Abstract
Numerous studies in both the field and laboratory illustrate factors involved in the endogenous, intrinsic and environmental control of avian migration, but we are lacking an integrated individual-based approach, connecting field and laboratory studies in a single species. The Northern Wheatear Oenanthe oenanthe appeared very feasible for an integrated individual-based one-species approach in the study of the control of bird migration as it can be studied individually in the field as well as kept indoor under controlled ‘common-garden’ conditions. We here present a brief overview of the results collected in our wheatear studies on the intrinsic disposition and extrinsic factors that control migratory behavior in an obligate migratory species.
Similar content being viewed by others
References
Åkesson S, Hedenström A (2000) Wind selectivity of migratory flight departures in birds. Behav Ecol Sociobiol 47:140–144
Alerstam T (1990) Bird migration. Cambridge University Press, Cambridge
Alerstam T (2011) Optimal bird migration revisited. J Ornithol 152:5–23
Alerstam T, Lindström Å (1990) Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner E (ed) Bird migration. Springer, Heidelberg, pp 331–351
Arizaga J, Bairlein F (2011) The role of age, sex, body size and fuel load in determining the social status of a migratory passerine during the non-breeding period. Ornis Fenn 88:154–160
Arizaga J, Schmaljohann H, Bairlein F (2011) Stopover behaviour and dominance: a case study of the Northern Wheatear Oenanthe oenanthe. Ardea 99:157–165
Arlt D, Pärt T (2008) Post-breeding information gathering and breeding territory shifts in Northern Wheatears. J Anim Ecol 77:211–219
Bairlein F (2002) How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89:1–10
Bairlein F (2008) The mysteries of bird migration—still much to be learnt. Br Birds 101:68–81
Bairlein F, Gwinner E (1994) Nutritional mechanisms and temporal control of migratory energy accumulation in birds. Ann Rev Nutr 14:187–215
Bairlein F, Norris DR, Nagel R, Bulte M, Voigt CC, Fox JW, Hussell DJT, Schmaljohann H (2012) Cross-hemisphere migration of a 25-gram songbird. Biol Lett 8:505–507
Bairlein F, Dierschke V, Delingat J, Eikenaar C, Maggini I, Bulte M, Schmaljohann H (2013) Revealing the control of migratory fueling: an integrated approach combining laboratory and field studies in Northern Wheatears Oenanthe oenanthe. Curr Zool 59:381–392
Bakken V, Runde O, Tjørve E (2006) NorskRingmerkingatlas, vol 2. Stavanger Museum, Stavanger
Baldwin MW, Winkler H, Organ CL, Helm B (2010) Wing pointedness associated with migratory distance in common-garden and comparative studies of stonechats (Saxicola torquata). J Evol Biol 23:1050–1063
Berthold P (1996) Control of bird migration. Academic Press, London
Berthold P (2012) Vogelzug, 7th edn. WBG, Darmstadt
Berthold P, Querner U (1981) Genetic basis of migratory behavior in European warblers. Science 212:77–78
Berthold P, Gwinner E, Sonnenschein E (2003) Avianmigration. Springer, Heidelberg
Buchmann M (2001) Die Brutbiologie des Steinschmatzers (Oenanthe oenanthe ) auf intensiv genutzten Flächen in Rheinland-Pfalz. Vogelwarte 41:1–17
Bulte M, Bairlein F (2013) Endogenous control of migratory behaviour in Alaskan Northern Wheatears Oenanthe oenanthe. J Ornithol 154:567–570
Bulte M, McLaren J, Bairlein F, Bouten W, Schmaljohann H, Shamoun-Barranes JZ (2014) Can wheatears weather the Atlantic? Modelling non-stop trans-Atlantic flights of a small migratory songbird. Auk 131:363–370
Bulte M, Maggini I, Bairlein F (2015) Genetic control of fuelling in a cross-hemispheric migratory songbird. PLoS One. (In revision)
Bulyuk VN, Tsvey A (2006) Timing of nocturnal autumn migratory departures in juvenile European Robins (Erithacus rubecula) and endogenous and external factors. J Ornithol 147:298–309
Buurma LS, Lensink R, Linnartz LG (1986) Altitude of diurnal broad front migration over Twente; a comparison of visual and radar observations in October 1984. Limosa 59:169–182
Chernetsov N, Kishkinev D, Kosarev V, Bolshakov CV (2011) Not all songbirds calibrate their magnetic compass from twilight cues: a telemetry study. J Exp Biol 214:2540–2543
Conder P (1989) The wheatear. Christopher Helm, London
Coppack T, Pulido F (2009) Proximate control and adaptive potential of protandrous migration in birds. Integr Comp Biol 49:493–506
Corman A-M, Bairlein F, Schmaljohann H (2014) The nature of the migration route shapes physiological traits and aerodynamic properties in a migratory songbird. Behav Ecol Sociobiol 68:391–402
Cornelius JM, Boswell T, Jenni-Eiermann S, Breuner CW, Ramenofsky M (2013) Contributions of endocrinology to the migration life history of birds. Gen Comp Endocrinol 190:47–60
Cramp S (1988) Handbook of the birds of Europe, the Middle East and North Africa. In: The birds of the Western Palearctic, vol 5. Oxford University Press, Oxford
Currie D, Thompson DBA, Burke T (2000) Patterns of territory settlement and consequences for breeding success in the wheatear Oenanthe oenanthe. Ibis 142:389–398
Dänhardt J, Lindström Å (2001) Optimal departure decisions of songbirds from an experimental stopover site and the significance of weather. Anim Behav 62:235–243
Delingat J, Dierschke V (2000) Habitat utilization by Northern Wheatears (Oenanthe oenanthe) stopping over on an offshore island during migration. Vogelwarte 40:271–278
Delingat J, Dierschke V, Schmaljohann H, Mendel B, Bairlein F (2006) Daily stopovers as optimal migration strategy in a long-distance migrating passerine: the Northern Wheatear Oenanthe oenanthe. Ardea 94:593–605
Delingat J, Bairlein F, Hedenström A (2008) Obligatory barrier crossing and adaptive fuel management in migratory birds: the case of the Atlantic crossing in Northern Wheatears (Oenanthe oenanthe). Behav Ecol Sociobiol 62:1069–1078
Delingat J, Hobson KA, Dierschke V, Schmaljohann H, Bairlein F (2011) Morphometrics and stable isotopes differentiate populations of Northern Wheatears (Oenanthe oenanthe). J Ornithol 152:383–395
Dierschke V, Delingat J (2001) Stopover behaviour and departure decision of Northern Wheatears, Oenanthe oenanthe, facing different onward non-stop flight distances. Behav Ecol Sociobiol 50:535–545
Dierschke V, Delingat J, Schmaljohann H (2003) Time allocation in migrating Northern Wheatears (Oenanthe oenanthe) during stopover: is refuelling limited by food availability or metabolically? J Ornithol 144:33–44
Dierschke V, Mendel B, Schmaljohann H (2005) Differential timing of spring migration in Northern Wheatears Oenanthe oenanthe: hurried males or weak females? Behav Ecol Sociobiol 57:470–480
Dierschke J, Dierschke V, Hüppop K, Hüppop O, Jachmann KF (2011) Die Vogelwelt der Insel Helgoland. OAG Helgoland, Helgoland
Eikenaar C, Schläfke JL (2013) Size and accumulation of fuel reserves at stopover predict nocturnal restlessness in a migratory bird. Biol Lett 9:20130712
Eikenaar C, Schmaljohann H (2015) Wind conditions experienced during the day predict nocturnal restlessness in a migratory songbird. Ibis 157:125–132
Eikenaar C, Fritzsch A, Bairlein F (2013) Corticosterone and migratory fueling in Northern Wheatears facing different barrier crossings. Gen Comp Endocrin 186:181–186
Eikenaar C, Bairlein F, Stöwe M, Jenni-Eiermann S (2014a) Corticosterone, food intake and refueling in a long-distance migrant. Horm Behav 65:480–487
Eikenaar C, Klinner T, Stöwe M (2014b) Corticosterone predicts nocturnal restlessness in a long-distance migrant. Horm Behav 66:324–329
Eikenaar C, Klinner T, Szostek KL, Bairlein F (2014c) Migratory restlessness in captive individuals predicts actual departure in the wild. Biol Lett 10:20140154
Eikenaar C, Klinner T, de Lille T, Bairlein F, Schmaljohann H (2014d) Fuel loss and flexible fuel deposition rates in a long-distance migrant. Behav Ecol Sociobiol 68:1465–1471
Erni B, Liechti F, Bruderer B (2002) Stopover strategies in passerine bird migration: a simulation study. J Theor Biol 219:479–493
Fiedler W (2005) Ecomorphology of the external flight apparatus of blackcaps (Sylvia atricapilla) with different migration behaviour. Ann NY Acad Sci 1046:253–263
Förschler MI, Bairlein F (2011) Morphological shifts of the external flight apparatus across the range of a passerine (Northern Wheatear) with diverging migratory behaviour. PloS One 6:e18732. doi:10.1371/journal.pone.0018732
Fransson T (1998) Patterns of migratory fuelling in Whitethroats Sylvia communis in relation to departure. J Avian Biol 29:569–573
Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, Vallin A (2001) Magnetic cues trigger extensive refuelling. Nature 414:35–36
Glutz von Blotzheim UN, Bauer KM (1988) Handbuch der Vögel Mitteleuropas, vol 11. Aula, Wiesbaden
Gwinner E (1986) Circannual rhythms. Springer, Berlin
Gwinner E (1990) Bird migration. Springer, Heidelberg
Gwinner E (1996) Circannual clocks in avian reproduction and migration. Ibis 138:47–63
Gwinner E (2009) Circannual rhythms. Endogenous annual clocks in the organizations of seasonal processes. Springer, Heidelberg
Haftorn S (1971) Norges fugler. Universitetsforlaget, Oslo
Hedenström A, Alerstam T (1997) Optimum fuel loads in migratory birds: Distinguishing between time and energy minimization. J Theor Biol 189:227–234
Jenni L, Schaub M (2003) Behavioural and physiological reactions to environmental variation in bird migration: a review. In: Berthold P, Gwinner, E, Sonnenschein E (eds) Avian migration. Springer, Berlin, pp 155–171
Kullberg C, Henshaw I, Jakobson S, Johansson P, Fransson T (2007) Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect. Proc R Soc Lond B 274:2145–2151
Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at baseline as compared to stress-related levels in the regulation of periodic life seasonal processes. Gen Comp Endocrinol 148:132–149
Liechti F (2006) Birds: blowin’ by the wind? J Ornithol 147:202–211
Lindström A, Alerstam T (1992) Optimal fat loads in migrating birds: a test of the time-minimization hypothesis. Am Nat 140:477–491
Maggini I, Bairlein F (2010) Endogenous rhythms of seasonal migratory body mass changes and nocturnal restlessness in different populations of Northern Wheatear Oenanthe oenanthe. J Biol Rhythm 25:268–276
Maggini I, Bairlein F (2012) Innate sex differences in the timing of spring migration in a songbird. PLoS One 7(2):e31271. doi:10.1371/journal.pone.0031271
Maggini I, Spina F, Voigt CC, Ferri A, Bairlein F (2013) Differential migration in Northern Wheatears (Oenanthe oenanthe) at a Mediterranean spring stopover site. J Ornithol 154:321–328
Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886
Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673
Morozova O, Marra MA (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92:255–264
Muheim R, Moore FR, Phillips JB (2006) Calibration of magnetic and celestial compass cues in migratory birds—a review of cue-conflict experiments. J Exp Biol 209:2–17
Newton I (2008) The migration ecology of birds. Elsevier, Amsterdam
Norberg UM (1990) Vertebrate flight: mechanics, physiology, morphology, ecology and evolution. Springer, Heidelberg
Pärt T (2001) The effect of territory quality on age-dependent reproductive performance in the Northern Wheatear, Oenanthe oenanthe. Anim Behav 62:379–388
Ramenofsky M, Wingfield JC (2006) Behavioral and physiological conflicts in migrants: the transition between migration and breeding. J Ornithol 47:135–145
Rappole JH (2013) The avian migrant. Columbia University Press, New York
Sapir N, Wikelski M, Avissar R, Nathan R (2011) Timing and flight mode of departure in migrating European bee-eaters in relation to multi-scale meteorological processes. Behav Ecol Sociobiol 65:1353–1365
Schmaljohann H, Dierschke V (2005) Optimal bird migration and predation risk: a field experiment with Northern Wheatears Oenanthe oenanthe. J Anim Ecol 74:131–138
Schmaljohann H, Naef-Daenzer B (2011) Body condition and wind support initiate shift in migratory direction and timing of nocturnal departure in a free flying songbird. J Anim Ecol 80:1115–1122
Schmaljohann H, Becker PJJ, Karaardic H, Liechti F, Naef-Daenzer B, Grande C (2011) Nocturnal exploratory flights, departure time, and direction in a migratory songbird. J Ornithol 152:439–452
Schmaljohann H, BuchmannM Fox JW, Bairlein F (2012a) Tracking migration routes and the annual cycle of a trans-Sahara songbird migrant. Behav Ecol Sociobiol 66:915–922
Schmaljohann H, Fox JW, Bairlein F (2012b) Phenotypic response to environmental cues, orientation, and costs of migration in songbirds flying half around the world. Anim Behav 84:623–640
Schmaljohann H, Korner-Nievergelt F, Naef-Daenzer B, Nagel R, Maggini I, Bulte M, Bairlein F (2013) Optimization of stopover in an Arctic long-distance migrant: the role of fuel load, ambient temperature and nocturnal take-off time. Front Zool 10:26
Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18
Smith RJ, Moore FR (2003) Arrival fat and reproductive performance in a long-distance passerine migrant. Oecologia 134:325–331
Smolinsky JA, Diehl RH, Radzio TA, Delaney DK, Moore FR (2013) Factors influencing the movement biology of migrant songbirds confronted with an ecological barrier. Behav Ecol Sociobiol 67:2041–2051
Spina F, Massi A, Montemaggiori A (1994) Back from Africa: who’s running ahead? Aspects of differential migration of sex and age classes in palearctic-african spring migrants. Ostrich 65:137–150
Thorup K, Ortvad TE, Rabøl J (2006) Do Nearctic Northern Wheatears (Oenanthe oenanthe) migrate nonstop to Africa? Condor 108:446–451
Tøttrup AP, Thorup K (2008) Sex-differentiated migration patterns, protandry and phenology in North European songbird populations. J Ornithol 149:161–167
Van Oosten HH, Versluijs R, Van Wijk R (2014) Migration routes and wintering areas of two Dutch Northern Wheatears Oenanthe oenanthe in the Sahel. Limosa 87:168–173
Wingfield JC, Schwabl H, Mattocks PW Jr (1990) Endocrine mechanisms of migration. In: Gwinner E (ed) Bird migration. Springer, Heidelberg, pp 232–256
Yamaguchi N, Arisawa Y, Shimada Y, Higuchi (2012) Real-time weather analysis reveals the adaptability of direct sea-crossing by raptors. J Ethol 30:1–10
Acknowledgments
This work was supported financially by the Deutsche Forschungsgemeinschaft (BA 816; SCHM 2647). We are also very grateful to the many other supporters who are listed in the respective publications.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Matthysen.
Rights and permissions
About this article
Cite this article
Bairlein, F., Eikenaar, C. & Schmaljohann, H. Routes to genes: unravelling the control of avian migration—an integrated approach using Northern Wheatear Oenanthe oenanthe as model organism. J Ornithol 156 (Suppl 1), 3–14 (2015). https://doi.org/10.1007/s10336-015-1224-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-015-1224-3