Vol. 578: 117–150, 2017 MARINE ECOLOGY PROGRESS SERIES Published August 31 https://doi.org/10.3354/meps12217 Mar Ecol Prog Ser Contribution to the Theme Section ‘Individual variability in seabird foraging and migration’ OPENPEN ACCESSCCESS INTRODUCTION: REVIEW 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, CB3 0ET, UK 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 INTRODUCTION tion was paid to the residual variation among individ- uals after accounting for these group effects. This The burgeoning of tracking and stable isotope residual variation was considered to define ‘individ- studies of seabirds and other marine predators since ual specialization’ in the seminal review by Bolnick the 1990s has provided a wealth of information on et al. (2003) and is also the focus of research on ‘be - numerous aspects of their ecology and life-history, havioural syndromes’ or ‘animal personalities’ in the including the striking variation in movement pat- field of animal behaviour (Dall et al. 2012). Research terns and foraging behaviour of individuals (Phillips on individual variation has burgeoned in the last et al. 2008, Wakefield et al. 2009a). Until relatively decade, spurred partly by reductions in cost and recently, this variation was examined largely by test- mass of tracking devices, allowing larger sample ing for effects of factors such as species, colony, sex, sizes, and by the increasing use of more powerful sta- age, year, season (breeding vs. nonbreeding period), tistical techniques (Carneiro et al. 2017, this Theme breeding phase or breeding status. Much less atten- Section). © The authors 2017. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 118 Mar Ecol Prog Ser 578: 117–150, 2017 Most seabirds show striking changes in distribu- catching prey or in selecting suitable locations, tion associated with stage of the annual cycle. Many weaker motor control or physiological fitness (e.g. species are migratory, making directed movements cardiovascular or muscular performance) of young from breeding to nonbreeding grounds to exploit birds or the selective disappearance of poor pheno- seasonal peaks in prey abundance or to avoid types among the adult population. Although there is inclement weather, with implications for survival and evidence that foraging ability can decline in old age subsequent fecundity (Daunt et al. 2014, Reiertsen et (Catry et al. 2006), changes in behaviour may not be al. 2014). The changing degree of central-place con- detectable—despite physiological ageing (Elliott et straint during the breeding period—from pre-laying al. 2015)—or are apparent only in particular environ- through incubation, brood-guard and later chick- ments (Lecomte et al. 2010, Froy et al. 2015). More- rearing (post-guard)—can lead to major shifts in dis- over, differences between old and young animals can tribution, activity patterns or diet within individuals be difficult to interpret, because lower activity (e.g. (Hedd et al. 2014, Quillfeldt et al. 2014). There may more time on the water recorded by a leg-mounted be within-breeding-season (date-related) differences immersion logger) might indicate either inferior in distribution or diet, which reflect extrinsic changes physiological function or greater efficiency allowing in the environment (Phillips et al. 2009b). In addition, more discretionary time to be spent resting (Catry et some seabirds (particularly albatrosses and petrels) al. 2011). adopt a bimodal (or dual) foraging strategy during Sexual segregation and other between-sex differ- chick-rearing, in which adults alternate between ences in foraging behaviour are apparent in many foraging close to the colony and increasing feeding seabirds. This may reflect habitat specialization or frequency for the benefit of the chick, and foraging avoidance of competition in sexually dimorphic spe- further afield to recover their own body condition cies and sex role specialization or sex-specific nutri- (Chaurand & Weimerskirch 1994, Weimerskirch et ent requirements in monomorphic or dimorphic spe- al. 1994). cies (Lewis et al. 2002, Phillips et al. 2004, 2011). Sex There is mounting evidence that movements and differences in distribution and behaviour of seabirds distributions of seabirds are influenced by age and tend to be more apparent during particular periods, breeding status. Failed breeders often depart on their for example during pre-laying (presumably related migration sooner than successful ones (Phillips et al. to sex-role partitioning of nest defense), affecting 2005, Bogdanova et al. 2011, Hedd et al. 2012), and attendance patterns (Hedd et al. 2014, Quillfeldt et they may spend the late breeding season in the same al. 2014). However, such effects are far from univer- areas as deferring (sabbatical) breeders, but be par- sal; despite a degree of spatial segregation, activity tially or completely segregated from active breeders patterns of male and female albatrosses are compa- (Phillips et al. 2005, González-Solís et al. 2007, Reid rable during the breeding and nonbreeding periods, et al. 2014). In this way, nonbreeders (failed or defer- suggesting little difference in prey type or foraging ring) may be avoiding competition with breeders method (Mackley et al. 2011, Phalan et al. 2007). (Clay et al. 2016). Juvenile and immature seabirds Similarly, in the 2 recent studies that recorded sex avoid competition with adults—possibly to compen- differences in the proportions of residents and mi - sate for poorer foraging skills—by using less produc- grants, the effects were in opposite directions (Pérez tive habitats and increasing their foraging time et al. 2014, Weimerskirch et al. 2015). (Daunt et al. 2007b, Fayet et al. 2015). Their distribu- Variation among and within individuals in foraging tions frequently differ from those of adults, often distribution and behaviour has major implications markedly so during the nonbreeding period even for our understanding of seabird ecology because it though adults are no longer limited by the central- affects the use of resources, level of intra-specific place foraging constraint (but see Péron & Grémillet competition and niche partitioning (Phillips et al. 2013, Gutowsky et al. 2014, de Grissac et al. 2016). 2004, de Grissac et al. 2016). In addition, it deter- Age effects on foraging ability are often apparent mines the responses of individuals and populations to amongst breeders: younger or less experienced birds environmental drivers (including climatic change) may forage less efficiently, with implications for breed- and the overlap with, and hence susceptibility to ing success (Daunt et al. 2007b, Limmer & Becker major anthropogenic threats, including fisheries and 2009, Harris et al. 2014a, Le Vaillant et al. 2016), or pollutants (Phillips et al. 2009a, Granadeiro et al. feed at lower trophic levels (Le Vaillant et al. 2013). 2014, Patrick et al. 2015). Individual variation is also Inferior foraging success among younger individuals at the root of carry-over effects, whereby processes in is thought to reflect the poorer skills in identifying or one season have consequences in subsequent sea- Phillips et al.: Individual variability in seabirds 119 sons (Harrison et al. 2011). Surprisingly, however, changes in reproductive demands and central-place there are rarely demonstrable life-history conse- foraging (Phillips et al. 2008, González-Solís & Shaf- quences of individual consistency in foraging strate- fer 2009). Energy requirements and breeding duties gies