Abstract
Running wheels are frequently used to improve the welfare of captive animals, increase environmental enrichment, and, by doing so, reduce stereotypic behaviors. With the exception of a single investigation, all previous scientific literature investigating wheel running behavior has been based on animals in captive environments. This specific study reported that free-ranging animals in the Netherlands voluntary run in wheels placed in nature. Our study explores that same line of investigation, examining whether wild animals will voluntarily use running wheels in a natural area in Paraguay in comparison to the urban and semi-urban settings in the Netherlands. Of the 1857 small mammal visits we recorded, only two occasions showed evidence of what could be considered as wheel running behavior; over 100-fold fewer than previously reported. The potential reasons for the observed difference in wheel running activity, such as different species pool or seasonality, are discussed. The difference, however, is expected to be due to the much lower probability of Neotropical mammals in a remote natural site encountering man-made objects and experiencing urbanization-related behavioral patterns.
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Data Availability
The data and materials for all experiments are available in the electronic supplementary data. The experiments described in this manuscript are not preregistered.
References
Bird BL, Branch LC, Miller DL (2004) Effects of coastal lighting on foraging behavior of beach mice. Conserv Biol 18(5):1435–1439. https://doi.org/10.1111/j.1523-1739.2004.00349.x
Clark JD, Gebhart GF, Gonder JC, Keeling ME, Kohn DF (1997) The 1996 guide for the care and use of laboratory animals. ILAR J 38(1):41–48. https://doi.org/10.1093/ilar.38.1.41
Colbert LH, Mai V, Tooze JA, Perkins SN, Berrigan D, Hursting SD (2006) Negative energy balance induced by voluntary wheel running inhibits polyp development in APCMin mice. Carcinog 27(10):2103–2107. https://doi.org/10.1093/carcin/bgl056
Collier G, Leshner AI (1967) An invariant in mouse running wheel behavior. Psychon Sci 8(1):9–10. https://doi.org/10.3758/BF03330641
Cooper JJ, Nicol CJ (1996) Stereotypic behaviour in wild caught and laboratory bred bank voles (Clethrionymus glareolus). Anim Welf 5(3):245–257
Cummins M (2006) Opossum on exercise wheel. Retrieved January 17, 2018, from Animal Advocates website: https://www.youtube.com/watch?v=e7YObR2A-hE
de Almeida AJ, Torquetti CG, Talamoni SA (2008) Use of space by neotropical marsupial Didelphis albiventris (Didelphimorphia: Didelphidae) in an urban forest fragment. Rev Bras Zootec 25(2):214–219. https://doi.org/10.1590/S0101-81752008000200008
Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: Modifications due to human-induced stress. Urban Ecosyst 9(1):5–12. https://doi.org/10.1007/s11252-006-3262-3
Ehninger D, Kempermann G (2003) Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex 13(8):845–851. https://doi.org/10.1093/cercor/13.8.845
Fleming TH (1971) Population ecology of three species of Neotropical rodents. Miscellaneous Publications, Museum of Zoology, University of Michigan, No, p 143
Fonio E, Benjamini Y, Sakov A, Golani I (2006) Wild mouse open field behavior is embedded within the multidimensional data space spanned by laboratory inbred strains. Genes, Brain Behav 5(5):380–388. https://doi.org/10.1111/j.1601-183X.2005.00170.x
Frantz SC, Comings JP (1976) Evaluation of urban rodent infestations—an approach in Nepal. Proceedings of the 7th Vertebrate Pest Conference
Garner JP (2005) Stereotypies and other abnormal repetitive behaviors: Potential impact on validity, reliability, and replicability of scientific outcomes. ILAR J 46(2):106–117. https://doi.org/10.1093/ilar.46.2.106
Garner JP, Mason GJ (2002) Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents. Behav Brain Res 136(1):83–92. https://doi.org/10.1016/S0166-4328(02)00111-0
Gebhardt-Henrich SG, Vonlanthen EM, Steiger A (2005) How does the running wheel affect the behaviour and reproduction of golden hamsters kept as pets? Appl Anim Behav Sci 95(3–4):199–203. https://doi.org/10.1016/j.applanim.2005.02.019
Hansen LT, Berthelsen H (2000) The effect of environmental enrichment on the behaviour of caged rabbits (Oryctolagus cuniculus). Appl Anim Behav Sci 68(2):163–178. https://doi.org/10.1016/S0168-1591(00)00093-9
Hay J, Arnott MA, Aitken PP, Kendall AT (1986) Experimental toxocariasis and hyperactivity in mice. Zeitschrift Für Parasitenkunde 72(1):115–120. https://doi.org/10.1007/BF00927742
Jacobs GH, Neitz J, Deegan JF (1991) Retinal receptors in rodents maximally sensitive to ultraviolet light. Nat 353(6345):655. https://doi.org/10.1038/353655a0
Janik D, Mrosovsky N (1993) Nonphotically induced phase shifts of circadian rhythms in the golden hamster: Activity-response curves at different ambient temperatures. Physiol Behav 53(3):431–436. https://doi.org/10.1016/0031-9384(93)90135-3
Kavanau JL (1967) Behavior of captive white-footed mice. Sci 155(3770):1623–1639. https://doi.org/10.1126/science.155.3770.1623
Lehrer EW, Schooley RL (2010) Space use of woodchucks across an urbanization gradient within an agricultural landscape. J Mammal 91(6):1342–1349. https://doi.org/10.1644/09-MAMM-A-254.1
Lund PW (1840) View of the fauna of Brazil, previous to the last geological revolution. Mag Nat His 4:1–389
Luniak M (2004) Synurbization: Adaptation of animal wildlife to urban development. In Proceedings of the 4th International Symposium On Urban Wildlife Conservation 50–55. https://doi.org/10.1099/mic.0.069724-0
Mason GJ (1991) Stereotypies: A critical review. Anim Behav 41(6):1015–1037. https://doi.org/10.1016/S0003-3472(05)80640-2
Mason GJ, Latham NR (2004) Can’t stop, won’t stop: Is stereotypy a reliable animal welfare indicator? Anim Welf 13:57–69. https://doi.org/10.2307/4493573
Mason GJ, Mendl MT (1993) Why is there no simple way of measuring animal welfare? Anim Welf 2:301–319
Mason G, Würbel H (2016) What can be learnt from wheel-running by wild mice, and how can we identify when wheel-running is pathological? Proc R Soc B: Biol Sci 283(1824):20150738. https://doi.org/10.1098/rspb.2015.0738
Mather JG (1981) Wheel-running activity: A new interpretation. Mammal Rev 11(1):41–51. https://doi.org/10.1111/j.1365-2907.1981.tb00246.x
Mathes WF, Nehrenberg DL, Gordon R, Hua K, Garland T, Pomp D (2010) Dopaminergic dysregulation in mice selectively bred for excessive exercise or obesity. Behav Brain Res 210(2):155–163. https://doi.org/10.1016/j.bbr.2010.02.016
Meijer JH, Robbers Y (2014) Wheel running in the wild. Proc R Society B: Biol Sci 281(1786):20140210. https://doi.org/10.1098/rspb.2014.0210
Mikesic DG, Drickamer LC (1992) Factors affecting home-range size in house mice (Mus musculus domesticus) living in outdoor enclosures. Am Midl Nat 127(1):31–40. https://doi.org/10.2307/2426319
Morgan KN, Tromborg CT (2007) Sources of stress in captivity. Appl Anim Behav Sci 102(3–4):262–302. https://doi.org/10.1016/j.applanim.2006.05.032
O’Farrell MJ (1974) Seasonal activity patterns of rodents in a sagebrush community. J Mammal 55(4):809–823. https://doi.org/10.2307/1379409
Ödberg FO (1987) The influence of cage size and environmental enrichment on the development of stereotypies in bank voles (Clethrionomys glareolus). Behav Proc 14(2):155–173. https://doi.org/10.1016/0376-6357(87)90042-8
Olsson IAS, Dahlborn K (2002) Improving housing conditions for laboratory mice: A review of “environmental enrichment.” Lab Anim 36(3):243–270. https://doi.org/10.1258/002367702320162379
Powell SB, Newman HA, Pendergast JF, Lewis MH (1999) A rodent model of spontaneous stereotypy: Initial characterization of developmental, environmental, and neurobiological factors. Physiol Behav 66(2):355–363. https://doi.org/10.1016/S0031-9384(98)00303-5
Prange S, Gehrt SD, Wiggers EP (2004) Influences of anthropogenic resources on raccoon (Procyon lotor) movements and spatial distribution. J Mammal 85(3):483–490. https://doi.org/10.1644/BOS-121
Rhodes JS, Van Praag H, Jeffrey S, Girard I, Mitchell GS, Garland T, Gage FH (2003) Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci 117(5):1006–1016. https://doi.org/10.1037/0735-7044.117.5.1006
Richter H, Ambrée O, Lewejohann L, Herring A, Keyvani K, Paulus W, Sachser N (2008) Wheel-running in a transgenic mouse model of Alzheimer’s disease: Protection or symptom? Behav Brain Res 190(1):74–84. https://doi.org/10.1016/j.bbr.2008.02.005
Richter SH, Gass P, Fuss J (2014) Resting is rusting: A critical view on rodent wheel-running behavior. Neurosci 20(4):313–325. https://doi.org/10.1177/1073858413516798
Šálek M, Drahníková L, Tkadlec E (2015) Changes in home range sizes and population densities of carnivore species along the natural to urban habitat gradient. Mammal Rev 45(1):1–14. https://doi.org/10.1111/mam.12027
Sherwin CM (1998) Voluntary wheel running: A review and novel interpretation. Anim Behav 56(1):11–27. https://doi.org/10.1006/anbe.1998.0836
Shyne A (2006) Meta-analytic review of the effects of enrichment on stereotypic behavior in zoo mammals. Zoo Biol 25(4):317–337. https://doi.org/10.1002/zoo.20091
Smith P (2007) Fauna Paraguay Handbook of the Mammals of Paraguay: White-eared opossum Didelphis albiventris. Mammals of Paraguay No 1
Smith P, Atkinson K, Brouard J-P, Pheasey H (2016) Reserva Natural Laguna Blanca, Departamento San Pedro: Paraguay’s first important areas for the conservation of amphibians and reptiles? Russian J Herpetol 23(1):25–34
Sneddon J, Lee J, Ballantyne R, Packer J (2016) Animal welfare values and tourist behaviour. Ann Tour Res 57:234–236. https://doi.org/10.1016/j.annals.2016.01.006
Snell-Rood EC, Wick N (2013) Anthropogenic environments exert variable selection on cranial capacity in mammals. Proc R Soc B: Biol Sci 280(1769):20131384. https://doi.org/10.1098/rspb.2013.1384
Terio KA, Munson L, Marker L (2004) Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. J Wildl Dis 40(2):259–266. https://doi.org/10.7589/0090-3558-40.2.259
The World Bank Group (2017a) Climate Change Knowledge Portal. Retrieved January 10, 2017. http://sdwebx.worldbank.org/.
The World Bank Group (2017b) World Bank Open Data. Retrieved January 17, 2018. http://data.worldbank.org/indicator/EN.POP.DNST
Umetsu F, Paul Metzger J, Pardini R (2008) Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: A test with Atlantic forest small mammals. Ecogr 31(3):359–370. https://doi.org/10.1111/j.0906-7590.2008.05302.x
Wagner JA (1842) Diagnosen neuer Arten brasilischer Säugthiere. Archiv für Naturgeschichte 8(1):356–362
Werner C, Fürster T, Widmann T, Pöss J, Roggia C, Hanhoun M, Laufs U (2009) Physical exercise prevents cellular senescence in circulating leukocytes and in the vessel wall. Circ 120(24):2438–2447. https://doi.org/10.1161/CIRCULATIONAHA.109.861005
Winrow CJ, Hemming ML, Allen DM, Quistad GB, Casida JE, Barlow C (2003) Loss of neuropathy target esterase in mice links organophosphate exposure to hyperactivity. Nat Genet 33(4):477–485. https://doi.org/10.1038/ng1131
Wollnik F, Breit A, Reinke D (1991) Seasonal change in the temporal organization of wheel-running activity of the European Hamster. Cricetus cricetus Naturwissenschaften 78(9):419–422. https://doi.org/10.1007/BF01133417
Würbel H (2001) Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci 24(4):207–211. https://doi.org/10.1016/S0166-2236(00)01718-5
Würbel H, Chapman R, Rutland C (1998) Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Appl Anim Behav Sci 60(1):69–81. https://doi.org/10.1016/S0168-1591(98)00150-6
Acknowledgments
We thank Karina Atkinson from Fundacion Para la Tierra for the permission to conduct our research at the Para La Tierra ecological station, Malvina Duarte, the owner of Laguna Blanca, for her foresight and support, Els van Suijlekom for her help conceiving the study, and particularly Bence Schmatovich for the useful comments and discussions about the topic. We also thank the staff members, interns, and volunteers who helped with fieldwork, Eleonóra Fitos for the habitat photographs, and Gabor L. Lovei, Nick A. Littlewood and two anonymous reviewers for comments on the manuscript. We would also like to thank Dierenbeschermingscentrum Amersfoort for allowing us to monitor captive animals’ behaviour, the United States Fish and Wildlife service, Lush Cosmetics, and Rolex Awards for Enterprise for their financial support which paid for equipment used during our study.
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PvL and MAG contributed equally to this work: conceived and designed the study, collected field data, participated in data analysis, drafted and finalized the manuscript; GP participated in the design of the study, provided habitat map, coordinated the study, and helped in drafting and finalizing the manuscript; JS contributed to the conception and design and helped draft the manuscript. All authors gave final approval for publication.
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All work was conducted with the relevant permits necessary for work with wildlife in Paraguay. The experiment was carried out in accordance with the relevant guidelines and regulations as set out in the Environmental Law 96/92 and 1561/00. All experimental protocols were overseen by JS, of Fundacion Para La Tierra, registered in the National Wildlife Registry (RNVS No 1384) and the official permission for the research approved by Secretaria del Ambiente (SEAM); Permiso No 110/2015.
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The authors declare that they have no conflict of interest.
Supplementary Information
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Supplementary Data S1. Movie clip of an unidentified mouse (Cricetidae, Oligoryzomys sp.) moving the wheel. Baited period, 21 April 2016, 03:03 (MP4 437 KB)
Supplementary Data S2. Captive mouse (Mus musculus) running in a similarly large sized wheel (diameter of 28 cm) with identical design as used in the study. Filmed by PvL on 28 August 2020 (MP4 6.3 MB)
Supplementary Data S3. Movie clip of wheel running behavior by unidentified opossum (Didelphidae, suspected gray short-tailed opossum Monodelphis domesitca) in the transitional forest. Baited period, 24 April 2016, 18:34 (MP4 504 KB)
Supplementary Data S4. Movie clip of wheel running behavior by unidentified rat in the transitional forest. Unbaited period, 23 May 2016, 18:01. Note that the second smaller wheel present in the video was part of a supplementary project investigating the influence of wheel size on rodent activity. The presence of this supplementary wheel had no statistical influence on the study and the subsequent data were omitted from the present analysis (MP4 650 KB)
Supplementary Data S5. Movie clip of wheel movement from inside the wheel (WMI) by unidentified mouse, whilst not running. Preliminary period, 3 March 2016, 00:11 (MP4 1.8 MB)
Supplementary Data S6. Movie clip of wheel movement from outside the wheel (WMO) by unidentified rat. Baited period, 18 April 2016, 03:23 (MP4 2.3 MB)
Supplementary Data S7. Movie clip of wheel pulling by an unidentified opossum (Didelphidae, suspected Marmosa sp.). Preliminary period, 15 March 2016, 01:34 (MP4 1.2 MB)
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Supplementary Data S8. Dataset of all wheel movements categorized chronologically with locations, date, time, taxa, wheel movements, wheel movement durations, and habitats (PDF 68 KB)
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van Lunteren, P., Groenewold, M.A., Pozsgai, G. et al. Does voluntary wheel running exist in Neotropical wild mammals?. acta ethol 24, 23–30 (2021). https://doi.org/10.1007/s10211-020-00359-2
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DOI: https://doi.org/10.1007/s10211-020-00359-2