of shelter from additional cage enhancements for group-housed BALB/cJ mice Neurosci. Lett. 2011 495 205 9 10.1016/j.neulet.2011.03.067 21457758 · DOI

Cited by

Sorted by citations

Authors
Bailoo, J. D., Murphy, E., Varholick, J. A., Novak, J., Palme, R., & Würbel, H.
Affiliations
  • University of Bern (CH)
  • University of Veterinary Medicine Vienna (AT)
Corresponding author
Bailoo, Jeremy D.
Venue
Scientific Reports
Published
2018-01-15
Volume
8
Issue
1
Pages
713-713
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2784208568
Cited by
37
References
7
Citations by year
2025: 2 · 2024: 11 · 2023: 2 · 2022: 2 · 2021: 5 · 2020: 5 · 2019: 4 · 2018: 6
FWCI
7.34
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Open Access CRIS of the University of Bern
Funders
FP7 Ideas: European Research Council (322576)
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Health Sciences › Veterinary › Small Animals › Animal testing and alternatives
  • Health Sciences › Veterinary › Small Animals › Veterinary Pharmacology and Anesthesia
Keywords
animal welfare, laboratory mice, space allowance, group size, stocking density, cage type, floor area, stress physiology, glucocorticoid metabolites, open field behavior, perseveration, stereotypy, food and water intake, body mass, aggression, BALB/cByJ
MeSH terms
Aggression, Animals, Animal Welfare, Behavior, Animal, Female, Housing, Animal, Male, Mice, Inbred BALB C, Mice, Inbred C57BL, Population Density

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review