Year-round recordings of behavioural and physiological parameters reveal the survival strategy of a poorly insulated diving endotherm during the Arctic winter
1 Centre d'Ecologie et Physiologie Energétiques, Centre National de
la Recherche Scientifique, 23 Rue Becquerel, 67087 Strasbourg Cedex 02,
France
2 French Polar Institute Paul-Emile Victor, Technopôle Brest-Iroise,
BP 75-29280 Plouzané, France
3 School of Biosciences, The University of Birmingham, Edgbaston, Birmingham
B15 2TT, UK
* Author for correspondence (e-mail: david.gremillet{at}c-strasbourg.fr)
Accepted 20 September 2005
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Summary |
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Key words: body temperature, data logger, diving, ecophysiology, great cormorant, Phalacrocorax carbo, heart rate, polar night
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Introduction |
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Seabirds and marine mammals are nonetheless successful apex predators in
Arctic and Antarctic food webs for two reasons. (1) They show extensive
morphological adaptation enabling them to reduce heat losses. Polar marine
mammals are large and accumulate subcutaneous fat layers, whereas polar
seabirds are protected by their waterproof plumages
(Wharton, 2002). (2) They
exploit highly profitable food resources and easily balance their costly way
of life (van Franeker et al.,
1997
).
Arctic great cormorants Phalacrocorax carbo do not conform to this
evolutionary mainstream. Great cormorants are diving, fish-eating birds that
originate from the tropics (van Tets,
1976). They have a partially permeable plumage and the highest
metabolic costs of diving among endotherms (Grémillet et al.,
2003
,
2005a
). Despite these
handicaps, great cormorants have colonized a wide range of climatic zones
ranging from equatorial Africa to northwest Greenland. In Greenland a small
population breeds and over-winters along the West coast, north of the polar
circle (Boertmann and Mosbech,
1997
; Lyngs,
2003
). Recent findings indicated that this population feeds on
both quantitatively and qualitatively modest prey resources
(Grémillet et al.,
2004
). We studied Greenland great cormorants as a model species of
a polar diving endotherm, which does not minimize its heat losses to the
water, nor exploits highly rewarding prey patches. This bird nonetheless copes
with very low temperatures for extended periods.
Former studies showed that Greenland great cormorants do not have
abnormally high food requirements during the summer period
(Grémillet et al.,
1999a). They compensate for their high foraging costs by reducing
the total time spent in the water (temperature
5°C) and this strategy
seems to be based upon a predatory performance (the amount of food gathered
per unit time) that is 10-30 times higher than that of other diving birds
(Grémillet et al.,
2001
). During the winter period they are thought to employ the
same strategy, i.e. a drastic reduction of time spent diving when the water is
cold. However, field observations were only performed towards the end of the
winter (Grémillet et al.,
2001
), so how the birds survive during the coldest months of the
year, during which they are routinely exposed to water temperatures less than
0°C and air temperatures less than -20°C, was unknown.
Using miniature data loggers, we performed year-round recordings of diving activity, heart rate and abdominal temperature in free-ranging male great cormorants from Greenland. We also determined the body composition of individuals at the end of the winter phase.
These empirical data and the output of an energetics model allowed us to test the hypotheses that Greenland great cormorants survive the Arctic winter because of (1) physiological adjustments: they adopt a lower metabolic state, expressed by markedly lower body temperatures and heart rates levels; (2) behavioural adjustments: they reduce the time spent searching for fish in cold water.
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Materials and methods |
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All experiments were conducted by trained veterinary personnel under permits of the ethics committee of the French Polar Institute, The Arctic Station Godhavn (Copenhagen University), the Danish Polar Center, the Danish veterinary administration, and the Greenland Home rule Government.
Analysis of ecophysiological data
Recorded heart rate, depth and temperature data were visualized and
analysed using Multitrace (Jensen Software Systems, Laboe, Germany). The
recordings provided information about the behavioural and the physiological
status of the birds. We discarded the first month of recordings to ensure that
the implanted cormorants had fully recovered from the surgery. We then
performed a general analysis using the entire data set (data recorded every
second day), and a more detailed analysis using data for every eighth calendar
day (i.e. every fourth recorded day). Daily averages were calculated for
different variables using the individual birds as the sampling unit.
General analysis
We assessed two variables every second calendar day.
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Body composition analysis and estimation of fasting endurance
Five great cormorants that had accidentally drowned in gill nets off Disko
in April 2000 were weighed (±1 g) and stored in sealed plastic bags at
-18°C until analysis. After thawing, the birds were plucked and weighed
again (±1 g). Leg and pectoral muscles, liver and abdominal fat
deposits were dissected and weighed (±0.01 g). These body compartments
and the remaining carcass were freeze-dried to constant mass and then ground
under liquid nitrogen. Prior to biochemical analysis, powdered samples were
freeze-dried again to eliminate traces of water. Protein concentrations were
obtained using the Kjeldahl method
(Campbell and Leatherland,
1980) and total lipids according to a gravimetric method using a
chloroform/methanol solution (2/1, v/v) as the extraction mixture
(Folch et al., 1957
).
Reproducibility between duplicate measurements was 1.1±0.2% (proteins)
and 0.7±0.1% (lipids).
Fasting endurance was estimated by first calculating the amount of
available energy from body lipid and protein masses that could be metabolized
during a prolonged but reversible fast in lean animals (95% and 25%,
respectively; Belkhou et al.,
1991) and from their caloric equivalents (39.3 and 18.0 kJ
g-1, respectively;
Schmidt-Nielsen 1990
).
Secondly, the maximal sustainable duration of fasting was estimated in each
bird using an iterative procedure integrating daily body component losses
according to Boos et al.
(2005
). To achieve this, we
assumed that the field metabolic rate averaged 12 W kg-1
(Grémillet et al.,
2003
); that in such fasting lean animals, lipids and proteins
accounted for 75 and 25% of the energy expenditure until
of lipid
reserves were used and for 63 and 37%, respectively, when the fast was further
prolonged (Belkhou et al.,
1991
; Cherel and Groscolas,
1999
); and that the hydration of the lean mass was 76±1%
(this study).
Energetics modeling
Using an algorithm detailed in Grémillet et al.
(2003) we calculated (1) the
theoretical daily food intake of the great cormorants studied, and (2) the
theoretical catch per unit effort (CPUE, expressed as gram fish caught per
minute spent underwater) required to achieve this daily food intake. This
theoretical CPUE therefore does not reflect the actual foraging performance of
the bird, but the minimal foraging success that is required to balance the
energy budget. Calculations were only performed for the periods during which
birds were not breeding and we assumed that the birds' body reserves were in a
steady state. Data recorded by the HRDLs provided most input values. Day
lengths were downloaded from
http://aa.usno.navy.mil/data/docs/RS_OneYear.html#formb.
Water temperatures were taken from the Arktisk Station database
(http://www.nat.ku.dk/as/indexuk.htm).
Birds were assumed to weigh 3.5 kg (the average body mass of birds when they
were implanted) while the average calorific value of the fish was assumed to
be 4.0 kJ g-1 (Grémillet
et al., 2004
). Assimilation efficiency, swim speed and time spent
wing-spreading per day were assumed to be as specified in Grémillet et
al. (2003
).
Abdominal temperatures of resting birds showed a limited, yet significant
decline during the winter phase (see Results,
Fig. 4A). To estimate the
amount of energy saved through this decrease in body temperature, we
calculated the thermal conductance (W m-2 °C-1) of
great cormorants resting in air using input data from Storch et al.
(1999). Heat losses (W) were
then determined: (1) for a bird with stable body temperature equivalent to the
average abdominal temperature in September; and (2) for the actual abdominal
temperatures measured throughout the winter months. The difference between (1)
and (2) gives the amount of energy (W) that might be saved via a
reduction of body temperature during the winter months. Calculations were
performed for birds resting during the active and the non-active phases. Using
time budget information, assimilation efficiency of the birds, and calorific
value of their prey, output values were then converted into the amount of
energy (kJ day-1) and fish (g day-1) saved per day.
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Results |
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All devices were recovered, but only seven provided recordings on all three channels. The retrieved units were surrounded by a very limited volume of scar tissue, indicating that thermal insulation of the loggers did not vary through time. Three data loggers ran for a whole year, while the four others recorded data for 10, 9, 8 and 7 months. We analysed the 210 million data points recorded by all seven devices. Fig. 1 shows examples of depth, heart rate and abdominal temperature traces.
Behaviour
Knowledge of the breeding phenology
(Salomonsen, 1967;
Lyngs, 2003
) and winter
observations (Grémillet et al.,
2001
) allowed us to set four temporal phases
(Fig. 2): (1) July-August,
which is the chick-rearing phase at the breeding site on Disko; (2) September
to April, which is the non-breeding phase, spent south of the Disko Bight
(Grémillet et al.,
2001
); (3) May, which is when the birds return to Disko to mate;
(4) June, which is the incubation period during which the work is shared by
both partners.
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Average dive depth increased gradually from 6 m to
18 m between
July and April (
2=158.7; d.f.=1,6; P<0.001),
falling rapidly during May 2003, to reach 2-3 m in early June 2003
(Fig. 3). Dive duration
(average 42±13 s, range 10-60 s)followed a similar upward trend
(
2=33.5; d.f.=1,6; P=0.001), from
20 s to
60 s between July and April. Dive to pause ratio was consistently
>1.0, demonstrating that birds were spending more time underwater than at
the water surface when foraging (average 1.36±0.25, range 1.0-2.1).
This ratio decreased significantly throughout the winter period from 1.9 to
1.1 (
2=21.3; d.f.=1,6; P=0.003), as dive depth
increased.
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Daily flight time varied between 25-160 min day-1 (average
78±28 min day-1), with flight activity being highest during
chick provisioning (124±28 min day-1) and lowest during the
polar night (55±8 min day-1) and the incubation period
(38±9 min day-1). Between September and April there was,
therefore, a significant, positive relationship between daily flight time and
day length (2=18.7; d.f.=1,6; P=0.005).
Physiology
Average abdominal temperatures of birds resting on land during the active
(10.00-15.00 h) and the non-active (02.00-05.00 h) phases
(Fig. 4A) decreased gradually
between September and March (2=52.5; d.f.=1,6;
P<0.001 and
2=53.4; d.f.=1,6; P<0.001,
respectively). The average temperature decrease between the beginning and the
end of this period was 0.78°C for resting during both the non-active and
active phases. Following this slow, minor decline, resting temperatures
dropped markedly in April and May (Fig.
4A). Original temperature levels were restored in June
(Fig. 4A). Mean abdominal
temperatures of diving birds followed a similar pattern and decreased on
average 0.65°C between September and March (
2=18.1;
d.f.=1,6; P=0.005). Markedly lower values were only observed in May
(Fig. 4B). In diving birds the
lowest abdominal temperatures were recorded immediately after a dive bout (see
Fig. 1). These temperatures
also decreased gradually between September and April (
2=34.1;
d.f.=1,6; P=0.001), with an average change of 1.22°C between the
beginning and the end of the period (Fig.
4B). Mean drop in abdominal temperature while diving
(
T, calculated between the beginning and the end of a dive
bout, see Materials and methods) ranged from 0.4°C to 1.9°C
(Fig. 4C).
T
increased significantly throughout the winter months (
2=15.4;
d.f.=1.6; P=0.008), and there was a significant, positive correlation
between
T and average dive depth (
2=27.0;
d.f.=1,6; P=0.002).
Mean heart rate at the bottom of dives (the lowest heart rates during the
dives) varied between 90-190 beats min-1
(Fig. 5A), and was negatively
correlated with dive depth, therefore decreasing throughout the winter phase
(2=28.6; d.f.=1,6; P=0.002). Mean heart rate at the
water surface ranged from 330-380 beats min-1
(Fig. 5A), with no significant
variation during the winter period (
2=2.3; d.f.=1,6;
P=0.182). Mean heart rate during resting on land varied between
50-100 beats min-1 for non-active phase and between 47-152 beats
min-1 for the active phase (Fig.
5B). Neither level changed significantly during the winter period
(
2=5.6; d.f.=1,6; P=0.056 and
2=3.0;
d.f.=1,6; P=0.134, respectively), but fell abruptly during the second
half of April 2003 (Fig.
5B).
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Body composition
Body composition of the five great cormorants carcasses gathered off Disko
in April 2000 revealed that birds were extremely lean, with average lipid
proportion of only 4.6±1.6% (4.1±0.9% lipid for the liver,
3.0±0.4% for the muscles and 17.3±8.5% for abdominal fat pads).
The lipid/protein ratio averaged 25.2±9.1%. Leg muscle proteins
accounted for 13.9±0.4% of the total protein mass and pectoral muscles
for 16.1±0.6%. Mobilisable energy reserves were of 7802±2081 kJ,
in which proteins represented 33.8±7.8%. The estimated fasting
endurance based upon these reserves was 2.8±0.8 days (range 2-4
days).
Food intake and foraging efficiency
Theoretical daily food intake for great cormorants wintering in Greenland
was 1170±110 g (range 950-1460 g between September and April). To
gather this quantity of food, birds required a theoretical foraging efficiency
of 41±15 g fish min-1 spent underwater (range 22-80 g
min-1). Foraging efficiency was positively correlated with day
length (F1,28=15.7, P<0.0001,
Fig. 6), with lowest average
foraging performances achieved during the polar night (28±4 g
min-1). The theoretical amount of energy saved via lower
abdominal temperatures at rest was between 1-25 kJ, which represents between
0.3-8 g of fish (i.e. less than 1% of the average theoretical food
intake).
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Discussion |
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Even if highly relevant, year-round recordings of ecophysiological
parameters are particularly challenging in diving animals because of technical
constraints and, more importantly, because of the potential handicap caused to
the animal. For instance, archival tags attached externally to diving
predators disrupt their hydrodynamic properties, and therefore jeopardize
energy balance and survival
(Ropert-Coudert et al., 2000).
External data loggers deployed in polar areas can also initiate icing on the
body of the animals, and create an additional handicap
(Kooyman and Ponganis, 2004
).
In order to study the adaptations of great cormorants to the Arctic winter, we
therefore chose to equip them with miniature data loggers placed inside the
abdominal cavity.
All birds bred normally after being implanted, as well as in the subsequent
year after the devices had been removed. 2-year resighting success was also
higher than in control birds marked with metal rings. Arctic winter conditions
put high selection pressure on great cormorants (see later), so the fact that
all birds studied survived the winter phase and reproduced successfully,
indicates that our method did not create a significant handicap. Recent
studies in eider ducks Someteria mollissima and macaroni penguins
Eudyptes chrysolophus, which used similar technology, came to a
similar conclusion (Guillemette et al.,
2002; Green et al.,
2004
).
Unlike most diving birds, great cormorants have a partly permeable plumage
and therefore do not appear to be morphologically designed to survive the
Arctic winter (Grémillet et al.,
2005a). We hypothesized that they show specific physiological and
behavioural adjustments to this thermal challenge, either in the form of a
depressed metabolism (expressed by lower body temperatures and lower heart
rates), or through a decrease of the time spent in cold water. Interestingly,
our field data do not support either of these hypotheses.
Physiological adaptation?
To reduce energy expenditure when facing thermoregulatory stress,
endothermic animals can allow their body temperatures to fluctuate and follow
that of the environment. By so doing they decrease the temperature
differential between their bodies and surrounding media, therefore minimizing
thermoregulatory costs (McKechnie and
Lovegrove, 2002). Theoretically, great cormorants wintering in
Greenland could display metabolic depression expressed by lower heart rates
and hypothermia when resting on land and/or when diving at sea. On land this
phenomenon would be the equivalent of torpor or hibernation, depending on its
magnitude and duration (Lyman et al.,
1982
; Kortner et al.,
2000
). At sea, birds could also allow their body temperature to
drop during dive bouts to save energy, as shown in bank cormorants
Phalacrocorax neglectus (Wilson
and Grémillet, 1996
) and South Georgian shags,
Phalacrocorax georgianus (Bevan et
al., 1997
). Higher body temperatures could be subsequently
restored using heat dissipated by muscular activity (e.g. wing-flapping,
flight).
Heart rates of resting great cormorants did not vary significantly during
the winter phase (Fig. 5B).
However, the abdominal temperatures of birds resting on land decreased
gradually during this period (Fig.
4A). The overall temperature drop between July and the following
April was <1°C, and average abdominal temperatures remained similar to
those recorded for great cormorants wintering in Europe (40°C for
resting during the active phase, and
39°C for resting during the
non-active phase; see Grémillet et
al., 2003
). Moreover, energetics modelled revealed that the
theoretical amount of energy saved through a temperature drop of 0.78°C
(i.e. the drop in abdominal temperature between September and March recorded
in resting birds) is 25 kJ, which is equivalent to 8 g of fish, and is less
than 1% of the average theoretical daily food intake. We conclude that great
cormorants wintering in Greenland do not save significant amounts of energy
via hypothermia and show no metabolic depression while resting on
land. Substantial adjustments nonetheless occurred in the spring (see later in
Discussion).
The abdominal temperatures of great cormorants while diving and after each
diving session, as well as their heart rates at the bottom of the dives,
decreased significantly during the winter period (Figs
4B,
5A). However, as for abdominal
temperatures and heart rate at rest, these variables were not at their lowest
levels during the most challenging period (November to February). Instead,
they showed a minor, gradual decrease throughout the winter period (Figs
4B,
5A). Markedly lower levels were
only reached for a short period in the spring (Figs
4B,
5A). Decreased abdominal
temperatures in diving birds can be caused by the cooling effect of water
and/or the cooling effect of food in the stomach. During deeper dives the body
insulation of great cormorants (plumage air) is compressed, and heat losses to
the water are higher (Grémillet et
al., 1998; Grémillet et
al., 2005a
). The fact that abdominal temperature of diving great
cormorants is lower in the spring than during the winter period could
therefore caused by deeper dives (Fig.
3).
The ingestion of cold food adds to the overall cooling effect. This is
probably why abdominal cooling is more pronounced after a dive bout than
during a dive bout: this latency corresponds to the time required for the
cooling effect of cold food to reach from the stomach into the rest of the
abdomen. Re-examination of abdominal temperature recordings performed in
gentoo penguins Pygoscelis papua (fig. 1 in
Bevan et al., 2002) and in
macaroni penguins Eudyptes chrysolophus (fig. 1 in
Green et al., 2002
) revealed
similar patterns, whose true cause (ingestion of cold food) might have been
previously overlooked. In diving birds feeding on ectothermic prey it is
consequently difficult to tell whether abdominal cooling corresponds to actual
body cooling towards the water, or towards the stomach. Let us nonetheless
assume that in Greenland great cormorants this cooling affects the whole of
the bird's body, and is entirely dedicated to energy saving by reducing the
difference in temperature between the bird's body and the water.
The average abdominal temperature of great cormorants diving in Greenland
was 0.65°C lower in April than it was in September. A thermodynamics model
(Grémillet et al.,
1998) indicates that such body cooling results in energy savings
of
2 W. Assuming that our bird spends 60 min per day in the water (this
was the overall average in this study), this converts into an energy saving of
7.2 kJ. Assuming an assimilation efficiency of 78%, and an average calorific
value of the prey of 4 kJ g-1 (see Materials and methods), this
means that a drop of 0.65°C in body temperature while diving allows the
bird to save
2.2 g of fish per day (less than 0.5% of the theoretical
daily food requirements). Great cormorants wintering in Greenland are thus
unlikely to save substantial amounts of energy via body cooling when
they are in the water. This conforms to former studies of captive great
cormorants, which showed that birds kept high, stable abdominal temperatures
even when diving in 1°C water, as long as they were not fed with cold fish
(Grémillet et al.,
2003
).
We therefore conclude that Greenland great cormorants showed no sign of metabolic depression during the coldest months of the year, thus excluding this mechanism as a means of making significant energy savings.
Behavioural adaptation?
The great cormorants that breed on Disko Island (70°N) winter south of
the Disko Bight (69°30'N;
Salomonsen, 1967;
Lyngs, 2003
). As they move
from their breeding sites to their wintering quarters in early September,
birds seem to encounter favourable feeding conditions. They show limited
foraging effort (and therefore high theoretical foraging yield) at depths of
less than 10 m (Fig. 3) and
spend only
30 min in the water every day
(Fig. 2). Reduced foraging
effort is also possible because they have stopped providing their chicks with
food (they were still spending 1-2 h in the water every day in August, the
late rearing-phase, see Fig.
2). High foraging efficiencies and relatively brief swimming
periods are also observed towards the end of the winter phase (March-April,
see Fig. 2). Data collected
over these limited time periods could therefore support the prediction that
these poorly insulated endotherms maximize their foraging efficiency and
minimize their foraging effort to survive the Arctic winter
(Grémillet et al.,
2001
). Our recordings performed throughout the winter phase show
that this assertion is not correct. Indeed, foraging effort increased markedly
between September and December, to reach its maximum levels during the coldest
and darkest months of the year (December to February). Time spent swimming
averaged 73±19 min day-1 during that phase, and was
therefore similar to the foraging effort of birds provisioning small chicks in
July (Fig. 2;
Grémillet et al.,
2001
).
Hence, we demonstrate that great cormorants wintering in Greenland do not
reduce their foraging time to compensate for heat losses to the colder water.
Foraging effort rather seems to be conditioned by varying light levels, with
foraging efficiency being lowest during the polar night
(Fig. 6; see also
Grémillet et al.,
2005b), resulting in an increase in foraging time
(Fig. 2). Birds also had to
work harder to catch sufficient fish during that period, because of greater
foraging depths (Fig.
3).Increased dive depth, which could be due to gradual prey
depletion, results in higher diving effort due to increased transit costs,
while the elevated hydrostatic pressure reduces plumage air volume and thermal
insulation in diving birds, causing even more pronounced heat losses to the
water (Grémillet and Wilson,
1999
).
On the edge of starvation
During the Arctic winter, great cormorants are under considerable
environmental stress, for which they do not compensate by way of major
physiological adjustments (Figs
4,
5) or by a decrease in their
daily foraging time (Fig. 2).
Their theoretical daily food intake is consequently very high (1170 g
day-1), twice as much as for great cormorants wintering in Europe
(Grémillet et al.,
2003). Birds could partly cover their energy requirements using
body reserves. We nonetheless think that the input due to body fuels is
relatively limited because: (1) surgical procedures performed during the
summer period revealed that birds had very low adiposity; (2) individuals
wintering in Greenland showed regular foraging activity
(Fig. 2), indicating that they
could not rely on fasting to overcome difficult periods such as the polar
night (Grémillet et al.,
2005b
); (3) discussions with local Inuit hunters also suggested
that the great cormorants hunted within our study zone remain lean year-round.
Limited fat deposits might nonetheless have been used to subsidize their
energy budgets and allow their survival. Thus, our daily food intake estimates
must be treated with caution, and further investigations are required to
determine the adiposity of Greenland great cormorants throughout the winter
period.
The present study shows that great cormorants are running out of body
reserves towards the end of the Arctic winter (April). Their adiposity is then
well below published values for other bird species at their annual minimal
adiposity (Johnston, 1970;
Piersma, 1988
). The overall
physiological status (adiposity, lipid/protein ratio) of great cormorants is
then comparable to that of a fasting animal in between phase II and phase III
of the fast (as defined by Belkhou et al.,
1991
; Cherel et al.,
1994
), and their remaining body reserves would only allow them to
survive for approximately 3 days without food.
Just as their body reserves are presumably at their lowest level (in late
April), the birds show drastic physiological changes in the form of low body
temperatures when diving and resting, and of markedly lower heart rate levels
when resting (Figs 4,
5B). These modifications
indicate a depressed metabolism, which can either be seen as a state of
metabolic stress caused by the exhaustion of body reserves (see above), and/or
as a physiological state permitting the fast accumulation of new body reserves
via reduced energy expenditure
(Butler and Woakes, 2001). Such
major changes occur just before/as birds move back to their breeding sites on
Disko Island, where they start to mate in May (see Results and
Fig. 2). This seems to be a
particularly challenging time for male great cormorants, maybe even more
challenging than the polar winter itself. Beyond the physiological shifts
described above, birds in May show the highest foraging effort ever recorded
for this species, with up to 4 h spent in the water per day
(Fig. 2). Suchhyperactivity
relates well with the potential accumulation of new body reserves at the onset
of the breeding season. This behaviour might be favoured by the occurrence of
vast capelin Mallotus villosus stocks within the foraging zone of the
birds. Millions of capelin aggregate in coastal waters off Disko Island in May
and spawn along gravel beaches in June
(Friis-Rødel and Kanneworff,
2002
). The foraging depths of great cormorants in May (
8 m)
and June (
3 m) correspond to the distribution of capelin during these
periods (E. Friis-Rødel, personal communication), suggesting that birds
might benefit from this bounty to restore their body reserves at the onset of
the breeding season.
Conclusions
Year-round recording of ecophysiological variables in great cormorants from
Greenland have allowed us to end the speculation concerning their potential
physiological or behavioural adaptations to the Arctic winter and to define
their energetic strategy. When facing very low air and water temperatures
between November and March, birds did not respond by way of major
physiological adjustments (i.e. low metabolism and associated low body
temperatures). Nor did they minimize the time spent swimming in cold water.
Birds probably metabolised their limited body reserves to cope with winter
conditions, getting into a physiological status comparable to the end of phase
II of a fast. However, more than anything else, they survived by sustained
high feeding activity, with an estimated catch of 1170 g of fish per day.
Previous investigations indicated that great cormorants wintering in Northern
Europe require 670 g of food per day (range 440-1100 g day-1;
Grémillet et al.,
2003
). It appears therefore that birds from Greenland routinely
ingest the quantity of fish, which was, up to the present, supposed to be the
maximum food intake for wintering great cormorants or great cormorants raising
large chicks (Grémillet et al.,
2003
). These very high feeding regimes occur throughout the winter
phase, even during the polar night (December and January).
With respect to the management of the expanding European great cormorant
populations, which have been accused of depleting valuable freshwater stocks
(Carss, 2003), two important
conclusions can be drawn. (1) Even when facing some of the most drastic
weather conditions on earth, great cormorants do not seem to require more food
to survive than the maximum food intake predicted for aquatic birds; (2)
contrary to previous suggestions, however, birds do not reduce their foraging
effort as ambient conditions deteriorate
(Grémillet et al.,
2001
). Rather, they respond to environmental constraints
via an increase in their daily food intake. By doing so they might
ingest a third of their body mass of fish every day for prolonged periods.
Our study underlines the original adaptation of great cormorants to the
high Arctic environment. These unusual birds survive particularly harsh winter
conditions despite their limited body insulation and body reserves, thereby
breaking the paradigm that efficient thermal insulation is a prerequisite to
the colonization of polar ecosystems by endotherms
(Grémillet et al.,
2001). Our measurements also demonstrate the great variability of
the behavioural and the physiological responses of a free-ranging animal
during the annual cycle (Figs
2,
3,
4,
5,
6), and underline the
limitations of field investigations conducted during limited time frames, e.g.
during the breeding period.
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References |
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