Skip to main content

Advertisement

SpringerLink
Log in

How do energy stores and changes in these affect departure decisions by migratory birds? A critical view on stopover ecology studies and some future perspectives

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

In birds, accumulating energy is far slower than spending energy during flight. During migration, birds spend, therefore, most of the time at stopover refueling energy used during the previous flight. This elucidates why current energy stores and actual rate of accumulating energy are likely crucial factors influencing bird’s decision when to resume migration in addition to other intrinsic (sex, age) and extrinsic (predation, weather) factors modulating the decision within the innate migration program. After first summarizing how energy stores and stopover durations are generally determined, we critically review that high-energy stores and low rates of accumulating energy were significantly related to high departure probabilities in several bird groups. There are, however, also many studies showing no effect at all. Recent radio-tracking studies highlighted that migrants leave a site either to resume migration or to search for a better stopover location, so-called “landscape movements”. Erroneously treating such movements as departures increases the likelihood of type II errors which might mistakenly suggest no effect of either trait on departure. Furthermore, we propose that energy loss during the previous migratory flight in relation to bird’s current energy stores and migration strategy significantly affects its urge to refuel and hence its departure decision.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adamík P, Emmenegger T, Briedis M, Gustafsson L, Henshaw I, Krist M, Laaksonen T, Liechti F, Procházka P, Salewski V, Hahn S (2016) Barrier crossing in small avian migrants: individual tracking reveals prolonged nocturnal flights into the day as a common migratory strategy. Sci Rep 6:21560

  • Åkesson S, Hedenström A (2007) How migrants get there: migratory performance and orientation. Bioscience 57:123–133

    Article  Google Scholar 

  • Åkesson S, Karlsson L, Walinder G, Alerstam T (1996) Bimodal orientation and the occurrence of temporary reverse bird migration during autumn in south Scandinavia. Behav Ecol Sociobiol 38:293–302

    Article  Google Scholar 

  • Åkesson S, Klaassen RHG, Holmgren J, Fox JW, Hedenström A (2012) Migration routes and strategies in a highly aerial migrant, the Common Swift Apus apus, revealed by light-level geolocators. PLoSONE 7:e41195

  • Åkesson S, Bianco G, Hedenström A (2016) Negotiating an ecological barrier: crossing the Sahara in relation to winds by common swifts. Phil Trans R Soc B 371:20150393

  • Alerstam T (1978) Reoriented bird migration in coastal areas: dispersal to suitable resting grounds? Oikos 30:405–408

    Article  Google Scholar 

  • Alerstam T (1990) Bird Migration. Cambridge University Press, Cambridge

    Google Scholar 

  • Alerstam T (2001) Detours in Bird Migration. J Theor Biol 209:319–331

    Article  CAS  PubMed  Google Scholar 

  • Alerstam T (2009) Flight by night or day? Optimal daily timing of bird migration. J Theor Biol 258:530–536

    Article  PubMed  Google Scholar 

  • Alerstam T (2011) Optimal bird migration revisited. J Ornithol 152:5–23

    Article  Google Scholar 

  • Alerstam T, Lindström à (1990) Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer, Berlin Heidelberg, pp 331–351

    Chapter  Google Scholar 

  • Alerstam T, Hedenström A, Åkesson S (2003) Long-distance migration: evolution and determinants. Oikos 103:247–260

    Article  Google Scholar 

  • Archibald KM, Buler JJ, Smolinsky JA, Smith RJ (2017) Migrating birds reorient toward land at dawn over the Great Lakes. Auk 134:193–201

    Article  Google Scholar 

  • Arizaga J, Belda EJ, Barba E (2011) Effect of fuel load, date, rain and wind on departure decisions of a migratory passerine. J Ornithol 152:991–999

    Article  Google Scholar 

  • Arzel C, Elmberg J, Guillemain M (2006) Ecology of spring-migrating Anatidae: a review. J Ornithol 147:167–184

    Article  Google Scholar 

  • Babak N (2013) usdm: Uncertainty analysis for species distribution models. R package version 11–12. http://CRAN.R-project.org/package=usdm. Accessed 08 Mar 2017

  • Bächler E, Liechti F (2007) On the importance of g(0) for estimating bird population densities with standard distance-sampling: implications from a telemetry study and a literature review. Ibis 149:693–700

    Article  Google Scholar 

  • Bächler E, Schaub M (2007) The effects of permanent local emigration and encounter technique on stopover duration estimates as revealed by telemetry and mark-recapture. Condor 109:142–154

    Article  Google Scholar 

  • Bäckman J, Andersson A, Alerstam T, Pedersen L, Sjöberg S, Thorup K, Tøttrup AP (2017) Activity and migratory flights of individual free-flying songbirds throughout the annual cycle: method and first case study. J Avian Biol 48:309–319

    Article  Google Scholar 

  • Baird J, Nisbet ICT (1960) Northward fall migration on the Atlantic coast and its relation to offshore drift. Auk 77:119–149

    Article  Google Scholar 

  • Bairlein F (1983) Habitat selection and associations of species in European passerine birds during southward, post-breeding migrations. Ornis Scand 14:239–245

  • Bairlein F (1985a) Autumn migration of palaearctic waterbirds across the Algerian Sahara. Avocetta 9:63–72

  • Bairlein F (1985b) Body weights and fat deposition of Palaearctic passerine migrants in the central Sahara. Oecologia 66:141–146

    Article  PubMed  Google Scholar 

  • Bairlein F (1991) Body mass of Garden Warblers (Sylvia borin) on migration: a review of field data. Vogelwarte 36:48–61

  • Bairlein F (1994) Manual of field methods. European-African Songbird Migration. Institut für Vogelforschung, Wilhelmshaven

  • Bairlein F, Beck P, Feiler W, Querner U (1983) Autumn weights of some Palaearctic passerine migrants in the Sahara. Ibis 125:404–407

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Bairlein F, Dierschke J, Dierschke V, Salewski V, Geiter O, Hüppop K, Köppen U, Fiedler W (2014) Atlas des Vogelzugs. Ringfunde deutscher Brut- und Gastvögel. AULA-Verlag, Wiebelsheim

    Google Scholar 

  • Bairlein F, Eikenaar C, Schmaljohann H (2015a) Routes to genes: unravelling the control of avian migration—an integrated approach using Northern Wheatear Oenanthe oenanthe as model organism. J Ornithol 156:S3–S14

    Article  Google Scholar 

  • Bairlein F, Fritz J, Scope A, Schwendenwein I, Stanclova G, van Dijk G, Meijer HAJ, Verhulst S, Dittami J (2015b) Energy expenditure and metabolic changes of free-flying migrating Northern Bald Ibis. PLoSONE 10:e0134433

  • Bates D, Mächler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 11–7. http://CRAN.R-project.org/packages=lme4. Accessed 08 Mar 2017

  • Battley PF, Piersma T, Dietz MW, Tang S, Dekinga A, Hulsman K (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc R Soc Lond B 267:191–195

    Article  CAS  Google Scholar 

  • Battley PF, van Gils JA, Piersma T, Hassell CJ, Boyle A, Hong-Yan Y (2005) How do red knots Calidris canutus leave Northwest Australia in May and reach the breeding grounds in June? Predictions of stopover times, fuelling rates and prey quality in the Yellow Sea. J Avian Biol 36:494–500

    Article  Google Scholar 

  • Battley PF, Warnock N, Tibbitts TL, Gill RE, Piersma T, Hassell CJ, Douglas DC, Mulcahy DM, Gartell BD, Schuckard R, Melville DS, Riegen A (2012) Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J Avian Biol 43:21–32

    Article  Google Scholar 

  • Bauchinger U, Biebach H (2001) Differential catabolism of muscle protein in Garden Warblers (Sylvia borin): flight and leg muscle act as a protein source during long-distance migration. J Comp Physiol B 171:293–301

    Article  CAS  PubMed  Google Scholar 

  • Bauchinger U, Klaassen M (2005) Longer days in spring than in autumn accelerate migration speed of passerine birds. J Avian Biol 36:3–5

    Article  Google Scholar 

  • Bauchinger U, McWilliams S (2009) Carbon turnover in tissues of a passerine bird: Allometry, isotopic clocks, and phenotypic flexibility in organ size. Physiol Biochem Zool 82:787–797

    Article  PubMed  Google Scholar 

  • Bauer S, Gienapp P, Madsen J (2008) The relevance of environmental conditions for departure decision changes en route in migrating geese. Ecology 89:1953–1960

    Article  PubMed  Google Scholar 

  • Bayly NJ (2006) Optimality in avian migratory fuelling behaviour: a study of a trans-Saharan migrant. Anim Behav 71:173–182

    Article  Google Scholar 

  • Bayly NJ (2007) Extreme fattening by sedge warblers, Acrocephalus schoenobaenus, is not triggered by food availability alone. Anim Behav 74:471–479

    Article  Google Scholar 

  • Bayly NJ, Gómez C (2011) Comparison of autumn and spring migration strategies of Neotropical migratory landbirds in northeast Belize. J Field Ornithol 82:117–131

    Article  Google Scholar 

  • Bayly NJ, Atkinson PW, Rumsey SJR (2012) Fuelling for the Sahara crossing: variation in site use and the onset and rate of spring mass gain by 38 Palearctic migrants in the western Sahel. J Ornithol 153:931–945

    Article  Google Scholar 

  • Bayly NJ, Gómez C, Hobson KA (2013) Energy reserves stored by migrating Gray-cheeked Thrushes Catharus minimus at a spring stopover site in northern Colombia are sufficient for a long-distance flight to North America. Ibis 155:271–283

    Article  Google Scholar 

  • Bensch S, Akesson S, Irwin DE (2002) The use of AFLP to find an informative SNP: genetic differences across a migratory divide in willow warblers. Mol Ecol 11:2359–2366

    Article  CAS  PubMed  Google Scholar 

  • Berthold P (1996) Control of bird migration. 1 edn. Chapman & Hall, London

    Google Scholar 

  • Berthold P, Querner U (1981) Genetic basis of migratory behavior in European warblers. Science 212:77–79

    Article  CAS  PubMed  Google Scholar 

  • Bibby CJ, Green RE (1981) Autumn migration strategies of reed and sedge warblers. Ornis Scand 12:1–12

  • Biebach H (1985) Sahara stopover in migratory flycatchers: fat and food affect the time progam. Experientia 41:695–697

    Article  Google Scholar 

  • Biebach H, Friedrich W, Heine G (1986) Interaction of bodymass, fat, foraging and stopover period in trans-sahara migrating passerine birds. Oecologia 69:370–379

    Article  CAS  PubMed  Google Scholar 

  • Biesel W, Nachtigall W (1987) Pigeon flight in a wind tunnel. IV. Thermoregulation and water homeostasis. J Comp Physiol B 157:117–128

    Article  Google Scholar 

  • Bohrer G, Brandes D, Mandel JT, Bildstein KL, Miller TA, Lanzone M, Katzner T, Maisonneuve C, Tremblay JA (2011) Estimating updraft velocity components over large spatial scales: contrasting migration strategies of golden eagles and turkey vultures. Ecol Lett 15:96–103

    Article  PubMed  Google Scholar 

  • Bolshakov CV, Bulyuk VN, Sinelschikova A (2000) Study of nocturnal departures in small passerine migrants: retrapping of ringed birds in high mist-nets. Vogelwarte 40:250–257

  • Bolshakov CV, Bulyuk VN, Chernetsov N (2003) Spring nocturnal migration of Reed Warblers Acrocephalus scirpaceus: departure, landing and body condition. Ibis 145:106–112

    Article  Google Scholar 

  • Bouten W, Baaij EW, Shamoun-Baranes J, Camphuysen KCJ (2013) A flexible GPS tracking system for studying bird behaviour at multiple scales. J Ornithol 154:571–580

    Article  Google Scholar 

  • Bowler JM (1994) The condition of Bewick’s swans Cygnus columbianus bewickii in winter as assessed by their abdominal profile. Ardea 82:241–248

    Google Scholar 

  • Bowlin MS, Wikelski M (2008) Pointed wings, low wingloading and calm air reduce migratory flight costs in songbirds. PLoSONE 3:e2154

  • Boyd H, Fox AD (1995) Abdominal profiles of Icelandic pink-footed geese Anser brachyrhynchus in spring. Wildfowl 46:161–175

  • Bridge ES, Thorup K, Bowlin MS, Chilson PB, Diehl RH, Fléron RW, Hartl P, Kays R, Kelly JF, Robinson WD, Wikelski M (2011) Technology on the move: Recent and forthcoming innovations for tracking migratory birds. Bioscience 61:689–698

    Article  Google Scholar 

  • Brown ME (1996) Assessing body condition in birds. Curr Ornithol 13:67–135

  • Brown JM, Taylor PD (2015) Adult and hatch-year blackpoll warblers exhibit radically different regional-scale movements during post-fledging dispersa. Biol Lett 11:20150593

    Article  PubMed Central  PubMed  Google Scholar 

  • Bruderer B (1994) Radar studies on nocturnal bird migration in the Negev. Ostrich 65:204–212

  • Bruderer B, Liechti F (1995) Variation in density and height distribution of nocturnal migration in the south of Israel. Isr. J Zool 41:477–487

    Google Scholar 

  • Bruderer B, Liechti F (1998) Flight behaviour of nocturnally migrating birds in coastal areas—crossing or coasting. J Avian Biol 29:499–507

    Article  Google Scholar 

  • Bruderer B, Liechti F (1999) Bird migration across the Mediterranean. In: Adam N, Slotow R (eds) Proc. Int. Ornithol. Congr. Birdlife South Africa, Durban, pp 1983–1999

  • Bulte M, Heyers D, Mouritsen H, Bairlein F (2017) Geomagnetic information modulates nocturnal migratory restlessness but not fueling in a long distance migratory songbird. J Avian Biol 48:75–82

    Article  Google Scholar 

  • Bulyuk VN (2012) Influence of fuel load and weather on timing of nocturnal spring migratory departures in European robins, Erithacus rubecula. Behav Ecol Sociobiol 66:385–395

    Article  Google Scholar 

  • Bulyuk VN, Tsvey A (2013) Regulation of stopover duration in the European Robin Erithacus rubecula. J Ornithol 154:1115–1126

    Article  Google Scholar 

  • Butler PJ, Woakes AJ (1980) Heart rate, respiratory frequency and wing beat frequency of free flying barnacle geese Branta leucopsis. J Exp Biol 85:213–226

    Google Scholar 

  • Butler PJ, Woakes AJ, Bevan RM, Stephenson R (2000) Heart rate and rate of oxygen consumption during flight of the barnacle goose, Branta leucopsis. Comp Biochem Phys A 126:379–385

    Article  CAS  Google Scholar 

  • Cantos FJ, Tellerìa JL (1994) Stopover site fidelity of four migrant warblers in the Iberian Peninsula. J Avian Biol 25:131–134

    Article  Google Scholar 

  • Carmi N, Pinshow B, Porter WP, Jaeger J (1992) Water and energy limitations on flight duration in small migrating birds. Auk 109:268–276

    Article  Google Scholar 

  • Carpenter FL, Paton DC, Hixon MA (1983) Weight gain and adjustment of feeding territory size in migrant hummingbirds. PNAS 80:7259–7263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Catry P, Encarnacão V, Araújo A, Fearon P, Fearon A, Armelin M, Delaloye P (2004) Are long-distance migrant passerines faithful to their stopover sites? J Avian Biol 35:170–181

    Article  Google Scholar 

  • Chernetsov N (2006) Habitat selection by nocturnal passerine migrants en route: mechanisms and results. J Ornithol 47:185–191

    Article  Google Scholar 

  • Chernetsov N (2012) Passerine migration—stopovers and flight. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Cherry JD (1982) Fat deposition and length of stopover of migrant white-crowned sparrows. Auk 99:725–732

    Google Scholar 

  • Chevallier D, Handrich Y, Georges J-Y, Baillon F, Brossault P, Aurouet A, Le Maho Y, Massemin S (2010) Influence of weather conditions on the flight of migrating black storks. Proc R Soc Lond B 277:2755–2764

    Article  CAS  Google Scholar 

  • Clausen P, Green M, Alerstam T (2003) Energy limitations for spring migration and breeding: the case of brent geese Branta bernicla tracked by satellite telemetry to Svalbard and Greenland. Oikos 103:426–445

    Article  Google Scholar 

  • Cohen EB, Moore FR, Fischer RA (2012) Experimental evidence for the interplay of exogenous and endogenous factors on the movement ecolgy of a migrating songbird. PLoSONE 7:e41818

  • Cohen EB, Moore FR, Fischer RA (2014) Fuel stores, time of spring, and movement behvior influence stopover duration of Red-eyed Vireo Vireo olivaceus. J Ornithol 155:785–792

    Article  Google Scholar 

  • Conklin J, Battley PF (2011) Impacts of wind on individual migration schedules of New Zealand bar-tailed godwits. Behav Ecol 22:854–861

    Article  Google Scholar 

  • Cormack RM (1964) Estimates of survival from the sighting of marked animals. Biometrika 51:429–438

    Article  Google Scholar 

  • Corman AM, 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

    Article  Google Scholar 

  • Crysler ZJ, Ronconi RA, Taylor PD (2016) Differential fall migratory routes of adult and juvenile Ipswich Sparrows (Passerculus sandwichensis princeps). Mov Ecol 4:3

  • Dänhardt J, Lindström à (2001) Optimal departure decisions of songbirds from an experimental stopover site and the significance of weather. Anim Behav 62:235–243

    Article  Google Scholar 

  • 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. Ardea 94:593–605

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Delingat J, Dierschke V, Schmaljohann H, Bairlein F (2009) Diurnal patterns in body mass change during stopover in a migrating songbird. J Avian Biol 40:625–634

    Article  Google Scholar 

  • DeLuca WV, Woodworth BK, Rimmer CC, Marra PP, Taylor PD, McFarland KP, Mackenzie SA, Norris DR (2015) Transoceanic migration by a 12 g songbird. Biol Lett 11:20141045

    Article  PubMed Central  PubMed  Google Scholar 

  • Deppe JL, Ward MP, Bolus RT, Diehl RH, Celis-Murillo A, Zenzal TJ, Moore FR, Benson TJ, Smolinsky JA, Schofield LN, Enstrom DA, Paxton EH, Bohrer G, Beveroth TA, Raim A, Obringer RL, Delaney D, Cochran WW (2015) Fat, weather, and date affect migratory songbirds’ departure decisions, routes, and time it takes to cross the Gulf of Mexico. PNAS 112:E6331–E6338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deutschlander ME, Muheim R (2009) Fuel reserves affect migratory orientation of thrushes and sparrows both before and after crossing an ecological barrier near their breeding grounds. J Avian Biol 40:1–5

    Article  Google Scholar 

  • Dierschke V (2002) Kaum ein Vogel kehrt zurück: Geringe Rastplatztreue von ziehenden Landvögeln zur Nordseeinsel Helgoland. Vogelwarte 41:190–195

  • 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

    Article  Google Scholar 

  • Dierschke V, Delingat J (2003) Stopover of Northern Wheatears Oenanthe oenanthe at Helgoland: where do the migratory routes of Scandinavian and Nearctic birds join and split? Ornis Svecica 13:53–61

  • 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

    Article  Google Scholar 

  • Dietz MW, Dekinga A, Piersma T, Verhulst S (1999a) Estimating organ size in small migrating shorebirds with ultrasonography: an intercalibration exercise. Physiol Biochem Zool 72:28–37

    Article  CAS  PubMed  Google Scholar 

  • Dietz MW, Piersma T, Dekinga A (1999b) Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J Exp Biol 202:2831–2837

    PubMed  Google Scholar 

  • Dorka V (1966) Das jahres- und tageszeitliche Zugmuster von Kurz- und Langstreckenziehern nach Beobachtungen auf den Alpenpässen Cou/Bretolet (Wallis). Ornithol Beob 63:165–223

  • Dossmann BC, Mitchell GW, Norris DR, Taylor PD, Guglielmo CC, Matthews SN, Rodewald PG (2015) The effects of wind and fuel stores on stopover departure behavior across a migratory barrier. Behav Ecol 27:567–574

    Article  Google Scholar 

  • Dowsett JR, Fry CH (1971) Weight losses of trans-saharan migrants. Ibis 113:531–533

    Article  Google Scholar 

  • Drost R (1941) Zieht der einzelne Vogel stets auf demselben Weg? Ardea 30:215–223

    Google Scholar 

  • Duriez O, Bauer S, Destin A, Madsen J, Nolet BA, Stillman RA, Klaassen M (2009) What decision rules might pink-footed geese use to depart on migration? An individual-based model. Behav Ecol 20:560–569

    Article  Google Scholar 

  • Eikenaar C, Bairlein F (2014) Food availability and fuel loss predict Zugunruhe. J Ornithol 155:65–70

    Article  Google Scholar 

  • Eikenaar C, Schläfke L (2013) Size and accumulation of fuel reserves at stopover predict nocturnal restlessness in a migratory bird. Biol Lett 9:0130712

    Article  Google Scholar 

  • Eikenaar C, Klinner T, de Lille T, Bairlein F, Schmaljohann H (2014a) Fuel loss and flexible fuel deposition rates in a long-distance migrant. Behav Ecol Sociobiol 68:1465–1471

    Article  Google Scholar 

  • Eikenaar C, Klinner T, Szostek KL, Bairlein F (2014b) Migratory restlessness in captive individuals predicts actual departure in the wild. Biol Lett 10:20140154

    Article  PubMed Central  PubMed  Google Scholar 

  • Eikenaar C, Fritzsch A, Kämpfer S, Schmaljohann H (2016) Migratory restlessness increases and refuelling rate decreases over the spring migration season in northern wheatears. Anim Behav 112:75–81

    Article  Google Scholar 

  • Eikenaar C, Källstig E, Andersson MN, Herrera-Dueñas A, Isaksson C (2017) Oxidative challenges of avian migration: a comparative field study on a partial migrant. Physiol Biochem Zool 90:223–229

    Article  PubMed  Google Scholar 

  • Ellegren H (1991) Stopover ecology of autumn migrating Bluethroats Luscinia s. svecica in relation to age and sex. Ornis Scand 22:340–348

    Article  Google Scholar 

  • Erni B, Liechti F, Bruderer B (2002a) Stopover strategies in passerine bird migration: a simulation study. J Theor Biol 219:479–493

    Article  PubMed  Google Scholar 

  • Erni B, Liechti F, Underhill LG, Bruderer B (2002b) Wind and rain govern the intensity of nocturnal bird migration in central Europe—a log-linear regression analysis. Ardea 90:155–166

    Google Scholar 

  • Féret M, Bêty J, Gauthier G, Giroux J-F, Picard G (2005) Are abdominal profiles useful to assess body condition of spring staging Greater Snow Geese? Condor 107:694–702

    Article  Google Scholar 

  • Fiedler W (2009) New technologies for monitoring bird migration and behaviour. Ringing Migration 24:175–179

    Article  Google Scholar 

  • Finlayson JC (1981) Seasonal distribution, weights and fat of passerine migratns at Gibraltar. Ibis 123:88–95

    Article  Google Scholar 

  • Fortin D, Liechti F, Bruderer B (1999) Variation in the nocturnal flight behaviour of migratory birds along the northwest coast of the Mediterranean Sea. Ibis 141:480–488

    Article  Google Scholar 

  • Fox AD, Hilmarsson JO, Einarsson O, Walsh AJ, Boyd H, Kristiansen JN (2002) Staging site fidelity of Greenland white-fronted geese (Anser albifrons flavirostris) in Iceland. Bird Study 49:42–49

  • Fransson T (1998a) A feeding experiment on migratory fuelling in whitethroats, Sylvia communis. Anim Behav 55:153–162

    Article  CAS  PubMed  Google Scholar 

  • Fransson T (1998b) Patterns of migratory fuelling in Whitethroats Sylvia communis in relation to departure. J Avian Biol 29:569–573

    Article  Google Scholar 

  • Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, Vallin A (2001) Magnetic cues trigger extensive refuelling. Nature 414:35–36

    Article  CAS  PubMed  Google Scholar 

  • Fry CH, Ash JS, Ferguson-Lees IJ (1970) Spring weights of some Palaearctic migrants at lake Chad. Ibis 112:58–82

    Article  Google Scholar 

  • Gauthreaux SA Jr (1971) A radar and direct visual study of Passerine spring migration in Southern Louisiana. Auk 88:343–365

    Article  Google Scholar 

  • Giladi I, Pinshow B (1999) Evaporative and excretory water loss during free flight in pigeons. J Comp Physiol B 169:311–318

    Article  Google Scholar 

  • Gill RE, 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

    Article  Google Scholar 

  • Gillings S, Atkinson PW, Baker AJ, Bennett KA, Clark NA, Cole KB, González PM, Kalasz KS, Minton CDT, Niles LJ, Porter RC, Serrano IDL, Sitters HP, Woods JL (2009) Staging Behavior in Red Knot (Calidris Canutus) in Delaware BAY: Implications for Monitoring Mass and Population Size. Auk 126:54–63

    Article  Google Scholar 

  • Gosler AG (1991) On the use of greater covert moult and pectoral muscle as measures of condition in passerines with data for the Great Tit Parus major. Bird Study 38:1–9

  • Goymann W, Spina F, Ferri A, Fusani L (2010) Body fat influences departure from stopover sites in migratory birds: evidence from whole island telemetry. Biol Lett 6:478–481

    Article  PubMed Central  PubMed  Google Scholar 

  • Green AJ (2001) Mass/length residuals: Measures of body cndition or generators of spurious results? Ecology 82:1473–1483

    Article  Google Scholar 

  • Green M, Alerstam T, Clausen P, Drent R, Ebbinge BS (2002) Dark-bellied Brent Geese Branta bernicla bernicla, as recorded by satellite telemetry, do not minimze flight distance during spring migration. Ibis 144:106–121

    Article  Google Scholar 

  • Guglielmo CC, Piersma T, Williams TD (2001) A sport-physiological perspective on bird migration: evidence for flight-induced muscle damage. J Exp Biol 204:2683–2690

    CAS  PubMed  Google Scholar 

  • Guglielmo CC, McGuire LP, Gerson AR, Seewagen CL (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J Ornithol 152:S75–S85

    Article  Google Scholar 

  • Gwinner E (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48

    CAS  PubMed  Google Scholar 

  • Gwinner E (2009) Circannual rhythms. Endogenous annual clocks in the organizations of seasonal processes. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Gwinner E, Wiltschko W (1978) Endogenously controlled changes in migratory direction of the garden warbler, Sylvia borin. J Comp Physiol A 125:267–273

    Article  Google Scholar 

  • Harrington BA, Hagan JH, Leddy LE (1988) Site fidelity and survival differences between two groups of New World red knots (Calidris canutus). Auk 105:439–445

    Google Scholar 

  • Hayes JP, Shonkwiler JS (2001) Morphometric indicators of body condition: worthwhile or wishful thinking? In: Spearman JR (ed) Body composition analysis of animals: a handbook of non-destructive methods. Cambridge University Press, Cambridge, pp 8–38

    Chapter  Google Scholar 

  • Hedenström A (2002) Aerodynamics, evolution and ecology of avian flight. TREE 17:415–422

    Google Scholar 

  • Hedenström A (2008) Adaptations to migration in birds: behavioural strategies, morphology and scaling effects. Phil Trans R Soc B 363:287–299

  • Hedenström A, Alerstam T (1997) Optimum fuel loads in migratory birds: Distinguishing between time and energy minimization. J Theor Biol 189:227–234

    Article  PubMed  Google Scholar 

  • Helms CW, Drury WHJ (1960) Winter and migratory weight and fat field studies on some north American buntings. Bird Banding 31:1–36

  • Henkel JR, Taylor CM (2015) Migration strategy predicts stopover ecology in shorebirds on the northern Gulf of Mexico. Anim Mig 2:63–75

  • Holmgren N, Ellegren H, Pettersson J (1993) Stopover length, body mass and fuel deposition rate in autumn migrating adult Dunlins Calidris alpina: evaluating the effects of moulting status and age. Ardea 81:9–20

    Google Scholar 

  • Hutto RL (1985) Habitat selection by nonbreeding, migratory land birds. In: Cody ML (ed) Habitat selection in birds. Acedemic Press, London, pp 455–476

    Google Scholar 

  • Jahn AE, Cuteo VR, Fox JW, Husak MS, Kim DH, Landoll DV, Ledezma JP, LePage HK, Levey DJ, Murphy MT, Renfrew RB (2013) Migration timing and wintering areas of three species of flycatchers (Tyrannus) breeding in the Great Plains of North America. Auk 130:247–257

    Article  Google Scholar 

  • Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528

    Article  Google Scholar 

  • 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 Heidelberg, pp 155–171

    Chapter  Google Scholar 

  • Jenni-Eiermann S, Almasi B, Maggini I, Salewski V, Bruderer B, Liechti F, Jenni L (2011) Numbers, foraging and refuelling of passerine migrants at a stopover site in the western Sahara: diverse strategies to cross a desert. J Ornithol 152:S113–S128

    Article  Google Scholar 

  • Jenni-Eiermann S, Jenni L, Smith S, Costantini D (2014) Oxidative stress in endurance flight: An unconsiderd factor in bird migration. PLoSONE 9:e97650

  • Johnson AB, Winker K (2008) Autumn stopover near the Gulf of Honduras by Nearctic-Neotropic migrants. Wilson. J Ornithol 120:277–285

    Google Scholar 

  • Johnson DH, Krapu GL, Reinecke KJ, Jorde DG (1985) An evaluation of condition indices for birds. J Wildlife Manage 49:569–575

    Article  Google Scholar 

  • Jolly G (1965) Explicit estimates from capture-recapture data with both death and immigration-stochastic model. Biometrika 52:225–247

    Article  CAS  PubMed  Google Scholar 

  • Jones PJ (1995) Migration strategies of palearctic passerines in Africa. Isr. J Zool 41:393–406

    Google Scholar 

  • Jouventin P, Weimerskirch H (1990) Satellite tracking of Wandering albatrosses. Nature 343:746–748

    Article  Google Scholar 

  • Kaiser A (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. J Field Ornithol 64:246–255

    Google Scholar 

  • Karlsson H, Nilsson C, Bäckman J, Alerstam T (2012) Nocturnal passerine migrants fly faster in spring than in autumn: a test of the time minimization hypothesis. Anim Behav 83:87–93

    Article  Google Scholar 

  • Kerlinger P (1989) Flight strategies of migrating hawks. University of Chicago Press, Chicago

    Google Scholar 

  • Klaassen M (2004) May dehydration risk govern long-distance migratory behaviour? J Avian Biol 35:4–6

    Article  Google Scholar 

  • Klaassen RHG, Alerstam T, Carlsson P, Fox JW, Lindström à (2011) Great flights by great snipes: long and fast non-stop migration over benign habitats. Biol Lett 7:833–835

    Article  PubMed Central  PubMed  Google Scholar 

  • Knudsen E, Lindén A, Both C, Jonzén N, Pulido F, Saino N, Sutherland WJ, Bach LA, Coppack T, Ergon T, Gienapp P, Gill JA, Gordo O, Hedenström A, Lehikoinen E, Marra PP, Møller AP, Nilsson ALK, Péron G, Ranta E, Rubolini D, Sparks TH, Spina F, Studds CE, Sæther SA, Tryjanowski P, Stenseth NC (2011) Challenging claims in the study of migratory birds and climate change. Biol Rev 86:928–946

    Article  PubMed  Google Scholar 

  • Komenda-Zehnder S, Liechti F, Bruderer B (2002) Is reverse migration a common feature of nocturnal bird migration?—an analysis of radar data from Israel. Ardea 90:325–334

    Google Scholar 

  • Kruckenberg H, Borbach-Jaene J (2004) Do greylag geese (Anser anser) use traditional roosts? Site fidelity of colour-marked nordic greylag geese during spring migration. J Ornithol 145:117–122

    Article  Google Scholar 

  • Kuenzi AJ, Moore FR, Simons TR (1991) Stopover of Neotropical landbird migrants on East Ship Island following trans-gulf migration. Condor 93:869–883

    Article  Google Scholar 

  • Labocha MK, Hayes JP (2012) Morphometric indices of body condition in birds: a review. J Ornithol 153:1–22

    Article  Google Scholar 

  • Larkin RP, Szafoni RE (2008) Evidence for widely dispersed birds migrating together at night. Integrative Comp Biol 48:40–49

  • Leyrer J, Pruiksma S, Piersma T (2009) On 4 June 2008 Siberian Red Knots at Elbe mouth kissed the canonical evening migration departure rule goodbye. Ardea 97:71–79

    Article  Google Scholar 

  • Liechti F (1993) Nächtlicher Vogelzug im Herbst über Süddeutschland: Winddrift und Kompensation. J Ornithol 134:373–404

    Article  Google Scholar 

  • Liechti F (2006) Birds: blowin’ by the wind? J Ornithol 147:202–211

    Article  Google Scholar 

  • Liechti F, Bruderer B (1998) The relevance of wind for optimal migration theory. J Avian Biol 29:561–568

    Article  Google Scholar 

  • Liechti F, Schaller E (1999) The use of low-level jets by migrating birds. Naturwissenschaften 86:549–551

    Article  CAS  PubMed  Google Scholar 

  • Liechti F, Erich D, Bruderer B (1996) Flight behaviour of White Storks Ciconia ciconia on their migration over Southern Israel. Ardea 84:3–13

    Google Scholar 

  • Liechti F, Witvliet W, Weber R, Bächler E (2013) First evidenve of a 200-day non-stop flight in a bird. Nat Comm 4:2554

  • Lindström à (1991) Maximum fat deposition rates in migrating birds. Ornis Scand 22:12–19

  • Lindström A, Alerstam T (1992) Optimal fat loads in migrating birds: a test of the time-minimization hypothesis. Am Nat 140:477–491

    Article  PubMed  Google Scholar 

  • Lindström Å, Hasselquist D, Bensch S, Grahn M (1990) Asymmetric contests over resources for survival and migration: a field experiment with bluethroats. Anim Behav 40:453–461

    Article  Google Scholar 

  • Lindström Å, Kvist A, Piersma T, Dekinga A, Dietz MW (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp Biol 203:913–919

    PubMed  Google Scholar 

  • Lisovski S, Gosbell K, Christie M, Hoye BJ, Klaassen M, Steward ID, Taysom AJ, Minton C (2016) Movement patterns of Sanderling (Calidris alba) along the East Asian Australasian Flyway and a comparison of methods to identify crucial areas for conservation. Emu 116:168–177

    Article  Google Scholar 

  • Lok T, Overdijk O, Piersma T (2015) The cost of migration: spoonbills suffer higher mortality during trans-Saharan spring migrations only. Biol Lett 11:20140944

    Article  PubMed Central  PubMed  Google Scholar 

  • Loria DE, Moore FR (1990) Energy demands of migration on Red-eyed Vireos, Vireo olivaceus. Behav Ecol 1:24–33

    Article  Google Scholar 

  • Lourenço PM, Kentie R, Schroeder J, Alves JA, Groen NM, Hooijmeijer JCEW, Piersma T (2010) Phenology, stopover dynamics and population size of migrating black-tailed godwits Limosa Limosa Limosa in Portuguese rice plantations. Ardea 98:35–42

    Article  Google Scholar 

  • Lyons JE, Haig SM (1995) Fat content and stopover ecology of spring migrant Semipalmated Sandpipers in South Carolina. Condor 97:427–437

    Article  Google Scholar 

  • Madsen J (2001) Spring migration strategies in pink-footed geese Anser brachyrhynchus and consequences for spring fattening and fecundity. Ardea 89:43–55

    Google Scholar 

  • Madsen J, Klaassen M (2006) Assessing body condition and energy budget components by scoring abdominal profiles in free-ranging pink-footed geese Anser brachyrhynchus. J Avian Biol 37:283–287

    Article  Google Scholar 

  • Maggini I, Bairlein F (2010a) Body condition and stopover of trans-Saharan spring migrant passerines caught at a site in southern Morocco. Ring Migr 26:31–37

    Article  Google Scholar 

  • Maggini I, Bairlein F (2010b) 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

    Article  Google Scholar 

  • Maggini I, Bairlein F (2013) Metabolic response to changes in temperature in northern wheatears from an arctic and a temperate populations. J Avian Biol 44:1–7

    Article  Google Scholar 

  • Mandel JT, Bildstein KL, Bohrer G, Winkler DW (2008) Movement ecology of migration in turkey vultures. PNAS 105:19102–19107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marsh RL (1983) Adaptations of the Gray Catbird Dumetella carolinensis to long distance migration: energy stores and substrate concentrations in plasma. Auk 100:170–179

    Google Scholar 

  • Masman D, Klaassen M (1987) Energy expenditure during free flight in trained and free-living Eurasian Kestrels Falco tinnunculus. Auk 104:603–616

    Google Scholar 

  • McLaren J, Shamoun-Baranes J, Bouten W (2013) Stop early to travel fast—modelling risk-averse scheduling among nocturnally migrating birds. J Theor Biol 316:90–98

    Article  PubMed  Google Scholar 

  • McWilliams SR, Guglielmo CG, P. P, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393

    Article  Google Scholar 

  • Meissner W (1998) Fat reserves in Dunlins Clidris alpina during autumn migration. Ornis Svecica 8:91–102

  • Michaeli G, Pinshow B (2001) Respiratory water loss in free-flying pigeons. J Exp Biol 204:3803–3814

    CAS  PubMed  Google Scholar 

  • Miller MR, Takekawa JY, Fleskes JP, Orthmeyer DL, Casazza ML, Perry WM (2005) Spring migration of Northern Pintails from California’s Central Valley wintering area tracked with satellite telemetry: routes, timing, and destinations. Can J Zool 83:1314–1332

    Article  Google Scholar 

  • Mills AM, Thurber BG, Mackenzie SA, Taylor PD (2011) Passerines use nocturnal flights for landscape-scale movements during migration stopover. Condor 113:597–607

    Article  Google Scholar 

  • Mitchell GW, Woodworth BK, Taylor PD, Norris DR (2015) Automated telemetry reveals age specific differences in flight duration and speed are driven by wind conditions in a migratory songbird. Mov Ecol 3:19

  • Moore FR, Aborn DA (2000) Mechanisms of en route habitat selection: how do migrants make habitat decisions during stopover. Stud Avian Biol 20:34–42

  • Moore F, Kerlinger P (1987a) Stopover and fat deposition by North American wood-warblers (Parulinae) following spring migration over the Gulf of Mexico. Oecologia 74:47–54

    Article  CAS  PubMed  Google Scholar 

  • Moore FR, Kerlinger P (1987b) Stopover and fat deposition by North American wood-warblers (Parulidae) following spring migration over the Gulf of Mexico. Oecologia 74:47–54

    Article  CAS  PubMed  Google Scholar 

  • Moore FR, Yong W (1991) Evidence of food-based competition among passerine migrants during stopover. Behav Ecol Sociobiol 28:83–90

    Article  Google Scholar 

  • Moore FR, Kerlinger P, Simons TR (1990) Stopover on a gulf coast barrier island by spring trans-gulf migrants. Wilson. J Ornithol 102:487–500

    Google Scholar 

  • Moore FR, Mabey S, Woodrey M (2003) Priority access to food in migratory birds: age, sex and motivational asymmetries. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian Migration. Springer, Berlin Heidelberg New York, pp 281–292

    Chapter  Google Scholar 

  • Moreau RE (1972) The Palaearctic-African Bird Migration Systems. Academic Press, London and New York

    Google Scholar 

  • Moriguchi S, Amano T, Ushiyama K, Fujita G, Higuchi H (2006) The relationship between abdominal profile index and body condition of greater white-fronted geese Anser albifrons. Ornithol Sci 5:193–198

  • Morris SR (1996) Mass loss and probability of stopover by migrant warblers during spring and fall migration. J Field Ornithol 67:456–462

    Google Scholar 

  • Morris SR, Holmes DW, Richmond ME (1996) A ten-year study of the stopover patterns of migratory passerines during fall migration on Appledore island, Maine. Auk 113:395–409

    Google Scholar 

  • Müller F, Taylor PD, Sjöberg S, Muheim R, Tsvey A, Schmaljohann H (2016) Towards a conceptual framework for explaining variation in the nocturnal departure time of songbird migrants. Mov Ecol 4:24

  • Navedo JG, Masero JA, Overdijk O, Orizaola G, Sánchez-Guzmán JM (2010) Assessing the role of multiple environmental factors on Eurasian Spoonbill departure decisions from stopover sites. Ardea 98:3–12

    Article  Google Scholar 

  • Newton SF (1993) Body condition of a small passerine bird: ultrasonic assessment and significance in overwinter survival. J Zool 229:561–580

    Article  Google Scholar 

  • Newton I (2008) The migration ecology of birds. Academic Press, London

    Google Scholar 

  • Nilsson C, Sjöberg S (2016) Causes and characteristics of reverse bird migration: an analysis based on radar, radio tracking and ringing at Falsterbo, Sweden. J Avian Biol 47:354–362

    Article  Google Scholar 

  • Nilsson C, Klaassen RHG, Alerstam T (2013) Differences in speed and duration of bird migration between spring and autumn. Am Nat 181:837–845

    Article  PubMed  Google Scholar 

  • Norberg UM (1995) How a long tail and changes in mass and wing shape affect the cost for flight in animals. Func Ecol 9:48–54

  • Norberg U (1996) Energetics of flight. Avian energetics and nutritional ecology. Chapman and Hall, New York

    Google Scholar 

  • Ormerod SJ (1990) Time of passage, habitat use and mass change of Acrocephalus warblers in a South Wales reedswamp. Ring Migr 11:1–11

    Article  Google Scholar 

  • Ottosson U, Bairlein F, Hall P, Hjort C, Rumsey SJR, Spina F, Waldenström J (2001) Timing of migration and spring mass of some Palaearctic migrants at Lake Chad. Ostrich S15:60

  • Ottosson U, Bairlein F, Hjort C (2002) Migration patterns of Palaearctic Acrocephalus and Sylvia warblers in north-eastern Nigeria. Vogelwarte 41:249–262

  • Ottosson U, Waldenström J, Hjort C, McGregor R (2005) Garden Warbler Sylvia borin migration in sub-Saharan West Africa: phenology an body mass changes. Ibis 147:750–757

    Article  Google Scholar 

  • Ouwehand J, Both C (2016) Alternate non-stop migration strategies of pied flycatchers to cross the Sahara desert. Biol Lett 12:20151060

    Article  PubMed Central  PubMed  Google Scholar 

  • Ouwehand J, Both C (2017) African departure rather than migration speed determines variation in spring arrival in pied flycatchers. J Anim Ecol 86:88–97

    Article  PubMed  Google Scholar 

  • Owen M (1981) Abdominal profile—a condition index for wild geese in the field. J Wildlife Manage 45:227–230

    Article  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Pennycuick CJ (1975) Mechanics of flight. In: Farner DS (ed) Avian Biology. 5 edn. Academic Press, New York, pp 1–75

    Google Scholar 

  • Pennycuick CJ, Einarsson O, Bradbury TAM, Owen M (1996) Migrating Whooper Swans Cygnus cygnus: satellite tracks and fligth performance calculations. J Avian Biol 27:118–134

    Article  Google Scholar 

  • Piersma T, Klaasen K, Bruggemann HJ, Blomert A, Gueye A, Ntiamoa-Baidu Y, Van Brederode NE (1990a) Seasonal timing of the spring departure of waders from the Banc d’Arguin, Mauritania. Ardea 78:123–133

    Google Scholar 

  • Piersma T, Zwarts L, Bruggemann JH (1990b) Behavioural aspects of the departure of waders before long-distance flights: flocking, vocalizations, flight paths and diurnal timing. Ardea 78:157–184

    Google Scholar 

  • Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 71:405–415

    Article  Google Scholar 

  • Piersma T, Rogers DI, Gonzáles PM, Zwarts L, Niles LJ, de Lima I, do Nascimento S, Minton CDT, Baker AJ (2005) Fuel storage rates before northward flights in red knots worldwide. Facing the severest ecological constraints in tropical intertidal environments. In: Greenberg R, Marra PP (eds) Birds of two Worlds. Johns Hopkins University Press, Baltimore, pp 262–273

    Google Scholar 

  • Pilastro A, Spina F (1997) Ecological and morphological correlates of residuel fat reserves in passerine migrants at their spring arrival in southern Europe. J Avian Biol 28:309–318

    Article  Google Scholar 

  • Prop J, Black JM, Shimmings P (2003) Travel schedules to the high arctic: barnacle geese trade-off the timing of migration with accumulation of fat deposits. Oikos 103:403–414

    Article  Google Scholar 

  • Rabøl J, Peterson FD (1973) Lengths of resting time in various night-migrating passerines at Hesselo, Southern Kattegat, Denmark. Ornis Scand 22:33–46

    Article  Google Scholar 

  • Ramenofsky M, Wingfield J (2006) Behavioral and physiological conflicts in migrants: the transition between migration and breeding. J Ornithol 147:135–145

    Article  Google Scholar 

  • Rayner JMV (1999) Estimating power curves of flying vertebrates. J Exp Biol 202:3449–3461

    CAS  PubMed  Google Scholar 

  • Rayner JMV, Viscardi PW, Ward S, Speakman JR (2001) Aerodynamics and Energetics of Intermittent Flight in Birds. Am Zool 41:188–204

  • Reed ET, Cooch EG, Goudie RI, Cooke F (1998) Site fidelity of Black Brant wintering and spring staging in the Strait of Georgia, British Columbia. Condor 100:426–437

    Article  Google Scholar 

  • Richardson WJ (1978) Timing and amount of bird migration in relation to weather: a review. Oikos 30:224–272

    Article  Google Scholar 

  • Richardson WJ (1982) Northeastward reverse migration of birds over Nova Scotia, Canada, in Autumn. Behav Ecol Sociobiol 10:193–206

    Article  Google Scholar 

  • Richardson WJ (1990) Timing of bird migration in relation to weather: updated review. In: Gwinner E (ed) Bird migration. Springer, Berlin Heidelberg, pp 78–101

    Chapter  Google Scholar 

  • Rotics S, Kaatz M, Resheff YS, Turjeman SF, Zurell D, Sapir N, Eggers U, Flack A, Fiedler W, Jeltsch F, Wikelski M, Nathan R (2016) The challenges of the first migration: movement and behaviour of juvenile vs. adult white storks with insights regarding juvenile mortality. J Anim Ecol 85:938–947

    Article  PubMed  Google Scholar 

  • Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. TREE 19:257–263

    Google Scholar 

  • Safriel UN, Lavee D (1988) Weight changes of cross-desert migrants at an oasis—do energetic considerations alone determine the length of stopover? Oecologia 76:611–619

    Article  PubMed  Google Scholar 

  • Salewski V, Schaub M (2007) Stopover duration of Palearctic passerine migrants in the western Sahara—independent of fat sores? Ibis:223–236

  • Salewski V, Thoma M, Schaub M (2007) Stopover of migrating birds: simultaneous analysis of different marking methods enhances the power of capture-recapture analyses. J Ornithol 148:29–37

    Article  Google Scholar 

  • Salewski V, Kéry M, Herremans M, Liechti F, Jenni L (2009) Estimating fat and protein fuel from fat and muscle scores in passerines. Ibis 151:640–653

    Article  Google Scholar 

  • Salewski V, Schmaljohann H, Liechti F (2010) Spring passerine migrants stopping over in the Sahara are not fall-outs. J Ornithol 151:371–378

    Article  Google Scholar 

  • Sandberg R, Moore FR (1996) Migratory orientation of red-eyed vireos, Vireo olivaceus, in relation to energetic condition and ecological context. Behav Ecol Sociobiol 39:1–10

    Article  Google Scholar 

  • Sandberg R, Moore FR, Bäckman J, Lohmus M (2002) Orientation of nocturnally migrating Swainson’s Trush at dawn and dusk: Importance of energetic conditon and geomagnetic cues. Auk 119:201–219

    Article  Google Scholar 

  • Sapir N, Wikelski M, McCue MD, Pinshow B, Nathan R (2010) Flight modes in migrating European bee-eaters: heart rate may indicate low metabolic rate during soaring and gliding. PLoSONE 5:e13956

  • Sapir N, Horvitz N, Wikelski M, Avissar R, Mahrer Y, Nathan R (2011) Migration by soaring or flapping: numerical atmospheric simulations reveal that turbulence kinetic energy dictates bee-eater flight mode. Proc R Soc Lond B 278:3380–3386

    Article  Google Scholar 

  • Schaub M, Jenni L (2001) Variation of fuelling rates among sites, days and individuals in migrating passerine birds. Func Ecol 15:584–594

  • Schaub M, Pradel R, Jenni L, Lebreton J-D (2001) Migrating birds stop over longer than usually thought: an improved capture-recapture analysis. Ecology 82:852–859

    Google Scholar 

  • Schaub M, Liechti F, Jenni L (2004) Departure of migrating European robins, Erithacus rubecula, from a stopover site in relation to wind and rain. Anim Behav 67:229–237

    Article  Google Scholar 

  • Schaub M, Jenni L, Bairlein F (2008) Fuel stores, fuel accumulation, and the decision to depart from a migration stopover site. Behav Ecol 19:657–666

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schmaljohann H, Liechti F (2009) Adjustments of wingbeat frequency and airspeed to air density in free flying migratory birds. J Exp Biol 212:3633–3642

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Schmaljohann H, Liechti F, Bruderer B (2007a) Daytime passerine migrants over the Sahara—are these diurnal migrants or prolonged flights of nocturnal migrants? Paper presented at the Ostrich, Proc. Pan African Ornithol. Congress, Djerba, 2007

  • Schmaljohann H, Liechti F, Bruderer B (2007b) Songbird migration across the Sahara—the non-stop hypothesis rejected! Proc R Soc Lond B 274:735–739

    Article  Google Scholar 

  • Schmaljohann H, Bruderer B, Liechti F (2008) Sustained bird flights occur at temperatures beyond expected limits of water loss rates. Anim Behav 76:1133–1138

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schmaljohann H, Fox JW, Bairlein F (2012) Phenotypic response to environmental cues, orientation and migration costs in songbirds flying halfway around the world. Anim Behav 84:623–640

    Article  Google Scholar 

  • Schmaljohann H, Korner-Nievergelt F, Naef-Daenzer B, Nagel R, Maggini I, Bulte M, Bairlein F (2013) Stopover optimization in a long-distance migrant: the role of fuel load and nocturnal take-off time in Alaskan northern wheatears (Oenanthe oenanthe). Front Zool 10:26

  • Schmaljohann H, Meier C, Arlt D, Bairlein F, van Oosten H, Morbey YE, Åkesson S, Buchmann M, Chernetsov N, Desaever R, Elliott J, Hellström M, Liechti F, López A, Middleton J, Ottosson U, Pärt T, Spina F, Eikenaar C (2016) Proximate causes of avian protandry differ between subspecies with contrasting migration challenges. Behav Ecol 27:321–331

    Article  Google Scholar 

  • Schmaljohann H, Lisovski S, Bairlein F (2017) Flexible reaction norms to environmental variables along the migration route and the significance of stopover duration for total speed of migration in a songbird migrant. Front Zool 14:17

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: valildating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Schwilch R, Piersma T, Holmgren NMA, Jenni L (2002) Do migratory birds need a nap after a long non-stop flight? Ardea 90:149–154

    Google Scholar 

  • Sears J (1988) Assessment of body condition in live birds; measurements of protein and fat reserves in the mute swan, Cygnus olor. J Zool 216:295–308

    Article  Google Scholar 

  • Seber GAF (1965) A note on the multiple-recapture census. Biometrika 52:249–259

    Article  CAS  PubMed  Google Scholar 

  • Shaffer SA, Tremblay Y, Weimerskirch H, Scott D, Thompson DR, Sagar PM, Moller H, Taylor GA, Foley DG, Block BA, Costa DP (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. PNAS 103:12799–12802

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shamoun-Baranes J, Leyrer J, van Loon E, Bocher P, Robin F, Meunier F, Piersma T (2010) Stochastic atmospheric assistance and the use of emergency staging sites by migrants. Proc R Soc Lond B 277:1505–1511

    Article  Google Scholar 

  • Shariatinajafabadi M, Wang T, Skidmore AK, Toxopeus AG, Kölzsch A, Nolet BA, Exo K-M, Griffin L, Stahl J, Cabot D (2013) Migratory herbivorous waterfowl track satellite-derived green wave index. PLoSONE 9:e108331

  • Sjöberg S, Alerstam T, Åkesson S, Schulz A, Weidauer A, Coppack T, Muheim R (2015) Weather and fuel reserves determine departure and flight decisions in passerines migrating across the Baltic Sea. Anim Behav 104:59–68

    Article  Google Scholar 

  • Skagen SK, Knopf FL (1994) Residency pattern of migrating Sandpipers at a midcontinental stopover. Condor 96:949–958

    Article  Google Scholar 

  • Skrip MM, Bauchinger U, Goymann W, Fusani L, Cardinale M, Alan RR, McWilliams SR (2015) Migrating songbirds on stopover prepare for, and recover from, oxidative challenges posed by long-distance flight. Ecol Evol 5:3198–3209

    Article  PubMed Central  PubMed  Google Scholar 

  • Smith VW (1966) Autumn and spring weights of some palearctic migrants in Central Nigeria. Ibis 108:492–512

    Article  Google Scholar 

  • Smith AD, McWilliams SR (2014) What to do when stopping over: behavioral decisions of a migrating songbird during stopover are dictated by initial change in their body condition and mediated by key environmental conditions. Behav Ecol 25:1423–1435

    Article  Google Scholar 

  • Smith RJ, Moore FR, May CA, Lank DB (2007) Stopover habitat along the shoreline of northern Lake Huron, Michigan: emergent aquatic insects as a food resource for spring migrating landbirds. Auk 124:107–121

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Spaar R, Bruderer B (1996) Soaring migration of Steppe Eagles Aquila nipalensis in southern Israel: Flight behaviour under various wind and thermal conditions. J Avian Biol 27:289–301

    Article  Google Scholar 

  • Spaar R, Bruderer B (1997a) Migration by flapping or soaring: Flight strategies of Marsh, Montagu’s and Pallid Harriers in southern Israel. Condor 99:458–469

    Article  Google Scholar 

  • Spaar R, Bruderer B (1997b) Optimal flight behaviour of soaring migrants? A case study of migrating Steppe Buzzards Buteo buteo vulpinus. Behav Ecol 8:288–297

    Article  Google Scholar 

  • Spina F, Pilastro A (1999) Strategy of sea and desert crossing in spring passerine migrants as suggested by the analysis of intra- and inter-specific variation of residual fat levels. Proceedings of the 22 International Ornithological Congress, Durban. BirdLife South Africa, Johannesburg

  • Stach R, Fransson T, Jakobsson S, Kullberg C (2015) Wide ranging stopover movements and substantial fuelling in first year garden warblers at a northern stopover site. J Avian Biol 46:315–322

    Article  Google Scholar 

  • Stanley CQ, MacPherson M, Fraser KC, McKinnon EA, Stutchbury BJM (2012) Repeat tracking of individual songbirds reveals consistent migration timing but flexibility in route. PLoSONE 7:e40688

  • Taylor PD, Mackenzie SA, Thurber BG, Calvert AM, Mills AM, McGuire LP, Guglielmo CG (2011) Landscape movements of migratory birds and bats reveal an expanded scale of stopover. PLoSONE 6:e27054

  • Tøttrup AP, Klaassen RHG, Strandberg R, Thorup K, Willemoes Kristensen M, Søgaard Jørgensen P, Fox JW, 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 Lond B 279:1008–1016

    Article  Google Scholar 

  • Trierweiler C, Klaassen RHG, Drent R, Exo K-M, Komdeur J, Bairlein F, Koks BJ (2014) Migratory connectivity and population-specific migration routes in a long-distance migratory bird. Proc R Soc Lond B 281:20132897

    Article  Google Scholar 

  • Tsvey A, Bulyuk VN, Kosarev V (2007) Influence of body condition and weather on departures of first-year European robins, Erithacus rubecula, from an autumn migratory stopover site. Behav Ecol Sociobiol 61:1665–1674

    Article  Google Scholar 

  • Van Wilgenburg SL, Hobson KA (2011) Combining stable-isotope (δD) and band recovery data to improve probabilistic assignment of migratory birds to origin. Ecol Appl 21:1340–1351

    Article  PubMed  Google Scholar 

  • van Gils JA, Beekman JH, Coehoorn P, Corporaal E, Dekkers T, Klaassen M, Van Kraaij R, De Leeuw R, De Vries PP (2008) Longer guts and higher food quality increases energy intake in migratory swans. J Anim Ecol 77:1234–1241

    Article  PubMed  Google Scholar 

  • van Wijk RE, Kölzsch A, Kruckenberg H, Ebbinge BS, Müskens GJDM, Nolet BA (2012) Individually tracked geese follow peaks of temperature acceleration during spring migration. Oikos 121:655–664

    Article  Google Scholar 

  • Visser ME, Perdeck AC, van Balen JH, Both C (2009) Climate change leads to decreasing bird migration distances. Glob Change Biol 15:1859–1865

  • Ward P (1969) The annual cycle of the Yellow-vented bulbul Pycnonotus goiavier in a humid equatorial environment. J Zool 157:25–45

    Article  Google Scholar 

  • Ward S, Rayner JMV, Möller U, Jackson DM, Nachtigall W, Speakman JR (1999) Heat transfer from starlings Sturnus vulgaris during flight. J Exp Biol 202:1589–1602

    PubMed  Google Scholar 

  • Ward S, Bishop CM, Woakes AJ, Butler PJ (2002) Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and bar-headed geese (Anser indicus). J Exp Biol 205:3347–3356

    CAS  PubMed  Google Scholar 

  • Weber TP, Hedenström A (2000) Optimal stopover decisions under wind influence: the effects of correlated winds. J Theor Biol 205:95–104

    Article  CAS  PubMed  Google Scholar 

  • Weimerskirch H, Wilson RP (2000) Oceanic respite for wandering albatrosses. Nature 406:955–956

    Article  CAS  PubMed  Google Scholar 

  • Wiersma P, Piersma T (1995) Scoring abdominal profiles to characterize migratory cohorts of shorebirds—an example with red knots. J Field Ornithol 66:88–98

    Google Scholar 

  • Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Costs of migration in free-flying songbirds. Nature 423:704

    Article  CAS  PubMed  Google Scholar 

  • Woodrey MS, Moore FR (1997) Age-related differences in the stopover of fall landbird migrants on the coast of Alabama. Auk 114:695–707

    Article  Google Scholar 

  • Woodworth BK, Francis CM, Taylor PD (2014) Inland flights of young red-eyed vireos Vireo olivaceus in relation to survival and habitat in a coastal stopover landscape. J Avian Biol 45:387–395

    Article  Google Scholar 

  • Woodworth BK, Mitchell GW, Norris DR, Francis CM, Taylor PD (2015) Patterns and correlates of songbird movements at an ecological barrier during autumn migration assessed using landscap- and regional-scale automated radiotelemetry. Ibis 157:326–339

    Article  Google Scholar 

  • Yamaura Y, Schmaljohann H, Lisovski S, Senzaki M, Kawamura K, Fujimaki Y, Nakamura F (2016) Tracking the Stejneger’s stonechat Saxicola stejnegeri along the East Asian–Australian Flyway from Japan via China to Southeast Asia. J Avian Biol 48:197–202

    Article  Google Scholar 

  • Yohannes E, Biebach H, Nikolaus G, Pearson DJ (2008) Passerine migration strategies and body mass variation along geographic sectors across East Africa, the Middle East and the Arabian Peninsula. J Ornithol 150:369–381

    Article  Google Scholar 

  • Yong W, Moore FR (1997) Spring stopover of intercontinental migratory thrushes along the northern coast of the Gulf of Mexico. Auk 114:263–278

    Article  Google Scholar 

  • Yong W, Finch DM, Moore FR, Kelly JF (1998) Stopover ecology and habitat use of migratory Wilson’s warblers. Auk 115:829–842

    Article  Google Scholar 

  • Zehnder S, Åkesson S, Liechti F, Bruderer B (2002) Observation of free-flying nocturnal migrants at Falsterbo: occurrence of reverse flight directions in autumn. Avian Sci 2:103–113

  • Zuur AE, Irwin DE, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Meth Ecol Evol 1:3–14

    Article  Google Scholar 

  • Zwarts L, Ens BJ, Kersten M, Piersma T (1990) Moult, mass and flight range of waders ready to take off for long-distance migrations. Ardea 78:339–364

    Google Scholar 

Download references

Acknowledgements

This work was supported by a Deutsche Forschungsgemeinschaft (DFG) Grant awarded to HS (SCHM 2647/2-1). We thank one reviewer for very helpful comments.

Author information

Authors and Affiliations

  1. Institute of Avian Research “Vogelwarte Helgoland”, An der Vogelwarte 21, 26386, Wilhelmshaven, Germany

    Heiko Schmaljohann & Cas Eikenaar

Authors
  1. Heiko Schmaljohann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cas Eikenaar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heiko Schmaljohann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schmaljohann, H., Eikenaar, C. How do energy stores and changes in these affect departure decisions by migratory birds? A critical view on stopover ecology studies and some future perspectives. J Comp Physiol A 203, 411–429 (2017). https://doi.org/10.1007/s00359-017-1166-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-017-1166-8

Keywords

Search

Navigation