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Individual Variability in Migration Timing Can Explain Long-Term, Population-Level Advances in a Songbird

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Migratory animals may be particularly at-risk due to global climate change, as they must match their timing with asynchronous changes in suitable conditions across broad, spatiotemporal scales. It is unclear whether individual long-distance migratory songbirds can flexibly adjust their timing to varying inter-annual conditions. Longitudinal data for individuals sampled across migration are ideal for investigating phenotypic plasticity in migratory timing programs, but remain exceptionally rare. Using the largest, repeat-tracking data set available to date for a songbird (n = 33, purple martin Progne subis), we investigated individual variability in migration timing across 7,000–14,000 km migrations between North American breeding sites and South American overwintering sites. In contrast to previous studies of songbirds, we found broad, within-individual variability between years in the timing of spring departure (0–20 days), spring crossing of the Gulf of Mexico (0–20 days), and breeding site arrival (0–18 days). Spring departure and arrival dates were fairly repeatable across years (depart r = 0.39; arrive r = 0.32). Fall migration timing was more variable at the individual level (depart range = 0–19 days; gulf crossing range = 1–15 days; arrive range = 0–24 days) and less repeatable, with fall crossing of the Tropic of Cancer being the least repeatable (r = 0.0001). In this first, repeat-tracking study of a diurnal migratory songbird, the high within-individual variability in timing that we report may reflect the greater influence of environmental and social cues on migratory timing, as compared to the migration of more solitary, nocturnally migrating songbirds. Further, large, within-individual variability in migration dates (0–24 days) suggest that advances in spring arrival dates with climate change that have been reported for multiple songbird species (including purple martins) could potentially be explained by intra-individual flexibility in migration timing. However, whether phenotypic plasticity will be sufficient to keep up with the pace of climate change remains to be determined.
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ORIGINAL RESEARCH
published: 06 September 2019
doi: 10.3389/fevo.2019.00324
Frontiers in Ecology and Evolution | www.frontiersin.org 1September 2019 | Volume 7 | Article 324
Edited by:
Brett K. Sandercock,
Norwegian Institute for Nature
Research (NINA), Norway
Reviewed by:
Jason Courter,
Malone University, United States
Kristen Covino,
Loyola Marymount
University, United States
*Correspondence:
Kevin C. Fraser
kevin.fraser@umanitoba.ca
Specialty section:
This article was submitted to
Behavioral and Evolutionary Ecology,
a section of the journal
Frontiers in Ecology and Evolution
Received: 27 March 2019
Accepted: 13 August 2019
Published: 06 September 2019
Citation:
Fraser KC, Shave A, de Greef E,
Siegrist J and Garroway CJ (2019)
Individual Variability in Migration
Timing Can Explain Long-Term,
Population-Level Advances in a
Songbird. Front. Ecol. Evol. 7:324.
doi: 10.3389/fevo.2019.00324
Individual Variability in Migration
Timing Can Explain Long-Term,
Population-Level Advances in a
Songbird
Kevin C. Fraser 1
*, Amanda Shave 1, Evelien de Greef 1, Joseph Siegrist 2and
Colin J. Garroway 1
1Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada, 2Purple Martin Conservation
Association, Erie, PA, United States
Migratory animals may be particularly at-risk due to global climate change, as they
must match their timing with asynchronous changes in suitable conditions across
broad, spatiotemporal scales. It is unclear whether individual long-distance migratory
songbirds can flexibly adjust their timing to varying inter-annual conditions. Longitudinal
data for individuals sampled across migration are ideal for investigating phenotypic
plasticity in migratory timing programs, but remain exceptionally rare. Using the largest,
repeat-tracking data set available to date for a songbird (n=33, purple martin Progne
subis), we investigated individual variability in migration timing across 7,000–14,000 km
migrations between North American breeding sites and South American overwintering
sites. In contrast to previous studies of songbirds, we found broad, within-individual
variability between years in the timing of spring departure (0–20 days), spring crossing of
the Gulf of Mexico (0–20 days), and breeding site arrival (0–18 days). Spring departure
and arrival dates were fairly repeatable across years (depart r=0.39; arrive r=0.32).
Fall migration timing was more variable at the individual level (depart range =0–19 days;
gulf crossing range =1–15 days; arrive range =0–24 days) and less repeatable, with
fall crossing of the Tropic of Cancer being the least repeatable (r=0.0001). In this first,
repeat-tracking study of a diurnal migratory songbird, the high within-individual variability
in timing that we report may reflect the greater influence of environmental and social
cues on migratory timing, as compared to the migration of more solitary, nocturnally
migrating songbirds. Further, large, within-individual variability in migration dates (0–24
days) suggest that advances in spring arrival dates with climate change that have been
reported for multiple songbird species (including purple martins) could potentially be
explained by intra-individual flexibility in migration timing. However, whether phenotypic
plasticity will be sufficient to keep up with the pace of climate change remains to
be determined.
Keywords: phenotypic plasticity, spring phenology, repeatability, climate change, avian, long-distance migration,
songbird
Fraser et al. Individual Variability in Songbird Migration
INTRODUCTION
Phenotypic plasticity in animal migration timing could provide
the means for rapid acclimation to environmental change,
as compared to adaptive responses through genetic change
(Charmantier and Gienapp, 2014). To what extent phenotypic
plasticity and/or micro-evolution are the mechanisms
responsible for population-level advances in the spring
migration timing of some landbirds has been hotly debated
(Knudsen et al., 2011; Charmantier and Gienapp, 2014). Steep
population declines among migratory species (Both et al., 2010),
lends urgency to determining whether constraints on adaptive
timing are a contributing factor.
Longitudinal data are ideal for research on these
themes because they provide the opportunity to investigate
phenotypic variation within individuals in response to varying
environmental conditions across years (Charmantier and
Gienapp, 2014). For songbird migration, most previous studies
have focused on the use of observational data to determine
the individual repeatability (r) of spring migration departure
and arrival dates. These studies report broad variation (r=
0.04–0.51), both within and among migratory species (Potti,
1998; Brown and Brown, 2000; Moller, 2001; Ninni et al., 2004;
Cooper et al., 2009; Studds and Marra, 2011). Direct-tracking
technologies (Stutchbury et al., 2009) provide the means to
examine complete annual migration tracks, but studies where
multiple migrations by the same individual are monitored
are still rare (Both et al., 2016). In a Neotropical songbird
(wood thrush, Hylocichla mustelina), within-individual spring
migration timing was remarkably repeatable, with a mean
difference of just 3 days in spring arrival date between years,
suggesting limited plasticity (n=10; Stanley et al., 2012). In
a Palearctic example (red-backed shrikes, Lanius collurio),
within-individual variability was similarly low, where mean
within-individual differences were 3–12 days, and breeding
arrival date (n=2) varied by only 1–4 days (Pedersen et al.,
2018). Thus, repeatability of migration timing of songbirds using
direct tracking is generally reported to be high, particularly in
spring. However, studies to date have relied on low sample size
(<20 individuals), are thinly spread across species and migratory
systems, and have focused on nocturnally migrating species
(Both et al., 2016).
In many migratory species, population-level advances in
spring migration timing have been observed over decadal scales
and linked to temperature increase with climate change (Butler,
2003; Mayor et al., 2017; Lehikoinen et al., 2019). Across
European and North American migratory landbird systems, the
mean advance over several decades in spring migration timing
was 1 week (Lehikoinen et al., 2019); with advances within
some species reported to be >2 weeks (Butler, 2003). There is
much debate as to whether these timing advances are the result
of phenotypic plasticity, micro-evolutionary change, or both
(Knudsen et al., 2011). For species with high, within-individual
repeatability in migration timing, these rapid population-level
advances in timing are difficult to reconcile. In Icelandic
black-tailed godwits (Limosa limosa islandica), population-level
arrival dates advanced by approximately 17 days over 20 years
(Gunnarsson and Tomasson, 2011) but over this same time
span individual arrival dates were highly consistent (r=0.51;
Gill et al., 2014). These results for black-tailed godwits suggest
that advances were not driven by individual plasticity of adult
migrants, but rather ontogenetic effects during development
could underlie these rapid advances in timing (Gill et al.,
2014). Such comparisons of individual variability vs. population-
level advances in timing remain rare, and need to be further
explored in other species and systems. There is currently a
deficit of knowledge about the mechanisms of adaptive change
(microevolutionary and/or phenotypic plasticity) in response
to environmental conditions during migration (Pulido and
Berthold, 2004) and the impact of longer-scale climatic effects
on the flexibility of migration patterns (Knudsen et al., 2011),
especially for long-distance migratory songbirds.
We investigated the phenotypic plasticity of migration timing
by using a diurnal, long distance, Neotropical migratory songbird
(purple martin, Progne subis) that travels 10, 000–20, 000 km
annually between North American breeding sites and South
American overwintering sites (Fraser et al., 2012, 2013a,b).
Purple martins are aerial insectivores, and like other swallows,
are thought to use a fly-and-forage strategy during their diurnal
migration (Brown and Tarof, 2013). At the population-level, this
species has advanced spring migration timing by 8–20 days over
the last 100 years (Arab and Courter, 2015). However, arrival
dates did not advance in response to a record-setting, early spring
in 2012 (Fraser et al., 2013a). Data on the variation in individual
timing across multiple migrations are therefore required to
further investigate the potential for phenotypic plasticity in
purple martins in response to environmental conditions and
to determine whether this can explain long-term advances in
timing. We used the largest repeat-track data set available for
a songbird, comprised of 33 individuals tracked across 2 years
by using light-level geolocators. Our objectives were to (1)
determine within-individual variation and repeatability (r) in
timing across both spring and fall migration, and (2) assess
whether the degree of within-individual variability provides a
potential mechanism to explain population-level advances in
spring timing reported for martins and whether this species can
serve as a model for similar investigations in other songbirds.
METHODS
Geolocator Analysis Methods
Light-level geolocators were deployed on adult purple martins
at 8 North American breeding sites (latitudinal range 38.36N
to 53.02N; Supplementary Table 1) using a leg-loop backpack-
style harness made of Teflon ribbon (Rappole and Tipton, 1991;
Stutchbury et al., 2009) and retrieved in the following year (or
subsequent year, n=2) at the same locations (2009–2016). This
study was conducted in accordance with the recommendations
of the Ornithological Council’s Guidelines to the Use of Wild
Birds in Research’ and was approved by the University of
Manitoba and York University Animal Care Committees (2009-
2 W, F14-009/1–3).
We defined sunrises and sunsets (twilights) from the raw
geolocator light data using the preprocessLight function in the
Frontiers in Ecology and Evolution | www.frontiersin.org 2September 2019 | Volume 7 | Article 324
Fraser et al. Individual Variability in Songbird Migration
R-package BAStag version 0.1.3 (Wotherspoon et al., 2016). We
used a light intensity threshold of 32 to define the separation of
day and night. Events that influenced the geolocator’s light sensor
outside of sunrise and sunset times (e.g., shading during day, light
during night) indicated false twilights. We used the initiation
of heavy shading (false twilights during daylight periods) in
spring, that clearly indicated entrance and exits of nest cavities,
to identify breeding arrival date. After defining arrival date, all
false twilights were removed.
The twilight dataset was used to define daily locations
and movement periods by using the R-package GeoLight
version 2.0 (Lisovski and Hahn, 2012). We used the coord
function to determine spatial coordinates throughout entire
migratory tracks. We calculated an appropriate sun elevation
angle using twilight data at each bird’s known breeding
location, before fall migration. Latitudes impacted by spring
and fall equinox periods were omitted by using a tolerance
level of 0.13 (Lisovski and Hahn, 2012). The resulting data
were used to determine daily coordinates and movement
periods and to identify spring and fall arrival and departure
dates, as well as the date individuals crossed the Tropic
of Cancer (23.4N). We used the changeLight function to
determine residency and movement periods, and shifts in
latitudinal and longitudinal coordinates, to identify departure
and fall arrival dates. We defined overwintering locations as
a tenure of >7 days within the known non-breeding range.
Most stopovers in this region were <7 days (Van Loon
et al., 2017), thus this provided a conservative estimate of
when birds had completed migration and arrived at their
overwintering destination.
Repeatability of Spring and Fall Migration
Phenology
To investigate if individuals are consistent in their migration
timing between years, repeatability was examined for birds
tracked for at least 2 years (individuals =33, geolocator tracks
=67). We examined the repeatability of migration departure
date (fall tracks =66, spring tracks =67), date passing the
Tropic of Cancer (23.4N; fall tracks =34, spring tracks =61),
and date of arrival at the breeding grounds or overwintering
grounds (fall tracks =67, spring tracks =67). We also
included 144 single-tracked (1 year only) individuals in the
analysis to better account for population level variability in
the analysis, resulting in a total of 5–57 tracks per breeding
location (Supplementary Table 1). Repeatability was calculated
as the fraction of variation in behavior between individuals, as
compared to the sum of phenotypic plasticity and measurement
error (Nakagawa and Schielzeth, 2010). Repeatability is a
proportion between 0 and 1, where low values indicate most
of the variation is due to plasticity and error. The adjusted
repeatability (value of repeatability calculated after controlling
for confounding effects) of aspects of migration timing were
calculated in linear, mixed-effects models using the package
MCMCglmm (Hadfield, 2010). In this case the confounding
effects of sex and age were set as fixed effects (males and older
birds may have earlier timing) with year, individual, and breeding
colony as random effects to control for repeated measures. We
did not include temperature or other weather factors in our
analysis owing to limitations in the number of repeat-track birds
per site. Confidence intervals for repeatability were estimated
by parametric bootstrapping with 1,000 replications. Results
were replicated with an uninformed prior which produced
quantitatively similar results (Table 1) with overlapping 95%
credibility intervals. All analyses were done in R version 3.5.3 (R
Core Team, 2018).
RESULTS
We found that spring migration timing (departure, crossing
23.4N, arrival) was more repeatable between years at the
individual level than timing during fall migration (spring range,
r=0.32–0.39; fall range, r=0.0001–0.001; Table 1,Figure 1).
The timing of spring departure was the most consistent across
years (r=39, CI =0.08–0.50), perhaps owing to strong
endogenous control of migration initiation. Spring crossing of
the Tropic of Cancer (23.4N) and breeding arrival date were
also fairly consistent across years (cross r=0.32; arrive r=
0.32). Fall arrival date was much less repeatable than breeding
arrival date (0.0009 vs. 0.32) (Figure 1). Variance explained
by the random factors of colony and year ranged from 32.47
to 90.76 and 3.09–30.94, respectively (Supplementary Table 2).
Age had a significant effect on timing across both spring and
fall migration, with ASY birds departing and arriving earlier
by 5.52–7.18 days as compared to SY birds. Sex impacted
the timing of spring departure and spring cross only, with
males migrating 6.46 and 6.08 days earlier than females
(Supplementary Table 3).
Within-individual variability between the first and second
year of tracking was broad (0–24 days), with individual timing
earlier (1–24 days), or later (1–23 days) in the second year of
tracking (Figure 2). In spring, departure date varied by 0–20
days, spring crossing of 23.4N by 0–20 days, and arrival at the
TABLE 1 | Adjusted repeatability estimates and 95% credibility intervals for spring
and fall migration (2008–2016) including departure dates (n=67; n=66), spring
and fall crossing the Tropic of Cancer (n=61, n=34), and spring and fall arrival
dates (n=67; n=67).
Timing Adjusted repeatability 95% CI
Spring departure from non-breeding site 0.39 0.08, 0.50
Spring crossing tropic of cancer 0.32 0.16, 0.54
Spring arrival at breeding site 0.32 0.12, 0.48
Fall departure from breeding site 0.001 <0.001, 0.38
Fall crossing tropic of cancer 0.0001 <0.001, 0.07
Fall arrival at non-breeding site 0.0009 <0.001, 0.47
Individuals were tracked for two spring migrations, except one individual tracked for three
spring migrations. Estimates and credibility intervals were calculated using MCMCglmm
(Hadfield, 2010)*. We included fixed effects of sex and age and controlled for non-
independence of year and individuals within breeding colonies by including them as
random effects. Uninformed prior distributions (V =1, nu =0.002) were used for
all variables.
Hadfield (2010)*.
Frontiers in Ecology and Evolution | www.frontiersin.org 3September 2019 | Volume 7 | Article 324
Fraser et al. Individual Variability in Songbird Migration
FIGURE 1 | Comparison of migration timing (day of year) at the individual level for the first vs. second year of tracking. Colors show breeding locations where
geolocators were retrieved and correspond to points indicated on the map. Line indicates 1:1, where points below the line indicate earlier migration in year two. The
map shows the year-round purple martin range in purple (Brown and Tarof, 2013).
breeding site by 0–18 days. Fall migration timing was generally
more variable at the individual level (depart range =0–19 days;
cross range =1–15 days; arrive range =0–24 days). Overall
within-individual variability over the year was therefore up to
24 days, which spans the 8–20 day population-level advance in
spring arrival date over 100 years, reported for purple martins
(Arab and Courter, 2015) (Figure 2).
DISCUSSION
Individual patterns of migration timing across years provide
invaluable clues regarding the phenotypic plasticity of migration
timing. We show that spring migration timing of a long-distance
migratory songbird was more repeatable, from start-to-finish,
than fall migration, with spring departure date being the most
consistent between years. We found broad, within-individual
variability in migration timing (year 1 as compared to year 2)
at key points around the annual cycle (start and stop dates,
and approximate midway points). We show that broad, intra-
individual variability (up to 24 days earlier or 23 days later in
the second year of tracking), was a feature of both spring and fall
migration. Our results therefore suggest individual plasticity as a
potential mechanism to account for population-level advances in
spring arrival date (8–20 days) reported for purple martin (Arab
and Courter, 2015). The degree of plasticity we show in individual
martins also exceed mean population-level advancements (1
week) for spring migration reported for North American and
European migratory landbird systems, including several species
of long-distance aerial insectivores (Lehikoinen et al., 2019).
It has been difficult to reconcile the decadal-scale advances
in spring migration timing at the population level, with
intra-individual data that show high consistency of migration
timing (e.g., Gill et al., 2014). It is debated whether strong
selection for advanced timing and rapid micro-evolution could
be responsible for population-level change (Knudsen et al.,
2011) because advances via these mechanisms are generally
predicted to take much longer. For example, using quantitative
genetic models an observed 14-days advance in laying date
in great tits (Parus major) was estimated to require more
than two centuries to attain via micro-evolution (Charmantier
and Gienapp, 2014). The predicted time period is considerably
longer than the scale of the 10–100-years advances reported
for multiple landbird species across North American and
European migration systems (Lehikoinen et al., 2019). If micro-
evolutionary responses cannot occur this quickly (Charmantier
and Gienapp, 2014), and individuals do not exhibit a high
level of phenotypic plasticity in spring timing, then how do
we explain population-level advances in timing over short
timescales? Our results show, that at least in purple martins,
individual variation is a potential explanation for the kinds of
advances reported in spring timing (Arab and Courter, 2015).
We found within individual variation of up to 24 days whereas
population level advancements for this species over 100 years
are between 8 and 20 days (Arab and Courter, 2015). Our
results contrast those for Icelandic godwit, where consistency in
individual timing precluded individual plasticity of adult birds
as a viable explanation for population-level advances in timing
(Gill et al., 2014). Further studies are required across species
and systems to determine whether individual plasticity is a
Frontiers in Ecology and Evolution | www.frontiersin.org 4September 2019 | Volume 7 | Article 324
Fraser et al. Individual Variability in Songbird Migration
FIGURE 2 | The difference in migration timing between year one and year two for individual purple martins tracked between North American breeding and South
American overwintering sites. A positive value indicates earlier timing in the second year of tracking. Sample sizes for each timing category are as follows: depart fall =
32, cross fall =10, arrive fall =32, depart spring =32, cross spring =28, arrive spring =33. Data show timing at migration start and end points, as well as the timing
of crossing the Tropic of Cancer (23.4N), in both spring and fall. Long-term data for mean breeding arrival date in spring across the range (from Arab and Courter,
2015) are included to enable comparison of these longer-term advances in timing over 100 years with short-term differences at the individual level (this study).
potential explanation for observed advances in timing. It would
also be valuable for future studies to investigate the influence
of additional factors on individual plasticity, such as nocturnal
vs. diurnal migratory strategies, foraging guild, short vs. long-
distance migration (Lehikoinen et al., 2019), nest strategy, and
within-species patterns.
We found moderate repeatability of spring migration timing
(range: r=0.32–0.39) that is lower than reported in other studies
of nocturnally migrating songbirds (e.g., range: r=0.49–0.71,
Stanley et al., 2012) and many long-distance migrants generally
(Both et al., 2016). We found the highest repeatability of timing
at spring departure from the non-breeding grounds as has been
shown for red-backed shrikes, Icelandic whimbrels, and black-
tailed godwits; perhaps owing to the strong role of endogenous
cues in migration initiation (Gwinner, 1996; Pedersen et al.,
2018; Carneiro et al., 2019; Senner et al., 2019). Sex and age
were also important factors influencing spring departure timing,
but differences between the sexes diminished by the time of
arrival at breeding areas, whereas older birds were consistently
earlier than younger ones. Relatively high repeatability of spring
arrival date may reflect strong selection on timing at the breeding
ground. In martins, high competition for nest cavities may
further contribute to higher repeatability of spring arrival dates
(Brown and Tarof, 2013). In contrast, fall timing was much
less repeatable (r=0.0001–0.001). Particularly low repeatability
of fall migration arrival date (r=0.0009), may reflect relaxed
selection on this trait in purple martins; a species that is non-
territorial in winter and joins large communal roosts, in contrast
to a songbird that is territorial in winter, where repeatability was
relatively high (r=0.62; Stanley et al., 2012). Intra-individual
variation in nest success may also have contributed to low fall
repeatability values in our study, if birds with failed nests depart
earlier than birds attending young from successful broods. The
overall, lower repeatability of migratory timing in our study of
a diurnal migrant as compared to results for some nocturnally
migrating songbirds (Both et al., 2016) may be influenced by
migratory strategy (diurnal vs. nocturnal). Phenological and
repeatability studies of songbirds have tended to focus more
on nocturnally migrating species and comparisons of short and
long-distance migrants (Both et al., 2016; Lehikoinen et al., 2019),
however, diurnal and nocturnal migrants may exhibit different
amounts of plasticity in timing to environmental change and
should be further investigated.
We found higher repeatability in spring than fall for
crossing of the Tropic of Cancer (23.4N), which is generally
associated with crossing of the Gulf of Mexico in martins, as
most individuals make a >800 km open-water crossing of this
“barrier” during spring and fall migration (Fraser et al., 2013a,b).
Lower repeatability in fall may indicate greater, population-level
synchronization of the timing of crossing in this season. In
wood thrushes, crossing of the gulf showed low repeatability
during both spring and fall (r=0.12, Stanley et al., 2012).
In spring, the timing of gulf crossing in martins is not largely
impacted by weather conditions (Abdulle and Fraser, 2018),
thus we infer that higher consistency in individual timing at
this barrier is a result of a carry-over effect of spring departure
timing, rather than an influence of conditions at this stage
of migration.
We speculate that the generally larger, intra-individual
variation (up to 24 days) that we found for martins as compared
to other songbirds (Stanley et al., 2012; Both et al., 2016; Pedersen
et al., 2018), may reflect the nature of migration and social
behavior in martins, and possibly other swallows. The intra-
individual variability we found for purple martins is more similar
to broad, within-individual variation recently shown for some
shorebirds (Senner et al., 2019; Verhoeven et al., 2019), than
to data reported for nocturnally migrating songbirds. Purple
martins are diurnal migrants that roost in large flocks during
stopovers across migration (Brown and Tarof, 2013), and may
use island-like habitats for stopover (Fraser et al., 2017; Fournier
et al., 2019). Large social aggregations and suitable stopover
habitat are unevenly distributed across a migratory landscape,
Frontiers in Ecology and Evolution | www.frontiersin.org 5September 2019 | Volume 7 | Article 324
Fraser et al. Individual Variability in Songbird Migration
thus martin stopover decisions may be influenced by these social
factors which could contribute to variation in their individual
timing. In contrast, diurnal songbirds that migrate singly during
the night may not require social stopover cues to the same
degree, which may favor more independent and consistent
migration schedules. While it has been demonstrated that short-
distance migrants may exhibit swifter phenological shifts in
response to environmental change than long-distance migrants
(Hurlbert and Liang, 2012; Kullberg et al., 2015; Takuji et al.,
2017), whether diurnal, long-distance migrants exhibit greater
phenotypic plasticity than nocturnal ones would be valuable
to determine.
Our data did not provide the opportunity to examine
variation in repeatability across populations breeding at different
latitudes, but such within-species investigations are an important
frontier. Such research would be particularly important for
purple martins and other aerial insectivores, where strong
north-south patterns of population decline are reported (Nebel
et al., 2010), and where relative limitations in behavioral
plasticity between populations could be playing a role. More
northern breeding populations may exhibit larger advances
in spring arrival dates than more southern ones (Arab and
Courter, 2015), which should be investigated in concert with
individual-level patterns.
CONCLUSION
In an era of rapid, global environmental change, it is critical
that we address the degree to which migratory birds can mount
phenotypic responses to change. In this first investigation using
a diurnal migrant and the largest repeat-tracking data set for a
songbird, we show that phenotypic plasticity in migration timing
is a potential mechanism to explain decadal-scale, population-
level advancement in spring migration timing. It remains to
be determined whether the degree of individual plasticity we
show is connected to, or cued by, temperature and whether any
advances in migration timing are sufficient to match advances
in seasonal phenology of lower trophic levels. Future research
should also investigate the role of environmental cues and
other mechanisms contributing to within-individual variation in
migration timing.
DATA AVAILABILITY
All datasets generated for this study are included in
the manuscript and/or the Supplementary Files.
ETHICS STATEMENT
This study was conducted in accordance with the
recommendations of the Ornithological Council’s Guidelines
to the Use of Wild Birds in Research’ and was approved by
the University of Manitoba and York University Animal Care
Committees (2009- 2W, F14-009/1-3).
AUTHOR CONTRIBUTIONS
KF, AS, and JS conducted fieldwork. KF, AS, EG, and CG analyzed
the data. KF, AS, EG, JS, and CG wrote the manuscript.
ACKNOWLEDGMENTS
For field assistance and support we thank Nanette Mickle, Paul
Mammenga, Tim Shaheen, Kelly Applegate, Michael North,
Larry Leonard, Edward Cheskey, Megan McIntosh, Pat Kramer,
Cassandra Silverio, Lee Bakewell, Richard Doll, Myrna Pearman,
Alisha Ritchie, Bridget Stutchbury, and John Tautin. Funding
and support were provided by University of Manitoba, NSERC,
Nature Canada, Central Lakes College, Minnesota Audubon,
Minnesota Ornithologists’ Union, Brainerd Lakes Audubon
Society, Mille Lacs Band of Ojibwe, and Ellis Bird Farm.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.
2019.00324/full#supplementary-material
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2019 Fraser, Shave, de Greef, Siegrist and Garroway. This is an open-
access article distributed under the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or reproduction in other forums is permitted,
provided the original author(s) and the copyright owner(s) are credited and that the
original publication in this journal is cited, in accordance with accepted academic
practice. No use, distribution or reproduction is permitted which does not comply
with these terms.
Frontiers in Ecology and Evolution | www.frontiersin.org 7September 2019 | Volume 7 | Article 324
... Additionally, urban habitats may provide relatively stable refugia for urban exploiters to replace or subsidize habitat made unsuitable by climate change. Purple martins (Progne subis), for example, are increasing their use of urban areas for nesting and migratory staging (Bridge et al., 2016) and displaying phenotypically plastic migration timing in association with rising global temperatures (Fraser et al., 2019). The simultaneous effects of land use change and climate change can also be balancing; for example, in Danish avian communities, agricultural land use change decreases species abundances, while warmer winters increase species abundances (Bowler et al., 2018). ...
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... Variability is a hallmark of behavior and is observed across timescales (Tinbergen, 1951). On long timescales, variability has been studied in the migratory behavior of birds; birds display interindividual variability in migratory patterns, timing, and kinematics such as migratory speed (Potti, 1998;Trierweiler et al., 2014;Fraser et al., 2019;Phipps et al., 2019). On shorter timescales, many studies have looked at variability in movement kinetics, kinematics, and endpoints of reaching movements (Gordon et al., 1994;Messier and Kalaska, 1999;van Beers et al., 2004;Wu et al., 2014). ...
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... Whereas early research posited that characteristics of individual movements remained fixed (Farner, 1950), contemporary studies find that many animals alter F I G U R E 1 Key examples of efforts to restore lost migrations across four major vertebrate groups the timing, direction, and duration of yearly migrations in response to environmental fluctuations. Such flexibility occurs across diverse vertebrates including fish (Meager et al., 2018), birds (Fraser et al., 2019), mammals (Xu et al., 2021), and herpetofauna (Jourdan-Pineau et al., 2012). Perhaps more surprisingly, all taxonomic groups include some individuals that go so far as to alter-nate between migratory and nonmigratory behavior (e.g., striped bass [Morone saxatilis], Secor et al., 2020;wood storks [Mycteria americana], Picardi et al., 2020; spotted salamanders [Abystoma talpoideum], Kinkead & Otis, 2007;and elk, Eggeman et al., 2016). ...
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... Migrations between distant residency regions commonly occur in response to maintaining optimal thermal envelopes (Kessel et al., 2014;Payne et al., 2016Payne et al., , 2018, but are often associated with seeking out highly productive areas (i.e., high prey availability) (e.g., Jorgensen et al., 2010;Barnett et al., 2011) and areas for reproduction (Chapman et al., 2015). While population-level movement may appear predictable, certain species can show variability in migration timing among individuals and across years as a result of the dynamic environment they inhabit and their individual physiological needs (Brodersen et al., 2012;Fraser et al., 2019;Bauer et al., 2020). Defining animal residency and migration routes and variation in timing of movements consequently is essential to accurately delineate core space use for wildlife management. ...
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Changes in phenology and distribution are being widely reported for many migratory species in response to shifting environmental conditions. Understanding these changes and the situations in which they occur can be aided by understanding consistent individual differences in phenology and distribution and the situations in which consistency varies in strength or detectability. Studies tracking the same individuals over consecutive years are increasingly reporting migratory timings to be a repeatable trait, suggesting that flexible individual responses to environmental conditions may contribute little to population‐level changes in phenology and distribution. However, how this varies across species and sexes, across the annual cycle and in relation to study (tracking method, study design) and/or ecosystem characteristics is not yet clear. Here, we take advantage of the growing number of publications in movement ecology to perform a phylogenetic multilevel meta‐analysis of repeatability estimates for avian migratory timings to investigate these questions. Of 2,433 reviewed studies, 54 contained suitable information for meta‐analysis, resulting in 177 effect sizes from 47 species. Individual repeatability of avian migratory timings averaged 0.414 (95% confidence interval: 0.3–0.5) across landbirds, waterbirds and seabirds, suggesting consistent individual differences in migratory timings is a common feature of migratory systems. Timing of departure from the non‐breeding grounds was more repeatable than timings of arrival at or departure from breeding grounds, suggesting that conditions encountered on migratory journeys and outcome of breeding attempts can influence individual variation. Population‐level shifts in phenology could arise through individual timings changing with environmental conditions and/or through shifts in the numbers of individuals with different timings. Our findings suggest that, in addition to identifying the conditions associated with individual variation in phenology, exploring the causes of between‐individual variation will be key in predicting future rates and directions of changes in migratory timings. We therefore encourage researchers to report the within‐ and between‐ individual variance components underpinning the reported repeatability estimates to aid interpretation of migration behaviour. In addition, the lack of studies in the tropics means that levels of repeatability in less strongly seasonal environments are not yet clear.
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