The comparative energetics and growth strategies of sympatric Antarctic and subantarctic fur seal pups at Îles Crozet
1 Department of Zoology, University of Melbourne, VIC 3010,
Australia
2 Centre d'Etudes Biologiques de Chizé, Centre National de la
Recherche Scientifique, 79360 Villiers en Bois, France
3 Department of Biology, Memorial University of Newfoundland, St. John's,
Newfoundland, Canada, A1B 3X9
4 Department of Ecology and Evolutionary Biology, University of California,
Santa Cruz, CA 95060, USA
5 School of Biological Sciences, Macquarie University, Sydney, NSW 2109,
Australia
* Author for correspondence (e-mail: j.arnould{at}zoology.unimelb.edu.au)
Accepted 2 September 2003
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Summary |
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Key words: maternal provisioning, metabolic rate, growth strategy, resource partitioning, energetics, weaning, fur seal, Arctocephalus gazella, Arctocephalus tropicalis
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Introduction |
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Otariid seals (fur seals and sea lions) are an ideal group for
investigating this topic, as females give birth to a single offspring, there
is no post-weaning maternal care, and offspring are entirely dependent on milk
for nutrition throughout most of lactation
(Bonner, 1984). Furthermore,
lactation in these species is characterised by mothers alternating between
short nursing periods ashore and long foraging trips to sea during which their
pup must fast (Gentry and Kooyman,
1986
). Consequently, the nutritional resources delivered to the
dependent pups must be allocated for growth, storage and behavioural
development (e.g. learning to swim) during fasting periods as well as when the
mother is ashore.
Lactation in otariid seals generally lasts 10-12 months, although in some
species offspring may be suckled for up to 3 years
(Bonner, 1984). Exceptions to
this pattern are the Antarctic fur seal (Arctocephalus gazella) and
the northern fur seal (Callorhinus ursinus), which have lactation
periods lasting only 4 months. The brevity of lactation in these two species
is thought to have evolved to exploit the predictably high but brief
productivity of the subpolar summer and to maximise maternal transfer and
offspring growth before the onset of the polar winter
(Gentry and Kooyman, 1986
). By
contrast, the longer lactation periods of the other otariid species are
thought to have evolved in response to the low seasonal variation but less
predictable nature of the temperate and sub-tropical marine environments they
inhabit. At three locations in the subantarctic region, however, there is the
surprising situation where species representative of each strategy breed
sympatrically. Macquarie Island, Marion Island and Iles Crozet are the
northern and southern extents, respectively, of the Antarctic fur seal and
subantarctic fur seal (Arctocephalus tropicalis) breeding ranges
(Guinet et al., 1994
;
Kerley, 1984
;
Robinson et al., 2002
). At
these sites, the majority of pupping for each species occurs in December but,
despite similarity in their maternal masses and pup birth masses
(Goldsworthy et al., 1997
;
Kerley, 1985
), Antarctic fur
seal pups wean at the end of the Austral summer (March-April) whereas
subantarctic fur seal pups wean in late winter (August-September). There are
few examples worldwide of such closely related sympatric species having such
divergent lactation strategies (Dempster
et al., 1992
; Innes and
Millar, 1994
).
Numerous studies have investigated the maternal characteristics (e.g. diet,
foraging behaviour, foraging areas, colony attendance patterns and milk
composition) and pup responses (e.g. growth rate and weaning mass) of
Antarctic and subantarctic fur seals at their sympatric sites in order to
understand the mechanisms driving the divergent strategies and their impacts
(Goldsworthy, 1999;
Goldsworthy and Crowley, 1999
;
Goldsworthy et al., 1997
;
Green et al., 1990
; Kerley,
1983
,
1984
,
1985
;
Klages and Bester, 1998
;
Robinson et al., 2002
). At
Macquarie Island and Marion Island, no differences have been found in maternal
diet, foraging areas or diving behaviour between the species during their
summer lactational overlap (Goldsworthy
and Crowley, 1999
; Goldsworthy
et al., 1997
; Klages and
Bester, 1998
; Robinson et al.,
2002
) yet, over the same time period, growth rates of Antarctic
fur seal pups are significantly greater than those of subantarctic fur seals
at all sympatric sites (Goldsworthy and
Crowley, 1999
; Kerley,
1985
; S. P. Luque et al., unpublished data). Goldsworthy and
Crowley (1999
) suggested that
the difference in growth rates could reflect either a higher milk consumption
rate in Antarctic fur seals or greater metabolic expenditure by subantarctic
fur seals. However, the limited information on pup metabolic rates for the
species is restricted to their allopatric sites (making comparisons difficult)
and there is no information on their milk consumption rates at sympatric sites
(Arnould et al., 1996a
,
2001
;
Beauplet et al., 2003
;
Georges et al., 2001
;
Guinet et al., 1999
).
Furthermore, while mass gain differs between the species, it is not known
whether the divergent lactation strategies influence the composition of growth
and development (Owens et al.,
1993
; Spray and Widdowson,
1950
).
The aims of this study, therefore, were to determine whether differences in body composition, metabolism and physiological development exist between sympatric Antarctic and subantarctic fur seal pups.
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Materials and methods |
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During the pupping period, 95 Antarctic and 58 subantarctic fur seal
newborn pups were sexed and identified by a unique numbered piece of plastic
tape glued to the fur on the top of the head
(Georges and Guinet, 2000a).
At about one month of age, each of these pups was tagged in the trailing-edge
of both fore-flippers with an individually numbered plastic tag (Dalton
Rototag, Nettlebed, UK). As part of concurrent studies, the attendance
patterns of mothers of marked pups were monitored from birth until the end of
March by visual inspection of the natal colony three times per day (09:00 h,
12:00 h and 17:00 h local time).
Sampling was conducted in February 2002 and was staggered by 10-15 days
between the species in order to cover similar pup ages. Mean ambient and sea
surface temperature during sampling were 8.0°C and 8.0°C, respectively
(http//ingrid.ldgo.columbia.edu/).
For all aspects of the study, selected pups were captured 1-3 days after the
mother's departure to sea following a normal suckling period in order to allow
sufficient time for complete voiding of ingested milk from the stomach
(Arnould et al., 1996a;
Donohue et al., 2002
;
Oftedal and Iverson, 1987
).
Each study pup was selected at random from the population of marked
individuals and sampled for only one aspect of the study. Upon each capture,
pups were weighed in a sack with an electronic suspension balance
(±0.01 kg). All the study pups still had the black natal pelage and,
based on close examination of the pelage, all individuals were considered to
be at the pre-moult stage.
Respirometry and resting metabolic rate
Oxygen consumption, determined by an open circuit respirometry system
(Butler and Woakes, 1982), was
used to measure the resting metabolic rates (RMR) of pups. Pups were placed in
a wooden respirometry chamber (80 cmx60 cmx50 cm; sealed with
silicone and varnish) that was equipped with a small Plexiglas window and
large fan that ensured complete and rapid mixing of air. Foam rubber seals
ensured an air-tight junction between the door and the body of the
respirometer. The chamber had a removable floor below which there was a basin
60 cm deep. The basin was filled with fresh water to within 10 cm of the rim
and covered by a sheet of wire grating when a pup was placed in it.
Air was drawn through the respirometer using an air pump (B105; Charles Austen Pumps, Byfleet, Surrey, UK), and flow rate (maintained at 50 l min-1) was measured using a rotameter (Fisher-Rosemount Ltd, Catham, Kent, UK). A subsample of the outlet air flow was passed through Drierite (CaSO4) and CO2 absorbent (Baralyme®) to an O2 analyser (S103; Qubit Systems Inc., Kingston, Ontario, Canada). Sampling of ambient air was conducted every 10 min by manually switching a valve in the chamber outlet airflow line. The O2 analyser was calibrated prior to each measurement period with atmospheric air and nitrogen (Air Products PLC, Crewe, Cheshire, UK). Ambient atmospheric pressure, temperature and humidity were measured on a digital barometer (Model BA116; Oregon Scientific Pty Ltd, Sydney, NSW, Australia) and recorded every 10 min. A humidity/temperature sensor was affixed inside the chamber.
The output signals from the O2 analyser and the humidity/temperature sensor passed through a purpose-built interface box that amplified the signals to a range of -10 V to +10 V and then transferred them to an analogue-digital converter unit (DAQPad-1200; National Instruments Corporation, Austin, TX, USA) in a desktop computer. The computer sampled the outputs 100 times per second, took a mean of these values and saved them to a file every 1 s with a program developed using a software package for automatic instrumentation (LabView® 4.0; National Instruments Corporation). Ambient atmospheric pressure, temperature and humidity readings were manually entered into the software package as they were recorded. Water temperature was measured with a glass thermometer (±0.1°C; Hanna Instruments Ltd Pty, Keysborough, VIC, Australia) prior to, and immediately after, the pup was in the basin. For logistical reasons, the body temperature of study pups was not recorded.
The pups were introduced into the chamber and left to rest and acclimatise for 1 h. Measurements of O2, humidity, temperature, pressure and flow were taken continuously throughout the duration of the experiment but for calculations of resting rates the values from the 10 min of minimum oxygen consumption after the hour of acclimatisation were used. Confirmation that the pup was resting but not sleeping was made by visual inspection through the Plexiglas window, which was usually kept covered. Once the measurements in air had been completed, the pup was placed in the water-filled basin and left to acclimatise for 1 h, and, thereafter, values from the 10 min of minimum oxygen consumption were used to calculate in-water standard rates. Due to equipment problems, in-air and in-water metabolic rates were not measured for all pups.
Oxygen consumption
(O2) was
calculated using the equation of Withers
(1977
):
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Body composition, daily energy expenditure and milk consumption
The body composition and daily energy expenditure (DEE) rates of pups were
measured using hydrogen isotope dilution and doubly labelled water (DLW)
techniques (Costa, 1987).
After weighing upon capture, a background blood sample (5 ml) was collected
into a heparinised syringe from each pup by venipuncture of an inter-digital
vein in a hind-flipper. They were then given an intramuscular injection of a
weighed dose (±0.01 g) of tritiated water (HTO;
1 ml, 7.4 mBq
ml-1). Each animal was also given an oral dose, by stomach tube, of
15-20 ml H218O 10% AP (Isotec Inc., Miamisburg, OH,
USA). Pups were then kept in an enclosure for 3 h before an equilibration
blood sample (5 ml) was collected, to determine the total body water (TBW)
pool size and initial plasma 18O levels, before being released at
the point of capture, left undisturbed and allowed to suckle normally during
the next visit ashore by their mother. Each pup was recaptured 2-3 days after
the departure of the mother on her subsequent foraging trip to sea (4-6 days
after initial capture), weighed and a final blood sample (5 ml) was
collected.
All blood samples were kept at 4°C for several hours before being
centrifuged (3000 r.p.m., for 10 min) and the plasma fraction separated.
Aliquot samples (2-5 ml) of plasma were stored frozen (-20°C) in plastic
screw-cap vials (with silicon O-rings; Sarstedt Inc., Newton, NC, USA) until
analysis. For tritium analysis, thawed sub-sample aliquots of plasma (0.2 ml)
were distilled into pre-weighed scintillation vials following the procedures
of Ortiz et al. (1978). The
vials were then re-weighed to obtain the mass of the sample water (±0.1
mg). Scintillant (10 ml Ultima Gold; Canberra Packard, Mt Waverly, VIC,
Australia) was added to the vials, which were then counted for 5 min in a
Packard Tri-Carb 2100TR liquid scintillation analyser (Canberra Packard) 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 to determine the specific activity of the tritium
injected. The 18O enrichment of plasma water was determined by
Metabolic Solutions (Nashua, NH, USA) using gas isotope ratio mass
spectrometry.
TBW was calculated from HTO dilution space using an equation determined
empirically in Antarctic fur seal pups
(Arnould et al., 1996b). Lean
body mass (LBM) was calculated from TBW assuming a hydration constant of 74.7%
(Arnould et al., 1996b
), and
total body lipid (TBL) was calculated by subtracting LBM from total body mass.
Total water influx (TWI) rates were calculated from the decrease in specific
activity of HTO and equations 5 and 6 in Nagy and Costa
(1980
), assuming an
exponentially changing TBW. Carbon dioxide production rates were calculated
using equation 3 of Nagy
(1980
). DEE was calculated
from CO2 production assuming a conversion factor of 27.44 kJ
l-1 CO2 (Costa,
1987
). Oxygen consumption was determined by dividing
CO2 production by the RQ (0.71; see above). Metabolic water
production (MWP) rates were calculated from the metabolic rate determined by
DLW assuming a conversion factor of 0.02629 g H2O kJ-1
(Schmidt-Nielsen, 1983
).
Milk consumption rates were calculated using the following equation
(Ortiz, 1987):
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Blood volume
The physiological ability of infant pinnipeds to make foraging dives has
been shown to increase throughout the period of maternal dependence
(Burns, 1999; Horning and
Trillmich,
1997a
,b
).
In the present study, therefore, factors affecting oxygen storage [haematocrit
(Hct), haemoglobin (Hb) and total blood volume] were measured and used as
indices of physiological development.
After weighing upon capture, a background blood sample (5 ml) was collected
into a heparinised syringe from each pup by venipuncture of an inter-digital
vein in a hind-flipper and stored cool (4°C) until all samples were
centrifuged (see below). Each pup was then given an intravenous injection
(1 ml) of a weighed dose of Evans Blue dye (0.5 mg kg-1 body
mass; Sigma-Aldrich, St Louis, MO, USA) to measure total blood volume
(El-Sayed et al., 1995
). After
completing the injection but before removing the needle from the blood vessel,
the syringe was flushed with blood 2-3 times to ensure that all dye was
administered. Serial blood samples (5 ml) were collected at 10 min, 20 min and
30 min post-injection to measure the equilibration and dilution of the dye
(El-Sayed et al., 1995
).
Prior to centrifugation, each background blood sample was thoroughly mixed by gentle agitation. An 20 µl sample was placed in 2.5 ml of Drabkins reagent (Sigma kit 525A; Sigma-Aldrich) and later assayed for Hb concentration by colorimetric analysis. Absorbance was measured in duplicate samples on a Spectronic 1001 (Milton Roy, Ivyland, PA, USA) spectrophotometer at a wavelength of 540 nm. Hb concentration of each sample was determined by comparison with a dilution curve created from protein standards. Hct was measured in triplicate from an aliquot of the whole blood as the packed red blood cell volume in capillary tubes following centrifugation for 5 min at 11 500 r.p.m.
Total blood volume was measured by colorimetric analysis of the Evans Blue
dilution. Following centrifugation at 3000 r.p.m. for 10 min, aliquots of
plasma were separated and stored frozen (-20°C) in plastic vials until
analysis several months later. In the laboratory, the thawed samples were
agitated and centrifuged again at 3000 r.p.m. for 5 min. The absorbance of the
decanted dyed plasma was determined on a Spectronic 1001 (Milton Roy)
spectrophotometer at 624 nm and 740 nm following procedures outlined in
Foldager and Blomqvist (1991).
Dye concentrations were determined from a serial dilution curve of Evans Blue
standards measured at both wavelengths. It is common practice to
back-calculate the dye concentration at the time of injection by determining
the intercept of a regression line between dye concentration of each serial
sample and the time it was collected
(Costa et al., 1998
;
El-Sayed et al., 1995
;
Foldager and Blomqvist, 1991
).
This method was not used because the regression between dye concentration and
time post-injection for most of the seals was not statistically significant
(P>0.05). Therefore, a mean dye concentration using all three
samples (i.e. 10 min, 20 min and 30 min post-injection) was calculated and
used for determination of blood volume. Plasma volume was calculated as
follows:
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Statistical analyses were performed using the Systat® statistical software (Version 7.0.1; SPSS Inc., Richmond, CA, USA). The Kolmogorov-Smirnov test was used to determine whether the data were normally distributed, and an F test was used to confirm homogeneity of variances (P>0.2 in all cases). Differences between linear regressions were tested by analysis of covariance (ANCOVA) after testing for homogeneity of slopes. Unless otherwise stated, data are presented as means ± 1 S.E.M. and results considered significant at the P<0.05 level.
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Results |
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Measurements of both in-air RMR and in-water SMR were made in 10 Antarctic and 13 subantarctic fur seal pups. Mean in-water SMR was significantly greater than in-air RMR for Antarctic fur seal pups (paired t-test, t9=2.59, P<0.03) but not for subantarctic fur seal pups (t12=0.82, P>0.4).
Body composition, daily energy expenditure and milk consumption
Body composition upon capture was determined for a total of 16 (eight male,
eight female) Antarctic and 14 subantarctic (seven male, seven females) fur
seal pups. No significant differences were detected between the sexes in
either species (P>0.2 in both cases) so the data were combined. As
expected, significant positive correlations were found between total body
water (TBW) and body mass in both species
(Fig. 2). However, the
regressions differed significantly between the species (ANCOVA,
F1,27=5.82, P<0.02), with Antarctic fur seal
pups having higher TBW per unit mass and, thus, relatively lower TBL stores
(22.2±1.0%) than subantarctic fur seal pups (26.1±1.0%;
t28=2.73, P<0.02;
Table 2).
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With the exception of one female Antarctic fur seal pup (18O levels were too close to background upon recapture), field metabolic rate measurements were obtained for all of the above individuals. There were no significant differences in CO2 production between the sexes for either species (P>0.1 in both cases) so data were combined. Antarctic fur seal pups had a significantly higher mean CO2 production rate (0.97±0.05 ml g-1 h-1) than subantarctic fur seal pups (0.81±0.05 ml g-1 h-1; t27=2.36, P<0.03). These values represent mean daily energy expenditure (DEE) and O2 consumption rates, respectively, of 638±33 kJ kg-1 day-1 and 1.36±0.07 ml g-1 h-1 for Antarctic fur seals and 533±33 kJ kg-1 day-1 and 1.14±0.07 ml g-1 h-1 for subantarctic fur seal pups (Table 2). The higher DEE of Antarctic fur seal pups resulted in them having significantly greater metabolic water production (MWP) rates (16.8±0.8 ml kg-1 day-1) than subantarctic fur seal pups (14.0±0.9 ml kg-1 day-1; t27=2.36, P<0.03). Mean milk water intake (MWI), however, did not differ significantly between the species (t27=1.66, P>0.1; Table 2). Consequently, as milk composition did not differ between the species (S. P. Luque, J. P. Y. Arnould and C. Guinet, unpublished data), there was no significant difference between the species in the amount of milk consumed per day by pups during the study period (t27=1.70, P>0.1; Table 2). The amount of milk consumed per maternal attendance bout also did not differ significantly between the species (t27=1.70, P>0.1).
Blood volume
Haematocrit (Hct) and haemoglobin (Hb) values were obtained for 10 (five
male, five female) Antarctic and eight subantarctic (five male, three female)
fur seal pups. There were no significant differences in either Hct or Hb
between the sexes for either species (P>0.1 in all cases) so data
were combined. Mean Hct did not differ significantly between Antarctic
(50.2±0.9%) and subantarctic (48.1±1.0%) fur seal pups
(t16=1.5, P>0.1). Similarly, there was no
significant difference in Hb content between Antarctic (14.5±0.3 g
dl-1) and subantarctic (14.6±0.4 g dl-1) fur seal
pups (t16=0.25, P>0.8).
Blood volume estimates were obtained for five Antarctic (two male, three female) and six subantarctic (four male, two female) fur seal pups. Blood volume as a proportion of body mass was significantly greater in Antarctic (11.5±0.8%) than subantarctic (8.9±0.5%) fur seal pups (t9=2.81, P<0.03). Assuming the same mean body composition for these pups as determined above, the difference in blood volume between the species was still significant when considered as a proportion of LBM (t9=2.35, P<0.05).
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Discussion |
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The in-water SMR of Antarctic fur seal pups was significantly greater than
their in-air RMR. Similar findings have been reported in comparable ambient
and water temperatures for similar-aged pre-moult northern fur seals
(Donohue et al., 2000). The
ratio of in-water SMR to in-air mass-specific RMR, however, was substantially
lower in Antarctic fur seals (1.3) than in northern fur seals (2.4), due
primarily to the greater in-water mass-specific SMR (37 ml O2
kg-1 min-1) yet similar RMR (15 ml O2
kg-1 min-1) of the latter species. Baker and Donohue
(2000
) found that premoult
northern fur seal pups spent little time in water, and Donohue et al.
(2000
,
2002
) suggested that this was
due to their inability to thermoregulate efficiently in water at that age. By
contrast, Antarctic fur seal pups in the present study spent considerable
amounts of time swimming in shallow water close to the shore (S. P. Luque, J.
P. Y. Arnould and C. Guinet, unpublished data), and similar-aged pups on South
Georgia have been recorded as spending up to 50% of their time in the water
(McCafferty et al., 1998
). It
is possible, therefore, that pre-moult Antarctic fur seals are better able to
thermoregulate in water than northern fur seal pups. Indeed, the higher body
lipid content (22%) of Antarctic fur seal pups in the present study compared
with that of northern fur seal pups (15%;
Donohue et al., 2000
) is
likely to provide them with greater subcutaneous thermal insulation.
Unexpectedly, in contrast to Antarctic fur seal pups, in-water SMR of
subantarctic fur seal pups was not significantly greater than their in-air
RMR. This could indicate that pre-moult subantarctic fur seal pups have better
thermoregulatory capabilities than Antarctic fur seal pups. If this was the
case, pre-moult subantarctic fur seal pups might be expected to spend
considerable amounts of time in water developing important swimming and diving
skills (Baker and Donohue,
2000; McCafferty et al.,
1998
). However, while the 4% greater body lipid content of
subantarctic fur seal pups might provide them with some advantage in thermal
insulation, they were rarely seen in water during the study (S. P. Luque, J.
P. Y. Arnould and C. Guinet, unpublished data, see below), suggesting that
they do not have exceptional thermoregulatory capabilities. An alternative
explanation is that pre-moult pups of this species have less developed
thermoregulatory ability than Antarctic fur seal pups, and immersion in water,
representing a severe thermal challenge they would not normally experience,
resulted in metabolic depression (Boily
and Lavigne, 1996
; Lee et al.,
1997
). Unfortunately, core body temperature could not be measured
in the present study, so this proposition cannot be investigated. Additional
studies determining the thermal conductance of subantarctic fur seal pups both
in water and in air are required to elucidate the reasons behind the
unexpected findings of their similar in-air RMR and in-water SMR.
A further surprising finding of the present study was that Antarctic fur
seal pups had a mean in-air mass-specific RMR 21% higher than that of
subantarctic fur seal pups. The higher TBL of subantarctic fur seals may have
provided them with some thermoregulatory advantage and, conversely, the
corresponding higher LBM of Antarctic fur seals would result in a greater
metabolically active mass and, thus, higher metabolic costs. On their own,
however, these factors are unlikely to account for the large differences in
RMR. One possibility is that the higher RMR of Antarctic fur seal pups is
related to their generally greater levels of activity (see below). Numerous
studies with humans and rats have shown that sustained increases in daily
activity levels result in the elevation of RMR
(Byrne and Wilmore, 2001;
Poehlman and Danforth, 1991
;
Tremblay et al., 1992
).
Concomitant with a higher mass-specific RMR, Antarctic fur seal pups also
had a daily energy expenditure 20% greater than that of subantarctic fur seal
pups. This is consistent with opportunistic observations at the study site of
subantarctic fur seal pups spending significantly less time in both
terrestrial and aquatic activities than Antarctic fur seal pups, preferring
instead to sleep (S. P. Luque, J. P. Y. Arnould and C. Guinet, unpublished
data). Indeed, the low DEE recorded for subantarctic fur seal pups at
Amsterdam Island (see below) has been attributed to their low activity levels
(Beauplet et al., 2003). The
ratio of DEE to in-air RMR was 1.3 for both species, which is less than the
ratio of 1.7 reported for premoult Antarctic fur seal pups at South Georgia
and northern fur seal pups (Arnould et al.,
2001
; Donohue et al.,
2002
). The DEE of Antarctic fur seal pups in the present study
(638 kJ kg-1 day-1) is less than the DEE reported for
free-ranging pre-moult northern fur seal pups (700 kJ kg-1
day-1; Donohue et al.,
2002
) and conspecific pups of similar age on South Georgia (1044
kg-1 day-1; calculated from MWP values in
Arnould et al., 2001
). These
differences may reflect the colder ambient and sea water temperatures during
summer at the Pribilof Islands (5°C and 4°C, respectively;
http://ingrid.ldeo.columbia.edu/SOURCES/.IGOSS/)
and South Georgia (4°C and 3°C, respectively; British Antarctic
Survey, unpublished data) in comparison with those during the present study
(8°C and 8°C, respectively;
http://ingrid.ldeo.columbia.edu/SOURCES/.IGOSS/),
leading to higher thermoregulatory costs. Similarly, the difference between
the DEEs of pre-moult subantarctic fur seal pups in the present study (533 kJ
kg-1 day-1) and on Amsterdam Island (416 kJ
kg-1 day-1; Beauplet
et al., 2003
) may reflect the substantially warmer summer climate
of the latter (17°C and 18°C for ambient and sea water temperatures,
respectively; Meteo France, unpublished data).
Errors in calculating DEE from CO2 production values can arise
if incorrect RQ values are assumed (Costa,
1988; Nagy, 1980
).
Indeed, differences in body composition may reflect differences in metabolic
fuel use (Beauplet et al.,
2003
; Blaxter,
1989
) such that differences in calculated DEE could be an artefact
of RQ assumptions. In the present study, however, if subantarctic fur seal
pups were catabolising proportionately more protein than were Antarctic fur
seal pups (as might be suggested by their body composition differences) then
the difference in DEE between the species would actually be greater.
Milk consumption and growth strategy
The lack of any significant difference in daily or per bout milk
consumption between Antarctic and subantarctic fur seal pups is consistent
with the similarity in foraging trip durations of their mothers (S. P. Luque,
J. P. Y. Arnould and C. Guinet, unpublished data). The mean daily milk energy
consumption by Antarctic fur seal pups in the present study (1.6 MJ
kg-1 day-1) is the same as that recorded for pre-moult
conspecific pups at South Georgia (1.6 MJ kg-1 day-1;
Arnould et al., 1996a) and
similar to that reported for pre-moult northern fur seal pups (1.4 MJ
kg-1 day-1; Donohue
et al., 2002
). By contrast, consumption by subantarctic fur seal
pups (1.2 MJ kg-1 day-1) is greater than reported for
similar-aged pre-moult pups of the Australian fur seal (A. pusillus
doriferus Jones; 0.8 MJ kg-1 day-1), a temperate
species with a comparable lactation length
(Arnould and Hindell, 2002
).
Unfortunately, milk consumption estimates are not available for other fur seal
species or for subantarctic fur seals at allopatric colonies, so it cannot be
ascertained whether pups of this nominally temperate species normally consume
such quantities of milk or if this only occurs at the subantarctic breeding
sites. Comparison of subantarctic fur seal pup growth rates during the first
four months at sympatric colonies (e.g. present study site, 70 g
day-1, S. P. Luque, J. P. Y. Arnould and C. Guinet, unpublished
data; Marion Island, 72 g day-1,
Kerley, 1985
) with those at
allopatric colonies further north (Gough Island, 58 g day-1,
Kirkman et al., 2002
;
Amsterdam Island, 54 g day-1,
Guinet and Georges, 2000
),
however, would tend to suggest a greater milk consumption by pups at the
subantarctic sites during this period.
As has been reported on Marion and Macquarie islands
(Goldsworthy and Crowley,
1999; Kerley,
1985
), Antarctic fur seal pup growth rates are significantly
greater than those of subantarctic fur seals at the present study site on
Possession Island (80 g day-1 and 70 g day-1,
respectively; S. P. Luque, J. P. Y. Arnould and C. Guinet, unpublished data).
This finding appears inconsistent with the observed parity in milk
consumption, especially in conjunction with the observed differences in the
rates of energy expenditure. Differences in body composition, however, could
account for this apparent contradiction. As adipose tissue is more energy
dense than lean mass, its deposition requires greater amounts of nutrition
(Blaxter, 1989
). This is
especially so in infant mammals, where the hydration of lean body mass is 3-4%
greater than in physiologically mature adults
(Adolph and Heggeness, 1971
;
Arnould et al., 1996b
;
Reilly and Fedak, 1990
).
Furthermore, if the observed body composition differences reflect differences
in metabolic substrate use, as has recently been shown for sex-based body
composition differences in subantarctic fur seals at Amsterdam Island
(Beauplet et al., 2003
),
preferential lipid catabolism could provide Antarctic fur seals with the
additional energy to account for their greater metabolic expenditure.
Consequently, it is feasible that equal milk energy consumption could produce
the differing growth rates.
A question that the findings of this study pose is why do Antarctic fur
seal pups not conserve energy and accumulate greater lipid reserves to sustain
them once they are weaned, especially as food availability may be reduced
during the colder winter months? Why do they have higher energy expenditure
rates than their sympatric congenerics? Pups of this species only have four
months in which to develop all the swimming and diving skills necessary to
forage independently (Bonner,
1984). While greater lipid reserves would provide some advantages
(e.g. thermal insulation, `nutritional buffer'), their benefit would be
limited if pups did not have any ability to dive and know how to hunt at
weaning. Hence, selection should favour the early acquisition of necessary
behavioural skills relative to species with longer maternal dependence.
Comparison of the diving behaviour of Antarctic and subantarctic fur seal pups
at Possession Island indicates that the former do indeed spend greater amounts
of time in water and learning to dive at an earlier age (S. P. Luque, J. P. Y.
Arnould and C. Guinet, unpublished data). Such increased activity would lead
to a higher energy expenditure (Baker and
Donohue, 2000
; Donohue,
1998
). Consistent with this earlier development of diving
behaviour in Antarctic fur seals is the finding of the present study that pups
of this species have greater mass-specific blood volumes than do subantarctic
fur seal pups. As Hb and Hct content did not vary between the species, the
larger blood volume translates into greater blood oxygen stores in Antarctic
fur seal pups (El-Sayed et al.,
1995
). Blood oxygen storage capacity in pinnipeds generally
increases with age until maturity (Costa
et al., 1998
; Horning and
Trillmich, 1997a
; Jorgensen et
al., 2001
). Consequently, the results of the present study suggest
that physiological development is faster in Antarctic than in subantarctic fur
seal pups.
The converse question posed by the findings of the present study is, as
pups of both species appear to receive similar amounts of nutrition during the
summer overlap in lactation, why do subantarctic fur seal pups not devote more
resources to faster behavioural and physiological development? The answer may
lie in the `anticipation' of a reduced rate of nutrient delivery during the
winter months. While there is no corresponding information available for the
present study site on Possession Island, average winter maternal foraging
trips of subantarctic fur seals at both Amsterdam Island and Marion Island are
the longest recorded for any otariid species (23-28 days;
Georges and Guinet, 2000b;
Kirkman et al., 2002
). The
fasting durations experienced in winter by pups at these sites, therefore, are
some of the most extreme for any infant mammal
(Guinet and Georges, 2000
).
Pups endure these fasts by greatly reducing activity, adopting protein
conserving pathways and relying mainly on lipid catabolism for metabolic
energy (Beauplet et al., 2003
).
Furthermore, initial body lipid stores and daily mass loss in these pups are,
respectively, positively and negatively related to the fasting durations
endured (G. Beauplet, unpublished data;
Guinet and Georges, 2000
).
Hence, a strategy of limiting energy expenditure and directing nutritional
resources to adipose tissue growth by subantarctic fur seal pups during the
summer months may be an adaptation for accumulating sufficient lipid reserves
to survive repeated extreme fasts later in lactation.
In summary, the results of the present study indicate that differences
exist in the resting metabolic rates, total energy expenditure and development
between Antarctic and subantarctic fur seal pups, two closely related
congeneric species (Wynen et al.,
2001), at a sympatric breeding site. These differences are
consistent with adaptations for rapid development of foraging abilities
necessary for the earlier nutritional independence in the former and extended
periods of fasting during prolonged maternal dependence in the latter. The
mechanisms controlling the physiological differences observed between the two
species are unknown but are likely to involve thyroid hormones, which are
known to play an important role in regulating metabolism and development in
neonatal mammals (Bernal and Refetoff,
1977
). While thyroid hormones have been shown to vary throughout
development, lactation and between seasons in phocid seals
(Haulena et al., 1998
;
John et al., 1987
;
Little, 1991
;
Litz et al., 2001
;
Ortiz et al., 2001
;
Woldstad and Jenssen, 1999
),
their dynamics in otariid seals remain to be investigated.
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Acknowledgments |
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References |
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