AESTRACT
Ihis study of the underwater behavior of harbor seals
at Hopkins Marine Life Refuge comprises two papers: Fart I
considers aspects of aquatic sleep patterns, while Fart II
describes an underwater vocalization behavior, referred to
as "rumbling".
Harbor seals were found to sleep in the shallow waters
near their haul-out. In the majority of cases a seal slept
in a prone position amongst the surf grass. Sleep was most
frequently observed at mid-tide levels. Fups were obseryed
in aquatic sleep only at the water's surface.
Rumbling is a highly stereotyped behavior involving
both vocalizing seals (rumblers) and hon-vocalizing
attendants. The low-frequency vocalization is performed by
males only and in a localized portion of the study site.
Attendants, also males, participate in the behavior by
situating themselves alongside the vocalizing seal so that
their heads are in close proximity. It is suggested that
this behavior is linked to reproductive activity.
INTRODUCTION
Due to the general wariness of the animals, few
behavioral studies have focused on the underwater activities
of free-ranging harbor seals, Ehoca vitulina (see, for
example, Venables and Venables 1759; Sullivan 1781; Allen
1785: Renouf and Lawson 1787). The seals of the Hopkins
Marine Life Refuge, Facific Grove, California, have become
acclimated to human activity on shore and in the water.
While snorkeling I was able to observe patterns in
underwater sleep and also noticed a highly stereotyped
underwater vocalization behavior, hereafter referred to as
"rumbling".
MATERIOLS AND METHODS
The study was conducted from April 25 to June 4, 1990
and consisted of approimately S hours of underwater
observation. Figure I illustrates the study site, located
in the area of Hopkins Marine Life Hefuge between Ogassiz
Heach and Seal Racks. I chose this site because it is a
reasonable area to observe over the time designated for this
study and because it is immediately adjacent to pne of two
groups of racks used as a haul-out by the approkimately 100
harbor seals resident to the refuge. The zeal population
consistsof bath sexes of all age classes, though it has
only become a birthing area in the past few years. The site
has a granite and sand substrate predominated by Phyllospadix
and algal growth; makimum depth is approximately ap m. In an
etfort to insure that all portions of the site were surveyed
adequately, it was divided into six manageable regions.
Ihis notation also allowed me to document the approximate
location of any observed behaviors.
All observations were made while snorkeling during
daylight hours, with notes recorded on underwater paper
mounted on a plexiglass clipboard. Observations were
conducted after dark on only three pecasions for reasons of
visibility and personal safety. In addition, the seals are
reported to be night foragers and therefore absent from the
haul-out area at this time (Osborn 185). I saw no seals in
the water or on the haul-out during my night sessions.
FART I: SLEEF
INTRODUCTION
While precise definitions of sleep are difficult, the
behavior can be recognized in mammals according to four
criteria (Campbell and Tobler 1984): (1) a characteristic
posture, (2) maintained quiescence, (3) a raised threshold
Of arousal, and (4) reversibility of the behavioral state.
There is no standardized method of distinguishing between
"drowsiness" and "sleep"
Captive gray seals have been described as sleeping at
the surtace of the tank with the nostrils clear of the
water, then sinking below the surface for up to four minutes
betore rising again to breathe (Ridqway et al 1975).
Similarly, the harbor seal is known to engage in what is
known as bottling, where the animal bobs at the surface with
the snout pointing directly overhead. Sullivan (1779)
observed an adult female harbor seal to alternate between
Bottling and sinking underwater in the same location for 68
minutes continucusly. However, the behavior of the seal
onme it is underwater, including the four sleep criteria
previously discussed, have never been described,
MATERIALS AND METHODS
I regarded as "sleep" any behavior in which the seal
remained in a characteristic sleep posture for at least ten
seconds, including those animals which may have been
more
properly described as "drowsy". Occasipnally a seal would
adopt such a posture for the required time but would moye
its head alertly as if looking for something in the water:
these instances were not recorded as sleep.
RESULTS
Festure:
In 887 of all recorded observations (n=42 of 48) the
sleeping seal was lying prone on the substrate. There were
a tew cases of a seal lying on its side or back. On four
occasions a seal was observed rolling back and forth in the
surge. In all cases the body was fully extended, with the
foreflippers resting at the seal's side.
Site:
Seals were found sleeping in thick patches of
Fhyllospadix in 757 of all cases (ne of 48). The grass
provides excellent camouflage as it moves with the surge and
is swept over the seal. In about half of these gmass¬
covered cases (5, n-19 of 3o) the seal was actually wedged
under something, a rock ledge or a railroad tie, which had
grass growing on or arpund it. The remainder of
observations found the seal sleeping on shorter vegetation
or on the open sandy substrate.
I was unable to identify individuals well enough to
determine whether each seal has its own preferred, specific
site.
Arousal:
It was not uncommon for my approach to awaken a
sleeping seal. However, often times the result was merely
that the seal would open its eyes and look around slowly.
apparently not awaking completely. Frequently then the seal
would remain in place. On many occasions I was able to swim
very close to a sleeping seal without eliciting any
response. Similarly, I often observed other seals to swim
within a foot of a sleeping seal without causing any
disturbance. The average underwater sleep duration was
about 1.5 minutes (x-1.6 min., n-35, range 10 seconds to 7.3
min.).
Related locomotor activities:
In all cases where the seal was wedged under something.
it approached its sleep site by swimming into it. Howeyer.
in 527 of the total observations where the data was taken
(n-12 of 23), the seal sank rather than swam to the
substrate. This sinking from the surface to the substrate
was achieved without any discernible motion of the fore- or
hindtlippers and without releasing bubbles. The motion
appears to be consistent with previous observations of
sinking and resurfacing, mentioned earlier. Seals surfaced
for air immediately upon leaving the sleep site in 877 (n=20
Ot 23) of all cases for which these data were recorded.
Diurnal patterns:
Prequency of sleep observations was related to tidal
Height, the greatest frequency occurring at mid-tide, rather
than time of day (Figure 2).
Note on pupE:
All above results reflect only the activities of seals
at least one year old; no pups were observed sleeping in
this manner. Instead, pups floated at the surface with the
back exposed and head and tail underwater. They maintained
this posture for minutes at a time and were often easily
approached while doing so.
DISCUSSION
In summary, we see that the underwater resting behavior
of harbor seals does meet the definition of sleep as
outlinedlearlier. The seals maintain a characteristic prone
Posture amongst the surf grass for up to seven minutes at a
time and, presumably during deeper stages of sleep, are not
easily aroused by the observer or other seals.
he seals were observed to sleep underwater most
frequently at mid-tide levels. This result is surprising
for two reasons: (1) it has been hypothesized that harbor
seals sleep in water as a result of being forced off the
haul-out by the rising tide (Riedman 1990), and (2) there
does not seem to be a significant rise in general aquatic
activity at higher tides, though there are much fewer seals
on the haul-out. Therefore, it would seem that many seals
leave the area altogether at high tide.
There are several biases introduced by the methods of
this study. While not likely causing a disturbance in the
general postural and site characteristics of the behavior.
my presence as a foreign observer of the seals probably did
interfere in the accuracy of measurements of sleep duration
and in the alternating surface/substrate patterns. In
addition, I am sure that I simply did not notice a
signiticant amount of sleep activity because the surf grass
provided such excellent camouflage. There were instances
when I lost track of the location of a sleeping seal, even
though I had seen it just a moment before, because of the
constant motion of the grass. Finally, my study focused
only on the underwater portion of sleep behavior. The
results should be combined with observations from land that
follow the seal as it floats and sinks in the water. In
this manner a more accurate portrayal of the in-water
sleeping abilities of the harbor seal can be compiled.
FORT II: RUMBLING
INTFODUCTION
Renouf and Lawson (1987) found that adult harbor seals
play socially only during the mating season, which extends
from April through June in California (Bonner 1990). Ralls
et al (1985) hypothesize that phocids are considered one of
the least vocal pinnipeds because most of their
Vocalizations occur underwater; they note that yocalization
rates are probably greatest during the mating season and
that sezually mature males are the most vocal animals. Yet
the best documented underwater activities of the harbor seal
are the clicking vocalizations thought to be associated with
echolocation (see, for example, Schevill, Watkins and Hay
1953; Renouf 1989). During my studies of underwater sleep,
I noticed a previously undescribed underwater vocalization
behavior, which I refer to as "rumbling". performed
exclusively by males and possibly associated with
reproductive behavior.
MOTERIALS AND METHODS
Vocalizations were recorded with a hydrophone and a
Sony portable recorder. Sonograms of the vocalizations were
produced on the Multigon Industries Uniscan II. Vided
recordings were made on two separate occasions using a Super
VHS format recorder in a waterproof housing. I used the
tapes primarily for illustrative purposes, only including
individual discrete bouts of behavior for analysis.
HESULTS
There are two possible roles played by male harbor
seals involved in rumbling behavior, both illustrated in
figure 3: the vocalizing seal and non-vocalizing
attendants. Vocalizing seals are not always attended.
The
age of the males involved is unknown, but in the majority of
observations the rumbling seal had a pronounced swelling
along the penile line, indicative of a certain degree of
sexual maturity. In addition, all but three isolated
observations occurred in an approximately 100 sg. m. region
of the study site immediately in front of one end of the
haul-out (see figure 1). The behavioral pattern seemed to be
distributed through daylight hours and not related to the
tidal cycle.
In the stereotypical pattern of rumbling behavior, as a
seal swims towards the substrate and arrives within a few
feet of the bottom, it rolls onto its back so that it reste
parallel to the substrate, upside down. Its throat and
chest region swell and its head begins to lift slightly
while the tail remains in place. Suddenly there follows a
full body contraction similar to that made by a person with
a severe cough. This motiom results in a loud burst of
sound, like a pop, followed by a low frequency rumbling roar
which lasts approximately three to five seconds. Sonograms
Ot three separate vocalizations made by two unattended seals
are very similar and show that the band of maximum energy
occurs between 150 and 200 Hz, with no harmonics (figure 4).
The seal may rumble several times while still on its
back. I will refer to each discrete period which the seal
spends on its back as one rumbling bout; therefore, the seal
may perform several vocalizations per bout. During the
vocalizations the swelling of the throat and chest
decreases, though there is not necessarily an accompanying
release of bubbles. In fact, there are generally few
bubbles, if any, released during the vocalizations.
Unce the seal completes this rumbling bout, it returns
to its upright position, briefly scans the area visually.
and then either rolls over to perform another bout in
appruximately the same location or completes the entire
rumbling episode by swimming to the surface. I define an
episode as that perind of time from the first rumbling bout
to the time when the seal either returns to the surface or
escapes my field of vision. On average a seal will perform
approximately three outs per episode( -.2
bouts/episode, range 1 to 7 bouts/episode, S.D. - 1.47
bouts/episode. n - 71). In addition, frequently the same
seal will perform a long series of episodes per obeervation
period, always returning to the same spot to vocalize.
bserved one seal perform a continucus series ofI
10
episodes, consisting of a combined total of 116 bouts.
during a one hour and forty minute period.
Rumbling behavior was observed during 15 of 25 separate
Observational sessions. On nine of these 15 occasions the
Fumbling seal was accompanied by at least one other seal
during one or more bouts. Though I could only consistently
identify four rumbling seals for the duration of the study,
it is possible that a total of up to thirty different
individuals were observed rumbling.
By my definition, an accompanying or attending seal may
assume any of a wide variety of body postures as long as the
following criterion is met: an attending seal alighs itself
alongside the vocalizing seal so that their heads are within
a tew inches of each other, if not in actual physical
contact. This posture is held only for the duration of an
individual bout; between bouts the accompanying seal often
swims away. Of the 358 bouts observed 68.47 (n-245) were
umattended, 24.97 (n=89) had one attendant, 6.17 (n=22) had
two attendants, and 0.67 (n-2) had three attendants. During
any one observational period, the members of a rumbling
behavior group remained consistent: that is, the same
Fumbling seal would have the same attending seals, though
not all of those attendants would necessarily be present at
all times. However, determining whether these groups
remained constant across
observational
periods was
difficult.
Although there was generally very little antagonism
amongst the seals involved in rumbling behavior. I did
11
observe at least one case of aggression and/or competition
between most of the possible combinations of rumbling roles:
between two attendants, between an attendant and rumbler.
between two rumblers, and between a rumbler and a seal not
participating in the behavior at all. While two or more
attendants never fought during bouts, they frequently fought
between bouts, though never to the extent of drawing blood.
For example, during one morning observation session I
noticed that one attendant was consistently head-thrusting
and scratching a second attendant. As the session
continued, the more aggressive attendant was frequently the
only accompanying seal.
When I returned to observe in the
atternoon, the same rumbling seal was performing and the
more aggressive attendant was still accompanying, but the
sther attendant never again appeared.
Un a separate occasion I observed a seal which
consistently had attendants. One of these attendants twice
performed a rumbling episode while the one it had been
attending was at the surface. However, this attendant¬
turned-rumbler vocalized alone, while the original rumbling
seal soon returned to perform more episodes and was still
attended by the thers of the group.
Humblers were also aggressive at times. On one
occasion I observed an unattended, vocalizing seal roll onto
its stomach, look around, spot another rumbling seal about
15 teet away, and approach this second seal as if to become
an attendant. Instead it began to scratch at the thrat of
12
the second seal with its foreflippers until that seal swam
away. Ihen the first seal began another rumbling bout in
this new location.
In another case of aggression on the part of the
rumbler, a male which had been attended while rumbling
earlier was rumbling alone. (This was the same seal which I
was able to observe for an hour and forty minutes
continuously.)
After vocalizing, he righted himself.
retracted his head so that his neck appeared thick, then
Burst upwards towards one of a pair of seals which had been
interacting at the surface. I was unable to determine the
sex of either of these seals. After a brief encounter. the
attacked seal left the area and the rumbler foreflipper
splashed (as described by Sullivan 1981) a short distance
away. However, the pair at the surface regrouped and was
attacked in the same manner by the rumbler three more times.
with the rumbler foreflipper splashing after each encounter.
Ihere were only two cases which definitely involyed
female seals, though not as attendant or rumbler. In one
instance a female rested under a nearby rock ledge while
rumbling occurred. However, she did nut seem to notice the
activity and the males behaved according to the standard
patterm.
During another session a male and
remale were
interacting far from the usual rumbling site. They were
tumbling around each other near the surface, biting each
uther's neck and grabbing each other with the foreflippers.
s I approached, the female swam away and the male rolled
onto his back and began swimming upside-down at a fairly
rapid pace. Occasionally as he swam he rumbled, which was
quite different from the basically stationary pattern I had
seen betore. He swam in a wide circle without surfacing or
righting himself, eventually arriving back at the original
site to which the female had returned. He righted himself
as soon as he saw her and they began playing again.
This
pattern was repeated twice, after which the male hauled out.
DISCUSSION
There is a wide variety of evidence to suggest that the
rumbling behavior is linked to mating. A somewhat similar
behavior known as ballooning is performed by a closely
related species, the spotted seal, Ehoca largha, exclusively
during its mating season (Beier and Wartzok 1979).
Ballooning is a male behavior in which the seal lies on the
bottom of the tank on his stomach and retracts his head so
that the thoracic region appears swollen. No vocalizations
appear to e associated with the behavior. However. this
same study also shows that the spotted seal des haye
underwater vocalizations which occur only during the mating
season, though Stirling (1973) found no such vocalizations
Tor the ringed seal, Fhoca hispida. Evelyn Hanggi (personal
communication), recording underwater vocalizations of harbor
seals at Foint Lobos. California, has heard only the
rumbles, and variations on them, and has found that they are
only prominent during May and June. Similarly, I observed
rumbling behavior primarily during May and the beginning of
June. For a review of pinniped vocalizations, refer to
Riedman (1790).
Given that these studies took place during the breeding
season for this species, it is possible that this behavior
is a form of lekking. Bradbury (1981) defines a lek species
as one in which 1) males contribute only gametes to the
next generation; 2) males gather at a site to which females
come and where most mating occurs; 3) this display site
contains no resources found exclusively at the site and
necessary to the females, except for the males themselves:
and 4) the females have a choice of mates. Lek behavior has
already been suggested for another pinniped, the walrus.
Udcbenus rosmarus. The male walrus exhibits acoustical and
visual displays in the water near groups of females,
subadulte, and young resting on the pack ice during their
breeding season (Ray and Watkins 1975). The authors also
suggest that the display may be a means of establishing
underwater territories or dominance hierarchies.
The
amecdotal evidence found in my studies regarding
interactions between vocalizers and attendants might
indicate that the harbor seal rumbling behavior is a
competitive yet nen-violent means of creating a male
hierarthy amongst the seals which vocalize, are attended, or
are attendants.
15
ACKNOWLEDGMENTS
I would like to thank my advisor, Chuck Baxter, for his
helpful suggestions and the loan of various equipment. and
Alan Baldridge for providing much enthusiasm and
encouragement and repeatedly pointing me in the right
direction. Thanks to John Lee, Mark Denny, and Khosrow
Lashkari for their collective attempts to explain acoustics
to me; to Marianne Reidman for her advice and the loan of
her very helpful book; and to Ken Norris and the members of
his lab for allowing me to use the Multigon. I am
particularly thankful to Nicole Crane for the amazing video
and the even more amazing feat of accessing functioning
sonogram equipment.
U course, many thanks go to the other students of
175H. I've never met such a great group!
Finally, for my incredible friend Diane Scott. thank
you for understanding.
LITERATURE CITED
Allen, S.G. 1985. Mating behavior in the harbor seal.
Marine Mammal Science i:84-87.
Beier, J.C. and D. Wartzok. 1979. Mating behaviour of
captive spotted seals (Fhoca langha). Animal Behavior
27:
781.
Bonner, W.N. 1990. The natural history of seals. Facts on
File, Inc., New York, NY.
Bradbury, J.W. 1981. The evolution of leks. Fages 138-167
in H.D. Alexander and D.W. Tinkle, eds. Natural
selection and social behavior: Research and new theory.
Chiron Fress, New York. NY.
Campbell, S.S. and I. Tobler. 1784. Animal sleep: O
review of sleep duration across phylogeny. Neurpscience
& Biobehavioral Reviews 8:267-700.
Osborn, L.S. 1985. Fopulation dynamics, behavior, and the
etfects of disturbance on haulout patterns of the
harbor seal Phoca vitulina richardsi. Senior thesis,
University of California, Santa Cru.
Ralls, K., F. Fiorelli and S. Gish. 1785. Vocalizations
and vocal mimicry in captive harbor seals, Ehoca
vitulina. Canadian Journal of Zoology 6:1050-105a.
Hay.
G.C. and W.A. Watkins. 1975. Social function of
Underwater sounds in the walrus Odobenus rosmarus.
Hapports et Froces-verbaus des Heunions Conseil
Fermanent International pour l'Exploration de la Mer
169: 524-526.
Renouf, D. and J.W. Lawson. 1987. Quantitative aspects of
harbour seal (Ehoca vitulina) play. Journal of Zoology
(London) 212:267-273.
Renouf, D. 1989. Sensory function in the harbor seal.
Scientific American 260:90-95.
Ridgway, S.H., R.J. Harrison, and F.L. Joyce. 1975. Sleep
and cardiac rhythm in the gray seal. Science 187:SS
SS5.
Riedman, M. 1990. The pinnipeds: Seals, sea lions, and
walruses. University of California Press, Berkeley, CO.
Schevill, W.E., W.A. Watkins and C. Ray. 1763. Underwater
sounds of pinnipeds. Science 141:50-53.
Stirling, I. 1973. Vocalization in the ringed seal (Ehoca
hispida). Journal Fisheries Research Board of Canada
J0: 1592-1594.
Sullivan, R.M. 1979. Behavior and ecology of harbor seals,
Ehoca vitulina, along the open coast of northern
Lalifornia. Master's thesis, Humboldt State University,
Sullivan, R.M. 1781. Aquatic displays and interactions in
harbor seals, Ehoca vitulina, with comments on mating
systems. Journal of Mammalogy o2:825-831.
Venables, U.M. and S.V. Venables. 1957. Vernal coition of
the seal, Fheca vitulina, in Scotland. Froceedings of
the loological Society of London 132:665-667.
FIGURE LEGEND
Figure 1: Map of study site
Figure 2: Graph of mean number of underwater sleep obseryations
per hour vs. tidal height. The sine-wave trace
represents a typical daily tide cycle.
Figure 3: Typical posture of rumbling seal (below) and one
attendant.
Figure 4: Sonograms of unattended rumbles. (A) and (B) were
recorded from the same seal.
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