1. Zool., Lond. (1996) 239, 769-782
The relationship between foraging behaviour and energy expenditure
in Antarctic fur seals
J. P. Y.
ARNauLD,
I. L.
BOYD
British Antarctic Survey, Natural Environment Research Council,
High Cross, Madingley Road, Cambridge CB3 GET, UK
AND
J. R.
SPEAKMAN
Department of Zoology, University of Aberdeen. Aberdeen AB9 2TN, Scotland
(Accepted 2 August 1995)
(With 3 figures in the text)
By using time-depth recorders to measure diving activity and the doubly-labelled water method
to determine energy expenditure, the relationship between foraging behaviour and energy
expenditure was investigated in nine Antarctic fur seal females rearing pups. At-sea metabolic
rate (MR) (mean of 6.34 ± 0.4 W· kg": 4.6 times predicted BMR) was positively correlated to
foraging trip duration (mean of 4.21 ± 0.54 days; r 2 = 0.5, P < 0.04). There were no relation­
ships between MR and the total number of dives, the total time spent diving or the total vertical
distance travelled during the foraging trip. There was, however, a close negative sigmoidal
relationship (r2 = 0.93) between at-sea MR and the proportion of time at sea spent diving. This
measure of diving behaviour may provide a useful, inexpensive means of estimating foraging
energy expenditure in this species and possibly in other otariids. The rate of diving (m- h -1) was
also negatively related to at-sea MR (r2 = 0.69, P < 0.005). Body mass gain during a foraging
trip had a positive relationship to the time spent at sea (r2 = 0.58, P < 0.02) and the total
amount of energy expended while at sea (r2 = 0.72, P < 0.004) such that, while females
undertaking long trips have higher metabolic rates, the energetic efficiency with which females
gain mass is independent of the time spent at sea. Therefore, within the range of conditions
observed, there is no apparent energetic advantage for females in undertaking foraging trips of
any particular duration.
Introduction
To satisfy the energetic cost of milk production, maternal food consumption must be increased
prior to, and/or during, lactation (Sadleir, 1984). During lactation, however, maternal foraging
activities may be hindered by the offspring: when foraging in the company of their offspring,
females have to spend more time being vigilant, and/or consume food oflower quality, in areas of
reduced danger from predators (Sadleir, 1969; Carl & Robbins, 1988); when foraging alone,
females are restricted in their foraging range by the fasting ability of the offspring and/or the
amount of resources they can carry (Broekhuizen & Maaskamp, 1980; Sadleir, 1984; Gittleman,
1988; Gittleman & Thompson, 1988). Maternal foraging efficiency (amount of energy consumed
per unit of energy expended while acquiring it) will therefore influence the rate at which the
mother can deliver resources to her offspring (Sadleir, 1984). This, in turn, will affect the growth
rates of the dependent offspring and the overall cost to the mother of successfully rearing them
(Gittleman & Thompson, 1988). Foraging activity in relation to provisioning rates is therefore of
769
(Q) 1996 The Zoological Society of London
770
J. P. Y. ARNOULD, 1. L. BOYD AND J. R. SPEAKMAN
major interest and has been the focus of numerous studies (e.g. Sadleir, 1982; Gittleman, 1988;
Allaye Chan-McLeod, White & Holleman, 1994).
Obtaining accurate measurements of energy expenditure under field conditions is complicated,
involving the use of labelled isotope techniques (Lifson & McClintock, 1966; Nagy, 1980;
Speakman & Racey, 1988) or the recording of heart rates (e.g. Butler et al., 1992; Boyd et al.,
1995b; Woakes, Butler & Bevan, 1995). Consequently, many studies have relied instead on
measurements of behaviour and activity-specific energy expenditure (time-energy budgets) to
obtain estimates offree-ranging energy expenditure (Weathers et al., 1984; Bennett, 1986; Nagy,
1989). In the study of seals (Pirmipedia), diving behaviour has been examined with the use of
time-depth recorders (TDRs; Gentry & Kooyman, 1986; Boyd & Croxall, 1992) to provide
indices of foraging effort (e.g. Croxall et al., 1985; Feldkamp, De Long & Antonelis, 1989; Testa,
Hill & Siniff, 1989; Boyd et al., 1994). Whereas energy expenditure has been measured in several
seal species (Costa & Gentry, 1986; Costa et al., 1989, 1991; Reilly, 1991; Lydersen & Hammill,
1993), the relationship between diving behaviour and energy expenditure has received little
attention (Butler et al., 1995). The ability to estimate foraging energy expenditure in seals from
behavioural information is therefore limited.
During lactation, fur seals and sea lions (Pinnipedia: Otariidae) alternate between short
nursing periods ashore and regular foraging trips to sea (Bonner, 1984). Studies of Antarctic fur
seal (Arctocephalus gazella) maternal attendance patterns have shown that some females
consistently undertake long trips (6-8 days), whereas others regularly make short trips (2-4
days) (Boyd, Lunn & Barton, 1991; Lunn et al., 1993). Boyd et al. (1991) found that females
making short foraging trips had a higher dive rate (metres dived per unit time) than those making
longer trips and suggested that as a result their rate of energy expenditure might be higher than
that oflong-trip females. Therefore, it might be predicted that females regularly undertaking long
foraging trips would expend less energy throughout lactation than those making short trips. Such
differences might have important implications for the overall cost of pup-rearing and inter­
individual variation in reproductive success (Clutton-Brock, Guinness & Albon, 1983; Clutton­
Brock, 1988). The foraging energy expenditure of Antarctic fur seals has previously been
examined in years of contrasting prey availability by Costa et al. (1989) but no data are available
on how it varies in relation to the range of foraging behaviours observed between individuals in
years of normal food abundance.
The aims of this study were: (1) to investigate the relationships between diving behaviour and
energy expenditure in Antarctic fur seals and (2) to assess whether there are differences in the
energetic costs, and efficiency, between the various foraging strategies they employ.
Methods
Study site and animals
The study was conducted at Bird Island (54°00' S, 38°02' W), South Georgia, during two consecutive
lactation periods (austral summers of 1991/92 and 1992/93). Hereafter, the year or sampling refers to the
year in which the summer began (i.e. year 1991 equals summer 1991/92). All study animals were mothers of
known-age pups selected at random throughout the lactation period from a group of 300 animals that had
been observed to give birth between I and 6 December. One of the study animals had previously been used in
Costa et al.'s (1989) study of Antarctic fur seal field metabolic rates in 1983 and 1984.
FUR SEAL FORAGING ENERGETICS
771
Foraging behaviour and trip duration
All seals were captured by standard noose-pole and restraint board techniques (Gentry & Holt. 1982).
Upon initial capture, females were weighed with a spring scale (100 ± 0.5 kg) and straight-line length was
measured to the nearest centimetre with a tape measure. Each animal was fitted with a small (40 g,
2 x 2 x 7 em) 165MHz radio-transmitter (Advanced Telemetry Systems Inc., Minnesota, USA) and a
Wildlife Computers MKIII time-depth recorder (TDR) (Wildlife Computers, Woodinville, WA, USA) on
the dorsal surface. The transmitter was glued directly to the fur while the TDR was clasped by nylon cable­
ties to a strip of nylon webbing (width 2 em) which was in turn glued to the dorsal fur by quick-setting epoxy
glue. Foraging trip duration and attendance were monitored by automatic receiving stations at the colony
linked to computer data-loggers (Boyd et al., 1991). Each animal was recaptured and weighed at the end of
one foraging trip and the instruments were removed.
The TDRs were programmed to sample at 10 s intervals when the animals were at sea. Diving behaviour
was analysed with the Wildlife Computers Dive-analysis software and only dives> 2 m were considered. The
total number of dives, number of divers per hour at sea, the total time spent diving (time submerged to a
depth >2 m), the proportion of time at sea spent diving, the total vertical distance travelled whilst diving and
the vertical distance travelled per hour at sea were recorded for each individual.
Energy expenditure
Energy expenditure was measured by the doubly labelled water (DLW) method (Lifson & McClintock.
1966; Nagy, 1980; Speakman, 1993). Upon capture. an initial blood sample (5 ml) was collected into a
heparinized syringe in order to determine the background levels of the injected isotopes. All blood samples
were collected by venipuncture of an interdigital vein in a hind flipper. Each animal was then given an oral
dose, by stomach tube, of 60-70ml H 218 0 10% AP (Isotec Inc., Miamisburg, OH, USA) and a 2ml
intramuscular injection of a weighed dose (± 0.0 I g) of tritiated water (HTO; 200 f.LCi. ml- 1). Each animal
was kept in an enclosure for 6 h, during which it was fitted with the TDR and transmitter. A second blood
sample (5 ml) was then collected before the animal was released. The time required for isotope equilibration
had previously been determined, by serial blood sampling of individuals, to be less than 2 and 4 h for
intramuscular (Costa, 1987: Arnould, Boyd & Speakman, 1996) and oral dosing (Fig. 1), respectively.
Females were recaptured when they next returned from a foraging trip and weighed, and a third blood
sample (5 ml) was collected.
All blood samples were stored at 4 "C for several hours before being centrifuged and the plasma fraction
separated. For HTO analysis. sub-samples (1-2 ml) of plasma were stored frozen (-20 '~C) in plastic vials
until analysed in November 1993. For H 2 180 analysis, aliquots (25-50111) of plasma were stored in flame­
sealed capillary tubes until analysis in January 1995.
To measure the specific activity of tritium in plasma, samples were thawed and 0.2 ml sub-samples were
distilled into pre-weighed scintillation vials following the procedures of Ortiz, Costa & Le Boeuf (1978). The
vials were then re-weighed to obtain the mass of the water sample, accurate to 0.1 mg. Scintillant (10 ml
Ultima Gold; Canberra Packard, Brook House, Pangboume, Berkshire, UK) was added to the vials which
were then counted for 10min in a Beckman LA170l scintillation counter with correction for quenching by
means of the sample channels ratio and an external standard to set the counting window for each vial.
Samples were analysed in duplicate and each vial was counted twice. Sub-samples (0.2 ml) of the injectant
were counted in the same way, and at the same time, as the water from the plasma samples, in order to
determine the specific activity of the tritium injected.
For 180xygen analysis, a modified version of the pasteur pipette method of Nagy (1983) was used to
vacuum-distil water from 100f.Ll plasma samples. This differed from the original protocol only in that the
sample was frozen under liquid nitrogen whilst the pipette was evacuated. The 180xygen content of the
derived water samples was evaluated by using a small sample equilibration technique. Briefly, approximately
20 f.Ll of the water sample was pipetted into the base of a pre-weighed (±O.OOO I g) 5 ml vacutainer which had
J. P. Y. ARNOULD, I. L. BOYD AND J. R. SPEAKMAN
772
10
9
t,....
8
0
o
-------,----,------.------,----.---------,
120
180
240
60
300
360
Time (min)
FIG. I. The specific activity of tritium in water distilled from plasma samples, serially collected following a pulse dose
of HTO administered orally, in five Antarctic fur seal females. Each symbol represents a separate individual.
its rubber cap removed. The vacutainer was re-weighed to obtain the mass of the water sample and then
recapped. The water samples in the vacutainer was frozen under liquid nitrogen and the air above it removed
with a small-gauge needle attached to a vacuum pump. The vacutainer was then allowed to return to room
temperature before 4ml of pure, previously isotopically characterized, carbon dioxide was drawn from a
tank of gas and introduced into the vacutainer with a gas-tight Hamilton syringe. Two vacutainers were
prepared in this way from each water sample.
Each vacutainer was incubated at 60 DC for 24 h to allow the oxygen in the water to come to isotopic
exchange equilibrium with the CO 2 in the vacutainers. Thereafter the vacutainers were frozen, using an
acetone-dry ice trap, to retain the water and the CO 2 was drawn off under vacuum and subdivided between
two separate breakseals. Each plasma sample thus generated 4 separate breakseal samples. The samples
were admitted directly to the inlet of a gas source isotope ratio mass spectrometer (Optima, VO Instruments)
and run in comparison to a known working standard. Delta values were normalized to the SMOW/SLAP
scale and were converted to ppm units using the absolute ratio of 0.0020052 for SMOW. This gas
preparation and analysis procedure has been previously validated in comparison to other methods and
found to provide accurate and precise results over a wide range of isotope enrichments (Speakman et al.,
1990; Roberts et al., 1995).
Because the H 2 18 0 was administered orally, we were not confident that the animals would receive an
accurately measured dose and, hence, oxygen dilution space could not be determined. Total body water
(TBW) was, therefore, calculated from the relationship between TBW and tritium dilution space by using
the equation:
TBW(kg)
=
0.11 + 0.97 . HTO space(kg)
determined empirically by Arnould et al. (1996) in Antarctic fur seals. Total body water at the end of the
study period was calculated by multiplying the fractional water content at the beginning of the study by
body mass upon recapture.
FUR SEAL FORAGING ENERGETICS
773
Carbon dioxide production can be calculated from DLW measurements by means of several different
standard equations available in the literature (Lifson & McClintock, 1966; Coward & Prentice, 1985;
Schoeller et al., 1986; Speakman, 1993; Speakman, Nair & Goran, 1993). Tn a study comparing estimates of
California sea lion (Zalophus californianusi CO 2 production determined through various equations, Boyd et
al. (1995b) found that Speakman et al.'s (1993) equation (Rl) provided the estimate closest to that measured
by respirometry. Hence, CO 2 production rates calculated by using this equation, accounting for any changes
in TBW, are presented for the animals in the present study.
A constant of 25.2 J . mr ' was used to convert CO 2 production to energy expenditure (Costa, 1987). This
was calculated from the average Antarctic fur seal diet and the calorific value of its chemical components
(Clarke, 1980; Croxall & Pilcher, 1984; Reid & Arnould, 1996). Time ashore was calculated as the difference
between the duration of the energy expenditure measurement and the time at sea (determined by radio­
telemetry). At-sea metabolic rate (MR, W .kg- l ) was then calculated for each animal by solving the
equation given by Costa et al. (1989):
MeasuredMR = [(AshoreMR)'(Proportionoftimeashore)]
+ [(At-seaMR)· (Proportion of time at sea)],
assuming the metabolic rate while ashore to be 4.96 W . kg-I, the rate reported for Antarctic fur seal females
ashore during the perinatal fast (Costa & Trillmich, 1988).
Statistical analyses followed methods outlined in Sokal & Rohlf (1981) and Zar (1984) using Unistat'P
Statistical Package (Version 4.5, Unistat Limited, London, UK). The Kolmogorov-Smirnov test was used to
determine whether data were normally distributed and an F-test was used to confirm homogeneity of
variances. Unless otherwise stated, data are presented as means ±l S.E. and results were considered to be
significant at the P < 0.05 level.
Results
In total, 14 animals were instrumented and dosed with DLW (six in 1991 and eight in 1992) but
upon recapture isotope levels were too close to background to determine CO 2 production in five
of the seals (four in 1991 and one in 1992). These animals were excluded from further analyses.
The body mass, TBW, isotope clearance and CO 2 production rates for the remaining individuals
are presented in Table I. Body mass change, metabolic rate, and diving behaviour are presented
in Table II.
The mean at-sea MR was 6.34±0.5W.kg- 1 (n=9), recorded for a mean foraging trip
duration of 4.21 ± 0.54 days. At-sea MR, however, was positively correlated with foraging trip
duration (r 2 = 0.5, P < 0.04; Fig. 2a). There was a positive relationship approaching significance
(r2 = 0.36, P = 0.09) between at-sea MR and the total number of dives (1222 ± 103) made
during the foraging trip. The total time spent diving (18.8 ± 1.3 h) and the total vertical distance
travelled (46.1 ± 0.51 km) during the foraging trip were not related to at-sea MR (P > 0.5 in both
cases). The proportion of time at sea spent diving (20.4 ± 1.9%), however, was negatively
correlated to at-sea MR (r2 = 0.76, P < 0.001). This relationship was found to approximate a
sigmoid curve with the equation:
M Rs
=
3.23
(1 + e 0 7S.(x-1671))
+ 5.26
r2 =
0.93
(Fig. 2b) where x = the proportion of time at sea spent diving (%) and MRs = At-sea MR
(W· kg "). At-sea MR was also negatively related to the rate of diving (469.4 ± 34.5 m- h- I )
during the foraging trip (r2 = 0.69, P < 0.005, Fig. 2c). There was also a negative relationship
between the number of dives made per hour at sea (13.0 ± 1.0 dives- h- I ) and at-sea MR, which
approached significance (r2 = 0.41, P = 0.061).
-.j
-.j
+­
'--'
TABLE I
Percentage TBW, bodv mass, measurement interval, percentage rime at sea, tritium and 180 clearance rates (k, and k o ' respectively ), CO 2 production rates and
metabolic rate ofAntarcticfur sealfemales fitted with TDRs
'"d
~
>.
~
Z
o
Body mass (kg)
Seal
TRW
(%)
Initial
Final
2
3
4
5
6
7
8
9
Mean
S.E.
63
55
68
68
66
67
69
69
66
65.7
1.5
32.5
45.0
36.5
38.5
39.0
32.0
36.5
36.5
28.5
36.1
1.5
33.0
46.0
40.5
42.5
39.0
32.5
38.0
38.0
28.0
37.5
Study interval
(days)
Time at sea
(%)
k.
(h- I )
ko
(h- I )
let/ko
CO 2 production
(m1'min- 1 • kg-I)
6.03
3.92
7.00
9.03
3.58
4.67
2.79
6.58
4.71
5.37
0.62
77.3
81.8
76.2
83.6
61.6
86.6
89.6
79.7
64.6
77.9
3.0
0.0132
0.0100
0.0122
0.0115
0.0137
0.0126
0.0186
0.0110
0.0121
0.0128
0.0008
0.0162
0.0127
00152
0.0141
0.0161
0.0160
0.0215
0.0134
0.0145
0.0156
0.0008
0.815
0.784
0.801
0.782
0.853
0.787
0.865
0.819
0.834
0.816
0.009
14.67
12.15
16.43
18.00
11.43
18.46
1402
13.21
12.21
14.51
0.81
C
Metabolic rate l '
Ij
(W.kg- 1)
:­
1.7
6.16
5.10
6.90
7.56
4.80
7.75
5.89
5.54
5.13
6.09
0.34
l'
ttl
o
><
Ij
>
Z
Ij
'--'
~
t:Il
'"d
rn
>
X
3:
>
Z
TABLE II
'TI
Foraging trip duration, bodv mass change, at-sea metabolic rate (MR) and diving behaviour of Antarctic fur seal females
Seal
Mass change
(kg)
Time at sea
(days)
At-sea MR
(W. kg")
Multiples
of predicted
BMR"
Number of dives
--------
Total
Per hour
Diving time (h)
----------
Total
% at sea
c::
Depth travelled (m)
- - - - - - -
Total
Per hour
~
[/J
tTl
;l>
r
'TI
I
2
3b
4
5
6
7
8
9
Mean
S.E.
0.5
1.0
4.0
4.0
0.0
0.5
1.5
1.5
-0.5
1.4
0.5
4.67
3.21
5.33
7.54
2.21
4.04
2.50
5.25
3.04
4.21
0.54
6.51
5.13
7.51
8.07
4.70
8.18
6.00
5.69
5.22
6.34
0.40
4.59
3.95
5.52
6.01
3.46
5.75
4.37
4.15
3.54
4.59
0.32
1351
922
1474
1923
1075
1038
877
1271
1070
1222
103
12.1
12.0
11.5
10.6
20.3
10.7
14.6
10.1
14.7
13.0
1.0
19.1
18.0
20.3
25.3
16.9
13.4
15.4
25.0
16.1
18.8
1.3
17.1
23.4
15.8
14.0
31.9
13.9
25.7
19.8
22.0
20.4
1.9
48508
37588
55860
72068
29072
23374
30044
76192
41912
46069
5916
433.1
488.2
436.4
398.2
548.5
241.0
500.7
604.7
574.1
469.4
34.5
0
~
;l>
8
Z
Q
tTl
Z
tTl
~
Q
tTl
>-J
..,
o
[/J
aBMR = 3.39· AfJ·75 W, where M is body mass in kg (Kleiber, 1975); bseal number 434 of Costa et al.'s (1989) study
.....,
.....,
v.
J. P. Y. ARNaULD, 1. L. BOYD AND J. R. SPEAKMAN
776
:l
(a)
•
:=
4
.
•
•
I
I
I
I
0
2
3
4
•
•
•
•
I
J
5
6
7
8
Time at sea (days)
~
'1
Cl
9
(b)
~
~
~
8
,
7
.2
g 6
Q)
E
C1l
"• ....... .
-,
"0
.0
5
~
-
-------­
Q)
en
~
4
20
15
10
25
•
35
30
40
Proportion of time at sea spent diving (%)
9
(c)
•
8
• •
•
7
6
5
4
200
250
300
350
400
450
•
• •• •
500
550
600
650
Rate of diving (m.h-1)
FIG. 2. The relationships between at-sea metabolic rate and (a) time spent at sea, (b) proportion of time at sea spent
diving (with fitted sigmoid curve, see text for equation) and (c) the rate of diving (m . h -1) in lactating Antarctic fur seal
females.
FUR SEAL FORAGING ENERGETICS
5
'Ci
5
(a)
•
4
~
c:
'(0
•
3
(J)
(J)
«l
(b)
~
c:
•
•
4
'(0
OJ
777
3
OJ
2
•
E
>,
-c
0
co
0
• ••
•
~ 2
•
• ..•
E
>,
-c
o
co
-----~-----------------
- 1 -1,--------,------,--,-----,---,---,-------,-----,
I
I
I
I
I
I
7
2 3 4 5 6
1
_0
1
o
j
--~--------------------
o
40
80
120
i
,
160
200
240
Energy expenditure at sea (MJ)
Time at sea (days)
FIG. 3. The relationship between body mass gain and (a) time spent at sea and (b1the total energy expenditure while at
sea in lactating Antarctic fur seal females,
The amount of mass gained while at sea (1.39 ± 0.51 kg) was positively correlated to the
duration of the foraging trip (1'2 = 0.58, P < 0.02, Fig. 3a). Body mass gain was also positively
related (r2 = 0.72, P < 0.004) to the total amount of energy expended while at sea (89.7 ± 17.6
MJ, Fig. 3b). In order to compare foraging efficiency between individual seals, therefore, a mass
gain efficiency index (g. Mr 1) was calculated by dividing the total mass gained during a foraging
trip with the total amount of energy expended during the trip. This index varied substantially
between individuals (12.1 ±4.5g.Mr 1, CV = 110%) but was not related to body mass
(P> 0.5) or the amount of time spent at sea (P> 0.4), the latter indicating that there is no
apparent advantage for females in following any particular pattern of foraging trip duration.
Discussion
Sources of error
When using TDRs to study the diving behaviour of marine vertebrates, selecting an appro­
priate sampling frequency can have important effects on the results, Boyd (1993) showed, in one
Antarctic fur seal, that the proportion of actual dives recorded decreased in a sigmoid fashion
with increasing sampling interval. In comparison to a 5-s sampling interval, sampling of every
lOs underestimated the total number of dives by 14% and overestimated dive duration by 16%
(Boyd, 1993). In the present study, to be certain that there would be sufficient TDR memory to
collect diving behaviour data for the entire foraging trip, a sampling interval of 10 s was used. It is
possible, therefore, that the total number of dives recorded for each individual in the present
study is an underestimate. However, as this error would apply to all individuals, it should not
affect the shape of the observed relationships between diving behaviour and energy expenditure,
only their elevations.
The attachment of instruments (radio transmitters, time-depth recorders, etc.) to the body
surface of marine animals increases drag while swimming and, hence, potentially also the total
778
J. P. Y. ARNaULD,!. L. BOYD AND J. R. SPEAKMAN
energy that must be expended during travelling and foraging (Feldkamp, 1987). Several studies
have shown that devices representing 2-8% of the body cross-sectional surface area can increase
foraging trip durations in free-ranging animals (Wilson, Grant & Duffy, 1986; B. G. Walker &
P. L. Boveng, pers. comm.). However, in the present study, the attached devices represented only
< 1% of the body cross-sectional surface area of Antarctic fur seal females. Using similar devices,
Boyd et at. (1991) found no difference in foraging trip duration between instrumented and non­
instrumented animals. Furthermore, Costa & Gentry (1986), also using similar-sized devices,
found no difference in metabolic rate between northern fur seals (Callorhinus ursinusi that were
carrying instruments and those that were not. None the less, it is expected that the devices used in
the present study would have had some minor cumulative effect and, while possibly not
influencing metabolic rate, may have increased the total amount of energy expended during
the foraging trip by increasing the time spent at sea (B. G. Walker & P. L. Boveng, pers. comm.).
The use of the DL W method for measuring energy expenditure is widespread and the errors
involved in this technique have been discussed in great detail by several authors (Lifson &
McClintock, 1966; Nagy, 1980; Schoeller et al., 1986; Speakman, 1993: Speakman et al., 1993).
Most studies validating the technique have been conducted on small animals «5 kg) and have
found that DLW estimates of mean energy expenditure were within ± 5% of that measured by
direct calorimetry or respirometry. Costa (1987) measured the energy expenditure of a single
subadult male northern fur seal by both DLWand material balance methods and found a
difference of only 3.3% between the results of each method. Similarly, Boyd et at. (1995b)
recently found no significant difference between DLW and respirometry estimates of energy
expenditure in six captive, exercising California sea lions of similar size to the animals in the
present study. However, Boyd et at. (1995b) found considerable individual variation in the
difference between the two methods and cautioned that DLW may in some circumstances
overestimate energy expenditure in pinnipeds. None the less, if DLW overestimated the
metabolic rates of Antarctic fur seals in the present study, the shape of the observed relationships
between energy expenditure and diving behaviour would not be altered unless the overestimation
was also a function of behaviour.
Comparison with previous studies
Mean foraging trip duration was similar to that previously reported for Antarctic fur seals in
years of normal food availability (Doidge, McCann & Croxall, 1986; Boyd et al., 1991). Likewise.
diving behaviour (number of dives, proportion of time spent diving, metres dived, and rate of
diving) was similar to that previously reported for the species (Croxall et al., 1985; Boyd et al.,
1991).
At-sea MR (6.34 W· kg-I) was 4.6 times the predicted basal metabolic rate (BMR; estimated
from Kleiber, 1975). This is considerably lower (by 35%) than the 9.8W.kg- 1 (6.7 times
predicted BMR) observed in the same species by Costa et at. (1989). Some of this discrepancy
may be accounted for by the fact that Costa et at. (1989) used the Lifson & McClintock (1966)
equations (modified by Nagy, 1980) for calculating CO 2 production, which Boyd et al. (1995b)
found to overestimate by 7% the result obtained by using the equation employed in the present
study. Indeed, recalculation of the CO 2 production of the animals in the present study using the
Lifson & McClintock (1966) equation gave results 9-13% greater than those obtained by using
the Speakman et at. (1933) equation. Most measurements obtained by using the Speakman et al.
(1993) equation were, however, within the considerable range reported by Costa et at. (1989). It is
FUR SEAL FORAGING ENERGETICS
779
possible that the large range observed by Costa et al. (1989) may, as was found in the present
study, have been attributable to differences in behaviour.
In their study of the energetics of exercising California sea lions, Boyd et al. (1995b) were
unable to raise metabolic rate to levels greater than six times predicted BMR for substantial
bouts of swimming. They suggested, therefore, that previous DLW measurements of average field
metabolic rates as high as 6.7 and 8.8 times predicted BMR in otariids (Costa et al., 1989, 1991)
were overestimates. The current estimates support this view. Moreover, using the relationship
between heart rate and oxygen consumption, Butler et al. (1995) recently measured a mean at-sea
metabolic rate in free-living lactating Antarctic fur seals of7.2 ± 0.3 W· kg- 1 (5.2 times predicted
BMR), a value similar to that found in the present study.
Foraging behaviour, energy expenditure, and mass gain efficiency
The negative relationships observed between the proportion of time spent diving (%), the rate
of diving (m- h -1) and at-sea MR were unexpected and might appear to be counter-intuitive. We
had expected a priori that diving would be the most energetically expensive activity during
foraging, thus resulting in positive relationships between diving behaviour and at-sea MR.
Likewise, making similar assumptions, Boyd et al. (1991) observed a negative relationship
between dive rate (m- h- 1) and foraging trip duration and suggested that females undertaking
short trips would therefore have a higher rate of energy expenditure.
These interpretations of the energetic cost of diving behaviour were based, however, on the
assumption that time spent at the surface is mostly spent resting. Consequently. animals with a
higher dive rate would spend less time resting and, therefore, have a higher rate of energy
expenditure (Boyd et al., 1991). However, recent analyses of Antarctic fur seal swimming speeds
(Boyd, 1996; Boyd, Reid & Bevan, 1995a) indicate that the majority oftime at the surface is spent
swimming between food patches. Butler et al. (1995) found that the metabolic rate during diving
in Antarctic fur seals is only 20% greater than that when swimming, the greatest elevation in MR
occurring after a bout of diving when the animal is at the surface. Hence, it may be that animals
with a higher dive rate spend a greater proportion of their time at the surface resting so that their
overall at-sea MR is lower than that of animals with a lower dive rate. Analysis of how females
allocate the time at the surface to swimming and resting in relation to diving behaviour over the
entire foraging trip is needed to clarify this question.
The close sigmoidal relationship observed between the proportion of time at sea spent diving
and metabolic rate may provide a useful, inexpensive means of estimating foraging energy
expenditure in this species, and possibly in other otariids. Boyd et al. (1994), however, observed
that in years of low prey availability both the average proportion of time spent diving and the
average rate of diving increase. It seems unlikely that, as one would predict from the negative
relationships between diving activity and metabolic rate observed in the present study, animals
expend less energy in search of food at times when it is more difficult to find. Therefore,
extrapolation of this relationship to estimate energy expenditure under different conditions
should be made with caution.
Females that undertake short foraging trips spend a greater proportion of the time at sea
diving and have a higher dive rate (Boyd et al., 1991; this study). The results of this study indicate
that they not only have low rates of energy expenditure but gain less mass during the foraging
trip. In contrast, animals staying at sea longer not only have higher metabolic rates, and spend
780
J. P. Y. ARNaULD, 1. L. BOYD AND J. R. SPEAKMAN
greater total amounts of energy, but gain more mass per trip while spending a lower proportion
of time diving. This suggests that, while animals making long trips may have to spend more time
and expend more energy in search of food patches, they are better at exploiting the patches, or the
patches are of higher quality than those encountered by females making short trips.
All the nutrition delivered to pups during attendance periods comprises milk carried ashore
and milk produced from body reserves while on land (Arnould & Boyd, 1995). Hence, the
amount of mass gained during a foraging trip should provide an index of the amount of milk to
be delivered to the pup. The findings of the present study, that mass gain is positively related to
foraging trip duration, therefore accords with previous observations that the amount of milk
females deliver to their pups during attendance periods is positively related to the duration of the
preceding foraging trip (Arnould & Boyd, 1995; Arnould, Boyd & Socha, In press).
Whereas the amount of milk delivered per attendance period is positively related to the
duration of the preceding foraging trip, Arnould & Boyd (1995) have shown that the overall rate
of milk delivery is independent of trip duration. Consequently, as indicated by the lack of
relationship (in years of normal food abundance) between maternal foraging trip duration and
pup growth rates (Boyd et al., 1991; Lunn, 1993), within the range of durations observed there
is no advantage to pups in mothers undertaking foraging trips of any particular duration
(Arnould & Boyd, 1995). In the present study, there was no relationship between the efficiency
with which females gained mass and the duration of foraging trips; thus, within the range of
durations observed, there is no apparent energetic advantage to females in following any
particular foraging trip duration strategy. It must be stressed, however, that these observations
were made in a year of normal food abundance and it is possible that particular foraging trip
duration strategies may confer energetic advantages in years of exceptionally low or high food
availability. This may explain how a range of individual foraging strategies can be maintained in
the population.
In summary, the results of the present study indicate that at-sea metabolic rate in Antarctic fur
seal females is negatively related to the proportion of time spent diving and the rate of diving
(m- h- 1) . Consequently, as diving intensity is negatively related to foraging trip duration (Boyd
et al., 1991), at-sea metabolic rate is positively related to time spent at sea. Animals that stay
longer at sea spend greater amounts of energy but also gain more mass, so that the efficiency with
which mass is gained is not related to foraging trip duration.
We thank K. Reid for assistance in the field and P. Thomson for conducting the 180xygen analyses. J. P.
Croxall kindly provided constructive comments on an earlier version of this paper.
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