Abstract
Annual cycle events may be interlinked, influence following annual cycle stages, and may alter performance of individuals. Such links, called carry-over effects, can explain individual variation in timing or reproductive success in migratory species. Identifying the key links affecting fitness may reveal the mechanisms of species population dynamics but the current evidence for the strongest carry-over effects is equivocal. Here, we aim to assess the carry-over effects in great reed warblers Acrocephalus arundinaceus, a long-distance migratory songbird, using 103 full-annual tracks from three European and two Asian breeding populations. Our results showed strong positive relationships within autumn and spring migration periods and buffering capacity of the non-breeding period preventing events to carry over between these periods. Moreover, we found no profound relation between the non-breeding habitat quality or seasonality (quantified using stable isotopes and remote sensing data) and the timing of spring migration. The strongest carry-over effects occurred in individuals from the southern European breeding population compared to the northern and the central European populations. A moderate relationship between the habitat seasonality during moult and the spring migration timing indicates the importance of the complete moult. The overall weak carry-over effects of non-breeding habitat conditions found in this study contrast with previous results and imply between-species differences in these crucial relationships. Moreover, the population-specific carry-over effects highlight the importance of multi-population approach and advise caution in interpretation of results from single-population studies. Finally, the carry-over effect from the moulting period indicates the significance of a so-far neglected link in the species.
Significance statement
Environmental conditions vary in space and time. Therefore, migratory species adjust the timing of migration in order to maximise their fitness. However, the links between annual cycle events in multiple populations and the consequences of environmental conditions outside the breeding range are scarcely known. In this study, we used tracking data of the great reed warbler, an insectivorous bird species breeding across western Eurasia and wintering in Africa, to study a complex system of links between annual events. We found that the strength of these links differed between geographically distinct populations but not between sexes. Moreover, harsh environmental conditions during moult delayed the timing of subsequent events. Our findings could help explain large-scale differences in population size changes observed in some species and highlight the importance of energetically demanding moult period for the life of migratory species. Finally, our results demonstrate the need for multi-population approach in studies on seasonal interactions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The dataset used in this study is available at https://doi.org/10.5281/zenodo.4088174 (Brlík et al. 2020b).
References
Barclay D, Thompson R, Higgins C (1995) The partial least squares (PLS). Approach to causal modeling: personal computer adoption and use as an illustration. Technol Stud 2:285–309
Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bearhop S, Hilton GM, Votier SC, Waldron S (2004) Stable isotope ratios indicate that body condition in migrating passerines is influenced by winter habitat. Proc R Soc Lond B 271:S215–S218. https://doi.org/10.1098/rsbl.2003.0129
Becquaert M (1952) Quelque curiosités ornithologiques belgo-congolaises: les rousse-rolles. Zooleo 16:331–340
Bensch S, Hasselquist D, Hedenström A, Ottosson U (1991) Rapid moult among Palearctic passerines in West Africa - an adaptation to the oncoming dry season. Ibis 133:47–52. https://doi.org/10.1111/j.1474-919X.1991.tb04809.x
BirdLife International, NatureServe (2014) Bird species distribution maps of the world. BirdLife International, http://datazone.birdlife.org/species/factsheet/great-reed-warbler-acrocephalus-arundinaceus. Accessed 10 Apr 2020
Briedis M, Bauer S (2018) Migratory connectivity in the context of differential migration. Biol Lett 14:20180679. https://doi.org/10.1098/rsbl.2018.0679
Briedis M, Hahn S, Adamík P (2017) Cold spell en route delays spring arrival and decreases apparent survival in a long-distance migratory songbird. BMC Ecol 17:11. https://doi.org/10.1186/s12898-017-0121-4
Briedis M, Krist M, Král M, Voigt CC, Adamík P (2018) Linking events throughout the annual cycle in a migratory bird - wintering period buffers accumulation of carry-over effects. Behav Ecol Sociobiol 72:93. https://doi.org/10.1007/s00265-018-2509-3
Briedis M, Bauer S, Adamík P, Alves JA, Costa JS, Emmenegger T, Gustafsson L, Koleček J, Liechti F, Meier CM, Procházka P, Hahn S (2019) A full annual perspective on sex-biased migration timing in long-distance migratory birds. Proc R Soc B 286:20182821. https://doi.org/10.1098/rspb.2018.2821
Brlík V, Koleček J, Burgess M et al (2020a) Weak effects of geolocators on small birds: a meta-analysis controlled for phylogeny and publication bias. J Anim Ecol 89:207–220. https://doi.org/10.1111/1365-2656.12962
Brlík V, Malmiga G, Dimitrov D et al (2020b) Population-specific assessment of carry-over effects across the range of a migratory songbird. Zenodo. https://doi.org/10.5281/zenodo.4088174
Buttemer WA, Bauer S, Emmenegger T, Dimitrov D, Peev S, Hahn S (2019) Moult-related reduction of aerobic scope in passerine birds. J Comp Physiol B 189:463–470. https://doi.org/10.1007/s00360-019-01213-z
Catry P, Campos A, Almada V, Cresswell W (2004) Winter segregation of migrant European robins Erithacus rubecula in relation to sex, age and size. J Avian Biol 35:204–209. https://doi.org/10.1111/j.0908-8857.2004.03266.x
Cohen J (1977) Statistical power analysis for the behavioral sciences. Academic Press, London
Cohen J (1992) A power primer. Psychol Bull 112:155–159. https://doi.org/10.1037//0033-2909.112.1.155
Collatz GJ, Berry A, Clark JS (1998) Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past, and future. Oecologia 114:441–454. https://doi.org/10.1007/s004420050468
Conklin JR, Battley PF, Potter MA, Fox JW (2010) Breeding latitude drives individual schedules in a trans-hemispheric migrant bird. Nat Commun 1:67. https://doi.org/10.1038/ncomms1072
Copete JL, Bigas D, Mariné R, Martínez-Vilalta A (1998) Frequency of complete moult in adult and juvenile great reed warblers (Acrocephalus arundinaceus) in Spain. J Ornithol 139:421–424. https://doi.org/10.1007/BF01653469
Cramp JS (ed) (1992) Birds of the Western Palearctic. Oxford University Press, Oxford
De Roo A, Deheegher J (1969) Ecology of the great reed-warbler, Acrocephalus arundinaceus (L.), wintering in the southern Congo savanna. Gefault 59:260–273
Deveson E (2013) Satellite normalized difference vegetation index data used in managing Australian plague locusts. J Appl Remote Sens 7:075096. https://doi.org/10.1117/1.JRS.7.075096
Dijkstra TK, Henseler J (2015) Consistent partial least squares path modeling. MIS Quart 39:297–316. https://doi.org/10.25300/MISQ/2015/39.2.02
Drake A, Rock C, Quinlan SP, Green DJ (2013) Carry-over effects of winter habitat vary with age and sex in yellow warblers Setophaga petechia. J Avian Biol 44:321–330. https://doi.org/10.1111/j.1600-048X.2013.05828.x
Drake A, Martin M, Green DJ (2014) Winter habitat use does not influence spring arrival dates or the reproductive success of yellow warblers breeding in the arctic. Polar Biol 37:181–191. https://doi.org/10.1007/s00300-013-1421-6
Dyrcz A (1995) Biology and ecology of different Asiatic populations of the great reed Acrocephalus arundinaceus. Jpn J Ornithol 44:123–142
Fudickar AM, Wikelski M, Partecke J (2012) Tracking migratory songbirds: accuracy of light-level loggers (geolocators) in forest habitats. Methods Ecol Evol 3:47–52. https://doi.org/10.1111/j.2041-210X.2011.00136.x
Goodenough AE, Coker DG, Wood MJ, Rogers SL (2017) Overwintering habitat links to summer reproductive success: intercontinental carry-over effects in a declining migratory bird revealed using stable isotope analysis. Bird Study 64:433–444. https://doi.org/10.1080/00063657.2017.1408566
Gow EA, Burke L, Winkler DW, Knight SM, Bradley DW, Clark RG, Bélisle M, Berzins LL, Blake T, Bridge ES, Dawson RD, Dunn PO, Garant D, Holroyd G, Horn AG, Hussell DJT, Lansdorp O, Laughlin AJ, Leonard ML, Pelletier F, Shutler D, Siefferman L, Taylor CM, Trefry H, Vleck CM, Vleck D, Whittingham LA, Norris DR (2019) A range-wide domino effect and resetting of the annual cycle in a migratory songbird. Proc R Soc B 286:20181916. https://doi.org/10.1098/rspb.2018.1916
Gunnarsson TG, Gill JA, Newton J, Potts PM, Sutherland WJ (2005) Seasonal matching of habitat quality and fitness in a migratory bird. Proc R Soc Lond B 272:2319–2323. https://doi.org/10.1098/rspb.2005.3214
Hair JF, Hult GTM, Ringle CM, Sarstedt M (2017) A primer on partial least squares structural equation modeling (PLS-SEM). Sage, Thousand Oakes
Hanzelka J, Horká P, Reif J (2019) Spatial gradients in country - level population trends of European birds. Divers Distrib 25:1527–1536. https://doi.org/10.1111/ddi.12945
Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S (2011) Carry-over effects as drivers of fitness differences in animals. J Anim Ecol 80:4–18. https://doi.org/10.1111/j.1365-2656.2010.01740.x
Hasselquist D (1998) Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology 79:2376–2390. https://doi.org/10.1890/0012-9658(1998)079[2376:PIGRWA]2.0.CO;2
Hasselquist D, Montràs-Janer T, Tarka M, Hansson B (2017) Individual consistency of long-distance migration in a songbird: significant repeatability of autumn route, stopovers and wintering sites but not in timing of migration. J Avian Biol 48:91–102. https://doi.org/10.1111/jav.01292
Hedenström A (2008) Adaptations to migration in birds: behavioural strategies, morphology and scaling effects. Phil Trans R Soc B 363:287–299. https://doi.org/10.1098/rstb.2007.2140
Hedenström A, Bensch S, Hasselquist D, Lockwood M, Ottosson U (1985) Migration, stopover and moult of the great reed warbler Acrocephalus arundinaceus in Ghana, West Africa. Ibis 135:177–180. https://doi.org/10.1111/j.1474-919X.1993.tb02829.x
Hobson KA (2011) Isotopic ornithology: a perspective. J Ornithol 152:S49–S66. https://doi.org/10.1007/s10336-011-0653-x
Koleček J, Procházka P, El-Arabany N et al (2016) Cross-continental migratory connectivity and spatiotemporal migratory patterns in the great reed warbler. J Avian Biol 47:756–767. https://doi.org/10.1111/jav.00929
Koleček J, Hahn S, Emmenegger T, Procházka P (2018) Intra-tropical movements as a beneficial strategy for Palearctic migratory birds. R Soc Open Sci 5:171675. https://doi.org/10.1098/rsos.171675
Lassau S, Hochuli DF (2008) Testing predictions of beetle community patterns derived empirically using remote sensing. Divers Distrib 14:138–147. https://doi.org/10.1111/j.1472-4642.2007.00438.x
Lemke HW, Tarka M, Klaassen RHG, Åkesson M, Bensch S, Hasselquist D, Hansson B (2013) Annual cycle and migration strategies of a trans-Saharan migratory songbird: a geolocator study in the great reed warbler. PLoS One 8:e79209. https://doi.org/10.1371/journal.pone.0079209
Lerche-Jørgensen M, Korner-Nievergelt F, Tøttrup AP, Willemoes M, Thorup K (2018) Early returning long-distance migrant males do pay a survival cost. Ecol Evol 8:11434–11449. https://doi.org/10.1002/ece3.4569
Lindström Å, Alerstam T, Hedenström A (2019) Faster fuelling is the key to faster migration. Nat Clim Chang 9:288–289. https://doi.org/10.1038/s41558-019-0443-7
Lisovski S, Hahn S (2012) GeoLight - processing and analysing light-based geolocator data in R. Methods Ecol Evol 3:1055–1059. https://doi.org/10.1111/j.2041-210X.2012.00248.x
Lisovski S, Hewson CM, Klaassen RHG, Korner-Nievergelt F, Kristensen MW, Hahn S (2012) Geolocation by light: accuracy and precision affected by environmental factors. Methods Ecol Evol 3:603–612. https://doi.org/10.1111/j.2041-210X.2012.00185.x
López-Calderón C, Hobson KA, Marzal A, Balbontín J, Reviriego M, Magallanes S, García-Longoria L, de Lope F, Møller AP (2017) Environmental conditions during winter predict age- and sex-specific differences in reproductive success of a trans-Saharan migratory bird. Sci Rep 7:18082. https://doi.org/10.1038/s41598-017-18497-2
Marra PP, Holmes RT (2001) Consequences of dominance-mediated habitat segregation in American Redstart during the nonbreeding season. Auk 118:92–104. https://doi.org/10.1642/0004-8038(2001)118[0092:CODMHS]2.0.CO;2
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. https://doi.org/10.1126/science.282.5395.1884
Martin PR, Kenyon HL, Hayes L (2020) Size-dependent costs of migration: migrant bird species are subordinate to residents, but only at small body sizes. J Evol Biol 33:495–504. https://doi.org/10.1111/jeb.13583
Murphy ME (1996) Energetics and nutrition of molt. In: Carey C (ed) Avian energetics and nutritional ecology. Springer, New York, pp 158–198
Newton I (1998) Population limitation in birds. Academic Press, London
Norris DR, Taylor CM (2006) Predicting the consequences of carry-over effects for migratory populations. Biol Lett 2:148–151. https://doi.org/10.1098/rsbl.2005.0397
Norris DR, Marra PP, Kyser TK, Sherry TW, Ratcliffe LM (2004) Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc R Soc Lond B 271:59–64. https://doi.org/10.1098/rspb.2003.2569
Pearson DJ (1975) The timing of complete moult in the great reed warbler Acrocephalus arundinaceus. Ibis 117:506–509. https://doi.org/10.1111/j.1474-919X.1975.tb04244.x
Pedersen L, Fraser KC, Kyser TK, Tøttrup AP (2016) Combining direct and indirect tracking techniques to assess the impact of sub-Saharan conditions on cross-continental songbird migration. J Ornithol 157:1037–1047. https://doi.org/10.1007/s10336-016-1360-4
Pettorelli N, Vik JO, Mysterud A, Gaillard JM, Tucker CJ, Stenseth NC (2005) Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol Evol 20:503–510. https://doi.org/10.1016/j.tree.2005.05.011
Piersma T (1987) Hink, stap of sprong? Reisbeperkingen van arctische steltlopers door voedselzoeken, vetopbouw en vliegsnelheid. Limosa 60:185–194
Procházka P, Brlík V, Yohannes E, Meister B, Ilieva M, Hahn S (2018) Across a migratory divide: divergent migration directions and non-breeding grounds of Eurasian reed warblers revealed by geolocators and stable isotopes. J Avian Biol 49:e01769. https://doi.org/10.1111/jav.01769
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 10 Apr 2020
Rakhimberdiev E, Duijns S, Karagicheva J et al (2018) Fuelling conditions at staging sites can mitigate Arctic warming effects in a migratory bird. Nat Commun 9:4263. https://doi.org/10.1038/s41467-018-06673-5
Robinson RA, Baillie SR, Crick HQP (2007) Weather-dependent survival: implications of climate change for passerine population processes. Ibis 149:357–364. https://doi.org/10.1111/j.1474-919X.2006.00648.x
Rockwell SM, Bocetti CI, Marra PP (2012) Carry-over effects of winter climate on spring arrival date and reproductive success in an endangered migratory bird, Kirtland’s warbler (Setophaga kirtlandii). Auk 129:744–752. https://doi.org/10.1525/auk.2012.12003
Ruwet JC (1965) Les oiseaux des plaines et du lac-barrage de la Lufira supérieure (Katanga méridional). Reconnaissance écologique et étologique. Éditions F.U.L.R.E.A.C. Université de Liège
Sage RF, Wedin DA, Li M (1999) The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, London, pp 313–374
Saino N, Ambrosini R, Caprioli M, Romano A, Romano M, Rubolini D, Scandolara C, Liechti F (2017) Sex-dependent carry-over effects on timing of reproduction and fecundity of a migratory bird. J Anim Ecol 86:239–249. https://doi.org/10.1111/1365-2656.12625
Sanchez S, Trinchera L, Russolillo G (2017) plspm: tools for partial least squares path modeling (PLS-PM). R package version 0.4.9. https://CRAN.R-project.org/package=plspm. Accessed 10 Apr 2020
Sanderson FJ, Donald PF, Pain DJ, Burfield IJ, Bommel FPJ (2006) Long-term population declines in Afro-Palearctic migrant birds. Biol Conserv 131:93–105. https://doi.org/10.1016/j.biocon.2006.02.008
Senner NR, Hochachka WM, Fox JW, Afanasyev V (2014) An exception to the rule: carry-over effects do not accumulate in a long-distance migratory bird. PLoS One 9:e86588. https://doi.org/10.1371/journal.pone.0086588
Senner NR, Conklin JR, Piersma T (2015) An ontogenetic perspective on individual differences. Proc R Soc B 282:20151050. https://doi.org/10.1098/rspb.2015.1050
Sorensen MC, Jenni-Eiermann S, Spottiswoode CN (2015) Why do migratory birds sing on their tropical wintering grounds? Am Nat 187:E65–E76. https://doi.org/10.1086/684681
Sorensen MC, Fairhurst GD, Eiermann SJ, Newton J, Yohannes E, Spottiswoode CN (2016) Seasonal rainfall at long-term migratory staging sites is associated with altered carry-over effects in a Palearctic-African migratory bird. BMC Ecol 16:41. https://doi.org/10.1186/s12898-016-0096-6
Spina F (1990) First data on complete summer moult in the great reed warbler (Acrocephalus arundinaceus) in northern Italy. J Ornithol 131:177–178. https://doi.org/10.1007/BF01647142
Studds CE, Marra PP (2005) Nonbreeding habitat occupancy and population processes: an upgrade experiment with a migratory bird. Ecology 86:2380–2385. https://doi.org/10.1890/04-1145
Sultan B, Janicot S (2003) The West African monsoon dynamics. Part II: the “preonset” and “onset” of the summer monsoon. J Clim 16:3407–3427. https://doi.org/10.1175/1520-0442(2003)016<3407:TWAMDP>2.0.CO;2
Sweet SK, Asmus A, Rich ME, Wingfield J, Gough L, Boelman NT (2015) NDVI as a predictor of canopy arthropod biomass in the Alaskan arctic tundra. Ecol Appl 25:779–790. https://doi.org/10.1890/14-0632.1
Tarka M, Åkesson S, Hasselquist D, Hansson B (2014) Intralocus sexual conflict over wing length in a wild migratory bird. Am Nat 183:62–73. https://doi.org/10.1086/674072
Tarka M, Hansson B, Hasselquist D (2015) Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird. J Evol Biol 28:1024–1038. https://doi.org/10.1111/jeb.12638
Tipple BJ, Pagani M (2007) The early origins of terrestrial C4 photosynthesis. Annu Rev Earth Planet Sci 35:435–461. https://doi.org/10.1146/annurev.earth.35.031306.140150
van Wijk RE, Schaub M, Bauer S (2017) Dependencies in the timing of activities weaken over the annual cycle in a long-distance migratory bird. Behav Ecol Sociobiol 71:73. https://doi.org/10.1007/s00265-017-2305-5
Vickery JA, Ewing SR, Smith KW, Pain DJ, Bairlein F, Škorpilová J, Gregory RD (2014) The decline of afro-Palaearctic migrants and an assessment of potential causes. Ibis 156:1–22. https://doi.org/10.1111/ibi.12118
Wotherspoon S, Sumner M, Lisovski S (2016) TwGeos: basic data processing for light-level geolocation archival tags. R package version 0.0–1. https://github.com/slisovski/TwGeos. Accessed 10 Apr 2020
Yee TW (2019) VGAM: vector generalized linear and additive models. R package version 1.1–1. https://CRAN.R-project.org/package=VGAM. Accessed 30 Oct 2020
Acknowledgments
We thank Jaroslav Koleček, Mihaela Ilieva, Milica Požgayová, Michal Šulc, Kateřina Sosnovcová, and others for their help in the field. Martins Briedis and Jaroslav Koleček provided valuable comments on the NDVI extraction and geolocator analysis, respectively, and Milica Požgayová extracted breeding site arrival dates. We are thankful to Silke Bauer, David Hořák, Simeon Lisovski, Martin Sládeček, Wouter Vansteelant, and anonymous reviewers for critical comments on the manuscript. The study is report number 66 for Kalimok field station and report number 194 for Kvismare Bird Observatory.
Funding
The study was financially supported by the Czech Science Foundation (grant no. 20-00648S to PP), the Swedish Research Council (grant no. 621-2013-4357 and 2016-04391 to DH; 621-2014-5222 and 2016-00689 to BH), Lunds Djurskyddsfond (for the Swedish part of the project), the Linnaeus Research Excellence project Centre for Animal Movement Research (CAnMove) funded by the Swedish Research Council and Lund University (grant no. 349-2007-8690), and Kungliga Fysiografiska Sällskapet (Duncker fonden to DH).
Author information
Authors and Affiliations
Contributions
PP and VB conceived the idea of the study. VB, DD, AG, SH, BH, DH, TE, GM, SP, PP, and MW participated in retrieving geolocators and collecting feather samples. VB designed the methodology with input from SH, BH, DH, TE, GM, PP, and MW. VB and GM analysed the light-level data. EY analysed the stable isotopic composition of feather samples. BH, DH, SH, and PP acquired funding. VB gathered the remote sensing data and conducted the final analysis. VB took lead in the manuscript writing. All authors read and commented on the manuscript and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The tagging of the great reed warblers in Kvismaren/Segersjo have been approved by the Linkoping Animal Ethics Board (permit nos. 25-08, 36-11, 44-14). The fieldwork was in compliance with the current Czech Law on the Protection of Animals against Mistreatment (experimental project nos. 038/2011 and 3030/ENV/17–169/630/17) and permitted by the Bulgarian Ministry of Environment and Waters (permit nos. 427/11.11.2011, 627/30.03.2015, 672/17.03.2016). All applicable institutional and national guidelines for the care and use of animals were followed.
Additional information
Communicated by W. Wiltschko
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PDF 555 kb)
Rights and permissions
About this article
Cite this article
Brlík, V., Malmiga, G., Dimitrov, D. et al. Population-specific assessment of carry-over effects across the range of a migratory songbird. Behav Ecol Sociobiol 74, 143 (2020). https://doi.org/10.1007/s00265-020-02929-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-020-02929-7