Unpredictable food availability induces metabolic and hormonal changes independent of food intake in a sedentary songbird

Journal of Experimental Biology

Volumn 215, Issue 16, 2012, Pages 2920-2930

  Fokidis, H Bobby ^a,b   Des Roziers, Matthieu Burin ^c   Sparr, Richard ^d   Rogowski, Christopher ^b   Sweazea, Karen ^e   Deviche, Pierre ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITÉ DE POITIERS   (France)

^d ARIZONA STATE UNIVERSITY   (United States)

^e ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Chronic stress; Corticosterone; Curve billed thrasher; Energy reserve; Fault bar; Food variability; Gluconeogenesis; Glucose; Lipid; Predictability; Protein; Vasotocin

Indexed keywords

CORTICOSTERONE; HORMONE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BLOOD; BODY WEIGHT; FEATHER; FEEDING BEHAVIOR; FOOD; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LYMPHOCYTE COUNT; MALE; METABOLISM; MUSCLE; ORGAN SIZE; OSMOLARITY; PHYSIOLOGY; SEDENTARY LIFESTYLE; SONGBIRD; TAIL; UNCERTAINTY;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; CORTICOSTERONE; FEATHERS; FEEDING BEHAVIOR; FOOD; HORMONES; LYMPHOCYTE COUNT; MALE; MUSCLES; ORGAN SIZE; OSMOLAR CONCENTRATION; SEDENTARY LIFESTYLE; SONGBIRDS; TAIL; UNCERTAINTY;

ANIMALIA; AVES; MIMIDAE; PASSERI; TOXOSTOMA CURVIROSTRE;

EID: 84864337436     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.071043     Document Type: Article

References (109)

1. Acquarone, C., Cucco, M., Cauli, S. L. and Malacarne, G. (2002). Effects of food abundance and predictability on body condition and health parameters: experimental tests with the hooded crow. Ibis 144, E155-E163
2. Anderies, J. M., Katti, M. and Shochat, E. (2007). Living in the city: resource availability, predation, and bird population dynamics in urban areas. J. Theor. Biol. 247, 36-49 (Pubitemid 46770782)
3. Angelier, F., Shaffer, S. A., Weimerskirch, H., Trouvé, C. and Chastel, O. (2007). Corticosterone and foraging behavior in a pelagic seabird. Physiol. Biochem. Zool. 80, 283-292. (Pubitemid 46581368)
4. Antoni, F. A. (1993). Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front. Neuroendocrinol. 14, 76-122. (Pubitemid 23210952)
5. Arrington, D. A., Davidson, B. K., Winemiller, K. O. and Layman, C. A. (2006). Influence of life history and seasonal hydrology on lipid storage in three neotropical fish species. J. Fish Biol. 68, 1347-1361. (Pubitemid 43940951)
6. Astheimer, L. B., Buttemer, W. A. and Wingfield, J. C. (1992). Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand. 23, 355-365.
7. Awerman, J. L. and Romero, L. M. (2010). Chronic psychological stress alters body weight and blood chemistry in European starlings (Sturnus vulgaris). Comp. Biochem. Physiol. 156A, 136-142.
8. Bauer, C. M., Glassman, L. W., Cyr, N. E. and Romero, L. M. (2011). Effects of predictable and unpredictable food restriction on the stress response in molting and non-molting European starlings (Sturnus vulgaris). Comp. Biochem. Physiol. 160A, 390-399.
9. Bednekoff, P. A. and Houston, A. I. (1994). Dynamic models of mass-dependent predation, risk-sensitive foraging, and premigratory fattening in birds. Ecology 75, 1131-1140.
10. Bednekoff, P. A. and Krebs, J. R. (1995). Great tit fat reserves-effects of changing and unpredictable feeding day length. Funct. Ecol. 9, 457-462.
11. Bennett, G. F. (1970). Simple techniques for making avian blood smears. Can. J. Zool. 48, 585-586.
12. Boon, P., Visser, G. H. and Daan, S. (1999). Feeding and growth of Japanese quail (Coturnix c. japonica) chicks with unpredictable food access. Neth. J. Zool. 49, 233-249. (Pubitemid 30184253)
13. Bortolotti, G. R., Marchant, T. A., Blas, J. and Cabezas, S. (2009). Tracking stress: localisation, deposition and stability of corticosterone in feathers. J. Exp. Biol. 212, 1477-1482.
14. Braun, E. J. and Sweazea, K. L. (2008). Glucose regulation in birds. Comp. Biochem. Physiol. 151B, 1-9.
15. Breuner, C. W., Greenberg, A. L. and Wingfield, J. C. (1998). Noninvasive corticosterone treatment rapidly increases activity in Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii). Gen. Comp. Endocrinol. 111, 386-394. (Pubitemid 28394931)
16. Bridge, E. S., Schoech, S. J., Bowman, R. and Wingfield, J. C. (2009). Temporal predictability in food availability: effects upon the reproductive axis in scrub-jays. J. Exp. Zool. 311A, 35-44.
17. Brown, D. R. and Sherry, T. W. (2006). Food supply controls the body condition of a migrant bird wintering in the tropics. Oecologia 149, 22-32 (Pubitemid 44366204)
18. Bull, C. D. and Metcalfe, N. B. (1997). Regulation of hyperphagia in response to varying energy deficits in overwintering juvenile Atlantic salmon. J. Fish Biol. 50, 498-510. (Pubitemid 27161679)
19. Campbell, T. W. (1996). Clinical pathology. In Reptile Medicine and Surgery (ed. D. R. Mader), pp. 248-257.Philadelphia, PA: W. B. Saunders.
20. Clerens, S., D'Hondt, E., Berghman, L. R., Vandesande, F. and Arckens, L. (2003). Identification of cGnRH-II in the median eminence of Japanese quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol. 131, 48-56. (Pubitemid 36293384)
21. Corbel, H., Geiger, S. and Groscolas, R. (2010). Preparing to fledge: the adrenocortical and metabolic responses to stress in king penguin chicks. Funct. Ecol. 24, 82-92.
22. Cox, R. M., Barrett, M. M. and John-Alder, H. B. (2008). Effects of food restriction on growth, energy allocation, and sexual size dimorphism in Yarrow's spiny lizard, Sceloporus jarrovii. Can. J. Zool. 86, 268-276. (Pubitemid 351679316)
23. Cray, C., Rodriguez, M. and Arheart, K. L. (2008). Use of refractometry for determination of psittacine plasma protein concentration. Vet. Clin. Pathol. 37, 438-442.
24. Cucco, M., Ottonelli, R., Raviola, M. and Malacarne, G. (2002). Variations of body mass and immune function in response to food unpredictability in magpies. Oecologica 23, 271-276.
25. Cuthill, I. C., Maddocks, S. A., Weall, C. V. and Jones, E. K. M. (2000). Body mass regulation in response to changes in feeding predictability and overnight energy expenditure. Behav. Ecol. 11, 189-195. (Pubitemid 30217961)
26. Dall, S. R. X. and Witter, M. S. (1998). Feeding interruptions, diurnal mass changes and daily routines of behaviour in the zebra finch. Anim. Behav. 55, 715-725. (Pubitemid 28173963)
27. Dallman, M. F., Akana, S. F., Pecoraro, N. C., Warne, J. P., la Fleur, S. E. and Foster, M. T. (2007). Glucocorticoids, the etiology of obesity and the metabolic syndrome. Curr. Alzheimer Res. 4, 199-204. (Pubitemid 46562395)
28. Dawson, A. and Goldsmith, A. R. (1997). Changes in gonadotrophin- releasing hormone (GnRH-I) in the pre-optic area and median eminence of starlings (Sturnus vulgaris) during the recovery of photosensitivity and during photostimulation. J. Reprod. Fertil. 111, 1-6.
29. Dawson, R. D. and Bortolotti, G. R. (1997). Total plasma protein level as an indicator of condition in wild American kestrels (Falco sparverius). Can. J. Zool. 75, 680-686. (Pubitemid 27253116)
30. DesRochers, D. W., Reed, J. M., Awerman, J., Kluge, J. A., Wilkinson, J., van Griethuijsen, L. I., Aman, J. and Romero, L. M. (2009). Exogenous and endogenous corticosterone alter feather quality. Comp. Biochem. Physiol. 152A, 46-52.
31. Díaz-Muñaoz, M., Vázquez-Martínez, O., Aguilar-Roblero, R. and Escobar, C. (2000). Anticipatory changes in liver metabolism and entrainment of insulin, glucagon, and corticosterone in food-restricted rats. Am. J. Physiol. 279, R2048-R2056.
32. dos Santos, R. N., Amadio, S. and Ferreira, E. J. G. (2010). Patterns of energy allocation to reproduction in three Amazonian fish species. Neotrop. Ichthyol. 8, 155-162.
33. dos Santos Schmidt, E. M., Paulillo, A. C., Dittrich, R. L., Hoppe, E. G. L. and Bertoli, R. S. (2008). Determination of ring-necked pheasant (Phasianus colchicus) serum protein concentrations by refractometry and the biuret method. Int. J. Poult. Sci. 7, 672-673.
34. Driedzic, W. R., Crowe, H. L., Hicklin, P. W. and Sephton, D. H. (1993). Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can. J. Zool. 71, 1602-1608.
35. Fan, H. P., Xie, M., Wang, W. W., Hou, S. S. and Huang, W. (2008). Effects of dietary energy on growth performance and carcass quality of white growing pekin ducks from two to six weeks of age. Poult. Sci. 87, 1162-1164. (Pubitemid 351871277)
36. Fauchald, P., Tveraa, T., Henaug, C. and Yoccoz, N. (2004). Adaptive regulation of body reserves in reindeer, Rangifer tarandus: a feeding experiment. Oikos 107, 583-591. (Pubitemid 39520811)
37. Fernandez-Fernandez, R., Martini, A. C., Navarro, V. M., Castellano, J. M., Dieguez, C., Aguilar, E., Pinilla, L. and Tena-Sempere, M. (2006). Novel signals for the integration of energy balance and reproduction. Mol. Cell. Endocrinol. 254, 127-132. (Pubitemid 44041763)
38. Fery, F., Plat, L., Melot, C. and Balasse, E. O. (1996). Role of fat-derived substrates in the regulation of gluconeogenesis during fasting. Am. J. Physiol. 33, 822-830.
39. Fokidis, H. B. and Deviche, P. (2011). Plasma corticosterone of city and desert curve-billed thrashers, Toxostoma curvirostre, in response to stress-related peptide administration. Comp. Biochem. Physiol. 159A, 32-38.
40. Fokidis, H. B. and Deviche, P. (2012). Brain arginine vasotocin immunoreactivity differs between urban and desert curve-billed thrashers, Toxostoma curvirostre: relationships with territoriality and stress physiology. Brain Behav. Evol. 79, 84-97.
41. Fokidis, H. B., Greiner, E. C. and Deviche, P. (2008). Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J. Avian Biol. 39, 300-310. (Pubitemid 351784420)
42. Fokidis, H. B., Orchinik, M. and Deviche, P. (2009). Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen. Comp. Endocrinol. 160, 259-270.
43. Fokidis, H. B., Sparr, R., Deviche, P., and Sweazea, K. (2010). Modeling changes in energy substrate usage in response to acute stress in birds. FASEB J. 24, 849.4.
44. Fokidis, H. B., Hurley, L., Rogowski, C., Sweazea, K. and Deviche, P. (2011a). Effects of captivity and body condition on plasma corticosterone, locomotor behavior, and plasma metabolites in curve-billed thrashers. Physiol. Biochem. Zool. 84, 595-606.
45. Fokidis, H. B., Orchinik, M. and Deviche, P. (2011b). Context-specific territorial behavior in urban birds: no evidence for involvement of testosterone or corticosterone. Horm. Behav. 59, 133-143.
46. Frayn, K. N., Arner, P. and Yki-Jarvinen, H. (2006). Fatty acid metabolism in adipose tissue, muscle and liver in health and disease. Essays Biochem. 42, 89-103.
47. French, S. S. and Moore, M. C. (2008). Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus. Gen. Comp. Endocrinol. 155, 148-156. (Pubitemid 350122482)
48. French, S. S., McLemore, R., Vernon, B., Johnston, G. I. H. and Moore, M. C. (2007). Corticosterone modulation of reproductive and immune systems trade-offs in female tree lizards: long-term corticosterone manipulations via injectable gelling material. J. Exp. Biol. 210, 2859-2865. (Pubitemid 47401654)
49. French, S. S., Fokidis, H. B. and Moore, M. C. (2008). Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban-rural gradient. J. Comp. Physiol. B 178, 997-1005.
50. Gross, W. B. and Siegel, H. S. (1983). Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis. 27, 972-979.
51. Guglielmo, C. G., O'Hara, P. D. and Williams, T. D. (2002). Extrinsic and intrinsic sources of variation in plasma lipid metabolites of free-living western sandpipers (Calidris mauri). Auk 119, 437-445. (Pubitemid 34536348)
52. Guglielmo, C. G., Cerasale, D. J. and Eldermire, C. (2005). A field validation of plasma metabolite profiling to assess refueling performance of migratory birds. Physiol. Biochem. Zool. 78, 116-125. (Pubitemid 40290162)
53. Haller, M. (2003). The hand-held refractometer-a useful tool in veterinary practice. Magyar Állatorvosok Lapja 125, 157-158.
54. Harmon, B. G. (1998). Avian heterophils in inflammation and disease resistance. Poult. Sci. 77, 972-977. (Pubitemid 128525109)
55. Harr, K. E. (2002). Clinical chemistry of companion avian species: a review. Vet. Clin. Pathol. 31, 140-151. (Pubitemid 35216566)
56. Hau, M., Wikelski, M. and Wingfield, J. C. (2000). Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird. J. Exp. Zool. 286, 494-504. (Pubitemid 30146921)
57. Hazard, D., Couty, M. and Guémené, D. (2007). Characterization of CRF, AVT, and ACTH cDNA and pituitary-adrenal axis function in Japanese quail divergently selected for tonic immobility. Am. J. Physiol. 293, R1421-R1429. (Pubitemid 47358969)
58. Holmes, D. J. and Ottinger, M. A. (2003). Birds as long-lived animal models for the study of aging. Exp. Gerontol. 38, 1365-1375. (Pubitemid 38041224)
59. Houston, A. I., McNamara, J. M., Barta, Z. and Klasing, K. C. (2007). The effect of energy reserves and food availability on optimal immune defence. Proc. R. Soc. B 274, 2835-2842. (Pubitemid 350057937)
60. Hurly, T. A. (1992). Energetic reserves of marsh tits (Parus palustris)-food and fat storage in response to a variable food supply. Behav. Ecol. 3, 181-188. (Pubitemid 23398809)
61. Jenni-Eiermann, S., Glaus, E., Grüebler, M., Schwabl, H. and Jenni, L. (2008). Glucocorticoid response to food availability in breeding barn swallows (Hirundo rustica). Gen. Comp. Endocrinol. 155, 558-565. (Pubitemid 351191917)
62. Jobling, M. and Johansen, S. J. S. (1999). The lipostat, hyperphagia and catch-up growth. Aquacult. Res. 30, 473-478. (Pubitemid 29475418)
63. Kabelik, D., Weiss, S. L. and Moore, M. C. (2008). Arginine vasotocin (AVT) immunoreactivity relates to testosterone but not territorial aggression in the tree lizard, Urosaurus ornatus. Brain Behav. Evol. 72, 283-294.
64. King, J. C., Lechan, R. M., Kugel, G. and Anthony, E. L. P. (1983). Acrolein: a fixative for immunocytochemical localization of peptides in the central nervous system. J. Histochem. Cytochem. 31, 62-68. (Pubitemid 13176008)
65. Lohmus, M., Sundstrom, F. and Moore, F. R. (2006). Non-invasive corticosterone treatment changes foraging intensity in red-eyed vireos Vireo olivaceus. J. Avian Biol. 37, 523-526. (Pubitemid 44337399)
66. Luquin, E., Pérez-Lorenzo, E., Aymerich, M. S. and Mengual, E. (2010). Two-color fluorescence labeling in acrolein-fixed brain tissue. J. Histochem. Cytochem. 58, 359-368.
67. Lynn, S. E., Breuner, C. W. and Wingfield, J. C. (2003). Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm. Behav. 43, 150-157. (Pubitemid 36293285)
68. Lynn, S. E., Stamplis, T. B., Barrington, W. T., Weida, N. and Hudak, C. A. (2010). Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm. Behav. 58, 214-222.
69. Macleod, R. and Gosler, A. G. (2006). Capture and mass change: perceived predation risk or interrupted foraging? Anim. Behav. 71, 1081-1087
70. Maillet, D. and Weber, J. M. (2006). Performance-enhancing role of dietary fatty acids in a long-distance migrant shorebird: the semipalmated sandpiper. J. Exp. Biol. 209, 2686-2695. (Pubitemid 44213114)
71. Martínez-Padilla, J. and Fargallo, J. A. (2007). Food supply during prelaying period modifies the sex-dependent investment in eggs of Eurasian kestrels. Behav. Ecol. Sociobiol. 61, 1735-1742 (Pubitemid 47222933)
72. McGraw, K. J., Crino, O. L., Medina-Jerez, W. and Nolan, P. M. (2006). Effect of dietary carotenoid supplementation on food intake and immune function in a songbird with no carotenoid coloration. Ethology 112, 1209-1216. (Pubitemid 44789649)
73. McWilliams, S. R., Guglielmo, C., Pierce, B. and Klaassen, M. (2004). Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J. Avian Biol. 35, 377-393. (Pubitemid 39275400)
74. Mikolajewski, D. J., Joop, G. and Wohlfahrt, B. (2007). Coping with predators and food limitation: testing life history theory for sex-specific larval development. Oikos 116, 642-649. (Pubitemid 46525291)
75. Morton, J. M., Kirkpatrick, R. L., Howerter, D. W., Eason, T. H. and Long, C. M. (1994). Depletion of lipid, lean, and ash masses in food-restricted American black ducks. Can. J. Zool. 72, 1492-1496.
76. Munn, A. J., Kern, P. and McAllan, B. M. (2010). Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). Naturwissenschaften 97, 601-605.
77. Naya, D. E., Veloso, C. and Bozinovic, F. (2008). Physiological flexibility in the Andean lizard Liolaemus bellii: seasonal changes in energy acquisition, storage and expenditure. J. Comp. Physiol. B 178, 1007-1015.
78. Panzica, G. C., Aste, N., Castagna, C., Viglietti-Panzica, C. and Balthazart, J. (2001). Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications. Brain Res. Rev. 37, 178-200. (Pubitemid 34020731)
79. Piersma, T., Gessaman, J. A., Dekinga, A. and Visser, G. H. (2004). Gizzard and other lean mass components increase, yet basal metabolic rates decrease, when red knots Calidris canutus are shifted from soft to hard-shelled food. J. Avian Biol. 35, 99-104. (Pubitemid 38370313)
80. Polo, V. and Bautista, L. M. (2002). Daily body mass regulation in dominancestructured coal tit (Parus ater) flocks in response to variable food access: a laboratory study. Behav. Ecol. 13, 696-704. (Pubitemid 35181188)
81. Pravosudov, V. V., Kitaysky, A. S., Wingfield, J. C. and Clayton, N. S. (2001). Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli). Gen. Comp. Endocrinol. 123, 324-331. (Pubitemid 32848464)
82. Prentice, S., Jobes, A. P. and Burness, G. (2008). Fault bars and fluctuating asymmetry in birds: are the two measures correlated? J. Field Ornithol. 79, 58-63. (Pubitemid 351334626)
83. Pyle, P. (1997). Identification Guide to North American Birds, Part 1. Bolinas, CA: Slate Creek Press.
84. Rahman, R. and Clayton, R. B. (1981). Sexual differentiation of hepatic metabolism of corticosterone and testosterone in the rat. J. Biochem. 90, 1567-1575. (Pubitemid 12140510)
85. Reznick, D. and Yang, A. P. (1993). The influence of fluctuating resources on lifehistory-patterns of allocation and plasticity in female guppies. Ecology 74, 2011-2019. (Pubitemid 24408493)
86. Rich, E. L. and Romero, L. M. (2005). Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am. J. Physiol. 288, R1628-R1636. (Pubitemid 40720713)
87. Rogers, C. M. and Reed, A. K. (2003). Does avian winter fat storage integrate temperature and resource conditions? A long-term study. J. Avian Biol. 34, 112-118. (Pubitemid 36639402)
88. Roman, Y., Bomsel-Demontoy, M. C., Levrier, J., Chaste-Duvernoy, D. and Jalme, M. S. (2009). Effect of hemolysis on plasma protein levels and plasma electrophoresis in birds. J. Wildl. Dis. 45, 73-80.
89. Romero, L. M. and Romero, R. C. (2002). Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104, 129-135. (Pubitemid 34186282)
90. Rozman, J., Runciman, D. and Zann, R. A. (2003). Seasonal variation in body mass and fat of zebra finches in south-eastern Australia. Emu 103, 11-19. (Pubitemid 36530821)
91. Saldanha, C. J., Deviche, P. J. and Silver, R. (1994). Increased VIP and decreased GnRH expression in photorefractory dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 93, 128-136. (Pubitemid 24027775)
92. Sapolsky, R. M., Romero, L. M. and Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89. (Pubitemid 32266068)
93. Schoech, S. J. and Hahn, T. P. (2005). Timing of reproduction and food supplementation: are high latitude species less responsive than low latitude to nonphotic cues? Integr. Comp. Biol. 45, 1069.
94. Serrano, D. and Jovani, R. (2005). Adaptive fault bar distribution in a long-distance migratory, aerial forager passerine? Biol. J. Linn. Soc. Lond. 85, 455-461. (Pubitemid 41080400)
95. Sewall, K. B., Dankoski, E. C. and Sockman, K. W. (2010). Song environment affects singing effort and vasotocin immunoreactivity in the forebrain of male Lincoln's sparrows. Horm. Behav. 58, 544-553.
96. Smith, S. B. and McWilliams, S. R. (2010). Patterns of fuel use and storage in migrating passerines in relation to fruit resources at autumn stopover sites. Auk 127, 108-118.
97. Swaddle, J. P. and Witter, M. R. (1994). Food, feathers and fluctuating asymmetries. Proc. R. Soc. B 255, 147-152.
98. Tweit, R. C. (1996). Curve-billed thrasher (Toxostoma curvirostre). In The Birds of North America, no. 235 (ed. A. Poole and F. Gill). Philadelphia, PA: The Birds of North America.
99. Vaanholt, L. M., De Jong, B., Garland, T., Jr, Daan, S. and Visser, G. H. (2007). Behavioural and physiological responses to increased foraging effort in male mice. J. Exp. Biol. 210, 2013-2024. (Pubitemid 46998746)
100. Van Gils, J. A., Battley, P. F., Piersma, T. and Drent, R. (2005). Reinterpretation of gizzard sizes of red knots world-wide emphasises overriding importance of prey quality at migratory stopover sites. Proc. R. Soc. B 272, 2609-2618. (Pubitemid 41796565)
101. Van Gils, J. A., Piersma, T., Dekinga, A. and Battley, P. F. (2006). Modelling phenotypic flexibility: an optimality analysis of gizzard size in red knots Calidris canutus. Ardea 94, 409-420. (Pubitemid 46714029)
102. Vleck, C. M., Vertalino, N., Vleck, D. and Bucher, T. L. (2000). Stress, corticosterone, and heterophil to lymphocyte ratios in free-living adelie penguins. Condor 102, 392-400. (Pubitemid 30322774)
103. Walsberg, G. E. and Thompson, C. W. (1990). Annual changes in gizzard size and function in a frugivorous bird. Condor 92, 794-795.
104. Warne, J. P., Akana, S. F., Ginsberg, A. B., Horneman, H. F., Pecoraro, N. C. and Dallman, M. F. (2009). Disengaging insulin from corticosterone: roles of each on energy intake and disposition. Am. J. Physiol. 296, R1366-R1375.
105. Watson, R. E., Jr, Wiegand, S. J., Clough, R. W. and Hoffman, G. E. (1986). Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7, 155-159. (Pubitemid 16082879)
106. Wingfield, J. C. (2003). Control of behavioural strategies for capricious environments. Anim. Behav. 66, 807-816.
107. Wingfield, J. C., Vleck, C. M. and Moore, M. C. (1992). Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool. 264, 419-428.
108. Witter, M. S. and Swaddle, J. P. (1997). Mass regulation in juvenile starlings: response to change in food availability depends on initial body mass. Funct. Ecol. 11, 11-15.
109. Witter, M. S., Swaddle, J. P. and Cuthill, I. C. (1995). Periodic food availability and strategic regulation of body mass in the European starling, Sturnus vulgaris. Funct. Ecol. 9, 568-574. (Pubitemid 26448245)