Modulation of the hypothalamic–pituitary–adrenal axis of an Arctic–breeding polygynandrous songbird, the Smith's longspur, Calcarius pictus

To successfully reproduce in the Arctic, birds must modulate their neuroendocrine and behavioural systems. These adjustments include an attenuation of the stress responsiveness of the hypothalamic–pituitary–adrenal (HPA) axis to external stimuli and a behavioural insensitivity to high corticosterone (B) levels. The HPA axis was examined in free–living territorial polygynandrous Smith's longspurs (Calcarius pictus) that migrate to breed on the Arctic tundra. Basal and stress–induced B levels were measured through the breeding season and were found to be significantly lower in females compared with males. This was not a consequence of adrenal insensitivity, because intrajugular injections of adrenocorticotrophin hormone (ACTH) enhanced B release in incubating females. In males the adrenocortical response to stress was significantlys attenuated during the parental phase compared with arrival at the breeding ground. In contrast to temperate passerines, there was no significant decrease in male territorial aggressive behaviour when B was experimentally elevated, suggesting a behavioural insensitivity to glucocorticoids. This mechanism is hypothesized to increase reproductive success by preventing interruptions to parental care during transient deleterious environmental perturbations, which are often experienced in the short Arctic breeding season. Modulation of the HPA axis in this species in relation to life–history stage, lifetime reproductive success and the polygynandrous mating system is discussed.

[1]  J. Wingfield,et al.  Seasonal changes of the adrenocortical responses to stress in redpolls, Acanthis flammea, in Alaska , 1994 .

[2]  J. Wingfield,et al.  Corticosterone has no effect on territorial aggressive behavior in the snow bunting: an Arctic-breeding songbird. , 2001 .

[3]  B. Follett,et al.  Chapter 8 – BIOLOGICAL ACTIONS OF STEROID HORMONES IN NONMAMMALIAN VERTEBRATES , 1972 .

[4]  B. Silverin Stress responses in birds , 1998 .

[5]  J. Wingfield,et al.  Plasma corticosterone, adrenal mass, winter weather, and season in nonbredding populations of Dark-eyed Juncos (Junco hyemalis hyemalis) , 1993 .

[6]  J. Wingfield,et al.  Arctic spring: hormone-behavior interactions in a severe environment. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[7]  P. Deviche,et al.  Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. , 2001, General and comparative endocrinology.

[8]  C. W. Helms,et al.  Winter and Migratory Weight and Fat Field Studies on Some North American Buntings , 1960 .

[9]  J. Wingfield,et al.  Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. , 1992, The Journal of experimental zoology.

[10]  J. Briskie Copulation patterns and sperm competition in the polygynandrous Smith's longspur , 1992 .

[11]  J. Wingfield,et al.  Corticosterone Treatment Has No Effect on Reproductive Hormones or Aggressive Behavior in Free-living Male Tree Sparrows, Spizella arborea , 2000, Hormones and Behavior.

[12]  J. Wingfield,et al.  The adrenocortical responses to stress in snow buntings (Plectrophenax nivalis) and Lapland longspurs (Calcarius lapponicus) at Barrow, Alaska , 1994 .

[13]  J. Wingfield,et al.  Effects of corticosterone on territorial behavior of free-living male song sparrows Melospiza melodia , 1986, Hormones and Behavior.

[14]  Masahiko Nakamura,et al.  Cloacal protuberance and copulatory behavior of the alpine accentor (Prunella collaris). , 1990 .

[15]  B. Silverin The stress response and autumn dispersal behaviour in willow tits , 1997, Animal Behaviour.

[16]  T. Hahn,et al.  Endocrine Bases of Spatial and Temporal Opportunism in Arctic-Breeding Birds , 1995 .

[17]  B. Silverin Behavioural and hormonal responses of the pied flycatcher to environmental stressors , 1998, Animal Behaviour.

[18]  J. Wingfield,et al.  Alterations in hypothalamic-pituitary-adrenal function associated with captivity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii). , 1999, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[19]  N. Davies,et al.  Cooperation and conflict among dunnocks, Prunella modularis, in a variable mating system , 1985, Animal Behaviour.

[20]  J. Wingfield,et al.  Hormones and Territorial Behavior during Breeding in Snow Buntings (Plectrophenax nivalis): An Arctic-Breeding Songbird , 1998, Hormones and Behavior.

[21]  J. Wingfield,et al.  Season and migration alters the corticosterone response to capture and handling in an Arctic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelii). , 1997, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[22]  J G Phillips,et al.  Stress and adrenal function. , 1984, The Journal of experimental zoology.

[23]  J. R. Cain,et al.  A model for drought inhibition of bobwhite quail (Colinus virginianus) reproductive systems , 1985 .

[24]  C. Breuner,et al.  Seasonal Regulation of Membrane and Intracellular Corticosteroid Receptors in the House Sparrow Brain , 2001, Journal of neuroendocrinology.

[25]  D. Yarian,et al.  Corticosterone, foraging behavior, and metabolism in dark-eyed juncos, Junco hyemalis. , 1990, General and comparative endocrinology.

[26]  K. Hunt Testosterone, estrogen, and breeding behavior in an Arctic bird, the Lapland longspur , 1997 .

[27]  J. Wingfield,et al.  Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[28]  J. Wingfield,et al.  Modulation of the Adrenocortical Responses to Acute Stress in Arctic Birds: A Possible Ecological Basis , 1995 .

[29]  John C. Wingfield,et al.  ECOLOGICAL BASES OF HORMONE-BEHAVIOR INTERACTIONS : THE EMERGENCY LIFE HISTORY STAGE , 1998 .

[30]  J. Wingfield,et al.  Interactions of corticosterone with feeding, activity and metabolism in passerine birds , 1992 .

[31]  J. Wingfield,et al.  Gender and seasonal differences in the adrenocortical response to ACTH challenge in an arctic passerine, Zonotrichia leucophrys gambelii. , 1994, General and comparative endocrinology.

[32]  J. Wingfield,et al.  Steroid Hormone Interrelationships with Territorial Aggression in an Arctic-Breeding Songbird, Gambel's White-Crowned Sparrow, Zonotrichia leucophrys gambelii , 2002, Hormones and Behavior.

[33]  J. Wingfield,et al.  Endocrine Responses of White-Crowned Sparrows to Environmental Stress , 1982 .

[34]  J. Wingfield,et al.  Seasonal and Acute Changes in Adrenocortical Responsiveness in an Arctic-Breeding Bird , 1995, Hormones and Behavior.

[35]  B. Silverin Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. , 1986, General and comparative endocrinology.

[36]  J. Wingfield,et al.  Adrenocortical responses to stress in breeding Pied Flycatchers Ficedula hypoleuca: relation to latitude, sex and mating status , 1998 .

[37]  J. Wingfield,et al.  Testosterone and Aggressive Behaviour during the Reproductive Cycle of Male Birds , 1985 .

[38]  J. Wingfield,et al.  The adrenocortical responses to stress in breeding Willow Warblers Phylloscopus trochilus in Sweden : effects of latitude and gender , 1997 .

[39]  J. Wingfield,et al.  Ecological factors underlying the adrenocortical response to capture stress in arctic-breeding shorebirds. , 2001, General and comparative endocrinology.