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Journal of Ornithology

, Volume 159, Issue 1, pp 191–203 | Cite as

Quantifying the non-breeding provenance of staging Ruffs, Philomachus pugnax, using stable isotope analysis of different tissues

  • Lucie E. Schmaltz
  • A. H. Jelle Loonstra
  • Eddy Wymenga
  • Keith A. Hobson
  • Theunis Piersma
Original Article

Abstract

International conservation efforts for migratory populations are most effectively based on quantification of the geographical linkages between wintering, staging, and breeding areas, patterns that may not remain constant in times of global change. We used stable isotope (δ 13C, δ 15N, and δ 2H) measurements of different tissues representing distinct periods of dietary integration to quantify the non-breeding provenance of a threatened staging population of Ruffs Philomachus pugnax. In 199 staging Ruffs captured in 2012 during northward migration in the Netherlands, we compared the multi-isotope patterns of feathers grown at wintering grounds, with the δ 13C and δ 15N profiles of blood cells and plasma representative of staging areas. Few birds had the 13C-depleted and 15N-enriched feathers suggestive of wintering quarters in European agricultural areas. Most Ruffs had higher feather δ 13C values, suggesting that they wintered in sub-Saharan Africa. Feather δ 2H values were not informative due to the overlap of values from European and African moulting sites. Blood cell δ 13C and δ 15N values indicated that sub-Saharan Ruffs fuelled on low trophic-level foods in habitats dominated by C3 terrestrial or freshwater aquatic primary production, e.g. the rice fields in Africa or the Mediterranean. Stable isotope ratios in plasma suggested that Ruffs made stopovers in southern European agricultural areas. Stable isotopes thus enabled assessments of wintering origin in large numbers of birds. We further propose that conservation measures to protect Ruffs must include the adequate management of sub-Saharan wetlands, based on a better understanding of the role of human-made rice fields for fuelling birds.

Keywords

Philomachus pugnax Wintering Spring migration Migratory connectivity Stable isotopes Shorebirds 

Zusammenfassung

Quantifizierung der Herkunft rastender Kampfläufer Philomachus pugnax mit Hilfe der stabilen Isotopen-Analyse von unterschiedlichen Gewebetypen

Internationale Schutzbemühungen für ziehende Populationen sind am effektivsten, wenn sie auf der Quantifizierung der geografischen Verbindungen zwischen Überwinterungs-, Rast- und Brutgebiet basieren, da in Zeiten des globalen Wandels deren Muster nicht konstant bleiben. Mit Hilfe stabiler Isotopen-Messungen (δ13C, δ15N und δ2H) aus verschiedenen Gewebetypen, die unterschiedliche Perioden der Nahrungsaufnahme repräsentieren, um die Herkunftsgebiete einer bedrohten Rastpopulation von Kampfläufern Philomachus pugnax zu quantifizieren. 2012 wurden dazu während des Heimzuges 199 rastende Kampfläufer in den Niederlanden gefangen. Wir verglichen die Multi-Isotopen-Muster der Federn, die in den Überwinterungsgebieten gewachsen waren, mit den δ13C und δ15N Profilen der Blutzellen und Plasma, die typisch sind für die Rastgebiete. Einige Vögel hatten 13C-verminderte und 15N-angereicherte Federn, was auf Überwinterungsgebiete in europäischen Agrargebieten hinweist. Die meisten Kampfläufer hatten höhere δ13C Werte in den Federn, was auf eine Überwinterung in Afrika südlich der Sahara hindeutet. Federn mit δ2H Werten lieferten keine Informationen aufgrund der Überlappung der Werte aus Europa und afrikanischen Mausergebieten. δ13C und δ15N Werte der Blutzellen deuten darauf hin, dass sich südlich der Sahara überwinternde Kampfläufer mit Nahrung niedriger Trophiestufen „auftanken“in Habitaten, dominiert von C3 aus terrestrischer oder Süßwasser-Primärproduktion, z. B. Reisfelder in Afrika oder im mediterranen Raum. Die Verhältnisse stabiler Isotope im Plasma legen nahe, dass Kampfläufer in Agrargebieten Südeuropas rasten. Stabile Isotope erlauben daher einen Rückschluss auf die winterlichen Herkunftsgebiete bei einer großen Anzahl von Vögeln. Darüber hinaus sollten Maßnahmen zum Schutz von Kampfläufern ein adäquates Feuchtgebietsmanagement in der Subsahara beinhalten, basierend auf einem besseren Verständnis der Rolle von Reisfeldern für die Fettdeposition für den Zug.

Notes

Acknowledgements

We thank the Frisian “wilsternetters” Albert Anne Mulder, Doede Anne Mulder, Eeltje Anne Mulder, Fons Baarsma, Jappie Boersma, Cees Dekker, Piet Feenstra, Albert Hendrik Mulder, Doede Hendrik Mulder, Douwe de Jager, Bauke de Jong, Joop Jukema, Bauke Kuipers, Willem Louwsma, Catharinus Monkel, Rein Mulder, Jaap Strikwerda, Fokke Tuinstra, Bram van der Veen, F. van der Veen, Arend Veenstra, Sierd Visser, Willem Visser, Piet Vlas, Douwe van der Zee, and Rinkje van der Zee for their dedication to catch Ruffs since 2004. We thank Marta Lomas Vega and Helena Bathala for their help in the field and Idrissa Ndiaye for his precious insights from the field in Senegal. This study was carried out under license of Animal Experimentation Committee (DEC) of the University of Groningen in accordance to the Dutch laws [reference number 6351B]. This work was financially supported by an Ubbo Emmius PhD grant from the University of Groningen, supplemented by the Province of Friesland and a start-up grant of the University of Groningen to TP. Stable isotope analyses were financed by an operating grant to KAH from Environment and Climate Change Canada.

References

  1. Alerstam T (1990) Bird migration. Cambridge University Press, CambridgeGoogle Scholar
  2. Bacetti N, Chelazzi L, Colombini I, Serra L (1998) Preliminary data on the diet of migrating ruffs Philomachus pugnax in northern Italy. Int Wader Stud 10:361–364Google Scholar
  3. Baker AJ, Gonzalez PM, Piersma T, Niles LJ, de Lima S, do Nascimento I, Atkinson PW, Collins P, Clark NA, Minton CDT, Peck MK, Aarts G (2004) Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proc R Soc B 271:875–882. doi: 10.1098/rspb.2003.2663 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458. doi: 10.1086/342800 CrossRefPubMedGoogle Scholar
  5. Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348. doi: 10.1007/s00442-004-1813-y CrossRefPubMedGoogle Scholar
  6. Castelijns H (1994) Black-tailed godwit Limosa limosa islandica and ruff Philomachus pugnax winter in increasing numbers in Zeeuws-Vlaanderen (SW-Netherlands). Limosa 67:113-11Google Scholar
  7. Catry T, Lourenço PM, Lopes RJ, Bocher P, Carneiro C, Alves JP, Delaporte P, Bearhop S, Piersma T, Granadeiro JP (2016) Use of stable isotope fingerprints to assign wintering origin and trace shorebird movements along the East-Atlantic flyway. Basic Appl Ecol 17:177–187. doi: 10.1016/j.baae.2015.10.005 CrossRefGoogle Scholar
  8. Caut S, Angula E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and application for diet reconstruction. J Appl Ecol 46:443–453. doi: 10.1111/j.1365-2664.2009.01620.x CrossRefGoogle Scholar
  9. Christianen MJA, Middelburg JJ, Holthuisjen SJ, Jouta J, Compton TJ, van der Heide T, Piersma T, Sinninghe Damsté JS, van der Veer HW, Schouten S, Olff H (2017) Benthis primary producers are key to sustain the Wadden Sea food web: a stable carbon isotope analysis at lanscape scale. Ecology 98:1498–1512CrossRefPubMedGoogle Scholar
  10. Coulton DW, Clark RG, Hebert CE (2010) Determining natal origins of birds using stable isotopes (δ 34S, δ 15N and δ 13C): model validation and spatial resolution for mid-continent Mallars. Waterbirds 33:10–21CrossRefGoogle Scholar
  11. Cramp S, Simmons KEL (1983) The birds of the Western Palearctic, vol III. Oxford University Press, OxfordGoogle Scholar
  12. Devos K, T’Jollyn F, Brosens D, Desmet P (2012) Watervogels—Wintering waterbirds in Flanders, Belgium. v3.3. Research Institute for Nature and Forest (INBO). Dataset/Occurrence. doi:10.15468/lj0udqGoogle Scholar
  13. Dietz MW, Spaans B, Dekinga A, Klaassen M, Korthals H, van Leeuwen C, Piersma T (2010) Do red knots (Calidris canutus islandica) routinely skip Iceland during southward migration? Condor 112:48–55. doi: 10.1525/cond.2010.090139 CrossRefGoogle Scholar
  14. Dietz MW, Piersma T, Dekinga A, Korthals H, Klaassen M (2013) Unusual patterns in 15N blood values after a diet switch in red knot shorebirds. Isotopes Environ Health Stud 49:283–292. doi: 10.1080/10256016.2013.776045 CrossRefPubMedGoogle Scholar
  15. Evans Ogden JL, Hobson KA, Lank DB (2004) Blood isotopic (δ 13C and δ 15N) turnover and diet-tissue fractionation factors in captive dunlin (Calidris alpina pacifica). Auk 121:170–177. doi: 10.1642/0004-8038(2004)121 CrossRefGoogle Scholar
  16. Gill JA, Clark J, Clark N, Sutherland WJ (1995) Sex-differences in the migration, moult and wintering areas of British ringed ruff. Ring Migr 16:159–167. doi: 10.1080/03078698.1995.9674107 CrossRefGoogle Scholar
  17. Gill REJR, Tibbitts TL, Douglas DC, Handel CM, Mulcahy DM, Gottschalck JC, Warnock N, McCaffery BJ, Battley PF, Piersma T (2009) Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc R Soc Lond B 276:447–457. doi: 10.1098/rspb.2008.1142 CrossRefGoogle Scholar
  18. Gilroy JJ, Gill JA, Buchart SHM, Jones VR, Franco AMA (2016) Migratory diversity predicts population declines in birds. Ecol Lett 19:301–317. doi: 10.1111/ele.12569 CrossRefGoogle Scholar
  19. Gutiérrez-Esposito C, Ramírez F, Afán I, Forero MG, Hobson KA (2015) Toward a deuterium feather isoscape for sub-Saharan Africa: progress, challenges and the path ahead. PLoS ONE 10:e0135938. doi: 10.1371/journal.pone.0135938 CrossRefGoogle Scholar
  20. Hebert CE, Wassenaar LI (2001) Stable nitrogen isotopes in waterfowl reflect agricultural land use in western Canada. Envir Sci Technol 35:3482–3487CrossRefGoogle Scholar
  21. Hebert CE, Wassenaar LI (2005) Feather stable isotopes in western north American waterfowl: spatial patterns, underlying factors, and management applications. Wildl Soc Bull 33:92–102CrossRefGoogle Scholar
  22. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326. doi: 10.1007/s004420050865 CrossRefPubMedGoogle Scholar
  23. Hobson KA (2005) Stable isotopes and the determination of avian migratory connectivity and seasonal interactions. Auk 122:1037–1048. doi: 10.1642/0004-8038(2005)122 CrossRefGoogle Scholar
  24. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188. doi: 10.2307/1368807 CrossRefGoogle Scholar
  25. Hobson KA, Wassenaar LI (2008) Tracking animal migration with stable isotopes. Academic Press, LondonGoogle Scholar
  26. Hobson KA, van Wilgenburg SL, Wassenaar LI, Larson K (2012) Linking hydrogen (δ 2H) isotopes in feather and precipitation: source of variance and consequences for assignment to isoscapes. PLoS ONE 7:e35137. doi: 10.1371/journal.pone.0035137 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hornman M, Hustings F, Koffijberg K, Klaassen O, Kleefstra R, van Winden E, Sovon Ganzen en Zwanenwerkgroep, Soldaat L (2013) Rapport Sovon-Watervogels in Nederland 2011/2012. Sovon Vogelonderzoek Nederland, NijmegenGoogle Scholar
  28. Hortas F, Masero J (2012) Combatiente. In: Atlas de las aves en invernio en España 2007–2010. del Moral JC, Molina B, Ana Bermejo A, Palomino D (eds) Ministerio de Agricultura, Alimentacion y Medio Ambiente-SEO/BirdLife, Madrid, pp 254–255Google Scholar
  29. IAEA/WMO (2001) Global network of isotopes in precipitation: the GNIP database. http://www.iaea.org/water
  30. Iwamura T, Possingham HP, Chadès I, Minton C, Murray NJ, Rogers DI, Treml EA, Fuller RA (2013) Migratory connectivity magnifies the consequences of habitat loss from sea-level rise for shorebird populations. Proc R Soc B 280:20130325. doi: 10.1098/rspb.2013.0325 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Iwamura T, Fuller RA, Possingham HP (2014) Optimal management of a multispecies shorebird flyway under sea-level rise. Conserv Biol 28:1710–1720. doi: 10.1111/cobi.12319 CrossRefPubMedGoogle Scholar
  32. Jukema J, Piersma T (2006) Permanent female mimics in a lekking shorebird. Biol Lett 2:161–164. doi: 10.1098/rsbl.2005.0416ER CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jukema J, Wymenga E, Piersma T (2001) Stopping over in SW Friesland: fattening and moulting in ruffs Philomachus pugnax during northward migration in the Netherlands. Limosa 74:17–26Google Scholar
  34. Karasov WH, Martinez del Rio C (2007) Physiological ecology: How animals process energy, nutrients and toxins. Princeton University Press, PrincetonGoogle Scholar
  35. Karlionova N, Meissner W, Pinchuk P (2008) Differential development of breeding plumage in adult and second-year male ruffs Philomachus pugnax. Ardea 96:39–45. doi: 10.5253/078.096.0105 CrossRefGoogle Scholar
  36. Kendall C (1998) Tracing nitrogen sources and cycling catchment. In: Kendall C, McDonnell JJ (eds) Isotope tracers in catchment hydrology. Elsevier, New York, pp 519–576CrossRefGoogle Scholar
  37. Klaassen M, Piersma T, Korthals H, Dekinga A, Dietz M (2010) Single-point isotope measurements in blood cells and plasma to estimate the time since diet switches. Funct Ecol 24:796–804. doi: 10.1111/j.1365-2435.2010.01689.x CrossRefGoogle Scholar
  38. Koopman K (1986) Primary moult and weight changes of ruffs in the Netherlands in relation to migration. Ardea 74:69–77Google Scholar
  39. López-Calderón C, Hobson KA, Marzal A, Balbontín J, Reviriego M, Magallanes S, García-Longoria L, de Lope F, Møller AP (2017) Wintering areas predict age-related breeding phenology in a migratory passerine bird. J Avian Biol 48:631–639CrossRefGoogle Scholar
  40. Márquez-Ferrando R, Figuerola J, Hooimeijer JCEW, Piersma T (2014) Recently created man-made habitats in Doñana provide alternative wintering space for the threatened continental European black-tailed godwit population. Biol Cons 171:127–135. doi: 10.1016/j.biocon.2014.01.022 CrossRefGoogle Scholar
  41. Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by stable-carbon isotope. Science 282:1884–1886. doi: 10.1126/science.282.5395.1884 CrossRefPubMedGoogle Scholar
  42. Meissner W, Scebba S (2005) Intermediate stages of age characters create dilemmas in ageing female ruffs Philomachus pugnax in spring. Wader Study Group Bull 106:30–33Google Scholar
  43. Melter J, Sauvage A (1997) Measurements and moult of ruffs Philomachus pugnax wintering in West Africa. Malimbus 19:12–18Google Scholar
  44. Münster OAG (1998) Mass of ruffs Philomachus pugnax wintering in West Africa. Int Wader Stud 10:435–440Google Scholar
  45. Newton I (2008) The migration ecology of birds. Academic Press, AmsterdamGoogle Scholar
  46. Onrust J, Loonstra AHJ, Schmaltz LE, Verkuil YI, Hooijmeijer JCEW, Piersma T (2017) Detection of earthworm prey by ruffs Philomachus pugnax. Ibis, in press. doi: 10.1111/ibi.12467 Google Scholar
  47. Oppel S, Pain DJ, Lindsell JA, Lachmann L, Diop I, Tegetmeyer C, Donald PF, Anderson G, Bowden GR, Tanneberger F, Flade M (2011) High variation reduces the value of feather stable isotope ratios in identifying new wintering areas for aquatic warblers Acrocephalus paludicola in West Africa. J Avian Biol 42:342–354. doi: 10.1111/j.1600-048X.2011.05252.x CrossRefGoogle Scholar
  48. Ouwehand J, Ahola MP, Ausems ANMA, Bridge ES, Burgess M, Hahn S, Hewson CM, Klaassen RHG, Laaksonen T, Lampe HM, Velmala W, Both C (2015) Light-level geolocators reveal migratory connectivity in European populations of pied flyctachers Ficedula hypoleuca. J Avian Biol 47:69–83. doi: 10.1111/jav.00721 CrossRefGoogle Scholar
  49. Pearson DJ (1981) The wintering and moult of ruffs Philomachus pugnax in the Kenyan Rift valley. Ibis 123:158–182. doi: 10.1111/j.1474-919X.1981.tb00922.x CrossRefGoogle Scholar
  50. Pernollet CA, Guelmami A, Green AJ, Curcó Masip A, Dies B, Bogliani G, Tesio F, Brogi A, Gauthier-Clerc M, Guillemain M (2015) A comparison of wintering duck numbers among European rice production areas with contrasting flooding regimes. Biol Cons 186:214–224. doi: 10.1016/j.biocon.2015.03.019 CrossRefGoogle Scholar
  51. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. doi: 10.1146/annurev.es.18.110187.001453 CrossRefGoogle Scholar
  52. Piersma T (2007) Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J Ornithol 148:S45–S59. doi: 10.1007/s10336-007-0240-3 CrossRefGoogle Scholar
  53. Piersma T, Lok T, Chen Y, Hassell CJ, Yang HY, Boyle A, Slaymaker M, Chan YC, Melville DS, Zhang ZW, Ma Z (2016) Simultaneous declines in summer survival of three shorebird species signals a flyway at risk. J Appl Ecol 53:479–490. doi: 10.1111/1365-2664.12582 CrossRefGoogle Scholar
  54. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  55. Prater AJ (1973) The wintering population of ruffs in Britain and Ireland. Bird Study 20:245–250. doi: 10.1080/00063657309476388 CrossRefGoogle Scholar
  56. Prater AJ, Marchant JH, Vuorinen J (1977) Guide to the identification and ageing of Holarctic waders. British Trust for Ornithology, UKGoogle Scholar
  57. Qninba A, Dakki M, Benhoussa A, El-Agbani MA (2006) Rôle de la côte Atlantique marocaine dans l’hivernage des limicoles (Aves, Charadrii). Ostrich 78:489–493. doi: 10.2989/OSTRICH.2007.78.2.59.173 CrossRefGoogle Scholar
  58. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
  59. Rakhimberdiev E, Verkuil YI, Saveliev AA, Väisänen RA, Karagicheva J, Soloviev MY, Tomkovich PS, Piersma T (2010) A global population redistribution in a migrant shorebird detected with continent-wide qualitative breeding survey data. Divers Distrib 17:144–151. doi: 10.1111/j.1472-4642.2010.00715.x CrossRefGoogle Scholar
  60. Runge CA, Watson JEM, Butchart SHM, Hanson JO, Possingham HP, Fuller RA (2015) Protected areas and global conservation of migratory birds. Science 350:1255–1257. doi: 10.1126/science.aac9180 CrossRefPubMedGoogle Scholar
  61. Sánchez-Guzmán JM, Morán R, Masero JA, Corbacho C, Costillo E, Villegas A, Santiago-Quesada F (2007) Identifying new buffer areas for conserving waterbirds in the Mediterranean basin: the importance of the rice in Extremadura, Spain. Biodivers Conserv 16:3333–3344. doi: 10.1007/s10531-006-9018-9 CrossRefGoogle Scholar
  62. Schmaltz LE, Juillet C, Tinbergen JM, Verkuil YI, Hooijmeijer JCEW, Piersma T (2015) Apparent annual survival of staging ruffs during a period of population decline : insights from sex and site-use related differences. Popul Ecol 57:613–624. doi: 10.1007/s10144-015-0511-4 CrossRefGoogle Scholar
  63. Schmaltz LE, Vega ML, Verkuil YI, Hooimeijer JCEW, Piersma T (2016) Use of agricultural fields by ruffs in southwest Friesland in 2003–2013. Ardea 104:23–32. doi: 10.5253/arde.v104i1.a2 CrossRefGoogle Scholar
  64. Skagen SK, Bart J, Andres B, Brown S, Donaldson G, Harrington B, Johnston V, Jones SL, Morrison RIG (2003) Monitoring the shorebirds of North America: towards a unified approach. Wader Study Group Bull 100:102–104Google Scholar
  65. Taylor CM, Norris DR (2010) Population dynamics in migratory networks. Theor Ecol 3:65–73. doi: 10.1111/j.1600-048X.2012.05573.x CrossRefGoogle Scholar
  66. Thorup K, Korner-Nievergelt F, Cohen EB, Baillie SR (2014) Large-scale spatial analyis of ringing and re-encounter data to infer movement patterns: a review including methodological perspectives. Methods Ecol Evol 5:1137–1350. doi: 10.1111/2041-210X.12258 CrossRefGoogle Scholar
  67. Tøttrup AP, Klaassen RHG, Strandberg R, Thorup K, Kristensen MW, Jørgensen PS, Fox J, Afanasyev V, Rahbek C, Alerstam T (2012) The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration. Proc R Soc B 279:1008–1016. doi: 10.1098/rspb.2011.1323 CrossRefPubMedGoogle Scholar
  68. Tréca B (1990) Régimes et préférences alimentaires d’anatidés et de scolopacidés dans le delta du Senegal, études de leur capacités d’adaptation aux modifications du milieu. Exploitation des milieux cultivés. PhD ThesisGoogle Scholar
  69. Tréca B (1994) The diet of ruffs and Black-tailed Godwits in Senegal. Ostrich 65:256–263CrossRefGoogle Scholar
  70. Triplet P, Diop I, Sylla SI, Schricke V (2014) Les oiseaux d’eau dans le delta du fleuve Sénégal (rive gauche). Bilan de 25 années de dénombrements hivernaux (mi-janvier 1989–2014). OMPO, ONCFS, DPN, SMBS, p 125Google Scholar
  71. van der Kamp J, Diallo M, Fofana B (2002a) Dynamique des populations d’oiseaux d’eau. In: Wymenga E, Kone B, van der Kamp J, Zwarts L (eds) Delta Intérieur du Niger: ecologie et gestion durable des ressources naturelles. A&W/Wetlands International/Rijkswaterstaat, Veenwouden, pp 87–140Google Scholar
  72. van der Kamp J, Zwarts L, Diallo M (2002b) Niveaux de crue, oiseaux d’eau et ressources alimentaires disponibles. In: Wymenga E, Kone B, van der Kamp J, Zwarts L (eds) Delta Intérieur du Niger: Ecologie et gestion durable des ressources naturelles. A&W/Wetlands International/Rijkswaterstaat, Veenwouden, pp 141–161Google Scholar
  73. van Gils JA, Ahmedou Salem MV (2015) Validating the incorporation of 13C and 15N in a shorebird that consumes an isotopically distinct chemosynbiotic bivalve. PLoS ONE 10:e0140221. doi: 10.1371/journal.pone.0140221 CrossRefPubMedPubMedCentralGoogle Scholar
  74. van Rhijn JG (1991) The ruff: individuality in a gregarious wading bird. T. & A.D, Poyser, LondonGoogle Scholar
  75. Verkuil YI, de Goeij P (2003) Do reeves make different choices? Meadow selection by spring staging ruffs Philomachus pugnax in Southwest Friesland. Limosa 76:157–168Google Scholar
  76. Verkuil YI, Wijmenga JJ, Hooijmeijer JCEW, Piersma T (2010) Spring migration of ruffs Philomachus pugnax in Fryslân: estimates of staging duration using resighting data. Ardea 98:21–33. doi: 10.5253/078.098.0104 CrossRefGoogle Scholar
  77. Verkuil YI, Karlionova N, Rakhimberdiev E, Jukema J, Wijmenga JJ, Hooijmeijer JCEW, Pinchuk P, Wymenga E, Baker AJ, Piersma T (2012) Losing a staging area : eastward redistribution of Afro-Eurasian ruffs is associated with deteriorating fuelling conditions along the western flyway. Biol Conserv 149:51–59. doi: 10.1016/j.biocon.2012.01.059 CrossRefGoogle Scholar
  78. Wassenaar LI, Hobson KA (2003) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Healt S 39:211–217CrossRefGoogle Scholar
  79. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–83. doi: 10.1016/S0169-5347(01)02380-1 CrossRefGoogle Scholar
  80. Werner SJ, Hobson KA, Van Wilgenburg S, Fischer JW (2016) Multi-Isotopic (δ 2H, δ 13C, δ 15N) tracing of moult origin for Red-winged Blackbirds associated with agro-ecosystems. PLoS ONE 11:e0165996. doi: 10.1371/journal.pone.0165996 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wilcove DS, Wikelski M (2008) Going, going gone: is animal migration disappearing? PLoS Biol 6:e188. doi: 10.1371/journal.pbio.0060188 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wymenga E (1999) Migrating ruffs, Philomachus pugnax, through Europe, spring 1998. Wader Study Group Bull 88:43–48Google Scholar
  83. Wymenga E, Zwarts L (2010) Use of rice fields by birds in West Africa. Waterbirds 33:97–104. doi: 10.1675/063.033.s107 CrossRefGoogle Scholar
  84. Wymenga E, Kone B, van der Kamp J, Zwarts L (2002) Delta intérieur du fleuve Niger: Ecologie et gestion durable des ressources naturelles. A&W/Wetlands International/Rijkswaterstaat, VeenwoudenGoogle Scholar
  85. Yerkes T, Hobson KA, Wassenaar LI, MacLeod R, Colucci JM (2008) Stable isotopes (δ 2H, δ 13C, δ 15N) reveal associations among geographical location and condition of Alaskan northern pintails. J Wildl Manage 72:715–725. doi: 10.2193/2007-115 CrossRefGoogle Scholar
  86. Zwarts L, Bijlsma RG, van der Kamp J, Wymenga E (2009) Living on the edge: wetlands and birds in a Changing Sahel. KNNV Publishing, ZeistGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2017

Authors and Affiliations

  1. 1.Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences (GELIFES)University of GroningenGroningenThe Netherlands
  2. 2.Altenburg & Wymenga Ecological ConsultantsFeanwâldenThe Netherlands
  3. 3.Environment CanadaSaskatoonCanada
  4. 4.Department of BiologyUniversity of Western OntarioLondonCanada
  5. 5.Department of Coastal SystemsNIOZ Royal Netherlands Institute for Sea Research, Utrecht UniversityDen Burg, TexelThe Netherlands

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