Seasonal Variation in Seal Counts
The abundance of hauled-out harbor seals in Alaska is thought to peak both during pup-rearing and molting, with molting counts usually being higher and thought to have a broader mix of age and sex classes (Calambokidis et al. 1987, Frost et al. 1999, Jemison and Kelly 2001, Boveng et al. 2003, Ver Hoef and Frost 2003, Jemison et al. 2006). In contrast, our estimates of abundance showed near peak levels prior to pupping, a sharp decline at the onset of pupping, and then a more gradual increase to a peak during molting. The cause of the decline in seal counts in DB just before pupping is unknown. Wind speed and precipitation, particularly on survey days, were below the levels observed in other studies where there was a reduction in the number of seals hauled out (Hoover 1983, Boveng et al. 2003). Despite seasonal variation in ice cover, there were no marked changes early in the season to explain the decline of seals, and overall ice cover did not seemingly limit use of the area. In Glacier Bay, declining use of ice habitat by seals was attributed to the declining ice cover in the years just prior to the retreating Muir Glacier's eventual grounding (Calambokidis et al. 1987). In contrast, Hubbard Glacier–which calves the vast majority of ice in Disenchantment Bay–is advancing, contrary to all but a few Alaskan tidewater glaciers (51 total) (Molnia 2007, Motyka and Truffer 2007, Krimmel 2008, Post et al. 2011). Floating ice cover is linked to seasonality in glacial calving, which is a complex function of other seasonal factors, including the glacier's advance/retreat cycle and speed, sea-surface temperature, subglacial freshwater runoff, and ice melt (Ritchie et al. 2008). Interestingly, in our study, maximum ice cover was centered on the peak pupping period when mothers have been shown to be increasingly selective in finding suitable ice for birthing and nursing (Hoover 1983).
The sharp decline in seal counts also appears unrelated to cruise ships, a conclusion supported by our space-time models (see below). To our knowledge, the first cruise ship entered DB on 14 May, at the midpoint in the overall decline in seal abundance. Due to thick ice and fog, this ship stopped barely within the study area and before any seals were within spotting range (ca. 1 km). According to ship schedules, we believe the next ship entered DB on 18 May, after declining seal counts had stabilized. If the distribution of seals on 14 May was similar to that on adjacent dates when aerial surveys were conducted (13 and 16 May), the nearest seals to the ship (cell total > 1) would have been at a distance of more than 12 km. Only at distances less than 500 m to ships have harbor seals been shown to flush from the ice (Jansen et al. 2010). If the subsequent decline in seal numbers was a response to single vessel at 12 km, it would be difficult to reconcile the steady increase in seal counts later in the season when ship encounters also increased, in terms of ships per day (up to four), number of ship-days per week (up to five), and deeper penetration into the bay with diminishing ice cover.
Alternatively, seals could have left the bay (or spent more time in the water) in response to other factors not measured in this study, such as the abundance and distribution of prey. Diet studies of harbor seals near Yakutat Bay showed the dominant prey to be walleye pollock (Theragra chalcogramma) and a variety of smelt (Pitcher 1980). During peak smelt runs, harbor seals are commonly seen milling in river systems (Marston et al. 2002), including in the mouths of the Situk (70 km from DB), Lost (70 km) and Alsek Rivers (140 km).3 In these river systems near DB, transient smelt runs reportedly occur from March to mid-June (Estes 1994). Capitalizing on these ephemeral prey resources may be key in building fat reserves for periods of fasting associated with rearing young, breeding, and molting (Bowen et al. 1992, Womble et al. 2005, Willson and Womble 2006). During our study, on 14 May 2002, when seal numbers in DB were near minimum, spawning smelt were reported in the Situk Estuary, as indicated by large feeding flocks of seabirds.4 This elevated abundance of prey nearby may have been an incentive for harbor seals to leave DB. Grigg et al. (2009) posited that despite high fidelity by harbor seals for haul-outs within San Francisco Bay, seasonal movements to the outer coast occur more often during periods of upwelling there, and when there was lower prey availability inside the bay. It is also noteworthy that local maxima in seal counts that occurred around the first of each month (Fig. 4) correspond approximately to the fullest phase of the moon. Similar propensity of seals hauling out (and foraging less) around the full moon have been observed in other studies (Trillmich and Mohren 1981, Watts 1993, Cronin et al. 2009), and are thought to reflect reduced food availability (i.e., deeper prey) and thus less efficient foraging (Horning and Trillmich 1999, Lea et al. 2010).
The reduced abundance of seals in DB at the onset of pupping is similar to that of ice-associated harbor seals in Aialik Bay, Alaska. Hoover's (1983) first seasonal counts of Aialik seals in mid-May occurred at an apparent minimum in seal counts. Seal numbers then steadily increased until peak pupping in mid-June, but then, unlike at DB, counts declined and did not rebound until early August. Seal numbers at DB rebounded to maximum levels by the end of June. At Aialik, increasing abundance during pupping coincided with a pronounced decline in juveniles present, a seasonal pattern supported by earlier unpubished work on ice-associated harbor seals at DB.5 This exodus of juveniles at Aialik was offset by an influx of adults which caused a peak in abundance near the time of peak pupping. Though little is known of the factors that influence local abundance and composition of harbor seal populations during the breeding season, we believe that movement of juveniles–which are not constrained by breeding/whelping requirements, i.e., they are more transient, and can compose up to half of the population (Hoover 1983)—explain much of the rapid change in counts at DB. Other observations in glacial fjords point to an important role for social dynamics in this pattern, with breeding males supplanting juveniles in order to maintain underwater territories near nursing females (Hoover 1983). Harbor seals regularly show seasonal patterns in haul-out abundance and habitat use though often with unexplained anomalies (Brown and Mate 1983, Bayer 1985, Rosenfeld et al. 1988, Mathews and Kelly 1996, Harris et al. 2003, Grigg et al. 2012).
Comparison with Other Sites
The timing of pupping is comparable between DB and other glacial sites, peaking in June, but there are apparent differences in productivity. At peak pupping at DB, the proportion of pups relative to the total abundance was 10%, a figure less than half that observed at other glacial haul-outs (Icy Bay: 23%, Mathews 1995; Aialik Bay: 21%–34%, Hoover 1983, Hoover-Miller et al. 2011; John Hopkins Inlet and Muir Inlet: 34%–36%, Mathews and Pendleton 2006; 37%–40%, Calambokidis et al. 1987; and one terrestrial haul-out, Tugidak Island: 23%–27%, Jemison and Kelly 2001). Despite possible biases related to differences in the criteria for classifying mothers and pups, we believe these contrasting figures to be consistent and large enough to not likely be attributed to bias or sampling error. In all studies to date, proximity to the mother has been required for classifying a small seal as a pup. Because mothers are known to forage during lactation (Boness et al. 1994), unaccompanied pups get lumped with the nonpups, resulting in an overall underestimation of productivity.
Effect of Modeled Covariates
Ice cover was a key factor affecting abundance and distribution with seals tending to haul out in areas of intermediate rather than scattered or dense ice coverage. We believe this pattern results from seals selecting greater than some minimum density of ice to facilitate sociality and provide protection from predators such as killer whales (Orcinus orca); and to avoid the densest ice for ease in breathing and swimming at the surface, and spy-hopping to find aggregations of animals. Denser ice may also not represent optimal habitat because it tends to occur near the glaciers where waves from calving often crash over ice, sometimes causing them to overturn.
Our results suggest that areas close to ships were regularly occupied by seals. This appears to conflict with the finding that seals increasingly escape into the water when approached within 500 m by cruise ships (Jansen et al. 2010). Still, the majority of seals in our study (during a given ship visit) likely were not approached closer than 500 m and thus continued drifting on the ice. At the same time, ships favored traveling through areas with less ice, usually within leads near more consolidated ice. This created spatial overlap, with most seals tolerating passing ships and remaining on the ice. It is also worth noting that seals and ships were not mapped simultaneously and thus a temporal discordance could have confounded any avoidance of ship corridors by seals (see below). So, contrary to our expectations, seals did not appear to actively avoid areas where cruise ships traveled. Similarly, Grigg et al. (2012) found that harbor seals in San Francisco Bay, California, occurred most often in areas of high human activity. The authors suggested that prey availability was a greater constraint than the cost of tolerating disturbance. Harbor seals in Danish waters exhibited weaker and shorter-lived reactions to disturbance during the breeding season, a pattern also thought to reflect a cost trade-off (Andersen et al. 2012). For seals in DB, unless disturbed closely by ships causing them to flush, the advantages of resting and staying dry on a stable piece of ice in areas frequented by ships (particularly for nursing moms) may outweigh the costs of more time traveling in the water to remain in less disturbed areas.
Though we did not detect an overt avoidance of areas used by ships, it is important to note that spatial scales, and distance effects, are likely to be obscured in glacial fjords where currents, ice, and relative locations of seals on the ice are constantly shifting over time. Seals also relocate without being disturbed, in response to ice drifting into less desirable areas, breaking up, turning over, or dispersing. To effectively filter out this variability would require greater transect coverage within short time periods of cruise ship presence and absence, or studies involving tracking of individual seals' behavior in relation to ships. The necessarily coarse quality of our data over these large fjords reflects more medium-term spatial processes (e.g., seals aggregating and drifting on the ice) and less short-term (e.g., seals flushing into the water).
Hypothesized Mechanism of Long-term Disturbance
Recent findings from multi-year studies have documented shifts in habitat use by seals believed to be driven by human disturbance (Cordes et al. 2011, Skeate et al. 2012). Our findings suggest that seals do not abandon the DB haul-out area as an immediate response to the number, proximity, or visit duration of cruise ships, despite seals being regularly flushed into the water. In the absence of data on seal abundance and distribution prior to the 1980s, before cruise ships entered DB in appreciable numbers, our study cannot address directly the long-term effects of vessel disturbance. However, clues regarding possible long-term effects can be drawn from existing, comparative counts at a neighboring, undisturbed area. Monthly counts of total seal abundance (by high-altitude aerial photogrammetry) from Icy Bay, a similar fjord with floating glacial ice (115 km away by water; Fig. 1), revealed a steady increase in numbers from May (1,011) to August (5,435) in contrast to counts at DB which showed an increase from May (1,544) to June (2,149) but then a modest decline to August (1,778; Jansen et al. 2006). Differences in seasonal use of these areas could arise from natural factors such as prey or ice conditions. We expect the tidewater glaciers at the two sites to have similar seasonal cycles of advance (winter/spring) and retreat (summer/fall), as supported by the seasonality in ice calving (i.e., ice cover) documented in our study. The timing and magnitude of peak ice cover could be different, as the transition to retreat (and increase in calving) expected during late spring is influenced by the rates of warming in seawater and freshwater discharge which may vary between sites (Ritchie et al. 2008). Observations in Aialik Bay support some consistency in ice-cover seasonality, exhibiting a pattern similar to what we found for DB (Hoover 1983). Interestingly, on the scale of decades, predictions of ice availability at the two sites may indeed be different, as glaciers calving into Icy Bay are rapidly thinning and retreating, whereas Hubbard Glacier in DB is slowly advancing (Molnia 2008).
From a theoretical standpoint, contrasting habitat use by seals at neighboring sites with striking differences in vessel use, combined with low productivity at DB, point to possible mechanisms that may have, over decades, led to differences in habitat desirability for seals. We hypothesize that a significant factor was the rapid expansion of cruise ship visitation to DB since the 1980s, which could have initiated a spatial shift in use away from DB and toward less disturbed areas, such as Icy Bay. Our observations of the occurrence and behavior of cruise ships, especially in relation to ice, document distinct seasonal intrusions into the seals' habitat at DB that may have differentially affected age-sex classes: (1) in May and June, ships regularly traveled through areas in south and central DB where we observed up to two-thirds of the mother-pup pairs (potentially diminishing habitat for pregnant and postpartum females and pups); (2) at the same time, denser ice cover further north and closer to the glaciers precluded ships from approaching the densest seal aggregations (potentially leaving undisturbed habitat for nonbreeders); and (3) declining ice cover in DB later in the summer allowed cruise ships access to the northern part of the bay where seals were previously isolated (potentially diminishing habitat for molting seals). Habitat displacement or abandonment in the presence of disturbance has been shown for several species of pinnipeds and other marine mammals (Grigg et al. 2004, Kirkman 2010, Kirkman et al. 2013), with new habitats believed to be lower quality and cause demographic impacts (Gerrodette and Gilmartin 1990, Stevens and Boness 2003, Bejder et al. 2006, Cartwright et al. 2012). Human disturbance can cause relatively rapid abandonment of traditional habitat with recolonization (post disturbance) taking much longer (Bartholomew 1949, Gerrodette and Gilmartin 1990, Skeate et al. 2012). In our study, the nearest alternative haul-outs to DB of more than a few seals are the ice field of Icy Bay and sandbars in the estuaries of the Dangerous and Alsek Rivers (approximately 500–1,000 seals in August6), 100–140 km to the southeast. Except for these sites, the ca. 500 km of outer coast between Cape Suckling and Cape Spencer–with DB and Icy Bay in the center–is completely exposed with only a few tens of seals hauling out at a given time (based on August surveys; NMML, unpublished data).
Seasonal patterns of ice cover mediated ship access to DB and to particular haul-out areas within the bay. We posit that denser ice cover provided a buffer that minimized disturbance for some seals during pup rearing but not for the majority during molting. During pup rearing, mothers and pups were likely at greater risk to disturbance because they tended to occur in areas to the south where there was greater overlap with ships. We argue that greater spatial overlap with ships means a higher frequency of flushing and thus greater energetic costs (Jansen et al. 2010), which could influence seals' longer-term decisions to reduce their seasonal use of DB. Those subjected to habitat degradation via chronic disturbance may decide over years to move entirely to a different area. Because seals rely on fat reserves to more efficiently nurse pups and molt out of the water (Pitcher and Calkins 1979), uninterrupted periods on a dry, stable platform promote energy savings and enhance fecundity and survival (Feltz and Fay 1966, Ashwell-Erickson et al. 1986, Boily 1995). Though we hypothesize that ship traffic contributed to reduced productivity and seasonal use of DB, we cannot rule out seasonal availability of ice, prey, or other features as factors in seals' decisions about where to pup and molt.