Spatial learning in pigs: Effects of environmental enrichment and individual characteristics on behaviour and performance

Animal Cognition

Volumn 12, Issue 2, 2009, Pages 303-315

  Jansen, Jarno ^a,b   Bolhuis, J Elizabeth ^a   Schouten, Willem G P ^a   Spruijt, Berry M ^a,c   Wiegant, Victor M ^d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Behavioural style; Environmental enrichment; Exploration; Social reinstatement; Spatial learning

Indexed keywords

ADAPTIVE BEHAVIOR; ANIMAL; ANIMAL HOUSING; ARTICLE; BEHAVIOR; COMPARATIVE STUDY; DISCRIMINATION LEARNING; ENVIRONMENT; EXPLORATORY BEHAVIOR; MAZE TEST; PROBLEM SOLVING; REWARD; SOCIAL BEHAVIOR; SWINE;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; DISCRIMINATION LEARNING; ENVIRONMENT; EXPLORATORY BEHAVIOR; HOUSING, ANIMAL; MAZE LEARNING; PROBLEM SOLVING; REWARD; SOCIAL BEHAVIOR; SPATIAL BEHAVIOR; SUS SCROFA;

ANIMALIA; SUIDAE;

EID: 67349174253     PISSN: 14359448     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10071-008-0191-y     Document Type: Article

References (69)

1. VE Beattie NE O'Connell DJ Kilpatrick BW Moss 2000 Influence of environmental enrichment on welfare-related behavioural and physiological parameters in growing pigs Anim Sci 70 443 450
2. RF Benus 2001 Coping in female mice from lines bidirectionally selected for male aggression Behav 138 997 1008 10.1163/156853901753286533
3. RF Benus B Bohus JM Koolhaas GA Van Oortmerssen 1991 Behavioural differences between artificially selected aggressive and non-aggressive mice: response to apomorphine Behav Brain Res 43 203 208 10.1016/S0166-4328(05)80072-5
4. B Bindu PA Alladi BM Mansooralikhan BN Srikumar TR Raju BM Kutty 2007 Short-term exposure to an enriched environment enhances dendritic branching but not brain-derived neurotrophic factor expression in the hippocampus of rats with ventral subicular lesions Neuroscience 144 412 423 10.1016/j.neuroscience.2006. 09.057
5. Bolhuis JE (2004) Personalities in pigs : individual characteristics and coping with environmental challenges. Ph.D. thesis, Wageningen University, The Netherlands, pp 176
6. JE Bolhuis HK Parmentier WGP Schouten JW Schrama VM Wiegant 2003 Effects of housing and individual coping characteristics on immune responses of pigs Physiol Behav 79 289 296 10.1016/S0031-9384(03)00090-8
7. JE Bolhuis WGP Schouten JA De Leeuw JW Schrama VM Wiegant 2004 Individual coping characteristics, rearing conditions, and behavioural flexibility in pigs Behav Brain Res 152 351 360 10.1016/j.bbr.2003.10.024
8. JE Bolhuis WGP Schouten JW Schrama VM Wiegant 2005 Individual coping characteristics, aggressiveness and fighting strategies in pigs Anim Behav 69 1085 1091 10.1016/j.anbehav.2004.09.013
9. JE Bolhuis WGP Schouten JW Schrama VM Wiegant 2005 Behavioural development of pigs with different coping characteristics in barren and substrate-enriched housing conditions Appl Anim Behav Sci 93 213 228 10.1016/j.applanim.2005.01.006
10. JE Bolhuis WGP Schouten JW Schrama VM Wiegant 2006 Effects of rearing and housing environment on pigs with different coping characteristics Appl Anim Behav Sci 101 68 85 10.1016/j.applanim.2006.01.001
11. Chapuis N (1987) Detour and shortcut abilities in several species of mammals. In: Ellen P, Thinus-Blanc C (eds) Cognitive processes and spatial orientation in animal and man. Nijhoff, Dordrecht, pp 97-106
12. AR Cools MA Gingras 1998 Nijmegen high and low responders to novelty: a new tool in the search after the neurobiology of drug use liability Pharmacol Biochem Behav 60 151 159 10.1016/S0091-3057(97)00586-8
13. IC De Jong ED Ekkel JA Van de Burgwal E Lambooij SM Korte MAW Ruis JM Koolhaas HJ Blokhuis 1998 Effects of strawbedding on physiological responses to stressors and behavior in growing pigs Physiol Behav 64 303 310 10.1016/S0031-9384(98)00066-3
14. IC De Jong IT Prelle JA Van de Burgwal E Lambooij SM Korte HJ Blokhuis JM Koolhaas 2000 Effects of environmental enrichment on behavioral responses to novelty, learning, and memory, and the circadian rhythm to cortisol in growing pigs Physiol Behav 68 571 578 10.1016/S0031-9384(99)00212-7
15. R Freire HW Cheng CJ Nicol 2004 Development of spatial memory in occlusion-experienced domestic chicks Anim Behav 67 141 150 10.1016/j.anbehav. 2003.03.015
16. KM Frick SM Fernandez 2003 Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice Neurobiol 24 615 626 10.1016/S0197-4580(02)00138-0
17. NA Geverink WGP Schouten G Gort VM Wiegant 2002 Individual differences in behavioral and physiological responses to restraint stress in pigs Physiol Behav 77 451 457 10.1016/S0031-9384(02)00877-6
18. NA Geverink WGP Schouten G Gort VM Wiegant 2003 Individual differences in behaviour, physiology and pathology in breeding gilts housed in groups or stalls Appl Anim Behav Sci 81 29 41 10.1016/S0168-1591(02)00253-8
19. NA Geverink MJW Heetkamp WGP Schouten VM Wiegant JW Schrama 2004 Backtest type and housing condition of pigs influence energy metabolism J Anim Sci 82 1227 1233 (Pubitemid 38572323)
20. TG Groothuis C Carere 2005 Avian personalities: characterization and epigenesis Neurosci Biobehav Rev 29 137 150 10.1016/j.neubiorev.2004.06.010
21. H Gundlach 1986 Brutfürsorge, Brutpflege, Verhaltensontogenese und Tagesperiodik beim Europäischen Wildschwein (Sus scrofa L.) Z Tierpsychol 25 955 995
22. DL Hammell DD Kratzer WJ Bramble 1975 Avoidance and maze learning in pigs J Anim Sci 40 573 579
23. M Haskell F Wemelsfelder MT Mendl S Calvert AB Lawrence 1996 The effect of substrate-enriched and substrate-impoverished environments on the diversity of behaviour in pigs Behav 133 741 761
24. S Held J Baumgartner A Kilbride RW Byrne M Mendl 2005 Foraging behaviour in domestic pigs (Sus scrofa): remembering and prioritizing food sites of different value Anim Cogn 8 114 121 10.1007/s10071-004-0242-y
25. MJC Hessing AM Hagelsø JAM Van Beek PR Wiepkema WGP Schouten R Krukow 1993 Individual behavioural characteristics in pigs Appl Anim Behav Sci 37 285 295 10.1016/0168-1591(93)90118-9
26. MJC Hessing AM Hagelsø WGP Schouten PR Wiepkema JAM Van Beek 1994 Individual behavioural and physiological strategies in pigs Physiol Behav 55 39 46 10.1016/0031-9384(94)90007-8
27. BR Ickes TM Pham LA Sanders DS Albeck AH Mohammed AC Granholm 2000 Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain Exp Neurol 164 45 52 10.1006/exnr.2000.7415
28. P Jensen 1986 Observations on the maternal behaviour of free-ranging domestic pigs Appl Anim Behav Sci 16 131 142 10.1016/0168-1591(86)90105-X
29. G Kempermann HG Kuhn FH Gage 1997 More hippocampal neurons in adult mice living in an enriched environment Nature 386 493 495 10.1038/386493a0
30. Koolhaas JM, De Boer SF, Buwalda B, Van der Vegt BJ, Carere C, Groothuis AGG (2001) How and why coping systems vary among individuals. In: Broom DM (ed) Coping with challenge. Welfare in animals including humans. Dahlem Workshop Report 87, Dahlem University Press, Berlin, pp 197-210
31. K Laughlin M Mendl 2000 Pigs shift too: foraging strategies and spatial memory in the domestic pig Anim Behav 60 403 410 10.1006/anbe.2000.1468
32. K Laughlin M Huck M Mendl 1999 Disturbance effects of environmental stimuli on pig spatial memory Appl Anim Behav Sci 64 169 180 10.1016/S0168-1591(99)00036-2
33. MG Leggio L Mandolesi F Federico F Spirito B Ricci F Gelfo L Petrosini 2005 Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat Behav Brain Res 163 78 90 10.1016/j.bbr.2005.04.009
34. KP Lewis 2000 A comparative study of primate play behaviour: Implications for the study of cognition Folia Primatol 71 417 421 10.1159/000052740
35. M Mendl HW Erhard M Haskell F Wemelsfelder AB Lawrence 1997 Experience in substrate-enriched and substrate-impoverished environments affects behaviour of pigs in a T-maze task Behav 134 643 659 (Pubitemid 127383387)
36. M Mendl K Laughlin D Hitchcock 1997 Pigs in space: spatial memory and its susceptibility to interference Anim Behav 54 1491 1508 10.1006/anbe.1997.0564
37. D Meshi MR Drew M Saxe MS Ansorge D David L Santarelli C Malapani H Moore R Hen 2006 Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment Nat Neurosci 9 729 731 10.1038/nn1696
38. MJ Morgan 1973 Effects of post-weaning environment on learning in the rat Anim Behav 21 429 442 10.1016/S0003-3472(73)80002-8
39. RC Newberry DGM Wood-Gush 1988 Development of some behaviour patterns in piglets under semi-natural conditions Anim Prod 46 103 109
40. O'Keefe J, Nadel L (1978) The Hippocampus as a Cognitive Map. Oxford University Press, New York
41. AK Olson BD Eadie C Ernst BR Christie 2006 Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways Hippocampus 16 250 260 10.1002/hipo.20157
42. IAS Olsson FH De Jonge T Schuurman FA Helmond 1999 Poor rearing conditions and social stress in pigs: repeated social challenge and the effect on behavioural and physiological responses to stressors Behav Proc 46 201 215 10.1016/S0376-6357(99)00036-4
43. V Petersen 1994 The development of feeding and investigatory behaviour in free-ranging domestic pigs during their first 18 weeks of life Appl Anim Behav Sci 42 87 98 10.1016/0168-1591(94)90149-X
44. B Poucet C Thinus-Blanc N Chapuis 1983 Route planning in cats, in relation to the visibility of the goal Anim Behav 31 594 599 10.1016/S0003-3472(83)80083-9
45. L Regolin G Vallortigara M Zanforlin 1994 Perceptual and motivational aspects of detour behaviour in young chicks Anim Behav 47 123 131 10.1006/anbe.1994.1014
46. L Regolin G Vallortigara M Zanforlin 1995 Object and spatial representations in detour problems by chicks Anim Behav 49 195 199 10.1016/0003-3472(95)80167-7
47. Renner MJ, Rozenzweig MR (1987) Enriched and impoverished environments. Effects on brain and behavior. Spinger, New York
48. MR Rosenzweig EL Bennett 1996 Psychobiology of plasticity: effects of training and experience on brain and behavior Behav Brain Res 78 57 65 10.1016/0166-4328(95)00216-2
49. MAW Ruis JHA Te Brake B Engel WG Buist HJ Blokhuis JM Koolhaas 2001 Adaptation to social isolation - acute and long-term stress responses of growing gilts with different coping characteristics Physiol Behav 73 541 551 10.1016/S0031-9384(01)00548-0
50. MAW Ruis JHA Te Brake JA Van de Burgwal IC De Jong HJ Blokhuis JM Koolhaas 2000 Personalities in female domesticated pigs: behavioral and physiological indications Appl Anim Behav Sci 66 31 47 10.1016/S0168-1591(99) 00070-2 (Pubitemid 30061494)
51. L Schley TJ Roper 2003 Diet of wild boar Sus scrofa in Western Europe, with particular reference to consumption of agricultural crops Mammal Rev 33 43 56 10.1046/j.1365-2907.2003.00010.x
52. NA Schmajuk AD Thieme HT Blair 1993 Maps, routes, and the hippocampus: a neural network approach Hippocampus 3 387 400 10.1002/hipo.450030312 (Pubitemid 23231471)
53. Schouten WGP (1986) Rearing conditions and behaviour in pigs. Ph.D. Thesis. Agricultural University, Wageningen, pp 151
54. NC Schrijver HI Bahr IC Weiss H Würbel 2002 Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats Pharmacol Biochem Behav 73 209 224 10.1016/S0091-3057(02)00790-6
55. IA Sneddon VE Beattie L Dunne W Neil 2000 The effect of environmental enrichment on learning in pigs Anim Welf 9 373 383
56. JM Siegford G Rucker AJ Zanella 2008 Effects of pre-weaning exposure to a maze on stress responses in pigs at weaning and on subsequent performance in spatial and fear-related tests Appl Anim Behav Sci 110 189 202 10.1016/j.applanim.2007.03.022
57. M Spinka RC Newberry M Bekoff 2001 Mammalian play: training for the unexpected Q Rev Biol 76 141 168 (Pubitemid 32494761)
58. EC Tolman 1948 Cognitive maps in rats and men Psychol Rev 55 189 208
59. G Vallortigara M Cailotto M Zanforlin 1990 Sex differences in social reinstatement motivation of the domestic chick (Gallus gallus) revealed by runway tests with social and nonsocial reinforcement J Comp Psychol 104 361 367
60. Van der Beek EM, Bolhuis JE, Karman AG, Van Eerdenburg FJCM, Wiegant VM (2000) Housing condition affects the correlation between volume of the dentate gyrus and the cortisol response to stress in pigs. Abstracts Society for Neuroscience, vol 26, part 1. 30th Annual Meeting, New Orleans (abstract)
61. MEM Verbeek PJ Drent PR Wiepkema 1994 Consistent individual differences in early exploratory behaviour and dominance in juvenile male great tits Anim Behav 48 1113 1121 10.1006/anbe.1994.1344
62. F Wemelsfelder M Haskell MT Mendl S Calvert AB Lawrence 2000 Diversity of behaviour during novel object tests is reduced in pigs housed in substrate-impoverished conditions Anim Behav 60 385 394 10.1006/anbe.2000.1466
63. Wickert DA, Barr GR (1966) Studies of learning ability in young pigs. J Anim Sci 25:1280
64. BM Williams Y Luo C Ward K Redd R Gibson SA Kuczaj JG McCoy 2001 Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity Physiol Behav 73 649 658 10.1016/S0031-9384(01)00543-1
65. DS Wilson 1998 Adaptive individual differences within single populations Philos Trans R Soc Lond B 353 199 205 (Pubitemid 28153919)
66. CDL Wynne B Leguet 2004 Detour behavior in the Quokka (Setonix brachyurus) Behav Proc 67 281 286 10.1016/j.beproc.2004.04.007
67. D Young PA Lawlor P Leone M Dragunow MJ During 1999 Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective Nat Med 5 448 453 10.1038/7449
68. A Zimmermann M Stauffacher W Langhans H Wurbel 2001 Enrichment-dependent differences in novelty exploration in rats can be explained by habituation Behav Brain Res 121 11 20 10.1016/S0166-4328(00)00377-6
69. P Zucca F Antonelli G Vallortigara 2005 Detour behaviour in three species of birds: quails (Coturnix sp.), herring gulls (Larus cachinnans) and canaries (Serinus canaria) Anim Cogn 8 122 128 10.1007/s10071-004-0243-x