Uso de isótopos estables para determinar conectividad migratoria en aves: alcances y limitaciones

Julián Torres Dowdall; Adrian Farmer; Enrique H. Bucher

doi:10.56178/eh.v21i2.789

Articles Published 01 December 2006 https://doi.org/10.56178/eh.v21i2.789

Using stable isotopes to determine migratory connectivity in birds: extent and limitations

deuterium isotopic variability migratory birds natural markers

Julián Torres Dowdall Programa de Maestría en Manejo de Vida Silvestre, Universidad Nacional de Córdoba. CC 122, 5000 Córdoba, Córdoba, Argentina | Department of Biology, Colorado State University. Fort Collins, EEUU

Adrian Farmer US Geological Survey, Fort Collins Science Center. 2150 Centre Avenue, Building C, Fort Collins, CO 80526-8118, EEUU

Enrique H. Bucher Centro de Zoología Aplicada, Universidad de Córdoba. CC 122, 5000 Córdoba, Córdoba, Argentina

Abstract

The need to unravel migratory connectivity in different bird species has generated the development of several techniques to determine the geographical origin of individuals. Using the stable isotopes composition of animal tissues is one of the emerging techniques that had the greatest development. The principles of the technique are, first, that there is a geographical pattern in stable isotopes values, as a result of natural and anthropogenic processes, and, second, that stable isotopes are assimilated when an organism eats, and eventually they become fixed in animal tissues, in proportions related to the natural abundance in the environment. The most commonly used tissue is from flight feathers, since they incorporate the stable isotope composition of the food and, once moult is finished, they stay metabolically inactive until they are replaced. Although this technique has been applied with success in several species, variability found within birds from the same origin limits its potential accuracy. This variability could be the result of different processes affecting the isotopic change between food and tissues of the target species, winter movements, or baseline changes through time (temporal changes in the hydrogen isotopic values in precipitation). A better understanding of the sources of error would help to design better studies in order to minimize variability and to develop better models to determine the geographic origin of individual birds.

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References

ATKINSON PW, BAKER AJ, BEVAN RM, CLARK NA, COLEKB, GONZÁLEZ PM, NEWTON J, NILES LJ Y ROBINSONRA (2005)Unravelling the migration and moultstrategies of a long-distance migrant using stableisotopes: Red Knot Calidris canutus movements inthe Americas. Ibis 147:738–739
BAIRLEIN F (2001) Results of bird ringing in the studyof migration routes. Ardea 89:7–19
BEARHOP S, ADAMS CE, WALDORN S, FULLER RA YMACLEOD H (2004) Determining trophic nichewidth: a novel approach using stable isotope analy-sis. Journal of Animal Ecology 73:1007–1012
BEARHOP S, WALDRON S, VOTIER SC Y FURNESS RW(2002) Factors that influence assimilation rates andfractionation of nitrogen and carbon isotopes inavian blood and feathers. Physiological and Biochemi-cal Zoology 75:451–458
BOWEN GJ, WASSENAAR LI Y HOBSON KA (2005) Globalapplication of stable hydrogen and oxygen isotopesto wildlife forensics. Oecologia 143:337–348
BOWEN GJ Y WILKINSON B (2002) Spatial distributionof δ18O in meteoric precipitation. Geology 30:315–318
CARLETON SA Y MARTINEZDEL RIO C (2005) The effectof cold-induced increased metabolic rate on the rateof 13C and 15N incorporation in house sparrows(Passer domesticus). Oecologia 144:226–232
CHAMBERLAIN CP, BLUM JD, HOLMES RT, XIAHONG F,SHERRY TW Y GRAVES GR (1997) The use of isotopetracers for identifying populations of migratorybirds. Oecologia 109:132–141
DAANSGARD W (1964) Stable isotopes in precipitation.Tellus 16:436–468
DENIRO MJ Y EPSTEIN S (1981) Influence of diet on thedistribution of nitrogen isotopes in animals.Geochimica et Cosmochimica Acta 45:341–351
EHLERINGER JR Y RUNDEL PW (1989) Stable isotopes:history, units, and instrumentation. Pp. 1–17 en: RUN-DEL PW, EHLERINGER JR Y NAGY KA (eds) Stable isoto-pes in ecological research. Springer-Verlag, Nueva York
ELSDON T Y GILLANDERS B (2003) Reconstructing mi-gratory patterns of fish based on environmentalinfluences on otolith chemistry. Reviews in FishBiology and Fisheries 13:219–235
EVANS-OEGEN L, HOBSON KA Y LANK DB (2004) Bloodisotopic (δ13C and δ15N) turnover and diet-tissuefractionation factors in captive Dunlin: implicationsfor dietary analysis of wild birds. Auk 121:170–177
FARMER A, ABRIL M, FERNÁNDEZ M, TORRES J, KESTER CY BERN C (2004) Using stable isotopes to associatemigratory shorebirds with their wintering locationsin Argentina. Ornitología Neotropical 15:377–384
FARMER AH, RYE R, LANDIS G, BERN C, KESTER C YRIDLEY I (2003) Tracing the pathways of neotropicalmigratory shorebirds using stable isotopes: a pilotstudy. Isotopes in Environmental and Health Studies39:169–177
GANNES LZ, O’BRIEN D Y MARTINEZDEL RIO C (1997)Stable isotopes in animal ecology: assumptions, ca-veats, and a call for more laboratory experiments.Ecology 78:1271–1276
GAYE-SIESSEGGER J, FOCKEN U, ABEL H-J Y BECKER K(2003) Feeding level and diet quality influencetrophic shift of C and N isotopes in Nile Tilapia(Oreochromis nicoticus (L.)). Isotopes in Environmentaland Health Studies 39:125–134
GUY R, FOGEL M Y BERRY J (1993) Photosynthetic frac-tionation of the stable isotopes of oxygen andcarbon. Plant Physiology 101:37–47
HANDLY L, AUSTIN A, ROBINSON D, SCRIMGEOUR C,RAVEN J, HEATON T, SCHMIDT S Y STEWART G (1999)The 15N natural abundance (δ15N) of ecosystemsamples reflects measures of water availability.Austral Journal of Plant Physiology 26:185–199
HEBERT CE Y WASSENAAR LI (2001) Stable nitrogen iso-topes in waterfowl feathers reflect agricultural landuse in western Canada. Environmental Science andTechnology 35:3482–3487
HOBSON KA (1999) Tracing origins and migration ofwildlife using stable isotopes: a review. Oecologia120:314–326
HOBSON KA (2002) Making migratory connectionswith stable isotopes. Pp. 379–391 en: BERTHOLD P YGWINNER P (eds) Avian migration. Springer-Verlag,Berlín
HOBSON KA (2005a) Stable isotopes and the determi-nation of avian migratory connectivity and seasonalinteractions. Auk 122:1037–1048
HOBSON KA (2005b) Flying fingerprints: making con-nections with stable isotopes and trace elements.Pp. 235–246 en: GREENBERG R Y MARRA PP (eds) Birdsof two worlds: the ecology and evolution of migration.Johns Hopkins University Press, Baltimore
HOBSON KA, ALISAUSKAS RT Y CLARK RG (1993)Stable isotope nitrogen isotope enrichment inavian tissue due to fasting and nutritional stress:implications for isotopic analyses of diet. Condor101:799–805
HOBSON KA, AUBRY Y Y WASSENAAR LI (2004a) Migra-tory connectivity in Bicknell’s Thrush: locatingmissing populations with hydrogen isotopes.Condor 106:905–909
HOBSON KA Y BAIRLEIN F (2003) Isotopic discrimina-tion and turnover in captive Garden Warblers (Sylviaborin): implications for delineating dietary and mi-gratory associations in wild passerines. CanadianJournal of Zoology 81:1630–1635
HOBSON KA, BOWEN GJ, WASSENAAR LI, FERRAND Y YLORMEE H (2004b) Using stable hydrogen and oxy-gen isotopes measurements to infer geographicalorigins of migrating European birds. Oecologia141:477–488
HOBSON KA Y CLARK RG (1992) Assessing avian dietsusing stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197
HOBSON KA Y WASSENAAR L (1997) Linking breedingand wintering grounds of neotropical migrant song-birds using stable hydrogen isotopic analysis offeathers. Oecologia 109:142–148
IAEA (2001) Global Network of Isotopes in Precipitation(GNIP) and Isotope Hydrology Information System(ISOHIS).International Atomic Energy Agency,Viena (URL: http://isohis.iaea.org/)
KELLY JF, ATUDOREI V, SHARP ZD Y FINCH DM (2002)Insights into Wilson’s Warbler migration from analysesof hydrogen stable-isotope ratios. Oecologia 130:216–221
KELSALL JP (1970) Chemical elements in waterfowlflight feathers. Canadian Wildlife Service 19:1–11
KELSALL JP Y BURTON R (1977) Identification of originsof lesser Snow Geese by X-ray spectrometry. Cana-dian Journal of Zoology 55:718–732
KELSALL JP Y CALAPRIC JR (1972) Chemical content ofwaterfowl plumage as a potential diagnostic tool.Journal of Wildlife Management 36:1088–1097
KENDALL C Y COPLEN TB (2001) Distribution of oxy-gen-18 and deuterium in river waters across theUnited States. Hydrological Processes 15:1363–1393
LAJTHA K Y MARSHALL JD (1994) Sources of variationin the stable isotopic composition of plants. Pp. 1–21en: LAJTHA K Y MICHENER RH (eds) Stable isotopes inecology and environmental sciences. Blackwell Scien-tific Publications, Oxford
LAJTHA K Y MICHENER RH (1994) Stable isotopes in ecol-ogy and environmental sciences. Blackwell ScientificPublications, Oxford
LOTT CA, MEEHAN TD Y HEATH JA (2003) Estimatingthe latitudinal origins of migratory birds usinghydrogen and sulfur stable isotopes in feathers: in-fluence of marine prey base. Oecologia 134:505–510
LOTT CA Y SMITH JP (2006) A GIS approach to esti-mating the origins of migratory raptors in NorthAmerica using hydrogen stable isotope ratios infeathers. Auk 123:822–835
MARRA PP, HOBSON KA Y COLMES T (1998) Linkingwinter and summer events in a migrant passerinebird by using stable-carbon isotope. Science282:1884–1886
MATTHEWS B Y MAZUMDER A (2004) A critical evalua-tion of intrapopulation variation of δ13C and isotopicevidence of individual specialization. Oecologia140:361–371
MEEHAN TD, GIERMAKOWSKI JT Y CRYAN PM (2004) GIS-based model of stable hydrogen isotope ratios inNorth American growing-season precipitation foruse in animal movement studies. Isotopes in Envi-ronmental and Health Studies 40:291–300
MURPHY ME (1996) Energetics and nutrition of molt.Pp. 158–198 en: CAREY C (ed) Avian energetics andnutritional ecology. Chapman & Hall, Nueva York
MYERS JP, MORRISON RIG, ANTAS PZ, HARRINGTON BA,LOVEJOY TE, SALLABERRY M, SENNER SE Y TARAK A(1987) Conservation strategy for migratory species.American Scientist 75:18–26
POAGE MA Y CHAMBERLAIN P (2001) Empirical relation-ships between elevation and the stable isotopecomposition of precipitation and surface waters:considerations for studies of paleoelevation change.American Journal of Science 301:1–15
ROYLE JA Y RUBENSTEIN DR (2004) The role of speciesabundance in determining the breeding origins ofmigratory birds using stable isotopes. EcologicalApplications 14:1780–1788
RUBENSTEIN DR, CHAMBERLAIN CP, HOLMES RT, AYRESMP, WALDBAUER JR, GRAVES GR Y TUROSS NC (2002)Linking breeding and wintering ranges of amigratory songbird using stable isotopes. Science295:1062–1065
RUBENSTEIN DR Y HOBSON KA (2004) From birds tobutterflies: animal movements patterns and stableisotopes. Trends in Ecology and Evolution 19:256–263
RUNDEL PW, EHLERINGER JR Y NAGY KA (1989) Applica-tions of stable isotopes in ecologicalresearch. Springer-Verlag, Nueva York
SILLETT TS, HOLMES RT Y SHERRY TW (2000) Impactsof a global climate cycle on population dynamics ofa migratory songbird. Science 288:2040–2042
STILL CJ, BERRY JA, COLLATZ GJ Y DEFRIES RS (2003)The global distribution of C3 and C4 vegetation:carbon cycle implications. Global BiogeochemicalCycles 17:1006–1029
THORROLD S, LATKOCZY C, SWA RT P Y JONES C (2001)Natal homing in a marine fish metapopulation.Science 291:297–299
TORRES DOWDALL J (2005) Uso de isótopos estables pararelacionar los hábitats estacionales de aves playerasneárticas. Tesis de Maestría, Universidad Nacionalde Córdoba, Córdoba
WASSENAAR L Y HOBSON KA (2000) Stable-carbon andhydrogen isotopes ratios reveal breeding origins ofRed-winged Blackbirds. Ecological Applications10:911–916
WASSENAAR LI Y HOBSON KA (2003) Comparativeequilibration and online technique for determina-tion of non-exchangeable hydrogen of keratins foruse in animal migration studies. Isotopes in Environ-mental and Health Studies 39:1–7
WEBSTER MS Y MARRA PP (2005) The importance ofunderstanding migratory connectivity and sea-sonal interactions. Pp. 199–209 en: GREENBERG RY MARRA PP (eds) Birds of two worlds: the ecologyand evolution of migration. Johns Hopkins Univer-sity Press, Baltimore
WEBSTER MS, MARRA PP, HAIG SM, BENSCH S Y HOLMESRT (2001) Links between worlds: unraveling migra-tory connectivity. Trends in Ecology and Evolution17:76–83
WHITE JWC (1989) Stable hydrogen isotope ratiosin plants: a review of current theory and somepotential applications. Pp. 142–160 en: RUNDELPW, EHLERINGER JR Y NAGY KA (eds) Applicationsof stable isotopes in ecological research. Springer-Verlag, Nueva York
WUNDER MB, KESTER CL, KNOFF FL Y RYE RO (2005)A test of geographic assignment using isotopetracers in feathers of known origin. Oecologia144:607–617
ZIEGEL H (1989) Hydrogen isotopes fractionationin plant tissues. Pp. 105–123 en: RUNDEL PW,EHLERINGER JR Y NAGY KA (eds) Applications ofstable isotopes in ecological research. Springer-Verlag,Nueva York

How to cite

Julián Torres Dowdall, Adrian Farmer, Enrique H. Bucher (2006). Using stable isotopes to determine migratory connectivity in birds: extent and limitations. El Hornero, Vol. 21 No. 2 (2006), 73-84. https://doi.org/10.56178/eh.v21i2.789

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[1] ATKINSON PW, BAKER AJ, BEVAN RM, CLARK NA, COLEKB, GONZÁLEZ PM, NEWTON J, NILES LJ Y ROBINSONRA (2005)Unravelling the migration and moultstrategies of a long-distance migrant using stableisotopes: Red Knot Calidris canutus movements inthe Americas. Ibis 147:738–739

[2] BAIRLEIN F (2001) Results of bird ringing in the studyof migration routes. Ardea 89:7–19

[3] BEARHOP S, ADAMS CE, WALDORN S, FULLER RA YMACLEOD H (2004) Determining trophic nichewidth: a novel approach using stable isotope analy-sis. Journal of Animal Ecology 73:1007–1012

[4] BEARHOP S, WALDRON S, VOTIER SC Y FURNESS RW(2002) Factors that influence assimilation rates andfractionation of nitrogen and carbon isotopes inavian blood and feathers. Physiological and Biochemi-cal Zoology 75:451–458

[5] BOWEN GJ, WASSENAAR LI Y HOBSON KA (2005) Globalapplication of stable hydrogen and oxygen isotopesto wildlife forensics. Oecologia 143:337–348

[6] BOWEN GJ Y WILKINSON B (2002) Spatial distributionof δ18O in meteoric precipitation. Geology 30:315–318

[7] CARLETON SA Y MARTINEZDEL RIO C (2005) The effectof cold-induced increased metabolic rate on the rateof 13C and 15N incorporation in house sparrows(Passer domesticus). Oecologia 144:226–232

[8] CHAMBERLAIN CP, BLUM JD, HOLMES RT, XIAHONG F,SHERRY TW Y GRAVES GR (1997) The use of isotopetracers for identifying populations of migratorybirds. Oecologia 109:132–141

[9] DAANSGARD W (1964) Stable isotopes in precipitation.Tellus 16:436–468

[10] DENIRO MJ Y EPSTEIN S (1981) Influence of diet on thedistribution of nitrogen isotopes in animals.Geochimica et Cosmochimica Acta 45:341–351

[11] EHLERINGER JR Y RUNDEL PW (1989) Stable isotopes:history, units, and instrumentation. Pp. 1–17 en: RUN-DEL PW, EHLERINGER JR Y NAGY KA (eds) Stable isoto-pes in ecological research. Springer-Verlag, Nueva York

[12] ELSDON T Y GILLANDERS B (2003) Reconstructing mi-gratory patterns of fish based on environmentalinfluences on otolith chemistry. Reviews in FishBiology and Fisheries 13:219–235

[13] EVANS-OEGEN L, HOBSON KA Y LANK DB (2004) Bloodisotopic (δ13C and δ15N) turnover and diet-tissuefractionation factors in captive Dunlin: implicationsfor dietary analysis of wild birds. Auk 121:170–177

[14] FARMER A, ABRIL M, FERNÁNDEZ M, TORRES J, KESTER CY BERN C (2004) Using stable isotopes to associatemigratory shorebirds with their wintering locationsin Argentina. Ornitología Neotropical 15:377–384

[15] FARMER AH, RYE R, LANDIS G, BERN C, KESTER C YRIDLEY I (2003) Tracing the pathways of neotropicalmigratory shorebirds using stable isotopes: a pilotstudy. Isotopes in Environmental and Health Studies39:169–177

[16] GANNES LZ, O’BRIEN D Y MARTINEZDEL RIO C (1997)Stable isotopes in animal ecology: assumptions, ca-veats, and a call for more laboratory experiments.Ecology 78:1271–1276

[17] GAYE-SIESSEGGER J, FOCKEN U, ABEL H-J Y BECKER K(2003) Feeding level and diet quality influencetrophic shift of C and N isotopes in Nile Tilapia(Oreochromis nicoticus (L.)). Isotopes in Environmentaland Health Studies 39:125–134

[18] GUY R, FOGEL M Y BERRY J (1993) Photosynthetic frac-tionation of the stable isotopes of oxygen andcarbon. Plant Physiology 101:37–47

[19] HANDLY L, AUSTIN A, ROBINSON D, SCRIMGEOUR C,RAVEN J, HEATON T, SCHMIDT S Y STEWART G (1999)The 15N natural abundance (δ15N) of ecosystemsamples reflects measures of water availability.Austral Journal of Plant Physiology 26:185–199

[20] HEBERT CE Y WASSENAAR LI (2001) Stable nitrogen iso-topes in waterfowl feathers reflect agricultural landuse in western Canada. Environmental Science andTechnology 35:3482–3487

[21] HOBSON KA (1999) Tracing origins and migration ofwildlife using stable isotopes: a review. Oecologia120:314–326

[22] HOBSON KA (2002) Making migratory connectionswith stable isotopes. Pp. 379–391 en: BERTHOLD P YGWINNER P (eds) Avian migration. Springer-Verlag,Berlín

[23] HOBSON KA (2005a) Stable isotopes and the determi-nation of avian migratory connectivity and seasonalinteractions. Auk 122:1037–1048

[24] HOBSON KA (2005b) Flying fingerprints: making con-nections with stable isotopes and trace elements.Pp. 235–246 en: GREENBERG R Y MARRA PP (eds) Birdsof two worlds: the ecology and evolution of migration.Johns Hopkins University Press, Baltimore

[25] HOBSON KA, ALISAUSKAS RT Y CLARK RG (1993)Stable isotope nitrogen isotope enrichment inavian tissue due to fasting and nutritional stress:implications for isotopic analyses of diet. Condor101:799–805

[26] HOBSON KA, AUBRY Y Y WASSENAAR LI (2004a) Migra-tory connectivity in Bicknell’s Thrush: locatingmissing populations with hydrogen isotopes.Condor 106:905–909

[27] HOBSON KA Y BAIRLEIN F (2003) Isotopic discrimina-tion and turnover in captive Garden Warblers (Sylviaborin): implications for delineating dietary and mi-gratory associations in wild passerines. CanadianJournal of Zoology 81:1630–1635

[28] HOBSON KA, BOWEN GJ, WASSENAAR LI, FERRAND Y YLORMEE H (2004b) Using stable hydrogen and oxy-gen isotopes measurements to infer geographicalorigins of migrating European birds. Oecologia141:477–488

[29] HOBSON KA Y CLARK RG (1992) Assessing avian dietsusing stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197

[30] HOBSON KA Y WASSENAAR L (1997) Linking breedingand wintering grounds of neotropical migrant song-birds using stable hydrogen isotopic analysis offeathers. Oecologia 109:142–148

[31] IAEA (2001) Global Network of Isotopes in Precipitation(GNIP) and Isotope Hydrology Information System(ISOHIS).International Atomic Energy Agency,Viena (URL: http://isohis.iaea.org/)

[32] KELLY JF, ATUDOREI V, SHARP ZD Y FINCH DM (2002)Insights into Wilson’s Warbler migration from analysesof hydrogen stable-isotope ratios. Oecologia 130:216–221

[33] KELSALL JP (1970) Chemical elements in waterfowlflight feathers. Canadian Wildlife Service 19:1–11

[34] KELSALL JP Y BURTON R (1977) Identification of originsof lesser Snow Geese by X-ray spectrometry. Cana-dian Journal of Zoology 55:718–732

[35] KELSALL JP Y CALAPRIC JR (1972) Chemical content ofwaterfowl plumage as a potential diagnostic tool.Journal of Wildlife Management 36:1088–1097

[36] KENDALL C Y COPLEN TB (2001) Distribution of oxy-gen-18 and deuterium in river waters across theUnited States. Hydrological Processes 15:1363–1393

[37] LAJTHA K Y MARSHALL JD (1994) Sources of variationin the stable isotopic composition of plants. Pp. 1–21en: LAJTHA K Y MICHENER RH (eds) Stable isotopes inecology and environmental sciences. Blackwell Scien-tific Publications, Oxford

[38] LAJTHA K Y MICHENER RH (1994) Stable isotopes in ecol-ogy and environmental sciences. Blackwell ScientificPublications, Oxford

[39] LOTT CA, MEEHAN TD Y HEATH JA (2003) Estimatingthe latitudinal origins of migratory birds usinghydrogen and sulfur stable isotopes in feathers: in-fluence of marine prey base. Oecologia 134:505–510

[40] LOTT CA Y SMITH JP (2006) A GIS approach to esti-mating the origins of migratory raptors in NorthAmerica using hydrogen stable isotope ratios infeathers. Auk 123:822–835

[41] MARRA PP, HOBSON KA Y COLMES T (1998) Linkingwinter and summer events in a migrant passerinebird by using stable-carbon isotope. Science282:1884–1886

[42] MATTHEWS B Y MAZUMDER A (2004) A critical evalua-tion of intrapopulation variation of δ13C and isotopicevidence of individual specialization. Oecologia140:361–371

[43] MEEHAN TD, GIERMAKOWSKI JT Y CRYAN PM (2004) GIS-based model of stable hydrogen isotope ratios inNorth American growing-season precipitation foruse in animal movement studies. Isotopes in Envi-ronmental and Health Studies 40:291–300

[44] MURPHY ME (1996) Energetics and nutrition of molt.Pp. 158–198 en: CAREY C (ed) Avian energetics andnutritional ecology. Chapman & Hall, Nueva York

[45] MYERS JP, MORRISON RIG, ANTAS PZ, HARRINGTON BA,LOVEJOY TE, SALLABERRY M, SENNER SE Y TARAK A(1987) Conservation strategy for migratory species.American Scientist 75:18–26

[46] POAGE MA Y CHAMBERLAIN P (2001) Empirical relation-ships between elevation and the stable isotopecomposition of precipitation and surface waters:considerations for studies of paleoelevation change.American Journal of Science 301:1–15

[47] ROYLE JA Y RUBENSTEIN DR (2004) The role of speciesabundance in determining the breeding origins ofmigratory birds using stable isotopes. EcologicalApplications 14:1780–1788

[48] RUBENSTEIN DR, CHAMBERLAIN CP, HOLMES RT, AYRESMP, WALDBAUER JR, GRAVES GR Y TUROSS NC (2002)Linking breeding and wintering ranges of amigratory songbird using stable isotopes. Science295:1062–1065

[49] RUBENSTEIN DR Y HOBSON KA (2004) From birds tobutterflies: animal movements patterns and stableisotopes. Trends in Ecology and Evolution 19:256–263

[50] RUNDEL PW, EHLERINGER JR Y NAGY KA (1989) Applica-tions of stable isotopes in ecologicalresearch. Springer-Verlag, Nueva York

[51] SILLETT TS, HOLMES RT Y SHERRY TW (2000) Impactsof a global climate cycle on population dynamics ofa migratory songbird. Science 288:2040–2042

[52] STILL CJ, BERRY JA, COLLATZ GJ Y DEFRIES RS (2003)The global distribution of C3 and C4 vegetation:carbon cycle implications. Global BiogeochemicalCycles 17:1006–1029

[53] THORROLD S, LATKOCZY C, SWA RT P Y JONES C (2001)Natal homing in a marine fish metapopulation.Science 291:297–299

[54] TORRES DOWDALL J (2005) Uso de isótopos estables pararelacionar los hábitats estacionales de aves playerasneárticas. Tesis de Maestría, Universidad Nacionalde Córdoba, Córdoba

[55] WASSENAAR L Y HOBSON KA (2000) Stable-carbon andhydrogen isotopes ratios reveal breeding origins ofRed-winged Blackbirds. Ecological Applications10:911–916

[56] WASSENAAR LI Y HOBSON KA (2003) Comparativeequilibration and online technique for determina-tion of non-exchangeable hydrogen of keratins foruse in animal migration studies. Isotopes in Environ-mental and Health Studies 39:1–7

[57] WEBSTER MS Y MARRA PP (2005) The importance ofunderstanding migratory connectivity and sea-sonal interactions. Pp. 199–209 en: GREENBERG RY MARRA PP (eds) Birds of two worlds: the ecologyand evolution of migration. Johns Hopkins Univer-sity Press, Baltimore

[58] WEBSTER MS, MARRA PP, HAIG SM, BENSCH S Y HOLMESRT (2001) Links between worlds: unraveling migra-tory connectivity. Trends in Ecology and Evolution17:76–83

[59] WHITE JWC (1989) Stable hydrogen isotope ratiosin plants: a review of current theory and somepotential applications. Pp. 142–160 en: RUNDELPW, EHLERINGER JR Y NAGY KA (eds) Applicationsof stable isotopes in ecological research. Springer-Verlag, Nueva York

[60] WUNDER MB, KESTER CL, KNOFF FL Y RYE RO (2005)A test of geographic assignment using isotopetracers in feathers of known origin. Oecologia144:607–617

[61] ZIEGEL H (1989) Hydrogen isotopes fractionationin plant tissues. Pp. 105–123 en: RUNDEL PW,EHLERINGER JR Y NAGY KA (eds) Applications ofstable isotopes in ecological research. Springer-Verlag,Nueva York