PART III—
DIVING AND FORAGING

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Twelve—
Theory of Geolocation by Light Levels

Roger D. Hill

ABSTRACT. A technique for determining the location of elephant seals is described. This technique requires an accurate determination of time of dawn and dusk on a daily basis. The time midway between dawn and dusk, the local apparent noon, determines the seal's longitude, and the day length is used to determine latitude. The longitude determination is equally accurate throughout the year and at all latitudes except those with no dawn and dusk events; the latitude determination is most accurate at the solstices and useless at the equinoxes. Other sources of error are the accuracy of the light-level measurement, atmospheric aberration, and the seal's behavior.

Elephant seals present a particular challenge to the researcher who wants to know where they go. Elephant seals generally surface for inadequate periods of time for reliable tracking by the Argos satellite system (Stewart et al. 1989); however, some researchers have had success with this system by mounting the transmitter on the seal's head. Elephant seals also dive so deep that any instrumentation must be solid or have a substantial pressure housing. These two problems combine to make it difficult to track an elephant seal reliably for more than a few months without the transmitter becoming detached. The price of satellite-transmitters is also generally too high for large-scale studies. However, elephant seals are reasonably faithful to their molting and breeding beaches, so that deployments and recovery of memory-based instruments such as time-depth recorders (TDRs) have been quite successful. In early 1989, it was suggested that I attempt to incorporate a geolocation feature into our TDRs. By recording and storing light levels, times of dawn and dusk could retroactively be determined and used to calculate position using standard solar navigational equations.

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Fig. 12.1
Circle A is dawn/dusk interface at
Time A.

The Theory

The principle of determination of location is reasonably straightforward: fig. 12.1 shows the earth, with the sun to the right. The bold circle that encompasses the earth is the line between day and night. Note that this circle does not pass through the north or south pole. Figure 12.2 shows the earth approximately 12 hours later. The sun is still to the right, but the earth has rotated by nearly 180° and Circle A from figure 12.1 has moved with it. Circle B is the line that currently divides day from night. If we consider a point on the earth for which the sun was rising in figure 12.1 and is now experiencing sunset, then the point must be on both Circle B and Circle A. The position is, therefore, an intersection of these two circles (one intersection is for A = dawn and B = dusk, the other is for A = dusk and B = dawn). If we know the times of dawn and dusk and the day of year (which affects the tilt of the earth and thus the position of the dawn-dusk circles), then we can theoretically calculate the location of their intersection and, hence, our position.

The standard equations used for solar navigation (Yallop and Hohenkerk 1985; Nautical Almanac Office 1991) predict the time at which a solar event occurs for a given day of year and location on the earth. The solar event of interest here is when the sun is at an azimuth of 96° (the center of the sun is 6° below the horizon). This is known as civil twilight and is when the sun's first light appears (dawn) or last light disappears (dusk). At these times light level is changing fastest, so that the times of these events can be determined from light-level measurements most accurately. Unfortunately, the standard equations yield the inverse of the required information, so an

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Fig. 12.2
Circle B is new dawn/dusk interface at
Time B. Circle A has rotated with the
earth from figure 12.1. Location that had
dawn at Time A and dusk at Time B is
at the intersection of the two circles.

iterative process is used to find the location for which predicted times of dawn and dusk coincide with measured values.

The iterative process starts with an estimate of longitude—longitude (°E) = (time of midnight) × 15, where time of midnight is halfway between dusk time and dawn time and all times are measured in Universal Time (UT) or Greenwich Mean Time (GMT)—and an estimate of latitude of –45° or +45°, depending on the previous position. This first guess of position is used to generate dawn and dusk times, which are compared with the observed dawn and dusk times to produce the next location estimate. This process continues until the observed and predicted dawn/dusk times match to the desired degree of accuracy.

Sources of Error

Equinoxes

Our ability to determine latitude fails near the vernal or autumnal equinoxes, as shown in figure 12.3. The dawn/dusk circle now passes through or very close to the north and south poles. This means that for all places on the earth, the dawn and dusk circles (A and B in fig. 12.2) will now be very close or overlap, and the ability to determine latitude is lost. This does not affect the calculation of longitude. (The location is somewhere on the dawn/dusk circles, which are now also circles of longitude because they pass through the poles.) The usefulness of the solar equations for

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Fig. 12.3
At the equinoxes, dawn and dusk circles
overlap, so that latitude determination
is not possible.

calculating latitude is effectively determined by the variation of day length (the time between dawn and dusk) with latitude for each day of the year. If a small difference in day length generates a large difference in latitude, then position is difficult to estimate because any small error in assessing day length will cause a large error in the latitude determination. Conversely, if a large change in day length generates a small difference in latitude, then the position calculated will be accurate.

The relationship between time of year, latitude, and day length is summarized in figure 12.4. The accuracy of a latitude determination for a given day and latitude is determined by the slope of day length with latitude. For example, Day 1 shows a good slope between –45° and +45° latitude, indicating the potential for a good estimate of latitude, and a steeper slope between –60° and –45° and between +45° and +60°, indicating the potential for even better latitude estimates. However, at about Day 265, there is almost no slope except very near the poles, indicating a complete inability to determine latitude from day length variations. Figure 12.5 shows an enlargement of figure 12.4 near the autumnal equinox. Note that between Day 252 and Day 281, the day length at both poles is 24 hours. This is because day length is measured from the time that the sun rises above 96° azimuth to when it sets below 96° azimuth (actually about 7 months at each pole). Had we chosen an azimuth of 90°, day length would have changed from 0 to 24 hours (or vice versa) at both poles on the same day. A side effect of using an azimuth of 96° is that for Days 252 through 281 (and for the equivalent days near the vernal equinox), a measured dawn and dusk time will generate two locations. The correct location must be chosen by comparison to previous locations. Although the quality of latitude determinations near the equinoxes is generally poor, studying the

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Fig. 12.4
Day length as a function of day of year and latitude.

Fig. 12.5
Day length as a function of day of year and latitude near the autumnal equinox.

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Fig. 12.6
Error in latitude determination caused by a 4-minute error in day length measurement
as a function of day of year and latitude.

gradient of day length with latitude (fig. 12.5) shows that a latitude determination will be possible in some ranges of latitude and day of year (e.g., Day 249, latitude + 45° to + 75°).

An alternate way of displaying this relationship between day of year, latitude, and day length is shown in figure 12.6. A theoretical uncertainty in the accuracy of a location (error) is plotted against latitude and day of year. The error is the range of latitude that is generated by moving dawn and dusk times by ± 4 minutes. An accuracy of ± 2 minutes is the limit of accuracy in observing dawn or dusk due to atmospheric phenomenon, and this has been doubled to reflect other likely errors. The error in latitude has been truncated at 20° for clarity. The slightly skewed nature of the two equinox "ridges" is again caused by using a dawn/dusk azimuth of 96°; had we used 90°, the ridges would not be twisted. The "plateaus" between the ridges show the days and locations where good locations can be expected from a measurement of light levels.

The simplest solution for reducing the ambiguity in latitude near the equinoxes is to use some other measurement to fix the latitude. The obvious choice is surface seawater temperature, which varies considerably with lati-

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tude and is available on a week-to-week basis from a combination of satellite imagery and oceanographic buoys. In the waters surrounding the United States, these data are compiled by the National Marine Fisheries Service and the National Weather Service. Latitude is found by determining which locations on the known line of longitude have the measured surface seawater temperature.

Accuracy of the Light-level Measurements

There are several sources of potential error in recording the light-level measurements, only some of which can be controlled. The time at which the light-level measurements were taken must be known accurately; one minute of inaccuracy in the estimate of dawn and dusk times will generate an error of 0.25° of longitude and an error in latitude of about 25% of the error shown in figure 12.5. To minimize the timing errors, users must carefully set the recorder's clock before deployment and note any time error on retrieval. The analysis program must then use this error data and adjust all time measurements accordingly. The magnitude of the light level will change over many orders of magnitude between night and day, so it should be recorded on a logarithmic scale and carefully calibrated so that it will not "peg-out" in bright sunshine or complete dark. Since one will have no control over the orientation of the light sensor when it is collecting data, it should be responsive to light over wide angles and be positioned so that it will generally point up. Obviously, none of these suggestions will help if the study animal is on shore, on its back, and the light sensor is buried in sand. Such data points must be excluded at analysis time.

Atmospheric Aberration

Light does not generally pass through the earth's atmosphere in straight lines; it bends when it encounters thermal or pressure gradients. For this reason, it is generally considered impossible to measure the time of dawn or dusk to an accuracy of greater than 2 minutes, even if one is observing the sun directly rather than measuring ambient light levels (C. Acton pers. comm.). This is a major source of error in this type of navigation; 2 minutes of inaccuracy in the estimate of dawn and dusk times will generate an error of 0.5° of longitude and an error in latitude of about 50% of the error shown in figure 12.5. Some compensation for hot and cold and high and low pressure days can be applied to the navigational equations if one has these data.

Animal Diving at Dawn or Dusk

Elephant seals are known to perform 20-minute dives alternating with 3-minute surface times for many hours at a time (Le Boeuf et al. 1986, 1988,

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1989; Stewart and DeLong 1990; DeLong and Stewart 1991). With behavior such as this, a light sensor will probably be at depth during the actual dawn and dusk times. The analysis of light levels must cope with this problem, and, generally, an interpolation technique around the times of dawn or dusk will work well to determine the actual dawn or dusk times. If there is an extended dive at dawn or dusk (greater than 30 minutes), then determination of the dawn or dusk times will not be possible.

Animal Moving between Dawn and Dusk

The above analysis assumes that the animal does not change its location between dawn and dusk. If it does move, the error induced depends on the direction it moves. If the animal moves along Circle A in figures 12.1 and 12.2 between dawn and dusk, then the movement will have no effect on the accuracy of the location, but the location given will be that of the animal at dusk, not some median position. Other directions of movement will have other results. Generally, large errors will only occur when the animal is covering large distances per day, and under these circumstances, a larger locational error is more acceptable. The analysis program could also minimize this error by performing the locational analysis from dusk to dawn (rather than dawn to dusk) when day length is greater than 12 hours.

The Equations

The equations used to predict dawn and dusk times also contain some inherent inaccuracies, as much as ± 2 minutes under certain circumstances. I have been unable to determine for which combinations of day and latitude these inaccuracies are worst, but it seems reasonable that the inaccuracies are going to be most severe where day length changes very rapidly with latitude. These are the same circumstances that give us inherently better locational accuracy. If this is true, then error from the equations will cancel some (or all) of the improved accuracy generated by rapidly changing day lengths. Until better equations can be provided to predict dawn and dusk times, some allowance for errors in the equations must be made.

Presentation of Errors

Since both latitude and day of year will have a profound effect on the accuracy of the latitude determination, it is important that positions generated from observed dawn/dusk times be provided with error estimates. Ideally, all locations should be plotted on a map using rectangles that indicate the limits of the animal's position to a given level of certainty. It should be noted that the center of such rectangles will not necessarily represent the likeliest location of the animal.

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Fig. 12.7
Example of analysis program's graphical output. The light-level curve is shown with
markers for derived dawn/dusk times and the calculated position range.

Practical Considerations

Wildlife Computers makes TDRs with temperature- and light-sensing options for use on diving animals. The TDR stores surface-seawater-temperature (SST) and light-level (LL) data when the instrument is at (or very near) the surface. These data are decoded and used by an analysis program to provide locations. The SST and LL data are stored whenever the study animal surfaces but generally no more frequently than every 15 minutes. These light-level data are extracted, plotted, and used to determine the times of dawn and dusk (see fig. 12.7). We have determined that dawn and dusk (sun is at an azimuth of 96°) correspond to a light level equal to the nighttime light level plus 5% of the difference between the night and day levels, when LL data are shown on a logarithmic scale.

It should come as no surprise that some of the errors inherent in attempting to geolocate a swimming or diving animal using light levels are unavoidable. Others, such as temperature effects and interpolation requirements, can be minimized in the analysis software. Our best efforts generally yield locations for elephant seals that are about ± 1 degree in latitude and longitude. Although not as precise as one might like, these location data have greatly expanded our knowledge of the foraging migrations of both southern and northern elephant seals (DeLong, Stewart, and Hill 1992).

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References

DeLong, R. L., and B. S. Stewart. 1991. Diving patterns of northern elephant seal bulls. Marine Mammal Science 7: 369–384.

DeLong, R. L., B. S. Stewart, and R. D. Hill. 1992. Documenting migrations of northern elephant seals using day length. Marine Mammal Science 8: 155–159.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, G. L. Kooyman, and R. W. Davis. 1986. Pattern and depth of dives in northern elephant seals, Mirounga angustirostris. Journal of Zoology, London 208: 1–7.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Canadian Journal of Zoology 67: 2514–2519.

Nautical Almanac Office. 1991. Almanac for Computers . Washington, D.C.: United States Naval Observatory.

Stewart, B. S., and R. L. DeLong. 1990. Sexual differences in migrations and foraging behavior of northern elephant seals. American Zoologist 30: 44A.

Stewart, B. S., S. Leatherwood, P. K. Yochem, and M.-P. Heide-Jorgensen. 1989. Prospects for tracking pinnipeds at sea using the Argos DCLS: Insights from studies of free-ranging harbor and ringed seals. In Proceedings of the 1989 North American Argos Users Conference and Exhibit , Landover, Maryland, 193–203.

Yallop, B. D., and C. Y. Hohenkerk. 1985. Compact Data for Navigation and Astronomy for the Years 1986–1990 . London: Her Majesty's Stationery Office.

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Thirteen—
Variation in the Diving Pattern of Northern Elephant Seals with Age, Mass, Sex, and Reproductive Condition

Burney J. Le Boeuf

ABSTRACT. A principal aim of studies of northern elephant seals from the Año Nuevo rookery in central California has been to obtain complete descriptions of diving behavior for the various stages of life from weaning to adulthood. Studies were conducted during the period 1983–1991 using a variety of methods on known-age animals of both sexes at various stages of development: measurement of the free-ranging diving pattern using attached time-depth recorders, determination of mass before and after trips to sea, and measurement of physiological variables during homing experiments with juveniles.

Some of the principal findings and conclusions are (1) all elephant seals of both sexes and all ages dive deep, long, and continuously for the entire periods that they are at sea; (2) by age 2, the dive pattern is similar to that of adults; (3) dive duration increases slightly with mass in nonpregnant females, but when pregnant females and adult males are included, the relationship weakens, indicating that other variables influence dive duration; (4) dive depth is independent of age and mass in animals older than 2 years of age; (5) adult males migrate farther north and west than females to specific foraging areas along the continental margin, while females disperse more widely in the open ocean and forage en route; (6) pregnant females dive longer and migrate farther away from the rookery than postbreeding females; and (7) yearlings home reliably during the spring molt and fall rest period, revealing a dive pattern like that of free-ranging animals and thus offer the opportunity for short-term studies of diving and the measurement of physiological variables.

In-depth studies of the diving behavior of elephant seals throughout development are filling in gaps in our knowledge of the marine aspect of their natural history and enhancing our understanding of the biology of diving and marine foraging.

Complete dive descriptions for the various stages of life from initial water entry to adulthood do not exist for any diving mammal. This is a serious

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Fig. 13.1
Annual distribution of time spent on land and at sea for male and female
northern elephant seals from birth to adulthood. Solid bars represent time
on land, waves represent time at sea, bars and waves represent initial water
experience prior to departure from the rookery. B = birth, W = weaning,
P (for females) = parturition, P (for males) = puberty. Primiparity in females
occurs at 3, 4, or 5 years of age. The numbers in the figure denote
the consecutive trips to sea by each sex.

omission. A thorough description of this kind yields vital information on life history, facilitates the understanding of body functions during diving, sheds light on foraging economics, and puts other dive-related processes in perspective.

One aim of our diving studies at Santa Cruz has been to obtain a description of the diving pattern of northern elephant seals of both sexes dur-

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TABLE 13.1 Free-ranging dive records obtained from northern elephant seals at Año Nuevo, 1983–1991.
	Instrument type			Totals
	Billups	Naito	Hill	Totals
Weanlings		1	1	2
Juveniles (1–2 years old)			8	8
Adult females
Nonpregnant	12	5	10	27
Pregnant	2		5	7
Adult males			6	6
	14	6	30	50

ing all periods at sea throughout development. Except for a single trip to sea during the year preceding puberty, individuals of both sexes spend two periods at sea each year of their lives. The approximate time and duration of these aquatic sojourns for each sex are shown in figure 13.1. This figure makes clear that elephant seals are among the most pelagic of all seals.

I summarize data from 50 dive records obtained from elephant seals at Año Nuevo from 1983 to 1991 (table 13.1), paying special attention to variation in dive pattern with age, mass, reproductive condition, and sex. I also present the main results of a translocation study of yearling elephant seals that shows that it is feasible to study diving in elephant seals in the short run. My aim is to give an overview of certain aspects of the diving research from this laboratory. The treatment will be topical because of space limitations and because each topic will be treated in depth elsewhere.

The general method used to collect all free-ranging dive data consisted of attaching a diving instrument and radio transmitter to a seal shortly before it went to sea and then recovering the instrument when the animal returned to the rookery months later (Le Boeuf et al. 1986, 1988, 1989). Instruments were attached to the pelage above the shoulders with marine epoxy. Nearly all seals were weighed before going to sea and on their return.

Generalizations

The data support several generalizations about diving in elephant seals. All northern elephant seals of both sexes and all age groups, from weanlings on their first pelagic trip to sea to adults, exhibit a diving pattern characterized by (1) continuous diving during all periods at sea; (2) deep diving, relative to other pinnipeds and cetacea; (3) long-duration dives, relative to other diving mammals, interspersed with brief surface intervals (about 1/10 the

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mean dive duration) and a few unpredictable surface intervals longer than 10 minutes; and (4) submergence for the majority of the time (83–92%) spent at sea. Data supporting these generalizations are summarized below.

Variation in Dive Pattern

Early Development

First Trip to Sea

On the very first trip to sea when the animals are only 3½ months old, both the depth and duration of dives are great, relative to other diving mammals. Two seals, a male and a female, exhibited mean dive durations of 9.5 and 10.5 minutes with maximum dive durations of 18 and 22 minutes, respectively. The one animal, on whom we measured dive depth over a 30-day period, exhibited a mean dive depth of 206 m and a maximum dive depth to 553 m. These figures are impressive, for they exceed the adult diving performance of most other pinnipeds that have been studied. Further details on the first diving records of these young seals are found in P. H. Thorson and B. J. Le Boeuf (this volume).

Juvenile Diving

Two-year-olds of both sexes dived to the same mean depths, in excess of 400 m, and remained submerged as long as adult males and females, a mean of 18 minutes or more (fig. 13.2). That is, by the end of the fourth trip to sea, when juveniles average 270 ± 26 kg, the adult pattern is essentially set, and 2-year-olds are accomplished divers. This has important implications for conducting studies of diving in the laboratory. It is feasible to transport juveniles but considerably more difficult to transport adult females whose mean nonpregnant weight is 395 ± 19 kg.

Age/Mass Effects

Dive Duration

One expects that dive duration will scale approximately linearly with mass because dive duration is limited by oxygen stores (Scholander 1940; Calder 1984). In seals, oxygen stores are determined mainly by blood volume and hemoglobin and myoglobin concentrations. Blood volume (V_b ) is linearly proportional to body mass (M_b ), V_b = M_b^1.0 , and the relationship between mass and metabolic rate (MR), which determines how quickly the oxygen stores are used, is MR = M_b^.75 . In elephant seals, hemoglobin and myoglobin concentrations increase with age (Thorson and Le Boeuf, this volume), and there is a high and positive correlation between age and mass (fig. 13.3; Deutsch et al., this volume; Clinton, this volume). Indeed, one expects dive duration to scale to both age and mass in postbreeding females because of the close relationship between these two variables (fig. 13.3).

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Fig. 13.2
Mean dive duration and mean dive depth of free-ranging northern elephant seals
as a function of age.

Fig. 13.3
The regression of mass on age in 23 postbreeding, nonpregnant female northern
elephant seals.

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Fig. 13.4
Mean dive duration as a function of mass in 23 postbreeding, nonpregnant female
northern elephant seals.

The relationship between dive duration and mass is positive in postbreeding females, but the association is not strong (fig. 13.4). If one adds weanlings, juveniles, pregnant females, and males to the picture (fig. 13.5), predictability worsens at the upper end. Indeed, it is not clear whether it is males or pregnant females that are outstanding. The long dives of pregnant females contradict the logic that the fetus parasitizes the stores of the mother, causing a shortening of dives. Whatever the explanation, the data indicate that mass predicts dive duration up to a point, but other factors besides mass and oxygen carrying capacity affect the duration of dives. Dive duration does not scale in a simple linear way with mass.

Dive Depth

Mean dive depth does not vary systematically with mass (fig. 13.6), and by association, with age (fig. 13.3), in nonpregnant females. Similarly, there is no relationship between mean dive depth and age across animals from all age categories (fig. 13.7).

Reproductive Condition

Pregnant females, whose diving behavior was recorded during the third trimester of pregnancy, had mean dive durations 39% longer than nonpregnant females (table 13.2). Each one of them had maximum dive durations in excess of 1 hour. Dives lasting more than 1 hour were never observed in

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Fig. 13.5
Mean dive duration as a function of mass in northern elephant seals ranging in age
from weanlings to adults of both sexes.

Fig. 13.6
Mean dive depth of 23 postbreeding, nonpregnant female northern elephant seals as
a function of their mass.

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Fig. 13.7
Mean dive depth as a function of age in northern elephant seals.

the 26 nonpregnant females that were recorded. Despite the longer dives, the surface intervals of pregnant females were no longer than those of nonpregnant females. Moreover, pregnant females exhibited slower dive rates and spent less time at the surface than nonpregnant females. These differences were even more prominent in three females that were recorded in both conditions. Differences of similar magnitude have been observed in southern elephant seals, M. leonina (Hindell 1990; Hindell et al. 1992; Slip, Hindell, and Burton, this volume).

Why do pregnant females dive longer than nonpregnant females? One reason might be that it takes pregnant females longer to reach the same depths, the deep waters where prey are located. Pregnant females have a greater lipid composition than nonpregnant females (36% vs. 24%, on average), which makes them more buoyant; increased buoyancy implies greater diving effort and time to reach depths. This is suggested by M. A. Hindell's (1990) observation that pregnant and nonpregnant females do not differ in the duration spent at the bottom of dives; the differences are in descent and ascent duration.

The proximate mechanisms enabling pregnant females to dive longer than nonpregnant females must be either greater oxygen availability or reduced demand for oxygen. Pregnant female mammals are said to have about 40% more blood than nonpregnant females; however, it is not clear how much of this extra blood is involved in nurturing the developing fetus. Alternatively, pregnant females may have lower metabolic rates than non-

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TABLE 13.2 Key statistics of the dive patterns of postbreeding females (nonpregnant), pregnant females, and males, 5 to 10 years of age.
	Mean dives/hour	Mean % time on surface	Maximum depth (m)	Mean depth (m)	Maximum duration (min)	Mean duration (min)	Mean SI (min)
Postbreeding females (N = 10)^a	2.6	9.7	1273	509 ± 147	47.5	20.8 ± 4.1	2.1 ± 0.5
Pregnant females (N = 5)	2.0	7.7	1181	473 ± 151	67.9	27.7 ± 6.4	2.1 ± 0.6
Adult males (N = 5)	2.5	13.5	1503	330 ± 127	66.7	21.2 ± 4.6	2.7 ± 0.9
^a For comparability, only the records obtained with Hill TDRs from Wildlife Computers are included.

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pregnant females. A preliminary observation consistent with this statement is that the horizontal swim speed of females during migration is significantly slower during the third trimester of pregnancy than when they are not pregnant (51.5 km vs. 75.0 km per day; t = 2.62, df = 2, p < .05). D. Renouf et al. (1991) report that gray seals, Halichoerus grypus , have lower resting metabolic rates when pregnant than when nonpregnant.

It is also possible that the differences in dive durations of pregnant and nonpregnant females reflect a change in prey or its availability (Lyons 1991). Pregnant females migrate farther away from the rookery than nonpregnant females, but much of the same route is traveled (see below). The diving records under both conditions are similar and offer no obvious evidence for this hypothesis.

Sex

Do the sexes differ with respect to diving pattern and migratory path? The great sexual dimorphism in this species makes this an interesting question: What are the bioenergetic consequences of extreme sexual dimorphism in size, especially with respect to foraging behavior?

Dive Pattern

Males and females have similar dive patterns, except that males dive approximately 180 m less deep than nonpregnant females, on average (table 13.2, fig. 13.2; see also DeLong and Stewart 1991). The maximum depths we have recorded are 1,503 m for a 5-year-old subadult male and 1,273 m for a 4-year-old female.

The shallower dive pattern of males relative to females is due mainly to a single sex difference in diving pattern (Le Boeuf et al. 1993). The most common dive type in the records of females appears to serve pelagic foraging (Le Boeuf et al. 1988, 1992); these dives are characterized by direct descent to depth, with several vertical excursions at the bottom of the dive, followed by direct ascent to the surface. Males exhibit these dives, too, but their most frequent dives are flat bottomed with a mean depth of 331 ± 243 m. Females do not exhibit these dives or do so only rarely. The dive shapes and the location in which they occur suggest that males are pursuing benthic prey on the edge of the continental shelf or on seamounts or guyots. Because males are much larger than females (Deutsch et al., this volume), their daily energy requirements are approximately three times greater than those of females. Benthic prey might provide the additional energy a male requires, or it might be that it is less costly for males to catch these prey. This hypothesis is consistent with reports that males but not females feed on cyclostomes and elasmobranchs (Condit and Le Boeuf 1984; Antonelis et al., this volume). What prevents females from doing the same thing? Two reasons come to mind. They may not be large enough to capture benthic

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prey, or it may be more costly for females to migrate to the places where these benthic prey are located.

Migratory Routes

To determine migratory routes and possible foraging areas, we attached geographic location, time-depth recorders (GLTDRs) to 21 animals: 9 postbreeding, nonpregnant females; 5 postmolt, pregnant females (3 of which were also recorded as postbreeding females), 6 males (3 adults of age 10 or over and 3 subadult males, 5–6 years of age), and 1 juvenile female, 1.4 years of age, on its third trip to sea. A photocell in each GLTDR recorded light levels, providing estimates of the time of sunrise and sunset as the animal traveled across latitudes and longitudes; from these data, an algorithm calculated geolocation (DeLong, Stewart, and Hill 1992; Hill, this volume). Geolocation estimates of latitude were adjusted in accordance with surface temperatures recorded by the GLTDR matched to mean sea surface temperature locations compiled semimonthly from satellites by the National Meteorological Center of the National Weather Service (Ashville, N.C.); that is, no geolocation estimate was accepted unless it was consistent with the surface temperature in the area. Recent validation experiments of geolocation from GLTDRs against a ship's Global Positioning System (GPS) off the coast of British Columbia, Canada, in June and July 1992 indicate that light-level estimates have a southerly bias (S. Blackwell and B. Le Boeuf, unpubl. data).

Despite the error associated with light-level estimates of location (Hill, this volume), preliminary data reveal that both adult males and postbreeding females migrated long distances and the migratory paths of the sexes overlapped in the eastern Pacific, especially along the coast up to about 58°N Lat. (fig. 13.8). The most northerly and most westerly migrations were undertaken by males. One adult male traveled as far as the eastern Aleutian Islands in southern Alaska, a round-trip migration of approximately 7,500 km; two others remained near the coast and went no farther north than about 49 degrees, near the state of Washington. Postbreeding females moved in a broad expanse of the eastern Pacific, from near the coastline to as far west as 150°W Long. The longest round-trip migrations of postbreeding females were about 4,866 km. The juvenile female traveled far north into the Gulf of Alaska, exceeding the distances traveled by most postbreeding, adult females.

Pregnant females had minimum round-trip migrations of about 3,900 to 6,800 km. Three of them, recorded when pregnant as well as nonpregnant, took similar routes under both conditions (fig. 13.9). The distance traveled during these biannual migrations was always less during the nonpregnant period.

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Fig. 13.8
Migratory destination or location at the end of recording of 6 breeding-age males
(open circles), 9 postbreeding females (vertically hatched circles), and 1 juvenile
female (J) that went to sea at Año Nuevo, California. The migratory paths of
males are shown in the unhatched area; those of females are shown by
horizontal hatching. The ultimate locations were derived from tracts plotted
every two days as illustrated in figure 13.9.

The data suggest several points that merit further study:

1. Geolocation by light levels—corrected with sea surface temperature—is not accurate enough to place a seal in a specific location, such as correlating location with bathymetry, but it is sufficient for showing general migration direction and distance.

2. The data presented here, along with more recent findings (Le Boeuf et al. 1993) and reports of other investigators (DeLong and Stewart 1991; DeLong, Stewart, and Hill 1992; Stewart and DeLong, this volume), provide evidence of sex differences in foraging behavior. Adult males migrate to the northern edge of the North Pacific from the state of Washington west to the eastern Aleutians; they move directly to a foraging area, as defined by concentrated diving in this vicinity for up to two months. The migrations of adult females are more removed from the continental margins and are characterized by steady movement in the open ocean in the general range of 44–52°N lat.; females do not forage in narrowly focused areas but forage steadily en route. Differences in the frequency of dive types suggest that

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Fig. 13.9
Similarity in the migratory paths of females when pregnant (third trimester) and
not pregnant (postbreeding period at sea). The pregnant period included the
months November, December, and mid-January; the nonpregnant period
included March, April, and mid-May. The records of pregnant females begin at
roughly the furthest point from Año Nuevo; during the postbreeding period,
the records begin at Año Nuevo and end at or near Año Nuevo. A third female,
"B857," followed a similar route during both trips to sea; her record is not
shown because it overlapped with that of the female "Renee."

males are diving in areas where they can reach the bottom and that females are diving in the water column in deeper water (Le Boeuf et al. 1993); however, the geolocation data available are too imprecise to test this hypothesis.

3. Adult seals from Año Nuevo migrate to the same general areas as adult seals from San Miguel Island, located 450 km south of Año Nuevo (DeLong and Stewart 1991; DeLong, Stewart, and Hill 1992; Stewart and DeLong, this volume; Le Boeuf et al. 1993). This suggests that seals from other rookeries in Mexico and California might do the same. This would make for considerable mixing of animals during the foraging periods and would make reassortment on their return to their respective rookeries all the more interesting.

Homing and Translocation

The study of elephant seal diving has revealed a diving pattern that is unusual and difficult to explain with current theory that accounts well for the

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diving behavior of the shallower-diving sea lions and fur seals (Le Boeuf et al. 1988). How, for example, can elephant seals spend so little time on the surface following dives lasting over 1 hour? The diving pattern of elephant seals is evidently adapted to spending much of the year at sea and most of time at sea underwater. This regimen, however, is a problem for an investigator who wants to understand the physiology of diving by conducting short-term experiments of the type that have proven so successful with Weddell seals, Leptonychotes weddelli (Kooyman 1981; Guppy et al. 1986; Qvist et al. 1986; Hill et al. 1987). With this practical application in mind, my graduate students and I set out to determine if elephant seals translocated from Año Nuevo would home quickly and reliably.

Recent studies conducted with Guy Oliver, Pat Morris, and Phil Thorson showed that 43 of 45 juveniles, 1½- to 2-year-olds of both sexes, translocated from the Año Nuevo rookery in the spring when molting and in the fall when resting to release sites on a beach or at sea up to 70 km away returned "home" to the rookery. Most of the translocated animals wore radio transmitters that facilitated reidentification and determination of the time of return; the two exceptional animals bore no radios and may have returned but were overlooked. Nearly all returnees were back on the rookery within 1 to 7 days.

Sixteen of the translocated animals bore time-depth recorders. When these animals were released in a place where they had to traverse deep water to return to the rookery, a deep diving pattern indistinguishable from free-ranging diving was observed. We have subsequently used this paradigm to conduct doubly labeled water studies (D. Costa and B. J. Le Boeuf, unpubl. data), measure swim speeds (P. Thorson, G. Kooyman, and B. J. Le Boeuf, unpubl. data). This paradigm should facilitate short-term studies of diving, especially physiological studies of diving requiring completion in a day or two.

Conclusion

The study of free-ranging diving of marine mammals is developing fast. At the marine mammal conference in Chicago in December 1991, there were 24 talks dealing with 18 species that were instrumented with radio transmitters, satellite tags, or time-depth recorders or that were tracked with sonar: 11 pinnipeds, 6 cetacea, and the manatee. Increasingly sophisticated microcomputer time-depth recorders with more channels and larger memories are generating a wealth of detail about the diving behavior of pinnipeds. In the near future, it is anticipated that GPS devices will be attached to seals, permitting precise location of the animals during their migrations. This technology is now being transferred to cetacea.

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The incoming data on elephant seals show that variation in dive pattern with age, sex, and reproductive condition as well as individual differences in foraging location can be substantial. Parametric studies taking this variation into consideration will be necessary to obtain a thorough understanding of the marine aspects of an animal's natural history. Satellite monitoring of the migratory path and diving pattern of juveniles during the first trip to sea may elucidate the causes of high at-sea mortality.

We are on the verge of learning much about the free-ranging dive pattern of elephant seals, as well as other diving mammals, and about diving biology in general. Studies of the underlying mechanics of the diving pattern of diving mammals is a fertile field for future investigation.

Acknowledgments

Many collaborators played key roles in the studies summarized here, and they have graciously allowed me to refer to unpublished data. These include Dan Costa, Pat Morris, Phil Thorson, Dan Crocker, Yasuhiko Naito, Tomohiro Asaga, Maria Kretzman, Jeanine Williams, Guy Oliver, and many others. The research reported here was funded by grants from the National Science Foundation, the Minerals Management Service, and the G. MacGowan Trust Fund.

References

Calder, William A., III. 1984. Size, Function, and Life History . Cambridge: Harvard University Press.

Condit, R., and B. J. Le Boeuf. 1984. Feeding habits and feeding grounds of the northern elephant seal. Journal of Mammalogy 65: 281–290.

DeLong, R. L., and B. S. Stewart. 1991. Diving patterns of northern elephant seal bulls. Marine Mammal Science 7: 369–384.

DeLong, R. L., B. S. Stewart, and R. D. Hill. 1992. Documenting migrations of northern elephant seals using day length. Marine Mammal Science 8: 155–159.

Guppy, M., R. D. Hill, R. C. Schneider, J. Qvist, G. G. Liggins, W. M. Zapol, and P. W. Hochachka. 1986. Microcomputer-assisted metabolic studies of voluntary diving of Weddell seals. American Journal of Physiology 250: R175–187.

Hill, R. D., R. C. Schneider, G. C. Liggins, A. H. Schuette, R. L. Elliott, M. Guppy, P. W. Hochachka, J. Qvist, K. J. Falke, and W. M. Zapol. 1987. Heart rate and body temperature during free diving of Weddell seals. American Journal of Physiology 253: R344–351.

Hindell, M. 1990. Population dynamics and diving behaviour of southern elephant seals. Ph.D. dissertation, University of Queensland, Australia.

Hindell, M. A., D. J. Slip, H. R. Burton, and M. M. Bryden. 1992. Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina ). Canadian Journal of Zoology 70: 370–379.

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Kooyman, G. L. 1981. Weddell Seal: Consummate Diver . Cambridge: Cambridge University Press.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, G. L. Kooyman, and R. W. Davis. 1986. Pattern and depth of dives in northern elephant seals, Mirounga angustirostris. Journal of Zoology 208: 1–7.

Le Boeuf, B. J., D. E. Crocker, S. B. Blackwell, P. A. Morris, and P. H. Thorson. 1993. Sex differences in diving and foraging behavior of northern elephant seals. In Marine Mammals: Advances in Behavioural and Population Biology , ed. I. Boyd, 149–178. Symposia of the Zoological Society of London no. 66. London: Oxford University Press.

Le Boeuf, B. J., Y. Naito, T. Asaga, D. Crocker, and D. P. Costa. 1992. Swim speed in a female northern elephant seal: Metabolic and foraging implications. Canadian Journal of Zoology 70: 786–795.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Canadian Journal of Zoology 67: 2514–2519.

Lyons, K. J. 1991. Variation in feeding behavior of female sea otters, Enhydra lutris , between individuals and with reproductive conditions. Ph.D. dissertation, University of California, Santa Cruz.

Qvist, J., R. D. Hill, R. C. Schneider, K. J. Falke, G. C. Liggins, M. Guppy, R. C. Elliot, P. W. Hochachka, and W. M. Zapol. 1986. Hemoglobin concentrations and blood gas tensions of free-diving Weddell seals. Journal of Applied Physiology 61: 1560–1569.

Renouf, D., R. P. Gales, E. Noseworthy, and D. Rosen. 1991. Longitudinal studies of seasonal variations in phocid bioenergetics. Ninth Biennial Conference on the Biology of Marine Mammals, December 5–9, 1991, Chicago, Ill.

Scholander, P. F. 1940. Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter Norske Videnskaps-Academie, Oslo 22: 1–131.

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Fourteen—
Diving Behavior of Southern Elephant Seals from Macquarie Island:
An Overview

David J. Slip, Mark A. Hindell, and Harry R. Burton

ABSTRACT. Results from 84 deployments of time-depth recorders on southern elephant seals, Mirounga leonina , at Macquarie Island are discussed. With loss and failure of instruments, data were collected from 31 seals: 14 postmolt females, 9 postbreeding females, 3 postmolt males, and 5 postbreeding males.

Water temperature data, also collected by the diving instruments, indicated that the major foraging areas of adult elephant seals from Macquarie Island were located in Antarctic waters and that males used areas over the Antarctic continental shelf, while females tended to inhabit deeper, offshore waters. Some individuals of either sex, however, spent the majority of their time in warmer waters associated with the Antarctic Polar Front or over the northern Campbell Plateau. Approximately 90% of the time at sea was spent submerged, with times on the surface generally less than 10 minutes.

Five characteristic dive types were identified, the most common of which were type 1 and type 2 dives. Both types are characterized by rapid descent to a depth followed by a protracted time at that depth interspersed with a number of small "wiggles," in turn followed by a rapid ascent to the surface. Type 1 dives exhibited marked diurnal variation, while type 2 dives showed no such variation and were usually in long sequences of very similar depths. We interpret type 1 as pelagic foraging dives and type 2 as benthic foraging dives. Type 2 dives were almost exclusively made by males while over the continental shelf. Type 1 dives were made by all animals.

The majority of dives made by southern elephant seals are characteristically deep (maximum depth = 1,430 m) and long (maximum duration = 120 min.). Estimated aerobic dive limits (ADL) were rarely exceeded by males or postbreeding females, but 44% of all dives made by postmolt (and, therefore, gestating) females exceeded ADL. Females in the last two trimesters of gestation performed the longest dives and most often exceeded ADL, suggesting that the estimated ADL is being underestimated in these animals and that these animals are making physiological adjustments that increase oxygen stores or reduce oxygen consumption.

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Although much is known of the onshore behavior of the southern elephant seal (e.g., Carrick Csordas, and Ingham 1962; Ling and Bryden 1981; Hindell and Burton 1988), it is only recently that their aquatic behavior has come under investigation. Studies of diving in free-ranging seals are becoming increasingly common with the development of more sophisticated technology (e.g., Gentry and Kooyman 1986; Le Boeuf et al. 1988, 1989; Boyd and Arnbom 1991; Hindell, Burton, and Slip 1991; Hindell, Slip, and Burton 1991; Hindell et al. 1992). Studies such as these describe diving in relation to potential prey distribution, foraging range and movement patterns, and the diving performance in terms of physiological implications.

The southern elephant seal is a major predator of squid and fish in the Southern Ocean ecosystem (Laws 1977). Nevertheless, the diet of the southern elephant seal is one of the least known of the marine mammals of the Southern Ocean, with studies based on stomach samples collected while seals were ashore for their annual breeding or molting haul-outs (Laws 1977; Clarke and MacLeod 1982; Green and Williams 1986). Difficulties in collecting dietary samples from southern elephant seals near their main foraging areas prevent us from constructing a complete picture of the feeding ecology of one of the major vertebrate consumers of the Southern Ocean.

The annual cycle of adult southern elephant seals has two distinct aquatic phases: one postbreeding and one postmolt. Females come ashore to breed on subantarctic islands between September and November, whereas breeding males are ashore between August and December (Ling and Bryden 1981; Hindell and Burton 1988). After giving birth and weaning a pup, females spend about 10 weeks at sea feeding before returning to shore to molt in January and February. Adult males spend 12 to 14 weeks at sea feeding before returning to molt in mid-March. The molting process takes about 4 weeks, after which the seals return to sea until the following breeding season. By deploying time-depth recorders (TDRs) on adult male and female southern elephant seals as they leave Macquarie Island (lat. 54°35¢ S, long. 158°55¢ E) for the postbreeding and postmolt period at sea, we have been able to gain insight into their diving behavior that has added to out undertanding of their potential diet, foraging behavior, and movement patterns, all of which are crucial to understanding the role of the southern elephant seal in the Southern Ocean ecosystem. These studies have also raised some interesting questions regarding mammalian diving physiology.

In this chapter, we present an overview of our current knowledge of the diving behavior of the southern elephant seal at Macquarie Island with respect to their movement patterns, diving patterns, and physiology.

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Deployment and Recovery of Recorders

Time-depth recorders from Wildlife Computers were deployed on adult male and female southern elephant seals at Macquarie Island in 1988 and 1990. These units were microprocessor-controlled recording units equipped with pressure transducer, temperature probe, and internal clock. In addition, 50% of the units deployed in 1990 were equipped with a light-sensing geolocation option (DeLong Stewart, and Hill 1989). The movements of two adult males were determined in 1990 and 1991 using platform transmitter terminals and the Argos satellite-based location and data collection system. Seals were sedated using a combination of ketamine hydrochloride and either diazepam or xylazine (see Woods, Hindell, and Slip 1989). The units were attached to the seals using quick-setting epoxy (Araldite K268 road-marker adhesive, Ciba-Geigy), and a radio transmitter was attached to the TDR to facilitate the recovery of the units. Each complete package weighed approximately 3 kg (see fig. 14.1).

Eighty-four TDRs have been deployed on southern elephant seals at Macquarie Island. In 1988, 6 and 13 units were deployed on postmolt males and females, respectively; 10 units were deployed on postbreeding males; and 10 were deployed on postbreeding females. In 1990, 13 and 12 units were deployed on postmolt males and females, respectively; 10 units were deployed on postbreeding males; and 10 were deployed on postbreeding females. The TDRs were programmed to record depth every 30 seconds and temperature every 300 seconds, a sampling protocol that allowed for up to 80 days of continuous recording. The units that were deployed on postmolt animals were programmed to begin recording at different intervals to cover the entire period the seals were at sea. Recorders began sampling in February, April, or June. Postbreeding females were at sea for about 70 days and postbreeding males for about 100 days, so recording began as the animals left Macquarie Island.

The recovery rate of recorders varied between sexes and time of year. The recovery rate was slightly higher for females than for males. Return rates were 68% for postmolt females and 55% for postbreeding females. For males, return rates were 47% and 40% for the postmolt and postbreeding periods, respectively. In addition, electronic failures reduced the number of successful recoveries to 16% and 56% for postmolt males and females and 25% and 45% for postbreeding males and females.

Location of Animals

The location of the foraging areas of southern elephant seals was initially estimated by examining the sea surface temperatures recorded for each

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Image not available.

Fig. 14.1
Male elephant seal with time-depth recorder inshore at Macquarie Island.
Photograph by David J. Slip.

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animal. These temperatures provided sufficient resolution to distinguish three general regions: cold Antarctic waters with sea surface temperatures less than 0°C, warmer subantarctic waters with sea surface temperatures greater than 4°C, and a midregion that we term "convergence" waters which corresponds to the region around the Antarctic Polar Front (APF), where sea surface temperatures are above 0°C but generally do not exceed 4°C.

To estimate the areas of the ocean where the seals were located with greater resolution, the daily sea temperature/depth profiles were examined for each animal and matched with detailed oceanographic data for the Southern Ocean (Gordon and Molinelli 1982). Full details of this technique for estimating foraging areas are given in M. A. Hindell, H. R. Burton, and D. J. Slip (1991). The accuracy of this technique is entirely dependent on the accuracy of the oceanographic data and thus may be subject to some error.

Although the estimated foraging areas were different for males and females, the major foraging areas of adult southern elephant seals were located in the cold Antarctic waters, with other areas located along the APF, and in warmer subantarctic waters north to about 50°S. All five postbreeding males showed temperature/depth profiles consistent with being in Antarctic waters. Comparisons with oceanographic data identified three regions of the Southern Ocean, all close to the Antarctic continent (fig. 14.2a).

Postmolt males appear to have three distinct foraging areas: two close to the Antarctic continent, and one in the warmer subantarctic waters close to Campbell Island (fig. 14.2b). The estimated foraging areas of adult males close to the Antarctic coast and the area close to Campbell Island were over shelf waters with depths of between 500 and 1,000 m.

The foraging areas of postbreeding females were either in Antarctic waters or close to the APF. The seven females that moved south to colder waters had temperature/depth profiles consistent with three discrete areas located close to the Antarctic coast but farther north than the areas estimated for adult males (fig. 14.2a). One of these females remained in Antarctic waters for about four weeks before it moved north and spent about three weeks in the warmer waters around the APF. Only two postbreeding females did not move into Antarctic waters, and the temperature/depth profiles for these animals were consistent with the oceanographic profiles of an area around the APF (fig. 14.2a). The temperature/depth profiles for postmolt females were consistent with three areas in Antarctic waters and one area around the APF (fig. 14.2b). The three areas in Antarctic waters were to the north of the estimated locations of the postmolt males, in water of depths greater than 1,000 m. Nine postmolt females had profiles consistent with these areas of Antarctic waters. Two postmolt females had temperature/depth profiles consistent with being north of the APF, one had

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Fig. 14.2
Location of foraging areas of the southern elephant seal as determined by water temperature data and satellite telemetry
(Slip, unpubl. data) for (A) postbreeding males, December to March (dark hatching), and postbreeding females, November
to January (light hatching); and (B) postmolt males, March to August (dark hatching), and postmolt females, February
to September (light hatching).

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profiles consistent with waters to the south of the APF, and two had profiles consistent with being close to the APF, at times crossing it.

Subsequent satellite telemetry data from two male southern elephant seals are consistent with the estimations made from seawater temperatures, with one animal located in the Ross Sea and another located to the north-west of Campbell Island (unpubl. data). Preliminary analyses of geolocation data for males and females are also consistent with the estimations made from seawater temperature.

Dive Patterns

All seals began diving as soon as they left Macquarie Island and dived almost continually throughout the recording period. The shelf around Macquarie Island extends only a few kilometers out to sea, so seals could begin deep diving within a few hours of leaving the island.

Approximately 90% of total time at sea was spent diving, and a dive rate of about 2.5 dives per hour was maintained throughout the entire period at sea. Approximately 99% of surface times between dives were of less than 10 minutes duration, with means ranging from 2.1 to 4.1 minutes for individual seals. Surface intervals longer than 10 minutes were defined as extended surface intervals (Le Boeuf et al. 1988) and generally occurred at higher frequencies at about the time the seals reached their foraging grounds. Extended surface intervals were more common at higher latitudes.

All seals that moved into Antarctic waters, both males and females, were recorded to haul out of the water for intervals of up to six hours two to three weeks after leaving Macquarie Island. It seems likely that these haul-outs were made onto ice floes, as few beaches are available in the areas indicated by the temperature profiles. Most of these seals made three to eight short haul-outs (usually less than three hours) over the recording period.

Characterization of Dive Types

Six characteristic dive types and the general form of the dive profile have been identified by principal component analysis (see Hindell, Slip, and Burton 1991). Typical examples of five of these dive types are illustrated in figure 14.3 (type 5 dives are rare; see below). Within these six dive types, there are two discrete groups of dives: those with more than one minute at the maximum depth, which were interpreted as foraging dives (types 1 and 2) and were the most common, constituting about 75% and 78% of total time at sea, respectively, for males and females, and those with less than one minute at the maximum depth, which were interpreted as nonforaging dives (types 3, 4, 5, and 6). The high proportion of type 1 and type 2 dives

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Fig. 14.3
Examples of dive types of the southern elephant seal.

is consistent with foraging dives, as elephant seals build up fat reserves quickly while at sea for reproduction and molting purposes.

Type 1 Dives

These dives were characterized by a rapid descent, followed by a period at the base of the dive containing shorter ascents and descents or "wiggles,"

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prior to a rapid ascent to the surface (fig. 14.3). The depth and duration of these dives were variable, but they were generally of depths ranging from 300 m to 700 m (mean = 426 ± 177 m), with a mean of 11.3 ± 4.7 minutes between the end of descent and the beginning of ascent. Males and females spent different proportions of total time at sea on type 1 dives (35.9% for males, 77.6% for females). Females showed a marked diurnal pattern in the maximum depth, with type 1 dives becoming 200 to 400 m shallower at night. In males, a less pronounced diurnal pattern of depth occurred when the seals were close to Macquarie Island, but there was little evidence of any pattern of depth in these dives as the seals moved to higher latitudes or when they were over the Campbell Plateau.

We interpret these dives as pelagic foraging dives while the seals were foraging for prey characterized by diurnal vertical migrations. These dives are analagous to the Type D dives described for the northern elephant seal (Le Boeuf et al. 1988).

Type 2 Dives

These are characterized by a rapid descent followed by an almost flat period at depth with relatively few, short "wiggles" and a rapid ascent to the surface. These dives generally occur in bouts lasting about 18 hours, with little more than 10 to 20 m variation in depth between consecutive dives. Males spent 39% of total time at sea undertaking type 2 dives, but this type of dive was rarely seen in females, constituting only 0.5% of their total time at sea.

We interpret these dives as benthic foraging dives. In support of this interpretation, these dives were generally of depths ranging from 450 to 550 m (mean = 486 ± 83 m), with a mean of 13.9 ± 5.1 minutes spent at the bottom of the dive, and occurred over the Antarctic continental shelf and over the Campbell Plateau where water depths are around 500 m. When type 1 and type 2 dives occurred in the same area, type 1 dives were never deeper than type 2 dives, and when a series of type 2 dives occurred, no deeper dives were ever seen within the series, suggesting that the ocean floor limited the depth to which seals could dive.

Type 3 Dives

These are characterized by a short, rapid period of descent to a depth usually greater than 200 m, followed by a longer period of slow descent that occupied most of the dive, then a rapid ascent to the surface. These dives generally occurred in bouts of at least two dives and accounted for 4% of time at sea. The shape of these dives is consistent with the seals conserving energy by resting or sleeping, with the slower phase of descent resulting

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from a cessation of active swimming. Northern elephant seals are also believed to sleep underwater (Le Boeuf et al. 1988).

When seals were located in the more northerly areas of their range, a distinct pattern emerged: type 3 dives occurred in the early hours of the morning. This pattern was less pronounced at higher latitudes. There was considerable individual variation in the pattern of these dives, with some seals exhibiting a fairly regular 24-hour cycle over several weeks, while others were more erratic and did not undertake type 3 dives every day.

Type 4 Dives

These dives are a simple parabolic shape. They occurred predominantly in the first two to three weeks after the animals left Macquarie Island and appeared again as the animals approached Macquarie Island. This suggests that the function of these dives may simply be travel, as apparent velocities of between 80 and 240 km per day have been recorded by satellite for male southern elephant seals over the first three weeks after leaving Macquarie Island (unpubl. data). This type of dive had a mean depth of 343 ± 133 m and a mean duration of 20.4 ± 6.8 minutes. Seals spent 1.9% of total time at sea undertaking these dives. Why elephant seals would dive so deeply with no purpose other than travel is unclear. It may be that it is a predator avoidance strategy. Killer whales are the major predator of elephant seals (although sharks may also be important in the northern part of their range), and it may be that by maximizing the time they spend at depth, elephant seals reduce the risk of encountering these animals. There may also be an exploratory nature to these dives, and if prey are encountered, the animal may take advantage of this and forage. This interpretation is supported by the occurrence of, generally, type 4 dives in series that were sometimes punctuated by type 1 foraging dives. The occurrence of composite dives (see type 6 dives below) suggests that seals can change from one type of dive to another in mid-dive.

Type 5 Dives

These are short, shallow dives of less than 1.5 minute duration and are rare, accounting for 0.4% of total time at sea. The purpose of these dives is unclear. It may be that they are an artifact of the sampling protocol.

Type 6 Dives

These dives are quite variable in form, including simple spike dives and dives that may be composite dives, and do not fit into the above categories. They are the most common group of nonforaging dives, accounting for 7.2% of total time at sea. Type 6 dives had a mean depth of 485 ± 249 m and a mean duration of 19.5 ± 6.7 minutes. The large variance associated

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with mean depth was accounted for by the very deep dives that were usually simple spikes.

These dives probably have several functions, including exploration and escape from predators. A composite dive might occur if a foraging dive is interrupted by the threat of a predator or if prey is discovered during a travel or exploratory dive.

Maximum Depths and Durations

There was considerable individual variation in mean depth of dive, ranging from 269 ± 159 m to 589 ± 175 m, and in mean duration of dive, ranging from 16.0 ± 7.9 minutes to 36.9 ± 11.5 minutes (table 14.1).

The maximum dive depth recorded was 1,430 m by a postbreeding female (table 14.1). Although dives to such depths are relatively uncommon, constituting less than 1% of all dives, most seals undertook some very deep dives; 87% of females and 63% of males recorded dives of over 900 m in depth. This difference between the sexes might be a result of males foraging in shallower waters than females. The very deep dives were type 6 dives, generally a simple deep spike. These can occur in the middle of a set of type 1 or type 4 dives and are generally single deep dives. However, deep dives of over 1,000 m can occasionally occur in bouts of 3 to 10 dives over several hours. The functions of these deep dives are unclear, although possible explanations include avoidance of predators, exploration, or chasing prey.

Most seals undertook at least some dives with duration time greater than 50 minutes, and the longest dive duration recorded was 120 minutes by a postbreeding female (table 14.1). The longest male dive was 88.5 minutes. A full description of the 120-minute dive is given in Hindell et al. (1992). Long duration dives were generally type 6 composite dives. Their function might have been, for example, to escape an attack by a predator following a bout of foraging. These long dives do not appear in consistent patterns, occurring at any time during the course of a bout of more moderate dives. The only other phocid known to dive for as long or as deep is the northern elephant seal (Le Boeuf et al. 1988, 1989).

Given the similarities in morphology and life cycles of the two species of elephant seal, it is hardly surprising that there are many similarities in diving behavior between the southern elephant seal and its northern cogenitor. Adult southern elephant seals show a general pattern of continuous, prolonged deep diving. On leaving Macquarie Island, type 4 or traveling dives were common, interspersed with some type 1 pelagic foraging dives and occasional type 3 resting dives. After two to three weeks, the animals appeared to reach their foraging grounds, and females settled into a pattern

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TABLE 14.1 Mean depth and duration of dives for each seal.
Seal	Sex/ Deployment	Mass (kg)	Depth (m)		Duration (min)		N
Seal	Sex/ Deployment	Mass (kg)	M ± SD	Max.	M ± SD	Max.	N
857	PMF	402	476 ± 197	1056	29.1 ± 8.4	58.6	1,881
1419	PMF	362	552 ± 207	1022	30.9 ± 8.0	78.5	2,836
1423	PMF	342	432 ± 151	1256	33.7 ± 13.6	120.0	1,362
1432	PMF	320	269 ± 159	856	16.0 ± 7.9	54.5	4,179
1440	PMF	422	396 ± 212	968	36.9 ± 11.5	78.5	2,386
3178	PMF	333	573 ± 195	1134	25.7 ± 6.6	52.0	3,927
3184	PMF	387	355 ± 157	758	28.8 ± 9.0	76.0	3,512
3186	PMF	278	446 ± 143	1044	20.1 ± 5.5	68.0	4,920
3187	PMF	304	380 ± 147	1158	21.7 ± 6.7	53.5	4,431
3189	PMF	282	296 ± 150	812	18.3 ± 7.7	55.5	5,071
3191	PMF	339	425 ± 170	1430	19.9 ± 4.9	56.5	2,577
3193	PMF	400	391 ± 176	928	28.9 ± 9.8	79.5	2,455
3196	PMF	430	456 ± 174	938	32.2 ± 9.1	98.5	2,554
3200	PMF	392	357 ± 119	1046	35.4 ± 8.2	66.0	2,353
905	PBF	295	382 ± 166	991	21.4 ± 6.6	66.0	4,458
1918	PBF	422	589 ± 166	1152	21.4 ± 6.6	53.0	4,554
1930	PBF	462	384 ± 166	911	21.3 ± 5.3	50.0	4,232
1938	PBF	366	490 ± 169	1100	22.3 ± 5.0	42.0	4,514
1948	PBF	425	347 ± 154	918	19.5 ± 6.8	52.5	4,568
6020	PBF	390	521 ± 167	978	21.1 ± 5.1	57.0	3,542
6010	PBF	344	547 ± 188	1004	20.7 ± 4.3	60.0	3,693
6012	PBF	367	420 ± 136	1118	17.0 ± 3.5	40.5	5,234
6002	PBF	298	414 ± 151	1218	19.0 ± 4.5	54.0	3,809
1475	PBM	1711	438 ± 137	1130	25.2 ± 6.4	63.0	3,836
1963	PBM	2122	426 ± 154	798	21.6 ± 6.3	88.5	4,462
1969	PBM	1657	401 ± 87	842	27.6 ± 6.1	62.5	3,654
6018	PBM	2143	526 ± 248	1210	26.7 ± 6.4	73.5	3,400
6035	PBM	1733	463 ± 144	1018	22.3 ± 5.5	67.5	4,407
4004	PMM	1275	390 ± 173	1282	22.0 ± 7.7	78.5	3,213
4017	PMM	2008	560 ± 145	846	31.9 ± 5.1	59.5	3,150
1453	PMM	3600	313 ± 224	1129	22.1 ± 1.1	78.5	3,453
NOTE: PMF = postmolt female, PBF = postbreeding female, PMM = postmolt male, PBM = postbreeding male, N = number of dives.

of type 1 pelagic foraging dives for most of the day, with a few hours of type 3 resting dives occurring in the early morning. The type 1 pelagic foraging dives became shallower at night, probably following the vertical migration of prey species. After males reached their foraging grounds, the general diving pattern was composed of up to 21 hours each day of type 2 benthic foraging, broken by a few hours of type 3 resting dives in the early hours of

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the morning. As the males and females returned to Macquarie Island, the most common dives were type 1 pelagic foraging dives and type 4 traveling dives.

Physiological Implications

The diving behavior of the southern elephant seal has some interesting physiological implications, as the animals dive continuously and deeply and remain submerged for long periods. An examination of the duration and depths of dives showed that postmolt females had significantly longer dive durations than postbreeding females, but there were no significant differences in dive depth between postbreeding and postmolt females (see fig. 14.4). When the data were pooled over years, it was possible to compare mean dive duration among four recording intervals—the three trimesters of pregnancy and the postbreeding period.

Seals recorded over the first trimester of pregnancy (February/April) and those recorded during the postbreeding period (November/January) had mean dive durations that were shorter than for those seals recorded over the second (April/June) and third (June/August) trimesters (fig. 14.5). However, mean dive depth and mean time spent at the bottom of the dive were not different among periods, suggesting that the longer dive durations were a result of slower ascents and descents.

When the theoretical aerobic dive limit (ADL) was calculated for each female using the equation ADL = (Lean Mass × TO₂ )/RMR, where TO₂ = 0.079 1 O₂ /kg (Kooyman 1989), and RMR = 0.0113 (Lean mass^0.75 ) 1 O₂ /minute (Schmidt-Neilsen 1983), it was possible to estimate the proportion of dives that exceeded this limit. Lean body mass was used to reduce bias introduced by differing amounts of metabolically inert blubber between individuals. Lean body mass was estimated from mean pre- and posthaulout blubber mass of similar aged southern elephant seals (unpubl. data). Initial analysis of data from the 1988 deployments showed that 44% of dives made by postmolt females exceeded the calculated ADL, whereas only 7% of dives made by postbreeding females and less than 1% made by adult males exceeded this limit (Hindell et al. 1992). When data from 1990 were included, it was possible to make comparisons among different periods in a yearly cycle. Although there were considerable individual differences, animals from the postbreeding period (November/January) and from the first trimester (February/April) exceeded the ADL on a much smaller proportion of dives than did females from the second (April/June) and third (June/August) trimesters (table 14.2).

The small proportion of dives that exceeded the ADL in the postbreeding group suggests that the calculation of ADL for this group is relatively accurate and supports the assertion that the diving metabolic rate approxi-

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Fig. 14.4
Mean dive duration and mean dive depth for adult female
southern elephant seals during the postmolt (PM) and
postbreeding (PB) periods at sea for 1988 and 1990.
Error bars are 95% confidence limits.

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Fig. 14.5
Mean dive duration for female elephant seals during the
three trimesters of pregnancy (Feb.–Apr., Apr.–June,
June–Aug.) and the postbreeding period (Nov.–Jan.).
Error bars are 95% confidence limits. Nested analysis of
variance showed significant differences among groups
(F_3,22 = 28.9, p < .0001, number of dives = 83,008).

mates RMR for these animals. However, it seems unlikely that the ADL was exceeded by such a high proportion of dives in the last two trimester groups as the animals would have had to regularly cope with the buildup of toxic anaerobic metabolites by extending the duration of the surface intervals. Also, the absence of any extended surface intervals following dives that exceeded the calculated ADL suggests that the animals are, for the most part, diving aerobically. It has been suggested that northern elephant seals rarely exceed their ADL, even with dives as long as 50 minutes (Le Boeuf et al. 1988). Thus, the estimation of ADL is probably an underestimation for seals during the second and third trimesters. This would be accentuated by the presence of the fetus, which must be placing additional oxygen demands on the mother's oxygen stores and, therefore, lowering her effective aerobic limits. These seals may be making physiological adjustments to increase their ADL. There are several ways in which this might be achieved. A change in blood volume, possibly associated with pregnancy, would increase ADL, as would a reduction in metabolic rate. Although the seals would be gaining mass over this time, most of this mass gain is

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TABLE 14.2 Proportion of dives of female southern elephant seals that exceed the estimated aerobic dive limit (ADL), where ADL = Lean mass × TO₂ /RMR, and TO₂ = 0.0791 O₂ /kg (Kooyman 1989).
Female	Deployment	Time of year	ADL (min)	% > ADL
1432	Postmolt	February–April	28.9	3.3
3191	Postmolt	February–April	27.9	3.8
3186	Postmolt	February–April	26.6	12.5
3189	Postmolt	February–April	26.7	13.4
3187	Postmolt	February–April	27.2	16.7
		Mean ± SD	27.5 ± 0.9	9.9 ± 5.4
3193	Postmolt	April–June	29.1	48.2
3184	Postmolt	April–June	28.9	54.3
1440	Postmolt	April–June	29.5	63.4
1419	Postmolt	April–June	28.4	68.4
3200	Postmolt	April–June	28.9	80.1
		Mean ± SD	29.0 ± 0.4	62.9 ± 11.1
3178	Postmolt	June–August	27.8	36.0
857	Postmolt	June–August	27.3	48.6
3196	Postmolt	June–August	29.6	63.5
1423	Postmolt	June–August	27.5	72.0
		Mean ± SD	28.1 ± 0.9	55.0 ± 13.8
6012	Postbreeding	November–January	28.8	0.3
1930	Postbreeding	November–January	30.2	2.2
6010	Postbreeding	November–January	28.0	2.4
1918	Postbreeding	November–January	29.5	2.9
6002	Postbreeding	November–January	27.0	3.8
1948	Postbreeding	November–January	29.5	4.1
6020	Postbreeding	November–January	28.9	5.5
1938	Postbreeding	November–January	28.5	8.0
905	Postbreeding	November–January	30.0	17.1
		Mean ± SD	28.9 ± 1.0	5.1 ± 4.7

through the addition of blubber reserves rather than an increase in lean mass. It may be that the seals reduce RMR through physiological adjustments, combined with behavioral changes that minimize energy consumption. It is suggested that the shorter dive durations immediately following the two periods of concentrated energy loss (molting and pup rearing, fig. 14.5) represent more concentrated and active periods of foraging to replenish the depleted fat stores. At these times, RMR would be elevated with respect to the less active foraging type 1 dives from April to August. Captive harbor seals, Phoca vitulina , continue to gain mass over the winter months in spite of reduced food intake and increased thermal energy demands, suggesting some form of reduction in metabolic rate (Renouf and Noseworthy 1990).

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Although seals from the later trimesters exhibited longer dive durations than the other two groups, there were no differences in mean depth of dives and no differences in time spent at the bottom of the dive. Thus, the increase in dive duration must be accounted for by slower ascents and descents. Less strenuous swimming during the ascent and descent would conserve energy, reduce metabolic rate, and, hence, increase the ADL. Weddell seals, Leptonychotes weddelli , may reduce their metabolic requirements by 75% during the descent phase of a dive and by 55% during the ascent phase (Qvist et al. 1986). If the southern elephant seal can lower its metabolism by approximately 40% of resting metabolic rate, then aerobic capacity would be exceeded on very few dives (see Hindell et al. 1992).

Thus, it may be that southern elephant seals make behavioral and physiological changes during the long postmolt period at sea which reduce RMR and increase ADL. To test this more fully, we need to examine diving behavior of individual seals over the entire postmolt period, a task that now seems possible with the development of larger memory TDRs.

Acknowledgments

We thank R. Woods, G. Bedford, K. Lawton, and all members of the 1988, 1989, 1990, and 1991 ANARE to Macquarie Island for their assistance in carrying out the fieldwork. K. Green also assisted in the field and commented on the manuscript, and J. Cox assisted with the figures. We thank the Tasmanian Department of Parks, Wildlife, and Heritage for permission to work at Macquarie Island.

References

Boyd, I. L., and T. Arnbom. 1991. Diving behaviour in relation to water temperature in the southern elephant seal: Foraging implications. Polar Biology 11: 259–266.

Carrick, R., S. E. Csordas, and S. E. Ingham. 1962. Studies on the southern elephant seal, Mirounga leonina (L.). III. The annual cycle in relation to age and sex. CSIRO Wildlife Research 7: 119–160.

Clarke, M. R., and N. MacLeod. 1982. Cephalopods in the diet of elephant seals at Signy Island, South Orkney Islands. British Antarctic Survey Bulletin 57: 27–31.

DeLong, R. L., B. S. Stewart, and R. D. Hill. 1989. Tracking marine mammals at sea with an archival data recorder. In Proceedings of the Eighth Biennial Conference on the Biology of Marine Mammals , December 7–11, Pacific Grove, Calif.

Gentry, R. L., and G. L. Kooyman. 1986. Fur Seals: Maternal Strategies on Land and at Sea . Princeton: Princeton University Press.

Gordon, A. L., and E. J. Molinelli. 1982. Southern Ocean Atlas . Surrey: Columbia University Press.

Green, K., and R. Williams. 1986. Observations of the food remains in faeces of elephant, leopard, and crabeater seals. Polar Biology 6: 43–45.

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Hindell, M. A., and H. R. Burton. 1988. Seasonal haulout patterns of the southern elephant seal (Mirounga leonina ) at Macquarie Island. Journal of Mammalogy 69: 81–88.

Hindell, M. A., H. R. Burton, and D. J. Slip. 1991. Foraging areas of southern elephant seals, Mirounga leonina , as inferred from water temperature data. Australian Journal of Marine and Freshwater Research 42: 115–128.

Hindell, M. A., D. J. Slip, and H. R. Burton. 1991. The diving behaviour of adult male and female southern elephant seals, Mirounga leonina. Australian Journal of Zoology 39: 595–619.

Hindell, M. A., D. J. Slip, H. R. Burton, and M. M. Bryden. 1992. Physiological implications of continuous, prolonged and deep dives of the southern elephant seal (Mirounga leonina ). Canadian Journal of Zoology 70: 370–379.

Kooyman, G. L. 1989. Diverse Divers: Physiology and Behavior . Berlin: Springer Verlag.

Laws, R. M. 1960. The southern elephant seal (Mirounga leonina Linn.) at South Georgia. Norsk Hvalfangst-Tidende 49: 466–476, 520–542.

———. 1977. Seals and whales of the Southern Ocean. Philosophical Transactions of the Royal Society, London, Series B 279: 81–96.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris . Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 67: 2514–2519.

Ling, J. K., and M. M. Bryden. 1981. Southern elephant seal, Mirounga leonina . In Handbook of Marine Mammals. 2. Seals , ed. S. H. Ridgeway and R. J. Harrison, 297–327. London: Academic Press.

Naito, Y., B. J. Le Boeuf, T. Asaga, and A. C. Huntley, 1989. Long-term diving records of an adult female northern elephant seal. Antarctic Record 33: 1–9.

Qvist, J., R. D. Hill, R. C. Schneider, K. J. Falk, G. C. Liggins, M. Guppy, R. L. Elliot, P. W. Hochachka, and W. M. Zapol. 1986. Hemoglobin concentrations and blood gas tensions of free-diving Weddell seals. Journal of Applied Physiology 61: 1560–1569.

Renouf, D., and E. Noseworthy. 1990. Feeding cycles in captive harbor seals (Phoca vitulina ): Weight gain in spite of reduced food intake and increased thermal demands. Marine Behavioral Physiology 17: 203–212.

Schmidt-Neilsen, K. 1983. Animal Physiology: Adaptation and Environment . Cambridge: Cambridge University Press.

Woods, R., M. A. Hindell, and D. J. Slip. 1989. Effects of physiological state on duration of sedation in southern elephant seals. Journal of Wildlife Diseases 25: 586–590.

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Fifteen—
Developmental Aspects of Diving in Northern Elephant Seal Pups

Philip H. Thorson and Burney J. Le Boeuf

ABSTRACT. The aim of this study was to describe the development of diving and measure concomitant changes in physiological correlates that enable this behavior in northern elephant seals, Mirounga angustirostris , during the first nine months of life.

Fifty-seven known-age juvenile seals born at Año Nuevo, California, were studied during the period 1988–1990. We measured (1) time spent in the water and changes in dive depth near the natal rookery during the 2½-month period following weaning, before the seals went to sea for the first time; (2) changes in blood volume, hematocrit, hemoglobin, and myoglobin in seals from near birth to eight months of age; (3) metabolic rate, from oxygen consumption, in 1½- to 3½- month-old juveniles diving in a hooded saltwater tank; and (4) the free-ranging dive pattern of 4-month-old juveniles during part of the first trip to sea.

Diving performance improved quickly during the 10-week period between weaning and going to sea, as reflected by increases in time spent in the water to 12½ hours per day, mean dive duration to 5.9 minutes, and mean dive depth to 16 m. Concurrently, blood and muscle oxygen stores increased, leading to a 46.7% elevation in mass specific oxygen stores, and diving metabolic rate decreased by approximately 50%. Metabolic rate also declined with increasing length of dives and total time submerged. The diving behavior of two 4-month-old seals during the first 12 to 26 days at sea resembled the continuous, deep, and long diving pattern of adults. Mean dive duration was 10 minutes (maximum = 22.3 min), mean surface interval was in the range 1.4 to 1.8 minutes, and mean dive depth was 206 m (maximum = 553 m); approximately 85% of the time at sea was spent submerged.

In only 10 weeks, newly weaned elephant seals undergo profound changes in mass specific blood volume, oxygen stores, and diving metabolic rate while learning to swim and dive near the rookery. These developments prepare them for long-duration deep diving over several months at sea.

Phocid seals suckle out of the water on the substrate where they are born. Consequently, in most species, pups get little or no experience swimming or

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diving prior to weaning. Newly weaned pups must develop these skills before they can forage on their own, often over long periods in the open ocean. Despite the critical importance for survival of the transition from a terrestrial to a marine existence, this period has not been studied in depth in any diving mammal.

Our aim was to study behavioral and physiological changes that accompany the development of diving in the northern elephant seal, M. angustirostris , a seal in which the move from land to sea is especially abrupt and demanding, requiring extreme adaptations for breath holding and withstanding high pressure. Adults lead a pelagic existence characterized by continuous, long duration, deep diving (Le Boeuf et al. 1986, 1988, 1989; DeLong and Stewart 1991; Hindell, Slip, and Burton 1991).

Northern elephant seal pups are nursed daily for up to 28 days before being weaned when the mother goes to sea (Le Boeuf, Whiting, and Gantt 1972). They remain on the natal rookery for the next 2½ months, fasting from food and water while learning to swim and dive. Within 2 weeks after weaning, the weanling enters the water for the first time, usually standing freshwater ponds, tide pools, or shallow water in protected coves or beaches (Rasa 1971; Reiter, Stinson, and Le Boeuf 1978). Initial attempts at swimming and diving are awkward and uncoordinated, but improvement is rapid. During this time, mean sleep apnea duration on land doubles from 4 to 8 minutes (Blackwell and Le Boeuf 1993). Within 8 to 10 weeks of weaning, these juveniles make the first pelagic trip to sea to forage, a journey that lasts approximately 4 months (Reiter et al. 1978).

The first trip to sea is a critical period in the life of elephant seals, as only a mean 46.0 ± 7.7% that depart in the late spring survive and return to the rookery in the fall (Le Boeuf, Morris, and Reiter, this volume). Little is known of the behavior of elephant pups during this period. Tag resight records reveal a general dispersal to the north, with pups from the most northerly rookeries in central California being observed as far north as northern California and Vancouver Island, British Columbia (Bonnell et al. 1979; Condit and Le Boeuf 1984). Examination of the stomach contents of juveniles reveals the remains of species common at depths of 200 m or more (Condit and Le Boeuf 1984; Antonelis et al. 1987).

The development of diving ability during the postweaning fast is important both for initial foraging success and for avoidance of white sharks, Carcharodon carcharias , a near-surface predator (Ainley et al. 1981; Le Boeuf, Riedman, and Keyes 1982). Critical to understanding diving performance is knowledge of the amount of oxygen stored, the rate that oxygen is utilized, and its effect on diving behavior. Changes in hemoglobin concentration, blood volume, and myoglobin concentration directly affect oxygen storage capacity (Snyder 1983; Kooyman 1989). Changes in metabolic rate

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with age affect the rate that oxygen stores are used. Oxygen storage capacity and diving metabolic rate determine the aerobic dive limit (ADL), the amount of time that a seal can remain submerged while diving aerobically (Kooyman et al. 1983).

The specific objectives of this study were to do the following: (1) describe the development of swimming and diving behavior of free-ranging juveniles near the natal rookery during the 2½-month period from weaning to departure from the rookery; (2) measure changes in blood volume, hematocrit, hemoglobin, and myoglobin in developing seals, from near birth to 8 months of age; (3) determine the metabolic rate of juveniles, 1½ to 3½ months old, during the course of diving, swimming, sleeping, and resting at the surface of a seawater tank; and (4) record the free-ranging dive pattern of juveniles, 3½ to 9 months of age, during the first pelagic trip to sea.

Methods

Diving Behavior near the Rookery during the Postweaning Fast

Diving behavior of juveniles, 1 to 3½ months of age, was studied in the waters surrounding their natal rookery at Año Nuevo, California, from February to May during the years 1988 to 1990. This encompasses the period from initial water entry to departure from the rookery on the first pelagic foraging trip to sea. All seals were known-age, having been marked with cattle ear tags (Dalton Jumbo Rototags, Oxon, England) in the inter-digital webbing of the hind flippers a few days after weaning.

Three types of instruments were used to record changes in time per day spent in the water, dive duration, and dive depth. The amount of time spent in the water was recorded with modified digital watches (Cairns et al. 1987), which were attached to 15 juveniles at 1½ months of age. The watches were glued to the hair on the back of a sleeping juvenile, using 5-minute epoxy (Devcon, Danvers, Mass.). When the seal entered the water, the watch shorted out, and time on the watch did not advance during the period in the water. When the pup exited, the watch began to operate. Watches were read at least twice a week.

Dive duration data were obtained with radio transmitters (Titley Micro-electronics, Blenheim, New Zealand) glued to the hair on the heads of 7 juveniles with 5-minute epoxy as they slept. Dive duration was measured using a stopwatch to record the time between when the radio signal was lost (submerged) and when the signal was recovered (surface). The range of the radio signal was approximately 4 km and was received with a Telonics TR-4 receiver (Mesa, Ariz.).

Maximum dive depth of 17 juveniles was measured with capillary tube depth recorders (Burger and Wilson 1988). Teflon tubing, 100 cm in

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length, was sealed at one end and dusted with blue dye powder. As the seal dived, pressure forced water part way up the tube, washing out the dye. The distance the water traveled through the tube was determined by pressure that is proportional to the maximum depth the seal attained. Maximum depth recorders (MDRs) were glued to the hair on the back of sleeping juveniles with 5-minute epoxy. After several days, the MDRs were recovered and maximum depth calculated from the equation of A. E. Burger and R. P. Wilson (1988).

Oxygen Storage Capacity

Total oxygen storage capacity was calculated as the sum of the blood, muscle, and lung oxygen stores, based on the equations of G. L. Kooyman et al. (1983).

Mass determinations, blood samples, and estimates of blood volume were obtained from 25 juveniles (11 males and 14 females) ranging in age from 2 days to 8 months old. The seals were restrained using a mixture of ketamine hydrochloride and diazepam at a dose of 4 mg/kg of body weight (Briggs, Hendrickson, and Le Boeuf 1975). Mass was determined for all seals by hoisting them in a modified canvas bag (Pernia, Hill, and Ortiz 1980) suspended from a 450 ± .5 kg spring scale (Chatillon, New York, N.Y.) attached to a tripod.

Blood samples were drawn from the extradural intravertebral vein using an 8.0-cm, 18-ga spinal needle (Geraci and Smith 1975). Samples were placed into sodium heparin Vacutainers (Becton-Dickson, Rutherford, N.J.). Blood volume was measured by first taking a blood sample, then injecting Evans blue dye into the extradural vein (4 mg/kg of body weight) (Linden and Mary 1983). A final blood sample was taken at least 20 minutes later, after allowing for equilibration.

Hematocrit was determined in duplicate from aliquots of whole blood that had been centrifuged at 11,500 rpm (IEC Micro Hematocrit, Needham Heights, Mass.). Hemoglobin (Hb) determinations were made using the cyanomethohemoglobin conversion method (Sigma Chemical Co., Assay Kit 525, St. Louis, Mo.). Blood volume was determined using the protocol of R. J. Linden and D. A. S. G. Mary (1983).

Myoglobin Assay

Muscle samples were obtained from 13 seals (8 females and 5 males) varying in age from stillborn pups to 8-month-old juveniles. For both fresh carcasses and live animals, muscle samples were taken from the latissimus dorsi just lateral to the pelvis. For biopsies of live seals, the site was cleaned with Betadyne solution, and a local anesthetic, lidocaine hydrochloride, was injected. A sterile 8 mm suction biopsy needle was inserted to obtain a tissue sample weighing approximately 75 mg (Dubowitz and Brooke 1973;

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Evans, Phinney, and Young 1982). The assay for myoglobin concentration was performed using the protocol of B. Reynafarje (1963).

Metabolic Studies

Twelve juveniles ranging in age from 1½ to 3½ months old were transported from Año Nuevo to the Long Marine Laboratory where they were held in outdoor seawater tanks. Metabolic rate was determined using an open-circuit respirometry system to measure oxygen consumption in a manner similar to the method of T. M. Williams (1987).

This system consisted of a metabolic hood (a plexiglass dome measuring 2 × 1 × 0.5 m) with an intake and exhaust port placed over a seawater tank which measured 2.5 by 1.8 by 2 m, the only area from which the seal could breathe. Ambient air was pulled through a dry gas meter (Singer, American Meter Division) and then through the metabolic hood by vacuum pump. An aliquot of the air exiting the dome was continually driven through a Baralyme column to remove carbon dioxide, and a Drierite column removed water before passing through an S-3A oxygen analyzer (Ametek, Sunnyvale, Calif.) to measure the fractional oxygen content. The analog output of the oxygen analyzer was converted to a digital signal (Sable Systems, Los Angeles, Calif.) and transferred to a computer. Equation 4b from P. C. Withers (1977) was used to calculate metabolic rate from the fractional change of oxygen.

Seals were weighed in the laboratory prior to experiments using a load cell platform scale (Senstek 2000, Canada). Water temperature of the metabolic tank ranged between 12 and 16°C, which is within the thermoneutral zone of weaned elephant seal pups (P. Thorson, unpubl. data).

Free-ranging Dive Pattern at Sea

Time-depth recorders (TDRs) were attached to 5 juveniles (4 females and 1 male) during 1989 and 3 juveniles (2 males and 1 female) in 1990 at Año Nuevo just prior to departing on their first foraging trip to sea when they were 3½ months old. Two types of TDRs were used, one mechanical and the other a microprocessor system (Wildlife Computers, Woodinville, Wash.). The mechanical TDR measured 2.5 cm in diameter by 8.5 cm long with a mass of 70 (Naito, Asaga, and Ohyama 1990). The TDR used a mechanical pressure transducing system with a timing circuit to record time and depth on pressure-sensitive paper. The pressure transducing system had a threshold limit of 227 m. When recovered, the record was enlarged and digitized for analysis. The microprocessor TDR measured 15 cm long by 2.5 cm wide with a mass of 100 g. The TDR had 256 kilobytes of memory and was programmed to sample depth every 10 seconds (maximum depth limit = 2,000 m) and temperature every 10 minutes. At recovery, the data in the TDR were downloaded to a computer and analyzed.

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The seals were chemically restrained, weighed, and blood sampled as mentioned above. TDRs were attached to the hair with 10-minute epoxy (Fibre Glass Evercoat, Cincinnati, Ohio), using the method of Le Boeuf et al. (1988, 1989).

Results

Diving Behavior near the Rookery during the Postweaning Fast

Newly weaned pups began entering the water at approximately 2 weeks postweaning at 1½ months of age. Time per day spent in the water was less than 2% at first and was concentrated at dawn and dusk. It increased to about 52% per day by 10 weeks postweaning, being concentrated at night, and remained at this level until departure on the first foraging trip to sea (fig. 15.1a).

The mean duration of dives in the waters surrounding the rookery increased from 1.9 minutes at initial water entry to 6.1 minutes at the end of the postweaning fast (fig. 15.1b). During this time, the seals did not venture far from the rookery and remained in water less than 12 m deep (except for one 16 m dive by seal H113 who was carrying a TDR; see below); mean dive depth increased with age (fig. 15.1c).

Changes in Physiological Variables over the First Eight Months of Life

Table 15.1 shows that as mass decreased during the postweaning fast, hematocrit, hemoglobin concentration, mass specific blood volume, and myoglobin concentration increased significantly (t-tests, all significant at p < .005). Consequently, mass specific oxygen stores increased by 46.7% over the postweaning fast, or 69.4% from the suckling period to the time when the seals were ready to go to sea. The highest levels of myoglobin concentration, mass specific blood volume, and total oxygen stores were reached in seals returning from their first trip to sea.

Metabolic Studies in Seawater Tanks during the Postweaning Fast

Diving metabolic rate decreased significantly (t-test = 5.43, df = 234, p < .001), by about 50%, over the course of the postweaning fast (fig. 15.2a). Metabolic rate also declined as a function of increasing dive duration (fig. 15.2b) and increasing percentage of time spent submerged, when observed in 30-minute blocks (fig. 15.2c). This trend was seen throughout the postweaning fast, although it was more pronounced in the later period.

Diving Behavior during the First Foraging Trip to Sea

Two of the eight TDRs deployed on juveniles before their first trip to sea were recovered and contained diving data; both of them were carried by

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Fig. 15.1
(A) Percentage of time spent in water during the postweaning
fast as a function of age based on 57 observations, from 15
individuals (9 females, 6 males). (B) Dive duration as a
function of age during the postweaning fast, based on 121
observations of 7 individuals (4 males, 3 females). (C) Changes
in dive depth during the postweaning fast as a function
of age, based on 110 observations of 17 individuals
(10 females, 7 males).

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Fig. 15.2
(A) Changes in diving metabolic rate, measured as oxygen
consumption, during the postweaning fast, based on 235
observations from 11 individuals (7 males, 4 females).
(B) Change in metabolic rate, measured as oxygen consumption,
as a function of dive duration. Data based on 137 observations
from 6 individuals (4 males, 2 females). (C) Relation between
metabolic rate, measured as oxygen consumption, and the
percentage of time spent underwater. Data based on 115 30-min
periods from 6 individuals (4 males, 2 females). Numbers in bars
represent the number of observations for that interval.

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TABLE 15.1 Mean hematocrit (Hct), hemoglobin concentration (Hb), mass specific blood volume (V_b ), myoglobin concentration (Mb), and mass specific oxygen stores of northern elephant seals during nursing and the postweaning fast and after the first foraging trip to sea.
Age	Mass (kg)	Hct (%)	Hb (g/dL)	V_b (ml/kg)	Mb (g/100g)	O₂ Stores (ml/kg)
Nursing
2–21 days (n = 12)	102 (22.6)	50.2 (2.3)	18.9 (1.0)	100 (8.9)	2.1 (1.2)	35.6
Postweaning
4 weeks (n = 20)	134 (19.2)	52.4 (2.9)	20.0 (1.8)	111 (14.6)	3.4 (1.1)	41.1
8 weeks (n = 15)	103 (20.2)	59.6 (6.4)	22.6 (2.3)	127 (12.9)	4.5 (1.2)	52.3
12 weeks (n = 12)	96.1 (13.3)	61.6 (4.2)	23.6 (3.2)	144 (18.2)	5.1 (1.3)	60.3
After first foraging trip to sea
8 months (n = 17)	90.1 (23.2)	58.1 (6.5)	22.8 (2.4)	175 (10.4)	5.7 (1.1)	68.8
NOTE: Numbers in parentheses represent ± 1 SD. Sample size is the same for all variables except myoglobin concentration (Mb), where n = 4 for all age classes.

females. The TDR of seal G372 was recovered in December 1990 at Año Nuevo, 7½ months after deployment; it recorded the first 12 days at sea, May 12–13, 1990. The TDR of seal H113 was recovered in March 1991 at Half Moon Bay, 45 km north of Año Nuevo, 10 months after deployment; it recorded the first 26 days at sea, May 14 to June 10, 1990.

A summary of the diving data for these two seals is shown in table 15.2. Both seals exhibited similar dive durations with a mean of about 10 minutes; seal H113 exhibited the longest dives, with the maximum lasting 22.3 minutes (fig. 15.3a). Approximately 90% of the surface intervals of both seals were between 0.5 and 1.75 minutes; only 5% were longer than 3 minutes (fig. 15.3b). Both seals had one extended surface interval longer than one hour, and both spent the majority of their time at sea underwater.

The mean depth of the dives of seal H113 was 206 m (median depth = 160 m), and its maximum dive depth was 553 m (table 15.2). Twenty-nine percent of the dives of seal G372 exceeded the depth limit of its TDR, 227 m. By comparison, 42% of the dives of the other seal exceeded 227 m.

Mean dive duration increased as a function of the time at sea for the first

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TABLE 15.2 Summary of the diving behavior of seal G372 (12 days at sea) and seal H113 (26 days at sea).
Seal	No. of dives	Mean duration (min)	Max. duration (min)	Mean depth (m)	Max. depth (m)	Mean SI (min)	Max. SI (min)	% Time underwater
G372	1,408	9.5 (1.2)	17.4	157^a (66)	227^a	1.8 (3.2)	66.1	84 (3.7)
H113	3,124	10.6 (3.5)	22.3	206 (120)	533	1.4 (4.4)	217.1	88 (4.1)
NOTE: Numbers in parentheses represent ± 1 SD.
^a The TDR deployed on G372 had a depth limitation of 227 m, which the seal exceeded on 29% of its dives; therefore, the values given for mean and maximum dive depths are biased.

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Fig. 15.3
(A) Frequency distributions of dive durations of 2 juvenile northern
elephant seals during the first 12 to 26 days at sea. (B) Frequency
distributions of surface intervals of 2 juvenile elephant seals during
the first trip to sea. (C) Frequency distributions of dive depth of 2
juvenile northern elephant seals during the first trip to sea.
The TDR of seal G372 had a depth limitation of 227 m.

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Fig. 15.4
Changes in mean dive duration per day (± 1 SD) of 2 juvenile
elephant seals and 4 adult female elephant seals during the
first 12 days at sea following lactation. Data on adult
females from unpublished records.

four days, but acclimation to diving deeply was as rapid as that of adult females with much more diving experience (fig. 15.4). There was no correlation between dive duration and postdive surface interval (r = .01).

Discussion

During the 10-week period following weaning, young elephant seals undergo behavioral and physiological changes that prepare them to forage for several months at sea, a period characterized by virtually continuous, deep, and long duration diving. The diving performance of 3½-month-old elephant seals on the first trip to sea is similar to that of adults and exceeds that of most other adult pinnipeds, in terms of dive duration and dive depth (Kooyman 1989; Le Boeuf, this volume). Perhaps no other marine mammal must make such a drastic transition in such a short time.

We summarize and discuss the principal changes during this critical period of development that prepare the animal to be a deep and long duration diver. We emphasize that concomitant with improvements in swim-

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ming and diving performance, there occur significant increases in oxygen storage capacity and decreases in diving metabolic rate.

Oxygen Storage Capacity

Blood is the most important storage site of oxygen in phocid seals, as it contains approximately 65% of the total oxygen stores, followed by the muscle (30%) and the lungs (5%) (Kooyman 1985, 1989). Blood oxygen storage capacity is determined by hemoglobin concentration and blood volume (Snyder 1983). Diving animals tend to have higher hemoglobin concentrations and blood volumes than terrestrial animals. Among marine mammals, the deeper and longer duration divers have the highest hemoglobin concentrations and blood volumes (Ridgway and Johnston 1966; Sleet, Sumich, and Weber 1981; Duffield, Ridgway, and Cornell 1983; Snyder 1983; Kooyman 1985, 1989), and as we would expect from adult diving performance, these values have been reported to be high for northern elephant seal pups (Simpson, Gilmartin, and Ridgway 1970; Castellini, Costa, and Huntley 1986; Hedrick, Duffield, and Cornell 1986; Wickham 1989). Changes in these values with development have received little attention. A. M. Kodama, R. Elsner, and N. Pace (1977) reported that mass specific blood and hemoglobin concentrations increased during the first year in the harbor seal, Phoca vitulina . M. M. Bryden and G. H. K. Lim (1972) reported that southern elephant seals, M. leonina , increased their mass specific blood volume during the postweaning fast and during the first trip to sea, an increment that is similar to what we observed in northern elephant seal pups (table 15.1). By the time juvenile elephant seals are ready to go to sea for the first time, their body is 14.4% blood, as compared to 21.2% blood for an adult female (P. Thorson, unpubl. data).

Total oxygen stores increase rapidly to a high level in developing elephant seals, due to increases in blood and muscle oxygen stores (table 15.1). When it is time to make the first trip to sea, these young juveniles have already amassed mass specific oxygen stores of 60.3 ml/kg, 73.5% of the mass specific oxygen stores recorded in adult females (82.1 ml/kg) (P. Thorson, unpubl. data). The oxygen stores in juvenile elephant seals are similar to those found in adult phocids of other species (Kooyman 1985, 1989).

Metabolic Rate

By 3 months of age, elephant seals had significantly lower metabolic rates and longer dive durations than they exhibited at weaning (figs. 15.1B, 15.2A). This is not surprising, as it is known that metabolic rate decreases with age (Brody 1945; Miller and Irving 1975; Ashwell-Erickson and Elsner 1981) and with increasing time spent fasting (Brody 1945; Kleiber 1975; Ashwell-Erickson and Elsner 1981; Worthy and Lavigne 1987; Rea and

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Costa 1992). Age and fasting effects alone, however, may not be responsible for the metabolic decrease we observed. During the postweaning fast, juvenile elephant seals spent an increasing amount of time swimming and diving, in the process utilizing protein and redistributing muscle mass (fig. 15.1; Bryden 1969). Using protein increases the metabolic rate, while diving decreases it.

The oxygen consumption pattern of juveniles was less consistent early in the postweaning fast than later on. This suggests that developing seals gained increasing control over their metabolic rate as their mass specific oxygen stores and diving experience increased. In addition, metabolic rate was inversely correlated with dive duration and the total amount of time spent diving (fig. 15.2), an effect that was most pronounced late in the postweaning fast. M. A. Fedak (1986) reported a similar trend for gray seals, Halichoerus grypus , swimming and diving in a water flume.

Diving Behavior on the First Trip to Sea

The diving pattern of juveniles during the first part of their first trip to sea suggests that they were diving aerobically. Postdive surface intervals are brief regardless of the duration of the previous dive (table 15.2). The percentage of dives that exceeded the ADL for the two juveniles in this study and for two juvenile Weddell seals is shown in table 15.3. With a diving metabolic rate of 1.5 times resting (Kooyman et al. 1973, 1983), 30.5 to 46.9% of the dives of the two juvenile elephant seals exceeded the ADL. This stands in marked contrast to the performance of immature Weddell seals who exceeded the ADL on only 4% of their dives, despite a 28% weight advantage. Moreover, for the immature Weddell seals, lactic acid and postdive surface intervals increased after dives above 10 minutes (Kooyman et al. 1983).

If the swim velocities of juveniles are relatively low on long duration dives, as preliminary data indicate (P. Thorson, unpubl. data) and as is the case in adult females (Le Boeuf et al. 1992; Crocker et al., this volume), the diving metabolic rate should be relatively low. Metabolic rate is highly correlated with swim velocity (Davis, Williams, and Kooyman, 1985; Ponganis et al. 1990; Williams, Kooyman, and Croll 1991); therefore, a decrease in swim velocity would decrease the diving metabolic rate and the ADL would increase. A diving metabolic rate of 0.36 to 0.39 1/min is 0.8 times the predicted basal metabolic rate (BMR) and would include even the longest dives of each pup at sea (table 15.3). Because diving metabolic rate in the laboratory decreases with increasing dive duration to levels below the predicted BMR (fig. 15.2b), it is possible for a seal to have a diving metabolic rate near resting when swim speed is low. Direct measurements of diving metabolic rate of Weddell seals have been recorded at near resting levels (Kooyman 1973; Castellini, Kooyman, and Ponganis 1992).

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TABLE 15.3 Comparison of the estimated aerobic dive limit (ADL) of 2 juvenile Weddell seals (combined) and 2 juvenile elephant seals during the first foraging trip to sea.
Seal	Mass (kg)	O₂ stores (1 O₂ )	VO₂ 1 (O₂ /min)	ADL (min)	% Dives (>ADL)
Weddell seal
1.5 · BMR 2.0 m/sec	140	8.2	0.69	11.9	3.5
Elephant seal
1.5 · BMR 2.0 m/sec	96	5.8	0.51–0.56	11.4	30.5
	109	6.6		11.8	46.9
1.0 · BMR 0.8 m/sec	96	5.8	0.36	16.1	1.1
	109	6.6	0.39	16.9	4.7
NOTE: Estimates of ADL for the juvenile Weddell seals are from Kooyman et al. (1983). Estimates of the ADL for the elephant seals are from this study. Estimates of swim velocity for Weddell seals are from Castellini, Kooyman, and Ponganis (1992) and for elephant seals from P. Thorson (unpubl. data).

The depth of dives attained by juvenile elephant seals during the first 2 to 3 weeks at sea is remarkable in two respects. The dives are deeper than those of most other adult pinnipeds (see Le Boeuf et al. 1988, for review). Second, great depths are reached despite a body composition that averages 48% lipids, double the mean lipid composition of nonpregnant adult females and adult males (Kretzmann 1990; Rea and Costa 1992; unpubl. data). Because of the high ratio of fat to lean body mass, juveniles going to sea for the first time are positively buoyant. Thus, it would seem that juveniles would require greater effort to reach depths than adults.

In conclusion, the 10-week period following weaning that northern elephant seal juveniles spend swimming and diving near the natal rookery provides critical preparation for life at sea. Increases in blood volume, hematocrit, hemoglobin concentration, and myoglobin concentration result in large oxygen storage capacity, which, combined with an increased ability to decrease metabolic rate while diving, enables them to maximize time underwater for travel, foraging, rest, and predator avoidance.

Acknowledgments

We thank V. Kirby, M. Kretzmann, P. Morris, L. Starke, and E. Theiss for assistance in the laboratory and in the field. M. A. Castellini, D. P. Costa, G. L. Kooyman, P. J. Ponganis, and G. A. J. Worthy provided invaluable advice on many aspects of this project. We are indebted to Y. Naito for providing four of the mechanical time-depth recorders as well as for digitizing the record of seal G372. We thank G. Strachan and the rangers at Año

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Nuevo State Reserve for their cooperation. This work was supported by grants from the Earl and Ethyl Myers Oceanographic and Marine Biology Trust, Friends of the Long Marine Laboratory, Biology and Marine Sciences boards of the University of California, Santa Cruz, the G. MacGowan estate, and the National Science Foundation. This work was conducted under federal permit number 496 issued by the National Marine Fisheries Service.

References

Ainley, D. G., C. S. Strong, H. P. Huber, T. J. Lewis, and S. H. Morrell. 1981. Predation by sharks on pinnipeds at the Farallon Islands. Fishery Bulletin 78: 941–945.

Antonelis, G. A., M. S. Lowry, D. P. De Master, and C. H. Ficus. 1987. Assessing northern elephant seal feeding habits by stomach lavage. Marine Mammal Science 3: 308–322.

Ashwell-Erickson, S., and R. Elsner. 1981. The energy cost of free existence for Bering Sea harbor and spotted seals. In The Eastern Bering Sea Shelf: Oceanography and Resources , ed. D. W. Hood and J. A. Calder, 869–899. Washington, D.C.: U.S. Department of Commerce.

Blackwell, S. B., and B. J. Le Boeuf. 1993. Developmental aspects of sleep apnoea in northern elephant seals. Journal of Zoology, London 231: 437–447.

Bonnell, M. L., B. J. Le Boeuf, M. O. Pierson, D. H. Dettman, and G. D. Farrens. 1979. Summary Report 1975–1978. Marine Mammal and Seabird Surveys of the Southern California Bight Area . III Pinnipeds . Bureau of Land Management, Department of the Interior, Contract AA550-CT7-36 to Principal Investigators: Kenneth S. Norris (Cetacea), Burney J. Le Boeuf (Pinnipeds), and George L. Hunt, Jr. (Birds).

Briggs, G. D., R. V. Hendrickson, and B. J. Le Boeuf. 1975. Ketamine immobilization of northern elephant seals. Journal of the American Veterinary Medicine Association 167: 546–548.

Brody, S. 1945. Bioenergetics and Growth with Special Reference to the Efficiency Complex in Domestic Animals . New York: Hafner Press.

Bryden, M. M. 1969. Relative growth of the major body components of the southern elephant seal, Mirounga leonina (L.). Australian Journal of Zoology 17: 153–177.

Bryden, M. M., and G. H. K. Lim. 1972. Blood parameters of the southern elephant seal (Mirounga angustirostris , Linn.) in relation to diving. Comparative Biochemistry and Physiology 28: 139–148.

Burger, A. E., and R. P. Wilson. 1988. Capillary-tube depth gauges for diving animals: An assessment of their accuracy and capability. Journal of Field Ornithology 59: 345–354.

Cairns, D. K., K. A. Bredin, V. L. Bert, and W. A. Montevecchi. 1987. Electronic activity recorders for aquatic wildlife. Journal of Wildlife Management 51: 395–399.

Castellini, M. A., D. P. Costa, and A. C. Huntley. 1986. Hematocrit variation during sleep apnea in elephant seal pups. American Journal of Physiology 251: R429–R431.

Castellini, M. A., G. L. Kooyman, and P. J. Ponganis. 1992. Metabolic rates of

― 287 ―

freely diving Weddell seals: Correlations with oxygen stores, swim velocity, and diving duration. Journal of Experimental Biology 165: 181–194.

Condit, R., and B. J. Le Boeuf. 1984. Feeding habits and feeding grounds of the northern elephant seal. Journal of Mammalogy 65: 281–290.

Davis, R. W., T. M. Williams, and G. L. Kooyman. 1985. Swimming metabolism of yearling and adult harbor seals, Phoca vitulina. Physiological Zoology 58: 590–596.

DeLong, R. L., and B. S. Stewart. 1991. Diving patterns of northern elephant seal bulls. Marine Mammal Science 7: 369–384.

Dubowitz, V., and M. Brooke. 1973. Muscle Biopsy: A Modern Approach . Philadelphia: W. B. Saunders Co.

Duffield, D. A., S. H. Ridgway, and L. H. Cornell. 1983. Hematology distinguishes coastal and offshore forms of dolphins (Tursiops ). Canadian Journal of Zoology 61: 930–933.

Evans, W. J., S. D. Phinney, and V. R. Young. 1982. Suction applied to a muscle biopsy maximizes sample size. Medicine and Science in Sports and Exercise 14: 101–102.

Fedak, M. A. 1986. Diving and exercise in seals: A benthic perspective. In Diving in Animals and Man , ed. A. Brubakk, J. W. Kanwisher, and G. Sundnes, 11–32. Tronheim: Tapir.

Fedak, M. A., L. Rome, and H. J. Seeherman. 1981. One-step-N₂ dilution technique for calibrating open-circuit VO₂ measuring systems. Journal of Applied Physiology 51: 772–776.

Geraci, J. R., and T. G. Smith. 1975. Functional hematology of ringed seals (Phoca hispida ) in the Canadian arctic. Journal of the Fisheries Research Board of Canada 32: 2559–2564.

Hedrick, M. S., D. A. Duffield, and L. H. Cornell. 1986. Blood viscosity and optimal hematocrit in a deep-diving mammal, the northern elephant seal (Mirounga angustirostris ). Canadian Journal of Zoology 64: 2081–2085.

Hindell, M. A., D. J. Slip, and H. R. Burton. 1991. The diving behaviour of adult male and female southern elephant seals, Mirounga leonina (Pinnipedia: Phocidae). Australian Journal of Zoology 39: 595–619.

Kleiber, M. 1975. The Fire of Life: An Introduction to Animal Bioenergetics . Huntington, N. Y.: Robert E. Kreiger Publishing.

Kodama, A. M., R. Elsner, and N. Pace. 1977. Effects of growth, diving history, and high altitude on blood oxygen capacity in harbor seals. Journal of Applied Physiology 42: 852–858.

Kooyman, G. L. 1973. Respiratory adaptation in marine mammals. American Zoologist 13: 457–178.

———. 1985. Physiology without restraint in diving mammals. Marine Mammal Science 1: 166–178.

———. 1989. Diverse Divers: Physiology and Behavior . Berlin: Springer Verlag.

Kooyman, G. L., M. A. Castellini, R. W. Davis, and R. A. Maue. 1983. Aerobic diving limits of immature Weddell seals. Journal of Comparative Physiology 151: 171–174.

Kooyman, G. L., D. H. Karem, W. B. Campbell, and J. J. Wright. 1973. Pulmonary gas exchange in freely diving Weddell seals, Leptonychotes weddelli. Respiratory Physiology 17: 283–290.

Kooyman, G. L., E. A. Wahrenbrock, M. A. Castellini, R. W. Davis, and E. E. Sin-

― 288 ―

nett. 1980. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: Evidence of preferred pathways from blood chemistry and behavior. Journal of Comparative Physiology 138: 335–346.

Kretzmann, M. B. 1990. Maternal investment and the post-weaning fast in northern elephant seals: Evidence for sexual equality. Master's thesis, University of California, Santa Cruz.

Lane, R. A. B., R. J. H. Morris, and J. W. Sheedy. 1972. A haematological study of the southern elephant seal, Mirounga leonina (Linn.). Comparative Biochemistry and Physiology 42A: 841–850.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., Y. Naito, T. Asaga, D. Crocker, and D. P. Costa. 1992. Swim speed in a female elephant seal: Metabolic and foraging implications. Canadian Journal of Zoology 70: 786–795.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Canadian Journal of Zoology 67: 2514–2519.

Le Boeuf, B. J., M. Riedman, and R. S. Keyes. 1982. White shark predation on pinnipeds in California waters. Fishery Bulletin 80: 891–895.

Le Boeuf, B. J., R. J. Whiting, and R. F. Gantt. 1972. Perinatal behaviour of northern elephant seal females and their young. Behaviour 43: 121–156.

Lenfant, C., K. Johansen, and J. D. Torrance. 1970. Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respiratory Physiology 9: 277–286.

Linden, R. J., and D. A. S. G. Mary. 1983. The measurement of blood volume. Techniques in the Life Sciences: Cardiovascular Physiology P305: 25.

Miller, K., and L. Irving. 1975. Metabolism and temperature regulation in young harbor seals, Phoca vitulina richardsi in water. American Journal of Physiology 229: 506–511.

Naito Y., T. Asaga, and Y. Ohyama. 1990. Diving behavior of Adélie penguins determined by time-depth recorder. Condor 92: 582–586.

Pernia, S., A. Hill, and C. L. Ortiz. 1980. Urea turnover during prolonged fasting in the northern elephant seal. Comparative Biochemistry and Physiology 65B: 731–734.

Ponganis, P. J., G. L. Kooyman, M. H. Zornow, M. A. Castellini, and D. A. Croll. 1990. Cardiac output and stroke volume in swimming harbor seals. Journal of Comparative Physiology 160B: 473–482.

Rasa, O. A. 1971. Social interaction and object manipulation in weaned pups of the northern elephant seal Mirounga angustirostris. Zeitschrift für Tierpsychologie 29: 82–102.

Rea, L. D., and D. P. Costa. 1992. Changes in standard metabolism during long-term fasting in northern elephant seal pups (Mirounga angustirostris). Physiological Zoology 65: 97–111.

― 289 ―

Reiter, J., N. L. Stinson, and B. J. Le Boeuf. 1978. Northern elephant seal development: The transition from weaning to nutritional independence. Behavioral Ecology and Sociobiology 3: 337–367.

Reynafarje, B. 1963. Simplified method for the determination of myoglobin. Journal of Laboratory and Clinical Medicine 61: 139–145.

Ridgway, S. H., and D. G. Johnston. 1966. Blood oxygen and ecology of porpoises. Science 151: 456–457.

Simpson, J. G., W. G. Gilmartin, and S. H. Ridgway. 1970. Blood volume and other hematological values in young elephant seals (Mirounga angustirostris ). American Journal of Veterinary Research 31: 1449–1452.

Sleet, R. B., J. L. Sumich, and L. J. Weber. 1981. Estimates of total blood volume and total body weight of a sperm whale (Physeter catodon ). Canadian Journal of Zoology 59: 567–570.

Snyder, G. K. 1983. Respiratory adaptations in diving mammals. Respiratory Physiology 54: 269–294.

Wickham, L. L. 1989. Blood viscosity in phocid seals: Possible adaptations to diving. Journal of Comparative Physiology 159B: 153–158.

Williams, T. M. 1987. Approaches for the study of exercise physiology and hydrodynamics in marine mammals. In Approaches to Marine Mammal Energetics , ed. A. C. Huntley, D. P. Costa, G. A. J. Worthy, and M. A. Castellini, 127–145. Lawrence, Kan.: Allen Press.

Williams, T. M., G. L. Kooyman, and D. A. Croll. 1991. The effect of submergence on heart rate and oxygen consumption of swimming seals and sea lions. Journal of Comparative Physiology 160B: 637–644.

Withers, P. C. 1977. Measurement of VO₂ , VCO₂ , and evaporative water loss with a flow-through mask. Journal of Applied Physiology 42: 120–123.

Worthy, G. A. J., and D. M. Lavigne. 1987. Mass loss, metabolic rate, and energy utilization by harp and gray seal pups during the postweaning fast. Physiological Zoology 60: 352–364.

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Sixteen—
Postbreeding Foraging Migrations of Northern Elephant Seals

Brent S. Stewart and Robert L. DeLong

ABSTRACT. Adult northern elephant seals depart southern California Channel Islands rookeries in February and early March to forage and replenish body reserves that were depleted during intensive breeding season fasts. Females remain at sea for around 66 days and males for around 120 days before they return to the Channel Islands to molt. During that period seals dive—and presumably forage—deeply and continually while migrating between southern California rookeries and haulouts and offshore, northern foraging areas between 40° and 48°N latitude (females) and the Gulf of Alaska and eastern Aleutian Islands (males); females cover over 5,500 km and males over 11,100 km during these round-trip postbreeding migrations. Males and females differ in their vertical and geographic distributions during these migrations, but the reasons for that segregation are unknown.

Adult northern elephant seals depart terrestrial rookeries from late January through early March and remain at sea, diving continually, for around 2 (females) to 4 (males) months before returning to land to molt (Le Boeuf et al. 1989; DeLong and Stewart 1991). Their behaviors while at sea during those postbreeding periods have been documented in extraordinary detail in recent years (e.g., Le Boeuf et al. 1988, 1989; DeLong and Stewart 1991), though the geographic locations of the seals have been unknown. In 1987, we began, in collaboration with colleague R. Hill, to develop and test a microprocessor-based event recorder that would allow simultaneous documentation of the locations and diving patterns of foraging northern elephant seals throughout their long periods at sea (DeLong, Stewart, and Hill 1992). Using data collected with those instruments, we describe here the postbreeding migrations of 8 adult male and 5 adult female northern elephant seals between San Miguel Island, in southern California, and pelagic foraging areas in the North Pacific, and we interpret intra- and in-

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tersexual variation in dive patterns in light of this new information on seal dispersion.

Methods

We instrumented 8 lactating females in 1990 and 16 adult males in 1989 and 1990 with microprocessor-based, geographic-location-time-depth recorders (termed geolocation recorders, or GLTDRs; DeLong, Stewart, and Hill 1992) at San Miguel Island (34°02¢ N, 120°23¢ W) at the end of the breeding season (February–March). We recovered the instruments when the seals returned to land to molt several months later (females, April–May; males, June–July). The design and function of the GLTDRs are described in detail by R. L. DeLong and B. S. Stewart (1991) and DeLong, Stewart, and Hill (1992). Briefly, we programmed the instruments to sample hydrostatic pressure ( = depth ± 2 m) at 30- or 60-second intervals for the entire periods the seals were at sea. Measurements of sea-surface temperature (SST) and ambient light levels were made and stored during the seals' brief interdive surface periods. We estimated each seal's latitudinal location each day by calculating day length and longitude from local apparent noon using daylight profiles stored in the GLTDRs and computer algorithms developed by DeLong, Stewart, and Hill (1992). Determination of location from daylight profiles and the factors that affect location accuracy are discussed in detail elsewhere (DeLong, Stewart, and Hill 1992; Hill, this volume). The most important influences on accurate calculation of latitude are the durations of seals' dives near twilight and the equinox, when day length does not vary substantially with latitude. Near the vernal equinox (March 22) we compared GLTDR sea-surface temperature measurements to latitudinal distributions of SST from other sources to determine seals' latitudinal locations (see DeLong, Stewart, and Hill 1992). We also used SST comparisons to validate all other locations. Our field calibration studies of these instruments indicate that locations that are calculated and corrected using this technique are accurate to around 60 nm or better (ibid.; Stewart and DeLong, unpubl. data). We determined the number of days that each seal was at sea by direct inspection of the dive records, which indicated departure and return dates and times.

Statistical analyses of dive parameters were performed using Systat. We report sample statistics (i.e.,

= sample mean, SD = standard deviation of the sample mean) as summary statistics for all dives of each seal and population statistics (i.e., µ = population mean, SEM = standard error of the population mean) as summary statistics for all dives of all seals. We used one- or two-way analysis of variance (Zar 1984) to compare seals' dive records.

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Results

We recovered instruments from 5 females and 9 males. The light-level sensor in one male's instrument failed, but all other GLTDRs contained depth, light-level, and SST data for the seals' entire periods at sea.

Females were at sea for around 66 days and males for around 120 days before returning to San Miguel Island to molt (tables 16.1, 16.2). All seals dove continually while at sea (figs. 16.1, 16.2, 16.3). Females' dives averaged 520 m deep (SEM = 15 m) and 22.3 minutes long (SEM = 1.3 min.), and males' dives averaged 367 m deep (SEM = 34 m) and 22.6 minutes long (SEM = 1 min.); interdive periods at the surface were routinely brief (females, µ = 2.1 min., SEM = 0.05 min.; males, µ = 3.2 min., SEM = 0.1 min.; fig. 16.4).

Seals spent little time at depths shallower than 200 m, except when rapidly descending or ascending to preferred depths, or greater than 800 m (figs. 16.1, 16.2, 16.3). As 20 to 50% of most dives were spent within a range of 30 m of maximum depth (DeLong and Stewart 1991; Stewart and DeLong, unpubl. data), we use maximum depth of each dive as an index of seals' water depth preference and presumably foraging habitat. Females dove deeper, on average, than males did (p < .01; tables 16.1, 16.2), although the greatest depths reached during their migrations were similar (females, 983–1,567 m; males, 831–1,581 m).

All seals began traveling north immediately upon entering the water in late February and March, covering about 90 to 100 km/day for approximately 16 (females, SD = 7.6 days) to 38 days (males, SD = 5.7 days) before travel speeds slowed (figs. 16.5, 16.6, 16.7). Seals then remained in somewhat more defined geographic areas for periods of around 36 (females, SD = 5.2 days) to 51 days (males, SD = 6.4 days). We refer to those areas as foraging areas and define them according to periods when distances covered between days during three or more consecutive days were less than 32 km, to distinguish them from rapid northward movements away from San Miguel Island in March and similar southward movements when seals were returning to the island to molt. We refer to the latter as north and south transits, respectively. South transits to molting beaches from foraging areas took females around 15 days and males around 31 days (table 16.2), traveling at minimum speeds of 90 to 100 km/day ( = 1.04–1.15 m/sec.). Foraging areas of females (figs. 16.5, 16.6) were less obvious than those of males, whose day-to-day movements in northern areas were small and highly concentrated (fig. 16.7). Female foraging areas therefore appear to be series of high-density clusters of daily locations rather than the single clusters characteristic of males (figs. 16.5, 16.6, 16.7).

Females covered at least 5,500 km during their postbreeding migrations and males at least 11,100 km. Seals remained in deep water (from one to

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Fig. 16.1
Depths of all dives made each day for 5 northern elephant seal
females during their postbreeding migrations in 1990.

several thousand or more meters) throughout their postbreeding migrations. Although males traveled through female foraging areas, between 40° and 48°N latitude, they did not linger there but continued rapidly north to the Gulf of Alaska and the eastern Aleutian Islands. Although the 1989 and 1990 foraging areas of some males overlapped, dives made in those areas

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Fig. 16.2
Depths of all dives made each day for 4 adult northern elephant
seal males during their postbreeding migrations in 1989.

were shallower in 1990 (µ = 318 m, SEM = 56.2) than they were in 1989 (µ = 415.7 m, SEM = 24.4; p < .01).

Dive depths were similar among all females, and dives made in foraging areas were deeper than those made during north or south transits (table 16.1). Similarly, depths of foraging area dives of males were usually deeper than transit area dives (table 16.2). Dives of 3 males in 1990 were notable exceptions; seals 90640 and particularly 90480 spent substantial periods at

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Fig. 16.3
Depths of all dives made each day for 4 adult northern elephant
seal males during their postbreeding migrations in 1990.

shallow depths, and there was much less variation around maximum depth during those periods compared to the records of other males (figs. 16.2, 16.3). The patterns of these 2 males while in foraging areas differed fundamentally in this way from those of females. But the dive depths of 3 other males (89030, 89750, 90680) in their foraging areas south of the eastern Aleutian Islands were similar to dive depths of females that foraged in areas far to the south (tables 16.1, 16.2; figs. 16.2, 16.3, 16.4).

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Fig. 16.4
Postbreeding season dive statistics for adult female and male northern elephant
seals ranging from San Miguel Island, California (individual seal identification
numbers are along the x axis; bars are standard deviations; there
are no location records for male 89120).

― 297 ―

TABLE 16.1 Depths of dives of adult female northern elephant seals during different stages of their postbreeding migrations.
Seal		North transit	Foraging area	South transit	Total
90290	Mean	402.5	520.1	508.2	502.6
	SD	112.0	135.5	153.1	143.8
	n₁	427	2056	1214	3697
	n₂	7	36	20	63
90350	Mean	492.4	553.5	541.1	526.3
	SD	151.5	117.1	146.7	140.6
	n₁	1957	1936	951	4844
	n₂	28	27	14	69
90398	Mean	495.6	538.9	504.3	523.7
	SD	127.7	133.7	180.9	143.2
	n₁	808	2324	666	3798
	n₂	14	40	13	67
90500	Mean	402.4	514.2	468.8	478.7
	SD	116.3	125.5	133.9	133.2
	n₁	1006	2425	908	4339
	n₂	16	39	16	68
90768	Mean	499.6	593.2	578.2	570.8
	SD	138.8	133.8	199.3	155.5
	n₁	705	2006	738	3449
	n₂	14	38	13	65
NOTE: SD = standard deviation; n₁ = number of dives; n₂ = number of days; mean and SD in m.

Discussion

DeLong and Stewart (1991) reported significant diurnal and seasonal variation in dive parameters of adult northern elephant seal males. By simultaneously documenting dive patterns and geographic locations of seals, we have shown that location and migratory behavior (transiting vs. stationary) can explain such apparent changes. The dive patterns that we report here for adult males in 1989 and 1990 are similar to those reported for postbreeding males in 1988 (DeLong and Stewart 1991). Similarly, the dive patterns of females from San Miguel Island in 1990 are similar to those reported by Le Boeuf et al. (1988, 1989) and Le Boeuf (this volume) for females that breed at Año Nuevo. Females appear to be more consistent in their patterns of dive depths, as shown in figure 16.1, than are males, who show greater seasonal and interindividual variability in preferred dive depths (figs. 16.2, 16.3). We are uncertain about the reasons for this difference, but we suspect that the greater physical oceanographic complexity

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TABLE 16.2 Depths of dives of adult male northern elephant seals during different stages of their postbreeding migrations.
Seal		North transit	Foraging area	South transit	Total
89030	Mean	384.2	518.9	428.9	442.4
	SD	117.5	187.2	122.5	158.1
	n₁	2767	2407	1697	6871
	n₂	38	46	39	123
89160	Mean	343.8	372.3	378.1	364.5
	SD	117.4	122.7	134.5	124.5
	n₁	1915	2636	1399	5950
	n₂	35	50	31	116
89408	Mean	348.4	432.8	366.6	386.2
	SD	111.7	120.3	131.1	125.3
	n₁	2530	2550	1171	6251
	n₂	43	44	27	114
89750	Mean	397.4	547	413	469.9
	SD	131.2	208	124	183.4
	n₁	1430	2369	1400	5200
	n₂	35	44	34	113
90480	Mean	208.0	184.4	323.7	222.7
	SD	88.1	37.5	118.9	96.7
	n₁	3553	3561	1870	8984
	n₂	48	50	36	134
90640	Mean	353.9	320.4	387.6	350.3
	SD	90.2	84.7	113.8	96.8
	n₁	3584	2312	1501	7397
	n₂	40	57	31	128
90680	Mean	386.4	524.5	410.2	463.3
	SD	133.7	149.6	170.7	162.5
	n₁	1857	3250	1064	6171
	n₂	31	58	30	119
90870	Mean	218.9	203.1	400.5	236.1
	SD	106.7	95.7	119.5	122.9
	n₁	2271	3982	1039	7292
	n₂	32	60	22	114
NOTE: SD = standard deviation; n₁ = number of dives; n₂ = number of days; mean and SD in m. The first 4 seals are 1989 records, and the latter 4 are from 1990.

― 299 ―

near the Aleutian Islands compared with the central Pacific Subarctic Transition Zone (e.g., Favorite, Diomead, and Nasu 1976; Wetherall 1991) may result in greater regional variability in thermocline depth and vertical water mass discontinuities in the foraging areas of males.

The foraging area dives of seal 90480 are particularly interesting because of his shallow, narrow depth range of dives during a 50-day period. D. E. Crocker et al. (this volume) proposed that this type of diving is indicative of foraging in benthic or epibenthic habitats. However, our location records for seal 90480 indicate that he was feeding in an area where water depths exceeded several thousand meters and that the nearest shallow water areas (i.e., < 300 m) were 241 to 322 km to the north. Further, sea-surface temperatures from other sources compared to the seal's GLTDR SST data confirm the location records. Although some seamounts do rise from the Aleutian Trench near where the seal was foraging, the charted tops of those seamounts are at least several hundred meters below the seal's foraging depths. We attribute the prolonged shallow diving of this seal to his preference for feeding at that depth rather than epibenthic foraging in shallow coastal habitats or on near-surface seamounts or guyots. Similar depth preferences can be seen throughout his north transit period in the high-density depth bands in his dive records (fig. 16.3), although there is greater variability around the high-density bands during those times. Similar clustering of dive depths, which appear to represent interindividual differences in depth preferences, can be seen in the records of other males, although they are most obvious as shallow depth preferences in the records of seals 90870, 90640, and 89160 for portions of their migrations. We also attribute the inter-annual differences in dive depths among males that foraged in similar areas to differences in individual preferences, as the similarities in SSTs in those areas in 1989 and 1990 (compare figs. 16.6 and 16.7 with figs. 16.9 and 16.10) do not suggest any yearly differences in oceanographic conditions there. Canyon, seamount, or current divergence and convergence influences could cause sharp temperature discontinuities between vertical water masses, which would result in substantial local variation in thermocline depth. Such local physical variability would have strong influences on prey distributions. I. L. Boyd and T. Arnbom (1991) showed that the dive depths of one female southern elephant seal were closely linked to temperature characteristics of the water column that were likely influencing prey concentrations. Simultaneous collection of oceanographic data in areas where elephant seals are known to be foraging would be invaluable during future research on elephant seal foraging dynamics.

Adult female and male northern elephant seals that breed at San Miguel Island evidently migrate to different areas of the North Pacific to forage and recover the substantial body mass they lost during breeding season fasts. Females are at sea about half as long as males in spring before they must

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― 301 ―

Fig. 16.5
Migratory routes of 3 northern elephant seal females from San Miguel Island, California, in 1990
(dots represent daily locations for all days that seals were at sea, except for seal 90350
whose instrument's memory filled up as it returned to San Miguel Island;
numbers in lower left corners are seal identification numbers).

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Fig. 16.6
Migratory routes of 2 northern elephant seal females from San Miguel Island, California, in 1990
(dots represent daily locations for all days that seals were at sea).

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Fig. 16.7
Postbreeding migratory routes and foraging areas of 8 northern elephant seal
males in 1989 and 1990 (all days that seals were at sea are plotted).

return to land to molt (tables 16.1, 16.2). This difference may explain why females do not continue to travel northward to the areas where males forage. A round-trip alone to those areas without lingering there would take around 60 days. It is intriguing, though, that males do not remain in the southern areas where females forage even though there appear to be adequate prey resources. Latitudinal differences in prey quality or size may constrain males to continue north in pursuit of more rewarding food resources. Sea-surface temperatures differ by 3 to 5° between the foraging areas of males and females (figs. 16.8, 16.9, 16.10), but we do not think that temperature alone would constrain the distribution of elephant seal adults in the North Pacific. Records from southern elephant seals (Fedak et al., this volume; Slip, Hindell, and Burton, this volume) show that adult males and females may occupy the same coastal Antarctic waters where SSTs are

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Fig. 16.8
Sea-surface temperature measurements recorded by GLTDRs attached to 5 adult
northern elephant seal females during their postbreeding migrations in 1990.

― 305 ―

Fig. 16.9
Sea-surface temperature measurements recorded by GLTDRs attached to 4
adult northern elephant seal males during their postbreeding migrations in 1989.

several degrees colder than in the Gulf of Alaska and the eastern Aleutian Islands where male northern elephant seals forage.

Le Boeuf (this volume) reported that some females from Año Nuevo Island traveled into offshore British Columbia waters to feed, an area of overlap with adult males. We can think of no reason other than time constraints that females from the Channel Islands do not migrate that far north. Certainly, additional studies are needed to examine the biotic and abiotic

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Fig. 16.10
Sea-surface temperature measurements recorded by GLTDRs attached to 4 adult
northern elephant seal males during their postbreeding migrations in 1990.

factors that influence the differential distributions of foraging northern elephant seals during their seasonal migrations.

Our studies indicate that northern elephant seals that breed on San Miguel Island feed in offshore waters in the mesopelagic zone while pursuing vertically migrating prey. Studies of the diets of these seals (Condit and Le Boeuf 1984; Antonelis et al., this volume; Stewart and DeLong

― 307 ―

1993) indicate that those prey are principally squid of several families that are known to be vertical migrators inhabiting mesopelagic habitats (Jefferts 1983; Roper and Young 1975). While in the California Current north of San Miguel Island, male and female elephant seals eat similar prey (Antonelis et al., this volume; Stewart and DeLong, unpubl. data). While transiting through that area, however, males and females are diving to different depths (tables 16.1, 16.2); thus they may be foraging on different size classes of those common prey, but we are unable to confirm this with the available data. Data on the diet of elephant seals in their offshore foraging areas are lacking, but we do know from the stomach contents of other predators (e.g., sperm whales, beaked whales, northern right whale dolphins, Pacific white-sided dolphins, Dall's porpoise) and midwater trawls (R. L. DeLong, unpubl. data) that squid species that are eaten by elephant seals in the southern part of the California Current are also present in the Subarctic Transition Zone, near the eastern Aleutian Islands and in the Gulf of Alaska. We presume that elephant seals are pursuing those prey during most of their periods at sea, but latitudinal differences in squid age and sex composition and behavior could explain the apparent differences in dive depths between male and female northern elephant seals.

Elephant seals depart breeding beaches in lean condition, having lost 40% or more of their body mass during breeding season fasts and lactation (Costa et al. 1986; Deutsch, Haley, and Le Boeuf 1990). We presume that they begin feeding immediately on entering the water, a hypothesis that is supported by diving records and the large increases in mass of males and females by the time they haul out to molt (Le Boeuf et al. 1988, 1989; DeLong and Stewart, unpubl. data). The continuity and characteristics (e.g., diurnal variation in dive depth to presumed depths of the deep scattering layer) of diving also suggest that the seals forage continuously while at sea. The identification of specific destinations where seals, particularly males, spend several weeks or more suggests that some areas of the North Pacific are more productive and energetically more rewarding to northern elephant seals than others. Satellite imagery has revealed dynamic primary productivity south of the eastern Aleutian Islands and in parts of the Gulf of Alaska, particularly in spring and summer when ocean warming and stabilization and longer days promote explosive phytoplankton blooms (Lewis 1989). Elephant seal males are evidently attracted to the deeper biological communities that respond to that heightened surface productivity. Southern elephant seals also appear to be attracted to similar areas of seasonally enhanced biological productivity along the Antarctic Peninsula and to other coastal Antarctic regions (Fedak et al., this volume; Slip, Hindell, and Burton, this volume). Elucidating the cues that attract, guide, and drive elephant seals to those areas will be challenging topics for future research.

The California Current and the North Pacific Transition Zone (NPTZ)

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and Subarctic Frontal Zone in the central North Pacific, where northern elephant seal females migrate to forage, are also known to be highly productive areas. The NPTZ, in particular, attracts large numbers of seabird, turtle, and other marine mammal predators during some seasons (e.g., Wetherall 1991). The near-surface communities of that area have been relatively well studied in recent years, especially since the explosive growth of the drift net squid fishery in the central North Pacific (ibid.). But little is known about the mesopelagic communities in that area which appear to play an important role in the foraging dynamics of female northern elephant seals.

The abilities of northern elephant seals to make long-distance, deep-water, foraging migrations appear to be important adaptations that permit them to range widely during most of the year to accumulate substantial resources that are essential to the energetically demanding terrestrial-bound activities of breeding and molt. Because elephant seals from the San Miguel Island and Año Nuevo rookeries evidently mix in foraging areas yet show strong fidelity to molting and breeding sites, continued study of intercolony differences and similarities in foraging patterns and migrations will be important to understanding the mechanisms that will limit and regulate the growth of each colony and of the still-increasing northern elephant seal population (see Stewart et al., this volume).

Acknowledgments

We thank P. Yochem, B. DeLong, D. DeLong, S. Melin, G. Antonelis, S. Osmek, H. Huber, T. Ragen, and J. Francine for field assistance, the Channel Islands National Park Service for facilitating our research at San Miguel Island, and G. Antonelis, J. Baker, I. Boyd, R. Gentry, J. R. Jehl, B. Le Boeuf, and P. Yochem for comments on earlier drafts of the manuscript. We thank Clairol Research Laboratories for supplying hair dye and bleach products used for marking seals and R. Hill, S. Hill, and M. Braun for consultation during development and field testing of the GLTDRs. GLTDRs were manufactured by Wildlife Computers (Woodinville, Wash.), and VHF transmitters were manufactured by ATS (Isanti, Minn.). BSS was supported by a contract to the U.S. Air Force, Space Systems Division. The research was conducted under Marine Mammal Permit No. 579 to BSS.

References

Boyd, I. L., and T. Arnbom. 1991. Diving behaviour in relation to water temperature in the southern elephant seal: Foraging implications. Polar Biology 11: 259–266.

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Condit, R., and B. J. Le Boeuf. 1984. Feeding habits and feeding grounds of the northern elephant seal. Journal of Mammalogy 65: 281–290.

Costa, D. P., B. J. Le Boeuf, A. C. Huntley, and C. L. Ortiz. 1986. The energetics of lactation in the northern elephant seal. Journal of Zoology 209: 21–33.

DeLong, R. L., and B. S. Stewart, 1991. Diving patterns of northern elephant seal bulls. Marine Mammal Science 7: 369–384.

DeLong, R. L., B. S. Stewart, and R. D. Hill. 1992. Documenting migrations of northern elephant seals using day length. Marine Mammal Science 8: 155–159.

Deutsch, C. J., M. P. Haley, and B. J. Le Boeuf. 1990. Reproductive effort of male northern elephant seals: Estimates from mass loss. Canadian Journal of Zoology 12: 2580–2593.

Favorite, F., A. J. Diomead, and K. Nasu. 1976. Oceanography of the Subarctic Pacific Region, 1960–1971. International North Pacific Fish Commission Bulletin 33: 1–187.

Jefferts, K. 1983. Zoogeography and systematics of cephalopods of the northeastern Pacific Ocean. Ph.D. dissertation, Oregon State University, Corvallis.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Canadian Journal of Zoology 67: 2514–2519.

Lewis, M. R. 1989. The variegated ocean: A view from space. New Scientist 1685: 1–4.

Roper, C. F. E., and R. E. Young. 1975. Vertical distribution of pelagic cephalopods. Smithsonian Contributions to Zoology 209: 1–51.

Stewart, B. S., and R. L. DeLong. 1990. Sexual differences in migrations and foraging behavior northern elephant seals. American Zoologist 30: 44A.

———. 1993. Seasonal dispersion and habitat use of foraging northern elephant seals. In Marine Mammals: Advances in Behavioral and Population Biology , ed. I. L. Boyd, 179–194. Symposia of the Zoological Society of London no. 66. London: Oxford University Press.

Wetherall, J. A., ed. 1991. Biology, oceanography, and fisheries in the North Pacific Transition Zone and Subarctic Frontal Zone. NOAA Technical Report NMFS 105: 1–110.

Zar, J. 1984. Biostatistical Analysis . Englewood Cliffs, N.J.: Prentice-Hall.

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Seventeen—
Functional Analysis of Dive Types of Female Northern Elephant Seals

Tomohiro Asaga, Yasuhiko Naito, Burney J. Le Boeuf, and Haruo Sakurai

ABSTRACT. The aim of this study was to elucidate the function of individual dive types observed in the dive records of female elephant seals, Mirounga angustirostris . Free-ranging dive records spanning 29 to 81 days were obtained from three adult females from Año Nuevo, California, in 1990, using time-depth recorders glued to the pelage on their backs.

Type D dives, assumed to serve pelagic foraging, (1) accounted for 75 to 80% of all dives, (2) occurred in series with a mean length of 10.1 to 22.9 dives, (3) had a bottom of dive element that accounted for 28 to 44% of the total dive duration, and (4) exhibited longer durations and deeper depths during the day than at night. Type A, or "transit," dives were sparsely and widely distributed in the record, accounting for only 1.7 to 7.1% of all dives; they rarely occurred in a series and were the deepest dives observed in all records. Type C dives accounted for 2.6 to 6.8% of all dives, and they were the shallowest dives. They occurred in series with a mean of 3.6 to 4.7 dives. The second descent segment of these dives, which accounted for 52 to 58% of the total dive duration, showed a 30 to 83% reduction in descent rate over the preceding descent segment. There was an inverse relationship between Type D and Type C dive frequency of occurrence as a function of time of day; C dives peaked between 0400 and 1000 hours, the time interval when D dives were least frequent.

The result of this study are consistent with the hypothesis derived from swim speed analysis that Type A, D, and C dives serve transit, pelagic foraging, and physiological processing functions, respectively.

By providing a continuous record of the duration and depth of dives, time-depth recorders (TDRs) provide insights into the at-sea behavior of marine mammals. Data from TDRs allowed us to focus on the individual dives of northern elephant seals, M. angustirostris , with the aim of elucidating their function and role in foraging.

The diving pattern of northern elephant seals differs in many respects

― 311 ―

from that of other pinnipeds. After lactation and weaning their pups, adult females go to sea to feed for 2½ months. During this period, their dives are long and deep. Mean dive depth is 446 to 544 m, and mean dive duration is 17.1 to 22.5 minutes (Naito et al. 1989; Le Boeuf et al. 1989). Sea lions (Zalophus californianus and Z. c. wollabaeki ) and fur seals (Callorhinus ursinus, Arctocephalus gazella, A. pusillus, A. australis , and A. galapagoensis ) dive to mean depths of less than 100 m, and mean dive durations are less than 3 minutes (Feldkamp, DeLong, and Antonelis 1989; Gentry, Kooyman, and Goebel 1986). Weddell seals, Leptonychotes weddelli , dive to less than 200 m most of the time, and more than half of their dives are less than 10 minutes in duration (Kooyman 1989). Elephant seals dive deeper than sperm whales, Physeter catodon , who dive to mean depths of 314 to 382 m, with most dives being less than 500 m (Papastavrou, Smith, and Whitehead 1989). These comparisons suggest that northern elephant seals dive longer and deeper than other pinnipeds and most whales.

Several studies have showed that many diving mammals dive in bouts, a series of dives over a certain period of time; diving bouts are followed by rest (Gentry, Kooyman, and Goebel 1986). Northern elephant seals do not dive in bouts but rather dive continuously for the duration that they are at sea. The dive bouts of Weddell seals, California sea lions, and fur seals last for several hours (Feldkamp, DeLong, and Antonelis 1989; Kooyman 1989; Kooyman et al. 1980), and so do those of blue-eyed shags, Paracrocorax atriceps , and Adélie penguins, Pygoscelis adeliae (Croxall et al. 1991; Naito et al. 1989). Female northern elephant seals dive continuously, sometimes up to 2½ months at a stretch during which the seal may exhibit more than 5,000 dives with only short surface intervals of less than 3 minutes between dives (Le Boeuf et al. 1989). Thus, an analysis of dive bouts, the usual approach in studying otariid diving behavior, is not applicable to the study of elephant seals. This discrepancy suggests that elephant seal diving differs fundamentally from the diving behavior of otariids.

Among California sea lions and northern fur seals, there may be rest at the surface, rest on land, or transit to foraging areas between dive bouts (Feldkamp, DeLong, and Antonelis 1989; Kooyman and Gentry 1986). These activities are also observed in gentoo penguins, Pygoscelis papua , and chinstrap penguins, P. antarctica (Trivelpiece et al. 1986). The diving behavior of northern elephant seals is devoid of swimming at the surface (Le Boeuf et al. 1992; see chap. 10), and it is not likely that they sleep at the surface (Le Boeuf et al. 1988). This is important for understanding their diving behavior, their migrations to foraging areas, and their rest or sleep activities at sea. There are temporal and frequency differences in dive types that we think elucidate the function of their unusual diving behavior.

In this study, we analyze the distribution of distinguishable dive types of free-ranging female northern elephant seals during the 2½-month period at

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sea after breeding. Our investigation is aimed at understanding the function of dives in relation to foraging and in elucidating their physiological basis.

Methods

The field aspects of this study were conducted at Año Nuevo Point, California, in 1988. Three adult female northern elephant seals were immobilized with ketamine hydrochloride (Briggs et al. 1975) during mid-February near the end of their lactation periods. A TDR and a radio transmitter (Advanced Telemetry Systems, Bethel, Minn.) were attached to the pelage of the back above the shoulders of each female with marine epoxy (Evercoat Ten-Set, Fibre-Evercoat Co., Cincinnati, Ohio). Each seal was weighed at this time (see Le Boeuf et al. 1988 for method).

The TDR (Naito et al. 1989) was 52 mm in diameter and 193 mm in length and weighed 980 g in air. It was housed in an aluminum casing that withstood pressures to 3,000 m in depth. The instrument contained a diamond stylus that inscribed a line on aluminum-coated paper (20 µ thick) proportional to water pressure. The motor was capable of running for 130 days, being powered with two 1.5 v lithium batteries. The depth range was 0 to 900 m. Recording error was estimated at less than 2% of depth and duration.

When the seals returned to the rookery in May, each one was weighed and the TDRs recovered. The recording paper was subsequently enlarged 14½ times with a reader-printer (Minolta PR507). From the strip chart records, the dives for each female were classified into five dive types based on their time-depth profiles (fig. 17.1). This classification is based on that of B. J. Le Boeuf et al. (1988) with little modification and is the same classification used in Le Boeuf et al. (1988) with little modification and is the same classification used in Le Boeuf et al. (1992) and D. E. Crocker et al. (this vol.). Type A dives have a straight descent to a sharp point, then direct ascent to the surface. Type B dives are similar except that the bottom of the dive is rounded. Both A and B dives have no bottom time. Type C dives have direct descent to a depth, at which point the descent rate decreases dramatically until the bottom of the dive, then following a rather sharp inflection point, ascent to the surface is direct. Type D dives are characterized by direct descent to a depth, at which point there occur 2 to 12 vertical excursions or "wiggles," ending in direct ascent to the surface. Type E dives show direct descent to the bottom of the dive, which is flat, and end in direct ascent to the surface. Dives that could not be put into one of these categories were excluded from analysis. Type E dives in this study correspond to Type E and F dives in Le Boeuf et al. (1988).

A Hitachi H-F8844-65 was used to digitize the dives. Each classifiable dive was digitized with 3 to 5 points (fig. 17.1), which gave a measure of dive depth, duration, and descent and ascent rates. The minimum mea-

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Fig. 17.1
Schematic profiles of five dive types observed in the dive records of northern
elephant seals (adapted from Le Boeuf et al. 1992). The points of each dive
type were digitized to determine dive elements.

sured value of surface intervals (SIs) was 0.4 minutes, set by the time resolution of the instrument. SIs greater than 10 minutes, extended surface intervals (ESIs), were excluded from statistical analysis.

In an attempt to elucidate the temporal patterning of dive types and their function, we analyzed the temporal patterning of each dive type. For analytical purposes, we defined a dive sequence as a series of dives of the same type bordered by a different dive type or an ESI. That is, we regarded a change in dive type or a surface interval of 10 minutes or more as an interruption signaling the end of a dive type sequence and the dives following a change in dive type or an ESI as the beginning of a new dive type sequence. An additional criterion was that a dive type sequence contain a minimum of three dives.

Results

All females returned to the breeding site. Their TDRs were recovered, and they were weighed. All females gained a mean of 1.0 kg/day, an indication that they succeeded in foraging and were not impeded by the instruments.

Summary Statistics

The entire dive records of two females, Tuf (81 days at sea) and Tow (64 days at sea), were obtained. For the third subject, Vi, the first 48 days of 77 days at sea were recorded; the last 29 days of the record were lost due to a tear in the recording paper. Summary statistics for all females are shown in table 17.1. Diving performance was similar to that of eight females reported in Le Boeuf et al. (1988).

Dive Type Distribution and Temporal Pattern

To clarify the temporal frequency of each dive type, we divided each record into three periods: (1) beginning—the first five days; (2) end—the last five days; and (3) middle—the entire rest of the record. Half of the Type B

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TABLE 17.1 Summary statistics for 3 adult females.
Seal	Recording duration (days)	Total no. of dives	Mean ± SD dive depth (m)	Max. dive depth (m)	Mean ± SD dive duration (min)	Max. dive duration (min)	Mean ± SD surface intervals (min)
Tuf	81	5657	524 ± 126	1093	18.2 ± 3.7	44.4	2.0 ± 0.7
Vi	48	3260	519 ± 136	1131	20.2 ± 4.3	45.0	1.6 ± 0.8
Tow	64	3640	446 ± 125	1250	22.5 ± 5.0	50.1	2.4 ± 0.8

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TABLE 17.2 Percentage of the various dive types in each dive period: beginning (first 5 days in a dive record), end (last 5 days in a dive record), and middle (intervening days).
Seal	Dive periods	Dive types
Seal	Dive periods	A	B	C	D	E
Tuf	Beginning	0.9	1.9	0.2	1.8	0.4
	Middle	7.1	2.1	6.8	74.4	0
	End	0.1	0.1	0.2	3.6	0.6
	Total	8.1	4.1	7.2	79.8	1.0
Vi	Beginning	0	7.6	0.2	2.2	0
	Middle	7.1	2.7	7.2	78.8	0
	End	—	—	—	—	—
	Total	7.1	10.3	7.4	81.1	0
Tow	Beginning	1.5	1.9	0	3.7	0.6
	Middle	1.7	2.2	2.6	79.6	0
	End	0.2	0.7	0	4.6	0.7
	Total	3.4	4.8	2.6	87.9	1.3

dives and all Type E dives occurred during the beginning and end periods (table 17.2). The mean depth of dives during these periods was not stable compared to dives in the middle period. Because dive depth is constrained by the shallow ocean floor between the rookery and the continental slope (Le Boeuf et al. 1988; Le Boeuf et al. 1989), the dive records for the beginning and end periods of each record were excluded from analysis. That is, all analysis here excludes the first five days of all records and the last five days of the records of females Tuf and Tow.

D dives were the dominant dive type in the middle period of all records (fig. 17.2). These dives occurred in long series. Type C dives occurred more frequently than Type A dives, except for female Tuf, and Type C dives occurred several times every day, except for female Tow. Type C dives were the majority of dives (68%) following ESIs. Type A dives occurred unpredictably. There were no Type E dives, and Type B dives were rare (2.1–2.7% of all dives); consequently, these dive types are excluded from further analysis.

Characteristics of Dive Parameters

Dive Depth-Duration Ratio

We tested the dive depth-duration difference among dive types. The mean dive depth-duration ratio of A, C, and D dives was 29.5 to 35.9, 13.7 to 21.2, and 22.4 to 31.3, respectively. Differences in these ratios among dive types were significant for all females (Mann-Whitney U = 13.3, p < .05). This indicates that the classification by dive depth-duration profiles was suitable for dive type analysis.

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Fig. 17.2
The dive records of 3 females showing the distribution of A, C, and D dive types during the middle period at sea.
This excludes the first five days of each record, when the animal is going from shallow to deep water, and the
last five days, when the reverse occurred.

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TABLE 17.3 Summary statistics of dive elements for three type dives.
Dive type	Seal	Mean ± SD dive depth (m)	Maximum dive depth (m)	Mean ± SD duration (min)	Maximum dive duration (min)	Mean ± SD surface intervals (min)	Mean ± SD bottom time^a(min)	Mean ± SD descent rate^b(m/sec)	Mean ± SD ascent rate (m/sec)
A	Tuf	594 ± 123	1093	16.7 ± 3.5	40.7	2.0 ± 0.7	—	0.80 ± 0.16	2.69 ± 1.06
	Vi	654 ± 239	1131	18.2 ± 6.0	36.8	1.8 ± 1.0	—	1.12 ± 0.28	1.35 ± 0.53
	Tow	547 ± 234	1250	18.8 ± 6.8	34.2	2.2 ± 0.9	—	0.82 ± 0.27	1.34 ± 0.52
C	Tuf	479 ± 92	791	22.7 ± 3.9	35.7	2.0 ± 0.8	13.1 ± 3.3	0.82 ± 0.16 (0.34 ± 0.06)	1.79 ± 0.90
	Vi	470 ± 79	662	25.5 ± 5.1	45.0	1.7 ± 0.8	13.3 ± 3.6	1.79 ± 0.82 (0.31 ± 0.11)	0.87 ± 0.24
	Tow	355 ± 85	583	26.4 ± 6.8	50.1	2.6 ± 1.0	14.0 ± 4.3	0.84 ± 0.26 (0.25 ± 0.04)	0.73 ± 0.32
D	Tuf	545 ± 90	834	17.7 ± 2.9	31.7	2.0 ± 0.6	4.9 ± 2.5	0.92 ± 0.16	3.24 ± 2.05
	Vi	558 ± 94	845	19.7 ± 3.0	31.4	1.6 ± 0.7	5.9 ± 2.5	1.33 ± 0.28	1.32 ± 0.69
	Tow	478 ± 105	1002	21.8 ± 3.9	45.9	2.5 ± 0.8	9.7 ± 3.8	0.99 ± 0.21	1.67 ± 0.43
^a Mean bottom time of C-type dives correspond to mean duration in second descent segment.
^b Mean descent rate of C-type dives correspond to that in first descent segment; mean descent rate in second descent segment is given in parentheses.

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Dive Depth, Dive Duration, and Surface Intervals

Table 17.3 shows that the mean depths of Type A dives were significantly deeper in all records than other dive types (t = 3.4, p < .05). Indeed, most dives (64–92%) deeper than 800 m were Type A dives, and these were the maximum depth dives for all females. In contrast, Type C dives were significantly shallower than other dive types (t = 13.3, p < .05). The longest mean dive durations of all females were Type C dives (t = 6.5, p < .05).

There were no significant differences in SIs among dive types in all females except for SIs following Tow's Type A dives, which were significantly longer than those of other females (t = 2.5, p < .05).

Bottom Time and Descent and Ascent Rates

The mean bottom duration of Type D dives accounted for 28 to 44% of the total duration of dives. The mean duration of the second descent segment of Type C dives (fig. 17.1) took up 52 to 58% of the total duration of the dives.

The mean descent rate during the second descent segment of Type C dives was significantly slower than in any other dive type (t = 8.8, p < .05). The mean descent rate during this segment represents a 30 to 83% reduction over the descent during the first descent segment of Type C dives. In addition, the mean descent rates between A and D dives, except for Vi, were statistically significant (t = 5.8, p < .05). The mean ascent rate of Type C dives was slower than that of other dive types (t = 5.2, p < .05).

Interrelationships between Dive Elements

Correlations between dive depth, dive duration, bottom time, and descent and ascent rates are shown in table 17.4. Significant correlations were observed between dive depth and dive duration for all dive types and all females. The positive relationship between these two variables was highest for Type C dives and lowest for Type D dives. The relationship between transit time and depth of Type D dives was strong for all females.

For Type C dives, there were high and positive correlations between dive depth and the duration of the second descent segment, as well as between total dive duration and the second descent segment. For Type D dives, there were weak negative correlations between dive depth and bottom duration. There were positive correlations between total dive duration and duration at the bottom of dives. Weak relationships were in evidence between dive depth and descent rate, total duration and descent rate, and total duration and ascent rate.

Diel Pattern

Number of Dives

There was an inverse relationship in the daily frequency pattern of C and D dives in all females (fig. 17.3). Type C dives peaked

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TABLE 17.4 Correlation coefficients between the dive elements of the major dive types for each female.
	Type	Seals	r *	Equation
Duration vs. depth	A	Tuf	0.32	y = 0.017x + 6.557
		Vi	0.70	y = 0.024x + 2.786
		Tow	0.36	y = 0.118x + 9.084
	C	Tuf	0.50	y = 0.028x + 9.089
		Vi	0.25	y = 0.023x + 14.573
		Tow	0.54	y = 0.065x + 3.298
	D	Tuf	0.35	y = 0.012x + 11.082
		Vi	0.47	y = 0.017x + 10.146
		Tow	0.13	y = 0.005x + 19.404
Transit vs. depth	D	Tuf	0.43	y = 0.019x + 2.191
		Vi	0.48	y = 0.019x + 3.251
		Tow	0.51	y = 0.019x + 3.03
Bottom^a vs. depth	C	Tuf	0.47	y = 0.019x + 3.904
		Vi	0.20	y = 0.014x + 6.704
		Tow	0.61	y = 0.043x – 1.089
	D	Tuf	–0.05	y = 0.007x + 8.883
		Vi	–0.10	y = 0.002x + 6.897
		Tow	–0.24	y = 0.014x + 16.366
Bottom^a vs. duration	C	Tuf	0.52	y = 0.602x – 0.569
		Vi	0.54	y = 0.546x – 0.597
		Tow	0.59	y = 0.513x + 0.478
	D	Tuf	0.25	y = 0.326x – 0.848
		Vi	0.38	y = 0.462x – 3.157
		Tow	0.45	y = 0.654x – 4.516
Descent rate vs. depth	D	Tuf	0.10	y = 0.001x + 0.664
		Vi	0.15	y = 0.001x + 0.894
		Tow	0.25	y = 0.001x + 0.577
Descent rate vs. duration	D	Tuf	–0.22	y = 0.016x + 1.208
		Vi	–0.10	y = 0.017x + 1.660
		Tow	–0.24	y = 0.018x + 1.373
Ascent rate vs. duration	D	Tuf	–0.15	y = 0.039x + 2.673
		Vi	–0.16	y = 0.010x + 1.116
		Tow	–0.25	y = 0.016x + 1.165
^a Bottom duration of C-type dives are equal to the duration in second descent segment.
* All correlations significant at p < .10 level.

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Fig. 17.3
A frequency distribution of three dive types as a function of time
of day for each of 3 females.

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Fig. 17.4
Mean dive duration and mean bottom time of D-type dives
as a function of time of day for 3 females.

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in frequency between 0400 and 1000 hours, when Type D dives were most infrequent. Type A dives did not vary systematically as a function of time of day.

Dive Elements

We describe the daily rhythm of dive elements of Type D dives only because the frequency of other dive types was low and did not vary with time of day.

Mean dive duration and mean bottom duration of Type D dives were longer during the day than at night (fig. 17.4). The time when these durations were longest corresponded with the modal frequency of Type C dives. To further investigate this association, we selected 10 Type A, C, and D dives at random, each of which was preceded and followed by a series of 10 consecutive Type D dives. We then tested for differences in dive durations of the Type D dives as a function of the preceding dive type. The majority of dive durations of Type D dives, 70 to 100% of them, increased following Type C dives but showed little increase after Type A dives (0–10%) and Type D dives (0–30%).

The mean dive depths of Tuf and Vi during the day (0600–2000 hrs) were deeper than at night (2100–0500 hrs), but this was not the case for female Tow. Mean SI, descent rate, and ascent rate for Type D dives did not vary with hour of the day for all females.

Dive Type Sequence

Type A dives showed the lowest number of dives in a sequence among the three dive types (table 17.5). Except for female Tow, 80% or more of Type C dives occurred in series. The mean duration of the second descent segment of Type C dives was about half of the dive sequence duration. The depth where the second descent segment began in Type C dives was constant in a dive sequence regardless of its maximum depth (F = 3.41, p < .01). The dive duration of Type C dives gradually increased toward the end of a dive sequence (50–80% of total dive sequence number).

More than 90% of Type D dives occurred in dive sequences. The total duration of these dive sequences in a day was 15.5 to 20.5 hours. The bottom duration corresponded to 24 to 39% of dive sequence duration, indicating that females remained at the maximum depth of dives for 3.6 to 8 hours every day.

Discussion

This study provides additional information on the putative function of dive types in elephant seals. Le Boeuf et al. (1988) hypothesized that Type D dives serve foraging. Using information provided by measurement of swim

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TABLE 17.5 Dive sequence characteristics for 3 adult female northern elephant seals.
Dive type	Subjects	Dive no.	Dives incl. (% )	Sequence no. per day	Mean ± SD sequence duration (hr)	Mean dive no.	Mean no. range	% Sequence underwater ± SD	% Sequence bottom time^a ± SD
A	Tuf	14	13	0.2	1.1 ± 0.2	3.4	3–4	92.8 ± 1.4	—
	Vi	—	—	—	—	—	—	—	—
	Tow	1	3	0.01	—	—	—	—	—
C	Tuf	60	81	0.9	1.9 ± 1.0	4.7	3–22	93.7 ± 2.4	55.5 ± 5.2
	Vi	39	82	0.9	1.8 ± 0.5	4.3	3–8	94.3 ± 2.4	52.0 ± 4.9
	Tow	10	39	0.2	1.6 ± 0.3	3.6	3–6	92.1 ± 2.9	50.8 ± 5.3
D	Tuf	357	93	5.0	3.1 ± 3.0	10.1	3–72	91.3 ± 1.6	23.5 ± 6.4
	Vi	97	99	2.3	8.7 ± 7.0	22.9	3–82	92.5 ± 1.8	27.8 ± 5.6
	Tow	147	99	2.7	7.6 ± 6.5	18.9	3–78	91.0 ± 2.3	39.2 ± 7.9
^a Bottom time of C dives refers to the duration of the second descent segment.

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speed, Le Boeuf et al. (1992) attributed a similar function to Type D dives and added that they served pelagic foraging. They further hypothesized that Type E dives served benthic foraging, especially in males, that Type A and B dives functioned primarily as transit dives during migrations, and that Type C dives were processing dives that facilitated digestion, were instrumental in the removal of anaerobic metabolites, or served rest or sleep. We discuss the relevance of the present data to the presumed function of dive types.

Type D dives made up 75% or more of the dive types in each of the dive records in this study, a percentage similar to that reported for females in an earlier study (Le Boeuf et al. 1988). The predominance of Type D dives—coupled with the large proportion of time spent at the dive bottom (34.0 ± 8.7% of the total dive duration), the up-and-down activity of the seal at the dive bottom, the rapid descent and ascent rates, and the length and duration of a series of these dives—is consistent with the hypothesis that they serve foraging (Le Boeuf et al. 1988; Le Boeuf et al. 1992).

This hypothesis is bolstered by a number of ancillary findings regarding Type D dives.

1. They occurred regularly throughout the period at sea with the exception of the first few days at sea and the last few days at sea when the animal was moving across the continental shelf. This suggests that feeding is not restricted to foraging areas but occurs throughout migration (Le Boeuf et al. 1992; see Le Boeuf, this volume).

2. The mean dive duration, mean bottom-of-dive duration, and mean dive depth of these dives are greater during the day than at night. This is consistent with the hypothesis that Type D dives reflect foraging in the deep scattering layer, which contains prey that come closer to the surface at night and retreat to depths at midday (Le Boeuf et al. 1988).

3. The frequency of Type D dives was lowest during the day when the frequency of Type C dives peaked. This is consistent with the idea that the latter type are processing dives and that the best time for the seal to reduce its dive rate and rest, digest food, or get rid of anaerobic metabolites is when it must dive deepest for prey. Data from ongoing studies show that Type D dives occur with great frequency in both sexes and in seals ranging in age from weanlings on their first trip to sea to adults (Le Boeuf, this volume).

Le Boeuf et al. (1992) hypothesized that A and B dives were primarily transit dives. This was based in part on the fact that the mean horizontal distance covered, 1.3 km, was greater for this dive than for other dive types (0.6–1.1 km), and they argued further that this dive shape was most

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efficient for horizontal travel. Our data show that Type A dives are on average deeper and of shorter duration than Type D dives. The shorter duration of Type A dives might be due to the greater energy expenditure required to go deeper, which puts a lower limit on dive duration. The swim speed data indicate that foraging may occur during transit. The consistency of Type A dives in females throughout the length of the periods at sea supports this idea. We suggest further that the dives might have an exploratory function. This is consistent with the dive's depth and its spiked bottom; at depth, the seal may decide to abort the dive and ascend when it does not find suitable prey.

With the exception of M. A. Hindell's dive analysis on southern elephant seals, M. leonina (Hindell 1990; Hindell, Slip, and Burton 1991), no other investigators have attempted detailed descriptions of dive types in other species. Dives resembling the A-type dives of elephant seals, however, have been observed in northern fur seals and South African fur seals (Gentry, Kooyman, and Goebel 1986; Kooyman and Gentry 1986); 90% of the dives of these animals had spiked bottoms resembling the shape of A-type dives of elephant seals. The investigators suggested that these dives served foraging. G. L. Kooyman (1981) came to the same conclusion about some of the dives of Weddell seals.

Several findings in this study are consistent with the hypothesis that Type C dives have a processing function and that the animal is drifting down during the second segment of descent (Le Boeuf et al. 1992). First, Type C dives are as long as the dive durations of the other dive types, even though reduced energy expenditure is expected due to the animal drifting down during the second segment of descent rather than powering down as in Type A and D dives. Second, the mean distance traveled during these dives (0.6 km) is less than for any other dive type (ibid.). Third, Type C dives were the most common dive type following an extended surface interval. Since we know from the swim speed study (ibid.) that the animal is not swimming, this is a strong argument that it is resting. The contiguity of ESIs and Type C dives suggests that the latter may have a "processing" function similar to that of ESIs. Fourth, Type D dives that followed Type C dives had a longer mean duration than normal. This suggests that the animal was now rested or in some way better prepared to dive long. Last, the peak frequency of Type C dives, coupled with the low frequency of Type D dives, suggests that these two dive types have opposite functions.

We conclude that our analysis of dive types is consistent with the hypotheses advanced regarding their function (ibid.). The ultimate tests of these hypotheses will be empirical and will require more sophisticated diving instruments than the ones currently in use.

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Acknowledgments

We thank D. Costa and P. Thorson for their support with fieldwork at Año Nuevo Point, California, and N. Satoh, head of the computer center of the National Institute of Polar Research in Tokyo, and his staff for their advice and help with data processing. This study was financed in part by a grant from the National Science Foundation.

References

Briggs, G. D., R. V. Hendrickson, and B. J. Le Boeuf. 1975. Ketamine immobilization of northern elephant seals. Journal of the American Veterinary Medicine Association 167: 546–548.

Croxall, J. P., Y. Naito, A. Kato, P. Rothery, and D. R. Briggs. 1991. Diving patterns and performance in the Antarctic blue-eyed shag, Phalacrocorax atriceps. Journal of Zoology, London 225: 177–199.

Feldkamp, S. D., R. L. DeLong, and G. A. Antonelis. 1989. Diving patterns of California sea lions, Zalophus californianus. Canadian Journal of Zoology 67: 872–883.

Gentry, R. L., G. L. Kooyman, and M. E. Goebel. 1986. Feeding and diving behavior of northern fur seals. In Fur Seals: Maternal Strategies on Land , ed. R. L. Gentry and G. L. Kooyman, 61–78. Princeton University Press.

Hindell, M. A. 1990. Population dynamics and diving behaviour of a declining population of southern elephant seals. Ph.D. dissertation, University of Queensland, Australia.

Kooyman, G. L. 1981. Weddell Seal: Consummate Diver . Cambridge: Cambridge University Press.

———. 1989. Diverse Divers: Physiology and Behavior . Berlin: Springer Verlag.

Kooyman, G. L., and R. L. Gentry. 1986. Diving behavior of South African fur seals. In Fur Seals: Maternal Strategies on Land , ed. R. L. Gentry and G. L. Kooyman, 142–152. Princeton: Princeton University Press.

Kooyman, G. L., E. A. Wahrenbrock, M. A. Castellini, R. W. Davis, and E. E. Sinnett. 1980. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: Evidence of preferred pathways from blood chemistry and behavior. Journal of Comparative Physiology 138: 335–346.

Le Boeuf, B. J., D. P. Costa, A. C. Huntley, and S. D. Feldkamp. 1988. Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 66: 446–458.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, continuous, deep diving by northern elephant seals. Canadian Journal of Zoology 67: 2514–2519.

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Naito, Y., B. J. Le Boeuf, T. Asaga, and A. C. Huntley. 1989. Long-term diving records of an adult female northern elephant seal. Nankyoku Shiryo (Antarctic Record ) 33(1): 1–9.

Papastavrou, V., S. C. Smith, and H. Whitehead. 1989. Diving behavior of sperm whale, Physeter macrocephalus , off the Galápagos Islands. Canadian Journal of Zoology 67: 839–846.

Trivelpiece, W. Z., J. L. Bengtson, S. G. Trivelpiece, and N. J. Volkman. 1986. Foraging behavior of gentoo and chinstrap penguins as determined by new radiotelemetry techniques. Auk 103: 777–781.

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Eighteen—
Swim Speed and Dive Function in a Female Northern Elephant Seal

Daniel E. Crocker, Burney J. Le Boeuf, Yasuhiko Naito, Tomohiro Asaga, and Daniel P. Costa

ABSTRACT. The objective of this chapter is to discuss the behavioral and metabolic implications of swim speed data recorded from a northern elephant seal during free-ranging diving. Variation in swim speed elucidates the observed diving pattern and aids in understanding foraging tactics.

The data were obtained from a swim speed-distance meter and a time-depth recorder attached to the shoulders of an 8-year-old female at Año Nuevo, California, in February 1990. Swim speed, distance, depth, and duration of dives were recorded continuously for 29 days.

Average swim speeds ranged from 0.91 to 1.66 m/sec for all dive segments save one. These numbers are similar to those obtained from diving otariids and fall within the predicted cruising speed range for an aquatic animal less than 3 m in length. Horizontal swim speed during transit is similar to indirect measurements of transit velocity made by other investigators. Based on swim speed and distance traveled for each of five dive types apparent in the record, the two-dimensional shape of the various dive types observed, and the temporal patterning of dive types, we hypothesize that the four most common dive types observed serve three general functions: transit, foraging (pelagic and benthic), and internal physiological processes.

The advent of the use of time-depth recorder (TDR) technology has opened up a new level of behavioral and physiological analysis of diving in marine mammals (Kooyman 1965, 1968; Kooyman, Billups, and Farwell 1983; Guppy et al. 1986; Hill et al. 1987; Le Boeuf et al. 1989). Changes in depth, however, represent only one dimension of the behavior exhibited by an animal as it moves through the water column. Crucial to the understanding and expansion of the ideas arising from the TDR data is the development and deployment of an instrument that measures swim velocity. Historically, these data have been hard to acquire. Recent development and deployment of a number of different velocity instruments have allowed researchers to

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begin to incorporate this measurement into their analyses of diving behavior and physiology (Ponganis et al. 1990, 1992; Le Boeuf et al. 1992).

Long duration divers like elephant seals must reconcile the conflicting metabolic demands of responses to hypoxia and exercise. The physiological adaptations with which the animal defends against hypoxia must be balanced against the rate of oxygen utilization required for active swimming. Much of what is known about the relationship between nondiving swimming velocity and metabolism comes from exercise studies in harbor seals, Phoca vitulina (Davis, Williams, and Kooyman 1985; Williams, Kooyman, and Croll 1990), gray seals, Halichoerus grypus (Fedak 1986), and California sea lions, Zalophus californianus (Feldkamp 1987; Williams, Kooyman, and Croll 1990). The sea lion study showed that oxygen consumption increased as an exponential function of swimming velocity. In contrast, investigations on freely diving Weddell seals, Leptonychotes weddelli (Kooyman et al. 1973), showed that reductions in metabolic rate together with extremely efficient swimming hydrodynamics allow the seal to swim while diving at only slightly higher than resting energy costs.

Swim velocity measured in a freely diving elephant seal offers an important clue to understanding the balance achieved between the opposing demands of exercise and apnea. The rarity of extended recovery periods in northern elephant seals, Mirounga angustirostris , and its implication of aerobic metabolism further underscores the importance of understanding this balance. Variations in swim velocity can offer significant insights toward understanding foraging tactics as well as other behaviors exhibited during diving.

Through simultaneous deployment of velocity and TDR instruments, the animal's swim velocity can be combined with the vertical component of its movements derived from the TDR data to map dives in two dimensions. This allows calculation of angles of descent and ascent as well as the horizontal component of the animal's movement. The shapes derived from this two-dimensional analysis and the energetic and behavioral implications derived from the velocity data allow us to begin to interpret the functions of the dive types classified as a result of the TDR data.

In this chapter, we discuss the behavioral and metabolic implications of swim speeds and the diving record obtained from an 8-year-old postpartum female northern elephant seal in 1990. We summarize the data from B. J. Le Boeuf et al. (1992) and offer further discussion of the results.

Measuring Swim Speed

The swim velocity instrument or, more accurately, the swim speed-distance meter (SSDM) measured distance traveled by the seal as a function of time

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Fig. 18.1
Schematic representations of five dive types that appear in northern elephant seal
diving records. The dive types depicted are idealized and not adjusted for depth
or time. (Adapted from Le Boeuf et al. 1992.)

from which swim speed was calculated. The SSDM and TDR used in this analysis are described in detail in Le Boeuf et al. (1992).

Dive Type Classification

From the TDR data, each dive was classified into one of five categories and a category of unclassifiable dives from shape on a strip chart representation of the time-depth profile (fig. 18.1). Most unclassifiable dives appeared to be composites of two of the five categories. Dive types were classified as follows: Type A dives, characterized by direct descent to a sharp inflection point, followed by direct ascent to the surface; Type B dives, characterized by direct descent ending in a rounded bottom, followed by direct ascent to the surface; Type C dives, characterized by direct descent to depth, at which point descent rate decreases noticeably but proceeds directly to the bottom of the dive, followed by direct ascent to the surface; Type D dives, characterized by direct descent to a depth, followed by 2 to 12 vertical excursions, followed by direct ascent to the surface; and Type E dives, characterized by direct descent to a flat bottom followed by direct ascent to the surface.

Swim Speed and Distance Calculations

Swim speeds were calculated for dive segments and paired with the TDR data to draw two-dimensional vector triangles, the missing dimension being the spatial orientation of the animal at any time. The horizontal distances calculated in this analysis do not equate to linear swimming distance as the animal could have been turning during the course of a dive. These distances calculated are simply the horizontal component of the animal's movement during the course of a dive segment or dive. As the maximum calibrated speed measured by the instrument was exceeded on some dives,

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all speeds and distances calculated should be considered minimum estimates. Similarly, angles of ascent and descent calculated are maxima. For a detailed explanation of the methods and potential sources of error, see Le Boeuf et al. (1992).

Swim Speed Measurements

Excluding the second descent segment of Type C dives, mean swim speeds for dive segments ranged from 0.91 to 1.66 m/sec. The mean velocity for all segments of all dives was 1.24 ± 0.21 m/sec.

On average, mean descent speeds were 27% faster than ascent speeds. This difference was statistically significant for all dive types. Descent speeds were similar across all dive types except for the second descent segment of Type C dives, which exhibited a significant reduction in swim speed. The second descent segment of Type C dives averaged 0.59 m/sec. in swim speed. Velocity on descent averaged 1.5 m/sec., while ascent and bottom velocity averaged 1.0 m/sec. No swimming was recorded at the surface above the stall speed of the instrument (0.4 m/sec.). Energetic concerns might preclude swimming above this speed due to increased drag at the surface. No swim speeds below 0.4 m/sec. were recorded during diving.

Comparison of Swim Speeds

The swim speeds recorded by the SSDM fall predominantly within the range of 1 to 2 m/sec., suggested by G. L. Kooyman (1989) as the cruising swimming velocity for animals up to 3 m in length. Recent investigations of swimming velocities in otariids (Ponganis et al. 1990) found a similar range for four species (0.9–1.9 m/sec.). It might seem that the larger elephant seal should swim faster than the smaller otariids since drag increases with the surface area or L² , while the power increases directly with muscle volume or L³ , where L = length. Y. U. G. Aleyev (1977) suggests that swim speed varies directly with the frequency of the propulsive movement, which decreases with increasing muscle length, but that the drag/power relationship holds true for animals with a length less than 4.5 m. This would include our experimental animal.

The shorter dive duration, trip duration, energetically costly surface swimming, and different foraging strategies seen in the otariids suggest that a different compromise must be reached between the metabolic requirements of exercise and apnea and may explain the similar swim velocities seen in the long duration diving elephant seals. Swimming at MCT velocities allows an animal to cover a given distance with the minimum total oxygen consumption. If, however, the animal's emphasis is on achieving a lower rate of oxygen consumption and thereby a longer duration dive,

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swimming at lower than MCT velocities might occur. A nonactive swimming or drift component to diving would contribute to this effect.

This idea is further supported by an energetic and physiological comparison of otariids and phocids. Studies have found that four species of lactating otariids expend energy at sea at five times the predicted basal level (Costa and Gentry 1986; Costa, Croxall, and Duck 1989; Costa, Thorson, and Kretzmann 1989; Costa, Antonellis, and DeLong 1990). Metabolic rates of diving elephant seals were estimated from dive durations and available oxygen stores to be only 1.3 times the predicted basal rate. Phocids have increased blood oxygen storage capacity due to a higher hematocrit (Lenfant, Johansen, and Torrance 1970). This increases blood viscosity and reduces optimal oxygen transport (Hedrick, Duffield, and Cornell 1986). Otariids, in contrast, have lower hematocrits that fall within a more optimal range for oxygen transport (Hedrick and Duffield 1991).

Comparison with Other Elephant Seal Investigations

A number of investigators in this volume present average daily transit velocities that allow comparison with the speeds measured by this instrument. We predict that these transit velocities would be somewhat lower than our recorded swim speeds as they ignore the vertical component of the animal's movement and include surface intervals for which our data indicate a lack of swimming. We can derive a comparable measure by dividing the calculated horizontal distance covered for each presumed transit dive by the dive duration. This yields a mean horizontal transit velocity of 1.00 ± 0.46 m/sec.

This speed is similar to the values reported for adult northern elephant seals, 0.89 to 1.03 m/sec. (Le Boeuf, this volume) and 1.04 to 1.15 m/sec. (Stewart and DeLong, this volume), and southern elephant seal females, 0.55 to 1.03 m/sec. (Fedak et al., this volume). D. J. Slip, M. A. Hindell, and H. R. Burton (this volume) present a range of transit speeds for southern elephant seals from 80 to 240 km/day or 0.9 to 2.8 m/sec. While the lower part of this range is similar to our measurements, a more complete accounting of which individuals exhibited higher transit speeds is required for meaningful comparison.

If we assume similar geometries to those obtained in this study, a transit speed of 2.8 m/sec. seems somewhat high. Using angles of ascent and descent derived from this study and assuming a nonswimming, surface interval of 1.5 minutes and an average dive duration of 20 minutes, a horizontal transit speed of 2.8 m/sec. yields a sustained swimming velocity of 3.4 m/sec. for the transit period. This is clearly beyond the capabilities exhibited by our female.

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One possible explanation is that elephant seals might sometimes adopt a different mode of swimming that maximizes transit velocity at the expense of the total dive duration. This could represent flexibility in diving behavior that might be essential in a high predation environment where the depth of dives might be bathymetrically constrained. This alteration in swimming mode would be evident in the relationship between transit velocity and dive duration. A number of new records obtained from southern elephant seals show a dramatic shift from high transit velocity, short duration dives over the continental shelf to the more typical diving pattern as the animals reach deep water (C. Campagna, B. J. Le Boeuf, unpubl. data).

Recent deployment of velocity instruments on translocated yearling elephant seals has measured swim velocities similar to those presented in this study (R. Andrews, pers. comm.; P. Thorson, pers. comm.).

Speed Changes during Dive Segments

Since the sampling regimen of the SSDM was linear with respect to distance, not time, we were unable to assess instantaneous velocity or acceleration. However, numerous instances of what we termed "burst diving," rapid decreases and increases in speed within dive segments, were observed in the data. This level of detail was lost in the average speeds calculated for dive segments. To quantify this aspect of diving behavior, we looked at the variance among speed values within segments of dives. Burst diving occurred predominantly during descent and most often at the bottom of Type D dives. This behavior was significantly less frequent on the ascent segments of all dive types. Changes in swim speed occurred most infrequently during the second descent segment of Type C dives.

Angles of Ascent and Descent and Distance Traveled

Figure 18.2 shows the average two-dimensional plots for each dive type. Angles of descent were on average shallower (30° to 56°) than angles of ascent (52° to 82°). Angles of descent and ascent could not be calculated for Type B dives, due to their rounded bottom. However, the great similarity between Type B and Type A dives in every other aspect of this analysis argued for combining them as Type AB dives for subsequent analysis.

Functions of Dive Types

The data suggest that the different dive types serve three main functions. We hypothesize that Type AB dives may serve as transit dives. The average two-dimensional shape of Type A and B dives is notable for the great amount of horizontal distance covered: the seal averaged 1.2 km per dive.

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Fig. 18.2
Two-dimensional shapes for each of the five
classified dive types, showing mean angles
of ascent and descent and mean distance
covered for segments of dives.
(Adapted from Le Boeuf et al. 1992.)

Similarly, Type A and B dives had the shallowest angles of ascent and descent. Moreover, there is the strong degree of asymmetry seen in these dives. Horizontal distance covered was approximately three times greater on descent than ascent.

Returning to the central question of oxygen utilization and the balance between swimming effort and responses to hypoxia, we propose that this

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asymmetry represents a more energetically efficient way of covering horizontal distance. If the animal is negatively buoyant, it could drift down or swim aided by gravity and then swim actively to the surface. On an average Type AB dive, this would enable the animal to cover 1.2 km of horizontal distance, while actively swimming or swimming unaided by buoyancy for only half of that distance. The energy savings would have to be substantial, as actual distance covered is increased. However as metabolic expenditure is directly related to swimming effort, this is possible.

Type AB dives were interspersed throughout the record but occurred in greatest numbers in long uninterrupted series during the first 19 days at sea. The strong asymmetry in shape, great horizontal distance covered, and temporal patterning of Type AB dives are all consistent with their hypothesized function as transit dives.

The data suggest that Type C dives may be "processing" dives, where behavior and energy utilization are focused on internal processes such as digestion and clearing of metabolites rather than external processes. Type C dives showed the shortest horizontal distance covered. The second descent segment of Type C dives averaged about a third of the speed of other segments of all dive types. This reduction in swim speed tended to occur at the same depth within a series of Type C dives. On average, this slow swimming period accounted for almost half (46.9%) of a Type C dive's duration.

It has been hypothesized that diving mammals are trying to maximize their time underwater while foraging (Kooyman 1981; Fedak, Pullen, and Kanwisher 1988; Kramer 1988). While this idea is not necessarily applicable to other types of dives, we argue that the pattern of C dives exhibited by northern elephant seals suggests its application to Type C dives. These dives occur in distinct bouts, with little variance in the inflection depth or second segment descent rate. It is unreasonable that the seal would return to the surface with remaining oxygen reserves and then spend potential foraging time and energy to return to depth and repeat the same behavior. If this is true—and whatever happens metabolically during diving is a constant across dive types—a dive type with a significantly lower swim speed would be expected to have a significantly longer duration. However, the mean duration of Type C dives (21.4 min.) is not significantly different from that of Type AB dives (21.6 min.), where the animal swims faster and covers on average twice the horizontal distance. Analysis of TDR records from 23 elephant seals including yearlings, adult females, and adult males show that Type C dive durations are not significantly different from Type A dive durations (Paired t-test, t = –0.05, p > .05; B. Le Boeuf, P. Morris, and D. Crocker, unpubl. data). From this, we infer that something different is happening metabolically during Type C dives.

Oxygen savings from reduced swim speed might be used in the process-

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ing of food or metabolites incurred during diving. Oxygen savings could be used in perfusion of organs that incurred restricted blood flow on other types of dives. Type C dives did not appear in the record until day 17. This coincides with a relative decrease in the frequency of Type AB dives and a concomitant increase in the frequency of Type D dives.

Feeding studies on northern elephant seals have shown increases in metabolic rate averaging 65% 4 to 5 hours after feeding (P. Thorson, pers. comm.). If foraging occurs in long bouts, the increase in energy expenditure due to digestion might negatively impact the balance between the increased oxygen utilization required for active foraging and the hypoxia of diving. However, if the metabolic changes associated with food processing could be coupled temporally with decreased oxygen requirements due to decreased swimming effort, this impact could be significantly lessened.

A subsequent paper will test a number of predictions based on this idea in an attempt to demonstrate a more conclusive pattern of evidence supporting this hypothesis. The real test, however, will be to attempt to illicit this dive type in the homing paradigm (see Le Boeuf, this volume) and to directly measure perfusion of the digestive tract and swimming muscles. The metabolic issue raised here, the overall significantly lower swim speed, and the temporal patterning of this dive type in the record, are consistent with Type C dives serving a physiological process.

Type D and Type E dives appear to have characteristics consistent with foraging. The vertical excursions seen at the bottom of Type D dives are consistent with searching, pursuing, and capturing prey. Type D dives occurred in long series and were the most common dive type. Both of these characteristics are consistent with foraging. Type E dives might serve feeding on the bottom, or benthic foraging. These dives also occurred in long series. The depths of the bottom segments within a series of Type E dives were relatively invariant. Though the depth sometimes changed slightly during the course of a bottom segment, the succeeding bottoms in a series appeared to start close to the depth at which the preceding bottom ended. This gives the impression that the animal's movement was following the bottom topography, though geolocation and bottom depths are needed to be conclusive. Moreover, the descent and ascent angles were abrupt in both of these dive types, suggesting that the animal descended directly to a depth where prey were found, spent one-third of the dive's duration foraging, then returned directly to the surface. The increased incidence of speed changes seen in both dive types, especially during the bottom segment of Type D dives, is also consistent with foraging.

A recent investigation of sex differences in foraging patterns in northern elephant seals (Le Boeuf et al. 1993) offers strong support for this characterization of Type D and E dives. Diurnal variation in depth for Type D dives was found which is consistent with movements of the deep scattering layer

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and was not evident in any other dive type. This dive type might account for most of the diurnal variation in dive depth and duration reported by many investigators.

A strong association of Type E dives with coastal regions was also demonstrated. However, the geolocation of many of these dives might be sufficiently far away from the continental shelf to preclude benthic foraging. Stewart and DeLong (this volume) also argue that the geolocation of their Type E dives precludes benthic foraging. However, a recent shipboard validation study of a geolocation TDR revealed a strong, consistent, southernly bias to geolocation estimates in the area in question (S. Blackwell and B. J. Le Boeuf, unpubl. data). This bias might preclude the use of light-level geolocation to obtain precise correlations between diving behavior and bathymetric features.

This analysis represents a first effort at using velocity and TDR instruments together to investigate questions concerning diving behavior. New and better instruments that allow assessment of instantaneous velocity and acceleration will allow a much finer level of analysis than that presented here. Future generations of instruments will also have higher upper ranges so that a more accurate picture will emerge. However, the relationships between the numbers in this study allowed us to formulate hypotheses that will form the basis of future investigations.

References

Aleyev, Y. U. G. 1977. Nekton . The Hague: W. Junk.

Briggs, G. D., R. V. Henrickson, and B. J. Le Boeuf. 1975. Ketamine immobilization of northern elephant seals. Journal of the American Veterinary Medicine Association 167: 546–548.

Costa, D. P., G. P. Antonelis, and R. DeLong. 1990. Effects of El Niño on the foraging energetics of the California sea lion. In Effects of El Niño on Pinnipeds , ed. F. Trillmich and K. Ono, 156–165. Berlin: Springer Verlag.

Costa, D. P., J. P. Croxall, and C. Duck. 1989. Foraging energetics of Antartic fur seals, Arctocephalus gazella , in relation to changes in prey availability. Ecology 70: 596–606.

Costa, D. P., and R. L. Gentry. 1986. Reproductive energetics of the northern fur seal. In Fur Seals: Maternal Strategies on Land and at Sea , ed. R. L. Gentry and G. L. Kooyman, 79–101. Princeton: Princeton University Press.

Costa, D. P., P. H. Thorson, and M. Kretzmann. 1989. Diving and foraging energetics of the Australian sea lion, Neophoca cinera. American Zoology 29: 71A.

Davis, R. W., T. M. Williams, and G. L. Kooyman. 1985. Swimming metabolism of yearling and adult harbor seals, Phoca vitulina. Physiological Zoology 58: 590–596.

Fedak, M. A. 1986. Diving and exercise in seals: A benthic perspective. In Diving in Animals and Man , ed. A. Brubakk, J. W. Kanwisher, and G. Sundnes, 11–32. Kongsvold Symposium, Royal Norwegian Society of Sciences and Letters, June 3–7, 1985. Trondheim: Tapir.

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Fedak, M. A., M. R. Pullen, and J. Kanwisher. 1988. Circulatory responses of seals to periodic breathing: Heart rate and breathing during exercise and diving in the laboratory and open sea. Canadian Journal of Zoology 66: 63–69.

Feldkamp, S. D. 1987. Swimming in the California sea lion: Morphometrics, drag, and energetics. Journal of Experimental Biology 131: 117–136.

Guppy, M., R. D. Hill, R. C. Schneider, J. Qvist, G. C. Liggins, W. M. Zapol, and P. W. Hochachka. 1986. Micro-computer-assisted metabolic studies of voluntary diving of Weddell seals. American Journal of Physiology 250: R175–R187.

Hedrick, M. S., and D. A. Duffield. 1991. Haematological and rheological characteristics of blood in seven marine mammal species: Physiological implications for diving behavior. Journal of Zoology, London 225: 273–283.

Hill, R. D., R. C. Schneider, G. C. Liggins, A. H. Schuette, R. L. Elliot, M. Guppy, P. W. Hochachka, J. Qvist, K. J. Falke, and W. Zapol. 1987. Heart rate and body temperature during free diving of Weddell seals. American Journal of Physiology 253: R344–R351.

Kooyman, G. L. 1965. Techniques used in measuring diving capacities of Weddell seals. Polar Record 12: 391–394.

———. 1968. An analysis of some behavioral and physiological characteristics related to diving in the Weddell seal. In Antarctic Research Series , vol. 11, Biology of the Antarctic Seas III , ed. W. L. Schmitt and G. A. Llano, 227–261. Washington, D.C.: American Geophysical Union.

———. 1981. Weddell Seal: Consummate Diver . Cambridge: Cambridge University Press.

———. 1989. Diverse Divers: Physiology and Behavior . Berlin: Springer Verlag.

Kooyman, G. L., J. O. Billups, and W. D. Farwell. 1983. Two recently developed recorders for monitoring diving activity of marine birds and mammals. In Experimental Biology at Sea , ed. A. G. Macdonald and I. G. Priede, 197–214. London: Academic Press.

Kooyman, G. L., R. L. Gentry, and D. L. Urquhart. 1976. Northern fur seal diving behavior: A new approach to its study. Science 193: 411–412.

Kooyman, G. L., D. H. Kerem, W. B. Campbell, and J. J. Wright. 1973. Pulmonary gas exchange in freely diving Weddell seals (Leptonychotes weddelli ). Respiration Physiology 17: 283–290.

Kramer, D. L. 1988. The behavioral ecology of air breathing by aquatic animals. Canadian Journal of Zoology 66: 89–94.

Le Boeuf, B. J., D. E. Crocker, S. A. Blackwell, P. A. Morris, and P. Thorson. 1993. Sex differences in foraging in northern elephant seals. In Marine Mammals: Advances in Behavioural and Population Biology , ed. I. L. Boyd, 149–178. Symposia of the Zoological Society of London no. 66. London: Oxford University Press.

Le Boeuf, B. J., Y. Naito, T. Asaga, D. E. Crocker, and D. P. Costa. 1992. Swim speed in a female elephant seal: Metabolic and foraging implications. Canadian Journal of Zoology 70: 786–795.

Le Boeuf, B. J., Y. Naito, A. C. Huntley, and T. Asaga. 1989. Prolonged, con-

― 339 ―

tinuous, deep diving in female northern elephant seals, Mirounga angustirostris. Canadian Journal of Zoology 67: 2514–2519.

Lenfant, C., K. Johansen, and J. D. Torrance. 1970. Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respiration Physiology 9: 277–286.

Naito, Y., B. J. Le Boeuf, T. Asaga, and A. C. Huntley. 1989. Long-term diving records of an adult female northern elephant seal. Antarctic Record 33: 1–9.

Ponganis, P. J., R. L. Gentry, E. P. Ponganis, and K. V. Ponganis. 1992. Analysis of swim velocities during deep and shallow dives of two northern fur seals, Callorhinus ursinus. Marine Mammal Science 8: 69–75.

Ponganis, P. J., E. P. Ponganis, K. V. Ponganis, G. L. Kooyman, R. L. Gentry, and F. Trillmich. 1990. Swimming velocities in otariids. Canadian Journal of Zoology 68: 2105–2112.

Williams, T. M., G. L. Kooyman, and D. A. Croll. 1990. The effect of submergence on heart rate and oxygen consumption of swimming seals and sea lions. Comparative Physiology 160B: 637–644.

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PART III— DIVING AND FORAGING

Twelve— Theory of Geolocation by Light Levels

Roger D. Hill

The Theory

Sources of Error

Equinoxes

Accuracy of the Light-level Measurements

Atmospheric Aberration

Animal Diving at Dawn or Dusk

Animal Moving between Dawn and Dusk

The Equations

Presentation of Errors

Practical Considerations

References

Thirteen— Variation in the Diving Pattern of Northern Elephant Seals with Age, Mass, Sex, and Reproductive Condition

Burney J. Le Boeuf

Generalizations

Variation in Dive Pattern

Early Development

First Trip to Sea

Juvenile Diving

Age/Mass Effects

Dive Duration

Dive Depth

Reproductive Condition

Sex

Dive Pattern

Migratory Routes

Homing and Translocation

Conclusion

Acknowledgments

References

Fourteen— Diving Behavior of Southern Elephant Seals from Macquarie Island: An Overview

David J. Slip, Mark A. Hindell, and Harry R. Burton

Deployment and Recovery of Recorders

Location of Animals

Dive Patterns

Characterization of Dive Types

Type 1 Dives

Type 2 Dives

Type 3 Dives

Type 4 Dives

Type 5 Dives

Type 6 Dives

Maximum Depths and Durations

Physiological Implications

Acknowledgments

References

Fifteen— Developmental Aspects of Diving in Northern Elephant Seal Pups

Philip H. Thorson and Burney J. Le Boeuf

Methods

Diving Behavior near the Rookery during the Postweaning Fast

Oxygen Storage Capacity

Myoglobin Assay

Metabolic Studies

Free-ranging Dive Pattern at Sea

Results

Diving Behavior near the Rookery during the Postweaning Fast

Changes in Physiological Variables over the First Eight Months of Life

Metabolic Studies in Seawater Tanks during the Postweaning Fast

Diving Behavior during the First Foraging Trip to Sea

Discussion

Oxygen Storage Capacity

Metabolic Rate

Diving Behavior on the First Trip to Sea

Acknowledgments

References

Sixteen— Postbreeding Foraging Migrations of Northern Elephant Seals

Brent S. Stewart and Robert L. DeLong

Methods

Results

Discussion

Acknowledgments

References

Seventeen— Functional Analysis of Dive Types of Female Northern Elephant Seals

Tomohiro Asaga, Yasuhiko Naito, Burney J. Le Boeuf, and Haruo Sakurai

Methods

Results

Summary Statistics

Dive Type Distribution and Temporal Pattern

PART III—
DIVING AND FORAGING

Twelve—
Theory of Geolocation by Light Levels

Thirteen—
Variation in the Diving Pattern of Northern Elephant Seals with Age, Mass, Sex, and Reproductive Condition

Fourteen—
Diving Behavior of Southern Elephant Seals from Macquarie Island:
An Overview

Fifteen—
Developmental Aspects of Diving in Northern Elephant Seal Pups

Sixteen—
Postbreeding Foraging Migrations of Northern Elephant Seals

Seventeen—
Functional Analysis of Dive Types of Female Northern Elephant Seals

Eighteen—
Swim Speed and Dive Function in a Female Northern Elephant Seal