Seasonal sea-ice cover has been decreasing in the southeastern
Bering Sea shelf, which might affect ecosystem dynamics and availability of
food resources to marine top predators breeding in the region. In this study,
we investigated the foraging responses of two seabird species,
surface-foraging red-legged kittiwakes
The Bering Sea is a productive marine ecosystem (Springer et al., 1996; Grebmeier, 2012) that supports immense populations of diverse marine fauna (Highsmith and Coyle, 1990; Piatt and Springer, 2003; Aydin and Mueter, 2007; Grebmeier, 2012). Sea-ice cover has been decreasing in duration and concentration over the southeastern Bering Sea shelf (Post et al., 2013), which influences the temperature of the water column in the region, including the extent of the “cold pool” (Stabeno and Overland, 2001; Overland and Stabeno, 2004; Sarmiento et al., 2004; Stabeno et al., 2007; Steele et al., 2008). Such shifts in the physical environment have been shown to affect the ecosystem, including the seasonality and biomass of primary production, metabolic rates, distribution, and abundance of consumers, and changes in pelagic–benthic coupling (Grebmeier et al., 2006; Mueter and Litzow, 2008; Hunt et al., 2011; Wassmann, 2011; Wassmann et al., 2011; Dorresteijn et al., 2012). The Bering Sea is a transition region between Arctic and sub-Arctic seas, and, hence, physical and biological changes in this region may also influence the extent of sea-ice cover and species abundance and composition in the adjacent Arctic Sea (i.e., the Chukchi Sea) (Shimada et al., 2006; Matsuno et al., 2012; Yamamoto et al., 2015).
Predicting the effects of climate change on marine top predators is a major challenge in ecology. Long-term monitoring of seabird demography has been conducted on the Pribilof Islands (Byrd et al., 2008a; Renner et al., 2012; Mudge et al., 2015), which host one of the largest concentrations of piscivorous seabirds in the North Pacific. Previous studies have demonstrated that historical fluctuations in the diet of seabirds (Byrd et al., 2008a; Sinclair et al., 2008; Renner et al., 2012) might reflect broad-scale changes in climate (e.g., regime shift: Benson and Trites, 2002). Although some studies found broad species- and regional-specific relationships between climate variables and breeding parameters (Byrd et al., 2008b), the mechanistic response of seabirds to local climate variability has been elusive and others suggested only weak relationships (Satterthwaite et al., 2012; Renner et al., 2014). This is probably due, in part, to reproductive failure that may occur at several stages of the breeding process (e.g., nest building, egg-laying, incubation, and chick-rearing). It may also be influenced by reproductive effort associated with foraging conditions not only in the current season but also during the previous breeding season (Harrison et al., 2011; Catry et al., 2013). Furthermore, seabirds can adapt their behavior by increasing foraging range and effort in response to changes in the environment, potentially masking effects on some breeding parameters (Kitaysky et al., 2000; Pinaud et al., 2005; Harding et al., 2007). Meanwhile, changes in behavior and prey availability relating to environmental conditions appear to affect their physiological condition (i.e., nutritional stress as reflected in secretion of corticosterone). For example, piscivorous birds breeding on the Pribilof Islands have been shown to experience greater food limitation on the continental shelf during cold years, attributed to higher levels of nutritional stress (Benowitz-Fredericks et al., 2008; Satterthwaite et al., 2012; Harding et al., 2013). To obtain more direct mechanistic insight into their responses to ecosystem dynamics in relation to climate variability, at-sea foraging behavior of breeding seabirds should be examined in concert with the physiological condition. However, there is little information available for the comparative at-sea behavior of seabirds in relation to different environmental conditions in this region (Kokubun et al., 2010; Paredes et al., 2014).
Ship-based observations can provide information on at-sea habitat utilization of species (Hunt et al., 2008, 2014; Kuletz et al., 2014; Wong et al., 2014) together with oceanographic characteristics (Piatt and Springer, 2003; Gall et al., 2013). Although these studies are valuable to detect seasonal, annual, and decadal changes in species distributions (Gall et al., 2013; Hunt et al., 2014; Kuletz et al., 2014), spatial and temporal coverage as well as the context of reproductive processes studied at colonies are limited. The recent availability of animal-borne devices enhances our ability to examine habitat utilization of free-ranging individuals (review by Burger and Shaffer, 2008) and may provide more insight into population processes in relation to ocean variability (Weimerskirch et al., 2001; Paredes et al., 2014).
In this study, we examined the foraging behavior of two seabird species that
exhibit different habitat use: surface-foraging red-legged kittiwakes
Fieldwork was conducted on St. George Island (56
Of the loggers retrieved, some failed to record locations. Hence, location data were available for 5 and 7 RLKIs (20 July–5 August) and 5 and 10 TBMUs (2–12 August) in 2013 and 2014, respectively. Data for RLKIs in 2013 were reanalyzed from Kokubun et al. (2015). At the time of recapture, blood samples were taken from the brachial vein of each individual and kept on ice until centrifugation to separate the plasma from the red blood cells, and both were kept frozen until assayed. Plasma was used for measurement of physiological stress exposure (corticosterone: CORT) and red blood cells for determining trophic level (stable isotopes: SI). CORT was measured only for samples that were taken within 3 min of capture, as it takes 3 min for levels of CORT to begin to rise in the blood in response to the acute stress of capture and restraint (Romero and Reed, 2005).
During the study period, we opportunistically obtained adult diets of RLKIs by
regurgitation at the time of logger deployment and/or retrieval. Prey species
of RLKI samples were identified visually or using otoliths (
GPS locations were re-sampled every 1 min by averaging fixes recorded within
each min for GiPSy-2. We used a forward–backward speed filter (McConnell et
al., 1992), and positions that exceeded 20 m s
To examine the differences in marine environment between the 2 study years
(2013 vs. 2014), satellite remote-sensed monthly mean sea surface
temperatures (SSTs) in August (NOAA POES AVHRR, GAC, 0.1
In addition to the GPS tracking, we also analyzed behavioral data of birds
obtained by geolocators (2.5 g, Mk19; Biotrack Ltd., UK) and accelerometers
(12 mm diameter
Foraging trip trajectories of red-legged kittiwakes, RLKI
CORT concentrations were measured for 8 RLKIs and 20 TBMUs in 2013 and 7 RLKIs
and 21 TBMUs in 2014. CORT concentrations (ng mL
Stable isotopes (
Statistical analyses were carried out in R software (version 2.15.3, R
Development Core Team 2008). Differences in foraging parameters (bathymetry
and distance from the colony in on-water locations and trip duration) between
the years were examined with generalized linear mixed models (GLMM) using
Poisson (for the bathymetry and trip duration) or Gaussian (for the distance)
distributions, including bird identity as a random factor. We tested the
interannual differences in CORT (log-transformed) and SI by conducting
one-way ANOVA. Statistical significance was assumed at
For RLKI, 12 trips in 2013 and 8 trips in 2014 were recorded with GPS
loggers. Two trips were recorded partially, and the other trips included
complete tracks (
The marine habitats of on-water locations during the foraging trips in red-legged kittiwakes (RLKI) and thick-billed murres (TBMU): on-shelf (0–200 m bottom depth), shelf break (200–1000 m bottom depth), and oceanic basin (> 1000 m bottom depth). Red bars represent 2013 and blue bars in 2014 (the mean and standard error).
For TBMU, 11 trips in 2013 and 22 trips in 2014 were recorded with GPS
loggers, including 2 partial tracks, 29 complete tracks, and 2 incomplete
tracks (recorded until close to the beginning of or during the homing commute
phase) (Fig. S1b), having 68
As some of the GPS data were incomplete (i.e., ended before reaching to the
colony; Fig. S1), the analysis of behavioral data obtained using
geolocators and accelerometers was also conducted. These results showed
similar foraging trip durations (minimum estimate as an index; see Fig. S2) between both years for RLKI (12.7
Log-transformed baseline CORT concentrations in RLKI were 0.72
The straight-line distances between the colony and on-water locations of red-legged kittiwakes (RLKI) and thick-billed murres (TBMU) in 2013 (blue bars) and 2014 (red bars). The mean and standard error are presented.
The mean and standard errors in plasma corticosterone concentrations of red-legged kittiwakes (RLKI) and thick-billed murres (TBMU) in 2013 (blue symbol) and 2014 (red symbol).
SSTs within the foraging range (< 350 km from the colony; Fig. 3)
were relatively warmer in 2014 (mean
Surface-feeding RLKI and pursuit-diving TBMU showed differences in habitat use. RLKI foraged extensively over the deep oceanic basin, while TBMU foraged mostly on the shelf. The behavioral and physiological responses to the ocean variability over 2 years differed between the species. Between the 2 study years, SST around the colony was relatively cooler in 2013 than in 2014, probably reflecting the later sea-ice retreat in 2013 as winter sea-ice conditions strongly influence water temperatures during the following summer (Khen, 1999; Overland et al., 1999; Kokubun et al., 2010; Stabeno et al., 2012).
RLKI showed a consistent use of the oceanic habitat with similar levels of
CORT in both years, though they reached to relatively farther areas in 2013
than 2014. In comparison, TBMU used the oceanic basin to the south of the
colony more frequently in 2013, exhibiting relatively farther travel
distances and higher levels of CORT. Based on the
During the study period, the fledgling success (the mean
RLKIs mainly feed on myctophids over deep oceanic regions (Sinclair et al.,
2008; Kokubun et al., 2015). As RLKIs are a surface-feeding seabird, they are
considered to feed on vertically migrating myctophids (Hunt et al., 1981).
The water column in the deep ocean may show less interannual variation in
water temperature compared to that of the shallower shelf region (see Results
in this study) where the deep cold pool (temperature remains below
< 2
Compared to RLKI, TBMU exhibited fluctuating physiological condition and flexible behavioral changes in parallel to the ocean variability between the years, yet without a difference in fledgling success. Late sea-ice retreat is associated with an early, cold-water phytoplankton bloom, relatively low biomass of small shelf copepods, and poor survival of larval and juvenile forage fish, including their main prey (juvenile walleye pollock: Hunt et al., 1996; Sinclair et al., 2008; Renner et al., 2012). However, early sea-ice retreat is associated with a later, warm-water plankton bloom, a large biomass of small shelf copepods later in the season, and high abundance of larval and juvenile forage fish (Hunt et al., 2002). Moreover, forage fish species including juvenile walleye pollock are less abundant on the continental shelf during cold years because they either disperse or travel deeper to avoid cold waters (Hollowed et al., 2012), as juvenile pollock are associated with warm bottom temperatures (Brodeur et al., 1998). A northern location of the ice edge during spring may be linked to higher SST and water temperature at depth (Kokubun et al., 2010; Stabeno et al., 2012). The cold pool acts as a cross-shelf migration barrier for subarctic fish species (e.g., walleye pollock and Pacific cod), forcing these fish to remain on the outer shelf and separating them from food sources in the middle shelf and coastal domain. Thus, a warmer shelf would provide them with a larger area of suitable habitat (Ciannelli and Bailey, 2005; Kotwicki et al., 2005). In addition, distribution and availability of euphausiids and copepods, the prey species for juvenile walleye pollock (Schabetsberger et al., 2000; Ciannelli et al., 2002), likely change in relation to interannual differences in water temperatures in the shelf region (Smith, 1991; Ohashi et al., 2013; Yamamoto et al., 2015). Hence, we assume that the abundance/availability of pollock on the shelf was probably relatively higher in 2014 (the year of warmer SSTs and earlier sea-ice retreat) compared to 2013 (the year of cooler SSTs and later sea-ice retreat). The closer proximity of St. George to the continental shelf break may be considered to be an important buffer in years when food supply on the shelf is poor (Byrd et al., 2008b; Renner et al., 2014). Previous studies showed that TBMU breeding on St. George Island traveled longer distances to forage at the shelf break and the ocean basin in a cold year (Harding et al., 2013). Seabirds are known to increase foraging ranges in response to reductions in prey availability (Suryan et al., 2000; Pinaud et al., 2005; Harding et al., 2007; Bertrand et al., 2012), but longer and farther foraging trips likely cause higher levels of nutritional stress (2013 in this study), especially for TBMU whose flight cost is presumed to be high (Houston et al., 1996).
In this study, chick-rearing RLKIs did not change their foraging locations
largely in relation to marine environmental changes probably due to their
reliance on myctophids, which live in the deep waters of the pelagic zone
(Sinclair and Stabeno, 2002), for feeding young (Kokubun et al., 2015).
However, their foraging effort might also be affected by the position and
strength of local eddies, which are reflected by atmospheric control (the
North Pacific Index and Multivariate ENSO Index; Ladd et al., 2012, and Ladd,
2014). TBMU showed fluctuations in physiological condition and flexible
foraging behavior, which probably corresponded to ocean variability
(exhibited longer and farther trips in the relatively cooler year of 2013).
Hence, although we compared foraging behavior of seabirds in different
environmental conditions only over 2 years with limited sample sizes, our
study has suggested that there is possible interspecific differences in
species' response to warming, which may reflect differences in ecosystem
dynamics between habitats they use for foraging, as the decrease in sea-ice
extent showed negative effects on foraging behavior for other species in a
different Arctic region (e.g., black guillemots
The marine environmental data from NOAA are published as National Oceanic and Atmospheric Administration (2015a) for SSTs and as National Oceanic and Atmospheric Administration (2015b) for IRI. Data obtained from RLKIs and TBMUs are available at the authors upon request.
We are grateful to Marc Romano, Matt Klostermann, US Fish and Wildlife Service, St. George Traditional Council, and St. George Island Institute for logistical support during fieldwork. Martina Müller, Ken Yoda, Toru Hirawake, Kozue Shiomi, and an anonymous referee provided valuable comments on the manuscript. This study was conducted with funds from the Green Network of Excellence Program (GRENE), Arctic Climate Change Research Project “Rapid Change of the Arctic Climate System and its Global Influences”, and with the approval of the University of Alaska IACUC (assurance #471022). Bird handling was conducted under US Fish and Wildlife permit MB703371-3 and Alaska Department of Fish and Game permits 13-079 and 14-109. Edited by: T. Hirawake