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First published online December 14, 2007
Journal of Experimental Biology 211, 49-57 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012229
Heat increment of feeding in double-crested cormorants (Phalacrocorax auritus) and its potential for thermal substitution
1 Institut Pluridisciplinaire Hubert Curien (IPHC), Département Ecologie,
Physiologie et Ethologie (DEPE), UMR 7178 CNRS-ULP, 23 Rue Becquerel, F-67087
Strasbourg Cedex 2, France
2 NRF Centre of Excellence at the Percy FitzPatrick Institute, University of
Cape Town, Rondebosch 7701, South Africa
3 Department of Zoology, University of British Columbia, 6270 University
Boulevard, Vancouver, British Columbia, V6T 1Z4, Canada
* Author for correspondence (e-mail: manfred.enstipp{at}c-strasbourg.fr)
Accepted 27 October 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2),
respiratory exchange ratio (RER), and stomach temperature, we studied the
magnitude and duration of HIF in seven double-crested cormorants
(Phalacrocorax auritus) following the voluntary ingestion of a single
herring (Clupea pallasi) while birds rested in air. Conducting trials
at thermoneutral (21.1±0.2°C) and sub-thermoneutral temperatures
(5.5±0.7°C), we investigated the potential of HIF for thermal
substitution. After the ingestion of a 100 g herring at thermoneutral
conditions,
O2was elevated
for an average of 328±28 min, during which time birds consumed
2697±294 ml O2 in excess of the resting rate. At
sub-thermoneutral conditions, duration (228±6 min) and magnitude
(1391±271 ml O2) of
O2elevation were
significantly reduced. This indicates that cormorants are able to use the heat
generated as by-product of digestion to substitute for regulatory
thermogenesis, if heat loss is sufficiently high. Altering meal size during
sub-thermoneutral trials, we also found that HIF in cormorants was
significantly greater after larger food intake. Based on these experimental
results, a simple calculation suggests that substitution from HIF might reduce
the daily thermoregulatory costs of double-crested cormorants wintering in
coastal British Columbia by 
38%. Magnitude of HIF and its potential for
thermal substitution should be integrated into bioenergetic models to avoid
overestimating energy expenditure in these top predators.
Key words: heat increment of feeding, thermal substitution, cormorant, thermoregulation, ecological energetics, respirometry, time–energy budget
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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),
which is specifically activated to maintain a stable body temperature during
periods of increased heat loss (Hohtola,
2002). Besides shivering, other thermogenic reactions occur in
birds and represent the obligatory component of thermogenesis. For example,
heat is produced during the processes associated with the digestion and
assimilation of food (heat increment of feeding, HIF) and during physical
activity (muscular work). These processes underlie behavioural control to some
extent and the heat produced could potentially be used to substitute for the
facultative component of thermogenesis, thereby reducing thermoregulatory
costs.
The heat increment of feeding (HIF), also referred to as specific dynamic
action (SDA), might be especially important in supplementing heat production
in resting endotherms exposed to sub-thermoneutral temperatures. In its
essence, HIF is the increase in resting metabolic rate observed after
ingestion of a meal, associated with heat production during the processes of
digestion, assimilation and nutrient interconversion
(Brody, 1945). Magnitude of HIF
depends on meal size (Janes and Chappell,
1995; Kaseloo and Lovvorn,
2003; Green et al.,
2006) and food composition
(Blaxter, 1989). For example,
because of differences in intermediary metabolism, high-protein foods tend to
provoke a greater HIF than foods containing mainly lipid or carbohydrate
(Blaxter, 1989). HIF has been
investigated across a wide range of animal species (for a review, see
McCue, 2006), although few
studies considered avian divers. Early studies, in which birds were force-fed,
produced conflicting results. Wilson and Culik found no evidence for HIF in
Adélie penguins Pygoscelis adeliae
(Wilson and Culik, 1991), and
suggested that the increase in energy expenditure observed following ingestion
was due to the physical costs of heating food to body temperature rather than
to HIF. By contrast, Janes and Chappell found HIF to be present in
Adélie penguin chicks, which accounted for 10% of the gross energy
(GE) intake (Janes and Chappell,
1995). More recent studies, in which birds ingested food
voluntarily while resting in air, confirmed the presence of HIF in
Brünnichs guillemots Uria lomvia
(Hawkins et al., 1997) and
little penguins Eudyptula minor
(Green et al., 2006). Further
confirmation is provided by studies of Kaseloo and Lovvorn, which most closely
replicated ecologically relevant conditions
(Kaseloo and Lovvorn, 2003;
Kaseloo and Lovvorn, 2005;
Kaseloo and Lovvorn, 2006).
They investigated HIF in mallard (Anas platyrhynchos) and lesser
scaup ducks (Aythya affinis) which dabbled and dived for their food,
respectively. Hence, just as for many other animal species, the presence of
HIF in aquatic birds has been clearly demonstrated. Despite this demonstration
and the recognition that HIF might account for a substantial portion of the
energy of the ingested food, its exact nature and functional significance are
still unclear (McCue, 2006).
The latter point is illustrated by the equivocal findings of studies
investigating the significance of HIF for thermoregulation. Results range from
none to partial and even complete use of heat generated by HIF or exercising
muscles for thermoregulation [see appendices 1 and 2 in Lovvorn
(Lovvorn, 2007)].
Cormorants are foot-propelled pursuit divers that forage predominantly on
fish (Johnsgard, 1993). They
are unique among aquatic birds in having a partially wettable plumage
(Grémillet et al.,
2005a), so that the thickness of their plumage air layer is
decreased. Consequently, their buoyancy is reduced and, therefore, the
mechanical work required to counter buoyancy during diving
(Lovvorn and Jones, 1991).
However, a partially wettable plumage will also increase heat loss in water,
especially during diving, and this effect will increase with dive depth. A wet
plumage will also lead to a greater heat loss when resting in air. It is
therefore no surprise that cormorants leave the water after a foraging bout
and vigorously shake off water from their plumage. Some cormorant species
inhabit thermally challenging environments. For example, a small population of
great cormorants Phalacrocorax carbo carbo winters in West Greenland
near the Artic Circle, encountering water temperatures below 0°C and air
temperatures as low as –30°C
(Grémillet et al.,
2005b). Heat loss under these circumstances might be extremely
high. This is illustrated by abdominal temperature decreases that have been
observed throughout dive bouts of great cormorants
[(Grémillet et al.,
2005b) average decrease 1.9°C]. Nevertheless, Greenland
cormorants continue to dive throughout the winter for up to several hours per
day (Grémillet et al.,
2005b). Consequently, thermoregulatory costs might account for a
substantial part of their overall daily energy budget, unless birds are able
to use heat produced through HIF or by exercising muscles (e.g. during flight
when leaving the foraging area) to substitute for shivering thermogenesis.
In the present study, we used double-crested cormorants (P. auritus), which are closely related and morphologically similar to great cormorants, to investigate the magnitude and time course of the heat increment of feeding following a standard meal (100 g herring, Clupea pallasi) at thermoneutral conditions. In a second set of trials, conducted at sub-thermoneutral temperatures, we tested the hypothesis that cormorants use the heat generated by HIF to substitute for shivering thermogenesis. Finally, we studied the effect of meal size on HIF.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). All experimental procedures were approved by the UBC
Animal Care Committee (Animal Care Certificates no. A02-0122 and A06-0421) and
were in compliance with the principles promulgated by the Canadian Council on
Animal Care.
Respirometry measurements
Rates of oxygen consumption
(O2) and carbon
dioxide production
(CO2) were
measured during trials using an open-circuit respirometry system (Sable
Systems, Henderson, NV, USA). A 55 l bucket (0.35 m diameterx0.65 m
high) with an airtight PlexiglasTM lid served as a respirometry chamber,
through which air was drawn via four small side holes near its
bottom. Air flow during the trials was maintained at 10–11 l
min–1 using a vacuum pump (Gast Manufacturing Inc., Benton
Harbour, MI, USA). The main airflow from the respiration chamber was dried
using silica gel before being led into a mass-flowmeter (Sierra Instruments
Inc., Monterey, CA, USA), which automatically corrected the measured flow to
STPD (273 K and 101.3 kPa). A sub-sample of 8 l
min–1 was bled into a manifold from which an oxygen
(paramagnetic O2-analyser PA-1B, Sable Systems; resolution:
0.0001%) and CO2 analyser (Beckman LB2 Medical
CO2-analyser, Schiller Park, IL, USA; resolution: 0.01%) sampled in
parallel. All connections between the various components of the respirometry
system were made with gas-impermeable TygonTM tubing.
Oxygen concentration inside the respiration chamber was above 20.5% and
CO2 concentration was below 0.4% during all trials. The gas
analysers were calibrated before each trial using 99.995% pure N2,
0.95% CO2 (PraxAir, Richmond, BC, Canada) and outside air (set to
20.95% O2 and 0.03% CO2). Analyser drift was minimal
but, if any occurred, it was corrected for during data analysis. Before a
trial the entire system was tested for leaks by infusing pure N2
gas. Time delay between air leaving the respiration chamber and arriving at
the gas-analysers was calculated by dividing the total volume of the tubing
and drying columns by the flow rate. The delay was found to be 13 s for both
analysers and was taken into account when calculating
O2 and
CO2 and relating
them to feeding events. The time constant of the respiration chamber was
calculated to be 5.5 min. Data from the flowmeter and the gas analysers were
fed into a universal interface (16 bits resolution, Sable Systems) and average
values were recorded every 5 s onto a desktop computer using Datacan (Sable
Systems).
Stomach temperature
In parallel with the respirometry measurements, temperature loggers
(MiniTemp-xl; length 70 mm, diameter 16 mm, mass 25 g, resolution 0.03 K;
earth&OCEAN Technologies, Kiel, Germany) were deployed in all birds to
monitor temperature inside the proventriculus (hereafter `stomach
temperature') during feeding trials as a proxy for body temperature.
Temperature loggers were programmed to record stomach temperature every 15 s
and were fed to the birds inside a refrigerated herring before the start of
experimentation. During HIF trials, temperature recordings enabled us to
determine the time required to warm the ingested cold fish to body
temperature. Furthermore, in separate trials five birds were fed various
amounts of herring and smelt (Osmerus mordax) (refrigerated at
5°C) when resting in their pen. The exact amounts (range:
19–118 g) and feeding times were noted to investigate the relationship
between the amount of fish ingested and the required heating time. Loggers
were equipped with a spring crown and were not regurgitated by the birds but
retrieved through stomach flushing at the end of experimentation, after about
10 days (for details, see Wilson and
Kierspel, 1998). Upon retrieval the data were downloaded to a
laptop computer.
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9°C, eqn 11.9
(Ellis and Gabrielsen, 2002)].
During these trials the respirometer was positioned outside (mean air
temperature: 6.6±0.4°C; range: 4.0–8.6°C) and birds were
fed a single herring of mass either 60 g or 100 g. (2) In Nov 2006, we
conducted feeding trials with five cormorants during which they were fed a
single 100 g herring. The respirometer during these trials was kept inside a
temperature-controlled room, with continuous ventilation from the outside.
Mean air temperature during these trials was 21.1±0.2°C (range:
20.0–22.6°C) and was well within the thermoneutral zone (TNZ) of
double-crested cormorants (Ellis and
Gabrielsen, 2002). Air temperatures in the respiration chamber
were monitored using a digital thermometer (Oregon Scientific, Portland, OR,
USA) and did not fluctuate by more than ±2°C during all trials.
All birds were fasted for 16 h (range: 13–29 h) before
experiments. At the beginning of a trial a bird was captured in its holding
pen, weighed and put into the respirometer. After the initial excitement,
birds settled quickly inside the darkened chamber and typically sat on a piece
of StyrofoamTM at the chamber bottom. When a stable level of
O2 and CO2 was reached and maintained for at least 10
min (usually after 1 h), the lid of the chamber was moved slightly to one
side and the bird was offered a single herring. In preliminary trials birds
would not ingest the offered fish voluntarily and were consequently force-fed.
Since this caused considerable disturbance to the birds, we discarded these
trials. Hence, only trials during which a bird readily took the herring
offered and ingested it voluntarily are reported here. Once the bird had
swallowed a fish, the lid was quickly closed again and the bird left
undisturbed for the remainder of the trial. The feeding procedure usually took
30 s. Fish offered during trials were refrigerated overnight to
temperatures naturally encountered by the birds during that time of year
(5°C). Herring were fed immediately after removal from the
refrigerator. A trial ended when the monitored O2 and
CO2 levels appeared to return to the resting level (i.e.
pre-feeding level). All trials were conducted during daylight hours and lasted
on average between 3.5 h (60 g herring) and 6.5 h (100 g herring).
Data analysis and statistics
Rates of oxygen consumption [using eqn 3b from Withers
(Withers, 1977)] and carbon
dioxide production were calculated in Datacan (Sable Systems) for each minute
of a trial. From this the respiratory exchange ratio was determined as
RER=CO2/O2.
Resting O2 was
established for each individual trial and served as a control measurement for
each HIF determination. It was calculated as the mean
O2 during a
stable 10 min period immediately preceding feeding. Following ingestion of a
herring, O2
increased to a peak value before declining linearly towards the resting value.
HIF was calculated as the elevation in oxygen consumption over the resting
rate during the course of digestion (see
Fig. 1). Note, however, that
HIF calculated in this way reflects the total amount of heat generated as a
by-product of digestion only, when the animal is at thermoneutral conditions
(see below). Ingestion was always accompanied by a brief spike in
O2
(Fig. 1), most likely caused by
movements associated with the feeding event. This initial spike was removed
(using linear interpolation) before calculating the magnitude of HIF
(indicated by the shaded area in Fig.
1A–C). In a few cases birds fed a 100 g herring did not
reach their resting
O2 by the end of
a feeding trial. Since
O2 declined in a
linear fashion after reaching a peak, we calculated a linear regression
between time and
O2 and
extrapolated this line to the resting value (see
Green et al., 2006).
Thermal substitution was investigated by comparing magnitude of HIF at
thermoneutral and sub-thermoneutral conditions. While at thermoneutral
conditions the calculated HIF reflects the total amount of heat generated as a
by-product of digestion, this is not necessarily the case at sub-thermoneutral
conditions (i.e. if thermal substitution occurs). When resting at
sub-thermoneutral conditions, the animal produces additional heat
(thermogenesis) to offset increased heat loss. If substitution of some or all
of the heat generated as a by-product of digestion for the thermogenesis
during rest occurs, HIF will appear to be of lower magnitude and/or duration
when compared with the thermoneutral condition. However, the total amount of
heat generated as by-product of digestion does not depend on ambient
temperature but on the size and constitution of the meal. We assumed that
substitution occurred if the calculated HIF was lower at sub-thermoneutral
conditions (Lovvorn,
2007).
Stomach temperatures were analysed using Multitrace (Jensen Software
Systems, Laboe, Germany). For each HIF determination, mean stomach temperature
was calculated over 5 min intervals throughout a trial. When a bird was fed a
cold fish, stomach temperature recorded by the logger declined precipitously.
After reaching a minimum value, temperature started to rise gradually towards
the pre-feeding value. The recorded stomach temperature should reflect body
temperature of a bird before feeding and again from 1 h after feeding,
when pre-feeding temperature was re-established. From changes in stomach
temperature (omitting the first hour after feeding) we calculated heat storage
throughout a trial as
TbMbc, where
Tb are the changes in body temperature (in °C),
Mb is body mass (in kg), and c is the mean
specific heat capacity of tissue [taken as 3.5 kJ kg–1
°C–1 (Dawson and
Whittow, 2000)]. To calculate the time required for birds to warm
up various amounts of ingested fish when resting in their pen, we first
selected feeding events from the stomach temperature traces where the
temperature returned to the pre-feeding value. This was not always the case,
especially after feedings in the late afternoon, when the temperature started
to decline towards the lower value maintained throughout the night (see
Enstipp et al., 2006a). For
each selected event we then calculated a baseline temperature before feeding,
taken as the mean temperature during 5 min immediately before feeding. In a
second step the time required to reach this pre-ingestion temperature was
measured.
All statistical analysis was performed using SigmaStat software (Jandel
Scientific, San Rafael, CA, USA). One-way analysis of variance (ANOVA) with
Tukey pairwise multiple comparisons was used to compare the effects of
environmental temperature and meal size on the magnitude and duration of HIF.
When single comparisons were made, as in comparing resting and peak values of
O2, Student's
t-test was used. All percentage values were normalised by arcsine
transformation beforehand. Significance was accepted at P<0.05.
Values given are grand means established from individual bird means and are
presented with standard error of the mean (± s.e.m.).
Calculation of thermoregulatory benefit
To explore the overall thermoregulatory benefit that double-crested
cormorants wintering in British Columbia potentially accrue from thermal
substitution via HIF, we estimated their maintenance costs, daily
energy expenditure (DEE), and daily food intake (DFI). Air temperatures
throughout coastal British Columbia during winter usually fluctuate between 0
and 10°C. Hence, we calculated maintenance costs of the cormorants (basal
metabolic rate and thermoregulatory costs) for an ambient temperature of
5°C (the mean temperature during our cold air trials) using values
from Table 1 and an energy
conversion factor of 19.7 kJ l–1 O2
(Enstipp et al., 2006a). DEE
was estimated from an algorithm established by Enstipp et al.
(Enstipp et al., 2006b),
modified for double-crested cormorants. This algorithm combines
time–activity data with activity-specific metabolic rates to estimate
DEE. We assumed the following time–activity budget (based on general
patterns observed in great cormorants): birds fly for 1 h, dive for 2 h (mean
dive depth and water temperature were taken as 10 m and 6°C,
respectively), and rest on land for the remainder of the day.
Activity-specific metabolic rates were taken from Enstipp et al.
(Enstipp et al., 2006a), with
the exception of flight costs, which were calculated using Pennycuick's
aerodynamic model (Pennycuick,
1989). Cormorants forage on a variety of fish species of different
nutritional composition and energy density. We assumed a composite energy
density for the ingested fish of 5 kJ g–1 wet mass, to
convert DEE into DFI. We furthermore assumed that birds acquire their DFI
during two foraging bouts, which are spread throughout the day, so as to make
best use of HIF for thermoregulatory savings. From HIFnet measured
in our cormorants digesting a 100 g herring
(Table 2) and the estimated
DFI, we calculated the daily HIFnet, assuming that the magnitude of
HIF changes in proportion with food intake
(Bech and Præsteng, 2004;
Green et al., 2006) and is
also comparable for fish species of varying energy density. The daily
HIFnet represents the maximum amount of energy savings possible
via HIF, if thermal substitution were complete.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2 of five
cormorants was 26.13±1.37 ml min–1
(Table 1). Immediately after
ingestion of a 100 g herring there was a brief spike in
O2
(Fig. 1A), most likely caused
by movements associated with the feeding event. However, within 20–25
min of feeding,
O2 regained a
stable, albeit elevated, level. This initial spike was removed and linear
interpolation was used when calculating the magnitude of HIF (shaded area in
Fig. 1A). After regaining a
stable level, O2
rose gradually (Fig. 1A,
Fig. 2) and reached a peak
value at 60 min, when it was significantly elevated over the resting rate
(P<0.001, t=–12.87). Thereafter,
O2 declined
steadily towards the resting level (Fig.
1A, Fig. 2). Oxygen
consumption was elevated for an average of 328±28 min after feeding,
during which time birds consumed 2697±294 ml O2 in excess of
the resting rate (Table 1).
Peak O2, taken
as the maximum value reached during a trial (excluding the initial spike), was
on average 1.7 times the resting rate
(Table 1).
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O2
was significantly elevated in cold temperature trials when compared with the
trials at thermoneutral conditions (P<0.001,
t=–6.00), confirming that birds were below their lower critical
temperature (Table 1,
Fig. 1A–C). After food
ingestion, O2
increased rapidly and within 30 min reached a more stable plateau (100 g
herring) or started to decline (60 g herring)
(Fig. 2). ANOVA comparisons
revealed that both ambient temperature and meal size significantly affected
the magnitude (P=0.001, F=16.74) and duration
(P<0.001, F=22.55) of HIF
(Table 1). At thermoneutral
conditions O2
elevation following the ingestion of a 100 g herring lasted significantly
longer (P=0.04, t=2.58) and was therefore significantly
greater (P=0.02, t=2.97) than when birds were at
sub-thermoneutral conditions (Table
1, Figs 1,
2). We only tested the effect
of meal size on HIF at low ambient temperatures. Under these conditions, HIF
was significantly greater (P=0.04, t=3.00) and lasted longer
(P<0.001, t=11.07) when meal size was bigger
(Table 1,
Fig. 1B,C,
Fig. 2).
Respiratory exchange ratio (RER)
The respiratory exchange ratio (RER) varied considerably throughout trials
of individual birds and also between birds. At thermoneutral conditions, mean
RER before feeding was 0.72±0.01
(Fig. 3). After food ingestion,
RER briefly increased to 0.74, before declining to a value below resting. For
the remainder of the trial, RER fluctuated between 0.68 and 0.70
(Fig. 3). Mean RER before
feeding at sub-thermoneutral conditions was 0.63±0.01. After ingestion
of a 100 g herring, RER increased briefly to 0.73. In the following 80 min it
varied between 0.68 and 0.73, before reaching a more stable level at 0.67 for
the remainder of the trial.
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35°C,
temperature rose again and reached the pre-ingestion level within 40–50
min after feeding. For the remainder of the trial temperature was relatively
stable, slowly declining to 40.7±0.3°C at the end of a 6.5 h trial
(Fig. 4). Mean stomach
temperatures during cold air trials, when birds ate a 100 g herring were
41.5±0.1°C before feeding and 41.7±0.2°C at trial end.
When fed 60 g herring in cold air, temperatures before feeding and at trial
end were 41.6±0.1°C and 40.7±0.2°C, respectively. Heat
storage, determined from changes in stomach temperature after food ingestion
(omitting the first hour after feeding) was negligible. Assuming that all body
tissues showed the same temperature variations as recorded by the
proventricular probe, mean heat storage was –2.8±0.9 kJ in warm
air trials, 2.0±1.4 kJ and –4.7±2.0 kJ in cold air trials
when fed 100 g and 60 g, respectively.
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5°C to body temperature
(P<0.001, F=90.57;
Fig. 5). As expected, the time
required to warm the ingested fish increased with meal size.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2
elevation were significantly reduced (by 48% and 30%, respectively),
when compared with trials at thermoneutral conditions
(Table 1). This strongly
suggests that cormorants are able to use the heat generated by HIF to
substitute for regulatory thermogenesis if heat loss is sufficiently high.
Knowledge of HIF and its overall effect on the energy budget of cormorants is
essential for the construction of bioenergetics models, in an attempt to
better understand the energy and food requirements of these top predators. If
thermal substitution (from HIF and muscular activity) is not taken into
consideration, time–energy budgets that include an independent value for
thermoregulation costs might greatly overestimate energy expenditure.
HIF at thermoneutral conditions
O2 of
double-crested cormorants when resting at air temperatures within their TNZ
was slightly lower than the mass-specific value reported in an earlier study
[12.56 vs 13.97 ml min–1 kg–1
(Enstipp et al., 2006a)].
Magnitude of the peak
O2 observed in
cormorants after ingestion of a 100 g herring (1.7 times resting,
Table 1) was similar to that
reported for other seabird species during digestion
(Baudinette et al., 1986;
Croll and McLaren, 1993;
Janes and Chappell, 1995;
Hawkins et al., 1997;
Green et al., 2006). It was
also similar to the increase observed in other fish eating endotherms, namely
pinnipeds [see table 3 in Rosen and Trites
(Rosen and Trites, 1997)]. The
time course of the changes in oxygen consumption following ingestion in the
cormorants was similar to that reported for little penguins
(Green et al., 2006) and
differed from that in Brünnichs guillemots
(Hawkins et al., 1997). In the
guillemots, oxygen consumption rate reached its peak within 7.5 min of fish
ingestion, which was followed by a relatively stable plateau phase for 50
min. Thereafter it declined slowly towards the pre-feeding value, which was
reached within 90 min of ingestion
(Hawkins et al., 1997). By
contrast, peak
O2 was distinct
and short-lived in the cormorants and oxygen consumption declined steeply
towards the pre-feeding value thereafter
(Fig. 1A,
Fig. 2). Cormorants reached
their peak O2
60 min after feeding (Fig.
2), which was in-between the 43 min and 73 min reported for little
penguins (Green et al., 2006)
and Adélie penguins (Janes and
Chappell, 1995), respectively.
O2 after
ingestion of a 100 g herring was elevated for 5.5 h in the cormorants
(Table 1,
Fig. 2). This is comparable to
the duration reported for little penguins
(Green et al., 2006), when
relative meal size is taken into consideration
(Table 2).
Warming the ingested food to body temperature might account for a
substantial part of the increase observed in
O2 after feeding
(Wilson and Culik, 1991). In
fact, Wilson and Culik attributed all of the increase observed in
O2 in
Adélie penguins after the ingestion of cold krill to this. However,
warming of the ingested food (Arctic cod Boreogadus saida for
Brünnichs guillemots and West Australian sardines Sardinops
neopilchardus for little penguins) accounted only for a minor fraction of
the observed increase in oxygen consumption of Brünnichs guillemots
(30%) (Hawkins et al.,
1997) and little penguins (17%)
(Green et al., 2006). In our
study it took birds on average 36 min to warm a 100 g herring from
5°C to body temperature when they rested within their TNZ
(Fig. 5).
O2 after fish
ingestion was elevated for a much longer duration (328±28 min), clearly
indicating that HIF persisted beyond the time required to heat the meal.
The costs of heating a herring from ambient to body temperature can be
calculated if we know the specific heat capacity of the herring. We used the
proximate composition of macronutrients for Pacific herring
(Zhao et al., 2006) (16.84%
lipid, 15.15% protein, 65.74% water, 2.16% ash) and the specific heat
capacities of these components (Kaseloo
and Lovvorn, 2003), to calculate the specific heat capacity of our
herring, estimated at 3.33 J g–1
°C–1. Hence, heating a 100 g herring from ambient
(5°C) to body temperature (41.2°C, mean stomach temperature of birds
before feeding) would require 12.05 kJ. We used an energy conversion factor of
19.08 kJ l–1 O2 (based on the proximate
composition of Pacific herring and the energy released from its components)
(Zhao et al., 2006;
Schmidt-Nielsen, 1997) to
convert the mean oxygen consumption after fish ingestion at thermoneutral
conditions attributable to HIF (26.7±3.0 ml O2
g–1 fish) to metabolic rate. The total HIF for a 100 g
herring was therefore calculated to be 50.9 kJ. Hence, fish warming in our
study accounted for only 23.7% of the measured increase in oxygen
consumption. If we use the energy density for Pacific herring given by Zhao et
al. [9.3 kJ g–1 wet mass
(Zhao et al., 2006)], a 100 g
herring would have a GE content of 930 kJ, and the 12.05 kJ warming costs
would represent 1.3% of that. Excluding the costs incurred when warming the
ingested food from ambient to body temperature, we arrive at a
HIFnet of 38.9 kJ for a 100 g herring
(Table 2).
Table 2 lists estimates of
the magnitude and duration of HIF for various bird species investigated at
thermoneutral conditions. Differences in experimental conditions (e.g.
relative meal size and composition) have to be considered when comparing these
values. The only studies to which our results can be directly compared are on
Brünnichs guillemots (Hawkins et al.,
1997) and little penguins
(Green et al., 2006). If we
take into account the relative meal size, then HIFnet observed in
cormorants was greater than in these two species
(Table 2). However, when
expressing HIFnet observed in cormorants on the basis of the GE
intake, it becomes clear that it falls into the lower range of what has been
observed in aquatic birds (4.2%; Table
2). While values for the guillemots and penguins are about double
the value observed in cormorants, the energy density of their ingested food
was considerably lower (Table
2). Low HIF values were also reported for harbour seals Phoca
vitulina when feeding on high-energy herring [5.1% of GE intake
(Markussen et al., 1994)].
Hence, it is intriguing that these relatively low HIF values (when expressed
as % GE intake) might be a consequence of the high energy density of the fish
ingested. Markussen et al. (Markussen et
al., 1994) took their results as evidence for a more efficient
utilization of the ingested meal, when seals fed on energy-rich food (i.e.
less `wasted energy' in the form of HIF).
Mean RER in our birds before feeding (0.72) was similar to the value of
0.73 reported in an earlier study (Enstipp
et al., 2006a) and identical to the value found in post-absorptive
European shags P. aristotelis resting in air
(Enstipp et al., 2005).
However, after food ingestion, RER in our cormorants declined somewhat (apart
from the brief initial increase) and fluctuated between 0.68 and 0.70
(Fig. 3). Although these values
are lower than what is conventionally expected, they follow the same pattern
observed in little penguins (Green et al.,
2006), digesting similar meal masses. When resting at
sub-thermoneutral conditions, RER before feeding was lower than expected at
0.63. After feeding, however, it increased to levels typical for diet
composition (for 80 min), before declining again to lower levels. RER
levels lower than conventionally expected have been reported throughout the
bird literature and some of the potential mechanisms (e.g. non-pulmonary
CO2 loss) and implications for studies on avian energetics have
been discussed (Walsberg and Wolf,
1995). However, more studies investigating these mechanisms,
especially for piscivorous species, are desirable.
Effect of meal size
We only investigated the effect of meal size when birds were at
sub-thermoneutral conditions. Nevertheless, under these conditions our results
show that duration of HIF and, therefore, its magnitude, changed significantly
with meal size (Table 1,
Fig 1B,C,
Fig 2). By contrast, peak
O2 during
digestion was not significantly affected by meal size, which was also true for
HIFnet, when expressed either on a mass-specific basis (per g fish)
or as percentage of the GE intake (0.14 kJ g–1 vs
0.12 kJ g–1 and 1.5% vs 1.3% for 100 g and 60 g
herring, respectively). These findings are similar to previous studies that
investigated the effect of meal size on HIF in birds and marine mammals
(Masman et al., 1989;
Markussen et al., 1994;
Janes and Chappell, 1995;
Chappell et al., 1997;
Rosen and Trites, 1997;
Bech and Præsteng, 2004;
Green et al., 2006). However,
in mallards, dabbling for grain, magnitude of HIF (% GE intake) increased with
increasing food intake (Kaseloo and
Lovvorn, 2003). Feeding conditions in the latter study differed,
however, in that mallards fed on low protein grain at intake levels below
maintenance requirements (for details, see
Kaseloo and Lovvorn,
2003).
HIF, thermal substitution and eco-physiological relevance
The significantly shorter duration of
O2 elevation and
its smaller magnitude at sub-thermoneutral conditions, when compared with
thermoneutral conditions (Table
1, Figs 1,
2), strongly suggest that
double-crested cormorants are able to use the excess heat to substitute for
regulatory thermogenesis under these conditions. HIFnet at the
lowest air temperature tested in our study (mean: 5.5°C) was reduced by
48%, indicating that thermal substitution at this temperature was only
partial. However, it is conceivable that thermal substitution might be
complete if heat loss is sufficiently high [e.g. at lower air temperatures or
during/after foraging in cold water (see
Kaseloo and Lovvorn, 2005)].
While the concept of using heat generated by HIF to offset thermoregulatory
costs has been around for more than 100 years, experimental evidence for it
has been equivocal. Results from studies in endotherms range from none to
partial and complete substitution [see
table 1 in Rosen and Trites
(Rosen and Trites, 2003) and
appendix 1 in Lovvorn (Lovvorn,
2007)]. For example, substitution from HIF accounted for >20%
of the metabolizable energy intake in lesser scaups diving for blue mussels at
a depth of 2 m (Kaseloo and Lovvorn,
2006). In kestrels Falco tinnunculus and tawny owls
Strix aluco, substitution from HIF was 50% and over 90%,
respectively, when birds rested at sub-thermoneutral ambient temperatures
(Masman et al., 1989;
Bech and Præsteng, 2004).
Similarly, substitution from HIF was clearly present in large house wren
chicks Troglodytes aedon and was complete in many cases, when ambient
temperature was sufficiently low (Chappell
et al., 1997). By contrast, in arctic tern chicks Sterna
paradisaea, no evidence for thermal substitution from HIF was found
(Klaassen et al., 1989) and
that was also the case for juvenile Steller sea lions Eumetopias
jubatus (Rosen and Trites,
2003). In mallards dabbling for low protein grain and in lesser
scaups diving for blue mussels to shallow depth (1.2 m), thermal substitution
from HIF was also negligible (Kaseloo and
Lovvorn, 2003; Kaseloo and
Lovvorn, 2006). These last two studies illustrate some of the
methodological problems when measuring thermal substitution (see
Lovvorn, 2007). For example,
the chances of detecting thermal substitution depend on the magnitude of HIF,
which in turn depends on meal size and protein content. Hence, thermal
substitution is more easily detected in animals eating large meals with high
protein content (Kaseloo and Lovvorn,
2003). This contrasts with conditions in the mallard study, where
birds ingested small amounts of low-protein grain. Also, in order for thermal
substitution to occur, heat loss has to be sufficiently high, while excess
heat (from HIF or exercising muscles) also has to be available to replace that
heat loss (Kaseloo and Lovvorn,
2005). Due to the greater compression of the plumage, heat loss in
lesser scaups must have been greater when diving to 2 m than when they dived
to shallow depth (1.2 m), so that thermal substitution was detectable in the
former situation but not in the latter
(Kaseloo and Lovvorn,
2006).
Potential reasons for varying results in studies that investigate thermal
substitution have recently been discussed
(Rosen and Trites, 2003;
Lovvorn, 2007). Besides
problems related to differences in calculation and experimental conditions,
one possible explanation could be real physiological differences between the
species studied with respect to taxonomy, ecology or developmental stage
(Rosen and Trites, 2003).
However, as pointed out by the authors, there appears to be no clear pattern
according to these criteria in the studies conducted so far. Clearly, more
studies on a greater range of species, conducted at the most relevant
ecological conditions, are needed before such a pattern might emerge.
The extra heat generated through HIF might serve cormorants at different
times of their daily routine by reducing the need for shivering thermogenesis.
For example, abdominal temperature decreases during diving have been observed
in various avian divers such as South Georgian shags P. georgianus
(Bevan et al., 1997), king
penguins Aptenodytes patagonicus
(Handrich et al., 1997) and
great cormorants (Grémillet et al.,
2005b). Heat produced during digestion might help to restore body
temperature after a dive bout. During times of inactivity at low ambient
temperatures (e.g. during roosting after foraging or during the night, when
locomotor activity is minimal), excess heat from HIF might be important to
maintain body temperature, thereby lowering the temperature for the onset of
residual thermogenesis. In sea otters Enhydra lutris, HIF might allow
animals to increase the time between activity bouts
(Costa and Kooyman, 1984).
These authors suggested that post-absorptive sea otters maintain their heat
balance through periodic activity bouts, while post-ingestive otters decrease
activity and use the heat produced from HIF to offset heat loss during rest. A
similar scenario was proposed for guillemots that spend most of their life at
sub-thermoneutral water temperatures
(Croll and McLaren, 1993). Of
course, to what extent muscular activity (for locomotion or shivering) can be
reduced because of the extra heat from HIF depends on the timing. Ideally,
bouts of activity and resting should be separated by the amount of time that
metabolism is elevated following food ingestion. While this seems to be the
case for sea otters (Costa and Kooyman,
1984), it is not clear if cormorants also structure their daily
activity patterns in such a way.
When exploring the overall thermoregulatory benefit that double-crested
cormorants wintering in British Columbia might accrue from thermal
substitution via HIF, we calculated maintenance costs and DEE to be
1009 kJ day–1 and 2000 kJ day–1,
respectively. This would require a DFI of 550 g of fish. When digesting a
100 g herring at thermoneutral conditions, HIFnet of the cormorants
was 38.9 kJ (Table 2). Hence,
550 g of fish, taken over two foraging bouts, would produce a daily
HIFnet of 214 kJ. In our herring trials at sub-thermoneutral
conditions (5°C), the measured
O2 elevation was
reduced by 48%, when compared with trials at thermoneutral conditions
(Table 1), representing thermal
substitution. If we extrapolate from these experimental trials to the
wintering scenario, this would amount to energy savings through HIF of
103 kJ per day. Such a saving represents 38% of the daily
thermoregulatory costs (calculated as the difference between RMR at 21.2 and
5.5°C, Table 1, 268 kJ
day–1) and 5% of the DEE. Hence, at the specific
conditions investigated, the extra heat generated via HIF would
reduce the need of cormorants to shiver by almost 40%. Thermoregulatory
savings via the excess heat from exercising muscles during activity
bouts are likely to reduce the need for shivering thermogenesis in cormorants
even further (Kaseloo and Lovvorn,
2006). However, one should be aware that the above calculations
are based on the combination of measurements under controlled laboratory
conditions and a simple model. Furthermore, thermal substitution patterns
might differ in birds resting in air or diving in cold water. Clearly, more
information is needed before the fraction of thermoregulatory costs that is
potentially met by substitution in free-ranging birds can be calculated with
greater accuracy.
Diving and HIF – evidence for delayed food-processing?
O2 has been
observed to increase within minutes of food ingestion in birds
(Janes and Chappell, 1995;
Hawkins et al., 1997;
Green et al., 2006) and this
was also the case in our study. However, such immediate onset of HIF would
seem to conflict with the need of avian divers to effectively manage their
finite oxygen stores during diving (Butler
and Jones, 1997). Any increase in metabolic rate during a dive
bout (i.e. HIF) would tend to reduce the aerobic dive capacity of these birds.
Apart from the studies by Kaseloo and Lovvorn
(Kaseloo and Lovvorn, 2003;
Kaseloo and Lovvorn, 2005;
Kaseloo and Lovvorn, 2006),
however, HIF measurements in avian divers were conducted while birds rested in
air. It is possible that birds foraging in the wild are able to delay the
onset of HIF to some degree. During diving, blood flow distribution changes as
part of the overall oxygen saving `dive response'
(Butler and Jones, 1997).
Hence, one possible mechanism to postpone digestion until after a dive bout
would be peripheral vasoconstriction of the gastrointestinal tract, which
seems to occur in shallow diving tufted ducks Aythya fuligula
(Butler et al., 1988;
Bevan and Butler, 1992).
Peripheral vasoconstriction has also been indicated during deep dives of South
Georgian shags [based on heart rate recordings
(Bevan et al., 1997)] and
emperor penguins Aptenodytes forsteri [based on temperature
recordings (Ponganis et al.,
2003)]. Furthermore, evidence for delayed food processing in
diving animals has emerged from studies on king penguins
(Gauthier-Clerc et al., 2000)
and grey seals Halichoerus grypus
(Sparling et al., 2007).
LIST OF ABBREVIATIONS
O2,CO2 rate
of oxygen consumption/CO2 production
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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