Extreme endurance flights by landbirds crossing the Pacific Ocean: Ecological corridor rather than barrier?

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1656, 2009, Pages 447-457

  Gill Jr , Robert E ^a   Tibbitts, T Lee ^a   Douglas, David C ^a   Handel, Colleen M ^a   Mulcahy, Daniel M ^a   Gottschalck, Jon C ^b   Warnock, Nils ^c,h   McCaffery, Brian J ^d   Battley, Philip F ^e,i   Piersma, Theunis ^f,g  

^a U S GEOLOGICAL SURVEY   (United States)

^b NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

^c PRBO CONSERVATION SCIENCE   (United States)

^d Yukon Delta National Wildlife Refuge   (United States)

^e UNIVERSITY OF AUCKLAND   (New Zealand)

^f ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^g UNIVERSITY OF GRONINGEN   (Netherlands)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ MASSEY UNIVERSITY   (New Zealand)

Author keywords

Bar tailed godwit; Climate change; Endurance exercise; Migration; Satellite telemetry; Weather

Indexed keywords

BREEDING SITE; CLIMATE CHANGE; FLIGHT BEHAVIOR; MIGRATION; SATELLITE IMAGERY; TRACKING; WADER; WEATHER;

ANIMAL EXPERIMENT; ARTICLE; BIRD; CLIMATE; DEHYDRATION; ECOLOGY; ENDURANCE; FEMALE; FLIGHT; MALE; NONHUMAN; PACIFIC OCEAN; PERFORMANCE; PHENOTYPE; PHYSIOLOGY; PRIORITY JOURNAL; SHOREBIRD; SLEEP; SURVIVAL RATE; TELEMETRY; VERTEBRATE;

PACIFIC OCEAN;

ANIMALIA; AVES; LIMOSA LAPPONICA; LIMOSA LAPPONICA BAUERI; VERTEBRATA;

EID: 58149137307     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1142     Document Type: Article

References (88)

1. Alerstam, T. 1990 Bird migration. Cambridge, UK: Cambridge University Press.
2. Alerstam, T. 2001 Detours in bird migration. J. Theor. Biol. 209, 319-331.
3. Alerstam, T. & Hedenström, A. 1998 The development of bird migration theory. J. Avian Biol. 29, 343-369.
4. Alerstam, T. & Lindström, Å. 1990 Optimal bird migration: the relative importance of time, energy, and safety. In Bird migration: physiology and ecophysiology (ed. E. Gwinner), pp. 331-351. Heidelberg, Germany: Springer.
5. Alerstam, T. et al. 2007 A polar system of intercontinental bird migration. Proc. R. Soc. B 274, 2523-2530.
6. Apanius, V. 1998 Stress and immune defense. Adv. Stud. Behav. 27, 133-153.
7. Ashcroft, F. 2000 Life at the extremes: the science of survival. Berkeley, CA: University of California Press.
8. Barter, M. & Wang, T. H. 1990 Can waders fly non-stop from Australia to China? Stilt 17, 36-39.
9. Batschelet, E. 1981 Circular statistics in biology. New York, NY: Academic Press.
10. Battley, P. F. & Piersma, T. 2005 Body composition and flight ranges of bar-tailed godwits (Limosa lapponica baueri) from New Zealand. Auk 122, 922-937.
11. Battley, P. F., Piersma, T., Dietz, M. W., Tang, S., Dekinga, A. & Hulsman, K. 2000 Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc. R. Soc. B 267, 191-195.
12. Bengtsson, L., Hodges, K. & Roeckner, E. 2006 Storm tracks and climate change. J. Clim. 19, 3518-3543.
13. Berthold, P., Gwinner, E. & Sonnenschein, E. (eds) 2003 Avian migration. Berlin, Germany: Springer.
14. Brower, W. A., Baldwin, R. G., Williams, C. N., Wise, J. L. & Leslie, L. D. 1988 Climatic atlas of the Outer Continental Shelf waters and coastal regions of Alaska. Bering Sea, vol. II. Anchorage, AK: University of Alaska, Arctic Environmental Information and Data Center.
15. Clapp, R. B. & Sibley, F. C. 1967 New records of birds from the Phoenix and Line Islands. Ibis 109, 122-125.
16. Cotton, P. A. 2003 Avian migration phenology and global climate change. Proc. Natl Acad. Sci. USA 100, 12 219-12 222.
17. Culik, B., Bannasch, R. & Wilson, R. 1994 External devices on penguins: how important is shape? Mar. Biol. 118, 353-357.
18. Derksen, D., Bollinger, K., Ward, D., Sedinger, J. & Miyabayashi, Y. 1996 Black brant from Alaska staging and wintering in Japan. Condor 98, 653-657.
19. Dewasmes, G., Cohen-Adad, F., Koubi, H. & Le Maho, Y. 1984 Sleep changes in long-term fasting geese in relation to lipid and protein metabolism. Am. J. Physiol. 247, R663-R671.
20. Dewasmes, G., Buchet, C., Geloen, A. & Le Maho, Y. 1989 Sleep changes in emperor penguins during fasting. Am. J. Physiol. 256, R476-R480.
21. Driscoll, P. V. & Ueta, M. 2002 The migration route and behaviour of eastern curlews Numenius madagascariensis. Ibis 144, E119-E130.
22. Gauthreaux, S. A. 1999 Neotropical migrants and the Gulf of Mexico: the view from aloft. In Gatherings of angels: migrating birds and their ecology (ed. K. P. Able), pp. 27-49. Ithaca, NY: Cornell University Press.
23. Gessaman, J. A., Workman, G. A. & Fuller, M. P. 1991 Flight performance, energetics and water turnover in tippler pigeons with harness and dorsal load. Condor 93, 546-554.
24. Gill Jr, R. E., Piersma, T., Hufford, G., Servranckx, R. & Riegen, A. 2005 Crossing the ultimate ecological barrier: evidence for an 11 000-km-long nonstop flight from Alaska to New Zealand and eastern Australia by bar-tailed godwits. Condor 107, 1-20.
25. Green, M. 2003 Flight strategies in migrating birds: when and how to fly. PhD dissertation, Department of Ecology, Lund University, Sweden.
26. Hamilton, T. D., Reed, K. M. & Thorson, R. M. 1986 Glaciation in Alaska: introduction and overview. In Glaciation in Alaska - the geologic record (eds T. Hamilton, K. Reed & R. Thorson), pp. 1-8. Anchorage, AK: Alaska Geological Society.
27. Hammond, K. A. & Diamond, J. 1997 Maximal sustained energy budgets in humans and animals. Nature 396, 457-462.
28. Hanson, B., Klink, K., Matsuura, K., Robeson, S. & Willmott, C. 1992 Vector correlation: review, exposition, and geographic application. Ann. Assoc. Am. Geogr. 82, 103-116.
29. Hasselquist, D., Lindström, Å., Jenni-Eiermann, S., Koolhaas, A. & Piersma, T. 2007 Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment. J. Exp. Biol. 210, 1123-1131.
30. Hedenström, A. 2008 Adaptations to migration in birds: behavioural strategies, morphology and scaling effects. Phil. Trans. R. Soc. B 363, 287-299.
31. Hedenström, A. & Alerstam, T. 1997 Optimal fuel loads in migratory birds: distinguishing between time and energy minimization. J. Theor. Biol. 189, 227-234.
32. Heusser, C. J., Heusser, L. E. & Peteet, D. M. 1985 Late-Quaternary climatic change on the American Pacific Coast. Nature 315, 485-487.
33. Houston, A. I. 1998 Models of optimal avian migration: state, time and predation. J. Avian Biol. 29, 395-404.
34. Kalnay, E. M. et al. 1996 The NCEP/NCAR 40-year reanalysis project. Bull. Am. Meteorol. Soc. 77, 437-471.
35. Kaspar, F., Spangehl, T. & Cubasch, U. 2007 Northern hemisphere winter storm tracks of the Eemian interglacial and the last glacial inception. Clim. Past 3, 181-192.
36. Klaassen, M. 2004 May hydration risk govern long-distance migratory behaviour? J. Avian Biol. 35, 4-6.
37. Korschgen, C., Kenow, K., Gendron-Fitzpatrick, A., Green, W. & Dein, F. 1996 Implanting intra-abdominal radiotransmitters with external whip antennas in ducks. J. Wildl. Manage. 60, 132-137.
38. Kvist, A., Lindström, Å., Green, M., Piersma, T. & Visser, G. H. 2001 Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413, 730-732.
39. Landys, M. M., Piersma, T., Visser, G. H., Jukema, J. & Wijker, A. 2000 Water balance during real and simulated long-distance migratory flight in the bar-tailed godwit. Condor 102, 645-652.
40. Landys-Ciannelli, M. M., Piersma, T. & Jukema, J. 2003 Strategic size changes of internal organs and muscle tissue in the bar-tailed godwit during fat storage on a spring stopover site. Funct. Ecol. 17, 151-159.
41. Lank, D., Butler, R., Ireland, J. & Ydenberg, R. 2003 Effects of predation danger on migration strategies of sandpipers. Oikos 103, 303-319.
42. Liechti, F. 2006 Birds: blowin' by the wind? J. Ornithol. 147, 202-211.
43. Liechti, F., Klaassen, M. & Bruderer, B. 2000 Predicting migratory flight altitude by physiological migration models. Auk 117, 205-214.
44. Lind, J. & Cresswell, W. 2006 Anti-predation behaviour during bird migration: the benefit of studying multiple behavioural dimensions. J. Ornithol. 147, 310-316.
45. Löptien, U., Zolina, O., Gulev, S., Latif, M. & Soloviov, V. 2008 Cyclonic life cycle characteristics over the Northern Hemisphere in coupled GCMs. Clim. Dynam. 31, 507.
46. MacMynowski, D. P. & Root, T. L. 2007 Climate and complexity of migratory phenology: sexes, migratory distance, and arrival distribution. Int. J. Biometeorol. 51, 361-373.
47. MAP Program 2007 MODELING, ANALYSIS, AND PREDICTIVE (MAP) Program. Goddard Earth Observing System Model, v. 5 (GEOS-5), NASA. See http://gmao.gsfc.nasa.gov/pubs/docs/GEOS-5.0. 1_Documentation_r3.pdf/.
48. McCabe, G., Clark, M. P. & Serreze, M. C. 2001 Trends in northern hemisphere surface cyclone frequency and intensity. J. Clim. 14, 2763-2768.
49. McCaffery, B. J. & Gill Jr, R. E. 2001 The bar-tailed godwit. In The birds of North America (eds A. Poole & F. Gill), no. 581. Philadelphia, PA: The Academy of Natural Sciences, and Washington, DC: American Ornithologists Union.
50. Meltofte, H. et al. 2007 Effects of climate variation on the breeding ecology of Arctic shorebirds. Med. Grønland Biosci. 59, 1-48.
51. Mendes, L., Piersma, T., Hasselquist, D., Matson, K. D. & Ricklefs, R. E. 2006 Variation in the innate and acquired arms of the immune system among five shore bird species. J. Exp. Biol. 209, 1105-1109.
52. Møller, A. P. & Erritzøe, J. 1998 Host immune defence and migration in birds. Evol. Ecol. 12, 945-953.
53. Morrison, R. I. G., Davidson, N. C. & Piersma, T. 2005 Transformations at high latitudes: why do red knots bring body stores to the breeding grounds? Condor 107, 449-457.
54. Mulcahy, D. & Esler, D. 1999 Surgical and immediate post-release mortality of harlequin ducks (Histrionicus histrionicus) implanted with abdominal radio transmitters with percutaneous antennae. J. Zoo Wildl. Med. 30, 397-401.
55. Newton, I. 2008 The migration ecology of birds. Oxford, UK: Academic Press.
56. Norris, K. & Evans, M. R. 2000 Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-26.
57. Obrecht III, H. H., Pennycuick, C. J. & Fuller, M. R. 1988 Wind tunnel experiments to assess the effect of backmounted radio transmitters on bird body drag. J. Exp. Biol. 135, 265-273.
58. Owen, J. C. & Moore, F. R. 2006 Seasonal differences in immunological condition of three species of thrushes. Condor 108, 389-398.
59. Pennycuick, C. J. 1998 Computer simulation of fat and muscle burn in long-distance bird migration. J. Theor. Biol. 191, 47-61.
60. Pennycuick, C. J. & Battley, P. F. 2003 Burning the engine: a time-marching computation of fat and protein consumption in a 5420 km non-stop flight by great knots Calidris tenuirostris. Oikos 103, 323-332.
61. Peterson, C. C., Nagy, K. A. & Diamond, J. 1990 Sustained metabolic scope. Proc. Natl Acad. Sci. USA 87, 2324-2328.
62. Piersma, T. 1997 Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80, 623-631.
63. Piersma, T. 2007 Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J. Ornithol. 148(Suppl.), S45-S59.
64. Piersma, T. & Drent, J. 2003 Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228-233.
65. Piersma, T. & Gill Jr, R. E. 1998 Guts don't fly: small digestive organs in obese bar-tailed godwits. Auk 115, 196-203.
66. Piersma, T. & Poot, M. 1993 Where waders may parallel penguins: spontaneous increase in locomotor activity triggered by fat depletion in a voluntarily fasting knot. Ardea 81, 1-8.
67. Pinto, J. G. et al. 2007 Changes in storm track and cyclone activity in three SRES ensemble experiments with the ECHAM5/MPI-0M1 GCM. Clim. Dynam. 29, 195-210.
68. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. 1998 On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. B 265, 1637-1641.
69. Raible, C. C. 2007 On the relation between extreme midlatitude cyclones and the atmospheric circulation using ERA40. Geophys. Res. Lett. 34, L07703.
70. Rattenborg, N. C. et al. 2004 Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii ). PLoS Biol. 2, 924-936.
71. Robin, J.-P., Groscolas, R. & Le Maho, Y. 1987 Anorexie animale: existence d'un 'signal d'alarme interne' anticipant la déplétion des réserves énergétiques. Bull. Soc. Ecophysiol. 12, 25-29.
72. Salathé Jr, E. P. 2006 Influences of a shift in North Pacific storm tracks on western North American precipitation under global warming. Geophys. Res. Lett. 33, L19820.
73. Sandberg, R. & Holmquist, B. 1998 Orientation and long-distance migration routes: an attempt to evaluate compass cue limitations and required precision. J. Avian Biol. 29, 626-636.
74. SAS Institute, Inc. 2004 SAS OnlineDoc 9.1.2. Cary, NC: SAS Institute Inc. See http://support.sas.com/onlinedoc/912/docMainpage.jsp.
75. Schmaljohann, H., Liechti, F. & Bruderer, B. 2007 Songbird migration across the Sahara: the non-stop hypothesis rejected! Proc. R. Soc. B 274, 735-739.
76. Schmaljohann, H., Bruderer, B. & Liechti, F. 2008 Sustained bird flights occur at temperatures beyond expected limits of water loss. Anim. Behav. 76, 1133-1138.
77. Schmid-Hempel, P. 2003 Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B 270, 357-366.
78. Shamoun-Baranes, J., van Loon, E., Liechti, F. & Bouten, W. 2006 Analyzing the effect of wind on flight: pitfalls and solutions. J. Exp. Biol. 210, 82-90.
79. Sillett, T. S. & Holmes, R. T. 2002 Variation in survivorship of a migratory songbird throughout its annual cycle. J. Anim. Ecol. 71, 296-308.
80. Stöckli, R., Vermote, E., Saleous, N., Simmon, R. & Herring, D. 2005 The Blue Marble Next Generation - a true color earth dataset including seasonal dynamics from MODIS (NASA Earth Observatory). See http:// earthobservatory.nasa.gov/Newsroom/BlueMarble.
81. Terry, J. P. 2007 Tropical cyclones: climatology and impacts in the South Pacific. New York, NY: Springer.
82. White, C. M. 1994 Species accounts. In Handbook of the birds of the world (eds J. del Hoyo, A. Elliott & J. Sargatal ), vol. 2, pp. 106-275. Barcelona, Spain: Lynx Edicions.
83. Williams, T. C. & Williams, J. M. 1999 The migration of birds over the Pacific Ocean. In Acta XXII Cong. Int. Ornithologici, Durban, South Africa (eds N. Adams & R. Slotow), pp. 1948-1957. Johannesburg, South Africa: BirdLife South Africa.
84. Wilson, J. G. & Overland, J. E. 1986 Meteorology. In Gulf of Alaska: physical environment and biological resources (eds D. W. Hood & S. T. Zimmerman), pp. 31-54. Washington, DC: Government Printing Office, and Anchorage, AK: U.S. Minerals Management Service, Ocean Assessments Division, OCS study, MMS86-0095.
85. Wilson, J. R., Nebel, S. & Minton, C. D. T. 2007 Migration ecology and morphometrics of two bar-tailed godwit populations in Australia. Emu 107, 262-274.
86. Yanase, W. & Abe-Ouchi, A. 2007 The LGM surface climate and atmospheric circulation over East Asia and the North Pacific in the PMIP2 coupled model simulations. Clim. Past 3, 439-451.
87. Ydenberg, R. C., Butler, R. W. & Lank, D. B. 2007 Effects of predator landscapes on the evolutionary ecology of routing, timing and molt by long-distance migrants. J. Avian Biol. 38, 523-529.
88. Yin, J. H. 2005 A consistent poleward shift of the storm tracks in simulations of 21st century climate. Geophys. Res. Lett. 32, L18701.