Skip to content
BY-NC-ND 4.0 license Open Access Published by De Gruyter Open Access October 23, 2018

Wintering Areas, Migratory Connectivity and Habitat Fidelity of Three Declining Nearctic- Neotropical Migrant Swallows

  • Tara Leah Imlay EMAIL logo , Keith A. Hobson , Amélie Roberto-Charron and Marty L. Leonard
From the journal Animal Migration


Conservation efforts directed at population declines for migratory animals must consider threats occurring at different stages often separated by vast distances. Furthermore, connectivity between populations and fidelity of individuals to specific habitats during the annual cycle are also important considerations. Avian aerial insectivores are experiencing steep population declines in North America, and those declines may be driven, in part, by conditions on the wintering grounds. Here, using geolocators (2 species; 4 individuals) and stable isotope (δ2H, δ13C and δ15N) measurements of feathers (3 species; 841 individuals), we identified approximate winter areas, and assessed migratory connectivity and among-year winter habitat fidelity for three aerial insectivores (Bank Swallow Riparia riparia, Barn Swallow Hirundo rustica and Cliff Swallow Petrochelidon pyrrhonota) that breed in northeastern North America. All three species of swallows are declining in this region. Our results, largely from the stable isotope analysis, suggest that these species likely winter throughout the Cerrado, La Plata Basin, and the Pampas, in South America. These most likely areas were similar among years (2013-2016) for Bank and Cliff Swallows, but varied for Barn Swallows (2014-2016). We found weak migratory connectivity for all three species, and, with one exception, weak habitat fidelity among years for individuals. For individual Barn Swallows captured in two or more years, we found high repeatability in δ13C values, suggesting some fidelity to similar habitats among years. The most likely wintering areas for these species coincide with large areas of South America experiencing high rates of land-use change.


1] Egevang C., Stenhouse I.J., Phillips R.A., Petersen A., Fox J.W., Silk J.R.D., Tracking of Arctic Terns Sterna paradisaea reveals longest animal migration, Proc. Natl. Acad. Sci. 2010, 107, 2078-208110.1073/pnas.0909493107Search in Google Scholar

[2] Schofield G., Hobson V.J., Fossette S., Lilley M.K.S., Katselidis K.A., Hays G.C., Fidelity to foraging sites, consistency of migration routes and habitat modulation of home range by sea turtles, Divers. Distrib. 2010, 16, 840-85310.1111/j.1472-4642.2010.00694.xSearch in Google Scholar

[3] Cherry S.G., Derocher A.E., Lunn N.J., Habitat-mediated timing of migration in polar bears: an individual perspective, Ecol. Evol. 2016, 6, 5032-504210.1002/ece3.2233Search in Google Scholar

[4] Mellone U., Lopez-Lopez P., Liminana R., Piasevoli G., Urios V., The trans-equatorial loop migration system of Eleonora’s Falcon: differences in migration patterns between age classes, regions and seasons, J. Avian Biol. 2013, 44, 417-42610.1111/j.1600-048X.2013.00139.xSearch in Google Scholar

[5] Muller M.S., Massa B., Phillips R.A., Omo D., Individual consistency and sex differences in migration strategies of Scopoli’s Shearwaters Calonectris diomedea differences, Curr. Zool. 2014, 60, 631-64110.1093/czoolo/60.5.631Search in Google Scholar

[6] Bunnefeld N., Borger L., Van Moorter B., Rolandsen C.M., Dettki H., Solberg E.J., et al., A model-driven approach to quantify migration patterns: Individual, regional and yearly differences, J. Anim. Ecol. 2011, 80, 466-47610.1111/j.1365-2656.2010.01776.xSearch in Google Scholar

[7] Wilcove D.S., Wikelski M., Going, going, gone: Is animal migration disappearing?, PLoS Biol. 2008, 6, 1361-136410.1371/journal.pbio.0060188Search in Google Scholar

[8] Webster M.S., Marra P.P., The importance of understanding migratory connectivity and seasonal interactions, In: Greenberg, R., Marra, P.P. (Eds.), Birds of Two Worlds: The Ecology and Evolution of Migration, John Hopkins University Press, Baltimore, Maryland, USA, 2005, 199-209Search in Google Scholar

[9] Webster M.S., Marra P.P., Haig S.M., Bensch S., Holmes R.T., Links between worlds: unraveling migratory connectivity, Trends Ecol. Evol. 2002, 17, 76-8310.1016/S0169-5347(01)02380-1Search in Google Scholar

[10] Taylor C.M., Norris D.R., Population dynamics in migratory networks, Theor. Ecol. 2010, 3, 65-7310.1007/s12080-009-0054-4Search in Google Scholar

[11] Morales J.M., Moorcroft P.R., Matthiopoulos J., Frair J.L., Kie J.G., Powell R.A., et al., Building the bridge between animal movement and population dynamics, Philos. Trans. R. Soc. B Biol. Sci. 2010, 365, 2289-230110.1098/rstb.2010.0082Search in Google Scholar PubMed PubMed Central

[12] Matthiopoulos J., Harwood J., Thomas L., Metapopulation consequences of site fidelity for colonially breeding mammals and birds, J. Anim. Ecol. 2005, 74, 716-72710.1111/j.1365-2656.2005.00970.xSearch in Google Scholar

[13] Rubenstein D.R., Chamberlain C.P., Holmes R.T., Ayres M.P., Waldbauer J.R., Graves G.R., et al., Linking breeding and wintering ranges of a migratory songbird using stable isotopes, Science (80-. ). 2002, 295, 1062-106610.1126/science.1067124Search in Google Scholar PubMed

[14] van Wijk R.E., Bauer S., Schaub M., Repeatability of individual migration routes, wintering sites and timing in a long-distance migrant bird, Ecol. Evol. 2016, 6, 8679-868510.1002/ece3.2578Search in Google Scholar PubMed PubMed Central

[15] Stutchbury B.J.M., Tarof S.A., Done T., Gow E., Kramer P.M., Tautin J., et al., Tracking long-distance songbird migration by using geolocators, Science (80-. ). 2009, 323, 896-89610.1126/science.1166664Search in Google Scholar PubMed

[16] Szep T., Liechti F., Nagy K., Nagy Z., Hahn S., Discovering the migration and non-breeding areas of Sand Martins and House Martins breeding in the Pannonian basin (central-eastern Europe), J. Avian Biol. 2017, 48, 114-12210.1111/jav.01339Search in Google Scholar

[17] English P.A., Mills A.M., Cadman M.D., Heagy A.E., Rand G.J., Green D.J., et al., Tracking the migration of a nocturnal aerial insectivore in the Americas, BMC Zool. 2017, 2, 510.1186/s40850-017-0014-1Search in Google Scholar

[18] Hallworth M.T., Scott Sillett T., Van Wilgenburg S.L., Hobson K.A., Marra P.P., Migratory connectivity of a neotropical migratory songbird revealed by archival light-level geolocators, Ecol. Appl. 2015, 25, 336-34710.1890/14-0195.1Search in Google Scholar PubMed

[19] Fraser K.C., Shave A., Savage A., Ritchie A., Bell K., Siegrist J., et al., Determining fine-scale migratory connectivity and habitat selection for a migratory songbird by using new GPS technology, J. Avian Biol. 2017, 48, 339-34510.1111/jav.01091Search in Google Scholar

[20] Cooper N.W., Hallworth M.T., Marra P.P., Light-level geolocation reveals wintering distribution, migration routes, and primary stopover locations of an endangered long-distance migratory songbird, J. Avian Biol. 2017, 48, 209-21910.1111/jav.01096Search in Google Scholar

[21] Finch T., Saunders P., Aviles J.M., Bermejo A., Catry I., de la Puente J., et al., A pan-European, multipopulation assessment of migratory connectivity in a near-threatened migrant bird, Divers. Distrib. 2015, 21, 1051-106210.1111/ddi.12345Search in Google Scholar

[22] Renfrew R.B., Kim D., Perlut N., Smith J., Fox J., Marra P.P., Phenological matching across hemispheres in a long-distance migratory bird, Divers. Distrib. 2013, 19, 1-1210.1111/ddi.12080Search in Google Scholar

[23] Costantini D., Moller A.P., A meta-analysis of the effects of geolocator application on birds, Curr. Zool. 2013, 59, 697-70610.1093/czoolo/59.6.697Search in Google Scholar

[24] Gomez J., Michelson C.I., Bradley D.W., Norris D.R., Berzins L.L., Dawson R.D., et al., Effects of geolocators on reproductive performance and annual return rates of a migratory songbird, J. Ornithol. 2014, 155, 1-810.1007/s10336-013-0984-xSearch in Google Scholar

[25] Scandolara C., Rubolini D., Ambrosini R., Caprioli M., Hahn S., Liechti F., et al., Impact of miniaturized geolocators on Barn Swallow Hirundo rustica fitness traits, J. Avian Biol. 2014, 45, 1-710.1111/jav.00412Search in Google Scholar

[26] Morganti M., Rubolini D., Akesson S., Bermejo A., de la Puente J., Lardelli R., et al., Effect of light-level geolocators on apparent survival of two highly aerial swift species, J. Avian Biol. 2018, 49, 1-1010.1111/jav.01521Search in Google Scholar

[27] Hobson K.A., Stable-carbon and nitrogen isotope ratios of songbird feathers grown in two terrestrial biomes: implications for evaluating trophic relationships and breeding origins, Condor 1999, 799-80510.2307/1370067Search in Google Scholar

[28] Inger R., Bearhop S., Applications of stable isotope analyses to avian ecology, Ibis (Lond. 1859). 2008, 150, 447-46110.1111/j.1474-919X.2008.00839.xSearch in Google Scholar

[29] Rubenstein D.R., Hobson K.A., From birds to butterflies: animal movement patterns and stable isotopes, Trends Ecol. Evol. 2004, 19, 256-6310.1016/j.tree.2004.03.017Search in Google Scholar PubMed

[30] Bowen G.J., Wassenaar L.I., Hobson K.A., Global application of stable hydrogen and oxygen isotopes to wildlife forensics, Oecologia 2005, 143, 337-34810.1007/s00442-004-1813-ySearch in Google Scholar PubMed

[31] Powell R.L., Yoo E.-H., Still C.J., Vegetation and soil carbon-13 isoscapes for South America: integrating remote sensing and ecosystem isotope measurements, Ecosphere 2012, 3, 10910.1890/ES12-00162.1Search in Google Scholar

[32] Hobson K.A., Clark R.G., Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation, Condor 1992, 94, 189-19710.2307/1368808Search in Google Scholar

[33] Hobson K.A., Van Wilgenburg S.L., Wassenaar L.I., Larson K., Linking hydrogen (δ2H) isotopes in feathers and precipitation: Sources of variance and consequences for assignment to isoscapes, PLoS One 2012, 7, e3513710.1371/journal.pone.0035137Search in Google Scholar PubMed PubMed Central

[34] Hache S., Hobson K.A., Villard M.-A., Bayne E.M., Assigning birds to geographic origin using feather hydrogen isotope ratios (δ2H): importance of year, age, and habitat, Can. J. Zool. 2012, 90, 722-72810.1139/z2012-039Search in Google Scholar

[35] Hobson K.A., Van Wilgenburg S.L., Faaborg J., Toms J.D., Rengifo C., Sosa A.L., et al., Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity, J. F. Ornithol. 2014, 85, 237-25710.1111/jofo.12065Search in Google Scholar

[36] Garcia-Perez B., Hobson K.A., A multi-isotope (δ2H, δ13C, δ5N) approach to establishing migratory connectivity of Barn Swallow (Hirundo rustica), Ecosphere 2014, 5, 1-1210.1890/ES13-00116.1Search in Google Scholar

[37] Hjernquist M.B., Veen T., Font L., Klaassen M., High individual repeatability and population differentiation in stable isotope ratios in winter-grown Collared Flycatcher Ficedula albicollis feathers, J. Avian Biol. 2009, 40, 102-10710.1111/j.1600-048X.2009.04412.xSearch in Google Scholar

[38] Yohannes E., Bensch S., Lee R., Philopatry of winter moult area in migratory Great Reed Warblers Acrocephalus arundinaceus demonstrated by stable isotope profiles, J. Ornithol. 2008, 149, 261-26510.1007/s10336-007-0271-9Search in Google Scholar

[39] Goodenough A.E., Coker D.G., Wood M.J., Rogers S.L., Overwintering habitat links to summer reproductive success: intercontinental carry-over effects in a declining migratory bird revealed using stable isotope analysis, Bird Study 2017, 64, 433-44410.1080/00063657.2017.1408566Search in Google Scholar

[40] Hobson K.A., Isotopic ornithology: A perspective, J. Ornithol. 2011, 152, S49-S6610.1007/s10336-011-0653-xSearch in Google Scholar

[41] Michel N.L., Smith A.C., Clark R.G., Morrissey C.A., Hobson K.A., Differences in spatial synchrony and interspecific concordance inform guild-level population trends for aerial insectivorous birds, Ecography (Cop.). 2016, 39, 774-78610.1111/ecog.01798Search in Google Scholar

[42] Nebel S., Mills A., McCracken J.D., Taylor P.D., Declines of aerial insectivores in North America follow a geographic gradient, Avian Conserv. Ecol. 2010, 5, 110.5751/ACE-00391-050201Search in Google Scholar

[43] Shutler D., Hussell D.J.T., Norris D.R., Winkler D.W., Robertson R.J., Bonier F., et al., Spatiotemporal patterns in nest box occupancy by Tree Swallows across North America, Avian Conserv. Ecol. 2012, 7, 310.5751/ACE-00517-070103Search in Google Scholar

[44] Smith A.C., Hudson M.-A.R., Downes C.M., Francis C.M., Change points in the population trends of aerial-insectivorous birds in North America: synchronized in time across species and regions, PLoS One 2015, 10, e013076810.1371/journal.pone.0130768Search in Google Scholar PubMed PubMed Central

[45] Imlay T.L., Mills Flemming J., Saldanha S., Wheelwright N.T., Leonard M.L., Breeding phenology and performance for four swallows over 57 years: relationships with temperature and precipitation, Ecosphere 2018, 9, e0216610.1002/ecs2.2166Search in Google Scholar

[46] Sauer J.R., Niven D.K., Hines J.E., Ziolkowski, D. J. J., The North American Breeding Bird Survey, Results and Analysis 1966 -2015. Version 2.07.2017, 2017Search in Google Scholar

[47] Garrison B.A., Bank Swallow (Riparia riparia), version 2.0, The Birds of North America (P. G. Rodewald, Ed.), Ithaca Cornell Lab Ornithol. 199910.2173/tbna.414.pSearch in Google Scholar

[48] Brown C.R., Bomberger Brown M., Barn Swallow (Hirundo rustica), version 2.0, The Birds of North America (P. G. Rodewald, Ed.), Ithaca Cornell Lab Ornithol. 199910.2173/tbna.452.pSearch in Google Scholar

[49] Brown C.R., Bomberger Brown M., Pyle P., Patten M.A., Cliff Swallow (Petrochelidon pyrrhonata), version 3.0, The Birds of North America (P. G. Rodewald, Ed.), Ithaca Cornell Lab Ornithol. 201710.2173/bna.cliswa.03Search in Google Scholar

[50] Imlay T.L., Mann H.A.R., Leonard M.L., No effect of insect abundance on nestling survival and mass in Barn, Cliff and Tree swallows, Avian Conserv. Ecol. 2017, 12, 1910.5751/ACE-01092-120219Search in Google Scholar

[51] Rappole J.H., Tipton A.R., New harness design for attachment of radio transmitters to small passerines, J. F. Ornithol. 1991, 62, 335-337Search in Google Scholar

[52] Pyle P., Identification guide to North American birds. Part I. Columbidae to Ploceidae, State Creek Press, Bolinas, California, USA, 1997Search in Google Scholar

[53] Imlay T., Steenweg R., Garcia-Perez B., Hobson K., Rohwer S., Temporal and spatial patterns of flight and body feather molt for Bank, Barn and Cliff Swallows, J. F. Ornithol. 2017, 88, 405-41510.1111/jofo.12235Search in Google Scholar

[54] Wotherspoon S., Sumner M.D., Lisovski S., TwGeos: Basic data processing for light-level geolocation archival tags. Version 0.0-1, 2016Search in Google Scholar

[55] Sumner M.D., Wotherspoon M.A., Hindell S.J., Bayesian estimation of animal movement from archival and satellite tags, PLoS One 2009, 4, 1055-105910.1371/journal.pone.0007324Search in Google Scholar PubMed PubMed Central

[56] Lisovski S., Hahn S., GeoLight - processing and analysing light-based geolocator data in R, Methods Ecol. Evol. 2012, 3, 1055-105910.1111/j.2041-210X.2012.00248.xSearch in Google Scholar

[57] Wassenaar L.I., Hobson K.A., Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for animal migration studies, Isotopes Environ. Health Stud. 2003, 39, 211-21710.1080/1025601031000096781Search in Google Scholar PubMed

[58] eBird, eBird: An online database of bird distribution and abundance [web application], EBird, Ithaca, NY 2012Search in Google Scholar

[59] Ridgely R.S., Allnutt T.F., Brooks T., McNicol D.K., Mehlman D.W., Young B.E., et al., Digital distribution maps of the birds of the western hemisphere, version 1.0, NatureServe, Arlington, Virginia, USA 2003Search in Google Scholar

[60] Hobson K.A., Kardynal K.J., An isotope (δ34S) filter and geolocator results constrain a dual feather isoscape (δ2H, δ13C) to identify the wintering grounds of North American Barn Swallows, Auk 2016, 133, 86-9810.1642/AUK-15-149.1Search in Google Scholar

[61] Van Wilgenburg S.L., Hobson K.A., Combining stableisotope (δD) and band recovery data to improve probabilistic assignment of migratory birds to origin, Ecol. Appl. 2011, 21, 1340-135110.1890/09-2047.1Search in Google Scholar PubMed

[62] Ambrosini R., Moller A.P., Saino N., A quantitative measure of migratory connectivity, J. Theor. Biol. 2009, 257, 203-21110.1016/j.jtbi.2008.11.019Search in Google Scholar PubMed

[63] Finch T., Butler S.J., Franco A.M.A., Cresswell W., Low migratory connectivity is common in long-distance migrant birds, J. Anim. Ecol. 2017, 86, 662-67310.1111/1365-2656.12635Search in Google Scholar PubMed

[64] R Core Team, R: A Language and Environment for Statistical Computing, 2017Search in Google Scholar

[65] Bates D., Maechler M., Bolker B., Walker S., Fitting linear mixed-effects models using lme4, J. Stat. Softw. 2015, 67, 1-4810.18637/jss.v067.i01Search in Google Scholar

[66] Hobson K.A., Kardynal K.J., Wilgenburg S.L. Van, Albrecht G., Salvadori A., Cadman M.D., et al., A continent-wide migratory divide in North American breeding Barn Swallows (Hirundo rustica), PLoS One 2015, 10, e012934010.1371/journal.pone.0129340Search in Google Scholar PubMed PubMed Central

[67] Baker A.J., Gonzalez P.M., Piersma T., Niles L.J., de Lima Serrano do Nascimento I., Atkinson P.W., et al., Rapid population decline in Red Knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay, Proc. R. Soc. B Biol. Sci. 2004, 271, 875-88210.1098/rspb.2003.2663Search in Google Scholar PubMed PubMed Central

[68] Woodworth B.K., Francis C.M., Taylor P.D., Inland flights of young Red-eyed Vireos Vireo olivaceus in relation to survival and habitat in a coastal stopover landscape, J. Avian Biol. 2014, 45, 387-39510.1111/jav.00276Search in Google Scholar

[69] Newton I., Weather-related mass-mortality in migrants, Ibis (Lond. 1859). 2007, 149, 453-46710.1111/j.1474-919X.2007.00704.xSearch in Google Scholar

[70] Wellicome T.I., Fisher R.J., Poulin R.G., Todd L.D., Bayne E.M., Flockhart D.T.T., et al., Apparent survival of adult Burrowing Owls that breed in Canada is influenced by weather during migration and on their wintering grounds, Condor 2014, 116, 446-45810.1650/CONDOR-13-161.1Search in Google Scholar

[71] Lambin E.F., Geist H.J., Lepers E., Dynamics of land-use and land-cover change in tropical regions, Annu. Rev. Environ. Resour. 2003, 28, 205-24110.1146/ in Google Scholar

[72] Hansen M.C., Stehman S. V., Potapov P. V., Quantification of global gross forest cover loss, Proc. Natl. Acad. Sci. 2010, 107, 8650-865510.1073/pnas.0912668107Search in Google Scholar PubMed PubMed Central

[73] Davidson N.C., How much wetland has the world lost? Long-term and recent trends in global wetland area, Mar. Freshw. Res. 2014, 65, 934-94110.1071/MF14173Search in Google Scholar

[74] Lee S.-J., Berbery E.H., Land cover change effects on the climate of the La Plata Basin, J. Hydrometeorol. 2012, 13, 84-10210.1175/JHM-D-11-021.1Search in Google Scholar

[75] Sano E.E., Rosa R., Brito J.L.S., Ferreira L.G., Land cover mapping of the tropical savanna region in Brazil, Environ. Monit. Assess. 2010, 166, 113-12410.1007/s10661-009-0988-4Search in Google Scholar PubMed

[76] Viglizzo E.F., Frank F.C., Carreno L. V., Jobbagy E.G., Pereyra H., Clatt J., et al., Ecological and environmental footprint of 50 years of agricultural expansion in Argentina, Glob. Chang. Biol. 2011, 17, 959-97310.1111/j.1365-2486.2010.02293.xSearch in Google Scholar

[77] Loarie S.R., Lobell D.B., Asner G.P., Mu Q., Field C.B., Direct impacts on local climate of sugar-cane expansion in Brazil, Nat. Clim. Chang. 2011, 1, 105-10910.1038/nclimate1067Search in Google Scholar

[78] Luyssaert S., Jammet M., Stoy P.C., Estel S., Pongratz J., Ceschia E., et al., Land management and land-cover change have impacts of similar magnitude on surface temperature, Nat. Clim. Chang. 2014, 4, 389-39310.1038/nclimate2196Search in Google Scholar

[79] Kelly J.F., Atudorei V., Sharp Z.D., Finch D.M., Insights into Wilson’s Warbler migration from analyses of hydrogen stable-isotope ratios, Oecologia 2002, 130, 216-22110.1007/s004420100789Search in Google Scholar PubMed

[80] Hahn S., Amrhein V., Zehtindijev P., Liechti F., Strong migratory connectivity and seasonally shifting isotopic niches in geographically separated populations of a long-distance migrating songbird, Oecologia 2013, 173, 1217-122510.1007/s00442-013-2726-4Search in Google Scholar PubMed

[81] Moller A.P., Hobson K.A., Heterogeneity in stable isotope profiles predicts coexistence of populations of Barn Swallows Hirundo rustica differing in morphology and reproductive performance, Proc. R. Soc. B Biol. Sci. 2004, 271, 1355-136210.1098/rspb.2003.2565Search in Google Scholar PubMed PubMed Central

[82] Fraser K.C., Stutchbury B.J.M., Silverio C., Kramer P.M., Barrow J., Newstead D., et al., Continent-wide tracking to determine migratory connectivity and tropical habitat associations of a declining aerial insectivore, Proc. R. Soc. B Biol. Sci. 2012, 279, 4901-490610.1098/rspb.2012.2207Search in Google Scholar PubMed PubMed Central

[83] Trierweiler C., Klaassen R.H.G., Drent R.H., Exo K.-M., Komdeur J., Bairlein F., et al., Migratory connectivity and population- specific migration routes in a long-distance migratory bird, Proc. R. Soc. B Biol. Sci. 2014, 281, 2013289710.1098/rspb.2013.2897Search in Google Scholar PubMed PubMed Central

[84] Szep T., Hobson K.A., Vallner J., Piper S.E., Kovacs B., Szabo D.Z., et al., Comparison of trace element and stable isotope approaches to the study of migratory connectivity: an example using two hirundine species breeding in Europe and wintering in Africa, J. Ornithol. 2009, 150, 621-63610.1007/s10336-009-0382-6Search in Google Scholar

[85] Lopez-Calderon C., Hobson K.A., Marzal A., Balbontin J., Reviriego M., Magallanes S., et al., Wintering areas predict age-related breeding phenology in a migratory passerine bird, J. Avian Biol. 2017, 48, 631-63910.1111/jav.01070Search in Google Scholar

[86] Norris D.R., Marra P.P., Kyser T.K., Sherry T.W., Ratcliffe L.M., Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird, Proc. R. Soc. B Biol. Sci. 2004, 271, 59-6410.1098/rspb.2003.2569Search in Google Scholar PubMed PubMed Central

[87] Saino N., Ambrosini R., Caprioli M., Romano M., Rubolini D., Scandolara C., et al., Sex-dependent carry-over effects on timing of reproduction and fecundity of a migratory bird, J. Anim. Ecol. 2017, 86, 239-24910.1111/1365-2656.12625Search in Google Scholar PubMed

[88] Cowley E., Siriwardena G.M., Long-term variation in survival rates of Sand Martins Riparia riparia: dependence on breeding and wintering ground weather, age and sex, and their population consequences, Bird Study 2005, 52, 237-25110.1080/00063650509461397Search in Google Scholar

[89] Drake A., Rock C., Quinlan S.P., Green D.J., Carry-over effects of winter habitat vary with age and sex in Yellow Warblers Setophaga petechia, J. Avian Biol. 2013, 44, 321-33010.1111/j.1600-048X.2013.05828.xSearch in Google Scholar

[90] Lopez-Calderon C., Hobson K.A., Marzal A., Balbontin J., Reviriego M., Magallanes S., et al., Environmental conditions during winter predict age- and sex-specific differences in reproductive success of a trans-Saharan migratory bird, Sci. Rep. 2017, 7, 1808210.1038/s41598-017-18497-2Search in Google Scholar PubMed PubMed Central

[91] Tonra C.M., Both C., Marra P.P., Incorporating site and year-specific deuterium ratios (d2H) from precipitation into geographic assignments of a migratory bird, J. Avian Biol. 2015, 46, 266-27410.1111/jav.00553Search in Google Scholar

[92] Vander Zanden H.B., Wunder M.B., Hobson K.A., Van Wilgenburg S.L., Wassenaar L.I., Welker J.M., et al., Contrasting assignment of migratory organisms to geographic origins using long-term versus year-specific precipitation isotope maps, Methods Ecol. Evol. 2014, 5, 891-90010.1111/2041-210X.12229Search in Google Scholar

[93] van Dijk J.G.B., Meissner W., Klaassen M., Improving provenance studies in migratory birds when using feather hydrogen stable isotopes, J. Avian Biol. 2014, 45, 103-10810.1111/j.1600-048X.2013.00232.xSearch in Google Scholar

[94] Van Wilgenburg S.L., Hobson K.A., Brewster K.R., Welker J.M., Assessing dispersal in threatened migratory birds using stable hydrogen isotope (δD) analysis of feathers, Endanger. Species Res. 2012, 16, 17-2910.3354/esr00383Search in Google Scholar

[95] Gomez C., Bayly N.J., Norris D.R., Mackenzie S.A., Rosenberg K. V., Taylor P.D., et al., Fuel loads acquired at a stopover site influence the pace of intercontinental migration in a boreal songbird, Sci. Rep. 2017, 7, 1-1110.1038/s41598-017-03503-4Search in Google Scholar PubMed PubMed Central

[96] Langin K.M., Reudink M.W., Marra P.P., Norris D.R., Kyser T.K., Ratcliffe L.M., Hydrogen isotopic variation in migratory bird tissues of known origin: implications for geographic assignment, Oecologia 2007, 152, 449-45710.1007/s00442-007-0669-3Search in Google Scholar PubMed

[97] Nordell C.J., Hache S., Bayne E.M., Solymos P., Foster K.R., Godwin C.M., et al., Within-site variation in feather stable hydrogen isotope (δ2Hf) values of boreal songbirds: Implications for assignment to molt origin, PLoS One 2016, 11, 1-1510.1371/journal.pone.0163957Search in Google Scholar PubMed PubMed Central

[98] Hallworth M.T., Studds C.E., Sillett T.S., Marra P.P., Do archival light-level geolocators and stable hydrogen isotopes provide comparable estimates of breeding-ground origin?, Auk 2013, 130, 273-28210.1525/auk.2013.13037Search in Google Scholar

[99] Gaston K.J., Fuller R.A., Commonness, population depletion and conservation biology, Trends Ecol. Evol. 2008, 23, 14-1910.1016/j.tree.2007.11.001Search in Google Scholar PubMed

[100] Runge C.A., Martin T.G., Possingham H.P., Willis S.G., Fuller R.A., Conserving mobile species, Front. Ecol. Environ. 2014, 12, 395-40210.1890/130237Search in Google Scholar

[101] Sherry T.W., Johnson M.D., Strong A.M., Does winter food limit populations of migratory birds?, In: Greenberg, R., Marra, P.P. (Eds.), Birds of Two Worlds: The Ecology and Evolution of Migration, John Hopkins University Press, Baltimore, Maryland, USA, 2005, 414-425Search in Google Scholar

[102] Rioux Paquette S., Garant D., Pelletier F., Belisle M., Seasonal patterns in Tree Swallow prey (Diptera) abundance are affected by agricultural intensification, Ecol. Appl. 2013, 123, 122-13310.1890/12-0068.1Search in Google Scholar PubMed

[103] Benton T.G., Bryant D.M., Cole L., Crick H.Q.P., Linking agricultural practice to insect and bird populations: a historical study over three decades, J. Appl. Ecol. 2002, 39, 673-68710.1046/j.1365-2664.2002.00745.xSearch in Google Scholar

[104] Pisa L.W., Amaral-Rogers V., Belzunces L.P., Bonmatin J.M., Downs C.A., Goulson D., et al., Effects of neonicotinoids and fipronil on non-target invertebrates, Environ. Sci. Pollut. Res. 2015, 22, 68-10210.1007/s11356-014-3471-xSearch in Google Scholar PubMed PubMed Central

[105] Morrissey C.A., Mineau P., Devries J.H., Sanchez-Bayo F., Liess M., Cavallaro M.C., et al., Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review, Environ. Int. 2015, 74, 291-30310.1016/j.envint.2014.10.024Search in Google Scholar PubMed

Received: 2018-04-11
Accepted: 2018-08-22
Published Online: 2018-10-23
Published in Print: 2018-10-01

© by Tara Leah Imlay et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Downloaded on 24.2.2024 from
Scroll to top button