A place to hide in the home-cage decreases yolk androgen levels and offspring emotional reactivity in Japanese quail

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Guesdon, Vanessa ^a,d,e,f   Bertin, Aline ^b,d,e,f   Houdelier, Cécilia ^a   Lumineau, Sophie ^a   Formanek, Laureline ^a   Kotrschal, Kurt ^b   Möstl, Erich ^c   Richard Yris, Marie Annick ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^d UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^e UNIVERSITÉ DE TOURS   (France)

^f IFCE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROSTENEDIONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL HOUSING; ARTICLE; CAGE; CONTROLLED STUDY; COPING BEHAVIOR; EGG LAYING; EGG YOLK; EMOTIONALITY; ENVIRONMENTAL FACTOR; EXPLORATORY BEHAVIOR; FEMALE; GROWTH RATE; NONHUMAN; PROGENY; QUAIL; SOCIAL BEHAVIOR; STRESS; ANIMAL; ANIMAL BEHAVIOR; COTURNIX; CROWDING; ECOSYSTEM; EMOTION; ENVIRONMENT; METABOLISM; SOCIAL ENVIRONMENT; TERRITORIALITY;

ANIMALIA; AVES; COTURNIX JAPONICA; PHASIANIDAE;

ANDROGENS; ANDROSTENEDIONE; ANIMALS; BEHAVIOR, ANIMAL; COTURNIX; CROWDING; ECOSYSTEM; EGG YOLK; EMOTIONS; ENVIRONMENT; FEMALE; SOCIAL ENVIRONMENT; TERRITORIALITY; TESTOSTERONE;

EID: 80053304001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023941     Document Type: Article

References (77)

1. Scherer KR, (1999) Appraisal theory. In: Dalgleish T, Power M, editors. Handbook of Cognition and Emotion Chichester John Wiley and Sons pp. 637-663 In:.
2. Weinberg J, Levine S, (1980) Psychology of coping in animals: the effect of predictability. In: Levine S, Ursin H, editors. Coping and Health New-York and London Plenum Press pp. 39-59 In:.
3. Weiss JM, (1972) Psychological factors in stress and disease. Scienti Am 226: 104-113.
4. Bassett L, Buchanan-Smith HM, (2007) Effect of predictability on the welfare of captive animals. Appl Anim Behav Sci 102: 223-245.
5. Puppe B, Ernst K, Schön PC, Manteuffel G, (2007) Cognitive enrichment affects behavioural reactivity in domestic pigs. Appl Anim Behav Sci 105: 75-86.
6. Greiveldinger L, Veissier I, Boissy A, (2009) Behavioural and physiological responses of lambs to controllable vs. uncontrollable aversive events. Psychoneuroendocrinol 34: 805-814.
7. Schwabl H, (1996) Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276: 157-263.
8. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising CM, (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav 29: 329-352.
9. Schwabl H, (1997) The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84: 406-408.
10. Groothuis TGG, Schwabl H, (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in Black-Headed Gull eggs. Funct Ecol 16: 281-289.
11. Mazuc J, Bonneaud C, Chastel O, Sorci G, (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 12: 1084-1090.
12. Guibert F, Richard-Yris MA, Lumineau S, Kotrschal K, Guemene D, et al. (2010) Social instability in laying quail: consequences on yolk steroids and offspring's phenotype. PLoS ONE 5 (11): e14069 doi:10.1371/journal.pone.0014069.
13. Müller W, Eising CM, Dijkstra C, Groothuis TGG, (2002) Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc R Soc B 269: 2249-2256.
14. Verboven N, Monaghan P, Evans DM, Schwabl H, Evans N, et al. (2003) Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc R Soc B 270: 2223-2232.
15. Guibert F, Richard-Yris MA, Lumineau S, Kotrschal K, Bertin A, et al. (2011) Unpredictable mild stressors on laying females influence the composition of Japanese quail eggs and offspring's phenotype. Appl Anim Behav Sci 132: 51-60.
16. Schwabl H, (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci U S A 90: 11446-11450.
17. Eising CM, Eikenaar C, Schwabl H, Groothuis TGG, (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc B 268: 839-846.
18. Eising CM, Muller W, Groothuis TGG, (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2: 20-22.
19. Eising CM, Groothuis TGG, (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66: 1027-1034.
20. Pilz KM, Smith HG, (2004) Egg yolk androgen levels increase with breeding density in the European Starling, Sturnus vulgaris. Funct Ecol 18: 58-66.
21. Rubolini D, Romano M, Boncoraglio G, Ferrari RP, Martinelli R, et al. (2005) Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Horm Behav 47: 592-605.
22. Tobler M, Sandell MI, (2007) Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. Horm Behav 52: 640-645.
23. Bruggeman V, Van As P, Decuypere E, (2002) Developmental endocrinology of the reproductive axis in the chicken embryo. Comp Biochem Physiol Part A 131: 839-846.
24. von Engelhardt N, Henriksen R, Groothuis TGG, (2009) Steroids in chicken egg yolk: Metabolism and uptake during early embryonic development. Gen Comp Endocrinol 163: 175-183.
25. Andersson S, Uller T, Lohmus M, Sundstrom F, (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17: 501-505.
26. Daisley JN, Bromundt V, Mostl E, Kotrschal K, (2005) Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. Horm Behav 47: 185-194.
27. Okuliarova M, Kostal L, Zeman M, (2006) Increased testosterone in egg differentially influences behaviour of Japanese quail during ontogeny. In: Yahav S, Tzschentke B, editors. New insights into fundamental physiology an perinatal adaptation of domestic fowl United Kingdom Nottingham University Press pp. 173-180.
28. Bertin A, Richard-Yris MA, Möstl E, Lickliter R, (2009) Increased yolk testosterone facilitates prenatal perceptual learning in Northern bobwhite quail (Colinus virginianus). Horm Behav 56: 416-422.
29. Hegyi G, Schwabl H, (2010) Do different yolk androgens exert similar effects on the morphology or behaviour of Japanese quail hatchlings Coturnix japonica? J Avian Biol 41: 258-265.
30. Gil D, Faure JM, (2007) Correlated response in yolk testosterone levels following divergent genetic selection for social behaviour in Japanese quail. J Exp Zool Part A 307: 91-94.
31. Bertin A, Richard-Yris MA, Houdelier C, Richard S, Lumineau S, et al. (2009) Divergent selection for inherent fearfulness leads to divergent yolk steroid levels in quail. Behav 146: 757-770.
32. Bertin A, Richard-Yris MA, Houdelier C, Lumineau S, Möstl E, et al. (2008) Habituation to humans affects yolk steroid levels and offspring phenotype in quail. Horm Behav 54: 396-402.
33. Guyomarc'h JC, Combreau O, Puigcerver M, Fontoura P, Aebischer N, (1998) Coturnix coturnix Quail. BWP Update vol. 2 Oxford Oxford University Press pp. 27-46.
34. Aubrais O, Hemon Y, Guyomarc'h JC, (1986) Habitat and use of space in the common quail (Coturnix coturnix corturnix) at the onset of the breeding period. Gibier Faune Sauvage 3: 317-342.
35. Gil D, Heim C, Bulmer E, Rocha M, Puerta M, et al. (2004) Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. J Exp Biol 207: 2215-2220.
36. Gil D, Graves J, Hazon N, Wells A, (1999) Male Attractiveness and Differential Testosterone Investment in Zebra Finch Eggs. Science 286: 126-128.
37. Lipar JL, Ketterson ED, Nolan V, Castro JM, (1999) Egg yolk layers vary in the concentration of steroid hormones in two avian species. Gen Comp Endocrinol 115: 220-227.
38. Möstl E, Spendier H, Kotrschal K, (2001) Concentration of immunoreactive progesterone and androgens in the yolk of hen's egg (Gallus domesticus). Wien Tierärztl Mschr 88: 62-65.
39. Jones RB, (1996) Fear and adaptability in poultry: insights, implications and imperatives. World Poult Sci 52: 133-174.
40. North MO, (1984) Commercial chicken production manual Nesport, Connecticut, USA AVI publishing.
41. Hackl R, Bromundt V, Daisley J, Kotrschal K, Möstl E, (2003) Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J Comp Physiol B 173: 327-331.
42. Palme R, Möstl E, (1993) Biotin-streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. pp. 111-117 Proc 5th Symp. Analys Steroids: Szombathely.
43. Hirschenhauser K, Mostl E, Kotrschal K, (1999) Seasonal patterns of sex steroids determined from feces in different social categories of greylag geese (Anser anser). Gen Comp Endocrinol 114: 67-79.
44. Mills AD, Marche M, Faure JM, (1987) Extraneous egg shell calcification as a measure of stress in poultry. Br Poult Sci 28: 177-181.
45. Odabasi AZ, Miles RD, Balaban MO, Portier KM, (2007) Changes in brown eggshell color as the hen ages. Poult Sci 86: 356-363.
46. Jones RB, (1986) The tonic immobility reaction of the domestic fowl: A review. World Poult Sci J 42: 82-97.
47. Jones RB, Mills AD, Faure JM, (1991) Genetic end experimental manipulation of fear related behavior in Japaneses quail chicks (Coturnix coturnix japonica). J Comp Psychol 105: 15-24.
48. Launay F, (1993) Conséquences comportementales et physiologiques de sélections pour l'émotivité et l'attraction sociale chez la caille Japonaise (Coturnix coturnix japonica). PhD. Thesis University of Rennes 1, France.
49. Launay F, Mills AD, Faure JM, Williams JB, (1993) Effects of CRF on isolated japanese quails selected for fearfulness and for sociability. Physiol Behav 54: 111-118.
50. Saint-Dizier H, Leterrier C, Lévy F, Richard S, (2008) Selection for tonic immobility duration does affect the response to novelty in quail. Appl Anim Behav Sci 112: 297-306.
51. Okuliarova M, Sarnikova B, Rettenbacher S, Skrobanek P, Zeman M, (2010) Yolk testosterone and corticosterone in hierarchical follicles and laid eggs of Japanese quail exposed to long-term restraint stress. Gen Comp Endocrinol 165: 91-96.
52. Janczak AM, Torjesen P, Rettenbacher S, (2009) Environmental effects on steroid hormone concentrations in laying hens' eggs. Acta Agric Scand Sect A-Ani Sci 59: 80-84.
53. Nätt D, Lindqvist N, Stranneheim H, Lundeberg J, Torjesen PA, et al. (2009) Inheritance of Acquired Behaviour Adaptations and Brain Gene Expression in Chickens. PLoS ONE 4: e6405.
54. Navara KJ, Hill GE, Mendonca MT, (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool 78: 570-578.
55. Sockman KW, Schwabl H, (2000) Yolk androgens reduce offspring survival. Proc R Soc B 267: 1451-1456.
56. Mills AD, Launay F, Jones RB, Williams J, Faure JM, (1994) Sélection divergente sur la peur et la sociabilité chez la caille japonaise Coturnix japonica: réponses et conséquences. In: Picard M, Porter R, Signoret JP, editors. Comportement et bien-être animal Versailles INRA éditions pp. 127-139.
57. Archer J, (1976) The organization of aggression and fear in vertebrates. In: Bateson PPG, Klopfer PH, editors. Perspectives in Ethology New York Plenium Publishing Corporation pp. 231-298.
58. Mills AD, Faure JM, (1986) The estimation of fear in domestic quail: correlations between various methods and measures. Biol Behav 11: 235-243.
59. Faure JM, Jones RB, Bessei W, (1983) Fear and social motivation as factor in open field behaviour of the domestic chick. A theoretical consideration. Biol Behav 8: 103-116.
60. Mills AD, Jones RB, Faure JM, Williams JB, (1993) Responses to isolation in Japanese-quail genetically selected for high or low sociality. Physiol Behav 53: 183-189.
61. Koolhass JM, Korte SM, de Boer SF, Van der Vegt BJ, Van Reenen CG, et al. (1999) Coping styles in animals: current status in behavior and a stress-physiology. Neurosci Biobehav Rev 23: 925-935.
62. Okuliarova M, Skrobanek P, Zeman M, (2007) Effect of increasing yolk testosterone levels on early behaviour in Japanese quail hatchlings. Acta Vet Brno 76: 325-331.
63. Groothuis TGG, Schwabl H, (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc B 363: 1647-1661.
64. Smiseth PT, Scott MP, Andrews C, (2011) Hormonal regulation of offspring begging and mediation of parent-offspring conflict. Anim Behav 81: 507-517.
65. Henriksen R, Rettenbacher S, Groothuis TGG, (2011) Prenatal stress in birds: Pathways, effects, function and perspectives. Neurosci Biobehav R 37: 1484-1501.
66. Hayward LS, Wingfield JC, (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen comp Endocr 135: 365-371.
67. Rettenbacher S, Mostl E, Grothuis TGG, (2005) Corticosterone in chicken eggs. Ann N Y Acad Sci 1046: 193-203.
68. Love OP, Williams TD, (2011) Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype. J Evolution Biol 24: 1497-1504.
69. Love OP, Wynne-Edwards KE, Bond L, Williams TD, (2008) Determinants of within- and among-clutch variation in yolk corticosterone in the European starling. Horm Behav 53: 104-111.
70. Saino N, Romano M, Ferrari RP, Martinelli R, Moller AP, (2005) Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J Exp Zoolog A Comp Exp Biol 303: 998-1006.
71. Janczak AM, Torjesen P, Palme R, Bakken M, (2007) Effects of stress in hens on the behaviour of their offspring. Appl Anim Behav Sci 107: 66-77.
72. Calandreau L, Bertin A, Boissy A, Arnould C, Constantin P, et al. (2011) Effect of one week of stress on emotional reactivity and learning and memory performances in Japanese quail. Behav Brain Res 217: 104-110.
73. Rettenbacher S, Möstl E, Groothuis TGG, (2009) Gestagens and glucocorticoids in chicken eggs. Gen Comp Endocrinol 164: 125-129.
74. Gil D, (2003) Golden eggs: Maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50: 281-294.
75. Mason G, Clubb R, Latham N, Vickery S, (2007) Why and how we use environmental enrichment to tackle stereotypic behaviour? Appl Anim Behav Sci 102: 163-188.
76. Young RJ, (2003) Environmental Enrichment for Captive Animals Oxford Blackwell Publishing.
77. Wells DL, (2009) Sensory stimulation as environmental enrichment for captive animals: a review. Appl Anim Behav Sci 118: 1-11.