|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online May 21, 2007
Journal of Experimental Biology 210, 1960-1970 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02767
Diving and foraging energetics of the smallest marine mammal, the sea otter (Enhydra lutris)
Department of Ecology and Evolutionary Biology, 100 Shaffer Road, University of California, Santa Cruz, CA 95060, USA
* Author for correspondence at present address: SPAWAR Systems Center San Diego, 53560 Hull Street Code 235, San Diego, CA 92152-6506, USA (e-mail: yeatesl{at}spawar.navy.mil)
Accepted 5 March 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: energetics, sea otter, foraging, diving, behavior
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). Whereas pinnipeds and cetaceans have maintained
aquatic lifestyles for over 50–60 million years, sea otters have been
fully aquatic for only 1–3 million years. A consequence of these
different evolutionary histories is that sea otters appear to lack some of the
more derived adaptations equated with a fully aquatic lifestyle typical of
cetaceans and pinnipeds. Such adaptations include insulation in the form of
blubber that can also act as an energy store, a well-developed dive response
that facilitates oxygen conservation when submerged
(Kooyman, 1989),
counter-current heat exchangers to retain and dissipate heat through thermal
windows (Williams and Worthy, 2002), and enhanced water conserving mechanisms,
e.g. complex nasal turbinates (Huntley et
al., 1984), reniculated kidneys (Williams and Worthy, 2002). Of
these, only the latter two are known for sea otters. In view of this, it is
reasonable to presume that marine living may be more energetically challenging
for sea otters in comparison to other marine mammal species.
This challenge is especially apparent when evaluating the allocation of
energy and the cost of various behaviors performed by sea otters. For example,
sea otters exhibit comparatively high resting metabolic rates that range from
2.8 to 3.2 times the levels predicted for a terrestrial mammal of similar size
(Iverson, 1972;
Morrison et al., 1974;
Costa, 1978;
Costa and Kooyman, 1982).
Although marine mammals generally exhibit higher resting metabolic rates than
do terrestrial mammals (Costa and
Williams, 1999), even within this group the sea otter represents
an extreme. Weddell seals Leptonychotes weddellii
(Williams et al., 2004b), grey
seals Halichoerus grypus
(Sparling and Fedak, 2004),
bottlenose dolphins Tursiops truncatus
(Williams et al., 2001) and
California sea lions Zalophus californianus
(Hurley and Costa, 2001)
demonstrate resting metabolic rates that average 1.5–2.0 times the
levels predicted by Kleiber (Kleiber,
1975) for terrestrial mammals. This difference between predicted
and measured rates is approximately half that observed for the sea otter.
Likewise, thermoregulatory costs are comparatively high for the sea otter
and are influenced by body size and a terrestrial form of insulation. In
general, the magnitude of heat transfer depends upon the surface
area-to-volume ratio of the animal, the gradient between core temperature and
environmental temperature, and the insulating barrier between the body core
and surrounding environment (Dejours,
1987). Compared to larger marine mammals, sea otters have a higher
surface area from which to lose heat relative to the tissue volume from which
to produce or retain heat. Furthermore, unlike other marine mammals that rely
on a thick, internalized blubber layer for insulation, sea otters prevent
excessive heat loss to the water through an air layer trapped against the skin
by an exceptionally dense fur covering
(Tarasoff, 1974;
Williams et al., 1992). A
potential disadvantage of this form of insulation is compression of the air
layer as the otter dives, thereby reducing the insulating quality of fur at
depth when the animal forages. Together these features result in elevated
thermal energetic costs for sea otters that must be compensated for by
activity, shivering or by the heat produced during the processing of food
(Costa and Kooyman, 1984).
It follows that sea otters must consume a comparatively large amount of
food to meet these elevated energetic demands. Typically, sea otters ingest
20–25% of their body mass in prey items per day
(Kenyon, 1969;
Costa and Kooyman, 1982)
spending 23–50% of the day foraging
(Estes et al., 1986;
Ralls and Siniff, 1990;
Tinker, 2004). In comparison,
similarly sized carnivorous terrestrial mammals and larger marine mammals
routinely consume 5–14% of their body mass in food each day spending as
little as 14% of the day hunting
(Schaller, 1972;
Shane et al., 1986;
Gorman et al., 1998;
Williams et al., 2004b).
Although the necessity for elevated feeding rates in sea otters has been
recognized (Kenyon, 1969;
Costa and Kooyman, 1982), few
studies have addressed the energetic costs associated with maintaining such
high rates of food intake. Neither the cost of individual dives nor the
metabolic rates resulting from prolonged foraging sessions by sea otters has
been determined. Furthermore, potential oxygen conserving mechanisms
characteristic of other foraging marine mammals have not been investigated. In
view of this lack of information and the importance of foraging costs in daily
activity and energy budgets (Stephens and
Krebs, 1986), we measured the energetic cost of diving and
foraging in adult male sea otters. The relative contribution of costs
associated with capturing, consuming and assimilating different types of prey
was determined. These data were then compared to the energy expended for
resting, grooming and swimming by this mammal. By combining the energetic
costs for these different behaviors with an activity budget for wild sea
otters, we then calculated a field metabolic rate for free-ranging otters that
was compared to values reported for other marine-living mammals.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
) enabling foraging patterns and activity budgets to be
determined visually. Water temperature along the coast ranges from 10°C to
19°C seasonally.
Captive studies
Animals
Two adult, male sea otters were used for the metabolic trials
(Table 1). Both animals had
been in captivity for 1 year prior to training and experimental measurements,
and were maintained in outdoor fiberglass holding pools (4.2 mx1.2 m or
6 mx1.5 m; diameter x depth). Fresh seawater was continuously
added at a minimum of 227 l min–1. Water temperature varied
with ambient ocean temperature along the coast. The captive animals were fed a
mixed diet of commercially obtained frozen squid (Loligo opalescens),
surf clam (Spisula solidissima), cod (Macruronus
novaelandiae) and tiger prawns (Panaeus vannamei) presented in
4–7 meals per day. Diets were supplemented with commercially available
live cancer crabs (Cancer spp.), mussels (Mytilus edulis)
and clams (Spissula spp). Animals were weighed weekly to the nearest
0.1 kg using a platform scale (Arlyn 320D, Rockaway, NY, USA).
|
Oxygen consumption and energetic costs
Energetic costs of different activities were determined from measurements
of oxygen consumption by the captive otters. Both animals were trained over a
period of 12 months to rest or make voluntary dives and then surface beneath a
clear acrylic dome (1.3 mx0.7 mx0.5 m; length x width
x peak height) that floated on the water. All measurements followed the
methods of Williams et al. (Williams et
al., 2004b) using an open-flow respirometry system for aquatic
mammals. Air was pulled through the dome at a rate of 180–190 l
min–1 by a mass flow controller (Flow kit 500H, Sable
Systems, Henderson, NV, USA). Sub-samples of dome exhaust were drawn through a
series of three columns filled with a desiccant (Drierite, W. A. Hammond
Drierite, Xenia, OH, USA) and a CO2 scrubber (Baralyme, Chemetron
Medical Division, Allied Healthcare Products, St Louis, MO, USA) at a rate of
500 ml min–1 before entering an oxygen analyzer (model FC1-B,
Sable Systems). The air flow was adjusted so that the oxygen content of the
dome remained above 20.10% for all trials. Oxygen content of the dome exhaust
was logged every 2.0 s on a laptop computer. Flow rates were corrected to STPD
prior to calculating the rate of oxygen consumption using equation 4b from
Withers (Withers, 1977).
Oxygen consumption of the otters was determined under four conditions: (1) resting quietly on the water surface, (2) grooming, (3) following serial foraging dives, and (4) following single non-foraging dives. The animals were post-absorptive (by fasting overnight) during the resting and single dive trials, and post-prandial for all other metabolic tests to simulate energetic status in the wild. For resting measurements, the otters floated beneath the metabolic dome in shallow holding pools. The lowest oxygen consumption measured over a continuous 5 min period during 10–20 min trials was used.
Foraging costs were determined by measuring oxygen consumption following prey-searching dives. Foraging trials were conducted in a 9.1 m deep, 4 m diameter seawater storage tower with the metabolic dome sealed on the surface of the water. To facilitate viewing otter behavior during submergence, four underwater video cameras (Lorex model CVC-699, Strategic Vista International Inc., Markham, Ontario, Canada) were mounted inside the tank. A rocky substrate and 3–5 kg of live crabs (Cancer spp.), live mussels (Mytilus edulis) or 1.0–1.4 kg of the otters' mixed diet (commercial squid, surf clams, tiger prawns and cod) were added to the bottom of the tank to simulate foraging conditions in the wild. On each test day an otter was placed in the tank and allowed to forage by making repeated dives to the bottom to collect prey items. Following collection of the food items the otters surfaced beneath the metabolic dome while handling and consuming prey. The duration of foraging trials was determined by the otter and ranged from 60–145 min. Oxygen consumption during grooming, which included vigorous rubbing and pleating of the fur, was recorded opportunistically during the inter-dive periods of the foraging trials.
In addition to the serial foraging dives, one otter (no. 180) was trained
to perform single non-foraging dives and then rest under the metabolic dome
upon surfacing. The resulting values for oxygen consumption rate
(
O2) were used
to assess locomotor costs associated with diving. During these trials, the
otter dove to a target at the bottom of the tank at 9.1 m and remained at
depth until receiving the signal to return and surface beneath the metabolic
dome. Upon returning, the otter rested beneath the dome and was rewarded with
small pieces of food, which required minimal handling and totaled less than
0.3 kg over a 10–20-min period while the post-dive oxygen consumption
was monitored.
Oxygen consumption rate was calculated using DATACAN V (Sable Systems
International, Henderson, NV, USA) by summing the amount of oxygen used during
a specific behavior (i.e. resting, grooming) divided by the duration of the
behavior. For foraging trials, metabolic rate was calculated by summing the
amount of oxygen used during the entire foraging bout (including diving,
post-dive recovery, prey manipulation and consumption of prey items) divided
by the duration of the bout. Single dive metabolic rates were calculated
according to Castellini et al. (Castellini
et al., 1992) by summing the amount of oxygen used during the
post-dive recovery period and dividing by the duration of recovery. The end of
the recovery period was defined as the point in time when
O2 returned to
within 10% of resting values. To evaluate locomotor costs (the amount of
oxygen consumed for performing a single dive), maintenance costs (measured as
resting metabolic rate) that were incurred during the dive and subsequent
recovery period were subtracted from the total oxygen consumed during recovery
assuming that maintenance costs remained constant throughout the dive
(Scholander, 1940;
Hurley and Costa, 2001). An
observer with a stopwatch recorded surface and sub-surface intervals for all
metabolic trials.
Plasma lactate concentration
To assess potential anaerobic contributions to diving metabolism, plasma
lactate concentration was measured for resting and diving sea otters. Prior to
the tests, the animals were trained to enter a protected contact box
specifically designed for blood sampling. The otter rested dorsally recumbent
while a clear acrylic door was partially lowered, leaving the caudal third of
the otter's body exposed. Blood samples were drawn from the popliteal vein
(approximately 1 cm from the femoral condyles) using a 22-gauge needle and a
12-ml syringe while the otter rested inside of the box. On different days, the
same procedure was performed immediately following 9.1-m dives in the water
tower that varied in duration. Blood samples were transferred to sterile tubes
(Becton Dickinson Vacutainer, Franklin Lakes, NJ, USA) containing a glycolytic
inhibitor (sodium fluoride and potassium oxalate) for plasma lactate
concentration analysis. The samples were immediately refrigerated until
further processing (<15 min post blood draw). Each vial was centrifuged for
10 min (2500 r.p.m.) and the plasma transferred to a new sterile tube.
Sub-samples were immediately shipped overnight on cold packs to the University
of California, San Diego, USA (Comparative Neuromuscular Laboratory) for
determination of plasma lactate concentration (using a YSI Sport 1500, Yellow
Springs, OH, USA).
Field studies
Animals
Eleven free-ranging, adult male otters were used in assessments of daily
activity budgets in the wild (Table
1). The otters were captured and tagged along the San Simeon (CA,
USA) coastline between March 2001 and October 2002. Each otter was captured by
re-breather equipped SCUBA divers using Wilson Traps
(Ames et al., 1986), and
transported to mobile veterinary surgical facilities onshore.
The otters were weighed to the nearest 0.1 kg using a platform scale (Arlyn
320D, Rockaway, NY, USA) and sedated for implantation of a radio tag.
Anesthesia was induced using an intramuscular injection of fentanyl
(Elkins-Sinn, Cherry Hill, NJ, USA; 0.5–0.11 mg kg–1
body mass) in combination with diazepam (Abbot Laboratories, North Chicago,
USA; 0.010–0.053 mg kg–1). Anesthesia was maintained
with an isoflourane gas and oxygen mixture
(Williams and Siniff, 1983;
Monson et al., 2001). The
otters were surgically implanted with an intra-abdominal VHF radio transmitter
(7.6 cmx10.2 cmx2.5 cm, 
120 g; Advanced Telemetry Systems
Inc., Isanti, MN, USA) following standardized procedures
(Williams and Siniff, 1983;
Monson et al., 2001). The
transmitters were allowed to float freely in the abdominal cavity and provided
consistent signals for 1–3 years.
For identification in the field, colored plastic tags (Temple Tags, Temple, TX, USA) were attached into the webbing of the hind flippers and a passive integrated transponder (PIT) chip was inserted under the skin of the right inguinal area. At the completion of all procedures, an intramuscular injection of naltrexone (Wildlife Pharmaceuticals, Fort Collins, CO, USA; 0.053 mg ml–1) was given as an antagonist to ensure that the animals were alert prior to release. Once the otters were active, they were released close to their original capture site or from the nearby shore.
Activity budgets
Daily activity budgets of wild otters were determined between July 2001 and
July 2003 using a combination of direct observation and radio telemetry.
During daylight hours direct observations were used in conjunction with
telemetry. The otters were visually monitored from shore using a 50x
spotting scope (Questar Inc., New Hope, PA, USA). The temporal pattern of the
VHF signal from the implanted radio tag enabled us to assign behavior,
according to published methods (Loughlin,
1980; Ralls and Siniff,
1990). During hours of darkness, activity was assessed from the
changes in the character of the transmitted radio signals. For example,
implanted tags in resting otters produced a constant, uninterrupted signal,
whereas those from active animals that were not feeding or resting produced a
constant pulse of variable strength. When otters were actively feeding, radio
signals were interrupted while the animals were submerged and steady while the
animal consumed prey at the surface.
The instantaneous behavior of focal animals was recorded at 10-min intervals over 24-h recording sessions. Behaviors were classified as resting, grooming (including somersaulting in the water, vigorously rubbing and pleating the fur), foraging (including eating on the water surface and actively diving) or swimming. Behaviors that did not fall into one of these classifications were categorized as `other' (e.g. interacting with conspecifics).
Daily activity budgets were calculated as the total number of 10-min
intervals assigned to each behavior. Periods when the radio transmitter signal
was poor were classified as `unknown' behaviors. These unknown periods were
removed prior to analysis. Thus, the calculated daily activity budgets
represent the proportions of known activities across 24 h. To reduce the
potential for bias (i.e. if any one behavior was more likely to be classified
as unknown), our analyses are limited to sessions in which 
10% of the
intervals were classified as `unknown'. This restriction reduced our sample
size from 11 to six adult otters for the determination of activity budgets
(Table 2) and subsequent field
metabolic rates.
|
Dive duration
The duration of individual dives was measured by two methods. During
daylight, duration was assessed visually and then timed by an observer with a
stopwatch. During the night, dive duration was determined by timing the
interval between VHF radio transmitter signals as described above.
Analysis
Energy budgets and field metabolic rate
Daily energy requirements for individual otters were calculated by
combining the activity budgets of the six wild otters with activity-specific
energetic costs from the captive otters. Costs were determined from the
O2 of each
behavior determined during the captive animal trials and supplemented with
data for submerged and surface swimming from Williams
(Williams, 1989). All oxygen
consumption rates were converted to energetic demand (MJ
day–1) using a factor of 20.083 kJ l–1
O2 (Schmidt-Nielsen,
1997). To estimate total daily energy expenditure, the energetic
rates for individual behavioral categories were summed according to measured
activity budgets over 24-h periods. The resulting value was termed the field
metabolic rate (FMR) and did not take into account air or water temperatures
during the time of observation.
It was not possible to measure oxygen consumption for some behaviors that
were observed in the wild (interacting with conspecifics, simultaneous surface
swimming and grooming). Therefore, the mean
O2 of surface
swimming (29.6 ml O2 min–1 kg–1)
(Williams, 1989), subsurface
swimming (17.55 ml O2 min–1 kg–1)
(Williams, 1989), and grooming
and foraging (this study), was used to generally represent the cost of `other'
behaviors.
Statistical analysis
Statistical analyses were performed using SYSTAT 10.2 (Systat Software Inc.
Richmond, CA, USA). Multiple comparisons of independent samples were made
using a multifactor ANOVA, unless otherwise stated. The type-I error rate for
all tests was set to 
=0.05. Comparisons between individual captive
otters under each experimental condition were made using a two-sample
t-test. A least squares non-linear regression was used to describe
total oxygen consumption in relation to dive time as determined by best fit
multiple regression comparisons (Systat Software Inc. Richmond, CA, USA).
Lastly, data for field metabolic rate and body mass were log transformed and a
least-squares allometric regression developed. All results are reported as
mean ± 1 s.d.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
Oxygen consumption and energetic costs
All metabolic experiments were conducted on different days; therefore
separate trials were assumed to be independent data points. Because resting
metabolic data for the two otters were not statistically different
(t=2.2, P=0.69), the data for both animals were combined.
Mean resting metabolic rate (RMR) for sedentary otters floating on the water
surface was 13.3±0.9 ml O2 kg–1
min–1 (N=23 trials) and was similar to previously
published values [11.7–13.5 ml O2 kg–1
min–1 (Morrison et al.,
1974; Costa and Kooyman,
1982; Williams,
1989)]. No relationship was detected between water temperature and
resting metabolism over the range of 13°C to 17°C examined in the
present study (N=23 trials, r2=0.09,
P=0.70).
Diving, grooming and foraging resulted in an increase in
O2 over resting
levels (Fig. 2), with the
resulting metabolic rates differing significantly among all activity states
(resting, grooming, foraging and diving one-way ANOVA, F=411.7,
P
|
 |
|
The rate of oxygen consumption during single dives did not vary during
these trials. Mean metabolic rate for single dives, 17.6±0.5 ml
O2 kg–1 min–1 (N=11
trials), was only 1.3 times resting values
(Fig. 2), and is similar to the
level reported for horizontal submerged swimming by sea otters
(Williams, 1989).
As might be expected because of the number of different behaviors involved, energetic costs were higher for foraging dives than for the single, non-foraging dives (Figs 2 and 4). Foraging bout duration for the captive otters ranged from 60 to 145 min and consisted of multiple dives and post-dive recovery periods that included prey handling and consumption. Metabolic rates measured during these bouts differed marginally between prey items. For otters foraging on live cancer crabs metabolic rate averaged 22.2±1.3 ml O2 kg–1 min–1 (N=7), which decreased to 20.1±2.7 ml O2 kg–1 min–1 (N=4) for mussels and 21.4±1.3 ml O2 kg–1 min–1 (N=8) for a mixed diet (Fig. 4). Statistically, there was no effect of prey type (F=1.25, P=0.20) or otter (F=1.83, P=0.20) on metabolic rate for the crab or mixed diet trials, nor was there an interaction effect between prey type and otter (two-way ANOVA, F=3.29, P=0.10). Owing to a low sample size, mussel trials were excluded from these statistical comparisons. The average foraging metabolic rate for all otters and prey types was 21.6±1.7 ml O2 kg–1 min–1 (N=19).
|
Plasma lactate concentration
Increased anaerobic metabolism, as manifested by an elevation in plasma
lactate concentration, was not observed in the captive diving sea otters in
this study. The concentration of plasma lactate was variable and ranged from
0.33 to 1.65 mmol l–1 in resting sea otters (mean =
0.97±0.46 mmol l–1; N=6). These lactate
levels were considerably higher than observed for other marine mammals
including bottlenose dolphins (Williams et al., 1993) and Weddell seals
(Kooyman et al., 1980;
Kooyman et al., 1983;
Guppy et al., 1986) whose
resting values typically average 0.5 mmol l–1.
Owing to the variation in resting levels it was not possible to detect a change in plasma lactate concentration with diving. Post-dive lactate concentration for single dives of 30–100 s ranged from 0.3 to 1.1 mmol l–1 and did not exceed the range for resting values in the captive otters. In general, no correlation between lactate concentration and dive duration was found in this study (r2=0.07, P=0.6).
To ensure that the blood sampling method did not contribute to elevated lactate levels during the resting trials we also tested blood samples obtained from anesthetized sea otters. Lactate levels were similarly elevated relative to other resting marine mammals for both sampling methods. The mean lactate level for anesthetized otters was 0.91±0.21 mmol l–1 (N=4).
Activity budgets
Twenty activity observation sessions comprising over 300 h of monitoring
were completed on 11 free-ranging sea otters. The greatest proportion of the
day for wild sea otters was spent feeding and resting
(Table 2) and was similar to
previously reported activity budgets for California sea otters
(Estes et al., 1986;
Ralls and Siniff, 1990;
Tinker, 2004).
For the six otters with the most complete records, over 75% of the day was
taken up with feeding and resting, 8.5±6.8% with swimming,
9.1±1.9% grooming, and 7.3±5.8% of the day involved `other'
behaviors (Table 2). Rather
than randomly dispersed across the day, these behaviors occurred in
predictable sequences (Yeates,
2006). Typically, a prolonged period of rest was followed by
foraging bouts interspersed with short periods of grooming. The resulting
behavioral cycle for wild otters consisted of resting, then grooming and
foraging, followed by another grooming session and finally back to resting.
The duration of these sequences varied with the individual otter, and occurred
throughout the day and night.
Energy budgets and field metabolic rate
Based on the activity budgets and energetic costs described above, we
calculated the daily energy expenditure for each behavior and the subsequent
field metabolic rate of wild California sea otters (detailed in
Table 3). We found that the
largest energetic expenditure for sea otters, 6.1±1.1 MJ
day–1, was associated with foraging
(Table 4). In comparison,
resting was a relatively low cost behavior but constituted a large proportion
of the day. As a result, sea otters on average spent 4.2±1.0 MJ
day–1 to support resting periods. High energy behaviors such
as grooming and swimming were often of short duration. The amount of energy
spent grooming, swimming and performing other behaviors including interacting
with conspecifics was 2.4±0.4 MJ, 1.6±0.4 MJ and 1.4±1.4
MJ, respectively. Together, these latter activities required a total of 5.4 MJ
day–1. When summed, the field metabolic of wild sea otters
was 15.7±2.7 MJ day–1
(Table 4).
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Kramer, 1988). In view of the
exceptionally high costs associated with these physiological and behavioral
functions for sea otters (Morrison et al.,
1974; Costa and Kooyman,
1982; Costa and Kooyman,
1984; Williams,
1989), it is not surprising that the cost of foraging was also
high for this marine mammal (Fig.
2).
Comparisons with other species of wild marine mammals are difficult since
few studies have examined the metabolic costs of diving and foraging for this
group with the exception of phocid seals. However, when the data for sea
otters are compared to this limited data set, we find that the smallest marine
mammal demonstrates higher relative and absolute costs for both diving and
foraging. In the present study, the metabolic rate of sea otters performing
single dives ranging in duration from 40 to 192 s was 17.6 ml O2
kg–1 min–1. This compares with 4.5 to 5.7 ml
O2 kg–1min–1 for phocid seals
including juvenile and adult grey seals weighing 41 to 128 kg
(Sparling and Fedak, 2004) and
adult 390 kg Weddell seals (Castellini et
al., 1992). These differences remain even when the disparity in
body mass between the otters and seals is taken into account. The predicted
diving costs for a 25 kg seal based on an allometric regression for diving
costs in relation to phocid body mass from the previous studies is 7.7 ml
O2 kg–1 min–1, a value that is
less than half that measured for the sea otters.
A wide variety of factors probably contribute to the higher diving costs observed for sea otters compared to phocid seals. These include differences in (1) swimming style, (2) buoyancy, (3) the metabolic effects of food processing and (4) thermoregulation. We can examine each of these for sea otters by subdividing the total cost of a foraging dive into its components as shown in Fig. 4. From these calculations, maintenance costs, as defined by resting metabolic rate, constituted over 60% of the diving costs for this species. Locomotor costs for performing the dive accounted for 16.6–19.4% of total diving costs, leaving 20.3–20.7% of the energy expended in a foraging dive to support hunting behaviors (e.g. searching for prey at depth) and prey handling and consumption at the surface.
From this calculation, maintenance functions represent the major energy
expenditure for foraging sea otters, and would likely be reduced if these
animals initiated a dive response when submerged. Weddell seals performing
extended (>14 min) dives beneath the Antarctic sea ice
(Castellini et al., 1992), as
well as elephant seals (Webb et al.,
1998a), grey seals (Sparling
and Fedak, 2004) and California sea lions
(Hurley and Costa, 2001)
resting and diving in a laboratory setting demonstrate a decrease in metabolic
rate during prolonged submergence. Thus, energetic costs for pinnipeds resting
on the water surface are 10–48% higher than total submergence costs for
the animals voluntarily swimming or diving in a pool. If sea otters followed a
similar trend, the oxygen consumed during the dive
(Fig. 3) would have been lower
than that measured during resting (Fig.
2), and the relative contribution of maintenance costs to the
total cost of a dive would have been smaller. Alternatively, a dive response
and or hypometabolism may be occurring in sea otters, but it is not detectable
because the possible costs associated overcome the effects of being positively
buoyant during shallow dives.
It is unclear to what extent, if at all, sea otters reduce foraging costs
through oxygen conserving mechanisms associated with hypometabolism,
bradycardia and decreased peripheral blood flow that constitute the dive
response reported for other marine mammals
(Scholander, 1940;
Kooyman, 1989). In
marine-adapted species, the response can be pronounced and serve as a means
for extending the duration of a dive
(Scholander, 1940). Owing to
the relatively short dive durations of sea otters
(Fig. 1) and the size of on
board oxygen stores (Kooyman,
1989), such a response may not be critical during foraging in
productive coastal areas. Using our measured diving metabolic rates
(Fig. 2) and published values
of total oxygen storage capacity for sea otters
(Lenfant et al., 1970), the
calculated aerobic dive limit (Kooyman et
al., 1983) for an adult sea otter ranges from 2.9 to 4.3 min
(180–275 s) depending on whether the animal dives with a full or
half-full lung of air. This range represents the extreme upper limit of dive
durations observed for wild sea otters
(Fig. 1), and indicates that
sea otters are able to dive aerobically during routine foraging dives along
coastal California.
Under the experimental conditions of the present study, we found that a
significant portion of the total diving cost for sea otters could be
attributed to the energy required for locomotion
(Fig. 4). Because of its small
body mass, proportionally high buoyancy
(Tarasoff and Kooyman, 1973)
and transitional style of propulsion, sea otters demonstrate larger transport
costs for swimming than reported for other marine mammals
(Williams, 1999). Therefore,
high locomotor costs during diving might be expected.
Several behavioral options allow more derived marine mammals to reduce
locomotor costs by simply avoiding active swimming. These include the use of
ballast and buoyancy control (Webb et al.,
1998b; Cashman,
2002), as well as controlled gliding on ascent or descent
(Williams et al., 2000). For sea otters, exceptionally large lungs and air in
the fur (Tarasoff and Kooyman,
1973) make the animal buoyant. This characteristic undoubtedly
contributes to the high cost of diving by increasing the physical forces that
must be overcome to reach depth. Using biomechanical models, Cashman
(Cashman, 2002) demonstrated
that the California sea otter does not reach neutral buoyancy within the
diving depths observed for wild coastal otters
(Tinker et al., 2007). As a
result, the animal must rely on locomotor power to overcome buoyancy when
locating prey at depth. This energetically costly task is circumvented in
larger or deeper-diving marine mammals by passive gliding aided by negative
buoyancy (Williams et al., 2000). Alternate behavioral strategies such as
carrying ballast or decreasing lung volume enable adult otters to reduce
buoyancy in the water column (Cashman,
2002). Presumably, this behavior will also serve to reduce
locomotor costs, particularly during deeper foraging dives.
The final energetic cost associated with foraging is the energy expended
during hunting and food processing. In the wild, sea otters feed on a wide
variety of invertebrate prey that require specific capture, collection and
handling techniques (Kenyon,
1969; McCleneghan and Ames,
1976; Jolly, 1997;
Tinker, 2004). The collection
of prey can involve digging in sediments or pulling items from rocky
substrates, which result in different handling times. Ingestion also involves
different tasks. Otters consuming mussels and clams crush the shells with
their incisors as well as hammer one mussel against another
(Wolrab, 2003). By contrast,
otters preying on crabs will tear the legs and claws from the large carapace
prior to consuming the meat (Wolrab,
2003).
Despite these varied tasks, we observed no significant difference between the energetic costs associated with foraging on different types of prey in the present study (Fig. 4). In general, the cost of handling and processing prey contributed approximately 20% to the total cost of a foraging dive for sea otters feeding on crab, mussels or a mixed diet. Of these, there was a general, although not significant, trend for higher energetic costs when the otters fed on crabs.
Another energetically expensive factor associated with prey processing is
the heat increment of feeding (HIF). In sea otters, the energy required for
digesting and absorbing food following a meal, the HIF, results in a prolonged
increase in resting metabolism (Costa and
Kooyman, 1984). The maximum increase in post-prandial oxygen
consumption reported in the previous study occurred approximately 82 min after
a 1.5 kg meal. By contrast, Weddell seals demonstrate an HIF response during
the post-dive recovery period immediately following ingestion of Antarctic
silverfish (Williams et al.,
2004b). In both species, the HIF response may last for several
hours depending on prey type, the size of the meal, and foraging patterns. For
sea otters, changes in core body temperature during and after a dive
(Yeates, 2006), and post-dive
defecation indicate that digestion and assimilation of prey occurred within
foraging bouts during the trials. Thus, HIF response probably contributes to
the energetic cost of prey handling by foraging sea otters.
|
).
Thus, the sea otter values did not differ from predicted values of FMR based
upon a regression of marine mammal FMR values against body size, despite
comparatively high foraging costs observed in the present study.
One explanation for this is related to differences in the activity budgets
for foraging marine mammals. Unlike actively foraging pinnipeds
(Costa and Gales, 2003) and
cetaceans (Shane et al., 1986;
Baird et al., 2005) that spend
the major portion of the day transiting to foraging areas or diving, sea
otters spend 40–49% of the day resting motionless on the water surface
(Ralls and Siniff, 1990)
(Table 2). Were the otter to
maintain activity levels typical of other marine mammals, FMR would be
significantly higher due to the high energetic cost of swimming
(Fig. 2).
In summary, the marine environment would initially appear to be energetically challenging for sea otters because of its small size, exceptional buoyancy, and costly style of swimming. Without the benefit of many of the energy conserving mechanisms reported for other marine mammals, we expected total daily energetic costs to be elevated for sea otters relative to other marine mammals. Instead, energetically costly behaviors were counterbalanced in part by prolonged periods of rest that composed up to 49% of the sea otter's day. Thus, by budgeting behavior as well as the costs associated with each, wild sea otters are able to maintain a daily energetic balance similar to that of larger, more derived marine mammals.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Ames, J. A., Hardy, R. A. and Wendell, F. E. (1986). A Simulated Translocation of Sea Otters, Enhydra lutris, with a Review of Capture, Transport and Holding Techniques. Technical Report 52. California: California Department of Fish and Game Marine Resources.
Baird, R. W., Hanson, M. B. and Dill, L. M. (2005). Factors influencing the diving behavior of fish-eating killer whales: sex differences and diel and interannual variation in diving rates. Can. J. Zool. 83,257 -267.
Berta, A. and Sumich, J. L. (1999). Marine Mammals: Evolutionary Biology. San Diego: Academic Press.
Cashman, M. E. (2002). Diving in the southern sea otter, Enhydra lutris nereis: morphometrics, buoyancy, and locomotion. Masters thesis, University of California Santa Cruz, USA.
Castellini, M. A., Kooyman, G. L. and Ponganis, P. J.
(1992). Metabolic rates of freely diving Weddell seals:
correlations with oxygen stores, swim velocity and diving duration.
J. Exp. Biol. 165,181
-194.
Costa, D. P. (1978). The ecological energetics, water and electrolyte balance of the California sea otter, Enhydra lutris. PhD thesis, University of California Santa Cruz, USA.
Costa, D. P. and Gales, N. J. (2003). Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Ecol. Monogr. 73, 27-43.[CrossRef]
Costa, D. P. and Kooyman, G. L. (1982). Oxygen consumption, thermoregulation, and the effect of fur oiling and washing on the sea otter, Enhydra lutris. Can. J. Zool. 60,2761 -2767.
Costa, D. P. and Kooyman, G. L. (1984). Contribution of specific dynamic action to heat balance and thermoregulation in the sea otter, Enhydra lutris. Physiol. Zool. 57,199 -203.
Costa, D. P. and Williams, T. M. (1999). Marine mammal energetics. In Biology of Marine Mammals (ed. J. E. Reynolds and S. Rommel), pp. 176-217. Washington, DC: Smithsonian Institution Press.
Dejours, P. (1987). Water and air characteristics and their physiological consequences. In Comparative Physiology: Life in Water and on Land (ed. P. Dejours, L. Bolis, C. R. Taylor and E. R. Weibel), pp.3 -11. New York: Springer.
Estes, J. A., Underwood, K. E. and Karmann, M. J. (1986). Activity time budgets of sea otters in California. J. Wildl. Manage. 50,6126 -6136.
Gorman, M. L., Mills, M. G., Raath, J. P. and Speakman, J. R. (1998). High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391,479 -481.[CrossRef]
Guppy, M., Hill, R. D., Schneider, R. C., Qvist, J., Liggins, G. C., Zapol, W. M. and Hochachka, P. W. (1986). Microcomputer-assisted metabolic studies of voluntary diving of Weddell seals, Leptonychotes weddelli. Am. J. Physiol. 250,R175 -R187.[Medline]
Huntley, A. C., Costa, D. P. and Rubin, R. D.
(1984). The contribution of nasal countercurrent heat exchange to
water balance in the Northern elephant seal, Mirounga angustirostris.J. Exp. Biol. 113,447
-454.
Hurley, J. A. and Costa, D. P. (2001). Standard
metabolic rate at the surface and during trained submersions in adult
California sea lions (Zalophus californianus). J. Exp.
Biol. 204,3273
-3281.
Iverson, J. S. (1972). Basal energy metabolism of mustelids. J. Comp. Physiol. 81,341 -344.[CrossRef]
Jolly, J. M. (1997). Foraging ecology of the sea otter, Enhydra lutris, in a soft-sediment community. Masters thesis, University of California Santa Cruz, USA.
Kenyon, K. W. (1969). The Sea Otter in the Eastern Pacific Ocean: North American Fauna No. 68. Washington: US Fish and Wildlife Service.
Kleiber, M. (1975). The Fire of Life: An Introduction to Animal Energetics. Huntington, NY: R. E. Krieger.
Kooyman, G. L. (1989). Diverse Divers: Physiology and Behavior. New York: Springer-Verlag.
Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. and Sinnett, E. E. (1980). Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol. 138,335 -346.
Kooyman, G. L., Castellini, M. A., Davis, R. W. and Maue, R. A. (1983). Aerobic diving limits of immature Weddell seals. J. Comp. Physiol. 151,171 -174.
Kramer, D. (1988). Behavioral ecology of air breathing mammals. Can. J. Zool. 66, 88-94.
Lenfant, C., Johansen, K. and Torrance, J. D. (1970). Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir. Physiol. 9, 277-286.[CrossRef][Medline]
Loughlin, T. R. (1980). Radio telemetric determination of the 24-hour feeding activities of sea otters, Enhydra lutris. In A Handbook on Biotelemetry and Radio Tracking (ed. C. J. Amlaner and D. W. MacDonald), pp.717 -724. Oxford: Pergamon Press.
McCleneghan, K. and Ames, J. A. (1976). Unique method of prey capture by a sea otter, Enhydra lutris. J. Mammal. 57,410 -412.[CrossRef]
Monson, D. H., McCormick, C. and Ballachey, B. E. (2001). Chemical anesthesia of northern sea otters (Enhydra lutris): results of past field studies. J. Zoo. Wildl. Med. 32,181 -189.[Medline]
Morrison, P., Rosenmann, M. and Estes, J. A. (1974). Metabolism and thermoregulation in the sea otter. Physiol. Zool. 47,218 -228.
Ralls, K. and Siniff, D. B. (1990). Time budgets and activity patterns in California sea otters. J. Wildl. Manage. 54,251 -259.[CrossRef]
Riedman, M. and Estes, J. A. (1991). The Sea Otter (Enhydra lutris): Behavior, Ecology, and Natural History. Washington, DC: US Department of the Interior, Fish and Wildlife Service.
Schaller, G. B. (1972). The Serengeti Lion. Chicago: University of Chicago Press.
Schmidt-Nielsen, K. (1997). Animal Physiology: Adaptation and Environment. New York: Cambridge University Press.
Scholander, P. F. (1940). Experimental investigation on the respiratory function in diving mammals and birds. Hvalradets Skrifter 22,1 -131.
Shane, S. H., Wells, R. S., Wursig, B. and Wursig, B. (1986). Ecology, behavior and social organization of the bottlenose dolphin: a review. Mar. Mamm. Sci. 2, 34-63.[CrossRef]
Sparling, C. E. and Fedak, M. A. (2004).
Metabolic rates of captive grey seals during voluntary diving. J.
Exp. Biol. 207,1615
-1624.
Stephens, D. W. and Krebs, J. R. (1986). Foraging Theory. Princeton: Princeton University Press.
Tarasoff, F. J. (1974). Anatomical adaptations in the river, otter, sea otter, and harp seal with reference to thermal regulation. In Functional Anatomy of Marine Mammals (ed. R. J. Harrison), pp. 111-141. Academic Press: New York.
Tarasoff, F. J. and Kooyman, G. L. (1973). Observations on the anatomy of the respiratory system of the river otter sea otter and harp seal part 1, the topography weight and measurements of the lungs. Can. J. Zool. 51,163 -170.[Medline]
Tinker, M. T. (2004). Sources of variation in the foraging behavior and demography of the sea otter, Enhydra lutris. PhD thesis, University of California Santa Cruz, USA.
Tinker, M. T., Costa, D. P., Estes, J. A. and Wieringa, N. (2007). Individual dietary specialization and dive behaviour in the California sea otter: using archival time-depth data to detect alternative foraging strategies. Deep-Sea Res. Part II Top. Stud. Oceanogr. 54,330 -342.[CrossRef]
Webb, P. M., Andrews, R. D., Costa, D. P. and Le Boeuf, B. J. (1998a). Heart rate and oxygen consumption of northern elephant seals during diving in the laboratory. Physiol. Zool. 71,116 -125.[Medline]
Webb, P. M., Crocker, D. E., Blackwell, S. B., Costa, D. P. and Le Boeuf, B. J. (1998b). Effects of buoyancy on the diving behavior of northern elephant seals. J. Exp. Biol. 201,2349 -2358.[Abstract]
Williams, T. D. and Siniff, D. B. (1983). Surgical implantation of radio telemetry devices in the sea otter. J. Am. Vet. Med. Assoc. 183,1290 -1291.[Medline]
Williams, T. D., Allen, D. D., Groff, J. M. and Glass, R. L. (1992). An analysis of California sea otter (Enhydra lutris) pelage and integument. Mar. Mamm. Sci. 8, 1-18.[CrossRef]
Williams, T. M. (1989). Swimming by sea otters: adaptations for low energetic cost of locomotion. J. Comp. Physiol. A 164,815 -824.[CrossRef][Medline]
Williams, T. M. (1999). The evolution of cost efficient swimming in marine strategies for cost-efficient diving by marine mammals. Science 288,133 -136.
Williams, T. M., Haun, J., Davis, R. W., Fuiman, L. A. and Kohin, S. (2001). A killer appetite: metabolic consequences of carnivory in marine mammals. Comp. Biochem. Physiol. 129A,785 -796.
Williams, T. M., Estes, J. A., Doak, D. F. and Springer, A. M. (2004a). Killer appetites: assessing the role of predators in ecological communities. Ecology 85,3373 -3384.[CrossRef]
Williams, T. M., Fuiman, L. A., Horning, M. and Davis, R. W.
(2004b). The cost of foraging by a marine predator, the Weddell
seal (Leptonychotes weddellii): pricing by the stroke. J.
Exp. Biol. 207,973
-982.
Withers, P. C. (1977). Measurement of
O2,
CO2 and
evaporative water loss with a flow through mask. J. Appl.
Physiol. 42,120
-123.
Wolrab, S. (2003). Prey handling in the southern sea otter (Enhydra lutris nereis): a study of inter-individual variation in handling behavior and the acquisition of prey handling skills. Masters thesis, Universitat Bielefeld, Germany.
Yeates, L. C. (2006). Physiological capabilities and behavioral strategies for marine living by the smallest marine mammal, the sea otter (Enhydra lutris). PhD dissertation, University of California Santa Cruz, USA.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
