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Technological advances in recent years have seen an explosion of tracking and stable isotope studies of seabirds, often involving repeated measures from the same individuals. This wealth of new information has enabled the extensive variation among and within individuals in foraging and migration strategies (movements, habitat use, feeding behaviour, trophic status, etc.) to be examined in unprecedented detail. Variation is underpinned by key life-history or state variables such as sex, age and breeding stage, and residual differences among individuals (termed ‘individual specialization’). This variation has major implications for our understanding of seabird ecology because it affects the use of resources, level of intra-specific competition, and niche partitioning. In addition, it determines the responses of individuals and populations to the environment, and the susceptibility to major anthropogenic threats. Here we review the effects of season (breeding vs nonbreeding periods), breeding stage, breeding status, age, sex, and individual specialization on variation in foraging and migration strategies, and the consequences for population dynamics and conservation.
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Mar Ecol Prog Ser
Vol. 578: 117–150, 2017 Published August 31
The burgeoning of tracking and stable isotope
studies of seabirds and other marine predators since
the 1990s has provided a wealth of information on
numerous aspects of their ecology and life-history,
including the striking variation in movement pat-
terns and foraging behaviour of individuals (Phillips
et al. 2008, Wakefield et al. 2009a). Until relatively
recently, this variation was examined largely by test-
ing for effects of factors such as species, colony, sex,
age, year, season (breeding vs. nonbreeding period),
breeding phase or breeding status. Much less atten-
tion was paid to the residual variation among individ-
uals after accounting for these group effects. This
residual variation was considered to define ‘individ-
ual specialization’ in the seminal review by Bolnick
et al. (2003) and is also the focus of research on ‘be -
havioural syndromes’ or ‘animal personalities’ in the
field of animal behaviour (Dall et al. 2012). Research
on individual variation has burgeoned in the last
decade, spurred partly by reductions in cost and
mass of tracking devices, allowing larger sample
sizes, and by the increasing use of more powerful sta-
tistical techniques (Carneiro et al. 2017, this Theme
© The authors 2017. Open Access under Creative Commons by
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restricted. Authors and original publication must be credited.
Publisher: Inter-Research ·
*Corresponding author:
Causes and consequences of individual variability
and specialization in foraging and migration
strategies of seabirds
Richard A. Phillips1,*, Sue Lewis2, Jacob González-Solís3, Francis Daunt2
1British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge, Cambridgeshire,
2Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian, EH26 0QB, UK
3Institut de Recerca de la Biodiversitat (IRBio) and Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals (BEECA),
Universitat de Barcelona, Av Diagonal 643, Barcelona 08028, Spain
ABSTRACT: Technological advances in recent years have seen an explosion of tracking and sta-
ble isotope studies of seabirds, often involving repeated measures from the same individuals. This
wealth of new information has allowed the examination of the extensive variation among and
within individuals in foraging and migration strategies (movements, habitat use, feeding behav-
iour, trophic status, etc.) in unprecedented detail. Variation is underpinned by key life-history or
state variables such as sex, age, breeding stage and residual differences among individuals
(termed ‘individual specialization’). This variation has major implications for our understanding of
seabird ecology, because it affects the use of resources, level of intra-specific competition and
niche partitioning. In addition, it determines the responses of individuals and populations to the
environment and the susceptibility to major anthropogenic threats. Here we review the effects of
season (breeding vs. nonbreeding periods), breeding stage, breeding status, age, sex and individ-
ual specialization on foraging and migration strategies, as well as the consequences for population
dynamics and conservation.
KEY WORDS: Individual specialization · Consistency · Sexual segregation · Age effects ·
Central-place constraint · Intrinsic variation · State dependence · Life-history
Contribution to the Theme Section ‘Individual variability in seabird foraging and migration’
Mar Ecol Prog Ser 578: 117–150, 2017
Most seabirds show striking changes in distribu-
tion associated with stage of the annual cycle. Many
species are migratory, making directed movements
from breeding to nonbreeding grounds to exploit
seasonal peaks in prey abundance or to avoid
inclement weather, with implications for survival and
subsequent fecundity (Daunt et al. 2014, Reiertsen et
al. 2014). The changing degree of central-place con-
straint during the breeding period from pre-laying
through incubation, brood-guard and later chick-
rearing (post-guard) can lead to major shifts in dis-
tribution, activity patterns or diet within individuals
(Hedd et al. 2014, Quillfeldt et al. 2014). There may
be within-breeding-season (date-related) differences
in distribution or diet, which reflect extrinsic changes
in the environment (Phillips et al. 2009b). In addition,
some seabirds (particularly albatrosses and petrels)
adopt a bimodal (or dual) foraging strategy during
chick-rearing, in which adults alternate between
foraging close to the colony and increasing feeding
frequency for the benefit of the chick, and foraging
further afield to recover their own body condition
(Chaurand & Weimerskirch 1994, Weimerskirch et
al. 1994).
There is mounting evidence that movements and
distributions of seabirds are influenced by age and
breeding status. Failed breeders often depart on their
migration sooner than successful ones (Phillips et al.
2005, Bogdanova et al. 2011, Hedd et al. 2012), and
they may spend the late breeding season in the same
areas as deferring (sabbatical) breeders, but be par-
tially or completely segregated from active breeders
(Phillips et al. 2005, González-Solís et al. 2007, Reid
et al. 2014). In this way, nonbreeders (failed or defer-
ring) may be avoiding competition with breeders
(Clay et al. 2016). Juvenile and immature seabirds
avoid competition with adultspossibly to compen-
sate for poorer foraging skills by using less produc-
tive habitats and increasing their foraging time
(Daunt et al. 2007b, Fayet et al. 2015). Their distribu-
tions frequently differ from those of adults, often
markedly so during the nonbreeding period even
though adults are no longer limited by the central-
place foraging constraint (but see Péron & Grémillet
2013, Gutowsky et al. 2014, de Grissac et al. 2016).
Age effects on foraging ability are often apparent
amongst breeders: younger or less experienced birds
may forage less efficiently, with implications for breed-
ing success (Daunt et al. 2007b, Limmer & Becker
2009, Harris et al. 2014a, Le Vaillant et al. 2016), or
feed at lower trophic levels (Le Vaillant et al. 2013).
Inferior foraging success among younger individuals
is thought to reflect the poorer skills in identifying or
catching prey or in selecting suitable locations,
weaker motor control or physiological fitness (e.g.
cardiovascular or muscular performance) of young
birds or the selective disappearance of poor pheno-
types among the adult population. Although there is
evidence that foraging ability can decline in old age
(Catry et al. 2006), changes in behaviour may not be
detectabledespite physiological ageing (Elliott et
al. 2015)or are apparent only in particular environ-
ments (Lecomte et al. 2010, Froy et al. 2015). More-
over, differences between old and young animals can
be difficult to interpret, because lower activity (e.g.
more time on the water recorded by a leg-mounted
immersion logger) might indicate either inferior
physiological function or greater efficiency allowing
more discretionary time to be spent resting (Catry et
al. 2011).
Sexual segregation and other between-sex differ-
ences in foraging behaviour are apparent in many
seabirds. This may reflect habitat specialization or
avoidance of competition in sexually dimorphic spe-
cies and sex role specialization or sex-specific nutri-
ent requirements in monomorphic or dimorphic spe-
cies (Lewis et al. 2002, Phillips et al. 2004, 2011). Sex
differences in distribution and behaviour of seabirds
tend to be more apparent during particular periods,
for example during pre-laying (presumably related
to sex-role partitioning of nest defense), affecting
attendance patterns (Hedd et al. 2014, Quillfeldt et
al. 2014). However, such effects are far from univer-
sal; despite a degree of spatial segregation, activity
patterns of male and female albatrosses are compa-
rable during the breeding and nonbreeding periods,
suggesting little difference in prey type or foraging
method (Mackley et al. 2011, Phalan et al. 2007).
Similarly, in the 2 recent studies that recorded sex
differences in the proportions of residents and mi -
grants, the effects were in opposite directions (Pérez
et al. 2014, Weimerskirch et al. 2015).
Variation among and within individuals in foraging
distribution and behaviour has major implications
for our understanding of seabird ecology because it
affects the use of resources, level of intra-specific
competition and niche partitioning (Phillips et al.
2004, de Grissac et al. 2016). In addition, it deter-
mines the responses of individuals and populations to
environmental drivers (including climatic change)
and the overlap with, and hence susceptibility to
major anthropogenic threats, including fisheries and
pollutants (Phillips et al. 2009a, Granadeiro et al.
2014, Patrick et al. 2015). Individual variation is also
at the root of carry-over effects, whereby processes in
one season have consequences in subsequent sea-
Phillips et al.: Individual variability in seabirds
sons (Harrison et al. 2011). Surprisingly, however,
there are rarely demonstrable life-history conse-
quences of individual consistency in foraging strate-
gies per se despite the many studies of adult quality
(consistent individual differences in breeding per-
formance) in seabirds (Lescroël et al. 2009, Crossin et
al. 2014, but see Patrick & Weimerskirch 2017).
Here we review the intrinsic group effects under -
lying individual variation in foraging and migration
patterns of seabirds, including breeding stage, season
(breeding vs. nonbreeding period), breeding status,
age, sex andafter those have been accounted for
the incidence, causes and consequences of the indi-
vidual effects that remain. We consider these last,
residual effects to be synonymous with individual
specialization sensu Bolnick et al. (2003) and expect
specialists to show repeatability or consistency in
foraging distribution, behaviour or diet. We do not re-
view effects of colony, as these may reflect differences
in resource availability or habitat accessibility, nor
effects of date or year per se, as these reflect environ-
mental variation and are extrinsic to individual deci-
sions and trade-offs. We explore whether the degree
of variation among and within individuals (i.e. both
groups effects and specialization) depends on phylo -
geny, biogeography or other factors and focus on the
consequences for life-histories and population dy-
namics and the implications for seabird conservation.
The impetus for this review and for this Theme
Section on ‘Individual variability in seabird foraging
and migration’ in Marine Ecology Progress Series was
the session on ‘Individual variation in movement
strategies’ at the 2nd World Seabird Conference in
Cape Town, South Africa, 27−30 October, 2015.
Breeding stage and season
(breeding vs. nonbreeding period)
Changes in seabird diet across the annual cycle,
particularly over different stages of the breeding
period, have been studied for several decades (Bar-
rett et al. 2007), but until the advent of suitable track-
ing technologies, information on year-round forag-
ing behaviour of seabirds was scarce. Subsequently,
many studies have recorded foraging distribution
and behaviour of individuals over extended periods,
showing that these vary markedly throughout the
annual cycle; some of these changes reflect differ-
ences in food availability or the underlying biophysi-
cal environment, and others are directly related to
changes in reproductive demands and central-place
foraging (Phillips et al. 2008, González-Solís & Shaf-
fer 2009). Energy requirements and breeding duties
change across the annual cycle, limiting foraging in
time and space (including to the most productive
habitats) to different extents.
During pre-laying, birds visit the colony frequently
or remain there for a prolonged period for pair bond-
ing and nest defence, but they are still free from
parental duties and may have time available for long
trips. Although the constraints for males and females
may differ, individuals typically forage further from
the colony and in more productive waters than in
later stages (Phillips et al. 2006, Paiva et al. 2008,
Pinet et al. 2012, Hedd et al. 2014). During incuba-
tion, most seabirds alternate incubation bouts, with
one parent incubating the clutch while the other is at
sea. In penguins, albatrosses, petrels and alcids,
birds may fast for several weeks on the nest while the
partner engages in foraging trips that are longer and
further afield than during chick rearing (Hull 2000,
Phalan et al. 2007, Ito et al. 2010, Péron et al. 2010,
Hedd et al. 2014). Nevertheless, trips usually shorten
when hatching approaches, allowing the chick to be
fed within a few days (Weimerskirch et al. 1997,
González-Solís 2004). In gulls and skuas, however,
incubation bouts are relatively short, and the forag-
ing range during that phase can be similar or shorter
than during chick rearing (Carneiro et al. 2014, Cam-
phuysen et al. 2015).
During brooding, the parents alternate foraging
with guarding the chicks, which are rarely left unat-
tended in order to reduce exposure to the elements or
predators. In pelagic seabirds, this is often regarded
as the period with the greatest energy requirements,
since an adult must forage both to meet its own
demands during the subsequent brooding stint and
those of the chicks (Ricklefs 1983). In some species
(including albatrosses, petrels and penguins), parents
are forced to forage closer to the colony than in any
other stage (Hull 2000, Charrassin & Bost 2001,
Phillips et al. 2004, González-Solís et al. 2007), even
though the areas visited may not be optimal, leading
to progressive deterioration in parental body condition
(Weimerskirch & Lys 2000, Green et al. 2009). In addi-
tion, the requirements of the chick in terms of prey
energetic or nutritional content, size or di gestibility
may necessitate a change in foraging behaviour of the
adult (Davoren & Burger 1999, Isaksson et al. 2016).
Several studies have shown that parents feed their
chicks with a high-quality diet, for example selecting
lipid-rich fishes (Wilson et al. 2004, McLeay et al.
2009, Bugge et al. 2011, Dänhardt et al. 2011), and a
Mar Ecol Prog Ser 578: 117–150, 2017
failure to do so may reduce chick survival (Annett &
Pierotti 1999, Grémillet et al. 2008). Alternatively, se-
lection of high quality prey may reflect the need to
maximise net energy gain per unit foraging effort for
parents that are unable to carry more than one item in
their bill (Wilson et al. 2004). In species delivering
mainly undigested food, chicks are limited in terms
of the size of prey they can swallow, and parents are
typically forced to seek small items, steadily increas-
ing the size with chick age, which may require parents
to change prey types and foraging areas over the
chick-rearing period (Pedrocchi et al. 1996, Rodway &
Montevecchi 1996, McLeay et al. 2009).
In many species there is a post-brooding period
(crèche in penguins) when parents leave chicks unat-
tended except when delivering meals so that they can
increase trip length. Initially, the foraging range usu-
ally remains more constrained than during incubation
(Phillips et al. 2004, Saraux et al. 2011, Froy et al.
2015), presumably because chicks have a lower fast-
ing capability than incubating adults until the mid- to
late chick-rearing phase (Phillips & Hamer 1999). Trip
duration tends to increase and parents forage further
away from the colony as the chick-rearing period pro-
gresses (Weimerskirch & Lys 2000, Dall’Antonia et al.
2001, Rishworth et al. 2014b). These longer trips are
likely prompted by the chicks’ increased fasting capa-
bility and energetic demand, as well as a deterioration
in food availability or an increase in foraging con-
specifics enhancing density-dependent competition
near the colony (Rishworth et al. 2014b). The ability to
increase intervals between feeding is limited by the
maximum payload, which is inversely related to adult
body mass in Procellariiformes (Phillips & Hamer
2000). Food delivery rates also depend on whether the
adults forage in coastal or inshore waters and deliver
food that is fresh and carried in the bill (terns and
alcids), partially-digested in the stomach (gulls, pen-
guins and other taxa) or further digested to an energy-
dense stomach oil in the proventriculus (Procellari-
iformes; except diving petrels, Pelecanoididae); in this
last group, the single chick stores extensive fat re-
serves, allowing the adults to exploit more remote ar-
eas (Ricklefs 1983, Phillips & Hamer 1999). Changes
in trip duration during breeding can be detected using
stable isotopes, and an increase in foraging range
may be associated with an expansion of the isotopic
niche (Ceia et al. 2014).
For breeding, seabirds need land that is free of ter-
restrial predators. Such breeding grounds may be
distant from productive foraging sites. One mecha-
nism for coping with low food availability close to the
breeding colony is to adopt a so-called ‘dual forag-
ing’ strategy, when parents alternate between short
and long foraging trips to balance their own ener-
getic requirement with that of the chick (Chaurand &
Weimerskirch 1994, Weimerskirch et al. 1994). Dur-
ing these short trips, parents forage within shorter
distances, maximising provisioning rates; however,
this apparently reduces their body condition, causing
the adult to switch to more distant and more produc-
tive waters with predictable food resources (frontal
zones, neritic areas, etc.) to restore its own reserves.
The dual foraging strategy is seen in many alba-
trosses, shearwaters and other petrels, but there is a
great deal of variability among species and popula-
tions, potentially related to differences in foraging
strategies and resource distribution around colonies
or between years (Granadeiro et al. 1998, Baduini &
Hyrenbach 2003, Phillips et al. 2009b). A similar but
less flexible strategy has also been postulated for
penguins (Ropert-Coudert et al. 2004, Saraux et al.
2011). Dual foraging has also been described in auks
(Welcker et al. 2009), possibly because the energetic
cost of transit in this group is particularly high (Costa
1991, Thaxter et al. 2010).
Changes in foraging behaviour also occur in the
nonbreeding period. After breeding, most species of
seabirds migrate to more suitable habitats, avoiding
low temperatures, shorter days and reduced food
availability around colonies. In some populations,
individuals move to a post-breeding, stopover area,
presumably offering good foraging opportunities at
that time of year, where they may spend considerable
time before departing for their main wintering grounds
(Anker-Nilssen & Aarvak 2009, Frederiksen et al.
2012, Bogdanova et al. 2017, this Theme Section).
Both conventional diet (stomach content analysis)
and stable isotope studies indicate that wintering
seabirds can change their diet or widen their trophic
niche, since individuals are no longer central-place
foragers and are free to select their favoured habitat
or prey (Cherel et al. 2007, Karnovsky et al. 2008,
Hedd et al. 2010, Harris et al. 2015). It is important to
note that we lack knowledge for most seabirds of
their prey during the winter; although stable isotope
studies offer a partial solution, ideally these need to
control for changes in isotopic baselines because of
the scale of seabird movements (Meier et al. 2017).
Activity levels decrease during part of or the entire
nonbreeding period in Procellariiformes (Mackley et
al. 2011, 2010, Cherel et al. 2016), sulids (Garthe et al.
2012), skuas (Magnusdottir et al. 2014, Carneiro et al.
2016) and alcids (Mosbech et al. 2012). Reasons for
this decrease may include lower energetic de mands,
freedom from parental care duties and removal of the
Phillips et al.: Individual variability in seabirds 121
central-place foraging constraint, higher food avail-
ability or lower costs of thermoregulation. In addition,
productive nonbreeding grounds may al low for a sit-
and-wait foraging strategy that is more energy-
efficient, or food availability may be en hanced by the
activities of subsurface predators or fisheries (Péron
et al. 2010). Seabirds generally, but not always, moult
in the nonbreeding period to avoid overlap with
other energetically de manding processes, such as re-
production or migration (Bridge 2006, Catry et al.
2013b). This may result in flight im pair ment, which
would explain a decrease in activity levels in the win-
ter in some species (Cherel et al. 2016), or in flight-
lessness, which may drive movements (particularly
by auks) to specific moulting areas (Linnebjerg et al.
2013, Frederiksen et al. 2016).
Lower activity during the nonbreeding period is
far from universal, and species that breed in high
latitudes, are resident year-round, or have limited
capacity to migrate, cope with winter conditions by
increasing their activity levels. Indeed, foraging time
of cormorants or shags breeding at high latitudes
peaks in mid- to late winter, possibly due to reduced
prey availability or high energetic costs associated
with thermoregulation (Grémillet et al. 2005, Daunt
et al. 2006, Lewis et al. 2015), and penguins some-
times dive longer and deeper to exploit less accessi-
ble prey during winter (Moore et al. 1999, Charrassin
& Bost 2001, Green et al. 2005).
Breeding status
Studies of seabird foraging and movements during
the breeding season usually focus on breeding adults
because of the relative ease with which they can be
caught for logger deployment and retrieval. How-
ever, an important component of the breeding popu-
lation comprises individuals that are not breeding or
have failed in their breeding attempt, and an increas-
ing number of studies aim to quantify the foraging
dynamics of these groups and to test whether they
show different behaviours compared to breeding
adults. Much of the attention has been directed at
failed breeders, whose failure may have been natu-
ral, a consequence of the deployment, or induced as
part of a manipulative experiment (Phillips et al.
2005, Bogdanova et al. 2011, Ponchon et al. 2014,
2015). Failed breeders often continue to associate
with the colony, operating as central-place foragers
but expanding their foraging areas (González-Solís
et al. 2007). The spatial overlap with breeders varies
among populations; it can be high (Ponchon et al.
2014), moderate (Phillips et al. 2008), or there may be
marked segregation (Jaeger et al. 2014, Reid et al.
2014, Clay et al. 2016). Further, failed breeders may
make visits to other colonies when breeders are still
actively rearing chicks; this behaviour is interpreted
as prospecting potential new breeding sites and may
be motivated by having failed at the current location
(Fijn et al. 2014, Ponchon et al. 2014, 2015). In con-
trast, successful breeders do not undertake prospect-
ing trips or only do so after breeding is finished (Fijn
et al. 2014, Ponchon et al. 2014, 2015).
Quantifying differences in foraging and movements
between breeding and nonbreeding individuals (the
latter including deferring breeders and older pre-
breeders, but not failed breeders) during the breeding
season is hampered by the difficulty in capturing
nonbreeders to deploy data loggers. There is consid-
erable indirect evidence from observations at breed-
ing sites that nonbreeders often attend the co lo ny in
the breeding season and act as central-place foragers,
suggesting that foraging overlap with breeders would
be substantial (Aebischer 1986, Harris & Wanless
1997). This has been confirmed by tracking black-
browed albatross Thalassarche mela no phris at South
Georgia (Phillips et al. 2005), but in the same species
elsewhere and in Cory’s shear water Calonectris bo-
realis, deferring adults segregate isotopically from
breeders, indicating differences in their foraging
niche (Campioni et al. 2015). Some of the most com-
pelling evidence for spatial segregation based on
breeding status during the breeding season is for bi-
ennial breeders such as the wandering albatross
Diomedea exulans and grey-headed albatross Tha-
lassarche chrysostoma, in which a pro portion of indi-
viduals spend the sabbatical period entirely at sea,
thousands of kilometres from the colony (Weimers -
kirch et al. 2015, Clay et al. 2016).
At the end of the breeding season, timing of depar-
ture from breeding colonies is strongly dependent on
breeding status, with failed and deferred breeders
typically leaving significantly earlier than successful
breeders (Phillips et al. 2005, 2007, Bogdanova et al.
2011, Hedd et al. 2012, Catry et al. 2013a). Carry-
over effects of breeding status on migration may
persist into the nonbreeding period, with evidence
that failed breeders arrive at wintering grounds early
and depart the wintering grounds later or earlier,
depending on the study species (Phillips et al. 2005,
Catry et al. 2013a, Bogdanova et al. 2017). There may
also be differences in migration destination; in black-
legged kittiwakes Rissa tridactyla, failed breeders
wintered further from the breeding colony on aver-
age than successful breeders (Bogdanova et al.
Mar Ecol Prog Ser 578: 117–150, 2017
2011), and evidence from stable isotope analyses
suggested that failed wandering albatrosses differed
from successful and deferred breeders in terms of
distribution in the following winter (Jaeger et al.
2014). Such differences are not always apparent,
however, and high overlap of individuals of differing
breeding status during the winter has been observed
in other studies (Phillips et al. 2005, 2007, Hedd et al.
2012, Clay et al. 2016).
Age-specific foraging and movements
Comparisons of juveniles and adults
A long-standing theory in avian ecology is that
juveniles have reduced survival probability because
they have a lower foraging proficiency, resulting
from a lack of experience or physical ability; this the-
ory is supported by widespread empirical evidence
across many avian species (Marchetti & Price 1989,
Wunderle 1991). These are topics of particular inter-
est in seabirds because of their slow maturity, which
suggests that the development of foraging is complex
and requires an extended period of learning. A list of
studies that tested for differences in foraging and
migration between juveniles, immatures and adult
seabirds is provided in Table 1. Early work on sea-
birds, based primarily on visual observations of feed-
ing individuals or flocks, provided clear evidence
that juveniles had lower foraging success than adults
(Orians 1969, Dunn 1972, Burger & Gochfeld 1981,
Porter & Sealy 1982, Greig et al. 1983, MacLean 1986).
Comparisons of multiple age classes showed pro-
gressive improvement in performance in the pre-
breeding years (Orians 1969, Porter & Sealy 1982,
MacLean 1986), and more recent studies indicate
that foraging effort and skills develop rapidly after
fledging (Yoda et al. 2004, Daunt et al. 2007b, Guo et
al. 2010, Orgeret et al. 2016); however, the foraging
proficiency of juveniles throughout their first winter
remains lower than that of adults, linked to a lower
survival probability (Daunt et al. 2007b, Orgeret et al.
2016). Indeed, in terms of survival prospects, the crit-
ical period is around independence, which, depend-
ing on the species, may occur at fledging or be a
gradual process as parents progressively reduce post-
fledging provisioning rate (Daunt et al. 2007b, Riotte-
Lambert & Weimerskirch 2013, Orgeret et al. 2016).
Biologging and biotelemetry have been instrumen-
tal in the study of movements during the juvenile
phase (Table 1). It has long been apparent from ring-
ing recoveries that juvenile seabirds often disperse
long distances and generally have a wider distri -
bution than adults (Weimerskirch et al. 1985), but at-
tachment of loggers to chicks has enabled the critical
months after fledging to be investigated in detail.
Fledglings typically undertake rapid and large-scale
movements in the first few months and (in flying sea-
birds) appear to target favourable wind patterns,
sometimes delaying departure until these become
available (Kooyman et al. 1996, Åkesson & Weimers -
kirch 2005, Trebilco et al. 2008, Alderman et al. 2010,
Riotte-Lambert & Weimerskirch 2013, Blanco et al.
2015, de Grissac et al. 2016, Weimerskirch et al. 2016).
Such movements can lead to striking segre gation
from adults in the nonbreeding period (Kooyman et
al. 1996, Jorge et al. 2011, Riotte-Lambert & Weimers -
kirch 2013). However, this is not universal, and the
degree of segregation seems largely to stem from
among-species variation in adult movements, with
the greatest segregation in species where adults stay
close to colonies throughout the year (Grémillet et al.
2015, de Grissac et al. 2016). Juveniles often forage in
less productive waters than adults, which may be key
to explaining their lower survival probability (Thiebot
et al. 2013, Gutowsky et al. 2014, Jaeger et al. 2014).
Detailed analyses suggest that it may take juve-
niles several months to attain the flight ability of
adults (Riotte-Lambert & Weimerskirch 2013). In asso-
ciation with this, the structure of their movements
also differs markedly from adults, with evidence of
longer, more sinuous pathways in juveniles (Péron &
Grémillet 2013, Riotte-Lambert & Weimerskirch 2013,
Missagia et al. 2015, de Grissac et al. 2016). There is
considerable interest in how individuals are able to
navigate during this juvenile period (Guilford et al.
2011, Fayet et al. 2015, de Grissac et al. 2016). How-
ever, understanding the mechanisms is challenging
because of the lack of information on potential cues
(ocean features, presence of conspe cifics, etc.), but
detailed analyses of movements suggest extensive
variation among species in the relative importance of
inheritance, cultural mechanisms and acquired mem-
ory through exploration (Guilford et al. 2011, Péron &
Grémillet 2013, de Grissac et al. 2016).
The immaturity period between the juvenile (first
winter) phase and adulthood is also a challenge to
study. Device deployments are restricted to the few
species where immatures can be captured (generally
at colonies), as loggers and transmitters deployed on
feathers on the last occasion when these birds were
accessible on land (at or before fledging) remain
secure only until the first moult, and those attached
Phillips et al.: Individual variability in seabirds 123
Taxon Age Nonbreeding Breeding Foraging Foraging Dive Flight Reference
classesaseason season effort success charac- charac-
location location teristics teristics
Herring gull Larus argentatus I, A Y Greig et al. (1985)
J, I, A Y MacLean (1986)
Lesser black-backed gull Larus fuscus J, I, A Y Y Jorge et al. (2011)
Bonaparte’s gull Chroicocephalus philadelphia J, I, A Y MacLean (1986)
Ring-billed gull Larus delawarensis J, I, A Y MacLean (1986)
Gull species (Larus spp.) × 4 J, I, A Y Burger & Gochfeld (1981)
Gull spp. × 6 J, I, A Y Porter & Sealy (1982)
Auk spp. × 2 J, I, A Y Porter & Sealy (1982)
Sandwich tern Thalasseus sandvicensis J, older Y Dunn (1972)
Brown pelican Pelecanus occidentalis J, AbY Orians (1969)
Northern gannet Morus bassanus I, A Y Votier et al. (2011)
J, A N Grémillet et al. (2015)
Brown booby Sula leucogaster J Y Y Yoda et al. (2004)
Red-footed booby Sula sula J Y Guo et al. (2010)
European shag Phalacrocorax aristotelis J, A Y Daunt et al. (2007b)
Wandering albatross Diomedea exulans J Y Y Åkesson & Weimerskirch
J, I Y Y Weimerskirch et al. (2006)
J, I, A Y Y Y Riotte-Lambert & Weimers-
kirch (2013)
I, A Y Y Jaeger et al. (2014)
Shy albatross Thalassarche cauta J Y Alderman et al. (2010)
Black-footed albatross Phoebastria nigripes J, A Y Gutowsky et al. (2014)
Black-browed albatross Thalassarche melanophris I, A Y Y Petersen et al. (2008)
White-capped albatross Thalassarche steadi I, A Y Y Petersen et al. (2008)
Black-browed albatross Thalassarche melanophris I, A Y Campioni et al. (2015)
Northern giant petrel Macronectes halli J, A Y Trebilco et al. (2008)
Southern giant petrel Macronectes giganteus J, A Y Y Blanco et al. (2015)
J, A Y Trebilco et al. (2008)
Cory’s shearwater Calonectris borealis I, A Y Campioni et al. (2015)
Ix, Ex Y Y Missagia et al. (2015)
Manx shearwater Puffinus puffinus I, A N Y Fayet et al. (2015)
Scopoli’s shearwater Calonectris diomedea J, A N Grémillet et al. (2015)
J, I, A N Y Y Péron & Grémillet (2013)
Sooty shearwater species J, I, A Y Porter & Sealy (1982)
Procellariiformes spp. × 9 J, A Y/N Y de Grissac et al. (2016)
Emperor penguin Aptenodytes forsteri J Y Kooyman et al. (1996)
J Y Thiebot et al. (2013)
King penguin Aptenodytes patagonicus J, A Y Orgeret et al. (2016)
aStudies restricted to juveniles typically compare with adults based on past work/unpublished data. bFirst winter birds defined as immatures
Table 1. Studies testing for differences in foraging and migration among juveniles (first year, J), immatures (subsequent sub-adult age classes, I) and adult seabirds (A).
Ix = inexperienced; Ex = experienced; Y = yes (effect detected); N = no effect
Mar Ecol Prog Ser 578: 117–150, 2017
to leg rings require the individual to be recaptured
after return to the colony (Daunt et al. 2007b, de Gris-
sac et al. 2016). Tracking has demonstrated that
immatures show limited or no segregation from
adults during the nonbreeding season until the point
when adults return to colonies in preparation for
breeding (Petersen et al. 2008, Péron & Grémillet
2013). Older immatures may also associate with colo -
nies and operate as central-place foragers, al though
trip structure, trip duration and resource use differ
from those of breeding adults (Votier et al. 2011,
Riotte-Lambert & Weimerskirch 2013, Campioni et
al. 2015). However, immatures also undertake pros -
pecting movements, where they visit multiple colo -
nies either during the breeding season or autumn
migration, resulting in seasonal segregation from
breeding adults from the same site (Votier et al. 2011,
Péron & Grémillet 2013). In addition to these spatial
differences associated with key age-specific behav-
iours, immatures exhibit lower foraging efficiency
than adults (Fayet et al. 2015), supporting the theory
that the acquisition of foraging skills is a lengthy and
complex process in seabirds that may in part explain
the long immaturity phase.
An increase in reproductive success with age is
widespread among iteroparous breeders (Clutton-
Brock 1988, Newton 1989, Forslund & Pärt 1995).
One of the principal mechanisms underpinning this
pattern is an improvement in foraging performance
with age (Curio 1983). Seabirds show marked changes
in foraging performance in early life, and for some
species, the immature period may be sufficiently
long that individuals have reached full for aging
capability by the time they recruit into the breeding
population (Weimerskirch et al. 2005). Alternatively,
individuals may require additional skills or experi-
ence to forage successfully both for themselves and
their young (Haug et al. 2015).
Despite growing evidence of differences in forag-
ing performance between young and older breeders
(Table 2), there have been few definitive studies of
the underpinning mechanisms. Young breeders
may be less successful at foraging because they are
poorer at locating prey, physically less capable
(Curio 1983) or because they are showing restraint
because of their higher residual reproductive value
(Williams 1966). A further challenge is to establish
whether individuals improve their foraging perform-
ance with age, and if the higher average perform-
ance of older age classes is due to differential sur-
vival rates of individuals of differing foraging abili-
ties (Smith 1981, Nol & Smith 1987, Reid et al. 2010).
Longitudinal studies are therefore essential to es -
tablish the relative importance of within-individual
improvements and natural selection (Limmer &
Becker 2009). In addition, it has proved difficult to
tease apart age from experience, since the two are
closely correlated (Pärt 1995). Finally, most seabirds
breed seasonally, and younger individuals usually
breed later in the year and less successfully; as such,
intrinsic performance is potentially confounded by a
deterioration in environmental conditions later in the
season, and experimental approaches are required to
tease these processes apart (Daunt et al. 1999, 2007a).
Habitat use and foraging behaviour and efficiency
may vary among different age classes. Although pro-
gressive changes in habitat type with age during the
nonbreeding season have been detected using stable
isotope analyses (Jaeger et al. 2014), in another recent
study, there were no significant differences in migra-
tion destinations or strategies between adult age
classes (Pérez et al. 2014). More attention has focussed
on age-related foraging performance during the
breeding season (Table 2). In line with theory, young
breeders often obtain less food than older breeders
(Daunt et al. 2007a, Limmer & Becker 2009, Le Vaillant
et al. 2013), and their diet may be of lower quality
(Navarro et al. 2010), with impacts on chick growth
rates and reproductive success (Daunt et al. 2001,
Limmer & Becker 2009). Such patterns may result
from age-specific differences in foraging efficiency
(Daunt et al. 2007a, Limmer & Becker 2009). Older
breeders may have greater experience in locating
profitable feeding areas, as shown in Cory’s shearwa-
ter where site fidelity to productive areas was higher
in experienced age classes (Haug et al. 2015). Older
individuals may also have physical advantages; for
example, Le Vaillant et al. (2012, 2013) showed that
they dive deeper, experience reduced underwater
drag and undertake more prey pursuits than younger
breeders. Older breeders may increase foraging effort
to maximise chick provisioning rates, in particular
when environmental conditions are poor (Daunt et
al. 2007a). Alternatively, they may reduce foraging
effort, potentially to maximise time spent on other
activities such as resting or guarding the young
(Weimerskirch et al. 2005, Zimmer et al. 2011, Harris
et al. 2014a, Lewis et al. 2015, Le Vaillant et al. 2016).
Young individuals may increase foraging effort to
compensate for their reduced efficiency; for example,
Weimerskirch et al. (2005) showed that younger and
older breeders expended similar foraging effort dur-
Phillips et al.: Individual variability in seabirds 125
Taxon Age Ages Main Non- Breeding Timing Foraging Foraging Dive Flight Reference
classes comparison breeding location of effort success charac- charac-
location foraging teristics teristics
Common tern Sterna hirundo Y, M n/aaYM Y Limmer & Becker (2009)
Audouin’s gull Larus audouinii Y, M 4−11 YM Y Navarro et al. (2010)
Brünnich’s guillemot Uria lomvia Y, M, O 3−30 MO N Elliott et al. (2015)
European shag Y, M 2; >2 YM Y Y Daunt et al. (2007a)
Phalacrocorax aristotelis Y, M, O 2−3; 4−5; YM,MO N Grist et al. (2014)
6−7; 8−9; 10+
Y, M, O 2−19 YM,MO N Lewis et al. (2015)
Imperial shag Phalacrocorax Y, M 2−3; min 6−7bYM Y Y Harris et al. (2014a)
Wandering albatross Y, M 6−11; 12−30 YM Y Y Weimerskirch et al. (2005)
Diomedea exulans Y, M, O 6−48+ MO Y Y Lecomte et al. (2010)
Y, M, O 3−11; 7−29; > 29 YM, MO Y Y Jaeger et al. (2014)
Y, O 8−16; 25−37 MO N Froy et al. (2015)
Y, M, O 8−35+ MO N Froy et al. (2015)
Grey-headed albatross M, O <28; 35+cMO Y Y Catry et al. (2006)
Thalassarche chrysostoma
Cory’s shearwater M, O 13−20; > 26 MO Y Catry et al. (2011)
Calonectris borealis Y, M, O n/adYM, MO N Pérez et al. (2014)
Y, M 7−14; > 20bYM Y Haug et al. (2015)
King penguin Y, M 5; 8−9 YM Y Le Vaillant et al. (2012)
Aptenodytes patagonicus Y, M 5; 9 YM Y Y Y Le Vaillant et al. (2013)
Y, M 4−11 YM Y Le Vaillant et al. (2016)
Little penguin Eudyptula Y, M, O 3−4; 5−10; 11−14 YM, MO Y Zimmer et al. (2011)
minor M, O 5−11; 12−18 MO Y N N Pelletier et al. (2014)
aCategorised as new recruit vs. experienced breeder. bCategorised as inexperienced vs. experienced. cMiddle-aged group, lower boundary = minimum 4 yr of breeding
experience. dAges not provided
Table 2. Studies testing for age-specific differences in foraging and migration among adult seabirds. Age classes: young (Y), middle-aged (M), old (O). +: minimum age. Main
comparison classed either as young vs. middle-aged (YM) or middle-aged vs. old (MO)
Mar Ecol Prog Ser 578: 117–150, 2017
ing daylight, but younger breeders foraged more at
night. However, interpretation of foraging effort is
challenging in the absence of data on foraging effi-
ciency (requiring data on energy expenditure, mass
and quality of prey, etc.), since it is not clear whether
increased effort might be a compensation for poor ef-
ficiency or, alternatively, if it maximises energy gain
when efficiency is high. Further, such patterns are
probably context dependent, with age-specific patterns
in foraging effort and efficiency likely to be more pro-
nounced during poor environmental conditions (Daunt
et al. 2007a).
Considering the opposite end of the breeding life-
span, there is widespread evidence that senescence
leads to a decline in breeding success in the oldest
age classes (Froy et al. 2013, Nussey et al. 2013). Al-
though the mechanisms underpinning these patterns
are poorly understood, the most frequent explanation
is a reduction in foraging performance with age due
to physiological declines, reducing the resources that
can be allocated to reproduction. Accordingly, studies
have shown marked differences in the foraging per-
formance of the oldest breeding age classes in com-
parison with middle-aged birds (Table 2). Catry et al.
(2006) showed that old grey-headed albatrosses un-
dertook longer trips and gained less mass than mid-
dle-aged birds. Similarly, old male wandering alba-
trosses undertook longer trips to remote foraging
grounds and showed less foraging activity (Lecomte
et al. 2010). In little penguins Eudyptula minor, there
is spatial segregation be tween old and middle-aged
breeders during foraging, and the oldest age classes
show reduced diving effort (Zimmer et al. 2011, Pel-
letier et al. 2014). Differences in effort were also
apparent in a study of Cory’s shearwaters, where old
individuals undertook fewer take-offs and landings
(which are energetically expensive) and spent more
time resting on the water (Catry et al. 2011).
Some studies have linked differences in activity
budgets and foraging patterns between young and
old birds to physiological declines (Catry et al. 2011),
but others have found no physiological changes and
instead interpreted this variation in terms of differ-
ences in foraging efficiency (Lecomte et al. 2010,
Weimerskirch et al. 2014). However, for reasons dis-
cussed above with regard to comparisons between
young and old individuals, interpretation of indices
of foraging effort is not straightforward in the
absence of information on energy gain. Low foraging
effort in old birds may indicate poor physical fitness,
resulting from physiological senescence, or may be
due to high foraging efficiency, linked to experience
(Catry et al. 2011, Froy et al. 2015). Furthermore,
age-related declines in foraging performance are not
universal; foraging behaviour of old Brünnich’s
guillemots Uria lomvia did not differ from younger
adults, despite evidence for physiological senescence
(Elliott et al. 2015). Age-related effects can also vary
with region; in contrast to results from wandering
albatrosses tracked in the Indian Ocean (Lecomte et
al. 2010), there was very limited evidence for age-
related variation in foraging in the same species in
the southwest Atlantic, which was attributed to po -
tential differences in oceanographic conditions (Froy
et al. 2015). The ability to tease apart the effects of
age from those of extrinsic conditions would be
enhanced considerably by longitudinal approaches
that examine within-individual changes over time
(Limmer & Becker 2009, Daunt et al. 2014).
Implications for population dynamics
and conservation
Despite limited evidence to date, age-specific varia-
tion in foraging and migration is likely to have impor-
tant effects on individual fitness. In turn, heterogene-
ity in fitness among age classes will have profound
consequences for population dynamics (Caswell 2001).
One important mechanism underpinning these links
is the interaction with extrinsic effects, whereby very
young or very old individuals may be disproportion-
ately impacted by poor environmental conditions be-
cause of lower foraging efficiency (Sydeman et al.
1991). These differences may arise from age-specific
variation in susceptibility, or differences in distribution
or scheduling of migration of very young or old indi-
viduals, leading to heterogeneity in environments ex-
perienced. A key factor in quantifying effects on pop-
ulation dynamics is the extent to which age-related
variation in foraging and migration is due to ageing
effects (longitudinal changes in individuals),or pro-
gressive appearance and disappearance of different
phenotypes in the population (Limmer & Becker 2009,
Reid et al. 2010). Long-term deployments of loggers
provide opportunities to distinguish these possibilities
(Daunt et al. 2014). Effects of ageing and its inter -
action with the environment may have important
im pli cations for conservation. Age-specific variation
in migration destinations could lead to differential ex-
posure to anthropogenic effects such as pollution or
fisheries. Equally, marine protection could benefit
some age classes more than others. Conservation and
management initiatives could potentially target those
individuals that make the highest contribution to pop-
ulation growth rate (Moreno 2003).
Phillips et al.: Individual variability in seabirds
General patterns and drivers
Sexual segregation of male and female birds dur-
ing foraging and migration is widespread and occurs
at a range of temporal and spatial scales (Catry et al.
2005). One of the earliest studies highlighting sexual
segregation in seabirds was on the wandering alba-
tross, based on at-sea distributions of birds sexed by
plumage (Weimerskirch & Jouventin 1987); this find-
ing was later confirmed using satellite-telemetry
(Prince et al. 1992, Weimerskirch et al. 1993). Sexual
segregation can also involve a preference by one sex
for a particular microhabitat (Table 3). In many bird
families, males winter closer and return sooner to the
breeding grounds than females (Cristol et al. 1999,
Catry et al. 2005). An extensive, but non-exhaustive
review of the recent literature on sex differences in
foraging and migration since the review by Phillips et
al. (2011) is provided in Table 3. Note that due to the
nature of the literature search (where sex, seabirds,
foraging or migration were included in the search
topic in Web of Science), there may be a bias towards
those studies that found positive sex differences.
Male and female seabirds may differ in scheduling
of migration. Female black-browed albatrosses began
migration 1 to 2 wk earlier than males and wintered
further north (Phillips et al. 2005). The same pattern
appears to be consistent across years in brown skuas
Stercorarius antarcticus (Carneiro et al. 2016). In
3 species of crested penguins Eudyptes sp., males
began migrating back to the breeding colonies ear-
lier than females (Thiebot et al. 2014b). Recent tech-
nological advances have facilitated similar studies on
smaller seabirds, which usually show a lower degree
of sexual size dimorphism or are monomorphic
(Table 3).
There are within-pair effects that appear to be
unrelated to sex; for example if there is assortative
mating of partners with similar strategies according
to arrival dates. In the Scopoli’s shearwater Calonec-
tris diomedea, pair members do not migrate together
but spend a similar number of days travelling to and
from similar (but not identical) terminal nonbreeding
areas (Müller et al. 2015). This was attributed to
shared genes, given that pairs breeding in close
proximity within the same colony (which were pre-
sumed to be more closely-related) also appeared to
have similar migration strategies. In addition, paired
Kerguelen shags showed some similarity in distribu-
tion and behaviour (Camprasse et al. 2017c, this
Theme Section). Further, there was pair-wise segre-
gation in wintering niche (spatial and isotopic) in the
southern rockhopper penguin Eu dyptes chrysocome
but no clear sexual segregation (Thiebot et al. 2015).
The general consensus is that sexual segregation
arises either from social dominance and competitive
exclusion by the dominant (often larger) sex, or by
habitat or niche specialization due to differences in
morphology or reproductive role (Peters & Grubb
1983). Social dominance and competitive exclusion
are particularly prevalent in dimorphic species where
one sex has an obvious physical advantage, but there
is increasing evidence for sex differences in mono -
morphic species as well (Lewis et al. 2002, Pinet et al.
2012, Hedd et al. 2014). A classic example of social
dominance is where larger, male giant petrels Macro -
nectes spp. dominate scavenging opportunities at seal
and penguin carcasses on land, where interference
competition clearly occurs, forcing females to prima-
rily forage at sea (González-Solís et al. 2000). In con-
trast, male and female black-browed and grey-headed
albatrosses are highly segregated during incubation
but not during brood-guard or post-chick rearing;
given that there were sex-specific differences in
flight performance but no obvious role of competitive
exclusion by the larger males, the seasonal segre -
gation was attributed to niche divergence (Phillips et
al. 2004).
In a recent review exploring the potential drivers or
correlates of sexual segregation, stable isotope ratios
rarely differed between males and females in mono -
morphic species, implying a link between sexual size
dimorphism and segregation in diet or distribution
(Phillips et al. 2011). Also, differences in δ13C (reflect-
ing carbon source) in albatrosses in the Southern
Ocean suggested the underlying mechanism was re-
lated to habitat specialization, whereas in other size-
dimorphic species (both male- and female-biased),
sex differences were more commonly in δ15N than
δ13C, which is more consistent with size-mediated
competitive exclusion or dietary specialization. Man -
cini et al. (2013) found no correlation between indices
of sexual size dimorphism and differences in mean
δ15N or δ13C values in males and females for 6 tropical
and 5 polar seabird species, yet their review indicated
that 70% of studies on di morphic seabird species from
temperate and polar regions showed some degree of
trophic or spatial segregation between sexes, com-
pared to only 20% of studies on dimorphic species in
the tropics. Therefore, sexual size dimorphism ap-
pears to facilitate trophic or spatial segregation, par-
ticularly in high latitude seabirds (potentially related
to more intense competition for resources during the
shorter breeding season); however, even in those re-
Mar Ecol Prog Ser 578: 117–150, 2017
Taxon Mean adult Dimorphism Wintering Timing of Foraging
mass (kg) of index location migration location
males (females)a
Brown skua Stercorarius antarcticus 1.765 (1.973) [17] −0.056 N Y
1.765 (1.973) [17] −0.056 N
1.765 (1.973) [17] −0.056 N Y
Audouin’s gull Larus audouinii 0.580 (0.492) [18] 0.082 Y*
Lesser black-backed gull Larus fuscus 0.941 (0.776) 0.096 Y
Black-legged kittiwake Rissa tridactyla 0.400 (0.400) [7] 0.000 Y N
Brünnich’s guillemot Uria lomvia 0.990 (1.000) [7] −0.005
Atlantic puffin Fratercula arctica 0.480 (0.510) [7] −0.030 Y
Christmas Island frigatebird Fregata andrewsi 1.400 (1.550) [7] −0.051 Y**, Y*
Australasian gannet Morus serrator 2.600 (2.520) [12] 0.016 N
2.510 (2.690) −0.035 Y
2.600 (2.520) [12] 0.016
Northern gannet Morus bassanus 2.956 (3.209) −0.041 N Y*
2.930 (3.070) [7] −0.023 N Y
2.810 (3.021) −0.036 Y
Cape gannet Morus capensis 2.705 (2.715) [13] −0.002
Masked booby Sula dactylatra 2.059 (2.470) −0.091
Imperial shag Phalacrocorax atriceps 2.810 (2.210) 0.120 Y
2.285 (1.929) [14] 0.084 Y
2.285 (1.929) 0.084
2.810 (2.210) [15] 0.120
2.285 (1.929) [14] 0.084 Y
South Georgia shag Phalacrocorax georgianus 2.600 (2.160) 0.092
Kerguelen shag, Phalacrocorax verrucosus 2.429 (2.133) 0.065 N
European shag Phalacrocorax aristotelis 1.928 (1.636) [16] 0.082 N
1.940 (1.600) [7] 0.096 Y
1.928 (1.636) 0.082
Wandering albatross Diomedea exulans 9.768 (7.686) [6] 0.119
9.768 (7.686) [6] 0.119 Y
9.768 (7.686) [6] 0.119 Y
9.768 (7.686) [6] 0.119
9.768 (7.686) [6] 0.119 Y Y
9.768 (7.686) [6] 0.119 Y
9.768 (7.686) [6] 0.119 Y
9.768 (7.686) [6] 0.119 Y
Black-browed albatross Thalassarche 3.650 (2.970) 0.103 Y
Southern giant petrel Macronectes giganteus 5.190 (3.940) [7] 0.137 Y Y
Northern giant petrel Macronectes halli 5.000 (3.800) [7] 0.136 Y Y
Barau’s petrel Pterodroma baraui 0.380 (0.380) 0.000 Y*
Scopoli’s shearwater Calonectris diomedea 0.676 (0.569) [8] 0.086 Y Y
0.676 (0.569) 0.086 Y
Cory’s shearwater Calonectris borealis 0.880 (0.810) [9] 0.041 Y
0.880 (0.810) [9] 0.041 Y
Streaked shearwater Calonectris leucomelas 0.549 (0.482) [10] 0.065 Y
0.549 (0.482) [10] 0.065 Y
Sooty shearwaters Ardenna grisea 0.897 (0.881) 0.009 N Y*
Balearic shearwater Puffinus mauretanicus 0.509 (0.495) [11] 0.014 N
King penguin Aptenodytes patagonicus 13.981 (12.782) 0.045
Adélie penguin Pygoscelis adeliae 5.350 (4.740) [1] 0.060
Chinstrap penguin Pygoscelis antarctica 4.980 (4.470) [1] 0.054
Gentoo penguin Pygoscelis papua 5.500 (5.060) [1] 0.042
5.500 (5.060) [1] 0.042 N
Southern rockhopper penguin Eudyptes c. 3.917 (3.869) 0.006 Y
chrysocome 3.917 (3.869) [2] 0.006 N Y
3.917 (3.869) [2] 0.006 Y
Eastern rockhopper penguin Eudyptes 3.050 (2.980) [3] 0.012 Y
chrysocome filholi
Northern rockhopper penguin Eudyptes 2.960 (3.120) [1] −0.026
chrysocome moseleyi 2.960 (3.120) [1] −0.026 Y
Macaroni penguin Eudyptes chrysolophus 4.650 (4.890) [1] −0.025 Y
4.650 (4.890) [1] −0.025 Y Y
African penguin Spheniscus demersus 3.452 (2.996) 0.071 Y**
Magellanic penguin Spheniscus magellanicus 3.800 (3.000) 0.118
4.490 (3.709) [4] 0.095
4.490 (3.709) [4] 0.095 N
Humboldt penguin Spheniscus humboldti 4.100 (3.200) 0.123
Little penguin Eudyptula minor 1.172 (1.048) [1] 0.056 N
1.247 (1.119) [5] 0.054
Table 3 (this and the next page). Studies testing for sex differences in foraging and migration strategies in seabirds since 2011.
Dimorphism index = (mean male mass − mean female mass)/(mean male mass + mean female mass), where positive values in-
dicate sexual size dimorphism (SSD), and negative values indicate reverse sexual size dimorphism (RSD). Diet (trophic level)
aMean adult body mass was taken from the reference in the final column (if available); otherwise, it was extracted from the
following sources: [1]Borboroglu & Boersma (2015), [2]Ludynia et al. (2013), [3]J.B. Thiebot pers. comm., [4]Forero et al. (2001),
[5]Salton et al. (2015), [6]Tickell (1968), [7]Schreiber & Burger (2002), [8]Müller et al. (2015), [9]Ramos et al. (2009), [10]Ochi et al.
Phillips et al.: Individual variability in seabirds 129
Timing Diving Flight Diet Diet Breeding No. Reference
of charac- (trophic (carbon stage years
foraging teristics level) source) in study
NB 2 Carneiro et al. (2016)
BR 1 Carneiro et al. (2014)
Y NB 3 Krietsch et al. (2017), this Theme Section
N N BR 1 García-Tarrasón et al. (2015)
BR 4 Camphuysen et al. (2015)
NB 1 Bogdanova et al. (2011)
Y Y* BR 1 Elliott & Gaston (2015)
NB 7 Fayet et al. (2016)
BR 2 Hennicke et al. (2015)
N N BR 3 Machovsky-Capuska et al. (2014)
BR 1 Wells et al. (2016)
Y~ BR 3 Machovsky-Capuska et al. (2016)
Y Y NB, BR 3 Stauss et al. (2012)
NB 2 Fifield et al. (2014)
Y Y BR 3 Cleasby et al. (2015)
Y BR 2 Rishworth et al. (2014b)
Y Y BR 1 Sommerfeld et al. (2013)
Y** BR 3 Quillfeldt et al. (2011)
N Y N BR 1 Quintana et al. (2011)
Y* NB, BR 1 Harris et al. (2013)
Y Y NB, BR 3 Michalik et al. (2013)
BR 4 Harris et al. (2014b)
Y BR 3 Ratcliffe et al. (2013)
N N N BR 2 Camprasse et al. (2017a)
NB 3 Grist et al. (2014)
BR 3 Soanes et al. (2014)
Y* NB, BR 3 Lewis et al. (2015)
N Y*** NB, BR 1 Ceia et al. (2012)
NB 1 Åkesson & Weimerskirch (2014)
BR 1 Carravieri et al. (2014)
Y Y NB, BR 1 Jaeger et al. (2014)
Y Y NB, BR 24 Weimerskirch et al. (2014)
NB 15 Weimerskirch et al. (2015)
BR 6 Cornioley et al. (2016)
BR 22 Jiménez et al. (2016)
BR 1 Patrick et al. (2014)
NB, BR 1 Thiers et al. (2014)
NB, BR 1 Thiers et al. (2014)
Y NB*, BR 3 Pinet et al. (2012)
NB 3 Müller et al. (2014)
NB 3 Müller et al. (2015)
NB 6 Pérez et al. (2014)
NB 3 Pérez et al. (2016)
NB*, BR 1 Yamamoto et al. (2011)
NB 5 Yamamoto et al. (2014)
NB, BR 1 Hedd et al. (2014)
BR 4 Meier et al. (2015)
Y Y N BR 1 Le Vaillant et al. (2013)
N N NB* 3 Gorman et al. (2014)
Y N NB* 3 Gorman et al. (2014)
Y N NB* 3 Gorman et al. (2014)
N Y N BR 1 Camprasse et al. (2017b), this Theme Section
Y BR 1 Ludynia et al. (2013)
N N NB 1 Thiebot et al. (2015)
Y Y Y BR 3 Rosciano et al. (2016)
NB 2 Thiebot et al. (2014b)
Y* Y* BR 1 Booth & McQuaid (2013)
NB 2 Thiebot et al. (2014b)
NB 2 Thiebot et al. (2014b)
N N NB Thiebot et al. (2014a)
Y BR 2 Pichegru et al. (2013)
Y BR 1 Rey et al. (2013)
N Y*** NB 1 Silva et al. (2014)
N N N BR 3 Rosciano et al. (2016)
Y BR 1 Rey et al. (2013)
N N N BR 1 Pelletier et al. (2014)
N Y~ Y** BR 9,17 Chiaradia et al. (2016)
based on δ15N, unless indicated otherwise by ‘~’ representing conventional diet analysis. Diet (carbon source) based on δ13C. BR =
breeding season; NB = nonbreeding season; NB* = pre-laying. Asterisks after (Y) indicate that sex specific differences only oc-
curred (*) during certain periods of the reproductive stage, (**) in certain years, (***) in some tissues (blood, bones or feathers)
(2010), [11]Genovart et al. (2003), [12]G. E. Machovsky-Capuska pers. comm., [13]Rishworth et al. (2014a), [14]Harris et al. (2013),
[15]Quillfeldt et al. (2011), [16]Lewis et al. (2015), [17]Phillips et al. (2002), [18]Ruiz et al. (1998)
Mar Ecol Prog Ser 578: 117–150, 2017
gions, this pattern is not ubiquitous (Phillips et al.
2007, Young et al. 2010, Mancini et al. 2013) (Table 3).
Sexes may also segregate by exploiting prey at
different depths, as shown in early studies on cor-
morants or shags Phalacrocorax spp., in which males
made deeper and longer dives than females (Wanless
et al. 1995, Kato et al. 2000). More recently, Quintana
et al. (2011) used GPS and dive recorders simultane-
ously and found that female imperial shags Phalacro-
corax atriceps foraged in shallow coastal waters,
whereas males preferred deeper offshore waters.
The authors suggested that this finding reflected the
preference by each sex for foraging at depths that
maximised their respective foraging efficiencies. In
line with this hypothesis, sex differences in foraging
behaviour and dive depths in northern gannets
Morus bassanus appear to indicate sex-specific habi-
tat segregation, but in this case, males foraged
mostly in mixed, shallow coastal waters and females
in stratified, deeper offshore waters (Lewis et al.
2002, Cleasby et al. 2015).
The sexes may also segregate temporally by under-
taking foraging trips at different times of the day. In
sexually dimorphic cormorants, males preferentially
forage in the afternoon (Wanless et al. 1995, Kato et
al. 2000, Harris et al. 2013). Links between time of
day and foraging patterns are also evident in mono -
morphic species, including the Brünnich’s guillemot
Uria lomvia, which exhibits strong sex-specific diur-
nal schedules, with one sex foraging mostly at night
and the other mostly at midday (Jones et al. 2002,
Paredes et al. 2008, Elliott et al. 2010). Diurnal pat-
terns of foraging in this species also resulted in spa-
tial segregation, as males (which mostly forage at
night) made shallower dives than females (in the
late afternoon), presumably because males specialize
on shallow prey normally found at night (Elliott &
Gaston 2015).
As with effects of age, the effects of sex may be
apparent only in some years. Sex differences in for-
aging location and diving behaviour were detected
in one year in the sexually dimorphic Japanese cor-
morant, Phalacrocorax capillatus, but not in the fol-
lowing year when food was abundant, suggesting
that segregation is more likely during intense intra-
specific competition (Ishikawa & Watanuki 2002).
More recently, Quillfeldt et al. (2011) showed in a
multi-year study during chick rearing that larger
male imperial shags dived deeper than females in
some years but not others, though the mechanism
was unclear.
Similarly, sex-specific foraging differences may
vary with environmental conditions within years.
Smaller female European shags, Phalacrocorax aris-
totelis, foraged for longer than males during strong
onshore winds, but not at lower wind speeds (Lewis
et al. 2015). In contrast, there was no evidence that
tide or weather influenced foraging behaviour of
either sex in the Brünnich’s guillemot (Elliott & Gas-
ton 2015). In other taxa, sexual segregation appears
to be related more obviously to sex differences in
reproductive roles (see following section).
Interactions between sex and stage of the
annual cycle
Although males and females share their breeding
duties to a similar extent in most seabirds, intersex-
ual competition for food, differences in energetic or
nutritional requirements, or different parental roles
can lead to sexual differences in foraging behaviour
during specific periods. Sex differences in stable iso-
tope ratios are more likely during the pre-laying and
later breeding periods than during the nonbreeding
period (Phillips et al. 2011). Tracking studies also
show that the sexes may segregate by location (Stauss
et al. 2012) or time of day (Harris et al. 2013) during
the breeding but not the nonbreeding season. These
results imply that sex differences in foraging strate-
gies are more likely when males and females have
different reproductive roles and when potential com-
petition and partitioning of resources between sexes
are probably higher (but see Silva et al. 2014).
During the pre-laying period, males and females
frequently differ in their diet or distribution, as indi-
cated, for example, by sexual differences in isotope
ratios (Phillips et al. 2011). Males (which usually per-
form a greater role in nest defence) often forage more
locally and visit the colony more frequently, whereas
females often go on a pre-laying exodus, engaging in
longer foraging trips in more productive waters to
meet energetic or other nutritional requirements for
the clutch (Lewis et al. 2002, Yamamoto et al. 2011,
Hedd et al. 2014, Quillfeldt et al. 2014, Pistorius et al.
2015). Indeed, changing energetic or nutritional
requirements during the breeding cycle would ex -
plain why sex differences are apparent only at cer-
tain stages in mono morphic species such as Barau’s
petrel Pterodroma baraui (Pinet et al. 2012) or why
late-incubation trips by male southern rockhopper
penguins are longer, as they do all the early chick-
guarding (Ludynia et al. 2013). In theory, such differ-
ences seem less likely if the male courtship feeds the
female, potentially contributing substantially to
clutch formation as in terns, gulls and skuas (Becker
Phillips et al.: Individual variability in seabirds
& Ludwigs 2004), but this does not seem to be the
case in the brown skua, as a higher proportion of
females than males undertake a pre-laying exodus
(Carneiro et al. 2016). In contrast, in some species
(including gadfly petrels), males perform longer for-
aging trips than females, perhaps to prepare them-
selves for the typically-long fasting bout post-laying
(Pinet et al. 2011, Rayner et al. 2012), and in the
black-legged kittiwake, males are more likely than
females to perform a pre-laying excursion, although
the reason for this is unclear (Bogdanova et al. 2011).
Sexual differences in foraging patterns may extend
into the incubation period, possibly due to the re -
quirement for females to replenish the energy, essen-
tial nutrients or minerals spent in clutch formation.
Hence, females may perform particularly long or dis-
tant foraging trips after laying (Lewis et al. 2002,
Phillips et al. 2004). The emperor penguin Apteno -
dytes forsteri is an ex treme example; the male incu-
bates the egg until hatching (60−70 d), while the
female forages to recover from egg formation and to
gather food to feed the chick just after hatching
(Williams 1995). After hatching in some penguins
and alcids, males brood the chick while the females
forage to pro vide meals for the offspring (Clarke et
al. 1998, Tremblay & Cherel 2003, Paredes et al. 2006,
Green et al. 2009); the reverse occurs in some terns
(Becker & Ludwigs 2004).
During chick-rearing, some species show sexual
differences in chick provisioning rates. Usually,
these differences involve more frequent visits or
larger meals from the male (Catry et al. 2005, Thax-
ter et al. 2009, Welcker et al. 2009), perhaps reflect-
ing de ferred costs of egg production in females or
sex-specific allocation of foraging effort between
parents and offspring (Monaghan et al. 1998, Thax-
ter et al. 2009). In Cape gannets Morus capensis,
females undertake a greater proportion of long trips
than males (Pistorius et al. 2015). In the Manx
shearwater Puffinus puffinus, only females adopt
the dual foraging strategy, whereas males perform
short foraging trips and provision chicks at a higher
rate (Gray & Hamer 2001). In several alcids, the role
of males in provisioning chicks increases during
later rearing or in the post-fledging period, when
males forage closer to the colony, dive longer and
deeper per day and are forced to forage at lower-
quality prey patches than females (Harding et al.
2004, Thaxter et al. 2009, Elliott et al. 2010, Burke et
al. 2015). Although sex differences usually decrease
or disappear after the breeding period, with males
and females showing similar distribution and forag-
ing behaviour, in some species, sexual segregation
in trophic niches persists year-round (Phillips et al.
2005, 2011). Males and females can differ in moult-
ing strategies (Hunter 1984, Weimerskirch 1991),
which in theory might result in different dietary
needs or foraging behaviour, but this has not been
investigated so far.
Interactions between sex and other factors
Sex-specific patterns of migration and foraging
may involve interactions with various other intrinsic
factors. For example, trip duration in the common
guillemot Uria aalge during incubation was longer
in low-quality females, i.e. those with consistently
lower long-term breeding success (Lewis et al. 2006).
There can also be interactions with age; older female
king penguins Aptenodytes patagonicus conducted
shorter trips, dived deeper and performed more prey
pursuits during the chick rearing phase and also had
higher blood δ15N than younger females (Le Vaillant
et al. 2013). As adults, male but not female wander-
ing albatrosses forage progressively farther south
with increasing age (Lecomte et al. 2010, Jaeger et
al. 2014).
Implications for population dynamics and
If sexual segregation in foraging or migration
behaviour has fitness consequences and if such
behaviour is heritable, there may be important
evolutionary consequences (Grémillet & Char-
mantier 2010). However, as far as we are aware,
no seabird study has determined the heritability of
sex-specific foraging and migration strategies. Sex-
ual segregation can have important implications
for population dynamics and conservation if there
are fitness costs associated with foraging location.
One principal mechanism is that segregation leads
to differing foraging efficiencies, with demographic
consequences (Jaeger et al. 2014). Sex-specific
variation in demographic rates could also arise from
differential association with anthropogenic factors
that have impacts on survival rates. Sexual segre-
gation of wandering and other albatrosses affects
the relative vulnerability of males and fe males to
bycatch by pelagic longline fleets (Bugoni et al.
2011, Jiménez et al. 2014, Gianuca et al. 2017).
Sexual segregation can also affect the relative risk
of exposure to organic contaminants (Carravieri et
al. 2014).
Mar Ecol Prog Ser 578: 117–150, 2017
Patterns of individual specialization:
incidence and types
Individual specialization is generally regarded as
the variation among individuals, in terms of distribu-
tion, behaviour, diet or other aspects of resource
acquisition, that remains after accounting for the
group effects outlined above (Bolnick et al. 2003, Dall
et al. 2012). Specialization is often used to describe
consistency in some aspect of the behaviour of an
individual, but there is no consensus as to the mini-
mum period over which that has to be maintained or
the extent to which it may just reflect stability in the
environment. The advantages and disadvantages of
different approaches commonly used to detect and
quantify individual specialization using conventional
diet, stable isotope or tracking data are reviewed by
Carneiro et al. (2017). To illustrate the diversity of
research and to explore taxonomic, biogeographic
and other patterns, we carried out a non-exhaustive
review of studies that tested for individual specializa-
tion (Table 4). This expands on a previous review by
Ceia & Ramos (2015) and includes studies examining
fidelity to foraging sites, staging areas or routes
during the breeding or nonbreeding seasons, and
consistency in breeding-season trip characteristics,
migration schedules, diving patterns and other aspects
of at-sea activity, habitat use, diet or trophic level in
the short or long term (Table 4).
Prior to the last decade, statistical analyses of char-
acteristics that might reflect individual specialization
were rare, although a number of studies documented
consistent spatial segregation among individuals that
were tracked for a sufficient length of time during the
breeding (Irons 1998, Hedd et al. 2001) or nonbreed-
ing seasons (Croxall et al. 2005). For example, in a
study on grey-headed albatrosses, all were success-
ful breeders from the same subcolony but showed
diverse movement strategies during the 16 mo non-
breeding period, from largely resident in the south-
west Atlantic Ocean to repeated use of the southwest
Indian Ocean or more distant regions in successive
winters (Croxall et al. 2005). As devices have become
smaller and cheaper, many more seabird studies
have shown that individuals repeatedly use the same
foraging areas (i.e. show high site fidelity) in succes-
sive trips during the breeding season or in multiple
nonbreeding seasons, or show consistency in depar-
ture bearing or other trip characteristics (Table 4).
High nonbreeding site fidelity at a fine scale has also
been determined using colour-ring resightings (Grist
et al. 2014). Few studies have examined site fidelity
among rather than within breeding seasons (but see
Wakefield et al. 2015, Patrick & Weimerskirch 2017).
During the nonbreeding season, individuals of most
species tracked to date (15 of 20; see Table 4) showed
a very high degree of foraging site fidelity at the
regional level, with the notable exceptions of a small
proportion of Cory’s shearwaters, sooty shearwaters
Ardenna grisea, long-tailed skuas Stercorarius longi -
caudus and 2 species of guillemots (Dias et al. 2011,
Hedd et al. 2012, McFarlane Tranquilla et al. 2014,
van Bemmelen et al. 2017, this Theme Section).
Site fidelity is usually considered to arise in sea-
birds either through a ‘win-stay, lose-shift’ strategy
that is optimal if there is high spatio-temporal corre-
lation in resource availability or through the benefit
of site familiarity (Irons 1998, Wakefield et al. 2015).
The incidence of site fidelity appears to be lower
in the breeding than in the nonbreeding season
(Table 4), but this is at least partly an issue of spatial
scale and accuracy of different tracking devices: GPS
loggers or satellite-transmitters for breeding birds
and geolocators for nonbreeding birds. In around
half of the species tracked in multiple years, site
fidelity of nonbreeding birds was much lower at the
mesoscale than the regional level, and there was
often little or no consistency in the use of staging
areas and migration routes (Table 4). Black-browed
albatrosses from South Georgia were consistent in
the centroid of their terminal wintering area, but
not in the use of staging sites (Phillips et al. 2005);
Scopoli’s shearwaters showed significant repeatabil-
ity in wintering region and some (but not all) aspects
of migration schedule but not in the most westerly
longitude reached during the return journey (Müller
et al. 2014); long-tailed skuas were generally faith-
ful to staging and wintering area and to migration
routes, but as the winter progressed, a small but in -
creasing number of individuals began to deviate
from their route in previous years (van Bemmelen et
al. 2017). Migration schedules (i.e. timing of depar-
ture and return to the colony and timing of major
movements during the winter) were usually consis-
tent within individuals across years, having excluded
the influence of changes in breeding success or
status (see Table 4). Migration timing can be affected
by extrinsic factors; relative consistency in date of
arrival at the colony among individual Desertas
petrels Pterodroma deserta was attributed to poten-
tial delays because unfavourable winds increased
return time from more distant regions or because
birds waited for a bright moonlight night before
departing (Ramirez et al. 2016).
Phillips et al.: Individual variability in seabirds
All studies that tested for individual consistency in
foraging behaviour have found evidence for this in
terms of diving depth, diving or flight bout duration,
proportion of daylight and darkness spent in flight,
landing rate, etc. (Table 4). However, this may reflect
a positive publication bias. The degree of individual
variability can also change seasonally; in the impe-
rial shag, there is an effect of photoperiod (and
hence daylight available for foraging) and degree of
constraint associated with breeding or moulting, on
the relative consistency in the time that foraging
begins and ends each day (Harris et al. 2013,
2014b). Results from conventional stomach contents
or stable isotope ratios indicate significant consis-
tency within individuals in many species in habitat
use, prey type or trophic level in the short or long
term (days to weeks, between the breeding and
nonbreeding seasons or annual); however, there
were exceptions, particularly among the albatrosses
and petrels (Table 4).
Drivers of individual specialization:
influence of species and sex
Individual specialization in some form has been
recorded in all orders of seabirds (Sphenisciformes,
Procellariiformes, Pelecaniformes and Charadriiformes)
but only half of the families (Spheniscidae, Dio -
medeidae, Procellariidae, Sulidae, Phlacrocoracidae,
Stercorariidae and Laridae, but not Pelecanoididae,
Hydrobatidae, Fregatidae, Phaethontidae, Sternidae
and Rhynchopidae) (Table 4). This likely reflects a
research bias, with fewer studies on tropical seabirds
and less tracking of smaller species because of the
greater impacts of devices on these birds. The corre-
spondence between the presence or absence of indi-
vidual specialization and phylogeny or region is
therefore unclear; nevertheless, all 10 studies to date
that tested for individual specialization in diverse
aspects of movement and foraging behaviour of cor-
morants and shags have found evidence for its exis-
tence, suggesting that it is the dominant pattern in
those taxa (Table 4).
Several studies have compared the degree of site
fidelity or behavioural consistency between males
and females, but results do not show a clear pattern.
Long-term consistency in habitat use was greater in
male than in female wandering albatrosses, possibly
because females shift distribution to the north to
reduce competition with males in the nonbreeding
period (Ceia et al. 2012). Female imperial shags were
less variable in the timing of foraging and other trip
characteristics, attributed to the lower costs of forag-
ing in males and hence their greater discretionary
time for accommodating the female, which typically
takes the first foraging shift each day (Harris et al.
2013, 2014b). In Kerguelen shags Phalacrocorax ver-
rucosus, males were less specialized in diving behav-
iour than females (Camprasse et al. 2017a). Similarly,
males showed more variability in dive depths in
South Georgia shags Phalacrocorax georgianus, pos-
sibly because maximum dive depth is more closely
correlated with body mass in females (Ratcliffe et al.
2013). Female Audouin’s gulls Larus audouinii for-
aged at sea throughout the week, whereas males
switched from foraging at sea during weekdays to
inland coastal habitats (rice fields) on weekends,
when fisheries discards were unavailable (García-
Tarrasón et al. 2015). In other studies, there were no
differences in behavioural consistency or wintering
site fidelity between sexes (Grist et al. 2014, Potier et
al. 2015), or there were sex differences in consis-
tency, but the direction depended on the parameter
(Müller et al. 2014).
Extrinsic explanations for individual specialization:
influence of prey predictability
Individual specialization appears to be widespread
in cormorants and shags (Table 4). This seems likely
to be related to their exploitation of benthic prey,
which may be constrained in terms of seabed habi-
tat. Such habitats contain numerous static features,
en abling foraging birds to memorize topographic
cues to improve encounter rate. Differing degrees of
spatial and temporal predictability of resources
might also explain relative fidelity to foraging sites
in more pelagic seabirds, as particular areas (shelf,
shelf breaks, fronts, etc.) reliably hold more prey
resources, and individuals return there in successive
trips. Indeed, this was the suggested explanation for
consistent differences in trip bearings and repeata-
bility in travel distances of individual northern gan-
nets only at the Bass Rock and not Great Saltee, UK,
on the basis that predictability of resources was
higher in the North Sea than in the Irish Sea (Hamer
et al. 2001). However, specialization does not always
relate to resource predictability; black-browed alba-
tross, shy albatross Thalassarche cauta and razorbill
Alca torda were not consistent in site or habitat use
although they all fed in neritic waters (Hedd et al.
2001, Granadeiro et al. 2014, Shoji et al. 2016). In
ad dition, although it is intuitive that specialization
would be less likely in tropical waters, given the
Mar Ecol Prog Ser 578: 117–150, 2017
Species Breeding colony Foraging site Foraging trip Fidelity to
fidelity within or bearing or dis- nonbreeding site,
between breeding tance (breeding route or staging
seasons season) areaa
King penguin Falklands W - X
Aptenodytes patagonicus
Macaroni penguin South Georgia
Eudyptes chrysolophus
Southern rockhopper penguin Falklands
Eudyptes c. chrysocome
Adélie penguin Syowa Station, W - ()
Pygoscelis adeliae Antarctica
Little penguin Penguin Island,
Eudyptula minor Australia
Yellow-eyed penguin Oamaru, W -
Megadyptes antipodes New Zealand
Black-browed albatross South Georgia N - , R/S - X
Thalassarche melanophris
Kerguelen W - (), B - ()
Grey-headed albatross South Georgia N -
Thalassarche chrysostoma
Shy albatross Tasmania W - X, B - X
Thalassarche cauta
Light-mantled albatross South Georgia
Phoebetria palpebrata
Wandering albatross South Georgia
Diomedea exulans
Crozet N -
White-chinned petrel South Georgia
Procellaria aequinoctialis
Yelkouan shearwater Malta N -
Puffinus yelkouan
Short-tailed shearwater Tasmania N -
Ardenna tenuirostris
Sooty shearwater Kidney Island N - (), R/S - ()
Ardenna grisea (Falklands)
Streaked shearwater Sangan, Mikura, N - , R/S -
Calonectris leucomelas Awa Islands, Japan
Cory’s shearwater Selvagem Grande N - (), R/S - X
Calonectris borealis (Madeira)
Berlenga (Portugal)
Canary Islands W -
Scopoli’s shearwater Sicily (Italy) N - , R/S - X
Calonectris diomedea
Desertas petrel Madeira N -
Pterodroma deserta
Thin-billed prion New Island,
Pachyptila belcheri Falklands
Broad-billed prion Rangatira,
Pachyptila vittata Chatham Islands
Northern gannet Bass Rock (UK) W - , B - √√
Morus bassanus
Great Saltee (UK) W - X X
Grassholm (UK) W - √√
and Brittany (France)
Alderney W - X
Various colonies, Canada N -
North Norway W - X ()
Table 4 (this and the next 3 pages). Evidence for significant individual specialization in distribution, movements, activity or
diet of seabirds. : significant effect; (): some evidence but with exceptions; X: study tested explicitly for specialization but
found no evidence; W: within breeding season; B: between breeding seasons; N: nonbreeding site; R/S: route or staging area;
Dep: at departure; Dur: during; Ret: at return; ST: short-term (days to weeks); LT: between seasons or annual
Phillips et al.: Individual variability in seabirds 135
Consistent Consistent Consistent Consistent Reference
migration activity or habitat usecdiet or trophic
schedulebdiving in short- leveldin short-
pattern or long-term or long-term
Baylis et al. (2015)
LT - Green et al. (2005),
Horswill et al. (2016)
LT - LT - Dehnhard et al. (2016)
Watanuki et al. (2003)
Ropert-Coudert et al.
Mattern et al. (2007)
Dur - , Ret - √√ Phillips et al. (2005),
Mackley et al. (2010)
ST - X ST - X Granadeiro et al. (2014)
ST - Patrick & Weimerskirch
(2014b, 2017)
Croxall et al. (2005),
Mackley et al. (2010)
Hedd et al. (2001)
Mackley et al. (2010)
ST - , LT - ST - , LT - X Mackley et al. (2010),
Ceia et al. (2012)
Weimerskirch et al. (2015)
Mackley et al. (2011)
Dep - , Dur - , Ret - Raine et al. (2013)
Yamamoto et al. (2015)
Dep - (), Dur - ()Hedd et al. (2012)
Dep - , Dur - Yamamoto et al. (2014)
Dep - , Dur - , Ret - Dias et al. (2011),
Dias et al. (2013)
ST - () ST - () Ceia et al. (2014)
Navarro & González-Solís
Dep - X, Dur - , Ret - X Müller et al. (2014)
Dep - , Ret - LT - LT - Ramirez et al. (2016)
ST - , LT - X ST - , LT - X Quillfeldt et al. (2008)
LT - X LT - X Grecian et al. (2016)
ST- , LT - ST - , LT- Hamer et al. (2001, 2007),
Wakefield et al. (2015)
Hamer et al. (2001)
ST - ST - Votier et al. (2010),
Patrick et al. (2014)
Soanes et al. (2013)
Dur - , Ret - Fifield et al. (2014)
Pettex et al. (2012)
(table continued on next 2 pages)
Mar Ecol Prog Ser 578: 117–150, 2017
greater variability and patchiness of resources
(Weimerskirch 2007), streaked shear waters Calo -
nectris leucomelas, which migrate to tropical waters,
showed a high degree of fidelity to nonbreeding
destination and migration route (Yamamoto et al.
2014). Availability and predictability can also vary
over time in the same habitats, which might partly
explain why the degree of consistency in diet or iso-
topic niche in the same species can depend on
breeding stage and year (Ceia et al. 2014).
Great cormorant Chausey Islands, W - , B -
Phalacrocorax carbo France
European shag Isle of May (UK)
Phalacrocorax aristotelis
Imperial shag Argentina W - √√
Phalacrocorax atriceps
South Georgia shag South Georgia
Phalacrororax georgianus
Kerguelen shag Kerguelen W - √√
Phalacrocorax verrucosus
Crozet shags Possession Island,
Phalacrocorax melanogenis Crozet
King cormorant Macquarie Island
Phalacrocorax purpurascens
Pelagic cormorant Gulf of Alaska W -
Phalacrocorax pelagicus
Double-crested Cormorant Oneida Lake, W -
Phalacrocorax auritus New York, USA
Japanese cormorants Teuri Island, Japan W - √√
Phalacrocorax capillatus
Razorbill Alca torda Skomer (UK) W - X X
Atlantic puffin Skomer N - , R/S -
Fratercula arctica
Great skua Bjørnøya N -
Stercorarius skua Shetland, UK W -
Brown skua South Georgia
Stercorarius lonnbergi South Shetland Islands N -
South polar skua King George Island N -
Stercorarius maccormicki
Long-tailed skua Sweden, Svalbard, N - (), R/S - ()
Stercorarius longicaudus and Greenland
Lesser black-backed gull North Norway N -
Larus fuscus
Yellow-legged gull Gulf of Cadiz, Spain
Larus michahellis
Dolphin gull Falkland Islands W -
Leucophaeus scoresbii
Black-legged Kittiwake Prince William Sound, W -
Rissa tridactyla Alaska
Pribilof Islands N - (), R/S - ()
Pigeon guillemot Prince William Sound, Alaska
Cepphus columba
Brünnich’s guillemot Various colonies, Canada N - ()
Uria lomvia Nunavut, Canada
Common guillemot Various colonies, Canada N - ()
Uria aalge Newfoundland, Canada W - √√
aStudies only included if 2 or more individuals tracked in multiple years. bWhere possible, studies were excluded that did not
control for differences in breeding success between years. cIncludes results from tracking and stable isotope studies.
dIncludes conventional diet and stable isotope studies
Species Breeding colony Foraging site Foraging trip Fidelity to
fidelity within or bearing or dis- nonbreeding site,
between breeding tance (breeding route or staging
seasons season) areaa
(Table 4 continued)
Phillips et al.: Individual variability in seabirds
Development of individual specialization:
the role of learning
Individual specialization is expected to offer a selec-
tive advantage where resources are to some extent
predictable; under these circumstances, birds can in-
crease foraging efficiency by reducing search times or
develop proficiency in locating or handling particular
types of prey. Specialization, particularly site fidelity,
likely develops largely from experience gained
Grémillet et al. (1999),
Potier et al. (2015)
Daunt et al. (2014)
Harris et al. (2013, 2014b)
LT - LT - Bearhop et al. (2006),
Ratcliffe et al. (2013)
ST - , LT - ST - , LT - Bearhop et al. (2006),
Camprasse et al. (2017a)
Cook et al. (2006)
Kato et al. (2000)
Kotzerka et al. (2011)
Coleman et al. (2005)
Ishikawa & Watanuki (2002)
Shoji et al. (2016)
Dur - Guilford et al. (2011),
Fayet et al. (2016)
Magnusdottir et al. (2012)
ST - , LT - Votier et al. (2004)
LT - LT - Phillips et al. (2007)
Dep - , Ret - √√ Krietsch et al. (2017), this
Theme Section
Kopp et al. (2011)
van Bemmelen et al. (2017),
this Theme Section
Helberg et al. (2009)
Navarro et al. (2017),
this Theme Section
ST - Masello et al. (2013)
Irons (1998)
Orben et al. (2015b)
LT - Golet et al. (2000)
Dep - X, Ret - X McFarlane
Tranquilla et al. (2014)
ST - ST - , LT - Woo et al. (2008),
Elliott et al. (2009)
Dep - (), Ret - √√ McFarlane
Tranquilla et al. (2014)
Regular et al. (2013)
Consistent Consistent Consistent Consistent Reference
migration activity or habitat usecdiet or trophic
schedulebdiving in short- leveldin short-
pattern or long-term or long-term
Mar Ecol Prog Ser 578: 117–150, 2017
(learned) when seabirds are immature. During these
formative years, individuals show high variability in
dispersal and movement patterns (Thiers et al. 2014, de
Grissac et al. 2016), in which the roles of genetics and
experience are not well understood. Whether individ-
ual wandering albatrosses are partial or full migrants
does not appear to be heritable (Weimerskirch et al.
2015). However, because fledgling seabirds migrate
for the first time without parents, initial dispersal direc-
tionand potentially the distance travelled — may be
heritable as in other birds (Piersma et al. 2005).
Although intrinsic factors will also play a role, in
the absence of a central-place foraging constraint,
the subsequent timing of movements and areas vis-
ited by immatures is probably dictated to a consider-
able extent by local conditions (including weather)
and the availability, patchiness and predictability of
prey (Mueller & Fagan 2008). Individual migration
pattern probably becomes fixed according to experi-
ence (Guilford et al. 2011, Péron & Grémillet 2013, de
Grissac et al. 2016). There is no effect of age per se on
the nonbreeding strategy in the wandering albatross
(Weimerskirch et al. 2015) nor on the likelihood of an
adult shifting its winter destination in the Cory’s
shearwater (Dias et al. 2011). Indeed, Cory’s shear-
waters may switch back and forth between different
regions (Dias et al. 2013), and long-tailed skuas may
switch between different routes in successive migra-
tions (van Bemmelen et al. 2017), indicating that these
changes are not the result of accidental displacement
by severe weather conditions. Hence, knowledge of
the previous experience of the individual is key to
understanding the navigation process, and the devel-
opment of individual specialization in movements in
Learning may also be responsible for development
of individual specializations in diving behaviour, par-
ticularly as benthic feeders such as shags and cor-
morants would benefit from local knowledge of bottom
topography and currents (Table 4). Learning could
also explain consistency in at-sea activity patterns (in-
cluding in flights and landings), trophic level or diet,
even in pelagic species, as individuals may specialize
in locating or handling particular types of prey (Table 4).
Indeed, learning seems the likeliest explanation for
dietary specializations in highly op portunistic species
with diverse diets, such as great skua Stercorarius skua,
brown skua and dolphin gull Leucophaeus scoresbii,
which presumably need to develop particular skills to
successfully pursue different foraging modes, whether
that is kleptoparasitism, predation of selected species
or scavenging, etc. (Votier et al. 2004, Phillips et al.
2007, Masello et al. 2013).
Implications of individual specialization
Links to physiology and life-history
Many studies have related differences between
individuals in distribution, timing, foraging success,
etc. to body condition, past experience or future
breeding performance (Bogdanova et al. 2011, Orben
et al. 2015a). By comparison, only a few studies have
examined the physiological correlates of specializa-
tion or the energetic or life-history consequences.
Specialization should in theory be advantageous if an
individual has fixed on a particular strategy that is
more profitable than the alternatives. Positive evi-
dence for an advantage of specialization is particu-
larly apparent among predatory seabirds. Specialist
western gulls Larus occidentalis that maintained
feeding territories within colonies of other seabirds
had higher reproductive success and similar or higher
survival rates compared to non-specialists (Spear
1993). Pairs of slaty-backed gulls Larus schistisagus
that delivered more depredated seabird chicks raised
more fledglings, and their chicks grew faster than
those of pairs that mainly delivered fish, possibly
because of the differences in energy value of the
meals (Watanuki 1992). Individual specialization has
also been linked to potential fitness advantages in
other seabirds. There were significant relationships
between repeatability in some dive characteristics of
great cormorants Phalacrocorax carbo and foraging
efficiency (Potier et al. 2015). In the black-browed
albatross, foraging trip characteristics were less vari-
able in successful than unsuccessful male breeders
and in females that were more faithful to foraging
sites but not necessarily to habitat (water depth) had
higher reproductive success (Patrick & Weimerskirch
2014a, 2017). Pairs of pigeon guillemots Cepphus
columba that were dietary specialists fledged more
chicks than the diet generalists, apparently because
they delivered larger individual prey items (Golet et
al. 2000).
Individual specialization has been linked to carry-
over effects in a number of studies. Individual Euro-
pean shags showed consistent differences in daily
foraging times during winter, and the shorter foraging
times were associated with earlier and more success-
ful breeding, demonstrating a clear carry-over effect
(Daunt et al. 2014). In this context, it is important to
note that carry-over effects may be evident in only a
proportion of colonies (Bogdanova et al. 2017); it is also
often hard to exclude the possibility that a cross-sea-
sonal correlation is unrelated to specialization and in-
stead due to stable within-individual performance, i.e.
Phillips et al.: Individual variability in seabirds 139
consistently good or poor performance or decision-
making year-round (Harrison et al. 2011). The mecha-
nisms underlying carry-over effects are not always
clear, but it seems that stress (reflected in feather corti-
costerone levels) affects energy or nutrient acquisition
and hence physiological condition, which has impacts
on behaviour and performance in the subsequent
season (Young et al. 2017, this Theme Section).
Intuitively, consequences of individual specializa-
tions might be most obvious when examining effects
of migration distance, as those individuals that travel
the furthest incur greater energy or time costs, reduc-
ing the time available for feeding and resting en
route or delaying the return to the colony. Late return
has repercussions for nest defence, mating opportu-
nities or re-establishment of the pair bonds and, ulti-
mately, timing of laying, which is typically closely
correlated with breeding performance. Yet, 2 studies
did not find evidence of a substantial energetic advan-
tage for individuals that remained closer to the colony,
having accounted for flight time to and within alter-
native wintering areas and for thermoregulatory
costs associated with resting on the water (Garthe et
al. 2012, Fort et al. 2013). Similarly, Ramirez et al.
(2016) did not detect differences in the level of in -
dividual repeatability in at-sea activity patterns of
Desertas petrels that migrated to different wintering
areas. In theory, the choice of a short- or long-distance
migration strategy may be neutral, reflect individual
optima or vary in terms of advantages or disadvan-
tages for survival or reproduction depending on the
year. If so, individual specialization in the form of
high nonbreeding-site fidelity may not affect subse-
quent body condition, survival or fitness unless there
is a major deterioration in the environment.
Various studies have not detected any convinc -
ing selective advantage of individual specialization.
Northern gannets that associated consistently with
fishing vessels were not in better body condition than
those which avoided vessels (Patrick et al. 2015);
short- and long-term consistency in trophic level or
carbon source was not related to body mass index in
wandering albatrosses (Ceia et al. 2012); there were
no effects of foraging area or site fidelity on chick
feeding frequency or meal mass in Adélie penguins
Pygoscelis adeliae (Watanuki et al. 2003) nor on
breeding success in European shags (Daunt et al.
2014); although Brünnich’s guillemots that were gen-
eralists tended to deliver slightly more energy per
day, specialists and generalists did not differ in any
other aspect of fitness (Woo et al. 2008); great skuas
that were bird specialists consistently laid earlier, had
larger clutch volumes and improved chick condition
but did not have higher breeding success or survival
than specialist fish predators (Votier et al. 2004);
lastly, consistency within or among years in trip or
dive characteristics did not influence body condition
in northern gannets (Wakefield et al. 2015). The lack
of a clear fitness benefit in many cases may be re lated
to changes over time in the predictability of re sources,
which could fluctuate within and between breeding
seasons. Specialists may be at an advantage when
predictability is high in certain areas, whereas gener-
alists likely benefit when resource availability is less
predictable and more heterogeneous.
Links to population dynamics and conservation
An understanding of variation both among and
within individuals allows the characterization of
populations and has implications for their resilience
in the face of environmental change (Nussey et al.
2007). Unless there is time for selection to act, popu-
lations that lack variability and individuals that lack
plasticity in movements and foraging behaviour are
Fig. 1. Use of different resources or habitats (represented by different shading) for more or less generalist or specialist
Mar Ecol Prog Ser 578: 117–150, 2017
likely to be at a considerable disadvantage. This is
illustrated by the schematic based on Bolnick et al.
(2003), which illustrates different hypothetical situa-
tions of resource (or habitat) use in Fig. 1: (1) gener-
alist individuals from a generalist population all
target multiple alternative resources (type A); (2)
specialist individuals from a generalist population
consistently target one of multiple alternative re -
sources (type B); and (3) specialist individuals from a
specialist population all consistently target the same
resource. The implications are that in the absence of
a change in behaviour, the loss or deterioration of
one resource or habitat would be catastrophic for the
specialist population (and for the specialists in the
generalist population that targeted that resource) but
of less consequence for the generalists, depending on
density-dependent competition for the resources that
remain. This can have implications in the design of
marine protected areas, since population-based ap -
proaches may not identify important areas used by a
relatively low proportion of specialized individuals,
or these areas may not be prioritized for manage-
ment. However, those areas, and the specialists that
use them, may buffer population-level impacts of a
deterioration in habitats used by the majority of birds.
The same principle applies to a localized in crease in
pollutants, competition with fisheries or fisheries
bycatch, etc. Indeed, many threats show extensive
spatial heterogeneity, such as fisheries bycatch risk
(Phillips et al. 2009a, Thiers et al. 2014) and exposure
to pollutants, including plastics, mercury, persistent
organic pollutants and hydrocarbons (Young et al.
2009, Montevecchi et al. 2012, Leat et al. 2013, Tartu
et al. 2013).
The importance of assessing the extent and dura-
tion of specialization can be illustrated by consider-
ing exposure to fisheries. In the Falklands, there
were significant differences between 2 study colo -
nies of black-browed albatrosses in the degree of
bird association with vessels, despite equal distances
to fishing areas (Granadeiro et al. 2011, 2014). Those
studies showed that a minority of individuals repeat-
edly followed vessels, suggesting they specialized in
the short-term on fisheries waste, but tracking in a
subsequent year and stable isotope analyses sug-
gested that any fisheries specialism did not persist. In
contrast, individual northern gannets did show spe-
cialization in following vessels or feeding on fisheries
waste (Patrick et al. 2015). Hence, in the absence of
any mitigation, fisheries bycatch represents a con-
stant risk to black-browed albatrosses that would be
maintained indefinitely if a proportion of the general-
ist population is attracted to vessels at random, but a
particular risk for a specific group of specialist north-
ern gannets that might be removed and not replaced.
The demographic implications of these and other
threats depends on the diversity of strategies (from
specialist to generalist) in the population, the proba-
bility of individuals encountering adverse conditions,
the degree of individual plasticity and the hetero-
geneity in vital rates associated with among-individual
specialization. Seabirds are clearly highly adaptable
in response to environmental pertubation, and some
specializations can be relatively short-lived (Wake-
field et al. 2015). Movement of individuals during the
breeding and nonbreeding seasons are clearly flexi-
ble, but other aspects of behaviour (such as depar-
ture bearings of fledglings) or timing of some events
may be innate, possibly responding to magnetic cues
or stimuli that are highly predictable, such as photo -
period; however, even then, there may be some
capacity for fine-tuning in response to environmental
factors (Helm et al. 2013).
As this review has shown, many intrinsic factors (in-
cluding stage of the annual cycle, breeding status,
age and sex) drive individual differences in movement
patterns and behaviour of seabirds. Understanding
the nature, drivers and consequences of this variation
is revealing in terms of ecology and life-histories and
determines the response of individuals, populations
and species to environmental changes, including an-
thropogenic threats. In addition, the effects of in trinsic
factors and their interactions with each other and with
the environment need to be considered in sampling
design and analyses, and before drawing conclusions
about underlying processes and mechanisms. They
also need to be taken into account when evaluating
evidence for individual specialization and its causes
and consequences. Effects of factors such as sex, stage,
age, as well as individual specializations are common
in terms of distribution, habitat use, diving, diet and
other components of foraging strategies at sea, but
their roles and extents are highly variable. Site fidelity
is scale-dependent for migrants, greater at the re-
gional level than in the use of staging areas and
routes, and can be low during the breeding season
(Table 4). Timing of movements during the nonbreed-
ing period is often consistent, but with some flexibility
in response to local conditions. As might be expected,
seabirds retain the flexibility to respond to local envi-
ronmental conditions or cues and intrinsic factors
(body condition, physiological constraints, etc.).
Phillips et al.: Individual variability in seabirds
There is much scope for more studies on the time -
scale or periods in which effects of sex, age and spe-
cialization are apparent (from days to years) and the
drivers underpinning these factors (resource avail-
ability and predictability, density-dependent compe-
tition, intrinsic characteristics, learning). Adults clearly
use memory (Regular et al. 2013) to guide subse-
quent decisions; under what conditions (i.e. changes
in resource availability or habitat suitability) they
might re-enter an exploratory phase as adults and
refine their movement and foraging strategies is
unknown. Although the papers in this Theme Section
have increased our understanding of the implications
of individual variation and specialization, there are
still many gaps in our knowledge. With regard to
individual specialization in particular, we would rec-
ommend research on the circumstances in which it
offers a selective advantage, the degree of genetic or
cultural transmission, the level of plasticity in re -
sponse to the environment, the energetic and other
physiological consequences and effects (immediate
or carry-over) on survival and reproduction. This is
particularly important in a rapidly changing world, as
the degree of plasticity of individuals affects the
capacity of populations to respond to changes in
Acknowledgements. We thank all the authors who con-
tributed to the session on ‘Individual variation in movement
strategies’ at the 2nd World Seabird Conference and to this
Theme Section. A number of researchers kindly provided
unpublished mass data for inclusion in Table 3. We also
thank the editorial staff at Inter-Research for support, and the
referees for their constructive comments on the manuscript.
Aebischer N (1986) Retrospective investigation of an ecolog-
ical disaster in the shag, Phalacrocorax aristotelis: a gen-
eral method based on long-term marking. J Anim Ecol
Åkesson S, Weimerskirch H (2005) Albatross long-distance
navigation: comparing adults and juveniles. J Navig
Åkesson S, Weimerskirch H (2014) Evidence for sex-
segregated ocean distributions of first-winter wandering
albatrosses at Crozet Islands. PLOS ONE 9:e86779
Alderman R, Gales R, Hobday AJ, Candy SG (2010) Post-
fledging survival and dispersal of shy albatross from
three breeding colonies in Tasmania. Mar Ecol Prog Ser
Anker-Nilssen T, Aarvak T (2009) Satellite telemetry reveals
post-breeding movements of Atlantic puffins Fratercula
arctica from Røst, North Norway. Polar Biol 32: 1657−1664
Annett CA, Pierotti R (1999) Long-term reproductive output
in western gulls: consequences of alternate tactics in diet
choice. Ecology 80:288−297
Baduini CL, Hyrenbach KD (2003) Biogeography of procel-
lariiform foraging strategies: does ocean productivity
influence provisioning? Mar Ornithol 31:101−112
Barrett RT, Camphuysen CJ, Anker-Nilssen T, Chardine JW
and others (2007) Diet studies of seabirds: a review and
recommendations. ICES J Mar Sci 64:1675−1691
Baylis AMM, Orben RA, Pistorius P, Brickle P, Staniland I,
Ratcliffe N (2015) Winter foraging site fidelity of king
penguins breeding at the Falkland Islands. Mar Biol
Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA,
Croxall JP (2006) Stable isotopes indicate sex-specific
and long-term individual foraging specialisation in
diving seabirds. Mar Ecol Prog Ser 311:157−164
Becker PH, Ludwigs JD (2004) Sterna hirundo common tern.
BWP Update 6:91−137
Blanco GS, Pisoni JP, Quintana F (2015) Characterization of
the seascape used by juvenile and wintering adult
Southern Giant Petrels from Patagonia Argentina. Estuar
Coast Shelf Sci 153:135−144
Bogdanova MI, Daunt F, Newell M, Phillips RA, Harris MP,
Wanless S (2011) Seasonal interactions in the black-
legged kittiwake, Rissa tridactyla: links between breed-
ing performance and winter distribution. Proc Biol Sci
Bogdanova MI, Butler A, Wanless S, Moe B and others
(2017) Multi-colony tracking reveals spatio-temporal
variation in carry-over effects between breeding success
and winter movements in a pelagic seabird. Mar Ecol
Prog Ser 578:167–181
Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM,
Hulsey CD, Forister ML (2003) The ecology of individu-
als: incidence and implications of individual specializa-
tion. Am Nat 161:1−28
Booth JM, McQuaid CD (2013) Northern rockhopper
penguins prioritise future reproduction over chick pro -
visioning. Mar Ecol Prog Ser 486:289−304
Borboroglu PG, Boersma PD (2015) Penguins: natural his-
tory and conservation. University of Washington Press,
Seattle, WA
Bridge E (2006) Influences of morphology and behavior on
wing-molt strategies in seabirds. Mar Ornithol 34:7−19
Bugge J, Barrett RT, Pedersen T (2011) Optimal foraging in
chick-raising Common Guillemots (Uria aalge). J Ornithol
Bugoni L, Griffiths K, Furness RW (2011) Sex-biased inci-
dental mortality of albatrosses and petrels in longline
fisheries: differential distributions at sea or differential
access to baits mediated by sexual size dimorphism?
J Ornithol 152:261−268
Burger J, Gochfeld M (1981) Age-related differences in
piracy behaviour of four species of gulls, Larus. Behaviour
Burke CM, Montevecchi WA, Regular PM (2015) Seasonal
variation in parental care drives sex-specific foraging by
a monomorphic seabird. PLOS ONE 10:e0141190
Camphuysen CJ, Shamoun-Baranes J, van Loon EE, Bouten
W (2015) Sexually distinct foraging strategies in an
omnivorous seabird. Mar Biol 162:1417−1428
Campioni L, Granadeiro JP, Catry P (2016) Niche segrega-
tion between immature and adult seabirds: Does pro-
gressive maturation play a role? Behav Ecol 27:426−433
Camprasse ECM, Cherel Y, Arnould JPY, Hoskins AJ, Bost
CA (2017a) Combined bio-logging and stable isotopes
reveal individual specialisations in a benthic coastal sea-
Mar Ecol Prog Ser 578: 117–150, 2017
bird, the Kerguelen shag. PLOS ONE 12:e0172278
Camprasse ECM, Cherel Y, Bustamante P, Arnould JPY,
Bost CA (2017b) Intra- and inter-individual variation in
the foraging ecology of a generalist subantarctic seabird,
the gentoo penguin. Mar Ecol Prog Ser 578:227–242
Camprasse ECM, Cherel Y, Arnould JPY, Hoskins AJ, Bus-
tamante P, Bost CA (2017c) Mate similarity in foraging
Kerguelen shags: a combined bio-logging and stable
isotope investigation. Mar Ecol Prog Ser 578:183196
Carneiro APB, Manica A, Phillips RA (2014) Foraging
behaviour and habitat use by brown skuas Stercorarius
lonnbergi breeding at South Georgia. Mar Biol 161:
Carneiro APB, Manica A, Clay TA, Silk JRD, King M,
Phillips RA (2016) Consistency in migration strategies
and habitat preferences of brown skuas over two winters,
a decade apart. Mar Ecol Prog Ser 553:267−281
Carneiro APB, Bonnet-Lebrun AS, Manica A, Staniland IJ,
Phillips RA (2017) Methods for detecting and quantifying
individual specialisation in movement and foraging
strategies of marine predators. Mar Ecol Prog Ser 578:
Carravieri A, Bustamante P, Tartu S, Meillere A and others
(2014) Wandering albatrosses document latitudinal vari-
ations in the transfer of persistent organic pollutants and
mercury to Southern Ocean predators. Environ Sci Tech-
nol 48:14746−14755
Caswell H (2001) Matrix population models: construction,
analysis and interpretation. 2nd edn. Sinauer, Sunder-
land, MA
Catry P, Phillips RA, Croxall JP (2005) Sexual segregation in
birds: patterns, processes and implications for conserva-
tion. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segrega-
tion in vertebrates: ecology of the two sexes. Cambridge
University Press, Cambridge, p 351−378
Catry P, Phillips RA, Phalan B, Croxall JP (2006) Senescence
effects in an extremely long-lived bird: the grey-headed
albatross Thalassarche chrysostoma. Proc Biol Sci 273:
Catry P, Granadeiro JP, Ramos J, Phillips RA, Oliveira P
(2011) Either taking it easy or feeling too tired: Old
Cory’s Shearwaters display reduced activity levels while
at sea. J Ornithol 152:549−555
Catry P, Dias MP, Phillips RA, Granadeiro JP (2013a) Carry-
over effects from breeding modulate the annual cycle of
a long-distance migrant: an experimental demonstration.
Ecology 94:1230−1235
Catry P, Poisbleau M, Lecoq M, Phillips RA (2013b) Differ-
ences in the timing and extent of annual moult of black-
browed albatrosses Thalassarche melanophris living in
contrasting environments. Polar Biol 36:837−842
Ceia FR, Ramos JA (2015) Individual specialization in the
foraging and feeding strategies of seabirds: a review.
Mar Biol 162:1923−1938
Ceia FR, Phillips RA, Ramos JA, Cherel Y, Vieira RP, Richard
P, Xavier JC (2012) Short- and long-term consistency in
the foraging niche of wandering albatrosses. Mar Biol
Ceia FR, Paiva VH, Garthe S, Marques JC, Ramos JA (2014)
Can variations in the spatial distribution at sea and iso-
topic niche width be associated with consistency in the
isotopic niche of a pelagic seabird species? Mar Biol
Charrassin JB, Bost CA (2001) Utilisation of the oceanic
habitat by king penguins over the annual cycle. Mar Ecol
Prog Ser 221:285−298
Chaurand T, Weimerskirch H (1994) The regular alternation
of short and long foraging trips in the blue petrel
Halobaena caerulea: a previously undescribed strategy
of food provisioning in a pelagic seabird. J Anim Ecol
Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable iso-
topes document seasonal changes in trophic niches and
winter foraging individual specialization in diving pred-
ators from the Southern Ocean. J Anim Ecol 76:826−836
Cherel Y, Quillfeldt P, Delord K, Weimerskirch H (2016)
Combination of at-sea activity, geolocation and feather
stable isotopes documents where and when seabirds
molt. Front Ecol Evol 4:3
Chiaradia A, Ramírez F, Forero MG, Hobson KA (2016) Sta-
ble isotopes (δ13C, δ15N) combined with conventional
dietary approaches reveal plasticity in central-place for-
aging behavior of Little Penguins Eudyptula minor. Front
Ecol Evol 3:154
Clarke J, Manly B, Kerry K, Gardner H, Franchi E, Corsolini
S, Focardi S (1998) Sex differences in Adélie penguin
foraging strategies. Polar Biol 20:248−258
Clay TA, Manica A, Ryan PG, Silk JR, Croxall JP, Ireland L,
Phillips RA (2016) Proximate drivers of spatial segrega-
tion in non-breeding albatrosses. Sci Rep 6:29932
Cleasby IR, Wakefield ED, Bodey TW, Davies RD and others
(2015) Sexual segregation in a wide-ranging marine
predator is a consequence of habitat selection. Mar Ecol
Prog Ser 518:1−12
Clutton-Brock TH (1988) Reproductive success: studies of
individual variation in contrasting breeding systems.
University of Chicago Press, Chicago, Il
Coleman JT, Richmond ME, Rudstam LG, Mattison PM
(2005) Foraging location and site fidelity of the double-
crested cormorant on Oneida Lake, New York. Water-
birds 28:498−510
Cook TR, Cherel Y, Tremblay Y (2006) Foraging tactics of
chick-rearing Crozet shags: Individuals display repeti-
tive activity and diving patterns over time. Polar Biol
Cornioley T, Börger L, Ozgul A, Weimerskirch H (2016)
Impact of changing wind conditions on foraging and
incubation success in male and female wandering alba-
trosses. J Anim Ecol 85:1318−1327
Costa DP (1991) Reproductive and foraging energetics of
high latitude penguins, albatrosses and pinnipeds: impli-
cations for life history patterns. Am Zool 31:111−130
Cristol DA, Baker MB, Carbone C (1999) Differential migra-
tion revisited: latitudinal segregation by age and sex
class. In: Nolan VJ, Ketterson ED, Thompson CF (eds)
Current ornithology, Book 15. Kluwer Academic/ Plenum
Press, New York, NY, p 33−88
Crossin GT, Cooke SJ, Goldbogen JA, Phillips RA (2014)
Tracking fitness in marine vertebrates: current knowl-
edge and opportunities for future research. Mar Ecol
Prog Ser 496:1−17
Croxall JP, Silk JRD, Phillips RA, Afanasyev V, Briggs DR
(2005) Global circumnavigations: tracking year-round
ranges of nonbreeding albatrosses. Science 307:249−250
Curio E (1983) Why do young birds reproduce less well? Ibis
Dall SR, Bell AM, Bolnick DI, Ratnieks FL (2012) An evolu-
tionary ecology of individual differences. Ecol Lett
DallAntonia L, Gudmundsson GA, Benvenuti S (2001) Time
Phillips et al.: Individual variability in seabirds
allocation and foraging pattern of chick-rearing razor-
bills in northwest Iceland. Condor 103:469−480
Dänhardt A, Fresemann T, Becker PH (2011) To eat or to
feed? Prey utilization of Common Terns Sterna hirundo
in the Wadden Sea. J Ornithol 152:347−357
Daunt F, Wanless S, Harris MP, Monaghan P (1999) Experi-
mental evidence that age-specific reproductive success
is independent of environmental effects. Proc Biol Sci
Daunt F, Monaghan P, Wanless S, Harris MP, Griffiths R
(2001) Sons and daughters: age-specific differences in
parental rearing capacities. Funct Ecol 15:211−216
Daunt F, Afanasyev V, Silk JRD, Wanless S (2006) Extrinsic
and intrinsic determinants of winter foraging and breed-
ing phenology in a temperate seabird. Behav Ecol Socio-
biol 59:381−388
Daunt F, Wanless S, Harris MP, Money L, Monaghan P
(2007a) Older and wiser: improvements in breeding suc-
cess are linked to better foraging performance in Euro-
pean shags. Funct Ecol 21:561−567
Daunt F, Afanasyev V, Adam A, Croxall JP, Wanless S
(2007b) From cradle to early grave: juvenile mortality in
European shags Phalacrocorax aristotelis results from
inadequate development of foraging proficiency. Biol
Lett 3:371−374
Daunt F, Reed TE, Newell M, Burthe S, Phillips RA, Lewis S,
Wanless S (2014) Longitudinal bio-logging reveals inter-
play between extrinsic and intrinsic carry-over effects in
a long-lived vertebrate. Ecology 95:2077−2083
Davoren GK, Burger AE (1999) Differences in prey selection
and behaviour during self-feeding and chick provision-
ing in rhinoceros auklets. Anim Behav 58:853−863
de Grissac S, Börger L, Guitteaud A, Weimerskirch H (2016)
Contrasting movement strategies among juvenile alba-
trosses and petrels. Sci Rep 6:26103
Dehnhard N, Eens M, Sturaro N, Lepoint G, Demongin L,
Quillfeldt P, Poisbleau M (2016) Is individual consistency
in body mass and reproductive decisions linked to indi-
vidual specialization in foraging behavior in a long-lived
seabird? Ecol Evol 6:4488−4501
Dias MP, Granadeiro JP, Phillips RA, Alonso H, Catry P
(2011) Breaking the routine: individual Cory’s shear -
waters shift winter destinations between hemispheres
and across ocean basins. Proc Biol Sci 278:1786−1793
Dias MP, Granadeiro JP, Catry P (2013) Individual variability
in the migratory path and stopovers of a long-distance
pelagic migrant. Anim Behav 86:359−364
Dunn EK (1972) Effect of age on the fishing ability of Sand-
wich Terns Sterna sandvicensis. Ibis 114:360−366
Elliott KH, Gaston AJ (2015) Diel vertical migration of prey
and light availability constrain foraging in an Arctic sea-
bird. Mar Biol 162:1739−1748
Elliott KH, Woo KJ, Gaston AJ (2009) Specialization in mur-
res: the story of eight specialists. Waterbirds 32:491−506
Elliott KH, Gaston AJ, Crump D (2010) Sex-specific behavior
by a monomorphic seabird represents risk partitioning.
Behav Ecol 21:1024−1032
Elliott KH, Hare JF, Le Vaillant M, Gaston AJ, Ropert-
Coudert Y, Anderson WG (2015) Ageing gracefully:
Physiology but not behaviour declines with age in a
diving seabird. Funct Ecol 29:219−228
Fayet AL, Freeman R, Shoji A, Padget O, Perrins CM, Guil-
ford T (2015) Lower foraging efficiency in immatures
drives spatial segregation with breeding adults in a long-
lived pelagic seabird. Anim Behav 110:79−89
Fayet AL, Freeman R, Shoji A, Boyle D and others (2016)
Drivers and fitness consequences of dispersive migration
in a pelagic seabird. Behav Ecol 27:1061−1072
Fifield DA, Montevecchi WA, Garthe S, Robertson GJ,
Kubetzki U, Rail JF (2014) Migratory tactics and winter-
ing areas of northern gannets (Morus bassanus) breed-
ing in North America. Ornithol Monogr 79:1−63
Fijn RC, Wolf P, Courtens W, Verstraete H, Stienen EW,
Iliszko L, Poot MJ (2014) Post-breeding prospecting trips
of adult Sandwich Terns Thalasseus sandvicensis. Bird
Study 61:566−571
Forero MG, Tella JL, Donazar JA, Blanco G, Bertellotti M,
Ceballos O (2001) Phenotypic assortative mating and
within-pair sexual dimorphism and its influence on
breeding success and offspring quality in Magellanic
penguins. Can J Zool 79:1414−1422
Forslund P, Pärt T (1995) Age and reproduction in birds:
hypotheses and tests. Trends Ecol Evol 10:374−378
Fort J, Steen H, Strom H, Tremblay Y and others (2013)
Energetic consequences of contrasting winter migratory
strategies in a sympatric Arctic seabird duet. J Avian Biol
Frederiksen M, Moe B, Daunt F, Phillips RA and others
(2012) Multicolony tracking reveals the winter distribu-
tion of a pelagic seabird on an ocean basin scale. Divers
Distrib 18:530−542
Frederiksen M, Descamps S, Erikstad KE, Gaston AJ and
others (2016) Migration and wintering of a declining sea-
bird, the thick-billed murre Uria lomvia, on an ocean
basin scale: conservation implications. Biol Conserv 200:
Froy H, Phillips RA, Wood AG, Nussey DH, Lewis S (2013)
Age-related variation in reproductive traits in the wan-
dering albatross: evidence for terminal improvement
following senescence. Ecol Lett 16:642−649
Froy H, Lewis S, Catry P, Bishop CM and others (2015) Age-
related variation in foraging behaviour in the wandering
albatross at South Georgia: no evidence for senescence.
PLOS ONE 10:e0116415
García-Tarrasón M, Bécares J, Bateman S, Arcos JM, Jover
L, Sanpera C (2015) Sex-specific foraging behavior in
response to fishing activities in a threatened seabird.
Ecol Evol 5:2348−2358
Garthe S, Ludynia K, Huppop O, Kubetzki U, Meraz JF, Fur-
ness RW (2012) Energy budgets reveal equal benefits of
varied migration strategies in northern gannets. Mar Biol
Genovart M, McMinn M, Bowler D (2003) A discriminant
function for predicting sex in the Balearic Shearwater.
Waterbirds 26:72−76
Gianuca D, Phillips RA, Townley S, Votier S (2017) Global
patterns of sex- and age-specific variation in seabird
bycatch. Biol Conserv 205:60−76
Golet GH, Kuletz KJ, Roby DD, Irons DB (2000) Adult prey
choice affects chick growth and reproductive success in
pigeon guillemots. Auk 117:82−91
González-Solís J (2004) Regulation of incubation shifts near
hatching by giant petrels: a timed mechanism, embry-
onic signalling or food availability? Anim Behav
González-Solís J, Shaffer SA (2009) Introduction and syn-
thesis: spatial ecology of seabirds at sea. Mar Ecol Prog
Ser 391:117−120
González-Solís J, Croxall JP, Wood AG (2000) Sexual size
dimorphism and sexual segregation in foraging strate-
Mar Ecol Prog Ser 578: 117–150, 2017
gies of northern giant petrels, Macronectes halli, during
incubation. Oikos 90:390−398
González-Solís J, Croxall JP, Afanasyev V (2007) Offshore
spatial segregation in giant petrels Macronectes spp.:
differences between species, sexes and seasons. Aquat
Conserv 17:S22−S36
Gorman KB, Williams TD, Fraser WR (2014) Ecological sex-
ual dimorphism and environmental variability within a
community of Antarctic penguins (Genus Pygoscelis).
PLOS ONE 9:e90081
Granadeiro JP, Nunes M, Silva MC, Furness RW (1998) Flex-
ible foraging strategy of Cory’s shearwater Calonectris
diomedea during the chick rearing period. Anim Behav
Granadeiro JP, Phillips RA, Brickle P, Catry P (2011) Alba-
trosses following fishing vessels: How badly hooked are
they on an easy meal? PLOS ONE 6:e17467
Granadeiro JP, Brickle P, Catry P (2014) Do individual sea-
birds specialize in fisheries’ waste? The case of black-
browed albatrosses foraging over the Patagonian Shelf.
Anim Conserv 17:19−26
Gray CM, Hamer KC (2001) Food provisioning behaviour of
male and female Manx shearwaters Puffinus puffinus.
Anim Behav 62:117−121
Grecian WJ, Taylor GA, Loh G, McGill RAR and others
(2016) Contrasting migratory responses of two closely
related seabirds to long-term climate change. Mar Ecol
Prog Ser 559:231−242
Green JA, Boyd IL, Woakes AJ, Warren NL, Butler PJ (2005)
Behavioural flexibility during year-round foraging in
macaroni penguins. Mar Ecol Prog Ser 296:183−196
Green JA, Boyd IL, Woakes AJ, Warren NL, Butler PJ (2009)
Evaluating the prudence of parents: daily energy expen-
diture throughout the annual cycle of a free-ranging
bird, the macaroni penguin Eudyptes chrysolophus.
J Avian Biol 40:529−538
Greig SA, Coulson JC, Monaghan P (1983) Age-related dif-
ferences in foraging success in the herring gull (Larus
argentatus). Anim Behav 31:1237−1243
Greig SA, Coulson JC, Monaghan P (1985) Feeding strate-
gies of male and female adult herring gulls (Larus argen-
tatus). Behaviour 94:41−59
Grémillet D, Charmantier A (2010) Shifts in phenotypic plas-
ticity constrain the value of seabirds as ecological indica-
tors of marine ecosystems. Ecol Appl 20:1498−1503
Grémillet D, Wilson RP, Storch S, Gary Y (1999) Three-
dimensional space utilization by a marine predator. Mar
Ecol Prog Ser 183:263−273
Grémillet D, Kuntz G, Woakes AJ, Gilbert C, Robin JP, Le
Maho Y, Butler PJ (2005) Year-round recordings of
behavioural and physiological parameters reveal the
survival strategy of a poorly insulated diving endotherm
during the Arctic winter. J Exp Biol 208:4231−4241
Grémillet D, Pichegru L, Kuntz G, Woakes AG, Wilkinson S,
Crawford RJ, Ryan PG (2008) A junk-food hypothesis for
gannets feeding on fishery waste. Proc Biol Sci 275:
Grémillet D, Péron C, Provost P, Lescroel A (2015) Adult and
juvenile European seabirds at risk from marine plunder-
ing off West Africa. Biol Conserv 182:143−147
Grist H, Daunt F, Wanless S, Nelson EJ and others (2014)
Site fidelity and individual variation in winter location
in partially migratory European shags. PLOS ONE 9:
Guilford T, Freeman R, Boyle D, Dean B, Kirk H, Phillips R,
Perrins C (2011) A dispersive migration in the Atlantic
puffin and its implications for migratory navigation.
PLOS ONE 6:e21336
Guo H, Cao L, Peng L, Zhao G, Tang S (2010) Parental care,
development of foraging skills, and transition to inde-
pendence in the red-footed booby. Condor 112:38−47
Gutowsky SE, Tremblay Y, Kappes MA, Flint EN and others
(2014) Divergent post-breeding distribution and habitat
associations of fledgling and adult Black-footed Alba-
trosses Phoebastria nigripes in the North Pacific. Ibis
Hamer KC, Phillips RA, Hill JK, Wanless S, Wood AG (2001)
Contrasting foraging strategies of gannets Morus bas-
sanus at two North Atlantic colonies: foraging trip dura-
tion and foraging area fidelity. Mar Ecol Prog Ser 224:
Hamer KC, Humphreys EM, Garthe S, Hennicke J and oth-
ers (2007) Annual variation in diets, feeding locations
and foraging behaviour of gannets in the North Sea: flex-
ibility, consistency and constraint. Mar Ecol Prog Ser 338:
Harding A, Van Pelt TI, Lifjeld JT, Mehlum F (2004) Sex dif-
ferences in Little Auk Alle alle parental care: transition
from biparental to paternal-only care. Ibis 146:642−651
Harris MP, Wanless S (1997) Breeding success, diet, and
brood neglect in the kittiwake (Rissa tridactyla) over an
11-year period. ICES J Mar Sci 54:615−623
Harris MP, Leopold MF, Jensen JK, Meesters EH, Wanless S
(2015) The winter diet of the Atlantic Puffin Fratercula
arctica around the Faroe Islands. Ibis 157:468−479
Harris S, Raya Rey A, Phillips RA, Quintana F (2013) Sexual
segregation in timing of foraging by imperial shags (Pha-
lacrocorax atriceps): Is it always ladies first? Mar Biol
Harris S, Raya Rey A, Quintana F (2014a) Breeding experi-
ence and foraging behaviour of Imperial Shags (Leuco-
carbo atriceps) in Argentina. Emu 114:222−228
Harris S, Raya Rey AR, Zavalaga C, Quintana F (2014b)
Strong temporal consistency in the individual foraging
behaviour of Imperial Shags Phalacrocorax atriceps. Ibis
Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S
(2011) Carry-over effects as drivers of fitness differences
in animals. J Anim Ecol 80:4−18
Haug FD, Paiva VH, Werner AC, Ramos JA (2015) Foraging
by experienced and inexperienced Cory’s shearwater
along a 3-year period of ameliorating foraging condi-
tions. Mar Biol 162:649−660
Hedd A, Gales R, Brothers N (2001) Foraging strategies of
shy albatross Thalassarche cauta breeding at Albatross
Island, Tasmania, Australia. Mar Ecol Prog Ser 224:
Hedd A, Fifield DA, Burke CM, Montevecchi WA and others
(2010) Seasonal shift in the foraging niche of Atlantic
puffins Fratercula arctica revealed by stable isotope
(δ15N and δ13C) analyses. Aquat Biol 9:13−22
Hedd A, Montevecchi WA, Otley H, Phillips RA, Fifield DA
(2012) Trans-equatorial migration and habitat use by
sooty shearwaters Puffinus griseus from the South
Atlantic during the nonbreeding season. Mar Ecol Prog
Ser 449:277−290
Hedd A, Montevecchi WA, Phillips RA, Fifield DA (2014)
Seasonal sexual segregation by monomorphic sooty
shearwaters Puffinus griseus reflects different reproduc-
tive roles during the pre-laying period. PLOS ONE
Phillips et al.: Individual variability in seabirds
Helberg M, Systad GH, Birkeland I, Lorentzen NH, Bustnes
JO (2009) Migration patterns of adult and juvenile Lesser
Black-backed Gulls Larus fuscus from northern Norway.
Ardea 97:281−286
Helm B, Ben-Shlomo R, Sheriff MJ, Hut RA, Foster R, Barnes
BM, Dominoni D (2013) Annual rhythms that underlie
phenology: biological time-keeping meets environ mental
change. Proc Biol Sci 280:20130016
Hennicke JC, James DJ, Weimerskirch H (2015) Sex-
specific habitat utilization and differential breeding
investments in Christmas Island frigatebirds throughout
the breeding cycle. PLOS ONE 10:e0129437
Horswill C, Matthiopoulos J, Ratcliffe N, Green JA and
others (2016) Drivers of intrapopulation variation in re -
source use in a generalist predator, the macaroni pen-
guin. Mar Ecol Prog Ser 548:233−247
Hull CL (2000) Comparative diving behaviour and segrega-
tion of the marine habitat by breeding Royal Penguins,
Eudyptes schlegeli, and eastern Rockhopper Penguins,
Eudyptes chrysocome filholi, at Macquarie Island. Can J
Zool 78:333−345
Hunter S (1984) Moult of the giant petrels Macronectes halli
and M. giganteus at South Georgia. Ibis 126:119−132
Irons DB (1998) Foraging area fidelity of individual seabirds
in relation to tidal cycles and flock feeding. Ecology
Isaksson N, Evans TJ, Shamoun-Baranes J, Åkesson S
(2016) Land or sea? Foraging area choice during breed-
ing by an omnivorous gull. Mov Ecol 4:11
Ishikawa K, Watanuki Y (2002) Sex and individual differ-
ences in foraging behavior of Japanese cormorants in
years of different prey availability. J Ethol 20:49−54
Ito M, Takahashi A, Kokubun N, Kitaysky AS, Watanuki Y
(2010) Foraging behavior of incubating and chick-rearing
thick-billed murres Uria lomvia. Aquat Biol 8: 279−287
Jaeger A, Goutte A, Lecomte VJ, Richard P and others
(2014) Age, sex, and breeding status shape a complex
foraging pattern in an extremely long-lived seabird.
Ecology 95:2324−2333
Jiménez S, Phillips RA, Brazeiro A, Defeo O, Domingo A
(2014) Bycatch of great albatrosses in pelagic longline
fisheries in the southwest Atlantic: contributing factors
and implications for management. Biol Conserv 171:9−20
Jiménez S, Domingo A, Brazeiro A, Defeo O and others
(2016) Sex-related variation in the vulnerability of
wandering albatrosses to pelagic longline fleets. Anim
Conserv 19:281−295
Jones IL, Rowe S, Carr SM, Fraser G, Taylor P (2002) Dif -
ferent patterns of parental effort during chick-rearing by
female and male thick-billed murres Uria lomvia at a low
arctic colony. Auk 119:1064−1074
Jorge PE, Sowter D, Marques PA (2011) Differential annual
movement patterns in a migratory species: effects of
experience and sexual maturation. PLOS ONE 6:e22433
Karnovsky NJ, Hobson KA, Iverson S, Hunt GL Jr (2008)
Seasonal changes in diets of seabirds in the North Water
Polynya: a multiple-indicator approach. Mar Ecol Prog
Ser 357:291−299
Kato A, Watanuki Y, Nishiumi I, Kuroki M, Shaughnessy P,
Naito Y (2000) Variation in foraging and parental behav-
ior of King Cormorants. Auk 117:718−730
Kooyman GL, Kooyman TG, Horning M, Kooyman CA
(1996) Penguin dispersal after fledging. Nature 383:397
Kopp M, Peter HU, Mustafa O, Lisovski S, Ritz MS, Phillips
RA, Hahn S (2011) South polar skuas from a single
breeding population overwinter in different oceans
though show similar migration patterns. Mar Ecol Prog
Ser 435:263−267
Kotzerka J, Hatch SA, Garthe S (2011) Evidence for forag-
ing-site fidelity and individual foraging behavior of
pelagic cormorants rearing chicks in the Gulf of Alaska.
Condor 113:80−88
Krietsch J, Hahn S, Kopp M, Phillips RA, Peter HU, Lisovski
S (2017) Consistent variation in individual migration
strategies of brown skuas. Mar Ecol Prog Ser 578: 213–225
Le Vaillant M, Wilson RP, Kato A, Saraux C and others
(2012) King penguins adjust their diving behaviour with
age. J Exp Biol 215:3685−3692
Le Vaillant M, Le Bohec C, Prud’Homme O, Wienecke B, Le
Maho Y, Kato A, Ropert-Coudert Y (2013) How age and
sex drive the foraging behaviour in the king penguin.
Mar Biol 160:1147−1156
Le Vaillant M, Ropert-Coudert Y, Le Maho Y, Le Bohec C
(2016) Individual parameters shape foraging activity in
breeding king penguins. Behav Ecol 27:352−362
Leat EHK, Bourgeon S, Magnusdottir E, Gabrielsen GW and
others (2013) Influence of wintering area on persistent
organic pollutants in a breeding migratory seabird. Mar
Ecol Prog Ser 491:277−293
Lecomte VJ, Sorci G, Cornet S, Jaeger A and others (2010)
Patterns of aging in the long-lived wandering albatross.
Proc Natl Acad Sci USA 107:6370−6375
Lescroël A, Dugger KM, Ballard G, Ainley DG (2009) Effects
of individual quality, reproductive success and environ-
mental variability on survival of a long-lived seabird.
J Anim Ecol 78:798−806
Lewis S, Benvenuti S, Dall’Antonia L, Griffiths R and others
(2002) Sex-specific foraging behaviour in a monomor-
phic seabird. Proc Biol Sci 269:1687−1693
Lewis S, Wanless S, Elston DA, Schultz MD and others
(2006) Determinants of quality in a long-lived colonial
species. J Anim Ecol 75:1304−1312
Lewis S, Phillips RA, Burthe SJ, Wanless S, Daunt F (2015)
Contrasting responses of male and female foraging effort
to year round wind conditions. J Anim Ecol 84:
Limmer B, Becker PH (2009) Improvement in chick provi-
sioning with parental experience in a seabird. Anim
Behav 77:1095−1101
Linnebjerg JF, Fort J, Guilford T, Reuleaux A, Mosbech A,
Frederiksen M (2013) Sympatric breeding auks shift
between dietary and spatial resource partitioning across
the annual cycle. PLOS ONE 8:e72987
Ludynia K, Dehnhard N, Poisbleau M, Demongin L, Masello
JF, Voigt CC, Quillfeldt P (2013) Sexual segregation in
rockhopper penguins during incubation. Anim Behav
Machovsky-Capuska GE, Hauber ME, Dassis M, Libby E
and others (2014) Foraging behaviour and habitat use
of chick-rearing Australasian Gannets in New Zealand.
J Ornithol 155:379−387
Machovsky-Capuska GE, Senior AM, Benn EC, Tait AH and
others (2016) Sex-specific macronutrient foraging strate-
gies in a highly successful marine predator: the Aus-
tralasian gannet. Mar Biol 163:75
Mackley EK, Phillips RA, Silk JRD, Wakefield ED,
Afanasyev V, Fox JW, Furness RW (2010) Free as a bird?
Activity patterns of albatrosses during the nonbreeding
period. Mar Ecol Prog Ser 406:291−303
Mar Ecol Prog Ser 578: 117–150, 2017
Mackley EK, Phillips RA, Silk JRD, Wakefield ED, Afanas -
yev V, Furness RW (2011) At-sea activity patterns of
breeding and nonbreeding white-chinned petrels Pro-
cellaria aequinoctialis from South Georgia. Mar Biol
MacLean AA (1986) Age-specific foraging ability and the
evolution of deferred breeding in three species of gulls.
Wilson Bull 98:267−279
Magnusdottir E, Leat EHK, Bourgeon S, Strom H and others
(2012) Wintering areas of great skuas Stercorarius skua
breeding in Scotland, Iceland and Norway. Bird Study
Magnusdottir E, Leat EHK, Bourgeon S, Jonsson JE and oth-
ers (2014) Activity patterns of wintering Great Skuas
Stercorarius skua. Bird Study 61:301−308
Mancini PL, Bond AL, Hobson KA, Duarte LS, Bugoni L
(2013) Foraging segregation in tropical and polar sea-
birds: testing the intersexual competition hypothesis.
J Exp Mar Biol Ecol 449:186−193
Marchetti K, Price T (1989) Differences in the foraging of
juvenile and adult birds: the importance of developmen-
tal constraints. Biol Rev Camb Philos Soc 64:51−70
Masello JF, Wikelski M, Voigt CC, Quillfeldt P (2013) Distri-
bution patterns predict individual specialization in the
diet of dolphin gulls. PLOS ONE 8:e67714
Mattern T, Ellenberg U, Houston DM, Davis LS (2007) Con-
sistent foraging routes and benthic foraging behaviour in
yellow-eyed penguins. Mar Ecol Prog Ser 343:295−306
McLeay LJ, Page B, Goldsworthy S, Ward T, Paton D (2009)
Size matters: variation in the diet of chick and adult
crested terns. Mar Biol 156:1765−1780
Meier RE, Wynn RB, Votier SC, Grive MM and others (2015)
Consistent foraging areas and commuting corridors of
the critically endangered Balearic shearwater Puffinus
mauretanicus in the northwestern Mediterranean. Biol
Conserv 190:87−97
Meier RE, Votier SC, Wynn RB, Guilford T and others (2017)
Tracking, feather moult and stable isotopes reveal forag-
ing behaviour of a critically endangered seabird during
the non-breeding season. Divers Distrib 23:130−145
Michalik A, McGill RAR, van Noordwijk HJ, Masello JF,
Furness RW, Eggers T, Quillfeldt P (2013) Stable isotopes
reveal variable foraging behaviour in a colony of the
Imperial Shag Phalacrocorax atriceps: differences
between ages, sexes and years. J Ornithol 154:239−249
Missagia RV, Ramos JA, Louzao M, Delord K, Weimerskirch
H, Paiva VH (2015) Year-round distribution suggests
spatial segregation of Cory’s shearwaters, based on indi-
vidual experience. Mar Biol 162:2279−2289
Monaghan P, Nager R, Houston D (1998) The price of eggs:
increased investment in egg production reduces the off-
spring rearing capacity of parents. Proc R Soc Lond B
Biol Sci 265:1731−1735
Montevecchi WA, Hedd A, McFarlane Tranquilla L, Fifield
DA and others (2012) Tracking seabirds to identify eco-
logically important and high risk marine areas in the
western North Atlantic. Biol Conserv 156:62−71
Moore GJ, Wienecke B, Robertson G (1999) Seasonal
change in foraging areas and dive depths of breeding
king penguins at Heard Island. Polar Biol 21:376−384
Moreno J (2003) Lifetime reproductive success in seabirds:
interindividual differences and implications for conser-
vation. Sci Mar 67:7−12
Mosbech A, Johansen KL, Bech NI, Lyngs P and others
(2012) Inter-breeding movements of little auks Alle alle
reveal a key post-breeding staging area in the Green-
land Sea. Polar Biol 35:305−311
Mueller T, Fagan WF (2008) Search and navigation in
dynamic environmentsfrom individual behaviors to
population distributions. Oikos 117:654−664
Müller MS, Massa B, Phillips RA, Dell’Omo G (2014) Indi-
vidual consistency and sex differences in migration
strategies of Scopoli’s shearwaters Calonectris diomedea
despite year differences. Curr Zool 60:631−641
Müller MS, Massa B, Phillips RA, Dell’Omo G (2015) Sea-
birds mated for life migrate separately to the same
places: behavioural coordination or shared proximate
causes? Anim Behav 102:267−276
Navarro J, González-Solís J (2009) Environmental determi-
nants of foraging strategies in Cory’s shearwaters
Calonectris diomedea. Mar Ecol Prog Ser 378:259−267
Navarro J, Oro D, Bertolero A, Genovart M, Delgado A,
Forero MG (2010) Age and sexual differences in the
exploitation of two anthropogenic food resources for an
opportunistic seabird. Mar Biol 157:2453−2459
Navarro J, Grémillet D, Ramirez FJ, Afán I, Bouten W,
Forero MG (2017) Shifting individual habitat specializa-
tion of a successful predator living in anthropogenic
landscapes. Mar Ecol Prog Ser 578:243–251
Newton I (1989) Lifetime reproduction in birds. Academic
Press, London
Nol E, Smith JN (1987) Effects of age and breeding ex -
perience on seasonal reproductive success in the song
sparrow. J Anim Ecol 56:301−313
Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary
ecology of individual phenotypic plasticity in wild popu-
lations. J Evol Biol 20:831−844
Nussey DH, Froy H, Lemaitre JF, Gaillard JM, Austad SN
(2013) Senescence in natural populations of animals:
widespread evidence and its implications for bio-
gerontology. Ageing Res Rev 12:214−225
Ochi D, Oka N, Watanuki Y (2010) Foraging trip decisions
by the streaked shearwater Calonectris leucomelas
depend on both parental and chick state. J Ethol 28:
Orben RA, Paredes R, Roby DD, Irons DB, Shaffer SA
(2015a) Body size affects individual winter foraging
strategies of thick billed murres in the Bering Sea. J Anim
Ecol 84:1589−1599
Orben RA, Paredes R, Roby DD, Irons DB, Shaffer SA
(2015b) Wintering North Pacific black-legged kittiwakes
balance spatial flexibility and consistency. Mov Ecol 3:36
Orgeret F, Weimerskirch H, Bost CA (2016) Early diving
behaviour in juvenile penguins: improvement or selec-
tion processes. Biol Lett 12:20160490
Orians GH (1969) Age and hunting success in the Brown
Pelican (Pelecanus occidentalis). Anim Behav 17:316−319
Paiva VH, Ramos JA, Martins J, Almeida A, Carvalho A
(2008) Foraging habitat selection by Little Terns Sternula
albifrons in an estuarine lagoon system of southern Por-
tugal. Ibis 150:18−31
Paredes R, Jones IL, Boness DJ (2006) Parental roles of male
and female thick-billed murres and razorbills at the Gan-
net Islands, Labrador. Behaviour 143:451−481
Paredes R, Jones IL, Boness DJ, Tremblay Y, Renner M
(2008) Sex-specific differences in diving behaviour of
two sympatric Alcini species: thick-billed murres and
razorbills. Can J Zool 86:610−622
Pärt T (1995) Does breeding experience explain increased
reproductive success with age? An experiment. Proc R
Phillips et al.: Individual variability in seabirds
Soc Lond B Biol Sci 260:113−117
Patrick SC, Weimerskirch H (2014a) Consistency pays: sex
differences and fitness consequences of behavioural
specialization in a wide-ranging seabird. Biol Lett 10:
Patrick SC, Weimerskirch H (2014b) Personality, foraging
and fitness consequences in a long lived seabird. PLOS
ONE 9:e87269
Patrick SC, Weimerskirch H (2017) Reproductive success is
driven by local site fidelity despite stronger specialisa-
tion by individuals for large-scale habitat preference.
J Anim Ecol 86:674−682
Patrick SC, Bearhop S, Grémillet D, Lescroel A and others
(2014) Individual differences in searching behaviour and
spatial foraging consistency in a central place marine
predator. Oikos 123:33−40
Patrick SC, Bearhop S, Bodey TW, Grecian WJ, Hamer KC,
Lee J, Votier SC (2015) Individual seabirds show consis-
tent foraging strategies in response to predictable fish-
eries discards. J Avian Biol 46:431−440
Pedrocchi V, Oro D, González-Solís J (1996) Differences
between diet of adult and chick Audouin’s Gulls Larus
audouinii at the Chafarinas Islands, SW Mediterranean.
Ornis Fenn 73:124−130
Pelletier L, Chiaradia A, Kato A, Ropert-Coudert Y (2014)
Fine-scale spatial age segregation in the limited foraging
area of an inshore seabird species, the little penguin.
Oecologia 176:399−408
Pérez C, Granadeiro JP, Dias MP, Alonso H, Catry P (2014)
When males are more inclined to stay at home: insights
into the partial migration of a pelagic seabird provided
by geolocators and isotopes. Behav Ecol 25:313−319
Pérez C, Granadeiro JP, Dias MP, Catry P (2016) Sex and
migratory strategy influence corticosterone levels in win-
ter-grown feathers, with positive breeding effects in a
migratory pelagic seabird. Oecologia 181:1025−1033
Péron C, Grémillet D (2013) Tracking through life stages:
adult, immature and juvenile autumn migration in a
long-lived seabird. PLOS ONE 8:e72713
Péron C, Delord K, Phillips RA, Charbonnier Y, Marteau C,
Louzao M, Weimerskirch H (2010) Seasonal variation in
oceanographic habitat and behaviour of white-chinned
petrels Procellaria aequinoctialis from Kerguelen Island.
Mar Ecol Prog Ser 416:267−284
Peters WD, Grubb TC (1983) An experimental analysis of
sex-specific foraging in the downy woodpecker, Picoides
pubescens. Ecology 64:1437−1443
Petersen SL, Phillips RA, Ryan PG, Underhill LG (2008)
Albatross overlap with fisheries in the Benguela
Upwelling System: implications for conservation and
management. Endang Species Res 5:117−127
Pettex E, Lorentsen SH, Grémillet D, Gimenez O and others
(2012) Multi-scale foraging variability in Northern gan-
net (Morus bassanus) fuels potential foraging plasticity.
Mar Biol 159:2743−2756
Phalan B, Phillips RA, Silk JRD, Afanasyev V and others
(2007) Foraging behaviour of four albatross species by
night and day. Mar Ecol Prog Ser 340:271−286
Phillips RA, Hamer KC (1999) Lipid reserves, fasting capa-
bility and the evolution of nestling obesity in procellari-
iform seabirds. Proc Biol Sci 266:1329−1334
Phillips RA, Hamer KC (2000) Growth and provisioning
strategies of Northern Fulmars, Fulmarus glacialis. Ibis
Phillips RA, Dawson DA, Ross DJ (2002) Mating patterns
and reversed size dimorphism in Southern Skuas (Ster-
corarius skua lonnbergi). Auk 119:858−863
Phillips RA, Silk JRD, Phalan B, Catry P, Croxall JP (2004)
Seasonal sexual segregation in two Thalassarche alba-
tross species: competitive exclusion, reproductive role
specialization or foraging niche divergence? Proc Biol Sci
Phillips RA, Silk JRD, Croxall JP, Afanasyev V, Bennett VJ
(2005) Summer distribution and migration of nonbreed-
ing albatrosses: individual consistencies and implications
for conservation. Ecology 86:2386−2396
Phillips RA, Silk JRD, Croxall JP, Afanasyev V (2006) Year-
round distribution of white-chinned petrels from South
Georgia: relationships with oceanography and fisheries.
Biol Conserv 129:336−347
Phillips RA, Catry P, Silk JRD, Bearhop S, McGill R,
Afanasyev V, Strange IJ (2007) Movements, winter distri-
bution and activity patterns of Falkland and brown
skuas: insights from loggers and isotopes. Mar Ecol Prog
Ser 345:281−291
Phillips RA, Croxall JP, Silk JRD, Briggs DR (2008) Foraging
ecology of albatrosses and petrels from South Georgia:
two decades of insights from tracking technologies.
Aquat Conserv 17:S6−S21
Phillips RA, Bearhop S, McGill R, Dawson DA (2009a) Stable
isotopes reveal individual variation in migration strate-
gies and habitat preferences in a suite of seabirds during
the nonbreeding period. Oecologia 160:795−806
Phillips RA, Wakefield ED, Croxall JP, Fukuda A, Higuchi H
(2009b) Albatross foraging behaviour: no evidence for
dual foraging, and limited support for anticipatory regu-
lation of provisioning at South Georgia. Mar Ecol Prog
Ser 391:279−292
Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sex-
ual segregation in distribution, diet and trophic level of
seabirds: insights from stable isotope analysis. Mar Biol
Pichegru L, Cook T, Handley J, Voogt N, Watermeyer J,
Nupen L, McQuaid CD (2013) Sex-specific foraging
behaviour and a field sexing technique for Endangered
African penguins. Endang Species Res 19:255−264
Piersma T, Pérez-Tris J, Mouritsen H, Bauchinger U, Bairlein
F (2005) Is there a ‘migratory syndrome’ common to all
migrant birds? Ann N Y Acad Sci 1046:282−293
Pinet P, Jaquemet S, Pinaud D, Weimerskirch H, Phillips RA,
Le Corre M (2011) Migration, wintering distribution and
habitat use of an endangered tropical seabird, Barau’s
petrel Pterodroma baraui. Mar Ecol Prog Ser 423:291−302
Pinet P, Jaquemet S, Phillips RA, Le Corre M (2012) Sex-spe-
cific foraging strategies throughout the breeding season
in a tropical, sexually monomorphic small petrel. Anim
Behav 83:979−989
Pistorius PA, Hindell MA, Tremblay Y, Rishworth GM (2015)
Weathering a dynamic seascape: influences of wind and
rain on a seabird’s year-round activity budgets. PLOS
ONE 10: e0142623
Ponchon A, Grémillet D, Christensen-Dalsgaard S, Erikstad
KE and others (2014) When things go wrong: intra-sea-
son dynamics of breeding failure in a seabird. Ecosphere
Ponchon A, Chambert T, Lobato E, Tveraa T, Grémillet D,
Boulinier T (2015) Breeding failure induces large scale
prospecting movements in the black-legged kittiwake.
J Exp Mar Biol Ecol 473:138−145
Porter JM, Sealy SG (1982) Dynamics of seabird multi-
Mar Ecol Prog Ser 578: 117–150, 2017
species feeding flocks: age-related feeding behaviour.
Behaviour 81:91−109
Potier S, Carpentier A, Grémillet D, Leroy B, Lescroël A
(2015) Individual repeatability of foraging behaviour in a
marine predator, the great cormorant, Phalacrocorax
carbo. Anim Behav 103:83−90
Prince PA, Wood AG, Barton T, Croxall JP (1992) Satellite
tracking of wandering albatrosses (Diomedea exulans) in
the South Atlantic. Antarct Sci 4:31−36
Quillfeldt P, McGill RAR, Masello JF, Weiss F, Strange IJ,
Brickle P, Furness RW (2008) Stable isotope analysis
reveals sexual and environmental variability and indi-
vidual consistency in foraging of thin-billed prions. Mar
Ecol Prog Ser 373:137−148
Quillfeldt P, Schroff S, van Noordwijk HJ, Michalik A, Ludy-
nia K, Masello JF (2011) Flexible foraging behaviour of a
sexually dimorphic seabird: large males do not always
dive deep. Mar Ecol Prog Ser 428:271−287
Quillfeldt P, Phillips RA, Marx M, Masello JF (2014) Colony
attendance and at-sea distribution of thin-billed prions
during the early breeding season. J Avian Biol 45:
Quintana F, Wilson R, Dell’Arciprete P, Shepard E, Laich AG
(2011) Women from Venus, men from Mars: inter-sex
foraging differences in the imperial cormorant Phalacro-
corax atriceps a colonial seabird. Oikos 120:350−358
Raine AF, Borg JJ, Raine H, Phillips RA (2013) Migration
strategies of the Yelkouan Shearwater Puffinus yelk-
ouan. J Ornithol 154:411−422
Ramirez I, Paiva VH, Fagundes I, Menezes D and others
(2016) Conservation implications of consistent foraging
and trophic ecology in a rare petrel species. Anim Con-
serv 19:139−152
Ramos JA, Granadeiro JP, Phillips RA, Catry P (2009) Flight
morphology and foraging behavior of male and female
Cory’s shearwaters. Condor 111:424−432
Ratcliffe N, Takahashi A, O’Sullivan C, Adlard S, Trathan
PN, Harris MP, Wanless S (2013) The roles of sex, mass
and individual specialisation in partitioning foraging-
depth niches of a pursuit-diving predator. PLOS ONE
Rayner MJ, Taylor GA, Gummer HD, Phillips RA, Sagar PM,
Shaffer SA, Thompson DR (2012) The breeding cycle,
year-round distribution and activity patterns of the
endangered Chatham Petrel (Pterodroma axillaris). Emu
Regular PM, Hedd A, Montevecchi WA (2013) Must marine
predators always follow scaling laws? Memory guides
the foraging decisions of a pursuit-diving seabird. Anim
Behav 86:545−552
Reid JM, Bignal EM, Bignal S, McCracken DI, Bogdanova
MI, Monaghan P (2010) Parent age, lifespan and off-
spring survival: structured variation in life history in a
wild population. J Anim Ecol 79:851−862
Reid TA, Ronconi RA, Cuthbert RJ, Ryan PG (2014) The
summer foraging ranges of adult spectacled petrels Pro-
cellaria conspicillata. Antarct Sci 26:23−32
Reiertsen TK, Erikstad KE, Anker-Nilssen T, Barrett RT and
others (2014) Prey density in non-breeding areas affects
adult survival of black-legged kittiwakes Rissa tridac tyla.
Mar Ecol Prog Ser 509:289−302
Rey AR, Putz K, Simeone A, Hiriart-Bertrand L, Reyes-Arria-
gada R, Riquelme V, Luthi B (2013) Comparative forag-
ing behaviour of sympatric Humboldt and Magellanic
Penguins reveals species-specific and sex-specific strate-
gies. Emu 113:145−153
Ricklefs RE (1983) Some considerations on the reproductive
energetics of pelagic seabirds. Stud Avian Biol 8:84−94
Riotte-Lambert L, Weimerskirch H (2013) Do naive juvenile
seabirds forage differently from adults? Proc Biol Sci
Rishworth GM, Connan M, Green DB, Pistorius PA (2014a)
Sex differentiation based on the gular stripe in the appar-
ently monomorphic Cape gannet. Afr Zool 49:107−112
Rishworth GM, Tremblay Y, Green DB, Connan M, Pistorius
PA (2014b) Drivers of time-activity budget variability
during breeding in a pelagic seabird. PLOS ONE 9:
Rodway MS, Montevecchi WA (1996) Sampling methods for
assessing the diets of Atlantic puffin chicks. Mar Ecol
Prog Ser 144:41−55
Ropert-Coudert Y, Kato A, Naito Y, Cannell BL (2003) Indi-
vidual diving strategies in the Little Penguin. Waterbirds
Ropert-Coudert Y, Wilson RP, Daunt F, Kato A (2004) Pat-
terns of energy acquisition by a central place forager:
benefits of alternating short and long foraging trips.
Behav Ecol 15:824−830
Rosciano NG, Polito MJ, Rey AR (2016) Do penguins share?
Evidence of foraging niche segregation between but not
within two sympatric, central-place foragers. Mar Ecol
Prog Ser 548:249−262
Ruiz X, González-Solís J, Oro D, Jover L (1998) Body size
variation in Audouin’s Gull Larus audouinii; a density-
dependent effect? Ibis 140:431−438
Salton M, Saraux C, Dann P, Chiaradia A (2015) Carry-over
body mass effect from winter to breeding in a resident
seabird, the little penguin. R Soc Open Sci 2:140390
Saraux C, Robinson-Laverick SM, Le Maho Y, Ropert-Coud-
ert Y, Chiaradia A (2011) Plasticity in foraging strategies
of inshore birds: how little penguins maintain body
reserves while feeding offspring. Ecology 92:1909−1916
Schreiber EA, Burger J (eds) (2002) Biology of marine birds.
CRC Press, Boca Raton, FL
Shoji A, Aris-Brosou S, Owen E, Bolton M and others (2016)
Foraging flexibility and search patterns are unlinked
during breeding in a free-ranging seabird. Mar Biol
Silva L, Saporit F, Vales D, Tavares M, Gandini P, Crespo
EA, Cardona L (2014) Differences in diet composition
and foraging patterns between sexes of the Magellanic
penguin (Spheniscus magellanicus) during the non-
breeding period as revealed by δ13C and δ15N values in
feathers and bone. Mar Biol 161:1195−1206
Smith JN (1981) Does high fecundity reduce survival in
Song Sparrows? Evolution 35:1142−1148
Soanes L, Atkinson P, Gauvain R, Green J (2013) Individual
consistency in the foraging behaviour of Northern Gan-
nets: implications for interactions with offshore renew-
able energy developments. Mar Policy 38:507−514
Soanes LM, Arnould JPY, Dodd SG, Milligan G, Green JA
(2014) Factors affecting the foraging behaviour of the
European shag: implications for seabird tracking studies.
Mar Biol 161:1335−1348
Sommerfeld J, Kato A, Ropert-Coudert Y, Garthe S, Hindell
MA (2013) The individual counts: within sex differences
in foraging strategies are as important as sex-specific dif-
ferences in masked boobies Sula dactylatra. J Avian Biol
Spear LB (1993) Dynamics of western gulls feeding in a
Phillips et al.: Individual variability in seabirds
colony of Brandt’s cormorants. J Anim Ecol 62:399−414
Stauss C, Bearhop S, Bodey TW, Garthe S and others (2012)
Sex-specific foraging behaviour in northern gannets
Morus bassanus: incidence and implications. Mar Ecol
Prog Ser 457:151−162
Sydeman WJ, Penniman JF, Penniman TM, Pyle P, Ainley
DG (1991) Breeding performance in the Western gull
effects of parental age, timing of breeding and year in
relation to food availability. J Anim Ecol 60:135−149
Tartu S, Goutte A, Bustamante P, Angelier F and others
(2013) To breed or not to breed: endocrine response to
mercury contamination by an Arctic seabird. Biol Lett
Thaxter CB, Daunt F, Hamer KC, Watanuki Y and others
(2009) Sex-specific food provisioning in a monomorphic
seabird, the common guillemot Uria aalge: nest defence,
foraging efficiency or parental effort? J Avian Biol
Thaxter CB, Wanless S, Daunt F, Harris MP and others
(2010) Influence of wing loading on the trade-off
between pursuit-diving and flight in common guillemots
and razorbills. J Exp Biol 213:1018−1025
Thiebot JB, Lescroël A, Barbraud C, Bost CA (2013) Three-
dimensional use of marine habitats by juvenile emperor
penguins Aptenodytes forsteri during post-natal disper-
sal. Antarct Sci 25:536−544
Thiebot JB, Cherel Y, Acqueberge M, Prudor A, Trathan PN,
Bost CA (2014a) Adjustment of pre-moult foraging
strategies in Macaroni Penguins Eudyptes chrysolophus
according to locality, sex and breeding status. Ibis
Thiebot JB, Authier M, Trathan PN, Bost CA (2014b) Gentle-
men first? ‘Broken stick’ modelling reveals sex-related
homing decision date in migrating seabirds. J Zool
(Lond) 292:25−30
Thiebot JB, Bost CA, Dehnhard N, Demongin L and others
(2015) Mates but not sexes differ in migratory niche in a
monogamous penguin species. Biol Lett 11:20150429
Thiers L, Delord K, Barbraud C, Phillips RA, Pinaud D,
Weimerskirch H (2014) Foraging zones of the two sibling
species of giant petrels in the Indian Ocean throughout
the annual cycle: implication for their conservation. Mar
Ecol Prog Ser 499:233−248
Tickell W (1968) Biology of great albatrosses. Antarctic bird
studies. Horn-Schafer, Baltimore, MD
McFarlane Tranquilla LA, Montevecchi WA, Fifield DA,
Hedd A, Gaston AJ, Robertson GJ, Phillips RA (2014)
Individual winter movement strategies in two species of
murre (Uria spp.) in the Northwest Atlantic. PLOS ONE
Trebilco R, Gales R, Baker GB, Terauds A, Sumner MD
(2008) At sea movement of Macquarie Island giant
petrels: relationships with marine protected areas and
Regional Fisheries Management Organisations. Biol
Conserv 141:2942−2958
Tremblay Y, Cherel Y (2003) Geographic variation in the for-
aging behaviour, diet and chick growth of rockhopper
penguins. Mar Ecol Prog Ser 251:279−297
van Bemmelen R, Moe B, Hanssen SA, Schmidt NM and
others (2017) Flexibility in otherwise consistent non-
breeding movements of a long-distance migratory sea -
bird, the long-tailed skua. Mar Ecol Prog Ser 578:197–211
Votier SC, Bearhop S, Ratcliffe N, Furness RW (2004) Repro-
ductive consequences for great skuas specializing as
seabird predators. Condor 106:275−287
Votier SC, Bearhop S, Witt MJ, Inger R, Thompson D, New-
ton J (2010) Individual responses of seabirds to com -
mercial fisheries revealed using GPS tracking, stable
isotopes and vessel monitoring systems. J Appl Ecol 47:
Votier SC, Grecian WJ, Patrick S, Newton J (2011) Inter-
colony movements, at-sea behaviour and foraging in an
immature seabird: results from GPS-PPT tracking, radio-
tracking and stable isotope analysis. Mar Biol 158:
Wakefield ED, Phillips RA, Matthiopoulos J (2009a) Quanti-
fying habitat use and preferences of pelagic seabirds
using individual movement data: a review. Mar Ecol
Prog Ser 391:165−182
Wakefield ED, Phillips RA, Matthiopoulos J, Fukuda A,
Higuchi H, Marshall GJ, Trathan PN (2009b) Wind field
and sex constrain flight speeds of central-place foraging
albatrosses. Ecol Monogr 79:663−679
Wakefield ED, Cleasby IR, Bearhop S, Bodey TW and others
(2015) Long-term individual foraging site fidelity— why
some gannets don’t change their spots. Ecology 96:
Wanless S, Harris MP, Morris JA (1995) Factors affecting
daily activity budgets of South-Georgian shags during
chick rearing at Bird Island, South Georgia. Condor
Watanuki Y (1992) Individual diet difference, parental care
and reproductive success in slaty-backed gulls. Condor
Watanuki Y, Takahashi A, Sato K (2003) Feeding area spe-
cialization of chick-rearing Adélie penguins Pygoscelis
adeliae in a fast sea-ice area. Ibis 145:558−564
Weimerskirch H (1991) Sex-specific differences in molt
strategy in relation to breeding in the wandering alba-
tross. Condor 93:731−737
Weimerskirch H (2007) Are seabirds foraging for unpre-
dictable resources? Deep-Sea Res II 54:211–223
Weimerskirch H, Jouventin P (1987) Population dynamics of
the wandering albatross, Diomedea exulans, of the
Crozet Islands: causes and consequences of the popula-
tion decline. Oikos 49:315−322
Weimerskirch H, Lys P (2000) Seasonal changes in the pro-
visioning behaviour and mass of male and female wan-
dering albatrosses in relation to the growth of their chick.
Polar Biol 23:733−744
Weimerskirch H, Jouventin P, Mougin JL, Stahl JC, Van
Beveren M (1985) Banding recoveries and the dispersal
of seabirds breeding in French Austral and Antarctic
Territories. Emu 85:22−33
Weimerskirch H, Salamolard M, Sarrazin F, Jouventin P
(1993) Foraging strategy of wandering albatrosses
through the breeding season: a study using satellite
telemetry. Auk 110:325−342
Weimerskirch H, Chastel O, Ackerman L, Chaurand T,
Cuenot-Chaillet F, Hindermeyer X, Judas J (1994)
Alternate long and short foraging trips in pelagic seabird
parents. Anim Behav 47:472−476
Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V
(1997) Alternative foraging strategies and resource
allocation by male and female wandering albatrosses.
Ecology 78:2051−2063
Weimerskirch H, Gault A, Cherel Y (2005) Prey distribution
and patchiness: factors in foraging success and efficiency
of wandering albatrosses. Ecology 86:2611−2622
Weimerskirch H, Åkesson S, Pinaud D (2006) Postnatal dis-
Mar Ecol Prog Ser 578: 117–150, 2017
persal of wandering albatrosses Diomedea exulans:
implications for the conservation of the species. J Avian
Biol 37:23−28
Weimerskirch H, Cherel Y, Delord K, Jaeger A, Patrick SC,
Riotte-Lambert L (2014) Lifetime foraging patterns of the
wandering albatross: Life on the move! J Exp Mar Biol
Ecol 450:68−78
Weimerskirch H, Delord K, Guitteaud A, Phillips RA, Pinet P
(2015) Extreme variation in migration strategies between
and within wandering albatross populations during their
sabbatical year, and their fitness consequences. Sci Rep
Weimerskirch H, Bishop C, Jeanniard-du-Dot T, Prudor A,
Sachs G (2016) Frigate birds track atmospheric condi-
tions over months-long transoceanic flights. Science
Welcker J, Steen H, Harding A, Gabrielsen GW (2009)
Sex specific provisioning behaviour in a monomorphic
seabird with a bimodal foraging strategy. Ibis 151:
Wells MR, Angel LP, Arnould JPY (2016) Habitat-specific
foraging strategies in Australasian gannets. Biol Open
Williams GC (1966) Natural selection, the costs of repro -
duction, and a refinement of Lack’s principle. Am Nat
Williams TD (1995) The penguins. Oxford University Press,
Wilson L, Daunt F, Wanless S (2004) Self-feeding and chick
provisioning diet differ in the Common Guillemot Uria
aalge. Ardea 92:197−207
Woo KJ, Elliott KH, Davidson M, Gaston AJ, Davoren GK
(2008) Individual specialization in diet by a generalist
marine predator reflects specialization in foraging
behaviour. J Anim Ecol 77:1082−1091
Wunderle J (1991) Age-specific foraging proficiency in
birds. Curr Ornithol 8:273−324
Yamamoto T, Takahashi A, Oka N, Iida T, Katsumata N,
Sato K, Trathan PN (2011) Foraging areas of streaked
shearwaters in relation to seasonal changes in the
marine environment of the Northwestern Pacific: inter-
colony and sex-related differences. Mar Ecol Prog Ser
Yamamoto T, Takahashi A, Sato K, Oka N, Yamamoto M,
Trathan PN (2014) Individual consistency in migratory
behaviour of a pelagic seabird. Behaviour 151:683−701
Yamamoto T, Hoshina K, Nishizawa B, Meathrel CE, Phillips
RA, Watanuki Y (2015) Annual and seasonal movements
of migrating short-tailed shearwaters reflect environ-
mental variation in sub-Arctic and Arctic waters. Mar
Biol 162:413−424
Yoda K, Kohno H, Naito Y (2004) Development of flight per-
formance in the brown booby. Proc R Soc Lond B Biol Sci
Young LC, Vanderlip C, Duffy DC, Afanasyev V, Shaffer SA
(2009) Bringing home the trash: Do colony-based differ-
ences in foraging distribution lead to increased plastic
ingestion in laysan albatrosses? PLOS ONE 4:e7623
Young HS, Shaffer SA, McCauley DJ, Foley DG, Dirzo R,
Block BA (2010) Resource partitioning by species but not
sex in sympatric boobies in the central Pacific Ocean.
Mar Ecol Prog Ser 403:291−301
Young RC, Orben RA, Will A, Kitaysky AS (2017) Relation-
ship between telomere dynamics and movement and
behavior during winter in the thick-billed murre. Mar
Ecol Prog Ser 578:253–261
Zimmer I, Ropert-Coudert Y, Kato A, Ancel A, Chiaradia A
(2011) Does foraging performance change with age in
female little penguins (Eudyptula minor)? PLOS ONE
Editorial responsibility: Rory Wilson,
Swansea, UK
Submitted: February 6, 2017; Accepted: May 30, 2017
Proofs received from author(s): August 1, 2017
... Consequently, understanding individual variation in migratory behavior can provide important insights into the potential for migration patterns to have carry-over effects into the breeding season and the reproductive health of a population. Individual variation in migratory behavior can be inferred from tracking devices through differences in movements (e.g., daily distance covered), behaviors (e.g., contact with water as indication of foraging/resting), and timing (e.g., start date, duration; Phillips et al. 2017). ...
... Because male Arctic Terns tend to be larger than females and head size can be used to differentiate between sexes (Devlin et al. 2004;Baak et al. 2020), this relationship may indicate sex differences in migration strategy during the southbound migration. Many seabird species demonstrate sex differences in foraging and migration behaviors (Phillips et al. 2017). Various factors could result in sexual differences in the southbound migration behavior of Arctic Terns, one of which could be associated to the known sexual difference in energy stores during the breeding season (Baak et al. 2020). ...
... Individual variation in migration can be observed through differences in movements, space use, and feeding behavior of many seabird species (Phillips et al. 2017). However, evidence for this has not been well documented in Arctic Terns, in part because overall migration routes are similar for individuals from the same colony (Phillips et al. 2017;Wong et al. 2021), and until recently, tags that could capture these fine-scale behavioral differences were too large to be carried by Arctic Terns over long time periods. ...
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Arctic Terns (Sterna paradisaea) share a few routes to undertake the longest annual migrations of any organism. To understand how the wide spatial range of their breeding colonies may affect their migration strategies (e.g., departure date), we tracked 53 terns from five North American colonies distributed across 30° of latitude and 90° of longitude. While birds from all colonies arrived in Antarctic waters at a similar time, terns nesting in the Arctic colonies migrated back north more slowly and arrived to their breeding grounds later than those nesting in the colony farther south. Arrival dates in Antarctic waters coincided with the start of favorable foraging conditions (i.e., increased ocean productivity), and similarly arrival dates at breeding colonies coincided with the start of local favorable breeding conditions (i.e., disappearance of snow and ice). Larger birds followed a more direct southbound migration route than smaller birds. On both southbound and northbound migrations, daily distances traveled declined as time spent in contact with the ocean increased, suggesting a trade-off between resting/foraging and traveling. There was more unexplained variation in behavior among individuals than among colonies, and one individual had a distinctive stop around Brazil. Terns nesting in the Arctic have a narrow time window for breeding that will likely increase with continuing declines in sea ice and snow. Departing Arctic Terns likely have few clues about the environmental conditions they will encounter on arrival, and their response to environmental changes at both poles may be assisted by large individual variation in migration strategy.
... Stable individual differences in hunting behavior within populations can be driven by specialization when individuals experience temporal and/or spatial fluctuations in the distribution, availability, or behavior of their prey (Araújo et al. 2011;Ceia and Ramos 2015;Phillips et al. 2017;Courbin et al. 2018). For instance, individual predators can specialize in specific tactics to meet the energy/time demands required to successfully capture the type of prey generally encountered (Bowen et al. 2002;Tinker et al. 2008;Arthur et al. 2016). ...
... Trophic interactions are dynamic processes that can also trigger flexible behavioral adjustments by individual predators (Helfman 1990;Heithaus et al. 2018). Predators can shift their hunting strategy in response to changes in prey density and heterogeneity (Inoue and Marsura 1983;Woo et al. 2008), prey behavioral type (McGhee et al. 2013), prey condition (Wignall and Taylor 2008), seasonality Phillips et al. 2017), or habitat structure (Wasiolka et al. 2009). Foraging mode shifts might thus be crucial for predators to maintain capture rates when coping with prey antipredator behavior and environmental change (Laurel and Brown 2006). ...
... Studies show that starvation can force ambush hunters to adopt a cursorial mode (Inoue and Marsura 1983), while ambush hunters often switch to a cursorial mode when prey density is lower (Helfman 1990). Otherwise, foraging shifts may be advantageous when prey encounters are unpredictable (Woo et al. 2008;Ceia and Ramos 2015;Phillips et al. 2017) that is, when predators can successfully adjust their strategy to varying types of prey. ...
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Predator–prey interactions are important drivers of community and ecosystem dynamics. With an online multiplayer videogame, we propose a novel system to explore within population variation in predator hunting mode, and how predator–prey behavioral interactions affect predator hunting success. We empirically examined how four predator foraging behaviors covary at three hierarchical levels (among environments, among individuals, and within individuals) to assess the structure of predator hunting mode. We also investigated how prey activity affects the foraging behavior and hunting success of predators. Our study supports key findings on predator foraging mode and predator-prey interactions from behavioral ecology. We found that individual predators displayed a diversity of hunting tactics that were conditioned by prey behavior. With prey movement, individual predators specialized either as cursorial or ambush hunters along a continuum of their hunting traits, but also shifted their strategy between encounters. Both types of hunters were generally better against slower moving prey, and they achieved similar prey captures over the sampling period. This suggests that virtual worlds supporting multiplayer online videogames can serve as legitimate systems to advance our knowledge on predator–prey interactions.
... In contrast, juvenile and immature yellow-legged gulls, without the reproductive restriction of adults, reached locations far from the breeding colony (Baert et al., 2021). This spatial segregation could also be a mechanism to reduce competition for food between ages, an ecological mechanism described in other seabirds (Gutowsky et al., 2014;Phillips et al., 2017). In fact, it has been suggested that the presence of spatial segregation between adults and juveniles/immatures is higher in seabird species where adults stay close to the colonies de Grissac et al., 2016). ...
... In fact, we found that juveniles showed more locations at sea with resting behaviour than adults. This result agrees with the results obtained by de Grissac et al. (2017) on juvenile individuals of wandering albatross (Diomedea exulans) using the same algorithm to estimate the behavioural state (Garriga et al., 2016), and with the evidence that juveniles had lower foraging success than adults in different species of seabirds (Phillips et al., 2017). Juvenile yellowlegged gulls have more positions associated with resting reflecting the comparatively higher energetic demands of adults that need to feed themselves and their chicks during the breeding period (de Grissac et al., 2017). ...