Rapid loss of fat but not lean mass prior to chick provisioning supports the flight efficiency hypothesis in tree swallows

Functional Ecology

Volumn 26, Issue 4, 2012, Pages 895-903

  Boyle, W Alice ^a,c   Winkler, David W ^b   Guglielmo, Christopher G ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b Fuller Evolutionary Biology Program   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Body composition; Condition; Energetic stress; Flight efficiency; Gonadal regression; Incubation; Mass loss; Quantitative magnetic resonance; Tachycineta bicolor

Indexed keywords

BODY CONDITION; BODY MASS; ENERGETICS; FAT; HYPOTHESIS TESTING; INCUBATION; NESTLING; PASSERINE; PHYSIOLOGICAL RESPONSE; POULTRY; QUANTITATIVE ANALYSIS; TREE;

AVES; TACHYCINETA; TACHYCINETA BICOLOR;

EID: 84864025391     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2012.01997.x     Document Type: Article

References (62)

1. Blem, C.R. (1976) Patterns of lipid storage and utilization in birds. American Zoologist, 16, 671-684.
2. Blem, C.R. & Blem, L.B. (2006) Variation in mass of female Prothonotary Warblers during nesting. Wilson Journal of Ornithology, 118, 3-12.
3. Bowlin, M.S. & Winkler, D.W. (2004) Natural variation in flight performance is related to timing of breeding in Tree Swallows (Tachycineta bicolor) in New York. Auk, 121, 345-353.
4. Brown, R.E. & Saunders, D.K. (1998) Regulated changes in body mass and muscle mass in molting Blue-winged Teal for an early return to flight. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 76, 26-32.
5. Burness, G.P., Ydenberg, R.C. & Hochachka, P.W. (2001) Physiological and biochemical correlates of brood size and energy expenditure in Tree Swallows. Journal of Experimental Biology, 204, 1491-1501.
6. Cichón, M. (2001) Body mass changes in female Collared Flycatchers: state-dependent strategy. Auk, 118, 550-552.
7. Conway, C.J. & Martin, T.E. (2000) Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution, 54, 670-685.
8. Curlee, A.P. & Beissinger, S.R. (1995) Experimental analysis of mass change in female Green-Rumped Parrotlets (Forups passerinus): the role of male cooperation. Behavioral Ecology, 6, 192-198.
9. DeSteven, D. (1980) Clutch size, breeding success, and parental survival in the Tree Swallow (Iridoprocne bicolor). Evolution, 34, 278-291.
10. Dietz, M.W., Piersma, T. & Dekinga, A. (1999) Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. Journal of Experimental Biology, 202, 2831-2837.
11. Elliott, K.H., Jacobs, S.R., Ringrose, J., Gaston, A.J. & Davoren, G.K. (2008) Is mass loss in Brünnich's Guillemots Uria lomvia an adaptation for improved flight performance or improved dive performance? Journal of Avian Biology, 39, 619-628.
12. Freed, L.A. (1981) Loss of mass in breeding wrens: stress or adaptation? Ecology, 62, 1179-1186.
13. Gerson, A.R. & Guglielmo, C.G. (2011) House sparrows (Passer domesticus) increase protein catabolism in response to water restriction. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 300, R925-R930.
14. Gosler, A.G., Greenwood, J.J.D. & Perrins, C. (1995) Predation risk and the cost of being fat. Nature, 377, 621-623.
15. Guglielmo, C.G. & Williams, T.D. (2003) Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the western sandpiper (Calidris mauri). Physiological and Biochemical Zoology, 76, 84-98.
16. Guglielmo, C.G., McGuire, L.P., Gerson, A.R. & Seewagen, C.L. (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. Journal of Ornithology, 152, S75-S85.
17. Hasselquist, D., Wasson, M.F. & Winkler, D.W. (2001) Humoral immunocompetence correlates with date of egg-laying and reflects work load in female Tree Swallows. Behavioral Ecology, 12, 93-97.
18. de Heij, M.E., van der Graaf, A.J., Hafner, D. & Tinbergen, J.M. (2007) Metabolic rate of nocturnal incubation in female great tits, Parus major, in relation to clutch size measured in a natural environment. Journal of Experimental Biology, 210, 2006-2012.
19. van den Hout, P.J., Mathot, K.J., Maas, L.R.M. & Piersma, T. (2010) Predator escape tactics in birds: linking ecology and aerodynamics. Behavioral Ecology, 21, 16-25.
20. Hussell, D.J.T. (1983) Age and plumage color in female Tree Swallows. Journal of Field Ornithology, 54, 312-318.
21. Jones, I.L. (1994) Mass changes of Least Auklets Aethia pusilla during the breeding season: evidence for programmed loss of mass. Journal of Animal Ecology, 63, 71-78.
22. Karasov, W.H. & Martínez del Río, C. (2007) Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins. Princeton University Press, Princeton, NJ.
23. Lindstrom, A., Kvist, A., Piersma, T., Dekinga, A. & Dietz, M.W. (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. Journal of Experimental Biology, 203, 913-919.
24. Martin, T.E. (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecological Mongraphs, 65, 101-127.
25. McCarty, J.P. (1995) Effects of short-term changes in environmental conditions on the foraging ecology and reproductive success of Tree Swallows, Tachycineta bicolor. Ph.D. thesis, Cornell University.
26. McCarty, J.P. (2001) Variation in growth of nestling tree swallows across multiple temporal and spatial scales. Auk, 118, 176-190.
27. McCarty, J.P. & Winkler, D.W. (1999a) Foraging ecology and diet selectivity of tree swallows feeding nestlings. Condor, 101, 246-254.
28. McCarty, J.P. & Winkler, D.W. (1999b) Relative importance of environmental variables in determining the growth of nestling Tree Swallows Tachycineta bicolor. Ibis, 141, 286-296.
29. Merilä, J. & Wiggins, D.A. (1997) Mass loss in breeding Blue Tits: the role of energetic stress. Journal of Animal Ecology, 66, 452-460.
30. Merkle, M.S. & Barclay, R.M.R. (1996) Body mass variation in breeding Mountain Bluebirds Sialia currucoides: evidence of stress or adaptation for flight? Journal of Animal Ecology, 65, 401-413.
31. Moreno, J. (1989) Strategies of mass change in breeding birds. Biological Journal of the Linnean Society, 37, 297-310.
32. Moreno, J., Potti, J. & Merino, S. (1997) Parental energy expenditure and offspring size in the pied flycatcher Ficedula hypoleuca. Oikos, 79, 559-567.
33. Murphy, M.T., Armbrecth, B., Vlamis, E. & Pierce, A. (2000) Is reproduction by Tree Swallows cost free? Auk, 117, 902-912.
34. Nagy, L.R., Stanculescu, D. & Holmes, R.T. (2007) Mass loss by breeding female songbirds: food supplementation supports energetic stress hypothesis in Black-throated Blue Warblers. Condor, 109, 304-311.
35. Niizuma, Y., Takahashi, A., Sasaki, N., Hayama, S., Tokita, N. & Watanuki, Y. (2001) Benefits of mass reduction for commuting flight with heavy food load in Leach's storm-petrel, Oceanodroma leucorhoa. Ecological Research, 16, 197-203.
36. Norberg, R.A. (1981) Weight decrease in breeding birds may result in more fledged young. American Naturalist, 118, 838-850.
37. Parejo, D. & Danchin, E. (2006) Brood size manipulation affects frequency of second clutches in the Blue Tit. Behavioral Ecology and Sociobiology, 60, 184-194.
38. Peig, J. & Green, A.J. (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos, 118, 1883-1891.
39. Petersen, A.J. (1955) The breeding cycle in the Bank Swallow. Wilson Bulletin, 67, 235-286.
40. Portugal, S.J., Green, J.A. & Butler, P.J. (2007) Annual changes in body mass and resting metabolism in captive barnacle geese (Branta leucopsis): the importance of wing moult. Journal of Experimental Biology, 210, 1391-1397.
41. Portugal, S.J., Butler, P.J., Green, J.A. & Cassey, P. (2011) Indications of phenotypic plasticity in moulting birds: captive geese reveal adaptive changes in mineralisation of their long bones during wing moult. Journal of Ornithology, 152, 1055-1061.
42. Potti, J. & Merino, S. (1995) Female mass losses are related to male age and body condition in the Pied Flycatcher Ficedula hypoleuca. Ardeola, 42, 173-181.
43. Racey, P.A. & Tam, W.H. (1974) Reproduction in male Pipistrellus pipistrellus (Mammalia: Chiroptera). Journal of Zoology, 172, 101-122.
44. Reid, J.M., Monaghan, P. & Ruxton, G.D. (2000) Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation. Proceedings of the Royal Society of London Series B-Biological Sciences, 267, 37-41.
45. Ricklefs, R.E. (1974) Energetics of reproduction in birds. Avian Energetics (ed. R.A. Paynter ), pp. 152-292. Nuttal Ornith. Club, No. 15, Cambridge, Mass., USA.
46. Schamber, J.L., Esler, D. & Flint, P.L. (2009) Evaluating the validity of using unverified indices of body condition. Journal of Avian Biology, 40, 49-56.
47. Schwilch, R., Grattarola, A., Spina, F. & Jenni, L. (2002) Protein loss during long-distance migratory flight in passerine birds: adaptation and constraint. Journal of Experimental Biology, 205, 687-695.
48. Slagsvold, T. & Johansen, M.A. (1998) Mass loss in female Pied Flycatchers Ficedula hypoleuca during late incubation: supplementation fails to support the reproductive stress hypothesis. Ardea, 86, 203-211.
49. Sokal, R.R. & Rohlf, F.J. (1995) Biometry, 3rd edn. Freeman & Hall, New York, NY.
50. Stearns, S.C. (1976) Life-history tactics: a review of ideas. Quarterly Review of Biology, 51, 3-47.
51. Steel, E.A. & Hinde, R.A. (1963) Hormonal control of brood patch and oviduct development in domesticated Canaries. Journal of Endocrinology, 26, 11-24.
52. Turner, J.S. (1994) Thermal impedance of a contact-incubated birds egg. Journal of Thermal Biology, 19, 237-243.
53. Vézina, F. & Salvante, K.G. (2010) Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction. Current Zoology, 56, 767-792.
54. Vézina, F. & Williams, T.D. (2003) Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiological and Biochemical Zoology, 76, 716-730.
55. Visser, M.E. & Lessells, C.M. (2001) The costs of egg production and incubation in Great Tits (Parus major). Proceedings of the Royal Society of London Series B-Biological Sciences, 268, 1271-1277.
56. Ward, S. & Bryant, D.M. (2006) Barn swallows Hirundo rustica form eggs mainly from current food intake. Journal of Avian Biology, 37, 179-189.
57. Weimerskirch, H., Le Corre, M., Ropert-Coudert, Y., Kato, A. & Marsac, F. (2006) Sex-specific foraging behaviour in a seabird with reversed sexual dimorphism: the Red-footed Booby. Oecologia, 146, 681-691.
58. Williams, J.B. (1988) Field metabolism of Tree Swallows during the breeding season. Auk, 105, 706-714.
59. Winkler, D.W. & Allen, P.E. (1995) Effects of handicapping on female condition and reproduction in Tree Swallows (Tachycineta bicolor). Auk, 112, 737-747.
60. Winkler, D.W. & Allen, P.E. (1996) The seasonal decline in Tree Swallow clutch size: physiological constraint or strategic adjustment? Ecology, 77, 922-932.
61. Winkler, D.W., Hallinger, K.K., Ardia, D.R., Robertson, R.J., Stuchbury, B.J. & Cohen, R.R. (2011) Tree Swallow (Tachycineta bicolor). The Birds of North America Online (ed. A. Poole ). Cornell Lab of Ornithology, Ithaca, NY. doi:
62. Witter, M.S. & Cuthill, I.C. (1993) The ecological costs of avian fat storage. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 340, 73-92.