Behavioral Ecology Vol. 10 No. 5: 516-524
© 1999 International Society for Behavioral Ecology
A life in the fast lane: energetics and foraging strategies of the great cormorant
Institut für Meereskunde Kiel, Düsternbrooker Weg 20, D-24105 Kiel Germany
Address correspondence to D. Grémillet, who is now at the Institute of Terrestrial Ecology, Banchory Research Station, Hill of Brathens, Glassel, Banchory, Kincardineshire AB31 4BY, Scotland. E-mail: dgrem{at}wpo.nerc.ac.uk .
Received 24 February 1998; revised 4 November 1998; accepted 3 February 1999.
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ABSTRACT |
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Body insulation is critically important for diving marine endotherms. However, cormorants have a wettable plumage, which leads to poor insulation. Despite this, these birds are apparently highly successful predators in most aquatic ecosystems. We studied the theoretical influence of water temperature, dive depth, foraging techniques, and prey availability on the energetic costs of diving, prey search time, daily food intake, and survival in foraging, nonbreeding great cormorants (Phalacrocorax carbo). Our model was based on field measurements and on data taken from the literature. Water temperature and dive depth influenced diving costs drastically, with predicted increases of up to 250% and 258% in males and females, respectively. Changes in water temperature and depth conditions may lead to an increase of daily food intake of 500-800 g in males and 440-780 g in females. However, the model predicts that cormorant foraging parameters are most strongly influenced by prey availability, so that even limited reduction in prey density makes birds unable to balance energy needs and may thus limit their influence on prey stocks. We discuss the ramifications of these results with regard to foraging strategies, dispersal, population dynamics, and intraspecific competition in this avian predator and point out the importance of this model species for our understanding of foraging energetics in diving endotherms.
Key words: diving behavior, diving endotherms, energetics, foraging strategies, great cormorants, insulation, Phalacrocorax carbo, prey density.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The energetics of warm-blooded animals are closely linked to the physical characteristics of their direct environment, especially to the temperature and the thermal conductivity of the surrounding medium. In this respect, diving homeotherms experience particularly drastic conditions because the thermal conductivity of water is more than an order of magnitude higher than that of air. To reduce heat losses, most diving warm-blooded animals have thus evolved toward a substantial increase of their superficial insulation in the form of a thick subcutaneous fat layer and/or an insulating air layer trapped in waterproof plumage or fur (Costa, 1991
). However, among the approximately 272 diving mammal and bird
species (Campbell and Lack,
1985; Kooyman,
1989), several obviously did not follow this mainstream
evolutionary pattern. Both cormorants (Phalacrocorax spp.) and
darters (Anhinga spp.) are, for example, well known for their
wettable plumage and thus represent an interesting case of poorly insulated
diving birds. In cormorants, plumage wettability is traditionally considered
an archaic morphological pattern that prevents the birds from spending
extended periods in the water and results in high overall thermoregulatory
costs and resulting high fish consumption
(Johnsgard, 1993). However,
recent studies have shown that daily food requirements in great cormorants are
normal for a seabird of their size
(Grémillet
et al., 1995;
Grémillet
and Argentin, 1998). These unexpected results are presumably
linked to particular foraging techniques allowing an extremely high predatory
efficiency
(Grémillet,
1997;
Grémillet
et al., 1998a), as well as to special energy-saving strategies
(Grémillet
et al., 1998b). However, all investigations on great cormorants
have been conducted during the temperate breeding season, and virtually no
data are available for the remaining 80% of the year (but see
Keller, 1997), despite the
fact that energy requirements are likely to be substantially higher during
this time due to less favorable abiotic conditions (see
Grémillet
et al., 1998b). In the present study, we use data from free-living birds together with data from the literature to explore the theoretical influence of water temperature, water depth, prey availability, and body mass on the energetics and the foraging strategies of nonbreeding great cormorants during the winter. This poorly insulated model species enables us to characterize the influence of abiotic and biotic parameters on the foraging energetics of diving endotherms.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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A four-step model was designed to assess the theoretical influence of water temperature, dive depth, search time for prey, and body mass on the daily food intake of nonbreeding great cormorants.
Calculation of heat loss to the water as a function of body mass,
water temperature, and water depth
We calculated heat loss using a model developed by
Grémillet et al.
(1998b). Briefly, heat losses
to the water in swimming great cormorants were calculated for a featherless
bird's body insulated by a regular air layer using
 | (1) |
T is the temperature
difference between the body temperature (°C) and the water temperature
(°C). The coefficient of heat transmission, k, can be calculated
by
 | (2) |
is the coefficient of heat transfer (W/m-2
· K-1), 
is the coefficient of steady-state heat
conduction (W/m · K-1) of a particular insulating
layer (here either a fat or air layer), and 
is the thickness of this
layer (m). Except for the parameters water depth, water temperature, and body
mass, the standard model input given in
Grémillet et al.
(1998b) was used throughout
the study (see Table 1). We
used a constant body temperature throughout the calculations. This assumption
is based on measurements conducted with stomach temperature loggers on
free-ranging cormorants swimming in water at 12°C (French Channel Islands;
Grémillet
et al., 1998b) and at 3-5°C (Disko, West Greenland;
Grémillet, unpublished data). The model was
run for different body masses, water temperatures, and water depths.
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The influence of water depth
To calculate heat losses of great cormorants foraging at different water
depths, it is necessary to know the diving patterns of the birds. These were
derived from data recorded in five free-ranging great cormorants breeding at
the Chausey Islands (48°55' N, 01°45' W), France, in April
and May 1996. Birds were caught under licence at the nest site using a
remote-controlled net trap
(Grémillet
and Wilson, 1998) and were fitted with a diving event electronic
processor (DEEP; Driesen and Kern GmbH, Am Hasselt 25, Bad Bramstedt, Germany;
mass 30 g; 88 mm x 17 mm x 10-17 mm; relative accuracy 0.04 bar),
which automatically recorded hydrostatic pressure at intervals of 8 s. The
device was attached underneath the tail of the birds with tape in order to
reduce hydrodynamic drag (Bannasch et al.,
1994). After a deployment period of 4-9 days, the bird was caught
again, the device recovered, and the data downloaded. To avoid individual
bias, we based calculations on a subsample of the dive profiles recorded
during 40 foraging trips, where 8 trips were chosen at random from each
individual. Additionally, we used general linear model analysis to test for
differences between the slopes of individual relationships (see
Table 2). This test was
negative in all cases, confirming that no bird effect biased this sample. Data
sets were analyzed using Andive8 (Jensen Software Systems, Lammerzweg, 19,
D-24235 Laboe, Germany). We divided dive profiles into two categories:
V-shaped dives (where the bottom duration was less than 16 s (i.e., twice the
recording interval of the DEEPs), and U-shaped dives with a bottom duration of
at least 16 s.
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In both V-shaped and U-shaped dives, significant relationships were defined
between maximum dive depth (MDD) and the following variables: transit time
(time spent between the water surface and MDD during descent and ascent),
bottom time (time spent at MDD) recovery time (time spent at the water surface
between two dives), and number of dives conducted per foraging trip (see
Table 2). Following guidelines
given in Wilson and Wilson
(1988) and Wilson et al.
(1996), and in accordance with
previous investigations (see
Grémillet
et al., 1998a), we assumed that bottom time comprised time
allocated to prey location during U-dives, whereas total transit time is used
to this end in V-dives. Moreover, based on analysis of direct field
measurements, we considered that cormorants were likely to conduct both U- and
V-dives within the same foraging area
(Grémillet
et al., 1998a) and that feeding rates were not affected by the
feeding zone
(Grémillet,
1997). Consequently, we assumed mean bottom time per foraging trip
in U-dives and mean transit time per foraging trip in V-dives to be the time
required by great cormorants breeding on Chausey to acquire their food load
irrespective of water depth. Using these fixed mean values for bottom time in
U-dives and for transit time in V-dives and relationships between MDD and
other dive parameters presented in Table
2, we then back-calculated transit times and recovery times during
dive cycles conducted for different water depths. These time lapses spent at
different depths were then used to calculate mean heat losses over typical V-
and U-dive cycles conducted for water depths between 2 m and 32 m (the depth
range recorded in birds from the Chausey Islands; see
Table 2) as
 | (3) |
 | (4) |
In U-dives, mean transit time and mean recovery time are
 | (5) |
 | (6) |
In V-dives, recovery time can be similarly expressed as
 | (7) |
Consequently, equations 3 and 4 can be simplified and
Qmean calculated as
 | (8) |
 | (9) |
These mean heat losses to the water were then calculated for U- and V-dive cycles conducted by male and female great cormorants for different water depths. Finally, mean heat losses were also determined for typical diving bouts conducted by great cormorants breeding on Chausey, which entail 64% of U-dives and 36% of V-dives (see Table 2).
The influence of water temperature
Mean heat losses to the water (W) were also calculated for temperatures
between 0°C and 25°C, as this span is the most extreme that may be
experienced by European great cormorants according to their distribution
(Johnsgard, 1993).
Influence of water temperature and dive depth on swimming costs
Using mean heat losses to the water calculated for different water depths,
water temperatures,, and body masses (males and females), we subsequently
calculated the overall energy costs of swimming that diving birds may
experience under these different conditions. To this end, we used energy costs
of swimming given by Schmid et al.
(1995), which were recorded
for birds diving at a mean MDD of 0.5 m in water at 12°C. Energy costs of
swimming were then calculated as
 | (10) |
),
Qmean is the heat flux to the water (W) experienced by a
bird diving under conditions given by Schmid et al.
(1995) (0.5 m depth and
12°C water temperature).
Influence of water temperature and dive depth on minimal search
time
We assumed minimal search time in foraging great cormorants to be the time
lapse at the end of which birds have an overall energy efficiency of 1.0
(i.e., the value that corresponds to a steady state for which energy gain and
energy loss are equal over 1 day). We calculated energy gain in foraging great
cormorants using prey-capture rates given in
Grémillet
(1997) as 15.3 g/min for males
and 9.0 g/min for females, where the time base is the time spent underwater.
This is correct as long as no relationship exists between total dive duration
and the prey-capture rate (which is the case in great cormorants; see
Grémillet,
1997).
Great cormorant chicks are fast growing offspring requiring a substantial
food supply
(Grémillet
et al., 1995;
Grémillet
and Argentin, 1998). Adult breeding great cormorants, which are
assumed to optimize their predatory efficiency, experience strong selection to
be particularly successful at this time, so that prey-capture rates can be
considered maximal for this species. These data were converted to derive catch
per unit time (CPUT) values for overall swimming time (which includes the
interdive recovery time as well as the time under water) using standard
relationships between dive time and recovery time
(Table 2). Mean CPUT was thus
taken to be 8.4 g/min in males and 5.3 g/min in females.
Energy loss during periods other than swimming and diving was compiled
using data taken from the literature, which are presented in
Table 3. Since nonbreeding
great cormorants typically forage once a day
(Grémillet
and Argentin, 1998;
Grémillet
et al., 1995), overall energy balance was calculated for a bird
that has to acquire enough energy during a single foraging trip to provide for
a full day's energy expenditure. Minimum search time was calculated for both
sexes of both great cormorant subspecies under different water depth and water
temperature conditions as the swimming time for which
 | (11) |
), AE is the assimilation efficiency of the birds,
taken to be 77% (Brugger,
1993), En is the energy requirements of the
bird for 1 day (J), except swimming costs (from En values
for males and females stated in Table
3), and Eswim is the energy costs of swimming
(W) for a particular body mass, water depth, and water temperature as
calculated in the previous section. Examples of the relationships between
energy gain and energy loss in foraging great cormorants are given in
Figure 1.
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Influence of water temperature and dive depth on daily food
intake
Using calculated minimal search times for the different sexes and
subspecies of great cormorants under different depth and temperature regimes,
we calculated their theoretical daily food requirements via
 | (12) |
Influence of prey availability on overall energy requirements
To assess the influence of different levels of prey availability on minimal
search time and daily food intake, all calculations concerning these variables
were repeated using standard CPUT values equal to 150%, 75%, or 50% of the
mean field values used above. We used these CPUT values to indicate specific
prey availabilities, assuming that the birds tend to optimize foraging
techniques so as to maximize their predatory yield. Consequently, prey
densities cited in this paper are cited as density 1.0 (which corresponds to
the average CPUT measured in the Chausey Islands area;
Grémillet,
1997), density 1.5, density 0.75, or density 0.5. Finally, we also
calculated the minimal CPUT necessary to reach an overall efficiency of 1.0 in
male and female great cormorants for different water temperatures and dive
depths.
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RESULTS |
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Influence of dive depth and water temperature on heat flux to the water and overall swimming costs
Both water temperature and dive depth influence theoretical heat losses to the water (Q) (Figure 2) and thus also overall swimming costs (Eswim) considerably. Using the entire range of temperatures and depths, the highest possible increase of these costs is predicted to be 250% in males and 258% in females. Dive depth variability has a much greater influence on heat loss and swimming costs than does water temperature (Figure 2).
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Influence of diving techniques on mean heat flux to the water in
great cormorants foraging under different abiotic conditions
Diving techniques do not apparently have a major influence on the swimming
energetics of great cormorants because, for comparable depth and temperature
conditions, birds conducting exclusively U-dives, exclusively V-dives, or both
U-dives and V-dives showed only minimal differences in their heat flux to the
water (less than 5% in all cases).
Influence of water temperature and dive depth on minimal search time
and daily food intake for a prey density equivalent to that found at
Chausey
The influence of water temperature and dive depth on minimal search time
(e.g., the swimming time needed by a bird to find enough fish to sustain
itself for a period of 24 h) and on daily food intake of nonbreeding great
cormorants was not as important as the influence of these parameters on heat
losses and swimming costs. Changing conditions from one extreme situation
(0°C water temperature, 32 m water depth) to the other (25°C water
temperature, 2 m water depth) caused a maximal variation of minimal search
time and thus of daily food intake of 62% in males
(Figure 3b) and 56% in females
(Figure 4b). Under these
conditions, daily food intake may vary between approximately 500 g and 800 g
in males and between approximately 440 g and 780 g in females; daily food
intake in birds from the Chausey Islands (12°C water temperature, 6 m
water depth) was calculated to be 580 g in males and 530 g in females (Figures
3b and
4b).
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Males are predicted to be able to cope with the entire range of water temperatures and dive depths assumed in our model by increasing their search time and their food requirements accordingly (Figure 3b), whereas females are predicted to fail for temperatures lower than 2°C and when diving deep (this is shown by the sudden drops in minimal search time and daily food intake to zero in Figure 4b, which shows areas of the function for which foraging efficiency never reaches 1.0).
Influence of prey availability on minimal search time and daily food
intake of great cormorants foraging under different abiotic conditions
Calculation of minimal search time and daily food intake in foraging great
cormorants with different catch per unit effort values, and thus theoretically
exposed to variable prey densities, shows that this particular parameter
strongly influences energetics. A reduction of prey density of only 25% (CPUT
of 0.75) causes an overall increase of 50-100% for minimal search time and DFI
in males (with predicted DFI varying between 550 g and 1230 g), and female
birds are predicted to exceed foraging efficiencies of 1.0 only for water
temperatures higher than 15°C and when diving to shallow depths (see
Figures 3c and
4c). A further decrease of prey
density to a CPUT of 0.5 results in the prediction that females fail to reach
a foraging efficiency of 1.0 irrespective of temperature or dive depth,
although males could do so if water temperatures exceeded 15°C and if
dives were shallow (Figure 3d).
An increase of prey density (CPUT of 1.5) results in no comparable decrease of
minimal search time and DFI. These apparently extremely suitable conditions
cause decreases in minimal search times and DFI of only 9-26% in males (with
DFI varying between about 460 g and 590 g) and 12-30% in females (with DFI
varying between about 390 g and 550 g; see Figures
3a and
4a).
Finally, we calculated that minimal required CPUTs in males exposed to different water temperatures and depth conditions remain lower than the value measured for free-living individuals, whereas in females minimal required CPUTs nearly correspond to measured field values (Figure 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Overall accuracy of the model
The above calculations were performed using literature data collected from different cormorant species (see Table 3), published data specifically recorded in great cormorants (Tables 1 and 2), and a model proposed by Grémillet et al. (1998b
). Due to the partial
use of literature data, we cannot provide overall confidence intervals for our
output data. However, it can be stated that (1) the thermodynamic model given
by Grémillet et al.
(1998b) predicts the minimum
loss of heat to the water; (2) variability in the diving techniques of the
birds (proportion of U- and V-dives) does not significantly influence our
output values (see Results); (3) both CPUT values and energy costs of swimming
are dominant input values that critically influence results presented above
(see equation 11). In this respect, it is important to note that both values
have been directly measured in great cormorants using highly precise, direct
measurement techniques (i.e., gas respirometry, automatic weighing, and
radio-tracking). Consequently, we consider our overall output values
concerning minimal search time and DFI for great cormorants exposed to
variable environmental conditions to be rather conservative estimates. In
addition, we stress that rather than to derive absolute values, our aim is to
elucidate trends in how water temperature, dive depth, and prey availability
might influence daily food intake and potential survival in nonbreeding great
cormorants as a model species of poorly insulated diving endotherms.
Relative importance of water temperature, water depth, and prey
availability on daily food intake and survival of the birds
Grémillet et al.
(1998b) studied the
theoretical influence of different biotic and abiotic factors on heat losses
of diving great cormorants and stressed the relevance of plumage air volume,
water depth, and water temperature on the diving energetics of these birds.
Results presented above confirm the substantial influence of different water
depth and water temperature regimes on the overall energetics of free-ranging
great cormorants (see Figure
2), although the final effect of both parameters on the DFI of the
birds is not as dramatic as suggested by
Grémillet et al.
(1998b), especially when prey
density is high (see Figures
3a,
b and
4a,
b). This is because water depth
and water temperature are only relevant for calculations of the energy costs
of swimming, which represent about 15% of total daily energy requirements (see
Grémillet
et al., 1995). Therefore, the influence of highly variable energy
costs of swimming is partly buffered by other, less variable costs such as
those of flying or resting on land, which were not taken into account by the
model. Thus, for normal prey densities (see Figures
3b and
4b), birds are able to cope
with a wide temperature and depth range by moderately increasing their
DFI.
However, prey availability appears to have a major influence on DFI and
survival of great cormorants, as even minor reductions in prey density lead to
a dramatic increase of DFI in males (Figure
3c,
d) and apparently compromise
survival in females at most depth and temperature regimes
(Figure 4c). This highlights
the physiological and ecological implications of the semiaquatic lifestyle
adopted by great cormorants. By minimizing the volume of air trapped in their
plumage, great cormorants are able to reduce their buoyancy, which allows them
to be agile underwater swimmers (Wilson et
al., 1992). This particular advantage allows them to be highly
efficient aquatic predators, with mean CPUT values 5-8 times those of African
penguins (Spheniscus demersus)
(Grémille
,
1997; Wilson and
Grémillet, 1996). However, due to
their minimal insulation and thus massive thermoregulatory costs when
searching for prey, great cormorants cannot overly extend their time in the
water and are thus dependent on high prey densities to survive.
Implications for our understanding of the ecology and population
dynamics of great cormorants
Our results confirm that estimates of DFI in great cormorants, which are
generally recorded during a particular season and for a particular location
(i.e., with specific depth and temperature conditions and for a particular
prey density) cannot be directly used for calculations concerning energy
requirements for birds living elsewhere. A general application derived from a
specific study may underestimate or overestimate real food requirements by
more than 100%. Furthermore, the extreme sensitivity of great cormorants as
predators toward the density of prey items within their foraging range throws
a new light onto the present political debate concerning possible depletion of
fish stocks by great cormorants (Kirby et
al., 1996). Great cormorants may indeed consume substantial
quantities of fish, especially under harsh winter conditions when water
becomes cooler and fish move deeper in the water column, but these birds are
apparently unable to survive when prey density is low. Consequently, great
cormorants are unlikely to exploit fish stocks below the replacement line
(sensu Russell et al., 1996),
thus depleting them. Rather, birds will probably forage in a certain area for
only as long as fish density is high enough, before they move away. Although
predators in general are predicted to display a similar strategy
(Stephen and Krebs, 1987), our
data demonstrate the extreme sensitivity of great cormorants toward prey
availability (Figures 3 and
4). This can be confirmed by
several empirical studies. Data collected on great cormorants wintering in
Switzerland showed, for example, that predator density was strongly correlated
to the trophic level of freshwater ecosystems
(Suter, 1995). Moreover, shags
from the Firth of Forth (Scotland), which rely heavily on sand eels
(Ammodytidae) during the breeding season, were shown to be extremely sensitive
to prey abundance, delaying the onset of breeding or failing completely in
some years when prey abundance was low (Wanless et al., unpublished data).
Similar behavior was also recorded by Rand
(1960) for cape cormorants
(Phalacrocorax capensis). This also explains the close link between
eutrophication of West European inland waters and the exponential increase of
great cormorant populations in this area since the late 1970s (see
Russell et al., 1996).
Intersexual discrepancies
The model identifies major intersexual differences with respect to
sensitivity to water temperature, water depth, and prey availability (see
Figures 3 and
4). This is principally due to
gender-linked differences in catch per unit effort values, although sexual
dimorphism (males are on average 40% heavier than females) also plays a role
in influencing the surface area/volume ratios of the birds and thus their
thermoregulatory costs. These intersexual differences may explain a number of
observed features in cormorant ecology. First, great cormorants have been
shown to be dispersal migrants
(Géroudet,
1959). The continental subspecies P. c. sinensis displays
the most marked migratory patterns, where birds from northwestern Europe
(Denmark, the Netherlands) move as far south as Morocco during the winter
months (Munsterman and van Eerden,
1989). Ring recoveries and direct observation of color-marked
birds show that lighter (female) birds tend to migrate much farther south than
heavier (male) birds (Munsterman and van
Eerden, 1989). The conventional explanation offered was that the
fittest, heaviest males tend to start breeding first and thus stay as close to
the breeding sites as possible, or that competition between birds tended to
drive lighter birds farther south
(Munsterman and van Eerden,
1989). Our results suggest that females may migrate farther south
during the winter because they simply cannot cope with the local environmental
conditions.
Second, a number of studies have demonstrated that there is usually a
clear-cut relationship between diving capacity (maximum depth reached and
aerobic dive limit) and body mass, with larger animals having a higher diving
capacity (Schreer and Kovacs,
1997; but see Boyd and Croxall,
1996). This may account for the observed differences between males
and females; males may be better able to exploit prey in deeper water due to
an increase in available time at depth. Note that this does not mean that CPUT
is higher at greater depths; indeed, Grémillet
(1997) showed that, even if
gender effects are eliminated, this is not the case. Rather, males may be able
to allocate a greater proportion of their dive time to searching and/or
handling prey (cf. Wilson et al.,
1996) than females, rather than engaging much time in transit
between the surface and the preferred foraging depth
(Kramer, 1988).
Utility of our model for the study of other diving endotherms
There are specific limitations to our model if we wish to expand it to
other cormorant species because heat flux to the water in diving cormorants is
not solely determined by water temperature and water depth, but also to a
major part by plumage air volume and body temperature of the bird (see
Grémillet
et al., 1998b).
All empirical and theoretical assessments of plumage air volume confirm the
extremely reduced plumage air volume in great cormorants, which was used in
this model
(Grémillet
et al, 1998b; Rijke,
1968; Wilson et al.,
1992). This morphological characteristic is considered typical for
all P. carbo subspecies, so that general application of our findings
to this species appears reasonable
(Johnsgard, 1993). However, it
is still unclear the extent to which plumage is wettable in other cormorant
species. The blue-eyed shag, for example, which dives to depths of more than
100 m in water at about 4°C for extended periods and has a mean body mass
of 2700 g (Croxall et al.,
1991), would presumably be unable to survive in subantarctic and
antarctic waters without a completely different plumage.
Great cormorants have been shown to maintain constant body temperature,
even when swimming for extended periods in cold water
(Grémillet
et al., 1998b, Grémillet,
unpublished data). An important assumption in the above calculations is that
in great cormorants the difference between water temperature and body
temperature remains constant during a dive bout. However, other seabird
species such as the bank cormorant (Phalacrocorax neglectus), the
blue-eyed shag, or the king penguin (Aptenodytes patagonicus) have
highly variable body temperatures (Bevan et
al., 1997; Handrich et al.,
1997; Wilson and
Grémillet, 1996), with body
temperature sinking during a foraging bout, which reduces the temperature
differential to the water and heat losses from the bird's body.
Conclusions
Most studies of diving endotherms focus on diving behavior per se and
particularly on the diving performance of the animals considered (e.g.,
Boyd and Croxall, 1996;
Charrassin et al., 1998;
Gales and Mattlin, 1997;
Kooyman et al., 1992;
Le Boeuf et al., 1988;
Wilson et al., 1991). The
unexpected ability of aquatic birds and mammals to spend prolonged periods at
depths and to cope with adverse abiotic conditions (i.e., limited oxygen
supplies, high pressure and viscosity, the substantial cooling effect of
water) therefore remain major topics
(Andrews et al., 1997;
Butler and Jones, 1997;
Carbone et al., 1996;
de Vries and van Eerden, 1995;
Shaffer et al., 1997;
Stephenson et al., 1989), with
particular effort being made to assess the energy expenditures related to this
unusual way of life (de Leeuw,
1996; Dolphin,
1987; Stephenson,
1994; Woakes and Butler,
1986). However, beyond these physiological considerations, the
actual benefits accrued by aquatic foragers and thus their overall foraging
efficiency, as well as its link to particular foraging tactics, has been
seldom addressed (but see Bost et al.,
1997; Costa et al.,
1989). This is mainly due to technical difficulties encountered
when assessing prey intake rates in these cryptic and highly mobile aquatic
predators (Duffy and Jackson,
1986; Wilson et al.,
1995). Unfortunately, despite advances, we have a biased
perception of their foraging energetics because we tend to underestimate the
importance of behavioral flexibility in these predators and their capacity to
compensate for substantial energy expenditures. In this respect, it is
striking that even in our model species, the great cormorant, which represents
a radical case of a poorly insulated, marine, warm-blooded predator, flexible
foraging techniques and the exploitation of high-density prey patches may
apparently easily balance substantial heat losses encountered when diving in
deep, cold waters.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This study was supported by the Institut für Meereskunde Kiel and the Arbeitsamt Kiel.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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