A century of change in Glaucous-winged Gull ( Larus
glaucescens) populations in a dynamic coastal
environment
Authors: Blight, Louise K., Drever, Mark C., and Arcese, Peter
Source: The Condor, 117(1) : 108-120
Published By: American Ornithological Society
URL: https://doi.org/10.1650/CONDOR-14-113.1
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Volume 117, 2015, pp. 108–120
DOI: 10.1650/CONDOR-14-113.1
RESEARCH ARTICLE
A century of change in Glaucous-winged Gull (Larus glaucescens)
populations in a dynamic coastal environment
Louise K. Blight,
1,2#
* Mark C. Drever,
1,3#
and Peter Arcese
1
1
Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, British Columbia, Canada
2
Procellaria Research & Consulting, Victoria, British Columbia, Canada
3
Canadian Wildlife Service, Environment Canada, Delta, British Columbia, Canada
#
These authors contributed equally to the paper.
* Corresponding author: lkblight@interchange.ubc.ca
Submitted July 17, 2014; Accepted November 12, 2014; Published January 28, 2015
ABSTRACT
As conspicuous midtrophic omnivores, gulls can serve as useful indicators to characterize long-term ecological changes
in marine ecosystems. Glaucous-winged Gulls (Larus glaucescens) have been studied in the Georgia Basin of British
Columbia, Canada, an urbanized coastal zone, since the late 1800s. We collated all available information to develop a
(noncontinuous) 111-year time series of counts at breeding colonies, and combined these counts with demographic vital
rates to assess how changes in historical gull egg harvesting practices, forage fish abundance, and Bald Eagle (Haliaeetus
leucocephalus) numbers affected gull population trajectories from 1900 to 2010. Mean counts at 87 breeding colonies in
the Georgia Basin showed a nonlinear trend, increasing from historical low counts in the early part of the twentieth
century to peak values in the 1980s, and declining thereafter to the end of the time series. Demographic models that
integrated temporal trends in clutch size and nesting success, and which also included a food-related decline in first-year
survival or a further reduction in nesting success as a function of eagle abundance, successfully reproduced trajectories of
gull population growth rates over the study period. Glaucous-winged Gulls have thus responded to a series of changes in
the Georgia Basin. These patterns are consistent with population release following cessation of egg harvesting; growing
reliance by gulls on nonfish foods and resulting declines in clutch size, productivity, and first-year survival; and the effects
of recovering Bald Eagle populations. These results highlight the value of compiling data from multiple retrospective
studies to better understand the complex factors affecting long-term trends in animal populations.
Keywords: clutch size, Haliaeetus, Migratory Bird Convention Act, piscivore, population regulation, seabirds,
shifting baselines
Un siglo de cambi o en las poblaciones de Larus glaucescens en un ambiente dina
´
mico costero
RESUMEN
En su calidad de omn
´
ıvoros conspicuos y consumidores secundarios, las gaviotas pueden servir como indicadores
´
utiles para caracterizar el cambio ecol
´
ogico a largo plazo de los ecosistemas marinos. Larus glaucescens ha sido
estudiada desde los a
˜
nos 1800 en la cuenca de Georgia, Columbia Brita
´
nica, Canada
´
, una zona costera urbanizada.
Cotejamos toda la informaci
´
on disponible para desarrollar una serie de tiempo no continua de 111 a
˜
nos de conteos en
las colonias reproductivas, y combinamos estos datos con las tasas demogra
´
ficas vitales para determinar c
´
omo los
cambios hist
´
oricos en las pra
´
cticas de cosecha de huevos de gaviota, la abundancia de peces, y el n
´
umero de Haliaetus
leucocephalus afectaron la trayectoria de la poblaci
´
on de gaviotas entre 1900 y 2010. Los conteos promedio en 87
colonias reproductivas en la cuenca de Georgia mostraron una tendencia no lineal, que se increment
´
o de conteos
hist
´
oricos bajos en la primera parte del siglo veinte a valores pico en los a
˜
nos 80 y luego declin
´
o hacia el final de la
serie temporal. Los modelos demogra
´
ficos que integraron las tendencias temporales en tama
˜
no de nidada y
´
exito
reproductivo, o una mayor reducci
´
on en el
´
exito reproductivo en funci
´
on de la abundancia de a
´
guilas, reprodujeron
exitosamente la trayectoria en las tasas de crecimiento de la poblaci
´
on de gaviotas durante el periodo de estudio. L.
glaucescens ha respondido a una serie de cambios en la cuenca de Georgia. Estos patrones son consistentes con una
liberaci
´
on de la poblaci
´
on luego del cese de la cosecha de huevos, con una creciente dependencia de las gaviotas de
alimentos diferentes a los peces, y un declive resultante en el tama
˜
no de la nidada, la productividad, y la supervivencia
en el primer a
˜
no, y con los efectos de la recuperaci
´
on de las poblaciones de H. leucocephalus. Estos resultados resaltan
el valor de recopilar m
´
ultiples estudios en retrospectiva para entender mejor los complejos factores que afectan las
tendencias de largo plazo en las poblaciones animales.
Palabras clave: Acto de la Convenci
´
on de Aves Migratorias, aves marinas, Haliaetus, pisc
´
ıvores, regulaci
´
on
poblacional, tama
˜
no de nidada, l
´
ıneas de referencia cambiantes
Q 2015 Cooper Ornithological Society. ISSN 0010-5422, electronic ISSN 1938-5129
Direct all requests to reproduce journal content to the Central Ornithology Publication Office at aoucospubs@gmail.com
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INTRODUCTION
A key question in ecology is what constitutes a ‘normal’
change in animal population numbers, given the large
fluctuations that may occur over time (Krebs et al. 2001).
Long-term time series are critical to addressing this
question because they are more likely to include multiple
population or climate cycles, and thus to reveal critical
underlying processes and the occurrence of rare but
influential events (Wiens 1977, 1984, Ludwig 1999).
Marine birds are often identified as sensitive indicators
of ocean systems (Furness and Camphuysen 1997, Piatt et
al. 2007, Parsons et al. 2008), with more than 200 papers in
the past 2 decades showing that seabird populations are
measurably affected by changes to marine environments
(Gr
´
emillet and Charmantier 2010). We present an analysis
aimed at identifying the range of population variation in
the Glaucous-winged Gull (Larus glaucescens), a potential
indicator species (Hebert et al. 1999, 2009, Gebbink et al.
2011), based on count data from breeding colonies
spanning a period of 111 years in the Georgia Basin,
British Columbia (BC), Canada.
The Glaucous-winged Gull is a long-lived marine bird
described as thriving in proximity to humans, but whose
numbers currently appear to be in decline over a
substantial portion of its southern range (Sullivan et al
2002, Bower 2009, Hayward et al. 2010). This decline has
prompted concern about future trends, although evidence
exists to suggest that Glaucous-winged Gull numbers in
the region were much lower at the start of the twentieth
century than at present (Dawson and Bowles 1909, Drent
and Guiguet 1961). Thus, it is plausible that the species
responded favorably to human-induced environmental
changes in the early 1900s, with these changes facilitating
population growth above a baseline supported by the
availability of natural foods (Vermeer 1992, Hayward et al.
2010). Under such a scenario, the recent decline would
simply represent a reversal of these influences and a return
to historical conditions. However, a detailed understanding
of population trends to the present day is lacking.
Larus gulls worldwide often nest colonially near human
population centers (Ward 1973, Pons 1992, Oro et al.
2004), and they have long drawn the attention of field
biologists (Dutcher and Baily 1903, Anonymous 1908).
Early studies of these species focused on behavior and
demography, and only incidentally recorded population
numbers (Province of British Colum bia 1915, Tinbergen
1953, Vermeer 1963). To provide a definitive estimate of
long-term population trends in the study region, we used
colony count data for Glaucous-winged Gulls nesting in
the Georgia Basin to esti mate long-term changes in mean
colony size from 1900 to 2010. We examined potential
causes of population change based on three hypotheses
developed to account for temporal trends in gull
populations generally (Grandgeorge et al. 2008, Hayward
and Verbeek 2008, Farmer and Leonard 2011), and that
were appropriate to the history and ecology of Glaucous-
winged Gulls in our region. We used a simple demographic
model to generate expected population trajectories based
on estimates of reproductive success and survival derived
from field data and historical accounts, and compared
these predicted trajectories to observed population trends
derived from colony counts.
Food Limitation
Food availability may have driven both increases and
decreases in Glaucous-winged Gull populations during the
last century. Expanding human populations in the Georgia
Basin may have increased the availability of food for gulls
in the form of garbage, and by doing so may have
facilitated gull population growth after 1920 (Vermeer
1992, Hayward et al. 2010), as has occurred in other
systems (Spaans 1971, Pons and Migot 1995). Alternati ve-
ly, changes in forage fish populations may have decreased
food availability (Therriault et al. 2009, McKechnie et al.
2014), which may explain recent declines in gull popula-
tions in the Georgia Basin. Population declines have
occurred in parallel with long-term decreases in egg
volume and clutch size (Blight 2011), a pattern consistent
with the theory that access to high-protein fish prey, as
opposed to lower-quality anthropogenic garbage, may be
critica l for successful egg production in various gull
species (Hiom et al. 1991, Bolton et al. 1992, Annett and
Pierotti 1999). Food shortages may also lead to increased
egg cannibalism at some colonies (Hayward et al. 2014),
which has the potential to contribute to clutch size
declines. These potential links between food abundance
or quality and reduced clutch size, reproductive success,
and population decline are hereafter referred to collec-
tively as the ‘food limitation’ hypothesis.
Predation by Bald Eagles
A second hypothesis, ‘predation limitation,’ might also
explain long-term population trends in Glaucous-winged
Gulls, given that Bald Eagles (Haliaeetus leucocephalus)
have regionally increased in number over time, presumably
along with predation rates. In the first half of the twentieth
century, Bald Eagles were suppressed by persecution, and,
later, by exposure to DDT and PCBs (Elliott and Harris
2002). Bald Eagles can affect gull reproduction and survival
directly via predation (Vermeer and Morgan 1989) and
indirectly by affecting behavior and predation risk (Hipfner
et al. 2012). Predation by eagles on gull eggs or young birds
likely increased as eagles recovered in the mid-to-late
1900s (Sullivan et al. 2002, Elliott et al. 2011). Under this
hypothesis, gull numbers should have grown or remained
stable in the absence of eagles, but grown more slowly or
declined as eagle populations recovered.
The Condor: Ornithological Applications 117:108–120, Q 2015 Cooper Ornithological Society
L. K. Blight, M. C. Drever, and P. Arcese A century of change in Glaucous-winged Gulls 109
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Cessation of Egg Harvesting
Reid (1988) suggested that increases in the productivity of
Glaucous-winged Gulls in the region occurred after the
adoption of the Canada–U.S. 1916 Migratory Bird
Convention (Migratory Bird Treaty in the USA), which
reduced or eliminated egg collecting and hunting of adults
throughout the Georgia Basin. Accounts from the late
1800s suggest that, historically, harvesting of seabird eggs
occurred at very high rates. On the Farallon Islands,
California, USA, seabird egg hunters regularly broke all
eggs found so that they could later return to collect freshly
laid second clutches; in 1886 alone , 108,000 eggs were
reported as having been taken from Common Murre (Uria
aalge) nests on these islands (Doughty 1971). Seabird
shooting and egg har vesting was also common in the
Georgia Basin prior to legislative protection. In 1915, a
warden was placed on Mandarte Island, BC, to protect
nesting birds because ‘‘human beings – whites, Indians,
and Japanese – carry . . . away the birds’ eggs and young’’
(Province of British Columbia 1916: N15). On nearby
Mitlenatch Island, Pearse (1923) noted poor reproductive
success because nests were ‘‘ systematically robbed’’ (p.
133) and that ‘‘ the place was cleaned of eggs’’ (p. 133).
Anthony (1906: 130) further noted th at recreatio nal
hunters would commonly ‘‘ slaught er w antonly large
numbers [of gulls] for the mere sport.’’ Thus, the ‘egg
harvesting hypothesis’ predicts that, once protected, gull
populations in the Georgia Basin increased until limited by
food or predators.
Each of the three general hypotheses has empirical
merit, invoking factors likely to have influenced gull
populations concurrently or sequentially over the last
century. We evaluated their potential demographic impacts
on gulls by fitting simple matrix population models and
comparing trajectories of hypothesized population growth
rates to observed population growth rates following the
general approach of Walters (1986), Hilborn and Mangel
(1997), and Walters and Martell (2004) . We used a time
series of gull colony counts, published demographic vital
rates and our own field data, previously documented
declines in clutch size, and annual eagle counts to test
whether declines in gull fecundity, predation by eagles, or
some combination of these two factors accounted for
observed population trends within our study area. Overall,
the objectives of our study were to use Glaucous-winged
Gull population trends and modeled hypotheses to
evaluate how gull population size changed over time in
the Georgia Basin and to determine whether population
trends were related to temporal variation in reproductive
output, within the general context of investigating what
these population trends suggested about baseline condi-
tions in the Georgia Basin.
METHODS
Study Area and Colony Counts
The Georgia Basin refers to the Canadian portion of the
Salish Sea, an inland body of water encompassing the
Strait of Georgia, BC; Puget Sound, Washington, USA; the
eastern portion of the Juan de Fuca Strait; and the region’s
islands and terrestrial watersheds (Figure 1). The area is
influenced by several major urban centers and is heavily
affected by human activity, being ranked as ‘very high
impact’ in a global assessment of anthropogenic impacts of
coastal ecosystems (Halpern et al. 2008).
We compiled all available published and unpublished
Glaucous-winged Gull counts at breeding colo nies (num-
ber of nests or breeding pairs per colony) obtained from
field studies conducted between 1900 and 2010 in the
inshore coastal waters of the Georgia Basin, Canada, and
supplemented these data by conducting colony censuses in
2009 and 2010 (Blight 2014). In a few cases we used
median values as our colony counts, when historical
estimates were provided as ranges (n ¼ 15). Our 2009 and
2010 counts were carried out following the methods of
FIGURE 1. The locations of Glaucous-winged Gull colonies used
to estimate population trends (1900–2010, noncontinuous data)
in the Georgia Basin, British Columbia, Canada.
The Condor: Ornithological Applications 117:108–120, Q 2015 Cooper Ornithological Society
110 A century of change in Glaucous-winged Gulls L. K. Blight, M. C. Drever, and P. Arcese
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Vermeer and Devito (1989), who censused all nonurban
Glaucous-winged Gull colonies in the Georgia Basin in
1986 (Vermeer and Devito 1989). Our censuses replicated
about 60% (49 of 83) of the sites counted in 1986, but we
selected these 49 sites to includ e most (~96% of 1986
numbers) of the breeding population. Of the 34 colonies
that we did not visit, 76% historically consisted of 10
pairs. We conducted censuses from June 13 to June 20 in
2009 (Mandarte Island and the Chain Island group) and
2010 (remaining colonies). Four colonies of 1–5 pairs were
surveyed using binoculars on July 1, 2010. The mid-June
census period was chosen to most closely replicate earlier
censuses and to coincide with the peak of egg laying
(Vermeer and Devito 1989, Sullivan et al. 2002, Blight
2011). Conduct ing counts prior to hatching avoids
disturbing gull chicks, which when frightened may flee
into adjacent territories where they may be killed by
neighboring birds (Hunt and H unt 1976). To avoid
disturbing sympatric nesting cormorants (Phalacrocorax
spp.), we counted any gulls nesting in their vicinity using
binoculars. As with previously published studies (Vermeer
and Devito 1989, K. Vermeer personal communication), we
counted only active nests (containing 1 egg, or evidence
of depredation), because Glaucous-winged Gulls often
build multiple nest cups prior to laying. Because count
data were collected by multiple observers over more than a
century, we were unable to determine the degree to which
an observer effect might have affected counts, and did not
attempt to correct for it. We also assumed equal nest
detectability with increasing colony size, because larger
colonies tended to be censused by more observers, and
Glaucous-winged Gull nests are fairly visible to observers,
generally being constructed in open grass or rocky areas.
Temporal Trends
Temporal trends in gull abundance were estimated using
generalized additive models (GAMs) by modeling colony
counts in relation to year, from 1900 to 2010. The GAM
approach is an extension of the General Linear Model, in
which predictors are smoothed functions rather than
linear relationships (Wood 2006). This approach allowed
for evaluation of nonlinear trends in mean gull colony
counts over time. Year 1900 was set to a value of 0, and we
used package ‘mgcv’ in R (Wood 2006) to fit a GAM that
included a Poisson error distribution and a unique colony
identifier as a random effect to account for the correlated
non-normally distributed error s (all R code is available in
the Supplemental Material Appendix).
Demographic Models
Using the stock reconstruction methods of Walters (1986)
and Walters and Martell (2004), we tested whether
observed and hypothesized changes in demographic vital
rates were sufficient to explain changes in mean gull
colony counts. We first calculated a time series of observed
population growth rates as the ratio of successive mean
predicted values from the trend model of colony counts
(Figure 2), i.e. predicted mean count at year t þ 1 divided
by the predicted mean count at year t. We then compared
this observed population trajectory to hypothesized
trajectories derived from different combinations of demo-
graphic vital rates in series of four scenarios of increasing
complexity, with these scenarios determined a priori. For
each scenario, a prebreeding birth-pulse deterministic
matrix population model (female-only; Caswell 2001) was
constructed for each year t from 1900 to 2010, similar to
the matrix model built for Yellow-legged Gulls (L.
cachinnans; Bosch et al. 2000). Each projection matrix
had the general form:
At½¼
000
CS t½
2
3 NS t½3 S1 t½
S20 0 0
0 S30 0
00S4 S4
2
6
6
6
6
4
3
7
7
7
7
5
:
Clutch size (CS [t]) adjusted per female, nesting success
(NS[t]), that is the proportion of eggs that hatched and
survived to become fledglings (Ricklefs 1973), and survival
probability (S1[t]) from fledging to 1 yr of age were
allowed to vary by year in scenarios. Survival probabilities
for the older age classes (S2, from 1 yr to 2 yr of age; S3, the
FIGURE 2. Trends in colony counts of Glaucous-winged Gulls in
the Georgia Basin, British Columbia, Canada, 1900–2010. Colony
counts are log-transformed as log
e
(x þ 1) to allow plotting of 0-
counts. Hollow points indicate counts of pairs or nests at 87
locations. Thick hollow points along the trend line indicate mean
colony counts with 95% confidence intervals (thin lines)
predicted from a Generalized Additive Model.
The Condor: Ornithological Applications 117:108–120, Q 2015 Cooper Ornithological Society
L. K. Blight, M. C. Drever, and P. Arcese A century of change in Glaucous-winged Gulls 111
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