Migratory birds are showing species-specific responses to climate change through changes in phenology, distribution and abundance. While many bird observatories collect standardised data on migratory passerines to provide invaluable information on changes in their abundances and migratory phenology, some bird observatories also undertake visual observations of passing migratory waterbirds and seabirds. In this study, we use two such long-term datasets of Great Cormorants (Phalacrocorax carbo) compiled during their spring migration. We explore the extent to which winter severity has affected their migration phenology and whether there have been long-term trends in migration timing. Observations were conducted at Lista Bird Observatory in southwest Norway (1992–2020) and at Skagen in north Jutland, Denmark (1974–98). At Skagen, there were no detectable long-term trends in Great Cormorant migratory timing. However, the median date (marking the passage of 50% of birds) was significantly advanced following warm winters. Changes in the date of passage of the first 10% of birds was close to doing so as well, but the late phase (the passage of 90% of birds) showed no relation to temperature. At Lista, winter temperatures in the southern part of the wintering area had no significant effect on the overall timing of the spring passage, but the first 10% of the Cormorants migrated significantly earlier in years with mild late March temperatures at Lista. The early phase of passage at Lista showed a significant long-term trend towards an advancement of migration, leading to an extended migration period. The findings of this study indicate that the timing of Great Cormorant spring migration does in some cases respond to late winter temperatures or show long-term trends, but that the responses and trends differ between sites and between the beginning, middle and late phases of the migration, with the early and middle phases generally showing stronger responses and trends than the late phase.

Due to anthropogenic climate change, global temperatures are rising at an accelerated rate, leading to milder winters and the earlier onset of spring (IPCC 2021). These changes have the potential to greatly affect bird populations via altered phenology, distributions and abundances (Møller et al. 2010; Knudsen et al. 2011; Lehikoinen et al. 2013; Stephens et al. 2016; Halupka et al. 2020). To obtain a better understanding of how these changes are affecting bird populations, it is necessary to conduct long-term monitoring. A multitude of studies have attempted to investigate long-term trends in the arrival dates of birds and how they are affected by warming temperatures (e.g. Newson et al. 2016). A common theme in these studies is that phenological responses in migratory birds are often species-specific (e.g. Rubolini et al. 2007; Usui et al. 2017). The spring migration phenology of birds is well studied, and many species show long-term trends towards an advancement in arrival at breeding grounds, often correlated with higher spring or winter temperatures (Sparks 1999; Butler 2003; Cotton 2003; Rubolini et al. 2007; Usui et al. 2017).

Though bird migration is extensively studied, many studies focus on the date of the first arrival of one individual to their breeding grounds, thereby potentially being representative of a more extreme migratory period performed by an atypical individual. Trends in these dates may therefore not adequately represent changes in the migration phenology of the whole population (Miller-Rushing et al. 2008; Miles et al. 2017; Lehikoinen et al. 2019). First arrival dates have also been shown to be sensitive to changes in population size and observation effort (Sparks et al. 2001; Tryjanowski & Sparks 2001; Lindén 2011), meaning increasing population size might result in advanced first arrival dates even though the mean or median arrival dates remain unchanged. To obtain a better overall picture of changes in the migration phenology of a given population, long-term, systematic observations over the whole migration period and across multiple individuals are needed (Miles et al. 2017; Lehikoinen et al. 2019).

Although whole migration data series are relatively uncommon, systematic observations of migratory birds have been conducted over many years at some sites around the world, particularly in Europe and North America (e.g. Hüppop & Hüppop 2003; Marra et al. 2005; Miller-Rushing et al. 2008; Miles et al. 2017; Lehikoinen et al. 2019). These studies have illustrated that the early, middle and late phases of migration can have different, or even contrasting, long-term trends and differential responses to temperatures (Vähätalo et al. 2004; Miller-Rushing et al. 2008; Miles et al. 2017; Lehikoinen et al. 2019). For instance, when earlier phases of spring migration have advanced with time and show stronger responses to warm temperatures than later phases, birds will experience an extended migration period (Vähätalo et al. 2004; Miles et al. 2017; Lehikoinen et al. 2019).

For birds, the timing of migration and breeding can have profound fitness and reproductive consequences, with earlier arrival and breeding usually being associated with elevated reproductive success (Verhulst et al. 1995; Smith & Moore 2005; Sergio et al. 2007). One hypothesis for why early phases of spring migration often respond more strongly to warm temperatures than late phases, is that early migrating individuals (most likely breeding adults in good condition) experience different selection pressures than late migrating individuals (likely immature or other non-breeding individuals) (Vähätalo et al. 2004; Rainio et al. 2006; Lehikoinen et al. 2019).

Many studies using bird observatory migration data focus on passerines captured for ringing (e.g. Hüppop & Hüppop 2003; Marra et al. 2005; Miller-Rushing et al. 2008) but some are also based on visual observations of larger-bodied migratory species such as seabirds and waterbirds (e.g. Vähätalo et al. 2004). For example, Lista Bird Observatory, on the southwestern coast of Norway is a bird observatory that conducts long-term, systematic observations of migratory seabirds and waterbirds. Systematic observations of migrating and staging birds, as well as standardised trapping and ringing of passerines, have been conducted at Lista in both spring and autumn since 1990 (López et al. 2020). One of the species included in these observations is the Great Cormorant Phalacrocorax carbo (hereafter ‘Cormorant’), a large migratory seabird and waterbird. Migration timing is important for Cormorants; their reproductive success decreases with later arrival at the breeding colony in spring, with strong selection for earlier arrival following warm winters and springs (Gienapp & Bregnballe 2012). Similarly, male Cormorants wintering closer to their breeding colonies have been found to arrive earlier and have higher lifetime reproductive success than males wintering further away (Bregnballe et al. 2006). By contrast, early arrival is likely less important for non-breeding immatures and first-year Cormorants, which tend to start their spring migration several weeks later than the adults (Bregnballe et al. 1997).

Although earlier arrival and shorter migration distances can lead to increased reproductive success in Cormorants, it can also have a cost. For example, Cormorants are vulnerable to low winter temperatures, and experience increased mortality during cold winters (Frederiksen & Bregnballe 2000; Herrmann et al. 2021), likely due to higher energetic requirements and the freezing of inland and coastal waters leading to reduced food accessibility (Herrmann et al. 2021). Due to their unique feather structure, Cormorants have a partly wettable plumage, which helps them in counteracting buoyancy when diving for fish, but which also substantially increases their energetic expenditure when diving in cold water (Grémillet & Wilson 1999; Grémillet et al. 2001; Grémillet et al. 2005).

We were interested to investigate a) whether large migratory seabirds like Cormorants, breeding along the Norwegian coast, showed a long-term trend towards earlier migration in spring, and b) to what extent preceding winter severity affected interannual variation in migratory timing. To do this, we used two long- term count datasets of spring migrating Cormorants: one from Lista Bird Observatory (during 1992–2020) and the other from Skagen, the northernmost tip of Denmark, (data from most years during 1974–98). We assume that the birds passing Skagen in spring will largely be the same individuals passing Lista in southwest Norway later the season.

We hypothesise that the timing of Cormorant spring migration will be affected by winter severity because high energetic expenditure during cold winters will constrain Cormorants from achieving sufficient body condition for migration and breeding, thus delaying their departure from winter quarters and spring staging sites. More specifically, we predict that early migrating Cormorants delay their migration following cold winters, whereas Cormorants migrating later in spring will be less affected. Furthermore, because of increasingly milder winters and the earlier onset of spring, we hypothesise that the early migrating Cormorants will show a long-term trend towards an advanced spring migration, whereas Cormorants migrating later in spring will not.

We extend thanks to the many observers who helped monitoring the migration of birds over the sea at Lista Bird Observatory. Many thanks to Palle A.F. Rasmussen who collated the data on Cormorant migration at Skagen. We also thank the County Governor of Agder, the Norwegian Environment Agency and Natur og Fritid AS for financial support for the monitoring at Lista Bird Observatory. Thanks to Tony Fox for reading and commenting on an earlier draft of this manuscript.

Bregnballe, T., Frederiksen, M. & Gregersen, J. 1997. Seasonal distribution and timing of migration of Cormorants Phalacrocorax carbo sinensis breeding in Denmark. Bird Study 44: 257–276. [Crossref]

Bregnballe, T., Frederiksen, M. & Gregersen, J. 2006. Effects of distance to wintering area on arrival date and breeding performance in Great Cormorants Phalacrocorax carbo. Ardea 94: 619–630.

Bregnballe, T., Lynch, J., Parz-Gollner, R., Volponi, S., Marion, L., Paquet, J.-Y., van Eerden, M. R. & Carss, D. N. 2014. Status of the breeding population of Great Cormorants Phalacrocorax carbo in the Western Palearctic in 2012. In: Bregnballe, T., Lynch, J., Parz-Gollner, R., Marion, L., Volponi, S., Paquet, J.-Y., Carss, D. N. & van Eerden, M. R. (eds.). Breeding numbers of Great Cormorants Phalacrocorax carbo in the Western Palearctic, 2012–2013. Danish Centre for Environment and Energy, Aarhus University.

Bregnballe, T., Herrmann, C, Pedersen, K. T., Wendt, J., Kralj, J. & Frederiksen, M. 2021. Long-term changes in winter distribution of Danish-ringed Great Cormorants. Ardea 109: 327–340. [Crossref]

Butler, C. J. 2003. The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America. Ibis 145: 484–495. [Crossref]

Cotton, P. A. 2003. Avian migration phenology and global climate change. Proceedings of the National Academy of Sciences 100: 12219–12222. [Crossref]

Dunn, E. H. 2016. Bird observatories: an underutilized resource for migration study. The Wilson Journal of Ornithology 128: 691–703. [Crossref]

Flore, B.-O. & Hüppop, O. 1997. Bestandsentwicklung, Durchzug und Herkunft des Kormorans Phalacrocorax carbo an einem Winterrastplatz auf Helgoland. Journal für Ornithologie 138: 253– 270. [Crossref]

Frederiksen, M. & Bregnballe, T. 2000. Evidence for density-dependent survival in adult cormorants from a combined analysis of recoveries and resightings. Journal of Animal Ecology 69: 737–752. [Crossref]

Gienapp, P. & Bregnballe, T. 2012. Fitness consequences of timing of migration and breeding in cormorants. PloS ONE 7: e46165. [Crossref]

Grémillet, D. & Wilson, R. P. 1999. A life in the fast lane: energetics and foraging strategies of the great cormorant. Behavioural Ecology 10: 516–524. [Crossref]

Grémillet, D., Wanless, S., Carss, D. N., Linton, D., Harris, M. P., Speakman, J. R. & Le Maho, Y. 2001. Foraging energetics of Arctic cormorants and the evolution of diving birds. Ecology Letters 4: 180– 184. [Crossref]

Grémillet, D., Chauvin, C., Wilson, R. P., Le Maho, Y. & Wanless, S. 2005. Unusual feather structure allows partial plumage wettability in diving great cormorants Phalacrocorax carbo. Journal of Avian Biology 36: 57–63. [Crossref]

Halupka, L., Czyż, B. & Macias Dominguez, C.M. 2020. The effect of climate change on laying dates, clutch size and productivity of Eurasian Coots Fulica atra. International Journal of Biometeorology 64: 1857–1863. [Crossref]

Herrmann, C., Feige, K.-D. Otto, D. & Bregnballe, T. 2021. Natural regulation of the Baltic population of the great cormorant Phalacrocorax carbo sinensis: the interplay between winter severity and density dependence. Ardea 109: 341–352. [Crossref]

Hüppop, O. & Hüppop, K. 2003. North Atlantic Oscillation and timing of spring migration in birds. Proceedings of the Royal Society B 270: 233–240. [Crossref]

Hüppop, K., Dierschke, J., Dierschke, V., Hill, R., Jachmann, K. F. & Hüppop, O. 2010. Phänologie des „sichtbaren“ Vogelzugs über der Deutschen Bucht. Vogelwarte 48: 181–267.

IPCC 2021. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Masson-Delmotte, V., Zhai, P., Pirani, A., Connors, S. L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Gomis, M. I., Huang, M., Leitzell, K., Lonnoy, E., Matthews, J. B. R., Maycock, T. K., Waterfield, T., Yelekçi, O., Yu, R. & Zhou B. (eds.). Cambridge University Press, Cambridge.

Jonzén, N., Lindén, A., Ergon, T., Knudsen, E., Vik, J. O., Rubolini, D., Piacentini, D., Brinch, C., Spina, F., Karlsson, L., Stervander, M., Andersson, A., Waldenström, J., Lehikoinen, A., Edvardsen, E., Solvang, R. & Stenseth, N. C. 2006. Rapid advance of spring arrival dates in long-distance migratory birds. Science 312: 1959–1961. [Crossref]

Knudsen, E., Lindén, A., Ergon, T., Jonzén, N., Vik, J. O., Knape, J., Røer, J. E. & Stenseth, N. C. 2007. Characterizing bird migration phenology using data from standardized monitoring at bird observatories. Climate Research 35: 59–77. [Crossref]

Knudsen, E., Lindén, A., Both, C., Jonzén, N., Pulido, F., Saino, N., Sutherland, W. J., Bach, L. A., Coppack, T., Ergon, T., Gienapp, P., Gill, J. A., Gordo, O., Hedenström, A., Lehikoinen, E., Marra, P. P., Møller, A .P., Nilsson, A. L. K., Péron, G., Ranta, E., Rubolini, D., Sparks, T. H., Spina, F., Studds, C. E., Saether, S., A., Tryjanowski, P. & Stenseth, N. C. 2011. Challenging claims in the study of migratory birds and climate change. Biological Reviews 86: 928–946. [Crossref]

Krüger, T. & Garthe, S. 2002. Das Vorkommen ausgewählter See- und Küstenvögel vor Wangerooge während des Herbstzuges: der Einfluß von Windrichtung und Windstärke. Journal für Ornithologie 143: 155–170. [Crossref]

Lehikoinen, A., Jaatinen, K., Vähätalo, A. V., Clausen, P., Crowe, O., Deceuninck, B., Hearn, R., Holt, C. A., Hornman, M., Keller, V., Nilsson, L., Langendoen, T., Tománková, I., Wahl, J. & Fox, A. D. 2013. Rapid climate driven shifts in wintering distributions of three common waterbird species. Global Change Biolo/gy 19: 2071–2081. [Crossref]

Lehikoinen, A., Lindén, A., Karlsson, M., Andersson, A., Crewe, T. L., Dunn, E. H., Gregory, G., Karlsson, L., Kristiansen, V., Mackenzie, S., Newman, S., Røer, J. E., Sharpe, C., Sokolov, L. V., Steinholtz, Å., Stervander, M., Tirri, I.-S. & Tjørnløv, R. S. 2019. Phenology of the avian spring migratory passage in Europe and North America: Asymmetric advancement in time and increase in duration. Ecological Indicators 101: 985–991. [Crossref]

Lindén, A. 2011. Using first arrival dates to infer bird migration phenology. Boreal Environment Research 16: 49–60.

Lorentsen, S.-H. 2014a. Trends and status of the breeding population of Great Cormorants in Norway with regard to the Atlantic sub-species Phalacrocorax carbo carbo. In: Bregnballe, T., Lynch, J., Parz- Gollner, R., Marion, L., Volponi, S., Paquet, J.-Y., Carss, D. N. & van Eerden, M. R. (eds.) Breeding numbers of Great Cormorants Phalacrocorax carbo in the Western Palearctic 2012 –2013. Danish Centre for Environment and Energy, Aarhus University. [Crossref]

Lorentsen, S.-H. 2014b. Status of the breeding population of Great Cormorants in Norway in 2012 with regard to the continental sub-species Phalacrocorax carbo sinensis. In: Bregnballe, T., Lynch, J., Parz-Gollner, R., Marion, L., Volponi, S., Paquet, J.-Y., Carss, D. N. & van Eerden, M. R. (eds.) Breeding numbers of Great Cormorants Phalacrocorax carbo in the Western Palearctic, 2012 –2013. Danish Centre for Environment and Energy, Aarhus University.

Lorentsen, S.-H., Anker-Nilssen, T., Barrett, R. T. & Systad, G. H. 2021. Population status, breeding biology and diet of Norwegian Great Cormorants. Ardea 109: 299–312. [Crossref]

López, A., Heggøy, O., Nordsteien, O. & Røer, J. E. 2020. Overvåking av trekkfugler i Sør-Norge 2020. En oppsummering av standardisert ringmerking og trekktellinger ved Jomfruland og Lista. BirdLife Norway, Trondheim.

Marion, L. & Le Gentil, J. 2006. Ecological segregation and population structuring of the Cormorant Phalacrocorax carbo in Europe, in relation to the recent introgression of continental and marine subspecies. Evolutionary Ecology 20: 193–216. [Crossref]

Marra, P. P., Francis, C. M., Mulvihill, R. S. & Moore, F. R. 2005. The influence of climate on the timing and rate of spring bird migration. Oecologia 142: 307–315. [Crossref]

Miles, W. T. S., Bolton, M., Davis, P., Dennis, R., Broad, R., Robertson, I., Riddiford, N. J., Harvey, P. V., Riddington, R., Shaw, D. N., Parnaby, D. & Reid, J. M. 2017. Quantifying full phenological event distributions reveals simultaneous advances, temporal stability and delays in spring and autumn migration timing in long‐distance migratory birds. Global Change Biology 23: 1400–1414. [Crossref]

Miller-Rushing, A. J., Lloyd-Evans, T. L., Primack, R. B. & Satzinger, P. 2008. Bird migration times, climate change, and changing population sizes. Global Change Biology 14: 1959–1972. [Crossref]

Mogstad, D. K. & Røv, N. 1997. Movements of Norwegian Great Cormorants. Supplemento alle Ricerche di Biologia della Selvaggina XXVI: 145–151.

Møller, A.P., Fiedler, W. & Berthold, P. 2010. Effects of Climate Change on Birds. Oxford University Press, Oxford.

Newson, S.E., Moran, N.J., Musgrove, A.J., Pearce-Higgins, J.W., Gillings, S., Atkinson, P.W., Miller, R., Grantham, M.J. & Baillie, S.R. 2016. Long-term changes in the migration phenology of UK breeding birds detected by large-scale citizen science recording schemes. Ibis 158: 481–495. [Crossref]

R Core Team 2022. R: A language and environment for statistical computing. Vienna, Austria.

Rainio, K., Laaksonen, T., Ahola, M., Vähätalo, A. V. & Lehikoinen, E. 2006. Climatic responses in spring migration of boreal and Arctic birds in relation to wintering area and taxonomy. Journal of Avian Biology 37: 507–515. [Crossref]

Ranke, P. S., López, A. & Røer, J. E. 2022. Tidsmessige endringer og forløp av fugletrekket om høsten. Jomfruland og Lista fuglestasjoner 1990–2021. BirdLife Norway, Trondheim.

Rubolini, D., Møller, A., Rainio, K. & Lehikoinen, E. 2007. Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Climate Research 35: 135–146. [Crossref]

Sergio, F., Blas, J., Forero, M. G., Donázar, J. A. & Hiraldo, F. 2007. Sequential settlement and site dependence in a migratory raptor. Behavioral Ecology 18: 811–821. [Crossref]

Smith, R. J. & Moore, F. R. 2005. Arrival timing and seasonal reproductive performance in a long- distance migratory landbird. Behavioral Ecology and Sociobiology 57: 231–239. [Crossref]

Sparks, T. H. 1999. Phenology and the changing pattern of bird migration in Britain. International Journal of Biometeorology 42: 134–138. [Crossref]

Sparks, T. H., Roberts, D. R. & Crick, H. Q. P. 2001. What is the value of first arrival dates of spring migrants in phenology? Avian Ecology and Behaviour 7: 75–85.

Stephens, P. A., Mason, L. R., Green, R. E., Gregory, R. D., Sauer, J. R., Alison, J., Aunins, A., Brotons, L., Butchart, S. H. M., Campedelli, T., Chodkiewicz, T., Chylarecki, P., Crowe, O., Elts, J., Escandell, V., Foppen, R. P. B., Heldbjerg, H., Herrando, S., Husby, M., Jiguet, F., Lehikoinen, A., Lindstrom, A., Noble, D. G., Paquet, J. -Y., Reif, J., Sattler, T., Szep, T., Teufelbauer, N., Trautmann, S., Van Strien, A. J., Van Turnhout, C. A. M., Vorisek, P. & Willis, S. G. 2016. Consistent response of bird populations to climate change on two continents. Science 352: 84–87. [Crossref]

Tryjanowski, P. & Sparks, T. H., 2001. Is the detection of the first arrival date of migrating birds influenced by population size? A case study of the Red-backed Shrike Lanius collurio. International Journal of Biometeorology 45: 217–219. [Crossref]

Usui, T., Butchart, S. H. M. & Phillimore, A. B. 2017. Temporal shifts and temperature sensitivity of avian spring migratory phenology: a phylogenetic meta-analysis. Journal of Animal Ecology 86: 250– 261. [Crossref]

van Eerden, M., van Rijn, S., Volponi, S., Paquet, J.-Y. & Carss, D. 2012. Cormorants and the European environment: exploring cormorant status and distribution on a continental scale. INTERCAFE COST Action 635 Final Report: 1–129.

Verhulst, S., Van Balen, J. H. & Tinbergen, J. M. 1995. Seasonal decline in reproductive success of the great tit: variation in time or quality? Ecology 76: 2392–2403. [Crossref]

Vähätalo, A. V., Rainio, K., Lehikoinen, A. & Lehikoinen, E. 2004. Spring arrival of birds depends on the North Atlantic Oscillation. Journal of Avian Biology 35: 210–216. [Crossref]

Wold, M., Ranke, P. S., Røer, J. E., Solvang, R. & Nicolaysen, H. I. 2012. Bestandsovervåking ved Jomfruland- og Lista Fuglestasjoner i 2011. Norsk Ornitologisk Forening. 21

• Appendices [PDF]