DIVING BEHAVIOR OF THE PACIFIC HARBOR SEAL (PHOCA VITULINA RICHARDII) IN MONTEREY BAY, CALIFORNIA
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1 MARINE MAMMAL SCIENCE, 21(2): (April 2005) by the Society for Marine Mammalogy DIVING BEHAVIOR OF THE PACIFIC HARBOR SEAL (PHOCA VITULINA RICHARDII) IN MONTEREY BAY, CALIFORNIA TOMOHARU EGUCHI JAMES T. HARVEY Moss Landing Marine Laboratories, 8272 Moss Landing Road Moss Landing, California 95039, U.S.A. ABSTRACT Physical environment and physiological characteristics of marine mammals potentially affect the duration and depth of diving. Harkonen (19876) proposed a hypothesis that the harbor seal would gain maximum energy by foraging at intermediate depths. To investigate this hypothesis, we studied diving behavior of the Pacific harbor seal (Phoca vitulina richardii) during 1995 through 1997 in Monterey Bay, California. Dive depths (n = 13,063 dives) were recorded via timedepth recorders. Approximately 80% of recorded dives were classified as square dives (type I), which typically were associated with foraging in pinnipeds. Approximately 11% of dives were V dives (type 11; 1,402 dives), and the remainder (1,225 dives) were skewed dives (type I11 and IV). The deepest recorded dive was 481 m, while the greatest duration was min. Body mass explained the variability of durations of long dives for females (95th percentile; D9,,9= X (massg), r2 = 0.91, 95% CI for slope = [0.08, 0.281, n = 5) and for males (DgS,$ = X (mass$),r2=0.83,95% CIforslope=[0.12,0.24],n=ll). Thelargeproportionof variability in deep dives, however, was explained by body mass only for males (95th percentile; Z9,,8 = X (mass$), r2= 0.83, 95% CI for slope = [3.93, 8.171, n= 11) and not for females (Z9,,p = X (massg), r2=0.58, 95% CI forslope=[-l.7,7.9],~~=5,95% CIforslope= [-1.7,7.9]). Mediandepthsof presumed foraging dives of harbor seals in the Monterey Bay area were between 5 and 100 m, which were within the range ofthe previously reported depths for other areas (< 100 m). Our findings generally supported H2konen s hypothesis that harbor seals forage in the intermediate depth in their environment. Key words: harbor seal, Phoca uitulina richara ii, time-depth recorders, dive types, optimal foraging depth, body mass. Harkonen (1987~) hypothesized that the harbor seal (Phoca vitulina) would gain maximum energy by foraging at intermediate water depths. This hypothesis was based on three premises: (1) harbor seals feed on benthic prey items, (2) that efficiency of a harbor seal as a predator decreases at extremely shallow and deeper Present address: Protected Resources Division, Southwest Fisheries Science Center, NOAA Fisheries, 8604 La Jolla Shores Drive, La Jolla, California 92037, U.S.A.; tomo.eguchi@noaa.gov. 283
2 284 MARINE MAMMAL SCIENCE, VOL. 21, NO. 2, 2005 depths, and (3) available foraging locations are dependent on local bathymetric conditions (Harkonen 1987a). Studies of food habits indicated that harbor seals consumed seasonally abundant pelagic and benthic fishes and mollusks (Harkonen 19876, Harvey et al. 1995, Brown and Pierce 1998, Tollit et al. 1998). In these studies, researchers showed that harbor seals were opportunistic predators and their food habits were related to their habitat. Studying harbor seals in Scotland, Tollit et al. (1998) reported a relationship between local geographical variations in diet of harbor seals and local differences in foraging habitats. Because deep dives were reported for harbor seals inhabiting the California coast (Kolb and Norris 1982), Tollit et al. (1998) suggested that the apparent support for Harkonen s hypothesis may be due to the available water depths near haul-out sites. Tollit et al. (1998) concluded that the choice of an optimal dive depth of a harbor seal should depend on several factors; (1) local bathymetric conditions, (2) the ability to maximize the proportion of time spent foraging, (3) the availability of prey geographically and vertically in the water column, and (4) the cost and benefits of feeding on different species. Implicit in the second factor was the effect of body mass on diving capabilities. The positive relationship between the body mass and breath-holding capability has been reported for several species of pinnipeds (Schreer et al. 2001). Large harbor seals are capable of longer, and possibly deeper, dives than small seals. Consequently, the optimal foraging depth within an environment may differ among different-sized individuals. Vertical partitioning of foraging areas among individuals may reduce the intraspecific competition, if the resources are limited relative to the size of the population. Conversely, if resources are not limiting, no vertical partitioning among individuals would be apparent. In this study we considered effects of local bathymetric conditions and body mass on foraging depths of harbor seals. Along the coast of central California, harbor seals are exposed to a wide range of water depths within a few kilometers of their haulout sites. The bottom topography of Monterey Bay and seasonal northwesterly wind provide upwelling within and to the north of the bay. Nutrient-rich water is brought up to the shallow water along the sea cliff and over the continental shelf, creating ideal foraging places for harbor seals. This physical environment provides opportunities for evaluating the hypothesis of Harkonen (1987a) and possible effects of breath-holding capabilities on foraging harbor seals. MET H o D s Diving depths of harbor seals were recorded using time-depth recorders (TDRs; Mk3e, Wildlife Computers, Redmond, WA). Each TDR was equipped with two depth channels for a hydrostatic pressure sensor, which recorded depth and time every 15 s with a resolution of 1 m. Each TDR was encased in flotation material (Syntactic Foam; Flotation Technologies, Biddeford, ME) with a radio transmitter ( MHz, Advanced Telemetry System (ATS), Isanti, MN), enabling us to locate the TDR package. The flotation was painted fluorescent orange and designed to float with the VHF antenna upright allowing recovery at sea. The combination of TDR, flotation, and VHF transmitter collectively was called a backpack. Each backpack was approximately 25 cm in length, 5 cm in diameter, and weighed 400 g. A backpack was attached to a base plate, which was glued to the dorsal pelage of the seal.
3 EGUCHI AND HARVEY HARBOR SEAL DIVING BEHAVIOR 285 A backpack was attached to a base plate using one of the following three methods: (1) a C-clamp, magnesium bolt (1.59 cm diameter), and steel nuts, (2) a U-shaped aluminum bracket, magnesium bolt (1.59 cm diameter), and steel nuts, and (3) two U-shaped aluminum brackets, stainless steel wire (0.8 mm diameter), and a remote release mechanism (RRM). For the first two methods, the base plate was glued to the dorsal pelage of the seal via a metal plate with fast-setting epoxy (Devcon, Wood Dale, IL) or neoprene patch with instant adhesive (Loctite 422). Magnesium bolts corroded in sea water and the backpack was released after one to four weeks. For the last method, the RRM was designed by Jamie Stamps (Sandia National Laboratories, Livermore, CA), collaborating with University of California, Santa Cruz (D. Croll and B. Tershey) and Moss Landing Marine Laboratories. The RRM consisted of receiving and transmitting units. The receiving unit glued in each backpack consisted of an electronic circuit, batteries (two AAA or AA), and a wire cutter. The circuit was designed to recognize a coded signal (FM with base frequency MHz). When the circuit received the signal, the electrical current ignited an explosive, which actuated a stainless steel blade (Guillotine, Quantic Industries, Inc., Hollister, CA) and cut the wire. A magnesium bolt was used as an auxiliary detachment method. Backpacks were detached or released from seals within a few days to four weeks of deployment. Harbor seals were caught in Elkhorn Slough between July 1994 and November 1996 (Fig. l), using methods described by Jeffries et al. (1993). Thirty-three TDRs were deployed on adult harbor seals (19 males and 14 females). Data from a retrieved TDR were downloaded to a personal computer upon recovery and then processed with Zero-Offset-Correction (ZOC) software (Wildlife Computers, Redmond, WA), which corrected drifts in readings of the pressure sensor. Zerooffset corrected data files were then processed with Dive Analysis (DA) software from Wildlife Computers to calculate statistics of dives. Several computer programs also were written to further analyze results. All dives 5 30 s and 5 3 m were discarded from further analyses to avoid possible bias from a brief submersion of a TDR and also by recommendation of the TDR manufacturer (the minimum depth of a dive should be at least twice the resolution of the recorder; Dive Analysis software manual, Wildlife Computers 1996). Dive records of each seal were separated into multiple presumed foraging trips. Although a foraging trip most likely included traveling and other activities, such as predator avoidance, we assumed the main purpose of the trip was foraging. A presumed foraging trip was distinguished from non-foraging periods by visually inspecting continuous dive records (Fig. 2). Only dives during presumed foraging trips were included in analyses. We used two methods for evaluating potential temporal effects of instruments on diving behavior of harbor seals. One was the ratio between seal body mass and tag weight (Cuthill 1991), and the other was to investigate the duration at surface as a function of time since tagging. We used the time at surface as an indicator ofphysical stress of a tagged seal caused by drag of the backpack. We, therefore, examined durations at surface of a tagged harbor seal as a function of time since tagging. Autocorrelation was calculated between kth readings of the duration at surface, where 1 < k - < 20. If absolute autocorrelation of surface time was less than 2/& at kth reading, then we assumed that data were statistically independent for every kth dive, where n= number of samples (Diggle 1990). We, therefore, extracted every kth readings from the beginning of each data set, which we call the reduced data set for the seal. The reduced data set was then analyzed by the least-square linear regression analysis.
4 286 MARINE MAMMAL SCIENCE. VOL. 21. NO Figare 1. Haul-out sites of harbor seals in Elkhorn Slough and approximate 100-m bottom concour of the Monterey Bay area. Majority of tagging was conducted at two major haul-out sites: the dike area (3) across the main channel from Seal Bend (4) and the mudflat (5) across the main channel from the dairy farm (7). To classify two-dimensional profiles of dives, we used the method described by Schreer and Testa (1995, 1996). Each dive was classified into one of four geometric types by using the similarity index described in Schreer and Testa (1996): square (type I), V (type II), skewed-right (type III), and skewed-left (type IV). We considered type I dives to be foraging dives (Le Boeuf et al. 1988, Hindell et al.
5 EGUCHI AND HARVEY HARBOR SEAL DIVING BEHAVIOR 287 Time (Day of the year + fraction of day) Figure 2. An example of continuous dive record during two presumed consecutive foraging trips of a harbor seal in Monterey Bay, CA. Linear interpolations were used to connect data points, which were recorded every 15 s via a TDR. Two segments of continuous record (A and B) were enlarged in lower figures. Day of the year 293 corresponds to 19 October The record was from seal s5595 (female, SL = 139 cm, mass = 83.5 kg) , Thompson and Fedak 1993, Lesage et al. 1999). Optimal foraging depths of tagged harbor seals were determined by computing the median and 97.5 th percentile of dive depths for each seal and all seals combined. Unless otherwise stated, we reported standard error or the 95% confidence interval as a measure of uncertainty around the mean. RESULTS Twenty-eight backpacks were recovered and useful data were retrieved from 20 TDRs. Because three tagged harbor seals did not exit Elkhorn Slough while the TDR was attached, dive data from these seals were discarded. We also excluded data from seal s5140 from all analyses because the backpack detached from the seal within 24 h of deployment. After visually inspecting dive records and eliminating dives that appeared to be concatenations of multiple dives, 13,063 dives were analyzed for 16 seals (Table 1). Because we caught only one female harbor seal during winter, we were unable to simultaneously compare differences in diving behavior between sexes and seasons. Median depths of dives of harbor seals were m for males (X = m, n = 11; Table 1) and m for females (X = m, n = 5; Table 1). There was a statistically significant positive relationship between the 2 median depth of dives and mass of the seal (Zmedian = X (mass), r = 0.37, 95% CI for slope= [0.32, 2.211, n = 16; Fig. 3a). When the relationship was grouped by sex, however, the slope of the regression line for female seals was not statistically different from zero (95% CI for slope = [-3.22, 6.041, n = 5). There
6 Table 1. Morphological data and dive statistics of harbor seals tagged with TDRs. Depth and durations (Dur.) of dives include average, SE in parentheses, and median in braces. Z95 and D95 indicate the 95'h percentile of depth and duration of dives, respectively. For each dive type (I-IV), the number of dives, median depths in parentheses, and median durations in braces are shown. Seal ID IV(m) Date Length Girth Mass number tagged (cm) (cm) (kg) n Depth z95 Dur. 095 I (m) I1 (m) 111 (m) Female ~5213 8/16/ (0.1) (0.1) (13.0) 14 (14.0) 42 (12.0) 18 (12.5) (13.0) (3.33) (3.42) (1.42) (2.33) (2.54) ~5332 4/13/ (1.0) (0.05) (78.0) 221 (83.0) 23 (28.0) 18 (18.0) (78.0) (5.50) (5.75) (5.25) (3.00) (2.50) s5486 7/20/ (0.2) (0.4) (5.0) 17 (5.0) 10 (6.5) 39 (7.0) (5.0) (2.75) (3.00) (0.75) (1.50) (2.25) ~5185 5/3/ (0.9) (0.1) (88.0) 27 (36.0) 47 (37.0) 22 (10.0) (86.0) (7.25) (7.25) (3.75) (4.25) (1.50) ~ /9/ " (1.2) (0.1) (20.0) 80 (16.0) 87 (11.0) 66 (8.0) (17.0) (7.00) (7.25) (3.00) (3.00) (2.75) Mean (14.2) (0.8) 7.42 (SE) (5.4) (4.1) (6.0) (24.5) (1.13) Male ~ (3.4) (77.0) ~ /13/ (2.0) (89.0) ~ /18/ (0.4) 28.3 (21.0) ~5425 1/1/ (2.3) 92.8 (53.5) ~5517 1/1/ (1.6) (8.0) 7.2 (0.1) (6.50) 6.0 (0.1) (6.25) 3.5 (0.1) (3.50) 6.6 (0.2) (6.75) 3.5 (0.1) (2.5) l(10.0) 522 (70.0) 299 (93.0) (6.75) (6.25) (90.0) 35 (89.0) (6.50) (5.25) (21.0) (3.50) (1.00) (54.5) 4 (37.5) (6.75) (2.25) (7.0) 60 (10.5) _~ (2.75) (2.13) 54 (50.0) (5.75) 38 (82.0) (5.88) 1 (6.0) (3.00) 1 (41.0) (1.25) 67 (9.0) (2.00) 14 (39.0) { 5.OO} 11 (36.0) (3.25) 1 (21.0) { 1.OO) 3 (35.0) (3.50) 56 (8.0) (2.50) w W c e N - z P N
7 Table 1. Continued. Seal ID IV(m) Date Length Girth Mass number tagged (cm) (cm) (kg) n Depth Z,, Dur. D,, I (m) 11 (m) I11 (m) s5875 8/24/ (5.5) (0.2) (0.1) (5.0) 21 (7.0) 61 (7.0) (5.0) (2.75) (2.75) (1.75) (2.50) (2.50) ~5596 1/3/ (1.2) (0.1) (23.0) 40 (32.0) 42 (15.5) 8 (18.5) (22.0) ( 5.OO} (5.50) (2.25) (2.13) (2.88) ~5306 2/28/ (8.0) (0.3) (84.0) 8 (371.0) 11 (137.0) 3 (12.0) { 85.O} (7.50) (7.50) (11.63) (11.00) (6.25) ~5145 9/12/ (1.2) (0.05) (94.0) 174 (84.5) 111 (103.0) 19 (16.0) (93.0) (3.25) (6.00) (4.88) (6.75) (3.50) s5276 9/17/ (0.4) (0.04) (20.0) 90 (13.5) 71 (17.0) 46 (10.0) (17.0) (2.75) (3.00) (1.75) (2.25) (1.88) ~ /9/ (2.2) (0.1) (91.0) 311 (202.0) 156 (98.0) 47 (30.0) ( 100.0) (8.50) (8.25) (9.25) (8.00) (6.00) Mean (SE) (2.4) (2.3) (18.2) (12.4) (37.6) (0.6) (1.1) a Axillary girth of harbor seals ~5306, ~5595, and s5205 were estimated using a regression equation (girth = X length, r2 =0.791), which was obtained from data collected from 148 harbor seals captured and measured in Elkhorn Slough, CA, between August 1994 and October 1996.
8 290 MARINE MAMMAL SCIENCE, VOL. 21, NO. 2, r * - a- v 5 = s 6- D c , I * Q/,/ 0,/, * / O, //- /,,,, - cl-.-:&- - * /-d * I / * +O + * I I I I 1 was a statistical1 significant linear relationship for males (Zmedian,$ = X (mass), Y Y = 0.41, 95% CI for slope = [0.13, 2.471, n = 11). Median durations of dives of harbor seals were min for males (X = 5.0 -t 0.7 min, n = 11; Table 1) and min for females (X = 5.16? 0.92 rnin, n = 5; Table 1). There was a significant positive relationship between the median duration of dives and mass of the seal (Dmedian = X (mass), y2 = 0.60, 95% CI for slope = t0.05, 0.131, n = 16; Fig. 3b). When the relationship was grouped by sex, a greater variability in the median duration of dives was explained by the linear model for females = X (mass), r2 = 0.86, 95% CI for slope = [0.04, 0.251, n = 5) than for males (Dmedian,$ = X (mass), Y = 0.69, 95% CI for slope = [0.05, 0.151, n = 11). Deep dives of harbor seals (the 95th percentiles of depth of dives for each seal; Z9,) were m for males (X = 154.4? 37.6 m, n = 11; Table 1) and m for females (5E = m, n = 5; Table 1). There was a significant positive linear relationship between Z9, and mass of the seal (Z9, = X (mass), v2 = 0.80, 95% CI for slope = [3.97, 7.171, n = 16; Fig. 4a). When the relationship was grouped by sex, however, the slope of the regression line for female seals was not significantly different from zero (95% CI = [-1.7, 7.91). For males, however, the linear model (Z9,,$ = X (mass&, 95% CI for slope = [3.93, 8.171, n = 11; Fig. 4a) explained 83% of the variability in
9 EGUCHI AND HARVEY HARBOR SEAL DIVING BEHAVIOR E J IM) Body Mass (kg) Figure 4. A linear relationship between the body mass and the 95th percentile of depths (a) and durations (b) of dives. A circle indicates a female seal and a star indicates a male seal. A solid line is the regression line for male and female combined, dotted line is for male seals, and dashed line is for female seals. Z9,,$. The deepest recorded dive during the study was 481 m (s5490), which appeared to be truncated at the limit of the pressure sensor. Dives of greater duration of harbor seals (the 95th percentiles of duration of dives for each seal; D95) were from 4.5 to 15.5 min for males (?= 9.4 * 1.1 min, n = 11; Table 1) and from 4.5 to rnin for females (%= 7.4 +_ 1.1 min, n = 5; Table 1). A linear relationship was found between the D9, and mass of the seal (D9, = X (mass), 95% CI for slope = [0.13, 0.211, Y' = 0.85, n = 16; Fig. 4b). For males and females, linear models explained greater than 80% of the variability in D9, (09,,? = X (mass?), 95% CI for slope = [0.08, 0.281, r' = 0.91, n = 5; D9,,3 = X (mass&), 95% CI for slope = [0.12,0.24], Y' = 0.83, n = 11; Fig. 4b). The greatest duration of a dive was min (~5306). Approximately 80% of recorded dives (10,436; Table 2) were classified as square dives (Type I) according to the similarity index described by Schreer and Testa (1996). Only 11% (1,402 dives) were V dives, and less than 10% (1,225 dives) were skewed dives (Table 2). No difference was found in the median depths of dives between the two dive types (95% CI for the mean of differences = [-62.9, 20.33, n = 16). For the average median durations, type I dives were greater in duration than type I1 dives (95% CI for the mean of differences = r0.33, 2.581; Table 2). DISCUSSION The total mass of a backpack (-400 g) was less than 1% of body mass for all seals tagged with backpacks, which was considerably less than the maximum (5%) recommended for radio-telemetry studies (Cuthill 1991). Further, the analysis on
10 ~ 292 MARINE MAMMAL SCIENCE, VOL. 21, NO. 2, 2005 Table 2. Mean median depths and durations for four dive types recorded for 16 harbor seals in the Monrerey Bay area. Values in brackets are based on all dives, whereas means and SE were computed for 16 seals. Type I Type I1 Type I11 Type IV N 16 [10,436] 16 [1,402] 16 [ percentage [80.0] [10.7] Mean median depth (SE; m) 47.7 (9.03) 69.0 (23.9) 41.3 (10.4) 17.9 (2.8) Mean median duration (SE; min) 5.37 (0.47) 3.91 (0.77) 4.04 (0.68) 3.11 (0.37) - - temporally independent reduced data sets indicated that rime since tagging was not a good indicator of the duration at the surface (r2 < 0.08). We assumed, therefore, effects of backpacks on diving behavior of tagged harbor seals were constant throughout the duration of backpack attachment, and probably did not affect the dive behavior of tagged seals. Square dives dominated (80%) recorded dives, according to the classification index of Schreer and Testa (1995, 1996; Table 2). Square dives were considered to be associated with foraging in pinnipeds (Le Boeuf et al. 1988, Hindell et al. 1991, Thompson and Fedak 1993, Lesage et al. 1999). Approximately 11% of all dives were classified as V-dives, which often were considered to be exploratory or traveling dives (Hindell et al. 1991, Bengtson and Stewart 1992, Thompson and Fedak 1993, Lesage et al. 1999). Without other information, such as stomach temperature, underwater behavior, or surface behavior, functions of these dive types were unknown. We think, however, square dives of harbor seals in Monterey Bay probably were associated with foraging because continuous dive records indicated square dives were repeated to a similar depth during a foraging bout (Fig. 2). The hypothesis by Harkonen (1987d), which predicted a harbor seal to forage at an intermediate depth, was generally supported by the findings of our study. Our study provided evidence for two of the three premises for the hypothesis; relationship between availability of prey and foraging depth and relationship between foraging grounds and bathymetric conditions. Benthic feeding of harbor seals, the final premise for the hypothesis, was inferred from other studies in the area. An additional component to the hypothesis was an apparent relationship between diving duration and diving capability (oxygen store) of harbor seals. Foraging dives of harbor seals in the Monterey Bay area were affected by their body mass (Fig. 3, 4). Relationships between duration of dives and body mass have been reported for many air-breathing diving vertebrates (Schreer and Kovacs 1997, Schreer et al 2001). The duration of a dive was limited by the oxygen stores of the seal (Schreer and Kovacs 1997, Schreer et al. 2001). Consequently, a large seal should be able to dive for greater duration than smaller seals. Our study provided additional information on the positive relationship between the breath-holding capability and body mass in pinnipeds. Depths of foraging dives, however, were affected by body mass to a lesser extent. Approximately 40% or less of variability in median depths of foraging depths was explained by the linear model that used body mass as the explanatory variable. These results indicated that duration of dives were affected strongly by oxygen stores, whereas, depths of dives were affected also by other unmeasured factors, such as the vertical distribution of prey in the environment. Because of the submarine canyons and strong northwesterly wind during spring and summer, coastal upwelling occurs in Monterey Bay. Productive waters from
11 EGUCHI AND HARVEY HARBOR SEAL DIVING BEHAVIOR 293 depth are brought up to surface during the upwelling season (Breaker and Broenkow 1994). During the non-upwelling season, however, upwelling abates and oceanic water flows into the bay from offshore, decreasing the productivity in the shallow water (Breaker and Broenkow 1994). Consequently, the assemblage of the potential harbor seal prey in the region varies temporally. Although no comprehensive studies of direct relationships between temporal and spatial distributions of prey species and feeding grounds of harbor seals have been conducted in the Monterey Bay area, analyses of fecal samples have indicated temporal changes in food habits of harbor seals in the area (Oxman 1995, Trumble 1995). Although the majority of fish and macro invertebrate species found in fecal samples were benthic, pelagic species became more dominant when the water in Monterey Bay was productive. During spring and summer, pelagic species (e.g., anchovy, Engraulis mordax; market squid, Lolzgo opalescens; and Pacific hake, Merhccizcs productus) became abundant in fecal samples of harbor seals. Similar findings of the importance of pelagic prey in the diet of harbor seals have been reported from other areas (Harkonen 19876, Tollit and Thompson 1996, Brown and Pierce 1998). These findings indicated that the first premise of Harkonen s hypothesis (ie., harbor seals are benthic predators) depended on the vertical distribution of abundant prey species and seasonality of prey distributions in the habitat. We think that harbor seals in Monterey Bay feed on seasonally abundant species, pelagic or benthic. Consequently, dive depths were shallower when harbor seals foraged on pelagic species than when they forage on benthic species. Relationships between dive depths of pinnipeds and seasonal productivity of oceans have been reported for other areas. Frost et al. (2001), for example, hypothesized that deeper dives of harbor seals during winter were caused by a decrease of available prey in the shallow water of Prince William Sound, AK. The Steller sea lion (Eumetopias ju6atus) in northern Gulf of Alaska also was reported to dive to shallower depths during winter corresponding with the shift in prey availability (Merrick and Loughlin 1997). Therefore, it was plausible that harbor seals in the Monterey Bay area changed their dive depths according to the productivity of the environment-shallower dives during the upwelling season and deeper dives in submarine canyons during the oceanic season. Because of limited sample sizes and the lack of knowledge about foraging locations of tagged harbor seals in our study, however, we were unable to explicitly test this possibility. The third premise of Harkonen s hypothesis also was supported; dive depths of harbor seals were influenced by the available water depths near their haul-out sites. Although most dives were to depths previously reported for harbor seals in other regions (Boness et al. 1994, Bjerge et al. 1995, Coltman et al. 1997, Tollit et al. 1998, Lesage et a/. 1999), deep dives (>200 m) wete observed in a few harbor seals in this study (Table 1). Although the majority of the bay is <200 m, a submarine canyon is within a few kilometers of a haul-out site for harbor seals in the area, making the deep water readily accessible to harbor seals. Harbor seals used this submarine canyon during the study, especially during the oceanic season. Additional information on underwater behavior of these seals, however, was necessary to determine the purposes of these dives. Based on the premise that square dives were associated with foraging, results of our study generally supported the hypothesis by Harkonen (1987~). Harbor seals in Monterey Bay spent the majority of their time at intermediate depths within the bay. Even though deeper waters >400 m were near their haul-out sites, presumed foraging dives were often found at between 50 and 200 m. As Tollit et al. (1998)
12 294 MARINE MAMMAL SCIENCE, VOL. 21, NO suggested, however, there were several factors that affected the apparent intermediate foraging depths, such as available water depths in the proximity of haulout sites, physiological limitations, and productivity of the water. Finally, no apparent vertical partitioning of prey within Monterey Bay among different sized harbor seals was found, indicating unlimited resources for harbor seals in the area. ACKNOWLEDGMENTS This study was supported by a grant from the Office of Naval Research (contract number: N , R&T code: ). This study was conducted under NMFS scientific research permits 737 and 974 (issued to JTH). We thank the fearless tagging team of Moss Landing Marine Laboratories (MLML) and many interns for their support in the field. Technical advice and support were provided from many people, especially A. DeRose (MLML), The Small Boat Operation of MLML, and R. Andrews. We also thank Michelle White for creating the maps. Tero Harkonen and an anonymous reviewer provided critical comments that significantly improved the manuscript. LITERATURE CITED BENGTSON, J. L., AND B. S. STEWART Diving and haulout behavior of crabeater seals in the Weddell Sea, Antarctica, during March Polar Biology 12: BJQRGE, A., D. THOMPSON, P. HAMMOND, M. FEDAK, E. BRYANT, H. AAREFJORD, R. ROEN AND M. OLSEN Habitat use and diving behaviour of harbour seals in a coastal archipelago in Norway. Pages in A. S. Blix, L. Wallee and 8. Ulltang, eds. Whales, seals, fish and man, Proceedings of the International Symposium on the Biology of Marine Mammals in the North East Atlantic, TromsG, Norway, 29 November December Elsevier Science, Amsterdam, The Netherlands. BONESS, D. J., W. D. BOWEN AND 0. T. OFTEDAL Evidence of a maternal foraging cycle resembling chat of otariid seals in a small phocid, the harbor seal. Behavioral Ecology and Sociobiology 34: BREAKER, L. C., AND W. W. BROENKOW The circulation of Monterey Bay and related processes. Oceanography and Marine Biology: An Annual Review 32:l-64. BROWN, E. G., AND G. J. PIERCE Monthly variation in the diet of harbour seals in inshore waters along the southeast Shetland (UK) coastline. Marine Ecology Progress Series 167: COLTMAN, D. W., W. D. BOWEN, D. J. BONES AND S. J. IVERSON Balancing foraging and reproduction in the male harbour seal, an aquatically mating pinniped. Animal Behaviour 54: CUTHILL, I Field experiments in animal behaviour: Methods and ethics. Animal Behaviour 42: DIGGLE, P. J Time series: A biostatistical introduction. Oxford University Press, New York, NY. FROST, K. J., M. A SIMPKINS AND L. F. LOWRY Diving behavior of subadult and adult harbor seals in Prince William Sound, Alaska. Marine Mammal Science 17: HARVEY, J. T., R. C. HELM AND G. V. MOREJOHN Food habits of harbor seals inhabiting Elkhorn Slough, California. California Fish and Game 81: 1-9. HINDELL, M. A,, D. J. SLIP AND H. R. BURTON The diving behaviour of adult male and female southern elephant seals, Mirounga leonina (Pinnipedia:Phocidae). Australian Journal of Zoology 39: HARKONEN, T. 1987a. Influence of feeding on haul-out patterns and sizes of sub-populations in harbour seals. Netherlands Journal of Sea Research 21: HARKONEN, T Seasonal and regional variations in the feeding habits of the harbour seal, Phaw uitufinu, in the Skagerrak and the Kattegat. Journal of Zoology 213:
13 EGUCHI AND HARVEY HARBOR SEAL DIVING BEHAVIOR 295 JEFFRIES, S., R. BROWN AND J. T. HARVEY Techniques for capturing, handling and marking harbour seals. Aquatic Mammals 19. 1: KOLB, P. M., AND K. S. NORRIS A harbour seal, Phoca vitulina richardsi, taken from a sable fish trap. California Fish and Game 68: LE BOEUF, B. J., D. P. COSTA, A. C. HUNTLEY AND S. D. FELDKAMP Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: LESAGE, V., M. 0. HAMMILL AND K. M. KOVACS Functional classification of harbor seal (Phoca vitulina) dives using depth profiles, swimming velocity, and an index of foraging success. Canadian Journal of Zoology 77: MERRICK, R. L., AND T. R. LOUGHLIN Foraging behavior of adult female and youngof-the-year Steller sea lions in Alaskan waters. Canadian Journal of Zoology 75: OXMAN, D. S Seasonal abundance, movements, and food habits of harbor seals (Phoca vitulina richardsi) in Elkhorn Slough, California. M.S. thesis, Moss landing Marine Laboratories, California State University, Stanislaus, CA. 126 pp. SCHREER, J. F., AND J. W. TESTA Statistical classification of diving behavior. Marine Mammal Science 11: SCHREER, J. F., AND J. W. TESTA Classification of Weddell seal diving behavior. Marine Mammal Science. 12: SCHREER, J. F., AND K. M. KOVACS Allometry of diving capacity in air-breathing vertebrates. Canadian Journal of Zoology 75: SCHREER, J. F., K. M. KOVACS AND R. J. O HARA HINES Comparative diving patterns of pinnipeds and seabirds. Ecological Monographs 71: THOMPSON, D., AND M. A. FEDAK Cardiac responses of grey seals during diving at sea. Journal of Experimental Biology 174: TOLLIT, D. J., AND P. M. THOMPSON Seasonal and between-year variations in the diet of harbour seals in the Moray Firth, Scotland. Canadian Journal of Zoology 74: TOLLIT, D. J., A. D. BLACK, P. M. THOMPSON, A. MACKAY, H. M. CORPE, B. WILSON, S. M. VAN PARIJS, K. GRELLIER AND S. PARLANE Variations in harbour seal Phoca vitulzna diet and dive-depths in relation to foraging habitat. Journal of Zoology TRUMBLE, S. J Abundance, movements, dive behavior, food habits, and motherpup interactions of harbor seals (Phoca vitulina richardsi) near Monterey Bay, California. M.S. thesis, Moss Landing Marine Laboratories, California State University, Fresno, CA. 100 pp. Received: 23 October 2000 Accepted: 19 October 2004
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