The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke
1 Department of Ecology and Evolutionary Biology, Center for Ocean Health,
Long Marine Laboratory, 100 Shaffer Road, University of California at Santa
Cruz, Santa Cruz, CA 95060, USA
2 University of Texas at Austin, Department of Marine Science, Marine
Science Institute, 750 Channel View Drive, Port Aransas, Texas 78373,
USA
3 Department of Marine Biology, Texas A&M University at Galveston, 5007
Avenue U, Galveston, TX 77553 USA
* Author for correspondence (e-mail: williams{at}biology.ucsc.edu)
Accepted 4 December 2004
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Summary |
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Key words: Weddell seal, Leptonychotes weddellii, dive, oxygen consumption, locomotor cost, plasma lactate, stroke frequency, foraging energetics
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Introduction |
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Energy intake from prey ingestion must exceed these costs if a predator is
to achieve a net positive energy balance. This in turn will dictate the
efficiency of the predator, and ultimately its survival
(Stephens and Krebs,
1986).
For aquatic birds and mammals, the problem of balancing foraging costs and
benefits is complicated by the limited availability of oxygen when diving.
Dunstone and O'Connor
(1979a,b
)
investigated the trade-offs associated with underwater predation by
air-breathing carnivores, using the American mink (Mustela vison
Schreber) hunting fish as a model system. These investigators demonstrated an
interaction between foraging economics, as predicted by optimality models
(Charnov, 1976
), and the
preferred hunting strategies of the mink, as constrained by oxygen reserves.
In this relatively simple situation, foraging economics explained 51% of the
variance in hunting patterns of the mink while oxygen constraints accounted
for another 23%.
Kramer (1988) expanded on
these studies by predicting optimum foraging patterns of diving birds and
mammals based on the physiological and morphological characteristics that
dictate oxygen gain during surface intervals. Theoretically, increased
distance to feeding sites resulted in longer dive durations and surface times
for breathing. Many species of marine mammal fit this pattern
(Costa and Gales, 2003
),
although hunting behavior, type of prey taken and type of dive (e.g.
exploratory versus hunting) can modify the response.
For actively foraging marine mammals, each energetic demand may
simultaneously draw on limited oxygen stores. As a result, the combined
energetic costs of locomotion and digestion while submerged can overwhelm the
metabolic capacity of some marine mammals, forcing a selection between
physiological activities when diving. Indirect evidence is provided from
studies on northern elephant seals, which show a temporal separation between
the cost of diving and of prey assimilation during submergence
(Crocker et al., 1997).
Following possible prey ingestion, elephant seals suspend swimming activity,
which theoretically allocates a greater proportion of the oxygen reserve to
metabolic processes necessary for warming the food, digestion and
assimilation. In this way sequential diving may continue and the seal remains
within its aerobic diving limits as it forages and processes prey. Similarly,
the exceptionally high costs (as estimated from post-dive surface intervals)
associated with lunge feeding by blue whales and fin whales confines
submergence by these huge marine mammals to comparatively short bouts
(Acevedo-Gutierrez et al.,
2002
).
Except for indirect evidence (Ponganis
et al., 1993; Crocker et al.,
1997
; Acevedo-Gutierrez et al.,
2002
) and theoretical models
(Williams et al., 1996
),
little is known regarding the energetic cost of foraging dives in marine
mammals. This is due in part to the difficulty of simultaneously measuring
metabolic rate and foraging behavior in free-ranging diving mammals. To
address this problem, we measured the energetic cost of foraging and
non-foraging dives in Weddell seals by using open flow respirometry and an
isolated ice hole technique coupled with an animal-borne video-data logging
system. Energetic costs associated with locomotion and prey warming and
assimilation were measured, and the contribution of these costs to the total
energetic demands of foraging determined. Using these results, we developed an
energetics model to predict the cost of a dive by Weddell seals, based on
stroking costs and the post-absorptive or post-prandial state of the
animal.
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Materials and methods |
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A climate-controlled research hut was placed over the isolated hole and served as the laboratory for the experiments. Location of the hut and ice hole was approximately 10 km west of Cape Armitage, Ross Island, adjacent to the McMurdo ice shelf.
Animals
Nine adult Weddell seals Leptonychotes weddellii Lesson (1 female,
8 males; body mass=387.4±6.6 kg, mean ±
S.E.M.) were used in these studies. The seals
were captured with a purse-string net on the sea ice near Ross Island and
transported approximately 15 km to the isolated ice hole (1.3 m diameter hole
in a 2.5 m long x 1.5 m wide shelf) that had been cut into the sea ice.
After a 2448 h holding period the animals were instrumented with a
video-data recording system, an indwelling intravertebral extradural vein
catheter and swimming stroke monitor, as described in Davis et al.
(1999). Following the
experiments, the instruments and catheter were removed and the seals returned
to their point of capture.
Aerobic and anaerobic costs of diving
Aerobic costs of diving were determined from the rate of oxygen
consumption, as measured by open flow respirometry
(Williams et al., 2001)
following the protocols of Castellini et al.
(1992
). Breathing by the seals
before and after dives was restricted to a LexanTM dome (2.4 m long
x 1.1 m wide x 0.4 m high) mounted at the water level over the
isolated ice hole. Air was drawn through the chamber using a vacuum pump
(Sears 2.0 hp Wet/Dry Vac; Chicago, IL, USA) at 510550 l
min1. Flow rates were monitored continuously with a dry gas
flow meter (American Meter Co. Inc., DTM-325, San Leandro, CA, USA). At these
flow rates the fractional concentration of oxygen in the dome remained above
0.2000 except for the initial seconds following a dive. Samples of air from
the exhaust port of the dome were dried (Drierite; Hammond Drierite Co.,
Xenia, OH, USA) and scrubbed of carbon dioxide (Sodasorb; Chemetron, St Louis,
MO, USA) before entering an oxygen analyzer (Sable Systems International,
Inc., Henderson, NV, USA; and AEI Technologies S3-A, Pittsburgh, PA, USA). The
percentage of oxygen in the expired air was monitored continuously and
recorded once per second on a personal computer using Sable Systems software.
Rate of oxygen consumption
(
O2) was
calculated using equations from Fedak et al.
(1981
) and an assumed
respiratory quotient of 0.77. This respiratory quotient was later confirmed in
independent tests using simultaneous
O2 and
CO2 measurements
for a subset of the seals. All values were corrected to STPD.
The entire system was calibrated daily with dry ambient air (20.94%
O2) and every 34 days with dry span gases (16.0%
O2) and N2 gas according to Fedak et al.
(1981). The flow of
calibration gases into the dome was controlled and monitored by an electronic
flow meter (Model #FMA-772V; Omega, Manchester, UK) that was accurate to
within 1% of total flow. Calibration of the flow meter was checked before and
after the study with nitrogen gas and a rotameter (Cole-Palmer Instruments,
Chicago, IL, USA). The theoretical fraction of O2 leaving the dome
was calculated according to Davis et al.
(1985
) and compared to
measured values from the oxygen analyzer.
Oxygen consumption during the dive was calculated from the difference
between total recovery oxygen consumption and resting rates in water following
the procedures of Hurley and Costa
(2001) and Scholander
(1940
). Prior to the diving
experiments, baseline post-absorptive oxygen consumption rates were determined
for each Weddell seal resting in the ice hole
(Williams et al., 2001
). These
were later validated with rates determined during prolonged (>20 min) rest
periods between dives by foraging and non-foraging seals. Following a dive,
oxygen consumption was monitored continuously, and diving metabolism
calculated from the recovery oxygen consumed in excess of resting rates for
either post-absorptive or post-prandial seals as determined from feeding
behavior logged by the animal-borne video-data recorder (see below). Only
post-dive recovery periods in which the seals rested quietly and remained on
the surface long enough for oxygen consumption to return to within 2% of
baseline levels were used in this analysis. In this way, the potential effects
of sequential dives on oxygen consumption were avoided.
To assess the contribution of anaerobic metabolism during diving, plasma
lactate concentration was measured in post-dive blood samples drawn from an
indwelling catheter placed in the extradural vein of the seals. Because the
metabolic dome prevented access to the catheter, blood samples were collected
in a separate series of dives covering the range of dive durations observed
for the respirometry tests. Samples (510 ml) were drawn within
1.55.0 min of resurfacing from a dive to correspond with peak recovery
lactate levels (Qvist et al.,
1986). Serial blood samples for seven dives confirmed that peak
changes in pH and [lactate] occurred during this period of recovery. Chilled
blood samples were immediately centrifuged (approximately 1000
g for 10 min) and the plasma stored in cryovials at
30°C until analysis. Total plasma [lactate] was determined using a
portable lactate analyzer (YSI 1500 Sport Lactate Analyzer, Yellow Springs,
OH, USA) calibrated daily with zero and lactate standard solutions.
Foraging behavior
The underwater foraging behavior of the seals was recorded continuously
using a video-data logging system carried by the free-ranging animals. Details
of the instrumentation and attachment procedures have been described
previously by Davis et al.
(1999) and Fuiman et al.
(2002
). Briefly, seals were
sedated with an intramuscular injection of ketamine hydrochloride (2 mg
kg1; Fort Dodge Laboratories, Fort Dodge, IA, USA) and
diazepam (0.1 mg kg1; Steris Corporation, Phoenix, AZ, USA)
and weighed. A low light-sensitive camera with an array of near-infrared LEDs
was mounted on a small piece of neoprene rubber glued to the fur on the head
of the seal, providing a view of the animal's eyes and muzzle, and of the
water for approximately 70 cm in front of the nose. Illumination from the LEDs
was invisible to the seals and their prey. The camera was attached by a cable
to a torpedo-shaped, reinforced housing (35 cm long x 13 cm diameter)
that contained an 8 mm videotape recorder and microprocessor (Pisces Designs,
San Diego, CA, USA). The video housing rested in a molded, non-compressible
foam cradle that was attached to a neoprene rubber pad on the dorsal midline
of the seal below the shoulders. The video images were synchronized with
measurements of depth from a pressure transducer, swimming speed from a flow
meter, compass bearing (Davis et al.,
1999
) and swimming stroke activity (described below).
The instrument pack and housing were neutrally buoyant in water. The
frontal area of the instruments represented less than 5.5% of the frontal area
of the seal, and was within the suggested limits and shapes for instrumented
free-ranging swimming animals (Wilson et
al., 1986; Culik et al.,
1994
). To assess the potential effects of the instruments on
swimming effort, we compared metabolic rates of seals with (N=82
dives) and without (N=63 dives) the video system and camera. Dive
durations ranged from 1.4 to 44.0 min and there was no significant difference
in recovery oxygen consumption (MannWhitney nonparametric test at
P=0.917) for the two groups (Fig.
1).
|
Each 8 mm videotape was duplicated in VHS format immediately after
recovery. Videotapes were screened for encounters with prey, almost entirely
fishes. The species of fish were identified by size, shape and pigmentation
according to Fuiman et al.
(2002).
Stroke mechanics and locomotor costs
The mode of swimming (burst-and-coast, continuous stroking, gliding),
relative stroke amplitude and stroke frequency were determined for the seals
from a single axis accelerometer (±2 g; 6 cm long x 3 cm wide
x 2.0 cm high; Ultramarine Instruments, Galveston, TX, USA) mounted on a
neoprene pad at the base of the tail of the seals. Lateral sweeps of the
posterior half of the body and the hind flippers, characteristic of phocid
swimming (Fish et al., 1988),
were monitored by the accelerometer. Output from the accelerometer was
recorded at 16 Hz with a microprocessor and synchronized with dive depth, time
and video images. Accuracy of the accelerometer in detecting stroke movements
was tested by comparing the output of the microprocessor to video sequences
obtained on dives in which the camera was directed backwards on the seal. In
this way, the correspondence between peak flipper excursions and peak output
from accelerometer microprocessor was confirmed.
To determine the amount of oxygen expended for locomotion, we examined the
relationship between total oxygen consumed during the post-dive recovery
period and the number of strokes performed during a dive. Prolonged (>12 s)
periods of gliding characteristic of the descent
(Williams et al., 2000) were
accounted for by assuming that metabolism remained at resting levels when the
seal was not actively stroking. Therefore, locomotor costs during a dive were
determined from the difference between total recovery oxygen and maintenance
costs according to the equation:
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Statistics
Linear regressions for the relationships between recovery oxygen
consumption and dive duration, and plasma lactate concentration and dive
duration, were determined by least-squares methods using statistical software
(Jandel Scientific Software 1995). Dives were classified as aerobic or
anaerobic depending on increases in post-dive plasma lactate concentration
above resting levels. To assess the effect of the heat increment of feeding on
metabolic rate, we calculated the residuals for total recovery oxygen
consumption of post-prandial and post-absorptive seals. Dives were classified
as feeding dives if the seals ingested a fish or performed a dive within 5 h
of ingesting a large meal (i.e. >5 Pleuragramma antarcticum). The
latter was used to account for the prolonged metabolic effect associated with
heating and assimilating a protein meal, characteristic of marine mammals
(Costa and Kooyman, 1984). The
recovery oxygen consumption residuals of these dives were then compared to
similar residuals for seals performing non-foraging dives (SYSTAT 1998; SPSS,
Inc.).
The effects of the instrumentation on diving performance were determined by
comparing metabolic rates of seals with and without instrumentation. Because
the test for normality failed, a MannWhitney nonparametric test was
used (Zar, 1974). All mean
values are ± 1 S.E.M. unless otherwise
noted.
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Results |
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![]() | (2) |
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Total oxygen consumption during the post-dive recovery period also showed a
biphasic relationship with dive duration
(Fig. 2B). Using the breakpoint
in plasma lactate concentration at 23 min to define aerobic and anaerobic
dives, we found that recovery oxygen consumption of aerobic dives increased
linearly as described by the equation:
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As reported by Castellini et al.
(1992) and Ponganis et al.
(1993
), the rate of oxygen
consumption (
O2)
measured after diving was highly variable for dives of shorter duration than
the aerobic dive limit (Fig.
2C). For dives shorter than 23 min,
O2 ranged from
1.61 to 7.64 ml O2 kg1 min1 and
showed no pattern with dive duration. The mean of this range, 3.84±0.39
ml O kg1 min1 (N=5 seals), was
similar to the average metabolic rate measured for animals resting on the
water surface. This value is 23.2% lower than reported by Castellini et al.
(1992
) for short dives by
Weddell seals, which may be attributed to differences in the classification of
short dives (<23 min in the present study, compared with <14 min in
Castellini et al., 1992
). For
longer dives,
O2
decreased with dive duration according to the relationship:
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Feeding costs
Antarctic silverfish Pleuragramma antarcticum Boulenger were the
common prey item of foraging Weddell seals in this study
(Fuiman et al., 2002), and
ingestion was associated with a higher recovery oxygen consumption than
post-absorptive dives of similar duration (Figs
3,
4). The elevation in metabolism
lasted for several hours after a foraging dive, suggesting a thermogenic
effect associated with the heating and assimilation of the fish. An example of
the response is illustrated in Fig.
3 for a Weddell seal performing repetitive dives into an
aggregation of silverfish. During a feeding bout of 11 sequential dives the
seal ingested 44 fish in the first four dives as well as an additional fish
during the tenth dive of this sequence. Residuals for the recovery oxygen
consumption showed that metabolic rate remained elevated an average of
33.73±1.98 ml O2 kg1 for over 5 h,
although fish were not necessarily caught on every dive.
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When comparing the post-dive recovery oxygen consumed for post-absorptive
and post-prandial seals, we found that dives associated with feeding were
consistently more costly than non-feeding dives of similar duration and
distance (Fig. 4). In this
subset of dives, the total distance traveled ranged from 1178 m to 5012 m,
while duration of the dives ranged from 10.6 min to 37.1 min. Together these
resulted in a range of energetic costs for feeding and non-feeding dives as
described by the equation:
![]() | (6) |
All paired dives fell above the line of equality with an average post-dive
oxygen consumption that was 44.7±3.6% (N=10 paired dives)
higher for feeding dives than non-feeding dives. A similar elevation in
metabolic rate following the ingestion of prey was observed for one seal at
rest. O2 for the
quiescent, post-absorptive seal determined prior to diving was 4.42 ml
O2 kg1 min1. During an extended
recovery period following a foraging dive, the same animal showed a resting
O2 of 6.78 ml
O2 kg1 min1, representing a 53%
increase in metabolic rate attributed to the assimilation of prey.
Locomotor and stroking costs
Total recovery oxygen consumed during the post-dive period of aerobic dives
increased linearly with the number of strokes executed
(Fig. 5A) according to the
equation:
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|
As might be expected, there was a linear increase in locomotor costs as the
number of strokes increased (Fig.
5B). The relationship for aerobic dives was described by:
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Discussion |
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There has been considerable discussion concerning the basal metabolic rate
(BMR) of marine mammals, but with little resolution
(Lavigne et al., 1986;
Andrews, 2002
). Current
evidence suggests that the BMR of many pinnipeds and cetaceans ranges from 1.4
to 2.1 times that predicted for domestic animals
(Kleiber, 1975
) and
approximates that of other carnivorous mammals
(McNab, 2000
) when marine
mammals are resting on the water surface
(Williams et al., 2001
). We
found similar results for resting Weddell seals. The BMR of Weddell seals was
4.07±0.21 ml O2 kg1 min1
in air and 3.58±0.24 ml O2 kg1
min1 in water. The latter value was within 14% of that
reported by Castellini et al.
(1992
) for Weddell seals
resting in an isolated ice hole, and 1.6x the Kleiber
(1975
) prediction. BMR
decreased by approximately 10% if the seals went into prolonged apneas during
the rest period. In view of this, it is likely that the metabolic rate of
inactive seals is lower when submerged for prolonged periods than when resting
and breathing apneustically on the water surface. Evidence for this is
provided by sleeping and diving Weddell seals (present study;
Castellini et al., 1992
) and
California sea lions trained to station underwater
(Hurley and Costa, 2001
). For
both species, post-submergence metabolism indicates a flexible resting
metabolic rate depending on the duration of breath-hold. In Weddell seals,
prolonged breath-holding while sleeping on the water surface or during long
(>14 min) dives resulted in the lowest metabolic rates
(Castellini et al., 1992
). The
metabolic rate of sea lions resting on the water surface was 23 times
predicted values (Kleiber,
1975
); this decreased to predicted levels when the animals
remained submerged for 7 min (Hurley and
Costa, 2001
).
We found a similar result for Weddell seals when extrapolating the
relationship between recovery oxygen consumption and stroke count
(Fig. 5A) to zero strokes
performed (i.e. submerged resting). The calculated submerged metabolic rate of
Weddell seals was 2.47 ml O2 kg1
min1, and was within 10% of the Kleiber
(1975) prediction. Therefore,
we used this value to represent the minimum basal metabolic costs of the
diving Weddell seal in our energetic analyses, recognizing that this minimum
value may vary slightly for short duration dives
(Fig. 2C).
Of the two remaining costs, the energy expended for locomotion can be
considerably higher than both resting and assimilation costs. Overall,
locomotor activity resulted in a 1.3- to 3.5-fold increase in metabolism over
resting rates, depending on the duration of the dive
(Fig. 6). Because oxygen
consumption increased linearly with the number of strokes taken during a dive
(Fig. 5), the resulting net
cost per stroke remained constant at 0.044 ml O2
kg1 stroke1. Consequently, each swimming
stroke performed by the seal had a predictable effect on the oxygen reserves
of the animal, more so than the duration of the dive because gliding can
represent a large fraction of the total dive duration
(Williams et al., 2000;
Davis et al., 2001
).
|
Similar analyses have been conducted for running animals, in which the cost
of terrestrial locomotion has been attributed to cost of each step
(Alexander and Ker, 1990;
Kram and Taylor, 1990
).
However, the cost per stroke of diving Weddell seals was considerably less
than reported for stride costs of running mammals. Using the same methods as
Taylor et al. (1982
), the
total cost per stroke for Weddell seals was calculated by dividing the
recovery oxygen consumption (ml O2 kg1) by the
number of strokes taken during the preceding dive, using a conversion factor
of 20.1 J/ml O2. Note that this value differs from the net cost per
stroke presented above, and does not account for the oxygen consumed during
gliding periods. The resulting value, 2.39 J kg1
stroke1 for swimming Weddell seals, compares with 5.0 J
kg1 stride1 for running mammals
(Taylor et al., 1982
). For
runners ranging in body mass over four orders of magnitude the metabolic
energy consumed at equivalent speeds remained nearly constant. Likewise, total
stroke costs varied little for five species of phocid seal
(Fig. 7). The total cost per
stroke ranged from 1.44 J kg1 stroke1 for
a 97 kg harp seal to 2.87 J kg1 stroke1
for a 33 kg harbor seal.
|
The difference between step and stroke costs among mammals may be explained
in part by the different physical forces that must be overcome during running
and swimming (Dejours, 1987).
Among runners, smaller plantar areas reduce the cost of overcoming
gravitational and frictional forces during locomotion. Conversely, propulsive
surfaces are often enlarged in aquatic mammals that must overcome hydrodynamic
drag (Fish, 1993
). The
distance traveled per step (Kram and
Taylor, 1990
) or stroke (T. M. Williams, unpublished data) will
also affect the energetic cost of running and swimming, respectively. In the
present study, it was not possible to differentiate between large and small
amplitude strokes, and a closer examination of the data from tail-mounted
accelerometers may allow investigators to classify unique stroke types (e.g.
accelerative, maintenance, braking, steering), each with a different energetic
cost. Such analyses of these individual stroke types may allow us to further
refine the locomotor costs associated with propulsive movements by large and
small phocid seals.
The final component of the generalized energetic model is the energy
required for prey warming, digestion and assimilation
(Fig. 6). For the Weddell seals
in this study, feeding resulted in a 44.7% increase in metabolic rate over a
wide range of dive durations and distances traveled
(Fig. 4). The pattern was
similar to that described by Ponganis et al.
(1993) for a juvenile Weddell
seal presumed to be foraging on Pleuragramma antarcticum. It is
unlikely that these increases were due to added locomotion associated with
capturing fish as both resting and diving metabolic rates increased following
feeding. Interestingly, the metabolic effect was apparent for dives in which
fish were ingested as well as dives taking place as long as 5 h after fish
ingestion (Fig. 3). This
suggests that the digestion, assimilation and warming of prey elevate
metabolism in foraging seals. Wilson and Culik
(1991
) have shown a similar
response in another diving endotherm, the Adelie penguin. For these birds cold
ingesta resulted in a marked energetic effect independent of the heat
increment of feeding.
The high energetic demands associated with foraging suggest a selective
advantage for aquatic mammals demonstrating high locomotor and assimilation
efficiencies. By reducing the energy expended for travel and for processing
prey, limited oxygen reserves could be extended and the duration of underwater
hunting prolonged. Relatively little is known about reducing assimilation
costs per se, although the timing and type of prey ingested has been
shown to have an effect on total energetic cost in marine mammals
(Costa and Kooyman, 1984;
Bowen et al., 2002
), and may be
regulated (Crocker at al.,
1997
). In comparison, several strategies enable swimmers to
increase locomotor efficiency. Intermittent forms of swimming in particular
have been shown to reduce the cost of forward movement in a wide variety of
aquatic animals. Burst-and-coast swimming by fishes
(Weihs, 1974
;
Fish et al., 1991
), and
porpoising (Au and Weihs,
1980
), wave-riding (Williams
et al., 1992
) and prolonged gliding
(Costa and Gales, 2000
;
Williams et al., 2000
;
Davis et al., 2001
) by marine
mammals lead to reduced locomotor costs. Gliding is an exaggerated from of
intermittent propulsion that has recently been observed for many diving
animals including Weddell seals, blue whales and elephant seals
(Williams et al., 2000
;
Davis et al., 2001
),
bottlenose dolphins (Skrovan et al.,
1999
), right whales (Nowacek
et al., 2001
), Adelie penguins
(Sato et al., 2002
) and other
diving birds (Lovvorn and Jones,
1991
; Lovvorn et al.,
1999
). The change from constant to interrupted propulsion acts to
reduce the total number of strokes required to complete a dive, and thus
enables the animal to conserve limited oxygen stores during submergence
(Williams, 2001
).
Budgeting the number of strokes serves as such an energy conserving
strategy for diving Weddell seals due to the relationship between recovery
oxygen consumption and stroke count (Fig.
5). Maximum aerobic efficiency is achieved by traveling the
greatest distance on the fewest number of strokes, a task that may be
accomplished by taking advantage of buoyancy changes with depth and using
intermittent propulsion (Williams et al.,
2000; Sato et al.,
2003
). This relationship also provides a useful tool for assessing
the energetics of diving for free-ranging seals. If, as in running animals
(Alexander and Ker, 1990
),
activity is priced by each locomotor movement, then the cost of diving may be
predicted from the sum of individual stroking costs.
Predicting foraging costs for a free-ranging marine predator
The underwater location and cryptic feeding behavior of marine mammals
makes the determination of foraging energetics particularly challenging for
this group. Over the past 30 years, a variety of approaches have been used to
study the energetics of these animals at sea. These can be generally
categorized as indirect measurements and time budget analyses in which field
observations of behaviors are matched with metabolic rates determined in
captivity (Butler and Jones,
1997; Costa,
2002
). The former includes the dilution of isotopically labeled
water and the use of physiological variables as surrogates for metabolism. For
example, breathing rates (Sumich,
1983
; Kreite,
1995
), heart rate (Williams et
al., 1992
; Boyd et al.,
1995
; Butler and Jones,
1997
), and swimming speed
(Kshatriya and Blake, 1988
;
Hind and Gurney, 1997
) have
been used to estimate the energetics of free-ranging marine mammals. However,
several factors such as the effect of diving bradycardia on heart rate and the
effect of prolonged gliding sequences on swimming speed can obscure the actual
activity level of the animal, thereby rendering the use of these indirect
measures inaccurate for some diving birds and mammals or for some types of
dives.
Alternatively, the relationship between energetic cost and stroke count
allows the energetic demands of a dive to be predicted from propulsive
movements. For Weddell seals that are not foraging, or at least have not fed
within 3 h of a dive the aerobic cost of a dive is described by the equation:
![]() | (9) |
![]() | (10) |
This method enables energetic costs to be assessed for free-ranging animals
in which direct energetic measurements are impossible and avoids the potential
problems associated with using heart rate or swimming speed as predictors for
metabolism (see McPhee et al.,
2003). In addition, the relative cost of discrete behaviors (i.e.
locating, chasing or traveling to prey) or segments of a dive (i.e. ascent,
bottom or descent periods) can be estimated by counting the number of strokes
performed during these periods.
In summary, the cost of foraging by Weddell seals entails many energetic components associated with locomotion and the ingestion of prey. The relative proportion of energy allocated to each of these components by a Weddell seal changes with the distance traveled on a foraging dive. For example, locomotor costs will increase proportionately on longer distance dives as the total number of strokes increases. Many questions remain regarding the effects of meal size and prey type on feeding costs, as well as variation in basal metabolism during prolonged submergence. However, by accounting for each of these costs and monitoring stroking mechanics, dive duration and feeding behavior, it is possible to estimate the aerobic demands of diving in free-ranging seals where the cryptic behavior and remote location prevent direct energetic measurements.
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Acknowledgments |
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References |
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