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First published online December 14, 2007
Journal of Experimental Biology 211, 1-8 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.005785
Review |
Energy saving processes in huddling emperor penguins: from experiments to theory
IPHC-DEPE, UMR 7178; Centre National de la Recherche Scientifique, Université Louis Pasteur, 23 rue Becquerel, 67087 Strasbourg, France
* Author for correspondence (e-mail: caroline.gilbert{at}c-strasbourg.fr)
Accepted 3 October 2007
 |
Summary |
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 TOP Summary IntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
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Key words: huddling, emperor penguin, energetic benefit, wind protection, microclimate, body temperature
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Introduction |
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TOPSummaryIntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
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). Males
and females fast for 45 days during the pairing period, and males fast another
70 days to assume the incubation task
(Prévost, 1961;
Isenmann, 1971), during which
their body temperature has to be constant and high in order to maintain their
egg at 35°C (Prévost,
1961; Prévost and
Sapin-Jaloustre, 1964; Boyd and
Sladen, 1971; Le Maho et al.,
1976; Pinshow et al.,
1976; Groscolas,
1986; Gilbert et al.,
2007). Although they are adapted to minimize heat loss
(Le Maho, 1977), energetically
costly heat production mechanisms must be activated because ambient
temperatures are always below their lower critical temperature
[TLcrit: –10°C
(Le Maho et al., 1976;
Pinshow et al., 1976)].
Breeding success then relies on the males' ability to make economic use of
their body fuels. Pioneering studies suggested that huddling is the key factor
for emperor penguins to protect themselves against cold and lower their energy
expenditure in order to survive their 4-month breeding fast during the
Antarctic winter (Cendron,
1952; Stonehouse,
1953; Prévost,
1961). Similarly, many studies on small mammals support the view
that huddling efficiently decreases metabolic heat production and maintenance
cost by 10–40% (Pearson,
1960; Gorecki,
1968; Gebczynski,
1969; Gebczynska,
1970; Fedyk, 1971;
Tertil, 1972;
Glaser and Lustick, 1975;
Stanier, 1975;
Alberts, 1978;
Martin et al., 1980;
Andrews and Belknap, 1986;
Yahav and Buffenstein, 1991;
Perret, 1998).
According to heat transfer physics, for any animal heat losses equivalent
to metabolic rate in a thermal steady state are dependent on the gradients
between the external temperature and its body temperature. These gradients,
moreover, depend on the cold-exposed body surface area and the thermal
conductance of the animals (Scholander et
al., 1950). Small animals closely packed together reduce their
body surface area exposed to the cold, contributing to energy savings
(Contreras, 1984;
Canals et al., 1997). Small
mammals possess a high surface:volume ratio, leading to important heat losses
compared with their metabolic heat production, and the reduction in
cold-exposed body surface area is estimated to account, on average, for
58–94% of the huddling energy savings of small rodents, depending on the
number of individuals involved and on the density of the group
(Canals et al., 1997). A second
process involved in energy savings is the increase in temperature surrounding
the grouped animals, which decreases heat losses by reducing the gradients
between external and body temperatures. A 5°C increase in ambient
temperature caused by huddling short-tailed field voles Microtus
agrestis accounted for 55% of the energetic benefits during huddling
(Hayes et al., 1992). A third
mechanism explaining energy savings relies on adjustments in body temperatures
of huddling animals (Vickery and Millar,
1984): huddling mammals and birds maintain a higher and more
constant body temperature than isolated ones, suggesting that huddling is used
as a warming mechanism (Stanier,
1975; Howell,
1976; Alberts,
1978; Andrews et al.,
1987; Yahav and Buffenstein,
1991; Boix-Hinzen and
Lovegrove, 1998; McKechnie and
Lovegrove, 2001; Bautista et
al., 2003; Cutrera et al.,
2003). However, other biological models lower their body
temperature during huddling bouts, presumably allowing them to maximize their
energy savings through a reduction of their metabolic heat production. For
example, great snow geese goslings Chen caerulescens atlantica lower
their body temperature during huddling by 0.8°C
(Fortin et al., 2000).
Similarly, mouse lemurs Microcebus murinus nesting in pairs increase
the duration of their hypothermic bouts compared with males nesting alone
(Séguy and Perret,
2005).
With respect to the emperor penguin, no study has yet evaluated the
respective parts of processes such as the reduction in cold-exposed body
surface area and the increase in temperature surrounding the grouped animals
and body temperature adjustments, in their energy savings during huddling.
Emperor penguins face thermal trade-offs that are different from small
mammals. Breeding male emperor penguins weigh on average 30 kg and are 1.2 m
tall (Prévost, 1961),
and thus possess a relatively low surface:volume ratio. Furthermore, they are
highly insulated and adapted to reduce any heat loss
(Le Maho, 1977). Hence,
reduction in their cold-exposed body surfaces may make a lesser contribution
to the energy savings permitted by huddling, compared with small animals.
Variations in body temperature of emperor penguins should also be limited by
the inertia inherent to their significant body mass. The warmth created inside
huddles was actually considered by pioneer authors to be the only mechanism
explaining energy savings observed in huddling emperor penguins
(Prévost, 1961;
Jouventin, 1971;
Jarman, 1973;
Le Maho, 1977), and the
reduction in cold-exposed body surface area during huddling and any consequent
body temperature adjustment was neglected. However, it was hypothesized that
huddling penguins may save energy through a lowering of their body temperature
(Ancel et al., 1997). In
support of that, pioneering studies reported that the rectal temperature of
huddling free-ranging birds was 1°C lower than in captive birds held in
small groups and 2°C lower than in captive birds held in isolation, even
though they all experienced similar climatic conditions within the general
colony area (Prévost,
1961; Prévost and
Sapin-Jaloustre, 1964; Mougin,
1966).
Recent studies by our group provide new insights into this complex social
behaviour and its related physiological mechanisms
(Gilbert et al., 2006;
Gilbert et al., 2007),
permitting an exploration of the respective contributions of these processes
to huddling energetics. Throughout their breeding cycle, males huddle, i.e.
are packed together, on average 38% of their time
(Gilbert et al., 2006), and
experience ambient temperatures within their thermoneutral zone thanks to
grouping [from –10°C to +20°C
(Le Maho et al., 1976;
Pinshow et al., 1976)]. In
parallel, their body temperature is adjusted during the breeding cycle: it
decreases by 1.7°C over the pairing period, and is maintained during
incubation. Overall, the body temperature of free-ranging birds during their
breeding cycle averages 36.7°C
(Gilbert et al., 2007).
Furthermore, birds engaged in particularly tight huddles do not show any sign
of hyperthermia. We have suggested, based on the heat transfer physics, that
birds saving energy over their winter fast enter a metabolic depression during
huddling, the extent of which depends on the reduction of their body surface
area exposed to the cold (Gilbert et al.,
2007).
|
).
Based on this, some studies
(Prévost, 1961;
Prévost and Sapin-Jaloustre,
1964; Ancel et al.,
1997) estimated the overall energetic benefits of huddling in
emperor penguins, comparing body mass losses or estimated metabolic rates of:
(1) `isolated' birds, fenced in at the colony; (2) `loosely grouped' birds,
restrained in small groups of 5–10 birds fenced in at the colony but
unable to huddle effectively; and (3) `free-ranging' birds, moving freely
within the colony and able to huddle (Fig.
1). In all studies, isolated and/or loosely grouped birds faced
climatic conditions identical to those of free-ranging birds. Since birds were
able to group themselves when loosely grouped and maintain social interactions
visually and acoustically when isolated, the effect of stress due to captivity
was probably far less than the thermal effects. Isolated birds were unable to
shelter themselves from the wind, in contrast to grouped birds that might
reduce the effect of wind-chill by grouping themselves loosely
(Jarman, 1973). The energy
savings of loosely grouped birds, when compared with isolated ones, could then
be attributed to the fact that grouped birds were able to reduce wind-chill
effects (Fig. 1). In contrast
to free-ranging birds, loosely grouped birds were unable to huddle effectively
and reduce their exposed body surface area by any significant extent. The
energy savings observed in free-ranging birds, when compared with loosely
grouped birds, can be attributed to (1) warming of the temperature around the
birds, (2) reduction in their cold-exposed body surface area while huddling
(Fig. 1), and (3) body
temperature adjustments of free-ranging birds, maintaining lower body
temperatures (Fig. 1), should
form part of their huddling energy savings. The two first mechanisms should be
additive, while the body temperature adjustments should contribute towards
these two processes. Our first aim was to review previous studies investigating the energetic benefits associated with huddling in emperor penguins, by comparing body mass losses and derived metabolic rates of free-ranging, loosely grouped and isolated birds. Estimation of huddling benefits has already been attempted, but results obtained recently enabled us to go further in examining the energy saving mechanisms. We then estimated the respective contributions to the energetic benefit from wind protection, warming of ambient temperatures when birds are not packed, reduced cold-exposed body surface area when birds are packed while huddling, and adjustments of the birds' deep body temperature. In conclusion, these estimations are discussed.
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A review of energy savings comparing isolated, loosely grouped and free-ranging birds |
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TOPSummaryIntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
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; Prévost and
Sapin-Jaloustre, 1964; Ancel et
al., 1997) (Fig.
2). To minimize the impact of stress, body masses of captive birds
were measured after habituation to their enclosure. On average, free-ranging
and loosely grouped penguins lost 132±8 and 178±23 g
day–1, respectively (mean ± s.d.), which represents a
26% reduction in daily body mass loss. Daily body mass loss in loosely grouped
birds was on average 40% lower than in isolated birds (299±8 g
day–1). The overall difference between isolated and
free-ranging birds was 56% (Fig.
2).
|
). Given that emperor penguins in the above studies were in
phase II of their fast [from day 10 to day 100
(Robin et al., 1988)] and that
the composition of the lost body mass was found to be steady under this
condition (61.7% lipids, 5.9% proteins and 32.4% water), the energetic
equivalent of 1 g body mass would be 25.5 kJ
(Groscolas, 1988). Hence,
according to this estimation, metabolic rate of free-ranging huddling penguins
would be reduced by 26%, compared to loosely grouped birds (132 g
day–1
39.0 W and 178 g
day–152.5 W, respectively). Second, an isotopic
dilution method was used to measure the daily changes in composition
(Ancel et al., 1997). Ancel et
al. found that body mass loss was 20% lower in free-ranging birds than in
loosely grouped birds (137 and 171 g day–1, respectively).
The estimated metabolic rate of free-ranging birds (1.5 W
kg–1) was 16% lower than that of loosely grouped birds (1.8 W
kg–1). Based on these two methods, the metabolic rate of
free-ranging birds was calculated to be on average 21% lower than in loosely
grouped birds (42.8±5.3 and 51.9±2.1 W, respectively; mean
± s.d.; Fig. 2). Using
the estimate from Groscolas (Groscolas,
1988), loosely grouped birds had an average metabolic rate 39%
lower than that of isolated birds (88.2 W;
Fig. 2). Hence, the average
reduction in metabolic rate of free-ranging penguins, compared with isolated
birds, was 51%. |
Estimating energetic benefits from wind protection: isolated versus loosely grouped birds |
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TOPSummaryIntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
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;
Guillard and Prévost,
1964; Mougin,
1966) (A.A., unpublished observations) were 4.9±0.9 m
s–1 and –16.6±0.8°C, respectively (mean
± s.d.).
Birds inside a huddling group, even if they are not packed together,
shelter themselves from the wind (Jarman,
1973). Unfortunately no external temperature measurements,
recorded on loosely grouped or isolated birds' backs, are available. We can
estimate the reduction in energy expenditure that a loosely grouped bird will
experience through wind shelter, when compared with an isolated bird
(Fig. 3). The metabolic rates
of emperor penguins have been independently measured using respirometry
(Le Maho et al., 1976;
Pinshow et al., 1976). Both
studies concluded that below an ambient temperature of –10°C (lower
critical temperature, TLcrit), the metabolic rate of
emperor penguins increases as a function of ambient temperature. Pinshow et
al. conducted measurements indoors at various low ambient temperatures but
without wind (Pinshow et al.,
1976). By contrast, Le Maho et al. conducted measurements
outdoors, where penguins were exposed to various low ambient temperatures at
low wind speeds, ranging between 0 and 5 m s–1
(Le Maho et al., 1976). The
resulting increase in metabolic rate at temperatures below –10°C
from these two studies differs slightly, with a steeper slope in the study by
Le Maho et al. (Le Maho et al.,
1976), presumably reflecting the effect of low wind speeds on
metabolic rate.
|
For our investigation, we decided to use the equations given by Le Maho et
al. (Le Maho et al., 1976),
because captive penguins kept outside and grouped loosely most likely still
experience the effects of low wind speeds. Several authors
(Stonehouse, 1967;
Drent and Stonehouse, 1971;
Le Maho et al., 1976;
Taylor, 1986;
Stahel et al., 1987;
Dawson et al., 1999) support
the view that the compact nature of penguin plumage confers a high resistance
to disorganization and penetration by wind, except in strong wind speeds
(>5 m s–1). Consequently, these authors argue that heat
loss by convection is negligible at low wind speeds. Similarly, Chappell et
al. (Chappell et al., 1989)
found that metabolic rate of Adélie penguins increases at high wind
speeds, especially when ambient temperatures are low. The same should be true
for emperor penguins facing wind speeds averaging 4.9 m s–1
at mean ambient temperatures of –16.6°C. Goldstein
(Goldstein, 1983) modelled the
combined effects of low temperatures and wind speeds on the birds'
mass-specific field metabolic rate (sFMRTaV):
 |
 | (1) |
T=Ta–TLcrit of
the birds in °C.
Chappell et al. (Chappell et al.,
1989) measured metabolic rates in Adélie penguins at
ambient temperatures of –20°C, i.e. 10°C below their lower
critical temperature (TLcrit) and wind speed of 5.7 m
s–1, and found values that were even higher than the
metabolic rate predicted by Goldstein's model
(Goldstein, 1983). They
attributed this difference to an increase in heat loss through poorly
insulated flippers. However, the ratio between flipper surface area and whole
body surface area in Adélie penguins is much greater than in emperor
penguins, which are adapted to breed during the Antarctic winter
(Le Maho, 1977).
We therefore applied Goldstein's model
(Goldstein, 1983) to the
emperor penguins exposed to average wind speeds of 4.9 m s–1.
Hence,
 | (2) |
T0.32
(m=30 000 g for a standard incubating male emperor penguin and
T=6.6°C, with Ta=–16.6°C and
TLcrit=–10°C).
sFMRLG can be derived from the established equation
(Le Maho et al., 1976) for
penguins exposed to low winds and Ta from –30°C
to –10°C:
 | (3) |
 | (4) |
 | (5) |
The metabolic rates derived from the above equations are much higher than
the mean estimated metabolic rates calculated from previous studies by,
respectively, 17% for isolated birds and 28% for loosely grouped birds
(Groscolas, 1988;
Ancel et al., 1997)
(Fig. 2). However, the mean
reduction in metabolic rate and body mass loss of birds loosely grouped
compared with isolated ones was 39% and 40%, respectively. This is close to
the 32% reduction estimated using Goldstein's model
(Goldstein, 1983). This
estimate is based on equations that were established from metabolic
measurements of penguins isolated in the laboratory. The higher metabolic rate
estimated using Goldstein's model
(Goldstein, 1983) could
possibly be due to the stress caused by the manipulations. The calculations,
derived from respirometry measurements, would then underestimate the metabolic
rate reduction of loosely grouped penguins compared with isolated birds by 7%.
This could be explained by the fact that we estimated only the thermal
effects, whereas reduction in daily body mass loss
(Prévost, 1961;
Prévost and Sapin-Jaloustre,
1964) encompasses all thermal and additional stress or
physiological effects. In conclusion, emperor penguins able to stay in a
group, even when loosely structured, gain an average thermal and, hence,
energetic benefit of 32%, simply by sheltering themselves from the
wind-chill.
|
Estimating energetic benefits from the warming of ambient temperatures and the reduction in cold-exposed body surfaces: loosely grouped versus free-ranging birds |
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TOPSummaryIntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
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Our rationale assumes, firstly, that the effect of warming ambient
temperatures relies on the increased time that birds spend within their
thermoneutral zone, i.e. when energy expenditure is the lowest. Throughout the
2005 pairing and incubation periods, five male emperor penguins were equipped
with a data logger recording light intensity and temperature (Mk9, Wildlife
Computers, Redmond, WA, USA) glued to their back feathers. From temperature
recordings, we could determine the time spent by birds at temperatures above
–10°C. We could also measure the time they spend huddling tightly,
i.e. are packed together, as the light intensity recorded by the device drops
rapidly to 0 when the birds' back is covered by another individual (for
details, see Gilbert et al.,
2006). Temperature recordings show that males spent on average
only 10±5% of their time exposed to external temperatures lower than
–10°C (i.e. free-ranging, loose grouping; mean ± s.d.;
Fig. 3). Furthermore, they
spent on average 49±5% of their time huddling, being packed (i.e.
free-ranging, tight huddling; mean ± s.d.;
Fig. 3). Then, the remaining
41% of their time was spent without being packed at ambient temperatures above
–10°C, i.e. within their thermoneutral zone, corresponding to a
minimum metabolic rate (i.e. free-ranging, loose huddling;
Fig. 3).
Secondly, we can assume that when birds are huddling, their metabolic rate
is lowered proportionally to the reduction in their cold-exposed body
surfaces. This hypothesis is based on the observation that during bouts of
tight huddling with ambient temperatures above 20°C, free-ranging emperor
penguins not only show no sign of hyperthermia, but also maintain a constant
body temperature, or even lower it by 0.5°C during pairing
(Gilbert et al., 2007). For
tightly huddling birds in close contact with neighbouring birds, thermal
gradients, driving lateral heat loss from the core to lateral surfaces, nearly
vanish. The surface areas exposed to the cold are restricted to the feet, the
upper part of the back, the neck and the head
(Fig. 4). Following heat
transfer physics, tightly huddling penguins must reduce their metabolic rate
by the same extent as the reduction in their cold-exposed body surface areas
in order to maintain or slightly lower their core temperature. If they could
not lower their metabolic rate, the cold-exposed areas might represent thermal
windows for extra heat dissipation. However, this would contradict the fact
that snow accumulates on their heads and upper backs during blizzards
(Fig. 4), and that penguins
must save energy during their incubating task. We thus suggested that they
enter metabolic depression, associated with deep sleep, while huddling tightly
(Gilbert et al., 2007).
Although a clear experimental demonstration of this remains to be done, we do
not see any other possible explanation because all living organisms are
subject to the thermodynamic laws.
|
), and to a calculated value of 6700 cm2 from
Walsberg and King's equation (Walsberg and
King, 1978). The body surface still exposed to cold during
huddling was estimated to be 1649 cm2. The reduction in
cold-exposed body surfaces of huddling emperor penguins would thus be about
74%. To estimate the energetic benefits from the mild ambient temperatures created within the loose huddling group and the reduction in the cold-exposed body surfaces while tightly huddling, we compared the field metabolic rate (FMR) of a free-ranging bird (FMRFR) spending 41% of its time within its thermoneutral zone without being packed and 49% of its time being packed, with the FMR of a loosely grouped bird (FMRLG), which is sheltered from the wind but spends 100% of its time at temperatures below its thermoneutral zone (TNZ).
Mass-specific metabolic rate outside the thermoneutral zone (sFMRLG)
According to Le Maho et al.'s equations
(Le Maho et al., 1976) (see
above):
 |
 | (6) |
Mass-specific metabolic rate within the thermoneutral zone (sFMRTNZ)
The mass-specific metabolic rate when birds are within their TNZ can be
estimated from published respirometry measurements [1.98 W
kg–1 (Le Maho et al.,
1976) and 1.83 W kg–1
(Pinshow et al., 1976]. For
our calculation, we used the 1.98 W kg–1 value
(Le Maho et al., 1976). Hence,
 | (7) |
Mass-specific metabolic rate when birds are huddling (i.e. packed; sFMRH)
Under huddling conditions we estimated that only 26% of the body surface is
still exposed to cold. Following our above assumption, metabolic rate of
huddling birds would be reduced by 74%, compared to that of an isolated bird
exposed to ambient temperatures below its thermoneutral zone. We chose to
consider the metabolic rate of an isolated bird, exposed to wind, as the body
surfaces (head, neck and upper back) still exposed to cold in huddles are
submitted to wind-chill. Hence,
 | (8) |
Estimation of the energetic benefit accrued from warmer ambient temperatures and reduction of cold-exposed body surfaces
The sFMR for a free-ranging emperor penguin (sFMRFR) that spends
10% of its time at ambient temperatures below –10°C, 41% at
temperatures above –10°C (without being packed) and 49% huddling
(i.e. being packed), would be as follows:
 | (9) |
).
Estimation of the energetic benefit accrued from the reduction of cold-exposed body surfaces
In the above calculation, we considered both processes of energy savings,
i.e. exposure to warmer ambient temperatures and reduction in cold-exposed
body surfaces. To evaluate the energy savings due to reduction in cold-exposed
body surfaces only, we compared the field metabolic rates of birds spending
90% of their time within their thermoneutral zone (sFMR0.9TNZ),
with the above calculation of sFMRFR (1.50 W kg–1)
for birds spending 41% of their time within their thermoneutral zone and 49%
of their time packed in huddles:
 |
 | (10) |
; Jarman,
1973), the role of ambient temperatures in energy savings would
thus be of less importance than the reduction in cold-exposed body
surfaces.
We must bear in mind, however, that the above estimates (sFMRFR
and sFMRLG) are based on metabolic rate measurements of captive
birds, even if they were otherwise kept under natural conditions
(Le Maho et al., 1976). These
measurements thus overestimate the energy expenditure of penguins during
breeding on their colony, either when isolated or loosely grouped. Ancel et
al. estimated that the metabolic rate of loosely grouped birds was 1.8 W
kg–1 (Ancel et al.,
1997), which is 25% lower than our estimate of 2.41 W
kg–1. The overestimation of our study, based on Le Maho et
al.'s calculations (Le Maho et al.,
1976), might be explained by the stress caused by the
manipulations, a different physiological status of the birds studied from
birds in the colony, and/or the higher body temperatures of the birds studied
in the laboratory [38.2°C, as determined by stomach temperature
measurements (Le Maho et al.,
1976)]. However, free-ranging emperor penguins maintain a
metabolic rate equivalent to our estimate of 1.50 W kg–1
(Ancel et al., 1997). Thus, we
must consider that the 38% reduction permitted by mild ambient temperatures
and reduction in cold-exposed body surfaces were overestimated due to the 25%
overestimation of the metabolic rate of loosely grouped birds. These
calculations, applied to birds that maintained a higher body temperature, did
indeed overestimate the energy savings due to the reduction in heat loss
gradients. Heat loss gradients between body and external temperatures are
indeed increased if body temperature is higher. Thus, lastly, we had to
estimate the energy savings permitted by physiological adjustments in body
temperature, which should reduce heat loss gradients and thus temporize the
energetic benefits of ambient temperatures and reduced cold-exposed body
surfaces in the above calculations.
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Estimating energetic benefits from body temperature adjustments |
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TOPSummaryIntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
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;
Prévost and Sapin-Jaloustre,
1964; Mougin,
1966) (Fig. 1)].
Lowering deep body temperature is an efficient strategy for decreasing energy
expenditure in birds and mammals [e.g. for birds
(Butler and Woakes, 2001;
McKechnie and Lovegrove,
2002)]. Free-ranging birds have a mean core temperature that is
higher [36.7±0.3°C; mean ± s.d.
(Gilbert et al., 2007)] than
rectal temperatures measured by previous authors
(Fig. 1), except for the
temperature range reported by Groscolas, who measured a mean rectal
temperature of 37.1°C for incubating and huddling birds
(Groscolas, 1986).
Free-ranging birds maintain a body temperature that is adjusted throughout
their breeding cycle: it is lowered when pairing by 1.7°C, and maintained
constant during incubation (Gilbert et
al., 2007). Furthermore, during the short period of egg exchange,
a highly active phase for the pairs, the body temperature of male emperor
penguins significantly increases by 1.2°C, to reach 37.7±0.2°C
(mean ± s.d.) (Gilbert et al.,
2007); this is a body temperature 1°C higher than their mean
body temperature. From newly analysed data, we can also approximate an active
temperature of males before their breeding cycle, i.e. of newly arrived males
on the colony, and after the completion of their incubation. During winter
2005, three males were equipped with body temperature loggers (SMAD,
DEPE-IPHC, Strasbourg, France). Their temperature profiles were similar to our
previous results: lowered during pairing and maintained during incubation at
about 36.9±0.2°C (mean ± s.d.). Moreover, their body
temperature at the beginning of the pairing period was 37.9±0.4°C,
and their body temperature after their incubation, i.e. after they had
exchanged the chick with the female, was 37.5±0.3°C (mean ±
s.d.). Hence, while the emperor penguins' mean body temperature is on average
36.7°C during their breeding cycle, their body temperature at arrival and
after departure from the colony averaged 37.7±0.4°C (mean ±
s.d.). Body temperature adjustments should thus play an important role in the
energy savings of breeding emperor penguins.
Reported mean stomach temperatures of isolated birds measured during
respirometry studies in the laboratory were 37.8°C
(Pinshow et al., 1976),
38.2°C (Le Maho et al.,
1976) and 39.4°C (Dewasmes
et al., 1980). As expected, the measured mass-specific metabolic
rate (measured at rest, within the TNZ) of emperor penguins was positively
correlated with stomach temperature: 1.83 W kg–1
(Pinshow et al., 1976), 1.98 W
kg–1 (Le Maho et al.,
1976) and 2.32 W kg–1
(Dewasmes et al., 1980),
accounting for body mass differences, which were small: 23.4 kg
(Pinshow et al., 1976), 24.8
kg (Le Maho et al., 1976) and
25.0 kg (Dewasmes et al.,
1980). Dewasmes et al. discussed the link between the decrease in
metabolic rate and body temperature decline, since mean stomach temperature in
their birds ranged from 38.5°C to 40.0°C
(Dewasmes et al., 1980). They
suggested that a core temperature decrease of 1°C might reduce metabolic
rate by as much as 40%. However, if we assume an apparent Q10
between 2 and 3, and that ambient temperature and conductance remain equal, a
core temperature decline of 1°C (from 37.7°C to 36.7°C) would
represent a reduction in metabolic rate by about 7–10%
(Heldmaier and Ruf, 1992;
Butler and Woakes, 2001). We
could also use the values from the above studies to plot mass-specific
metabolic rate as a function of body temperature
(Fig. 5). Using this
relationship, a core temperature decline of 1°C between temperatures of
37.7°C (active body temperature) and 36.7°C (observed during the
breeding cycle), would thus represent a metabolic reduction of 17% (from 1.83
to 1.51 W kg–1).
|
;
Prévost and Sapin-Jaloustre,
1964; Mougin,
1966). Assuming that tightly huddling penguins reduce their
metabolic rate to the same extent as the reduction in cold-exposed body
surface area, they run no risk of cooling off or overheating. By contrast, an
emperor penguin in a small group is unable to achieve tight packing densities
and, therefore, to drastically reduce its cold-exposed body surface area. A
decline in metabolic heat production in this case would lead to body cooling
that would jeopardize a successful incubation. Support for this hypothesis
emerges from Prévost's first studies
(Prévost, 1961).
Thyroid glands of free-ranging male emperor penguins were sampled throughout
their breeding cycle, and it was found that the epithelium thickness of these
glands decreased after the arrival at the colony, was minimal from April to
July, and finally increased again in August, when males departed to sea.
Prévost concluded that the thyroid gland, active before arrival, was
likely to be inactive during the males' breeding fast
(Prévost, 1961). As the
thyroid is the major organ stimulating thermogenesis, this implies that active
thermogenesis is somehow depressed during the breeding fast of male emperor
penguins. Furthermore, T3 and T4 plasma levels were reduced during incubation
(Groscolas and Leloup, 1986).
Inactivity of the thyroid gland can be linked to the metabolic depression
occurring during huddling, and also to downregulation of the core temperature
throughout the breeding cycle. Groscolas and Leloup also showed that the
depressed plasma T4 level in incubating males was associated with a low body
temperature, and suggested huddling behaviour as the cause
(Groscolas and Leloup, 1986).
This is consistent with body temperature profiles of breeding male emperor
penguins recorded in the 2005 study. The possible link between huddling
behaviour, reduction in thyroid hormone activity, and a reduced metabolic rate
has also been suggested in reproductively inhibited huddling prairie deer mice
Peromyscus maniculatus bardii
(Cronin and Bradley,
1988). |
Conclusion |
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TOPSummaryIntroductionA review of energy...Estimating energetic benefits...Estimating energetic benefits...Estimating energetic benefits...ConclusionReferences |
|---|
). Indeed, according to the experiment we designed, we
estimated that 74% of cold-exposed body surfaces would be reduced, leading to
a metabolic rate as low as 0.92 W kg–1. This metabolic
reduction occurring in tightly packed birds should, however, be tested,
possibly using infrared thermography images, which would prove that the
remaining cold-exposed body surfaces are not efficient thermal windows to
dissipate heat, and thus that emperor penguins inside huddles enter metabolic
depression.
Moreover, estimations of metabolic reduction due to wind protection, mild
ambient temperatures within groups, and reduction in cold-exposed body
surfaces were performed using metabolic equations designed with captive
penguins that maintained higher body temperatures than birds in the colony. We
thus overestimated the metabolic rate of isolated and loosely grouped birds.
Mass-specific metabolic rates for a standard penguin of 30 kg, isolated and
loosely grouped, would be 2.93 W kg–1 and 1.73 W
kg–1, respectively, according to
Fig. 1. However, the values
found from our calculations are 3.53 W kg–1 for isolated
penguins and 2.41 W kg–1 for loosely grouped penguins. This
represents an overestimation of 17% and 28%. However, the estimated metabolic
rate of free-ranging emperor penguins is close to Ancel et al.'s estimation
(Ancel et al., 1997). This is
partly due to the high percentage of time spent inside huddles, while their
metabolic rate is drastically reduced. Another limit to this study is that all
the processes are linked together. We estimated independently the effect of
wind protection, gained from being loosely grouped. We also assumed that
microclimate warming and reduction in cold-exposed body surfaces benefits
should be additive in huddling benefits. However, energy savings linked to a
downregulation of body temperature should interfere with these three
mechanisms, reducing their contribution through reduced heat loss
gradients.
This study provides new insights into the processes involved in the energy
savings due to grouping and huddling in free-ranging birds in their colony. We
estimated that a major part of energy savings for loosely grouped birds is due
to wind protection (32%). Furthermore, though overestimated, exposure to mild
ambient temperatures and reduction of cold-exposed body surfaces would
represent a 38% reduction in metabolic rate. The reduction in cold-exposed
body surfaces in huddling emperor penguins would account for about two thirds
of the energy savings due to huddling. This contradicts pioneering hypotheses
that attributed the major energy savings to the microclimate created within
the huddling groups (Prévost,
1961; Jouventin,
1971; Jarman,
1973; Le Maho,
1977). However, it corresponds to the lower range of the benefits
due to reduction in cold-exposed body surfaces in small mammals, representing
58–94% of huddling energy savings
(Canals et al., 1997).
Hence this review, as a first-step analysis, provides an explanation of the complex contributions of four processes towards the energetic benefits gained by huddling. This study should permit the design of an improved model of energy savings in huddling emperor penguins, these energetic benefits being the key for them to successfully assume their incubation in the midst of the Antarctic winter.
|
Acknowledgments |
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