全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Maternal Diet Influences Offspring Feeding Behavior and Fearfulness in the Precocial Chicken

DOI: 10.1371/journal.pone.0077583

Full-Text   Cite this paper   Add to My Lib

Abstract:

Background In chicken, oils in the maternal diet confer a specific scent to the yolk. Embryos are known to perceive and memorize chemosensory signals of the surrounding environment; however, the potential impact of the maternal diet has not previously been investigated. In the present study, we hypothesized that chicken embryos memorize the chemical signals of the maternal diet and that this perceptual learning may orient subsequent feeding behavior of the hatchlings. Methodology/Principal Findings Laying hens were fed standard food enriched with 2% menhaden oil (MH group) or 2% soybean oil (controls). The scent of menhaden was significantly more detected in MH egg yolks than in control yolks by a human panel. We analyzed the development and behavior of offspring towards different types of food, bearing or not bearing the menhaden scent. When chicks were exposed to a 3-min choice test between the familiar food bearing the menhaden scent and the familiar food without menhaden, no effect of treatment was observed. In a 3-min choice test with unfamiliar food (mashed cereals) MH chicks showed a clear positive orientation toward the unfamiliar food bearing the menhaden scent. By contrast, control chicks showed a preference for the non-odorized unfamiliar food. MH chicks expressed higher emotional reactivity level than control chicks as expressed by food neophobia and longer immobility in a restraint test. Conclusion/Significance Chicks exposed in ovo to menhaden oil via the maternal diet preferentially oriented their feeding behavior towards food containing menhaden oil, but only when the food was unfamiliar. We propose that oil in the maternal diet engenders maternal effects and contributes to the development of behavioral phenotype in the offspring. In ovo chemosensory learning may have evolved to prepare precocial offspring for their environment. This suggests a common principle of embryonic chemosensory learning across vertebrate taxa.

References

[1]  Basso A, Fernández A, Althabe O, Sabini G, Piriz H, et al. (1977) Passage of mannitol from mother to amniotic fluid and fetus. Obstet Gynecol 49: 628–631.
[2]  Nolte DL, Provenza FD, Callan R, Panter KE (1992) Garlic in the ovine fetal environment. Physiol Behav 52: 1091–1093.
[3]  Nolte DL, Mason JR (1995) Maternal ingestion of ortho-aminoacetophenone during gestation affects intake by offspring. Physiol Behav 58: 925–928.
[4]  Coureaud G, Schaal B, Hudson R, Orgeur P, Coudert P (2002) Transnatal olfactory continuity in the rabbit: Behavioral evidence and short-term consequence of its disruption. Dev Psychobiol 40: 372–390.
[5]  Simitzis PE, Deligeorgis SG, Bizelis JA, Fegeros K (2008) Feeding preferences in lambs influenced by prenatal flavour exposure. Physiol Behav 93: 529–536.
[6]  Hepper PG, Wells DL (2006) Perinatal Olfactory Learning in the Domestic Dog. Chem Senses 31: 207–212.
[7]  Todrank J, Heth G, Restrepo D (2011) Effects of in Utero Odorant Exposure on Neuroanatomical Development of the Olfactory Bulb and Odour Preferences. Proc R Soc B 278: 1949–1955.
[8]  Hepper PG (n.d.) Adaptive fetal learning: prenatal exposure to garlic affects postnatal preferences. Anim Behav 36: 935–936.
[9]  Mennella JA, Johnson A, Beauchamp GK (1995) Garlic ingestion by pregnant women alters the odor of amniotic fluid. Chem Senses 20: 207–209.
[10]  Schaal B, Marlier L, Soussignan R (2000) Human Foetuses Learn Odours from their Pregnant Mother’s Diet. Chem Senses 25: 729–737.
[11]  Mennella JA, Jagnow CP, Beauchamp GK (2001) Prenatal and Postnatal Flavor Learning by Human Infants. Pediatrics 107: e88–e88.
[12]  Beauchamp GK, Mennella JA (2009) Early Flavor Learning and Its Impact on Later Feeding Behavior. J Pediatr Gastr Nutr 48: S25–S30.
[13]  Mizuno K, Ueda A (2004) Antenatal olfactory learning influences infant feeding. Early Hum Dev 76: 83–90.
[14]  Isingrini M, Lenoir A, Jaisson P (1985) Preimaginal learning as a basis of colony-brood recognition in the ant Cataglyphis cursor. P Natl Acad Sci 82: 8545.
[15]  Caubet Y, Jaisson P, Lenoir A (1992) Preimaginal induction of adult behaviour in insects. Q J Exp Psychol- B 44: 165–178.
[16]  Sneddon H, Hepper PG, Manolis C (2001) Embryonic chemosensory learning in the saltwater crocodile Crocodylus porosus. In: Crocodilian Biology and Evolution Surrey Beatty, Chipping Norton, Australia: 378–382.
[17]  Brannon EL (1972) Mechanisms controlling migration of sockeye salmon fry University of Washington.
[18]  Hepper PG, Waldman B (1992) Embryonic olfactory learning in frogs. Q J Exp Psychol- B 44: 179–197.
[19]  Guibé M, Boal JG, Dickel L (2010) Early exposure to odors changes later visual prey preferences in cuttlefish. Dev Psychobiol 52: 833–837.
[20]  Hirao A, Aoyama M, Sugita S (2009) The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus. Behav Process 80: 115–120.
[21]  Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67: 169–176.
[22]  Balthazart J, Schoffeniels E (1979) Pheromones are involved in the control of sexual behaviour in birds. Naturwissenschaften 66: 55–56.
[23]  Cohen J (1981) Olfaction and parental behavior in ring dove. Biochem Syst Ecol 9: 351–354.
[24]  Cunningham SJ, Castro I, Potter MA (2009) The relative importance of olfaction and remote touch in prey detection by North Island brown kiwis. Anim Behav 78: 899–905.
[25]  Nevitt GA, Haberman K (2003) Behavioral attraction of Leach’s storm-petrels (Oceanodroma leucorhoa) to dimethyl sulfide. J Expl Biol 206: 1497–1501.
[26]  Papi F (1990) Olfactory navigation in birds. Cell Mol Life Sci 46: 352–363.
[27]  Jorge PE, Marques PAM, Phillips JB (2009) Activational effects of odours on avian navigation. P Roy Soc B-Biol Sci 277: 45–49.
[28]  Amo L, Galván I, Tomás G, Sanz JJ (2008) Predator odour recognition and avoidance in a songbird. Funct Ecol 22: 289–293.
[29]  Hagelin JC (2007) The citrus-like scent of crested auklets: reviewing the evidence for an avian olfactory ornament. J Ornithol 148: 195–201.
[30]  Sneddon H, Hadden R, Hepper P (1998) Chemosensory learning in the chicken embryo. Physiol Behav 64: 133–139.
[31]  Bertin A, Calandreau L, Arnould C, Nowak R, Levy F, et al. (2010) In Ovo Olfactory Experience Influences Post-hatch Feeding Behaviour in Young Chickens. Ethology 116: 1027–1037.
[32]  Bertin A, Calandreau L, Arnould C, Lévy F (2012) The Developmental Stage of Chicken Embryos Modulates the Impact of In Ovo Olfactory Stimulation on Food Preferences. Chem Senses 37: 253–261.
[33]  Cunningham GB, Nevitt GA (2011) Evidence for olfactory learning in procellariiform seabird chicks. J Avian Biol 42: 85–88.
[34]  Józsa R, Hollósy T, Tamás A, Tóth G, Lengvári I, et al. (2005) Pituitary adenylate cyclase activating polypeptide plays a role in olfactory memory formation in chicken. Peptides 26: 2344–2350.
[35]  Sirri F, Meluzzi A (2011) Modifying egg lipids for human health. Woodhead Publ Ser Food Sci, Tech Nutr 214: 272–288.
[36]  Plagemann I, Zelena K, Krings U, Berger RG (2011) Volatile flavours in raw egg yolk of hens fed on different diets. J Sci Food Agr 91: 2061–2065.
[37]  Gonzalez-Esquerra R, Leeson S (2000) Effect of Feeding Hens Regular or Deodorized Menhaden Oil on Production Parameters, Yolk Fatty Acid Profile, and Sensory Quality of Eggs. Poulty Sci 79: 1597–1602.
[38]  Leskanich CO, Noble RC (1997) Manipulation of the n-3 polyunsaturated fatty acid composition of avian eggs and meat. Worlds Poult Sci J 53(2) p. 155–183.
[39]  Schaal B, Orgeur P (1992) Olfaction in utero: Can the rodent model be generalized? Q J Exp Psychol- B 44: 245–278.
[40]  Fountain ED, Mao J, Whyte JJ, Mueller KE, Ellersieck MR, et al. (2008) Effects of Diets Enriched in Omega-3 and Omega-6 Polyunsaturated Fatty Acids on Offspring Sex-Ratio and Maternal Behavior in Mice. Biol Reprod 78: 211–217.
[41]  Vinot N, Jouin M, Lhomme-Duchadeuil A, Guesnet P, Alessandri J-M, et al. (2011) Omega-3 Fatty Acids from Fish Oil Lower Anxiety, Improve Cognitive Functions and Reduce Spontaneous Locomotor Activity in a Non-Human Primate. PLoS One 6: e20491.
[42]  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. Behaviour 146: 757–770.
[43]  Bertin A, Richard-Yris M-A, Houdelier C, Lumineau S, M?stl E, et al. (2008) Habituation to humans affects yolk steroid levels and offspring phenotype in quail. Horm Behav 54: 396–402.
[44]  Jones RB (1987) Food Neophobia and Olfaction in Domestic Chicks. Bird Behav 7: 78–81.
[45]  Sauveur B, Reviers M de (1988) Reproduction des volailles et production d’oeufs. Editions Quae. 480 p.
[46]  Elswyk ME, Dawson PL, Sams A (1995) Dietary Menhaden Oil Influences Sensory Characteristics and Headspace Volatiles of Shell Eggs. J Food Sci 60: 85–89.
[47]  Turro I, Porter RH, Picard M (1994) Olfactory cues mediate food selection by young chicks. Physiol Behav 55: 761–767.
[48]  Marples N, Kelly D (1999) Neophobia and dietary conservatism: two distinct processes? Evol Eco 13: 641–653.
[49]  Lecuelle S, Bouvarel I, Chagneau A-M, Lescoat P, Laviron F, et al. (2010) Feeding behaviour in turkeys with a change-over from crumbs to pellets. Appl Anim Behav Sci 125: 132–142.
[50]  Siddall EC, Marples NM (2008) Better to be bimodal: the interaction of color and odor on learning and memory. Behav Ecol 19: 425–432.
[51]  Shafey TM, Dingle JG, McDonald MW (1992) Comparison between wheat, triticale, rye, soyabean oil and strain of laying bird on the production, and cholesterol and fatty acid contents of eggs. Brit Poultry Sci 33: 339–346.
[52]  Van Elswyk ME (1997) others (1997) Comparison of n-3 fatty acid sources in laying hen rations for improvement of whole egg nutritional quality: a review. Brit J Nutr 78: S61–S69.
[53]  Marples NM, Roper TJ (1996) Effects of novel colour and smell on the response of naive chicks towards food and water. Anim Behav 51: 1417–1424.
[54]  Wauters A, Richard-Yris M, Talec N (2002) Maternal Influences on Feeding and General Activity in Domestic Chicks. Ethology 108: 529–540.
[55]  Hale C, Green L (1988) Effects of early ingestional experiences on the acquisition of appropriate food selection by young chicks. Anim Behav 36: 211–224.
[56]  Jones BR (2000) Presence of a Familiar Odourant Accelerates Acceptance of Novel Food in Domestic Chicks. Int J Comp Psy 13.
[57]  Burghardt GM (1971) Chemical-Cue Preferences of Newborn Snakes: Influence of Prenatal Maternal Experience. Science 171: 921–923.
[58]  Yo T, Siegel PB, Faure JM, Picard M (1998) Self-Selection of Dietary Protein and Energy by Broilers Grown Under a Tropical Climate: Adaptation When Exposed to Choice Feeding at Different Ages. Poult Sci 77: 502–508.
[59]  Yo T, Siegel P, Guerin H, Picard M (1997) Self-selection of dietary protein and energy by broilers grown under a tropical climate: effect of feed particle size on the feed choice. Poult Sci 76: 1467–1473.
[60]  Bouvarel I, Tesseraud S, Leterrier C (2010) L’ingestion chez le poulet de chair: n’oublions pas les régulations à court terme. Prod Anim 23: 391.
[61]  Groothuis TG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos T R Soc B 363: 1647–1661.
[62]  Ho DH, Reed WL, Burggren WW (2011) Egg yolk environment differentially influences physiological and morphological development of broiler and layer chicken embryos. J Exp Biol 214: 619–628.
[63]  Gallup GG (1977) Tonic immobility: The role of fear and predation. Psychol Rec 27: 41–61.
[64]  Jones RB (1996) Fear and adaptability in poultry: Insights, implications and imperative. Worlds Poult Sci J 52: 131–174.
[65]  Jones RB, Faure JM (1981) Sex and strain comparisons of tonic immobility (“Righting time”) in the domestic fowl and the effects of various methods of induction. Behav Process 6: 47–55.
[66]  Campo JL, Carnicer C (1993) Realized Heritability of Tonic Immobility in White Leghorn Hens: A Replicated Single Generation Test. Poult Sci 72: 2193–2199.
[67]  Antruejo A, Azcona JO, Garcia PT, Gallinger C, Rosmini M, et al. (2011) Omega-3 enriched egg production: the effect of α -linolenic ω -3 fatty acid sources on laying hen performance and yolk lipid content and fatty acid composition. Bri Poultry Sci 52: 750–760.
[68]  Tannenbaum BM, Brindley DN, Tannenbaum GS, Dallman MF, McArthur MD, et al. (1997) High-Fat Feeding Alters Both Basal and Stress-Induced Hypothalamic-Pituitary-Adrenal Activity in the Rat. Am J Physiol Endocrinol Metab 273: E1168–E1177.
[69]  Hamazaki T, Itomura M, Sawazaki S, Nagao Y (2000) Anti-stress effects of DHA. BioFactors 13: 41–45.
[70]  Sol D, Griffin AS, Bartomeus I, Boyce H (2011) Exploring or Avoiding Novel Food Resources? The Novelty Conflict in an Invasive Bird. PLoS One 6: e19535.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133