Animal welfare issues under laboratory constraints, an ethological perspective: rodents and marmosets

  • Augusto Vitale
  • Francesca Cirulli
  • Francesca Capone
  • Enrico Alleva
Part of the Animal Welfare book series (AWNS, volume 2)


Animal Welfare Nonhuman Primate Pain Sensitivity Common Marmoset Lion Tamarin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abbott DH, Hearn JP. Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey (Callithrix jacchus). J Reprod Fert 1978; 53:155-166CrossRefGoogle Scholar
  2. Alleva E. Assessment of aggressive behavior in rodents. In Methods in Neurosciences: Paradigms for the Study of Behavior. Conn MP ed, Academic Press, New York 1993; vol 14:111-137Google Scholar
  3. Alleva E, Castellano C, Oliverio A. Effects of L- and D-amino acids on analgesia and locomotor activity of mice: their interaction with morphine. Brain Res 1980; 198:249-252CrossRefPubMedGoogle Scholar
  4. Alleva E, Caprioli A, Laviola G. Postnatal social environment affects morphine analgesia in male mice. Physiol Behav 1986; 36:779-781CrossRefPubMedGoogle Scholar
  5. Alleva E, Laviola G, Bignami G. Morphine effects on activity and pain reactivity of developing mice with or without late prenatal oxazepam exposure. Psychopharmacology 1987; 92:438-40CrossRefPubMedGoogle Scholar
  6. Alleva E, Petruzzi S, Ricceri L. Evaluating the social behaviour of rodents: Laboratory, semi-naturalistic and naturalistic approaches. In Behavioural Brain Research in Naturalistic and Semi-naturalistic Settings. Alleva E, Fasolo A, Lipp HP, Nadel L, Ricceri L eds, Kluwer Academic, Dordrecht, The Netherlands 1995; 359-374Google Scholar
  7. Alleva E, Cirulli F, Bianchi M, Bondiolotti GP, Chiarotti F, De Acetis L, Panerai AE. Behavioural characterization of interleukin-6 overexpressing or deficient mice during agonistic encounters. Eur J Neurosci 1998; 12:3664-3672CrossRefGoogle Scholar
  8. Amir S, Brown ZW, Amit Z. The role of endorphins in stress: evidence and speculations. Neurosci Biobehav Rev 1979; 4:77-86CrossRefGoogle Scholar
  9. Ankier SI. New hot plate tests to quantify antinociceptive and narcotic antagonist activities. Eur J Pharmacol 1974; 27:1-4CrossRefPubMedGoogle Scholar
  10. Bateson P. Assessment of pain in animals. Anim Behav 1991; 42:827-839CrossRefGoogle Scholar
  11. Bigi S, Maestripieri D, Aloe L, Alleva E. NGF decreases isolation-induced aggressive behavior, while increasing adrenal volume in adult male mice. Physiol Behav 1992; 51:337-343CrossRefPubMedGoogle Scholar
  12. Bigi S, De Acetis L, Chiarotti F, Alleva E. Substance P effects on intraspecific aggressive behaviour of isolated male mice: an ethopharmacological analysis. Behav Pharmacol 1993a; 4:495-500CrossRefPubMedGoogle Scholar
  13. Bigi S, De Acetis L, De Simone R, Aloe L, Alleva E. Neonatal capsaicin exposure affects isolation-induced aggressive behavior and hypothalamic substance P levels in adult male mice. Behav Neurosci 1993b; 107:363-369CrossRefPubMedGoogle Scholar
  14. Blanchard RJ, McKittrick CR, Blanchard DC. Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol Behav 2001; 73:261-271CrossRefPubMedGoogle Scholar
  15. Brain PF, Nowell NW. Isolation versus grouping effects on adrenal and gonadal functions in albino mice: I. The male. Gen Comp Endocrinol 1971a; 16:149-154CrossRefPubMedGoogle Scholar
  16. Brain PF, Nowell NW. Isolation versus grouping effects on adrenal and gonadal functions in albino mice: II. The female. Gen Comp Endocrinol 1971b; 16:155-159CrossRefPubMedGoogle Scholar
  17. Brain PF, Stanislaw H. A reevaluation of the effects of differential housing on physiology and behaviour in male and female mice. Aggress Behav 1988; 8:130-132CrossRefGoogle Scholar
  18. Bressers WMA, Haccou P, Kruk MR, Meelis M, Van Erp AMM, Willekens-Bramer DC. A time-structured analysis of hypothalamically induced increases in self-grooming and activity in rat. Behav Neurosci 1995; 109:1158-1171CrossRefPubMedGoogle Scholar
  19. Brug DR, Slotnick BM. Response of colony mice to intruders with different fighting experience. Aggress Behav 1983; 9:49-58CrossRefGoogle Scholar
  20. Buchanan-Smith HM. Environmental control: An important feature of good captive Callitrichids environments. In Marmosets and Tamarins in Biological and Biomedical Research. Pryce C, Scott L, Schnell C eds, DSSD Imagery, Salisbury 1997; 47-53Google Scholar
  21. Byron JK, Bodri MS. Environmental enrichment for laboratory marmosets. Lab Anim Europe 2001; 1:34-37Google Scholar
  22. Cairns RB, Hood KE, Midlam J. On fighting in mice: Is there a sensitive period for isolation effects? Anim Behav 1985; 33:166-180CrossRefGoogle Scholar
  23. Carere C, Casetti R, De Acetis L, Perretta G, Cirulli F, Alleva E. Behavioural and nociceptive response in male and female spiny mice (Acomys cahirinus) upon exposure to snake odour. Behav Proc 1999; 47:1-10CrossRefGoogle Scholar
  24. Caston J, Devulder B, Jouen F, Lalonde R, Delhaye-Bouchaud N, Mariani J. Role of an enriched environment on the restoration of behavioral deficits in Lurcher mutant mice. Dev Psychobiol 1999; 35:291-303CrossRefPubMedGoogle Scholar
  25. Cirulli F, Adriani W, Laviola G. Sexual segregation in infant mice: Behavioural and neuroendocrine responses to d-amphetamine administration. Psychopharmacology 1997; 134:140-152CrossRefPubMedGoogle Scholar
  26. Cirulli F, Berry A, Alleva E. Early disruption of the mother-infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci Biobehav Rev 2003; 27:73-82CrossRefPubMedGoogle Scholar
  27. Cotman C, Berchtold NC. Exercise: a behavioural intervention to enhance brain health and plasticity. Trends Neurosci 2002; 25:295-300CrossRefPubMedGoogle Scholar
  28. Crowcroft P, Rowe FP. Social organization and territorial behaviour in the wild house (Mus musculus L.). Proc Zool Soc Lond 1963; 140:517-531Google Scholar
  29. Crawley JN, Schleidt WM, Contrera JF. Does social environment decrease propensity to fight in male mice? Behav Biol 1975; 73-83Google Scholar
  30. Darwin C. The Expression of the Emotions in Man and Animals. Murray, London 1872.CrossRefGoogle Scholar
  31. Dawkins MS. Behavioural deprivation: a central problem in animal welfare. Appl Anim Behav Sci 1988; 20:209-225CrossRefGoogle Scholar
  32. Dawkins MS. From an animal’s point of view: motivation, fitness, and animal welfare. Behav Brain Sci 1990; 13:1-25Google Scholar
  33. Della Seta D, De Acetis L, Aloe L, Alleva E. NGF effects on hot plate behaviors in mice. Pharmacol Biochem Behav 1994; 49:701-705CrossRefPubMedGoogle Scholar
  34. DeRosa C, Vitale A, Puopolo M. The puzzle-feeder as feeling enrichment for common marmosets (Callithrix jacchus): a pilot study. Lab Anim 2003; 37:100-107CrossRefGoogle Scholar
  35. Digby LJ. Sexual behaviour and extragroup copulation in a wild population of common marmosets (Callithrix jacchus). Folia primatol 1999, 70:136-145CrossRefPubMedGoogle Scholar
  36. D’Udine B, Alleva E. On the teleonomic study of maternal behaviour. In The Dialetics of Biology Group. Muir A, Rose S eds, Allison and Busby, London, UK 1980; 50-61Google Scholar
  37. Duncan IJH, Fraser D. Understanding animal welfare. In Animal Welfare. Appleby MC, Hughes BO eds, CAB International, Wallingford 1997; 19-31Google Scholar
  38. Eddy NB, Touchberry CF, Lieberman JE. Synthetic analgesics. I. Methadone isomers and derivatives. J Pharmacol Exp Ther 1950; 98:121-37PubMedGoogle Scholar
  39. Estep DQ, Lanier DL, Dewsbury DA. Copulatory behaviour and nesting-building behaviour of wild house mice (Mus musculus L.). Anim Learn Behav 1975; 3:329-336PubMedGoogle Scholar
  40. European Commission. Third report from the Commission to the Council and the European Parliament on the statistics on the number of animals used for experimental and other scientific purposes in the member States of the European Union 2003a. European Commission. The welfare of non-human primates used in research. Report of the scientific committee on animal health and animal welfare 2003b;
  41. Flecknell PA. Refinement of animal use - assessment and alleviation of pain and distress. Lab Anim 1994; 28:222-231CrossRefPubMedGoogle Scholar
  42. Fraser AF. The behaviour of suffering in animals. Appl Anim Behav Sci 1984; 13:1CrossRefGoogle Scholar
  43. Galef BG, Sorge RE. Use of PVC conduits by rats of various strains and ages housed singly and in pairs. J Appl Anim Welf Sci 2000; 3:279-292CrossRefGoogle Scholar
  44. Hubrecht RC. Home-range size, use and territorial behavior in the common marmoset (Callithrix jacchus jacchus), at the Tapacurà Field Station, Recife, Brazil. Int J Primatol 1985; 6:553-560CrossRefGoogle Scholar
  45. Hunskaar S, Berge OG, Hole KA. Modified hot-plate test sensitive to mild analgesics. Behav Brain Res 1986; 21:101-108CrossRefPubMedGoogle Scholar
  46. Inglett BJ, French JA, Simmons LG, Vires KW. Dynamics of intrafamily aggression and social reintegration in lion tamarins. Zoo Biol 1989; 8:67-78CrossRefGoogle Scholar
  47. International Association for the Study of Pain. Report of subcommittee on taxonomy. Pain 1979; 6: 249-252Google Scholar
  48. Kleinman DG. Characteristics of reitroduction and sociosexual interactions in pairs of lion tamarins (Leontopithecus rosalia) during the reproductive cycle. In Biology and Conservation of the Callitrichidae. Kleinman DG ed, Smithsonian Institution Press, Washington DC 1979; 181-190Google Scholar
  49. Laviola G, De Acetis L, Bignami G, Alleva E. Prenatal oxazepam enhances mouse maternal aggression in the offspring, without modifying acute chlordiazepoxide effects. Neurotoxicol Teratol, 1991; 13:75-81CrossRefPubMedGoogle Scholar
  50. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, Chao MV, Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 1992; 69:737-749CrossRefPubMedGoogle Scholar
  51. Maestripieri D, De Simone R, Aloe L, Alleva E. Social status and nerve growth factor serum levels after agonistic encounters in mice. Physiol Behav 1990; 47:161-164CrossRefPubMedGoogle Scholar
  52. McGrew WC, McLuckie EC. Phylopatry and dispersion in the cotton-top tamarin, Saguinus o. oedipus: An attempted laboratory simulation. Int J Primatol 1986; 7:401-422CrossRefGoogle Scholar
  53. McGrew WC, Brennan JA, Russell J. An artifical “gum-tree” for marmosets (Callithrix j. jacchus). Zoo Biol 1986; 5:45-50CrossRefGoogle Scholar
  54. Mittermaier RA, Rylands AB, Coimbra-Fihlo AF, Fonseca GAB eds. Ecology and Behaviour of Neotropical Primates. World Wildlife Fund, Washington DC 1988Google Scholar
  55. Nelson RJ, Chiavegatto S. Molecular basis of aggression. Trends Neurosci 2001; 24:713-719CrossRefPubMedGoogle Scholar
  56. Nevison CM, Hurst JL, Barnard CJ. Strain-specific effects of cage enrichment in male laboratory mice (Mus musculus). Anim Welf 1999; 8:361-379Google Scholar
  57. Newberry RC. Environmental enrichment: increasing the biological relevance of captive environments. Appl Anim Behav Sci 1995; 44:229-243CrossRefGoogle Scholar
  58. Ostermeyer NC. Maternal aggression. In Parental Behaviour of Rodents. Elwood RW ed, Wiley, Chichester 1983: 151-179Google Scholar
  59. Petto AJ, Devin M. Food choices in captive common marmoset (Callithrix jacchus). Lab Primate Newsl 1988; 27:7-9Google Scholar
  60. Pietropaolo S, Branchi I, Chiarotti F, Alleva E. Utilization of a physically-enriched environment by laboratory mice: age and gender differences. Submitted.Google Scholar
  61. Rachels J. Created from Animals: The Moral Implications of Darwinism. Oxford University Press, Oxford 1990Google Scholar
  62. Reinhardt V. Caged rhesus monkeys voluntary work for ordinary food. Primates 1994; 35:95-98CrossRefGoogle Scholar
  63. Reinhardt V, Roberts LR. Effective feeding enrichment for non-human primates: a brief review. Anim Welf 1997; 6:265-272Google Scholar
  64. Rodgers RJ, Hendrie CA. Social conflict activates status-dependent endogenous analgesic or hyperalgesic mechanisms in male mice: effects of naloxone on nociception and behaviour. Physiol Behav 1983; 30:775-780CrossRefPubMedGoogle Scholar
  65. Rosenzweig MR, Krech D, Bennett EL. Heredity environment, brain biochemistry, and learning. In Current Trends in Psychological Theory. Pittsburg PA, University of Pittsburgh Press 1961; 87-110Google Scholar
  66. Rothe H, Darms K. The social organisation of marmosets: a critical evaluation of recent concepts. In Marmosets and Tamarins: Systematics, Behaviour and Ecology. Rylands AB ed, Oxford University Press, Oxford 1993; 176-199Google Scholar
  67. Rothe H, Koenig A. Variability of social organisation in captive common marmoset (Callithrix jacchus). Folia primatol 1991; 57:28-33CrossRefGoogle Scholar
  68. Russell WMS, Burch RL. The Principles of Humane Experimental Technique. University Federation for Animal Welfare, South Mimms, England 1959Google Scholar
  69. Rylands AB. The Callitrichidae: a biological review. In Marmosets and Tamarins in Biological Research. Pryce C, Scott L, Schnell C eds, DSSD Imagery, Salisbury 1997; 1-9Google Scholar
  70. Saylor A, Salmon M. Communal nursing in mice: Influence of multiple mothers and growth of the young. Science 1969; 164:1309-1310CrossRefGoogle Scholar
  71. Schnaffer CM, Caine NG. The peacefulness of cooperatively breeding primates. In Natural Conflict Resolution. Aureli F, De Waal FBM eds, University of California Press, Berkeley 2000; 155-169Google Scholar
  72. Sherwin CM. Preferences of individually housed TO strain laboratory mice for loose substrate or tubes for sleeping. Lab Anim 1996; 30:245-251CrossRefPubMedGoogle Scholar
  73. Sherwin CM. Observations on the prevalence of nest building in non-breeding TO strain mice and their use of two nesting materials. Lab Anim 1997; 31:125-132CrossRefPubMedGoogle Scholar
  74. Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT. Primate Societies. Chicago University Press, Chicago 1987Google Scholar
  75. Spillantini MG, Aloe L, Alleva E, De Simone R, Goedert M, Levi-Montalcini R. Nerve growth factor mRNA and protein increase in hypothalamus. Proc Natl Acad Sci USA 1989; 86:8555-8559CrossRefPubMedGoogle Scholar
  76. Stevenson MF, Poole TP. An ethogram of the common marmoset (Callithrix jacchus jacchus): general behavioural repertoire. Anim Behav 1976; 24:428-451CrossRefPubMedGoogle Scholar
  77. Taber RI. Predictive value of analgesic assays in mice and rats. In Narcotic Antagonists. Advances in Biochemical Psychopharmacology. Braude MC, Harris LS, May EL, Smith JP, Villarreal JE eds, Raven Press, New York 1974; 191-212Google Scholar
  78. Tomasello M, Call J. Animal Cognition. Oxford University Press, New York 1997Google Scholar
  79. Viercki CJ Jr, Cooper BY. Guidelines for assessing pain modulation in laboratory animal subjects. In Advances in Pain Research and Therapy. Kruger L, Liebeskind JC eds, Raven Press, New York 1984; 305-22Google Scholar
  80. Visalberghi E, Alleva E. Book review of: The Inevitable Bond: Examining Scientist-Animal Interactions (Davis D and Balfour D, eds. Cambridge UP 1992). Quart J Exptl Psychol 1998; 46B:222-224Google Scholar
  81. Vitale A, Alleva E. Ethological and welfare considerations in the study of aggression in rodents and nonhuman primates. In Animal Models of Human Emotion and Cognition. Haug M, Whalen RE eds, American Psychological Association, Washington DC 1999; 283-295CrossRefGoogle Scholar
  82. Wiesel TN, Hubel DH. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 1963; 26:1003-1017PubMedGoogle Scholar
  83. Woolfe G, MacDonald AD. The evaluation of the analgesic action of Pethidine hydrochloride (Demerol). J Pharmacol Exp Ther 1944; 80:300-307Google Scholar
  84. Wright EM Jr, Marcella KL, Woodso JF. Animal pain: evaluation and control. Lab Anim 1985; 20Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Augusto Vitale
    • 1
  • Francesca Cirulli
    • 2
  • Francesca Capone
    • 3
  • Enrico Alleva
    • 4
  1. 1.Department of Cell Biology and NeurosciencesIstituto Superiore di SanitàItaly
  2. 2.Department of Cell Biology and NeurosciencesIstituto Superiore di SanitàItaly
  3. 3.Department of Cell Biology and NeurosciencesIstituto Superiore di SanitàItaly
  4. 4.Department of Cell Biology and NeurosciencesIstituto Superiore di SanitàItaly

Personalised recommendations