Aquatic Mammals 2006, 32(3), 363-369, DOI 10.1578/AM.32.3.2006.363
Field Metabolic Rates of Walrus (Odobenus rosmarus)
Measured by the Doubly Labeled Water Method
Mario Acquarone,1 Erik W. Born,2 and John R. Speakman3
1
National Environmental Research Institute, Frederiksborgvej 399, DK-4000 Roskilde, Denmark
2
Greenland Institute of Natural Resources, P.O. Box 570, DK-3900 Nuuk, Greenland
3
Aberdeen Centre for Energy Regulation and Obesity (ACERO), School of Biological Sciences,
University of Aberdeen, Aberdeen AB3 2TZ, United Kingdom
Current Address: Frue Kirkestræde 5, DK-5000 Odense, Denmark (MA)
Abstract
Introduction
The energy and food requirements of free-ranging
pinniped species are difficult to measure and, as a
consequence, are unknown for most species. They
can be inferred from measures of Field Metabolic
Rate (FMR) made by the Doubly Labeled Water
(DLW) method, however. In this work, we confirmed
our hypothesis that the FMR of pinnipeds measured
by DLW can be described by an allometric relationship as a function of body weight. Although costly
and difficult to apply, the DLW method is one of the
few possible methods generating estimates of energy
demands for unrestrained, free-living animals. The
results of its application on two adult, male, freeliving Atlantic Walruses (Odobenus rosmarus rosmarus), weighing 1,370 kg and 1,250 kg, respectively,
estimated from length and girth measures, are presented here. These data extend the size range of the
seven pinniped species for which the DLW method
has been applied by a factor of 10. The animals were
measured at a site in northeast Greenland (76° N)
during the summer. FMR was dependent on the pool
model for estimating metabolic rate and was approximately 13% higher when using the single-pool compared with the two-pool model. The estimates using
the two-pool model were 328.1 (SE 8.7) MJ•day -1
and 365.4 (SE 15.4) MJ•day -1 for each of the two
walruses. These figures were combined with estimated FMR using the same method in seven other
pinniped species to derive a new, refined predictive
equation for pinniped FMR (Ln-FMR [MJ•day -1] =
0.173 + 0.816 Ln-Total Body Mass [kg]). This equation suggests that pinniped food requirements might
sometimes be twice as high as that assumed in some
fisheries models, which are based on multiples of the
theoretical basal metabolism.
Conflicts between fisheries and marine mammals have escalated and are likely to increase
during the next century (DeMaster et al., 2001).
Fisheries models for evaluating the impact of
marine mammal predators on fish stocks require
accurate estimates of food intake rates (Innes
et al., 1987; Bowen, 1997; Trites et al., 1997;
Bjorge et al., 2002; Winship et al., 2002). Field
energy demands (generally called Field Metabolic
Rate or FMR) and thus food consumption rates of
free-ranging marine mammals have been estimated
from their heart rate (Boyd et al., 1999) or by multiplying their inferred Basal Metabolic Rate (BMR)
by some factor (Innes et al., 1987). While heart
rate monitoring is a valuable method for estimating metabolic rates (Butler et al., 2004), it requires
species-specific validation of the relationship
between heart rate and metabolic rate, and it may
not accurately reflect metabolic rates during digestive events (McPhee et al., 2003). Furthermore, the
adaptations of marine mammals to diving—for
example, bradycardia (Elsner, 1999)—may complicate its interpretation. On the other hand, the use
of BMR to estimate food consumption of marine
mammals is problematic because the conditions
required for the measurement of BMR were established for terrestrial animals (White & Seymour,
2003) and may be inappropriate for marine mammals. Moreover, individual estimates for species
around an allometric prediction of BMR are often
substantially discrepant, and the multiplication
factor used to convert basal to field metabolism
generates its own uncertainty in the final result.
In consequence, the resultant estimates using this
BMR-factorial approach may easily be in error by
a factor of 2.
An alternative approach is to calculate the
energy demands from CO2 production, measured from the differential elimination of two
Key Words: Walrus, Odobenus rosmarus, field
metabolic rate, feeding rates, pinnipeds, Doubly
Labeled Water, Greenland
364
Acquarone et al.
isotopic tracers in body water known as the
Doubly Labeled Water (DLW) technique (Lifson
& McClintock, 1966; Speakman, 1997; Costa &
Gales, 2003). This technique avoids some of the
problems associated with the other methods, and
the resultant FMR measurement can be incorporated directly into fisheries and other ecological
models. A problem with the DLW technique is the
high cost of the isotopic labels, which increases
enormously with body mass (Butler et al., 2004).
Because of the high costs of working on larger
species, the seven pinniped species for which
DLW estimates of FMR have been published
are far lighter than the largest species (Reeves
et al., 1992) and ranged only between 27 and
114 kg (Nagy et al., 1999; Costa & Gales, 2003).
A reliable allometric equation for FMR versus
body mass (BM) can be generated for animals
within this BM range (Nagy et al., 1999), but the
predicted estimates for larger animals are potentially inaccurate due to extreme extrapolation,
which has perhaps contributed to the reluctance
of modelers to include DLW measurements into
fisheries model calculations. Our hypothesis for
this work was that FMR of pinnipeds measured
by DLW can be described by an allometric relationship as a function of body weight, which is
valid for a large part of the spectrum of pinniped
body sizes.
In this study, we used the DLW method to estimate the FMR of two free-ranging male walruses.
The BM of the two animals in this study extends
by ten-fold the mass of the previous largest pinniped measured by the DLW method (and they are
by far the largest animals studied using this methodology). These estimates extend the validity of
the allometric equation for pinniped FMR across
most of the body size ranges of pinnipeds.
Materials and Methods
Study Site and Animals
The study animals, all adult male Atlantic walruses (O. r. rosmarus) (Table 1), were chosen from
an all-male group on a terrestrial haulout site in
northeast Greenland at 76° 52.8' N, 19° 37.9' W
(Born et al., 1995). In August 2001, two walruses
were enriched with DLW. Before handling, they
were completely immobilized (Born & Knutsen,
1992a). During immobilization, the animals’ axillary girth and standard body length (American
Society of Mammalogists, 1967) were measured for estimation of Total Body Mass (TBM)
(Knutsen & Born, 1994; Born et al., 2003); a satellite radio and a time-depth recorder (TDR) were
attached, one on each tusk; and venous access
was gained by catheterization of the epidural vein
in the lumbar region for isotope enrichment and
blood sampling. Upon recapture, a similar immobilization procedure was used, the size measures
were repeated, and blood sampling and instrument
data were retrieved.
For comparison, in August 2000, three other
walruses and an additional walrus in 2001 were
also instrumented with satellite radios and TDRs
to obtain behavioral data, but they were not
enriched with DLW. By monitoring the activity
patterns of a control group of animals not using
DLW, we could confirm that the behavioral patterns of the animals that were measured were not
adversely affected by the DLW protocols and are,
hence, relevant more widely than the small sample
we could afford to inject with isotopes.
Energy Expenditure
At initial capture, the two designated animals’
venous blood was sampled through the catheter for
determination of background isotope concentration. Each animal was subsequently administered
an intravenous dose of 97.75 g of deuterated water,
43.9% 2H2O (Merck 1.13366, E.Merck, D-6100,
Darmstadt, Germany), and 157.62 g of 18Oxygenenriched water, 41.5% H218O (Rotem Industries
Ltd., P.O. Box 9046, Beer-Sheva 84190, Israel). A
series of blood samples was then taken at approximately 30-min intervals for 4 h for determination of
the isotope equilibration curve and isotope dilution
spaces. Animal A was enriched on 16 August 2001
at 1642 h (all times reported are Universal Time
[UT]) and recaptured on the 21 August 2001 at
1752 h. Animal B was enriched on 7 August 2001 at
2108 h and recaptured on 16 August 2001 at 1530 h.
Immediately after sampling, whole blood was flame
sealed into 100-ml precalibrated glass pipettes
(Modulholm A/S, Vasekaer 6-8, DK-2730 Herlev,
Denmark, VITREX model 1272). Seawater background samples were collected and flame sealed
in 2.0-ml glass vials throughout the experimental
period to investigate variation in environmental isotope enrichment. All samples were stored at ambient temperature (max. 3° C) while in the field (max.
20 d) and were subsequently kept refrigerated at 5°
C prior to analysis.
All blood samples were vacuum distilled into
Pasteur pipettes (Nagy, 1983), and the distillate was used for determination of both 18O and
2
H concentration. For 2H-analysis H2 gas was
produced by reduction with excess LiAlH2 as
described in Ward et al. (2000). For 18O-analysis,
10 ml of distillate was measured using the small
sample equilibration method (Speakman et al.,
1990). The isotopic composition of the injectate
was measured by diluting a weighed quantity of
the injectate (0.1 to 0.2 ml) into a weighed quantity of tap water (60 ml). This mixture was then
treated in exactly the same manner as the distillate
365
Field Metabolic Rates of Walrus
from the blood samples. In each batch of samples
for analysis, laboratory standards were included to
account for day-to-day variation in the analyzer.
All isotope enrichments were measured in d-units
and converted to ppm using the established ratios
for reference materials. We evaluated precision of
the derived estimate of CO2 production using the
iterative procedures in Speakman (1995) and converted the mean estimate to metabolic rate assuming an RQ of 0.85. Calculations were made using
the DLW program (Version 1.0, Speakman and
Lemen, Naturware, 1999).
Activity of the Animals
The two study animals and four other walruses
were instrumented with satellite-linked radio
transmitters and TDRs to obtain data on movement, haulout, and dive activity (Table 1).
An ARGOS System SPOT2 satellite-linked radio
transmitter with “time at temperature” histograms
and a MK7 TDR with 500-m range (Wildlife
Computers, 16150 NE 85th Street, Suite 226,
Redmond, WA 98052, USA) were each attached to
a tusk of six adult male walruses, using the method
in Born & Knutsen (1992b). The TDRs were programmed to sample depth, temperature, and light
level at intervals of 5, 300 and 300 or 15, and 600
and 120 s, respectively. The GIS software ArcView,
Version 3.2a, was used for calculation of the horizontal movement of the walruses after satellite-telemetered locations of all-quality classes had been run
through a PC-SAS®ARGOS-filter, Version 5.0 (D.
Douglas USGS, Alaska Science Center, 100 Savikko
Road, P.O. Box 240009, Douglas, AK 99824, USA,
unpub. method).
The TDR data were analyzed using the
software provided by the manufacturer (the
Zero-Offset-Correction and Dive-Analysis). Periods
when the walruses were hauled out on land or ice
were excluded from the analysis of dive activity.
Minimum depth for dives to be analyzed and maximum depth to be considered at surface were set to
6 m. The time spent at sea or out of the water was
determined by analyzing the temperature record of
the TDR, where only temperatures below 2.5° C
were considered as coming from a submerged
sensor. Numbers of dives, dive duration, and surface
times were also determined for each individual.
Results
All six animals spent on average 33.0% of their
time hauled out (Table 1), which is typical of walruses during summer (Born et al., 1997). Diving
activity accounted for 50.8% of the time spent
at sea, with an average rate of 165 dives per day,
each lasting 3.5 to 5.5 min (Figure 1; Table 1).
Although the time spent hauled out by the two
DLW animals was similar, Animal B was diving
more actively than Animal A as indicated by the
number of dives per day, the mean dive duration
and dive depth, and the maximum depth reached
(Table 1). The data for the two DLW animals
did not differ from the other four controls in any
parameter studied.
A previous study (Lydersen et al., 1992) had
suggested that isotopes (tritium) in walruses
might equilibrate with body water within 1 h. We
found, however, that equilibration time of the isotopes took approximately 2.5 to 3.0 h. We therefore used these estimates of the initial isotope
enrichment combined with the recapture samples
to estimate FMR. Environmental background isotope enrichments measured in sea water did not
fluctuate significantly during the study period and
did not differ significantly from the background
enrichments in the animals’ blood collected prior
to injection.
Body water (BW) percentage of BM from dilution of the oxygen isotope was 45.0% in Animal
A and 49.5% in Animal B. The lower BW content of the larger Animal A suggested that it had
relatively more body fat. The estimated FMRs
were 345.0 (SE 7.5) MJ•day -1 for Animal A and
Table 1. Activity of six adult male walruses in northeast Greenland during August 2000 and 2001; the energy expenditure
of Animals A and B was determined using DLW in 2001. Animals D, E, and F were studied in 2000; and A, B, and C were
studied in 2001.
ID
A
B
C
D
E
F
Average
Condition
Mass
kg
Days
monitored
n
Time
hauled out
%
Dives/day
n
Mean dive
duration
min (sd)
Mean depth
m (sd)
Max depth
m
DLW
DLW
Control
Control
Control
Control
Control
1,370
1,250
1,546
1,115
1,086
1,284
1,275
5.0
8.7
14.9
12.0
7.2
12.0
10.0
27.2
27.2
41.1
47.8
34.5
20.0
33.0
108
133
208
170
200
170
165
3.5 (2.1)
4.4 (2.1)
4.8 (1.8)
5.1 (1.4)
4.9 (1.1)
5.5 (2.2)
4.7
12.6 (5.5)
15.8 (10.5)
14.9 (12.9)
12.1 (5.1)
11.3 (4.2)
12.3 (7.6)
13.2
55
145
192
84
51
189
119
366
Acquarone et al.
Figure 1. Dive profiles measured by use of time-depth recorders in six adult male walruses in northeast Greenland in August
2000 and 2001 (see also Table 1)
417.4 (SE 6.2) MJ•day -1 for Animal B, using
the single-pool model for calculation (Lifson &
McClintock, 1966) (mean = 381.2 MJ•day -1).
Using the two-pool model (Speakman, 1997) and
the mean observed dilution space ratio of 1.09
(Schoeller et al., 1986), the corresponding estimates were 328.1 (SE 8.7) MJ•day -1 and 365.4
(SE 15.4) MJ•day -1, respectively (mean = 346.8
MJ•day -1). A best-fit relationship between FMR
and BM, including only the previous DLW studies of pinnipeds (Table 2; Lifson & McClintock’s
[1966] single-pool calculation) explained 88.3%
of the variation in FMR. For a pinniped weighing 1,300 kg, this equation would predict an FMR
of 665 MJ. The direct estimate of FMR in the
present study was 43.0% lower than this prediction, highlighting the difficulties of extrapolation
beyond the original data from which the equation
was generated. This discrepancy clearly indicated the need for a more precise equation for
larger pinnipeds. We derived such an equation
using the estimated FMR for the walrus measured here based on the single-pool model. The
new allometric equation (Ln-FMR [MJ•day 1] = 0.173 + 0.816 Ln-Total Body Mass [kg]) for
Table 2. Average body mass and Field Metabolic Rate
by the Doubly Labeled Water method in eight species of
pinnipeds
BM
[kg]
FMR
[MJ/d]
Arctocephalus
galapagoensis
Arctocephalus gazella
27.0
11.7
34.2
25.7
Callorhinus ursinus
43.4
30.6
Neophoca cinerea
76.4
40.9
Zalophus californianus 78.0
38.6
Species
Scientific name
Galapagos
fur seal1
Antarctic
fur seal1, 2
Northern
fur seal1, 2
Australian
sea lion1, 2
Californian
sea lion2
Harbour seal2
New Zealand
sea lion1, 2
Walrus3
Phoca vitulina
Phocarctos hookeri
Odobenus rosmarus
99.0
114.1
52.5
68.0
1,310.0 381.2
Costa & Gales, 2003; Nagy et al., 1999; this study
1
2
3
367
Field Metabolic Rate of Walrus
Figure 2. Field Metabolic Rate (FMR) in relation to body
mass (BM) in eight different pinniped species based on
measurements using the Doubly Labeled Water method
(actual data and references in Table 2); 95% confidence
intervals of the regression are shown as dashed lines.
pinniped FMR explained 96.1% of the variation
(n = 8 species) (Figure 2). Including data on
diving behavior and activity (where available) did
not improve the relationship.
Discussion
An FMR of 381 MJ•day -1 for a 1,300 kg walrus
as measured in this study corresponds to the consumption of about 95 kg food per day (fresh matter)
calculated from the mean energy composition of
the walrus prey items from East Greenland (Born
et al., 2003) and assuming the average digestive
coefficient for energy for a clam diet (92.7%)
(Fisher et al., 1992). This value is within and at
the upper end of the previously estimated range of
42 to 92 kg food intake for free-ranging walruses
weighing 1,100 to 1,200 kg (Fay, 1982).
The greater FMR value of Animal B may have
been due to its higher diving activity (Table 1).
The mean haulout time for all six animals measured by TDR in this study was similar to previous
estimates from this and other areas: 30% from this
area (Born & Knutsen, 1997), 26% from Alaska
(Hills, 1992), and 26% from Svalbard (Gjertz
et al., 2001). Variability in haulout time between
individuals at all sites is considerable (Born &
Knutsen, 1997; Gjertz et al., 2001) as was also
observed in the present study.
For consistency with the previous studies, the
single-pool equation of Lifson & McClintock
(1966) to derive FMR was used here but this
equation overestimates energy demands for animals that are larger than 5 to 10 kg (Speakman,
1997). A two-pool model calculation is probably
more appropriate. Since most papers do not quote
the necessary parameters to make recalculations,
we were unable to construct a prediction based on
the two-pool method. Our estimates, and those of
Costa & Gales (2003), indicated that the overestimate using the single-pool method (Lifson &
McClintock, 1966) might only be 9 to 17% (averaging 13%). Since we had to derive a predictive
equation based only on the single-pool model,
this overestimate of food requirements should be
borne in mind if the equation is utilized in a predictive manner.
Current fisheries models that have utilized estimated daily food consumption predicted from multiples of BMR (predicted
from BM using the Kleiber equation [Kleiber,
1932, 1961]) have routinely assumed that the
FMR of pinnipeds is around 3x BMR (Trites
et al., 1997; Nilssen et al., 2000; Bjorge et al.,
2002; Winship et al., 2002). Our study, along with
the other DLW studies contributing to the derived
equation, however, suggested that this is a serious
underestimate of pinniped food intake even if the
overestimate from using the single-pool model is
taken into account. FMRs derived from the equation in this study averaged between 5.5 (for a
100-kg seal) and 6.5 (for a 1,300-kg seal) times
the Kleiber BMR prediction (4.8x to 5.7x if the
13% lower estimate from the two-pool model is
used). Using these direct estimates of FMR would
more than double the estimated daily food requirements of pinnipeds and their projected impacts on
prey species. Consequently, many current fisheries
models may seriously underestimate the impacts
of marine mammal predators on fish stocks.
The allometric equation for pinniped FMR
derived here can be utilized to revise the impact of
pinnipeds on fish stocks in fisheries models since
it provides a mass-specific prediction of FMR for
most species without the need for extrapolation.
Most importantly, it is based on direct measurements of FMR, rather than inferences from multiples of basal metabolism. The costs of the DLW
method preclude its routine use in studies of the
energetics of larger pinniped species such as the
walrus. Nevertheless, the current study demonstrated that occasional measurements of FMR can
improve and refine the assumptions that underpin
models being used to assess levels of competition
between seals and fisheries.
Acknowledgments
We thank the veterinarians, D. Griffiths and T.
Møller, for immobilizing the walruses, P. Thomson
for technical assistance in the isotope analysis, and
P. Thompson for commenting on the draft of this
paper. The Danish Natural Science Foundation
supported this study financially together with
the employers of the authors (in particular, the
368
Acquarone et al.
Commission for Scientific Research in Greenland,
the Greenland Institute of Natural Resources,
the Danish National Environmental Research
Institute, and the University of Aberdeen) and the
European Commission’s MCTS.
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