Theoretical models of adaptive energy management in small wintering birds

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 362, Issue 1486, 2007, Pages 1857-1871

  Brodin, Anders ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Adaptive fat regulation; Energy reserves; Food hoarding; Nocturnal hypothermia; Small birds; Theoretical models

Indexed keywords

CACHING; ENVIRONMENTAL CHANGE; MORTALITY; PASSERINE; SURVIVORSHIP;

AVES;

EID: 35148886300     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1812     Document Type: Review

References (116)

1. Acquarone, C., Cucco, M., Li Cauli, S. & 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. (doi:10.1046/j.1474-919X.2002.t01-2-00094_1.x)
2. Andersson, M. & Krebs, J. 1978 On the evolution of hoarding behaviour. Anim. Behav. 26, 707-711. (doi:10.1016/0003-3472(78) 90137-9)
3. Bednekoff, P. A. 1996 Translating mass dependent flight performance into predation risk: an extension of Metcalfe & Ure. Proc. R. Soc. B 263, 887-889.
4. Bednekoff, P. A. & Houston, A. I. 1994a Dynamic models of mass-dependent predation, risk-sensitive foraging, and premigratory fattening in birds. Ecology 75, 1131-1140.
5. Bednekoff, P. A. & Houston, A. I. 1994b Avian daily foraging patterns: effects of digestive constraints and variability. Evol. Ecol. 8, 36-52. (doi:10.1007/BF01237664)
6. Bednekoff, P. A. & Houston, A. I. 1994c Optimizing fat reserves over the entire winter: a dynamic model. Oikos 71, 408-415.
7. Bednekoff, P. A. & Krebs, J. R. 1995 Great tit fat reserves: effects of changing and unpredictable feeding day length. Ecology 9, 457-462.
8. Bednekoff, P. A., Biebach, H. & Krebs, J. 1994 Great tit fat reserves under unpredictable temperatures. J. Avian Biol. 25, 156-160.
9. Brodin, A. 1992 Cache dispersion affects retrieval time in hoarding willow tits. Ornis Scand. 23, 7-12.
10. Brodin, A. 1993a Low rate of loss of willow tit caches may increase the adaptiveness of long-term hoarding. Auk 110, 642-645.
11. Brodin, A. 1993b Radio-ptilochronology - tracing radioactively labelled food in feathers. Ornis Scand. 24, 167-173.
12. Brodin, A. 1994a The disappearance of caches that have been stored by naturally foraging willow tits Parus montanus. Anim. Behav. 47, 730-732. (doi:10.1006/anbe.1994.1100)
13. Brodin, A. 1994b The role of naturally stored food supplies in the winter diet of the boreal willow tit Parus montanus. Ornis Svecica 4, 31-40.
14. Brodin, A. 2000 Why do hoarding birds gain fat in winter in the wrong way? Suggestions from a dynamic model. Behav. Ecol. 11, 27-39. (doi:10.1093/beheco/11.1.27)
15. Brodin, A. 2001 Mass-dependent predation and metabolic expenditure in wintering birds: is there a trade-off between different forms of predation. Anim. Behav. 62, 993-999. (doi:10.1006/anbe.2001.1844)
16. Brodin, A. 2005 Hippocampus volume does not correlate to food hoarding rates in the field in two closely related bird species, the black-capped chickadee Poecile atricapilla and the willow tit Parus montanus. Auk 122, 819-828.
17. Brodin, A. & Clark, C. W. 1997 Long-term hoarding in the Paridae: a dynamic model. Behav. Ecol. 8, 178-185.
18. Brodin, A. & Kunz, C. 1997 An experimental study of cache recovery by hoarding willow tits after different retention intervals. Behaviour 134, 881-890.
19. Brodin, A. & Lundborg, K. 2003 Rank-dependent hoarding effort in willow tits (Parus montanus): a test of theoretical predictions. Behav. Ecol. Sociobiol. 54, 587-592. (doi:10.1007/s00265-003-0661- 9)
20. Brodin, A., Lundborg, K. & Clark, C. W. 2001 The effect of dominance on food hoarding: a game theoretical model. Am. Nat. 157, 66-75. (doi:10.1086/317008)
21. Carpenter, F. L. & Hixon, M. A. 1988 A new function for torpor: fat conservation in a wild migrant hummingbird. Condor 90, 373-378.
22. Chaplin, S. B. 1976 The physiology of hypothermia in the black-capped chickadee, Parus atricapillus. J. Comp. Physiol. 112, 335-344.
23. Clark, C. W. & Dukas, R. 2000 Winter survival strategies for small birds: managing energy through hypothermia. Evol. Ecol. Res. 2, 473-491.
24. Clark, C. W. & Ekman, J. 1995 Dominant and subordinate fattening strategies: a dynamic game. Oikos 72, 205-212.
25. Clark, C. W. & Mangel, M. 2000 Dynamic state variable models in ecology - methods and applications. New York, NY: Oxford University Press.
26. Cooper, S. J. 2002 Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol. Biochem. Zool. 75, 386-395. (doi:10.1086/342256)
27. Cooper, S. J. & Swanson, D. L. 1994 Seasonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96, 638-646.
28. Cucco, M., Ottonelli, R., Raviola, M. & Malacarne, G. 2002 Variations of body mass and immune function in response to food unpredictability in magpies. Acta Oecol. 23, 271-276. (doi:10.1016/S1146-609X(02) 01154-2)
29. Cuthill, I. C., Hunt, S., Cleary, C. & Clark, C. 1997 Colour bands, dominance, and body mass regulation in male zebra finches (Taeniopygia guttata). Proc. R. Soc. B 264, 1093-1099. (doi:10.1098/rspb.1997. 0151)
30. Cuthill, I. C., Maddocks, S. A., Weall, C. V. & Jones, E. K. M. 2000 Body mass regulation in response to changes in feeding predictability and overnight energy expenditure. Behav. Ecol. 11, 189-195. (doi:10.1093/beheco/11.2.189)
31. Dall, S. R. X. & Witter, M. S. 1998 Feeding interruptions, diurnal mass changes and daily routines of behaviour in the zebra finch. Anim. Behav. 55, 715-725. (doi:10.1006/anbe.1997.0749)
32. Ekman, J. 1989 Ecology of non-breeding social systems of Parus. Wilson Bull. 101, 263-288.
33. Ekman, J. B. & Askenmo, C. E. H. 1984 Social rank and habitat use in willow tit groups. Anim. Behav. 32, 508-514.
34. Ekman, J. B. & Lilliendahl, K. 1993 Using priority to food access: fattening strategies in dominance-structured willow tit (Parus montanus) flocks. Behav. Ecol. 4, 232-238.
35. Gentle, L. K. & Gosler, A. G. 2001 Fat reserves and perceived predation risk in the great tit, Parus major. Proc. R. Soc. B 268, 487-491. (doi:10.1098/rspb.2000.1405)
36. Gosler, A. G., Greenwood, J. J. D. & Perrins, C. 1995 Predation risk and the cost of being fat. Nature 377, 621-623. (doi:10.1038/377621a0)
37. Grubb, T. C. J. & Pravosudov, V. V. 1994 Toward a general theory of energy management in wintering birds. J. Avian Biol. 25, 255-260.
38. Haftorn, S. 1956 Contributions to the food biology of tits especially about storing of surplus food. Part III. The willow tit (Parus atricapillus L.). Kgl. Norske Vidensk. Selsk. Skrifter 3, 1-80.
39. Haftorn, S. 1959 The proportion of spruce seeds removed by the tits in a Norwegian spruce forest in 1954-55. Kgl. Norske Vidensk. Selsk. Forh. 32, 121-125.
40. Haftorn, S. 1972 Hypothermia of tits in the arctic winter. Ornis Scand. 3, 153-166.
41. Haftorn, S. 1974 Storage of surplus food by the boreal chickadee Parus hudsonicus in Alaska, with some records on the mountain chickadee Parus gambeli in Colorado. Ornis Scand. 5, 145-161.
42. Haftorn, S. 1992 The diurnal body weight cycle in titmice Parus spp. Ornis Scand. 23, 435-443.
43. Hainsworth, F. R. 1981 Energy regulation in hummingbirds. Am. Sci. 69, 420-429.
44. Hedenström, A. 1992 Flight performance in relation to fuel load in birds. J. Theor. Biol. 158, 535-537.
45. Hitchcock, C. L. & Houston, A. I. 1994 The value of a hoard: not just energy. Behav. Ecol. 5, 202-205.
46. Houston, A. I. & McNamara, J. M. 1993 A theoretical investigation of the fat reserves and mortality levels of small birds in winter. Ornis Scand. 24, 205-219.
47. Houston, A. I. & McNamara, J. M. 1999 Models of adaptive behaviour. An approach based on state. Cambridge, UK: Cambridge University Press.
48. Houston, A. I., McNamara, J. M. & Hutchinson, J. M. C. 1993 General results concerning the trade-off between gaining energy and avoiding predation. Phil. Trans. R. Soc. B 341, 375-397.
49. Houston, A. I., Welton, N. J. & McNamara, J. M. 1997 Acquisition and maintenance costs in the long-term regulation of avian fat reserves. Oikos 78, 331-340.
50. Hughes, P. M. & Rayner, J. M. V. 1991 Addition of artificial loads to long-eared bats Plecotus auritus: handicapping flight performance. J. Exp. Biol. 161, 285-298.
51. Hurly, T. A. 1992 Energetic reserves of marsh tits (Parus palustris): food and fat storage in response to variable food supply. Behav. Ecol. 3, 181-188.
52. Hutchinson, J. M. C. & McNamara, J. M. 2000 Ways to test stochastic dynamic programming models emprically. Anim. Behav. 59, 665-676. (doi:10.1006/anbe.1999.1362)
53. Irving, L., West, G. C. & Peyton, L. J. 1967 Winter feeding program of Alaska willow ptarmigan shown by crop contents. Condor 69, 69-77.
54. Jansson, C. 1982 The year round diets of the willow tit Parus montanus Conrad and the crested tit P. cristatus L. Ph.D. thesis, Göteborgs Universitet, Göteborg.
55. Jansson, C., Ekman, J. & von Brömssen, A. 1981 Winter mortality and food supply in tits Parus spp. Oikos 37, 313-322.
56. Källander, H. 1993 Hamstrande nötväckor klarar vintern bättre (Hoarding nuthatches copes better with the winter). Fauna Flora 88, 23-27.
57. Källander, H. & Smith, H. G. 1990 Food storing in birds: an evolutionary perspective. Curr. Ornithol. 7, 147-207.
58. King, J. R. 1972 Adaptive periodic fat storage by birds. In Proc. 15th Int. Ornithol. Congr. (ed. K. H. Voous), pp. 200-217. Leiden, The Netherlands: E.J. Brill.
59. Koenig, W. D. & Mumme, R. L. 1987 Population ecology of the cooperatively breeding acorn woodpecker. Princeton, NJ: Princeton University Press.
60. Koivula, K., Orell, M., Rytkönen, S. & Lahti, K. 1995 Fatness, sex and dominance; seasonal and daily body mass changes in willow tits. J. Avian Biol. 26, 209-216.
61. Kullberg, C. 1998 Does diurnal variation in body mass affect take-off ability in wintering willow tits? Anim. Behav. 56, 227-233. (doi:10.1006/anbe.1998.0765)
62. Kullberg, C., Fransson, T. & Jakobsson, S. 1996 Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc. R. Soc. B 263, 1671-1675.
63. Kullberg, C., Jakobsson, S. & Fransson, T. 1998 Predator-induced take-off strategy in great tits (Parus major). Proc. R. Soc. B 265, 1659-1664. (doi:10.1098/rspb.1998.0485)
64. Lange, H. & Leimar, O. 2003 Social stability and daily body mass in great tits. Behav. Ecol. 15, 549-554. (doi:10.1093/beheco/arh044)
65. Lee, S. J., Witter, M. S., Cuthill, I. C. & Goldsmith, A. R. 1996 Reduction in escape performance as a cost of reproduction in gravid starlings, Sturnus vulgaris. Proc. R. Soc. B 263, 619-623.
66. Lehikoinen, E. 1987 Seasonality of the daily weight cycle in wintering passerines and its consequences. Ornis Scand. 18, 216-226.
67. Lilliendahl, K. 1997 The effect of predator presence on body mass in captive greenfinches. Anim. Behav. 53, 75-81. (doi:10.1006/anbe. 1996.0279)
68. Lilliendahl, K. 1998 Yellowhammers get fatter in the presence of a predator. Anim. Behav. 55, 1335-1340. (doi:10.1006/anbe.1997.0706)
69. Lilliendahl, K. 2000 Daily accumulation of body reserves under increased predation risk in captive greenfiches Carduelis chloris. Ibis 142, 587-595.
70. Lilliendahl, K. 2002 Daily patterns of body mass gain in four species of small wintering birds. J. Avian Biol. 33, 212-218. (doi:10.1034/j.1600-048X.2002.330302.x)
71. Lima, S. L. 1985 Maximizing feeding efficiency and minimizing time exposed to predators: a trade-off in the black-capped chickadee. Oecologia 66, 60-67. (doi:10.1007/BF00378552)
72. Lima, S. L. 1986 Predation risk and unpredictable feeding conditions: determination of body mass in birds. Ecology 67, 377-385.
73. Lindström, Å. & Piersma, T. 1992 Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135, 70-78.
74. Lucas, J. R. 1994 Regulation of cache stores and body mass in Carolina chickadees (Parus carolinensis). Behav. Ecol. 5, 171-181.
75. Lucas, J. R. & Walter, L. R. 1991 When should chickadees hoard food? Theory and experimental results. Anim. Behav. 41, 579-601.
76. Lucas, J. R., Pravosudov, V. V. & Zielinski, D. L. 2001 A reevaluation of the logic of pilferage effects, predation risk, and environmental variability on avian energy regulation: the critical role of time budgets. Behav. Ecol. 12, 246-260. (doi:10.1093/beheco/12.2.246)
77. Lundborg, K. & Brodin, A. 2003 The effect of dominance rank on fat deposition and food hoarding in the willow tit Parus montanus - an experimental test. Ibis 145, 78-82. (doi:10.1046/j.1474-919X.2003. 00124.x)
78. Macleod, R., Barnett, J. A., Clark, K. & Cresswell, W. 2005 Body mass strategies in blackbirds Turdus merula: the starvation-predation risk trade-off. J. Anim. Ecol. 74, 292-302. (doi:10.1111/j.1365-2656. 2005.00923.x)
79. Mangel, M. & Clark, C. W. 1988 Dynamic modeling in behavioral ecology. Princeton, NJ: Princeton University Press.
80. McNamara, J. M. 1990 The starvation-predation trade-off and some behavioural and ecological consequences. In Behavioural mechanisms of food selection (ed. R. M. Hughes). NATO ASI Series A, Life Sciences, pp. 39-59. New York, NY: Springer.
81. McNamara, J. M. & Houston, A. I. 1987 Starvation and predation as factors limiting population size. Ecology 68, 1515-1519.
82. McNamara, J. M. & Houston, A. I. 1990 The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheor. 38, 37-61. (doi:10.1007/BF00047272)
83. McNamara, J. M. & Houston, A. I. 1994 The effect of a change in foraging options on intake rate and predation rate. Am. Nat. 144, 978-1000. (doi:10.1086/285721)
84. McNamara, J. M., Houston, A. I. & Krebs, J. R. 1990 Why hoard? The economics of food storing in tits, Parus spp. Behav. Ecol. 1, 12-23.
85. McNamara, J. M., Houston, A. I. & Lima, S. L. 1994 Foraging routines of small birds in winter: a theoretical investigation. J. Avian Biol. 25, 287-302.
86. McNamara, J. M., Ekman, J. & Houston, A. I. 2004 The effect of thermoregulatory substitution on optimal reserves of small birds in winter. Oikos 105, 192-196. (doi:10.1111/j.0030-1299.2004.12188.x)
87. McNamara, J. M., Barta, Z., Houston, A. I. & Race, P. 2005 A theoretical investigation of the effect of predators on foraging behaviour and energy reserves. Proc. R. Soc. B 272, 929-934. (doi:10.1098/rspb.2004.3037)
88. Metcalfe, N. B. & Ure, S. E. 1995 Diurnal variation in flight performance and hence potential predation risk in small birds. Proc. R. Soc. B 261, 395-400.
89. Nakamura, H. & Wako, Y. 1988 Food storing behavior of willow tit Parus montanus. J. Yamashina Inst. Ornithol. 20, 21-36.
90. Norberg, U. M. 1989 Vertebrate flight. In Zoophysiology, vol. 27, pp. 1-291. Berlin: Springer.
91. Pravosudov, V. V. 1985 Search for and storage of food by Parus cinctus lapponicus and P. montanus borealis (Paridae). Zool. Zh. 64, 1036-1043.
92. Pravosudov, V. V. & Grubb, T. C. J. 1997 Energy management in passerine birds during the nonbreeding season. Curr. Ornithol. 14, 189-234.
93. Pravosudov, V. V. & Grubb, T. C. 1998 Management of fat reserves in tufted titmice Baelophus bicolor in relation to predation risk. Anim. Behav. 56, 49-54. (doi:10.1006/anbe.1998.0739)
94. Pravosudov, V. V. & Lucas, J. R. 2001a A dynamic model of short-term energy management in small food-caching and non-caching birds. Behav. Ecol. 12, 207-218. (doi:10.1093/beheco/12.2.207)
95. Pravosudov, V. V. & Lucas, J. R. 2001b Daily patterns of energy storage in food-caching birds under variable daily predation risk: a dynamic state variable model. Behav. Ecol. Sociobiol. 50, 239-250. (doi:10.1007/s002650100361)
96. Rands, S. A. & Cuthill, I. C. 2001 Separating the effects of predation risk and interrupted foraging upon mass changes in the blue tit Parus caeruleus. Proc. R. Soc. B 268, 1783-1790. (doi:10.1098/rspb.2001.1653)
97. Reinertsen, R. E. 1996 Physiological and ecological aspects of hypothermia. In Avian energetics and nutritional ecology (ed. C. Carey), pp. 125-157. London, UK: Chapman & Hall.
98. Reinertsen, R. E. & Haftorn, S. 1986 Different metabolic strategies of northern birds for nocturnal survival. J. Comp. Physiol. 156, 655-663.
99. Rogers, C. M. 1987 Predation risk and fasting capacity: do wintering birds maintain optimal body mass? Ecology 68, 1051-1061.
100. Smulders, T. V. 1998 A game theoretical model of evolution of food hoarding: applications to the Paridae. Am. Nat. 151, 356-366. (doi:10.1086/286124)
101. Smulders, T. V. & Dhont, A. A. 1997 How much memory do tits need? Trends Ecol. Evol. 12, 417-418. (doi:10.1016/S0169-5347(97)01200- 7)
102. Stephens, D. W. & Krebs, J. R. 1986 Foraging theory. Princeton, NJ: Princeton University Press.
103. Stoutjesdijk, F. 2003 Birds in the cold: the effects of plumage structure and environment on operative temperature, shown by spherical models. Ornis Svecica 13, 123-136.
104. Thomas, R. J. 2000 Strategic diel regulation of body mass in European robins. Anim. Behav. 59, 787-791. (doi:10.1006/anbe.1999.1360)
105. van der Veen, I. T. 1999 Effects of predation risk on diurnal mass dynamics and foraging routines of yellowhammers (Emberiza citrinella). Behav. Ecol. 10, 545-551. (doi:10.1093/beheco/10.5.545)
106. van der Veen, I. T. 2002 Seeing is believing: information about predators influences yellowhammer behavior. Behav. Ecol. Sociobiol. 51, 466-471. (doi:10.1007/s00265-002-0464-4)
107. van der Veen, I. T. & Lindström, K. M. 2000 Escape flights of yellowhammers and greenfinches: more man just physics. Anim. Behav. 59, 593-601. (doi:10.1006/anbe.1999.1331)
108. van der Veen, I. T. & Sivars, L. E. 2000 Causes and consequences of mass loss upon predator encounter: feeding interruption, stress or fit-for-flight. Funct. Ecol. 14, 638-644.
109. Veasy, J. S., Metcalfe, N. B. & Houston, D. C. 1998 A reassessment of the effect of body mass upon flight speed and predation risk in birds. Anim. Behav. 56, 883-889. (doi:10.1006/anbe.1998.0880)
110. Verhulst, S. & Hogstad, O. 1996 Social dominance and energy reserves in flocks of willow tits. J. Avian Biol. 27, 203-208.
111. Welton, N. J., Houston, A. I., Ekman, J. & McNamara, J. M. 2002 A dynamic model of hypothermia as an adaptive response by small birds to winter conditions. Acta Biotheor. 50, 39-56. (doi:10.1023/A: 1014761227478)
112. Witter, M. S. & Cuthill, I. C. 1993 The ecological cost of avian fat storage. Phil. Trans. R. Soc. B 340, 73-92.
113. Witter, M. S. & Swaddle, J. P. 1995 Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris. Behav. Ecol. 6, 343-348.
114. Witter, M. S. & 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. (doi:10.1046/j.1365-2435.1997.00041.x)
115. Witter, M. S., Cuthill, I. C. & Bonser, R. H. C. 1994 Experimental investigations of mass-dependent predation risk in the European starling, Sturnus vulgaris. Anim. Behav. 48, 201-222. (doi:10.1006/anbe. 1994.1227)
116. Witter, M. S., Swaddle, J. P. & Cuthill, I. C. 1995 Periodic food availability and strategic regulation of body mass in the European starling, Sturnus vulgaris. Funct. Ecol. 9, 568-574.