The Energetics of Parenting in an Avian Model: Hormonal and Neurochemical Regulation of Parental Provisioning in Doves

Neurobiology of the Parental Brain

Volumn , Issue , 2008, Pages 269-291

  Buntin, John D ^a   Strader, April D ^b   Ramakrishnan, Selvakumar ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882828054     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374285-8.00017-2     Document Type: Chapter

References (113)

1. Albertson B.D., Siekiewicz M.L., Kimball D., Munabi A.K., Cassorla F., Loriaux D.L. New evidence for a direct effect of prolactinon rat adrenal steroidogenesis. Endocr. Res. 1987, 13:317-333.
2. Badyaev A.V., Hill G.E. Paternal care as a conditional strategy: Distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch. Behav. Ecol. 2002, 13:591-597.
3. Badyaev A.V., Duckworth R.A. Evolution of plasticity in hormonally integrated parental tactics. Functional Avian Endocrinology 2005, 375-386. Narosa Publishing House, New Delhi. A. Dawson, P.J. Sharp (Eds.).
4. Bates R.W., Miller R.A., Garrison M.M. Evidence in the hypophysectomized pigeon of a synergism among prolactin, growth hormone, thyroxine, and prednisone upon weight of the body digestive tract, kidney, and fat stores. Endocrinology 1962, 71:260-345.
5. Bengtsson H., Ryden O. Parental feeding rate in relation to begging behavior in asynchronously hatched broods of the great tit. Parus major. Behav. Ecol. Sociobiol. 1983, 12:243-251.
6. Boswell T., Li Q., Takeuchi S. Neurons expressing neuropeptide Y mRNA in the infundibular hypothalamus of Japanese quail are activated by fasting and co-express agouti-related protein mRNA. Brain Res. Mol. Brain Res. 2002, 100:31-42.
7. Breuner C.W., Orchinik M. Seasonal regulation of membrane and intracellular corticosterone receptors in the house sparrow brain. J. Neuroendocrinol. 2001, 13:412-420.
8. Brisbin I.L. Bioenergetics of the breeding cycle of the ring dove. Auk 1969, 86:54-74.
9. Brown J.L., Vleck C.M. Prolactin and helping in birds: has natural selection strengthened helping behavior?. Behav. Ecol. 1998, 9:541-545.
10. Buntin J.D. Time course and response specificity of prolactin-induced hyperphagia in ring doves. Physiol. Behav. 1989, 45:903-909.
11. Buntin J.D. Neural and hormonal control of parental behavior in birds. Adv. Study Behav. 1996, 25:161-213.
12. Buntin J.D., Tesch D. Effects of intracranial prolactin administration on maintenance of incubation readiness, ingestive behavior, and gonadal condition in ring doves. Horm. Behav. 1985, 19:188-203.
13. Buntin J.D., Ruzycki E. Characteri-zation of prolactin binding sites in the brain of the ring dove (Streptopelia risoria). Gen. Comp. Endocrinol. 1987, 65:243-253.
14. Buntin J.D., Figge G.R. Prolactin and growth hormone stimulate food intake in ring doves. Pharmacol. Biochem. Behav. 1988, 31:533-540.
15. Buntin J.D., Walsh R.J. In vivo autoradiographic analysis of prolactin binding sites in brain and choroid plexus of the domestic ring dove. Cell Tissue Res. 1988, 251:105-109.
16. Buntin J.D., Ruzycki E., Witebsky J. Prolactin receptors in dove brain: Autoradiographic analysis of binding characteristics in discrete brain regions and accessibility to blood-borne prolactin. Neuroendocrinology 1993, 57:738-750.
17. Buntin J.D., Becker G.M., Ruzycki E. Facilitation of parental behavior in ring doves by systemic and intracranial injections of prolactin. Horm. Behav. 1991, 25:424-444.
18. Buntin J.D., Hnasko R.M., Zuzick P.H., Valentine D.L., Scammell J.G. Changes in bioactive prolactin-like activity in plasma and its relationship to incubation behavior in breeding ring doves. Gen. Comp. Endocrinol. 1996, 102:221-232.
19. Buntin L., Berghman L.R., Buntin J.D. Patterns of fos-like immunoreactivity in the brains of parent ring doves (Streptopelia risoria) given tactile and non-tactile exposure to their young. Behav. Neurosci. 2006, 120:651-664.
20. Burley N. Clutch overlap and clutch size: Alternative and complementary reproductive tactics. Am. Nat. 1980, 115:223-246.
21. Chen P., Smith M.S. Regulation of hypothalamic neuropeptide Y messenger ribonucleic acid expression during lactation:Rrole of prolactin. Endocrinology 2004, 145:823-829.
22. Criscuolo F., Bertile F., Durant J.M., Raclot T., Gabrielson G.W., Massemin S., Chastel O. Body mass and clutch size may modulate prolactin and corticosterone levels in eiders. Physiol. Biochem. Zool. 2006, 79:514-521.
23. de Greef W.J., Ooms M.P., Weber R.F.A. Plasma levels of luteinizing hormone during hyperprolactinemia: response to central administration of antagonists of corticotropin-releasing factor. Neuroendocrinology 1995, 61:19-26.
24. denBoer-Visser A.M., Dubbeldam J.L. The distribution of dopamine, substance P, vasoactive intestinal polypeptide and neuropeptide Y immunoreactivity in the brain of the collared dove, Streptopelia decaocto. J. Chem. Neuroanat. 2002, 23:1-27.
25. Drent R.H., Daan S. The prudent parent: Energetic adjustments in avian breeding. Ardea 1980, 68:225-252.
26. Eldridge J.C., Lymangrover J.R. Prolactin stimulates and potentiates adrenal ste-roid secretion in vitro. Horm. Res. 1984, 20:252-260.
27. Fechner J.H., Buntin J.D. Localization of prolactin binding sites in ring dove brain by quantitative autoradiography. Brain Res. 1989, 487:245-254.
28. Foreman K.T., Lea R.W., Buntin J.D. Changes in feeding activity, plasma LH, and testes weight in ring doves following hypothalamic injections of prolactin. J. Neuroendocrinol. 1990, 2:667-673.
29. Frith H.J. Breeding habits in the family Megapodiidae. Ibis 1956, 98:620-640.
30. Gamoke C., Moore J.C., Buntin J.D. Motivational influences underlying prolactin-induced feeding in doves (Streptopelia risoria). Behav. Neurosci. 2000, 114:963-971.
31. Garcia M.C., López M., Gualillo O., Seoane LM., Diéguez C., Senaris R.M. Hypothalamic levels of NPY, MCH, and prepro-orexin mRNA during pregnancy and lactation in the rat: Role of prolactin. FASEB J. 2003, 17:1392-1400.
32. Gittleman J.L., Thompson S.J. Energy allocation in mammalian reproduction. Am. Zool. 1988, 28:863-875.
33. Goldsmith A.R., Edwards C., Koprucu M., Silver R. Concentrations of prolactin and luteinizing hormone in plasma of doves in relation to incubation and development of the crop gland. J. Endocrinol. 1981, 103:251-256.
34. Groscolas R., Robin J.-P. Long-term fasting and re-feeding in penguins. Comp. Biochem. Physiol. A. 2001, 128:645-655.
35. Hahn T., Breininger J.F., Baskin D.G., Schwartz M.W. Coexpression of AgRP and NPY in fasting activated hypothalamic neurons. Nature Neurosci. 1998, 1:271-272.
36. Hansen E.W. Squab-induced crop growth in experienced and inexperienced ring dove (Streptopelia risoria) foster parents. J. Comp. Physiol. Psychol. 1971, 77:375-381.
37. Hnasko R.M., Buntin J.D. Functional mapping of neural sites mediating prolactin-induced hyperphagia in doves. Brain Res. 1993, 623:257-266.
38. Horseman N.D., Buntin J.D. Regulation of pigeon milk crop milk secretion and parental behaviors by prolactin. Annu. Rev. Nutr. 1995, 15:213-238.
39. Ikemoto S., Panksepp J. Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant b rain regions. Behav. Neurosci. 1996, 110:331-345.
40. Jewett D.C., Cleary J., Levine A.S., Schaal D.W., Thompson T. Effects of neuropeptide Y on food-reinforced behavior in satiated rats. Pharm. Biochem. Behav. 1992, 42:207-212.
41. Jewett D.C., Cleary J., Levine A.S., Schall D.W., Thompson T. Effects of neuropeptide Y, insulin, 2-deoxyglucose, and food deprivation on food-motivated behavior. Psychopharmacology 1995, 120:267-271.
42. Kameda Y., Miura M., Nishimaki T. Localization of neuropeptide Y mRNA and peptidein chicken hypothalamus and their alterations after food deprivation, dehydration, and castration. J. Comp. Neurol. 2001, 436:376-388.
43. Kitaysky A.S., Wingfield J.C., Piatt J.F. Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct. Ecol. 1999, 13:577-584.
44. Kitaysky A.S., Wingfield J.C., Piatt J.F. Corticosterone facilitates begging and affects resource allocation in the black-legged k-ittiwake. Behav. Ecol. 2001, 12:619-625.
45. Klinghammer E., Hess E.H. Parental feeding in ring doves (Streptopelia risoria): innate or learned?. Z. Tierpsychol. 1964, 21:338-347.
46. Koch K.A., Wingfield J:C., Buntin J.D. Glucocorticoids and parental hyperphagia in ring doves (Streptopelia risoria). Horm. Behav. 2002, 41:9-21.
47. Koch K.A., Wingfield J.C., Buntin J.D. Prolactin-induced parental hyperphagia in ring doves: Are glucocorticoids involved?. Horm. Behav. 2004, 46:498-505.
48. Kooy A., de Greef W.J., Vreeburg J.T., Hackeng W.H., Ooms M.P., Lamberts S.W., Weber R.F. Evidence for the involvement of corticotropin-releasing factor in the inhibition of gonadotropin release induced by hyperprolactinemia. Neuroendocrinology 1990, 51:261-266.
49. Kuenzel W.J., McMurtry J. Neuro-peptide Y. Brain localization and cental effects on plasma levels in chicks. Physiol. Behav. 1988, 44:669-678.
50. Lang E.M. Flamingoes raise their young on a liquid containing blood. Experientia 1963, 19:532-533.
51. Lea R.W., Sharp P.J., Chadwick A. Daily variations in the concentration of plasma prolactin in broody bantams. Gen. Comp. Endocrinol. 1982, 48:275-284.
52. Lea R.W., Vowles D.M., Dick H.R. Factors affecting prolactin secretion during the breeding cycle of the ring dove (Streptopelia risoria) and its possible role in incubation. J. Endocrinol. 1986, 110:447-458.
53. Lea R.W., Klandorf H., Harvey S., Hall T.R. Thyroid and adrenal function in the ring dove (Streptopelia risoria) during food deprivation and a breeding cycle. Gen. Comp. Endocrinol. 1992, 86:136-146.
54. Lehrman D.S. The physiological basis of parental feeding behavior in the ring dove (Streptopelia risoria). Behaviour 1955, 7:241-286.
55. Li C., Kelly P.A., Buntin J.D. Inhibitory effects of anti-prolactin receptor antibodies on prolactin binding in brain and prolactin-induced feeding behavior in ring doves. Neuroendocrinology 1995, 61:125-135.
56. Li C., Chen P., Smith M.S. Neuro-peptide Y (NPY) neurons in the arcuate nucleus (ARH) and dorsomedial nucleus (DMH), areas activated during lactation, project to the paraventricular nucleus of the hypothalamus (PVN). Regul. Pept. 1998, 75(75):93-100.
57. Li C., Chen P., Smith M.S. Neuropeptide Y and tuberoinfundibular dopamine activities are altered during lacation: Role of pro-lactin. Endocrinology 1999, 140:118-123.
58. Lynn S.E., Breuner C.W., Wingfield J.C. Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm. Behav. 2003, 43:150-157.
59. Malabu U.H., Kilpatrick A., Ware M., Vernon R.G., Williams G. Increased neuropeptide Y concentrations in specific hypothalamic regions of lactating rats: Possible relationship to hyperphagia and adaptive changes in energy balance. Peptides 1994, 15:83-87.
60. McNeil A.M., Strader A.D., Buntin J.D. Corticosterone influences energy state and orexigenic neuropeptides in female ring doves. Horm. Behav. 2002, 41:480. (abstract).
61. Mirabella N., Esposito V., Squillacioti C., DeLuca A., Paino G. Expression of agouti-related protein (AgRP) in the hypothalamus and adrenal gland of the duck (Anas platyrhynchos). Anat. Embryol. (Berl.) 2004, 209:137-141.
62. Mondloch C. Chick hunger and begging affect parental allocation of feedings in pigeons. Anim. Behav. 1995, 49:601-613.
63. Mondloch C.J., Timberlake W. The effect of parental food supply on parental feeding and squab growth in pigeons, Columba livia. Ethology 1991, 88:236-248.
64. Morton G.J., Schwartz M.W. The NPY/AgRP neuron and energy homeostasis. Int. J. Obes. Relat. Metab. Disord. 2001, 25(suppl 5):S56-S62.
65. Mrosovsky N., Sherry D.F. Animal anorexias. Science 1980, 22:837-842.
66. Murton R.K., Isaacson A.J., Westwood N.J. The food and growth of nestling wood-pigeons in relation to the breeding season. Proc. Zool. Soc. London 1963, 141:747-781.
67. Nagra C.L., Breitenbach R.P., Meyer R.K. Influence of hormones on food intake and lipid deposition in castrated pheasants. Poultry Sci. 1963, 42:77-775.
68. O'Connell Y., McKenna T.J., Cunningham S.K. The effect of prolactin, human chorionic gonadotropin, insulin, and insulin-like growth factor 1 on adrenal steroidogenesis in isolated guinea pig adrenal cells. J. Steroid Biochem. Mol. Biol. 1994, 48:235-240.
69. O'Dwyer T.W., Buttemer W.A., Priddel D.M., Downing J.A. Prolactin, body condition, and the cost of good parenting: An interyear study in a long-lived seabird, Gould's Petrel (Pterodroma leucoptera). Funct. Ecol. 2006, 20:806-811.
70. Ottosson U., Backman J., Smith H. Begging affects parental effort in the pied flycatcher, Ficedula hypoleuca. Behav. Ecol. Sociobiol. 1997, 41:381-384.
71. Patel M.D. The physiology of the formation of "pigeon's milk". Physiol. Zool. 1936, 9:129-152.
72. Peterson C.C., Nagy K.A., Diamond J. Sustained metabolic scope. Proc. Natl. Acad. Sci. USA 1990, 87:2324-2328.
73. Pickavance L., Dryden S., Hopkins D., Bing C., Frankish H., Wang Q., Vernon R.G., Williams G. Relationships between hypothalamic neuropeptide Y and food intake in the lactating rat. Peptides 1996, 17:577-582.
74. Pravosudov V.V. Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc. Roy. Soc. Lond. B. 2003, 270:2599-2604.
75. Pravosudov V.V., Kitaysky A.S., Wingfield J.C., Clayton N.S. Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli). Gen. Comp. Endocrinol. 2001, 123:324-331.
76. Prevost, J., and Vilter, V. (1963). Histologie de la secretion oesophagienne du Manchot empereur. Proc. 13th Int. Ornithol.Cong., 1085-1094.
77. Price K., Ydenberg R. Begging and provisioning in broods of asynchronously hatched yellow-headed blackbird nestlings. Behav. Ecol. Sociobiol. 1995, 37:201-208.
78. Rajman M., Juráni M., Lamosová D., Mácajová, Sedlacková M., Kost'ál L., Jezová D., Vyboh P. The effect of feed restriction on plasma biochemistry in growing meat-type chickens (Gallus gallus). Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2006, 145:363-371.
79. Ramakrishnan S., Strader A.D., Wimpee B., Chen P., Smith M.S., Buntin J.D. Evidence for increased neuropeptide Y synthesis in mediobasal hypothalamus in relation to parental hyperphagia and gonadal activation in breeding ring doves. J. Neuroendocrinol. 2007, 19:163-171.
80. Ramesh R., Kuenzel W.J., Buntin J.D., Proudman J.A. Identification of growth-hormone- and prolactin-containing neurons within the avian brain. Cell Tissue Res. 2000, 299:371-383.
81. Ramos C., Silver R. Gonadal hormones determine sex differences in timing of incubation by doves. Horm. Behav. 1992, 26:586-601.
82. Rapaport L. Provisioning in wild golden lion tamarins (Leontopithicus rosalia): Benefits to omnivorous young. Behav. Ecol. 2006, 17:212-221.
83. Richard-Yris M.-A., Garnier D.H., Leboucher G. Induction of maternal behavior and some hormonal and physiological correlates in the domestic hen. Horm. Behav. 1983, 17:345-355.
84. Ricklefs R.E. Energetics of reproduction in birds. Avian Energetics 1974, 152-297. Nuttall Ornithological Club, Cambridge MA. R.A. Paynter (Ed.).
85. Roberts S.B., Cole T.J., Coward W.A. Lactational performance in relation to energy intake in the baboon. Am. J. Clin. Nutr. 1985, 41:1270-1276.
86. Saino N., Ninni P., Incagli M., Calza S., Sacchi R., Møller A.P. Begging and parental care in relation to offspring need and condition in the barn swallow (Hirundo rustica). Am. Nat. 2000, 156:637-649.
87. Sauve D., Woodside B. The effect of central administration of prolactin on food intake in virgin female rats is dose-dependent, occurs in the absence of ovarian hormones, and the latency to onset varies with feeding regimen. Brain Res. 1996, 729:75-81.
88. Sauve D., Woodside B. Neuroanatomi-cal specificity of prolactin-induced hyperphagia in virgin female rats. Brain Res. 2000, 868:306-314.
89. Schoech S.J., Mumme R.L., Wingfield J.C. Prolactin and helping behaviour in the cooperatively breeding Florida scrub-jay, Aphelocoma c. coerulescens. Anim. Behav. 1996, 52:445-456.
90. Schooley J.P., Riddle O., Bates R.W. Replacement therapy in hypophysectomized juvenile pigeons. Am. J. Anat. 1941, 69:124-154.
91. Sherry D.F. Parental care and the development of thermoregulation in red junglefowl. Behaviour 1981, 76:240-279.
92. Sherry D.F., Mrosovsky N., Weight loss and anorexia during incubation in birds. J. Comp. Physiol. Psychol. 1980, 94:89-98.
93. Siegel H.M., Van Kampen M. Energy relationships in growing chickens given daily injections of corticosterone. Br. Poultry Sci. 1984, 25:477-485.
94. Silver R., Andrews H., Ball G.F. Parental care in an ecological perspective: a quantitative analysis of avian subfamilies. Am. Zool. 1985, 25:823-840.
95. Silverin B. Endocrine correlates of brood size in adult pied flycatchers, Ficedula hypoleuca. Gen. Comp. Endocrinol. 1982, 47:18-23.
96. Silverin B. Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. Gen. Comp. Endocrinol. 1986, 64:67-74.
97. Silverin B. Testosterone and corticosterone and their relation to territoriality and parental behavior in the pied flycatcher. Hormones, Brain, and Behavior in Vertebrates. 2. Behavioral Activation in Males and Females-Social Interaction and Reproductive Endocrinology 1990, 129-144. S. Karger, Basel. J. Balthazart (Ed.).
98. Slawski B.A., Buntin J.D. Preoptic area lesions disrupt prolactin-induced parental feeding behavior in ring doves. Horm. Behav. 1995, 29:248-266.
99. Strader A.D., Buntin J.D. Neuropeptide Y: A possible mediator of p-rolactin-induced feeding and regulator of energy balance in the ring dove (Streptopelia risoria). J. Neuroendocrinol. 2001, 13:386-392.
100. Strader A.D., Buntin J.D. Changes in agouti-related peptide during the ring dove breeding cycle in relation to prolactin and parental hyperphagia. J. Neuroendcrinol. 2003, 15:1046-1053.
101. Strader A.D., Schiöth H.G., Buntin J.D. The role of the melanocortin system and the melanocortin-4 receptor in ring dove (Streptopelia risoria) feeding behavior. Brain Res. 2003, 960:112-121.
102. Torner L., Neumann I.D. The brain prolactin system: Involvement in stress response adaptations in lactation. Stress 2002, 5:249-257.
103. Van Roo B.L., Ketterson E.D., Sharp P.J. Testosterone and prolactin in two songbirds that differ in paternal care: The blue-headed vireo and the red-eyed vireo. Horm. Behav. 2003, 44:435-441.
104. Vandeputte-Poma J. Feeding, growth, and metabolism of the pigeon, Columba livia domestica: duration and role of crop milk feeding. J. Comp. Physiol. 1980, 135:97-99.
105. Vleck C.M., Mays N.A., Dawson J.W., Goldsmith A.R. Hormonal correlates of parental and helping behavior in cooperatively breeding Harris' hawks (Parabuteo unicinctus). Auk 1991, 108:638-648.
106. Walsh R.J., Slaby F.J., Posner B.I. A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 1987, 120:1846-1850.
107. Wang Q., Buntin J.D. The roles of stimuli from young, previous breeding experience, and prolactin in regulating parental behavior in ring doves (Streptopelia risoria). Horm. Behav. 1999, 35:241-253.
108. Weathers W.W., Sullivan K.A. Juvenile foraging proficiency, parental effort, and avian reproductive success. Ecol. Monogr. 1989, 59:223-246.
109. Weber R.F., Calogero A.E. Prolactin stimulates rat hypothalamic corticotropin-r-eleasing hormone and pituitary adrenocorticotropin secretion in vitro. Neuroendocrinology 1991, 54:248-253.
110. Westmoreland D., Best L.B. What limits mourning doves to a clutch of two eggs?. Condor 1987, 89:486-493.
111. Whittingham L.A., Robertson R.J. Nestling hunger and parental care in red-winged blackbirds. Auk 1993, 110:240-246.
112. Woodside B. Prolactin and the hyperphagia of lactation. Physiol. Behav. 2007, 91:375-382.
113. Xiao X.Q., Grove K.L., Lau S.Y., McWeeney S., Smith M.S. Deoxyribonucleic acid microarray analysis of gene expression pattern in the arcuate nucleus/ventromedial nucleus of the hypothalamus during lactation. Endocrinology 2005, 146:4391-4396.