Individual improvements and selective mortality shape lifelong migratory performance

Journal name:
Nature
Volume:
515,
Pages:
410–413
Date published:
DOI:
doi:10.1038/nature13696
Received
Accepted
Published online
Corrected online

Billions of organisms, from bacteria to humans, migrate each year1 and research on their migration biology is expanding rapidly through ever more sophisticated remote sensing technologies2, 3, 4. However, little is known about how migratory performance develops through life for any organism. To date, age variation has been almost systematically simplified into a dichotomous comparison between recently born juveniles at their first migration versus adults of unknown age5, 6, 7. These comparisons have regularly highlighted better migratory performance by adults compared with juveniles6, but it is unknown whether such variation is gradual or abrupt and whether it is driven by improvements within the individual, by selective mortality of poor performers, or both. Here we exploit the opportunity offered by long-term monitoring of individuals through Global Positioning System (GPS) satellite tracking to combine within-individual and cross-sectional data on 364 migration episodes from 92 individuals of a raptorial bird, aged 1–27 years old. We show that the development of migratory behaviour follows a consistent trajectory, more gradual and prolonged than previously appreciated, and that this is promoted by both individual improvements and selective mortality, mainly operating in early life and during the pre-breeding migration. Individuals of different age used different travelling tactics and varied in their ability to exploit tailwinds or to cope with wind drift. All individuals seemed aligned along a race with their contemporary peers, whose outcome was largely determined by the ability to depart early, affecting their subsequent recruitment, reproduction and survival. Understanding how climate change and human action can affect the migration of younger animals may be the key to managing and forecasting the declines of many threatened migrants.

At a glance

Figures

  1. A river of raptors.
    Figure 1: A river of raptors.

    Migration routes of black kites born in Doñana National Park, southwestern Spain. Pre-breeding tracks are shown in red and post-breeding tracks in yellow. Eleven pre-breeding tracks starting from further south were shortened for clarity of presentation.

  2. Migration performance across and within individuals.
    Figure 2: Migration performance across and within individuals.

    a, Across individuals, pre-breeding departure date improved rapidly during the first 7 years of life and then reached a plateau. b, In these initial years, surviving birds (red line) had earlier departure dates (right axis) than birds that died within the next year (blue line). Similarly, within individuals, the repeatability of departure (black bars, left axis) was lowest in the initial years of life, when individual improvements (grey bars, left axis) were highest, and stabilized after birds were 7 years old. Therefore, the cross-sectional pattern depicted in a was consistent with both within-individual improvements and selective removal of inferior performers. Individual improvements were calculated as proportional changes from year t to year t + 1 and multiplied by 3 for clarity of presentation. Details of within-individual improvements and repeatability analyses are given in Extended Data Tables 5, 6 and 8. The fitted line in a is a smoother. Error bars represent 1 standard error of the mean (s.e.m.).

  3. Age-related changes in average speed, duration and timing of pre-breeding migrations.
    Figure 3: Age-related changes in average speed, duration and timing of pre-breeding migrations.

    a, Speed was maximum for young adults and minimum for juveniles. b, Journey duration was longest for juveniles, shortest for young adults and intermediate in older kites. c, Arrival date occurred progressively earlier with age until seven years old and reached a stable value thereafter, replicating the departure pattern of Fig. 2a. The complete set of all components is shown in Extended Data Fig. 1. Error bars represent 1 s.e.m.

  4. Age-related changes in average speed, duration and timing of post-breeding migrations.
    Figure 4: Age-related changes in average speed, duration and timing of post-breeding migrations.

    a, Speed was maximum for older individuals, minimum for juveniles and intermediate for young adults. b, Journey duration became progressively shorter with age. c, Arrival date was earliest for older birds and latest for young adults. The complete set of all components is shown in Extended Data Fig. 2. Error bars represent 1 s.e.m.

  5. Mean components of pre-breeding migration.
    Extended Data Fig. 1: Mean components of pre-breeding migration.

    aj, Migration components varied cross-sectionally with age in timing (a, b), speed of progression (c, d), duration (e, f, g, h), route length (i) and longitudinal position of the route (j). Error bars represent 1 s.e.m.

  6. Mean components of post-breeding migration.
    Extended Data Fig. 2: Mean components of post-breeding migration.

    aj, Migration components varied cross-sectionally with age in timing (a, b), speed of progression (c, d), duration (e, f, g, h), route length (i) and longitudinal position of the route (j). Error bars represent 1 s.e.m.

Tables

  1. Estimates of pre-breeding and post-breeding migration by 92 individual black kites of Donana National Park, southwestern Spain
    Extended Data Table 1: Estimates of pre-breeding and post-breeding migration by 92 individual black kites of Doñana National Park, southwestern Spain
  2. Summary of main results of the mixed models examining the effects of age and environmental variables on migration components
    Extended Data Table 2: Summary of main results of the mixed models examining the effects of age and environmental variables on migration components
  3. Cross-sectional effect of age and environmental variables on migration components in the pre-breeding migration
    Extended Data Table 3: Cross-sectional effect of age and environmental variables on migration components in the pre-breeding migration
  4. Cross-sectional effect of age and environmental variables on migration components in the post-breeding migration
    Extended Data Table 4: Cross-sectional effect of age and environmental variables on migration components in the post-breeding migration
  5. Longitudinal effect of age, migration timing and environmental variables on migration components in the pre-breeding migration
    Extended Data Table 5: Longitudinal effect of age, migration timing and environmental variables on migration components in the pre-breeding migration
  6. Repeatability of migration components for different age classes
    Extended Data Table 6: Repeatability of migration components for different age classes
  7. Mixed effects models testing the relationship between migration components and fitness
    Extended Data Table 7: Mixed effects models testing the relationship between migration components and fitness
  8. Longitudinal effect of age, migration timing and environmental variables on migration components in the post-breeding migration
    Extended Data Table 8: Longitudinal effect of age, migration timing and environmental variables on migration components in the post-breeding migration

Videos

  1. Video 1: The speed of kites in the pre-breeding migration varied with age and was at the maximum in birds of age 3-6, intermediate for birds above 7 years old and lowest in 1-2 years olds
    Video 1: Video 1: The speed of kites in the pre-breeding migration varied with age and was at the maximum in birds of age 3-6, intermediate for birds above 7 years old and lowest in 1-2 years olds
    In this video simulation, individuals of all ages are imposed to depart for migration at the same time. They then travel with a speed proportional to the mean value for their age, class and progress along the average population route (see Methods). Under this scenario of equal departure timings, individuals of 3-6 years of age are the first to arrive to the breeding quarters, followed by kites older than seven years and then by 1-2 years old birds. This pattern changes radically when incorporating differences in timing of departure among age classes (see Supplementary Video 2).
  2. Video 2: When incorporating differences in timing of departure among age-classes, older birds always arrived at the breeding quarters before younger ones, independently of differences in speed performance.
    Video 2: Video 2: When incorporating differences in timing of departure among age-classes, older birds always arrived at the breeding quarters before younger ones, independently of differences in speed performance.
    In this simulation, differences in the timings of departure among age classes are proportional to the observed mean differences in timing. The birds then travel with a speed proportional to the mean value for their age, class and progress along the average route, as in Supplementary Video 1. Under this scenario, age-differences in departure times are so large that they fully dictate the order of arrival and older birds always arrive earlier than younger ones. Therefore, the higher speed of 3-6 years olds, shown in Supplementary Video 1, is swamped by the capability to depart early, which is typical of older, more experienced individuals. Note that the migration speeds in Video 1 and 2 have been arranged so that, in both cases, the overall video-duration is 50 seconds, while the relationship between migratory speed and the time lags in sequential departures are always proportional to their observed averages.

Change history

Corrected online 19 November 2014
A minor change was made to the main text.

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Author information

Affiliations

  1. Department of Conservation Biology, Estación Biológica de Doñana—CSIC, Avenida Americo Vespucio, 41092 Seville, Spain

    • Fabrizio Sergio,
    • Alessandro Tanferna,
    • Renaud De Stephanis,
    • Lidia López Jiménez,
    • Julio Blas &
    • Fernando Hiraldo
  2. Population Ecology Group, Institute for Mediterranean Studies (IMEDEA), CSIC-UIB, 07190 Esporles, Spain

    • Giacomo Tavecchia
  3. Department of Theoretical and Applied Sciences, Insubria University, 21100 Varese, Italy

    • Damiano Preatoni

Contributions

F.S., A.T., L.L.J., J.B. and F.H. conducted fieldwork. F.S., A.T., R.D.S., G.T. and D.P. prepared the database, extracted and processed the environmental data from internet sources and analysed the data. F.S. and F.H. obtained funding. R.D.S., A.T. and F.S. developed the Supplementary Videos. All authors took part in the conceptual planning of the study and in the preparation of the manuscript.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

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Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Mean components of pre-breeding migration. (300 KB)

    aj, Migration components varied cross-sectionally with age in timing (a, b), speed of progression (c, d), duration (e, f, g, h), route length (i) and longitudinal position of the route (j). Error bars represent 1 s.e.m.

  2. Extended Data Figure 2: Mean components of post-breeding migration. (281 KB)

    aj, Migration components varied cross-sectionally with age in timing (a, b), speed of progression (c, d), duration (e, f, g, h), route length (i) and longitudinal position of the route (j). Error bars represent 1 s.e.m.

Extended Data Tables

  1. Extended Data Table 1: Estimates of pre-breeding and post-breeding migration by 92 individual black kites of Doñana National Park, southwestern Spain (365 KB)
  2. Extended Data Table 2: Summary of main results of the mixed models examining the effects of age and environmental variables on migration components (205 KB)
  3. Extended Data Table 3: Cross-sectional effect of age and environmental variables on migration components in the pre-breeding migration (580 KB)
  4. Extended Data Table 4: Cross-sectional effect of age and environmental variables on migration components in the post-breeding migration (601 KB)
  5. Extended Data Table 5: Longitudinal effect of age, migration timing and environmental variables on migration components in the pre-breeding migration (252 KB)
  6. Extended Data Table 6: Repeatability of migration components for different age classes (312 KB)
  7. Extended Data Table 7: Mixed effects models testing the relationship between migration components and fitness (127 KB)
  8. Extended Data Table 8: Longitudinal effect of age, migration timing and environmental variables on migration components in the post-breeding migration (315 KB)

Supplementary information

Video

  1. Video 1: Video 1: The speed of kites in the pre-breeding migration varied with age and was at the maximum in birds of age 3-6, intermediate for birds above 7 years old and lowest in 1-2 years olds (2.73 MB, Download)
    In this video simulation, individuals of all ages are imposed to depart for migration at the same time. They then travel with a speed proportional to the mean value for their age, class and progress along the average population route (see Methods). Under this scenario of equal departure timings, individuals of 3-6 years of age are the first to arrive to the breeding quarters, followed by kites older than seven years and then by 1-2 years old birds. This pattern changes radically when incorporating differences in timing of departure among age classes (see Supplementary Video 2).
  2. Video 2: Video 2: When incorporating differences in timing of departure among age-classes, older birds always arrived at the breeding quarters before younger ones, independently of differences in speed performance. (2.69 MB, Download)
    In this simulation, differences in the timings of departure among age classes are proportional to the observed mean differences in timing. The birds then travel with a speed proportional to the mean value for their age, class and progress along the average route, as in Supplementary Video 1. Under this scenario, age-differences in departure times are so large that they fully dictate the order of arrival and older birds always arrive earlier than younger ones. Therefore, the higher speed of 3-6 years olds, shown in Supplementary Video 1, is swamped by the capability to depart early, which is typical of older, more experienced individuals. Note that the migration speeds in Video 1 and 2 have been arranged so that, in both cases, the overall video-duration is 50 seconds, while the relationship between migratory speed and the time lags in sequential departures are always proportional to their observed averages.

Additional data