Energetic costs of diving and thermal status in European shags (Phalacrocorax aristotelis)
1 Centre d'Ecologie et Physiologie Energétiques, CNRS, 23 Rue
Becquerel, F-67087 Strasbourg Cedex 2, France
2 Norwegian Institute for Nature Research, Tungasletta 2, N-7485 Trondheim,
Norway
* Author for correspondence (e-mail: manfred.enstipp{at}c-strasbourg.fr)
Accepted 17 July 2005
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Summary |
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Key words: metabolism, diving, thermoregulation, European shag, Phalacrocorax aristotelis, energetics, HIF
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Introduction |
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Great cormorants and European shags (Phalacrocorax aristotelis)
are foot-propelled pursuit divers that forage on benthic and pelagic fish,
which they catch inshore. Both species range from mild temperate climatic
zones to thermally challenging arctic zones
(Johnsgard, 1993). The plumage
of shags and cormorants is supposedly wettable
(Rijke, 1968
), and the plumage
air volume is reduced when compared with other aquatic birds
(Wilson et al., 1992
;
Grémillet et al.,
2005
), reducing buoyancy. Buoyancy is the dominant factor
determining dive costs in lesser scaup ducks (Aythya affinis;
Stephenson, 1994
); hence, a
reduction in buoyancy will tend to reduce dive costs. However, unlike in
penguins, the subcutaneous fat layer of shags and cormorants is negligible and
they have to rely on plumage air as an insulating layer when diving in cold
water. A thinner insulating layer will make them prone to heat loss; hence, it
is not surprising that cormorants and shags leave the water at the end of a
foraging bout to rest on land.
Schmid et al. (1995)
measured the diving metabolic rate of great cormorants (P. c.
sinensis) as
10-12 times their metabolic rate when resting in air
(RMR). This is in strong contrast to the diving metabolic rates that
have been reported for other diving birds, which typically range between two
and four times basal metabolic rate (BMR) for wing-propelled divers
and between three and five times BMR for foot-propelled divers (see
Table 1). Schmid et al.
(1995
) attributed these
exorbitant costs to the poor insulation of cormorants (supposedly wettable
plumage) and the less efficient mode of propulsion (drag-based oscillations,
generating thrust only during one phase of the cycle) when compared with
wing-propelled divers (lift-based oscillations, generating thrust during both
phases of the cycle; Lovvorn,
2001
; Lovvorn et al.,
2004
). However, Johanssen and Norberg (2003) showed that, instead
of relying entirely on drag-based propulsion, great cormorants (and probably
most foot-propelled divers) use a combination of drag-based and lift-based
propulsion during diving, increasing hydrodynamic and, hence, energetic
efficiency. Similarly, Grémillet et al.
(2001
) used a model
integrating the effect of water temperature and dive depth on energy
expenditure during diving to estimate the energetic costs of foraging great
cormorants (P. c. carbo) in Greenland and France. They calculated
that dive costs will vary between nine and 21 times RMR
(Schmid et al., 1995
) when
diving in shallow/warm water and deep/cold water, respectively.
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These high energy costs during foraging contrast with the finding by
Grémillet et al. (2003)
that daily food requirements in cormorants are normal for a seabird of its
mass. Hence, it was suggested that cormorants might employ a behavioural
strategy whereby birds will minimize the amount of time spent in the water to
reduce daily energy expenditure, especially when wintering in thermally
challenging climates (Grémillet et
al., 2001
). Great cormorants in Greenland were observed to reduce
their time spent in water from
50 min day-1 in the summer to
9 min day-1 in the winter
(Grémillet et al.,
2001
). Such a strategy has not been observed in other species
within the Phalacrocoracidae family. European shags wintering in Scotland, for
example, spend up to 7 h day-1 diving in water of around 5-6°C
(Daunt et al., in press
).
Since European shags typically dive to much greater depth and for longer
durations than great cormorants, the energetic challenge might be even more
pronounced for them. Could it be that the energetic costs associated with
foraging in Phalacrocorax are overestimated? Grémillet et al.
(2005
) demonstrated that the
plumage of cormorants is only partially wettable (while the outer feather part
is wettable, the central part is highly waterproof) and that birds maintain a
thin insulating layer of air within their plumage. Hence, insulation during
diving might be better, and heat loss lower, than previously expected assuming
an entirely wettable plumage. In both bank cormorants (Phalacrocorax
neglectus) and South-Georgian shags (Phalacrocorax georgianus)
there is a progressive reduction in abdominal temperature throughout dive
bouts (Wilson and Grémillet,
1996
; Bevan et al.,
1997
). This abdominal temperature drop, supposedly reflecting a
temperature decline in other tissues as well, was suggested as a mechanism to
reduce metabolic rate during diving and increase aerobic dive duration. Given
the paucity of data on the energetic costs associated with diving in
foot-propelled pursuit divers and the exorbitant costs suggested by previous
studies, we felt it was important to investigate the energetic costs
associated with diving in another Phalacrocorax species, the European
shag. Such an investigation is especially important in light of the
contrasting foraging strategies pursued by shags and cormorants during
winter.
The purpose of this study was: (1) to study the energetic costs associated with diving in European shags and any modifying effects of temperature and food and (2) to assess abdominal temperature changes during diving as a potential mechanism to extend dive duration and save energy.
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Materials and methods |
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Training protocol
Within the first week of capture, the shags were introduced to a v-shaped
shallow dive trench (17.5 m long x 2 m wide x 1 m deep) that had
been dug, lined with thick PVC sheeting and filled with seawater. Two
submersible water pumps (ITT Flygt, Oslo, Norway) provided a continuous
exchange with seawater from the adjacent lagoon (200 l min-1).
Over the course of 4 weeks, the surface of the trench was progressively
covered with transparent PVC sheets until only a small section remained open
at one end. Birds that submerged here swam to the opposite end of the trench
where a fish was placed, swallowed the fish underwater and returned to the
uncovered section. Eventually, the open section was covered by a floating
platform with a metal frame in its centre that allowed placement of a
Plexiglas dome, serving as a respiration chamber. Starting 2 weeks before data
collection, birds were captured every day, weighed and placed inside the dome.
Birds dived continuously while the respirometry system was running. Training
trials lasted between 10 and 30 min and ended when a bird stopped diving
voluntarily for more than 5 min. At the end of a trial, the bird was released
from the chamber and returned to its pen.
Respirometry system
Oxygen consumption was measured using an open flow-through respirometry
system (Sable Systems, Henderson, NV, USA). To measure the metabolic rate
during shallow diving, we used a transparent Plexiglas dome in the shape of a
truncated pyramid as the respiration chamber (0.6 m long x 0.6 m wide
x 0.4 m high; volume, 50 litres), which was partially immersed and
received outside air through small holes on its four sides just above the
waterline. Similarly, to measure RMR in air we used a 55-litre bucket
(0.35 m diameter x 0.65 m height) with an airtight Plexiglas lid where
air was drawn in via four small side holes near its bottom. Air from
the respiration chambers was fed directly into the laboratory, which was set
up inside a hut adjacent to the dive trench
(Fig. 1). Airflow from the
respiration chamber was dried using silica gel before being led into a
mass-flowmeter (Sierra Instruments Inc., Monterrey, CA, USA), which
automatically corrected the measured flow to STPD (273 K and 101.3 kPa). A
sub-sample of 10 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 Tygon tubing.
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Air flow through the respiration chamber was maintained at 10 l
min-1 during the resting-in-air trials and at
80 l
min-1 during the dive trials (Piston pump; GAST Manufacuring Inc.,
Benton Harbour, MI, USA). 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 pure
N2, 1.03% CO2 (AGA, Trondheim, Norway) and outside air
(set to 20.95% O2 and 0.03% CO2). Analyser drift was
minimal; nevertheless, any drift was corrected. 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 corresponding flow rate. The delay was found to be 27.0 s (resting in
air) and 16.8 s (diving) for the oxygen analyser and 17.8 s (resting in air)
and 7.65 s (diving) for the CO2 analyser, respectively. These delay
times were taken into account when calculating oxygen consumption rates
(
O2) and
CO2 production rates
(
CO2) and
relating them to diving events. The time constant of the respiration chambers
was calculated to be 5.5 min for resting in air and 0.6 min for diving,
respectively.
Data from the flowmeter and the gas analysers were fed into a universal interface (16 bits resolution; Sable Systems) and mean values were recorded every 1 s (dive measurements) or 5 s (BMR measurements) onto a desktop computer using Datacan (Sable Systems).
Resting metabolism
Basal metabolic rate (BMR) was measured during the night
(22.00-06.00 h) and day (08.00-18.00 h) while birds were resting,
post-absorptive and presumably within their thermo-neutral zone [measurements
between 10 and 19°C air temperature; using the equation given by Ellis and
Gabrielsen (2002) reveals a
lower critical temperature for our birds of
6°C]. Birds were fasted
overnight or for at least 7 h before being placed inside the respiration
chamber. After the initial disturbance, birds calmed down quickly and sat
quietly in the darkened chamber for the remainder of the trial. A stable
O2 was typically
reached within the first hour of these 3-5 h-long trials. Air temperature in
the respiration chamber was monitored using a digital thermometer (Oregon
Scientific, Portland, OR, USA) and usually did not differ from outside air
temperature by more than ±2°C. Birds were familiarized with the
procedure on at least two occasions before data collection began. BMR
was determined from at least three trials per bird during September 2001.
Diving metabolism
Diving metabolic rate was measured in all birds during September and
October 2001 in water temperatures ranging from 4.9 to 12.6°C. Water
temperature was measured after each set of trials 10 cm below the surface. At
the beginning of a trial, a bird was captured, weighed and placed inside the
respiration chamber, from which it dived continuously. Through the window in
the laboratory hut (Fig. 1) it
was possible to observe the undisturbed bird. All relevant behaviour of the
birds was marked onto the respirometry traces, so that behaviour as well as
dive and surface events could be related to the respirometry recordings. In a
subset of trials, swim speed was recorded. For this, an observer with a
digital stopwatch was placed on a ladder 2 m above ground at the 10 m mark of
the dive trench. Swim speed (m s-1) was calculated by dividing the
distance swum (10 m) by the time taken. Only dives in which birds swam in a
straight line were included in the analysis. The majority of trials lasted
20 min (range, 10-50 min), during which birds dived voluntarily and
without any interference. A trial was terminated when a bird remained at the
surface for more than 10 min. A maximum of two dive trials per bird per day
was conducted.
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During some trials, birds would dive very little or not at all but rest at the surface. Stable resting periods from these trials were selected to calculate the metabolic rate during resting on water for both the post-absorptive and the absorptive state. Only resting periods that were separated from any diving activity by at least 5 min were included in the analysis.
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 employed with all birds to
measure stomach temperature during the dive trials. Stomach temperature should
reflect abdominal body temperature during post-absorptive dive trials if no
food is ingested. Temperature loggers were programmed to record stomach
temperature every 5 s and were fed to the birds inside a herring. The loggers
were equipped with a spring crown and were not regurgitated by the birds but
retrieved when the memory was filled, after about 5 days
(Wilson and Kierspel, 1998).
After retrieval, the data were downloaded onto a laptop computer, the logger
was cleaned, re-programmed and re-fed to the bird.
Data analysis and statistics
Oxygen consumption rates
(O2) were
calculated using equation 3b in Withers
(1977
). BMR was
calculated from the lowest 15-min running average value of
O2. Although our
respirometry system was sufficiently fast to allow separation of individual
dive and surface events, we were interested in obtaining an estimate of the
overall energetic costs associated with foraging activity. Hence, we decided
to calculate diving metabolic rate (MRd) as the mean value
of
O2 during a
dive bout from its start until 30 s after the last dive in a bout (i.e.
MRd = oxygen consumption during the entire dive bout
divided by the sum of all dive and surface durations within that bout). A dive
bout was characterised by continuous diving activity and ended, by definition,
when the bird started other activities (e.g. wing-flapping; see
Fig. 2) or remained at the
surface for longer than 2 min (using a log-survivorship plot as bout-ending
criterion; Slater and Lester,
1982
). Birds typically started to dive from the moment they were
introduced into the respirometry chamber. Because of the intrinsic time
constant of our system, however, it took approximately 1 min before our system
stabilised at an equilibrium point (see
Fig. 2). Dives performed during
this time were excluded from analysis. Oxygen consumption rates (ml
O2 min-1) were transformed to kJ using the caloric
equivalent corresponding to the respiratory exchange ratio (RER) of
the birds. The RER was calculated by dividing
CO2 by
O2 and averaged
0.72±0.09 (mean ± S.D.) during resting in
air, 0.74±0.07 during post-absorptive diving and 0.76±0.03
during absorptive diving. Hence, a conversion factor of 19.7 kJ l-1
O2 (Schmidt-Nielsen,
1997
) was used to transform these values to Watts (W).
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Cost of transport (COT in J kg-1 m-1) is defined as the amount of energy required to move one unit of body mass (1 kg) over one unit of distance (1 m). We calculated COT as the energy expenditure during a dive trial (W kg-1) divided by the mean swim speed (m s-1) during that trial. We included only post-absorptive dive trials in the COT analysis, which spanned a temperature range of 5-13°C.
Insight into the insulative properties of birds can be gained by
calculating their thermal conductance (TC). We calculated TC
for our shags (post-absorptive trials) when resting in air and water and
during diving using the following equation:
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where TC is in W m-2 °C-1, MR
(metabolic rate) is in W; Tb is the body temperature (mean
stomach temperature during a trial) in °C, Ta is the
ambient temperature in °C and SA is the surface area in
m2, which was estimated using Meeh's formula:
SA=10xMb0.67
(Drent and Stonehouse, 1971),
where Mb is in g and SA is in cm2.
Stomach temperatures were analysed using Multitrace (Jensen Software Systems, Laboe, Germany). Resting values during the night and day were established from periods when birds were calm. Temperature recordings were averaged over a period of 6 h during the night (between 23.00 h and 05.00 h) and over periods of at least 2 h during the day (between 08.00 h and 18.00 h). Temperature recordings from the entire period of experimentation were included in the analysis.
Stomach temperatures during the various phases of a dive trial were taken as averages from the first and last minute of a trial (`diving start' and `diving end', respectively) and as the single highest value during a trial (`diving peak'). Only stomach temperature recordings from birds that had not ingested food for at least 3 h were included in the analysis to exclude periods of decreased stomach temperature after food ingestion.
One-way repeated-measures analysis of variance (ANOVA) with Tukey pairwise
multiple comparisons was used for comparison of metabolic rate during
different activities and feeding status and for comparing stomach temperatures
during various phases. When single comparisons were made, as in comparing
BMR measured during the day and during the night, Student's paired
t-test was used. Significance was accepted at P<0.05. The
relationship between energy expenditure and water temperature that takes into
account variability between subjects was determined using repeated-measures
multiple linear regression, with each bird being assigned a unique index
variable (Glantz and Slinker,
1990). All mean values are presented with standard deviation
(±1 S.D.).
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Results |
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Water temperature had a significant effect on post-absorptive diving metabolic rate, so that metabolic rate increased with a decrease in water temperature (Fig. 4). The equation relating post-absorptive diving metabolic rate to water temperature was: MR=28.461-0.671Tw, where Tw is water temperature in °C and MR is measured in W kg-1 (P<0.01, t=-3.52, r2=0.69).
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When plotting COT against swim speed, the relationship was best described by an inverse first-order polynomial regression with a minimum COT value of 17.8 J kg-1 m-1 at a swim speed of 1.3 m s-1 (r2=0.48, P=0.018).
Thermal conductance when resting in air of 10-19°C was 2.05±0.16 W m-2 °C-1 and tripled when floating on water of 5-13°C (6.64±0.28 W m-2 °C-1). Diving within the same temperature range increased thermal conductance even further to 7.88±0.5 W m-2 °C-1, almost four times the value when resting in air. There was no detectable change in TC with a decrease in water temperature within the range tested (P=0.62, t=-0.50).
Mean stomach temperature when resting during the day was
40.6±0.2°C, which declined significantly during the night to
39.2±0.1°C (Fig. 5).
At the start of a dive trial, temperature was significantly elevated from the
daytime resting value and continued to rise during diving. After about 5-10
min of diving, however, a peak was reached after which temperature started to
decline (Fig. 2B). Stomach
temperature at the end of a dive trial was significantly lower than the peak
value reached during diving, but this drop was not significant when compared
with the temperature at the start of a dive trial
(Fig. 5). The mean temperature
increase early in a dive trial was 0.3°C, while temperature at the
end of a trial was, on average,
0.6°C below the temperature at the
start. Stomach temperature changes during a dive trial and the cooling rate
(°C min-1 in water) were not affected by the water temperature
during a trial. Temperature drop and cooling rate were similar during trials
in warm and cold water (range, 5-13°C).
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Discussion |
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The BMR we measured in European shags is almost identical to the
predicted BMR of 4.60 W kg-1, again using the allometric
equation given by Ellis and Gabrielsen
(2002), which is based on 77
seabird species. It is slightly lower, however, than the BMR value
for European shags measured by Bryant and Furness
(1995
; 5.28±0.22 W
kg-1).
The energetic costs of diving in European shags (expressed as multiples of
BMR) are thus comparable to dive costs of other foot-propelled divers
that have been investigated (Table
1). They are, however, considerably higher than dive costs
observed in most wing-propelled divers. The energetic costs associated with
diving are generally higher in foot-propelled than wing-propelled divers, with
diving metabolic rates ranging between 3-5 and 2-4x BMR,
respectively (Table 1). This
general difference might be the consequence of an inherently lower efficiency
of foot propulsion, which is mostly drag based, when compared with wing
propulsion, which is mostly lift based
(Lovvorn and Liggins, 2002).
Wing propulsion allows thrust on both upstroke and downstroke, whereas foot
propulsion in most species has little or no thrust on the upstroke (but see
Johanssen and Norberg, 2003). While some foot-propelled divers (e.g. South
Georgian shags; Bevan et al.,
1997
) achieve dive performances (in terms of dive depth and swim
speed) that are comparable with that of wing-propelled divers, Lovvorn and
Liggins (2002
) suggested that
they might do so at great locomotor cost.
Cormorants and shags are both foot-propelled divers, so the propulsive
mechanism alone is not likely to explain the observed difference in their
diving metabolic costs. However, European shags are considerably smaller in
size than great cormorants and their body shape is slimmer and more
streamlined when compared with the more bulky great cormorant. Hydrodynamic
drag is the most important mechanical cost during steady swimming in birds
that dive to depth, where work against buoyancy will be reduced. Lovvorn et
al. (2001) showed that the
hydrodynamic drag experienced by diving birds strongly depends on body size
and shape. Hence, the drag experienced by European shags during diving might
be reduced when compared with the great cormorant, in turn lowering energetic
costs.
Another important factor to consider is buoyancy. In fact, the high diving
costs observed in foot-propelled benthivore ducks (as indicated by
Table 1) are mostly caused by
the large amount of air trapped within their respiratory system and plumage
(Lovvorn and Jones, 1991).
Stephenson (1994
) found that
buoyancy was the dominant factor determining dive costs in lesser scaups
diving to the bottom of a 1.5 m-deep tank. Buoyancy accounted for
75% of
the mechanical cost of underwater locomotion in these ducks. In foot-propelled
pursuit divers, such as cormorants and shags, overall buoyancy is reduced when
compared with diving ducks (Lovvorn and
Jones, 1991
). While this would tend to decrease diving costs, it
should be stressed that cormorants and shags are still highly buoyant,
answering to the demands of aerial flight. Double-crested cormorants
(Phalacrocorax auritus) have a specific buoyancy of 2.7 N
kg-1 (Lovvorn and Jones,
1991
) and ascend passively by means of positive buoyancy from
dives to 10 m depth (Enstipp et al.,
2001
). Hence, work against buoyancy might still contribute heavily
to the overall dive costs in cormorants and shags, especially when diving in
shallow tanks. In this context, it is interesting to note that cormorants
evolved a dynamic buoyancy control mechanism that enables them to counter the
destabilizing effects of buoyancy at shallow depth simply by tilting their
body and tail (Ribak et al.,
2004
). While this tilting behaviour would tend to increase drag
and, hence, energetic costs, the authors speculated that this might be at
least partly offset by the fact that cormorants use a burst-and-glide pattern
during diving. When diving in the wild, great cormorants typically descend to
shallow depths, where work against buoyancy might still be substantial (mean
dive depth, 3-7 m; Grémillet et
al., 2001
). European shags, on the other hand, dive to depths
where costs associated with overcoming buoyancy will be greatly reduced (mean
dive depth, 26 m; range, 4-61 m; Wanless
et al., 1997
), decreasing the overall dive costs in European shags
when compared with great cormorants. However, since shags in our study dived
within a 1 m-deep trench, this cannot explain the measured difference in
diving metabolic rate between both species.
The relatively high diving costs observed in cormorants and shags might
also be the result of their poor insulation, increasing thermoregulatory
costs. In support of this, Table
1 shows that the metabolic rates of ducks resting on water are
similar to their resting rates in air, indicating a good insulation and low
thermoregulatory costs. By contrast, metabolic rate in great cormorants and
European shags is greatly increased when floating on water (4.5 and 4.1x
BMR, respectively), indicating greater heat loss and thermoregulatory
costs when compared with resting in air. Similarly, Ancel et al.
(2000) reported a metabolic
rate for Brandt's cormorants of 10.9 W kg-1 when resting in warm
water (20°C) during the day. This would correspond to 2.5x
BMR (BMR predicted from the allometric equation provided by
Ellis and Gabrielsen, 2002
).
Heat loss will be further increased during diving, when the insulating plumage
air layer will be compressed by the increase in hydrostatic pressure and when
movement through the water will disturb the boundary layer. De Vries and van
Erden (1995
) found that the
thermal conductance of aquatic bird carcasses increased by a factor of 4.8
during diving when compared with air. In our study, the thermal conductance of
European shags increased by a factor of 3.8 during diving. In great cormorants
(using data from Grémillet et al.,
2003
) thermal conductance was not only higher in absolute terms
but it also increased by a greater factor (4.4) during diving, indicating
better insulative properties in European shags. We used the heat loss model
developed by Grémillet et al.
(1998
) and our measurements of
energy expenditure during diving to estimate the minimal insulating plumage
air volume in European shags. The value of 0.38x10-3
m3 at a depth of 1 m corresponds to a 2.71 mm air layer, which is
60% greater than the calculated value for great cormorants. Hence, a
thicker plumage air layer in shags will provide a better insulation, reducing
heat loss during diving. This will be especially important for shags during
winter, when they spend extended periods foraging in cold water. Heat
generated by muscular activity during diving will also help to reduce
thermoregulatory costs.
Factors modifying diving metabolic rate
Water temperature had a marked effect on metabolic rate of shags during
diving and when resting in water, so that metabolic rate increased when water
temperature decreased (Fig. 4).
Relatively few studies have investigated the effect that water temperature has
on the metabolic rate of unrestrained birds resting in water or diving. In
tufted ducks (Aythya fuligula), common eiders (Somateria
mollissima), common murres (Uria aalge), thick-billed murres
(Uria lomvia) and little penguins (Eudyptula minor) that
rest in water, metabolic rate increased with a decrease in water temperature,
which was especially drastic at water temperatures below the point of thermal
neutrality (Bevan and Butler,
1992; De Leeuw,
1996
; Jenssen et al.,
1989
; Croll and McLaren,
1993
; Stahel and Nicol,
1982
). To our knowledge, the effect of water temperature on diving
metabolic rate has only been investigated in tufted ducks
(Bevan and Butler, 1992
;
de Leeuw, 1996
) and great
cormorants (Grémillet et al.,
2003
). The increase in metabolic rate with a decrease in water
temperature observed in our study during diving and when resting in water (16%
and 17%, respectively) was similar to what has been found in other aquatic
birds. The following comparisons are all based on calculations covering the
same temperature range investigated in our study (4.9-12.6°C). Metabolic
rate of tufted ducks resting in water and diving increased with a decline in
water temperature by 12% and 8.5%, respectively
(de Leeuw, 1996
). Similarly,
in diving great cormorants, metabolic rate increased by 17% when water
temperature declined (Grémillet et
al., 2003
). The greatest increase observed, however, was in common
and thick-billed murres when resting in water (28% and 30%, respectively;
Croll and McLaren, 1993
). It
is not intuitively obvious why this temperature effect on metabolic rate
should be the strongest in two species that, outside the breeding season,
spend their entire time at sea with water temperatures below their lower
critical temperature (15°C; Croll and
McLaren, 1993
). The increase in metabolic rate of shags with
declining water temperature was linear throughout the temperature range
tested. This suggests that the point of thermal neutrality for European shags
in water is above 12.6°C, the highest temperature tested in our study.
The increase in metabolic rate that accompanies the process of digestion,
assimilation of food and nutrient interconversion by animals is known as the
`heat increment of feeding' (HIF; Brody,
1945). Heating ingested cold food to body temperature also
requires energy and will elevate metabolic rate further. Feeding before a
trial elevated metabolic rate in shags during diving and when resting in water
by an average of 13% and 15% above the post-absorptive rate, respectively
(Fig. 3). This is similar to
the increase observed in common and thick-billed murres when diving after food
ingestion (fig. 1 in Croll and McLaren,
1993
). An increased metabolic rate during diving would tend to
reduce dive duration, as the available oxygen during a dive would be used up
at a faster rate. Birds diving in the wild might therefore structure their
foraging bouts accordingly. The increase in metabolic rate that we observed in
our shags is lower than the increase observed in thick-billed murres after
food ingestion when resting in air (40%;
Hawkins et al., 1997
) or in
sea otters (Enhydra lutris) when fed while resting in water (54%;
Costa and Kooyman, 1984
). The
latter authors suggested that otters might use the heat produced from the HIF
to substitute for heat that otherwise has to be generated by activity or
through shivering and, hence, reduce thermoregulatory costs. This could be an
important energy-saving mechanism, especially for aquatic animals where
foraging is often interspersed with long resting bouts on the water surface.
However, European shags typically do not spend extended periods of rest on the
water surface after a foraging bout but rather leave the water to rest on
land. During chick rearing, European shags in Scotland spent
85% of their
daily time resting at the colony (Enstipp
et al., in press
). Cool air temperatures, wet and windy conditions
are often prevalent and might require heat production that could be augmented
by the HIF. Furthermore, stomach temperature of shags in our study remained
elevated throughout dive trials even in 5°C water. If this also holds true
for their extended dive bouts during winter (up to 7 h;
Daunt et al., in press
) the
additional heat generated by the HIF could be important in offsetting
thermoregulatory costs during these dives. If, on the other hand, European
shags, like South Georgian shags, allow body temperature to fall during these
long dive bouts, the HIF might be an energetically inexpensive way of
replacing heat lost during diving at the end of a foraging bout
(Bevan et al., 1997
). Heat
generated during flight, when shags leave the foraging area, might contribute
even stronger to this end.
Stomach temperature
The stomach temperature patterns of diving European shags recorded in our
study are similar to patterns observed in wild shags
(Grémillet et al.,
1998). Stomach temperature of shags in our study remained elevated
throughout dive trials lasting up to 50 min in water as cold as 5°C (Figs
2B,
5). This is similar to the
situation observed in great cormorants diving under comparable conditions
(Schmid et al., 1995
;
Grémillet et al.,
2001
). Hence, unlike in South Georgian shags or bank cormorants,
there is no evidence that European shags or great cormorants might employ a
strategy of regional hypothermia to potentially lower energetic costs and
increase aerobic dive duration (Bevan et
al., 1997
).
Our study has shown that the energetic costs during shallow diving in European shags are considerably lower than in great cormorants and are comparable with other foot-propelled divers. This difference might be partially explained by lower hydrodynamic costs during diving in the shags, owing to their smaller size and more streamlined body shape. It might also be explained by a better thermal insulation in shags, reducing thermoregulatory costs during diving. Water temperature and feeding status had a strong impact on diving energetics in shags, so that metabolic rate increased with declining water temperatures and remained elevated after food ingestion for up to 5 h. We found no evidence that European shags might employ a strategy of regional hypothermia, since stomach temperature remained elevated throughout dive trials. Shags in this study were diving within a shallow dive trench. Hence, the effects that depth might have on the energetic costs during diving could not be evaluated. The increase in ambient pressure when diving to depth will decrease the amount of air trapped within the plumage and hence thermal insulation. The resulting increase in heat loss might outweigh any energetic advantages that a decreased buoyancy at greater depth might produce, especially if water temperature is low. However, the energetic consequences of diving to depth remain to be investigated.
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