Enrichment for Laboratory Zebrafish: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Chloe Stevens.

Enrichment is accepted as an essential requirement for meeting the behavioural needs and improving the welfare of many laboratory animal species, but in general, provision for zebrafish is minimal.

  • zebrafish
  • environmental enrichment
  • welfare
Please wait, diff process is still running!

References

  1. Harper, C.; Lawrence, C. The Laboratory Zebrafish; CRC Press: Boca Raton, FL, USA, 2011.
  2. Kinth, P.; Mahesh, G.; Panwar, Y. Mapping of Zebrafish Research: A Global Outlook. Zebrafish 2013, 10, 510–517.
  3. Lidster, K.; Readman, G.D.; Prescott, M.J.; Owen, S. International survey on the use and welfare of zebrafish Danio rerio in research. J. Fish Biol. 2017, 90, 1891–1905.
  4. Aleström, P.; D’Angelo, L.; Midtlyng, P.J.; Schorderet, D.F.; Schulte-Merker, S.; Sohm, F.; Warner, S. Zebrafish: Housing and husbandry recommendations. Lab. Anim. 2019, 54, 213–224.
  5. Lawrence, C.; Eisen, J.S.; Varga, Z.M. Husbandry and Health Program Survey Synopsis. Zebrafish 2016, 13, S5.
  6. Tsang, B.; Zahid, H.; Ansari, R.; Lee, R.C.-Y.; Partap, A.; Gerlai, R. Breeding Zebrafish: A Review of Different Methods and a Discussion on Standardization. Zebrafish 2017, 14, 561–573.
  7. Huntingford, F.A.; E Adams, C.; A Braithwaite, V.; Kadri, S.; Pottinger, T.G.; Sandoe, P.; Turnbull, J.F. Current issues in fish welfare. J. Fish Biol. 2006, 68, 332–372.
  8. Ashley, P.J. Fish welfare: Current issues in aquaculture. Appl. Anim. Behav. Sci. 2007, 104, 199–235.
  9. Brown, C. Fish intelligence, sentience and ethics. Anim. Cogn. 2015, 18, 1–17.
  10. Stevens, C.H.; Croft, D.P.; Paull, G.C.; Tyler, C.R. Stress and welfare in ornamental fishes: What can be learned from aquaculture? J. Fish Biol. 2017, 91, 409–428.
  11. Reed, B.; Jennings, M. Guidance on the Housing and Care of Zebrafish Danio Rerio; RSPCA: West Sussex, UK, 2011.
  12. Lawrence, C. Advances in Zebrafish Husbandry and Management. Methods Cell Biol. 2011, 104, 429–451.
  13. Sanders, G.E. Zebrafish Housing, Husbandry, Health, and Care: IACUC Considerations. ILAR J. 2012, 53, 205–207.
  14. Message, R.; Greenhough, B. “But It’s Just a Fish”: Understanding the Challenges of Applying the 3Rs in Laboratory Aquariums in the UK. Animals 2019, 9, 1075.
  15. Newberry, R.C. Environmental enrichment: Increasing the biological relevance of captive environments. Appl. Anim. Behav. Sci. 1995, 44, 229–243.
  16. Young, R.J. Environmental Enrichment for Captive Animals; Blackwell Science: Oxford, UK; Malden, MA, USA, 2003; ISBN 9780632064076.
  17. Olsson, I.A.S.; Dahlborn, K. Improving housing conditions for laboratory mice: A review of ‘environmental enrichment’. Lab. Anim. 2002, 36, 243–270.
  18. Simpson, J.; Kelly, J.P. The impact of environmental enrichment in laboratory rats—Behavioural and neurochemical aspects. Behav. Brain Res. 2011, 222, 246–264.
  19. Poole, T. Happy animals make good science. Lab. Anim. 1997, 31, 116–124.
  20. Williams, T.D.; Readman, G.D.; Owen, S.F. Key issues concerning environmental enrichment for laboratory-held fish species. Lab. Anim. 2009, 43, 107–120.
  21. Volgin, A.D.; Yakovlev, O.V.; Demin, K.A.; De Abreu, M.S.; Rosemberg, D.B.; Meshalkina, D.A.; Alekseeva, P.A.; Friend, A.J.; Amstislavskaya, T.G.; Kalueff, A.V. Understanding the Role of Environmental Enrichment in Zebrafish Neurobehavioral Models. Zebrafish 2018, 15, 425–432.
  22. Hutchinson, E.; Avery, A.; Vandewoude, S. Environmental Enrichment for Laboratory Rodents. ILAR J. 2005, 46, 148–161.
  23. Wurbel, H.; Garner, J.P. Refinement of Rodent Research through Environmental Enrichment and Systematic Randomization 2007. Available online: (accessed on 2 October 2020).
  24. Bayne, K. Environmental enrichment and mouse models: Current perspectives. Anim. Model. Exp. Med. 2018, 1, 82–90.
  25. Franks, B.; Sebo, J.; Horowitz, A. Fish are smart and feel pain: What about joy? Anim. Sentience 2018, 3, 16.
  26. Sneddon, L.U.; Wolfenden, D.C.; Leach, M.C.; Valentim, A.M.; Steenbergen, P.J.; Bardine, N.; Broom, D.M.; Brown, C. Ample evidence for fish sentience and pain. Anim. Sentience 2018, 3, 17.
  27. Sneddon, L.U. Evolution of nociception and pain: Evidence from fish models. Philos. Trans. R. Soc. B Biol. Sci. 2019, 374, 20190290.
  28. Birch, J. Animal sentience and the precautionary principle. Anim. Sentience 2017, 2, 1.
  29. Fife-Cook, I.; Franks, B. Positive Welfare for Fishes: Rationale and Areas for Future Study. Fishes 2019, 4, 31.
  30. Dawkins, M.S. Behaviour as a tool in the assessment of animal welfare. Zoology 2003, 106, 383–387.
  31. Mellen, J.; Macphee, M.S. Philosophy of environmental enrichment: Past, present, and future. Zoo Biol. 2001, 20, 211–226.
  32. Näslund, J.; Johnsson, J.I. Environmental enrichment for fish in captive environments: Effects of physical structures and substrates. Fish Fish. 2016, 17, 1–30.
  33. Benefiel, A.C.; Dong, W.K.; Greenough, W.T. Mandatory “Enriched” Housing of Laboratory Animals: The Need for Evidence-based Evaluation. ILAR J. 2005, 46, 95–105.
  34. Wilkes, L.; Owen, S.F.; Readman, G.D.; Sloman, K.A.; Wilson, R.W. Does structural enrichment for toxicology studies improve zebrafish welfare? Appl. Anim. Behav. Sci. 2012, 139, 143–150.
  35. Woodward, M.A.; Winder, L.A.; Watt, P.J. Enrichment Increases Aggression in Zebrafish. Fishes 2019, 4, 22.
  36. Egan, R.J.; Bergner, C.L.; Hart, P.C.; Cachat, J.M.; Canavello, P.R.; Elegante, M.F.; Elkhayat, S.I.; Bartels, B.K.; Tien, A.K.; Tien, D.H.; et al. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav. Brain Res. 2009, 205, 38–44.
  37. Maximino, C.; De Brito, T.M.; Batista, A.W.D.S.; Herculano, A.M.; Morato, S.; Gouveia, A. Measuring anxiety in zebrafish: A critical review. Behav. Brain Res. 2010, 214, 157–171.
  38. Bonga, S.E.W. The stress response in fish. Physiol. Rev. 1997, 77, 591–625.
  39. DePasquale, C.; Sturgill, J.; Braithwaite, V.A. A Standardized Protocol for Preference Testing to Assess Fish Welfare. J. Vis. Exp. 2020, 156.
  40. Bloomsmith, M.A.; Brent, L.Y.; Schapiro, S.J. Guidelines for developing and managing an environmental enrichment program for nonhuman primates. Lab. Anim. Sci. 1991, 41, 372–377.
  41. Suriyampola, P.S.; Shelton, D.S.; Shukla, R.; Roy, T.; Bhat, A.; Martins, E.P. Zebrafish Social Behavior in the Wild. Zebrafish 2016, 13, 1–8.
  42. Sundin, J.; Morgan, R.; Finnøen, M.H.; Dey, A.; Sarkar, K.; Jutfelt, F. On the Observation of Wild Zebrafish (Danio rerio) in India. Zebrafish 2019, 16, 546–553.
  43. Shelton, D.S.; Shelton, S.G.; Daniel, D.K.; Raja, M.; Bhat, A.; Tanguay, R.L.; Higgs, D.M.; Martins, E.P. Collective Behavior in Wild Zebrafish. Zebrafish 2020, 17, 243–252.
  44. Stednitz, S.J.; Washbourne, P. Rapid Progressive Social Development of Zebrafish. Zebrafish 2020, 17, 11–17.
  45. Al-Imari, L.; Gerlai, R. Sight of conspecifics as reward in associative learning in zebrafish (Danio rerio). Behav. Brain Res. 2008, 189, 216–219.
  46. Saverino, C.; Gerlai, R. The social zebrafish: Behavioral responses to conspecific, heterospecific, and computer animated fish. Behav. Brain Res. 2008, 191, 77–87.
  47. Collymore, C.; Tolwani, R.J.; Rasmussen, S. The Behavioral Effects of Single Housing and Environmental Enrichment on Adult Zebrafish (Danio rerio). J. Am. Assoc. Lab. Anim. Sci. 2015, 54, 280–285.
  48. Krueger, L.D.; E Thurston, S.; Kirk, J.; Elsaeidi, F.; Freeman, Z.T.; Goldman, D.; Lofgren, J.L.; Keller, J.M. Enrichment Preferences of Singly Housed Zebrafish (Danio rerio). J. Am. Assoc. Lab. Anim. Sci. 2020, 59, 148–155.
  49. Pritchard, V.L.; Lawrence, J.; Butlin, R.K.; Krause, J. Shoal choice in zebrafish, Danio rerio: The influence of shoal size and activity. Anim. Behav. 2001, 62, 1085–1088.
  50. Ruhl, N.; McRobert, S.P. The effect of sex and shoal size on shoaling behaviour in Danio rerio. J. Fish Biol. 2005, 67, 1318–1326.
  51. Ruhl, N.; McRobert, S.P.; Currie, W.J.S. Shoaling preferences and the effects of sex ratio on spawning and aggression in small laboratory populations of zebrafish (Danio rerio). Lab. Anim. 2009, 38, 264–269.
  52. Lawrence, C. Zebrafish. In Comfortable Quarters for Laboratory Animals; Liss, C., Litwak, K., Tilford, D., Reinhardt, V., Eds.; Animal Welfare Institute: Washington, WA, USA, 2015; pp. 87–99. ISBN 9780938414797.
  53. Pagnussat, N.; Piato, Â.L.; Schaefer, I.C.; Blank, M.; Tamborski, A.R.; Guerim, L.D.; Bonan, C.D.; Vianna, M.R.; Lara, D.R. One for All and All for One: The Importance of Shoaling on Behavioral and Stress Responses in Zebrafish. Zebrafish 2013, 10, 338–342.
  54. White, L.J.; Thomson, J.S.; Pounder, K.C.; Coleman, R.C.; Sneddon, L.U. The impact of social context on behaviour and the recovery from welfare challenges in zebrafish, Danio rerio. Anim. Behav. 2017, 132, 189–199.
  55. Tunbak, H.; Vazquez-Prada, M.C.; Ryan, T.M.; Kampff, A.R.; Dreosti, E. Whole-brain mapping of socially isolated zebrafish reveals that lonely fish are not loners. eLife 2020, 9, e55863.
  56. Shams, S.; Chatterjee, D.; Gerlai, R. Chronic social isolation affects thigmotaxis and whole-brain serotonin levels in adult zebrafish. Behav. Brain Res. 2015, 292, 283–287.
  57. Shams, S.; Facciol, A.; Chatterjee, D.; Gerlai, R.; Seguin, D. Effect of social isolation on anxiety-related behaviors, cortisol, and monoamines in adult zebrafish. Behav. Neurosci. 2017, 131, 492–504.
  58. Parker, M.O.; Millington, M.E.; Combe, F.J.; Brennan, C.H. Housing Conditions Differentially Affect Physiological and Behavioural Stress Responses of Zebrafish, as well as the Response to Anxiolytics. PLoS ONE 2012, 7, e34992.
  59. Forsatkar, M.N.; Safari, O.; Boiti, C. Effects of social isolation on growth, stress response, and immunity of zebrafish. Acta Ethol. 2017, 20, 255–261.
  60. Giacomini, A.C.V.V.; Abreu, M.S.; Zanandrea, R.; Saibt, N.; Friedrich, M.T.; Koakoski, G.; Gusso, D.; Piato, A.L.; Barcellos, L.J.G. Environmental and Pharmacological Manipulations Blunt the Stress Response of Zebrafish in a Similar Manner. Sci. Rep. 2016, 6, 28986.
  61. Lindsey, B.W.; Tropepe, V. Changes in the social environment induce neurogenic plasticity predominantly in niches residing in sensory structures of the zebrafish brain independently of cortisol levels. Dev. Neurobiol. 2014, 74, 1053–1077.
  62. Kareklas, K.; Elwood, R.W.; Holland, R.A. Grouping promotes risk-taking in unfamiliar settings. Behav. Process. 2018, 148, 41–45.
  63. Giacomini, A.C.V.V.; De Abreu, M.S.; Koakoski, G.; Idalêncio, R.; Kalichak, F.; Oliveira, T.A.; Da Rosa, J.G.S.; Gusso, D.; Piato, A.L.; Gil Barcellos, L.J. My stress, our stress: Blunted cortisol response to stress in isolated housed zebrafish. Physiol. Behav. 2015, 139, 182–187.
  64. Kurtzman, M.S.; Craig, M.P.; Grizzle, B.K.; Hove, J.R. Sexually segregated housing results in improved early larval survival in zebrafish. Lab. Anim. 2010, 39, 183–189.
  65. Reolon, G.K.; De Melo, G.M.; Rosa, J.G.D.S.D.; Gil Barcellos, L.J.; Bonan, C.D. Sex and the housing: Effects on behavior, cortisol levels and weight in zebrafish. Behav. Brain Res. 2018, 336, 85–92.
  66. Barton, B.A. Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids. Integr. Comp. Biol. 2002, 42, 517–525.
  67. Petitjean, Q.; Jean, S.; Gandar, A.; Côte, J.; Laffaille, P.; Jacquin, L. Stress responses in fish: From molecular to evolutionary processes. Sci. Total Environ. 2019, 684, 371–380.
  68. Ellis, T.; Yildiz, H.Y.; López-Olmeda, J.; Spedicato, M.T.; Tort, L.; Øverli, Ø.; Martins, C.I.M. Cortisol and finfish welfare. Fish Physiol. Biochem. 2011, 38, 163–188.
  69. Silva, P.F.; De Leaniz, C.G.; Luchiari, A.C. Fear contagion in zebrafish: A behaviour affected by familiarity. Anim. Behav. 2019, 153, 95–103.
  70. Faustino, A.I.S.; Tacão-Monteiro, A.; Oliveira, R.F. Mechanisms of social buffering of fear in zebrafish. Sci. Rep. 2017, 7, srep44329.
  71. Madeira, N.; Oliveira, R.F. Long-Term Social Recognition Memory in Zebrafish. Zebrafish 2017, 14, 305–310.
  72. Martins, E.P.; Bhat, A. Population-level personalities in zebrafish: Aggression-boldness across but not within populations. Behav. Ecol. 2014, 25, 368–373.
  73. Soares, S.M.; Kirsten, K.; Pompermaier, A.; Maffi, V.C.; Koakoski, G.; Woloszyn, M.; Barreto, R.E.; Gil Barcellos, L.J. Sex segregation affects exploratory and social behaviors of zebrafish according to controlled housing conditions. Physiol. Behav. 2020, 222, 112944.
  74. Ramsay, J.M.; Feist, G.W.; Varga, Z.M.; Westerfield, M.; Kent, M.L.; Schreck, C.B. Whole-body cortisol is an indicator of crowding stress in adult zebrafish, Danio rerio. Aquaculture 2006, 258, 565–574.
  75. Pavlidis, M.; Digka, N.; Theodoridi, A.; Campo, A.; Barsakis, K.; Skouradakis, G.; Samaras, A.; Tsalafouta, A. Husbandry of Zebrafish, Danio Rerio, and the Cortisol Stress Response. Zebrafish 2013, 10, 524–531.
  76. Castranova, D.; Lawton, A.; Lawrence, C.; Baumann, D.P.; Best, J.; Coscolla, J.; Doherty, A.; Ramos, J.; Hakkesteeg, J.; Wang, C.; et al. The Effect of Stocking Densities on Reproductive Performance in Laboratory Zebrafish (Danio rerio). Zebrafish 2011, 8, 141–146.
  77. Engeszer, R.E.; Patterson, L.B.; Rao, A.A.; Parichy, D.M. Zebrafish in The Wild: A Review of Natural History and New Notes from The Field. Zebrafish 2007, 4, 21–40.
  78. Spence, R.; Gerlach, G.; Lawrence, C.; Smith, C. The behaviour and ecology of the zebrafish, Danio rerio. Biol. Rev. 2007, 83, 13–34.
  79. Arunachalam, M.; Raja, M.; Vijayakumar, C.; Malaiammal, P.; Mayden, R.L. Natural History of Zebrafish (Danio rerio) in India. Zebrafish 2013, 10, 1–14.
  80. Parichy, D.M. Advancing biology through a deeper understanding of zebrafish ecology and evolution. eLife 2015, 4, e05635.
  81. Jones, N.A.; Spence, R.; Jones, F.A.; Spence-Jones, H.C. Shade as enrichment: Testing preferences for shelter in two model fish species. J. Fish Biol. 2019, 95, 1161–1165.
  82. Schroeder, P.; Jones, S.; Young, I.S.; Sneddon, L.U. What do zebrafish want? Impact of social grouping, dominance and gender on preference for enrichment. Lab. Anim. 2014, 48, 328–337.
  83. Kistler, C.; Hegglin, D.; Würbel, H.; König, B. Preference for structured environment in zebrafish (Danio rerio) and checker barbs (Puntius oligolepis). Appl. Anim. Behav. Sci. 2011, 135, 318–327.
  84. DePasquale, C.; Fettrow, S.; Sturgill, J.; Braithwaite, V.A. The impact of flow and physical enrichment on preferences in zebrafish. Appl. Anim. Behav. Sci. 2019, 215, 77–81.
  85. Lavery, M.; Braithwaite, V.; Miller, N.; Mason, G. Identifying enriched housing conditions for zebrafish (Danio rerio) that vary along a scale of preference. In Proceedings of the 53rd Congress of the ISAE: Animals Lives Worth Living, Bergen, Norway, 5–9 August 2019; Newberry, R.C., Braastad, B.O., Eds.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2019; p. 388.
  86. Tan, S.L.T.; Handasyde, K.A.; Rault, J.-L.; Mendl, M. Insensitivity to reward shifts in zebrafish (Danio rerio) and implications for assessing affective states. Anim. Cogn. 2019, 23, 87–100.
  87. Lee, C.J.; Paull, G.C.; Tyler, C.R. Effects of environmental enrichment on survivorship, growth, sex ratio and behaviour in laboratory maintained zebrafish Danio rerio. J. Fish Biol. 2018, 94, 86–95.
  88. Hamilton, I.M.; Dill, L.M. Monopolization of food by zebrafish (Danio rerio) increases in risky habitats. Can. J. Zoöl. 2002, 80, 2164–2169.
  89. Marcon, M.; Mocelin, R.; Benvenutti, R.; Costa, T.; Herrmann, A.P.; De Oliveira, D.L.; Koakoski, G.; Barcellos, L.J.G.; Piato, A. Environmental enrichment modulates the response to chronic stress in zebrafish. J. Exp. Biol. 2018, 221, jeb176735.
  90. Von Krogh, K.; Sørensen, C.; Nilsson, G.E.; Øverli, Ø. Forebrain cell proliferation, behavior, and physiology of zebrafish, Danio rerio, kept in enriched or barren environments. Physiol. Behav. 2010, 101, 32–39.
  91. A Keck, V.; Edgerton, D.S.; Hajizadeh, S.; Swift, L.L.; Dupont, W.D.; Lawrence, C.; Boyd, K.L. Effects of Habitat Complexity on Pair-Housed Zebrafish. J. Am. Assoc. Lab. Anim. Sci. 2015, 54, 378–383.
  92. Manuel, R.; Gorissen, M.; Stokkermans, M.; Zethof, J.; Ebbesson, L.O.; Van De Vis, H.; Flik, G.; Bos, R.V.D. The Effects of Environmental Enrichment and Age-Related Differences on Inhibitory Avoidance in Zebrafish (Danio rerio Hamilton). Zebrafish 2015, 12, 152–165.
  93. DePasquale, C.; Neuberger, T.; Hirrlinger, A.M.; Braithwaite, V.A. The influence of complex and threatening environments in early life on brain size and behaviour. Proc. R. Soc. B Boil. Sci. 2016, 283, 20152564.
  94. Spence, R.; Magurran, A.E.; Smith, C. Spatial cognition in zebrafish: The role of strain and rearing environment. Anim. Cogn. 2011, 14, 607–612.
  95. Roy, T.; Bhat, A. Learning and Memory in Juvenile Zebrafish: What makes the Difference—Population or Rearing Environment? Ethology 2016, 122, 308–318.
  96. Wafer, L.N.; Jensen, V.B.; Whitney, J.C.; Gomez, T.H.; Flores, R.; Goodwin, B.S. Effects of Environmental Enrichment on the Fertility and Fecundity of Zebrafish (Danio rerio). J. Am. Assoc. Lab. Anim. Sci. 2016, 55, 291–294.
  97. Marcon, M.; Mocelin, R.; Sachett, A.; Siebel, A.M.; Herrmann, A.P.; Piato, A. Enriched environment prevents oxidative stress in zebrafish submitted to unpredictable chronic stress. PeerJ 2018, 6, e5136.
  98. Bhat, A.; Greulich, M.M.; Martins, E.P. Behavioral Plasticity in Response to Environmental Manipulation among Zebrafish (Danio rerio) Populations. PLoS ONE 2015, 10, e0125097.
  99. Basquill, S.P.; Grant, J.W. An increase in habitat complexity reduces aggression and monopolization of food by zebra fish (Danio rerio). Can. J. Zoöl. 1998, 76, 770–772.
  100. Carfagnini, A.G.; Rodd, F.H.; Jeffers, K.B.; Bruce, A.E.E. The effects of habitat complexity on aggression and fecundity in zebrafish (Danio rerio). Environ. Boil. Fishes 2009, 86, 403–409.
  101. Weber, D.N.; Ghorai, J.K. Experimental Design Affects Social Behavior Outcomes in Adult Zebrafish Developmentally Exposed to Lead. Zebrafish 2013, 10, 294–302.
  102. Delaney, M.; Follet, C.; Ryan, N.; Hanney, N.; Lusk-Yablick, J.; Gerlach, G. Social Interaction and Distribution of Female Zebrafish (Danio rerio) in a Large Aquarium. Biol. Bull. 2002, 203, 240–241.
  103. Lee, C.J.; Tyler, C.R.; Paull, G.C. Can simple tank changes benefit the welfare of laboratory zebrafish Danio rerio? J. Fish Biol. 2018, 92, 653–659.
  104. Selye, H. Stress without Distress. In Psychopathology of Human Adaptation; Serban, G., Ed.; Springer: Boston, MA, USA, 1976; pp. 137–146. ISBN 9781468422382.
  105. Sykes, D.J.; Suriyampola, P.S.; Martins, E.P. Recent experience impacts social behavior in a novel context by adult zebrafish (Danio rerio). PLoS ONE 2018, 13, e0204994.
  106. Graham, C.; Von Keyserlingk, M.A.; Franks, B. Free-choice exploration increases affiliative behaviour in zebrafish. Appl. Anim. Behav. Sci. 2018, 203, 103–110.
  107. DePasquale, C.; Armstrong, P.; Li, X. The influence of enrichment on spatial pattern separation in zebrafish (Danio rerio). Bios 2020, 91, 31.
  108. Braithwaite, V.A.; Salvanes, A.G.V. Environmental variability in the early rearing environment generates behaviourally flexible cod: Implications for rehabilitating wild populations. Proc. R. Soc. B Biol. Sci. 2005, 272, 1107–1113.
  109. Gonzales, J.M.; Law, S.H.W. Feed and Feeding Regime Affect Growth Rate and Gonadosomatic Index of Adult Zebrafish (Danio rerio). Zebrafish 2013, 10, 532–540.
  110. Monteiro, J.F.; Martins, S.; Farias, M.; Costa, T.; Certal, A.C. The Impact of Two Different Cold-Extruded Feeds and Feeding Regimens on Zebrafish Survival, Growth and Reproductive Performance. J. Dev. Biol. 2018, 6, 15.
  111. Fowler, L.A.; Williams, M.B.; Dennis-Cornelius, L.N.; Farmer, S.; Barry, R.J.; Powell, M.L.; Watts, S.A. Influence of Commercial and Laboratory Diets on Growth, Body Composition, and Reproduction in the Zebrafish Danio rerio. Zebrafish 2019, 16, 508–521.
  112. Dametto, F.S.; Fior, D.; Idalencio, R.; Rosa, J.G.S.; Fagundes, M.; Marqueze, A.; Barreto, R.E.; Piato, A.; Barcellos, L.J. Feeding regimen modulates zebrafish behavior. PeerJ 2018, 6, e5343.
  113. Martins, C.I.M.; Galhardo, L.; Noble, C.; Damsgård, B.; Spedicato, M.T.; Zupa, W.; Beauchaud, M.; Kulczykowska, E.; Massabuau, J.-C.; Carter, T.; et al. Behavioural indicators of welfare in farmed fish. Fish Physiol. Biochem. 2011, 38, 17–41.
  114. Attia, J.; Millot, S.; Di-Poï, C.; Bégout, M.-L.; Noble, C.; Vázquez, F.J.S.; Terova, G.; Saroglia, M.; Damsgård, B. Demand feeding and welfare in farmed fish. Fish Physiol. Biochem. 2011, 38, 107–118.
  115. Oliveira, R.; Galhardo, L. Psychological Stress and Welfare in Fish. Annu. Rev. Biomed. Sci. 2009, 11, 1–20.
  116. Burn, C.C. Bestial boredom: A biological perspective on animal boredom and suggestions for its scientific investigation. Anim. Behav. 2017, 130, 141–151.
  117. Bagatto, B.; Pelster, B.; Burggren, W.W. Growth and metabolism of larval zebrafish: Effects of swim training. J. Exp. Biol. 2001, 204, 4335–4343.
  118. Hasumura, T.; Meguro, S. Exercise quantity-dependent muscle hypertrophy in adult zebrafish (Danio rerio). J. Comp. Physiol. B 2016, 186, 603–614.
  119. Suniaga, S.; Rolvien, T.; Scheidt, A.V.; Fiedler, I.A.K.; Bale, H.A.; Huysseune, A.; Witten, P.E.; Amling, M.; Busse, B. Increased mechanical loading through controlled swimming exercise induces bone formation and mineralization in adult zebrafish. Sci. Rep. 2018, 8, 1–13.
  120. Luchiari, A.C.; Chacon, D.M.M. Physical exercise improves learning in zebrafish, Danio rerio. Behav. Process. 2013, 100, 44–47.
  121. DePasquale, C.; Leri, J. The influence of exercise on anxiety-like behavior in zebrafish (Danio rerio). Behav. Process. 2018, 157, 638–644.
  122. Huntingford, F.; Kadri, S. Exercise, stress and welfare. In Swimming Physiology of Fish: Towards Using Exercise to Farm a Fit Fish in Sustainable Aquaculture; Palstra, A.P., Planas, J.V., Eds.; Springer: Berlin, Germany, 2013; pp. 161–174. ISBN 978-3-642-31049-2.
  123. Sambrook, T.D.; Buchanan-Smith, H.M. Control and Complexity in Novel Object Enrichment. Anim. Welf. 1997, 6, 207–216.
  124. Morgan, K.N.; Tromborg, C.T. Sources of stress in captivity. Appl. Anim. Behav. Sci. 2007, 102, 262–302.
  125. Mellor, D.J. Welfare-aligned Sentience: Enhanced Capacities to Experience, Interact, Anticipate, Choose and Survive. Animals 2019, 9, 440.
  126. Oliveira, J.; Silveira, M.; Chacon, D.; Luchiari, A. The Zebrafish World of Colors and Shapes: Preference and Discrimination. Zebrafish 2015, 12, 166–173.
  127. Avdesh, A.; Martin-Iverson, M.T.; Mondal, A.; Chen, M.; Askraba, S.; Morgan, N.; Lardelli, M.; Groth, D.M.; Verdile, G.; Martins, R.N. Evaluation of Color Preference in Zebrafish for Learning and Memory. J. Alzheimer’s Dis. 2012, 28, 459–469.
  128. Roy, T.; Suriyampola, P.S.; Flores, J.; López, M.; Hickey, C.; Bhat, A.; Martins, E.P. Color preferences affect learning in zebrafish, Danio rerio. Sci. Rep. 2019, 9, 1–10.
  129. De Abreu, M.S.; Giacomini, A.C.; Genario, R.; Dos Santos, B.E.; Marcon, L.; Demin, K.A.; Kalueff, A.V. The impact of housing environment color on zebrafish anxiety-like behavioral and physiological (cortisol) responses. Gen. Comp. Endocrinol. 2020, 294, 113499.
  130. Avdesh, A.; Chen, M.; Martin-Iverson, M.T.; Mondal, A.; Ong, D.; Rainey-Smith, S.; Taddei, K.; Lardelli, M.; Groth, D.M.; Verdile, G.; et al. Regular Care and Maintenance of a Zebrafish (Danio rerio) Laboratory: An Introduction. J. Vis. Exp. 2012.
  131. Barcellos, H.H.A.; Koakoski, G.; Chaulet, F.; Kirsten, K.S.; Kreutz, L.C.; Kalueff, A.V.; Barcellos, L.J.G. The effects of auditory enrichment on zebrafish behavior and physiology. PeerJ 2018, 6, e5162.
  132. Schirmer, A.; Jesuthasan, S.J.; Mathuru, A.S. Tactile stimulation reduces fear in fish. Front. Behav. Neurosci. 2013, 7, 167.
  133. Easter, J.S.S.; Nicola, G.N. The Development of Vision in the Zebrafish (Danio rerio). Dev. Biol. 1996, 180, 646–663.
  134. Osborne, N.; Paull, G.; Grierson, A.; Dunford, K.; Busch-Nentwich, E.M.; Sneddon, L.U.; Wren, N.; Higgins, J.; Hawkins, P. Report of a Meeting on Contemporary Topics in Zebrafish Husbandry and Care. Zebrafish 2016, 13, 584–589.
  135. Toth, L.A.; Kregel, K.; Leon, L.; I Musch, T. Environmental Enrichment of Laboratory Rodents: The Answer Depends on the Question. Comp. Med. 2011, 61, 314–321.
  136. Eskola, S.; Lauhikari, M.; H-M, V.; Laitinen, M.; Nevalainen, T. Environmental enrichment may alter the number of rats needed to achieve statistical significance. Scand. J. Lab. Anim. Sci. 1999, 26, 134–144.
  137. Van De Weerd, H.A.; Aarsen, E.L.; Mulder, A.; Kruitwagen, C.L.J.J.; Hendriksen, C.F.M.; Baumans, V. Effects of Environmental Enrichment for Mice: Variation in Experimental Results. J. Appl. Anim. Welf. Sci. 2002, 5, 87–109.
  138. Wolfer, D.P.; Litvin, O.; Morf, S.; Nitsch, R.M.; Lipp, H.-P.; Würbel, H.; Wuerbel, H. Cage enrichment and mouse behaviour. Nat. Cell Biol. 2004, 432, 821–822.
  139. Sorrells, A.D.; Corcoran-Gomez, K.; Eckert, K.A.; Fahey, A.G.; Hoots, B.L.; Charleston, L.B.; Charleston, J.S.; Roberts, C.R.; Markowitz, H. Effects of environmental enrichment on the amyotrophic lateral sclerosis mouse model. Lab. Anim. 2009, 43, 182–190.
  140. Mikkelsen, L.F.; Sørensen, D.B.; Krohn, T.; Lauritzen, B.; Ottesen, J.L. Clinical pathology and cardiovascular parameters are not influenced by housing rats under increased environmental complexity. Anim. Welf. 2010, 19, 449–460.
  141. Bailoo, J.D.; Murphy, E.; Boada-Saña, M.; Varholick, J.A.; Hintze, S.; Baussière, C.; Hahn, K.C.; Göpfert, C.; Palme, R.; Voelkl, B.; et al. Effects of Cage Enrichment on Behavior, Welfare and Outcome Variability in Female Mice. Front. Behav. Neurosci. 2018, 12, 232.
  142. André, V.; Gau, C.; Scheideler, A.; Aguilar-Pimentel, J.A.; Amarie, O.V.; Becker, L.; Garrett, L.; Hans, W.; Hölter, S.M.; Janik, D.; et al. Laboratory mouse housing conditions can be improved using common environmental enrichment without compromising data. PLoS Biol. 2018, 16, e2005019.
  143. Hubrecht, R.C.; Kirkwood, J. The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals; Wiley-Blackwell: Oxford, UK, 2010; ISBN 9781444318784.
  144. Richter, S.H.; Garner, J.P.; Würbel, H. Environmental standardization: Cure or cause of poor reproducibility in animal experiments? Nat. Methods 2009, 6, 257–261.
  145. Moons, C.P.H.; Van Wiele, P.; O Odberg, F. To enrich or not to enrich: Providing shelter does not complicate handling of laboratory mice. Contemp. Top. Lab. Anim. Sci. 2004, 43, 18–21.
  146. LaFollette, M.R.; Riley, M.C.; Cloutier, S.; Brady, C.M.; O’Haire, M.E.; Gaskill, B.N. Laboratory Animal Welfare Meets Human Welfare: A Cross-Sectional Study of Professional Quality of Life, Including Compassion Fatigue in Laboratory Animal Personnel. Front. Vet. Sci. 2020, 7, 114.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback