Marine protected areas (MPAs) are increasingly being used as a conservation tool for highly mobile marine vertebrates and the focus is typically on protecting breeding areas where individuals are aggregated seasonally. Yet movements during the non-breeding season can overlap with threats that may be equally as important to population dynamics. Thus understanding habitat use and movements of species during the non-breeding periods is critical for conservation. Glacier Bay National Park, Alaska, is one of the largest marine mammal protected areas in the world and has the only enforceable protection measures for reducing disturbance to harbor seals in the United States. Yet harbor seals have declined by up to 11.5%/year from 1992 to 2009. We used satellite-linked transmitters that were attached to 37 female harbor seals to quantify the post-breeding season migrations of seals and the amount of time that seals spent inside vs. outside of the MPA of Glacier Bay. Harbor seals traveled extensively beyond the boundaries of the MPA of Glacier Bay during the post-breeding season, encompassing an area (25,325 km2) significantly larger than that used by seals during the breeding season (8,125 km2). These movements included the longest migration yet recorded for a harbor seal (3,411 km) and extended use (up to 23 days) of pelagic areas by some seals. Although the collective utilization distribution of harbor seals during the post-breeding season was quite expansive, there was a substantial degree of individual variability in the percentage of days that seals spent in the MPA. Nevertheless, harbor seals demonstrated a high degree of inter-annual site fidelity (93%) to Glacier Bay the following breeding season. Our results highlight the importance of understanding the threats that seals may interact with outside of the boundaries of the MPA of Glacier Bay for understanding population dynamics of seals in Glacier Bay.
Citation: Womble JN, Gende SM (2013) Post-Breeding Season Migrations of a Top Predator, the Harbor Seal (Phoca vitulina richardii), from a Marine Protected Area in Alaska. PLoS ONE 8(2): e55386. https://doi.org/10.1371/journal.pone.0055386
Editor: Andreas Fahlman, Texas A&M University-Corpus Christi, United States of America
Received: August 27, 2012; Accepted: December 23, 2012; Published: February 14, 2013
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: Funding and logistical support was provided by the National Park Service (NPS)-Natural Resource Preservation Program (Project# 35747), Glacier Bay National Park & Preserve, the NPS Coastal Cluster Program, the Alaska Fisheries Science Center-National Marine Mammal Laboratory-Polar Ecosystem Program, the Alaska Department of Fish & Game, the Alaska Sealife Center, and the United States Fish & Wildlife Service. JNW was supported by a Horace M. Albright-Conrad L. Wirth Fellowship through the National Park Foundation, the Oregon State University (OSU) Hatfield Marine Science Center Mamie Markham Research Fellowship, the OSU Marine Mammal Institute, the OSU Pinniped Ecology Applied Research Laboratory, the OSU Department of Fisheries & Wildlife Munson Wildlife Fellowship, and NPS NRAC Professional Development Grants. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Two common objectives for marine protected areas (MPAs) are enhancement of commercial fisheries for sustaining or rebuilding yield, and conservation of biodiversity –. Although the target of biodiversity conservation is often specific habitat features or sensitive ecosystems, increasingly MPAs are being utilized as tools to conserve highly mobile pelagic taxa such as marine mammals, seabirds, and turtles –. For example, the number and diversity of MPAs designated for the conservation of marine mammals is growing globally  with increasing calls for more and larger networks of MPAs .
Nevertheless, MPA designation can be less than effective in meeting conservation goals for highly mobile marine taxa for a number of reasons. Although the timing and location of the MPAs should correspond to the temporal and spatial distribution of the threat, the actual designation of the MPA boundaries more likely reflects trade-offs between sociocultural, economic, and biological factors , . The vaquita (Phocoena sinus) provides a good example where a clearly defined population threat such as bycatch  can be mitigated with a simple MPA-based solution by expanding existing MPA boundaries  but economic constraints prevents its implementation sufficiently to meet the conservation objectives. Additionally, MPAs may not meet species conservation objectives because they may not correspond temporally or spatially with the most pressing threat to the population . For example, many MPAs are established to protect the breeding aggregations of pinnipeds, sea turtles, seabirds, and cetaceans. While important, research demonstrates that major threats may actually occur during post breeding migrations  or during dispersal of juveniles .
Recognizing that MPAs are a means to a conservation end, monitoring and research for understanding threats and reducing uncertainty into population responses is not just fundamental to understanding MPA effectiveness  but also central to conservation efforts for all highly mobile vertebrates .
Glacier Bay National Park (Figure 1) is a Biosphere Reserve and World Heritage Site, encompassing over 600,000 acres (242,811 hectares) of marine waters . Although the park was not created solely to protect marine mammals, it functionally serves as the one of the largest marine mammal protected areas in the world  with a suite of regulations intended to minimize threats to these species and to sustain a healthy ecosystem for their conservation. For example, regulations require large ships to reduce speed in areas of contemporary and historically high concentrations of endangered humpback whales (Megaptera novaeangliae) to reduce the probability of a collision. Glacier Bay is also home to the only enforceable regulations in United States waters aimed at protecting harbor seals (Phoca vitulina richardii) from vessel and human-related disturbance . Spatial and temporal regulations for vessels transiting in and near harbor seal breeding areas, and operating regulations once in those areas, are all aimed at reducing impacts of human visitation. Furthermore, subsistence hunting of harbor seals has been prohibited in the park since 1974  and commercial fishing within the MPA boundaries of Glacier Bay is being phased out .
The map includes harbor seal haulout sites (black circles), closures associated with harbor seal haulout sites (red areas), non-motorized area closures (green areas), dates of closures for each area, and the boundary of marine protected area of Glacier Bay National Park (grey outline). Harbor seals were tagged at the glacial ice haulout site in Johns Hopkins Inlet.
By most measures the populations of marine mammals that utilize Glacier Bay are healthy and increasing. Populations of humpback whales using Glacier Bay and surrounding areas are increasing by 5.1% per year . Steller sea lions (Eumetopias jubatus) have increased in the Glacier Bay region by 8.2%/year from the 1970’s to 2009, representing the highest rate of growth for this species in Alaska . In addition a Steller sea lion rookery and several haul outs have recently been established in the Glacier Bay region , . Sea otters (Enhydra lutris), once hunted to extirpation in southeastern Alaska  have increased exponentially in Glacier Bay from just a few animals in 1995 to greater than 2,300 in 2004 .
In sharp contrast, harbor seals have been rapidly declining ,  despite stable or slightly increasing trends in nearby populations . A suite of recent studies suggest that (1) harbor seals in Glacier Bay are not significantly stressed due to nutritional constraints , (2) the clinical health and disease status of seals within Glacier Bay is not different than seals from other stable or increasing populations , and (3) disturbance by vessels does not appear to be a primary factor driving the decline .
Collectively then, harbor seals in Glacier Bay may be one of the most protected populations of marine mammals in the world, yet the most recent population monitoring data suggest that the declines have not abated or reversed . Here we explore the extent to which harbor seals may be using habitat outside the MPA of Glacier Bay. Although evidence suggests that substantially fewer seals occur in Glacier Bay in late-summer and autumn , it is unknown if seals move beyond the boundaries of Glacier Bay, the regions that they may travel to, and the potential threats encountered. Thus, a first fundamental step is to identify movement patterns and habitat use of harbor seals in relation to the boundaries of the MPA of Glacier Bay. Our primary objectives were to quantify the (1) spatial distribution of seals during the post-breeding season (September−April), (2) estimate the utilization distribution of seals relative to the boundaries of the MPA of Glacier Bay, (3) quantify the degree of individual variability in residency patterns of seals in Glacier Bay, and (4) and assess the degree of inter-annual fidelity of seals back to Glacier Bay the following breeding season (May–June).
Materials and Methods
All harbor seal capture, handling, and research was conducted under Marine Mammal Protection Act (MMPA) permit numbers 358-1787-00 and 358-1787-01 issued to the Alaska Department of Fish & Game and MMPA permit number 782-1676-02 issued to the National Marine Mammal Laboratory by National Oceanic and Atmospheric Administration (NOAA) -Protected Resources Division. Harbor seal capture, handling, and research was also authorized by Glacier Bay National Park under Scientific Research and Collecting permit numbers GLBA-2007-SCI-0003, GLBA-2008-SCI-0004, and associated Glacier Bay National Park and Preserve Waivers to park regulations. Animal use protocols used in this research were reviewed and approved by the Institutional Animal Care and Use Committee at the State of Alaska Department of Fish & Game (protocol 07-16).
Glacier Bay is an estuarine fjord in southeastern Alaska that constitutes a part of Glacier Bay National Park (Figure 1). Distinct oceanographic and circulation patterns , , as a result of rapid and repeated advances and retreats of tidewater glaciers over the past 225 years –, have resulted in sustained levels of mixing, high levels of primary productivity, and abundant communities of forage fish , . Johns Hopkins Inlet (58° 50.896' N, −137° 6.121' W), an expansive (12 km long × 2.5 km wide) tidewater glacial fjord in the upper West Arm of Glacier Bay (Figure 1), was chosen as the capture location for seals because the inlet hosts the largest aggregation of seals (>2,000) in Glacier Bay during the summer months and represents one of the primary glacial ice pupping sites for harbor seals in Alaska , , . In Johns Hopkins Inlet, seals rest upon glacial ice and icebergs that have calved from two advancing tidewater glaciers, the Johns Hopkins glacier and the Gilman glacier.
Harbor Seal Capture and Instrument Deployment
Juvenile and adult female harbor seals were captured using monofilament nets deployed from inflatable skiffs in September of 2007 (n = 15 seals captured) and 2008 (n = 22 seals captured) (Table 1). Following capture, seals were transported to a research vessel (R/V Steller) where they were weighed and curvilinear body length and axial girth were measured. Seal age was determined via morphometrics; seals >3 years old were classified as adults, seals ≤3 years of age were considered as juveniles .
To quantify the spatial and temporal distribution of harbor seals from September through June, we attached satellite-linked transmitters (Spot5, 71.5 mm × 34 mm × 26 mm, 78 g, Wildlife Computers, Redmond, Washington, U.S.A.) to the fur on the heads of juvenile and adult female harbor seals using Devcon 5-minute epoxy adhesive. The instruments were only attached to seals that had obviously completed molting. Instruments were deployed over a 5-day period (11–15 September) in 2007 and over a 7-day period (13–19 September) in 2008. The transmitters were powered by two AA batteries and included a 0.5 w transmitter with a transmission repetition rate of 45 seconds. Conductivity switches inhibited transmissions while seals were in the water and quantified the percent time per hour that the seal was out of water. Instruments were shed during the annual molt which began the following June after capture and varied depending upon the age of the animal, with younger seals molting earlier than older seals .
Track Analysis Using State-Space Models
Locations from each satellite-linked transmitter were estimated by Service Argos (Collecte Localisation Satellite, CLS America, Inc., Largo, Maryland) and downloaded. The Argos locations were filtered with the Douglas Argos-Filter Algorithm v. 7.03  using the following parameters: spatial redundancy (5 km) and maximum sustained rate of movement (10 km/hr).
Following filtering, hourly positions between observed locations were predicted using a continuous-time version of the correlated random walk model (CTCRW) . The CTCRW model incorporates a covariate for Argos location error which is comprised of 6 location classes (Location Class 3, 2, 1, 0, A, B). In addition, a continuously-valued covariate for the percent of each hour spent out of the water for a seal was included in the movement model to account for haulout behavior of seals. The CTCRW model was fit using the Kalman-filter on a state-space version of the continuous time stochastic movement process using the CRAWL package  in R (version 13.1). The CTCRW model resulted in an estimate of the most probable track of a seal at hourly intervals, while accounting for Argos location error . Locations that fell on land were removed to establish the final set of locations that were used for subsequent analyses.
Utilization Distribution of Harbor Seals Relative to MPA of Glacier Bay
Utilization distributions  were used to quantify space use of seals relative to the boundary of the MPA of Glacier Bay National Park. A utilization distribution depicts the intensity of use of an area by an animal or a group of animals  and is defined as the probability distribution of detecting an animal in given grid cell within a specified time period .
The tracks for all seals were pooled to collectively estimate the utilization distribution of seals during the post-breeding season. Utilization distributions for seals were estimated at two-month intervals, or five different time periods, from September through June. The two-month time intervals groupings were based upon similarities in the average distance moved per day per month. Grid cells were chosen as the spatial unit of analysis as they often perform better than other methods, such as minimum convex polygons and kernel density estimation, for quantifying space use of animals . A grid cell size of 25 km2 was chosen to allow for detection of individual-scale movements while also providing relatively smooth contours between grid cells . Seal locations were spatially joined with grid cells in ArcGIS and the total number of seal locations per grid cell was summed. The number of seal locations per grid cell was normalized by dividing the number of seal locations per grid cell by the total number of locations for that time period which yielded the proportion of total locations per grid cell for each time period. Proportions of locations per grid cell were sorted from largest to smallest and the cumulative proportions of locations per grid cell were determined to create utilization distributions using custom tools in ArcGIS .
The utilization distribution identified the set of all grid cells where a seal location occurred and quantified the probability of detecting a seal in given grid cell within a specified time interval. Grid cells included in the 100% utilization distribution represented areas with the lowest intensity of use by seals whereas grid cells in the 10% utilization distribution represented areas with the highest intensity of use . Utilization distributions of seals for each two-month interval were evaluated with respect to the boundaries of the MPA of Glacier Bay (Figure 1) by estimating the percentage of grid cells that occurred in the 10 (highest), 50, 80, and 100% (lowest) utilization distributions that occurred in the MPA. For the purposes of these analyses, the MPA of Glacier Bay was defined as Glacier Bay proper or all waters inside a line drawn between Point Gustavus (58°2.748′ N, 135°54.927′ W) and Point Carolus (58°22.694′ N, 136°2.535′ W) as all NPS seasonal closures and protection measures focused on harbor seals occur within these boundaries (Figure 1). There were three grid cells that overlapped with the boundary of the MPA of Glacier Bay between Point Gustavus and Point Carolus. If greater than 50% of the area of the grid cell fell inside the boundary of the MPA then the grid cell was considered to be inside the MPA. If greater than 50% of the area of the grid cell fell outside of the boundary of the MPA then the grid cell was considered to be outside of MPA.
Individual Residency Periods of Harbor Seals in Glacier Bay
The residency periods of individual harbor seals were estimated by determining the proportion of days that a seal spent in Glacier Bay during the post-breeding period, from September through April, using the Douglas Argos-Filter Algorithm (v. 7.03)  which selected the best location for each seal per day based on the distance, angle, and rate to the previous and subsequent locations . Residency periods were estimated by plotting the best daily location for each seal in ArcGIS and then assigning each daily location to inside or outside of the MPA of Glacier Bay. The number of days that individual seals spent inside of Glacier Bay was summed to estimate residency periods for individual seals. We only considered seals with complete records, which included seals with tags that transmitted from September through April (n = 27 seals), encompassing 8 months of the post-breeding season.
Multi-response permutation procedures (MRPP), based on a rank-transformed Sørenson distance matrix , , were used to test for differences in the percentage of days spent by seals in Glacier Bay and the cumulative distance traveled by juvenile and adult seals using PC-ORD . The Sørenson proportional coefficient  was used as the distance measure and the A test statistic, which ranges from 0 to 1, was reported as a measure of effect size along with the corresponding p values.
Transmitters remained attached to harbor seals for the majority of the post-breeding season (September – April) providing excellent spatial coverage of seal distribution and totaling 8,836 seal tracking days. The average deployment period for satellite-linked transmitters was 238.8 days ±83.7 (SD) (range: 37–335 days) and in some cases transmitters provided location data on individual seals for up 11 months (September to August). Transmitters deployed on adult females ( = 272.4 days ±80.1) (range: 106–335 days) transmitted slightly longer on average than those deployed on juvenile seals ( = 224.0 days ±85.4) (range: 37–328 days) likely reflecting the differences in the timing of the annual molt as juveniles molt earlier than adults. 73% (27 of 37) of tags transmitted through May 1st (∼8 months) of the following year after capture.
Utilization Distribution of Harbor Seals Relative to MPA of Glacier Bay
During the post-breeding season, both juvenile and adult female harbor seals ranged extensively both within and beyond the boundaries of the MPA of Glacier Bay. Whereas the glacial ice breeding area of Johns Hopkins Inlet encompasses approximately 22 km2, the area used by seals during the post-breeding season encompassed approximately 25,000 km2 of which only 2,400 km2 was in the MPA of Glacier Bay. Once the seals exited the MPA, they ranged extensively to regions throughout the inside and outside waters of the northern portion of southeastern Alaska and to areas along the continental shelf region of the eastern Gulf of Alaska from Sitka to Prince William Sound (Figures 2, 3, 4, 5). Some seals traveled up to 900 km away (minimum one-way distance) from Glacier Bay to areas in and near Prince William Sound in south-central Alaska. The areas used by seals were primarily restricted to waters along the continental shelf with a few exceptions (Figures 2, 3, 4, 5). Several seals also visited other glacial fjord habitats, including Disenchantment Bay and Icy Bay near Yakutat, during the post-breeding season.
Boundary of the marine protected area (MPA) of Glacier Bay is shown as black line. JHI indicates tagging location in Johns Hopkins Inlet.
Boundary of the marine protected area (MPA) of Glacier Bay is shown as black line. JHI indicates tagging location in Johns Hopkins Inlet.
Boundary of the marine protected area (MPA) of Glacier Bay is shown as black line. JHI indicates tagging location in Johns Hopkins Inlet.
For harbor seals whose tags transmitted from September through April (n = 27), the average cumulative straight-line distance traveled was 2,011 km (±698 SD) (range: 804–3,411 km). The average cumulative distance traveled by juvenile seals (n = 18) was 2,018 km (±501 SD) (range: 1,237–3,239 km) and by adult females seals (n = 9) was 1,198 km (±1,025 SD) (range: 804–3,411 km). There were three seals, one juvenile and two adult females, whose cumulative distance traveled during the post-breeding season exceeded 3,000 km. Differences were not detected in the cumulative distance traveled between juvenile and adult female seals (MRPP: A = 0.04, p = 0.07).
The percentage of tagged seals inhabiting Glacier Bay decreased substantially in mid- to late September in 2007 (Figure 6a) and 2008 (Figures 6b). The median date of departure of seals from Glacier Bay was 25 September in 2007 (range: 15 Sept to 4 Nov 2007) and 19 September in 2008 (range: 14 Sept to 19 Oct 2008). Tagged seals were largely absent from Johns Hopkins Inlet for extended periods ranging from 27 October 2007 to 22 April 2008 (173 days or ∼5.7 months) and from 6 November 2008 to 2 February 2009 (88 days or ∼3 months). The percentage of tagged seals in Glacier Bay began to increase starting in late April and early-May in 2008 (Figure 6a) and in mid-May in 2009 (Figure 6b).
The percentage of tagged harbor seals in the marine protected area (MPA) of Glacier Bay decreased in mid- to late September in 2007 (A) and in 2008 (B). The percentage of tagged harbor seals in Glacier Bay began to increase starting in late April and early-May in 2008 (A) and in mid-May in 2009 (B).
Collectively, the utilization distribution of seals was most expansive in September and October (25,325 km2), November and December (22,025 km2), and January and February (20,300 km2) (Table 1) demonstrating that some seals ranged extensively from the breeding area in Johns Hopkins Inlet to areas far outside the MPA of Glacier Bay during the post-breeding season (Figures 2, 3, 4). Although the utilization distribution of seals from September through February collectively encompassed an extensive area ranging from northern Southeast Alaska through the eastern Gulf of Alaska and up to Prince William Sound, high-intensity use areas were consistently concentrated in a region spanning from mid-Glacier Bay (inside the MPA) into the adjacent region of Icy Strait (outside of MPA) (Figures 2, 3, 4). A sizeable fraction of the areas most heavily used by seals (the 10% utilization distributions) occurred inside the MPA of Glacier Bay from September through April (Table 1). High-intensity use areas that occurred outside of Glacier Bay were found in Icy Strait, Cross Sound, Lynn Canal, and near Dry Bay along the Yakutat Forelands (Figures 2, 3, 4, 5).
In contrast, during the breeding season (May-June) the size of the area used by seals (8,125 km2) was substantially reduced and was concentrated primarily in the MPA of Glacier Bay (Figure 7), specifically in Johns Hopkins Inlet. Areas that were used by seals during the breeding season that were outside of Glacier Bay included Disenchantment Bay, a known glacial ice harbor seal pupping site near Yakutat, as well as areas in Icy Strait-Cross Sound, Dry Bay, Lynn Canal, and Taku Inlet (Figure 7).
Individual Residency Periods of Harbor Seals in Glacier Bay
Although the collective utilization distribution of harbor seals during the post-breeding season was quite expansive, there was a substantial degree of individual variability in the residency patterns or percentage of days that seals spent in the MPA of Glacier Bay. Some seals were more resident to Glacier Bay spending the majority of the post-breeding season inside the MPA whereas other seals were more migratory (Figure 8). Two seals, both juvenile females, spent 100% of time in Glacier Bay and several seals (6 juveniles and 1 adult) spent ≥75% of time in Glacier Bay. Juvenile female seals spent on average 43% (±36% SD) of days in Glacier Bay during the non-breeding season, significantly more than adults (19.8% ±36% SD) (MRPP: A = 0.13, p = 0.005) (Figure 8).
There was a substantial degree of individual variability in the percentage of days that harbor seals spent in the MPA of Glacier Bay. Some harbor seals were more resident to Glacier Bay spending the majority of the post-breeding season inside the MPA whereas other seals were more non-resident spending extended periods of time outside of Glacier Bay.
There were several seals that exhibited more non-resident behavior and traveled extensively to regions outside of Glacier Bay. Eleven seals spent greater than 90% of days, and 16 seals spent greater than 75% of days outside the MPA of Glacier Bay. Seals that exhibited more non-resident behavior spent extended periods of time in Icy Strait-Cross Sound (4 adults), Lynn Canal (3 juveniles), and the eastern Gulf of Alaska (2 juveniles, 2 adults). In general, once seals arrived at a post-breeding area, they remained primarily in the same region for the majority of the post-breeding period.
Of particular interest were four seals that spent >70% of their time in the eastern Gulf of Alaska along the continental shelf between an area just north of Sitka Sound to Prince William Sound. In the eastern Gulf of Alaska, seals were focused in nearshore areas as well as near the margin of the continental shelf in more pelagic habitat. One adult female seal (PV08GB21) spent >200 days in the eastern Gulf of Alaska region. From September till February, she made several extended forays up to 23 days in length to a pelagic region near the continental shelf margin, approximately 95 km from shore. From late February through mid-May, PV08GB21 transitioned to nearshore areas and exhibited a high degree of fidelity to the Alsek and Dangerous rivers where eulachon (Thaleichthys pacificus), an energy-rich forage fish, aggregates for spawning (Figure 9). Similarly, seal# PV08GB22, also an adult female, spent >130 days in the eastern Gulf of Alaska and made repeated visits to the Fairweather Grounds (∼170 kilometers southwest of Yakutat) near the continental shelf margin. PV08GB22 also traveled along the continental shelf to the Copper River Delta and Cape St. Elias just east of Prince William Sound.
Seal #PV08GB21 spent >200 days in the eastern Gulf of Alaska region and exhibited a high degree of fidelity to a region approximately 95 km from shore on the continental shelf from September 2008 to February 2009. Beginning in late February, PV08GB21 transitioned to a nearshore area at the Alsek River where eulachon (Thaleichthys pacificus) aggregate for spawning. Seal #PV08GB21 was tagged in Johns Hopkins Inlet in September of 2008.
Site Fidelity of Harbor Seals to Glacier Bay
Despite extensive migration and movements of seals away from the MPA of Glacier Bay during the post-breeding season, there was a high degree of inter-annual site fidelity (return rate) of seals to Glacier Bay the following pupping/breeding season (defined as May 1st). For seals with tags that transmitted through May 1st of the year after capture (27 of 37 or 73%), 93% (16 of 18 juveniles; 9 of 9 adults) returned to Glacier Bay and 78% returned to Johns Hopkins Inlet (14 of 18 juveniles; 7 of 9 adults) (Table 2). For those instruments that stopped transmitting before May1st, 80% (8 of 10) were last located in Glacier Bay National Park; however, it is unknown if the instruments stopped transmitting due to instrument failure, instrument loss, or seal mortality.
Relative to most other MPAs, the size of the MPA of Glacier Bay is extensive (2,400 km2) and seals generally stayed within the protected area during the breeding season. In contrast, during the post-breeding season harbor seals traveled extensively beyond the boundaries of the Glacier Bay encompassing an area of approximately 25,325 km2. Some harbor seals undertook relatively extensive migratory movements ranging up to 900 km away (one-way distance) to areas in Prince William Sound in south-central Alaska and a few seals traveled cumulative distances exceeding 3,000 km during the post-breeding season. Such extensive post-breeding season migrations and extended use of pelagic areas has not been previously reported for harbor seals from glacial fjords in Alaska or elsewhere and is in contrast to movement patterns of seals reported from most terrestrial breeding areas –.
Although seals ranged extensively beyond the MPA during the post-breeding season there was a high degree of inter-annual fidelity (93%) back to Glacier Bay the following breeding season (May-June). Such a high degree of site fidelity is consistent with genetic studies that suggest that philopatry occurs at smaller scales in harbor seals , . The high degree of site fidelity of harbor seals to Glacier Bay during the breeding season also supports the recent designation of harbor seals in the Glacier Bay and Icy Strait region as one of twelve stocks of harbor seals in Alaska . Fidelity to breeding sites or philopatry is not uncommon in pinnipeds – or harbor seals , – and may confer benefits such as familiarity with local conditions or reduced risk of predation. However, such a high degree of breeding site fidelity may also come at a cost as threats that seals may encounter during the post-breeding season may influence the population dynamics of seals in Glacier Bay.
Most harbor seals traveled extensively; however, there was a substantial degree of individual variability in residency patterns of seals in Glacier Bay. Some seals spent greater than 90% of the post-breeding period outside of the MPA of Glacier Bay whereas other seals remained in Glacier Bay for the entire post-breeding season. Although the relatively high degree of intra-population variation suggests that individual seals may employ different strategies, it is unknown if differences in behavioral strategies of seals may confer fitness advantages. However, populations that exhibit variability in migratory and residency patterns can create challenges for identifying and managing for different behavioral ecotypes –. Ultimately it will be important to ensure that both migratory and resident behaviors are accounted for in the context of designing and monitoring the effectiveness of MPAs.
Although harbor seals are primarily thought to forage in more nearshore shallow coastal areas, some seals exhibited fidelity to more offshore regions. Use of more offshore and pelagic regions near the continental shelf edge suggests that these habitats may be of substantial ecological significance to harbor seals as foraging areas (Figure 9). The presumed foraging trips (n = 5) by seal# PV08GB21 to the pelagic region near the continental shelf-edge were on average 14.4 days in length and ranged up to 23 days. Such persistent use of focal regions by seals and other highly mobile taxa can present opportunities for conservation of important habitats ; however, spatial protections are currently limited for pelagic regions and dynamic oceanographic features that are used by highly mobile marine species –.
Our study focused only on the post-breeding season migrations of juvenile and adult female harbor seals as females are particularly important in terms of population productivity. However, previous studies have demonstrated that the behavior of male harbor seals may differ from that of females. For example, female harbor seals captured in Prince William Sound, Alaska, typically had larger home ranges than males from September to March . In contrast, during the breeding season, male harbor seals typically traveled greater distances than females in the Pacific Northwest and Scotland , . Collectively, these studies demonstrate that sex-specific differences occur and emphasize the importance of understanding and accounting for such differences to ensure effective conservation strategies .
The extensive post-breeding season distribution of seals coupled with the high degree of breeding site fidelity to Glacier Bay suggests that a more thorough understanding of the distribution of seals that comprise this stock relative to human-related threats may provide a better understanding of potential factors that may be driving population trajectories in Glacier Bay. However, spatially explicit data regarding human-related threats and the extent to which seals from Glacier Bay interact with these threats are generally lacking.
Commercial and subsistence gillnet fisheries for salmon (Oncorhynchus spp.) occur in several areas in southeastern Alaska, including Yakutat Bay, along the coast of the Yakutat Forelands in the eastern Gulf of Alaska, Lynn Canal, and in the Taku Inlet-Stephens Passage area. Many of these areas are also used by harbor seals from Glacier Bay during the post-breeding season; however, the extent to which harbor seals interact with gillnet fisheries in southeastern Alaska is largely unknown. Evidence from other regions of Alaska and from studies elsewhere suggests that gillnet fisheries and their potential impact on pinnipeds may be significant , . An estimated 20,867 pinnipeds were caught as bycatch in commercial fisheries in the Pacific Ocean from 1990–1999 and approximately 98% of bycatch of pinnipeds occurred in gillnet fisheries . Similarly, studies in Norway documented substantial interaction between bottom-set gillnets and young-of-year harbor seals , . Although there has been limited observer effort associated with marine mammal and gillnet fishery interactions in southeastern Alaska, interactions have been observed in other regions of Alaska , , suggesting that such interactions may warrant further attention.
Another potential source of mortality is associated with the subsistence harvest of harbor seals by Alaska Natives which is authorized under the Marine Mammal Protection Act. Although subsistence harvest of harbor seals has not been permitted in Glacier Bay National Park since 1974 , the extensive post-breeding season distribution of seals from Glacier Bay may expose seals to subsistence harvest outside of the park. Harbor seals are an important cultural and subsistence resource for Alaska Natives, particularly in southeastern Alaska, and harvest has taken place for many generations . Harvested seals are used for meat, oil, skins, and handicrafts as well as for an important item for trading and cultural exchange –. Subsistence surveys and anthropological studies demonstrate that harbor seals may be harvested during all months; however, there are typically two distinct seasonal peaks for harvest of seals which occur during spring and in autumn/early winter , . These time periods co-occur with the time period during which seals travel beyond the boundaries of Glacier Bay; however, it is currently unknown whether or not either of these potential threats may have population-level effects on harbor seals in Glacier Bay.
This study advances our understanding of the distribution of a pinniped of conservation concern, the harbor seal, relative to boundaries of one of the largest MPAs in the northern hemisphere. Our results have several implications not only for the conservation of harbor seals in Glacier Bay and other glacial fjord habitats in Alaska but also for evaluating and improving the design of MPAs for other wide-ranging species, such as seabirds, cetaceans, and other pinniped species. First, MPAs are often created in the absence of spatially explicit data for species throughout the annual cycle. The use of discrete areas for breeding and non-breeding activities by highly mobile pelagic taxa highlights the challenges and complexities associated with designing protected areas for species that may inhabit dramatically different regions over the course of the annual cycle , , . Second, individuals may exhibit a high degree of variability in residency patterns, movements, and migratory behavior thus creating challenges for identifying and managing for different behavioral ecotypes –. Finally, the high-degree of fidelity to breeding areas highlights the importance of understanding the spatial distribution of species of conservation concern throughout the annual cycle as threats encountered during the post-breeding season may influence population dynamics.
Similar to other large marine vertebrates, harbor seals are long-loved and relatively late-reproducing species and these life history characteristics make them particularly sensitive to late-stage or adult mortality . Although the MPA of Glacier Bay provides special protection measures for harbor seals during the breeding season, harbor seals have not recovered. Thus, before firm conclusions regarding the effectiveness of the MPA for harbor seals can be made, it will be important to identify the extent to which harbor seals from the Glacier Bay/Icy Strait stock interact with potential threats and how such threats may or may not impact the population dynamics of harbor seals in Glacier Bay. Similarly, quantifying survival and reproductive rates of seals along with identifying the sources of age-specific mortality  for harbor seals both inside and outside of the MPA would also be beneficial.
Our study highlights the challenges associated with managing for highly mobile species that travel in and out of protected areas; however, there are approaches that could be taken to facilitate increased protection for these species. First, a more mechanistic understanding of the relationship between habitat features, prey availability, and the seasonal distribution of highly mobile species is critical and would allow for a predictive approach that could be used to identify features or areas (e.g., seamounts, canyons, eddies, and fish aggregations) where highly mobile species may aggregate. Second, a predictive model of species occurrence relative to habitat features could be coupled with data regarding known and potential threats to predict areas of likely interaction , . Coupling these two approaches would provide a mechanistic basis for implementing dynamic time-area closures that could reduce the likelihood of interaction between highly mobile species and potential threats , , . Finally, increasing the size of MPAs may not necessarily result in complete protection for highly mobile species and also may not be a feasible alternative for a variety of reasons. However, a network of protected areas that collectively encompasses important breeding, feeding, and migratory areas could be a more viable approach that could result in increased protection of highly mobile species throughout much of the annual cycle , .
Studies of this nature showcase the utility of coupling satellite telemetry and geographic information systems as effective tools for identifying the spatial and temporal distribution of species of conservation concern relative to protected area boundaries , , , , , which is an important first step in marine spatial planning. Information regarding where species go and the habitats they use is essential for designing protected areas, evaluating the effectiveness of those protected areas, and ultimately for working with stakeholders across jurisdictional boundaries in an attempt to reduce or ameliorate potential anthropogenic threats for species of conservation concern.
Numerous individuals provided essential field and logistical assistance including G. Blundell, N. Bool, S. Conlon, R. Dziuba, J. Herreman, D. Holcombe, J. Jansen, S. Karpovich, J. King, N. Lazzaretti, T. Ose, L. Polasek, J. Prewitt, C. Schmale, and J. Wells. The captain (D. Foley) and the crew of the R/V Steller provided exceptional field support. We thank J. London for advice regarding tag programming, D. Gregovich for assistance with programming, D. Douglas for guidance with Service Argos and data filtering, and S. Maxwell for sharing scripts. The manuscript benefitted greatly from constructive feedback provided by L. Ciannelli, C. Epps, M. Horning, K. White, D. Wright, and three anonymous reviewers.
Conceived and designed the experiments: JNW SMG. Performed the experiments: JNW SMG. Analyzed the data: JNW. Contributed reagents/materials/analysis tools: JNW SMG. Wrote the paper: JNW SMG.
- 1. Gerber LR, Botsford LW, Hastings A, Possingham HP, Gaines SD, et al. (2003) Population models for marine reserve design: a retrospective and prospective synthesis. Ecol Appl 13: S47–S64.
- 2. Lubchenco J, Palumbi SR GainesSR, Andelman SR (2003) Plugging a hole in the ocean: the merging science of marine reserves. Ecol Appl 13: 3–7.
- 3. Leslie HM (2005) A synthesis of marine conservation planning approaches. Conserv Biol 19: 1701–1713.
- 4. Hooker SK, Whitehead H, Gowans S (1999) Marine protected area design and the spatial and temporal distribution of cetaceans in a submarine canyon. Conserv Biol 13: 592–602.
- 5. Hooker SK, Whitehead H, Gowans S (2002) Ecosystem consideration in conservation planning: energy demand of foraging bottlenose whales (Hyperoodon ampullatus) in a marine protected area. Biol Conserv 104: 51–58.
- 6. Hooker SK, Gerber LR (2004) Marine reserves as a tool for ecosystem-based management: the potential importance of megafauna. BioScience 54: 27–39.
- 7. Notarbartolo-Di-Sciara G, Agardy T, Hyrenbach D, Scovazzi T, Van Klavern P (2008) The Pelagos Sanctuary for Mediterranean marine mammals. Aquat Conserv 18: 367–391.
- 8. Gormely AM, Slooten E, Dawson S, Barker RJ, Rayment W, et al. (2012) First evidence that marine protected areas can work for marine mammals. J Appl Ecol 49: 474–480.
- 9. Hoyt E (2011) Marine protected areas for whales, dolphins, and porpoises: a world handbook for cetacean habitat conservation and planning. New York: Earthscan. 464 p.
- 10. Ballard G, Jongsomjit G, Veloz SD, Ainley DG (2012) Coexistence of mesopredators in an intact polar ocean ecosystem: the basis for defining a Ross Sea marine protected area. Biol Conserv 156: 72–82.
- 11. Sala E, Aburto-Oropeza O, Paredes G, Parra I, Barrera JC, et al. (2002) A general model for designing networks of marine reserves. Science 298: 1991–1993.
- 12. Roberts CM, Branch G, Bustamante RH, Castilla JC, Dugan J, et al. (2003) Application of ecological criteria in selecting marine reserves and developing reserve networks. Ecol Appl 13: S215–S228.
- 13. Rojas-Bracho L, Taylor BL (1999) Risk factors affecting the vaquita (Phocoena sinus). Mar Mamm Sci 15: 974–989.
- 14. Gerrodette T, Rojas-Bracho L (2011) Estimating the success of protected areas for the vaquita, Phocoena sinus. Mar Mamm Sci 27: E101–E125.
- 15. Gerber LR, Estes J, Crawford TG, Peavey LE, Read AJ (2011) Managing for extinction? Conflicting conservation objectives in a large marine reserve. Conserv Lett 4: 417–422.
- 16. Shillinger GL, Palacios DM, Bailey H, Bograd SJ, Swithenbank AM, et al. (2008) Persistent leatherback turtle migrations present opportunities for conservation. PLoS Biol 6(7): e171 .
- 17. Peckham SH, Diaz DM, Walli A, Ruiz G, Crowder LB, et al. (2007) Small-scale fisheries bycatch jeopardizes endangered pacific loggerhead turtles. PLoS ONE 2(10): e1041 .
- 18. Botsford LW, Micheli F, Hastings A (2003) Principles for the design of marine reserves. Ecol Appl 13: S25–S31.
- 19. Martin TG, Chadès I, Arcese P, Marra PP, Possingham HP, et al. (2007) Optimal conservation of migratory species. PLoS ONE 2(8): e751 .
- 20. National Research Council (2001) Marine protected areas: Tools for sustaining ocean ecosystems. Washington, DC: National Academy Press. 288 p.
- 21. Jansen JK, Boveng PL, Dahle SP, Bengtson JL (2010) Reaction of harbor seals to cruise ships. J Wildl Manage 74: 1186–1194.
- 22. Catton T (1995) Land Reborn Land reborn a history of administration and visitor use in Glacier Bay National Park and Preserve. Anchorage: National Park Service, United States Department of the Interior. 398 p.
- 23. Mackovjack J (2010) Navigating troubled waters: A history of Commercial Fishing in Glacier Bay, Alaska. Harpers Ferry: National Park Service, United States Department of the Interior. 258 p.
- 24. Hendrix AN, Straley JM, Gabriele CM, Gende SM (2012) Bayesian estimation of humpback whale (Megaptera novaeangliae) population abundance and movement patterns in southeast Alaska. Can J Fish Aquat Sci 69: 1783–1797.
- 25. Mathews EA, Womble JN, Pendleton GW, Jemison LA, Maniscalco JM, et al. (2011) Population expansion and colonization of Steller sea lions in the Glacier Bay region of southeastern Alaska: 1970s to 2009. Mar Mamm Sci 27: 852–880.
- 26. Womble JN, Sigler MF, Willson MF (2009) Linking seasonal distributions with prey availability in a central-place forager, the Steller sea lion. J Biogeogr 36: 439–451.
- 27. Kenyon KW (1969) The sea otter in the eastern Pacific Ocean. North America Fauna, No. 68. United States Fish and Wildlife Service. 352 p.
- 28. Bodkin JL, Ballachey BE, Esslinger GG, Kloecker KA, Monson DH, et al. (2007) Perspectives on an invading predator–Sea otters in Glacier Bay. In: Reston: U.S.Geological Survey Scientific Investigations Report Piatt JF, Gende SM, editors. Proceedings of the Fourth Glacier Bay Science Symposium. 2007–5047: 133–136.
- 29. Mathews EA, Pendleton GW (2006) Declines in harbor seal (Phoca vitulina) numbers in Glacier Bay National Park, Alaska, 1992–2002. Mar Mamm Sci 22: 170–191.
- 30. Womble JN, Pendleton GW, Mathews EA, Blundell GM, Bool NM, et al. (2010) Harbor seal decline continues in the rapidly changing landscape of Glacier Bay National Park, Alaska, 1992–2008. Mar Mamm Sci 26: 686–697.
- 31. Small RJ, Pendleton GW, Pitcher KW (2003) Trends in the abundance of Alaska harbor seals, 1983–2002. Mar Mamm Sci 19: 344–362.
- 32. Blundell GM, Womble JN, Pendleton GW, Karpovich SW, Gende SM, et al. (2011) Use of glacial ice and terrestrial habitats by harbor seals in Glacier Bay, Alaska: costs and benefits. Mar Ecol Prog Ser 429: 277–290.
- 33. Hueffer K, Holcomb D, Ballweber LR, Gende S, Blundell GM, et al. (2011) Serological surveillance of multiple pathogens in a declining harbor seal population in Glacier Bay National Park and a reference site. J Wildl Dis 47: 984–988.
- 34. Young C (2009) Master’s Thesis: Disturbance of harbor seals by vessels in Johns Hopkins Inlet in Glacier Bay National Park, Alaska. [M.S.] Moss Landing Marine Laboratory, California; San Jose State University. 112 p.
- 35. Mathews EA, Kelly BP (1996) Extreme temporal variation in harbor seal (Phoca vitulina richardsi) numbers in Glacier Bay, a glacial fjord in Southeast Alaska. Mar Mamm Sci 12: 483–488.
- 36. Etherington LL, Hooge PN, Hooge ER, Hill DF (2007) Oceanography of Glacier Bay, Alaska: Implications for biological patterns in a glacial fjord estuary. Estuaries Coast 30: 927–944.
- 37. Hill DF, Ciavola S, Etherington L, Klaar M (2009) Estimation of freshwater runoff into Glacier Bay, Alaska and incorporation into a tidal circulation model. Estuar Coast Shelf Sci 82: 95–107.
- 38. Cooper WS (1937) The problem of Glacier Bay, Alaska: a study of glacier variations. Geogr Rev 27: 37–62.
- 39. Field WO (1947) Glacier recession in Muir Inlet, Glacier Bay, Alaska. Geogr Rev 37: 369–399.
- 40. Hall DK, Benson CS, Field WO (1995) Changes of Glaciers in Glacier Bay, Alaska using ground and satellite measurements. Physical Geogr 16: 27–41.
- 41. Robards MD, Drew GS, Piatt JF, Anson JM, Abookire AA, et al.. (2003) Ecology of selected marine communities in Glacier Bay: zooplankton, forage fish, seabirds and marine mammals. Anchorage: United States Geological Survey-Alaska Science Center, Department of the Interior. 156 p.
- 42. Arimitsu ML, Piatt JF, Litzow MA, Abookire AA, Romano MD, et al. (2008) Distribution and spawning dynamics of capelin (Mallotus villosus) in Glacier Bay, Alaska: a cold water refugium. Fish Oceanogr 17: 137–146.
- 43. Calambokidis JB, Taylor BL, Carter SD, Steiger GH, Dawson PK, et al. (1987) Distribution and haul-out behavior of harbor seals in Glacier Bay, Alaska. Can J Zool 65: 1391–1396.
- 44. Blundell GM, Pendleton GW (2008) Estimating age of harbor seals (Phoca vitulina) with incisor teeth and morphometrics. Mar Mamm Sci 24: 577–590.
- 45. Daniel RG, Jemison LA, Pendleton GW, Crowley SM (2003) Molting phenology of harbor seals on Tugidak Island, Alaska. Mar Mamm Sci 19: 128–140.
- 46. Douglas DC, Weinzierl R, Davidson SC, Kays R, Wikelski M, et al. (2012) Moderating Argos location errors in animal tracking data. Methods Ecol Evol 3: 999–1007.
- 47. Johnson DS, London JM, Lea M-A, Durban JW (2008) Continuous-time correlated random walk model for animal telemetry data. Ecol 89: 1208–1215.
- 48. Worton BJ (1989) Kernel methods for estimating the utilization distribution in home-range studies. Ecol 70: 164–168.
- 49. Kie JG, Matthiopolous J, Fieberg J, Powell RA, Cagnacci C, et al. (2010) The home-range concept: are traditional estimators still relevant with modern telemetry technology? Philos Trans R Soc Lond B Biol Sci 365: 2221–2231.
- 50. Kernohan B, Gitzen RA, Millspaugh J (2001) Analysis of Animal Space Use and Movements. In: Millspaugh J, Marzluff J, editors. Radio Tracking and Animal Populations. San Diego: Academic Press. 126–168.
- 51. Getz WM, Wilmers CC (2004) A local nearest-neighbor convex hull construction of home ranges and utilization distributions. Ecography 27: 489–505.
- 52. Maxwell SM, Breed GA, Nickel BA, Makanga-Bahouna J, Pemo-Makaya E, et al. (2011) Using satellite tracking to optimize protection of long-lived marine species: olive Ridley sea turtle conservation in Central Africa. PLoS ONE 6(5): e19905 .
- 53. Kenow KP, Meyer MW, Evers DC, Douglas DC, Hines JE (2002) Use of satellite telemetry to identify Common Loon migration routes, staging areas and wintering range. Waterbirds 25: 449–458.
- 54. Mielke PW, Berry KJ, Johnson ES (1976) Multiresponse permutation procedures for a priori classifications. Communications in Statistics A5: 1409–1424.
- 55. Mielke PW, Berry KJ (2001) Permutation methods: A distance function approach. Springer Series in Statistics. New York: Springer. 439 p.
- 56. McCune B, Mefford MJ (2006) PC-ORD Multivariate Analysis of Ecological Data Version 5.10. Gleneden Beach: MjM Software.
- 57. Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69: 57–68.
- 58. Lowry LF, Frost KJ, VerHoef J, DeLong RA (2001) Movements of satellite tagged subadult and adult harbor seals in Prince William Sound, Alaska. Mar Mamm Sci 17: 835–861.
- 59. Small RJ, Lowry LF, VerHoef JM, Frost KJ, DeLong RA, et al. (2005) Differential movements by harbor seal pups in contrasting Alaska environments. Mar Mamm Sci 21: 671–694.
- 60. Peterson SH, Lance MM, Jefferies SJ (2012) Acevedo-Gutiérrez (2012) Long distance movements and disjunct spatial use of harbor seal (Phoca vitulina) in the inland waters of the Pacific Northwest. PloS ONE 7 (6): e39046 .
- 61. Sharples RJ, Moss SE, Patterson TA, Hammond PS (2012) Spatial variation in foraging behaviour of a marine top predator (Phoca vitulina) determined by a large-scale satellite tagging program. PLoS ONE 7(5): e37216 .
- 62. Goodman SJ (1998) Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol Biol Evol 15: 104–118.
- 63. Westlake RL (2002) O’Corry-Crowe (2002) Macrogeographic structure and patterns of genetic diversity in harbor seals (Phoca vitulina) from Alaska to Japan. J Mammal 83: 1111–1126.
- 64. Allen BM, Angliss RP (2012) Alaska marine mammal stock assessments, 2011. United States Department of Commerce, NOAA Tech. Memo. NMFS AFSC-234. 288 p.
- 65. Lunn NJ, Boyd IJ (1991) Pupping-site fidelity of Antarctic fur seals at Bird Island, South Georgia. J Mammal 72: 202–206.
- 66. Pomeroy PP, Twiss SD, Redman P (2000) Philopatry, site fidelity and local kin associations within grey seal breeding colonies. Ethology 106: 899–919.
- 67. Campbell RA, Gales NJ, Lento GM, Baker CS (2008) Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea. Biol Lett 2008 4: 139–142.
- 68. Yochem PK, Stewart BS, DeLong RL, DeMaster DP (1987) Diel haul-out patters and site fidelity of harbor seals (Phoca vitulina richardsi) on San Miguel Island, California, in autumn. Mar Mamm Sci 3: 323–332.
- 69. Thompson PM (1989) Seasonal changes in the distribution and composition of common seal (Phoca vitulina) haul-out groups. J Zool 217: 281–294.
- 70. Härkönen T, Harding KC (2001) Spatial structure of harbour seal populations and the implications therof. Can J Zool 79: 2115–2127.
- 71. Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, et al. (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161: 1–28.
- 72. Lowther AD, Harcourt RG, Hamer DJ, Goldsworthy SJ (2011) Creatures of habit: foraging habitat fidelity of adult female Australian sea lions. Mar Ecol Prog Ser 443: 249–263.
- 73. Hyrenbach KD, Forney KA, Dayton PK (2000) Marine protected areas and ocean basin management. Aquat Conserv 10: 437–458.
- 74. Game ET, Grantham HS, Hobday AJ, Pressey RL, Lombard AT, et al. (2009) Pelagic protected areas: the missing dimension in ocean conservation. Trends Ecol Evol 24: 360–369.
- 75. Hooker SK, Cańada A, Hyrenbach KD, Corrigan D, Polovina JJ, et al. (2011) Making protected area networks effective for marine top predators. Endanger Species Res 13: 203–218.
- 76. Thompson PM, Mackay A, Tollit DJ, Enderby S, Hammond PS (1998) The influence of body size and sex on the characteristics of harbour seal foraging trips. Can J Zool 76: 1044–1053.
- 77. Read AJ, Drinker P, Northridge S (2006) Bycatch of marine mammals in U.S. and global fisheries. Conserv Biol 20: 163–169.
- 78. Hamer DJ, Ward TM, Shaughnessy PM, Clark SR (2011) Assessing the effectiveness of the Great Australian Bight Marine Park in protecting the endangered Australian sea lion Neophoca cinera from bycatch mortality in shark gillnets. Endanger Species Res 14: 203–216.
- 79. Bjørge A, Bekkby T, Bakkestuen V, Framstad E (2002a) Interactions between harbour seals, Phoca vitulina, and fisheries in complex coastal waters explored by combined Geographic Information System (GIS) and energetics modeling. ICES J Mar Sci 59: 29–42.
- 80. Bjørge A, Ønien N, Hartvedt S, Bøthun G, Bekkby T (2002b) Dispersal and bycatch mortality in gray, Halichoerus grypus, and harbor seals, Phoca vitulina, seals tagged at the Norwegian coast. Mar Mamm Sci 18: 963–976.
- 81. Barlow J, Baird RW, Heyning J, Wynne K, Manville MF, et al. (1994) A review of cetacean and pinniped mortality in coastal fisheries along the West coast of the USA and Canada and the East Coast of the Russian Federation. Report of the International Whaling Commission 15: 405–426.
- 82. Matkin CO, Fay FH (1980) Marine mammal fishery interactions on the Copper River and in Prince William Sound, Alaska 1978. United States Marine Mammal Commission Report No. MMX-78107.
- 83. Emmons GT (1991) The Tlingit Indians. Edited with additions by de Laguna F. Seattle: University of Washington Press. 530 p.
- 84. de Laguna F (1972) Under Mount St. Elias: The history and culture of the Yakutat Tlingit. Smithsonian Contributions to Anthropology 7. Washington, D.C.: Smithsonian Institution Press. 3 vols. 1, 395 p.
- 85. Wolfe RJ, Fall JA, Reidel M (2009) The subsistence harvest of harbor seal and sea lions by Alaska natives in 2008. Alaska Native Harbor Seal Commission and Alaska Department of Fish & Game Subsistence Technical Paper No. 339. 91 p.
- 86. Yorio P (2009) Marine protected areas, spatial scales, and governance: implications for the conservation of breeding seabirds. Conserv Lett 2: 171–178.
- 87. Gerber LR, Heppell SS (2004) The use of demographic sensitivity analysis in marine species conservation planning. Biol Conserv 120: 121–128.
- 88. Horning M, Mellish J-AE (2012) Predation on an upper-trophic level marine predator, the Steller sea lion: evaluating high juvenile mortality in a density dependent conceptual framework. PLoS ONE 7(1): e30173 .
- 89. Howell EA, Kobayashi DR, Parker DM, Balazs GH, Polovina JJ (2008) TurtleWatch: a tool to aid in the bycatch reduction of loggerhead turtles Caretta caretta in the Hawaii-based pelagic longline fishery. Endanger Species Res 5: 267–278.
- 90. Zydelis R, Lewison RL, Shaffer SA, Moore JE, Boustany AM, et al. (2011) Dynamic habitat models: using telemetry data to project fisheries bycatch. Proc Biol Sci 278: 3191–3200.
- 91. Hyrenbach KD, Keiper C, Allen SG, Anderson DJ, Ainley DG (2006) Use of national marine sanctuaries by far-ranging predators: commuting flights to the California Current System by breeding Hawaiian albatrosses. Fish Oceanogr 15: 95–103.