The effects of environmental enrichment on the behaviour of suckling piglets and lactating sows: A review

Livestock Science

Volumn 143, Issue 2-3, 2012, Pages 116-131

  Vanheukelom, Valerie ^a,b   Driessen, Bert ^a,b   Geers, Rony ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b Thomas More University College   (Belgium)

Author keywords

Behaviour; Environmental enrichment; Piglets; Sows; Welfare

Indexed keywords

SUIDAE;

EID: 84855796353     PISSN: 18711413     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.livsci.2011.10.002     Document Type: Review

References (112)

1. Andersen I.L., Berg S., Bøe K.E. Crushing of piglets by the mother sow (Sus scrofa) - purely accidental or a poor mother?. Appl. Anim. Behav. Sci. 2005, 93:229-243.
2. Arey D.S., Sancha E.S. Behaviour and productivity of sows and piglets in a family system and in farrowing crates. Appl. Anim. Behav. Sci. 1996, 50:135-145.
3. Arey D.S., Petchey A.M., Fowler V.R. The preparturient behaviour of sows in enriched pens and the effect of pre-formed nests. Appl. Anim. Behav. Sci. 1991, 31:61-68.
4. Arey D.S., Petchey A.M., Fowler V.R. The effect of straw on farrowing site choice and nest building behaviour in sows. Anim. Prod. 1992, 54:129-133.
5. Barnett J.L., Hemsworth P.H., Cronin G.M., Jongman E.C., Hutson G.D. A review of the welfare issues for sows and piglets in relation to housing. Aust. J. Agric. Res. 2001, 2001(52):1-28.
6. Beattie V.E., Walker N., Sneddon I.A. Effect of rearing environment and change of environment on the behaviour of gilts. Appl. Anim. Behav. Sci. 1995, 46:57-65.
7. Beattie V.E., O'Connell N.E.O., Kilpatrick D.J., Moss B.W. Influence of environmental enrichment on welfare-related behavioural and physiological parameters in growing pigs. Anim. Sci. 2000, 70:443-450.
8. Benus R.F., Den Daas S., Koolhaas J.M., Van Oortmerssen G.A. Routine formation and flexibility in social and non-social behaviour of aggressive and non-aggressive male mice. Behavior 1990, 112:176-193.
9. Bergeron R., Bolduc J., Ramonet Y., Meunier-Salaün M.C., Robert S. Feeding motivation and stereotypies in pregnant sows fed increasing levels of fibre and/or food. Appl. Anim. Behav. Sci. 2000, 70:27-40.
10. Blackshaw J.K., Swain A.J., Blackshaw A.W., Thomas F.J.M., Gillies K.J. The development of playful behaviour in piglets from birth to weaning in three farrowing environments. Appl. Anim. Behav. Sci. 1997, 55:37-49.
11. Boissy A., Manteuffel G., Jensen M.B., Moe R.O., Spruijt B., Keeling L.J., Winckler C., Forkman B., Dimitrov I., Langbein J., Bakken M., Viessier I., Aubert A. Assessment of positive emotions in animals to improve their welfare. Physiol. Behav. 2007, 92:375-397.
12. Bolhuis J.E., Schouten W.G.P., Schrama J.W., Wiegant V.M. Behavioural development of pigs with different coping characteristics in barren and substrate-enriched housing conditions. Appl. Anim. Behav. Sci. 2005, 93:213-228.
13. Bolhuis J.E., Schouten W.G.P., Schrama J.W., Wiegant V.M. Effects of rearing and housing environment on behaviour and performance of pigs with different coping characteristics. Appl. Anim. Behav. Sci. 2006, 101:68-85.
14. Bornett H.L.I., Edge H.L., Edwards S.A. Alternatives to nose-ringing in outdoor sows: 1. The provision of a sacrificial rooting area. Appl. Anim. Behav. Sci. 2003, 83:267-276.
15. Boyle L.A., Leonard F.C., Lynch P.B., Brophy P. Influence of housing system during gestation on the behaviour and welfare of gilts in farrowing crates. Anim. Sci. 2000, 71:561-570.
16. Boyle L.A., Regan D., Leonard F.C., Lynch P.B., Brophy P. The effect of mats on the welfare of sows and piglets in the farrowing house. Anim. Welf. 2000, 9:39-48.
17. Boyle L.A., Leonard F.C., Lynch P.B., Brophy P. Effect of gestation housing on behaviour and skin lesions of sows in farrowing crates. Appl. Anim. Behav. Sci. 2002, 76:119-134.
18. Broom D.M. Animal welfare: concepts and measurements. J. Anim. Sci. 1991, 69:4167-4175.
19. Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci. 2005, 21:513-521.
20. Burri M., Wechsler B., Gygax L., Weber R. Influence of straw length, sow behaviour and room temperature on the incidence of dangerous situations for piglets in a loose farrowing system. Appl. Anim. Behav. Sci. 2009, 117:181-189.
21. Castrén H., Algers B., de Passillé A.-M., Rushen J., Uvnäs-Moberg K. Preparturient variation in progesterone, prolactin, oxytocin and somatostatin in relation to nest building in sows. Appl. Anim. Behav. Sci. 1993, 38:91-102.
22. Chaloupková H., Illman G., Bartoš L., Špinka M. The effect of pre-weaning housing on the play and agonistic behaviour of domestic pigs. Appl. Anim. Behav. Sci. 2007, 103:25-34.
23. Colson V., Orgeur P., Foury A., Mormède P. Consequences of weaning piglets at 21 and 28 days on growth, behaviour and hormonal responses. Appl. Anim. Behav. Sci. 2006, 98:70-88.
24. Council Directive 2001/93/EC 2001. Official Journal of the European Communities L 316/36.
25. Cox L.N., Cooper J.J. Observations on the pre- and post-weaning behaviour of piglets reared in commercial indoor and outdoor environments. Anim. Sci. 2001, 72:75-86.
26. Cronin G.M., Smith J.A. Effects of accommodation type and straw bedding around parturition and during lactation on the behaviour of primiparous sows and survival and growth of piglets to weaning. Appl. Anim. Behav. Sci. 1992, 33:191-208.
27. Cronin G.M., Smith J.A. Suckling behaviour of sows in farrowing crates and straw-bedded pens. Appl. Anim. Behav. Sci. 1992, 33:175-189.
28. Cronin G.M., Smith J.A., Hodge F.M., Hemsworth P.H. The behaviour of primiparous sows around farrowing in response to restraint and straw bedding. Appl. Anim. Behav. Sci. 1994, 39:269-280.
29. Cronin G.M., Simpson G.J., Hemsworth P.H. The effects of the gestation and farrowing environments on sow and piglet behaviour and piglet survival and growth in early lactation. Appl. Anim. Behav. Sci. 1996, 46:175-192.
30. D'Eath R.B. Socialising piglets before weaning improves social hierarchy formation when pigs are mixed post-weaning. Appl. Anim. Behav. Sci. 2005, 93:199-211.
31. Damm B.I., Bildsøe M., Gilbert C., Ladewig J., Vestergaard K.S. The effects of confinement on periparturient behaviour and circulating prolactin, prostaglandin F2alpha and oxytocin in gilts with access to a variety of nest materials. Appl. Anim. Behav. Sci. 2002, 76:135-156.
32. Damm B.I., Lisborg L., Vestergaard K.S., Vanicek J. Nest-building, behavioural disturbances and heart rate in farrowing sows kept in crates and Schmid pens. Livest. Prod. Sci. 2003, 80:175-187.
33. Damm B.I., Forkman B., Pedersen L.J. Lying down and rolling behaviour in sows in relation to piglet crushing. Appl. Anim. Behav. Sci. 2005, 90:3-20.
34. Day J.E.L., Burfoot A., Docking C.M., Whittaker X., Spoolder H.A.M., Edwards S.A. The effects of prior experience of straw and the level of straw provision on the behaviour of growing pigs. Appl. Anim. Behav. Sci. 2002, 76:189-202.
35. de Jong I.C., Prelle I.T., van de Burgwal J.A., Lambooij E., Korte S.M., Blokhuis H.J., Koolhaas J.M. Effects of environmental enrichment on behavioral responses to novelty, learning, and memory, and the circadian rhythm in cortisol in growing pigs. Physiol. Behav. 2000, 68:571-578.
36. de Jonge F.H., Boleij H., Baars A.M., Dudink S., Spruijt B.M. Music during playtime: Using context conditioning as a tool to improve welfare in piglets. Appl. Anim. Behav. Sci. 2008, 115:138-148.
37. Dudink S., Simonse H., Marks I., de Jonge F.H., Spruijt B.M. Announcing the arrival of enrichment increases play behaviour and reduces weaning-stress-induced behaviours of piglets directly after weaning. Appl. Anim. Behav. Sci. 2006, 101:86-101.
38. Dybkjær L., Olsen A.N.W., Møller F., Jensen K.H. Effects of farrowing conditions on behaviour in multi-suckling pens for pigs. Acta Agric. Scand. Sect. A, Anim. Sci. 2001, 51:134-141.
39. Farm Animal Welfare Council Report on the Welfare of Pigs Kept Outdoors 1996, FAWC, Surbiton, UK.
40. Fraser D. Some behavioural aspects of milk ejection failure by sows. Br. Vet. J. 1977, 133:126-133.
41. Fraser D., Phillips P.A., Thompson B.K., Tennessen T. Effect of straw on the behaviour of growing pigs. Appl. Anim. Behav. Sci. 1991, 30:307-318.
42. Harris M.J., Gonyou H.W. Increasing available space in a farrowing crate does not facilitate postural changes or maternal responses in gilts. Appl. Anim. Behav. Sci. 1998, 59:285-296.
43. Herskin M.S., Jensen K.H., Thodberg K. Influence of environmental stimuli on maternal behaviour related to bonding, reactivity and crushing of piglets in domestic sows. Appl. Anim. Behav. Sci. 1998, 58:241-254.
44. Hillman E., von Hollen F., Bünger B., Todt D., Schrader L. Farrowing conditions affect the reactions of piglets towards novel environment and social confrontation at weaning. Appl. Anim. Behav. Sci. 2003, 81:99-109.
45. Hötzel M.J., Pinheiro Machado F.L.C., Wolf F.M., Dalla Costa O.A. Behaviour of sows and piglets reared in intensive outdoor or indoor systems. Appl. Anim. Behav. Sci. 2004, 86:27-39.
46. Jansen J., Bolhuis E., Schouten W.G.P., Spruijt B.M., Wiegant V.M. Spatial learning in pigs: effects of environmental enrichment and individual characteristics on behaviour and performance. Anim. Cogn. 2009, 12:303-315.
47. Jarvis S., McLean K.A., Calvert S.K., Deans L.A., Chirnside J., Lawrence A.B. The responsiveness of sows to their piglets in relation to the length of parturition and the involvement of endogenous opioids. Appl. Anim. Behav. Sci. 1999, 63:195-207.
48. Jarvis S., Calvert S.K., Stevenson J.S., Leeuwen N., Lawrence A.B. Pituitary-adrenal activation in pre-parturient pigs (Sus scrofa) is associated with behavioural restriction due to lack of space rather than nesting substrate. Anim. Welf. 2002, 11:371-384.
49. Jarvis S., Reed B.T., Lawrence A.B., Calvert S.K., Stevenson J.S. Peri-natal environmental effects on maternal behaviour, pituitary and adrenal activation, and the progress of parturition in the primiparous sow. Anim. Welf. 2004, 13:171-181.
50. Jarvis S., D'eath R.B., Robson S.K., Lawrence A.B. The effect of confinement during lactation on the hypothalamic-pituitary-adrenal axis and behaviour of primiparous sows. Physiol. Behav. 2006, 87:345-352.
51. Jensen P. Nest building in domestic sows: the role of external stimuli. Anim. Behav. 1993, 45:351-358.
52. Johnson A.K., Morrow-Tesch J.L., McGlone J.J. Behaviour and performance of lactating sows and piglets reared indoors or outdoors. J. Anim. Sci. 2001, 79:2571-2579.
53. Kanaan V.T., Pajor E.A., Lay D.C., Richert B.T., Garner J.P. A note on the effects of co-mingling piglet litters on pre-weaning growth, injuries and responses to behavioural tests. Appl. Anim. Behav. Sci. 2008, 110:386-391.
54. Krause E.T., Naguib M., Trillmich F., Schrader L. The effects of short term enrichment on learning in chickens from a laying strain (Gallus gallus domesticus). Appl. Anim. Behav. Sci. 2006, 101:318-327.
55. Kutzer T., Bünger B., Kjaer J.B., Schrader L. Effects of early contact between non-littermate piglets and of the complexity of farrowing conditions on social behaviour and weight gain. Appl. Anim. Behav. Sci. 2009, 121:16-24.
56. Lewis E., Boyle L.A., O'Doherty J.V., Lynch P.B., Brophy P. The effect of providing shredded paper or ropes to piglets in farrowing crates on their behaviour and the health and behaviour of their dams. Appl. Anim. Behav. Sci. 2006, 96:1-17.
57. Maletínská J., Špinka M. Cross-suckling and nursing synchronisation in group housed lactating sows. Appl. Anim. Behav. Sci. 2001, 75:17-32.
58. Marchetti C., Drent P.J. Individual differences in the use of social information by captive great tits. Anim. Behav. 2000, 60:131-140.
59. McGlone J.J., von Borell E.H., Deen J., Johnson A.K., Levis D.G., Meunier-Salaün M., Morrow J., Reeves D., Salak-Johnson J.L., Sundberg P.L. Review: Compilation of the scientific literature comparing housing systems for gestating sows and gilts using measures of physiology, behavior, performance, and health. Prof. Anim. Sci. 2004, 20:105-117.
60. Morrow-Tesch J., McGlone J.J. Sensory systems and nipple attachment behaviour in neonatal pigs. Physiol. Behav. 1990, 47:1-4.
61. Morrow-Tesch J., McGlone J.J. Sources of maternal odors and the development of odor preferences in baby pigs. J. Anim. Sci. 1990, 68:3563-3571.
62. Munsterhjelm C., Peltoniemi O.A.T., Heinonen M., Hälli O., Karhapää M., Valros A. Experience of moderate bedding affects behaviour of growing pigs. Appl. Anim. Behav. Sci. 2009, 118:42-53.
63. Newberry R.C. Environmental enrichment: Increasing the biological relevance of captive environments. Appl. Anim. Behav. Sci. 1995, 44:229-243.
64. O'Connell N.E., Beattie V.E., Sneddon I.A., Breuer K., Mercer J.T., Rance K.A., Sutcliffe M.E.M., Edwards S.A. Influence of individual predisposition, maternal experience and lactation environment on the responses of pigs to weaning at two different ages. Appl. Anim. Behav. Sci. 2005, 90:219-232.
65. Olsson I.A.S., de Jonge F.H., Schuurman T., Helmond F.A. Poor rearing conditions and social stress in pigs: repeated social challenge and the effect on behavioural and physiological responses to stressors. Behav. Processes 1999, 46:201-215.
66. Pedersen L., Studnitz J.M., Jensen K.H., Giersing A.M. Suckling behaviour of piglets in relation to accessibility to the sow and the presence of foreign litters. Appl. Anim. Behav. Sci. 1998, 58:267-279.
67. Peña Y., Prunell M., Rotllant D., Armario A., Escorihuela R.M. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 2009, 34:1390-1404.
68. Penny R.C.H., Farmer A.M.T., Lomas M.J. 'Up and away!' - Do hot air balloons scare outdoor pigs?. Pig J. 1995, 34:59-67.
69. Petersen V., Recen B., Vestergaard K. Behaviour of sows and piglets during farrowing under free-range conditions. Appl. Anim. Behav. Sci. 1990, 26:169-179.
70. Petersen V., Simonsen H.B., Lawson L.G. The effect of environmental stimulation on the development of behaviour in pigs. Appl. Anim. Behav. Sci. 1995, 45:215-224.
71. Pitts A.D., Weary D.M., Fraser D., Pajor E.A., Kramer D.L. Alternative housing for sows and litters Part 5. Individual differences in the maternal behaviour of sows. Appl. Anim. Behav. Sci. 2002, 76:291-306.
72. Poole T.B. The nature and evolution of behavioural needs in mammals. Anim. Welf. 1992, 1:203-220.
73. Ramonet Y., Meunier-Salaün M.C., Dourmad J.Y. High-fiber diets in pregnant sows: digestive utilization and effects on the behavior of the animals. J. Anim. Sci. 1999, 77:591-599.
74. Rhodes T., Appleby M.C., Douglas K.C.L., Firkins L.D., Houpt K.A., Irwin C., McGlone J.J., Sundberg P., Tokach L., Wills R.W. A comprehensive review of housing for pregnant sows. J. Am. Vet. Med. Assoc. 2005, 227:1580-1590.
75. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 1996, 78:57-65.
76. Rosenzweig M.R., Bennett E.L., Diamond M.C. Brain changes in response to experience. Sci. Am. 1972, 226:22-29.
77. Rutherford K.M.D., Robson S.K., Donald R.D., Jarvis S., Sandercock D.A., Scott E.M., Nolan A.M., Lawrence A.B. Pre-natal stress amplifies the immediate behavioural responses to acute pain in piglets. Biol. Lett. 2009, 5(4):452-454.
78. Schaefer A.L., Salomons M.O., Tong A.K.W., Sather A.P., Lepage P. The effect of environment enrichment on aggression in newly weaned piglets. Appl. Anim. Behav. Sci. 1990, 27:41-52.
79. Schmid H. Ethological design of a practicable farrowing pen. Proceedings of the International Congress on Applied Ethology, Berlin 1993, 238-242.
80. Schrøder-Petersen D.L., Simonsen H.B. Tail biting in pigs. Vet. J. 2001, 162:196-210.
81. Scott K., Taylor L., Gill B.P., Edwards S.A. Influence of different types of environmental enrichment on the behaviour of finishing pigs in two different housing systems 1. Hanging toy versus rootable substrate. Appl. Anim. Behav. Sci. 2006, 99:222-227.
82. Scott K., Taylor L., Gill B.P., Edwards S.A. Influence of different types of environmental enrichment on the behaviour of finishing pigs in two different housing systems 3. Hanging toy versus rootable toy of the same material. Appl. Anim. Behav. Sci. 2009, 116:186-190.
83. Sneddon I.A., Beattie V.E., Dunne L., Neil W. The effect of environmental enrichment on learning in pigs. Anim. Welf. 2000, 9:373-383.
84. Špinka M. How important is natural behaviour in animal farming systems?. Appl. Anim. Behav. Sci. 2006, 100:117-128.
85. Špinka M., Newberry R.C., Bekoff M. Mammalian play: training for the unexpected. Q. Rev. Biol. 2001, 76:141-168.
86. Stolba A., Wood-Gush D.G.M. The identification of behavioural key features and their incorporation into a housing design for pigs. Ann. Rec. Vet. 1984, 15(2):287-298.
87. Studnitz M., Jensen M.B., Pedersen L.J. Why do pigs root and in what will they root? A review on the exploratory behaviour of pigs in relation to environmental enrichment. Appl. Anim. Behav. Sci. 2007, 107:183-197.
88. Thodberg K., Jensen K.H., Herskin M.S., Jørgensen E. Influence of environmental stimuli on nest building and farrowing behaviour in domestic sows. Appl. Anim. Behav. Sci. 1999, 63:131-144.
89. Thodberg K., Jensen K.H., Herskin M.S. Nursing behaviour, post partum activity and reactivity in sows. Effects of farrowing environment, previous experience and temperament. Appl. Anim. Behav. Sci. 2002, 77:53-76.
90. Van de Weerd H.A., Baumans V. Environmental enrichment in rodents. AWIC Resource Series 1995, 2:145-149.
91. Van de Weerd H.A., Day J.E.L. A review of environmental enrichment for pigs housed in intensive housing systems. Appl. Anim. Behav. Sci. 2009, 116:1-20.
92. Van de Weerd H.A., Docking C.M., Day J.E.L., Avery P.J., Edwards S.A. A systematic approach towards developing environmental enrichment for pigs. Appl. Anim. Behav. Sci. 2003, 84:101-118.
93. Van de Weerd H.A., Docking C.M., Day J.E.L., Edwards S.A. The development of harmful social behaviour in pigs with intact tails and different enrichment backgrounds in two housing systems. Anim. Sci. 2005, 80:289-298.
94. Van de Weerd H.A., Docking C.M., Day J.E.L., Breuer K., Edwards S.A. Effects of species-relevant environmental enrichment on the behaviour and productivity of finishing pigs. Appl. Anim. Behav. Sci. 2006, 99:230-247.
95. Wattanakul W., Steward A.H., Edwards S.A., English P.R. Effects of grouping piglets and changing sow location on suckling behaviour and performance. Appl. Anim. Behav. Sci. 1997, 55:21-35.
96. Wattanakul W., Stewart A.H., Edwards S.A., English P.R. The effect of cross-suckling and presence of additional piglets on sucking behaviour and performance of individually housed litters. Anim. Sci. 1998, 66:449-455.
97. Weary D.M., Fraser D. Vocal responses of piglets to weaning: effect of piglet age. Appl. Anim. Behav. Sci. 1997, 54:153-160.
98. Weary D.M., Pajor E.A., Bonenfant M., Fraser D., Kramer D.L. Alterative housing for sows and litters. Part 4. Effects of sow-controlled housing combined with a communal piglet area on pre- and post-weaning behaviour and performance. Appl. Anim. Behav. Sci. 2002, 76:279-290.
99. Weary D.M., Jasper J., Hötzel M.J. Understanding weaning distress. Appl. Anim. Behav. Sci. 2008, 110:24-41.
100. Webster S., Dawkins M. The post-weaning behaviour of indoor-bred and outdoor-bred pigs. Anim. Sci. 2000, 71:265-271.
101. Wechsler B. Normal behaviour as a basis for animal welfare assessment. Anim. Welf. 2007, 16:107-110.
102. Wells D.L. Sensory stimulation as environmental enrichment for captive animals: a review. Appl. Anim. Behav. Sci. 2009, 118:1-11.
103. Wemelsfelder F. Animal boredom: is a scientific study of the subjective experiences of animals possible?. Advances in Animal Welfare Science 1984, 115-154. Martinus Nijhoff, Boston, MA. M.W. Fox, L.D. Mickley (Eds.).
104. Wemelsfelder F., Haskell M., Mendl M.T., Calvert S., Lawrence A.B. Diversity in behaviour during novel object tests is reduced in pigs housed in substrate-impoverished conditions. Anim. Behav. 2000, 60:285-394.
105. Widowski T.M., Curtis S.E. The influence of straw, cloth tassel, or both on the prepartum behavior of sows. Appl. Anim. Behav. Sci. 1990, 27:53-71.
106. Will B., Galani R., Kelche C., Rosenzweig M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog. Neurobiol. 2004, 72:167-182.
107. Wood-Gush D.G.M., Vestergaard K. The seeking of novelty and its relation to play. Anim. Behav. 1991, 42:599-606.
108. Worobec E.K., Duncan I.J.H., Widowski T.M. The effects of weaning at 7, 14 and 28 days on piglet behaviour. Appl. Anim. Behav. Sci. 1999, 62:173-182.
109. Würbel H., Garner J.P. Refinement of rodent research through environmental enrichment and systematic randomization. NC3Rs 2007, 9:1-9.
110. Yeates J.W., Main D.C.J. Assessment of positive welfare: a review. Vet. J. 2008, 175:293-300.
111. Zonderland J.J., Wolthuis-Fillerup M., van Reenen C.R., Bracke M.B.M., Kemp B., den Hartog L.A., Spoolder H.A.M. Prevention and treatment of tail biting in weaned pigs. Appl. Anim. Behav. Sci. 2008, 110:269-281.
112. Zoric M., Nilsson E., Mattsson S., Lundeheim N., Wallgren P. Abrasions and lameness in piglets born in different farrowing systems with different types of floor. Acta Vet. Scand. 2008, 50(37). Electronic publication, 9 pages.