Linking northern fur seal behavior with prey distributions: the impact of temporal mismatch between predator studies and prey surveys
© Kuhn et al. 2015
Received: 23 December 2014
Accepted: 24 April 2015
Published: 14 August 2015
An essential part of foraging ecology research is identifying how the distribution and abundance of prey influence predator behavior. However, in marine systems, temporal or spatial mismatches often exist between prey surveys and predator tracking periods, especially for species with large foraging ranges. Using northern fur seals (Callorhinus ursinus) as a model, we investigated how conclusions about predator–prey relationships change with increasing temporal disparity between predator tracking periods and prey surveys. To measure foraging behavior, northern fur seals (n = 20) from St. Paul Island (Alaska, USA) were equipped with satellite tracking transmitters and time-depth recorders from July to October 2006. Fur seal dive and movement metrics were examined in relation to the relative abundance of the fur seals’ primary prey, walleye pollock (Gadus chalcogrammus), reported from the annual eastern Bering Sea groundfish survey. Relationships between foraging behavior metrics and prey abundance were examined within the Bering shelf survey grid cells at three timescales: within 2 weeks of the prey survey, within 1 month, and over the northern fur seal reproductive season (>4 months).
We found significant relationships between northern fur seal behavior and prey abundance, even with the limited sample size at the shortest temporal resolution (2 weeks). Changes in dive behavior that were associated with areas of abundant pollock (for example, increased vertical distance traveled and longer periods of diving) were consistent with previously reported metrics of pinniped foraging success. When behavioral metrics, such as vertical distance traveled and time spent diving, remained significantly related to prey abundance at multiple temporal scales, the relationship strength was reduced as temporal mismatch increased.
Our results suggest that relationships between behavioral metrics and prey abundance vary as temporal mismatch increases between prey surveys and predator tracking periods. For northern fur seals, pollock surveys conducted early in the reproductive season may still provide information useful to examine predator–prey relationships as the reproductive season progresses, albeit with diminished predictive power. Understanding predator–prey relationships, including the impact of varying temporal scales, is particularly valuable for guiding research and conservation strategies for northern fur seals as the population continues to decline.
A key aspect of foraging ecology research is understanding how predator behavior is influenced by the abundance and distribution of prey resources. In the marine environment, predator–prey relationships are challenging to discern given the vast three-dimensional scale and inability to make direct observations in most systems. In addition, measuring prey landscapes for wide-ranging marine predators is a massive undertaking, which can be costly in terms of both resources and time. As a result, few studies have been able to simultaneously measure prey availability and predator behavior over a predator’s entire temporal and spatial foraging range (for example, [1, 2]). Incomplete overlap between predator and prey surveys can lead to spatial or temporal mismatches between datasets and potentially inaccurate conclusions about predator–prey relationships.
On a small scale, predator–prey interactions can be identified through transect surveys (for example, [3, 4]) or focal follow studies [1, 5]. These studies may benefit from direct observations of feeding while simultaneously measuring predator densities and prey patch characteristics, making it possible to address questions of fine-scale behavior [6–8]. However, these studies have limited spatial coverage and often examine only a small portion of the predators’ full foraging range. This can result in spatial mismatches and may limit inferences about predator–prey relationships on a larger scale. For example, Vlietstra  showed that fluctuations in regional prey abundance can shape predator–prey density relationships at small spatial scales. For three marine bird species, predator densities were only correlated with local prey biomass when regional prey abundance was low . Therefore, understanding larger prey landscapes may be critical for accurately interpreting predator–prey relationships.
Researchers can also examine predator–prey relationships by correlating predator behavior measured remotely, via bio-logging devices, with surveys of prey landscapes throughout the foraging range [10–12]. Bio-logging devices include instruments that provide at-sea locations (satellite or GPS) or measure underwater behavior, such as time-depth recorders and accelerometry tags [13, 14]. Bio-logging applications can provide highly detailed measures of behavior over long timescales (months to years); however, the expanded timescales may lead to temporal mismatch between measures of predator behavior and prey surveys [15–17]. For example, Garthe et al.  tracked northern gannets (Sula bassana) from late July to August 2003 to examine foraging behavior in relation to prey densities (capelin, Mallotus villosus) that were measured in mid-July. Although a relationship was found for capelin density and gannet foraging sites, the authors noted that it was surprising that the relationship was not stronger and suggested that movements of the spawning capelin, after the prey survey, could be responsible . Without knowing the impact of temporal or spatial discrepancies, our understanding of predator–prey relationships may be inaccurate or incomplete.
As is the case with many marine predator–prey studies [15–17], temporal mismatches exist between prey surveys and predator tracking periods in this system. Diet studies based on scat indicate that northern fur seals foraging on the Bering Sea shelf predominantly consume walleye pollock (Gadus chalcogrammus), with frequency of occurrence ranging from 62 to 89% [22, 27, 28]. In addition, stable isotopes in northern fur seal tissue suggest that this diet is consistent throughout most of the reproductive season . An annual groundfish survey that measures walleye pollock abundance is conducted on the Bering Sea shelf in early summer (late May to July) . This survey covers the entire Bering shelf foraging habitat used by northern fur seals; however, fur seals rely on this prey resource from June to November . To determine if this survey can provide valuable information about the influence of prey availability on northern fur seal behavior, it is necessary to know the potential impact of this temporal mismatch. Therefore, we investigated how relationships between northern fur seal behavior and prey abundance change with increasing temporal disparity between predator tracking periods and prey surveys.
Fur sea behavior
Fur seals (n = 20) ranged in mass from 30.4 to 54.0 kg (average 39.9 ± 1.3 kg), and mass change was −2.9 ± 0.9 kg over the tracking period (range −9.2 to 4.8 kg, n = 17). Average tracking duration was 76.7 ± 4.8 days, with a range of 13–93 days. Two fur seals were not equipped with a time-depth recorder, three fur seals were not recaptured, and one time-depth recorder failed, which resulted in dive data from 14 fur seals. Location data were acquired from all fur seals (n = 20); however, for four fur seals, the platform terminal transmitters (PTTs) did not transmit through the duration of the study period. This was because one fur seal lost her PTT during the study, and the PTTs for the three fur seals that were not recaptured stopped transmitting before the end of the reproductive season. As a result, these four fur seals had abbreviated location records (13, 26, 58, and 59 days).
Summary of behavior metrics by grid for each temporal scale
Hours in grid/area (h/km2)
0.01 ± 0.002 (0.0007–0.04)
0.02 ± 0.001 (0.0007–0.19)
0.03 ± 0.001 (0.0007–0.37)
Transit rate (km/h)
3.0 ± 0.33 (0.5–7.2)
4.2 ± 0.11 (0.5–10.4)
4.2 ± 0.09 (0.5–12.8)
Dives/grid hour (count/h)
5.4 ± 0.84 (0.22–18.8)
4.0 ± 0.21 (0.06–21.1)
6.4 ± 0.21 (0.06–71.8)
Dives/grid area (count/km2)
0.06 ± 0.009 (0.0007–0.18)
0.07 ± 0.004 (0.0008–0.50)
0.19 ± 0.01 (0.0007–3.12)
Vertical distance/grid hour (m/h)
433.3 ± 57.8 (3.6–1,383.8)
285.4 ± 13.3 (1.4–1,509.7)
386.6 ± 10.4 (1.4–2,436.0)
Vertical distance/grid area (m/km2)
5.8 ± 1.06 (0.02–25.1)
5.2 ± 0.41 (0.01–57.8)
11.3 ± 0.62 (0.01–185.9)
Bottom time/grid hour (min/h)
2.8 ± 0.34 (0.02–6.6)
2.4 ± 0.13 (0–19.6)
3.9 ± 0.12 (0–28.7)
Bottom time/grid area (min/km2)
0.04 ± 0.006 (0.0001–0.12)
0.04 ± 0.003 (0–0.43)
0.12 ± 0.006 (0–1.51)
Percent bottom time
26.6 ± 1.0 (16.4–36.0)
29.9 ± 0.51 (0–50.9)
33.1 ± 0.36 (0–62.5)
Dive time/grid hour (min/h)
9.7 ± 1.3 (0.11–30.7)
6.9 ± 0.32 (0.04–40.7)
10.1 ± 0.26 (0.02–49.8)
Dive time/grid area (min/km2)
0.12 ± 0.02 (0.0007–0.39)
0.12 ± 0.009 (0.0003–1.3)
0.30 ± 0.02 (0.001–3.8)
Descent rate (m/s)
1.0 ± 0.05 (0.54–1.6)
1.04 ± 0.02 (0.26–1.8)
1.02 ± 0.01 (0.19–2.7)
Ascent rate (m/s)
0.93 ± 0.05 (0.49–1.4)
0.91 ± 0.02 (0.34–1.7)
0.90 ± 0.01 (0.25–1.7)
0.63 ± 0.05 (0–1.1)
0.50 ± 0.02 (0–2.1)
0.67 ± 0.01 (0–3.0)
Wiggles/grid hour (count/h)
3.1 ± 0.48 (0–11.4)
2.2 ± 0.19 (0–32.1)
4.5 ± 0.17 (0–31.0)
Wiggles/grid area (count/km2)
0.04 ± 0.007 (0–0.2)
0.04 ± 0.003 (0–0.5)
0.12 ± 0.007 (0–1.8)
Pollock distribution and abundance
During the annual groundfish assessment survey, walleye pollock were captured at 96% of the survey stations with WTCPUE ranging from 0.002 to 1,031.7 kg/ha and NUMCPUE ranging from 0.17 to 1,617.6 fish/ha . The highest densities were found northwest of St. Paul Island on the outer shelf region and just south of St. Paul Island (Fig. 1a, Figure ten in ). Within the grid cells that fur seals used, WTCPUE averaged 126.6 ± 6.3 kg/ha (0.01–1,016.1 kg/ha) and NUMCPUE averaged 171.8 ± 8.7 fish/ha (0.60–1,396.6 fish/ha).
Relationships between fur seal behavior and prey
Results of models used to examine relationships between walleye pollock abundance and northern fur seal behavior
Pollock catch per effort (WTCPUE/NUMCUPE)
Hours in grid/area (h/km2)
NS/P = 0.02
Transit rate (km/h)
Dives/grid hour (count/h)
P = 0.04/P = 0.04
Dives/grid area (count/km2)
P = 0.03/P = 0.02
Vertical distance/grid hour (m/h)
P = 0.01/P = 0.01
P < 0.001/P < 0.001
P = 0.03/P = 0.005
Vertical distance/grid area (m/km2)
P = 0.04/P = 0.04
P = 0.003/P = 0.003
P = 0.03/NS
Bottom time/grid hour (min/h)
Bottom time/grid area (min/km2)
P = 0.04/NS
Percent bottom time
Dive time/grid hour (min/h)
P = 0.02/P = 0.03
P = 0.03/P = 0.03
NS/ P = 0.02
Dive time/grid area (min/km2)
NS/P = 0.04
P = 0.03/P = 0.04
Descent rate (m/s)
P = 0.001/P = 0.001
P = 0.03/P = 0.009
Ascent rate (m/s)
P < 0.001/P < 0.001
P = 0.002/P < 0.001
P = 0.002/P = 0.002
P = 0.04/P = 0.02
Wiggles/grid hour (count/h)
P = 0.01/NS
Wiggles/grid area (count/km2)
P = 0.003/NS
P = 0.04/NS
At the intermediate timescale (1 month), a similar pattern was found with multiple dive metrics related to walleye pollock abundance (Table 2). Vertical distance traveled per grid hour (WTCPUE: t = 3.62, r 2 = 0.07, P < 0.001, and NUMCPUE: t = 3.68, r 2 = 0.07, P < 0.001), vertical distance by area (WTCPUE: t = 3.04, r 2 = 0.05, P = 0.003, and NUMCPUE: t = 2.98, r 2 = 0.04, P = 0.003), dive time per grid hour (WTCPUE: t = 2.14, r 2 = 0.02, P = 0.03, and NUMCPUE: t = 2.17, r 2 = 0.02, P = 0.03), and dive time per area (WTCPUE: t = 2.13, r 2 = 0.02, P = 0.03, and NUMCPUE: t = 2.06, r 2 = 0.02, P = 0.04) were all positively related to prey abundance (Table 2), but with notably lower r 2 values. At the intermediate temporal scale, there was a positive relationship between descent rate and ascent rate for both WTCPUE (t = 3.25, r 2 = 0.05, P = 0.001, and t = 4.30, r 2 = 0.09, P < 0.001, respectively) and NUMCPUE (t = 3.27, r 2 = 0.05, P = 0.001, and t = 4.32, r 2 = 0.09, P < 0.001, respectively). Measures of wiggle behavior were also significant at the intermediate scale, but these metrics varied between WTCPUE and NUMCPUE (Table 2). The average number of wiggles per dive increased with WTCPUE (t = 3.12, r 2 = 0.05, P = 0.002) and NUMCPUE (t = 3.12, r 2 = 0.05, P = 0.002); however, both the number of wiggles per grid hour and per grid area were only significantly related to WTCPUE (t = 2.56, r 2 = 0.03, P = 0.01, and t = 3.05, r 2 = 0.05, P = 0.003, respectively). As temporal scale increased, measures of dive frequency (by hour or area) which were significant at the 2-week scale were no longer significant (Table 2).
At the scale of the full northern fur seal reproductive season, some dive metrics remained significant, and for the first time, grid residence time was significantly related to prey abundance (Table 2). Similar to the intermediate timescale, descent rate and ascent rate increased with WTCPUE (t = 2.12, r 2 = 0.01, P = 0.03, and t = 3.09, r 2 = 0.01, P = 0.002, respectively) and NUMCPUE (t = 2.60, r 2 = 0.01, P = 0.009, and t = 3.63, r 2 = 0.02, P < 0.001, respectively). In addition, some measures of wiggle behavior remained significantly related to WTCPUE, such as average wiggles per dive (t = 2.22, r 2 = 0.01, P = 0.04) and wiggles per area (t = 2.22, r 2 = 0.01, P = 0.04); however, only wiggles per dive was related to NUMCPUE (t = 2.56, r 2 = 0.01, P = 0.02, Table 2). As with the other two temporal scales, vertical distance traveled during a dive and dive time in a survey grid increased with prey abundance. For vertical distance per hour in a grid, both WTCPUE (t = 2.13, r 2 = 0.01, P = 0.03) and NUMCPUE (t = 2.77, r 2 = 0.01, P = 0.005) were significant, but vertical distance by area was only related to WTCPUE (t = 2.22, r 2 = 0.01, P = 0.03). Dive time per grid hour was only correlated with NUMCPUE (t = 2.4, r 2 = 0.01, P = 0.02), whereas bottom time per grid area was only correlated with WTCPUE (t = 2.0, r 2 = 0.01, P = 0.04). Hours spent in grid was only related to NUMCPUE, but this was a negative relationship (t = − 2.25, r 2 = 0.01, P = 0.02, Table 2).
Fur seal behavior and prey density
By spatially and temporally linking northern fur seal behavior with prey abundance, we were able to examine how relationships change in response to varying temporal disparity. The metrics of northern fur seal behavior that were significantly related to prey abundance at the shortest temporal scale are consistent with indices of foraging behavior identified in other marine predators, including northern fur seals in Russia (for example, [30–32]). Dive rate or dive frequency has been shown to increase when animals are successfully catching prey or when animals are on their main foraging grounds [30, 33, 34]. For example, when feeding occurred, gray seal (Halichoerus grypus) dive bouts had a greater number of dives than when prey were not captured . Subantarctic fur seals (Arctocephalus tropicalis) significantly increased dive rate (dives/h) during the feeding phase of their foraging trips in areas where their main prey were abundant . During this feeding phase, subantarctic fur seals also increased the vertical distance per hour during dives to over seven times greater than what was measured during the earlier transit phase . An increase in vertical distance during diving was also found to be positively related to mass gain for northern fur seals breeding at Lovushki Island, Russia . Although the mass gain was determined for an entire foraging trip, this suggests that successful foraging is related to diving effort for northern fur seals . Associated with the increased diving activity (frequency and distance covered), increased time spent diving has also been related to marine predator feeding behavior [35, 36]. In a captive setting, gray seals were found to significantly increase dive duration with increasing prey encounter rate . For European shags (Phalacrocorax aristotelis), the amount of prey ingested was positively related to both the duration of a single dive and the duration of an entire dive bout .
Other metrics that have been associated with increased prey encounter rate for marine predators were not found to be significant for northern fur seals at the shortest temporal scale. For example, undulations (wiggles) during the bottom phase of a dive have been linked to prey capture attempts for species such as penguins and seals [31, 37, 38]. For northern fur seals in Russia, Skinner et al.  did not find a relationship between wiggles and mass gain over a foraging trip and suggested this behavior may not reflect actual prey capture attempts in this species. For gray seals, accumulated bottom time was 3.5 times greater for feeding versus non-feeding bouts , but a similar relationship was not found for northern fur seals. However, many studies have shown that dive indices related to prey capture can vary significantly among species and may be shaped by the specific prey being targeted [39–41]. For example, when using the ‘sit and wait’ foraging strategy, harbor seal (Phoca vitulina) dives were found to have longer bottom times and lower bottom swim speeds than when employing an active foraging strategy . As a result, future studies examining how predator–prey relationships change over time should validate these dive metrics to confirm they are indicative of foraging success or prey encounter for northern fur seals.
The one behavioral metric that appears to be consistently related to foraging behavior for marine predators, and that we found to be insignificant, is residence time in an area (for example, [42, 43]). Marine predators feeding on patchily distributed prey can increase foraging success by employing area-restricted search patterns in response to prey encounter [44–46]. This area-restricted search behavior should increase retention within a grid cell if animals are successfully foraging. For example, the swimming paths of basking sharks (Cetorhinus maximus) became more convoluted as prey density increased, resulting in sharks spending the greatest amount of time in the highest density prey patches . Bailey and Thompson  showed that bottlenose dolphins (Tursiops truncatus) concentrated search effort in areas where feeding occurred compared to their movements throughout the rest of the study region. For northern fur seals, grid residence time was only significantly related to prey abundance at the longest temporal scale, which was a weak negative relationship. It has been previously suggested that northern fur seals forage while transiting, which may limit the number or intensity of area-restricted search periods during foraging trips, reducing residency times [47, 48]. In addition, other fur seal behaviors not related to feeding, such as resting and grooming, may impact time in a grid cell regardless of prey abundance. Finally, it is important to consider the constraints faced by female northern fur seals during the reproductive season, which may shape how fur seals allocate their time at sea. Trip durations are limited by the fasting duration of the dependent pup waiting onshore [23, 24, 49]. Therefore, if grids with higher densities of prey are distributed away from the rookery, females must spend a larger proportion of their time traveling, which may reduce the amount of time available to forage before needing to return to the rookery. To examine the impacts of this constraint, distance from the rookery could be included as a factor in further models examining the relationship between prey abundance and residence time [22, 50].
Impacts of temporal disparity
As the temporal disparity increased, relationships between prey abundance and northern fur seal behavior changed. Metrics of dive rate lost significance with increased temporal disparity, but other dive variables, such as vertical distance traveled during a dive and total dive time, remained significant. Nevertheless, the strength of these relationships decreased as temporal mismatch between northern fur seal data and the prey survey increased, and at the scale of the full reproductive season, r 2 values for all relationships were nearly zero. Because many significant relationships persisted at the intermediate scale, this suggests that using fur seal behavioral data within 1 month of prey surveys may still provide valuable information to examine predator–prey relationships, albeit with diminished predictive power. This consistency at the intermediate temporal scale could be related to the behavior of the fur seals’ prey, the stability of the environment, or the strong foraging site fidelity previously described for northern fur seals [51–54].
After spawning in the spring , walleye pollock migrate to the Bering shelf region to forage [53, 54]. For the purpose of stock assessment, it is assumed that walleye pollock do not change distribution during the 3-month survey period . However, based on interannual variability in walleye pollock distribution in relation to water temperature, Kotwicki et al.  proposed that during the summer some walleye pollock may move to the north and northeast as water temperature increases and suitable habitat becomes more available. These movements appear to be based on fish size, with immature fish migrating a shorter distance and most of the larger fish not moving at all . Therefore, if a survey grid is primarily composed of these relatively stationary size classes, measurements of abundance reported in June/July may accurately reflect localized abundance later in the summer.
Additionally, the early season surveys may be identifying hotspots for walleye pollock that are enhanced by physical or oceanographic features, resulting in high fish retention after the survey has occurred [52, 57–59]. The middle shelf region of the Bering Sea, which is defined by depths of 50–100 m, is characterized by a strong, persistent thermocline [60–64]. Thermoclines can act to aggregate prey, increasing encounter rate and foraging success for marine predators [54, 65–67]. In addition, at the inner front, which separates the middle and inner shelf regions, nutrient-rich bottom waters from the middle shelf can be mixed with the surface layer, leading to prolonged primary production [57, 68]. The regional stability and localized enrichment could make this a profitable foraging area for fish and other marine predators, acting as a hotspot over the summer months.
A final factor that may be influencing the consistency in pollock–fur seal relationships at the intermediate temporal scale is foraging site fidelity by northern fur seals [51, 69]. When prey resources are predictable, predators can increase foraging success by returning to areas of previous success [70, 71]. Call et al.  found that most northern fur seals returned to foraging locations on subsequent trips over a 48 ± 1.9-day period (two to eight trips per individual). Therefore, even if changes in prey distribution occur at the intermediate temporal scale, fur seals could still be visiting grids that had previously been associated with high walleye pollock abundance before moving on to new foraging areas.
For northern fur seals, autumnal storms have been linked to disruptions in foraging behavior that result in changes to the foraging site fidelity that has been previously described and, in some cases, leads to increased foraging effort . In 2006, in particular, Sterling  showed that, after a storm in early September, northern fur seals spent more time foraging than prior to the storm. These late season storms can impact lower trophic levels by dispersing nutrients and causing shifts in circulation patterns [57, 60], which may in turn lead to shifts in prey distribution or the disruption of features that lead to persistent hotspots (for example, ). As a result, these late season environmental changes may reduce the predictability of prey encounters and could be linked to the reduced strength of predator–prey relationships at the longest temporal scale, the entire reproductive season.
Study limitations and future directions
For this study, as temporal mismatch between datasets was reduced, we were also faced with a reduction in the amount of data available to examine fur seal behavior. As a result of the small sample size at the 2-week scale, we limited model complexity to single-metric analyses. Complex models that include interactions between behavioral metrics (for example, ), including distance from the rookery, may be more suitable for examining predator–prey relationships for northern fur seals, but these types of models would require testing with a larger dataset. In addition, the limited power with the smaller sample size may have reduced our ability to find significance for some behavior metrics at the shortest temporal scale, such as ascent rate and wiggles, which were significant at other scales. Nevertheless, we believe this study provides a starting point for further analyses by identifying the impacts of temporal mismatch and emphasizing the need to take it into consideration for future research examining predator–prey relationships.
Although walleye pollock are the dominate prey of northern fur seals at the Pribilof Islands, diet can vary among breeding locations and years [27, 28, 73]. For this study, we assumed fur seals were foraging on walleye pollock and that other secondary prey species did not influence the behavioral metrics examined. This assumption is supported by diet data acquired from scat analyses for fur seals at the study locations in 2006 [22, 27]. At the Reef and Vostochni rookeries, walleye pollock frequency of occurrence in scat was 68.9 and 89.3%, respectively [22, 27]. An additional 25% frequency of occurrence of unidentified gadids were found in the scats from the Reef rookery, which likely included walleye pollock and would have resulted in an even higher frequency of occurrence at that location [22, 27].
An additional consideration is the coarse resolution of the prey survey data (20 × 20 nm grids). Predators can respond to their environment, including prey availability, at multiple spatial scales (for example, [74, 75]). Northern fur seals have been shown to respond to environmental factors from the scale of meters up to the entire foraging range [50, 76]. Here, we found that, even at this coarse spatial scale, significant relationships exist between fur seal behavior and prey abundance. The benefit of using this prey survey dataset is that it is collected annually and it covers the entire Bering shelf summer foraging range of northern fur seals. Recently, additional surveys of walleye pollock have occurred during the summer season, including biennial acoustic surveys of the mid-water column and late season mid-water trawl surveys [77–79]. Together, these surveys provide a comprehensive dataset for walleye pollock distribution in the Bering Sea, although the eastern Bearing Sea bottom trawl survey is still the most consistent and covers the largest range [29, 77–79]. Integrating these data on walleye pollock with continued studies of northern fur seal at-sea behavior, and having an understanding of the impacts of temporal mismatch, will allow for future research to examine fur seal behavior in relation to prey and to track how these relationships change over time.
As marine environments continue to change, either from climate-related or anthropogenic threats, it becomes crucial to understand relationships between marine predators and their prey. Walleye pollock is the most abundant forage fish in the Bering Sea  and many species of fish, seabirds, and marine mammals depend on this population as a prey resource [81, 82]. In addition, walleye pollock distribution and recruitment are fundamentally linked to temperature variability in the Bering Sea [53, 83, 84]. As climate models predict future warming in the Bering Sea, changes to walleye pollock distribution and abundance may have adverse impacts on northern fur seal populations [85, 86]. By identifying northern fur seal behaviors associated with prey encounter and potential foraging success, it may be possible to predict or model the impacts of climate-related changes to the northern fur seals’ habitat and prey resources. This is particularly valuable for developing effective management and conservation strategies as the northern fur seal population continues to decline.
By spatially and temporally linking predator tracking data with prey surveys, we were able to examine the impact of temporal disparity on our understanding of predator–prey relationships. Although relationships between northern fur seal behavior and walleye pollock abundance existed at all temporal scales, the correlation strength was noticeably diminished as temporal mismatch increased. For northern fur seals, it appears that prey surveys collected within 1 month of predator-tracking studies may still provide valuable information about the influence of prey abundance on predator behavior.
Fur seal dive and location analysis
Research was conducted on St. Paul Island, Alaska (USA, Fig. 1a) from 7 July to 18 October 2006. Adult female northern fur seals were instrumented at two rookeries, Reef (n = 10, 57.1°N, 170.3°W) and Vostochni (n = 10, 57.3°N, 170.1°W). Females with new-born pups were removed from a harem and weighed using a digital scale (±0.2 kg). Bio-logging instruments were attached to the dorsal pelage using quick-set epoxy while the individuals were physically restrained. After multiple foraging trips, the fur seals were recaptured to recover instruments and reweighed prior to release.
Eighteen fur seals were equipped with an Mk9 time-depth recorder (TDR; Wildlife Computers, Redmond, USA) and a KiwiSat 101 (Sirtrack, Havelock North, New Zealand) PTT that provided at-sea locations. An additional two fur seals were equipped with only a PTT. For animals equipped with a TDR, dive depth and ambient water temperature were sampled at 5-s intervals (resolution and accuracy: 0.05 m ± 1% of depth reading and 0.05°C ± 0.01°C). To maximize transmission duration, PTTs were duty-cycled for 4 h on and 4 h off starting at 03:00 GMT. PTTs shut off after a 4-h dry period and restarted when submerged. To facilitate instrument recovery, each female was also equipped with a VHF tag (Advanced Telemetry Systems, Isanti, MN, USA).
Dive data were processed using Instrument Helper (Wildlife Computers), with a dive defined by a minimum depth of 5 m and duration of 10 s. Dive depth (m), dive duration (s), number of wiggles (vertical excursions >1 m during bottom time), wiggle distance (total vertical distance covered by all wiggles, m), descent rate (m/s), and ascent rate (m/s) were calculated for each dive. Bottom time (s) was calculated as the time between the first and last inflection points at greater than 90% of the maximum dive depth, and percent bottom time was calculated as bottom time divided by dive duration. Vertical distance was the distance covered during descent and ascent plus the sum of wiggle distances in the bottom phase of the dive .
To remove erroneous locations, PTT locations were filtered based on a maximum transit rate of 3 m/s (R package ‘argosfilter’) [22, 69, 87, 88]. Foraging tracks were reconstructed by modeling the filtered PTT data using a continuous-time correlated random walk model . Locations were modeled hourly to determine residence time (hours spent in each grid) and transit rate (km/h) and modeled for each dive for all other behavioral metrics.
Walleye pollock distribution and abundance were measured during the NOAA Fisheries annual groundfish assessment survey from May to July 2006 , and data were downloaded from the Groundfish Assessment Program of the Alaska Fisheries Science Center (NOAA, http://www.afsc.noaa.gov/RACE/groundfish/survey_data/). Details of the survey study design can be found in Lauth and Acuna . Bottom trawls were conducted in the center of 37.04 × 37.04 km (20 × 20 nm) grids on the Bering Sea shelf, with higher density surveying occurring around the Pribilof Islands at the corners of some grids (Fig. 1a). Trawls were conducted for 30 min at a transit speed of 1.54 m/s . Walleye pollock weight [weight catch per unit effort (WTCPUE, kg/ha)] and density [fish per unit effort (NUMCPUE, fish/ha)] were calculated for each trawl. WTCPUE and NUMCPUE values were used as an index of relative abundance for comparison among grid cells (from hereon called ‘abundance’). For walleye pollock stock assessment analyses, it is assumed that distributions remained stationary during the duration of the groundfish survey (30 May through 28 July) .
Although the groundfish survey focuses on walleye pollock distributed near the sea floor, primarily targeting fish that are generally 4 years and older [29, 90], we believe these data can be used as an index of the juvenile and adult walleye pollock available to fur seals. Walleye pollock are cannibalistic, and it is estimated that approximately 40% of the juvenile mortality results from consumption by older fish [90, 91]. This high level of mortality occurs when there is spatial overlap between age classes [91, 92]. Bolt et al.  showed that over a 20-year period (1985–2006), between 55 and 85% of the bottom trawl survey stations had co-occurrence of young and adult walleye pollock. In 2006, a mid-water survey of walleye pollock, which included age 1 and older fish, also found little spatial segregation between the distributions of young and older walleye pollock (see Figures 1.10 and 1.20 in ). Therefore, we believe the bottom trawl survey data can be an indication of the walleye pollock available for northern fur seals on the Bering Sea shelf.
Relationships between fur seal behavior and prey abundance
Using dive and movement variables previously suggested as metrics for increased prey encounter rate or foraging success in marine predators (for example, [30, 32, 93, 94]), we examined relationships between fur seal behavior and prey abundance in each survey grid utilized by fur seals. Because survey stations were not all the same size (due to the higher density sampling around the Pribilof Islands, Fig. 1a), behavior metrics that were based on counts within a grid cell were adjusted for grid area. For each fur seal, we calculated hours per grid area, average transit rate, dives per hour in grid, dives per grid area, vertical distance per hour in grid, vertical distance per grid area, bottom time per hour in grid, bottom time per grid area, average percent of bottom time during dives, average wiggles per dive, wiggles per hour in grid, wiggles per grid area, total dive time per hour in grid, total dive time per grid area, average descent rate, and average ascent rate (Table 2). Each dive and movement metric was determined at three temporal intervals: over the full reproductive season (July to October, ‘full’), within 1 month of the prey survey (‘1 month’), and within 2 weeks of the survey (‘2 weeks’). Behavior metrics in a grid were assessed for each temporal scale by identifying the actual prey survey date and including only measurements that occurred within the specified time window. This spatial and temporal linking ensured that we were only measuring behavioral metrics that occurred within 2 weeks or 1 month of the prey survey.
We assumed that behavior metrics at the shortest timescale accurately reflected fur seals’ response to prey abundance. If significant relationships were maintained as the temporal scales increased, this would suggest that walleye pollock distributions do not change significantly between July (during the survey period) and October. This temporal consistency in prey distributions would be only slightly longer than what is assumed for the stock assessment analyses (May to July) . However, if the relationships break down with increasing temporal disparity, then significant shifts in the pollock distribution or fur seal diet may have occurred over the fur seal reproductive season.
We used linear mixed effect models (R package ‘lme4’)  to compare behavior metrics with walleye pollock catch weight (WTCPUE) and abundance (NUMCPUE). To account for variation in behavior among fur seals, animal ID was included as a random factor in all models. All relationships were considered significant at P < 0.05 and means are reported ±SE.
All northern fur seal research was conducted in accordance with and under the authority of the United States Marine Mammal Protection Act (National Marine Fisheries Service, NMFS Permit 782-1708). At the time of the study, there were no additional requirements by NMFS for institutional review of these procedures. Recently, an NMFS Institutional Animal Care and Use Committee was established for the Alaska Fisheries Science Center and the capture and handling protocols described here were approved by this committee.
CK determined the study design, analyzed fur seal data in relation to walleye pollock abundance, and drafted the manuscript. JS collected northern fur seal behavior data and contributed to manuscript preparation. TZ was responsible for the initial analysis of northern fur seal dive and movement data and contributed to the manuscript preparation. All authors read and approved the final manuscript.
Staff of the Alaska Ecosystems Program collected northern fur seal field data and provided support with data analysis. Funding and personnel were also contributed by the University of Alaska Fairbanks and the North Pacific Research Board. We thank R. Ream, H.M. Liwanag, Reny Tyson, and one anonymous reviewer for providing critical reviews that greatly improved the final manuscript. The findings and conclusions in the paper are those of the author(s) and do not necessarily represent the views of the National Marine Fisheries Service, National Oceanic and Atmospheric Administration (NOAA). Reference to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA.
Compliance with ethical guidelines
Competing interests The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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