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First published online March 14, 2008
Journal of Experimental Biology 211, 1093-1101 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.010728
The effect of food temperature on postprandial metabolism in albatrosses
1 School of Biological Sciences, Institute for Conservation Biology, University
of Wollongong, Wollongong, NSW 2522, Australia
2 Department of Biological Sciences, University of California Riverside,
Riverside, CA 92521, USA
* Author for correspondence (e-mail: hb01{at}uow.edu.au)
Accepted 27 November 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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20% of body mass, SDA was 4.22±0.37% of assimilated food energy,
and potentially contributed 17.9±1.0% and 13.2±2.2% of the
required heating energy of food at 0°C for Diomedea and
Thalassarche albatrosses, respectively, and proportionately greater
quantities at higher food temperatures. Cold food increased the rate at which
postprandial metabolic rate increased to 3.2–4.5 times that associated
with food ingested at body temperature. We also found that albatrosses
generated heat in excess by more than 50% of the estimated thermostatic
heating demand of cold food, a probable consequence of time delays in
physiological responses to afferent signals.
Key words: specific dynamic action, postprandial metabolic rate, albatrosses, cold, food, thermoregulation
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Because food
is patchily distributed in space and time in the marine environment,
albatrosses must fly long distances to satisfy their energy needs. When food
is encountered, it is often aggressively contested by other individuals,
resulting in gorge feeding of substantial amounts of food in 3–4 min
(H.B., M.A.C. and W.A.B., unpublished observations).
In the southern hemisphere, some albatross species forage as far south as
the polar pack ice (Weimerskirch et al.,
1993), where sea surface temperature (SST) can be below 0°C
(National Oceanographic Data Centre 2005). Their diets comprise predominantly
marine ectotherms, mainly cephalopods and fish
(Warham, 1990;
Cherel and Klages, 1998),
which are ingested at ambient SST. Meal masses taken by free-flying
albatrosses often exceed 20% of body mass (Mb)
(Imber and Russ, 1975;
Berutti and Harcus, 1978;
Clarke et al., 1981;
Cooper et al., 1992). As
albatrosses are homeothermic endotherms with core temperatures of
40°C (Warham, 1971),
most of their food is sufficiently cold to produce thermoregulatory costs,
which reduce the net energy obtained from a given amount of food.
When an endotherm ingests a cold (lower than core temperature) meal, a rise
in postprandial metabolic rate (PPMR) will result from warming the cold meal
(Wilson and Culik, 1999), from physical activities associated with feeding,
and from postfeeding processes termed (alternatively) specific dynamic action
(SDA), heat increment of feeding or dietary-induced thermogenesis. SDA (used
here) has been studied in a wide array of endothermic vertebrates, including
fish (Fitzgibbon et al.,
2007), and results in part from the transport of food through the
alimentary tract (Masman et al.,
1989), but most (>90%) is associated with postdigestive
stimulation of cellular protein synthesis
(Ricklefs, 1974;
Jobling, 1983;
Blaxter, 1989;
Brown and Cameron, 1991a;
Brown and Cameron, 1991b).
Because the metabolic heat produced by SDA is known to substitute for
thermogenesis in birds exposed to sub-thermoneutral temperatures
(Biebach, 1984;
Baudinette et al., 1986;
Chappell et al., 1997;
Masman et al., 1989;
Kaseloo and Lovvorn, 2003;
Bech and Præsteng, 2004),
we considered that SDA-related heat production could also contribute to
warming the cold meals from which it was derived.
If SDA is to make a substantial contribution to the cost of warming cold food, the heat generated by SDA must be concurrent with the warming of a meal, which presumably begins immediately after ingestion. This requires food to be quickly processed and for digestion products to be delivered to protein-synthesising tissue within a very short time. To determine SDA and food-temperature effects on metabolic rate (MR) in albatrosses, we measured postprandial MR (PPMR) for meals isothermal to body core temperature (Tb; i.e. with no warming costs). We estimated the relative contributions of SDA and thermogenesis to warming cold meals by predicting the time course of meal warming from a mathematical model, and by measuring PPMR of albatrosses fed cold (0°C and 20°C) meals.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). All of the
Diomedea were recaptured banded adults of breeding age and all
Thalassarche were at least 5 years old, as indicated by their adult
plumage and primary moult patterns
(Brooke, 1981). The Indian
yellow-nosed albatross is the smallest of the albatross species and the
Gibson's and wandering among the largest. For this study we used one D.
exulans, seven D. gibsoni and seven T. carteri. Body
mass (fasted) of individuals, was measured with a Pesola spring balance to the
nearest 50 g as 2158±113 g (mean ± s.e.m.), range
1850–2300 g, for the yellow-nosed albatross and 6288±237 g, range
5450–7500 g, for the Diomedea species. D. gibsoni and
D. exulans are closely related species with virtually identical life
histories and for this study were treated as one species
(Warham, 1990). Birds were transferred to the University of Wollongong and held in an air-conditioned facility for up to 4 days; they were returned to sea following PPMR measurements. All aspects of care and handling of birds conformed to the Australian code of practice for the care and use of animals for scientific purposes (Australian National Health and Medical Research Foundation 1999–2004) and had gained approval from the University of Wollongong Animal Ethics Committee (permit no. AE04/11).
Metabolic rate measurements
To identify thermoneutral temperature ranges for Diomedea
albatrosses, we continuously measured the metabolic rate of six D.
gibsoni in a positive pressure open-system respirometer while lowering
the chamber temperature from an initial 18°C to 3°C in 1°C steps
over a period of 8 h. Five birds showed no MR response to the temperature
changes, and one bird increased MR by 40% when the chamber temperature
fell to 6°C. From these results we assumed that chamber temperatures of
14°C that we intended to use for a range of metabolic rate studies
were albatross thermoneutral. As our intention was to simply identify a
thermoneutral temperature range for other measurements, we did not extend this
study.
We used two negative pressure open-system respirometers as described by
Hill (Hill, 1972) to determine
rates of oxygen consumption. Measurements were carried out at chamber
temperatures of 14±1°C (thermoneutral for albatrosses) and air-flow
rates of 20–30 standard litres per minute (s.l.p.m.). Flow rates were
monitored by either a Hastings HFM201 100 s.l.p.m. mass flowmeter or a Singer
DTM115 slide valve flowmeter modified to give a flow-related pulsed voltage
output. At these temperatures we anticipated that albatrosses confined in
chambers might suffer thermal stress if unable to readily dispose of
postprandial heat output. Accordingly, the chambers were large enough to
permit birds to assume resting postures and were provided with cool
(13–14°C) fresh running water to allow metabolic heat dissipation
via their immersed feet. This feature also eliminated soiling of
plumage by faeces, which were released in copious amounts after a meal.
Of the 15 birds used in the study, six were measured at three meal temperatures and the remainder at two, as detailed in Table 1. PPMR measurements were recorded at meal temperatures (Tf) of 0°C, 20°C or 40°C. Repeated measurements on individuals were made on successive days and birds were fasted overnight before each measurement session. All measurements were made in daylight hours, corresponding to the active phase of the albatross circadian cycle.
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To determine resting metabolic rate (RMR) and assess handling effects, we
placed birds in chambers 1–2 h prior to feeding. At the end of this
period birds were removed from the chambers, force fed meals of 20% of
body weight of chopped cuttlefish (Sepia apama Gray) and returned to
the chambers, a process requiring usually less than 2 min. Feeding was simply
a matter of holding the bill and gape open, covering the glottis and dropping
in the cuttlefish pieces, which, being well mixed with mucus, slipped readily
into the proventriculus. Birds were then returned to the chambers and
metabolic rates were measured until PPMR returned to RMR levels, a period of
10–12 h. Food was weighed with an Ohaus model E1F110 balance (Nanikon,
Switzerland) to the nearest 0.1 g.
Excurrent air samples, scrubbed of moisture and CO2, were drawn
through either an Applied Electrochemistry S3A (Pittsburgh, PA, USA) or a
Sable Systems FC1 oxygen analyser (Las Vegas, NV, USA) at a rate of 200
ml min–1. Oxygen analysers were referenced to ambient air for
4 min in each 30 min period, using a Sable Systems Mutliplexer V2.0, to
account for baseline drift. Chamber temperatures and oxygen readings were
sampled at 2 s intervals using a DataTaker DT500 data logger (Melbourne,
Victoria, Australia). Warthog LabHelper software
(www.warthog.ucr.edu)
on a Macintosh computer acquired data and controlled gas-sample switching.
Determination of SDA and the thermoregulatory component of postprandial metabolism
We define PPMR simply as the MR after a meal is consumed and this will be
elevated above RMR by SDA and food heating costs. As we need to refer
specifically to the elevation in PPMR following a meal we define elevated PPMR
(PPMRe) as:
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Because food that is isothermal to a bird's core temperature does not
directly perturb its thermal homeostasis, we assumed that SDA would be the
only cause of elevation of PPMR following ingestion of food heated to core
temperature (Tf=40°C) in quiescent birds. PPMR has the
potential to include an activity component, but by using quiescent birds and
adjusting the data for any observed activity (as described below), we assumed
that we had eliminated this factor. We accordingly determined SDA as the
integrated difference between PPMR and RMR over the period of postfeeding MR
elevation. That is:
 | (1) |
 | (2) |
Not all birds tolerated a long session enclosed in a chamber, as indicated by restlessness and elevated MR. Intolerant birds were removed from chambers once restlessness was observed and data from these sessions were not used. All other birds used were generally quiescent, but exhibited infrequent short bursts of activity associated with posture changes, scratching, etc., with corresponding increases in MR. The data acquired within these periods of activity were amended by interpolating between average MR values that occurred before and after a given activity period.
PPMR rise time
As the respirometer chambers were opened for a short period to remove and
feed the birds, the chamber steady-state gas mixture was replaced to a large
extent by ambient air. After the birds were replaced and the chambers sealed,
the observed rates of rise in PPMR (see
Fig. 2) were therefore less
than actual rates due to dilution of the chamber gas mixture. To correct for
this effect, we used nitrogen to determine respirometer chamber dynamic volume
and to derive the chamber time constant (
c) over the range of
flow rates used for this study. The chamber response function was of the form
A(t)=Aexp(–t/c), where
t is elapsed time and A is the initial nitrogen fraction of
the chamber gas. We estimated the value of c (in min) from:
 | (3) |
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Measurement of physical properties of S. apama
For this study we required values for specific heat, density and thermal
conductance of S. apama tissue, and for measurements of these
properties we used tissue samples from coarsely minced and homogenised whole
animals. Single samples only from each of 10 animals were used for
measurements of density and specific heat, and from seven animals for thermal
conductance.
Specific heat of wet tissue samples, weighed to the nearest 10 mg, was
determined by cooling samples of 200 g to 0°C and measuring the
temperature change when these were added to water at 27°C in a
Gallenkamp CBA-301 adiabatic calorimeter (Loughborough, UK). Calibrated
standard thermometers accurate to 0.005°C were used for all temperature
measurements.
Specific heat of cuttlefish (Cv) was then determined
from:
 | (4) |
T
is the observed temperature change in calorimeter water content and
Mc is cuttlefish mass. We used 4.15 J g–1
as the value for Ch.
Volumes of cuttlefish samples (200 g) were determined using water
displacement at 20°C and density (
) was then estimated from:
 | (5) |
To determine thermal conductivity (Kt) we placed cuttlefish tissue columns of 5 cm length and 1 cm2 square cross-sectional area within a polyurethane foam shell with 3 cm deep walls. Bead thermistors were inserted into and along the axis of the tissue columns at 1 cm intervals. These were pre-calibrated against a standard mercury thermometer and capable of measuring temperature with an accuracy of <0.1°C. One end of the column was clamped to 0°C and 1 W of power applied to the other using a 1 cm2 square resistive grid. Current and voltage values, 1 A at 1 V, applied to this grid were regulated to within 0.1% of nominal values. The measurement configuration is shown (not to scale) in Fig. 1.
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Following application of power, temperature rise along the column was
sampled at 1 min intervals using a Sable Systems Universal Interface and Sable
Datacan application software resident on an IBM-C PC. Thermal conductivity of
the cuttlefish tissue was determined from the mean of the temperature drop
(T in °K) over the second 1 cm length of the column after
steady-state conditions were observed to exist using (for unit cross-section
and length):
 | (6) |
Differences between temperature drops over the second and third 1 cm lengths of the column were used to estimate loss of heat through the boundaries of the column. This was <1% and was ignored.
A Mettler PM400 electronic balance (Toledo, OH, USA) was used for all mass measurements.
Data analysis
We used Warthog Lab Analyst software
(www.warthog.ucr.edu)
to calculate and evaluate oxygen consumption
(
O2, in ml
min–1) and used:
 | (7) |
).
Microsoft Excel and WinSTAT were used for data analysis, descriptive
statistics and ANOVA. All percentage data were arcsine square-root transformed
to satisfy the requirements of parametric analyses
(Zar, 1998). Unless stated
otherwise, all values are presented as means ± 1 s.e.m. Measurements at
either two or three food temperatures were made on all birds used in this
study, necessitating repeated measures ANOVA testing of some results.
Thermal modelling of an ingested meal
A cold meal ingested by an albatross is under pressure laterally from
elastic proventricular walls and vertically from meal weight. As a
consequence, the food tends to form a bolus, which can be readily determined
by palpation of the proventriculus. The bolus can be approximated in shape by
a sphere. If the body core is assumed to be adiabatic and maintained at
40°C, and if the food bolus is assumed to be isotropic and radially
isothermal, then the transfer of heat from body core to the meal can be
approximated by a simplified form of the general heat equation. The form and
general solution of this equation for the time averaged temperature rise of
the bolus is derived below. We used Eqn
11 to predict the average temperature rise over time of an
ingested cold meal, subject to the above assumptions.
The time rate of change of temperature distribution in a three-dimensional
body [
(r,t)] given by the general heat equation (see
Carslaw and Jaeger, 1959;
Churchill, 1963) is:
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is the Laplacian operator, and thermal
diffusivity 
is:
 | (8) |
and Cv are thermal
conductivity, density and specific heat, respectively.
Expressed in spherical coordinates, where the sphere is isotropic and
radially isothermal, it can be reduced to:
 |
 |
r, for a sphere of radius
Rf, this reduces to:
 | (9) |
(r,t) of:
 |
 | (10) |
>, which is most relevant, is given by:
 | (11) |
is given by:
 | (12) |
 | (13) |
Eqn 11 is the general
solution for the time-averaged temperature rise in a spherical meal bolus and
has the form of a rapidly converging series of inverted decaying exponential
terms. Four terms are adequate and it is readily determined that (i) the
effects of higher order terms (N>1) have effectively ended after
2 and (ii) the meal average temperature will have attained 86.5% of its
final value after 2, and effectively 100% of its final value after
4.
Solutions for Eqns 8,
11,
12 and
13 use the values of the
physical properties of S. apama tissue that we measured as described
previously in this section. Meal bolus radius was found from meal mass using
Eqn 13. By applying this model
to each meal mass fed to a given albatross, we could predict the amount of
heat energy required to raise a meal to Tb. By measuring
O2 over the
4 period after feeding we could then determine the amount of heat energy
delivered from SDA following this meal. From concurrent studies (H.B., M.A.C.
and W.A.B., unpublished data) we found S. apama to have a high
protein content (Table 2), and
for oxygen consumption we used a thermal equivalence of 20.1 kJ
ml–1 O2, which corresponds to a respiratory
quotient (RQ) of 0.85 for a protein substrate.
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We estimated the energy cost of heating a cold meal
(Hm) from:
 | (14) |
T=Tb–Tf. Among other environmental factors, model precision is dependent on the shape of the food bolus. Any variation from truly spherical will reduce food warming rate, and predictions are therefore essentially first-order approximations.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Saiwarun et al., 2001). Also
listed in Table 2 are values
for energy density and protein content, determined from concurrent studies
(H.B., M.A.C. and W.A.B., unpublished data).
Rates of change and rise times of PPMR
Air exchange during the period that metabolic chambers were open to feed
the birds meant that we had to estimate (as explained in Materials and
methods, above) rather than measure the true metabolic responses after the
chambers were closed. However, it is clear that the initial rate of increase
in PPMR was much greater when albatrosses were fed cold compared with
isothermal meals. PPMR increased linearly towards a maximum value
(PPMRmax) at a rate of 0.75±0.08 W kg–1
min–1 in Diomedea albatrosses fed meals at 0°C
and 0.86±0.20 W kg–1 min–1 for meals
at 20°C. In contrast, PPMR of albatrosses fed similar-sized meals at
40°C increased at a rate of only 0.17±0.03 W kg–1
min–1. Mean initial rates of change of PPMR
(dMR/dt0) were 4.4–5 times greater at meal
temperatures of 0°C and 20°C than at 40°C
(Table 3), and PPMR rise times,
the time between attaining 10% and 90% of PPMRmax, were
18–24% of the 40°C value. These differences are readily apparent
when comparing PPMR profiles measured at meal temperatures of 0°C and
40°C in Fig. 2, for an
individual D. gibsoni.
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After meals at 0°C and 20°C the PPMR responses of Thalassarche albatrosses, while of lower peak values, were similar to those of the larger Diomedea, rising relatively quickly and linearly (Table 3) to PPMRmax. Mean dMR/dt0 values were 3.2 times greater and rise times were 23–24.5% of those measured for meal temperatures of 40°C. These cold meal rise times were not significantly different between the genera (t=2.36, P>0.1) or between meal temperatures of 0°C and 20°C (t=0.72, P>0.4).
PPMR and SDA
Observed PPMR increased to levels exceeding RMR within 10 min after animals
were fed cold meals and in excess of 20 min for meals at 40°C. PPMR
typically attained a peak (PPMRmax) within several hours and then
gradually returned to RMR over a period of 10–12 h
(Fig. 2). Mean
PPMRe, integrated over the period of elevation and expressed as a
percentage of energy assimilated (AEn), is given in
Table 4 for the three meal
temperatures used in this study, and individual values are displayed in
Fig. 3. Based on meals of
S. apama, these values represent 4.22±0.37% of AEn,
or 5.07±0.45% of gross energy intake (GEI).
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As we measured PPMR of albatross individuals at either two or three meal temperatures, we performed repeated measures ANOVAs for mass-specific PPMRe values at the meal temperatures used. PPMRe differed significantly between all meal temperatures examined (30.35>F>115.4, 0.002>P>0.0002), but there were no significant differences in PPMRe between individuals ingesting food at a given food temperature (0.65<F<6.06, 0.64>P>0.08).
Between genera there were found no significant differences in mass-specific PPMRe at each of the meal temperatures (0.40<F<0.47, 0.79<P<0.82).
Metabolic response to feeding and its contribution to meal warming
The metabolic heat production associated with SDA over 4 for the
various sized meals fed to Diomedea and Thalassarche
albatrosses is contrasted in Fig.
4 with the predicted energy needed to warm 0°C meals to
Tb (based on Eqn
12). The difference between these two values represents the amount
of thermoregulatory energy that individual albatrosses must generate to warm
these meals.
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, was 17.9±1.0%
(N=4) for Diomedea and 13.2±2.2% (N=5) for
Thalassarche albatrosses. For Tf=20°C, where
food heating requirements are 50% of the Tf=0°C
values, we estimated the maximum contribution from SDA to be 40.2±4.2%
(N=2) for Diomedea and 25.7±2.0% (N=6) for
Thalassarche albatrosses. These results are summarised in
Table 5.
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The meal sizes (20% of Mb) fed to
Diomedea and Thalassarche, 1090±55 g and
412±18 g, respectively, were significantly different
(P
Metabolic overcompensation in response to a cold meal
In all cases where Tf<Tb, we
found that the total thermoregulatory energy expended during the period of
PPMR elevation was significantly greater than the amount required to heat a
cold meal to Tb levels
(Fig. 5; P<0.001 at
0°C and 20°C). This was determined by first subtracting SDA heat
production (estimated using the values in
Table 4) from the total
thermogenesis associated with PPMR (using Eqn
2) and comparing this difference to the energy needed to warm a
given mass of food at a particular temperature at feeding to
Tb. The extent of this metabolic overcompensation was
63.5±12.4% (N=11) at Tf=0°C and
51.0±11.5% (N=7) at Tf=20°C, but these
values are not significantly different (t=1.75, P>0.23).
We found no significant differences between genera (P>0.22).
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We checked for correlations between meal temperatures and activity levels for all measurement sessions. All birds were generally quiescent throughout all sessions and any activity that occurred was very brief, sporadic and unrelated to meal temperature.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Signals from these sensors in albatrosses can therefore be
expected to initiate thermoregulatory responses to cold meals well before the
start of digestion and the onset of SDA-related thermogenesis.
In every case where albatrosses were fed a cold meal, total postprandial
heat production exceeded the amount required to raise Tf
to Tb, as predicted from
Eqn 1. Similar excess
thermogenesis has been reported in humans after cold drinks
(Boschmann et al., 2003) and
Pekin ducks when core temperature was reduced by thermodes implanted in the
hypothalamus (Simon-Oppermann et al.,
1978). This MR overcompensation is apparently associated with
delays in physiological responses to afferent signals, as demonstrated in
pigeons Columba livia by Østnes and Bech
(Østnes and Bech,
1998).
To prevent their legs from freezing when exposed to sub-zero temperatures
for extended periods, pigeons regularly flush their legs and feet with pulses
of warm blood. This process, `cold induced vasodilation', injects
corresponding pulses of cold blood into the body core. Each cold pulse
triggers an immediate rise in MR, which persists for some time after core
temperature has been restored to Tb, thus delivering more
heat than required (Johansen and Millard,
1974; Murrish and Guard,
1974; Østnes and Bech,
1998) and offering an explanation for the observed
overcompensation.
In this study, as birds were quiescent in the respirometer chambers, activity costs did not contribute to PPMR. Cold meal PPMR therefore had three major components: the thermoregulatory demand of heating cold food, SDA and thermogenic overcompensation.
For any organism an upper limit can be expected in the rate of increase in
MR following a thermoregulatory challenge. In the pigeon, the maximum MR value
was measured as 1.05 W kg–1 min–1
(Østnes and Bech,
1998). From the pooled 0°C and 20°C
dMR/dt0 values given in
Table 3, we found the
equivalent values for Diomedea and Thalassarche albatrosses
(dMR/dt0) to be 0.78±0.52 and 0.32±0.03 W
kg–1 min–1, respectively.
It is apparent that thermal signals propagate rapidly through the blood
stream (Østnes and Bech,
1998). A body core cooling event is therefore expected to generate
a cold front that will propagate throughout the body, rapidly triggering a
chain of responses from cold sensors located throughout the vascular system
and other sites within the body core (Lin
and Simon, 1982; Fruhstorfer
and Lindblom, 1983; Simone and
Kajander, 1997; Simon,
2000). Conceivably, such a large ensemble of coincident afferent
signals will strongly stimulate a marked and rapid thermoregulatory response
to counter a drop in core temperature, resulting in the rapid rise in PPMR
observed in albatrosses fed cold meals.
Regardless of the physical and neurological bases, the thermoregulatory overcompensation represents an additional cost to processing a cold meal, and consequently reduces the net energy available from a given meal.
SDA measurement
The amount of SDA is known to vary as a function of food type
(Blaxter, 1989) and diet energy
density (Costa and Kooyman,
1984; Rosen and Trites,
1997), with protein diets producing the greatest effect. Results
of SDA measurements in adult birds fed protein meals are listed in
Table 6. Kestrels and tawny
owls were fed whole mice (Masman et al.,
1989; Bech and Præsteng,
2004), and their SDA values would include an activity component
associated with food fragmentation, whereas pre-chopped albatross meals were
placed directly into the oesophagus. Furthermore, because food temperature was
not reported by Masman et al. (Masman et
al., 1989), the SDA value they report may include a
thermoregulatory component.
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Costa and Williams (Costa and Williams,
2000) reviewed SDA studies of adult marine mammals. They reported
SDA values ranging from 4.7 to 16.8% of GEI, with the majority of values above
10% GEI. Although we could not verify that any of these studies corrected for
food temperature effects, it appears that the PPMRe values we found
for albatrosses fed cold meals were comparable to the `SDA' values reported
for these marine mammals.
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Comparison of model predictions with in vivo measurements
Weimerskirch and Wilson (Weimerskirch
and Wilson, 1992) implanted breeding wandering albatrosses at the
Crozet Islands with stomach temperature loggers to identify feeding patterns
during their 6–18 day foraging flights over the Southern Ocean. The
Crozet Islands lie at 46°25'S, 51°40'E, below the
subtropical front (STF) where SST ranges between 6 and 8°C
(Smith et al., 2005).
Wandering albatrosses from these islands regularly forage north of the STF
(Weimerskirch et al., 1993),
and recordings from one bird's 6 day trip suggest that this albatross fed
below the STF at the extremes of its journey, but moved north of the STF where
SST is 12°C (Smith et al.,
2005) at other times. Stomach temperature dropped rapidly after
ingestion of cold food and returned to 38–39°C over a consistent
time course (Fig. 6). After a
particularly large meal, ingested some 60 h into the trip, stomach temperature
restoration time was about 4 h (=4), and attained 90% of its final value
after 2 h (=2), suggesting that stomach thermodynamics predicted by our
model are comparable with those of free-living albatrosses.
Ecological significance
Albatrosses can be considered energetically frugal animals. Field metabolic
rates of foraging/brooding albatrosses with chicks were found to be <2.4
basal metabolic rate (BMR) (Adams et al.,
1986; Bevan et al.,
1995; Arnould et al.,
1996). Their reproductive costs are reduced by raising a single
chick over 7–8 month periods in the smaller species and 12 months in the
Diomedea (Tickell,
1968; Tickell and Pinder,
1975; Thomas et al.,
1983; Warham and Sagar,
1998); natal philopatry and lifelong pair bonding minimise many
costs associated with breeding. Moult and breeding are mutually exclusive and
body moult proceeds very slowly, taking 3–6 years to complete
(Tickell, 1968;
Brooke, 1981;
Prince et al., 1993); and
transport costs are typically very low, permitting long-distance foraging at
sites very remote from breeding locations
(Pennycuick, 1983;
Pennycuick, 1987;
Weimerskirch et al., 1984;
Weimerskirch et al., 2000;
Cooper, 1988;
Costa and Prince, 1987;
Croxall and Prince, 1990). In
such a regime, subtle energy gains may result in marginal increases in adult
or juvenile survival or in breeding success parameters to which albatross
populations have been shown to be very sensitive
(Croxall et al., 1990;
Robertson, 1991). Accordingly,
food temperature may influence the manner in which resources are partitioned
between age groups, sexes and species of albatrosses. For example, satellite
tracking of wandering albatrosses breeding on the Crozet Islands showed that
breeding males generally forage at higher latitudes than females and juvenile
birds (Weimerskirch et al.,
1993; Weimerskirch et al.,
2000).
Male wandering albatrosses are significantly larger (20–27%) than
females and juveniles and contribute more resources than females to chick
rearing (Tickell, 1968;
Weimerskirch et al., 2000;
Shaffer et al., 2001).
Conceivably, males will take larger meals than females and the greater thermal
time constant of the meal boluses will result in lower heating rates and
longer digestion times, and extend the time available for SDA heat to
contribute to meal warming. This is apparent from the significant difference
(P<0.001) between the possible contributions of SDA to meal
warming in Diomedea and Thalassarche albatrosses. Lower
convection heat losses from the larger body diameters of males can be expected
(Buttemer et al., 1986) and
overall males will have thermoregulatory advantages over females and
juveniles, making foraging in colder regions more energetically affordable.
Conversely, smaller females and juveniles may be restricted to foraging at
lower latitudes where the higher SST would lower the energy cost of warming
food and would be accompanied by a greater relative contribution of
SDA-derived thermogenesis for food warming. Sexual segregation of foraging
sites is found in other albatross species, with females consistently foraging
at lower latitudes. This has been documented in wandering and grey-headed
albatrosses (Thalassarche chrysostoma) breeding on Marion Island,
grey-headed and black-browed (T. melanophrys) albatrosses at South
Georgia and Buller's albatrosses (T. bulleri) on islands south of New
Zealand (Nel et al., 2000;
Nel et al., 2002;
Phillips et al., 2004;
Stahl and Sagar, 2000a;
Stahl and Sagar, 2000b).
In conclusion, because Diomedea and Thalassarche
albatrosses forage in southern latitudes where SST is generally at or below
20°C, meals can be expected to provoke a rapid postprandial rise in MR in
defence of core temperature. Meal-generated postprandial heat production will
consist of three components; the energy demand of warming food, thermogenic
overcompensation and SDA. Due to the rapidity of the thermogenic response to
cold meals and the significantly lower rate of rise of SDA, SDA will make only
a minor contribution to the energy demand of warming cold meals, but this
contribution will increase proportionately with increasing food temperature.
Studies of some species have found that SDA, which is an unregulated heat
source, can be used to offset thermoregulatory costs in endotherms
(Costa and Kooyman, 1984;
Jensen et al., 1999).
Albatross feeding is usually associated with a considerable amount of activity
including flight, swimming, and contesting and mechanically processing forage.
Thus thermoregulatory costs associated with maintaining body temperature and
food warming may be further offset by metabolic heat associated with these
activities.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) is compared with estimated total
meal heating cost (
).
measured expense, 
estimated expense). The differences are attributable to an inherent delay in
lowering MR after thermal equilibration of body and meal temperatures has
occurred.