Predicting Source Populations of Vagrants Using Breeding Population Data: A Case Study of the Lesser Black-Backed Gull (Larus fuscus)

Abstract

Vagrancy is critical in facilitating range expansion and colonization through exploration and occupation of potentially suitable habitat. Uncovering origins of vagrants will help us better understand not only species-specific vagrant movements, but how the dynamics of a naturally growing population influence vagrancy, and potentially lead to range expansion. Under the premise that occurrence of vagrants is linked to increasing population growth in the core of the breeding range, we assessed the utility of breeding population survey data to predict source populations of vagrants. Lesser Black-backed Gulls (LBBG) (Larus fuscus) served as our focal species due to their dramatic and well-documented history of vagrancy to North America in the last 30 years. We related annual occurrence of vagrants to indices of breeding population size and growth rate of breeding populations. We propose that the fastest growing population is the most likely source of recent vagrants to North America. Our study shows that it is possible to predict potential source populations of vagrants with breeding population data, but breeding surveys require increased standardization across years to improve models. For the Lesser Black-backed Gull, Iceland’s breeding population likely influenced vagrancy during the early years of colonization, but the major increase in vagrants occurred during a period of growth of Greenland’s population, suggesting that Greenland is the source population of the most recent pulse of vagrant LBBG to North America.

Full text

fevo-09-637452 November 30, 2021 Time: 13:55 # 1
ORIGINAL RESEARCH
published: 03 December 2021
doi: 10.3389/fevo.2021.637452
Edited by:
Karin Charlotta Harding,
University of Gothenburg, Sweden
Reviewed by:
Steven Carl Latta,
National Aviary, United States
Daniel Oro,
Center for Advanced Studies
of Blanes, Spanish National Research
Council (CSIC), Spain
*Correspondence:
Lucinda C. Zawadzki
lucinda.zawadzki@gmail.com
Specialty section:
This article was submitted to
Population, Community,
and Ecosystem Dynamics,
a section of the journal
Frontiers in Ecology and Evolution
Received: 03 December 2020
Accepted: 12 November 2021
Published: 03 December 2021
Citation:
Zawadzki LC, Hallgrimsson GT,
Veit RR, Rasmussen LM,
Boertmann D, Gillies N and Guilford T
(2021) Predicting Source Populations
of Vagrants Using Breeding
Population Data: A Case Study of the
Lesser Black-Backed Gull (Larus
fuscus). Front. Ecol. Evol. 9:637452.
doi: 10.3389/fevo.2021.637452
Predicting Source Populations of
Vagrants Using Breeding Population
Data: A Case Study of the Lesser
Black-Backed Gull (Larus fuscus)
Lucinda C. Zawadzki1*, Gunnar T. Hallgrimsson2, Richard R. Veit3,4,
Lars M. Rasmussen5, David Boertmann6, Natasha Gillies1and Tim Guilford1
1Department of Zoology, University of Oxford, Oxford, United Kingdom, 2Faculty of Life and Environmental Sciences,
University of Iceland, Reykjavik, Iceland, 3Department of Biology, College of Staten Island, Staten Island, NY, United States,
4City University of New York (CUNY) Graduate Center, New York, NY, United States, 5Greenland Institute of Natural
Resources, Nuuk, Greenland, 6Department of Ecoscience, Aarhus University, Roskilde, Denmark
Vagrancy is critical in facilitating range expansion and colonization through exploration
and occupation of potentially suitable habitat. Uncovering origins of vagrants will help us
better understand not only species-specific vagrant movements, but how the dynamics
of a naturally growing population influence vagrancy, and potentially lead to range
expansion. Under the premise that occurrence of vagrants is linked to increasing
population growth in the core of the breeding range, we assessed the utility of breeding
population survey data to predict source populations of vagrants. Lesser Black-backed
Gulls (LBBG) (Larus fuscus) served as our focal species due to their dramatic and well-
documented history of vagrancy to North America in the last 30 years. We related
annual occurrence of vagrants to indices of breeding population size and growth rate
of breeding populations. We propose that the fastest growing population is the most
likely source of recent vagrants to North America. Our study shows that it is possible
to predict potential source populations of vagrants with breeding population data, but
breeding surveys require increased standardization across years to improve models. For
the Lesser Black-backed Gull, Iceland’s breeding population likely influenced vagrancy
during the early years of colonization, but the major increase in vagrants occurred during
a period of growth of Greenland’s population, suggesting that Greenland is the source
population of the most recent pulse of vagrant LBBG to North America.
Keywords: vagrancy, range expansion, colonization, long-distance dispersal (LDD), source population, Lesser
black-backed gull
INTRODUCTION
Anthropogenic climate change continues to threaten species’ survival (Román-Palacios and Wiens,
2020), and species must remain flexible if they are to escape extinction driven by climate change.
Occupation of potentially suitable habitat through range expansion and colonization is one way in
which species can survive climatic effects. Vagrancy, a process by which organisms engage in long-
distance dispersal movements outside of their known species range (Grinnell, 1922;Baker, 1978),
may provide the mechanism through which individuals can explore and occupy potentially suitable
habitat. Though these movements have often been attributed to internal errors in navigation
Frontiers in Ecology and Evolution | www.frontiersin.org 1December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 2
Zawadzki et al. Predicting Source Populations of Vagrants
(Rabøl, 1969;DeSante, 1973;Cottridge and Vinicombe, 1996), or
passive displacement by wind or weather systems (Williamson,
1959;Elkins, 1979;McLaren, 1981;McLaren et al., 2006),
vagrancy is a natural part of mobile populations (Baker, 1978;
Hengeveld, 1989), and can result in range expansion (e.g., Veit
and Lewis, 1996;Massa et al., 2014) and colonization of new
habitat (e.g., Veit and Lewis, 1996;Veit et al., 2016). Vagrants,
however, are often difficult to study directly due to their inherent
rarity and unpredictable occurrence. In order to investigate the
role that vagrancy plays in range expansion and colonization,
we therefore need to study variability in this behavior through
a variety of methods.
It has been suggested that in order to naturally colonize
new habitat, a species must have a growing source population
(Hengeveld, 1989;Sz˝
ucs et al., 2014). Of the studies that have
examined factors that influence vagrancy (DeBenedictis, 1971;
DeSante, 1973;Hampton, 1997;Veit, 1990, 1997, 2000;Elkins,
1999;Thorup, 2004;McLaren et al., 2006;Pfeifer et al., 2007;
Jiguet et al., 2008;De Juana and Garcia, 2010;Farnsworth et al.,
2015;Ralph and Wolfe, 2018;Zawadzki et al., 2019), the majority
have found that vagrancy is strongly correlated with population,
either of the species’ overall population size (DeBenedictis, 1971;
DeSante, 1983;Thorup, 2004;Pfeifer et al., 2007;Ralph and
Wolfe, 2018), or annual variation in population size (Veit, 1990,
1997, 2000;McLaren et al., 2006;De Juana and Garcia, 2010;
Jiguet et al., 2008;Zawadzki et al., 2019). It has also been
found that increased incidence of vagrancy is linked to annual
population growth in the core of a species’ breeding range (Veit,
1997;McLaren et al., 2006;Zawadzki et al., 2019). Population
size and growth are therefore highly influential predictors when
estimating vagrant occurrence. Vagrancy is likely a density-
dependent phenomenon whereby increased productivity in a
given year leads to the production of more individuals than
the current habitat can support, leading to increased dispersal
(Southwood et al., 1974) and vagrancy (DeBenedictis, 1971;
DeSante, 1983;Patten and Marantz, 1996) to find newly suitable
habitat. Data on a species’ population size and growth will
be important in understanding range expansions, as colonizers
may be coming from regions that have experienced the most
rapid population growth, and may therefore be predisposed to
vagrancy (Phillips et al., 2010).
Using this information, we may be able to track colonization
of species undergoing range expansion, to determine where
vagrants are coming from, and may even be able to predict
which species are likely to occur as vagrants in the future.
Though tagging of individuals at known breeding sites through
either field-readable bands or GPS devices may provide more
direct evidence on individual movement, the likelihood that
any one bird tagged or banded will occur as a vagrant is
low. Recovery rates of banded passerines within their normal
range are already as low as 1.5% (North, 2020). Modeling with
long-term population data is thus vital in understanding range
expansion and colonization of vagrants.
Breeding population surveys of birds provide information
on annual breeding pairs at colonies or nesting-sites where
species are known to breed. Though protocol often vary by
country, data from these surveys provide long-term estimates of
population size and growth that may be useful for studying how
population dynamics in the breeding range influence vagrancy.
To examine the potential use of breeding population survey data
in determining source populations of vagrants, we investigated
the relationship between annual breeding population size and
growth rate of three known breeding populations of Lesser Black-
backed Gulls (L. fuscus; hereafter LBBG) in western Europe, and
the occurrence of vagrant LBBG in North America during the
years 1986–2018. LBBG are a unique case since they have a well-
documented history of vagrancy to North America, yet, as with
most vagrants, it is unknown where they are arriving from. We
predict that Greenland is the source population of vagrant LBBGs
to North America based on Greenland’s increasing population
after colonization, and proximity to North America.
MATERIALS AND METHODS
Study Species
Lesser Black-backed Gulls are a polytypic species whose breeding
range extends from Greenland to western Asia (Olsen and
Larsson, 2004). During the mid- to late-twentieth century, LBBGs
experienced a rapid increase in global population (Liebers and
Helbig, 2002;Olsen and Larsson, 2004), mainly attributed to
an increase in population growth of the Atlantic subspecies:
(1) intermedius, whose breeding range extends from Belgium
and Netherlands, to Norway, and (2) graellsii, which breeds
in Greenland and Iceland, along western Europe, south to
the Iberian Peninsula (Olsen and Larsson, 2004;Wetlands
International, 2020). As their populations increased, LBBGs
expanded their range westward across the Atlantic (Post and
Lewis, 1995), moving from breeding grounds in western Europe
to Iceland in the 1920s (Olsen and Larsson, 2004), and
subsequently colonizing Greenland between 1985 and 1990
(Boertmann, 2008). Iceland’s breeding population increased
from a 1,250 breeding pairs in 1974 to over 40,000 breeding
pairs in 2004 (Hallgrimsson et al., 2011). The colonization of
Greenland also rose rapidly, increasing from 13 records of non-
breeding individuals by 1984 (Boertmann, 2008), to an estimated
2,060 breeding pairs in 2016, the majority of which nest in
southwestern Greenland (Boertmann and Frederiksen, 2016;
Boertmann et al., 2020).
This rapid expansion shifted the LBBG breeding range closer
to North America, and was accompanied by increased numbers
of vagrant LBBGs on the continent. The first LBBG was recorded
in North America in 1934 (Edwards, 1935), and LBBG have now
been seen in every state and Canadian province (Figure 1;eBird,
2017), with over 1,000 individuals recorded annually since 2005
(National Audubon Society, 2020). LBBGs are mainly seen in
North America from September to March (Figure 2), though
sightings do occur year-round. Despite increasing occurrence
of LBBGs each year, they have yet to breed in North America
(with the exception of two hybrid pairs with Herring Gulls
(Larus argentatus); vanVliet et al., 1993;Ellis et al., 2007;Ellis
et al., 2014). This means that colonization of North America by
LBBGs is a result of repeated vagrancy by gulls arriving from
outside the continent.
Our study focuses on the Atlantic subspecies graellsii, which is
predominantly responsible for the westward range expansion of
Frontiers in Ecology and Evolution | www.frontiersin.org 2December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 3
Zawadzki et al. Predicting Source Populations of Vagrants
FIGURE 1 | eBird map of LBBG sightings in part of North America. The frequency is the percentage of submitted checklists from that region in which a LBBG was
recorded. Image provided by eBird (www.ebird.org) and created November 10, 2020.
LBBG across the Atlantic that coincided with the rapid increase
in global population during the mid- to late-twentieth century
(Olsen and Larsson, 2004;Sibley, 2014;Burger et al., 2020). The
other Atlantic subspecies intermedius was not involved in this
FIGURE 2 | Monthly totals of LBBG recorded in Massachusetts from the
journal Bird Observer between the years 1971–2018. LBBG are more
commonly seen from September to March.
range expansion, and the other three recognized subspecies,
fuscus,heuglini, and taimyrensis (Liebers and Helbig, 2002;
Collinson et al., 2008), are restricted to breeding and wintering
sites outside the Atlantic area (Cramp and Simmons, 1983;
Olsen and Larsson, 2004), and are very unlikely to have
contributed to these movements (Sibley, 2014).
Vagrant Data
We collected records of vagrant LBBGs in North America from
two sources. Numbers of wintering gulls (14 December to 5
January) were taken from Christmas Bird Count (CBC) data
(Figure 3;National Audubon Society, 2020) from 1986 to 2018.
All count circles with available data within the North American
continent were included, covering the contiguous United States,
all Canadian provinces, Central America (Mexico and Panama)
and the Caribbean (Bahamas, Bermuda, the Dominican Republic,
Haiti, and Puerto Rico). To correct for variation in observer
effort across years, data were extracted as CBC trend estimates of
median abundance (T. Meehan, pers. comm. 2020, Meehan et al.,
2020), which were calculated using Bayesian hierarchical models
(Soykan et al., 2016).
Additional year-round sighting records of gulls were extracted
from Bird Observer1, a Massachusetts-based journal, and used to
analyze ages of vagrant LBBG. Data were available from 1973
1Bird Observer, Arlington, MA, United States. Available online at: https://www.
birdobserver.org/Issues/Complete-Archive
Frontiers in Ecology and Evolution | www.frontiersin.org 3December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 4
Zawadzki et al. Predicting Source Populations of Vagrants
FIGURE 3 | Records of individual LBBG seen in North America during yearly Christmas Bird Counts (CBC) and from Bird Observer records from 1986 to 2018.
LBBG sightings increased rapidly after the early 1990s, and in the last decade, over 1,000 individuals have been present each year. CBC and Bird Observer records
are positively correlated with each other (r= 0.82, p<0.001).
to 2018. We chose this publication due to its intensive and
consistent record-keeping of birds sighted in the state throughout
the year (Veit, 1997), often with individuals identified to age.
Additionally, Massachusetts has a high concentration of LBBGs
each year (Veit and Petersen, 1993;Nisbet et al., 2013), and
is likely reflective of the pattern of sightings throughout North
America (Figure 3; correlation between CBC and Bird Observer
(see footnote 1) data: r= 0.82, p<0.001).
While eBird has a large collection of sighting records of
vagrant LBBG, we chose to use CBC and Bird Observer (see
footnote 1) data since data from these sources are available for
the entire time series of our study, and records are ensured
to be single individuals (Zawadzki et al., 2019). eBird was
not founded until 2002, therefore any sightings prior to this
year may not be available on the platform. Additionally, eBird
often reports multiple sightings for the same individual, and
there are no consistent methods to distinguish single birds
from multiple records. Further, standardization of protocol
used during CBCs ensures that vagrant data are consistent
across years.
We refrain from drawing an arbitrary line over whether each
particular LBBG in North America is a vagrant, but rather
define vagrancy as the process of birds moving outside of the
core of their species’ range, driven by growing populations
(DeBenedictis, 1971;DeSante, 1983;Patten and Marantz, 1996;
Veit, 1997, 2000;Zawadzki et al., 2019) and exploratory
movements (Grinnell, 1922;Baker, 1978,Baker, 1980). This
definition incorporates vagrants that become recurrent seasonal
visitors, and those vagrant individuals that travel to an area and
stay for their lifetime. Accordingly, all sightings of LBBG in
North America have been included in our analyses, including
individuals that may return annually each winter.
Breeding Population Data
Breeding population data were extracted from countries where
graellsii breed, i.e., the United Kingdom (hereafter, UK), Iceland,
and Greenland (Figure 4). UK data were taken from the Seabird
Monitoring Programme (SMP) (JNCC, 2020), which annually
monitors breeding seabird colonies in Britain and Ireland. Data
are recorded as numbers of apparently occupied nests (AON),
and an estimate of AON for each year is derived from these
counts (I. Win, pers. comm. 2020, JNCC, 2020). Data were
available from 1986 to 2018.
Iceland and Greenland do not have routine monitoring
programs, therefore information on breeding colonies came from
other sources. Population estimates from Iceland were obtained
by estimating the number of active nests at the breeding colony
of Midnesheidi, Reykjanes Peninsula in southwest Iceland, the
largest breeding colony in Iceland. We chose to only use data
from Midnesheidi because it is the only LBBG colony that has
been consistently surveyed in Iceland, and population trends
at this colony are likely representative of the overall breeding
population in the country (Hallgrimsson et al., 2006). The
addition of limited surveys of other colonies around Iceland
would only increase the estimates by a few hundred nests per year
(Hallgrimsson et al., 2006), which is within the 95% confidence
interval of the nest estimates at Midnesheidi. Estimates were
taken between the years 1990 and 2006. Nests were counted
within a sample of 4,000 m2plots within the colony, and the
number of plots surveyed each year ranged from 28 to 34.
Outlines of the whole colony were observed and marked on
a map, and the colony edge was observed from high points
using a telescope and by walking with a GPS unit. The edge
was determined through observations of nest defense by adults,
a standard means of determining breeding status of birds (e.g.,
Frontiers in Ecology and Evolution | www.frontiersin.org 4December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 5
Zawadzki et al. Predicting Source Populations of Vagrants
FIGURE 4 | Indices of annual breeding population size from 1986 to 2018 for (A) the UK, (B) Iceland (colony of Midnesheidi), and (C) Greenland (colony of Eqaluit),
and Christmas Bird Count (CBC) trend estimates of vagrants. Trend estimates are calculated from CBC surveys as estimates of median abundance, using Bayesian
hierarchical methods (Soykan et al., 2016;Meehan et al., 2020). Normalized values were obtained by dividing each value in a given dataset by the maximum value of
that dataset.
Mitchell et al., 2004). The colony area was then calculated using
global information system (GIS; Esri Inc, 2008, ArcMapTM 9.3).
To calculate the mean density, and 95% confidence limits of
active nests, we used the program NEGBINOM (Krebs, 1999).
The size of the breeding population was found by multiplying the
density by the area.
Greenland data were collected from the Greenland Seabird
Colony Register. These data consisted of a series of sightings
and surveys conducted across Greenland between 1986 and 2018.
Data prior to 1990 were excluded from our analysis since the
first confirmed case of breeding was not until 1990. Due to
inconsistent survey efforts across Greenland, we used data from
the most consistently surveyed colony of Eqaluit in southwest
Greenland to represent breeding populations across Greenland.
The first evidence of breeding LBBG was at Eqaluit in 1990,
and Eqaluit has been surveyed 12 times between 1990 and 2018.
Counts of LBBG were recorded as either individuals, pairs, or
nests. A total pair count was calculated for each year, using the
formula: pairs in year t+nests in year t+(individuals in year
t)×0.7, where 0.7 is the kvalue used to convert individuals to
pairs (Harris et al., 2015).
Breeding data from all populations were converted to indices
for model analysis. Indices were calculated as percentages relative
to the base-year (first year of monitoring), which was set to 100%
(Thomas, 1993). Percentages were divided by 100 to derive an
index value. Growth rates (r) for each population were calculated
as r= ln(λ).
Model Analysis
Generalized Linear Models
We constructed generalized linear models (GLMs) for each
breeding population to estimate the relationship between
numbers of vagrants in North America (as trend estimates
from CBC data), and indices of annual breeding population
size and annual growth rate (r). We constrained our models to
1986 to 2018, when range expansion to Greenland and North
America occurred. We formulated four competitive GLMs,
including a null (no predictors). Models were ranked using
Akaike information criterion (AIC) comparison, with AIC values
corrected for small sample sizes (AICc) using function aictab
from the package “AICcmodavg” (Mazerolle, 2020). The model
with the lowest AICc value was chosen as the best model if
it was at least two AICc values lower than the next most
competitive model (Burnham and Anderson, 2003). All analyses
were conducted using R (R Core Team, 2019).
Generalized Additive Models
Due to the non-linear trajectory of population count data,
we also constructed generalized additive models (GAMs) for
each breeding population to estimate the relationship between
numbers of vagrants in North America (as trend estimates
Frontiers in Ecology and Evolution | www.frontiersin.org 5December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 6
Zawadzki et al. Predicting Source Populations of Vagrants
from CBC data), and indices of annual breeding population
size. Growth rates (r) were not included in these models due
to insufficient sample sizes to include additional smoothing
parameters. GAMs are much better at dealing with variability
in count data due to the non-linear estimates calculated (Wood,
2006;Knape, 2016), and are often used to estimate changes
in population over time (Knape, 2016). Our GAMs were
constrained to the same timeframe as our GLMs. A total of
four models were constructed, including a null (no explanatory
variables), using the package “mgcv” in R (Wood, 2017). We
used a negative binomial distribution of errors to correct for
overdispersion in our data (Lindén and Mäntyniemi, 2011).
Models were ranked using AIC comparison using the function
model.sel from package “MuMIn” (Barto´
n, 2020) to determine
which model best fit our data. All analyses were conducted using
R (R Core Team, 2019).
RESULTS
Generalized Linear Models
Our most competitive model was the model for Greenland’s
breeding population (Table 1). Occurrence of vagrancy was
positively correlated with both Greenland’s index of population
size and growth rate, albeit not significantly (Table 1). The
model for Iceland competed with the model for Greenland
as the most competitive model, differing in AICc value by
only 1.25. Iceland’s index of population size and growth rate
were positively correlated with vagrancy, of which the index of
population size was significantly correlated with vagrancy. UK
breeding populations were significantly inversely related with
vagrant occurrence (Table 1), and were the least competitive
models alongside the null models.
Generalized Additive Models
Our most competitive GAM was the model for Iceland’s
breeding population (Table 2). Plots of this relationship indicate
that Icelandic breeding populations seem to influence vagrant
occurrence at two extremes (Figure 5B). When Icelandic
populations are low or high, vagrants are abundant in North
America. However, when Icelandic populations are steady,
numbers of vagrants in North America are low. On the other
hand, our GAM for Greenland’s breeding population showed
a direct positive relationship between breeding population size
and occurrence of vagrants in North America (Figure 5C),
indicating occurrence of vagrants increases with increasing
breeding population size in Greenland. UK breeding populations
were inversely correlated with vagrancy (Figure 5A), and were
the least competitive models alongside the null models.
DISCUSSION
We conclude that it is possible to predict potential source
populations of vagrants using breeding population data. Our
GLMs and GAMs for each breeding population modeled
occurrence of vagrants better than the null model (Tables 1,2).
However, there are limitations present in this type of analysis if
survey efforts are inconsistent or incomplete during the breeding
season. For LBBG, the source population was likely derived from
breeding populations in both Greenland and Iceland, though
Greenland is most likely the source of the recent (since 2000)
surge of vagrants to North America. The model that related
Greenlandic populations to occurrence of vagrants was our most
competitive model for our GLMs, while the model that related
Icelandic populations to occurrence of vagrants was our most
competitive model for our GAMs. While we acknowledge that
other unknown or untested factors could also explain vagrancy,
these are secondary to our study since we are focused on testing
whether breeding population data can be used to predict a
plausible source population of vagrants under the premise that
population growth drives vagrancy (Patten and Marantz, 1996;
Ralph and Wolfe, 2018;Zawadzki et al., 2019).
The ability to predict source populations of vagrants through
breeding data alone is invaluable to studies on vagrancy, and will
be widely applicable to a variety of vagrant species. Vagrants are
difficult to study directly due to their inherent rarity, and have
been seldom studied as a result. Having a methodology available
to be able to study vagrants indirectly will increase the possibility
for research in this area. This is particularly true of short-lived
passerines, which are often too small for direct studies on their
movement, such as through GPS-tracking. Further, this strong
relationship between population and occurrence of vagrants has
important implications for the role that vagrancy plays in both
range expansion and colonization of species. Range expansion
and/or colonization are a likely result of vagrancy, and studies
on population dynamics of species can provide inference into
species that are more likely to expand their range in the future
(e.g., Jiguet and Barbet-Massin, 2013). Since population dynamics
are also tied to a species’ habitat, it is imperative that we explore
how habitat change influences vagrancy through its continued
effect on population (DeBenedictis, 1971;DeSante, 1983;Patten
and Marantz, 1996).
Source Population of Lesser
Black-Backed Gulls
Iceland’s breeding population was likely important during early
years of colonization in North America (either directly or
indirectly; Figure 5B), prior to its stark decline in 2005 (82%
decline between 2004 and 2006). Early colonization of North
America coincided with an increase in both the Icelandic
and Greenlandic breeding populations (Figure 4). It has been
proposed that Greenland’s breeding population was founded by
Icelandic gulls between 1986 and 1990 (Boertmann, 2008). It is
therefore possible that some vagrant LBBG in North America
originated from Iceland prior to their decline in 2005, either
directly from Iceland, or through colonization of Greenland and
subsequent migration to North America, though any records
of LBBG in North America prior to 1990 must have derived
from other populations since a breeding population was not
yet established in Greenland. Nevertheless, it is unambiguous
that the major increase of vagrant LBBG to North America
occurred during a period of growth of the Greenland population
(Figure 4). Greenland’s population has been significantly
influential across the entire time series (Figure 5C).
Frontiers in Ecology and Evolution | www.frontiersin.org 6December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 7
Zawadzki et al. Predicting Source Populations of Vagrants
TABLE 1 | Parameter estimates for univariate generalized linear models (GLMs) of the relationship between trend estimates of vagrant LBBG occurrence in North
America from CBC data and indices of annual breeding population size and growth rate (r) of the breeding population in the UK, Iceland, and Greenland.
Population Population size p-value Growth rate (r)p-value n1AICc AICc weight Adj. R2
Greenland 0.13 0.08 0.36 0.53 12 0.00 0.65 0.20*
Iceland 2.11 0.03 −0.74 0.06 7 1.25 0.35 0.88
UK −5.68 <0.001 −4.88 0.02 33 89.82 0.00 0.63
Null − − − − 33 131.56 0.00 n/a
Models were constrained to the years 1986–2018. The best model was selected based on the lowest AICc value. Effect sizes are listed for each predictor.
*Best model as selected based on the lowest AICc value.
Bold-faced p-values are significant (i.e. p < 0.05).
TABLE 2 | Model selection for generalized additive models (GAMs) of the relationship between trend estimates of vagrant LBBG occurrence in North America from CBC
data and indices of annual breeding population size and growth rate (r) of the breeding population in the UK, Iceland, and Greenland.
Population Population size pGrowth rate (r)pDeviance (%) k n 1AICc Adj. R2
Iceland 0.64 0.42 0.22 0.64 41.3 4 6 0.00 0.87*
Greenland 1.22 0.27 0.20 0.66 28.9 6 11 15.02 0.05
UK 11.15 <0.01 1.41 0.23 64.5 33 32 102.68 0.88
Null − − − − 0.0 – 33 122.27 n/a
Models were constrained to the years 1986–2018. GAMs were run with negative binomial errors. The best model was selected based on the lowest AICc value. Effect
sizes are listed for each predictor.
*Best model as selected based on the lowest AICc value.
Bold-faced p-values are significant (i.e. p < 0.05).
Recent tracking efforts by Pennsylvania’s (PA) Game
Commission confirm this link (Barber et al., in press). Barber
et al. (in press) affixed 9 wintering vagrant LBBG in Pennsylvania
with GPS devices, and discovered that five of these individuals
traveled to Greenland in the summer for two consecutive
migrations. Furthermore, a noticeable “jump” in the arrival
of first calendar year to third calendar year birds occurred in
Massachusetts and Rhode Island in 2005–2010 [Bird Observer
(see footnote 1), eBird, 2017], and again in 2018–2021, including
500 immatures (<2 years old) at Fire Island, New York. Due to
absence of breeding in North America, these birds must derive
from a rapidly growing colony elsewhere. Therefore, our premise
that increasing source populations are producing large numbers
of vagrants is supported. Peaks of immature gulls in North
America also coincide with peaks in breeding population size of
Greenland LBBG (Supplementary Figure 1).
The large number of unbanded gulls in North America also
indicates that they are arriving from locations where graellsii
remain unbanded, such as colonies in western Iceland and
Greenland. In spite of considerable color-banding effort in
Iceland, Netherlands, and the British Isles, only two banded gulls
have been re-sighted in North America: (1) a juvenile gull banded
in Netherlands that was spotted as an adult in Long Island,
New York on 7 October 1997, and (2) a first-winter gull from
southwestern Iceland, that was seen during its first winter in
Puerto Rico on 16 and 20 November 2002 (Hallgrimsson et al.,
2011). No other re-sightings have been reported even though
thousands of LBBG are seen in North America each year.
Our models also suggest that vagrant LBBG do not originate
from the UK, and vagrancy is inversely correlated with UK LBBG
populations (Table 1 and Figure 5A). UK breeding populations
have declined rapidly since 2000 (Figure 4A), as a result of
increased culling practices, and changes to landfill and fishing
practices (Ross-Smith et al., 2014a,b;Nager and O’Hanlon, 2016).
This rapid decline in UK breeders at a time when vagrants were
increasing makes it unlikely that vagrant gulls originate from UK
colonies. Additionally, decadal censuses of wintering gulls have
found that UK-breeding LBBG are wintering more frequently
in the UK (Burton et al., 2003, 2013;Banks et al., 2009;Ross-
Smith et al., 2015), rather than migrating to southwest Europe
and northwest Africa (Hallgrimsson et al., 2012). Since UK LBBG
show high wintering site fidelity (Thaxter et al., 2012), increased
residency of UK LBBG further decreases the likelihood that
North American vagrants originate from UK colonies.
Age of Vagrant Lesser Black-Backed
Gulls
It has often been speculated that the recent influx of LBBG
to North America is a result of breeding on the continent,
rather than repeated instances of vagrancy. These breeding claims
lack support. Only two instances of breeding have ever been
confirmed in North America, and both cases were hybridizations
between a LBBG and a Herring Gull (Larus argentatus)—one
nesting pair in Juneau, Alaska in 1993 (vanVliet et al., 1993),
and another pair on Appledore Island, Maine from 2007 to
present, which has since fledged five hybrid chicks (Ellis et al.,
2007, 2014). Additionally, despite the presence of some breeding
plumaged adults during summer for nearly two decades, they
have not been seen visiting breeding habitats, even though
LBBG are known to breed in mixed gull colonies (Camphuysen,
2011). The majority of vagrant LBBG seen in North America
are juveniles [Bird Observer (see footnote 1); Supplementary
Figure 2A], particularly first calendar year birds (Supplementary
Frontiers in Ecology and Evolution | www.frontiersin.org 7December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 8
Zawadzki et al. Predicting Source Populations of Vagrants
FIGURE 5 | Trends between annual breeding population size and numbers of vagrants using GAMs. The black line indicates the trend of the model, and the gray
lines represent the lower and upper 95% confidence intervals. The graphs are allocated as follows: (A) CBC vagrants ∼UK pairs, (B) CBC vagrants ∼Iceland pairs,
(C) CBC vagrants ∼Greenland pairs. CBC vagrants are calculated as trend estimates from CBC surveys, which are an estimate of median abundance, using
Bayesian hierarchical methods (Soykan et al., 2016;Meehan et al., 2020). Breeding pair indices were calculated as the percent change in total breeding pairs in that
year relative to the base-year (first year of monitoring), which was set to 100%. Percentages were divided by 100 to create an index.
Figure 2B), and adults are mainly seen outside of the breeding
season (Supplementary Figure 3), making breeding unlikely.
Baker (1980) proposed that LBBG follow an exploratory
migration model, whereby young birds explore during the first
18 months after fledging, and areas that are found to be
more suitable for overwintering will facilitate a change in their
migratory behavior as adults. Tracking studies of immature LBBG
also show that pre-breeding LBBG are more prone to these pre-
migratory and post-migratory dispersal movements (Pütz et al.,
2007, 2008;Camphuysen, 2011). This coincides with the age
profile we see in North America, where younger birds are seen
throughout the year, while adult birds are mainly present during
the winter season.
Methodological Constraints
Our analysis did pose limitations due to inconsistent survey
efforts during breeding. For LBBG, while surveys in the UK
are annually consistent (JNCC, 2020), survey efforts in Iceland
and Greenland vary widely from year to year, and many years
are missing from the dataset. Furthermore, in Greenland, the
same colonies are not surveyed each year, creating between-
year variation that is not representative of the actual size of
the breeding population (Boertmann and Frederiksen, 2016;
Boertmann et al., 2020), and could only be resolved by limiting
analyses to one colony (which itself was under-surveyed; n= 12;
Supplementary Tables 1, 2). These irregularities constrained
our models since we only had small sample sizes to work with.
Despite these limitations, we feel that the data available faithfully
identify the periods of maximum growth for each of these
populations, though there is room for improvement in collecting
future datasets.
Long-term, consistent, and systematic breeding bird surveys
are necessary to more accurately assess patterns of vagrant
occurrence and establishment of vagrant colonies. Such surveys
do exist in a number of countries for other species [e.g.,
North American Breeding Bird Survey (Pardieck et al., 2020),
SMP (JNCC, 2020), Netherlands Ecological Monitoring Network
(Sovon, 2019), and many others], but this is not the case
globally, particularly in areas of the globe that are less accessible.
Furthermore, species that are secretive or classified as pests
(many gulls) may be overlooked, even in countries where robust
breeding survey efforts are in place. Annual study plots with
standardized protocol for each species (where possible) should
be the aim, and would benefit not only future studies on LBBG
Frontiers in Ecology and Evolution | www.frontiersin.org 8December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 9
Zawadzki et al. Predicting Source Populations of Vagrants
vagrancy, but on vagrancy and population dynamics as a whole.
For species in which frequent surveys are not possible, modeling
could be supplemented by other field methods, such as tracking
of vagrant individuals to their breeding/summering grounds
with GPS devices, or stable isotope analysis to determine the
natal origin of vagrant individuals (De Jong et al., 2019), but
both of these methods pose additional problems themselves
since vagrants are hard to catch, and isoscapes (for stable
isotope analysis) are not as well-defined across Europe (Hobson
et al., 2004). Improving survey efforts of native breeders would
be the best way to improve studies of vagrancy since these
studies often require indirect means of analysis. Furthermore,
from an analytical perspective, statistical approaches must be
carefully considered to improve our understanding of population
dynamics of vagrants. For example, GAMs may provide a
more robust alternative to GLMs when accounting for temporal
variation in count data, and are increasingly becoming the norm
when modeling changes in populations over time (Knape, 2016).
CONCLUSION
Our study shows that data on breeding populations can be used
to determine plausible source populations of vagrants, but the
fit of these models will be greatly improved with standardized
survey efforts at breeding sites, and implementation of GAMs
over GLMs for count data. For LBBG, Greenland and Iceland
have influenced the increase in vagrant LBBG to North America.
While Iceland may have contributed to vagrancy in early years of
colonization, Greenland populations have consistently increased
alongside numbers of vagrants, suggesting Greenland is the
source population of vagrant LBBG. We predict that within the
next few decades LBBG will occur regularly enough in North
America to be considered an established wintering population,
and, following Boertmann’s (2008) predictions, may even
establish a small breeding population. Future studies of vagrant
LBBG should incorporate GPS-tracking of wintering gulls in
North America to their breeding/summering grounds to verify
the results of our model analysis, and uncover the migratory
routes of North American LBBG. Stable isotope analyses and
mitochondrial DNA studies (Liebers and Helbig, 2002) may also
help to directly elucidate the origin of vagrant LBBG.
DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included
in the article/Supplementary Material, further inquiries can be
directed to the corresponding author.
AUTHOR CONTRIBUTIONS
LZ compiled available breeding population and vagrant data,
designed the models and analyzed the data, and wrote the
manuscript with input from all authors (GH, RV, LM, DB, NG,
TG). GH collected Iceland data in the field. LR and DB collected
Greenland data in the field. RV suggested the topic, and assisted
LZ with collection and processing of the data. NG, TG, and
RV aided LZ in analysis and interpretation of the models. TG
supervised the project. All authors contributed to the article and
approved the submitted version.
FUNDING
Monitoring at Midnesheidi was financially supported by the
ISAVIA Keflavik Airport authorities.
ACKNOWLEDGMENTS
We would like to thank all that have helped with the completion
of this project. Flemming Merkel answered many of our
questions about Greenland data during the early stages of
analyses, Ilka Win at the JNCC provided data for UK LBBG
and helped us understand the dataset, and Tim Meehan and
Geoff LeBaron at Audubon assisted with interpretation of
CBC data. We thank Agnar Ingolfsson and Pall Hersteinsson
who started the count of Icelandic gulls at Midnesheidi, and
introduced the survey to GH. We would also like to thank
Karin Harding and four reviewers whose constructive comments
and input helped greatly improve our manuscript. Furthermore,
many thanks to the various nature conservations, research
organizations, and volunteers who collected data on LBBG in
the UK (through the SMP), Iceland and Greenland, as well
as the compilers for both Christmas Bird Counts and Bird
Observer (see footnote 1). And the utmost thanks to the dedicated
birders across North America whose participation in Christmas
Bird Counts and lone efforts continue to help us document
vagrancy in action.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.2021.
637452/full#supplementary-material
REFERENCES
Baker, R. R. (1978). The Evolutionary Ecology of Animal Migration. New York, NY:
Holmes and Meier Publishers.
Baker, R. R. (1980). The significance of the Lesser black-backed gull to models of
bird migration. Bird Study 27, 41–50. doi: 10.1080/00063658009476655
Banks, A. N., Burton, N. H. K., Calladine, J. R., and Austin, G. E. (2009). Indexing
winter gull numbers in great britain using data from the 1953 to 2004 winter
gull roost surveys. Bird Study. 56, 103–109. doi: 10.1080/00063650802681623
Barber, et al. (in press). Summer Locations of LBBG (L. fuscus) Wintering in PA.
Barto´
n, K. (2020). MuMIn: Multi-Model Inference. R Package Version 1.43.17.
Available online at: https://CRAN.R-project.org/package=MuMIn.
Boertmann, D. (2008). The lesser black-backed gull, Larus fuscus, in Greenland.
Arctic 61, 129–133. doi: 10.14430/arctic17
Boertmann, D., and Frederiksen, M. (2016). Status of Greenland populations of
great black-backed gull (Larus marinus), lesser black-backed gull (Larus fuscus)
and herring gull (Larus argentatus). Waterbirds 39, 29–35. doi: 10.1675/063.
039.sp109
Frontiers in Ecology and Evolution | www.frontiersin.org 9December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 10
Zawadzki et al. Predicting Source Populations of Vagrants
Boertmann, D., Merkel, F., and Gilg, O. (2020). Seabird breeding colonies in East
and North Greenland: a baseline. Arctic 73, 20–39. doi: 10.14430/arctic69885
Burger, J., Gochfeld, M., Kirwan, G. M., Christie, D. A., and de Juana, E. (2020).
“Lesser black-backed gull (Larus fuscus), version 1.0,” in Birds of the World, eds
J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie, and E. de Juana (Ithaca, NY:
Cornell Lab of Ornithology). doi: 10.2173/bow.lbbgul.01
Burnham, K. P., and Anderson, D. R. (2003). Model Selection and Multimodel
Inference: A Practical Information-Theoretic Approach. 2nd Edn. New York, NY:
Springer-Verlag.
Burton, N. H. K., Banks, A. N., Calladine, J., and Austin, G. E. (2013). The
importance of the United Kingdom for wintering gulls: population estimates
and conservation requirements. Bird Study 60, 87–101. doi: 10.1080/00063657.
2012.748716
Burton, N. H. K., Musgrove, A., Rehfisch, M. M., Sutcliffe, A., and Waters, R.
(2003). Numbers of wintering gulls in the United Kingdom, Channel Islands,
and Isle of man: a review of the 1993 and previous winter gull roost surveys. Br.
Birds 96, 376–401.
Camphuysen, C. J. (2011). Lesser Black-Backed Gulls Nesting at Texel: Foraging
Distribution, Diet, Survival, Recruitment and Breeding Biology of Birds Carrying
Advanced GPS Loggers. NIOZ-Report 2011-05. Texel: Royal Netherlands
Institute for Sea Research.
Collinson, J. M., Parkin, D. T., Knox, A. G., Sangster, G., and Svensson, L. (2008).
Species boundaries in the herring and lesser black-backed gull complex. Br.
Birds. 101, 340–363.
Cottridge, D., and Vinicombe, K. (1996). Rare Birds in Britain and Ireland - A
Photographgic Record. London: Harper Collins.
Cramp, S., and Simmons, K. E. L. (eds) (1983). The Birds of the Western Palearctic,
Vol. 3. Oxford: Oxford University Press.
De Jong, A., Torniainen, J., Bourski, O. V., Heim, W., and Edenius, L. (2019).
Tracing the origin of vagrant Siberian songbirds with stable isotopes: the case
of the yellow-browed warbler (Abrornis inornatus) in fennoscandia. Ornis Fenn
96, 90–99.
De Juana, E., and Garcia, E. F. J. (2010). Vagrancy or migration: why do american
teals cross the atlantic? Ardeola 57, 417–430.
DeBenedictis, P. (1971). Wood warblers and vireos in California: the nature of the
accidental. Calif. Birds 2, 111–128.
DeSante, D. F. (1973). An Analysis of the Fall Occurrences and Nocturnal
Orientations of Vagrant Wood Warblers (Parulidae) in California. PhD thesis.
Stanford, CA: Stanford University.
DeSante, D. F. (1983). Annual variability in the abundance of migrant landbirds on
Southeast Farallon Island. California. Auk 100, 826–852. doi: 10.1093/auk/100.
4.826
eBird (2017). eBird: An Online Database of Bird Distribution and Abundance [Web
Application]. Ithaca, NY: Cornell Lab of Ornithology.
Edwards, J. L. (1935). The lesser black-backed gull in New Jersey. Auk 52:85.
doi: 10.2307/4077132
Elkins, N. (1979). Nearctic landbirds in Britain and Ireland: a meterological
analysis. Br. Birds. 72, 417–433.
Elkins, N. (1999). Recent records of Nearctic landbirds in Britain and Ireland.
Br. Birds 92, 83–95. Available online at: https://britishbirds.co.uk/content/
recent-records- nearctic-landbirds- britain-and- ireland
Ellis, J. C., Bogdanowicz, S. M., Stoddard, M. C., and Clark, L. W. (2014).
Hybridization of a lesser black-backed gull and herring gulls in eastern North
America. Wilson J. Ornithol. 126, 338–345. doi: 10.1676/13-095.1
Ellis, J. C., Stoddard, M. C., and Clark, L. W. (2007). Breeding by a lesser black-
backed gull (Larus fuscus) on the Atlantic coast of North America. North Am.
Birds 61, 546–548.
Esri Inc (2008). ArcMap (Version 9.3). Esri Inc. Available online at: https://desktop.
arcgis.com/en/arcmap/ (accessed 2018).
Farnsworth, A., La Sorte, F. A., and Iliff, M. J. (2015). Warmer summers and
drier winters correlate with more winter vagrant Purple Gallinules (Porphyrio
martinicus) in the North Atlantic Region. Wilson J. Ornithol. 127, 582–592.
doi: 10.1676/14-086.1
Grinnell, J. (1922). The role of the “accidental.” Auk 39, 373–380. doi: 10.2307/
4073434
Hallgrimsson, G. T., Gunnarsson, H. V., Torfason, O., Buijs, R.-J., and
Camphuysen, K. C. J. (2012). Migration pattern of Icelandic lesser black-backed
gulls Larus fuscus graellsii: indications of a leap-frog system. J. Ornithol. 153,
603–609. doi: 10.1007/s10336-012- 0816-4
Hallgrimsson, G. T., Gunnarsson, H., and Hersteinsson, P. (2006). Stærð
sílamáfsvarps á Álftanesi á Mýrum [Size of the Lesser Black-backed
Gull colony at Álftanes on Mýrar (W-Iceland) in 2005]. Bliki 27,
55–57.
Hallgrimsson, G. T., van Swelm, N. D., Gunnarsson, H. V., Johnson, T. B., and
Rutt, C. L. (2011). First two records of Europe-banded lesser black-backed gulls
Larus fuscus in America. Mar. Ornithol. 39, 137–139.
Hampton, S. (1997). Rare migrants in California: the determinants of their
frequency. West. Birds 28, 30–42.
Harris, M. P., Heubeck, M., Newell, M. A., and Wanless, S. (2015). The need for
year-specific correction factors (k values) when converting counts of individual
common guillemots uria aalge to breeding pairs. Bird Study 62, 276–279. doi:
10.1080/00063657.2015.1017444
Hengeveld, R. (1989). Dynamics of Biological Invasions. London: Chapman and
Hall.
Hobson, K. A., Bowen, G. J., Wassenaar, L. I., Ferrand, Y., and Lormee, H. (2004).
Using stable hydrogen and oxygen isotope measurements of feathers to infer
geographical origins of migrating European birds. Oecologia 141, 477–488.
doi: 10.1007/s00442-004- 1671-7
Jiguet, F., and Barbet-Massin, M. (2013). Climate change and rates of vagrancy
of Siberian bird species to Europe. IBIS 155, 194–198. doi: 10.1111/ibi.1
2001
Jiguet, F., Doxa, A., and Robert, A. (2008). The origin of out-of-range pelicans in
Europe: wild bird dispersal or zoo escapes? Ibis 150, 606–618. doi: 10.1111/j.
1474-919X.2008.00830.x
JNCC (2020). Seabird Population Trends and Causes of Change: 1986-2018 Report.
[Online]. Peterborough: Joint Nature Conservation Committee.
Knape, J. (2016). Decomposing trends in Swedish bird populations using
generalized additive mixed models. J. Appl. Ecol. 53, 1852–1861. doi: 10.1111/
1365-2664.12720
Krebs, C. (1999). Ecological Methodology. Menlo Park, CA: Benjamin Cummings.
Liebers, D., and Helbig, A. J. (2002). Phylogeography and colonization history
of lesser black-backed gulls (Larus fuscus) as revealed by mtDNA sequences.
J. Evol. Biol. 15, 1021–1033. doi: 10.1046/j.1420-9101.2002.00454.x
Lindén, A., and Mäntyniemi, S. (2011). Using the negative binomial distribution
to model overdispersion in ecological count data. Ecoloy 92, 1414–1421. doi:
10.1890/10-1831.1
Massa, C., Doyle, M., and Fortunato, R. C. (2014). On how cattle egret
(Bubulcus ibis) spread to the Americas: meteorological tools to assess probable
colonization trajectories. Int. J. Biometeorol. 58, 1879–1891. doi: 10.1007/
s00484-014-0790-z
Mazerolle, M. J. (2020). AICcmodavg: Model Selection and Multimodel Inference
Based On (Q)AIC(c). R Package Version 2.3-1.
McLaren, I. A. (1981). The incidence of vagrant landbirds on Nova Scotian islands.
Auk 98, 243–257.
McLaren, I. A., Lees, A. C., Field, C., and Collins, K. J. (2006). Origins and
characteristics of Nearctic landbirds in Britain and Ireland in autumn: a
statistical analysis. IBIS 148, 1–20. doi: 10.1111/j.1474-919X.2006.00574.x
Meehan, T. D., LeBaron, G. S., Dale, K., Krump, A., Michel, N. L., and Wilsey,
C. B. (2020). Abundance Trends of Birds Wintering in the USA and Canada,
From Audubon Christmas Bird Counts, 1966-2019, Version 3.0. New York, NY:
National Audubon Society.
Mitchell, P. I., Newton, S. F., Ratcliffe, N., and Dunn, T. E. (2004). Seabird
Populations of Britain and Ireland. London: T. & AD Poyser.
Nager, R. G., and O’Hanlon, N. J. (2016). Changing numbers of the three gull
species in the British Isles. Waterbirds. 39, 15–28. doi: 10.1186/s12862-015-
0484-0
National Audubon Society (2020). The Christmas Bird Count Historical Results
[Online]. Available online at: http://www.christmasbirdcount.org (accessed
July 14, 2020).
Nisbet, I. C., Veit, R. R., Auer, S. A., and White, T. P. (2013). Marine birds of the
eastern United States and the bay of fundy. Nuttall Ornithol. Monogr. 29:188.
doi: 10.1371/journal.pone.0194389
North, M. R. (2020). Significant recoveries of banded birds. North Am. Bird Bander.
45, 130–134.
Frontiers in Ecology and Evolution | www.frontiersin.org 10 December 2021 | Volume 9 | Article 637452

fevo-09-637452 November 30, 2021 Time: 13:55 # 11
Zawadzki et al. Predicting Source Populations of Vagrants
Olsen, K. M., and Larsson, H. (2004). Gulls of North America, Europe and Asia.
Princeton: Princeton University Press.
Pardieck, K. L., Ziolkowski, D. J. Jr., Lutmerding, M., Aponte, V. I., and Hudson,
M.-A. R. (2020). North American Breeding Bird Survey Dataset 1966 - 2019:
U.S. Geological Survey Data Release. Reston, VA: U.S. Geological Survey, doi:
10.5066/P9J6QUF6
Patten, M. A., and Marantz, C. A. (1996). Implications of vagrant southeastern
vireos and warblers in California. Auk 113, 911–923. doi: 10.2307/408
8868
Pfeifer, R., Stadler, J., and Brandl, R. (2007). Birds from the Far East in Central
Europe: a test of the reverse migration hypothesis. J. Ornithol. 148, 379–385.
doi: 10.1007/s10336-007- 0140-6
Phillips, B. L., Brown, G. P., and Shine, R. (2010). Evolutionarily accelerated
invasions: the rate of dispersal evolves upwards during the range advance of
cane toads. J. Evol. Biol. 23, 2595–2601. doi: 10.1111/j.1420-9101.2010.02118.x
Post, P. W., and Lewis, R. H. (1995). The lesser black-backed gull in the
americas: occurrence and subspecific identity. Part I: Taxonomy, distribution,
and migration. Birding 27, 282–290.
Pütz, K., Helbig, A. J., Pedersen, K. T., Rahbek, C., Saurola, P., and Juvaste, R.
(2008). From fledging to breeding: long-term satellite tracking of the migratory
behaviour of a Lesser Black-backed Gull Larus fuscus intermedius.Ringing Migr.
24, 7–10. doi: 10.1080/03078698.2008.9674376
Pütz, K., Rahbek, K. C., Saurola, P. L., Pedersen, K. T., Juvaste, R., and Helbig, A. J.
(2007). Satellite tracking of the migration pathways of first-year LBBGs Larus
fuscus departing from the breeding grounds of different subspecies. Vogelwelt
128, 141–146.
R Core Team (2019). R: A Language and Environment for Statistical Computing.
Vienna: R Foundation for Statistical Computing.
Rabøl, J. (1969). Reversed migration as a cause of westward vagrancy by four
Phylloscopus warblers. Br. Birds 62, 89–92.
Ralph, C. J., and Wolfe, J. D. (2018). Factors affecting the distribution and
abundance of autumn vagrant New World warblers in northwestern California
and southern Oregon. PeerJ. 6:e5881. doi: 10.7717/peerj.5881
Robbins, C. S. (1980). Predictions of future Nearctic landbird vagrants to Europe.
Br. Birds 73, 448–457.
Román-Palacios, C., and Wiens, J. J. (2020). Recent responses to climate change
reveal the drivers of species extinction and survival. Proc. Natl. Acad. Sci. U. S. A.
117, 4211–4217. doi: 10.1073/pnas.1913007117
Ross-Smith, V. H., Grantham, M. J., Robinson, R. A., and Clark, J. A. (2014a).
Analysis of Lesser Black-Backed Gull Data to Inform Meta-Population Studies.
BTO Research Report No. 654. Norfolk: Thetford.
Ross-Smith, V. H., Robinson, R. A., Banks, A. N., Frayling, T. D., Gibson,
C. C., and Clark, J. A. (2014b). The lesser black-backed gull Larus
fuscus in England: how to resolve a conservation conundrum. Seabird 27,
41–61.
Ross-Smith, V. H., Robinson, R. A., and Clark, J. A. (2015). Dispersal and
Movements of Lesser Black-Backed Gull in Europe. BTO Research Report No.
671. Norfolk: Thetford.
Sibley, D. A. (2014). The Sibley Guide to Birds, 2nd Edn. New York, NY: Alfred A.
Knopf.
Southwood, T. R. E., May, R. M., Hassell, M. P., and Conway, G. R. (1974).
Ecological strategies and population parameters. Am. Nat. 108, 791–804. doi:
10.1086/282955
Sovon (2019). Netwerk Ecologische Monitoring (Network Ecological Monitoring).
Provincies & CBS. Available online at: https://www.sovon.nl/ (accessed July 15,
2020).
Soykan, C. U., Sauer, J., Schuetz, J. G., LeBaron, G. S., Dale, K., and Langham,
G. M. (2016). Population trends for North American winter birds based on
hierarchical models. Ecosphere 7:e01351. doi: 10.1002/ecs2.1351
Sz˝
ucs, M., Melbourne, B. A., Tuff, T., and Hufbauer, R. A. (2014). The roles of
demography and genetics in the early stages of colonization. Proc. R. Soc. B.
281:20141073. doi: 10.1098/rspb.2014.1073
Thaxter, C. B., Ross-Smith, V. H., Clark, N. A., Conway, G. J., Wade, H., Masden,
E. A., et al. (2012). Measuring the Interaction Between Marine Features of
Special Protection Areas with Offshore Wind Farm Development Zones Through
Telemetry: Second Year Report. BTO Research Report No. 610. Norfolk:
Thetford.
Thomas, G. E. (1993). Estimating annual total heron population counts. Appl. Stat.
42, 473–486. doi: 10.2307/2986326
Thorup, K. (2004). Reverse migration as a cause of vagrancy. Bird Study 51,
228–238. doi: 10.1080/00063650409461358
vanVliet, G., Marshall, B., Craig, D., and Egolf, J. (1993). First record of nesting
activity by a Lesser Black-backed Gull (Larus fuscus) in North America. Bull.
Pac. Seabirds Group 20:21.
Veit, R. R. (1997). Long-distance dispersal and population growth of the yellow-
headed blackbird Xanthocephalus xanthocephalus. Ardea 85, 135–143.
Veit, R. R. (1990). Do vagrant birds in Massachusetts reflect population growth and
dispersal rather than weather patterns? Bird Obs. 18, 86–91.
Veit, R. R. (2000). Vagrants as the expanding fringe of a growing population. Auk
117, 242–246. doi: 10.1093/auk/117.1.242
Veit, R. R., and Lewis, M. A. (1996). Dispersal, population growth, and the Allee
effect: dynamics of the house finch invasion of eastern North America. Am. Nat.
148, 255–274. doi: 10.1086/285924
Veit, R. R., and Petersen, W. R. (1993). Birds of Massachusetts. Massachusetts, MA:
Massachusetts Audubon Society.
Veit, R. R., Zawadzki, L. C., Manne, L. L., Cales, P., Fibikar, D., Curley, S., et al.
(2016). Vagrancy and colonization of St. Thomas and St. John, U.S. Virgin
Islands, by Adelaide’s Warblers (Setophaga adelaidae). J. Caribb. Ornithol. 29,
47–50.
Wetlands International (2020). Waterbird Population Estimates. Available online
at: http://wpe.wetlands.org/ (accessed July 25 2020).
Williamson, K. (1959). The September drift-movements of 1956 and 1958. Br. Birds
52, 334–377.
Wood, S. (2006). Generalized Additive Models: An Introduction With R. Boca
Raton, FL: CRC Press. doi: 10.1201/9781420010404
Wood, S. N. (2017). Generalized Additive Models: An Introduction With R, 2nd Edn.
Boca Raton, FL: Chapman and Hall/CRC.
Zawadzki, L. C., Veit, R. R., and Manne, L. L. (2019). The influence of population
growth and wind on vagrancy in a North American passerine. Ardea 107,
131–147. doi: 10.5253/arde.v107i2.a2
Conflict of Interest: 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.
Publisher’s Note: All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated organizations, or those of
the publisher, the editors and the reviewers. Any product that may be evaluated in
this article, or claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Copyright © 2021 Zawadzki, Hallgrimsson, Veit, Rasmussen, Boertmann, Gillies and
Guilford. 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 11 December 2021 | Volume 9 | Article 637452